key: cord-257641-wmbgpnr9 authors: katsarou, maria; grassi, viviana; lomazzi, chiara; domanin, maurizio; trimarchi, santi title: acute retrograde type a intramural hematoma during sars-cov-2 time date: 2020-10-15 journal: j vasc surg doi: 10.1016/j.jvs.2020.09.019 sha: doc_id: 257641 cord_uid: wmbgpnr9 nan mostly affecting the descending aorta. 1 type a imhs involve, type b imhs do not involve the 3 ascending aorta. retrograde type a imh (retro-taimh) origins in the descending aorta and 4 extend into the arch or ascending aorta. taimhs with distal ad carry an in-hospital mortality 5 risk of 12-26%. 1-2 6 we report the case of an 85-year-old woman with acute retro-taimh and distal ad. the 7 patient's consent for publication was obtained. she was admitted to the emergency room with 8 acute onset dyspnea, chest pain but no evidence of malperfusion. emergency computed 9 tomography angiography (cta) identified a retro-taimh with ad with proximal entry tear 10 above the celiac axis (a/cover). 11 the patient was hemodynamically stable. she was treated with hypotensive and analgesic 12 therapy and hospitalized for intensive monitoring. follow-up cta was performed at 24 hours 13 (b) and 7 days (c) showing progressive to complete thrombosis of the entry tear, with reduction 14 in aortic diameter which is the most important predictor of imh regression and positive 15 outcome. 3 complete symptom regression occurred. the event was observed during the sars-16 cov-2 pandemic peak in lombardy and the patient was found to be positive to the virus five 17 days after symptom onset, with progressive dyspnea and worsening findings on chest x rays (d). 18 she died due to pulmonary complications at 19 days. 19 hybrid treatment with ascending aortic replacement and distal thoracic aortic endovascular 20 repair (tevar), or with frozen elephant trunk is the most appropriate treatment for acute 21 retro-taimh. tevar is a valid alternative only in patients with prohibitive surgical risk, 22 although landing zones may be unsuitable and the risk of neurological and cardiac complications 23 may be high. 4 medical treatment appears to be appropriate in asymptomatic patients, in those 1 with non-complicated retro-taimh and in patients with high open surgical / tevar risks. 4 considering both the absence of end-organ malperfusion and the advanced age of the patient, we 3 chose medical treatment, that allows to reduce mortality by 67-95%. 5 this choice was proven 4 effective with symptom recovery and clinical stability, until the deadly overlap of the sars-5 cov-2. 6 j o u r n a l p r e -p r o o f the differences and similarities between intramural hematoma of the descending 6 aorta and acute type b dissection prognostic value of clinical and morphologic findings in short-10 term evolution of aortic intramural haematoma. therapeutic implications management of retrograde type a imh with acute arch tear/type b dissection diagnosis and management of patients with aortic dissection key: cord-031922-3pfxrhbc authors: petrie, john r title: sglt2 inhibitors and renal complications in type 1 diabetes date: 2020-09-15 journal: lancet diabetes endocrinol doi: 10.1016/s2213-8587(20)30311-9 sha: doc_id: 31922 cord_uid: 3pfxrhbc nan adding in non-insulin agents is one of several promising strategies under investigation to improve glycaemic control in type 1 diabetes. unlike uptitration of insulin, the ideal so-called adjunct drug would not cause increased hypoglycaemia and weight gain. 1 it would also reduce rates of cardiovascular, renal, and other adverse outcomes by improving glycaemic control or other mechanisms. these complications still result in an average reduction in life expectancy of 11-13 years among people with type 1 diabetes. 2 of several drug classes repurposed from type 2 to type 1 diabetes, sglt2 inhibitors have made the most progress. the concept behind these drugs is that inhibiting reabsorption of glucose (and sodium) in the proximal renal tubules reduces blood glucose only when it is above a reduced renal threshold, so hypoglycaemia is not increased, while weight is reduced due to urinary loss of glucose equivalent to approximately 200 kcal per day. because adverse cardiovascular events are reduced in patients with type 2 diabetes with these drugs (as has been found in the empareg, canvas, declare-timi trials), 3 the hypothesis that this might also happen in type 1 diabetes is not unreasonable. in this issue of the lancet diabetes & endocrinology, per-henrik groop and colleagues 4 report the effect of the sglt2 inhibitor dapagliflozin on albuminuria in adults with type 1 diabetes in a post-hoc subgroup analysis of the depict-1 and depict-2 phase 3 trials. 5 they report that in the 251 (15%) of 1646 participants with albuminuria at baseline, dapagliflozin reduced urinary albumin excretion (the urinary albumin to creatinine ratio [uacr]) compared with placebo with a mean change from baseline at 52 weeks of −13·3% (95% ci −37·2 to 19·8) for dapagliflozin 5 mg and −31·1% (−49·9 to −5·2) for dapagliflozin 10 mg. this finding is biologically plausible given compelling recent evidence that dapagliflozin and see articles page 845 in pregnancy have noted that some patients will still require insulin in the third trimester. 3 for future consideration, metformin clearance is increased in pregnancy, but the effects on dose selection or efficacy are unknown. metformin is excreted into the milk during lactation, and although caution is advised, no adverse effects have become evident. initial studies indicated that infants who were exposed to metformin in utero subsequently gained weight normally and generally achieve slightly above average growth, but more data on child development would be welcome. 7 other potential adjuncts to insulin treatment in pregnancy include sulfonylureas such as glibenclamide. this drug has been shown to improve maternal glycaemic control but crosses the placenta and stimulates fetal insulin secretion, with consequent macrosomia and risk of hypoglycaemia to the fetus and neonate. 8 no adequate clinical data exist regarding the use of dpp-4 inhibitors, glp-1 receptor agonists, or sglt2 inhibitors in pregnancy, but these medications are not recommended on the basis of preclinical studies that suggest possible adverse effects during the late stages of fetal development. in conclusion, mity 4 has provided prospective, controlled evidence to support the low-cost, potentially beneficial, metabolic effects of metformin with insulin in the management of pregnancy for type 2 diabetes and gestational diabetes, and substantiated a favourable safety profile for neonates. i report personal fees from abbott diabetes care, boehringer ingelheim, astrazeneca, lexicon-sanofi, merck, msd, napp, and novo, outside of the submitted work. other sglt2 inhibitors reduce rates of end-stage kidney disease in patients with chronic kidney disease, 6 whether or not associated with type 2 diabetes. mechanistically, sglt2 inhibitors are thought to protect the glomerulus by reflex constriction of the afferent arteriole in response to renal tubular sodium loss rather than by relaxation of the efferent arteriole as with renin-angiotensin system blocking drugs. despite the many beneficial effects of sglt2 inhibition in several conditions, including heart failure, their promotion of ketosis has been the major barrier to widespread uptake in type 1 diabetes, in which diabetic ketoacidosis still accounts for more than 20% of deaths. 7 this adverse effect is unlikely to be eliminated because many of the positive effects, particularly on heart failure outcomes, are thought to be mediated by increased availability of free fatty acids and ketone bodies for metabolism. nevertheless, of the sglt2 inhibitors that have entered phase 3 trials in type 1 diabetes, dapagliflozin (depict programme) and sotagliflozin (intandem programme) have relatively favourable therapeutic profiles. 7, 8 in pooled analyses of dapagliflozin, a dose of 5 mg per day on average reduced hba 1c by 0·34% versus placebo at 52 weeks in the context of a three times increase in adjudicated diabetic ketoacidosis risk versus placebo (4·62 events per 100 patient years in the dapagliflozin group vs 1·27 events per 100 patient years in the placebo group), decreasing substantially in those with a bmi of 27 kg/m² or higher (1·86 vs 1·17 per 100 patient years). 5 based on such therapeutic profiles, both dapagliflozin and sotagliflozin were granted a european (but not us) license for adjunct therapy in type 1 diabetes in the first half of 2019 for those with a bmi of 27 kg/m² or higher. the uk national institute for healthcare excellence (nice) subsequently recommended both drugs (dapagliflozin in august, 2019, and sotagliflozin in february, 2020) to be cost-effective for use within the uk national health service for individuals who additionally had a relatively high insulin requirement (≥0·5 units/kg per day) and had completed an evidence-based qualityassured structured education programme. notably, as of august, 2020, dapagliflozin is widely available but sotagliflozin has yet to be launched in many countries. nice estimated that around 90 000 of the estimated 370 000 adults with type 1 diabetes in the uk might be eligible for sglt2 inhibition. 9 however, more than 1 year on from approval, uptake has been much lower (petrie jr, unpublished) . although many diabetologists have cared for people with type 1 diabetes who have derived great benefit from dapagliflozin (usually in the context of regular blood ketone monitoring; petrie jr, unpublished), their enthusiasm has been tempered by small numbers of patients who have been admitted to hospital for severe treatment-resistant diabetic ketoacidosis attributed to sglt2 inhibitor therapy, in some cases presenting late due to relative euglycaemia. 10 the strength of this perception was reinforced during the early months of the covid-19 pandemic by guidance from the association of british clinical diabetologists that sglt2 inhibitors should be stopped in all people with diabetes (even those with type 2) who had been admitted to hospital. some uk centres and clinics went even further and proactively contacted stable patients with type 1 diabetes to advise discontinuation of the drug, even those who were able to skip doses on sick days as recommended. as sglt2 inhibitors are restarted now that the uk is coming out of the covid-19 lockdown, can re-introduction now be informed by the knowledge that renoprotection is an additional and previously unrecognised benefit of dapagliflozin? the analysis by groop and colleagues 4 has some limitations. because it was based on a non-prespecified surrogate measure in small numbers of individuals during relatively short-term follow-up, they could not report on clinical renal outcomes. the 26·8% (se 9·0) reduction in mean percentage change uacr from baseline to week 52 observed in those allocated to the placebo group indicated considerable regression to the mean. additionally, despite evidence suggesting dose-dependence of dapagliflozin, reduction in uacr with the recommended dose of dapagliflozin (5 mg per day) was not significant. this finding is in contrast with significant reduction in uacr with sotagliflozin (200 mg per day), but no significant reduction with the higher dose (400 mg per day). 8 despite these considerations, when taken in the context of evidence with sglt2 inhibition in other conditions and data for sotagliflozin, the dapagliflozin analysis by groop and colleagues contributes to proof of concept for renoprotection for this class of drug in type 1 diabetes and helps support the benefit rather than the for a press release from astrazeneca about dapagliflozin in people with and without diabetes see https://www.astrazeneca.com/ media-centre/pressreleases/2020/farxiga-phase-iiidapa-ckd-trial-will-be-stoppedearly-after-overwhelmingefficacy-in-patients-withchronic-kidney-disease.html for more on european license of dapagliflozin see https://www. astrazeneca.com/media-centre/ press-releases/2019/forxigaapproved-in-europe-for-type sglt2 inhibitors in type 1 diabetes: knocked down, but up again? estimated life expectancy in a scottish cohort with type 1 diabetes the effects of sglt2 inhibitors on cardiovascular and renal outcomes in diabetic patients: a systematic review and metaanalysis effect of dapagliflozin as an adjunct to insulin over 52 weeks in individuals with type 1 diabetes: post-hoc renal analysis of the depict randomised controlled trials benefit:risk profile of dapagliflozin 5 mg in the depict-1 and -2 trials in individuals with type 1 diabetes and bmi ≥27 kg/m² canagliflozin and renal outcomes in type 2 diabetes and nephropathy time trends in deaths before age 50 years in people with type 1 diabetes: a nationwide analysis from scotland sotagliflozin: a review in type 1 diabetes nice recommends innovative treatment for type 1 diabetes. national institute for health and care excellence optimising the benefits of sglt2 inhibitors for type 1 diabetes key: cord-030631-cc79j9j4 authors: marcus, benjamin a.; achenbach, peter; ziegler, anette-gabriele title: typ-1-diabetes: früherkennung und ansätze zur prävention: update 2020 date: 2020-08-19 journal: diabetologe doi: 10.1007/s11428-020-00668-x sha: doc_id: 30631 cord_uid: cc79j9j4 the incidence of type 1 diabetes is increasing, especially in young children. early diagnosis is possible in the asymptomatic stage of islet autoimmunity. screening is offered to high-risk families, but also feasible and useful in the general population, in studies such as fr1da(plus) in bavaria (germany). complications at clinical manifestation can be prevented by early diagnosis. participation in experimental interventions to delay stage progression is possible. numerous approaches to secondary prevention are being pursued. treatment with the monoclonal antibody teplizumab successfully delayed progression to clinical diabetes in patients in stage 2. infants at high risk for developing type 1 diabetes can be identified by genetic screening. primary prevention pursues, among others, the goal of preventing the onset of the autoimmune reaction. the point trial aims to improve immune tolerance to insulin by oral exposure in high-risk children and to delay or prevent the onset of autoimmunity. following up on the focus issue “early detection and preventive treatment of type 1 diabetes” published in this journal in 2018, this article gives an update on selected developments over the past 2 years. große prospektive geburtskohorten haben unser verständnis für die entstehung des typ-1-diabetes und den natürlichen verlauf dieser chronischen autoimmunerkrankung entscheidend vorangebracht, und tun dies ist auch weiterhin. wir kennen die genetischen faktoren, die das auftreten der erkrankung begünstigen. wir können einen typ-1-diabetes heute durch den nachweis von inselantikörpern diagnostizieren, lange bevor es zu veränderungen des glukosestoffwechsels oder gar zu symptomen kommt. in einer bahnbrechenden präventionsstudie konnten die klinische manifestation bereits um mehrere jahre hinausgezögert und die betazellfunktion stabilisiert werden, was auch die suche nach ei-ner kausalen therapie befruchten könnte. das immer bessere verständnis der komplexen vorgänge, die zur fehlleitung des immunsystems und zur fortschreitenden zerstörung von betazellen führen, eröffnet darüber hinaus verschiedene ansatzpunkte, das entstehen von autoimmunität zu verhindern und den prozess aufzuhalten. im themenheft dieser zeitschrift früherkennung und präventive behandlung des typ-1-diabetes -weichenstellungen für die zukunft [1] vom juni 2018 wurden diese bereiche bereits ausführlich dargestellt. in diesem beitrag sollen als update ausgewählte neue ergebnisse und entwicklungen der letzten 2 jahre vorgestellt werden. der nachweis von gegen unterschiedliche betazellantigene gerichteten autoantikörpern im blut ist der etablierte und derzeit wichtigste marker für den autoimmunprozess, der den typ-1-diabetes charakterisiert. es kommt zu einem untergang der insulinproduzierenden zellen der bauchspeicheldrüse durch autoreaktive t-zellen mit zunächst langsam, dann kurz vor der manifestation rasch abnehmender insulinproduktion. eine gestörte glukosetoleranz lässt sich erst feststellen, wenn bereits ein großteil der betazellen ihrer funktion nicht mehr nachkommen kann. die 4 wesentlichen autoantikörper sind insulinautoantikörper (iaa), glutamatdekarboxylaseautoantikörper (gada), antikörper ge-gen das insulinomassoziierte antigen 2 (ia-2a) und zinktransporter-8-autoantikörper (znt8a). autoantikörpern markiert das frühstadium des typ-1-diabetes der nachweis von 2 oder mehr dieser autoantikörper beim asymptomatischen kind ohne gestörten glukosestoffwechsel ist inzwischen als eines der frühstadien des typ-1-diabetes (stadium 1) anerkannt. beim stadium 2 liegen zudem mäßig erhöhte nüchternglukosewerte und/oder eine gestörte glukosetoleranz vor. der (neu) manifestierte typ-1-diabetes nach gültigen klinischen und laborchemischen kriterien ist das stadium 3 (. tab. 1). anhand in der covid-19-pandemie leistet die fr1da plus -studie einen über die typ-1-diabetes-früherkennung hinausgehenden beitrag zur epidemiologischen forschung. mit einem von italienischen wissenschaftlern entwickelten, nichtkommerziellen verfahren werden die kapillarblutproben auch auf igg-antikörper (igg: immunglobulin g) gegen die rezeptorbindungsdomäne des s-proteins von sars-cov-2 ("severe acute respiratory syndrome coronavirus 2") untersucht. der luciferaseimmunopräzipitationstest (lips) funktioniert nach einem ähnlichen prinzip wie der nachweis von iaa [19] . dabei wird auch auf anonymisierte fr1da-proben seit august 2019 zurückgegriffen. so kann die immunitätslage von kindern im stark betroffenen bayern vor und im gesamten verlauf der pandemie ermittelt werden [13] . the incidence of type 1 diabetes is increasing, especially in young children. early diagnosis is possible in the asymptomatic stage of islet autoimmunity. screening is offered to highrisk families, but also feasible and useful in the general population, in studies such as fr1da plus in bavaria (germany). complications at clinical manifestation can be prevented by early diagnosis. participation in experimental interventions to delay stage progression is possible. numerous approaches to secondary prevention are being pursued. treatment with the monoclonal antibody teplizumab successfully delayed progression to clinical diabetes in patients in stage 2. infants at high risk for developing type 1 diabetes can be identified by genetic screening. primary prevention pursues, among others, the goal of preventing the onset of the autoimmune reaction. the point trial aims to improve immune tolerance to insulin by oral exposure in high-risk children and to delay or prevent the onset of autoimmunity. following up on the focus issue "early detection and preventive treatment of type 1 diabetes" published in this journal in 2018, this article gives an update on selected developments over the past 2 years. um zu prüfen, ob teplizumab die klinische manifestation verhindern kann, wurden in einer trialnet-studie angehörige von personen mit typ-1-diabetes behandelt, die selbst bereits ein frühstadium mit multiplen inselautoantikörpern und eine dysglykämie oder gestörte glukosetoleranz (stadium 2) entwickelt hatten. die ergebnisse dieser untersuchung, die für mehr als die hälfte der behandelten eine verdoppelung der zeit bis zur klinischen erkrankung auf 4 jahre ergaben, wurden im new england journal of medicine (nejm) publiziert [14] . somit konnte erstmals die manifestation der erkrankung wirksam hinausgezögert werden, was einen durchbruch für die präventive therapie des typ-1-diabetes darstellt. in die doppelblinde, randomisierte und plazebokontrollierte phase-2-studie wurden 76 verwandte von patienten mit typ-1-diabetes, 2 oder mehr autoantikörpern und dysglykämie eingeschlossen, mehrheitlich kinder ab 8 jahren und jugendliche. sie erhielten 2 wochen lang 1-mal täglich infusionen mit teplizumab oder kochsalz. im followup erfolgten mindestens halbjährlich glukosetoleranztests, die nachbeobachtungszeit betrug im median etwas über 2 jahre, 75 % der probanden konnten über mehr als 3 jahre nachverfolgt werden. bei 19 (43%) der 44 mit teplizumab behandelten teilnehmenden und 23 (72 %) von 32 in der plazebogruppe wurde ein klinischer typ-1-diabetes diagnostiziert. im ersten jahr nach der behandlung war der effekt besonders ausgeprägt: hier manifestierte sich die erkrankung nur bei 3 (7 %) teilneh-mern in der teplizumab-vs. 14 (44 %) in der plazebogruppe. jährlich erkrankten 14,9 % auf den diesjährigen "scientific sessions" der "american diabetes association" (ada) wurden daten aus dem erweiterten follow-up der studie vorgestellt -und bei der medianen hinauszögerung noch ein weiteres, 3., jahr hinzugefügt. zudem war teplizumab in der lage, den c-peptid-abfall nach manifestation nicht nur zu bremsen, sondern signifikant umzukehren. dies könnte bedeuten, dass nicht nur die zerstörung der betazellen gestoppt, sondern auch die insulinproduktion in dysfunktionalen zellen teilweise wiederhergestellt wurde [26] . auch wenn derzeit noch "nur" davon ausgegangen werden sollte, dass sich für die behandelten patienten der beginn der erkrankung weiter in die zukunft verschiebt und der effekt bei einer dauerhaft therapiebedürftigen erkrankung moderat erscheinen mag, wirkt sich gerade bei kindern jedes gewonnene klinisch gesunde jahr noch weit mehr aus als im erwachsenenalter. für eine individualisierte sekundärprävention interessant wird die tatsache, dass anhand von biomarkern -hla-merkmalen (hla: humanes leukozytenantigen) und dem fehlen von znt8a -abgeschätzt werden kann, bei welchen patienten ein ansprechen auf die anti-cd3-behandlung bessere erfolgschancen hat [28] . inzwischen wurden mehr als 60 genloci identifiziert, die in unterschiedlichem ausmaß für das entstehen eines typ-1-diabetes prädisponieren. die meisten davon sind mit der immunantwort so-wie der entwicklung und dem erhalt von toleranz gegenüber antigenen assoziiert [4] . die genetische empfänglichkeitalleinführtaberwahrscheinlichnicht zum entstehen der inselautoimmunität. es wird angenommen, dass umweltfaktoren, die auf eine genetische prädisposition treffen, entscheidend mit zur initiierung des autoimmunprozesses beitragen. dabei liegt es nahe, dass dem frühen säuglingsalter, in dem dieser prozess noch nicht in gang gekommen ist, eine besondere bedeutung zukommt [23] . nichtpharmakologische interventionen zielen auf die zusammensetzung der ernährung und ggf. gezielte supplementationen ab, auch das darmmikrobiom rückt immer mehr in den fokus [33] . in der interventionellen präventionsstudie babydiet wurde gezeigt , dass -obwohl die zu frühe einführung von gluten mit der beikost, vor dem 3. lebensmonat, mit einem höheren risiko einhergeht -eine darüber hinausgehende glutenfreie ernährung das entstehen der inselautoimmunität nicht verhindert. auch durch elimination anderer potenziell antigener proteine durch die verwendung stark hydrolysierter säuglingsmilch konnte in der prospektiven trigr-studie die diabetesinzidenz nicht gesenkt werden [16, 18] . es lassen sich weiterhin keine über die allgemeingültigen empfehlungen zu einer gesunden säuglingsernährung hinausgehenden ernährungsmaßnahmen zur senkung des typ-1-diabetes-risikos ableiten. die identifikation von neugeborenen und säuglingen mit einem hohen genetischen typ-1-diabetes-risiko ist heute einfach und kostengünstig möglich, sodass sie auch in bevölkerungsweiten studien angeboten werden kann. die "global platform for the prevention of autoimmune diabetes" (gppad), ein netzwerk kooperierender wissenschaftler und institutionen [37] , führt dies seit 2017 regional in 5 europäischen ländern durch. in deutschland wird das virusinfekte werden mit dem typ-1-diabetes in verbindung gebracht, insbesondere virale atemwegsinfekte in der frühen kindheit und infektionen mit enteroviren und durchfallerregern. hier könnten zukünftig entsprechende impfungen, z. b. gegen coxsackie-viren [31] , oder antivirale therapien zur senkung des erkrankungsrisikos beitragen [10] . dervorfast15 jahreneingeführten rotavirenimpfung wird ein kürzlich festgestellter geringer rückgang der diabetesinzidenz bei vollständig geimpften kindern zugeschrieben. hinweise hierzu lieferten retrospektive auswertungen aus australien und den usa [24, 27] , wobei die ergebnisse einer weiteren amerikanischen analyse dies zuletzt wieder in frage stellten [11] . zumindest lässt sich sicher sagen, dass auch die rotavirenimpfungso wie alle anderen empfohlenen schutzimpfungen -sich keinesfalls negativ auf das typ-1-diabetes-risiko auswirkt. die erstmalige, wirksame verzögerung der manifestation mit teplizumab allein ist schon bemerkenswert [32] , die mögliche reaktivierung zuvor nicht sezernierender betazellen könnte auch die entwicklung kausaler therapien mit vorantreiben. in größeren studien mit mehreren behandlungszyklen und in der weite-ren langfristigen nachbeobachtung der studienpatienten wird das potenzial der substanz weiter untersucht werden. die kombination mit anderen, schon im frühen stadium 3 in klinischen studien eingesetzten, vielversprechenden und verträglichen immunmodulatoren wie z. b. abatacept oder niedrig dosiertem antithymozytenglobulin, die an anderen stellen der pathogenese des typ-1-diabetes angreifen [5, 9] , sowie mit weiteren aufkommenden betazellregenerativen therapien wird bereits geplant. studien zur früherkennung stoßen bei eltern auf zuspruch, und auch familien, die bisher nicht von typ-1-diabetes betroffen waren, sind am angebot primärer und sekundärer präventionsstudien sehr interessiert. die möglichkeit, komplikationen bei der manifestation zu verhindern und erste erfolge in der medikamentösen sekundärprävention werden die schon länger geführte debatte um eine verstetigung und ausweitung von typ-1-diabetes-früherkennungsuntersuchungen, z. b. als zusätzliches angebot bei den gesetzlichen vorsorgeuntersuchungen, sicher befruchten [22] . früherkennung und präventive behandlung des typ-1-diabetes typ-1-diabetes im asymptomatischen frühstadium classification and diagnosis of diabetes: standards of medical care in diabetes-2020 type 1 diabetes the challenge of modulating β-cell autoimmunity in type 1 diabetes type 1 diabetes trialnet: a multifaceted approach to bringing disease-modifying therapy to clinical use in type 1 diabetes predicting type 1 diabetes using biomarkers birth and coming of age of islet autoantibodies a future for cd3 antibodies in immunotherapy of type 1 diabetes rationale for enteroviral vaccination and antiviral therapies in human type 1 diabetes association betweenrotavirusvaccinationandtype1diabetes in children teplizumab preserves c-peptide in recent-onset type 1 diabetes: two-year results from the randomized, placebo-controlled protégé trial etablierte früherkennungsstudie zu typ-1-diabetes testet nun tausende kinder auch auf antikörper gegen sars-cov-2 an anti-cd3 antibody, teplizumab, in relatives at risk for type 1 diabetes landmark models to define the age-adjusted risk of developing stage 1 type 1 diabetes across childhood and adolescence prevention strategies for type 1 diabetes: a story of promising efforts and unmet expectations recruiting young pre-symptomatic children for a clinical trial in type 1 diabetes: insights from the fr1da insulin intervention study effect of hydrolyzed infant formula vs conventional formula on risk of type 1 diabetes: the trigr randomized clinical trial ketoacidosis at onset of type 1 diabetes in children up to 14 years of age and the changes over a period of 18 years in saxony, eastern-germany: a population based register study immunological biomarkers for the development and progression of type 1 diabetes screening for type 1 diabetes: are we nearly there yet? type 1 diabetes-early life origins and changing epidemiology association of rotavirus vaccination with the incidence of type 1 diabetes in children treatment of type 1 diabetes with teplizumab: clinical and immunological followup after 7 years from diagnosis provention bio's teplizumab continued to significantly delay the onset of insulin-dependenttype1diabetes(t1d)inpresymptomatic patients lower incidence rate of type 1 diabetes after receipt of the rotavirus vaccine in the united states traveling down the long road to type 1 diabetes mellitus prevention who is enrolling? the path to monitoring in type 1 diabetestrialnet'spathwaytoprevention continuous glucose monitoring predicts progression to diabetes in autoantibody positive children a hexavalent coxsackievirus b vaccine is highly immunogenic and has a strong protective capacity in mice and nonhuman primates delaying diabetes onset the human gut microbiome in early-onset type 1 diabetes from the teddy study früherkennung des typ-1-diabetes in der fr1da-studie identification of infants with increased type 1 diabetes genetic risk for enrollment into primary prevention trials-gppad-02 study design and first results why is the presence of autoantibodies against gad associated with a relatively slow progression to clinical diabetes? oral insulin therapy for primary prevention of type 1 diabetes in infants with high genetic risk: the gppad-point (global platform for the prevention of autoimmune diabetes primary oral insulin trial) study protocol yield of a public health screening of children for islet autoantibodies in bavaria key: cord-028840-7n77vko9 authors: chardonnet, kostia; saurin, alexis; valiron, benoît title: toward a curry-howard equivalence for linear, reversible computation: work-in-progress date: 2020-06-17 journal: reversible computation doi: 10.1007/978-3-030-52482-1_8 sha: doc_id: 28840 cord_uid: 7n77vko9 in this paper, we present a linear and reversible language with inductive and coinductive types, together with a curry-howard correspondence with the logic [image: see text] : linear logic extended with least and greatest fixed points allowing inductive and coinductive statements. linear, reversible computation makes an important sub-class of quantum computation without measurement. in the latter, the notion of purely quantum recursive type is not yet well understood. moreover, models for reasoning about quantum algorithms only provide complex types for classical datatypes: there are usually no types for purely quantum objects beside tensors of quantum bits. this work is a first step towards understanding purely quantum recursive types. computation and logic are two faces of the same coin. for instance, consider a fig. 1 features a graphical presentation of the corresponding proof. horizontal lines stand for deduction steps-they separate conclusions (below) and hypotheses (above). these deduction steps can be stacked vertically up to axioms in order to describe complete proofs. in fig. 1 the proofs of a and a → b are symbolized with vertical ellipses. the ellipsis annotated with s indicates that s is a complete proof of a → b while t stands for a complete proof of a. this connection is known as the curry-howard correspondence [4, 8] . in this general framework, types correspond to formulas and programs to proofs, while program evaluation is mirrored with proof simplification (the so-called cutelimination). the curry-howard correspondence formalizes the fact that the proof s of a → b can be regarded as a function-parametrized by an argument of type a-that produces a proof of b whenever it is fed with a proof of a. therefore, the computational interpretation of modus-ponens corresponds to the application of an argument (i.e. t) of type a to a function (i.e. s) of type a → b. when computing the corresponding program, one substitutes the parameter of the function with t and get a result of type b. on the logical side, this corresponds to substituting every axiom introducing a in the proof s with the full proof t of a. this yields a direct proof of b without any invocation of the "lemma" a → b. paving the way toward the verification of critical softwares, the curry-howard correspondence provides a versatile framework. it has been used to mirror first and second-order logics with dependent-type systems [3, 10] , separation logics with memory-aware type systems [9, 13] , resource-sensitive logics with differential privacy [6] , logics with monads with reasoning on side-effects [11, 17] , etc. this paper is concerned with the case of reversible computation, a sub-class of pure quantum computation. in general quantum computation, one has access to a co-processor holding a "quantum" memory. this memory consists of "quantum" bits having a peculiar property: their state cannot be duplicated, and the operations one can perform on them are unitary, reversible operations. the co-processor comes with an interface to which one can send instructions to allocate, update or read quantum registers. quantum memories can be used to solve classical problems faster than with purely conventional means. quantum programming languages are nowadays pervasive [5] and several formal approaches based on logical systems have been proposed to relate to this model of computation [12, 14, 16] . however, all of these languages rely on a purely classical controlflow: quantum computation is reduced to describing a list of instructions-a quantum circuit-to be sent to the co-processor. in particular, in this model operations performed on the quantum memory only act on quantum bits and tensors thereof, while the classical computer enjoys the manipulation of any kind of data with the help of rich type systems. this extended abstract aims at proposing a type system featuring inductive and coinductive types for a purely reversible language, first step towards a rich quantum type system. we base our study on the approach presented in [15] . in this model, reversible computation is restricted to two main types: the tensor, written a ⊗ b and the co-product, written a ⊕ b. the former corresponds to the type of all pairs of elements of type a and elements of type b, while the latter represents the disjoint union of all elements of type a and elements of type b. for instance, a bit can be typed with 1 ⊕ 1, where 1 is a type with only one element. the language in [15] offers the possibility to code isos-reversible maps-with pattern matching. an iso is for instance the swap operation, typed with a ⊗ b ↔ b ⊗ a. the language also permits higher-order operations on isos, so that an iso can be parametrized by another iso, and is extended with lists ). however, if [15] hints at an extension toward pure quantum computation, the type system is not formally connected to any logical system. the main contribution of this work is a curry-howard correspondence for a purely reversible typed language in the style of [15] . we capitalize on the logic [1, 2] : an extension of the additive and multiplicative fragment of linear logic with least and greatest fixed points allowing inductive and coinductive statements. this logic contains both a tensor and a co-product, and its strict linearity makes it a good fit for a reversible type system. the logic [1, 2] is an extension of the additive and multiplicative fragment of linear logic [7] . the syntax of linear logic is extended with the formulas μx.a and its dual νx.a (where x is a type variable occuring in a), which can be understood at the least and greatest fixed points of the operator x → a. these permit inductive and coinductive statements. we are only interested in a fragment of which contains the tensor, the plus, the unit and the μ and ν connectives. note that our system only deals with closed formulas. our syntax of formulas is a, b :: the derivation rules are shown in fig. 2 . they defined a binary relation δ γ on set of formulas defined inductively. for each rule the assumptions are above the line while the conclusion is under. in the rules, the comma stands for the disjoint union: observe that each formula has to be used exactly once and cannot be duplicated or erased. in one can for instance define the type of natural numbers as μx.1 ⊕ x, of lists of type a as μx.1 ⊕ (a ⊗ x) and of streams of type a as νx.a ⊗ x. we consider proofs to be potentially non-well-founded derivation trees: they are not necessarily finite as we can for instance consider the formula μx.x and apply the rule μ r an infinite number of times. among non well-founded proof-objects we distinguish the regular derivation trees that we call circular pre-proofs. these trees can then be represented in a compact manner, see fig. 3 . one problem with such a proof-system is to determine whether or not infinite derivations are indeed proofs. indeed, if every infinite derivation is accepted as a proof, it would be possible to prove any formula f, as shown in fig. 4 . to answer this problem, comes with a validity criterion for derivations. it roughly says that a derivation is valid if, in every infinite branch of the derivation, there exists an infinite number of rules μ l or an infinite number of rules ν r . the intuition is that since μx.a formulas represent least fixed points, their objects are finite. an infinite number of rule μ r would mean producing an infinite object, which is not possible. on the other hand, we can explore an arbitrarily large object as input with the rule μ l . for the other case, since νx.a formulas represent greatest fixed points, their object are infinite. we therefore want to ensure that we can produce infinite objects: hence the infinite number of rules ν r . this criterion can be understood in a more operational way as a requirement for productivity. our language is based on the one presented in [15] . we build on the reversible part of the paper by extending the language to support both a more general rewriting system and inductive and coinductive types. the language is defined by layers. terms and types are presented in table 1 , while typing derivations, based on ,can be found in tables 2 and 3 . the language consists of the following pieces. basic type. they are first-order and typed with base types. the constructors inj l and inj r represent the choice between either the left or right-hand side of a type of the form a ⊕ b; the constructor , builds pairs of elements (with the corresponding type constructor ⊗); fold and pack respectively represent inductive and coinductive structure for the types μx.a and νx.a. a value can serve both as a result and as a pattern in the clause of an iso. generalized patterns are used as special patterns: v g : a can match any value of type a. terms are expressions at "surface-level": applying an iso always gives a term, whereas it is an expression only when the argument is a generalized pattern. first-order isos. an iso of type α acts on terms of base types. an iso is a function of type a ↔ b, defined as a set of clauses of the form the tokens e i and e i in the clauses are expressions. compared to the original language in [15] , we allow general expressions both on the left and on the right of a clause. in order to apply an iso to a term, the iso must be of type a ↔ b and the term of type a. in the typing rules of isos, the od predicate (taken from [15] and not described in this paper) syntactically enforces the exhaustivity and non-overlapping conditions that the left-hand-side and right-hand-side of clauses should satisfy. exhaustivity for an iso {e 1 ↔ e 1 | . . . | e n ↔ e n } of type a ↔ b means that the expressions on the left (resp. on the right) of the clauses describe all possible values for the type a (resp. the type b). non-overlapping means that two expressions cannot match the same value. for instance, the left and right injections inj l e and inj r e are non-overlapping while a pattern v g is always exhaustive. higher-order isos. an iso of type t manipulate other isos as basic blocks. since isos represent closed computations, iso-variable are non-linear and can be duplicated at will while term-variable are linear. the constructions λf.ω and ω 1 ω 2 represent respectively the abstraction of a function and the application of an iso to another. the construction μg.ω represents the creation of a recursive function, rewritten as ω[g := μg.ω] by the operational semantics. the typing rule for μg.ω has a productivity criterion. indeed, since isos can be non-terminating (because of coinduction), productivity is important to ensure that we work with total functions. these checks are crucial to make sure that our isos are indeed bijections in the mathematical sense. the construction inv ω corresponds to the inversion of the iso ω. if ω is of type a ↔ b then inv ω is of type b ↔ a. finally, our language is equipped with a rewrite system (→) on terms. the evaluation of an iso applied to an argument works with pattern-matching. the non-overlapping and exhaustivity conditions guarantee subject-reduction (see proposition 3.1). we can define the iso of type : remark 3.1. in our two examples, the left and right-hand side of the ↔ on each function respect both the criteria of exhaustivity-every-value of each type is being covered by at least one expression-and non-overlapping-no two expressions cover the same value. both isos are therefore bijections. t : a and t → t then we have t : a. moreover, it enjoys confluence: let → * be the reflexive, transitive closure of →. if t → * t 1 and t → * t 2 then there exists t 3 such that t 1 → * t 3 and t 2 → * t 3 . we conjecture that well-typed isos are indeed isomorphisms: an iso ω : a ↔ b corresponds to both a computation sending a value of type a to a result of type b and a computation sending a value of type b to a result of type a. we can mechanically translate such an iso to a pair of derivations π, π ⊥ in , where π is a proof of a b and π ⊥ is a proof of b a. this mechanical translation constructs circular pre-proofs, as discussed in sect. 2. we however still need to show that the obtained derivations respect the validity criterion for circular proof. once proven, we would obtain a static correspondence between programs and proofs. we would however still need to show that this entails a dynamic correspondence between the evaluation procedure of our language and the cutelimination procedure of . for that, we would need to make sure that the proofs we obtain are indeed isomorphisms, meaning that if we cut the aforementioned proofs π and π ⊥ , performing the cut-elimination procedure would give either the identity on a or the identity on b. isomorphism of proofs. provided that the above holds, we moreover have simulation of evaluation. provided that t is a value and v is a normal form, if ω t → * v, if π is the proof corresponding to ω t, and if π is the proof corresponding to v, then π → * π with the cut-elimination procedure. we define the two mutually recursive proofs π 1 and π 2 by π 1 = π(ψ f , π 2 ) and π 2 = π(ψ f ⊥ , π 1 ) where ψ f and ψ f ⊥ correspond to the isos f and inv f . the proof associated with the iso in eq. (1) is π 1 . the proof π(φ 1 , φ 2 ) is shown in fig. 5 . we presented a higher-order, linear, reversible language with inductive and coinductive types together with an interpretation of programs into derivations in the logic . this work is still in progress: a number of proofs still need to be completed. after completing the proofs of our current conjectures, we want to extend our language to linear combinations of terms in order to study purely quantum recursive types and generalized quantum loops: in [15] , lists are the only recursive type which is captured and recursion is terminating. the logic would help providing a finer understanding of termination and non-termination. infinitary proof theory: the multiplicative additive case least and greatest fixed points in linear logic interactive theorem proving and program development -coq'art functionality in combinatory logic open source software in quantum computing linear dependent types for differential privacy linear logic the formulae-as-types notion of construction rustbelt: securing the foundations of the rust programming language formal verification of a realistic compiler the next 700 relational program logics. pacmpl 4(popl) qwire: a core language for quantum circuits separation logic: a logic for shared mutable data structures a categorical model for a quantum circuit description language from symmetric pattern-matching to quantum control a lambda calculus for quantum computation with classical control dependent types and multi-monadic effects in f key: cord-008700-knbf8m4x authors: rodrigues, merlyn r.; lennette, david a.; arentsen, juan j.; thompson, charla title: methods for rapid detection of human ocular viral infections date: 2013-10-30 journal: ophthalmology doi: 10.1016/s0161-6420(79)35507-5 sha: doc_id: 8700 cord_uid: knbf8m4x recent methods for detection of viruses in clinical specimens include immunofluorescence, immunoperoxidase, immune adherence hemagglutination, radioimmunoassay, enzyme-linked immunosorbent assay (elisa), and immunoelectron microscopy. some are useful for the detection of traces of viral antigens but are more complicated and timeconsuming than others. simple techniques of immunofluorescence and negative stain electron microscopy are used for the rapid detection of viruses in human adenoviral, herpetic, rubella, molluscum contagiosum, and vaccinial infections. in 1977, 50 conjunctival specimens obtained from patients with epidemic keratoconjunctivitis (ekc) were examined by direct immunofluorescence. the specimens were conjunctival swabs or scrapings from patients with acute follicular keratoconjunctivitis. adenovirus groupantigen specific, fluorescein conjugated rabbit antiserum was used. titration of this conjugate, dilated in 10% mouse brain suspension in pbs ph 7.5, gave an optimum dilution for use of 1:20. at this dilution, antigen-positive cells stained brilliantly (4+), while antigen-negative cells were only faintly stained but were readily discernible (1 + or less). conjunctival scrapings were prepared on clean microscope slides and air dried as rapidly as was feasible-preferably on the returnair intake grill of a laminar-flow biologic safety cabinet. following thorough air drying, the. slides were 452 volume r6 march 1979 ocular viral infections 453 acetone fixed at room temperature for ten minutes. the slides with the conjugate diluted in brain suspension were incubated for 30 minutes at 37c in a moist chamber, followed by a ten-minute wash in pbs ph 7.4 with intermittent agitation. the slides were examined at a magnification of x200, using standard exciter/barrier filter combinations for fluorescein with 200 w hgarc illumination. scrapings were scored as positive if any cells of normal morphology were observed with typical granular cytoplasmic fluorescence. scrapings were read as negative if no such cells were found and as inconclusive if only atypical fluorescence and fewer than 50 cells were noted. controls.-fl uorescein -ia be led preserum from the animals used to produce the antibodies became commercially available only after the study was completed. before the study was conducted on clinical specimens, the working titer of the conjugates was established at varying dilutions by staining uninfected cells, homologous-infected cells, and heterologous-infected cells. at a working dilution that produced brightto-brilliant fluorescence with the homologous agents, there was negligible background fluorescence with either uninfected or heterologousinfected (herpes simplex virus 1 [hsv-1], herpes simplex virus 2, and herpes zoster with adenovirus) cells. the conjugates were stored at -soc after reconstitution, and only small amounts of working dilutions were prepared to avoid repeated freezing and thawing. the clinical specimens were examined with absorbed-conjugate con-trois that were retested approximately monthly with uninfected, homologous-infected, and heterolologous-infected cell cultures. during the study, conjugated normal rabbit serum was used as a control conjugate at the same dilution as the virus-specific conjugates. the intention was to determine whether accurate results could be obtained by immunofluorescence without multiple controls. cell culture isolation.-specimens of conjunctival scrapings for viral isolation were collected in 2-ml quantities of hank's balanced salt solution, with 0.5% gelatin added previously, dispensed and sterilized in 1-gm vials. the specimens were refrigerated until delivered to the virology laboratory, usually within 24 hours. they were treated by adding antibiotics (amphotericin b and psnb, a standard mixture of penicillin, streptomycin, neomycin, and bacitracin), then inoculated in 0.2 ml volumes into two tubes each of human embryonic lung or kidney fibroblast cells and primary rhesus monkey kidney cells. primary human embryonic kidney cells were used when available, as were hela 299 cells. cell cultures were held for a minimum of one month; any cultures that showed nonspecific degeneration earlier were passed to fresh cells of the same type. no further ''blind" passages were made. if typical adenovirus cytopathic effects were observed, the cells were held until the effects were estimated to involve well over half of the cell sheet, then harvested for titration and neutralization by the intersecting serum pool scheme. final serotyping was confirmed using monotypic antisera at a dilution providing approximately 20 antibody units against 100 to 300 tcidso. adequate smears and 'scrapings from patients with dendritic corneal lesions were fixed in acetone for ten minutes at room temperature, air dried, inoculated with a 1:20 dilution of conjugate in brain suspension for 30 minutes at 37c, and washed for ten minutes in pbs ph 7.2. with fluorescence micros--copy of the slides it was usually possible to differentiate type 1 and type 2 herpes simplex viruses if type-specific conjugates were used. lens aspirate from a 2-year-old patient with clinical ocular rubella was examined by immunofluorescence and negative stain electron microscopy. indirect immunofluorescence was performed with two human sera, pretested by a standard rubella hemagglutination-inhibition antibody (hal) test. the positive serum had a titer of 1:640, and the negative serum, a titer of less than 1:10, by hal these sera were then used in an indirect immunofluorescence test on rubella-infected and uninfected bhk-cells, a susceptible line used for laboratory propagation of rubella virus. titration of the positive serum revealed a working titer of 1:40; working titer is defined as a dilution that gives brilliant (4+) fluorescence of infected bhk-21 cells and minimal (±) fluorescence of noninfected cells. the conjugate used was a 1:25 antihuman igg rabbit serum. the lens smears were fixed in acetone for ten minutes at room temperature, ringed with fast-drying enamel and overlaid with positive and negative sera, incubated for 30 minutes at 37c, washed in pbs ph 7.4 (also used to dilute the serum), stained with the antihuman igg for 30 minutes at 30c, washed, mounted in polyvinyl alcohol ph 7.5, and examined with ultraviolet illumination at x200. the conjunctival and corneal scrapings were fixed in 2.5% buffered glutaraldehyde. the suspension was placed in drops in formvar-coated grids that were then stained for approximately 30 seconds in 3% phosphotungstic acid at ph 6.5. the specimens were examined by electron microscopy. the patients had conjunctival hyperemia and folliculosis (fig 1) . early subepithelial corneal infiltrates were present in 60% of the patients, preauricular nodes were present in 80%, and conjunctival pseudomembranes were present in approximately 10%. of 50 specimens from patients with ekc, positive immunofluorescence for adenovirus was present in 22 cases. cytoplasmic fluorescence was marked (fig 2) , but stippled nuclear fluorescence was also observed (fig 3) . cultures and typing showed that 20 of these were a hybrid type 10-19, one was type 3, and one was type 11. in three persons with herpetic dendritic keratitis (fig 4 and 5) , positive immunofluorescence was present (fig 6) ; all were herpes simplex hominis type 1. herpes simplex virions obtained from scrapings of dendritis lesions measured 100 nm in diameter and displayed mostly intact capsids (fig 7) . a 2-year-old boy with ocular rubella had unilateral cataract (fig 8) and microphthalmos. smears of the cataractous lens revealed positive immunofluorescence with the positive serum in the form of diffuse and granular cytoplasmic fluorescence, and diffuse streaks of amorphous extracellular material. molluscum contagiosum lid lesions displayed circumscribed nodules with a central umbilication (fig 9) . scrapings stained with hematoxylin-eosin revealed large basophilic cytoplasmic inclusions in the granular layer. n~gative stain electron microscopy disclosed brick-shaped virions (fig 10) measuring 250x200 nm with the usual interlacing pattern of surface threads. in one patient with a vaccinia lid lesion (fig 11) , both mulberry (m) and capsule (c) forms were observed (fig 12 and 13 ). recent advances in electron microsaopy as well as immunologic techniques have facilitated the rapid detection of viruses in clinical specimens. a hapten-sandwich procedure was reported for immunospecific labeling of cell surface antigens with markers visible by scanning electron microscopy (sem). 1 antihapten antibody was used to link hapten-modified tobacco mosaic virus and bushy stunt virus. viral identification by sem of preparations stained with fluorescein-labeled antibody was described by springer et al, 2 using hemagglutination of chicken erythrocytes by influenza virus as a model. transmission electron microscopy has been widely used for the study of viral structure and morphogenesis, although the low concentration of viral particles in some clinical used for the preparation of highly concentrated suspensions of mosaic viruses and human adenovirus type 5. the advantage of this technique over conventional negative staining is the formation of two-dimen-sional and three-dimensional crystalline arrays of viruses. the packing arrangement of the viruses could be varied according to the type of negative stain and ph used during the preparation. doane et al 6 described a two-hour embedding procedure for intracellular detection of viruses in tissue culture as well as tissue biopsy specimens. the total processing time by this method required two hours compared with an average of 24 to 32 hours by the standard method. however, there was slight decrease of specimen detail with less than optimal staining compared with the standard techniques. doane 4 reported that identification of viris by immunoelectron microscopy was useful for the study of viral antigens and antibodies. he was able to identify elusive viruses including rubella, hepatitis-associated antigens, rhinovirus, and coronavuus. gardner and mcquillin 7 have described the value of immunofluorescence in the diagnosis of rubella, adenoviral infections, and measles. immunofluorescence of human viral infections, particularly herpes simplex, has been reported. s the most common causes of viral keratoconjunctivitis are herpes simplex, adenovirus, and chlamydia. the most frequent types of adenoviruses encountered in ocular infections are types 8 and 19; types 3 (pharyngoconjunctival fever), 7, and 10 are sporadically seen. viral isolations occur during ekc outbreaks, usually in the spring and fall in the united states. clinically, adenovirus ekc is characterized by the acute "onset of a follicular conjunc-tivitis, hyperemia, photophobia, and lacrimation. diffuse epithelial keratitis followed by subepithelial infiltrates are a frequent finding. all of these features were present in the cases · studied. however, the clinical manifestations of the patients with hybrid type 10-19 infection resembled ekc caused by other types of adenoviruses. there was no evidence of systemic involvement. outbreaks of ekc frequently occur in schools, swimming pools, outpatient departments, and hospitals. the epidemics occur from contamination of eye solutions, instruments, and from infected fingers of doctors and nurses. 9 • 10 three of the patients in this study were ophthalmologists who had acquired the infection from examining patients with adenoviral infections. simultaneous nosocomial and community outbreaks of ekc with types 8 and 19 adenovirus were recently described. 10 in a recent epidemic of ekc at a vietnamese refugee camp in florida, adenovirus type 8 was recovered in 81% of cases cultured within two weeks of onset of infection.u dawson et ap 2 described adenovirus-like particles in the conjunctiva of one patient and in the corneal epithelium of another by transmission electron microscopy of tissue culture preparations. they found that among 15 patients with ekc caused by adenovirus type 8, 2 had persistent corneal erosions during the acute stage of the disease, 7 had conjunctival scarring, and 9 had inflammatory membranes. an outbreak of adenovirus type 19 in the united states was described by hierholzer and associates 13 and by burns and potter. 14 an epidemic of ekc caused by adenovirus type 19 occurred in london. 15 in this study, volume rfi adenovirus type 19 was isolated from 21 patients using human embryonic kidney cells. another re-port16 described difficulties encountered in typing adenovirus related to types 10 to 19 in an outbreak of keratoconjunctivitis in bristol. the same problem was encountered in this study, since the hybrid type [10] [11] [12] [13] [14] [15] [16] [17] [18] [19] showed characteristics of type 10 determined by neutralization and of type 19 by hemagglutination inhibition. in 1969, ellison and associates 17 compared methods available at that time for the laboratory diagnosis of ocular adenovirus type 3 infections. they used fluorescent antibody staining, examination of conjunctival cytology by the giemsa and papanicolaou stains, and standard virus isolations and antibody titers. they believed that virus culture was the most reliable way to identify adenoviral infections, since attempts at more rapid techniques using fluorescence antibody methods were unsuccessful. more recently, however, vastine and asso-ciates18 used a direct immunofluorescence technique for the diagnosis of acute adenoviral keratoconjunctivitis with positive results in 25 patients with epidemic keratoconjunctivitis. in an earlier report, schwartz et ap 9 described positive immunofluorescence studies in all 39 patients with adenoviral isolation. the fluorescence staining was predominantly present in the cytoplasm, but speckled nuclear fluorescence was also noted. in the present study, positive results with immunofluorescence and cultures were obtained in patients examined within the first week of infection, negative results were found in persons with advanced or chronic disease. thus, fluorescent antibody staining provides a more rapid and sensitive method for the detection of adenoviruses in infected conjunctival cells than viral culture, which usually requires one to eight weeks for virus identification. the direct immunofluorescent method is more rapid (requiring less than one hour) than the indirect technique, which takes a few hours to perform. adequate controls are essential for the reliability of immunofluorescence and should be easier with the new commercial preserum conjugates. frenkel and piekarski2° emphasized the problems in the diagnosis of toxoplasma organisms and others by immunofluorescence with appropriate positive and negative controls. the present study showed a good relation of viral isolates to positive immunofluorescence; the latter was confirmed by culture. adenovirus virions were also noted in conjunctival scrapings by negative stain electron microscopy. kajima and associates 21 were unable to demonstrate adenovirus by this method, although the organisms were demonstrated by conventional thin section electron microscopy. this could be due to more superficial smears or scrapings in their cases. in certain areas, adenoviral infection may be confused with keratoconjunctivitis (ahc) produced by enterovirus type 70. 21 in ahc, the presence of conjunctival hemorrhage, slight folliculosis, and fre-quent pain in the early stage distinguishes this condition from ekc. in keratoconjunctivitis caused by echovirus 7, associated gastrointestinal symptoms, fever, headache, and lymphadenopathy are present at an early stage, but conjunctival folliculosis was not reported. 22 the two main antigenic types of herpes virus hominis are type 1, commonly associated with infections of the eye, mouth, skin, and upper body, and type 2, associated with genital infections. neumann-haefelin et al2 3 reported 154 patients with hsv type 1 and three with type 2 ocular infections. in the present study, the typical virions of herpes simplex keratitis were readily identified both by immunofluorescence and by negative stain transmission electron microscopy. the patients clinically manifested typical dendritic corneal lesions, which stained with fluorescein. dawson and togni2 4 observed virus particles in corneal epithelium and stroma of human corneal buttons. the virus may replicate in the corneal stroma without any overt inflammation. collin and abelson 25 recently described a case of apparent herpes simplex keratouveitis where the virus was demonstrated by transmission electron microscopy in the cornea removed at the time of a third corneal transplant, indicating that the virus persisted for a considerable period of time. in a case of herpetic iritis, virus was found in the anterior chamber by immunofluorescence and electron microscopy. 26 in specimens of molluscum, the virions displayed typical brickshaped structures 27 and were the largest viruses observed. the mol-luscum lid lesion was a centrally umbilicated lid nodule. light microscopy showed typical cytoplasmic inclusions in the stratum corneum and granulosum. rapid techniques for the detection of viruses in specimens from patients with epidemic keratoconjunctivitis, herpes simplex keratitis, rubella, vaccinia, and molluscum were used. these included direct and indirect immunofluorescence and negative stain electron microscopy. in 1977, 50 conjunctival specimens from patients with ekc showed positive immunofluorescence in 22 cases. the latter were from subjects with onset of infection of up to one week. cultures and typing showed that 20 of these were hybrid type 10-19, one was type 3, and one was type 1. herpes simplex hominis type 1 was recovered in culture and demonstrated by direct immunofluorescence and negative stain electron microscopy in three patients with herpetic dendritic keratitis. in one patient with ocular rubella, lens aspirate showed positive indirect immunofluorescence. in patients with vaccinial and molluscum lid lesions, virions were demonstrated by negative stain electron microscopy. hapten-sandwich labeling: ii. immunospecific attachment of cell surface markers suitable for scanning electron microscopy viral identification by scanning electron microscopy of preparations stained with fluorescein-labeled antibody application of electron microscopy to the diagnosis of virus infection doane fw: lndentification of viruses by immunoelectron microscopy a negative staining-carbon film technique for studying viruses in the electron microscope: i preparative procedures for examining icosahedral and filamentous viruses two-hour embedding procedure for intracellular detection of viruses by electron microscopy rapid virus diagnosis application of immunofluorescence adenoviruses rapid diagnosis of herpes virus hominis infections by immunofluorescent antibody techniques community and hospital outbreaks of epidemic keratoconjunctivitis simultaneous nosocomial and community outbreak of epidemic keratoconjunctivitis with types 8 and 19 adenovirus epidemic keratoconjunctivitis at a vietnamese refugee camp in florida adenovirus type 8 infections in the united states potter mh: epidemic keratoconjunctivitis due to adenovirus type 19 epidemic keratoconjunctivitis and chronic papillary conjunctivitis in london due to adenovirus type 19 epidemic adenovirus keratoconjunctivis cytologic diagnosis of adenoviral epidemic keratoconjunctivitis by direct immunofluorescence the demonstration of toxoplasma and other organisms by immunofluorescence: a pitfall electron microscopy as a diagnostic procedure for viral infections of the eye. twentysecond concilum herpes simplex eye infections: clinical manifestations, pathogenesis and management herpes simplex virus in human cornea, retrocorneal fibrous membrane, and vitreous herpetic iritis: demonstration of virus in the anterior chamber by fluorescent antibody techniques and electron microscopy acknowledgment peter laibson, md, provided a specimen of a herpetic dendrite, and brian altman, md, provided the specimen of lens aspirate from a patient with ocular rubella. serum and antisera were obtained from microbiolo· gical associates, the research resources branch of the national institute of allergy and infectious diseases, and miles laboratories. key: cord-292908-rbn3foj3 authors: hohdatsu, t.; sasamoto, t.; okada, s.; koyama, h. title: antigenic analysis of feline coronaviruses with monoclonal antibodies (mabs): preparation of mabs which discriminate between fipv strain 79-1146 and fecv strain 79-1683 date: 1991-06-30 journal: veterinary microbiology doi: 10.1016/0378-1135(91)90096-x sha: doc_id: 292908 cord_uid: rbn3foj3 abstract we prepared 31 monoclonal antibodies (mabs) against either fipv strain 79-1146 or fecv strain 79-1683, and tested them for reactivity with various coronaviruses by indirect flourescent antibody assay (ifa). sixteen mabs which reacted with all of the 11 strains of feline coronaviruses, also reacted with canine coronavirus (ccv) and transmissible gastroenteritis virus (tgev). in many of them, the polypeptide specifity was the recognition of transmembrane (e1) protein of the virus. we succeeded in obtaining mabs which did not react with eight strains fipv type i viruses (showing cell-associated growth) but reacted with fipv type ii (79-1146, ku-1) and/or fecv type ii (79-1683) viruses (showing non-cell associated growth). these mabs also reacted with ccv or tgev. these mabs recognized peplomer (e2) glycoprotein, and many antigenic differences were found in this e2 protein. these results suggest that fipv type ii and fecv type ii viruses are antigenically closer to tgev or ccv than to fipv type i viruses. furthermore, the mab prepared in this study has enabled discrimination between fipv strain 79-1146 and fecv strain 79-1683, which was thought to be impossible by the previous serological method. for serological diagnosis of feline infectious peritonitis virus (fipv) infection, detection of antibody by indirect fluorescent antibody assay (ifa) is popular (pedersen, 1976b; horzinek and osterhaus, 1979; scott, 1979) . on the other hand, feline enteric coronavirus (fecv) which antigenically crossreacts with fipv, and causes only mild enteritis without inducing fip, may be present (mckeirnan et al., 1981; pedersen et al., 1981a; pedersen et al., 1981b; pedersen et al., 1984) . thus, the serological diagnosis of fip and the mechanisms of its onset become more complex. pedersen et al. (1984a) classified the feline coronaviruses in terms of the disease types. they divided fipv into types i and ii according to the presence or absence of the induction of fip, ability of the viruses to proliferate in cell cultures, and the antigenic relationship with porcine and canine coronaviruses. fecv has been divided into types i and ii in the same way. types i and ii of fipv in this classification can be serologically discriminated by the neutralization test. fipv type i and fecv type ii can also be distinguished by the neutralization test. cultivation of fecv type i in cells is not possible at present, and its serological position remains unclear. on the other hand, even the neutralization test cannot discriminate between fipv type ii and fecv type ii. it goes without saying that, since all feline coronaviruses show cross-reaction in ifa, it is impossible to discern the types of virus infection. there are many healthy but fipv antibody-positive cats living outdoors. as long as fipv type ii and fecv type ii cannot be distinguished serologically, the clinical diagnostic significance of antibody detection in such cats is low. in this study, we attempted to distinguish between the 79-1146 strain classified as fipv type ii and the 79-1683 strain classified as fecv type ii, by means of monoclonal antibodies (mabs). at the same time, we examined feline coronaviruses for antigenic differences by using the mabs. we also investigated the antigenic relationship between feline coronaviruses and canine and porcine coronaviruses. cell cultures. feline whole fetus cells (fcwf-4), crandell feline kidney cells (crfk) and swine kidney cells (cpk) were grown in eagle's minimum essential medium (mem) containing 20% leibovitz l-15 medium (l-15 ) 10% fetal calf serum, 100 units ml-~ penicillin and 100 #g ml-~ streptomycin. the maintenance medium was mem containing 20% l-15 and antibiotics as above. the cells were maintained in a humidified 5% co2 incubator at 37 ° c. viruses. the coronavirus isolates used in this study and their sources are shown in table 1 . among these virus strains, the authors isolated the strain ku-1 of fipv from the liver cells of a kitten with the effusive form of fip, and the strain ku-2 of fipv from the peritoneal cells of an adult cat, also with effusive fip. among the fipv strains used in the study, strains ucd-1, nw-1, ucd-2, ucd-3, ucd-4, black, yayoi and ku-2 show cell-associated growth, and are therefore regarded as type i virus strains in the classification of pedersen et al. (1984a) . moreover, since strain ku-1, like strain 79-1146, pedersen et al., 1984b mckeirnan et al., 1981 pedersen et al., 1981a pedersen, 1976a pedersen et al., 1981a pedersen and black, 1983 pedersen and floyd, 1985 pedersen and floyd, 1985 pedersen and floyd, 1985 black, 1982 pedersen and black, 1983 hayashi et al., 1981 mckeirnan et al., 1981 pedersen et al., 1984b furuuchi et al., 1975 harada el al., 1967 binn et al., 1975 grows well even in crfk cells in a non-cell associated manner, it is considered to be a type ii virus strain. fipv and fecv, tgev, and ccv were passaged two or three times in fcwf-4 cells, cpk cells, and crfk cells, respectively, and were used for the study. preparation of virus antigen. the antigen was prepared with the fipv 79-1146 strain or fecv 79-1683 strain grown in fcwf-4 cell cultures. infectious culture fluid concentrated about tenfold by ammonium sulfate precipitation was layered onto a discontinuous sucrose density gradient (20 and 60%) in an rps 28 rotor (hitachi koki co., ltd., japan) and centrifuged at 27 000 r.p.m, for 2 h. the virus bands formed were collected, diluted in nte buffer, (0.1 m nac1, 0.01 m tris-hc1, ph 7.4, 0.001 m edta) and centrifuged at 80 000 g for 1 h. the virus-containing pellet was suspended in a 1/500 volume of nte buffer. production of antibody-secreting hybrydomas. balb/c mice, about 5 weeks of age, were inoculated intraperitoneally with a mixture of 50/~g of the viral antigen prepared as above and 10 9 cells of pertussis adjuvant. four or six weeks later the mice received an intravenous booster dose of 50/~g of viral antigen, and spleen cells were obtained for fusing 3 d later. the fusion was carried out by essentially the same method described by k/shler and milstein (1975) . polyethyleneglycol-4000 (merck, germany) was used as a fusing agent and the ratio of mouse spleen cells and mouse myeloma cells (p-3/x-63-ag8o6,5,3 ) was 10: 1. the selective medium contained hypoxanthine ( 10-4 m), aminopterin (4× l0 -7 m) and thymidine (1.6× 10 -5 m). the fused cells at a concentration of 3.5 × 10 6 spleen cells per ml was dispensed in 100 /a volumes into wells of 96-well, flat-bottomed microplates (corning glass works, corning, ny ) and incubated at 37 ° c in a humid atmosphere containing 5% co2. after incubation for 2 weeks, the wells were examined and those which contained hybridoma cultures were tested for feline coronavirus specific antibody by an indirect immunofluorescence test (see below). the colonies in antibody positive wells were passaged in 24-well multiplates (coming glass works, corning, ny) and incubated in medium containing hypoxanthine ( 10 -4 m) and thymidine ( 1.6× 10 -5 m). the cells were then cloned by the soft agar method. body-secreting hybridoma cultures were concentrated tenfold by 50% saturation with ammonium sulfate and used for determination of antibody class and subclass by double diffusion in 1% agar gel containing 0.1% nan3. rabbit antisera against mouse immunoglobulins, igg 1, igg 2a, igg 2b, igg 3, igm and iga, and x and 2 chains (miles laboratories, u.s.a. ) were placed in center wells and test samples were added to adjacent wells. the plates were incubated overnight at room temperature in a humidified chamber. indirect fluorescent antibody assay. hybridoma culture supernatant fluid was added to acetone-fixed infected monolayers, incubated for 30 min at 37°c, washed 3 times with phosphate buffered saline solution (pbs) and then stained with rabbit anti-mouse-igg,a,m serum conjugated with fluorescein isothiocyanate (fitc) (miles lab., u.s.a. ). after a further 30 min incubation at 37°c, slides were washed in pbs. stained monolayers were mounted in buffered glycerol and examined using a fluorescence microscope. neutralization (nt) test. serial twofold dilution of the mabs were mixed with an equal volume of a virus suspension diluted so as to contain approximately 200 tcidso/0.1 ml. the mixtures were incubated at 37°c for 60 min. each mixture was then inoculated into cell cultures in flat-bottomed microplates, and incubated in an atmosphere of 5% co2 in air at 37 °c for 6 d. two wells were employed for each antibody dilution. the antibody titer was expressed as the reciprocal of the highest dilution of mab that completely inhibited cytopathic effect in the test. western immunoblotting. viral antigen separated in polyacrylamide gel by sodium dodecyl sulfate-polyacrylamide gel electrophoresis (sds-page) were transferred to nitrocellulose sheets of 0.45/zm pore size. the transfer was carried out electrophoretically by the method adapted from towbin et al. ( 1979 ) in a transfer-blot cell apparatus at 120 ma and 10 v for 14 h using transfer buffer consisting of 3 g 1-~ tris (ph 8.3), 20% methanol and 43.2 g 1-1 glycine. the nitrocellulose sheets were then cut into strips and incubated at 37 °c for 2 h in pbs containing 10% fetal-calf serum. the supernatant fluid of antibody-secreting hybridoma cultures was added in 1 ml volumes to individual strips and incubated at 37°c for 2 h. the strips were then washed 3 times with pbs containing 0.05% tween-20, and incubated at 37°c for 2 h with horseradish peroxidase-conjugated rabbit antibody against mouse igg,a,m (miles lab., u.s.a. ) diluted 1 : 300 with pbs containing 10% fetal calf serum. the strips were then washed and treated with substrate solution containing 0.05 g diaminobenzidine, 50 #1 of 30% h202 in 100 ml of 0.05 m tris-hc1, ph 7.2. when distinct bands appeared about 10 min later, the reaction was stopped by pouring offthe substrate solution and rinsing with distilled water. determination of polypeptide specificity by enzyme-linked immunosorbent assay (elisa). the polypeptide specificity of the mabs which could not be determined by western immunoblotting was determined according to the method of . briefly, the virus antigen described above was first disrupted with 1% nonidet p-40 (np-40). this material was placed on a 15-50% linear sucrose density gradient containing 0.1% np-40, and centrifuged at 80 000 g for 17 h. after fractionation, each fraction was diluted with nte buffer, and allowed to be absorbed by 96-well, flat-bottomed microelisa plates. the mabs against n, e 1 and e2 proteins with polypeptide specificity clarified by western immunoblotting were delivered into the wells of each fraction, and subjected to elisa. elisa was performed according to the method of hohdatsu et al. ( 1987 ) . among the mabs which recognize each protein, fractions which reacted strongly with a single type of mab were collected. elisa was performed with these fractions used as antigens, and the polypeptide specificity of the mabs was determined. 79-1146 was used as the immunogen, 25 mabs (f2-1, f29-1, f16-4, f18-2, f19-1, f30-1, f34-1, f35-2, f36-1, f41-1, f51-1, f52-1, f70-2, f75-3, f15-2, f24-1, f25-1, f46-4, f49-1, f69-3, f80-1, f6-3, f22-3, f23-2, f50-4) were obtained. in addition, with fecv strain 79-1683 as the immunogen, 6 mabs (el 5-2, e19-1, e22-2, e6-2, e25-2, e-12-1 ) were obtained. the polypeptide specificity, ig isotypes, and nt activity to fipv strain 79-1146 of these mabs are shown in table 2 . for most mabs, western immunoblotting could determine their polypeptide specificity. however, this method failed to determine the specificity of 4 mabs, f6-3, f22-3, f23-2 and f50-4. elisa using np-40 disrupted, sucrose gradient-purified viral polypeptide revealed that these mabs recognise e2 protein. moreover, western immunoblotting and elisa using viral polypeptide yielded the same results with respect to the other mabs. figure 1 shows examples of the western immunoblotting reaction of mabs which recognize n, e1 and e2 proteins. as shown in table 2 , two (f69-3, el2-1 ) of the 31 mabs had nt activity to fipv strain 79-1146. we examined the mabs for reactivity with feline coronaviruses by ifa. as shown in table 3 by means of indirect if test, with fitc-conjugated rabbit anti-mouse immunoglobulin, on each virus-infected cvfk or cpk cell culture grown on coverslips. the monoclonal antibodies were used undiluted cell culture fluids. the minus sign indicates negative reactivity. the polypeptide specificity of each of the mabs was determined by its reactivity to each of the three major structural components of the fipv virion either by immunoblotting of sds-page or by elisa. did react with the only strain of fecv. all mabs in group iv, v and vi were found to recognize e2 protein. we examined the mabs for reactivity with porcine and canine coronaviruses by ifa. table 4 shows the results. all mabs in group i, which reacted with all feline coronaviruses, also reacted with ccv and tgev. mabs in groups ii and iii, which did not react with ucd-2, ucd-3, ucd-4 and black strains, did not react with ccv and tgev either. however, out of four mabs in group iv, which reacted only with the 79-1146 and ku-1 strains of fipv and strain 79-1683 of fecv, three reacted with either ccv or tgev. moreover, among the mabs in group v, which reacted only with the 79-1146 and ku-1 strains of fipv, two reacted with the sh strain of tgev, and 1 type reacted with the 1-71 strain of ccv. furthermore, mabs in group vi, which reacted with fecv alone, reacted with the 1-71 strain of ccv. thirty-one mabs were prepared by using strain 79-1146, classified as fipv type ii, and strain 79-1683, classified as fecv type ii, as immunogens. table 3 shows their reactivity with 11 strains of feline coronavirus. all 16 mabs in group i reacted with feline coronaviruses. besides feline coronaviruses, these mabs reacted with the 1-71 strain of ccv, and the sh and to-163 strains of tgev. these results confirm the previous reports (pedersen et al., 1978; horzinek et al., 1982; pedersen et al., 1984a) that these virus strains are antigenically close to each other. concerning polypeptide specificity, many mabs in this group i recognize e 1 protein. among these viruses, many common epitopes seem to exist, particularly in the e 1 protein. among eight virus strains with the characteristics of fipv type i, reactivities of e6-2 and e22-2 in group ii, and f29-2 in group iii with the mabs were different, and all of these mabs recognized n protein. four mabs in group iv (f50-4, f46-4, f69-3 and f 15-2 ) reacted with the 79-1146 and ku-1 strains of fipv type ii and strain 79-1683 strain of fecv type ii, but not with fipv type i viruses. of these mabs, however, f50-4 reacted with ccv, and f46-4 and f69-3 reacted with ccv and tgev. similarly, among the mabs in group v, which react with fipv type ii viruses alone, f6-3 reacted with ccv, and f24-1 and f49-1 reacted with the sh strain of tgev. furthermore, all mabs in group vi, which react with the 79-1683 strain of fecv alone reacted with ccv. as pedersen et al. (1984a) have reported from their study with polyclonal antibody, these results suggest that fipv type ii viruses and fecv type ii viruses are antigenically closer to tgev or ccv than to fipv type i viruses. at present, the authors are preparing mabs with neutralizing activity using fipv strain 79-1146 as immunogen, and are determining the serological re-lationships among these viruses by the presence or absence of the neutralization epitope. moreover, since all 12 mabs in groups iv, v and vi recognize e2 protein, it was assumed that there are many antigenic differences in e2 protein among these viruses. by using mabs, also found antigenic differences among feline coronaviruses, especially in the e2 protein. conventional serological methods have failed to discriminate between strain 79-1146 of fipv type ii and strain 79-1683 of fecv type ii. however, mabs in group v reacted with fipv type ii viruses alone, while mabs in group vi reacted with the 79-1683 strain of fecv type ii alone. these mabs have enabled the discrimination of these viruses, by clearly indicating antigenic differences among them. the proportions of types i and ii of fipv and types i and ii of fecv actually present in the natural environment are not clear. as stated in the introduction, the neutralizing test can appraise infection with type i and ii of fipv at the serological level. however, in the case of infection with viruses other than fipv type i, distinction of infection particularly by fipv type ii an fecv type ii at the serological level is difficult. in the future, it will be of use to be able to distinguish infection of these viruses by competitive enzyme immunoassay (fiscus et al., 1985; using type-specific mabs. the mabs in groups v and vi which the authors have prepared in this study are expected to be useful as such type-specific mabs. recovery and characterization of a coronavirus from military dogs with diarrhoea recovery and in-vitro cultivation ofa coronavirus from laboratory-induced cases of feline infectious peritonitis (fi p ) antigenic comparison feline coronavirus isolates: evidence for markedly different peplomer glycoproteins competitive enzyme immunoassays for the rapid detection of antibodies to feline infectious peritonitis virus polypeptides epitope-specific antibody responses to virulent and avirulent feline infectious peritonitis virus isolates comparison between virulent and attenuated strains of transmissible gastroenteritis virus studies on transmissible gastroenteritis in pigs. iii. isolation of cytopathogenic virus and its use for serological investigation serodiagnosis for feline infectious peritonitis by immunofluorescence using infected suckling mouse brain sections antigenic variation of porcine transmissible gastroenteritis virus detected by monoclonal antibodies feline infectious peritonitis: a worldwide serosurvey antigenic relationships among homologous structural polypeptides of porcine, feline and canine coronaviruses continuous cultures of fused cells secreting antibody of predefined specificity isolation of feline coronaviruses from two cats with diverse disease manifestations morphologic and physical characteristics of feline infectious peritonitis virus and its growth in autochthonous peritoneal cell cultures serologic studies of naturally occurring feline infectious peritonitis attempted immunization of cats against feline infectious peritonitis, using avirulent live virus or sublethal amounts of virulent virus experimental studies with three new strains of feline infectious peritonitis virus: fipv-ucd2, fipv-ucd3 and fipv-ucd4 antigenic relationship of feline infectious peritonitis virus to coronaviruses of other species infection studies in kittens utilizing feline infectious peritonitis virus propagated in cell culture 198 lb. an enteric coronavirus infection of cats and its relationship to feline infectious peritonitis pathogenic differences between various feline coronavirus isolates pathogenicity studies of feline coronavirus isolates 79-1146 and 79-1683 fip antibody test-interpretation and recommendations electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications this work has been funded by the kitasato research foundation under grant no. 6. key: cord-026548-z2ifu1d6 authors: lagaillardie, nicolas; neykova, rumyana; yoshida, nobuko title: implementing multiparty session types in rust date: 2020-05-13 journal: coordination models and languages doi: 10.1007/978-3-030-50029-0_8 sha: doc_id: 26548 cord_uid: z2ifu1d6 multiparty session types (mpst) is a typing discipline for distributed protocols, which ensures communication safety and deadlock-freedom for more than two participants. this paper reports on our research project, implementing multiparty session types in rust. current rust implementations of session types are limited to binary (two-party communications). we extend an existing library for binary session types to mpst. we have implemented a simplified amazon prime video streaming protocol using our library for both shared and distributed communication transports. in the last decade, the software industry has seen a shift towards programming languages that promote the coordination of concurrent and/or distributed software components through the exchange of messages over communication channels. languages with native message-passing primitives (e.g., go, elixir and rust) are becoming increasingly popular. in particular, rust has been named the most loved programming language in the annual stack overflow survey for four consecutive years (2016-19) 1 . the advantage of message-passing concurrency is well-understood: it allows cheap horizontal scalability at a time when technology providers have to adapt and scale their tools and applications to various devices and platforms. messagepassing based software, however, is as vulnerable to errors as other concurrent programming techniques [16] . much academic research has been done to develop rigorous theoretical frameworks for verification of message-passing programs. one such framework is multiparty session types (mpst) [5] -a type-based discipline that ensures that concurrent and distributed systems are safe by design. it guarantees that message-passing processes following a predefined communication protocol, are free from communication errors and deadlocks. rust is a particularly appealing language for the practical embedding of session types. its affine type system allows for static typing of linear resourcesan essential requirement for the safety of session type systems. rust combines efficiency with message-passing abstractions, thread and memory safety [15] , and has been used for the implementation of large-scale concurrent applications such as the mozilla browser, firefox, and the facebook blockchain platform, libra. despite the interest in the rust community for verification techniques handling multiple communicating processes 2 , the existing rust implementations [8, 9] are limited to binary (two-party) session types. in this short paper, we present our design and implementation for multiparty session types in rust. our design follows a state-of-the-art encoding of multiparty into binary session types [13] . we generate local types in rust, utilising the scribble toolchain [12, 18] . our library for mpst programming in rust, mpst-rust, is implemented as a thin wrapper over an existing binary session types library [9] . differently from other mpst implementations that check the linear usage of channels at runtime (e.g. [6, 13] ), we rely on the rust affine type system to type-check mpst programs. in addition, since we generate the local types from a readable global specification, errors caused by an affine (and not linear) usage of channels, a well-known limitation of the previous libraries [8, 9] , are easily avoided. this paper is organised as follows: sect. 2 gives an overview of our framework with a usecase; sect. 3 shows our implementation and discusses the advantages of our approach; and sect. 4 concludes with related and future work. our library is available from https://github.com/nicolaslagaillardie/mpst rust github. framework overview: mpst in rust. our design resembles the top-down methodology of multiparty session types, as illustrated in fig. 1 . it follows three main steps [5, 17] . first, a global type, also called a global protocol, is defined as a shared contract between communicating endpoint processes. a global protocol is then projected to each endpoint process, resulting in a local type. a local type involves only the interactions specific to a given endpoint. finally, each endpoint process is type-checked against its projected local type. the specific parts of our framework that distinguish it from other stateof-the-art mpst works are highlighted in red, which corresponds to our new library for mpst programming in rust, mpst-rust. it is realised as a thin wrapper on top of an existing rust library for validation of binary (2-party-only) session types. developers use the mpst primitives provided by mpst-rust to implement endpoint programs. also, our framework allows the types for each communication primitive to be either (1) generated from the scribble toolchain; or (2) written by the developers. the scribble toolchain [18] provides facilities for writing, verifying and projecting global protocols. our framework guarantees that processes implemented using mpst-rust primitives with scribble-generated types are free from deadlocks, reception errors, and protocol deviations. next, we explain, via an example, how the framework of mpst can be applied to rust. example: amazon prime video streaming. the amazon prime video streaming service is a usecase which can take full advantage of multiparty session types. each streaming application connects to servers, and possibly other devices, to access services, and follows some specific protocol. to present our design, we use a simplified version of the protocol, illustrated in the diagram in fig. 1 (right). the diagram should be read from top to bottom. the protocol involves three services -an authenticator service, a server and a client. at first, client connects to authenticator by providing an identifying id. if the id is accepted, the session continues with a choice on client to either request a video or end the session. the first branch is, a priori, the main service provided by amazon prime video. client cannot directly request videos from server, and has to go through authenticator instead. on the diagram, the choice is denoted as the frame alt and the choices are separated with the horizontal dotted line. the protocol is recursive, and client can request new videos as many times as needed. the arrow going back on client side in fig. 1 represents this recursive behaviour. to end the session, client first sends close message to authenticator, which then subsequently sends a close message to server. implementing the authenticator role using mpst-rust. due to space limitations, we only show the implementation of the authenticator role (hereafter role a), the implementations of the other roles (role b for the server and role c for the client) are similar. the rust code for role a using the mpst-rust library is given in fig. 2 (left). it closely follows the local protocol in fig. 2 (right), that is projected from the global protocol by the scribble toolchain. first, line 1 declares a function authenticator that is parametric in a multiparty channel s of type videop_a. the type videop_a specifies which operations are allowed on s. this type can either be written by the developer, or generated by scribble (cf. listing 1). on line 3, a receives an identifying id from c. the function recv_mpst_a_to_c, provided by mpst-rust library returns the received value (the id) and the new multiparty channel, to be used in subsequent communications. line 3 rebinds ok the multiparty channel s with the new channel that is returned. then, on line 4, we send back the answer to c, by utilising another mpst-rust communication primitive, send_mpst_a_to_c. the variable s is rebound again to the newly returned multiparty channel. note that although the name of the function, send_mpst_a_to_c, suggests a binary communication, the function operates on a multiparty channel s. our implementation follows the encoding, presented in [13] , which encodes a multiparty channel as an indexed tuple of binary channels. internally, send_mpst_a_to_c extracts from s the binary channel established between a and c and uses it for sending. lines 9-26 proceeds by implementing the recursive part of the protocol. the implementation of authenticator_recurs realises an internal choice -a can either receive a videorequest or a close. this behaviour is realised by the mpst-rust macro offer_mpst_a_to_c! (line 12), which is applied to a multiparty channel s of a sum type between choicea::video and choicea::end. the behaviour of each branch in the protocol is implemented as an anonymous function. for example, code in lines 13-21 supplies an anonymous function that implements the behaviour when c sends a videorequest, while lines 22-26 handle the close request. finally, close_mpst(s) closes all binary channels stored inside s. the types of the multiparty channel, as well as the generic types in the declaration of the mpst-rust communication functions, enable compile-time detection of protocol violations, such as swapping line 3 and line 4, using another communication primitive or using the wrong payload type. fig. 2 (left) , are given in listing 1. these types can be either written by the developer or generated from a global protocol, written in scribble. reception error safety is ensured since the underlying mpst-rust library checks statically that all pairs of binary types are dual to each other. deadlock-freedom is ensured only if types are generated from scribble since this guarantees that types are projected from a well-formed global protocol. next, we explain a type declaration for the authenticator role. lines 27-37 specify the three sessionmpst types which correspond to the types of the session channels used in fig. 2 (left) -types videop_a (line 1), video_prec_a (line 9), and the types used inside the offer construct -choicea::video (line 13), and choicea::end (line 22). in the encoding of [13] , which underpins mpst-rust, a multiparty channel is represented as an indexed tuple of binary channels. this is reflected in the implementation of sessionmpst, which is parameterised on the required binary session types. for example, the videop_a takes as a parameter the binary types between a and c, and between a and b. at the beginning of the protocol (lines 1-7 in fig. 2 (left) ) b and a do not interact, hence the binary type for b is end. the type inita (line 2 in listing 1) specifies the behaviour between a and c, notably that a first receives a message, then it sends a message, and later it continues as the type recvchoice. the binary session types between a and b, and between a and c are given in lines 12-14 and lines 2-9 respectively; we use the primitives declared in the existing binary session types library [9] . the generic parameter n refers to a trait such as i32. the third parameter for videop_a (line 27) is a queue-like data structure, queueainit (line 17), that codifies the order of usage of each binary channel inside a multiparty session channel. this is needed to preserve the causality, imposed by the global protocol. the queues for the other sessionmpst types are given in lines 21-24. for instance, the queue for the choicea:video branch of the protocol is queueavideo. note that, according to the protocol, a first has to receive a videorequest message from c, and then it has to forward that message to b hence, swapping of lines 17 and 18 from fig. 2 is a protocol violation error. we can detect such violations since the queue for the type choicea::video, queueavideo (line 21), is specified as roleatoc, which codifies that first the channel for c and then the channel for b should be used. note that none of the defined queues is recursive. recursion is implicitly specified on binary types, while each queue is related to a sessionmpst type. distributed execution environment. the default transport of mpst-rust is the built-in rust communication channels (crossbeam channel). also, to test our example in a more realistic distributed environment, we have also connected each process through mqtt (mq telemetry transport) [7] . mqtt is a messaging middleware for exchanging messages between devices, predominantly used in iot networks. at the start of the protocol, each process connects to a public mqtt channel, and a session is established. therefore, we have mapped binary channels to mqtt sockets, in addition to the built-in rust channels. multiparty channels as an ordered tuple of binary channels. the main idea of the design of our framework is that a multiparty session can be realised with two ingredients: (1) a list of separate binary sessions (one session for each pair of participants) and (2) a queue that imposes the ordering between the binary channels. listing 2 (lines 2-3) shows the implementation of a multiparty channel in a 3-party protocol. the sessionmpst structure holds two fields, session1 and session2, that are of a binary session type. for an illustration purpose, we show only the implementation of a multiparty channel for three processes. the same approach can be generalised, using our code generation tool, to any number of communicating processes. for example, in case of a protocol with four roles, each multiparty session will have four fields -a field for the binary session between each pair of participants and a field for the queue. the order of usage of the binary channels of a sessionmpst object is stored inside the queue field. for instance, the behaviour that role a has to communicate first with role b, then with a role c, and then the session ends can be specified using a queue of type roleatob>. note that all queue types, such as roleatob, roleatoc, are generated. as explained in sect. 2, programming with mpst-rust relies on communication primitives, such as send_mpst_a_to_b, that have the sender and receiver roles baked into their name. to ensure that the binary channels are used as specified by the global protocol, each communication function is parametric on a generic quadruple type where t is a payload type, s1 and s2 are binary session types and r is a type for a queue (mpst-queue type) that imposes the order in which the binary sessions inside a multiparty session must be used. 1 // basic structure for mpst 2 pub struct sessionmpst< s1: session, s2: session, r: role> { 3 pub session1: s1, pub session2: s, pub queue: r } 4 // implementation of a communication function from the mpst-rust library 5 pub fn send_mpst_a_to_b(x: t, 6 s: sessionmpst, s2, roleatob>,) -> sessionmpst 7 where t: ..., s1: listing 2 (lines 5-9) shows the implementation for send_mpst_a_to_b(). as clear from the type parameters, the client of the function should supply a mpstqueue type roleatob. the binary session type s1 should be encapsulated in a send. the body of the function sends the message of type t on the binary channel stored in the first field, session1 (corresponding to the binary session with role b), of the multiparty session s. since the communication is on a binary channel, we reuse the binary send primitive from [9] . external and internal choices are implemented as macros that require an argument of type sessionmpst. the implementation of offer_mpst_a_to_c is given in lines 11-14. in essence, a choice is implemented as a broadcast from one role to the others. in our usecase, the active role that makes the choice is c. hence, the macro offer_mpst_a_to_c explicitly performs a receive (recv_mpst_a_-to_c(s)) on the session channel s. the received value is pattern matched and passed to any of the functions given as arguments to offer_mpst_a_to_c. similarly, choose_mpst_c_to_all in lines 19-26 is a macro that performs a select operation. the active role c sends the selected label to all roles in the protocol. in our particular example, c sends the selected label l to a and b. discussions. our implementation, although intuitive, does not resolve the inherent conflict between rust, which is affine, and session types, which are linear. the implementation suffers from the same drawback as [9] . however, the mpst methodology is a step forward in terms of usability. differently than the rust local types which can get convoluted, the syntax of global protocols is user-friendly and readable. developers can use the global protocol as guidance, and hence avoid errors such as prematurely ending of a session. moreover, as observed in kokke's library [9] , most of the errors are caused by misuse of methods and functions. since we are code-generating the local types, the chance of misspelling is significantly reduced. another viable option for our framework is to take the bottom-up approach: to check directly whether a set of manuallywritten rust local types satisfy safety/liveness properties by a model checker [14] or the multiparty compatibility (a property which guarantees deadlock-freedom of communicating automata, which are equivalent to local session types) [2, 11] . the rust library in [8] implements binary session types, following [4] . it checks at compile-time that the behaviours of two endpoint processes are dual, i.e the processes are compatible. the library in [9] , based on the egv calculus by fowler et al. [3] , provides constructs for writing and checking binary session types, and additionally supports exception handling constructs. we build on top of the library in [9] since it offers several improvements in comparison to [8] . most importantly, the treatment of closing a channel prematurely in [8] may lead to memory leaks. both libraries suffer from a well-known limitation of binary session types 3 . notably, since deadlock-freedom is ensured only inside a session, a rust endpoint process, that communicates with more than one other process, is prone to deadlocks and communication errors. our framework solves that limitation by expanding the scope of a session to multiple participants. our proposed design follows the methodology given by [6] , which generates java communicating apis from scribble. this, and other multiparty session types implementations, exploit the equivalence between local session types and communicating automata to generate session types apis for mainstream programming languages (e.g., java [6, 10] , go [1] , f# [13] ). each state from state automata is implemented as a class, or in the case of [10] , as a type state. to ensure safety, state automata have to be derived from the same global specification. all of the works in this category use the scribble toolchain to generate the state classes from a global specification and detect linearity violations at runtime. this paper proposes the generation of protocol-specific apis, which promotes type checking of protocols at compile-time. this is done by projecting the endpoints' state space in those protocols to groups of channel types in the desired language. in the future, we plan to implement the bottom-up approach, in addition to the top-down approach outlined in this paper, as to compare their productivity and scalability. distributed programming using role parametric session types in go multiparty compatibility in communicating automata: characterisation and synthesis of global session types exceptional asynchronous session types: session types without tiers language primitives and type discipline for structured communication-based programming multiparty asynchronous session types hybrid session verification through endpoint api generation mqtt-s-a publish/subscribe protocol for wireless sensor networks session types for rust rusty variation: deadlock-free sessions with failure in rust typechecking protocols with mungo and stmungo verifying asynchronous interactions via communicating session automata session types for rust a linear decomposition of multiparty sessions for safe distributed programming less is more: multiparty session types revisited the rust programming language. 1.35.0 edn understanding real-world concurrency bugs in go a very gentle introduction to multiparty session types the scribble protocol language acknowledgement. the work has been partially supported by the following funding schemes vetss, epsrc ep/k011715/1, ep/k034413/1, ep/l00058x/1, ep/n027833/1, ep/n028201/1, ep/t006544/1 and, ep/t014709/1. key: cord-010657-5qtsj8xv authors: heckman, carol a.; dalbey, walden e. title: pathogenesis of lesions induced in rat lung by chronic tobacco smoke inhalation date: 1982-07-01 journal: j natl cancer inst doi: 10.1093/jnci/69.1.117 sha: doc_id: 10657 cord_uid: 5qtsj8xv lesions were induced in the lungs of specific-pathogen-free f344 rats by chronic tobacco smoke exposure. animals exposed to 7 cigarettes/day were killed after 1, 1.5, or 2 years of exposure. parallel lifetime exposures induced pulmonary tumors in 9% of the animals. in serially killed animals, four types of lesions were found: 1) perivascular or peribronchiolar accumulation of lymphoreticular cells, 2) fibrotic and cellular enlargement of peribronchiolar septa, 3) type ii cell hyperplasia with septal fibrosis, and 4) air-space enlargement (emphysema). however, emphysema occurred only in animals exposed to a higher (10 cigarettes) dose of tobacco smoke. ultrastructural studies showed all of the focal lesions to be infiltrated by cells typical of the inflammatory response. the type ii hyperplastic and peribronchiolar alveolar lesions involved larger portions of the parenchyma in fibrotic changes but differed in structure, location, and frequency. the incidence of the peribronchiolar alveolar lesions was temporally related to tumor incidence. numerous previous reports have described the effects of tobacco smoke exposure on lung structure. in studies by roe's group (1, 2) , the major lesions induced in the rat lung by lifetime exposure were columnar, cuboidal, and squamous metaplasias of the alveolar epithelium. all three types of lesions were significantly more frequent in smoke-exposed than in control animals (1) and could be induced by intratracheal instillation of smoke condensate (2) . however, neoplasms could be induced only by intratracheal instillation of the polycyclic aromatic hydrocarbon-containing fraction of smoke condensate (2) . no statistically significant increase in pulmonary neoplasm incidence was found in animals exposed to smoke by inhalation, presumably because the animals died prematurely from chronic respiratory disease (1). short-term studies conducted independently by walker et al. (3) on rats exposed to tobacco smoke for 6 weeks showed characteristic lesions at the level of the respiratory bronchiole, including peribronchiolar and perivascular infiltration by lymphocytes, focal pneumonitis, and alveolar cuboidal or columnar metaplasia. the metaplastic changes, along with increases in macrophage size and number, were thought to be dose-dependent. the other lesions were considered early manifestations of chronic pulmonary infection (3) , morphologic changes have also been induced in the lungs of beagle dogs by 2-5 years of tobacco smoke exposure (4) . marked fibrosis and emphysema were found, as were type ii cell hyperplasia and squamous metaplasia of the alveolar epithelium. at the epithelial-mesenchymal interface, projections of the epithelial cells into the stroma and thickening and reduplication of the basal lamina (5) were also seen. despite the substantial number of experiments with chronic tobacco smoke inhalation, only two laboratories have reported significant induction of pulmonary tumors in exposed rodents. one report showed a twofold higher inci-dence of adenocarcinomas in smoke-exposed mice than in control mice, the gas phase of the smoke was found to induce an even higher tumor incidence than the whole smoke (6) . more recently, a lifetime exposure of rats to tobacco smoke produced a 9% incidence of respiratory tract tumors, including adenomas, adenocarcinomas, and squamous cell carcinomas (7) . in this experiment, animals exposed in parallel with those for the lifetime study were killed at earlier intervals for assessment of morphologic lesions induced by smoke inhalation. the present report characterizes those lesions. many of the alterations appeared to be similar to those described above. however, 1 lesion was found that had not been found in previous experiments, i.e., fibrotic thickening of alveolar septa in peribronchiolar locations. exposure conditions.-spf female f344 rats were exposed to tobacco smoke in the maddox/ornl smoking machine as previously described (7) . beginning at 12-14 weeks of age, the animals were gradually exposed to increasing dosages of tobacco smoke from standard 85-mm, nonfiltered experimental cigarettes (national cancer institute code 16). two final dose levels were used, 7 or 10 cigarettes/day, and the animals were killed at time intervals from 1 to 2 years after exposure began. the exact number of animals killed at various times in each dose group is shown in table 1. since mortality was high in the lo-cigarette-per-day group, all the remaining animals in this group were killed at 1.5 years. both untreated and sham-exposed groups were killed in parallel with the exposed animals. additional data were tz"ssue preparation.-before they were killed, the animals were anesthetized with 30 mg fentobarbital/kg body weight. for tissue fixation the trachea was cannalized; the airways and lungs were removed and fixed with buffered formaldehyde under 20 cm of pressure for 24-48 hours. the lung lobes were cut along the bronchus, except for the left lobe, which was cut in cross section just anterior to the entry of the bronchus. the tissues were embedded in paraffin. sections from the right lobes were used to determine the number of fibrotic lesions in the lungs of smoke-exposed animals. all of the sections were examined, and the cumulative number of lesions, normalized to the number of animals killed, was used as an estimate of the frequency of each type of lesion. sections from the left lobes, stained with hematoxylin and eosin, were used for morphometric analysis. for each sample, 10 fields were selected at random and viewed at 100x magnification through a weibel ocular. fields comprised of more than one-third conducting airways or vasculature were excluded. the mean linear intercept was determined, and point counts (420 points/lobe) were made to obtain the volume percent of alveolar versus nonalveolar air space and respiratory versus nonrespiratory tissue. alveoli were defined as enclosed circles or as open semicircles with a radius greater than half the distance across the opening. additional sections of the left lobes were stained with snook's silver stain for reticulum, aldehyde fuchsin, and lushbaugh's stain. each time rats were killed, tissues were also processed for electron microscopy by airway perfusion of a 2% glutaraldehyde solution containing 4.6% tyrode's solution and 0.05 m collidine buffer (ph 7.3). the tissues were fixed for 2 hours under 15-cm pressure and retained in collidine buffer until further processing. after exposure to 2% osmium tetroxide in 0.1 m cacodylate for 3 hours, selected blocks of tissue were dehydrated in acetone and embedded in a standard epoxy mixture (9) . sections 2}.tm in thickness were cut on the sorvall jb-4 microtome and stained with 0.05% toluidine blue in 2.5% sodium carbonate. selected areas of the blocks were thin sectioned on the sorvall mt-2 ultramicrotome, mounted on formvar-coated grids, and stained with uranyl acetate and lead citrate (10) . thin sections were examined with the siemens 101 or hitachi hu-11b electron microscope. for each pathologic change studied, at least four examples were examined ultrastructurally. some changes in the lung parenchyma following smoke exposure were readily apparent on a gross level. lungs from animals exposed to 7 cigarettes/day for 1 year had dark foci about 1 mm in diameter scattered over their surfaces. with longer exposures or with exposure to 10 cigarettes/day, there were increasing numbers of larger white nodules about 1-4 mm in diameter. four types oflesions could be distinguished microscopically in the pulmonary parenchyma: i) perivascular or peribronchiolar accumulation of lymphoreticular cells, 2) fibrotic and cellular enlargement of peribronchiolar septa, 3) type ii cell hyperplasia with septal fibrosis, and 4) air-space enlargement (emphysema). the first type of lesion was most common in the lungs of animals exposed to 7 cigarettes/day for 2 years. the last lesion type was seen only in animals exposed to 10 cigarettes/day. perivascular lesions occurred frequently in the lung parenchyma after 2 years of smoke exposure, averaging 3 lesions/section of approximately 0.5 cm 2 . the frequency after a 2-year exposure was approximately double that after a i-year exposure. the lesions were characteristically associated with venules and arterioles in the parenchyma. they were most common in branches of the pulmonary vein located at or below the level of the terminal bronchiole (figs. la, 1b) and were also found in bronchial veins, but they were never seen in the adventitia of major arteries. perivascular accumulations of cells were also found rarely in unexposed rats and consisted of large lymphocytes and macrophages (fig. ic). the lesions of smoke-exposed lung tissues contained predominantly particulate-laden macrophages (figs. la, ib). an ultrastructural analysis of several lesions associated with venules showed that lymphocytes, plasma cells, and, occasionally, fibroblasts were closely apposed to macrophages in the adventitia ( fig. 2 ). while macrophages and lymphocytes were usually seen adjacent to the basal lamina of the epithelium, the cell mass was separated from the epithelium by a basement membrane in some lesions. in addition to the adventitial lesions, a separate lesion was sometimes found around major veins, consisting of lymphocytes within the lumen of lymphatic vessels. the lymphatic endothelium in these lesions frequently contained smoke particulates (figs. 3a, 3b). however, lesions with characteristics intermediate between those of the lymphatic and adventitial lesions were not found, so a common etiology seemed unlikely. lesions similar to the other adventitial perivascular lesions were also found near the bronchiolar-alveolar junction, most frequently between the bronchiole and the bronchial vein and extending only part of the way around the bronchiole. therefore, most of these lesions \ ere also perivascular in location. septal enlargement was characteristic in peribronchiolar locations, but it was also found in type ii hyperplasias. the enlarged septa in both lesions had similar ultrastructural features. generally, both histologic types of lesions were larger than perivascular lesions and could be discerned readily in paraffin-embedded lung tissue. neither type of lesion was found in the lungs of control animals, and the frequency of both types increased with the number of cigarettes smoked and the cumulative time of smoke exposure (table 2). the type ii hyperplastic lesions always constituted more than 90% of the total number oflarge lesions. however, the total number of peribronchiolar lesions increased markedly in the later stages of exposure at a dose of 7 cigarettes/ day. in animals exposed at the higher dose rate of 10 cigarettes/day for 1.5 years, the peribronchiolar lesions constituted only 2% of the large lesions, even though the cumulative dose of tobacco smoke was comparable to that delivered in the 2-year exposure at the lower dose rate. the peribronchiolar lesions constituted 7% of the large lesions under the latter conditions. in paraffin-embedded sections treated with lushbaugh's stain for collagen, the amount of collagen seen in lesions showing septal enlargement appeared to increase in relation to the dose of tobacco smoke. no obvious increases in reticular fibers (snook's silver stain) or elastic fibers (aldehyde fuchsin) were observed. although the two types of lesions exhibiting septal enlargement differed in location, frequency, and the type of lining epithelium present, the septal constituents were similar when examined ultrastructurally. peri bronchiolar lesions were characterized by an attenuated epithelium septal thickening may also have occurred in loci separate from larger lesions, this was evidently rare; a few areas where enlargement was seen in isolation from neighboring lesions were found by serial sectioning to be adjacent to lesions. type ii hyperplastic lesions were observed most frequently at the pleura (figs. 5a-5c) but were also in the lung parenchyma adjacent to the distal airways ( fig. ib) . in animals exposed to a dose of 7 cigarettes/day for i or 2 years, about 60% of the lesions were located on the pleura. when pleural lesions embedded in epoxy resins were serially sectioned, nearly all of them were found to be adjacent to sites where one or more alveolar ducts terminated on the pleura; about half were also distal to or surrounding perivascular lesions (fig. 5b ). fibrosis was obvious at the light microscopic level in the alveolar septa of all type ii cell lesions. the septal enlargements studied by electron microscopy contained numerous cells of the lymphoreticular system, i.e., plasma cells, lymphocytes, polymorphonuclear leukocytes, macrophages, and mast cells. fibroblasts were also seen in all of the lesions and frequently appeared hypertrophic relative to those in unaffected septa ( fig. 6 ). there were also extensive bundles of collagen fibers within the interstitium. capillaries within the septa had swollen or hypertrophic endothelial cells that frequently occluded the lumen. in other areas the basal lamina showed extensive thickening, infolding, or reduplication ( fig. 6 ). the largest peri bronchiolar lesions exhibited an aberrant morphology in which lengths of the basal lamina were completely surrounded by lymphoreticular cells, indicating areas of probable fusion of adjacent septa. although the cellular constituents were similar to those in smaller lesions, they included fragments of cells embedded in an amorphous extracellular material resembling fibrin (fig. 7) . these were thought to be derived from capillaries that were no longer patent. in densely fibrotic and cellular areas, there were relatively few capillaries of normal appearance. both the squamous and type ii epithelial cells in these areas sometimes contained an osmiophilic cytoplasm with an elaborate endoplasmic reticulum. both epithelial cells and fibroblasts in these areas frequently contained osmiophilic granules resembling lipid droplets ( fig. 7) . the cellular and extracellular constituents involved in enlargement of the interstitium in type ii hyperplastic lesions were similar to those described in the preceding section. all of the type ii lesions studied showed some degeneration of basal lamina structure; in areas where marked degeneration occurred, the type i epithelium was separated from the underlying connective tissue (fig. 8 ). degenerative changes were frequently, though not always, found in areas where luminal macrophages were in close contact with the type i epithelium. the presence of phagocytes (i.e., macrophages and polymorphonuclear leukocytes) in the interstitium had little relationship to the position of basal lamina degeneration. the lining epithelium in hyperplastic lesions consisted of cells with an undifferentiated appearance, which could be flattened, distorted in shape, or hypertrophic. some of the cells showed long microvilli on their luminal surfaces. in addition, most lesions contained cuboidal, type iii cells, with an extensive endoplasmic reticulum rather than the lamellar bodies typical of type ii cells ( fig. 9 ). other type iii cells had a dense cytoplasm, abundant profiles of endoplasmic reticulum, and osmiophilic inclusions ( fig. 10 ). lymphocytes were frequently found as cellular constituents of the epithelium. binucleate cells and evidence of stratification in the epithelium were seen in about half of the lesions. a few lesions also contained large cells with an exceptionally clear cytoplasm ( fig. 8 ). in addition to the focal lesions described above, we detected a general tendency for enlargement of the air space in animals exposed to a high dose of tobacco smoke for 1 year or more. this trend was indicated by an increase in the apparent nonalveolar air space. although a similar trend was seen in the surviving animals of the low-dose group, it fell short of statistical significance. exposure of animals to 7 cigarettes/day for up to 2.5 years did not significantly influence the mean linear intercept (table 3) . however, exposure to 10 cigarettes/day had a more pronounced effect on lung architecture: the mean linear intercept was 10creased significantly above control levels at both 1 and 1.5 years of exposure (table 3) . we obtained the present results on tobacco smoke inhalation in parallel with a lifetime study that demonstrated the induction of several types of lung tumors by tobacco smoke (7) . the animals were maintained under spf conditions; thus the histopathologic interpretation of pulmonary lesions was not complicated by chronic lung disease, and survival was not compromised by infection. in the lifetime experiment, the observation of tobacco smoke-induced tumors clearly was dependent on the long-term survival of the experimental animals. the mean survival time (â± sd) was 2.3â±o.6 years for rats exposed to 7 cigarettes/ day, 2.4â±o.4 years for untreated controls, and 2.6â±0.4 years for sham-exposed controls. the survival curves for these 3 groups were not significantly different. the earliest of the 5 adenomas found among the treated animals appeared at 2.0 years, and the average age at death of the animals with these tumors was 2.6 years. for the 5 other lung and nasal tumors, which were adenocarcinomas and a squamous cell carincoma, the average age at death was 3.1 years. only 1 alveologenic carcinoma was observed in the control animals over their life-span. the final incidences of respiratory tract tumors were 9 and 1 % in the experimental and control groups, respectively. the present studies have shown that the most common type of focal lesions to develop in the lungs of tobacco smoke-exposed animals consisted of accumulated lymphocytes and macrophages in the vascular adventitia. similar accumulations were also found in the lamina propria of terminal bronchioles, where some of them were continuous with lesions surrounding the bronchial veins or branches of the pulmonary veins. while all of the focal lesions were found to include cellular infiltrates typical of the inflam"values are means â± sd. b significantly different from untreated controls (p<0.05). c animals were exposed for 30 mo, followed by 7 mo without treatment. matory response, the cell types found in the vascular adventitia were typically restricted to lymphocytes and macrophages. similar accumulations of lymphoreticular cells in perivascular locations have been noted in the normal course of aging in the rat (11) and in cases of multiple sclerosis in humans (12). although perivascular lesions were often contained within some of the more extensive lesions, it is not clear whether they played an essential role in the pathogenesis of the larger lesions. the larger lesions could have been induced by infiltration of lymphoreticular cells into the surrounding parenchyma or could have been initiated independently. since these locations were probably subjected to tobacco smoke exposure under similar local conditions, inflammatory responses could have resulted from the same, presumably chemotactic, biochemical intermediaries in both cases. however, the larger lesions showed the full spectrum of inflammatory cells, including polymorphonuclear leukocytes and mast cells. another feature common to the more extensive lesions was degradation of the basal lamina, particularly under the type i or squamous epithelial cells. we considered this alteration a possible contributing factor in fibrogenesis and/or epithelial hyperplasia. the proximity of phagocytes, particularly macrophages, to these sites suggested that enzymes released from the cells during phagocytosis may affect the structure of the lamina. the presence of lymphocytes, monocytes, and macrophages in the interstitium has also been reported in human diffuse interstitial lung diseases (13) . lesions of comparable structure to the type ii hyperplastic and peribronchiolar fibrotic lesions have been induced in many previous studies of lung pathology, but authors have tended to classify the cuboidal and columnar metaplastic lesions together. the exceptions that particularly note "bronchiolization" of the peribronchiolar alveoli have been reports on mice and hamsters infected with infll!enza virus (14), mice exposed to synthetic smog or calcium chromate dust (15) , and hamsters treated with chemical carcinogens (16) . in experiments on rats treated with various agents, particularly intratracheal instillation of tobacco smoke condensate (2) or of casein and carbon particulates (j 7), or a single exposure to benzo[a)pyrene followed by lifetime tobacco smoke inhalation (1), bronchiolization appeared to have occurred but to have been classified with other types of metaplasia. our studies, based on the improved structural detail obtained by the examination of tissues embedded in epoxy resins, suggest that the bronchiolar lesions differ in several respects from the more common cuboidal metaplasias, which were identified here as type ii hyperplasias. since only about half of the peribronchiolar lesions showed epithelial metaplasia, our studies are also the first performed on rodents to suggest that fibrotic and cellular enlargement of the peri bronchiolar septa precedes the replacement of the squamous, type i epithelium with a columnar epithelium. however, prominent areas of peribronchiolar fibrosis without columnar metaplasia have also been noted in the lungs of human smokers and of nonsmokers exposed to lung irritants (18). in the present studies, hyperplasia of the type ii epithelium appeared concurrently with changes in the intersti(ium. alveolar bronchiolization was rather infrequent and appeared to occur well after inflammatory and fibrotic changes in the interstitium. in addition, the two types of larger lesions differed in other respects: their locations were typically dissimilar, the type ii lesions being mainly at the pleura. more importantly, the frequency of the lesions was related to the duration of tobacco smoke exposure. increasing the time of exposure at the lower dose of tobacco smoke from 1 to 2 years led to approximately a tripling in the frequency of type ii hyperplasias but to a sixfold increase in the frequency of peribronchiolar lesions. while exposure to 10 cigarettes/day for 1.5 years induced as many type ii hyperplasias as the 2-year exposure to 7 cigarettes/day, it induced far fewer peri bronchiolar lesions. thus the peribronchiolar lesions were dependent on the duration of exposure and/or on the age of the exposed animals. in summary, the rat inhalation model offers a prototype of human syndromes induced by tobacco smoke exposure. however, the exposure level required for induction of emphysematous changes also leads to high mortality. the ultrastructure of the lesions appears to implicate the inflammatory response in their pathogenesis. the least common lesion seen, fibrosis of the peribronchiolar alveoli, is temporally related to tumor incidence and can be considered a precursor lesion. . note that several of the lymphatic endothelial cells contain aggregated smoke particulates (arrows). animal was exposed to 7 cigarettes/day for 2 yr. bar = 10 /lm. x 1,500 . animals were exposed to 7 cigarettes/day for 2 yr. bar = 100 /lm. x 170 figure 5.-small pleural type ii hyperplastic lesion. sa) type ii hyperplasia distal to terminal bronchiole. bar = 500 /lm. x 25. 5b) pulmonary vein with lymphoreticular cell accumulations (arrows) apical to type ii hyperplastic lesion. bar = 500 /lm. x 25. 5c) high-magnification view of the epithelium, showing type ii cells (arrows). animal was exposed to 7 cigarettes/day for 2 yr. toluidine blue. bar = 10 /lm. x 860 figure 6.-minimal septal enlargement at the periphery of a peribronchiolar fibrotic lesion. plasma cells (p), lymphocytes (l), and hypertrophic fibroblasts (f) are present in interstitium. collagenous thickenings (c) are also found at irregular intervals within alveolar septa. thickening (arrows) and reduplication (double arrows) of basal lamina underlying the epithelium were also found. most capillaries contained a hypertrophied endothelium (e), which frequently occluded the lumen completely. a few hypertrophic type ii cells (ii) were present. bar = 10 /lm. x 1,600. inset: higher magnification view of occluded capillary at top of micrograph (e) with an adjacent plasma cell (p). capillary lumen is marked by arrowheads. note extensive infolding of basal lamina (double arrows). animal was exposed to 7 cigarettes/day for 2 yr. bar = 3 /lm. x 3,400 figure 7.-portion of a peri bronchiolar fibrotic lesion that contains fibrotic septa showing collagenous thickenings (c), a fibroblast containing osmiophilic granules (f), and capillaries in which the endothelium appears to be degenerating (d). animal was exposed to 7 cigarettes/day for 2 yr. bar = /lm. x 1,700 figure s.-portion of a type ii hyperplastic lesion showing cuboidal epithelial cells with exceptionally clear cytoplasm and secretory inclusions (se) and collagenous areas in the interstitium (c). most of the cells comprising the cuboidal population are type ii cells (ii). degradation of the basal lamina was extensive, leading to detachment of type i epithelial cells from the septum in some areas (arrows). animal was exposed to 7 cigarettes/day for 2 yr. bar = 10 mm. x 1,600 figure 9.-type ii hyperplastic lesion showing cuboidal and squamous (s) epithelial cells. a columnar cell with extensive endoplasmic reticulum represented a third type of epithelial cell (iii). basal lamina underlying the epithelium is degraded in several areas (arrows). lymphocytes (l) are present in both epithelium and interstitium. interstitium also contains plasma cells (p), mast cells (m), macrophages with ingested particulate matter, and extensive areas filled with collagen fibers (c). hypertrophic fibroblasts (f), were present. nearly all capillary endothelial cells (e) were hypertrophied and occluded the capillary lumen. profiles of linearly oriented acellular structures adjoined macrophages in the air space (a). animal was exposed to 10 cigarettes/day for 1.5 yr. bar = 10 /lm. x 1,800 figure 1o.-portion of a type ii hyperplastic lesion containing cuboidal cells (iii) that showed numerous profiles of endoplasmic reticulum and densely osmiophilic granules in the cytoplasm. basal lamina also was reduplicated (arrows). animal was exposed to 7 cigarettes/day for 2 yr. bar = 5 /lm. x 2,300 response of rat lung to inhaled tobacco smoke with or without prior exposure to 3,4-benzpyrene (bpl given by intratracheal instillation it administered repeatedly by intratracheal instillation inhalation toxicity studies on cigarette smoke. vi. 6-week comparative experiments using modified flue-cured cigarettes: histopathology of the lung electron microscopic observations on pulmonary fibrosis and emphysema in smoking dogs alveolar cell hyperplasia in the lungs of smoking dogs effects of chronic inhalation of whole fresh cigarette smoke and of its gas phase on pulmonary tumorigenesis in snell's mice chronic inhalation of cigarette smoke by f344 rats the laboratory diagnosis of mycoplasma infectioll rapid and improved methods for embedding tissues in epon 812 and araldite 502 the use of lead citrate at high ph as an electronopaque stain in electron microscopy pathology of aging rats multiple sclerosis: presence of lymphatic capillaries alld lymphoid tissue in the brain and spinal cord analysis of airspace and interstitial mononuclear cell populations in human diffuse inlerstitiallung disease histology and ultrastructure of metaplasia of alveolar epithelium following infection of mice and hamsters with influenza virus morphogenesis of alveolar bronchiolization morphology of experimentally induced respiratory tumors in syrian golden hamster response of rat lung to 3,4-benzyprene administered by intratracheal instillation in infusine with or without carbon black pathological changes in the peripheral airways of young cigarette smokers animal was exposed to 10 cigarettes/day for 1.5 yr. bar = 200 j.lm. ib) perivascular lesion (arrow) associated with a small venule near the alveolar duct (ad) key: cord-299756-m0va36er authors: raaben, matthijs; groot koerkamp, marian ja; rottier, peter jm; de haan, cornelis am title: type i interferon receptor-independent and -dependent host transcriptional responses to mouse hepatitis coronavirus infection in vivo date: 2009-08-03 journal: bmc genomics doi: 10.1186/1471-2164-10-350 sha: doc_id: 299756 cord_uid: m0va36er background: the role of type i ifns in protecting against coronavirus (cov) infections is not fully understood. while covs are poor inducers of type i ifns in tissue culture, several studies have demonstrated the importance of the type i ifn response in controlling mhv infection in animals. the protective effectors against mhv infection are, however, still unknown. results: in order to get more insight into the antiviral gene expression induced in the brains of mhv-infected mice, we performed whole-genome expression profiling. three different mouse strains, differing in their susceptibility to infection with mhv, were used. in balb/c mice, which display high viral loads but are able to control the infection, 57 and 121 genes were significantly differentially expressed (≥ 1.5 fold change) upon infection at 2 and 5 days post infection, respectively. functional association network analyses demonstrated a strong type i ifn response, with irf1 and irf7 as the central players. at 5 days post infection, a type ii ifn response also becomes apparent. both the type i and ii ifn response, which were more pronounced in mice with a higher viral load, were not observed in 129svev mice, which are much less susceptible to infection with mhv. 129svev mice lacking the type i interferon receptor (ifnar-/-), however, were not able to control the infection. gene expression profiling of these mice identified type i ifn-independent responses to infection, with ifn-γ as the central player. as the balb/c and the ifnar-/129svev mice demonstrated very similar viral loads in their brains, we also compared their gene expression profiles upon infection with mhv in order to identify type i ifn-dependent transcriptional responses. many known ifn-inducible genes were detected, several of which have previously been shown to play an important protective role against virus infections. we speculate that the additional type i ifn-dependent genes that we discovered may also be important for protection against mhv infection. conclusion: transcriptional profiling of mice infected with mhv demonstrated the induction of a robust ifn response, which correlated with the viral load. profiling of ifnar-/mice allowed us to identify type i ifn-independent and -dependent responses. overall, this study broadens our present knowledge of the type i and ii ifn-mediated effector responses during cov infection in vivo. cytokines are key regulators that dictate many aspects of innate and adaptive immunity. induction of type i interferons (ifns), a well-known subset of cytokines with antiviral activity, is triggered by a selection of cellular pattern recognition receptors, including tlrs (toll-like receptors), rig-i (retinoic acid-inducible gene i), and mda5 (melanoma differentiation-associated protein 5). these receptors are activated in response to a range of pathogenspecific factors, which includes double-stranded rna produced during virus infection [1, 2] . secreted type i ifns (i.e. ifn-α and ifn-β), subsequently induce an antiviral transcription program in the infected cell as well as in adjacent cells, thereby magnifying the "danger" signal and protecting against the infection. the role of type i ifns in controlling coronavirus (cov) infections is not well understood. a number of studies has shown that covs, like the mouse hepatitis virus (mhv) and the severe acute respiratory syndrome (sars)-cov, are poor inducers of type i ifns in cell culture, and even escape from detection by cytoplasmic pattern recognition receptors [3] [4] [5] [6] [7] [8] . consistently, virus-encoded ifn antagonistic functions have been described for both mhv and sars-cov [9, 10] . in vivo, however, mhv infection appeared to induce the production of ifn-α in plasmacytoid dendritic cells (pdcs) by a tlr7-dependent mechanism [11] . moreover, mhv infections of primary neuronal cultures and of the central nervous system (cns) induced ifn-β gene expression, indicating that the production of type i ifns in vivo is not limited to pdcs [12, 13] . furthermore, neuronal cultures infected with mhv exhibited increased expression of several type i ifninduced transcription factors [14] . more recently, roth-cross and co-workers reported that macrophages and macrophage-like microglia cells produce ifn-β in the cns of mhv-infected mice in a mda5-dependent manner [15] . several studies have demonstrated the importance of the type i ifn response in controlling mhv infection in vivo. the exogenous delivery of type i ifns was shown to inhibit mhv infection of and spread to the mouse brain [16, 17] . consistently, infection of mice lacking the functional type i ifn receptor (ifnar-/-) with mhv resulted in increased viral replication and extended tissue tropism [11, 17, 18] . although many type i ifn-responsive genes have been identified [19] , the protective effectors against mhv infection are yet unknown [20] . in order to get more insight into the antiviral gene expression induced in the brains of mhv-infected mice, we performed whole-genome expression profiling. three different mouse strains (balb/c, 129svev and ifnar-/-129svev mice), differing in their susceptibility to infec-tion with mhv, were used. previously, we have observed that 129svev mice are significantly more resistant to infection via the intranasal route than balb/c mice [17] . the reason for the significant difference in susceptibility is not known, but may be related to different antiviral immune responses in these two mouse strains. furthermore, gene expression profiling of 129svev mice lacking the type i ifn receptor, which are not able to control the mhv infection [11] , allowed us to identify type i ifn-independent transcriptional responses. we started by comparing the whole-genome expression profiles in the brains of the balb/c and the 129svev mice upon infection with mhv. to this end, mice were inoculated intranasally with 10 6 tcid 50 of mhv strain a59 or with pbs (control). groups of mice (n = 4) were sacrificed at 2 and 5 days post inoculation after which the brains were harvested and total rna was isolated. the extent of virus replication was determined by quantitative reverse transcriptase (rt)-pcr targeting mhv-specific rna sequences as described earlier [21] . previously, we demonstrated that the viral rna load correlates well with viral infectivity in tissue homogenates [17] . while no viral rna could be detected yet at 2 days post inoculation (data not shown), viral rna was observed in the brain of both mouse strains at day 5 ( figure 1a ). as expected, the balb/ c mice displayed a much higher viral rna load than the 129svev mice. next, the rna extracts were processed for microarray analysis using the pbs-inoculated groups as the reference. in total, 57 and 121 genes were significantly differentially expressed (≥ 1.5 fold change) in balb/c mice at 2 and 5 days post infection, respectively. in contrast, in the 129svev mice, no significant induction of gene expression was observed. the results are depicted in figure 1b as a gene tree that was built based on the genes with a significantly altered expression level in balb/c mice at 5 days post infection (i.e. expression-based cluster analysis). from these data we were able to identify host genes, the increased expression (≥ 1.5 fold) of which could already be detected at day 2 (i.e. early genes; figure 1c ) or only at day 5 (i.e. late genes; figure 1d ). the group of earlyinduced transcripts contained many ifn-inducible genes, including the well-known interferon regulatory factor 7 (irf7), signal transducer and activator of transcription 1 (stat1), and 2'-5' oligoadenylate synthetase (oas) genes (additional file 1a). within the cluster of "late" genes (additional file 1b) several chemokines (i.e. ccl2, ccl5, ccl7, cxcl9, and cxcl10) could be identified. next, in order to construct a functional association network, we applied the string 8.0 software [22] to the list of proteins encoded by the "early" and "late" genes. we also included known interactors of our hits in this analysis, while proteins that did not demonstrate any known interactions were excluded for clarity. the results are shown in figure 2a and 2b. functional association network analysis of the proteins encoded by the "early" genes revealed two main modules. one module contained several proteins involved in antigen presentation, while the other module contained numerous proteins involved in the type i ifn response. the key player in this latter module appeared to be irf7, which is the master regulator of type i ifn-dependent responses [23] . functional association network analysis of the proteins encoded by the "late" genes revealed a large network of proteins involved in host-pathogen interactions. although the microarray analyses did not reveal the induction of ifn-γ gene expression itself, ifn-γ appeared at a central position in the network. in addition, the induction of a type i ifn response was also evident from this network as demonstrated by the presence of the transcription factors irf1 and irf8, both of which demonstrated elevated mrna levels upon mhv infection. in conclusion, these results demonstrate that mhv infection induces a robust ifn response both at 2 and 5 days post infection, in which the transcription factors irf7, irf1, and irf8 appear to be the key players. at 5 days post infection, a type ii ifn response also becomes apparent. to confirm and extend these observations, we next analyzed the induction of type i and ii ifn gene expression (i.e. ifn-α4 and ifn-β1, and ifn-γ, respectively) by using quantitative rt-pcr. in agreement with the microarray expression profiles, significant induction of these type i and ii ifns could only be detected in the mhv-infected balb/c animals ( figure 1e ). the observation that the balb/c mice, unlike the 129svev mice, exhibited abundant expression of ifn-responsive genes upon mhv infection appears counter intuitive as the 129svev mice are much more resistant to the infection than the balb/c mice. apparently, the resistance of 129svev mice to mhv infection is not controlled by a more robust ifn response. the reason for the observed difference in susceptibility between the different mouse strains after intranasal inoculation is not known. mhv-a59 was recently shown to replicate efficiently in the liver of 129svev mice after intraperitoneal inoculation [11] . interestingly, the resistance of 129svev mice after intranasal inoculation is not restricted to infection with mhv, as it was also observed for vesicular stomatitis virus [24] . the microarray expression profiles described above suggested that the induction of an ifn response correlates with the viral load within the brain. to confirm this, we examined the data of the individual balb/c mice at 5 days post infection in more detail. clearly, the animals with the highest viral loads (mouse 2 and 4; figure 3a ), also dis-played significantly higher levels of induction of type i and ii ifn expression ( figure 3b ). likewise, the amplitude of the gene expression profiles ( figure 3c and additional file 2) of the individual mice also correlated with the viral loads in the brain. these observations are in agreement with results obtained by the profiling of sars-covinfected macaques [25] . also in that study a positive correlation between virus load and the induction of gene expression was observed. a few genes (n = 6), including isg20, showed an inverse correlation with the viral load. we currently have no explanation for this observation as expression of isg20 is known to be induced by type i ifns [26, 27] . interestingly, isg20 has been shown to exhibit antiviral activity against other viruses [28, 29] . to study the role of type i ifn-independent and -dependent gene expression in the control of mhv infection in vivo in more detail, we next made use of the ifnar-/-mice [30] . these mice are highly susceptible to mhv infection as compared to the parental 129svev mice [11, 17] . indeed, when these mice were inoculated intranasally with 10 6 tcid 50 of mhv-a59, viral rna levels in their brains became much higher than in animals from the parental strain at 5 days post infection ( figure 4a ). interestingly, at this time point the viral rna levels in the ifnar-/-mice were comparable to those in the brains of the balb/c mice. however, efficient dissemination of the infection, resulting in high viral loads in the liver as determined by quantitative rt-pcr, was only observed in the ifnar-/-mice and not in the wild-type mice, which displayed viral rna levels just above background ( figure 4b ). thus, in agreement with previous studies, a type i ifn-dependent response is required to inhibit virus dissemination [11, 15] . whole-genome expression profiling of brains of the ifnar-/-mice revealed the significantly induced expression of 73 genes (≥ 1.5 fold) at 5 days post infection. in contrast, at day 2, hardly any alterations in gene expression could be detected in these knock-out mice (additional file 3). figure 4c shows an expression-based cluster analysis of these 73 genes for the wild-type and ifnar-/mice. comparison of the complete expression profiles of these mice revealed that the transcriptional profile at day 5 in the ifnar-/-mice has a larger similarity with the profile at day 2 of the parental 129svev mice than with that of the knock-out mice at day 2 post infection ( figure 4c ). this observation may suggest the presence of an early host response to infection with mhv in the parental mice, even though no significant induction (≥ 1.5 fold) of gene expression could be detected ( figure 1b) . such a response, may not be evident in transcriptional profiles of whole organs, but might only be apparent at the cellular level. we speculate that early decisive events are happening in initial target cell populations such as dcs and macro-early and late transcriptional responses to infection with mhv as the knock-out mice lack a functional type i ifn receptor, the upregulation of gene expression observed in these mice apparently occurs independently of type i ifn signalling. not much is known yet about type i ifn-independent responses to infection. the observation that the transcriptional upregulation of irf1 was independent of type i ifn signalling is consistent with the notion that ifn-γ can also induce expression of this gene [32,33]. the type i ifn receptor-independent expression profile within the brains of ifnar-/-mice after mhv infection likewise, we also observed increased transcription of ifitm1 and ifitm3 independent of type i ifn signalling, again corresponding with the literature [34, 35] . interestingly, the expression of various genes encoding proteins involved in antigen presentation (i.e. h2, b2m, psmb8, psmb9, and ctss) was also increased in the absence of type i ifn signalling. psmb8 and psmb9 encode immunoproteasome subunits which facilitate antigen presentation to cd8 + t cells after virus infection, a process that is primarily regulated by ifn-γ [36] . furthermore, also the expression of the major histocompatibility complex class ii (mhc ii) invariant chain, also called cd74 [37], was increased upon infection of the knock-out mice. these data are in agreement with the observation that the induction of genes involved in antigen processing is independent of stat1 activation by . we also observed the transcriptional upregulation of the 3 isoforms of metallothionein (mt1, mt2, and mt3), which encode proteins known to scavenge toxic metals [39] . the induction of these genes, which was not apparent in either wild-type mice, could reflect an acute-phase reaction in the brain of mhv-infected ifnar-/-mice, which likely contributes to pathogenesis as has been shown for other viruses [40-42]. we constructed a functional association network by applying the string 8.0 software [22] to the list of proteins encoded by the type i ifn-independent genes (additional file 3). we also included known interactors of our hits in this analysis, while proteins that did not demonstrate any interactions were again excluded for clarity. the result is shown in figure 5 . the analysis revealed ifn-γ as the central player in the type i ifn-independent antiviral network as this protein appeared to link a number of smaller modules. the induction of ifn-γ gene expression could be confirmed using quantitative rt-pcr (data not shown). the finding that ifn-γ-mediated transcriptional responses are not dramatically affected in the absence of type i ifn signalling is in agreement with reports referred to above and with a recent publication by ireland et al. [18] , which shows that ifn-γ expression is significantly induced in the cns of mhv-infected ifnar-/-mice. while the production of ifn-γ by nk cells plays a major role in the protection against infection with mhv [43-47], the ifn-γ-mediated transcriptional responses that we observed were not protective against acute mhv infection in the ifnar-/-mice. several studies have shown that mhv [11, 15, 17] as well as several other viruses [48-50] replicate to much higher levels (up to 10 5 fold difference) in ifnar-/-mice than in their wild-type counterparts. in this study we show that a strong correlation exists between the amplitude of type i and ii ifn host responses with the viral load. the huge differences in virus replication between wild-type and ifnar-/-mice therefore do not permit a fair comparison between gene expression profiles of these mice, with the aim of identifying type i ifn-dependent responses. indeed, as no significant gene expression is observed in the wild-type 129svev mice, a comparison with the expression profile of the ifnar-/-mice only provides information about type i ifn-independent and not ifndependent responses. we now observe, in agreement with our previous study, that the brain of balb/c and ifnar-/ -129svev mice contain very similar mhv loads at day 2 and 5 post infection [17] . since the type i ifn-responsive pathway is very well conserved among many different species [51], we considered it acceptable to compare the gene expression profiles of these mice with the aim of identifying type-i ifn-dependent responses, although comparing transcriptional profiles of wild-type and ifnar-/-mice from a different genetic background should obviously be done very cautiously. ideally, a comparison between wildtype balb/c and ifnar-/-balb/c mice would have been more accurate. while the induced expression of a number of genes was similar for the two mouse strains (i.e. type i ifn signalling-independent gene-expression), that of other genes was only observed in the balb/c mice (i.e. tentative type i ifn signalling-dependent gene expression). the expression of yet other genes appeared to be partially dependent of type i ifn signalling: increased expression of these genes was observed in the ifnar-/mice, but much more so in the balb/c mice. genes, the expression of which was upregulated (≥ 1.5 fold) in the balb/c mice but not significantly changed in the ifnar-/-mice upon infection with mhv, were tentatively designated as type i ifn-dependent. genes, the transcriptional upregulation of which was at least 2 times higher in the balb/c mice than in the ifnar-/-mice, were also added to the list of tentative type i ifn-dependent genes. as expected, this set of genes (n = 82) contained many known ifn-responsive genes like isg20, ifit1, ifit3, isgf3g, mx2 and ube1l (additional file 4). functional association network analyses showed irf1 and irf7 to be the key players in the network (additional file 5). several of the tentative type i ifn-dependent genes (including mx2 and ube1l) have previously been shown to play an important protective role against virus infections [52-56]. we speculate that other genes present in this list may also be important for full protection against mhv infection. transcriptional profiling of mice infected with mhv demonstrated the induction of a robust ifn response, which correlated with the viral load. profiling of ifnar-/-mice allowed us to identify type i ifn-independent anddependent responses. overall, this study broadens our present knowledge of the type i ifn-mediated effector responses during cov infection in vivo. [6] [7] [8] week old balb/c were obtained from charles river laboratories, while type i ifn receptor knock-out mice (ifnar-/-) [30] and the parental 129svev mice were obtained from b&k universal ltd. mice were inoculated intranasally with 10 6 tcid 50 of mhv strain a59 and sacrificed at the indicated time-points for organ dissection. control animals were treated with pbs. the study proto-col was approved by the animal ethics committee of the utrecht university, and all experiments were performed in accordance with accepted institutional and governmental policies. whole brains and livers were dissected from the mhvinfected and control mice. the tissues were added to lysing matrix d tubes (mp biomedical), containing 1 ml of the type i ifn-independent gene expression network figure 5 the type i ifn-independent gene expression network. the genes listed in additional file 3 (n = 73) were subjected to functional association network analysis by using the string 8.0 database as described in the legend of figure 2 . the key player in the network, ifn-γ, is indicated in red. rnapro™ solution (q-biogene), and processed using a fastprep instrument (mp biomedical). the tissues were homogenized at 6,000 rpm for 40 sec and immediately placed on ice. subsequently, the homogenates were centrifuged at 14,000 rpm for 10 minutes at 4°c and supernatants were harvested and stored at -80°c. total rna was isolated from the homogenates using the trizol reagent (invitrogen) according to the manufacturer's protocol. rna was further purified using the rneasy mini-kit with subsequent dnasei treatment on the column (qiagen). rna integrity was determined by spectrometry and by a microfluidics-based platform using a uv-mini1240 device (shimadzu) and a 2100 bioanalyzer (agilent technologies), respectively. 3], respectively), were measured by quantitative pcr using assay-on-demand reagents and equipment (pe applied biosystems), according to the manufacturer's instructions. the quantitative pcr reactions were performed in a total reaction volume of 20 μl containing 10 μl taqman ® universal pcr master mix (2×), 5 μl cdna, 1 μl taqman ® gene expression assay mix (20×), and 4 μl water using an abi prism 7000 sequence detection system under the following conditions: 95°c for 10 mins, followed by 40 cycles of 95°c for 15 secs and 60°c for 1 min. for all assays, we performed "no-rt" (reaction using total rna as the substrate) and "no template" (reaction using water as the substrate) controls. in both cases, omitting cdna from the reaction resulted in a lack of pcr product generation. all assays were analyzed with abi prism 7000 software v1.2.3f2 (pe applied biosystems). the comparative ctmethod was used to determine the fold change for each gene (primer efficiencies were similar for both the endogenous control primer set and genes of interest primer sets [data not shown]). note that the ct values of all samples were within the limits of the standard curves (data not shown). the housekeeping gene gapdh (nm_008084.2) was used as a reference in all experiments, since expression of this gene was found constant among samples. the amounts of viral rna were determined by quantitative rt-pcr as described before [21] . the microarray experiments were performed as described previously [5] . briefly, mrna was amplified from 1 μg of total rna by cdna synthesis with oligo(dt) doubleanchored primers, followed by in vitro transcription using a t7 rna polymerase kit (ambion). during transcription, 5-(3-aminoallyl)-utp was incorporated into the single stranded crna. cy3 and cy5 nhs-esters (amersham biosciences) were coupled to 2 μg crna. rna quality was monitored after each successive step using the equipment described above. corning ultragaps slides, printed with a mouse array-ready oligo set (operon; 35,000 spots), were hybridized with 1 μg of each alternatively labeled crna target at 42°c for 16-20 h. two independent dyeswap hybridizations (4 arrays) were performed for each experimental group. after hybridization the slides were washed extensively and scanned using the agilent g2565aa dna microarray scanner. after data extraction using imagene 5.6 software (biodiscovery), lowess normalization [57] was performed on mean spot-intensities in order to correct for dye and printtip biases [58] . the microarray data was analysed using anova (r version 2.2.1/maanova version 0.98-7) http://www.r-project.org [59] . briefly, in a fixed effect analysis, sample, array and dye effects were modelled. pvalues were determined by a permutation f2-test, in which residuals were shuffled 5,000 times globally. genes with p < 0.05 after family wise error correction were considered significantly changed. cluster analysis (standard correlation) was performed with genespring gx 7.2 software (silicon genetics). when indicated, the confidence level was increased by applying a fold change cut-off. the resulting genelists were subjected to genespring 7.2 software for further analysis. arrayexpress accession numbers miame-compliant data in mage-ml format as well as complete descriptions of protocols have been submitted to the public microarray database arrayexpress http:// www.ebi.ac.uk/arrayexpress/ with the following accession numbers: microarray layout, p-umcu-8; gene expression data of mhv-infected mice, e-mexp-2081; protocols for total rna isolation and mrna amplification, p-mexp-34397; crna labeling, p-mexp-34400 and p-mexp-35534; hybridization and washing of slides, p-mexp-34401; scanning of slides, p-mexp-34430; data normalization, p-mexp-34431. innate immune recognition of viral infection type i interferons in host defense group 2 coronaviruses prevent immediate early interferon induction by protection of viral rna from host cell recognition transcriptional profiling of acute cytopathic murine hepatitis virus infection in fibroblast-like cells mouse hepatitis coronavirus replication induces host translational shutoff and mrna decay, with concomitant formation of stress granules and processing bodies preferential infection of mature dendritic cells by mouse hepatitis virus strain jhm mouse hepatitis virus does not induce beta interferon synthesis and does not inhibit its induction by double-stranded rna inhibition of beta interferon induction by severe acute respiratory syndrome coronavirus suggests a two-step model for activation of interferon regulatory factor 3 mouse hepatitis coronavirus a59 nucleocapsid protein is a type i interferon antagonist severe acute respiratory syndrome coronavirus nsp1 suppresses host gene expression, including that of type i interferon, in infected cells control of coronavirus infection through plasmacytoid dendritic-cell-derived type i interferon differential regulation of innate and adaptive immune responses in viral encephalitis inhibition of the alpha/beta interferon response by mouse hepatitis virus at multiple levels viral induction of central nervous system innate immune responses murine coronavirus mouse hepatitis virus is recognized by mda5 and induces type i interferon in brain macrophages/microglia protective effect of recombinant murine interferon beta against mouse hepatitis virus infection non-invasive imaging of mouse hepatitis coronavirus infection reveals determinants of viral replication and spread in vivo type i interferons are essential in controlling neurotropic coronavirus infection irrespective of functional cd8 t cells interferome: the database of interferon regulated genes interferon and cytokine responses to sarscoronavirus infection cyclooxygenase activity is important for efficient replication of mouse hepatitis virus at an early stage of infection this work was supported by grants from the m.w. beijerinck virology fund, royal netherlands academy of arts and sciences, and the netherlands organization for scientific research (nwo-vidi-700.54.421) to c.a.m. de haan. we thank connie bergmann for advice and monique oostra, marne hagemeijer, and mijke vogels for stimulating discussions. the authors declare that they have no competing interests. mr and mjagk conducted all the experiments. mr wrote the manuscript. pjmr and camdeh coordinated the research efforts and assisted with writing the manuscript. all authors read and approved the final manuscript. key: cord-001124-qcjbtflt authors: carrero, javier antonio title: confounding roles for type i interferons during bacterial and viral pathogenesis date: 2013-10-24 journal: international immunology doi: 10.1093/intimm/dxt050 sha: doc_id: 1124 cord_uid: qcjbtflt although type i interferons (ifn-i) were initially defined as potent antiviral agents, they can also cause decreased host resistance to some bacterial and viral infections. the many antiviral functions of the ifn-i include direct suppression of viral replication and activation of the immune response against viruses. in addition to their antiviral effects, ifn-i are also protective against several extracellular bacterial infections, in part, by promoting the induction of tnf-α and nitric oxide. in contrast, there is a negative effect of ifn-i on host resistance during chronic infection with lymphocytic choriomeningitis virus (lcmv) and acute infections with intracellular bacteria. in the case of lcmv, chronic ifn-i signaling induces adaptive immune system suppression. blockade of ifn-i signaling removes the suppression and allows cd4 t-celland ifn-γ-mediated resolution of the infection. during acute intracellular bacterial infection, ifn-i suppress innate immunity by at least two defined mechanisms. during francisella infection, ifn-i prevent il-17 upregulation on γδ t cells and neutrophil recruitment. following listeria infection, ifn-i promote the cell death of macrophages and lymphocytes, which leads to innate immune suppression. these divergent findings for the role of ifn-i on pathogen control emphasize the complexity of the interferons system and force more mechanistic evaluation of its role in pathogenesis. this review evaluates ifn-i during infection with an emphasis on work carried out ifn-i-receptor-deficient mice. the type i interferons (ifn-i) are an extensive family of pleiotropic cytokines that all signal through the ubiquitously expressed ifn-i receptor, termed the 'ifn-α receptor' (ifnar) (1) . the activity of these cytokines was discovered in the 1950s because of their ability to 'interfere' with viral infection (2) . molecular cloning techniques and genome sequencing have led to the identification of an extensive number of members of the ifn-i family. in mice, the two best analyzed members of this family are the cluster of 13 ifn-α subtypes and 1 ifn-β molecule. genetic ablation of ifnar (ifnar -/-) in the mouse is sufficient to prevent signaling by all members of the ifn-i family and is the biologically defining activity that groups the ifn-i molecules into one family (1) . ifnar is composed of two chains (ifnar1 and ifnar2) that coordinately activate the kinases jak1 and tyk2 (tyrosine kinase 2) upon ifn-i binding. jak1 (janus kinase 1) and tyk2 phosphorylate stat1 and stat2 that, together with interferon regulatory factor 9 (irf9), form the interferon-stimulated gene factor 3 (isgf3) complex (3) . isgf3 binds to interferonstimulated response elements to cause upregulation of over 300 genes. the type ii interferon receptor, ifngr1-ifngr2, which binds ifn-γ, the only type ii interferon, activates jak1 and jak2, leading to stat1 phosphorylation and homodimerization (4) . because of the similarities in signaling, many of the genes that are upregulated by ifn-i are also upregulated by ifn-γ, providing some degree of redundancy between the ifn-i and ifn-γ signaling pathways (5) . however, there are a large number of genes unique to ifn-i. although many of the ifn-i-specific genes have defined antiviral functions, the role of many remains unresolved. the antiviral activity of ifn-i was initially defined with conditioned supernatant inhibition of viral growth and then with purified cytokines. however, it was the generation of mice deficient in ifnar signaling that permitted examination of infections under more physiological conditions (6) . this review will focus on the role of ifn-i during murine infection with viral and bacterial pathogens. there is also extensive work on the role ifn-i in the pathogenesis of autoimmunity and cancer, and more recently, in fungal and protozoan infections (7) (8) (9) . although this work has contributed to our understanding of the biological activities of ifn-i, it is beyond the scope of this review. because of the extent of the ifn-i literature, this review will mostly limit itself to experiments that have examined viral and bacterial pathogenesis in ifnar -/mice with a particular emphasis on work that has examined lethality and pathogen burden. four major themes will be covered: first, there is a broad summary of the (generally) protective role of ifn-i in mice infected with viruses. second is the recent finding that ifn-i promote the suppression of adaptive immunity seen during chronic infection with lymphocytic choriomeningitis virus (lcmv). third, there is an examination of the divergent results that have been obtained using different bacterial pathogens. finally, there is a detailed examination of the role of ifn-i during listeria monocytogenes infection. the consensus in the field is that ifnar signaling is protective against most types of viral infection. table 1 summarizes some of the results obtained after infecting wild-type and ifnar -/mice with multiple species and strains of viruses. in most cases, the absence of systemic ifnar signaling by the mouse led to an increase in viral titer, lethality, or both compared with controls. ifn-i is important in handling all major genetic classes of viruses including single-stranded rna (ssrna; +/-stranded), double-stranded rna and double-stranded dna viruses, and acute retroviruses (ssrna-rt). the two exceptions to the strict requirement for ifnar are influenza and dengue virus infections. in the case of influenza and potentially other respiratory viruses, the type iii interferon system (which comprises ifn-λ subtypes and signals using il-10r2-ifnlr1) plays a dominant role in restricting acute epithelial cell infection, thereby limiting the requirement of ifn-i signaling (10, 11) . in dengue, ifnγ-mediated protection is dominant over ifn-i, although the combined ifnar -/-× ifngr -/mice are more susceptible than the ifngr -/mice (12) . the effects of ifn-i that limit viral infection are extensive, but several aspects are important to consider. ifn-i signaling enhances the susceptibility of virally infected cells to undergo programmed cell death, thereby limiting viral replication (4, 23) . dendritic cells (dcs) exposed to ifn-i become activated and secrete proinflammatory cytokines that lead to activation of the adaptive immune response (1) . nk cells become potent killers of virally infected cells after exposure to ifn-i (24, 25) . ifn-i has direct effects on adaptive αβ t cells and sensitizes them to activation via the tcr (26, 27) . ifn-i production by plasmacytoid dcs promotes b-cell activation and production of antiviral antibody (28, 29) . in general, these effects of ifn-i signaling are beneficial to the host, as they lead to control of viral replication and spread. the importance of host ifn-i signaling is further reinforced by viral evolution. viruses have evolved extensive immune-evasion strategies many of which center around inhibition of the host ifn-i response (30, 31) . however, the biological responses to ifn-i do not always lead to beneficial outcomes to the host. in the case of viral infections, the best studied example of the negative role of ifn-i are chronic viral infections, in particular infection with lcmv. a long-standing finding in the lcmv field is that small genetic changes can convert an acutely infective strain of lcmv (armstrong 53b) into a chronically infective strain (armstrong 53b clone 13; cl13) (32) . several hallmarks of the negative effects of chronic viral infection have been discovered using this system. mice become chronically infected with lcmv because of t-cell 'exhaustion' that prevents normal clearance (33) . several factors have been implicated in the suppression of t-cellmediated clearance of chronic lcmv; most salient among them are il-10 and pd-1 (programmed cell death 1). il-10 is known to antagonize inflammatory activation on multiple immune cell types and its neutralization prevents chronic infection with lcmv (34) . pd-1, a member of the cd28/ctla4 family of t-cell regulators, is upregulated on exhausted t cells found in chronically infected mice. its ligands, pd-1l and pd-2l, are broadly expressed and inducible by interferons (35) . the interaction of pd-1 with pd-l1 acts to limit t-cell activity during chronic infection. blockade of the pd-1-pd-l1 interaction using mabs derepresses cd8 t-cell activity and leads to enhanced adaptive immune responses to lcmv infection (36) . in two recent publications, the effects of il-10 and pd-1 in limiting the response to lcmv infection have been causally linked to ifn-i signaling (37, 38) . during the initial stages of infection with cl13, the absence of ifn-i signaling allows for an increased viral titer and delayed clearance during the acute phase of the response (6, 18) . wild-type mice control the primary infection well but become chronic carriers. ifnar -/mice also become chronic carriers albeit at higher viral loads. the cl13 strain induces higher levels of ifn-α and ifn-β than the acutely infective armstrong strain (37) . the major early producer of ifn-i are plasmacytoid dcs that are infected with the virus (37) . the presence of ifn-i is associated with a prolonged signature of interferon-inducible genes in spleen cells (38) . despite having higher early titers of lcmv, ifnar -/mice show reduced il-10 in serum and reduced pd-l1 expression on myeloid cells. in wild-type mice, blockade of ifnar signaling with neutralizing mabs replicates this effect, leading to reduction of il-10 and pd-l1. furthermore, neutralization of ifnar after the establishment of chronic infection leads to reduced viral burden (37) . therefore, ifnar plays a major role in the establishment of chronic infection with lcmv and neutralization of ifnar has therapeutic potential for patients harboring chronic viral infections. the response of ifnar -/mice to bacterial infections varies depending on the species and route of infection. table 2 summarizes some of the findings of ifnar -/mice infected with several important pathogenic bacteria. in streptococcus, escherichia coli, and helicobacter infections, ifnar -/mice have higher titers and/or lethality than wild-type controls. during brucella, francisella, salmonella, chlamydia, mycobacterium, or yersinia infections, ifnar -/mice control infection better than wild-type. the ifnar -/mice are more resistant to l. monocytogenes given systemically. a recent report has shown that during oral infection with listeria, ifnar signaling may be protective. based on these initial studies, the simplest conclusion is that ifnar signaling is beneficial during extracellular bacterial infection and detrimental during intracellular bacterial infection. type i ifn signaling provides increased protection during streptoccocus infection by promoting upregulation of tnf-α, ifn-γ and nitric oxide (49) . this is associated with restriction of bacterial growth. ifnar -/mice have bacteremia, increased systemic titers, and decreased survival. in vitro, streptococcus spp. induce ifn-β production through cell-type-specific signaling pathways (52) . strepcococcus can trigger ifn-i via the complex of irf3, stimulator of interferon genes (sting) and tank-binding kinase 1 (tbk1). in streptococcus-infected macrophages, ifn-β is induced through the irf3-sting-tbk1 complex and this is partially dependent on myd88 (ifn-i can also be produced in a myd88-independent pathway). in contrast, streptococcusinfected dcs induce ifn-β through irf5 and myd88. more mechanistic studies are still required to resolve the molecular triggers and in vivo cellular sources of ifn-i during streptoccocus infection. helicobacter pylori-infected ifnar -/mice have higher titers, but the mechanism of ifn-i action in this infection remains unresolved (50) . further work needs to be done on the extracellular bacterial infections to determine how ifn-i is protective and what distinguishes ifn-i from ifn-ii in these types of infections. following brucella infection, there is ifnar-dependent upregulation of tnf-related apoptosis-inducing ligand (trail) and splenic apoptosis that is associated with increased susceptibility to infection (39) . ifnar -/mice also express more ifn-γ and nitric oxide. in the case of salmonella enterica and chlamydia muridarum, ifn-i signaling sensitizes the infected macrophage to undergo cell death (47, 40) . prevention of macrophage cell death during s. enterica infection led to decreased bacterial titer. ifnar −/− mice infected with francisella have decreased titers and lethality compared with controls. this is attributed to the inhibitory effect of ifn-i signaling on il-17a/f expression (41) . ifnar -/mice express more il-17a/f, have an expansion of il-17 + γδ t cells and increased neutrophils at the site of infection. finally, treatment with ifn-i agonists such as poly(i:c) also promotes negative outcomes during bacterial infection. in the case of mycobacterium tuberculosis, intranasal delivery of poly(i:c) throughout the course of infection led to increased inflammatory infiltrates and necrosis of lung tissue that was dependent of ifnar signaling (53) . similar detrimental effects of poly(i:c) treatment are also seen following streptoccocus pneumoniae, staphylococcus aureus and l. monocytogenes infections (54) (see below). the first example of the detrimental effect of ifn-i during bacterial infection was discovered following l. monocytogenes infection. to date, it remains the best examined system, yielding information on the mechanisms of ifn-i induction, cellular sources and targets of ifn-i, and the nature of biological outcomes. macrophages infected with l. monocytogenes induce expression of ifn-i that is dependent on bacterial expression of the pore-forming toxin listeriolysin o (llo) (55, 56) . llo is important for the bacterial egress from the nascent phagosome to the cytosol (57) . llo alone does not induce strong levels of ifn-i production by the infected macrophage, suggesting that the presence of cytosolic bacteria is the driver of ifn-i production (56) . this is reinforced by experiments demonstrating that bacillus subtilis expressing llo gain access to the cytosol and also strongly induce ifn-responsive genes. the major molecular driver of ifn-i induction by l. monocytogenes is the cyclic dinucleotide c-di-amp (58) . the cyclic dinucleotides were initially discovered in bacteria as a second messenger system that also doubles as a pathogen-associated molecular pattern (59) . interestingly, c-di-amp is actively exported from the bacteria and the induced expression of a c-di-amp synthesizing enzyme (di-adenylate cyclase) increases ifnb1 gene expression by infected macrophages (58) . a sensor for cyclic dinucleotides has been identified as the helicase ddx41, which recruits sting, tbk1 and irf3 (see above) to drive upregulation of ifn-i genes (60) . splenic macrophages (cd11b + cd11c -pdca1 -b220 -) and tnf/inos-producing dcs (tip-dcs; cd11b + cd11c + ly6c + ) produce ifn-i following l. monocytogenes infection in vivo (61, 62) . mice lacking ccr2 expression, which do not recruit tip-dcs to the spleen, have reduced expression of ifn-α following l. monocytogenes infection (63) . to date, there is no clear demonstration that a l. monocytogenes-infected myeloid cell population is producing ifn-i in vivo. on the basis of experiments using immunofluorescent colocalization, tip-dcs appear not to be infected (62) . the work that identified ifn-i production by splenic macrophages did not evaluate the infected status of the cells (61) . therefore, at this time, the connection between the molecular mechanisms of induction and in vivo cellular sources of ifn-i cannot be definitely established. listeria monocytogenes causes apoptotic cell death of macrophages that is enhanced by ifnar signaling. within 2 h of infection, bone marrow-derived macrophages upregulate ifn-β and phosphorylate stat1 (64) . deletion of ifnar on macrophages raises their resistance to l. monocytogenesmediated killing significantly. the death induced by l. monocytogenes is dependent on bacterial expression of llo (64) . since llo is essential for virulence, it is unclear if it has a direct role in killing the infected macrophage or is only important for allowing egress of the bacteria to the cytosol. ifnar-dependent macrophage death is also found following infection of mice with l. monocytogenes (43) . a population of tnf-α-producing cd11b + macrophages is depleted following infection of wild-type mice. this population is maintained in ifnar -/mice, demonstrating a role for ifn-i in sensitization of macrophage death. it is not known at this time if the macrophages that die in vivo are infected by the bacteria. the most profound ifnar-dependent effect seen in mice infected with l. monocytogenes is the extensive depletion of white-pulp lymphocytes via apoptotic cell death (42) . in wildtype mice, apoptosis begins in the periarteriolar lymphoid sheath (t-cell area) and extends to the entire white pulp in a dose-dependent manner (65) . removal of ifnar significantly limits the number of apoptotic profiles and the extent of apoptotic death in any given white pulp (42) . treatment of t cells with ifn-α sensitizes them to llo-induced apoptosis suggesting that secreted llo may be a killer molecule in vivo (42) . additionally, ifn-i upregulate trail on nk cells and trail receptor (dr5) on the t cells and macrophages, providing a second potential mechanism for interferon-mediated lymphocyte and macrophage killing (66) . trail -/mice harbor lower bacterial burdens than wild-type counterparts, have decreased splenic lymphocyte apoptosis, and increased accumulation of myeloid cells in the spleen following l. monocytogenes infection. the reduction in lymphocyte death seen following l. monocytogenes infection is the major reason that ifnar -/mice are more resistant to infection (67) . several lines of evidence support this conclusion. first, mice deficient in lymphocytes (scid/ rag mice) are highly resistant to l. monocytogenes infection (68, 69) . second, mixed bone marrow chimeras that create mice that are ifnar + in all cells except lymphocytes are also resistant to l. monocytogenes infection (69) . this demonstrates the dominance of ifn-i signaling effects on lymphocytes. third, induction of ifn-i using poly(i:c) increases the susceptibility to infection of wild-type but not scid mice (69, 44) . finally, l. monocytogenes infection induces myeloid cell expression of il-10 that is dependent on ifnar expression by lymphocytes (69) . the upregulation of il-10 is a negative regulator of pathogen handling and il-10 -/mice are more resistant to infection despite having normal lymphocyte apoptosis (69, 70) . as an aside, the work on ifnar effects on l. monocytogenes infection was conducted on three different genetic backgrounds with different susceptibilities to infection. in all three strains-c57bl/6 (44), 129s6 (42) and balb/c (43)-ifnar signaling was detrimental to the outcome of infection. this demonstrates that ifnar effects are dominant over the genetic susceptibilities of the mouse strains to l. monocytogenes infection. further work needs to be done to determine if this applies to other bacterial infection models. the initial paradigm of the ifn-i system is that it provides antiviral protection that sometimes goes awry in certain autoimmunities. this simplified view has been replaced with a more complex and interesting role for the interferons in regulating immune responses. chronic viral infections are teaching us that while early ifn-i is important in controlling viremia, pathogens that can overcome this initial control benefit from the immune regulation that takes place following long-term interferon induction. the clinical relevance of this can be seen during infection of patients with hiv, where chronic ifn-i leads to trail-mediated t-cell death and poor disease outcome (71) . future work needs to be done to determine the applicability of ifn-i modulation as a therapeutic to important chronic human viral infections. another important area of research is the interface between viral and bacterial coinfections. the clinical importance of severe bacterial infections occurring after a primary viral infection is well established (72) . respiratory bacterial infections are more dangerous to patients when they occur following infection with viruses such as influenza and respiratory syncytial virus. this observation has been replicated in mouse models of infection (73, 74) . however, the interaction between viral and bacterial infection is not always deleterious. infection with herpesvirus induces prolonged ifn-γ production that leads to protection against infection with l. monocytogenes and yersinia pestis (75) . the main distinguishing feature between the two potential outcomes (acute versus chronic virus) and (detrimental versus beneficial) appears to center on the balance between ifn-i and ifn-γ effects. this reinforces the need to understand the molecular effects of these cytokines during bacterial infection. in the bacterial world, ifn-i were once believed to be relatively unimportant. this idea was reversed by research on l. monocytogenes. careful examination of additional bacterial infections has demonstrated that both route and tropism of bacterial infections matter in the requirement of ifn-i. future studies will be needed to determine cellular sources, molecular triggers and biological outcomes of ifn-i for many classes of bacterial pathogens. it will be interesting to see if bacteria have evolved mechanisms to manipulate the ifn-i system like some viruses do. recently, it has been shown that the balance of ifn-i and ifn-ii may be important in the outcome of human mycobacterial infections (76) . reminiscent of chronic lcmv infection, il-10 is also a key player in the ifn-i-mediated suppression of mycobacterial immunity. future work will be needed to determine if chronic ifn-i production is a common determinant of negative outcomes in infectious diseases. finally, we need a better understanding of how the genes specific for ifn-i lead to different outcomes from their close cousin, ifn-ii. national institute of allergy and infectious diseases (ai062832). type i interferons (alpha/beta) in immunity and autoimmunity the jak-stat pathway at twenty mechanisms of type-i-and type-ii-interferon-mediated signalling how cells respond to interferons systematic identification of type i and type ii interferon-induced antiviral factors functional role of type i and type ii interferons in antiviral defense type i interferon: friend or foe? type i interferons and the innate immune response-more than just antiviral cytokines interferons, immunity and cancer immunoediting lambda interferon renders epithelial cells of the respiratory and gastrointestinal tracts resistant to viral infections induction and function of type i and iii interferon in response to viral infection interferon-dependent immunity is essential for resistance to primary dengue virus infection in mice, whereas t-and b-cell-dependent immunity are less critical interferon function is not required for recovery from a secondary poxvirus infection effects of type i interferons on friend retrovirus infection alpha/beta interferons regulate murine gammaherpesvirus type i interferons and infection latent gene expression and reactivation from latency the role of alpha/beta and gamma interferons in development of immunity to influenza a virus in mice the role of interferon in influenza virus tissue tropism critical role for alpha/beta and gamma interferons in persistence of lymphocytic choriomeningitis virus by clonal exhaustion of cytotoxic t cells type i interferons are essential in controlling neurotropic coronavirus infection irrespective of functional cd8 t cells type i interferons produced by hematopoietic cells protect mice against lethal infection by mammalian reovirus theiler's virus infection of 129sv mice that lack the interferon alpha/beta or interferon gamma receptors alpha/beta interferon protects against lethal west nile virus infection by restricting cellular tropism and enhancing neuronal survival type i interferons in host defense type 1 interferons and the virus-host relationship: a lesson in detente coordinated and distinct roles for ifn-alpha beta, il-12, and il-15 regulation of nk cell responses to viral infection regulation of effector and memory t-cell functions by type i interferon type i interferon-mediated stimulation of t cells by cpg dna plasmacytoid dendritic cells promote rotavirusinduced human and murine b cell responses plasmacytoid dendritic cells induce plasma cell differentiation through type i interferon and interleukin 6 mechanisms of evasion of the type i interferon antiviral response by flaviviruses recent advances in understanding viral evasion of type i interferon molecular basis of viral persistence: a single amino acid change in the glycoprotein of lymphocytic choriomeningitis virus is associated with suppression of the antiviral cytotoxic t-lymphocyte response and establishment of persistence virus persistence in acutely infected immunocompetent mice by exhaustion of antiviral cytotoxic effector t cells interleukin-10 and the interleukin-10 receptor pd-1 and its ligands in tolerance and immunity restoring function in exhausted cd8 t cells during chronic viral infection persistent lcmv infection is controlled by blockade of type i interferon signaling blockade of chronic type i interferon signaling to control persistent lcmv infection myd88 and sting signaling pathways are required for irf3-mediated ifn-β induction in response to brucella abortus infection type i ifns enhance susceptibility to chlamydia muridarum lung infection by enhancing apoptosis of local macrophages type i ifn signaling constrains il-17a/f secretion by gammadelta t cells during bacterial infections type i interferon sensitizes lymphocytes to apoptosis and reduces resistance to listeria infection mice lacking the type i interferon receptor are resistant to listeria monocytogenes type i interferon production enhances susceptibility to listeria monocytogenes infection dynamic roles of type i and type ii ifns in early infection with mycobacterium tuberculosis the type i ifn response to infection with mycobacterium tuberculosis requires esx-1-mediated secretion and contributes to pathogenesis type i interferon induces necroptosis in macrophages during infection with salmonella enterica serovar typhimurium opposing roles for interferon regulatory factor-3 (irf-3) and type i interferon signaling during plague type i ifn signaling is crucial for host resistance against different species of pathogenic bacteria nod1 contributes to mouse host defense against helicobacter pylori via induction of type i ifn and activation of the isgf3 signaling pathway route of infection determines the impact of type i interferons on innate immunity to listeria monocytogenes type i interferon production induced by streptococcus pyogenes-derived nucleic acids is required for host protection intranasal poly-ic treatment exacerbates tuberculosis in mice through the pulmonary recruitment of a pathogen-permissive monocyte/macrophage population poly i:c enhances susceptibility to secondary pulmonary infections by gram-positive bacteria production of type i ifn sensitizes macrophages to cell death induced by listeria monocytogenes a specific gene expression program triggered by gram-positive bacteria in the cytosol listeriolysin o: a phagosome-specific lysin c-di-amp secreted by intracellular listeria monocytogenes activates a host type i interferon response innate sensing of bacterial cyclic dinucleotides: more than just sting the helicase ddx41 recognizes the bacterial secondary messengers cyclic di-gmp and cyclic di-amp to activate a type i interferon immune response characterization of the interferon-producing cell in mice infected with listeria monocytogenes a fluorescence reporter model defines "tip-dcs" as the cellular source of interferon β in murine listeriosis tnf/inos-producing dendritic cells mediate innate immune defense against bacterial infection ifn-beta increases listeriolysin o-induced membrane permeabilization and death of macrophages lymphocyte apoptosis during early phase of listeria infection in mice reduced apoptosis and ameliorated listeriosis in trail-null mice mechanisms and immunological effects of apoptosis caused by listeria monocytogenes regulation of macrophage ia expression in mice with severe combined immunodeficiency: induction of ia expression by a t cell-independent mechanism lymphocytes are detrimental during the early innate immune response against listeria monocytogenes both innate and acquired immunity to listeria monocytogenes infection are increased in il-10-deficient mice hiv-1 immunopathogenesis: how good interferon turns bad how do viral infections predispose patients to bacterial infections? type i interferon induction during influenza virus infection increases susceptibility to secondary streptococcus pneumoniae infection by negative regulation of γδ t cells viral infection augments nod1/2 signaling to potentiate lethality associated with secondary bacterial infections herpesvirus latency confers symbiotic protection from bacterial infection type i interferon suppresses type ii interferon-triggered human anti-mycobacterial responses i wish to thank dr emil r. unanue for his support and insightful discussions. the content is solely the responsibility of the author and does not necessarily represent the official views of the national institutes of health. key: cord-284514-b7no0yrv authors: davies, robert l; maccorquodale, roslyn; caffrey, bridget title: diversity of avian pasteurella multocida strains based on capsular pcr typing and variation of the ompa and omph outer membrane proteins date: 2003-02-02 journal: vet microbiol doi: 10.1016/s0378-1135(02)00300-0 sha: doc_id: 284514 cord_uid: b7no0yrv one hundred avian pasteurella multocida isolates recovered from cases of fowl cholera and related infections in england and wales over a 13-year period were characterised by capsular pcr typing and analysis of outer membrane protein (omp) profiles. sixty-eight percent of the strains were of capsular type a, 14% were type f, 5% were type d, 4% were type b and 9% were untypable. nineteen distinct omp profiles (omp-types) were identified based mainly on molecular mass heterogeneity of the heat-modifiable (ompa) and porin (omph) proteins. fifty-six percent of the isolates were represented by 15 omp-types, whereas 44% of the isolates were associated with four omp-types. the extensive molecular mass heterogeneity of the ompa and omph proteins supports previous findings that avian p. multocida strains are very diverse. furthermore, the isolates studied were associated with different clinical symptoms and were recovered from a wide range of lesions and tissues. the high degree of strain diversity together with the wide variety of clinical symptoms suggest that certain avian strains of p. multocida are opportunistic pathogens of relatively low virulence. strains of capsular types b, d and f, as well as the untypable isolates, were associated exclusively with specific omp-types and represent distinct and widely disseminated clonal groups. these observations support the view that avian strains of p. multocida have a clonal population structure. based on previous studies, the molecular mass heterogeneity of the ompa and omph proteins might provide a selective advantage to p. multocida by generating antigenic variation. pasteurella multocida is the aetiological agent of fowl cholera, a widely distributed and economically important disease of poultry, particularly chickens, turkeys, ducks and geese rimler and glisson, 1997) . the organism is also responsible for disease in wild birds, commercially raised game birds and caged birds . four capsular serogroups are recognised among avian strains of p. multocida, namely a, b, d and f rimler, 1987, 1989; rimler and rhoades, 1987) . strains of serogroup a are recognised as the primary cause of fowl cholera, whereas isolates of serogroups b, d and f are less frequently associated with disease rimler, 1987, 1989; wilson et al., 1993) . in addition, some avian strains of p. multocida are non-encapsulated and are not serogroupable wilson et al., 1993) . sixteen somatic serotypes (1-16) are also recognised in p. multocida , 1990a and most of these have been demonstrated in avian capsular serogroup a strains . there is considerable evidence, based on a wide range of molecular studies (snipes et al., 1989; carpenter et al., 1991; christiansen et al., 1992; wilson et al., 1993 wilson et al., , 1995 blackall et al., 1995 blackall et al., , 1998 gunawardana et al., 2000; petersen et al., 2001) , that avian strains of p. multocida are extremely diverse. in particular, a study of the population genetics of australian strains using multilocus enzyme electrophoresis (mlee) identified 56 electrophoretic types among only 81 field isolates (blackall et al., 1998) . based on dna-dna hybridisation and sugar fermentation patterns p. multocida has been subdivided into three subspecies, subsp. multocida, subsp. gallicida, and subsp. septica (mutters et al., 1985) and all of these have been isolated from birds (snipes et al., 1989; hirsh et al., 1990; fegan et al., 1995) . however, conflicting results from ribotyping and 16s rrna sequence data (petersen et al., 2001) suggest that the precise phylogenetic relationships of strains representing each of these subspecies is complex and has yet to be satisfactorily resolved. control of fowl cholera is primarily by good management practice and vaccination in areas where the disease is endemic (rimler and glisson, 1997) . both whole-cell bacterins and live vaccines composed of attenuated strains are currently available but neither is entirely satisfactory. bacterins only induce serotype-specific protection, whereas live vaccines sometimes cause disease (bierer and derieux, 1975; schlink and olson, 1987; prantner et al., 1990) and there is increasing interest in the development of subunit vaccines (kasten et al., 1995; luo et al., 1999) . outer membrane antigens that might be considered as potential vaccine candidates include the heat-modifiable or ompa and the porin or omph proteins mittal, 1996, 1997; luo et al., 1997 luo et al., , 1999 . both of these proteins are expressed in high copy number, are surface exposed and immunogenic (hancock, 1991; tagawa et al., 1993; yi and murphy, 1997; zeng et al., 1999; neary et al., 2001) . the omph protein has been shown to be heterogeneous in strains of p. multocida representing somatic serotypes 1-16 (luo et al., 1999) and there is evidence that anti-omph antibodies are protective in chickens (luo et al., 1999) and mice . there is less information available about the ompa protein of p. multocida, but this protein also exhibits variation in other bacterial species (duim et al., 1997; webb and cripps, 1998) . the aim of the study was to investigate capsular and outer membrane protein (omp) diversity among avian p. multocida strains isolated from diseased poultry in england and wales. in particular, heterogeneity of the ompa and omph proteins was examined and used as the basis for an omp classification scheme. since ompa and omph are important surface-exposed components of the outer membrane, analysis of their diversity in avian p. multocida strains will contribute to our understanding of host-pathogen interactions in fowl cholera, including the role of these proteins in immune evasion, and to the development of improved vaccines against this pathogen. one hundred avian field isolates of p. multocida were investigated. these were obtained from regional laboratories of the veterinary laboratories agency (vla) and originated from widespread geographic locations within england and wales over a 13-year period (1987) (1988) (1989) (1990) (1991) (1992) (1993) (1994) (1995) (1996) (1997) (1998) (1999) . the isolates were recovered predominantly from cases of fowl cholera and related acute disease conditions such as septicaemia and pneumonia. however, some isolates were associated with chronic conditions such as conjunctivitis, sinusitis, swollen head, arthritis, etc. properties of the isolates and details of the clinical symptoms of the birds of origin are provided in table 1 . the capsular reference strains x73 (a), m1404 (b), p3881 (d), p1235 (e) and p4679 (f) were kindly provided by dr. r. rimler, national animal disease center, ames, ia. the isolates were stored at à85 8c in 50% (v/v) glycerol in brain heart infusion broth (bhib). from à85 8c stock cultures, bacteria were streaked onto blood agar (brain heart infusion agar containing 5% (v/v) defibrinated sheep's blood) and incubated overnight at 37 8c. for preparation of dna, a few colonies were inoculated into 10 ml volumes of bhib and grown overnight at 37 8c at 120 rpm. for preparation of outer membranes, 0.4 ml of overnight growth in bhib was inoculated into 400 ml volumes of bhib in 2 l erlenmeyer flasks and incubated for 7 h at 37 8c at 120 rpm. cells from 1.0 ml of overnight cultures were harvested by centrifugation for 1 min at 13;000 â g and washed once in sterile, distilled h 2 o. dna was prepared with the instagene matrix (bio-rad) according to the manufacturers' instructions and stored at à20 8c. the capsular types were determined by multiplex capsular pcr typing with the capsule-specific primer pairs (capa, capb, capd, cape and capf) described by townsend et al. (2001) . isolates that were negative for all five capsular types were confirmed as p. multocida with a p. multocida-specific primer set (kmt1t7 and kmt1sp6) (townsend et al., 2001) in separate pcr reactions (see section 3) and classified as untypable. all primers were synthesised by sigma-genosys (cambridge, uk) and the capsular gene fragments were amplified with a taqdna polymerase kit (boehringer mannheim) according to the manufacturers instructions. pcrs were carried out in a geneamp pcr system 9700 (applied biosystems) thermal cycler using the following amplification parameters: denaturation at 94 8c for 30 s, annealing at 58 8c for 30 s and extension at 72 8c for 1 min. thirty cycles were performed and a final elongation step of 72 8c for 10 min was used. production of pcr amplicons of the expected size was confirmed by electrophoresis in 2% agarose gels. pooled pcr amplicons of capsular type a, b, d, e and f reference strains were used as standards in each gel. omps were prepared by sarkosyl extraction as previously described (davies et al., 1992; davies and donachie, 1996) . protein concentrations were determined by the modified lowry procedure (markwell et al., 1978) and adjusted to 2.0 mg/ml. omps were separated by sds-page in 12% (w/v) resolving gels (hoefer se600 electrophoresis apparatus) using the sds discontinuous system of laemmli (laemmli, 1970) as previously described (davies et al., 1992; davies and donachie, 1996) . unless otherwise stated all samples were heated at 100 8c for 5 min prior to electrophoresis. twenty micrograms of protein were loaded per lane and the proteins were visualised by staining with coomassie brilliant blue. protein molecular mass standards (pharmacia) consisted of phosphorylase b (94 kda), bovine serum albumin (67 kda), ovalbumin (43 kda), carbonic anhydrase (30 kda), trypsin inhibitor (20.1 kda) and a-lactalbumin (14.4 kda). the molecular masses of individual proteins were calculated with the labworks tm image acquisition and analysis computer software. the capsular types of the 100 avian p. multocida isolates were determined by capsular pcr typing and typical results are shown in fig. 1 . the distribution of capsular types among the 100 isolates is summarised in table 1 . sixty-eight (68%) isolates were of capsular type a, 14 (14%) were of type f, five (5%) were of type d, four (4%) were of type b and nine (9%) isolates were untypable. capsular type e was not detected among the population sampled. the p. multocida-specific primers were omitted from the capsular primer mixture because they interfered with the capsule-specific primers and resulted in a reduction of capsular pcr product (i.e. reduced band intensity). therefore, isolates that were negative for capsular typing were confirmed as untypable p. multocida in separate pcr assays with the p. multocida-specific primers (townsend et al., 2001) . microscopic examination of the untypable isolates after indian ink staining indicated that they were non-encapsulated. the stability of the omp profiles was examined by comparing the profiles of two isolates after repeated subculture and at different stages of the growth cycle. the profiles of these isolates were identical after 5, 10, 15 and 20 rounds of subculture on blood agar and after 6, 8, 12 and 24 h of growth in bhib (results not shown). the omp profiles of the 100 isolates were analysed by sds-page and provisionally assigned to omp-types based on profile similarity (described below). isolates assigned to the same omp-type were subsequently rerun on up to three or four occasions such that isolates of the same omp-type were directly compared on the same gel. an omp classification scheme was devised-based, firstly, on molecular mass variation of the two major proteins, ompa and omph (omp-type 1, 2, etc.), and, secondly, on variation of minor protein patterns (omp-type 1.1, 1.2, etc.). the ompa and omph proteins have overlapping molecular mass ranges (33-39 kda) and were distinguished on the basis of their different behaviours in sds-page gels after heat-treatment. the omph porin protein is tightly associated with peptidoglycan and is not released unless heated at a temperature of approximately 60 8c or higher (rosenbusch, 1974) . therefore, the omph protein does not migrate into the gel unless heated at 60 8c or higher prior to sds-page. in contrast, the ompa protein is not associated with peptidoglycan and freely migrates into the gel after heat-treatment at temperatures below 60 8c prior to sds-page. however, the ompa protein undergoes a characteristic conformational change when heated at 100 8c that results in an increase in its apparent molecular mass in sds-page gels (beher et al., 1980) . therefore, to identify ompa and omph, one isolate representing each omp-type was subjected to heat-treatment at 50, 60, 70, 80, 90 and 100 8c prior to sds-page. the results for two isolates of omp-types 3.1 and 10.2 are shown in fig. 2 . the ompa (a) and omph (h) proteins for each omp-type are indicated in fig. 3 and the results are described below. the 100 isolates consisted of 14 major omp groups that were classified as omp-types 1-14 based on variation of ompa and omph (described above). based on variation of minor proteins isolates of omp-types 1, 2 and 10 could be further subdivided into omptypes 1.1-1.3, 2.1 and 2.2, and 10.1-10.3, respectively. profiles representing each of these omp-types (with the exception of omp-types 1.3 and 10.3) are shown in fig. 3 . the molecular mass of ompa (a) varied from 36.9 to 37.9 kda and that of omph (h) varied from 33.1 to 38.3 kda. the distribution of omp-types among the avian isolates is shown in table 1 . isolates of omp-types 2.2 (15%), 7.1 (11%), 1.2 (9%) and 4.1 (9%) were the most numerous and accounted for 44% of the total. a smaller number of isolates, ranging from 1 to 7, were associated with each of the other 15 omp-types but these accounted for 56% of the total number of isolates. there was a strong correlation between certain capsular types and specific omp-types (table 1 ). the frequently occurring capsular type a was associated with 68 isolates representing 12 of the 19 omp-types. in contrast, capsular type b was associated exclusively with the four isolates of omp-type 12.1; these isolates originated from four different regional laboratories. capsular type d was associated with 1/3 isolates of omptype 5.1 and with the four isolates of omp-type 13.1; three of the four isolates of omptype 13.1 originated from different regional laboratories and the single omp-type 5.1 isolate came from a fourth laboratory. capsular type f was associated with the two isolates of omp-type 1.3, with 11/15 isolates of omp-type 2.2 and with 1/5 isolates of omp-type 6.1. all seven of the isolates representing omp-types 10.1-10.3 were untypable, as were 2/3 isolates of omp-type 5.1. the seven untypable/omp-type 10 isolates originated from six different regional laboratories; the two omp-type 5.1 isolates also came from different laboratories. overall, the majority of omp-types were represented by a single capsular type, but isolates of omp-types 2.2 and 6.1 were associated with capsular types a and f, and isolates of omp-type 5.1 were either untypable or possessed capsular type d. there are a number of difficulties associated with conventional capsular serotyping of p. multocida (chengappa et al., 1986; rhoades, 1987, 1989) . however, townsend et al. (2001) described an alternative and highly specific multiplex capsular pcr assay that is based on nucleotide sequence variation within the five capsular biosynthetic loci. this pcr-based capsular typing method was used in the present study and found to be a reliable and rapid method for capsular typing large numbers of p. multocida isolates. reference strains were used as internal standards and no cases of ambiguity occurred. the observed incidence of capsular serotypes in our sample was very similar to that described in the study of 246 isolates by rhoades and rimler (1987) . in the latter investigation, capsular types a, f, b and d were associated with 67, 5, 2 and 2% of isolates, respectively, whereas 24% of strains were untypable. the significantly higher incidence of serotype a strains with respect to isolates of serotypes b, d and f in this and previous studies wilson et al., 1993) suggests that the various serotypes differ in their virulence characteristics. although virulence studies have shown that strains of serotypes b, d and f are potentially pathogenic rimler, 1988, 1990b) , there is very little information about the comparative virulence of strains representing the different serotypes. the omp profiles of the avian p. multocida isolates were very diverse. the isolates could be classified into 19 distinct omp-types based on variation of ompa and omph and, to a lesser extent, of the minor proteins. fifty-six percent of the isolates were represented by 15 omp-types, whereas 44% of the isolates were associated with four omp-types. the high degree of heterogeneity observed in the omp profiles, and of ompa and omph in particular, was not unexpected because previous studies have shown that avian p. multocida strains are extremely diverse (snipes et al., 1989; christiansen et al., 1992; wilson et al., 1993 wilson et al., , 1995 blackall et al., 1995 blackall et al., , 1998 petersen et al., 2001) . in particular, blackall et al. (1998) identified 56 electrophoretic types among only 81 p. multocida isolates from australian poultry by mlee. in a previous study of mannheimia haemolytica (davies and donachie, 1996) , 184 strains were sub-divided into three distinct groups based on their omp profiles and these were subsequently shown to represent phylogenetically distinct lineages by mlee (davies et al., 1997) . however, no such demarcation was apparent among the omp profiles of the avian p. multocida isolates. omp patterns have been shown to be closely associated with electrophoretic types and clones identified by mlee in other species (achtman et al., 1983; musser et al., 1985 musser et al., , 1988 achtman and pluschke, 1986; kapur et al., 1992; davies et al., 1997) . the exclusive association of isolates of the less common capsular types with specific omp-types provided evidence that omp-types mark individual clonal groups of p. multocida (achtman and pluschke, 1986) . for example, isolates of omp-type 1.3 were associated with capsular type f, isolates of omp-type 10 were untypable, isolates of omp-type 12.1 were associated with capsular type b and isolates of omp-type 13.1 were associated with capsular type d (table 1) . furthermore, almost all of the isolates representing each of these groups originated from a different regional laboratory. this is significant because a characteristic feature of clonal bacterial populations is that strains representing the same clone originate from widespread geographic origins (selander and musser, 1990) . the association of capsular types b and d and certain untypable isolates, with specific omptypes is also important because it demonstrates for the first time that strains of these uncommon capsular types, together with untypable isolates, probably represent specific clones of p. multocida. in contrast, dziva et al. (2001) were unable to demonstrate a relationship between rapd patterns and capsular serogroups in their study of zimbabwean isolates of p. multocida (dziva et al., 2001) . isolates of omp-types 2.2 and 6.1 were associated with capsular types a and f. this observation is probably due to the close relationships of these two capsular types (townsend et al., 2001) . in many pathogenic bacterial species, the majority of cases of infectious disease are often caused by a small proportion of the total number of extant clones (selander and musser, 1990) . in this respect, avian p. multocida strains differ from many other pathogens because the majority of cases of disease were associated with a relatively large number of omp-types/clones. a possible reason for this is that the isolates were recovered from a diverse range of lesions and tissues and were associated with different types of infection ranging from pneumonia and septicaemia to sinusitis, conjunctivitis and swollen head. high levels of diversity were also observed among eschericha coli strains isolated from chickens with swollen-head syndrome and from birds with colibacillosis (white et al., 1990) . it was suggested that the large number of clonal genotypes associated with these avian diseases was due either to the opportunistic nature of the infections or to the widespread occurrence of unknown virulence factors (white et al., 1990; whittam, 1995) . swollen-head syndrome associated with e. coli is thought to be the result of a secondary infection subsequent to an initial viral infection caused by paramyxovirus, coronavirus, or pneumovirus. the high level of diversity observed among avian p. multocida isolates, together with the wide range of clinical symptoms and tissues of origin, similarly suggests that a high proportion of the isolates might represent opportunistic pathogens of relatively low virulence. in particular, isolates associated with conjunctivitis, sinusitis and swollen head could potentially be secondary pathogens following initial viral infection. confirmation of this hypothesis will require the comparison of bacterial isolates from diseased birds with the normal avian flora. the ompa and omph proteins of avian isolates of p. multocida were shown to be heterogeneous since numerous molecular mass variants were identified (fig. 3) . however, the omph protein (33.1-38.3 kda) is clearly more heterogeneous than the ompa protein (36.9-37.9 kda). comparative nucleotide sequence analysis of the omph proteins representing the 16 somatic serotypes of p. multocida has shown that the molecular mass heterogeneity of this protein is due to variation in the number of amino acids (318-333) in the protein (luo et al., 1999) . however, most of this variation is confined to two discrete hypervariable regions (amino acids 60-80 and 200-220) which are thought to correspond to external surface-exposed loops (luo et al., 1999) . similar heterogeneity occurs in the corresponding p2 (omph) and p5 (ompa) proteins of haemophilus influenzae, and has also been shown to be due to differences in the size of hypervariable surface-exposed loop regions (forbes et al., 1992; sikkema and murphy, 1992; duim et al., 1997; webb and cripps, 1998) . these surface-exposed loops are thought to interact with the host immune system and, by undergoing antigenic variation, provide the bacterium with an important defence mechanism murphy, 1994, 1997; neary et al., 2001) . furthering knowledge of the molecular basis of this diversity in p. multocida will lead to a better understanding of the role of these proteins in avian disease and contribute to the development of improved vaccines. in summary, this investigation of capsule and omp variation has confirmed the view that avian p. multocida isolates are very diverse. a possible explanation for the high level of strain diversity observed in the study is that many of the isolates were associated with chronic infections, were recovered from a wide range of lesions and tissues, and represent opportunistic pathogens. the association of certain capsular types with specific omp-types suggests that omp profiles mark individual clones of p. multocida. in particular, isolates of the uncommon capsular types b and d and certain untypable isolates, represent distinct clonal groups. the ompa and omph proteins exhibit extensive molecular mass heterogeneity that might provide a selective advantage to the pathogen by generating antigenic variation. clonal analysis of descent and virulence among selected escherichia coli six widespread bacterial clones among escherichia coli k1 isolates major heat-modifiable outer membrane protein in gram-negative bacteria: comparison with the ompa protein of escherichia coli immunologic response to turkey poults of various ages to an avirulent pasteurella multocida vaccine in the drinking water characterisation of pasteurella multocida isolated from fowl cholera outbreaks on turkey farms population structure and diversity of avian isolates of pasteurella multocida from australia molecular epidemiology of pasteurella multocida in turkeys identification of type d pasteurella multocida by counterimmunoelectrophoresis transmission of pasteurella multocida on california turkey premises in 1988-1989 intra-specific diversity and host specificity within pasteurella haemolytica based on variation of capsular polysaccharide, lipopolysaccharide and outer-membrane proteins outer membrane protein and lipopolysaccharide variation in pasteurella haemolytica a1 under different growth conditions evolutionary genetics of pasteurella haemolytica isolates recovered from cattle and sheep molecular variation in the major outer membrane protein p5 gene of nonencapsulated haemophilus influenzae during chronic infections random amplification of polymorphic dna and phenotypic typing of zimbabwean isolates of pasteurella multocida phenotypic characterisation of pasteurella multocida isolates from australian poultry variation in length and sequence of porin (ompp2) alleles of non-capsulate haemophilus influenzae molecular characterisation of avian pasteurella multocida isolates from australia and vietnam by rep-pcr and pfge bacterial outer membranes: evolving concepts serum resistance is correlated with encapsulation of avian strains of pasteurella multocida characteristics of pasteurella multocida isolated from waterfowl and associated avian species in california outer membrane protein patterns mark clones of escherichia coli o2 and o78 strains that cause avian septicemia pasteurella multocida produces a protein with homology to the p6 outer membrane protein of haemophilus influenzae cleavage of structural proteins during the assembly of the head of bacteriophage t4 cloning and characterization of the major outer membrane protein gene (omph) of pasteurella multocida x-73 sequence analysis of pasteurella multocida major outer membrane protein (omph) and application of synthetic peptides in vaccination of chickens against homologous strain challenge a modification of the lowry procedure to simplify protein determination in membrane and lipoprotein samples a population genetic framework for the study of invasive diseases caused by serotype b strains of haemophilus influenzae clonal population structure of encapsulated haemophilus influenzae reclassification of the genus pasteurella trevisan 1887 on the basis of deoxyribonucleic acid homology, with proposals for the new species pasteurella dagmatis, pasteurella canis, pasteurella stomatis, pasteurella anatis, and pasteurella langaa antibodies to loop 6 of the p2 porin protein of nontypeable haemophilus influenzae are bactericidal against multiple strains genetic diversity of pasteurella multocida fowl cholera isolates as demonstrated by ribotyping and 16s rrna and partial atpd sequence comparisons the pathogenesis of pasteurella multocida serotype a:3,4 infection in turkeys: a comparison of two vaccine strains and a field isolate capsular groups of pasteurella multocida isolated from avian hosts virulence of avian capsular serogroup b pasteurella multocida for turkey poults fowl cholera somatic serotypes of pasteurella multocida strains isolated from avian hosts (1976-1988) virulence and toxigenicity of capsular serogroup d pasteurella multocida strains isolated from avian hosts fowl cholera serogroup f, a new capsule serogroup of pasteurella multocida pasteurella multocida characterization of the major envelope protein from escherichia coli. regular arrangement on the peptidoglycan and unusual dodecyl sulphate binding vaccination of turkey breeder hens and toms for fowl cholera with cu strain population genetics of bacterial pathogenesis molecular analysis of the p2 porin protein of nontypeable haemophilus influenzae use of an rrna probe and restriction endonuclease analysis to fingerprint pasteurella multocida isolated from turkeys and wildlife characterization of a heat-modifiable outer membrane protein of haemophilus somnus genetic organization of pasteurella multocida cap loci and development of a multiplex capsular pcr typing system characterization of an outer membrane protein of pasteurella multocida belonging to the ompa family role of outer membrane protein h (omph)-and ompa-specific monoclonal antibodies from hybridoma tumors in protection of mice against pasteurella multocida the 32 kda major outer-membrane protein of pasteurella multocida capsular serotype d secondary structure and molecular analysis of interstrain variability in the p5 outer-membrane protein of non-typable haemophilus influenzae isolated from diverse anatomical sites genetic relationships among strains of avian escherichia coli associated with swollen-head syndrome genetic population structure and pathogenicity in enteric bacteria comparison of dna fingerprinting and serotyping for identification of avian pasteurella multocida isolates pasteurella multocida isolated from wild birds of north america: a serotype and dna fingerprint study of isolates from 1978 to 1993 mapping of a strain-specific bactericidal epitope to the surface-exposed loop 5 on the p2 porin protein of non-typeable haemophilus influenzae importance of an immunodominant surface-exposed loop on outer membrane protein p2 of nontypeable haemophilus influenzae molecular cloning of the pasteurella haemolytica poma gene and identification of bovine antibodies against poma surface domains this study was supported by a wellcome trust university award to r.l. davies (053669/z/98/z). we are extremely grateful to staff of the veterinary laboratories agency (vla) for the provision of isolates, including those at bury st. edmunds for making available strains of their p. multocida collection. key: cord-259935-xyo2pe4g authors: wang, ching-ying; lu, chien-yi; li, shih-wen; lai, chien-chen; hua, chun-hung; huang, su-hua; lin, ying-ju; hour, mann-jen; lin, cheng-wen title: sars coronavirus papain-like protease up-regulates the collagen expression through non-samd tgf-β1 signaling date: 2017-05-02 journal: virus res doi: 10.1016/j.virusres.2017.04.008 sha: doc_id: 259935 cord_uid: xyo2pe4g sars coronavirus (cov) papain-like protease (plpro) reportedly induced the production of tgf-β1 through p38 mapk/stat3-meidated egr-1-dependent activation (sci. rep. 6, 25754). this study investigated the correlation of plpro-induced tgf-β1 with the expression of type i collagen in human lung epithelial cells and mouse pulmonary tissues. specific inhibitors for tgf-βri, p38 mapk, mek, and stat3 proved that sars-cov plpro induced tgf-β1-dependent up-regulation of type i collagen in vitro and in vivo. subcellular localization analysis of smad3 and smad7 indicated that non-smad pathways in tgf-β1 signaling involved in the production of type i collagen in transfected cells with psars-plpro. comprehensive analysis of ubiquitin-conjugated proteins using immunoprecipitation and nanolc–ms/ms indicated that sars-cov plpro caused the change in the ubiquitination profile of rho gtpase family proteins, in which linked with the increase of rho-like gtpase family proteins. moreover, selective inhibitors tgf-βri and stat6 (as1517499) ascertained that stat6 activation was required for plpro-induced tgf-β1-dependent up-regulation of type i collagen in human lung epithelial cells. the results showed that sars-cov plpro stimulated tgf-β1-dependent expression of type i collagen via activating stat6 pathway. severe acute respiratory syndrome (sars)-associated coronavirus (cov), a member of betacoronoviruses in the coronaviridae family, is identified as the causative agent for the outbreak of sars in asia and other countries in [2002] [2003] . like other human coronaviruses (hcovs) hcov-229e, hcov-oc43, hcov-nl63, hcov-hku1, and mers-cov (li and lin, 2013; huang et al., 2015) , sars-cov genome is an approximately 30 kb positive-strand rna consisting of a 5′ cap, a 3′ poly (a) tract, and 14 open reading frames (orfs). the largest orfs orf1a and orf1ab encode for the polyprotein replicases 1a and 1ab mainly involving in the sars-cov replication, as cleaved in cis and in trans by orf1a-encoded papain-like protease (plpro) and 3c-like protease (3clpro). plpro, a de-ubiquitinating/de-isgylating enzyme (barretto et al., 2005; ratia et al., 2006) , has the antagonistic activities of type i interferon (ifn) via blocking irf-3 and erk1 phosphorylation, preventing the iκbα degradation, and de-ubiquitinating the sting-traf3-tbk1 complex (li et al., 2011; frieman et al., 2009; sun et al., 2012) . recently, plpro shows the inhibitory effect on tolllike receptor 7 (tlr7) mediated cytokine production through removing lys63-linked ubiquitin chains of traf3 and traf6 (li et al., 2016a) . sars-cov up-regulates pro-inflammatory cytokines like ifn-γ, il-18, tgf-β1, tnf-α, il-6, ip-10, mcp-1, mig, and il-8 (huang et al., 2005; he et al., 2006) , in which recruits immune responder cells into the lungs, triggers acute respiratory distress syndrome (ards), and even causes lung fibrosis in the late phase (huang et al., 2005; he et al., 2006) . among sars-cov proteins, the nucleocapsid induces a smad3dependent induction of tgf-β1 expression (zhao et al., 2008) ; spike protein stimulates the il-8 up-regulation in lung cells (chang et al., 2004) ; nsp1 provokes the expression of ccl5, cxvl10, and ccl3 (law http://dx.doi.org/10.1016 (law http://dx.doi.org/10. /j.virusres.2017 received 10 january 2017; received in revised form 3 april 2017; accepted 10 april 2017 et al., 2007) ; plpro elavates the production of tgf-β1 and pro-fibrotic markers via ubiquitin proteasome, p38 mapk, and erk1/2-mediated signaling (li et al., 2012) . recently, sars-cov plpro notably initiates ros/p38 mapk/stat3 pathway to activate egr-1 dependent expression of tsp-1, tgf-β1 and vimentin in vitro and in vivo (li et al., 2016b) . therefore, plpro becomes a virulent factor in sars pathogenesis. tgf-β1 plays a crucial mediator of tissue fibrosis in lung, skin, liver, heart, and kidney through modulating the expression of pro-fibrotic proteins including type i collagen, fibronectin, α-sma, and vimentin (kubiczkova et al., 2012) . in the canonical smad signalling pathway, tgf-β1 interacts with the tgf-β type i receptor, activates receptorregulated smads (smad2 and smad3) complexed with smad4, and then translocate to the nucleus to synthesize tgf-β1-induced transcriptional genes like type i collagen (leask and abraham, 2004; kubiczkova et al., 2012) . in non-canonical tgf-β signaling pathways, tgf-β1 activates mapks (erk, jnk and p38 mapk), rho-like gtpases (rhoa, rac and cdc42), pi3k/akt, wnt/β-catenin, or ca 2+ signaling cascades in tgf-β1-induced transcriptional response (zhang, 2009 ). the activation of p38 mapk is responsible for tgf-β-induced epithelial-tomesenchymal transition of mouse mammary gland epithelial cells under a receptor independent of receptor-mediated smad activation (yu et al., 2002) . the activation of rhoa in tgf-β-induced emt response is also independent of smad2 and/or smad3 (bhowmick et al., 2001) . our prior study demonstrated sars-cov plpro triggering the tgf-β1 production in vitro and in vivo that linked with up-regulating the expression of pro-fibrotic proteins (vimentin and glial fibrillary acidic protein) (li et al., 2016b) . this study assesses possible effects and mechanisms of sars-cov plpro-induced tgf-β1 upregulation on the expression of type i collagen. the induction ability of sars-cov plpro on in vitro and in vivo expression of type i collagen was characterized. in addition, subcellular localization of smad3, smad7, and stat6 was performed to elucidate the key factors involved in the induction of type i collagen by plpro. the relationship between tgf-β upregulation and the mechanism of type i collagen induction by plpro was validated by the specific inhibitors of tgf-β receptor kinase, p38 mapk and stat6. human alveolar basal epithelial a549 cells grew in dulbecco's modified eagle's medium (hyclone laboratories) and were transfected with control vector pcdna3.1/his c (invitrogen), or psars-plpro containing sars-cov plpro gene, as described in our prior reports (li et al., 2011 (li et al., , 2012 (li et al., , 2016a (li et al., , 2016b . in addition, psars-plpro (h273a) that had the alanine substitution for histidine at position 273 by ala within plpro gene was constructed using pcr-based sitedirected mutagenesis with a mutated primer pair (5′-ggtaact atc-agtgtggtgcttacactcatataactgctaag-3′ and 5′-cttagcagt tatatgagtgtaagcaccacactgatagttacc-3′). a549 cells transiently expressing recombinant plpro 2 days post transfection was analyzed using western blotting, real-time rt-pcr, sirius staining, and immunofluorescent staining assays. to detect the mrna expression of type i collagen, total rnas extracted from transfected cells treated with or without a tgf-β1 inhibitor (sb-431542) were further examined the mrna levels of type i collagen using quantitative real-time pcr. the relative fold mrna levels were normalized by gapdh mrna, presented as the relative ratio (b). for verifying the protein levels of type i collagen, transfected cells with serial doses of indicated plasmids were stained using sirius red staining kit (c). ** p value < 0.01 by student's t-test. the lysate of transfected cells was performed by western blotting with primary antibodies including rabbit anti-tgf-β1 (cell signaling), anti-e. coli synthesized plpro mouse serum, anti-phospho stat6 (tyr641) (cell signaling), and anti-β-actin mab (abcam), and hrpconjugated secondary antibodies like goat anti-mouse or anti-rabbit igg. immune complexes were detected using enhanced chemiluminescent hrp substrate (millipore). to measure the expression of type i collagen, tgf-β1, and vimentin in transfected cells, total rnas extracted from transfected cells 2 days post transfection and mouse lung tissues were analyzed using two-step real time rt-pcr with sybr green i, as described in our prior reports (li et al., 2016b) . primer pairs included (1) 5′-gttcgtgaccgtgac-ctcg-3′ and 5′-tcttgtccttggggttcttgc-3′ for human type i collagen, (2) 5′-gagcggagagtactggatcg-3′ and 5′-tactcgaac-gggaatccatc-3′ for mouse type i collagen, (3) 5′-ggcctttcctgc-ttctcatgg-3′ and 5′-ccttgctgtactgcgtgtcc-3′ for human tgf-β1, (4) 5′-tctctgaggctgccaaccg-3′ and 5′-cgaaggtgacgagc-catttcc-3′ for human vimentin, (5) 5′-cagaacagcctcccgaatg-3′ and 5′-tgctacgctcactccattac-3′ for human rac1, (6) 5′-agcc-acatcgctcagacac-3′ and 5′-gcccaatacgaccaa atcc-3′ for human gapdh, and (7) 5′-tgaggccggtgctgagtatgtcg-3′ and 5′-ccacagtcttctgggtggcagtg-3′ for mouse gapdh. specific pcr product was quantified using the abi prism 7900ht sequence detection system (pe applied biosystems). relative mrna levels of indicated genes were normalized relative to gapdh mrna. for the detection of collagen expression, the tissue sections were stained with sirius red solution for 2 h, and then rinsed 10 times with 0.5% glacial acetic acid in pbs. after dehydrating with ethanol, stained sections were mounted on the glass slides, and then examined using light microscopy (olympus, bx50). the mouse mode with a direct chest injection was performed as described in our prior report (li et al., 2016b) . empty vector pcdna3.1 or recombinant plasmin psars-plpro (50 μg/100 μl) in 3% sucrose/ pbs was injected into the right chest of 5 eight-weeks-old balb/c male mice using a 1-ml syringe with a 28-gage needle every 2 days. after 15 injections, the mice were sacrificed; the lung tissues were fixed, dehydrated, embedded in paraffin, and cut at 4-5 μm thickness using a rotary microtome. for immunohistochemistry (ihc) staining, mouse lung tissues were performed with anti-e. coli synthesized plpro serum, as descried in our previous report (li et al., 2016b) . for h & e staining, sections were stained with hematoxylin for 3 min, eosin for 3 min, dehydrated in ethanol, and then mounted as slides that were examined and photographed using light microscopy (olympus, bx50). sirius staining and sybr green real time rt-pcr assays were mentioned above. for determining the effects of sars-cov plpro on the nuclear translocalization of smad3, smad7, and stat6, a549 cells grew on the glass coverslip in 6-wellt were transfected with psars-cov plpro or pcdna3.1, and treated with or without 1 μm kartogenin (sigma). for testing the role of rac1 in stat6 signal, the rac1 mutant plasmid, pmx-ig-rac1 t17n provided by dr. takehito uruno (kyushu university, japan), was co-transfected into cells. after 2-day incubation, cells were fixed with 3.7% formaldehyde in pbs for 1 h, blocked with 1% bovine serum albumin in pbs for 1 h, and then incubated with specific primary antibodies against smad3, smad7, and stat6 at 4°c to detect the mrna expression of type i collagen, total rnas extracted from lung tissues were examined the mrna levels of type i collagen using quantitative real-time pcr. the relative fold mrna levels were normalized by gapdh mrna, presented as the relative ratio (b). ** p value < 0.01 by student's t-test. overnight. subsequently, cells were reacted with fitc-or af546conjugated secondary antibodies in a dark box for 2 h, finally, cells were stained with 4′,6-diamidino-2-phenylindole (dapi) for 10 min. after washing with pbs, stained cells were photographed using the immunofluorescence microscopy (olympus, bx50). the lysates from plpro-expressing and empty vector cells were reacted with anti-ubiquitin antibodies for 4 h at 4°c, and then incubated with protein a-sepharose beads. the ubiquitin-conjugated proteins were collected after centrifugation, washed four times with net buffer, embedded in sds-page gel, and then digested in gel. the peptides of ubiquitin-conjugated proteins were recovered for nanolc-ms/ms spectra. proteins were identified according to mass spectra obtained were compared to swissport database (release 51.0) via mascot algorithm (version 2.2.07), as described in our prior reports (li et al., 2012) . peptides were identified if mascot individual ion scores exceeded 30. all data were collected from 3 independent experiments and analyzed using student's t-test or χ 2 test. statistical significance was considered at p < 0.05. to examine the association of sars-cov plpro-induced tgf-β1 production with the collagen up-regulation, a549 lung epithelial cells transiently transfected with pcdna3.1 and psars-plpro were analyzed the production of tgf-β1 and type i collagen using western blot, realtime rt-pcr and sirius red staining assays (fig. 1) . transfected cells with psars-plpro, but not pcdna3.1, secreted the active form of tgf-β1, and significantly increased the mrna and protein expression of type i collagen. importantly, sb-431542 (a selective tgf-βri inhibitor) treatment at 100 nm caused the 4-fold reduction of type i collagen mrna in transfected cells with psars-plpro (fig. 1b) . in a mouse model, the expression of type i collagen in lung tissues from chest injection with pcdna3.1 or psars-plpro was examined using sirius staining and quantitative rt-pcr (fig. 2) . the expression of sars-plpro in lung tissues of mice was determined using ihc staining with anti-e. coli synthesized plpro serum, and ihc positivity for plpro expression within lung tissues was observed in the group infected with psars-plpro ( fig. 2a) . h & e and sirius staining assays indicated that pulmonary inflammation with the infiltration of immune cells and the increase of type i collagen was identified in the psars-plpro group, but not vector control and solvent groups ( fig. 2a) . real-time pcr confirmed that plpro triggered the mrna expression of type i collagen fig. 3 . analysis of tgf-β1 and type i collagen levels in transiently transfected cells in response to the inhibitors for p38 mapk and stat3. to detect the mrna expression of tgf-β1 or type i collagen, total rnas extracted from transfected cells treated with or without the rac1 mutant plasmid (a), an inhibitor for p38 mapk (sb203580) (c) or stat3 (stattic) (d) were examined the mrna levels of type i collagen using quantitative real-time pcr. the relative fold mrna levels were normalized by gapdh mrna, presented as the relative ratio (a, b). for verifying the protein levels of type i collagen, transfected cells treated with or without an inhibitor for p38 mapk (sb203580) or mek (u0126) were stained using sirius red staining kit (c). ** p value < 0.01 by student's t-test. c.-y. wang et al. virus research 235 (2017) [58] [59] [60] [61] [62] [63] [64] [65] [66] in mouse lung tissues in comparison with vector control and solvent groups (fig. 2b) . to examine the proteolytic enzymatic activity of plpro on the production of tgf-β1 and type i collagen, the catalytic mutant of plpro (h273a) was constructed, and then used to investigate whether plpro (h273a) up-regulated tgf-β1 and type i collagen in vitro (fig. 3a) . importantly, plpro(h273a) with the catalytic mutation lose the ability to induce the expression of tgf-β1 and type i collagen in vitro. since sars-plpro had been demonstrated to stimulate p38 mapk/stat3mediated activation of tgf-β1 production (li et al., 2016b) , sb203580 (a specific p38-mapks inhibitor), u0126 (a mek1/2 inhibitor), and stattic (a small-molecule inhibitor of stat3 activation) were used to further confirm the correlation between the tgf-β1 production and type i collagen up-regulation in transfected cells with psars-plpro and pcdna3.1 (fig. 3b-d) . sb203580 significantly reduced the mrna expression of tgf-β1, in which was linked with down-regulation of type i collagen in transfected cells with psars-plpro in presence of sb203580 or u0126 ( fig. 3b and c) . stattic also suppressed the mrna expression of type i collagen in transfected cells with psars-plpro ( fig. 3d) . overall, results of the in vitro and in vivo data demonstrated that the proteolytic enzymatic activity was required for sars-cov plpro-dependent tgf-β1-mediated up-regulation of pro-fibrotic gene type i collagen. to examine whether smad-dependent pathways involve in tgf-β1mediated up-regulation of type i collagen in response sars-cov plpro, subcellular localization of receptor-regulated smad3 and inhibitory smad7 in transfected cells were detected using the immunofluorescent and dapi staining (fig. 4) . imaging analysis of transfected cells indicated that smad3 localized in the nucleus of pcdna3.1-transfected cells, but not psars-plpro-transfected cells (fig. 4a) . moreover, smad7 was detected in the nucleus of both transfected cells (fig. 4b) . interestingly, kartogenin, a stimulator for tgf-β1/smad3 signal pathway , was used to verify the inhibitory effect of plpro on tgf-β1/smad3 signal in transfected cells (fig. 4c) . after 24 h treatment with kartogenin, samd3 nuclear translocation was spotted within the nucleus in vector control cells, but not in plproexpressing cells. most samd3 was in the cytoplasm of psars-plpro transfected cells treated with kartogenin. the result indicated that sars-cov plpro inactivated smad-dependent pathways, implying that non-smad pathways in tgf-β1signaling for the production of type i collagen would be initiated by sars-cov plpro. non-smad pathways in tgf-β1 signaling include map kinase, rholike gtpase, and phosphatidylinositol-3-kinase/akt pathways (zhang, 2009) . to examine the possible pathways involved in tgf-β1-dependent up-regulation of type i collagen by sars-cov plpro, the profiles of ubiquitin-conjugated proteins in transfected cells with vector control and psars-plpro were determined using immune-precipitation and nanolc-ms/ms. interestingly, several proteins of the ras gtpase family were identified (table 1 ), in which indicated the ubiquitination of these ras family gtpase proteins was influenced by sars-cov plpro. fig. 5a represented the mass spectrum of rac1 identified by lc-ms/ms. rac1, a rho gtpase, had an increase of the ubiquitination in plpro-expressing cells compared to vector control cells. real-time rt-pcr and western blotting assays revealed the elevation of rac1 mrna and protein expression in transfected cells with psars-plpro compared to vector control ( fig. 5b and c) . rho gtpases were identified in the regulation of g protein-coupled receptor signaling through activation of jak/stat and modulated stat-dependent gene expression (pelletier et al., 2003) . in addition, stat-6-dependent collagen production has been demonstrated in human skin fibroblasts and mouse airway fibroblasts in response to bovine milk and platelet-derived growth factor, respectively (kippenberger et al., 2015; lu et al., 2014) . for analyzing the correlation between plpro-induced rac1 upregulation and stat6 activation, co-transfection of pcdna3.1 or psars-plpro plus the rac1 mutant plasmid pmx-ig-rac1 t17n was performed, and the stat6 activation in co-transfected cells was measured using immunofluorescence staining with anti-stat6 and fitc-conjugated secondary antibodies. plpro expression caused the stat6 expression and induced the translation of stat6 in the nucleus. remarkably, the rac1 mutant slightly affected the stat6 up-regulation by plpro, but significantly reduced plpro-induced stat6 nuclear translocation (fig. 5d) . later, the functional activity of stat6 in tgf-β1-dependent collagen up-regulation was further characterized in vector control and plpro-expressing cells (figs. 6 and 7) . nuclear localization and phosphorylation of stat6 was observed in transfected cells with psars-plpro, but not vector control cells (figs. 6 and 7 a) . importantly, sb-431542, a selective tgf-βr inhibitor, significantly reduced the entry of stat6 in the nucleus of plpro-expressing cells (fig. 6) . the result indicated that rho gtpases/stat6 was responsible for one of non-smad pathways in sars plpro-induced tgf-β1 signals. furthermore, a stat6 inhibitor as1517499 markedly suppressed tgf-β1-dependent collagen expression in plpro-expressing cells (fig. 7) . the results demonstrated that stat6 activation was required for sars plpro-induced tgf-β1-dependent production of type i collagen. plpro has been demonstrated to trigger the tgf-β1 production in human promonocytes, human lung epithelial cells, and pulmonary tissues in mouse models (li et al., 2012 (li et al., , 2016b . sars-cov plpro induced the ros-mediated p38 mapk and stat3 activation of egr-1 expression, in which egr-1 specifically bound to the tgf-β1 promoter region between −175 to −60, resulting in the increase of tgf-β1 production. this study indicated that sars-cov plpro stimulated the production of type i collagen in vitro and in vivo ( fig. 1-3) . sars-cov plpro-induced collagen deposition in pulmonary tissues was associated with lung inflammation and pulmonary fibrosis in mice injected with psars-plpro (fig. 3) . the specific inhibitor for tgf-β receptor, sb-431542, blocked the up-regulation of type i collagen in transfected cells with psars-plpro. moreover, the inhibitors for p38 mapk and stat3 that involved in egr-1-dependent tgf-β1 production significantly reduced the expression of tgf-β1 and type i collagen. overall, the results revealed that sars-cov plpro elicited tgf-β1dependent up-regulation of type i collagen. tgf-β1-dependent profibrotic response was considered as the crucial character in sars-cov plpro-induced pathogenesis. an elevated level of pro-inflammatory cytokines including tgf-β1 was detected in sars-cov-infected cells in autopsy tissues from died sars patients (he et al., 2006) , in which implied the association of pro-inflammatory cytokines with the severity and mortality of sars. the increase of serum tgf-β1 concentration during the early phase of sars could be associated with lung infiltration (beijing group of national research project for sars, 2003) . meanwhile, the decrease of serum tgf-β1 concentration markedly lowered in the severity of sars patients (zhang et al., 2004) . in canonical pathway, tgf-β1interacts with type i and ii tgf-β receptors and causes the activation of a serine/threonine kinase domain in tgf-β receptors and the recruitment and phosphorylation of smad2 and smad3. the phosphorylated smad2/3 complexed with smad4 was trans-localized into nucleus to regulate the target gene expression (kubiczkova et al., 2012) . subcellular localization analysis demonstrated that smad3 was predominant in cytoplasmic, but not in the nucleus in transfected cells with psars-plpro compared to vector control (fig. 4) , revealing that canonical smad-dependent signaling pathway was not involved in plpro-induced tgf-β1-dependent upregulation of type i collagen. tgf-β also activates non-canonical non-smad pathways, including mapks (erk1/erk2, jnk and p38), pi3k kinases, akt/pkb, mtor, and rho-like gtpase family proteins (ras, rhoa, rac1, and cdc42) (zhang, 2009; kubiczkova et al., 2012) . particularly, activation of rhoa pathway was required for tgf-βmediated process of epithelial-to-mesenchymal trans-differentiaion in a dominant-negative smad3 cells (bhowmick et al., 2001) . in addition, rac1 activation promoted tgf-β-dependent collagen expression in mesangial cells (hubchak et al., 2009) . lc-ms/ms analysis demonstrated that sars-cov plpro influenced the ubiquitination status of ras-related c3 botulinum toxin substrate 1 (rac1), ras gtpaseactivating-like protein iqgap1, ras-related protein rab (rab5c), putative ras-related protein rab (rab1c), and ras gtpase-activating protein-binding protein (g3bp1) ( table 1) . real-time rt-pcr and western blotting assays indicated the increased expression of rac1 in transfected cells with psars-plpro compared to vector control (fig. 5) . since activation of jak/stat pathway in a rac-dependent manner was identified in response to the agonist of protein-coupled receptors (pelletier et al., 2003) , stat-dependent signals were investigated in this study. the tgf-βri inhibitor sb-431542 significantly attenuated the phosphorylation and nuclear localization of stat6 in transfected cells with psars-plpro (fig. 6) . meanwhile, the stat6 inhibitor as1517499 meaningfully reduced tgf-β1-dependent up-regulation of type i collagen in plpro-expressing cells (fig. 7) . the results indicated fig. 6 . nuclear localization of stat6 in transfected lung epithelial cells in response to sb-431542. for analyzing the effect of sb-431542 on nuclear localization of stat6, transfected cells were treated with or without sb-431542 for 2 days, washed, fixed, and reacted with primary antibodies against phospho-stat6, followed by fitc-conjugated secondary antibodies. after staining with dapi for 10 min, imaging was analyzed by immunofluorescent microscopy. that stat6 activation was required for plpro-induced tgf-β1-dependent expression of type i collagen in human lung epithelial cells and mouse lung tissues. the result was accordant with the previous reports in that stat6-dependent collagen production has been demonstrated in human skin fibroblasts and mouse airway fibroblasts (kippenberger et al., 2015; lu et al., 2014) . sars-cov plpro affected on the ubiquitination and expression profile of rho-like gtpase family proteins that could link with the activation of stat6 signaling in tgf-β1dependent collagen expression, in which suggested that a new gtpase proteins/stat6 pathway might play a critical role in tgf-β1-dependent collagen production in plpro-expressing cells. in summary, sars-cov plpro induced p38 mapk/stat3-mediated tgf-β1-dependent up-regulation of type i collagen, causing pulmonary pro-fibrotic responses. plpro diminished the nuclear localization of smad3, changed the expression profiling of rho-like gtpase family proteins, and activated stat6-mediated tgf-β1-dependent production of type i collagen. the results let us conclude that sars-cov plpro induced non-smad signals including stat6 activation in tgf-β1dependent pulmonary pro-fibrotic responses. fig. 7 . analysis of stat6-mediated plpro-induced production of type i collagen. to determine the phosphorylation of stat6, transfected cells with 0.5, 1, 2, 5 or 10 μg of pcdna3.1 or pplpro were harvested 2 days post transfection; the cell lysates were examined using western blotting with anti-phospho-stat6 (tyr641) or anti-β actin antibodies (a). for analyzing mrna levels of type i collagen (b) and vimentin (c), transfected cells were treated with or without as1517499 for 4 h, and then their mrna levels of type i collagen and vimentin were measured by quantitative pcr. relative mrna levels were normalized by gapdh mrna, presented as relative ratio. ** p value < 0.01 by student's t-test. the papain-like protease of severe acute respiratory syndrome coronavirus has deubiquitinating activity dynamic changes in blood cytokine levels as clinical indicators in severe acute respiratory syndrome transforming growth factor-beta1 mediates epithelial to mesenchymal transdifferentiation through a rhoa-dependent mechanism induction of il-8 release in lung cells via activator protein-1 by recombinant baculovirus displaying severe acute respiratory syndrome-coronavirus spike proteins: identification of two functional regions severe acute respiratory syndrome coronavirus papain-like protease ubiquitin-like domain and catalytic domain regulate antagonism of irf3 and nf-kappab signaling expression of elevated levels of pro-inflammatory cytokines in sars-cov-infected ace2+ cells in sars patients: relation to the acute lung injury and pathogenesis of sars an interferon-gamma-related cytokine storm in sars patients epidemiology of human coronavirus nl 63 infection among hospitalized patients with pneumonia in taiwan rac1 promotes tgfbeta-stimulated mesangial cell type i collagen expression through a pi3k/aktdependent mechanism stat6-dependent collagen synthesis in human fibroblasts is induced by bovine milk tgf-β-an excellent servant but a bad master role for nonstructural protein 1 of severe acute respiratory syndrome coronavirus in chemokine dysregulation tgf-beta signaling and the fibrotic response human coronaviruses: clinical features and phylogenetic analysis severe acute respiratory syndrome coronavirus papain-like protease suppressed alpha interferon-induced responses through downregulation of extracellular signalregulated kinase 1-mediated signalling pathways correlation between tgf-β1 expression and proteomic profiling induced by severe acute respiratory syndrome coronavirus papain-like protease sars coronavirus papain-like protease inhibits the tlr7 signaling pathway through removing lys 63-linked polyubiquitination of traf3 and traf6 sars coronavirus papain-like protease induces egr-1-dependent upregulation of tgf-β1 via ros/p38 mapk/stat3 pathway platelet-derived growth factor mediates interleukin-13-induced collagen i production in mouse airway fibroblasts rho family gtpases are required for activation of jak/stat signaling by g protein-coupled receptors severe acute respiratory syndrome coronavirus papain-like protease: structure of a viral deubiquitinating enzyme coronavirus papain-like proteases negatively regulate antiviral innate immune response through disruption of sting-mediated signaling a heterocyclic molecule kartogenin induces collagen synthesis of human dermal fibroblasts by activating the smad4/ smad5 pathway tgf-β receptor-activated p38 map kinase mediates smad-independent tgf-β responses analysis of serum cytokines in patients with severe acute respiratory syndrome non-smad pathways in tgf-beta signaling severe acute respiratory syndrome-associated coronavirus nucleocapsid protein interacts with smad3 and modulates transforming growth factor-beta signaling this study was supported by china medical university under the aim for top university plan of the ministry of education, taiwan (chm106-6-2). this project was also funded by grants from the ministry of science and technology, taiwan (most102-2628-b-039-044-my3, most105-2320-b-039-053-my3) and china medical university (cmu105-s-20, cmu103-asia-07, and cmu105-asia-10). key: cord-015503-j99cgsjt authors: tang, xiaolu; wu, changcheng; li, xiang; song, yuhe; yao, xinmin; wu, xinkai; duan, yuange; zhang, hong; wang, yirong; qian, zhaohui; cui, jie; lu, jian title: on the origin and continuing evolution of sars-cov-2 date: 2020-03-03 journal: natl sci rev doi: 10.1093/nsr/nwaa036 sha: doc_id: 15503 cord_uid: j99cgsjt the sars-cov-2 epidemic started in late december 2019 in wuhan, china, and has since impacted a large portion of china and raised major global concern. herein, we investigated the extent of molecular divergence between sars-cov-2 and other related coronaviruses. although we found only 4% variability in genomic nucleotides between sars-cov-2 and a bat sars-related coronavirus (sarsr-cov; ratg13), the difference at neutral sites was 17%, suggesting the divergence between the two viruses is much larger than previously estimated. our results suggest that the development of new variations in functional sites in the receptor-binding domain (rbd) of the spike seen in sars-cov-2 and viruses from pangolin sarsr-covs are likely caused by mutations and natural selection besides recombination. population genetic analyses of 103 sars-cov-2 genomes indicated that these viruses evolved into two major types (designated l and s), that are well defined by two different snps that show nearly complete linkage across the viral strains sequenced to date. although the l type (∼70%) is more prevalent than the s type (∼30%), the s type was found to be the ancestral version. whereas the l type was more prevalent in the early stages of the outbreak in wuhan, the frequency of the l type decreased after early january 2020. human intervention may have placed more severe selective pressure on the l type, which might be more aggressive and spread more quickly. on the other hand, the s type, which is evolutionarily older and less aggressive, might have increased in relative frequency due to relatively weaker selective pressure. these findings strongly support an urgent need for further immediate, comprehensive studies that combine genomic data, epidemiological data, and chart records of the clinical symptoms of patients with coronavirus disease 2019 (covid-19). the coronavirus disease 2019 (covid-19) epidemic started in late december 2019 in wuhan, the capital of central china's hubei province. since then, it has rapidly spread across china and in other countries, raising major global concerns. the etiological agent is a novel coronavirus, sars-cov-2, named for the similarity of its symptoms to those induced by the severe acute respiratory syndrome. as of february 28, 2020, 78,959 cases of sars-cov-2 infection have been confirmed in china, with 2,791 deaths. worryingly, there have also been more than 3,664 confirmed cases outside of china in 46 countries and areas (https://www.who.int/emergencies/diseases/novel-coronavirus-2019/situation-reports/), raising significant doubts about the likelihood of successful containment. further, the genomic sequences of sars-cov-2 viruses isolated from a number of patients share sequence identity higher than 99.9%, suggesting a very recent host shift into humans [1] [2] [3] . coronaviruses are naturally hosted and evolutionarily shaped by bats [4, 5] . indeed, it has been postulated that most of the coronaviruses in humans are derived from the bat reservoir [6, 7] . unsurprisingly, several teams have recently confirmed the genetic similarity between sars-cov-2 and a bat betacoronavirus of the sub-genus sarbecovirus [8] [9] [10] [11] [12] [13] . the whole-genome sequence identity of the novel virus has 96.2% similarity to a bat sars-related coronavirus (sarsr-cov; ratg13) collected in yunnan province, china [2, 14] , but is not very similar to the genomes of sars-cov (about 79%) or mers-cov (about 50%) [1, 15] . it has also been confirmed that the sars-cov-2 uses the same receptor, the angiotensin converting enzyme ii (ace2), as the sars-cov [11] . although the specific route of transmission from natural reservoirs to humans remains unclear [5, 13] , several studies have shown that pangolins may have provided a partial spike gene to sars-cov-2; the critical functional sites in the spike protein of sar-cov-2 are nearly identical to one identified in a virus isolated from a pangolin [16] [17] [18] . despite these recent discoveries, several fundamental issues related to the evolutionary patterns and driving forces behind this outbreak of sars-cov-2 remain unexplored [19] . herein, we investigated the extent of molecular divergence between sars-cov-2 and other related coronaviruses and carried out population genetic analyses of 103 sequenced genomes of sars-cov-2. this work provides new insights into the factors driving the evolution of sars-cov-2 and its pattern of spread through the human population. for each annotated orf in the reference genome of sars-cov-2 (nc_045512), we extracted the orthologous sequences in human sars-cov, four bat sars-related coronaviruses (sarsr-cov: ratg13, zxc21, zc45, and bm48-31), one pangolin sarsr-cov from guangdong (gd) [17] , and six pangolin sarsr-cov genomes from guangxi (gx) [18] (table s1) . we aligned the coding sequences (cdss) based on the protein alignments (see materials and methods). most orfs annotated from sars-cov-2 were found to be conserved in other viruses, except for orf8 and orf10 (table 1 ). the protein sequence of sars-cov-2 orf8 shared very low similarity with sequences in sars-cov and bm48-31, and orf10 had a premature stop codon in both sars-cov and bm48-31 (fig. s1) . a one-base deletion caused a frame-shift mutation in orf10 of zxc21 ( fig. s1 ). to investigate the phylogenetic relationships between these viruses at the genomic scale, we concatenated coding regions (cdss) of the nine conserved orfs (orf1ab, e, m, n, s, orf3a, orf6, orf7a, and orf7b) and reconstructed the phylogenetic tree using the synonymous sites ( fig. 1a) . we also used codeml in the paml [20] 1a ). in parallel, we also calculated the pairwise dn, ds, and ω values between sars-cov-2 and another virus ( table 1) . the genome-wide phylogenetic tree indicated that sars-cov-2 was closest to ratg13, followed by gd pangolin sarsr-cov, then by gx pangolin sarsr-covs, then by zc45 and zxc21, then by human sars-cov, and finally by bm48-31 (fig. 1a) . notably, we found that the nucleotide divergence at synonymous sites between sars-cov-2 and other viruses was much higher than previously anticipated. for example, although the overall genomic nucleotides overall differ ~4% between sars-cov-2 and ratg13, the genomic average ds was 0.17, which means the divergence at the neutral sites is 17% between these two viruses (table 1) . this is because the nonsynonymous sites are usually under stronger negative selection than synonymous sites, and calculating sequence differences without separating these two classes of sites may underestimate the extent of molecular divergence by several folds. notably, the ds value varied considerably across genes in sars-cov-2 and the other viruses analyzed. in particular, the spike gene (s) consistently exhibited larger ds values than other genes (table 1 ). this pattern became clear when we calculated the ds value for each branch in fig. 1a for the spike gene versus the concatenated sequences of the remaining genes ( fig. s2 ). in each branch, the ds of spike was 2.22 ± 1.35 (mean ± sd) times as large as that of the other genes. this extremely elevated ds value of spike could be caused either by a high mutation rate or by natural selection that favors synonymous substitutions. synonymous substitutions may serve as another layer of genetic regulation, guiding the efficiency of mrna translation by changing codon usage [21] . if positive selection is the driving force for the higher synonymous substation rate seen in spike, we expect the frequency of optimal codons (fop) of spike to be different from that of other genes. however, our codon usage bias analysis (table s2 ) suggests the fop of spike was only slightly higher than that of the genomic average (0.717 versus 0.698, see materials and methods). thus, we believe that the elevated synonymous substitution rate measured in spike is more likely caused by higher mutational rates; however, the underlying molecular mechanism remains unclear. both sars-cov and sars-cov-2 bind to ace2 through the rbd of spike protein in order to initiate membrane fusion and enter human cells [1, 2, [22] [23] [24] [25] [26] . five out of the six critical amino acid (aa) residues in rbd were different between sars-cov-2 and sars-cov (fig. 1b) , and a 3d structural analysis indicated that the spike of sars-cov-2 has a higher binding affinity to ace2 than sars-cov [23] . intriguingly, these same six critical aas are identical between gd pangolin-cov and sars-cov-2 [16] . in contrast, although the genomes of sars-cov-2 and ratg13 are more similar overall, only one out of the six functional sites are identical between the two viruses ( fig. 1b) . it has been proposed that the sars-cov-2 rbd region of the spike protein might have resulted from recent recombination events in pangolins [16] [17] [18] . although several ancient recombination events have been described in spike [27, 28] , it also seems likely that the identical functional sites in sars-cov-2 and gd pangolin-cov may actually the result of coincidental convergent evolution [18] . if the functional aa residues in the sars-cov-2 rbd region were acquired from gd pangolin-cov in a very recent recombination event, we would expect the nucleotide sequences of this region to be nearly identical between the two viruses. however, for the cds sequences that span five critical aa sites in the sars-cov-2 spike (ranging from codon 484 to 507, covering five adjacent functional sites: f486, q493, s494, n501, and y505; fig. s3 originated from the gd pangolin-cov due to a very recent recombination event. alternatively, it seems more likely that a high mutation rate in spike, coupled with strong natural selection, has shaped the identical functional aa residues between these two viruses, as proposed previously [18] . although these sites are maintained in sars-cov-2 and gd pangolin-cov, mutations may have changed the residues in the ratg13 lineage after it diverged from sars-cov-2 (the blue arrow in fig. 1a ). in summary, it seems that the shared identity of critical aa sites between sars-cov-2 and gd pangolin-cov might be due to random mutations coupled with natural selection, and not necessarily recombination. the genome-wide ω value between sars-cov-2 and other viruses ranged from 0.044 to 0.124 (table 1) we downloaded 103 publicly available sars-cov-2 genomes, aligned the sequences, and identified the genetic variants. for ease of visualization, we marked each virus strain based on the location and date the virus was isolated with the format of "location_date" throughout this study (see table s1 for details; each id did not contain information of the patient's race or ethnicity). although sars-cov-2 is an rna virus, for simplicity, we presented our results based on dna sequencing results throughout this study (i.e., the nucleotide t (70/83) of nonsynonymous mutations), indicating either a recent origin [30] or population growth [31] . in general, the derived alleles of synonymous mutations were significantly skewed towards higher frequencies than those of nonsynonymous ones (p < 0.01, wilcoxon rank-sum test; fig. 2 ), suggesting the nonsynonymous mutations tended to be selected against. however, 16.3% (7 out of 43) synonymous mutations, and one nonsynonymous (orf8 (l84s, 28,144)) mutation had a derived frequency of ≥ 70% across the sars-cov2 strains. the nonsynonymous mutations that had derived alleles in at least two sars-cov-2 strains affected six proteins: orf1ab (a117t, i1607v, l3606f, i6075t), s (h49y, v367f), orf3a (g251v), orf7a (p34s), orf8 (v62l, s84l), and n (s194l, s202n, p344s). to detect the possible recombination among sars-cov2 viruses, we used haploview [32] to analyze and visualize the patterns of linkage disequilibrium (ld) between variants with minor alleles in at least two sars-cov-2 strains (fig. 3a ). since most mutations were at very low frequencies, it is not surprising that many pairs had a very low r 2 or lod value ( fig. 3b -c). consistent with another recent report [31] , we did not find evidence of recombination between the sars-cov2 strains. however, we found that snps at location 8,782 (orf1ab: t8517c, synonymous) and 28,144 (orf8: c251t, s84l) showed significant linkage, with an r 2 value of 0.954 (fig. 3b, red) and a lod value of 50.13 (fig. 3c, red) . among the 103 sars-cov-2 virus strains, 101 of them exhibited complete linkage between the two snps: 72 strains exhibited a "ct" haplotype (defined as "l" type because t28,144 is in the codon of leucine) and 29 strains exhibited a "tc" haplotype (defined as "s" type because c28,144 is in the codon of serine) at these two sites. thus, we categorized the sars-cov-2 viruses into two major types, with l being the major type (~70%) and s being the minor type (~30%). although we defined the l and s types based on two tightly linked snps, strikingly, the separation between the l (blue) and s (red) types was maintained when we reconstructed the haplotype networks using all the snps in the sars-cov-2 genomes ( fig. 4a ; the number of mutations between two neighboring haplotypes was inferred parsimoniously). this analysis further supports the idea that the two linked snps at sites 8,782 and 28,144 adequately define the l and s types of sars-cov-2. to determine whether l or s type is ancestral, we examined the genomic alignments of sars-cov-2 and other highly related viruses. strikingly, nucleotides of the s type at sites 8,782 and 28,144 were identical to the orthologous sites in the most closely related viruses ( fig. 4b) . remarkably, both sites were highly conserved in other viruses as well. hence, although the l type (~70%) was more prevalent than the s type (~30%) in the sars-cov-2 viruses we examined, the s type is actually the ancestral version of sars-cov-2. to further examine the relationship among the strains in the l and s types, we reconstructed a phylogenetic tree of all the 103 sars-cov-2 viruses based on their whole-genome sequences. our phylogenetic tree also clearly shows the separation of the two types (fig. 5) . viruses of the l type (blue) first clustered together, and likewise, viruses of the s type (red) were also more closely related to each other. therefore, our whole-genome comparisons further confirm the separation of the l and s types. thus far, we found that, although the l type is derived from the s type, l (~70%) is more prevalent than s (~30%) among the sequenced sars-cov-2 genomes we examined. this pattern suggests that l has a higher transmission rate than the s type. furthermore, our mutational load analysis indicated that the l type had accumulated a significantly higher number of derived mutations than s type (p < 0.0001, wilcoxon rank-sum test; fig. s5 ). we propose that, although the l type newly evolved from the ancient s type, it transmits faster or replicates faster in human populations, causing it to accumulate more mutations than the s type. thus, our results suggest the l might be more aggressive than the s type due to the potentially higher transmission and/or replication rates. to test whether the two types of sars-cov-2 had differences in temporal and spatial distributions, we stratified the viruses based on the locations and dates they were isolated ( fig. 6 and table s3 ). if the l type is more aggressive than the s type, why did the relative frequency of the l type decrease compared to the s type in other places after the initial breakout in wuhan? one possible explanation is that, since january 2020, the chinese central and local governments have taken rapid and comprehensive prevention and control measures. these human intervention efforts might have caused severe selective pressure against the l type, which might be more aggressive and spread more quickly. the s type, on the other hand, might have experienced weaker selective pressure by human intervention, leading to an increase in its relative abundance among the sars-cov-2 viruses. thus, we hypothesized that the two types of sars-cov-2 viruses might have experienced different selective pressures due to different epidemiological features. of note, the above analyses were based on very patchy sars-cov-2 genomes that were collected from different locations and time points. more comprehensive genomic data is required for further testing of our hypothesis. it is currently unclear how the l type specifically evolved from the s type during the development of sars-cov-2. however, we found that the sequence of viruses isolated from to further investigate the heteroplasmy of sars-cov-2 viruses in patients, we searched 12 deep-sequencing libraries of sars-cov-2 genomes that were deposited in the sequence read archive (sra) ( table s4 , materials and methods). we found 17 genomic sites that showed evidence of heteroplasmy of sars-cov-2 virus in five patients, but we did not find any other instances of the co-existence of l and s types in any patient (table 2) . these findings evince the developing complexity of the evolution of sars-cov-2 infections. further studies investigating how the different alleles of sars-cov-2 viruses compete with each other will be of significant value. in this study, we investigated the patterns of molecular divergence between sars-cov-2 and other related coronaviruses. although the genomic analyses suggested that sars-cov-2 was closest to ratg13, their difference at neutral sites was much higher than previously realized. our results provide novel insights into tracing the intermediate natural host of sars-cov-2. with population genetic analyses of 103 genomes of sars-cov-2, we found that sars-cov-2 viruses evolved into two major types (l and s types), and the two types were well defined by just two snps that show nearly complete linkage across sars-cov-2 strains. although the l type (~70%) was more prevalent than the s type (~30%) in the sars-cov-2 viruses we examined, our evolutionary analyses suggested the s type was most likely the more ancient version of sars-cov-2. our results also support the idea that the l type is more aggressive than the s type. since nonsynonymous sites are usually under stronger negative selection than synonymous sites, calculating sequence differences without separating these two classes of sites could lead to a potentially significant underestimate of the degree of molecular divergence. for example, although the overall nucleotides only differed by ~4% between sars-cov-2 and ratg13, the genomic average ds value, which is usually a neutral proxy, was 0.17 between these two viruses ( table 1) . of note, the genome-wide ds value is 0.012 between humans and chimpanzees [33] , and 0.08 between humans and rhesus macaques [34] . thus, the neutral molecular divergence between sars-cov-2 and ratg13 is 14 times larger than that between humans and chimpanzees, and twice as large as that between humans and macaques. the genomic average ds value between sars-cov-2 and gd pangolin-cov is 0.475, which is comparable to that between humans and mice (0.5) [35] , and the ds value between our analyses of molecular evolution and population genetics suggested that some amino acid changes might be favored by natural selection during the evolution of sars-cov-2 and other related viruses. however, negative selection appears to be the predominant force acting on these viruses. interestingly, the virus isolated from one patient in shenzhen on january 13, 2020 (sz_2020/01/13.a, gisaid id: epi_isl_406592) had c at both positions 8,782 and 28,144 in the genome, belonging to neither l nor s type ( fig. 4a and 5) . notably, this strain had one stop-gain mutation in orf1ab and had accumulated 20 silent and 5 nonsynonymous mutations after diverging from the ancestor haplotype (fig. 4a ). thus, it is possible that functional constraints on the genomic sequence were weakened after the disruption of orf1ab in this strain. notably, on viruses isolated from a patient living in south korean (skorea_2020/01.a, gisaid: epi_isl_411929), acquired six nonsynonymous mutations that were different from the most recent common ancestor of sars-cov-2: orf1ab (m902i and t6891m), s (s221w), orf3a (w128l and g251v), and e (l37h). if these changes are not due to sequencing errors, it would be interesting to test whether and how these mutations affect the transmission and pathogenesis of sars-cov-2. in this work, we propose that sars-cov-2 can be divided into two major types (l and s types): the s type is ancestral, and the l type evolved from s type. intriguingly, the s and l types can be clearly defined by just two tightly linked snps at positions 8,782 (orf1ab: t8517c, synonymous) and 28,144 (orf8: c251t, s84l). however, it is currently unclear whether l type evolved from the s type in humans or in the intermediate hosts. it is also unclear whether the l type is more virulent than the s type. orf1ab, which encodes replicase/transcriptase, is required for viral genome replication and might also be important for viral pathogenesis [36] . although the t8517c mutation in orf1ab does not change the protein sequence (it changes the codon agt (ser) to agc (ser)), we hypothesized this mutation might affect orf1ab translation since agt is preferred while agc is unpreferred (table s2 ). orf8 promotes the expression of atf6, the er unfolded protein response factor, in human cells [37] . thus, it will be interesting to investigate the function of the s84l aa change in orf8, as well as the combinatory effect of these two mutations in sars-cov-2 pathogenesis. in summary, our analyses of 103 sequenced sars-cov-2 genomes suggest that the l type is more aggressive than the s type and that human interference may have shifted the relative abundance of l and s type soon after the sars-cov-2 outbreak. as previously noted [19] , the data examined in this study are still very limited, and follow-up analyses of a larger set of data are needed to have a better understanding of the evolution and epidemiology of sars-cov-2. there is a strong need for further immediate, comprehensive studies that combine genomic data, epidemiological data, and chart records of the clinical symptoms of patients with sars-cov-2. the set of 103 complete genome sequences were downloaded from gisaid (global initiative on sharing all influenza data; https://www.gisaid.org/) with acknowledgment, genbank (https://www.ncbi.nlm.nih.gov/genbank), and nmdc (http://nmdc.cn/#/ncov). sequences and annotations of the reference genome of sars-cov-2 (nc_045512) and other related viruses were downloaded from genbank or gisaid (table s1 ). the genomic sequences of sars-cov-2 were aligned using muscle v3.8.31 [38] . the annotated cdss of other viruses were downloaded from genbank. to avoid missing annotations in other viruses, we also annotated the orfs using cdss annotated in sars-cov-2 using exonerate (--model protein2genome:bestfit --score 5 -g y) [39] . the protein sequences of sars-cov-2 and other related viruses were aligned with muscle v3.8.31 [38] , and the codon alignments were made based on the protein alignment with revtrans [40] . the codon alignments of the conserved orfs were further concatenated for down-stream evolutionary analysis. the phylogenetic tree was constructed by the neighbor-joining method in mega-x [41] using the parameters of kimura 2-parameter model, and only the third positions of codons were considered. yn00 from paml v4.9a [20] was used to calculate the pairwise divergence between sars-cov-2 and other viruses for each individual gene or for the concatenated sequences. the free-ratio model in codeml in the paml [20] package was used to calculate the dn, ds, and ω values for each branch. positive selection was detected using easycodeml [42] , a recently published wrapper of codeml [20] . the m7 and m8 models were compared. in the m7 model, ω follows a beta distribution such that 0⩽ω⩽1, and in the m8 model, a proportion p 0 of sites have ω drawn from the beta distribution, and the remaining sites with proportion p 1 are positively selected and have ω 1 >1. the lrts between m7 and m8 models were conducted by comparing twice the difference in log-likelihood values (2 ln δl) against a χ 2 -distribution (df=2). the positively selected sites were identified with the bayes empirical bayes (beb) score larger than 0.95. dnasp v6.12.03 [43] was used to generate multi-sequence aligned haplotype data, and popart v1.7 [44] was used to draw haplotype networks based on the haplotypes generated by dnasp. raxml v8.2.12 [45] was used to build the maximum likelihood phylogenetic tree of 103 aligned sars-cov-2 genomes with theparameters "-p 1234 -m gtrcat". we downloaded 12 sars-cov-2 metagenomic sequencing libraries (table s2) , and mapped the ngs reads to the reference genome of sars-cov-2 (nc_045512) using bwa (0.7.17-r1188) [46] with the default parameters. snp calling was done using bcftools mpileup (bcftools 1.9) [47] . we calculated the rscu (relative synonymous codon usage) value of each codon in the sars-cov-2 reference genome (nc_045512). the rscu value for each codon was the observed frequency of this codon divided by its expected frequency under equal usage among the amino acid [48] . the codons with rscu > 1 were defined as preferred codons, and those with rscu < 1 were defined as unpreferred codons. the fop (frequency of optimal codons) value of each gene was calculated as the number of preferred codons divided by the total number of preferred and unpreferred codons. the authors declare that they have no conflicts of interest. for each gene, the dn and ds values between sars-cov-2 and another virus are given, and the dn/ds (ω) ratio is given in the parenthesis. genomic characterisation and epidemiology of 2019 novel coronavirus: implications for virus origins and receptor binding a pneumonia outbreak associated with a new coronavirus of probable bat origin identification of a novel coronavirus causing severe pneumonia in human: a descriptive study origin and evolution of pathogenic coronaviruses bat origin of a new human coronavirus: there and back again. science china life sciences bats are natural reservoirs of sars-like coronaviruses detection of group 1 coronaviruses in bats in north america genome composition and divergence of the novel coronavirus (2019-ncov) originating in china evolution of the novel coronavirus from the ongoing wuhan outbreak and modeling of its spike protein for risk of human transmission. sci china life sci the 2019-new coronavirus epidemic: evidence for virus evolution discovery of a novel coronavirus associated with the recent pneumonia outbreak in humans and its potential bat origin genomic characterization of the 2019 novel human-pathogenic coronavirus isolated from a patient with atypical pneumonia after visiting wuhan evolutionary perspectives on novel coronaviruses identified in pneumonia cases in china full-genome evolutionary analysis of the novel corona virus (2019-ncov) rejects the hypothesis of emergence as a result of a recent recombination event return of the coronavirus: 2019-ncov evidence of recombination in coronaviruses implicating pangolin origins of ncov-2019 isolation and characterization of 2019-ncov-like coronavirus from malayan pangolins identification of 2019-ncov related coronaviruses in malayan pangolins in southern china moral imperative for the immediate release of 2019-ncov sequence data. national science review paml 4: phylogenetic analysis by maximum likelihood codon optimality, bias and usage in translation and mrna decay receptor recognition by novel coronavirus from wuhan: an analysis based on decade-long structural studies of sars cryo-em structure of the 2019-ncov spike in the prefusion conformation characterization of spike glycoprotein of 2019-ncov on virus entry and its immune cross-reactivity with spike glycoprotein of sars-cov identification of two critical amino acid residues of the severe acute respiratory syndrome coronavirus spike protein for its variation in zoonotic tropism transition via a double substitution strategy difference in receptor usage between severe acute respiratory syndrome (sars) coronavirus and sars-like coronavirus of bat origin a new coronavirus associated with human respiratory disease in china homologous recombination within the spike glycoprotein of the newly identified coronavirus may boost cross-species transmission from snake to human moderate mutation rate in the sars coronavirus genome and its implications origin time and epidemic dynamics of the 2019 novel coronavirus decoding evolution and transmissions of novel pneumonia coronavirus using the whole genomic data haploview: analysis and visualization of ld and haplotype maps the chimpanzee s, analysis c. initial sequence of the chimpanzee genome and comparison with the human genome evolutionary and biomedical insights from the rhesus macaque genome initial sequencing and comparative analysis of the mouse genome sars coronavirus replicase proteins in pathogenesis discovery of a rich gene pool of bat sars-related coronaviruses provides new insights into the origin of sars coronavirus muscle: multiple sequence alignment with high accuracy and high throughput automated generation of heuristics for biological sequence comparison revtrans: multiple alignment of coding dna from aligned amino acid sequences molecular evolutionary genetics analysis across computing platforms easycodeml: a visual tool for analysis of selection using codeml dnasp 6: dna sequence polymorphism analysis of large data sets popart: full-feature software for haplotype network construction raxml version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies fast and accurate short read alignment with burrows-wheeler transform the sequence alignment/map format and samtools codon usage in regulatory genes in escherichia coli does not reflect selection for 'rare' codons the authors thank the researchers who generated and shared the sequencing data from note the derived alleles of synonymous mutations are skewed towards higher frequencies than those of nonsynonymous mutations. a. ld plot of any two snp pairs among the 29 sites that have minor alleles in at least two strains. the number near slashes at the top of the image shows the coordinate of sites in the genome. color in the square is given by standard (d'/lod), and the number in square is r 2 value. b. the r 2 of each pair of snps (y-axis) against the genomic distance between that pair (x-axis). c. the lod of each pair of snps (y-axis) against the genomic distance between that pair (x-axis). note that in both b and c, the red point represents the ld between snps at 8,782 and 28,144. a. the haplotype networks of sars-cov-2 viruses. blue represents the l type, and red is the s type. the orange arrow indicates that the l type evolved from the s type. note that in this study, we marked each sample with a unique id that starting with the geological location, followed by the date the virus was isolated (see table s1 for details). each id did not contain information of the patient's race or ethnicity. b. evolution of the l and s types of sars-cov-2 viruses. genome sequence alignments with the seven most closely related viruses indicated that the s type was most likely the ancient version of sars-cov-2. ".", the nucleotide sequence is identical; "-", gap. in our recent publication (https://doi.org/10.1093/nsr/nwaa036), we showed that among circulating sars-cov-2 (with 103 genomes analyzed) two different viral genomes co-exist. we identified them as lineages l and s. the concerned amino acid we used to define the l and s lineages is located in orf8 (open reading frame 8), which plays a yet undefined role in the viral life cycle. based on the finding that "l" lineage has a higher frequency than lineage s, we described the l lineage as aggressive. we now recognize that within the context of our study the term "aggressive" is misleading and should be replaced by a more precise term "a higher frequency". in short, while we have shown that the two lineages naturally co-exist, we provided no evidence supporting any epidemiological conclusion regarding the virulence or pathogenicity of sars-cov-2. by saying so, corrections will be made in the print version of this paper to avoid being misleading. key: cord-292344-3bj567gr authors: zimmet, p. title: the burden of type 2 diabetes: are we doing enough? date: 2003-09-30 journal: diabetes & metabolism doi: 10.1016/s1262-3636(03)72783-9 sha: doc_id: 292344 cord_uid: 3bj567gr summary increasing levels of obesity, arising from energy-rich diets and sedentary lifestyles, are driving a global pandemic of type 2 diabetes. the prevalence of type 2 diabetes worldwide is set to increase from its present level of 150 million, to 225 million by the end of the decade and to as many as 300 million by 2025. shocking as they are, these figures represent only clinically diagnosed diabetes, and many more cases of diabetes remain undiagnosed and untreated. in addition, up to one-quarter of western populations have impaired glucose tolerance or the dysmetabolic syndrome, which are considered to represent pre-diabetic states. type 2 diabetes is appearing increasingly in children and adolescents, and the frequency of diagnosis of paediatric type 2 diabetes is outstripping that of type 1 diabetes in some areas. the long-term complications associated with type 2 diabetes carries a crushing burden of morbidity and mortality, and most type 2 diabetic patients die prematurely from a cardiovascular event. diabetic patients are more than twice as costly to manage as non-diabetic patients, due mainly to the high costs associated with management of diabetic complications. indeed, diabetes care already accounts for about 2-7% of the total national health care budgets of western european countries. controlling the type 2 diabetes epidemic will require changes to the structure of healthcare delivery. well-resourced interventions will be required, with effective co-ordination between all levels of government, health care agencies, multidisciplinary health care teams, professional organisations, and patient advocacy groups. above all, intervention is needed today. diabetes metab, 2003,29,6s9-6s18 • www.e2med.com/dm p zimmet t oday we are seeing a paradox in global public health. in recent decades, we have seen the reemergence of communicable diseases such as tuberculosis, and a new group including hiv/aids, ebola virus and, most recently, the devastating epidemic of severe acute respiratory syndrome (sars). in addition, there is still a global crisis resulting from widespread malnutrition. however, against this background, we are seeing a dramatic rise in prevalence of chronic non-communicable diseases such as type 2 diabetes, cardiovascular diseases, hypertension and obesity in developed and developing nations. there were already signals that diabetes was to become the epidemic of the 21 st century in the early 1970s. at this time, bennett and his colleagues discovered an extraordinarily high prevalence of type 2 diabetes in the pima indians of the usa [1] , and we reported on the equally high rates of diabetes in the micronesian population of nauru and other pacific island communities [2, 3] . over subsequent decades, numerous reports have highlighted the high prevalence of type 2 diabetes in a number of other populations including native americans, afro-americans, and mexican americans in the usa [4] [5] [6] [7] , native canadians [8] , australian aborigines and torres strait islanders [9] , and polynesians in new zealand [10, 11] . the prevalence of type 2 diabetes is rising relentlessly around the world (fig 1) . current estimates suggest that, globally, the number of persons with diabetes will rise from 151 million in the year 2000, to 221 million by the year 2010, and to 300 million by 2025 [12, 13] . this rise is predicted to occur in virtually every nation, with the greatest increases expected in developing countries. type 2 diabetes will account for nine patients in every ten of these diagnoses. this explosive increase in the prevalence of type 2 diabetes, and the consequences of its complications and associated disorders, represents the greatest health care challenge facing the world today [14] . the highest rates of type 2 diabetes occur in native americans and pacific islanders, followed by hispanics or mexican americans, people originating from the indian subcontinent, south east asians and african americans [12, 13] . in addition, a relatively high prevalence has been reported from some of the middle east arab states [15, 16] , and from disadvantaged minorities in the developed countries, including australia's indigenous population [17, 18] . type 2 diabetes affects up to 40% of adults in native american and pacific island populations [1, 2, 19, 20] and the years 1976 to 1988 saw an increase from 11.4% to 14.3% in the prevalence of diabetes among people age 40-74 years in the usa [21] . in china, a prevalence figure of 2.5%, from a 1994 survey of 224,251 subjects aged 25-74 from all parts of the country, was about three-fold higher than prevalence estimates from a decade before [22] . the type 2 diabetes prevalence in an urban south indian population among individuals aged over 20 years rose from 8.3% in 1989 to 11.6% in 1995 [23] , while in denmark, a 38% rise in diabetes prevalence has been reported over a 22year period [24] . in our recent national study in australia, 7.4% of adults were found to have diabetes compared to an estimated 3.4% in 1981 [18] . our studies in mauritius have provided a future guide to the magnitude of the global diabetes epidemic [25] . the population of this nation are asian indian, creole (black) and chinese, and these three ethnic groups account for over 66% increasing prevalence of type 2 diabetes by region [12] . of the world's population. mauritians have a high diabetes prevalence [26] and a 40% secular increase occurred between 1987 and 1992 in mauritian asian indians and creoles [27, 28] . the mauritian chinese share this high prevalence [26] . data showing that the prevalence of type 2 diabetes doubled between 1984 and 1992 in singaporean chinese, together with the high prevalence in taiwan [29, 30] , provide an alarming indicator of the magnitude of the anticipated epidemic in the people's republic of china (prc) [25] . in the prc, the prevalence of type 2 diabetes was, until recently, less than 1% [31] , but recent studies show a three-fold increase in prevalence in certain areas of china within the last two decades [22] . if china has just 50% of the prevalence of diabetes in taiwan, the number of individuals with diabetes will increase dramatically from 8 million in 1996 to well over 35 million by 2010. diabetes prevalence is currently estimated at 6.2% in the developed world, and forecast to rise to 7.6% by 2025 [13] . developing countries are starting from a lower baseline, at 3.5%, but this is set to increase by more than a third, to 4.9%, in 2025. the lower overall prevalence in developing countries conceals considerable heterogeneity between individual nations. in latin american countries, the crude prevalence of type 2 diabetes for 2000 ranges from 1.2% in chile to 8.2% in argentina [32] and in africa from 0.7% in tanzania to 10.0% in the northern sudan [33] . in asia, the overall prevalence is low in some countries, such as bangladesh (roughly 1-2%), but higher in others, such as pakistan (4-7%) [12, 13] . the pacific islands bear an especially heavy burden of diabetes, as described above, with an estimated prevalence of 7% in kiribati, 8% in the cook islands, 11% in fiji, and 24% in nauru [13] . increased rates of obesity due to low levels of physical activity and high-energy diets are driving this global epidemic [14] . for example, between 1990 and 1998, the average body weight of men and women in the usa increased by 3.4 kg and 3.9 kg, respectively, while the prevalence of diabetes increased from 4.9% to 6.5% [34] . obesity, particularly abdominal obesity, promotes the development of insulin resistance and the dysmetabolic syndrome (also known as the "metabolic syndrome", or "syndrome x") and, ultimately, type 2 diabetes [35] [36] [37] [38] . approximately one quarter of the population of the developed world are already believed to have the dysmetabolic syndrome [36, 39] . impaired glucose tolerance or impaired fasting glucose develop in response to worsening insulin resistance before the clinical diagnosis of type 2 diabetes is made, and signify an increased risk of developing type 2 diabetes [40] . between 10% and 25% of western populations may already have igt [21, 41] . for example, the australian diabetes, obesity and lifestyle study (ausdiab) recently surveyed the glycaemic status of a population of 11,247 adults [18] . the overall preva-lence of diabetes was 7.4%, but the combined prevalence of impaired fasting glucose or impaired glucose tolerance was more than twice as high, at 16.4%. these glucose-intolerant, but non-diabetic, individuals represent a reservoir of potential new diabetes cases. approximately 4-9% of individuals with impaired glucose tolerance go on to develop type 2 diabetes each year [42] . demographic, social and cultural factors profoundly influence the prevalence of diabetes in a developing nation, as shown by recent studies in india. the overall prevalence of diabetes in that country was estimated at 4.0% in the year 2000 [13] . however, a survey in madras, an urban area of southern india, showed that the prevalence of diabetes had risen by 40% between 1988-1989 and 1994-1995, and by a further 16% in the year 2000 [25, 43] . increasing urbanisation and sedentary work was significantly associated with this increased prevalence [44, 45] . indeed, 12% of urban residents, and only 2% of rural residents were found to have type 2 diabetes in this survey. south asians who migrate to developed nations face a similar increase in the risk of developing diabetes [46, 47] . a greater tendency to insulin resistance is already evident in children of south asian descent in the uk, which is associated with a steeply rising incidence of type 2 diabetes [48, 49] . the impact of urbanisation on diabetes prevalence in india is consistent with experience from other cultures, such as australian aborigines, pacific islanders and native americans [17, 50] . global estimates predict that the ratio of people with diabetes in urban and rural areas in the developing world will rise from 1.5-fold, at present, to more than 3-fold in 2025 [13] . other socio-economic factors, particularly poverty, also increase the risk of type 2 diabetes [51] . patients with a diagnosis of diabetes represent the tip of the iceberg, and a large number of patients with undiagnosed diabetes may also be at risk of adverse clinical outcomes. in the ausdiab study, there was one undiagnosed case for every known case of diabetes [18] . an observational study carried out in an apparently healthy, elderly (70-79 years) population in the us revealed that 8% of the 3,075 participants had undiagnosed diabetes. higher estimates have been observed in patients with a previous mi (12%; [52] ) or awaiting coronary angioplasty (17.9%; [53] ). a study in the uk, which surveyed 553 subjects without known diabetes in an impoverished urban area, illustrates how genetic and socioeconomic factors combine to amplify the problem of undiagnosed diabetes [54] . the age-adjusted prevalence of diabetes in this population was high in subjects of south asian or african-caribbean descent (33% and 22%, respectively), as would be expected from earlier studies. however, the age-adjusted prevalence of type 2 diabetes was unexpectedly high (20%) in subjects of european descent. similarly, data from the third us national health and nutrition examination survey suggested that the adult prevalence of undiagnosed type 2 diabetes nationwide was 2.7%, though this concealed wide vari-6s12 diabetes metab, 2003,29,6s9-6s18 • www.e2med.com/dm p zimmet ations between men and women and between ethnic groups [21] . for example, the prevalence of undiagnosed diabetes among middle-aged (50-59 years) mexican-american men and women was 12.9% and 7.5%, respectively, compared with 3.3% and 5.8%, respectively, for the general population within this age range. there is compelling evidence that undiagnosed diabetes is associated with cardiovascular risk factors characteristic of insulin resistance or the dysmetabolic syndrome, including hypertension and abdominal obesity [53] [54] [55] . the additional increases in metabolic dysfunction associated with westernisation and urbanisation of the developing world, as described above, can only exacerbate this problem in the future. type 2 diabetes mellitus in children, teenagers and adolescents is a serious new aspect of the type 2 diabetes epidemic and is an emerging public health problem of significant proportions [14] . while, globally, type 1 diabetes is still numerically the major form in children, it is likely that type 2 diabetes is set to be the predominant form within 10 years in many ethnic groups and potentially in europid groups. type 2 diabetes has already been reported in children from japan, the united states, pacific islands, hong kong, australia and the united kingdom [14] . the prevalence of type 2 diabetes in the general population of the usa has been estimated at 4.1/1000 12-19 year olds [56] . dabelea et al. have studied pima indian children since the late 1960s, and have demonstrated rising rates of glucose intolerance with time and age, as well as a female preponderance [57] . from 1967-76 to 1987-96, the prevalence of type 2 diabetes has markedly increased from 2.4% in males and 2.7% in females to 3.8% in males and 5.3% in females. diagnoses of type 2 diabetes now outnumber diagnoses of type 1 diabetes by 4:1 in children in parts of japan and china, compared with a ratio of about 1:3 of total diagnoses of diabetes in urban usa centres [58, 59] . obesity and insulin resistance are driving this explosion of paediatric diabetes, as in adults [60] . a diagnosis of diabetes has a profound impact on life expectancy, and a patient diagnosed with type 2 diabetes in middle age (40-49 years) stands to lose as much as 10 years of life expectancy [61] . given the close association between type 2 diabetes and the cardiovascular risk factors constituting the dysmetabolic syndrome, it is not surprising that most type 2 diabetic patients ultimately die from a cardiovascular cause [62] . indeed, type 2 diabetes confers the same degree of risk of premature death as a previous myocardial infarction in a non-diabetic subject [63] . a substantial proportion of type 2 diabetic patients already have diabetic complications at the time of diagnosis of diabetes. for example, retinopathy, peripheral neuropathy and proteinuria were present in 35%, 12% and 2%, respectively, of the newly-diagnosed patients in the uk prospective diabetes study (ukpds) at baseline [64] . the cost of diabetes in europe -type 2 (code-2) study has investigated the prevalence of diabetic complications in a randomly selected cohort of type 2 diabetic patients. less than half (41%) of the german cohort of 2,701 patients (mean age 67 years) did not have diabetic complications, while 23% had at least two, and 3% had at least three complications [65] . cardiovascular complications were present in 43% of patients, cerebrovascular complications in 12%, and neuropathy or diabetic foot syndrome, retinopathy and nephropathy were present in 23%, 11% and 6% of patients, respectively. the code-2 data are consistent with previous estimates of the prevalence of coronary heart disease and other complications in type 2 diabetic patients in various countries (fig 2) . the prognosis of type 2 diabetes in patients who already have diabetic complications is extremely poor. a retrospective review of 126 patients referred to a combined diabetesrenal clinic showed that their median survival was only 61 months [66] . similarly, odds ratios for all-cause and cardiovascular mortality in 104 finnish type 2 diabetes patients with diabetic retinopathy were 5.1 and 5.6, respectively, compared with non-diabetic control subjects [67] . diabetes is expensive to manage, and the per capita costs of managing a diabetic patient are 2-4-fold higher than for a non-diabetic patient [68] . however, the additional cost burden associated with type 2 diabetes begins long before diabetes is diagnosed. analysis of data from a managed care organisation in the usa showed that the cumulative costs associated with inpatient, outpatient and pharmacy provision for patients with type 2 diabetes were higher, on average, than those incurred by control subjects matched for gender and age for each of the 8 years preceding diagnosis of diabetes [69] . by the time of diagnosis, the total cost of treatment was $9,643 higher for a diabetic patient, compared with a control subject (fig 3) . costs for the 8 years following diagnosis were higher in diabetic subjects, as would be expected, with a total difference in average total costs of $18,057 between a type 2 diabetic patient and a matched control subject (fig 3) [70] . most of the cost of managing type 2 diabetes is associated with the management of diabetes-related complications, especially where hospital treatment is required. the ukpds performed separate health economic evaluations, based on the main cohort, who were managed with conventional dietbased treatment or intensive glycaemic management with a sulphonylurea or insulin [71] , and on overweight patients, who were managed with diet or with intensive metforminbased treatment [72] . the total costs incurred during 11 years of follow-up are shown in table i . managing complications accounted for about two-thirds of the total costs in the diettreated group of the main cohort, and about three quarters of the costs in diet-treated overweight patients. complications accounted for more than half of the total costs during follow-up even after intensive glycaemic management with a sulphonylurea or insulin (main cohort) or metformin (overweight cohort), which significantly reduced the incidence of microvascular and macrovascular complications, respectively [64, 73] . comparing the health economic costs between countries is difficult, because of variations in the costs of services and standard clinical practice, and variations in how data are presented. however, in general terms, the cost of managing complications drives the overall treatment costs in most countries. fig 4 compares the average annual costs of managing a type 2 diabetic patient across europe: in most countries, costs arising from hospital treatment (mainly associated with the management of complications) were markedly greater than out-ofcolumns show the average of estimates of the prevalence of individual complications for adults with type 2 diabetes presented by amos et al. [12] . numbers beneath columns show the number of estimates used in each case. chd: coronary heart disease; pvd: peripheral vascular disease. cumulative costs of managing a type 2 diabetic patient and an age-and gender-matched control subject in a managed care organisation over a period of 8 years before (a and b) or after (c and d) the diagnosis of diabetes [69, 70] . hospital (ambulatory) costs [51] . data from the usa, from a model based on the interventions used in the ukpds, show that the annual costs of managing complications in patients receiving diet-based therapy ($37,602) accounted for 78% of total direct costs of care ($48,343) [74] . a retrospective analysis of 11,768 patients within a managed care organisation in the usa compared the costs of diabetes management in type 2 diabetic patients with no evidence of significant cardiovascular or renal disease ("no complications"), in patients under treatment or investigation for risk factors for cardiovascular or renal conditions ("pre-event"), and in patients with a history of cardiovascular events or clinically significant renal dysfunction ("post-event") [75] . direct costs were lowest in the "no complications" group (fig 5) , and increased in the "preevent" group for men and women. however, the greatest differences in costs were between the "pre-event" and "postevent" groups, with a greater than doubling of costs for patients who developed cardiovascular complications. data are from separate analyses, from the perspective of a healthcare purchaser. all costs are undiscounted direct costs and are in uk £ (1997 values). additional costs for specialist care were for eye or renal care in lean patients and eye care in overweight patients. the analysis in lean patients presented individual costs from the clinical trial setting and adjusted the total for the routine community care setting; the analysis in obese patients presented all costs after adjustment for the routine care setting, hence na (= not available) for trial costs for overweight patients. the percentage of costs due to complications was calculated using trial costs for lean patients and standard practice costs for overweight patients, for the same reason. total costs (in uk £) associated with type 2 diabetes and its management during 11 years of follow-up in the uk prospective diabetes study [71, 72] . direct medical costs per type 2 diabetic patient in some european countries in 1998 [51] . additional treatment costs arising from the development of cardiovascular or renal diabetic complications [75] . costs are in 1993 prices from the perspective of a health care purchaser. patients were stratified as follows. no complication: patients in the analysis either had no history of cardiovascular or renal disease or treatment; pre-event: patients were under treatment with an antihypertensive drug, had made at least two visits to a cardiologist, or had had at least one positive test for microalbuminuria; post-event: patients had suffered at least one major cardiovascular event (e.g. myocardial infarction, stroke, revascularisation, or hospitalisation for congestive heart failure) or had documented clinical renal dysfunction indicated by high serum creatinine measurements. the high prevalence of type 2 diabetes means that the overall costs of managing the disease, including costs arising from managing diabetic complications, are high enough to place a substantial burden on national economies. the total direct healthcare expenditure on the management of diabetes in the usa in 1997 was $44 billion. of this amount, only $7 billion was required for glycaemic management, with $36 billion required for the management of complications and other problems related to diabetes [76] . the total costs of managing type 2 diabetes in europe already range between roughly 2% and 8% of national healthcare budgets in europe (fig 4) . the burden on some other economies is even higher. for example, diabetes care in mexico accounts for 15% of the total healthcare budget, which equates to 0.8% of gross domestic product [77] . moreover, the burden grows heavier as the global epidemic of type 2 diabetes evolves. projections based on the uk diabetic population suggest that the total costs of managing type 2 diabetes will increase from £1.8 billion in 2000 to £2.2 billion by 2040, an increase of 24% [78] (fig 6) . national governments have either failed to recognise the future socioeconomic burden of type 2 diabetes or are ignoring it. the global epidemic of type 2 diabetes is already threatening healthcare budgets, and the burden will continue to increase. we should not forget that these prevalence figures relate to people with a clinical diagnosis of type 2 dia-betes. many more people have undiagnosed diabetes, and there is a vast reservoir of people with igt, most of whom will develop diabetes eventually, and who are already at substantial risk of developing cardiovascular disease [40] . increasing rates of obesity will place ever more people at risk of developing the dysmetabolic syndrome, type 2 diabetes, and cardiovascular disease. the increasing prevalence of type 2 diabetes in children and adolescents underlines the urgency of taking action. the diabetes prevention program has shown us that preventing type 2 diabetes with lifestyle interventions or with pharmacologic therapy is cost-effective in either the european or american settings [79, 80] . however, extending these benefits beyond the tightly-controlled structure of a randomised clinical trial will require an unprecedented degree of public health intervention. educating the public on the dangers of obesity and glucose intolerance will certainly be important. some steps in this direction have been made. for example, efforts are underway to improve the lifestyles of school-age children in japan [81] , and health workers in philadelphia in the usa patrol the streets armed with weighing machines to spread the message of the dangers of obesity [82] . in finland, a simple questionnaire is being used as a screening tool to identify citizens at risk of type 2 diabetes, who may benefit from further follow-up and intervention [83] . mounting a successful challenge to the diabetes epidemic, however, will require major alterations to the structure of society. for example, the intervention in finland is being mounted in collaboration with a broad range of governmental agencies and healthcare advocacy groups, as part of a broader strategy dating back several decades [84] . support from the highest level of governments is also needed, as resources to mount diabetes prevention efforts must be made available, and changes to taxation and reimbursement structures relating to resources for people to improve their lifestyles would also certainly help in the longer term. the rising tide of type 2 diabetes and its complications will place an increasingly heavy burden of morbidity and mortality on patients and their families for decades to come. moreover, the expenditure required to manage these patients will stretch the healthcare systems even of the richest countries. all involved in the provision of healthcare, including the full range of healthcare professionals, professional societies, patient advocacy groups, healthcare agencies, or any level of government, bear a share of the responsibility for halting the diabetes epidemic. above all, action is required immediately, if we are to stand any chance of success. diabetes mellitus in american (pima) indians the high prevalence of diabetes mellitus on a central pacific island the high prevalence of diabetes mellitus in nauru, a central pacific island all-cause mortality and cardiovascular disease mortality in three american indian populations, aged 45-74 years, 1984-1988. the strong heart study the prevalence and health burden of self-reported diabetes in older mexican americans: findings from the hispanic established populations for epidemiologic studies of 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glucose-intolerant patients: modelling the long-term implications of the diabetes prevention program in the french, german and uk settings costs associated with the primary prevention of type 2 diabetes mellitus in the diabetes prevention program descriptive epidemiology of non-insulin dependent diabetes mellitus detected by urine glucose screening in school children in japan us public health and the 21 st century: diabetes mellitus the diabetes risk score: a practical tool to predict type 2 diabetes dehko: development programme for the prevention and care of diabetes in finland key: cord-284608-ba7wq52t authors: sias, catia; salichos, leonidas; lapa, daniele; del nonno, franca; baiocchini, andrea; capobianchi, maria rosaria; garbuglia, anna rosa title: alpha, beta, gamma human papillomaviruses (hpv) detection with a different sets of primers in oropharyngeal swabs, anal and cervical samples date: 2019-03-04 journal: virol j doi: 10.1186/s12985-019-1132-x sha: doc_id: 284608 cord_uid: ba7wq52t background: recent studies have shown a 13-fold increase of oropharyngeal cancer in the presence of hpv, while α-hpv detection seems to be rare in oral cavity in comparison to anal or cervical district, many novel β and γ types have been isolated in this anatomical site suggesting a wide tropism range. currently, there are no guidelines recommending hpv oral cavity screening as a mandatory test, and it remains unknown which hpv types should be included in hpv screening programs. our goal was to assess hpv prevalence in oropharyngeal, anal, and cervical swabs using different sets of primers,which are able to amplify α, β, γ hpv types. methods: we analysed the presence of hpv dna in oropharyngeal (n = 124), anal (n = 186), cervical specimens (n = 43) from hiv positive and negative patients using fap59/64 and my09/11 primers. all untyped strains were genetically characterized through pcr amplification and direct sequencing of partial l1 region, and the resulting sequences were classified through phylogenetic analysis. results: hpv prevalence was 20.9% in 124 oropharyngeal swab samples, including infections with multiple hpv types (5.6%). hpv prevalence in this anatomical site was significantly associated with serostatus: 63.3%in hiv positive and 36.3% in hiv negative patients (p < 0.05). unclassified types were detected in 6 specimens. in our analysis, we did not observe any difference in hpv (α, β, γ) prevalence between men and women. overall, β species were the most frequently detected 69.7%. when using anal swabs, for hiv positive patients, β genus prevalence was 1% and γ genus was 3.7% including 6 unclassified types. in cervical samples from 43 hiv positive women (18 hpv negative and 25 positive by my09/11 pcr), only one sample was positivite for β(1) species (2.4%) using fap primers. six of the untyped strains clustered with sequences from species 7, 9, 10, 8,12 of γ genus. four sequences remained unclassified. finally, β and γ hpv prevalence was significantly lower than their respective hpv prevalence as identified by the luminex system in all anatomical sites that were analyzed in previous studies. conclusion: this study provides new information about viral isolates present in oropharyngeal site and it will contribute to improve the monitoring of hpv infection. electronic supplementary material: the online version of this article (10.1186/s12985-019-1132-x) contains supplementary material, which is available to authorized users. human papillomavirus (hpv) persistent infections are considered the primary cause of ano-genital cancer, where greater than 99% of cervical cancer and more than 60% of anal cancer contain hpv dna [1, 2] . throughout the past years, several studies have suggested the link between hpv infection and other epithelial cancers, including cutaneous and oropharyngeal cancers. oropharyngeal cancers are often referred to as "head and neck cancer" (hnc), and mainly include squamous-cell carcinoma which occurs in the oral cavity, base of tongue, tonsils, adenoids pharynx and larynx. recent studies on hpv infection in oral exfoliated cells have shown that there is a 13-fold higher risk for oropharyngeal cancer in the presence of virus [3] [4] [5] . the highest prevalence (up to 50%) for these hpv associated cancers has been found in the tonsillar cancers sub-set [6] [7] [8] . since hpv16 presented a global prevalence in oropharyngeal squamous cell carcinoma (opscc) and oral squamous cell carcinoma (oscc) of 40.6 and 14.9% respectively [9] , iarc categorized this genotype as a risk factor with for the pathogenesis of both cancers [10] . additionally, other hpv types have also been linked with these cancers, including hpv18, 31, and 33 [11] including β and ɣ types [4] . furthermore, while α-hpv detection seems to be rare in oral cavity in comparison to anal or cervical districts [12] , many novel β and γ types have been isolated in oral cavity [13] suggesting a wide tropism range of these genera [14] . at the same time, different studies on hpv prevalence provided contradicting result for β and ɣ types not only in oropharyngeal site, but also in cervical and anal anatomical sites [14] [15] [16] [17] [18] [19] . to date, there are no guidelines recommending hpv oral cavity screening as a mandatory test, and no hpv dna test has been approved for hpv detection in oral cavity. in addition, it remains unknown which hpv types should be included in oral cavity screening. agalliou [4] highlighted the link between β, γ hpv types and oral cancers, assessing the presence of hpv types which are not generally detected with commercial assays in cervical cancer screening. even though different methods have been used to detect novel hpv types, the association between new β and γ hpv types and oral cavity cancer has not yet been established. in this study, we analyzed the presence of hpv dna in oral, anal, and cervical specimens collected from hiv positive and hiv negative individuals, living in the same geographic area (regione lazio) by using my09/11 [20, 21] fap59/64 primers [22] . these primers, both targeting highly conserved region within l1 orf, are considered broad range pv primers and allow the detection of the great majority of already known and officially recognized hpv types. my09/11 had been used in α hpv detection in cervical sites, where they showed good sensitivity in alpha hpv types amplification [21] , while fap primers officially recognized hpv from α-pv, β-pv, and ɣ-pv genera, and might detect potentially new types [22] [23] [24] [25] . this property is particularly relevant, since ɣ and β papillomaviruses have been already identified in several anatomic sites [14, 26] . granted that that hpv prevalence is significantly higher among hiv infected people and at multiple anatomic sites [26] [27] [28] [29] we included both hiv positive and hiv negative people in our study in order to also verify whether β and ɣ hpv positivity is influenced by host immune status. this is a retrospective study carried out at laboratory of virology inmi l spallanzani on residual oropharyngeal samples collected for respiratory virus detection, anal and cervical swabs collected for hpv testing in diagnostic routine. the hospital ethics committee approved the protocol. date of birth, date of swabs sampling, hiv serostatus were recorded from institutional database. in hiv positive patients, the most recent cd4 t cell count (± 1 month from the date of sample collection) and hiv rna viral load (± 1 month from the date of sample) with a detection limit of 40cp/ml (abbott molecular inc., des plaines, il, usa) were used to correlate clinical features and hpv positivity. oropharyngeal swabs -oropharyngeal samples were collected as following: the nylon-flocked tip was rotated 3-4-times against right and left buccal mucosa, palatine, tonsils, upper and lower pharynx area. the swab was then plunged and stirred in 1.5 ml dmem medium with streptomycin and ampicillin. specimens were refrigerated within 3-5 h after collection until processing. anal swabs -we retrospectively analysed 186 anal swabs previously tested by my09/11 primers and typed by clart hpv2 clinical array or sanger sequencing (see hpv detection and typing section, below). one hundred samples belonged to hiv positive women (50 hpv positive by my09/11 pcr and 50 negative by my09/11 pcr), 86 anal swabs were collected from men who have sex with men (msm). all msm specimen resulted positive in my09/11 pcr. cervical swabs -a total of 43 cervical swabs (18 hpv negative and 25 hpv positive, assigned by my09/11 pcr) were considered in this study. all samples belonged to hiv positive women. general characteristics of hiv infected patients are presented in additional file 1: table s1 . oropharyngeal swabs were removed from the medium which we divided in two parts: half part was used for detecting respiratory viruses panel (influenza-a, b, rsv, rhinovirus, coronaviruses, metapneumovirus, adenovirus) and the other half was employed in testing hpv dna, having been stored at − 80°c until use. before nucleic acid extraction, all specimens were pre-treated. briefly, 600 μl of clinical material was digested with 20 μl proteinase k solution (qiagen, hilden germany) and lysed with al lysis buffer (qiagen, hilden, germany) at 56°c for 10 min. nucleic acid extraction was done with a magnetic bead-based automated platform (qiasymphony, hilden, germany) in accordance with the manufacturer's instructions. nucleic acids were eluted in 60 μl of ave elution buffer (qiagen, hilden, germany). nucleic acid from anal and cervical swabs were extracted as described elsewhere [30, 31] . samples that were β-globin negative were excluded from the study [32, 33] . ten μl of eluted nucleic acids were employed for evaluating the presence of hpv types by using my09(5'cgtccmarrggawactgatc3') and my11(5'gcmcagggwcataayaatgg3') [20, 21] pcr and faststart dna polymerase (roche diagnostics gmbh, mannheim, germany). the pcr assay conditions were: 95°c for 5 min, then 39 cycles (denaturation 95°c/30 s, annealing 55°c/45 s, and extension 72°c/1 min). one last step for extension was employed at 72°c for 10 min. fifteen μl of the pcr products were mixed with 6 loading solution in 1.8% agarose gel electrophoresis stained by ethidium bromide and run for 30 min at 130 v. hpv genotyping of positive samples was conducted using genomica clinical hpv array (genomica, madrid, spain). clart hpv2 clinical array hpv is able to detect: 6, 11, 16, 18, 26, 31, 33, 35, 39, 40, 42, 43, 44, 45, 51, 52, 53, 54, 56, all adequate samples were retested using fap 59 (5'taacwgtiggicayccwtatt3') and fap 64 (5'ccwatatcwvhcatitciccatc3') primers [22] able to detect α, β and γ hpv types. faststart dna polymerase were used in this assay condition: 5 min at 94°c, 40 cycles (denaturation 94°c/30 s, annealing 52°c /45 s, and extension 72°c 1 min) followed by a final extension step at 72°c for 7 min. pcr products were also run on agarose gel. positive samples with fap set of primers and those positive with my09/11 pcr protocol, but negative in genomica typing assay were purified and sequenced on the automated abi prism 3100 instrument, by using a bigdye terminator cycle sequencing kit (applied biosystems, warrington, uk). hpv sequences were aligned using mafft [34] using the l-ins-i method. after visual inspection using seaview [35] we removed sample sequence q1359 and q1017 were excluded from the alignment because they represented mixed infection and the sanger sequence interpretation was not optimal. reference sequences hm999999_hpv147 and gu129016_hpv148 were also excluded from the alignment. then, we further implemented gblocks [36] to remove ambiguous positions using the least stringent options. to infer a maximum likelihood tree, we implemented raxml [37] using a gtrcat model, with 100 bootstrap replicates. tree visualization was achieved using figtree [38] . finally, pairwise similarity matrices were constructed using blast. oropharyngeal swabs-a total of 124 oropharyngeal swabs with β-globin positive signal were considered in this study. hpv prevalence was 20.9% (26/124), including infections with multiple hpv types (7/124, 5.6%) ( table 1 ). my09/11 pcr gave positive results in 18 samples. however, a blast search against genbank indicated that 5 amplified fragments were identical to human sequences (5/124, 4%), thus true hpv positive rate was estimated at 10.5%. out of 13, three samples were identified as α and ten as β types. alpha-types were detected in two hiv positive patients (2/55, 3.6%), and in 1 hiv negative patient. hpv α-types, 16 and 70, were detected in hiv positive subjects (2/55, 3.6%) after being typed by clart hpv2 clinical array, while hpv13 was amplified in hiv negative subject (1/69, 1.4%); it was typed by sanger sequencing. all β hpv types belonged to β 2 species (table 1) , and hpv145 was the most frequent type (4/10), both in hiv positive and hiv negative patients; 20 samples were identified as positive by fap pcr. no specific amplicons were observed. seven fap-detected hpv types were found in samples that also gave positive results with my09/my11 pcr (table 1) . types β 1 were the most represented (n = 13), while one sample was identified as γ type (hpv132, γ 12 ). additionally, one mixed infection (q1017) and 5 untyped hpv strains were also detected. among β 1 species, the most frequent types were hpv5 (n = 5, 38.6%) and hpv19 (n = 5, 38.6%). three multiple infections harboured β 1 and β 2 types, whereas β 2 types and untyped strains were observed in 4 other multiple infections. no multiple infection harboured α with β or γ species (table 1) . overall, β species were most prevalent (n = 23/33, 69.7%). hpv distribution differed significantly when the number of hpv β, γ-types were considered in hiv positive and hiv negative subjects: 21 (21/33, 63.6%) vs 12 (12/33, 36 .3%) respectively (chi square test, p < 0.005). hiv positive people with hpv in oropharyngeal swabs showed a mean cd4 t cell count of 532.3 ± 275.6. among hiv positive patients with detectable hpv, 6/16 had no detectable hiv rna in plasma and the other patients (n = 10) showed a mean rna copies/ml169.0 ± 130.0. hpv prevalence rates were compared for statistical significance, using a chi squared test, in men and women both hiv positive and hiv negative. however, no difference was observed (chi square test, p > 0.05). anal swabs-eighty-six anal swabs from msm resulted positive by my09/11 pcr, and 100 anal swabs from women (50 hpv positive by my09/11 pcr and 50 negative by my09/11 pcr) were retested with fap primers. among msm anal swabs, 15 samples showed single hpv infection by clart array testing, and 71 patients harboured multiple hpv infection with at least one high risk (hr) type. in 61.2% of samples we observed a clinically evident anal pathology, including 7 subjects with anal intraepithelial neoplasia (ain) ii, 46 patients with ain i. among hpv positive women, 18 harboured a single infection (ain ii, n = 0; ain i, n = 5); atypical squamous cells of undetermined significance (asc-us), n = 0; normal, n = 13) and 31 samples showed hpv multiple infection, all with at least 1hr type (62%) (ain 2,n = 0; ain i, n = 9; normal cytology, n = 22). hpv type was undetermined in one sample. among single infection with ain i, one specimen was infected with a low risk (lr)type (hpv81). nineteen anal swab specimens were identified as hpv positive by fap primers detection (female anal swabs, n = 3; male anal swabs, n = 16) ( table 2 ). overall α-type strains were detected in 9 samples with fap primers which were not previously detected by my09/11 primers. all but one α-type strains were also detected with α mucosal hpv multiple infection typed with clart hpv2 clinical array which included at least one hr type. hpv β 2 types (hpv9 and hpv37) were found in two specimens co-infected with α hpv types; 2 specimens harboured γ 10 hpv types (hpv121 and hpv180), both associated with type α hpv multiple infections. all fap untyped strains (n = 6) were found in anal specimens infected by α types with at least one high hr type. considering cytological aspects, 12/19 samples, which resulted positive with fap primer pcr, had ain (i, ii) lesions, while 7/19 samples showed normal cytology (table 2) . among anal swabs from females (n = 100), only 3 samples (3.0%), previously tested my09/11 hpv positive, resulted hpv positive with fap primer (hpv32, α 1 species; hpv114, α 3 species; hpv90, α 14 species). no untyped hpv strains were observed among female samples. overall, β genus prevalence was 1% and γ genus was 3.7% including untyped isolates. mean of cd4 t cell count was 690.7 ± 343.9 cells/μl. overall 170/186 patients (91.4%) were under antiretroviral therapy (art). all patients without art had a cd4 t cell count > 400/ μl. current art use was not associated with risk of β and ɣ infection (chi square test, p > 0.05). cervical swabs-twelve specimens showed a single hpv infection, and 13 had multiple infections by clart hpv2 array; 17/25 samples harboured at least 1 hr genotype. cytology findings were available for 20 specimens already resulted positive by clart hpv2 clinical array: 10 had normal cytology, 6 were asc-us or low grade squamous intraepithelial lesion (lsil), 3 harboured hpv single infections, 3 showed hpv multiple infections, and 4 were high grade squamous intraepithelial lesion (hsil). all my09/11 hpv negative women (n = 18) showed normal cytological findings. eleven/43 cervical samples resulted fap positive (25.6%). however, only 6 hpv types were not previously detected by my09/11 primers. five samples harboured α types (hpv90, n = 3 α 14 ; hpv32, n = 1, α 1 ; hpv68 α 7 , n = 1), and only one specimen gave positivity for β 1 (hpv14) (2.4%). the mean cd4 t cell count was 539 ± 230 cells/μl. ninety-six percent of women were receiving art per who guideline of starting art at cd4t cell count < 350 cell/mm 3 . the woman harboring β hpv strain was under art. she had a cd4 t cell count of 540 cells/μl and hiv rna viral load was not detected. overall cervical and anal β and γ type positivity was not related to immune status as measured by cd4 t cell count (see table 2 ) and art treatment. furthermore, the immune-re constitution could potentially prevent the persistence of β and ɣ types in anal and cervical sites or alternatively, β and ɣ types might show to have a less tropism to these anatomical sites. for the phylogenetic analysis of our untyped hpv samples we used 10 partial cds sampled sequences from major capsid protein l1 fap pcr products and 59 reference sequences. our reference sequences represent 50 classified and 9 untyped hpv sequences (see table 3 ). according to our phylogenetic analysis, 6 of our sampled sequences (q1766, q1644, q760, q337, q656 and q654) clustered with previously classified reference sequences from species 7, 10, 8, 12 and 9 -γ genus. sequences q763, q1234, q2164 and q127 remained unclassified while showing great similarity with unclassified genomic regions af489714 (fams9), kp692119, and af217684.1 respectively (see fig. 1 and table 3 ). in hnc, particularly oropharyngeal cancer, the true prevalence and involvement of hpv in the carcinogenetic process is still unknown. in fact, many studies report low prevalence of hpv obtained with systems used for the determination of hpv in cervical cancer screening (specific for α types), while other authors found higher prevalence when they used a platform able to detect hpv types belonging to genera other than α genus [4] both in oral cavity and in oral cancer [4, 39] . agalliu recently found a correlation between the infection of some β, ɣ hpv types and oscc [4] . furthermore, a recent meta-analysis provided additional evidence of the involvement of β hpv types in the development of scc in immunocompetent individuals [40] . additionally, several mechanistic studies have consistently showed that e6 and e7 from several β hpv types are able to target cellular proteins, such as p53 and prb, and to deregulate fundamental events involved in cellular transformation [41] . thus β and ɣ hpv types detection could be included in a hpv screening test for oral cancer prevention, while a correct and suitable detection of hpv infection is becoming a priority. currently, there are few studies that compare the hpv prevalence obtained using the protocols, which are normally for cervical cancer screening with those obtained using methods that are able to detect hpv types belonging to genera other than α or new ones. in this study, in order to assess the impact of pcr system in hpv prevalence determination, we carried out the detection of hpv with my09/11 primer set, used in several genotyping molecular assays (for example linear array hpv genotyping test, roche molecular system, ca usa; clart hpv2 clinical arrays, genomica, madrid, spain,) and fap primers able to detect α, β, γ hpv types in several specimens. in oropharyngeal swabs samples, my09/ 11 primer set was able to detect 39.4% (13/33) of hpv positive samples, while fap set of primers detected the presence of hpv in 20/33 samples (60.6%). beta hpv was the main genus detected with a prevalence of 69.7% in hpv positive samples. this prevalence was in agreement with bottalico et al. that used fap primer and my09/11 for detecting hpv in oral swabs [14] . hpv5 was the most frequent β 1 type and hpv145 the main type among β 2 species as described by bottalico [14] . hpv38, which was reported as the main β 2 type in forslund study [42] , was absent in our samples. hr, namely hpv16, was observed only in one specimen from an hiv positive subject, whereas hr hpv were frequently observed in bottalico study group [14] . the low frequency of hr could be imputed to immune status of the patients. our patients were under haart therapy and most of them had a cd4 t cell count > 200 /μl. no severe compromise of the immune-system could have limited a persistence of hr in this anatomical site. unfortunately, no information was given in the bottalico paper on patient cd4 t cell count, and this fact did not allow a correct comparison of these results. according to previous data reported by forslund et al. [42] , no difference in hpv prevalence was observed among men and women suggesting that host specific factors could contribute to hpv persistence and neoplasia development. gamma genus represented 21.8% of hpv positive samples. to note, 6/7 γ strains were untyped. phylogenetic analysis revealed that 2 samples (q1766 and q1644) belonged to γ 7 species, while q656 to γ 12 species and q337 to γ 9 species. interestingly, the oral untyped genotypes fell in different genera and cluster with the anal untyped strains, suggesting a specific tropism of these gamma types for oral mucosa. gamma 12 and 7 were the most representative γ species described by bottalico in oral rinse and agalliu in hnc, suggesting their potential involvement in oscc development. unlike forslund and hampras [42, 43] , we did not identified any β 3, β 4, β 5 hpv types. this may be due to the types of biological samples that were used or to differences in the efficiency of extraction methods that were applied, which could have influenced the outcome of pcr [44] . finally, differences in results might also be explained by the geographical distribution of hpv types. in general, differences in hpv β and γ types and their prevalence were observed by the luminex platform. according to him study [43] , among β 1 genotypes, hpv12 and hpv5 were the prevalent genotypes. while, among β 2 strains, hpv38 was the most represented,and it was never detected in our samples. interestingly hr hpv38 was also the main β 2 type observed also in moscicki study, whereas hpv21 represented the main β 1 type [45] . a different pattern of β types could be related to a different cellular input as described in a previous study [46] , where several β hpv types showed essentially increasing prevalence with increasing dna input. beta hpv types 8, 14, 20, 21, 23, 38 , and 92 showed increased prevalence only in higher dna input groups [46] . this may impose compromises in comparisons between studies; for example, our hpv38 negative result could be explained by an insufficient dna input in the pcr assay. further research is needed to establish whether there is an influence between cell number input and hpv β detection in oropharyngeal anatomical site and which cut-off would be suggested to avoid false negative results. possible type-specific differences in sensitivity to cellular input have to be evaluated in wider studies. if they are confirmed, they may be explained by the different sensitivities in detection systems and/or in the fig. 1 a maximum likelihood phylogenetic analysis was inferred on 10 unknown collected samples (bold) and 59 reference sequences using the gtrcat model. out of 10 unknown samples, 6 sequences were clustered within previously classified hpv species lineages. bootstrap supports lower than 70% were excluded from the tree. genbank accession number: mh647655-mh647663 different viral load spectra. we detected 9 α strains in anal site fap primers that had not been typed by genomica, and 2 β 2 types, hpv9 and hpv37, that had not been reported among oropharyngeal swabs. βeta types frequency was sensibly lower to that found by luminex system reported by torres et al. [17] which found 65.6% of β types in anal swabs from hiv positive msm and 59.1% among hiv negative msm. in this study, hpv12 and hpv 107 were the prevalent types among β 1 species, while hpv38 and hpv120 were the most frequently observed β 2 types. among γ genus, the γ 10 species was the most prevalent in both msm hiv positive and -negative groups, while we observed only γ untyped strains. donà reported higher prevalence of β (27.6%) and γ types (29.3%) in a group of msm similar to ours using the luminex system [16] . some hypothesis could put forth to explain these data: i) the luminex system could be much more sensitive than the fap system, or ii) that cross-reactivity could occur in β and γ types detection when α multiple infections are present. in literature, cross-reactivity was also observed among α genotypes. preisler observed cross-reactivity both in lr and hr genotypes using hc2, cobas, and aptima assays, despite what manufacturer claims: about 25% of hpvdna results in primary screening accounting for cross-reactivity, regardless of the assay [47] . to obtain improved analytical and clinical performance, cross-reactivity studies should be focused, since this aspect could influence the effectiveness in a future head neck hpv cancer screening. in cervical swabs the fap primers mainly showed the presence of α genotypes (hpv90, α 14 ; hpv32, α 1 ) which were not detected by clart hpv2 clinical array/ my09-11primers and 1 β 1 type (hpv14). this low prevalence of β types confirms the data reported by bottalico et al. [14] , which found a prevalence of 1% of the β types and 3% of the γ types in the cervical samples, emphasizing a weak β and γ type tropism towards the female genital mucosa. however, the genotypes hpv93 and hpv124, detected by bottalico in cervical specimens, were never observed among our cervical samples, suggesting a different geographic distribution of hpv β and γ type similarly to that described for α genus. conversely, these findings were in disagreement with those obtained by luminex system, as described in previous study [18] . a quantitative detection of the viral load in hair follicles demonstrated that the β genotype copy number was considerably lower than that reported for mucosal high-risk types from α genus in cervical tissue [48] . thus, only comparable viral load detection studies with different methods and the potential for multiple infections detection could explain these differences in prevalence of β types, which are reported in literature. overall, our results confirmed a prevalence of > 20% for hpv strains in the oropharyngeal anatomical district. the genus β and γ were predominant when the analysis was carried out with fap primers. the discrepancy on the prevalence and hpv types reported in other studies [16] [17] [18] 49] seems to be due to the detection system: highest prevalence was always obtained with the luminex system. different sensitivity and specificity of hpv detection methods were also a problem in the determination of α hpv types, as described in a systematic review where approximately 30-60% of all positive results showed discordance [50] . a global proficiency program like labnet for α types in cervical hpv infection surveillance programs should be planned also for α, β and γ hpv type detection in oropharyngeal samples [51] . standardizing methods for oral sample collection and hpv detection would ensure comparability between different detection methods in oral cavity samples [52, 53] . in addition, considering that γ genus has been growing rapidly (currently 98 γ types have been identified) surpassing α and β genera, and that 77% of the new types deposited in the hpv center within 2015 belonged to γ genus [54-56], our data reinforces the relevance of using primer sets able to detect a wide spectrum of hpv strains including β and γ types as well as new genotypes for hpv detection in the oropharyngeal anatomical site. this seems to be a crucial point since the meta genomic approach applied in some analysis [13] should be used with caution, taking in account the possibility of having an overestimation of hpv types [57] and requiring a confirmation of positivity by the sanger method. additional file 1 worldwide burden of cancer attributable to hpv by site, country and hpv type casecontrol study of human papillomavirus and oropharyngeal cancer associations of oral α-, β-, and γ-human papillomavirus types with risk of incident head and neck cancer detection and quantitation of human papillomavirus (hpv) dna in the sera of patients with hpv-associated head and neck squamous cell carcinoma hpv infections and tonsillar carcinoma human papillomavirus (hpv) in head and neck cancer. an association of hpv 16 with squamous cell carcinoma of waldeyer's tonsillar ring incidence of human papillomavirus (hpv) positive tonsillar carcinoma in stockholm, sweden: an epidemic of viral-induced carcinoma? hpv dna, e6/e7 mrna, and p16ink4a detection in head and neck cancers: a systematic review and meta-analysis preventable exposures associated with human cancers prevalence of microsatellite instability, inactivation of mismatch repair genes, p53 mutation, and human papillomavirus infection in korean oral cancer patients oral human papillomavirus in healthy individuals: a systematic review of the literature characterization of three novel human papillomavirus types isolated from oral rinse samples of healthy individuals the oral cavity contains abundant known and novel human papillomaviruses from the betapapillomavirus and gammapapillomavirus genera betapapillomaviruses in the anal canal of hiv positive and hiv negative men who have sex with men beta and gamma human papillomaviruses in the anal canal of hiv-infected and uninfected men who have sex with men prevalence of beta and gamma human papillomaviruses in the anal canal of men who have sex with men is influenced by hiv status cervical infection with cutaneous beta and mucosal alpha papillomaviruses prevalence and epidemiologic profile of oral infection with alpha, beta, and gamma papillomaviruses in an asian chinese population the use of polymerase chain reaction amplification for the detection of genital human papillomaviruses identification and assessment of known and novel human papillomaviruses by polymerase chain reaction amplification, restriction fragment length polymorphisms, nucleotide sequence, and phylogenetic algorithms a broad range of human papillomavirus types detected with a general pcr method suitable for analysis of cutaneous tumours and normal skin molecular methods for identification and characterization of novel papillomaviruses diversity of human papillomaviruses in skin lesions multiple oral carcinomas associated with a novel papillomavirus in a dog beta and gamma human papillomaviruses in anal and genital sites among men: prevalence and determinants prevalence and risk factors for anal human papillomavirus infection in human immunodeficiency virus (hiv)-positive and high-risk hiv-negative women relationship between prevalent oral and cervical human papillomavirus infections in human immunodeficiency virus-positive and -negative women high diversity of alpha, beta and gamma human papillomaviruses in genital samples from hiv-negative and hiv-positive heterosexual south african men an anal cancer screening program for msm in italy: prevalence of multiple hpv types and vaccine-targeted infections frequency and multiplicity of human papillomavirus infection in hiv-1 positive women in italy oral human papillomavirus dna detection in hiv-positive men: prevalence, predictors, and co-occurrence at anal site enzymatic amplification of beta-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia mafft: a novel method for rapid multiple sequence alignment based on fast fourier transform seaview and phylo_win: two graphic tools for sequence alignment and molecular phylogeny selection of conserved blocks from multiple alignments for their use in phylogenetic analysis raxml-vi-hpc: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models beta-hpv types in patients with head and neck pathology and in healthy subjects association between β-genus human papillomavirus and cutaneous squamous cell carcinoma in immunocompetent individuals-a metaanalysis the biology of beta human papillomaviruses the nasal mucosa contains a large spectrum of human papillomavirus types from the betapapillomavirus and gammapapillomavirus genera prevalence and concordance of cutaneous beta human papillomavirus infection at mucosal and cutaneous sites analysis of the effect of dna purificationon detection of human papillomavirus in oral rinse samples by pcr prevalence and transmission of beta and gamma human papillomavirus in heterosexual couples prevalence and multiplicity of cutaneous beta papilloma viruses in plucked hairs depend on cellular dna input crossreactivity profiles of hybrid capture ii, cobas, and aptima human papillomavirus assays: split-sample study beta-papillomavirus dna loads in hair follicles of immunocompetent people and organ transplant recipients concordance of beta-papillomavirus across anogenital and oral anatomic sites of men: the him study concordant testing results between various human papillomavirus assays in primary cervical cancer screening: systematic review continuing global improvement in human papillomavirus dna genotyping services: the 2013 and 2014 hpv labnet international proficiency studies detection of oral hpv infection -comparison of two different specimen collection methods and two hpv detection methods oral human papillomavirus infection incidence and clearance: a systematic review of the literature international standardization and classification of human papillomavirus types towards quality and order in human papillomavirus research hpviewer: sensitive and specific genotyping of human papillomavirus in metagenomic dna we are grateful to all member of virology laboratory inmi l. spallanzani for sample collection. we thank dr. mariana badescu for english editing. the authors declare that they have no competing interests. key: cord-262545-bs8p50ig authors: luk, andrea o. y.; ke, calvin; lau, eric s. h.; wu, hongjiang; goggins, william; ma, ronald c. w.; chow, elaine; kong, alice p. s.; so, wing-yee; chan, juliana c. n. title: secular trends in incidence of type 1 and type 2 diabetes in hong kong: a retrospective cohort study date: 2020-02-20 journal: plos med doi: 10.1371/journal.pmed.1003052 sha: doc_id: 262545 cord_uid: bs8p50ig background: there is very limited data on the time trend of diabetes incidence in asia. using population-level data, we report the secular trend of the incidence of type 1 and type 2 diabetes in hong kong between 2002 and 2015. methods and findings: the hong kong diabetes surveillance database hosts clinical information on people with diabetes receiving care under the hong kong hospital authority, a statutory body that governs all public hospitals and clinics. sex-specific incidence rates were standardised to the age structure of the world health organization population. joinpoint regression analysis was used to describe incidence trends. a total of 562,022 cases of incident diabetes (type 1 diabetes [n = 2,426]: mean age at diagnosis is 32.5 years, 48.4% men; type 2 diabetes [n = 559,596]: mean age at diagnosis is 61.8 years, 51.9% men) were included. among people aged <20 years, incidence of both type 1 and type 2 diabetes increased. for type 1 diabetes, the incidence increased from 3.5 (95% ci 2.2–4.9) to 5.3 (95% ci 3.4–7.1) per 100,000 person-years (average annual percentage change [aapc] 3.6% [95% ci 0.2–7.1], p < 0.05) in boys and from 4.3 (95% ci 2.7–5.8) to 6.4 (95% ci 4.3–8.4) per 100,000 person-years (aapc 4.7% [95% ci 1.7–7.7], p < 0.05] in girls; for type 2 diabetes, the incidence increased from 4.6 (95% ci 3.2–6.0) to 7.5 (95% ci 5.5–9.6) per 100,000 person-years (aapc 5.9% [95% ci 3.4–8.5], p < 0.05) in boys and from 5.9 (95% ci 4.3–7.6) to 8.5 (95% ci 6.2–10.8) per 100,000 person-years (aapc 4.8% [95% ci 2.7–7.0], p < 0.05) in girls. in people aged 20 to <40 years, incidence of type 1 diabetes remained stable, but incidence of type 2 diabetes increased over time from 75.4 (95% ci 70.1–80.7) to 110.8 (95% ci 104.1–117.5) per 100,000 person-years (aapc 4.2% [95% ci 3.1–5.3], p < 0.05) in men and from 45.0 (95% ci 41.4–48.6) to 62.1 (95% ci 57.8–66.3) per 100,000 person-years (aapc 3.3% [95% ci 2.3–4.2], p < 0.05) in women. in people aged 40 to <60 years, incidence of type 2 diabetes increased until 2011/2012 and then flattened. in people aged ≥60 years, incidence was stable in men and declined in women after 2011. no trend was identified in the incidence of type 1 diabetes in people aged ≥20 years. the present study is limited by its reliance on electronic medical records for identification of people with diabetes, which may result in incomplete capture of diabetes cases. the differentiation of type 1 and type 2 diabetes was based on an algorithm subject to potential misclassification. conclusions: there was an increase in incidence of type 2 diabetes in people aged <40 years and stabilisation in people aged ≥40 years. incidence of type 1 diabetes continued to climb in people aged <20 years but remained constant in other age groups. the hong kong diabetes surveillance database hosts clinical information on people with diabetes receiving care under the hong kong hospital authority, a statutory body that governs all public hospitals and clinics. sex-specific incidence rates were standardised to the age structure of the world health organization population. joinpoint regression analysis was used to describe incidence trends. a total of 562,022 cases of incident diabetes (type 1 diabetes [n = 2,426]: mean age at diagnosis is 32.5 years, 48.4% men; type 2 diabetes [n = 559,596]: mean age at diagnosis is 61.8 years, 51.9% men) were included. among people aged <20 years, incidence of both type 1 and type 2 diabetes increased. for type 1 diabetes, the incidence increased from 3.5 (95% ci 2.2-4.9) to 5.3 (95% ci 3.4-7.1) per 100,000 person-years (average annual percentage change [aapc] 3.6% [95% ci 0.2-7.1], p < 0.05) in boys and from 4.3 (95% ci 2.7-5.8) to 6.4 (95% ci 4.3-8.4) per 100,000 person-years (aapc 4.7% [95% ci 1.7-7.7], p < 0.05] in girls; for type 2 diabetes, the incidence increased from 4.6 (95% ci 3.2-6.0) to 7.5 (95% ci 5.5-9.6) per 100,000 person-years (aapc 5.9% [95% ci 3.4-8.5], p < 0.05) in boys and from 5.9 (95% ci 4.3-7.6) to 8 , p < 0.05) in women. in people aged 40 to <60 years, incidence of type 2 diabetes increased until 2011/2012 and then flattened. in people aged �60 years, incidence was stable in men and declined in women after 2011. no trend was identified in the incidence of type 1 diabetes in people aged �20 years. the present study is limited by its reliance on electronic medical records for identification of people with diabetes, which may result in incomplete capture of diabetes cases. the differentiation of type 1 and type 2 diabetes was based on an algorithm subject to potential misclassification. there was an increase in incidence of type 2 diabetes in people aged <40 years and stabilisation in people aged �40 years. incidence of type 1 diabetes continued to climb in people aged <20 years but remained constant in other age groups. why was this study done? • diabetes affects over 400 million people worldwide, and over half of the diabetes population comes from asian countries. • most studies on the burden of diabetes in asia reported the diabetes prevalence, i.e., the proportion of the population with disease, but few have considered diabetes incidence, i.e., the rate at which new cases have developed in the population. • knowledge of disease incidence informs how population exposure to risk factors has changed over time and is useful for projection of future prevalence. what did the researchers do and find? • we identified 562,022 people with new-onset type 1 or type 2 diabetes occurring between 2002 and 2015 in the electronic medical record system of the hong kong hospital authority. • we calculated the incidence rates of diabetes according to age categories and gender and analysed incidence trends over time. • we found that the incidence of both type 1 and type 2 diabetes increased in children and adolescents (aged <20 years). • incidence of type 2 diabetes also increased in people aged 20 to <40 years but was stable in people aged �40 years. type 2 diabetes mellitus is a complex progressive disease of rapidly growing prevalence. the global prevalence of type 2 diabetes is currently estimated at 415 million and is projected to escalate to 642 million over the next 25 years [1] . more than half of the world's population of those with type 2 diabetes comes from asia, where rapid industrialisation and urbanisation have contributed to an obesogenic living environment and increasing rates of overweight and obesity [1] . the majority of published population-based studies on the epidemiology of type 1 and type 2 diabetes in asia, including china, reported prevalence data, but few examined the incidence of diabetes [2, 3] . although the prevalence informs the disease burden, the incidence reflects how population exposure to risk factors has changed over time, and these estimates are necessary for the accurate projection of future prevalence. importantly, disease incidence communicates to the health policy makers whether strategies to prevent diabetes have been effective. recently, quan and colleagues reported the incidence and prevalence of diabetes in hong kong and detected a decline in the incidence of diabetes over a 9-year period between 2006 and 2014 [4] . however, diabetes types were not differentiated, and trends among the paediatric population were not explored. we accessed the territory-wide database hosted by the hong kong hospital authority (ha) and described the secular trends in incidence of type 1 and type 2 diabetes from 2002 to 2015. hong kong is a special administrative region of people's republic of china and has a population of 7.44 million. the hong kong ha is a statutory body formed in 1996 that governs all 47 public hospitals and 73 government outpatient clinics in hong kong. because of the wide cost differential between public and private healthcare sectors, around 89% of the local residents receive care for chronic illnesses in the ha [5] . a territory-wide electronic medical record system, adopted in 2000, captures demographic information, diagnostic and procedure codes, laboratory results, and drug prescriptions of people attending public hospitals and clinics. the hong kong diabetes surveillance database (hkdsd) is a population-based cohort of people with diabetes in hong kong identified from the ha electronic medical record system between 1 january 2000 and 31 december 2016. the analysis was not prespecified and was planned after obtaining and reviewing the content of the database. diabetes was ascertained based on one or more of the following qualifying criteria: (1) glycated haemoglobin (hba1c) � 6.5% (48 mmol/mol) in any one available hba1c measurement [6] ; (2) fasting plasma glucose (fpg) � 7.0 mmol/l in any one available fpg measurement [7] ; (3) prescription of noninsulin antihyperglycaemic drugs and/or (4) prescription of insulin for at least 28 days continuously, with or without (5) recording of the diagnostic code of diabetes based on the international classification of diseases, ninth revision (icd-9) code 250; and/or (6) recording of the diagnostic code of diabetes according to the revised edition of the international classification of primary care, world organization of national colleges, academics, and academic associations of general practitioners/family physicians code t89 or code t90. to minimise misclassification of normal individuals as having diabetes, people who received diagnostic coding of diabetes but did not fulfil any of the laboratory or drug criteria throughout the observation are not considered. to avoid inclusion of women with gestational diabetes, we removed episodes occurring within 9 months prior to or 6 months after delivery (icd-9 codes 72-75) or occurring within 9 months before or after any pregnancy-related encounter (icd-9 codes 630-676). however, women with subsequent episodes that met the criteria for diabetes occurring outside the context of any obstetric events would be included. the separation of diabetes types is not reliable based on coding alone in administrative databases. in the hkdsd, a small subset of people received icd-9 coding for both type 1 and type 2 diabetes. for the purpose of this analysis, we developed and validated an algorithm to delineate type 1 from type 2 diabetes using another database, the hong kong diabetes register (hkdr). in brief, the hkdr contains clinical information on people with physician-diagnosed diabetes who were referred to two public hospitals (prince of wales hospital and alice ho miu ling nethersole hospital) for assessment of diabetes complications. in the hkdr, diabetes subtype was determined by the referring physician and was independently confirmed with chart review by one of the investigators (ck) of the present study. type 1 diabetes was defined as clinical presentation with diabetic ketoacidosis and/or continuous requirement of insulin within 1 year of diagnosis. positivity for islet autoantibodies was not used to define autoimmune diabetes because antibodies were not routinely measured. of 24,060 patients in the hkdr, we excluded people with onset dates outside of 1 january 2002 to 31 december 2015 (n = 8,403) and those with missing data on diabetes subtype (n = 357). of the remaining 15,297 people with newly diagnosed diabetes, type 1 diabetes was confirmed in 103 patients. the cohort was separated in a 2:1 ratio for derivation and validation of the algorithm, respectively. we considered icd-9 codes (type 1 diabetes: icd-9 250.x1 or 250.x3, type 2 diabetes: icd-9 250.x0 or 250.x2) and types of insulin treatment in the algorithms, and we tested 12 combinations for sensitivity, specificity, positive predictive value (ppv) and negative predictive value (npv) for identifying type 1 diabetes. of these combinations, ratios of type 1 to type 2 diabetes codes �4 or prescription of a combination of short-and long-acting insulin and no noninsulin antihyperglycaemic treatment within the first year of diagnosis yielded the optimal sensitivity of 100.0% (95% ci 76.8-100.0), specificity of 100.0% (95% ci 87.2-100.0), ppv of 100.0% (95% ci 76.8-100.0), and npv of 100.0% (95% ci 87.2-100.0) in the hkdr for people aged <20 years in the validation cohort. the sensitivity and ppv of this algorithm for identifying type 1 diabetes decreased to 50.0%-71.4% and 28.6%-62.5%, respectively, in people aged �20 years, which is expected because of the rarity of type 1 diabetes at older ages. an incident case of diabetes was identified by the first occurrence of any episode fulfilling the definition of diabetes and at least 2 years of diabetes-free observation prior. at least 1 year of surveillance from the date of diagnosis was required to enable discrimination of type 1 and type 2 diabetes. thus, although the database includes cases of diabetes from 1 january 2000 to 31 december 2016, incidence of diabetes was described from 1 january 2002 to 31 december 2015. the date of diagnosis was the date to first fulfil the qualifying event. we estimated sexspecific annual incidence rates of type 1 and type 2 diabetes. the numerator was the number of incident cases of diabetes in the hkdsd in each calendar year, and the denominator was the estimated hong kong population of the previous year at midyear as reported by the local census and statistics department. calculated rates were expressed per 100,000 person-years. we reported age-standardised rates (using the age structure of the world health organization standard population) for the entire population and for subgroups by sex and age categories (<20 years, 20 to <40 years, 40 to <60 years, �60 years). we calculated the annual percentage change (apc) and the average apc (aapc) in incidence rates with 95% ci by sex and by age bands. joinpoint regression analysis was used to describe incidence trends over time. the optimal number of line segments that best fit the pattern was identified, and apcs were computed for the slope before and after each joinpoint using regression analysis. because of an observed irregularity in the number of new cases of type 2 diabetes in 2004, trend analysis including reporting of apc and aapc for both type 2 and type 1 diabetes (for consistency) was restricted to the period between 1 january 2005 and 31 december 2015. in a sensitivity analysis, we conducted trend analysis for type 2 diabetes using restricted cubic spline, which allowed for a more flexible fitting of the change in incidence rates, and results are presented in the supporting information. statistical significance was set at p-value of <0.05. analysis was performed using sas version 9.4 (cary, nc) and joinpoint regression program version 4.6.0.0 (national cancer institute, bethesda, md). of 778,051 people captured in the hkdsd, we excluded 33,916 people who had diabetes codes but did not fulfil other criteria of diabetes. we further excluded 137,569 cases of prevalent diabetes (episodes fulfilling diabetes between 1 january 2000 and 31 december 2001) and 44,544 cases of diabetes that occurred between 1 january 2016 and 31 december 2016. the remaining 562,022 people with incident type 1 or type 2 diabetes occurring between 2002 and 2015 were included in the analysis (s1 fig, s1 table) . demographic and clinical characteristics of the cohort at diagnosis are detailed in s2 table. trends in incidence of type 1 diabetes using the derived algorithm, 2,426 people with newly diagnosed diabetes were classified as having type 1 diabetes, among whom 774 (31.9%) were aged <20 years and 845 (34.8%) and 807 (33.3%) were aged 20 to <40 years and �40 years, respectively (s1 table) . age-standardised incidence of type 1 diabetes increased from 2005 to 2015 in people aged <20 years in both sexes, from 3.5 (95% ci 2.2-4.9) to 5.3 (95% ci 3.4-7.1) per 100,000 person-years (aapc 3.6% [95% ci 0.2-7.1], p < 0.05) in boys and from 4.3 (95% ci 2.7-5.8) to 6.4 (95% ci 4.3-8.4) per 100,000 person-years (aapc 4.7% [95% ci 1.7-7.7], p < 0.05) in girls (table 1) . broken down into narrower age bands, the incidence of type 1 diabetes peaked in the age groups of 5-9 years in the female sex and 10-14 years in the male sex and declined with increasing age. among those aged 20 to <40 years and �40 years, incidence of type 1 diabetes remained stable over time (table 1 ). sex differences in the risk of type 1 diabetes were detected in the people aged <20 years but not in people aged �20 years. the rate ratio for type 1 diabetes was 1.38 (95% ci 1.10-1.37, p < 0.05) in girls compared with boys. among 559,596 incident cases of type 2 diabetes, 1,182 (0.2%) presented below 20 years of age, 22,924 (4.1%) presented in people aged 20 to <40 years, and 535,490 presented (95.7%) in people aged �40 years (s1 table) . the incidence rose with age and peaked in the age groups of 65-75 years in both men and women (fig 1) . table, the majority (76.2%) of the new episodes of type 2 diabetes in 2004 was identified by first-time use of noninsulin antihyperglycaemic drugs alone, suggesting that these occurrences could be prevalent cases initially diagnosed and followed outside of ha and later presenting to ha for continuation of existing treatment. incident cases captured in 2004 or before were excluded from subsequent trend analysis. an increase in the incidence of type 2 diabetes was observed in the <20 years and 20 to <40 years age groups (table 1 , fig 2a and 2b) . for people <20 years old, the age-standardised incidence of type 2 diabetes increased from 4.6 (95% ci 3.2-6.0) to 7.5 (95% ci 5.5-9.6) per 100,000 person-years ( 2) in men and women, respectively, for the entire period (p < 0.05). the sex disparity in incidence of type 2 diabetes varied by age. for people <20 years old, the incidence was disproportionately higher in girls than in boys, with an overall rate ratio of 1.22 (95% ci 1.10-1.37, p < 0.05). upon reaching young adulthood, the risk reversed, and men had higher incidence rates than women. in people aged 40 to <60 years, we detected an initial increase in incidence followed by stabilisation in both sexes (table 1, fig 2c) . in men, the incidence of type 2 diabetes increased from 697.0 (95% ci 681. using the territory-wide hkdsd, we conducted time trend analyses on the incidence of type 1 and type 2 diabetes in people in hong kong. between 2005 and 2015, the incidence of type 2 diabetes increased in people aged <20 years and 20 to <40 years, increased and then stabilised in people aged 40 to <60 years, and was unchanged in those aged �60 years. incidence of type 1 diabetes continued to climb in people aged <20 years but remained constant in other age groups. although the incidence of type 1 diabetes was the highest in those <20 years old, adult-onset type 1 diabetes accounted for over two-thirds of newly diagnosed cases during the surveillance period. among those <20 years old, type 2 diabetes contributed to more than half of the newly presented cases. the key strengths of this study were the use of population-level data through access to the electronic medical record system of the hong kong ha and its low susceptibility to selection bias. given the scarcity of population-level data on secular changes in diabetes incidence in asia, our results are timely in providing insights into the contemporary diabetes epidemic in this region. importantly, this study highlights the emerging problem of young-onset diabetes and calls for effective strategies to reduce modifiable risk factors for diabetes in this group. the multinational european diabetes (eurodiab) register, which included 29,311 incident cases of type 1 diabetes in youth aged <15 years recorded between 1989 and 2003, revealed regional differences in the trend of diabetes incidence [8] . in areas with a high burden of type 1 diabetes, such as the nordic countries, the united states, and australia, the incidence appeared to have stabilised over the past decade [9, 10, 11] . conversely, the incidence of type 1 diabetes has continued to rise in places of low disease prevalence, including east asia [12, 13] . based on a registry of 622 newly diagnosed cases of type 1 diabetes in children aged <15 years in shanghai, zhao and colleagues observed an increase in incidence from 1.5 per 100,000 person-years in 1997-2001 to 5.5 per 100,000 person-years in 2007-2011 [12] . from the 2012-2014 national health insurance service database containing 706 physician-reported cases of type 1 diabetes in children aged <15 years in south korea, kim and colleagues reported an incidence of 3.2 per 100,000 person-years, which was 2.3-fold higher compared with the rate recorded in the earlier period of 1995-2000 [13] . in the present study, we also detected an increase in the incidence of type 1 diabetes in children and adolescents, and the increase occurred in both sexes. in hong kong, the incidence of type 1 diabetes has not been determined since the last report 2 decades ago. based on retrospective retrieval of 255 paediatric cases of newly diagnosed diabetes between 1984 and 1996, huen and colleagues recorded an incidence of 1.4 per 100,000 person-years for type 1 diabetes in children aged <15 years in hong kong, which was considerably lower than our updated estimates of 5.3-6.4 per 100,000 person-years in a comparable age group [14] . our observations, together with others' observations showing a similar rise in incidence, remain unexplained, although environmental factors, including obesity, nutrition, climate, and infection, have been implicated in the induction and acceleration of beta cell destruction [15] . from surveys of hong kong school children, the prevalence of overweight or obesity rose from 11.6% in the mid-1990s to 16.7% in 2005 [16] , and the prevalence was 17.6% in primary school students and 19.9% in secondary school students in the last estimation in 2018 [17] . it is noteworthy that although the incidence was the highest in the paediatric population, adults aged >20 years accounted for two-thirds of the newly diagnosed cases in our database. in contrast to the rising trend of childhood-onset type 1 diabetes, the incidence of adult-onset type 1 diabetes has not increased. the growing number of young people acquiring type 2 diabetes is a major health concern that is now seen globally. in the present study, 60% of incident cases of diabetes in people aged <20 years were type 2 diabetes. the search for diabetes in youth registry, which systematically identified and followed youth with diabetes in the us, reported an annual increase of 4.8% in the incidence of type 2 diabetes in people aged <20 years between 2002 and 2012, from 7.0 to 9.0 per 100,000 person-years in boys and from 11.1 to 16.2 per 100,000 person-years in girls [18] . furthermore, the increase was larger in asians and pacific islanders (annual increase 16.0%) than europeans (annual increase 3.3%). similarly, wu and colleagues reported an increase in incidence from 0.7 to 3.6 per 100,000 person-years using a registry of 392 newly diagnosed cases of young-onset diabetes presented between 2007 and 2013 in zhejiang, china [19] . among those aged <20 years in hong kong, the average annual increase in incidence was 4.8%-5.9%, and the last recorded crude incidence rates in 2015 were 8.3 and 9.2 per 100,000 person-years in boys and girl, respectively, which were lower than the us figures but higher than rates in china. similarly, we detected an increase in incidence of type 2 diabetes in people aged 20 to <40 years in both sexes. besides exposure to an increasingly obesogenic environment, intrauterine effects from gestational diabetes and/or maternal obesity and exposure to present-day endocrine disruptors may be responsible [20] [21] [22] . it is also possible that the observed incidence trend of young-onset type 2 diabetes was the result of people seeking medical attention earlier in their disease trajectory rather than an actual fall in the age of diabetes development. in this regard, people who would develop diabetes were diagnosed progressively earlier, thus removing people from the undiagnosed pool who would have otherwise presented at an older age. in people aged 40 to <60 years, the incidence of type 2 diabetes in both sexes initially increased and then flattened from 2011/2012 onward. in women aged �60 years, the incidence was stable until 2011 and declined thereafter, whereas in men aged �60 years, the incidence remained constant. the absence of a rise might reflect levelling off in exposure to risk factors. in hong kong, the prevalence of obesity has been stable in men and has declined in women since the mid-1990s [23, 24] , which is attributable to a series of government-led health promotion initiatives targeting healthier lifestyles, such as the eatsmart programme and mandatory nutrition labelling during this period [25] . women are generally more receptive to health information and ready to adopt a healthy lifestyle compared with men, which might in part account for the sex difference in trends of obesity and type 2 diabetes [26] . cigarette smoking is linked to the development of type 2 diabetes [27] . antismoking advertising campaigns and government policy to ban smoking in many public areas have resulted in a reduction in smoking rates over the past 35 years, from 23.3% in 1982 to 10.0% in 2017 in hong kong [28] . lastly, saturation effect could be an explanatory factor, wherein increased health awareness and improved screening efforts during earlier periods have captured most of the high-risk individuals, thus depleting the pool of undiagnosed type 2 diabetes over time. in support of this, we observed a significant decline in hba1c values at diagnosis of type 2 diabetes from 2002 to 2011, possibly reflecting proactive case finding and earlier detection. although screening programmes for diabetes have not been formally introduced in hong kong, governmental policies to enhance primary care, including the dissemination of a reference framework for diabetes care, could have an effect toward improving diabetes detection [29, 30] . the increasing number of outpatient and inpatient attendances to public healthcare facilities over time also supports an increasing opportunity for diagnosing diabetes [31] . limited studies indicated interethnic variation in the risks for type 2 diabetes. alangh and colleagues reported 10-year secular trends in diabetes incidence in ontario, canada, and found that incidence increased moderately by 24% in the european population as compared with a 15-fold increase in the chinese population, in which the absolute incidence rate was twice that of europeans (19.6 versus 10.0 per 1,000 person-years) by 2005 [32] . from contemporary studies, the ageand sex-adjusted diabetes incidence rates among adults were 370 per 100,000 person-years in the united kingdom [33] , 398 per 100,000 person-years in sweden [34] , and 710 per 100,000 person-years in the us during the 2012-2014 period [35] . over a comparable reporting period, the rates were 1,099 and 949 per 100,000 person-years in men and women in our study, 830 per 100,000 person-years in korea [36] , and 800 per 100,000 person-years in taiwan [37] . differences in methods used to capture incident cases and diagnostic intensities would have influenced the estimates. allowing for these factors, available data, including those from the present study, suggest that the incidence of type 2 diabetes may be higher in east asians than europeans. although chinese people are leaner than europeans, for the same bmi, the former have more visceral fat, greater insulin resistance, and more metabolic complications [38] . moreover, low body weight is linked to poorer pancreatic beta cell reserve, and chinese people are more vulnerable to external factors, such as glucolipotoxicity, that trigger progressive decline in beta cell function [39] . a sharp peak in the incidence of type 2 diabetes was recorded in 2004, and this could be connected to the severe acute respiratory syndrome epidemic in 2003 in hong kong [40] . the excess of 21,000 new cases of type 2 diabetes in 2004 compared with 2003 might be due to heightened health vigilance at the aftermath of the epidemic, which prompted increased doctor visits. the modest dip in the number of new cases in the ensuing 3 years (from 2005 to 2007) compared with numbers between 2002 and 2003 could support earlier identification of cases during the transitory period, leaving fewer cases to be detected in subsequent years. the excess might also represent an injection of prevalent cases from the private sector to the public system in response to economic adversity. we acknowledge the following limitations in the study. an electronic medical record database was used to identify patients with diabetes, and we cannot exclude the possibility of incomplete capture. the data source included patients who attended only public healthcare facilities, and those receiving care in the private sector-who represent about 10% of the entire disease population-were not included. as such, the incidence rates as reported were likely underestimations of the actual figure by up to 10%. however, except for 2004, there was no evidence that the ratio of medical care in private sector versus public sector has changed over time, and therefore, this is unlikely to affect assessment of incidence trends. two-hour plasma glucose by an oral glucose tolerance test (ogtt) was not included as one of the qualifying criteria for diabetes, which could also underestimate incidence rates, especially in the paediatric population in whom hba1c alone has low sensitivity of diagnosing type 2 diabetes [41] . the categorisation of type 1 and type 2 diabetes was based on an algorithm rather than direct inspection of the clinical notes. although the algorithm was developed in an independent data set in which the diagnosis of type 1 diabetes was verified by reviewing medical records, the absence of confirmatory tests such as anti-islet cell antibodies or c-peptide levels could lead to incorrect differentiation of type 1 and type 2 diabetes, affecting the accuracy of the algorithm. misclassifying type 2 as type 1 diabetes would significantly inflate the incidence of type 1 diabetes, whereas the impact on incidence of type 2 diabetes was probably minimal. the probability of incorrect grouping would be greater in older patients in whom the algorithm performed less well, and estimates of incidence of type 1 diabetes in adults will require confirmation in other cohorts. because of limitations in details of the extracted information, we could not discern patients with other aetiologies of diabetes, such as maturity-onset diabetes of the young and secondary diabetes. owing to the asymptomatic nature of diabetes, diagnosis is often delayed. despite the good quality of the surveillance database, undiagnosed cases could not be captured, leading to underreporting of case burden. the recorded incidence rates were also sensitive to secular changes in people's health-seeking behaviour, screening practice, and prescription behaviour. in this report on the secular trend of the incidence of diabetes in hong kong, we revealed that the incidence of type 1 diabetes increased in people aged <20 years and was stable in other age groups. the incidence of type 2 diabetes also increased in people aged <40 years and accounted for over half of new cases of diabetes among people aged <20 years. in people aged �40 years, the incidence of type 2 diabetes remained constant. these observations provide an impetus for scaling up measures to prevent development of diabetes in people at risk. (a) incidence trends of type 2 diabetes in boys aged <20 years using restricted cubic spline. (b) incidence trends of type 2 diabetes in men aged 20 to <40 years using restricted cubic spline. (c) incidence trends of type 2 diabetes in men aged 40 to <60 years using restricted cubic spline. (d) incidence trends of type 2 diabetes in men aged �20 years using restricted cubic spline. (e) incidence trends of type 2 diabetes in girls aged <20 years using restricted cubic spline. (f) incidence trends of type 2 diabetes in women aged 20 to <40 years using restricted cubic spline. (g) incidence trends of type 2 diabetes in women aged 40 to <60 years using restricted cubic spline. (h) incidence trends of type 2 diabetes in women aged �20 years using restricted cubic spline. international diabetes federation china noncommunicable disease surveillance group. prevalence and control of diabetes in chinese adults china national diabetes and metabolic disorders study group. prevalence of diabetes among men and women in china diabetes incidence and prevalence in hong kong, china during 2006-2014 thematic household survey report no. 50. hong kong sar: census and statistics department standards of medical care in diabetes-2010 report of the expert committee on the diagnosis and classification of diabetes mellitus solté sz g; eurodiab study group. incidence trends for childhood type 1 diabetes in europe during 1989-2003 and predicted new cases 2005-20: a multicentre prospective registration study norwegian childhood diabetes study group. incidence of type 1 diabetes in norway among children aged 0-14 years between 1989 and 2012: has the incidence stopped rising? results from the norwegian childhood diabetes registry regular peaks and troughs in the australian incidence of childhood type 1 diabetes mellitus (2000-2011) a plateau in new onset type 1 diabetes: incidence of pediatric diabetes in the united states military health system rapidly rising incidence of childhood type 1 diabetes in chinese population: epidemiology in shanghai during 1997-2011 increasing incidence of type 1 diabetes among korean children and adolescents: analysis of data from a nationwide registry in korea epidemiology of diabetes mellitus in children in hong kong: the hong kong childhood diabetes register the accelerator hypothesis: weight gain as the missing link between type i and type ii diabetes secular changes in height, weight and body mass index in hong kong children the government of the hong kong special administrative region search for diabetes in youth study. incidence trends of type 1 and type 2 diabetes among youths incidence and time trends of type 2 diabetes mellitus in youth aged 5-19 years: a population-based registry in zhejiang, china diabetes and obesity in the offspring of pima indian women with diabetes during pregnancy glucose intolerance and cardiometabolic risk in adolescents exposed to maternal gestational diabetes: a 15-year follow-up study arsenic exposure and prevalence of type 2 diabetes in us adults epidemiology of cardiovascular risk factors in hong kong worsening trend of central obesity despite stable or decline body mass index in hong kong chinese between 1996 and the government of the hong kong special administrative region. promoting health in hong kong: a strategic framework for prevention and control of non-communicable diseases a demographic perspective on gender, family and health in europe cigarette smoking is an independent risk factor for type 2 diabetes: a four-year community-based prospective study tobacco and alcohol control office. department of health. the government of the hong kong special administrative region the government of the hong kong special administrative region. our partner for better health the government of the hong kong special administrative region. hong kong reference framework for diabetes care for adults in primary care settings. food and health bureau the government of the hong kong special administrative region rapid increase in diabetes incidence among chinese canadians between examining trends in type 2 diabetes incidence, prevalence and mortality in the uk between incidence, prevalence and mortality of type 2 diabetes requiring glucose-lowering treatment, and associated risks of cardiovascular complications: a nationwide study in sweden prevalence and incidence trends for diagnosed diabetes among adults aged 20 to 79 years trends in diabetes incidence in the last decade based on korean national health insurance claims data time trend analysis of the prevalence and incidence of diagnosed type 2 diabetes among adults in taiwan from 2000 to 2007: a populationbased study asians have lower body mass index but higher percent body fat than do whites: comparisons of anthropometric measurements diabetes in asia: epidemiology, risk factors, and pathophysiology a major outbreak of severe acute respiratory syndrome in hong kong utility of hemoglobin a(1c) for diagnosing prediabetes and diabetes in obese children and adolescents we acknowledge the hong kong hospital authority for providing the data for research. key: cord-266488-wc6k06sm authors: feng, mingqian; bian, hejiao; wu, xiaolin; fu, tianyun; fu, ying; hong, jessica; fleming, bryan d; flajnik, martin f; ho, mitchell title: construction and next-generation sequencing analysis of a large phage-displayed v(nar) single-domain antibody library from six naïve nurse sharks date: 2018-11-07 journal: antib ther doi: 10.1093/abt/tby011 sha: doc_id: 266488 cord_uid: wc6k06sm background: shark new antigen receptor variable domain (v(nar)) antibodies can bind restricted epitopes that may be inaccessible to conventional antibodies. methods: here, we developed a library construction method based on polymerase chain reaction (pcr)-extension assembly and self-ligation (named “easel”) to construct a large v(nar) antibody library with a size of 1.2 × 10(10) from six naïve adult nurse sharks (ginglymostoma cirratum). results: the next-generation sequencing analysis of 1.19 million full-length v(nar)s revealed that this library is highly diversified because it covers all four classical v(nar) types (types i–iv) including 11% of classical type i and 57% of classical type ii. about 30% of the total v(nar)s could not be categorized as any of the classical types. the high variability of complementarity determining region (cdr) 3 length and cysteine numbers are important for the diversity of v(nar)s. to validate the use of the shark v(nar) library for antibody discovery, we isolated a panel of v(nar) phage binders to cancer therapy-related antigens, including glypican-3, human epidermal growth factor receptor 2 (her2), and programmed cell death-1 (pd1). additionally, we identified binders to viral antigens that included the middle east respiratory syndrome (mers) and severe acute respiratory syndrome (sars) spike proteins. the isolated shark single-domain antibodies including type i and type ii v(nar)s were produced in escherichia coli and validated for their antigen binding. a type ii v(nar) (pe38-b6) has a high affinity (k(d) = 10.1 nm) for its antigen. conclusions: the naïve nurse shark v(nar) library is a useful source for isolating single-domain antibodies to a wide range of antigens. the easel method may be applicable to the construction of other large diversity gene expression libraries. classical immunoglobin g (igg) is widely used in many biotechnologies and therapeutics [1] . igg is best described as a heterodimeric homodimer, consisting of two copies of disulfide-bonded heavy (h) and light (l) chains. the h and l chain variable (v) domains (vh and vl, respectively) combine to form the antigen-binding region. when these two v domains are synthesized as a dual-domain singlechain v fragment (scfv), the minimum size of the fragment is 25-30 kda. in recent years, single-domain immunoglobulins such as the shark v nar (new antigen receptor variable domain) and the camelid heavy-chain variable domain (v h h) antibodies have been explored, both of which can be isolated as soluble, stable, monomeric binding domains [2] [3] [4] . these v nar and v h h domain antibodies range from 12 to 15 kda in size, roughly half the size of a scfv binding domain. cartilaginous fish (sharks, rays, skates, and chimaeras) are phylogenetically the oldest living organisms that use antibodies as part of their adaptive immune system [3, 4] . they produce three different antibody isotypes that function in their humoral immune responses, immunoglobulin m (igm), immunoglobulin w (igw), and immunoglobulin new antigen receptor (ignar) [3] [4] [5] [6] . ignar antibodies are homodimeric proteins composed of heavy chains with an antigen-binding region at the end of each chain. they serve as a major component in humoral responses [4, 7] . a number of camelid v h h domains are being evaluated in phase i, ii, and iii clinical trials [8, 9] . even though the shark v nar is less known, it has the potential to be used in biological therapeutics based on (i) their small size and ability to penetrate dense tissues inaccessible to igg [10] , (ii) their ability to bind in protein clefts and buried functional sites (e.g. enzyme pocket sites for substrate) [11] , (iii) their solubility and robustness in harsh conditions [12] , and (iv) their ability for high-affinity (including sub-nanomolar) binding. additionally, these antibodies have the potential to bind a wide range of antigens, despite the nature of their single-domain architecture [13] . the v nar domain is an ig superfamily domain with two β sheets held together by two canonical cysteine residues in framework regions (frs) 1 and 3. in addition to these canonical cysteines, complementarity determining region 3 (cdr3) can have one or two additional cysteines forming additional disulfide bonds within the v domain. ignars are classified into four types based on the number and position of non-canonical cysteines in the v nar domain [14] . type i v nar contains two non-canonical cysteine residues in cdr3 encoded by the diversity region or by n-nucleotide additions that form two disulfide bonds with fr2 and 4. interestingly, type i has only been reported in nurse sharks, ginglymostoma cirratum [14] . type ii v nar domains form disulfide bonds between one dencoded non-canonical cysteine in cdr3 and another non-canonical cysteine in cdr1. type iii is similar to type ii except there is a highly conserved tryptophan residue in cdr1 positioned adjacent to the disulfide bond. type iv has no non-canonical disulfide bonds as found in other three v nar types. both type i and type ii v nar s have protruding cdr3s that enable binding to pockets and grooves [15, 16] . classical igg and camelid v h h contain a cdr2 loop that is not present in shark v nar s and are replaced with highly diverse amino acids, termed hypervariable region 2 (hv2) [11] . additionally, there is a second hypervariable region, named hv4, which is inserted in the middle of fr3, therefore separating fr3 into fr3a and fr3b. shark v nar domains may have advantageous properties over conventional igg. first, sharks are evolutionarily distant from mammals on the phylogenetic tree, therefore can generate high-affinity binders to structurally conservative mammalian drug targets. these may include highly conserved heparan sulfate proteoglycans, g-protein coupled receptors, and ion channels that may exhibit poor immunogenicity in mice and rabbits [15, 17] . second, the elongated cdr3 in shark and camel antibodies has the ability to seek out buried epitopes and enzyme functional sites [2, 15, 17, 18] . the shark ignar cdr3 regions are relatively longer (ranging from 9 to 34 a.a. and including various numbers of cysteine residues) compared to mouse or human counterparts. this can potentially lead to a larger diversity of structures that can interact with more diversified antigens [16] . similarly, the longer cdr3 region in shark antibodies possesses the extraordinary capacity to form long finger-like extensions that can probe proteins for hidden epitopes [2] . third, conventional antibodies may have poor tissue penetration ability due to their large size [19] . whole igg is 150 kda and scfv fragments 25-30 kda. v nar domains can be as small as 12-15 kda. finally, shark v nar domain antibodies have structural advantages and are easily expressed in escherichia coli systems [2] . sharks enrich their blood with urea to maintain osmotic balance in the marine environment, so shark antibody structure has evolved to become particularly stable [4] . phage display technology has been used to isolate shark v nar antibodies. in one study, two shark v nar libraries with a size of 10 7 clones were constructed from both naïve spiny dogfish (squalus acanthias) and smooth dogfish (mustelus canis) sharks [20] . phage antibodies were isolated from immunized sharks for specific antigens such as hen egg white lysozyme [21] [22] [23] [24] . synthetic shark v nar singledomain libraries were also pursued [25] [26] [27] [28] [29] . however, none of these approaches has generated a large shark v nar single-domain library that covers the wide range of diversity required (>10 10 ) commonly for therapeutic antibody discovery. in this study, we developed a pcr-extension assembly and self-ligation-based method (named easel) to make a large phage-displayed v nar single-domain library from six nurse sharks. nurse sharks were chosen to maximize the diversity of the v nar library because they exclusively have been reported to contain type i v nar domains. to assess its diversity and analyze the v nar sequences on the largest scale in the field, we conducted next-generation sequencing (ngs) analysis on 1.19 million unique full-length v nar s. the unique sequences were then analyzed using unbiased methods to investigate their cysteine numbers and cdr3 lengths for all v nar sequences together as well as type i and type ii/iii v nar s separately. to validate the potential of this library as a new platform for therapeutic antibody discovery, we conducted phage panning to identify shark antibody therapeutics, 2019 3 v nar binders to a panel of tumor and viral antigens. these included antigens associated with liver and breast cancers, as well as antigens against viral proteins associated with sars and mers. these selected binders including type i and ii v nar s were produced successfully in e. coli as soluble proteins for antigen-binding validation. this work validated the large diversity of the nurse shark v nar library and the utility of the shark v nar library as a platform for therapeutic antibody discovery. to construct a large shark v nar library, we developed a method called easel. as illustrated in figure 1a , we isolated peripheral blood leukocytes from six adult nurse sharks (g. cirratum) and amplified shark v nar sequences with pcr primers. the reverse primers contain a 19-nucleotide sequence on the pcomb3x backbone. extension overlap pcr was conducted to combine the v nar and phagemid backbone (fig. 1b) . finally, after gel purification we performed a self-ligation with t4 ligase to circularize the assembled v nar pcomb3x plasmids. our shark v nar library size (∼1.2 × 10 10 ) was determined by titration based on the number of individual tg1 bacteria colonies on agar plates. this high-efficiency method is a significant improvement over the conventional phage library construction method, which usually requires many rounds of restriction enzyme digestion and ligation, making the previous method labor intensive and time consuming. moreover, the sequence diversity of the shark v nar is preserved and represented in our method to a maximum degree due to highly efficient pcr-based amplification and ligation. to analyze the diversity of the library, we performed deep sequencing of the whole library using ngs. each sequencing was done twice in both forward and reverse direction for paired-end reads. the merging of paired-end reads was then performed with high stringency by combining the forward and reverse sequencing results to ensure accuracy for each unique sequence. nearly 1.2 million full-length v nar sequences with in-frame translation were used for further analysis with a focus on cysteine numbers, cdr3 length, amino acid variability, and v nar type counts. this is the largest scale shark v nar sequence analysis reported thus far. as shown in figure 2a , the presence of two canonical cysteines located at both amino acid 21 and 82 are used as a key criterion to characterize type i-iv v nar s. the sequences that do not contain one or both of these cysteines are considered as other types (n = 56 508; ∼5% of the total v nar s) because they do not fit in with the four known v nar type families. the sequences that have both 21c and 82c (n = 1 138 843) are further categorized based on their placement of additional cysteines. type iv v nar s contain only two canonical cysteines found at position 21 and 82 (n = 19 494). type i v nar s contain an extra cysteine at position 34 (n = 281 361; ∼24% of the total v nar s). this group can be further divided into subtypes based on how many additional cysteines they contain. the classical definition of a type i v nar describes an antibody that has a total of six cysteines. about 11% of the total v nar s are classical type i. type ii and iii v nar s have at least one extra cysteine at amino acid 28 (n = 837 988; 70% of the total v nar s). among them, ∼57% of the total v nar s are classical type ii. unique full-length v nar s are defined as having one differing amino acid in sequence. as shown in figure 2b , 85% (1 022 715) of the 1.2 million sequences only appeared once in ngs results, and 8.5% of the 1.2 million sequences appeared twice. only 1% of the 1.2 million sequences appeared more than 10 times. the most frequently repeated clone appeared 2832 times in ngs results. the percentage of the different types of v nar is plotted in the pie chart in figure 2c . based on the number of extra cysteines in these sequences, the type i (six cysteines in total) and type ii (four cysteines in total) v nar s are considered classical to others (other numbers of cysteines) as shown in figure 2d and e, respectively. representative sequences of type i-iv shark v nar s with different numbers of cysteines were randomly picked from ngs data and shown here as examples (fig. 3) . the frs and cdr1, cdr3, hv2, and hv4 are marked based on stanfield et al. [11] and fennell et al. [13] in figure 3 . these sequences were aligned to sequences on imgt database for cdr determination. as shown in figure 3 , part of the hv2 sequence was identified as "cdr2" in the imgt database. these v nar s may have multiple cysteine residues in cdr3 based on the sequences from ngs data. we analyzed the total number of cysteines, the number of cysteines found in cdr3, the length of cdr3, and the amino acid sequence variability. due to the high variability of cdr3 lengths, we defined cdr3 to be the sequence between conserved framework sequences tyrc (end of fr3b) and xxxgtxxtvn (fr4). the total cysteines in v nar sequences can vary from 0 to 11 (fig. 4a ) and the cdr3 can have 0-6 cysteines (fig. 4b ). the cdr3 length varies greatly as well, and it can be between 0-40 amino acids according to the ngs data (fig. 3c ). the separate analysis of type i and type ii/iii v nar s showed type i v nar s (shown as blue lines) have more total cysteines and in cdr3 than type ii/iii (shown as red lines) ( fig. 4a and b). the cdr3 lengths for type i v nar s are also slightly longer compared to type ii/iii (fig. 4c ). these findings are consistent with published small-scale sequence analysis: type i v nar s have more even numbers of cysteines in cdr3 (0, 2, or 4) (fig. 4b) [7, 16] . the high variability of cdr3 length and cysteine numbers are crucial to the diversity of v nar s since binding diversity is dependent on the cdr3 structure diversity. amino acid sequence variation analysis showed the sequence diversity is mainly contributed to cdr3 with minimal variation in cdr1, hv2, and hv4 (fig. 5) . taken together, we designed a pcr-based method to establish a large shark v nar singledomain antibody library with the size of 10 10 . the library contains all types (i-iv) of shark v nar sequences as well as many other previously undefined types. to evaluate the library's potential for therapeutic development, we chose a variety of human tumor biomarkers and virus antigen proteins as selection targets. these include glypican-3 (gpc3), her2 and pd1, the spike proteins of the mers and sars viruses, and pseudomonas exotoxin (pe38). after four rounds of panning, specific binders to the listed targets were identified by monoclonal phage elisa (fig. 6a ). the binders were assigned the following names based on their targets and well numbers, which include gpc3-f1, her2-a6, pd1-a1, mers-a3, mers-a7, mers-a8, mers-b4, mers-b5, sars-01, and pe38-b6. only one binder was isolated for all antigens, except mers spike protein. five binders were isolated for mers spike protein. sequence analysis showed that most of these binders were type ii v nar except for one type i and two undefined types. one type ii binder (pe38-b6) targeting pe38 fragment was produced in e. coli hb2151 strain as a single-domain protein. it had 10.1 nm k d binding affinity for its antigen as measured by octet kinetic assay ( fig. 6b and c) . the affinity is high as a monomeric single-domain soluble protein isolated from a naïve shark library without immunization. we also produced the type i binder (mers a8) and type ii binder mers a7 in e. coli. the protein yield varied based on protein sequences. pe38-b6 has a relatively low yield (3 mg from 2 l e. coli culture). mers a8 binder yielded 3.1 mg and mers a7 yielded 8.7 mg of single-domain soluble protein from 600 ml e. coli culture. nickel-charged histrap columns (ge healthcare, chicago, il) were used to purify these proteins from the polymyxin b lysed bacteria pellet supernatants. the elution profile showed the protein elution in figure 7a and d. sodium dodecyl sulfate polyacrylamide gel electrophoresis (sds-page) of the elution peaks in figure 7b and e showed the later peak eluted by higher imidazole concentrations had over 90% purity of the target soluble v nar s. both mers a8 and a7 had specific binding to the phage panning antigen mers spike protein in figure 7c and f. the type i binder (mers a8) had higher signals. tsk size exclusion column purification for the type ii binder pe38-b6-his soluble single-domain protein showed this protein is monomeric. the 16.8 kda protein was eluted with one peak that is slightly earlier than 13.7 kda control protein peak ( fig. 7g and h) . taken together, binders to tumor and viral antigens, including type i and type ii single domains containing multiple cysteine residues, can be selected from the library and produced as functional single-domain proteins in e. coli. our data indicate that the new shark phage library is a valuable platform for discovery of v nar binders. in the present study, we developed the easel method to construct phage display libraries based on pcr extension assembly followed by self-ligation. by using this easel method, we successfully constructed a large phagedisplayed v nar library with a size of 10 10 from six antigen-antibody therapeutics, 2019 5 we also demonstrated that type i and type ii shark v nar binders can be produced from e. coli as functional single-domain proteins. the large nurse shark v nar singledomain phage library described here provides an attractive single-domain antibody platform for drug discovery. in this study, we use two canonical cysteines located at both amino acid 21 and 82 as a key criterion to characterize type i-iv v nar families. about 5% of the total v nar s do not fit in any one of the four known v nar type families. we have identified ∼11% of the total v nar s are classical type i and 57% classical type ii. while a majority of the v nar s are either classical type i or type ii, ∼30% of the v nar s do not fit any of the four classical types. most of these nonclassical v nar s have various numbers of cysteines (fig. 2) . future structural and functional analysis of the binders isolated from the library for various antigens will be needed to understand the role of these non-classical v nar s in therapeutic antibody discovery and engineering. the key for a successful isolation of antibodies is the phage library used for the selection [30] . various methods have been employed to make antibody phage display libraries. most widely used methods consist of pcr amplification of antibody fragments, followed by enzymatic digestion and ligation with the vector. these methods are time consuming and have a low efficiency in the ligation and transformation step. in the present study, we developed the easel method to construct a large shark v nar phage library. we used a labeling pcr to add homologue regions to the v nar pool. then an overlap extension pcr was used to assemble v nar and phagemid dna, followed by self-ligation of the whole library dna. it only took several weeks to make the shark v nar library while conventional approaches would require several months. our protocol has significantly shortened the time required to construct a large gene library. another contemporary method used for gene cloning is "gibson assembly". this method is based on enzymatic assembly for joining multiple overlapping dna fragments into a single reaction system [31] . our method may be more efficient than gibson assembly. gibson assembly requires 5-exonuclease to nick the 5-terminals of the dna fragments to make them complementary followed by annealing together. dna polymerase was then used to fill the gap, and dna ligase was used to seal the gap. therefore, the two termini that antibody therapeutics, 2019 7 are being ligated have to be identical for each other for ∼20 nucleotides. the gibson assembly reaction may fail due to complications related to total repeat density (direct, inverse, and palindromic repeat elements), extremes in g/c content, and secondary structures near the 3' and 5' termini of the sequence. to our best knowledge, there is no report using the gibson assembly for the development of a large phage-displayed antibody library. in our method, we only need the conventional t4 dna ligase to run a standard ligation at 16 • c for 12-24 h. the two ends of the dna are blunt and do not need to be identical for blunt-end ligation. therefore, our method is similar to traditional blunt-end ligation, and the terminal part of the dna fragment sequence can be varied. during the preparation of this manuscript, our laboratory has applied the easel method to successfully make 20 large camel v h h singledomain phage libraries. taken together, the new easel library construction method is robust, comprehensive, and quick. the new easel method also maximized the sequence diversity of cdr3 represented in the phage library to increase the selection of high-affinity binders. a previous study produced a shark phage library with 10 7 diversity using the conventional cloning method. our library has 10 10 diversity and contains all known four types of v nar single domains. the majority of the sequences are type ii and type i v nar as shown in figure 2c . interestingly, type iv v nar sequences are significantly under-represented as shown in figure 2c . the shark v nar sequences in the ncbi database are mostly derived from bamboo shark, dogfish shark, wobbegong shark, and other types of smaller sharks [12] [13] [14] [15] [16] [17] . the percentage of v nar types can be significantly different between various species of sharks. interestingly, our deep sequencing analysis showed that 56 174 of the nurse shark v nar sequences in our library were not categorized in any one of the known v nar types (types i-iv). whether these novel types of v nar s possess unique confirmations and biophysical properties should be analyzed structurally and functionally when binders for cancer or viral antigens are found from these novel types of v nar s in the future. since the method we used to assemble the unique v nar sequences for analysis is highly accurate and the number of the unique sequences analyzed is large, we used unbiased methods to analyze all the sequences for cysteine number and cdr3 length without further subdividing them into the four known v nar types. a significant percentage of the sequences are not classical v nar as defined in the known four types. analyzing the data sequences altogether would provide more comprehensive picture of the sequence patterns in the naïve nurse shark without having to fit the sequences into a defined v nar type. the extra cysteines in both type i and type ii v nar s are important for stabilizing the antigen-binding regions [11] . extra disulfide bonds formed by these cysteines are essential for forming diverse antigen-binding surfaces. it may be one strategy for increasing antigen-binding region diversity in heavy chain-only antibodies. interestingly, the sequence variation mostly lies in cdr3 with minimal variation in cdr1, hv2, and hv4. previous literature suggested there are sequence variability in hv2 and hv4 during in vivo affinity maturation [24] . it was also shown that somatic mutations within hv2/4 can contribute to antigen binding [21] . however, ngs results in the present study showed there is minimal sequence variability in cdr1, hv2, and hv4 in our naïve shark library. it is possible that these naïve sharks used in our study have been kept in captivity for a long time, therefore do not have as much sequences diversity in antibody therapeutics, 2019 9 cdr1, hv2, and hv4. another major type of heavy chain-only domain antibody v h h from camels also has highly diversified cdr3. the lengths of v h h cdr3 are much longer than conventional vh from camel igg. the median cdr3 length of v h h is 20 amino acids (similar with shark v nar ), whereas median length for camel vh cdr3 is only 15 amino acids [32] . however, there is no comprehensive study on the cysteine numbers and locations in camel v h h sequences for comparison with shark v nar . we hypothesize that the diversity of this large naïve shark library can be further increased significantly by randomizing the cdr1 sequences and keeping the highly diverse cdr3 [33, 34] . for example, the eight amino acids in cdr1 can be completely randomized to further diversify our v nar library. furthermore, affinity maturation of the binders in figure 6 can be performed by randomizing cdr1. in summary, we believe this shark library has a suitable size and diversity for antibody discovery and can potentially be used as a large single-domain antibody discovery platform. the potential immunogenicity of shark antibodies could be a concern in clinical applications. these concerns could be addressed by identifying the b-cell and t-cell immunogenic epitopes and silence them by specific site mutations [35, 36] . furthermore, durable immune tolerance to highly immunogenic proteins (e.g. bacterial toxins) can be induced by nanoparticles containing rapamycin in vivo [37] . in conclusion, we have built a large, highly diverse phage-displayed v nar library using b cells isolated from nurse sharks. it provides a new platform to discover single-domain antibodies for therapeutic and diagnostic applications. the easel library construction method described here may be applicable to the construction of other large gene expression libraries including antibody libraries derived from other species and t-cell receptors. the gpc3-positive human hepatocellular carcinoma cell line hepg2 was maintained as adherent monolayer cultures in dmem medium (invitrogen, carlsbad, ca) supplemented with 10% fetal bovine serum (hyclone, logan, ut), 1% l-glutamine, and 1% penicillin-streptomycin (invitrogen) in a 5% co 2 incubator at 37 • c. gpc3-negative a431 cells (human epithelial carcinoma cell line) were engineered in our laboratory to express high levels of human gpc3 by transfection with a plasmid encoding full-length gpc3 [38, 39] . both a431 and the stably transfected cells (g1) [39] were maintained in dmem with supplements. the gpc3 peptide (a.a. 510-560) was synthesized. the recombinant extracellular domain of her2 and pd1, the s-protein of mers and srs were purchased from sino biological (beijing, china). the recombinant pe38 and mpe24 were made in our laboratory according to the pub-lished methods [40] . the recombinant gpc3-hfc was generated as previously published [41] . six naïve nurse sharks (three males and three females, ranging from 2.5 to 6 ft long) were bled for 10 ml of blood in phosphate buffered saline (pbs)/1000 iu/ml heparin. the buffy coat was collected, spun, and resuspended in 3.5 ml of trizol for rna preparation. total rna was isolated using the trizol reagent (thermo fisher scientific, grand island, ny) according to the manufacturer's instruction. five micrograms of total rna were reverse-transcribed into cdna in a total of 20 μl volume using the superscript iii first-strand synthesis system (thermo fisher scientific) according to the manufacturer's instruction. one forward primer and two reverse primers were synthesized to pcr amplify the v nar sequence from the cdna product. forward primer ignar-f: gctc-gagtgaccaaacaccg, reverse primer ignar-r1: ggtggccggcctggccactattcacagtcacgg cagtgccat, reverse primer ignar-r2: ggtggc-cggcctggccactattcacagtcacgacagtgc-cacc. primer pairs of ignar-f/ignar-r1, ignar-f/ignar-r1 were used to amplify the v nar fragment in a 50 μl of pcr volume that contains 1 μl of cdna product. the pcr cycling parameters were the following: initial denaturation at 94 • c for 3 min, 40 cycles of denaturation at 98 • c for 10 s, annealing at 60 • c for 15 s, and elongation at 72 • c for 45 s using primestar (clonetech). in the meantime, the linear vector backbone fragment was prepared by pcr using forward primer ignarcom3x-f: agtggccaggccggccacc, and reverse primer ignarcom3x-r: ggccgcctgggccacggta. five nanograms of the plasmid pcomb3x was used as the template in a total of 50 μl of pcr reaction volume. the primers to amplify the vector backbone were forward ignarcom3x-f: agtggccaggccggccacc and reverse ignarcom3x-r: ggccgcctgggccacg-gta. the pcr cycling parameters were the following: initial denaturation at 94 • c for 3 min, then 25 cycles of denaturation at 98 • c for 10 s, annealing at 60 • c for 15 s, and elongation at 72 • c for 3 min using primestar (takara, shiga, japan). to assemble the v nar and the amplified vector backbone, 100 ng of vector backbone was mixed with 30 ng of v nar pcr products in a 50 μl of pcr reaction volume, the overlapping extension pcr was primed by primers of ignar-f/ignarcom3x-r using primestar. twenty micrograms of the assembled pcr product were circularized by intra-molecular self-ligation in a 1 ml of ligation buffer using t4 dna ligase (new england biolabs, ipswich, ma). the ligation products were cleaned up by removing the enzymes and transformed into 500 μl of electroporation competent tg1 cells (lucigen, middleton, wi) to make the library. this method is referred to as easel method in this study. ngs of the library was generated from shark v nar insert dna digested out of plasmid library using xhoi and msci restriction enzymes (new england biolabs). the shark v nar library was excised out from the vector with restriction enzyme (xhoi and msci) and gel purified. the insert fragments were ligated to illumina adaptor and sequenced on illumina miseq with 2 × 250 bp paired-end reads using both nebnext ultra ii dna library preparation kit and kappa hyper prep library preparation kit. paired-end reads were merged to cover the full length of the insert using flash [42] . merged sequence reads were then analyzed with custom perl scripts. all dna sequences were oriented and translated to protein sequences. sequences with stop codons were removed from further analysis. we also required the amino acid sequences to start with "rv" at the n-terminus and end with "xxxgtxxtvns" at the c-terminus to be considered as full-length v nar s. after the selection with these criteria, there are almost 2 million v nar amino acid sequences from this experiment, with more than 1 million unique v nar sequences. we aligned all v nar sequences by anchoring the constant regions and allow cdr3 regions to have variable lengths from 0 to 40 amino acids. we then calculated the variability according to methods described in wu and kabat [43] . we further classified v nar sequences into different subtypes based on residue numbers and positions. type i and type ii/iii sequences were also analyzed separately for the cdr3 lengths, total cysteine numbers, and cdr3 cysteine numbers. library tg1 bacterial stock was inoculated into 2.5 l of 2yt media containing 2% glucose, 100 μg/ml ampicillin, and cultured at 37 • c with shaking (250 rpm). when the cells reached mid-log phase (od 600 between 0.4-0.8), super-infection was performed by adding helper phage m13ko7 at 5 × 10 9 pfu/ml. after 1 h of continued growth, the tg1 cells were pelleted and resuspended in 2.5 l of 2yt media containing 100 μg/ml ampicillin and 50 μg/ml kanamycin, and incubated at 25 • c overnight. after the cells were centrifuged and filtered with a 0.22 μm membrane, the supernatant was stored at 4 • c for panning. the phage panning protocol has been described previously [44, 45] . briefly, a 96 well maxisorp elisa plate (nunc/thermo fisher scientific, rochester, ny) was used to capture various antigens (100 μg/ml) in pbs buffer at 4 • c overnight. after the coating buffer was decanted, the plate was treated with blocking buffer (2% bovine serum albumin in pbs) at room temperature for 1 h. then 30 μl pre-blocked phage supernatant (typically contained 10 10 -10 11 cfu) in 30 μl blocking buffer was added per well for 1 h at room temperature to allow binding. after four washes with pbs containing 0.05% tween-20, bound phages were eluted with 100 mm triethylamine. after four rounds of panning, single colonies were picked and identified by using phage elisa. the antigenic proteins were used to coat a 96 well plate at 5 μg/ml in pbs buffer, 50 μl/well, at 4 • c overnight. the irrelevant antigen used was 5 μg/ml bsa in pbs. after the plate was blocked with 2% bsa in pbs buffer, 25 μl pre-blocked phage supernatant (typically 10 10 -10 11 cfu) were added to the plate. binding was detected by hrp conjugated mouse anti-m13 antibody (ge healthcare life sciences, pittsburg, pa). the cut-off value for positive binder was set as 3× higher signal of antigen binding compared to background noise. the pcomb3x phagemids containing the v nar binders were transformed into hb2151 e. coli cells. the formed colonies were pooled for culture in 2 l 2yt media containing 2% glucose, 100 μg/ml ampicillin at 37 • c until the od600 reaches 0.8-1. culture media was then replaced with 2yt media containing 1 mm iptg (sigma), 100 μg/ml ampicillin, and shook at 30 • c overnight for soluble protein production. bacteria pellet was spun down and lysed with polymyxin b (sigma) for 1 h at 37 • c to release the soluble protein. the supernatant was harvested after lysis and purified using histrap column (ge healthcare) using akta. the shark single-domain soluble protein pe38-b6-his was buffer exchanged in pbs buffer after purification. the binding kinetics of pe38-b6-his was measured with fortebio octet red96 located at the biophysics core in national heart, lung and blood institute. pe38-b6-his diluted in assay buffer pbs supplemented with 0.1% tween-20 and 1% (w/v) bsa. the octet red96 program was as follows: 10 min presoak, 120 s baseline establishment, 300 s antigen loading, 60 s baseline re-establishment after antigen loading, 600 s pe38-b6-his association, 30 min dissociation. a total of 1 μg/ml pe38-b6-his was used to load the ni-nta biosensor, and serial diluted antigen protein pe38 was used for binding assay. the binding kinetics was calculated with fortebio octet red96 software. all statistical analyses were conducted using graphpad prism 5 (graphpad software, inc., la jolla, ca). differences between groups were analyzed using the two-tailed student's t-test of means. antibody-based immunotherapy of cancer single domain antibodies: promising experimental and therapeutic tools in infection and immunity antibody repertoire development in cartilaginous fish the structural analysis of shark ignar antibodies reveals evolutionary principles of immunoglobulins diversity and repertoire of igw and igm vh families in the newborn nurse shark unprecedented multiplicity of ig transmembrane and secretory mrna forms in the cartilaginous fish structural analysis of the nurse shark (new) antigen receptor (nar): molecular convergence of nar and unusual mammalian immunoglobulins the development of nanobodies for therapeutic applications nanobodies as versatile tools to understand, diagnose, visualize and treat cancer ribosome display and affinity maturation: from antibodies to single v-domains and steps towards cancer therapeutics crystal structure of a shark single-domain antibody v region in complex with lysozyme dimerisation strategies for shark ignar single domain antibody fragments dissection of the ignar v domain: molecular scanning and orthologue database mining define novel ignar hallmarks and affinity maturation mechanisms structural insights and biomedical potential of ignar scaffolds from sharks shark novel antigen receptors--the next generation of biologic therapeutics? structural analysis, selection, and ontogeny of the shark new antigen receptor (ignar): identification of a new locus preferentially expressed in early development display scaffolds: protein engineering for novel therapeutics inaugural editorial: searching for magic bullets comparisons of the intraocular tissue distribution, pharmacokinetics, and safety of 125i-labeled full-length and fab antibodies in rhesus monkeys following intravitreal administration selection of cholera toxin specific ignar single-domain antibodies from a naive shark library maturation of shark single-domain (ignar) antibodies: evidence for induced-fit binding selection and characterization of naturally occurring single-domain (ignar) antibody fragments from immunized sharks by phage display shark immunity bites back: affinity maturation and memory response in the nurse shark, ginglymostoma cirratum first molecular and biochemical analysis of in vivo affinity maturation in an ectothermic vertebrate rapid isolation of ignar variable single-domain antibody fragments from a shark synthetic library isolation of anti-toxin single domain antibodies from a semi-synthetic spiny dogfish shark display library isolation of the new antigen receptor from wobbegong sharks, and use as a scaffold for the display of protein loop libraries isolation and characterization of an ignar variable domain specific for the human mitochondrial translocase receptor tom70 selection and affinity maturation of ignar variable domains targeting plasmodium falciparum ama1 construction of human naive antibody gene libraries enzymatic assembly of dna molecules up to several hundred kilobases comparative analysis of immune repertoires between bactrian camel's conventional and heavy-chain antibodies generation of semi-synthetic shark ignar single-domain antibody libraries construction of histidine-enriched shark ignar variable domain antibody libraries for the isolation of ph-sensitive vnar fragments recombinant immunotoxin with t-cell epitope mutations that greatly reduce immunogenicity for treatment of mesothelin-expressing tumors a recombinant immunotoxin against the tumor-associated antigen mesothelin reengineered for high activity, low off-target toxicity, and reduced antigenicity tolerogenic nanoparticles restore the antitumor activity of recombinant immunotoxins by mitigating immunogenicity inactivation of wnt signaling by a human antibody that recognizes the heparan sulfate chains of glypican-3 for liver cancer therapy high-affinity monoclonal antibodies to cell surface tumor antigen glypican-3 generated through a combination of peptide immunization and flow cytometry screening immunotoxin targeting glypican-3 regresses liver cancer via dual inhibition of wnt signalling and protein synthesis therapeutically targeting glypican-3 via a conformation-specific single-domain antibody in hepatocellular carcinoma flash: fast length adjustment of short reads to improve genome assemblies an analysis of the sequences of the variable regions of bence jones proteins and myeloma light chains and their implications for antibody complementarity in vitro antibody affinity maturation targeting germline hotspots in vitro antibody evolution targeting germline hot spots to increase activity of an anti-cd22 immunotoxin we thank dr gregory piszczek from biophysics core facility in national heart, lung, and blood institute for octet assay technical support. antibody therapeutics, 2019 11 key: cord-314328-gft6phd6 authors: lawrence, c.; seckold, r.; smart, c.; king, b. r.; howley, p.; feltrin, r.; smith, t. a.; roy, r.; lopez, p. title: increased paediatric presentations of severe diabetic ketoacidosis in an australian tertiary centre during the covid‐19 pandemic date: 2020-10-23 journal: diabet med doi: 10.1111/dme.14417 sha: doc_id: 314328 cord_uid: gft6phd6 aims: to determine if the frequency of severe diabetic ketoacidosis at presentation of new‐onset type 1 diabetes to an australian tertiary centre increased during the initial period of restrictions resulting from the covid‐19 pandemic (march to may 2020). methods: data were collected on presentations of newly diagnosed type 1 diabetes as well as on all paediatric presentations to the emergency department of a tertiary centre between 2015 and 2020. data from the period of initial covid restrictions in australia (march to may 2020) were compared to the period march to may of the previous 5 years (pre‐pandemic periods). results: the number of new diagnoses of type 1 diabetes was comparable in the pandemic period and pre‐pandemic periods (11 in 2020 vs range 6–10 in 2015–2019). the frequency of severe diabetic ketoacidosis was significantly higher in the pandemic period compared to the pre‐pandemic periods (45% vs 5%; p <0.003), odds ratio 16.7 (95% ci 2.0, 194.7). the overall frequency of diabetic ketoacidosis was also significantly higher during the pandemic period (73% vs 26%; p <0.007), odds ratio 7.5 (95% ci 1.7, 33.5). none of the individuals tested positive for covid‐19. presentations of people aged <18 years to the emergency department decreased by 27% in the pandemic period compared to the average of the pre‐pandemic periods (4799 vs 6550; range 6268 to 7131). conclusions: a significant increase in the frequency of severe diabetic ketoacidosis at presentation of type 1 diabetes was observed during the initial period of covid‐19 restrictions. we hypothesize that concern about presenting to hospital during a pandemic led to a delay in diagnosis. these data have important implications for advocacy of seeking healthcare for non‐pandemic‐related conditions during a global pandemic. march 3 . restrictions enacted in australia included school shutdowns and the closure of non-essential businesses, while the majority of outpatient health appointments were conducted by telehealth. these restrictions successfully flattened the curve with the expected surge of covid-19 cases and uncontrolled community spread not seen in australia during the time period described in this study. however, concern has emerged that, with fewer presentations to general practitioners and emergency departments 4 , other serious health concerns may have gone undiagnosed. the prevalence of diabetic ketoacidosis (dka) at diagnosis of type 1 diabetes in the paediatric population in australia was recently reported as 24.5% 5 . dka is an avoidable complication if symptoms and signs of diabetes mellitus are recognized early 6 . dka places increased burden on the healthcare system and may require intensive care support in tertiary care settings for management. additionally the presence of dka at diagnosis has been associated with poor long-term glycaemic control 7 . during a pandemic, it is important to minimize avoidable admissions to intensive care units when resources may be limited. emerging research during the covid-19 pandemic has shown an increase in children with type 1 diabetes presenting with dka in countries such as italy 8 and the usa 9 . a recent study of the german population found the frequency of severe dka was significantly higher during the covid-19 pandemic, and that children under the age of 6 years were at the highest risk 10 . we report one australian centre's experience of presentations of newly diagnosed type 1 diabetes in a paediatric cohort during the covid-19 pandemic restrictions (march to may inclusive) compared to pre-pandemic presentations in the march to may periods of the years 2015 to 2019. all children and adolescents aged <18 years with the initial diagnosis of type 1 diabetes treated at the john hunter children's hospital between 1 january 2015 and 31 may 2020 were identified from the hospital paediatric endocrine database and digital medical records. age, date of diagnosis, hba 1c , initial venous blood gas result (ph, bicarbonate and glucose), c-peptide, type 1 diabetes-associated antibody status (presence of glutamic acid decarboxylase, islet antigen 2, islet cell and insulin antibodies) and the results of covid-19 tests were collected. in addition, the total number of presentations of children and young people aged <18 years to the john hunter hospital emergency department was collected for the march to may period in 2015 to 2020. we defined data collected from 1 march 2020 to 31 may 2020 as the 'pandemic period' and the corresponding march to may periods in the 5 years prior to this as 'pre-pandemic' conditions. diabetic ketoacidosis was defined as a venous ph <7.3 on presentation, with severe dka represented by a ph <7.1 as per the 2018 international society for paediatric and adolescent diabetes (ispad) guidelines 11 . a diagnosis of type 1 diabetes was defined as the presence of dka or the presence of hyperglycaemia and autoantibodies associated with type 1 diabetes 12 . odds ratios, fisher's exact test and anova were used to test for differences between the pandemic and pre-pandemic groups. ethics approval was granted by the hunter new england health research ethics committee (approval number: au202006-10). the age of onset, gender, total presentations and classification by severity of dka are presented in table 1 and fig. 1 for each of the march to may periods in 2015 to 2020. data collection was complete, with no missing data. the numbers of new presentations of type 1 diabetes in the march to may period across 2015 to 2020 were fairly consistent; the prepandemic number ranged from 6 to 10 (median 9) across 2015 to 2019, compared with 11 in 2020. there was no significant difference in age or gender across the groups. the frequency of severe dka at the time of new type 1 diabetes diagnosis was significantly higher during the period of pandemic restrictions compared to pre-pandemic (45% vs 5%; p <0.003), odds ratio of 16.7 (95% ci 2.0, 194.7). the frequency of dka (mild, moderate or severe dka) was also significantly higher during the period of pandemic restrictions compared to pre-pandemic conditions (73% vs 26%; p • diabetic ketoacidosis is an avoidable complication of type 1 diabetes, associated with significant morbidity and, rarely, mortality. • during covid-19 restrictions, healthcare utilization has changed significantly. • we report a significant increase in the frequency of severe diabetic ketoacidosis at presentation of new-onset type 1 diabetes during the covid-19 pandemic at our tertiary centre. this study reports a significant increase in the frequency of children and adolescents presenting with severe dka at onset of type 1 diabetes during the covid-19 pandemic. the reason for this is unclear. this was not attributable to covid-19 infection in the individuals. however, we hypothesize that presentations with new-onset type 1 diabetes may have been delayed as a result of concern regarding covid-19 and the restrictions put in place to combat the covid-19 pandemic. during the pandemic period, people were advised to minimize contact with others. children had less contact with people outside of their primary household, with online learning rather than face-to-face schooling, a reduction in contact with friends and family and an increase in virtual medical appointments. unemployment rates rose and many workers had to adapt to working from home. disruption to everyday routine could easily have led to the symptoms of type 1 diabetes being missed. additionally, the media showed images of people lined up outside hospitals to be tested for covid-19 and overseas infection rates and deaths were widely reported. it is possible that people felt that going to their doctor or the emergency department would have placed them at risk of contracting covid-19. this is supported by the fact that emergency department presentations to the john hunter children's hospital fell during this time period. the increase in presentations of children and adolescents with severe dka at diagnosis of type 1 diabetes during the covid-19 pandemic is a major concern. not only is severe dka life-threatening, but it also requires the use of intensive care beds and resources during a period of potential high demand. previous research has shown that delayed recognition of type 1 diabetes symptoms is associated with dka at disease onset 6 . however, early diagnosis of type 1 diabetes requires people to have contact with health professionals and present to hospitals. interventions aimed at raising community awareness of the signs and symptoms of type 1 diabetes have been shown to reduce the frequency of dka at diagnosis 13, 14 . during a pandemic where schools are in shutdown and many primary care consultations occur via telehealth, alternative ways of raising awareness need to be considered. it is vital that in the eventuality of a subsequent wave of covid-19, strategies are implemented in order to avoid a similar increase in severe dka. these could include social media campaigns, traditional media advertising, mailouts or advertising in local primary health services. this observational study adds to the limited existing literature describing an increased frequency of severe dka during the covid-19 pandemic. although this study reports the experience of a single centre, the john hunter children's hospital diabetes centre provides care for all children with type 1 diabetes over the large geographic region of newcastle and the greater hunter. our experience during the period of pandemic restrictions was anomalous in comparison with the preceding 5 years at our centre. the results reported in this study are likely to be representative of other australian tertiary centres, most of which have experienced some degree of lockdown. performing similar studies in centres with differing case rates of covid-19 and severity of restrictions enacted would help determine if our experience is universal. limitations of this study include the small sample size, which precludes stratified analyses and increases the chance of type ii errors. this study is hypothesis-generating; additional studies that evaluate the reasons for delayed presentations of type 1 diabetes could be used to target campaigns more effectively to reduce this delay. in summary, in the present study we report a significant increase in presentations of severe dka in a paediatric population with newly diagnosed type 1 diabetes during the covid-19 pandemic when social distancing restrictions were enacted. this illustrates the need to encourage children and their families to continue to seek and receive healthcare for non-pandemic-related health concerns during a global pandemic. detai l/30-01-2020-state ment-on-the-secon d-meeti ng-of-the-inter natio nal-healt h-regul ation s-(2005)-emerg ency-commi ttee-regar ding-the-outbr eak-of-novel -coron aviru s-(2019-ncov) australian government department of health. australian health sector emergency response plan for novel coronavirus wa confirms first novel coronavirus death royal australian college of general practitioners. racgp launches nationwide campaign to stop people neglecting their health due to covid-19 temporal trends in diabetic ketoacidosis at diagnosis of paediatric type 1 diabetes between 2006 and 2016: results from 13 countries in three continents is diabetic ketoacidosis at disease onset a result of missed diagnosis? diabetic ketoacidosis at diagnosis of type 1 diabetes predicts poor long-term glycemic control diabetes study group of the italian society for pediatric endocrinology and diabetes* et al. has covid-19 delayed the diagnosis and worsened the presentation of type 1 diabetes in children? diabetes care unintended consequences of covid-19: remember general pediatrics ketoacidosis in children and adolescents with newly diagnosed type 1 diabetes during the covid-19 pandemic in germany diabetic ketoacidosis and the hyperglycemic hyperosmolar state definition, epidemiology, and classification of diabetes in children and adolescents effectiveness of a prevention program for diabetic ketoacidosis in children. an 8-year study in schools and private practices a diabetes awareness campaign prevents diabetic ketoacidosis in children at their initial presentation with type 1 diabetes: population awareness prevents dka the authors would like to thank dr michael anscombe, director of paediatric emergency, and the john hunter none declared. children's hospital paediatric emergency department team for their assistance in data collection and care of acutely unwell children with type 1 diabetes. the authors would also like to thank prof. patricia crock, dr komal vora and the john hunter children's hospital paediatric diabetes team for caring for children with type 1 diabetes in the hunter region. the authors would particularly like to acknowledge the children and families cared for by the john hunter children's hospital. c. lawrence https://orcid.org/0000-0002-0995-5714 c. smart https://orcid.org/0000-0003-3104-8800 b. r. king https://orcid.org/0000-0002-8958-7404 p. lopez https://orcid.org/0000-0003-0831-199x key: cord-240471-rz0pj5a3 authors: dodds, p. s.; minot, j. r.; arnold, m. v.; alshaabi, t.; adams, j. l.; dewhurst, d. r.; reagan, a. j.; danforth, c. m. title: probability-turbulence divergence: a tunable allotaxonometric instrument for comparing heavy-tailed categorical distributions date: 2020-08-30 journal: nan doi: nan sha: doc_id: 240471 cord_uid: rz0pj5a3 real-world complex systems often comprise many distinct types of elements as well as many more types of networked interactions between elements. when the relative abundances of types can be measured well, we further observe heavy-tailed categorical distributions for type frequencies. for the comparison of type frequency distributions of two systems or a system with itself at different time points in time -a facet of allotaxonometry -a great range of probability divergences are available. here, we introduce and explore `probability-turbulence divergence', a tunable, straightforward, and interpretable instrument for comparing normalizable categorical frequency distributions. we model probability-turbulence divergence (ptd) after rank-turbulence divergence (rtd). while probability-turbulence divergence is more limited in application than rank-turbulence divergence, it is more sensitive to changes in type frequency. we build allotaxonographs to display probability turbulence, incorporating a way to visually accommodate zero probabilities for `exclusive types' which are types that appear in only one system. we explore comparisons of example distributions taken from literature, social media, and ecology. we show how probability-turbulence divergence either explicitly or functionally generalizes many existing kinds of distances and measures, including, as special cases, $l^{(p)}$ norms, the s{o}rensen-dice coefficient (the $f_1$ statistic), and the hellinger distance. we discuss similarities with the generalized entropies of r{'e}nyi and tsallis, and the diversity indices (or hill numbers) from ecology. we close with thoughts on open problems concerning the optimization of the tuning of rankand probability-turbulence divergence. driven by an interest in developing allotaxonometry [1] -the detailed comparison of any two complex systems comprising many types of elements-we find ourselves needing to compare zipf distributions: heavytailed categorical distributions of type frequencies [2] [3] [4] [5] . we take a relaxed definition of what a heavy tail means for a distribution: a slow decay over orders of magnitude in type rank. though not required, power-law decay tails are emblematic signatures of heavy-tailed distributions commonly presented by complex systems [6] [7] [8] [9] [10] , both observed and theoretical, and provide important examples to contemplate in our efforts to develop a comparison tool. across fields, efforts to measure and explain how two probability distributions differ have led to the development of a great many probability divergences [11] [12] [13] [14] . divergences have been constructed for a host of motivations quite apart from our focus here on allotaxonometry, with example families scaffolded around l p -norms, inner products, and information-theoretic structures. as we will discuss, for heavy-tailed distribution comparisons * peter.dodds@uvm.edu which exhibit variable 'probability turbulence' [1, 15] , we find these divergences lack appropriate adaptability. here, we introduce a tunable, interpretable instrument that we call probability-turbulence divergence (ptd) along with related allotaxonographs-visualizations which show in detail how two categorical distributions differ according to a given measure. we refer the reader to ref. [1] for our motivation for creating allotaxonometry and allotaxonographs, the notion of rank turbulence, and a detailed justification for the form of rankturbulence divergence (rtd) we developed there. we establish probability-turbulence divergence using largely the same arguments. we will therefore be concise in our presentation and expand only when the probability version's behavior departs from that of its rank counterpart. in sec. ii, we formally define probability-turbulence divergence. we describe the divergence's general analytic behavior as a function of its single parameter, α, and we determine its form for the two limits of the parameter, α=0 and α=∞. when α=0, in particular, we find an interesting departure from the equivalent tuning for rank-turbulence divergence, and which we will later connect to the sørensen-dice coefficient [16, 17] and the f 1 score [18] . in sec. iii, we then provide realizations of probabilityturbulence divergence as an instrument through example allotaxongraphs. for three disparate examples, we con-typeset by revt e x arxiv:2008.13078v1 [physics.soc-ph] 30 aug 2020 sider 1. frequency of n-gram use in jane's austen's pride and prejudice, 2. frequency of n-gram use on twitter, and 3. tree species abundance [19] . we show how for the kinds of heavy-tailed distributions we are interested in that a probability-turbulence divergence histogram can be constructed to accommodate both a logarithmic scale and the presence of zero probabilities. similar to rankturbulence divergence histograms, these graphs clearly show whether or not a probability-based divergence is a suitable choice for any given comparison. to feature the tunability of probability-turbulence divergence, we present flipbooks as part of our online appendices (compstorylab.org/allotaxonometry/) for allotaxonometry. in sec. iv, we show that probability-turbulence divergence is either a generalization of or may be connected to a number of other kinds of divergences and similarities (e.g., the sørensen-dice coefficient), and then discuss limited functional similarities with the rényi entropy and diversity indices [20] [21] [22] [23] [24] . we outline data and allotaxonometry code in sec. v and offer some concluding thoughts in sec. vi. we aim to compare two systems ω 1 and ω 2 for both of which we have a list of component types and their probabilities. for simplicity, we will speak of probability, acknowledging that relative frequency, rate of usage, or some other term may be the more appropriate descriptor for a given system. we denote a type by τ and its probability in the two systems as p τ,1 and p τ,2 . we represent the probability distributions for the two systems as p 2 and p 1 . we call types that are present in one system only 'exclusive types'. in general, we will use expressions of the form ω (1) -exclusive and ω (2) -exclusive to indicate to which system a type solely belongs. in general, we are interested in divergences that are some function of a sum of contributions by type. here, we will consider a single parameter family of divergences that are of the simplest form, i.e., a direct sum of contributions: by the rank-ordered set r 1,2;α , we indicate the union of all types from both systems, sequenced such that the contributions δd p α,τ (p 1 p 2 ) are monotonically decreasing (hence the necessity of an α subscript). we impose this order for general good housekeeping, secondarily allowing us to handle possibilities such as truncated summations due to sampling, or convergence issues for theoretical examples. following on from ref. [1] , we define probabilityturbulence divergence as: . (2) where the parameter α may be tuned from 0 to ∞ and n p 1,2;α is a normalization factor. per ref. [1] and below in sec. ii b, the roles of the prefactor (α + 1)/α and the power 1/(α + 1) are to govern the behavior of ptd in the limit α → 0. by construction and regardless of the choice of normalization factor, we can see from eq. (2) that probabilityturbulence divergence will equal 0 when both distributions are the same. (we show below that for α = 0, distinct distributions can also register d p α (p 1 p 2 ) = 0.) the core of eq. (2) is the absolute value of the difference of each type τ 's probability raised to the power of α: this α-tuned quantity controls the order of contributions by types to the overall value of ptd. as α → 0, lower probabilities-corresponding to the rare types-are relatively accentuated. for α → ∞, the higher of the two probabilities will dominate (unless they are equal), meaning the most common types will come to the fore. as for rank-turbulence divergence, we choose n p 1,2;α so that when the two systems are entirely disjoint-that is, they share no types-then probability-turbulence divergence maximizes at 1. the normalization is thus specific to the two distributions being compared. we imagine that the types in each system have an extra descriptor specifying belonging to ω (1) or ω (2) . with no matching types, the probability of a type present in one system is zero in the other, and the sum can be split between the two systems' types: where r 1 and r 2 are the zipf ordered sets of types for each system. we can more compactly express the normalization as: where, as for the definition of probability-turbulence divergence in eq. (2), the sum for the normalization is again over the ordered set r 1,2;α . types that appear in both systems will have their contribution [ p τ,1 ] α/(α+1) and [ p τ,2 ] α/(α+1) counted appropriately. b. limit of α=0 for probability-turbulence divergence the limit of α=0 requires some care and will vary from the equivalent limit for rank-turbulence divergence [1] . first, at the level of individual type contribution, if both p τ,1 > 0 and p τ,2 > 0 then if instead a type τ is exclusive to one system, meaning either p τ,1 = 0 or p τ,2 = 0, then the limit diverges as 1/α, which would seem problematic. we nevertheless will arrive at a well-behaved divergence through the normalization term n p 1,2;0 . requiring as we have that the extreme of disjoint systems have a divergence of 1, we observe that each of the types in the case of disjoint systems would contribute 1/α. therefore, in the α → 0 limit, we must have: because the normalization also diverges as 1/α, the divergence will be zero when there are no exclusive types and non-zero when there are exclusive types. we can combine these cases into a single expression: the term δ pτ,1,0 + δ 0,pτ,2 returns 1 if either p τ,1 = 0 or p τ,2 = 0, and 0 otherwise when both p τ,1 > 0 and p τ,2 > 0. (by construction, we cannot have p τ,1 = p τ,2 = 0 as each type must be present in either one or both systems. ) we see then that d p 0 (p 1 p 2 ) is the ratio of types that are exclusive to one system relative to the total possible such types, n 1 + n 2 . if and only if all types appear in both systems with whatever variation in probabilities, then d p 0 (p 1 p 2 ) = 0. the limit of α = 0 therefore exhibits special behavior as for α > 0, probabilityturbulence divergence only scores 0 for exactly matching distributions. c. type contribution ordering for the limit of α=0 in terms of contribution to the divergence score, all exclusive types supply a weight of 1/(n 1 + n 2 ). we can order them by preserving their ordering as α → 0, which amounts to ordering by descending probability in the system in which they appear. and while types that appear in both systems make no contribution to d p 0 (p 1 p 2 ), we can still order them according to the log ratio of their probabilities, eq. (6) . the overall ordering of types by divergence contribution for α=0 is then: (1) exclusive types by descending probability and then (2) types appearing in both systems by descending log ratio. d. limit of α=∞ for probability-turbulence divergence the α → ∞ limit is straightforward and in line with that of rank-turbulence divergence [1] : where the normalization from eq. (5) has become the dominant contributions to probability-turbulence divergence in the α → ∞ limit therefore come from the most common types in each systems, providing they are not equally abundant. we assert that the successful use of our rankand probability-turbulence divergences is best achieved through consideration of rich graphical representations by what we have called allotaxonographs. in this section, we present and describe three sets of allotaxongraphs comparing probability distributions using probabilityturbulence divergence for: • normalized usage frequencies of 2-grams in the first and second halves of jane austen's pride and prejudice [29] for α=3/4, 0, and ∞ (figs. 1, 2, and 3); • normalized usage frequencies of n-grams in all english-identified tweets on 2020/03/12 and 2020/05/30 for n = 1, 2, and 3 and for α = 1/4, 3/4, and ∞ (figs. 4, 5, and 6); • relative abundances of tree species on barro colorado island for five year census concluding in 1985 and 2015 (fig. 7) . the pride and prejudice examples show how ptd may be adjusted to fit well (α=3/4) or poorly (α=0 and ∞). we bin all non-zero probability pairs (log 10 pτ,1, log 10 pτ,2) in logarithmic space. colors indicate counts of 2-grams per cell, and we highlight example 2-grams along the edges of the histogram. for pairs where one of the probabilities is zero, we add a separate rectangular panel along the bottom of each axis (lighter gray and lighter blue). contour lines indicate where probability-turbulence divergence is constant (the jump to the zero probability region necessitates a break in smoothness). based on the histogram, we choose α=3/4 to engineer an approximate fit to the histogram's periphery. the gray scale for 2-grams is indexed by their percentage contribution to probability-turbulence divergence, δd p 3/4,τ , showing a mixture of rare and common 2-grams. ranked list on the right: we order the most salient 2-grams according to their overall contribution δd p 3/4,τ which we mark by bar length. we show the rank pair for each 2-gram in light gray opposite each 2-gram. corresponding flipbook: flipbooks s1, s2, and s3 in the paper's online appendices (compstorylab.org/allotaxonometry/), show how the instrument changes for the same comparison with α being tuned from 0 to ∞ for 1-, 2-, and 3-grams. see ref. [1] for a general introduction and motivation for allotaxonometry and allotaxonographs in the context of rank-turbulence divergence. the examples for 2-grams and 3-grams can also be seen as demonstrations of possible comparisons of features of complex networks and systems (e.g, 2-grams in text as directed edges). as for rank-turbulence divergence [1] but with some key modifications, our allotaxonographs for probabilityturbulence divergence pair two complimentary visualizations: a map-like histogram and a ranked list. in isolation, both the histogram and the ranked list have important but limited descriptive power. the histogram helps us see how well our choice of α performs, information that is entirely lost by the ranking process. and the ranked list would be difficult to intuit from the histogram alone. many aspects of our allotaxonographs are configurable. on gitlab, we provide our universal code for generating allotaxonographs for rank-turbulence divergence, probability-turbulence divergence, and other probability divergences (see sec. v b). in the paper's online appendices (compstorylab.org/allotaxonometry/), we complement all of our allotaxonographs with pdf flipbooks which move systematically through a range of α values. compare with the good fit afforded by α=3/4 for the allotaxonograph in fig. 1 . the contour lines for α=0 do not conform well to the histogram. at this extreme of the parameter's range, probability-turbulence divergence elevates exclusive types above all types that appear in both systems, and the ranked list on the right comprises only system-exclusive 2-grams. per sec. ii b and eq. (8), exclusive types each equally contribute 1 (n 1 +n 2 ) to d p 0 while types appearing in both systems have zero weight. the ordering of 2-grams is determined by maintaining their contribution order as α approaches 0. we force the contour lines in the main body of the histogram to remain equally spaced, even as they all represent 0 in the α → 0 limit. see sec. iv for the connection between d p 0 and the sørensen-dice coefficient [16, 17, 25] and the f1 score [18, 26] . see also flipbooks s1, s2, and s3 in the paper's online appendices (compstorylab.org/allotaxonometry/). for a primary, familiar example to help us explain our probability-turbulence divergence allotaxonographs, we compare the normalized usage frequency distributions of 2-gram usage between the first and second halves of pride and prejudice [29] . we note that we are mostly intent here on showing how allotaxonographs function. we are not attempting to reveal astonishing insights into one of the most well regarded and well studied novels of all time. in fig. 1 , we show an allotaxonograph with α=3/4 which we will contend below provides a good fit. first, the histogram on the left bins all pairs (log 10 p τ,1 , log 10 p τ,2 ). the form we see here is typical of comparisons between systems with heavy-tailed zipf distributions. we rotate the axes so as not to privilege one system over the other, as this might lead to a false sense of an independent-dependent variable relationship [1, 30] . we indicate counts per cell using the perceptually uniform colormap magma [31] . because of the logarithmic scale, the cells start to separate for lower values of probability, corresponding to counts of 0, 1, 2, and so on. in general, types that are common in both systems will be located towards the top of histogram, those that are in both will be at the bottom, and those appearing more prevalently in one system will appear further away from the vertical midline. exactly how much this latter category matters is a function of the divergence at hand. the most extreme cells can be readily understood. the bottommost pair of cells represent all 2-grams that appear once in one half of pride and prejudice and zero the contour lines show constant values of δd p 3/4,τ . we provide a key for the contour lines in the upper right with the histogram removed. as a guide, the gray-scale for the annotations varies with each 2-gram's contribution to the overall divergence score, with darker meaning higher contribution. for α=3/4, 'miss bingley' stands out in particular, while 'irretrievable that' on the left is backgrounded. for all of our allotaxonographs, we place 10 contour lines on each half of the histogram's diamond. these contour lines are evenly spaced not by height but are rather anchored to the bottom axes of the main histogram where they are evenly spaced in logarithmic space. while it may appear that we have omitted annotations internal to the histogram for convenient purposes of visualizing the histogram more cleanly, our annotations are intentional. because individual 2-grams internal to the histogram will never dominate standard divergences, highlighting them would be badly misleading [14, 32] . for our allotaxonographs, the annotations along the bottom of the histogram potentially fall into this trap: 'irretrievable that' and 'were during', each appearing once overall, are just two examples of tens of thousands of such 2-gram hapax legomena. such types may matter in aggregate but not individually. now, our allotaxonographs for probability-turbulence divergence must depart from those of rank-turbulence divergence because we have to accommodate instances of log 10 p when p = 0. for ranks, types with 0 counts in one system-exclusive types-are assigned a tied rank for last place, necessarily a finite number. here, on a logarithmic scale our exclusive types would have to be located on one axis at log 10 p = −∞. we end the main histogram's domain for the lower value of log 10 p τ,i such that log 10 p τ,i > 0. we then add lighter colored regions to the bottom of both sides of the histogram, and locate log 10 p τ,i = 0 along their midlines. the transition is a discrete jump (we do not smoothly interpolate), and we connect the contour lines with a dotted line. as can be seen in fig. 1 , the jump is increasingly clear for contour lines for lower values of δd p 3/4,τ , nearer the histogram's vertical midline. the last piece for the histogram is the list of balances at the bottom right. these summary quantities are intended to be both informative and diagnostic, and they have important if subtle differences. the first bars show the balance of total 2-gram counts which for our example of pride and prejudice is 50/50 by construction. the second and third balances refer to sizes of lexicons, and these are well balanced too. if we create a lexicon of all 2-grams for pride and prejudice, about 58.3% of them appear in the first half and 58.4% in the second. if we instead create separate lexicons of 2-grams for the two halves of pride and prejudice, the third line of the balances records the percentage of 2-grams that are exclusive to each half. while it could be said that we are ultimately creating a simple 2-d histogram for a joint probability distribution with heavy tails, to our knowledge, there have been relatively few other attempts to do so [14, 32] . as we have described them, we believe our histograms are crafted with a number of special details that make them well suited to their task. the ranked list on the right maps the two dimensions of the histogram onto an ordered single dimension of divergence contributions, largest first. the left-right arrangement is solely done to be consistent with the histogramall contributions are positive. the light gray numbers opposite each 2-gram (e.g., 430 31 for 'miss bingley') indicate the 2-gram's zipf rank in the first and second fig. 5. allotaxonograph using probability-turbulence divergence to compare normalized 2-gram usage ranks on two days of english-language twitter, 2020/03/12 and 2020/05/30. details are the same as for fig. 1 and 4 . we see that the comparison of 2-gram distributions produces different, broader histogram that that formed by 1-gram distributions (fig. 4) . we choose α=3/4 to provide a balance of 2-grams across five orders of magnitude for non-zero probability. in contrast to the 1-gram version, the top 2-grams are more evenly distributed on both sides of the list. while some 2-grams are function words combined with the 1-grams we saw in fig. 4 , meaningful 2-grams also appear ('tom hanks','toilet paper', 'george floyd', and 'police brutality'). see flipbook 5 at the paper's online appendices (compstorylab.org/allotaxonometry/) for the instrument's variation as a function of α. half of pride and prejudice (and in general, ω (1) and ω (2) ). we see dominant contributions from character names and references to characters (first half: 'her uncle') functional 2-grams (first half: 'she had', second half: 'in the'), and non-specific references to places and people (second half: 'the room', 'young ladies', 'young man'); in the ranked list, we add open triangles to types if they are exclusive to one system, corresponding to those appearing in the zero probability expansions of the histogram. for example, 'to brighton' appears only in the first half of pride and prejudice, and 'the parsonage' only in the second. finally, we see that the choice of α=3/4 generates a list with 2-grams from across the rare-to-common spectrum. the balanced darker shadings of annotations in the histogram add further support. in reducing such a high dimensional categorical space-where each unique type represents a dimension-we have first collapsed the data to a 2-d histogram, and then to a 1-d list. being able to find the shape in the histogram to which can apply an instance of probabilityturbulence divergence gives us some suggestive proof in the pudding. we see in both allotaxonographs that the contour lines do not match well with the edges of the histogram, in contrast to those realized by the choice of α=3/4. we also see how α=0 favors exclusive 2-grams (i.e., those that do not appear in either the first or second half of the novel), while α=∞ privileges 2-grams that are common 6 . allotaxonograph using probability-turbulence divergence to compare 3-gram usage ranks on two days of english-language twitter, 2020/03/12 and 2020/05/30. details are the same as for fig. 1 and 4 . the histogram has broadened even further out from the 2-gram, and now is well suited to probability-turbulence divergence with the extreme of α=∞, d p ∞ . fragmentary and meaningful 3-grams appear alongside each other, including 'world health organization' and 'black lives matter'. social amplification is also apparent as 3-grams for highly retweeted tweets dominate the rank list. see flipbook 6 at the paper's online appendices (compstorylab.org/allotaxonometry/) for the instrument's variation as a function of α. in one or both halves. as we showed in sec. ii b, when α=0, the divergence contribution for all types that appear in both systems is δd p 0,τ = 0, while for all exclusive types, δd p 0,τ = 1 (n1+n2) (as reflected in the equal bars in the ranked list). thus, the vertical contour lines in fig. 2 , which again are present because we anchor them at evenly spaced locations along the bottom of the main histogram, all correspond to a divergence of δd p 0,τ =0. the dashed parts of the visible contour lines then collapse to the bottom zero point, showing how the exclusive types provide the only non-zero contributions to δd p 0,τ . finally, in flipbooks s1, s2, and s3 in the paper's online appendices (compstorylab.org/allotaxonometry/), we give the reader a view into how our allotaxonometric comparisons of the usage frequencies of 1-grams, 2-grams, and 3-grams in the two halves of pride and prejudice behave as a function of α. all of the flipbooks are especially informative in showing how contour lines and ranked lists change with α. for our second set of allotaxonographs, we compare two key dates of two major events through the lens of english-speaking twitter: 2020/03/12, the date that covid-19 became the major story in the united states, and 2020/05/30, four days after the murder of george floyd in minneapolis, minnesota by police officer derek chauvin. we compare day-scale normalized usage frequency distributions for 1-, 2-, and 3-grams for these two dates in figs. 4, 5, and 6. we choose 2020/03/12 as a key date for the covid-19 pandemic for several reasons. first and primarily, the world health organization (who) officially declared the covid-19 outbreak to be a pandemic on 2020/03/11, a decision that was amplified immediately online but discussion of which most strongly appeared in the news and on twitter on the following day. the date of 2020/03/11 also saw a confluence of three major events that jolted the united states and dramatically elevated the story of the pandemic, all occurring tightly around a 15 minute period between 9 and 10 pm edt (2 am to 3 am utc). first, the national basketball association (nba) abruptly suspended its season. the central event was the abandoning of a game just before tipoff between the utah jazz and oklahoma thunder, upon the league learning that rudy gobert, a center for the utah jazz, had tested positive for covid-19. other players would test positive in the coming days and weeks, as would staff for teams and members of the media. just a few days earlier, gobert had joked with the media about his perception of institutional overreaction to the coronavirus, by touching microphones at an interview. second, tom hanks announced that both he and his wife rita wilson had tested positive for covid-19 while hanks was working on a baz lurhmann film in australia. hanks was at the time the most high profile figure known to have contracted covid-19. third, president donald trump gave an oval office address, the second of his presidency, "on the coronavirus pandemic." the address marked a strong shift in trump's rhetoric regarding the danger of the covid-19 outbreak. the main decision announced was the ban of travel from europe to the us for 30 days, which was needed to be clarified later to not also mean a ban on trade. futures on us stock market dropped during the speech. combined, these disparate events were a major part of the covid-19 pandemic becoming the dominant story for what would become weeks and then months ahead. the murder of george floyd on 2020/05/25, memorial day in the us, precipitated black lives matter protests and civilian-police confrontations in minneapolis. the protests would grow over the following weeks, and begin to spread around the world. and, at least in the first week, george floyd's murder overtook coronavirus as the dominant story in the us [33] . with the above context in mind, we can sensibly examine the allotaxonographs of figs. 4, 5, and 6 our primary observation is that the three histograms vary considerably as we move through 1-, 2-, and 3grams. the histograms broaden with increasing n, with the 3-gram histogram losing a scaling form and squaring up in the axes. the rapidly growing combinatoric possibilities of n-grams with increasing n means that we see more and more exclusive n-grams as we look across the three allotaxonographs. for 1-grams, around 60% of each date's lexicon are exclusive, for 2-grams, the percentage increase to around 70%, and 3-grams we reach 80% (see the bottom of the three balance summaries in each allotaxonograph). the maximum counts per cell is 10 6 for 1-grams, is 10 7 for 2-grams, and 10 8 for 3-grams. the cells with the most n-grams are of course the the hapax legeomenathe bottommost two cells in the histogram-those n-grams which appear once on one of the dates and not at all on the other. to obtain good balance for the most dominant ngrams, we select α=1/4, 3/4, and ∞. different kinds of terms dominate depending on n with 'coronavirus', 'the coronavirus', and 'tested positive for' leading on 2020/03/12, and 'minneapolis' 'george floyd' and 'of george floyd' at the top on 2020/05/30. because social amplification is encoded in twitter's data stream through retweets, dominant 2-grams and especially 3-grams are liable to belong to the most retweeted messages of the day, and may lead to some variation in the dominant n-grams. (by contrast, we do not have a measure of popularity of individuals phrases or sentences within pride and prejudice with just the bare text.) for example, 'toilet paper' and 'world health organization' appear as dominant 2-grams and 3-grams but none of their five distinct 1-grams are near the top of the ranked list in fig. 4 . on the other hand, some dominant 1-grams may be used in diverse 2-grams and 3-grams and thus may not appear in the ranked lists for 2-grams and 3-grams. examples from fig. 4 are 'antifa' and 'breonna'. for all three n-gram comparisons of these two dates on twitter, we provide flipbooks 4, 5, and 6 at the paper's online appendices (compstorylab.org/allotaxonometry/). readers may use these to easily explore how the choice of α affects the fit for the contour lines in the histogram and the ordering of which n-grams dominate probability-turbulence divergence. we include one final allotaxonograph from an entirely different field of research, ecology. in fig. 7 we show a probability-turbulence divergence allotaxonograph for tree species abundance in barro colorado island for censuses completed in 1985 and 2015. this example also shows how allotaxonographs can be used to inspect how well divergence measures perform for data sets that are much smaller than our examples from literature and twitter. the species that dominates the overall divergence score is one that has diminished in abundance, piper cordulatum [34] [35] [36] [37] . in ref. [1] , we compared these distributions with rank-turbulence divergence, and the overall orderings of dominant species are broadly consistent. in flipbook 7 at the paper's online appendices (compstorylab.org/allotaxonometry/), we show how the dominant contributions of species vary as a function of α. allotaxonograph using probability-turbulence divergence to compare tropical forest tree species abundance on panama's barro colorado island (bci) for 5 year censuses completed in 1985 and 2015 [19] . the choice of α=5/12 produces a set of dominant species reasonably well balanced across the abundance spectrum. see ref. [1] for the corresponding rank-turbulence divergence allotaxonographs. see flipbook 7 in the supplementary information for the instrument's variation as a function of α. a. links to existing probability-based divergences probability-turbulence divergence shares some characteristics with other divergences (see refs. [11] and [12] for two example compendia). in particular, we find known distances and similarities which correspond with or function similarly to probability-turbulence divergence for α=0, 1/2, 1, and ∞. for α=0, probability-turbulence divergence partners the similarity measure sørensen-dice coefficient, s sd (p 1 p 2 ) [16, 17, 25] , which was independently developed in the context of ecology by dice (1945) and sørensen (1948) (see also ref. [38] ). for two systems, the sørensen-dice coefficient is the number of shared types relative to the mean of the number of types in each system. using our notation, and referring back to eq. (8), we have: where we are again summing over the union of types r 1,2;0 . the quantity 1 − δ pτ,1,0 − δ pτ,2,0 is 1 when a type appears in both systems and 0 otherwise. the sørensen-dice coefficient has arisen in many settings, with different names. for example, in statistics, the sørensen-dice coefficient is the f 1 score of a test's accuracy [18, 26] . examples of divergences matching the internal structure of d p 1/2 include the hellinger [39] , mautusita distance [40] , and squared-chord distance [12] . in terms of the probability-turbulence divergence's internal structure of |[ p τ,1 ] α −[ p τ,2 ] α |, a large selection of divergences match up with the the α=1 instance. these include l (p) -norm type constructions of the form: while the overall divergence values for these various divergences will differ, the rank orderings of the contributing types will be identical to that of d p 1 . finally, in the α=∞ limit, d p ∞ agrees, up to a normalization factor of 2, with the motyka distance [11] . while none of these other divergences provide direct tunability of the type probability-a severe limitation, as we hope our examples have conveyed-there are well established quantities which do. as we observed for rank-turbulence divergence in [1] , the parameter α's effect is similar to its counterparts in various kinds of generalized entropy [20] [21] [22] and, more directly, the diversity indices (or hill numbers) from ecology [23, 24] . rényi entropy, α h, and the associated diversity index, α n , are defined as: where α ≥ 0. we acknowledge that, at the risk of a minor dislocation from relevant literature, we have had to confront some notation peril here as a standard notation for the diversity index is α d. we have also already used n in our present paper but this choice tracks sensibly: as α → 0, we retrieve the natural logarithm of the number of distinct types n (species richness in ecology) for rényi entropy, and therefore the diversity index is 0 n = n . as α → ∞, the most abundant type will dominate, with min-entropy the limit: ∞ n = min τ 1/p τ = 1/max τ p τ . in the α → 1 limit, we recover shannon's entropy, h, as well as 1 n = e h1 = e h . there are similar aspects for probability-turbulence divergence and the diversity index in the limits of α=0 and ∞. for α=0, for example, both reduce to quantities involving simple counts of distinct types. nevertheless, we note that we cannot construct probability-turbulence divergence from manipulations of rényi entropy or the diversity index. we can, roughly speaking, only create a difference of sums whereas we need a sum of absolute differences with suitable exponents. pride and prejudice: we sourced a plain text version of jane austen's pride and prejudice from project gutenberg (http://www.gutenberg.org/ebooks/1342). normalized n-gram usage frequency on twitter: we collected around 10% of all tweets sent on these dates based on coordinated universal time (utc) meaning they covered 4:00:00 am to 3:59:59 am eastern daylight time (edt) and 7:00:00 am to 6:59:59 am pacific daylight time (pdt). for the eastern and central time zone's in the united states, especially, this shift provides a better, more functional coverage of people's activity. we provide historical access to the top 10 6 1-grams, 2-grams, and 3-grams across more than 100 languages as part of our storywrangler for twitter project [28, 41] . species abundance on barro colorado island: we accessed the dataset for bci censuses performed roughly every 5 years over 35 years through the online repository described in ref. [19] . all scripts and documentation reside on gitlab: https://gitlab.com/compstorylab/allotaxonometer. for the present paper, we wrote the scripts to generate the allotaxonographs in matlab (laboratory of the matrix). we produced all figures and flipbooks using matlab version r2020a. we welcome ports to other languages. as is, the core script is highly configurable and can be used to create a range of allotaxonographs as well as simple unlabeled rank-rank and probabilityprobability histograms. instruments accommodated by the script include rank-turbulence divergence [1] , probability-turbulence divergence, and generalized symmetric entropy divergence which includes jensen-shannon divergence as a special case. we have defined, analyzed, and demonstrated the use of probability-turbulence divergence as an instrument of allotaxonometry. as the probability-based analog of our rank-turbulence divergence, the instrument is able to perform well when comparing heavy-tailed zipf distributions of type frequencies. we have shown further that probability-turbulence divergence generalizes a range of existing probability-based divergences, either in matching in exact form or equating in how types are ordered by type contribution. while we view rank-turbulence divergence as our most general, interpretable instrument, for systems in which probabilities (or rates) of types occurring are well defined, and the resulting distributions involved are heavy-tailed, probability-turbulence divergence provides a more nuanced instrument. we also favor divergences which compare distributions in as transparent a way as possible. to that end, we have made the core of probability-turbulence divergence a simple difference of powers of probabilities (eq. (3)). by contrast, we view some divergences as being problematic in being overly constructed. we venture that jensen-shannon divergence (jsd), which we ourselves have used elsewhere, is one such instrument. the creation of an artificial mixed distribution is a contrivance we avoid here, and is perhaps indicative of taking information theory too far [42, 43] . in our experience, we have also found that the visual information delivered by our allotaxonographs, especially in their coupling of histograms and ranked lists, has been essential to working effectively with divergences of all kinds. one caution we make is that in the examples we have explored in the present paper, we have taken distributions as they are. that is, we have not contended with issues of sub-sampling and missing tail data [44] . we can say that types appearing with high rate (e.g., common n-grams on twitter) will not be affected by accessing more data, as they are well estimated rates. in our paper on rank-turbulence divergence, we examined how truncation of distributions affects allotaxonographs, and such an approach is always available for any divergence. finally, in our present paper and in ref. [1] , we have so far made choices of α based on inspection of the relevant histogram. a clear next step is to find ways to determine an optimal α for any given pair of distributions, and to do so only when sufficiently robust scaling is apparent. from a storytelling perspective, we are concerned with finding an α that returns a ranked list of distinguishing types for two distributions such that the list comprises a balance of types from across the full range of observed probabilities [45] . we have performed some preliminary work for such an optimization, and note here that simple regression is made difficult by the overwhelming weight of rare types relative to common ones. allotaxonometry and rank-turbulence divergence: a universal instrument for comparing complex systems on a class of skew distribution functions power laws, pareto distributions and zipf's law powerlaw distributions in empirical data emergence of scaling in random networks complexity: a guided tour, complexity growth, 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flora of barro colorado island, panama phenology of neotropical pepper plants (piperaceae) and their association with their main dispersers, two short-tailed fruit bats, carollia perspicillata and c. castanea (phyllostomidae) hierarchical fruit selection by neotropical leaf-nosed bats (chiroptera: phyllostomidae) stigler's law of eponymy neue begründung der theorie quadratischer formen von unendlichvielen veränderlichen decision rules, based on the distance, for problems of fit, two samples, and estimation (2020), storywrangling.org the bandwagon on the limitations of jensen-shannon divergence and its generalizations: allotaxonographs and critique robust estimation of microbial diversity in theory and in practice text mixing shapes the anatomy of rank-frequency distributions the authors are grateful for the computing resources provided by the vermont advanced computing core which was supported in part by nsf award no. oac-1827314, financial support from the massachusetts mutual life insurance company and google open source under the open-source complex ecosystems and networks (ocean) project. key: cord-269734-u43gt8fh authors: teijaro, j.r. title: pleiotropic roles of type 1 interferons in antiviral immune responses date: 2016-09-20 journal: adv immunol doi: 10.1016/bs.ai.2016.08.001 sha: doc_id: 269734 cord_uid: u43gt8fh since isaac's and lindenmann's seminal experiments over 50 years ago demonstrating a soluble factor generated from heat killed virus-stimulated chicken embryos could inhibit live influenza virus replication, the term interferon has been synonymous with inhibition of virus replication. while the antiviral properties of type 1 interferon (ifn-i) are undeniable, recent studies have reported expanding and somewhat unexpected roles of ifn-i signaling during both acute and persistent viral infections. ifn-i signaling can promote morbidity and mortality through induction of aberrant inflammatory responses and recruitment of inflammatory innate immune cell populations during acute respiratory viral infections. during persistent viral infection, ifn-i signaling promotes containment of early viral replication/dissemination, however, also initiates and maintains immune suppression, lymphoid tissue disorganization, and cd4 t cell dysfunction through modulation of multiple immune cell populations. finally, new data are emerging illuminating how specific ifn-i species regulate immune pathology and suppression during acute and persistent viral infections, respectively. systematic characterization of the cellular populations that produce ifn-i, how the timing of ifn-i induction and intricacies of subtype specific ifn-i signaling promote pathology or immune suppression during acute and persistent viral infections should inform the development of treatments and modalities to control viral associated pathologies. many viruses harbor viral proteins with specific functions geared toward preventing ifn-i production and/or signaling, highlighting the evolutionary selective pressure exerted by ifn-i during viral replication (devasthanam, 2014) . the absence of ifn-i signaling during acute virus infection in vivo increases virus replication, dissemination, and lethality during multiple viral infections in animal models. global deletion of ifnar1 results in enhanced mortality during vesicular stomatitis virus (vsv), vaccinia virus (vv), west nile virus (wnv), and lymphocytic choriomeningitis virus (lcmv) infections (muller et al., 1994) . moreover, infection of ifnar1 ko mice with acute lcmv armstrong (arm) (nakayama et al., 2010; zhou, cerny, fitzgerald, kurt-jones, & finberg, 2012) and treatment of arm-infected mice with an ifnar1 neutralizing antibody elevated viral loads and promoted virus persistence (teijaro et al., 2013; wilson et al., 2013) . dendritic cell-specific deletion of ifnar1 results in elevated virus replication and systemic persistence of the cw3 strain of murine norovirus (mnov) despite increased cell-mediated and humoral adaptive immune responses (nice et al., 2016) . ifn-i signaling has been shown to be essential for controlling wnv infection and restricting viral pathogenesis (sheehan, lazear, diamond, & schreiber, 2015) . mice deficient in ifnar1 signaling display increased susceptibility to wnv infection (pinto et al., 2014; samuel & diamond, 2005) . during infection with the coronavirus, mouse hepatitis virus (mhv-a59), the magnitude of the ifn-i and -ii responses directly correlated with viral loads (raaben, koerkamp, rottier, & de haan, 2009 ). moreover, ifn-i produced by plasmacytoid dendritic cells (pdcs) was essential to control virus replication and prevent mortality following mhv-a59 infection in mice (cervantes-barragan et al., 2007) . during experimental infection of mice and nonhuman primates with the lassa hemorrhagic fever virus, delayed or reduced induction of ifn-i and downstream gene signatures correlated with high viral loads and fatal outcome (baize et al., 2009; yun et al., 2012) . deletion of ifn-i related signaling pathways during respiratory virus infections in animal models results in diverse effects depending on the virus strain and genetic background (durbin et al., 2000; price, gaszewska-mastarlarz, & moskophidis, 2000) . in the context of respiratory viral infection, genetic deletion of stat1 reduced virus control, enhanced pathology, and mortality during sars-cov and influenza virus infection (durbin et al., 2000; frieman et al., 2010) . interestingly, stat1-deficient animals were highly susceptible to influenza virus infection, displaying elevated viral titers and increased pathology compared to stat1-sufficient mice. studies in mouse models of influenza virus have revealed conflicting evidence for the role of ifnar1 in controlling influenza virus replication, morbidity, and mortality. infection of ifnar1 à/à mice with the pr8 strain of influenza virus resulted in altered recruitment of ly6c hi vs ly6c int monocytes in the lung, translating into increased production of the neutrophil chemoattractant, kc (cxcl8), elevated numbers of neutrophils in the lung and increased morbidity and mortality (seo et al., 2011) . therefore, modulation of type 1 interferon signaling and production needs to be balanced to have enough to control virus infection but not promote excessive inflammation. the discrepancy between influenza pathogenicity in ifnar1 and stat1-deficient mice was later clarified when animals lacking both ifnar1/ifn-λ were unable to control influenza virus replication. this is further supported in humans where null mutations in the human interferon regulatory factor-7 gene results in reduced ifn-i and -iii production from myeloid dcs and pdcs and life-threatening seasonal influenza virus infection (ciancanelli et al., 2015) . exposure of bone marrow cells to ifn-i prior to their recruitment to lung endows these cells with an antiviral program that protects from virus infection after entry into the infected lung (hermesh, moltedo, moran, & lopez, 2010) . deletion of the ifn-β or ifnar1 genes in mice with a functional mx1 gene increased virus replication and reduced the ld 50 20-fold (koerner, kochs, kalinke, weiss, & staeheli, 2007) . infection of ifnar1-deficient mice with low dose mouse adapted h1n1 influenza viruses resulted in mortality, elevated viral loads, exacerbated lung pathology, and reduced numbers of il-10-producing cells as compared to ifnar1-sufficient controls (arimori et al., 2013) . moreover, exogenous administration of il-10 to ifnar1-deficient animals following influenza virus infection partially restored survival and ameliorated lung pathology. thus, ifn-i can be protective during influenza virus infection either through suppressing virus spread or prompting induction of immune-suppressive cytokines to reign in excessive inflammation. in addition to directly inhibiting virus propagation, ifn-i also has potent immune stimulatory functions which support the resolution of virus infection. ifn-i promotes upregulation of mhc-i expression in multiple cell lineages (lindahl, gresser, leary, & tovey, 1976a , 1976b , which is required for optimal t cell stimulation, differentiation, expansion, and killing of virus-infected cells. autocrine signaling of ifn-i on dendritic cells promotes their activation and t cell stimulatory capacity (montoya et al., 2002) . ifn-i signaling during virus infection promotes conversion of pdcs into myeloid derived dcs and impairs hematopoietic differentiation of bone marrow progenitors into dcs (sevilla, mcgavern, teng, kunz, & oldstone, 2004; zuniga, mcgavern, pruneda-paz, teng, & oldstone, 2004) . following exposure to ifn-i, metallophilic macrophages induce expression of the usp18 protein which prevents jak1 phosphorylation and inhibits ifn-i signaling in these cells. in turn, repression of ifn-i signaling allows for restricted virus replication in these macrophages, promoting the production of viral antigens which are recognized by b cells, the final result is the facilitation of antiviral antibody generation and enhanced virus control (honke et al., 2012) . ifn-i also exerts potent costimulatory effects directly on cd8 t cells, enhancing cd8 t cell proliferation upon ifnar1 signaling (curtsinger, valenzuela, agarwal, lins, & mescher, 2005; kolumam, thomas, thompson, sprent, & murali-krishna, 2005) . the timing of cd8 t cell exposure to ifn-i significantly influences the differentiation and magnitude of the response (welsh, bahl, marshall, & urban, 2012) . exposure of naïve cd8 t cells to apc and ifn-i prior to antigenic stimulation promotes the maintenance of a naïve phenotype with reduced proliferation despite production of effector cytokines. direct ifn-i signaling on naïve and memory t cells promotes rapid apoptosis, inhibits proliferation, and promotes early effector differentiation of memory cells upon exposure. blockade of ifn-i signaling during wnv infection has significant effects on t cell expansion, cytokine production, and differentiation when administered during the maturation phase of the t cell response, however, had no effect when given prior to infection (pinto et al., 2011) . moreover, low dose priming with the vv ankara strain had little effect on effector or memory t cell recall in ifnar1 à/à mice (volz, langenmayer, jany, kalinke, & sutter, 2014) . in addition to t cells, ifn-i signaling is known to be important for nk cell function. ifn-i signaling promotes nk cell cytolytic capacity and survival during acute viral infection (hwang et al., 2012; martinez, huang, & yang, 2008; nguyen et al., 2002) and was recently reported to protect antiviral cd8 t cells from nk cell lytic effects (crouse et al., 2014; xu et al., 2014) . reconstitution of ifnar1 à/à mice with ifnar1 +/+ nk cells restored early control of vv infection in vivo (martinez et al., 2008) , suggesting that nk cell intrinsic ifnar1 signaling is important for early control of vv replication. moreover, direct ifn-i signaling on nk cells was required to induce nk cell ifn-γ production during acute lcmv infection. early ifn-γr signaling was required for promoting initial virus control in the peritoneum (mack, kallal, demers, & biron, 2011) , suggesting that ifn-i signaling directly on nk cells promotes virus control during acute lcmv infection. ifn-i signaling during viral infection can also signal to regulatory t cells and subsequently alter their suppressive functions. it was recently demonstrated that ifnar1 signaling on foxp3 + tregs limits their suppressive function during acute lcmv infection, thus promoting virus control (srivastava, koch, pepper, & campbell, 2014) . deletion of ifnar1 on foxp3 + cells blunted virus-specific t cell responses and elevated virus loads. thus, ifn-i signaling on suppressive t cell populations temporarily suspends suppressive function and allows for optimal antiviral t cell responses during an ongoing viral infection. similar to effects on t cells, ifn-i signaling has both positive (le bon et al., 2001) and negative effects on antiviral b cell responses. the survival and maturation of immature b cells can be inhibited by ifn-i signaling (lin, dong, & cooper, 1998) . in contrast to immature b cells, ifn-i signaling promotes b cell activation, antibody production, and isotype switch following influenza, vsv, and wnv infection (coro, chang, & baumgarth, 2006; fink et al., 2006; purtha, chachu, virgin, & diamond, 2008; rau, dieter, luo, priest, & baumgarth, 2009 ). however, it was also reported that influenza virus-specific antibody levels were elevated at later time points following influenza virus challenge in ifnar1-deficient mice compared to ifnar1-sufficient controls (price et al., 2000) . during acute lcmv infection, blockade of ifn-i signaling in both wild-type and stat3-deficient mice enhanced t follicular helper cell (t fh ), germinal center b cell differentiation, and anti-lcmv antibody responses (ray et al., 2014) . elevated antibody responses during acute viral infections following ifnar1 blockade suggest that, in certain circumstances, ifn-i signaling can restrain optimal antiviral antibody responses. the correlation of an aggressive immune response and severe disease following influenza virus infection in humans and animal models has been discussed previously (la gruta, kedzierska, stambas, & doherty, 2007 ). an aggressive innate response, with elevated recruitment of inflammatory leukocytes to lung, likely contributed to the morbidity of the 1918 influenza infection (ahmed, oldstone, & palese, 2007; kobasa et al., 2007) . in fact, lung injury during infection of macaques with the 1918 h1n1 influenza virus strain directly correlated with early dysregulated inflammatory gene expression, including elevated ifn-i signatures (cilloniz et al., 2009; kobasa et al., 2007) . more recently, clinical studies on avian h5n1-infected humans documented a significant association between excessive early cytokine responses and immune cell recruitment as predictive of poor outcome (de jong et al., 2006 ). an aberrant cytokine/chemokine response was observed in patients with severe disease during the most recent h1n1 pandemic in 2009 (arankalle et al., 2010) . type i interferon signaling is well known to inhibit influenza virus replication and spread (garcia-sastre & biron, 2006) . the production of the ns1 protein, one of 11 viral proteins, acts to inhibit type 1 interferon production and signaling (hale, randall, ortin, & jackson, 2008) , suggesting that ifn-i signaling exerts substantial selection pressure on virus fitness. deletion or mutation of the ns1 gene results in significant increases in the levels of type 1 interferon in infected cells and significantly lower virus titers both in vitro and in vivo (garcia-sastre, egorov, et al., 1998; jiao et al., 2008; kochs, garcia-sastre, & martinez-sobrido, 2007) . despite strong evidence demonstrating extensive antiviral properties of ifn-i, several studies also suggest pathogenic roles for ifn-α during influenza virus infection. the production of several proinflammatory cytokines and chemokines is known to be amplified by ifn-i receptor signaling. in addition to protective effects of ifn-i signaling, pathogenic roles for ifn-i have been reported during influenza virus infection ( fig. 1a) . appearance of ifn-α in lavage fluid directly coincides with symptom onset during human experimental influenza virus infection (hayden et al., 1998) , suggesting that ifn-i signaling and pathological responses in humans temporally coincide. recently, it was paradoxically reported that deletion of ifnar1 or depletion of pdcs in svev129 mice inhibited pulmonary pathology and improved survival following lethal influenza virus challenge (davidson, crotta, mccabe, & wack, 2014) . reduced immune pathology and enhanced survival in mice deficient in ifn-i signaling transpired without significant increases in viral loads or impediment of eventual viral clearance (fig. 1b) . in contrast to deletion of ifn-i signaling, treatment of influenza virus-infected mice with ifnα resulted in enhanced morbidity and mortality; thus, ifn-i can promote pathological consequences during acute influenza virus infection. over the past 5 years, we identified that therapeutic administration of sphingosine 1 phosphate (s1p) analogs early during influenza virus infection in mice resulted in reduced morbidity and mortality . s1p is a lipid metabolite converted from ceramide precursors to sphingosine. fig. 1 ifn-i signaling enhances cytokine/chemokine amplification, innate immune cell recruitment, and immune pathology during respiratory viral infections. (a) viral infection in the lung with influenza or sars-cov promotes the induction of delayed ifn-i production which enhances cytokine/chemokine production, recruitment of nk cells, and neutrophils and inflammatory macrophage/monocytes all which contribute to lung immune-mediated pathology. (b) blockade or genetic deletion of ifnar1 blunts cytokine/chemokine amplification, inhibits recruitment of nk cells, neutrophils, and inflammatory macrophages/monocytes resulting in reduced immunopathology, and improved survival. treatment of mice with s1p1r agonists early during influenza virus infection suppresses ifn-i amplification from plasmacytoid dendritic cells which lowers ifn-i levels. the end result is blunting of cytokine/chemokine amplification, inhibition of nk cell, neutrophil, and inflammatory macrophage/monocyte recruitment into the lung, reduced immunopathology, and improved survival. the subsequent phosphorylation by sphingosine kinase 1 and 2 produces bioactive s1p in vivo where it acts on s1p-specific g-protein couples receptors (gpcrs) (chalfant & spiegel, 2005) . the levels of bioactive s1p are regulated through the actions of s1p phosphatases and lyases which dephosphorylate and degrade s1p, respectively. highest levels of s1p are found in the blood and lymph with significantly lower levels maintained in peripheral tissues (cyster, 2005) . s1p binds and signals through five gpcrs denoted as s1pr1-5 which couple to various g-protein signaling effectors. the expression of s1p receptors is heterogeneous, being found on both hematopoietic and nonhematopoietic lineages (im, 2010) . the functional coupling to multiple heterotrimeric g-proteins promote the diverse cellular functions associated with s1p receptor signaling. signaling through these five receptors is known to modulate multiple cellular processes including: cell adhesion, migration, survival, proliferation, endocytosis, barrier function, and cytokine production (rivera, proia, & olivera, 2008) . recently, we identified a novel regulatory function of s1pr1 signaling in blunting early cytokine amplification and innate immune cell recruitment following influenza virus infection (fig. 1b) . early administration of a promiscuous s1pr agonist, aal-r, or an s1p1r-selective agonist (cym-5442) significantly blunted production of multiple pro-inflammatory cytokines and chemokines following infection with either wsn or human pandemic h1n1 2009 influenza virus walsh et al., 2011) . further, both aal-r-and cym-5442-mediated reduction of early innate immune cell recruitment and cytokine/chemokine production correlated directly with reduced lung pathology and improved survival during h1n1 2009 influenza virus infection. while these s1pr agonists clearly inhibited innate immune responses, significant inhibition of activated t cell recruitment into the lung at various times post infection occurred in mouse adapted (marsolais et al., 2009 ) and human pathogenic strains of influenza virus . the above findings were extended using genetic and chemical tools to probe functions of the s1p1 receptor (s1p1 gfp knockin transgenic mice, s1p1 receptor agonists and antagonists), revealing that pulmonary endothelial cells modulate innate immune cell recruitment and cytokine/chemokine responses early following influenza virus infection . importantly, s1p1r agonist treatment blunted cytokine/chemokine production and innate immune cell recruitment in the lung independently of endosomal and cytosolic innate sensing pathways (teijaro, walsh, rice, rosen, & oldstone, 2014) . further, s1p1r signaling suppression of cytokine amplification was independent of multiple innate signaling adaptor pathways but required the myd88 adaptor for cytokine amplification following influenza virus challenge. immune cell infiltration and cytokine production were found to be distinct events, both orchestrated by signaling through the s1p1r. suppression of early innate immune responses through s1p1r signaling also reduced mortality during infection with human pathogenic strains (h1n1/2009 swine) of influenza virus in a ferret model, demonstrating that s1pr1-mediated blunting of influenza virus pathogenesis in mice could be extended to a model more closely resembling human disease. the link between s1pr1 and ifn-α amplification following influenza virus infection was striking. in fact, the absence of ifnar1 abolished cytokine amplification and the capacity of s1p1r agonists to further blunt cytokine/chemokine responses (teijaro et al., 2016 . to understand how s1pr1 signaling regulates ifn-α and cytokine amplification, we assessed the pulmonary cell subsets that produce ifn-α and cytokines/chemokines following influenza virus challenge. expression of s1p1r was quickly observed in purified pdcs; moreover, s1p1r agonists suppressed ifn-i induction/amplification from both mouse and human pdcs following influenza virus simulation (teijaro et al., 2016) . further mechanistic studies revealed that s1p1r agonist-mediated suppression was independent of gi/o signaling and required signaling through the s1p1r c-terminus. biochemically, s1p1r agonists accelerated the turnover of ifnar1 and promoted trafficking to lysosomes for degradation, abrogating stat1 phosphorylation, blunting the ifn-i autoamplification loop. the fact that ifn-i production/signaling can down modulate s1pr1 expression/activity indirectly through upregulation of cd69 which promotes internalization of s1pr1 in t cells is significant (shiow, 2006) and suggests that s1p1r and ifn-i signaling are closely linked and capable of counter regulating one another. an additional study also reported ifn-i modulation in pdcs via other s1prs (dillmann et al., 2016) , suggesting that this phenomenon could be more promiscuous than originally thought. similar to influenza virus infection, aberrant innate cytokine/chemokine responses and immune cell recruitment into lungs correlate with disease severity in human patients (huang et al., 2005) . ifn-i signaling during murine sars-cov infection appears to be dispensable for virus control while also potentiating immune pathology. however, the role ifn-i signaling plays in this pathology has only recently been systematically addressed. deletion of ifnar1 in mice does not mirror the enhanced viral loads or pathological consequences observed in stat1 à/à mice in sars-cov infection, suggesting an ifnar1-independent stat-1-dependent pathway is necessary for controlling sars-cov (frieman et al., 2010) . this study provocatively suggests that ifn-i signaling is dispensable for controlling sars-cov replication in vivo. recently, an important study was published where the authors further highlighted the importance of ifn-i signaling in respiratory virus pathology by reporting that delayed ifn-i induction and signaling during sars-cov infection in mice promoted the development and infiltration of inflammatory monocyte-macrophages into the lung, resulting in exacerbated lung pathology and lethal pneumonia (channappanavar et al., 2016) . attenuation of ifn-i signaling either through genetic deletion or through antibody neutralization of ifnar1 prevented inflammatory monocyte-macrophage infiltration into the lung, abrogated lung immune pathology, and resulted in mild clinical disease. importantly, genetic deletion or blockade of ifn-i signaling resulted in control of viral loads similar to control animals, reinforcing that ifn-i signaling is dispensable for control of sars-cov infection in vivo. one possibility is that in the absence of ifn-i signaling, induction of an ifn-iii (ifn-λ) antiviral program may effectively limit viral replication. the results found in this study were strikingly similar to those found in influenza virus-infected svev129 mice and suggest that strategic modulation of ifn-i signaling could ameliorate pathologies associated with severe respiratory virus infection. collectively, the studies above suggest that ifn-i signaling is essential to cytokine and chemokine amplification and innate immune cell recruitment and can promote excessive immunopathology during acute respiratory viral infections (fig. 1) . importantly, that ifn-i production and signaling can be blunted without enhancing virus propagation following acute respiratory viral infection suggests that this pathway can be modulated without compromising host antiviral responses. the correlation between blunting ifn-i signaling, lessened immune pathology, and improved survival during multiple respiratory viral infections highlight the need to mechanistically dissect how ifn-i promotes immune pathology during these infections. the role of ifn-i signaling in restraining chronic/persistent viral infection is well documented. inhibition of ifn-i signaling by antibody blockade of ifnar1 results in elevated virus replication early following lcmv cl13 infection and treatment of mice with ifn-i during the early stages of persistent lcmv infection promotes rapid virus control (wang et al., 2012) . mechanistically, ifn-i therapy increased expansion of virus-specific cd8 t cells and prevented t cell exhaustion; however, whether this was due to ifn-i-mediated immune stimulatory effects, lowering of antigen levels, or both was not systematically addressed. an additional study reported that deletion of the 2 0 -5 0 oligoadenylate synthetase-like 1 gene prior to lcmv cl13 infection facilitated sustained ifn-i production/signaling, promoted t cell expansion, reduced t cell exhaustion, and promoted rapid virus control (lee, park, jeong, kim, & ha, 2013) . similar to persistent lcmv infection, ifn-i administration can exert protective effects through slowing siv replication and disease progression if administered early following infection (sandler et al., 2014) and has shown some efficacy in patients with persistent hiv infection (asmuth et al., 2010; azzoni et al., 2013) . moreover, treatment with pegylated ifn-α in conjunction with the antiviral drug ribavirin was the standard of care for treating patients with chronic hepatitis c virus (hcv) infection until recently (heim, 2013; moreno-otero, 2005) . however, despite success in hcv therapy, the modest efficacy observed following ifn-α administration requires ribavirin and, even in combination, only a slim majority of patients respond. moreover, patients who fail to control hcv following ifn-i therapy were reported to express a higher ifn-i gene signature prior to treatment (sarasin-filipowicz et al., 2008) . similar trends were observed following ifn-i administration during hiv and siv infections, where ifn-i administration had only the modest effects if given during established persistent infection (asmuth et al., 2008; hubbard et al., 2012) . the reasons for the discrepancies observed in human persistent viral infections, where ifn-i therapy can promote control (50-60% of hcv patients) while in others (during established hiv infection) minimal benefit is observed, remain unknown. one could imagine a scenario where in some persistently infected hcv patients, elevated ifn-i signatures persist, and addition of pegylated ifn-α provides minimal benefit while patients with lower ifn-i signatures respond to the therapy. whether treatment with pegylated ifn-α earlier during infection (prior to sustained ifn-i signatures) would be beneficial would be interesting to discern. a similar profile appears to exist in persistent siv infection, where early administration of ifn-i promotes control of viral loads and pathogenesis, while later administration has modest effects on viral titers and disease outcome. during infection with a model gamma herpesvirus, mhv68, the lack of ifn-i signaling exacerbated virus replication, increased reactivation from latency, and resulted in enhanced morbidity and mortality (barton, lutzke, rochford, & virgin, 2005; dutia, allen, dyson, & nash, 1999) . taken together, ifn-i therapy may be beneficial during the early stages of persistent, latent chronic viral infection, or infections with lower ifn-i signatures; however, blocking ifn-i signaling either alone or in conjunction with antiviral or immune checkpoint therapies may prove more effective once virus persistence and elevated ifn-i signatures are established. however, the ultimate outcome will likely depend on the persistent virus studied, genetic susceptibilities of individuals, and subtype and timing of ifn-i species produced; all which require further investigation. moreover, given the undesirable side effects of ifn-i administration, ifn therapy can do as much harm as good during viral infection, highlighting the need for developing alternative approaches to treat persistent viral infections. during persistent viral infections, chronic immune activation, negative immune regulator expression, an elevated interferon signature, and lymphoid tissue destruction correlate with disease progression. elevated ifn-i signatures have been observed during lcmv infection in mice (hahm, trifilo, zuniga, & oldstone, 2005) and hiv and hcv infections in humans and nonhuman primates (bosinger et al., 2009; jacquelin et al., 2009; wieland et al., 2014) . chronic immune activation following hiv infection has been reported, and suppression of this hyperactivated state has been proposed as a potential strategy to alleviate hiv-associated pathologies (boasso, hardy, anderson, dolan, & shearer, 2008; d'ettorre, paiardini, ceccarelli, silvestri, & vullo, 2011) . disease following experimental siv infection in rhesus macaques correlates with elevated ifn-i production and inflammatory signatures (jacquelin et al., 2009; manches & bhardwaj, 2009 ). in contrast, siv infection in sooty mangabeys and african green monkeys, which develop modest pathology despite equivalent viral loads as macaques, correlate with reduced ifn-i and inflammatory gene signatures (bosinger et al., 2009) . similar correlations with respect to reduced immune activation exist in hiv-infected elite controllers, although whether reduced immune activation follows virus control is uncertain (deeks & walker, 2007; saez-cirion et al., 2007) . blockade of pd-1 signaling during chronic siv infection reduces hyperimmune activation and microbial translocation in rhesus macaques and lowers ifn-i signatures in the blood and colon (dyavar shetty et al., 2012) . moreover, an elevated interferon signature is observed in hcv-infected patients despite limited control of virus replication and development of liver pathology (guidotti & chisari, 2006; su et al., 2002; wieland et al., 2014) . in fact, hcv infection in culture blocks isg protein expression through activation of rna-dependent protein kinase (garaigorta & chisari, 2009) , creating a paradoxical ifn-i-dependent viral advantage. thus, ifn-i signaling pathways have the potential to aid viral fitness and promote pathology during persistent viral infection. these studies further highlight the viability of the ifn-i signaling system as a target to promote control of persistent viral infection. while the literature suggests a causative role for ifn-i in contributing to pathogenesis of persistent virus infections, definitive studies assessing how ifn-i neutralization affects the outcome of virus persistence were lacking until recently. two laboratories assessed the role ifn-i signaling plays during persistent infection using the lcmv clone-13 (cl13) strain of virus. during their investigation, they found that blockade of ifn-i signaling using an ifnar1 neutralizing antibody reduced immune system activation, decreased expression of negative immune regulatory molecules il-10 and pd-l1 and restored lymphoid architecture in mice persistently infected with lcmv (fig. 2) . importantly, blockade of ifnar1 both prior to and following established persistent lcmv infection promoted faster virus clearance and required an intact cd4 t cell compartment (teijaro et al., 2013; wilson et al., 2013) . blockade of ifn-i signaling significantly enhanced cd4 t cell differentiation into th1 effectors as well as increased t fh cell differentiation (osokine et al., 2014) . the above studies demonstrate for the first time a direct causal link between ifn-i signaling, immune activation, negative immune regulator expression, lymphoid tissue disorganization, and long-term virus persistence. more recently, it was reported that during cl13 infection, both type i and ii interferon promoted the induction and suppressive capacity of cd95 + cd39 + immune regulatory dcs (iregdcs), respectively (cunningham et al., 2016) . while ifn-γ promoted the differentiation of iregdcs from monocytes, ifn-i promoted the suppressive functions of iregdcs. genetic deletion of ifnar1 prevented the expression of pd-l1 and production of il-10 from iregdcs, relieving their suppressive capabilities. in addition to modulating the suppressive capacity of iregdcs, ifn-i signaling also limited their generation/expansion. during mnov infection, selective genetic deletion of ifnar1 in dcs increased expression of the cellular activation markers cd80, cd86, and mhcii, suggesting that direct ifn-i signaling on dcs may be responsible for restraining dc function in vivo (nice et al., 2016) . generation of elevated numbers of iregdcs was also observed during hiv and mycobacterium tuberculosis infections as well as cancer, suggesting that iregdc generation is common in immunosuppressive environments. the ifn-i-driven immune-suppressive state during persistent lcmv infection also inhibits macrophage function. a recent study found that mice infected with the persistent docile strain of lcmv have impaired humoral immune responses to a superinfecting vsv infection (honke et al., 2016) . the absence of virus replication in cd169 + macrophages was not due to antiviral cd8 t cell-mediated killing of cd169 + macrophages but instead the result of sustained ifn-i responses and an elevated ifn-i antiviral gene program. in turn, reduction in vsv replication and antigen production in cd169 + macrophages reduced antigen production in these cells which was essential for antiviral antibody generation. the existence of multiple ifn-i subspecies (14 ifn-α species in mice and 13 in humans in addition to ifn-β) suggests that either the ifn-i system requires redundancy to be effective or that individual ifn-i species evolved to execute specific functions. certainly, different ifn-α species and β display varying degrees of affinity for the ifnar1/2 receptor complex (ng, mendoza, garcia, & oldstone, 2016; thomas et al., 2011) , with ifn-β displaying the highest binding affinity. lcmv persistence was influenced more by ifn-β than ifn-α signaling as treatment of mice infected with lcmv cl13 with an ifn-β neutralizing antibody displayed accelerated virus clearance compared to a polyclonal ifn-α antibody which had minimal effects on virus control (ng et al., 2015) . ifn-β neutralization did not exacerbate early virus replication, improved lymphoid architecture, and enhanced virus-specific cd4 and cd8 t cell responses. however, while ifn-β neutralization clearly promoted faster virus clearance as compared to neutralization with a polyclonal ifn-α antibody, the contribution of ifn-α species not neutralized by the polyclonal antibody used was not investigated. nevertheless, neutralizing ifn-β may promote adaptive immune control of virus without significantly affecting virus replication and thus may represent a safer approach to promoting control of persistent virus infection in vivo. the dichotomy between ifn-α and β was further highlighted upon infection of new zealand black (nzb) mice with lcmv cl13. infection of nzb mice with cl13 resulted in early lethality that was found to be due to cd8 t cell-dependent thrombocytopenia and pulmonary endothelial cells loss (baccala et al., 2014) . interestingly, despite upregulation of pd-1/pd-l1 expression and il-10 production, t cell function remained intact. moreover, this enhanced pathology correlated with elevated ifn-i protein levels and gene signatures; however, unlike infection in c57bl/6j mice, the pathology required ifn-α signaling and was ifn-β independent. it was recently reported that ifn-β signaling required binding to ifnar1 but was independent of ifnar2. deletion of ifnar1 ameliorated lps-induced sepsis induction, while ifnar2 à/à mice were unaffected (de weerd et al., 2013) ; thus, it would be interesting to test how ifnar2 à/à nzb mice respond to cl13 infection. the above studies demonstrate that ifn-α and -β species can differentially modulate immune responses in various viral infections, highlighting the importance of future investigation into how different ifn-i subtypes modulate viral control and disease pathogenesis. several important questions still remain that provide exciting avenues for investigating the roles of ifn-i signaling during viral infection in the future. although ifn-i signaling can trigger various downstream effector pathways, how signaling via select ifn-i species dictate specific outcomes following viral infections remain incompletely understood. specifically, there is a great need to understand the roles individual ifn-i-α and -β subsets play in restraining viral replication or promoting immune inflammatory/suppressive programs in vivo. further, how ifn-i signaling in specific cellular subsets in vivo regulates immune pathological and immunesuppressive responses will be interesting to dissect. the ifnar1-floxed mouse strain which was generated recently will be instrumental in future studies to investigate this question. illuminating what cell types require ifn-i signaling in vivo should pave the way for generating a detailed understanding of the cellular and molecular mechanisms by which ifn-i signaling acts to promote immune pathology and suppression in acute and persistent viral infections. the capacity of ifn-i signaling to promote immune pathology during acute respiratory viral infection appears in animal models of both influenza and sars-cov infection. the necessity of ifn-i signaling to restrain viral spread during acute viral infection suggest that targeting the ifn-i signaling pathway may be ill advised. however, one wonders whether targeting specific ifn-i species to suppress detrimental inflammation can be achieved without compromising virus clearance during acute respiratory viral infections. moreover, the production of ifn-λ during respiratory viral infection may be sufficient to control viral loads while ifn-i signaling is inhibited. recent results in mouse models suggest this may be possible; however, further studies are needed. moreover, whether the effects observed in mice will translate to human respiratory viral infections is unknown and should be investigated with caution. in the context of the immune-suppressive programs elicited by ifn-i signaling during persistent virus infection, the recent demonstration that blockade of ifn-β enhanced virus control by inducing improved lymphoid architecture and enhanced virus-specific cd4 and cd8 t cell responses, suggest that targeting selective ifn-i species can redirect immune responses sufficiently to promote immune-mediated virus control. importantly, relief of the immune-suppressive environment in this case was not accompanied by elevated viral loads following treatment with ifn-β-neutralizing antibody, suggesting that more selective modulation of specific ifn-i species can allow for preservation of some antiviral functions. the mechanisms by which the different ifn-i species interact with the ifnar1 and ifnar2 receptors to induce differential downstream signaling suggests this pathway could be manipulated pharmacologically. it is interesting to postulate whether small molecules or biologics could be developed to block binding/signaling of specific ifn-i species (i.e., ifn-β or specific α-species). for example, could ifn-β signaling be selectively inhibited without altering ifn-α species engagement with the ifnar1/2 receptor complex during ongoing viral infection using a small molecule or antibody therapeutic? could a small molecule be designed to reverse aspects of the immune-suppressive environment and promote virus control without compromising virus replication? on the contrary, could selective ifn-i agonists be developed to increase ifn-i signaling in a productive way to lower viral loads and bring persistent/chronic viral infection under control? a similar question could be posited during acute viral infections where ifn-i signaling promotes aberrant inflammation and immune pathology. moreover, it would be interesting to investigate whether selective biological or pharmacological modulation of ifn-i signaling may translate to treat autoimmune disease states associated with elevated and sustained ifn-i signaling. however, any therapy that enhances or blocks ifn-i signaling will need to be approached carefully, given the delicate balancing act required for controlling virus replication while safely modulating immune responses. protective immunity and susceptibility to infectious diseases: lessons from the 1918 influenza pandemic role of host immune response and viral load in the differential outcome of pandemic h1n1 (2009) influenza virus infection 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doi: 10.1016/j.cimid.2014.01.002 sha: doc_id: 293819 cord_uid: tbdsr5iw in recent years, several emerging zoonotic vector-borne infections with potential impact on human health have been identified in europe, including tularaemia, caused by francisella tularensis. this remarkable pathogen, one of the most virulent microorganisms currently known, has been detected in increasingly new settings and in a wide range of wild species, including lagomorphs, rodents, carnivores, fish and invertebrate arthropods. also, a renewed concern has arisen with regard to f. tularensis: its potential use by bioterrorists. based on the information published concerning the latest outbreaks, the aim of this paper is to review the main features of the agent, its biology, immunology and epidemiology. moreover, special focus will be given to zoonotic aspects of the disease, as tularaemia outbreaks in human populations have been frequently associated with disease in animals. seventy-five per cent of emerging infectious diseases are zoonotic [1] . some wildlife species have been recognised as being major reservoirs for infectious diseases and the proximity of wildlife habitats and the existence of arthropod vectors with a wide geographical spread have rendered epidemiological cycles more complex [1] . tularaemia is a zoonosis caused by the francisella tularensis bacterium, which was first isolated in 1912 in tulare county, california, by george mccoy and charles chapin [2] [3] [4] . initially termed bacterium tularense, it was allocated to a new genus and named f. tularensis in honour of the pioneer of research on the organism, edward francis [2, 4] . arthropod-borne transmission of tularaemia was first demonstrated by francis in 1919 when he isolated the etiologic agent in a patient with "deer fly fever" [2, 5, 6] . tularaemia was recognised as an important disease in the last century and since then there has been a growth in enthusiasm for research on this pathogen [7, 8] . interest has arisen with regard to f. tularensis as it has emerged in new locations, populations and settings, and increasingly figured in scientific research gauging its potential use in bioterrorism [7, 9] . the european centre for disease control and prevention (ecdc) 2012 surveillance report refers a total of 891 confirmed cases of tularaemia in a number of european countries in 2010, with sweden reporting the highest confirmed case rate, followed by finland and hungary [10] . tularaemia is considered an unusual disease and the confirmed case rate in europe has remained stable from 2006 to 2010. recent outbreaks of tularaemia have occurred in several european countries, presented in table 1 , including the czech republic, kosovo, bulgaria, germany, sweden, finland, spain, turkey, france and norway [11] [12] [13] [14] [15] [16] [17] [18] [19] [20] . besides these outbreaks, sporadic case notifications have occurred in austria, estonia, italy, lithuania, poland, romania, slovakia and the united kingdom [10] . although there are no reports of tularaemia for denmark during this period, a confirmed case of the disease in a human was recorded there in 2003 [21] . in portugal, the bacterium has been detected in the blood of an asymptomatic man and in a dermacentor reticulatus tick by molecular methods [9] . f. tularensis is one of the most virulent microorganisms currently known, while as few as ten microorganisms can cause potentially fatal disease in man and animals [7, 22] . this high rate of infectivity has led the centre for disease control and prevention (cdc) to classify f. tularensis as a category a biowarfare agent [23] . f. tularensis is a gram-negative, catalase-positive, pleomorphic and non-motile cocobacillus, characterised as a facultative intracellular pathogen that can grow within different types of cells including macrophages, hepatocytes and epithelial cells [2, 22, 24, 25] . the cell wall of f. tularensis has an unusually high level of fatty acids with a unique profile for the genus, and wild strains have a lipid-rich capsule, with neither toxic nor immunogenic properties [2, 5, 6] . capsule loss has been related to a decrease in virulence, although the viability or survival of the bacterium within neutrophils may remain unaltered. f. tularensis is a gamma ( )-proteobacteria of the francisellaceae family [2, 4, 22] . f. tularensis is the most common and pathogenic species and is formally divided into three subspecies with different pathogenicities and geographic distributions: tularensis, holarctica and mediasiatica. the species francisella novicida is currently widely accepted as a fourth subspecies of f. tularensis [3, 4, [26] [27] [28] [29] [30] [31] , as it shares with f. tularensis an average of 99.2% nucleotide identity over a 1.1 mbp of genome sequence [4, 26, 27, 30] . however, some objections to the transfer of f. novicida to the subspecies rank of f. tularensis have been recorded, based on recent multiple genome sequencing results, which show divergent evolutions for f. tularensis and f. novicida populations. therefore, separate species may be retained [32] . the f. tularensis subspecies tularensis, regarded as the most virulent subspecies and classified as type a, occurs predominantly in north america [3, 4, 6, 22, 33] . two distinct genetic sub-populations have been identified, ai and aii, which have different geographic distributions, hosts and vectors [3, 4, 6, 26, 30, 34] . sub-population ai has been additionally sub-divided into groups aia and aib [3, 6, 30, 35] . the subspecies holarctica, related to milder forms of the disease and classified as type b, occurs throughout the northern hemisphere [3, 22, 30, 33] . human infection with aib strains usually have a fulminant clinical progression and are associated with high mortality rates, in contrast with infections by aia and aii strains or type b tularaemia [25, 30, 35] . recently, this subspecies has also been detected in tasmania, australia [36] . subspecies mediasiatica presents a similar virulence to subspecies holarctica, but its geographic distribution is restricted so far to central asia [26, 33] . f. novicida is less virulent and has been isolated in north america, australia and thailand [3, 26, [29] [30] [31] [32] [33] 37] . based on a high degree of similarity between 16s rrna gene sequences, other microorganisms have been classified as probable members of the francisellaceae family; these include the francisella-like endosymbionts or fles [6, 8, 38] . fles belong to a distinct phylogenetic clade from f. tularensis species [39] . the effect of fles, if any, on vector competency and in the transmission of f. tularensis by ticks is still unknown [6] . fles have a worldwide distribution and are vertically transmitted by hard and soft ticks of the genera amblyomma, dermacentor, ixodes and ornithodoros [39] [40] [41] [42] . fles have been detected in ticks in north america [20, 111, 112] a information unavailable. (texas, california, minnesota), canada (alberta) and european countries such as spain, portugal, hungary, serbia and bulgaria [38] [39] [40] [41] [42] [43] [44] [45] . their pathogenicity to humans is undetermined. they have recently been detected in freeliving small mammals in europe, suggesting the possible transmission of some fle types from ticks to small mammals, although, to date, attempts to demonstrate it have failed [39, 41, 42, 45, 46] . the phylogeographic distribution of f. tularensis is given in fig. 1 ; the geographic locations where fles have been detected in ticks are also indicated. in nature, f. tularensis has been detected in a high number of wild species including lagomorphs, rodents, insectivores, carnivores, ungulates, marsupials, birds, amphibians, fish, and invertebrates [6, 22, 27, 39, [46] [47] [48] . lagomorphs and rodents are considered as the main reservoirs of f. tularensis [6, 22, 46] . wild lagomorphs, such as the european brown hare (lepus europaeus), are thought to be suitable sentinels for f. tularensis and disease surveillance [46, 47] . recently, there have been serological evidences that foxes and raccoon dogs could also act as biological indicators for tularaemia [48] . natural infections with f. tularensis have also been documented in different arthropods, although only a subset of these have been identified as important in f. tularensis transmission to humans. still, few pathogens show the adaptability of f. tularensis to such a wide range of arthropod vectors capable of infection dissemination [6] . arthropod found infected in nature include ticks of the genera amblyomma, dermacentor, ixodes and ornithodoros, mosquitoes of the genera aedes, culex, anopheles and ochlerotatus excrucians, and flies from the tabanidae family (tabanus spp., chrisozona spp. and chrisops spp.) [6, 22, 27, 49] . nevertheless, vector competence has only been demonstrated in ticks of the genera dermacentor [35] . tick-borne transmission of f. tularensis usually results in sporadic cases, although occasional outbreaks have also been reported [6] . although regarded as merely mechanical vectors, mosquitoes have been associated with widespread epidemics of tularaemia and are capable of transient disease transmission [6, 50] . both ticks and mosquitoes may be infected in the larval phase. transtadial transmission has been demonstrated in ticks although in mosquitoes evidences for transtadial transmission are only based in molecular methods [35, 50] . although transovarial transmission of f. tularensis in ticks was reported [2, 6, 51] , a recent study in dermacentor variabilis has proved otherwise [52] . despite dissemination to ovaries and then to the oocytes, the pathogen was not recovered from the subsequently hatched larvae. tabanid flies are regarded as mechanical vectors for f. tularensis and the long-term survival of this bacterium does not occur in these arthropods [6] . the epidemiologic characteristics of vector-borne tularaemia vary throughout the northern hemisphere and also within a given geographic location. this is thought to be related to the abundance of different vectors and host species. this could explain why, in the usa, sweden, finland and russia, the arthropod bite is a common mode of transmission to humans, whilst in western and central europe, contact with infected animals and the ingestion of contaminated food or water have been reported as more common transmission modes. differences in transmission patterns have also been recorded within the usa: in western states, both ticks and deer flies are considered to be important vectors of tularémia, while in the east only ticks are considered relevant. in sweden and finland, mosquitoes have been identified as the primary vectors [6] . in portugal, the role of ticks and small mammals in the transmission of tularaemia is still the subject of research. a collection of 4949 mosquitoes belonging to the genus culex (63.97%), ochlerotatus (35.34%), anopheles (0.42%), culiseta (0.14%) and a small number of aedes aegypti females from the island of madeira (0.12%) have been analysed, although all the results were found to be negative [53] . so far, this is in accordance with previous findings regarding the epidemiology characteristics of vector-borne tularaemia, suggesting that, in portugal, mosquitoes have no role in the transmission of this disease. ticks are thought to be the most important vectors of tularaemia in the majority of countries where tularaemia is endemic [53] . nevertheless, major on-going research on tularaemia, aiming at gauging the overall impact of the disease in portugal, is expected to throw further light on the main f. tularensis sources. in endemic areas, tularaemia is a seasonal disease, with higher incidence in late spring, summer and autumn, occurring annually over a 5-year period or unreported for more than a decade. often, the number of cases varies widely from 1 year to another, which is thought to be due to temperature or precipitation variability. however, the association between climactic conditions and tularaemia outbreaks has yet to be demonstrated [49] . f. tularensis has been found to be extremely resistant to environmental stress, surviving for weeks in soil, water and animal carcasses, at low temperatures [22] . human tularaemia outbreaks are often preceded by animal outbreaks, particularly in wild lagomorphs and rodents. this is usually related to an increase in the numbers of these species, increasing the probability of exposure to infected animals [4, 22, 27, 49] . the transmission of tularaemia to humans can occur either by direct contact with infected animals or indirectly due to arthropod vector bites, the ingestion of contaminated water, food or aerosols inhalation. aerosols can be dispersed by ventilators, farming, and the deposition of contaminated hay, either intentionally or unintentionally [22] . domestic dogs and cats can also transmit tularaemia to humans after contact with an infected animal, environment or infected ticks [54] [55] [56] . personto-person transmission has not been described so far [2, 22, 49, 54] . tularaemia has been reported to occur in any age group. men tend to present a higher prevalence than women [2, 49] . professions that are prone to contact with reservoirs or arthropod vectors have been associated with a higher infection risk: these include laboratory technicians, hunters, farmers, veterinary surgeons, and anyone handling the flesh of infected animals [22, 27] . few pathogens show the adaptability of f. tularensis to varying vector, host and environmental conditions. variations occur in local transmission cycles in association with differing ecologies. both f. tularensis type a and type b are associated with different life cycles in which different animal hosts and arthropod vectors intervene [6] . type a tularaemia is more commonly associated with the terrestrial cycle of the disease, with wild lagomorphs such as rabbits and hares acting as vertebrate hosts in which amplification of the agent occurs and where arthropods are disease-disseminating vectors [6, 22, 54, 57] . type b tularaemia is more frequently associated with the aquatic cycle, although outbreaks of tick-borne tularaemia involving subspecies holarctica have been reported [2, 6, 57] . in this life cycle, f. tularensis circulates in rodents such as beavers, muskrats and voles, and can be introduced in water courses from animal carcasses [6, 22, 27, 54] . there is also evidence that f. tularensis can persist in water courses in association with amoebas [27, 49, 58] . contaminated water can be the source of infection to humans, flies and mosquitoes [49] . an unusual waterborne outbreak of human tularaemia has been described in spain associated with crayfish (procambarus clarkii) caught in a contaminated freshwater stream. the crayfish acted as mechanical vectors, through mud-or water-contaminated carapaces, although the presence of f. tularensis in crayfish stomach and hepatopancreas could indicate their eventual role as hosts [51] . a diagrammatic representation of the terrestrial and aquatic cycles of tularaemia is shown in fig. 2 . f. tularensis is a remarkable bacterial pathogen that can invade and multiply in a wide range of cell types [4, 22, 24, 25, 59] . antigen-presenting cells (apc) such as macrophages or dendritic cells, appear to be the primary cell types targeted by the bacterium at the outset of infection [59] . the virulence of the bacterium is directly related to its capacity to replicate within the cytosol of infected cells [60] . f. tularensis clearly possesses several mechanisms by which it manipulates immunity. the bacterium evades detection at the point of entry in the host in three ways: (a) it has modified cell-surface structures that enable it to avoid interaction with host receptors that are associated with the induction of inflammation; (b) it targets cells that lack co-receptors which facilitate binding to receptors that might alert the host cell to invasion; (c) it utilises receptors that fail to initiate the production of proinflammatory cytokines [60] . the entry of f. tularensis in macrophages occurs by means of a specific mechanism inherent to francisella spp. [24] . the bacterium induces the macrophage to produce asymmetric spacious pseudopod loops in a "looping phagocytosis" process [4, 61] . uptake of f. tularensis is markedly enhanced by serum opsonisation, which depends on serum intact complement factor c3 and host cell receptors (cr3), involving bacterial surface polysaccharides [4, 62] . utilisation of cr3 (and of mannose receptors of dendritic cells (mr) under non-opsonising conditions) is considered to be a fairly innocuous route for entry of f. tularensis, since it is not associated with the induction of signalling cascades that result in pro-inflammatory cytokines production. when opsonised by serum, f. tularensis binds ic3b and gains entry to host cells via the cr3 receptor [59] . the lipopolysaccharide (lps) of subspecies tularensis is only moderately inflammatory and acts as an extremely weak toll-like receptor (tlr) 4 agonist stimulating a reduced production of pro-inflammatory cytokines [59, 63] . these is attributed to the presence of only four acyl groups on the lps that do not bind to the "lps-binding proteins", subverting tlr4 recognition [4, 25, 59] . in addition to lps, f. tularensis possesses two other tlr agonists [59] : tul4 and ftt1103 lipoproteins. these interact with tlr2 and may alert the host cell for the presence of the bacterium prior to phagocytosis [4, 25, 59] . tlr2/myeloid differentiation primary response gene (88) (myd88) signalling is essential for the production of pro-inflammatory cytokines and is critical for host defence against francisella infection [24, 61, 63, 64] . f. novicida has been used as a model organism to study immunity to f. tularensis. nevertheless, f. novicida expresses a structurally distinct chemotype of lps that is more pro-inflammatory in mice than the dominant lps chemotype, and is expected to result in different inflammasome activations [25] . f. novicida escapes the phagossome and replicate in the cell cytosol where it is recognised by the inflammasome signalling system [24, 25, 60, 64] . inflammasome stimuli activate the protease cysteine aspartate-specific caspase-1, promoting the release of potent pro-inflammatory cytokines responsible for cell apoptosis [24, 60] . this results in f. novicida release from infected cells and enables the infection of new ones [24, 60] . f. tularensis survival and replication within macrophages is enabled by a large set of virulence genes that include the "macrophage growth locus" (mgl) a and b and the "francisella pathogenicity island", fpi [24] . fpi encodes for a putative type vi secretion system [4, 8] and contains 19 genes that have been demonstrated as essential for intra-cellular growth and virulence [24] . less virulent f. novicida presents only one copy of fpi in contrast with f. tularensis subspecies tularensis and holarctica that present two copies [4, 24] . genes within the fpi are regulated by mgla [4] . although current knowledge of the gene's functions is far from complete, this is one of the most active areas of francisella research [8] . following phagocytosis of opsonised f. tularensis by polymorphonuclear cells (pmn), the bacterium actively inhibits superoxide anion generation (ros) via nadph oxidase. this allows f. tularensis to evade the phagosome and persist in the cell cytosol. the contribution of polymorphonuclear cells seems to be related to the secretion of cytokines and chemokines that recruit effector cells to the infection site [25] . however, an excessive recruitment of neutrophils, modulated by an increase in metaloprotease-9 from the matrix, plays an important role in modulating leucocyte recruitment and seems to be directly related to f. tularensis pathogenesis [24, 25] . natural killer (nk) cells from the liver, spleen and lung also play an important role in the innate immune response, in particular by producing inf-␣ following primary infection by f. tularensis [25] . as f. tularensis is an intracellular pathogen, cellular immune response is believed to be the main defence mechanism. memory effector t cells cd4+ and cd8+ are clearly important for the primary control of infection. these cells produce type th1 cytokines like inf-␥, tnf-␣ and il-2 that are critical for the initial response to f. tularensis infection [25] . although the role of humoral immunity in f. tularensis infection is believed to be less important, some studies have demonstrated the enhanced recovery of infected humans that have received hyper-immune serum [59] . also, infection-specific igm, iga and igg antibodies produced are good exposition indicators and may interfere with the ability of bacteria to infect host cells [25, 49, 59] . the contribution of b cells in defence is thought to be dependent on strain virulence [8, 25] . research on anti-francisella antibodies targets is expected to allow for the identification of new diagnostic or reactive antigens and the development of vaccines [8] . furthermore, f. tularensis is capable of influencing multiple pathways, and continued research into the specific mechanisms by which f. tularensis evades, modulates and suppresses the host immune response will improve our understanding of tularaemia pathogenesis and the regulation of host immunity [59] . relevant clinical disease has been reported with f. tularensis subsp. tularensis and holarctica. clinical manifestations of tularaemia depend on strain virulence, infective dose and infection route, the extent of systemic involvement and host immune status [2, 4, 49] . the incubation period averages 3-5 days but ranges from 1 to 20 days. the disease has an acute onset, with the occurrence of fever (38-40 • c), chills, fatigue, generalised myalgia and headaches, resembling a flu-like syndrome [2, 22, 49] . the subspecies tularensis (type a) causes severe disease, potentially fatal if untreated. the subspecies holarctica (type b) causes less severe disease and fatalities are rare [49] . depending on the route of infection, the following forms of the disease are described: ulceroglandular, glandular, oculoglandular, oropharyngeal, pneumonic, typhoidal and septic [22, 49] . ulceroglandular and glandular forms of the disease are the most common and frequently result from an arthropod bite or animal contact [2, 4, 49] . in ulceroglandular tularémia, a soft, painless ulcer develops at the inoculation site and evolves to a scar [6, 22] . this presentation is associated with fever, lymphadenopathy and, in type a tularaemia, pneumonia and pleural effusion can occur [49] . in glandular tularaemia, the primary ulcer is unrecognisable [2, 6, 22, 49] . direct contamination of the eye through contaminated fingers, splashes or aerosols, may be followed by oculoglandular tularaemia. unilateral conjunctivitis, with ulcers or papules in some patients, photophobia and epiphora are the main signs of this form of the disease [2, 49] . oropharyngeal tularaemia is acquired by means of contaminated food or water intake and aerosol inhalation [22] . it develops with ulcerative and exudative stomatitis and pharyngitis [49] . pneumonic tularaemia occurs by means of contaminated aerosol inhalation but can also arise as a complication of any of the other disease forms by haematogenous generalisation [2, 22, 49] . initial disease development is characterised by fever, cough, pleuritic chest pain and dyspnoea, along with other unspecific symptoms. type a tularaemia is associated with significantly severer and more fulminant forms of pneumonia [2, 49] . typhoidal tularaemia refers to a systemic and febrile form of the disease in which no route of infection acquisition can be established [2, 49] . septic tularaemia is a severe and often fatal form of the disease that can occur as a complication of the ulceroglandular form in type a tularaemia [22, 49] . patients can present unspecific and neurologic symptoms, and septic shock, sirs (systemic inflammatory response syndrome), dic (disseminated intravascular coagulation), haemorrhages, sars (severe acute respiratory syndrome) and multiple organ failure [22, 49] . in type b tularaemia, complications of meningitis and septicaemia have only occasionally been described [49] . clinical manifestations largely depend on the susceptibility of animal species to f. tularensis [49] . in wild animals, clinical signs of tularaemia are not well documented, and post-mortem findings are highly unspecific and include splenomegaly and punctual necrotic lesions in the liver and spleen [49, 54] . in one experimental study in european brown hares (lepus europaeus), clinical signs developed 1-day postinoculation with a f. tularensis subspecies holarctica strain. these included fever, lethargy and anorexia. two of the five hares in the study succumbed to the infection on days 5 and 9 following inoculation. pathological findings included splenomegaly, diffuse spleen necrosis and focal liver necrosis with hepatocytes vacuolisation. the remaining three hares were euthanised and revealed no pathological lesions. both bacterial culture and mouse inoculation test failed to produce f. tularensis isolation [46] . in a natural outbreak of tularaemia in brown hares in france, all eight hares involved presented splenomegaly, congestion and haemorrhagic lesions of several organs, tracheitis and bronchitis [65] . a similar study carried out in hungary on european brown hares naturally infected with f. tularensis subspecies holarctica also showed very similar results [47] . in another study, 20 female new zealand white rabbits (oryctolagus cuniculus) were exposed to type a tularaemia aerosols, with three different doses. seven of them died while the others developed fever, anorexia and weight loss, with all infecting doses. haematological findings in six rabbits included lymphopenia, monocytopenia and thrombocytopenia. a bibasilar pneumonia and gastrointestinal tract gas distension were the only radiological findings. necropsy findings demonstrated hepatosplenomegaly with extensive spleen necrosis and small white nodules. some of the rabbits presented nodular lesions in the lungs while others showed haemorrhagic lesions [66] . a situation of particular public health significance, given the risk of pet-to-human transmission, is associated with infected prairie dogs (cynomys ludovicianus) sold as pets in the usa and exported internationally [67, 68] . a ban was put in place in the european union and other countries regarding the import of prairie dogs and other rodent species after the usa monkeypox outbreak in 2003 [68, 69] . wild-caught prairie dogs are particularly susceptible to environmental stress, such as capture, transit and crowding, which can enhance disease manifestations. clinical signs include lethargy, dehydration and grossly enlarged cervical lymph nodes. prairie dogs can produce specific antibodies against f. tularensis and survive tularaemia infection, suggesting their potential role as f. tularensis reservoirs in nature. moreover, one study found that all seropositive animals harboured live infectious bacteria, suggesting persistent infection [67] . tularaemia has also been described in domestic dogs and cats [49, 55] , which may be infected by means of arthropod bites, direct contact with infected animals, their ingestion, or contaminated aerosols [70, 71] . cats usually develop severe illness with unspecific clinical signs like fever, lethargy, prostration, vomiting and anorexia, dehydration, regional or generalised lymphadenopathy, splenomegaly, tongue and oropharyngeal ulceration and jaundice [49, 72, 73] . pathological findings include multiple necrotic foci on the lymph nodes, spleen, liver and lungs. frequently, panleukopenia with toxic degeneration of the neutrophils and hyperbilirubinaemia with bilirubinuria are present [73] . dogs are less susceptible and rarely manifest signs of the disease [55, 56] . nevertheless, they can act as carrier hosts [70] and transmit the bacterium by means their fur after contact with contaminated dead animals or soil [74] . in most cases, infection is self-limiting and recovery is spontaneous. however, only few cases of natural infection in dogs have been reported [55, 56] . in humans, samples should preferably be collected before the onset of antibiotherapy and depend on the clinical form of the disease. samples may include non-heparinised whole blood, serum, respiratory tract secretions and washes, swabs from visible lesions, lymph node aspirates or biopsies, urine, and autopsy materials [49] . in animals, serum is the preferential sample for all disease forms, but plasma and dry blood on paper filters can also be used. blood samples should be collected at least 14 days after the onset of the symptoms. lymph nodes or bone marrow aspirates, organs (lung, liver, spleen) and cerebrospinal fluid can also be used [49] . in the context of an outbreak or epidemiologic studies, samples should include arthropod vectors as well as environmental samples like water, soil and rodent faeces [49, 54] . culture is the gold standard for f. tularensis and must be carried out in biosecurity level 3 facilities (bsl-3) [2, 22, 49] . f. tularensis is a fastidious microorganism. optimal growth conditions occur at 37 • c and ph 6.9 [5, 24] . cysteine-enriched media, such as enriched chocolate agar (ca) or 9% cysteine heart agar with blood medium (chab) must be used for this purpose [22, 49, 54] . growth in a chab medium enables the presumptive identification of f. tularensis by characteristic growth at 24-48 h of round and smooth green opalescent shiny colonies, 2-4 mm in diameter [4, 22, 27, 49, 54] . antibiotic supplementation of chab is possible in order to optimise growth and inhibit contaminants [22, 49, 54] . for cultures made from blood, the use of the bactec tm (bd) system or equivalent, bact/alert tm (biomérieux) is recommended [49, 54] . liquid media is not suitable for f. tularensis growth, even when supplemented with cysteine [4, 27, 54] . basic biochemical tests provide a presumptive identification of isolates and may be further complemented by immunological and molecular methods. some additional biochemical tests, such as the ability to ferment glucose or glycerol, or the presence of the citrulline ureidase pathway are useful for subtyping purposes [54] . the commercial microlog microstation tm system (biolog inc., hayward, ca) based on the ability to ferment glucose has been successfully used for differentiating between subspecies tularensis and holarctica [54, 67] . also, the commercially available microbial identification system (mis) and library generation system (lgs) (midi, inc, newark, nj) enables cell-wall fatty-acid analysis and can be used for the identification of francisella at the genus level. it has also enabled the identification of atypical f. tularensis strains lacking cysteine requirements [54, 75] . immune based techniques have also been employed for identification: immunoblot analysis and immunofluorescence microscopy, either from grown cultures or clinical samples [54] . antibodies against f. tularensis reach detectable levels 10-20 days post-infection [49] . a fourfold increase in the titre between acute and convalescent sera or a titre of 1:160 or greater of agglutinating antibodies is considered for diagnostic purposes [2, 27, 54, 76] . titres peak at a level of 320-1280 and decline slowly [76] . serologic methods include the whole-cell agglutination test (widal's reaction), the tube agglutination test, microagglutination assays, haemagglutination, elisa (enzyme-linked immunosorbent assay) and immunoblot [2, 22] . elisa has repeatedly been more sensitive than agglutination assays, with the additional advantage of determining separately different antibody classes (igm, igg and iga) [54] . a combination of a first elisa screening test complemented by an immunoblot confirmatory test, with higher specificity, is the current recommended two-step approach for the serological diagnosis of tularaemia [54] . the same approach can be used for animals. serology has a limited use in highly susceptible species since death usually precedes the development of specific antibodies [47] . however, in endemic areas, antibodies for f. tularensis are frequently detected in wild animals that have developed immunity, including foxes and coyotes. this seroconversion is suspected as being related to subspecies holarctica infection since infection by the subspecies tularensis is expected to be fatal [27, 49] . molecular methods are valuable diagnostic tools whenever culture is either not possible or is negative [2, 22, 49] . moreover, they reduce the high risk of laboratory-acquired infections over conventional biochemical typing [2, 21, 77] . during recent years, polymerase chain reaction (pcr)based methods have been successfully used for the rapid identification and classification of francisella isolates, with increased sensitivity and specificity [54, 78] . however, false positive results related to non-pathogenic closely related francisella subspecies, occurring naturally in the environment, may hamper species and subspecies identification [78] . conventional pcr targets are tul4 and fopa genes, which encode for f. tularensis superficial membrane lipoproteins. both protocols show a good level of sensitivity and reasonable specificity in f. tularensis detection and may be used in blood, tissue or aerosol samples [4, 49, 54] . pcr product specificity is confirmed by sequencing, reverse-line blotting (rlb) or restriction fragment-length polymorphism (rflp) [54] . real time pcr for f. tularensis detection has been developed, in particular, taqman tm (applied biosystems) real time pcr multiple assay shows high specificity and sensitivity using four target genes: isftu2, 23 kda, tul4 and fopa [49, 54] . real-time pcr for the differentiation between the subspecies tularensis and holarctica is also now available [79] . further discrimination has been achieved using highresolution genotyping methods including pulse-field gel electrophoresis (pfge), amplified fragment-length polymorphism (aflp), ribotyping, 16s rdna gene sequencing, canonic insertion deletions and paired-end sequence mapping [26, 27, 34, 80] . still, as f. tularensis exhibits highly conserved genomic sequences among strains of diverse origin, genetic polymorphisms allowing for individual strain typing have been difficult to find [77] . as for other bacteria, more recent pcr-based techniques such as variable-number tandem repeats (vntr), multiple-locus vntr analysis (mlva) and short-tandem repeats (str) typing have been successfully used for identification at the subspecies level and for molecular epidemiology purposes [54, 77, 80] . one of the most discriminatory methods for the molecular subtyping of f. tularensis is mlva, which consists of a series of vntr loci that are pcr amplified via flanking primer sites and examined for size variation [79] . one mlva system designed for f. tularensis is based on polymorphisms of 25 vntr loci, ft-m1 to ft-m25. this mlva typing system has a greater discriminatory power when applied to a worldwide set of f. tularensis isolates and provides accurate classification at the subspecies level [77] . this mlva system has recently been improved by redesigning the subset of the 25 previously identified vntrs to produce a new optimised, multiplexed mlva system with a similar level of discrimination but with fewer time and cost requirements [79] . ten of the previously described vntr loci were selected based on their discrimination ability within the subspecies: ft-m02, ft-m03, ft-m04, ft-m05, ft-m06, ft-m010, ft-m20, ft-m22, ft-m23 and ft-m24. locus ft-m20 was split into two loci, ft-m20a (which contains the originally described 12 bp repeat and is polymorphic across subspecies) and ft-m20b (which contains the insertion with its 15 bp repeat and varies only among type a.ii and f. novicida isolates) [79] . while providing discrimination among strains, vntrs are unsuited for determining deeper phylogenetic relationships due to mutational saturation. in this case, more accurate and alternative markers should be used, such as whole-genome sequence single nucleotide polymorphism (snps) [79] . additional studies have shown a remarkable degree of discrimination of the f. tularensis phylogenetic structure, using a combined analysis with canonical whole-genome snps for major clade typing, and mlva for high-resolution typing [26, 79] . in a different study, the combined analysis of insertion-deletion markers, for subspecies and major clade typing, along with mlva, was used [80] . microarrays have also allowed for the differentiation of the four f. tularensis subspecies and have been proven useful for pathogenicity and virulence marker identification [54] . tularaemia usually responds to antibiotic therapy. historically, aminoglycosides have been the drugs of choice for humans. although clinically effective, they are rarely used now due their ototoxicity and nephrotoxicity. nevertheless, gentamicin has been used for treatment of pneumonic tularaemia and aminoglycosides are now generally used in the most serious cases. chloramphenicol is effective but seldom the first choice due to its possible irreversible effects on haematopoiesis. tetracyclines have been associated with high relapse rates on withdrawal. fluoroquinolones, such as ciprofloxacin, have been shown to be highly effective in per os and are the best choice for uncomplicated tularaemia. also, ciprofloxacin has proved suitable and effective in the treatment of tularaemia in children and pregnant women [4, 49] . in domestic animals, gentamicin, enrofloxacin, doxycycline and chloramphenicol are referred to as therapeutic options for dogs [55, 70] . in cats, there are reports of the use of doxycycline or enrofloxacin and amoxicilin-clavulanic acid as being beneficial in the early stages of the disease [81] . currently, there is no available licensed vaccine against f. tularensis although an attenuated type b strain, known as the live vaccine strain (lvs) was developed in the united states during the 1950s and used to vaccinate military personnel and laboratory workers [4, 49, [82] [83] [84] . lvs failed to uniformly protect against pneumonic tularaemia and when delivered in high titres caused mild tularaemia as an undesirable side-effect [85] . one focus of current research work in the usa and in europe is to develop a vaccine for protection against f. tularensis intentional release [49] . the restricted efficacy of the lvs has fostered extensive research with a view to providing alternative vaccine formulations, including the exploration of different live and killed attenuated strains and immunogenic components to produce subunit vaccines [4, 82] . in view of its immunogenic antigens, an effort has been made to develop attenuated strains of schus4, a representative strain of type a tularaemia, for vaccine production. in fact, between lvs and schus4 strains there are about 35 genes that encode for different protein sequences, whose functions are not well defined, and may represent important immunogenic antigens. still, given the increased virulence of the schus4 strain, only a small number of bacteria should be required to generate effective protection against wild type f. tularensis [85] . a recently published study demonstrated that inoculation with low doses of specific attenuated mutants of the f. tularensis strain schus4 provided protection against parenteral and intranasal challenge with a fully virulent wild type schus4 strain [86] . this favours the role of t-cell memory response as a critical determinant of f. tularensis immunity, additionally to the humoral response. this feature is the basis of the challenges foreseen for vaccine development, aiming at identifying antigen determinants that elicit an effective cellular-mediated immune response [4, 82, 84, 85] . cell-mediated immunity was found to persist three decades after tularaemia vaccination. a recent study sought to identify the t-cell responses present in immune individuals in order to characterise f. tularensis-specific immune response [84, 86] . the findings showed that the production of inf-␥, macrophage inflammatory protein (mip)-1␤ and cd107a (lysosomeassociated membrane protein 1 or lamp-1) by peripheral blood mononuclear cells appeared to be a characteristic of protective immune responses and that a correlation exists between these parameters and immunity [84] . several factors such as human demographics and behaviour, international travel and commerce, including the animal trade, climactic changes and microorganism adaptation, have a potential impact on disease ecology and the emergence of zoonosis. the same factors are thought to be related to the emergence of tularaemia. special concerns regarding this bacterium exist in relation to its high infectivity, and easy dispersion through aerosols and contaminated water, which make it a potential bioterrorism weapon. also, tularaemia presents a wide geographic distribution and has recently emerged in new settings, particularly in europe. in portugal, an on-going research project on tularaemia aims to increase our knowledge about the disease, particularly its impact in this country, which is still poorly understood, in view of the fact that there is little information available to risk population and health professionals, with the result that there is a possible underestimation of prevalence in man and animals. to this regard, efforts have been made by the national institute of health to increase awareness of the disease among risk populations, particularly hunters and health professionals. in accordance with the preliminary results, on-going research will further identify and characterise f. tularensis circulating strains and develop molecular and typing methods with increased sensitivity, specificity and discriminatory power. the role of autochthon wild lagomorphs in the f. tularensis life cycle, their involvement in animal-to-human transmission and their suitability as tularaemia sentinels will be accessed. moreover, considering the economic and social relevance of hunting-related activities in this country, with very few studies having acknowledged its relation to zoonotic disease transmission risks, research into infection in game species is of major importance. f. tularensis is also associated with a considerably wider range of hosts and vectors than most zoonotic pathogens, although there is little information on bacterium mechanisms for adaptation to such a wide diversity of arthropod vectors. despite our increasing knowledge of tularaemia and its etiological agent, many aspects of f. tularensis biology and epidemiology need to be further examined, particularly its pathogenicity and virulence, vaccine development, and the specific mechanisms by which f. tularensis evades, modulates and suppresses the host immune response. as with any zoonotic emergent disease, the role of wild and domestic animals in f. tularensis epidemiology needs to be further evaluated, in particular, those which may act as reservoirs. other epidemiologic data such as the population dynamics of susceptible animals, particularly lagomorphs and rodents in europe, should be part of surveillance programmes, as they are thought to be directly associated with disease transmission patterns. from a public health perspective, disease surveillance in animals is crucial in order to prevent and monitor human outbreaks, particularly in endemic areas, where contact between humans and wildlife 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cord-103108-vmze2mdx authors: vanheer, lotte; schiavo, andrea alex; van haele, matthias; haesen, tine; janiszewski, adrian; chappell, joel; roskams, tania; cnop, miriam; pasque, vincent title: revealing the key regulators of cell identity in the human adult pancreas date: 2020-09-25 journal: biorxiv doi: 10.1101/2020.09.23.310094 sha: doc_id: 103108 cord_uid: vmze2mdx cellular identity during development is under the control of transcription factors that form gene regulatory networks. however, the transcription factors and gene regulatory networks underlying cellular identity in the human adult pancreas remain largely unexplored. here, we integrate multiple single-cell rna sequencing datasets of the human adult pancreas, totaling 7393 cells, and comprehensively reconstruct gene regulatory networks. we show that a network of 142 transcription factors forms distinct regulatory modules that characterize pancreatic cell types. we present evidence that our approach identifies key regulators of cell identity in the human adult pancreas. we predict that heyl and jund are active in acinar and alpha cells, respectively, and show that these proteins are present in the human adult pancreas as well as in human induced pluripotent stem cell-derived pancreatic cells. the comprehensive gene regulatory network atlas can be explored interactively online. we anticipate our analysis to be the starting point for a more sophisticated dissection of how transcription factors regulate cell identity in the human adult pancreas. furthermore, given that transcription factors are major regulators of embryo development and are often perturbed in diseases, a comprehensive understanding of how transcription factors work will be relevant in development and disease biology. highlights reconstruction of gene regulatory networks for human adult pancreatic cell types an interactive resource to explore and visualize gene expression and regulatory states predicting putative transcription factors driving pancreatic cell identity heyl and jund as candidate regulators of acinar and alpha cell identity, respectively a fundamental question in biology is how a single genome gives rise to the great diversity of cell types that make up organs and tissues. a key goal is to map all cell types of developing and mature organs such as the pancreas, an essential organ at the basis of multiple human disorders including diabetes and cancer (kahn, cooper and del prato, 2014; kamisawa et al., 2016; han et al., 2020) . single-cell rna sequencing (scrna-seq) provides a powerful tool to resolve cellular heterogeneity, identify cell types and capture highresolution snapshots of gene expression in individual cells (grün et al., 2016) . with the advent of singlecell transcriptomics, great progress has been made toward the creation of a reference cell atlas of the pancreas (baron et al., 2016; segerstolpe et al., 2016; wang et al., 2016; xin et al., 2016; enge et al., 2017; lawlor et al., 2017; augsornworawat and millman, 2020; han et al., 2020) . work from several groups provided cellular atlases of the pancreas during mouse development (stanescu et al., 2017; byrnes et al., 2018; scavuzzo et al., 2018) , in adult mice (muraro et al., 2016) and in human fetal and adult pancreas (liu et al., 2014; baron et al., 2016; muraro et al., 2016; segerstolpe et al., 2016; wang et al., 2016; enge et al., 2017; han et al., 2020) . efforts have also been made to map cellular identity during pancreas development starting from human pluripotent stem cells hrvatin et al., 2014; zhu et al., 2016; han et al., 2020; hogrebe et al., 2020; peterson et al., 2020) . taken together, these studies provide an opportunity to better understand the maintenance and establishment of cellular identity among different pancreatic cell types. work over the past decades indicated that cellular identity is established by combinations of transcription factors (tfs) that recognize and interact with cis-regulatory elements in the genome. these transcription factors, together with chromatin modifiers, give rise to gene expression programs. a small number of core tfs are thought to be sufficient for the establishment and maintenance of gene expression programs that define cellular identity during and after development (ohno, 1979) . studies conducted in both mouse and human have successfully identified tfs that are pivotal for the acquisition and maintenance of pancreatic cell fates (dassaye, naidoo and cerf, 2016) . these include pdx1 (zhou et al., 2008; shih et al., 2015) , mafa (nishimura, takahashi and yasuda, 2015) , ngn3 (gradwohl et al., 2000) , nkx2.2 (sussel et al., 1998) , pax4 (sosa-pineda et al., 1997) , nkx6.1, neurod1 (mastracci et al., 2013) , arx (collombat et al., 2003) , mafb (artner et al., 2006) , rfx6 (smith et al., 2010) , gata4 (ketola et al., 2004) , foxa2 and sox9 (shroff et al., 2014; shih et al., 2015) . conditional deletion of tfs such as foxa2 and pdx1 in adult beta cells results in the loss of cellular identity and function (sund et al., 2001; gao et al., 2014) . genetic evidence for the role of these tfs in establishing human pancreatic cell identity is provided by the identification of tf loss-of-function mutations that cause pancreatic agenesis (stoffers et al., 1997; sellick et al., 2004; allen et al., 2012; shaw-smith et al., 2014; de franco et al., 2019) or neonatal or young-onset diabetes (senée et al., 2006; solomon et al., 2009; rubio-cabezas et al., 2010 smith et al., 2010; bonnefond et al., 2013; flanagan et al., 2014) . in addition, tf overexpression can reprogram somatic cells to adopt alternative identities (takahashi and yamanaka, 2006; zhou et al., 2008; vierbuchen et al., 2010; lima et al., 2016) . for example, the induced expression of ngn3, pdx1, and mafa was shown to reprogram mouse alpha cells into beta-like cells in vivo (zhou et al., 2008) . however, how key tfs underlie the maintenance of cellular identity in the human pancreas remains incompletely understood. over the past decade, multiple approaches to reconstruct gene regulatory networks (grns) from bulk and single-cell omics data have been developed (ghazanfar et al., 2016; lim et al., 2016; matsumoto et al., 2017; fiers et al., 2018) . in particular, it is now possible to combine single-cell transcriptomic data with cisregulatory information to infer grns (janky et al., 2014; aibar et al., 2017; van de sande et al., 2020) . because tfs recognize dna motifs in the genome, one can measure if inferred target genes are expressed within single cells, and therefore quantify the activity of tfs. such approaches have revealed the regulatory programs in distinct systems including the drosophila brain (davie et al , 2018) , cancer (wouters et al., 2020) , during early mouse embryonic development (peng et al , 2019) , in a mouse cell atlas (suo et al., 2018 ) and a human cell atlas (han et al., 2020) . analysis of grns in the human adult pancreas has identified distinct endocrine and exocrine regulatory states with multiple stable cell states for alpha, beta and ductal cells (kumar and vinod, 2019) . type 2 diabetes and body mass index (bmi) were shown not to impact grn activity of alpha and beta cells (kumar and vinod, 2019) . previous data shows that type 2 diabetic (faerch et al., 2015; dennis et al., 2019; dybala and hara, 2019; zaharia et al., 2019) and non-diabetic human islet preparations vary greatly depending on age (enge et al., 2017; westacott et al., 2017) and bmi (henquin, 2018) warranting the exploration of grns in larger cohorts. hence, it remains unclear whether previous grn findings can be extrapolated to a broader, highly heterogeneous non-diabetic and type 2 diabetes patient population. the development of integration methods provides an opportunity to analyze multiple scrna-seq studies from multiple laboratories and patients (butler et al., 2018; luecken et al., 2020) . additional knowledge on how grns maintain cellular identity in the human adult pancreas may further the understanding of disease states as well as improve efforts to convert patient cells into functional, mature beta cells for diabetes treatment. here, we build an integrated human pancreas gene regulatory atlas. in this resource, we use single-cell transcriptomes of the human adult pancreas, taking advantage of integration strategies and computational tools to reconstruct grns. our analysis identifies the grn landscape and candidate regulators that are critical for cellular identity in the human adult pancreas. integrating multiple human adult pancreas scrna-seq datasets can further improve the power of scrnaseq analyses to create a human adult pancreas cell atlas. we set out to analyse and integrate five publicly available datasets covering a total of 35 non-diabetic, 15 type 2 diabetic and 1 type 1 diabetic individuals using seurat v3.0 cca integration tools ( figure 1a , detailed donor information can be found in table s1 ) (segerstolpe et al., 2016; wang et al., 2016; xin et al., 2016; enge et al., 2017; lawlor et al., 2017; hafemeister and satija, 2019; stuart et al., 2019) . after filtering out low quality transcriptomes and data integration, uniform manifold approximation and projection for dimension reduction (umap) visualisation revealed that 7393 cells localize into distinct clusters ( figure 1b) . cells from each original dataset localize together suggesting that the location of cells on the umap is not driven by the dataset of origin ( figure 1c ). we next sought to identify pancreatic cell types ( figure 1d ). clustering analyses based on the expression of well-established cell type specific markers led to the identification of eight cell types in the human adult pancreas: beta, alpha, gamma, delta, acinar, ductal, stellate and endothelial cells ( figure 1b , table s2 ). umap visualization allowed for the segregation of endocrine, exocrine and other lineages ( figure s1a ). beta cells grouped together, away from other clusters and were marked by ins expression (figure 1e ). other distinct clusters corresponded to alpha, gamma and delta cells based on global transcriptional similarity and elevated expression of gcg, ppy and sst, respectively, and other markers ( figure 1e , table s2 ). using a similar approach, we reliably detected other, previously described, major pancreatic cell types (acinar, ductal, endothelial and stellate, figure 1b ). all cell types were detected in both non-diabetic and type 2 diabetic pancreases ( figure 1f ). an additional four rare cell populations, that cannot be robustly identified through clustering analyses, were identified manually by assessing the expression of ghrl (epsilon cells), tps1ab (schwann cells), cd86 (mast cells) and sox10 (major histocompatibility complex (mhc) class 2 cells) (wierup et al., 2002; segerstolpe et al., 2016) (figure 1g ). these rare cell types often cluster with other common cell types. importantly, our annotation recapitulated previous annotations to a large extent (figure s1b-c). in summary, we reconstructed an integrated single-cell atlas of the human adult pancreas, and annotated 12 pancreatic cell types. next, we set out to comprehensively reconstruct grns for all pancreatic cell types from single-cell transcriptomic data, applying single-cell regulatory network inference and clustering (pyscenic) (aibar et al., 2017; van de sande et al., 2020) . pyscenic links cis-regulatory sequence information together with single-cell transcriptomes in three sequential steps by 1) co-expression analysis, 2) target gene motif and chip-seq track enrichment analysis, and 3) regulon activity evaluation (figure 2a) . each regulon consists of a tf with its predicted target genes (co-expressed genes with an enriched tf motif), altogether forming a regulon. pyscenic identified 142 regulons that characterize the grns of the human adult pancreas 5 ( figure 2b /c, table s3 ). multiple regulons identified here as active in the pancreas correspond to tf binding motifs enriched in accessible chromatin in the pancreas (assessed by atac-seq in facs-purified pancreatic cells, (arda et al., 2018) ), supporting the validity of the approach ( figure s2a ). umap visualization based on the activity of 142 regulons in non-diabetic and type 2 diabetic pancreata revealed groups of cells that differ from one another based on their regulatory activity ( figure 2b -c). in particular, there are distinct regulatory states for exocrine and endocrine pancreatic lineages, stellate and endothelial cells (figure 2b /c). endocrine cell types clustered together, indicating shared regulatory states, while exocrine cell types formed two distinct clusters. stellate and endothelial cells differed most from other cell types in their regulatory states. these results are consistent with previous analyses (baron, veres, samuel l. wolock, et al., 2016; lawlor et al., 2017; kumar and vinod, 2019) and are also in line with our findings above based on gene expression analysis ( figure 1d ). as expected, regulons active in endocrine cell types include rfx6, pax6 and neurod1 ( figure 2d -g). these tfs have reported roles in endocrine cell fate commitment and maintenance of cell identity throughout adult life (smith et al., 2010; hart et al., 2013; mastracci et al., 2013) . using iregulon for visualization, many of the neurod1 target genes identified here have been previously linked to beta cell survival and function, such as snap25, tspan2, (gierl et al., 2006; haumaitre et al., 2008; hart et al., 2013; churchill et al., 2017) . clustering all cells based on the activity of all regulons identifies regulatory modules ( figure 2d , red squares). in the exocrine pancreas, one regulatory module, containing nr5a2, was shared between acinar and ductal cells, although with a tendency for increased regulon activity in ductal cells ( figure 2d /h). other exocrine regulons included onecut1, rest and hnf1b with reported roles in exocrine development (nissim et al., 2016; kropp, zhu and gannon, 2019) and the adult exocrine pancreas (quilichini et al., 2019; bray et al., 2020 ) ( figure 2d ). in summary, this analysis confirms the expected separation of exocrine and endocrine cells with distinct gene regulatory programs, and identifies known and novel candidate regulators of pancreas cell states. several regulatory modules are shared between different cell types within the endocrine and exocrine pancreas. additionally, each cell type is defined by cell-type specific regulatory modules ( figure 1d ). in the endocrine pancreas, alpha and beta cells shared endocrine regulons (mafb, meis2), whereas we observed distinct activities for arx and irx2 regulons in alpha cells and rxrg and pdx1 in beta cells ( figure 2d /h), expanding previous findings (kumar and vinod, 2019) . using iregulon for visualization, pdx1 target genes include slc6a17, pdia6 and abhd3, which have been reported to control insulin release (thomas, brown and brown, 2014; eletto et al., 2016; rorsman and ashcroft, 2018 ) ( figure s2c ). interestingly, gamma and delta cells overlapped with alpha and beta cells, respectively, suggesting a shared regulatory state ( figure 2c/d) . this includes shared regulon activity for arx in gamma and alpha and pdx1 in beta and delta cells ( figure 2d /h), consistent with their reported expression in published scrna-seq studies (baron et al., 2016; segerstolpe et al., 2016; lawlor et al., 2017) . gata4 and rbpjl, known acinar-specific tfs, were highly active in acinar cells (masui et al., 2010; carrasco et al., 2012) ( figure 2h) . similarly, ductal cells were characterised by highly active sox9 and pou2f3 regulons, in line with previous literature (shroff et al., 2014; yamashita et al., 2017) (figure 2h ). in sum, this analysis confirms that alpha, beta, acinar and ductal cells are defined by the activity of distinct tf combinations that form gene regulatory modules. in conclusion, the network approach recovers many of the expected regulators of pancreatic cellular identity allowing for the comprehensive characterisation of the gene regulatory state of all major human adult pancreatic cell types. a comprehensive network analysis provides an opportunity to predict and identify critical regulators of cell identity. to identify regulons with highly cell type-specific activities within the human adult non-diabetic pancreas, we calculated regulon specificity scores (rss) (a complete list of rsss can be found in table s4 ) (suo et al., 2018) . the rss utilises jensen-shannon divergence to measure the similarity between the probability distribution of the regulon's enrichment score and cell type annotation wherein outliers receive a higher rss and are therefore considered cell type-specific (suo et al., 2018) . it can therefore be used to rank the activity of tfs within specific cell types. among the top regulons identified in alpha cells, we recover well known regulators of alpha and endocrine cell fate such as arx, irx2, pax6, mafb, neurod1 and rfx6 ( figure 3a /b) (collombat et al., 2003; artner et al., 2006; delporte et al., 2008; smith et al., 2010; dorrell et al., 2011; mastracci et al., 2013) . in addition, we identified jund, egr4, srebf1 and stat4, which have not yet been implicated in alpha cell identity. egr1 (but not egr4) has been shown to transcriptionally regulate glucagon expression (leungtheung-long et al., 2005) as well as the pdx1 promoter in beta cells (eto, kaur and thomas, 2007) . stat4 and jund have been described in pancreatic tissue in general and beta cells, respectively, but not in alpha cells (yu and kim, 2012; good et al., 2019) (figure 3b /c). these tfs respond to the jnk and egfr signalling pathways and may have important physiological functions. both jund and the jund/jnk signaling pathway have been implicated in pancreatic cancer (shin et al., 2009; recio-boiles et al., 2016) . immunocytochemistry of the human adult pancreas confirmed the presence of nuclear jund in islets ( figure 3di ). we also detected nuclear jund protein in a subset of human induced pluripotent stem cells (ipscs) subjected to beta cell differentiation (figure 3e/f) . surprisingly, we also detected jund protein in ductal cells, despite lower jund regulon activity in this cell type (figures 3c, 3dii) . thus, protein 7 expression does not always predict regulatory activity. nevertheless, these results show that jund is present and active in a subset of pancreatic cell types in the human adult pancreas and human pluripotent stem cell derived islet cells. altogether, this analysis predicts tfs active in human alpha cells, recovering known as well as new candidate tfs. among the top regulons identified in beta cells, we retrieved well-known as well as new candidate regulators of beta and endocrine cell identity. known tfs include rxrg, pdx1, neurod1, pax6 and rfx6 (zhou et al., 2008; miyazaki et al., 2010; smith et al., 2010; mastracci and sussel, 2012; hart et al., 2013) (figure 3g /h). in addition, we found that znf705d, ascl2 and hoxd13 were highly ranked regulons ( figure 3h /i). hoxd13 and bhlhe41 have been shown to be present in the exocrine pancreas (cantile et al., 2009; sato et al., 2012) . interestingly, ascl2 has been reported to interact with β-catenin of the wnt pathway, the latter has an established role in endocrine fate specification during in vitro differentiation (schuijers et al., 2015; sharon et al., 2019; vethe et al., 2019) . many putative target genes of ascl2 including pdx1, ins, abcc8, foxa1, kcnk16, fxyd2 are directly related to glucose sensing and beta cell identity, in line with the beta cell-specific regulatory activity of ascl2 ( figure s3a ) (gao et al., 2010; arystarkhova et al., 2013; vierra et al., 2015; park, lee and park, 2016) . fxyd2γa, a regulatory subunit of the na + -k + -atpase, is a transcript exclusively expressed in human beta cells (flamez et al., 2010) . immunohistochemistry of human adult pancreas sections showed that ascl2 is expressed in ins + beta and islet cells ( figure 3j) . surprisingly, ascl2 was mainly localized to the cytoplasm ( figure 3j) , which is unexpected for tfs which tend to localize to the nucleus (baranek, sock and wegner, 2005) . cytoplasmic localization of ascl2 has been reported in the context of colon and breast cancer (zhu et al., 2012; xu et al., 2017) . these results implicate additional tfs including ascl2 in the regulation of beta cell identity. they also illustrate the value of network analyses to increase our understanding of the biology of the human pancreas. in summary, grn analysis and regulon ranking allowed us to pinpoint both known and novel candidate regulators of pancreatic endocrine cell identity, providing a resource for further investigation of their roles in cellular identity and function. similarly, the comprehensive network analysis provides an opportunity to predict and identify critical regulators of exocrine cell identity. we also identify known and new tfs in acinar cells. among the top acinar-specific regulons, we recovered well known regulators of acinar and exocrine cell identity such as ptf1a, rbpjl, gata4 and nr5a2 (ketola et al., 2004; masui et al., 2010; nissim et al., 2016; sakikubo et al., 2018) (figure 4a/b) . these findings are in line with a recent study that used single-nucleus rna-seq on pancreatic acinar tissue (tosti 8 et al., 2019) . furthermore, we identified mecom, heyl and tgif1 as highly ranked regulons ( figure 4b /c). interestingly, aberrant mecom expression has been linked to the induction of gastric genes in acinar cells, which disrupts acinar cell identity and increases susceptibility to malignancy (hoang et al., 2016) . the loss of tgif1 has been linked to pancreatic ductal adenocarcinoma progression making further exploration of these regulons interesting in the context of cancer biology (weng et al., 2019) . ectopic expression of tgif2 (but not tgif1) reprograms mouse liver cells towards a pancreas progenitor state (cerdá-esteban et al., 2017) . heyl is a reported notch signalling target gene in ngn3 + exocrine cells (gomez et al, 2015) . we confirmed nuclear expression of heyl in human acinar and islet cells (figure 4di /ii, detailed donor information can be found in table s1 ) by immunohistochemistry, in agreement with elevated heyl regulon activity in acinar cells ( figure 3c ). further functional studies in the healthy pancreatic context (matsumoto et al., 2004; coleman et al., 2013) . in summary, grn analysis and regulon ranking allowed us to pinpoint both known and novel candidate regulators of pancreatic exocrine cell identity. specifically, we identified heyl as a candidate tf that might be important for acinar cell identity, warranting further investigation. to enable users to easily navigate the human pancreatic cell network atlas, we provide a loom file that allows for the visualisation and exploration of the data using the web-based portal scope (davie et al., 2018) (.loom file and tutorial available at http://scope.aertslab.org/#/pancreasatlas/*/welcome and https://github.com/pasquelab/scpancreasatlas). features such as cell type annotation as defined in this paper, gene expression and regulon activity can be explored on the regulon and gene expression based umap. this resource enables users to select and visualize up to three genes or regulons simultaneously and select subsets of cells for downstream analyses. for example, the expression of covid-19 related genes can be interactively explored (yang et al., 2020) . target genes of a specific regulon can be downloaded to facilitate further exploration, for example in iregulon or gene ontology analysis (janky et al., 2014) . a list of predicted target genes of all 142 regulons can also be found in table s5 . furthermore, a list of target genes can be manually defined to compute the activity of a custom regulon. this resource can be used to further study cell identity and gene regulation in the context of the pancreas, diabetes and cancer. in this resource, we take advantage of integration strategies and new computational tools to reconstruct an integrated cell and grn atlas of the human adult pancreas from single-cell transcriptome data. this approach provides a comprehensive analysis of the gene regulatory logic underlying cellular identity in the human adult pancreas in a broad range of individuals, limiting the influence of inter-donor variability. we recovered known regulators of pancreatic cell identity and uncovered novel candidate regulators of cell identity that can be further investigated for their roles in cellular identity and function. by validating regulon analyses and creating an easily accessible interactive online resource which allows for the exploration of the gene regulatory state of 7393 cells from 51 individuals, this approach extends beyond previous gene regulatory studies in the human adult pancreas (augsornworawat and millman, 2020) . the present analysis identified regulators of pancreatic development, function and survival that are known to be critical in humans because loss-of-gene function causes pancreatic agenesis or young onset diabetes. for example, ptf1a (sellick et al., 2004; weedon et al., 2014) and gata4 (shaw-smith et al., 2014) , whose loss of function are linked to pancreatic agenesis and neonatal diabetes, were among the top acinarspecific regulons (figure 3 ). in addition, monogenic diabetes related genes pdx1 (nicolino et al., 2010 ), neurod1 (rubio-cabezas et al., 2010 , pax6 (solomon et al., 2009) , rfx6 (smith et al., 2010; patel et al., 2017) and glis3 (senée et al., 2006) were among the top beta cell-specific regulons (figure 3 and table s4 ). stress signalling (table s4) . creb3 and creb3l2 are non-canonical er stress transducers that are induced in human islets and clonal beta cells upon exposure to the saturated fatty acid palmitate (cnop et al., 2014) . interestingly, srebf1 and -2 undergo similar er exit and proteolytic processing in the golgi as these er stress transducers, but they do so in response to changes in er cholesterol content; both also have high regulon activity in alpha and beta cells. xbp1 is abundantly expressed in the exocrine and endocrine pancreas (cnop et al., 2017) , but the xbp1 regulon has its highest specificity in beta cells. atf3 and atf4 are tfs that are activated upon eif2α phosphorylation, an er stress response pathway to which no less than 5 monogenic forms of diabetes belong (eizirik, pasquali and cnop, 2020) . our data underscores the importance of these tfs for endocrine pancreatic cell identity. given that we predict novel regulators of cell identity in the human pancreas, it will be interesting to also expand this analysis to pancreas embryonic development. our work may also be beneficial in guiding improvements of and better understanding the in vitro derivation of pancreatic cell types. for example, the emergence of sst-positive cells together with beta-like cells at the end of in vitro differentiation could be explained by the overlap in regulatory states between beta and delta cells (baron et al., 2016) . grn analyses are particularly interesting for in vitro derived beta cells since a better understanding of the regulatory logic underlying control of beta cell fate may improve or facilitate future applications in regenerative medicine (pagliuca et al., 2014; rezania et al., 2014; nostro et al., 2015; russ et al., 2015; baeyens et al., 2018) . alternatively, many observed grns such as ascl2, mecom, ppard, gata6 and cdx2 are linked to pancreatic cancer making the additional exploration of grns interesting in the context of cancer biology (matsumoto et al., 2004; zhu et al., 2012; coleman et al., 2013; hoang et al., 2016; xu et al., 2017; weng et al., 2019; brunton et al., 2020) . finally, recent reports have stratified type 2 diabetes patients based on age at diagnosis, bmi, hba1c and insulin secretion and sensitivity, and identified subtypes with different genetic predisposition, treatment response, disease progression and complication rates (ahlqvist et al., 2018) . hence, it would be interesting to assess differences in gene regulatory state and gene expression profiles of alpha and beta cells between different type 2 diabetic subgroups. it is important to note that pyscenic is a stochastic algorithm that does not produce precisely the same regulons for repeated applications, limiting reproducibility when comparing different datasets (huynh-thu et al., 2010; van de sande et al., 2020) . to mitigate this uncertainty, we ran the full pyscenic pipeline five times and only kept consistent regulons with the highest regulon activity. the performance of pyscenic, and other grn inference methods, suffers due to the large amount of drop-out events in scrna-seq data warranting caution when interpreting results (chen and mar, 2018) . this could explain the absence of wellestablished pancreas tfs such as mafa (olbrot et al., 2002) , mnx1 (flanagan et al., 2014) , neurog3 (krentz et al., 2017) , foxa2 (lee et al., 2002) and nkx2-2 (mastracci et al., 2011) in this analysis. nevertheless, in support of the validity of our findings, atac-seq, literature and immunohistochemistry of human pancreas sections corroborate several pyscenic predictions. chen and colleagues underline the importance of using large sample sizes to derive the most accurate network inference possible (chen and mar, 2018) , highlighting the importance of dataset integration to increase the number of cells analysed. in the future, it will be interesting to extend our analyses to include many more cells and patients. in spite of current caveats, grn analysis has enabled the capture of biological relevant information (butte et al., 2000) . one additional limitation of this study is the assumption that all tfs bind their binding motifs in the promoters of expressed genes. however, tf binding can be restricted to a subset of tf motifs in the genome due to influence of chromatin processes including the presence of nucleosomes as well as dna methylation. therefore, additional approaches such as single cell multi-omics that capture additional layers of genome regulation will be helpful to increase our understanding of gene regulation in the context of the human pancreas. taken together, our grn atlas, containing 51 individuals, provides a valuable resource for future studies in the human pancreas development, donor variability, homeostasis and disease including type 2 diabetes 11 and pancreatic cancer. finally, our results provide new insights into the activity of tfs and gene regulation in the human adult pancreas from a gene regulatory perspective. questions about data analysis should be directed to the lead contact, vincent pasque (vincent.pasque@kuleuven.be). the reviewer tokens for this geo repository is cfsjciumfferjkd. motif discovery of bulk atac-seq data paired-end raw reads for bulk atac-seq (see key resource table) were downloaded from sra using sra toolkit (v2.9.4). reads were aligned and further analyzed using the encode atac-seq pipeline with default parameters using the encode human reference genome grch38.15 (lee, 2016) . bed files containing the global open chromatin landscape of adult alpha (alpha_1; ea4 and alpha_2; ea28), beta (beta_1; ea5 and beta_2; ea29), acinar (acinar_1; ea7 and acinar_2; ea27) and ductal (ea11) cells or cell type specific differentially accessible regions were used as input for motif discovery by homer (v4.10.4) using the 'findmotifsgenome.pl' with options using hg38 with size given (heinz et al., 2010) . the tfs whose motifs identified by homer correspond with tfs identified by pyscenic are visualized in figure s2a . analysis of publicly available scrna-seq data raw reads for five publicly available scrna-seq datasets (see key resource table) were downloaded from sra using sra toolkit (v2.9.4). afterwards, reads were aligned to the human reference genome grch38.95 using star (v2.5.3a) with default parameters followed by the conversion to the coordinate sorted bam format. next, the featurecounts command from the "rsubread" (v1.5.2) package in r (v3.6.1) was used to assign mapped reads to genomic features. low quality transcriptomes with a mitochondrial contamination greater than 5% and less than 200 expressed genes per cell were excluded from subsequent analyses. the resulting raw count matrix was batch corrected using the findintegrationanchors and integratedata functions from the "seurat" package (v3.1.1) after which subsequent analyses were carried out in the r package "seurat" (v3.1.4). gene expression was used to cluster all 7393 cells with umap, using seurat's function runumap. clusters for cell type annotation were defined using seurat's shared nearest neighbour algorithm findclusters function after which differential expression analysis was performed using wilcoxon's rank sum test with a minimum cutoff of 0.25 average log fold change and min.pct of 0.25. pyscenic grns were inferred using pyscenic (python implementation of scenic, v0.9.15) in python version 3.6.9 (aibar et al., 2017) . integrated read counts were used as input to run genie3 (huynh-thu et al., 2010) which is part of arboreto (v0.1.5). grns were subsequently inferred using pyscenic with the hg38_refseq-r80 motif database and default settings. to control for the stochasticity, which is inherent to pyscenic, a consensus grn was generated by merging results from five repeat pyscenic runs. if regulons were identified in multiple pyscenic runs, only the regulon with the highest auc value was retained. regulon activity represented by aucell values was used to cluster all 7393 cells with umap, using seurat's runumap function. all 142 regulons within non-diabetic cell types were visualized using the 'clustermap' function of the python package "seaborn" (v0.9.0). the z-score for each regulon across all cells was calculated using the z-score parameter of the seaborn 'clustermap' function. extended analysis of the target genes of specific regulons was conducted in cytoscape (v3.7.1) using the iregulon application (v1.3). the list of target genes of a specific regulon was downloaded from the loom file through the scope platform (https://github.com/pasquelab/scpancreasatlas) (davie et al., 2018) . to quantify the cell-type specificity of a regulon, we utilized an entropy-based strategy as described previously (suo et al., 2018) using the aucell matrix as input in matlab r2019b. the top 10 most specific regulons were subsequently visualized using the r package ggplot2 (v3.1.1). the complete regulon ranking list is available in table s2 . control ipsc line hel115.6 (cosentino et al., 2018) was differentiated into beta cells using a previously published 7-step protocol (cosentino et al., 2018) . at the end of the stage 4, cells were seeded into 24-well aggrewell 400 microwell plates (stem cell technologies) at a density of 0.9 ·10 6 cells per well after which differentiation was carried out as described previously (cosentino et al., 2018) . stage 7 differentiated beta cells were washed twice with pbs containing 0.5 mm edta and incubated in accumax (sigma #a7089) for 8 min at 37 °c after which 50% volume of knockout serum replacement (thermofisher #10828028) was added to stop the reaction. after centrifugation at 400 g for 5 min at room temperature, cells were resuspended in 1 ml ham's f-10 medium, supplemented as indicated before (demine et al., 2020) . 75,000 cells in 500 μl medium were seeded per square of a nunc lab-tek ii icc chamber (thermofisher). immunohistochemistry analyses were carried out largely as described previously (demine et al., 2020) , immunohistochemistry analyses were carried out largely as described previously (ceulemans et al., 2017) , using primary antibodies against the following proteins: ascl2 (merck, mab4418, clone 7e2, 1/5000), jund (atlas antibodies, hpa063029, 1/50), heyl (atlas antibodies, hpa076960, 1/200) and ins (agilent, ir002, 1/100). pictures were taken using a leica dmlb (leica microsystems). the integrated single-cell rna-seq data and pyscenic results can be explored interactively in scope (davie et al., 2018) . loompy (v2.0.17) (linnarsson lab., 2015) was used to create the loom files which were uploaded to scope. the embedding of the regulon and integrated gene expression based umap clustering, as seen in this article, were added to the loom file. this table is related to figure 1 , 2, 3 and 4. this table is related to figure 1 . this table is related to figure 2 , 3 and 4. list of regulon specificity scores for all 142 regulons of non-diabetic alpha, beta, acinar and ductal cells. this table is related to figure 3 and 4. list of putative target genes for each regulon. this table is related to figure 2 , 3 and 4. novel subgroups of adult-onset diabetes and their association with 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reveals type 2 diabetes genes elevated ascl2 expression in breast cancer is associated with the poor prognosis of patients skn-1a/pou2f3 functions as a master regulator to generate trpm5-expressing chemosensory cells in mice a human pluripotent stem cell-based platform to study sars-cov-2 tropism and model virus infection in human cells and organoids role of janus kinase/signal transducers and activators of transcription in the pathogenesis of pancreatitis and pancreatic cancer risk of diabetes-associated diseases in subgroups of patients with recent-onset diabetes: a 5-year follow-up study', the lancet diabetes and endocrinology in vivo reprogramming of adult pancreatic exocrine cells to β-cells' ascl2 knockdown results in tumor growth arrest by mirna-302b-related inhibition of colon cancer progenitor cells genome editing of lineage determinants in human pluripotent stem cells reveals mechanisms of pancreatic development and diabetes we thank stein aerts, kristofer davie and the stein aerts lab for discussions and creating the permanent scope link, shengbao suo for sharing the matlab script for calculating the regulon specificity score, the key: cord-001273-plz1ja2e authors: dussurget, olivier; bierne, hélène; cossart, pascale title: the bacterial pathogen listeria monocytogenes and the interferon family: type i, type ii and type iii interferons date: 2014-04-28 journal: front cell infect microbiol doi: 10.3389/fcimb.2014.00050 sha: doc_id: 1273 cord_uid: plz1ja2e interferons (ifns) are secreted proteins of the cytokine family that regulate innate and adaptive immune responses to infection. although the importance of ifns in the antiviral response has long been appreciated, their role in bacterial infections is more complex and is currently a major focus of investigation. this review summarizes our current knowledge of the role of these cytokines in host defense against the bacterial pathogen listeria monocytogenes and highlights recent discoveries on the molecular mechanisms evolved by this intracellular bacterium to subvert ifn responses. listeria monocytogenes is a pathogenic gram-positive bacillus responsible for a foodborne disease in humans and animals called listeriosis (vázquez-boland et al., 2001) . this highly versatile bacterium can be isolated from multiple sources such as human and animal feces, soil, water, plants and food. as a common contaminant of fruits, vegetables, seafood, meat and cheese, it represents a major economic problem for the food industry. infection usually originates from ingestion of contaminated food (schlech et al., 1983) and may cause febrile gastroenteritis in otherwise healthy persons (ooi and lorber, 2005) . in contrast, in immunocompromised individuals it leads to a severe invasive disease, which manifests itself as septicemia, meningitis and encephalitis. in the specific case of pregnant women, infection may cause fetal loss or neonatal bacteremia and meningitis. in the united states, incidence of listeriosis ranged from 2.5 to 3.2 cases per million population between 2004 and 2009 (cartwright et al., 2013) . in france, incidence was 3.9 per million between 2001 and 2008, and increased risk of listeriosis was noticed in people with underlying diseases, such as chronic lymphocytic leukemia (goulet et al., 2012) . while relatively rare, listeriosis is among the most deadly foodborne diseases with mortality rates reaching up to 50% depending on the clinical manifestations (lorber, 1997) . in addition to the immunological status of the patient, the clinical outcome of the disease depends on the pathogenic potential of the infecting bacteria. l. monocytogenes strains of serovars 1/2a, 1/2b, and 4b account for 95% of human cases and serovar 4b alone is associated to most outbreaks (swaminathan and gernersmidt, 2007) . the capacity of l. monocytogenes to survive and multiply within the gastrointestinal tract is critical for the initial infection, persistence and transmission. l. monocytogenes is well adapted to this environment and produces multiple factors to compete with microbiota and counteract antimicrobial peptides, acidity, hyperosmolarity, hypoxia, bile and iron deprivation (gahan and hill, 2005) . crossing of the intestinal epithelium is thought to occur by invasion of enterocytes, in particular goblet cells and m cells of the peyer's patches. invasion of enterocytes requires the specific interaction between the listeria surface protein inla and its cellular receptor e-cadherin (lecuit et al., 2001; disson et al., 2008) , which can take place at sites of cell extrusion at the tip and other locations of intestinal villi (pentecost et al., 2006; nikitas et al., 2011) . indeed, as recently shown, upon interaction with e-cadherin, listeria preferentially crosses the intestinal barrier by transcytosis through goblet cells (nikitas et al., 2011) . entry through ileal peyer's patches via m cells does not rely on inla. it has been reported to require listeria invasion protein inlb (chiba et al., 2011) . after translocation, bacteria reach lymph nodes, the liver and spleen and finally secondary target sites of infection, including the central nervous system and the placenta. a remarkable feature of l. monocytogenes is its capacity to invade non-professional phagocytic cells such as enterocytes, hepatocytes and trophoblast cells. the exceptional repertoire of virulence factors necessary for entry, survival and multiplication has been extensively studied cossart, 2011) . expression of many virulence genes relies on the transcriptional activator prfa, whose role is pivotal for l. monocytogenes transition from saprophytic to intracellular lifestyle (freitag et al., 2009; toledo-arana et al., 2009) . elimination of l. monocytogenes is mostly based on the capacity of the host to mount an efficient cellular immune response to infection (mackaness, 1962; shi and pamer, 2011) . in particular, the fate of infection depends on the level of macrophage activation and on listeria ability to counteract bactericidal mechanisms of host cells (shaughnessy and swanson, 2007; corr and o'neill, 2009; stavru et al., 2011) . bacterial escape from the phagosome and avoidance of autophagy for intracytosolic replication and cell-cell spread have been well characterized. they have been shown to depend on five major virulence factors: the secreted pore-forming toxin listeriolysin o (llo) and two phospholipases c (plca and plcb) for vacuolar escape, the surface protein acta for actin-based motility and both acta and a surface protein of the internalin family, inlk, for autophagy evasion (cossart, 2011; dortet et al., 2012) . other strategies of immune escape that lead to the modulation of cytokine expression occur through a variety of mechanisms. modifications of l. monocytogenes peptidoglycan by the n-deacetylase pgda and the o-acetyl transferase oata prevent lysozyme-dependent release of microbe-associated molecular patterns (mamps), activation of pathogen-recognition receptors (prrs) and subsequent production of pro-inflammatory cytokines (boneca et al., 2007; aubry et al., 2011; rae et al., 2011) . the toxin llo induces dephosphorylation of histone h3 and deacetylation of histone h4, which correlate with decreased expression of pro-inflammatory genes, such as the chemokine gene cxcl2 (hamon et al., 2007) . the secreted internalin inlc inhibits inflammation by interacting with ikk-α, a component of the iκb-kinase complex, which is essential for nf-κb activation and expression of proinflammatory genes (gouin et al., 2010) . other evasion mechanisms remain to be characterized, such as the control of the expression of il-6 by the surface internalin inlh (personnic et al., 2010) . l. monocytogenes also has the capacity to modulate interferon (ifn) production during infection. type i ifn production by infected cells can be controlled by listeria multidrug efflux pumps mdrm and mdrt, via the secretion of the second messenger cyclic-di-amp (crimmins et al., 2008; woodward et al., 2010; schwartz et al., 2012) . synthesis of type iii ifn has also recently been shown to be tuned by listeria nucleomodulin lnta (lebreton et al., 2011) . our knowledge concerning the role of the ifn cytokine family during listeriosis has rapidly expanded in the last few years and will be the focus of this review. ifns form a family of proteins secreted by many cell types in response to infection. they were originally named for their capacity to interfere with viral proliferation (isaacs and lindemann, 1957) . this diverse family is composed of three groups of cytokines, namely type i-, type ii-, and type iii-ifns, which are important components of innate immune responses ( table 1) . type i-ifns consist of ifn-α, ifn-β, ifn-δ, ifn-ε, ifn-ζ, ifnκ, ifn-ν, ifn-τ, and ifn-ω (levy et al., 2011) . type ii-ifn is composed of a single cytokine, ifn-γ (pestka et al., 2004) . type iii-ifns are ifn-λ1, ifn-λ2, and ifn-λ3 (formerly il-29, il-28a, and il-28b) and ifn-λ4 (kotenko, 2011; prokunina-olsson et al., 2013) . type i-and type iii-ifns have similar signal transduction systems (see below) and are phylogenetically closer from each other than type ii-ifn (pestka et al., 2004) . sequence conservation and chromosome location suggest that type i-ifn genes evolved from a single ancestor through duplication. however, the extent of type i-ifn gene diversification varies greatly depending on the species (pestka et al., 2004) . generally, a single gene encodes the type i-ifn in fish. in contrast, multiple gene duplications and diversification led to the emergence of sub-types of type i-ifns in mammals ( table 1) . gene duplication varies also within each sub-type. a single ifn-β gene is found in the human and mouse genomes (decker et al., 2005; honda et al., 2006; durbin et al., 2013) . in contrast 13 ifn-α genes and one pseudogene and 14 ifn-α genes and three pseudogenes are found in the human and mouse genomes, respectively (van pesch et al., 2004; durbin et al., 2013) . a single gene encodes type ii-ifn and four genes encode type iii-ifns in human (decker et al., 2005; levy et al., 2011) . of note, ifn-λ1 and ifn-λ4 are pseudogenes in mice, which prevents the study of these cytokines in this animal model ( table 1 ) (fox et al., 2009 ). ifns are important components of the immune system, which generally trigger cellular protective defenses in response to infection or tumor formation. type-ii ifn (ifn-γ) is a paradigm for this, being an important mediator of innate and adaptive immune responses with a key role in clearance of viral and bacterial pathogens and in tumor control. ifn-γ was first described as an antiviral protein (wheelock and sibley, 1965) , but is now known to exhibit broader biological activities, non-redundant with that of other types of ifns. the crucial role of ifn-γ in immunity to infection is reflected by the phenotype of mice lacking the ifn-γ receptor or the ifn-γ gene, which are highly susceptible to mycobacterium bovis bcg infection (dalton et al., 1993; kamijo et al., 1993) . genetic deficiencies resulting in the loss of ifn-γ production or signaling in mice lead to increased susceptibility to infections by other intracellular pathogens, such as l. monocytogenes (see below), salmonella typhimurium and some viruses harty and bevan, 1995; jouanguy et al., 1999) . these defects also lead to the loss of tumor control (kaplan et al., 1998) . patients with deficiencies in the ifn-γ pathway, for instance by mutation in the gene for the ifn-γ receptor 1, are characterized by severe infections with viruses and intracellular bacteria including l. monocytogenes, salmonella sp. and mycobacteria (jouanguy et al., 1996; newport et al., 1996; roesler et al., 1999; van de vosse et al., 2009) . ifn-γ mediates macrophage activation, i.e., increased phagocytosis and production of pro-inflammatory cytokines, of microbicidal reactive oxygen and nitrogen species, leading to clearance of intracellular pathogens (schoenborn and wilson, 2007) . in addition, ifn-γ controls differentiation of t cells in th1 effector cells, antigen processing and presentation by antigen-presenting cells, which participate to cellular immunity against intracellular pathogens (schroder, 2003; hu and ivashkiv, 2009 ). the immunostimulatory and immunomodulatory properties of ifn-γ have therapeutic implications. indeed, ifn-γ is used in patients with chronic granulomatous disease to reduce infection and mortality, **protein length in amino-acids and protein modifications (g: glycosylation, p: phosphorylation). ***13 genes and a pseudogene in the human genome, 14 genes and three pseudogenes in the mouse genome. although the clinical benefit has not been demonstrated in all studies (holland, 2010) . type i-ifns are produced in responses to viruses, many bacteria and parasites. however, in contrast to type ii ifns, these cytokines are not always protective against bacterial infections. indeed, the role of type i-ifns in response to bacterial infection is complex and depends on the microorganism (decker et al., 2005; monroe et al., 2010; carrero, 2013) . they contribute to resistance of the host against infection by extracellular bacteria, such as escherichia coli, helicobacter pylori, streptococcus agalactiae and s. pneumoniae (mancuso et al., 2007; watanabe et al., 2010) . in contrast, they are associated with suppression of innate immune responses and increased susceptibility of the host to infection by l. monocytogenes (see below), brucella abortus, chlamydia muridarum, francisella novicida, salmonella enterica, staphylococcus aureus, and yersinia pestis (auerbuch et al., 2004; carrero et al., 2004; o'connell et al., 2004; qiu et al., 2008; martin et al., 2009; henry et al., 2010; de almeida et al., 2011; patel et al., 2012; robinson et al., 2012; archer et al., 2014) . these different effects on infection are likely linked to the wide range of cellular responses induced by their downstream effectors, the products of ifn-stimulated genes (isgs) (schoggins et al., 2011) . although type i-ifns have long been known to induce antiviral response in the infected host (isaacs and lindemann, 1957) , they can also induce apoptosis, autophagy, differentiation and migration, inhibit proliferation as well as angiogenesis and mediate cellular damage, inflammation or autoimmunity (trinchieri, 2010) . as a result, type i-ifns have a therapeutic potential that can be used to treat tumors and viral infections (pestka, 2007; heim, 2013; wilson and brooks, 2013) , while being detrimental for the host in response to a subset of pathogens. type iii-ifns have been discovered in 2003 (kotenko et al., 2003; sheppard et al., 2003) and their activities have been less extensively characterized than those of type i-and type ii-ifns. however, several studies suggest that type i and type iii-ifns share common biological activities (levy et al., 2011; zheng et al., 2013) . although type iii-ifns respond to different stimuli, use different receptors and are not always expressed by the same cells as type i ifns (see below), engagement of type i-and type iii-ifn receptors leads to similar transcriptional responses. like type i-ifns, type iii-ifns have been involved in antiproliferative and antiviral responses (iversen and paludan, 2010; mordstein et al., 2010; durbin et al., 2013; hamming et al., 2013) . recently, type iii-ifns have been shown to be induced in response to bacterial pathogens, but their downstream effects are not yet characterized (pietilä et al., 2010; lebreton et al., 2011; bierne et al., 2012) . transcription of ifn genes is induced rapidly in response to microbial infection. type i-ifns can be produced by all cells, while type iii-ifns are secreted by specific cell types, including dendritic and epithelial cells. type i-and type iii-ifns activation is initiated by detection of mamps by prrs such as endosomal transmembrane toll-like receptors and cytosolic receptors (stetson and medzhitov, 2006; monroe et al., 2010) . upon recognition of mamps, prrs trigger diverse signaling pathways that involve adaptor proteins and cytosolic or organelle-bound protein scaffolds activating kinases converging to phosphorylation of transcription factors and their subsequent translocation into the nucleus (figure 1) . irf1, irf3, irf4, irf5, irf7, and irf8 are important for transcription of the ifn-α genes, with irf7 considered as the master regulator of ifn-α response (honda et al., 2005; tailor et al., 2007; levy et al., 2011) . regulation of the ifnβ gene is more complex. activated irf3, irf7, ap-1, and nf-κb bind to the enhancer/promoter regions of the ifn-β gene and participate to the formation of the enhanceosome, which alters chromatin structure and allows transcription (panne et al., 2007; panne, 2008) . in contrast, irfs and nf-κb independently activate transcription of type iii-ifn genes (iversen and paludan, 2010) . regulation of the ifn-γ gene expression is different from that of type i and type iii-ifn genes. nk cells and nkt cells are effectors of the innate immune response and primary sources of ifn-γ. mature nk and nkt cells quickly react to infection by inducing ifn-γ secretion. upon recognition of ligands expressed on infected cells, nk cell activating-receptors trigger signaling cascades involving adaptor proteins and protein tyrosine kinases leading to activation of ras/sos, plc-γ and mapk pathways and induction of ifn-γ production (schoenborn and wilson, 2007) . in addition to receptors, il-2, il-15, il-12, il-18, and type i-ifns also contribute to induction of ifn-γ production by nk cells (newman and riley, 2007; schoenborn and wilson, 2007; marçais et al., 2013) . similarly, il-12 and il-18 induce ifn-γ production by nkt cells (godfrey and berzins, 2007) . in nk and nkt cells, the ifn-γ gene locus is transcriptionally permissive within accessible chromatin and allows rapid ifn-γ expression upon activation of transcription factors, such as ap-1, nf-κb, stat4, and t-bet (glimcher et al., 2004; schoenborn and wilson, 2007; lazarevic et al., 2013) . in addition, naive cd4 and cd8 t cells can differentiate into th1 cd4 effector t cells and cd8 cytotoxic t lymphocytes capable of ifn-γ secretion (wilson et al., 2009) . ifn-γ production by cd4 and cd8 t cells depends on il-12, il-18 and ifn-γ itself and share many signaling pathways with nk cells. multiple transcription factors act at the ifn-γ promoter, e.g., ap-1, atf-2/c-jun, c/ebp, eomes, ets-1, nfat, nf-κb, runx3, stats and t-bet (schoenborn and wilson, 2007; samten et al., 2008; wilson et al., 2009; lazarevic et al., 2013) . moreover, distal regulatory elements modify the chromatin and remodel the ifn-γ gene locus to facilitate ifn-γ production (wilson et al., 2009 ). ifns are rapidly secreted upon infection and then bind to their receptors on the surface of target cells (table 1) . type i-ifns bind the ubiquitous ifnar receptor, which consists of two chains, ifnar1 and ifnar2 (piehler et al., 2012) . type iii-ifns bind and signal through a different receptor complex, made of two chains: ifnlr1 (also known as il-28rα) and il10r2. this receptor is expressed primarily by epithelial cells and hepatocytes (iversen and paludan, 2010) . thus, the physiological roles of type i-and type iii-ifns are distinct because of the different distribution of their receptors in tissues, type iii-ifns acting predominantly at mucosal surfaces (mordstein et al., 2010; durbin et al., 2013) . type i-and type iii-ifns use different receptors but trigger the same jak-stat signal transduction cascade involving tyk2, jak1, stat1, and stat2 albeit with different kinetics (figure 2 ) (marcello et al., 2006) . ultimately, stat1, stat2, and irf9 form a transcription factor complex, referred to as isgf3, which translocates to the nucleus and binds to ifn-stimulated responsive elements (isre) in the promoter of isgs (schindler et al., 2007) . type ii-ifn, uses a heterodimeric receptor consisting of ifnγr1 and ifnγr2 chains, expressed by many cell types (bach et al., 1997) . ifn-γ activates jak1, jak2 and stat1, leading to transcription of genes bearing a γ-activation sequence (gas) in their promoter (figure 2 ) (schindler et al., 2007) . mamps activate prrs of host cells such as epithelial cells and macrophages (figure 1) . infection induces a robust type i-ifn response. in mice, macrophages have been identified as the major source of ifn-β (stockinger et al., 2009) . in vitro, ifn-β production by bone-marrow-derived murine macrophages has been shown to require bacterial escape from the phagosome and activation of cytosolic surveillance pathways (o'riordan et al., 2002) . induction of ifn-β depends on the adaptor protein sting and the cytosolic prr ddx41, which are activated by bacterial secondary messengers c-di-amp and c-di-gmp and by bacterial dna (woodward et al., 2010; burdette et al., 2011; sauer et al., 2011; parvatiyar et al., 2012; archer et al., 2014) . sting is a direct receptor for cyclic-dinucleotides, including the cellular second messenger cyclic gmp-amp (cgamp) which is produced by the cytosolic sensor cgamp synthase (cgas) upon interaction with microbial dna (ablasser et al., 2013; gao et al., 2013; wu et al., 2013; sun et al., 2013; schoggins et al., 2014) . interestingly, type i-ifn production requires activation of the rig-i helicase by listeria rna in non-immune cells lacking a functional sting signaling pathway (abdullah et al., 2012; hagmann et al., 2013) . another cytosolic prr, the leucine-rich repeat-containing protein lrrfip1, has also been implicated in ifn-β production by mouse primary peritoneal macrophages in response to listeria infection, possibly by sensing double stranded dna and rna (yang et al., 2010) . while production of ifn-β in response to listeria infection is independent from tlrs in bone-marrowderived macrophages (mccaffrey et al., 2004; stockinger et al., 2004; o'connell et al., 2005) , tlr-2 contributes significantly to ifn-β secretion by peritoneal macrophages, suggesting that specific macrophage populations have evolved different recognition strategies in response to listeria infection (aubry et al., 2012) . listeria infection has recently been shown to induce type iii-ifn gene expression in cells of epithelial origin, such as intestinal and trophoblast cells and hepatocytes (lebreton et al., 2011; bierne et al., 2012) . similar to type i-ifn, type iii-ifn induction is triggered by intracellular listeria . listeria infection also triggers a rapid and robust ifn-γ response. after intravenous infection of mice with l. monocytogenes, nk and t cells are the main sources of ifn-γ (thale and kiderlen, 2005; bou ghanem et al., 2009) . ifn-γ producing v1δ + -γδ t cells are other murine immune cells induced at an early stage of listeria infection in mice inoculated intraperitoneally (hamada et al., 2008) . using oral infection of mice, the natural route of infection in permissive hosts, l. monocytogenes has been shown to induce ifn-γ production by intraepithelial lymphocytes of the small intestine (okamoto, 1994) . more recently, human e-cadherin (hecad) expressing mice, a mouse line permissive for listeria oral infection (lecuit et al., 2001) , were used to study cells involved in intestinal mucosal immunity. infection induced ifn-γ production in nk cells of the small intestine (reynders et al., 2011) . the production of ifn-γ by immune cells promotes bacterial clearance and is thus critical in controlling primary l. monocytogenes infections (zenewicz and shen, 2007) . injection of neutralizing monoclonal anti-ifn-γ antibodies in mice infected intraperitoneally with l. monocytogenes inhibits macrophage activation and increases the mortality rate (buchmeier and schreiber, 1985) . in addition, resistance of ifn-γ gene or ifn-γ receptor knock-out mice infected intravenously with l. monocytogenes is frontiers in cellular and infection microbiology www.frontiersin.org april 2014 | volume 4 | article 50 | 6 severely impaired harty and bevan, 1995) . recent work using cell-type specific inactivation of stat1 in mice elegantly demonstrated the key role of ifn-γ and stat1 in macrophage activation and clearance of listeria (kernbauer et al., 2012) . interestingly, the role of stat1 was extremely different after infection of immunized mice. stat1 signaling in t cells and dendritic cells was critical for adaptive immunity to listeria, while ifn-γ-activated macrophages were not essential anymore once memory cells were produced. upon oral infection of hecad mice with listeria, ifn-γ contributes to the control of bacterial burden in the intestine and of bacterial dissemination to other organs. for instance, blocking ifn-γ with neutralizing antibodies increases listeria load in the small intestine, the mesenteric lymph nodes and in the spleen of mice infected orally (reynders et al., 2011) . in contrast to ifn-γ, type i-ifn is beneficial to l. monocytogenes. mice lacking type i-ifn receptor or irf3 are more resistant to listeria intraperitoneal or intravenous infection (auerbuch et al., 2004; carrero et al., 2004; o'connell et al., 2004; garifulin et al., 2007; jia et al., 2009) . the role of type i-ifns in increasing host susceptibility could be explained by modulation of components of the immune response involved in controlling bacterial growth such as induction of t cell apoptosis, resulting in greater il-10 secretion by phagocytic cells, in turn dampening the innate immune response (carrero and unanue, 2006) , the downregulation of ifn-γr (rayamajhi et al., 2010; kearney et al., 2013) , or neutrophil recruitment (brzoza-lewis et al., 2012) . as shown recently, sting-dependent activation of type i-ifn reduces the adaptive immune response to l. monocytogenes (archer et al., 2014) . in contrast, recent studies showed that type i-ifns can also play a beneficial role for the host during listeria infection, pointing to the infection route and the timing of type i-ifn production as determinative factors (pontiroli et al., 2012; kernbauer et al., 2013) . interestingly, different strains of l. monocytogenes have been shown to vary greatly in their capacity to induce ifn-β (reutterer et al., 2008; schwartz et al., 2012) . the lo28 strain hyperinduces ifn-β (reutterer et al., 2008) . this strain bears a nonfunctional brta (also named tetr), the transcriptional repressor of the multidrug efflux pump mdrt (schwartz et al., 2012; yamamoto et al., 2012) . in listeria, mdrt allows secretion of cdi-amp, which triggers ifn-β. thus, derepression of mdrt in the lo28 strain promotes ifn-β production. of note, high expression of mdrt in lo28 correlates with both induction of ifn-β and lower virulence. another listeria multidrug resistance transporter, mdrm, has been involved in the stimulation of ifn-β production, possibly by secreting c-di-amp (crimmins et al., 2008; woodward et al., 2010; witte et al., 2012) . the role of type iii-ifns during listeriosis remains to be determined. since listeria colonizes several tissues of epithelial origins, such as the liver, intestine and placenta, it is tempting to speculate that ifn-λs play a role in the interaction of listeria with epithelia. however, a prerequisite to address this question is the establishment of a new animal model, i.e., a mouse line expressing a human e-cadherin, thus permissive for listeria infection of epithelia (lecuit et al., 2001) and impaired in type iii-ifn responses, such as il28rα knockout mice (mordstein et al., 2010) . one should keep in mind that the mouse model is not optimal to address the role of type iii-ifn in human listeriosis. indeed, ifn-λ1 is a pseudogene in mice, while human cells produce this cytokine upon infection with l. monocytogenes. in addition, the type iii-ifn receptor is expressed at very low levels in the mouse liver and the ifn-λ response of the mouse liver is very weak (mordstein et al., 2010) . in line with this, it has been recently shown that mouse hepatocytes, in contrast to human hepatocytes, are not responsive to ifn-λ (hermant et al., 2014) . the beneficial or detrimental effects of ifns on listeria infection rely on the functional properties of their downstream effectors. indeed, ifns elicit expression of hundreds of interferonstimulated genes (isgs), which encode proteins involved in a broad range of cellular functions (reviewed in macmicking, 2004) . however, while about 2,000 isgs have been identified so far (rusinova et al., 2012) , their functions in immunomodulation remain to be characterized. to date, the contribution of interferon-induced proteins on listeria infection has mostly been studied in the context of the ifn-γ pathway. the antilisterial activity of ifn-γ in phagocytic cells involves induction of oxidative and nitrosative defences, via increased expression of enzymes that control production of reactive oxygen and nitrogen species, such as nox2/cybb, duox2, and inos/nos2 (macmicking, 2012). these enzymes play an important role in protecting infected cells against listeria cytoinvasion (myers et al., 2003; lipinski et al., 2009) . the assembly of these enzymes requires ifn-γ-inducible guanosine triphosphatases (gtpases) of the gbp (guanylate binding protein) family (boehm et al., 1998) , which not only participate to oxidative pathways but also regulate autophagy (kim et al., 2011) . several gbps have been shown to protect cells from listeria infection by coordinating a potent oxidative and vesicular trafficking program (kim et al., 2011) . ifn-γ also induces the expression of many nuclear genes encoding mitochondrial respiratory chain machinery, via activation of the nuclear receptor errα (estrogen-related receptor α). errα contributes to mitochondrial ros production and efficient clearance of l. monocytogenes (sonoda et al., 2007) . a family of ifn-γ-induced chemokines (cxcl9, cxcl10, cxcl11) displays direct antimicrobial activity against l. monocytogenes (cole et al., 2001) . in dendritic cells, one of the ifn-γ-associated isgs is the immunoregulatory enzyme indoleamine 2,3-dioxygenase (ido), a key enzyme of the tryptophan metabolism. ido is proposed to play a role in the containment of listeria within granulomatous structures, thus avoiding massive t cell activation (popov et al., 2006) . the function of type i ifn-associated isgs in listeria infection is less documented. zwaferink et al. have observed that upregulation of inos/nos2 by ifn-β promotes necrotic death of macrophages (zwaferink et al., 2007) . additionally, several interferon-inducible proteins belong to inflammasomes; thus, type i ifn may potentiate inflammasome activation and cell death by pyroptosis (malireddi and kanneganti, 2013 ). yet, the link between these effectors and the observed harmful effects of type i ifns on the host is still unclear. likewise, the role of of interest, a subset of isgs is amongst the most induced genes in the intestinal tissue of gnotobiotic humanized mice infected orally with l. monocytogenes (archambaud et al., 2012) . however, which type of ifns triggers this response and for which function on the intestinal mucosa remain to be explored. in addition, ifn-independent pathways may contribute to expression of these isgs. listeria has evolved several mechanisms to avoid immune detection and evade ifn responses. it has been demonstrated that deacetylation of listeria peptidoglycan by the deacetylase pgda confers resistance to host lysozyme, thus preventing release of mamps, such as dna, rna and lipopeptides, that trigger ifnβ production (boneca et al., 2007) . listeria pgda mutants are rapidly killed in murine macrophages, which produce lysozyme, and induce a strong secretion of ifn-β compared to wildtype listeria. the role of pgda is not limited to the control of type i-ifn production as a pgda mutant hyperinduces proinflammatory cytokines as well. modification of peptidoglycan by pgda is an extremely efficient mechanism of immune escape used by listeria, which correlates with its critical role in virulence. remarkably, listeria has evolved a sophisticated strategy to modulate, either negatively or positively, the expression of isgs in epithelial cells, by targeting a chromatin-repressive complex, bahd1 (bierne et al., 2009; lebreton et al., 2011 lebreton et al., , 2012 . indeed, listeria infection promotes, albeit via an unknown mechanism, the targeting of bahd1 at the promoter of a set of isgs, thereby downregulating type i-and type iii-ifn responses. on the other hand, listeria can produce a nucleomodulin, lnta, which when secreted by intracellular bacteria, enters the nucleus of infected cells, binds bahd1 and inhibits its function (lebreton et al., , 2014 . thus, lnta stimulates ifn responses. consistent with the presence of hdac1/2 in the bahd1-associated complex, the level of acetylation of lysine 9 on histone h3, which is a mark of active chromatin, increases at the promoters of isgs in the presence of lnta. when, in which host conditions, and how lnta targets bahd1 specifically at isgs remains an open question. the lnta-mediated stimulation of type iii-ifn responses might support localized pro-bacterial conditions, as was proposed for ifn-i responses. we have an extensive knowledge of the molecular and cellular mechanisms involved in listeria-host interactions. yet, our understanding of the immune response to listeria, and more specifically the role ifns and of their downstream effectors, is far from complete and often relies on studies performed in cultured cells or in mice. however, murine and human listeriosis differ in many aspects (lecuit, 2007; hoelzer et al., 2012) . for instance, e-cadherin, the major receptor for listeria in epithelial cells, is not functional for listeria uptake in the mouse. thus, the route of entry of listeria is not strictly the same in mice and humans. moreover, isgs induced in response to infection are not identical in mice and humans. additionally, murine hepatocytes do not respond to type iii-ifns (hermant et al., 2014) , precluding the study of these ifns during infection by human hepatotropic pathogens, such as l. monocytogenes. altogether, species-specific differences provide limits to the use of mouse models in characterizing ifn pathways engaged during listeria infection in humans, especially in key epithelial organs such as the gut, liver and placenta. it will be important to perform future studies using adapted animal models, such as humanized mice permissive to oral infection or transgenic mice with human xenografts (walters et al., 2006) , since the effect of type i-ifn on listeria infection depends on the route and time of infection (pontiroli et al., 2012; kernbauer et al., 2013) and type iii-ifn requires bacterial interaction with epithelia . finally, numerous isgs are induced upon listeria infection in vitro, but the relevant isgs and their cellular functions remain to be identified. validation of isgs identified in cultured cells in adequate in vivo models or deduced from analyses of patient samples, will be required to address the complex role of ifns and bacterial subversion strategies and provide new insights into listeria pathogenesis. rig-i detects infection with live listeria by sensing secreted bacterial nucleic acids cgas produces a 2 -5 -linked cyclic dinucleotide second messenger that activates sting impact of lactobacilli on orally acquired listeriosis sting-dependent type i ifn production inhibits cell-mediated immunity to listeria monocytogenes both tlr2 and trif contribute to interferon-β production during listeria infection oata, a peptidoglycan o-acetyltransferase involved in listeria monocytogenes immune escape, is critical for virulence mice lacking the type i interferon receptor are resistant to listeria monocytogenes the ifn gamma receptor: a paradigm for cytokine receptor signaling human bahd1 promotes heterochromatic gene silencing activation of type iii interferon genes by pathogenic bacteria in infected epithelial cells and mouse placenta two families of gtpases dominate the complex cellular response to ifn-gamma a critical role for peptidoglycan n-deacetylation in listeria evasion from the host innate immune system multiple mechanisms contribute to the robust rapid gamma interferon response by cd8+ t cells during listeria monocytogenes infection type i interferon signaling regulates the composition of inflammatory infiltrates upon infection with listeria monocytogenes requirement of endogenous interferon-gamma production for resolution of listeria monocytogenes infection sting is a direct innate immune sensor of cyclic di-gmp the arsenal of virulence factors deployed by listeria monocytogenes to promote its cell infection cycle lymphocyte apoptosis as an immune subversion strategy of microbial pathogens confounding 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listeria monocytogenes during infection in non-immune cells importance of murine vdelta1 gammadelta t cells expressing interferon-gamma and interleukin-17a in innate protection against listeria monocytogenes infection interferon lambda 4 signals via the ifn-λ receptor to regulate antiviral activity against hcv and coronaviruses histone modifications induced by a family of bacterial toxins specific immunity to listeria monocytogenes in the absence of ifn gamma 25 years of interferon-based treatment of chronic hepatitis c: an epoch coming to an end type i ifn signaling constrains il-17a/f secretion by gammadelta t cells during bacterial infections human but not mouse hepatocytes respond to interferon-lambda in vivo animal models of listeriosis: a comparative review of the current state of the art and lessons learned chronic granulomatous disease type i interferon gene induction by the interferon regulatory factor family of transcription factors irf-7 is the master regulator of type-i interferon-dependent immune responses cross-regulation of signaling pathways by interferon-gamma: implications for immune responses and autoimmune diseases immune response in mice that lack the interferon-gamma receptor virus interference. i. the interferon mechanisms of type iii interferon expression myd88 and type i interferon receptor-mediated chemokine induction and monocyte recruitment during listeria monocytogenes infection interferon-gamma-receptor deficiency in an infant with fatal bacille calmette-guérin infection il-12 and ifn-gamma in host defense against mycobacteria and salmonella in mice and men mice that lack the interferon-gamma receptor have profoundly altered responses to infection with bacillus calmette-guérin and subsequent challenge with lipopolysaccharide demonstration of an interferon gamma-dependent tumor surveillance system in immunocompetent mice type i ifns downregulate myeloid cell ifn-gamma receptor by inducing recruitment of an early growth response 3/ngfi-a binding protein 1 complex that silences ifngr1 transcription route of infection determines the impact of type i interferons on innate immunity to listeria monocytogenes conditional stat1 ablation reveals the importance of interferon signaling for immunity to listeria monocytogenes infection a family of ifn-gamma-inducible 65-kd gtpases protects against bacterial infection ifn-λs ifn-λs mediate antiviral protection through a distinct class ii cytokine receptor complex t-bet: a bridge between innate and adaptive immunity bacteria tune interferon responses by playing with chromatin structural basis for the inhibition of the chromatin repressor bahd1 by the bacterial nucleomodulin lnta a bacterial protein targets the bahd1 chromatin complex to stimulate type iii interferon response human listeriosis and animal models a transgenic model for listeriosis: role of internalin in crossing the intestinal barrier induction and function of type i and iii interferon in response to viral infection duox2-derived reactive oxygen species are effectors of nod2-mediated antibacterial responses listeriosis cellular resistance to infection ifn-inducible gtpases and immunity to intracellular pathogens interferon-inducible effector mechanisms in cellautonomous immunity role of type i interferons in inflammasome activation, cell death, and disease during microbial infection type i ifn signaling is crucial for host resistance against different species of pathogenic bacteria regulation of mouse nk cell development and function by cytokines interferons α and λ inhibit hepatitis c virus replication with distinct signal transduction and gene regulation kinetics staphylococcus aureus activates type i ifn signaling in mice and humans through the xr repeated sequences of protein a a specific gene expression program triggered by gram-positive bacteria in the cytosol induction of type i interferons by bacteria what have we learned from the il28 receptor knockout mouse? localized reactive oxygen and nitrogen intermediates inhibit escape of listeria monocytogenes from vacuoles in activated macrophages whatever turns you on: accessory-celldependent activation of nk cells by pathogens a mutation in the interferon-gamma-receptor gene and susceptibility to mycobacterial infection transcytosis of listeria monocytogenes across the intestinal barrier upon specific targeting of goblet cell accessible e-cadherin type i interferon production enhances susceptibility to listeria monocytogenes infection immune activation of type i ifns by listeria monocytogenes occurs independently of tlr4, tlr2, and receptor interacting protein 2 but involves tnfr-associated nf kappa b kinase-binding kinase 1 host defense and endogenous interferon-gamma in the intestines during an oral infection with listeria monocytogenes gastroenteritis due to listeria monocytogenes innate recognition of bacteria by a macrophage cytosolic surveillance pathway the enhanceosome an atomic model of the interferon-beta enhanceosome the helicase ddx41 recognizes the bacterial secondary messengers cyclic di-gmp and cyclic di-amp to activate a type i interferon immune response opposing roles for interferon regulatory factor-3 (irf-3) and type i interferon signaling during plague listeria monocytogenes invades the epithelial junctions at sites of cell extrusion the stress-induced virulence protein inlh controls interleukin-6 production during murine listeriosis the interferons: 50 years after their discovery, there is much more to learn interferons, interferon-like cytokines, and their receptors structural and dynamic determinants of type i interferon receptor assembly and their functional interpretation inhibition of dynamin-dependent endocytosis interferes with type iii ifn expression in bacteria-infected human monocyte-derived dcs the timing of ifnβ production affects early innate responses to listeria monocytogenes and determines the overall outcome of lethal infection indoleamine 2,3-dioxygenase-expressing dendritic cells form suppurative granulomas following listeria monocytogenes infection a variant upstream of ifnl3 (il28b) creating a new interferon gene ifnl4 is associated with impaired clearance of hepatitis c virus type i ifns enhance susceptibility to chlamydia muridarum lung infection by enhancing apoptosis of local macrophages mutations of the listeria monocytogenes peptidoglycan n-deacetylase and o-acetylase result in enhanced lysozyme sensitivity, bacteriolysis, and hyperinduction of innate immune pathways antagonistic crosstalk between type i and ii interferons and increased host susceptibility to bacterial infections type i ifn are host modulators of strain-specific listeria monocytogenes virulence identity, regulation and in vivo function of gut nkp46(+)rorγt(+) and nkp46(+)rorγt(-) lymphoid cells type i interferon induces necroptosis in macrophages during infection with salmonella enterica serovar typhimurium listeria monocytogenes and recurrent 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listeria monocytogenes strain naturally overexpressing the multidrug efflux pump mdrt the role of the activated macrophage in clearing listeria monocytogenes infection il-28, il-29 and their class ii cytokine receptor il-28r monocyte recruitment during infection and inflammation nuclear receptor err-alpha and coactivator pgc-1beta are effectors of ifn-gamma-induced host defense cell biology and immunology of listeria monocytogenes infections: novel insights type i interferons in host defense characterization of the interferon-producing cell in mice infected with listeria monocytogenes ifn regulatory factor 3-dependent induction of type i ifns by intracellular bacteria is mediated by a tlr-and nod2-independent mechanism cyclic gmp-amp synthase is a cytosolic dna sensor that activates the type i interferon pathway the epidemiology of human listeriosis. microbes infect the feedback phase of type i interferon induction in dendritic cells requires interferon regulatory factor 8 sources of 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c-di-amp secreted by intracellular listeria monocytogenes activates a host type i interferon response cyclic gmp-amp is an endogenous second messenger in innate immune signaling by cytosolic dna listeria monocytogenes strain-specific impairment of the tetr regulator underlies the drastic increase in cyclic di-amp secretion and beta interferoninducing ability the cytosolic nucleic acid sensor lrrfip1 mediates the production of type i interferon via a β-catenin-dependent pathway innate and adaptive immune responses to listeria monocytogenes: a short overview interferon-λs: special immunomodulatory agents and potential therapeutic targets stimulation of inducible nitric oxide synthase expression by beta interferon increases necrotic death of macrophages upon listeria monocytogenes infection conflict of interest statement: the authors declare that the research was con the authors declare no conflict of interest. the authors' work has been supported in part by the institut pasteur, inserm, inra, université paris-diderot, labex ibeid, anr (grant epilis), french ligue nationale contre le cancer, fondation louis-jeantet, fondation le roch, and european research council (advanced grant award 233348 to pascale cossart). pascale cossart is an international research scholar of the howard hughes medical institute. key: cord-321878-bnjupaik authors: deliwala, smit s.; ponnapalli, anoosha; seedahmed, elfateh; berrou, mohammed; bachuwa, ghassan; chandran, arul title: a 29-year-old male with a fatal case of covid-19 acute respiratory distress syndrome (cards) and ventilator-induced lung injury (vili) date: 2020-07-23 journal: am j case rep doi: 10.12659/ajcr.926136 sha: doc_id: 321878 cord_uid: bnjupaik patient: male, 29-year-old final diagnosis: acute respiratory distress syndrome (ards) • covid-19 •multi organ failure/septic shock • pneumothorax symptoms: cough • dyspnea • fatigue • myalgia medication:— clinical procedure: mechanical ventilation • thoracentesis specialty: critical care medicine objective: unknown ethiology background: covid-19 patients that develop acute respiratory distress syndrome (ards) “cards” behave differently compared to patients with classic forms of ards. recently 2 cards phenotypes have been described, type l and type h. most patients stabilize at the milder form, type l, while an unknown subset progress to type h, resembling full-blown ards. if uncorrected, phenotypic conversion can induce a rapid downward spiral towards progressive lung injury, vasoplegia, and pulmonary shrinkage, risking ventilator-induced lung injury (vili) known as the “vili vortex”. no cases of in-hospital phenotypic conversion have been reported, while ventilation strategies in these patients differ from the lung-protective approaches seen in classic ards. case report: a 29-year old male was admitted with covid-19 pneumonia complicated by severe ards, multi-organ failure, cytokine release syndrome, and coagulopathy during his admission. he initially resembled cards type l case, although refractory hypoxemia, fevers, and a high viral burden prompted conversion to type h within 8 days. despite ventilation strategies, neuromuscular blockade, inhalation therapy, and vitamin c, he remained asynchronous to the ventilator with volumes and pressures beyond accepted thresholds, eventually developing a fatal tension pneumothorax. conclusions: patients that convert to type h can quickly enter a spiral of hypoxemia, shunting, and dead-space ventilation towards full-blown ards. understanding its nuances is vital to interrupting phenotypic conversion and entry into vili vortex. tension pneumothorax represents a poor outcome in patients with cards. further research into monitoring lung dynamics, modifying ventilation strategies, and understanding response to various modes of ventilation in cards are required to mitigate these adverse outcomes. the cluster of pneumonia cases associated with the novel coronavirus (covid-19) or severe acute respiratory syndrome coronavirus 2 (sars-cov-2) that emerged from wuhan, china and spread rapidly across continents was labeled by the world health organization (who) as a global pandemic. as of may 19, 2020, 1.5 million cases of covid-19 were present in the united states (us), with roughly 85 400 deaths [1] . covid-19 pneumonia seems to behave differently from other viral types of pneumonia, with large swings in respiratory functioning, inferring that not all previous practices can be adopted, and new strategies are needed to mitigate the high mortality rates (79% to 86%) seen in advanced cases [2, 3] . supplemental oxygen use was seen in 38.9% of infected patients, with 28.7% requiring mechanical ventilation and less than 1% requiring advanced therapies such as extracorporeal membrane oxygenation (ecmo); however, these numbers may likely be underrepresented with preventative measures such as social distancing and stay-at-home executive orders leading to reluctance and delay in receiving care [4] . the progression of covid-19 to ards ("cards") represents a life-threatening sequela, with its ability to lower blood oxygenation levels and induce systemic hypoxemia and multi-organ failure [3, 5] . despite cards meeting the berlin diagnostic criteria, its trajectory is characterized by severe hypoxemia with near-normal respiratory compliance, unlike its classic form [5, 6] . patients with cards can present within a broad spectrum from perceived normal breathing ("silent hypoxemia") to floored respiratory compromise with a wide array of overlapping features in between [6] . recently, 2 cards phenotypes have been parsed out, type l and type h, with each one having its distinct pathophysiological pathway. understanding these nuances are vital to providing appropriate treatment and avoiding sub-optimal outcomes [5] . we present a case of cards with subsequent sequelae and numerous challenges in management. we aim to strengthen the existing literature, explore the cards phenotypes, and discuss therapeutic and ventilator strategies to counteract the unique lung injury seen in covid-19 pneumonia that progress to ards. a 29-year-old male with a history of asthma, previous gunshot wound, and obesity, presented to the hospital with dyspnea, cough, fatigue, and myalgias. he used tobacco products and worked at an auto-parts manufacturing unit. on arrival, he was febrile, tachycardic, and tachypneic requiring supplemental oxygen. he appeared ill with a high work of breathing and a productive cough. workup revealed lymphopenia to 1.4 k/ul, thrombocytopenia to 121 000 k/ul, and an unremarkable chest radiograph ( figure 1 ); the patient was transferred to the intensive care unit (icu) with a high suspicion for covid-19. testing for sars-cov-2 was completed using a nasopharyngeal swab transported in an m4 viral tube to the state department of health and human services. samples were tested on the sars-cov-2 real-time polymerase chain reaction (rt-pcr) abbott id now™ point-of-care system under the food and drug administration (fda) emergency use authorization (eua). computed tomography (ct) of the chest could not be performed due to concern for virus transmission and environmental contamination due to high demands and short downtime for decontamination. by day 3, the patient required higher flow rates on a non-rebreather mask, and by day 4, persistent fevers, tachypnea, and new consolidative changes in the right middle and lower lung zones were noted. he was empirically started on broad-spectrum antibiotics with hydroxychloroquine. foregoing bi-pap or c-pap due to concerns for aerosolization, he was placed on mechanical ventilation. his chest x-ray by day 8 revealed extensive consolidative infiltrates bilaterally and a pao 2 /fio 2 (pf) ratio of 59 consistent with severe acute respiratory distress syndrome (ards) (figure 2 ). testing for sars-cov-2 came back positive, confirming covid-19 pneumonia. over the following days, he went into septic shock requiring vasopressor support, while previously sent cytokine labs, including an interleukin-6 (il-6) of 46 pg/ml, were consistent with cytokine release syndrome. he was given a dose of tocilizumab 400 mg. on day 10, extensive acute deep vein thromboses (dvts) was discovered in his left upper extremity with d-dimer levels over 10 µg/ml. his previous prophylactic dose of enoxaparin was increased to a therapeutic dose. his fevers did not abate, requiring cooling, neuromuscular blockade, and deep sedation. ards strategies, including low tidal volumes, proning, recruitment maneuvers, diuretics, nitric oxide, and vitamin c, were used despite his rising pressures. during these periods, he exhibited high plateau pressures, often over 30 cm of h 2 o. worsening status prompted consideration of transfer to a specialized ecmo center. however, surrounding centers had limited the inflow of patients adhering to strict infection control measures, while judicious resource allocation and logistical challenges made transportation unfeasible. on day 17, after a sudden episode of desaturation, a chest x-ray revealed left-sided tension pneumothorax in the left mid and lower lung fields ( figure 3 ) with a chest tube draining 700 ml of serosanguineous fluid mixed with blood clots intermittently blocking output with persistent air leaks. fluid characteristics were not obtained, and his overall clinical trajectory began declining. a family discussion was held to discuss his poor prognosis and address the goals of care. his code status was changed to do-not-resuscitate (dnr) with an emphasis on comfort measures. he eventually desaturated and went into asystole, passing away after spending 20 days in the hospital. trends in oxygenation in our patient can be seen in table 1 . ards can be mitigated by opening collapsed alveoli with higher positive end-expiratory pressures (peeps), recruiting maneuvers, or proning. in contrast, these high pressures are poorly tolerated, leading to the use of low tidal volumes to minimize ventilator-induced lung injury (vili). despite this, high rates of barotrauma were reported from the previous sars epidemic [7] . covid-19 patients complicated by ards ("cards") can present despite lacking traditional risk factors such as advancing age, pre-existing co-morbidities, or an advanced lung pathology [5] . despite the initial insult being the inoculation of sars-cov-2, cards can occur from injuries from either the gas or vascular side of the alveoli [6] . approaching cards from the gas side cards is defined by 2 phenotypes based on its clinical trajectory. "type l" has a relatively compensated clinical state while "type h" resembles full-blown ards ( table 2 ). our patient, initially a type l, had scattered infiltrates with rising minute ventilation over days. type l patients are perceived to be breathing normally ("silent hypoxemia") and often respond to supplemental oxygen. at the same time, deep swings in respiration can induce patient self-inflicted lung injury (p-sili), triggering an inflammation cascade and a rapid downward spiral towards progressive pulmonary injury and pulmonary shrinkage, known as the 'vili vortex' towards full-blown ards [6] . evidence of transformation to type h by day 8 was noted by his rising plateau and driving pressures, lower static compliance, and low pf ratios signifying a bulkier lung. refractory hypoxia, fevers, and systemic insults led to a dependency on high peeps and fio 2 to maintain oxygen saturation above 88%. post-mortem studies reveal numerous thromboses in covid-19 patients with d-dimer serving as a surrogate marker of pulmonary endothelial damage, promoting ventilation-perfusion mismatches and subsequent hypoxemia [5, 6, 8] . dvts were noted in over 50% of patients, suggesting that coagulopathy may be an independent risk factor for poor prognosis [9] . our patient reflected coagulopathy and vasoplegia with rising d-dimer levels in the days leading up to his dvt, while the development of cytokine release syndrome and coagulopathy signaled his growing disease burden. once this occurs, vasoregulation is altered due to the failure of hypoxic vasoconstriction from the endothelial damage resulting in significant hypoxemia. if the respiratory drive is not altered by oxygen administration, the generated inspiratory increases transpulmonary pressures across vascular channels, risking vili. this can also serve as a learning point, that early intubation strategies can help minimize the powerful respiratory effort leading to vasoplegia. if uncorrected, high plateau pressures reflecting high trans alveolar pressures can increase thoracic compliance leading to high oxygen and peep requirements that can redirect blood to damaged parts with high permeability affecting hemodynamics and contributing to type h conversion. the accepted thresholds for vili protection include a plateau pressure of 30 cmh 2 developed spontaneous pneumothorax with a 50% drop in his pf ratio because of his high plateau pressures, respiratory swings, and inflammation. the incidence of pneumothorax has been reported to be roughly 6% in covid-19 patients [12] , although these represented spontaneous cases from the community, unlike our case which was a consequence of progressive lung injury and the inability to liberate the patient from the vili vortex. the development of pneumothorax after intubation can portend a poor prognosis in patients with cards [12] [13] [14] . categorizing lung injury from covid-19 into cards type l or type h can help unwanted practices and initiate targeted ventilator approaches to correct the underlying mismatch. the surviving sepsis campaign recommended that mechanically ventilated covid-19 patients be managed similarly to other patients with respiratory failure in the icu, although with the growing body of evidence, cards is displaying a distinct course [15] . the 3 essential contributors to cards and entry into the vili vortex are 1) sars-cov-2 burden, 2) ventilator responsiveness, and 3) time of symptom onset [6] . the paucity of reported cases brings into light the importance of isolated reports in guiding therapy in the current climate. this case represents the first reported cards patient that developed a pneumothorax as a consequence of his phenotype conversion. in previous cases of sars patients, pneumothorax was noted at 14-37 days after the initial diagnosis [16] , suggesting that a sustained period of lung inflammation serves as a pre-requisite, a similar time course as our patient recently a scoring system was proposed to predict the risk of developing critical illness in covid-19, allowing early interventions and resource allocation to mitigate the high disease burden [17] . covid-19 patients that develop ards ("cards") come in 2 phenotypes: type l and h. type l is often stable while type h presents like full-blown ards. these patients require different ventilator strategies with the goal of avoiding conversion to type h and limiting vili. in these cases, pneumothorax may represent an indicator of a poor outcome. an interactive web-based dashboard to track covid-19 in real time respiratory support in novel coronavirus disease (covid-19) patients, with a focus on resource-limited settings respiratory conditions in coronavirus disease 2019 (covid-19): important considerations regarding novel treatment strategies to reduce mortality covid-19: timing is important management of covid-19 respiratory distress covid-19 pneumonia: different respiratory treatments for different phenotypes? critically ill patients with severe acute respiratory syndrome clinical phenotypes of sars-cov-2: implications for clinicians and researchers autopsy findings and venous thromboembolism in patients with covid-19 driving pressure and mechanical power: new targets for vili prevention a comparison of oesophageal and central venous pressures in the measurement of transpulmonary pressure change emergency tracheal intubation in 202 patients with covid-19 in wuhan, china: lessons learnt and international expert recommendations sars-cov-2 infection associated with spontaneous pneumothorax covid-19 with spontaneous pneumothorax, pneumomediastinum and subcutaneous emphysema surviving sepsis campaign: guidelines on the management of critically ill adults with coronavirus disease 2019 (covid-19) severe acute respiratory syndrome complicated by spontaneous pneumothorax development and validation of a clinical risk score to predict the occurrence of critical illness in hospitalized patients with covid-19 none. key: cord-307128-wwjeu8ie authors: walz, lucas; cohen, avi j.; rebaza, andre p.; vanchieri, james; slade, martin d.; dela cruz, charles s.; sharma, lokesh title: janus kinase-inhibitor and type i interferon ability to produce favorable clinical outcomes in covid-19 patients: a systematic review and meta-analysis date: 2020-08-11 journal: medrxiv doi: 10.1101/2020.08.10.20172189 sha: doc_id: 307128 cord_uid: wwjeu8ie background: novel coronavirus (sars-cov-2) has infected over 17 million. novel therapies are urgently needed. janus-kinase (jak) inhibitors and type i interferons have emerged as potential antiviral candidates for covid-19 patients for their proven efficacy against diseases with excessive cytokine release and by their ability to promote viral clearance in past coronaviruses, respectively. we conducted a systemic review and meta-analysis to evaluate role of these therapies in covid-19 patients. methods: medline and medrxiv were searched until july 30(th), 2020, including studies that compared treatment outcomes of humans treated with jak-inhibitor or type i interferon against controls. inclusion necessitated data with clear risk estimates or those that permitted back-calculation. results: we searched 733 studies, ultimately including four randomized and eleven non-randomized clinical trials. jak-inhibitor recipients had significantly reduced odds of mortality (or, 0.12; 95%ci, 0.03–0.39, p=0.0005) and icu admission (or, 0.05; 95%ci, 0.01–0.26, p=0.0005), and had significantly increased odds of hospital discharge (or, 22.76; 95%ci, 10.68–48.54, p<0.00001), when compared to standard treatment group. type i interferon recipients had significantly reduced odds of mortality (or, 0.19; 95%ci, 0.04–0.85, p=0.03), and increased odds of discharge bordering significance (or, 1.89; 95%ci, 1.00–3.59, p=0.05). conclusions: jak-inhibitor treatment is significantly associated with positive clinical outcomes regarding mortality, icu admission, and discharge. type i interferon treatment is associated with positive clinical outcomes regarding mortality and discharge. while these data show promise, additional randomized clinical trials are needed to further elucidate the efficacy of jak-inhibitors and type i interferons and clinical outcomes in covid-19. the spread of a highly pathogenic, novel coronavirus (sars-cov-2) has emerged as the deadliest pandemic since influenza in 1918 and has proved to be the ultimate challenge for public health organizations, health care providers, and governments at all levels. [1] severe disease caused by sars-cov-2 (covid-19) has strained intensive care unit (icu) and personal protective equipment (ppe) resources around the world, [2] leading to icu mortality rates as high as 20% in some population subsets. [3] as of july 30 th , sars-cov-2 has infected over 17 million worldwide and led to the death of over 650,000. [4] currently, only few medications have been suggested to improve the disease outcome . cc-by-nc-nd 4.0 international license it is made available under a is the author/funder, who has granted medrxiv a license to display the preprint in perpetuity. the copyright holder for this preprint this version posted august 11, 2020. . https://doi.org/10.1101/2020.08.10.20172189 doi: medrxiv preprint and limit the lethal disease in susceptible populations. a small number of large-scale randomized clinical trials have been conducted so far, having demonstrated modest effectiveness for agents such remdesivir or dexamethasone. [5, 6] additional therapeutics against covid-19 are being explored, but there remains a lack of large scale rcts of many potentially useful therapies, possibly missing some important therapeutics that can alter outcomes in covid-19 patients. janus-kinases (jaks) are transmembrane proteins that serve to mediate and amplify extracellular signals from growth factors and cytokines. their inhibitors have been found to be effective in treating patients with inflammatory diseases. [7] these inhibiting drugs function by targeting specific janus kinases. both baricitinib and ruxolitinib predominantly inhibit jak1 and jak2. [7] jak-inhibitors may be used to control high levels of cytokines and inflammation, [8] similar to secondary hemophagocytic lymphohistiocytosis (shlh) caused by cytokine storm, seen in patients with severe sars-cov-2 infection. [9] these inhibitors have proved helpful in "off-label" indications, where excessive cytokine release plays a central role in the disease progression. [10] while the hypothesis of jak-inhibitors successfully combating high levels of cytokine expression in sars-cov-2 infection has been shown in some small studies, [11] their effect on a larger population has not been investigated. type i interferons-α/β are proteins secreted by infected cells meant to induce antiviral states in neighboring cells and stimulate cytokine production. [12] type i and type iii interferons have potent antiviral effects. these interferons work through activation of jak/stat pathway to activate a multitude of genes that are collectively known as interferon stimulated genes (isgs). these isgs act together to block the viral life cycle at different levels. given the widespread expression of type i interferon receptors, they function as broad spectrum antivirals that can directly and indirectly inhibit the replication of rna viruses at various moments in a viral life cycle through several mechanisms. [13] these interferons have been found to have positive therapeutic effects in the treatment of viral hepatitis, [14] and even past coronaviruses, such as the previous sars and mers outbreaks. [15, 16] additionally, a recent investigation revealed that several severe cases of covid-19 presented with a rare, x-chromosome loss-. cc-by-nc-nd 4.0 international license it is made available under a is the author/funder, who has granted medrxiv a license to display the preprint in perpetuity. (which was not certified by peer review) the copyright holder for this preprint this version posted august 11, 2020. . https://doi.org/10.1101/2020.08.10.20172189 doi: medrxiv preprint of-function mutation that impaired type i interferon response, [17] while another demonstrated an association between covid-19 severity and type i interferon deficiency. [18] various studies have found reasons to support the use of type i interferons in combination with other antivirals to promote positive outcomes among patients with covid-19, but many are restricted by the number of patients they treated with interferon. [19] interestingly, these interferons perform their functions by activating jak pathway. uncertainty and a lack of clinically proven prophylactic and therapeutic options have precipitated the periodic update of treatment guidelines for patients infected with covid-19. as such, systematic reviews evaluating effects in larger patient populations are necessary to ascertain drug-related covid-19 outcomes. in this meta-analysis, we evaluate janus kinase-inhibitors and type i interferons for their efficacy and ability to produce positive outcomes in patients infected with sars-cov-2. reviews and meta-analyses (prisma). [20] search strategy and study quality assessment medline (via pubmed) and medrxiv were searched since inception throughout july 30 th , 2020 by three investigators (lw, ac, jv). the following terms were searched in free-text fields for jak-inhibitors. for medline: "covid-19" and "jak inhibitor" or "ruxolitinib" or "tofacitinib" or "fedratinib" or "baricitinib". for medrxiv: "covid-19 jak inhibitor" or "covid-19 ruxolitinib" or "covid-19 tofacitinib" or "covid-19 fedratinib" or "covid-19 baricitinib". the following terms were searched in free-text fields for type i interferons. . cc-by-nc-nd 4.0 international license it is made available under a is the author/funder, who has granted medrxiv a license to display the preprint in perpetuity. (which was not certified by peer review) the copyright holder for this preprint this version posted august 11, 2020. . https://doi.org/10.1101/2020.08.10.20172189 doi: medrxiv preprint three investigators (lw, ac, jv) independently screened titles and abstracts generated by the search. after selection, full electronic articles were then carefully evaluated for data extraction. randomized studies included in the final analyses were scored by one investigator (lw) to formally assess for risk of bias utilizing the risk of bias (rob) 2 tool (supplementary table 3 ). [21] non-randomized studies included in the final analyses were scored by one investigator (lw), utilizing the newcastle-ottawa scale (nos) according to the following study characteristics: (1) representativeness of exposed cohort, (2) selection of nonexposed cohort, (3) exposure assessment, (4) outcome of interest not present at the start of the study, (5) comparability of cohorts, (6) outcome assessment, (7) adequacy of length of time before followup, and (8) adequacy of follow-up of cohorts (supplementary table 4 we included clinical trials that utilized combination or sole jak-inhibitor or type i interferon (ifn-α, ifn-β) for the treatment of confirmed covid-19 infection. for inclusion, possible studies must have compared treatment outcomes of those treated with a jak-inhibitor or type i interferon against a defined control group that did not receive this treatment. selection required data with clearly indicated risk ratios or odds ratios (or), or those that permitted their back-calculation. inclusion necessitated that the trial be a human study accessible in english, and could include pediatric or adult studies, observational studies, retrospective cohorts, randomized clinical trials, and case reports. studies that utilized in vivo or animal studies, as well as those examining histological, pathological, and cellular mechanisms were excluded. duplicate studies, review articles, commentaries, and proposed protocol were also excluded. trials were excluded if they primarily examined other therapies where outcomes were unclear as to which participants received jak-inhibitors or type i interferons. finally, studies were not included if they presented outcomes considered heterogenous across the review that made statistical synthesis impossible (e.g. mean vs median). . cc-by-nc-nd 4.0 international license it is made available under a is the author/funder, who has granted medrxiv a license to display the preprint in perpetuity. the copyright holder for this preprint this version posted august 11, 2020. . https://doi.org/10.1101/2020.08.10.20172189 doi: medrxiv preprint each full article that met inclusion criteria was carefully reviewed with the following baseline information extracted: first author, publication year, country, study type, type of jak-inhibitor or interferon used, number of total participants, number of participants receiving jak-inhibitor or interferon, and outcome measurements ( table 1 ). the outcome measurements consolidated included mortality, disease severity (mild/moderate vs severe/critical), mechanical ventilation, intensive care unit (icu) admission, discharge, and acute respiratory distress syndrome (supplementary table 1 reported. heterogeneity was assessed using tau-squared and chi-squared tests for random effects and fixed effect models, respectively, as well as the i 2 statistic. for i 2 > 50%, the random effects model was used. otherwise, the fixed effects model was utilized. an alpha of 0.05 was adopted to determine significance. the meta-analysis results are presented on forest plots, with a study's calculated or plotted as a black square whose size is proportional to the weight afforded to the study. bidirectional bars stemming from these black squares correspond to the risk estimate's 95% ci. diamonds were used to represent the summary or; its center aligns with the or and its width represents the summary 95% ci. publication bias was assessed using funnel plots (supplementary figure 1; supplementary figure 2 ). the initial database search returned 731 articles. two additional articles were added by manually searching retrieved reviews. after removing two duplicates, 698 articles were excluded following title and abstract screening by three investigators. after comprehensive evaluation of 33 full text articles, only 15 . cc-by-nc-nd 4.0 international license it is made available under a is the author/funder, who has granted medrxiv a license to display the preprint in perpetuity. the copyright holder for this preprint this version posted august 11, 2020. . https://doi.org/10.1101/2020.08.10.20172189 doi: medrxiv preprint studies complied with the inclusion criteria. the majority of the studied excluded in the final step were excluded on the basis of not presenting outcome data in terms of those who did and did not receive jakinhibitor or interferon treatment. the remainder of excluded studied were due to a focus on jak inhibition or interferon therapy as prophylaxis or heterogeneity in reporting of time among outcomes, precluding calculating pooled measures. of the included studies, six were pre-prints. overall, the 15 studies were comprised of four observational studies, six retrospective cohorts, four rcts, and one prospective cohort. figure 1 presents the meta-analysis flow chart and table 1 presents the designs and characteristics of included studies. while some studies did not report which drugs were given to which patients as standard of care, many others reported treating patients with glucocorticoids, hydroxychloroquine, chloroquine, arbidol, and lopinavir/ritonavir. all studies were conducted within a hospital setting. a total of five studies investigated the effect of jak inhibition in a controlled setting (table 1) figure . cc-by-nc-nd 4.0 international license it is made available under a is the author/funder, who has granted medrxiv a license to display the preprint in perpetuity. the copyright holder for this preprint this version posted august 11, 2020. . https://doi.org/10.1101/2020.08.10.20172189 doi: medrxiv preprint 2b). finally, analysis of 2 studies of 215 patients, 125 of which were treated with a jak-inhibitor, revealed that those treated with jak-inhibitor had significantly higher odds than those treated with standard care to be discharged at 2 weeks (or, 22.76; 95% ci, 10.68 -48.54; p<0.00001; figure 2e ). the analysis examining the relationship between treatment with jak-inhibition and requiring mechanical ventilation, developing ards, icu admittance, and hospital discharge demonstrated very little heterogeneity (i 2 =0). meta-analysis of 3 sets of studies with 990, 454, and 1480 patients receiving type i interferon therapy revealed that there were no significant associations between receiving type i interferon therapy, compared to standard of care, and icu admittance, requiring mechanical ventilation, or developing a severe or critical case of covid-19, respectively (p>0.05; figure 3b ; figure 3c ; figure 3d ).[28-36] the analyses included 97, 167, and 537 control patients, respectively. the data exhibited very high heterogeneity in cases of icu admittance and disease severity (both i 2 >90%), but relatively low in the case of mechanical ventilation (i 2 =12%). in the analyses of the 803 and 1415 type i interferon receiving patients, intervention therapy was respectively associated with higher odds of being discharged (or, 1.89; 95% ci, 1.00 -3.59; p=0.05; n=895; figure 3e ), and significantly lower odds of mortality (or, 0.19; 95% ci, 0.04 -0.85); p=0.03, n=1906; figure 3a) , when compared to standard of care. the studies included in these analyses enlisted 92 and 491 control patients, respectively. discharge data exhibited very low heterogeneity (i 2 =0%), while mortality data demonstrated very high heterogeneity (i 2 =90%). as sars-cov-2 continues to infect millions and kill thousands daily, there is an urgent need to find novel therapies that can effectively limit covid-19 severity. type i interferon therapy as well jak inhibitors represent paradoxical approaches to treat covid-19. while type i interferon therapy aims to limit the viral replication at the early time points to limit the subsequent disease, jak-inhibitors aim to limit the overt inflammation that may be detrimental to the host and cause systemic inflammatory response. . cc-by-nc-nd 4.0 international license it is made available under a is the author/funder, who has granted medrxiv a license to display the preprint in perpetuity. the copyright holder for this preprint this version posted august 11, 2020. . https://doi.org/10.1101/2020.08.10.20172189 doi: medrxiv preprint however, no major randomized clinical trials have been performed to determine their efficacy in limiting the disease severity in covid-19. to our knowledge, this is the first systematic review and meta-analysis to investigate the role of janus kinase-inhibitor or type i interferon on clinical outcomes in patients with covid-19. the results suggest a robust association between jak-inhibitor and significantly decreased odds of mortality and icu admission, as well as significantly increased odds for 14-day patient discharge. furthermore, a significant association between type i interferon and reduced mortality was also found, in addition to an association with hospital discharge bordering significance. these results suggest the potential benefit of these therapeutic options for covid-19. furthermore, as recent findings have shown that persistent viral presence contributes to disease severity, [37] the timing of the administration of both interventions may be of utmost importance. as jak inhibitors attenuate jak signaling and subsequent cytokine release, their administration may best be suited for patients with progressing covid-19 who have not yet experienced a cytokine storm. [38] by . cc-by-nc-nd 4.0 international license it is made available under a is the author/funder, who has granted medrxiv a license to display the preprint in perpetuity. the copyright holder for this preprint this version posted august 11, 2020. . https://doi.org/10.1101/2020.08.10.20172189 doi: medrxiv preprint contrast, as type i interferons induce cellular antiviral states via the jak/stat pathway, its administration may be most efficacious early on in disease progression where the virus is still replicating. while the literature surrounding this is sparse, one study included in this meta-analysis concluded that early administration of interferon-alpha-2b could induce positive outcomes in covid-19 patients compared to standard treatment, while its late administration was associated with slower recovery. [36] it is important to highlight that this meta-analysis attempted to overcome the challenges posed by studies with insufficient power to detect an effect between jak-inhibitor or type i interferon treatment and clinical outcomes, as half of the included studies in this analysis utilized sample sizes less than 100.[23, 25-28, 30, 35] nevertheless, despite the broad range of sample sizes and populations, the screening step of our analysis predominantly resulted in low effect size heterogeneity as evidenced by the i 2 statistics displayed in figure 2 and figure 3 . this study contained no restrictions regarding study type in the exclusion criteria and, as such, many of the studies included are of retrospective design. accordingly, baseline characteristics of patients cannot be ignored, especially as factors such as age, gender, and pre-existing comorbidities have been found in meta-analyses to be linked to negative clinical outcomes, including mortality, among covid-19 patients. [39] one study in particular contained a large disparity in the distribution of chronic conditions across those who received type i interferon therapy and controls. [31] in addition, these non-randomized studies are inherently limited in their ability to deduce the causality of association between the treatments of interest and clinical outcomes; they should be interpreted with caution. another limitation of this study is the aspect of drug combination. included studies varied in the drugs administered in the control arm and in addition to jak-inhibitor or type i interferon in the treatment group. types and doses of jakinhibitors and type i interferons also differed across studies. moreover, publication bias may have been present in some of the analyses conducted (supplemental figure 1; supplemental figure 2 ). the low number of studies make it difficult to assess asymmetry in funnel plot analyses. however, we attempted to mitigate this bias with the inclusion of six unpublished articles. a further limitation of this study is the . cc-by-nc-nd 4.0 international license it is made available under a is the author/funder, who has granted medrxiv a license to display the preprint in perpetuity. the copyright holder for this preprint this version posted august 11, 2020. . https://doi.org/10.1101/2020.08.10.20172189 doi: medrxiv preprint exclusion of a large number of studies that presented heterogenous data that precluded pooled analyses. lastly, this meta-analysis included two studies consisting of similar study teams that examined the same association, [24, 25] enhancing the likelihood of bias in the same direction in analyses where both of these studies were included. in conclusion, this meta-analysis supports the value of jak-inhibitor and type i interferon therapy as antivirals in combating sars-cov-2 infection. this study consolidates existing data and reaffirms the conclusion that, within covid-19 patients, jak-inhibitor treatment is significantly associated with positive clinical outcomes in terms of mortality, icu admission, and discharge, as well as type i interferon treatment's association with positive clinical outcomes in regard to mortality and discharge. although these findings should assist physicians deciding which antivirals to administer to sars-cov-2 infected patients, they also point to a clear need of additional well-designed rcts examining the relationship of jak-inhibitor and type i interferon and clinical outcomes of covid-19 patients. lucas walz (lw); conception of investigation, planning of investigation, data retrieval, article screening, data analysis, written reporting, data interpretation. avi j. cohen (ac); planning of investigation, data retrieval, article screening, data analysis, written reporting, data interpretation. andre p. rebaza, md (ar); written reporting, data interpretation. james vanchieri (jv): data retrieval, article screening. . cc-by-nc-nd 4.0 international license it is made available under a is the author/funder, who has granted medrxiv a license to display the preprint in perpetuity. the copyright holder for this preprint this version posted august 11, 2020 . cc-by-nc-nd 4.0 international license it is made available under a is the author/funder, who has granted medrxiv a license to display the preprint in perpetuity. the copyright holder for this preprint this version posted august 11, 2020. . https://doi.org/10.1101/2020.08.10.20172189 doi: medrxiv preprint . cc-by-nc-nd 4.0 international license it is made available under a is the author/funder, who has granted medrxiv a license to display the preprint in perpetuity. the copyright holder for this preprint this version posted august 11, 2020. . cc-by-nc-nd 4.0 international license it is made available under a is the author/funder, who has granted medrxiv a license to display the preprint in perpetuity. (which was not certified by peer review) the copyright holder for this preprint this version posted august 11, 2020. . https://doi.org/10.1101/2020.08.10.20172189 doi: medrxiv preprint jak-inhibitor treatment group saw significantly reduced odds of mortality and icu admission, as well as significantly higher odds of discharge, when compared to standard treatment. there was no significant difference between groups in regards to requiring mechanical ventilation, or the development of ards. type i interferon group saw significantly reduced odds of mortality, as well as increased odds of discharge that bordered significance, when compared to standard treatment. there was no significant . cc-by-nc-nd 4.0 international license it is made available under a is the author/funder, who has granted medrxiv a license to display the preprint in perpetuity. (which was not certified by peer review) the copyright holder for this preprint this version posted august 11, 2020. . https://doi.org/10.1101/2020.08.10.20172189 doi: medrxiv preprint responding to covid-19 -a once-in-a-century pandemic? fair allocation of scarce medical resources in the time of covid-19 clinical characteristics of covid-19 in covid-19 dashboard by the remdesivir for the treatment of covid-19 -preliminary report dexamethasone in hospitalized patients with covid-19 -preliminary report therapeutic targeting of jaks: from hematology to rheumatology and from the first to the second generation of jak inhibitors side effects of ruxolitinib in patients with sars-cov-2 infection: two case reports combined il-6 and jak-stat inhibition therapy in covid-19 related shlh, potential game changer baricitinib, a drug with potential effect to prevent sars-cov-2 from entering target cells and control cytokine storm induced by covid-19 global virus outbreaks: interferons as 1st responders hepatitis c: therapeutic perspectives interferon alfacon-1 plus corticosteroids in severe acute respiratory syndromea preliminary study epub 2013/10/03. eng. 17. van der made ci, simons a, schuurs-hoeijmakers j, et al. presence of genetic variants among young men with severe impaired type i interferon activity and inflammatory responses in severe covid-19 patients subcutaneous administration of interferon beta-1a for covid-19: a non-controlled prospective trial the prisma statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration rob 2: a revised tool for assessing risk of bias in randomised trials therapeutic effectiveness of interferon-alpha2b against covid-19: the cuban experience triple combination of interferon beta-1b, lopinavirritonavir, and ribavirin in the treatment of patients admitted to hospital with covid-19: an open-label, randomised, phase 2 trial. the lancet prolonged sars-cov-2 viral shedding in patients with covid-19 was associated with delayed initiation of arbidol treatment: a retrospective cohort study epidemiological and clinical features of 291 cases with coronavirus disease 2019 in areas adjacent to hubei, china: a double-center observational study medical treatment of 55 patients with covid-19 from seven cities in northeast china who fully recovered: a single-center, retrospective, observational study retrospective multicenter cohort study shows early interferon therapy is associated with favorable clinical responses in covid-19 patients persistent viral presence determines the clinical course of the disease in covid-19. the journal of allergy and clinical immunology in practice cytokine storm and leukocyte changes in mild versus severe sars-cov-2 infection: review of 3939 covid-19 patients in china and emerging pathogenesis and therapy concepts a comparison of mortality-related risk factors of covid-19 a systematic review and meta-analysis. the journal of infection interpretation; supervision.lokesh sharma, phd (ls): conception of investigation, planning of investigation, written reporting, data interpretation; supervision.. cc-by-nc-nd 4.0 international license it is made available under a is the author/funder, who has granted medrxiv a license to display the preprint in perpetuity. the copyright holder for this preprint this version posted august 11, 2020. . https://doi.org/10.1101/2020.08.10.20172189 doi: medrxiv preprint pmid: pmc7334925. eng.. cc-by-nc-nd 4.0 international license it is made available under a is the author/funder, who has granted medrxiv a license to display the preprint in perpetuity. (which was not certified by peer review)the copyright holder for this preprint this version posted august 11, 2020. pneumonia: a retrospective study. medrxiv. 2020:2020.05. 15.20084293 . cc-by-nc-nd 4.0 international license it is made available under a is the author/funder, who has granted medrxiv a license to display the preprint in perpetuity. the copyright holder for this preprint this version posted august 11, 2020. . https://doi.org/10.1101/2020.08.10.20172189 doi: medrxiv preprint difference between groups in regards to requiring icu admission, mechanical ventilation, or the development of severe or critical disease. . cc-by-nc-nd 4.0 international license it is made available under a is the author/funder, who has granted medrxiv a license to display the preprint in perpetuity. the copyright holder for this preprint this version posted august 11, 2020. . https://doi.org/10.1101/2020.08.10.20172189 doi: medrxiv preprint . cc-by-nc-nd 4.0 international license it is made available under a is the author/funder, who has granted medrxiv a license to display the preprint in perpetuity. the copyright holder for this preprint this version posted august 11, 2020. . https://doi.org/10.1101/2020.08.10.20172189 doi: medrxiv preprint . cc-by-nc-nd 4.0 international license it is made available under a is the author/funder, who has granted medrxiv a license to display the preprint in perpetuity. the copyright holder for this preprint this version posted august 11, 2020. . https://doi.org/10.1101/2020.08.10.20172189 doi: medrxiv preprint . cc-by-nc-nd 4.0 international license it is made available under a is the author/funder, who has granted medrxiv a license to display the preprint in perpetuity. (which was not certified by peer review)the copyright holder for this preprint this version posted august 11, 2020. . https://doi.org/10.1101/2020.08.10.20172189 doi: medrxiv preprint key: cord-332133-6hdk8801 authors: li, mao-zhong; zhang, tie-gang; li, ai-hua; luo, ming; jiao, yang; dong, mei; gong, cheng; huang, fang title: a pneumonia case associated with type 2 polio vaccine strains date: 2017-01-05 journal: chin med j (engl) doi: 10.4103/0366-6999.196575 sha: doc_id: 332133 cord_uid: 6hdk8801 nan since the world health assembly endorsed a plan to completely eradicate polio in 1988, the large-scale use of the attenuated oral poliovirus vaccine (opv) has drastically decreased the number of polio cases. however, the opv vaccine brings rare but serious adverse consequences, especially in the type 2 vaccine strains. most vaccine-associated paralytic poliomyelitis (vapp) outbreaks are associated with type 2 polio vaccine strains, and approximately 26-31% of genetically divergent vaccine-derived polioviruses (vdpvs) cases are associated with the type 2 component of opv. [1, 2] other than vapp cases and vdpvs, type 2 polio vaccine strains can also cause a variety of illnesses. [3] to the best of our knowledge, no cases of pneumonia resulting from type 2 polio vaccine strains have been reported. however, here we report an infant case associated with the type 2 polio vaccine strain. a 3-month-old male infant with no underlying diseases was admitted to beijing haidian hospital on july 31, 2015, where he was diagnosed with lobular pneumonia exactly 26 days after he had received his second dose of trivalent opv (topv). the infant was born from a second regular pregnancy by normal delivery (35/36 weeks gestation, birth weight: 3550 g). the infant also received two birth dose vaccinations (the bacillus calmette-guerin vaccine and hepatitis b vaccine), and no adverse reactions to the vaccinations were reported. the infant had no signs of immunodeficiency. his family had no history of travel in the months before he became ill. on july 23, 2015, 18 days after his second dose of topv, he developed a fever, concomitant cough, some phlegm, and his body temperature reached 40°c. an antibiotic was given by intravenous drip for 3 days in a local hospital in anhui province, but a low-grade fever and cough persisted until his hospitalization in beijing haidian hospital. blood tests in the haidian hospital revealed the following results: the total white blood cell count was 1.165 × 10 10 /l (normal range: 1.500 × 10 10 /l-2.000 × 10 10 /l); n: 14.8%; the total platelet count was 7 × 10 11 /l; and hemoglobin was 110 g/l. the laboratory tests showed that the c-reactive protein was 5.0 mg/l (normal range ≤10.0 mg/l). chest radiographs showed thickness or turbulence in the texture in both lungs and blotches of shadows in the right lung. further clinical features were respiratory sounds and pulmonary rales. in the hospital, treatments included antibiotic therapy and respiratory management such as aerosols, suctioning, back therapy, and body positioning. he was given intravenous tazobactam sodium 1 g/d and ambroxol hydrochloride and ge injections 15 mg/d. after 3 days of treatment, his body temperature returned to normal and his cough was mild. he was released on august 8 after his cough and pulmonary rales disappeared and after the chest films revealed significant absorption of the infected lesions. except for the presence of the pneumonia symptoms, he had no problems with his growth and development. a nasopharyngeal swab sample was collected at the time of admission. total nucleic acid (rna and dna) was extracted from the clinical specimens using a thermo the results were positive for the enterovirus rna, but no other respiratory pathogens were detected. subsequently, a type 2 polio vaccine strain was identified with cycle threshold values of 25 using the enterovirus molecular serotyping method and the poliovirus intratypic differentiation method. [4] to further characterize this virus strain, the entire vp1 region was determined directly from the nasopharyngeal swab with the method provided by national polio laboratory of china. the vp1 sequences were compared with the sequences available in the genbank database using the basic local alignment search tool. the results showed that the sequence had 100% nucleotide similarity compared with that of the parental sabin type 2 strains. meanwhile, the poliovirus nucleic acid was identified in the patient's nasopharyngeal swab sample using an ion torrent pgm deep sequencing instrument for a viral metagenome analysis. several other viruses were identified in this sample, including the fowl adenovirus c, the streptococcus phage, the human endogenous retrovirus, and the choristoneura occidentalis granulovirus, but none were associated with this pneumonia. the virus was also isolated from the patient's nasopharyngeal swab sample using rhabdomyosarcoma (rd) (human rd cell) and l20b (murine cell lines expressing the human poliovirus receptor) cell lines provided by national laboratory for poliomyelitis in china cdc. this case investigation revealed that the patient received his first dose of topv on june 4 and the second dose on july 5, in accord with china's immunization schedule. he was hospitalized in the capital institute of pediatrics with pneumonia on june 31, which was 27 days after taking the first topv, and he had similar respiratory clinical symptoms within 35 days after his second dose of topv. unfortunately, the clinical specimens could not be obtained from his first hospitalization. the results of the clinical and laboratory tests indicated that this pneumonia was caused by the polio virus. to the best of our knowledge, the relationship between the polio vaccine strain and pneumonia has not been previously reported. the polio vaccine strain can propagate and excrete in the upper respiratory system within several days after the opv administration. in this case, it was unclear whether the polio vaccine strain was a provoking factor or only a contributing factor to the pneumonia onset and development. the clinical and virologic investigation revealed that respiratory illnesses were diagnosed in many patients but only the sabin poliovirus could be detected in their respiratory tracts, suggesting that ingested opvs spread and cause diseases beyond the gastrointestinal tract. [3] the poliovirus caused outbreaks of human acute respiratory diseases or "minor illnesses" without clinical symptoms of the involvement of the central nervous system. a search of the database revealed that opvs spread through the nasopharynx which is detected by serum neutralization from patients with acute respiratory infections. [5] notably, an epidemiological investigation found that an infant had similar respiratory clinical symptoms after each dose of topv. thus, these reports, along with the case in this study, support the causal relationship between the type 2 polio vaccine and pneumonia. additional studies are necessary to better understand the role of opv in the pathogenesis of respiratory tract infections. however, this report provides an initial case of pneumonia, the outcomes associated with type 2 polio vaccine strains, and the implications for the safety of attenuated opv in the absence of wild virus diseases. this report also offers clinical support for the world health organization's plan to eliminate the type 2 component of opv in 2016 by removing the topv and using the bivalent opv, which contains only type 1 and 3 components of opv. there are no conflicts of interest. vaccine-derived polioviruses polio endgame: the global introduction of inactivated polio vaccine investigations of clinical isolations of oral poliovirus vaccine strains between 2000 and 2005 in southern taiwan genotyping of enteroviruses isolated in kenya from pediatric patients using partial vp1 region non-rhinovirus enteroviruses associated with respiratory infections in peru (2005-2010) key: cord-309795-2kozsv4z authors: dewidar, bedair; kahl, sabine; pafili, kalliopi; roden, michael title: metabolic liver disease in diabetes – from mechanisms to clinical trials date: 2020-06-20 journal: metabolism doi: 10.1016/j.metabol.2020.154299 sha: doc_id: 309795 cord_uid: 2kozsv4z abstract non-alcoholic fatty liver disease (nafld) comprises fatty liver (steatosis), non-alcoholic steatohepatitis (nash) and fibrosis/cirrhosis and may lead to end-stage liver failure or hepatocellular carcinoma. nafld is tightly associated with the most frequent metabolic disorders, such as obesity, metabolic syndrome, and type 2 diabetes mellitus (t2dm). both multisystem diseases share several common mechanisms. alterations of tissue communications include excessive lipid and later cytokine release by dysfunctional adipose tissue, intestinal dysbiosis and ectopic fat deposition in skeletal muscle. on the hepatocellular level, this leads to insulin resistance due to abnormal lipid handling and mitochondrial function. over time, cellular oxidative stress and activation of inflammatory pathways, again supported by multiorgan crosstalk, determine nafld progression. recent studies show that particularly the severe insulin resistant diabetes (sird) subgroup (cluster) associates with nafld and its accelerated progression and increases the risk of diabetes-related cardiovascular and kidney diseases, underpinning the critical role of insulin resistance. consequently, lifestyle modification and certain drug classes used to treat t2dm have demonstrated effectiveness for treating nafld, but also some novel therapeutic concepts may be beneficial for both nafld and t2dm. this review addresses the bidirectional relationship between mechanisms underlying t2dm and nafld, the relevance of novel biomarkers for improving the diagnostic modalities and the identification of subgroups at specific risk of disease progression. also, the role of metabolism-related drugs in nafld is discussed in light of the recent clinical trials. finally, this review highlights some challenges to be addressed by future studies on nafld in the context of t2dm. nonalcoholic fatty liver diseases (nafld) is currently defined by lipid deposition that exceeds more than 5% of hepatocytes, as assessed from liver biopsy, and/or by more than 5 .6% hepatocellular fat content per liver weight, as assessed from magnetic resonance (mr) methods, in the absence of significant alcohol consumption and other causes of fatty liver [1, 2] . nafld, which affects about 25% of the population [3] , comprises a broad range of abnormalities ranging from simple fatty liver (steatosis) to non-alcoholic steatohepatitis (nash), characterized by inflammation, necrosis, and hepatocellular ballooning, and progression to liver fibrosis, cirrhosis, and hepatocellular carcinoma (hcc) [2] . some gene variants promote risk of nafld by altering lipid droplet formation and de novo lipogenesis (dnl), such as variants of patatin-like phospholipase domain-containing protein 3 (pnpla3) and glucokinase regulatory protein [4] , or by decreasing very-low-density lipoproteins (vldl) export as shown for a missense mutation (e167k) in transmembrane 6 superfamily member 2 (tm6sf2) [5] . nevertheless, nafld is tightly associated with common acquired metabolic diseases such as obesity and type 2 diabetes (t2dm). the mutual relationship between both diseases is illustrated by several epidemiological data. the prevalence of steatosis and nash has been estimated to be 50 and 56%, respectively, in t2dm [6] . the age-adjusted relative risk of nafld is about 5.36fold higher in t2dm compared to healthy humans [7] . t2dm is also an emerging risk factor for nash progression to advanced fibrosis, cirrhosis and hcc [8, 9] . diabetes was even a better predictor for hcc development in people with nash and cirrhosis compared to other metabolic risk factors such as hyperlipidemia, body mass index (bmi) and hypertension [10] . recently, a consensus panel has proposed to rename nafld a metabolic-dysfunction-associated fatty liver disease (mafld) based on the presence of overweight/obesity, t2dm and evidence of so-called "metabolic dysregulation" [11] . future will tell, if this will help to better understand the multiple relationships between nafld and t2dm. in this context, nafld per se associates with more than double risk of incident diabetes pointing to specific liver-related mechanisms [12, 13] . moreover, multicenter studies in skandinavia and germany have recently found that diabetes can be stratified into subtypes j o u r n a l p r e -p r o o f the circulation. on the contrary, a recent study demonstrated that obesity-induced insulin resistance preceded inflammation in adipose tissues of mice [29] . indeed, adipose tissue inflammation might be a protective feedback mechanism as its local inhibition in mice induced ectopic lipid accumulation in liver, glucose intolerance, and systemic inflammation [30] . besides released inflammatory cytokines and ffa, adipose tissue could still communicate with the liver and muscle through secretion of different adipokines such as adiponectin and leptin. persons with nash have lower serum adiponectin compared to those with nafld with or without normal liver enzymes [31] . by contrast, the circulating levels of leptin were higher in people with nafld and t2dm, probably due to increased leptin resistance, and were associated with disease severity [32] . increased ffa influx to skeletal muscle promotes accumulation of intramyocellular lipid (imcl). reduced mitochondrial oxidation contributes as well to imcl as shown in aging and insulin-resistant humans [33] . consequently, skeletal muscle exhibits insulin resistance, which often precedes the onset of t2dm and insulin resistance in the liver [34] . lipid intermediate metabolites, in particular sn 1,2 diacylglycerols (dag), link imcl to skeletal muscle insulin resistance through activation of protein kinase c-theta (pkcθ) resulting in its translocation from cytoplasm to the plasma membrane [35] . muscles of insulin resistant humans with obesity and t2dm showed increased dag content and pkcθ activity as compared to healthy humans [35] . mutation studies highlighted serine amino acid residue (ser1101) of irs1 to be a substrate for activated pkcθ [36] . as a consequence of skeletal muscle insulin resistance, postprandial energy storage shifts from glycogen synthesis in the muscle into triacylglycerol (tag) in the liver, promoting nafld development [25] . gut microbiome is increasingly recognized as a modulator of liver pathogenesis through what is called the "gut-liver axis" [37] . distinctive alterations of gut microbiome were reported in humans having nash and t2dm [38] . the intestinal microbiome alters host metabolism by modulating the production of short-chain fatty acids (scfa) e.g. butyrate, acetate, and propionate, which have beneficial effects on insulin sensitivity, lipid and glucose metabolism [38] . also, intestinal dysbiosis could associate with increased intestinal permeability permitting translocation of bacterial lipopolysaccharide (lps) into the systemic circulation, j o u r n a l p r e -p r o o f 6 which could induce fat deposition in the liver, nash progression, weight gain, and diabetes [39] . moreover, intestinal microbiome could suppress the expression of fasting-induced adipocyte factor (fiaf) in intestinal epithelium, which functions as an inhibitor of circulating lipoprotein lipase, resulting in increased tag storage in the peripheral tissues [22] . also, ethanol-producing microbiome could increase blood alcohol concentration in nash, which is metabolized in the liver generating high levels of reactive oxygen species (ros). the last mechanism could explain the histological similarity between nash and alcoholic steatohepatitis [22] . furthermore, microbiota metabolize liver-derived primary bile acids into secondary bile acids. the latter are reabsorbed into bloodstream and may act as signaling molecules via a variety of receptors including farnesoid x receptor (fxr), which regulates the transcription of different metabolic genes involved in bile acid synthesis, transport, lipogenesis, and glucose homeostasis [40] . insulin resistance in both skeletal muscle and adipose tissues initiates liver steatosis by providing precursors and substrates for dnl and mitochondrial β-oxidation e.g. glucose, ffa and glycerol [25] . although reesterification of ffa derived from diet and adipose tissue is the dominant contributor to tag pool in the liver (59%), it did not increase in people with nafld. on the other side, dnl-derived ffa contribute by about 26%, which is severalfold higher as compared to individuals without nafld (10%) [41] . later, insulin resistance of the liver develops, resulting in increased gluconeogenesis and elevation of endogenous glucose production (egp) from the liver, which contributes to fasting hyperglycemia in individuals with t2dm [25] . insulin signaling inhibits typically hepatic gluconeogenesis through akt-induced phosphorylation of forkhead box (foxo1) and induces lipogenesis through activation of sterol regulatory element-binding proteins (srebp1c) and mammalian target of rapamycin complex (mtorc1) pathways. during hepatic insulin resistance, insulin does not suppress gluconeogenesis efficiently, while dnl is preserved or even increased. to explain this discrepancy, pathway-selective hepatic insulin resistance was postulated, which means that only one arm of insulin signaling is defective i.e. akt/foxo1 leading to reduced insulin-mediated suppression of gluconeogenesis, whereas insulin-activated srebp-1c/mtorc1 pathway remains intact and activates lipogenesis [28] . actually, dnl was reduced after induction of hepatic insulin resistance by feeding mice with j o u r n a l p r e -p r o o f 7 a high-fat diet (hfd) [42] , which challenges the concept of selective hepatic insulin resistance and suggest the existence of alternate mechanisms that contribute to increased dnl and gluconeogenesis in insulin-resistant liver, for example, hyperinsulinemia, insulinindependent re-esterification of adipose tissue-derived ffa, and increased acetyl coa generation from β-oxidation of ffa, which allosterically activates pyruvate carboxylase enzyme, leading to enhanced gluconeogenesis [25] . in addition, increased blood glucose level can activate carbohydrate response element-binding protein (chrebp) signaling pathway, thereby stimulating expression of several glycolytic genes, which provide additional metabolic precursors for dnl [43] . in line, chrebp overexpression induced stearoyl-coa desaturase 1 (scd1) expression, an enzyme responsible for the biosynthesis of monounsaturated fatty acids (mufa), resulting in increased liver fat content [44] . pkc epsilon (pkcε) is crucial in mediating hepatic insulin resistance and once activated by dag, it translocates to the cell membrane, and phosphorylates specific threonine residue (thr1160 in human and thr1150 in mouse) on insulin receptor leading to destabilization of the active configuration of insulin receptor kinase and inhibition of its tyrosine kinase activity [45] (figure 2 ). in general, both hyperglycemia and toxic lipids such as ceramides, dag, ffa, and cholesterol can induce deleterious effects on liver cells (glucolipotoxicity), which might initiate nafld progression from simple steatosis to nash and fibrosis via various mechanisms, including cell death, oxidative stress, endoplasmic reticulum (er) stress and mitochondrial disorders [46] . alterations in the activity and abundance of oxidative phosphorylation (oxphos) proteins and antioxidant enzymes were described in various animal models of nafld [47] . impaired hepatic mitochondrial function was evident as well in t2dm and nash [48, 49] . in a mouse model of choline-deficient diet-induced nafld, mitochondrial oxphos was increased at 12 weeks but lost at a later time point [50] . also, the higher maximal respiration rate of liver mitochondria was severalfold higher in insulin-resistant obese individuals with fatty liver as compared to lean individuals [51] . these studies highlight the flexibility of mitochondria to adapt to increased metabolic inputs to keep energy homeostasis and to protect against the harmful effects of increased ffa and tag in the liver. in nash, mitochondrial flexibility was lost, which was associated with increased ros production and exhaustion of protective antioxidant enzymes [51] (figure 2 ). whether loss of mitochondrial flexibility is a cause or consequence for nafld progression remains obscure. depletion of atp due to j o u r n a l p r e -p r o o f mitochondrial disorders, together with hyperglycemia and lipid overload could be inducers for another signaling pathway, termed unfolded protein response "upr", which is adaptive response to resolve unfolded or misfolded proteins and to restore er homeostasis [52, 53] . prolonged upr stress can activate jnk and nf-kb signaling pathways, which are involved in insulin resistance, liver steatosis, and inflammation [52] . furthermore, er stress could increase insulin resistance through induction of lipin-2 expression, which is a phosphatase enzyme that catalyzes biosynthesis of dag leading to activation of dag/pkcε axis [54] . interestingly, upr could also increase liver steatosis through activation of srebp-1c signaling pathway [53] . elevated ros and upr are well-identified pathways that could induce hepatocytes death in nash. hepatocytes apoptosis and necroptosis are the main forms of cell death in human steatohepatitis and diet-induced mouse models of nash [55] . the key fibrogenic liver cells, hepatic stellate cells (hscs), usually exist in a quiescent state and get activated by engulfment of apoptotic bodies, the inflammatory milieu, or damage-associated molecular patterns (damps) released from stressed and dying hepatocytes [56] . interestingly, ffa-mediated lipotoxic effects stimulate hepatocytes to release extracellular vesicles (evs) with distinctive micrornas (mirna) profile that increase the expression of fibrogenic genes in the surrounding hscs [57] (figure 3 ). free cholesterol could directly sensitize hscs to the action of tumor growth factor (tgf)-β, a potent fibrogenic cytokine [58] . treatment of human and rat immortalized hscs cell lines with saturated fatty acid increased the expression of various profibrogenic genes [59] . macrophages aggregate as well around dead hepatocytes forming a crown-like structure, a phenomenon that exists only in persons with nash but not in those with simple steatosis [60] . recruitment of more inflammatory cells from systemic circulation is facilitated by "find me" signals that are released from dead cells [61] . inhibition of inflammatory monocytes recruitment via inhibition of c-c chemokine receptors type 2 and type 5 (ccr2/ccr5) suppressed fibrogenesis and steatohepatitis in murine nash [62] . macrophages can modulate also hepatic insulin resistance and favor tag accumulation in hepatocytes through secretion of il-1β that downregulates peroxisome proliferator-activated receptor (ppar) α, a key transcriptional pathway involved in fatty acid oxidation [63] . liver sinusoidal cells (lsecs) are fenestrated cells that exist in close vicinity to hepatocytes, j o u r n a l p r e -p r o o f macrophages and hscs, which, under physiological conditions, regulate lipid transport, maintain the quiescence of kupffer cells, resident liver macrophages, and hscs [64] . at early stage of nafld, lsecs lose their fenestrae, a process termed capillarization, which could favor liver steatosis and initiate hscs activation [64] (figure 3 ). during nash, lsecs display a pro-inflammatory phenotype that promotes steatohepatitis [64] . autophagy is a self-degradative process which is used by the cells to remove misfolded proteins and damaged organelles [65] . singh et al. showed that the cells can use autophagic process as lipolytic mechanism to mobilize lipids from intracellular lipid store, which is termed in this case "macrolipophagy" [66] . various in vitro and in vivo studies showed that autophagy was decreased in fatty hepatocytes [67] . impairment of autophagy by palmitic acid in macrophages induces inflammatory il-1β production [68] . on the other side, selective loss of autophagic activity reduced liver fibrogenesis in cultured hscs [69] and protected against diet-induced insulin resistance [70] . the results highlight that the net effect of autophagy on nafld might depend on the tissue or type of the cells that show autophagic dysfunction and the stage of nafld. the liver biopsy is considered the gold standard for nafld diagnosis, especially for distinguishing steatosis from inflammation and fibrosis [2] . nevertheless, this technique has several limitations not only resulting from the invasive procedure and rare post-interventional complications, but also due to the small tissue volume, which might not be representative for the whole liver and may not take into account inhomogeneous distribution of nafldassociated alterations. novel imaging modalities such as ultrasound-or mr-based techniques are of increasing value, as recently reviewed [71] , but are still not generally available, so that there is an urgent need for noninvasive screening tools. non-invasive detection of nash and fibrosis remains challenging today. biomarker-based panels such as aspartate aminotransferase (ast)/platelets count ratio index, fibrosis-4 (fib-4) index, fibrotest, fibrospect ii, and nafld fibrosis score (nfs) offer variable diagnostic efficacy for assessing different stages of liver fibrosis [73, 74] . although combination of these panels could enhance their predictive values [73] , they still suffer from limited accuracy even compared to the alanine aminotransferase (alt) and ast, particularly in t2dm [75] . in this regard, transient elastography looks like a promising alternative in diabetes clinics for detection of liver fibrosis in nafld [74] . numerous biomarkers have been developed to specifically track features of nash progression and fibrosis. cytokeratin (ck) 18, an intermediate filament protein that is cleaved during cell death to ck18 m30 and ck18 m65, has been intensively investigated as a surrogate of nash-associated liver cell damage, but a recent meta-analysis of 25 studies reported a maximum sensitivity of 0.75 for nash diagnosis [76] and suboptimal diagnostic value was shown in t2dm [75] . the ecm turnover marker, type iii procollagen, can offer a diagnostic efficacy of 0.81 and 0.88 to detect moderate and advanced liver fibrosis in t2dm, respectively [77] . in 2016, the european associations for the study of the liver, obesity and diabetes (easl-easo-easd) jointly released recommendations for diagnosis and monitoring of disease severity in persons with suspected nafld and metabolic risk factors [78] . people with metabolic risk factors, such as t2dm, should undergo assessment by abdominal ultrasound, serum transaminases and fibrosis markers (e. g. fib-4, nfs). elevated transaminases or steatosis plus abnormal fibrosis test shall require referral to a specialist. this strategy has raised the question of a possible overreferral when adhering to these guidelines [79] . however, recent analyses show that a refined strategy of specific combining indices such as fli and fib-4 could reduce the number of people with t2dm for further diagnostic work up to a reasonable size [80] . this retrospective analysis also found that certain non-invasive biomarkers are consistently associated with different patterns of diabetes-related complications. analyses of the plasma metabolomic of insulin-resistant individuals with nafld suggested that bile salts, e. g. glycocholate, taurocholate, and glycochenodeoxycholate allow to detect nash in one study [81] , while another study reported an association with insulin resistance j o u r n a l p r e -p r o o f but not with liver necroinflammation [82] . also amino acids, specifically a glutamate-serineglycine index, was associated with hepatic insulin resistance and transaminases and discriminated individuals with fibrosis grade 3-4 from those with grade 0-2 independently of bmi [83] . the diagnostic performance of a serum-based lipidomic analysis was substantially lower for nafld detection in t2dm compared to healthy individuals [84] . nevertheless, certain sphingolipid species were recently found to be increased in insulin-resistant nash and to correlate with hepatic oxidative stress and inflammation [85] . one circulating small noncoding rna, mirna-122, was found to be more than 5.7fold in steatosis and further doubled in nash [86] . this mirna was also higher in t2dm with nafld than in those without nafld and provided better prediction of nafld when combined with ldl and waist-to-hip ratio [87] . moreover, extracellular vesicles (ev), which among other cargo also transport mirna, may be promising biomarkers for nafld as shown by higher serum levels in people with nafld, obesity and diabetes [107] . recently, metagenomics data derived from gut microbiota alterations allowed to detect advanced fibrosis in 86 nafld patients, of whom 23% had t2dm, with a robust diagnostic accuracy (auroc: 0.936) [88] . the current guidelines recommend only lifestyle modification and -for certain groupsbariatric or metabolic surgery to treat nafld [1, 2] . although the numerous activities in this field, no pharmacological treatment is currently approved or expecting approval for the use in nafld with or without concomitant t2dm (table 1 and 2), except for obeticholic acid (oca). marketing authorization application for oca has been submitted to the u.s. food and drug administration (fda) and european medicines agency (ema), awaiting fda decision by june 2020 [89] . against this background, current guidelines and recommendations primarily advise lifestyle modification (healthy nutrition and exercise) and weight loss in overweight/obese persons. the easl-easo-easd guidelines recommend to consider pharmacological treatment in people with nash when combined with fibrosis and in those with less severe disease, but high risk conditions for disease progression such as t2dm [78] . the american association for the study of liver diseases (aasld) recommends to limit pharmacological treatment to those with biopsy-proven nash and fibrosis [1] . j o u r n a l p r e -p r o o f weight management and physical exercise are key to the treatment of both nafld and t2dm. a proof-of-concept study showed that a hypocaloric diet with weight loss of ~8 kg within 12 weeks not only normalized fasting egp and thereby hyperglycemia, but decreased hepatic tag content down to normal concentrations in obese t2dm humans with nafld [90] . subsequent studies in larger cohorts extended these results by demonstrating that a very low-caloric diet with weight loss of about 15% rapidly normalized liver fat content in 90 in dividuals with t2dm, which persisted for one year if weight loss was maintained [91] . interestingly, mediterranean, low-saturated fat and high plant-based protein diets also improve steatosis in nafld combined with t2dm despite minor or no relevant weight loss [92, 93] . in addition, physical activity and exercise training interventions can also decrease liver fat content, which may not be exclusively depending on concomitant weight loss [94] . although the beneficial effects of structured behavioral treatment to improve histological endpoints, likely extend beyond reduction of hepatic fat content to ameliorating the grade and stage of inflammation and fibrosis [95] , only a minority of the people manages to adhere to dietary weight loss and exercise programs, which raises the issue of other therapeutic approaches [94] . weight-loss inducing drugs could be an attractive option for persons with nafld with a bmi > 30 kg/m 2 or >27 kg/m 2 in the presence of at least one metabolic comorbidity, as an adjunct treatment to lifestyle modifications [96, 97] . currently, the most-popular weight-loss inducing medications associated with at least 5% body weight decrease in one year as compared to placebo are orlistat, the fixed combination of phentermine and topiramate or naltrexone and bupropion, and the glucagon-like peptide-1 (glp-1) receptor agonist (glp-1ra), liraglutide [97] . of these drugs, orlistat treatment failed to improve liver histology when compared to placebo [98] , while no reports are available for topiramate, naltrexone, bupropion and phentermine regarding hepatic endpoints in humans with nafld [99] . only bariatric or metabolic surgery is a therapeutic option to induce sustained weight loss partricularly in people with combined nafld and t2dm. in obese humans, bariatric surgery resulted in 85% resolution of nash within one year [101] and in 77% complete remission of t2dm [102] . surgical weight loss improves glucose metabolism and insulin sensitivity by different mechanisms such as increased glp-1 secretion [103] and epigenetic modification [104, 105] . several antihyperglycemic drug classes were or are currently being investigated in clinical trials and preclinical models to evaluate their efficacy for people with nafld and with or without t2dm. metformin reduces body weight, hepatic gluconeogenesis -by yet unclear mechanisms [106] , and the risk of macrovascular complications, which is still controversially discussed due to lack of optimally designed clinical trials [116] . despite its action on hepatic metabolism, former small-scale studies reported conflicting results [109, 110] (table 1 ) and recent metaanalysis failed to demonstrate any effect of metformin on liver histology [111] . nevertheless, epidemiological, observational and preclinical studies suggest that metformin may reduce the risk of hcc and also in t2dm, possibly by promoting apoptosis, but controlled clinical trials are not available [112] . dpp4 degrades incretins such as glp-1 so that dpp-4i treatment increases the postprandial levels of endogenous glp-1, which leads to lower glucose peaks after meals [113, 114] . in individuals with nafld with prediabetes or recent onset diabetes, sitagliptin did not improve liver steatosis or liver fibrosis compared to placebo as assessed by mr-based techniques [115] . in line, another recent trial reported no benefits for sitagliptin versus placebo on liver fibrosis or steatohepatitis in t2dm [116] (table 1) . in contrast, a moderate reduction in liver fat content was observed with vildagliptin in individuals with t2dm [117] . j o u r n a l p r e -p r o o f 14 the actions of endogenous glp-1 are mimicked by glp-1 receptor agonists (glp-1ra), which effectively reduce blood glucose levels and also reduce the risk for cvd in t2dm [118] . in individuals with nafld and t2dm, liraglutide in combination with metformin reduced liver, subcutaneous, and visceral fat [119] . also, liraglutide improved hepatic steatosis measured by mr-based methods as well as resolved biopsy-proven nash without worsening of fibrosis [100, 120] (table 1) . however, a recent subanalysis did not detect an effect of liraglutide on liver fat content quantified by 1 h-mrs [121] (table 1) . respective trials with semaglutide and dulaglutide are still waiting for results (nct02970942, nct03648554). in an animal model of t2dm, exenatide also counteracted hcc development by suppression of stat3-regulated genes [122] . glucose-dependent insulinotropic polypeptide (gip) represents the second important incretin with proposed beneficial effects on peripheral energy metabolism [123] . tirzepatide, a novel dual agonist for gip and glp-1 receptors with probably greater efficacy than glp-1ra [124] , decreased transaminases and surrogate markers of liver injury paralleled by increased circulating adiponectin levels in people with t2dm [125] . a clinical trial on nash resolution is currently ongoing in persons with nash with or without t2dm (nct04166773). sglt2i inhibit reabsorption of glucose in the proximal renal tubule resulting in glucosuria and calory loss, thus effectively reducing blood glucose level and body weight in t2dm. moreover, sglt2is show beneficial effects on cardiovascular risk and progression of nephropathy [118, 126] . most, but not all recent randomized controlled trials (rcts) showed that sglt2i treatment resulted in reduction in liver fat content compared to placebo [127] [128] [129] [130] [131] (table 1) . in an open-label pilot study in liver-biopsy proven cohort of nash with t2dm, treatment with empagliflozin for 6 months reduced liver steatosis, ballooning and fibrosis and induced nash resolution in approximately half of those persons [132] . animal models further suggested anti-inflammatory, anti-oxidant and pro-apoptotic actions of sglt2i with cardio-protective effects as well as inhibition of nash progression and tumor growth of hcc [133, 134] . the dual sglt1/2i, licogliflozin, is expected to block both intestinal and renal glucose (re)absorption [135] and currently investigated to evaluate its efficacy on resolution of nash as monotherapy and as combination therapy with the fxr agonist, tropifexor, in people with nash and fibrosis (nct04065841). first results hint at improvement of transaminases and reduction of steatosis by licogliflozin in nash [136] . ppars is a family of nuclear receptors composed of multiple isoforms with wide tissue distribution [137] . the ppar-γ agonist pioglitazone had convincing efficacy on nash resolution in individuals with and without t2dm, but with conflicting results on fibrosis [138] [139] [140] (table 1) . of note, pioglitazone has been withdrawn in many european countries because of its disadvantageous safety profile [231] . however, pioglitazone exerts beneficial effects on cardiovascular outcomes in persons with t2dm and a history of cvd [141] . it has been proposed that non-ppar-γ dependent mechanisms, as the inhibition of the mitochondrial pyruvate carrier (mpc), might mediate the beneficial effects of pioglitazone on nafld [142] . however, a novel drug with ppar-γ sparing effects and mpc binding activity did not improve histological components of nash in individuals with t2dm compared to placebo [143] . elafibranor is a dual agonist for ppar-α and ppar-δ without ppar-γ stimulation [144] . based on a post-hoc analysis, nash was resolved without worsening of fibrosis in a higher percentage of people with and without t2dm in the elafibranor group as compared to the placebo [145] and a follow-up study on these findings has been initiated ( table 2) . recent announcements on an interim analysis state that elafibranor treatment failed to resolve nash and improve fibrosis when compared to placebo [146] . saroglitazar is another dual ppar-α/γ agonist with higher affinity for ppar-α. in a mouse model of nash, saroglitazar reduced liver steatosis, inflammation and prevented fibrosis development and a respective clinical trial is ongoing [147] ( table 2) . lanifibranor is a pan-ppar agonist for ppar-α, β, and γ receptors focused on treatment of liver fibrosis and nash (nct03008070). in an animal model of liver fibrosis, lanifibranor decreased hepatic collagen deposition [148] . several other strategies for pharmacological targeting of nash have emerged over the last few years; however, these strategies are not specifically designed for t2dm, but for the whole nafld collective. they comprise antiinflammatory drugs, but also modulators of other pathways, which are briefly summarized in the following sections. j o u r n a l p r e -p r o o f fxr can be activated by bile acids in a negative feedback mechanism to suppress bile acid synthesis [40] . oca is a potent semisynthetic and selective fxr agonist approved for treatment of primary biliary cholangitis [149] . oca treatment resulted in histologic improvement of nash in people with and without t2dm compared to placebo [150, 151] ; however, concerns were raised about oca-induced changes in plasma lipoprotein profile [152] . tropifexor, another potent fxr agonist [153] , is currently being tested in combinatorial approaches of nash treatment (cenicriviroc and licogliflozin; nct03517540). oltipraz is a synthetic dithiolethione with antisteatotic effects by inhibiting the activity of lxr-α. it activates adenosine monophosphate activated protein kinase (ampk) and inactivates s6k1, affecting lxr-α thus reducing lipogenesis and increasing lipid oxidation [154] . a recent 24-week phase 2 clinical trial found decreased steatosis measured by 1 h-mrs with oltipraz compared to placebo treatment [154] and a respective phase 3 clinical trial is ongoing ( table 2 ). chemokine receptors type 2 (ccr2) and type 5 (ccr5) are expressed on various inflammatory and fibrogenic cells [155] . cenicriviroc is a ccr2/crr5 dual antagonist that reduced insulin resistance, liver inflammation and fibrosis in diet-induced models of nash [62] . in recent rcts in a nash cohort with fibrosis, cenicriviroc treatment did not improve nas but may reduce liver fibrosis [156, 157] . currently, there is an ongoing clinical trial to evaluate the effects of cenicriviroc on fibrosis in nash ( table 2) . both people with obesity, metabolic syndrome or t2dm as well as those with nafld are at increased risk for dyslipidemia. statins, inhibitors of 3-hydroxy-3-methyl-glutaryl-coenzyme a (hmg-coa) reductase, are generally safe and have unmet efficacy to decreased serum ldl and prevent cardiovascular outcomes, despite slightly increasing the risk of t2dm [2] . use of statins associated with a 46% lower relative risk of hepatic decompensation and mortality in cirrhosis and a trend towards lower fibrosis progression in non-cirrhotic liver diseases [158] . however, the data on liver histology ist limited [159] so that statins are not currently recommended for the management of nafld [2] . the inhibitor of intestinal j o u r n a l p r e -p r o o f cholesterol absorption, ezetimibe, decreased the histological nas, but not consistently liver fat content in an analysis of the few available studies [160] . fenofibrate, a ppar-α agonist, does not affect or even increase liver fat content or volume [161, 162] . nevertheless, the combination of statins with certain anti-nash drugs, such as oca, could be beneficial to counteract drug-related increases in ldl during long-term treatment. inhibition of dnl in nafld may be achieved by inhibition of acc as this enzyme catalyzes the conversion of acetyl coa into malonyl coa, which acts as a substrate for fatty acid synthesis and inhibitor for fatty acid β-oxidation [163] . in a recent clinical trial in individuals with nash with and without t2dm, treatment with the dual acc1 and acc2 inhibitor gs-0976 decreased liver steatosis without improvement of fibrosis [164] . the major concern of this strategy is that decreased dnl in nafld might channel lipids towards other harmful directions, e.g. increased blood lipids [163] . scd1 is a key enzyme for hepatic lipogenesis that catalyzes the conversion of saturated fatty acids to mufa and its downregulation protected mice from high carbohydrate-induced liver steatosis [165] . a clinical trial with aramchol, an inhibitor of scd1, showed a reduction in liver fat content, resolution of nash and improvement of liver fibrosis in persons with nafld with prediabetes or t2dm [166] . these results paved the way for a respective phase 3 clinical trial ( table 2) . mitochondrial uncoupling describes any process that uncouples the electron transport from atp synthesis in mitochondria [167] . 2,4-dinitrophenol (dnp) was widely used for the treatment of obesity before its discontinuation due to life-threatening serious adverse events [168] . to overcome the side effects of dnp, improved formulas of dnp were recently developed to decrease the toxic to effective dose ratio (dnp-methyl ether (dnpme) and controlled-release mitochondrial protonophore (crmp)) [169, 170] . oral crmp targets mainly the liver due to the first-pass effect and decreased hepatic insulin resistance, hepatic steatosis and liver fibrosis in a methionine-choline deficient rat model of nash [170] . crmp was also effective in nonhuman primates with diet-induced nafld for reduction of hepatic steatosis and egp [171] . thyroid hormone deficiency has been associated with nafld development [172] . thyroid hormone analogues decreased liver fat, liver transaminases, and inflammatory and fibrosis markers in animal models of nash [172] . resmetirom is a liver-targeted highly selective thr-β agonist which showed efficacy in reducing liver fat content in nash with and without t2dm [173] . currently, there is ongoing clinical trial for evaluation of long-term outcomes of resmetirom and its efficacy on nash resolution ( table 2 ). vitamin e is a potent antioxidant [174] . in nash without t2dm, vitamin e improved nas without worsening of fibrosis [139] . despite concerns regarding adverse effects of long term vitamin e usage, treatment with vitamin e for ≥2 years reduced the risk of liver failure in a nash cohort with advanced fibrosis and with or without t2dm [175] . therapeutic manipulation of intestinal microbiome is still in its infancy. rodent data showed efficacy for fecal microbiota transplantation in improving nafld in a diet-induced nash model [176] . also, modulation of the intestinal microbiota by antibiotic treatment reduced liver transaminases in nafld [177] . the use of prebiotics and probiotics in obese nafld/nash is currently not supported by high-quality clinical studies with mr-or biopsy-based endpoints [178]. the evidence for shared pathophysiological mechanisms between t2dm and nafld will help to develop strategies for detecting and treating both diseases and preventing their leading complication, cvd. altered lipid and energy metabolism, insulin resistance, low-grade inflammation and intestinal dysbiosis represent key targets. in addition to weight loss by lifestyle modification or bariatric surgery, glp-1ra and sglt2i are promising antihyperglycemic concepts with beneficial effects on nafld and cvd. in addition, many j o u r n a l p r e -p r o o f metabolism-based drugs are currently studied comprising ppar agonists, endocrine dual coagonists to modulators of hepatic metabolism or microbiota. nevertheless, several roadblocks need to be overcome to reduce the burden of nafld in t2dm. first, there is still lack of preclinical animal models that encapsulate essential features of human nash and diabetes. second, available biomarkers lack diagnostic efficacy to identify nafld progression. innovative strategies such as cluster analysis already enabled detection of a diabetes subtype (sird) with high risk of nafld [14] . combination with computational integration of multiomics data shall identify specific disease signatures and pave the way to precision medicine and targeted management of t2dm and nafld. finally, studies on so-called endpoints are scarce, which may be due to the need of long-term studies to evaluate liver-related mortality, to the current neglect to accept cvd morbidity and mortality as nafld outcome and to ongoing discussions on the relevance of surrogate markers. the research of the authors is supported in part by grants from the german federal ministry phase iii registered interventional trials on "clinicaltrials.gov" for nafld as accessed on 10 th april 2020. bl, baseline; ccr2/5, c-c chemokine receptors type 2 and type 5; fxr, farnesoid x receptor; hba 1c , glycated haemoglobin; lxr, liver x receptor; mpc, mitochondrial pyruvate carrier; na, data not available; nafld, non-alcoholic fatty liver disease; nfs, nafld fibrosis score; ppar, peroxisome proliferator-activated receptor; nash, non-alcoholic steatohepatitis; scd, stearoyl-coa desaturase; sglt, sodium-glucose cotransporter; thr, thyroid hormone receptor; t2dm, type 2 diabetes. *only placebo-controlled, randomized clinical trials are listed, except for saroglitazar, a 4-arm active-controlled study. the diagnosis and management of nonalcoholic fatty liver disease: practice guidance from the american association for the study of liver diseases easl-easd-easo clinical practice guidelines for the management of non-alcoholic fatty liver disease global epidemiology of nonalcoholic fatty liver disease-meta-analytic assessment of prevalence, incidence, and outcomes exomewide association study identifies a tm6sf2 variant that confers susceptibility to nonalcoholic fatty liver disease high prevalence of nonalcoholic fatty liver disease in 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anticipated nash drug has to wait for its fda hearing, thanks to covid-19 reversal of nonalcoholic hepatic steatosis, hepatic insulin resistance, and hyperglycemia by moderate weight reduction in patients with type 2 diabetes remission of human type 2 diabetes requires decrease in liver and pancreas fat content but is dependent upon capacity for β cell recovery ad libitum mediterranean and low-fat diets both significantly reduce hepatic steatosis: a randomized controlled trial isocaloric diets high in animal or plant protein reduce liver fat and inflammation in individuals with type 2 diabetes treatment of nafld with diet, physical activity and exercise fatty liver italian network. behavior therapy for nonalcoholic fatty liver disease: the need for a multidisciplinary approach association of pharmacological treatments for obesity with weight loss and adverse events: a systematic review and meta-analysis efficacy of orlistat in non-alcoholic fatty liver disease: a systematic review and 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randomized trial pioglitazone, vitamin e, or placebo for nonalcoholic steatohepatitis randomized, placebocontrolled trial of pioglitazone in nondiabetic subjects with nonalcoholic steatohepatitis pioglitazone for the primary and secondary prevention of cardiovascular and renal outcomes in patients with or at high risk of type 2 diabetes mellitus: a meta-analysis targeting metabolism, insulin resistance, and diabetes to treat nonalcoholic steatohepatitis insulin sensitizer msdc-0602k in non-alcoholic steatohepatitis: a randomized, double-blind, placebo-controlled phase iib study the opportunities and challenges of peroxisome proliferator-activated receptors ligands in clinical drug discovery and development elafibranor, an agonist of the peroxisome proliferator-activated receptor-α and -δ, induces resolution of nonalcoholic steatohepatitis without fibrosis worsening announces-results-from-interim-analysis-of-resolve-it-phase-3-trial-of-elafibranor-in-adultswith-nash-and-fibrosis.html dual pparα/γ agonist saroglitazar improves liver histopathology and biochemistry in experimental nash models synthesis , and evaluation of a novel series of indole sulfonamide peroxisome proliferator activated receptor (ppar) α/γ/δ triple activators: discovery of lanifibranor, a new antifibrotic clinical candidate targeting fxr in cholestasis obeticholic acid for the treatment of non-alcoholic steatohepatitis: interim analysis from a multicentre, randomised, placebo-controlled phase 3 trial farnesoid x nuclear receptor ligand obeticholic acid for non-cirrhotic, non-alcoholic steatohepatitis (flint): a multicentre, randomised, placebo-controlled trial impact of obeticholic acid on the lipoprotein profile in patients with non-alcoholic steatohepatitis discovery of tropifexor (ljn452), a highly potent non-bile acid fxr agonist for the treatment of cholestatic liver diseases and nonalcoholic steatohepatitis (nash) randomised clinical trial: the efficacy and safety of oltipraz, a liver x receptor alpha-inhibitory dithiolethione in patients with nonalcoholic fatty liver disease cenicriviroc for the treatment of non-alcoholic steatohepatitis and liver fibrosis a randomized, placebo-controlled trial of cenicriviroc for treatment of nonalcoholic steatohepatitis with fibrosis cenicriviroc treatment for adults with nonalcoholic steatohepatitis and fibrosis: final analysis of the phase 2b centaur study statin use and risk of cirrhosis and related complications in patients with chronic liver diseases: a systematic review and meta-analysis prescription of statins in suspected non-alcoholic fatty liver dise ase and high cardiovascular risk, a population-based study ezetimibe decreased nonalcoholic fatty liver disease activity score but not hepatic steatosis effect of fenofibrate and niacin on intrahepatic triglyceride content, ve ry low-density lipoprotein kinetics, and insulin action in obese subjects with nonalcoholic fatty liver disease effects of free omega-3 carboxylic acids and fenofibrate on liver fat content in patients with hypertriglyceridemia and non-alcoholic fatty liver disease: a double-blind, randomized, placebo-controlled study acetyl coa carboxylase inhibition reduces hepatic steatosis but elevates plasma triglycerides in mice and humans: a bedside to bench investigation acetyl -coa carboxylase inhibitor gs-0976 for 12 weeks reduces hepatic de novo lipogenesis and steatosis in patients with nonalcoholic steatohepatitis hepatic stearoyl-coa desaturase-1 deficiency protects mice from carbohydrate-induced adiposity and hepatic steatosis one-year results of the global phase 2b randomized placebo-controlled arrest trial of aramchol, a stearoyl coa desaturasemodulator in nash patients n mitochondrial uncoupling and lifespan emerging pharmacological targets for the treatment of nonalcoholic fatty liver disease, insulin resistance, and type 2 diabetes reversal of hypertriglyceridemia, fatty liver disease and insulin resistance by a liver-targeted mitochondrial uncoupler controlled-release mitochondrial protonophore reverses diabetes and steatohepatitis in rats controlledrelease mitochondrial protonophore (crmp) reverses dyslipidemia and hepatic steatosis in dysmetabolic nonhuman primates nonalcoholic fatty liver disease and hypercholesterolemia: roles of thyroid hormones, metabolites, and agonists mgl-3196) for the treatment of non-alcoholic steatohepatitis: a multicentre, randomised, double-blind, placebo-controlled, phase 2 trial nonalcoholic fatty liver disease and diabetes: part ii: treatment vitamin e improves transplant-free survival and hepatic decompensation among patients with nonalcoholic steatohepatitis and advanced fibrosis total fecal microbiota transplantation alleviates high-fat diet-induced steatohepatitis in mice via beneficial regulation of gut microbiota efficacy of rifaximin on circulating endotoxins and cytokines in patients with nonalcoholic fatty liver disease key: cord-254404-lrsqrc2u authors: yañez-guerra, luis alfonso; zhong, xingxing; moghul, ismail; butts, thomas; zampronio, cleidiane g; jones, alexandra m; mirabeau, olivier; elphick, maurice r title: echinoderms provide missing link in the evolution of prrp/snpf-type neuropeptide signalling date: 2020-06-24 journal: elife doi: 10.7554/elife.57640 sha: doc_id: 254404 cord_uid: lrsqrc2u neuropeptide signalling systems comprising peptide ligands and cognate receptors are evolutionarily ancient regulators of physiology and behaviour. however, there are challenges associated with determination of orthology between neuropeptides in different taxa. orthologs of vertebrate neuropeptide-y (npy) known as neuropeptide-f (npf) have been identified in protostome invertebrates, whilst prolactin-releasing peptide (prrp) and short neuropeptide-f (snpf) have been identified as paralogs of npy/npf in vertebrates and protostomes, respectively. here we investigated the occurrence of npy/npf/prrp/snpf-related signalling systems in a deuterostome invertebrate phylum – the echinodermata. analysis of transcriptome/genome sequence data revealed loss of npy/npf-type signalling, but orthologs of prrp-type neuropeptides and snpf/prrp-type receptors were identified in echinoderms. furthermore, experimental studies revealed that the prrp-type neuropeptide pqdrskamqaertgqlrrlnprf-nh(2) is a potent ligand for a snpf/prrp-type receptor in the starfish asterias rubens. our findings indicate that prrp-type and snpf-type signalling systems are orthologous and originated as a paralog of npy/npf-type signalling in urbilateria. neuropeptides are neuronally secreted signalling molecules that regulate many physiological processes and behaviours in animals, including feeding, digestion, reproduction and social behaviour. they typically exert effects by binding to cognate g-protein coupled receptors (gpcrs) on target cells, which leads to changes in the activity of downstream effectors (e.g. ion channels, enzymes) (jékely et al., 2018) . investigation of the evolution of neuropeptide signalling has revealed that many of the neuropeptide systems found in vertebrates have orthologs in invertebrate deuterostomes (urochordates, cephalochordates, hemichordates, echinoderms) and protostomes (e.g. arthropods, nematodes, molluscs, annelids, platyhelminthes). thus, the evolutionary origin of over thirty neuropeptide signalling systems has been traced back to the common ancestor of the bilateria (urbilateria) (jékely, 2013; mirabeau and joly, 2013; elphick et al., 2018) . one of the neuropeptide systems that originated in urbilateria is neuropeptide y (npy)-type signalling. npy is a 36-residue peptide that was first isolated from the porcine hypothalamus tatemoto, 1982) but which is also expressed by neurons in many other regions of the nervous system (adrian et al., 1983; morris, 1989) and in peripheral organs such as the gut and cardiovascular system (holzer et al., 2012; farzi et al., 2015) . accordingly, npy is pleiotropic (pedrazzini et al., 2003) , although it is most widely known as a potent stimulant of food snpf-type signalling may be restricted to protostomes (mirabeau and joly, 2013) . subsequently, snpf-type peptides and a cognate receptor have been characterised in the bivalve mollusc crassostrea gigas, confirming the occurrence of this signalling system in the lophotrochozoan branch of the protostomes (bigot et al., 2014) . furthermore, the physiological roles of snpf-type neuropeptides have been characterised in c. gigas and in other molluscs (hoek et al., 2005; zatylny-gaudin et al., 2010; bigot et al., 2014) . important insights into neuropeptide evolution have been obtained recently by pharmacological characterisation of g-protein coupled neuropeptide receptors in invertebrate deuterostomes (kawada et al., 2010; roch et al., 2014; bauknecht and jékely, 2015; semmens et al., 2015; tian et al., 2016; yañez-guerra et al., 2018) . however, currently little is known about the occurrence and characteristics of npy/npf/prrp/snpf-related signalling systems in invertebrate deuterostomes. phylogenetic analysis of bilaterian g-protein coupled neuropeptide receptors has demonstrated the occurrence of npy/npf receptor-related proteins in ambulacrarians -the echinoderm strongylocentrotus purpuratus and the hemichordate saccoglossus kowalevskii (mirabeau and joly, 2013) . furthermore, the precursor of a putative npy/npf-type peptide was identified in s. kowalevskii (mirabeau and joly, 2013; elphick and mirabeau, 2014) . a candidate npy/npf-type precursor has also been identified in the cephalochordate branchiostoma floridae, but an npy/npf-type receptor has yet to be identified in this species (mirabeau and joly, 2013; elphick and mirabeau, 2014) . a more recent finding was the discovery of a family neuropeptide precursor-type proteins in echinoderms that contain a peptide that shares sequence similarity with npy/npf-type peptides (zandawala et al., 2017) . however, it is not known if these proteins are orthologs of vertebrate npy-type precursors and protostome npftype precursors. to address this issue, detailed analysis of the sequences of the echinoderm npy/npf-like peptides and precursors and the genes encoding these peptides/proteins is needed. furthermore, the receptors for echinoderm npy/npf-like peptides need to be identified. accordingly, here we show that npy/npf-type signalling has in fact been lost in echinoderms and report the discovery and pharmacological characterisation of a prrp/snpf-type signalling system in an echinoderm -the starfish asterias rubens. these findings provide important new insights into the evolution of neuropeptide signalling in the bilateria. the sequence of a transcript (contig 1060225; genbank accession number mk033631.1) encoding the precursor of an npy-like neuropeptide has been reported previously based on analysis of neural transcriptome sequence data from the starfish a. rubens (zandawala et al., 2017) . here, a cdna encoding this precursor was cloned and sequenced, revealing that the open reading frame encodes a 108-residue protein comprising a predicted 19-residue signal peptide, a 23-residue npy-like peptide sequence with an n-terminal glutamine residue and a c-terminal glycine residue, followed by a putative monobasic cleavage site (figure 1-figure supplement 1a) . analysis of radial nerve cord extracts using mass spectrometry (lc-ms-ms) revealed the presence of a peptide with the structure pqdrskamqaertgqlrrlnprf-nh 2 , showing that the n-terminal glutamine and c-terminal glycine in the precursor peptide are post-translationally converted to a pyroglutamate residue and an amide group, respectively ( figure 1-figure supplement 1b) . alignment of the sequences of the a. rubens neuropeptide and orthologs from other echinoderms with related peptides in other taxa revealed that they share sequence similarity with both prrp-type neuropeptides ( figure 1a ) and with npy/npf-type neuropeptides ( figure 1b) . however, the echinoderm peptides comprise 22-25 residues and are similar in length to vertebrate prrps, which are 20-31 residues as full-length peptides and in some species can occur as n-terminally truncated peptides due the presence of a monobasic cleavage site (hinuma et al., 1998; tachibana and sakamoto, 2014) . this contrasts with npy/npf-type neuropeptides, which are longer peptides ranging in length from 36 to 40 residues (fadda et al., 2019) . furthermore, by analysing sequence data from the hemichordate s. kowalevskii and the cephalochordate b. floridae, here we identified novel neuropeptides that share sequence similarity with the echinoderm figure 1 . comparison of the sequences of echinoderm npy/npf/prrp-like peptides with related peptides in other taxa. (a) comparison with prrp-type neuropeptides. conserved residues are highlighted in black (identical) or grey (conservative substitutions) (b) comparison with npy/npf-type neuropeptides. conserved residues are highlighted in black (identical) or grey (conservative substitutions). the arrowheads indicate residues that have been shown to be important for the three-dimensional structure of the npy/npf-type peptides but which are not present in the echinoderm peptides. the colour coding of phyla is as follows: dark blue (echinodermata), light blue (hemichordata), purple (chordata), orange (platyhelminthes), red (lophotrochozoa), yellow (priapulida), green (arthropoda), grey (nematoda). the full names of the species and the accession numbers of the sequences are listed in figure 1 -source data 1. figure 1 continued on next page neuropeptides and with vertebrate prrps ( figure 1a) . thus, sequence alignment reveals that, in addition to a shared characteristic of a c-terminal rfamide or a ryamide (y and f being conservative substitutions), there are other residues in the echinoderm peptides that are identical or structurally similar to equivalently positioned residues in chordate prrps ( figure 1a) . contrastingly, the echinoderm peptides lack two proline (p) residues that are a conserved feature of the n-terminal region of many npy/npf-type peptides, with the exception of some peptides that have only one of these proline residues and a peptide in the cephalochordate branchiostoma floridae that has neither ( figure 1b) . furthermore, there are four other residues that are highly conserved in bilaterian npy/npf-type peptides -tyrosine (y), leucine (l), tyrosine (y), and isoleucine (i) residues, which are marked with arrowheads in figure 1b . these residues have been shown to be important for the formation of the three-dimensional structure in vertebrate npytype peptides (blundell et al., 1981; glover et al., 1983; glover et al., 1984; allen et al., 1987) , so these residues may likewise be important for npf receptor activation and bioactivity. importantly, none of these residues are present in the echinoderm peptides. it is noteworthy, however, that all but one of the aforementioned six conserved residues in npy/ npf-type peptides are present in a peptide from a species belonging to a sister phylum of the echinoderms -the hemichordate saccoglossus kowalevskii ( figure 1b ; mirabeau and joly, 2013; elphick and mirabeau, 2014) . collectively these findings indicate that the echinoderm neuropeptides originally described as npy-type peptides (zandawala et al., 2017) are not orthologs of npy/ npf-type peptides but are orthologs of chordate prrp-type peptides. therefore, henceforth we will refer to the a. rubens neuropeptide pqdrskamqaertgqlrrlnprf-nh 2 as arprrp and we will refer to orthologs in other echinoderms equivalently. echinoderm prrp-like peptide genes have the same exon-intron structure as chordate prrp genes to investigate further the proposition that arprrp and other echinoderm prrp-like neuropeptides are orthologs of chordate prrps, we compared the exon-intron structure of genes encoding these peptides ( figure 2 ). this revealed that a common characteristic is the presence of an intron that interrupts the coding sequence at a position corresponding to the n-terminal or central region of the echinoderm prrp-like peptides and vertebrate prrps. furthermore, in echinoderm prrp-like peptide genes and vertebrate prrp genes the intron interrupts the coding sequence in the same frame, at a position between the first and second nucleotide of the interrupted codon (a phase one intron), which is denoted by +1 in figure 2 . genes encoding novel precursors of prrp-like peptides in s. kowalevskii and b. floridae also have a phase one intron. furthermore, in the b. floridae gene and in one of the s. kowalevskii genes (skow 2) the intron is located in the region of the gene encoding the n-terminal part of the neuropeptide, whereas in the other s. kowalevskii gene (skow1) the intron is located in a region encoding the c-terminal part of the neuropeptide. the presence of a conserved intron in the same frame in echinoderm prrp-like peptide genes, the two s. kowalevskii prrp-like peptide genes and chordate prrp-type genes supports our hypothesis that the echinoderm and hemichordate prrp-like peptides are orthologs of chordate prrp-type neuropeptides. by way of comparison, echinoderm prrp-like peptide genes have a different exon-intron structure to npy/npf genes. previous studies have reported that a conserved feature of npy/npf genes is an intron that interrupts the coding sequence for npy/npf-type peptides, with the intron located between the second and third nucleotide of the codon for the arginine residue of the c-terminal rf or ry dipeptide (mair et al., 2000) . here we show this conserved feature in npy/npf genes in source data 1. accession numbers of the precursor sequences used for the peptide alignments in figure 1 . species from several animal phyla, including a hemichordate (sister phylum to the echinoderms), chordates, molluscs, an annelid, a priapulid, an arthropod and a nematode (figure 2-figure supplement 1). in echinoderm prrp-like peptide genes, the exon encoding the neuropeptide is likewise interrupted by an intron but it is located in a different position to the intron that interrupts the coding sequence for npy/npf-type peptides. thus, it does not interrupt the codon for the arginine of the c-terminal rf or ry motif, but instead it is located between the first and second nucleotide of the codon for a residue located in the n-terminal or central regions of echinoderm prrp-like peptides ( figure 2-figure supplement 1) . another difference is that typically in npy/npf genes there is another intron that interrupts the coding sequence in the c-terminal region of the precursor protein, whereas in the echinoderm prrp-like peptide precursor genes the coding sequence for the c-terminal region of the precursor protein is not interrupted by an intron (figure 2-figure supplement 1) . collectively, these findings provide further evidence that echinoderm prrp-like peptides are not orthologs of npy/npf-type neuropeptides. . the protein-coding exons are colour-coded to show regions that encode the n-terminal signal peptide (blue), the neuropeptide (red), monobasic or dibasic cleavage sites (green) and other regions of the precursor protein (grey). note that a common characteristic is that an intron interrupts the coding sequence in the n-terminal or central region of the neuropeptide, with the intron consistently located between the first and second nucleotides (phase one intron represented by +1) of the codon for the amino acid shown after intron. taxa are highlighted in phylum-specific colours: dark blue (echinodermata), light blue (hemichordata), purple (chordata). the full names of the species and the accession numbers of the sequences are listed in figure 2 -source data 1. the online version of this article includes the following source data and figure supplement(s) for figure 2: source data 1. accession numbers of the sequences used for the gene structure analysis in figure 2 and discovery of orthologs of snpf/prrp-type receptors in a. rubens and other echinoderms having obtained evidence that echinoderm npy/prrp-like peptides are not orthologs of npy/npftype neuropeptides but are orthologs of prrp-type peptides, we then investigated the occurrence in a. rubens and other echinoderms of proteins related to gpcrs that mediate effects of npy/npftype peptides, prrp-type peptides and snpf-type peptides in other bilaterians. using receptor sequences of h. sapiens npy-type, d. melanogaster npf-type, h. sapiens prrp-type and d. melanogaster snpf-type receptors as queries for similarity-based analysis of a. rubens neural figure 3 . blosum62 cluster map of npy/npf/prpr/snpf-type receptors and closely related tachykinin-type receptors (tkr) and luqin/ryamide-type receptors (lq/ryar). nodes are labelled with phylum-specific colours, as shown in the key, and connections represent blast relationships with a p value > 1e-65. note that the echinoderm receptors (boxed) have more connections with prrp/snpf-type receptors than with npy/npf-type receptors. the sequences of the receptors included in this figure are listed in figure 3 -source data 1. the online version of this article includes the following source data and figure supplement(s) for figure 3: source data 1. accession numbers of the receptor sequences used for the clans analysis in figure 3 . transcriptome sequence data, a transcript (contig 1120879) encoding a 386-residue protein was identified as the best hit (figure 3-figure supplement 1). furthermore, homologs of the a. rubens protein encoded by contig 1120879 were also identified in other echinoderms for which genome sequences have been obtained, including the starfish a. planci, the sea urchin s. purpuratus and the sea cucumber a. japonicus, and importantly no other npy/npf/prrp/snpf-type receptors were identified in these species. to investigate relationships of the novel echinoderm receptors with other bilaterian neuropeptide receptors, we generated a sequence database including bilaterian npy/ npf/prrp/snpf-type receptors and other closely related receptors (tachykinin-type, luqin-type receptors) as outgroups. these receptor sequences were then analysed using two different methodologies. firstly, we performed a cluster-based analysis of the receptor sequences using clans ( figure 3 ). this analysis revealed three main clusters: 1. a cluster comprising the outgroup receptors (tachykinin/luqin), 2. a cluster comprising npy/npf-type receptors and 3. a cluster comprising snpf-type receptors and prrp-type receptors. interestingly, the echinoderm receptors showed stronger connections with the snpf/prrp receptor cluster ( figure 3 , black square) than with the npy/npf receptor cluster. these findings indicate that snpf-type receptors and prrp-type receptors are orthologous, as has been proposed previously based on cluster-based analysis of receptor sequences (jékely, 2013). furthermore, these findings indicate that npy/npf/prrp/snpf-type receptors in echinoderms are not orthologs of npy/npf-type receptors but are orthologs of snpf/prrp-type receptors. however, it is noteworthy that the lines linking the echinoderm receptors and nematode snpf-type receptors with other snpf/prrp-type receptors in clans are quite long (figure 3) , which is indicative of sequence divergence. secondly, we performed a phylogenetic analysis of the receptor sequences using the maximum likelihood method. for this analysis, in addition to bilaterian npy/npf-type receptors, deuterostome prrp-type receptors and protostome snpf-type receptors, we included tachykinintype, luqin-type and gpr83-type receptors as outgroups. this revealed that the echinoderm receptors are positioned within a branch of the phylogenetic tree that comprises npy/npf-type, prrp-type and snpf-type receptors, with the other receptor types included in the analysis occupying an outgroup position ( figure 4 ). more specifically, the echinoderm receptors are positioned in a clade comprising snpf-type receptors, with bootstrap support of >90%, indicating that the echinoderm receptors are orthologs of protostome snpf-type receptors. however, it is noteworthy that snpf-type receptors and prrp-type receptors do not form a monophyletic clade as would be expected for orthologous receptors. this may be a consequence of sequence divergence in the echinoderm and nematode snpf/prrp-type receptors that is reflected in the long branches leading to these receptors. because the phylogenetic analysis revealed that the echinoderm receptors are positioned in a clade comprising protostome snpf-type receptors (figure 4 ), we also compared the sequences of echinoderm prrp-type peptides and protostome snpf-type peptides (figure 4-figure supplement 1) and the structures of the genes encoding these neuropeptides (figure 4-figure supplement 2). this revealed that sequence identity is restricted to a few residues in the c-terminal regions of the peptides and, furthermore, the echinoderm prrp-type peptides are much longer than protostome snpf-type peptides (figure 4-figure supplement 1). this contrasts with the much higher levels of sequence similarity shared between echinoderm prrp-type neuropeptides and chordate prrp-type neuropeptides, as shown in figure 1a . another difference is that protostome snpf-type neuropeptide precursors typically give rise to multiple snpf-type peptides, whereas echinoderm prrp-type precursors are similar to chordate prrp-type precursors in containing a single prrp-type neuropeptide that is located adjacent to the signal peptide (figure 4-figure supplement 1). accordingly, comparison of the exon/intron structure of the genes encoding prrp-type precursors in echinoderms and snpf-type precursors in protostomes also revealed limited similarity (figure 4 -figure supplement 2). collectively, our analysis of sequence data indicates that npy/npf/prrp/snpf-type receptors in echinoderms are not orthologs of npy/npf-type receptors but are orthologs of snpf/prrp-type receptors. therefore, henceforth we refer to these echinoderm receptors as snpf/prrp-type receptors and specifically refer to the snpf/prrp-type receptor in the starfish a. rubens as ar-snpf/ prrpr. furthermore, having identified ar-snpf/prrpr we proceeded to investigate if arprrp acts as a ligand for this receptor. . phylogenetic tree showing that a candidate receptor for the a. rubens neuropeptide arprrp is an ortholog of protostome snpf-type receptors. the tree includes npy/npf-type receptors, chordate prrp-type receptors and protostome snpf-type receptors, with gpr83-type, luqin-type, and tachykinin-type receptors as outgroups to root the tree. interestingly, the candidate receptor for the a. rubens neuropeptide arprrp (red arrow) and orthologs from other echinoderms are positioned in a clade comprising protostome snpf-type receptors, whereas candidate receptors for prrptype peptides in the hemichordate s. kowalevskii are positioned in a clade containing chordate prrp-type receptors. note that npy/npf-type receptors form a distinct clade that includes an npy/npf-type receptor from the hemichordate s. kowalevskii, but no echinoderm receptors are present in this clade. the tree was generated in w-iq-tree 1.0 using the maximum likelihood method. the stars represent bootstrap support (1000 replicates, see legend) and the coloured backgrounds represent different taxonomic groups, as shown in the key. the names with text in blue represent the receptors for which ligands have been experimentally confirmed. the asterisks highlight receptors where the reported ligand is atypical when compared with ligands for receptors in the same clade. species names are as follows: aaeg (aedes aegypti), acal (aplysia californica), ajap (apostichopus japonicus), amis (alligator mississippiensis), apla (acanthaster planci), arub (asterias rubens), bbel (branchiostoma belcheri), bdor (bactrocera dorsalis), bflo a cdna encoding ar-snpf/prrpr was cloned and sequenced ( figure 3-figure supplement 1) and its sequence has been deposited in genbank under accession number mh807444.1. analysis of the sequence of ar-snpf/prrpr using protter revealed seven predicted transmembrane domains, as expected for a gpcr ( figure 5-figure supplement 1) . the cloned receptor was then co-expressed with ga16 in cho-k1 cells expressing apoaequorin to produce the cell system cho-ar-snpf/ prrpr. synthetic arprrp (pqdrskamqaertgqlrrlnprf-nh 2 ) was tested as a candidate ligand for ar-snpf/prrpr at concentrations ranging from 10 à14 m to 10 à5 m, comparing with cells incubated in assay media without the addition of the peptide. this revealed that arprrp at a concentration of 10 à5 m triggers luminescence responses (defined as 100%) in cho-ar-snpf/prrpr cells that were approximately five times the background luminescence detected with the assay media used to dissolve the peptide ( figure 5a) , demonstrating that arprrp acts as a ligand for the receptor. furthermore, arprrp induced dose-dependent luminescence in cho-ar-snpf/prrpr cells with a halfmaximal response concentration (ec 50 ) of 1.5 â 10 à10 m ( figure 5b ). importantly, no response to arprrp was observed in cho-k1 cells transfected with the vector alone, demonstrating that the signal observed in cho-ar-snpf/prrpr cells exposed to arprrp can be attributed to activation of the transfected receptor ( figure 5-figure supplement 2) . because arprrp contains a potential dibasic cleavage site (see underlined arginine residues in its sequence: pqdrskamqaertgqlrrlnprf-nh 2 ), we hypothesised that the c-terminal pentapeptide of arprrp (lnprfamide) may also be generated from arprrpp in vivo. therefore, we also tested synthetic lnprfamide as a candidate ligand for ar-snpf/prrpr. however, this peptide did not induce luminescence responses in cho-ar-snpf/ prrpr cells ( figure 5b) . therefore, we conclude that the 22-residue amidated peptide arprrp is the natural ligand for ar-snpf/prrpr in a. rubens. the a. rubens luqin-type neuropeptide arlq also did not induce luminescence responses in cho-ar-snpf/prrpr cells, demonstrating the selectivity of ar-snpf/prrpr for arprrp as a ligand ( figure 5b ). the discovery of an npy-like neuropeptide, named npf, in a platyhelminth provided the first definitive molecular evidence that npy-type neuropeptides originated in a common ancestor of the bilateria (maule et al., 1991) . subsequently, analysis of transcriptomic/genomic sequence data has enabled identification of npy/npf-type neuropeptides and their cognate receptors in a variety of invertebrate taxa, revealing a high level of conservation of this signalling system in bilaterian phyla (zatylny-gaudin and favrel, 2014; fadda et al., 2019) . here we report the first detailed analysis npy/npf-related signalling systems in echinoderms -invertebrate deuterostomes that have provided key insights into the evolution of other neuropeptide signalling systems (semmens et al., 2015; tian et al., 2016; elphick et al., 2018; yañez-guerra et al., 2018) . recently, we reported the discovery of echinoderm proteins comprising putative neuropeptides that share sequence similarity with npy/npf-type peptides (zandawala et al., 2017) . however, here our detailed analysis of the sequences of these peptides and the genes encoding them has revealed that they are not orthologs of the npy/npf-type neuropeptides. consistent with this finding, orthologs of npy/npf-type receptors were also not found in echinoderms. therefore, we conclude that npy/npf-type neuropeptide signalling has been lost in the phylum echinodermata ( figure 6 ). this is a noteworthy because, to the best of our knowledge, the only other taxon in which loss of npy/npf-type signalling has been reported are the urochordates, a sub-phylum of the phylum chordata (mirabeau and joly, 2013 ; figure 6 ). the evolutionary and functional significance of loss of npy/npf-type signalling in echinoderms and urochordates is rubens prrp/snpf-type receptor ar-snpf/prrpr, the promiscuous g-protein g a16 and the calcium-sensitive luminescent gfp-apoaequorin fusion protein g5a. for comparison, the background luminescence of cells that were not exposed to arprrp is shown (basal media; grey bar). mean values (± s.e.m) were determined from three independent experiments performed in triplicate (b). graph showing the selectivity of arprrp as a ligand for ar-snpf/prrpr. arprrp causes dose-dependent luminescence in cho-k1 cells expressing ar-snpf/prrpr, with an ec 50 of 0.15 nm. ar-snpf/prrpr is not activated by a c-terminal pentapeptide fragment of arprrp (lnprfamide) or by the a. rubens luqin-type peptide arlq. each point represents mean values (± s.e. figure 5 continued on next page unknown. however, insights into this issue may emerge from functional characterisation of npy/ npf-type signalling in other invertebrates. the nematode c. elegans is a powerful model system for functional characterisation of neuropeptide signalling systems (frooninckx et al., 2012) . however, npy/npf-type signalling has thus far only been partially characterised in this species. here, our phylogenetic analysis (figure 4) indicates that there are two c. elegans receptors that are orthologs of npy/npf-type receptors: npr-12, which is an orphan receptor, and npr-11, which has been shown to be activated by the peptide mdanafrmsfamide (chalasani et al., 2010) . however, this peptide shares little sequence similarity with npy/npf-type peptides from other bilaterians. furthermore, receptor assays only showed activation at peptide concentrations of 10 and 30 mm (chalasani et al., 2010) , which are high when compared to other npy/npf-type receptors that are typically activated by ligands in the nanomolar range (bard et al., 1995; lundell et al., 1997; garczynski et al., 2002; saberi et al., 2016) . recently, based on similarity-based sequence alignments, it has been suggested that the mature peptide derived from the c. elegans protein flp-27 may be an ortholog of npy/npf-type peptides (fadda et al., 2019) . here, our analysis of the structure of the gene encoding the flp-27 precursor has revealed that it has the characteristic structure of npy/npf-type genes, with an intron interrupting the codon for the c-terminal arginine of the npf-type peptide sequence (figure 2 -figure supplement 1). thus, based on our analysis of c. elegans sequence data, we conclude that the npy/ npf-type peptide derived from the flp-27 precursor protein is likely to act as a ligand for the npr-11 and/or npr-12 receptors. this finding provides a basis for functional characterisation of npy/ npf-type signalling in c. elegans. if the echinoderm npy-like peptides are not orthologs of npy/npf-type neuropeptides, then what are they? here we show that these peptides share sequence similarity with vertebrate prrp-type neuropeptides ( figure 1a) . furthermore, analysis of the structure of the genes encoding the echinoderm neuropeptides revealed that the coding sequence for the neuropeptides is interrupted by an intron in the phase one frame, a feature that is also a characteristic of genes encoding vertebrate prrp-type neuropeptides (figure 2) . these findings indicate that the echinoderm neuropeptides are orthologs of vertebrate prrp-type neuropeptides. to further address this issue we analysed echinoderm genome/transcriptome sequence data to identify candidate cognate receptors for the echinoderm prrp-like peptides. a cluster-based analysis of receptor sequence data using clans revealed the presence in echinoderms of receptor proteins that show strong connections with a receptor cluster comprising vertebrate prrp-type receptors and protostome snpf-type receptors (figure 3) . accordingly, a previous cluster-based analysis of receptor sequence data has reported that vertebrate prrp-type receptors cluster with protostome snpf-type receptors, indicating that these receptors may be orthologous (jékely, 2013). a novelty of our analysis is the inclusion of several echinoderm receptor sequences. it is noteworthy, however, that whilst strong connections between the echinoderm receptors and prrp/snpf-type receptors in other taxa can be seen using clans, the lines linking to the echinoderm receptors are quite long (figure 3 ). this suggests that the echinoderm receptors are orthologs of prrp/snpf-type receptors but have undergone sequence divergence. interestingly, a group of snpf-type receptors in the nematode c. elegans appears to be similarly divergent with respect to other snpf/prrp-type receptors (figure 3) . . phylogenetic diagram showing the occurrence of npy/npf-type, snpf-type and prrp-type neuropeptide signalling in the bilateria. the tree shows the phylogenetic relationships of selected bilaterian phyla. a gene duplication event giving rise to the paralogous npy/npf-type (green) and prrp/snpf (purple) signalling systems is shown at a position in the tree corresponding to the common ancestor of the bilateria. phyla in which npy/ npf-type peptides/precursors and npy/npf-type receptors have been identified are labelled with green-filled squares. phyla in which prrp-type peptides/precursors and prrp-type receptors have been identified are labelled with blue-filled squares. phyla in which snpf-type peptides/precursors and snpf-type receptors have been identified are labelled with red-filled squares. the inclusion of an asterisk in filled squares indicates that activation of a receptor by a peptide ligand has been demonstrated experimentally. note that in the starfish asterias rubens (this study) a prrp-type peptide (blue triangle) is the ligand for receptor that has been found to be an ortholog snpf/prrp-type receptors (figure 3) or an ortholog of snpf-type receptors ( figure 4) ; hence this receptor is represented here as a red triangle. note also the mutually exclusive patterns in the phylogenetic distribution of snpftype signalling and prrp-type signalling, with the former found in protostomes and the latter found in vertebrates, cephalochordates and hemichordates, which is supportive of the hypothesis that these signalling systems are orthologous. our discovery of a prrp/snpf-type signalling system in echinoderms provides a missing link in the evolution of this neuropeptide signalling system. npy/npf-type signalling occurs in most phyla, but it has been lost in echinoderms and urochordates. the inclusion of a question mark for the putative npy/npf-type peptide identified in the cephalochordate b. floridae (mirabeau and joly, 2013; elphick and mirabeau, 2014) signifies that it is atypical of npy/npf-type peptides, which may explain why npy/npf-type receptors have yet to be identified in cephalochordates. the inclusion of a question mark in the c. elegans green square figure 6 continued on next page to further investigate the relationship of the echinoderm receptors with snpf/prrp-type receptors, we performed a phylogenetic analysis of sequence data using the maximum likelihood method (figure 4) . in this analysis, the echinoderm receptors are positioned in a clade comprising protostome snpf-type receptors. however, snpf-type receptors and prrp-type receptors do not form a monophyletic clade in the tree. interestingly, this finding has been reported previously as part of a wider analysis of neuropeptide receptor relationships in the bilateria (mirabeau and joly, 2013) . thus, there is inconsistency in the findings from cluster-based analysis (clans) (jékely, 2013; figure 3) and phylogenetic tree-based analysis (mirabeau and joly, 2013; figure 4 ) of receptor relationships. one possible explanation for this inconsistency would be that gene duplication in a common ancestor of the bilateria gave rise to two snpf/prrp-type signalling systems, which were then differentially lost/retained in bilaterian lineages, but in such a scenario gene loss in several lineages would have to be invoked. alternatively, the inconsistency may, at least in part, be a consequence of sequence divergence in echinoderm and nematode snpf/prrp-type receptors with respect snpf/prrp-type receptors in other taxa, which is reflected in their position peripheral to the main cluster of snpf/prrp-type receptors in the clans. accordingly, it is noteworthy that in the phylogenetic tree (figure 4) there is a long branch leading to the echinoderm receptor clade and likewise nematode snpf-type receptors also have long branches (figure 4) . nevertheless, collectively our sequence analysis indicates that the echinoderm receptors are orthologs of snpf/prrptype receptors. therefore, it was of interest to determine if echinoderm prrp-type neuropeptides act as ligands for snpf/prrp-type receptors in this phylum. here we show that the a. rubens prrp-type neuropeptide arprrp (pqdrskamqaertg qlrrlnprf-nh 2 ) is a potent ligand for the a. rubens snpf/prrp-type receptor ar-snpf/prrpr ( figure 5 ). these findings demonstrate for the first time the existence and molecular identity of a prrp-type signalling system in an echinoderm. furthermore, our identification of orthologs of arprrp and ar-snpf/prrpr in other echinoderms, including for example the sea urchin s. purpuratus, demonstrates the conservation of this signalling system in this phylum. in addition, our comparative analysis of sequence data has also enabled identification of genes/transcripts encoding prrp-type neuropeptides in the hemichordate s. kowalevskii and the cephalochordate b. floridae (figure 1 ). previous studies have concluded that snpf-type signalling is paralogous to npy/npf-type signalling in protostomes (nässel and wegener, 2011) and that prrp-type signalling is paralogous to npy/ npf-type signalling in vertebrates (lagerströ m et al., 2005) . evidence that the prrp-type and snpf-type signalling systems may be orthologous has also been reported previously (jékely, 2013), but this hypothesis has not been tested experimentally. our discovery of a starfish prrp-type neuropeptide that acts as a ligand for a starfish ortholog of snpf-type receptors is important because it provides a missing link for reconstruction of the evolutionary history of prrp/snpf-type neuropeptide signalling (figure 6) . comparison of the sequences of vertebrate prrp-type neuropeptides and protostome snpf-type neuropeptides reveals low levels of sequence similarity, which no doubt in part explains why prrptype and snpf-type neuropeptides have not been recognised as orthologs. in figure 4 -figure indicates that the peptide identified as a ligand for the c. elegans npy/npf-type receptor (chalasani et al., 2010) does not have the typical features of an npy/npf-type peptide. the grey square for snpf in m. expansa, for which only transcriptome sequence data are available, indicates that snpftype peptides and snpf-type receptor(s) are likely to be present in this species because snpf-type peptides and snpf-type receptors have been identified in another platyhelminth species, s. mediterranea, for which a genome sequence is available. species names are as follows: h. sapiens (homo sapiens), c. intestinalis (ciona intestinalis), b. floridae (branchiostoma floridae), s. kowalevskii (saccoglossus kowalevskii), a. rubens (asterias rubens), p. dumerilii (platynereis dumerilii), l. stagnalis (lymnaea stagnalis), m. expansa (moniezia expansa), s. mediterranea (schmidtea mediterranea), c. gigas (crassostrea gigas), d. melanogaster (drosophila melanogaster), c. elegans (caenorhabditis elegans). silhouettes of representative animals from each phylum are from www.openclipart.com and they are free from copyright. supplement 1 we illustrate this in an alignment of the echinoderm prrp-type neuropeptides and protostome snpf-type neuropeptides, with sequence identity restricted to a few residues in the c-terminal regions of these peptides. this contrasts with the higher levels of sequence similarity shared between echinoderm prrp-type neuropeptides and vertebrate prrp-type neuropeptides, as shown in figure 1a . furthermore, echinoderm prrp-type precursors are similar to chordate prrptype precursors in containing a single long neuropeptide, whereas protostome snpf-type precursors typically contain multiple smaller neuropeptides. thus, there is little evidence of orthology from comparison of echinoderm prrp-type and protostome snpf-type neuropeptide, precursor and gene sequences. consequently, our conclusion that the echinoderm prrp-type peptides are orthologs of protostome snpf-type peptides is principally based on the orthology of their receptors (figure 3 ) and our experimental demonstration that a prrp-like peptide (arprrp) acts as a ligand for a snpf/ prrp-type receptor (ar-snpf/prrpr) in the starfish a. rubens ( figure 5) . it is important to note, however, that this is not unprecedented in investigations of the evolution of neuropeptide signalling. thus, whilst the sequences of some neuropeptides and neuropeptide precursors are highly conserved throughout the bilateria, others are so divergent that they can be unrecognisable as orthologs. an example of the former are vasopressin/oxytocin (vp/ot)-type neuropeptides and precursors. an example of the latter are neuropeptide-s (nps)/crustacean cardioactive peptide (ccap)-type neuropeptides and precursors, which are paralogs of vp/ot-type neuropeptides and precursors (semmens et al., 2015) . thus, by way of comparison, npy/npf-type neuropeptides are similar to vp/ot-type neuropeptides in exhibiting a high level of sequence conservation throughout the bilateria. conversely, prrp/snpf-type neuropeptides are similar to nps/ccap-type neuropeptides in being highly divergent, with neuropeptides in protostomes and deuterostomes exhibiting modest sequence similarity. the discovery of prrp/snpf-type signalling in echinoderms has provided a unique opportunity to speculate on the ancestral characteristics of this signalling system in urbilateria. it is noteworthy that, by comparison with the protostome snpf-type peptides, the echinoderm prrp-type peptides have more features in common with the paralogous npy/npf-type peptides. prrp-type peptides are not as long as npy/npf-type peptides but they are nevertheless much longer than protostome snpf-type peptides. furthermore, it was the sequence similarity that echinoderm prrp-type peptides share with npy/npf-type peptides that originally facilitated their discovery (zandawala et al., 2017) . additionally, the structure of the prrp-type precursors is similar to npy/npf-type precursors because the neuropeptide is located immediately after the signal peptide, whereas this is not a feature of protostome snpf-type precursors. based on these observations, we propose that prrp-type peptides and precursors may more closely resemble the ancestral characteristics of the prrp/snpf type signalling system in urbilateria. furthermore, we speculate that the common ancestor of the paralogous npy/npf-type and prrp/snpf-type neuropeptide precursors may have been similar to npy/npf-type precursors with respect peptide, precursor and gene structure. then, following gene duplication, these ancestral characteristics were retained in the paralog that gave rise to the bilaterian npy/npf-type peptides/precursors. in contrast, the paralog that gave rise to prrp/snpf-type signalling diverged from the ancestral condition. however, the extent of divergence varies in the deuterostome and protostome lineages. in deuterostomes, the prrp-type peptides/precursors have many npy/npf-type characteristics and we conclude that this reflects less divergence from the proposed ancestral condition. conversely, in the protostomes, the snpf-type peptides/precursors exhibit little similarity with npy/npf-type peptides/precursors and we conclude that this reflects more divergence from the proposed ancestral condition. in conclusion, our discovery of a prrp/snpf-type signalling system in echinoderms has provided a missing link that unites prrp-type peptides in vertebrates and snpf-type peptides in protostomes as members of a bilaterian family of neuropeptides, as illustrated in figure 6 . this represents an important advance in our knowledge of neuropeptide signalling systems in the bilateria and illustrates the value of insights from echinoderms in enabling reconstruction of the evolutionary history of neuropeptides. animals starfish (asterias rubens) were obtained from a fisherman based at whitstable (kent, uk). they were then maintained in a circulating seawater aquarium at~11˚c in the school of biological and chemical sciences at queen mary university of london and were fed on mussels (mytilus edulis) collected near margate (kent, uk). cloning and sequencing of a cdna encoding the precursor of an a. rubens npy/npf/prrp-like peptide a transcript encoding the a. rubens precursor of an npy/npf-like peptide was reported previously (genbank: mk033631) (zandawala et al., 2017) . however, in this paper we show that the npy/npflike peptide derived from this precursor shares more sequence similarity with prrp-type peptides. a cdna containing the complete open reading frame of the precursor was amplified by pcr using a. rubens radial nerve cord cdna, the forward primer aagtcaaaaggcgagcaaga, the reverse primer aaagggatgtggtgttggtg and q5 polymerase (neb; cat. no. m0491s). the pcr products were ligated into the pbluescript ii ks (+) vector (invitrogen; cat. no. k280002) that had been cut previously with the restriction enzyme ecorv by performing blunt-end ligation with t4 dna ligase (neb; cat. no. m0202s). the cloning was confirmed by restriction enzyme digestion and sequencing (tubeseq service; eurofins genomics). structural characterisation of the a. rubens npy/npf/prrp-like peptide using mass spectrometry after confirming the nucleotide sequence of the a. rubens precursor of a npy/npf/prrp-like peptide by cloning and sequencing, mass spectrometry was used to determine the mature structure of the peptide. the methods employed, including extraction of peptides from a. rubens radial nerve cords, treatment of samples, equilibration of columns, reverse phase chromatography for the initial separation and injection into a orbitrap-fusion (thermoscientific) for tandem mass spectrometry (ms/ms), were performed using a previously reported protocol for the identification of the starfish neuropeptides (lin et al., 2017) . the methods employed for data analysis are described below. mass spectra were searched using sequest proteome discoverer (thermo fisher scientific, v. 2.2) against a database comprising forty-three different precursor proteins identified by analysis of a. rubens neural transcriptome data, including the a. rubens arprrp precursor and all proteins in gen-bank from species belonging to the asteriidae family and the common repository of adventitious proteins database (http://www.thegpm.org/crap/index.html). theoretical peptides were generated allowing up to two missed cleavages and variable modifications, including amidation (à0.98402) of c-terminal glycines and pyroglutamate (à17.02655) of n-terminal glutamines, and oxidation of methionine (+15.99). precursor mass tolerance was 10 ppm and fragment ions were searched at 0.8 da tolerances. results from discoverer were collated and annotated in scaffold version 4.8.4 (proteome software). sequence alignment of echinoderm npy/npf/prrp-like peptides with npy/npf-type peptides, prrp-type peptides, and snpf-type peptides from other taxa the amino acid sequences of echinoderm npy/npf/prrp-like peptides were aligned with the sequences of npy/npf-type peptides, prrp-type peptides and snpf-type peptides from a variety of bilaterian species (see figure 1 -source data 1 and figure 4 -figure supplement 1-source data 1 for lists of the sequences). to identify candidate ligands for prrp-type receptors in the cephalochordate b. floridae and the hemichordate s. kowalevskii, we analysed transcriptomic and genomic sequence data for these species (putnam et al., 2008; simakov et al., 2015) . the data analysed also included a list of predicted s. kowalevskii proteins kindly provided to o. mirabeau by dr. r.m. freeman (harvard medical school, usa). the methods employed to identify candidate neuropeptide precursors have been reported previously (mirabeau and joly, 2013) but here we had the more specific objective of identifying proteins with an n-terminal signal peptide followed by a neuropeptide with a predicted c-terminal rfamide or ryamide motif. this resulted in discovery of one candidate prrp-type precursor in the cephalochordate b. floridae and two candidate prrp-type precursors in the hemichordate s. kowalevskii. alignments were performed using mafft version 7 (5 iterations, substitution matrix; blosum62) and then manually curated. highlighting of the conserved residues was done using boxshade (www.ch.embnet.org/software/box_form.html) with 50% conservation as the minimum for highlighting. finally, the sequences were highlighted in phylum-specific or superphylum-specific colours: dark blue (echinodermata), light blue (hemichordata), purple (chordata), orange (platyhelminthes), red (lophotrochozoa), yellow (priapulida), green (arthropoda), grey (nematoda). comparison of the exon/intron structure of genes encoding npy/npf/ prrp-like peptides in echinoderms and genes encoding npy/npf-type peptides, prrp-type peptides and snpf-type peptides in other taxa the sequences of transcripts and genes encoding precursors of echinoderm precursors of npy/npf/ prrp-like peptides and precursors of npy/npf-type, prrp-type and snpf-type peptides from other taxa were obtained from genbank. the sequence of a predicted transcript encoding a second s. kowalevskii precursor (skow2) of a prrp-like peptide was determined based on a genscan prediction (burge and karlin, 1997; burge and karlin, 1998) from scaffold 51909 (genbank accession number nw_003156735.1). see figure 2 -source data 1 and figure 4 -figure supplement 2source data 1 for a list of the transcript and gene sequences analysed. the online tool splign (kapustin et al., 2008) (https://www.ncbi.nlm.nih.gov/sutils/splign/splign.cgi) was employed to determine the exon/intron structure of genes and schematic figures showing gene structure were generated using ibs 1.0 (liu et al., 2015) . identification of a candidate receptor for the npy/npf/prrp-like peptide in a. rubens and analysis of its relationship with npy/npf/ prrp/snpf-type receptors in other taxa to identify a candidate receptor for the a. rubens npy/npf/prrp-like peptide, a. rubens neural transcriptome sequence data were analysed using the blast server sequenceserver (priyam et al., 2015) , submitting npy-type receptors from h. sapiens (genbank np_000900.1, np_000901.1, np_001265724.1), an npf-type receptor from d. melanogaster (genbank aaf51909.3), a prrp-type receptor from h. sapiens (np_004239.1) and snpf-type receptors from d. melanogaster (genbank; np_524176.1) and c.gigas (genbank xp_011451552.1) as query sequences. a transcript (contig 1120879) encoding a 386-residue protein (http://web.expasy.org/translate/) was identified as the top hit in all blast searches and this has been deposited in genbank under the accession number mh807444. the protein sequence was also analysed using protter v1.0 (omasits et al., 2014) . using blast, homologs of the a. rubens protein were identified in other echinoderms for which genome sequences are available, including the starfish acanthaster planci (xp_022101544.1), the sea urchin strongylocentrotus purpuratus (xp_003725178.1) and the sea cucumber apostichopus japonicus (pik36230.1). furthermore, no other npy/npf/prrp/snpf-type receptors were identified in these species. to investigate the relationship of the echinoderm receptors with neuropeptide receptors from other bilaterians, a database of receptor sequences was generated that included npy/npf-type, prrp-type, snpf-type, tachykinin-type, luqin-type and gpcr83-type receptors (the latter three receptor types being included as outgroups), including representative species from the phyla chordata, hemichordata, echinodermata, mollusca, annelida, platyhelminthes, nematoda, priapulida, and arthropoda (see figure 3 -source data for a list of the sequences used). a cluster-based analysis of the receptor sequences was performed using clans (frickey and lupas, 2004 ). an allagainst-all blast was performed using the scoring matrix blosum62 and linkage clustering was performed with an e-value of 1e-68 to identify coherent clusters. the clustering was first performed in 3d and then the map was collapsed to 2d to enable generation of the diagram shown in figure 3 (see figure 3 -source data for a list of sequences used). using the same receptor sequences, a phylogenetic tree was generated using the maximum-likelihood method. receptor sequences were aligned using muscle in the online tool ngphylogeny (iterative, 16 iterations, upgmb as clustering method) (edgar, 2004; lemoine et al., 2019) and the alignment was automatically trimmed using trimal with automatic selection of trimming method using the online tool ngphylogeny (capella-gutierrez et al., 2009) . the trimming contained a total of 239 residues that were used to generate the maximum-likelihood tree using w-iq-tree online version 1.0 (the model was automatically selected, being lg+g+i+f the chosen substitution model, branch tests used were ultrafastbootstrap 1000 replicates and sh-alrt 1000 replicates) (trifinopoulos et al., 2016) . the sequence database used for this tree, together with the trimmed alignment, and the raw tree are available at zenodo (https://zenodo.org/record/3837351). to enable the pharmacological characterisation of a candidate receptor for the a. rubens npy/npf/ prrp-like peptide, a cdna encoding this receptor was cloned into the eukaryotic expression vector pcdna 3.1(+) (invitrogen; . to facilitate expression of the cloned receptor, the forward primer included a partial kozak consensus sequence (acc) and a sequence corresponding to the first 15 bases of the open reading frame of contig 1120879 (accatgcagatgacaacc) and the reverse primer consisted of a stop codon and a sequence reverse complementary to the 3' region of the open reading frame of contig 1120879 (gcgtcacatagtggtatcatg). pcr was performed using the forward primer and reverse primers, a. rubens radial nerve cord cdna and q5 polymerase (neb; cat. no. m0491s). pcr products were ligated into the pcdna 3.1(+) vector that had been cut previously with the restriction enzyme ecorv by performing blunt-end ligation with t4 dna ligase (neb; cat. no. m0202s). successful ligation and the direction of the insert was determined by restriction enzyme digestion and sequencing (tubeseq service; eurofins genomics). cell lines and pharmacological characterisation of a candidate receptor for the npy/npf/prrp-like peptide in a. rubens chinese hamster ovary (cho)-k1 cells stably expressing the calcium sensitive apoaequorin-gfp fusion protein (g5a) (baubet et al., 2000) were used here for receptor assays. these cells have been used previously for neuropeptide receptor deorphanisation (bauknecht and jékely, 2015) and were generously supplied to us by dr gá spá r jé kely (university of exeter). the cell line was generated using the cho-k1 cell line from sigma-aldrich (85051005), which is certified by the european collection of authenticated cell cultures (ecacc). following transfection with a plasmid encoding g5a, cells were selected for stable transfection using geneticin g418 sulfate (thermo fisher scientific, cat. no. 10131035) . the methods we used for cell culture and receptor assays have been described previously (yañez-guerra et al., 2018) . upon reaching a confluency of approximately 80%, cells were transfected with a plasmid containing the ar-snpf/prrp receptor cdna and a plasmid containing the promiscuous gaà16 protein that can couple a wide range of gpcrs to the phospholipase c signalling pathway. the transfection was achieved using 5 mg of each plasmid and 10 ml of the transfection reagents p3000 and lipofectamine 3000 (thermo fisher scientific; cat. no. l3000008), as recommended by the manufacturer. it was not possible to authenticate the cho-k1 (g5a) cells or test the cells for mycoplasma contamination at the time of manuscript submission due to laboratory closure during the covid-19 pandemic. after transfection with the a. rubens receptor, cells were exposed to the a. rubens npy/npf/ prrp-like peptide pqdrskamqaertgqlrrlnprf-nh 2 (custom synthesised by peptide protein research ltd., fareham, uk), which was diluted in dmem/f12 nutrient mixture medium at concentrations ranging from 10 à14 m to 10 à5 m in clear bottom 96-well plates (sigma-aldrich; cat. no. cls3603-48ea). luminescence was measured over a 30 s period using a fluostar omega plate reader (bmg labtech; fluostar omega series multi-mode microplate reader) and data were integrated over the 30 s measurement period. for each concentration, measurements were performed in triplicate, and the average of each was used to normalise the responses. the responses were normalised to the maximum luminescence measured in each experiment (100% activation) and to the background luminescence with the vehicle media (0% activation). dose-response curves were fitted with a four-parameter curve and ec 50 values were calculated from dose-response curves based on at least three independent transfections using prism 6 (graphpad, la jolla, usa). editing; ismail moghul, software, formal analysis, writing -review and editing; thomas butts, supervision, writing -review and editing; cleidiane g zampronio, formal analysis, investigation, visualization, methodology, writing -review and editing; alexandra m jones, formal analysis, supervision, funding acquisition, investigation, visualization, writing -review and editing; olivier mirabeau, software, formal analysis, investigation, methodology, writing -review and editing; maurice r elphick, conceptualization, resources, formal analysis, supervision, funding acquisition, writing -original draft, project administration, writing -review and editing all data generated or analysed during this study are included in the manuscript and supporting files. neuropeptide y distribution in human brain molecular structure of mammalian neuropeptide y: analysis by molecular cloning and computer-aided comparison with crystal structure of avian homologue cloning and functional expression of a human y4 subtype receptor for pancreatic polypeptide, neuropeptide y, and peptide yy chimeric green fluorescent protein-aequorin as bioluminescent ca2+ 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by the mexican council of science and technology (conacyt studentship no. 418612) and queen mary university of london and by a leverhulme trust grant (rpg-2016-353) awarded to mre. xz was supported by a phd studentship awarded by the china scholarship council and queen mary university of london. we are grateful to gá spá r jé kely (university of exeter) for providing the cho-k1 (g5a) cell line used here for receptor deorphanisation assays. the funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. luis alfonso yañ ez-guerra, xingxing zhong, conceptualization, data curation, formal analysis, validation, investigation, visualization, methodology, writing -original draft, writing -review and key: cord-025995-nxeg03xj authors: gerba, charles p.; goyal, sagar m. title: pathogen removal from wastewater during groundwater recharge date: 2013-11-17 journal: artificial recharge of groundwater doi: 10.1016/b978-0-250-40549-7.50015-1 sha: doc_id: 25995 cord_uid: nxeg03xj nan solid wastes, and sewage oxidation ponds. additional sources of pathogens in groundwater may involve artificial recharge of groundwater aquifers with renovated wastewater including deep well injection, spray irrigation of crops and landscape, basin recharge, and land application of sewage effluent and sludges. leakage of sewage into the groundwater from septic tanks, treat ment lagoons, and leaky sewers is estimated to be over a trillion gallons a year in the united states [6] . it should be realized that, as opposed to surface water pollution, con tamination of groundwater is much more persistent and is difficult to erad icate. because restoration of groundwater quality is difficult, time-consuming, and expensive, efforts should be made for the protection of groundwater quality rather than only for its restoration after degradation. secondary sewage treatment including disinfection by chlorination may not be able to remove all of the pathogens present in sewage. thus, intentional or unintentional recharge of groundwater with treated sewage effluent may be potentially hazardous to human and animal life. soil is considered a living filter, capable of removing pathogenic mi croorganisms from applied wastewater. the extent to which soil can remove these microorganisms depends on several factors such as the nature of the soil, the nature of the pathogen concerned, temperature, and antagonism from native microflora. because of their large size, parasitic protozoa and helminths may be efficiently removed by filtration through soil and may not be able to gain entrance into the groundwater. bacterial removal by soils also occurs largely by filtration, although adsorption is also involved. viruses, on the other hand, are thought to be removed by the process of adsorption only [7] . unfortunately, however, viruses cannot be considered as permanently immobilized because they have been shown to elute and migrate further in soil following rainfall events [8] [9] [10] . several investigators have reported on the isolation of viruses from groundwater [11] and several outbreaks of viral hepatitis, yersiniosis, ty phoid, and shigellosis have also been attributed to contaminated groundwater [1] . documented evidence of health problems associated with groundwater recharge is, however, lacking. the paucity of information on health problems associated with groundwater recharge programs may reflect either the absence of a problem, lack of intensive surveillance, or the insensitivity of present epidemiologic tools to detect recurrent small-scale incidents of disease. often the low fecal car riage rates of agents of infectious disease and the low background of enteric disease in the united states has been cited as further evidence that the potential of public health hazard as a result of direct or indirect reuse of wastewater is minimal. it should be realized, however, that levels of enteric disease in the united states are low primarily because of good sanitation, personal hygiene, and a network of sanitary engineering works. as a result of this low exposure to pathogens, the population at large may have become highly susceptible to even small numbers of pathogens. waterborne outbreaks of disease are no longer on the decline in this country (figure 9 .1). a total of 50 waterborne outbreaks occurred during 1980, increasing the annual average of outbreaks to 39 for the 5-year period from 1976-1980. this number represents more than a 50 percent increase over the 1971-1975 average of 24. the 5-year averages have steadily in creased from an annual average of ten during [1951] [1952] [1953] [1954] [1955] . before that pe riod, the trend was declining [12] . it should be emphasized that reporting of waterborne disease out breaks, particularly in individual systems, is notoriously poor. according to craun [1] outbreaks in municipal water systems, which number 40,000 and serve about 177 million people, are probably the most likely to be reported. outbreaks in semipublic systems, which number about 200,000 and serve numerous transients, are the next most likely to be reported. the least likely to be reported are the outbreaks in individual water systems, which number about 10,000,000. in fact, one third of the individual groundwater supplies in a rural neighborhood of oregon were found to be fecally contaminated in a recent survey [13] . waterborne hypothesis cannot be proved in all instances because epidemiologic investigations are sometimes incomplete or conducted long after the outbreak has subsided. also, the surveillance of waterborne diseases by the centers for disease control (cdc) is largely passive and clearly rep resents a fraction of the total number that occur. according to cdc, "the likelihood of an outbreak coming to the attention of health authorities varies considerably from one locale to another depending largely upon consumer awareness, physician interest, and disease surveillance activities of state and local health and environmental agencies. large interstate-outbreaks and outbreaks of serious illness are more likely to come to the attention of health authorities." of 673 documented outbreaks of waterborne disease from 1946 to 1978, 425 (63%) were attributed to illness of probable viral etiology (e.g., hepatitis a, poliomyelitis, gastroenteritis). this number probably represents only a fraction of the actual number of virus-caused outbreaks, because of the difficulties involved in proving a viral etiology of a waterborne outbreak. in fact, direct evidence of virus involvement in waterborne outbreaks is limited to hepatitis a, adenovirus, and recently to norwalk agent and rotavirus [3] . the lack of documentation of waterborne viral disease outbreaks may be ascribed to limitations in methodology for the detection of viruses in water and relative insensitivity of epidemiologic techniques to detect lowlevel transmission of viral diseases through water. it is easy to recognize the outbreaks of infectious hepatitis by the water route because of their explo sive nature and characteristic symptomatology. most enteric viruses, how ever, cause a wide variety of symptoms so that scattered cases of acute illness would probably have too varied symptoms to be attributed to a single etiologic agent. also, the presence of small numbers of viruses in water may result only in an inapparent infection in a person coming in contact with contaminated water. the virus may then multiply in the respiratory and gastrointestinal tract of that person who may, in turn, act as an effective carrier and transmit the virus to others. the development of acute disease in these contact persons will be epidemiologically classified as "transmitted by direct contact" rather than being waterborne. intensive surveillance is, therefore, necessary to determine the "real" cause of an outbreak. a discussion on epidemiology is incomplete without consideration of minimum infective dosage of various microorganisms. infective doses of most bacterial pathogens are relatively high. for instance, approximately 10 8 enteropathogenic escherichia coli or vibrio cholerae cells must be con-sumed by healthy male volunteers to produce disease in a significant pro portion of subjects. in case of shigella, however, 10-100 cells are enough to cause dysentery. similarly, the infectious dose of protozoan cysts and helminth ova is very low, perhaps 10. the symptoms of helminth infections are dose-related, however. currently available information suggests that even a single virus particle may produce infection under favorable condi tions. after reviewing infective dose data for various microorganisms in human subjects, akin [14] reached the conclusion that infective dose for some members of bacterial, viral, and parasitic groups may be as low as =^10 detectable units. pathogenic microorganisms such as bacteria, viruses, protozoa, and parasitic worms are almost always present in domestic sewage. the number and types of organisms present in sewage, however, vary from community to com munity depending on urbanization, population density, sanitary habits, sea son of the year, and rates of disease in the contributing community [15] . the most common bacterial pathogens associated with sewage are salmonella, shigella, vibrio, and campylobacter (table 9 .1). salmonella occurs [17] . since 1973, however, 31 cases of cholera have been documented along the gulf coast. the strains from all these cases appear essentially identical, suggesting that the toxigenic v. cholerae 01 has persisted in that region for at least 8 years. extra efforts should, therefore, be made to keep track of this potential problem. more than 110 different virus types may be present in raw sewage (table 9 .2). they range in size from about 27 nm for polio virus to 70 nm for rotavirus and up to 100 nm for enteric coronavirus. all virus groups found in sewage contain single-or double-stranded rna except adenoviruses, which consist of double-stranded dna. these viruses are capable of causing a variety of illnesses at very low dosage levels [14] . the amount of virus present in raw sewage is highly variable but as high as 500,000 infec tious virus particles per liter have been detected [18] . studies indicate that bacteria and viruses are not removed effectively from wastewaters during primary treatment [19] ; removal of viruses during secondary treatment (active sludge) is dependent largely on virus adsorption to solids. since rotavirus adsorbs poorly to activated sludge floes, it can be speculated that wastewater treatment processes that are highly effective in the removal of enteroviruses may not be as effective in removing rota and reoviruses. even within the enterovirus group, virus adsorption to activated sludge was found to be both type-and strain-dependent [56] . it stands to reason, therefore, that different viruses will have different removal char acteristics during activated sludge treatment. an average of 90 to 95 percent of the enteric bacteria in sewage are reported to be removed by activated sludge process (table 9 .3). coagulation with alum or lime is considered to be generally efficient for virus removal. in laboratory studies, 3-4 log reduction of viruses is common following lime treatment at ph 11. in field studies, however, viruses were isolated from lime sludge and lime-treated effluent [20] . other tertiary treatments such as ferric chloride-polyelectrolyte flocculation, sand or granular filtration, re verse osmosis, and carbon adsorption have been found to significantly re duce the level of pathogens. feachem et al. [21] reviewed the literature on pathogen removal by various sewage treatment processes. removal, but to look at orders of magnitude." they further stated that to talk of percent removal is misleading because a 99 percent removal of path ogens from raw sewage containing 10 5 pathogens per liter will produce an effluent that still contains 10 3 pathogens per liter. this level may still be of great public health concern, depending on how the effluent is going to be used. as efficient as it may be, sewage treatment processes cannot be ex pected to remove/inactivate all of the pathogens present. disinfection of treated wastewater is, therefore, practiced to ensure further inactivation of microorganisms. in the united states, chlorination is practically the only process used for disinfection of wastewater. unfortunately, however, there is a great variability in resistance to chlorine among different microorga nisms. it is generally agreed that bacteria are much more susceptible to chlorine than are viruses and protozoan cysts. also, chlorine may be very [21] . effective against mircoorganisms cultivated in the laboratory under artificial conditions, but it may not be as effective on naturally occurring strains of bacteria and viruses. the fate of pathogenic bacteria and viruses in the subsurface will be deter mined by their survival and their retention by soil particles. both survival and retention are largely determined by the three factors shown in figure 9 .2. climate will control two important factors in determining viral and bacterial survival: temperature and rainfall. the survival of microorganisms is greatly prolonged at low temperature; below 4° c they can survive for months or even years [18] . at higher temperatures, inactivation or dieoff is fairly rapid. in the case of bacteria, and probably viruses, the dieoff rate is approximately doubled with each 10° c rise in temperature between 5° c and 30° c [22] . above 30° c temperature is probably the dominant factor determining virus survival time. rainfall mobilizes previously retained bac teria and viruses and greatly promotes their transport in groundwater. sev eral studies have shown that the greatest degree of drinking water well contamination occurs after periods of heavy rainfall [23] [24] [25] . the nature of the soil will also play a major role in determining survival and retention. soil properties influence moisture-holding capacity, ph and organic matter-all of which will control the survival of bacteria and virus in the soil. other soil properties such as particle size, cation exchange ca pacity, and clay content will influence retention. resistance of microorga nisms to environmental factors will vary among different species as well as strains. bacteria are believed to be removed largely by filtration processes while adsorption is the major factor controlling virus retention [18] . the following sections are a summary of the recent state of knowledge on factors currently believed to influence microbial persistence and transport in the subsurface. the straining or filtration of bacteria at the soil surface is a major limitation in their travel through soils. when suspended particles, including bacteria, accumulate on the soil surface, as water passes through the soil these par ticles themselves become the filter [26] . such a filter is capable of removing even finer particles, by bridging or sedimentation, before they reach and clog the original soil surface. this phenomenon will in fact largely be dom inant if only a portion of the suspended particles are larger than the pore openings. as soon as a few such particles have accumulated, they become the straining surface for finer particles [26] . in studies in which e. coli suspended in distilled water was allowed to percolate into sand columns, krone [26] found that after the first arrival of bacteria the concentration in column effluents continued to rise until a max imum was reached, after which it fell, suggesting that accumulating bacteria at the soil surface enhances the straining removal. this same effect is seen during the land application of domestic sewage when repeated cycles of flooding and drying of infiltration basins is practiced [27] . for example, at the flushing meadows project near phoenix, arizona, treated sewage effluent is spread into basins underlaid with loamy sand. the greatest numbers of coliforms and fecal coliforms are observed after the start of each new inundation period when newly infiltrated water arrives at the bottom of sampling wells, after which time a general decrease in values occurs. a similar phenomenon occurs when water containing microorga nisms is pumped into recharge wells. studies using sandy soils of various effective porosities indicate removal of bacteria from a liquid percolating through a given depth of soil is inversely proportional to the particle size of the soil. the greatest removal of bacteria occurs on the surface mat (top 2-6 mm) that forms on the soil. adsorption is the major factor in the removal of viruses by soil and also plays a role in bacterial removal. factors that reduce the repulsive forces between the two surfaces, such as the presence of cations, would be ex pected to allow closer interaction between them and allow adsorption to proceed. the very small size of clays, their generally platy shapes, the oc currence of large surface area per given volume, make them ideal adsorption sites for bacteria and viruses in soils. thus, adsorption phenomena will play a more important role in the removal of microorganisms in soils that contain clays [26] . many factors are known to control microbial adsorption to soils and these are listed in tables 9.4 and 9.5. soils differ considerably in their textural, chemical, and mineralogical prop erties and hundreds of soil types have been classified in this country [28] . furthermore, both vertical and horizontal variability is a normal character istic of many soils. it is generally agreed that fine-textured soils retain mi croorganisms more effectively than sandy soils since the soil clay mineral fraction displays a high sorptive capacity toward viruses as a result of its high surface area and ion-exchange capacity. following examination of nine [94] . soils from arkansas and california, it was shown that virus adsorption in creased with the clay content and the specific surface area of the soil [29] . iron oxides, particularly magnetite, also display a high affinity toward viruses [30] . hori et al. [31] found that polio virus removals from distilled water in 6-in columns of three hawaiian soils, including two low-humic latosols (lahaina and wahiawa) and a volcanic cinder (tantalus), averaged >99, >99, and 22 percent, respectively. with the two low-humic latosols, there was a trend of decreased retention over the 5-day test period. goyal and gerba [32] noted considerable differences in the abilities of nine different soils to adsorb a number of enteric viruses. statistical analysis indicated that ph was the most important soil characteristic influencing virus retention, with soils having a ph <5 giving consistently high retention. exchangeable alu minum was another factor that correlated with the adsorption efficiency of in contrast to these findings, wang et al. [35] and lance et al. [36] found greater removal of poliovirus in sandy soils than total and fecal coliforms, and fecal streptococcus. but the lowest removal was observed with coliphage f2 [35] , indicating that virus type plays a significant role in the extent of virus removal. additional studies are needed on the relative re moval of bacteria and viruses by soil types. moore et al. [37] recently reported that poliovirus type 2 adsorption to 34 different soil materials suspended in a synthetic freshwater was neg atively correlated with soil organic matter content and with available neg ative surface charge as measured by adsorption capacity for a cationic polyelectrolyte. soil ph, surface area, and elemental composition were not significantly correlated with virus adsorption. furthermore, additional stud-ies by this same group indicated that the two poorest adsorbents for both poliovirus and reovirus among 34 different soil materials were a muck soil and a silt loam, both of which had high organic matter content [37] . these authors were also able to show a highly negative correlation between virus adsorption and the capacity of soils to bind a cationic polymer, pdadm (polydiallyldimethyl ammonium chloride). it was suggested that the ability to bind the polymer could serve as an indicator of the extent of viral ad sorption [37] . the results of these studies indicate that soil type greatly influences the extent of virus transport or retention. it may be possible to distinguish soils by general class with respect to virus retention, based on their textural, mineralogic, and chemical properties. however, further studies with a wide range of soil types and viruses are needed to determine if such classifications are possible and to identify the soil characteristics that most influence virus retention. the effects of ph on virus adsorption to soils are explainable on the basis of electrochemical features of virus and soil surfaces. the surface charge of a virus is influenced primarily by ionization of the carboxyl and amino groups on the outer surface of the virion protein capsid; and at neutral ph, most viruses are negatively charged. soils also tend to be generally electronega tive at neutral ph; therefore, virus adsorption is not favored due to repul sion of the two negatively charged surfaces. however, if the ph of the surrounding medium is lowered, protonation causes decreased ionization of virion carboxyl groups and increased ionization of amino groups. as a re sult, viruses become less electronegative or even electropositive at lower ph levels. although soil particles will also tend to become more electropositive at lower ph levels, the isoelectric points of soil particles are generally lower than those of viruses. for example, electrophoretic mobility studies have shown that a common soil clay mineral, montmorillonite, is negatively charged at ph 4.5 to 10.5. muck soils also have a high negative charge [38] . at lower ph levels, the viruses may be electropositive but the soils are still electronegative, thereby resulting in electrostatic attraction and increased adsorption. the relationship between virus adsorption and ph is not clearcut, however, because of many complicating factors. the ph of the soil, as conventionally measured, does not reflect necessarily the ph at the surface of soil colloidal particles such as clays. various soil components (clay, sand, oxides of aluminum and iron) display different isoelectric points. there is also a lack of information on the isoelectric points of more than 100 viruses that occur in wastewater or groundwater. so far, we know that the isoelectric point varies with virus type and strain [38] [39] . the results of a number of studies indicate that virus retention by soils generally increases at lower ph levels. in an early report drewry and eliassen [29] found decreased bacteriophage tl, t2, and f2 adsorption to ar kansas and california soils at higher ph levels. more recently, burge and enkiri [33] found that the rates of bacteriophage 0x174 adsorption to five soils were significantly correlated with soil ph. in batch adsorption studies with a variety of viruses and nine soils by goyal and gerba [32] , ph was found to be the single most important soil factor influencing adsorption. soils having a saturated ph less than 5 were the best adsorbers. studies by sobsey et al. [34] showed that poliovirus type 1 and reovirus type 3 adsorp tion to eight different soil materials suspended in settled sewage at ph levels between 3.5 and 7.5 was generally greater at the lower ph levels. in studies by duboise et al. [40] with cores of sandy forest soil receiving poliovirus in sewage effluent at various ph levels between 5.5 and 9.0, virus retention was best at ph 5.5, and the release and migration of retained viruses by subsequent distilled water applications was lower from the cores that re ceived sewage effluent having lower ph values. similar observations have been made for bacteria [41] . the types and concentrations of ionizable salts in the soil-water environment greatly influence the extent of bacteria and virus transport. in general, in creasing concentrations of ionic salts and increasing cation valencies enhance virus adsorption. divalent cations (e.g., ca 2+ , mg 2 + ) are very efficient in promoting virus adsorption to a sandy soil [42] . cations are necessary to reduce the repulsive forces on both the virus and soil particles and allow adsorption to take place. viral and bacterial retention by soils is generally greater in the presence of sewage effluents than in distilled water [40] [41] . wastewater effluents have indeed higher conductivity (500-600 fxmhos/ cm) than distilled water (2-10 fxmhos/cm) or rainwater (20-40 |xmhos/cm). rainwater, being of lower conductivity than sewage effluents, may thus lead to reduced viral and bacterial adsorption or to desorption with the subse quent redistribution of these organisms within the soil profile. this phenom enon was well demonstrated via soil core studies under controlled laboratory conditions [8, 34, 40, 41] . landry et al. [43] showed that virus penetration was more extensive in rainwater-rinsed cores than in wastewater-rinsed cores. moreover, the desorbed viruses may readsorb at greater depths. heavy rainfall might then remobilize soil-bound viruses with the potential contam ination of groundwater supplies [10] . however, it now appears that the ability of rainwater to release viruses depends on the soil type, the release being more pronounced in sandy than in clay soils [34] . the elution pattern also depends on the virus type and strain. for example, poliovirus 3 and echovirus 6 were mobilized by artificial rainwater, whereas echovirus 1 was not affected. the elution pattern of the reference strain of poliovirus 1 differed from that of field and mutant strains [9] . rainfall will also effect bacterial retention by lowering ionic concen tration and increasing infiltration rates. several surveys have indicated that rainfall and well depth are related to microbial groundwater quality. studies in washington indicated that shallow drinking water wells average medium coliform values of 8 mpn per 100 ml with an average depth of 9.4 m (31 ft), while deep wells with an average depth of 153.3 m (503 ft) average 4 mpn per 100 ml [15] . it was also observed that virtually all bacterial con tamination coincided with the periods of heaviest rainfall. brooks and cech [44] observed in rural eastern texas that practically all dug wells with depths of 50 ft (15 m) or less were positive for either fecal coliforms or fecal strep tococci. while presence of fecal bacteria was much less common in deeper wells, some wells as deep as 250 ft (80 m) were positive. increased levels of bacterial contamination of drinking well water after periods of rain have been noted in several studies [23] [24] [25] 45] . in one study, it was noted that while an increase in coliform bacteria appears almost immediately after periods of heavy rainfall in shallow wells, in deeper wells the increase did not occur until 2 weeks later [46] . thus, any satisfactory study of well water quality should include sampling during periods of highest rainfall. soluble organic materials are known to compete with viruses and bacteria for adsorption sites. it may then be possible that organics present in sewage may interfere with virus sorption to soils. however, several studies have shown that viruses are well adsorbed to various types of soils in the presence of secondary and even primary wastewater effluents. as discussed above, wastewater effluents contain enough salts to overcome any interference by soluble organic matter. humic and fulvic acids are highly colored organic compounds that are naturally present in both water and soils. recent studies indicate that these compounds can cause increased virus transport through soils not only by interfering with virus adsorption but also by causing desorption. bitton et al. [48] found that poliovirus retention by columns of sandy soil was exten sively reduced when applied in highly colored (high concentrations of humic and fulvic acids) cypress dome water compared to its retention from tap water. more recently, scheuerman et al. [49] reported extensive interfer ence by humic and fulvic acids with poliovirus type 1 retention in columns of organic sediment, muck soil, and brown-red sand. soils that were capable of retaining all or most of the applied virus in the absence of these organics retained considerably less virus in their presence. the extent of virus trans port through the columns correlated with the color of the column effluents. this phenomenon was confirmed by bixby and o'brien [50] , who re ported that fulvic acids complex ms2 phage and prevent its adsorption to soil. more recently, such soils were found to display a lower adsorption capacity than other mineral soils [34, 37] . the results of a number of studies suggest that organic soils and other soils or waters with high concentrations of humic and fulvic acids may not be suitable for land application of wastewater. the effects of other organics in waters and soils on virus retention remain uncertain. additional studies are needed to further understand and quantify the effects of humic and fulvic acids in water and soil on the infectivity and retention of a variety of viruses in different soils. such studies are also needed for other classes of water, wastewater, and soil organics. hydraulic conditions in soils receiving wastewater appear to have a consid erable effect on virus transport for at least some soils. such conditions as flow rate, hydraulic loading, and application frequency may all influence the extent of virus migration through soils. vaughn et al. [51] reported that infiltration rate greatly influenced poliovirus removal in a groundwater re charge system where tertiary effluent was applied to a coarse sand-fine gravel soil. recharge at 75 to 100 cm per hour resulted in considerable virus movement into groundwater while at two lower recharge rates, 6 and 0.5-1.0 cm per hour, there was considerably less virus movement. at the lower infiltration rates, the surface mat of sewage solids that formed on the soil surface may have contributed to the greater virus removals observed. lance et al. [8] found that poliovirus type 1 removal was not affected by infiltration rates in the range of 15 to 55 cm per day. more recently lance and gerba [52] found that increasing flow rates from 0.6 to 1.2 m per day resulted in increased movement of viruses down the column. however, there was no further increase in virus movement at flow rates up to 12 m per day. in comparative studies of several soils it was found that by linear regression analyses, the rate of virus removal in soil columns was negatively correlated with the flow rate of the percolating sewage effluent [53] . the authors suggested that flow rate of water through the soil may be the most important factor in predicting the potential virus movement into groundwater. little virus movement has been observed in unsaturated soil columns [54] . although the results of at least some studies suggest that virus migra tion increases with increasing hydraulic loads and flow rates and under con ditions of saturated flow, further studies are needed with a wide range of soil types and field conditions to quantify the extent of virus movement through soils under different hydraulic conditions. recent studies have shown that different types and strains of viruses are not equally retained by soils. these virus-specific differences in adsorption to soils are probably related to physicochemical differences in virus capsid surfaces. although all enteric viruses possess outer capsids comprised of polypeptide subunits and generally behave as charged, amphoteric, colloidal particles, the surfaces of the virions differ in the details of their configura tion, charge density and distribution, and other features. in fact, even the same virus can display different surface properties that will influence its physicochemical behavior as a result of conformational changes brought about by ph effects and interactions with soluble chemicals and particulate surfaces [55] . goyal and gerba [32] found that different enteric virus types and strains varied in their ability to adsorb to soils. for example, adsorption efficiencies of six different strains of echovirus type 1 in suspensions of sandy soil in deionized water ranged from 0 to 99.7 percent. type and strain dependence of enterovirus adsorption to a sandy loam soil suspended in distilled water was also reported in another study from the same laboratory [56] . adsorp tion efficiencies of ten different virus types and strains ranged from 0 percent for echovirus type 1, strain v239, and coxsackie virus b4, strain v216, to 99.9 percent for echovirus type 7, wallace strain, and poliovirus type 1, strain lsc. landry et al. [9] reported type and strain differences in enter ovirus adsorption to sandy soil cores. vaccine strain poliovirus type 1 (lsc), a widely employed enterovirus model in soil and other environmental stud ies, was efficiently adsorbed but not readily eluted with either distilled water or sewage effluent. some of the other enteroviruses tested, including field strains, were less efficiently adsorbed and more easily eluted. it was con cluded that vaccine strain poliovirus type 1 may be an inappropriate model for studying the nature and extent of virus transport in soils. in contrast to the findings from batch laboratory studies by the same group, hurst et al. [57] found that under field conditions at a rapid infiltra tion site, echovirus type 1, farouk strain, did not migrate as far down in the soil as poliovirus type 1, strain lsc. they suggested that the adsorptive behavior of viruses in laboratory batch studies may not be totally reflective of their behavior under field conditions, possibly because of virus adsorption to soil particles prior to infiltration. it is now agreed that poliovirus type 1 adsorbs well to most soils. it was recently concluded that viruses may be grouped into three categories according to their adsorptive behavior [39] . category 1 contains the poorly adsorbed viruses (echovirus 1, echovirus 11, coxsackie virus b4, 0x174, ms2) and category 2 includes the highly adsorbed viruses (poliovirus 1, echovirus 7, coxsackie virus b3, t2, and t4). phage f2 was placed in a third category exhibiting the lowest adsorption of all viruses tested. at the turn of the century, it was found that the eating of raw vegetables grown on soil fertilized with raw sewage resulted in outbreaks of typhoid fever. as a result, the survival of enteric bacteria in soil systems has been extensively studied. there are several major reviews on the survival of en teric bacteria in soil [58] [59] [60] , and we will only consider herein factors that affect the length of survival of these bacteria. less is known about virus survival. most enteric bacterial pathogens dieoff very rapidly outside of the human gut, whereas indicator bacteria such as e. coli will persist for longer periods of time. survival times among different types of bacteria and viruses vary greatly and are difficult to assess without studying each type individ ually. in most cases, it appears that 2 to 3 months is sufficient for reduction of pathogenic to negligible numbers once they have been applied to the soil, although survival times as long as 5 years have been reported [59] . factors known to influence bacterial and viral survival in the soil are listed in tables 9.5 and 9.6. a major factor determining the survival of bacteria in soil is moisture. young and greenfield [61] showed that moisture was a factor in the viability of e. coli in soils. beard [62] stated that moisture was the most important deter mining factor in the survival of salmonella typhosa. bacterial survival was determined in various types of soil exposed outdoors in clay flowerpots. the survival in all types of soil tested was found to be greatest during the rainy season. in sand, where drying was rapid due to its low moisture-retaining power, survival time was short-between 4 and 7 days during dry weather. in soils that retain a high amount of moisture such as loam and adobe peat, the organisms persisted longer than 42 days. bouma et al. [63] have suggested that survival data for fecal organisms could be compared with soil-moisture characteristic curves, and hence the distance of soil filteration necessary for removal be defined as a function of moisture content. soil moisture also influences virus survival in soil. bagdasar'yan [64] reported that enteroviruses survived three to six times longer in soils with 10 percent moisture content than in air-dried soils. duboise et al. [5] found that poliovirus type 1 was inactivated considerably more rapidly in drying soil, as the moisture content decreased from 13 to 0.6 percent, than in the same soil type maintained at 15 or 25 percent moisture content. inactivation of 99 percent of the initial viruses occurred within 1 week in drying soil but took 7-8 and 10-11 weeks in soils with 25 to 15 percent moisture content, respectively. yaeger and o'brien [55] compared the degree of poliovirus inactiva? tion in eight different soils saturated with riverwater, groundwater, or septic wastewater and in the same soils that were allowed to dry out during the course of the experiment. upon drying, none of the initial viruses was de tectable in any of the dried soils (>99.999% inactivation), but considerable quantities were still present in the same types of saturated soils. in experi ments on the rate of poliovirus inactivation at different soil moisture levels, there was a sharp increase in the inactivation rate at 1.2 percent soil moisture compared to that at 2.9 percent. hurst et al. [66] also observed differences in poliovirus inactivation rates at different soil moisture levels, with the greatest inactivation rate at a moisture level of 15 percent. inactivation proceeded more slowly at both higher and lower moisture levels, but the slowest inactivation rates were at 5 and 10 percent. in a field study on virus survival in a rapid-infiltration system for wastewater, hurst et al. [57] found that virus inactivation rates were greater in more rapidly drying soils. allowing soils in rapid-infiltration systems to pe riodically dry and become aerated between wastewater applications en hances virus inactivation. the effects of both drying and aerobic microbial activity may contribute to virus inactivation under these conditions. in stud ies on the mechanisms of virus inactivation in soils, yeager and o'brien [55] found that the loss of poliovirus infectivity in moist and dried soils resulted from irreversible damage to the virus particles, including (1) dis sociation of viral genomes and capsids, and (2) degradation of viral rna. in both moist and dried nonsterile soils, viral rna was released from cap sids and found in a degraded form. in dried, sterile soils, viral rna was released but remained largely as intact molecules. viral capsid components were not readily recoverable from drying soils due to irreversible binding, but they could be recovered as empty capsids from moist soils. further experiments with dried viruses showed that their capsids became isoelectrically altered. the results of these studies suggest that poliovirus and perhaps other viruses are inactivated by different mechanisms in moist and drying soils. temperature is a major factor in the survival of enteric organisms in soil and other environments. temperature affects chemical and biologic pro cesses in soils, which may indirectly affect the survival of enteric viruses and bacteria. s. typhosa may survive as long as 24 months at freezing temper atures [62] . mirzoev [67] pointed out that in areas with prolonged winterse.g., the russian arctic-the processes of soil self-disinfection are slowed down or suspended. he showed that low temperatures (down to -45° c) were very favorable for the survival of dysentery bacilli, which he was able to detect 135 days after it had been added to the soil. van donsel et al. [68] found that a 90 percent reduction in the number of fecal coliforms took 3.3 days in the summer and 13.4 days in the winter in exposed soil plots. bagdasar'yan [64] observed that viruses could survive up to 170 days in soil at 3 to 10° c and that survival was higher at 3 to 10° c than at 18 to 23° c. similar observations were made by lefler and kott [42] with regard to poliovirus type 1 and bacteriophage f2 survival in a sandy soil in israel. yeager and o'brien [55] found that coxsackie virus bl inactivation rates in sandy loam soils suspended in riverwater, groundwater, and septic wastewater increased as temperatures were increased from 4 to 37° c. in pilotscale outdoor studies on poliovirus persistence on vegetables and in soils irrigated with sewage effluent in cincinnati, ohio, larkin et al. [69] and tierney et al. [70] found that 99 percent inactivation in soils took about 2 months during the winter months and only 2 to 3 days in the warm summer months of june and july. in a field study by hurst et al. [57] on virus survival and movement in a rapid-infiltration system for wastewater, the rate of inactivation of indigenous viruses was greater in the fall than in the winter, possibly due in part to the effects of higher temperatures in the former season. the direct effects of ionic salts and ph on microbial survival in soils have been less extensively investigated than their effects on virus retention by soils. hurst et al. [57] determined that virus inactivation in soils correlated with soil levels of resin-extractable phosphorous, exchangeable aluminum, and soil ph. because these same factors also influence virus adsorption to soils, the observed differences in survival rates may be related to changes in the extent of virus adsorption to the soil material and, therefore, changes in the extent of virus protection from inactivation in the adsorbed state. beard [62] also found that the death of s. typhosa was very rapid in peat soil with a ph between 3 and 4. kligler [71] found that moist, slightly alkaline soils were the most favorable for the survival of s. typhosa. cuthbert et al. [72] inoculated various peat (ph 2.9-4.5) and limestone (ph 5.8-7.8) soils held in the laboratory with e. coli and strep, faecalis. they found that both organisms could persist for several weeks in the limestone soils, but would die out in a few days in acid peat soils. they felt that the low ph could act to adversely affect not only the viability of the organism but also the availability of nutrients or to interfere with the action of inhibiting agents. the frequent addition of broth culture fluid to soil has been found to in crease the survival of s. typhosa [59] . under field conditions, it has been found that some aftergrowth of e. coli and strep, faecalis can occur, partic ularly after wet weather [68] . the survival of fecal coliforms is greatly ex tended in organic soils over that observed in mineral soils [73] . the extended survival and growth in organic soils may be due not only to the presence of organics but to the high moisture-holding capacity of these soils [73] . the effects of organic matter on enteric virus survival in soils have not been established, but recent findings suggest that fulvic and humic acids may mask virus infectivity by a reversible process. bixby and o'brien [50] found that fulvic acid complexation of bacteriophage ms2 caused consid erable loss of infectivity and prevented adsorption to soil. the infectivity of the complexed phage could be restored by treating with 3 percent beef extract solution at ph 9. soil moisture, temperature, ph, and the availability of organic matter can also indirectly influence the survival of enteric bacteria by regulating the growth of antagonistic organisms [68] . bryanskaya [74] showed that actinomyces in soil were capable of suppressing the growth of salmonella and dysentery bacilli. in addition, the longer survival time of enteric organisms after inoculation into sterilized soil as compared to unsterilized soil found by a number of workers [59] indicates that antagonism is an important fac tor. tate [73] observed that the protozoan population of a muck soil in creased dramatically after addition of e. coli and suggested that soil protozoa could play a significant role in the decline of these organisms in these soils. since it is evident that enteric bacteria are capable of utilizing nutrients found in nature, it could be argued that competition by the natural soil microflora is in large part responsible for their eventual disappearance from the soil. bagdasar'yan [64] noted greater enterovirus inactivation in nonsterile than in sterile sandy and loamy soils, incubated at 3-10 and 18-23° c. in more recent studies by sobsey et al. [34] on rates of poliovirus and reovirus inactivation in eight different soil suspensions in settled sewage at 20° c, the time required for 99 percent inactivation was almost always shorter in nonsterile than in sterile suspensions. hurst et al. [66] observed increased inactivation of poliovirus and echovirus in nonsterile sandy soil wetted with distilled water and incubated under aerobic conditions at 23° and 37° c, compared to sterile control samples. however, inactivation rates in sterile and nonsterile samples were similar at 1° c under aerobic conditions and at 1°, 23°, and 37° c under anaerobic conditions. thus, appreciable virus in activation due to microbial activity in soils appears to occur only under aerobic conditions and at moderate to high temperatures. although the mechanisms of microbially mediated antiviral activity in soils have not been fully elucidated, yaeger and o'brien [55] have reported differences in poliovirus structural changes during inactivation in sterile and nonsterile soils depending on soil moisture level. in both sterile and non sterile soils under moist conditions, viral rna was probably damaged be fore release from capsids. in sterile, dried soils released rna genomes remained largely intact, but in nonsterile, dried soils the released rna was degraded. the role of microbially produced nucleases in these findings is uncertain. data available indicate that viruses survive longer than bacteria in soil (ta ble 9.7) [75] . field and laboratory studies using mcfeters's-type survival chambers indicate that enteric bacteria can survive from a few days to more [22] . than a month [76] [77] . it is also possible that under some conditions they could regrow in groundwater if sufficient nutrients are present. e. coli bac teria have been found to survive and even multiply on organic matter filtered out from lake water during underground recharge projects in israel [78] . in some areas of israel surface water during the rainy season is used to recharge the underground water supply. during those parts of the year when there is an increased need for water the same wells transformed to pumping wells. during such projects it was found that although the water pumped under ground contained less than 2 coliforms per 100 ml after chlorination, the repumped water contained counts as high as 10 5 -10 6 per 100 ml, which persisted for long periods of time after the initiation of pumping. subsequent studies showed that organic matter that had accumulated in the sand around the well casing enabled the regrowth of the few remaining coliforms. also of interest was the finding that so long as recharge continued, the bacteria did not multiply; it was only during the period between recharge and pump ing that growth occurred [79] . enteroviruses have been detected at the surface of soils irrigated with sewage in the united states [80] . a field study revealed virus survival for at least 28 days in soil following application of a package treatment plant effluent in a cypress dome in gainesville, florida [10] . other field studies confirmed the important role played by temperature and soil moisture in virus persistence in soils [57, 81] . similarly, it appears that virus survival in sludge-amended soils is controlled primarily by desiccation and soil tem perature [69, 82] . during surface application of digested sludge on soils in pensacola, florida, it was shown that indigenous enteroviruses were able to survive only 9 days after sludge application [83] . a simple conceptual model based on the current state of knowledge on indicator and pathogen dieoff has been described by reddy et al. [22] . microbial dieoff was described by assuming first-order kinetics. first-order dieoff rate constants (k) were calculated from the literature for enteric mi crobial dieoff in soil-water systems. correction factors were presented to adjust constants for changes in temperature, moisture, and ph of the soil. average dieoff rate constants (log 1() /day _1 ) for selected microorganisms are shown in table 9 .7. in the article by reddy et al. [22] , data on dieoff of viruses during anaerobic digestion were used. only data on virus dieoff in soil systems is shown in table 9 .7. these values were obtained from various experiments and represent an average value of several soil and environ mental variables. such an approach could prove useful for estimating mi crobial survival in soil-water systems, but a greater database is needed especially for viruses and other pathogenic bacteria. also, most of our da tabase on microbial survival is in soil-water systems and not in groundwater. even though there have been no reports of disease outbreaks associated with land treatment of wastewater, there are a growing number of studies concerning the detection of viruses in groundwater after wastewater appli cation to land or direct groundwater recharge. these studies are summarized in table 9 .8. wellings et al. [10] demonstrated vertical and lateral movement of virus in secondary effluent discharged into a cyprus dome (a wetland eco system). poliovirus 1, coxsackievirus b4, and echoviruses 7, 11, and 14 were recovered from 3 m-deep wells in three of 71 samples, at concentrations ranging from 4 to 353 pfu. viruses migrated 7 to 38 m laterally from the application point and survived at least 28 days. the soil at this site ranged from a top 0.6 m layer of black organic soil (4-12% clay) to a sandy clay and a solid blue clay with a permeability of 3 x 10" 2 cm per minute to 3 x 10~6 cm per minute. thus, the viruses moved horizontally as well as vertically and survived many days under ambient conditions, indicating a necessity to evaluate such sites for their aquifer movement and transmission of viruses to drinking water sources. in an earlier study, wellings et al. [84] recovered viruses from groundwater after spray irrigation of secondary sewage effluent onto an imolokee sand (little or no silt or clay). of particular interest in this study was that viruses survived chlorination, sunlight, spraying, and percolation through 3 to 6 m of sandy soil; furthermore, after a period of heavy rains, a burst of viruses was detected in samples that had previously been negative. these studies demonstrate that soil type, rainfall, and other factors can affect viral movement into groundwater, and that viruses are capable of surviving long periods-which, when combined with the ability to move long distances laterally, could lead to wide dispersal through an aquifer. vaughn and landry [85] and vaughn et al. [86] reported isolations of viruses from four groundwater recharge sites, from a stormwater recharge basin, and from groundwater under a sanitary landfill in new york. these sites have soils of coarse sand, fine gravel, and 1 to 2 percent silt. at the groundwater recharge sites, viruses were recovered at depths up to 11.4 m and at distances up to 45.7 m from the injection point of secondary or tertiary chlorinated effluent. as much as 22 to 33 percent of the 100-gal samples at the four sites were positive for viruses, with concentrations of 1.3 to 10.6 pfu per gallon. in addition, total coliforms were found in these samples. in order to reach the groundwater, viruses moved through 5.5 to 9 m of the overlying soil. moreover, at the 12 pines site, viruses were discovered in groundwater under basins where effluent seeded with viruses was applied at rates of 6 to 100 cm per hour. the slower infiltration rates were more effective in re moving the viruses, suggesting that site management is important. both the landfill and stormwater recharge basin also yielded viruses. at the landfill stie, viruses were detected at depths of 22.8 m and up to 408 m downstream. coxsackievirus b3 and other unidentified viruses were de tected. at the stormwater recharge site, samples taken at 9-m depths directly in the basin were positive for echoviruses 11 and 23 and for coxsackievirus a6. this contamination may have originated from runoff from cesspools in the area. schaub and sorber [87] reported on a study of viruses in groundwater under rapid infiltration cells at ft. devens, massachusetts. the soil consisted of silty sand and gravel underlaid by bedrock. the groundwater contained viruses at depths of 29 m and lateral distances of 183 m, with concentrations of about 8.3 percent of the applied effluent. fecal streptococcal bacteria were also found in the 28.9 m-deep well. marker f2 virus was applied at this same site; only about 50 percent of the virus was removed, and it was detectable for at least 11 days. this site was deemed to have poor filtration properties, which points out the need for site-specific evaluation. at the vineland, new jersey, rapid-infiltration site [88] primary ef fluent was applied to cohansey sand and coarse gravel. viruses were found at 16.8 m depths and up to 250 m lateral distances in 19 of 40 samples. polio-, echo-, and coxsackie viruses were identified. total coliforms and fecal coliforms were found consistently at depths up to 6 m beneath the recharge basins. total coliforms also occasionally occurred at greater depths and downstream. in contrast, no fecal coliforms were found in samples taken below 9.1 m and coliforms occurred only once in a shallow well 50 m downgradient. thus, viruses penetrated deeper into the ground and moved longer distances than did the coliforms. the potential for viruses to migrate great distances, as in the previous study, was further demonstrated by noonan and mcnabb [89] , who used the phages 0x174 and t4 to demonstrate lateral movements of 140 m and 911 m, respectively, in new zealand groundwater in just 96 hours. the viruses moved at greater than 300 m per day and survived for at least 7 days. in laboratory studies, 6.2 days were necessary for a 90 percent reduc tion in liter; so in this case, the viruses could theoretically travel at least 2.5 km in groundwater before a 90 percent reduction could be effected under these conditions. viruses in groundwater at other recharge sites have been studied with varying success. at the flushing meadows site near phoenix, arizona [90] , it was found that a fine loamy sand over coarse sand and gravel effectively removed viruses. laboratory studies confirmed that this soil was an excellent adsorber. no viruses were detected in any of the samples of renovated water, even though levels of 158 to 475 pfu per liter were detected in the effluent applied. however, coliform organisms were detected in the reno vated water, suggesting that the removal mechanisms must have been dif ferent for viruses and bacteria, and that viruses may have been present. since this site is no longer in existence, these findings cannot be confirmed. however, since then, virus has been detected in a sample from an 18.3 mdeep well at a nearby land application site. the isolate was identified as coxsackievirus b3. at two land treatment sites where sewage is used to irrigate cropland, both positive and negative virus isolations have been made [80, 88] . at the lubbock, texas, site, coxsackievirus b3 was isolated from a depth of 30.5 m; at roswell, new mexico, no virus isolates were detected in samples taken from 3 to 30 m depths. in the latter case, irrigation is seasonal and inter mittent, whereas application at the lubbock site is continuous. at an operational land application site in kerrville, texas [91] , no viruses were detected in the monitoring wells at depths of 10.7 to 19.8 m even though viruses could be detected in 1.4 m-deep lysimeters. in one often-cited report [92] on the santee project, no viruses were detected in renovated water. this is not surprising, since the detection meth ods available at that time were not quantitative. these negative results must therefore be considered highly questionable, as should the results obtained at the whittier narrows, california [33] , projects, which did not employ techniques sensitive enough to detect low levels of virus. this situation reiterates the need for careful evaluation of methods used in any report before negative conclusions are accepted. summaries of data on the soil penetration of bacteria at some of the most important rapid-infiltration systems land treatment sites are presented in table 9 .9. the data suggest that bacteria at rapid-infiltration sites may pen etrate about 10 m vertically and variable distances laterally. these distances are, of course, highly site-specific, and the vertical distance may be more than 10 m but is usually much less. to prevent the entry of enteric bacteria into groundwater, it would thus be advisable (unless an underdrain system is installed) not to site land treatment systems where the water table is shallow, particularly if the soil is sandy or gravelly, large cracks or root tunnels are present, or a thin soil mantle overlies rock with solution channels or fissures. this is especially true for rapid-infiltration systems. once in the groundwater, the bacteria may travel long distances in situations where coarse soils or solution channels are present, but normally the filtering action of the matrix should restrict horizontal travel to only a few hundred feet. the actual distance travelled also depends on the rate of movement of the groundwater and the survival time of the bacteria. the rate of movement of groundwater is highly site-specific but often is ex tremely slow. from the foregoing discussion, it is apparent that many factors control the removal of pathogenic bacteria and viruses during the percolation of sewage through the soil. most of this chapter has dealt with the fate of viruses in soil because of their apparent greater potential for health problems associ ated with land treatment. although the presence of viruses in groundwater has been demonstrated, it would appear that with proper site selection and management the presence of viruses could be minimized or eliminated. the key is to define the processes involved in the survival and transport of pathogens in groundwater. with proper design, land treatment could be used as an effective method for reducing the number of pathogens in wastewater. with the proper soil type, viruses and bacteria can be reduced to levels as effectively as by chlorination as currently practiced, after the travel of wastewater through only a few centimeters of soil. as we have shown, high removals by soil can be achieved from even raw wastewater. in the soil natural processes will eventually destroy the pathogens. thus, in groundwater recharge operations, the soil should be considered as part of the treatment process and not simply as a final disposal source. the key to operating such systems for pathogen removal is to gain an understanding of the processes involved and methods by which they can be quantified and controlled. based on both field and laboratory experiments, several potential treatment practices may be useful in enhancing virus removal during land application of sewage, and these are summarized in table 9 .10. [11] . waterborne disease-a status report emphasizing outbreaks in groundwater review of the causes of waterborne disease outbreaks out breaks of waterborne disease in the united states viruses in soil systems magnitude of the groundwater contamination problem wastewater bacteria and viruses in soil virus movement in soil col umns flooded with secondary sewage effluent adsorp tion of enterovirus to soil cores and their subsequent elution by artificial rainwater demon stration of virus in groundwater after effluent discharge into soil viruses in groundwater waterborne disease: occurrence is on the upswing bacterial contamination of drinking water supplies in a mod ern rural neighborhood a review of infective dose data for enteroviruses and other enteric microorganisms in human subjects public health implications of the appli cation of wastewaters to land gastroenteritis association with a sewage leak health effects of land treatment; microbiological viruses in water: the problem, some solutions virus survival in wastewater treatment viruses in sewage: effect of phosphate removal with calcium hydroxide (lime) appropriate technology for water supply and sanitation: health aspects of excreta and sillage management-a state of the art review behavior and transport of microbial pathogens and indicator organisms in soils treated with organic wastes well-water quality deteri oration in central pierce county, washington the relationship between rainfall and well water pollution in a west african (gambian) village the pollution hazard to village water supplies in eastern botswana the movement of disease producing organisms through soils high-rate land treatment. ii. water quality and economic aspects of the flushing meadows project fundamentals of soil science virus movement in groundwater adsorption of viruses onto surfaces in soil and water migration of poliovirus type 2 in percolating water through selected oahu soils comparative adsorption of human enteroviruses, simian rotavirus, and selected bacteriophages to soils virus adsorption by five soils interactions and survival of enteric viruses in soil materials comparative movement of dif ferent enteroviruses in soil poliovirus adsorption by 34 minerals and soils influence of ph and electro lyte composition on adsorption of poliovirus by soils and minerals quantitative assess ment of the adsorptive behavior of viruses to soils poliovirus survival and move ment in a sandy forest soil effect of dissolved salts on the filtration of coliform bacteria in sand dunes virus survival in water and wastewater systems poliovirus retention in 75-cm soil cores after sewage and rainwater application nitrates and bacterial distribution in rural do mestic water supplies bacterial contamina tion of drinking water supplies in a modern rural neighborhood hohe nitratgehalte in einem landlichen gebiet in nigeria verursacht durch ungeordnete ablagerung hauslicher alofalle and exkremente poliovirus removal from primary and sec ondary sewage effluent by soil filtration effect of secondary treated effluent on the movement of viruses through a cypress dome soil transport of viruses through organic soils and sediments influence of fulvic acid on bacteriophage adsorption and complexation in soil virus re moval during groundwater recharge: effects of infiltration rate on adsorp tion of poliovirus to soil poliovirus movement during high rate land filtration of sewage water effect of soil permeability on virus removal through soil columns enterovirus inactivation in soil type and strain dependence of enterovirus adsorption to activated sludge, soils, and estuarine sediments survival of enteroviruses in rapid-infiltration basins during the land application of wastewater the use of sewage for irrigation: a literature review literature review on the occurrence and survival of enteric, pathogenic and relative organisms in soil, water, sewage and sludges, and on vegetation recycling treated municipal wastewater and sludge through forest and cropland observations on the viability of the bact. coli group under natural and artificial conditions longevity of eberthella tyhosus in various soils university of wiscon sin-extension geological and natural history survey survival of viruses of the enterovirus group (poliomy elitis, echo, coxsackie) in soil and on vegetables infectious disease potential of land application of wastewater effects of environmental variables and soil characteristics on virus survival in soil extent of survival of dysentery bacilli at low temperatures and self-disinfection of soil and water in the far north seasonal variations in survival of indicator bacteria in soil and their contribution to storm-water pollution persistence of virus on sewage-irrigated vegetables persistence of poliovirus 1 in soil and on vegetables grown in soil previously flooded with inoculated sewage sludge or effluent investigations of soil pollution and the relation of the various types of privies to the spread of intestinal infections survival of bacterium coli type 1 and streptococcus faecalis in soil cultural and environmental factors affecting the longevity of escherichia coli in histosols antagonistic effect of actinomyces on pathogenic bac teria in soil virus survival in receiving water comparative survival of indicator bacteria and enteric pathogens in well water survival of enteric viruses and indicator bacteria in groundwater water quality aspects of groundwater recharge in israel clogging and contamination processes in re charge wells viruses in groundwater be neath sewage irrigated cropland high levels of microbial contamination of vegetables irrigated with wastewater by the drip method fate of vi ruses following land application of sewage sludge. i. survival and transport patterns in core studies under natural condition survival of enteroviruses and coliform bacteria in a sludge lagoon virus survival following wastewater spray irrigation of sandy soils an assessment of the occurrence of hu man viruses in long island aquatic systems survey of human virus occurrence in wastewater-recharged groundwater on long island virus and bacteria removal from wastewater by rapid infiltration through soil long-term effects of land application of domestic wastewater the quality and movement of groundwater in alluvial aquifers of virus and bacteria removal from wastewater by land treatment viral transport to groundwater at a wastewater land application site virologic assess ment of sewage treatment at water reclamation at whittier nar rows groundwater pollution microbiology virus removal following wastewater spray irrigation of sandy soils long-term recharge of trickling filter effluent into sand dan region project, groundwater recharge with municipal effluent virus removal with land filtration key: cord-315094-pzixgqcy authors: benetka, viviane; kübber-heiss, anna; kolodziejek, jolanta; nowotny, norbert; hofmann-parisot, margarete; möstl, karin title: prevalence of feline coronavirus types i and ii in cats with histopathologically verified feline infectious peritonitis date: 2004-03-26 journal: vet microbiol doi: 10.1016/j.vetmic.2003.07.010 sha: doc_id: 315094 cord_uid: pzixgqcy feline coronaviruses (fcov) vary widely in virulence causing a spectrum of clinical manifestations reaching from subclinical course to fatal feline infectious peritonitis (fip). independent of virulence variations they are separated into two different types, type i, the original fcov, and type ii, which is closely related to canine coronavirus (ccv). the prevalence of fcov types in austrian cat populations without fip has been surveyed recently indicating that type i infections predominate. the distribution of fcov types in cats, which had succumbed to fip, however, was fairly unknown. pcr assays have been developed amplifying parts of the spike protein gene. type-specific primer pairs were designed, generating pcr products of different sizes. a total of 94 organ pools of cats with histopathologically verified fip was tested. a clear differentiation was achieved in 74 cats, 86% of them were type i positive, 7% type ii positive, and 7% were positive for both types. these findings demonstrate that in fip cases fcov type i predominates, too, nonetheless, in 14% of the cases fcov type ii was detected, suggesting its causative involvement in cases of fip. feline infectious peritonitis (fip) is a fatal, immune-mediated disease of domestic and wild fe-et al., 1982; wege et al., 1982) . barlough et al. (1985) showed that an infection with ccv caused seroconversion but no clinical signs in the cats examined, neither was the course of the subsequently experimentally induced fip disease more severe. in contrast to these findings, mcardle et al. (1992) demonstrated that after infection with ccv the course of fip disease was more severe, and that ccv induced in some cats similar symptoms as in the dog. furthermore, one ccv strain caused in a cat clinical symptoms which were not discernible from fip. after all, the importance of ccv for the cat remains uncertain (sparkes et al., 1992) . two biological types of fcovs are known, feline infectious peritonitis virus (fipv) and feline enteric coronavirus (fecv) (pedersen, 1976b (pedersen, , 1983 (pedersen, , 1987 pedersen et al., 1981) . the genome of some fecv strains proved to be 0.3 kb shorter, suggesting a deletion of 300 bp at the 3 -end (vennema et al., 1992) . molecular studies showed that fipv arises by mutation from fecv (pedersen et al., 1981; evermann et al., 1991; hök, 1993; poland et al., 1996; herrewegh et al., 1997; vennema et al., 1994 vennema et al., , 1998 . both fipv and fecv may, depending on their virulence, cause viremia (herrewegh et al., 1995; fehr et al., 1996; gunn-moore et al., 1998; horzinek, 2000) . fcovs are separated into two different types based upon their growth ability in vitro, their antigenic relationship to ccv, their neutralisation reactivity with sprotein-specific mabs (fiscus and teramoto, 1987a,b; hohdatsu et al., 1991 hohdatsu et al., , 1992 and upon sequence analysis of the s-protein gene (motokawa et al., 1995) . while type i shows no or little replication in cell culture (fipv ucd1, ucd2, ucd3, ucd4, tn-406, nw1, yayoi, ku-2, dahlberg, fecv ucd), type ii induces a lytic cytopathic effect (fipv 79-1146, nor15 (df2) , cornell-1, fecv 79-1683) . the ability of an fcov strain to propagate in cell culture does not correlate with its virulence in vivo (mochizuki et al., 1997) . among the fcov types i and ii, both fipv and fecv strains are represented. the s-protein gene of type ii is closely related to those of tgev and ccv, showing a similarity of the nucleotide sequence of 91 and 81%, respectively, but of only 46% with the s-protein gene of type i (motokawa et al., 1995) . herrewegh et al. (1998) demonstrated that fcov type ii resulted from recombination of fcov type i with ccv. recent studies indicate that type ii uses the feline aminopeptidase n (fapn), a cell-surface metalloprotease on the intestinal, lung and kidney epithelial cells, as receptor, and that fapn may also bind ccv, tgev and hcv. it is not clear whether or not this receptor specificity of type ii plays a role in the pathogenesis or pathological alterations of fip (williams et al., 1991; de groot and horzinek, 1995; hohdatsu et al., 1998; tresnan and holmes, 1998) . the prevalence of types i and ii has been surveyed in two studies from austria and japan, respectively, both suggesting that the majority of fcov infections is due to type i (hohdatsu et al., 1992; posch et al., 1999 posch et al., , 2001 . fcovs are ubiquitous in the cat population, highly infectious by the oronasal route and therefore endemic in multi-cat households, catteries and shelters. investigations showed that a high percentage of cats without fip symptoms from exposed environments were positive for fcov infection: 39-85% were seropositive, 37-95% viremic and 73-81% excreted virus in their faeces (addie and jarrett, 1992b; sparkes et al., 1992; herrewegh et al., 1995; foley et al., 1997a,b; gunn-moore et al., 1998) . posch et al. (1999 posch et al. ( , 2001 found 71% seropositive cats in austrian cat populations without signs of fip, 26% of these cats tested positive for fcov nucleic acid in blood. there is strong evidence for the existence of persisting and chronic infections, with virus persisting in the intestine and other organs of healthy cats. asymptomatic carriers may excrete virus over a period of months or even years (foley et al., 1997a; herrewegh et al., 1995 herrewegh et al., , 1997 . asymptomatic carriers and shedders represent coronavirus reservoirs and therefore the main problem in the prevention of fip in multi-cat environments (addie and jarrett, 1992a,b; addie et al., 1995 addie et al., , 1996 foley et al., 1997a,b; herrewegh et al., 1997) . approximately 5-10% of seropositive cats develop fip, with the highest incidence in cats between 6 months and 5 years of age, and the majority of cases occurring in cats ≤1 year of age (scott, 1991; addie and jarrett, 1992a) . the higher incidence of fip among purebred cats (scott, 1991) , cheetahs (evermann et al., 1988) and cats from fip-susceptible bloodlines may be an indication for a genetic predisposition. in addition, the sex of the host may influence the outbreak of the disease. while pedersen (1976a) found no generic disposition, potkay et al. (1974) and binder and hartmann (2000) observed a higher incidence of fip among males than among females. although serological testing by immunofluorescence assay (ifa) (moestl, 1983) or elisa (mochizuki and furukawa, 1989 ) is a helpful tool for fip diagnosis, results can only be interpreted in correlation with clinical symptoms (sparkes et al., 1991) . at present, the only conclusive fip diagnosis can be established by histopathological examination of a biopsy or post mortem material. the recently developed reverse transcriptase polymerase chain reaction (rt-pcr) assays, using primers targeted to highly conserved regions of the viral genome (3 -utr (untranslated region) (herrewegh et al., 1995; fehr et al., 1996) , or s-protein gene (li and scott, 1994; gamble et al., 1997) ), which are common to all fcov strains, became a valuable tool for the detection of fcov nucleic acid in blood, body cavity effusions, faeces and tissue samples of infected cats. in particular the n-terminal domain of the s-protein gene allows a differentiation between the two types i and ii. posch et al. (1999 posch et al. ( , 2001 developed an rt-pcr using primers targeted to the s-protein gene to study the prevalence of the two fcov types in cats without fip symptoms, and showed that 55% of the pcr-positive cats proved positive for type i, 28% for type ii and 17% for both types. with the retrospective study presented here we investigated the prevalence of the two types of fcovs in cats with histopathologically verified fip using nested and seminested rt-pcr assays, with primers targeted as well to the s-protein gene. the aim of this study was to investigate the distribution of the two fcov types in fip diseased cats. furthermore-since fcov types i and ii may use different receptors-we wanted to investigate whether the two types are associated with differences in the clinical course of the disease and/or distinct histopathological changes. finally we intended to get more information about the importance of ccv for the cat. ccv itself may infect the cat, or it may be involved indirectly, regarding the possibility that recombinations between fcov type i and ccv may happen in the field at any time (horzinek, 2000) . between 1997 and 2000 a total of 1754 cats were examined at the institute of pathology and forensic veterinary medicine of the university of veterinary medicine, vienna, and 154 of these cats were diagnosed with fip. the analysis of breed, gender and age of the 154 cats with fip compared to the 1600 cats without fip symptoms is shown in table 1 . the statistical evaluation of the parameters breed, gender and age in the two groups "cats with fip" and "cats without fip" was carried out by χ 2 -test using the program spss for ms windows, version 8.0. from 94 of the 154 cats with histopathologically confirmed fip organ samples (lung, liver, spleen, kidney, gut) were available, either formalin-fixed paraffinembedded tissues (pet) (n = 65, 1997-1998) or fresh organ samples (n = 29, 1999-2000) . pet samples had been fixed in buffered formaldehyde for 48 h and were then embedded in paraffin. fresh organ samples were taken during section and either processed immediately or stored at −80 • c until used. the preparation of pet samples was carried out essentially as described by sorg and metzler (1995): four to six 5 m thick sections of paraffin-embedded organs from each cat were pooled and deparaffinised by incubating for 30 min in xylene and washing twice for 5 min in ethanol at room temperature. after centrifugation and air drying for 10 min at 37 • c, 25-50 l proteinase k and 200-400 l (depending on the sample size) buffer atl (qiagen, valencia, ca, usa) were added and the samples were then incubated at 37 • c for 5 days. when necessary, another equivalent of proteinase k and buffer atl was added at the second or third day of incubation. after inactivation of proteinase k at 95 • c for 8 min and centrifugation, rna was extracted from the upper aqueous phase using a commercially available kit (qiaamp viral rna mini kit, qiagen, valencia, ca, usa). the extracts were then stored at −80 • c. one to three grams of each organ sample were pooled and homogenised with sterile sand, and resuspended in 2-3 ml diethyl pyrocarbonate (depc)treated water. after centrifugation the rna was the general screening for fcov was carried out by rt-and nested (n) pcr as described by herrewegh et al. (1995) using the primers p205 and p211 for rt-pcr and p204 and p276 for npcr, respectively. samples positive in these assays were submitted to further analysis employing oligonucleotide primers, which had been designed in regions of the s-protein gene allowing a differentiation between fcov types i and ii. to improve the sensitivity of the pcr assays, a second round of amplifications (npcr with primers b, seminested with primers a) was carried out following rt-pcr. the primers were selected with the help of the primer designer program (scientific and educational software, version 3.0) and are shown in table 2 . rt-pcr was carried out as a single-tube assay with a reaction volume of 25 l (22.5 l pcr mixture and 2.5 l template) using a commercially available kit (access rt-pcr system, promega, madison, wi, usa). the mgso 4 concentration was optimised at 1 and 2 mm using the primers fecv1 and fecv2, respectively. negative samples were re-tested by employing the one step rt-pcr kit from qiagen (valencia, ca, usa). cycler schemes were carried out following the instructions of the manufacturers. an amount of 2.5 l of the rt-pcr product was added to 22.5 l of the master mix for npcr and seminested pcr, respectively, containing 10 mm tris-hcl (ph 9 at 25 • c), 50 mm kcl, 0.1% triton x-100, 200 m each 2 -deoxynucleoside 5 -triphosphate, 1.5 mm mgcl 2 , 1.25 u taq polymerase and 40 pm of each primer. forty-five cycles of denaturation at 94 • c, primer annealing at 60 • c and primer extension at 72 • c, 30 s each, were employed. as the possibility of false positive results due to carryover of amplification products in particular during npcr cannot be ruled out, a number of precautions were taken to minimise the risk of contamination. these included the physical separation of all pcr procedures, the use of at least four negative controls of rnase free water for each assay and of three or more primer pairs for each sample. the rt-pcr amplification product was added to the master mix for the npcr in a laboratory specifically installed for this purpose. finally sequence analysis of 15 amplification products served as an additional control. twenty microlitres of each pcr product were analysed by electrophoresis in a 1% agarose gel for 1 h 10 min at 90 v, and visualised by ethidium bromide staining. the 100 bp ladder (amersham pharmacia biotech inc., piscataway, nj, usa) served as molecular weight marker. bands were visualised with uv illumination and photographed using the eagle eye tm ii uv gel imaging system (stratagene, la jolla, ca, usa). sequence analysis was performed after gel extraction of the amplified product (qia quick gel extraction kit, qiagen, valencia, ca, usa) and sequencing pcr (abi prism big dye tm terminator cycle sequencing ready reaction kit, perkin elmer, alameda, ca, usa) using the sequence analyser abi prism 310 genetic analyser (pe applied biosystems). partial nucleotide sequences (a stretch of 108 bp within the s-protein gene region) of selected 11 type i and 2 type ii positive samples, as well as one of the five samples which had tested positive for both types, were determined; their alignment is shown in fig. 1 . extracts of cell culture supernatants from five different fcov-strains (type i: fipv ku2, fipv nw1; type ii: fipv 79-1146, fecv 79-1683, fipv df2) were submitted to rt-pcr, nested and seminested pcr employing the primers fecv1a, fecv1b, fecv2a and fecv2b. gel extracts of the strains fipv ku2 and fipv 79-1146, containing 8.85 and 6.69 pmol/l dna, respectively, obtained after rt-pcr with the primers fecv1b and fecv2b, were diluted in rnase free water with a concentration of 1% trna, and served as template for npcr. as far as antibody titres had been recorded in the case histories, they were compared to the pcr results. the results of the pathological examination were analysed according to the following criteria: during section the presence and amount of fip typical effusion (low, medium, high amount) and of fip suspicious granulomas and pyogranulomas (granulomas yes, no and localisation) were recorded. the subsequent histopathological examination confirmed the diagnosis fip only in the presence of the typical vasculitis with central necrosis and perivascular infiltration with plasma cells, macrophages, lymphocytes and neutrophils. general data of 154 fip-diseased cats were analysed and compared to those of 1600 cats without fip symptoms examined during the same period of time (1997) (1998) (1999) (2000) at the institute of pathology and forensic veterinary medicine of the university of veterinary medicine in vienna (table 1 ). the statistical examination showed that the incidence of fip was significantly higher among males versus females (p = 0.035), among purebred versus domestic short hair cats (p = 0.000) and among young animals up to 1 year (p = 0.000). a significantly greater number of males among fip-diseased cats was found in the age category 0-1 year (p = 0.04), but in cats older than 1 year this trend could not be observed (p > 0.05). while 6 of the 65 pet samples tested negative, nucleic acid could be detected in all 29 fresh organ samples with the primers described by herrewegh et al. (1995) . the differentiation of the two types was accomplished in 47 of the 59 pet samples which tested positive for fcov (the pcr result of one additional sample was questionable) and in 27 out of 29 fresh organ samples (one additional questionable result). in total, a differentiation was possible in 74 samples. among these, 64 (86%) tested positive for type i, 5 (7%) for type ii and 5 (7%) for both types i and ii (table 3) . of the 69 samples positive for type i, 68 tested positive with the fecv1b primers, 25 with both the fecv1a and fecv1b primer pairs, and 1 with the fecv1a primers only. of the 2 samples with a questionable pcr result, 1 tested questionably positive with the fecv1a primer pair and negative with the fecv1b primers, the second one vice versa. of the 10 samples positive for type ii, 1 tested positive employing the fecv2a primers and 9 using the fecv2b primers. of these results 60 (58%) were already achieved after rt-pcr. extracts of cell culture supernatants of five different fcov strains, the type i strains fipv ku2 and fipv nw1, and the type ii strains fipv 79-1146, fecv 79-1683 and fipv df2, were subjected to rt-pcr and nested or seminested pcr with the primer pairs fecv1a, fecv1b, fecv2a and fecv2b. employing the primers fecv1a and fecv1b, the type i strains ku2 and nw1 showed amplification products of the estimated size, whereas the type ii strains 79-1683, 79-1146 and df2 tested negative (fig. 2, primers fecv1b ). with the primers fecv2a and fecv2b the strains 79-1683, 79-1146 and df2 tested positive whereas the type i strains remained negative (fig. 3 , primers fecv2b). gel extracts of the strains fipv ku2 and fipv 79-1146, obtained after rt-pcr with the primer pairs fecv1b and fecv2b, tested positive in the nested pcr assays up to a dilution of 10 −6 and 10 −9 , respectively. antibody titres to fcov were known from the case history for 25 cats, 20 of them had titres of ≥1:400, 3 of 1:100, 1 of 1:10 and 1 was indicated as serologically negative. in the group of cats with fcov antibody titres of ≥1:400 twelve tested positive for fcov nucleic acid of type i and were negative for type ii, and one was positive for type ii but negative for type i; for seven cats a differentiation between the two types could not be achieved. all three cats with titres of 1:100 tested positive for type i and negative for type ii. the single cat with a titre of 1:10 and the sero-negative cat tested both negative for fcov nucleic acid. partial nucleotide sequences of the s-protein gene of 11 type i and 2 type ii positive samples as well as of one sample positive for both types were deter-mined. the sequences were compiled (resulting in a readable stretch of 108 bp) and aligned using the sequence of the type i strain fipv ku2 as a reference. in the alignment, also the corresponding sequences of the fcov type ii reference strain 79-1146 and of the ccv reference strain insavc-1 were included. the analysis of the samples revealed a nucleotide identity of 86-91% for the type i specimens, and of 73-75% for the type ii samples, respectively, in reference to the type i strain fipv ku2 (fig. 1) and of 77 and 78% for the type ii specimens in reference to the ccv strain insavc-1. histopathologic examination exhibited no differences related to the type of fcov detected. both types were found in effusive and non-effusive fip as well as in cases with signs of both forms; a statistical evaluation was not possible due to the small number of type ii positive samples. the comparison of the two groups, cats with fip (n = 154) and cats without fip symptoms (n = 1600) examined in the years 1997-2000 at the institute of pathology and forensic veterinary medicine of the veterinary university in vienna showed significant differences. the statistical evaluation using the χ 2 -test of the parameters breed, gender and age in the two groups showed that the incidence of fip was significantly higher among purebred cats, males, and among cats 1 year of age or younger. the percentage of purebred cats in fip-diseased cats was more than twice as high as in the comparative group (33.6% versus 13.5%, p ≤ 0.001). these findings are sustained by earlier studies (pedersen, 1983) . foley and pedersen (1996) observed a higher susceptibility for fip in purebred cats when a first degree relative succumbed to fip. due to inbreeding a genetic predisposition may have evolved in certain breeds of cats, which may allow fcov to propagate more efficiently in these cats than in cats with a wider genetic history. in the group of the cats with fip, the majority was male (62.4%), only 37.6% were female. although in the comparative group the percentage of males was slightly higher as well (53.4% males versus 46.6% females), the difference between the groups was significant (p ≤ 0.05). these findings are in contrast to pedersen (1976a) , who did not find a sexual predisposition, but in accordance with potkay et al. (1974) and binder and hartmann (2000) , who also reported a higher incidence of fip among males. the majority of the cats with fip was 1-year-old or younger (52.1%), in the comparative group only 33.1% were in this age class. addie and jarrett (1992a) found as well as scott (1991) a higher incidence of fip in cats of up to 1 year. when comparing the incidence of males and females in the age groups 0-1 year and older than 1 year between the cats with and without fip, we found that among younger cats the incidence of males was significantly higher in the cats with fip than in the comparative group. the role of sex-specific differences in the immune system, in particular the cell mediated immunity and the importance of these factors in neutered animals (hormonal influence) are still not clear. in a total of 93.6% of the samples, fcov nucleic acid could be detected. only six pet samples tested negative, whereas all fresh organ samples tested positive. in respect to the expected lower rna concentration in the pets due to the formalin fixation procedure on one hand and due to the long storage time (2-3 years) on the other hand, we chose primers which amplified, compared to those employed by posch et al. (1999 posch et al. ( , 2001 , a smaller segment of the viral genome. with these primers we achieved a differentiation of the two types in 47 of 65 pet specimens and in 27 of 29 fresh organ samples, in addition two samples exhibited a questionable pcr result. as expected, the percentage of positive pcr results was lower in the pet samples than in the fresh organ samples. specificity was tested on five different fcov strains with four different primer pairs (figs. 2 and 3, primers fecvb). we found no false positive results and all amplification products showed bands of the expected size. despite the use of different primer pairs, in some samples the pcrs remained negative, probably due to the variability in the s-protein gene of fcov. the oligonucleotide primers employed in the pcr assays exhibited high sensitivity, the fecv1b primers proved to amplify specific nucleic acid up to a dilution of 10 −6 , and the fecv2b primers showed amplification even up to a dilution of 10 −9 . since the original rna concentration was similar in both samples, these findings indicate a higher sensitivity for the detection of type ii viruses. thus, in those samples, in which the differentiating pcr was unsuccessful, fcov type i may predominate as well. on the other hand, due to the lower sensitivity of the type i pcr, we cannot exclude a causative involvement of type i in the type ii positive cats. of the 74 samples in which a differentiation was achieved, 64 (86%) tested positive for type i, 5 (7%) for type ii and 5 (7%) for both types i and ii, thus identifying type i as the causative agent in the majority of the fip cases we examined. whereas posch et al. (1999 posch et al. ( , 2001 identified type ii in 45% (including those samples with both types) of fcov-positive cats without fip symptoms, we found type ii only in 14% of cats with fip involved, among them 7% showing a double infection with both types i and ii. these findings are in contrast to the results of hohdatsu et al. (1992) in japanese cats, in which none of the healthy cats tested positive for type ii, whereas among the chronically diseased cats without fip symptoms over 10% and among the fip-diseased cats even more than 30% were infected with fcov type ii. due to their close antigenic relationship in the s-protein gene and the need to choose primers from this region for a possible differentiation between the two fcov types, an infection with ccv would also have been detected (data not shown). therefore, a causative involvement of ccv in the type ii positive fip cases cannot be ruled out in this study. the importance of ccv for the cat still remains unclear (barlough et al., 1985; mcardle et al., 1992) , but the possible recombination between fcov type i and ccv horzinek, 2000) requires further investigation, in particular the role of ccv in double infections with both fcov types observed especially in multi-cat households. the temperature-sensitive fipv strain used as fip vaccine is a type ii strain (fipv df2). regarding the fact that the majority of the fip cases we examined was due to type i, the question arises whether this fact contributes to some of the observed vaccine failures, and whether the inclusion of also a type i strain in the vaccine should be considered. the sequencing results show even in the very short region, which had been sequenced, a clear discrimination between fcov type i, fcov type ii and ccv strains (fig. 1) . the 11 partial sequences of the austrian fcov type i samples show significant differences, compared to the reference strain ku2, which resulted in identity rates of (only) 86-91% to the reference strain; also within the austrian fcov type i samples several nucleotide changes can be noticed, indicative of a quite high mutation rate. the fcov type ii samples form an own group with an identity to the fcov type i reference strain of only 73-75%, respectively. ccv exhibits an identity to fcov-1 ku-2 of 72%; its much closer relationship to fcov type ii than to fcov type i can nicely be observed by the similarity of several nucleotide changes of fcov type ii and ccv. these findings support the observation that fcov type ii may arise from recombinations with ccv . nonetheless, ccv also exhibits several unique nucleotide changes. the sequencing data of one of the five samples showing double infections (fig. 1) demonstrate clearly the plausability of such co-infections. among the cats with known antibody titres, all cats positive for fcov nucleic acid showed antibody titres of 1:100 or higher. neither during section nor in the histopathologic examination any differences related to the fcov type detected could be identified. in the group of the type i positive cats 58% showed signs of both forms (effusive and non-effusive) of fip, followed by 28% with non-effusive and 14% with effusive fip. in the type ii positive samples all forms of fip were represented as well. these findings do not point towards a pathogenetic importance of the receptor-specificity of type ii (hohdatsu et al., 1998) , but emphasises the role of the immune response and the genetic predisposition of the individual in the outbreak of the disease. our findings suggest an involvement of each of both fcov types in fip which is in accordance with earlier reports that both types of fcov are able to cause fip; they also correlate with the results obtained in healthy fcov-infected cats, supporting the predominance of fcov type i infections in both fcov-infected healthy and fip-diseased cats. fcov type ii, the probable recombination between type i and canine coronavirus, was involved in 14% of the fip cases investigated. it has to be assumed that these recombinations occur in the field and therefore contact with dogs excreting canine coronavirus may play a role in the emergence of new type ii fcov. however, the samples positive for fcov type ii need further investigations with respect to their relationship and even differentiation to ccv. special interest should also be paid to cats with double infections concerning the role of field infections with ccv and their role in the development of fip. finally, no differences in the histopathological changes were found related to the fcov type detected. a study on naturally occurring feline coronavirus infections in kittens feline coronavirus antibodies in cats risk of feline infectious peritonitis in cats naturally infected with feline coronavirus feline coronavirus in the intestinal contents of cats with feline infectious peritonitis experimental inoculation of cats with canine coronavirus and subsequent challenge with feline infectious peritonitis virus klinik der felinen infektiösen peritonitis. 9 feline infectious peritonitis biological and pathological consequences of feline infectious peritonitis virus infection in the cheetah perspectives on the epizootiology of feline enteric coronavirus and the pathogenesis of feline infectious peritonitis nachweis feliner coronaviren mittels 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shift and genetic drift during feline coronavirus evolution the biology and pathogenesis of coronaviruses receptor for mhv is a member of carcinoembryotic antigen family of glycoproteins we cordially thank helga lussy, claudia pallan and dr. barbara bauder for their excellent technical assistance. key: cord-329398-8o39bwv7 authors: li, kunwei; fang, yijie; li, wenjuan; pan, cunxue; qin, peixin; zhong, yinghua; liu, xueguo; huang, mingqian; liao, yuting; li, shaolin title: ct image visual quantitative evaluation and clinical classification of coronavirus disease (covid-19) date: 2020-03-25 journal: eur radiol doi: 10.1007/s00330-020-06817-6 sha: doc_id: 329398 cord_uid: 8o39bwv7 objectives: to explore the relationship between the imaging manifestations and clinical classification of covid-19. methods: we conducted a retrospective single-center study on patients with covid-19 from jan. 18, 2020 to feb. 7, 2020 in zhuhai, china. patients were divided into 3 types based on chinese guideline: mild (patients with minimal symptoms and negative ct findings), common, and severe-critical (patients with positive ct findings and different extent of clinical manifestations). ct visual quantitative evaluation was based on summing up the acute lung inflammatory lesions involving each lobe, which was scored as 0 (0%), 1 (1–25%), 2 (26–50%), 3 (51–75%), or 4 (76–100%), respectively. the total severity score (tss) was reached by summing the five lobe scores. the consistency of two observers was evaluated. the tss was compared with the clinical classification. roc was used to test the diagnosis ability of tss for severe-critical type. results: this study included 78 patients, 38 males and 40 females. there were 24 mild (30.8%), 46 common (59.0%), and 8 severe-critical (10.2%) cases, respectively. the median tss of severe-critical-type group was significantly higher than common type (p < 0.001). the icc value of the two observers was 0.976 (95% ci 0.962–0.985). roc analysis showed the area under the curve (auc) of tss for diagnosing severe-critical type was 0.918. the tss cutoff of 7.5 had 82.6% sensitivity and 100% specificity. conclusions: the proportion of clinical mild-type patients with covid-19 was relatively high; ct was not suitable for independent screening tool. the ct visual quantitative analysis has high consistency and can reflect the clinical classification of covid-19. key points: • ct visual quantitative evaluation has high consistency (icc value of 0.976) among the observers. the median tss of severe-critical type group was significantly higher than common type (p < 0.001). • roc analysis showed the area under the curve (auc) of tss for diagnosing severe-critical type was 0.918 (95% ci 0.843–0.994). the tss cutoff of 7.5 had 82.6% sensitivity and 100% specificity. • the proportion of confirmed covid-19 patients with normal chest ct was relatively high (30.8%); ct was not a suitable screening modality since december 2019, a number of cases of pneumonia with fever, cough, and dyspnea as clinical manifestations have been found in wuhan, hubei province, china [1] . the analysis of the whole genome sequence of the respiratory samples suggests that it is a new type of betacoronavirus [2] , which resembled severe acute respiratory syndrome coronavirus (sars-cov) [3] . on february 11, 2020, the world health organization (who) officially named it coronavirus disease . who has recently declared the outbreak a public health emergency of international concern [4] . as of march 12, 2020, 124,922 laboratory-confirmed and clinical-confirmed cases have been documented globally (i.e., the usa, vietnam, germany) [4] [5] [6] [7] , 80,980 laboratory-confirmed and clinical-confirmed cases and 3173 deaths in china as of march 12, 2020 [8] . on jan. 15, 2020, the first confirmed family cluster was reported in zhuhai, china, where the parents presented with unexplained pneumonia after coming from wuhan to visit their daughter who was living in zhuhai, china; afterwards, the daughter also developed respiratory symptoms and infection with sars-cov-2 was confirmed. as of february 13, the journal radiology has published several articles on the imaging features of covid-19 [9] [10] [11] [12] , but all of them are descriptive analyses. in february 2020, the chinese society of radiology issued the radiologic diagnosis of pneumonia with covid-19. ct plays an important role in the screening and diagnosis of covid-19. the first edition of the experts [13] divided ct manifestations into three stages: early, progressive, and severe according to the extent and features of the pulmonary abnormalities. however, it did not clarify the relationship between the extent of inflammation and the clinical presentation of the patient. in this study, we used a simple convenient method to quantify the imaging findings. we performed a retrospective, single-center study of the sars-cov-2 laboratory-confirmed cases with which included 78 cases between jan. 18, 2020 and feb. 7, 2020 in zhuhai, china. a confirmed case was defined as positive by highthroughput sequencing or real-time reverse-transcriptase polymerase-chain-reaction (rrt-pcr) assay of nasal and pharyngeal swab specimens [1] . the rrt-pcr test kits used on the patients in this study was manufactured by shanghai zhijiang biotechnology co. this study was approved by the ethics committee of the fifth affiliated hospital of sun yatsen university and the requirement for informed consent was waived since the study had no risk and would not adversely affect the subjects' rights or welfare. patient selection for this study was consecutive, and no exclusion criteria were applied. all scans were performed with the patient in the supine position during end-inspiration without intravenous contrast on two ct scanners, uct 760 and umi 780 scanners (united imaging). the scanning range was from the apex to lung base. all images were obtained with a standard dose scanning protocol, reconstructed at 1.0 mm slice thickness, with 1 mm increment, 512 mm × 512 mm, and a sharp reconstruction kernel (b_vsharp_b). lung window setting was with a window level of − 600 hounsfield units (hu) and window width of 1500 hu. image analysis was performed using the institutional digital database system (neusoft v5.5.4.50720). all ct images were reviewed by two radiologists with 5 and 3 years of experience in imaging (y.f. and w.l.). imaging was reviewed independently and final decisions reached by consensus. for disagreement between the two primary radiologist interpretations, a third experienced thoracic radiologist with 17 years of experience (k.l.) adjudicated a final decision. no negative control cases were examined. for each of the 78 patients, the ct scan was evaluated for the following characteristics: (1) distribution: presence of peripheral or peribronchovascular; (2) density: presence of ground-glass opacities, mixed ground-glass opacities, or consolidation; (3) internal structures: presence of air bronchogram, interlobular septal thickening, cavitation; (4) number of lobes affected by ground-glass or consolidative opacities; (5) presence of fibrotic lesions; (6) presence of centrilobular nodules; (7) presence of a pleural effusion; (8) presence of thoracic lymphadenopathy (defined as lymph node size of ≥ 10 mm in short-axis dimension); and (9) presence of underlying lung disease such as tuberculosis, emphysema, or interstitial lung disease were noted. ground-glass opacification was defined as hazy increased lung attenuation with preservation of bronchial and vascular margins and consolidation was defined as opacification with obscuration of margins of vessels and airway walls [14] . two radiologists (y.f. and w.l.) reviewed all images independently blinded to the clinical information. percentage of involvement in each lobe was recorded as well as the overall lung "total severity score (tss)". each of the five lung lobes was assessed for percentage of the lobar involvement and classified as none (0%), minimal (1-25%), mild (26-50%), moderate (51-75%), or severe (76-100%), with corresponded score as 0, 1, 2, 3, or 4. the tss was reached by summing the five lobe scores (range from 0 to 20) [9] . the final score of each case was decided by a third experienced thoracic radiologist (k.l.). all cases were divided into four groups: minimal, common, severe, and critical according to whether there were clinical symptoms, severity of pneumonia, respiratory failure, shock, other organ failure, etc., based on the diagnosis and treatment plan of covid-19 issued by national health commission (7th ed.) (in chinese) [15] . (1) mild type: mild clinical symptoms without pneumonia in imaging; (2) common type: fever, respiratory tract and other symptoms with pneumonia in imaging; (3) severe type: respiratory distress, respiratory rate ≥ 30 times/min; in resting state, oxygen saturation ≤ 93%; pao2/fio2 ≤ 300mmhg; (4) critical type: respiratory failure requiring mechanical ventilation, shock and other organ failure requiring icu monitoring and treatment. statistical analysis was performed using ibm spss statistics for windows, version 25.0 (ibm corp.). continuous data conforming to normal distribution expressed by mean ± standard deviation; for those not conformed (median, p25, p75) were listed. intragroup correlation coefficient (icc) was used to test the consistency of tss scores of two observers, icc values < 0.4, 0.4~0.75, and > 0.75 represent poor, moderate, and good repeatability, respectively. the distribution balance of involved lobes and the number of involved lobes in different clinical types were compared by chi-squared test or fisher exact test when sample sizes were small and by analysis of variance tests. wilcoxon-rank test was used for comparison of tss among different clinical types, since tss did not conform to the normal distribution. roc was used to test the differential diagnosis ability of tss in common-type group and severe-critical-type group. seventy-eight patients were included in the study. the clinical subtype classification was as follows: 24 (30.8%) had minimal, 46 (59.0%) had common, 6 (7.7%) had severe, and 2 (2.6%) had critical disease. the demographic data for all patients are shown in table 1 . all patients were discharged after a mean hospitalized period of 20 ± 7 days (range 9-45 days). no patients died in this cohort. the consistency test results of ct visual quantitative analysis of two observers showed good repeatability with icc 0.976 (95% confidence interval 0.962-0.985). the distribution of pulmonary lobe involvement in different clinical types is shown in table 2 . all 5 lobes were involved in the severe-critical type while the lower lobes were usually involved in the common type (40/46, 87.0%). compared with the severe-critical type, the common type had a lower incidence of right upper lobe and middle lobe involvement (p = 0.016; p = 0.006, respectively), and also a lower incidence of right lower lobe, left lower lobe, and left upper lobe involvement; however, there was no significant difference table 3 . common type can involve one, two, three, and four lobes. however, due to less number of cases, there was no significant difference in the first three groups statistically. common type and severe-critical type can both involve 5 lobes, but severe-critical type had a higher incidence than common type (p = 0.001). for the common type, the involved lobe number of 5 was significantly higher than 1-4 (p = 0.015). the results of tss are shown in fig. 1 . score of mild type was 0, while common type was 1-11 (median 5, p25 2.75, p75 6.25) and severe-critical type was 8-18 (median 10, p25 9, p75 15.25). the score of severe-critical type was significantly higher than common type (p < 0.001). figures 2 and 3 were from common-type and severe-critical-type patients, respectively. roc analysis showed the area under the curve (auc) of tss for diagnosing severe-critical type was 0.918 (95%ci 0.843-0.994). the tss cutoff of 7.5 had 82.6% sensitivity and 100% specificity (fig. 4) . covid-19 is a new disease which is caused by betacoronavirus. the diameter of the virus particle is very small, about 60~140 nm; therefore, it is easy to reach the lung terminal structure, such as alveolar septum, alveolar wall, and interlobular septum, which causes extensive edema and lymphocyte infiltration in the lung interstitium; early alveolar exudation is not prominent, but the disease progresses rapidly [16] . in this study, the imaging features were consistent with the previous literature reports [9] [10] [11] [12] [13] [16] [17] [18] of viral pneumonia; most of the patients had ground-glass opacities and mixed ground-glass opacities; no patients demonstrated consolidation without ground-glass opacification. subpleural distribution was common. it also occurred around the bronchovascular bundle. air bronchograms and interlobular septal thickening were often present. no patients had in a recent study done by michael et al, they introduced a method to score the severity of inflammation on ct images based on summing up degree of acute lung inflammation lesions involvement of each lobe (including fig. 2 a 32-year-old female had fever, cough, and sputum with a body temperature of 38.8°c for 5 days and admitted to the hospital on jan. 27, 2020. the leukocytes and lymphocytes were decreased. she was living in zhuhai and traveled to wuhan on jan. 21 and stayed there for 2 days. she was healthy and nonsmoker. chest ct (images a-c) on the 1st day after admission demonstrated bilateral peripheral ground-glass opacities with linear opacities. tss was 5. the clinical type was common type. followup ct (images d, e) on the 20th day after onset showed peripheral shrinking consolidation with ground-grass opacities in both lungs fig. 1 the total severity score (tss) of different clinical classifications. there were 24 cases of light type (31%), 46 cases of common type (60%), and 8 cases of severe-critical type (9%). the median tss was 10 in severecritical-type group (range 8-18), which was significantly higher than that of common type (median 5, ranged [1] [2] [3] [4] [5] [6] [7] [8] [9] [10] [11] ground-glass opacity or consolidation or other fuzzy interstitial opacities) [9] . we used the same method to quantify pulmonary inflammation and correlate to the clinical classifications. there was significant difference in scores between common type and severe-critical type (p < 0.001). however, there was also a score overlap between the two groups, which showed that 8 cases in the common type had a higher score, and 5 cases in the severe-critical type had a lower score. among 8 cases of common type, 7 cases had fibrotic lesions which indicated that the lesions began to be repaired, and all of the 8 patients were less than 70 years old (range 36-65, average 52.5 years), none of them had pulmonary complications. the specific situation of 5 patients in a severe-critical type which had a lower score was as follows: 3 of the 5 patients were over 70 years old; among them, 1 patient was a female smoker with diabetes, aged 80 years old, with moderate emphysema and a small amount of pleural effusion; 1 patient was a 70-year-old female, with emphysema and a small amount of pleural effusion as well; the other one was 75-year-old female with high blood pressure; the forth case was a 44-year-old male without any underlying disease; however, ct images showed only progressive lesions such as ground-glass opacification and consolidation without any fibrotic lesions (fig. 5 ). the last case was a 58year-old female without any underlying disease; further analysis [19] . however, the most recent report from guangzhou had similar findings, which showed 23.6% fig. 5 a 44-year-old male was admitted to the hospital 1 day after fever and cough with a body temperature of 39°c. the leukocytes were normal and lymphocytes were decreased. he was living in zhuhai and traveled to macao 12 days before the onset of the disease and stayed in macao for 1 week. he was healthy and nonsmoker. chest ct (images a-c) on the 4th day after admission demonstrated bilateral peripheral ground-glass opacities without consolidation. tss was 9. the clinical type was severe-critical type. follow-up ct (images d, e) on the 22nd day after onset showed bilateral fibrotic changes with traction bronchiectasis and ground-grass opacities confirmed patients without abnormalities on chest ct [20] . to further explore our data, we found several characteristics. nine cases had a short time interval from onset to the latest ct examination with a range of 0-7 days, which indicated that the chest ct could be normal at the early phase. another 9 cases had a longer time interval from onset to the latest ct scan with a range of 8-19 days. the negative findings may not relate to the shorter onset time. it remains to be further explored whether the ct negativity may relate to the degree of infection and autoimmunity. finally, the last 6 patients had no symptoms. these patients were negative in both clinical and imaging, suggesting that some cases were potential sources of infection, which should be paid more attention to. in this study, the number of cases between groups was significantly different because too few severe-critical patients were included in this study, which decreased the reliability of statistical results. only image analysis was carried out without combining clinical information in this study; however, advanced age, underlying diseases, and pleural effusions may lead to a lower tss but severe situation. in our next study, we will include more cases, and make a comprehensive evaluation combining the clinical characteristics and laboratory examination information. the proportion of clinical mild-type patients with covid-19 was relatively high, screening for covid-19 with chest ct alone can lead to misdiagnosis in some patients, which would lead to a potential infection risk, so ct was not suitable as an independent screening tool. visual quantitative analysis based on ct images has high consistency and high diagnostic ability, which can reflect clinical classification; it is expected to accurately assess the clinical severity of covid-19 and guide the clinical treatment by combining with the clinical information. clinical features of patients with 2019 novel coronavirus in wuhan genomic characterization and epidemiology of 2019 novel coronavirus: implications of virus origins and receptor binding a novel coronavirus from patients with pneumonia in china importation and human-to-human transmission of a novel coronavirus in vietnam transmission of 2019-ncov infection from an asymptomatic contact in germany first case of 2019 novel coronavirus in the united states national health commission of the people's republic of china ct imaging features of 2019 novel coronavirus (2019-ncov) ct imaging of the 2019 novel coronavirus (2019-ncov) pneumonia. radiology ct manifestations of two cases of 2019 novel coronavirus (2019-ncov) pneumonia evolution of ct manifestations in a patient recovered from 2019 novel coronavirus (2019-ncov) pneumonia in wuhan imaging diagnosis of 2019-ncov pneumonia: expert recommendation of chinese society of radiology, the first edition fleischner society: glossary of terms for thoracic imaging notice on the issuance of a program for the diagnosis and treatment of novel coronavirus (2019-ncov) infected pneumonia (trial revised fifth edition viral pneumonias in adults: radiologic and pathologic findings radiographic and ct features of viral pneumonia severe acute respiratory syndrome: temporal lung changes at thin-section ct in 30 patients epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in wuhan, china: a descriptive study clinical characteristics of coronavirus disease 2019 in china publisher's note springer nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations acknowledgments the authors thank claudia henschke, david yankelevitz, and rowena yip from mount sinai medical center for polishing the manuscript. key: cord-316943-ef3i96bo authors: sciberras, justine; camilleri, lara maria; cuschieri, sarah title: the burden of type 2 diabetes pre-and during the covid-19 pandemic – a review date: 2020-10-19 journal: j diabetes metab disord doi: 10.1007/s40200-020-00656-4 sha: doc_id: 316943 cord_uid: ef3i96bo introduction: diabetes mellitus is a chronic disease and a global epidemic. it is a known fact that co-morbidities, including diabetes mellitus, pose a higher risk of infection by covid-19. additionally, the outcomes following infection are far worse than in people without such co-morbities. factors contributing to the development of type 2 diabetes mellitus (t2dm) have long been established, yet this disease still bestows a substantial global burden. the aim was to provide a comprehensive review of the burden of diabetes pre-covid-19 and the additional impact sustained by the diabetes population and healthcare systems during the covid-19 pandemic, while providing recommendations of how this burden can be subsided. methodology: literature searches were carried out on ‘google scholar’ and ‘pubmed’ to identify relevant articles for the scope of this review. information was also collected from reliable sources such as the world health organisation and the international diabetes federation. results: t2dm presented with economic, social and health burdens prior to covid-19 with an significant ‘disability adjusted life years’ impact. whilst people with diabetes are more susceptible to covid-19, enforcing lockdown regulations set by the public health department to reduce risk of infection brought about its own challenges to t2dm management. through recommendations and adapting to new methods of management such as telehealth, these challenges and potential consequences of mismanagement are kept to a minimum whilst safeguarding the healthcare system. conclusion: by understanding the challenges and burdens faced by this population both evident pre-covid and during, targeted healthcare can be provided during the covid-19 pandemic. furthermore, implementation of targeted action plans and recommendations ensures the care provided is done in a safe and effective environment. electronic supplementary material: the online version of this article (10.1007/s40200-020-00656-4) contains supplementary material, which is available to authorized users. diabetes mellitus is a chronic disease resulting from the reduction in the body's response to insulin production by the pancreas either due to an increase in insulin resistance or due to decreased insulin production [1] . in the past three decades, incidence of diabetes has quadrupled worldwide [2] . diabetes has also classified as the 7th leading cause of death globally in 2016 [3] . according to the recent data published by the international diabetes federation, 463 million adults (20-79 years) suffered from diabetes in 2019. if not adequately controlled, the global diabetes prevalence is expected to increase by approximately 51% in 2045 [4] . the contributing factors for the development of type 2 diabetes (t2dm) can be broadly divided into genetic and environmental factors. electronic supplementary material the online version of this article (https://doi.org/10.1007/s40200-020-00656-4) contains supplementary material, which is available to authorized users. some specific risk factors include, obesity, smoking, leading a sedentary lifestyle, age and also the presence of metabolic syndrome [5, 6] . the pathophysiology and the underlying risk factors have long been established, yet the incidence of diabetes is still on a progressive incline [7] the 2019 coronavirus sars-cov2 pandemic has further increased the burden on the diabetes population, those at risk of dyglcyaemic changes as well as the healthcare services [8] . the aim of this article was to provide a comprehensive review of the burden of diabetes pre-covid-19 and the additional impact sustained by the diabetes population and healthcare systems during the covid-19 pandemic, while providing recommendations of how this burden can be subsided. a literature search was carried out in july 2020 through 'pubmed' and 'google scholar' using the keywords 't2dm', 'covid-19' and 'public health'. articles were then filtered using several inclusion criteria including; english language, human studies and literature type. the latter mainly included systematic reviews, meta-analysis and literature reviews. the authors then filtered the resulting articles by title and abstract and the remaining 65 articles which fitted the aim of this review were thus considered. additionally, information was also collected from reliable reports such as those of the world health organization (who) and international diabetes federation (idf). having an understanding of the impact of t2dm at an individual, community and population level is paramount for public health authorities and policymakers alike. the burden of a disease can be quantified in terms of the quality of life, morbidity, premature mortality, economic and healthcare impact [9] . public health policies and plans for provision of services all depend on the general population's state of health and comorbid diseases which change over time. developed in the 1990s, the dalys metric is used to gauge the total burden of a disease by considering the number of years lost to a disease, premature mortality, or disability. it is also used to compare health and life expectancy globally. such a calculation gives policy makers a better understanding of the overall duration of life in comparison to duration spent in poor or good health [9] . a global observation of the incline in dalys across 10 years comparing individuals at different age categories (15-49 years, 50-69 years vs 70+ years) adapted from the global burden of disease website can be seen in figs. 1, 2 and 3 respectively. [10] . as seen in the graphs, the higher incidence of t2dm at a younger age range is contributing to the increase in dalys. this will place a strain on healthcare costs and economic healthcare services as well as [10] decreased work productivity and increased likelihood of early retirement or mortality. this will ultimately be a burden on the country's economy. the universal rise in life expectancy has left policy makers questioning whether individuals maintain a good quality of life during these additional years, as reported by the global burden of disease (gbd) study and illustrated in figs. 1, 2 and 3. such evaluations are extremely relevant to decisions involving extension of retirement ages and health care stipulations. namely to increase efforts for risk prevention of non-communicable diseases such as t2dm from early stage of the disease. great inequalities between the burden of a disease and healthy life expectancy are present globally irrespective of a country's quintile on the socio-demographic index or between sexes [11] . this implies that quantity is more prevalent than quality of life worldwide. the disabling outcomes of a disease such as t2dm has considerable implications for the health care system plans and disbursements [12] . economic status and healthcare t2dm presents with economic, social and health burdens not only for the individual but also for families and careers as well as the healthcare system. additionally, employment is another social factor which is often impacted, leading to further strain on the country's economy [13] . a country's ability to prevent t2dm lies in the presence of an identification and targeting strategy aimed at high risk individuals. this is dependent on the infrastructure and human resources available with a consequential effect on the management plan of the diagnosed individuals [13] . furthermore, statistical data regarding epidemiology would be essential for health care providers in the identification of the risk factors contributing to t2dm at a country level. this would aid in surveilling, diagnosing, monitoring as well as treating t2dm. in previous studies diabetes was reported to be more common with individuals with high socio-economic status [14] [15] [16] . in contrast, a recent study reported that a higher t2dm prevalence was associated with individuals having a lower socioeconomic status due to limited access to health care and [17] . moreover, this factor was also observed in low and middle income asian countries experiencing fast economic advancement [16] . coronaviruses are enveloped viruses known to cause respiratory infections in humans. whilst most of these viruses are harmless and cause mild symptoms, a novel virus known as sars (severe acute respiratory syndrome) -cov 2 as well as covid-19 emerged in december of 2019, which proved to be more harmful than the previously known coronaviruses [18] . it is now a known fact that co-morbidities such as obesity, diabetes mellitus (dm), hypertension as well as advanced age all increase the chances of being infected with covid-19 [19] . additionally, reports from the centres for disease control and prevention stated that patients with diabetes and metabolic syndrome might be 10 times more likely to die due to covid-19 [20] . there are several possible mechanisms which can make diabetic patients more susceptible to covid-19. some of these mechanisms include; impaired macrophage activity; impaired neutrophil recruitment and cytokine storm. however, the one mechanism which seems to be considered most is the increased viral load due to the virus entering the cells efficiently. in fact, the receptor which this virus uses is the angiotensin-converting enzyme 2(ace2) receptor which can be found expressed by various tissues including lungs, kidneys, pancreas and the heart [18, 21] . firstly, the sars cov-2 spike protein bind to the ace2 cell surface where the s protein is then primed by the cellular proteases such as tmprss1 and furin. priming involves cleaving the s protein at the s1/s2 domains, allowing the virus to fuse to the cell surface [18] . virions are then taken up into endosomes where the sars cov 2 is cleaved and possibly activated by cathepsin l [22] . inside the cell sars cov 2 replicates itself whilst ace catalyzes the conversion of angiotensin i to angiotensin ii and ace 2 converts angiotensin ii to ang 1-7 [23] . since ace 2 receptors are also found in the pancreas, the entry of coronavirus in the pancreatic cells may result in acute beta cell dysfunction [21] . finally this may lead to a state of acute hyperglycaemia which if left uncontrolled predisposes the diabetic individual to a greater risk of infection and also a higher chance of mortality [24, 25] . certain medications prescribed to diabetic patients such as glp-1 agonists, angiotensin receptor blockers (arb's) and angiotensin converting enzyme inhibitors (acei's) are thought to upregulate ace2 expression [26] . acei initially inhibits the angiotensin converting enzyme (ace) leading to decreased angiotensin i levels. this possibly causes a negative feedback loop that ultimately upregulates more ace2 receptor which can now interact with the decreased angiotensin i substrate available [27, 28] . additionally, evidence of a 5-fold increase in ace2 levels with lisinopril and a 3-fold increase in ace2 levels with losartan was also published [26, 29] . therefore, due to the ace 2 receptor being expressed in various tissues as well as due to the upregulation of ace2 receptor there is thus an increase in potential binding sites for sars-cov-2. this mechanism takes place in patients with diabetes and/or hypertension since they usually take acei or arb's. hence, infection by covid-19 may be more severe in these patients [30, 31] . whilst the above mentioned mechanism seems to confirm that arb's and acei's upregulate ace2 expression, other studies which contradict this have been published. these studies claim that the administration of these medicines is actually beneficial to patients infected with covid19 [32] [33] [34] [35] . lack of exercise one of the many mitigation legislations put forward by governments along with public health authorities to contain the spread of covid-19 was to institute social-distancing restrictions along with the closure of gyms and parks [36] . furthermore, the population was advised to limit going out of their homes unnecessarily [25, 37] . exercise has long been established to be an important requisite as part of the diabetes management and prevention plans [38] . several studies carried out over the years found that lifestyle interventions including 150 min/week of physical activity and diet-induced weight loss of 5-7% reduced the risk of progression from impaired glucose tolerance (igt) to type 2 diabetes by 58% [39] [40] [41] . a systematic review and meta-analysis carried out on structured exercise interventions also concluded that structured exercise programs had a statistically and clinically significant beneficial effect on glycaemic control [42, 43] . consequently, the world health organization (who) released a guideline called 'stay physically active during quarantine' which contains possible ways to stay active during covid-19. the use of online classes and videos were encouraged as were frequent walking breaks around the house [44] . the mandated lockdowns resulted in the limited access to fresh fruit and vegetables. individuals including those with diabetes might have resorted to the consumption of long shelf-life canned or packaged foods that are typically high in calories and/or fats, with a potential increase in the consumption of carbohydrates [45] [46] [47] . such food consumption increases the risk of weight gain and impose a higher cardiovascular, thrombotic and respiratory complications [48, 49] . the concurrent presence of obesity within the diabetes population poses additional detrimental effects on the functioning capabilities of the lungs lead to a decrease forced expiratory volume (fev) and forced vital capacity (fvc) [50] . additionally, it has been hypothesized that pulmonary lipofibroblasts together with normal adipocytes play a role in the pathogenic response of covid-19. this is believed to be brought about by the increased expression of the ace-2 receptors which turns the adipocytes into reservoirs for the virus. moreover, the adipocytes aid in the transdifferentiation of lipofibroblasts into myofibroblasts leading to pulmonary fibrosis. consequently, the presence of fibrosis leads to severe outcomes of the covid-19 infection among the diabetesobese population [51] . a recurrent issue during lockdown appeared to be an increased 'mental stress' and changes in sleeping habits [52] . anxiety mainly stemmed from contracting the virus, being restricted to the place of residence for a long period of time and also not being able to meet with loved ones [53] . the increased levels of anxiety were reported by more than 80% of the participants from north india who stated that they were worried about covid-19, out of which 12.5% reported difficulties in sleeping [54] . another study carried out in china reported that 53.8% of participants sustained a moderate to severe impact on their mental health due to covid-19 pandemic [55] . fig. 1 in the supplement material is a guideline released by the national diabetes service scheme (australia) intended in helping with management of worries and anxiety related to covid-19 and diabetes [56] . similarly, the european country of malta also released a set of recommendations to help the local diabetic population in managing their condition as well as to reduce anxiety related to covid-19 [57] the national health service (nhs) also published 'guidance for: supporting people with diabetes during the covid-19 pandemic' which compiles informative websites that the diabetic population might need to access during these difficult times [58] .apart from these guidelines, a number of countries including the european country of malta, set up designated helpline to provide aid to all those experiencing mental health issues including the diabetes population [36, [56] [57] [58] . whilst covid-19 and the subsequent stress can be a source of sleep disturbance, one has to also take into account diet; lifestyle and diseases [55] . in fact, shorter sleep duration and unstable sleeping patterns have been linked to obesity and cardiovascular problems [59, 60] . an association was also found between sleep disorders and patients with t2dm, where increased rates of insomnia, excessive sleeping during the day and a more frequent use of sleep medications were reported [61] . these changes in sleeping patterns may be due to the t2dm itself as well as due to complications which come with it such as polyuria and peripheral nephropathy [62] . lockdown restrictions challenged individuals including those with diabetes with inadequate vitamin d levels due to low sunlight exposure during this pandemic [25] . vitamin d deficiency can lead to an increased mortality and morbidity due to covid-19 [63] vitamin d supplementation is not only thought to decrease the risk of infection but it is also being suggested as a cure for infection patients [64] vitamin d has numerous mechanisms through which it decreases the risks of microbial infections and death. these mechanisms can be grouped into three main categories; physical barrier, cellular natural immunity and adaptive immunity [65] . it was observed that infected elderly with diabetes had an elevated fasting blood glucose as opposed to their hba1c which remained stable [66] . however, during the acute phase of the covid-19 infection it is essential that strict glucose control is maintained to prevent the occurrence of complications [66, 67] . a number of healthcare recommendations and guidelines have been issued during these unprecedent times by different stakeholders including the institute for healthcare excellence on managing the diabetic population pre-covid-19 [68] . examples of these recommendations can be found as part of the supplement material (supplement tables 1, 2 change in healthcare services due to covid-19 individuals with diabetes are not always able to self-cafe and modify drug doses, especially those in marginalised and disadvantaged populations as well as elderly deprived of social support. these populations are dependent on health professionals [69] . in such cases, where no designated point of reference is available, managing their own condition can place further psychological stress on the patients, which might have been the case during the covid-19 lockdown periods. complications arising from poorly managed blood glucose such as diabetic ketoacidosis raises the risk for morbidity and mortality. this will not only put a strain on an individual and the family unit but also on the health care system [70] . most outpatient services were temporary halted during the pandemic whilst those that continued their services were challenged due to staff reduction as these were deployment to frontline duties or illnesses [36] . hence, ensuring that delivery of care does not cease during this pandemic was a great feat. virtual care was a tool employed by many countries in an attempt to continue provision of service whilst also preventing nosocomial exposure to covid-19. telehealth was consequently beneficial for countries, such as usa,uk and india, when providing a service in distant locations with shortage of staff [71] [72] [73] . using such technologies enabled imparted education to individuals with diabetes about changes in insulin dosing as well as general self-care. the ongoing communication empower individuals and allow them to independently manage their condition. studies carried out prior to the pandemic indicated that virtual communication can successfully lower hb a1c [74] . practitioners through telemedicine can further emphasize the importance of controlling glucose levels as well as relate the potentially improved outcomes of covid-19 if encountered [75] . however, such a tool is not always viable due to limited accessibility, acceptance and knowledge on the use of technology. in fact, some individuals still requested to be seen in the traditional face-to-face setting [76] . moreover, practitioners in developing countries should always consider financial implications of therapies on an individual. simple treatment regimens and low-cost therapy should ideally be prescribed especially to underprivileged populations [75] . the guidelines observed in supplement fig. 3 have formulated by the british national health system (nhs) to assess the risk of covid-19 susceptibility before setting up an outpatient assessment or follow up [77] . healthcare professionals can potentially encounter clients who are awaiting result or have been confirmed as covid-19 positive. hence it is essential to encourage staff to wear ppes whilst also adhering to recommended sanitisation procedures; especially in aerosol generating practices. such procedures should also be enforced in hospital routine activities such as waste, food, utensil and laundry handling. bornstein et al., compiled a list of guidelines for healthcare workers to follow when dealing with diabetic patients in different scenarios. these guidelines can be found in fig. 2 in the supplementary material [78] . easy and practical recommendations that were compiled by wang et al., (2020) that can be relayed to patients are listed in fig. 3 which can be accessed in the supplement material [77] . the extensive impacts on health revealed by this pandemic has demonstrated the vulnerability of individuals with noncommunicable diseases (ncds) [79] . a study carried out in italy showed that 96% of patients that died in hospitals had previous comorbidities, with t2dm being second highest amongst hypertension, malignant tumours, cardiac and respiratory diseases [80] . the link between ncd and covid-19 mortality has also been made in usa, china and spain [79, 81, 82] . measures undertaken for ncds included quarantine and physical distancing. this could potentially result in poor management of the condition by both the patient -through behavioural risk factors -and the healthcare professional [83] . rescheduling of routine medical tests and appointments can further hinder management as well as limited access to primary healthcare centres, pharmacies and transport. all these factors will make it tougher to ensure continuity of care. research from other pandemics indicates that exacerbation of ncds occurs without proper healthcare management [84] . this is due to stress that is brought about by changes in routine, uncertain economic situations and new regulations which will ultimately raise rates of disability, morbidity and mortality in patients with ncds [79] . the importance of t2dm management to avoid serious repercussions on health and overall economy is not a new concept. hence it is important to equip patients with the right knowledge about the current pandemic and its possible effects on their overall health. it is crucial, now more than ever, to ensure that patients have direct contact with a healthcare practitioner to mitigate any queries or concerns that they may have. this will ultimately empower individuals to adhere to recommendations whilst also avoiding extra stressors which may exacerbate hyperglycaemic effects such as kidney failure, amputation, nerve damage and heart disease [85] . t2dm has been a global burden for decades; however, additional burden has been imposed with the onset of covid-19 pandemic. consequently, at a global level, healthcare systems as well as the diabetes population were impacted during this pandemic. mitigation restrictions that were aimed to curb the spread may have imposed a higher burden on the diabetes population. having an understanding of the 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response characteristics of sars-cov-2 patients dying in italy presenting characteristics, comorbidities, and outcomes among 5700 patients hospitalized with covid-19 in the the epidemiological characteristics of an outbreak of 2019 novel coronavirus diseases (covid-19) in china. zhonghua liu xing bing xue za zhi= zhonghua liuxingbingxue zazhi coronavirus: should i worry about my lockdown eating? care of non-communicable diseases in emergencies difficulties to treatment adherence according to the perception of people living with type 2 diabetes publisher's note springer nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations key: cord-260793-bb4h255w authors: brann, david h.; tsukahara, tatsuya; weinreb, caleb; lipovsek, marcela; van den berge, koen; gong, boying; chance, rebecca; macaulay, iain c.; chou, hsin-jung; fletcher, russell; das, diya; street, kelly; de bezieux, hector roux; choi, yoon-gi; risso, davide; dudoit, sandrine; purdom, elizabeth; mill, jonathan s.; hachem, ralph abi; matsunami, hiroaki; logan, darren w.; goldstein, bradley j.; grubb, matthew s.; ngai, john; datta, sandeep robert title: non-neuronal expression of sars-cov-2 entry genes in the olfactory system suggests mechanisms underlying covid-19-associated anosmia date: 2020-05-18 journal: biorxiv doi: 10.1101/2020.03.25.009084 sha: doc_id: 260793 cord_uid: bb4h255w altered olfactory function is a common symptom of covid-19, but its etiology is unknown. a key question is whether sars-cov-2 (cov-2) – the causal agent in covid-19 – affects olfaction directly by infecting olfactory sensory neurons or their targets in the olfactory bulb, or indirectly, through perturbation of supporting cells. here we identify cell types in the olfactory epithelium and olfactory bulb that express sars-cov-2 cell entry molecules. bulk sequencing revealed that mouse, non-human primate and human olfactory mucosa expresses two key genes involved in cov-2 entry, ace2 and tmprss2. however, single cell sequencing and immunostaining demonstrated ace2 expression in support cells, stem cells, and perivascular cells; in contrast, neurons in both the olfactory epithelium and bulb did not express ace2 message or protein. these findings suggest that cov-2 infection of non-neuronal cell types leads to anosmia and related disturbances in odor perception in covid-19 patients. sars-cov-2 (cov-2) is a pandemic coronavirus that causes the covid-19 syndrome, which can include upper respiratory infection (uri) symptoms, severe respiratory distress, acute cardiac injury and death (1-4). cov-2 is closely related to other beta-coronaviruses, including the causal agents in pandemic sars and mers (sars-cov and mers-cov, respectively) and endemic viruses typically associated with mild uri syndromes (hcov-oc43 and hcov-229e) (5) (6) (7) . clinical reports suggest that infection with cov-2 is associated with high rates of disturbances in smell and taste perception, including anosmia (8) (9) (10) (11) (12) . while many viruses (including coronaviruses) induce transient changes in odor perception due to inflammatory responses, in at least some cases covid-related anosmia has been reported to occur in the absence of significant nasal inflammation or coryzal symptoms (11, (13) (14) (15) . this observation suggests that cov-2 might directly target odor processing mechanisms, although the specific means through which cov-2 alters odor perception remains unknown. cov-2 -like sars-cov -infects cells through interactions between its spike (s) protein and the ace2 protein on target cells. this interaction requires cleavage of the s protein, likely by the cell surface protease tmprss2, although other proteases (such as cathepsin b and l, ctsb/ctsl) may also be involved (4) (5) (6) (16) (17) (18) (19) (20) . other coronaviruses use different cell surface receptors and proteases to facilitate cellular entry, including dpp4, furin and hspa5 for mers-cov, anpep for hcov-229e, tmprss11d for sars-cov (in addition to ace2 and tmprss2), and st6gal1 and st3gal4 for hcov-oc43 and hcov-hku1 (6, (21) (22) (23) . we hypothesized that identifying the specific olfactory cell types susceptible to direct cov-2 infection (due to e.g., ace2 and tmprss2 expression) would provide insight into possible mechanisms through which covid-19 causes altered smell perception. the nasal epithelium is divided into a respiratory epithelium (re) and olfactory epithelium (oe), whose functions and cell types differ. the nasal re is continuous with the epithelium that lines much of the respiratory tract and is thought to humidify air as it enters the nose; main cell types include basal cells, ciliated cells, secretory cells (including goblet cells), and brush/microvillar cells (24, 25) (figure 1 ). the oe, in contrast, is responsible for odor detection, as it houses mature olfactory sensory neurons (osns) that interact with odors via receptors localized on their dendritic cilia. osns are supported by sustentacular cells, which act to structurally support sensory neurons, phagocytose and/or detoxify potentially damaging agents, and maintain local salt and water balance (26) (27) (28) ; microvillar cells and mucus-secreting bowman's gland cells also play important roles in maintaining oe homeostasis and function (24, 29) (figure 1 ). in addition, the oe contains globose basal cells (gbcs), which are primarily responsible for regenerating osns during normal epithelial turnover, and horizontal basal cells (hbcs), which act as reserve stem cells activated upon tissue damage (30) (31) (32) . osns elaborate axons that puncture the cribriform plate at the base of the skull and terminate in the olfactory bulb, whose local circuits process olfactory information before sending it to higher brain centers (figure 1 ). it has recently been demonstrated through single cell rna sequencing analysis (referred to herein as scseq) that cells from the human upper airway -including nasal re goblet, basal and ciliated cells -express high levels of ace2 and tmprss2, suggesting that these re cell types may serve as a viral reservoir during cov-2 infection (33) . however, analyzed samples in that dataset did not include any osns or sustentacular cells, indicating that tissue sampling in these experiments did not include the oe (34, 35) . here we query both new and previously published bulk rna-seq and scseq datasets from the olfactory system for expression of ace2, tmrpss2 and other genes implicated in coronavirus entry. we find that non-neuronal cells in the oe and olfactory bulb, including support, stem and perivascular cells, express cov-2 entryassociated transcripts and their associated proteins, suggesting that infection of these non-neuronal cell types contributes to anosmia in covid-19 patients. schematic of a sagittal view of the human nasal cavity, in which respiratory and olfactory epithelium are colored (left). for each type of epithelium, a schematic of the anatomy and known major cell types are shown (right). in the olfactory bulb in the brain (tan) the axons from olfactory sensory neurons coalesce into glomeruli, and mitral/tufted cells innervate these glomeruli and send olfactory projections to downstream olfactory areas. glomeruli are also innervated by juxtaglomerular cells, a subset of which are dopaminergic. to determine whether genes relevant to cov-2 entry are expressed in osns or other cell types in the human oe, we queried previously published bulk rna-seq data derived from the whole olfactory mucosa (wom) of macaque, marmoset and human (36) , and found expression of almost all cov-entry-related genes in all wom samples ( figure s1a ). to identify the specific cell types in human oe that express ace2, we quantified gene expression in scseq derived from four human nasal biopsy samples recently reported by durante et al (37) . neither ace2 nor tmprss2 were detected in mature osns, whereas these genes were detected in both sustentacular cells and hbcs (figures 2a-e) . in contrast, genes relevant to cell entry of other covs were expressed in osns, as well as in other oe cell types. we confirmed the expression of ace2 proteins via immunostaining of human olfactory epithelium biopsy tissue, which revealed expression in sustentacular and basal cells, and an absence of ace2 protein in osns ( figures 2f and s1e ). together, these results demonstrate that sustentacular and olfactory stem cells, but not mature osns, are potentially direct targets of cov-2 in the human oe. given that the nasopharynx is a major site of infection for cov-2 (10), we compared the frequency of ace2 and tmprss2 expression among the cell types in the human re and oe (37) . sustentacular cells exhibited the highest frequency of ace2 expression in the oe (2.90% of cells) although this frequency was slightly lower than that observed in respiratory ciliated and secretory cells (3.65% and 3.96%, respectively). while all hbc subtypes expressed ace2, the frequency of expression of ace2 was lower in olfactory hbcs (0.84% of cells) compared to respiratory hbcs (1.78% of cells) ( figure 2b ). in addition, all other re cell subtypes showed higher frequencies of ace2 and tmprss2 expression than was apparent in oe cells. these results demonstrate the presence of key cov-2 entry-related genes in specific cell types in the oe, but at lower levels of expression than in re isolated from the nasal mucosa. we wondered whether these lower levels of expression might nonetheless be sufficient for infection of cov-2. it was recently reported that nasal re has higher expression of cov-2 entry genes than re of the trachea or lungs (38) , and we therefore asked where the oe fell within this previously established spectrum of expression. to address this question, we developed a two step alignment procedure in which we first sought to identify cell types that were common across the oe and re, and then leveraged gene expression patterns in these common cell types to normalize gene expression levels across all cell types in the oe and re ( figure s2 ). this approach revealed a correspondences between goblet cells in the re and bowman's gland cells in the oe (96% mapping probability, see methods), and between pulmonary ionocytes in the re and a subset of microvillar cells in the oe (99% mapping probability, see methods); after alignment, human oe sustentacular cells were found to express ace2 and tmprss2 at levels similar to those observed in the remainder of the non-nasal respiratory tract ( figure 2g) (38) . these results are consistent with the possibility that specific cell types in the human olfactory epithelium express ace2 at a level that is permissive for direct infection. (37) . each dot represents an individual cell, colored by cell type (hbc = horizontal basal cell, osn = olfactory sensory neuron, sus = sustentacular cell, mv: microvillar cell, resp.: respiratory, oec = olfactory ensheathing cell, smc=smooth muscle cell). (b) percent of cells expressing ace2 and tmprss2. ace2 was not detected in any osns, but was observed in sus cells and hbcs, among other olfactory and respiratory epithelial cell types. olfactory and respiratory cell types are shown separately. ace2 and tmprss2 were also co-expressed above chance levels (odds ratio 7.088, p-value 3.74e-57, fisher's exact test). (c) umap representations of 865 detected immature (gng8) and mature (gng13) osns. neither ace2 nor tmprss2 are detected in either population of osns. the color represents the normalized expression level for each gene (number of umis for a given gene divided by the total number of umis for each cell). (d) umap representations of all cells, depicting the normalized expression of cov-2 related genes ace2 and tmprss2, as well as several cell type markers. ace2 and tmprss2 are expressed in respiratory and olfactory cell types, but not in osns. ace2 and tmprss2 are detected in hbc (krt5) and sustentacular (cyp2a13) cells, as well as other respiratory epithelial cell types, including respiratory ciliated (foxj1) cells. (e) various cov related genes including ace2 and tmprss2, are expressed in respiratory and olfactory cell types, but not in osns. gene expression for ace2 and tmprss2 as well as marker genes for olfactory and respiratory epithelial cell types are shown normalized by their maximum expression across cell types. mhv, mouse hepatitis virus. (f) ace2 immunostaining of human olfactory mucosal biopsy samples. ace2 protein (green) is detected in sustentacular cells and krt5-positive basal cells (red; white arrowhead). nuclei were stained with dapi (blue). bar = 25 µm. the ace2 and krt5 channels from the box on the left are shown individually on the right (g) gene expression across cell types and tissues in durante figure s4 ). the tissues correspond to progressive positions along the airway from nasal to distal lung. ace2 expression in olfactory hbc and sustentacular cells is comparable to that observed in other cell types in the respiratory tract. to further explore the distribution of cov-2 cell entry genes in the olfactory system we turned to the mouse, which enables interrogative experiments not possible in humans. to evaluate whether that expression patterns observed in the mouse correspond to those observed in the human oe, we examined published datasets in which rna-seq was independently performed on mouse wom and on purified populations of mature osns (39) (40) (41) . the cov-2 receptor ace2 and the protease tmprss2 were expressed in wom, as were the cathepsins ctsb and ctsl (figures 3a and s3a) (39) . however, expression of these genes (with the exception of ctsb) was much lower and ace2 expression was nearly absent in purified osn samples (figures 3a and s3a, see legend for counts). genes used for cell entry by other covs (except st3gal4) were also expressed in wom, and de-enriched in purified osns. the deenrichment of ace2 and tmprss2 in osns relative to wom was also observed in two other mouse rna-seq datasets (40, 41) ( figure s3b ). these data demonstrate that, as in humans, ace2 and other cov-2 entry-related genes are expressed in the mouse olfactory epithelium. the presence of ace2 and tmprss2 transcripts in mouse wom and their (near total) absence in purified osns suggest that the molecular components that enable cov-2 entry into cells are expressed in non-neuronal cell types in the mouse nasal epithelium. to identify the specific cell types that express ace2 and tmprss2, we performed scseq (via drop-seq, see methods) on mouse wom ( figure 3b ). these results were consistent with observations made in the human epithelium: ace2 and tmprss2 were expressed in a fraction of sustentacular and bowman's gland cells, and a very small fraction of stem cells, but not in osns (zero of 17,666 identified mature osns, figures 3c and s3c-d) . of note, only dorsally-located sustentacular cells, which express the markers sult1c1 and acsm4, were positive for ace2 ( figures 3d and s3d-e) . indeed, reanalysis of the ace2+ subset of human sustentacular cells revealed that all positive cells expressed genetic markers associated with the dorsal epithelium ( figure s1d ). an independent mouse scseq data set (obtained using the 10x chromium platform, see methods) revealed that olfactory sensory neurons did not express ace2 (2 of 28769 mature osns were positive for ace2), while expression was observed in a fraction of bowman's gland cells and hbcs ( figure s4 , see methods). expression in sustentacular cells was not observed in this dataset, which included relatively few dorsal sustentacular cells (a possible consequence of the specific cell isolation procedure associated with the 10x platform, which distinguishes it from drop-seq; compare figures s4c and 3d) . staining of the mouse wom with anti-ace2 antibodies confirmed that ace2 protein is expressed in sustentacular cells and is specifically localized to the sustentacular cell microvilli ( figure 3e -k). ace2+ sustentacular cells were identified exclusively within the dorsal subregion of the oe; critically, within that region many (and possibly all) sustentacular cells expressed ace2 ( figure 3f -g). this observation is consistent with the possibility that ace2 protein can be broadly expressed in cell populations that exhibit sparse expression when characterized by scseq. staining was also observed in bowman's gland cells but not in osns ( figure 3h -j). taken together, these data demonstrate that ace2 is expressed by sustentacular cells that specifically reside in the dorsal epithelium in both mouse and human. considered positive if any transcripts (umis) were expressed for a given gene. sustentacular cells (sus) from dorsal and ventral zones are quantified separately. ace2 is detected in dorsal sustentacular, bowman's gland, hbcs, as well as respiratory cell types. (d) umap representation of sustentacular cells, with expression of cov-2 related genes ace2 and tmprss2, as well as marker genes for sus (both pan-sus marker cbr2 and dorsal specific marker sult1c1) indicated. each point represents an individual sustentacular cell, and the color represents the normalized expression level for each gene (number of umis for a given gene divided by the total number of umis for each cell; in this plot ace2 expression is binarized for visualization purposes). ace2-positive sustentacular cells are found within the dorsal sult1c1positive subset. umap plots for other cell types are shown in figure s2 . (e) ace2 immunostaining of mouse main olfactory epithelium. as shown in this epithelial hemisection, ace2 protein is detected in the dorsal zone and respiratory epithelium. note that the punctate ace2 staining beneath the epithelial layer is likely associated with vasculature (see figure 5f ). bar = 500 µm. arrowheads depict the edges of ace2 expression, corresponding to the presumptive dorsal zone (confirmed in g). viral injury can lead to broad changes in oe physiology that are accompanied by recruitment of stem cell populations tasked with regenerating the epithelium (13, 30) . to characterize the distribution of ace2 expression under similar circumstances, we injured the oe by treating mice with methimazole (which specifically ablates osns), and then employed a previously established lineage tracing protocol to perform scseq on hbcs and their descendants during subsequent regeneration (see methods) (32) . this analysis revealed that after injury ace2 and tmprss2 are expressed in subsets of sustentacular cells and hbcs, as well as in the activated hbcs that serve to regenerate the epithelium (figures 4a-c and s5; note that activated hbcs express ace2 at higher levels than resting hbcs). analysis of the ace2+ sustentacular cell population revealed expression of dorsal epithelial markers ( figure 4d ). to validate these results, we re-analyzed a similar lineage tracing dataset in which identified hbcs and their progeny were subject to smart-seq2-based deep sequencing, which is more sensitive than scseq (32) . in this dataset, ace2 was detected in more than 0.7% of gbcs, nearly 2% of activated hbcs and nearly 3% of sustentacular cells but was not detected in osns ( figures s5b) . furthermore, larger percentages of hbcs, gbcs and sustentacular cells expressed tmprss2. immunostaining with anti-ace2 antibodies confirmed that ace2 protein was present in activated stem cells under these regeneration conditions ( figure 4e ). these results demonstrate that activated stem cells recruited during injury express ace2, and do so at higher levels than those in resting stem cells. given the potential for the re and oe in the nasal cavity to be directly infected with cov-2, we assessed the expression of ace2 and other cov entry genes in the mouse olfactory bulb (ob), which is directly connected to osns via cranial nerve i (cn i); in principle, alterations in bulb function could cause anosmia independently of functional changes in the oe. to do so, we performed scseq (using drop-seq, see methods) on the mouse ob, and merged these data with a previously published ob scseq analysis, yielding a dataset with nearly 50,000 single cells (see methods) (42) . this analysis revealed that ace2 expression was absent from ob neurons and instead was observed only in vascular cells, predominantly in pericytes, which are involved in blood pressure regulation, maintenance of the blood-brain barrier, and inflammatory responses (figures 5a-d and s6-7) (43) . although other potential cov proteases were expressed in the ob, tmprss2 was not expressed. we also performed smart-seq2-based deep sequencing of single ob dopaminergic juxtaglomerular neurons, a population of local interneurons in the ob glomerular layer that (like tufted cells) can receive direct monosynaptic input from nose osns (figures 5e and s8, see methods); these experiments confirmed the absence of ace2 and tmprss2 expression in this cell type. immunostaining in the ob revealed that blood vessels expressed high levels of ace2 protein, particularly in pericytes; consistent with the scseq results, staining was not observed in any neuronal cell type ( figure 5f ). these observations may also hold true for other brain regions, as re-analysis of 10 deeply sequenced scseq datasets from different regions of the nervous system demonstrated that ace2 and tmprss2 expression is absent from neurons, consistent with prior immunostaining results ( figure s9 ) (44) . given the extensive similarities detailed above in expression patterns for ace2 and tmprss2 in the mouse and human, these findings (performed in mouse) suggest that ob neurons are likely not a primary site of infection, but that vascular pericytes may be sensitive to cov-2 infection in the ob. here we show that subsets of oe sustentacular cells, hbcs, and bowman's gland cells in both mouse and human samples express the cov-2 receptor ace2 and the spike protein protease tmprss2. human oe sustentacular cells express these genes at levels comparable to those observed in lung cells. in contrast, we failed to detect ace2 expression in mature osns at either the transcript or protein levels. these observations suggest that cov-2 does not directly enter osns, but instead may target oe support and stem cells. similarly, neurons in the ob do not express ace2, whereas vascular pericytes do. thus primary infection of non-neuronal cell types -rather than sensory or bulb neurons -may be responsible for anosmia and related disturbances in odor perception in covid-19 patients. the identification of non-neuronal cell types in the oe and bulb susceptible to cov-2 infection suggests four possible, non-mutually-exclusive mechanisms for the acute loss of smell reported in covid-19 patients. first, local infection of support and vascular cells in the nose and bulb could cause significant inflammatory responses whose downstream effects could block effective odor conduction, or alter the function of osns or bulb neurons (14) (45). second, damage to support cells (which are responsible for local water and ion balance) could indirectly influence signaling from osns to the brain (46) . third, damage to sustentacular cells and bowman's gland cells in mouse models can lead to diffuse architectural damage to the entire oe, which in turn could abrogate smell perception (47) . finally, vascular damage could lead to hypoperfusion and inflammation leading to changes in ob function. immunostaining in the mouse suggests that ace2 protein is (nearly) ubiquitously expressed in sustentacular cells in the dorsal oe, despite sparse detection of ace2 transcripts using scseq. similarly, nearly all vascular cells positive for a pericyte marker also expressed ace2 protein, although only a fraction of ob pericytes were positive for ace2 message when assessed using scseq. although ace2 transcripts were more rarely detected than protein, there was a clear concordance at the cell type level: expression of ace2 mrna in a particular cell type accurately predicted the presence of ace2 protein, while ace2 transcript-negative cell types (including osns) did not express ace2 protein. if humans also exhibit a similar relationship between mrna and protein (a reasonable possibility given the precise match in olfactory cell types that express cov-2 cell entry genes between the two species), then ace2 protein is likely to be broadly expressed in human dorsal sustentacular cells. thus, in the there may be many sustentacular cells available for cov-2 infection in the human epithelium (which in turn could recruit a diffuse inflammatory process). that said, it remains possible that damage to the oe could be caused by more limited cell infection. for example, infection of subsets of sustentacular cells by the sdav coronavirus in rats ultimately leads to disruption of the global architecture of the oe, suggesting that focal coronavirus infection may be sufficient to cause diffuse epithelial damage (47) . the natural history of cov2-induced anosmia is only now being defined; while recovery of smell has been reported, it remains unclear whether in a subset of patients smell disturbances will be long-lasting or permanent (8) (9) (10) (11) (12) 48) . we observe that activated hbcs, which are recruited after injury, express ace2 at higher levels than those apparent in resting stem cells. while on its own it is likely that infection of stem cells would not cause acute smell deficits, in the context of infection the dual challenge of loss of sustentacular cells, together with the inability to effectively renew the oe over time, could result in persistent anosmia. many viruses, including coronaviruses, have been shown to propagate from the nasal epithelium past the cribriform plate to infect the ob; this form of central infection has been suggested to mediate olfactory deficits, even in the absence of lasting oe damage (18, (49) (50) (51) (52) (53) . the rodent coronavirus mhv passes from the nose to the bulb, even though rodent osns do not express ceacam1, the main mhv receptor (50, 54) ( figures s3c, s4e, s5a) , suggesting that covs in the nasal mucosa can reach the brain through mechanisms independent of axonal transport by sensory nerves; interestingly, ob dopaminergic juxtaglomerular cells express ceacam1 ( figure 4e ), which likely supports the ability of mhv to target the bulb and change odor perception. one speculative possibility is that local seeding of the oe with cov-2-infected cells can result in osn-independent transfer of virions from the nose to the bulb, perhaps via the vascular supply shared between the ob and the osn axons that comprise cn i. although cn i was not directly queried in our datasets, it is reasonable to infer that vascular pericytes in cn i also express ace2, which suggests a possible route of entry for cov-2 from the nose into the brain. given the absence of ace2 in ob neurons, we speculate that any central olfactory dysfunction in covid-19 is the secondary consequence of pericyte-mediated vascular inflammation (43) . we note several caveats that temper our conclusions. although current data suggest that ace2 is the most likely receptor for cov-2 in vivo, it is possible (although it has not yet been demonstrated) that other molecules such as bsg may enable cov-2 entry independently of ace2 ( figures 2e, s3c , s4e, s5a) (55, 56) . in addition, it has recently been reported that low level expression of ace2 can support cov-2 cell entry (57); it is possible, therefore, that ace2 expression beneath the level of detection in our assays may yet enable cov-2 infection of apparently ace2 negative cell types. we also propose that damage to the olfactory system is either due to primary infection or secondary inflammation; it is possible (although has not yet been demonstrated) that cells infected with cov-2 can form syncytia with cells that do not express ace2. such a mechanism could damage neurons adjacent to infected cells. any reasonable pathophysiological mechanism for covid-19-associated anosmia must account for the high penetrance of smell disorders relative to endemic viruses, the apparent suddenness of smell loss (which can precede the development of other symptoms), and the transient nature of dysfunction in many patients (8) (9) (10) (11) (12) (11, (13) (14) (15) ; definitive identification of the disease mechanisms underlying covid-19-mediated anosmia will require additional research. nonetheless, our identification of cells in the oe and ob expressing molecules known to be involved in cov-2 entry illuminates a path forward for future studies. human scseq data from durante et al. (37) was downloaded from the geo at accession gse139522. 10x genomics mtx files were filtered to remove any cells with fewer than 500 total counts. additional preprocessing was performed as described above, including total counts normalization and filtering for highly variable genes using the spring gene filtering function "filter_genes" with parameters (90, 3, 10) . the resulting data were visualized in spring and partitioned using louvain clustering on the spring k-nearest-neighbor graph. four clusters were removed for quality control, including two with low total counts (likely background) and two with high mitochondrial counts (likely stressed or dying cells). putative doublets were also identified using scrublet and removed (7% of cells). the remaining cells were projected to 40 dimensions using pca. pca-batch-correction was performed using patient 4 as a reference, as previously described (58) . the filtered data were then re-partitioned using louvain clustering on the spring graph and each cluster was annotated using known marker genes, as described in (37) . for example, immature and mature osns were identified via their expression of gng8 and gng13, respectively. hbcs were identified via the expression of krt5 and tp63 and olfactory hbcs were distinguished from respiratory hbcs via the expression of cxcl14 and meg3. identification of sus cells (cyp2a13, cyp2j2), bowman's gland (sox9, gpx3), and mv ionocytes-like cells (ascl3, cftr, foxi1) was also performed using known marker genes. for visualization, the top 40 principal components were reduced to two dimensions using umap with parameters (n_neighbors=15, min_dist=0.4). the filtered human scseq dataset contained 33358 cells. each of the samples contained cells from both the olfactory and respiratory epithelium, although the frequency of osns and respiratory cells varied across patients, as previously described (37) . 295 cells expressed ace2 and 4953 cells expressed tmprss2. of the 865 identified osns, including both immature and mature cells, none of the cells express ace2 and only 2 (0.23%) expressed tmprss2. in contrast, ace2 was reliably detected in at least 2% and tmprss2 was expressed in close to 50% of multiple respiratory epithelial subtypes. the expression of both known cell type markers and known cov-related genes was also examined across respiratory and olfactory epithelial cell types. for these gene sets, the mean expression in each cell type was calculated and normalized by the maximum across cell types. data from deprez et al. (34) were downloaded from the human cell atlas website (https://www.genomique.eu/cellbrowser/hca/; "single-cell atlas of the airway epithelium (grch38 human genome)"). a subset of these data was combined with a subset of the durante data for mapping between cell types. for the deprez data, the subset consisted of samples from the nasal re that belonged to a cell type with >20 cells, including basal, cycling basal, suprabasal, secretory, mucous multiciliated cells, multiciliated, sms goblet and ionocyte. we observed two distinct subpopulations of basal cells, with one of the two populations distinguished by expression of cxcl14. the cells in this population were manually identified using spring and defined for downstream analysis as a separate cell type annotation called "basal (cxcl14+)". for the durante data, the subset consisted of cells from cell types that had some putative similarity to cells in the deprez dataset, including olfactory hbc, cycling respiratory hbc, respiratory hbc, early respiratory secretory cells, respiratory secretory cells, sustentacular cells, bowman's gland, olfactory microvillar cells. to establish a cell type mapping: 1) durante (37) and deprez (34) data were combined and gene expression values were linearly scaled so that all cells across datasets had the same total counts. pca was then performed using highly variable genes (n=1477 genes) and pcabatch-correction (58) with the durante data as a reference set. 3) the table of votes t was z-scored against a null distribution, generated by repeating the procedure above 1000 times with shuffled cell type labels. the resulting z-scores were similar between the two possible mapping directions (durante -> deprez vs. deprez -> durante; r=0.87 pearson correlation of mapping zscores). the mapping z-scores were also highly robust upon varying the number of votes-cast per cell (r>0.98 correlation of mapping z-scores upon changing the vote numbers to 1 or 50 as opposed to 5). only cell-type correspondences with a high zscore in both mapping directions (z-score > 25) were used for downstream analysis. to establish a common scale of gene expression between datasets, we restricted to cell type correspondences that were supported both by bioinformatic mapping and shared a nominal cell type designation based on marker genes. these included: basal/suprabasal cells = "respiratory hbcs" from durante et al., and "basal" and "suprabasal" cells from deprez we next sought a transformation of the durante data so that it would agree with the deprez data within the corresponding cell types identified above to account for differing normalization strategies applied to each dataset prior to download (log normalization and rescaling with cell-specific factors for deprez et al. but not for durante et al.), we used the following ansatz for the transformation, where the pseudocount p is a global latent parameter and the rescaling factors ! are fit to each gene separately. in the equation below, t denotes the transformation and !" represents a gene expression value for cell i and gene j in the durante data: the parameter p was fit by maximizing the correlation of average gene expression across all genes between each of the cell type correspondences listed above. the rescaling factors ! were then fitted separately for each gene by taking the quotient of average gene expression between the deprez data and the log-transformed durante data, again across the cell type correspondences above. normalized gene expression tables were obtained from previous published datasets (36, (39) (40) (41) . for the mouse data sets, the means of the replicates from wom or osn were used to calculate log2 fold changes. for the mouse data from saraiva et al. and the primate data sets (36, 39) , the normalized counts of the genes of interest from individual replicates were plotted. below is a table with detailed sample information. sample information for the bulk rna-seq data analyzed in this study a new dataset of whole olfactory mucosa scseq was generated from adult male mice (8-12 weeks-old). all mouse husbandry and experiments were performed following institutional and federal guidelines and approved by harvard medical school's institutional animal care and use committee (iacuc). briefly, dissected main olfactory epithelium were cleaned up in 750 µl of ebss (worthington) and epithelium tissues were isolated in 750 µl of papain (20 u/ml in ebss) and 50 µl of dnase i (2000 u/ml). tissue pieces were transferred to a 5 ml round-bottom tube (bd) and 1.75 ml of papain and 450 µl of dnase i were added. after 1-1.5 hour incubation with rocking at 37°c, the suspension was triturated with a 5 ml pipette 15 times and passed through 40 µm cell strainer (bd) and strainer was washed with 1 ml of dmem + 10 % fbs (invitrogen). the cell suspension was centrifuged at 300g for 5 min. cells were resuspended with 4 ml of dmem + 10 % fbs and centrifuged at 300g for 5 min. cells were suspended with pbs + 0.01 % bsa and concentration was measured by hemocytometer. drop-seq experiments were performed as previously described (59) . microfluidics devices were obtained from flowjem and barcode beads were obtained from chemgenes. 8 of 15 min drop-seq runs were collected in total, which were obtained from 5 mice. 8 replicates of drop-seq samples were sequenced across 5 runs on an illumina nextseq 500 platform. paired end reads from the fastq files were trimmed, aligned, and tagged via the drop-seq tools (v1.13) pipeline, using star (v2.5.4a) with genomic indices from ensembl release 93. the digital gene expression matrix was generated for 4,000 cells for 0126_2, 5,000 cells for 0105, 0126_1, 051916_ds11, 051916_ds12, 051916_ds22, 5,500 cells for 051916_ds21, and 9,500 cells for 0106. processing of the wom drop-seq samples was performed in seurat (v2.3.1). cells with less than 500 umis or more than 15,000 umis, or higher than 5% mitochondrial genes were removed. potential doublets were removed using scrublet. cells were initially preprocessed using the seurat pipeline. variable genes "findvariablegenes" (y.cutoff = 0.6) were scaled (regressing out effects due to numi, the percent of mitochondrial genes, and replicate ids) and the data was clustered using 50 pcs with the louvain algorithm (resolution=0.8). in a fraction of sustentacular cells, we observed co-expression of markers for sustentacular cells and other cell types (e.g. osns). re-clustering of sustentacular cells alone separately out these presumed doublets from the rest of the sustentacular cells, and the presumed doublets were removed for the analyses described below. the filtered cells from the preprocessing steps were reanalyzed in python using scanpy and spring. in brief, the raw gene counts in each cell were total counts normalized and variable genes were identified using the spring gene filtering function "filter_genes" with parameters (85, 3, 3); mitochondrial and olfactory receptor genes were excluded from the variable gene lists. the resulting 2083 variable genes were zscored and the dimensionality of the data was reduced to 35 via principal component analysis. the k-nearest neighbor graph (n_neighbors=15) of these 35 pcs was clustered using the leiden algorithm (resolution=1.2) and was reduced to two dimensions for visualization via the umap method (min_dist=0.42). clusters were manually annotated on the basis of known marker genes and those sharing markers (e.g. olfactory sensory neurons) were merged. the mouse wom drop-seq dataset contained 29585 cells that passed the above filtering. each of the 16 clusters identified contained cells from all 8 replicates in roughly equal proportions. of the 17666 mature osns and the 4674 immature osns, none of the cells express ace2. in contrast, in the olfactory epithelial cells, ace2 expression was observed in the bowman's gland, olfactory hbcs, dorsal sustentacular cells. mice were sacrificed with a lethal dose of xylazine and nasal epithelium with attached olfactory bulbs were dissected and fixed in 4% paraformaldehyde (electron microscope sciences, 19202) in phosphate-buffered saline (pbs) for overnight at 4°c or for 2 hours at room temperature. tissues were washed in pbs for 3 times (5 min each) and incubated in 0.45m edta in pbs overnight at 4°c. the following day, tissues were rinsed by pbs and incubated in 30 % sucrose in pbs for at least 30 min, transferred to tissue freezing medium (vwr, 15146-025) for at least 45 min and frozen on crushed dry ice and stored at -80°c until sectioning. tissue sections (20 µm thick for the olfactory bulb and 12 µm thick for nasal epithelium) were collected on superfrost plus glass slides (vwr, 48311703) and stored at -80°c until immunostaining. for methimazole treated samples, adult c57bl/6j mice (6-12 weeks old, jax stock no. 000664) were given intraperitoneal injections with methimazole (sigma m8506) at 50 µg/g body weight and sacrificed at 24, 48, and 96-hour timepoints. sections were permeabilized with 0.1% triton x-100 in pbs for 20 min then rinsed 3 times in pbs. sections were then incubated for 45-60 min in blocking solution that consisted of pbs containing 3% bovine serum albumin (jackson immunoresearch, 001-000-162) and 3% donkey serum (jackson immunoresearch, 017-000-121) at room temperature, followed by overnight incubation at 4°c with primary antibodies diluted in the same blocking solution. primary antibodies used are as follows. after secondary antibody incubation, sections were washed twice for 5-10 min in pbs, incubated with 300 nm dapi in pbs for 10 min and then rinsed with pbs. slides were mounted with glass coverslips using vectashield mounting medium (vector laboratories, h-1000) or prolong diamond antifade mountant (invitrogen, p36961). for co-staining of ace2 and nqo1, slides were first stained with ace2 primary antibody and donkey anti-goat igg alexa 488 secondary. after 3 washes of secondary antibody, tissues were incubated with unconjugated donkey anti-goat igg fab fragments (jackson immunoresearch, 705-007-003) at 30 µg/ml diluted in blocking solution for 1 hour at room temperature. tissues were washed twice with pbs, once in blocking solution, and incubated in blocking solution for 30-40 min at room temperature, followed by a second round of staining with the nqo1 primary antibody and donkey anti-goat igg alexa 555 secondary antibody. confocal images were acquired using a leica spe microscope (harvard medical school neurobiology imaging facility) with 405 nm, 488 nm, 561 nm, and 635 nm laser lines. multi-slice z-stack images were acquired, and their maximal intensity projections are shown. for figure 3e , tiled images were acquired and stitched by the leica las x software. images were processed using fiji imagej software (60) , and noisy images were median-smoothed using the remove outliers function built into fiji. sult1c1 rna was detected by fluorescent rnascope assay (advanced cell diagnostics, kit 320851) using probe 539921-c2, following the manufacturer's protocol (rnascope fluorescent multiplex kit user manual, 320293-um date 03142017) for paraformaldehyde-fixed tissue. prior to initiating the hybridization protocol, the tissue was pre-treated with two successive incubations (first 30 min, then 15 min long) in rnascope protease iii (advanced cell diagnostics, 322337) at 40°c, then washed in distilled water. at the end of protocol, the tissue was washed in pbs and subjected to the 2-day immunostaining protocol described above. human olfactory mucosa biopsies were obtained via irb-approved protocol at duke university school of medicine, from nasal septum or superior turbinate during endoscopic sinus surgery. tissue was fixed with 4% paraformaldehyde and cryosectioned at 10 µm and sections were processed for immunostaining, as previously described (37) . sections from a female nasal septum biopsy were stained for ace2 ( figure 2f ) using the same goat anti-ace2 (thermo fisher, pa5-47488, 1:40) and the protocol described above for mouse tissue. the human sections were co-stained with rabbit antikeratin 5 (abcam, ab24647; ab_448212, 1:1000) and were detected with alexafluor 488 donkey anti-goat (jackson immunoresearch, 705-545-147) and alexafluor 594 donkey anti-rabbit (jackson immunoresearch, 711-585-152) secondary antibodies (1:300). as further validation of ace2 expression and to confirm the lack of ace2 expression in human olfactory sensory neurons ( figure s1e ), sections were stained with a rabbit anti-ace2 (abcam, ab15348; rrid:ab_301861, used at 1:100) antibody immunogenized against human ace2 and a mouse tuj1 antibody against neuronspecific tubulin (biolegend, 801201; rrid:ab_2313773). anti-ace2 was raised against a c-terminal synthetic peptide for human ace2 and was validated by the manufacturer to not cross-react with ace1 for immunohistochemical labeling of ace2 in fruit bat nasal tissue as well as in human lower airway. recombinant human ace2 abolished labeling with this antibody in a previous study in human tissue, further demonstrating its specificity (61) . the tuj1 antibody was validated, as previously described (37) . biotinylated secondary antibodies (vector labs), avidin-biotinylated horseradish peroxidase kit (vector) followed by fluorescein tyramide signal amplification (perkin elmer) were applied per manufacturer's instructions. for dual staining, tuj1 was visualized using alexafluor 594 goat anti-mouse (jackson immunoresearch, 115-585-146; rrid: ab_2338881). human sections were counterstained with 4',6-diamidino-2-phenylindole (dapi) and coverslips were mounted using prolong gold (invitrogen) for imaging, using a leica dmi8 microscope system. images were processed using fiji imagej software (nih). scale bars were applied directly from the leica acquisition software metadata in imagej tools. unsharp mask was applied in imagej, and brightness/contrast was adjusted globally. 2 month-old and 18 month-old wild type c57bl/6j mice were obtained from the national institute on aging aged rodent colony and used for the wom experiments; each experimental condition consisted of one male and one female mouse to aid doublet detection. mice containing the transgenic krt5-creer(t2) driver (62) and rosa26-yfp reporter allele (63) were used for the hbc lineage tracing dataset. all mice were assumed to be of normal immune status. animals were maintained and treated according to federal guidelines under iacuc oversight at the university of california, berkeley. the olfactory epithelium was surgically removed, and the dorsal, sensory portion was dissected and dissociated, as previously described (32) . for wom experiments, dissociated cells were subjected to fluorescence-activated cell sorting (facs) using propidium iodide to identify and select against dead or dying cells; 100,000 cells/sample were collected in 10% fbs. for the hbc lineage tracing experiments krt5-creer; rosa26yfp/yfp mice were injected once with tamoxifen (0.25 mg tamoxifen/g body weight) at p21-23 days of age and sacrificed at 24 hours, 48 hours, 96 hours, 7 days and 14 days post-injury, as previously described (32, 64) . for each experimental time point, yfp+ cells were isolated by facs based on yfp expression and negative for propidium iodide, a vital dye. cells isolated by facs were subjected to single-cell rna-seq. three replicates (defined here as a facs collection run) per age were analyzed for the wom experiment; at least two biological replicates were collected for each experimental condition for the hbc lineage tracing experiment. single cell cdna libraries from the isolated cells were prepared using the chromium single cell 3' system according to the manufacturer's instructions. the wom preparation employed v3 chemistry with the following modification: the cell suspension was directly added to the reverse transcription master mix, along with the appropriate volume of water to achieve the approximate cell capture target. the hbc lineage tracing experiments were performed using v2 chemistry. the 0.04% weight/volume bsa washing step was omitted to minimize cell loss. completed libraries were sequenced on illumina hiseq4000 to produce paired-end 100nt reads. sequence data were processed with the 10x genomics cell ranger pipeline (2.0.0 for v2 chemistry), resulting in the initial starting number before filtering of 60,408 wom cells and 25,469 hbc lineage traced cells. the scone r/bioconductor package (65) was used to filter out lowly-expressed genes (fewer than 2 umi's in fewer than 5 cells) and low-quality libraries (using the metric_sample_filter function with arguments hard_nreads = 2000, zcut = 4). cells with co-expression of male (ddx3y, eif2s3y, kdm5d, and uty) and female marker genes (xist) were removed as potential doublets from the wom dataset. for both datasets, doublet cell detection was performed per sample using doubletfinder (66) and scrublet (67) . genes with at least 3 umis in at least 5 cells were used for downstream clustering and cell type identification. for the hbc lineage tracing dataset, the bioconductor package scone was used to pick the top normalization ("none,fq,ruv_k=1,no_bio,batch"), corresponding to full quantile normalization, batch correction and removing one factor of unwanted variation using ruv (68) . a range of cluster labels were created by clustering using the partitioning around medoids (pam) algorithm and hierarchical clustering in the clusterexperiment bioconductor package (69) , with parameters k0s= (10, 13, 16, 19, 22, 25) and alpha=(na,0.1,0.2,0.3). clusters that did not show differential expression were merged (using the function mergeclusters with arguments mergemethod = 'adjp', cutoff = 0.01, and demethod = 'limma' for the lineagetraced dataset). initial clustering identified one macrophage (msr1+) cluster consisting of 252 cells; upon its removal and restarting from the normalization step a subsequent set of 15 clusters was obtained. these clusters were used to filter out 1515 cells for which no stable clustering could be found (i.e., 'unassigned' cells), and four clusters respectively consisting of 31, 29 and 23 and 305 cells. doublets were identified using doubletfinder and 271 putative doublets were removed. inspection of the data in a three-dimensional umap embedding identified two groups of cells whose experimentally sampled timepoint did not match their position along the hbc differentiation trajectory, and these additional 219 cells were also removed from subsequent analyses. analysis of wom scseq data were performed in python using the open-source scanpy software starting from the raw umi count matrix of the 40179 cells passing the initial filtering and qc criteria described above. umis were total-count normalized and scaled by 10,000 (tpt, tag per ten-thousands) and then log-normalized. for each gene, the residuals from linear regression models using the total number of umis per cell as predictors were then scaled via z-scoring. pca was then performed on a set of highlyvariable genes (excluding or genes) calculated using the "highly_variable_genes" function with parameters: min_mean=0.01, max_mean=10, min_disp=0.5. a batch corrected neighborhood graph was constructed by the "bbknn" function with 42 pcs with the parameters: local_connectivity=1.5, and embedding two-dimensions using the umap function with default parameters (min_dist = 0.5). cells were clustered using the neighborhood graph via the leiden algorithm (resolution = 1.2). identified clusters were manually merged and annotated based on known marker gene expression. we the filtered hbc lineage dataset containing 21722 cells was analyzing in python and processed for visualization using pipelines in spring and scanpy (70, 71) . in brief, total counts were normalized to the median total counts for each cell and highly variable genes were selected using the spring gene filtering function ("filter_genes") using parameters (90, 3, 3) . the dimensionality of the data was reduced to 20 using principal components analysis (pca) and visualized in two-dimensions using the umap method with parameters (n_neighbors=20, min_dist=0.5). clustering was performed using the leiden algorithm (resolution=1.45) and clusters were merged manually using known marker genes. expression of candidate cov-2-related genes was defined if at least one transcript (umi) was detected in that cell, and the percent of cells expressing candidate genes was calculated for each cell type. in the wom dataset ace2 was only detected in 2 out of 28,769 mature osns (0.007 %), and in the hbc lineage dataset, ace2 was not detected in any osns. furthermore, ace2 was not detected in immature sensory neurons (gbcs, inps, or iosns) in either dataset. single-cell rna-seq data from hbc-derived cells from fletcher et al. and gadye et al (32, 64) , labeled via krt5-creer driver mice, were downloaded from geo at accession gse99251 using the file "gse95601_oehbcdiff_cufflinks_eset_counts_table.txt.gz". processing was performed as described above, including total counts normalization and filtering for highly variable genes using the spring gene filtering function "filter_genes" with parameters (75, 20, 10) . the resulting data were visualized in spring and a subset of cells were removed for quality control, including a cluster of cells with low total counts and another with predominantly reads from ercc spike-in controls. putative doublets were also identified using scrublet and removed (6% of cells) (67) . the resulting data were visualized in spring and partitioned using louvain clustering on the spring k-nearest-neighbor graph using the top 40 principal components. cell type annotation was performed manually using the same set of markers genes listed above. three clusters were removed for quality control, including one with low total counts and one with predominantly reads from ercc spike-in controls (likely background), and one with high mitochondrial counts (likely stressed cells). for visualization, and clustering the remaining cells were projected to 15 dimensions using pca and visualized with umap with parameters (n_neighbors=15, min_dist=0.4, alpha=0.5, maxiter=500). clustering was performed using the leiden algorithm (resolution=0.4) and cell types were manually annotated using known marker genes. the filtered dataset of mouse hbc-derived cells contained 1450 cells. the percent of cells expressing each marker gene was calculated as described above. of the 51 osns identified, none of them expressed ace2, and only 1 out of 194 inps and iosns expressed ace2. in contrast, ace2 and tmprss2 were both detected in hbcs and sus cells. single-cell rnaseq data from whole mouse olfactory bulb (42) were downloaded from mousebrain.org/loomfiles_level_l1.html in loom format (l1 olfactory.loom) and converted to a seurat object. samples were obtained from juvenile mice (age postnatal day [26] [27] [28] [29] . this dataset comprises 20514 cells passing cell quality filters, excluding 122 cells identified as potential doublets. a new dataset of whole olfactory bulb scseq was generated from adult male mice (8-12 weeks-old). all mouse husbandry and experiments were performed following institutional and federal guidelines and approved by harvard medical school's institutional animal care and use committee (iacuc). briefly, dissected olfactory bulbs (including the accessory olfactory bulb and fractions of the anterior olfactory nucleus) were dissociated in 750 µl of dissociation media (dm: hbss containing 10mm hepes, 1 mm mgcl2, 33 mm d-glucose) with 28 u/ml papain and 386 u/ml dnase i (worthington). minced tissue pieces were transferred to a 5 ml round-bottom tube (bd). dm was added to a final volume of 3.3 ml and the tissue was mechanically triturated 5 times with a p1000 pipette tip. after 1-hour incubation with rocking at 37°c, the suspension was triturated with a 10 ml pipette 10 times and 2.3 ml was passed through 40 µm cell strainer (bd). the suspension was then mechanically triturated with a p1000 pipette tip 10 times and 800 µl were filtered on the same strainer. the cell suspension was further triturated with a p200 pipette tip 10 times and filtered. 1 ml of quench buffer (22 ml of dm, 2.5 ml of protease inhibitor prepared by resuspending 1 vial of protease inhibitor with 32 ml of dm, and 2000u of dnase i) was added to the suspension and centrifuged at 300g for 5 min. cells were resuspended with 3 ml of quench buffer and overlaid gently on top of 5 ml of protease inhibitor, then spun down at 70g for 10min. the pellet was resuspended using dm supplemented with 0.04 % bsa and spun down at 300g for 5 min. cells were suspended in 400 µl of dm with 0.04 % bsa. drop-seq experiments were performed as previously described (59) . microfluidics devices were obtained from flowjem and barcode beads were obtained from chemgenes. two 15 min drop-seq runs were collected from a single dissociation preparation obtained from 2 mice. two such dissociations were performed, giving 4 total replicates. 4 replicates of drop-seq samples were pooled and sequenced across 3 runs on an illumina nextseq 500 platform. paired end reads from the fastq files were trimmed, aligned, and tagged via the drop-seq tools (1-2.0) pipeline, using star (2.4.2a) with genomic indices from ensembl release 82. the digital gene expression matrix was generated for 8,000 cells per replicate. cells with low numbers of genes (500), low numbers of umis (700) or high numbers of umis (>10000) were removed (6 % of cells). potential doublets were identified via scrublet and removed (3.5 % of cells). overall, this new dataset comprised 27004 cells. raw umi counts from juvenile and adult whole olfactory bulb samples were integrated in seurat (72) . integrating the datasets ensured that clusters with rare cell types could be identified and that corresponding cell types could be accurately matched. as described below (see figure s5 ), although some cell types were observed with different frequencies, the integration procedure yielded stable clusters with cells from both datasets. briefly, raw counts were log-normalised separately and the 10000 most variable genes identified by variance stabilizing transformation for each dataset. the 4529 variable genes present in both datasets and the first 30 principal components (pcs) were used as features for identifying the integration anchors. the integrated expression matrix was scaled and dimensionality reduced using pca. based on their percentage of explained variance, the first 28 pcs were chosen for umap visualisation and clustering. graph-based clustering was performed using the louvain algorithm following the standard seurat workflow. cluster stability was analysed with clustree on a range of resolution values (0.4 to 1.4), with 0.6 yielding the most stable set of clusters (73) . overall, 26 clusters were identified, the smallest of which contained only 43 cells with gene expression patterns consistent with blood cells, which were excluded from further visualisation plots. clustering the two datasets separately yielded similar results. moreover, the distribution of cells from each dataset across clusters was homogenous ( figure s5 ) and the clusters corresponded previous cell class and subtype annotations (42) . as previously reported, a small cluster of excitatory neurons (cluster 13) contained neurons from the anterior olfactory nucleus. umap visualisations of expression level for cell class and cell type markers, and for genes coding for coronavirus entry proteins, depict log-normalized umi counts. the heatmap in figure 4b shows the mean expression level for each cell class, normalised to the maximum mean value. the percentage of cells per cell class expressing ace2 was defined as the percentage of cells with at least one umi. in cells from both datasets, ace2 was enriched in pericytes but was not detected in neurons. acute olfactory bulb 300 µm slices were obtained from dat-cre/flox-tdtomato (b6.sjl-slc6a3 tm1.1(cre) bkmn/j , jax stock 006660 / b6.cg-gt(rosa)26sor tm9(cag-tdtomato)hze , jax stock 007909) p28 mice as previously described (74) . as part of a wider study, at p27 these mice had undergone brief 24 h unilateral naris occlusion via a plastic plug insert (n = 5 mice) or were subjected to a sham control manipulation (n = 5 mice); all observed effects here were independent of these treatment groups. single cell suspensions were generated using the neural tissue dissociation kit -postnatal neurons (miltenyi biotec. cat no. 130-094-802), following manufacturer's instructions for manual dissociation, using 3 fired-polished pasteur pipettes of progressively smaller diameter. after enzymatic and mechanical dissociations, cells were filtered through a 30 µm cell strainer, centrifuged for 10 minutes at 4° c, resuspended in 500 µl of acsf (in mm: 140 nacl, 1.25 kcl, 1.25 nah2po4, 10 hepes, 25 glucose, 3 mgcl2, 1 cacl2) with channel blockers (0.1 µm ttx, 20 µm cnqx, 50 µm d-apv) and kept on ice to minimise excitotoxicity and cell death. for manual sorting of fluorescently labelled dopaminergic neurons we adapted a previously described protocol (75) . 50 µl of single cell suspension was dispersed on 3.5mm petri dishes (with a sylgard-covered base) containing 2 ml of acsf + channel blockers. dishes were left undisturbed for 15 minutes to allow the cells to sink and settle. throughout, dishes were kept on a metal plate on top of ice. tdtomato-positive cells were identified by their red fluorescence under a stereoscope. using a pulled glass capillary pipette attached to a mouthpiece, individual cells were aspirated and transferred to a clean, empty dish containing 2 ml acsf + channel blockers. the same cell was then transferred to a third clean plate, changing pipettes for every plate change. finally, each individual cell was transferred to a 0.2 ml pcr tube containing 2 µl of lysis buffer (rlt plus -qiagen). the tube was immediately placed on a metal plate sitting on top of dry ice for flash-freezing. collected cells were stored at -80c until further processing. positive (more than 10 cells) and negative (sample collection procedure without picking a cell) controls were collected for each sorting session. in total, we collected samples from 2.5 hours elapsed between mouse sacrifice and collection of the last cell in any session. samples were processing using a modified version of the smart-seq2 protocol (76) . briefly, 1 µl of a 1:2,000,000 dilution of ercc spike-ins (invitrogen. cat. no. 4456740) was added to each sample and mrna was captured using modified oligo-dt biotinylated beads (dynabeads, invitrogen). pcr amplification was performed for 22 cycles. amplified cdna was cleaned with a 0.8:1 ratio of ampure-xp beads (beckman coulter). cdnas were quantified on qubit using hs dna reagents (invitrogen) and selected samples were run on a bioanalyzer hs dna chip (agilent) to evaluate size distribution. for generating the sequencing libraries, individual cdna samples were normalised to 0.2ng/µl and 1µl was used for one-quarter standard-sized nextera xt (illumina) tagmentation reactions, with 12 amplification cycles. sample indexing was performed using index sets a and d (illumina). at this point, individual samples were pooled according to their index set. pooled libraries were cleaned using a 0.6:1 ratio of ampure beads and quantified on qubit using hs dna reagents and with the kapa library quantification kits for illumina (roche). samples were sequenced on two separate rapid-runs on hiseq2500 (illumina), generating 100bp paired-end reads. an additional 5 samples were sequenced on miseq (illumina). paired-end read fastq files were demultiplexed, quality controlled using fastqc (https://www.bioinformatics.babraham.ac.uk/projects/fastqc/) and trimmed using trim galore (https://www.bioinformatics.babraham.ac.uk/projects/trim_galore/). reads were pseudoaligned and quantified using kallisto (77) against a reference transcriptome from ensembl release 89 (gencode release m17 grcm38.p6) with sequences corresponding to the ercc spike-ins and the cre recombinase and tdt genes added to the index. transcripts were collapsed into genes using the sumacrossfeatures function in scater. cell level quality control and cell filtering was performed in scater (78) . cells with <1000 genes, <100,000 reads, >75% reads mapping to ercc spike-ins, >10% reads mapping to mitochondrial genes or low library complexity were discarded (14% samples). the population of olfactory bulb cells labelled in dat-tdtomato mice is known to include a minor non-dopaminergic calretinin-positive subgroup (79) , so calretininexpressing cells were excluded from all analyses. the sctransform function in seurat was used to remove technical batch effects. an analysis of single-cell gene expression data from 10 studies was performed to investigate the expression of genes coding for coronavirus entry proteins in neurons from a range of brain regions and sensory systems. processed gene expression data tables were obtained from scseq studies that evaluated gene expression in retina (gse81905) (80) inner ear sensory epithelium (gse115934) (81, 82) and spiral ganglion (gse114997) (83) , ventral midbrain (gse76381) (84) , hippocampus (gse100449) (85), cortex (gse107632) (86), hypothalamus (gse74672) (87), visceral motor neurons (gse78845) (88) , dorsal root ganglia (gse59739) (89) and spinal cord dorsal horn (gse103840) (90) . smart-seq2 sequencing data from vsx2-gfp positive cells was used from the retina dataset. a subset of the expression matrix that corresponds to day 0 (i.e. control, undisturbed neurons) was used from the layer vi somatosensory cortex dataset. a subset of the data containing neurons from untreated (control) mice was used from the hypothalamic neuron dataset. from the ventral midbrain dopaminergic neuron dataset, a subset comprising dat-cre/tdtomato positive neurons from p28 mice was used. a subset comprising type i neurons from wild type mice was used from the spiral ganglion dataset. the "unclassified" neurons were excluded from the visceral motor neuron dataset. a subset containing neurons that were collected at room temperature was used from the dorsal root ganglia dataset. expression data from dorsal horn neurons obtained from c57/bl6 wild type mice, vgat-cre-tdtomato and vglut2-egfp mouse lines was used from the spinal cord dataset. inspection of all datasets for batch effects was performed using the scater package (version 1.10.1) (78) . publicly available raw count expression matrices were used for the retina, hippocampus, hypothalamus, midbrain, visceral motor neurons and spinal cord datasets, whereas the normalized expression data was used from the inner ear hair cell datasets. for datasets containing raw counts, normalization was performed for each dataset separately by computing pool-based size factors that are subsequently deconvolved to obtain cell-based size factors using the scran package (version 1.10.2) (91). violin plots were generated in scater. (39) . normalized counts for each gene in the whole olfactory mucosa (wom) and olfactory sensory neurons (osns) are shown. each circle represents a biological replicate and each color indicates the category of the gene shown on the right (cov-2 and other covs: genes involved in the entry of these viruses, other categories: marker genes for specific cell types such fig. 2a for three bulk rna-sequencing datasets. mhv, mouse hepatitis virus. left plot is same as fig. 2a except for the addition of ceacam1. (c) gene expression for cov-related genes including ace2 and tmprss2 as well as marker genes for olfactory and re subtypes are shown normalized by their maximum expression across cell types. ace2 and tmprss2 are expressed in wom respiratory and non-neuronal olfactory cell types, but not in osns. (d) umap representations of gene expression in the wom dataset for cov-2 related genes ace2 and tmprss2, as well as marker genes for each cell type. each point represents an individual cell, and the color represents the normalized expression level for each gene (number of umis for a given gene divided by the total number of umis for each cell). (e) fluorescent in situ hybridization of an identified dorsal sustentacular cell marker, sult1c1 (in yellow), combined with immunostaining for the known dorsal osn marker nqo1 (white). note that sult1c1 rna fills the apical cytoplasm; given that sustentacular cells are ubiquitous in the epithelium, this is apparent as broad antisense signal for sult1c in a pattern that is characteristic of the apical anatomy of sustentacular cells. sult1c1 rna is detected in sustentacular cells in the nqo1-positive dorsal olfactory epithelium. nuclei were stained with dapi (blue). bar = 20 µm. granule cells (0) granule cells (1) immature neurons (2) granule cells (3) calretinin neurons (4) astrocytes (5) olfactory ensheathing cells (6) immature neurons (7) interneurons (8) microglia (9) oligodendrocytes (10) dopaminergic neurons (11) interneurons (12) mitral/tufted cells -aon (13) astrocytes (14) vascular (15) oligo precursor cells (16) pericytes (17) external tufted cells (18) mitral/tufted cells (19) perivascular macrophages (20) vip neurons (21) vascular leptomeningeal cells (22) intermediate progenitor cells (23) granule cells ( hypothalamus (romanov) retina (shekhar) inner ear spiral ganglion (shrestha) dorsal root ganglia (usoskin) clinical characteristics of coronavirus disease 2019 in china the epidemiology and pathogenesis of coronavirus disease (covid-19) outbreak characteristics of and important lessons from the coronavirus disease 2019 (covid-19) outbreak in china: summary of a report of 72 314 cases from the chinese center for disease control and prevention a pneumonia outbreak associated with a new coronavirus of probable bat origin differences and similarities between severe acute respiratory syndrome (sars)-coronavirus (cov) and sars-cov-2. would a rose by another name smell as sweet? coronavirusesdrug discovery and therapeutic options hosts and sources of endemic human coronaviruses coincidence of covid-19 epidemic and olfactory dysfunction outbreak self-reported 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the mouse utricle using new celltype-specific markers sensory neuron diversity in the inner ear is shaped by activity sensory neuron diversity molecular diversity of midbrain development in resource molecular diversity of midbrain development in mouse, human and stem cells dissociable structural and functional hippocampal outputs via distinct subiculum cell classes variation in activity state, axonal projection, and position define the transcriptional identity of individual neocortical projection neurons molecular interrogation of hypothalamic organization reveals distinct dopamine neuronal subtypes visceral motor neuron diversity delineates a cellular basis for nipple-and pilo-erection muscle control unbiased classification of sensory neuron types by large-scale single-cell rna sequencing neuronal atlas of the dorsal horn defines its architecture and links sensory input to transcriptional cell types pooling across cells to normalize single-cell rna sequencing data with many zero counts we thank members of the datta lab, james schwob, bernardo sabatini, andreas schaefer, kevin franks, michael greenberg and vanessa ruta for helpful comments on the manuscript. we thank james lipscombe and andres crespo for technical support. data and materials availability: reanalyzed datasets are obtained from the urls listed in supplementary materials. all data is currently being deposited and will be made publicly accessible from the ncbi geo at accession gse148360. normalized expression * * * olfactory ensheathing cells (oec) and respiratory cells. (e) gene expression for cov-related genes including ace2 and tmprss2 as well as marker genes for olfactory and re subtypes are shown normalized by their maximum expression across cell types. ace2 and tmprss2 are expressed in wom respiratory and olfactory cell types, but not in osns. (f) cov-2 related genes ace2 and tmprss2, as well as marker genes for cell types in fig. 2c ., in umap representation of wom dataset with normalized expression. gfap-positive oecs (olfactory ensheathing cells) and muc5b-positive secretory cells are indicated by asterisks. key: cord-307110-eiobmxp2 authors: zhao, shan; li, wentao; schuurman, nancy; van kuppeveld, frank; bosch, berend-jan; egberink, herman title: serological screening for coronavirus infections in cats date: 2019-08-13 journal: viruses doi: 10.3390/v11080743 sha: doc_id: 307110 cord_uid: eiobmxp2 coronaviruses (covs) are widespread among mammals and birds and known for their potential for cross-species transmission. in cats, infections with feline coronaviruses (fcovs) are common. several non-feline coronaviruses have been reported to infect feline cells as well as cats after experimental infection, supported by their ability to engage the feline receptor ortholog for cell entry. however, whether cats might become naturally infected with covs of other species is unknown. we analyzed coronavirus infections in cats by serological monitoring. in total 137 cat serum samples and 25 fcov type 1 or type 2-specific antisera were screened for the presence of antibodies against the s1 receptor binding subunit of the cov spike protein, which is immunogenic and possesses low amino acid sequence identity among coronavirus species. seventy-eight sera were positive for antibodies that recognized one or more coronavirus s1s whereas 1 serum exclusively reacted with human coronavirus 229e (hcov-229e) and two sera exclusively reacted with porcine delta coronavirus (pdcov). we observed antigenic cross-reactivity between s1s of type 1 and type 2 fcovs, and between fcov type 1 and porcine epidemic diarrhea virus (pedv). domain mapping of antibody epitopes indicated the presence of conserved epitope(s) particularly in the cd domains of s1. the cross-reactivity of fcov type 1 and pedv was also observed at the level of virus neutralization. to conclude, we provide the first evidence of antigenic cross-reactivity among s1 proteins of coronaviruses, which should be considered in the development of serological diagnoses. in addition, the potential role of cats in cross-species transmission of coronaviruses cannot be excluded. coronaviruses (covs) are enveloped viruses with a positive-stranded rna genome and classified into four genera (alpha-, beta-, gamma-and deltacoronavirus) within the subfamily orthocoronavirinae in the family coronaviridae of the order nidovirales. covs are found in a variety of mammals and birds, in which they can cause respiratory, enteric and systemic infections [1] [2] [3] . additionally, covs have proven ability for cross-species transmission, exemplified by the emergence of severe acute respiratory syndrome (sars) coronavirus in 2002/2003, and of the middle-east respiratory syndrome (mers) coronavirus in 2012 [4] . both viruses belong to the betacoronavirus genus and have an animal origin. sars coronavirus crossed over from bats via intermediate hosts to humans, became human-adapted and quickly spread worldwide before its containment. mers coronavirus recurrently enters the human population via its dromedary camel reservoir host, with limited, non-sustained human-to-human transmission particularly in healthcare settings [5] [6] [7] . apart from sars-and mers-cov, all four globally endemic human covs (hcov-oc43, hcov-nl63, hcov-229e and hcov-hku1) originate viruses 2019, 11, 743 2 of 16 from animals [8] [9] [10] [11] . in addition, cross-species transmission potential of covs is also illustrated by the occurrence of chimeric coronaviruses that resulted from recombination events between feline covs (fcov) and canine covs (ccov) [12, 13] . in order to get insight into the frequency of interspecies transmission of coronaviruses within and between animal and human populations and the risk of subsequent development of a pandemic, it is useful to screen for coronavirus infections in animal species; especially those that are in close contact with humans. serological assays that can detect virus-specific antibody responses against infection play an important role in these epidemiological studies [14] . cats live in close contact with humans and often roam around freely in the environment. hence cats are an interesting species to study for infections with coronaviruses. infections with feline coronaviruses (fcovs) are recognized and widespread [15, 16] . fcovs are classified into two types, type 1 and type 2, based on the genetic and antigenic difference of their spike (s) protein [17] . in the field, the majority of fcov infections are caused by fcov type 1, while fcov type 2, derived from recombination events of type 1 fcovs and ccovs obtaining the s gene and some flanking regions of ccovs, is less prevalent [18, 19] . depending on the virulence of the fcov strain and the immune response of the cat, the clinical presentation can range from apparently asymptomatic, through diarrhea, to full-blown feline infectious peritonitis [20] . fcovs are members of the genus alphacoronavirus, to which also hcov-229e, porcine transmissible gastroenteritis virus (tgev), and ccov belong. the latter three viruses and fcov type 2 have been proven to use feline aminopeptidase n (fapn) as a functional receptor in vitro [21] . the receptor for type 1 fcov has still not been identified [22] . notably, previous studies have shown that hcov-229e and ccov could infect cats after experimental inoculation, causing an asymptomatic infection [23, 24] . thus, cats might potentially become naturally infected with covs of other species which may lead to virus-host adaptation e.g., mutation or recombination, resulting in emergence of novel coronaviruses and potentially new diseases [19, 25] . the extent to which infections with covs of other species occur in the field, has not been explored in previous epidemiological studies of cov infections in cats [15, [26] [27] [28] . being the main envelope protein of coronaviruses, the spike (s) protein mediates cell attachment and membrane fusion to allow viral entry. s functions as the main determinant of cell-, organ-and host-tropism. additionally, it is also the major target of neutralizing antibodies. spike comprises two functionally interdependent subunits, s1 and s2, with s1 responsible for receptor binding and s2 for membrane fusion [3, 29] . the s1 subunit is the least conserved and the most variable immunogenic antigen between coronavirus species [30] . therefore, the s1 subunit is well suited as an antigen to screen for coronavirus type specific antibodies [31] . in this study, covs infection in cats were detected through profiling antibody presence in serum samples from cats. recombinant cov spike s1 subunits of different animal and human covs were expressed in a mammalian expression system and used for screening of cat sera for the presence of antibodies against the respective proteins. positive samples were also tested by virus neutralization assays to support the specificity of the reaction [32] [33] [34] . this investigation intends to extend our knowledge of cov epidemiology, potential reservoirs, and cross-species transmission. specific fcov type 1 and fcov type 2 sera were obtained from specific pathogen free (spf) cats previously infected with strain uu2 or rm and fipv-1146 respectively [35, 36] . in addition, for the serological survey, 137 feline sera were retrieved from the serum bank in our lab. these had all been collected from cats in the netherlands. most of the samples (>80%) were from a study on antibody titer testing for feline panleukopenia virus. the other samples were send to our lab for fip or felv-fiv diagnostics. sera of uninfected spf cats were included as negative controls. all samples were stored at −20 • c until analysis. african green monkey kidney cells (vero-ccl81), human hepatoma cells (huh7), pig kidney epithelial cells (llc-pk1), human embryonic kidney 293 cells stably expressing the sv40 large t antigen (hek-293t) were maintained in dulbecco modified eagle medium (dmem, lonza, basel, switzerland) supplemented with 10% fetal bovine serum (fbs, bodinco, alkmaar, the netherlands). virus strains used in this study have been described previously [37] [38] [39] . briefly, recombinant porcine epidemic diarrhea virus (pedv) (rpedv-s dr13 -gfp) was propagated and titrated in vero cells, and hcov-229e in huh7 cells. pdcov was propagated and titrated in llc-pk1 cells, but supplemented with 1 µg/ml tpck-treated trypsin (sigma-aldrich, inc., st louis, mo, usa) in dmem. synthetic sequences of 12 coronavirus spike s1 subunits (hcov-hku1 (gb: yp_173238.1), mers-cov (gb:yp_009047204.1), sars-cov (gb: aax16192.1), hcov-oc43 (gb: aar01015.1), hcov-229e (gb: np_073551.1), hcov-nl63 (gb: yp_003767.1), tgev (gb: abg89325.1), pedv (gb: aog30832.1), bcov (gb: p15777.1), pdcov (gb: aml40825.1), fcov type 1 (gb: fj938060.1), fcov type 2 (gb: ay994055.1)) and different domains of pedv s1 subunit (s1 0 and s1 a-d , as identified and described in [40] ) were cloned into pcaggs expression plasmids as described previously [41] . similarly, the expression constructs encoding chimeric proteins in which s1s were fused to the fc domain of mouse igg2a. for protein production, hek-293t cells were transfected with plasmid dna conjugated to polyethyleneimine (polysciences, inc., warrington, pa, usa). at 8-16 h post transfection, inoculum was removed and the transfection mixture was replaced by 293 sfm ii expression medium (gibco®, life technologies inc., grand island, ny, usa). at 6-7 days post transfection, cell supernatants were harvested and proteins were collected by protein a sepharose beads (ge healthcare bio-sciences ab, uppsala, sweden). proteins were then eluted with 0.1 m citric acid, ph 3.0 and neutralized with 1 m tris-hcl, ph 8.8. concentrations of proteins were assessed by nanodrop spectrophotometry (thermofisher scientific inc., waltham, ma, usa) and confirmed by sodium dodecyl sulphate polyacrylamide gel electrophoresis (sds-page) with bovine serum albumin (bsa, bioivt, west sussex, uk) as standard. typical yields for proteins were 0.2-0.5 mg/ml. for long term storage, proteins were stored at −80 • c upon usage. to study the potential cross-reaction between fcov type 1 and 2 in more detail, models of fcov type 1 (strain: uu2; genbank accession no.: fj938060.1) and fcov type 2 (strain: 79-1146; genbank accession no.: ay994055.1) s proteins were generated via the automated protein structure swiss-model homology modelling server (https://swissmodel.expasy.org/) [42] using the elucidated hcov-nl63 cryo-em structure (pdb code: 5szs) as the input model. figures were made with pymol (the pymol molecular graphics system, version 1.0 schrödinger, llc.). fcov s1 domains of both type 1 and 2, namely s1 0-cd , were expressed as murine fc fusion proteins in hek-293t cells as described above. high binding microtiter plates (greiner bio-one bv, alphen aan den rijn, the netherlands) were coated overnight at 4 • c with equal molar amount of protein (0.25 pmol per well, diluted in phosphate buffered saline (pbs, ph 7.4)). after three washes with washing buffer (pbs containing 0.05% tween-20), the plates were blocked for 2 h at 37 • c with blocking buffer (pbs containing 5% milk powder (protifar, nutricia, zoetermeer, the netherlands), 0.05% tween-20). protein coating efficiency was assessed by binding of anti-mouse igg antibodies in a direct elisa, and confirmed the equimolar coatings of all proteins. to detect antigenic reaction with serum samples, sera were tested in duplicate at a 1:200 dilution in blocking buffer, and then incubated in the plates at 37 • c for 1 h. after washing, plates were incubated with a 1:4000 diluted horseradish peroxidase (hrp)-conjugated goat anti cat igg (rockland immunochemicals, inc., pottstown, pa, usa) at 37 • c for 1 h. the peroxidase reaction was then visualized via adding tmb super slow one component hrp microwell substrate (biofx®, surmodics ivd, inc., eden prairie, mn, usa) for 10 min. reaction was stopped with 12.5% sulfuric acid and optical densities (od) were measured at 450 nm. negative sera (from uninfected spf cats) were included to determine the elisa cut-off values; sera with od values higher than 5-fold the od of negative sera were considered positive. all 12 s1 proteins were coated on the same elisa plates making it easy to screen and compare the od values of individual sera in one assay. hereby we excluded the sera that give high background od values against all proteins being considered false positive. neutralization assays were performed with some of the covs to support the specificity of elisa results. cat sera were serially diluted 2-fold in dmem and mixed 1:1 with rpedv-s dr13 -gfp, hcov-229e or pdcov (2000 50% tissue culture infective doses [tcid 50 ]/ml). these mixtures were then incubated at 37 • c for 1h, and 100 µl of each mixture was used for inoculation with vero, huh7 and llc-pk1 cell monolayers in 96-well plates, respectively. for pdcov infection, tpck-treated trypsin (sigma-aldrich, inc., st louis, mo, usa) was supplied to llc-pk1 tissue culture medium at a final concentration of 1 µg/ml. at 2-5 days post infection, cytopathic effect (cpe) could be observed via microscopy. virus neutralization titers (vnt) were expressed as the highest serum dilution resulting in 90% reduction of cytopathic effect (hcov-229e and pdcov) or virus-induced fluorescent cells (pedv). before virus neutralization, sera were inactivated through incubation at 56 • c for 30 min. experiments were performed in triplicate. feline sera (n = 137) were screened by indirect elisa for antibody reactivity against 12 cov s1 antigens. the od values against these 12 antigens are shown in figure 1 . in total, 78 of the 137 sera (56.9%) contained anti-cov antibodies, while 43 sera showed reactivity against more than one cov s1 antigen. none of the samples had to be discarded because of reactivity against all of the proteins indicating a potential false positive result. the frequency of different combinations of cov-s1 reactive samples is summarized in table 1 . reactivity against eight out of 12 cov s1 antigens could be observed, whereas none of the sera recognized the s1 protein of hcov-hku1, mers-cov, sars-cov and hcov-oc43. different s1 antigens were grouped by amino acid sequence phylogeny (left panel) using mega7. each column of the heat map represents an individual sample, and columns were arranged in a descending order based on elisa-reactivity against feline coronavirus (fcov) type 1. table 1 . numbers of positive cat samples and different combinations of reactivity found. the number of positive sera against each individual s1 is shown in the bottom row. positive elisa reactions are colored in orange. cut-off value was determined as the 5-fold over the od450 of negative sera. fcov type1-s1 fcov type2-s1 pdcov-s1 tgev-s1 229e-s1 bcov-s1 different s1 antigens were grouped by amino acid sequence phylogeny (left panel) using mega7. each column of the heat map represents an individual sample, and columns were arranged in a descending order based on elisa-reactivity against feline coronavirus (fcov) type 1. table 1 . numbers of positive cat samples and different combinations of reactivity found. the number of positive sera against each individual s1 is shown in the bottom row. positive elisa reactions are colored in orange. cut-off value was determined as the 5-fold over the od450 of negative sera. number of cats (total = 137) fcov type1-s1 fcov type2-s1 pedv-s1 pdcov-s1 tgev-s1 229e-s1 nl63-s1 bcov-s1 as expected, many sera were positive for fcov s1, with 75 sera (54.7%) positive for fcov type 1 and 26 sera (19.0%) for fcov type 2 s1 ( figure 1 ). all of the fcov type 2 s1 positive sera also tested positive for fcov type 1 s1, while 15 of 26 fcov type 2 s1 positive sera also reacted with tgev s1. the fcov type 2 s1 and tgev s1 elisa reactivities showed a strong nonparametric spearman correlation (spearman r = 0.84, p < 0.0001). with respect to this, we suggest that the tgev s1 positivity was due to cross-reactivity of fcov type 2 s1, as fcov type 2 shows close antigenic and genetic relationship with tgev (s1 shares 70.4% amino acid sequence identity). the remaining 11 fcov type 2 s1 positive but tgev s1 negative sera do react with fcov type 1 s1. an explanation might be the cross-reactivity between fcov type 1 and type 2. remarkably, 40 feline sera were reactive with s1 proteins from human, porcine and bovine covs (table 1) , including hcov-229e (16/137), hcov-nl63 (2/137), pedv (27/137), pdcov (8/137) and bcov (1/137). od values of feline sera positive for hcov-nl63 s1 and bcov s1 were relatively low ( figure 1a ). elisa reactivity towards non-feline cov s1 proteins might be explained by infection with the respective or related covs or by the presence of cross-reacting antibodies, although there was low sequence identity (< 32.8%) between s1 proteins of fcov type 1 and related non-feline coronaviruses (for the complete comparison of s1 sequence identities, see table 2 ). yet, all of pedv-s1 positive sera were also positive for fcov type 1 s1 ( figure 1b , table 1 ). the elisa results of fcov type 1 s1 and pedv s1 showed a strong nonparametric spearman correlation (spearman r = 0.83, p < 0.0001). thus, this might indicate the occurrence of antibody cross-reactivity against fcov type 1 and pedv s1 antigens. many of the hcov-229e and pdcov s1 positive sera also reacted with fcov type 1 s1, but no strong nonparametric spearman correlation was observed (hcov-229e, r = 0.216; pdcov, r = 0.307). one feline serum only reacted with hcov-229e viruses 2019, 11, 743 7 of 16 s1, and two feline sera only recognized pdcov s1. ( figure 1b , table 1 ). this observation led us to hypothesize that cross-reactivity may not play a role in elisa reactivity of these three sera, but that the three cats had been infected with these viruses or related viruses. 1 fcov type1-s1 (fj938060.1) 2 fcov type2-s1 (ay994055.1) 28.5 3 pedv-s1(aog30832.1) 32.8 30. 2 4 pdcov-s1 (aml40825. in our screening, 43 samples were shown to be positive for two or more s1 proteins including fcov type 1. the data prompted us to test different hypotheses which may explain this phenomenon: specific reaction through natural virus infection or reaction due to cross-reactivity with fcov-s1 antigens. to explore this further, we employed 25 fcov type 1 specific sera derived from specific pathogen free (spf) cats that had been experimentally infected with fcov type i strain rm (n = 9) or strain uu2 (n = 16). these sera were tested for their elisa reactivity against seven cov s1 proteins (excluding tgev s1) that showed positive reactivity in the previous serological screening. as expected, all 25 sera were positive for fcov type 1 s1 in our elisa; interestingly, four samples also reacted with fcov type 2 s1, and five samples with pedv s1. no positive elisa-reactivity was detected with s1 of hcov-229e, pdcov, hcov-nl63 or bcov (table s1 ). thus, fcov type 1 infection could lead to the generation of antibodies that cross-react in the s1-elisa with fcov type 2 and pedv s1 proteins. the elisa cross-reactivity of fcov type 1 specific sera with fcov type 2 s1 antigens prompted us to map the domains responsible for cross-reaction within the s1 subunit. hence, to identify domain borders within s1, we built homology-based models of both fcov type 1 and type 2 spike using the related elucidated hcov-nl63 cryo-em structure as the template model. as shown in figure 2a , continuous structural domains can be identified for the s1 subunit of both spikes, namely s1 0 , and s1 a through s1 d . amino acid sequence identities of these domains between fcov type 1 and type 2 differ, ranging from 22.4% to 57.4% ( figure 2b ). several s1 proteins for both type 1 and type 2 fcov-s1 comprising one or two domains were expressed and purified ( figure 2c ). fcov type 1 specific sera (n = 4 for strain rm and n = 3 for strain uu2) and type 2 (n = 6, strain 79-1146) specific sera were then tested against these proteins in elisa format. the four fcov type 1 specific sera that cross-reacted with s1 of fcov type 2 again showed binding to fcov type 2 s1. but the fcov type 2 specific sera showed little to no reactivity against fcov type 1 s1. as shown in figure 3 , the type specific antisera reacted with all of the homologous s1 domains, with s1 and s1 b of both type 1 and type 2 displaying the strongest reaction. interestingly, the cd domain showed the highest level of cross-reactivity between fcov type 1 and 2, in agreement with its highest sequence identity among s1 domains (figure 3) . the other three domains showed little to no cross-reactivity. antisera reacted with all of the homologous s1 domains, with s1 and s1 b of both type 1 and type 2 displaying the strongest reaction. interestingly, the cd domain showed the highest level of crossreactivity between fcov type 1 and 2, in agreement with its highest sequence identity among s1 domains ( figure 3 ). the other three domains showed little to no cross-reactivity. the s1 subunit of one protomer are colored, with s1 0 shown in cyan, s1 a in blue, s1 b in green, and the domains s1 cd in red. the s2 part of the protomer is marked in light gray. (b) schematic presentation of the fcov type 1 (strain uu2) and type 2 (stain 79-1146) s protein with the signal peptide (sp), the s1 subunit (the domains are colored as described in the legend of figure 2a ) and the s2 subunit (the c-terminal transmembrane domain is indicated by a black box). amino acid sequence identities between fcov type 1 and type 2 s1 domains are indicated. (c) diagram of the different s1 subdomains sequence. all s1 subdomains were c-terminally tagged with the fc part of mouse igg2a (not shown in the figure) and expressed as fc fusion proteins. the s1 subunit of one protomer are colored, with s1 0 shown in cyan, s1 a in blue, s1 b in green, and the domains s1 cd in red. the s2 part of the protomer is marked in light gray. (b) schematic presentation of the fcov type 1 (strain uu2) and type 2 (stain 79-1146) s protein with the signal peptide (sp), the s1 subunit (the domains are colored as described in the legend of figure 2a ) and the s2 subunit (the c-terminal transmembrane domain is indicated by a black box). amino acid sequence identities between fcov type 1 and type 2 s1 domains are indicated. (c) diagram of the different s1 subdomains sequence. all s1 subdomains were c-terminally tagged with the fc part of mouse igg2a (not shown in the figure) and expressed as fc fusion proteins. viruses 2019, 11, x for peer review 9 of 16 figure 3 . elisa-reactivity of fcov specific antisera against different s1 subdomains of fcov type 1 and 2. equimolar amount of purified s1 proteins and the four s1 subdomains were coated onto 96well plates and antibody binding was determined by elisa. the fcov type 1 and 2 specific antisera used in the screening were derived from experimentally infected specific pathogen free (spf) cats and are indicated at the right side of each panel, absorbance values and antigens in use are shown on the y-and x-axis, respectively. graphs represent the mean values from three independently performed experiments. standard deviations are indicated as error bars. because the fcov type 1 specific cat sera also showed elisa reactivity with pedv-s1 (table s1 ), we analyzed the reaction of the five pedv-s1 positive cats in more detail. samples were analyzed via elisa using antigens comprising different pedv-s1 domains, as described in our previous study [40] . cat sera taken pre-and post-fcov infection were collected and tested. as indicated in figure 4 , all five cats had developed pedv-s1 reactivity to different extent after fcov type 1 inoculation. noticeably, all sera showed the highest od values with the cd domain, while the other domains, including the s1 b containing the presumed receptor binding domain (rbd) [40] , were non-reactive ( figure 4 ). on the other hand, the swine pedv positive control serum exhibits strong reactivity against all pedv-s1 domains. the next question we asked was whether fcov type 1 specific sera could neutralize pedv infection in tissue culture, as they showed no reactivity with the s1 b of pedv spike. as shown in figure 5 , pedv neutralizing antibodies were detected in three out of five fcov type i specific cat sera. figure 3 . elisa-reactivity of fcov specific antisera against different s1 subdomains of fcov type 1 and 2. equimolar amount of purified s1 proteins and the four s1 subdomains were coated onto 96-well plates and antibody binding was determined by elisa. the fcov type 1 and 2 specific antisera used in the screening were derived from experimentally infected specific pathogen free (spf) cats and are indicated at the right side of each panel, absorbance values and antigens in use are shown on the y-and x-axis, respectively. graphs represent the mean values from three independently performed experiments. standard deviations are indicated as error bars. because the fcov type 1 specific cat sera also showed elisa reactivity with pedv-s1 (table s1) , we analyzed the reaction of the five pedv-s1 positive cats in more detail. samples were analyzed via elisa using antigens comprising different pedv-s1 domains, as described in our previous study [40] . cat sera taken pre-and post-fcov infection were collected and tested. as indicated in figure 4 , all five cats had developed pedv-s1 reactivity to different extent after fcov type 1 inoculation. noticeably, all sera showed the highest od values with the cd domain, while the other domains, including the s1 b containing the presumed receptor binding domain (rbd) [40] , were non-reactive (figure 4 ). on the other hand, the swine pedv positive control serum exhibits strong reactivity against all pedv-s1 domains. the next question we asked was whether fcov type 1 specific sera could neutralize pedv infection in tissue culture, as they showed no reactivity with the s1 b of pedv spike. as shown in figure 5 , pedv neutralizing antibodies were detected in three out of five fcov type i specific cat sera. the experiment was carried out in duplicate and repeated three times. error bars indicate standard deviations. sera were collected from spf cats prior (cat 91-131p) and after (cat 91-131) experimentally inoculated with fcov type 1. positive serum: pedv positive swine serum collected from the field; negative serum: serum from fcov negative spf cat. several serum samples from field cats, but not virus-specific serum samples from fcov inoculated spf cats, were found to be elisa positive for hcov-229e (n = 16) and pdcov s1 (n = 8) ( figure 1a) . also, a few feline sera displayed unique elisa positivity for s1 of hcov-229e (n = 1) or pdcov (n = 2) ( figure 1b, table 1 ). this could indicate that these antibodies were induced upon infection with these specific viruses. to corroborate the possibility of a natural infection in these cats with hcov-229e or hcov-229e-like viruses, we tested sera neutralization antibody titers. the results showed that one of the hcov-229e s1 reactive feline sera was able to neutralize hcov-229e infection (vnt = 32); no neutralization of pdcov was detected for the all pdcov-s1 positive sera. coronavirus infections are endemic and ubiquitous in feline populations. two viral types, type 1 and 2, are distinguished and both of them could well sustain themselves in the cat reservoir [15, 43] . both have been shown to have worldwide distribution, with the seropositivity rate up to 90% among animal shelter populations and in multi-cat households [20, 44] . the majority of natural infections are caused by type 1 fcovs, while in the field type 2 fcovs are less common and mainly occur in asia [15, 28, [45] [46] [47] . covs are generally considered to be host-specific; however, cross-species transmission does occur which may lead to incidental infections like the spillover of mers-cov from dromedary camel to humans, where humans function as an incidental and ultimately dead-end host [4] . but covs might also adapt to the new host exemplified by the animal origin of all four endemic human covs (hcov-oc43, hcov-nl63, hcov-229e and hcov-hku1) [8] [9] [10] [11] . whereas in cats infections with fcov are well recognized, studies regarding possible natural infections with other animal and human coronaviruses are lacking to the best of our knowledge. knowing the genetic variability of coronaviruses and the use of orthologous receptors by non-feline covs, studies on cross-species transmission are desirable. this may provide insight regarding whether cross-species transmission does occur. in the present study we used the highly immunogenic s1 antigens to screen cat sera for the presence of antibodies against feline and non-feline coronaviruses, as a first indication of possible infections with these viruses. in our study, 78 of the 137 cat sera were shown to be seropositive for coronaviruses. the seropositive rate (54.7%) against s1 of fcov type 1 is consistent with previous studies [15, 47] . all of the fcov type 2 s1 positive sera of naturally infected cats were also positive for fcov type 1 s1, which might be the result of cross reaction between the two proteins, despite their low amino acid identity. elisa with specific antisera from experimentally fcov type 1 and type 2 infected cats showed that sera of several fcov type 1 infected cats could cross-react with fcov type 2 s1. domain mapping elisa results showed that fcov type 1 specific sera react to different levels with the s1 domains of fcov type 1 s1 protein, and also reacts with fcov type 2 s1 cd . vice versa, fcov type 2 specific sera also reacted with s1 cd of fcov type 1. these observations pose a potential two-way cross-reactivity between s1 cd domains. interestingly, in parallel with our findings on feline coronaviruses, we identified a number of samples that were seropositive against the s1 of pedv, a viral pathogen that mainly replicates in the porcine intestinal epithelium. to study the possibility of cross-reaction, samples derived from preand post-fcov infected cats were screened against pedv s1 in elisa. the reactivity found against pedv s1 with fcov specific sera shows that cross-reaction can occur at the level of domain s1 cd ; the other pedv s1 domains showed no reaction with the fcov positive sera. judging from these observations, it seems that s1 cd plays an important role in cross-reaction between fcov type 1 and 2, and also fcov and pedv. as s1 cd is the most conserved domain among fcov and also between fcov and other alphacoronaviruses (for a systematic assessment of sequence identities, see table 3 ), it is reasonable to hypothesize that antibodies can develop against conserved epitopes within this region and subsequently cause cross-reaction. this should be taken into account when developing and interpreting serological assays. table 3 . identities of amino acid sequences of fcov type 1 (strain: uu2) s1 and s1 domains compared with the amino acid sequences of other alphacoronaviruses. (identities are shown in %; na: not available) the genbank accession numbers of these viruses are as follows: fcov type 1 (uu2), fj938060.1; fcov type 1 (rm), fj938051.1; fcov type 2, ay994055.1; tgev, abg89325.1; pedv, aog30832.1; hcov-229e, np_073551.1; hcov-nl63, yp_003767.1. amino acid % identity to fcov type 1(uu2) s1 s1 0 s1 a s1 b s1 cd noticeably, elisa reactivity among cat sera towards the n-terminal fcov s1 domains 0 and a was less consistent and generally lower compared to whole s1, which seems to correlate with the higher antigenic variation in those domains found among fcov type 1 strains [48] (figure 3 ). especially the sera from fcov-rm infected cats (cat 91, 93, 95 and 115) showed lower od values against s1 a . this phenomenon could be explained as the samples displaying higher reactivity were from cats inoculated with fcov-uu2 (cat 089, 131 and 129), the particular strain from which the s1 region was used as an antigen in the elisa studies. in the meantime, the possibility of the variable elisa reactivity might be due to the difference in individual antibody levels. in principle, the distinct antigenic reactivity of s1 0 and s1 a between the two fcov types might facilitate the development of a specific elisa method which allows the serological discrimination of fcov type 1 and type 2 infections in cats. in order to provide further insight regarding cross-reactivity between fcov type 1 and pedv, we performed virus neutralization assays. cross-neutralization of pedv infection could be observed for some of the feline fcov type 1 post-infection sera, in contrast to the pre-infection serum counterparts. since fcov specific pedv neutralizing sera did not react with pedv s1 0 , s1 a or s1 b , it is likely that the cross-neutralizing antibodies are targeting conserved epitopes in the s1 cd domain or the s2 subunit of the pedv spike protein [49] . given the unknown tgev infection background of the pedv positive pigs, the cross-reaction of pedv specific sera against fcov type 1 could not be explored in our study, as tgev positive pig samples would certainly influence the outcome [12, 18, 50] . of note, our findings cannot exclude the possibility that field cats might incidentally get naturally infected with pedv or pedv-like viruses, as there had been one report showing the detection of pedv in one stray cat via pcr assay [51] . it would be interesting to include more sera of cats from pig farms in future studies. considering the fact that cats play an important role in human society and have constant interaction with humans, it is of interest to conduct serological surveys for possible reverse zoonosis of human pathogens. in our study s1 antigens of several human coronaviruses were included and this led us to identify hcov-229e seropositive feline samples in our elisa survey (table 1) ; one serum in particular reacted solely with hcov-229e s1 but not with any other coronavirus. of the hcov-229e s1 reactive feline sera one showed low neutralizing activity against hcov-229e infection. this might suggest that positive cats were indeed exposed to hcov-229e or related viruses. mers seropositivity is also seen in other species besides the dromedary host [52] . rare cases of seropositivity might be considered as spill-over infections from the dromedary camel reservoir. similar (perhaps dead-end) spill-over infections of 229e from the human reservoir to cats might also occur. a similar principle could also apply for pdcov, a porcine pathogen that emerged rather recently. both hcov-229e and pdcov use apn as their receptor and have been reported to also be able to use feline apn for cellular entry [21, 37] . although reports are lacking regarding the natural infection of these two viruses in cats, hcov-229e was shown to cause a priming effect of fcov antibody in experimentally fcov infected cats suggesting that infection occurred [24] . therefore, the detection of antibodies against s1 of hcov-229e in a portion of the cats might be specific and due to the exposure to hcov-229e through daily interaction with humans. eight cats were seropositive for pdcov of which two cats were seropositive only for pdcov and not for any other covs. this could be caused by infection with pdcov or pdcov-related viruses through avian sources, considering the fact that cats are natural avian predators and the presumed avian origin of pdcov [2, 37] . our findings emphasize the potential role of cats as incidental hosts for non-feline coronaviruses and the need of in-depth study of naturally infected pathogens in cats. besides serological studies, efforts should also focus on isolation and identification of these viruses in cats. in conclusion, we presented a thorough serological survey in cats using s1 proteins of different animal and human coronaviruses. we demonstrated, despite the low amino acid identity, cross-reactivity between s1 proteins of fcov type 1 and 2, and between that of fcov type 1 and pedv. this should be considered when developing fcov serological assays as well as interpreting the results. our observation that some feline sera displayed antibody reactivity exclusively against non-feline cov s1 proteins warrant further research into the epidemiology and cross-species transmission of coronaviruses in cats and other animals that are in close contact with humans. further large scale serological studies regarding coronaviruses infection across animal species using arrays of cov s1 antigens can shed light into the hitherto unresolved host promiscuity of coronaviruses and the risk of cross-species transmission. supplementary materials: the following are available online at http://www.mdpi.com/1999-4915/11/8/743/ s1, table s1 : elisa reactivity (od450 values) of 25 fcov type 1 specific antisera against s1 antigens of different coronaviruses. the authors declare no conflict of interest. pre-fusion structure of a human coronavirus spike protein discovery of seven novel mammalian and 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infection in non-camelid domestic mammals this article is an open access article distributed under the terms and conditions of the creative commons attribution (cc by) license key: cord-312955-gs65c3fy authors: schreiber, gideon title: the role of type i interferons in the pathogenesis and treatment of covid-19 date: 2020-09-30 journal: front immunol doi: 10.3389/fimmu.2020.595739 sha: doc_id: 312955 cord_uid: gs65c3fy type i interferons (ifn-i) were first discovered over 60 years ago in a classical experiment by isaacs and lindenman, who showed that ifn-is possess antiviral activity. later, it became one of the first approved protein drugs using heterologous protein expression systems, which allowed its large-scale production. it has been approved, and widely used in a pleiotropy of diseases, including multiple-sclerosis, hepatitis b and c, and some forms of cancer. preliminary clinical data has supported its effectiveness against potential pandemic pathogens such as ebola and sars. still, more efficient and specific drugs have taken its place in treating such diseases. the covid-19 global pandemic has again lifted the status of ifn-is to become one of the more promising drug candidates, with initial clinical trials showing promising results in reducing the severity and duration of the disease. although sars-cov-2 inhibits the production of ifnβ and thus obstructs the innate immune response to this virus, it is sensitive to the antiviral activity of externally administrated ifn-is. in this review i discuss the diverse modes of biological actions of ifn-is and how these are related to biophysical parameters of ifn-i–receptor interaction and cell-type specificity in light of the large variety of binding affinities of the different ifn-i subtypes towards the common interferon receptor. furthermore, i discuss how these may guide the optimized use ifn-is in combatting covid-19. type i interferons (ifn-i) are a family of cytokines that bind the type i interferon receptor, constituted of two transmembrane subunits, ifnar1 and ifnar2 ( figure 1 ). the two receptors are constituted of an extracellular domain, which binds ifn-i, a transmembrane helix and an unstructured intracellular domain (icd) that binds jaks and stats (1, 2) . jak1 is associated with ifnar2 and tyk2 with ifnar1. stat1 and stat2 (and maybe also other stats) were found to be constitutively bound to the icd of ifnar2 (3) (4) (5) . binding results in close proximity of the intracellularly associated jaks, jak1 and tyk2, resulting in their activation through cross phosphorylation ( figure 1 ) (6, 7) . this also results in receptor phosphorylation, which role is still under debate (3, (8) (9) (10) . the phosphorylated stats dissociate from the receptor and form homo and hetero dimers, which are transported to the nucleus, where they serve as transcription factors for a large number of genes. the most prominent effects are associated with stat1/stat2 heterodimerization, which together with irf9 form the interferon-stimulated gene factor 3 (isgf3), which bind a distinct group of target genes harboring the interferonstimulated response elements (isre). in addition to this, ifn-i drives stat1/stat1 and stat3/stat3 homodimerization, the formation of a stat2/irf9 binary complex and more (6, (10) (11) (12) (figure 2 ). this leads to the transcription activation or suppression of over 1,000 genes, which drive a wide range of innate and adaptive immune functions. these, in turn respond against various pathogens, act as important regulators in tumor immunity and have a role in pathophysiology and autoimmune diseases (10, (13) (14) (15) (16) (17) (18) . stat2 knockout cells still activate a stat1/stat1 response mediated by irf1, while stat1 knockout cells activate a stat2/irf9-induced response (10) . surprisingly, no change in the gene induction relative to wildtype cells was observed in stat3 knockout hela cells, despite the strong ifn-i-induced phosphorylation of stat3. however, as ifn-i responses are cell-type specific, a stat3/stat3induced response may still be found in other cells than hela. due to this wide range of physiological responses, ifn-i has provided therapeutic benefits for multiple diseases, including multiple sclerosis, some cancers and viral diseases (hepatitis b and c) (19) (20) (21) . due to the efficient activation of antiviral activities by ifn-is, most viruses have contemplated mechanisms to avoid its actions (22) (23) (24) . for example, the ebola virus, which outbreak in central africa killed tens of thousands of people (25, 26) , avoids ifn-i activity by producing the vp24 protein that binds the karyopherin alpha nuclear transporter. thereby, it inhibits the nuclear transport of phosphorylated stat1, rendering cells refractory to ifn-is. another example of viral mechanisms that evolved to eliminate ifn-i functions in inducing innate immunity is given by the sars corona virus, where both the production of ifnb and the ifn-i induced signaling are attenuated. recently, a more infective version of sars has emerged, sars-cov-2 (which causes the covid-19 disease). covid-19 cases have been first reported by the end of 2019 in china, and rapidly became a world-wide epidemic with unprecedented consequences (27, 28) . sars-cov-2 seems to have originated from horseshoe bats. similar virus strains that circulate in bats in hubei province in china may in the future cause further new zoonotic outbreaks (29) . sars-cov-2 has 83% homology to the sars-cov virus that also spread from china in 2002 (30) . sars-cov-2 proved to be much more infectious compared to the original sars virus, resulting in a global epidemic. as ifn-i drives strong antiviral activities, the mechanisms sars-cov and sars-cov-2 combat ifn-i activities has been a matter of intense research, with at least 6 proteins being identified to counteract ifn-i functions in the sars-cov virus (31) . in addition, ifn-is were implicated in contributing to the severity of the cytokine storm, which is a major complication of sars-cov and sars-cov-2 and can lead to respiratory distress syndrome (ards) and death (31, 32) . in this review i will describe our current knowledge on the involvement of ifn-is in the development of the covid-19 disease, and how this relates to the different activities associated with type i interferons. type i interferon receptors are found on all cell types, and are a major component of the innate immune system. human type i interferons include 13 similar ifnas with 80% homology between them and single ifnw, k, ϵ and b, with lower homology (30-50%). all of them bind the receptor complex, composed of ifnar1 and ifnar2 at the same proximal location (1, 2, 33) . despite structural similarities among the ternary ifn-i-ifnar1-ifnar2 complexes, ifn-is drive a range of different activities, dependent on the cell type and the interferon subtype (34) . this apparent paradox has major implications for understanding the role of ifn-i in health and disease and its varied applications as a drug against a pleiotropy of diseases. ifn-i signaling is initiated by binding of ifn-i to its receptor. it has been suggested that cytokine receptors are pre-associated, with ligand binding activating signaling through the induction of conformational changes (35) . however, more recent singlemolecule receptor tracking on life cells has clearly shown that for many of the cytokines, its role is to bring the receptors into close proximity, which drives signaling (36) . this seems to be the case also for ifn-i induction, as shown both using single receptor tracking and mutational analysis ( figure 1 ) (37, 38) . while structurally, the ternary ligand-receptor complex seems to be the same for all ifn-is, the binding affinity differs by many orders of magnitude. the tightest binding ifn-i is ifnb, which binds ifnar1 with 100 nm affinity and ifnar2 with subnanomolar affinity. the different ifna subtypes bind ifnar1 with 0.5 to 5 µm affinity and ifnar2 with 1 to 100 nm affinity, with ifna1 being the weakest binding ifna (39, 40) . even weaker binding was measured for ifnϵ, with~100-fold reduced affinity relative to ifna proteins (15) . interestingly, ifnϵ is constitutively expressed by the reproductive tract epithelium and is regulated by hormones during the estrus cycle, reproduction, menopause and by exogenous hormones. thus, its mode of action is different from other ifn-is (41) . these large differences in binding affinity between ifn-i subtypes were suggested to result in major differences in biological activity. to obtain a better insight into the molecular mechanisms of their actions, ifna2 was engineered to cover the whole range of binding affinities of natural ifn-is to both the high affinity (ifnar2) and low affinity (ifnar1) receptor chains (1) . these studies have shown that indeed, the binding affinity to both receptors is a major determinant of ifn-i activity (42) . using both natural and engineered ifn-is has shown that even weak binding ifn-is activate the cellular antiviral program at very low (pm) concentrations (39) . moreover, the antiviral program was activated in all cell-lines tested. despite the 50-fold higher affinity of ifnb over ifna2 towards binding ifnar receptors, its potency to elicit an antiviral response is similar. for example, in wish cells (originally thought to be of amniotic origin, but later found to be a hela (cervix cancer) contaminant) the ec 50 for antiviral activity of ifna2 is 0.3 pm, while the ec 50 for ifnb is 0.15 pm (43) . wish cells have been extensively used to characterize ifn-i activity, including for definition of ifn-i unit activity. an upper limit for antiviral potency was further verified by engineering an ifna2 variant, yns-a8-tail, with 50fold tighter binding to ifnar1 and 15-fold tighter binding to ifnar2 in comparison to ifna2 (thereby surpassing the receptor binding affinity of natural ifnb). still, the ec 50 for antiviral activity is only 3-fold lower in comparison to ifna2 (44, 45) . conversely to antiviral activity, ifnb is much more potent in activating the antiproliferative program relative to ifna2, a result that was also verified using the ifna2 variant, yns-a8tail (45) . the ec 50 for antiproliferative activity on wish cells is 2 nm for ifna2, 50 pm for ifnb and 20 pm for yns-a8-tail. a similar increase in antiproliferative potency was observed also for ovcar3 and hela cells. interestingly, while antiviral activity was observed in all cell lines tested, some cell lines were not susceptible to ifn-i induced antiproliferative activity (for example t47d and k562), independent on the concentration and subtype of ifn-i (45) . to better understand the molecular basis for this finding, ifn-i induced gene expression was monitored using various ifn-i subtypes or engineered mutants on the background of different cell-lines. these experiments showed that low concentrations of weaker binding interferons activate the expression of mostly antiviral genes. higher concentrations of interferons activate also other genes, many of them related to immune-modulation (45) . examples for such genes are chemokines such as cxcl10 and 11, which are involved in chemotaxis of t cells and natural killer cells, induction of apoptosis, regulation of cell growth and more. we gave the term of "robust" for the common ifn-i induced program (including its antiviral activity) and "tunable" for the other programs induced by ifn-is, which include between others antiproliferative and immunomodulatory activities (34) . further investigations into these two programs has shown that cells with low receptor numbers activate only the robust program, and that not all cell types execute the tunable program, conversely to the robust program that is common to all cells (46) . tighter binding ifn-is at higher concentrations are essential for the activation of the tunable program. genes upregulated by the robust program are mostly classical antiviral genes, such as mx1 and mx2, oas1 and 2, pkr, ifit1, 2 and 3, isg15, and many more. figure 3a according to string and go analysis, the commonly upregulated genes have a strong antiviral signature. the top go terms (fdr <10 −25 ) are response to type i interferon, innate immune response, response to virus, defense response and immune system process. it is interesting to note that antiviral genes constitute most of the upregulated genes common to all 4 cell lines. antiviral genes are also the majority of upregulated genes in k562 and t47d cells. conversely, ovcar3 and hela cells have many unique upregulated genes, many of them related to immunomodulatory functions, cell cycle, apoptosys and more. ifn-i. the diagram shows that 53 genes are commonly upregulated by all 4 cell-lines. figure 3b shows string protein interaction analysis of these common genes. clearly, these form a tightly interacting mesh of gene products. gene ontology analysis shows these genes to have an extremely high signature for antiviral activity and ifn-i activation. promoter analysis of common isgs has shown them to be driven by the classical isre promoter sequence (45) . conversely, for tunable genes no clear promoter sequence was identified. the exact mechanism of how tunable genes are upregulated by ifn-i is thus not yet fully understood. from an immunological point of view, ifn-is have three major functions: 1. to activate an antiviral state in infected and neighboring cells that limits spread of infection. 2. modulate innate immune responses, including antigen presentation and natural killer cell functions while restraining pro-inflammatory pathways. 3. activating the adaptive immune system for the development of high-affinity antigen-specific t and b cell responses (47) . as ifn-is are highly active molecules, their expression and signaling potency is highly regulated. opposing augmenting and suppressive signals are induced by host factors. suppressive pathways include ifn-i activation of usp18, an isg that suppresses signal transduction by reducing the ability of ifn-is to form an active receptor complex (38, 48) . a second inhibitory mechanism is the induction of socs1 and socs3, which kir domain block the substrate binding groove on jak, thereby inhibiting stat phosphorylation (49) . a third mechanism is by rapid endocytosis and subsequent lysosomal degradation of activated ifnar complexes (50, 51) resulting in reduced receptor numbers ( figure 1 ). it has been demonstrated that a mutant in ifnar1 (s535a and s526a in human and mouse respectively), which fails in ifnar1 endocytosis through blocking its ubiquitination result in high incidence of inflammation (51, 52) . at the transcriptional level, ifn-i response can also be regulated by mir-155, which is highly induced by pattern recognition receptors and inflammatory signaling, and suppresses the expression of over 100 genes. between them genes related to the interferon pathway. it was shown that mir-155-deficient cd8(+) t cells had enhanced type i interferon signaling and were more susceptible to interferon's antiproliferative effect (53) . high basal ifn-i levels are implicated in various immunological diseases, such as systemic lupus erythematosus and more (18, 54, 55) . however, ifn-i has also anti-inflammatory effects, as best demonstrated by their ability to suppress multiple-sclerosis (56) . it is important to note that beneficial results in treating multiplesclerosis were observed only for ifnb but not for ifna treatment (56) . to see whether this relates to the higher receptor binding affinity of ifnb, we established a transgenic mouse harboring the human interferon-receptors extracellular domains fussed to the mouse intracellular domains and compared the severity of eae in a mice model upon treatment with ifna2, ifnb and the high-affinity engineered ifn-yns-a8-tail. we found that the ifn-yns-a8-tail had the strongest suppressive effect on the development of eae (57) . the effect was further enhanced by pasylation of ifn-yns-a8-tail, which extends it plasma half-life by 10-fold. interestingly, we found a tight relation between the increased levels of expression of pd-l1 in mice and the severity of the disease. these data show that tight binding ifn-is induce preferential anti-inflammatory responses, at least in this ms mouse model. another example for the immunosuppressive activity of ifn-i was shown for lcmv infection, which induces consistent ifn-i production including the immunosuppressive factors il-10 and pd-l1 (58) . in addition to the above, interferons contribute to inflammasome activation through several different mechanisms, including caspase-11 expression and the ifn-i inducible gbp protein expression, which was reported to have an important role in caspase-11 activation and pyroptotic cell death (59) . ifn-is have important roles in protecting the lung from spread of respiratory viruses. in addition to their direct role, ifn-is have also been found to be critical in initiating lung inflammatory responses, by inducing recruitment and activation of immune responses, which have to be kept under control. ifn-is have been shown to result in the production of chemokines such as ccl2 and cxcl10, which play important roles in the recruitment of monocytes/macrophages, t cells, nk cells, and dcs, therefore directly influencing inflammation in the lung (60) . this varied effect of type i ifns on t cells is partly dependent on the different stats induced by type i ifns. in the absence of ifn-is, the detection of accumulating viral rna and downstream processing of the signal is compromised, leading to viral spread and also to reduced inflammation in the lung. interestingly, there is an age-related reduction of ifn-i production and isg induction after viral infection, which may be related to the higher susceptibility of elderly population to lung infections (61). viruses have developed many strategies to interfere with the synthesis of ifn-is or the ifn-i induced responses. one of them, is the stimulation of turnover of the interferon receptors. among other viruses implicated in accelerating the turnover of ifnar1 are ebv, herpes simplex virus, hepatitis c and b viruses, vesicular stomatitis virus and the sars coronavirus (62, 63) . sars-cov has been shown to suppress ifn-i responses in the host through multiple mechanisms. a subdued ifn-i response diminishes antigen presentation and reduces the antiviral adaptive th-1 immune response. ifn-is communicate between cells against pathogens and have a critical role in the immune system, such as activating natural killer (nk) cells and macrophages. in addition, ifn-is cause flu-like symptoms, which are observed in various diseases. these symptoms may have a role in alerting a person of his/her sickness, in order to limit disease-spread to other individuals. in sars-cov and mers-cov, the induction of ifnb is suppressed altogether. this dampening approach is highly associated with the disease severity and increased mortality (64) . in the lethal cases of sars-cov or mers-cov infections, the increased influx of inflammatory cells is always observed. in a mouse model of sars-cov infection, imbalance in ifn-i and inflammatory cells were shown as the main cause of fatal pneumonia (65) . in addition to these, sars-cov implements strategies to evade the immune response by antagonizing ifn-i induced signaling pathways. the orf6 protein blocks the expression of stat1activated genes (66) . sars-cov and mers-cov encode papainlike protease (plp) that is able to impede the immune response function (67) . in addition, sars-cov interacts with isg15 and antagonizes the ifn-i-mediated antiviral response (68) . the mers-cov orf4b antagonizes the antiviral ifnb production by inhibiting irf3 and irf7 (69) . also sars-cov inhibits activation of irf3/7, slowing ifnb production upon infection (70) . while irf3 is expressed in many different cell types, plasmacytoid dendritic cells are the only cells constitutively expressing irf7 (47) . ifn-i treatment has been studied against mers-cov and sars-cov in numerous experiments, both in vitro and in vivo, and in combination or not with lopinavir/ritonavir, ribavirin, remdesivir, corticosteroids, or ifng. while ifna and b were efficient in vitro and in certain animal models, their success in humans was less convincing [for review see, (71, 72) ]. it should be noted that reduction in ards mortality (not related to sars) was also found to be at best marginal upon treatment with ifn-i (73) . still, one has to consider that mice studies have shown the timing of ifn-i administration to be critical, with positive effects being observed if ifn-i was administered shortly after infection. conversely, ifn-i failed to inhibit viral replication and resulted in unwanted side-effects when administered later in the disease circle (74, 75) . these include elevated lung cytokine/chemokine levels, vascular leakage, and impaired virus-specific t cell responses. it is interesting to note that a knockout of the ifn-i receptor in mice resulted in its protection from lethal sars-cov infection. these findings have major implications on how to treat humans against sars and mers, and could have affected the outcome of the clinical studies. the covid-19 pandemic started in december 2019 in wuhan, china. by the summer of 2020, thirty million cases were reported worldwide, with over 900,000 fatalities. as covid-19 is closely related to the sars-cov virus, the interest in the effect of interferons on its disease progression, and its potential as a drug was immediate. disease progression of covid-19 goes through a number of stages. the initial stage, which last from 2 to 14 days (usually 5-6 days) from infection is asymptomatic. a certain proportion of patients never produce any symptoms (the percentage of those is under debate, but a range of 30-50% is most likely). of those who develop symptoms, they are mostly mild (80% of those who develop symptoms). from the remaining 20%, about half will develop severe symptoms, which require hospitalization in intensive care units. the mortality rate, from those developing symptoms is 2% to 5%. the numbers given above are average, and change dramatically with age. at young age most of the infected people will be asymptomatic, while over the age of 70 about 80% will have symptoms. moreover, as the age progresses, symptom severity increases (76) . the major complication of severe infection is pneumonia, which can develop into acute respiratory distress syndrome (ards). in addition, covid-19 has been linked to cardiovascular sequelae, such as myocardial injury, arrhythmias, cardiomyopathy and heart failure, acute kidney injury, neurological complications, and acute ischemic stroke (28) . developing severe symptoms and death is strongly related to background conditions. the strongest relation is to age, with the risk to people under 50 being very small, while the risk peaks for people over the age of 75. in addition, chronic kidney disease, chronic obstructive pulmonary disease, immunocompromised state, obesity, heart conditions and type 2 diabetes are linked to higher incidents of sever disease (76) . cov-2 is presumed to infect people mostly though inhalation of viral particles, which can be airborne, in droplets or otherwise through infection through touching infected surfaces. the spike protein on the cov-2 surface binds to the human ace2 protein, which serves as its receptor ( figure 4) . the homotrimeric spike glycoprotein is made from s1 and s2 subunits. its binding and subsequent cleavage by the host protease tmprss2 results in the fusion between cell and viral membranes and cell entry (77) . blocking the ace2 receptors by specific antibodies voids viral entry (77) (78) (79) . interestingly, cov-2 receptor-binding domain (rbd) exhibited significantly higher binding affinity to ace2 than the sars-cov rbd, which was speculated to relate to the higher infectivity of covid-19 in relation to sars. after membrane fusion, the virus enters through the endosomal pathway and the viral rna is released into the host cell. the viral rna is then translated into viral polyproteins, which are cleaved into small products by viral proteases (papain-like protease [plpro] and the main protease [mpro]). viral proteins and genome rna are subsequently assembled into virions in the er and golgi and then transported and released out of the cell. the exact mechanism of viral self-assembly is still under intense investigation (80, 81) . investigating ace2 and the viral entry-associated protease tmprss2 expression levels in lung tissue and trachea has shown that tmprss2 is expressed in both tissues, while ace2 is predominantly expressed in a transient secretory cell type (82) . in addition, ace2 and tmprss2 co-expressing cells were found within lung type ii alveolar cells (which also release pulmonary surfactant), enterocytes, and nasal goblet secretory cells (83) . using single-cell rna-sequencing, ace2 and tmprss2 were found to be highly expressed also in the nasal goblet and ciliated cells (84) . the inhaled virus likely binds to epithelial cells in the nasal cavity and starts replicating. the virus propagates and migrates down the respiratory tract along the conducting airways, and a more robust innate immune response is triggered. for about 80% of the infected patients, the disease will be mild and mostly restricted to the upper and conducting airways. unfortunately, about 20% of the infected patients will progress to more severe disease and will develop pulmonary infiltrates and some of them will develop ards (85). like many other viruses, also sars-cov and sars-cov-2 have evolved mechanisms to reduce their exposure to ifn-i. in both viruses, mechanisms to block the production of ifnb were identified. while the antiviral potency of ifn-is on sars-cov is moderate, sars-cov-2 seems to be highly sensitive to ifn-i. this is evident by the significant reduction in viral replication observed following ifn-i treatment at both 24 and 48 h postinfection (86) . in sars-cov-2-infected cells, ifn-i results in elevated stat1 levels and isg production (in contrast to sars-cov infected cells). this raises the question of why the innate immune system fails to combat sars-cov-2? the apparent answer to this is in the inhibition of ifnb production by proteins of the sars-cov-2 virus. within cells, rna viruses are sensed by the innate immune system through three major classes of pattern recognition receptors (prrs): toll-like receptors (i.e. tlr-3, -7, -8), rig-i-like receptors (rlrs), and nod-like receptors (nlrs) (87) . to identify the molecular mechanisms that block ifnb production through activation of irf3/7, several research groups transfected cells individually with all the cov-2 viral genes and with either rig i, mda5, or mavs (88, 89) . among the 27 cov-2 proteins transfected to cells, they identified nsp14 and orf6 as competent suppressors of ifnb. yuen et al. also identified nsp13 and 15, while lei et al. identified nsp1, nsp12 and the m protein as potent inhibitors of the mavs pathway, leading to inhibition of ifnb production ( figure 4) . orf6 was between the strongest suppressors of ifnb production in both studies. orf6 was also the only sars-cov-2 gene suppressing the activity of an interferon-stimulated response element (isre) promoter in both studies. lei et al. also identified nsp1 and nsp14 as potent inhibitors of the induction of an isre promotor. in another study, li et al. showed that the viral orf6, orf8, and nucleocapsid proteins were strong inhibitors of ifnb production, and through this of the ifn-i innate immune response (90) . in this study, orf6 and orf8 also inhibited induction of transcription an isre promotor driving a luciferase as reporter, following ifnb treatment. in addition to the above-mentioned sars-cov-2 genes, orf3b was implicated by konno et al. as being a potent antagonist towards ifn-i production (91) . an interesting civet in this study is the finding that a natural variant, with a longer orf3b reading frame increased disease severity in two patients. in light of the much higher than expected coding capacity of the sars-cov-2 genome, where many more proteins than genes were identified (92), we may find even more proteins and peptides being involved in eliminating the innate immune response, including through inhibition of ifn-i activities. another mechanism by which sars-cov-2 inhibit antiviral functions of the cell is thought the activity of the papain-like protease (plpro), which is essential for viral polyprotein processing. this gene was found to preferentially cleave the ubiquitin-like modifier interferon-stimulated gene 15 (isg15), figure 4 | sars-cov-2 has multiple effects on the immune system, including inhibition of ifnb production, which results in isgs not to be produced, cd4+ and cd8+ exhaustion and increased levels of pro-inflammatory proteins (tnfa, il6, nf-kb). currently, the most promising drugs against covid-19 include ifn-is, antiinflammatory and antiviral drugs, protease inhibitors, antibodies, sars-cov2 -ace2 (receptor) binding inhibitors and more. which is an ifn-i induced gene with strong antiviral activity (93) . this represents another layer of attenuation of ifn-i responses by sars-cov-2 and is similar to the mechanism previously identified for sars-cov (68) . inhibition of ifnb production by cov-2 got further confirmation from measuring the levels of different cytokines in sars-cov-2-infected patients. an integrated immune analysis, including immune cell analysis, whole-blood transcriptomics and cytokine quantification on covid-19 patients at 8 to 12 days after disease onset has shown an impaired ifn-i response that is a result of low ifn-i levels (94) . this, in turn results in the low production of interferon-stimulated genes. conversely, high levels of il6 and tnfa were measured ( figure 4) (95, 96) . this is in contrast to what is seen in patients infected with highly pathogenic influenza viruses. the high production of pro-inflammatory cytokines and low production of ifn-is during sars-cov-2 infection suggests effective activation of nf-kb but not irf3 and irf7 (95) . impaired ifn-i production during severe covid-19 may also lead to an imbalance in the pro-inflammatory versus pro-repair functions of airway macrophages. this was indeed seen in severely ill patients with covid-19. other innate immune cells such as natural killer (nk) cells are also regulated by ifn-is during coronavirus infection. severe covid-19 is associated with exhaustion of cd4+ and cd8+ t cells (97) , which may be a result of deficient ifn-i production, as ifn-is promote survival of t cells. an important issue to consider is that early production of ifn-is promote efficient t cell responses, while a delayed response may inhibit t cell proliferation or their exit from lymphoid organs and thus cause their functional exhaustion. indeed, t reg cell counts in covid-19 patients inversely correlate with disease severity (98, 99) . interestingly, transcriptomic analysis of blood, lung, and airways of cov-2-infected patients showed that while ifnb was indeed not highly expressed in either, a number of ifnas were highly upregulated in the lung and airways but not in blood (100) . moreover, a clear ifn-i-induced gene expression profile was also detected for lung and airways, but not for blood (pbmcs). a similar finding of elevated ifna but not ifnb, during covid-19 infection was also found by wei et al. (101) . in this study, the elevated ifn-i response was restricted to the stage in the disease were patients were in intensive care. in another study of 26 patients, of whom 5 did not produce ifn-i, those patients had higher viral load, required more aggressive medical intervention and their time of stay in the intensive care unit was longer that ifn-i producing patients (102) . pdcs are the most rapid and abundant ifn-i producers. pdcs express tlr7 and tlr9 which are important in sensing viruses. the response of pdcs to viruses, particularly ifn-i production, is significantly impaired with ageing while secretion of all other pro-inflammatory cytokines was comparable to that of younger individuals (103) . this may relate to the master regulator for ifn-i production, irf7, which expression, phosphorylation and nuclear translocation decreases with age. in addition, local neutrophil-mediated inflammation is increased with age, while cytotoxicity of nk cells induced by type i ifn-is decreases in aged mice (104) . in addition to age, other factors were also associated with reduced interferon responses. one of them is obesity, which is related to impaired ifna and ifnb responses, which may relate to inadequate response of obese people against viral infections (105) . clinical trials of using ifn-i for treating corona viruses has a long history. already in 1983, intranasal human ifna2 was given both before and after corona virus challenge, a strain that is causing common cold. the incidence of colds, the severity of symptoms and signs, and virus replication were all reduced in subjects receiving interferon as compared with those given placebo (106) . for sars-cov, no randomized placebo-controlled trials have been performed to test the efficacy of ifn-is, however, comparing the clinical outcome of patients treated with ifn-a (infacon-1) with patients at different locations (not a control group) that were not treated, has suggested clinical benefits (107) . these studies have raised the hope that ifn-i may be a potent drug also against covid-19. this hope was further exuberated by the observation that externally administrated ifn-i induced a strong antiviral response, much more than that observed for sars-cov (86) . while some of the sars-cov-2 proteins may affect isg production (most notably, orf6 and 8, see above), the main defense of sars-cov-2 against ifn-i innate immunity seems to be the prevention of ifnb production, which can be substituted by external administration. a major problem in assessing the efficiency of ifn-i against covid-19 is the lack of a good small animal model. while such models are now under development, they are still not perfect. in a recent study, mice were infected with a replication-deficient adenovirus containing human ace2, and then infected with sars-cov-2. these mice developed pneumonia, severe pulmonary pathology, and high-titer virus replication in lungs. to test the role of ifn-i in disease development, ifnar1 ko mice were infected with sars-cov-2, showing higher viral titer over time. next, the mice were treated prior to infection with poly i:c, a strong inducer of ifn-i. this resulted in significantly diminished clinical disease and induced more rapid virus clearance (108) . these results suggest that at least in a mice model, ifn-i may benefit disease recovery. due to the lack of a good animal model, and the availability of clinically approved ifn-i therapies, multiple clinical studies have been conducted administrating different subtypes of ifn-is using different routes of administration (for summary see table 1 ). in a preventive study, nasal drops of ifna1 were given to 2,944 healthy medical staff in shiyan city hospital, hubei province for 28 days to prevent sars-cov-2 infections. none of them developed serious side effects or was infected with cov-2. while the study lacked a control group from the same city, overall in hubei province 3,387 medical staff were diagnosed with covid-19 (109) . the study thus gives an indication that ifn-i may help in preventing infection for high risk medical personal. to test the benefit of subcutaneous injection of ifnb on early stage patients, an open clinical trial was conducted with 127 patients, 86 were assigned to the combination of lopinavir, ritonavir, ribavirin, and three doses of 8 million international units of ifnb, while the control group of 41 patients were given all the above except ifnb. the median number of days from symptom onset to start of study treatment was 5 days. patients given also ifnb had a significantly shorter median time from the start of treatment to negative nasopharyngeal swab (5-11 days) in comparison to the control group (8-15 days) . moreover, ifnb reduced viral load and number of significantly ill patients relative to the control group, this without significant side-effects (110) . in a medical study on the effects of treatment with ifna2b in a cohort of confirmed covid-19 patients, some of the 77 participants were given nebulized ifna2b with or without arbidol while others were given only arbidol. treatment with ifna2b with or without arbidol reduced the duration of detectable virus in the upper respiratory tract and reduced duration of elevated blood levels of il6 and c-reactive protein, which are inflammatory markers (111) . while the study did not include a standard care group, and all patients recovered, it still provides an indication of ifn-i efficiency. the efficiency of ifnb1a subcutaneously injected three times weekly for 2 weeks for treatment of severe covid-19 was tested in a randomized clinical trial. all the patients (including the control group) received standard of care, including a range of other medicines (hydroxychloroquine, antibiotics, antiviral medicine and more). while the clinical response was not significantly different between the ifnb1 and the control groups, the 28-day overall mortality was significantly lower (19% vs. 44%) in the ifnb1 treated group (112) . in a retrospective study of patients receiving ifna2 through inhalation, alone or in combination with other drugs at a relative early versus late stage of the infection, it was found that those receiving ifna2 at an early stage had a significantly lower rate of mortality. in contrast, late interferon therapy increased mortality and delayed recovery (113) . the study suggests a relation between the time of ifn-i treatment and its efficiency. synairgen, a uk-based company, performed a controlled clinical trial of inhaled ifnb on 221 patients and reported that compared with placebo the odds of developing severe disease during the treatment period decreased by 79% for hospitalized patients receiving sng001, and that patients who received sng001 were more than twice as likely to recover from the virus during the treatment period versus those randomized to placebo. these are between the best results achieved so far in curing covid-19. more clinical trials are now under way to evaluate ifn-i efficiency, but clearly the initial trials have been encouraging. moreover, due to the many years of experience in treating patients with ifn-is, the availability of the drug and its relatively modest cost make it an excellent candidate for mass treatment, once approved. however, critical questions remain concerning the use of ifn-is for covid-19 and other diseases ( figure 4) . these questions relate to the optimal ifn-i subtype, drug-concentration, duration of treatment, mode of treatment and at which frequency should it be given. ample experience exists with subcutaneously administration, which is almost the only route ifn-is were used in the clinic. here, non-modified ifn-is are usually administrated two to three times weekly, while pegylated ifn-is are administrated once per week or less. injection of ifn-is will result in a systemic response, where ifn-is were shown to have antiviral functions as well as pro and anti-inflammatory functions. contrary, if given by inhalation, it will directly target the epithelial, and thus replace the ifnb, which production is inhibited by the virus. administration as nasal drops of ifna may be an excellent prophylactic method for people at high risk. ideally, these questions could be answered using animal models. the problem is that the disease in those is not equivalent to that observed in humans. due to the severity of the disease and the high proven safety of ifn-is, more clinical trials on humans, testing the many open questions related to its best mode of administration may be the fastest way forwards. the subtype to use is another important question. for multiple-sclerosis, ifnb has been used for many years (114) , as it seems to provide a better anti-inflammatory response than ifnas. this may relate to its higher binding affinity to the interferon receptors, as has been demonstrated using a tight binding ifna mutant (yns-a8 tail), which binding affinity even surpasses that of ifnb [see above (57) ]. for combating viral disease, most notable hepatitis c, ifna2 has been most commonly used (115) , which was later replaced by pegylated (long plasma half-life) ifna2 (116) . also, for cancers ifnas were mostly used (117) . a good clinical explanation of why specific ifn-i subtypes were used is often missing, and decisions of which interferon to use may often relate to availability rather than to efficacy. moreover, due to the specie specificity of ifn-is, one cannot deduce from mouse experiments, which ifn-i to use in humans, as the data are not transferable (57, 118) . the main difference between ifnas and ifnb is that the later has a stronger potency to induce antiproliferative and immunomodulatory responses (tunable), while ifna will provide a cleaner antiviral response (robust) without the additional responses associated with ifnb. the open question is which is desired for covid-19 treatment, where complications arise from the exuberated immune response. another, important parameter is the time of intervention by ifn-i, in early or late-stage covid-19 disease. in a recent study in mice it has been shown that prolonged ifn-i and iii signaling interferes with lung repair during influenza recovery, probably through p53 induction, which reduces epithelial proliferation and healing, while early treatment protects mice (119) . in sars-cov-2 this is further complicated by the "cytokine-storm" symptoms of severe covid-19, as indicated by elevated il6 and tnf-alpha levels. whether ifn-administration, particularly ifnb suppresses or exacerbate the sars-cov-2 cytokine storm needs to be urgently determined, as to provide a guide for future application of ifn-i therapy in sars-cov-2 treatment. the author confirms being the sole contributor of this work and has approved it for publication. structural linkage between ligand discrimination and receptor activation by type i interferons structural and dynamic determinants of type i interferon receptor assembly and their 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of hepatitis c biological properties of recombinant alpha-interferons: 40th anniversary of the discovery of interferons bridging the species divide: transgenic mice humanized for type-i interferon response type i and iii interferons disrupt lung epithelial repair during recovery from viral infection the author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.copyright © 2020 schreiber. this is an open-access article distributed under the terms of the creative commons attribution license (cc by). the use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. no use, distribution or reproduction is permitted which does not comply with these terms. key: cord-311332-n8tvglif authors: kostoff, ronald n. title: literature-related discovery: potential treatments and preventatives for sars() date: 2011-04-20 journal: technol forecast soc change doi: 10.1016/j.techfore.2011.03.022 sha: doc_id: 311332 cord_uid: n8tvglif literature-related discovery (lrd) is the linking of two or more previously disjoint concepts in order to produce novel, interesting, plausible, and intelligible connections (i.e., potential discovery). lrd has been used to identify potential treatments or preventative actions for challenging medical problems, among myriad other applications. severe acute respiratory syndrome (sars) was the first pandemic of the 21st century. sars was eventually controlled through increased hygienic measures (e.g., face mask protection, frequent hand washing, living quarter disinfection), travel restrictions, and quarantine. according to recent reviews of sars, none of the drugs that were used during the pandemic worked. for the present paper, sars was selected as the first application of lrd to an infectious disease. the main goal of this research was to identify non-drug non-surgical treatments that would 1) prevent the occurrence, or 2) reduce the progression rate, or 3) stop/reverse the progression of sars. the mesh taxonomy of medline was used to restrict potential discoveries to selected semantic classes, and to identify potential discoveries efficiently. to enhance the volume of potential discovery, databases were used in addition to medline. these included the science citation index (sci) and, in contrast to previous work, a full text database. because of the richness of the full text, ‘surgical’ queries were developed that targeted the exact types of potential discovery of interest while eliminating clutter more efficiently. literature-related discovery (lrd) is the linking of two or more previously disjoint concepts in order to produce novel, interesting, plausible, and intelligible connections (i.e., potential discovery). the open discovery systems (ods) component of lrd starts with an unsolved problem, and generates solutions to that problem through potential discovery. ods lrd has been used to identify potential treatments or preventative actions for challenging medical problems, among myriad other applications. the closed discovery systems (cds) component of lrd starts with an unsolved problem and a potential solution, and generates potential mechanisms that link the solution to the problem. ods is the only approach that will be used for the present study. two points should be emphasized before proceeding further. first, linking of disjoint literatures is a necessary but not sufficient condition for discovery. there needs to be value-added in the novel concept(s) that results. second, while the term 'potential discovery' is used in this paper and throughout the lrd literature, 'hypothesis' is more accurate. what results from these lrd 'discovery' studies are hypotheses that have to be tested in the laboratory/field before they can be properly termed 'discoveries'. e-mail address: ronald.kostoff@pubpolicy.gatech.edu. 1 the mitre corporation (retired). a 2009 review paper by the author showed that, while a number of lrd published papers claimed to have generated potential discovery, essentially none of these claims could be validated [1] . the only published lrd potential discovery claims that could be validated as credible hypotheses were in a journal special issue devoted to lrd (e.g., [2, 3] ). the four medical papers in this special issue describe the application of ods lrd to four chronic diseases: raynaud's phenomenon (rp), cataracts, parkinson's disease (pd), and multiple sclerosis (ms). the present paper presents a comprehensive approach to systematic acceleration of potential discovery and innovation, and demonstrates the generation of large amounts of potential discovery for prevention/treatment of an infectious disease: severe acute respiratory syndrome (sars). the general issues of potential discovery and innovation in the lrd context are discussed in the first paper of the special issue [4] , and the general methodology for this discovery approach was shown in the second paper of the special issue [5] . the sars biomedical background has been published in a detailed review article, and the interested reader is referred to that article [6] . the present paper provides an overview of the etiology and challenges of sars, then presents a retrieval and analysis of the core sars literature and literatures related directly to the core sars literature (e.g., immune system component literatures). these related literatures might contain the seeds of potential discovery (treatments and preventive measures) for sars, and some examples of potential discovery are presented. in contrast to previous work, this paper includes full text analysis for the related literatures. this provided a substantial increase in the volume of potential discovery retrieved. also, examples of interesting but non-discovery (i.e., potential innovation) concepts from the core sars literature are presented, since they have practical value in their own right. the four previous medical papers in the lrd special issue also included potential discovery from indirectly-related literatures. the indirectly-related literatures for the present infectious disease proof-of-principle demonstration were not examined. the amount of potential discovery retrieved from the directly related literature alone (including the full text directly related literature) is voluminous. a major challenge is to select those combinations of potential discoveries that provide the maximum synergy. until these potential discoveries have been exploited, there is little practical need of going to indirectly related literatures to search for yet more potential discovery. in the practical situation, even the potential innovation as defined above has not been exploited, and accelerating these potential innovations should be the first order of business [55] [56] [57] [58] [59] . sars is a contagious disease that resulted in the hospitalization of about 8000 people world-wide in 2002-2003, and resulted in the deaths of about 800 people. according to the author's interpretation of reviews of the pandemic, none of the drugs worked (e.g., "despite an extensive literature reporting on sars treatments, it was not possible to determine whether treatments benefited patients during the sars outbreak. some may have been harmful.") [60] . those who recovered did so by natural means; their immune systems were sufficiently strong to contain the viral attack. many were aided by public health interventions (e.g., face mask protection, frequent hand washing, living quarter disinfection, travel restrictions, and quarantine) as well. the subject of sars was selected for study because of its pandemic nature, and its apparent intractability to all drug treatments. the main goal of this study was to identify non-drug non-surgical treatments that would 1) prevent or delay the onset, or 2) reduce the progression rate, or 3) stop/reverse the progression, of sars. for much of the study, medline was used as the data source, and the mesh taxonomy of medline was used to restrict potential discoveries to selected semantic classes. the second goal was to generate large amounts of potential discovery in more than an order of magnitude less time than required for the rp study. to enhance the volume of potential discovery, a full text database was used in contrast to previous work. because of the richness of the full text, 'surgical' queries were developed that targeted the exact types of potential discovery of interest while eliminating clutter more efficiently. the 'surgical' nature of these queries compensated for the additional 'noise' characteristic of the more voluminous full text. however, since the full text database (science direct-sd) did not have an associated mesh taxonomy, the mesh taxonomy headings were essentially used as text phrases to restrict sars treatment and prevention potential discoveries to selected substances. the science citation index (sci) was also used to search for discovery, and again the mesh taxonomy headings were used as text phrases to restrict potential discoveries to selected substances. approximately four times as many records were retrieved from medline when mesh terms were included in the query compared to using only terms in the title or abstract, due to the greater choice of potential discovery substances. this means the sci or sd queries as presently constituted will retrieve only about 25% of the records that are possible using mesh to define the substance pool. before the specific approach and results are described, the medical issues for sars that served as targets for the discovery search query will be summarized. the first pandemic of the 21st century was the outbreak of sars caused by the sars coronavirus (sars-cov). as far as is known, this outbreak was not due to the deliberate release of the sars-cov, but rather was a naturally occurring event. the appearance of sars seems to have involved: 1) a zoonotic origin for sars-cov (e.g., horseshoe bats and/or chiroptera as one wildlife reservoir [7] ); 2) transmission to intermediate hosts (e.g., civet cats, raccoon dogs [8] ); 3) human contact with these intermediate hosts in southern china [guangdong province, fall 2002] and subsequent cross-species transmission of the coronavirus to humans [8] ; 4) transmission of the virus through both non-hospital personal contact and hospital staff contact [9] ; and, 5) global transmission of the virus via travelers from affected regions in asia to other countries. sars was eventually controlled through increased hygienic measures (e.g., face mask protection, frequent hand washing, living quarter disinfection), travel restrictions, and quarantine. a number of recent reviews have focused on different components of the above sars etiology, with the central focus of 1) identifying common characteristics of those who succumbed to the disease in order to 2) develop treatment targets for future outbreaks. a careful reading of these reviews shows that the humoral and cellular components of the adaptive immune system of those who succumbed were deficient on presentation and deteriorated thereafter. there is controversy about whether adequate antiviral interferons were generated during the innate response, but there is common agreement that the switch from innate to adaptive immunity was defective [10] [11] [12] [13] [14] [15] [16] [17] [18] [19] [20] [21] [22] [23] . specifically, those who succumbed from sars-cov infection tended to have the following characteristics, based on diagnostic measurements made at the time of presentation with symptoms: • older age • male gender • presence of comorbidities • elevated ldh or c-reactive protein/high initial lactate dehydrogenase level • higher initial viral load of sars coronavirus • elevated neutrophil count/neutrophilia • high levels of chemokines cxcl10 and il-18 • high levels of il-6, il-8, and mcp-1 • significant increase in the th2 cytokines il-4, il-5, il-10 • increased levels of ip-10, mig and il-8 • lower levels/deficient anti-sars spike antibody production • lymphopenia/low counts of cd4 and cd8 at presentation • reduced ace2 expression • reduced levels of il-12p70 and tnf-alpha (relative to positive outcome) • positive rt-pcr on nasopharyngeal aspirate samples • elevated pulse rate • raised serum albumin • raised serum creatinine phosphokinase (cpk) levels • increased serum creatine kinase, and urea • deviated isg and immunoglobulin gene expression levels these characteristics served as the targets to be improved by potential discoveries. [5] is a flow chart that outlines the steps used in the present study. these steps include: database selection; query development to identify the core sars literature; retrieval of the core sars literature; analysis of the retrieved core sars literature to identify the main generic themes (biomedical roadblocks); query development for, and retrieval of, literatures that represent the main generic themes; subtraction of the sars core literature from the literatures that represent the main generic themes; intersection of the net retrieved literatures for the main generic themes with the literature of desired solution types (e.g., non-drug substances); searches for potential discovery candidates in the net retrieved literature for the given classes of substances; and validation of potential discovery candidates as potential discovery. three databases were selected for source material. medline is very comprehensive in the coverage of medical issues. the sci overlaps medline strongly in coverage of the major medical journals and biology journals, but in addition covers technical disciplines well beyond the medical sphere. the sci also allows citing papers, references, and papers that share common references to be retrieved. for both these databases, titles, abstracts, and keywords were searched. in addition, it was desired to ascertain the increase in potential discovery possible from searching full text. the sd database was used for this purpose. the core sars literature is defined as those documents that the research/medical community would associate unambiguously with sars. an iterative relevance feedback approach was used, and produced the following query: "(severe-acute-respiratory-syndrome or sars-virus or (sars and (coronavirus or infect* or virus* or viral or epidemic* or epidemiology or antibodies or antibody or vaccine* or influenza or pandemic* or outbreak* or syndrome)) or sars-patient* or sars-transmission or sars-cov)". the query was inserted in the three databases to retrieve the core sars literature. multiple grouping approaches were used to identify the main generic themes of the core sars literature: document clustering, auto-correlation mapping of phrases, and factor matrix analysis of phrases, using the vantage point software package [24] . these grouping techniques were applied to retrievals from the medline and sci databases, and no significant differences were observed. this step represents the main methodological advance over the author's previous lrd studies. whereas previous lrd approaches used boolean combinations of important biomedical terms (e.g., protein and aggregation) in the query for retrieving generic biomedical literatures, the present approach used functional proximity queries (e.g., inhibit within x words of viral within x words of entry). this type of query allowed 'surgical' targeting of relevant records, and for full text in particular was necessary to filter out the large numbers of irrelevant records that would occur with a boolean query. the query has two components: (t not s) and c. t represents the technical query terms of interest, and s represents the technical query terms defining the sars core literature (shown in section 2.2). t not s will retrieve those records of interest in the total database, excluding records found in the sars core literature. c mainly represents the substances/behaviors that are in the potential discovery pool. as an example, if non-drugs were the only types of discovery of interest, c would be the pool of all nondrug records. thus, all records in medline, for example, that addressed medicinal plants would be included in c. c also includes the journals whose articles tend to focus on such substances/behaviors, and thus would expand the substance pool for potential discovery beyond a simple listing of substances. the specific steps employed in determining t are as follows. as stated previously, multiple grouping approaches were used to identify the main generic themes of the core sars literature. the main problem was deciding which hierarchical level of grouping to use for the query. initially, groupings at the lowest level of detail (e.g., cd4, cd8, il1, il2, ifn-gamma, etc.) were examined. however, a detailed examination of the sars literature showed inconsistencies in the desired directions of some of these items, based on clinical observations and data. this led to examination of functional groupings at a higher level of aggregation (e.g., inhibit viral replication, enhance humoral immunity, improve cell-mediated immunity, increase th1, etc.), which could accommodate different directions at the lowest level of detail while achieving the targets represented by the higher level of aggregation. to retrieve the directly related literature from which potential discovery would be extracted, this higher level functional query was applied to the search engines of three databases: sci, medline, and sd. the first two of these databases provide abstracts as the major text source, and sd provides full text. since the sd analysis took place a few months after the sci and medline analyses, the initial query was modified slightly to exploit the sd search engine features. appendix 1 of [54] contains the full sci and medline queries, and appendix 2 of [54] contains the full sd query. the unique features of each are explained in these appendices. there were two types of fundamental terms in the full query (type i and type ii) , and examples from the more abbreviated sd query will be presented here. type 1 focused on inhibiting viral entry to healthy cells and/or inhibiting their replication, whereas type 2 focused on improving immune system component performance. these two generic categories were identified from analysis of the retrieved sars core literature. factor analysis and document clustering of this core literature identified these key thrust areas, and further phrase frequency analysis of the retrieved sars core literature identified the biomedical term ('viral entry')functional term ('inhibit') combinations eventually selected for the query. in the proximity form of the query used below, 'a pre/5 b' is a precedence relation, and means that term a precedes term b, with a spacing ranging from zero (adjacency) to five words. 'a w/15 b' is a proximity relation, and means that term a is within 15 words of term b. this proximity form of the query (as contrasted to the boolean form used in prior lrd studies) provided highly 'relevant' retrievals, where 'relevant' is defined as any article that contains a potential discovery or innovation candidate. ref [54] contains a more detailed discussion of 'relevance' in the present context. type 1 (((inhibit* pre/5 "virus entry") or (inhibit* pre/5 "viral entry") or (inhibit* w/15 replicat* w/15 virus) or (inhibit* w/15 replicat* w/15 viral)) and (potent pre/15 "antiviral activity")) type 2 (((enhanc* pre/5 "humoral immun*") and (enhanc* pre/5 "humoral response*") and ((enhanc* pre/5 "antibod* response*") or (enhanc* pre/5 "antibod* production") or (enhanc* pre/5 "virus neutraliz*") or (enhanc* pre/5 "viral neutraliz*"))) or ((enhanc* pre/5 "cellular immun*") and (enhanc* pre/5 "cell mediated immun*") and ((enhanc* pre/5 cd4) or (enhanc* pre/5 cd8) or (enhanc* pre/5 "t cell response*") or (enhanc* pre/5 "t cell immune response*"))) or ((enhanc* pre/5 "innate immun*") and (enhanc* pre/5 "innate antiviral") and ((enhanc* pre/5 "antiviral activity") or (enhanc* pre/5 "antiviral response*")))). when the type 1 query shown above was applied to full text, reasonable numbers of relevant articles were retrieved. when the type 1 query was applied to abstracts, the articles retrieved were highly relevant, but the numbers retrieved (as will be shown) were miniscule. to obtain more articles when searching the abstracts, a modified type 1 query was generated. this modified form changed the 'and' (in the query above) to an 'or', a much less restrictive condition. this resulted in an order of magnitude more retrieved and relevant articles (when searching abstracts), although still small compared to the retrievals obtained from searching full text. type 2 queries focused on enhancing the performance of the different components of the immune system. there were a number of variants of the type 2 query shown above that were examined. appendix 1 of ref. [54] shows the form of the query used to generate the sci results. the type 2 entry under the t component is for 'improv*', but the full query added blocks that replaced 'improv*' with enhanc* or induc* or stimulat* or increas* or activat* or regulat*. obviously, other such terms could be identified and used as well, but these terms were deemed adequate for the present proof-of-principle demonstration, which shows the feasibility of the methodology. the query examples provided above were for the sd database, which has intrinsic proximity query capabilities in addition to boolean query capabilities. the sci search engine does not have adjacency/proximity search capability presently. the only search capabilities are boolean/co-occurrence in a selected field or among all fields (e.g., a same b, or a and b). to overcome this deficiency, the author developed an algorithm that would provide such capability [25] . in the algorithm, sci stopwords are used to set spacing between terms. thus, a query term of the form [improv*-of-humoral-immun*] will retrieve those records containing variants of improv* that precede variants of 'humoral-immun*' with one word intercalated. the intercalated word could be any word, not just the stopword used in the query. as can be seen from the terms in appendix 1of ref. [54] , the actual query used did not go beyond precedence spacings of two words, but a larger production-oriented study could use greater spacings between the terms of interest. this would retrieve far more records, and lead to more candidate potential discoveries. in appendix 1 of ref. [54] , the s block of terms represents the core sars records, and its inclusion as a negation expression insures the records retrieved are disjoint from the core sars literature. in appendix 1 of ref. [54] , the blocks listed under c are the types of substances/behaviors considered for discovery. they consist of records from non-drug journals as shown, and records that contain non-drug substances. the value of including the journals is that their records could include substances/behaviors not identified in the substances/behaviors blocks (i.e., pre-specified lists of substances/behaviors). obviously, many more substances/behaviors could be added to the list in a more comprehensive production-oriented study. the records retrieved by the t not s query were intersected with the records retrieved by the c query, to yield records that identified non-drug substances/approaches that would produce immune system changes in the desired directions. these records were inspected visually, and sample results are presented in the next section. the purpose of this study is to identify potential discovery and innovation. for this purpose, 'relevant' is interpreted as any article that contains a potential discovery or innovation candidate. what is potential discovery? it is the linking of two or more literature concepts (that have not been linked previously in the literature; i.e., disjoint) in order to produce novel, interesting, plausible, and intelligible connections. a potential discovery candidate is an interesting linkage that has to be vetted against prior knowledge to validate disjointness. in practice, a major roadblock is defining 'prior knowledge', and in particular the databases that will be used to represent 'prior knowledge' for the vetting process and how these databases will be interpreted. to make the problem tractable, only the main source databases are selected for the 'prior knowledge' determination. in the present case, the same three major sources that were used in previous lrd medical studies have been selected for the 'prior knowledge' determination: sci; medline; and patent database as represented by derwent innovation index (dii). for each candidate potential discovery, a query was developed that intersected the candidate potential discovery (e.g., curcumin) with the sars core literature query (severe acute respiratory syndrome or .....), and the query was inserted into each of the three validation databases. if no prior records were retrieved, the concept was viewed as a potential discovery. if prior records were identified, the concept could still be viewed as a potential innovation if the judgment was made that the concept could be developed at a more accelerated pace. application of the full query to the sci/ssci database (1989-2008, articles and reviews) yielded 662 records. the records were sampled for 'relevancy' to discovery or innovation, using the definitions of relevancy as discussed previously. approximately 85% were judged to be 'relevant' (potential discovery candidates). in addition, the 7000 most recent papers in the sci that cited the 662 records were retrieved. these citing papers covered approximately the seven year period 2002-2008, and about 50% were judged to be relevant. in the previous lrd studies on medical topics, before the ability to retrieve all the papers that cite an initial retrieval became available in the sci, only spot checks could be done of papers that cited potential discovery candidates. not only are papers that cite potential discovery candidates good potential discovery candidates themselves, but the author's preliminary (unpublished) experiments which show many different types of citation linkages (e.g., papers that share references) to potential discovery candidates will identify good potential discovery candidates. application of the query to the medline database yielded 1149 records. while the version of the medline database used (through the web of knowledge search engine) goes back to 1950, it effectively started in about 1975, when abstracts were introduced. the records retrieved were sampled for 'relevancy' to discovery or innovation, using the definitions of relevancy as discussed previously. approximately 80% were judged to be 'relevant' (potential discovery or innovation candidates). there is much overlap between medline and the sci. application of the appropriate query from appendix 1 of ref. [54] to the science direct database (1999-2008) yielded different types of results, depending on which field was searched, and some of these findings are reported in table 1 . the retrieval results among sci, medline, and science direct are not comparable due to the different journal coverage of each database. specific examples of potential discovery from each of these databases will be shown later in the present results section. in table 1 , the science direct results are for the three components of the type 1 query. the first row (inhibit*acetabularia) reflects the intersection of the terms for the 'inhibit' group (e.g., "(inhibit*-virus-entry or inhibit*-viral-entry or inhibit*-of-virusentry or inhibit*-of-viral-entry or inhibit*-of-of-virus-entry or inhibit*-of-of-viral-entry or (inhibit*-replication same (virus or viral)) or (inhibit*-of-replication same (virus or viral)) or (inhibit*-of-of-replication same (virus or viral)))" and the group of substances and behaviors that starts with 'acetabularia' (e.g., acetabularia or achlya or acupressure or acupuncture or algae or alkaloid* or allium or angiosperms or anthocerotophyta or anthocyanins.....) listed in appendix 2 of ref. [54] . the second and third rows substitute the euglendia and plankton groups for the acetabularia group. for the first row, the second column (unmod query -absrec) contains the number of records retrieved when the full text query was applied to the abstract field. the full text query was designed to provide 'surgical' targeting of key phrase relations in the full text, contains the intersections of a number of proximal relations, and is a rather restrictive condition. applied to the full text, the query is very effective, but it is far too restrictive for the abstract field, as the results show. very few records are retrieved, and they are all relevant (column 3). essentially no records were retrieved in this column for any of the type 2 queries, since the type 2 queries are even more restrictive (more intersecting terms) than the type 1 query. column 4 (mod. query -absrec) contains records retrieved using the modified type 1 query applied to the abstract field. all occurrences of 'and' were replaced with 'or'. on average, about an order of magnitude more records were retrieved with the modified query compared to the full text query, but the numbers are still small. the relevance of the retrieved records is still quite high. for the type 2 query components (not shown), the column 4 retrievals were about half as much for the 'enhance' group, about twice as much for the 'induce' group, about the same for the 'stimulate' group, and about the same for the 'increase' group. there were overlaps among the groups, and search engine limitations did not allow estimation of the degree of overlap. column 5 is the relevance percentage of the column 4 retrievals. it is highest for the 'inhibit' group, is about 60% for the 'enhance' group, and is about 50% for the other three (type 2) groups. column 6 (unmod. query -fltxrec) represents the retrievals for the full text query of appendix 2 applied to the full text. they are almost an order of magnitude larger than those of column 4, and the relevance percentage (column 7) is almost the same as that for the abstracts in column 5. the percentage is highest for the 'inhibit' group, is about 80% for the 'enhance' group, and is about 50% for the other three (type 2) groups. column 8 (ft/abs-norm) is the ratio of full text retrievals to abstract retrievals (normalized to the total numbers of full text and abstract records in the database) using the restricted form of the full text query for each, and column 9 is the same ratio where the less restricted form of the query was used to search the abstracts. the bottom line is that many potential discovery candidates have been retrieved. many more are possible: increasing the substance base (through more non-drug items or by inclusion of drugs) would probably increase the number of candidates by an order of magnitude; increasing the number of terms in the query would enhance the retrieval; relaxing the proximity conditions would increase the retrieval; relaxing the intersection requirements would increase the retrieval; and adding further types of citation linkages would increase the retrieval. a major factor in the high relevance fractions achieved is the form of the query terms; they were not used in any previous lrd studies, but will become a fixture in future studies. this remainder of this section contains representative examples of potential discovery from literatures related directly to the core sars literature. before proceeding to analyses, a few illustrative examples from the core sars literature restricted to semantic classes will be presented. while these are not discovery, they nevertheless reflect the types of impact that the non-drug approaches could potentially have for delaying or preventing the onset of sars. in addition, as will be discussed later, some of these core concepts are prime candidates for innovation. for example, "aurintricarboxylic acid (ata) has been shown to inhibit the replication of viruses from several different families, including ….. the coronavirus causing severe acute respiratory syndrome. vaccinia virus replication is significantly abrogated upon ata treatment, which is associated with the inhibition of early viral gene transcription. this inhibitory effect may be attributed to two findings. first, ata blocks the phosphorylation of extracellular signal-regulated kinase 1/2, an event shown to be essential for vaccinia virus replication. second, ata inhibits the phosphatase activity of the viral enzyme h1l, which is required to initiate viral transcription. thus, ata inhibits vaccinia virus replication by targeting both cellular and viral factors essential for the early stage of replication" [26] . as another example, "we identified that three widely used chinese medicinal herbs of the family polygonaceae inhibited the interaction of sars-cov s protein and ace2. the ic50 values for radix et rhizoma rhei (the root tubers of rheum officinale baill.), radix polygoni multiflori (the root tubers of polygonum multiflorum thunb.), and caulis polygom multiflori (the vines of p. multiflorum thunb.) ranged from i to 10 [lg/ml]. emodin, an anthraquinone compound derived from genus rheum and polygonum, significantly blocked the s protein and ace2 interaction in a dose-dependent manner. it also inhibited the infectivity of s protein-pseudotyped retrovirus to vero e6 cells. these findings suggested that emodin may be considered as a potential lead therapeutic agent in the treatment of sars" [27] . more detailed descriptions of the following potential innovations and discoveries can be found in ref. [54] . cimicifuga rhizoma, meliae cortex, coptidis rhizoma, phellodendron cortex and sophora subprostrata radix decreased the mhv production and the intracellular viral rna and protein expression, and could be potential candidates for new anti-coronavirus drugs [28] ; betulinic acid and savinin were competitive inhibitors of sars-cov 3cl protease [29] ; quercetin-3-beta-galacto side was identified as an inhibitor of the protease [(3cl(pro))] [30] ; alpha,beta-unsaturated peptidomimetics, anilides, metalconjugated compounds, boronic acids, quinolinecarboxylate derivatives, thiophenecarboxylates, phthalhydrazide-substituted ketoglutamine analogs, isatin and natural products have been identified as potent inhibitors of the sars-cov main protease [31] ; tannic acid and 3-isotheaflavin-3-gallate were found to be inhibitive. these two compounds belong to a group of natural polyphenols found in tea, and only theaflavin-3,3′-digallate (tf3) was found to be a 3clpro inhibitor [32] . glf[fermentation product of chinese medicinal mushroom] up-regulated the cell-mediated immune response related cytokines (il-2, ifn-gamma, and tnf-alpha) expression in different lymphoid tissues [33] ; jacalin, an antigen-specific lectin from jackfruit seeds, has been shown to induce mitogenic responses and to block infection by hiv-1 in cd4(+) t lymphocytes [34] ; sulforaphane significantly downregulated the serum levels of proinflammatory cytokines such as il-1 beta, il-6, tnf-alpha, and gm-csf during metastasis [35] ; immunomodulatory activity of methanolic extract of m. koenigii leaves was evaluated on humoral and cell mediated immune response to ovalbumin, and the extract holds promise as immunomodulatory agent, which acts by stimulating humoral immunity and phagocytic function. [36] ; the aqueous extract of t. cordifolia was found to enhance phagocytosis in vitro. the aqueous and ethanolic extracts also induced an increase in antibody production in vivo. [37] ; oral intake of the fucoidan might take the protective effects through direct inhibition of viral replication and stimulation of both innate and adaptive immune defense functions. [38] ; atractylodes macrocephala koidz (amk) markedly stimulated lymphocyte proliferation, antibody production, and cytokine secretion in mouse splenocytes, showing the ability to induce the preferential stimulation of th1 type, rather than th2 type t lymphocytes [39] ; a potent anti-influenza virus activity was discovered in summer leaves of japanese wasabi [(wasabia japonica)], inhibiting influenza virus replication regardless of the hemagglutinin antigen type. [40] ; purification of an antiviral peptide from seeds of sorghum bicolor l strongly inhibited the replication of herpes simplex virus type i (hsv-1) [41] . combined treatment with pidotimod and red ginseng acidic polysaccharide has an immunostimulatory effect in a synergistic manner on antibody response to challenge with lipopolysaccharide and sheep red blood cells without toxic changes [42] ; myrica rubra leaf ethanol extract showed anti-influenza virus activity irrespective of the hemagglutinin antigen type in the influenza virus type a (h1n1), its subtype (h3n2), and type b [43] ; oral intake of l. paracasei ncc2461 by aged mice enhanced the specific adaptive immune response to in vivo antigenic challenge without altering other cellular and humoral immune responses [44] ; methanol extract of asarum sieboldii inhibited the h5n1 influenza viruses from the infected cells [45] ; caffeoyl glycoside from the roots of picrorhiza scrophulariiflora (kutki) stimulated cell proliferation of splenocytes and peritoneal macrophages, enhanced the cytotoxicity of natural killer (nk) cells, increased cd4 and cd8 cell populations, and has immunomodulatory activity by regulating expression of th1 and th2 related cytokines [46] . korean mistletoe lectin c increased influenza-specific antibodies with dominant igg1 subclass in serum, igg in genital secretions and iga in saliva, and significantly enhanced influenza-specific lymphocyte proliferation and cytotoxic activity in spleens and in mediastinal lymph nodes. when kml-c was used as a mucosal adjuvant, mice were completely protected from mortality after the challenge with a homologous (h1n1) mouse-adapted influenza virus [47] ; seeds of cochinchina momordica numerically increased the antibody levels, suggesting potential to improve the immune responses by use as an adjuvant [48] ; ag85b of mycobacteria, which cross-reacts among mycobacteria species, elicits helper t-cell type 1 (th1) immune responses as a novel adjuvant [49] ; probiotic bacillus cereus var. toyoi-treated piglets showed a significantly lower frequency of cd8(high)/cd3+ t cells and cd8(low)/cd3+ t cells and a significant higher cd4+/cd8+ ratio [50] . different components of kefir have an in vivo role as oral biotherapeutic substances capable of stimulating immune cells of the innate immune system, to down-regulate the th2 immune phenotype or to promote cell-mediated immune responses against tumors and also against intracellular pathogenic infections [51] ; lentinan possesses antiviral activity due to an induction of interferon-γ production; enhances host resistance against infections with bacteria as well as fungi, parasites, and viruses, including the agent of aids, and reduces the toxicity of azt [52] ; a polyphenol rich extract (cystus052) from the mediterranean plant cistus incanus exerts a potent anti-influenza virus activity in a549 or mdck cell cultures infected with prototype avian and human influenza strains of different subtypes [53] . because the purpose of the sars study was to demonstrate an approach, and not necessarily to be comprehensive, a number of shortcuts were taken. not all possible semantic categories for potential discoveries were identified, only the most obvious. relatively few terms were selected for the queries; many more were available. not all retrieved records were examined; only enough to demonstrate the quality of results. the potential expansion to indirectly related literatures using both text linking and citation linking described previously was not done. thus, the results obtained should be viewed as the tip of a very large iceberg. in previous medical applications of lrd, the discovery approach was to cluster the disease literature into groups of disease characteristics, generate combinatorials of intra-group characteristics (essentially synonyms), construct a discovery query from these combinatorials, and apply the query to non-drug substances/behaviors. in the present application, a somewhat different approach was taken. since the characteristics of those who had succumbed to sars tended to be sub-optimal performance of different immune system components, the query combined the immune system components at a higher aggregation level with functional terminology designed to improve this performance (e.g., enhance humoral immunity). such a query structure allowed a large number of potential discovery candidates to be identified. as the previous paragraph shows, much more is possible in terms of potential discovery volume. the picture from the handful of potential discoveries reported in this paper (and the hundreds of additional potential discoveries possible with a properly resourced study) is a synergy of lifestyle/dietary practices that could be interpreted as anti-sars. along with non-discovery items such as aurintricarboxylic acid (ata), emodin (an anthraquinone compound derived from genus rheum and polygonum), cimicifuga rhizoma, meliae cortex, coptidis rhizoma, phellodendron cortex, sophora subprostrata radix, betulinic acid, savinin, abietane-type diterpenoids and lignoids, quercetin-3-beta-galacto side, d.alpha,beta-unsaturated peptidomimetics, anilides, metal-conjugated compounds, boronic acids, quinolinecarboxylate derivatives, thiophenecarboxylates, phthalhydrazide-substituted ketoglutamine analogs, isatin, tannic acid, and 3-isotheaflavin-3-gallate (tf2b) are potential discovery items such as ganoderma lucidum, jacalin, sulforaphane, methanolic extract of m. koenigii leaves, tinospora cordifolia, fucoidan, atractylodes macrocephala koidz, wasabia japonica, seeds of sorghum bicolor l, pidotimod and red ginseng acidic polysaccharide (rgap), myrica rubra leaf ethanol extract, l. paracasei ncc2461, methanol extract of asarum sieboldii, caffeoyl glycoside, and adjuvants korean mistletoe lectin c, cochinchina momordica seed, ag85b, probiotic bacillus cereus var. toyoi, kefir, lentinan, polyphenol rich extract (cystus052) from the mediterranean plant cistus incanus. as stated above, more laboratory tests and field trials would have to be done on all these items to insure that they are anti-sars and safe, but these preliminary literature-based results offer some promise of what is possible. there is a major disconnect between the absence of therapies presently or potentially available on all the major medical web sites (and in sars mainstream journal review papers), and the potential therapies suggested by what has already been demonstrated in the core sars literature, much less what this study has generated from the related literatures. few medical web sites even mention any of the approaches shown in the sars core results section. the core literature and related literature potential discoveries and innovations have the potential to evolve into mainline medical treatments. literature-related discovery literature-related discovery (lrd): potential treatments for parkinson's disease literature-related discovery (lrd): potential treatments for multiple sclerosis literature-related discovery (lrd): introduction and background literature-related discovery (lrd): methodology the highly cited sars research literature evolution of genomes, host shifts and the geographic spread of sars-cov and related coronaviruses towards our understanding of sars-cov, an emerging and devastating but quickly conquered virus the outbreak pattern of sars cases in china as revealed by a mathematical model pathology and pathogenesis of severe acute respiratory syndrome interferon and cytokine responses to sars-coronavirus infection pathogenetic mechanisms of severe acute respiratory syndrome analysis of serum cytokines in patients with severe acute respiratory syndrome pathogenesis of severe acute respiratory syndrome clinical features, pathogenesis and immunobiology of severe acute respiratory syndrome sars coronavirus and innate immunity interferon-mediated immunopathological events are associated with atypical innate and adaptive immune responses in patients with severe acute respiratory syndrome human immunopathogenesis of severe acute respiratory syndrome (sars) mechanisms of severe acute respiratory syndrome pathogenesis and innate immunomodulation, microbiol characterization and inhibition of sars-coronavirus main protease t cell responses to whole sars coronavirus in humans severe acute respiratory syndrome coronavirus as an agent of emerging and reemerging infection molecular pathogenesis of severe acute respiratory syndrome, microbes infect adjacency and proximity searching in the science citation index and google aurintricarboxylic acid inhibits the early stage of vaccinia virus replication by targeting both cellular and viral factors emodin blocks the sars coronavirus spike protein and angiotensin-converting enzyme 2 interaction in vitro inhibition of coronavirus replications by the traditionally used medicinal herbal extracts, cimicifuga rhizoma, meliae cortex, coptidis rhizoma, and phellodendron cortex specific plant terpenoids and lignoids possess potent antiviral activities against severe acute respiratory syndrome coronavirus binding interaction of quereetin-3-beta-galactoside and its synthetic derivatives with sars-cov 3cl(pro): structure-activity relationship studies reveal salient pharmacophore features characterization and inhibition of sars-coronavirus main protease inhibition of sars-cov 3c-like protease activity by theaflavin-3,3'-digallate (tf3), evid. based complement effects of fermentation products of ganoderma lucidum on growth performance and immunocompetence in weanling pigs glycosylation-dependent interaction of jacalin with cd45 induces t lymphocyte activation and th1/th2 cytokine secretion modulation of cell-mediated immune response in b16f-10 melanoma-induced metastatic tumor-bearing c57bl/6 mice by sulforaphane immunomodulatory activity of methanolic extract of murraya koenigii (l) spreng. leaves enhanced phagocytosis and antibody production by tinospora cordifoliaa new dimension in immunomodulation defensive effects of a fucoidan from brown alga undaria pinnatifida against herpes simplex virus infection stimulating effects on mouse splenocytes of glycoproteins from the herbal medicine atractylodes macrocephala koidz anti-influenza virus activity of extract of japanese wasabi leaves discarded in summer antiviral activity and mode of action of a peptide isolated from sorghum bicolor synergistic immunostimulatory effect of pidotimod and red ginseng acidic polysaccharide on humoral immunity of immunosuppressed mice anti-influenza virus activity of myrica rubra leaf ethanol extract evaluated using madino-darby canine kidney (mdck) cells effect of lactobacillus paracasei ncc2461 on antigenspecific t-cell mediated immune responses in aged mice screening of a natural feed additive having anti-viral activity against influenza a/h5n1 immunopotentiation of caffeoyl glycoside from picrorhiza scrophulariiflora on activation and cytokines secretion of immunocyte in vitro intranasal immunization with influenza virus and korean mistletoe lectin c (kml-c) induces heterosubtypic immunity in mice improvement of the efficacy of influenza vaccination (h5n1) in chicken by using extract of cochinchina momordica seed (ecms) innovation of vaccine adjuvants bacillus cereus var. toyoi enhanced systemic immune response in piglets effects of kefir fractions on innate immunity nutraceuticals: a piece of history, present status and outlook a polyphenol rich plant extract, cystus052, exerts anti influenza virus activity in cell culture without toxic side effects or the tendency to induce viral resistance literature-related discovery: potential treatments and preventatives for sars, dtic technical report number ada525270, defense technical information center innovation forecasting: a case study of the management of engineering and technology literature evaluating innovation networks in emerging technologies mining ideas from textual information a compared r&d-based and patent-based cross impact analysis for identifying relationships between technologies quantitative mapping of scientific research-the case of electrical conducting polymer nanocomposite sars: systematic review of treatment effects he conducted research at bell labs and mitre corp, and managed programs at department of energy and office of naval research. he is presently a research affiliate with the school of public policy, ga tech, where he focuses on textual data mining. he is listed in who's who in america, who's who in science and engineering the research described in this paper was supported by mitre corporation internal research funds. key: cord-332186-3jy9zoz2 authors: edens, fw; parkhurst, cr; qureshi, ma; casas, ia; havenstein, gb title: atypical escherichia coli strains and their association with poult enteritis and mortality syndrome date: 1997-07-01 journal: poultry science doi: 10.1093/ps/76.7.952 sha: doc_id: 332186 cord_uid: 3jy9zoz2 abstract to date, no definitive etiology has been described for poult enteritis and mortality syndrome (pems). however, two atypical escherichia coli colony types are isolated consistently from moribund and dead poults afflicted with pems. to test the infectivity of these e. coli strains, poults were placed into floor pens in three isolation treatment rooms: 1) control: no bacterial challenge, 2) e. coli colony types 1 or 2 posthatch oral challenge: 10(8) cfu/per poult at 1 d, and 3) e. coli colony types 1 or 2 posthatch oral challenge: 10(8) cfu/per poult at 6 d. daily intramuscular injections of cyclophosphamide (100 micrograms per poult) from 1 to 5 d posthatch were given to half of the poults in each treatment. atypical e. coli challenge caused bw depression, and cyclophosphamide treatment exacerbated the response. all e. coli-challenged poults developed diarrhea similar to pems. mortality was increased by both atypical e. coli colony types, but at 21 d e. coli colony type 2 caused greater mortality than colony type 1. with cyclophosphamide treatment, mortality was exacerbated with both colony types, but colony type 2 at 1 d caused the greatest mortality. ultrastructural damage to ileum epithelium cell microvilli and subcellular organelles indicated that part of the bw depression could be attributed to malabsorption of nutrients. it was concluded that the atypical e. coli colony types 1 and 2 play a significant role in the pems disease. since 1991, the number of verified cases of poult enteritis and mortality syndrome (pems) has increased significantly each year. until 1994, pems was a problem localized in the carolinas and georgia (barnes and guy, 1995; barnes et al., 1996; brown, 1995) , but in 1995 pems was verified in at least six additional states and was suspected in outbreaks of severe enteritis with diarrhea and high mortality in three other countries (brazil, canada, and portugal; anonymous communication) . these reports signaled the possibility of a turkey disease outbreak in epidemic proportions on a national and international scale. poults between 7 and 28 d of age appear to be at the greatest risk for pems (brown, 1995; barnes and guy, 1995; barnes et al., 1996) . symptomatic poults display signs of irritability (walking and high pitched vocaliza-tion) initially, followed by anorexia, diarrhea of increasing severity, dehydration, growth depression in excess of 40%, near total morbidity, and finally mortality in excess of 1%/d for 3 or more consecutive d. survivors are stunted severely and never reach target market weights. recently, qureshi et al. (1997) reported that pems afflicted poults are severely immunosuppressed. our observations indicated that t cell-mediated immune response and b cell-mediated humoral immunity both are suppressed significantly. furthermore, the bursa of fabricius, spleen, and thymus are atrophied as a result of pems. whether the dysfunction is a direct result of a viral or bacterial infection or whether it is indirectly associated with a severe stress response due to an infection from an unidentified etiology has not been ascertained. the pems problem is complicated by the fact that no etiological agent(s) have been identified (brown, 1995; barnes and guy, 1995; barnes et al., 1996; qureshi et al., 1996) . numerous potential viral agents have been investigated, including adenovirus, coronavirus, coronavirus-like particles, enterovirus, astrovirus, birnavirus (serotype 2), rotavirus (type d), reovirus, bursa epithelial virus, and others. however, alone these viruses have not been shown to induce pems (brown, 1995; barnes and guy, 1995; barnes et al., 1996) . nevertheless, brown (1995) reported that a coronaviruslike particle and a serotype 2 birnavirus could both reduce growth in 3-wk-old poults. co-challenge with these two agents depressed growth and feed conversion significantly and caused 60% mortality, resulting in a condition analogous to pems. it also has been observed that cryptosporidiosis complicates the pems problem on some farms, but cryptosporidium infections alone do not cause pems (brown, 1995; barnes and guy, 1995; barnes et al., 1996) . on the other hand, barnes et al. (1996) suggest that after an unidentified virus infects the turkey poults, opportunistic enteric bacteria (such as salmonella, escherichia coli, or clostridium) further complicate the pems condition and cause mortality in the immunocompromised poult. research on pems has been very slow to yield insight that could lead to a solution to the problem. however, we have consistently isolated from moribund pemsinfected poults two pure cultures of atypical e. coli along with several other atypical e. coli strains. although the isolation of these strains was fortuitous, it appears that their presence in nearly every set of pems-infected poults sent to one of the north carolina department of agriculture (ncda) regional diagnostic laboratories suggests that they may be very important. indeed, these e. coli strains may represent a significant breakthrough in the diagnosis and control of pems. this report describes the effects of single oral inoculations of these two atypical strains of e. coli on growth and livability of turkey poults. this project was approved and was conducted under the supervision of the north carolina state university animal care and use committee, which has adopted animal care and use guidelines governing all animal use in experimental procedures. british united turkey poults from a commercial hatchery were obtained within 6 h after hatching. the poults received neither vaccinations nor hatchery services such as beak, snood, or toe trimming. they were transported to north carolina state university's dearstyne avian research center disease isolation facility. for experiment 1, they were segregated randomly into treatment groups, wing-banded, and placed into electrically heated battery brooders, where they were maintained through 14 d of age. in experiment 2, they were placed in floor pens with pine wood shavings litter and were maintained through 21 d of age. a turkey starter ration, containing 28.13% crude protein and a metabolizable energy level of 2,915 kcal/kg (table 1) , was provided. water was available ad libitum in zinc galvanized drinkers. ambient temperature in the two experiments was regulated at 34 c for 7 d after placement, when it was reduced to 30 c until 14 d. from 14 through 21 d, the temperature was set at 27 c. in experiment 2, two radiant heaters 3 were suspended 24 in above each floor pen to provide a supplementary heat source, if required by the poults. the poults were provided continuous light throughout the experimental periods. air exchange rate in the isolation rooms was designed to provide a minimum of four changes per hour to prevent ammonia build-up. nevertheless, environmental conditions were altered by reducing air flow in the isolation rooms to allow moisture build-up in the litter under the poults. by the end of 21 d, the litter moisture was elevated to more than 45%, a condition not unlike that found in commercial turkey production areas in the southeast during periods of hot humid weather when there are severe outbreaks of pems. in experiment 1, moribund pems-infected poults were obtained from a commercial turkey producer, killed by carbon dioxide asphyxiation, and dissected to remove the ceca. precautions were taken to prevent contact between the excised ceca and either the body surface or necropsy table. the isolated ceca were placed into sterile plastic packets before stomaching. the contents were streaked onto macconkey agar plates and incubated 24 h at 37 c. escherichia coli colonies were isolated from these plates and propagated anaerobically 24 h at 37 c in brain heart infusion (bhi) broth and were used in three separate trials. in experiment 2, e. coli, identified by colony morphology (smooth, raised, mucoid, and slow-growing colony as type 1; rough, flat, congo red-positive fast-growing colony as type 2) were isolated consistently from pemsinfected poults at a ncda regional diagnostic laboratory and propagated on bhi broth. the type 1 and type 2 colonies were designated as atypical forms based upon their bbl biochemical profiles (edens et al., unpublished data) . in experiment 1, day-old healthy, mixed-sex poults from a commercial hatchery were given a single oral challenge with 1 ml of the anaerobic e. coli culture (10 8 cfu/ml per poult) derived from the ceca of pems-infected poults from a commercial source. control poults were given orally an equal volume of bhi broth. in trial 1, there were 30 control poults, 120 poults challenged at 1 d of age, and 18 poults challenged at 5 d of age. in trials 2 and 3, there were 50 control poults, 50 challenged at 1 d with a live bacterial culture, 50 challenged at 1 d with a killed bacterial culture (autoclaved culture) followed at 5 d with a live bacterial culture, 50 challenged with killed organisms at 1 d, and 50 challenged with a live bacterial culture at 1 d followed by killed organisms at 5 d. no attempt was made to identify the serotypes of this mixture of e. coli colonies used in this oral inoculum. the birds were maintained in heated metal brooding batteries from hatching until 2 wk of age. in experiment 2, either atypical e. coli colony type 1 or type 2 was given orally to male poults at either 1 or 6 d of age. the challenge dose of 1 ml for each poult contained 10 8 cfu of a single colony type. an equal volume of bhi broth was given to the control poults. there were four replicate groups of 25 poults for each of the colony types administered, and two replicates of 25 each for the controls. thus, a total of 250 poults were involved in experiment 2. in experiment 2, two replicate groups of the poults were given either atypical e. coli colony type 1 or atypical e. coli colony type 2 at either 1 or 6 d of age and one replicate of the control group were given cyclophosphamide (cpd, 100 mg per poult) intramuscularly for 5 consecutive d beginning at day of hatch. cyclophosphamide is an alkylating agent that binds readily to b cell dna, rendering those cells inactive (lerman and weidanz, 1970; glick, 1971 glick, , 1977 , and it was administered to mimic the immunodepression or immunodysfunction found in field cases of pems. the cpd treatment was administered in sterile avian saline (0.85% sodium chloride) in a volume of 100 ml. an equal volume of avian saline was given to all other poults. a total of 125 poults were given cpd. body weights were determined on a weekly basis, and mortality was determined on a daily basis. at 21 d of age, surviving poults were killed by carbon dioxide asphyxiation and each poult was examined and rated for its level of enteritis based upon the presence of distended, gaseous intestines and ceca each containing yellowish, liquid fecal material with excessive mucous content. the bursa of fabricius from each poult was examined macroscopically for the presence of bursa cores consisting of hard caseous material. at the time of necropsy, representative samples of the ileum from five poults from each treatment were collected for transmission electron microscopic examination of the effects of e. coli infection on the morphology of the epithelial lining of the ileum. tissues (2 to 4 mm 2 ) were fixed in ice cold glutaraldehyde and 0.1 m sodium cacodylate buffer, ph 7.4. the samples were washed 3 · 15 min each in ice cold 0.1 m sodium cacodylate buffer, then postfixed for 2 h in 1% osmium tetroxide in sodium cacodylate buffer. the tissue samples were then washed again 3 · 15 min each in ice cold sodium cacodylate buffer, trimmed to 1-mm cubes, and dehydrated in 10% graded series of ethanol solutions (30 to 70% for storage at 4 c). samples were then dehydrated to 3 · 95% ice cold ethanol for 15 min each, and finally the tissues were dehydrated to 3 · 100% ethanol for 15 min each, with gradual return to room temperature (25 c). the tissues were infiltrated with a 1:1 ethanol:spurr's (firm mixture) for 6 h at room temperature followed by overnight infiltration in 1:3 ethanol:spurr's at room temperature. the samples were then placed in 100% spurr's mixture for 2 · 3 h changes before embedding in flat molds overnight at 70 c. both thick (1 m) and thin (800 å ) sections were cut using an ultramicrotome. thick sections were mounted on glass slides and stained with toluidine blue. thin sections were mounted on 200-mesh grids and stained with 4% aqueous uranyl acetate for 1 h at room temperature, rinsed in three changes of filtered distilled water, then stained 4 min at room temperature with reynold's lead acetate and rinsed. grids were viewed with a joel 100s transmission electron microscope at 80 kv. weekly bw, total weekly mortality, and the percentage of survivor poults found to have bursa cores were analyzed statistically using the general linear models procedure of sas (sas institute, 1985) . the bw and mortality data were subjected to analysis of variance and the bursa core data were analyzed by t test. percentage data were converted to arc sine square root percentages before analysis. means were separated using least significant difference. statements of significance were based onp £ 0.05 or less. the effect of anaerobic-isolated and cultured e. coli from pems-afflicted poults on bw and mortality in experiment 1 are presented in table 2 . oral challenge with the e. coli isolates at 1 d caused a significant decrease in bw by 5 and 7 d postchallenge in trials 1, 2, and 3, respectively. this depression in bw persisted through 14 d. challenge at 5 d of age also caused a significant depression in bw at 14 d. presentation of killed cultures at 1 d provided some protection from the challenge with live organisms at 5 d, based on intermediate bw gain compared to groups given live organisms alone at 1 d and to control poults. mortality was increased significantly in trial 1 when live organisms were inoculated at 1 d. mortality was not recorded in trials 2 and 3 because poults were taken daily for determination of other parameters (data not reported here). table 3 are the bw data for experiment 2. during the first week after oral challenge with atypical e. coli colony types 1 or 2, poults inoculated at 1 d had significantly reduced bw in comparison to the controls, whereas those inoculated at 6 d had bw intermediate to the controls and those inoculated at 1 d. during week 1, poults given the cpd experienced a small but nonsignificant decrease in bw. however, this decrease in bw due to cpd reduced the difference between controls and the e. coli-treated groups resulting in no group differences. at 21 d, there was a clear difference between control poults and poults given the two colony types of e. coli. among the e. coli treatment groups, poults given colony type 2 at 1 d had significantly smaller bw than all other treatment groups. in the groups given both cpd and one or the other of the two different atypical e. coli colony types at either 1 or 6 d, the treatment groups given atypical e. coli colony . transmission electron micrographs of microvilli associated with epithelium cells in the ileum of 21-d-old turkey poults from a) control, b) atypical escherichia coli colony type 1 and c) atypical e. coli colony type 2. the electron micrographs indicate that the microvilli in the poults given atypical e. coli colony type 1 at 1 d of age were beginning to degenerate with membrane separation and were thinner, taller, less numerous than control, and that there was disruption of organelles within the cells. the microvilli in the poults given atypical e. coli colony type 2 at 1 d of age were degenerating with membrane separation, decreased numbers and disruption of the organelles within the cells. (mv: microvilli; tw: terminal web; g: glycocalyx; jc: junctional complex; bar = 34 hm). type 2 at 1 d or e. coli colony type 1 at 6 d were not different from the treatment group given only atypical e. coli colony type 2 at 1 d. mortality data for experiment 2 are presented in table 4 . treatment groups given the cpd in combination with atypical e. coli colony types 1 or 2 given at 1 d and atypical e. coli colony type 1 given at 6 d had significantly elevated mortality during week 1. during week 2, mortality of control poults was significantly lower than all other groups given atypical e. coli colony types 1 or 2 with or without cpd treatment. poults given atypical e. coli colony types 1 or 2 at 1 d experienced the greatest mortality rates among these groups not given cpd. however, the addition of cpd to the treatment regimen further increased mortality rates of those groups given atypical e. coli colony types 1 or 2 at 1 d. nevertheless, by 14 d those poults given cpd and inoculated with atypical e. coli colony types 1 or 2 at 6 d were also showing significant increases in mortality compared to their respective controls. at 21 d, there was significantly elevated mortality in the poults given atypical e. coli colony type 2 at 1 d in comparison to all other groups not given cpd. there was no difference between groups given atypical e. coli colony type 1 at either 1 or 6 d. mortality in the group of poults given the atypical e. coli colony type 2 at 6 d was significantly higher than in their controls but less than in all other treatment groups given the atypical e. coli colony types and not in combination with cpd. the cpd treatment, due to its immunosuppressive effects on b cell function, allowed relatively high rates of mortality during the first 7 d posthatch, and this presumably was due to reduced ability to resist naturally occurring, opportunistic bacterial pathogens. the cpd treatment regimen had an additive effect on mortality in all groups given the atypical e. coli colony types at either 1 or 6 d in comparison to control + cpd and groups not given cpd. the atypical e. coli colony type 2 given at 1 d in combination with cd had the highest mortality rate among all the treatment groups whereas the group given atypical e. coli colony type 1 at 6 d in combination with cpd had the lowest mortality rate. presence of caseous cores in the bursa of fabricius of survivor poults at 21 d is indicated in table 5 . control poults with and without cpd treatment did not show any bursa cores. however, cores of various sizes were found in each of the treatments in which the two atypical e. coli colony types were given. the greatest number of cores was found in poults given atypical e. coli colony type 2 in combination with cpd treatment, and this greater core number coincided with the greatest mortality rate. furthermore, the frequency of bursa core presence in survivor poults appeared to be related to poult age at the time of e. coli exposure and to the cotreatment with cpd, which induced immunosuppression due to its rapid alkylating action on dna in b cell populations. presented in figure 1 are transmission electron micrographs of epithelial cells from the lumen of the ileum in 21-d-old poults in control and atypical e. coli colony types 1 and 2 treatments. control epithelial cells appeared to be normal in every detail. in figure 1a , the microvilli in a control poult are highlighted, and it can be seen that they are erect, in large numbers, and have glycocalyx-covered tips that appeared to be functional. the central core of the microvilli extend into the apical portion of the cell to form a well-defined terminal web. membranes on the microvilli were intact and were continuous with the cell membrane. membrane tight and intermediate junctions and desmosome between epithelial cells appeared normal. organelles below the terminal web of the epithelial cells appeared to be normal and contained rough and smooth endoplasmic reticulum with large numbers of ribosomes, mitochondria, lysosome-like bodies, and some small, smooth membrane-enclosed dense granules that appeared to be similar to recently absorbed lipids reflecting the reduced lipid content of the lower small intestine. in figure 1b , the microvilli on a commonly appearing epithelial cell from the ileum of a 21-d-old poult given atypical e. coli colony type 1 at 1 d are emphasized. the microvilli are more slender, more uneven, and fewer in number than those found in control poults. the membranes of these microvilli also appeared to be degenerating, and the glycocalyx on the tips of the microvilli were absent or appeared to be losing their integrity. the multiple filaments forming the central core of these microvilli appeared to be reduced in number, reflecting the absence or degenerative appearance of the glycocalyx, and this continued to be evidenced by the degenerative appearance of the terminal web. the junctional complex also had a degenerative appearance, as evidenced by a breakdown in the tight junction, loss of integrity of the intermediate junction, and desmosome. organelles within the cytoplasm appeared to be abnormal, especially the mitochondria, which were enlarged and appeared to be nonfunctional. however, there was little evidence to suggest that absorption of nutrient from the lumen was occurring because no lipid containing smooth granules were observed. the rough endoplasmic reticulum was disrupted with few attached ribosomes along with other disrupted membrane structures in the cytoplasm. in figure 1c , the microvilli on epithelial cells from a 21-d-old poult given atypical e. coli colony type 2 at 1 d have lost their integrity. the microvilli were fewer in number, had lost rigor, had degenerating membranes, and the glycocalyx structures were largely absent or abnormal in appearance. the multiple filaments forming the central core of these microvilli appear to be reduced in number, reflecting the absence or degenerative appearance of the glycocalyx, and this continues to be evidenced by the degenerative appearance of the terminal web, which is irregular and not well formed almost to the point of being nonexistent. the junctional complex also appeared to be degenerating, as evidenced by a breakdown in the tight junction, loss of integrity of the intermediate junction, and desmosome. organelles within the cytoplasm appeared to be abnormal, especially the mitochondria, which were enlarged and appeared to be nonfunctional. the rough endoplasmic reticulum was also disrupted and appeared to be degenerating based upon the lack of attached ribosomes and an apparent increase in free cytoplasmic ribosomes. shown in figure 2 are goblet cells in the ileum of poults from a 21-d-old control (figure 2a ) and from a 21-d-old poult exposed to the atypical e. coli colony type 1 (given at 1 d; figure 2b ). in control poults, the secretory vesicles in the apical portion of the goblet cells appeared to be filled with mucous ready for secretion. the reticular area beneath the secretory apical region was well developed, and the endoplasmic reticulum was recognized easily. however, a drastic contrast was presented when goblet cells from poults given the atypical e. coli colony types were examined ( figure 2b ). these goblet cells were depleted of secretory material and the reticular area within the cytoplasm was not distinct. additionally, the nuclei of many of the goblet cells appeared to be degenerating. shown in figure 3 are sections of a goblet cell and adjoining epithelial cells from the ileum of a poult that had been given atypical e. coli colony type 1 at 1 d. however, the third cell type shown in this figure was a macrophage that had migrated through an epithelial cell tight junction or a goblet-epithelial cell junction and was feeding on bacteria in the ileum lumen. this appearance was not an isolated condition but was seen in many sections from poults given one or the other of the atypical e. coli colony types at 1 d. although several viral agents have been isolated from pems-afflicted poults, barnes and guy (1995) and barnes et al. (1996) have indicated that no single virus or combination of viruses has been shown to induce the disease. they suggest that the mortality is caused by one or more specific or novel infectious agents that may act singly or in combination. however, brown (1995) did indicate that a combination of a coronavirus and a serotype 2 birnavirus (infectious bursal disease virus) created a condition analogous to pems. newberry et al. (1993) demonstrated that virulent hemorrhagic enteritis virus (hev) can interact with e. coli strains (o1:k1 and an atypical/untypable strain isolated from a dead hevinfected poult), causing turkey poult colibacillosis and a high rate of mortality shortly after e. coli challenge. presumably, the hev had already damaged the intestinal tract allowing rapid bacterial translocation. this observation was consistent with earlier findings by larsen et al. (1985) and sponenberg et al. (1985) , who also found increased incidence of poor performance and increased mortality as a result of e. coli infections after hev infection. this work was confirmed and extended by van den hurk et al. (1994) , who observed a synergistic effect between hev and e. coli o78 (via an intratracheal route of administration) co-infections in which there was higher mortality (61%) than with e. coli alone (0%), and survivors had decreased bw gain (18% less per day) with the hev and e. coli co-infection. the induction of colibacillosis with high mortality and decreased performance as a result of co-infection with hev and e. coli untypable, o78, and o1 serotypes points out the potential for a virus etiology, which may potentiate the development of pems. the presence of the atypical e. coli colony types 1 and 2 in moribund pems-afflicted turkey poults and the fact that these strains of e. coli cause severe diarrhea, body weight gain depression, bursa cores similar to the pems condition, and high rates of mortality in both infected and infected/cpd-immunodepressed poults, represents the first clear evidence that there may be specific virulent organisms involved in the pems disease condition. whether the atypical e. coli infections in association with pems is a primary or secondary infection remains to be determined. nevertheless, anecdotal evidence from field reports during the summer of 1995 indicated that a new fluoroquinalone antibiotic, sarafloxacin , 4 which has efficacy against gramnegative bacteria such as e. coli and salmonella ssp., stopped mortality in pems-afflicted flocks of turkey poults. however, after the antibiotic had been terminated there was a recurrence of a pems-like condition. 4 abbott laboratories, north chicago, il 60064-4000. as these atypical e. coli strains are sensitive to sarafloxacin and resistant to all other commonly used antibiotics that have been tested (edens et al., unpublished data) , this field observation supported the concept that pems can be due to bacterial agents acting singly or in combination with an unknown viral etiology, which may induce immunodysfunction allowing these atypical e. coli strains to penetrate the gut epithelial barrier. after these e. coli strains become systemic, high rates of mortality and unthriftiness in the survivors can be observed. one of the signs of pems is inhibited or reduced growth accompanied by wasting of the muscle mass (brown, 1995; barnes and guy, 1995; barnes et al., 1996) . bacterial infections are known to result in whole body nitrogen loss proportional to the duration and severity of the disease (beisel, 1984) . in fact, wasting of muscle in the pems condition is a classic example of catabolic losses of amino acid nitrogen from skeletal muscle (beisel, 1984; rennie, 1985) that is used in noncarbohydrate gluconeogenesis. in this study with the atypical e. coli strains, wasting of muscle tissue was not always apparent in every poult, but in many of the survivor poults, there was very little muscle mass remaining at 21 d of age, similar to the condition in field cases of pems. it has been noted that virulent e. coli strains in both chickens (tian and baracos, 1989; leitner and heller, 1992) and turkeys (leitner and heller, 1992) can cause diarrhea, wasting, and mortality. however, it was noted by both groups that stressors, such as inanition after virulent e. coli infection, exacerbated the disease and subsequent mortality. indeed, feed consumption was depressed within 24 h postinfection with virulent e. coli (tian and baracos, 1989 ) and remained depressed for at least 25 d after infection similar to the pems problem associated with field outbreaks. leitner and heller (1992) noted that a brief period of inanition at 5 d of age resulted in rapid penetration of the intestine by virulent e. coli causing bacteremia and colonization of liver and spleen of poults. thus, this suggests that the atypical e. coli strains, which are known to have binding and penetrating ability for avian epithelial cells, have an opportunity to translocate from the intestine to the viscera causing septicemia during the time when pemsafflicted poults exhibit feed refusal but are eating litter that can be heavily ladened with atypical e. coli colony types 1 and 2 (edens et al., unpublished data). however, it is still not clear whether the atypical e. coli strains may be the primary or secondary cause of the feed refusal behavior in pems-afflicted poults, but as an enteroinvasive organism, the atypical e. coli have the potential to cause septicemia quickly. on the other hand, the disruption of the cellular integrity of the intestinal epithelium in response to infections by the atypical e. coli colony types 1 and 2 suggests that there may be another problem associated with pems. simply taken, the loss of functional microvilli and ultrastructural damage to the organelles within the epithelium cells suggests that there is a significant malabsorption problem associated with pems. this conclusion is based upon observations of elevated feed conversion ratios in pems poults (barnes and guy, 1995; brown, 1995; barnes et al., 1996; edens, unpublished data) . it appears clear that part of the reduction in weight gain can be attributed largely to the inability of the infected poults to absorb nutrient from the chymal content of the intestine. furthermore, the observation that there are large numbers of macrophages that migrate through the intestinal epithelium cells to phagocytize bacteria in the lumen of the ileum suggests that in cases of secretory diarrhea both transcellular and paracellular exudation of body fluids might occur which would exacerbate the diarrhea and dehydration associated with pems. additionally, the breakdown of the epithelial cell junctional complex integrity would also aid in the translocation of the atypical e. coli strains and other potentially pathogenic bacteria as well. protection against the infectivity of anaerobic bacteria from the ceca of pems-infected poults was observed in our first studies when killed bacteria were given orally at 1 d followed at 5 d with an oral challenge by a live culture of the anaerobes. the resistance to infection by the 5 d administration of live organisms is not clearly understood. perhaps, the presentation of the killed organisms at 1 d, before the intestinal epithelial cells seal and form a barrier to invasion of microorganisms, allowed the immature immune system in the intestinal tract to rapidly process antigenic information presented by the heat-killed bacterial cells. this would be consistent with the observations that even in ovo administration of antigen can stimulate early immune response in chickens (sharma, 1986; williams et al., 1992) . this finding suggests that antigenic sites on the killed bacterial cell membranes or in the cytoplasm can induce an immune response that can be protective to the poults regardless of the level of and kinds of maternal antibodies passed to the poult. on the other hand, this observation may indicate that there are insufficient maternal antibodies in the newly hatched poult to protect it from the ravages of these and other atypical and pathogenic bacteria and that a specific immune stimulant may be required to develop immunocompetence against specific pathogens such as these atypical e. coli strains. it appears that the dominance of atypical e. coli colony types 1 or 2 in a majority of the pems and flushing cases examined by us to date argues for their involvement in the etiology of pems. the fact that these atypical e. coli strains, colony types 1 and 2 and an additional 27 unique and atypical strains, are resistant to most of the commonly used antibiotics (edens et al., unpublished data) also argues for their involvement in the pems disorder. the fact that these atypical e. coli colony types can cause significant depression in weight gain, cause development of bursa cores similar to the earlier observations of barnes and guy (1995) , brown (1995) , and barnes et al. (1996) , and cause high mortality rates, especially in immunocompromised poults, also argues for their involvement in the pems disease. the fact that these atypical e. coli colony types 1 and 2 are resistant to nearly all commonly-used antibiotics but sensitive to sarafloxacin and that sarafloxacin therapy completely stops pems-associated mortality argues for the inclusion of these bacteria as potential etiologies for pems. therefore, we conclude that the atypical e. coli colony types 1 and 2 are involved in the etiology of the pems disease, but we can not make a definitive statement at this time about whether these e. coli strains are involved in primary or secondary infections associated with pems. furthermore, there are numerous other atypical strains of e. coli that have been isolated from pems and flushing poults that are also antibiotic resistant, and these can not be ruled out as possible etiologies for pems. spiking mortality of turkeys (smt) and related disorders: an update poult enteritis and mortality syndrome ("spiking mortality of turkeys") and related disorders-an update and overview. newsletter, college of veterinary medicine and college of agriculture and life sciences metabolic effect of infection spiking mortality: pathology, performance, and prevention morphological changes and humoral immunity in cyclophosphamide-treated chicks the bursa of fabricius and immunoglobulin synthesis colibacillosis of turkeys exacerbated by hemorrhagic enteritis virus. laboratory studies colonization of escherichia coli in young turkeys and chickens selective suppression of humoral immunity. the effect of cyclophosphamide on the ontogeny of the humoral immune response in chickens use of virulent hemorrhagic enteritis virus for the induction of colibacillosis in turkeys immune system dysfunction during exposure to poult enteritis and mortality syndrome agents muscle protein turnover and wasting due to injury and disease sas user's guide: statistics. version 5 edition embryo vaccination of specific pathogen free chickens with infectious bursal disease virus and tissue distribution of the vaccine virus and protection of hatched chicks against the disease field outbreaks of colibacillosis of turkeys associated with hemorrhagic enteritis virus effect of escherichia coli infection on growth and protein metabolism in broiler chicks (gallus domesticus) commercial broiler studies of marek's disease vaccination in ovo key: cord-347207-1u4i6qmc authors: almomani, huda y.; pascual, carlos rodriguez; al-azzam, sayer i.; ahmadi, keivan title: randomised controlled trial of pharmacist-led patient counselling in controlling hypoglycaemic attacks in older adults with type 2 diabetes mellitus (rose-adam): a study protocol date: 2020-07-29 journal: res social adm pharm doi: 10.1016/j.sapharm.2020.07.012 sha: doc_id: 347207 cord_uid: 1u4i6qmc introduction: hypoglycaemia is one of the most serious adverse effects of diabetes treatment. older adults are at the highest risk to develop hypoglycaemia. several studies have established the important positive role of educational interventions on achieving glycaemic control and other clinical outcomes, however, there is still a lack in studies that evaluate the impact of such type of interventions on hypoglycaemia risk in elderly patients with type 2 diabetes. the purpose of this research is to evaluate the effectiveness of pharmacist-led patient counselling on reducing hypoglycaemic attacks in older adults with type 2 diabetes mellitus. methods: and analysis: this study is an open-label, parallel controlled randomised trial, which will be conducted in the outpatient clinics at the largest referral hospital in the north of jordan. participants who are elderly (age ≥ 65 years), diagnosed with type 2 diabetes mellitus, and taking insulin, sulfonylurea, or any three anti-diabetic medications will be randomly assigned to intervention (sugar handshake) and control (usual care) groups. the sugar handshake participants will have an interactive, individualised, medications-focused counselling session reinforced with a pictogram and a phone call at week six of enrolment. the primary outcome measure is the frequency of total hypoglycaemic events within 12 weeks of follow up. secondary outcomes include the frequency of asymptomatic, symptomatic, and severe hypoglycaemic events, hypoglycaemia incidence, and time to the first hypoglycaemic attack. we will also conduct a nested qualitative study for process evaluation. ethics and dissemination: the human research ethics committee of the university of lincoln and the institutional review board of king abdullah university hospital approved this protocol. the findings of this study will be presented in international conferences and published in a peer-reviewed journal. trial registration number: the study protocol has been registered with clinicaltrials.gov, nct04081766. background 36 hypoglycaemia is the major limiting factor in diabetes management. 1 hypoglycaemia has 37 been found to be associated with cardiovascular events such as myocardial infarction, 38 arrhythmias and cardiovascular mortality as well as cerebral complications such as 39 dementia. 2-6 . additionally, hypoglycaemia can impact patients' quality of life. 7 patients with 40 moderate or worse symptoms of hypoglycaemia are less satisfied with their treatment and 41 report poorer adherence to their medications. 8 the great burden of hypoglycaemia is largely 42 presented by the considerable health care cost resulting from hospitalisations, ambulance 43 services, emergency department visits, and absenteeism from work. 9, 10 44 older adults are the most susceptible age group to develop hypoglycaemia and to 45 experience hypoglycaemia-related complications. 11 the correlation between ageing and 46 hypoglycaemia in type ii diabetes is multifactorial. [11] [12] [13] [14] [15] factors such as physiological changes 47 in elderly that would affect the pharmacokinetics profile of anti-diabetic drugs, 48 comorbidities that affect heart and kidneys, nutrition changes and cognitive impairment that 49 could affect concordance and compliance with treatment regimen [11] [12] [13] [14] [15] . as the population of 50 older adults is increasing, globally; it is expected to see an increase in the prevalence of 51 t2dm in older adults. 16,17 52 in jordan, the prevalence of diabetes in people aged 60 years and over increased 53 significantly over ten years period. 18 it is estimated that the number of elderly persons in 54 jordan will be three times higher in 2050 than it was in 2017, consequently more older 55 adults will be at risk of developing type ii diabetes and diabetes-related complications. 19 56 there are several studies on the association between hypoglycaemia and patient 57 characteristics such as patients' perspectives and attitudes towards diabetes management 58 skills, self-monitoring of blood glucose, and non-adherence to anti-diabetic medications in 59 jordanian population. 20-23 however, there is a dearth of data on the interventions that could 60 potentially prevent hypoglycaemia in such patients, especially the older population. 61 therefore, it is imperative to develop diabetes-related care strategies targeted to this broad 62 population of patients to cope with the growing figures in the future. 63 in the context of diabetes, pharmacist-led care interventions appear to have a pivotal role in 64 glycaemic control, improving self-care activities, medication adherence, improving quality of 65 life, and reducing related complications. 24-28 pharmacist-led care interventions can be 66 individualised to each patient to achieve glycaemic control. 24,29,30 67 however, a few randomised controlled trials (rcts) have investigated the impact of such 68 interventions on hypoglycaemia in adults diagnosed with t2dm. 31 although elderly people 69 are considered heterogenous group with different characteristics from younger adults, none 70 of these trials has explored the effect of educational interventions in this age category. 71 jordanian pharmacy education equips the pharmacists with robust clinical knowledge and 72 clinical skills to work with other healthcare professionals to provide optimal quality care to 73 the patients 32 . therefore, the aim of this study is to evaluate the effectiveness of 74 pharmacist-led patient counselling on preventing hypoglycaemia in older adults with t2dm. 75 educational interventions are considered to be "complex" interventions compared with 76 classic examples of drug interventions in rcts. 33 that is an educational interventions' 77 success or failure could be attributed to a myriad of factors besides the interventions' 78 effectiveness. the factors such as the delivery of the intervention, understanding of the 79 intervention by the patients and implementation of intervention would decide the fate of an 80 educational intervention. 34 for this reason, a process evaluation is valuable to identify 81 whether an intervention works and how, barriers for its implementation, and how to 82 improve it in the future. 34 undertaking qualitative studies to evaluate the interventions 83 during the implementation stage helps in modifying the ongoing interventions as well as the 84 study design to make them more feasible and effective. 35 the study will be a single-centre, two groups, 1:1 parallel, open-label, pragmatic randomised 102 controlled trial with a nested process evaluation embedded; and will be conducted in two 103 clinics at a referral tertiary hospital in jordan. participants will be randomly assigned to 104 either the intervention group hereinafter referred to as the "sugar handshake" group or 105 the control group. figure 1 illustrates the detailed study flow chart. hypoglycaemic episodes pose some challenges as the frequency of hypoglycaemic events is 114 the primary factor in calculating the sample size. 37, 38 we referred to the most relevant study 115 that used a similar outcome measure, methodology and intervention to our research to 116 calculate the needed sample size. 39 the previous study found that the mean total number of 117 hypoglycaemic attacks in the control and the intervention groups were 5.26±6.5 and 118 2.58±2.3 per patient in 24 weeks, respectively. we used the reported frequency of 119 hypoglycaemic attacks in both groups to calculate the minimum required sample size. 120 therefore, we need to recruit at least 184 patients to achieve a significance level of 0.05 and 121 a study power of 80%. 40 accounting for 10% to compensate attrition rate and missing data, 122 the final sample size wished to be recruited is 204 participants (102 in each group). 123 we will recruit older adults who are 65 years and above, diagnosed with t2dm and being 125 prescribed sulfonylurea, insulin, or any three anti-diabetic medications. exclusion criteria 126 include patients unable to understand instructions or to give consent, diagnosed with 127 haemolytic anaemia or haemoglobinopathies, on palliative care for cancer, with advanced-128 stage or end-stage diseases who are terminally ill, diagnosed with psychosis or severe 129 depression, or with life expectancy < 6 months, impaired mental capacity, unwilling to take 130 home glucose measurements or to use the glucose meter, or unwilling to return for follow 131 up. patients who have a partner or a first-degree relative who has been enrolled in the 132 study, are excluded as well. 133 we will use two recruitment methods to reach potentially eligible patients: an 134 advertisement placed in the reception room where patients wait for their appointments, 135 and through direct identification of potentially eligible patients at the recruitment sites. ha 136 will be responsible for recruiting participants in the endocrinology and diabetic foot care 137 clinics meanwhile the research assistant (ra) will recruit from the cardiology clinics. ha and 138 the ra will explain the trial purpose and processes and provide participant information 139 sheets (supplementary file 1) to the interested patients. they will also confirm the eligibility 140 of patients who are willing to participate and will ask them to sign a written consent form 141 we will randomly assign participants to the intervention and control groups on a 1:1 basis. 148 the random sequence will be generated using the website (www.randomization.com) to 149 generate the randomisation schedule. envelopes will be used to conceal the allocation and will 150 be opened by the researcher sequentially at the time of each participant's enrolment. the study 151 envelopes will contain the study name, the participants' codes, the group to which the 152 participants are randomised. the randomisation sequence and the study envelopes will be 153 prepared by a third independent party who will not be involved in the study. the envelopes will 154 be closed and opaque and will be given to the researcher and the ra who are involved in 155 conducting the study. the envelopes that will contain the group allocation will be kept in a 156 locked cabinet in the hospital. 157 158 blinding 159 160 since this is an open-label study, the patients and the data collectors will not be blinded to 161 the assigned group. eligible patients will be informed about the purpose of the study and the 162 study-related activities before they sign the consent form. proper measures will be taken 163 along the trial duration to minimise performance and ascertainment bias that may result 164 from unblinding participants. 165 all participants will be unblinded to the study groups and to the real purpose of the trial at 166 the follow-up visit that would mark the end of the trial. additionally, participants who are 167 assigned to the control group will receive the sugar handshake intervention at the follow-168 up visit. 169 intervention group (sugar handshake) 170 the educational intervention, the sugar handshake, is designed to promote behavioural 172 change to prevent hypoglycaemia. we applied the principles of the behaviour wheel theory 173 (bcw)to design the intervention. 41 our educational intervention would enhance the physical 174 and psychological capabilities of the patients through improving their knowledge and skills in 175 managing and preventing hypoglycaemia. the intervention would also lead to the 176 behavioural change by a conducive environment to promote behaviour change by 177 addressing the physical and cultural needs of the patients. 178 we have structured the reporting of the intervention in line with the tidier (template for 179 intervention description and replication) checklist and guide. 42 participants assigned to the 180 sugar handshake group will receive individualised counselling regarding hypoglycaemia in 181 addition to the usual care provided at the trial sites. the intervention is designed by ha who 182 is a pharmacist with prior work experience in patient counselling and pharmacist-related 183 clinical services. ha has trained the ra on delivering the intervention. the intervention is 184 delivered in two steps i.e., a face-to-face conversation at the enrolment visit followed by a 185 phone call six weeks later. 186 step one: face-to-face conversation at the enrolment visit 187 the sugar handshake intervention will cover comprehensive strategies to prevent and 195 handle hypoglycaemia with instructions related to anti-diabetic medications and managing 196 drug-related problems. table 1 step two: phone call at the 6 th week: 206 participants will receive a 20-minute follow up call at week six of enrolment; so that the first 207 step of the intervention would be reinforced as well as participants' queries/questions 208 would be answered. 209 participants will also be asked about the number and timing of having hypoglycaemic attacks 210 during the first six weeks in the trial to re-consider modifying the intervention components. 211 participants in this group will be offered guidance on hypoglycaemia diagnosis and the 214 proper use of the glucose meters in addition to the usual care. they will also be provided 215 with instructions on hypoglycaemia treatment. as participants in both groups will receive 216 the same information regarding hypoglycaemia recognition, they will have similar ability to 217 recognise hypoglycaemic attacks. at week 6 of enrolment, participants will receive a phone 218 call to remind them of using the glucose meters and documenting hypoglycaemic attacks. 219 of special note, participants who complete the trial duration will receive the intervention at 220 the debrief visit and after returning the hypoglycaemia diaries. 221 all participants in both groups will be given glucose meters and test strips with a 224 demonstration on proper use to measure their blood glucose levels at morning before 225 breakfast daily for 12 consecutive weeks. they will also be handed diaries and instructed to 226 additionally, it is impractical for dm patients to measure their bg levels frequently to 254 diagnose hypoglycaemia. hence, it is imperative to account for both symptomatic and 255 asymptomatic types of hypoglycaemia. 256 we will use diaries to measure types of hypoglycaemia and we will ask participants to fill in 259 the diary on a daily basis for 12 weeks. participants will be asked to fill in the diary with the 260 date of each day and the fasting blood glucose reading. additionally, they will be asked to 261 tick on the boxes for every time they experience severe hypoglycaemia, symptoms of 262 hypoglycaemia at the time of fasting blood glucose measurement, and symptoms of 263 hypoglycaemia during the rest of the day. participants will document a symptomatic attack if 264 the symptoms resolve after receiving the corrective actions. 265 the rate of each type of hypoglycaemia will be measured according to the hypoglycaemia 266 diaries filled by the participants. severe hypoglycaemia will be measured directly according worked and what didn't, and how the study could be improved in future research. 284 we will collect qualitative data using semi-structured interviews from a handful of 285 participants in each study group. we have prepared the interview guide (table 3) based on 286 the objectives of the study and the mrc domains for process evaluation. 287 table 3 : interview schedule 288 you have previously read in the participant information sheet that we are conducting a phone interview as a part of this study and you accepted to participate in it. therefore, i would like to ask you some questions about your experience with the study processes that have been provided to you at the inclusion visit. the information will help us in improving several aspects of the study. the interview should take about 10 minutes. are you available to respond to the questions at this time? 2. i would like to start by asking: how do you describe your participation in the study so far? if needed, the interviewers may explain the question by the follow-up question: how do you rate your participation in the study from good to poor and why? 3. what has worked for you from the study processes that you were asked to do? -why do you think they have? what hasn't worked for you from the study processes that you were asked to do? -why do you think they haven't? 4. from your perspective, how the study could be improved? please consider any aspects of the study that you think could be improved. per-protocol analysis will be conducted including participants who are compliant to 80% or 293 more of the study protocol. 45, 46 the missingness in the primary outcome will be handled 294 under the assumption of "missing at random" rather than "missing completely at random", 295 because we are expecting that the probability of missing data depends on observed 296 covariates or outcomes rather than unobserved data. therefore, the method chosen to 297 handle missing data in the outcomes is multiple imputations. 47,48 298 descriptive analysis will be used across randomised groups and quantitative analysis will be 299 conducted in rstudio version 3.4.2 (28-9-2017). 49 continuous variables will be presented as 300 means, standard deviation, median and interquartile range, meanwhile, categorical variables 301 will be presented as frequencies and percentages. the randomised groups will be examined 302 and compared for all variables. categorical variables will be evaluated using the chi-square 303 test. continuous variables will be tested for normality and based on the distribution of the 304 data, appropriate parametric or non-parametric tests will be used. for example, paired t 305 test or wilcoxon test would be applied to assess the differences in baseline variables 306 between both groups and between participants who completed the trial as well as the 307 participants who will be lost to follow up. 308 the primary and secondary outcomes (total and types of hypoglycaemic attacks) will be 309 measured across the randomised groups and compared using the analysis of covariance 310 (ancova), and the appropriate parametric or non-parametric tests dependent on the 311 normality of distribution. subgroup analysis will also be performed using interaction terms in 312 regression models. 313 we will use logistic regression analysis to examine associations between the categorical 314 outcome variable ( frequent vs infrequent hypoglycaemia episodes) and independent 315 variables such as sex, age, educational level, living arrangements, duration of diabetes, 316 number of current medications, experiencing previous hypoglycaemia, the status of self-317 monitoring of blood glucose, types of anti-diabetic medications, baseline hba1c and 318 interactions between the independent variables. the findings will be also presented as odds 319 ratio and 95% confidence intervals. a p value of less than 0.05 will be considered statistically 320 significant. hypoglycaemia rates will be described with kaplan-meier survival curves, 321 considering the time to the first hypoglycaemic attack as the outcome measure. 50 322 qualitative data analysis 323 the interviews will be audio-recorded then transcribed and translated into the english 324 language. we will use the thematic analysis approach to analyse the collected data for there is a need for protocol amendments through the embedded evaluation process, the 344 changes will be discussed by the supervisory team and will be communicated in writing to 345 the human research ethics committee of the university of lincoln and the institutional 346 review board of kauh. 347 upon completion of the study, we will provide the trial site with an executive summary of 349 the findings in the form of a report. participants would be able to get the results of the study 350 from their health care professionals at the trial site no later than one year after the end of 351 data collection. we are planning to disseminate the study outcomes through peer-reviewed 352 publications and presentations in conferences. we will comply with the authorship eligibility 353 the sugar handshake intervention is designed to be pragmatic and to facilitate 373 transferability of evidence into practice. therefore, pharmacists can easily deliver it to the 374 patients in different working positions including hospitals and community pharmacies. 375 moreover, the delivery of the sugar handshake intervention is cheap and will not cost an 376 extra burden on patients. previous studies concerning the attitudes, religious beliefs, and 377 self-management skills amongst patients with t2dm helped in assuring the appropriateness 378 of contextual and cultural delivery as well as the implementation of the study and the 379 sugar handshake intervention. 20-23 using blood glucose/hypoglycaemia diaries to 380 objectively report and measure several types of hypoglycaemia is another strength. this will 381 facilitate a more accurate measurement of hypoglycaemic events where the concern that 382 patients may forget to report the experienced episodes is reduced. 383 a plausible limitation that warrants consideration is the short follow up duration (12 weeks), 384 which may make it difficult to examine the sustainability of the intervention effect. 385 however, we anticipate that this duration will decrease the dropout rate. moreover, we 386 expect the effect of our intervention to last up to at least six months as concluded by a 387 previous trial. 39 another concern is the enrolment of relatives into different groups upon 388 randomisation, which will introduce contamination bias. therefore, if a patient happens to 389 have a relative who has already participated in the trial, he would be excluded. additionally, 390 participants may not fully adhere to the intervention during the follow-up period. for this reason, they will receive a phone call reminder at week six of enrolment. individualising the 392 intervention according to each patient's lifestyle and potential causes of hypoglycaemia will 393 enhance the adherence to the intervention as well. 394 as this is an open-label study, performance bias and ascertainment bias may result from 395 unblinding participants and the data collectors, respectively. participants in the control 396 group may be less adherent to the trial protocol and more likely to withdraw from the trial. 397 however, efforts will be made to standardise the trial protocol, frequency and time of follow 398 up, and treatment of experienced hypoglycaemia across both groups to minimise 399 performance bias. we also anticipate that the objective measurement of the outcomes 400 would minimise ascertainment bias. 401 the prevalence of diabetes in jordan has been growing rapidly to reach 23.7% in 2017. 60 in 402 light of the lack of awareness regarding diabetes diagnosis, causes, and management we 403 would expect a further increase in the number of jordanians who are diagnosed with 404 diabetes and who would suffer from diabetes-related complications. 20,60 while pharmacists 405 are easier to access than physicians, a possible strategy to mitigate the burden of diabetes is 406 to establish and support the pharmacist-led, patient-oriented services. 61 international hypoglycaemia study group ihs. minimizing hypoglycemia in diabetes diabetes care adverse macrovascular events, and 456 inflammation in the edinburgh type 2 diabetes study. diabetes care association of 460 hypoglycaemia and risk of cardiac arrhythmia in patients with diabetes mellitus: a 461 systematic review and meta-analysis severe 465 hypoglycaemia, mild cognitive impairment, dementia and brain volumes in older adults 466 with type 2 diabetes: the atherosclerosis severe hypoglycemia 470 and risks of vascular events and death 475 effects of severe hypoglycemia on cardiovascular outcomes and death in the veterans 476 affairs diabetes trial. diabetes care predictors of quality of life and other patient-reported outcomes in the 480 panorama multinational study of people with type 2 diabetes impact of 484 symptomatic hypoglycemia on medication adherence healthcare 495 resource use, direct and indirect costs of hypoglycemia in type 1 and type 2 diabetes, 496 and nationwide projections. results of the hypos-1 study management of hypoglycemia in older adults with type 2 diabetes sircar et al m. review of hypoglycaemia in the older adult: clinical implications and 503 cardiovascular disease 507 predicts severe hypoglycemia in patients with type 2 diabetes diabetes management in older adults with chronic 511 curr diab rep older adults: standards of medical care in diabetes-2019 diabetes care the department of economic and social affairs of the united nations. world economic 517 and social survey, 2007: development in an ageing world the burden of disease in older people and implications for 520 health policy and practice. the lancet an increase in prevalence of 524 diabetes mellitus in jordan over 10 years personalized diabetes management: moving from 572 algorithmic to individualized therapy self-efficacy-focused education in persons with 576 diabetes: a systematic review and meta-analysis the role of structured education in the management of 580 hypoglycaemia pharmacy education in jordan: updates when are complex interventions 'complex'? when are simple 586 interventions 'simple'? developing and 590 evaluating complex interventions: the new medical research council guidance process 594 evaluation of complex interventions: medical research council guidance spirit 2013 statement: defining standard 600 protocol items for clinical trials hypoglycemia: a 602 review of definitions used in clinical trials evaluating antihyperglycemic drugs for 603 diabetes hypoglycemia event rates: a comparison 606 between real-world data and randomized controlled trial populations in insulin-607 treated diabetes. diabetes ther intensive individualized 610 reinforcement education is important for the prevention of hypoglycemia in patients 611 with type 2 diabetes the behaviour change wheel: a new method for 617 characterising and designing behaviour change interventions better 621 reporting of interventions: template for intervention description and replication 622 (tidier) checklist and guide hypoglycemia 625 and diabetes: a report of a workgroup of the american diabetes association and the diabetes care understanding 629 the new hba1c units for the diagnosis of type 2 diabetes research council (mrc) guidance. mrc popul health sci res netw the prevention and handling of the missing data a comparative analysis of generalized estimating 647 equations methods for incomplete longitudinal ordinal data with ignorable dropouts using thematic analysis in psychology community-based peer-led diabetes self-655 management effectiveness of hypoaware, a brief 658 partly web-based psychoeducational intervention for adults with type 1 and insulin-659 treated type 2 diabetes and problematic hypoglycemia: a cluster randomized 660 efficacy of structured education in patients with type 2 diabetes mellitus 663 receiving insulin treatment diabetes x-pert programme makes a difference the effect of an education 670 programme (medias 2 bsc) of non-intensive insulin treatment regimens for people 671 with type 2 diabetes: a randomized, multi-centre trial exclusion of older adults from ongoing clinical trials about type 2 diabetes 676 using shared 679 decision-making to address possible overtreatment in patients at high risk for 680 hypoglycemia: the veterans health administration's choosing wisely hypoglycemia 681 safety initiative. clin diabetes publ am diabetes assoc a novel 685 intervention including individualized nutritional recommendations reduces 686 hemoglobin a1c level, medication use, and weight in type 2 diabetes. jmir diabetes time trends in 690 diabetes mellitus in jordan between 1994 and 2017 health care and pharmacy practice in jordan pharmacist-led study in controlling hypoglycemia in older adults with 698 type 2 diabetes mellitus (rose-adam) we would like to acknowledge the university of lincoln and isra university for their support 420 to conduct this study. we would also acknowledge the physicians and nursing staff working 421 at kauh for facilitating recruitment and the study implementation. key: cord-353867-617f90wq authors: ory, marcia g.; lee, shinduk; towne, samuel d.; flores, starr; gabriel, olga; smith, matthew lee title: implementing a diabetes education program to reduce health disparities in south texas: application of the re-aim framework for planning and evaluation date: 2020-08-30 journal: int j environ res public health doi: 10.3390/ijerph17176312 sha: doc_id: 353867 cord_uid: 617f90wq health disparities in diabetes management and control are well-documented. the objective of this study is to describe one diabetes education program delivered in the united states in terms of the re-aim (reach, effectiveness, adoption, implementation, and maintenance) planning and evaluation framework. questionnaires, clinical data, and administrative records were analyzed from 8664 adults with diabetes living in south texas, an area characterized by high health disparities. the diabetes education program delivered was a professionally led 12-month program involving 8 h of in-person workshop education followed by quarterly follow-up sessions. changes in average blood glucose levels over the past 3 months (e.g., a1c levels) were the primary clinical outcome. descriptive and multiple generalized linear mixed models were performed. this community-based initiative reached a large and diverse population, and statistically significant reductions in a1c levels (p < 0.01) were observed among participants with type 2 diabetes at 3 months. these reductions in a1c levels were sustained at 6-, 9-, and 12-month follow-up assessments (p < 0.01). however, considerable attrition over time at follow-up sessions indicate the need for more robust strategies to keep participants engaged. for this diabetes education program, the re-aim model was a useful framework to present study processes and outcomes. health disparities are often geographically bound and occur more frequently in impoverished populations characterized by low socio-economic status and a dearth of available healthcare resources [1] [2] [3] [4] . the u.s.-mexico border is impacted by extremely high disparities in income, education, and healthcare access, and these social determinants of health make this region among the nation's figure 1 illustrated the 27 counties formally included in the healthy south texas initiative [30] , and the counties in which the diabetes education program was offered were marked with a red dot. counties along the us-mexico border were included, as well as areas adjacent to border counties, which were all referred to as south texas. including urban, small town, and rural areas, the overall estimated population in these counties in 2015 was approximately 2.8 million, and these areas were among the most impoverished in the nation in terms of socioeconomic status and lack of healthcare services [31, 32] . as a community-driven initiative, inclusionary criteria were broad with the intent of serving those both directly and indirectly involved in a person's diabetes prevention and management. while the focus was on adults with type 2 diabetes, persons with pre-diabetes and type 1 diabetes were invited, as well as family members or friends providing care for persons with diabetes. as indicated in figure 1 , the formal diabetes education program was offered in 14 of the 27 south texas counties in two primary hubs clustered around nueces and hidalgo counties. given the community-based nature of this initiative and the desire to reach as many participants as possible to show widespread program penetration, participants were recruited from a variety of sources including screenings at health fairs, referrals from healthcare facilities, outreach to community partnerships with flyers and other social media, and self-referrals. although there was no attempt to standardize referral sources, which differed by organizational sponsorship and location, promotional materials (e.g., flyers) were standardized with a uniform healthy south texas brand. the diabetes education program was a recognized american diabetes association (ada) program that was professionally led but also included community health workers for outreach and programming assistance [27] . all ada-recognized programs provided quality education for people with diabetes and followed the national standards for diabetes self-management education and support (dsmes) guidelines [33] . ada-recognized diabetes education programs were eligible for reimbursement through many federal and private u.s. insurers [34] . offered in both spanish and english, the program consisted of 8 hours of face-to-face educational workshop sessions led by at least one trained health professional (e.g., registered nurse (rn), registered dietician (rd), pharmacist, or certified diabetes educator). workshop sessions were followed with brief (e.g., 15-30 min) in-person individualized follow-up educational and support sessions offered on a quarterly basis for a year. focal workshop topics included a discussion of, as well as hands-on experiential learning about what diabetes is, blood glucose monitoring, given the community-based nature of this initiative and the desire to reach as many participants as possible to show widespread program penetration, participants were recruited from a variety of sources including screenings at health fairs, referrals from healthcare facilities, outreach to community partnerships with flyers and other social media, and self-referrals. although there was no attempt to standardize referral sources, which differed by organizational sponsorship and location, promotional materials (e.g., flyers) were standardized with a uniform healthy south texas brand. the diabetes education program was a recognized american diabetes association (ada) program that was professionally led but also included community health workers for outreach and programming assistance [27] . all ada-recognized programs provided quality education for people with diabetes and followed the national standards for diabetes self-management education and support (dsmes) guidelines [33] . ada-recognized diabetes education programs were eligible for reimbursement through many federal and private u.s. insurers [34] . offered in both spanish and english, the program consisted of 8 h of face-to-face educational workshop sessions led by at least one trained health professional (e.g., registered nurse (rn), registered dietician (rd), pharmacist, or certified diabetes educator). workshop sessions were followed with brief (e.g., 15-30 min) in-person individualized follow-up educational and support sessions offered on a quarterly basis for a year. focal workshop topics included a discussion of, as well as hands-on descriptive statistics (mean and standard deviation or frequency and percentage) were used to describe the characteristics of participants. not all implementation sites collected the exact same set of variables; thereby, the descriptive statistics reflected available data (i.e., not all variables had the same number of missing cases). bivariate analyses (e.g., independent t-tests or chi-square tests) were performed to compare the characteristics of participants recruited during the first biennium and second biennium. next, retention rates were estimated for each follow-up session. as a part of retention analysis, characteristics of participants who attended and did not attend each follow-up session were described and were then compared using bivariate analyses. this study used data collected between september 2015 and december 2019. although having four additional data collection months after the second biennium ended in august 2019 allowed for more follow-ups, not all participants had an opportunity to complete all their follow-up sessions. intervention delivery dates were used to identify and exclude participants from the retention analyses based on their eligibility to participate in the follow-up. for example, participants who participated in the workshop after june 2019 were excluded from the retention analyses for the 6-month follow-up. similarly, participants who participated in the workshop after march 2019 were excluded from the retention analyses for the 9-month follow-up; and those who participated in the workshop after december 2018 were excluded from the retention analyses for the 12-month follow-up. multiple generalized linear mixed models with participant-level random intercepts were fitted to examine changes in a1c level over time among participants with pre-diabetes or type 2 diabetes. persons with type 1 diabetes (n = 221) or gestational diabetes (n = 12) were not included in the regression models due to small sample sizes. separate models were performed for the first and second biennia. the first set of models examined changes in a1c levels over time in participants with type 2 diabetes (n = 1922 in the first biennium and n = 2733 in the second biennium). the second set of models examined changes in a1c level over time in participants with pre-diabetes (n = 380 in the first biennium and n = 482 in the second biennium). the third set of models examined any differences in the changes in a1c levels over time based on diabetes type (pre-diabetes or type 2 diabetes) (n = 2302 in the first biennium and n = 3215 in the second biennium). the next set of models examined changes in a1c level among participants with type 2 diabetes by their baseline a1c level (i.e., 4.0-5.6%, 5.7-6.4%, 6.5-7.9%, 8.0-8.9%, 9.0-9.9%, 10.0-11.9%, and 12.0% or higher) (n = 1912 in the first biennium and n = 2722 in the second biennium). in addition, a separate regression model was used to examine any racial/ethnic differences in changes in a1c level (n = 2302 in the first biennium and n = 3215 in the second biennium). all regression models controlled for covariates including age, sex, race/ethnicity, education, language, and baseline bmi category. given that there were only 5 participants reported speaking "other" as their primary language, they were excluded from the regression analyses. a significance level of 0.01 was used. this study involved retrospective reviews and analyses of limited data, and this study was reviewed and approved by the institutional review board at texas a&m university (irb2019-0225d). results were presented based on the five re-aim elements to provide a case study of this applied research about diabetes self-management education [29] . reach was defined as "the absolute number, proportion, and representativeness of individuals who are willing to participate in a given initiative, intervention, or program, and reasons why or why not" [36] . the number of persons who participated in the program and their general characteristics were tracked (table 1 ). the majority of program participants were aged between 45 and 64 years (55.3%), female (61.6%), hispanic (68.6%), and had high school or less education (72.2%). most participants reported english as their primary language (89.5%) ( table 1 ). the intervention could be attended by individuals with pre-diabetes or diabetes as well as their family and friends. among the program participants with a recorded diabetes type, nearly 15% had pre-diabetes and more than 80% had type 2 diabetes. the mean a1c level was 6.2% among those with pre-diabetes, 8.7% among those with type 1 diabetes, and 8.6% among those with type 2 diabetes. * p < 0.01; ** p < 0.001; a . p-values from bivariate analyses (e.g., independent t-tests or chi-square tests) comparing the characteristics of participants recruited during the first biennium and second biennium; b . chi-square comparison was performed after excluding "other" language (n = 8650); c . in total, 21.7% of diabetes type records were missing, and frequency and percentage were calculated based on available data (n = 6788); d . mean and standard deviation of baseline a1c percentage measures were estimated among those with pre-diabetes and type 1 and type 2 diabetes. bmi, body mass index. a1c, average blood glucose level over the past 3 months. there were statistically significant differences in characteristics of the participants recruited during the first and second biennium (table 1) , indicating changes in program participant profiles and expanded program reach. compared to participants recruited during the first biennium, those recruited during the second biennium tended to be younger (22.0% vs. 17.1% aged 18-44 years), normal or overweight (32.4% vs. 29.6%), and not knowing their diabetes type (2.0% vs. 0.4%) ( table 1) . in addition to considering initial recruitment, it was important to assess population representativeness over time. the program consisted of an educational session and four quarterly follow-ups to track behavioral goals and clinical outcomes. however, less than 50% of participants attended the first scheduled quarterly follow-up session at 3 months, and the attendance rate for the subsequent follow-up sessions further decreased to 30.5% at 6 months, 23.0% at 9 months, and 18.4% at 12 months. the attendance rates at 9 and 12-month follow-up sessions were higher during the second biennium than during the first biennium (24.8% vs. 21.0% at 9 months and 21.1% vs. 15.9% at 12 months). table 2 shows the number and characteristics of overall program participants who attended and did not attend at each follow-up assessment. for all four follow-ups, retention rates were higher among those in the older age group, females, non-hispanic individuals, those with more than a high school education, and those whose primary language was spanish ( table 2) . retention rates tended to be lowest for those with bmis classified as being underweight (table 2) . among participants with type 2 diabetes, those not attending a follow-up session at any given time point had significantly higher baseline a1c levels than those who attended the follow-up session ( table 2) . among participants with pre-diabetes or type 1 diabetes, no statistically significant differences were observed based on baseline a1c level attending a follow-up session at any given time point (table 2 ). at the 3-month follow-up, the retention rate was significantly different based on participants' diabetes type ( table 2 ). the retention rate was highest among those with pre-diabetes (54.9% at 3 months) and type 2 diabetes (51.3%), followed by those with type 1 diabetes (44.3%) and those who were unaware of their diabetes type (35.5%) ( table 2 ). however, the association between retention rates and diabetes type was not statistically significant at subsequent follow-ups (table 2) . effectiveness was defined as "the impact of an intervention on important individual outcomes, including potential negative effects, and broader impact including quality of life and economic outcomes; and variability across subgroups (generalizability or heterogeneity of effect)" [36] . this study evaluated changes in a1c level among participants from baseline to each follow-up time point. in both the first and second biennium, a statistically significant reduction in a1c level was observed among participants with type 2 diabetes at the 3-month follow-up (b = −0.97, p < 0.001 in the first biennium and b = −1.13, p < 0.001 in the second biennium), and this a1c level reduction was sustained at the 6-month (b = −0.98, p < 0.001 and b = −1.20, p < 0.001), 9-month (b = −1.10, p < 0.001 and b = −1.19, p < 0.001), and 12-month (b = −0.95, p < 0.001 and b = −1.32, p < 0.001) follow-up. for example, for participants with type 2 diabetes who joined during the second biennium, the average a1c level dropped from 8.6% at baseline to 7.5% at 3 months, and this a1c level reduction was sustained at subsequent follow-ups (7.4% at 6 months, 7.3% at 9 months, and 7.3% at 12 months). on average, participants with pre-diabetes had a1c levels that remained controlled (<6.5%) from baseline to the subsequent follow-ups. for example, in the first biennium, a statistically non-significant reduction in a1c level was observed among participants with pre-diabetes at all follow-ups (b = −0.12 and p = 0.06 at 3 months; b = −0.13 and p = 0.07 at 6 months; b = −0.12 and p = 0.13 at 9 months; and b = −0.12 and p = 0.19 at 12 months). participants who had type 2 diabetes showed significantly greater reductions in a1c level than those with pre-diabetes (p < 0.001 for the interaction term between time and diabetes type in both the first and second biennia) ( figure 2 ). table 2 . characteristics of the program participants who attended and did not attend 3-, 6-, 9-, and 12-month follow-up assessments. p-values from bivariate analyses (e.g., independent t-tests or chi-square tests) comparing the characteristics of participants who attended and did not attend the follow-up session; e . excluded 5 participants who reported "other" primary language to prevent possibility of identifying the individuals; f . excluded 12 participants who reported having gestational diabetes to prevent possibility of identifying the individuals; g . high missing response rates and frequency and percentage were calculated based on available data (n = 6776 at 3 months, 6400 at 6 months, 5834 at 9 months, and 5288 at 12 months); h . mean and standard deviation of baseline a1c percentage measures were estimated among those with pre-diabetes, type 1 diabetes, or type 2 diabetes. bmi, body mass index. a1c, average blood glucose level over the past 3 months. significant reduction in a1c level was observed among participants with pre-diabetes at all followups (b = −0.12 and p = 0.06 at 3 months; b = −0.13 and p = 0.07 at 6 months; b = −0.12 and p = 0.13 at 9 months; and b = −0.12 and p = 0.19 at 12 months). participants who had type 2 diabetes showed significantly greater reductions in a1c level than those with pre-diabetes (p < 0.001 for the interaction term between time and diabetes type in both the first and second biennia) (figure 2 ). (a) (b) figure 2 . estimated changes in a1c from baseline to 3, 6, 9, and 12-month follow-up after adjusting for age, gender, ethnicity, education, language, and baseline bmi category, by diabetes type and biennia: (a) first biennium; (b) second biennium. a1c, average blood glucose level over the past 3 months. bmi, body mass index. changes in a1c values over time among participants with type 2 diabetes were also examined based on baseline a1c values. estimated changes in a1c by baseline a1c values show similar trends over time among the participants enrolled during the first biennium ( figure 3a ) and second biennium (figure 3b ). for both biennia, there was a statistically significant modification effect of the baseline a1c level on changes in a1c values over time (p < 0.001 for the interaction term between time and the baseline a1c level in both the first and second biennia). participants with high baseline a1c values (e.g., 8% or higher) achieved a decline in their a1c values at the 3-month follow-up assessments and maintained during the subsequent follow-ups. the estimated a1c level decline was most pronounced for those with highest baseline a1c values (e.g., 12% or higher). on average, participants with controlled diabetes at the baseline remained in control during the subsequent follow-ups. level on changes in a1c values over time (p < 0.001 for the interaction term between time and the baseline a1c level in both the first and second biennia). participants with high baseline a1c values (e.g., 8% or higher) achieved a decline in their a1c values at the 3-month follow-up assessments and maintained during the subsequent follow-ups. the estimated a1c level decline was most pronounced for those with highest baseline a1c values (e.g., 12% or higher). on average, participants with controlled diabetes at the baseline remained in control during the subsequent follow-ups. in a separate regression model, which included the interaction term between time and race/ethnicity, there was no statistically significant differences in changes in a1c values over time among participants with pre-diabetes or type 2 diabetes (p = 0.11 in the first biennium and p = 0.25 in the second biennium). adoption was defined as "the absolute number, proportion, and representativeness of settings and intervention agents (people who deliver the program) who are willing to initiate a program, and why" [36] . in lieu of being able to quantify adoption, the general adoption approach was described. the coastal bend health education center (cbhec) in corpus christi served as the healthy south texas regional headquarters. the texas a&m south texas center, mcallen campus, served as a second regional hub. while planning the intervention roll-out, a hub-and-spoke model was determined to be the most effective strategy in which a central "hub" supports multiple "spokes" in communities to provide a range of services. with this approach, cbhec and the mcallen campus identified other regional partners to help recruit and deliver the program. due to the staffing requirements (e.g., needing a health professional to lead the educational workshops and sessions), the program was not delivered in all counties; rather, it was more selectively offered around the two hubs-with the spokes representing adjacent service areas. in accordance with ongoing collaborative health promotion activities in their respective local communities, both cbhec and the mcallen campus were able to call upon their extended healthcare and public health networks for program delivery assistance. regional partners that helped deliver the program represented diverse community and clinical entities including community-based organizations, federally qualified health centers, hospitals, clinics, pharmacies, school districts, academic institutions of higher education, state agencies and not-for-profit social service organizations, behavioral health organizations, and city and county government offices. partnerships varied with some organizations assuming a fuller responsibility for delivering courses on their own, some helping with overall recruitment, and some solely offering physical space for classes. implementation was defined as "the intervention agents' fidelity to the various elements of an intervention's key functions or components, including consistency of delivery as intended and the time and cost of the intervention. adaptations are also included in this re-aim element" [36] . as an ada-recognized program, there was a need to demonstrate that ada principles of diabetes education were being followed. this involved an annual review by a designated quality control coordinator to review delivery processes, certify them as compliant, or note aspects to be corrected. program standardization across sites was facilitated by having a centralized hub for training and data reporting, in coordination with the scientific-administrative oversight functions provided by healthy south texas leadership. cbhec trained staff in program delivery using a standardized program manual and holding periodic problem-solving feedback sessions with regional program managers and implementers. adaptations to the program were discussed with the evaluation team to enhance program reach and retention. for example, program staff reported that many participants found it difficult to attend a single-day, 8-h workshop. therefore, other options were offered such as spreading the workshop over multiple days in two 4-h sessions or four 2-h sessions. program costs were not tracked in the first biennium, but efforts were made to retrospectively estimate actual program costs based on personnel, supply and space costs toward the end of the second biennium. the program was estimated to cost between usd 800 and 1200 per participant, albeit with substantial variation based on how established the program was delivered at different sites, methods of recruitment, and the number of participants in each class. a major indicator of program implementation was how many participants engaged in all program activities (e.g., the initial educational workshop plus four quarterly follow-up sessions to track behavioral goals and clinical outcomes over time). as seen in table 2 , only about 50% of participants attended the first quarterly follow-up session at 3 months, and attendance rates decreased for the subsequent follow-up sessions. given that process evaluation activities were initially built into the program evaluation, program staff were made aware of this issue concerning attendance. subsequent action was taken in an attempt to bolster follow-up rates. retention rates at 9 and 12-month follow-up sessions during the second biennium were significantly higher than the rates during the first biennium (i.e., 24.8% vs. 21.0% at 9 months and 21.1% vs. 15.9% at 12 months). maintenance was defined at the individual level as "the long-term effects of a program on outcomes after a program is completed" and at the setting level as "the extent to which a program or policy becomes institutionalized" [36] . at the individual level, the trajectory of a1c level change over time during the 12-month intervention period has already been reported in the effectiveness section (figures 2 and 3) . at the setting level, programs included within the healthy south texas initiative were intentionally designed to be housed within and delivered by established community partners who could draw upon their existing networks to facilitate programmatic spread and sustainability. for legislative feedback purposes, the amount of actual and in-kind dollars the health science center leveraged during the first two biennia was calculated. from private and public sources, over usd 15,000,000 was identified in direct support and in-kind dollars for the healthy south texas initiative (including delivery of the diabetes education program, as well as other disease prevention and health promotion activities) by governmental and nongovernmental entities. the program is still ongoing with a legislative commitment for a third biennium (september 2019-august 2021), and program delivery remains a core function of the two regional hubs. the healthy south texas diabetes education program reached and benefitted large numbers of participants in a region with documented health inequities that have perpetuated health disparities [13] . utilizing the re-aim framework for both planning and evaluation enabled the study team to describe this diabetes program in terms of its reach, adoption, implementation, effectiveness and maintenance [37] , and explore the unique challenges faced when applying and assessing re-aim elements in community settings [38, 39] . this community-based initiative reached a large and diverse population in this region, thus supporting the external validity of the positive results observed. the hispanic population accounted for over two-thirds of the total population in the service region [40]; hence, the ability to provide the program in spanish was a critical element that enabled the program to reach this population. an estimated 65,000 persons were served in the first two biennia across a broader range of diabetes outreach and education activities implemented by the texas a&m health science center healthy south texas initiative, in which the diabetes education program was a single component. this initiative capitalized on its understanding of the local community and organizational context, which has been deemed critical for the implementation and dissemination of other health promotion programs [41] . this enabled the implementation sites to draw upon highly visible stakeholders and their diverse relationships with community and clinical organizations for outreach and delivery. culture, language, and access to resources are known barriers to access to care in the hispanic population with type 2 diabetes [42] , and collaboration with diverse local community and clinical entities enabled recruitment of culturally competent staff and facilitators to reach the hispanic population, who are likely to be an underserved population in the region. this study has generated several general take-home messages to be considered before implementing future health promotion initiatives. foremost, program planners should conduct community needs assessments and/or engage stakeholders from the communities they wish to target during initial planning, when assessing feasibility, and when deciding which components to include (e.g., considering potential cultural competency considerations and the need to tailor materials). while research studies typically need to offer incentives for participant recruitment [43] , the healthy south texas initiative promoted program adoption by providing sites with necessary materials and/or subcontracted for services, which allowed programs to be offered free to participants who may have otherwise lacked resources to pay for such services. this was a critical component that helped alleviate or limit the participants' financial burden as a major barrier to participation, particularly among the socioeconomically disadvantaged population. when considering the generalizability of this evaluation in future settings and populations, program implementers and other key stakeholders should consider this option, where possible, as it may determine whether or not participants can access similar services in other initiatives. balancing fidelity to program implementation with the need for adaptation remains challenging in translational research [44] . over the past two biennia, many of the recommended re-aim strategies for improving the implementation processes were implicitly followed and should serve as explicit guideposts in future studies [29, 37] . for example, some sites adapted intervention delivery modes and routinized follow-up reminder contacts. other sites switched the health professional type needed to lead workshops to accommodate local needs and preferences. for example, one hub determined that in their setting a registered dietician was preferable to a registered nurse, and the ada offered some latitude when selecting the specific type of health professional used to lead workshops without jeopardizing the ada-recognized status or program fidelity. of particular note, the high attrition rates for follow-up visits raises issues about the feasibility and appropriateness of the current diabetes education program structure. the first biennium was a learning curve for the problem facilitators and implementation sites, and additional activities (e.g., reminder calls) were considered and conducted to enhance follow-up rates in the second biennium. reviewing other successful chronic disease self-management programs [45] , the difficulties of expecting the targeted population to consistently engage in intervention sessions over a 12-month period were recognized. hence, one major adaptation for future programming is to consider modifications of the current diabetes education program and/or the development of a new iteration of such a program with a shorter active intervention period. long-term supports are still valuable for participant success and should still be incorporated in some capacity (e.g., by their healthcare provider, virtually, telephonically). the effectiveness of the diabetes education program demonstrated significant decreases in a1c levels over time which were clinically meaningful [46] . however, a closer look provides guidance for future targeting, which is a major concern in intervention research [47] . while reducing a1c levels is a clinical goal for persons with elevated a1c levels, targeting those with a1c values of 8 and above has greater potential to be most cost effective, given these a1c levels are associated with the most diabetes complications and need for costly medical care [19] . findings from our study indicate that self-management programs adhering to ada best practices can achieve large decreases in a1c levels among this population. maintenance of individual and system-level outcomes is often the most challenging re-aim element to achieve [36, 48, 49] . it is critical to be aware of how context can influence outcomes at both levels. the practical robust implementation and sustainability model (prism) framework, which is now an integral part of the re-aim framework [50] , helps us understand the contributory role of recipients, implementation and sustainability, infrastructure, and the external environment. one successful maintenance strategy at the individual maintenance level was to pair the diabetes education program with opportunities for class-based exercise programming throughout the year. based on feedback from program managers, participants seemed to enjoy these sessions and kept them engaged in the diabetes education program. additionally, the diabetes education program was seen as a core component of the two healthy south texas regional hubs, and organizational efforts are underway to build capacity and support for continued delivery through a network of concerned partners. in the current third biennium of state funding (september 2019-august 2021), program staff are fully aware of the importance of context during these unprecedented times. thus, different options for long-term sustainability are being explored, noting that the current covid-19 crisis may make future state support less likely due to budgetary considerations [51] . toward this end, strategies for defining and promoting the value proposition of this and other health education programs are being formulated. for example, fee-for-service options, seeking insurance reimbursement for recognized diabetes management programs, and/or providing the program for a modest charge to community or healthcare organizations as a community benefit are being investigated. to assist in making a value proposition based on the potential return on investments made, economic evaluation studies that can demonstrate objective value in multiple ways (e.g., monetary outcomes, measures of gains in quality of life, reductions in years of potential life lost, reductions in potentially preventable hospitalizations) are recommended. such studies are important to inform local, state, and national stakeholders about the potential return on investment for these and similar studies and should complement other evaluation activities of similar initiatives to reach a broader audience. while there were many strengths in this community-based study, there were some limitations that must be acknowledged. this is a case study of a single diabetes education program in a geographic area. hence, the findings, while promising, may not be generalizable to all community diabetes prevention and control programs or to other areas with differing population characteristics, settings, or varying levels of baseline risk (e.g., a1c level). additionally, in contrast to academic-based research studies, service delivery often has priority in community-driven programs relative to data collection and management processes, which can limit the types and quality of data collected. for example, although there was a record of engagement by partnering organizations, there was no record of the extent to which organizations agreed to participate when asked. furthermore, while a large sample size was used, lack of randomization in community settings could be impacted by selection bias. the re-aim model provided a general framework for reporting the planning and evaluation of this initiative. as such, full measures on all re-aim dimensions were not collected. while this is a potential shortcoming, it is also aligned with the recognition that applying the re-aim model in "real-world" studies does not depend on the assessment of all five dimensions [39] . despite the relatively large numbers of community residents served by the diabetes education program, the proportion reached relative to people with diabetes residing in these south texas counties was still minimal, given the high rates of adults with diabetes in the south texas region [52] . further, the large attrition rate for follow-up sessions was considerable, which may highlight recruitment or fidelity issues and introduce self-selection and/or a healthful bias (i.e., participants with type 2 diabetes with lower a1c levels had better retention rates at all follow-up sessions). finally, data were not collected longer than 12 months following the diabetes education program workshop; therefore, an assessment of long-term clinical control and management among participants was not possible. similarly, as the healthy south texas initiative is still ongoing, long-term program delivery and institutionalization post external funding could not be assessed. however, lessons can be learned from this initiative that advance knowledge about research translation. in line with guidelines for implementing evidence-based diabetes prevention and control programs [53] , two successful strategies were employed to enhance reach with the ultimate goal of reducing health disparities in underserved populations. first, community health workers were integral to participant recruitment because they were seen as trusted members in the community [54] . another successful strategy was establishing and using diabetes health champions [55] (i.e., persons in the program who had successfully lowered their own a1c levels) to serve as program promoters who could engage populations typically characterized as "hard to reach" and who were unaware of, or previously uninterested in, participating in health promotion programs [56] . the diabetes education program provided an example of dedicated effort to meet the overall public health goal of diabetes prevention and management for all americans, especially among those experiencing a multitude of social determinants of health inequities [57] . offering the diabetes education program through two regional hubs was a major advantage for program reach and adoption as well as launching the initiative quickly. overall, the diabetes education program, as part of the healthy south texas initiative, made a substantial impact on the target area reaching diverse and potentially at-risk populations with measured benefits as evidenced in the current study. for long-term programmatic sustainability, such programs will need to be viewed as essential to routine diabetes regional risk: mapping single and multiple chronic conditions in the united states regional differences in rural and urban mortality trends; nc rural health research program: chapel hill trends in socioeconomic status-related differences in mortality among people with chronic obstructive pulmonary disease understanding associations among race, socioeconomic status, and health: patterns and prospects healthy border 2020: a prevention & health 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health champions approaches to recruiting 'hard-to-reach' populations into re-search: a review of the literature this article is an open access article distributed under the terms and conditions of the creative commons attribution (cc by) license the authors would like to thank the healthy south texas team within the texas a&m health science center for their work to deliver and evaluate this program. a special thanks is given to the diabetes education program trainers, educators, and staff in corpus christi and mcallen who are continually dedicated to improving lives in south texas. additionally, the authors would like to thank carrie l. byington, former senior vice president of the texas a&m university health science center and vice chancellor for health services of the texas a&m university system (currently executive vice president and head of uc health at the university of california) and susan ballabina, deputy vice chancellor for texas a&m agrilife for their leadership role in the healthy south texas initiative during the study period. the authors declare no conflict of interest. key: cord-343982-ymaql0hx authors: carr, m. j.; wright, a. k.; leelarathna, l.; thabit, h.; milne, n.; kanumilli, n.; ashcroft, d. m.; rutter, m. k. title: impact of covid-19 on the diagnoses, hba1c monitoring and mortality in people with type 2 diabetes: a uk-wide cohort study involving 13 million people in primary care date: 2020-10-27 journal: nan doi: 10.1101/2020.10.25.20200675 sha: doc_id: 343982 cord_uid: ymaql0hx background: the covid-19 pandemic has already disproportionately impacted people with diabetes. timely diagnosis and appropriate monitoring in people with type 2 diabetes (t2d) are necessary to reduce the risk of long-term complications. methods: we constructed a cohort of 23m patients using electronic health records from 1709 uk general practices registered with the clinical practice research datalink (cprd), including 13m patients followed between march and july 2020. we compared trends in diagnoses, monitoring and mortality in t2d, before and after the first covid-19 peak, using regression models and 10-year historical data. we extrapolated the number of missed or delayed diagnoses using uk office for national statistics data. findings: in england, rates of new t2d diagnoses were reduced by 70% (95% ci 68%-71%) in april 2020, with similar reductions in northern ireland, scotland and wales. between march and july, we estimated that there were more than 45,000 missed or delayed t2d diagnoses across the uk. in april, rates of hba1c testing in t2d were greatly reduced in england (reduction: 77% (95% ci 76%-78%)) with more marked reductions in northern ireland, scotland and wales (reduction: 84% (83-84%)). reduced rates of diagnosing and hba1c monitoring were particularly evident in older people, in males, and in those from deprived areas. mortality rates in t2d in england were more than 2-fold higher (110%) in april compared to prior trends, but were only 66% higher in northern ireland, scotland and wales. interpretation: as engagement with the nhs increases, healthcare services will need to manage the backlog and the expected increase in t2d severity due to delayed diagnoses and reduced monitoring. older people, men, and those from deprived backgrounds with t2d may be groups to target for early intervention. funding: national institute for health research (nihr) greater manchester patient safety translational research centre the first wave of the covid-19 pandemic has had major health and economic effects across the world. so far in the uk, there have been more than 50k covid-related deaths 1 with disproportionate impacts in people with diabetes; 2 nearly a third of all covid-related deaths having occurred in people with diabetes. 3 the impact on the nhs, and in particular on diabetes services, has been enormous, with the suspension of much routine care. as we enter the second wave in the uk, there is an urgent need to minimise the harm done through suspension of routine services and to prioritise care and resources to areas of greatest need. the diagnosis of type 2 diabetes occurs almost exclusively in primary care. 4 timely diagnosis is critically important as delays will increase the risk of long-term complications. there is limited data on the indirect consequences of the covid-19 pandemic on the incidence and monitoring of diabetes in primary care. likewise, there is limited information on covid-19 impacts on mortality rates in people with diabetes during and after the first wave of covid-19. therefore we used a large primary care longitudinal dataset, broadly representative of the uk population, aiming to compare: i) the uk-wide incidence of type 2 diabetes; ii) the frequency of hba1c testing; and iii) mortality rates in people with type 2 diabetes, before and after the nationwide covid-19 lockdown in march 2020. we compared observed and predicted rates using data covering ten years prior to the pandemic. since older people and more socially disadvantaged groups have been disproportionally affected by covid-19 infections, and since the same groups may be more adversely impacted by the unintended consequences of government interventions, we aimed to study variation in outcomes by gender, age group, deprivation level and region. we examined primary care electronic health records using the clinical practice research datalink (cprd) aurum and gold databases. 5, 6 the study population consisted of 19,763,481 patients from 1,368 general practices in england, with a further 36 practices in northern ireland (339,153 patients), 195 practices in scotland (1,804,938 patients), and 110 in wales (1,277,009 patients). a total of 22,717,623 patients were included for estimating the expected rates in the pre-covid-19 period (january 2010-february 2020). in line with guidance from the cprd's central administration, aurum and gold databases were analysed separately. the cprd contains anonymised consultation records and includes patient demographic information, symptoms, diagnoses, medication prescriptions, and date of death. we also examined practice-level index of multiple deprivation (imd) quintiles, 7 a measure representing an area's relative level of deprivation, ranked within each uk nation. . cc-by 4.0 international license it is made available under a perpetuity. is the author/funder, who has granted medrxiv a license to display the preprint in (which was not certified by peer review) preprint the copyright holder for this this version posted october 27, 2020. ; https://doi.org/10.1101/2020. 10.25.20200675 doi: medrxiv preprint to enable comparisons of rates before the covid-19 outbreak, during its peak and after the peak, we included patient records from january 2010 that established long-term trends and patterns of seasonality. we focussed primarily on reporting observed versus expected rates from 1/3/20 to 10/7/2020. first, we estimated incidence rates of type 2 diabetes diagnoses, new prescriptions for metformin (the most commonly prescribed medication in new-onset type 2 diabetes) and insulin, and rates of hba1c testing and mortality in people with type 2 diabetes. incident type 2 diabetes was identified from read/snomed/emis codes used in cprd gold and aurum (see https://clinicalcodes.rss.mhs.man.ac.uk). the cprd aurum and gold databases were analysed separately, with data from aurum restricted to english practices and gold providing information on practices in northern ireland, scotland and wales. the use of two discrete data sources also enabled independent replication of our findings. all code lists and medication lists were verified by two senior clinical academics (a diabetologist: mkr, and a senior academic pharmacist: dma). for each patient, we defined a 'period of eligibility' for study inclusion which commenced on the latest of: the study start date (1st january 2010); the patient's most recent registration with their practice; the date on which data from the practice was deemed 'up-to-standard' by the cprd. a patient's period of eligibility ended on the earliest of: registration termination; the end of data collection from their practice; death. for incident diagnoses and prescriptions, we also applied a 'look-back' period during which a patient was required to have been registered for at least a year prior to the event. flow diagrams illustrating the delineation of the study cohorts using cprd aurum and gold are presented in supplementary figures 7 and 8 respectively. the denominator for the incidence rates was the aggregate person-months at risk for the whole eligible study population. mortality and testing rates in people with type 2 diabetes were calculated using the person-months at risk from all those with type 2 diabetes as the denominator. incidence, mortality and testing rates were stratified by gender, age group (<18, 18-29, 30-44, 45-64, 65-79 and ≥80 years), practice-level deprivation (imd quintiles) and region (in england) or nation (in the rest of the uk). the data were structured in a time-series format with event counts and 'person-months at risk' aggregated (by year and month) with stratification by gender, age group, deprivation quintile and region (or nation in gold). mean-dispersion negative binomial regression models were used to estimate expected monthly event counts from march 2020 onward based on antecedent trends since 2010. the natural logarithm of the denominator (person-months at risk) was used as an offset in each regression model. to account for possible seasonality and long-term linear trends, calendar month was fitted as a categorical variable and time as a continuous variable with the number of months since the start of the study serving as the unit of measurement. for each month studied, observed and expected event counts were converted to rates using the observed person-month denominator. the monthly expected rates, and their 95% confidence intervals, is the author/funder, who has granted medrxiv a license to display the preprint in (which was not certified by peer review) preprint the copyright holder for this this version posted october 27, 2020. ; https://doi.org/10.1101/2020.10.25.20200675 doi: medrxiv preprint were plotted against the observed rates. as they share a common denominator, differences between expected and observed monthly rates are expressed as a percentage 'rate reduction (or increase)'. extrapolated estimates of the number of missed (or delayed) diagnoses of type 2 diabetes were derived using the discrepancy between observed and expected frequencies from march 2020 onward, and approximations of the proportional representation of the populations of england and the rest of the uk (in cprd aurum and gold respectively) using data from the office for national statistics. 8 all data processing and statistical analyses were conducted in stata version 16 (statacorp lp, college station, tx). we followed record (reporting of studies conducted using observational routinelycollected health data) guidance (see online supplement). 9 the funders of the study had no role in study design, data collection, data analysis, data interpretation, or writing of the report. our focus was on the impact of the covid-19 pandemic between march and july 2020. using the inclusion criteria described in the study design, a mixed cohort was utilised consisting of patients whose period of eligibility began before 1st march 2020 and those who became eligible for inclusion between 1st march 2020 and 10th july 2020. the study cohort was comprised of 13,352,550 patients (median (iqr) age: 42 (25, 59) years, 50% female) of whom 707,103 had type 2 diabetes. of those with type 2 diabetes, the median (iqr) age was 67 (57, 77) years, 44% were female and 25% lived in an area that was in the most deprived quintile compared to the rest of the uk. in april 2020, the rate of new diagnoses of type 2 diabetes in english primary care was reduced by 70% (95% ci 68% to 71%) compared to the expected rates based on 10-year historical trends (figure 1a; supplementary table 1). prior to march 2020, rates of type 2 diabetes diagnoses in english practices were higher in older individuals, in men, and in people from deprived areas. these groups experienced the greatest reductions in rates for new type 2 diabetes diagnosis at the time of the first covid-19 peak (supplementary figure 1 ). the reduced rates of type 2 diabetes diagnosis in april were mirrored by reduced rates of new metformin prescriptions in english practices (reduction: 53% (95% ci 51% to 55%; in april, rates of hba1c testing in england were greatly reduced in people with type 2 diabetes (reduction: 77% (95% ci: 76% to 78%)); is the author/funder, who has granted medrxiv a license to display the preprint in (which was not certified by peer review) preprint the copyright holder for this this version posted october 27, 2020. the reduced rates of diagnosis, new insulin/metformin prescribing and hba1c testing increased gradually between may and july 2020 though levels remained well below expected rates based on 10-year historical data ( figure 1a-d) . overall in english practices, between 1/3/20 and 10/7/20, the rate of diagnosis of type 2 diabetes was reduced by 46% (95% ci: 44% to 49%), metformin prescribing was reduced by 33% (30% to 35%), insulin prescribing fell by 12% (7% to 16%), and hba1c testing in people with type 2 diabetes was reduced by 48% (46% to 49%); supplementary table 1. . cc-by 4.0 international license it is made available under a perpetuity. is the author/funder, who has granted medrxiv a license to display the preprint in (which was not certified by peer review) preprint the copyright holder for this this version posted october 27, 2020. ; https://doi.org/10.1101/2020.10.25.20200675 doi: medrxiv preprint in april 2020, mortality rates in people with type 2 diabetes in england were more than 2-fold higher compared to prior trends (mortality rate increase: 110% (95% ci: 102% to 118%); figure 2a; supplementary table 1). peaks in mortality were seen particularly in individuals aged over 65 years (supplementary figure 5a). mortality rates returned to expected levels in people with type 2 diabetes and sub-groups between may and june 2020 (figure 2a) . overall, between 1/3/20 and 10/7/20, the rate of mortality in people with type 2 diabetes in english practices was increased by 30% (95% ci: 25% to 35%); supplementary table 1. is the author/funder, who has granted medrxiv a license to display the preprint in (which was not certified by peer review) preprint the copyright holder for this this version posted october 27, 2020. ; https://doi.org/10.1101/2020.10.25.20200675 doi: medrxiv preprint metformin prescribing reduced: 26% vs. 33%; supplementary tables 1 and 2). over the same 4½ month period, the overall reduction in hba1c testing in type 2 diabetes was greater in cprd gold practices based in northern ireland, scotland and wales (gold vs. aurum: 56% vs. 48%) but the mortality rate increase was lower than in england (gold vs. aurum: 16% vs. 30%; figure 2; supplementary tables 1 and 2). using primary care data from 13 million people in the uk, and 10-year historical data, we have shown that within the first 4 months of the nationwide 'lockdown' in march 2020, the indirect consequences of the covid-19 pandemic led to: i) a 69-70% reduction in new diagnoses of type 2 diabetes, with older individuals, males, and people from deprived areas experiencing the greatest reduction in diagnosis rates; ii) a 77-84% reduction in hba1c testing; iii) a reduction in metformin and insulin prescribing, particularly in older people with type 2 diabetes, supporting the reduced rates of diagnosis and monitoring; and iv) a short-term 110% increase in mortality rate in people with type 2 diabetes in england and a 66% increased mortality rate across the rest of the uk. there is limited prior data on the impact of the covid-19 pandemic on the diagnosis of type 2 diabetes. a study using primary care data from salford, uk showed 135 fewer diagnoses of type 2 diabetes than expected between march and may 2020, which amounted to a 49% reduction in activity. 10 here we extend these observations by assessing primary care data across the uk and by providing supplementary data on hba1c testing and mortality. we show that the reduced rate of diagnosis applies to all areas of the uk and not just to deprived areas of the uk such as salford. to the best of our knowledge, no study has reported the impact of the covid-19 pandemic on hba1c monitoring in diabetes, and no study has described national variation in mortality rates in people with type 2 diabetes following the first peak of the pandemic. our data have important clinical implications. in early march 2020, gps were advised to minimise the number of face-to-face contacts they had with their patients, including nhs health-checks. 11 our data suggests that this reduction of clinical services has led to major reductions in the diagnosis and monitoring of type 2 diabetes. the concomitant reductions in new prescriptions issued for metformin and insulin further support these findings. type 2 diabetes develops over many years, so it seems unlikely that people's behaviour during the pandemic has reduced the true incidence of these conditions. assuming that the true incidence of type 2 diabetes has remained constant from march 2020, our data suggest that, across the uk, the indirect consequences of the pandemic have led to more than 45k missed/delayed diagnoses of type 2 diabetes in the 4½ months between 1/3/20 and 10/7/20. this figure may be an underestimate if sedentary lifestyles and adverse dietary changes during lockdown have increased obesity rates in the general population. 12 these data are a clinical concern because undiagnosed type 2 diabetes will cause potentially serious long-term complications. the huge reduction in the rate of hba1c testing is another important concern for people with type 2 diabetes, because they, and their clinicians, often rely solely on hba1c data to make decisions about . cc-by 4.0 international license it is made available under a perpetuity. is the author/funder, who has granted medrxiv a license to display the preprint in (which was not certified by peer review) preprint the copyright holder for this this version posted october 27, 2020. ; https://doi.org/10.1101/2020.10.25.20200675 doi: medrxiv preprint treatment. the reduction in new prescriptions for insulin was largely observed in older individuals suggesting this reduction was explained by a failure to intensify therapy in people with poorly controlled long-duration type 2 diabetes. there are already concerns in the uk about clinical inertia in diabetes management, with frequent failures to escalate care when glucose control is poor. 13 these hba1c data indicate potential further delays in the management of type 2 diabetes that are predicted to cause avoidable diabetes-related long-term complications. a reduced frequency of hba1c testing in primary care might also contribute to missing people with non-diabetic hyperglycaemia who might benefit from referral to the nhs diabetes prevention programme. the higher covid-related death rate in people with diabetes has been well-documented, 2,3,14 and our data support these observations. here, we add to these data by showing national differences in the impact of covid-19 on mortality rates in people with type 2 diabetes, with higher rates observed in england compared to the rest of the uk. further research is required to understand how population characteristics including ethnicity, population density and deprivation might explain these differences. as engagement with health services increases, and hopefully is maintained during the second covid-19 peak, our data predict a marked increase in presentations with incident type 2 diabetes. should this occur, then healthcare services will need to manage this backlog, and the expected increase in the severity of diabetes brought about by delayed diagnoses. older individuals, males and people from deprived backgrounds appear to be most adversely affected by reductions in rates of diagnosis and monitoring of type 2 diabetes. as outpatient diabetes services start to open up, these individuals may be a group to target for early intervention, and in particular, for hba1c testing and treatment intensification when appropriate. if a second full lockdown occurs, then effective public communications should ensure that patients remain engaged with diabetes services including hba1c screening 15 and monitoring, and the use of remote consultations. 16, 17 our study had several strengths: this is the first uk-wide study reporting the indirect impact of the covid-19 pandemic on the diagnosis of type 2 diabetes, related prescribing and hba1c testing in primary care. our findings in english practices were replicated using data from other parts of the uk. by combining assessments of diabetes coding and prescribing, our data supports the conclusion that reduced rates of diagnoses are genuinely explained by missed diagnoses. our study has some limitations: first, ethnicity coding is not adequately captured in primary care and therefore we had limited ability to explore ethnicityrelated variation in care and outcomes. future studies will incorporate linked secondary care data that has more complete capture of ethnicity data. second, it is possible that some diabetes diagnoses may have been made in a hospital setting following an acute presentation and that the related primary care coding had not been updated at the time of our data extraction. while hospital presentation of incident diabetes may have occurred in some instances, it would not explain the reductions in new prescribing for metformin and this potential explanation does not fit with our local experience. in general, people have avoided hospital attendance during the pandemic. for example, one study documented a 23% reduction in emergency admissions in the uk. 18 finally, although our results and conclusions are relevant to the uk population, generalisability to other healthcare systems may be limited. is the author/funder, who has granted medrxiv a license to display the preprint in (which was not certified by peer review) preprint the copyright holder for this this version posted october 27, 2020. ; https://doi.org/10.1101/2020. 10.25.20200675 doi: medrxiv preprint in conclusion, we highlight marked reductions in the diagnosis and monitoring of type 2 diabetes as indirect consequences of the covid-19 pandemic. over the coming weeks, healthcare services will need to manage this predicted backlog, and the expected increase in the severity of diabetes due to delayed diagnoses. older people, men and those from deprived backgrounds with type 2 diabetes may be specific groups to target for early hba1c testing and intervention. should a second full national lockdown occur, then effective public communications should ensure that patients remain engaged with diabetes services including hba1c screening and monitoring and the use of remote consultations. the lead authors (mjc and akw: the manuscript's guarantors) affirm that the manuscript is an honest, accurate, and transparent account of the study being reported; that no important aspects of the study have been omitted; and that any discrepancies from the study as planned have been explained. the corresponding author had full access to all of the data and the final responsibility to submit for publication. all clinical codes used in the study are published on clinicalcodes.org. electronic health records are, by definition, considered "sensitive" data in the uk by the data protection act and cannot be shared via public deposition because of information governance restriction in place to protect patient confidentiality. access to data are available only once approval has been obtained through the individual constituent entities . cc-by 4.0 international license it is made available under a perpetuity. is the author/funder, who has granted medrxiv a license to display the preprint in (which was not certified by peer review) preprint is the author/funder, who has granted medrxiv a license to display the preprint in (which was not certified by peer review) preprint is the author/funder, who has granted medrxiv a license to display the preprint in (which was not certified by peer review) preprint the copyright holder for this this version posted october 27, 2020. ; https://doi.org/10.1101/2020.10.25.20200675 doi: medrxiv preprint supplementary figure 2: comparison of monthly hba1c testing rates in people with type 2 diabetes in primary care by age, gender, deprivation level and by region before and after the first covid-19 peak in england (cprd aurum) is the author/funder, who has granted medrxiv a license to display the preprint in (which was not certified by peer review) preprint the copyright holder for this this version posted october 27, 2020. ; https://doi.org/10.1101/2020.10.25.20200675 doi: medrxiv preprint supplementary figure 3: comparison of monthly incidence rates for metformin prescribing in primary care by age, gender, deprivation level and by region before and after the first covid-19 peak in england (cprd aurum) is the author/funder, who has granted medrxiv a license to display the preprint in (which was not certified by peer review) preprint the copyright holder for this this version posted october 27, 2020. ; https://doi.org/10.1101/2020.10.25.20200675 doi: medrxiv preprint supplementary figure 4: comparison of monthly incidence rates for insulin prescribing in primary care by age, gender, deprivation level and by region before and after the first covid-19 peak in england (cprd aurum) is the author/funder, who has granted medrxiv a license to display the preprint in (which was not certified by peer review) preprint the copyright holder for this this version posted october 27, 2020. ; https://doi.org/10.1101/2020.10.25.20200675 doi: medrxiv preprint supplementary figure 5: comparison of monthly mortality rates in people with type 2 diabetes in primary care by age, gender, deprivation level and by region before and after the first covid-19 peak in england (cprd aurum) is the author/funder, who has granted medrxiv a license to display the preprint in (which was not certified by peer review) preprint the copyright holder for this this version posted october 27, 2020. ; https://doi.org/10.1101/2020.10.25.20200675 doi: medrxiv preprint supplementary figure 6: comparison of observed and expected monthly incidence rates for type 2 diabetes in primary care, hba1c monitoring and new prescriptions for metformin and insulin before and after the first covid-19 peak in northern ireland, scotland and wales (cprd gold) is the author/funder, who has granted medrxiv a license to display the preprint in (which was not certified by peer review) preprint the copyright holder for this this version posted october 27, 2020. ; https://doi.org/10.1101/2020. 10 is the author/funder, who has granted medrxiv a license to display the preprint in (which was not certified by peer review) preprint the copyright holder for this this version posted october 27, 2020. ; https://doi.org/10.1101/2020.10.25.20200675 doi: medrxiv preprint uk's record on pandemic deaths risk factors for covid-19-related mortality in people with type 1 and type 2 diabetes in england: a population-based cohort study associations of type 1 and type 2 diabetes with covid-19-related mortality in england: a whole-population study van den bruel a. opportunities for earlier diagnosis of type 1 diabetes in children: a case-control study using routinely collected primary care records data resource profile: clinical practice research datalink (cprd) diagnosis of physical and mental health conditions in primary care during the covid-19 pandemic: a retrospective cohort study letter to general practices the silent pandemic: how lockdown is affecting future health legacy benefits of blood glucose, blood pressure and lipid control in individuals with diabetes and cardiovascular disease: time to overcome multifactorial therapeutic inertia? factors associated with covid-19-related death using opensafely h(ome)ba1c testing and telemedicine: high satisfaction of people with diabetes for diabetes management during covid-19 lockdown endocrinology in the time of covid-19: remodelling diabetes services and emerging innovation video consultations for covid-19 what is happening to non-covid deaths? reasons: (a) registration ended prior to study period due to death or migration from practice (n = 12,440,573); (b) registration end date defined on or prior to registration start date (n = 21,315); (c) aged under 5 on study period end ) and/or compare expected and observed rates acceptability defined by cprd as meeting certain quality standards reasons: (a) registration ended prior to study period due to death or migration from practice (n = 2,159,261); (b) registration end date defined on or prior to registration start date (n = 146,723); (c) aged under 5 on study period end ) and/or compare expected and observed rates supplementary table 1: comparison of observed and expected monthly incidence rates for type 2 diabetes in primary care, hba1c monitoring in type 2 diabetes, new prescriptions for metformin and insulin, and deaths in people with type 2 diabetes between 1/3/20 and 10/7/20 and at the covid-19 peak in april 2020, in england (cprd aurum) key: cord-259748-x7dq1sy4 authors: wan, dongshan; jiang, wei; hao, junwei title: research advances in how the cgas-sting pathway controls the cellular inflammatory response date: 2020-04-28 journal: front immunol doi: 10.3389/fimmu.2020.00615 sha: doc_id: 259748 cord_uid: x7dq1sy4 double-stranded dna (dsdna) sensor cyclic-gmp-amp synthase (cgas) along with the downstream stimulator of interferon genes (sting) acting as essential immune-surveillance mediators have become hot topics of research. the intrinsic function of the cgas-sting pathway facilitates type-i interferon (ifn) inflammatory signaling responses and other cellular processes such as autophagy, cell survival, senescence. cgas-sting pathway interplays with other innate immune pathways, by which it participates in regulating infection, inflammatory disease, and cancer. the therapeutic approaches targeting this pathway show promise for future translation into clinical applications. here, we present a review of the important previous works and recent advances regarding the cgas-sting pathway, and provide a comprehensive understanding of the modulatory pattern of the cgas-sting pathway under multifarious pathologic states. pattern-recognition receptors (prrs) serve as innate cellular sensors of danger signals, such as pathogen-associated molecular patterns (pamps) or danger-associated molecular patterns (damps), and yield cellular-stress response. dna molecules are vital genetic components within cells, which are compartmentalized restrictively into specific regions. the occasionally misplaced dna is degraded rapidly by scavenger cells and extracellular or intracellular ribonucleases. aberrant accumulation of dna is relevant to tissue damage (1) . in 2008, several research teams discovered a new protein on the endoplasmic reticulum (er) which can be activated by immune-stimulatory dna (isd) and initiate type-i interferon (ifn) responses, which was named "stimulator of interferon genes" (sting, also known as mita, eris) (2) (3) (4) . sting does not bind to dna directly, and bacteria-derived cyclic di-guanylate monophosphate (c-dgmp) or cyclic di-adenosine monophosphate (c-damp) were confirmed to be ligands for sting (5, 6) . subsequently, it was found that some dna sensors can facilitate sting activation, such as interferon gamma inducible protein 16 (ifi16) (7) . however, sting activation could not be fully explained by the upstream factors/ligands that had been found. it was postulated that an unknown upstream regulator might be responsible for sting activation. in 2013, wu and sun found that cyclic guanosine monophosphate-adenosine monophosphate (cgamp) was a novel secondary messenger serving as a ligand of sting (8) . beside it, they purified a new protein named "cyclic-gmp-amp synthase" (cgas) that had cytosolic dna-sensing ability and can synthesize cgamp (8) . also, they found that the cgas-cgamp-sting pathway was indispensable for host anti-viral immunity (9) . their work filled in the gaps missing from upstream of sting. stimulator of interferon genes or cyclic-gmp-amp synthase is expressed widely in a broad spectrum of cells including immune, non-immune, cancer cells (10) . mounting evidence has demonstrated that the cgas-sting pathway is important for mediating cellular immune sensing, and shows particular responses pattern to the isd distinguished from other nucleotide-sensing pathways. it is also regulated delicately by several molecules or feedback loops to maintain cellular homeostasis. nevertheless, cgas-cgamp-sting pathway itself has distinctive or even opposing effects under different conditions. in this review, we cover the roles of cgas-sting pathway in cellular type-i ifn immune response, and several cellular processes including autophagy, survival and senescence. we also summarize the literature on intrinsic cellular mechanisms modulating cgas-sting pathway as well as its cross-regulations with other dna-sensing pathways. moreover, the inflammationmodulation capacities of this pathway in infectious disease, inflammation and cancers have been elucidated too, and a pervasive pattern of this pathway has been described, which could provide a plausible explanation of the contradictory findings of studies. finally, current or prospective therapeutic strategies targeting the pathway, and issues that need to be addressed in the future, are discussed. cyclic-gmp-amp synthase belongs to the structurally conserved cgas/dncv-like nucleotidyltransferase (cd-ntases) superfamily. the latter is expressed universally in prokaryotes and eukaryotes, and can use purines or pyrimidines selectively as substrates for the production of linear or cyclic di-or even tri-nucleotide compounds, which act as secondary intracellular messengers (11) . cyclic-gmp-amp synthase is distributed mainly in the cytosol (also nucleus in some specific conditions) (8) . generally speaking, cgas is activated upon the recognition of b-type double-stranded dna (dsdna) without sequence-specificity but not a-type dsdna or rna (12, 13) . hybrid dna:rna or stemlike single-stranded dna (ssdna) are also low-affinity ligands for cgas (14, 15) . after binding with ligands, cgas undergoes an allosteric structural change, and subsequently catalyzes its substrates guanosine triphosphate (gtp) and adenosine triphosphate (atp) to produce a mixed phosphodiester-linked cyclic dinucleotide: g(2 -5 )pa (3 -5 ) p cgamp (abbreviated as 2 ,3 -cgamp or cgamp) (16) . cgas also catalyze the synthesis of linear dinucleotides such as amp-2 -atp, gmp-2 -gtp, and amp-2 -gtp as intermediate products (17) . there are two major dsdna-binding sites on opposite sides of the catalytic pocket: a and b site. site a is the primary contact surface for dsdna, whereas site b is complementary, binding another dsdna. it allows for cgas to the formation of a 2:2 cgas:dsdna complex structure directed into two orientations with dsdna at least 20 bp (18) (19) (20) (figure 1a) . increased numbers of back-to-back dimers of cgas hold the two dsdna molecules together and permit successive recruitment of cgas which, consequently, forms a 2n:2 cgas:dsdna higherordered "ladder-like" oligomerization, with cgas arrayed "head to head/tail to tail" (19, 21) . the dna-binding protein hu, mitochondrial transcription factor a (tfam), or bacterial high mobility group box 1 protein (hmgb1) can bend the dsdna into a u-shaped structure and, thus, facilitate binding of cgas dimers to the same strand as it travels in opposite directions (21) (figure 1b) . human cgas, unlike mouse cgas, is prone to formation of this ladder-like network with long dsdna, because of the human-specific residues k187 and l195. these two dsdna-interfacing residues of site a loosen the interaction of dsdna with cgas, leading to dsdna curving and allowing more convenient binding for the next adjacent cgas (20, 21) ( figure 1c) . finally, accumulated cgas-dsdna complexes can go through a liquid-phase separation and condense into gellike droplets as a reaction unit ( figure 1d) . this conformation requires a sufficiently long dsdna strand to form multivalent interaction positions, also requires the function of the n-terminal tail of cgas and a recently discovered dsdna-binding site in the catalytic domain of cgas (site c) (22, 23) . meanwhile, the n-terminal tail of cgas mediates cgas localization onto the membrane by binding to phosphatidylinositol 4,5bisphosphate (pi (4, 5) p2) and prevents liberation of cgas and oligomerization, but can release cgas during cell stress (24). the structure of cgas determines long strand dsdna (>500-1,000 bp) could potentially stimulate the enzyme activity and cgamp production of cgas (25). the ability of human cgas to discriminate long dsdna strands from shorter dsdna may contribute to the specific sensing and recognition of the "danger dna" of pathogens, necrotic cells or cancer cells rather than irrelevant shorter dsdna, thereby enhancing the immunity against them specifically. double-stranded dna is restricted into the nucleus or mitochondria and is rarely present in the cytoplasm. extrinsic dsdna from pathogens such as viruses, bacteria, transcellular vesicles or rupture of dying cells can be internalized into the cytosol in several diverse ways (26-28). these extrinsic dsdna sources are engulfed by endosome through phagocytosis and digested immediately by dnaseii when fusing with lysosomes (29, 30). however, some escaping mechanisms under certain conditions could help protect them from being degraded. for example, antimicrobial peptide ll37 could efficiently transports self-dna from endosome into cytosol of monocytes (28). cell oxidative stress can lead to phagosomal acidification delay and probably release endosome context including dsdna owing to increased membrane permeability (27, 31). the intrinsic self-dsdna can also be segregated inaccurately and released into the cytosol (32, 33). for example, genomic dna (gdna) injury as a result of genotoxic stress and dna self-instability or replication errors leads to double-strand breaks (dsbs) and can be repaired by several ways (34). impaired mediators of dna-damage repair response mediators, such as ataxia telangiectasia mutated (atm)-rad3, poly adpribose polymerase (parp) and breast cancer1/2 (brca1/2) multiple cgas molecules can bind two double-stranded dnas (dsdna) to form a 2n:2 cgas:dsdna higher-ordered "ladder-like" oligomerization. mitochondrial transcription factor a (tfam) can bend the dsdna into a u-shaped structure and promote polymerization. (c) cgas can recognize b-type dsdna. in humans, the cgas dna-interfacing residue of site a loosens the interaction of dsdna to curve dsdna away for more convenient binding with next adjacent cgas. cgas can catalyze gtp and atp to synthesize cyclic guanosine monophosphate-adenosine monophosphate (cgamp). the n-terminal tail binds to the cell membrane, associating with phosphatidylinositol 4,5-bisphosphate [pi (4,5)p2]. (d) accumulation of cgas-dna complex goes through a liquid-phase separation and condenses into gel-like droplets. are associated with persisting dsbs and accumulation of cytosolic dna (35-37). extra-nuclear micronuclei formation during mitosis is a source of cytosolic dsdna caused by dsbs (32, 38). followed by homologous recombination repair of collapsed replication forks, dna cleavage by methyl methanesulphonate (mms) and ultraviolet-sensitive 81 (mus81) also lead to cytosolic dsdna presenting (39). furthermore, manually cre/loxp recombination technology can induce dsdna damage during dna cleavage, which results in the accumulation of cytoplasmic dsdna (40). in normal cellular mitotic processes, chromosomal dna can be exposed to the cytoplasm, while it is hard to bind and trigger cgas (41). in addition, mitochondrial dna (mtdna) is also a considerable ligand of cgas and can be released into the cytosol under mitochondrial stress or dysfunction of proteins which participates in maintaining mitochondrial operations (33, 42, 43) (figure 2a) . cells have several types of nucleases to restrict cytosolic dna to avoid cgas activation. for example, three-prime repair exonuclease 1 (trex1 also known as dnaseiii) is a cytosolic dna exonuclease which removes unprotected dsdna from the cytosol (44) . rnaseh2 locates to the nucleus and specifically degrades the rna in rna:dna hybrids participating in dna replication (45) . dnaseii is a lysosomal dnase which degrades undigested dna in endosomes or autophagosomes to prevent their entry into the cytoplasm (30). sam domain and hd domain-containing protein 1 (samhd1) is characterized as a dntpase and restricts reverse transcription of the rna virus (46, 47) . samhd1 can also stimulate the exonuclease (but not the endonuclease) activity of mre11 to degrade nascent cdns (including cgamp) might be exported by some ways. (c) inflammatory signaling mediated by the cgas-sting pathway. after sensing dna, cgas produces cgamp and extracellular cdns, promoting stimulator of interferon genes (sting) to undergo dimerization. sting can exit from the endoplasmic reticulum (er), and be translocated from the er to the er-golgi vesicle, and arrives at the golgi. sting and tank binding kinase 1 (tbk1) can be oligomerized and cluster at the golgi. the sting-tbk1/iκb kinase (ikk) signalosome forms a scaffold to phosphorylate interferon regulatory factor 3 (irf3) and inhibitor of nf-κbα (iκbα). then, dimerized irf3 and the activated canonical nf-κb p50/p65 complex can be translocated into the nucleus as transcription factors to promote transcription of type-i ifn. (d) autophagy initiation and degradation. sting activation on er triggers er stress and mechanistic target of rapamycin complex1 (mtorc1) dysfunction. er stress and mtorc1 dysfunction can stimulate the unc-51 like autophagy activating kinase (ulk1) complex and beclin1-phosphatidylinositol 3-kinase catalytic subunit type 3 (pi3kc3) complex. autophagy-related protein 9 (atg9) and light chain 3 (lc3) are associated with genesis and elongation of the autophagosome. after autophagy initiation, cgas-sting is ubiquitinated and binds with p62. then, they are packaged into autophagosomes and terminally sorted to lysosomes (bold arrows represent main signaling pathways, thinner arrows represent regulatory signaling pathways, and dashed arrows represent bypass or suspicious pathways). ssdna, and start dna-repair responses at stalled replication forks (48) . depletion of samhd1 leads to the cleaving of nascent ssdna by the activity of mre11 endonuclease and cytosolic translocation of gdna (48) . deficiency of any of these nucleases can lead to accumulation of self-dna in the cytoplasm, thereby activating the cgas-sting pathway against dna molecules (30) (figure 2a ). the production of asymmetrically linked 2 ,3 -cgamp catalyzed by cgas has the highest affinity for sting to promotes sting dimerization (49, 50) . cgamp as a second messenger can be also transferred among cells in several ways to pass danger signaling of frontiers in immunology | www.frontiersin.org cytosolic dna. intercellular gap junction consists of two docking hexamer channels formed by different connexins, which allows many small molecules, including cgamp, to pass bi-directionally through cells. and intercellular transfer of cgamp through gap junction is largely dependent on connexin 43 (51) (52) (53) . additionally, cgamp can be packaged into virons and pre-notify newly infected cells (54, 55) . cell fusion is a distinct manner for intracellular transmission of the human immunodeficiency virus (hiv); cgamp also enter membrane-fused bystander cells in this way (56) . extracellular vesicles such as exosomes can contain cgamp along with viral dna, host gdna or mtdna, and mediate cells communication (57, 58) . there were no evidences that cgamp could be pumped out to extracellular space by a channel/transporter. however, it was found that slc19a1 can transmit cyclic dinucleotides (cdns) into cell plasma (59, 60) . notably, ectonucleotide pyrophosphatase/phosphodiesterase family member 1 (enpp-1) can degrade extracellular cgamp (61) (figure 2b ). besides triggering sting, these exogenous cgamp can directly bind to cgas and prompt its activation as well (62) . after binding to cgamp, the "lid" region of the sting dimer undergoes a conformational change that converts sting from an inactive "open" formation to an active "closed" formation. following that, the sting dimer translocates from the er to perinuclear er-golgi intermediate compartment (ergic) vesicles, finally arriving at the golgi to form punctuate structures with downstream molecules (2, 63) . er-retention of sting caused by mutations results in reduced ifn signaling (64, 65) . the translocon-associated protein β (trapβ) recruited by inactive rhomboid protein 2 (irhom2) initially forms the trap translocon complex that mediates sting exit from the er (2, 66). they both assist cytoplasmic coat protein complex-ii (copii) to drive er-vesicle formation and carry the sting complex to the golgi (67, 68) . trafficking sting can bind directly to and be phosphorylated by tank binding kinase 1 (tbk1) dimer or iκb kinase (ikk) complex (3, 69, 70) . the c-terminal tail (ctt) of sting is a linear unfolded segment, which determines the optimization of combination specificity. sting ctt in mammals tends to bind tbk1, whereas in fish it tends to activate nuclear factor-kappab (nf-κb) signal (71) . the sting phosphorylation site ser366 in the ctt cannot reach the kinase-domain active site of its directly bound tbk1, instead can reach the kinase-domain active site of the next adjacent tbk1 binding with another sting and be phosphorylated, while tbk1 phosphorylate each other (72, 73) . hence, sting and tbk1 can aggregate on the golgi to form the sting signalosome. clustering sting undergoes palmitoylation and full activation (74) . it is also possible for sting-ikk to cluster and form the sting signalosome in this manner. the sting-tbk1/ikk signalosome produces a scaffold to phosphorylate interferon regulatory factor 3 (irf3) or inhibitor of nf-κbα (iκbα). activated irf3 undergo dimerization (70) . the activation of iκbα leads to its polyubiquitination and degradation by the proteosome, thereby eliminating its inhibition of nf-κb. there is also evidence suggesting that nf-κb activation might not require sting trafficking from the er (75) . then, the dimerized irf3 or activated nf-κb p50/p65 (p65 is also known as rela) complex are translocated into the nucleus as transcription factors and bind to the promoter of type-i ifn to aid the transcription of type-i ifn (2, 3, 70) . meanwhile, activation of nf-κb p52/relb can prevent recruitment of p65 and inhibit the p50/p65 signal (76) (figure 2c ). expressed type-i ifn can propagate among cells in paracrine or autocrine manners. the binding of ifnα/β with its receptor triggers janus kinase (jak) and signal transducer and activator of transcription (stat) pathways, then induce transcription of type-i ifn-stimulated genes (isgs), which have ifn-sensitive response elements (isres) in their 5 -untranslated regions (utrs) (77) . irf3 can also bind partially to several isres alone (78) . herein, the expression of some isgs including interferon-induced protein with tetratricopeptide repeats (ifit) and pro-inflammatory cytokines such as tumor necrosis factor α (tnfα), interleukin (il)-6, c-x-c motif chemokine ligand 10 (cxcl10) and c-c motif chemokine ligand 5 (ccl5) is increased remarkably by the cgas-sting pathway (79) . furthermore, cgas and sting are both isgs, suggesting a positive feedback loop in spreading of the ifn signal (80, 81) . stimulator of interferon genes activation on the er also triggers an er stress response with an "unfolded protein response (upr) motif " on the c-terminus of sting, which leads to and er stress-mediated autophagy (82, 83) . sting-tbk1 activation and er stress also induce mechanistic target of rapamycin complex 1 (mtorc1) dysfunction (84) . er stress or reduced mtorc1 signaling activates unc-51-likeautophagy activating kinase (ulk1) complex and the beclin-1-class iii phosphatylinositol 3-kinase (pi3kc3 also known as vps34) complex, which promotes initiation of the classical autophagy path (85) . cgas can also interact directly with the autophagy protein beclin-1-pi3kc3 complex and trigger autophagy (86) . furthermore, cgas-dsdna polymer can form a liquid-phase condensate (as mentioned above), which could theoretically be an initiator of autophagy (87) . after autophagy initiation, autophagy-related protein 9 (atg9) undertakes the genesis of the autophagosome along with light chain3 (lc3) undergoing lipidation, thereby resulting in elongation of the autophagosome (88) . lc3 can also be recruited directly by ergic-loading sting and bypass the classical autophagy pathway (68, 89) . cgas-sting-mediated autophagy can spread to the whole cell and help the elimination of intracellular microorganisms, subcellular organelles or misfolded proteins, as well as the er itself that loads the sting signalosome (90-92) ( figure 2d ). cgas-sting-mediated autophagy is also indispensable for removing cytosolic dna and inflammatory signaling factors to restrict the inflammatory response raised by the pathway itself (93) . excessive signaling of the autophagy cascade can lead to irreversible apoptosis termed "autophagic cell death" (94) . consequently, oligomerized cgas or sting undergoes ubiquitination and is packaged into autophagosomes with the help of p62, to be terminally sorted into lysosomes (79, 83, 95, 96) . cgas or sting is digested immediately in the autophagolysosome after transient activation of downstream signaling (68, 79, 83, 89) . autophagy functions as a negative feedback loop which ensures transient cgas-sting signaling and avoids consistent over-reaction of the pathway. thus, impairment of autophagy may give rise to destructive inflammatory diseases (31). we cataloged factors in the literature that could potentially up-or down-regulate expression of cgas/cgamp/sting in pre-translational or post-translational stages (tables 1, 2) . the regulatory mechanisms of tbk1, irf, and nf-κb in signaling pathways associated with expression of type-i ifn are outside the scope of this review. pyhin family member absent in melanoma 2 (aim2) is a cytoplasmic dsdna sensor. it can recruit apoptosis-associated speck-like protein containing a card (asc) by its pyhin domain and form the aim2 inflammasome. the inflammasome activates caspase-1, which activates il-1 and trigger pyroptosis (97) . the aim2 pathway could counteract the cgas-sting pathway (98) . first, cgas is a target for caspase-1 cleavage (99) . second, gasdermin d activated by caspase-1 can lead to potassium ion (k + ) efflux which inhibits cgas (100) . conversely, the cgas-sting pathway can trigger the aim2 inflammasome or nlr family pyrin domain containing 3 (nlrp3) by several means, and the process lags behind canonical ifn signaling (96, 101) . in this way, the inhibitory nucleic-acid sensor nlr family card domain containing 3 (nlrc3) can counteract sting by binding and occupying it, but viral dna as a possible nlrc3 ligand can reverse its occupation of sting (102) (figure 3a) . another pyhin family member, ifi16, is a dna sensor located in the nucleus. ifi16 can bind to viral dna sequences or damaged chromatin dna and be translocated to the cytoplasm to recruit sting cooperatively with tnf receptor associated factor 6 (traf6) and p53 (103, 104) . several studies have shown that ifi16 (which can stimulate the phosphorylation and recruitment of sting and tbk1) is required for the full response of sting (105, 106) ( figure 3b) . conversely, cgas can partially enter the nucleus and interact with ifi16 to promote its stability (107) . therefore, it is inferred that during viral infection, ifi16 can facilitate recognition of decapsidated viral dna in the nucleus, while cgas in the cytoplasm engages with viral gene transcription products (104, 108) . however, sting signaling can trigger ifi16 degradation by tripartite motif-containing 21 (trim21) ubiquitination (109) . tlr is also an important prr for multiple pamps (110) . tir domain-containing adaptor-inducing ifnβ (trif) is downstream of several subtypes of tlrs (including tlr3). trif may be responsible for interacting with sting and helping the dimerization of sting (111) . during viral infection, the tlr9-myeloid differentiation primary response 88 (myd88)-irf3/7 pathway is necessary for mouse monocytes recruitment to lymph nodes, whereas the sting pathway is necessary for local production of type-i ifn (112) . however, sting signaling can induce suppressor of cytokine signaling1 (socs1) expression, which can negatively regulate myd88 activity (113) (figure 3c ). oxidized mtdna can be released into the cytoplasm during cell stress elicited by hypoxia, viral infection and mitochondrial damage, etc.; oxidized mtdna is resistant to degradation by the cytosolic nuclease trex1 (114) . in addition, mtdna accompanied with tfam (a mtdna-binding protein that can bend mtdna) is also a reasonable target for recognition by cgas (21, 33) . however, during regulated cell death (as represented by apoptosis), it undergoes mtdna release but has certain mechanisms to ensure a minimal cgas-stingmediated immune response. mitochondrial outer membrane permeabilization (momp) activation, which is executed by bcl-2-associated x protein (bax) and bcl-2 antagonist or killer (bak), is a highly controlled conserved process in regulated cell figure 3 | interaction of the cgas-sting pathway with other dna-sensing pathways and its role in cell survival. (a) absent in melanoma2 (aim2) pathway and pyroptosis and necroptosis. aim2 can be triggered by cgamp and form an inflammasome, consequently triggering interleukin (il)-1 production and pyroptosis. stimulator of interferon genes (sting) trafficking to the lysosome ruptures the lysosome membrane, resulting in k + efflux and activation of the nlrp3 inflammasome, leading to pyroptosis. cyclic-gmp-amp synthase (cgas) and interferon regulatory factor 3 (irf3) can be a target for caspase-1 cleaving. gasdermin d can lead to k + efflux and inhibition of cgas. (b) interferon gamma inducible protein 16 (ifi16). ifi16 can be transported to the cytoplasm to help to recruit sting and tank binding kinase 1 (tbk1). ifi16 as a pyhin family protein may form the inflammasome only in theory. (c) toll-like receptor (tlr) pathway. tir domain-containing adaptor-inducing ifnβ (trif) may be responsible for helping the dimerization of sting. sting signaling can induce suppressor of cytokine signaling 1 (socs1) expression, which negatively regulates myd88 activity. (d) apoptosis. mitochondrial outer membrane permeabilization (momp) formed by bax/bak induced by mitochondrial stress can release oxidized mitochondrial dna (mtdna) and cytochrome c into the cytosol. oxidized mtdna is a suitable ligand for cgas recognition and is resistant to dnaseiii (trex1) degradation. cytochrome c binds to apoptotic protease-activating factor 1 (apaf1) and initiates the formation of an apoptosome cooperatively with caspase-9 to activate caspase-3, which can induce apoptosis. caspase-3 can cleave cgas. death. bak and bax activated by apoptosis signals cooperatively form a pore-like conformation on the mitochondrial outer membrane, leading to a permeability change of outer and also inner membranes (115, 116) . consequently, the mitochondrial matrix, including cytochrome c and oxidized mtdna-tfam, is released into the cytoplasm (115, 117) . cytochrome c binds to apoptotic protease-activating factor 1 (apaf1) and initiates the formation of the apoptosome cooperatively with caspase-9, which further triggers the intrinsic apoptosis program (117) . in vivo and in vitro studies have shown that an absence of caspase-9 is associated with greater release of type-i ifn (43, 117) . this occurs because caspase-9 and its downstream caspase-3 can cleave cgas and irf3 to restrain deleterious inflammation (118) (figure 3d) . the cgas-sting pathway can also initiate programmed cell death. activation of sting enhances phosphorylation and activation of receptor interacting serine/threonine kinase 3 (rip3) and mixed lineage kinase domain-like pseudokinase (mlkl). proapoptotic bcl2 binding component 3 (puma), a member of bh3-only family, is subsequently activated in a rip3/mlkl-dependent manner, which promotes leakage of mtdna by momp (119, 120) . activated irf3 can bind directly to bax to form irf3/bax complex and induce apoptosis (47) . excessive cgas-sting-mediated autophagy signaling can cause "autophagic cell death" and prevent malignant transformation of cells through dna damage (94, 121) . sting trafficking to the lysosome can broaden permeabilization of the lysosome membrane, thereby rupturing the lysosome and releasing its contents, resulting in "lysosomal cell death (lcd)". lcd further triggers k + efflux and nlrp3 activation, ultimately resulting in pyroptosis (96, 101) (figure 3d) . moreover, stimulating sting-dependent type-i ifn and tnfα signals simultaneously can lead to necroptosis of tumor cells (122, 123) . cell senescence is recognized as a permanent arrest of the cell cycle, and is common in aging, immunity, ontogenesis and infectious defense (124) . it lacks a specific biomarker but can be identified by the expression of several antiproliferative molecules (representatively rb-p16 andp53-p21 pathway) (125) . during senescence, changes in the nuclear structure and loss of the nuclear lamina protein disrupt the integrity of the nuclear envelope, leading ultimately to dna damage and cytoplasmic chromatin fragments (126) . cellular senescence can be accelerated by accumulation of cytoplasmic chromatin in turn (127) . these senescent cells produce the senescence-associated secretory phenotype (sasp), which shapes an inflammatory microenvironment (128) . the cgas-sting pathway has been reported to be involved in the recognition of cytoplasmic chromatin fragments from senescence-related dna damage, and mediate the expression of sasp genes (129) (130) (131) (132) . along with these actions, the expression of trex1 and dnaseii is inhibited by dna damage through the inhibition of e2f/dp (a potential transcription factor of trex1 and dnaseii) (130) . for hematopoietic stem cells (hscs), dna damage can promote excessive secretion of type-i ifn in the hsc niche and activate p53 pathway, both of which can lead to long-term senescence and exhaustion of hscs (133, 134) . hscs expressing a circular rna named "cia-cgas" in the nucleus, however, are protected from this exhaustion as a result of cia-cgas having stronger affinity than that of self-dna, which prevents it from being sensed (135) . it implied a novel target to manipulate the immune environment in bone marrow and help for finding treatment approaches for hematopoiesis-based diseases, such as aplastic anemia. utilizing cellular senescence to restrain tumor growth is discussed below. cgas-sting signaling has an essential role in defense against a broad spectrum of intracellular dna and rna viruses (9, 26, 50) . hiv is a typical rna retrovirus: there is neither dsdna in its genome, nor production of nucleic acids (50) . nevertheless, cgas can detect the presence of hiv. rna:dna hybrids synthesized during reverse transcription that can be sensed by cgas explain (at least in part) this phenomenon (14) . cgas may be triggered by endogenous dna broken and released during hiv infection as well theoretically. however, some studies found the new mechanisms. the early reverse-transcription production of hiv-1 can flank short stem loops with paired base, which lead to the production of y-type dna containing unpaired guanosines that can activate cgas well (15) . moreover, nucleolus protein non-pou domain-containing octamer-binding protein (nono), as a sensor of capsid components of hiv, can help cgas to be translocated to the nucleus and assist cgas to sense hiv dna accompanied by polyglutamine-binding protein 1 (pqbp1) (136, 137) . the assistance proffered by nono in assisting cgas to sense dna is also associated with its role in constructing a ribonuclear complex with dna-dependent protein kinase (dna-pk) subunits around hexamethylene bisacetamide-inducible protein1 (hexim1), termed as "hexim1-dna-pk -paraspeckle components-ribonuclear protein complex (hdp-rnp), " which also has a role in repair of dna damage and transduction of genotoxic signals (138) . this complex is also required to accompany cgas-pqbp1 in sensing dna virus, such as kaposi's sarcoma-associated herpes virus (139) . in addition, during virus infection, sting activation can lead to global suppression of translation in cells, which restricts viral replication (140) . compared with hiv-1, hiv-2 is less infective because it can infect dendritic cells (dcs) and elicit an anti-virus immune response. as a result, hiv-2 can cross-protect against hiv-1 (141). this phenomenon has been attributed to the fact that hiv-2 (instead of hiv-1) can encode protein vpx, which overcomes the samhd1 restriction of dntp in dcs (46, 142) . hiv-1 can infect dcs via vpx presentation, nevertheless, hiv-1 still cannot be fully sensed and induce an efficient immune response owing to certain escape mechanisms. whether it is hiv-1 or hiv-2, a completely robust ifn response is required at pre-and post-integration sensing stages (143) . cgas in dcs can detect reverse-transcribed cdna of hiv-2 before and after integration, whereas hiv-1 sensing is after genome integration owing to its capsid protection (144, 145) . it was suggested that during initial infection by hiv-1, nucleotides are recruited into the intact capsid through the hexamer pores on the hiv-1 capsid. therefore, the capsid-coated hiv-1 virus prevents the encapsidated reverse-transcription production from being sensed by the cytosolic nucleic-acid sensors (146) . hiv-1 capsids can be ubiquitinated and then degraded by the host e3 ubiquitin ligase function of trim5, which leads to detection of viral dna, meanwhile hiv-1 could use some host protein like cyclophilins to evade the sensing (147, 148) (figure 2a) . similarly, other viruses also have evasion mechanisms to escape cgas-sting pathway surveillance (table 3) . therefore, identifying and preventing such viral-evasion factors could be a viable means to design novel anti-viral drugs. cgas-sting pathway is responsible to protect against intracellular or extracellular bacterial infection (especially hsv, herpes simplex virus; cmv, cytomegalovirus; irhom2, inactive rhomboid protein 2; trapβ, translocon-associated protein β; kshv, kaposi's sarcoma-associated herpes virus; hdp-rnp, hexim1-dna-pk-paraspecklecomponents-ribonuclear protein complex; lana, latency-associated nuclear antigen; virf1, viral interferon regulatory factor 1; plpro, papain-like protease; lc3, light chain3; mtor, mechanistic target of rapamycin; traf3, tnf receptor associated factor 3; hcv, hepatitis c virus; hpv, human papilloma virus; hbv, hepatitis b virus; hiv, human immunodeficiency virus; nf-κb, nuclear factor-κ b. intracellular infections). cdns (e.g., c-dgmp, c-damp, and cgamp) produced by bacteria are essential for the regulation of bacterial function, such as biofilm formation, colonization, and reproduction (149, 150) . as ligands for sting, cdns can bind directly to and activate sting independently of cgas, which contributes to several immune responses from bacteria (151) . usually, bacteria can enter or be engulfed by the cell through the endophagosome and be sequestered from the cytosolic sense receptor. some bacteria, such as mycobacterium tuberculosis (mtb), can survive in vacuoles, resulting in an insufficient cellular immune response to defend against it (152) . in contrast, the esx-1 secretion system of the mycobacterium can translocate the phagosomal vacuolar matrix including bacterial genome molecules into the cytoplasm and trigger the cgas-sensing pathway (153) . for other bacteria, such as legionella pneumophila or and brucella abortus, the host guanylate binding proteins (gbps) facilitate rupture of phagosome vacuoles and are indispensable for controlling their infection (154, 155) . autophagy signaling mediated by cgas/sting is also involved in microorganism clearance mentioned above (90, 91) . bacteria have evolved strategies to confront this pathway too. bacterial phosphodiesterase cdnp produced by mtb or group-b streptococci can degrade cdns (156, 157) . cpsa (a type of mtb lytr-cpsa-psr domain-containing protein) can prevent autophagy responses for eliminating pathogens (90) . chlamydia trachomatis inclusion membrane proteins can maintain the stability of the inclusion membrane and avoid inclusion lysis (leading to pathogen antigens leaking out and being detected by the host cell) (158, 159) . yersinia outer protein j (yopj) deubiquitinates sting and impedes the formation of the sting signalosome (160) . the cgas-sting pathway activation even impedes the elimination of listeria monocytogenes because bacterial dna can be packaged into evs and transferred into t cells, where it induces apoptosis of t cells (161, 162) . several protozoans, such as toxoplasma gondii and malaria parasites, have an intracellular period in their lifecycle. t. gondii could engage cgas-sting exclusively (163) . however, irf3 activation inducing isg expression promotes t. gondii development independently of ifn expression (163) . p. falciparum can target erythrocytes, lacking a nucleus and unable produce ifn, but infected erythrocytes can secrete evs containing parasitic gdna to monocytes and trigger cgas (164) . the immune system is regulated by a complicated network. disorder of immune signaling can elicit non-infectious inflammatory or autoimmune diseases. excessive, uncontrolled production of type-i ifn can lead to a spectrum of inflammation diseases termed "type-i interferonopathies, " which have some common manifestations (165) . cgas-sting is the one of main sources of type-i ifn, acts as a cellular immune-sensing signaling axis, and is involved in type-i interferonopathies. stimulator of interferon genes -associated vasculopathy with onset in infancy (savi) is a typical sting-related hereditary inflammatory type-i interferonopathy, and is manifested by interstitial lung disease, dermatomyositis and arthritis. its pathology is featured by leukocytoclastic vasculitis and microthrombotic angiopathy of small dermal vessels (166, 167) and patients can also suffer from lymphopenia (166) (167) (168) (169) . the etiology of savi is a gain of function (gof) mutant in sting which leads to constitutive sting activation without cdns stimulation (166) . currently, several mutant amino acids residues have been found in or close to the dimerization domain (v155m, n154s, g166e, v147l, and v147m) (64, 166, 168, 170) , as well as r284g, r284s, r281q, and c206y in the cgamp-binding domain (171) . other types of type-i interferonopathies, such as systemic lupus erythematosus (sle) and aicardi-goutières syndrome (ags), have relationships with defective clearance of cytosolic nucleic acids caused by congenital dysfunction of trex1, rnaseh2, and samhd1. sle is a heterogeneous autoimmune disease which has prominent type-i and also -ii ifn signatures (172) . ags comprises some systemic autoimmune syndromes overlapping with sle, and can be classified as a "lupuslike disease" (173) . additionally, ags also causes severe developmental neurological disorders, including cerebral calcifications, encephalopathy and cerebral atrophy. systemic lupus erythematosus is a representative model for elucidating the mechanism of type-i interferonopathies. in sle, the level of self-dna which is packaged into apoptosis-derived membrane vesicles along with the level of anti-dsdna antibody is increased in the serum of patients (174) . a study revealed increasing levels of isgs (including cgas/sting) as well as the cgamp-detected ratio in peripheral-blood mononuclear cells of sle patients (175) . as innate immune cells, dcs have essential roles in antigen presentation, cytokine secretion, and priming the adaptive response of immune cells (176) . plasmacytoid dcs (pdcs) can internalize and recognize self-dna and they are the main source of type-i ifn in serum during sle (177) . ifnα/β is essential for complete function of immature pdcs (178) . ifnα/β and il-1 can induce mitochondrial oxidative stress in dcs and decrease atp production, which blocks proton-pump function and increases ph of lysosomes. this process inhibits mitochondrial degradation and blocks mtdna clearance, which engages the cgas-sting pathway (31, 179). moreover, monocytes may sense mtdna through cgas-sting and differentiate into dcs (31, 180). neutrophil extracellular traps (nets) are complexes released by neutrophils exposed to stimuli or autoantibody immune complexes. nets comprise extracellularly released chromatin, myeloperoxidase enzymes, and also oxidized mtdna. in lupus-like diseases, nets can be induced by ifnα/β and may play a major part in priming pdcs (181, 182) . all mechanisms stated above contribute to a more aggravated type-iifn response and exacerbate disease. a similar phenomenon can be observed in savi, ataxia telangiectasia (at) and artemis deficiency (183) . however, compared with savi, dcs in sle can prime t-cell maturation significantly and increasing secretion of pro-inflammatory cytokines, such as il-6 and tnfα can also lead to activation of adaptive immunity ( figure 4a) . the cgas-sting pathway can mediate systemic inflammation as well as autoimmune activation. however, it is also involved in the local inflammation of multiple tissues. with regard to ischemic myocardial infarction (mi), cardiac macrophages can sense dying ruptured cells and lead to fatal post-mi cardiac inflammation, which is reversed by ablation of cgas/sting/irf3 (184, 185) . in a non-alcoholic steatohepatitis (nash) model induced by a methionine-and choline-deficient or high-fat diet, lipotoxicity can cause mitochondrial damage and up-regulate sting/irf3 expression in hepatocytes, which in turn promotes lipid accumulation and inhibits glycogen synthesis. all above bring out hepatic inflammation and hepatocytes apoptosis (186) . in this model, mice with deficiency of sting presents alleviated insulin resistance and lower levels of low-density lipoprotein in serum, and also decreased hepatic inflammation and fibrosis/steatosis, in which hepatic macrophages/kupffer cells may take a big part (187, 188) . lipotoxicity can induce p62 to be phosphorylated through the cgas-sting-tbk1 pathway, which causes aggravated protein inclusions in hepatocytes and it indicates that p62 could be a biomarker for nash prognosis (189) . mtdna-dependent inflammation induced by lipotoxicity also occurs in adipose tissue and endothelial cells of blood vessels, which contributes to tissue inflammation, insulin resistance, and cardiovascular diseases (42, 190) . in traumatic brain injury (tbi), local injury initiates breakdown of the blood-brain barrier and global neuroinflammation (191) . sting expression is up-regulated in tbi and can lead to increased expression of pro-inflammatory cytokines and enlargement of secondary injury (192) . reduced autophagy-associated protein expression induced by sting may contribute to the dysfunction of autophagy and dampen the elimination of necrotic tissue, thereby intensifying inflammation (192) . during silicosis, silica can yield cytosolic dsdna release and engage cgas-sting, which activates dcs and macrophages to cause severe lung inflammation. it also leads to death of epithelial cells through the nlrp3 pathway and pulmonary fibrosis (193) . similarly, mtdna release in renal tubule cells has been found to be associated with acute kidney injury by cytotoxic drugs and chronic renal fibrosis (194, 195) . neurodegenerative diseases are correlated with local inflammation (196) . in the central nervous system (cns), microglia is considered to be the main source of cgas-sting-dependent ifn expression (197) . in neurodegenerative diseases, levels of the marker of microglia activation-cluster of differentiation 68 (cd68), and pro-inflammatory cytokines are increased (198) . a significant feature of parkinson's disease (pd) is the neuronal loss of cerebral nuclei (especially dopaminergic neurons in the substantianigra). serine/threonine-protein kinase pink1 and e3 ubiquitin-protein ligase parkin are ubiquitinrelated factors that take part in removing damaged mitochondria by autophagy, and their dysfunction lead to the early onset of pd (199) . parkin −/− and pink1 −/− mice, following exhaustive exercise, show inflammation and loss of dopaminergic neurons, which can be rescued by loss of sting (200) . similarly, at is a genetic disease caused by missense mutation of a dna-repair protein: atm. at patients usually show neurodegenerative defects (especially ataxia) complicated with telangiectasia on their eyes or body, deficiency of adaptive immune cells, and predisposition to cancer (201) . nevertheless, up-regulation of expression of type-i ifn can also be found in at patients and mice, causing them to be prone to autoimmune diseases (36, 183, 202) . this syndrome is related to p53-mediated senescence but also the chronic inflammation mediated by the cgas-sting pathway which engages cytosolic uncombined broken gdna caused by atm dysfunction (127) . in addition, accumulation of cellular mtdna occurs in age-related macular degeneration characterized by retinal pigmented epithelium (rpe) degeneration. this can trigger chronic inflammation by cgas-sting pathway, in which nlrp3 inflammasomes, inflammatory/apoptotic caspases are also involved (203, 204) . with regard to other diseases in which adaptive immune cells prime, cgas-sting has a different role. multiple sclerosis (ms) is a local inflammatory disease of cns. ms is characterized by over-reactive microglia, infiltration of self-reactive t cells, demyelization of nerve fibers and hyperplasia of gliocytes. autoantibodies against proteins expressed in immune-privileged regions of cns also contribute to its pathogenesis (205) . in ms, ifnα/β can attenuate disease severity effectively. this implies a protective role for type-i ifn in cns, which is considered to counteract the pro-inflammatory ifnγ (206) . using experimental autoimmune encephalitis (eae) as a ms model, sting was found to be indispensable for amelioration of type-i ifnmediated neuroinflammation, and it could be induced by a conventional anti-viral drug ganciclovir (207) . ultraviolet (uv) radiation is a factor inversely related to the morbidity of ms (208) . it was found that uv-b irradiation can recruit inflammatory monocytes and produce type-i ifn in a sting-dependent manner (209) . all above indicate that cgas-sting-ifnα/β pathway may have a beneficial effect on some cns inflammatory diseases such as ms. a possible reason for the observed effect above is due to indoleamine 2,3-dioxygenase (ido), which can catabolize tryptophan (trp) oxidatively. trp withdrawal or trpoxidative catabolites can interact with general control non-derepressible 2 (gcn2) and mtor, of which both can control cellular aminoacid metabolism and suppress t helper 1 (t h 1) cells immunity (210) . ifnα/β is a potent ido inducer to suppress proliferation of cd4 + t h 1 cells and promote differentiation of foxp3 + regulatory t (t reg ) cells, which are believed to suppress cnsspecific autoimmunity (210, 211) . in addition, dna released from dying cells can be internalized directly by t cells and sensed by cgas-sting pathway, which leads to enhancement of the t h 2 transcription factor gata3 but suppression of the t h 1 transcription factor t-bet. consequently, this process polarizes naive t cells toward t h 2 differentiation (212). studies mentioned above may (at least in part) explain why the cgas-sting signal is a negative regulator of ms. the inhibitory role of cgas-sting in inflammation is also attributed to its apoptosis-triggering role. in some subtypes of savi and mouse models, apoptosis of blood-vessel endothelial cells or bronchial epithelial cells and leucopenia can be observed (especially t-cell lymphopenia) (166, 169, 170) . when the sting signal is stimulated, apoptosis occurs more frequently in normal or cancerous t cells (119) . also, bone-marrow chimeras and gene-knockout studies have shown that t cells defect in savi are not associated with type-i ifn signaling or cgas (213, 214) . localization of sting at the golgi can cause delay of t-cell mitosis and reduced proliferation independently of irf3 and tbk1 (215) . furthermore, a "upr motif " on the c-terminus of sting can cause er stress and upr, resulting in ca 2+ overloading and t-cell death (82) . a controversial view is that b cells express sting variously and may undergo apoptosis through this way (166, 216, 217) . however, simultaneous signaling by sting and the b-cell antigen receptor can promote b-cell activation and antibody production independently of type-i ifn (217) (figure 4b) . as for some diseases with inflammatory responses involved, the acute phase of pancreatitis causes dying acinar cells to produce free dsdna, which activates cgas-sting signaling in macrophages, and exacerbates inflammation severity (218) . however, in the chronic phase of pancreatitis, cgas-sting activation decreases pancreatic inflammation, which may be mediated by limiting t h 17 response (219). for gut mucosal immunity, transient stimulation of sting could strengthen the function of antigen-presenting cells (apcs) and promote t h 1 and t h 17 immune responses against microbes (220) . chronic sting signaling, however, elicits an il-10 response to control the inflammation and avoids inflammatory enterocolitis such as bowel disease (221) . sting knockout mice present reduced numbers of goblet cells, a decreased ratio of commensal versus harmful bacteria and compromised t reg cells in the gut, making it prone to enterocolitis (222) . chromosomal instability (cin) is an intrinsic feature of cancer, and results spontaneously from errors in chromosome segregation during the mitosis of cancer cells. cin can also be induced manually by radiotherapy or chemotherapy, which causes dsbs. it results in micronuclei formation outside the nucleus, of which rupture brings out irrepressible accumulation of cytosolic self-dna and engages cgas (32, 38, 223). however, normal mitotic processes involve exposure of chromosomal dna to the cytoplasm, but this cannot initiate a substantial inflammatory reaction or apoptosis because nucleosomes can suppress dsdna-cgas binding in a competitive manner (41). an appropriate immune response against tumors via a type-i ifn plays an indispensable part in limiting tumors and prolonging host survival (224) . it was found sting-deficient mice are prone to developing several types of cancer and have poor survival under a tumor burden, whereas stimulation of sting can elicit robust immunity to tumors (225) (226) (227) . a mechanism is many cancer cells expressing cgas can recognize cytosolic dna and produce cgamp to stimulate secretion of type-i ifn through sting (228, 229) . excessive expression of trex1 in cancer cells, which can be induced by radiotherapy, attenuates this progression (228) . cgas-sting can also promote senescence of cancer cells through the p53-p21 pathway (129) . cgas-sting-mediated autophagy contributes to autophagic cell death if mitotic crisis occurs to avoid transformation of cancer cells (121) . melanoma cells can also transfer cgamp produced by them to proximal non-cancerous host cells through gap-junction channels and activate sting in these cells, which contributes to the recruitment of tumor-infiltrating immune cells such as natural killer (nk) cells (51, 230) . expression of the nk cellspecific ligand nkg2d retinoic acid early transcript 1 (rae1) on cancer cells is highly up-regulated by sting once nk cells permeate into tumor tissue (231) . the activation of sting in the endothelium within the tumor microenvironment (tme) could contribute to the remodeling of tumor vasculatures, and may have positive effects on tumor regression (232) . dendritic cells are the main source of type-i ifn in several types of tmes and are dependent on sting signaling (229) . more preferentially than macrophages, infiltrating dcs take up tumor-derived dna or cgamp from dying cell fragments by phagocytosis (27, 29, 129, 226, 233) . moreover, cancer cells can package dna into exosomes and transfer dna to dcs (234) . produced cgamp by cancer cells can also be transferred to dcs through forming gap junction (53) . by activating cgas-sting signal in dcs, cd8α + subtype dcs secret chemokines such as ccl5 and cxcl10 and crossprime infiltrating anti-tumor cd8 + t cells (29, 226, (235) (236) (237) . in contrast, numbers of immune-suppressing cells such as t reg cells, myeloid-derived suppressor monocytes and m2 macrophages have been reported to be decreased (225, 238, 239) . expression of il-15/il-15rα complex is up-regulated in myeloid cells with the help of sting/type-i ifn and promotes tumor regression (240) . tumor cells can evade intrinsic cellular surveillance in different ways. in various cancer cell lines, cgas, sting, tbk1, and irf3 are mutated frequently and their decreased expressions are also related to the high level of methylation (241) . sting expression has been shown to be suppressed by the alternative lengthening of telomeres (alt) pathway, which is responsible for prolonging the telomere length and maintaining the proliferation of tumor cells (242) . a hypoxic environment in tumor cells can lead to accumulation of lactic acid and is associated with the inhibition of tumor-conditional dcs and reduced expression of ifn signaling molecules (243) . in breast cancer, functional up-regulation of expression of human epidermal growth factor receptor 2 (her2), a ligand-independent receptor tyrosine kinase (rtk), can arrest the expression of rac-alpha serine/threonineprotein kinase (akt1) (a key factor in the mtor pathway), which is reported to inhibit the activation of cgas and tbk1 (244, 245) . patients with lung adenocarcinoma have a low probability of survival if they have reduced expression of cgas (132) . thus, expression of the cgas-sting and dna-damage marker histone γh2ax in tumor cells could be considered as independent prognostic factors to predict therapy response and clinical outcome, and could be superior to that of traditional markers like immunogenic cell death and t cells number (246) . however, some scholars have arrived at opposite conclusions. when dsbs occur in cancer cells, cgas can be relocated to the nucleus and obstruct the formation of the parp1-timeless complex, thereby inhibiting homologous recombination repair and maintaining cin, which potentiates tumor evolution (35, 223) . it has also been reported that cgas recognizing cin activates non-canonical nf-κb signaling and potentiates cellular metastasis programs (247) . furthermore, sting −/− mice are resistant to skin carcinogenesis in a 7,12-dimethylbenz(a)anthracene (dmba)-treatment model. it has been demonstrated that when dmba-induced nuclear dna leaks into the cytoplasm, sting can induce chronic inflammatory stimulation that contributes to cancer development (248) . during brain metastasis, cgamp transferred to bystander cells (e.g., astrocytes) can also produce ifnα and tnfα in the tme but, in this context, it will support tumor development and chemoresistance (249) . coordinating with myeloid cells penetrating into the tumor, myeloidderived suppressor cells can also be recruited through the c-c chemokine receptor type 2 (ccr2) (250) . another study found that microparticles yielded by tumor cells can turn macrophages into the m2 type through cgas-sting-tbk1, contrary to previous findings (251) . immune-system interactions with tumor cells are complicated. the effect of cgas-sting on cancer is dependent on the type of tumor, host immune state, activated cell types, therapeutic intervention, and the magnitude of cgas-sting activation. like inflammation generated by cgas-sting, a time-dependent inflammatory anti-tumor response mediated by cgas-sting may be present. temporary activation of cgas-sting in innate immune cells could enhance the anti-tumor effect, whereas sustained activation of cgas-sting might induce immune tolerance of the tumor. more investigations are necessary to ascertain the exact role of cgas-sting in oncology, and elucidate the specific advantages and adverse effects of targeting the cgas-sting pathway in cancer therapy ( figure 5 ). considering the pivotal role of the cgas-sting pathway in infection, inflammation and cancer, positive modulation of the pathway signaling is a promising way to enhance the immune state and restrict microorganisms or heterogeneous cells, whereas negative modulation can control aberrant inflammation. radiotherapy or chemotherapy drugs such as cisplatin or cyclophosphamide can induce dsbs and micronuclei, then trigger the cgas-sting pathway to enhance tumor immunogenicity (252) (253) (254) . in addition, parp inhibitors such as olaparib have promising effects on cancer cells lacking brca2 because of their cooperative dna-repair functions (253) . although cgas activation is inhibited by nucleosomes, taxol can induce mitotic cell-cycle arrest and sustain divided chromatin in the cytosol to activate the cgas-sting pathway slowly, and accumulation of signaling could stimulate apoptosis of cancer cells (41). inhibitors of topoisomerase 1 or 2 used conventionally as chemotherapy drugs trigger minor damage to dna and accumulation of cytosolic dna, which can engage cgas and enhance the anti-tumor or anti-infection responses of cells (255) (256) (257) . cgas-sting is essential on anti-tumor immune checkpoints therapies. for example, blockade of cd47-signal regulatory protein α (sirpα) signaling on dcs can activate nadph oxidase 2 (nox2) and increase the ph in phagosomes along with incomplete degradation of mtdna, which can trigger cgas-sting (129) . sting deficiency in mice abrogates the anti-tumor effect of cd47 blockade (258) . a similar phenomenon also can be seen in anti-programmed cell death-1 (pd-1) therapy (259) . there is greater infiltration of ifnγ + cells and cd8 + t cells and pd-1/pd-1 ligand 1 (pd-l1) expression in tme treated by sting-ligand derivatives (260) . therefore, in several types of tumors, combined administration of a sting agonist and immune-checkpoint antibody could elicit a more curative outcome compared with one therapy alone (238, 261) . viruses can infect cells lacking cgas-sting more effectively, and have higher oncolytic activity compared with virus therapy alone. hence, the use of oncolytic viruses such as talimogene laherparepvec is beneficial for treating tumors with low expression of cgas/sting. sting expression can be regarded as a prognostic measurement for such therapy (262) . some artificial analog molecules of cdns, such as 5,6dimethylxanthenone-4-acetic acid (dmxaa) and 10-carboxymethyl-9 (10h) acridone (cma) can bind the cdn pocket of mouse-specific sting dimers and promote conformational transition of sting from inactive "open" to an active "closed" state (263, 264) . dmxaa showed convincing efficacy in restraining tumors in mice (265) . however, dmxaa is restricted in activating mouse-specific sting but not humanspecific sting, which could be an explanation for the failure of dmxaa in treating 1299 non-small-cell lung cancer patients in a phase-iii clinical trial (nct00662597) (266) . nonetheless, with three substitutions (g230i, q266i, and s162a), human sting can also be induced by dmxaa to undergo conformational transition (264) . another new compound, amidobenzimidazole, has been found to be an agonist of sting without lid closure and has potential therapeutic value (267) . cyclic dinucleotides and their derivates that can stimulate sting directly are candidate adjuvants to restrain tumors. intratumoral administration of c-damp, c-dgmp, or cgamp analogs alone or combined with other adjuvants or tumor antigens have shown anti-tumor effects (259, 268) ; phase-i or ii clinical trials (nct02675439, nct03172936, and nct03937141) of dithio-(rp,rp)-c-damp (known as adu-s100) are ongoing (261) . to avoid the degradation and ensure maximal phagocyte internalization of cdns, endosomolytic nanoparticles have been designed to package and deliver cdns. for example, ph-sensitive nanoparticles (e.g., stingnanoparticles) can release their contents if located in acidic endosomal environments (269) . for treatment of type-i interferonopathies, lessons can be taken from the treatment of canonical autoimmune disease such as sle, but there are several differences. for example, it was found that corticosteroid pulse therapy, γ-immunoglobulins, disease-modifying anti-rheumatic drugs, anti-cd20, and some immunosuppressants (e.g., methotrexate) have limited efficacy against savi (166, 171) . jak inhibitors such as ruxolitinib, tofacitinib and baricitinib that reduce type-i ifn downstream signaling have shown therapeutic value against savi, but further verification of their efficacy is needed (270) . moreover, novel immune therapies, such as anti-ifnα and anti-ifnar immunoglobin, are in clinical trials for sle. these could also be tested against savi in the future (165) . pharmaceutically screening has revealed that some antimalaria drugs, such as suramin, have an inhibitory effect on cgas by blockade of interaction between dna and cgas (271) . in addition, novel small molecules such as ru320521 or g150 can occupy the enzymatic pocket of species-specific cgas to abrogate cgamp synthesis (272, 273) . recently, a study found that aspirin can acetylate cgas at three lysine residues and block cgas activity (274) . with regard to sting, the cyclopeptide astin c can block irf3 recruitment onto the sting signalosome (275) . the molecule h-151 can block the palmitoylation of human-sting (276) . all of these agents are potential candidates for alleviating type-i interferonopathies. the cgas-sting pathway is primarily responsible for the modulation of immune response in cells when facing cytosolic dsdna challenge. moreover, it is complicatedly cross-regulated by other cellular processes or cellular signaling networks. the exact fundamental mechanism of the pathway in cells and the effect on the whole organism in specific states is not completely clear and requires further investigation. in conclusion, the cgas-sting pathway has dichotomous roles in the immune system. in general, cgas-sting-type-i ifn signaling can promote the innate immune response in myeloid cells but alleviate the adaptive immune response exerted by t cells and b cells. cgas shows high expression in apcs such as macrophages and dcs, but sting is expressed in most cells (10) . cgas-sting signaling corresponding to cytoplasmic dsdna in apcs can boost innate and adaptive immunity transiently. in this situation, the dna challenge signal is limited to only macrophages and dcs. their pro-inflammatory and antigenpresenting functions to adaptive immune cells are promoted in the short-term. if the signal spreads to other bystander cells, such as t cells, b cells, local resident cells by means of cgamp transfer, or just aberrant sting activation by gof, it causes apoptosis in bystander cells or adaptive immune cells and immune tolerance in the long-term. therefore, it is reasonable to conclude that the intrinsic function of the cgas-sting pathway is essential for the innate immune system responses of the host immediately after pathogen invasion or abnormal cell appearing. once the challenge persists, the cgas-sting pathway controls the adaptive immune system to avoid chronic, detrimental inflammatory reactions or autoimmune diseases. the inflammatory response exists universally in almost all physiologic and pathologic progressions. cgas-sting is pivotal in modulating cellular inflammation, so it is promising to extend our conception of the cgas-sting pathway onto more diseases with inflammatory responses involved, especially cns-based diseases such as stroke, in which the inflammatory reaction exists but was recognized less. moreover, for targeting the cgas-sting pathway for therapeutic purposes, drugs should be optimized to augment the desirable effect and prevent its unwanted effects. for example, to eliminate tumor cells or infectious agents, agonists of cgas-sting would be a rational option if designed to target apcs exclusively but not t cells or b cells. in this scheme, the antitumor immune response is enhanced while avoiding apoptosis of adaptive immune cells and infiltration of immune suppressor cells. also, most research on the cgas-sting pathway has focused on its ifn-expressing role but overlooked autophagy and cell-death roles, which are also main downstream signaling of the pathway. therefore, some drugs, such as emricasan, are potential apoptosis inhibitors that may have a complementary effect on ameliorating apoptosis of blood-vessel endothelial cells or bronchial epithelial cells, and lymphopenia, in savi. until now, studies of the cgas-sting pathway have been done mainly in the laboratory but it has large space to be explored in clinical or translational fields. additionally more prrs and cellular immune-surveillance pathways may remain to be discovered to piece together the molecular puzzles of the cell. dw drafted the manuscript and drew the figures. wj and jh conceived and revised the review. frontiers in immunology | www.frontiersin.org recognition of endogenous nucleic acids by the innate immune system sting is an endoplasmic reticulum adaptor that facilitates innate immune signalling the adaptor protein mita links virus-sensing receptors to irf3 transcription factor activation an endoplasmic reticulum ifn stimulator, activates innate immune signaling through dimerization c-di-amp secreted by intracellular listeria monocytogenes activates a host type i interferon response sting is a direct innate immune sensor of cyclic di-gmp ifi16 is an innate immune sensor for intracellular dna cyclic gmp-amp synthase is a cytosolic dna sensor that activates the type i interferon pathway pivotal roles of cgas-cgamp signaling in antiviral defense and immune adjuvant effects an expression atlas of human primary cells: inference of gene function from coexpression networks bacterial cgas-like enzymes synthesize diverse nucleotide signals structural mechanism of cytosolic dna sensing by cgas structure of human cgas reveals a conserved family of second-messenger enzymes in innate immunity cytosolic rna:dna hybrids activate the cgas-sting axis sequence-specific activation of the dna sensor cgas by y-form dna structures as found in primary hiv-1 cdna cgas produces a 2 -5 -linked cyclic dinucleotide second messenger that activates sting the catalytic mechanism of cyclic gmp-amp synthase (cgas) and implications for innate immunity and inhibition the cytosolic dna sensor cgas forms an oligomeric complex with dna and undergoes switch-like conformational changes in the activation loop cyclic gmp-amp synthase is activated by double-stranded dna-induced oligomerization structure of the human cgas-dna complex reveals enhanced control of immune surveillance cgas senses long and hmgb/tfam-bound u-turn dna by forming protein-dna ladders dna-induced liquid phase condensation of cgas activates innate immune signaling human cgas catalytic domain has an additional dna-binding interface that apoptotic caspases suppress mtdna-induced sting-mediated type i ifn production obsessive-compulsive disorder is associated with broad impairments in executive function: a meta-analysis ribonuclease h2 mutations induce a cgas/sting-dependent innate immune response restriction by samhd1 limits cgas/sting-dependent innate and adaptive immune responses to hiv-1 host restriction factor samhd1 limits human t cell leukemia virus type 1 infection of monocytes via sting-mediated apoptosis samhd1 acts at stalled replication forks to prevent interferon induction cyclic gmp-amp containing mixed phosphodiester linkages is an endogenous high-affinity ligand for sting cyclic gmp-amp synthase is an innate immune sensor of hiv and other retroviruses cell intrinsic immunity spreads to bystander cells via the intercellular transfer of cgamp connexin-dependent transfer of cgamp to phagocytes modulates antiviral responses cancer-cell-intrinsic cgas expression mediates tumor immunogenicity viruses transfer the antiviral second messenger cgamp between cells transmission of innate immune signaling by packaging of cgamp in viral particles cgas-mediated innate immunity spreads intercellularly through hiv-1 envinduced membrane fusion sites priming of dendritic cells by dna-containing extracellular vesicles from activated t cells through antigen-driven contacts cells infected with herpes simplex virus 1 export to uninfected cells exosomes containing sting, viral mrnas, and micrornas slc19a1 is an importer of the immunotransmitter cgamp slc19a1 transports immunoreactive cyclic dinucleotides hydrolysis of 2 3 -cgamp by enpp1 and design of nonhydrolyzable analogs cgas facilitates sensing of extracellular cyclic dinucleotides to activate innate immunity sting regulates intracellular dna-mediated, type i interferon-dependent innate immunity activation by translocation from the er is associated with infection and autoinflammatory disease atg9a controls dsdna-driven dynamic translocation of sting and the innate immune response irhom2 is essential for innate immunity to dna viruses by mediating trafficking and stability of the adaptor sting tmed2 potentiates cellular ifn responses to dna viruses by reinforcing mita dimerization and facilitating its trafficking autophagy induction via sting trafficking is a primordial function of the cgas pathway phosphorylation of innate immune adaptor proteins mavs, sting, and trif induces irf3 activation sting specifies irf3 phosphorylation by tbk1 in the cytosolic dna signaling pathway modular architecture of the sting c-terminal tail allows interferon and nf-kappab signaling adaptation structural basis of sting binding with and phosphorylation by tbk1 a conserved plplrt/sd motif of sting mediates the recruitment and activation of tbk1 activation of sting requires palmitoylation at the golgi ubiquitination of sting at lysine 224 controls irf3 activation non-canonical nf-kappab antagonizes sting sensor-mediated dna sensing in radiotherapy immunomodulatory functions of type i interferons dna-binding landscape of irf3, irf5 and irf7 dimers: implications for dimer-specific gene regulation attenuation of cgas-sting signaling is mediated by a p62/sqstm1-dependent autophagy pathway activated by tbk1 positive feedback regulation of type i ifn production by the ifn-inducible dna sensor cgas positive feedback regulation of type i interferon by the interferon-stimulated gene sting sting-mediated disruption of calcium homeostasis chronically activates er stress and primes t cell death sting senses microbial viability to orchestrate stress-mediated autophagy of the endoplasmic reticulum chronic innate immune activation of tbk1 suppresses mtorc1 activity and dysregulates cellular metabolism mtor signaling in growth, metabolism, and disease crosstalk between the cgas dna sensor and beclin-1 autophagy protein shapes innate antimicrobial immune responses a brief history of autophagy from cell biology to physiology and disease autophagy in the renewal, differentiation and homeostasis of immune cells sting directly activates autophagy to tune the innate immune response mycobacterium tuberculosis is protected from nadph oxidase and lc3-associated phagocytosis by the lcp protein cpsa extracellular m. tuberculosis dna targets bacteria for autophagy by activating the host dna-sensing pathway upr, autophagy, and mitochondria crosstalk underlies the er stress response dnase2a deficiency uncovers lysosomal clearance of damaged nuclear dna via autophagy self-consumption: the interplay of autophagy and apoptosis trafficking-mediated sting degradation requires sorting to acidified endolysosomes and can be targeted to enhance anti-tumor response the dna inflammasome in human myeloid cells is initiated by a sting-cell death program upstream of nlrp3 aim2 recognizes cytosolic dsdna and forms a caspase-1-activating inflammasome with asc antagonism of the sting pathway via activation of the aim2 inflammasome by intracellular dna inflammasome activation triggers caspase-1-mediated cleavage of cgas to regulate responses to dna virus infection gasdermin d restrains type i interferon response to cytosolic dna by disrupting ionic homeostasis a noncanonical function of cgamp in inflammasome priming and activation viral dna binding to nlrc3, an inhibitory nucleic acid sensor, unleashes sting, a cyclic dinucleotide receptor that activates type i interferon non-canonical activation of the dna sensing adaptor sting by atm and ifi16 mediates nf-kappab signaling after nuclear dna damage nuclear ifi16 induction of irf-3 signaling during herpesviral infection and degradation of ifi16 by the viral icp0 protein ifi16 is required for dna sensing in human macrophages by promoting production and function of cgamp ifi16 and cgas cooperate in the activation of sting during dna sensing in human keratinocytes cgas-mediated stabilization of ifi16 promotes innate signaling during herpes simplex virus infection viral dna sensors ifi16 and cyclic gmp-amp synthase possess distinct functions in regulating viral gene expression, immune defenses, and apoptotic responses during herpesvirus infection sting-mediated ifi16 degradation negatively controls type i interferon production assembly and localization of toll-like receptor signalling complexes sting requires the adaptor trif to trigger innate immune responses to microbial infection sequential activation of two pathogen-sensing pathways required for type i interferon expression and resistance to an acute dna virus infection cross-regulation of two type i interferon signaling pathways in plasmacytoid dendritic cells controls anti-malaria immunity and host mortality oxidative damage of dna confers resistance to cytosolic nuclease trex1 degradation and potentiates sting-dependent immune sensing mitochondria and cell death: outer membrane permeabilization and beyond mitochondrial inner membrane permeabilisation enables mtdna release during apoptosis apoptotic caspases prevent the induction of type i interferons by mitochondrial dna apoptotic caspases suppress type i interferon production via the cleavage of cgas, mavs, and irf3 signalling strength determines proapoptotic functions of sting puma amplifies necroptosis signaling by activating cytosolic dna sensors autophagic cell death restricts chromosomal instability during replicative crisis induction of necroptotic cell death by viral activation of the rig-i or sting pathway tnfalpha and radioresistant stromal cells are essential for therapeutic efficacy of cyclic dinucleotide sting agonists in nonimmunogenic tumors cellular senescence: aging p16ink4a induces an age-dependent decline in islet regenerative potential autophagy mediates degradation of nuclear lamina extranuclear dna accumulates in aged cells and contributes to senescence and inflammation senescenceassociated secretory phenotypes reveal cell-nonautonomous functions of oncogenic ras and the p53 tumor suppressor cytoplasmic chromatin triggers inflammation in senescence and cancer downregulation of cytoplasmic dnases is implicated in cytoplasmic dna accumulation and sasp in senescent cells innate immune sensing of cytosolic chromatin fragments through cgas promotes senescence cgas is essential for cellular senescence dna-damage-induced type i interferon promotes senescence and inhibits stem cell function bacterial c-di-gmp affects hematopoietic stem/progenitors and their niches through sting a circular rna protects dormant hematopoietic stem cells from dna sensor cgas-mediated exhaustion pqbp1 is a proximal sensor of the cgas-dependent innate response to hiv-1 nono detects the nuclear hiv capsid to promote cgas-mediated innate immune activation p53 induces formation of neat1 lncrna-containing paraspeckles that modulate replication stress response and chemosensitivity hexim1 and neat1 long non-coding rna form a multi-subunit complex that regulates dna-mediated innate immune response stingdependent translation inhibition restricts rna virus replication inhibition of hiv-1 disease progression by contemporaneous hiv-2 infection samhd1 is the dendritic-and myeloid-cell-specific hiv-1 restriction factor counteracted by vpx reshaping of the dendritic cell chromatin landscape and interferon pathways during hiv infection the capsids of hiv-1 and hiv-2 determine immune detection of the viral cdna by the innate sensor cgas in dendritic cells hiv-1 activation of innate immunity depends strongly on the intracellular level of trex1 and sensing of incomplete reverse transcription products hiv-1 uses dynamic capsid pores to import nucleotides and fuel encapsidated dna synthesis restriction of hiv-1 and other retroviruses by trim5 hiv-1 evades innate immune recognition through specific cofactor recruitment cyclic di-gmp: second messenger extraordinaire cyclic gmp-amp signalling protects bacteria against viral infection a bacterial cyclic dinucleotide activates the cytosolic surveillance pathway and mediates innate resistance to tuberculosis tuberculosis pathogenesis and immunity mycobacterium tuberculosis differentially activates cgas-and inflammasome-dependent intracellular immune responses through esx-1 brucella abortus triggers a cgas-independent sting pathway to induce host protection that involves guanylate-binding proteins and inflammasome activation beneficial effects of yogasanas and pranayama in limiting the cognitive decline in type 2 diabetes group b streptococcus degrades cyclic-di-amp to modulate stingdependent type i interferon production inhibition of innate immune cytosolic surveillance by an m. tuberculosis phosphodiesterase absence of specific chlamydia trachomatis inclusion membrane proteins triggers premature inclusion membrane lysis and host cell death the chlamydia trachomatis inclusion membrane protein cpos counteracts sting-mediated cellular surveillance and suicide programs yersinia yopj negatively regulates irf3-mediated antibacterial response through disruption of sting-mediated cytosolic dna signaling intracellular bacteria engage a sting-tbk1-mvb12b pathway to enable paracrine cgas-sting signalling sting-dependent type i ifn production inhibits cell-mediated immunity to listeria monocytogenes induction of interferon-stimulated genes by irf3 promotes replication of toxoplasma gondii malaria parasite dna-harbouring vesicles activate cytosolic immune sensors type i interferon in rheumatic diseases activated sting in a vascular and pulmonary syndrome inherited sting-activating mutation underlies a familial inflammatory syndrome with lupus-like manifestations stimulator of interferon genes-associated vasculopathy with onset in infancy: a mimic of childhood granulomatosis with polyangiitis severe combined immunodeficiency in stimulator of interferon genes (sting) v154m/wild-type mice sting-associated vasculopathy develops independently of irf3 in mice disease-associated mutations identify a novel region in human sting necessary for the control of type i interferon signaling personalized immunomonitoring uncovers molecular networks that stratify lupus patients aicardi-goutieres syndrome and the type i interferonopathies apoptosisderived membrane vesicles drive the cgas-sting pathway and enhance type i ifn production in systemic lupus erythematosus expression of cyclic gmp-amp synthase in patients with systemic lupus erythematosus. arthritis rheumatol the role of dendritic cells in autoimmunity human plasmacytoid dentritic cells elicit a type i interferon response by sensing dna via the cgas-sting signaling pathway interferon priming is essential for human cd34+ cell-derived plasmacytoid dendritic cell maturation and function interleukin-1beta induces mtdna release to activate innate immune signaling via cgas-sting induction of dendritic cell differentiation by ifn-alpha in systemic lupus erythematosus neutrophil extracellular traps enriched in oxidized mitochondrial dna are interferogenic and contribute to lupus-like disease netting neutrophils are major inducers of type i ifn production in pediatric systemic lupus erythematosus type i ifnrelated netosis in ataxia telangiectasia and artemis deficiency cytosolic dna sensing promotes macrophage transformation and governs myocardial ischemic injury irf3 and type i interferons fuel a fatal response to myocardial infarction activation of the sting-irf3 pathway promotes hepatocyte inflammation, apoptosis and induces metabolic disorders in nonalcoholic fatty liver disease expression of sting is increased in liver tissues from patients with nafld and promotes macrophage-mediated hepatic inflammation and fibrosis in mice sting-mediated inflammation in kupffer cells contributes to progression of nonalcoholic steatohepatitis lipotoxicity induces hepatic protein inclusions through tank binding kinase 1-mediated p62/sequestosome 1 phosphorylation sting-irf3 triggers endothelial inflammation in response to free fatty acid-induced mitochondrial damage in diet-induced obesity priming the inflammatory pump of the cns after traumatic brain injury stingmediated type-i interferons contribute to the neuroinflammatory process and detrimental effects following traumatic brain injury sting-dependent sensing of self-dna drives silica-induced lung inflammation mitochondrial damage and activation of the sting pathway lead to renal inflammation and fibrosis mitochondrial damage causes inflammation via cgas-sting signaling in acute kidney injury how neuroinflammation contributes to neurodegeneration sensing of hsv-1 by the cgas-sting pathway in microglia orchestrates antiviral defence in the cns chronic neurodegeneration induces type i interferon synthesis via sting, shaping microglial phenotype and accelerating disease progression the roles of pink1, parkin, and mitochondrial fidelity in parkinson's disease parkin and pink1 mitigate sting-induced inflammation atm and the molecular pathogenesis of ataxia telangiectasia autoimmune phenomena in ataxia telangiectasia mitochondrial dna has a pro-inflammatory role in amd cgas drives noncanonical-inflammasome activation in age-related macular degeneration multiple sclerosis type i/ii interferon balance in the regulation of brain physiology and pathology activation of the sting-dependent type i interferon response reduces microglial reactivity and neuroinflammation modulation of the immune system by uv radiation: more than just the effects of vitamin d? ultraviolet b irradiation causes stimulator of interferon genes-dependent production of protective type i interferon in mouse skin by recruited inflammatory monocytes. arthritis rheumatol engineering dna nanoparticles as immunomodulatory reagents that activate regulatory t cells activation of the sting adaptor attenuates experimental autoimmune encephalitis nucleic acid sensing by t cells initiates th2 cell differentiation sting-associated lung disease in mice relies on t cells but not type i interferon hierarchy of clinical manifestations in savi n153s and v154m mouse models intrinsic antiproliferative activity of the innate sensor sting in t lymphocytes agonist-mediated activation of sting induces apoptosis in malignant b cells b cell-intrinsic sting signaling triggers cell activation, synergizes with b cell receptor signals, and promotes antibody responses sting signaling promotes inflammation in experimental acute pancreatitis habtezion a. sting signalling protects against chronic pancreatitis by modulating th17 response stingactivating adjuvants elicit a th17 immune response and protect against mycobacterium tuberculosis infection sting-dependent signaling underlies il-10 controlled inflammatory colitis the cytosolic sensor sting is required for intestinal homeostasis and control of inflammation the multifaceted role of chromosomal instability in cancer and its microenvironment immunogenic cell death in cancer and infectious disease sting contributes to antiglioma immunity via triggering type i ifn signals in the tumor microenvironment sting-dependent cytosolic dna sensing mediates innate immune recognition of immunogenic tumors suppression of sting associated with lkb1 loss in kras-driven lung cancer dna exonuclease trex1 regulates radiotherapy-induced tumour immunogenicity growing tumors induce a local sting dependent type i ifn response in dendritic cells tumorderived cgamp triggers a sting-mediated interferon response in nontumor cells to activate the nk cell response rae1 ligands for the nkg2d receptor are regulated by sting-dependent dna sensor pathways in lymphoma sting activation reprograms tumor vasculatures and synergizes with vegfr2 blockade dendritic cells but not macrophages sense tumor mitochondrial dna for cross-priming through signal regulatory protein alpha signaling exosomes shuttle trex1-sensitive ifn-stimulatory dsdna from irradiated cancer cells to dcs host type i ifn signals are required for antitumor cd8+ t cell responses through cd8{alpha}+ dendritic cells sting-dependent cytosolic dna sensing promotes radiation-induced type i interferondependent antitumor immunity in immunogenic tumors targeting dna damage response promotes antitumor immunity through sting-mediated t-cell activation in small cell lung cancer intratumoral sting activation with t-cell checkpoint modulation generates systemic antitumor immunity sting signaling remodels the tumor microenvironment by antagonizing myeloid-derived suppressor cell expansion il-15 is a component of the inflammatory milieu in the tumor microenvironment promoting antitumor responses suppression of sting signaling through epigenetic silencing and missense mutation impedes dna damage mediated cytokine production extrachromosomal telomere repeat dna is linked to alt development via cgas-sting dna sensing pathway downregulation of membrane trafficking proteins and lactate conditioning determine loss of dendritic cell function in lung cancer her2 recruits akt1 to disrupt sting signalling and suppress antiviral defence and antitumour immunity akt kinase-mediated checkpoint of cgas dna sensing pathway dna damage predicts prognosis and treatment response in colorectal liver metastases superior to immunogenic cell death and t cells chromosomal instability drives metastasis through a cytosolic dna response inflammation-driven carcinogenesis is mediated through sting carcinomaastrocyte gap junctions promote brain metastasis by cgamp transfer host stingdependent mdsc mobilization drives extrinsic radiation resistance tumor cellderived microparticles polarize m2 tumor-associated macrophages for tumor progression parp inhibition enhances tumor cell-intrinsic immunity in ercc1-deficient non-small cell lung cancer parp inhibitor efficacy depends on cd8(+) t-cell recruitment via intratumoral sting pathway activation in brca-deficient models of triple-negative breast cancer radiotherapy combined with novel sting-targeting oligonucleotides results in regression of established tumors topoisomerase 1 inhibition promotes cyclic gmp-amp synthasedependent antiviral responses topoisomerase ii inhibitors induce dna damage-dependent interferon responses circumventing ebola virus immune evasion cgas/sting axis mediates a topoisomerase ii inhibitor-induced tumor immunogenicity cd47 blockade triggers t cell-mediated destruction of immunogenic tumors sting activation of tumor endothelial cells initiates spontaneous and therapeutic antitumor immunity a sting agonist given with ox40 receptor and pd-l1 modulators primes immunity and reduces tumor growth in tolerized mice magnitude of therapeutic sting activation determines cd8(+) t cellmediated anti-tumor immunity recurrent loss of sting signaling in melanoma correlates with susceptibility to viral oncolysis species-specific detection of the antiviral small-molecule compound cma by sting bindingpocket and lid-region substitutions render human sting sensitive to the species-specific drug dmxaa the sting agonist dmxaa triggers a cooperation between t lymphocytes and myeloid cells that leads to tumor regression randomized phase iii placebo-controlled trial of carboplatin and paclitaxel with or without the vascular disrupting agent vadimezan (asa404) in advanced non-small-cell lung cancer design of amidobenzimidazole sting receptor agonists with systemic activity sting ligand c-di-gmp improves cancer vaccination against metastatic breast cancer endosomolytic polymersomes increase the activity of cyclic dinucleotide sting agonists to enhance cancer immunotherapy efficacy of the janus kinase 1 /2 inhibitor ruxolitinib in the treatment of vasculopathy associated with tmem173-activating mutations in 3 children suramin potently inhibits cgamp synthase, cgas, in thp1 cells to modulate ifnbeta levels small molecule inhibition of cgas reduces interferon expression in primary macrophages from autoimmune mice development of human cgas-specific small-molecule inhibitors for repression of dsdnatriggered interferon expression the cyclopeptide astin c specifically inhibits the innate immune cdn sensor sting targeting sting with covalent small-molecule inhibitors trim56-mediated monoubiquitination of cgas for cytosolic dna sensing the ubiquitin ligase trim56 regulates innate immune responses to intracellular doublestranded dna the e3 ubiquitin ligase rnf185 facilitates the cgas-mediated innate immune response rnf26 temporally regulates virus-triggered type i interferon induction by two distinct mechanisms the e3 ubiquitin ligase amfr and insig1 bridge the activation of tbk1 kinase by modifying the adaptor sting trim14 inhibits cgas degradation mediated by selective autophagy receptor p62 to promote innate immune responses p38 inhibition provides anti-dna virus immunity by regulation of usp21 phosphorylation and sting activation usp18 recruits usp20 to promote innate antiviral response through deubiquitinating sting/mita the deubiquitinase cyld is a specific checkpoint of the sting antiviral signaling pathway sumoylation promotes the stability of the dna sensor cgas and the adaptor sting to regulate the kinetics of response to dna virus senp7 potentiates cgas activation by relieving sumo-mediated inhibition of cytosolic dna sensing g3bp1 promotes dna binding and activation of cgas zcchc3 is a cosensor of cgas for dsdna recognition in innate immune response manganese increases the sensitivity of the cgas-sting pathway for double-stranded dna and is required for the host defense against dna viruses tmem203 is a binding partner and regulator of sting-mediated inflammatory signaling in macrophages the erassociated protein zdhhc1 is a positive regulator of dna virus-triggered, mita/sting-dependent innate immune signaling association of abnormal elevations in ifit3 with overactive cyclic gmp-amp synthase/stimulator of interferon genes signaling in human systemic lupus erythematosus monocytes s6k-sting interaction regulates cytosolic dna-mediated activation of the transcription factor irf3 glycogen synthase kinase 3beta regulates irf3 transcription factor-mediated antiviral response via activation of the kinase tbk1 trim9 short isoform preferentially promotes dna and rna virus-induced production of type i interferon by recruiting gsk3beta to tbk1 lsm14a plays a critical role in antiviral immune responses by regulating mita level in a cell-specific manner trim29 promotes dna virus infections by inhibiting innate immune response trim30alpha is a negative-feedback regulator of the intracellular dna and dna virustriggered response by targeting sting the ubiquitin ligase rnf5 regulates antiviral responses by mediating degradation of the adaptor protein mita usp13 negatively regulates antiviral responses by deubiquitinating sting oligoadenylatesynthetase-family protein oasl inhibits activity of the dna sensor cgas during dna virus infection to limit interferon production interactome and proteome dynamics uncover immune modulatory associations of the pathogen sensing factor cgas sensing of bacterial cyclic dinucleotides by the oxidoreductase recon promotes nf-kappab activation and shapes a proinflammatory antibacterial state the ca(2+) sensor stim1 regulates the type i interferon response by retaining the signaling adaptor sting at the endoplasmic reticulum nitro-fatty acids are formed in response to virus infection and are potent inhibitors of sting palmitoylation and signaling nlrc3, a member of the nlr family of proteins, is a negative regulator of innate immune signaling induced by the dna sensor sting ppm1a regulates antiviral signaling by antagonizing tbk1-mediated sting phosphorylation and aggregation ptpn1/2-mediated dephosphorylation of mita/sting promotes its 20s proteasomal degradation and attenuates innate antiviral response nlrx1 sequesters sting to negatively regulate the interferon response, thereby facilitating the replication of hiv-1 and dna viruses nlrx1 promotes immediate irf1-directed antiviral responses by limiting dsrnaactivated translational inhibition mediated by pkr mitigating sox2-potentiated immune escape of head and neck squamous cell carcinoma with a sting-inducing nanosatellite vaccine mediates hypoxia-induced immunosuppression by repressing cgas nrf2 negatively regulates sting indicating a link between antiviral sensing and metabolic reprogramming kdm5 histone demethylases repress immune response via suppression of sting herpes simplex virus 1 abrogates the cgas/sting-mediated cytosolic dna-sensing pathway via its virion host shutoff protein, ul41 herpes simplex virus 1 tegument protein vp22 abrogates cgas/sting-mediated antiviral innate immunity species-specific deamidation of cgas by herpes simplex virus ul37 protein facilitates viral replication evasion of the sting dna-sensing pathway by vp11/12 of herpes simplex virus 1 herpes simplex virus 1 gamma134.5 protein inhibits sting activation that restricts viral replication human cytomegalovirus protein ul31 inhibits dna sensing of cgas to mediate immune evasion type i interferon production by inactivating the dna sensor cgas without affecting sting essential role of hcmv deubiquitinase in promoting oncogenesis by targeting anti-viral innate immune signaling pathways human cytomegalovirus tegument protein ul82 inhibits sting-mediated signaling to evade antiviral immunity the herpesviral antagonist m152 reveals differential activation of sting-dependent irf and nf-kappab signaling and sting's dual role during mcmv infection human cytomegalovirus-encoded us9 targets mavs and sting signaling to evade type i interferon immune responses inhibition of cgas dna sensing by a herpesvirus virion protein cytoplasmic isoforms of kaposi sarcoma herpesvirus lana recruit and antagonize the innate immune dna sensor cgas modulation of the cgas-sting dna sensing pathway by gammaherpesviruses sars coronavirus papain-like protease inhibits the type i interferon signaling pathway through interaction with the sting-traf3-tbk1 complex poxviruses evade cytosolic sensing through disruption of an mtorc1-mtorc2 regulatory circuit viral and metazoan poxins are cgamp-specific nucleases that restrict cgas-sting signalling zika virus elicits inflammation to evade antiviral response by cleaving cgas via ns1-caspase-1 axis denv inhibits type i ifn production in infected cells by cleaving human sting dengue virus ns2b protein targets cgas for degradation and prevents mitochondrial dna sensing during infection dna tumor virus oncogenes antagonize the cgas-sting dna-sensing pathway influenza a virus targets a cgas-independent sting pathway that controls enveloped rna viruses hepatitis c virus ns4b blocks the interaction of sting and tbk1 to evade host innate immunity hepatitis c virus ns4b protein targets sting and abrogates rig-i-mediated type i interferon-dependent innate immunity hepatitis b virus polymerase disrupts k63-linked ubiquitination of sting to block innate cytosolic dnasensing pathways hiv-2/siv vpx targets a novel functional domain of sting to selectively inhibit cgas-stingmediated nf-kappab signalling we thank k. wood from barrow neurological institute for discussions and editing. the authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.copyright © 2020 wan, jiang and hao. this is an open-access article distributed under the terms of the creative commons attribution license (cc by). the use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. no use, distribution or reproduction is permitted which does not comply with these terms. key: cord-334588-2vy4xkz6 authors: klaumann, francini; correa-fiz, florencia; franzo, giovanni; sibila, marina; núñez, josé i.; segalés, joaquim title: current knowledge on porcine circovirus 3 (pcv-3): a novel virus with a yet unknown impact on the swine industry date: 2018-12-12 journal: front vet sci doi: 10.3389/fvets.2018.00315 sha: doc_id: 334588 cord_uid: 2vy4xkz6 porcine circovirus 3 (pcv-3) is a recently described virus belonging to the family circoviridae. it represents the third member of genus circovirus able to infect swine, together with pcv-1, considered non-pathogenic, and pcv-2, one of the most economically relevant viruses for the swine worldwide industry. pcv-3 was originally found by metagenomics analyses in 2015 in tissues of pigs suffering from porcine dermatitis and nephropathy syndrome, reproductive failure, myocarditis and multisystemic inflammation. the lack of other common pathogens as potential infectious agents of these conditions prompted the suspicion that pcv-3 might etiologically be involved in disease occurrence. subsequently, viral genome was detected in apparently healthy pigs, and retrospective studies indicated that pcv-3 was already present in pigs by early 1990s. in fact, current evidence suggests that pcv-3 is a rather widespread virus worldwide. recently, the virus dna has also been found in wild boar, expanding the scope of infection susceptibility among the suidae family; also, the potential reservoir role of this species for the domestic pig has been proposed. phylogenetic studies with available pcv-3 partial and complete sequences from around the world have revealed high nucleotide identity (>96%), although two main groups and several subclusters have been described as well. moreover, it has been proposed the existence of a most common ancestor dated around 50 years ago. taking into account the economic importance and the well-known effects of pcv-2 on the swine industry, a new member of the same family like pcv-3 should not be neglected. studies on epidemiology, pathogenesis, immunity and diagnosis are guaranteed in the next few years. therefore, the present review will update the current knowledge and future trends of research on pcv-3. the evolution of emerging diseases is associated with factors embedded in the concept "host-agent-environment triangle" (1) . to infect the host and cause disease, the pathogen needs to evade host defenses, which may occur through single point mutations, genome rearrangements, recombination and/or translocation (2) . genetic uniformity generated through genetic selection of the host (3) and the fact that demographic changes, intensification of farming, and international commerce have occurred markedly over the last decades, must be also considered as essential factors for the development of emerging diseases (4) (5) (6) . as well as in humans, emerging diseases drastically affect animal populations, especially food-producing animals. livestock production in large communities (i.e., pig farms or poultry flocks) represents an excellent environment to facilitate the transmission and maintenance of huge viral populations, contributing to the pathogen evolution (through mutation, recombination and reassortment, followed by natural selection) (7) (8) (9) . the intensification of livestock during the last four decades has probably been one of the main factors that contributed to the emergence of new pathogens and/or pathogen variants, leading to changes in the epidemiology and presentation of diseases (10) . the number of viral infectious diseases in swine has significantly increased in the last 30 years. several important worldwide distributed viruses have been reported in this period, including porcine reproductive and respiratory syndrome virus (prrsv, family arteriviridae), porcine circovirus 2 (pcv-2, family circoviridae) and porcine epidemic diarrhea virus (pedv, family coronaviridae). in addition to those worldwide widespread viruses, an important number of novel swine pathogens causing different types of diseases has been described (11, 12) . although their economic impact might be variable, they are considered significant infection agents and their monitoring is nowadays performed in some parts of the world. among others, relevant examples are porcine deltacoronavirus (associated with diarrhea) (12) , senecavirus a (causing a vesicular disease and increased preweaning mortality) (11) , porcine sapelovirus (found in cases of polioencephalomyelitis) (13) , porcine orthoreovirus (assumed to cause diarrhea) (14) , atypical porcine pestivirus (cause of congenital tremors type ii) (15) and hku2-related coronavirus of bat origin (associated with a fatal swine acute diarrhea syndrome) (16) . besides overt emerging diseases of swine, many other novel infectious agents have been detected in both healthy and diseased animals, and their importance is under discussion. this group of agents is mainly represented by torque teno sus viruses, porcine bocavirus, porcine torovirus and porcine kobuvirus, which are thought to cause subclinical infections with no defined impact on production (13, 17, 18) . an exception may be represented by hepatitis e virus (hev); although it seems fairly innocuous for pigs, it is considered an important zoonotic agent (19, 20) . recently, a novel member of the circoviridae family named porcine circovirus 3 (pcv-3), with unknown effects on pigs, has been discovered (21, 22) . porcine circovirus 3 (pcv-3) was first described in 2015 in north carolina (usa) in a farm that experienced increased mortality and a decrease in the conception rate (21) . sows presented clinical signs compatible with porcine dermatitis and nephropathy syndrome (pdns) and reproductive failure. in order to identify the etiological pathogen, aborted fetuses and organs from the affected sows were collected for further analyses. whilst histological results were consistent with pcv-2-systemic disease, both immunohistochemistry (ihc) and quantitative pcr (qpcr) methods to detect pcv-2 yielded negative results. samples were also negative for prrsv and influenza a virus. homogenized tissues from sows with pdnslike lesions and three fetuses were tested through metagenomic analysis, revealing the presence of an uncharacterized virus (21) . further analyses using rolling circle amplification (rca) followed by sanger sequencing showed a circular genome of 2,000 nucleotides. palinski et al. (21) also performed a brief retrospective study through qpcr on serum samples from animals clinically affected by pdns-like lesions (but negative for pcv-2 by ihc) and pigs with porcine respiratory diseases. results revealed pcv-3 qpcr positivity in 93.75 and 12.5% of the analyzed samples, respectively (21) . interestingly, almost concomitantly, another research group from the usa reported a clinical picture pathologically characterized by multi-systemic and cardiac inflammation of unknown etiology in three pigs of different ages ranging between 3 and 9 week-old (22) . several tissues from these animals were tested by next-generation sequencing (ngs) methods and pcv-3 genome was found. beyond ngs, in situ hybridization was performed in one out of these three pigs, confirming pcv-3 mrna in the myocardium (cytoplasm of myocardiocytes and inflammatory cells mainly, although to a very low frequency). based on these two initial works, the name pcv-3 was proposed as the third species of circoviruses affecting pigs, since pairwise analysis demonstrated significant divergence with the existing pcvs. the novel sequences showed <70% of identity in the predicted whole genome and capsid protein amino acid (aa) sequence compared to the other members of the circovirus genus (22) . taking into account the economic importance and the well-known effects of pcv-2 on the swine industry, a new member of the same family like pcv-3 should not be neglected. studies on epidemiology, pathogenesis, immunity and diagnosis are guaranteed in the next few years, but the scientific community is still in its very beginning on the knowledge of this new infectious agent. therefore, the objective of the present review is to update the current knowledge and forecast future trends on pcv-3. porcine circovirus 3 (pcv-3) belongs to the family circoviridae, genus circovirus. until 2016, the circoviridae family was divided into two different genera named circovirus and gyrovirus (23); however, on the basis of the viral structure and genome, a new taxonomical grouping has been recently established by the international committee on taxonomy of virus. the genus gyrovirus has been removed from the family circoviridae and reassigned into the anelloviridae family, and the new taxon cyclovirus has been included into the circoviridae family (24) . this new genus is closely related with circovirus genus members, with some differences in the genomic structure such as the orientation of the major open reading frames (orfs). moreover, viral sequences of the genus cyclovirus have been reported in both vertebrates and invertebrates, including humans and other mammals (25) (26) (27) (28) (29) , birds (30) , and insects (31) . members of the circovirus genus have been detected in vertebrates (32) ; most recently one study reported the presence of a circovirus genome in invertebrates (33) . one of the first circovirus discovered, psittacine beak and feather disease virus, was described in avian species (34) and, subsequently, several reports revealed the presence of similar virions in other species such as swine (35) , fishes (36) , bats (37) (38) (39) , chimpanzees (40) , dogs (41) humans (40) , and minks (42) . since 2016, three species of porcine circoviruses have been formally accepted, including porcine circovirus 1 (pcv-1), pcv-2 and pcv-3 (21, 22) . structurally, circoviruses are small single-stranded dna (ssdna) viruses (43) , characterized by a non-enveloped virion with icosahedral symmetry, and a circular genome with a diameter ranging from 13 to 25 nm. members of this family are constituted by 60 capsid protein subunits organized in a dodecahedral pentamer clustered unit (44) . pcv-1 has a genome size ranging from 1,758 to 1,760 nucleotides (nt) (45) (46) (47) , while the circular genomes of pcv-2 and pcv-3 consist of 1,766-1,769 and 1,999-2,001 nt, respectively (21, 46, (48) (49) (50) . porcine circoviruses contain three major orfs arranged in the strands of the replicative form (rf) (21) . for pcv-1, a total of seven putative orfs capable to encode proteins larger than 5 kda have been predicted on both dna strands (47) , being six of them larger than 200 nt (51, 52) . pcv-2 contains, besides the three major orfs, eight more predicted ones, but just orf4 has been characterized in more detail (53) (54) (55) . pcv-3 contains so far three identified orfs, but only orf1 and orf2 have been characterized. the general characteristics of the three major orfs of pcvs are summarized in table 1 . orf1 encodes for rep and rep ′ proteins involved in replication initiation, of 312 and 168 aa, respectively, in pcv-1, and of 314 and 297 aa, respectively, for pcv-2 (56). orf1 apparently codes for a single replicase protein in pcv-3, of 296-297 aa (21, 22) . orf1 is located on the positive strand and considered the most conserved region of the circovirus genome (57) . the origin of replication (ori), constituted by a conserved non-anucleotide motif [(t/n)a(g/t)tattac], is located on the same strand as orf1 and, consequently, this frame is involved in rolling circle replication (rcr) (58) . orf2 encodes the only structural protein (cap). it consists of 230-233 aa for pcv-1, 233-236 aa for pcv-2 (56, 59, 60) and 214 aa for pcv-3 (21, 22) . orf2 is located on the negative dna viral strand and cap protein is considered the most variable (46, 61, 62) , and most immunogenic (63) viral protein. nucleotide similarity of 67% in cap protein between pcv-1 and pcv-2 was detected through phylogenetic analyses (64) ; moreover, the similarity in this protein is much lower (24%) among pcv-1 and pcv-3 (22) while being 26-37% between pcv-2 and pcv-3 (21, 22) . the orf3 is oriented in the opposite direction of orf1, also in the negative strand, which codifies for a non-structural protein with apoptotic capacity (56, 65) . the orf3 protein consists of 206 aa for pcv-1, 104 aa for pcv-2 and 231 aa for pcv-3 (21, 66) . the apoptotic activity of orf3 protein has been described both in vitro and in vivo for pcv-1 and pcv-2 (67, 68), while its putative function in pcv-3 is still unknown. lastly, orf4, also located in the negative strand, has only been described in the pcv-2 genome. this gene codifies for a protein of approximately 60 aa with anti-apoptotic function (53, 54) . table 2 summarizes the nucleotide and amino acid raw distances (calculated by means of the median pairwise distances) among and within porcine circoviruses. the similarity between pcv-3 sequences ranges from 97 to 100% throughout the analyzed years and tested countries (48, (69) (70) (71) . phylogenetic analyses suggested two main groups classified as pcv-3a and pcv-3b and several sub-clusters (48, 72, 73) , based on differences found between both groups in the aa sites 122 and 320 (s122a and a320v). in fact, certain antigenicity differences among groups have been proposed (74) , although it is still too early to discuss about potential different genotypes or subgroups for pcv-3. additionally, the progressive increase in sequence availability is revealing the presence of other branching patterns, which hardly fit with the "two genotype" classification. therefore, similarly to pcv-2, a higher heterogeneity might be found in the future. a phylogenetic tree including full-length sequences of pcv-3 is depicted in figure 1 . after the first description reported from the usa, several countries located in asia, europe and south america (figure 2 ) have demonstrated the presence of pcv-3 genome in domestic pig (70, 73, (75) (76) (77) (78) (79) (80) . pcv-3 genome has been detected at all tested ages, including sows, mummified fetuses and stillborn (21, 79, 81) . the frequency of viral detection found by pcr in pigs is variable according to the collected samples around the world ( table 3) . a lower frequency of pcv-3 pcr positivity has been detected in lactating pigs when compared with nursery and fattening ones; the highest prevalence was found in animals after weaning (48, 77, 82) . however, these studies included different pigs from fairly limited age-groups and not the same animals over time. in a very recent work performed on longitudinally sampled pigs in spain (83), pcv-3 dna was found at all age-groups in four tested farms, and the frequency of infection was not clearly dominant at any age. also, pcv-3 has been detected at moderate to high rate in sera pools from sows in poland (77) and thailand (84) . pcv-3 genome has been detected by pcr in oral fluids and nasal swabs (76, 82) as well as in feces (85, 95) , semen (70) , and colostrum (84) . kedkovid et al. (84) found a positive correlation between detection in serum samples and in colostrum, suggesting that the colostrum is influenced by the viremic stage of the sow. no specific studies have been performed on the virus detection in the environment, but one study indicates that the virus was found in 2 out of 4 sponges used for sampling pig transporting trucks after sanitation (89) . besides domestic pigs, pcv-3 infects wild boar. viral dna sequences retrieved from wild boar showed more than 98% similarity with the available sequences from domestic pigs (95, 96) . the prevalence found in tested serum samples was similar or higher than that found in domestic pigs, ranging from 33 to 42.66%. additionally, infection susceptibility was associated with the age in both studies; juvenile animals were statistically less often pcv-3 pcr positive than the older ones. in fact, a potential reservoir role of the wild boar with respect to pcv-3 infection has been suggested (95, 96) . pcv-3 seems to be restricted to suidae species. however, pcv-3 genome has been found in 4 out of 44 (9.09%) serum samples of dogs from china. the authors suggested that the virus might infect, therefore, non-porcine species (97) . to date, there is no further evidence regarding susceptibility to pcv-3 infection in other species. pcv-3 has been detected in pigs with different clinical/ pathological conditions, such as respiratory, reproductive, gastrointestinal and neurological disorders; however, the virus has been also detected in apparently healthy animals (21, 71, 98) . the conditions in which pcv-3 has been found are summarized in table 4 . noteworthy, in most of these scenarios there are not complete diagnostic studies, but only the detection of the viral genome in a number of pigs affected by different clinical signs. even though the viral genome was detected, it is worthy to state that it does not imply a causative role of pcv-3 in the observed condition. thus, this section compiles the peer-reviewed papers, reporting pcv-3 dna detection in different disease scenarios. the amount of viral dna in serum samples (10 2 -10 7 copies/ml) (21) and tissues (10 4 -10 11 copies/mg) (86, 91) in postweaning pigs and adults was rather variable, as well as in stillborn or fetal tissues (10 6 -10 9 copies/mg) (21, 75) . in most of these cases, the number of pcv-3 genome copies should be considered moderate to low (21, 91) . in addition, detection was possible in some instances, but the viral load was below the limit of quantification of the qpcr, which may emphasize the subclinical nature of the infection in these cases (48, 81) . an association between high viral load and severity has been demonstrated for other porcine circovirus (pcv-2), especifically under pcv-2-sd (102) and pcv-2-reproductive disease (103) scenarios. however, the meaning of a given genome viral load for pcv-3 in healthy or diseased pigs is still to be elucidated. pcv-3 genome was initially retrieved from sows with clinical signs compatible with pdns in usa. in the affected farm, a decrease of 0.6% in the conception rate was found while the sow mortality showed a 10.2% increase (21) . in china, pcv-3 was found in serum samples from sows with reproductive problems characterized by acute loss of neonatal piglets (70) . moreover, a comparative study between healthy sows and sows with a clinical picture characterized by chronic reproductive failure (including increase in abortion and sow mortality rates) revealed that pcv-3 positivity was higher in affected sows (39 out of 84, 46.42%) than in healthy ones (23 out of 105, 21.9%) (69) . viral genome has also been found in tissues from stillborn in farms experiencing reproductive failure in china (69) (70) (71) and korea (94) . pcv-3 dna was also detected in pigs with respiratory disorders, as already indicated in the first report of this virus (21) . two more studies reported pcv-3 genome in animals from china with abdominal breathing and lesions including lung swelling and congestion (87, 99) . more recently, the viral genome has been detected in fattening pigs from thailand suffering from porcine respiratory disease complex (prdc), characterized by coughing, dyspnea, fever and anorexia; the prevalence was higher in diseased animals (60%; 15 out of 25) than in healthy ones (28%; 7 out of 25) (91). multisystemic inflammation and myocarditis were initially linked with the presence of pcv-3 (22). one single study described pcv-3 in weaned pigs that suffered from gastrointestinal disorders (diarrhea), showing higher prevalence in pigs with clinical signs (17.14%, 6 out of 35) compared to those with non-diarrhea signs (2.86%; 1 out of 35) (87). in another report, animals with congenital tremors were analyzed and pcv-3 was the only pathogen found in the brain, with high amount of viral dna (101). a number of studies found pcv-3 in apparently healthy animals (69, 76, 81, 87, 93), which makes much more complicated the overall interpretation of this virus as potential causative agent of disease. whilst the initially pcv-3 pcr positive cases were negative for three of the most important swine infectious agents (pcv-2, prrsv, and porcine parvovirus, ppv) (21, 22, 87) , subsequent studies revealed frequent co-infection with other viruses. all pathogens found in co-infections with pcv-3 are summarized in table 5 . it is still too early to establish the overall picture of pcv-3 infection, since it is a widespread virus in healthy animals. therefore, the likelihood of disease may not depend on its presence only, but other factors may serve as illness triggering factors or up-regulate its replication under disease scenarios. the detection of the virus is currently based on molecular techniques such as conventional pcr and qpcr and its characterization by sanger sequencing or ngs. in fact, the first pcv-3 complete genome was identified by ngs, and subsequently sanger sequencing has been systematically applied to obtain novel pcv-3 sequences. several primer na, not available in the published study; * , pcv-3 positivity in lower frequency than diseased animals. pairs and probes have been designed for these molecular techniques (21, 89, 101) . moreover, a duplex qpcr for the simultaneous detection of pcv-2 and pcv-3 has been also attempted (105) . in situ hybridization, a technique used to detect viral genome on histological tissue sections, has been performed in two studies (22, 91) . however, the technique is not yet completely standardized, since it is still used in minimal number of laboratories worldwide and a thorough description of the infected cell types is still missing. a minimum number of studies showed the development and validation of serological tests. two reports have published limited information about indirect enzyme-linked immunosorbent (elisa) tests using recombinant pcv-3 cap protein (21, 106) . more recently, a pcv-3 specific monoclonal antibody has been produced, presumably working on formalin-fixed, paraffin-embedded tissues by means of immunohistochemistry (72) . infection of cell cultures with pcv-3 tissue homogenates has been attempted in pk-15 (21, 75) and swine testicle cells (st) (21) without success. the cells were observed for cytopathic effects and monitored by qpcr for viral growth. however, the ct-values did not increase at each cellular passage and no cytopathic effect was observed (21, 75) . therefore, there is not any pcv-3 isolate so far available. definitely, in order to elucidate the pcv-3 pathogenesis, further establishment of laboratory techniques such as viral isolation, serology, and detection of viral components in tissues is needed. in consequence, the potential association of pcv-3 with any clinical condition, if any, is difficult to be demonstrated due to existing technical limitations. porcine circoviruses (pcvs) are ssdna ubiquitous viruses, widespread worldwide in the domestic pig population (107) . two species were known to infect suidae species before 2015: pcv-1, considered non-pathogenic, and pcv-2, the cause of one of the most devastating porcine diseases, pcv-2-sd. pcv-3 represents an expansion of the swine virosphere within the circoviridae family, but the up-to-date knowledge is still very limited and there is not yet any clue on its potential pathogenesis or disease causation role. it is at least curious that 20 years ago there were serious doubts about pcv-2 as a cause of an overt disease characterized by severe lesions and high mortality (108), while nowadays pcv-3 has been found within a number of clinical conditions and putative association has been established from the very beginning (21, 22) . current literature has already reported the presence of pcv-3 in animals affected by different clinical pictures, although just few of them included healthy control groups (71, 76, 87, 91) . in all studies, the frequency of pcv-3 detection in diseased animals was higher; although these results did not prove any disease causality, at least open the avenue to definitively ascertain its role in clinical/pathological manifestations. further studies on potential disease association of pcv-3 are needed. no data is available regarding the pathogenesis of pcv-3 infection. the lack of virus isolation has impeded the establishment of an infection model to date. it is known that pcv-3 can be found in different tissues of domestic pig and wild boar (86, 87, 95) , indicating the systemic nature of the infection. however, the point of viral entry, primary replication, organic distribution and persistence are still unsolved issues. pcv-3 has been found in feces, nasal swabs, oral fluids, and trucks transporting pigs (82, 85, 95) , which allows speculating that horizontal transmission through direct contact is probably an important route. detection of viral genome in fetuses and stillborn from farms with history of reproductive failure (21, 70, 75) , as well as in semen and colostrum, points out also to vertical transmission as another likely route. definitively, more studies are needed to ascertain the potential excretion routes of this virus. co-infection of pcv-3 with both pcv-2 and prrsv has been reported (70, 78, 91, 92, 94) . in fact, this was expected since both well-known pathogens are widespread in the pig population (109) (110) (111) . noteworthy, it is known that both pcv-2 and prrsv are able to affect the immune system and, therefore, co-infections with these viruses are not unusual (112, 113) . other pathogens were also detected in pcv-3 pcr positive samples (78, 114) . very recently, pcv-3 has been found by ngs approach in pigs affected by periweaning failure-to-thrive syndrome in co-infection with ppv and ungulate bocaparvovirus 2 (100). since experimental and field studies demonstrated that co-infection with ppv increase the effect of pcv-2 in causing pcv-2-sd (115) , at this point it cannot be ruled out that a similar effect may occur with pcv-3. further investigations are needed to determine whether pcv-3 might act as a secondary agent upregulating its replication once pigs are immunosuppressed or immunomodulated, or whether the frequency of co-infection is independent of the immune system affection. although pcv-3 genome has been detected at higher prevalence in weaned pigs (48, 77, 82) , only one study has monitored pcv-3 infection longitudinally (83) . in this study, pcv-3 was found in pigs at all ages with a similar frequency. this infection dynamics contrasts with that of pcv-2, which infects pigs mainly between five and 12 weeks of age, and rarely in animals at the lactation phase (116) (117) (118) . this is explained by the fact that colostrum antibodies are protective against infection and then decline during the lactation and weaning phases. once maternally derived antibodies waned, an infection is followed by active seroconversion (117) (118) (119) . this seroconversion usually occurs between 9 and 15 weeks of age and the antibodies may last until 28 weeks of age at least (117, (120) (121) (122) . regrettably, information about infection in sows, maternally derived immunity and how protective the immunity might be against pcv-3 is completely lacking at this moment. it is known that pcv-3 can be found in colostrum (84) , implying the possibility of vertical transmission (sow to piglet) and emphasizing the potential importance of early infections. again, available information regarding these issues on pcv-3 is still to be generated. one study performed in samples from captured and re-captured wild boar revealed long-lasting infection (potential persistent infection), since the virus was detected during a period of at least 5-7 months in few animals (95) . susceptibility of wild boar to pcv-3 was not a surprise, since this species shows susceptibility to several pathogens that affect humans and animals (123), including pcv-2; moreover, the wild boar can also develop pcv-2-sd (124) . taking into account the potential long period of infection observed in some animals and even a higher overall prevalence in wild boar when compared with domestic pigs, such potential reservoir role deserves further investigations (95, 96) . infection of pcv-3 in other non-suidae species is, at this point, still to be demonstrated. although pcv-3 dna has been found in sera from dogs in china (97) , the lack of other detection techniques able to confirm a true infection with this virus prevents the assumption of multiple species susceptibility. another interesting aspect yet currently unknown is the potential impact of pcv-3 on public health. dna from pcv-1 and pcv-2 has been found in vaccines intended for use in humans (125) , probably associated to the use of reagents from swine origin in the vaccine manufacturing. at this point, no information regarding pcv-3 and its role as a contaminant of human medicines do exist. on the other hand, porcine circoviruses belong to a group of microorganisms that still has not been fully addressed in terms of risk evaluation for xenotransplantation (126) , so, pcv-3 should be also a priori added to such list. palinski et al. (21) conducted a brief study in paraffin fixed tissues from 2010 to 2016 in north america and results showed a high percentage of pcr positivity in these samples, suggesting that the virus emerged before the year of its discovery. in fact, pcv-3 has been already demonstrated retrospectively in sweden in 1993 (93) and spain (81) and china in 1996 (78) , indicating that this is not a new virus and it has been circulating during several decades in domestic pigs. moreover, pcv-3 has been detected in the oldest samples so far tested in these studies, suggesting that this virus could have been infecting pigs for even a longer period. however, these findings cannot be assumed as a proof of non-pathogenicity, especially when mirroring another closely-related circovirus, pcv-2. although this latter virus was initially detected in association with disease by midlate 1990s, retrospective studies showed evidence of pig infection a number of decades before (120, (127) (128) (129) . in fact, in most of these investigations, evidence of pcv-2 infection coincided with the very first investigated year, suggesting again that pcv-2 might be even an older circulating virus. in addition, a retrospective study on pcv-3 conducted in samples of wild boar from spain during a 14-year period (95) detected the virus in the first tested year (2004). overall, obtained data confirmed that pcv-3 is not a new virus and has been circulating for a fairly, non-determined long time in swine and wild boar populations. in fact, the most common ancestor of pcv-3 was estimated to be originated approximately in 1966 (73, 130) . genetic characterization of pcv-3 is mainly done through sanger sequencing. phylogenetic analyses of pcv-3 genomes available from the genbank indicate they are part of different clusters. however, nucleotide identity among these sequences is really high (>97%). in consequence, it seems that pcv-3 has remained fairly stable over the years without an independent molecular evolution according to specific areas of the world. moreover, these findings do not point out a high mutation rate as has been suggested (48, 131) . if such mutation rate were high, it would have generated a higher genomic heterogeneity, which should have been detected at least in the performed retrospective studies accounting for more than 20 years. further studies on the evolution on pcv-3 are crucial to solve out these controversies. the first metagenomics sequence available from pcv-3 revealed low identity with cap and rep genes of pcv-1 and pcv-2 and a closer identity with other circoviruses such as canine circovirus (21, 22) and barbel circovirus (71) . the circovirus genus members are able to infect a wide range of hosts, and cross-species transmission has also been reported (40) . franzo and collaborators (132) hypothesized the possibility of pcv-3 being the product of recombination related with a host jump. the analysis of genome composition of pcv-3 found the rep gene closely related with that of bat circoviruses and cap gene with that of avian ones (132) . recently, novel circoviruses isolated in civets, showing higher similarity in terms of aa sequence in rep protein with pcv-3, have been described (133) . the increasing new data should be useful to clarify the relationships and origin of this virus. on the other hand fux et al. (48) found nucleotide changes, which resulted in two aa alterations in orf1/orf2 and orf3 (a24v and r27k), between the two proposed genotypes (pcv-3a and pcv3b). li et al. (131) also suggested two groups with two individual subclades termed pcv-3a-1 and pcv-3a-2. the aa site 24 from orf2, predicted to be under positive selection, was suggested to be located in a potential epitope region. the presence of possible genotypes was also suggested in other studies (73, 76) . however, considering the high similarity found in partial or complete pcv-3 sequences (>98% in most of the cases), the importance of determining genotypes or groupings at this stage seems poorly relevant. due to the sensitivity limitations of sanger sequencing, it must be emphasized the need to apply ngs technology to discover minor variants, which might unravel the presence of quasispecies undetected by the currently used technology. porcine circovirus 3 is a recently discovered virus widespread in both domestic pigs and wild boar population. the virus can be found at all tested ages and few animals may display a persistent infection. although the virus has been found in several clinical and pathological conditions, a definitive proof of its pathogenicity is still lacking. phylogenetic information available to date indicates a low genetic variability of pcv-3 in comparison with other single stranded-dna viruses and indicates that the virus genome has been relatively stable across the years. fk and js did the majority of the writing and communicated with the coauthors to coordinate the document editing. js designed the outline of the manuscript. gf provided the phylogenetic analyses. fc-f, gf, ms, and jn revised the manuscript, did partial writing and approved the final version for publication. we would like to acknowledge the funding of the e-rta2017-00007-00-00 project, from the instituto nacional de investigación y tecnologia agraria y alimentaria (spanish government). the funding from cerca programme/generalitat de catalunya to irta is also acknowledged. one world, one health: the threat of emerging swine diseases. a north american perspective natural genome-editing 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(paguma larvata) key: cord-355239-fc52dn3v authors: kato, kentaro; ishiwa, akiko title: the role of carbohydrates in infection strategies of enteric pathogens date: 2014-11-15 journal: trop med health doi: 10.2149/tmh.2014-25 sha: doc_id: 355239 cord_uid: fc52dn3v enteric pathogens cause considerable public health concerns worldwide including tropical regions. here, we review the roles of carbohydrates in the infection strategies of various enteric pathogens including viruses, bacteria and protozoa, which infect the epithelial lining of the human and animal intestine. at host cell entry, enteric viruses, including norovirus, recognize mainly histo-blood group antigens. at the initial step of bacterial infections, carbohydrates also function as receptors for attachment. here, we describe the function of carbohydrates in infection by salmonella enterica and several bacterial species that produce a variety of fimbrial adhesions. during invasion by enteropathogenic protozoa, apicomplexan parasites utilize sialic acids or sulfated glycans. carbohydrates serve as receptors for infection by these microbes; however, their usage of carbohydrates varies depending on the microbe. on the surface of the mucosal tissues of the gastrointestinal tract, various carbohydrate moieties are present and play a crucial role in infection, representing the site of infection or route of access for most microbes. during the infection and/or invasion process of the microbes, carbohydrates function as receptors for various microbes, but they can also function as a barrier to infection. one approach to develop effective prophylactic and therapeutic antimicrobial agents is to modify the drug structure. another approach is to modify the mode of inhibition of infection depending on the individual pathogen by using and mimicking the interactions with carbohydrates. in addition, similarities in mode of infection may also be utilized. our findings will be useful in the development of new drugs for the treatment of enteric pathogens. enteric pathogens, many of which are zoonotic, exert a major impact on public health worldwide including tropical regions. in humans and animals, the enteric pathogens, which include viruses, bacteria and protozoa, infect the intestine epithelial lining, resulting in food poisoning or diarrheal disease. when enteric pathogens enter humans or animals via the oral route, they must withstand the proteolytic conditions in the stomach before penetrating the mucus layer and accessing the underlying gut epithelium for attachment or cell invasion. adhesion of the enteric pathogens to the intestine epithelial tissue is a prerequisite for the initiation of infection. in many systems it is mediated by lectins present on the surface of the pathogen that bind to complementary carbohydrates on the surface of the host cells. carbohydrates such as heparan sulfate have been reported to play a crucial role in the entry or budding of viruses [1] , and bacterial lectins typically act in the form of elongated submicroscopic multisubunit protein appendages, known as pili [2] . recently, the surface proteins of apicomplexan parasites have also been reported to bind to carbohydrates on host cells [3] . thus the initial steps of host cell recognition by enteric pathogens may incorporate common strategies. once pathogens invade the host cells, they initiate their survival mechanisms to avoid extermination by host immunity. ultimately, if infection of host cells could be inhibited, proliferation of the pathogens could be prevented and pathogenesis could be controlled. insights obtained from studies designed to address this concept will be invaluable to develop novel therapies using innovative drug design and engineered vaccine candidates to limit the infectivity of widespread enteric pathogens. here, we review the recent major advances in research on the role of carbohydrates in the infection strategies of enteric pathogenic viruses, bacteria and protozoa. we further discuss how our knowledge regarding these carbohydrates may influence prophylactic and therapeutic drug development for the treatment of diseases caused by enteric pathogens. carbohydrates function as receptors for virus entry. negatively charged carbohydrates, which are expressed on many types of cells and tissues such as sialic acid and heparan sulfate, are common viral receptors. orthomyxovirus, polyomavirus, reovirus, coronavirus, paramyxovirus and parvovirus recognize sialic acid as a receptor. adenoassociated virus, herpesvirus and flavivirus recognize heparan sulfate. on the other hand, the enteric virus norovirus recognizes histo-blood group antigens (hbgas), which are not charged. here, we focus on the association of carbohydrates with norovirus as the virus enters the host cell. norovirus, a member of the family caliciviridae, is a major cause of acute water-and food-borne gastroenteritis [4] . norovirus infection is associated with up to 90% of epidemic nonbacterial acute gastroenteritis cases worldwide [5] . noroviruses are divided into at least five genotypes, three of which (genogroups i, ii, and iv) infect humans. except for a few genotypes, all noroviruses bind to hbgas including abh antigens and lewis antigens [5, 6] . in hbgas, carbohydrate core structures constitute antigenically distinct phenotypes, namely type 1 (galβ1-3glcnacβ) and type 2 (galβ1-4glcnacβ). h antigen (fuc-α1-2gal), i.e., o-type antigen, is generated by fucose transfer to a galactose residue with an α1-2 linkage of type 1 or type 2. the a antigen (galnac α1-3(fuc-α1-2)gal) and b antigen (gal α1-3(fuc-α1-2)gal) of hbgas are generated by transfer of galnac and gal, respectively, to an h structure irrespective of the carbohydrate core structure. fut1 and fut2 are α1,2futs that catalyze the transfer of fuc to the gal residue of type 1 and 2 chains, thereby resulting in the synthesis of h type 1 and h type 2, respectively. hbgas are found in saliva and mucosal secretions from the intestinal epithelial cells of secretors (i.e., individuals who have the fut2 gene that encodes a fucosyltransferase). non-secretors, who do not express fut2 fucosyltransferase and consequently do not express h type 1 or le b in the gut, are not infected after challenge with the prototype strain of norovirus, nv/68 [5, 6] . moreover, the association data between blood type and nv/68 infection showed that, among secretor volunteers, blood groups o and a were associated with an increased risk of infection, while blood group b was associated with a decreased risk. on the other hand, epidemiological studies have shown that some norovirus strains with abh phenotypes that differ from that of nv/68 can infect individuals. gii/4, which is known as a global epidemic strain, binds more hbgas than other strains, suggesting that the strength of transmission of gii/4 strains is related to the broad recognition of hbgas [6] . the recognition sites on hbgas by norovirus have been classified according to the interaction of the virus with the h, a, b, and le epitopes ( fig. 1 ) [6, 7] . hbgas are important factors for determining host specificity, although it is still unclear whether hbgas act as the primary receptor or enhance norovirus infectivity. researchers including ourselves have demonstrated that feline calicivirus (fcv), a member of the genus vesivirus, infects the upper respiratory tract by attaching to α2-6linked sialic acids and using junctional adhesion molecule-1 for internalization [8, 9] . it is comparatively easy to study the life cycle of fcv because the virus replicates efficiently in cell culture without specific supplementation, whereas noroviruses are not cultivable in cell culture. carbohydrates also function as receptors for bacterial attachment at the initial step of infection. here, we describe the role of carbohydrates in bacterial infections, focusing on salmonella enterica and several assortative bacterial species that produce a variety of fimbrial adhesions (fig. 2) . salmonella strains cause disease in diverse mammalian hosts. some salmonella strains have a narrow host range, such as salmonella enterica serovar typhi (s. typhi) and serovar paratyphi (s. paratyphi), which cause disease only in humans, whereas strains such as salmonella enterica serovar typhimurium (s. typhimurium) and serovar enteritidis (s. entertitidis) cause infection in numerous species including mice, poultry, pigs, sheep, cattle, horses and humans [2] . infected orally, salmonella reach the intestinal tract and then mainly attach to the m cells of the intestinal epithelium to initiate invasion [10] . after colonization of the intestinal epithelium, typhoid salmonella, s. typhi and s. paratyphi, invade m cells. however, s. typhi and s. paratyphi can also survive being engulfed by macrophages, which then spread throughout the body via the lymphatic and blood systems. non-typhoidal salmonella, s. typhimurium and s. enteritidis cannot survive within macrophages (fig. 3) . they cause gastroenteritis in humans and animals by colonizing the intestinal epithelium and then invading and destroying the m cells and enterocytes [2] . bacterial adherence requires both specific and nonspecific interactions. in the case of salmonella, the negative charge produced by sialic acid on the surface of the host cell is required as a non-specific adherence factor [11] . for their specific interactions, salmonella and assor-tative bacteria possess various adhesion molecules such as a variety of bacterial fimbriae. at the initial infection step, bacterial attachment is mainly controlled by these bacterial fimbriae. individual fimbria recognize and bind to specific receptors to promote adhesion to the host cell surface [2, 12] . long polar fimbriae (lpf) and plasmid-code fimbriae (pef) are categorized as type 4 fimbriae (fig. 2) . std fimbriae are categorized as π-fimbriae [2, [13] [14] [15] . a previous report showed that when one of the fimbriae carried by salmonella typhimurium was deleted, only virulence for mouse was moderately altered, and that multiple fimbrial adhesins were required for full virulence [16] . for salmonella and assortative bacteria, type 1 fimbria is the std fimbriae are categorized as π-fimbriae. bacterial flagella are the moving apparatus of bacteria, but their components can also contribute to the binding to sugar-containing molecules. k. kato et al. 43 best characterized [17] . type 1 fimbriae consist of a major component (fima) and a minor component (fimh) (fig. 2) . fimh lies at the tip of type 1 fimbriae, where it mediates binding to d-mannose-containing structures and enables the bacteria to colonize various host tissues [18] . type 1 fimbriae are also produced by other gram-negative bacteria, such as escherichia coli and klebsiella pneumoniae [19] . the fimh protein of enterobacterial species including salmonella recognizes mannose-containing oligosaccharides [18] . in the case of e. coli, previous reports have shown that fimh protein has a considerably high affinity for oligosaccharides containing manα1-3, such as manα1-3manβ1-4glcnac and manα1-6(manα1-3)manα1-6(manα1-4)man, which are constituents of cell surface glycoproteins [19] . the process of bacterial adhesion to the epithelial cell surface mediated by type 1 fimbriae (fimh) is conservative among enterobacteria. type 1 fimbriae are highly expressed on the bacterial surface, allowing large quantities of bacteria to adhere via the fimh-mannose interaction (fig. 3 ). type 4 fimbriae are thin and flexible, and generally expressed at a lower level than type 1 fimbriae. some type 4 fimbriae are only present at low levels on the surface of bacteria, and are localized at the bacterial pole. although their expression level is low, type 4 fimbriae frequently play an important role in bacterial infection. like type 1 fimbriae, type 4 fimbriae are thought to recognize carbohydrates as specific receptors, but the receptor molecules and precise functions of some type 4 fimbriae have yet to be determined. for example, the function of the type 4 fimbria bundle-forming pili (bfp), an important virulence factor for pathogenic e. coli strains, is not yet known (fig. 2) . bfp may not be involved in initial adhesion; rather, it may participate in the formation of the bacterial colony by forming bundles that link one bacterium to another [20] . although the function of and receptors for type 4 fimbriae remain unclear, bacterial virulence has been shown to decrease when type 4 fimbriae are deleted [16] . lpf medisalmonella and assortative bacteria express a variety of fimbriae. the minor component of type 1 fimbriae, fimh, is present at the tip of type 1 fimbriae, mediates binding to d-mannose-containing structures and enables bacteria to colonize various host tissues [18] . type 1 fimbria is highly expressed on the bacterial surface, allowing large amounts of bacteria to adhere via the fimh-mannose interaction. the various kinds of type 4 fimbriae play an important role in bacterial infection. plasmid-encoded fimbria (pef) is required for bacterial attachment to intestinal epithelial cells. pef specifically binds to trisaccharide galβ1-4(fucα1-3)glcnac, also known as the lewis x (le x ) blood group antigen [13] . long polar fimbria (lpf) mediates the adhesion of s. typhimurium to murine peyer's patches [21] . extracellular matrix proteins (ecms) may act as receptors for lpf. ecms are modified with various carbohydrate moieties, and the presence of mannose inhibits the lpf-ecm interaction. mannose-containing carbohydrates may participate in bacterial adhesion via lpf [23] . std fimbriae are categorized as π-fimbriae and are well conserved among s. enterica serotypes but absent from other related bacterial species. std fimbriae recognize and bind the h type 2 histo-blood group oligosaccharide, the terminal fucα1-2galβ1 moiety. s. typhi and s. paratifi can survive within the macrophages after they are engulfed by phagocytosis. non-typhoidal salmonella, s. typhimurium and s. enteritidis, however, are unable to survive within macrophages. ates the adhesion of s. typhimurium to murine peyer's patches [21] . lpf was first described in s. typhimurium, and is found in numerous pathogenic e. coli strains [22] . although its specific receptor remains unclear, extracellular matrix proteins (ecms), which comprise an interlocking mesh of fibrous proteins and glycosaminoglycans, may act as a receptor for lpf of enterohemorrhagic e. coli o157:h7 (fig. 3 ). ecms are modified by various carbohydrate moieties, and the addition of mannose inhibits lpf-ecm interaction. then mannose-containing carbohydrates may participate in bacterial adhesion by lpf [23] . in some cases, type 4 fimbriae are encoded on plasmids. such plasmids frequently encode virulence factors for host bacteria, and are therefore called "virulence plasmids" [24] . pef is required for bacterial attachment to intestinal epithelial cells. it specifically binds to trisaccharide galβ1-4(fucα1-3)glcnac, also known as the lewis x (le x ) blood group antigen (fig. 3 ) [13] . the le x antigen is defined by the presence of a terminal galβ1-4(fucα-3)glcnac moiety on saccharide chains of glycoproteins or glycosphingolipids; in the human intestine, it is expressed mainly in crypt epithelial cells [25] . s. typhimurium possesses pef as an adhesin that binds to a crypt-specific histo-blood group antigen that may be relevant to the pathogenesis of human infections. abundant crypt abscesses are commonly found in s. typhimurium patients, raising the possibility that the pathogen may bind to human crypt epithelium at a later stage of infection. in a situation where peyer's patches are unavailable because of an inflammatory reaction, salmonella can colonize at the crypt epithelium remaining intact and persist on the surface of the host intestinal tract [13, 25] . on the other hand, some type 4 fimbriae participate in "fimbria-mediated (pilus-mediated) conjugal transfer" of so-called "conjugative plasmids". conjugative plasmids can also be virulence plasmids if they encode not only the structural genes of the fimbriae but also other virulence factors, such as a drug resistance gene. these conjugative plasmids spread to other bacteria by horizontal transfer, and type 4 fimbriae encoded on the plasmids play an important role in this event. for example, the r64 plasmid, which encodes the pilv gene and engages in the adhesion of type 4 fimbriae, recognizes the di-saccharide moiety of bacterial surface polysaccharides (the core oligosaccharide or o-antigen unit of lipopolysaccharides, a unique structure of the bacterial cell surface) and determines the recipient bacteria of the conjugal transfer [26, 27] . categorized as π-fimbriae, the std fimbriae are well conserved among s. enterica serotypes but absent from related bacterial species (fig. 2) . std fimbriae recognize and bind the h type 2 histo-blood group oligosaccharide, the terminal fucα1-2galβ1-4glcnac moiety. this structure represents the h type 2 oligosaccharide of the o blood group antigen [14] . the h type 2 oligosaccharide of the o blood group antigen moiety is expressed as part of the mucin-type sugar chains of glycoproteins in the host cell. the terminal fucα1-2 moiety of h type 2 oligosaccharide of the o blood group antigen is essential for the recognition of std fimbriae (fig. 3) . carbohydrate molecules act not only as "anchors" for pathogens but also as the determinants of host and tissue specificity. the variety of adhesion factors carried by a bacterium reflects its pathogenic profile, magnitude of virulence, host specificity, and tissue specificity. in the case of salmonella and assortative bacteria, the fimh adhesins show amino acid sequence diversity. this diversity in fimh structure results in the variation in affinity profiles. e. coli fimh shows a high affinity for aromatic αmannosides as well as manα1-3 structures. on the other hand, the fimh of salmonella species shows a high affinity for α-mannosides and a low affinity for aromatic αmannosides [19] . in the case of salmonella, allelic variation of fimh adhesion directs not only host cellspecific recognition but also distinctive binding to mammalian and avian receptors. this allele-specific binding profile parallels the host specificity of the respective fimh-expressing pathogen [28] . similarly, the lewis b (le b ) blood group phenotype in combination with secretor status may hinder colonization of helicobacter pylori in certain populations [29] . h. pylori express blood group antigen b-binding adhesion (baba), and baba binds to le b antigens. salmonella and assortative bacteria contain various adhesion factors, including several kinds of fimbriae, which contribute to bacterial virulence; however, analyses of their specific receptor moieties and functions are not yet complete [13, 15] . carbohydrate moieties on the surface of pathogens are also recognized by hosts and trigger host defense mechanisms. the bacterial surface is covered with various kinds of carbohydrates. for gram-negative bacteria, including salmonella, the major carbohydrate component of the bacterial surface is lipopolysaccharide (lps). lps is categorized as a glycolipid, and is a major component of the bacterial outer membrane. because the saccharide moieties of lps differ structurally from mammalian carbohydrates, they function as targets of the host immune response. to avoid this host immune response, the lps of some bacteria, for example c. jejuni, is structurally similar to the glycosphingolipids of gangliosides [30, 31] . similarly, the lps of most h. pylori strains expresses the le a and le b antigens [29] . interestingly, the carbohydrate on the surface of the k. kato et al. 45 host cell itself can be involved in the host defense mechanism. the salmonella flagella component flic contributes to bacterial attachment to the host cell by interacting with ganglioside molecules on the surface of the host cell, but gangliosides also act as co-receptors for salmonella enterica flic and promote flic induction of the human innate immune response [32] . gangliosides, i.e. sialic acidcontaining glycosphingolipids, are ubiquitous components of eukaryotic cell membranes that have been identified as receptors for bacterial toxins and viruses. an in vitro assay showed that a nonflagellated mutant of s. enteritidis, constructed by disrupting the flic gene, was about 50-fold less invasive than the wild-type strain, but bacterial adherence was unaffected [33] . at the attachment of salmonella enteritidis flic to the host cell surface, gangliosides thus function as receptors. on the other hand, the flagella component protein flic induces the host innate immune response by binding to toll-like receptor 5 of the host cell, and gangliosides react as co-receptors with tlr5 on the flic-induced response. an in vitro assay showed that the incorporation of exogenous ganglioside gd1a into the caco-2 cell membrane increased the effect of flic. incubation of caco-2 cells with a glucosylceramide synthase inhibitor reduced the innate immune response stimulated by flic [32] . human enteropathogenic protozoas include the apicomplexans toxoplasma gondii and cryptosporidium as well as giardia and entamoeba histolytica. they are all zoonotic pathogens that invade and colonize their target tissues in the alimentary tract of the human host. they form hard cysts that resist degradation in the stomach. host-derived proteases and low ph trigger their excystation [34] . in this section, we describe the role of carbohydrates in toxoplasma gondii invasion of intestinal epithelial cells. the ability of t. gondii to infect chinese hamster ovary (cho) cells deficient in sialic acids was reduced by 26.9% compared to wild-type cells, indicating that sialic acid is critical for attachment and invasion of t. gondii (fig. 4 ) [35] . t. gondii microneme protein 1 (tgmic1) forms a macromolecular complex with tgmic4 and tgmic6. single deletion of the tgmic1 gene significantly decreases the invasion of host cells, suggesting an essential role for tgmic1 in host cell attachment and invasion of t. gondii [36] . structural analysis of tgmic1 revealed a novel cellbinding motif called microneme adhesive repeat region (marr), which provides a specialized structure for glycan discrimination [37] . carbohydrate microarray analyses showed that tgmic13, tgmic1 and its homologue neospora caninum mic1 share a preference for α2-3-over α2-6-linked sialyl-n-acetyllactosamine sequences [38] . p104, a pan/apple domain-containing protein expressed at the apical end of the extracellular parasite, functions as a ligand in the attachment of t. gondii to chondroitin sulfate and other receptors on the host cell, facilitating invasion by the parasite (fig. 4) [39] . t. gondii display gpi-anchored surface proteins identified as surface antigen glycoprotein (sag) 1 related sequences (srs) [40] . sag1, sag2a and sag3 have some capacity for host cell attachment through glycan recognition (fig. 4) [41, 42] . sag3 binds to sulfated proteoglycans such as heparin, fucoidan, and dextran sulfate with high affinity [43] . targeted disruption of sag3 significantly reduces host cell binding of t. gondii [41] . e. histolytica fibronectin receptor (ehfnr) shows 99% homology to the intermediate subunit-2 of the gal/ galnac-specific lectin [44] . electron microscopy revealed the close association of a purified ehfnr complex to adhesion plates and phagocytic invaginations. lipid rafts participate in interactions between e. histolytica and the host extracellular matrix, and it appears that raft-associated gal/ galnac lectin serves as a collagen receptor [45] . cryptosporidium parvum surface receptors, gp900 and proteolytic fragments of the 60-kda precursor protein, gp40 and gp15, are characterized as mucin-like and heavily o-glycosylated proteins [46] [47] [48] . the gp900 and gp40 of sporozoites and merozoites have carbohydrate residues that are bound by αgalnac-specific lectins, suggesting that αgalnac residues are involved in the attachment of parasites to host cells via adherence to internal mucus. apicomplexan protozoan parasites also induce host innate immune responses via the carbohydrate molecules present on their cell surface [49] . glycosylphosphatidylinositol (gpi) protein anchors are abundant in the membranes of tachyzoites and other apicomplexan protozoan parasites including trypanosoma, leishmania and plasmodium spp., where they can serve as ligands for innate recognition [50] . the gpi moieties of t. cruzi and p. falciparum were found to be tlr2 ligands [51, 52] , and t. gondii both stimulate cytokine production in macrophages and serve as tlr2 as well as tlr4 agonists. in the case of t. gondii, gpi induces tnf-α production in macrophages through the activation of the transcription factor nf-κb [53] . carbohydrates serve as receptors for infections by viruses, bacteria and protozoa, but the usage of carbohydrates by these microbes varies depending on the microbe. at the initial infection step, these organisms do not simply utilize the electrical forces created by the positive and negative charges of the carbohydrates; rather, they make use of other systems in certain instances. one similarity shared by all three microbes regarding their interactions with carbohydrates, however, is that heparan sulfate plays an important role at entry or invasion of the host cell. blood group antigen oligosaccharides are highly expressed in the gastrointestinal epithelium [54] . however, there are individual differences in terms of the presence of these antigens. in addition, there are individual differences in sensitivity to pathogens that recognize and bind to blood group antigens, such as norovirus and h. pylori. these individual differences in antigen expression profiles benefit the survival of the host species because the risk of an attack by a fatal virulent pathogen may be decreased to avoid extinction. a large array of glycoproteins, glycolipids and proteoglycans decorate the surface of animal cells. these glycoconjugates mediate many fundamental cellular processes, including cell-cell and cell-matrix adhesion, motility, growth and signaling [55] [56] [57] . mucosal tissues represent the site of infection or route of access for most parasites, including viruses, bacteria and protozoa [58] . on the surface of the mucosal tissues of the gastrointestinal tracts, various carbohydrate moieties are present and play a crucial role in infection. mucosal surfaces are coated with a layer of viscous mucus that ranges in thickness from 300 μm in the stomach to 700 μm in the intestine [59] [60] [61] . mucin glycoproteins from mucus-producing cells in the epithelium or submucosal glands are the major macromolecular constituent of mucus and are responsible for the viscous properties of the mucus gel. in addition to forming a relatively impervious gel, which acts as a lubricant, a physical barrier and a trap for microbes, mucus provides a matrix for a rich array of antimicrobial molecules. underneath the mucus layer, the cells present a dense forest of highly diverse glycoproteins and glycolipids, which form the glycocalyx. membrane-anchored cell-surface mucin glycoproteins are a major constituent of the glycocalyx in all mucosal tissues. the oligosaccharide moieties of the molecules that form the glycocalyx and the mucus layer are highly diverse, and the average turnover time of the human jejunal glycocalyx is 6-12 h [62] . consequently, both the secreted and adherent mucosal barriers are constantly renewed and can rapidly adjust to changes in the environment, for example, in response to microbial infection. epithelial mucins are a heterogenous family of large complex glycoproteins containing a dense array of olinked carbohydrates typically comprising over 70% of their mass. the carbohydrate structures present on mucosal surfaces vary according to cell lineage, tissue location and developmental stage [58] . mucin glycosylation can alter in response to mucosal infection and inflammation, and this may be an important mechanism for unfavorable changes in the niche occupied by mucosal pathogens. the o-linked glycans of muchin proteins contain 1-20 residues, which occur both as linear and branched structures [58] . in addition to the o-linked glycans, mucins contain a smaller number of n-linked oligosaccharides, which have been implicated in folding, oligomerization (muc2) and surface localization (muc17) [63] [64] [65] . the terminal structures of mucin oligosaccharides are highly heterogeneous k. kato et al. and vary between and within species as well as between and even within tissues. the array of oligosaccharide structures on individual mucin molecules is also somewhat determined by stochastic events as the mucin protein moves through the golgi apparatus [66] . the secreted mucins themselves likely function as decoys for adhesins that have been evolved by pathogens to engage the cell surface, as the mucins express many of the oligosaccharide structures found on the cell surface and are constitutively produced in large amounts, constantly washing the mucosal surfaces [58] . proteoglycans are present on the cell surface [67] and are also components of glycocalyx. glycosaminoglycan chains are composed of highly sulfated saccharides that give the cell surface a potent negative charge. one of the prototypical membrane proteoglycans is syndecan-1, which carries conserved attachment sites for glycosaminoglycan chains [67] . the syndecans exemplify hybrid proteoglycans because they contain mixtures of the two major types of glycosaminoglycan chains, heparan sulfate and chondroitin sulfate. the other major family of membrane proteoglycans is the glypicans, which contain gpi anchors in a tissue-specific and temporally regulated manner. their presence in the basolateral membranes of polarized cells varies [68] . glycolipids are also a component of the cell membrane. a large variety of glycolipids is present on the surface of animal cells. the carbohydrate moieties vary, and each glycolipid may exhibit a special function, as an annular lipid, surface receptor marker or matrix lipid. for brain and neuronal cells, gangliosides (sialic acid-bearing glycolipids) are the major cell surface determinants [69] . glycolipids function as the receptor for various biologic factors and also as the receptor for various pathogens. they are present at the undermost part of the glycocalyx. pathogens can recognize the glycolipids, directly bind to the cell membrane, and invade the host cell. glycolipids also function as receptors for certain effector molecules, such as bacterial toxins, produced by pathogens and directly react with the host cell. for example, cholera toxin binds to ganglioside gm1 [70] . thus, for pathogens living in the outer mucus layer, it is difficult to make contact with the surface of normal epithelial cells because of the huge amount of mucin that functions as a "decoy" or "physical barrier". mucosal pathogens have, therefore, developed mechanisms to subvert these defense mechanisms of the mucosal layer. on the other hand, intestinal m cells, specifically designed to capture and present microbes to the underlying lymphoid tissue, can be regarded as a "hole" in the mucin barrier. the dome epithelium lacks goblet cells and therefore does not produce gel-forming mucins. their apical cell surface has only sparse microvilli and an apparently thin glycocalyx [71, 72] . m cells are specialized epithelial antigen-transporting cells that constitute a minor proportion (5%~10% in humans and mice) of the follicle-associated epithelium that covers the lymphoid follicles of organized gut-associated lymphoid tissue such as peyer's patches [73] [74] [75] [76] . glycoprotein 2 (gp2) was identified as an m cell-specific molecule [77] . the gp2 expressed on m cells functions as a bacterial uptake receptor [77] . gp2 recognizes fimh, a major component of the type 1 fimbriae, which binds to certain glycoproteins on mammalian cells in a mannosedependent manner [78] . consequently, even though m cells constitute only a very small percentage of mucosal epithelial cells, they are the major point of attachment and/or entry used by numerous mucosal pathogens including bacteria (e.g., s. typhimurium, shigella flexneri, yersinia enterocolitica and vibrio cholerae), viruses (e.g., reovirus, hiv-1 and polio virus) and parasites (e.g., cryptosporidia) [72, 79, 80] . during cell-pathogen interactions (i.e., infection and/or invasion), carbohydrates function as receptors for various pathogens. on the other hand, carbohydrates (glycoconjugates) can also function as a barrier to infection. on the surface of mucosal tissue, the glycocalyx physically prevents microbes from accessing the cell membrane. some glycoconjugates, a component of the glycocalyx, contain carbohydrate structures that are recognized by pathogens. mucins often contain oligosaccharide moieties that correspond to the receptor for various pathogens. on the surface of the mucosal layer, microbes binds to these receptor moieties and are captured at the mucus layer, which consequently blocks the infection. moreover, when secretory mucins containing receptor carbohydrate structures "trap" pathogens, the pathogens are also carried away. m cells are specialized epithelial antigentransporting cells scattered in the follicle-associated epithelium that covers the gut lymphoid follicles such as peyer's patches. m cells can efficiently engulf particles as large as bacteria; however, the mucus layer of m cells and the surrounding area is relatively thin. glycoconjugates such as gp2 are expressed on the surface of m cells and function as receptors for bacterial attachment [74] . in the case of the host-parasite interaction, the various kinds of glycoconjugates sometimes function as receptors for the invading pathogens, but they can also function as barriers 48 tropical medicine and health vol. 43 no.1, 2015 and traps for the host defense system. in recent years, the damage caused by enteric pathogens, especially norovirus and salmonella, has expanded through the food chain [4, 5, 81] . these pathogens cause food poisoning in humans and gastrointestinal diseases in animals all over the world. even today, they are often responsible for large-scale outbreaks of food poisoning. therefore, the prevention and treatment of infections caused by these pathogens is essential. in this review, we discussed the interaction between host cells and microbes such as viruses, bacteria and protozoa that involve carbohydrates such as sialic acids, heparan sulfate, and the carbohydrate moieties of abh and lewis antigens, mannose components, ecms and le x . the development and use of drugs that target these carbohydrates is anticipated, even though the microbes vary widely and have different modes of infection. accordingly, when an anti-microbial drug is developed on the basis of the interaction between a microbe and a carbohydrate, host cell modification of the drug's structure and/or inhibition of the mode of infection will need to be individualized while still taking advantage of the similarities between interactions. moreover, the host gastrointestinal tract cell surface, which is the object of microbial infection, is composed of glycoproteins, glycolipids, and proteoglycans. these molecules are potential targets for carbohydrate drugs used in the treatment of infectious diseases. oseltamivir and zanamivir are neuraminidase inhibitors that competitively inhibit the activity of the viral neuraminidase on the sialic acid that is found on glycoproteins on the surface of host cells [82] . by blocking the activity of this enzyme, they prevent new viral particles being released from infected cells. there are various kinds of polysaccharides on the surface of bacteria. lipoteichoic acid (lta), a type of glycolipid, is a component of the bacterial cell wall of grampositive bacteria. studies have shown that lta stimulates the immune system [83, 84] . recently, lta has been studied for use as a novel kind of biologically active substance. recently, sulfated polysaccharides have been analyzed as drug candidates for protozoan infectious diseases [3, 85, 86] . according to our data, the sulfated positions in the carbohydrates can be critical for the inhibitory quality [3] . collectively, these studies highlight the possibility that carbohydrate drugs may be developed for the prophylaxis and treatment of parasitic infectious diseases. the results of our studies highlight the possibilities for countermeasures against malaria and toxoplasmosis [3, 85] . heparan sulfate glycosaminoglycans as primary cell surface receptors for herpes simplex virus salmonella enterica serovar 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dextran sulfates on the acute infection and growth stages of toxoplasma gondii gellan sulfate inhibits plasmodium falciparum growth and invasion of red blood cells in vitro this study was supported by grants-in-aid for young scientists, and scientific research on innovative areas (3308) from the ministry of education, culture, science, sports, and technology (mext) and for research on global health issues from the ministry of health, labour and welfare of japan, the program for promotion of basic and applied researches for innovations in bio-oriented industry (brain), the science and technology research promotion program for agriculture, forestry, fisheries and food industry, the naito foundation, and the program to disseminate tenure tracking system from the japan science and technology agency (jst). we thank mr. tatsuya iwanaga for his help with the illustrations. key: cord-265005-e6rpryrh authors: tomasello, elena; pollet, emeline; vu manh, thien-phong; uzé, gilles; dalod, marc title: harnessing mechanistic knowledge on beneficial versus deleterious ifn-i effects to design innovative immunotherapies targeting cytokine activity to specific cell types date: 2014-10-30 journal: front immunol doi: 10.3389/fimmu.2014.00526 sha: doc_id: 265005 cord_uid: e6rpryrh type i interferons (ifn-i) were identified over 50 years ago as cytokines critical for host defense against viral infections. ifn-i promote anti-viral defense through two main mechanisms. first, ifn-i directly reinforce or induce de novo in potentially all cells the expression of effector molecules of intrinsic anti-viral immunity. second, ifn-i orchestrate innate and adaptive anti-viral immunity. however, ifn-i responses can be deleterious for the host in a number of circumstances, including secondary bacterial or fungal infections, several autoimmune diseases, and, paradoxically, certain chronic viral infections. we will review the proposed nature of protective versus deleterious ifn-i responses in selected diseases. emphasis will be put on the potentially deleterious functions of ifn-i in human immunodeficiency virus type 1 (hiv-1) infection, and on the respective roles of ifn-i and ifn-iii in promoting resolution of hepatitis c virus (hcv) infection. we will then discuss how the balance between beneficial versus deleterious ifn-i responses is modulated by several key parameters including (i) the subtypes and dose of ifn-i produced, (ii) the cell types affected by ifn-i, and (iii) the source and timing of ifn-i production. finally, we will speculate how integration of this knowledge combined with advanced biochemical manipulation of the activity of the cytokines should allow designing innovative immunotherapeutic treatments in patients. specifically, we will discuss how induction or blockade of specific ifn-i responses in targeted cell types could promote the beneficial functions of ifn-i and/or dampen their deleterious effects, in a manner adapted to each disease. type i interferons (ifn-i) were the first cytokines discovered, over 50 years ago, based on their potent anti-viral effects (1, 2) . ifn-i play a crucial, non-redundant role in vertebrate anti-viral defenses (3) (4) (5) . ifn-i also mediate protective effects in other physiopathological contexts, including cancer (6) and multiple sclerosis (ms) (7) . on the contrary, ifn-i responses can be deleterious in a number of circumstances, including bacterial or fungal infections (8-10), many autoimmune diseases (11) , and, paradoxically, certain chronic viral infections (12) (13) (14) . it is only recently that an integrated picture has emerged of the cellular and molecular mechanisms regulating the production of ifn-i and underlying their functions. much knowledge was gained recently on another class of potent innate anti-viral interferons, the lambda, or type iii ifns (ifn-iii). we will review knowledge on ifn-i/iii (ifns) and discuss how it could be harnessed to develop innovative therapeutic strategies aimed at surgically tuning ifn activity toward protective responses in a manner adapted to each disease. we will focus on ifn-α/β/λ because they are the best characterized ifns and already used therapeutically. recent reviews are covering information on other ifn-i subsets including ifn-ε, which is produced at mucosal sites and promotes local anti-viral defenses (15, 16) . dendritic cells (dcs) are rare heterogeneous mononuclear phagocytes functionally characterized by their unique efficacy for antigen-specific activation of naïve t lymphocytes. dcs are sentinel cells of the immune system, able to sense and integrate a variety of danger input signals for delivery of output signals instructing the activation and functional polarization of effector immune cells. in mammals, five major dc subsets exist, which differ in their expression of innate immune recognition receptors (i 2 r 2 s) and in their functional specialization: monocyte-derived dcs (modcs), langerhans cells, cd11b + dcs, xcr1 + dcs, and plasmacytoid dcs (pdcs) (17) . a recurrent theme of this review will be the intricate relationships between ifns and dcs, since these cells can be a major source and/or target of these cytokines under various conditions. www.frontiersin.org the first section will synthesize current knowledge on ifn production and protective anti-viral functions. the i 2 r 2 s and downstream signaling pathways responsible for ifn-i production during viral infection will be listed. the roles of different cell types for this function will be discussed. the two main mechanisms through which ifn-i promote anti-viral defense will be reviewed, succinctly for direct anti-viral effects and in greater details for immunoregulatory functions. the second section will focus on the detrimental functions of ifn-i. selected diseases will be discussed to illustrate how different, and sometimes opposite, processes underlie deleterious ifn-i responses depending on the physiopathological contexts. ifn-i induction of unbridled inflammatory responses causing lethal tissue damage will be discussed as a major pathological mechanism during bacterial encounters secondary to influenza infection or in some autoimmune diseases. inappropriate functional polarization of immune responses by ifn-i will be discussed as one potential cause for enhanced susceptibility to bacterial or fungal infections. the complex and disputed role of ifn-i in chronic viral infections will be reviewed, with emphasis on the physiopathology of the infections by human immunodeficiency virus type 1 (hiv-1) and human hepatitis c virus (hcv), with an outlook for the development of novel immunotherapeutic strategies to combine with anti-viral drugs. the third section will recapitulate how the balance between beneficial versus deleterious ifn-i responses is modulated by several key parameters including (i) the source and timing of ifn-i production, (ii) the cell types affected by ifn-i, and (iii) the signaling pathways activated by ifn-i. in the last section, we will speculate how integration of all the knowledge discussed before combined with advanced biochemical manipulation of the activity of the cytokines should allow designing innovative immunotherapeutic treatments, based on induction or blockade of specific ifn-i responses in targeted cell types. this"activity-by-targeting"concept is based on the design of novel "immuno-ifns" consisting in covalent association between a mutated ifn-i with decreased affinity for its receptor and an antibody with high avidity for a molecule specifically expressed on target cell types (18) . this design ensures lack of activity of the immuno-ifns on all cell types but those targeted, contrary to previous strategies using ifns with close to maximal potency that were still able to mediate strong off-target effects despite their coupling to cell-type specific antibodies and/or their local delivery. type i interferons expression is not detectable under steady state conditions in vivo using classical methods such as gene expression analysis by rt-pcr or protein titration by elisa or bioassays. however, mice deficient for the expression of the alpha chain of the ifn-i receptor (ifnar1) harbor alteration in the ontogeny or functions of various cell types (19) (20) (21) (22) (23) (24) (25) (26) . hence, extremely small or localized but functionally relevant quantities of ifn-i must be produced under steady state conditions (27) . indeed, the existence of steady state responses to ifn-i in various organs in vivo was demonstrated by using reporter mice expressing the firefly luciferase under the control of the promoter of ifnb1 (28) or of mx2 (29) , a canonical ifn-i-stimulated gene (isg). steady state ifn-i responses are promoted by gut commensals (30) . early and transiently after many viral infections, large amounts of ifns can be detected, in blood and spleen in the case of systemic infections or locally in the case of confined infections. ifn induction during viral infections results from the detection of specific danger signals by specialized i 2 r 2 s. this includes the detection of pathogen-associated molecular patterns as well as the sensing of stress signals or damage-associated molecular patterns (31, 32) . based on the nature and intracellular location of the danger signals that induce the production of the cytokines, the cellular sources of ifns during viral infection can be classified in two main groups. infected cells often contribute to ifn production as a response to their sensing of endogenous viral replication, or consecutive to the metabolic stress induced during massive translation of viral structural proteins, or as a result of plasma membrane perturbations upon viral entry. specific subsets of uninfected cells can also significantly contribute to ifn production upon engulfment of material containing viral-derived nucleotide sequences and sensing of these molecules in endosomes by specific i 2 r 2 s. all sensing pathways leading to ifn induction converge on the activation of interferon response factors 3 or 7 (irf3/7), which are the master transcription factors inducing ifn genes. most cell types constitutively express irf3 but not irf7 or only at low levels. irf7 expression requires ifn-i stimulation. ifn-β can directly be induced by irf3. all but one of the ifn-α subtypes require irf7 for their induction. hence, ifn-β secretion promotes its own production and that of ifn-α in an autocrine manner (33, 34) . this positive feedback loop strongly amplifies ifn production during viral infections, promoting fast and widespread induction of cell-intrinsic anti-viral defenses in uninfected cells to prevent virus dissemination. other feedback loops tightly regulate ifn-i production positively or negatively. this section reviews different mechanisms controlling ifn production and how they could play different roles in host/virus interactions. different innate immune recognition receptors are involved in sensing various types of viral nucleic acids in distinct categories of cells during viral infections, which may promote different types of anti-viral defenses. for each selected sensor shown, the types of viral nucleic acids recognized and the downstream signaling cascade induced are represented in a simplified, schematic manner. the potential specific role of each cell type in anti-viral defenses is also indicated at the bottom of each panel. (a) potentially all types of infected cells can detect endogenous viral replication through cytosolic sensors triggering their local production of ifn-β/λ to control viral replication in an autocrine and paracrine fashion in infected tissues. (b) uninfected xcr1 + dcs selectively produce high levels of ifn-λ and ifn-β upon engulfment of materials containing dsrna and the consecutive triggering of tlr3 in endosomes. the receptor of ifn-λ is mostly expressed by epithelial cells. hence, xcr1 + dcs might be involved in inducing local ifn responses in virally infected epithelial tissues. since xcr1 + dcs are especially efficient at producing ifn-iii upon hcv stimulation, they might contribute to local or systemic ifn production during infection with this virus, to promote ifn-λ-mediated protection of hepatocytes. uninfected xcr1 + dcs and other uninfected cells may produce some ifn-β upon engulfment of materials containing ssrna and the consecutive triggering of tlr8 in endosomes. the contribution of this pathway to anti-viral defense is not well understood yet, in part because mouse tlr8 is deficient for this function. (c) uninfected pdcs selectively produce high levels of all subsets of ifns upon engulfment of materials containing ssrna or cpg dna and the consecutive triggering of tlr7/9 in endosomes. however, pdcs seem to be activated for this function only in lymphoid tissues. hence, pdc might contribute to systemic ifn production during blood-borne viral infections or as a failsafe mechanism activated upon abnormal widespread dissemination of a viral infection once it has escaped local confinement at its portal of entry. cm, cell membrane; nm, nuclear membrane. particular nucleotide sequences or tertiary structures, their signaling pathways and their physiological significance have been recently reviewed (31, 32) . cytosolic rna sensors encompass dexd/h helicases among which the retinoic-acid-inducible gene (rig)-i-like receptors (rlrs) have been the most studied, namely rig-i and melanoma differentiation associated gene 5 (mda5). rig-i recognizes rna with a 5 -ppp or 5 -pp (38) (uncapped) moiety, or double-stranded rna (dsrna), both structures being present in viral, but not in cytosolic eukaryotic, rna molecules. mda5 might specifically recognize long dsrna fragments. both rig-i and mda5 contain a dexd/h box-containing rna helicase domain, and 2 caspase recruitment domains (card1/2), which bind to mitochondrial anti-viral signaling protein (mavs). rna/rlr/sting molecular complexes initiate a signaling cascade leading to irf3/7-dependent induction of ifns (figure 1 ). other dexd/h helicases can promote ifn-i production in dcs, www.frontiersin.org although their physiological roles for in vivo immune defenses against viral infections remain to be established (32) . cytosolic dna sensors able to induce ifn-i (mostly ifn-β) and ifn-iii encompass molecules belonging to different protein families, including dexd/h helicases, the inflammasome component ifn-γ-inducible protein 16 (ifi16) , the z-dna binding protein 1 (zbp1), and the cyclic gmp-amp (cgamp) synthase (cgas) (31, 32) . most of the cytosolic dna sensors activate sting and lead to irf3/7-and nfκb-dependent induction of ifn-β and ifn-iii. many cell types express zbp1 and are able to produce ifn-i upon triggering of this molecule, including macrophages, dcs, and fibroblasts following an hsv-1 infection (39, 40) . upon dna binding, cgas catalyzes the production of cgamp. cgas is critical for the detection of lentiviruses including hiv-1/2 (41, 42) and can contribute to sensing of, and protection against, other rna viruses, including in vivo in mice (43) . cgamp also acts as a secreted second messenger signal alerting uninfected cells to directly induce their expression of intrinsic immune anti-viral defenses. the cgas/sting/irf3 signaling cascade and the irf1 transcription factor are "master" inducers of cell-intrinsic immunity able to control the replication of most dna and some rna viruses at least in part independently of ifns (43) . infected cells become a factory for production of viral particles. hijacking of the translation apparatus of the host cell for massive production of viral structural proteins leads to an overload of the capacity of the er for correct folding of newly synthesized proteins. er overload induces a homeostatic response of the cell, the unfolded protein response (upr). upr aims at restoring normal er functions by inhibiting translation. upr activation in infected cells contributes to prevent viral replication, including through inhibition of the production of viral proteins, promotion of ifn-i production, and induction of cell suicide (44) . toll-like receptors (tlrs) are among the first and best characterized i 2 r 2 s. tlrs are transmembrane proteins with a leucine-rich repeat extracellular domain involved in ligand recognition and an intracellular toll/interleukin-1 receptor domain essential for signaling (45) . among the nine tlrs conserved between mouse and human, tlr3, tlr7, tlr8, and tlr9 are located in endosomes where they can detect the abnormal presence of nucleic acids such as occurs upon endocytosis of virions or of virally infected cell material. tlr3 recognizes dsrna, tlr7/8 ssrna, and tlr9 dna sequences containing unmethylated cytidinephosphate-guanosine (cpg) motifs. tlr fine specificity and signaling pathways have been reviewed recently (32) and are summarized in figure 1 . we will discuss the expression patterns and functions of endosomal tlrs with regards to ifn production in uninfected specialized immune cell types, pdcs and xcr1 + dcs. plasmacytoid dcs uniquely produce very large amounts of ifns in response to in vitro stimulation with many viruses, without being infected (46) . ifn-i mrnas represent up to 40% of all mrnas in pdcs at the peak of their activation (47) . in vitro, upon exposure to influenza virus, herpes virus type 1, cytomegaloviruses, or vesicular stomatitis virus, individual pdcs produce 100-1000 times more ifns than total pbmcs, monocytes, modcs, cdcs, neutrophils, and fibroblasts (47) (48) (49) (50) (51) (52) . however, in vitro, high molarity infection of cdcs with certain viruses unable to inhibit ifn-i production in their target cells can also induce massive ifn-β secretion (53) . pdcs produce high levels of all subtypes of ifns, contrary to many other cell types including infected cells, which often preferentially produce ifn-β (46, 47) . in vivo, pdc depletion during systemic viral infections leads to over 95% decrease of ifn-i production, while the total number of pdcs producing ifn-i (<100,000 in one mouse) is much lower than the total number of infected cells (54) (55) (56) (57) (58) (59) . this shows that in vivo also individual activated pdcs produce much more ifn-i/iii than most other cell types, including virus-infected cells. the professional ifn-producing function of pdcs largely results from their high constitutive and selective expression of irf7, tlr7, and tlr9 (figure 1) . these molecules are pre-associated in readyto-signal complexes located in specialized endosomes specific to pdcs (60, 61) . pdcs must also be equipped for efficient sensing and up-take of virions and virus-infected cells. the corresponding cell surface i 2 r 2 s remain to be identified. selective expression of tlr3 in xcr1 + dc endows them with a unique ability to produce very high amounts of ifn-β and ifn-iii upon stimulation with dsrna or hcv irrespective of their own infection. xcr1 + dcs are very potent for antigenspecific activation of cd8 + t cells, in particular through crosspresentation of exogenous antigens that they have captured from other cells and processed for association with class i major complex histocompatibility (mhc-i) molecules (62) . in mice, xcr1 + dcs are crucial for the initiation of protective adaptive immune responses against tumors and a variety of viruses (63) . mouse and human xcr1 + dcs constitutively and selectively express high levels of tlr3 (figure 1) . they produce large amounts of ifn-iii and ifn-β upon stimulation with a synthetic mimetic of dsrna, polyinosinic:polycytidylic acid (polyi:c) (64, 65) . human xcr1 + dcs uniquely respond to stimulation with hcv by producing large amounts of ifn-iii in a tlr3-dependent manner (66, 67) , irrespective of their own infection. positive feedback loops. in addition to irf7 induction, other positive feedback mechanisms exist to amplify the production of ifns rapidly after initiation of a viral infection as illustrated by the following selected examples. ifns induce the expression of many cytosolic rna/dna sensors and of tlr7. this broadens the spectrum of host's cell types able to detect endogenous viral replication for ifn induction. induction of oasl by ifns in human cells enforces rig-i signaling, counteracting viral immune frontiers in immunology | microbial immunology evasion genes interfering with this sensing pathway (68) . the ifninducible ribonuclease l (rnasel) generates viral and cellular rna degradation products, which engage rlrs for amplification of ifn production (69, 70) . the ifn-inducible protein kinase r (pkr) stabilizes ifn-i mrna (71) . to prevent unbridled responses deleterious for the host, ifn activity must be tightly controlled including during viral infections. several negative feedback loops exist to terminate ifn production, after anti-viral defenses have been activated. the isg ubiquitin specific peptidase 18 (usp18) binds to ifnar2, preventing it from recruiting signal transducer and activator of transcription 1 (stat1). ifns induce the expression of tam receptor tyrosine kinases in dcs, monocytes, and macrophages. tam receptors associate and signal in part through ifnar1. they activate the suppressors of cytokine signaling-1/3 (socs-1/3). socs inhibit tlr and rlr signaling, thereby terminating ifn production (72) . tam receptor ligands, gas6 and pros, bind phosphatidylserine on dying cells and are produced by activated dcs and monocytes/macrophages. thus, ifn induction of tam inhibitory receptors on uninfected phagocytic immune cells could limit their propensity to produce the cytokines upon engulfment of dying virally infected cells. ifns induce tetherin on most cell types. pdcs express a receptor for tetherin, leukocyte immunoglobulin-like receptor, subfamily a (with tm domain), member 4 (lilra4). lilra4 triggering on pdcs inhibits their production of ifn-i. hence, through lilra4 engagement by tetherin, pdcs can monitor their efficacy at inducing an antiviral gene expression program in neighboring cells through ifns, and timely terminate their ifn production. how positive and negative feedback loops integrate in time and space to promote optimal kinetics and intensity of ifn production in order to efficiently control viral infection without causing severe immunopathology is not completely understood. positive feedback loops may occur very rapidly after initiation of viral infection to allow rapid secretion of high levels of the cytokines for fast and strong induction of anti-viral cell-intrinsic immunity. negative feedback loops occur likely later to terminate the response and thus avoid chronicity of cytokine production and its ensuing deleterious effects. pdcs do not constitute the major source of ifn production upon local infections by several viruses in the lung or in the female reproductive tract. pdcs are dispensable for resistance against these infections (56, 73, 74) . during pulmonary infection by newcastle disease virus (ndv), ifn-i are produced locally in the lungs mainly by infected alveolar macrophages. lung pdcs do not express the cytokines (73) . selective depletion of lung alveolar macrophages leads to systemic dissemination of ndv, and to a strong activation of pdcs for ifn-i production specifically in the spleen. even in the case of systemic viral infections such as caused by intravenous injection of ndv or intraperitoneal injection of mouse cytomegalovirus (mcmv), pdc ifn production is confined to the spleen. it is not detected in other organs even those with high viral replication (59, 73) . hence, splenic pdcs are especially prone to high level ifn production upon systemic acute viral infections. pdcs located in non-lymphoid organs, in particular mucosal barrier tissues, appear to be inhibited for ifn production. thus, ifn production by infected cells serves as first line of defense to block virus replication at its portal of entry in the body. ifn production by uninfected pdcs might constitute a failsafe mechanism mainly activated in the spleen when viral infection gets systemic (75) . under these conditions, to promote health over disease, the benefits for the host of producing high circulating levels of ifns in order to induce widespread cell-intrinsic anti-viral defenses might prevail over the deleterious effects that this could cause on certain cell types or tissues. indeed, pdcs are required for protection against hsv-2 and hsv-1 in mice only in systemic but not local infections (56) . this observation is consistent with the crucial role of pdcs for protection of mice against systemic infection by mouse hepatitis virus (mhv), a fast replicating coronavirus (55) . conflicting results have been obtained on the role of pdcs during intranasal influenza infection (74, (76) (77) (78) . a possible explanation is that pdc ifn production contributes to resistance to highly pathogenic influenza strains that might systemically spread from the lung early after infection, even if at low levels. another intriguing observation is that ifns are critical for host resistance to mcmv and that pdcs are the major source of ifns in this infection model but are dispensable for virus control (54) . studies are ongoing to understand this apparent paradox. patients bearing genetic mutations disrupting endosomal tlr signaling do not appear to suffer from life-threatening viral infections (79, 80) , contrary to patients impaired in ifnar signaling (4, 81) . a notable exception is the specific susceptibility to severe herpes virus encephalitis in individuals' deficient for tlr3 signaling (82, 83) . however, contrary to extracellular tlr, endosomal tlr have evolved under strong purifying selection in human beings (84) . hence, while pdcs and endosomal tlr might have been required for protection of our species against viral infections in the past, this appears not to be the case anymore perhaps due to improved social, hygiene, and health care in modern society (75) . attesting to the importance of ifns for anti-viral defense in vertebrates, many mammalian viruses encode immune evasion genes specifically inhibiting the production of ifns in infected cells (39, 85) . pdcs or xcr1 + dcs might be essential for ifndependent host protection against these viruses, because they are spared from the intracellular functions of viral immune evasion genes (75) . to the best of our knowledge, mcmv does not encode for immune evasion genes inhibiting ifn production. however, mcmv manipulates ifn-i responses through specific inhibition of stat1 functions in infected cells. thus, pdcs might be dispensable for resistance against systemic mcmv infection due to sufficient levels of ifn production by infected cells locally in all infected tissues. hepatocyte responses to ifn-iii appear to play a www.frontiersin.org critical role in human resistance to hcv. in infected hepatocytes, hcv induces the expression of cellular micrornas binding to ifn-iii mrna and leading to its degradation. uninfected xcr1 + dcs produce high levels of ifn-iii in vitro upon hcv stimulation (66, 67) . hence, during acute hcv infection in vivo, xcr1 + dc may be a strong and early source of ifn-iii not subjected to virus immune evasion strategies, therefore, contributing to protect naturally resistant individuals. in secondary lymphoid organs, a subset of macrophages is critical for the clearance of viruses from the lymph (86) . these macrophages are located on viral entry routes, near to subcapsular sinuses where the afferent lymph drained from non-lymphoid tissues flows. contrary to other subsets of macrophages, subcapsular sinus macrophages are highly susceptible to viral infection, because they constitutively express only low levels of effector molecules of cell-intrinsic anti-viral immunity and because their responses to ifns are inhibited by their high constitutive expression of usp18. subcapsular sinus macrophages rapidly become infected by viruses incoming from the lymph and produce large amounts of ifns. this altruistic suicide prevents virus dissemination to other adjacent cell types and promotes the induction of innate and adaptive anti-viral immunity (87) . upon instruction by ifns, cells express a wide variety of viral restriction factors, whose combined action blocks pathogen invasion by interfering with the different stages of viral life cycle (figure 2a ). this has been extensively reviewed recently (88) and will only be described succinctly here. virus fusion with host cell membrane can be blocked by cholesterol-25hydrolase (ch25h) that inhibits sterol biosynthesis. some viruses enter cells by escaping from endosomes/lysosomes, which can be blocked by interferon inducible transmembrane (ifitm) proteins. virus uncoating can be blocked by tripartite motif (trim) proteins, such as trim5α, which bind to hiv-1 capsid thus promoting its degradation, and by myxoma resistance gtpases, mx1, and mx2, which efficiently trap viral structural proteins at an early stage following virus entry into the cell. mx1 inhibits a number of viruses, including influenza virus through sequestration of its nucleocapsid. mx2 associates with host cyclophilin a and hiv-1 capsid protein. virion assembly can be blocked at transcriptional, translational, and posttranslational levels. the adenosine deaminase acting on rna 1 (adar1) and the apolipoprotein b mrna editing enzyme, catalytic polypeptide-like (apobec) deaminases induce viral rna destabilization and hypermutation (89, 90) . the sterile alpha motif and histidine-aspartic domain (hd) containing protein 1 (samhd1) blocks reverse transcription by hydrolyzing dntps (91) . adar1, apobec, and samhd1 functions have been mainly studied in infections by hiv-1 and other retroviruses. the 2 ,5 -oligoadenylate synthase (oas) proteins, the ifn-induced proteins with tetratricopeptide repeats (ifit), and pkr inhibit viral and host protein translation by using complementary mechanisms (88) . the major post-translation modification induced by ifns is the binding of the ubiquitinlike modifier isg15 to several viral and host proteins, a process called isgylation. most of the known isgylated proteins are targeted for degradation, with few exceptions that are on the contrary stabilized like irf3 (88) . finally, the egress and budding of virions of many enveloped viruses can be inhibited by tetherin or by viperin (88) . many anti-viral isgs have been functionally characterized only recently, largely thanks to large-scale screening approaches. they display a variable degree of viral specificity (43, 92) that might inversely relate to the extent of their side effects on host cells ( figure 2b ). anti-viral effectors acting on a broad spectrum of viruses often target key metabolic pathways that are also crucial for host cell functions. this is the case for the control of cholesterol metabolism by ch25h (93) or of protein translation by pkr, oas, or ifits (88) . other anti-viral restriction factors such as mx2 may specifically target one molecule of a very restricted set of viruses with no apparent side effects on host cells. some anti-viral isgs target specific functions critical for only a restricted array of viruses and might similarly exert side effects only on a subset of host cell types. for example, samhd1 inhibits retrovirus replication through dntp depletion, which might more specifically affect proliferating host cells. hence, the infected host must balance the intensity, breadth, and location of isg induction to circumvent viral replication while preventing life-threatening damages to vital cell types or tissues. one of the mechanisms contributing to this balance is translational control of the expression of isgs, especially those with pro-apoptotic or anti-proliferative functions (94) . while many anti-viral isgs are transcriptionally activated in most ifn-stimulated cells, their translation can be specifically blocked in uninfected cells by cellular microrna. this inhibition is relieved upon cell infection through negative regulation of the function of the rna-induced silencing complex. hence, ifn stimulation of uninfected cells prepares them for rapid and strong induction of cell-intrinsic anti-viral defenses upon viral infection while avoiding their unnecessary exposure to the toxic effects of certain isgs. further knowledge on the functions and the dynamic regulation of isgs is essential to develop novel therapeutic strategies against viral infections aiming at modulating ifn responses to promote their protective anti-viral cell-intrinsic functions over their deleterious toxic effects. a better understanding of the immunoregulatory effects of ifns will also help. type i interferon can modulate the functions of a broad spectrum of immune cells ( figure 3a ). we will review this knowledge, focusing on the functions of dcs, nk cells, t cells, and b cells, since they are involved in the control of most viral infections. we will discuss the hypothesis that dcs play a central role in ifn-i orchestration of innate and adaptive immunity for the induction of optimal anti-viral defenses (figure 3) . during viral infections and cancer immunosurveillance, ifn-i constitute one of the most important input signal acting on dcs to promote their delivery of appropriate output signals to t cells, b cells, and nk cells for protective immunity ( figure 3a ). dcs deliver three types of signals to activate and functionally polarize t cells. signal 1 is the triggering of the t cell receptor by viral peptide-mhc complexes. signal 2 is the triggering of activating t cell co-stimulation receptors such as cd28 or cd27 by the cd80/86 and cd70 co-stimulation molecules expressed on dcs. signal 3 corresponds to cytokines, which can promote t cell proliferation and acquisition of specific effector functions. under steady state conditions, most dcs are in an immature state characterized by low level expression of mhc-ii (signal 1) and co-stimulation molecules (signal 2) and by the lack of production of t cell-activating www.frontiersin.org cytokines (signal 3). upon activation, including early after viral infections in vivo, dcs up-regulate their expression of signal 1 and activating signal 2 and secrete t cell-activating cytokines. this process is called dc maturation. gene expression profiling of dcs stimulated by microbial stimuli identified a core set of genes upregulated in mature dcs irrespective of the stimulus they receive, irrespective of the subset they belong to, and conserved across evolution (95) . most of these genes are induced during dc maturation in part through cell-intrinsic ifn-i signaling (95) . consistently, cell-intrinsic ifnar signaling in dcs is required in many circumstances for the induction of protective immunity, including efficient cd8 t cell responses during viral infection or tumor development (96) (97) (98) , th1 responses upon polyi:c injection independently of il-12 or ifn-γ effects (99, 100) , as well as follicular helper t cell and humoral responses (101, 102) . mechanistically, ifn-i promote dc immunogenicity for efficient t cell activation through a variety of effects ( figure 3b) . it drives dc up-regulation of signal 2 in vivo during viral infections (103) and boosts their capacity to cross-present antigens for increased delivery of signal 1 to cd8 t cells (96) (97) (98) . it shapes their delivery of activating signal 3, in particular inducing il-15 and promoting or inhibiting il-12 depending on experimental conditions (58, 104) . finally, it is necessary to induce their metabolic shift from mitochondrial oxidative phosphorylation to aerobic glycolysis, which fuels the increased needs in energy and the expansion of the intracellular organelles required for the production and proper intracellular routing of the signal 1 and 2 proteins (100, 105). selective inactivation of ifnar on cdcs compromises mouse resistance to mcmv and mhv infections (103, 106) . in contrast, ifnar expression is not required on nk cells for protection against mcmv and on pdcs, t cells, and b cells for early control of mhv replication (103, 106) . although cell-intrinsic ifn-i signaling in nk cells can promote their activation (107) (figure 3a) , ifn-i-induced il-15 trans-presentation by dcs plays a more prominent role for this function in many conditions including in vivo during mcmv infection (103, 108) ( figure 3c) . cell-intrinsic ifn-i signaling in cd4 t cells (109), cd8 t cells (110, 111) , and b cells (112) can also contribute to their efficient activation and functional polarization (figure 3 ). this depends on experimental settings. cd8 t cell-intrinsic ifn-i responses are crucial for mounting efficient cytotoxic cd8 t cell responses against lcmv but are less critical against vaccinia virus and vesicular stomatitis virus (110, 113, 114) . mechanistically, cell-intrinsic ifn-i signaling in cd8 t cells can promote their survival during their antigen-induced proliferation (110) . cell-intrinsic signaling in dcs and cd8 t cells may act in a synergistic manner. indeed, conditional inactivation of ifn-i responsiveness was required to occur simultaneously in both of these two cell types to dramatically affect cd8 t cell expansion upon vaccination with a modified ankara vaccinia virus (115) . in summary, ifn-i generally play a crucial, beneficial, role in immune defenses against viral infections, both through the induction of cell-intrinsic anti-viral defenses and through the orchestration of innate and adaptive immunity. however, if these responses are not properly regulated, they can contribute to diseases as we will now discuss. a frequent side effect of ifn-i treatment against cancer or chronic viral infections is the induction of autoimmune reactions. consistently, isg expression is a hallmark of many spontaneous systemic or tissue-specific autoimmune diseases, including systemic lupus erythematosous (sle), sjogren's syndrome, psoriasis, and other skin disorders (11) . the dysregulation of ifn-i responses observed in patients with these autoimmune diseases likely results from both genetic and environmental factors. genome-wide association studies show that polymorphisms in genes involved in ifn-i responses strongly correlate with increased susceptibility to many autoimmune diseases (11) . diverse environmental factors can also contribute to the onset of autoimmune diseases. microbial infections often precede first clinical manifestations of autoimmune diseases. whether infections (116) and/or alterations in the commensal microbiota of the affected barrier tissues (117, 118) are the cause or rather the consequence of autoimmunity is still matter of debate. infection-or dysbiosis-induced tissue damages and unbridled ifn-i responses can contribute to initiate autoimmune reactions. gender is another prominent factor affecting susceptibility to autoimmune diseases. women are more prone to autoimmunity, which may result from endocrine regulation of ifn-i responses. pdc ifn-i production is enhanced in human and mouse females, due at least in part to cell-intrinsic enhancement of tlr7/9 responses by the female hormone estradiol (119). in autoimmune diseases, different mechanisms could operate to initiate the dysregulation of immune responses leading to a vicious circle of reciprocal activation between innate ifn-i responses and adaptive self-reactive lymphocyte responses (figure 4) . adaptive immune cells are educated to spare "self." this occurs through negative selection of potentially autoimmune b and t cells during their development in the bone marrow or thymus, respectively, a process called central tolerance. self-reactive b or t cells that have escaped this pruning can be either deleted or functionally inactivated once they have egressed in secondary lymphoid organs or non-lymphoid tissues, a process called peripheral tolerance. in some individuals, polymorphisms in genes involved in the promotion of central or peripheral tolerance lead to a higher number, diversity, and/or responsiveness of self-reactive lymphocytes in the periphery, in particular of b cells secreting anti-dna or anti-rnp antibodies (120, 121) . mammalian dna or rna are poor inducers of pdc ifn-i induction under normal conditions. however, pre-existing anti-dna or anti-rnp autoantibodies can break this innate tolerance of pdc. indeed, antibodies binding to self nucleic acids can protect them from degradation and compact them into nanoparticles that are very effective for the induction of ifn-i in pdc (figure 4) . dna-containing immune complexes (ics) are frequently found in the serum of sle patients (sle-ics) and can activate pdc ifn-i production (122) . in turn, pdc ifn-i activate cdcs, monocytes (123) , and b cells, leading to a vicious circle of reciprocal activation between dcs and frontiers in immunology | microbial immunology figure 4 | a simplified model of the deleterious role of ifn-i in several autoimmune diseases. when exposed to different kinds of injuries (microbial infection, commensal microbiota dysbiosis, chemical or physical insults), healthy tissues can undergo cell damage and death. these events induce the release of apoptotic bodies encompassing self rna or dna. neutrophil recruitment and activation in inflamed tissues can also constitute a potent source of self nucleic acids, through the release of neutrophil extracellular traps (net). self rna or dna can associate with cationic peptides (e.g., ll37) as shown in psoriatic patients or with inflammatory molecules (e.g., high mobility group box 1, hmgb1) to generate nanoparticles that are extremely efficient for ifn-i production by pdc and eventually other cell types. pdc can also be efficiently activated for ifn-i production by immune complexes (ics) generated by the association between self nucleic acids and auto-antibodies as frequently found in the serum of systemic lupus erythematosus patients. ifn-i promote the differentiation and/or the maturation of antigen-presenting cells, in particular different subsets of dc. activated dc can then present self-antigens for activation of auto-reactive t cd4 + cells, including follicular helper lymphocytes, which in turn activate auto-reactive b cells for auto-antibody secretion, leading to a vicious circle of reciprocal activation between innate and auto-reactive adaptive immune cells. idc, immature dc; mdc, mature dc; mo-dc, monocyte-derived dc. see main text for further details. self-reactive lymphocytes and to the exacerbation of autoimmune responses (figure 4) . certain infections or dysbiosis of the commensal microbiota of the affected barrier tissues could promote chronic production of host amphiphatic peptides able to combine with eukaryotic dna or rna, likely released from dying cells, thus forming pdc-activating nanoparticles. indeed, in psoriatic skin, both a high expression of ll37 and a massive infiltration of pdcs is observed (124) (figure 4) . hence, to treat many autoimmune diseases, novel therapeutic strategies could be designed to target dysregulated pdc ifn-i production or b cell activation by ifn-i. one of the most common complications of primary infections by many respiratory viruses, in particular influenza virus, is a lifethreatening pneumonia due to secondary pulmonary infections by bacteria, such as streptococcus pneumoniae, staphylococcus aureus, or haemophilus influenza (125, 126) . these pathologies affect especially infants, elderly, and immunocompromised patients. retrospective studies indicate that secondary bacterial pneumonia was highly recurrent in lung tissues isolated from patients who died during last century influenza pandemics, independently of antibiotic availability (127, 128) . influenza virus induces high ifn-i responses in human beings and mice. in both hosts, secondary bacterial infections are lethal only when they occur in a limited time window following primary viral infection (3-7 days), around the peak of ifn-i responses, before complete virus clearance. mouse models of viral/bacterial coinfections are being used to dissect disease mechanisms (129) . ifnar1-deficient mice appear more resistant to secondary pulmonary bacterial infections, showing that ifn-i responsiveness contributes to disease (130) . similarly, after lymphochoriomeningitis virus (lcmv) infection, wild-type but not ifnar1-deficient mice are more susceptible to lpsinduced septic shock (131) . several mechanisms may contribute to the detrimental role of ifn-i in secondary bacterial infections ( figure 5) . early during viral infection, ifn-i decrease the host ability to control bacterial replication, by dominantly polarizing immune responses toward anti-viral functions, simultaneously inhibiting the development of the types of immune responses required for protection against most bacterial infections. ifn-i can inhibit the production of chemokines required for the recruitment to the respiratory tract of antibacterial effector innate immune cells, in particular neutrophils or monocytes/macrophages (132, 133) (figure 5) . depending on the experimental models used, ifn-i can on the contrary induce a ccr2-dependant recruitment of classical monocytes (134) . in infected tissue, ifn-i might skew the functional polarization of resident or infiltrating monocytic cells toward immunosuppression, because it does limit their antibacterial functions by inhibiting their il-1 production (135) (136) (137) while it might promote their production of il-10 and nitric oxygen intermediates. the exact nature of infiltrating monocytic cells is not clear and could correspond to activated classical monocytes, modcs, monocyte-derived macrophages, or myeloidderived suppressor cells (mdscs). the boundaries between these putatively different cell types are currently ill-defined (138) . these cells could fuel local replication of monocyte/macrophage-tropic bacteria (134) , be immunosuppressive (139) or contribute to local immunopathology (140) . the role of ifn-i on monocytes/macrophages is complex and will require further investigations to determine when it is protective versus deleterious and what the underlying mechanisms are. depending on the context, ifn-i can either promote or inhibit the induction of th1 cytokines such as il-12 and ifn-γ, and myeloid cell responses to ifn-γ (10, (141) (142) (143) . ifn-i can also polarize cd4 t cell responses toward th1 at the expense of th17, while the th17-type cytokines il-17a and il-22 are required for host defense against pulmonary www.frontiersin.org bacteria by inducing the production of anti-microbial peptides and of tissue repair molecules ( figure 5 ) (141) (142) (143) . ifn-i may not only affect host resistance to bacterial infection, but also host tolerance, i.e., the ability of the host to tolerate a given burden of pathogen without undergoing excessive tissue damages (143, 144) . hence, to counter ifn-i deleterious effects during secondary bacterial infections, it will be important to better delineate the respective contribution of lung tissue tolerance modulation and of immune-mediated resistance weakening. another well documented example of deleterious effects of ifn-i due to their inappropriate functional polarization of immune responses is the enhanced susceptibility to fungal infections of patients with genetically determined hyperactive ifn-i responses, as exemplified in the hereditary disease chronic mucocutaneous candidiadis (cmc) (figure 5 ) (145) . patients with cmc have a significant deficit in th17 cd4 t cells, at least in part as a consequence of altered responsiveness to il-6 or il-21. several stat1 mutations were identified in patients with autosomal dominant cmc. gain-of-function stat1 mutations were found to hard wire cd4 t cell responses to cytokines toward stat1 signaling, compromising their stat3-dependent ability to produce il-17 upon il-6 or il-21 stimulation. this was associated to induction of a global ifn-i transcriptomic signature in blood (145) . deleterious ifn-i effects on immunity to candida might not only occur in cmc patients but also in other types of individuals upon secondary fungal infections occurring shortly after a primary viral infection, likewise to the situation discussed above for secondary bacterial infections. indeed, polyic induced ifn-i abrogate innate immunity to systemic candidiasis in mice (146) , and ifnar-deficient mice can be more resistant to candida infection under certain experimental settings (147) . however, the role of ifn-i in the modulation of the ability of immunocompetent hosts to control fungal infection is disputed (148, 149) . the inhibition of th17 responses by ifn-i could be protective in at least one important human pathology, ms (figure 5) . ms represents a striking exception to the previously discussed detrimental role of ifn-i in autoimmune diseases. indeed, a large proportion of ms patients have low serum ifn-i activity and low isg levels. these ms patients present a significant reduction of ms relapse upon ifn-β administration (150) . the underlying mechanisms are not yet completely unraveled. however, in the experimental autoimmune encephalitis mouse model of ms, th17 responses bear a major contribution to nervous system damages and are inhibited by the il-10 and il-27 induced upon ifn-i administration (151) . in summary, ifn-i responses can be deleterious in autoimmunity by promoting a vicious circle of reciprocal activation between innate immune cells and auto-reactive cd4 t or b lymphocytes. ifn-i responses can also be deleterious upon secondary bacterial or fungal infections in the lung or the kidneys occurring shortly after a primary viral infection, by compromising the recruitment of anti-microbial innate effector cells and/or by preventing the proper functional polarization of immune responses. we will now discuss how ifn-i responses can also compromise host immune defenses against certain viruses and promote chronic infections. different lcmv strains such as armstrong and clone-13 (cl13), respectively, lead to acute versus chronic infections in mice. a hallmark of chronic lcmv infection is the loss of the proliferative potential and effector functions of anti-viral cd8 t cells, a process called exhaustion. exhausted cd8 t cells are characterized by a high expression of the inhibitory receptors pd-1, ctla4, and lag-3 (152) . in vivo blockade of these inhibitory receptors can reverse t cell exhaustion and allow resolution of the chronic infection (152) . ifn-i and isgs are induced early after infection with all strains of lcmv, albeit to lower levels with those leading to chronic infection. this early ifn-i production is critical to limit viral replication (3). in models of acute infection, ifn-i responses rapidly return to normal, undetectable, levels, before viral replication is completely controlled. in contrast, isg induction is maintained in chronic infection, including the expression of pd-1 ligands on apcs and of the immunosuppressive il-10 cytokine, consistent with a prolonged expression of ifn-i albeit at low levels (13, 14) . in vivo neutralization of ifn-i by antibody administration promoted resolution of chronic lcmv cl13 infection, allowing the frontiers in immunology | microbial immunology restoration of functional anti-viral cd8 t cell responses at least in part through cd4 t cell-and ifn-γ-dependent mechanisms (13, 14) . during persistent lcmv cl13 infection, chronic low level ifn-i production polarizes cd4 t cell responses toward t follicular helper (tfh) rather than th1 functions. thus, chronic ifn-i responses promote enhanced anti-viral b cell responses but facilitate cd8 t cell exhaustion due to deficient cd4 t cell help, therefore contributing to host failure to prevent chronic infection (153) . strikingly, establishment of chronic infection by lcmv cl13 could also be prevented by early administration of two shots of a high dose of exogenous ifn-i, at days 2 and 5 post-lcmv inoculation. this treatment allowed viral clearance by rescuing anti-viral cd8 t cell from exhaustion (154) . altogether, these studies show that the timing and duration of ifn-i production during viral infections is critical in determining how this response will impact the balance between the virus and the host. an early and robust but transient production of ifn-i promotes strong induction of cell-intrinsic viral restriction mechanisms as well as adequate polarization of adaptive anti-viral immune responses, which combined effects lead to viral clearance. in contrast, if the production of ifn-i is too low and/or too late, both viral replication and low ifn-i responses become chronic, their combined action leading to induction of immunosuppressive effects and to inadequate functional polarization of cd4 t cells. this results in cd8 t cell exhaustion and maintenance of chronic infection. chronic viral replication and cd8 t cell exhaustion is also a hallmark of hiv-1 infection. we will now discuss the complex and disputed role of ifn-i in this disease. both in hiv-1 infection and in its most relevant animal model, infection of non-human primates with simian immunodeficiency virus (siv), disease progression after the acute phase of the infection is associated with high and chronic expression of isgs while ifn-i production is inconsistently detected (155) (156) (157) . in contrast, the individuals that do not progress toward disease despite persistent high viral loads show much lower immune activation, in particular low isg expression, after the acute phase of the infection (158) (159) (160) (161) . hence, chronic low levels of ifn-i are associated to disease progression independently of the level of viral replication. therefore, an outstanding question still open for a better understanding of the physiopathology of hiv-1 infection is whether chronic ifn-i responses are merely a marker of progression, or whether they are implicated in driving disease development. in addition to mechanisms similar to those uncovered in the mouse model of chronic lcmv infection, during hiv-1 infection other effects of ifn-i could promote a vicious circle of reciprocal activation between chronic viral replication and sustained, deleterious immune responses (figure 6 ). very early after hiv-1 infection, in most individuals, ifn-i production might be too weak or too late to induce a combination of cell-intrinsic defense mechanisms and of immune responses efficient enough to prevent later establishment of chronic infection. on the contrary, as demonstrated in the case of the mouse model of lcmv infection, ifn-i responses could favor cd8 t cell exhaustion, either by direct cell-intrinsic effects on cd8 t cells (figure 6 , ) or by contributing to deprive them from cd4 t cell help (figure 6, ) . several effects of ifn-i might compromise anti-hiv-1 th1 responses or more generally contribute to the global depletion of cd4 t cells. these mechanisms include functional polarization of anti-hiv-1 cd4 t cells toward tfh rather than th1 responses, cxcl10 production leading to enhance recruitment of memory cd4 t cells to the sites of viral replication where they fuel chronic viral replication with new hiv-1 target cells (figure 6, to ) , direct pro-apoptotic and anti-proliferative effects on cd4 t cells (figure 6 , ), as well as trail induction on pdcs licensing them for killing cd4 t cells irrespective of their infection (figure 6 , ) (162, 163) . altogether, these mechanisms entertain chronic viral replication and continuous depletion of cd4 t cells, leading to the dramatically enhanced susceptibility to opportunistic infections (figure 6 , ) characteristic of the acquired immunodeficiency syndrome (aids) (figure 6, ) . other lines of evidences have been reported to support a deleterious role of pdc activation during hiv-1 infection. women undergo faster hiv-1 disease progression than men with similar viral loads, which may result in part from the highest ifn-i production of women's pdcs including in response to hiv-1 stimulation (164) . pdc recruitment and activation in the vaginal mucosa of female macaques early after local siv inoculation contribute to attract and activate cd4 t cells, which can then be infected and promote virus dissemination from its portal of entry (165) . however, in vivo blockade of pdc ifn-α production by administration of tlr7/9-antagonistic oligonucleotides early after siv infection of macaques did not decrease t lymphocyte activation, which suggests that additional sources of ifn-i likely contribute to the immune dysfunction observed in siv/hiv-1 infections. targeting dysregulated ifn-i responses during hiv-1 infection might represent an interesting adjuvant therapeutic strategy to highly active antiretroviral treatments. administration of ifn-i in the non-pathogenic siv infection model of sooty mangabeys was not sufficient to switch it into a pathogenic model. no cd4 t cell depletion ensued, no hyperactivation of immune responses were observed. viral loads were even significantly decreased. however, this could be consistent with the positive impact of early and high dose ifn-i administration in chronic lcmv infection (154) . indeed, during the review process of this manuscript, it was reported that, early during primary siv infection in the pathogenic rhesus macaque model, a high dose injection of ifn-i was protective while neutralization of endogenous ifn-i was deleterious. in contrast, in the same animal model, prolonged ifn-i administration accelerated disease development in the chronic stage of the infection (166) . in mice with a humanized immune system, pdc depletion strongly decreased isg induction and enhanced viral replication both in the acute and chronic phases of hiv-1 infection. however, pdc depletion during chronic infection decreased infection-induced t cell apoptosis and increased t cell numbers in lymphoid organs (167) . these results further emphasize the dual role of ifn-i and pdcs in the physiopathology of hiv-1 infection. a strong and transient production of ifn-i early after infection benefits the host by lowering the set-point of viral replication during chronic infection. sustained production of low levels of ifn-i during chronic infection contributes to immune dysregulation and cd4 t cell depletion. further studies will be necessary to examine whether complementing standard-of-use antiretroviral drugs with pdc www.frontiersin.org depletion, ifn-i neutralization, or selective inhibition of t cell responses to ifn-i could yield additional benefits to chemotherapy in non-human primates during chronic siv infection. ifn-i administration has been used for many years to treat another human chronic viral disease, hcv infection. roughly, half of the patients do not show sustained virological responses (svr). the treatment causes severe side effects in many individuals. new chemotherapeutic drugs very potent at blocking hcv replication in vivo have recently become available. hence, whether ifn-i administration still constitutes a viable treatment against chronic hcv infection is being questioned (168, 169) . we will now discuss this issue. chronic hcv infection is the main cause of liver cirrhosis and hepatocellular carcinoma. there is currently no vaccine against hcv. the most common therapy for chronic hcv patients is the administration of recombinant pegylated ifn-α (peg-ifn-α) combined with the anti-viral drug ribavirin. however, because of ifnar pleiotropic expression, ifn-α administration induces severe side effects including flu-like syndrome, fever, fatigue, myalgia, and nervous depression ( figure 7a ) (170) . moreover, only about half of treated patients harbor svr (171) . prior-totreatment high hepatic isg expression is a negative predictor of svr upon peg-ifn-α therapy. high isg expression in untreated patients likely results from chronic but low ifn-i production triggered by persistent hcv replication. indeed, hepatocytes from non-responder patients were found to be infected at a greater frequency and to exhibit dampened antiviral and cell death responses (172) . what the cellular sources of ifn-i production are and why they persist only in non-responder patients still remain to be established. in chronic hcv infection, cytotoxic effector lymphocytes may contribute to the development of hepatocarcinoma by causing low level but sustained hepatocyte death and renewal. in contrast, local production of ifn-γ in the liver by nk and t lymphocytes could promote resistance to disease through non-cytolytic control of viral replication. as discussed previously for lcmv and hiv-1, low chronic production of endogenous ifn-i in hcv patients could compromise both innate and adaptive anti-viral immune responses. chronic exposure to ifn-i could dampen the ability of frontiers in immunology | microbial immunology utr of ifnl3 mrna to promote their degradation. the favorable ifnl3 allele associated with responsiveness to peg-ifn-α treatment may allow endogenous expression of sufficient levels of ifnl3 for efficient induction of cell-intrinsic anti-viral defenses in hepatocytes. this process is, however, hampered by the limited expression of the receptor for this cytokine (ifnλr1) in these patients. peg-ifn-α treatment might promote resolution of the infection by inducing ifnλr1 in these patients, potentiating their response to their endogenous production of ifnl3. in the patients that do not respond to peg-ifn-α treatment, endogenous levels of ifnl3 are insufficient for efficient induction of cell-intrinsic anti-viral defenses in hepatocytes, due to the degradation of the corresponding mrna in infected hepatocytes. in these patient's hepatocytes, however, ifnλr1 is already expressed to high levels prior to treatment due to their high endogenous ifn-i responses. administration of exogenous ifn-λ might cure these patients. see main text for further details. nk and cd8 t cells to produce ifn-γ (173, 174) and promote cd8 t cell exhaustion (175) . it could also induce an antagonist form of cxcl10, a chemokine required for recruitment to the liver of anti-viral nk and cd8 t cell effectors (176) . it may also polarize monocytes toward immunosuppressive functions (177) . therefore, better understanding ifn-i effects in hcv infection is critical to improve care of both responders and non-responder patients to peg-ifn-α. for responder patients, the issue is to modify the treatment to favor beneficial antiviral and immunoactivating effects over side effects strongly affecting patient's quality of life (figure 7a ). this might be achieved by specific delivery of ifn-i to targeted cell types as discussed later. for non-responder www.frontiersin.org patients, the issue is to understand the mechanisms underlying treatment failure to determine whether alternative therapies could be designed (figure 7a) . genome-wide association studies identified various single nucleotide polymorphisms (snp) in the gene encoding il-28b/ifn-λ3, one of the ifn-iii, as well in its 5 and 3 non-coding regions (178) (179) (180) (181) . one snp, called rs12979860, is located 3 kb upstream of the ifnl3 gene. patients harboring the cc genotype have a favorable prognosis to ifn-i treatment. patients with the tt genotype are at high risk of treatment failure (178, 179) . in europeans, the favorable cc genotype is the major, most common, ifnl3 allele. the unfavorable tt snp is the minor allele. the frequency of these alleles is reversed in africans. the favorable allele allows escape of ifnl3 mrna from degradation by cellular microrna induced upon hcv infection (181) . until recently, ifnl3 genotypes and hepatic isg expression were considered as independent predictors of response to peg-ifn-α treatment in hcv patients (171) . here, we propose a potential explanation, which integrates both factors in a relatively simple model ( figure 7b ). our main hypothesis is that efficient control of hcv infection depends on hepatocyte response to ifn-λ rather than ifn-α. this is supported by reports that ifn-λ induces a stronger and more sustained isg expression in hepatocyte cell lines in vitro (182) , and that polyi:c-induced control of hcv replication in humanized liver in chimeric mice is correlated to the induction of ifn-λ but not ifn-i in human hepatocytes (183) . responder patients harboring the favorable ifnl3 allele preventing the degradation of the corresponding rna in infected cells might express significant levels of endogenous ifn-λ3, although this is disputed. however, they express only low levels of ifn-λr1, which limits ifnλ3 efficiency ( figure 7b ) (184) . how these patients benefit from peg-ifn-α treatment could be that it induces ifn-λr1 expression on hepatocytes thus boosting endogenous ifn-λ3 effects (184) . in contrast, high isg-expressing non-responder patients harboring the unfavorable ifnl3 allele might not express enough ifn-λ3 for virus control. however, they do express ifn-λr1 as a result of their endogenous production of ifn-i. hence, peg-ifn-α might be ineffective in these patients because they already express ifn-λr1 but fail to produce endogenous ifn-λ3 due to the degradation of its mrna in infected hepatocytes (figure 7b) . these patients may be good candidates for peg-ifn-λ therapy, currently undergoing clinical development. since the expression of ifn-λr1 is mainly restricted to epithelial cells, melanocytes, and hepatocytes, some of the side effects related to ifn-i treatment might be strongly attenuated in peg-ifn-λ therapy. however, as ifn-i are key to induce anti-viral immune responses, it will be critical to determine whether, beside viral clearance, peg-ifn-λ therapy can also induce long-term immune protection against hcv. ifn-i transduce intracellular signals through a single receptor, ifnar, but via a multitude of downstream signaling pathways. the janus activated kinase (jak)/stat pathway was the first to be identified (185) . ifnar is composed of two distinct subunits, ifnar1 and ifnar2, which are constitutively associated with members of the jak family, tyrosine kinase 2 (tyk2) and jak1, respectively (186) . the binding of ifn-i to their receptor leads to the phosphorylation of jak1 and tyk2, which in turn induce the phosphorylation and activation of the stat proteins (186) . different stat complexes can form upon triggering of ifnar (figure 8) . a transcriptional complex that forms in most conditions of ifn-i stimulation and induces the expression of many molecules of cell-intrinsic anti-viral immunity is interferonstimulated gene factor 3 (isgf3), a heterotrimer composed of pstat1, pstat2, and irf9 (187) (figure 8) . following its translocation into the nucleus, isgf3 binds to isre regulatory sequences in target genes. many molecules playing a key role in the function of innate or adaptive immune leukocytes are also induced by isgf3, including cd80, cd86, or il-15 in dc, and granzyme b in nk cells. isgf3 is generally composed of stat1 phosphorylated on tyr701 and ser727 and of stat2 phosphorylated on tyr689. however, alternative isgf3 complexes have been described in various contexts which could participate to the diversity of ifn-i effects (188) . the pstat1 homodimer also plays a prominent role in cell-intrinsic ifn-i-dependent gene induction. it binds ifnγactivated sequences (gas) and controls the expression of many pro-inflammatory molecules (187) . pstat1 homodimers can form upon stimulation with either ifn-i or ifn-γ. many gasregulated genes can be induced by either cytokines. depending on cell types, jak signaling downstream of ifnar can lead to the activation of virtually all stat proteins and to their combinatorial association into a variety of complexes with different affinities for specific gas elements (189) (190) (191) (figure 8) . this diversity contributes to ifn-i induction of different transcriptional programs in distinct cell types (39) . stat complex formation depends in part on the relative abundance of stat molecules in the cell (192) . while stat1, stat2, stat3, and stat5 can be activated in most cell populations, stat4 and stat6 are mainly activated in lymphocytes (193) . for example, quiescent nk cells express more stat4 than stat1, leading to constitutive association of ifnar to stat4 in these cells. hence, quiescent nk cells mount pstat4 homodimer-dependent responses to ifn-i stimulation, including ifn-γ production and t-bet-driven proliferation (figure 8 ) (194, 195) . changes in stat levels can also occur upon the differentiation/activation of a given cell type and lead to a shift in its functional response to the cytokines (196) . upon activation, nk cells decrease their expression of stat4 and increase that of stat1, shifting their ifn-i response from stat4-dependent in a quiescent state to stat1dependent in pre-activated cells. this translates into opposite ifn-i effects on ifn-γ production and proliferation for quiescent versus pre-activated nk cells (194) . however, this outcome can be modulated by simultaneous exposure to other cytokines such as il-15 or il-12/18. a reverse stat1-to-stat4 shift occurs in dc during their maturation, shifting their functional responses from inhibition to activation of il-12 production in response to combined stimulations with ifn-i and cd40l (197) . this frontiers in immunology | microbial immunology ifn-i binding to ifnar triggers the phosphorylation of tyk2 and jak1, which in turn phosphorylate a variety of stat proteins. activated stats are able to form complexes, as homo-or hetero-dimers. the heterodimer stat1-stat2 binds to a third partner, ifn-regulatory factor 9 (irf9), in order to form the isgf3 complex. this complex translocates into the nucleus and binds to specific regulatory sequences, ifn-stimulated response elements (isre), to activate the expression of many interferon-stimulated genes (isgs). in particular, isgf3 induces most, if not all, of the isgs encoding effector molecules of cell-intrinsic anti-viral defenses such as oas or mx1. alternative jak/stat pathways include the formation of stat1 or stat4 homodimers, which may drive different functional responses to ifn-i. stat1 homodimers bind to ifnγ-activated sequences (gas) in the promoter of certain isgs, which may promote inflammatory, anti-proliferative, and pro-apoptotic responses. stat4 homodimers also bind to gas but promote ifn-γ production and pro-proliferative responses. enables mature dc to efficiently activate cd8 t cells. other yet unknown mechanisms control the formation of different stat complexes in distinct cell types. the nature and dynamics of the signaling pathways triggered by ifn-α or -β were evaluated in bulk cultures of human blood leukocytes using flow cytometry (191) or high throughput mass cytometry (190) . a diversity of phosphorylation patterns of stat1/3/5 was observed upon ifn-i stimulation. ifn-α activation induced phosphorylation of stat1, stat3, and stat5 in most cell types, peaking at 15 min (190) . ifn-β-induced stat1 phosphorylation was found to be poor in b cells as compared to monocytes and t cells (191) . however, the underlying mechanism remains to be identified since b cells did not express lower amount of ifnar2 or stat1 or enhanced levels of the inhibitory socs1 molecule. the high stat1 activation in monocytes led to their induction of ifn-i-dependent pro-apoptotic genes while this was not the case in b cells. these results strikingly differ from those obtained in the other study upon ifn-α stimulation, where stat1 phosphorylation was on the contrary lower in cd14 + monocytes and was prolonged in b cells and nk cells (190) . the differences between these two studies might have resulted from the use of different subsets and doses of ifn-i. in any case, both studies consistently reported that cd4 t cells showed the highest activation of stat5. all cd4 t cells but not all cd8 t cells activated stat5 and for a longer time (190) . ifn-β activation of stat3 was delayed in cd4 t cells and b cells as compared to cd8 t cells and monocytes (191) . different stat complexes may lead to distinct transcriptional programs linked to different biological functions (figure 8) . more systematic studies are needed to understand this complexity. besides changing stat levels between cell types or www.frontiersin.org activation states, the processes controlling differential formation of stat complexes downstream of ifnar triggering remain to be identified. in addition to jak/stat signaling, other pathways can be activated downstream of ifnar, including those involving the phosphatidylinositol 3-kinase (pi3k), mitogen-activated protein kinases (mapk), and the crk adaptor molecules (39, 198) . this leads to the activation of other transcription factors such as irf, nf-κb, or pu.1, which contribute to orchestrate cell responses to the cytokines by regulating both distinct and overlapping sets of genes as compared to stat (199, 200) . in summary, ifnar signals through a remarkable diversity of pathways, including but not limited to diverse combinations and kinetics of stat phosphorylations. this explains at least in part the diversity of ifn-i effects, including their induction of opposite responses depending on the physiopathological contexts and/or the nature of the principal responding cell types (200, 201) . ifn-iii induce the same signaling pathways as ifn-i, although they engage a different heterodimeric receptor, composed of the il-28ra and il-10rb chains and preferentially expressed on epithelial cells including hepatocytes. in mice and human beings, numerous ifn-i subtypes exist. functional and population genetic analyses showed that these ifn-i subtypes significantly differ in their functions (202) (203) (204) (205) (206) (207) . hence, one of most extraordinary feature of ifn-i biology is how ifn-i subtypes can elicit so many pleiotropic and diverse functions by interacting with the same receptor complex (208) . both ifnar1 and ifnar2 are required for the initiation of ifn-i-dependent signals, as mice deficient in either one are highly susceptible to viral infections (3, 5) . the assembling of the ifnreceptor ternary complex is a two-step process. first, a binary complex is formed by the binding of one side of the ifn molecule to ifnar2. then, a single binary complex interacts with ifnar1 via the other side of the ifn molecule. the stability of the ternary complex will be determined in part by the association and dissociation kinetics between the cytokine and the two receptor chains, as well as by ifnar expression levels since the cell surface concentrations of the receptor subunits are relatively low. hence, both the affinity of ifn-i subsets for ifnar and the amounts of ifn-i, ifnar1, and ifnar2 will regulate their biological effects ( figure 9a ) (209, 210) . cell membrane density of ifnar1 and ifnar2 is also involved in differential ifn-β-versus ifn-α-induced functional activities, such as anti-proliferative function (211) . a variety of cell-intrinsic parameters can also impact the lifetime of the ifn-receptor ternary complex, such as the rate of endocytosis/degradation/recycling of signaling complexes, and negative isg regulators such as usp18 that decrease the affinity of ifn-ifnar1 binding (203, 212) . based on a definition of a prototypic cytokine-receptor binding module and by analogy with the epo receptor system, ifn-i subtypes were originally postulated to form ternary complexes of differing architectures, resulting in distinct geometry and assembling of intracellular signaling components (213) . experimental evidence rejected this hypothesis. rather, the differential activities of ifn-i subtypes are determined by the stability of the ligand/receptor ternary complex (207, 212) . differential affinities of the ifn-i subtypes for ifnar1 and ifnar2 extracellular domains generate subtype-specific signaling cascades and biological outcomes ( figure 9a ) (210, 214) . crystal structure of ternary ifn-i/ifnar1/ifnar2 complex illuminated the biochemical complexity of ifn-i interaction with their cognate receptors (215) . the main conformational features of ifn-i/ifnar1/ifnar2 ternary complexes are conserved among the different ifn-i, but are quite different from the other cytokine receptors (214, 215) . in the formation of the binary ifn-i/ifnar2 complex, ifn-i ligand discrimination resides on differential energetics during the interaction of anchor points with ifnar2, shared by all ifn-i, as well as on key amino acid substitution among ifn-i subtypes (215) . ifnar1 then performs major conformational changes to interact with ifn-i associated in the binary complex, thus displaying an optimized functional plasticity (215) . these differences in the chemistry of ifn-i subtype interaction with ifnar2 and ifnar1 thus explain the different affinities of ifn-α versus ifn-β within ternary complex and their differential activities (210) . the functions regulated by ifn-i strongly depend on the main responding cell types ( figure 9b ). this has been studied in vitro by examining the functional consequences of the stimulation of different cell types with ifn-i, and in vivo by determining the contribution of cell-intrinsic ifn-i responses of different cell types to resistance or susceptibility to various diseases. an emerging concept is the central role of dc responses to ifn-i for induction of protective immunity against viral infections or tumors (figure 3) . the development of mutant mice allowing conditional genetic inactivation of ifnar1 in a cell-type specific manner using the cre-lox system (216) has been instrumental in accelerating our understanding of how different cell types respond to ifn-i in vivo and what their respective contribution is to protective or deleterious ifn-i responses. this has been investigated most extensively in viral infections (106, 111, 112, 115, 217) but also in cancer (97, 98) , bacterial infections (218), autoimmunity (216, 219) , sepsis (220), or inflammatory diseases (221) . efforts are being pursued to better understand which cell types respond to ifn-i in a manner promoting protective versus deleterious effects in different physiopathological settings. that knowledge will considerably help to develop novel strategies to modulate ifn-i functions for promoting health over disease. the development of mutant mice allowing conditional genetic inactivation of stat1, stat3, and stat5 (222-226) will help better understanding how different signaling pathways in different cell types determine the outcome of ifn-i response in vivo in various conditions. this knowledge might lead to the development of strategies aiming at targeting a given cell type with a specific subset of ifn-i, or in the presence of antagonists of certain signaling pathways, to surgically tune ifn-i responses in vivo toward the most desirable outcome. frontiers in immunology | microbial immunology for example, the affinity of ifn-β for ifnar1 is 100-times higher than that of ifn-α2, and ifnβ is much more potent in inhibiting cellular proliferation or (continued ) ifn-i can also determine distinct functional outcomes. for example, during viral infections, early and transient high levels of ifn-i promote protective dc and t cell responses, while delayed, chronic and low level ifn-i production compromises host immune defenses and promotes chronic viral infections. within a given cell type, the outcome of ifn-i stimulation also depends on time of exposure to these cytokines relative to other modulatory signals (timing relative to other stimuli). for example, in naïve cd8 t cells, tcr signaling prior to ifn-i stimulation leads to increased expression of stat4 and promotes ifn-γ production and proliferation, while ifn-i stimulation prior to tcr triggering leads to stat1-dependent anti-proliferative and pro-apoptotic effects. the formation of specific stat complexes is a highly dynamic process. it depends not only on the cell type but also on its specific state at the time it sees ifn-i. hence, major parameters controlling the effects of ifn-i in a given cell type also include its microenvironment ( figure 9c ) and the timing of its exposure to the cytokines both in terms of duration of the stimulation and of previous activation history ( figure 9d) . the tam receptor ligand gas6 is expressed within tumor cells in various solid cancers (227, 228) . elevated gas6 expression is of bad prognosis in different cancers (228, 229) . in a mouse model of ovarian cancer, early during tumorigenesis tumor-infiltrating dcs were found to be immunogenic and promote antitumor immunity, but they were later altered in the course of tumor development to acquire immunosuppressive properties beneficial to the tumor (230) . one may thus hypothesize that expression of tam soluble ligands in certain tumors and of tam receptors on tumor-infiltrating dcs might contribute to dampen dc response to ifn-i and therefore facilitate their polarization by the tumor microenvironment into immunosuppressive cells (figure 9c) . acute versus chronic exposure to ifn-i can lead to strikingly opposite effects on a given cell type (13, 14, 231) . in addition to duration, the time when a cell is exposed to ifn-i can also dramatically impact its functional response, depending on its previous activation history ( figure 9d) . in vitro stimulation of dcs with ifn-β can lead to opposite outcomes depending whether it occurs simultaneously to, or after, tnfα-induced maturation. ifn-β polarizes dcs toward th1 induction in the former case, and toward il-10-secreting t cells in the latter case. these opposite effects result at least in part from the differential expression of il-12/18 by dcs (232) . similarly, ifn-i effect on the functional polarization of cd4 t cells is strongly modulated by the other cytokines present in the lymphocyte microenvironment at the same time (233) . ifn-i can also mediate opposite effects on cd8 t cells depending whether it occurs before or after cognate engagement of the t cell receptor. indeed, while cd8 t cells have the potential to respond to ifn-i by inducing both stat1-and stat4-dependent genes, this depends upon their activation history. naïve cd8 t cells respond mostly to ifn-i through stat1 signaling, leading to the inhibition of their proliferation and eventually to the induction of their apoptosis. however, cognate triggering of the t cell receptor causes a decrease in stat1 and an increase in stat4 expression in cd8 t cells. this leads to a shift of their ifn-i response from stat1-to-stat4 signaling, resulting in the promotion of their proliferation and ifn-γ production. during lcmv infection, this mechanism promotes stat4-dependant expansion of anti-viral cd8 t cells, but stat1-dependant inhibition of naïve cd8 t cell proliferation (234) . since the late 70s the clinical potential of ifn-i for the treatment of patients suffering of viral infection or cancer diseases has been widely acknowledged (235) . today, this expectation is tempered because ifn-i treatment can induce severe side effects and sufficient doses cannot be administered in patients. therefore, there is a strong need to create tuned ifn molecules devoid of side effects. based on our current understanding of ifn-i responses as reviewed above, many parameters could be tuned individually or in a combined manner to modulate ifn-i activity to promote their beneficial effects over the deleterious ones in a number of diseases. these parameters include modifying the affinity of ifn-i for its receptor, playing with the local quantity/concentration of ifn-i and with the duration of its delivery, and modulating the nature of the cells that are responding to ifn-i. we will discuss here novel strategies being developed to deliver ifn-i to, or block ifn-i responsiveness of, a specific target cell type in vivo (figure 10 ). if ifn-i-induced side effects are a consequence of the pleiotropic nature of ifn-i, and if the bioactivities mediating deleterious effects have some degree of independence from those mediating beneficial effects, one could mutate the ifn-i molecules in order to skew their activity toward a desired bioactivity. indeed, introducing key mutation in ifn-α2 allowed increasing its affinity to ifnar1 by a factor of 100. accordingly, this ifn-α2 mutant is 100times more potent in inhibiting cell proliferation, but as potent as wt ifn-α2 in inducing an anti-viral state (236) (237) (238) . hence, it is possible to tune ifn activity by modifying its binding to ifnar. however, translating such an approach for the design of molecules for clinical application is severely hampered by the poor understanding we have on the ifn-i bioactivities mediating the side effects. furthermore, we are far from having established the list of bioactivities that could be differentially modulated by changing the stability of the ifn-i/ifnar complex. we know more about the frontiers in immunology | microbial immunology cell types that mediate beneficial versus deleterious ifn responses in various diseases. hence, we will now discuss strategies aimed at focusing ifn activity to specific cell types to promote health over disease. several strategies have been developed to specifically target ifns on tumor cells, tumor-infiltrated immune cells or infected tissues. these strategies include intra-lesional injection (239, 240) , adenoviral-mediated gene transfer (241) (242) (243) , engineered tumorinfiltrating monocytes (244) , and fusion of ifns with a cleavable protecting shell (245) . another strategy to increase cytokine accumulation within the tumor or infected tissue is antibody-mediated targeting of cytokine delivery, where a cytokine moiety is fused to an antibody directed against a specific cell surface marker (figure 10) . the fusion molecule retains both antigen-binding and ifn-i bioactivities, and is enriched at the targeted site upon in vivo injection (246) (247) (248) (249) . when targeted to human cd20, ifn-i inhibited the proliferation of lymphoma cells engrafted in immunodeficient mice (250) . an ifn-i targeted to a tumor antigen can also amplify the therapeutic effect of the antibody by acting on tumor-infiltrated dcs, thus increasing antigen cross-presentation and antitumor cytotoxic t cell responses (249) . on non-targeted cells, the antibody conjugation negatively impacts ifn-i potency, but only modestly (18, 248, 251) (figure 10a) . fusion molecules generally retain full ifn-i biological activity on the cells expressing the antibody target ( figure 10b) . hence, this difference only leads to a modest ratio between the ifn-i specific activity measured on target and non-target cells (figure 10b) . such a targeting efficiency is definitely too low to reduce the toxic effect of ifn-i administration, because it will not specifically focus ifn-i activities on "beneficial cells" without stimulating "deleterious cells." the engineering of immuno-ifn-i must be improved to reach the very high targeting efficacy required to significantly diminish the treatment side effects. we recently reported an innovative strategy reaching this goal (18) . it is based on the postulate that the antibody moiety of an immuno-ifn-i stabilizes the ifn-i/receptor-complex by avidity. it also takes into account the fact that the biological potency of an ifn-i is proportional to the stability of the ifn-i/receptor complex up to a certain threshold beyond which increasing the stability does not increase its potency (238, 252) . ifn-α2 and ifn-β are used in most immuno-ifn-i studies. they have evolved to retain close to maximal potency. hence, their targeting by an antibody that only provides a modest gain in terms of biological potency. however, it is expected that decreasing the affinity of the ifn-i for its receptor, by introducing a mutation, would increase the targeting effect of the antibody (figures 10 c,d) . this is indeed the case. using an ifn-i with a single point mutation that dramatically decreases its affinity for ifnar2 ( figure 10c ) allows engineering immuno-ifns that are up to 1000-fold more potent on cells expressing the antibody target ( figure 10d) . the three log targeting efficiency of these novel types of immuno-ifns is found for various activities measured in vitro or in vivo when delivered in mice. if the toxic side effect experienced by the patients treated with ifn-i is due to systemic ifn-i activity, this targeting technology may find considerable clinical applications since such engineered immuno-ifns are virtually inactive while "en route" and are activated only after binding of the fused antibody to the desired target. it remains to define the useful targets according to pathologies, for example, tumor cells themselves and professional cross-presenting xcr1 + dcs for cancer (97, 98, 249) , or hepatocytes for chronic hcv infection. to treat autoimmune diseases, novel therapeutics targeting ifn-i have been developed, including two ifn-α-neutralizing monoclonal antibodies currently in clinical trials (sifalimumab and rontalizumab) (253, 254) . however, long-term systemic neutralization of ifn-i activity may increase susceptibility to viral infection and tumor development. alternative strategies are needed to specifically inhibit ifn-i deleterious effects in these diseases without globally compromising ifn-i anti-viral and www.frontiersin.org anti-tumoral functions. the sequential nature of the assembling of the ifn-i/receptor complex opens the possibility to design ifn-i antagonists specifically targeting the cell subsets responsible for ifn-i deleterious effects. an ifn-α2 carrying a single amino acid substitution that blocks the ifn-i/ifnar1 interaction engages ifnar2 in a complex, which cannot bind ifnar1 (255) . since the binary ifn-i/ifnar2 complex is devoid of any ifn-i activity, such mutant behaves as a potent ifn-i antagonist. when linked to an antibody specific for a cell surface marker, the antagonistic activity of the mutant ifn-i should be significantly reinforced specifically on the cells expressing the target. hence, it should be possible to design and construct targeted antagonists that inhibit responsiveness to endogenous ifn-i specifically on the cell subsets on which the cytokines act to promote autoimmunity or severe side effects, leaving the other cells fully responsive. for example, in chronic hcv patients treated with peg-ifn-α, one of the most deleterious side effects is nervous depression, which might be prevented by co-administration of an ifn-i antagonist specifically targeting neurons or other cells of the central nervous system. in the last decade, several major technological breakthroughs and the generation of novel animal models have remarkably advanced our understanding of the mode of action of ifns. in vitro high throughput screening allowed systematically studying the functions of isgs by ectopic expression or knock-down. advance biophysical investigation of the interactions between ifn-i and the ifn-i receptor allowed to rigorously investigate the mechanistic basis for the differential bioactivities of ifn-i subtypes. the analyses of the responses of different cell types to ifns or to viral infection, in vitro but also in vivo in various pathologies, demonstrated that ifn-i often mediate beneficial versus deleterious roles by acting on different cell types. from integrative analysis of these data, a picture is now emerging suggesting that it will be possible to segregate protective from deleterious ifn-i effects, based (i) on their differential induction depending on ifn-i subsets or on the magnitude/timing of ifn-i production, (ii) on their conditioning in different tissues, (iii) or on their occurrence in different cell types. hence, innovative immunotherapeutic treatments are being designed to tune ifn-i activity toward desired effects in order to promote health over disease in a manner adapted to each physiopathological condition. in particular, a proof-of-concept has been made in vitro that it will be possible to target ifn-i activity on given cell types or tissues to administer to patients sufficiently high doses of the cytokine at the site of interest while limiting unwanted effects in other tissues or cell types. the next steps will be to demonstrate efficacy of this strategy in vivo in preclinical 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infection of natural hosts from pathogenic siv infection of rhesus macaques comparative transcriptomics of extreme phenotypes of human hiv-1 infection and siv infection in sooty mangabey and rhesus macaque hiv turns plasmacytoid dendritic cells (pdc) into trail-expressing killer pdc and down-regulates hiv coreceptors by toll-like receptor 7-induced ifn-alpha plasmacytoid dendritic cells express trail and induce cd4+ t-cell apoptosis in hiv-1 viremic patients sex differences in the toll-like receptor-mediated response of plasmacytoid dendritic cells to hiv-1 glycerol monolaurate prevents mucosal siv transmission type i interferon responses in rhesus macaques prevent siv infection and slow disease progression plasmacytoid dendritic cells suppress hiv-1 replication but contribute to hiv-1 induced immunopathogenesis in humanized mice chronic hepatitis c: future treatment host-targeting agents in the treatment of hepatitis c: a beginning and an end? the interferons: 50 years after their discovery, there is much more to learn immune responses to hcv and other hepatitis viruses interferon lambda alleles predict innate antiviral immune responses and hepatitis c virus permissiveness altered interferon-alpha-signaling in natural killer cells from patients with chronic hepatitis c virus infection natural killer cells are polarized toward cytotoxicity in chronic hepatitis c in an interferon-alfa-dependent manner coexpression of pd-1, 2b4, cd160 and klrg1 on exhausted hcv-specific cd8+ t cells is linked to antigen recognition and t cell differentiation evidence for an antagonist form of the chemokine cxcl10 in patients chronically infected with hcv monocyte activation by interferon alpha is associated with failure to achieve a sustained virologic response after treatment for hepatitis c virus infection genetic variation in il28b and spontaneous clearance of hepatitis c virus genetic variation in il28b predicts hepatitis c treatment-induced viral clearance a variant upstream of ifnl3 (il28b) creating a new interferon gene ifnl4 is associated with impaired clearance of hepatitis c virus the favorable ifnl3 genotype escapes mrna decay mediated by aurich elements and hepatitis c virus-induced micrornas distinct and overlapping genomic profiles and antiviral effects of interferon-lambda and -alpha on hcv-infected and noninfected hepatoma cells targeted induction of interferon-lambda in humanized chimeric mouse liver abrogates hepatotropic virus infection ifn-lambda receptor 1 expression is induced in chronic hepatitis c and correlates with the ifn-lambda3 genotype and with nonresponsiveness to ifn-alpha therapies how cells respond to interferons jak-stat pathways and transcriptional activation in response to ifns and other extracellular signaling proteins regulation of type i interferon responses stat2 and irf9: beyond isgf3. jakstat (2013) single-cell mass cytometry of differential immune and drug responses across a human hematopoietic continuum multiplexed mass cytometry profiling of cellular states perturbed by small-molecule regulators major differences in the responses of primary human leukocyte subsets to ifn-beta critical role for stat4 activation by type 1 interferons in the interferongamma response to viral infection immunomodulatory functions of type i interferons high basal stat4 balanced by stat1 induction to control type 1 interferon effects in natural killer cells type 1 interferon induction of natural killer cell gamma interferon production for defense during lymphocytic choriomeningitis virus infection changing partners at the dance: variations in stat concentrations for shaping cytokine function and immune responses to viral infections dendritic-cell maturation alters intracellular signaling networks, enabling differential effects of ifn-alpha/beta on antigen cross-presentation mechanisms of type-i-and type-ii-interferon-mediated signalling type i interferon [corrected] gene induction by the interferon regulatory factor family of transcription factors complex modulation of cell type-specific signaling in response to type i interferons alternate interferon signaling pathways ifn-beta induces serine phosphorylation of stat-1 in ewing's sarcoma cells and mediates apoptosis via induction of irf-1 and activation of caspase-7 usp18-based negative feedback control is induced by type i and type iii interferons and specifically inactivates interferon alpha response interferon-alpha and -beta differentially regulate osteoclastogenesis: role of differential induction of chemokine cxcl11 expression differential activity of type i interferon subtypes for dendritic cell differentiation evolutionary genetic dissection of human interferons the receptor of the type i interferon family interferons as biomarkers and effectors: lessons learned from animal models protection against progressive leishmaniasis by ifn-beta multifaceted activities of type i interferon are revealed by a receptor antagonist receptor density is key to the alpha2/beta interferon differential activities structural and dynamic determinants of type i interferon receptor assembly and their functional interpretation the type i interferon receptor: structure, function, and evolution of a family business differential receptor subunit affinities of type i interferons govern differential signal activation structural linkage between ligand discrimination and receptor activation by type i interferons distinct and nonredundant in vivo functions of ifnar on myeloid cells limit autoimmunity in the central nervous system type i interferons protect t cells against nk cell attack mediated by the activating receptor ncr1 lymphadenopathy in a novel mouse model of bartonella-induced cat scratch disease results from lymphocyte immigration and proliferation and is regulated by interferon-alpha/ beta cytosolic rig-i-like helicases act as negative regulators of sterile inflammation in the cns expression of type i interferon by splenic macrophages suppresses adaptive immunity during sepsis myeloid type i interferon signaling promotes atherosclerosis by stimulating macrophage recruitment to lesions stat3 activation is responsible for il-6-dependent t cell proliferation through preventing apoptosis: generation and characterization of t cell-specific stat3-deficient mice generation of mice with a conditional stat1 null allele conditional stat1 ablation reveals the importance of interferon signaling for immunity to listeria monocytogenes infection loss of stat1 from mouse mammary epithelium results in an increased neu-induced tumor burden inactivation of stat5 in mouse mammary epithelium during pregnancy reveals distinct functions in cell proliferation, survival, and differentiation meta-analysis of microarray data identifies gas6 expression as an independent predictor of poor survival in ovarian cancer axl and growth arrest-specific gene 6 are frequently overexpressed in human gliomas and predict poor prognosis in patients with glioblastoma multiforme gas6 expression identifies high-risk adult aml patients: potential implications for therapy ovarian cancer progression is controlled by phenotypic changes in dendritic cells ifnalpha activates dormant haematopoietic stem cells in vivo timing of ifn-beta exposure during human dendritic cell maturation and naive th cell stimulation has contrasting effects on th1 subset generation: a role for ifn-beta-mediated regulation of il-12 family cytokines and il-18 in naive th cell differentiation combinatorial flexibility of cytokine function during human t helper cell differentiation regulating type 1 ifn effects in cd8 t cells during viral infections: changing stat4 and stat1 expression for function interferons at age 50: past, current and future impact on biomedicine inquiring into the differential action of interferons (ifns): an ifn-alpha2 mutant with enhanced affinity to ifnar1 is functionally similar to ifn-beta an interferon alpha2 mutant optimized by phage display for ifnar1 binding confers specifically enhanced antitumor activities the stability of the ternary interferon-receptor complex rather than the affinity to the individual subunits dictates differential biological activities intra-lesional low-dose interferon alpha2a therapy for primary cutaneous marginal zone b-cell lymphoma intratumoral injection of interferon-alpha and systemic delivery of agonist anti-cd137 monoclonal antibodies synergize for immunotherapy delivery of interferon alpha using a novel cox2-controlled adenovirus for pancreatic cancer therapy the efficacy of radiotherapy relies upon induction of type i interferondependent innate and adaptive immunity a trial of intrapleural adenoviral-mediated interferon-alpha2b gene transfer for malignant pleural mesothelioma tumortargeted interferon-alpha delivery by tie2-expressing monocytes inhibits tumor growth and metastasis targeting cytokines to inflammation sites livertargeting of interferon-alpha with tissue-specific domain antibodies antibody-based targeting of interferon-alpha to the tumor neovasculature: a critical evaluation targeting ifn-alpha to b cell lymphoma by a tumor-specific antibody elicits potent antitumor activities targeting the tumor microenvironment with interferon-beta bridges innate and adaptive immune responses targeted delivery of interferon-alpha via fusion to anti-cd20 results in potent antitumor activity against b-cell lymphoma targeted delivery of interferon-alpha to hepatitis b virus-infected cells using t-cell receptor-like antibodies variations in the unstructured c-terminal tail of interferons contribute to differential receptor binding and biological activity safety and pharmacodynamics of rontalizumab in patients with systemic lupus erythematosus: results of a phase i, placebo-controlled, double-blind, dose-escalation study safety profile and clinical activity of sifalimumab, a fully human anti-interferon alpha monoclonal antibody, in systemic lupus erythematosus: a phase i, multicentre, double-blind randomised study mutation of the ifnar-1 receptor binding site of human ifn-alpha2 generates type i ifn competitive antagonists the studies performed in the laboratories are supported by funding from inserm, cnrs, aix-marseille university, the labex mabimprove, and the european community's seventh framework programme fp7/2007-2013 (grant agreement 223608 for gilles uzé, european research council starting grant agreement number 281225 for marc dalod including salary support to emeline pollet and thien-phong vu manh). we thank past and present laboratory members for their contribution to studies on dcs or ifns. we apologize for not quoting certain studies because of space limitations. the authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. key: cord-018595-x3tleomb authors: dodiuk-gad, roni p.; chung, wen-hung; shear, neil h. title: adverse medication reactions date: 2017-04-25 journal: clinical and basic immunodermatology doi: 10.1007/978-3-319-29785-9_25 sha: doc_id: 18595 cord_uid: x3tleomb cutaneous adverse drug reactions (adrs) are among the most frequent adverse reactions in patients receiving drug therapy. they have a broad spectrum of clinical manifestations, are caused by various drugs, and result from different pathophysiological mechanisms. hence, their diagnosis and management is challenging. severe cutaneous adrs comprise a group of diseases with major morbidity and mortality, reaching 30 % mortality rate in cases of toxic epidermal necrolysis. this chapter covers the terminology, epidemiology, pathogenesis and classification of cutaneous adr, describes the severe cutaneous adrs and the clinical and laboratory approach to the patient with cutaneous adr and presents the translation of laboratory-based discoveries on the genetic predisposition and pathogenesis of cutaneous adrs to clinical management guidelines. the world health organization defined an adverse drug reaction (adr) in 1972 as "a response to a drug that is noxious and unintended and occurs at doses normally used in man" [1] . edwards and aronson [2] proposed a different definition in 2000: "an appreciably harmful or unpleasant reaction, resulting from an intervention related to the use of a medicinal product, which predicts hazard from future administration and warrants prevention or specific treatment, or alteration of the dosage regimen, or withdrawal of the product." the terms 'adverse reaction' and 'adverse effect' are interchangeable, except that an adverse reaction is seen from the point of view of the patient and adverse effect is seen from the point of view of the drug. however, both terms must be distinguished from 'adverse event'. an adverse event is an adverse outcome that occurs while a patient is taking a drug, but is not or not necessarily attributable to it [2] . differentiating between serious adr and severe adr is imperative. serious adr is a legal term applied to any untoward medical occurrence that at any dose results in death, is life-threatening, requires inpatient hospitalization or prolongation of existing hospitalization, results in persistent or significant disability/incapacity, or is a congenital anomaly/birth defect [3] . conversely, the term 'severe' is a clinical term used to describe the intensity (severity) of a medical event, as in the grading 'mild', 'moderate', and 'severe'; thus, a severe skin reaction need not be serious [2] . adrs are associated with significant morbidity and mortality and have considerable economic implications. clinical manifestations of an adr are variable and may include cutaneous and or systemic features [4] . when analyzing the type of adrs most encountered, two major groups emerge; common-mild reactions and raresevere reactions. common-severe reactions are not approved for clinical usage and rare-mild reactions are usually not noticed or reported. cutaneous adrs are among the most frequent adverse reactions in patients receiving drug therapy [5] . they accounted for 65 % of all reported adrs in a 4-year retrospective study in taiwan [6] . the prevalence and incidence of cutaneous adrs vary greatly among different populations [7] [8] [9] [10] [11] . in the usa, a 7-year prospective study found that the prevalence of cutaneous adrs was 2.2 % in hospitalized patients [7] ; and an 11-year retrospective study found the annual incidence of cutaneous adrs to be 2.26 per 1,000 persons [11] . in denmark, in a 1-year cross-sectional study the prevalence of cutaneous adrs was 0.33 % in in-patients and 0.14 % in outpatients [8] . in southern china, in an 8-year retrospective study, the prevalence of cutaneous adrs was 0.14 % in hospitalized patients [9] . in india, in a 12-month prospective study, the primary incidence of cutaneous adrs was 2.05 per 1,000 persons [10] . the need to survey adrs in clinical practice is universally recognized. various methods may be employed: spontaneous surveillance, prescription-event monitoring (pem), linkage analysis, case-control surveillance and cohort studies [5] . in 1963, the 16th world health assembly reaffirmed the need for early detection and rapid dissemination of information on adverse reactions due to medications. this affirmation led to the creation of the world health organization (who) programme for international drug monitoring, under whose auspices systems have been created in member states for the collection and evaluation of individual case safety reports (icsrs) [12] . in 1978 the who set up its international drug monitoring programme in sweden at the uppsala monitoring centre (umc) http://www.who-umc. org. the us food and drug administration (fda) provides several options for reporting adverse events. one such option is medwatch, the fda safety information and adverse event reporting program http://www.fda.gov/safety/ medwatch/default.htm, founded in 1993 as a system for both consumers and healthcare professionals to report adverse events. medwatch is intended to detect safety hazard signals for medical products; in the event a signal is detected, the fda can issue medical product safety alerts or order product recalls, withdrawals, or labelling changes to protect the public health [13] . a number of international research groups are investigating severe cutaneous adrs (scars): the regiscar network, an international registry of scar established in 2003, the japanese research committee, j-scar, the asian scar consisting of japan and taiwan scar groups (j-scar and t-scar) established in 2010, and the southeast asia network, sea-scar, with ten member countries: brunei, cambodia, indonesia, laos, malaysia, myanmar, philippines, thailand, singapore, and vietnam. the international serious adverse event consortium (isaec), a non-profit organization formed in 2007, is a pharmaceutical industry-and fda-led international consortium that focuses on identifying and validating dna variants useful in predicting the risk of rare drug-induced serious adverse events [14] . mechanisms of adverse drug reactions (adrs) can be classified into immunologic and non-immunologic etiologies. there are two common types of immune-mediated drug reactions: immediate-type hypersensitivity (type i hypersensitivity) and delayed-type hypersensitivity (type iv hypersensitivity). 1. immediate-type drug hypersensitivity: immediate-type drug hypersensitivity reactions usually occur minutes to hours after drug exposure, with clinical manifestations including pruritus, urticaria, angioedema, and bronchospasm to anaphylaxis. the reaction is mediated mainly by drug-specific ige, the most common causative agents being penicillins, cephalosporins and neuromuscular blocking agents. ige-mediated reactions to drugs are usually thought to be an immune response to a hapten/carrier complex. in the primary drug sensitization, drug-specific ige is formed when plasma cells transformed from activated b cells interact with t cells. in an allergic reaction, drug allergens bind to mast cells with high-affinity fc receptor, to which drug-specific ige is bound, causing mast cells to release mediators, such as histamine, leukotrienes, prostaglandins and cytokines [15] . 2. delayed-type drug hypersensitivity: delayed-type drug hypersensitivity reactions usually take several days to weeks following drug exposure, with variable clinical presentations that may include maculopapular eruption (mpe), fixed drug eruption (fde), acute generalized exanthematous pustulosis (agep), stevens-johnson syndrome (sjs), toxic epidermal necrolysis (ten) and drug reaction with eosinophilia and systemic symptoms (dress). t cell receptor (tcr), cd4+ and cd8+ t cells are involved in different delayed-type drug hypersensitivity reactions [16] . drugs are low molecular weight and usually considered not able to bind to tcrs to activate adaptive immunity. in the case of drug allergy, drug interactions with tcrs may involve a drug-peptide complex presented by human leucocyte antigen (hla) molecules of antigen-presenting cells (apcs). this process is known as the hapten concept; an example is β-lactams that covalently bind to lysine residues [17] . drugs can also interact directly with tcrs without binding to the peptide/hla of the apc in what is known as the p-i concept (pharmacological interaction of drugs with immune receptors) [18] . for example, carbamazepine is not able to bind covalently to peptides or proteins, but can associate with low affinity to tcrs and provoke t cell activation [19] . the immunohistologic characteristics of delayed type drug hypersensitivity are summarized in table 25 .1. the skin of mpe is infiltrated by numerous mononuclear cells (cd4 and cd8 t cells, monocyte/macrophages) and some eosinophils. typically, interface dermatitis is seen with a predominance of cd4+ t cells. these cells are located mainly in the perivascular dermis, and both cd4+ and cd8+ t cells are located at the dermoepidermal junction [20] . skin manifestations of dress may vary from mpe-like to exfoliative dermatitis and are characterized by a heavy infiltration of cd4+ and cd8+ t cells, monocyte/macro-phages and eosinophils [21] . mpe and dress share many pathological features, but dress exhibits more severe dyskeratosis (keratinocyte death in epidermis) and a greater extent of systemic involvement and eosinophilia [26] . immunohistology of skin lesions in agep reveals intraepidermal pustules with infiltration of neutrophils surrounded by il-8 producing t cells [22] . despite very diverse clinical presentations, constant features of delayed-type drug hypersensitivity are the presence of high numbers of drug-specific cd8+ cytotoxic t cells and low numbers of innate nk lymphocytes [20, 27, 28] . cd8+ t cells of cutaneous adrs have classic cytotoxic functions: lysis of autologous lymphocytes or keratinocytes in an mhc class i-restricted and drug-dependent manner [28] . cytotoxic immune cells in sjs/ten drug-induced sjs and ten are severe cutaneous adrs in which cytotoxic t lymphocytes (ctls) and natural killer (nk) cells are activated, and subsequently carry out the cellular immune reactions directed at keratinocytes in a major histocompatibility class (mhc) i-restricted manner. upon activation of these immunocytes, various cytotoxic signals, including granulysin, perforin/granzyme b, fas/fas ligand, and cytokines/chemokines, are relayed to the skin lesions to mediate the disseminated keratinocyte death [23] [24] [25] . it is noteworthy that the number of granulysin-positive cells in fixed drug eruptions was found to be similar to that observed in sjs/ten [27] . non-immune-mediated hypersensitivity is commonly referred to as pseudoallergic reactions because they do not involve a specific immune mechanism -neither ige-mediated (type i) nor delayed (type iv) hypersensitivity. clinical manifestations, which range from milder erythematous to urticarial reactions to severe lethal anaphylaxis, may be indistinguishable from immune system-mediated hypersensitivity reactions. common non-immune-mediated hypersensitivity can be caused by contrast media, vancomycin, non-steroidal anti-inflammatory drugs (nsaids), opiates, plasma expanders, and drugs used in general anesthesia [29] . nsaids-induced pseudoallergic reactions have been attributed to cyclooxygenase-1 inhibition and overproduction of leukotrienes, and may require higher drug doses than are needed for true ige-mediated reactions [30] . mast cell drug-specific t cells mediate skin inflammation in variable clinical presentations of delayed-type drug hypersensitivity through the release and induction of different cytokines and chemokines (table 25 .1) [31] . the heterogeneous cytokines include th1 cytokines (interferon-γ) and th2 cytokines (il-4, il-5) [22] . increased expression of il-5, which is a key cytokine for activation of eosinophils, is commonly seen in delayed-type drug hypersensitivity [32] . the activation of eosinophils can be further enhanced by the chemokines eotaxin and rantes [33] . thymus and activation-regulated chemokine (tarc/ccl17) has been reported to be a dress specific cytokine [34] . in addition to th1 and th2 cytokines, a recent study demonstrated the involvement of il-17aproducing th17 in dress and sjs/ten [35] . elevated expression of the neutrophil-attracting il-8 has been known to be the key cytokine involved in agep. there are several cytokines involved in sjs/ ten. numerous studies have shown tumor necrosis factor alpha (tnf-α) strongly expressed in sjs/ten lesions and correlated with disease severity [24, 36, 37] . tnf-α is a potent cytokine that induces cell apoptosis, cell activation, differentiation, and inflammatory processes [38, 39] . interferon gamma (ifn-γ) is a common cytokine involved in delayed-type drug hypersensitivity, including sjs/ ten. ifn-γ was intensely expressed in the superficial dermis and epidermis of sjs/ten lesions [36, 37] . ifn-γ is also known to promote antigen presentation and thus stimulate the cell-mediated immunity by upregulation of mhc molecules [40] [41] [42] . in addition to tnf-α and ifn-γ, several cytokines and chemokine receptors that are responsible for trafficking, proliferation, and activation of t-cells and other immune cells have been found elevated in the skin lesions, blister fluids, blister cells, pbmcs, or plasma of sjs/ten patients . these cytokines/chemokines include il-2, il-5, il-6, il-10, il-12, il-13, il-15, il-18, ccr3, cxcr3, cxcr4, and ccr10 [24, 36, 37, [43] [44] [45] . the central hypothesis proposed to explain the severe mucocutaneous lesions of sjs/ten is the cd8+ cytotoxic t cell and natural killer (nk) cell-mediated cytotoxic immune reactions. three major cytotoxic signals from cytotoxic cells are reported to be involved in the extensive skin necrosis of sjs/ten, including the fas-fasl interaction, perforin/granzyme b, and granulysin, which can induce keratinocyte apoptosis [23, 28, 46] . granulysin is not only a cytotoxic protein; it is also a chemoattractant and proinflammatory activator that can promote monocyte expression of ccl20 [47] , and is capable of promoting antigen-presenting (dendritic) cells and leukocyte recruitment, and activating specific immune responses, such as il-1b,il-6, il-10, tnf-a [48] . reports on the familial occurrence of severe drug hypersensitivity and cases occurring in identical twins suggest genetic links [49] [50] [51] [52] . the hla genes show strong association with drug hypersensitivity. examples of strong associations of hla alleles with specific drug-induced hypersensitivity reactions include abacavir, nevirapine, carbamazepine, and allopurinol (table 25. 2). the view that hla alleles are the main genetic determinants of sjs/ten was first proposed by roujeau et al. [61] , who reported the weak associations of hla-a29, b12, and mpe maculopapular drug eruption, dress drug reaction with eosinophilia and systemic symptoms, sjs/ten stevens-johnson syndrome/toxic epidermal necrolysis dr7 in sulfonamide-related ten, and hla-a2, b12 in oxicam-related ten in europeans [61] . following the immunological hypothesis, the most striking evidence of genetic susceptibility to sjs/ten was provided by the findings that hla-b*15:02 is strongly associated with carbamazepine-induced sjs/ten [53] , hla-b*58:01 with allopurinol-induced sjs/ten or dress [54] , and hla-b*5701 with abacavir hypersensitivity [62] . the hla association to specific drug-induced hypersensitivity can be ethnic and phenotype-specific. the strength of hla associations with specific drug-induced hypersensitivity in different populations has been found related to the prevalence of the susceptibility allele in the ethnic population. the association of hla-b*15:02 with carbamazepineinduced sjs/ten was replicated in other asian countries, including thailand, hong kong, malaysia, china, vietnam, cambodia, reunion, philippines and indian ethnicities, which carry high hla-b*15:02 allele frequency, but not in europeans, which carry low hla-b*15:02 allele frequency (<1 %) [63] . in contrast, the strong association of hla-b*58:01 with allopurinol-induced sjs/ten is more universal, being found in han chinese in china, thai populations, korean, japanese, and european populations; hla-b*58:01 is the allele common to all these populations [64] . the phenotype-specific characteristics are exemplified by carbamazepine hypersensitivity. while hla-b*15:02 is strongly associated with carbamazepine-induced sjs/ten, it is not associated with carbamazepine-induced dress; in an international study, hla-a*31:01was strongly associated with carbamazepine-induced dress, but not with carbamazepineinduced sjs/ten [65] . phenytoin -an aromatic antiepileptic drug structurally related to carbamazepine -also frequently causes sjs/ten and dress [66, 67] . hla-b*15:02 has been associated with phenytoin-related sjs/ten in asians, although the association is much weaker than that found for carbamazepine-related sjs/ten [68] . a recent genome-wide association study by chung wh et al. turned up cytochrome (cyp) 2cvariants, including cyp2c9*3, that showed a strong association with phenytoin-related scar. the significant association between cyp2c9*3 and phenytoin-related severe cutaneous ards was replicated in different asian populations [69] . similar to delayed-type drug hypersensitivity, genetic predisposing factors have been reported in immediate-type drug hypersensitivity. β-lactam allergy was reported associated with gene variants of il13, il4, and il4ra [70] [71] [72] [73] . several genetic predisposing factors, including gene polymorphisms in cysteinyl leukotriene receptor type 1 (cysltr1) and leukotriene c4 synthase (ltc4s) [74] and high-affinity ige receptor (fcepsilonr1) [75] , were associated with aspirin. cutaneous adrs may be classified in terms of their presumed mechanism, severity of the reaction, histological findings, and cutaneous morphological manifestations. the modern pharmacological classification of adrs differentiates two basic types of reactions; type a, predictable reactions, and type b, unpredictable or idiosyncratic reactions. type a reactions ('augmented') are dose-dependent, common and predictable based on the pharmacology of the drug; about 80 % of all adrs are type a. type b reactions ('bizarre') do not occur at any dose in most patients, but may be dose dependent in susceptible individuals. they are uncommon, affecting a small number of patients based on an individual predisposition that depends on both genetic and environmental factors [76, 77] . the pathogenesis of type a reaction was described in the sixteenth century by paracelsus, the swiss german renaissance physician who founded the discipline of toxicology: "all things are poison, and nothing is without poison; only the dose permits something not to be poisonous" [78] . the pathogenesis of type b reaction was designated in the first century bc didactic poem, de rerum natura (on the nature of things), by the roman poet and philosopher lucretius: "one man's meat is another man's poison" [79] . type b reactions can be categorized into different subtypes according to gell and coombs' classification system [80] . the effector phase of the allergic reaction is classified into four types: type i mediated by drug-specific ige antibodies, types ii and iii mediated by drug specific igg or igm or iga antibodies, and type iv induced by drug-specifc t lymphocytes [81] . this classification system may be helpful in daily clinical practice as a guide to diagnostic and therapeutic decisions. in addition to the basic classification of type a and b reactions, further types of reactions were subsequently added; type c-dose and time-related, 'chronic'; type dtime-related. 'delayed'; type e-withdrawal effects, 'end of use'; and type f-unexpected failure of therapy, 'failure' [2] . the diagnosis of a cutaneous adr must be followed by differentiation between a simple reaction involving only the skin and a complex reaction that includes systemic involvement of organs in addition to the skin [82] . systemic involvement should be explored even in a mild cutaneous eruption due to a drug since the severity of skin manifestation does not necessarily mirror the severity of the systemic involvement. systemic involvement is evaluated by assessing the patient's symptoms, including fever, facial edema, malaise, chills, dyspnea, cough, palpitations, nausea, vomiting, diarrhea, sore throat and arthralgia. further investigation is based on the patient's symptoms. basic laboratory screen, conducted in cases of suspected systemic involvement, includes a full blood count, liver and renal function tests, and urine analysis [83] . skin biopsy is an invaluable diagnostic modality in the assessment of drug eruptions. histologically, drug eruptions can elicit a variety of inflammatory disease patterns in the skin and panniculus, and overlapping reaction patterns. ackerman et al.'s basic patterns of inflammatory skin diseases [84] (table 25. 3) are a helpful guide. the most common pattern of drug eruptions is the perivascular type, while psoriasiform and granulomatous patterns are rarely reported [85] . drug eruptions may also mimic specific skin diseases such as lupus, lichen planus or lymphoma [85] . a single drug may cause a wide range of reaction patterns and no reaction pattern is specific for a particular drug [88] . while the histological changes are not distinctive in many cases of drug eruption, a few important histopathological clues may aid in the diagnosis: (1) overlapping histological patterns in one specimen (e.g., lichenoid and spongiotic). (2) presence of eosinophils (although not mandatory); although eosinophils are an important tell-tale sign of a drug-induced reaction, they may also be conspicuous in skin rashes devoid of a drug association and sparse or absent in some drug exanthems. (3) apoptotic keratinocytes. (4) mismatch between clinical and histomorphological features [85, 86, 88] . in a study assessing the histological pattern of 104 cases of diagnosed drug eruption during a 5-year period in one institution [89] , the majority of the cases (94 %) were morbilliform-type rashes. the most common histological pattern was superficial perivascular and interstitial with interface changes. eosinophils were present in only 50 % of cases, and approximately half (53 %) of the cases exhibited epidermal-dermal interface changes [89] . in view of the large diversity of cutaneous drug reactions, it is helpful to approach them as clinicopathologic entities and to base the diagnosis on a combination of clinical, histological and disease course data [89] . heightened awareness of the possible mimicry of other skin diseases and of the suspicious histopathological clues pointing to drug etiology are key elements to the appropriate histological diagnosis of drug reactions in the skin [85, 88, 89] . a widely accepted approach to diagnosing the type of drug eruption is a simplified method based on the morphology of the primary lesions. the four main categories are maculopapular, urticarial, pustular and blistering [82] . the diagnosis of the drug eruption can be challenging since the same cutaneous morphology can be manifested in a simple reaction involving only the skin and in a complex reaction including systemic involvement in addition to the skin. therefore, there are two major steps in diagnosing drug eruptions: determine the morphology and assess systemic involvement [90] . terminology the term 'maculopapular' is descriptive. morbilliform means measles-like, the rash of measles consisting of macules and papules that tends to confluence. the etymon of 'exanthema' is the greek 'exanthema', which means 'a breaking out'. thus exanthema merely means 'rash', and 'exanthematous rash' literally means 'rash-like rash'. therefore, the terminology is redundant [89] . polymorphous pink-to-red macules and or papules usually in a symmetric distribution that may coalesce to form plaques ( fig. 25 .1) [91] . the eruption begins on the trunk and upper extremities and progressively becomes confluent. in addition, purpuric lesions may appear on the ankles and feet [90] . the drug eruption can also manifest in a scarlatiniform pattern of pinpoint-sized pink-red papules coalescing and giving the skin the texture of sandpaper [92] . frequency the most common drug-induced eruptions, occurring in 1-5 % of first-time users of most drugs [91] . lag period 7-14 days [90] . symptoms pruritus and low-grade fever are common [91] . the eruption usually begins on the trunk and becomes generalized. palms and soles are often involved; mucous membranes are usually spared [90] . histology nonspecific changes consisting of mostly superficial but also deep perivascular and interstitial infiltrate of lymphocytes. eosinophils and epidermal-dermal interface changes appear in approximately half the cases [89] . differential diagnosis viral exanthems, scarlet fever, toxic shock syndrome, acute graft versus host disease (gvhd), kawasaki disease, juvenile idiopathic arthritis [90] . treatment identifying and discontinuing the causative drug are the most important steps in management. symptomatic treatment with antipruritic agents and potent topical glucocorticoids may be helpful [91] . a decision can be made to continue the drug and offer symptomatic treatment if the drug is of paramount importance, but the risk: benefit ratio of this option has to be carefully weighed, and the evolution of the eruption must be meticulously monitored [90] . prognosis the eruption often fades within 7-14 days of discontinuation of the offending drug and scaling and desquamation may follow. re-challenge may lead to reappearance of the reaction within a few days [90] . offending drugs the most common classes of drugs implicated are penicillins, sulfonamides, cephalosporins, and antiepileptics [90] . terminology the term 'urticaria', first introduced by william cullen in the eighteenth century, is derived from urtica urens (common european stinging nettle). one of the earliest descriptions of urticaria comes from china, and is more than erythematous macules and papules coalescent into illdefined plaques on the trunk -maculopapular morphology of cutaneous adr 2,000 years old. in the huangdi neijing, written around 200 bc, urticaria is referred to as feng yin zheng ('wind type concealed rash'). in ancient latin medical literature, urticaria was called 'uredo' (urere means 'to burn'), and in the old persian medical texts, 'essera' (meaning 'elevation') [93] . skin signs urticaria is induced by superficial dermal swelling due to plasma leakage and vasodilation triggered by activation of mast cells. the skin manifestations of this process include erythematous and edematous papules and plaques (wheals) of various sizes that may coalesce to form large plaques [94] . wheals may be characterized by pink or pale center and assume a figurate or polycyclic configuration. linear lesions can be seen with dermatographism [92, 94] . frequency drug-induced urticarial eruptions are the second most common type of cutaneous drug eruption and account for approximately 5 % of all cutaneous drug eruptions [85] . lag period urticaria occurs within minutes to days of drug administration [94] . symptoms a major clinical feature is pruritus, the lack of which should put the diagnosis in doubt. the lesions can also be painful if they occur on the soles, over joints, or in areas where the skin is tightly adhered to subcutaneous tissue [94] . a single lesion lasts less than 24 h and upon resolution leaves normal skin. however, new lesions may continue to arise for various periods of time. acute urticaria is defined when a bout of hives lasts less than 6 weeks; when it lasts longer, it is defined as chronic urticaria [95] . urticaria may be associated with angioedema [93] . angioedema is defined as a deep, dermal, subcutaneous and/or mucous swelling that may involve the intestinal lining and the upper respiratory tract. symptoms include slight heat, burning, pain and sensation of pressure or tightness. however, pruritus is minimal or absent. swelling of gastrointestinal tract mucosa can induce abdominal pain, vomiting and diarrhea. edema of the respiratory tract may induce various symptoms including life-threatening asphyxia. drug-induced angioedema is associated with urticaria in approximately 50 % of cases. some drugs may induce angioedema without urticaria [96] . common sites of involvement lesions of urticaria can appear anywhere on the skin, including the palms, soles and scalp, but not on mucosal surfaces [94] . angioedema most commonly occurs in the head, neck and hands, but can occur anywhere and frequently involves mucosal tissue. swelling may be more prominent in areas of looser skin, such as the scrotum, labia, lips, and eyelids [94] . histology urticarial drug reactions are characterised by dermal edema and a superficial and deep perivascular and interstitial dermatitis. the mixed inflammatory infiltrate comprises lymphocytes, histiocytes, mast cells, eosinophils and neutrophils. the presence of neutrophils and deep vascular plexus involvement may be a clue to the drug-induced nature of the urticaria [86] . the wheals with central red halo of urticaria may resemble the target lesions of erythema multiforme. four clinical signs of urticaria can help distinguish it from erythema multiforme: (1) the central zone consists of normal skin, whereas in erythema multiforme, skin is dusty, bullous or crusted. (2) each lesion is transient, lasting less than 24 h, whereas erythema multiforme lesions are 'fixed' for a few days. (3) new lesions appear daily and in erythema multiforme all lesions appear within the first 72 h. (4) there may be associated swelling of face, hands and feet and in erythema multiforme there is no edema [97] . differential diagnosis of urticaria includes also bullous pemphigoid, urticarial vasculitis and serum sickness-like reaction (sslr). drug-induced urticaria needs to be differentiated from cases of urticaria induced by other etiologies, such as food, environmental allergens, insects, systemic illness, physical stimuli, genetic and idiopathic [94] . urticaria and angioedema are the most common symptoms of anaphylaxis (88 % of cases), and are one of the clinical criteria of the national institute of allergy and infectious disease (niaid) and the food allergy and anaphylaxis network (faan) for the diagnosis of anaphylaxis [98] . therefore, all cases of sudden acute urticaria and angioedema should be evaluated for indications of the anaphylactic type of reaction: presence of respiratory compromise, decreased blood pressure, and end-organ dysfunction (collapse, syncope, incontinence) [98] . treatment the most important step in the management of drug induced urticaria with or without angioedema is withdrawal of the causative agent. in most cases of acute urticaria, when the trigger is removed the rash quickly resolves. h1-receptor blockers are the mainstay of treatment for patients with only cutaneous symptoms. systemic glucocorticoids are indicated in all cases with upper airway edema and should be considered in cases with extensive cutaneous involvement. epinephrine is reserved for angioedema with upper airway involvement [94] . the presence or absence of any airway involvement should be specifically investigated. prognosis both urticaria and angioedema fade without visible sequelae. following resolution, there should be no residual pigmentary changes unless excoriated [94] . offending drugs many drugs can induce acute urticaria, and do so by both immunologic and non-immunolgic mechanisms. the major drugs responsible for immunologically based urticaria are antibiotics, especially penicillins and cephalosporins [90] . the major drugs triggering mast cell release (non-immunolgic mechanisms) are aspirin, nonsteroidal anti-inflammatory drugs (nsaids), opioids and radiocontrast media [90] . viral infections or connective tissue diseases may induce or augment urticarial drug reactions [86] . the national institute of allergy and infectious diseases (niaid) and the food allergy and anaphylaxis network (faan) defined anaphylaxis as a systemic reaction resulting from the sudden release of multiple mediators from mast cells and basophils, often life threatening, and usually unexpected. the world allergy organization (wao) has divided anaphylaxis into immunologic (further divided into immunoglobulin e [ige]-mediated and non-ige-mediated), non-immunologic, and idiopathic causes. drugs are the second most common cause of anaphylaxis after food, which constitutes 20 % of triggers [98] . common medications associated with anaphylaxis include penicillins, nsaids, and biologic response modifiers [99] . the niaid/ faan definition of anaphylaxis has been translated into clinical diagnostic criteria that include an acute onset of illness (minutes to hours) and involvement of the dermatologic, respiratory, cardiovascular, or gastrointestinal systems [98] . epinephrine is the only first-line treatment for anaphylaxis and is the sole effective treatment for an acute reaction. delays in administration have been associated with fatalities. supportive treatment with oxygen, fluids and additional drugs are also necessary according to the cardiopulmonary resuscitation (cpr) anaphylaxis algorithm [98] . • serum sickness-like reaction (sslr) -see severe cutaneous adverse drug reactions. terminology the term pustule originates in classical latin in which pustule means a blister [100] . skin signs pustular drug eruptions are characterized by monomorphic eruption consisting of erythematous papules (mostly follicular) and pustules at the same location lacking comedones. acneiform drug eruptions (acne medicamentosa) the term acneiform is applied to eruptions that resemble acne vulgaris. frequency varies, depending on the drug. the highest incidence involves epidermal growth factor receptor inhibitors (egfris), affecting 60-100 % of patients [101] . lag period the eruption begins after a variable delay; corticosteroids may induce an acneiform eruption from shortly after their introduction (2-4 weeks) to several months [101] . acneiform eruptions induced by egfris usually appear after 1-2 weeks of treatment but can also occur after only a few days [102] . symptoms pruritus, tenderness and pain may occur. in cases of chemotherapy-related side effects, their appearance and severity are part of the criteria used for the classification of the adr [103] . common sites of involvement lesions may be located in and beyond the seborrheic areas, such as the arms, trunk, lower back and genitalia [104] . histology drug-induced acneiform eruptions show histopathologic features similar to acne vulgaris. early lesions most commonly have a corneocytic plug within a widened infundibulum, accompanied by infundibular spongiosis, perifollicular edema, with sparse perivascular and periinfundibular infiltrates of neutrophils and lymphocytes. larger older lesions show similar findings but the infiltrate is denser, with more neutrophils around the involved follicles, and infundibular rupture [85, 88] . in a review of the histological findings of acneiform eruptions induced by egfris [105] , all ten cases showed a superficial, predominantly neutrophilic suppurative folliculitis with ectatic infundibula and a rupture of the epithelial lining. differential diagnosis the main differential diagnosis is acne. the following clinical characteristics of acneiform drug eruptions may aid in differentiating between the two entities: (1) clinical presentation: monomorphic pattern, lack of comedones and cysts and localization on areas beyond the seborrheic area. (2) patient characteristics: age of onset before or after the teens, and absence of past history of acne. (3) resistance to conventional acne therapy. (4) time relationship: onset after recent drug introduction, improvement after drug withdrawal, and recurrence after drug reintroduction [101] . the differential diagnosis also includes folliculitis, rosacea, perioral dermatitis, demodicosis, acne cosmetic, acne mechanica, chloracne, acne necrotica and acneiform presentation of cutaneous lymphomas [104] . treatment the main treatment is withdrawal of the offending drug and the application of topical treatments as needed (benzoyl peroxide topical antibiotics and topical retinoids) [90] . the management of acneiform eruptions associated with chemotherapy differs from all other types of acneiform drug euptions, as acneiform eruption is an expected outcome and discontinuation of the medication is not an option in a patient who is responding to therapy [102, 103, 106, 107] . in fact, continuation of egfri therapy in these patients may be especially favourable in view of studies that have shown an increased survival with increasing severity of rash [102] . the cutaneous reaction serves as an important clinical tool for determining tumor response and survival [102] . the national cancer institute developed a scale for defining the degree of rash and laid down management guidelines for each stage [103] . other management protocols were suggested by bachet et al. [107] , who recommended that unless contraindicated, a tetracycline should be routinely prescribed for the prevention of acneiform eruption in patients treated with an egfri for more than 6 weeks. chiang et al. [106] reported successful treatment with isotretinoin for high grade and refractory cases. prognosis in most patients with acneiform drug eruption, the rash resolves upon discontinuation of the offending drug and the use of topical treatment. in egfri-induced acneiform eruption, prophylactic administration of a tetracycline was associated with significantly lower incidence of grade 2-3 folliculitis and improved quality of life of patients [107] . few cases of drug-induced eosinophilic pustular folliculitis have been reported [88, [108] [109] [110] [111] . drugs reported include chemotherapy (cyclophosphamide, methotrexate, and 5-fluorouracil) [108] , minocycline [109] , carbamazepine [110] , and allopurinol with timedium bromide [111] . clinical presentation includes pruritic follicular papules and pustules on the face, scalp, trunk and arms [88] . histological findings include spongiosis of the follicular epithelium, and an intraand perifollicular lymphohistiocytic infiltrate with numerous eosinophils that form microabscesses within the follicular epithelium [88] . topical steroids are the first line of treatment [108] . acute generalized exanthematous pustulosis (agep) -see severe cutaneous adverse drug reactions. terminology the term pseudoporphyria was coined in 1975 by korting to describe patients with chronic renal failure and a bullous disease resembling porphyria cutanea tarda (pct) [112] . frequency the incidence of pseudoporphyria is unknown. however, in a 6-month prospective study, 12 % (9/74) of children taking naproxen for juvenile idiopathic arthritis developed pseudoporphyria [113] . lag period the skin lesions appear following drug intake combined with exposure to light. various time durations were reported, weeks to months [114] [115] [116] . the clinical features of pseudoporphyria may be identical to those of pct; both exhibit vesicles, bullae, milia, and scarring on sun-exposed skin. in contrast to pct, however, hypertrichosis, hyperpigmentation, sclerodermoid changes, and dystrophic calcification are rarely reported in pseudoporphyria [117] . often, fragility and bruising may be the only clinical signs [116] . in children, facial scarring resembling erythropoietic protoporphyria (epp) may be found [117] . symptoms skin fragility and photosensitivity [116] . the lesions appear on sunexposed skin, particularly the hands and feet, but also on the face and extensor surfaces of legs [116] . histology the histological features are identical to those seen in pct. the blisters are subepidermal and the floor of the blister is typically lined by well-preserved dermal papillae (festooning). there is usually no significant inflammatory component although a light perivascular lymphocytic infiltrate may occasionally be seen in the superficial dermis. thickening of the superficial vessels (highlighted by a pas stain) and dermal sclerosis with elastosis may be apparent. in both pseudoporphyria and pct, direct immunofluorescence reveals granular deposits of igg and c3 at the basement membrane zone and in the perivascular region [115] . differential diagnosis while pseudoporphyria and pct share clinical and histologic features, they can be differentiated by several features. most important, by definition, biochemical porphyrin abnormalities are absent in pseudoporphyria. epidemiologically, pseudoporphyria affects mainly women while there is a male predilection in pct. clinically, hypertrichosis, hyperpigmentation, sclerodermoid changes, and dystrophic calcification are frequently evident in pct and conspicuously absent in pseudoporphyria [117] . the differential diagnosis also includes other types of cutaneous porphyria that manifest with blistering, epidermolysis bullosa acquisita, polymorphous light eruption, and other photosensitive dermatosis [117] . treatment treatment entails discontinuation of suspected agents and sun protection, especially against uva wavelengths, for several months following withdrawal of the drug [114] . prognosis blisters may continue to appear for weeksmonths after discontinuation of the offending drug [117] . offending drugs the most common group of drugs causing pseudoporphyria are nsaids [117] . other groups are antibiotics, diuretics and retinoids. additional culprits are hemodialysis, renal failure, tanning beds and excessive sun exposure [117] . terminology fixed drug eruption (fde) was first reported by boums in 1889 [118] , and the term was coined by brocq in 1894 [119] . frequency the incidence is not known, but is suspected to vary greatly by geographic region [120] . lag period after initial use of the offending agent, a variable refractory period of weeks, months or years may pass before the lesions first appear on the skin of a sensitized individual [121] . repeated exposure to the agent typically results in acute lesions within 30 min to 8 h. a refractory phase may occur following an acute flare in which exposure to the offending drug will not exacerbate the lesion for weeks to months [121] . in its classical form, fde typically presents round or oval, sharply demarcated, red to livid, slightly elevated plaques ranging from several millimeters to over 10 cm in diameter. vesicles or even blisters can develop [122] . usually only a single lesion appears. sometimes, multiple lesions are present and even lead to generalized fde characterized by multiple, sharply defined, deep red macules distributed bilaterally and often symmetrically. generalized bullous fde is characterized by flaccid blisters arising on these macules. mucosal lesions are usually bullous and may appear with or without involvement of other areas of the skin [122] . symptoms patients often complain of burning and itching in the lesions. general symptoms such as fever, nausea, dysuria, abdominal cramps and diarrhea are rare [122] . pruritus and burning may be the only manifestations of reactivation in a postinflammatory hyperpigmentation lesion [121] . common sites of involvement the eruption can occur anywhere on the body, but the lips, palms, soles, genitalia (especially male genitalia), groin and occasionally oral mucosa are favored sites [121] . the diagnostic hallmark of fde is the reappearance of the lesions precisely over the previously affected sites. studies investigating the predilection areas indicate that some specific kind of drugs cause fde predominantly at specific sites: examples are tetracycline and location on the male genital area, and naproxen and fde on the lips [122] . in rare cases, fde manifests in old trauma sites such as bcg vaccination, burn scar, venipuncture site or insect bite. with each recurrence, additional sites may be affected. the presence of numerous lesions is referred to as generalized fde [122] . histology histologically, the acute phase is characterized by marked basal cell hydropic degeneration, with lymphocyte tagging along the dermoepidermal junction and individual keratinocyte necrosis. marked pigmentary incontinence is typical, and may be the sole histological finding in late lesions [121] . differential diagnosis skin lesions can imitate various dermatoses, including lichen planus, erythema multiforme, erythema annulare centrifugum, and pityriasis rosea. in generalized fde, residual pigmentation in healed lesions may be reminiscent of erythema dyschromicum perstans. involvement of oral and genital mucosa raises the possibility of herpes simplex, pemphigus vulgaris, aphthous stomatitis, behçet syndrome, and erosive lichen planus [122] . generalized bullous fde may resemble sjs/ten. the following typical clinical features of generalized bullous fde may aid in differentiating between conditions: (1) blistering usually affects only a small percentage of body surface area, and between the large blisters there are sizable areas of intact skin. (2) erosive mucosal involvement is rare, and when it does occur is rather mild. (3) patients usually do not feel sick or have fever, and generally are in much better overall health than those with sjs/ten. (4) most patients report a history of a similar, often local reaction [123] . treatment for mild lesions, topical corticosteroids usually suffice. in severe involvement, especially generalized bullous fde, systemic corticosteroids may be indicated. strict avoidance of the causative drug and cross-reacting substances is essential for prophylaxis. successful desensitization was reported [122] . prognosis the prognosis of localized fde is good and the lesions fade within a few days to leave a post-inflammatory brown pigmentation [122] . generalized bullous fde does not have this benign nature and the mortality rate was 22 % in a recent case control study of 58 patients [120] . offending drugs the most common groups of drugs implicated are antibiotics, analgesics, antiphlogistics and hypnotics [122] . there is usually only one causative drug (monosensitivity), but sometimes several drugs can induce fde in the same patient (multisensitivity). it has also been claimed that recurrences of fde can be induced in nonspecific fashion by mast cell degranulators such as food, acetylsalicylic acid, bacterial toxins, or physical stimuli [122] . • drug-induced/triggered autoimmune blistering dermatosis (pemphigus, bullous pemphigoid (bp)) and linear iga bullous dermatosis (labd) [127] . cases of autoimmune blistering dermatosis resulting from exposure to drugs present clinical, histologic and immunopathologic features identical or very similar to those seen in idiopathic disease, but are induced by systemic ingestion or local use of certain drugs. there appear to be two main types: drug-induced autoimmune blistering dermatosis proper, the acute and self-limiting type with rapid resolution after withdrawal of the offending agent; and drug-triggered autoimmune blistering dermatosis in which the role played by the drug is only secondary to hereditary and immunologic factors. the drug stimulates a predisposition (hidden susceptibility) to develop the disease and is considered the chronic type in which the disease persists despite withdrawal of the offending agent [128, 129] . frequency unknown. [130, 133, 136] . of note, drug-induced labd patients tend to be older than idopathic type patients [134, 135] . the polymorphic nature of the eruption may mimic other bullous diseases and or drug-induced bullous diseases such as sjs, ten, and fde [136] . treatment treatment consists of discontinuing the offending agent, and, depending on the severity of the disease, systemic immunosuppressive treatment [129] . prognosis drug-induced autoimmune blistering dermatosis remits after the offending drug is withdrawn, while drugtriggered autoimmune blistering dermatosis may persist despite withdrawal of the offending agent and chronic immunosuppressive treatment may be required [129, 130] . two major groups of chemical structures were found in the drugs or their metabolites implicated in pemphigus: sulfhydryl radical drugs (thiol drugs or sh drugs) such as penicillamine, and phenol drugs such as aspirin [128, 137, 138] . bp many drugs were reported [129, 132, 136] , the most frequent being nsaids, cardiovascular agents and penicillin-derived antibiotics [136] . in addition, external use of skin and mucous membrane preparations has been documented to provoke cases of either bp or cicatricial pemphigoid [136] . labd of the various drugs reported, vancomycin is the most common [134, 135, 139] . reactions. the incidence of dress remains to be determined because of variable presentations and lack of universally accepted diagnostic criteria [140] . the estimated risk at first or second prescription of an aromatic antiepileptic drug was 1-4.5 in 10,000 [141] . a slight female predominance was found in the regiscar study (male/female 0.8) [142] . the drugs most commonly inducing dress are anti-convulsants (mainly aromatic anti-convulsants such as carbamazepine), allopurinol, sulfonamides (the anti-infective sulfamethaxazole-trimethoprim, and the anti-inflammatory sulfasalazine), and antibiotics (such as vancomycin and minocycline) [142] . numerous other drugs have been reported [140, 143, 144] . the role of human herpesvirus (hhv) reactivation in the development of this adverse drug reaction is well recognized, especially hhv-6 [145] . hhv-6 reactivation is among the diagnostic criteria of the japanese consensus group for dress/drug-induced hypersensitivity syndrome [146] . the reactivation of other herpesviruses, including hhv-7, cytomegalovirus (cmv), epstein-barr virus (ebv), and human herpes simplex virus was also reported [147] . dress is considered to result from complex interactions between genetic predisposition, exposure to drug and viral reactivation [148] . delayed onset of 2-8 weeks after drug administration followed by a stepwise development of manifestations. rechallenge can result in a reaction within hours to days [26] . the lag period differs between drugs; carbamazepine tended to show a longer latency (median 29 days) than allopurinol (median 20 days) in the regiscar study [142] . dress has multi-organ involvement with cutaneous, mucosal, hematological and solid organ manifestations. the cutaneous involvement in dress is typically extensive and symptomatic (pruritus, burning and pain) [142, 143] . various dermatological features were reported. walsh et al. [143] proposed a classification system based on four distinct patterns: (1) urticated papular exanthema, the most common, (2) morbilliform erythema, (3) exfoliative erythroderma, and (4) erythema multiforme-like (em-like), which was prognostic of more severe hepatic involvement. the extent of skin involvement varies between studies: it exceeded 50 % of the body surface area in most of the patients (79 %) according to the regiscar study [142] ; head and neck edema observed in most patients [26, 142] ; and pustules reported in various studies, predominantly in a facial distribution of the edema [142, 143] . [142] . most frequent were oral lesions including lips, oral cavity and throat [142] . the manifestations of oral lesions in dress include cheilitis, erosions and dysphagia that may appear before skin lesions, and oropharaynx is considered the first site of herpesvirus reactivation in dress [149] . involvement of eyes and genitalia were also reported in the regiscar study [142] . multi-organ involvement is common in dress and may include a wide variety of systems. highgrade fever (38-40 °c) is a typical early manifestation that may last for several weeks; it often precedes the cutaneous eruption by several days [142] . lymphadenopathy is common and has two distinct types: a benign pattern of lymphoid hyperplasia and a pseudolymphoma pattern [150] . hematologic abnormalities are frequent and diverse, the most common being marked leukocytosis, eosinophilia and atypical lymphocytes [142] . however, neutrophilia, monocytosis, thrombocytopenia, anemia, pancytopenia and hemophagocytic syndrome were also reported [140, 142, 143, 151] . hypereosinophilia and activated neutrophils, if persistent, can contribute to organ damage [142] . the liver is the most frequently affected visceral organ in dress; hepatitis with isolated elevation of liver enzymes is common and usually anicteric and without cholangitis. however, severe acute hepatitis with liver failure may result and is the primary cause of mortality in dress [150] . renal involvement is common [150] . involvement of the following organs was also reported: lungs, muscle, heart, pancreas, colon, thyroid, joints, parotid gland and brain [150] . the type of organs involved was found to be related to the eliciting drug [152] . the most common pathological changes found in a study of 32 patients with dress were basket-weave hyperkeratosis (94 %), dyskeratosis (97 %), lymphocytic exocytosis (91 %), spongiosis (78 %), papillary edema (66 %), perivascular lymphocytic infiltration (97 %), eosinophilic infiltration (72 %), and interface vacuolization in the dermoepidermal junction (91 %) [26] . the presence of severe dyskeratosis was correlated with a greater extent of systemic involvement [26] . in a different study assessing the histological findings of 27 cases with dress [143] , the predominant pathological pattern was spongiotic dermatitis with superficial lymphocytic infiltrate (59 %); necrotic keratinocytes were noted in 33 % of cases, and were associated with a worse hepatic involvement [143] . the diverse presentations in dress have hampered efforts to define diagnostic criteria. three diagnostic criteria have been proposed: bacquet et al. [153] , the japanese study group of severe cutaneous adverse reactions to drugs (j-scar) [146] , and the regiscar network [154] . the first step in the management is immediate withdrawal of the culprit drug. the treatment is tailored according to the severity and extent of systemic involvement, and the diagnosis of viral reactivation of herpesviruses (mostly hhv-6) [150, 155, 156] . management protocol for dress based on the consensus of experts was designed by the french society of dermatology [156] , and includes four visceral involvement severity categories and corresponding treatment: counselling both the patient and his family members about drug avoidance is necessary. first-degree relatives have a higher risk of developing the same drug reactions [90] . increased knowledge of hla susceptibility genes enables screening patients with dress for several high risk drugs [148, 157] . symptoms are usually present for several weeks even after discontinuation of the offending agent and appropriate treatment [155] . late complications include the appearance of autoimmune diseases such as lupus erythematosus and autoimmune thyroiditis, with laboratory evidence of autoantibodies [144] . systemic corticosteroids were found beneficial in the prevention of autoimmune disease. however, this effect needs to be counterbalanced against the higher risk of viral reactivation and infection. [144] . in a 1-year follow-up study of 52 affected patients with dress in taiwan, the overall cumulative incidence of long-term sequelae was 11.5 %; four developed autoimmune diseases (graves disease, type 1 diabetes mellitus and autoimmune hemolytic anemia); and the other two developed renal failure and required lifelong hemodialysis. the author concluded that the sequelae of dress can be divided into two major types that appear in different age groups: young patients tend to develop autoimmune diseases; elderly patients are more vulnerable to end-organ failure [158] . mortality in dress has been estimated at 10 %, with most patients dying from liver failure [159] . pancytopenia, leukocytosis, tachycardia, tachypnea, coagulopathy, gastrointestinal bleeding and systemic inflammatory response syndrome were associated with a poor outcome in dress patients [159, 160] . the incidence of sslr is unknown. epidemiology studies in children suggest that the overall frequency induced by cefaclor is 0.024-0.2 % per course of the drug [76] . most reactions were reported in children under 5 years old, mainly during the second and third courses of therapy [161] . cefaclor is the most common cause of sslr in children, inducing 84.1 % of cases [162] . other drugs implicated include other cephalosporins, [163] penicillins, [164] minocycline, [165] insulin, [166] and infliximab [167] . usually 7-14 days (range 0-20 days) [162, 168] . skin the skin is the most frequent finding in sslr, including erythema that progresses to urticarial lesions (pruritic and migratory), urticarial wheals with dusty to purple centers ('purple urticaria') that morphologically resemble erythema multiforme (em) [161] and other cutaneous manifestations including morbilliform or scarlatiniform eruptions [82] . mucous membranes are not involved [161] . systemic involvement joint involvement may be prominent, presenting with edema, decreased range of motion, warmth, pain, and difficulty walking. polyarticular involvement is often observed, with involvement mainly of the wrists, ankles, hips and knees [169] . some authors suggested that joint involvement may be related in part to increased fluid in the skin around affected joints due to urticarial eruption rather than arthritis [161] . fever, malaise, myalgia and lymphadenopathy were also reported. neurologic involvement, gastrointestinal symptoms and renal complications were rarely documented [163] . notable laboratory abnormalities include elevated erythrocyte sedimentation rate (esr), c-reactive protein (crp) and leukocytosis [163, 170] . the histological findings of sslr appear to be in the spectrum of urticaria with no vasculitis [171] . histology can be helpful in differentiating sslr from acute hemorrhagic edema of infancy, which is characterized by vasculitis [171] . there are no diagnostic criteria. the diagnosis is based on clinical findings [161] . withdrawal of the offending agent and symptomatic treatment with oral antihistamines and topical corticosteroids are usually sufficient. a short course of oral corticosteroids may be required in patients with severe symptoms [82] . the disease course is benign and resolves in a few days. however, a few cases lasting several weeks have been described [170] . no long-term morbidity has been reported [172] . the estimated incidence of agep is 1-5 cases per million per year [173] . female predominance was reported in several studies [174] [175] [176] . the majority of cases appear to be related to drugs (>90 %), mainly antibacterials [4] . in a large multinational casecontrol study (the euroscar study), the following agents were highly suspected drugs for agep: prestinomycin, ampicillin/amoxicillin, quinolones, (hydroxy)chloroquine, anti-infective sulfonamides, terbinafine and diltiazem [176] . latent periods fall into two categories, according to the offending drug: median duration of 1 day, associated with antibiotics (including sulphonamides), and median duration of 11 days for all other associated drugs [176] . longer periods of months were reported in a few agep cases with an underlying malignancy [177] . agep is a severe acute pustular cutaneous reaction characterized by a rapid clinical course [174] . skin the typical morphology of agep is an acute edematous erythema with burning and or itching sensation, followed by dozens to hundreds of small (pinhead sized) non-follicular sterile pustules with a predilection for the big folds, or with widespread distribution (fig. 25.2) . sometimes confluence of pustules may mimic a positive nikolsky's sign [176, 178] . additional cutaneous manifestations include marked edema of the face, purpura, blisters and target-like lesions [173, 174, 179] , all of which overlap with manifestation of agep and ten [180, 181] , and acute localized exanthematous pustulosis (alep) [179, 182] . mild, nonerosive mucous membrane involvement of one location (mostly oral) occurs in about 20 % of cases [183] . systemic involvement fever (above 38 °c) and leukocytosis with neutrophilia are almost always apparent. lymphadenopathy, myalgia, headache, mild eosinophilia, elevated crp, slight reduction of creatinine clearance, and mild elevation of aminotransferases were also reported [173, 175] . a 10-year retrospective review of 58 patients with agep [184] turned up 10 patients (17 %) with at least one systemic involvement in the acute phase, 7 with abnormal hepatic function test, 6 with renal insufficiency, two with acute respiratory distress and one patient with agranulocytosis. mean peripheral neutrophil counts and mean c-reactive protein levels were elevated significantly in patients with systemic involvement [184] . biopsy specimen should be obtained from an early pustular lesion [183] . a histopathological study of 102 agep cases [185] found the following histopathological features: (1) all cases demonstrated pustules (sub/intracorneal and or intraepidermal). the agep validation score developed by the euro-scar study group is a standardized scoring system made up of data related to clinical features (morphology and clinical course) and histopathology. based on this score, agep cases can be categorized as no agep, possible agep, probable agep, and definite agep [173] . treatment consists of discontinuation of the causative drug and supportive treatment. although, specific treatment is generally unnecessary, topical and systemic steroids were reported [174, 175] . the treatment of overlapping agep and ten cases is not yet established [180] , although successful treatment with infliximab was documented [181] . after elimination of the causative drug, pustules usually spontaneously disappear in a few days with desquamation, and the reaction fully resolves within 15 days [183] . the overall prognosis is good, although high fever or superinfection of skin lesions can sometimes lead to life-threatening situations in patients of old age or poor general condition [173] . the mortality rate is about 5 % [4] . the annual incidence of sjs and ten is 1.2-6 and 0.4-1.2 per million individuals, respectively [186, 187] . the annual incidence of sjs and/or ten in hiv patients is estimated at 1-2 per 1000 individuals, approximately 1000-fold higher than that of the general population [188] . the incidence of sjs/ten increases with age; children less than 15 years of age account for only 10 % of the samples in most studies [189] . women are two times more likely to be affected by sjs/ten than men in the adult population, while the male to female ratio is about equal in children [189] . drug exposure is the most common cause of sjs/ten [190] , with more than 200 drugs identified [191] . the groups of medications associated with high risk of inducing sjs/ fig. 25.2 multiple, pin-head sized, non-follicular pustules on erythematous skin on the trunk in a patient with agep ten vary according to the population. in the general population in europe, high risk drugs for sjs/ten include allopurinol, carbamazepine, cotrimoxazole and other anti-infective sulfonamides, lamotrigine, nevirapine, oxicam-nsaids, phenytoin, phenobarbital and sulfasalazine [192] . in the pediatric population in europe, they include anti-infective sulfonamides, phenobarbital, carbamazepine and lamotrogone [189] . in africa, they include antibacterial sulfonamides, nevirapine, tuberculosis drugs, nsaids, antiepileptics, aminopenicillin, analgesics and allopurinol [193] . non-medication triggers, implicated mainly in sjs, include infections, contrast media and vaccinations [194] [195] [196] . alden is an algorithm for the assessment of drug causality in sjs/ten developed by the regiscar study group and consists of 6 parameters according to which the drug causality is classified as very unlikely, unlikely, possible, probable and very probable [197] . usually 4-28 days. the median latency was longer (above 30 weeks) for drugs with no associated risk [192] . sjs and ten represent different degrees of a severe, acute and life-threatening mucocutaneous reaction. we will refer to this disease spectrum as a single entity, namely sjs/ ten. the classification of sjs/ten, defined by bastuji-garin et al. [198] , is based on the extent of epidermal detachment and the findings of characteristic skin lesions (table 25 .4). it should be emphasized that only necrotic skin, which is already detached (e.g., blisters, erosions), or detach-able skin (positive nikolsky sign whereby slight rubbing of the skin results in exfoliation of the outermost layer) should be included in the evaluation of the extent of epidermal detachment [190] . the characteristic skin morphology of sjs/ten consists of 'flat, atypical target lesions' and 'spots/macules', which are defined as follows. flat, atypical target lesions are round lesions, with only two zones and/or a poorly defined border, nonpalpable with the exception of potential central blister. 'spots/macules' are nonpalpable, erythematous or purpuric macules with irregular shape and size, often confluent [198] . epidermal necrosis, the hallmark process of sjs/ten, induces flaccid blisters with positive asboe-hansen sign (lateral extension of bullae with pressure), erosions, positive nikolsky sign, and in severe cases extensive skin sloughing [199] . at least 1 % of epidermal detachment is required for the diagnosis of sjs/ten [83] . in rare instances, extensive epidermal necrosis occurs with only widespread erythema and no evidence of 'flat, atypical target lesions' or 'spots/macules'; these cases were classified as 'ten without spots' (table 25 .4). a characteristic sign of sjs/ten is severe pain and tenderness of the skin [83] . mucosal involvement is evident in most of the cases with erythema, erosions and ulceration, due to necrosis of the epithelial lining [199] . sjs/ten involve more than 2 mucosal sites in 17-71 % of cases [200] . most common sites are oral (fig. 25.3) , ocular and genital mucous membranes, although any mucous membrane may be involved, such as respiratory, gastrointestinal and urethral [199] . fuchs syndrome is a unique type of sjs that involves the mucosa without skin lesions and was reported to be associated with mycoplasma pneumoniae, mostly in children and adolescents [201] . table 25 .4 classification of erythema multiforme major (emm), stevens-johnson syndrome (sjs) and toxic epidermal necrolysis (ten) according to bastuji-garin et al. [198] emm sjs a sjs-ten overlap ten ten with spots ten without spots/ten with widespread erythema systemic involvement systemic findings in sjs/ten include: (1) flu-like symptoms (malaise, fever, anorexia) that are usually the initial signs of the disease in the prodromal phase prior to the cutaneous involvement. (2) epidermal barrier breakdown-related symptoms including hypothermia, dehydration and sepsis. (3) organ involvement induced by necrosis of epithelial lining, including respiratory distress syndrome, colitis, hepatitis and nephritis [199] . characteristic histologic features include extensive keratinocyte destruction via apoptosis with separation of the epidermis from the dermis at the dermoepidermal junction. a paucicellular, dermal mononuclear infiltrate has been commonly described. lymphocytes cross the dermoepidermal junction with moderate infiltration of the epidermis. em and sjs often demonstrate less keratinocyte destruction on a background of extensive dermal mononuclear inflammation [202] . in a retrospective analysis of the clinical records and histologic material of 37 patients with ten, the histologic spectrum ranged from sparse to extensive dermal mononuclear inflammation, the extent of which predicts clinical outcome approximately as well as scorten. increased inflammation correlated with a worse prognosis; a mean cell count of dermal mononuclear >215 cells per high-power field predicted a worse prognosis (65 %) vs 24 % mortality in those with <215 cells in patients with 30 % or more total body surface area sloughing [202] . however, in a retrospective study analyzing clinical records and skin biopsy of 108 patients with sjs, sjs/ten overlap and ten, dermal infiltrate severity was not associated with day-1 scorten or hospital death, but full-thickness epidermal necrosis was associated with mortality [203] . diagnostic criteria based on integration of the major clinical characteristics of skin and mucous membrane findings, pathology assessment, lag period and systemic signs remain to be defined. the management of sjs/ten consists of a multidisciplinary approach that includes the following important aspects: 1. identification and withdrawal of the culprit drug: documenting the medication history during the previous 2 months and withdrawal of all suspected and unessential medications [123] . 2. transfer of the patient to intensive care, burn unit or other specialty unit: supportive care including thermoregulation, fluid replacement, nutritional support, monitoring for infection, sedation and pain management, and psychological support [204] . 3. assessment of skin, mucous membranes and systemic involvement and the scorten score: type of lesions in the skin, extent of epidermal detachment, and mucous membranes and systemic involvement. all patients should be evaluated by an ophthalmologist promptly following the diagnosis and at regular follow-up intervals to minimize potential long-term ocular sequelae [205] . possible acute manifestations include the eyelids, conjunctiva and cornea, and result in the classification of ocular involvement as mild, moderate or severe [206] . bringing other specialists in on the patient's care is decided in accordance with the relevant findings. the scorten system, a severity-of-illness score for toxic epidermal necrolysis, developed to stratify severity of illness and predict mortality in patients with ten, includes seven independent risk factors: age, malignancy, tachycardia, initial body surface area of epidermal detachment, serum urea, serum glucose, and bicarbonate [207] . 4. skin treatment: there are no clinical guidelines for the skin care of patients with sjs/ten. debridement of the necrotic epidermis was recommended in past publications [187, 204] . recent publications advise avoiding debridement, which may cause hypertrophic scars, and recommend considering the detached epidermis as a natural biological dressing that favors reepithelialization [14, 205, 208] . various topical treatments reported include bioactive skin substitutes, semi-synthetic and synthetic dressings, and topical antimicrobials [187, 204] . a recent report on the management of sjs/ten in an experienced french referral center described the following treatment; wound care once a day with minimal manipulation to prevent skin detachment, including a bath containing a solution of chlorhexidine 1/5000 (morphine is given prior to the bath and/or equimolar mix of oxygen and nitrogen monoxide during the bath); if bathing is not possible, the chlorhexidine solution is sprayed 2-3 times daily on the skin, blister fluid is aspirated while maintaining the blister roof, vaseline is systemically applied over all detached skin areas, topical sulfa-containing medications are avoided, and hydrocellular or absorbent nonadhesive dressings are applied at least once daily to cover pressure points [205] . 5. mucous membranes treatment: specialized care is essential to prevent lifelong complications [208] . although there is no standardized care for ocular management, the following supportive local treatment is advised: tear replacement solutions, removal of pseudomembranes, lysis of symblepharon, debridement of loosened epithelium, topical antibiotics to prevent secondary infection, topical corticosteroid to prevent scar formation, and cycloplegic drops to relieve pain, photophobia and ciliary spasm [206] . amniotic membrane transplantation was found effective in the acute and chronic stages of sjs/ten [209, 210] . a 'triple-ten' protocol for severe ocular cases was recently reported [211] , comprised of the following: (1) subconjunctival triamcinolone (kenalog 20 mg) administered into each of the fornices to curb the local inflammatory response without compromising systemic immunity. (2) placement of amniotic membrane tissue mounted on a polycarbonate skirt (prokera) over the corneal and limbal regions to facilitate reepithelialization of the ocular surface. (3) insertion of a steeply curved acrylic scleral shell spacer (technovent, sc21) to vault the lids away from the globe and provide a barrier to symblephara formation. this treatment offers an effective therapeutic option, without the need for microsurgical equipment, microscope, or sutures in the critical care setting. oral-the mouth should be rinsed several times a day with an antiseptic or anifungal solution and the lips lubricated with an ointment such as dexpanthenol [123] . genital-wet dressings or sitz baths and lubrication with emollient are recommended to avoid adhesions and strictures of genital erosions in females [123, 205] . a specialist is required in case of involvement of other mucous membranes: respiratory, gastrointestinal and/or urethral. 6 . systemic immunomodulatory treatment: the optimal therapeutic regimen has yet to be established, but according to recent publications, the following conclusions can be drawn: the use of ivig does not yield survival benefits in sjs/ten [212] ; cyclosporine decreased the death rate and the progression of detachment (dosage of 3 mg/kg/ day for 10 days) [213] ; systemic corticosteroids were associated with clinical benefit according to the euroscarstudy [214] and were reported to be the most common treatment for sjs/ten in a recent survey of 50 drug hypersensitivity experts from 20 countries [14] . one of the suggested protocols is iv dexamethasone 1.5 mg/kg pulse therapy (given for 30-60 min) for 3 consecutive days [215] . treatment with anti-tnf biologic treatment was reported to be beneficial [216] [217] [218] . a prospective, randomized, open-label trial currently underway in taiwan [14] comparing etanercept versus systemic corticosteroids in patients with sjs/ten, reported that the average duration to reach maximal skin detachment and complete skin healing was shorter in the etanercept group. in vitro investigations demonstrated that etanercept, steroids or thalidomide significantly decreased granulysin expression of blister cells. etanercept did not, however, increase the cytotoxic effect to keratinocytes found with thalidomide [14] . 7. causality assessment and communication with the patient and his/her family, health-care providers and regulatory agencies: recent discoveries of specific hlas that predict genetic susceptibility to sjs/ten offer a simple, fast, safe and reliable method for establishing clear causality between a drug and a disease [148] . the hlas are specific to a drug and an ethnic background [148] . since these tests are available only for certain drugs and a negative test does not exclude the drug as the offending agent, additional clinical and laboratory methods are available for assessing causality. the mortality rates of sjs/ten are variable. that of ten may approach 30 % [191] , and that of children with sjs/ten is approximately 2-7.5 % [189] . in a large-scale, populationbased, 1-year follow-up study of 460 sjs/ten patients, the 6-week in-hospital mortality rate was 23 %, and the death rate from 6 weeks to 1 year was 14 % [219] . the mortality rate at 1 year in this study was 24 % for sjs, 43 % for sjs and ten overlap, and 49 % for ten. several factors were found to affect mortality: age, severity of reaction, recent malignancy, preexisting severe kidney or liver disorder, and recent infection. the last two factors were recognized for the first time in this study as being independent risk factors for death. all other factors are part of the scorten [207] . the severity of the reaction was a major risk factor for death in the first few weeks, and severe co-morbidities and older age had major impact on mortality after 6 weeks [219] . early and late physical complications are common among patients who survive sjs/ten [219] , with some 80 % experiencing long-term sequelae [220] . complications may affect multiple organ systems including skin, nails, hair, oral and genital mucosal sufaces, eyes, kidneys, gastrointestinal tract, and respiratory system [221] . ocular complications, which can lead to blindness, are the major long-term morbidity [206] . a few studies have dealt with the quality of life of patients surviving sjs/ten [221] [222] [223] , which was found to be lower in every domain from before hospitalization to follow-up and a low rate of return to previous employment was documented [221] . patients reported concerns about social interactions, fear of taking medications, and fear of contracting an illness necessitating medication [223] . insufficient information and support for patients surviving sjs/ ten was also documented [221] [222] [223] . unfortunately, because of the rarity of sjs/ten, most physicians are not aware of the long-term complications of the diseases [220] . there are several methods to approach a patient with a cutaneous adr. the following is the authors' protocol: clinical assessment of drug-induced skin injury: 4ds by dr. shear a cutaneous eruption in a patient taking a medication should immediately raise the suspicion of a cutaneous adr. the physician must then determine whether the patient's clinical symptoms are signs of a cutaneous adr or of another skin disease not related to a drug. the diagnosis of a cutaneous adr is based on three key clinical elements (fig. 25.4) : (1) appearancethe morphology of the cutaneous eruption according to four main categories of the primary lesion: maculopapular, urticarial, bullous and pustular (see section "morphological classification of cutaneous adrs"). (2) systemicextra-cutaneous signs (fever, dyspnea, lymphadenopathy, etc.) that distinguish between a simple reaction involving only the skin and a complex reaction that includes systemic involvement in addition to the skin (see section "severity of cutaneous adrs: skin only (simple) versus skin and systemic involvement (complex)") and (3) histologyhistopathology and direct immunofluorescence studies of skin biopsies to confirm the clinical impression and to distinguish between a drug-induced eruption and other skin diseases (see section "histological classification of cutaneous adrs"). establishing a differential diagnosis that takes into account all possible diagnoses is essential. ranking the approximate likelihood of each condition is encouraged. all medications, regardless of route of administration, must be considered, especially new drugs taken in the 8 weeks prior to the skin reaction. drugs taken intermittently, such as vitamins, sedatives, pain relievers, laxatives and natural products, must also be considered. assessment of the lag period -the time between initiation of the drug and onset of the cutaneous reaction -is crucial in view of the different lag times for different cutaneous drug reactions. a recommended method for drug exposure analysis is to chart a timeline in order to visualize the chronology and facilitate comprehension of the event. the timeline includes the relevant information (starting day, dosage, and discontinuing day) for each drug and the signs and symptoms throughout the period in question [82] . the most important challenge in assessing drug-induced skin injury is establishing whether there is a causal relationship between the suspected drug and the untoward clinical event. the following methods are helpful: (1) patient history: the patient should be questioned about previous cutaneous reactions to drugs, and whether rechallenge with the drug improved the eruption [82] . these data should also be part of the above timeline. (2) good communication strategies will aid in the interactions with the patient and family following a cutaneous adr and decrease the likelihood of lawsuits, especially in cases of severe reactions such as sjs/ten. physicians are advised to follow these steps: (1) express empathy and say "sorry" according to the "apology laws" in an honest and respectful fashion and in a way that protects the physician from having an apology used against him in case of legal action. http:// www.sorryworks.net/. (2) provide disclosure in a "disclosure meeting" planned according to the acronym cones: context -arrange the setting for a quiet, uninterrupted meeting and decide on the participants; opening shot -the first sentence in the meeting explains the aim of the conversation; narrative -lay out the facts; it is advised to avoid using the words "error" and "mistake" since the adr is a result of multiple factors, particularly when the facts are not completely known; emotions -provide an empathic environment; summary (3) provide the patient with clear information on his cutaneous adr, the name of the offending drug, potential cross-reacting drugs, and drugs which can be safely taken as an alternative to the offending drug. in addition, advise the patient to wear a medic-alert bracelet. (4) family counselling is part of the management plan since the predisposition to some cutaneous adrs may be genetic [191] . information on the adverse event must be provided to the family physician and entered in the patient's records. report the cutaneous adr to the manufacturer and regulatory agencies [225] . the strong associations found between hla alleles and specific drug-induced hypersensitivity reactions have fostered pharmacogenetic testing to prevent the development of lifethreatening drug-induced hypersensitivity reactions, such as sjs/ten and dress. the usefulness of such testing is dependent on a number of factors, including the incidence and severity of the adverse event, the sensitivity and specificity of the predictive markers, and the availability of equally effective, alternative medications for individuals who test positive. although the incidence of sjs/ten is relatively low, it is life-threatening and many patients who survive have longterm sequelae, such as ocular complications. hla-b*1502 is a useful and strong predictive marker with high sensitivity and specificity for carbamazepine-induced sjs/ten in asian populations. this genetic association is strong enough that it prompted the usfda and many countries to relabel the genetic information for carbamazepine, and to recommend screening for hla-b*1502 before prescribing the drug for subjects of asian descent. the hla-b*1502 test for carbamazepine-induced sjs/ten has very high sensitivity (near 100 %) and specificity (97 %). with the 0.25 % prevalence rate of carbamazepine-induced sjs/ten among chinese, the hla-b*1502 test has a 7.7 % positive predictive value and 100 % negative predictive value for detecting [226] . in view of the serious consequences of sjs/ten and the availability of alternative drugs, withholding carbamazepine from screened patients who test positive for hla-b*1502 and switching to alternative antiepileptic drugs is reasonable and feasible in the high risk populations, including chinese and south-east asians. abacavir is used in the treatment of hiv infection, and has been associated with drug hypersensitivity syndrome in 8 % of patients [227] . hla-b*5701 is a strong and useful predictive marker with high sensitivity and specificity for abacavir hypersensitivity in caucasians, prompting the usfda and many other countries to recommend screening for it before prescribing the drug. the hla-b*5701 test for immunologically-mediated abacavir hypersensitivity has very high sensitivity (100 %) and specificity (97.4 %) as well as positive predictive value (55 %) and negative predictive value (100 %) [55] . hla-b*5801 is a potentially useful predictive marker for allopurinol-induced sjs/ten or dress, with 3 % positive predictive value and almost 100 % negative predictive value for detecting allopurinol-induced sjs/ten or dress in chinese (table 25. 2). this association was significant in caucasian and other asian populations as well. the recent american college of rheumatology guidelines for the management of gout recommend hla-b*5801 screening for populations with high frequency of the allele [228] . other recently discovered hla alleles related to drug hypersensitivity of potential usefullness in clinic practice are hla-b*1301 for dapsone hypersensitivity [58] , hla-a*3101 for carbamazepine-related dress [65] , and cyp2c9*3 for phenytoin hypersensitivity [69] . the lymphocyte transformation test (ltt) is a widely used in vitro assay for the diagnosis and identification of offending drugs with t cell-mediated drug hypersensitivity [229] . ltt is based on the activation and proliferation of t cells from pbmc obtained from drug-sensitized patients after stimulation, and incubation with the culprit drug in vitro [230] . following in vitro stimulation by specific drugs, drug-specific t cells are activated and release several cytokines that promote proliferation of t cells. this in vitro proliferation of specific drug-activated t cells can be detected by the incorporation of 3h-thymidine during dna synthesis after 6 days of culture. the results of ltt are expressed as the stimulation index (si): the relationship between the 3h-thymidine uptake in cells (counts per minute (c.p.m.)) with and without the drug antigen [229] . the general sensitivity of the ltt is 50-80 %, varying with different drugs and different phenotypes of delayed-type hypersensitivity reactions; thus, a negative result does not exclude the possibility of drug hypersensitivity. extensive studies on ltt for beta-lactam drugs report even higher sensitivity [230] [231] [232] [233] [234] . the specificity of the ltt is 85-100 % in different studies [231] [232] [233] 235] . ltt for the diagnosis of drug hypersensitivity has limitations. because it is measured by radioisotopes, the sensitivity can be very low and negative results are commonly observed for specific drugs (e.g., allopurinol, lamotrigine) and specific phenotypes (e.g., sjs/ten) [236, 237] . several nonradioactive methods have been developed for measuring lymphocyte proliferation or activation in in vitro tests for diagnosis of delayed-type drug hypersensitivity, including the use of carboxyfluorescein succinimidyl ester (cfse) cell staining dye [238, 239] , and measuring cytokines or cytotoxic proteins expression, such as inf-γ, il-2, il-4, il-5, il-13, granzyme-b, and macrophage migration inhibitory factor [240] [241] [242] [243] [244] . flow cytometry-assisted basophil activation test (bat), which measures specific cell makers such as cd69 or cd203c to quantify basophil activation after antigenspecific stimulation, has been widely used in the diagnosis of immediate-type drug hypersensitivity [245] . bat directly measures basophil responses instead of ige sensitization. it has been applied to the diagnosis of different drugs implicated in immediate-type hypersensitivity, including beta-lactam antibiotics, neuromuscular blocking agents, aspirin, nsaids and radiocontrast media [246] [247] [248] . the sensitivity of bat varies in different types of drugs: that for beta-lactam antibiotics ranged from 28.6 to 55 % [249, 250] ; that for nsaids ranged from 30 to 70 % [251, 252] . recent data have shown that the unique interaction between drug, t-cell receptor and hla molecule is a key factor in the development of immune-mediated adverse reactions to drugs. the discovery of strong association of specific hla alleles with specific drug-induced hypersensitivity (e.g., hla-b*1502 to carbamazepine-sjs/ten, hla-b*5801 to allopurinol-sjs/ten/dress, and hla-b*5701 to abacavir hypersensitivity), and studies of the functional role of hla-b* allele (e.g., hla-b*1502) directly interacting with a specific drug (e.g., carbamazepine) and unique t-cell receptor support the hypotheses of the 'pharmacological interaction with immune receptors' (p-i) [18, 19, 253] . in recent years, bioinformatics and computer modeling have been applied to elucidate how drug molecules interact with specific hla in drug hypersensitivity. hla alleles have been associated with liver injury induced by different drugs (such as flucloxacillin). using silico strategies to examine hla haplotype relationships, and bioinformatics tools, alfirevic et al. [254] demonstrated a connection between the different hla alleles associated with drug-induced liver injury caused by therapeutically and structurally different drugs, suggesting a mechanism of peptide binding of one of the associated hla alleles [254] . computer modeling of the molecular interaction between hla-b*1502 and carbamazepine predicted a favorable drug-binding position in the b pocket of the hla-b*1502 protein, where the side chain of arg62 could form a hydrogen bond with the ketone group of 5-carboxamide of carbamazepine ( fig. 25.5 ) [253] . cutaneous adrs have a wide spectrum of clinical manifestations that may be caused by multiple drugs and different mechanisms. in this decade, our understanding of the pathogenesis of cutaneous adrs had progressed greatly. understanding how a drug can possibly cause reactions in the skin has led to an understanding of the cellular immunology, cytokines and immunogenetics. these key insights can help mitigate the risk of reactions by 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in vitro tests recent applications of basophil activation tests in the diagnosis of drug hypersensitivity a new basophil activation test using cd63 and ccr3 in allergy to antibiotics usefulness of the basophil activation test (bat) in the diagnosis of life-threatening drug anaphylaxis basophil activation and sulfidoleukotriene production in patients with immediate allergy to betalactam antibiotics and negative skin tests diagnosis of immediate-type beta-lactam allergy in vitro by flow-cytometric basophil activation test and sulfidoleukotriene production: a multicenter study the flow-cytometric determination of basophil activation induced by aspirin and other non-steroidal antiinflammatory drugs (nsaids) is useful for in vitro diagnosis of the nsaid hypersensitivity syndrome basophil activation tests in the diagnosis of drug reactions direct interaction between hla-b and carbamazepine activates t cells in patients with stevens-johnson syndrome in silico analysis of hla associations with drug-induced liver injury: use of a hla-genotyped dna archive from healthy volunteers key: cord-343409-oao75pzy authors: hayward, joshua a; tachedjian, mary; cui, jie; field, hume; holmes, edward c; wang, lin-fa; tachedjian, gilda title: identification of diverse full-length endogenous betaretroviruses in megabats and microbats date: 2013-03-27 journal: retrovirology doi: 10.1186/1742-4690-10-35 sha: doc_id: 343409 cord_uid: oao75pzy background: betaretroviruses infect a wide range of species including primates, rodents, ruminants, and marsupials. they exist in both endogenous and exogenous forms and are implicated in animal diseases such as lung cancer in sheep, and in human disease, with members of the human endogenous retrovirus-k (herv-k) group of endogenous betaretroviruses (βervs) associated with human cancers and autoimmune diseases. to improve our understanding of betaretroviruses in an evolutionarily distinct host species, we characterized βervs present in the genomes and transcriptomes of megaand microbats, which are an important reservoir of emerging viruses. results: a diverse range of full-length βervs were discovered in megaand microbat genomes and transcriptomes including the first identified intact endogenous retrovirus in a bat. our analysis revealed that the genus betaretrovirus can be divided into eight distinct sub-groups with evidence of cross-species transmission. betaretroviruses are revealed to be a complex retrovirus group, within which one sub-group has evolved from complex to simple genomic organization through the acquisition of an env gene from the genus gammaretrovirus. molecular dating suggests that bats have contended with betaretroviral infections for over 30 million years. conclusions: our study reveals that a diverse range of betaretroviruses have circulated in bats for most of their evolutionary history, and cluster with extant betaretroviruses of divergent mammalian lineages suggesting that their distribution may be largely unrestricted by host species barriers. the presence of βervs with the ability to transcribe active viral elements in a major animal reservoir for viral pathogens has potential implications for public health. retroviruses (family retroviridae) are a diverse and widely distributed family of rna viruses distinguished by their use of a viral rna-dependent dna polymerase (reverse transcriptase; rt) and ability to integrate into the genomes of their cellular hosts [1] . in addition to the existence of infectious viral particles that are horizontally transmitted between hosts (exogenous retroviruses), the capacity of retroviruses to integrate into the host germline also generates vertically transmissible endogenous retroviruses (ervs) [1, 2] . ervs may or may not be capable of producing infectious viral particles, and germline integration over the course of multiple generations typically leads to the accumulation of mutations that render them defective and non-functional [2] . the retroviral family is composed of seven genera: alpharetrovirus, betaretrovirus, gammaretrovirus, deltaretrovirus, epsilonretrovirus, lentivirus, and spumavirus [3] . the genomic organization of retroviruses is classified as either 'simple' or 'complex' , with simple retroviruses encoding the structural polyproteins gag and env, and the functional polyproteins pro and pol [4] . complex retroviruses encode additional accessory and regulatory proteins with diverse functions that typically establish and maintain virus replication and pathogenesis [5] . the core elements of all retroviruses are flanked by a pair of typically untranslated nucleotide regions at their 5′ and 3′ ends. in the provirus, formed by integration of the viral cdna into the host cell chromosome, these regions are referred to as 'long terminal repeats' (ltr) [4] . exogenous retroviruses of zoonotic origin have been associated with disease in humans, the most notable being human immunodeficiency virus (hiv) [6] . other retroviruses such as human foamy virus (hfv) and human t-cell leukemia virus (htlv) are known to be capable of infecting humans [7, 8] . the retroviruses most recently associated with human disease are betaretroviruses. the up-regulation of gene products derived from the human endogenous retrovirus-k (herv-k) group of betaretroviruses has been linked to a diverse range of cancers such as those of the breast, ovaries, and prostate alongside other significant human maladies [9, 10] . the genus betaretrovirus consists of the type b and type d groups of exogenous and endogenous retroviruses and the herv-k group of endogenous retroviruses. among the exogenous, infectious members of the genus are the type b mouse mammary tumour virus (mmtv), the type d jaagsiekte sheep retrovirus (jsrv), which causes pulmonary carcinoma in sheep, and the type d mason-pfizer monkey virus (mpmv) which causes wasting and immunosuppression in new-born rhesus monkeys [11] [12] [13] . all betaretroviruses utilize variants of the lysine trna primer binding site (pbs) and encode a deoxyuridine triphosphatase (dutpase), within their pro gene which functions as a nucleocapsid-dutpase fusion protein [14] [15] [16] . type b and type d betaretroviruses differ in several respects including their complement of accessory factors, virion morphology, strategies for rna nuclear export, and the length of their ltr regions. type b betaretroviruses contain spherical viral cores and have ltrs of~1,200 nucleotides while type d contain cylindrical viral cores and have ltrs of~300 nucleotides. the prototypical type b betaretrovirus, mmtv, encodes the accessory proteins regulator of export of mmtv mrna (rem) and negative acting factor (naf ), which have roles in viral mrna export, protein synthesis and gene expression [17] [18] [19] , in addition to the virulence factor, superantigen (sag) [20] . the type d retrovirus jsrv has been shown to encode the trans-acting factor rej which has a role in protein synthesis and may assist rna nuclear export [21] . while no distinct oncogenes or sag-like virulence-associated proteins are known to be encoded by type d betaretroviruses, the env protein of jsrv is associated with oncogenesis [13, 14] . there are two major strategies employed by betaretroviruses to export unspliced or partially spliced viral rna from the nucleus that use distinct export pathways. complex betaretroviruses such as mmtv employ a hiv rev-like accessory protein encoded within the env gene that binds and facilitates export of intron containing retroviral rna by recruitment of the cellular karyopherin export factor, chromosome region maintenance 1/exportin 1 (crm1/xpo1) [17, 19] . simple betaretroviruses such as mpmv contain a constitutive transport element (cte) within the nucleotide sequence at the 3′ end of the retroviral genome that recruits a cellular binding factor, tap (nuclear rna export factor 1; nxf1) which mediates nuclear export [22, 23] . importantly, ervs provide a unique opportunity to study the evolutionary history of this family of viruses as they are essentially genetic 'fossils' of past retroviral infections [2, 24] . as such, their existence serves as an indication of the potential host range of a given retroviral lineage and may be interpreted as evidence for the possible existence of exogenous retroviruses that have yet to be isolated. indeed, previous studies have reported a number of endogenous betaretroviruses (βervs) in species for which no exogenous betaretrovirus has yet been identified. these include mammalian species as diverse as primates, horses, rats, lemurs, and an australian marsupial, the common brushtail possum [25] [26] [27] . there are over 1,100 known species of bats (order chiroptera), accounting for approximately 20% of all mammalian species [28] . bats are relatively divergent from other mammals, having branched off from the perissodactyla (containing horses) approximately 88 million years ago (mya) [29] . they are divided into two major groups: megabats (suborder megachiroptera) which are mainly fruit-eating, and microbats (suborder microchiroptera), small insectivores that navigate by means of echolocation [30] . notably, bats harbour over 100 viral species from a diverse range of virus families including the paramyxoviridae, coronaviridae, herpesviridae, rhabdoviridae, arenaviridae, togaviridae, flaviviridae, orthomyxoviridae, reoviridae, bunyaviridae, filoviridae, and picornaviridae [31] . bats, belonging to the mammalian superorder laurasiatheria, are a major viral reservoir that is evolutionarily distinct from another major viral reservoir, rodents, which together with primates belong to the superorder euarchontoglires [29, 32] . bats have recently gained attention as they have been implicated in numerous newly emerging diseases of humans caused by viruses such as sars-coronavirus, hendra virus, nipah virus, and the ebola virus [33] [34] [35] . this track record of zoonotic transmission of previously unknown viral pathogens from bats to humans has prompted calls for a proactive approach to future emerging diseases originating in bats [30] . to this end a natural history survey of bats has begun, and we have recently reported the discovery of diversified defective endogenous gammaretroviruses in both mega-and microbats [36, 37] . previous studies of βervs have tended to focus on isolated viruses, although a report on the βervs of murid hosts indicated that the genus betaretrovirus might possess a diverse and previously unrecognized range of sub-types extending beyond the classical type b/type d paradigm [25] . using transcriptome and genome analyses of the megabats pteropus alecto (black flying fox) and pteropus vampyrus (large flying fox), and the microbats myotis lucifugus (little brown bat), rhinolophus megaphyllus (eastern horseshoe bat), and rhinolophus ferrumequinum (greater horseshoe bat), we herein examine βervs present in a diverse range of bat species. in conjunction with phylogenetic analyses, we incorporated the diversity of genomic organizations and the use of specific lysine trna pbs to identify eight distinct groups of betaretroviruses. to determine if bats contained and expressed a full suite of integrated endogenous betaretroviral genes we generated and analyzed transcriptome databases of p. alecto, r. megaphyllus, and r. ferrumequinum. gag, pol, and env protein sequences were translated from the genomes of extant betaretroviruses: mmtv, jsrv, mpmv, squirrel monkey retrovirus (smr), and simian retrovirus (srv). local tblastn searches were conducted to determine if the transcriptomes contained nucleotide sequences that, when translated into any of their six reading frames, contained significant protein sequence similarity to the betaretoviral protein query sequences. because the variation in length between different transcripts causes difficulty when interpreting relatedness if similarity is expressed as a percentage identity, the significance of the similarity levels observed was determined on the basis of the e-value (probability of random sequence identity) of the blast hits. each transcriptome was found to contain mrna sequences with notable similarity (e-values < 1×10 -10 ) to the betaretroviral proteins gag, pol, and env, with the exception of the r. ferrumequinum transcriptome in which no betaretroviral gag-like transcripts were identified (table 1) . reciprocal blastx searches of the transcript hits with the lowest e-values (i.e. the top hits presented in table 1 ) against the ncbi non-redundant protein database returned predominantly betaretroviral hits. the majority of the mrna sequences identified within the bat transcriptomes were partial, not being of sufficient length to reveal an entire gag, pol, or env gene sequence. as a point of reference, the nucleotide sequence lengths of mpmv gag, pol, and env are 1,974, 2,583, and 1,758, respectively, while the majority of the transcripts identified in the blast analyses were <1,000. the p. alecto transcriptome was found to contain two retroviral transcripts 5,433 and 5,830 nucleotides in length which overlap each other by 3,152 bases with 100% sequence identity. the extent of overlap and perfect identity indicated that the two sequences likely represented a fulllength retroviral genomic sequence >8,103 bases in length that was later determined through phylogenetic analysis to be a βerv. this full-length p. alecto βerv genomic transcript was named paerv-βa (pteropus alecto endogenous retrovirus -betaretrovirus a) ( figure 1 ). in addition to paerv-βa, different transcripts covering the length of one distinct betaretroviral pol transcript (papol-01) most closely related to jsrv pol and one env transcript (paenv-01) similar to type c gammaretrovirus and mpmv-like type d betaretrovirus env were identified in the p. alecto transcriptome. a single transcript (rfenv-01) covering the length of a gammaretrovirus-like env gene most similar to rd114 env was identified in the r. ferrumequinum transcriptome. these transcripts were incorporated into the subsequent phylogenetic analyses. the paerv-βa sequence was found to begin 25 nucleotides upstream of the gag start methionine and contains all of the expected core retroviral genes along with the betaretroviral dutpase domain ( figure 1 ). all of the genes were found to be defective as they each contained frameshift mutations. in addition, the pol and env genes contained premature stop codon mutations. identification of a 19 nucleotide polypurine tract (ppt) allowed the delineation of the beginning of the unique 3′ (u3) region. conserved retroviral active site motifs were present in the protease (dxg), reverse transcriptase (ddd), and integrase (dde) domains. the major homology region (mhr; nucleotide coordinates 1,456 -1,496) and zinc fingers (nucleotide coordinates 1,752 -1,805 and 1,866 -1,919) conserved in gag were also present. two additional orfs were identified; the first overlaps the 3′ end of the pro gene while the second overlaps the u3 region. however, protein translations of the orfs compared to the publicly accessible protein family (pfam) database revealed no known protein domains. in addition, blastp analysis of the translations against the ncbi non-redundant protein database yielded no hits. later identification of closely related p. vampyrus βervs (pverv-βj and pverv-βk) indicated that the orf overlapping the u3 region was not legitimate. given the successful identification of betaretrovirus-like nucleotide sequences in the transcriptomes, we sought to mine the publicly available genomes of p. vampyrus and m. lucifugus for full-length endogenous betaretroviruses. the aforementioned extant betaretoviral protein sequences together with the retroviral mrna sequences identified in the bat transcriptomes were used to conduct tblastn and tblastx searches on the p. vampyrus and m. lucifugus genomes. these searches revealed a number of hits in the genomes that contained betaretroviral gag, pol, and env genes. full-length ervs were delineated by the identification of retroviral gag, pol, and env sequences positioned next to each other and located between a pair of ltrs. in total, we identified 11 full-length βervs in p. vampyrus and six in m. lucifugus (table 2 ). these bat βervs contain all of the expected core elements and the betaretrovirus-specific dutpase domain. as retroviruses were previously categorized based on the specific trna that anneals to their pbs required for initiation of reverse transcription, we determined the specific trna used by all identified bat βervs through nucleotide alignment with known mammalian lysine trna sequences (additional file 1: figure s1 ). the pbs was intact and could be identified in the majority of the bat βervs, and all but one (mlerv-βe) was found to harbour a pbs complementary to either trna lysine 1,2 (lys 1,2) or trna lysine 3 (lys 3) typical of betaretroviruses. reciprocal blastp searches confirmed that the gag, pol, and env of these full-length ervs were more similar to known betaretroviral proteins than those of other retroviral genera with pol sequence similarities ranging from 64% to 76% (additional file 2: table s1 ). all of the bat βervs possessed ltrs of 300-500 nucleotides in length, as expected for type d betaretroviruses with the exception of pverv-βb with ltr length typical of type b betaretrovirues (1265 bp) ( table 2 ). each bat βerv was found to contain a ppt immediately upstream of their 3′ ltr regions. we analyzed each pro and pol figure 1 a schematic representation of paerv-βa. two transcripts were identified in the p. alecto illumina sequenced transcriptome that overlapped by 3,152 nt with 100% sequence identity which were used to assemble the paerv-βa genomic sequence. indicated are the retroviral genes gag, pro, pol, and env, which have been rendered defective by random mutation since integration. also shown are the key enzymatic active sites of the viral protease (d×g), reverse transcriptase (ddd), and integrase (dde); the betaretroviral dutpase domain in pro; two unique open reading frames (orfs); the polypurine tract (ppt); and the (unique 3') (u3) region. orf* does not appear to be genuine, but rather has arisen as a result of an insertion mutation that has disrupted a stop codon. gene and identified the expected enzymatic active site motifs in the retroviral protease (d×g), reverse transcriptase (ddd), and integrase (dde) domains. the gag gene of each βerv contained the expected mhr and zinc-knuckles. while the m. lucifugus genome sequencing coverage was relatively high (7× coverage), the p. vampyrus genome has only been sequenced to 2.6x coverage. the nature of a low-coverage genome such as this means that within the assembled 'scaffolds' there occasionally exist stretches of nucleotides of ambiguous identity. in this regard, several of the bat βervs reported herein contain short 'non-sequenced regions' (nsr) ( table 2) . as a result, the pbs present in pverv-βa and the mhr of pverv-βb could not be identified as they contained nsrs overlapping those elements. to confirm that each βerv was the product of a retroviral integration event, the four-nucleotide repeats known as genomic target site duplication (tsd) sequences that flank the proviruses were identified (additional file 2: table s2 ). tsds were identified for all proviral βervs with the exception of pverv-βd and f whose 5′ ltrs were masked by nsr, the genome size is given for the proviral version of the βervs. § the genome size of paerv-βa is uncertain as the known sequence begins 25nt upstream of the gag gene and does not include the (unique 5') region. b the core retroviral genes gag, pro, pol, and env that contain frameshift or premature stop mutations are described as 'defective' , those that contain neither of these are described as 'intact' in bold font. c the pro open reading frame (orf) of each βerv was found to encode a betaretroviral dutpase protein domain. d the number of orfs that do not code for the core genes and are 300 nucleotides or greater in length. e the length of the long terminal repeats (ltrs). * for those βervs whose 5′ and 3′ ltr lengths differ, the value of the 5′ ltr is given. f the specific lysine (lys) trna complementary to the primer binding site (pbs) for each βerv is given. † the specific identity of the pbs of mlerv-βe is uncertain. nsr: non-sequenced region. pverv-βk whose 3′ ltr appears to be truncated, and pverv-βb which is the sole βerv to have intact and unambiguous ltrs yet no identifiable tsds. to determine if closely related clusters of βervs were generated as a result of post-integration chromosomal duplication events, we compared their flanking chromosomal dna through a blastn analysis (additional file 2: table s3 ). one pair of bat βervs (pverv-βk and pverv-βj) was found to have homology in the chromosomal regions immediately up-and downstream of the proviruses. pverv-βk and pverv-βj appear to have arisen as a result of a duplication of a single integrated provirus. the truncation of the 3′ ltr of pverv-βk suggests a chromosomal duplication event. next, we examined the phylogenetic relationships of the bat βervs identified in our analysis of the bat genomes and transcriptomes (table 2) . accordingly, the gag, pol, and env of the full-length bat βervs were aligned with those of known exogenous and endogenous betaretroviruses and phylogenetic trees were estimated for each ( figure 2 ). in all three trees a great diversity of bat βervs was observed, with individual βervs clustering with members of the type d (e.g. mpmv and jsrv), type b (e.g. mmtv), and herv-k groups. the close relationship between viral sequences derived from transcriptomes and some endogenous viral sequences mined from bat genomes suggests that at least some of the bat βervs have the ability to transcribe. notably, a number of bat βervs (pverv-βj, k and paerv-βa), together with several exogenous betaretroviruses, were found to possess env sequences that formed a cluster so highly divergent, and more closely related to gammaretroviruses, as to require omission from the initial betaretroviral env tree bootstrap values are denoted as ** >90%; * >70% and < 90%. the trees are midpoint rooted for purposes of clarity only. βerv proteins of p. vampyrus and p. alecto are highlighted in red text. βervs of m. lucifugus are highlighted in blue text. the clades within the gag and pol trees highlighted with a grey background (γ-env) contain betaretroviruses whose env sequence is not sufficiently closely related to the env of other betaretroviruses to be included in the env tree. ( figure 2c ). finally, we also found some evidence for within-genome recombination (e.g. mlerv-βc, d and e) as reflected in the phylogenetic incongruence between the gag and pol and env trees. our reciprocal tblastx searches indicated that the p. alecto erv (paerv-βa) and two of the p. vampyrus ervs (pverv-βj and k) encoded env sequences that were more similar to gammaretroviral env, while still possessing gag and pol sequences that closely resembled those of known betaretroviruses (see above). to confirm this observation we undertook a phylogenetic analysis of the env sequences of known gammaretroviruses and betaretroviruses, together with the newly identified βerv env sequences ( figure 3 ). this analysis confirmed previous observations [12, 38] that the env sequences of some extant type d betaretroviruses, namely mpmv, smr and simian retrovirus serotypes 1 and 4 (srv1 and srv4), cluster with gammaretroviral env, as do those of pverv-βj, k, paerv-βa, paenv-01 (env sequence derived from p. alecto), and rfenv-01 (env sequence derived from r. ferrumequinum). other type d retroviruses such as jsrv and the enzoonotic nasal tumor viruses (entv) of sheep and goats did not fall into this cluster. this indicates that a recombination event has occurred, in which a sub-lineage of type d betaretroviruses acquired a gammaretroviral env gene. our analysis of the full-length bat βervs revealed an unexpected diversity of genomic organizations, as a number were found to contain unique orfs. some of these orfs were in alternative reading frames within the core element domains and others were either upstream of gag, or downstream of env. furthermore, the differential use of trna lys 1,2 and trna lys 3 was not found to be restricted to either type b or type d betaretroviruses. rather, it appears that a switch between the two has occurred multiple times throughout the history of the genus. this diversity of genomic organization was used in conjunction with the phylogenetic analyses of gag, pol, and env (with prime consideration given to the highly conserved pol phylogeny) and the trna usage to identify eight distinct groups within the betaretrovirus genus ( figure 4 ). the eight betaretroviral subgroups that we propose are distinguished from each other by major evolutionary differences such as deep phylogenetic divergence with strong bootstrap support (>90% of trees resolving the clade), significant mutations in key genetic features such as a switch to the use of a different pbs, or the presence of retroviral genes from a different genus. group i (represented by herv-k113) consists of the herv-k group of endogenous betaretroviruses which contain a pbs similar to trna lys 1,2 and have a deep phylogenetic divergence from other betaretroviruses. no known exogenous betaretroviruses or bat βervs currently reside in group i. group ii (represented by mlerv-βa) consists of a phylogenetic cluster of endogenous bat βervs that branched off from group i early in betaretroviral history. three bat βervs are included in this group. the pbs of mlerv-βa and mlerv-βb are complementary to trna lys 1,2 and lys 3, respectively, while the trna usage of pverv-βa is unknown as a 100 nucleotide nsr overlaps its pbs. mlerv-βa contains a large 1,493 nucleotide insertion within its 5′ ltr that contains a 323 codon orf. this insertion presumably arose post-integration and the nature of this genetic element is unknown. a pfam domain search and blastp analysis of the translation of the orf against the ncbi non-redundant protein sequence database did not identify any known protein domains or similarity to any known protein. group iii (represented by mlerv-βc) consists of microbat ervs that possess a phylogenetically divergent pol (bootstrap support >90%) and a pbs complementary to trna lys 3. within this group is mlerv-βc, the first fully intact bat βerv to be identified, and which raises the possibility that exogenous members of group iii may yet exist as undiscovered infectious betaretroviruses. group iv (represented by mlerv-βe) appears to have diverged as a part of the type b betaretroviral lineage. however, the precise phylogenetic position of group iv's sole member, mlerv-βe, is not supported by high bootstrap support in any of the trees. furthermore the precise identity of its pbs is uncertain. the pbs does not appear to be specifically complementary to either lys 1,2 or lys 3 trna, but rather it appears to be complementary to an alternative mammalian lysine trna. there are presently no known extra copies of mlerv-βe within the m. lucifugus genome. mlerv-βe is distinguished by its possession of a unique orf upstream of gag. this orf begins within the 5′ ltr and terminates three nucleotides upstream of the gag start methionine, within the same reading frame. orfs upstream of gag may be relevant to gag expression considering that murine gammaretroviruses encode an alternative n-terminally extended version of gag, glyco-gag, that has a role in the promotion of viral replication [39, 40] . no promoter elements or tata boxes were predicted to exist upstream of the orf, however a tata box is predicted within the orf coupled with a possible start methionine downstream, encoding a potential 84 amino acid protein. group v (represented by pverv-βb) consists of archetypically structured type b betaretroviruses (mmtv-like) that contain long ltrs (~1,200 bases). it is possible that the extension of the 3′ ltr has facilitated the emergence of orfs in this location as in the case of mmtv's sag gene. in this regard, pverv-βb has an orf within its 3′ ltr. this orf is 123 codons in length, much shorter than mmtv's sag protein, which is 320 amino acids long. while it is possible that the orf was longer at integration and has simply been interrupted by stop codon mutations since that time, a tblastn analysis of mmtv's sag protein against the 3′ ltr of pverv-βb did not reveal any significant sequence similarity. also in this group is eqerv, an endogenous horse betaretrovirus, which does not contain a sag gene or sag-like orf within its 3′ ltr [27] . group vi (represented by pverv-βd) consists of jsrv-like type d betaretroviruses that contain short ltrs (~300 bases) and env protein sequences that do not phylogenetically cluster with those of the gammaretrovirus genus. members of this group harbour a pbs complementary to trna lys 1,2 and may or may not contain additional orfs within their core element domains, as is the case for jsrv and entv's orf-x located within pol, and pverv-βd, which has an orf overlapping the 3′ end of the env gene. group vii (represented by pverv-βf) consists wholly of bat βervs. group vii members are phylogenetically type d-like and are primarily distinguished by a pbs complementary to trna lys 3 as opposed to trna lys 1,2 which is the expected pbs complementarity for type d betaretroviruses. also, several bat βervs in this group possess a unique orf upstream of gag that is distinct from that of group iv's mlerv-βe. this orf begins within the 5′ ltr and terminates 26 nucleotides upstream of the gag start codon. promoter elements and tata boxes are predicted to exist upstream of this orf. as there were differences in the start position of this orf in the various group vii bat βervs (pverv-βe -i), likely due to random mutation since integration, a nucleotide alignment of the region was generated (additional file 1: figure s2 ). the alignment demonstrated that the consensus orf contained a possible start methionine that would code for a 101 amino acid protein. one member of this group, pverv-βe, is almost fully intact as it does not appear to contain any frameshift mutations and only a single premature stop codon within the pro gene. group viii (represented by pverv-βj) consists of mpmv-like type d betaretroviruses. the distinguishing feature of this group is the possession of an encoded env polyprotein that phylogenetically clusters with those of gammaretroviruses rather than those of other betaretroviruses. the bat βervs in this group have an additional feature which is an orf beginning 40 bases downstream of the env stop codon and terminating 15 bases into the 3′ ltr. this is exemplified in pverv-βj. a nucleotide sequence alignment of the extreme 3′ region (additional file 1: figure s3 ) of the closely related pverv-βj, k, and paerv-βa generated a consensus sequence that contained this orf and revealed that the equivalent orf sequences in pverv-βk and paerv-βa are respectively interrupted by a frameshifting deletion mutation and stop mutation. this orf contains a possible start methionine that would generate a 90 amino acid protein. this alignment also indicated that the alternative orf* in paerv-βa (figure 1 ) was likely to be an artifact as the u3 region contained an eight nucleotide insertion that disrupts a stop codon which, if the insertion did occur after integration, has generated an artificial orf. the paerv-βa genome was derived from illumina based transcriptome sequencing while the pverv-βj and pverv-βk genomes were derived through wholegenome shotgun/sanger sequencing. accordingly, each method can be used to orthogonally verify the other. a full alignment of the three proviruses (additional file 3: figure s4 ; demonstrating 96.66% nucleotide identity between pverv-βj and pverv-βk and 93.77% between pverv-βk and paerv-βa) supports the veracity of these proviral sequences and provides further evidence that the group viii βervs are likely derived from a single integration event. the unique orfs identified in the bat βervs of all groups were subjected to a blastp analysis against the ncbi non-redundant protein database and pfam domain search. however, no blast hits or known protein domains were identified. to determine if the groupings we had assigned were congruent with known functional differences between retroviruses with respect to betaretroviral rna nuclear export strategies, we analyzed the bat βervs, alongside known exogenous and endogenous betaretroviruses, for evidence of motifs indicative of the major export strategies (additional file 2: table s4 ). to this end we employed a computational analysis to search for the presence of nuclear localization signals (nls) and nuclear export signals (nes) common to the retroviral rev-like proteins used in the archetypal rev/rev-responsive element (rre) equivalent export mechanism. we also searched for the presence of tap-binding elements (tbe) within and downstream of the env gene, which would imply the utilization of the cte export pathway, and for direct nucleotide repeats (dr) and inverted nucleotide repeats (ir) that might suggest the formation of stem-hairpin-loop structures known to be associated with the cte [23] . while a number of βervs were predicted to contain either an nls or an nes, only mlerv-βb and pverv-βb were found to contain both. these βervs broadly cluster with herv-k and mmtv, which respectively encode the rev-like proteins rec and rem, and the presence of both nls and nes points to the possibility that they encode rev-like proteins and make use of the crm1 nuclear rna export pathway. the majority of the βervs in group vii were found to contain tbe, indicating that the original exogenous forms of these retroviruses likely utilized the nuclear export pathway accessed by the cte. we used an analysis of the ltrs to estimate the time since integration of the bat βervs. this analysis evaluated the extent of the difference between the nucleotide sequences of the 5′ and 3′ ltrs of each βerv, which are expected to be identical at the time of integration. the number of nucleotide differences between the 5′ and 3′ ltr is assumed to be proportional to the time since integration, although this may be compromised by such factors as gene conversion [41] . under this assumption, all βervs integrated into the genomes of the ancestors of modern bats within a wide time range of between 3.2 and 36.3 million years ago (mya), and hence long after the divergence of bats from other mammalian lineages (table 3) . this, in turn, suggests that (i) that the original exogenous forms of these βervs targeted ancient bats, and (ii) there has been a continual integration of betaretroviruses into bat genomes during their evolutionary history. we coupled our analysis of the genomic features of the bat βervs with the phylogenetic patterns observed in the gag, pol, and env trees (with primacy given to the phylogeny of the highly conserved polymerase sequences) to generate a hypothetical series of events that may have led to the current state of diversity in the genus betaretrovirus ( figure 5 ). our analysis indicates that while the ancient progenitor betaretrovirus likely made use of a trna lys pbs, its specific identity is uncertain. groups i and ii appear to have branched off together early in betaretroviral history. this has led, in the case of the herv-k betaretroviruses, to the emergence of distinct genetic elements such as the np9 and rec proteins, whose current endogenized forms have possible roles in tumorgenesis [42, 43] . group iii's phylogenetic position places its point of divergence after the split of groups i and ii but prior to the split between the type b and type d lineages. the divergence between type d and type b βervs seems to have occurred as a result of their differential use of trna lys 1,2 and trna lys 3, respectively. within the type b lineage are groups iv and v which, although possibly splitting after the divergence of type b and type d, differ in the length of their ltrs, their trna usage, and their additional genetic elements. within the type d lineage an early event appears to have been a recombination between a betaretrovirus and a gammaretrovirus, which has caused a divergence between jsrv-like and mpmv-like type d betaretroviruses. in this split, group viii appears to have diverged from groups vi and vii through the acquisition of a gammaretroviral env gene. group vii later diverged from group vi by a switch from the use of trna lys 1,2 to trna lys 3 and differentiation of their additional orfs. we searched for the expression of betaretroviral genes in the transcriptomes of the megabat p. alecto and the microbats r. megaphyllus and r. ferrumequinum. through this analysis we determined that betaretroviral genes were being transcribed into mrna within each species and we identified that a full-length genomic transcript of a betaretrovirus (paerv-βa) was being expressed in p. alecto. as each of the genes of paerv-βa were found to contain mutations that likely rendered them non-functional, it seems reasonable to conclude that the transcript was expressed from a defective βerv rather than a functional exogenous betaretrovirus. it is important to note that we cannot exclude the possibility that the reported paerv-βa transcript was derived from multiple similar sequences during transcriptome assembly and due to recombination between similar transcripts during cdna synthesis or pcr as published [44] . our analysis of the genomes of the megabat p. vampyrus and the microbat m. lucifugus revealed that they contain a genetically diverse range of full-length βervs. in the case of m. lucifugus this included an intact βerv (mlerv-βc) that did not contain any mutations that would clearly render the gene products non-functional. however, it should be noted that as revealed by the ltr analysis, nucleotide substitutions have occurred in the mlerv-βc sequence. while the critical enzymatic active site motifs are intact, whether or not the nucleotide substitutions that have occurred in the coding domains would have a detrimental effect on the functionality of the gene products is not known. in analyzing the genetic content of the full-length βervs for the presence of orfs, aside from those coding for the core genes, we set a minimum cut-off of 100 [25] . nd: not dated; these βervs could not be dated using this method. pverv-βd and pverv-βf contained non-sequenced regions within their 5′ ltr, while pverv-βg and pverv-βk contained bulk deletions within their 3′ ltrs. codons to limit the amount of incidental non-coding orfs that would be identified. however, many retroviral accessory and regulatory genes, such as rec and np9 of herv-k and vpr and tat of hiv-1, are shorter than 100 codons and are often encoded over the span of two exons. despite the high minimum cut-off, it is striking that the bat βervs possessed a diverse array of additional orfs. while we cannot confirm that these are indeed protein coding domains, much less speculate on their function, the existence of similar elements is not without precedent among the betaretroviruses. one example is the 'orf x' of jsrv, the function of which is unknown but it has been found to be broadly conserved amongst jsrv isolates [45] . several of the orfs we identified overlap the proviral ltrs, which consist of typically untranslated regions. this is also not unprecedented, with a prime example being the sag gene of the betaretrovirus mmtv, which is situated entirely within the u3 region of the 3′ ltr. the presence of unique orfs in βervs may indicate the evolution of novel retroviral genes whose products have regulatory or accessory functions required for the retroviral life-cycle and/or pathogenesis. in addition to the βervs reported in this study we noted the presence in both mega-and microbats of betaretrovirus-like retroelements that resemble βervs but lack the env gene; these were not investigated further (data not shown). we reported each βerv as a distinct entity. nevertheless it is reasonable that some of their number, particularly the βervs within each of groups vii and viii, represent a common progenitor infectious betaretrovirus that has undergone duplication events via retrotransposition or recombination since an original, single integration event. for example, the integration time of pverv-βj coupled with its similarity to paerv-βa and pverv-βk may mean that these βervs originated from a single integration into the genome of the common ancestor of p. vampyrus and p. alecto and that at least a single duplication event has occurred within p. vampyrus (or the common ancestor). however, it is also arguable that multiple integrations of closely related infectious retroviruses separated from each other by perhaps a small number of infectivity cycles occurred. we attempted to address this question by a comparative analysis of the flanking genomic dna located immediately up-and downstream of the proviruses and by identifying the tsd that border each provirus and arise as a by-product of the integration mechanism [46] . unique tsd indicate distinct integration events. in the case of the group viii βervs a tsd for pverv-βk could not be identified as its 3′ ltr appears to be truncated. this may indicate that it is a copy of pverv-βj that has arisen through a chromosomal duplication event. this appears to be confirmed by the identification of genomic dna bordering pverv-βj that is homologous to genomic dna flanking pverv-βk. as paerv-βa is a genomic transcript it does not contain tsd. in the case of group vii βervs all of the identifiable tsd differ from one another, indicating separate integration events. additionally, no flanking genomic dna homology was identified amongst the members of the group. notably, both the phylogenetic and ltr analyses revealed a great diversity of βervs in bat genomes. our molecular clock dating suggested that the earliest viral incorporation event occurred at approximately 36 mya which is older than the separation of the megabats and microbats studied (around 20 mya) [28] . in addition, it is clear that some of the βervs present in bat genomes were vertically transmitted from their ancestors; e.g. mlerv-βa and pverv-βa are grouped together and are of similar age having been integrated approximately 30 mya. however, it is also the case that many of the bat βervs formed via independent viral invasion and incorporation as they have different phylogenetic positions as well as different estimated ages of integration. in addition to their genomic diversity, we observed that a number of phylogenetic clusters within the genus differed in their more fundamental aspects. specifically, the use of trna lys 1,2 or trna lys 3 was not restricted to the divide between type b and type d betaretroviruses, and a clade that was distinct in both gag and pol trees possessed a gammaretroviral env gene. this prompted us to define eight sub-groups (group i-viii) within the genus that accounted for these fundamental differences in the context of phylogenetic divergences at the amino acid level of the core polyproteins. our ltr analysis also revealed that bats have been infected with betaretroviruses for most of their evolutionary history. this supports the notion that bats are a potential reservoir for infectious betaretroviruses. a previous study reported a short, partial retroviral sequence (cperv-β5, ac138156) in the genome of the microbat carollia perspicillata (seba's short-tailed bat) [25] . however, this sequence contained large deletions, was missing the entire pro and pol genes, and only fragments of the gag and env genes remained. the partial env of cperv-β5 most closely matched the env of the betaretrovirus smr and on that basis it was reported as a betaretroviral sequence. in this study, we report a series of complete βervs in mega-and microbat genomes representing the breadth of the genus betaretrovirus. although cperv-β5 does contain a lysine trna-specific pbs, without a pol gene to phylogenetically differentiate it or the presence of the characteristically betaretroviral dutpase domain within pro, it cannot be known with certainty whether it is a group viii betaretrovirus or a gammaretrovirus. the study by ballie et al. [25] and a recent study by anai et al. [47] both noted the similarity between the env of type c gammaretroviruses and some type d betaretroviruses which was attributed to a likely recombination event. we have shown that the betaretroviruses, which possess a gammaretrovirus-like env, form a single clade in both gag and pol phylogenies. this indicates that a single recombination event produced these group viii betaretroviruses. furthermore, the typical mammalian gammaretroviral use of trna proline and glycine-specific pbs and the absence of dutpase domains from their pro genes [14] can be used to infer that the nature of the recombination event was the insertion of a type c gammaretroviral env gene into a type d betaretrovirus. previous studies also determined a recombinatorial origin for the type d env [12, 38] . however, this conclusion was reached prior to the sequencing of the genome of jsrv [48] , which does not possess a gammaretrovirus-like env, and its subsequent classification as a type d retrovirus. as such, it was hypothesized that it was this recombination event that gave rise to the type d lineage of betaretroviruses [12, 38] . our analysis aimed to provide a clarification of the differences between, within, and outside of the type b and d groups of betaretroviruses. accordingly, we suggest that the fundamental feature giving rise to the division between the type b and d lineages may have been the use of different primer binding sites, not the possession or not of a type c env gene, which appears to be a more recent and more significant lineage divergence within the type d group. ballie et al. [25] described seven groups within the genus betaretrovirus. these groupings were made solely on the basis of pol gene nucleotide sequence similarity. while manually determining amino acid sequences from genes that contain frameshift mutations is difficult, when the manual reconstruction is closely informed by the alignment of each translated frame against known betaretroviral polymerases, amino acid sequence reconstruction is a viable option. as such, our phylogenetic analyses differ from those undertaken previously in that they are based on amino acid sequence alignments, and our groupings are based on differences in the fundamental genomic features in addition to phylogenetic clustering. tristem [49] reported on the identification and classification of the highly diverse endogenous retroviruses present in the human genome (hervs) and suggested that trna pbs specificity, in addition to the polymerase phylogeny of endogenous retroviruses, should inform their classification. this is because even if the ervs of a given species cluster together in phylogenies, the use of different trna pbs may be evidence of separate origins. indeed, that study made the assumption that hervs with alternative pbs homologies were derived from cross-species transmissions. with this in mind, we analyzed the pbs sequences of the identified βervs and used this information to aid and inform the delineation of our grouping scheme. mammalian cells restrict the export of intron containing mrna from the nucleus to the cytoplasm, and betaretroviruses have been found to utilize two different mechanisms to circumvent this restriction and export unspliced genomic rna and singly-spliced env mrna. the type b betaretrovirus mmtv, and the herv-k endogenous retroviruses are known to use rem and rec, respectively, which are hiv rev-like export proteins, that possess equivalent mechanisms of action [17, [50] [51] [52] . the type d betaretroviruses mpmv and srv make use of the cis-acting cte, which in the absence of a retroviral accessory protein, recruits cellular proteins to effect nuclear export of intron containing viral rna [22, 23] . this apparent dichotomy has been complicated by recent lines of investigation that have found that i) mmtv likely possesses a second, rem-independent mechanism for the export of singly-splice env mrna [52] ; and ii) the type d betaretrovirus jsrv contains both a cte and a rev-like protein, rej, which while found to possess a primary function related to gag synthesis, also enhances rna export in some cell types [21, 53] . this indicates that betaretroviruses may make use of multiple export mechanisms, possibly providing some measure of redundancy to promote productive replication in different contexts. we conducted a computational analysis to predict the presence of rna export motifs that would indicate which mechanism was utilized by each βerv. we found that bat βervs, clustering with betaretroviruses known to utilize the crm1 export pathway, typically contained one or both of the nls and nes motifs, suggesting that they too encode a rev-like protein. it was not surprising that some βervs were predicted to contain one motif but not the other, as random mutation since integration is expected to interfere with sequence-based motif prediction. it is also possible that the nes of some betaretroviral rev-like proteins (such as is the case for herv-k rec) are encoded at the exon boundary and/or within a frame different to that used by env, making the prediction of nes from the env protein sequence challenging. a number of βervs in group vii were found to contain retroviral tap-binding motifs, defined as published [23] , implicating their use of the cte:tap export pathway. the presence of putative nls and nes in some group vii βervs suggests that rev-like elements may also be present. as rev-like proteins are encoded within the env gene, the recombination event that replaced the betaretroviral env with a gammaretroviral env and gave rise to group viii would have caused the incidental loss of any encoded rev-like protein. such a lineage would only have remained viable if it either possessed an alternative mechanism for export, or never made use of a rev/rre equivalent export mechanism in the first place. that rev-like proteins are widely distributed amongst the betaretroviruses suggests that it is not unreasonable that the progenitor of group viii did possess a rev-like protein. this possibility is supported by the existence of the rej protein of jsrv, as jsrv clusters alongside group viii in the type d lineage. in addition, several bat βervs in groups vi and vii contain putative nls and nes motifs, suggesting that members of these groups contain rev-like elements. if group viii did lose a rev-like protein upon acquisition of a gammaretroviral env, then two explanations for the lineage's survival are apparent: i) the recombination event was confined to env and the betaretroviral cte possessed by mpmv and srv, which is located immediately downstream of env, already existed as a redundant export mechanism and remained after the event, or ii) the recombination event included the nucleotide sequence downstream of the env gene, and a putative cte-like element was acquired in the process. with regard to the second possibility it is important to note that the mrna nuclear export mechanism of gammaretroviruses has not been elucidated and the proposal of a cte-like element remains hypothetical. however, this notion is supported by the observation that accessory proteins have not been reported for gammaretroviruses, expression of unspliced and singly-spliced viral mrna would require nuclear export, and that a cte-like cisacting nuclear export element would necessarily be located in singly-spliced env mrna. in either event, our analysis leads to the surprising implication that the betaretroviruses are part of a fundamentally complex retroviral genus and that one lineage, group viii, has evolved through gene replacement into a simple retrovirus sub-group that does not possess any distinct accessory proteins or virulence factors. using the phylogenetic analysis of retroviral pol sequences we proposed a pathway through which the genus betaretrovirus may have evolved from its progenitor. this hypothetical evolutionary history paints an interesting picture of a broad and diverse retroviral genus whose distribution may be largely unrestricted by host species barriers. the βerv members of a number of groups are represented in hosts who are distantly related, such as group viii, which contains host species from bats, primates, rodents, and marsupials. this suggests that cross-species transmission of betaretroviruses is a likely and common occurrence, such that betaretroviruses may be particularly adept at evading host defences. this possibility is intriguing, particularly in light of the wide array of additional orfs found within the genus that hint at the existence of as yet undiscovered betaretroviral accessory and virulence factors; these could, for example, act as countermeasures to circumvent the action of host intracellular restriction factors that are known to act as barriers to cross-species transmission [54] . the wide distribution of diverse βervs in bats and rodents suggests that these two largest groups of mammals play a major role as both hosts and cross-species transmitters for betaretroviruses. bats and rodents are globally distributed, appearing on all continents with the exception of antarctica [30, 55] . as such it appears reasonable to postulate that they have both played a large role in the global spread and evolution of betaretroviruses. we have demonstrated the presence of a range of βervs in mega-and microbats that possess a diversity that cannot be confined to the classical type b/type d division. among their number we identified an intact βerv that may be capable of producing infectious virions, and our ltr analysis indicates that betaretroviruses have been circulating in bat populations throughout their evolution and likely still do. our evidence that bats have carried a range of exogenous infectious betaretroviruses and that cross-species transmission has been commonplace has important implications for disease emergence. indeed, the reported association between the betaretrovirus mmtv and human breast cancer and primary biliary cirrhosis may mean that betaretroviral zoonosis is already causing disease in humans [56] [57] [58] . urban expansion into the natural habitats of bats is gradually increasing the amount of overlap between bat and human environments, and with it the amount of contact between bats and humans [59] . in many countries the practice of hunting bats as a source of consumable bushmeat is common [60] . these circumstances provide the opportunity for retroviral transmission between bats and humans. we propose that the transmission of a betaretroviral infection from bats into humans is possible. as such, it is imperative to continue to survey those viruses present in bats. approval for the use of bat tissue was granted by the australian animal health laboratories animal ethics committee (protocol aec1281) and by the animal ethics committee of east china normal university (approval number 20110224). p. alecto transcriptome datasets were generated from the non-stimulated thymus tissue of a healthy male juvenile bat and the pooled total rna obtained from mitogen-stimulated spleen, white blood cells, and lymph node and the unstimulated thymus and bone marrow obtained from one pregnant female and one adult male as described previously [61] . the p. alecto transcriptome is accessible through the ncbi sequence read archive (http://www.ncbi.nlm.nih.gov/traces/sra/) [sra: srp008674]. the r. ferrumequinum transcriptome was generated using whole brain tissue as published [37] . the p. alecto and r. ferrumequinum transcriptomes were sequenced using the illumina next-generation sequencing (ngs) platform as described previously [37, 61] . the p. alecto transcriptome was assembled using velvet, oases, and mira software packages as described previously [61] . the r. ferrumequinum transcriptome was assembled using the brujin graph and soapdenovo software packages as described previously [37] . the generation of the r. megaphyllus transcriptome was conducted as follows: four wild bats, (one female and 3 male) were caught in the booloumba creek caves in queensland, australia in november 2006 and tissues from brain, kidney, large and small intestines, liver, lung, spleen, heart, skin, bone and reproductive organs were pooled and stored in rnalater (ambion). total rna was isolated from the 12 pooled bat tissues using the qiagen rneasy kit. dna was prepared from purified total rna (2.5 μg per cdna reaction) using the evrogen mint cdna synthesis kit (cat # sk001) but with a modified oligodt adapter primer containing the recognition sequence for gsui (5′ agcagtggtatcaacg cagagt ctggag(t) 20 vn). the cdna was normalized with a duplex specific nuclease (dsn) using a modification of the protocol described in the evrogen trimmer cdna normalization kit (cat # nk001). after the second limited pcr amplification (12 cycles) with the m2 primer, pcr buffer, primers and enzyme were removed using the machery nagel nucleospin ii kit. dna was then digested overnight with gsui to remove the 3′ polya tail adapter sequence so as to remove stretches of homopolymer ts and as which can effect the 454 sequencing run due to cross-talk (homopolymer flash). five micrograms of normalized amplified double stranded cdna was purified using the machery nagel nucleopsin kit with the selective removal of the gsui digested 43 base pair (bp) 3′polya adapter sequence using a modification of the binding conditions. library preparation for roche 454 sequencing for the gs flx platform was performed by the australian genome research facility ltd, st lucia, queensland with sequence output of 74 mb, 374,360 single-end reads with an average read length of 239 bp. clc genomics workbench version 4.5.1 (clc bio, aarhus, denmark) was used to trim reads based on quality and to remove the evrogen normalization primer sequence, subsequent 337,805 reads were de novo assembled using clc genomics workbench default settings and blast databases were prepared using either de novo assembled or trimmed unassembled reads. the gag, pol, and env genes of each genome sequence were translated into protein sequences using the clc main workbench 6.6 (clc bio). to identify the transcripts of interest we used the tblastn function of the clc main workbench incorporating the following parameters: blosum62 matrix, word size = 3, e-values < 1×10 -10 , gap costs of existence 11, extension 1, and low complexity filtered. to confirm that the transcripts identified were more similar to betaretroviruses than other retroviral genera we performed a reciprocal blast analysis of each transcript against the ncbi non-redundant protein database (http://blast.ncbi.nlm. nih.gov/blast.cgi) using the blastx function of the clc main workbench with the following parameters: blosum80 matrix, word size = 3, e-values < 1 × 10 -10 , gap costs of existence 10, extension 1, low complexity filtered, and limit by entrez query = viruses. annotated sequences of the full-length betaretroviral sequences included in the phylogenetic analyses (paerv-βa, papol-01, paenv-01, and rfenv-01) are included as additional file 4. we generated the genomic sequence of paerv-βa using two transcripts identified in the p. alecto transcriptome during the initial blast analysis which were aligned using the clc main workbench and trimmed by 245 and 401 nucleotides at the 5′ and 3′ extremities of their overlapping region, respectively. to determine the presence of full-length βervs in mega-and microbats we retrieved the genomes of m p. vampyrus and m. lucifugus from the ensembl database (http://www.ensembl.org/index.html). we searched for genomic sequences with similarity to the aforementioned extant betaretroviral proteins by conducting a tblastn analysis of the genomes using the clc main workbench with the following parameters: blosum62 matrix, word size = 3, e-values < 1×10 -10 , gap costs of existence 11, extension 1, and low complexity filtered. we searched for genomic sequences with similarity to the betaretroviral transcripts identified in the bat transcriptomes by conducting a tblastx analysis of the genomes using the clc main workbench with the following parameters: blosum80 matrix, word size = 3, e-values < 1×10 -10 , low complexity filtered. to sort fulllength from fragmented βervs and various other retroelements within the blast output, a script was created using microsoft office excel 2003 (microsoft corporation, redmond, usa) that compared the blast data for the gag, pol, and env analyses and identified scaffolds that emerged as a hit in each. the long terminal repeats (ltrs) which were used to delineate the full-length βervs were identified by subjecting each identified gene scaffold to a blastn analysis in which the entire sequence was aligned with itself to identify repeated sequences using the following parameters: word size = 11, match score = 1, mismatch score = −3, gap costs of existence 5, extension 2, and low complexity filtered. transcription promoter elements within the 5′ ltrs of the βervs were predicted using the online promoter predictor tool nnpp 2.2 [62] (http://www.fruitfly.org/ seq_tools/promoter.html). tata boxes were predicted using the hamming-clustering method through the online hctata tool [63] (http://zeus2.itb.cnr.it/~webgene/ wwwhc_tata.html). poly(a) signal sites were predicted using the hamming-clustering method through the online hcpolya tool [63] (http://zeus2.itb.cnr.it/~webgene/ wwwhc_polya.html). primer binding sites were identified by an alignment of the genomic nucleotide sequence between the 5′ ltr and the beginning of the gag gene of each βerv against the university of strasbourg's online trna database [64] (http://trna.bioinf.uni-leipzig. de/dataoutput/search) using the associated blast tool (default parameters). open reading frames (orfs) were identified within each βerv using the clc main workbench. the dutpase protein domains and nucleocapsid zinc knuckles were identified by subjecting the translated gag and pro genes to a protein family (pfam) domain search [65] through the clc main workbench using the publicly accessible pfam database (http://pfam. sanger.ac.uk/). the conserved major homology region (mhr) of gag and enzymatic active sites of the retroviral protease (dxg), reverse transcriptase (ddd), and integrase (dde) were identified through a protein sequence alignment, using the create alignment function of the clc main workbench, between the gag, pro, and pol of each bat βerv against those of the aforementioned extant betaretroviruses. prediction of rna export elements nls and nes were predicted by analyzing the env, or if known, the rev-like protein sequence of each betaretrovirus. nls were predicted using the online tool cnls mapper [66] (http://nls-mapper.iab.keio.ac.jp/ cgi-bin/nls_mapper_form.cgi) with a prediction score threshold of 3.0. nes were predicted using the online tool netnes 1.1 [67] (http://www.cbs.dtu.dk/services/ netnes/). the strength of each nes prediction within the env/rev-like protein is defined as strong if the scores for the neural network model and hidden markov model, together with the overall nes score, are above the algorithm-assigned threshold. the strength is weak if one of the scores is below the threshold. no nes is predicted for proteins in which more than one score is below the threshold. tbe, dr, and ir were identified by subjecting the nucleotide sequence within and downstream of env ending at the poly(a) signal site within the 3′ ltr of each betaretrovirus to a blastn analysis in which the sequence was aligned against itself to identify repetitive elements using the following parameters: word size = 11, match score = 1, mismatch score = −3, gap costs of existence 5, extension 2, and low complexity not filtered. all nucleotide and protein alignments were conducted using the create alignment function of the clc main workbench except where stated otherwise. to determine the evolutionary relationships among the different bat betaretroviruses we inferred the phylogenetic relationships among the gag, pol and env amino acid sequences. all of the reference sequences were downloaded from ncbi (additional file 2: table s5 ) and aligned with bat sequences using muscle [68] . we employed the gblocks program [69] to remove regions of high sequence diversity and hence uncertain alignment. phylogenetic relationships were then inferred using the maximum likelihood (ml) method available in phyml 3.0, employing spr (subtree pruning and regrafting) branch-swapping [70] and incorporating 1,000 bootstrap replications to determine the robustness of each node. the prottest 2.4 program [71] was used to select the best-fit model of amino acid substitution, which was found to be lg+i+г for all data sets. a time-scale for βerv evolution was established as described previously [36] and employing the bayesian markov chain monte carlo method (mcmc) available in the beast v1.7 package [72] . we first acquired the genomic substitution rates (r) for mega-and microbats. for this, divergence times of mega-and microbats were taken from the fossil record [28] and used to calibrate date estimates for the rest of the species tree, assuming an uncorrelated lognormal relaxed molecular clock. all phylogenetic trees were inferred using the gtr substitution model and the yule speciation prior, and the beast analyses were run until all relevant parameters converged, with 10% of the mcmc chains discarded as burn-in. the estimated substitution rates were then used to calculate the age of each βerv using the following formula: t=(d/r)/2, where t is the invasion time of each βerv (million years), d is the number of differences per site among the both 5′ and 3′ ltrs, and r is the genomic substitution rate (substitutions per site per year). the genbank accession numbers of the retroviruses used in this study are listed in additional file 2: table s5 . additional file 1: figure s1 . alignment of extant and bat betaretroviral primer binding sites (pbs). the pbs of bat endogenous betaretroviruses and those of known extant and exogenous betaretroviruses are aligned and grouped according to the specific lysine trna complementary to the pbs. *the pbs complementarity of mlerv-βe is uncertain. figure s2 . alignment of the orf present in the group vii endogenous betaretroviruses (βervs) of bats. the region from the beginning of the 5 ′ ltr to the beginning of the gag gene of each group vii bat βerv was aligned and a consensus sequence generated. the annotations belong to the consensus sequence and depict the 5 ′ ltr, predicted promoter element and tata boxes, the pbs complementary to trna lys3 (lys 3 pbs), and an open reading frame (orf). figure s3 . annotated alignment of the group viii endogenous betaretroviruses (βervs) of bats. the region from the end of the env gene to the 3 ′ long terminal repeat (ltr) of each group viii bat βerv was aligned and a consensus sequence generated. the annotations belong to the consensus sequence and depict an open reading frame (orf), the beginning of the 3 ′ ltr, and mutations in paerv-βa and pverv-βk that influence the presence of orfs. additional file 2: table s1 . comparison of βerv polymerase sequences to those of known betaretroviruses. table s2 . identification of the target site duplications (tsd) flanking endogenous betaretroviruses. table s3 . comparison of the 5 ′ and 3 ′ flanking regions of phylogenetically clustered βervs. table s4 . analysis of betaretroviral rna export motifs. table s5 . genbank accession numbers and ensembl database locations of the retroviruses used in this study. historical introduction to the general properties of retroviruses studies of endogenous retroviruses reveal a continuing evolutionary saga retroviral virions and genomes converging strategies in expression of human complex retroviruses origin of hiv-1 in the chimpanzee pan troglodytes troglodytes persistent zoonotic infection of a human with simian foamy virus in the absence of an intact orf-2 accessory gene human t-cell leukemia virus type 1 (htlv-1) and leukemic transformation: viral infectivity, tax, hbz and therapy identification, characterization, and comparative genomic distribution of the herv-k (hml-2) group of human endogenous retroviruses expression of human endogenous retrovirus type k envelope protein is a novel candidate prognostic marker for human breast cancer mouse mammary tumor virus p75 and p110 cux1 transgenic mice develop mammary tumors of various histologic types nucleotide sequence of mason-pfizer monkey virus: an immunosuppressive d-type retrovirus sheep retrovirus structural protein induces lung tumours retroviral taxonomy, protein structures, sequences, and genetic maps barabás o: dutpase and nucleocapsid polypeptides of the mason-pfizer monkey virus form a fusion protein in the virion with homotrimeric organization and low catalytic efficiency flexible segments modulate co-folding of dutpase and nucleocapsid proteins mouse mammary tumor virus encodes a self-regulatory rna export protein and is a complex retrovirus naf, a trans-regulating negativeacting factor encoded within the mouse mammary tumor virus open reading frame region a novel, mouse mammary tumor virus encoded protein with rev-like properties a maternally inherited superantigen encoded by a mammary tumour virus identification and mutational analysis of a rej response element in jaagsiekte sheep retrovirus rna a small element from the mason-pfizer monkey virus genome makes human immunodeficiency virus type 1 expression and replication 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diverse groups of endogenous gammaretroviruses in mega and microbats discovery of retroviral homologs in bats: implications for the origin of mammalian gammaretroviruses receptor interference groups of 20 retroviruses plating on human cells gag-related polyproteins of moloney murine leukemia virus: evidence for independent synthesis of glycosylated and unglycosylated forms moloney murine leukemia virus glyco-gag facilitates xenotropic murine leukemia virus-related virus replication through human apobec3-independent mechanisms on the estimation of the insertion time of ltr retrotransposable elements a novel gene from the human endogenous retrovirus k expressed in transformed cells human endogenous retrovirus rec interferes with germ cell development in mice and may cause carcinoma in situ, the predecessor lesion of germ cell tumors analysis of 454 sequencing error rate, error sources, and artifact recombination for detection of low-frequency drug resistance mutations in hiv-1 dna an accessory open reading frame (orf-x) of jaagsiekte sheep retrovirus is conserved between different virus isolates retroviral dna integration: viral and cellular determinants of target-site selection infectious endogenous retroviruses in cats and emergence of recombinant viruses nucleotide sequence of the jaagsiekte retrovirus, an exogenous and endogenous type d and b retrovirus of sheep and goats identification and characterization of novel human endogenous retrovirus families by phylogenetic screening of the human genome mapping project database identification of a rev-related protein by analysis of spliced transcripts of the human endogenous retroviruses htdv/herv-k rec (formerly corf) function requires interaction with a complex, folded rna structure within its responsive element rather than binding to a discrete specific binding site indik s: identification of the remresponsive element of mouse mammary tumor virus jaagsiekte sheep retrovirus encodes a regulatory factor, rej, required for synthesis of gag protein antiretroviral restriction factors rodent evolution: back to the root mouse mammary tumor virus-like sequences in human breast cancer human mammary tumor virus in inflammatory breast cancer cloning the human betaretrovirus proviral genome from patients with primary biliary cirrhosis distribution and activity of bats at local and landscape scales within a rural-urban gradient bats as bushmeat: a global review the immune gene repertoire of an important viral reservoir, the australian black flying fox application of a time-delay neural network to promoter annotation in the drosophila melanogaster genome hamming-clustering method for signals prediction in 5′ and 3′ regions of eukaryotic genes trnadb 2009: compilation of trna sequences and trna genes the pfam protein families database systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs analysis and prediction of leucine-rich nuclear export signals muscle: multiple sequence alignment with high accuracy and high throughput improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments new algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of phyml 3.0 prottest: selection of best-fit models of protein evolution bayesian phylogenetics with beauti and the beast 1.7 submit your next manuscript to biomed central and take full advantage of: • convenient online submission • thorough peer review • no space constraints or color figure charges • immediate publication on acceptance • inclusion in pubmed, cas, scopus and google scholar • research which is freely available for redistribution additional file 3: figure s4 . unannotated alignment of the full proviral genomes of the group viii endogenous betaretroviruses (βervs) of bats.additional file 4: annotated sequences of paerv-βa, papol-01, paenv-01, and rfenv-01. the authors declare that they have no competing interest.authors' contributions mt, jah, jc, and gt conceived the study. jah, jc and mt performed the analyses, mt generated the r. megaphyllus transcriptome, hf collected bats from which tissue was obtained to generate the transcriptome data. all authors contributed to the writing of the paper. all authors have read and approved the submission of the manuscript. key: cord-344093-3bniy5b5 authors: peteranderl, christin; herold, susanne title: the impact of the interferon/tnf-related apoptosis-inducing ligand signaling axis on disease progression in respiratory viral infection and beyond date: 2017-03-22 journal: front immunol doi: 10.3389/fimmu.2017.00313 sha: doc_id: 344093 cord_uid: 3bniy5b5 interferons (ifns) are well described to be rapidly induced upon pathogen-associated pattern recognition. after binding to their respective ifn receptors and activation of the cellular jak/signal transducer and activator of transcription signaling cascade, they stimulate the transcription of a plethora of ifn-stimulated genes (isgs) in infected as well as bystander cells such as the non-infected epithelium and cells of the immune system. isgs may directly act on the invading pathogen or can either positively or negatively regulate the innate and adaptive immune response. however, ifns and isgs do not only play a key role in the limitation of pathogen spread but have also been recently found to provoke an unbalanced, overshooting inflammatory response causing tissue injury and hampering repair processes. a prominent regulator of disease outcome, especially in—but not limited to—respiratory viral infection, is the ifn-dependent mediator trail (tnf-related apoptosis-inducing ligand) produced by several cell types including immune cells such as macrophages or t cells. first described as an apoptosis-inducing agent in transformed cells, it is now also well established to rapidly evoke cellular stress pathways in epithelial cells, finally leading to caspase-dependent or -independent cell death. hereby, pathogen spread is limited; however in some cases, also the surrounding tissue is severely harmed, thus augmenting disease severity. interestingly, the lack of a strictly controlled and well balanced ifn/trail signaling response has not only been implicated in viral infection but might furthermore be an important determinant of disease progression in bacterial superinfections and in chronic respiratory illness. conclusively, the ifn/trail signaling axis is subjected to a complex modulation and might be exploited for the evaluation of new therapeutic concepts aiming at attenuation of tissue injury. interferons (ifns) are well described to be rapidly induced upon pathogen-associated pattern recognition. after binding to their respective ifn receptors and activation of the cellular jak/signal transducer and activator of transcription signaling cascade, they stimulate the transcription of a plethora of ifn-stimulated genes (isgs) in infected as well as bystander cells such as the non-infected epithelium and cells of the immune system. isgs may directly act on the invading pathogen or can either positively or negatively regulate the innate and adaptive immune response. however, ifns and isgs do not only play a key role in the limitation of pathogen spread but have also been recently found to provoke an unbalanced, overshooting inflammatory response causing tissue injury and hampering repair processes. a prominent regulator of disease outcome, especially in-but not limited to-respiratory viral infection, is the ifn-dependent mediator trail (tnf-related apoptosis-inducing ligand) produced by several cell types including immune cells such as macrophages or t cells. first described as an apoptosis-inducing agent in transformed cells, it is now also well established to rapidly evoke cellular stress pathways in epithelial cells, finally leading to caspase-dependent or -independent cell death. hereby, pathogen spread is limited; however in some cases, also the surrounding tissue is severely harmed, thus augmenting disease severity. interestingly, the lack of a strictly controlled and well balanced ifn/trail signaling response has not only been implicated in viral infection but might furthermore be an important determinant of disease progression in bacterial superinfections and in chronic respiratory illness. conclusively, the ifn/ trail signaling axis is subjected to a complex modulation and might be exploited for the evaluation of new therapeutic concepts aiming at attenuation of tissue injury. (73) cell death induction, e.g., bcl-2-associated x protein, caspase-8, fas-associated protein with death domain, fas ligand, and tnf-related apoptosis-inducing ligand (trail) dsrna, polyi:c (4, 110) iav (4, 5, 10, 115) sendai virus (110) trail virus control by apoptosis induction in infected cells iav (6, 170, 171) tissue injury by apoptosis of both infected and non-infected alveolar epithelial cells, lung macrophages iav (5, 7, 10) rsv (137) necrosis of fibroblasts, dendritic cells, and epithelial cells iav (146, 147, 168) increased cellular infiltration cov (175) decreased expression of na,k-atpase, impaired epithelial fluid reabsorption iav (11) introduction in 1957, isaacs and lindenmann (1) first recognized the potential of a soluble and probably cell-derived factor to combat influenza virus infection and named this factor interferon [(ifn) from latin interferre, to interfere]. since then, three subgroups of ifns have been defined, primarily by their differential receptor usage. while the groups of type i ifn and type iii ifn comprise largely agents directly limiting pathogen spread by improving cellular counter measurements, ifn-γ, the sole type ii ifn, has been mainly implicated in the modulation of innate and also adaptive immune responses (2, 3) . accordingly, type i and iii ifns are key signaling molecules in viral control, and lack of both signaling pathways results in increased viral loads and disease severity. still, there is accumulating evidence that not only lack of an antiviral response but that also an unbalanced overshooting activation of ifns contributes to an exaggerated inflammatory reaction, tissue injury, reduced proliferative capacity, and thus enhanced disease severity ( table 1) . especially in viral infections, this effect has not only been tracked down to ifn signaling in general but specifically to the exaggerated production of key effector ifn-stimulated genes (isgs) (4) . a prominent example is the tnf-related apoptosis-inducing ligand (trail) that displays an ambivalent role in viral infection (5-7) ( table 1) . whereas first identified as factor produced by immune cells in non-respiratory infection (8, 9) , trail is now especially well studied in influenza a virus (iav) infection, where it is released in high amounts from bone marrow-derived macrophages upon pathogenassociated molecular patterns (pamps) recognition and type i ifn production (10) . macrophage-released soluble trail, but also membrane-bound cell-associated trail, acts via distinct receptors on infected but also on non-infected, neighboring cells. in viral infection, its preliminary role is to drive infected cells into apoptosis to limit virus spread. however, studies performed within the last decade demonstrate that trail's antiviral activity seems to be outweighed by the functional and structural damage it induces not only in infected but also in bystander cells such as uninfected cells of the alveolar epithelium (10, 11) . this process is not only relevant in promoting viral disease progression but has further implications in bacterial superinfection and probably also in chronic diseases. the recognition of the ambivalent role of ifn-driven signaling in vivo is a first important step to better understand disease progression and to envision novel treatment options for primary viral respiratory infection targeting distinct host-derived signaling mediators such as trail. it is a commonly accepted concept that-as janeway (12) already proposed in 1989-immune activation toward invading pathogens is mounted upon recognition of pamps. pamps are evolutionary conserved biomolecules such as proteins, lipids, nitrogen bases, sugars, and complexed biomolecules such as lipoglycans that are essential to the survival of a given pathogen (13) . pamps are recognized by distinct pattern recognition receptors (prrs) that are germ-line encoded and-similar to pamps-usually show a high evolutionary conservation. the first recognized and probably most intensely studied family of prrs are the toll-like receptors [tlrs; reviewed in mogensen (14) ; leifer and medvedev (15) ]. in viral infection, both host cell membrane-localized tlrs (tlr2, tlr4, detecting viral envelope proteins) and endosomal tlrs (tlr3, tlr7, tlr8, and tlr9 , nucleic acid sensors) initiate signal transduction cascades leading to ifn production (figure 1 ). tlr activation results in either myeloid differentiation factor 88 (myd88) or tir-domaincontaining adaptor protein-inducing ifn-β (trif) recruitment that both trigger various downstream signaling events, eventually leading to ifn regulatory factor (irf)3, irf7, and nfκb nuclear translocation as well as map kinase and activator protein 1 (ap-1) activation (16, 17) . similar to endosomal tlrs, the cytosolic retinoic acidinducible gene (rig)-i-like receptors (rlrs) are specialized to recognize viral nucleic acid contents and are central prrs relevant to mount an antiviral response, providing resistance to most rna (e.g., orthomyxoviruses) and some dna (e.g., reoviruses) viruses [reviewed in ref. (18, 19) ]. both melanoma differentiation-associated gene 5 (mda-5) and rig-i recognize dsrna, 5′-triphosphate rna, or the synthetic analog to dsrna, polyi:c (20, 21) . both drive the dimerization of the mitochondriaassociated adaptor protein ifn-β promoter stimulation 1 (ips-1) (also named mavs, visa, cardif). a subsequently activated cascade including tradd (tnf receptor type 1-associated death domain protein), traf3 (tnf receptor-associated factor 3), and tank (traf family member-associated nf-κb activator) induces the phosphorylation of irf3 and irf7, resulting in type i ifn production (22) . the third rlr, lgp2, so far has primarily been implicated to regulate rig-i or mda-5 as a cofactor; however, a recent study by stone et al. (23) demonstrated a novel, non-redundant, and independent role of lgp2 in west nile virus infection. another class of prr, the nucleotide oligomerization domain (nod)-like receptors (nlrs), has mainly been implicated in bacterial recognition (24) , still several nlrs are activated as well upon virus infection. especially, nlrp3 is known to recognize rna of different viruses including hepatitis c virus, measles virus, influenza, and vesicular stomatitis virus (vsv) (25) (26) (27) (28) , resulting in inflammasome formation and caspase-1-dependent activation of il-1β and il-18 (29) (30) (31) . in addition, virus infections are sensed also by a structurally diverse group of viral rna and dna sensors residing in the cytoplasm. these include the cyclic gmp-amp synthase that synthesizes the second messenger cgamp. cgamp in turn activates stimulator of ifn genes (sting), tank-binding kinase 1, and irf3, triggering ifn production (32) (33) (34) . moreover, sting itself acts as a prr and has been implicated in dna virus recognition including hsv, adenovirus, vaccinia virus, and papilloma virus and in sensing of retroviral rna-dna hybrids (35) and rna viruses after being activated by rig-i (36, 37) . another cytosolic nucleic acid sensor, pkr, is well known for its phosphorylation of eukaryotic initiation factor 2 α (eif2α) in response to viral dsrna. phosphorylation of eif2α results in its deactivation, host translational shut-off, and the limitation of viral replication. of note, the pkr-eif2α-driven inhibition of protein synthesis can contribute to an ips-1-dependent ifn-β induction (38) . furthermore, pkr has been implicated in efficient type i ifn activation by tlr3 in response to dsrna (39) and can mediate-at least partially-activities of irf1 (40) . in addition to type i ifns, also type iii ifns exert antiviral activity and are widely expressed after viral recognition, being produced by most cell types including epithelial, endothelial, fibroblast, and polymorphonuclear cells [reviewed in ref. (41, 42) ]. like type i ifns, type iii ifns are induced in viral infection by the prr rig-i as well as tlr3 and tlr9 and rely on the activation of the same transcriptional activators, including irf3, irf7, and nfκb. these observations initially led to the conclusion that type i and type iii ifn comprised two completely redundant systems to induce isgs in response to pamp recognition. however, more recent data suggest distinct selection mechanisms for either type i or type iii ifn expression. as such, ips-1 specifically induces ifn-λ, but not type i ifn, when located at the peroxisomal membrane instead of the mitochondrial membrane in response to rig-i activation by reovirus, sendai virus, or dengue virus challenge (43) . interestingly, type iii ifn induction is largely independent toward ap-1 translocation, which facilitates an instantaneous induction of ifn-λ after viral recognition, highlighting it as an important immediate factor driving innate microbial defense mechanisms. release of ifns upon pathogen recognition is a highly conserved mechanism-found from teleost fish to insects and mammals-to prepare the surrounding cells as well as the host defense against the invading threat (44, 45). whereas often high-level ifn production relies on specialized sentinel cells such as macrophages or dendritic cells (dcs), mostly all cells of the multicellular organisms are able to respond to at least one type of ifn by expression of respective receptors. receptor binding then induces a signal transduction cascade relying on the janus kinase (jak) and signal transducer and activator of transcription (stat), which results in efficient transcription of a plethora of different isgs in infected as well as bystander cells (46, 47) . ifns engage a classical canonical signal transduction cascade employing jak/stat molecules after binding to their respective receptors. herein, type i ifns ligate to their common heterodimeric receptor consisting of the ifn-α receptor (ifnar)1 and ifnar2 subunits, whereas type iii ifns act via a interleukin-10 receptor 2 (il-10r2)/ifn-λ receptor 1 (ifnlr1) heterodimer that to date has been reported to be restricted in its expression to epithelial cells (48) . in type i ifn signaling, ifnar engagement leads to the activation of the receptor-associated protein tyrosine kinases jak1 and tyrosine kinase 2 followed by the recruitment or repositioning of already associated but elsewise latent cytoplasmatic transcription factors stat1 and stat2. consequently, stat1/stat2 are phosphorylated on conserved tyrosine residues, they disassemble, undergo conformational changes enabling their heterodimerization as well as the exposure of a nuclear localization sequence. subsequently, the stat1/stat2 heterodimer translocates into the nucleus where it interacts with the irf9 to form the trimeric ifn-stimulated factor 3 (isgf3). isgf3 binds cognate dna sequences, the ifn-stimulated response elements (isre), finally leading to isg induction. also type iii ifn interaction with the il-10r2/ifnlr1 receptor complex triggers stat1/stat2 heterodimerization, nuclear translocation, and isgf3 assembly (49) . interferon signaling results in the induction of isgs evoking different cellular responses against viral infection, both in infected as well as in non-infected cells, including direct antiviral, immune-modulatory, or cell death-inducing effects to enable an immediate and robust response to a pathogen challenge. many isgs directly interfere with viral replication on an intracellular level. well-studied examples of antiviral isgs comprise ifn-induced transmembrane proteins (ifitms) effective in iav, west nile virus, and dengue virus infection (50, 51) , the myxovirus resistance protein a (mxa) that interferes with vsv mrna production and binds the iav nucleocapsid to prevent nuclear translocation of viral genetic material (52) (53) (54) , the 2-5-oligoadenylate synthase (oas), which activates rnase l triggering viral rna degradation, or the prr pkr, which besides activating the ifn response has a major impact on viral protein translation by inhibiting the eif2α (55) . more recently identified isgs include the plasminogen activator inhibitor 1 that blocks iav infection by inhibiting glycoprotein cleavage executed by extracellular airway proteases (56) or the antiviral isg20 that limits iav viral replication via its exonuclease activity most likely by interfering with the viral np (57) . accordingly, ifn pretreatment usually results in the establishment of an antiviral state that limits viral replication and spread from the start of infection and thus favors milder disease outcomes. ifn-α pretreatment has been demonstrated to limit viral spreading of seasonal iav strains and thus decrease morbidity and mortality in mice, guinea pigs as well as ferrets (58) (59) (60) . as shown by a study by tumpey et al. (61) , this effect can be attributed to the early induction of antiviral isgs including mxa. importantly, type i ifn pretreatment also dampens early replication of highly pathogenic avian influenza in ferrets (58) . also in respiratory syncytial virus (rsv) infection, treatment with recombinant ifn-α results in significantly decreased lung viral titers, alveolar inflammatory cell accumulation, and clinical disease in rsv-infected mice (62) . in addition, respiratory infections caused by emerging coronaviruses (cov) can be ameliorated by type i ifn pretreatment strategies. in an in vivo macaque model (macaca fascicularis) of severe acute respiratory syndrome (sars)-cov infection, it could be demonstrated that pretreatment with pegylated ifn-α significantly diminished cov replication and excretion and resulted in reduced pulmonary damage (63) . macaques also serve as a preclinical model for middle east respiratory syndrome (mers)-cov, and similar to sars-cov, ifn-α in combination therapy with ribavirin reduces viral replication and severe histopathological changes (64) . in line, genetic alteration leading to an enhanced type i ifn signaling has been demonstrated to limit iav-induced disease outcomes, as a recent study by xing et al. (65) reported that deletion of trim29, a negative regulator of nemo, which leads to nfκb induction and therefore enhanced type i ifn production, is protective in vivo in iav-infected mice. conversely, the genetic depletion of ifn signaling in ifn receptor-deficient mice can result in a lack of viral control, resulting in enhanced viral titers in different viral infections including rsv or iav (66, 67) . still, it must be noted that this effect is often mild in ifnar-or ifnlr-deficient animals, which is probably related to a certain redundancy between type i and type iii ifn signaling in limiting viral spreading in epithelial cells (68) . in contrast, ifnar/ ifnlr-double knockout or stat1 knockout animals that are deficient in both type i and type iii ifn signal transduction succumb more readily to infection due to excessive viral replication (69) (70) (71) . vice versa, mutations in key isgs such as ifitm3 are associated with increased iav disease severity in mice and humans (72) . however, ifn pretreatment and genetic loss-of-function approaches generally are not relevant to human respiratory virus-induced hospitalizations, where patients already present with ongoing respiratory infection and inflammation, and preclinical studies underline that type i ifn signaling in an already inflamed organ is rather detrimental and enhances tissue injury, and lack of type i ifn in vivo may even ameliorate disease outcome. accordingly, in cases where the antiviral defense was not compromised (e.g., in animals with efficient type iii ifn signaling) ifnar-deficient mice infected with sendai virus or iav were reported to be more resistant to infection-induced morbidity and mortality (73, 74) . similarly, in sendai virus in vivo infection, wetzel et al. (75) showed that increased ifn-β levels in the lung homogenate correlates to increased morbidity and mortality, and also for sars-cov, a recent study demonstrates that high type i ifn induction in an already ongoing viral infection contributes to mortality in sars-cov-infected mice (76) . also for iav infection, type i ifn application after infection has been proven to drive disease severity (74) . of note, the detrimental effects of type i ifns were especially pronounced in mice lacking central antiviral factors, namely the ifit protein in sendai virus infection and mxa in iav. interestingly, beilharz et al. (77) demonstrated that application of low doses of ifn-α reduces viral load, which to a certain degree led to attenuated disease progression, whereas high dose application of type i ifn contributed to morbidity (77) . in line, high expression levels of isgs have been shown to correlate to worse outcomes in ards patients (78) . this observation corresponds to reports stating that the ifn threshold needed to induce antiviral isgs-showing a beneficial effect in acute respiratory viral infection-is by at least 10-fold lower than the ifn dose necessary to trigger isgs that show immunomodulatory, death-inducing, or anti-proliferative effects and thus can contribute to disease progression (79) (80) (81) (82) . altogether, these data demonstrate that ifns may significantly contribute to unbalanced inflammation and tissue injury during respiratory viral infection depending on expression levels and duration of ifn-related signaling events. to date, the underlying mechanisms leading to the ifndependent enhanced disease progression are not fully understood but often result from a dysregulated ifn signaling response. one mode of action of ifn and ifn-stimulated isgs is to stimulate negative feedback loops on ifn signaling. for example, suppression of jak1 or stat1 via specific phosphatases, expression of suppressor of cytokine signaling (socs)1 and socs3, or ubiquitination and endocytosis of the ifn receptors (83) (84) (85) (86) desensitize cells to ifn signaling and allow recovery and the return to homeostasis after microbial challenge. as demonstrated by bhattacharya et al. (87) , the lack of ifnar downregulation and thus the failure to initiate ifn-desensitization contributes to increased inflammatory signaling, extensive lung injury and, importantly, also impaired tissue regeneration (87) . moreover, ifns are immunomodulatory and shape the specific responses of cells of the immune system, which has been implied to influence disease progression both positively and negatively. in a recent study, type i ifns have been associated in the regulation of innate lymphoid immune cells (ilc)2 in iav infection, where they-in concert with ifn-γ and il-27-promote an ilc2-dependent restriction of immunopathology (88) . moreover, type i ifns play an important role in stimulating the immune response driven by dcs; they stimulate the expression of mhc molecules as well as the co-stimulatory ligands cd80 and cd86 and thus activate t cell responses (89, 90) . additionally, ligand-driven activation of ifnar enhances the proliferation of cd8 positive t cells, especially early in infection. however, late in infection, type i ifns were also implied in decreasing t cell expansion upon sars-cov and arenavirus infection (76, 91) , which might potentially be related to the above described desensitization upon prolonged ifn signaling and might be detrimental if initiated too early in infection. in line, pinto et al. (92) reported an impairment of t cell responses upon type ifn induction in west nile virus infection. in b cells, the lack of ifnar has been demonstrated to result in enhanced release of neutralizing antibodies in iav infection (93) implying a repressive role for type i ifn in b cell antibody production. however, immunization studies by le bon et al. (94) reported the necessity of ifnar on b cells for efficient igm and igg production, underlining the need for further studies to understand the detailed effects of ifn-dosage and timing adaptive immunity activity upon respiratory viral infection. type i ifns additionally induce the production of high levels of pro-inflammatory cytokines that have been closely linked to worsened outcomes of acute respiratory viral infection. especially in iav, disease severity and disease progression are linked with an overshooting, ifn-driven inflammatory response, in which further exogenous supplementation with type i ifn in fact correlates with increased morbidity and mortality (74, 95) . in non-human primates, iav infection with a highly pathogenic h5n1 isolate evokes a strong induction of type i ifn, resulting in severe lung injury by a necrotizing bronchiolitis and alveolotis (96) . ifn levels in turn have been demonstrated to cause elevated pro-inflammatory cytokine levels after in vivo iav infection and additionally, in human alveolar macrophages, the release of pro-inflammatory cytokines (e.g., mcp-1) are preceded by a robust type i ifn response (97) . importantly, also in human infection with h5n1, levels of pro-inflammatory cytokines are strongly elevated in bronchoalveolar lavage fluid, and cytokine levels have been associated with organ damage and worsened disease outcomes (98, 99) . still, it should be noted that due to strain differences in virus-elicited prr activation and, importantly, ifn antagonism by the iav non-structural (ns)1 protein, ifn levels and disease severity do not always directly correlate; actually, the extent to which ns1 can suppress the ifn response relates to prolonged viremia and thus can also be a determinant of virus pathogenicity both in human bronchial epithelial cells and in an in vivo model of iav infection (100, 101) . alongside iav, also in rsv infection the induction of high levels of pro-inflammatory cytokines has been directly related to type ifn, as rsv-infected but ifnar-deficient mice presented with significantly diminished pro-inflammatory cytokine release, which translated into an attenuated disease course (67) . also in sars-cov, the late phase type i ifn induction relates to accumulation of inflammatory macrophage populations and elevated lung cytokine levels (76) . in addition to antiviral, immunomodulatory, and pro-inflammatory isgs, ifn signaling results in the transcription and translation of cell death-inducing isgs. in the context of viral infection, these factors provide a mode to block viral spreading and reinfection by killing those infected cells, in which the internal activation of antiviral isgs is not sufficient to restrict viral replication. thus, the infected cell is sacrificed to prevent the release of infectious progeny virions to limit viral spreading. however, especially in the lung, the disruption of the alveolar epithelial barrier by cell death of infected cells, but importantly also non-infected bystander cells induced by factors such as trail, significantly contributes to worsened disease outcomes. controlled cell death or apoptosis can be induced by intrinsic and extrinsic signals. the intrinsic apoptosis pathway is initiated by diverse intracellular stimuli that influence the expression and activation of b cell lymphoma (bcl)-2 family proteins that govern the permeabilization status of the outer mitochondrial membrane. once cytochrome c is released from the mitochondria, it binds to the intracellular adaptor protein, apoptotic peptidase activating factor 1, forming the so-called apoptosome that in turn recruits pro-caspase-9 (102). caspases (cysteine-aspartic proteases) exert their action by cleaving other proteins and substrates. herein, initiator caspases such as caspase-8 and caspase-9 target other downstream caspases, whereas effector caspases, including caspase-3, -6, and -7, directly cause apoptosis by cleaving and thus inactivating or disassembling a vast array of cellular integral proteins and complexes (103) . the extrinsic apoptosis pathway relies on an extracellular signal exerted by ligands of the tumor necrosis factor (tnf) receptor (tnfr) superfamily, including trail, tnf-α, and fas ligand (fasl) (104) . their ligation to their respective cell surface-expressed death receptors (dr) leads via the signal transmission by fas-associated protein with death domain (fadd) to the activation of the initiator caspases-8 or -10, finally stimulating effector caspases including caspase-3 (105) . to date, several type i and type iii ifn-induced, proapoptotic factors have been identified (106) . both caspase-4 and caspase-8 have been shown to be upregulated upon type i ifn signaling (4, 107); caspase-8 enhances the fadd-driven extrinsic apoptosis pathway, whereas the less-studied caspase-4 may promote pro-il-1β cleavage and inflammasome-driven cell death (pyroptosis) in macrophages (108, 109) . chattopadhyay et al. (110) demonstrated that sendai virus infection and polyi:c treatment resulted in bcl-2-associated x protein (bax) activation and apoptosis induction via one of the key transcription factors of ifn genes, irf3. in addition irf5 was reported to enhance trail-dependent extrinsic apoptosis by nuclear translocation resulting in the translation of to date undefined factors that increase cell death upstream of caspase-8 activation (111) . furthermore, both rlrs, rig-i and mda-5, trigger the proteins puma and noxa that induce bcl and the ifn/trail signaling axis frontiers in immunology | www.frontiersin.org march 2017 | volume 8 | article 313 thus activate the intrinsic mitochondrial apoptotic cascade (112) . also, pkr influences a cell's susceptibility to apoptotic signals, as it was demonstrated to sensitize to the fadd/caspase-8 apoptosis pathway upon type i ifn signaling after challenge with iav or dsrna (4) and the oas-rnasel system has been suggested to contribute to ifn-α-related cell death induction, but the exact mechanisms remain to be elucidated (113) . finally, also two classical initiators of the extrinsic apoptosis cascade are induced as isgs. both fasl and its receptor fas are upregulated on mrna levels by ifn-α (114) , and fasl was reported to be induced by type i ifn in iav infection in the murine lung in vivo (115) . also, the proapoptotic factor trail (or tnfsf10, apo2l) is induced by ifn-mediated and isgf3-executed transcriptional activation, as has been shown by sato et al. (116) , who revealed the presence of the isre sequence within the trail promoter region (116) . in iav infection, trail is released in high amounts from infected alveolar macrophages depending on a pkr-and ifn-β-driven autocrine signaling loop. binding of ifn-β to macrophageexpressed ifnar activates a jak/stat-dependent release of trail, which then acts through its receptor dr5 on the alveolar epithelial cells (5, 10) . however, certain prerequisites may decrease the ability of a cell to undergo apoptosis, including a shortage in pro-caspase-8 availability, expression of cellular fadd-like il-1β-converting enzyme-inhibitory proteins (c-flips) that block fadd-driven caspase activation, inactivation, or degradation of fadd itself, or expression of cyld, which acts as a receptor-interacting serine/threonine-protein (rip)1 kinase de-ubiquitinase and thus stabilizes rip1. however, in these cases ifn signaling can still promote a caspase-independent, programmed inflammatory cell death by activating the necroptosis pathway (117, 118) . necroptosis is induced by a complex formation by rip1 and rip3 kinases that activate both poly-adp-ribose (par) polymerase 1 (parp-1) and/or mixed lineage kinase domain-like (mlkl), leading to atp depletion, calpain activation, par polymer accumulation or cell membrane permeabilization, and release of damage-associated molecular patterns, respectively [reviewed in ref. (119, 120) ]. both a type i ifn-dependent jak/stat-driven activation of pkr as well as signaling by the prr dai (dnadependent activator of irfs) initiates necroptosis via rip1/rip3 activation, respectively (117, 121) . importantly, the activation of proapoptotic and pro-necroptotic pathways in respiratory infection can result in a structural disruption of the airway and the alveolar epithelial barrier, which is a major hallmark of respiratory disease and its progression to the acute respiratory distress syndrome (122, 123) . in virusinduced lung injury, especially expression of trail, which can initiate both apoptosis as well as necroptosis has been correlated with more severe outcomes. as described earlier, trail belongs to the superfamily of tnf ligands and has been reported to be inducible by both type i and type iii ifns. trail has been found to be present in various cells of the immune system, among them natural killer (nk) cells, t cells, nk t cells, dc subsets such as ifn-γ-producing killer dcs and macrophages, and can be displayed in large amounts on the cell surface or be shed upon ifn-and/or pro-inflammatory cytokine signaling (124) (125) (126) . in addition to cells of the immune system, fibroblasts have been shown to produce trail after ifnγ treatment or viral challenge. also, club cells and the alveolar epithelium have been reported to produce trail (127) (128) (129) (130) . similar to other ligands of the tnf superfamily, trail is a homotrimeric type ii transmembrane protein with a conserved c-terminal extracellular domain that mediates receptor binding and can be cleaved by metalloproteinases to generate a soluble mediator (131) . however, trail can induce cell death also in its membrane-bound form, that is, similar to trail expression levels and trail shedding, upregulated by type i ifn (126) . direct cell-to-cell trail-dr interactions have been demonstrated to play a role in macrophage, nk as well as cd4 + t cell-mediated induction of cellular death (132, 133) . in humans, five different binding partners for trail are present: the membrane-bound dr4 (trail-r1) and dr5 (trail-r2) that both induce a proapoptotic signaling cascade, the membrane-bound anti-apoptotic decoy receptors (dcr)1 and dcr2, and the soluble interaction partner osteoprotegerin (134) . in the murine system, only dr5 has been identified to ligate to trail (135) . in the human respiratory compartment, both dr4 and dr5 have been demonstrated to be present under steady-state conditions (136, 137) . however, upon viral infection, cell-sensitivity to trail-induced apoptosis is enhanced, which has been attributed to increased trail receptor expression especially on infected cells, as dr levels are markedly increased in iav-, adenovirus-, and paramyxovirus-infected cells in contrast to non-infected bystander cells (10, 138, 139) . of note, studies on the dependency of dr upregulation upon type i ifn signaling after iav infection have yielded conflicting results in different strains of mice (10, 74) , highlighting the complex interplay of ifn-induced cascades in a host-and tissue-specific context, whereas the exact virus-and host-specific mechanisms for dr regulation remain less well defined. moreover, previous assumptions that also dcr expression would correlate with cell-sensitivity to trail-induced cell death could not be experimentally verified (125) . tumor necrosis factor-related apoptosis-inducing ligand ligation to the proapoptotic receptors dr4 or dr5 triggers a trimerization of the receptors. subsequently, depending on additional stimuli, presence or absence of adaptor molecules or inhibitory proteins, different signaling pathways can be activated (figure 2) . in the classical trail-dependent extrinsic apoptosis induction, the proteins rip, tradd, and fadd are subsequently recruited to the dr cytoplasmic domain upon trail ligation (140, 141) . these factors and the proapoptotic drs all share a cytoplasmic death domain (dd), which is lacking or truncated and thus inactive in the dcr. the dd plays a central role in the concerted formation of the death-inducing signaling complex (disc). disc formation exposes a second functional domain of fadd, the death effector domain that is directly able to recruit pro-caspase-8 figure 2 | trail/dr5-mediated cellular signaling pathways. in presence of rip1, tradd, and fadd, trail ligation to dr5 results in apoptosis induction, which is initiated by recruitment of the pro-caspase-8 or -10 to fadd. these in turn activate the effector caspases-3 and -7, which leads to dna fragmentation and apoptosis induction. in addition, tradd can trigger a traf2-and jnk-dependent activation of bax and subsequent release of mitochondrial cytochrome c, inducing the pro-caspase-9 activation. in the presence of cyld, c-flip or absence of sufficient amounts of fadd or pro-caspase-8, trail ligation to dr triggers the interaction of rip1 and rip3 kinase, which in turn cause cell death via induction of mlkl and/or parp-1. in the presence of ciaps, fadd is not recruited to dr5 upon trail ligation, and tak1 is activated by tradd/traf2 interactions. tak1 induces nemo followed by iκb degradation and nfκb activation, as well as mkk and jnk activation leading to ap-1 nuclear translocation; both events promote the production of cytoprotective factors such as xiap, ciaps, and c-flip. additionally, tak1 triggers ampk activation and thus mtorc inhibition, which results in enhanced autophagic activity. abbreviations: ap-1, activator protein 1; tnf, tumor necrosis factor; trail, tnf-related apoptosis-inducing ligand; dr5, death receptor 5; rip1, receptor-interacting serine/threonine-protein kinase 1; tradd, tnf receptor type 1-associated death protein; fadd, fas-associated protein with death domain; traf, tnf receptor-associated protein; jnk, janus kinase; bax, bcl-2-associated x protein; c-flip, cellular fadd-like il-1β-converting enzyme-inhibitory proteins; rip, receptor-interacting serine/threonine-protein; mlkl, mixed lineage kinase domain-like; parp-1, poly-adp-ribose (par) polymerase 1; ciap, cytoprotective factors including inhibition of the autophagic machinery; xiap, x-linked inhibitor of apoptosis protein; ampk, amp-activated protein kinase; mtorc, mammalian target of rapamycin complex; traf2, tnf receptor-associated protein 2; mkk, mitogen-activated protein kinase. and pro-caspase-10. how exactly disc formation induces caspase activation is still under debate. the most probable scenarios include either an autocatalytic cleavage of caspase-pro-domains enabled by the spatial proximity between pro-caspases (generated by their recruitment to disc), by pro-caspase dimerization, or by pro-caspase conformational stabilization (125) . removal of the pro-domain of caspase-8 and caspase-10 results in the activation of the effector caspases-3 and -7, which cleave dna fragmentation factor 45 and lead to apoptosis (142, 143) . moreover, trailbinding to dr4 and dr5 can induce the jnk either via caspase-8 or recruitment of tnf receptor-associated protein 2 (traf2) to the disc complex, which results in the activation of the intrinsic apoptotic cascade by bax-dependent mitochondrial cytochrome c release (144) . in addition, trail signaling is also able to induce necroptosis by both activating the rip1/rip3 kinase downstream effectors parp-1 and mlkl, contributing to epithelial cell death and tissue injury (145) (146) (147) . it has become apparent in recent years that trail signaling is closely linked to induction of autophagy, a process generally associated with the blockade of apoptosis and necrosis. indeed, autophagy has been reported to improve cellular survival in cell stress by catabolic removal of cytoplasmic long-lived proteins and damaged organelles. it also contributes to viral clearance and the transfer of viral material to endosomal-/lysosomallocated tlr7 or mhc class ii compartments for the activation of adaptive immunity (148). several studies outline that trail ligation to dr5 can result in a traf2-dependent activation of tak1 (map3k7) that has been attributed a central role in trail-induced autophagy activation (149) . tak1 modulates the ikk-dependent translocation of nfκb, and it also induces jnk activation via mitogen-activated protein kinase. both events lead to expression of autophagy-related factors including inhibition of the autophagic machinery (ciap)1, ciap2, x-linked inhibitor of apoptosis protein, and c-flip (150, 151) . especially, c-flip has been associated with desensitization of cells to trail-induced apoptosis, favoring autophagy-related cascades (152) . another study revealed that upon trail signaling the amp-activated protein kinase (ampk) is activated. ampk in turn inhibits the mammalian target of rapamycin complex 1 that itself is an inhibitor of autophagy, thus the activation of the autophagic machinery is promoted (153) . the decision if trail signaling results rather in necroptotic or apoptotic cell death or in activation of autophagy seems to be dependent on the presence of ciaps that promote rip kinase ubiquitination and degradation (146) , but also on the balance between active caspases and autophagic proteins such as beclin-1 (154, 155) . this suggests a scenario where autophagy is activated as cell protective mechanism until cell stress-as executed by enhanced trail signaling or additional viral infection-increases over a threshold to favor cell death induction. accordingly, as trail signaling is not restricted to infected cells, excessive cell death activation might be limited by autophagy induction in non-infected bystander cells. however, autophagy is not only related to cell survival but can also positively affect apoptosis and induce-even if the exact mechanisms are still under debate-autosis, the autophagy-related cell death, another mode of trail to trigger cell death (156, 157) . of note, autophagy activation needs to be placed into its virus-specific context, as some viruses, including dengue virus, poliovirus, and coxsackie b virus (158) , can exploit autophagic pathways for their own replication and thus promote apoptosis and tissue injury. as discussed above, trail is a potent activator of cell death. however, its signaling outcomes can differ largely depending on its delivered form (e.g., membrane-bound versus soluble), the availability of drs on the target cell membrane, alternate intracellular pathways that might be activated and finally the pathogen itself, as it might exploit trail-induced pathways for its own survival and replication. in acute respiratory infection, trail signaling is often part of an ifn-driven overshooting inflammatory reaction that promotes unspecific tissue injury and thus disease severity by increasing functional and structural changes in infected but also non-infected cells, as will be outlined below. the release and effects of trail have been especially well studied in iav infection in the last decade. earlier studies reported that within 3 days after infection, bronchial, bronchiolar, and alveolar epithelial cells undergo apoptosis (159) . this early induction of cell death is mainly attributed to direct apoptosis induction by the virus itself, as iav actively promotes apoptosis for efficient viral replication (160) . herein, the viral ns1 and pb-f2 proteins not only play a crucial role (161, 162) but also the viral m2 protein has been implicated in this process as it inhibits autophagy in infected cells (163) . in addition, our own data revealed that later in iav in vivo infection, the recruitment of bone marrowderived macrophages via the cc chemokine receptor type 2 (ccr2)-cc-chemokine ligand 2 (ccl2) axis significantly contributes to alveolar cell apoptosis and structural damage of the alveolar epithelium (5) . studies by wurzer et al. (164) had previously demonstrated that iav promotes the production of proapoptotic factors in an auto-and paracrine fashion via nfκb transcriptional activation by iav (164) . subsequently, brincks et al. (6) elucidated that human peripheral blood mononuclear cell treated with iav released trail and that increased trail levels correlated with type i as well as ii ifn induction. additionally, trail sensitivity was increased in influenza virusinfected cells. in line, our investigations could elucidate that iav triggers a pkr-dependent translocation of nfκb that results the production of type i ifns. these in turn induce, via ligation to the ifnar receptor complex, expression and shedding of trail by bone marrow-derived macrophages (10) . in addition, davidson et al. (74) demonstrated that type i ifn application to iavinfected mice increased morbidity and lung injury, which could be attributed to both dr5 and trail upregulation inducing epithelial cell apoptosis. importantly, högner et al. also reported that the iav strain used in these studies, a/pr8 (h1n1), which is highly pathogenic for mice, induced an approximately 800-fold induction in macrophage trail expression, whereas the lower pathogenic virus a/x-31 (h3n2) only stimulated trail by a factor of eight. of note, the relation between trail induction and iav strain-specific pathogenicity also translates to the highly pathogenic avian h5n1 iav, causing severe pneumonia in mice as well as in humans (165, 166) . moreover, human infection with both the highly pathogenic h5n1 as well as the pandemic 1918 h1n1 iav strains are characterized by a massive influx of mononuclear phagocytes into the alveoli, which is correlated with extensive alveolar epithelial cell apoptosis (97, 167) . additionally, macrophages gained from bronchoalveolar lavages of patients presenting with ards caused by the pandemic h1n1/2009 virus strain showed high surface expression and release of trail (10) . another recent report demonstrates that in highly pathogenic avian influenza, in addition to macrophages also the alveolar epithelium might be involved in causing elevated levels of trail in the alveolar space (130) . besides its role in apoptosis, trail signaling upon iav infection has also been implicated in the induction of necroptosis in fibroblasts, dcs, and lung epithelial cells (146, 147, 168) . rodrigue-gervais et al. (146) demonstrated that lack of cipa2 promotes rip3 kinase-mediated necroptosis in response to trail-but also the proapoptotic factor faslreleased from hematopoietic cells. this contributed to severe lung epithelial degeneration and increased mortality, even though viral control was not compromised. nogusa et al. (147) further elucidated that iav-induced necroptosis depends on rip3 kinase activation of mlkl, and that rip3 kinase deficiency, similar to ciap2-deficiency, increased iav-susceptibility in vivo. in iav infection, as mentioned earlier, dr5 expression is elevated on infected alveolar epithelial cells, but not in noninfected cells in vivo, which might impact on trail susceptibility to apoptosis induction (10) . however, both infected as well as neighboring bystander cells were found to be targeted for apoptosis induction by macrophage-released trail. nonetheless, we could recently show that specifically in noninfected cells within the iav-infected lung, trail severely compromises the function of the ion channel na,k-atpase, which was mediated via induction of the stress kinase ampk (11) , thereby potentially revealing a cross-link to trailinduced autophagic cell stress pathways in bystander cells both in vitro and in vivo. the trail-induced and ampk-mediated downregulation of the na,k-atpase, a major driver of vertical ion and fluid transport from the alveolar airspace toward the interstitium, resulted in a reduced capacity of iav-infected mice to clear excessive fluid from the alveoli. thus, trail signaling contributes to intensive edema formation, a hallmark of disease in virus-induced ards (123) . notably, this effect of trail on na,k-atpase expression was induced independently of cell death pathways elicited by caspases, as treatment of cells and mice with a specific caspase-3 inhibitor diminished apoptosis in alveolar epithelial cells but still allowed for the reduction of the na,k-atpase (11) . conclusively, treatment of iav-infected mice with neutralizing antibodies directed against trail or the abrogation of recruitment of trail + bone marrow-derived macrophages inhibited apoptosis of both non-infected and bystander cells. thus, lung leakage due to loss of alveolar barrier function was reduced, whereas alveolar fluid clearance capacity was enhanced, resulting in reduced edema, improved survival, and outcome upon iav challenge in vivo. however, trail has also been shown to be upregulated on nk, dc, and on cd4 + and cd8 + t cells after iav infection (169) . studies by brincks et al. demonstrated that especially cd8 + t involved in cytotoxic t cell responses toward iav and drive iav-infected cells into apoptosis via trail, thus contributing to efficient virus clearance (6, 170) . in addition, both fasl and trail are involved in dc-mediated ctl activation and cytotoxicity against iav-infected cells (6, 171) . furthermore, studies showed delayed viral clearance upon neutralizing anti-trail antibody administration (169, 172) . our data, however, demonstrate that the transfer of trail-deficient bone marrow into irradiated wild-type mice, resulting in loss of trail production by bone marrow-derived macrophages upon iav infection, does not impact on the capacity to fully clear viral particles from the lung at day 7 after infection, suggesting that other compensatory mechanisms are recruited to guarantee viral clearance (10) . taken together, in iav infection, trail acts both as an important mediator of infected cell killing but particularly as a detrimental factor contributing to tissue injury and impaired inflammation resolution when released in excessive amounts by recruited immune cells. respiratory syncytial virus is an important cause of respiratory tract infections especially in children worldwide. generally, there seem to be virus-elicited anti-apoptotic mechanisms active in the lung epithelium, as rsv-infected primary human airway cells show a minimal cytopathic effect (173) . however, several cell lines including small airway cells, primary tracheal-bronchial cells, and a549 and hep-2 showed increased expression of trail and its ligands dr4 and dr5 in an in vitro rsv infection model (174) . moreover, soluble trail released from leukocytes was elevated in the bronchoalveolar lavage fluid of patients with rsv-associated respiratory failure, suggesting that similar to iav, trail contributes to rsv-induced epithelial injury and disease progression (137) . also in cov respiratory tract infection, trail levels, but less so fasl, have been reported to be markedly elevated (175, 176) . for sars-cov that presents with a severe damage to both the upper and lower respiratory tract (177) , especially dcs respond with a strong induction of trail production, which was suggested to correlate to increased cellular lung infiltrations present in sars-cov patients (175) . interestingly, sars-cov infection drives cells into apoptosis by a pkr-driven but eif2α-independent pathway (178) , which might-similarly as seen in iav infection-suggest a pkr-induced and autocrine/paracrine executed activation of apoptosis. also mers-cov, which causes pneumonia and respiratory failure, has been demonstrated to induce profound cell death within 24 h of infection, irrespective of viral titers produced by the infected cells. however, type i ifn expression is strongly reduced in mers-cov in comparison to seasonal human cov in in vitro infection models, including human monocyte-derived macrophages, calu-3, and human lung fibroblasts (179, 180) , which might also dampen downstream trail induction. therefore, the exact mechanism by which mers-cov promotes cell death remains to be investigated. recurrently, viral infections of the respiratory tract are followed by outgrowth of colonizing gram-positive bacteria that aggravates the course of illness. this is well documented for iav, where "super" infections with streptococcus pneumoniae and staphylococcus aureus are the most frequent and increase viral pneumonia-associated morbidity and mortality (181) . during the 1918 iav pandemic, bacterial pneumonia was evident in most cases (182) and also during the recent 2009 h1n1 pandemic, coinfections were a relevant factor for severe disease in a young patient population without comorbidities (183) . interestingly, virus-induced elevation of the type i ifn response levels might promote secondary bacterial outgrowth by several mechanisms [reviewed in ref. (184) ]. in line, it has been repeatedly demonstrated that lack of type i ifn signaling results in better bacterial clearance and increased survival rates in iav-and s. pneumoniae-superinfected mice (185) (186) (187) . herein, ifn-induced apoptosis induction as well as depletion or impaired recruitment of lymphocyte subsets necessary for bacterial control play a critical role (188, 189) . bacterial clearance from the lung has been reported to rely on sufficient phagocyte generation, recruitment, and survival. type i ifn has been demonstrated to cause apoptosis in bone marrow-derived granulocytes, affecting the numbers of recruited neutrophils (189) , but also to impair expression of the cytokines cxcl1 (or kc) and cxcl2 (or mip-2), thus inhibiting neutrophil recruitment to the lungs with severe effects on survival of superinfected mice (185) . a recent report by schliehe et al. (190) elucidated the mechanistic background for impaired cxcl1 expression and secretion and demonstrated that type i ifns activate the histone methyltransferase setdb2, which in turn represses the cxcl1 promoter and thus impairs neutrophil recruitment and bacterial clearance. moreover, type i ifn production decreases ccl2 production, thus inhibiting macrophage recruitment, which as well has been reported to have detrimental effects on bacterial clearance and disease progression in bacterial superinfection after viral insult in vivo (186) . in addition, type i ifns also impair γδ t cell function and il-17 release, which was shown to increase susceptibility to s. pneumoniae superinfection after iav challenge (187) . also in s. aureus pneumonia, a robust type i ifn response is correlated to excessive morbidity and tissue injury (191) . in a model of polyi:c, s. aureus (methicillinresistant strain, mrsa) superinfection, polyi:c treatment prior to bacterial infection enhanced type i ifn levels and decreased bacterial clearance and survival (192) . furthermore, shepardson et al. (193) demonstrated that late type i ifn induction rendered mice more susceptible to secondary bacterial pneumonia in a model of iav-mrsa superinfection. only limited data are available on a direct role of trail in respiratory disease progression due to bacterial superinfections. in a model of iav-haemophilus influenza infection, neither deficiency for cc chemokine receptor type 2, inhibiting bone marrow-derived macrophage recruitment, nor deficiency of fas or tnfr1 impacted outcome (194) . yet, during s. pneumoniae single infection, early cell death of macrophages is thought to limit an exuberant inflammatory reaction and accordingly, a study by steinwede et al. (195) revealed that neutrophil-derived trail limits tissue injury by inducing cell death in dr5-epressing lung macrophages in bacterial mono-infection (195) . in contrast, in the iav-s. pneumoniae superinfection mouse model, iavinduced trail has a detrimental effect on overall mortality (7), as trail-induced epithelial injury enhanced bacterial outgrowth of s. pneumoniae-administered at day 5 after iav infection-markedly. importantly, administration of anti-trail neutralizing antibodies enhanced bacterial control by the host organism. thus, the activation of ifn/trail-mediated signaling in viral infection has detrimental implication for outcome of secondary bacterial infection following viral insult, rendering the ifn/trail signaling axis an interesting therapeutic target not only in respiratory viral infections but also in complicating bacterial superinfection. an increasing number of reports connect progression of chronic respiratory disease to acute respiratory virus infection or proapoptotic signaling events. in fact, trail has been reported to be a critical determinant for promoting the development of chronic lung disease in early life (196) ; targeting trail by genetic deletion or neutralizing antibody application in early-life respiratory infections ameliorated infection-induced histopathology, inflammation, as well as emphysema-like alveolar enlargement and lung function. furthermore, trail was also shown to play a role in the development of allergy and asthma. trail is not only elevated in the sputum of asthmatic patients but has also been reported to be highly expressed in an experimental mouse model of asthma, where it induces ccl20 secretion by bronchial epithelial cells, thus promoting th2 cell responses and airway hyperreactivity (197) . in copd, acute exacerbations driven by viral and bacterial infection are a major factor increasing both mortality and morbidity, and both influenza and s. pneumoniae have been identified among the most common causes of copd exacerbations (198) . indeed, primary bronchial epithelial cells isolated from subjects with copd show an impaired production of type i ifn (199) , which has been implied in the enhanced susceptibility of copd patients to respiratory infections; however, even in absence of high ifn induction, both an abnormally elevated loss of alveolar epithelial cells due to apoptosis as well as elevated trail and dr5 levels were reported (200) , implying a possible link between viral/bacterial induction of trail and acute exacerbations in copd. trail induction has also been directly linked to cigarette-smoke exposure, a common cause of copd, and trail deficiency resulted in decreased pulmonary inflammation and emphysema-like alveolar enlargement in vivo (201) . moreover, increased levels of both trail and dr5 were associated to impaired lung function and increased systemic inflammation in human copd patients (202) . while alveolar epithelial cell death is closely connected to idiopathic pulmonary fibrosis (ipf), trail and its receptors dr4 and dr5 in aec were shown to be upregulated in ipf lungs (129) . also, in pulmonary arterial hypertension virus infection is considered to be a possible risk factor (203) , and pulmonary hypertension has been reported to be a side effect of prolonged treatment with type i ifn (204, 205) . in line, trail has been closely linked to disease progression in pulmonary hypertension. trail has been found to be increased within pulmonary vascular lesions of patients with pulmonary hypertension (206) and also in a mouse model of hypoxia-induced pulmonary hypertension, levels of soluble trail correlated with right ventricular systolic pressure, right ventricular hypertrophy, and pathologic alterations (33, 34) . importantly, neutralizing antibody-treatment against trail showed positive effects on survival while reducing pulmonary vascular remodeling (207) . notably, the extent to which infection-induced trail release causes or exacerbates chronic lung disease or in how far trail production in chronic lung diseases affects susceptibility to respiratory viral and complicating bacterial infection remains to be elucidated. respiratory viral infections are major causative agents for lung injury and ards; however, in many cases antivirals are not sufficient to limit disease (208). besides the fact that most viruses are subject to strong selective pressures that favor quickly evolving, drug-resistant virus variants, recent advances in understanding the processes that contribute to tissue injury and ards highlight a crucial role of immune-related, ifn-driven events. therefore, novel therapeutic strategies often aim to improve the outcome of severe respiratory infection by modulating host cell responses; however, to date, clinical trials trying to improve severe viral infections or ards outcomes by targeting host pathways have not resulted in approval of new drugs (122) . of note, for establishment of such therapies it has to be considered that the timing and intensity of induction and amplification as well as of dampening and termination of the ifn-driven immune response needs to precisely match the pathogen-and organ-specific requirements of a given infection. a non-controlled regulation of these processes may lead to either an unrestricted pathogen spreading or, on the other extreme, to an overshooting inflammatory response, including the increased production of pro-inflammatory and proapoptotic mediators, elevated levels of recruited immune cells, and/or aberrant repair processes. notably, both too low and too high levels of ifn-induced effects facilitate disease progression with a possible increase of fatal outcomes in ards patients (78) . accordingly, preclinical in vivo studies of ifn-directed therapies yielded seemingly adverse results, depending on the context, timing, and dosage of ifn modulation. however, in multiple settings of acute respiratory viral infection, studies demonstrate that an exaggerated signaling derived from type i ifn in an already inflamed tissue contributes to worsened outcomes, and importantly, might favor secondary bacterial superinfection [e.g., ref. (75, 76, 209) ]. interestingly, davidson et al. (209) demonstrated that type iii ifn release upon influenza challenge-in contrast to type i ifn induction-does not trigger an unbalanced inflammatory response that critically contributes to respiratory disease progression in vivo, highlighting it as a possible therapeutic option in iav-induced lung injury. most likely, this effect derives from the lack of the ifn-λr1/il-10r2 receptor complex, but presence of ifnar, on immune cells, including bone marrowderived macrophages. nonetheless, other reports identify ifn-λ as a driver of macrophage polarization to an inflammatory m1 phenotype (41) that has been attributed to further promote an overshooting inflammatory response, highlighting the need for further studies of type iii ifn biology in pathogen-associated disease progression. as generally ifn-directed therapeutic approaches target various downstream signaling events that might both act beneficially as well as detrimentally on viral replication and pathogenesis, a further approach is to address specific isgs that primarily show detrimental effects on disease progression. as outlined above, trail or its downstream signaling events might comprise a suitable target for adjunct therapies in addition to antivirals. accordingly, our own data in a preclinical mouse model of iav infection demonstrate a clear benefit of the systemic application of neutralizing antibodies against trail at days 3 and 5 postinfection for lung injury, morbidity, and mortality (10, 11) . targeting trail as a major determinant of disease severity in respiratory viral infections including iav, but also rsv and cov, may yield therapeutic approaches that are superior to ifn-directed strategies, as they seemingly do not bear the risk of compromising host defense. yet, it should be thoroughly excluded that blocking trail-induced cell death of infected cells will not lead to an overwhelming viral spreading, especially as reports on viral loads upon trail inhibition in preclinical models of iav are controversial (6, 10, 170) . accordingly, additional studies are needed to understand how and to which extent virus-infected cells can be killed or viral spreading can be controlled by other means in the absence of trail. moreover, targeting pathways and signaling hubs downstream of trail/drs, such as ampk (11), in a well-timed and lung compartment-specific way, may open new therapeutic avenues but requires more detailed preclinical studies on efficacies and side effects. a valid approach might be the use of a combination therapy of such a treatment together with a classical antiviral drug therapy limiting viral replication; however, exact dosage, timing, kinetics, and application routes remain to be defined. cp and sh performed bibliographic research and drafted the manuscript. this work was supported by the german research foundation (sfb-tr84 b2, sfb1021 c05, kfo309 p2/p8, exc147), by the german center for lung research (dzl), and by the german center for infection research (dzif). 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factor related apoptosis-inducing ligand axis in the pathogenesis of pulmonary arterial hypertension inhibition of tumor necrosis factor-related apoptosis-inducing ligand (trail) reverses experimental pulmonary hypertension luks am. ventilatory strategies and supportive care in acute respiratory distress syndrome ifnλ is a potent anti-influenza therapeutic without the inflammatory side effects of ifnα treatment the authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. is cited, in accordance with accepted academic practice. no use, distribution or reproduction is permitted which does not comply with these terms. key: cord-336201-fl606l3b authors: daryabor, gholamreza; atashzar, mohamad reza; kabelitz, dieter; meri, seppo; kalantar, kurosh title: the effects of type 2 diabetes mellitus on organ metabolism and the immune system date: 2020-07-22 journal: front immunol doi: 10.3389/fimmu.2020.01582 sha: doc_id: 336201 cord_uid: fl606l3b metabolic abnormalities such as dyslipidemia, hyperinsulinemia, or insulin resistance and obesity play key roles in the induction and progression of type 2 diabetes mellitus (t2dm). the field of immunometabolism implies a bidirectional link between the immune system and metabolism, in which inflammation plays an essential role in the promotion of metabolic abnormalities (e.g., obesity and t2dm), and metabolic factors, in turn, regulate immune cell functions. obesity as the main inducer of a systemic low-level inflammation is a main susceptibility factor for t2dm. obesity-related immune cell infiltration, inflammation, and increased oxidative stress promote metabolic impairments in the insulin-sensitive tissues and finally, insulin resistance, organ failure, and premature aging occur. hyperglycemia and the subsequent inflammation are the main causes of microand macroangiopathies in the circulatory system. they also promote the gut microbiota dysbiosis, increased intestinal permeability, and fatty liver disease. the impaired immune system together with metabolic imbalance also increases the susceptibility of patients to several pathogenic agents such as the severe acute respiratory syndrome coronavirus 2 (sars-cov-2). thus, the need for a proper immunization protocol among such patients is granted. the focus of the current review is to explore metabolic and immunological abnormalities affecting several organs of t2dm patients and explain the mechanisms, whereby diabetic patients become more susceptible to infectious diseases. the metabolic syndrome is defined by the presence of metabolic abnormalities such as obesity, dyslipidemia, insulin resistance, and subsequent hyperinsulinemia in an individual (1) . dyslipidemia, the main characteristic of metabolic syndrome, is defined by decreased serum levels of high-density lipoproteins (hdls) but increased levels of cholesterol, free fatty acids (ffas), triglycerides (tg), vldl, small dense ldl (sdldl), and oxidized ldl (ox-ldl) ( table 1 ) (2) . individuals with the metabolic syndrome are much more likely to develop type 2 diabetes mellitus (t2dm), cardiovascular diseases (cvds), and fatty liver disease (2) (3) (4) . t2dm, the most common form of diabetes (∼90%), is characterized by a systemic inflammatory disease accompanied by insulin resistance (ir) or decreased metabolic response to insulin in several tissues, including the adipose tissue, liver, and skeletal muscle, as well as by reduced insulin synthesis by pancreatic beta cells (4, 5) . studies on immunometabolism have indicated that the metabolic states and immunological processes are inherently interconnected (6) . in this scenario, metabolites derived from the host or microbiota regulate immunological responses during health and disease (6) . accordingly, in obese individuals, expanded adipose tissue at different locations, by initiating and perpetuating the inflammation, induces a chronic low-level inflammatory state that promotes ir (4). every organ system in human body can be affected by diabetes, but the extent of organ involvement depends largely on the severity and duration of the disease (figure 1 and table 1 ). during the progression of diabetes, hyperglycemia promotes mitochondrial dysfunction and induces the formation of reactive oxygen species (ros) that cause oxidative stress in several tissues such as blood vessels and pancreatic beta cells (7) (8) (9) . accumulating damage to the mitochondria, as well as several macromolecules, including proteins, lipids, and nucleic acids by ros promotes the process of aging (10) . as a result, pancreatic β cells that require functional mitochondria to maintain insulin synthesis fail to generate high enough levels of insulin (11, 12) . in the absence of compensatory mechanisms, stress-responsive intracellular signaling molecules are activated and cellular damage occurs. elevated intracellular levels of ros and subsequent oxidative stress play an important role in the pro-atherosclerotic consequences of diabetes and the development vascular complications (9, 13) . moreover, the non-enzymatic covalent attachment of glucose and its toxic derivatives [e.g., glyoxal, methylglyoxal (mgo), and 3deoxyglucosone] to the biological macromolecules such as nucleic acids, lipids, and proteins leads to the formation of advanced glycation end products (ages) (14, 15) . accumulated ages block the insulin signaling pathway and promote inflammation (16, 17) . in addition, the attachment of ages to their receptors [e.g., cd36, galectin-3, scavenger receptors types i (sr-a1), and ii (sr-a2)] on the surfaces of immune cells in the circulation and tissues activates the expression of pro-inflammatory cytokines and increases free radical generation (18) . furthermore, due to the chronic exposure of cells to high glucose levels in untreated t2dm patients, glucose toxicity might occur in several organs. this will figure 1 | effects of t2dm on body organs. t2dm is an inflammatory state that affects circulatory system, gastrointestinal tract, pancreatic beta cells, liver, and skeletal muscles and makes them dysfunctional. nfald, non-alcoholic fatty liver disease; nash, non-alcoholic steatohepatitis; er, endoplasmic reticulum. eventually lead to nephropathy, cardiomyopathy, neuropathy, and retinopathy. gut microbiome dysbiosis is another important factor that can facilitate the induction and progression of metabolic diseases such as t2dm (19) . the gut microbiome dysbiosis, by altering the barrier functions of intestine and the host metabolic status, promotes the insulin resistance in diabetic patients (19) . diabetes also impairs the immune system and increases the susceptibility of patients to serious and prolonged infections (20) . this is likely to be the case with the severe acute respiratory syndrome coronavirus 2 (sars-cov-2), as well (21, 22) . in the current paper we will review recent research to explore the impairment of body organs in t2dm patients and explain how diabetic patients become more susceptible to certain infectious diseases. vascular homeostasis is an important function of the endothelium. under homeostatic conditions, the ecs maintain the integrity of blood vessels, modulate blood flow, deliver nutrients to the underlying tissues, regulate fibrinolysis and coagulation, control platelet adherence and patrol the trafficking of leukocytes (figure 2a ) (23) . normal ecs also internalize high-density lipoproteins (hdls) and its main protein part apolipoprotein a-i (apoa-i) in a receptor-mediated manner to activate endothelial cell nitric oxide (enos) synthase and promote anti-inflammatory and antiapoptotic mechanisms ( figure 2b ) (24) . hdl receptors on the surfaces of ecs include: the atp-binding cassette (abc) transporters a1 and g1, the scavenger receptor (sr)-b1 and the ecto-f1-atpase (24) . according to the epidemiological studies, diabetes mellitus is considered as one of the main risk factors for cvd (figure 1 ) (25) . from the beginning of t2dm, the functions of ecs are impaired, which is the main cause of disease-related side-effects (26) . ecs can initiate and perpetuate the inflammatory milieu during the pathogenesis of diabetes. due to the negative impacts of hyperglycemia and subsequent oxidative stress, cvds are more common among diabetic patients (27) . it has been observed that incubation of human aortal endothelial cells (haecs) with a medium containing high glucose concentrations (hg, 20 mm) increases the intracellular levels of mgo and glycated proteins that in turn activate the unfolded protein response (upr) and trigger inflammatory and prothrombotic pathways (28) . glycated apoa-i, which is formed during hyperglycemia, modifies its structure, decreases its lipid-binding ability, prevents cholesterol efflux from macrophages and impairs its anti-inflammatory function (29, 30) . vaisar et al. have shown that hdls from diabetic patients have a reduced capacity to trigger enos production and suppress tumor necrosis factor-α (tnf-α)mediated inflammatory responses within ecs (31) . diseases such as t2dm that induce high levels of vascular injury are accompanied by an elevated number of circulating endothelial cells (cecs) (32) . t2dm-related risk factors such as dyslipidemia, hyperglycemia, and hyperinsulinemia as well as other conditions (e.g., inadequate physical activity, smoking, and high blood pressure) facilitate the formation of atherosclerotic plaques/lesions (33) . dyslipidemia, due to the elevated flux of ffa from insulin-resistant tissues and spillover from entry (c) blood vessels in t2dm patients. during the progression of the disease, red blood cells become glycated, while activated ecs synthesize elevated levels of adhesion molecules and chemokines that facilitate monocytes recruitment, adhesion, and transmigration across the endothelium toward the subendothelial region. monocytes are then differentiated into macrophages and eventually, by excess lipid uptake, generate foam cells. subsequently, further immune cell infiltration into the atherosclerotic lesion occurs, where their inflammatory cytokines promote platelet activation, ec apoptosis, and increased generation of ros and ox-ldl. (d) interactions between oxldl and its receptor aggravate ros generation, nf-κb activation and inflammation. ec, endothelial cell; rbc, red blood cell; plt, platelet; hdl, high-density lipoprotein; ox-ldl, oxidized low-density lipoprotein; ros, reactive oxygen species; enos, endothelial nitric oxide synthase; no, nitric oxide; lox-1, lectin-type oxidized ldl receptor 1. into adipocytes, is considered as an important risk factor for developing cvd among diabetic patients. this is because dyslipidemia promotes inflammation, endothelial dysfunction, and platelet hyperactivation (34, 35) . during the progression of atherosclerosis, lipids, immune cells, and extracellular matrix accumulate in the arterial intima or subendothelial regions ( figure 2c ) (33) . advanced plaques can impede blood flow and cause tissue ischemia or might become disrupted and generate a thrombus that stops the blood flow of important organs. vascular complications of diabetes engage either tiny or large blood vessels (micro-and macroangiopathy, respectively). microangiopathies, which can be seen in the kidneys, vasa nervorum and eye tissues, cause nephropathy, neuropathy, and retinopathy. macroangiopathies, by inducing atherosclerosis in the coronary, carotid, and peripheral arteries, increase the risk of myocardial infarction (mi), stroke and peripheral artery disease (pad). macrovascular complications due to ec dysfunction are considered as an important cause of mortality and morbidity among diabetic patients (36) . oxidative stress has an essential role in the induction of vascular complications during the course of diabetes (8) . ec dysfunction (e.g., delayed replication, dysregulated cell cycling, and apoptosis), as well as enhanced ox-ldl formation are some consequences of oxidative stress. it has been well-established that sdldl and ox-ldl have an enhanced atherogenic ability and are more useful biomarkers than total ldl for predicting cvd (37, 38) . sdldl particles have a smaller size than other ldl particles. thus, sdldl particles are more easily oxidized, and their atherogenic potential is enhanced. during oxidative stress, levels of ox-ldl increase by the excess action of reactive oxygen species (ros) (13) . subsequently, ox-ldl interaction with scavenger receptors, including cd36, sr-a1/cd204, sr-b1, and lectin-like ox-ldl receptor-1 (lox-1) on the surface of ecs activates the nadph oxidase that in turn increases the expression of ros and activates the transcription factor nf-αb (39) . afterwards, the expression of lox-1, adhesion molecules (e.g., selectins and integrins) and the secretion of pro-inflammatory cytokines and chemokines are increased, while no synthesis is decreased in ecs ( figure 2d ) (39) (40) (41) . ec-derived chemokines bind to their cognate receptors on the surfaces of monocytes and recruit them toward the inflamed endothelium. following this, selectin-based rolling and integrin-based attachment of monocytes to the ecs cause their migration toward the subendothelial region, where they develop into lipid-laden macrophages or foam cells later on (42) . the scavenger receptor lox-1 plays an important role in the uptake of ox-ldl during atherogenesis. it is strongly expressed on the surfaces of ecs, but has an inducible pattern of expression on the surface of macrophages and smooth muscle cells (43) . the accelerated uptake of ox-ldl by macrophages accounts for their transformation into foam cells, the initial hallmark of atherosclerosis (41, 43) . besides, diabetes leads to both quantitative and qualitative defects in circulating angiogenic progenitor cells (capcs) that take part in the repair of injured endothelium (44) . it has been shown that humans or mice with decreased numbers of cd31 + cd34 + cd133 + cd45 dim sca-1 + flk-1 + capcs have an increased prevalence of t2dm, elevated hba1c levels and aggravated cvd risk scores (44, 45) . in diabetic patients, despite elevated serum levels of proangiogenic molecules, like angiopoietin-1/2, epo, and vegf-a, angiogenesis is impaired. this is mainly due to the decreased expression levels of vegfr2 and cxcr4 on the surfaces of capcs, which makes them unresponsive to the angiogenic factors (44, 46) . it has also been shown that circulating proangiogenic granulocytes composed of eosinophils and neutrophils are also impaired in diabetic patients (47) . besides, elevated levels of ages in t2dm cause ec dysfunction and vascular inflammation (48) . ren et al. have shown that incubation of human coronary artery endothelial cells (hcaecs) with ages causes decreased expression (at both mrna and protein levels) and enzymatic activity of enos, increased levels of ros, diminished mitochondrial membrane potential and declined activity of catalase and superoxide dismutase in treated cells (49) . another study by lan et al. has shown that ages in the pancreas decrease ec viability and induce their apoptosis in an nfκb signaling-related manner (50) . however, apigenin (4 ′ ,5,7trihydroxyflavone) can protect ecs against oxidative stress and subsequent inflammatory reactions mediated by ages (51) . apigenin binds to methylglyoxal (mgo) and forms a complex that inhibits age formation. chettab et al. have shown that the expression of icam-1 as well as the production of il-8, are significantly increased in huvecs cultured in hg medium compared to cells cultured in normal glucose (ng, 5.5 mm) conditions (52). bammert et al. found out that incubation of huvecs with hg media promotes the generation of endothelial microparticles (emps) that, when added to normally cultured huvecs, downregulate the expression of anti-apoptotic microrna mir-let7a, but enhance the synthesis of active caspase-3 and cause cell apoptosis (53) . several micrornas, including mir-21, mir-26a, mir-30, mir-92a, mir-126, mir-139, mir-199a, mir-222, and mir-let7d, regulate vascular homeostasis. it has been shown that the expressions of mir-26a and mir-126 are significantly reduced in circulating mps isolated from diabetic patients compared with normal individuals. this could be involved in making diabetic individuals more susceptible to coronary heart disease (54) . moreover, hg media upregulate the expression of nadph oxidase that will induce the generation of ros. this leads to subsequent apoptosis of the huvecs through a ros-dependent caspase-3 pathway (55). su et al. have demonstrated that argirein medication, by inactivating nadph oxidase, can prevent endothelial cell apoptosis in a rat model of t2dm and hence attenuate vascular dysfunction (56) . hg further increases the permeability of the huvecs in a protein kinase c (pkc)-dependent manner (57, 58) . hassanpour et al. showed that incubation of endothelial progenitor cells with the serum of t2dm patients inhibits their migration toward bfgf, increases their expression of vegfr-2, but reduces their expression of vegfr-1 and induces their apoptosis (59) . however, humanin (hn), a mitochondriumderived peptide, is cytoprotective against apoptosis during pathological conditions, such as diabetes mellitus (60) . it has been demonstrated that simultaneous incubation of h9c2 cells, a line of rat cardiac myoblasts, with h 2 o 2 and hn decreases the intracellular levels of ros, preserve mitochondrial function/structure and decline cellular apoptosis (61) . wang et al. have indicated that the treatment of huvecs with hn before their incubation with hg medium increases the expression of enos, while decreasing the expression of endothelin 1 (et-1), vcam-1, tnf-α, il-1β, and e-selectin in a krüppellike factor 2 (klf2)-dependent manner. such changes in the expression of integrins prevent the attachment of monocytes to huvecs (62) . accordingly, hn might be used to prevent the development of hyperglycemia-associated ec dysfunction in t2dm. ec activation and expression of adhesion molecules also facilitate activation and adhesion of platelets. this will increase the risk of thrombosis and promote the development of thrombotic angiopathy, typical for diabetic patients. platelets are tiny anucleated cellular fragments generated from megakaryocytes in the bone marrow. they circulate in the blood for ∼5-9 days and play essential roles in hemostasis and in controlling vascular integrity (63) . circulating inactive platelets move in the proximity of vessel walls (figure 2a ) and rapidly get activated in response to vascular injury. at the end of their life, platelets are cleared from circulation with the action of the liver and spleen-resident macrophages. platelets have an essential role in the initiation and progression of inflammation. platelet hyperactivation that occurs during inflammatory states (e.g., t2dm) facilitates the pathogenesis of cvds ( figure 2c ) (64, 65) . it has been shown that elevated levels of resistin, an adipokine, in diabetic patients enhances oxidative stress, promotes endothelial dysfunction and facilitates platelet activation (66) . activated platelets with an increased mean volume [mean platelet volume (mpv)] secrete microparticles (mps) and soluble adhesion molecules (e.g., sp-selectin and scd40l) that in turn activate endothelial and immune cells (67) (68) (69) . higher levels of platelet-derived mps, which correlate positively with fasting blood sugar and glycated hemoglobin, have been shown in newly diagnosed t2dm patients compared to healthy individuals (70) . in t2dm patients thrombotic microangiopathies can lead to the development of cvds (71) . platelets in the patients adhere to ecs and aggregate more rapidly than in healthy individuals thereby increasing the risk of thrombosis. in a mouse model of t2dm, zhu et al. have shown that ages interact with cd36, a member of the type 2 scavenger receptor family, on the surfaces of murine platelets to activate them and induce a prothrombotic state (72) . elevated levels of the p2y12 receptor on the surface of platelets in t2dm expose diabetic patients to a prothrombotic condition. this receptor has an essential role in platelet activation (73) . zhou et al. have shown that long non-coding rna (lncrna) metallothionein 1 pseudogene 3 (mt1p3), which is markedly upregulated in megakaryocytes of t2dm patients, enhances the expression of p2y12 receptor in platelets (74) . they indicated that this is due to the inhibitory action of mt1p3 on mir-126. virtually all parts of the human digestive system, including the gastrointestinal tract, pancreas, and the liver are affected by diabetes. the git is populated with a myriad of microorganisms, including principally bacteria but also archaea, viruses, fungi, and protozoans that dynamically influence the health status and homeostasis of the host. the physiological functions of the git resident microbes improve gut integrity, protect against microbial pathogens and regulate immune responses (75) . mucosal barriers, such as intestinal epithelial cells (iecs) and the mucus layer, spatially isolate the host immune system and gut microbiota to prevent unnecessary immune activation and intestinal inflammation. they also facilitate the uptake of nutrients through receptors and transporters. however, hyperglycemia, in a glut2-dependent manner, can influence the mucus and alter the integrity of adherence and tight junctions between intestinal epithelial cells of diabetic mice. this will enhance the permeability of the intestinal barrier leading to so called "leaky gut." subsequently, hyperglycemia may facilitate the dispersal of an enteric infection into a systemic infection (figure 1 ) (76) . interestingly, the reversal of hyperglycemia, conditional deletion of glut2 from the iecs and inhibition of glucose metabolism will fix the barrier dysfunction and prevent the spread of bacteria (76). xu et al. have shown that faecalibacterium prausnitzii, one of the most frequent commensal bacteria in normal individuals with essential roles in gut homeostasis, generates anti-inflammatory molecules that enhance the expression of tight junctions and improve intestinal integrity during diabetes (77) . however, in some cases, gut microbiota dysbiosis or altered microbial composition of the intestines could induce t2dm and lead to its progression (78) . of interest, the widely used antidiabetic drug metformin can improve barrier integrity and restore the healthy microbiota composition of the gut in diabetic patients (79) . the intestinal commensal bacterium akkermansia muciniphila can also act as a sentinel to reduce microbial translocation across the gut and prevent the subsequent inflammation in patients with t2dm (80) . hyperglycemia can further decrease the intracellular levels of glutathione (gsh) but increase inos activity and no production in the iecs (81). zhao et al. have found out that hyperglycemia in a pkcα-dependent manner inhibits the ubiquitination, internalization and degradation of the divalent metal transporter 1 (dmt1) present on the microvillar membranes of iecs. subsequently, intestinal iron uptake is enhanced and accumulated iron ions aggravate diabetes-related complications and increase mortality (82, 83) . the pancreas consists of the exocrine and endocrine compartments. the endocrine part is made of different cell types, including α, β, δ, and ε cells that secrete glucagon, insulin, somatostatin, and ghrelin hormones, respectively. these cells are aggregated into specialized structures called islets of langerhans, which play an important role in controlling blood glucose levels through the secretion of insulin and glucagon. in t2dm, despite normal levels of β-cell replication and islet formation, β-cell apoptosis is increased so that the number of cells declines by ∼50% (figure 1 ) (84) . during the progression of t2dm, the insulin-resistant state forces β-cells to compensate for the lack of insulin by elevating its synthesis to restore the normal blood glucose level. however, in severe diabetic patients, β-cell exhaustion, and subsequent persistent hyperglycemia occur (7) . furthermore, chronic elevated serum levels of free fatty acids, seen in obesity and t2dm, induce lipotoxicity in beta-cells and suppress their insulin secretion ability (85) . to alleviate chronic inflammation, overcome insulin resistance (ir) and to prevent β-cell apoptosis, stem cells or stem cell derivatives such as insulin-producing cells (ipcs) and exosomes have been suggested (86) (87) (88) (89) . their effects are believed to be mainly due to their anti-inflammatory activities. secretagogin (scgn) is predominantly expressed by pancreatic β-cells protecting their normal functions. scgn also acts as an insulin binding protein to make it more stable, avoid its aggregation, improve its functions and enhance its secretion (90, 91) . in t2dm patients, due to the islet cell dysfunction and endoplasmic reticulum (er) stress, serum levels of scgn are elevated reflecting stress and dysfunctional islet cells (92) . moreover, in patients with t2dm, islet amyloid polypeptide (iapp or amylin), a peptide hormone and one of the main secretory products of pancreatic β-cells, tends to deposit in the islets of langerhans, form insoluble fibrils and impair secretory functions of β-cells (93) . iapp is costored with insulin in the secretory granules of pancreatic β cells. in steady-state conditions it regulates food intake, insulin secretion, and glucose metabolism (94). ribeiro et al. have noted that pancreatic extracellular vesicles (evs) from healthy individuals, but not from t2dm patients, directly bind to iapps and prevent amyloid formation within the pancreatic islets (95) . the authors showed that the altered protein-lipid composition of the evs is the main reason for this discrepancy (95) . however, chatterjee et al. have shown that β-cells from t2dm patients have a dysfunctional proteasome complex that fails to degrade pancreatic iapp, whereby amyloid formation is induced (96) . furthermore, in t2dm patients, lipids accelerate the formation of fibrillary iapp, which aggravates islet cell damage (97) . dhar et al. have demonstrated that chronic use of mgo in sprague-dawley rats increases the expression of nf-αb, mgo-derived ages and their receptors in pancreatic β cells. mgo can also induce apoptosis of islet β cells, increase fasting plasma glucose levels and impair glucose tolerance (98) . in t2dm patients the plasma level of mgo directly correlates with fasting blood sugar and hba1c levels (99) . bo et al. further showed that mgo in a dose-based manner impairs insulin secretion of pancreatic β-cell lines min6 and ins-1 through increased generation of ros and by induction of mitochondrial dysfunction (100). robertson et al. have found out that elevated levels of ros in pancreatic β-cells inhibit the pancreas duodenum homeobox-1 (pdx-1) transcription factor that is needed for insulin synthesis (7) . it has been shown that chronic use of mgo in animals could induce t2dm, while simultaneous use of alagebrium, which breaks age compounds, attenuates the disease (98) . it has also been reported that during the course of diabetes dedifferentiation and conversion of β-cells into αand δ-"like" cells occurs (101) . in conclusion, the pancreatic β cell function is progressively reduced during the progression of t2dm. the liver is by far the most important metabolic organ with essential roles in regulating homeostasis and mediating glucose and lipid metabolism. metabolic activities of the tissue are precisely controlled by the actions of metabolic substrates, including free fatty acids (ffas) and hormones (102) . t2dm patients usually suffer from a chronic liver condition called non-alcoholic fatty liver disease (nafld). it is characterized by steatosis that means ectopic fat storage in hepatocytes and subsequent insulin resistance (figure 1 ) (103) . lipid accumulation in hepatocytes leads to impaired biogenesis of mir-206 that facilitates insulin signaling and prevents lipogenesis (104) . several factors such as obesity, increased serum levels of fatty acids, and insulin resistance can increase the risk of fatty liver disease. p2y2 receptor, through the induction of the c-jun n-terminal kinase (jnk) and prevention of insulin signaling, can promote insulin resistance in hepatocytes in t2dm (105) . in some cases, nafld may progress into an aggressive form of inflammatory fatty liver disease called non-alcoholic steatohepatitis (nash), which might cause liver cirrhosis and organ failure (106). dang et al. have indicated that exosomes released from the adipose tissues of obese mice due to the smaller mir-141-3p content can promote insulin resistance in the murine hepatocyte cell line aml12 (alpha mouse liver 12) (107) . the adipokine visfatin that is released from the adipose tissue of obese individuals has also been shown to activate the pro-inflammatory stat3 signaling pathway and nf-κb in the human liver cell line hepg2 and promote their insulin resistant state (108) . nevertheless, the hepatocyte growth factor (hgf) can alleviate the insulin resistance of hepatocytes and control their triglyceride and cholesterol contents (109) . skeletal muscle (sm) is the main tissue that releases glucose after insulin stimulation. hence, insulin resistance in sm has a pivotal role in the metabolic dysregulation of t2dm. insulin resistance in sm is the primary defect of t2dm that facilitates the progression of fatty liver disease, deposition of fat in the liver (figure 1 ) (110) . skeletal muscle from diabetic patients expresses less genes related to insulin signaling and metabolic pathways, but more apoptosis and immune-related genes (111) . this inflammatory milieu is mainly due to the proinflammatory actions of obesity-related adipose tissue mediators, which are released into the circulation and promote inflammation within the sm (4). furthermore, obesity causes intermyocellular and perimuscular adipose tissue expansion that acts like adipose tissue depots to enhance sm inflammation (112) . it has been shown that human skeletal muscle cells (hsmc), isolated from diabetic patients, after a 24-h culture generate significantly more tnf-α, il-6, il-8, il-15, monocyte chemotactic protein (mcp)-1, growth-related oncogene (gro)-α, and follistatin compared to non-diabetic individuals (113) . this altered secretion of myokines (e.g., cytokines secreted by sms) is an intrinsic feature of sm during the progression of t2dm. in sm, glut-4, which is quickly translocated to the cell surface, facilitates glucose uptake in response to insulin hormone as well as muscle contraction. pinto-junior et al. have shown that the use of age-albumin in rats increases the expression of the inflammatory molecule nf-κb1 within the sm. nf-κb1 binds to the promoter of the glut-4 gene and suppresses its expression (at both mrna and protein levels) (114) . accordingly, glut-4 levels on the surfaces of sm decrease and subsequently, whole-body ir develops. the immune system is generally classified into two main arms, innate and adaptive (or acquired) immunity. adaptive immunity is mediated by b cells, which produce antibodies and t cells, which are classified into cd4 + helper cells and cytotoxic cd8 + cells. a considerable literature has discussed the dysfunctional immune responses in diabetic patients ( table 2 ) (115) (116) (117) (118) (119) (120) . abnormal immune cell activation and subsequent inflammatory environment has an essential role in the progression of t2dm (121) . in this regard, chronic inflammation due mainly to the activation of the myeloid cell lineage (e.g., macrophages and neutrophils), is directly related to the induction of ir (4, 122). their numbers are elevated, are larger and more granular, express diminished levels of antioxidant genes but elevated levels of pro-apoptotic and pro-inflammatory genes. complement system attachment of c-type lectin proteins to mannose residues is decreased, lectin pathway is impaired, cd59 activity is reduced, mac deposition in vascular walls is increased. dendritic cells (dcs) their numbers and activity are reduced. their cholesterol efflux is decreased, generate foam cells, have dysfunctional efferocytosis. are activated, constitutively release nets, produce high levels of mpo, ros, and calprotectin (s100a8/a9), are more susceptible to apoptosis, their migration, phagocytosis and microbial killing are impaired. nk cells their numbers are increased but are usually dysfunctional, express high levels of glut4 but decreased levels of nkg2d and nkp46, have reduced degranulation capacity, are more susceptible to apoptosis. nkt cells their numbers are increased, produce high levels of ifn-γ, il-4, and il-17, express high levels of nkp30, nkg2d, and nkp44 but low levels of nkg2a and 158b. innate lymphoid cells (ilcs) ilc1s are increased and produce high levels of ifn-γ. humoral immunity (b cells) germinal centers are reduced, ab production and isotype switching is defective, abs become glycated, abs fail to activate complement. functions of osteoclasts, which are bone-resident innate immune cells (126) . this may affect bone structure and delay bone healing. defects in the innate, as well as adaptive immunity, are supposed to be the main cause of diabetic individuals' susceptibility to infections (127) . furthermore, some microorganisms, especially bacteria, in hyperglycemic conditions are better nourished and become more virulent, while also having a better milieu to cause infections. complement system the complement system is a first-line defense mechanism against invading microorganisms. it acts via different but interconnected classical, alternative, and lectin pathways (128) . ilyas et al. have shown that under high glucose conditions, the attachment of ctype lectin proteins to high-mannose containing glycoproteins is substantially decreased in a dose-dependent manner. these carbohydrate-binding proteins include mannose-binding lectin (mbl), surfactant protein d (sp-d), dendritic cell-specific intercellular adhesion molecule-3-grabbing non-integrin (dc-sign, cd209), and dc-sign-related (dc-signr) protein (129) . reduced binding of mbl in the presence of high levels of sugar causes a significant reduction in the lectin pathway activity, but does not influence classical or alternative pathway activity (129) . nevertheless, barkai et al. did not find significant differences in the function of classical or mbl pathways between t2dm and healthy individuals (130) . however, significantly decreased activity of ficolin-3-mediated lectin and alternative pathways, as well as decreased levels of c4d and soluble complement c5b-9 (sc5b-9) were seen in diabetic patients with escherichia coli-mediated urinary tract infections (130) . this may be linked to a reduced ability of diabetics to protect themselves against bacterial infections. the lipopolysaccharides of certain gram-negative bacteria, like salmonella serotype o6,7 as well as the cell walls of fungi, are rich in mannose. possibly, because of this, in addition to additional provision of nutrients, an increased prevalence of fungal infections is seen in t2dm patients (131, 132) . patel et al. found a significantly higher prevalence of oral candida carriage in diabetic patients compared to healthy controls (131) . they found that candida albicans was the most commonly isolated species followed by c. tropicalis, but uncommon species such as c. lusitaniae and c. lipolytica were also isolated (131) . another study by jhugroo et al. showed that c. albicans is the predominant yeast isolated from oral mucosal lesions of diabetic patients, followed by. c. tropicalis and c. krusei dendritic cells (dcs) are a heterogeneous population of specialized and professional antigen-presenting cells (apcs) that create a crucial link between the innate and adaptive immune responses (136, 137) . some studies have shown that the numbers of dcs are reduced in both type 1 and 2 diabetes (138, 139). seifarth et al. have found that t2dm patients with poor metabolic control have decreased numbers of both myeloid and plasmacytoid dcs compared with healthy controls. this could make them more susceptible to opportunistic infections (139) . in the case of good blood glucose control, the reduction in dc numbers was less prominent but still significant, especially for myeloid dc1 (mdc1) cells (139) . another study by blank et al. demonstrated that women with t2dm and poor glycemic control (hba1c ≥ 7%) have fewer numbers of circulating plasmacytoid dcs (pdcs) compared to diabetic women with good glycemic control (hba1c < 7%) or to healthy women (140). montani et al. have recently shown that hyperglycemic medium and hyperglycemic sera derived from t2dm patients prevent the maturation of monocytes into effective dcs and their activation in vitro (141) . interestingly, quercetin, a flavonoid with antiinflammatory and antioxidant characteristics, prevented such effects (141) . macrophages are important immune cells that play critical roles through all stages of the pathogenesis of t2dmrelated atherosclerosis (41). swirski et al. have shown a significantly elevated number of pro-inflammatory monocytes in the circulation of apoe −/− mice, an animal model of atherosclerosis, compared to control mice (142) . modifications of the lipoproteins in the arterial walls of diabetic individuals make them pro-inflammatory and activate the overlying endothelium. in response, monocytes are recruited into the subendothelial region, differentiate into macrophages and internalize the accumulated lipoproteins. finally, cholesterol-laden foam cells are generated. they promote inflammation and progression of the disease through the synthesis and secretion of cytokines, chemokines, ros, and matrix metalloproteinases (mmps) (figure 2c ) (42) . foam cells lose their migratory potential, die by apoptosis and generate a necrotic core within the atherosclerotic plaque (143) . it has been demonstrated that the use of mesenchymal stem cells in apoe −/− mice reduces the numbers of monocytes/macrophages at the site of inflammation, decreases lipid deposition and diminishes plaque size (144). ma et al. have studied the effects of long-term hyperglycemia in diabetic mice and found out that compared to non-diabetic control mice, the numbers of f4/80 + macrophages isolated from spleen (spms), as well as from peritoneal exudates (pems) of diabetic mice are significantly decreased (145) . subsequently, sun et al. showed that stimulation of pems from diabetic mice in vitro with ifn-γ and lipopolysaccharide (lps) significantly decreased the expression of intercellular adhesion molecule 1 (icam-1 or cd54), cd86, tnf-α, and il-6, while it increased the production of nitric oxide (no) (146) . they further showed that stimulation of pems isolated from diabetic mice with il-4 caused an enhanced arginase activity (146) . kousathana et al. have demonstrated that circulating monocytes isolated from diabetic patients produce higher levels il-6, while having an impaired activation of the nlrp3 inflammasome and subsequently reduced il-1β production (147) . however, they showed that proper glycemic control would restore such modifications. poor inflammatory responses in circulating monocytes, as well as in macrophages, are responsible for elevated susceptibility to infections and their severity in patients with t2dm. macrophages play a critical role in tissue repair. early in wound healing, they are pro-inflammatory to clear pathogens and debris but later, they resolve inflammation and promote tissue repair. in pathological conditions, failure to transform from pro-inflammatory to the anti-inflammatory proliferative phase can cause chronic inflammation in the affected tissue (148). have shown that an impaired wound healing process in animals with t2dm is due to high levels of nlrp3 inflammasome activity, which promotes the generation of il-1β and il-18 in macrophages (149, 150) . efficient skin wound healing process is mediated by the up-regulation of the peroxisome proliferatoractivated receptor (ppar)-γ in macrophages that convert their pro-inflammatory phenotype into healing-related. pparγ suppresses cytokine production by macrophages and hence is upregulated in inflamed tissue-resident macrophages. however, in t2dm, pparγ expression is down-regulated in skin-resident macrophages that enhance the activity of nlrp-3 inflammasome and cause chronic inflammation. using myeloid-specific pparγ −/− mice, it has been shown that the absence of ppar-γ in macrophages is sufficient to delay the healing process and extend tissue inflammation (150) . in t2dm patients, chronic hyperglycemia and hyperlipidemia trigger the secretion of a damage-associated s100a8 molecule (calgranulin a) from pancreatic islets that in turn increase macrophage infiltration (151) . westwell-roper et al. have shown that iapp aggregates in t2dm patients polarize islet-resident macrophages toward the m1-like f4/80 + cd11b + cd11c + phenotype that produces pro-inflammatory cytokines, including tnf-α, il-1β, and il-6. furthermore, m1 cells promote islet inflammation, cause β-cell malfunction and apoptosis (152) . in t2dm, excess phagocytosis of apoptotic β-cells by macrophages induces their lysosomal permeabilization, generation of ros, inflammasome activation, and pro-inflammatory cytokines secretion (153) . collectively, these observations reveal that the functions and plasticity of macrophages are compromised during the progression of t2dm. neutrophils are the most prevalent circulating leukocytes and one of the main components of innate immunity. they are recruited to the sites of infection through chemotaxis following complement activation, most importantly by c5a. activated neutrophils bind via their surface receptors to induced ligands on the surfaces of inflamed endothelial cells to migrate to tissues. there they phagocytose and kill invading microbes with lysosomal enzymes, antimicrobial peptides and by the generation of ros (154). neutrophils from patients with t2dm, but not from healthy individuals, are activated and produce elevated levels of ros. so, it could increase the risk of random organ injury (155) . in diabetic patients, the plasma levels of homocysteine are elevated, which is mainly due to its impaired clearance rate (156) . this will induce neutrophils to constitutively release neutrophil extracellular traps (nets) that can cause vascular damage and delays in wound healing (157, 158) . it has been shown that the circulating level of hydrogen sulfide (h 2 s) is significantly reduced in fasting blood of patients with t2dm compared with healthy individuals as well as in streptozotocin-induced diabetic rats compared with controls (159) . h 2 s is produced from cysteine by the action of several enzymes. it acts as a regulator of cell signaling and homeostasis (160) . it is essential to maintain balanced levels of antioxidants and protect tissues from oxidative stress (160) . the use of h 2 s or the endogenous l-cysteine in vitro blocks the production of il-8 and monocyte chemoattractant protein-1 (mcp-1) in the human u937 monocyte cell line incubated in high-glucose medium (159) . yang et al. have shown that h 2 s treatment decreases netosis and enhances the healing process of diabetic wounds by preventing ros-dependent erk1/2 and p38 activation (161) . it has been shown that the levels of net components, including histones, elastase and proteinase-3, are elevated in the sera from patients with diabetic foot ulcers (162) . wang et al. have recently indicated that hg dramatically enhances nadph oxidasedependent net generation in diabetic rats and humans. it was proposed that this could have a role in the induction of diabetic retinopathy (163) . indeed, patients with t2dm have elevated plasma levels of mgo, which can induce the production of proinflammatory cytokines like tnf-α, il-6, and il-8 by neutrophils and make them more susceptible to apoptosis (99) . myeloperoxidase (mpo), which is abundantly produced by neutrophils, but only to a small extent by monocytes and macrophages, might be useful as an early biomarker of inflammation in diabetic individuals (164) . binding of mpo to endothelial cells increases its half-life. thereby, more proinflammatory oxidant hypochloric acid (hclo) is generated that extends the damage to blood vessels (165) . in t2dm patients, neutrophil activities, including migration, phagocytosis and microbial killing are impaired. this makes diabetic individuals more susceptible to infections (166) . it has been welldocumented that neutrophils isolated in animal models of t2dm have an impaired tlr4 signaling pathway. this is reflected as a diminished cytokine and chemokine production, possibly as a consequence of reduced phosphorylation of nfκb and iκbα (167) . the half-life of these neutrophils as well as their in vivo migration and myeloperoxidase activity are decreased. during hyperglycemia, neutrophils produce calprotectin (s100a8/a9), which interacts with the receptor for advanced glycation end products (rage) on the surface of hepatic kupffer cells and promotes the synthesis of il-6 (168). subsequently, il-6 stimulates hepatocytes to increase the generation of thrombopoietin that in turn attaches to its receptor on the surfaces of bone marrow precursor cells and megakaryocytes to enhance their proliferation and expansion. this results in reticulated thrombocytosis, which means elevated megakaryocyte activity and thrombopoiesis. interestingly, diabetes-related thrombocytosis and subsequent atherothrombosis can be reduced by lowering blood glucose, depleting kupffer cells or neutrophils or by preventing the binding of s100a8/a9 to rage using paquinimod (168) . thom et al. have shown that the incubation of human and murine neutrophils with hg medium would cause their cytoskeletal and membrane instability. this will induce the generation of 0.1 to 1 µm diameter microparticles and activate the nlrp3 inflammasome (169) . microparticles, which are potently pro-inflammatory, are found in the circulation of healthy individuals, but their generation is increased during cell activation in several diseases, including t2dm and cardiovascular diseases (170, 171) . furthermore, serum levels of soluble fasl (sfasl) are increased in patients with t2dm thereby activating neutrophils and aggravating the inflammatory milieu (172, 173) . the proinflammatory roles of sfasl are mediated through increased amounts or activity of nfκb, il-1β, caspase-1, cd11b/cd18, and ros (173) . caspase-1 activation prevents the sfasl-dependent apoptosis of neutrophils and inhibits their expression of fas and caspase-3 (173) . accordingly, hyperglycemia disturbs the normal functions of neutrophils and increases the susceptibility to infections by pathogenic microorganisms. the expression level of nkg2d is negatively correlated with hba1c levels implying that chronic hyperglycemia would cause nk cell dysfunction (176) . also, hyperglycemia increases the expression of unfolded protein response (upr) genes in nk cells and induces their apoptosis (176) . nkt cells express simultaneously markers of both t cells (tcr and cd3) and nk cells [cd16, cd56, cd314 (nkg2d), and cd337 (nkp30)]. nkt cell subsets produce a broad range of cytokines, including gm-csf, ifn-γ, tnf-α, il-2, il-4, il-5, il-9, il-10, il-13, il-17, and il-21 (178) . they recognize lipids and glycolipids presented by cd1d molecules. phoksawat et al. have shown that the frequency of cd3 + cd4 + cd28 null cd56 + nkg2d hi nkt cells, which produce high levels of il-17, are increased in diabetic patients and their numbers are directly correlated with hba1c levels (179, 180) . lv et al. have recently shown that the numbers of cd3 + cd56 + nkt cells are higher in diabetic patients compared to healthy individuals (181) . they further showed that such cells are mostly cd4 + , produce elevated levels of ifn-γ and il-4 and express high levels of nkp30, nkg2d, and nkp44 but low levels of inhibitory receptors nkg2a and 158b (181) . the co-culture of these cells with huvecs significantly decreased their proliferation and migration abilities that were mainly il-4dependent (181) . taken together these studies show that diabetic individuals appear to have elevated levels of inflammationpromoting nkt cells. ilcs are critical effectors of innate immunity that produce both regulatory and pro-inflammatory cytokines to promote tissue repair, immunity, and inflammation (182) . mature ilcs lack the tcrs. based on their cell surface markers, cytokine production as well as expression of transcription factors the ilcs are classified into types 1, 2, and 3 (183) . these correspond to the different types of cd4+ t helper cells: th1, th2, and th17, respectively. ifn-γ is the cytokine signature of ilc1s, while type 2 cytokines (e.g., il-5 and il-13) are mainly produced by ilc2s and the main product of ilc3s are il-17 and il-22. regarding transcription factors, t-bet is mainly expressed by ilc1s, gata3 and rorα are mostly expressed by ilc2s and rorγt is predominantly expressed by ilc3 (183) . in t2dm, the numbers of circulating as well as adipose tissue-resident ilc1s are increased compared with normal individuals (184, 185) . the frequency of circulating ilc1s is positively correlated with fasting plasma glucose (fpg), hba1c, homeostasis model assessment for insulin resistance (homa-ir), serum-free fatty acids (ffas) and adipose tissue insulin resistance index (adipo-ir) (184, 185) . it has also been shown that patients with increased numbers of ilc1 have an elevated risk of developing t2dm (184) . a study by wang et al. indicated that adipose tissue-resident ilc1s, via the production of ifn-γ, promote tissue fibrosis and induce diabetes in obese individuals (185) . liu et al. have demonstrated that the numbers of ilc2s as well as serum cytokine levels of il-4, il-5, and il-13 are significantly elevated in diabetic kidney disease patients and have a positive correlation with disease severity (186) . they further demonstrated that ilc2s, through the tgf-β1 signaling pathway, are involved in renal fibrosis seen in diabetic kidney disease (184) . however, galle-treger et al. indicated that the engagement of the glucocorticoid-induced tumor necrosis factor receptor (gitr/or tnfrsf18) on the surface of activated ilc2s promotes their secretion of il-5 and il-13, ameliorates glucose homeostasis, protects against the onset of and improves established insulin resistance (187) . the protective role of ilc2s during acute metabolic stress has also been well-documented by dalmas et al. (188) . humoral immunity (b cells) elevated levels of blood glucose generate covalent sugar adducts with several proteins through non-enzymatic glycation. this can impair humoral immunity in many ways, e.g., by modifying the structure and functions of immunoglobulins (igs) (189) (190) (191) (192) (193) (194) . such modifications in the structure of igs can be determined using matrix-assisted laser desorption ionization (maldi) mass spectrometry (119, 191) . the molecular mass of igs in diabetic patients is higher than in normal subjects (189) . this can lead to reduced efficiency of vaccines that stimulate humoral immunity in these patients. it has been shown that immunization with influenza (flu) vaccines in diabetic patients induces normal or even elevated levels of flu-specific antibodies compared with normal individuals (195) (196) (197) (198) . however, the ability of the dysfunctional glycated antibodies to neutralize viruses is impaired, which will increase the susceptibility to infections. farnsworth et al. have shown that in t2dm, class switch defects in the assembly of antibody genes are also present (199) . in a model system, mice with t2dm have decreased amounts of specific anti-staphylococcus aureus antibodies (total as well as igg), which will increase the risk of infection and morbidity of diabetic mice. however, the levels of igm were elevated, but inefficient in protecting against infection, possibly because of their inability to directly promote phagocytosis. in another study, farnsworth et al. have demonstrated that defects in humoral immunity, as shown by decreased levels of total igg and anti-staphylococcus aureus antibody, aggravate foot infections in a murine model of t2dm (200) . this was due to a reduced germinal center induction and decreased numbers of t and blymphocytes within the germinal centers. this causes failures in antibody generation and class-switch recombination (200) . mathews et al. have shown that the protective levels of antibodies against streptococcus pneumoniae surface protein a are lower in diabetic patients compared to non-diabetic individuals. these antibodies also have a reduced potential to trigger complement activation on the surface of pneumococci, whereby phagocytosis of the bacteria becomes compromised (201) . they showed that hyperglycemia reduces both the antibody titers as well as the ability to deposit complement on the bacteria. the abovementioned changes in the ability to protect against s. aureus and s. pneumoniae are important, because these bacteria belong to the most common infection-causing pathogens in diabetic patients. another major group is constituted by gram-negative bacteria that commonly cause e.g., urinary tract infections. many studies have shown that t-cell functions are impaired in individuals with t2dm (202) (203) (204) (205) . elevated levels of activated cd4 + cd278 + t helper cells, cytotoxic t-cells, and th17 cells have been observed in obese diabetic patients compared to nonobese ones (205, 206) . nevertheless, pbmcs isolated from obese diabetic patients produced smaller amounts of il-2, il-6, and tnf-α after stimulation with phytohemagglutinin (pha) (205) . martinez et al. indicated that diabetic patients have reduced pathogen-specific memory th17 responses as well as decreased numbers of cd4+ t cells in response to stimulation with streptococcus pneumoniae (206) . th17 cells are critical for the recruitment of neutrophils to the infection site and improve the phagocytosis of invading bacteria and yeast (207) . moura et al. have shown that diabetic patients, particularly those with foot ulcers, have reduced levels of naive t-cells, but an elevated number of effector t cells and a reduction in the tcr-vβ repertoire diversity (204) . the observed changes are mainly due to an abnormal amount of inflammatory cytokines (e.g., ifn-γ and tnf-α) produced during infection and to subsequent robust stimulation of t-cells. leung et al. have reported that ischemic tissues of t2dm patients contain elevated numbers of tnf-α and ifn-γ producing th1 cells but diminished numbers of regulatory t cells (tregs), which suppress angiogenesis and decrease vascular density (208) . the high rate of infectious diseases in t2dm patients might also be linked to a reduction in the mitochondrial dna function that causes downstream lymphocyte dysfunction and subsequently increased susceptibility to infection (209) (210) (211) (212) . in support, we have recently shown that the numbers of ifn-γ producing cells against cytomegalovirus (cmv), epstein-barr virus (ebv), and influenza virus are fewer in t2dm patients compared to normal controls (202) . kumar et al. have also investigated the functions of cd8 + t cells and nk cells in the whole blood of t2dm patients infected with mycobacterium tuberculosis (m.tb). compared to controls, the patients exhibited a reduction in cytokine production (ifn-γ, il-2, il-17a/f, and tnf-α) and decreased expression of cytotoxic molecules (perforin, granzyme b, and cd107a) (203, 213) . these studies conclude that the functions of both cd4 + and cd8 + t-cell are defective in t2dm patients. t2dm is usually associated with an elevated risk of asymptomatic bacteriuria, urinary tract infections (utis), pyelonephritis and non-sexually transmitted genital infections, such as balanitis and vulvovaginal infections (213) (214) (215) . the incidence of infections with a complicated course is significantly higher in diabetic patients compared to healthy controls ( table 3) . it seems that it is principally defects in the innate immune responses of diabetic individuals that are responsible for the increased susceptibility and prevalence of infections (4, 225 (199, 201) cd8 + tcells mycobacterium tuberculosis (203, 213) susceptible to the causative pathogen of lyme disease, borrelia burgdorferi (216) . the disease is mainly due to the ability of the bacteria to escape complement opsonization and attack, which leads to an impaired uptake and killing of bacteria by neutrophils (227) . neutrophil dysfunction also increases the susceptibility of diabetic animals to staphylococcus aureus (217) (233) . during the progression of t2dm in human subjects, the basal phenotype of macrophages is altered so their capacity to control mycobacterium tuberculosis is diminished (222) . martinez et al. have indicated that alveolar macrophages isolated from diabetic mice express decreased levels of macrophage receptor with collagenous structure (marco) and cd14 that are engaged in the recognition of trehalose 6,6'-dimycolate, a bacterial cell wall component (223) . diabetes increases the severity of tuberculosis (tb) and enhances the risk of progression to the active form in latent infections (234, 235) . diabetic tb patients have elevated frequencies of th1 and th17 cells as well as increased serum levels of inflammatory cytokines, including ifn-γ, tnf-α, il-1β, il-2, il-6, il-17a, and il-18 but decreased levels of il-22 compared to non-diabetic tb patients. this can contribute to dysfunctional immune responses and poor immune control of a tb infection (236) . a positive correlation between the serum levels of ifn-γ, tnf-α, il-2, and il-17a with hb-a1c levels was also observed. this indicates an association between impaired control of diabetes and the proinflammatory milieu. tripathi et al. have demonstrated that serum levels of il-22 were significantly decreased in tb-infected t2dm mice and humans compared to non-diabetic tb-infected mice and humans (224) . they revealed that the treatment of tb-infected diabetic mice with recombinant il-22 or ilc3s (cellular source of il-22) increased the survival of mice, prevented the accumulation of neutrophils near alveoli, diminished the generation of neutrophil elastase 2 (ela2) and prevented epithelial cell damage (224) . tan et al. have shown that b. pseudomallei and m. tuberculosisinfected pbmcs of diabetic patients fail to produce il-12. this leads to a decreased ifn-γ production, poor bacterial killing and elevated intracellular bacterial loads (237) . an impaired il-12 production is mainly due to decreased intracellular glutathione (gsh) concentrations within the infected cells of diabetic individuals (237) . such a combination of an inflammatory microenvironment and dysfunctional immune responses enhances the bacterial load and can subsequently amplify lung injury and fibrosis in diabetic tb patients. chellan et al. have further shown that infections caused by enterococcus faecalis, staphylococcus aureus, and pseudomonas aeruginosa are more prevalent in the wounds of diabetic patients (238) . t2dm patients are more susceptible to utis caused by antibioticresistant escherichia coli, proteus spp., klebsiella spp., coagulasenegative staphylococci, enterobacter spp., and enterococci (215, 239) . diabetic patients are also more susceptible to helicobacter pylori (h. pylori) infections (240). cui et al. have recently reported that t2dm patients have an increased risk of infection with kaposi's sarcoma-associated herpesvirus (kshv or hhv-8) (241) . they further showed that the viral load and antibody titers are positively correlated with blood glucose levels (241) . diabetic patients also have been shown to have an increased risk of infection with the severe acute respiratory syndrome coronavirus (sars-cov) ( (248) . the influenza virus that usually causes self-limiting infections can induce severe forms of the disease in diabetic patients (249, 250) . following the 2009 h1n1 influenza pandemic, diabetic individuals suffered from more severe infections compared to non-diabetic people (251, 252) . diabetic patients have also a higher prevalence of chronic cytomegalovirus (cmv), herpes simplex virus (especially hsv-1), and varicellazoster virus infections (253) (254) (255) . accordingly, it seems that the immune response against viruses is impaired in diabetics, and these patients need more care during viral infections. coronavirus virions are enveloped positive-strand rna spherical viruses with a diameter of ∼125 nm characterized by spike proteins projecting from their surface and with an unusual large rna genome (256) . the spike (s) protein of the virus binds to its receptor on the surface of cells by which intracellular proteases are induced (257) (258) (259) . subsequently, the s protein priming and cleavage occurs that allow viral fusion to the plasma membrane and entrance of viral genome into the cells (259) . sars-cov and sars-cov-2 use angiotensin-converting enzyme 2 (ace2) as their receptor while mers-cov uses dipeptidyl peptidase-4 (dpp4) to enter the cells (260, 261) . ace2 is strongly expressed in blood vessels, pancreas, intestine, brain, lungs, heart, and testis (262) . interestingly, nasal epithelial cells, especially goblet, and ciliated cells express the highest levels of ace2 and the intracellular protease transmembrane serine protease 2 (tmprss2) that facilitates the entrance of the sars-cov-2 (263) . furthermore, the expression of ace2 is significantly up-regulated in diabetic patients and those treated with ace inhibitors (264) . coronaviruses cause respiratory, enteric and central nervous system (cns) diseases in various animal species except rats and mice (264) . most coronavirus infections are mild, but major outbreaks of deadly pneumonia have been caused by sars-cov, mers-cov, and sars-cov-2 in 2002, 2014, and 2019-2020, respectively (265) . on march 11, 2020, the world health organization (who) announced the pandemic of sars-cov-2, the etiologic agent of coronavirus disease-19 (covid-19) (265) . the novel coronavirus pandemic, which has emanated from wuhan, china, promotes symptoms similar to those caused by the sars-cov outbreak in 2002. the viral pandemic, which has put the world on alert, has caused over 7.9 × 10 6 confirmed human cases and at least 43 × 10 4 deaths throughout the world (https://www.worldometers.info/coronavirus/) by june 14, 2020. most of the infected people experience only mild to moderate respiratory disease and recover soon without the need for special treatment. however, aged individuals and those with health problems, including diabetes, obesity, cardiovascular disease (cvd), hypertension, immune deficiency, and chronic respiratory disease are more likely to develop serious illness (https://www.who.int/health-topics/coronavirus#tab= tab_1). patients death is mainly due to the acute respiratory distress syndrome, disseminated intravascular coagulation, hemorrhage, coagulopathy, acute organ (e.g., kidney, heart, liver) injury, multi-organ failure, and secondary bacterial infections (266) . elevated levels of adipose-tissue derived adipokines, interferon, and tnf-α in diabetic patients may impair immune-responses against sars-cov-2 (267, 268) . it has been shown that diabetic patients have impaired clearance of sars-cov-2 from their circulation (269) . accordingly, diabetic patients due to the diminished viral clearance, impaired t cell function, and accompanied cardiovascular disease are more susceptible to the coronaviruses infection and subsequent cytokine release syndrome (crs) (270, 271) . in support, elevated levels of il-1β, il-2, il-6, il-7, il-8, il-10, ifn-γ, interferon gamma-induced protein 10 (ip-10), granulocyte colony-stimulating factor (g-csf), macrophage inflammatory protein 1α (mip1α), serum ferritin, fibrinogen, plasminogen, c-reactive protein (crp), and d-dimer have been observed in patients with covid-19 (266, 269, 272, 273) . covid-19 patients, especially those requiring intensive care unit (icu) have decreased total lymphocytes (lymphopenia), t cells (both cd4+ and cd8+), b cells, and nk cells (274, 275) . it should be noted that most of the surviving t cells in such patients have an exhausted phenotype (274) . consequently, disease severity is mainly because of the host immune response to viral infection. current evidence about the relationship between pathophysiological mechanisms of diabetes and covid-19 are limited and further research is still needed. patients with t2dm have an elevated risk of infection with plasmodium falciparum (276) , toxoplasma gondii (277), opisthorchis viverrini (278), strongyloides stercoralis (279), cryptosporidium parvum (280), blastocystis hominis (281), ascaris lumbricoides (280, 282, 283) , and giardia lamblia (283) . interestingly, diabetic patients who were treated with metformin had less p. falciparum infections compared to untreated patients (276) . omaña-molina et al. have shown that in a mouse model of t2dm the animals have an increased susceptibility to granulomatous amoebic encephalitis (gae) caused by trophozoites of acanthamoeba culbertsoni (284) . the possible reasons for the increased risk of diabetics for parasitic infections are metabolic abnormalities and immune dysregulation. chellan et al. have shown a higher prevalence of fungal infections in the wounds of diabetic patients (238) . the prevalence correlated with the levels of hba1c. the most widely observed fungal isolates were c. albicans, candida parapsilosis, c. tropicalis, trichosporon asahii, and aspergillus species. some of them were resistant to antifungal medications (238) . al mubarak et al. have also demonstrated that diabetic patients with periodontitis are more susceptible to infection with c. albicans, c. dubliniensis, c. tropicalis, and c. glabrata (285) . the incidence of candidiasis was significantly increased in patients over the age of 40 with hba1c > 9 (285). it has also been shown that diabetic patients are more susceptible to utis caused by c. albicans (239) . hyperglycemia impairs the normal functions of the circulatory system, gastrointestinal tract, pancreatic beta cells, liver as well as of skeletal muscles to boost systemic insulin resistance. a hyperglycemic environment also leads to immune cells dysfunction. it increases 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human vascular endothelial cells is mediated through nf-kappab and c-jun nh2-terminal kinase pathway and prevented by pi3k/akt/enos pathway improvement of vascular dysfunction by argirein through inhibiting endothelial cell apoptosis associated with et-1/nox4 signal pathway in diabetic rats high glucose-induced human umbilical vein endothelial cell hyperpermeability is dependent on protein kinase c activation and independent of the ca 2+ -nitric oxide signalling pathway effects of high glucose on human umbilical vein endothelial cell permeability and myosin light chain phosphorylation functional convergence of akt protein with vegfr-1 in human endothelial progenitor cells exposed to sera from patient with type 2 diabetes mellitus humanin: a harbinger of mitochondrialderived peptides? a humanin analog decreases oxidative stress and preserves mitochondrial integrity in cardiac myoblasts humanin prevents high glucose-induced monocyte adhesion to endothelial cells by targeting klf2 novel clearance mechanisms of platelets flow cytometric analysis of platelets type 2 diabetes mellitus reveals 'angry' platelets platelet activity and hypercoagulation in type 2 diabetes increased circulating resistin is associated with insulin resistance, oxidative stress and platelet activation in type 2 diabetes mellitus increased levels of soluble adhesion molecules in type 2 (non-insulin dependent) diabetes mellitus are independent of glycaemic control molecular mechanisms underpinning microparticle-mediated cellular injury in cardiovascular complications associated with diabetes association between mean platelet volume in the pathogenesis of type 2 diabetes mellitus and diabetic macrovascular complications in japanese patients increased erythrocyte-and platelet-derived microvesicles in newly diagnosed type 2 diabetes mellitus type 2 diabetes and cardiovascular disease: have all risk factors the same strength? advanced glycation end products induce a prothrombotic phenotype in mice via interaction with platelet cd36 central role of the p2y12 receptor in platelet activation long non-coding rna metallothionein 1 pseudogene 3 promotes p2y12 expression by sponging mir-126 to activate platelet in diabetic animal model introduction to the human gut microbiota hyperglycemia drives intestinal barrier dysfunction and risk for enteric infection faecalibacterium prausnitzii-derived microbial anti-inflammatory molecule regulates intestinal integrity in diabetes mellitus mice via modulating tight junction protein expression considering gut microbiota in treatment of type 2 diabetes mellitus metformin effect on gut microbiota: insights for hiv-related inflammation the bacterium akkermansia muciniphila: a sentinel for gut permeability and its relevance to hiv-related inflammation high glucose decreases intracellular glutathione concentrations and upregulates inducible nitric oxide synthase gene expression in intestinal epithelial cells the role of iron in diabetes and its complications hyperglycemia promotes microvillus membrane expression of dmt1 in intestinal epithelial cells in a pkcalpha-dependent manner betacell deficit and increased beta-cell apoptosis in humans with type 2 diabetes fatty acid-induced lipotoxicity in pancreatic beta-cells during development of type 2 diabetes mesenchymal stem cell therapy in type 2 diabetes mellitus establishment of insulin-producing cells from human embryonic stem cells underhypoxic condition for cell based therapy human mesenchymal stem cell derived exosomes alleviate type 2 diabetes mellitus by reversing peripheral insulin resistance and relieving β-cell destruction a simple method for the generation of insulin producing cells from bone marrow mesenchymal stem cells secretagogin affects insulin secretion in pancreatic beta-cells by regulating actin dynamics and focal adhesion secretagogin regulates insulin signaling by direct insulin binding. iscience secretagogin is increased in plasma from type 2 diabetes patients and potentially reflects stress and islet dysfunction islet amyloid polypeptide, islet amyloid, and diabetes mellitus human iapp amyloidogenic properties and pancreatic betacell death extracellular vesicles from human pancreatic islets suppress human islet amyloid polypeptide amyloid formation functional proteasome complex is required for turnover of islet amyloid polypeptide in pancreatic beta-cells lipid accelerating the fibril of islet amyloid polypeptide aggravated the pancreatic islet injury in vitro and in vivo chronic methylglyoxal infusion by minipump causes pancreatic beta-cell dysfunction and induces type 2 diabetes in sprague-dawley rats proinflammatory and proapoptotic effects of methylglyoxal on neutrophils from patients with type 2 diabetes mellitus methylglyoxal impairs insulin secretion of pancreatic β-cells through increased production of ros and mitochondrial dysfunction mediated by upregulation of ucp2 and mapks evidence of beta-cell dedifferentiation in human type 2 diabetes direct effects of thyroid hormones on hepatic lipid metabolism prevalence and associated factors of non-alcoholic fatty liver disease in patients with type-2 diabetes mellitus microrna-206 prevents hepatosteatosis and hyperglycemia by facilitating insulin signaling and impairing lipogenesis evidence for p2y2 receptor facilitation of hyperglycemiainduced insulin resistance in human hepatocytes exosomal transfer of obesity adipose tissue for decreased mir-141-3p mediate insulin resistance of hepatocytes visfatin induces inflammation and insulin resistance via the nfκb and stat3 signaling pathways in hepatocytes hepatocyte growth factor alleviates hepatic insulin resistance and lipid accumulation in high-fat diet-fed mice pathogenesis of type 2 diabetes: tracing the reverse route from cure to cause transcriptional profiles of type 2 diabetes in human skeletal muscle reveal insulin resistance, metabolic defects, apoptosis, and molecular signatures of immune activation in response to infections intermuscular and perimuscular fat expansion in obesity correlates with skeletal muscle t cell and macrophage infiltration and insulin resistance altered myokine secretion is an intrinsic property of skeletal muscle in type 2 diabetes advanced glycation end products-induced insulin resistance involves repression of skeletal muscle glut4 expression chemotaxis of polymorphonuclear leukocytes from patients with diabetes mellitus impaired leucocyte functions in diabetic patients infections in patients with diabetes mellitus impaired immune responses in streptozotocin-induced type i diabetes in mice. involvement of high glucose infections in patients with diabetes mellitus: a review of pathogenesis differential effect of hyperglycaemia on the immune response in an experimental model of diabetes in balb/cbyj and c57bl/6j mice: participation of oxidative stress type 2 diabetes as an inflammatory disease pyrin and hematopoietic interferon-inducible nuclear protein domain proteins: innate immune sensors for cytosolic and nuclear dna glycemic reduction alters white blood cell counts and inflammatory gene expression in diabetes methylglyoxal disturbs the expression of antioxidant, apoptotic and glycation responsive genes and triggers programmed cell death in human leukocytes effect of high glucose on cytokine production by human peripheral blood immune cells and type i interferon signaling in monocytes: implications for the role of hyperglycemia in the diabetes inflammatory process and host defense against infection osteoclasts in bone regeneration under type 2 diabetes mellitus host susceptibility factors to bacterial infections in type 2 diabetes complement: a key system for immune surveillance and homeostasis high glucose disrupts oligosaccharide recognition function via competitive inhibition: a potential mechanism for immune dysregulation in diabetes mellitus decreased ficolin-3-mediated complement lectin pathway activation and alternative pathway amplification during bacterial infections in patients with type 2 diabetes mellitus oral candidal speciation, virulence and antifungal susceptibility in type 2 diabetes mellitus characterization of oral mucosa lesions and prevalence of yeasts in diabetic patients: a comparative study identification of c1q as a binding protein for advanced glycation end products glycation inactivation of the complement regulatory protein cd59: a possible role in the pathogenesis of the vascular complications of human diabetes complement activation in patients with diabetic nephropathy mechanisms regulating dendritic cell specification and development reduced frequency of peripheral plasmacytoid dendritic cells in type 1 diabetes reduced frequency of peripheral dendritic cells in type 2 diabetes circulating dendritic cell number and intracellular tnf-alpha production in women with type 2 diabetes high glucose and hyperglycemic sera from type 2 diabetic patients impair dc differentiation by inducing ros and activating wnt/β-catenin and p38 mapk ly-6chi monocytes dominate hypercholesterolemia-associated monocytosis and give rise to macrophages in atheromata macrophage apoptosis and necrotic core development in atherosclerosis: a rapidly advancing field with clinical relevance to imaging and therapy human gingiva-derived mesenchymal stem cells modulate monocytes/macrophages and alleviate atherosclerosis diabetesinduced alteration of f4/80+ macrophages: a study in mice with streptozotocin-induced diabetes for a long term the phenotype and functional alterations of macrophages in mice with hyperglycemia for long term defective production of interleukin-1 beta in patients with type 2 diabetes mellitus: restoration by proper glycemic control macrophage dysfunction impairs resolution of inflammation in the wounds of diabetic mice sustained inflammasome activity in macrophages impairs wound healing in type 2 diabetic humans and mice macrophage ppargamma and impaired wound healing in type 2 diabetes signaling between pancreatic beta cells and macrophages via s100 calciumbinding protein a8 exacerbates beta-cell apoptosis and islet inflammation resident macrophages mediate islet amyloid polypeptide-induced islet il-1beta production and beta-cell dysfunction apoptotic beta-cells induce macrophage reprogramming under diabetic conditions preliminary study on overproduction of reactive oxygen species by neutrophils in diabetes mellitus effects of insulin on methionine and homocysteine kinetics in type 2 diabetes with nephropathy diabetes primes neutrophils to undergo netosis, which impairs wound healing elevated homocysteine levels in type 2 diabetes induce constitutive neutrophil extracellular traps low levels of hydrogen sulfide in the blood of diabetes patients and streptozotocintreated rats causes vascular inflammation? antioxidant and cell-signaling functions of hydrogen sulfide in the central nervous system hydrogen sulfide primes diabetic wound to close through inhibition of netosis netosis delays diabetic wound healing in mice and humans hyperglycemia induces neutrophil extracellular traps formation through an nadph oxidasedependent pathway in diabetic retinopathy myeloperoxidase is associated with insulin resistance and inflammation in overweight subjects with first-degree relatives with type 2 diabetes mellitus leukocyte-derived myeloperoxidase amplifies high-glucose-induced endothelial dysfunction through interaction with high-glucose-stimulated, vascular non-leukocyte-derived reactive oxygen species neutrophil function and metabolism in individuals with diabetes mellitus obesity and type 2 diabetes mellitus induce lipopolysaccharide tolerance in rat neutrophils neutrophil-derived s100 calcium-binding proteins a8/a9 promote reticulated thrombocytosis and atherogenesis in diabetes neutrophil microparticle production and inflammasome activation by hyperglycemia due to cytoskeletal instability microparticles and type 2 diabetes microparticles as potential biomarkers of cardiovascular disease increased levels of soluble fas in serum from diabetic patients with neuropathy sfasl-mediated induction of neutrophil activation in patients with type 2 diabetes mellitus the dysfunction of nk cells in patients with type 2 diabetes and colon cancer nk cell count and glucotransporter 4 (glut4) expression in subjects with type 2 diabetes and colon cancer natural killer cell function, an important target for infection and tumor protection, is impaired in type 2 diabetes oxidative stress mediates a reduced expression of the activating receptor nkg2d in nk cells from end-stage renal disease patients diverse cytokine production by nkt cell subsets and identification of an il-17-producing cd4-nk1.1-nkt cell population aberrant nkg2d expression with il-17 production of cd4+ t subsets in patients with type 2 diabetes il-17 production by nkg2d-expressing cd56+ t cells in type 2 diabetes role of natural killer t (nkt) cells in type ii diabetes-induced vascular injuries the biology of innate lymphoid cells innate lymphoid cells-a proposal for uniform nomenclature type 1 innate lymphoid cells are associated with type 2 diabetes adipose group 1 innate lymphoid cells promote adipose tissue fibrosis and diabetes in obesity group 2 innate lymphoid cells participate in renal fibrosis in diabetic kidney disease partly via tgf-β1 signal pathway costimulation of type-2 innate lymphoid cells by gitr promotes effector function and ameliorates type 2 diabetes interleukin-33-activated islet-resident innate lymphoid cells promote insulin secretion through myeloid cell retinoic acid production evidence for an increased glycation of igg in diabetic patients glycation of monoclonal antibodies impairs their ability to bind antigen non-enzymatic glycation of igg: an in vivo study glycation of human igg induces structural alterations leading to changes in its interaction with anti-igg reactive immunization suppresses advanced glycation and mitigates diabetic nephropathy the immune response to influenza vaccination in diabetic patients humoral immune response and delayed type hypersensitivity to influenza vaccine in patients with diabetes mellitus cytotoxic t-cell response to influenza a subunit vaccine in patients with type 1 diabetes mellitus the antibody response to influenza vaccination is not impaired in type 2 diabetics a humoral immune defect distinguishes the response to staphylococcus aureus infections in mice with obesity and type 2 diabetes from that in mice with type 1 diabetes exacerbated staphylococcus aureus foot infections in obese/diabetic mice are associated with impaired germinal center reactions, ig class switching, and humoral immunity impaired function of antibodies to pneumococcal surface protein a but not to capsular polysaccharide in mexican american adults with type 2 diabetes mellitus islet amyloid polypeptide is not a target antigen for cd8+ t-cells in type 2 diabetes type 2 diabetes mellitus is associated with altered cd8(+) t and natural killer cell function in pulmonary tuberculosis impaired t-cell differentiation in diabetic foot ulceration individuals with obesity and type 2 diabetes have additional immune dysfunction compared with obese individuals who are metabolically healthy impaired cd4+ and t-helper 17 cell memory response to streptococcus pneumoniae is associated with elevated glucose and percent glycated hemoglobin a1c in mexican americans with type 2 diabetes mellitus protection against streptococcus pneumoniae serotype 1 acute infection shows a signature of th17-and ifn-gamma-mediated immunity regulatory t cells promote apelin-mediated sprouting angiogenesis in type 2 diabetes mitochondrial hyperpolarization: a checkpoint of t-cell life, death and autoimmunity genetic factors related to mitochondrial function and risk of diabetes mellitus the role of mitochondria in the pathogenesis of type 2 diabetes role and clinical significance of lymphocyte mitochondrial dysfunction in type 2 diabetes mellitus acute pyelonephritis in diabetes mellitus: single center experience vulvovaginal candidiasis and its related factors in diabetic women urinary tract infections in patients with type 2 diabetes mellitus: review of prevalence, diagnosis, and management hyperglycemia impairs neutrophil-mediated bacterial clearance in mice infected with the lyme disease pathogen insulin treatment directly restores neutrophil phagocytosis and bactericidal activity in diabetic mice and thereby improves surgical site staphylococcus aureus infection impaired phagocytosis of capsular serotypes k1 or k2 klebsiella pneumoniae in type 2 diabetes mellitus patients with poor glycemic control human polymorphonuclear neutrophil responses to burkholderia pseudomallei in healthy and diabetic subjects neutrophil extracellular traps exhibit antibacterial activity against burkholderia pseudomallei and are influenced by bacterial and host factors a critical role for neutrophils in resistance to experimental infection with burkholderia pseudomallei type-2 diabetes alters the basal phenotype of human macrophages and diminishes their capacity to respond, internalise, and control mycobacterium tuberculosis impaired recognition of mycobacterium tuberculosis by alveolar macrophages from diabetic mice il-22 produced by type 3 innate lymphoid cells (ilc3s) reduces the mortality of type 2 diabetes mellitus (t2dm) mice infected with mycobacterium tuberculosis diabetic complications and dysregulated innate immunity culture characterization of the skin microbiome in type 2 diabetes mellitus: a focus on the role of innate immunity complement evasion by borrelia burgdorferi: serumresistant strains promote c3b inactivation metformin reduces airway glucose permeability and hyperglycaemiainduced staphylococcus aureus load independently of effects on blood glucose impaired early cytokine responses at the site of infection in a murine model of type 2 diabetes and melioidosis comorbidity programmed death ligand 1 on burkholderia pseudomallei-infected human polymorphonuclear neutrophils impairs t cell functions diabetes alters immune response patterns to acute melioidosis in humans diabetes exacerbates infection via hyperinflammation by signaling through tlr4 and rage tb-diabetes co-morbidity in ghana: the importance of mycobacterium africanum infection diabetes and immunity to tuberculosis type 2 diabetes mellitus coincident with pulmonary tuberculosis is associated with heightened systemic type 1, type 17, and other proinflammatory cytokines glutathione deficiency in type 2 diabetes impairs cytokine responses and control of intracellular bacteria spectrum and prevalence of fungi infecting deep tissues of lowerlimb wounds in patients with type 2 diabetes common uropathogens and their antibiotic susceptibility pattern among diabetic patients helicobacter pylori infection is associated with type 2 diabetes, not type 1 diabetes: an updated meta-analysis kaposi's sarcoma associated herpesvirus seropositivity is associated with type 2 diabetes mellitus: a case-control study in xinjiang, china plasma glucose levels and diabetes are independent predictors for mortality and morbidity in patients with sars risk factors for primary middle east respiratory syndrome coronavirus illness in humans, saudi arabia prevalence of hepatitis c virus infection in type 2 diabetic patients at a tertiary care hospital prevalence and genotype distribution of hepatitis c virus infection among patients with type 2 diabetes mellitus prevalence of hepatitis b and hepatitis c among diabetes mellitus type 2 individuals impaired virus clearance, compromised immune response and increased mortality in type 2 diabetic mice infected with west nile virus seroprevalence and risk factors associated with hbv and hcv infection among subjects with type 2 diabetes from south india one health multiple challenges: the interspecies transmission of influenza a virus. one health influenza virus and glycemic variability in diabetes: a killer combination? front microbiol diabetes and the severity of pandemic influenza a (h1n1) infection mortality of 2009 pandemic influenza a (h1n1) in germany association of type 2 diabetes mellitus and seroprevalence for cytomegalovirus an association of herpes simplex virus type 1 infection with type 2 diabetes increased risk of herpes zoster in diabetic patients comorbid with coronary artery disease and microvascular disorders: a population-based study in taiwan human coronavirus: host-pathogen interaction middle east respiratory syndrome coronavirus infection mediated by the transmembrane serine protease tmprss2 the spike glycoprotein of the new coronavirus 2019-ncov contains a furinlike cleavage site absent in cov of the same clade sars-cov-2 cell entry depends on ace2 and tmprss2 and is blocked by a clinically proven protease inhibitor identification of a receptor-binding domain in the s protein of the novel human coronavirus middle east respiratory syndrome coronavirus as an essential target for vaccine development covid-19, coronavirus, sars-cov-2 and the small bowel covid-19 infection and mortality: a physiologist's perspective enlightening clinical features and plausible interventional strategies sars-cov-2 entry genes are most highly expressed in nasal goblet and ciliated cells within human airways receptor recognition by the novel coronavirus from wuhan: an analysis based on decadelong structural studies of sars coronavirus the proximal origin of sars-cov-2 elevated plasmin(ogen) as a common risk factor for covid-19 susceptibility ifn-γ/tnfα synergism as the final effector in autoimmune diabetes: a key role for stat1/ifn regulatory factor-1 pathway in pancreatic β cell death clinical characteristics of 28 patients with diabetes and covid-19 in wuhan, china covid-19 pandemic, coronaviruses, and diabetes mellitus diabetes in covid-19: prevalence, pathophysiology, prognosis and practical considerations diabetes is a risk factor for the progression and prognosis of covid-19 the trinity of covid-19: immunity, inflammation and intervention reduction and functional exhaustion of t cells in patients with coronavirus disease 2019 (covid-19) characteristics of peripheral lymphocyte subset alteration in covid-19 pneumonia type 2 diabetes mellitus and increased risk for malaria infection toxoplasma gondii infection in diabetes mellitus patients in china: seroprevalence, risk factors, and case-control studies association between helminth infections and diabetes mellitus in adults from the lao people's democratic republic: a cross-sectional study is there an association between positive strongyloides stercoralis serology and diabetes mellitus? intestinal parasitosis and associated factors among diabetic patients attending arba minch hospital, southern ethiopia intestinal parasitic infections in patients with diabetes mellitus: a case-control study intestinal parasitic infections among diabetes mellitus patients host-parasite interactions in individuals with type 1 and 2 diabetes result in higher frequency of ascaris lumbricoides and giardia lamblia in type 2 diabetic individuals type 2 diabetes mellitus balb/c mice are more susceptible to granulomatous amoebic encephalitis: immunohistochemical study the prevalence of oral candida infections in periodontitis patients with type 2 diabetes mellitus the authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.copyright © 2020 daryabor, atashzar, kabelitz, meri and kalantar. this is an open-access article distributed under the terms of the creative commons attribution license (cc by). the use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. no use, distribution or reproduction is permitted which does not comply with these terms. key: cord-326785-le2t1l8g authors: nan title: pathological society of great britain and ireland. 163rd meeting, 3–5 july 1991 date: 2005-06-15 journal: j pathol doi: 10.1002/path.1711640412 sha: doc_id: 326785 cord_uid: le2t1l8g nan claire m allen, d m hansell. mary n sheppard depanmenls of diagnosbc radrology and lung palhalogy royal bromplon nahonal hean and lung hosprlal, sydney slree:. london sw3 6np percutaneous fine needle biopsy 1s an established diagnostic technique for lung lesion^ afirm diagnosisofbenign versus malignant is often achieved but histological interpretation of small fragments or groups of cells is difficult manual cutting (twcut) needles provide asuperior histological specimen but are associated with a high complication rate and have been mainly used for pleural lesions this 1s the first prospective study to assess the feasibility of obtaining histological samplesfrom lung lesionswing apoweredcuning needle (biopty gun) we have biopsied 33 patients using biopty gun there were no major complications histological diagnoses were obtained in 30 patients (22 malignant, 8 benign) the malignant lesions identified included 7 nan-small cell carcinomas. 4 adenocarcmamas. 3 squamous cell carcinomas, 3 bronchiolaalveolar cell carcinomas, 2 8-cell lymphomas, 1 small cell carcinoma. 1 atypical camnoid and 1 metastatic breast carcmoma. the benign 1es1ons included 1 sarcoidosis. 1 clyptogenic organising pneumonia. 1 wegener's, 4 resolving pneumonias with chronic inflammation the rad~ologistls assessmentaftheamauntoftissueobtainedconelated withgood histology.01 thethreefalsenegativespecimens obtained the radtdogist noted the inadequacy of the samples ~n two cases and the third was a geographic miss percutaneous biopsy using the biopty gun is a simple and effective means of obtaining good quality histological material from lung parenchyma with a high degree of diagnostic accuracy for bath benign and malignant lesions inorganic particulate matter in "normal" lung: a study using light microscopy (lm), scanning electron microscopy (sem), and energy dispersive x-ray analysis (edxa) london, onlano. l2partmeni of palhology 375 soulh sireel london onlano n6a 4g5 canada h e possible association between inhaled inorganic matter and some cases of usual inter5tltial flbrosis (uipi has been of longstanding interest to pathologists and cllnoians. unfortunately. most analytical techniques are impracticable ~n the context of a pathology sewice laboratory in an anempt to find a practicable s01utm to this problem and to establish a baseline for inorganic particle load in a "normal" population, a study was undertaken using techniqueswhichwauld beavailable ~nmostlargepathologylaboratories ninecaseswereselectedfram the case(centra1andperipheralparliansaf lower. middleand upperlobesjandexamined with thesemand edxaand compared with the lm appearance to determine the panicle type and distrlbutm m a "normal" population. a wide range of inorganic matter was ldentlfied canespanding to siiicb. aluminium and magnesium s4cate5, rutile and alumina "like" particles varying from < 1 p to 15p in size in addition. trace elements including zinc. cadmium and increase in number of particles wasalso noted in areas of fibrosis which were present in two cases (old mflammatory disease) preseumably related to problems in particle clearance the findings of this pilot study suggest that although the sem and edxa will likely prove useful tools in the evaluation of lung biopsy soeclmens. the findinq of lnorqanic material in cases of uip must be interpreted with caution autopsy senicb whlch had no known expcsure to lnorganlc dust sectlons were taken from the nght lung each pulmonary adenomatosis has been described as adl~tinctive pathologlcal change seen in the lungsolexperimental area of replacement of normal alveolar lining cells by a taller more glandular type of eplthelwm. usually wlthwt significant cytological atypia. we describe 10 cases i" whlch a smtlar change was seen as an mdental fcndlng ~n resection specimensfor primary pulmonary adenocaranoma. the lesions (usually multlpleand each 5 mm orless m diameter) were identified in lung parenchymaat a distance from the tumour and consisted of thickened alveolar walls lined by prominent, distinctly atypical cells morphologically slmllar to type i 1 pneumacytes and cytologically different to the associated turnour reactive changes 8" lung involved by obstrmtive pneumonitis were not included !n thts sews all of the associated tumwra were peripheral adenocarcinamas and all showed a pattern of alveolar wall spread at the tumour periphery clinically 7 of the patients were female and all were smokers or ex-smokers the slgnlflcance of this lesion in the histogenesis of primary pulmonary ademcarcinoma is. as yet, unclear animals often i" assoclatlon wlth exposure to inhaled camnogens morphologically the lesion is a clrcumscrlbed departmen1 ofli~slopafhology sf richard's hosprlal. chrcheslei wesf sussex. po1 9 4se a series of 450consecutive personally conducted autopsies in patlenfsdying suddenly outside hospnal and where the death was reported to h m coroner 15 presented cot deaths were excluded. in 384 cases the death had been reported because theattendingdoctarwas unwillingtoissueadeathcertlficate. in theother66cases. deathwasnot duetonaturalcausesandfallowedsuicidearan accident oftheformetgroup, therewere t36unsuspected malor findings cn 11 8 patients (30.7%). that 1s to say findings which were either the cause of death or would have led to admission to hospital far assessment and possible treatment 1 they had been discovered in life the largest group were cardiovascular (56) but there were 22 cases of unsuspected malignant disease there were only five malor unsuspected findings in the group of unnatural deaths years). these results highlight the loss of teaching material in the coroner's system, at a time when hospnal postmortem rates are in universal decline. this matenal would be of value to medical students and to pathologists in traming. and largely comes from cases of lmle or no medico-legal significance. 7%) and these were in older sublects (mean age 71. a total of 140 postwnortem specimens refened to the royal victoria ho~pdal electron microscopy unit dunng the years 1984-1988 havebeen reviewed thkscompnsed3.4vo of thetotalnumber of sewre-relatedcaaesreferred to theunit.oulof 14ocasesreferred. 56wereexaminedandrecorded indetail theremainderdidnotundergoelectron microscopic examination for various reasons, such as a concius~ve diagnosis being reached by light microscopy alone. and semi-thin sections showing severe tissue mtoiysis. the most common tssues referred for examination were lung, kidney. liver, brain and head the range of e m. studies carried out included transmission electron microscopy item). scanning electron microscopy (semi and x-ray microanalysis on sem. theelectron micrographs wererevlewedwlth respect totlssuepresewatlanand th15wa5correlatedwlth the timeintervalbetweendeathand autopsy. electron microscopy was considered, an review. to have been diagnostically useful in 46% of cases an which it was deployed c s herringtan, a k graham, k cooper, j 0 0 mcgee it was shown prev10usiy that the discrimination of human papillamavirus (hpv) types 6 and 11 by nlsh in archival biopsy matenal requires dlfferent conditions from those predicted by conventional solufion kinetic analysis the parameter tm' (tissue tm) was defined in order to describe these differences in this study. these pnnciples were extended to the discrimination of hpv 16.31 and 33 in 15 casesol cln the results of nlsh analysis werecompared with both immunohistochemistry for viral capsid protein and pcr typing these data demonstrate that crosshybndisatm of high nsk viral types occurs ~n clinical lesions under conventional hybridisation and stnngency washmgcondit10ns thiscross hybridisation isnot due to thepresenceofviralcapsidproteinand 1sm0relikelyto be areflectionoftheendpoint usedinn1sh.i e thepresenceofvisiblesignal.practcally.multiplenlshsignalsduet0 closelyrelatedprobesinarchival materialarenot indicativeofmultiplehpvinfectionunlesstheyarepresent either ~n morphologically discrete areas of the biopsy or their presence has been confirmed by another molecular technique. motegenerally, thepresenceof asignal in nlsh usingaparticularprobedoes not implythattheidentity of the target nucleic acid is that of the probe medical students in the autopsy room shows that 29 0% thought faces should be covered during autopsy, and 12 4% thought that genitals should be covered. about half the group were indifferent to both proposals 35 9% thought the patient's identrty should be concealed from observers three students thought there should be no conversation at all. 24 0% thought that conversation should be limned to procedures and findings and 44 2% thought it should be limited to professional maners;conversely. 42 1% thought thereshwldbenolimitson thetopicsdiscwaed nearlyso% thoughtstudents should beencouragedtoassistbutnotpressuredintadoingsa.3.3% thoughtthatallshould becompelledtoassist, but 12 4% thought that students should onlv obsewe. and not be allowed to ass1s.t. 9 6% of students thought that they should oni!iobsene autopsies on patients they had clerked. whereas 13 4% thought they should onlfbe on autopsies on patients they had not clerked. fmally. 31 6% thought that relations should give spmfic perm1551on before students observed autopsies. whereas 45.4% thought not a quantitative study of the effects of fibroblast growth factor on wound strength and cellularity fibroblast growih factor (fgf) has potent angiogenic and fibrogenlc effects and is lmpllcated in the formatlon of granulation tissueand healing few attempts have been made toquantity theseeffectsmnvo. we havestudled arat skinwound modelusing red cellghostsasan fgfvehicle tensiometv ofthewoundsshowed amaxlmaleffectof the fgf after seven days when the wound strength was 50% above that m controls (p < 0 01) this effect had disappeared by fourteen days. computerized image analys~ using a joyce lo& mini magiscan measured total nuclear content of areas i" the wounds. permitting a topographic analysis of cellulanty versus distance from the wound centre cellularlty effects showed adifferent time course from wound strength. a 34% increase at fouldays anda42% decreaseat sevendays. relative tocontrols(bothp < 0.05) attwelvedaysthecellularityeffectwasstill sqnlflcant at a 31 vo decrease but by twenw-one days it had dwappeared the results suggest that fgf causes an early transient increase in cellulardy and more rapid increase in wound strength: most of these cells are macrophages and fibroblasts suggesting a connection between thesetwo obsenat10ns. the adhesion molecule$ 81 integrin (cd29). 82 integrin (cdl8). and intercellular adhesion molecule-1 (icam-1, cd54) are essential to the intimate co-operation of antigen presenting cells (apcs), t cells and keratinocytes cyclosponn. which is an effective treatment for psonas~s, may cause immunosuppression by altering antigen presentation we have pertormed a quantitative immunohistochemical assessment of the effect of low dose ~yclosporin on the expression of p1-integnn. p2-integnn and icam-f m the epidermis in chronic plaque psonas1s. staininglevels werecompared withclinicalresponseasassessed bythepsoriasisareaseverihllndex(pas1 score) pt-lntegnnand cam expressionon keratioocyteswerenotaltered bytherapy buttherewasasignificantdecrease inthemeanlevelsof p2positivelargedendriticcells(apc5)within theepidermis.bz-integnn wasnot expressed by keratinacytes there was a strong correlation between p2 expression and pas1 score after three months on cyclosporln and one month off therapy these results lndlcate that p2 stalnlng on large dendrltlc epidermal cells previous studies enumerating silver stained n~c l~l a r organiser regions in problematic cutaneous melanocytic lesions have yielded inconsistent. but generally favourable, resulis. it seems probable that such inconsistencies. arise largely from differences ~n fixation. staining and counting strategies. our group, having devised improved methods of agnor staining and counting. is now able to re-examine the potential role 01 agnors in borderline lesions pilot work demonstrated potentially significant differences in agnor dispersal between benign and malignant lesions and i" this study bath agnor numbers and dispersal patiems have been evaluated a range of melanocytic lesions including banal naev~. dysplastic naevi. typical melanomas, spiu naevi, atypical spih le~ions and minimal deviation melanomas were collected virtualty all of the unusual lesions had been diagnosed by specialists in dermatopathology. using a combined assessment of agnor numbers and dispersal, it proved possible to discriminate borderlip lesions from banal naevl and typical melanomas. benign borderline lesions -such as spit2 naevi ~ possess numerous nor$ but display tight clustenng in contrast to malignant melanomas wherenordispersa1 isaprominentfeature discriminatinganetypeaf borderlinelesionfromanathercauld not be achieved however, in practice this distinction is probably less important than assigning a aoirary specimen to a benign or malignant group a larger prospective trial of agnors in melanocytic lesions 6 currently in progress with a mean total exposure of 36 pack-years. alihough p53 was expressed more commonly in adenocarcinoma (30rof lo)andsquamouscarc~noma(28~~of29)than~nsmallcelltumours(l0%of2o),thiscouldbeaccountedfor by the smoking history. since patients with non-small cell carcinoma smoked more (a mean af 42 pack-yeas) than those with small cell lesions (mean of 33 pack-years). there was no relationship between p53 expression and sunlyal. s. a. sun. j. r. ~a s n e y depaitmenl ofpathology university of liverpol, p 0 box 147, l!vemooi. l69 3bx activation of thec-myconcqene with overexpression of itsancopratein product ocurs in bronchlal malignancles ofalltypes, but has beenmost extensivelystudied insmall celicarcmoma, wherensaverexpression~n culturedllnes has beenassociatedwithdevelopmentoffast-growingvanants whlchlosemuchofthelrendocrlnephenohlpeand aner their morphology. it has been suggested that these vanant lines might be the equlvalent of the large cell bronchial endocrine carcinomas sometimes seen i " yiyo, but this is not proven. we have used th0 myc 1 -9e10 monoclonal antibody and the avidin-biotin technique to study the panem of expression of the p62 oncoprotein product of the c-myc gene in turnour deposits of twelve subjects coming to necropsy with disseminated small cell carcinoma in an attempt to relate 11 l o morphological vanablity and metastatic site. anhough expression bore no relationship to morphological vanation. it ohen differed markedly horn site to slte. whereas parts of the primary t m w r strongly overexpressed the protein ~n all but one wbfect, there was considerable vanability between secondary deposits. oossiblv mdicatina arelation~hi~ between c-mycex~resslon and propensltvfor metastasls to certain iocations. tumour growth rate is a key parameter of neoplastic aggression. and is determined by the balance of cell gain and loss.apoptos~sisama]ormadeoftumourcellloss, but linleis knownof itsregulation. dieremesin turnourgrowth conferred by hpvtypes 16and 16 werestudied in aratfibroblast modelsystem. immortaiisedcells weretransfected with hpv 16 and 18 expression vectors. either alone or with activated c-ha-rasl. monoclonal cell lines were established. and their vector dna content was confirmed by pcr tumour cell 111185 ddfered in their growth properties m wvo and m vilro. hpv 18 containing turnours were larger and showed less apoptosis than those containing hpv 16, although bothshowed moreapoptasls than thenodulestormed bytheparentfibroblastsalone. in all turnours the presence of ras greatly reduced apoplosis and increased the growth rate. very similar propetlies wereobswvedin culture, and apoptoticratesshowed astranglnveneconelatlonwlthratesofnet cellgrowth. hpvs appeared iostim"latetumourcei1 apoptasis, butthiswas suppressed byras. melowerapaploslsassoclatedwilh hpv 16 compared with hpv 16 may partly explain the more aggressive phenotype of cervical c a n m containing hpv 16. it hasbecomeapparent thatanumberof maleculesmaybeexpressed byrestingorqu~escentcellsandarelostwith transition into the cell cycle. in addition to being of biological interest, such molecules may prove useful as operatcanal mahers of quiescent cell populations in histological material and allow the further characterisation of cellular subpopulations. one such molecule is statin. a 57kd protein previously reported to be expressed only by cells ~n go. we have shown bylaserconfocalfluarescence microscopythat thestatin antigen is associated with the nuclear envelope with a dstnbution 51m1l ar to that of nuclear lamins. using a monoclonal antibody (5-44) that recognises slatin we have defined the tissue distribution of statin immunoreactivlty in a range of continuously renewing, conditionaily renewing and non-renewing tissues. the distribution of immunoreactivlty 1s essentially as would be expected of a maher of quiescent ceils. in contrast. in established pancreatic carcinoma and other epithelial ceil lines. we have found $latin immunoreactivity ~n cycling cells using biotinylated k67 slatin double labelling techniques. in conciusion. statin lmmunoreactivitv in normal tissues correlates with auiescence but this realtionship is lost, at least in vifro. 10 loss of cell-cell and cell-substratum adhesion are imponantfactors during turnourprogression. tumour promoten are compounds which although not carcinogenic themsews increase the frequency of turnour development in animals previously exposed to carcinogens. we have used the turnour promoter tpa on cultured human renal epithelia ~ells10 mimic nwplastlc transformation. following tpa treatment we haveexamined thedistribution of vlnculin, b1 integrin and actin within thetreatedcells byfluorescencemicroscopy.treatment of therenal epithelium by tpacauses arounding up of the cells and a loss of adhesion toeither laminin or fibronecttn substrata fiuorescent microscopic examination reveals a progressive loss of reactivity for vinculin and b1 inlegrin within local conlacts. these changes are accompanied by a redistribution of the actin microfilaments from orientated bundles of stress fibres to a circumferential arrangement these changesofareduction in focal contact componentsand disarganised actin cytoskeietan mimic the changes we have previously described in renal carcinoma. glutathione s-transferases are a diverse group of enzymes with an important role !n the metabolism 01 faelgn compounds including some carcinogens and cancer chemotherapeutic agents. increased expression of gst pi is seen in manyanimal and humancancersandisassociated with resistancetocalboplatinandcisplatin in humanlung cancet cell iines. gsts are involved m steroid hormone transport and metabolism and have a role in the complex metabolic relationships between settoli ceils and germ cells. we have studied gst isoenzymne expression by an immunohistochemical method in 16 stage i teratomata. 16 stage i 1 tetatomata, 6 stage i seminoma, 11 cases of intratubulargerm cell neaplasia(1tgcn) and a groupof cryptorchid and normal testes. the stage i 1 teratomata had beentreated with cisplatin based therapyand bothprimmaryandpost-therapymetaftatictumourtissuewerestudied. gstalphaexpression correlated with morphological evidence of epithelial differentiation in teratomata.therewas no difference in gst expression between stage i and stage i 1 pnmary testicular iumours nor between primary testicularand post-therapy metastatic tumours. gstexpression did not correlate with survwal. gst pi was strongly expressed in the neoplastic germ cells of itgcn but was weak or negative in normal germ cells. this may be significant in view 01 the potential for later contralateral turnour development tn patients treated by cisplatin based therapy. in summary, gstexpression in testicular germ cell turnours reflectedlheirdifferentiationandappsared to be unrelated l o therapy and subsequent survival. a case illustrating the usefulness of electron-microscopic examination of fine needle aspirates 1s described fine needleaspiration wasperlormedon asubcutanwusnoduleinthechsstwall ofaneldedyman whowassuspmted tobesuffering from bronchogeniccaronomaanclinicaland radiologicalfindings.mesmears werenotdiagnan~c. but ~n view of the history af asbestos exposure, the needle washings were submined for eiectron-microscopic examination, which showed mesathelial differentiation and a diagnosis of metastatic malignant mesotheiioma was suggested. an autopsy perlormed eight months later confirmed the diagnosis of malignant mesotheboma. t. dorman, a ti ismail, b cunan, m. leader pathology department hoyal college of surgeons m ireland, dublln many histologi~allymalignantfeaturessuch as hypercellularltyand high mitoticcounts, but clinically followa benign course. demoid tumours and fibromafoses can be densely cellular but usually quite bland histologically and are associated wdh infiltrative marginsand repeated local recurrences. in addtion irradiated tissue often contains many cellswithcytologicalfeaturesol malignancy thisstudyexaminesthepioidyofsuch lesionsbyboth olthecunently availabletechniques using dlsaggregated formalin fixed paraffin embedded tissue sixteen cases 01 nf, 6 dfsts. 7 dts. 29fibromatoses(1nci~ding palmar, plantar. retrcpentonealand soh tissue) and 5 miscellaneouscases including 1 leiomyoblastoma, 1 inflammatory pseudosarcoma and plexiform histlocytama. one malignant fibrous histimytoma and t paragangliama were included as possible poslive controls. 10 cases containing numerous irradiation fibroblasts were alm analysed all 'pseudosarcwnas' were euploid by both image analysis and flow cytometry the malignant fibrous histiocytoma was aneuploid by image analysis and flow cytometry and the paragangliomawasaneuplaid by imageanalysis and tetraploid by flow cytometv themndwonsof thisstudv are that pseudosarcomas are euploid and aneuploidy would appear to be confined to malignant tumours of mesenchymal ongm. other sites we collected 32 cases to study their morphology and antigenic profile after staining for the epithelial markefficam5.2 flow molecularweight keratins)andlp34 (high molecular wefghtkeratins), thegeneralmelanoma and neural markers s1 w. neurone specific enoias8 (nse). protein gene product 9.5 (pgp) and the melanoma s w i f l c marker hmb 45, the neuroepithelia markers leu 7 and glial fibnllary acidic protein (gfap), and the intermediate ftlaments vimentln vim) and nsurofilament (nr the following turnour types emerged: i pure spindle celltype(n = 5),11,purepolyganalcelltumaun(n = 12)comp0sedofpleomorphiccells(n = 3).undwmcellswith an alveolar in = 3) or sheet arrangement (n = 6). and 111 mixed pleomorphic spindle and polygonal cell tumouffi (n = 13). two tumouffi proved to be lymphomas an intraepithelial melanocytic component could be established in 7 cases within adjacent respiratory or squamous melaplastic epithelium. in 2 cases n e w trunks a~mclated with tumour contained increased numbers of atypical schwann cells. consistently expressed were s1w (30130 and colon ovanan tumour antigen (cota). csais a heat stablemucin associated antigen present m normal colonic epithelial cells and is expressed m greater quantitites tn colon8c adenmarcinomas cota is a heat stable antigen present 8 n colanicneoplasiaand mumowwananturnours but not ~nnormalcalonicepithelium 5psmionsfrom to1 primary adenocarcinomas (30 ovanan, 20 colo-rectal, 9 gastric. 10 breast. 5 oesophageal. 10 prostatlc. 13 pancreattc, 3endometnal and t gallb1adder)and two adenmarcinomas metastatic tothe liverwere incubated with anti csa and anti cota antibodies using the p.a.p technique with positive and negative controls. while anti csa positivitywasseenin 19d20~0loni~aden0carcin0ma~(9wsakand lo~tr~"g).~twasalsaseen 1n20af30ovanan (13 weekand 7 strong). 6 of 9 gastric (3weakand 3 strong), 6 of 10 breast(5 weak and 1 strong). 5 of 5 oesophageal (4 weak and 1 strong). 5 of 10 prostatic (all weak). 11 of 13 pancreatic (9 weak and 7 strong). 3 of 3 endometnal (all weak) and the gallbladder ademcarcinoma. both liver metastatic adenocarcinomas were negative in additim while anti cota staining was positive m 16 of 20 colonic adenocarcinomas (6 weak and 10 strong) and 20 of 30 ovarian adenocarcinomas.~twasalsapositive~n5af 9gastnc(3weakandzstrong).3al lobreast(2weakand 1 stlmg), all 50esophageal(allweak)5of 10pr0~tati~(allweak), 11 0113pa"creatic(low8akand t strong),all3endometnal(all weak) and the case of gallbladder endocarcinoma (strons) both liver metastatic adenocarcinomas were negative. m e c o~c~u s~o~ of this study 1s that anti csa and anti cota are not adequately specific in the identification of a ~olonlc or ovarian origin af an adenocarcinoma and cannot reliably be applied to the identification of a metastatic adenocarcinoma of unknown primary site the early intfa-epithelial changes of adenocarcinoma of the nose and paranasal sinuses were sought in the histological sections from 30 high grade adenocarcinomas and 4 cyclindric cell carcinomas from this region none of which had had previous radiotherapy treatment. 7 of the cases came from wwd-workers. 1 i r m a polishw and 1 from a plasterer attention was directed to the non-neoplastic epithellm of the surface and of the sera-muclnous glands. in 14 casesofadenocarcinomaand t of cylindriccell carcinoma surfacechaogeswere detected these took the form of hyperplasm of goblet cells of the rsspiratq epithelwm accompanied by dysplastic changes of other epithelial cdls: m the latter these became enlarged and irregular m shape with large hyperchromatic nude and prominent nucleoli. lnthsmajorityof iesionsthesechangeswereisolatedin theepithelium. changesof thesetypes were never seen in sefomucinous gland epithelium. in addition similar changes were not noted m the coverlng respiratoryepithelium in 50casesofnasal polyps evenwhen severely inflamed thesemsmchangesso described haematoporphynn derivative sensitised tumwr tissue. 1s underwing evaluaton 4" widesptead and m i s t a n t papillary tumoursand ,n casesof rvldespreadseveredysplasra/carnnoma,nufu". arewewof spallents (21,7m, ages 4 6 8 0 years. pre-and post therapy) has revealed no change ~n histological grade and stage ~n 7 patients, progression to invasion in t case and a redunion to mild urothellal atypla alone in 1 case. local tissue changes following treatment were limnedto oedema and an acute lntlammatoryreactlon. no metaplastlc. stromalfibroblast or nene changes were seen variations ~n bladdw size. both increased and dlmtnlshed, wwe encountered the histological grading of tcc following pot shows little improvement. but studies are in progress to improve lhght delivery in the bladder, and hence improve treatment outcome. a armour. a. s. jack bpartment of pathology, umverslty of i d s . leeds. lsz 9jt follicular lymphoma is a disease characterised by widespread lymph node involvement usually at the time of presentation proper tie^ of lymphocyte homing and circulation appear to be mediated by a variety of cell adhesion molecules. the a m of this study was to compare mrmal nodal lymphocytes with the neoplastic populatlm m folllcularlymphoma. hall casesalloftheneaplasticfolliclesexpressed lcaml but thisyanedfromonlyafewcellsto 70% of cells within a follicle this dosltlvlty included dendmic retic~l~rn cells. germinal centre cells and neoplastic lymphocytes. leu 6 (lymphocyte homing receptor) showed an inverse pattern of expression in all but 3 cases the phenotype (icaml + l a 87 is a feature of germinal centres and scanwed paracontcal blasts in reaclive nodes anhough there is uniformity of expression of lcaml in germinal centres which is not apparent in any folllcular lyumphoma case. this study showed a loss of lcamt and increased leu 8 expression by neoplastic lymphocytes within follicles this may relate to the propensity of this disease to spread widely throughout the lymphatic system activation leads to an alteredfunction and aconcomitant aneration in the chemistry ofthe cell surface, which ~s a site nchincalbohydrate. rat lymph nodelymphacytes.eitherunactivatedoraclivatedfot5days1namixedlymphocyte reanlon. were treated with biotinylated iectins from a large panel. chosen to probe surface glycans lmlns were revealed with awdln-phycoerythnn and cell populations were analysed in a fluorescence activated cell-sorter double-stalnlng with fitc-monoclonal antlbodles defined the functional lymphocyte subsets. uea-1 and lta boundtonoce11sof anytype. unactivatedb-cells boundall theremaininglectins.savempa. toagreaterextentthan did unactlvatedt-cellsand b-cell actlvatlon produced no change i" glycan sxpresslon. unactlvated and actlvatedtcells all expressed a2.6-linked sialyl residues, but o-2.3-linked sialyl expression was hetrogeneous, did not conespond toanysubsets,and wa~unchangedonanlvatian.alargegroupof lectinsshowedlow wno binding to unactlvatedt-cells, but boundonactivatianexactly in parallel to1l-2 receptorexpressionctacantigen) thes~ngle structure gawgalnacal,3galpl,4glcnac-) galigalnacat ,3gal~1,4glcnac-) r could account for their binding the presence of neoplastic (light chain restricted) b cell follicles in low grade b c d gastrolntestlnal (gi) mmphomaof although malt 1s not present in normal human gastric mucosa, lymphold t,ssue ,* acqulr& ,n response lo colonisationof themucosa by helrcob~cleipyioii. we have investigated the possibility that thisacquiied lymphoid t1ssue is 01 malt type whlch may povovlde the background i" which lymphoma can arl~e w e examined gast,,c b~0p5~e5fr0m450casesafh~l~~~bacrerassaciatedgastntis.and biopsyandresectionspecimensfram60casesaf t"mours has contr'buted to a peklstence of ihe more "iew arefofl'cle (fee) gastrlc 8 cell lymphomaof malt in 175 cases of hebcobaciergastritis prominent lymphoid follicles were idenfilled in 8aftheee b cell clusters were identified within the gastric epithelium. reminiscent oltheteatures seen 10 the dome epithelium of sm11811 intestinal peyer'z patch. thls b cell-eplthelh assoclatlon was not assaclated with the eplthelm cell changes or the glandular destructm seen ~n lymphoeplthellal i~s i o~s 01 malt lymphomas. in 54/60 cases of gastric maltlymphoma helicobaclercould be identified oltheremaining6cases.5 weiegastrecfamy specimens 8n which specimen washing may have contributed to the negativefindings. we suggest that gastrlc malt 1s acqulred in response to local immunological stimulation as a result of mucosal colonisation by hel~cobaclerpylon, and that the development of malt lymphoma is a subsequent event mucosa associated hmphold tlssue (malti has been explained on the bas15 of speclftc colonization at reactlve b lymphomasbe included in lhecatqoryof malt lymphoma but the frequent presenceotafoll~culapanem in these foltic1es by ihe neaplastlc cantrocyte-like(ccl) it has been low grade cellthyro1d we have ihe and 'nvesflgated the and genotype of' of primary low gradebcelllymphomasofthethyro'd alsodemonstratedfeatures ofmalt1ymphama'ncludtng cclce115and l y m p h~' t h~' a l l~' o n s . m e appearances and immunoh'sto'og~ofthefo'l'c'es werethoseofto'l'cularcalon'rat'on described 'ngimaltmmphomarather thanfccfoll'cular'~mphoma thepredomlnant iwg1 ~ane'naffoll~cularcolon~rat~~nconformed tothatdeslgnated cclcells show'ng astnk'ngly h'gh prol'feratton late no evidence of the '(14 ' ' 1 transiocat'an was found in any on dna extracted from fresh (n = 1) or paraffln embedded (n = 9) t15sue mese ilndlngs argue against a fcc lineage lor primary thyroid lymphomas and support their 1ncius1on 8" the maltcategory we have used a panel of antibode$ to demonstrate stages of granulocyte maturation by immunoh~st0chemistry i" decalcified. wax-embedded bane marrow trephine biopsies antibodies reactive with muramidase. u-1 -ant~tryps,n. neutraphil elaslase and cd68 react with early granulocyte precursors. cd15 and calgranulin identity later granulocytes. ihdiylduai antibodies dlfier rn the populations 01 cells ldentlfled theantlbcdtes also react with cells of mwlocyte llneageand provide information concerning theorganlsatlon afmonopolesls about whlch liffle is known in normal marrow granulopoiesis is zonal wlth maturation occurring radially around trabeculae and blood vessels this pattern is exaggerate3 in reactive hyperplasia and chronic granulocytic leukaemia (cgl) there is marked disruption of this zonal organisation in myeloproliferative and myelodysplastic states, with considerable overlap 01 patterns between these conditions in chronic mvelomonacvtic leukaemia (cmml) there is comdlete absence of zonal arrangement of granulopaiesis possibly due to monocytic proliferation obscuring the underlying marrow spaces and that by analogy with cgl cmml represents an exaggeration of this normal panern granulopoletlc panern we hypotheslse that monopoles15 normally occurs 8" a randomly dispersed fashion within as previously shown by us in animals untreated with cyclosparin a. the cell birth rate fell from an initial prelmmunisation valueof 32 cellsit 000cellsihour to 18 cells11 000 celldhouran day 2 followed by a rise1044 cellsit 000 cellslhour on day 4 however, in cyclosporin a treated animals the cell birth rate (1 7 5 ce11s/looo cells/hour) was signiticantlydepressed belowthecontrol pre-immunisation levelandremained suppressedupfaday4fallowed by an abrupt rise these results are consisten1 with the hypothesis that t lymphocytes or their pmducts not only drwe the morphological appearancescompnsed lymphoepithelia lesions (in onecase). numerous lymphoid follicles and a diffuse infiltrate of monocytoid cells (centrocyte like cells) there was striking plasma cell differentiation and colonisation of lymphad folllcks by monacytoid cell?. and neoplastic plasma cells. lmmunahistochemistry convincingly demonstrated heavy and light chain restriction ~n all the biopsies from both the cases the bladder 1s developmentally related to the hind gut and this manifests 8" the variety of metaplastic epithelium seen at this site circulating cells. encauntenng the endothelial surface. make contacts 10 an environment rich 8 n glycan. a large panel of biotinylated lectins was used to probe far variations in the glycans expressed on endathelia of artenes. veins, arterioles, venules. capillanes, high endothelia vessels and lymphatics m a range of normal and pathological human tissues formalin-fixed, paraffln embedded specimens from the files of manchester royal infirmary and manchester royal eye hospital were used lectins were revealed with an avidin-peraxidasesystem no differences werefound between arterial. arteriolar, venular, veinous or lymphatic endothelia all expressed abundant complex-type n-linked glycans. of several subtypes. capillaries were highly variable and showed heterogeneity ~n their expression of 1) outer chain sequences fn n-linked glycansand 2) mucin-type sequences. both between different. normal organs and within an organ. implying that the surrounding tissue probably had a regulatory effect where endothelium was reactive, additional aneratiom wete seen and actively growmg endothelium in granulation tissue expressed hqhmannose siwctwes. high endolhelial ybss~is showed a much lower density and narrower range of glycan expression thandidad~acenlnormalcapillanes,despite theirknownvery highrateofglycansynthesisand secretion the iymphocyteiln-homing receplor(s) would be a component of this restricted porlfolio of glycan monocyte margination in atherosclerosis associated with immunological injury n. j. combs, p j gallagher. p. s bass clinical and experimental evidence indicates that immunological injury is associated with accelerated atherosclerosis. allograft recipients may develop accelerated atheroscleross and anlmalsgwen serum sickness and a high fat diet develop more extensive atherosclerosis than controls fed the diet alone we have tested the hypothesis that atherosclerosis ~n these animals is associated with increased adhesion of monocytes to the aortic endothelium. chronicswum sickness was induced in genetically hyperlipidaemic rabbits with nativeanionic bovine serum albumin (nbsa) or highly cationised protein (cbsa) rabbits given nbsa showed a spectrum of glomerular endocapillary prollferativechange thasegiven cbsa developed early membranous glomerulopathy in controls the numberofmanocytesadherent to theendothelium ranged from 37y5isq mm and m animals given senm sickness 15-305isq mm (nbsa)or14~5isqmm(cbsa) as therewerenosignificant intergroupdifferences theseiesultsdo not support the hypothesis that immunological injury increases monocyte adhesion to the aortic endothelium departmen! oipatholcgy, souihampfon universily hospdals soufhamplon. so9 4xy amyloidcan beidentified 1nupta20% of elderty hearts,especiallyin themyocardium oftheatrialappendages in a small prapanionofth%lecasesamylaid~salsapresent inthecardiacvalve~ butisolatedvalvulardepos,tsarerare. a 73 year old male presented with bilateral leg weakness and an intradural turnour. he died 3 days after spinal surgeryanddeposltsofaglloblaslomamunlforme wereldentlfledm both thecerebrumand thecord therewasno hlstory of cardiac disease but all four valves showed translucent verrucous thrkenlngs. these had a uniform eosnophilc hi~lologicalappearance. stainedwithcongo red and had ultrastnucturalfeatures of amyloid amyloid p proteinwas identified immunohistochemically ~n thesedeposits but negative multswere obtained withantibodies t o m . aland a4 proteins. mwewas no evidenceof cerebrovascular ormyocardial amyloidosis the involvementof all four cardiac valves. the stnking absence of amyloid i" other organs and the a~~o~l a t i o n with a widespread glioblastoma are unusuai but unexplained features of this case the ima 1s used as a bypass of narrowed coronary arteries it is said to be less prone than vein gratk to develop subsequent occlusivedisease. thisstudy of pairs of imasfrom subjects of vario~s ageswas to see if the histological structure ofthevessel might explain immunityto graft disease sixteen imas were fixed in distension byformalln at 150 cm of water pressure and secllon~ taken at the level of each nb (first to stxth). all arteries undelwent similar changes along thelr length. wlth no slgniflcant difference between left and rlght lntimal changes were minor conssting of lbro-elastic muscular thickening in all age groups and in those who had died from vascular disease theinternalelastic lamellawaswelldefinedat all levels. buttheexternallamellawasclearlydefinedonlyatthelevel ofthefmhandslxthnbs(i.e. mthedetalartwyj. medral thrckne~~decreasedalongthelengthofthearter~esandinall cases changes from an elastic to a muscular structure, generally at the level of the fourth or fiflh rib the ratio of medial thickness to numbw of lmdlae in~reases along the artery. notably at its point of change muscle fibre orientation changes from inter-mixed cir~ular and longitudinal in the elastic part to predominantly circumferential in the muscular pan. the pronounced stnctural differences of the ima compared to the similar sired epicardia coronary arteries. which are muscular. may be of relevance in explaining their markedly different incidence of atheroma. naomi carter, s variend fatty change of the heart is a pwrly defined pathological entity which in the adult hean can be caused by severe hypoxia nutritional disorders. poisoning by selected drugs and catecholaminerelease it is most commonly seen ~n association with coronary artery disease little data exists with regard to the paediatric hean in 980 pediatric deaths coming to post mortem over a 10 year period. there were 66 cases of myocardial fatty change of varying seventy and distribution detected ~n 0 1 1 red 0-stained sections infection and congenital disordenwereimplicated 1n39deaths infectionand cangenitaldisordenwereimplicated 1n39deaths. 5910fallcasesoffarmchangeand 2 2% of all deaths seven ofthe5e~ases had acombined ~nfecti~u~andcangennalaetiology othercausesofdeath included turnour, traumaandcomplicationsofbinh 3 6% of casesofsudden infant dealhsyndrome(s1ds) hada fatty heart only one case of the total 66 cases showed deflnlte hlstaloglcal evldence of ischaemic myocardial damage. insome instances, thedegreeaffattychangemayberelatedtathedurationand seventyoftheundertyng condition someofthesechildren may havean occunnutritional orenlymedisarderwhich ~sexpressedatacellular level ~n the form o! fatty change and that contibutes to their early death. we havecampared thereparting oftemporalarterybiopsiesbetween 1973-78(135cases)and 198691 (91 cases). the overall incidence of positive biopsies was 24.5% and 26.5% in each period the number of patients with clear clinical evidence of cranial arteritis was 42% but in 1973-78, 58% and in 198691, 66% of these had positive temporal artery biopsies when the histology was reviewed approximately 6% of biopsies in each period had been erroneou~ly reported as healed or atypical artentis. in contrast. a true histological diagnosis of artetitis was missed in~nlya~inglepatient approximately 18% ofall patientswithaclinicaldiagnosisof giant cellarteritisdevelopedan additional symptom or pathological change associated with steroid treatment frequent final clinical diagnoses in patients with negative temporal artery biopsies were transient ischaemic attacks, cerebrovascular accidents. unexplained headache or migraine. polyarteritis or polymyalgia hwmatica these resuns confirm that one third of patients with deflnite clinical evidence of cranial arteritis will have negative biopsies pathologists continue to misinterpret normal arterial ageing changes as evidence of healed or atypical arteritis depanmenf 01 hslopafhology and depanmen! 01 resp8raioiy medicne. sl banholomew s hospifal london ecla /be adhesion ~fepithelium to extracellularmatrices is mediated partly byafamily of heterodimeric molecules known as megrins we haveexamined theexpressionofthealpha-1 toalpha-6integnn subunits in~unured human branchia epithelial cells. and in bronchial biops8es from normal subjects and atopic asthamtics. we have also studied the expression of intercellular adhesion molecule-t (icam-1, cd54, rhinovirus receptor) br~nchialepithelia cells from surgical specimens were grown as explant cultures on glass covenlips. bronchial biopsies were taken from right upper and middle lobe carinas lmmunastaining was performed on acetone fixed cells and frozen tissue sections using alkaline phosphatase and immunoperoxidase techniques all biopsies showed strong positive staining of epithelium for alphe?, alpha~3 and alpha-6 integnns. stainingforalpha-5 was weak or negativeand epithelium was negative foralpha-1 and alpha-4 except in twoasthmaticswhere itwas weakhi alpha-4 posittve. in contrast. cultured bronchial epithelial cellswere positive for all these mtegrinsexcept alpha-1. epithelium was positive for cam-1 in 91 17 asthmatics but negative 10 all other biopsies. cultured cells were ~trongly positive for this molecule it 85 concluded that expression of some adhesion molecules bv bronchial emhelium may vaw ~n relation to the cellular environment and that ths may be imponant tn disease l%panmen! of pafhology univeisrty of birmingham and departmenrs o! 'immunology and 3his!opalho!ogy eas! blood eosinophils are in a relatively inactive state with migration into tissues eosinophils became more activated these activated cells are hypodense compared to most blood eosnoph11s low affinity receptors for both ige (fcerii. cd231 and igg (fcgriii. cd16) have been documented on activated. hypodense eosinophils this study assessed the expression of these proteins on ttssue eosmophk derived from nasal wlyps the blood and nasal polyps of seven patients undergoing nasal polypectomy were studied nornodense and hypodense eosinophils were isolated from venous blood by centrifugation an a discontinuous percoll gradient percoll wassimilarly used to obtainaneosinophilrichpreparationfromcellsearactedoutafthenasalpolyps cytospin preparationswetem?.de of these samples frozen sections of each polyp were also prepared lmmunostaining using an alkaline phosphataseianti-alkalln phosphatase detection system demonstrated that neither blood nor nasal polyp eosinophilsexpressed detectablecd23orcdt6 l t i~p~~~i b l e t h a t e~~i n~p h l l s o f na~alp~lyp~aresimilarto blood eosinophils and are in a relatively inactive state lavage and biopsy studies. the relationships between mucosal inflammation. bronchospasm and bronchial hyperreactivity are unclear since bronchial smwth muscle has an essential rolein the pathophydogyof asthma. we haveexamined theextentto which it ~sin~ol~ed~nallergicinflammation bi0p~ie~in~l~ding~moothmu5clefr0m 10 asthmatics (age range 19371 who did not use steroids and 4 controls (age range 2243) were embedded i" araldite and stainedformast cells ~monocional ant1bodyaat)and eosinophils(monoclona1 antibody eg2). mast cell numben in the lamina propria and smooth muscle were similar for both asthmatic and control sub e m (mean values. astham lamina propna 70 81mm2. smooth muscle 72 timm2, controls 87 5/mm2 and 43 blmm'respectively) eosinophil numbers in the lamina propria were increased 10-fold in the asthmatics (p = 0 008) but there was no significant increase in the number of eosinaphils rn the bronchial smooth muscle eosinophil numbers in the asthmatics correlated positively with fev, we conclude that the role of muco~al inflammation in the pathophysiology of asthma has yet to be determined we present5 cases ofextra-pulmonary pneumocystosis diagnosed on routinesurgical specimens (two biopsiesof liver. and one each of gastric mucosa. small intestine and a pen-anal mass). in each case. the histological features were similar to those seen in the lung. and as in other material from cases of aids, munlple pathology was often found extra-pulmonaly pneumocystasis 1s now being reported from a widerangeof clinical specialties. one reason forthismcreasemaybe that impraved patient suiyiy~i with"topicay inhalatiooalpentamidinetherapyallowsvisceral foci of infection to become clinically apparent this hypothesis is supported by the finding that 4 ofour5cases were taking nebulised pentamidme inthesehypersensltivitystatestothatobselved mbronchiectasis (a chronic suppurative lung condition not thought to in~olve a hypersensitivity aetiology) and in smokers and non-smokers with no evidence of active pulmonary inflammation ourresuns havesh0wnthattheb:tlymphocyteratioisnodifferent ineaaandsarcoidfromthat seen ~n bronchiectasis and in normal lungs. we believe that thns is further evidence to suggest that bal is an unrepiesentativetechnlquetorlhestudyof interstitial lung diseasesand that morecansiderationshould begivento the possibility of humoral immune components in the pathogenesis of ea4 determine its effects upon the number of pulmonary neuroendocrine cells and their peptides. in one experiment. the concentration of noradrenaline in the lung was estimated by chromatography, and that of the peptides bombesm. neurotensin and caknonin gene-related peptide (cgrp) by radiaimmunoassay. there was significantly ies5 noradrenaline and bornbesin in the lungs of test rats than in controls but the levels of neurotensin and cgrp were unchanged. in a second experiment, pulmonary neuroendocrlne cells in histological sections were labelled with antiserato bombesin,calc,t~tonin,cgrp andproteingenepmduct9 5[pgp 9 s ) a~d =~" " t~d . t h~, e w =~ nochange in the number of labelled neuroendocrine cells expressed per unit area of lung or per unit length of airway between test and control rats for calcitonln. cgrp or pgp 9.5. bornbesin-containing cells could not be identified in either group. an increase ~n pulmonary neuroendocrine cells could not be identified ~n either group. an increase in pulmonary neuroendacrine cells immunoreactive for bomtesin and calcitonin occu~s in the early stages of plexogenicpulmonaryartertopathy in man. theabsence ofsucha change in monocrotallnedulmonanhydertenslon in the rat suggests that this is a poor model for the human disease. this preliminary study was carried out to assess the quantitative expression of neuroendocrine and mast cells in adun humanlungsofcasesofasbestos-relateddisease.tencaseseachofasbestasis, pleuralplaques,carcinoma and mesothelioma were studied m comparison with ten normals wnh no history 01 exposure to asbestos the lung sections were stained lor neuroendocrine markers neurone specific enolase (nso and chromagranln. and, chloroacstate esterase and toluidine blue for mast cells. there was a notable variation in the number of neuroendocrine and mast cells between the control and asbestos-related disease group the variation was also seen between the various asbestos-related diseases. though not statistically sbgnificant. the trend of the vanatton indicated that the individual diseases follow a particular pattern a n lhe expresston of these two cell popuipioiis. we have studied fibrous turnours of the pleura using morphology. immunohistwhemislry and eleclronmaroscopy. the findings were compared and contrasted with reactive pleural fibrosis and desmoplastlc mesothelioma. the fibroustumwn hadarangeof histologicalappearancesand30% weremalignant ~nnature.theimmunophemtype was uniform and consistent with positive staining for vimentin and alpha m w t h muscle actin. this was ~n sharp contrast to findings ~n reactive pleural fibrosis and desmoplastic mesothelioma. uttrastructural appearances of the fibrous tumours of the pleura were supportive of a myofibroblastic ongin. we propose that fibrous tumours of the pleura arise from the submesothelial myofibroblast. the malignant fibrous turnours have a distinct immunohistochemical profile and electron microscopic features to differentiate l from themalignant mesenchymai mesothelioma. a study was undenaken to evaluate the use of immunaperoxidase stains on paraffin embedded tissue lo define the cell type in routine lung cancer preparations. and in particular to identdy a subgroup of turnours showing neuroendocrinedifferentiation. forty lour consecutivethoracotamycaseswere selected. following apilot study of 6 cases. to assess digestion times and potentiaily useful antibodies, the remaining cases were processed using a battery of monoclonal antibodies: cytokeratr iaelfae3, 348e12). neuron specitic enolase (nse), chromogranin. and beta 2 microglobulm. in addition to the 3 carcinoid turnours and 1 oat cell carcinoma in the study 3 large cell carcinomas and 5 adenmarcinomas demonstrated positive neuroendocrine markers. uiirastnrcturally, dense core granules could be demonstrated in only 2/3 of the large cell carcinomas and in 1/5 adenocarcmomas. the discrepancy between the lmmunoperoxldase staining and electron microscopic features likely reflects the heterogeneityafthese turnours. in thisstudy noneof the turnours co-expressed neuroendocrine markersand beta 2 microglabulm. however, the staining panern was inconsistent m the remaining cases high molecular weight cytokeratin (34pe12) was stronglyposltlve m all casesot squamouscell carcinoma and negativein everyihing else. in summary. monoclonal nse and chromogranin appeared to provide sufficient information to identity neuroendocrinedifterentiatian in thecasesexamined m this study. high molecularweight cytokeratinwasfound to bea usefuldiscriminaforforsquamouscelicarcinoma. beta2 microglobulin was negativemall the turnoursshowing neuroendocrine differentiation. butthe inconsistency of staining m non neuroendocrinetumaurs. made it less helpful for routine laboratory use although endocrine differentiation is the essence of small cell carcinoma of the bronchus, its occurrence m other morphological ("on-small cell) types of bronchial 1umour (large cell, squamous and adenmarcdnoma) is welldescribed however, its prevalence m such tumours is uncertam, estimates differing from study to rudy and accordingto how it is sought. we have examined, byimmunalabellmg, expression offiveendocrine markerproteins (neuron-specific enolase (nso, protein gene product [pgp) 9.5, the bb isoenzyme of creatine kinase [ck-bb), synaptophysinands-t 00protein)m60 bronchoscopictissue biopsiesof "on-smallcellcarcinomaandasse~ns varlabiltty within and between tumour deposits in 16 subjects coming to necropsy with disseminated disease exactly half of the tissue biopsy specimens immunolabelled for one or more marken; one for four, four for three, twenty lor two and five for one. possibly indicating an element of endocrine dtflerentiation inapparent from their morphology. expression was even more prevalent amongst the extensively-sampled turnours at necropsy, but since theinlraductionofthenewgeneralpractnianercontractmapril 1990,lhere hasbeenasignlicant increasein thenurnbeisof skin biopsiesreceivedmhistopathologydepa~ments in ourdepartment there has beenalhreefold increase in numbers of general practiioner skin biopsies. the aims of this study were to crnlcally appraise these biopsiesand comparethem tosimilarlysized skin biapsiesreceivedfrom hospital in-patientsviageneraland plastic surgeons for the six months prior to and aner 1st april 1990. data collected included numbers received, ranae of pathological diagnoses, quality 07 information supplied on the request card, accuracy 01 clinical diagnoses. adequacy of excision, age. sex and sites of lesions the resuns showed a similar range of pathological diagnoses. the quality of clinical information supplied was comparable in the two groups as was the age and sex of patients. general practitioner biopsies were less common from the face. clinical recognition of lesions was somewhat less accurate amongst general practitioners than amongst hospital surgeons inadequate excision was more common m general practnioner cases. 5.5% of general practitioner lesions were found unexpectedly to be premalignant or malignant (eight cases) and all ofthesewere inadequatelyexclsed. important implicationsemergingfromthisstudy are dlscussed an audit of skin biopsy specimens from general practitioners in grampian region: changes in requesting practice and specimen type assessmen1 ofresaction marginsofsurgicalspecimens~s becming more important m manyfieldsofpathology. we wwe interested in developing a means of assessing surgical margins 10 dermatopatholqy in both conventionally removed skin ellipses and m skin ellipses removed during m o~s chemasurgery technique many of the conventionally used markers, such as indian ink, alcian blue and tipp-ex correction fluid are difficult to use i" that they are messytoapply. slow todry and show insufficient contrast wiih oneanother both lnthegrass specimen and microscopically weused"superman'paint,apaintusedforresinandplastermodels,wh,chcomesin awlderange of colours. the paint was easyto apply. did not run and dried qwckiy becauseof the variety of colours avaciablewe were able to apply contrasting c~l o u n to the vertical and horizontal axes of b x c~s i o~ af skm elhpses removed by mohschemosurgery.thepaint proyidedagaodmarkergrasslyand wasnot affected byfreezinqthetissue model paint provides another marker lor surgical bxcij~ii margins and 1s particularly useful for moh's chemasurgery where horizontal and vertical axes aremarked inorderto assess theadequacyoftheexcision.the model paint may also be usetul in other branches of surgical pathology where resection margins are important. in psoriasis there is altered bpidermal dmwentiattan and increased epidermal turnover both 01 which involve changesin intercellularadhesion aquantnative imm~noh~st0chernicaicompa~~sonof the expression of the integrin staining of integrin p subunlts 1-4 and e subunlts 1 4 were disclosed usmg an andin-blatln peraxidase techn!que. large epidermal dendritic cells (antigen presenting cells) expressed p-2 the psoriatic skm.showed increased 6-1 a-3.0-6. and p-2expression. buta-2and~-4showednosignificantdifferencefromnormal thelncreasedlntegrin expression by keratinocytes seems to be a reflection of awered epidermal differentiation rather than increased keratinoc ?turnover themcrease in ~-2pasitivedendriticceilscauidbeareflectianofalteredanfigen handkngin psonatic gin. interleukm-2 (il-2). used m the treatment of patients with metastabc disease fallmg to respond to conventional treatment, can induce regression oftumwrbuik in certain patients however, the systemlc administration ofil-2 is associated wlth a number of toxic effects, including dermatological compl#catlons. these have been poorly documented we have prospectivehl studied the dermatological reactions 10 5 patlents treated wiih il-2 for metastats cdorectal ~arconoma. pre-and past-treatment biopsies were obtwied where possible, arid sect~ons stained with h 8e. giemsaand pas: hesh tissues weresubjected to immunophenotyplng.there were3 femaleand 2malepatients.with treatmentrour~sranginginnumbwfrom 1-5 onlyonepatlenthadapastmedlcal hlstoryof any skm complaint (eczema]. four patlenk suffered a dlffilse eryihematous reaction with mild desquamatm and dryness the other patient developed genwalised erythroderma and an additlonal photosensitivity type reaction. histology, anerthe initialcourse. revealed patchyspmgios1s. exocylosis and basal layer epidermaldamagewnh a mild perivascular chronic inflammatory cell mfinrate. with suhsequent treatment there wasthlckenmg ofthe epiderrnls, plgrnent incontinence. dermal oedema and more marked chronic perivascular cell tnfiltrate. immunohistcchemistry revealed markedchanges inthe expression of cdt , hladr, cam-1 and cd25 m the derm15. these changes were greatly heightsnedwith subsequent liealmsnts. with addnional changes tn other t cetl markers. clearly il-2 enhances the parenchymal expression of antibody-dependent and antigen-mdependent accessory molecules which are important in focusing the immune response. claire m. thornton. maureen y. waish weexaminedalfprimarycutaneaus malignant melanomas seen rn thmdepartmmtover a fweyear permd from 1986 to 1990. the total number of tumoum was 354 the number of cases of malignant melanoma both invasive and m m u , increased from 57 cases ~n 1966 to 92 cases in 1990. superfmal spreading melanoma was the most common type of melanoma, accounting for 60% of the total cases this was followed by the nodular melanoma whch accountedfor 18%. wlthlentigamallgnamelanomaandacral lent~g~nousmelanomabe~ngtheleast commontypes. therewasanincreasmg numberoftumourspresentlngwlth abreslow'sdepthoflessthan t 5mm. thefigurermng from 46% of cases in 1986 lo 64% of cases m 1990 most cases were stdl of ciar*e kud ivanhough mcreasing numbersaftumour presented at clarke levels i and i 1 wlth a corresponding reduction ~n cases presenting at clarke level v more lesions presented with a flat cross sectlonal profile ~n the later years the figures lncreaslng from 30% in 1986 1064% in i w o he numbor of i c s~s showlng surface ulceratan at predentatlon d-reased from 57% in t966to14% in 1990 themltotlcact~vlty. thedegreeofp~gmentalion. theintensiiyofthe~nnammatorycell infiltrate. the predominant cell type and the mcldence of vascular lnvaslon showed no change over the study penod classification of benign vascular tumours is notoriousiy difliwlt and ciinicopathological correlation is often imprecise. this almost certainly reflects the tendency of pathologists to lump together different lesions under the broad heading 'haemangioma', sometimes with capillarylcavernous subtyping. twelve cases of a distinctive subset of cavernous haemangiomas, to be known as sinusoidai haemangioma, are presented. these presented in adws (8 female. 4 male. mean age 49 years. range 2&77). five arose in the upper limb and five an the trunk (of which two developed in mammary subcutis). all were solitary and presented as a bluish cutanmus swelling up to 3.5 cm in diameter of variable duration. one case was associated with ipsilateral gynaecomastia. average foiiow-up of 5.6 years has revealed no tendency far local recurrence or metastasis. histologically these were subcutaneous/deep dermal lesions with a lobular, sieve-like appearance and focally ill-defined margins. they were composed of dilated. thin-walled interwmmunicating vascular channels with a pseudopapillary architecture. thrombi were common and two cases showed central infarction. vascular spaces were lined by monolayered endothelium which was often plump and hyperchromatic but n d mitotic. distinction from wnventional cavernous haemangioma and angiosarcoma (particularly in breast lesions) is discussed. current methods forthe identification of herpes simplex virus (hsvj may fail to identity the presence ofthe virus in biopsy or autopsy material. we have investigated 2 autopsy cases and 3 neurosurgical biopsy cases of clinically suspected herpes simplex encephalitis by a nested polymerase chain reaction (pcr). dna was extracted from routineiyprocessedand paraffin embedded material byproteinase k incubation, phenol chloroform extractionand ethanol precipitation. nested pcr was performed using known oligonmlaotide primers designed from the hsvtype 1 giywprotein d gene from an area with the lowest homology with hsv type 2. two of 2 autopsy c a w and 2 of 3 neurosurgical biopsy cases ware pcr positive for hsv. the third neurosurgical biopsy case was not confirmed by pcr as being due to hsv. such primers lo hsv allow the rapid retraspeaive diagnosis of herpes simplex encephaliis and should be of value to neurapathologists. tissueembedded at lowtemperaturein lowicryl-k4m resin hasbeenshownto besuitableforimmunogoldlabellng of cellular antigens, and to be capable of withstanding the processing required for hybridization of nucleic acid probas.theaimofthisstudywastoestablish basic wnditionssuitabieforhybridirationof digoxigenin labelled dna probes to lowicryl embedded material, both at the light and electron microscope levels. cultured haemopoietii cells wereembedded afler brief aldehyde fixation. digaxigenin labelled whole human dna or plasmid per322 (negative control) probeswereappliedtothinandsem-thinsectionsafterproteolytictilgestion and/or denaturation by heat or alkali. hybrids were detected in semi-thin sections by standard wlourimetric methods. and in thin sections by immunogold techniques. elaborate blocking procedures and prolonged washes were found to be unnecessary. specificnu~l~earsignaiwasseenatbdhthelightandemisv~iwiththewhalednaprobe,revealingdetailsof nuclear dna distribution not evident in paraffin sections or cytospun preparations. non-specific binding and background were minimal. signal was greatly reduced if the denaturing step was mined, and was slightly increased by protwlytic digestion, though at the expense of cytoplasmic morphological integrity. while the sensitivity of this system is limited by the fact that hybridization occurs only at the suriace of the section, it is a rapid and specific means of nudaic acid detection, and offers the dossibilitv of accurate iocalization of intracellular human and viral nucleic acid sequences at a fundamental level. of prostatic carcinoma, mouse liver, kidney and gut were used. acp was demonstrated using an kc-dye cwpling method. the acp was unaffected by the addition of 10 mm tartrate. although the acp was known to be 'tartrate sensitive'. the addition of 100 mm tartrate or 50 mm sodium fluoride weakened but did not eliminate the reaction. mouse tissues, prostatic carcinoma and leiomyosarcoma tissues were processed using variausfixatives and embedding procedures. these were tested for acp and trap. the acp in the muilinucleated giant calk of the leiomyosarcoma survived standard formalin fixation and paraffin wax processing and was tartrate resistant. as expected mouse liver, kidney and gut acp and prostatic acp did nd survive most fixatives and embedding procedures. however acp could be demonstrated in those tissues processed bythe 'amex' method. i.e. fixed in acetoneat -2o' c. processed throughmethyi benzoateand xyianeto paraffin wax. theacp.thus imalised in paraffin blocks was eliminated by the addition of 10 mm tartrate to the incubating medium. if needed the amex pracedure prrsenes some tartrate sensitive acp in paraffin blocks. acp that survives standard fixation and embedding procedures is iikeiy to be tarfrate resistant. showed acp only in osteoclasts. various elements ot tissue processing procedures were examined to find the wnditionsnecessarytoachievemaximum acp localisation. tissue blockswere pr-ssbdintowaxusingstandard embeddingprocedures. threefixativeswereused. 10% neutral bufferedfmalin, formalcalcium and ethanol allat +4'cfor 18 hours.twodecalcifyingfluids wereemployed, 14%ethylenediamine-tetraaceticacid(edta)ph7.2at +4%, zo' c and37'c.andformicacidisodium citrateat+4%forw8 hats. formalinfixed edtatreatedtissuaat +4% produced maximum acp activity. acp was shown in osteociasts, some ostwcytes, chandrocytes. cement lines., tide mark, periosteaicellsand large macrophage likecells inbona matraw. formalinfixed tissues decalcified in edtaatzo'cand37'c werenegativeforacpaswerealltissuesfixedinethana1. lnformalcalciumfixedtissueand formic acidlsodium citrate decalcified tissue the acp reaction was weaker. with some elements, e.g. chondrocvtic acp missing. all the acp preserved through paraffin processing was tartrate resistant. it is well recognised that morphology and optical resoiution are vastly improved with resin as opposed to paraffin embedding of tissue. however, difficulties in producing consistent immunopetoxidase reactions on resin sections have caused many departments to abandon thetechnique. although antigenicity is preserved the low optical density of diaminobenzidine (dae) means that the reaction product is barely visible in thin resin sections. the aim of this study was to develop a method whereby antibodies wmmonly used on paraffin sections wuld be successfully applied to 1 pm resin sections. tissues fixed for 18-24 hrs in 10% formol saline were partially dehydrated and infinratedwithlr whiteresinat4°cfollowed bypolymerisationat40cusingacatalyticmethod. 1 pmsectionswere reacted with polyclonai and monocionai antibodms using a standard indirect immunoparoxidase technique. visualisationwas with a silveramplification systemfordae (amenham) appiiedasthetinalstage. excellent resuns have been obtained with a rangeof antibodies including s100, von wiilibrand factor. immunoglobulins, uchll and l26(dakoltd.). usingthistechniqueitisnowpossibletocombinehighresoiutioniightmicroscopywithaprecise immunocytochemicai reaction. the advantages are obvious and are particularly relevant in the field of lymph node pathology. however, at 15 and 20 gythe number in muscle dropped significantly 5.12 and 24 hoursfoilowing treatment, but hadrecoverad to w n t m levels byfivedays. in the lamina propria, agnor numbersincreasedinitiailyaflerthe5.10 and 15 gy treatments but returned to control values by five days. with 20 gy the agnor numbers showed a significant fall 48 hours after irradiation: this decline continued up to five days. it is evident that &nor numbers within the small intestine are affected following irradiation. the variation in counts is dependent on dose, cell type and time since irradiation. karen m. britten, w. r. roche oepartment of pathology, southampton unwewty general hosp~lai, southampton, so9 4xy in response to ever-increasing demands for immunophendyping in inflammatory disorders, we have developed anernatwefixation and embeddingtechniquesforsmall biopsy specimens. bronchial biopsieswerefixed in buttered formaiin and processed lor embedding in araidite or were fixed in acetone containing protease inhibitors and embedded in the water-soiubk resin glycol methacrylate (gma). gma allowed for the investigation of a full phenotypic profile akin to that which may be wfwmed in frozen section while yielding far superior morphology and greater numbers of d a n s from small biopsies. the phenotypic markers included those for t-ceiis (cd3. cd4, cd8,cd25andlfal),macrophages(cdllc, cd14),mastcelis~b5b6andaat)andeosinophils(mbp, egl and eg2). wehaveaisodemonstratednautrophiieiastase,cytokinesandtheceiiadhesionmolecuiesicaml .elamand vcam. similar high qualty sections were obtained with araidne but the repertoire of antibodies was restricted to thoseantibodieswhichcannarmailybeappiiedin paraffin. wesuggestthatforsmaii biopsies whichrequiredetailed immunohistochemistry, such as in the areas of transplantation and mucosa immunology, fixation in acetone at -20% with the inclusion of protease inhibrors and processing into glvcolmethacwiate with careful temderature control gives optimum results. these included 10% formaiin at vanous temperatures, microwave treatments. bouin's fluid and a wmmercialiy avaiiabieproduct "rapid fix".thetissueswereroutinelyprocessed. embedded in paranin wax andstained wilhthe haematoxylinandeosin method. an eval"ation~fthefi~alion methodswasaisocarriedoutforimmunocytachemicai stains. from microscopic examination of the results t was evident that for the haematoxyiin an+eosm stains. 10% formaiinat6o'cwa~ wnsistentiytheoplimum methodof choice. farimmunocytochamistryali methodsrasuited in a poor performance using a standard trypsinisetion time. however, an acceptable result was achieved from 10% formalinat60°canda microwave fixative method. byreducingthetrypsinisation time. this. however, required strict wntroi. thus it is possible to fix tissue within one hour. by a method which is cost effective and which can be used within limitations for immunacytochemistry. we set out to study the extent and time dependency of storage related artefacts in cytospin fluid (shandon). we assessedtheeffectof stwage in cytospin fluidon the nuciearmarphoiqlyof breast fnac. 10 fnaspecimsns were coiiected on day 1 and slides were made from each specimen on day 3. day 6 and day 8. these were fixed with a spray fixative. between each sampk preparation, the cytospin colleaion fluid was kept at 4%. the slides were fauigen stained and 5 nuclear morphological parameters (area, perimeter, form ar. farm pe. and convexity-concavity) weremeasured using aseescansoiitaire plus imageanalysis system. there wasasignlticantchange in ail the parametem betwwn day 3 and day 6, and between day 3 and day 8 (p < 0.05). the measurements were repeatableon differentoccasionswithoutsignificant difference in theresuns. these results indicate thatstorage in cytospin fluid significantly aners nuclear morphology. the nuclei become progressively larger and more irregular in shape. il is therefore important to standardize the storage conditions of fna specimens. if accurate objective comparisons are required. the identification of macromolecular components of hydrated patholqlicai tissues revealed by low temperature scanningeiectron microscopy (ltsem) isan emergingfieldof enquiry. in orderthatthetechnicaidetaiisforltsem labeilingmaybeestablishedanexperimentaiprotocoi has beendrawninwhichiabeiparticiesofhighatomicnumber are visualized. the experiment comprises a mcdei system in which bovine serum albumen as a known amigen is dissolved in phosphatebutteredsalineand adsorbedontonitroceiiuiosemembtane. theantigen onthemembrane is subsequently reacted mth rabbt anti-cow antibody and then elther protein a-goid or goat anti-rabbn-gold. aner treatmentwithadeveiopertoaddaiayerofsiivertothegoidparticies,thepreparationsareanachedtostubs,rapidiy frozen in nitrogen slush at -21ooc, coated with aluminium and observed on the ltsem stage at approximately -191°c. backscaneredeiectronimagingathighacceleratingvoltages(30 kv)isusbdtodetectsilver-enhancedgoid partic1es.these areciearlyvisuaiized. thefrozen hydrated preparationsarestabieunderthe described wndtions of ltsem operation. in contrast dry, wnventionai. sem preparations are beam sensitive; their initially observed delicate uitrastncture quickly dearades an exeosure to even the moderate i15 kw electron beams emdioved in secondary electron imaging. a new approach to systematic storage of pathological specimens for low temperature scanning electron microscopy as greater numbers of pathological specimens are stored for wnvenient future imaging by iow temperature scanning electron microscopy (ltsem). it is increasingly important to maximise expensive cryostare capacity. a cassenesystem hasthereforebeendeveiopedwhichincreasesthe hoidingcapacityof cryostoresbyafactord2.5 over conventional bee storage. each c-he consists of an aluminium disc 44.5 mm in diameter wilh 6 cylindrical wells10 5mmindiametereveniyspacedand 1.5mmapart. specimens. mountedan jeolstubs,areretainedinthe wells by set screws. five cassettes fit into each 60 x 60 mm glass storage jar, gwmg a capacny for a 10 canister cryastore(w4th 4@rs percanister)of 12oostub-mounted specimens an addtionai benefit ofthecassettesystem is that each specimen is afforded a mechanically and thermally protected environment. specimen collection for ltsem may take place in a distant operating theatre or laboratory. lmmobiiiration of specimens whilst they are in transit excludes any possibility of their being damaged during normal handling and improves the prospects for survivalof accidents.afurther benefitisthataparticuiar mountedspecimencannow bemorespeedily identlledand removed for ltsem from rs well. many pathological condtions are charactensed by the presence of cellular degeneration accompanied by cytoskeietai abnormalities. in many such diswders it is not clear whether cytoskeietai abnormalities are pftmary process or are part of a secondary response to cellular insun by other agents or mechanisms. we have used a fibroblast ceii culture mcdei to study the effects of physical distension on the cellular cyioskeielon. inert beads of 2 and4pm were introduced intoceils byallowingendocytosisor bymicroinjection.thecytoskeietai response tothese beads was studied using immunofiuorescence microscopy. beads introduced by endocytosis migrated to the prinuciear region and over 46 hours became enmeshed in intermediate filament and mlcrotubuiar aggregates. actln microfilament organiselionwas not alfected. incontrast. microinjectionof beadsproduced an immediatecollapseof morofilaments,wiulvimenbnandtubuiin distribution being presened.the immediateresponseto microlnlectlon is similar to the collapse of actin filaments s w n upon thermal stress. this experimental model has shown !hat aggregates of cytoskeietai proteins may be produced within cells as a secondary responseto intraceiiuiar debris, and that microinjection may induce cytoskeietal abnormalnies similar to those seen in thermal stress. thedetection of numerical chromosome aberrations m interphasetumourceiis bynonisotopic insitu hybridisation has been previously described but the application d t h s technique to paraffin embedded material has been wmpiicatsd bythe requirementfottissuesectioning with the production of partial nuciei. inthisstudy, the analysis 014-20pm thickparaffin sectionsolconventionally processed caski ceilsusing both human papliiomavlrus(hpv1 type l e a d achromosome 11 specificalphoid probe wascompared with resunsomained usingintactceils.the use of sectioned material did not give signal distributions comparable to those obtained using whale cells. this is consistent wnh a mathematical model derived for the relationship between section thickness. nuclear size and nuclear retention in paranln sections. a method was therefore developed for the extraction and analysis of nuclei fromthick(50pm)paraltinsectionsandappiiedtotheanaiysisof squamouscelicarcinomasofthecervix(n = 11). the number of copies of chromosome 11 varied from 2 to 7 and this variation was apparent both between lesions and between tumour ceiis within the same ieaon. this is comparable to resuns obtained wth cervical carcinoma derived csll lines. there was. however, no clear relationship between the presence of hpv sequences and chromosome 11 number. these preliminary results suggest that the postulated loss of host suppression of hpv gene function by deletion of genes on chromosome 11 does not occur through gross chromosomal abnormalities. membranous giomeruionephritls (mgn). an immune-mediated disease, is a frequent caused renal morbidity in man. cationic bovine serum albumin (cbsa), given to nzw rabbits in a chronic serum sickness-type protocol. is knowntoinduceglomerularchangessimilartothe humandisease. we~ssedtheenectofashortcourseofthe immunosuppressivedrug cyaon thedevelopmentof early stage.cbsa-induced mgn. fourteen male nzwrabbts received an iv immunismg dose of 1 mg cbsa and 1 p g e. coliendotoxin. one week later they commenced daily iy inlectionsaf 25mgcbsafor21 ~onsec~t~vedays. three rabbtsweresacftficed atthistime. sixofthe remaining 11 rabbits were commenced on a short cou~sb of o m cya. whilst continuing to recewe daily doses of cbsa. the 5 remainingrabbitswsregivencbsaonly.after32consecutivedosesofcbsathesell anlmaisweresacnficed.ali3 rabbns given 21 doses cbsa showed early stage mgn and those given 32 doses of the cationic protein showed a more mature, established disease (thickened glomerular capillary wails wth diffuse. global. granular deposition of igg/c3 and subepithelial electmn dense deposits). four of the 6 cya-treated cbsa rabbns showed a marked reduction in giomerular capillary wail c3 deposition. three of these 4 rabbns had considerably less severe disease ultrastructuraiiy. these results suggest that cya may aker the course of cbsa-lnduced mgn. 'oroartment of pathology university of edmburgh m&~aischooi: late renal aliogran loss 1s due to arterial intimai proliferation and iumenai narrowing. there are few studies ofthe phenotypes of the intimai cells. we analysed these lesions by light microscopy and immunmyiochemistry using antisera against t-lymphocytes. b-iymphocytes. macmphages, smooth muscle cells, class ii hla or molecules and the proideration antigen pclo 31 vessels were studied from 20 gran nephrectomies resected between 3 and 171 months post-transplantation. we identified an arterial endolheliaiilis, r-rted in cardiac aliografts, but not emphaszed in renal graftrejection. 4 panernsolarterial pathoiogywwerewgnisd: (1) endotheiialitis in nnteriobuiar arteries without intimal proliferation, (2) endothelialiis in larger arteries accompanied by intimal prdtferat!on of smooth muscle. (3) '"inactive" lesions with thickened intima (i foam cells) but no endotheliaiitis, and (4) 'natural" atherosclerosis of larger arteries. the endothellaidis tended to m u r in shmw sumving grafts. the pedominant cell was the macrophage. with fewer t-lymphocytes. pclo was expressed in mononuclear ceiis, smwth muscle cells and endothalid ceiis. pmicuiariy. but not exclusively in younger grafls. we proposb these ledonsevolve, variably. from an early endotheiiaiitis to late chronic vascular rejmlon or gralt athwmierosis. the predomlnance of the macrophage at ail stages, suggests it plays a significant roia in the evolution of these lesions. the rat is used to study the response of the renin-angiotensm system m diseases such as hypertension there are structural differences in the jga butthere are few comparisons of its response to stimulalion between species we used renin antisera and an lmmunoperoxidase technique to stain renin-containing cells (rcc) ~n rat (n = i t ) and human kldneys(l5 nephrectomy and 11 autopsycases). westmulated therenin-angintensin system experimentally by clipping one renal artery (5 rats) and inducing sodium depletion (6 rats) and studied the analogous human diseases-renal artery stenosts (1 0 cases) andaddison'sdissase(6 untreated and 5 treated eases). wecounted the rcc and plotted their distribution on scatter diagrams. there were some dinerences in distribution between the species but in boththerewasagradient in distributionof rcc which predominated m the superficial renal cortex. in sodium depleted rats. recruitment of rcc in the iuxtamedullary jgas abolished this gradient. while in some of the animals with renal artery clip hypeitension the normal gradient was reversed, with most rcc in the deep cortex. in bdhu~nreatedaddison'5diseaseand~nrenalanerystanosistherewasanoveralincrease(xs)m rcc butthenormal gradientoftheirdistnbution withintherenalcortexwasmainlained.theseresults haveimpl,cationsfortheroleolthe intrarenal renin-anglotensln system in the control of renal haemodynamcs. we have developed a model of adult human prostatic epdhelium that allows arch$tectuml and cytologioai features to be maintained. epithelial organolds produced by enzymic digestion of human benlgh prostatic hyperplasla tissue weresuspendedm type collagengelandsubcutaneouslyxenogranedintointact malenudemice.thexenogranis progressively invaded by mouse stromal cells thesesurround theepithelial organoids and supportthe reformation of epithelial structures with a lumen, lined by a mixed epithelial layer. as the lumen forms tall columnar epithelial cells begin to be seen, these progressively express the prostate specific epithelial markers. psa and psap further the xenograflsexpress appropriatecyiokeratin markers in boththeluminaland basaleplthellal cells. gelsplaced within a 0.45 pm millipore chamber, which do not undergo stromal invaston. lose all epithelial organisation with disorganised sheetsand ballsofcellsbeingfound.these cellsdonot express thesecretory markers. in the absence 0lanandr0genic~tim~i~sep,th~l~~l structures wsth a lumen are formed but there are no tall columnar secretory cells and noexpression ofthesecretory markers. thismodel hasfurther been investigated todetermine theresponseof human prostatic cells growing in vivo to the antiandrogen flutamide and to a 4-aza-steroid 5e-reductase inhibitor these observations indicate the essential role of both stromal cells and androgens m dictating functional dlfferentlatnon this model will allow the dissection of the regulatory processes involved in prostatic differentiation. hepatocyte growth factor (hgf) is the most potent known mitogen for adult rat hepatocytes in pimary cuiture and isthoughtto haveanimportant rolelnlivergrowihandrepalr linle~sknownaboutthemechanismofactionof hgf on hepatocytes. since the adenylate cyclase system has been implicated in hepalocyie growth control. we examined the role of adenylate cyclase and cyclic amp wmp) in hgf-stimulated dna synthesis. human recombinant hgf (hrhgf. 10 numl) had no elfect on baa1 or stimulated adenylate cyclase activity in membranes prepared from freshly isolated rat hepatocytes. similarly, hrhgf had noeffect on intracellular camplevels in cultured hepatocytes. furthermore, agents which increase camp inhibited hrhgf-stimulated dna synthesis m primary hepatocyte cui1ures glucagon had an i . c. , of lo-'; fotskolin (107. ibmx (10"m). 8-broma camp (300 pm) and dibutyryl camp (300 pm) completely inhiblfed hrhgf-stimulated dna synthesvs. from thts. we conciude that adenylate cyclase and camp do not have a role m hgf-stimulated dna synthesis m pnmarycultures oladult rat hepatocytes. the receptor for hgf has recently been identified in tissues other than the liver, as c-met a protooncogenewith intrinsictyrosinekinaseactivitv. whether or notc-metactsasthsrecedtorfor hgf ~n heoatocvtes 1s currently under investigation a novel in wvomodel of intestinal differentiation is descnbed. fourteen-day, undifferentiatedfetal rat small intestine. stripped of the major part of 11s mesenchyme. then suspended in a type i collagen gel and renografted ~n a nude mouse. undergoessmall mntestbnal morphogenesis and cytod$ffeienbat$on. all tourmapr epithelial imeages. namely paneth. goblet. columnar and endocrine. are present. double labelling m sit" hybndlzatlon, employing biotinylated and digoxigenin labelled dna probes to whole rat dna and whole mouse dna, reveals an unusual ]uxtaposition of species specific stroma. the outer longitudinal smooth muscle layer, and the major part of the lamina propria. p53isthemost commdnlyalteredgene~n humanturnours. mutati~nleadstothep~oducfionolanabnormalprotein which can be detected by immunohistology. such abnormalales are seen in a wide variety of turnours, including colon cancer. abnormal p53 protein levelshavebeen detewed in 5&55% of sporadiccolorectaltumours. in order to determine i p53 mutations occur in carcinomas arising from dyspiasla. we have investigated the prevalence of such mutations m colorectal carcinomas from patients wr)h long-standing ulceratwe colitis 1%). lmmunocytochemicalstalnlng waspwformedon3freshand32 paralflnembeddeduccarclnomasand35sporadlc carcinomacontrols matched forsite, stageand grade six areas ofdysplasla, (fourassoclatedwlth uccancers)and 7 sporadic adenomas were also stained. p53 protein was detected by immunohistochem~stry m the 3 fresh uc cancers and 8/32 (25%) ofthe paraffin embedded uc cancers usmg the antibodies cmi, pab 240, pab 1801 and pab421. slmllarresuitswere obtained in thesporadic carcinomasw,th 113fresh cancers positlvefor p53 and 7/32 (22%) of the paraffin embedded cancers. two areas of dysplasla which were associated with p53 postlve uc cancer~also showed positive p53 staining, alongwith an adenoma. our results indicatethatunlike k-ras mutations, p53 proteinabnormalities occurat a similarfrequencyln sporadic colorectal carcmomas, carcinomasar8sing !n uc as well as being present in uc dysptasasla. this work suggests that p53 mutations play a mle m the dysplastacarcinoma sequence. threepanernsofstainingareloundin humancolonusingatechniquetodemonstrateo-acetylationofsialomucins (mpasj. 8% afindivdualsshowunifwmmpas-positivity. theremaindwareeitherent~~ympas-negativewmpasnegativewith occasional positive crypts. we suggestthatthisrepresentspalymorphismof an autosomal gene (0sa) controlling 0-acetylation of sballc acid. isolated crypt-restricted mpas-posltivky in otherwise negative indivtduais representing somatic mutation of the ma* gene in crypt stem cells of osa'/osa-individuals. to test this we have studied colons from 80 patients with rectal carcinoma, half of whom had received 4000cgy radiation 28 days preoperataely. radialiond~dnotaffecttheprevalenceofthethreepnenotypesbutincreasedthefrequencyofmpasposltlvecryptsinanegativebackground(t6 2~1 0~~~6 . 5~ to*, p <0.05), largelyduetocryptsshowingseclorial mpas-positivlty (8.2 x lo* ys 0.4 x to4, p < o.c€ql). consistent with incomplete crypt colonisation by a recently mutated phenotype. the prevalenceofthisosa*/osa~phenot~e(radiated43%, non-radiated 39%) isveqcloseto the predicted heterorygosily rate (40.3%. hardy-welnberg law). thew resuns suggest that human colonic crypts are monoclonal with a longer stem cell cycle than the mouse and that mpas staining provides a method for measuring human stem cell mutattonal load. pouchrris m leo-anal resarvoirs is a frequent complication of restorative practocolectamy which is associated wtih constderable morbidity. long term complications of pouchitis are unknown, however patient follow-up wlth sigmoidoscopic surveillanceis mandatory to assessdysplamc or neoplastic changes in resldual rectal mucosa. we examined epithelial cell proliferative activdy in the ileal mucosa of pouch biopsies using the antibody pclo which detects nuclear expression of the 36 kd nuclear protein proliferating cell nuclear antigen (pcna). ten patienls with functtoning ,lea-anal pouch reservoirs of at least one year duration were biopsied and assessed histologically for evldence of pouchitis formalin fixed paraffin embedded biopsies from anterior and posterior pouch wall were examlned with pclo using the pap technique. ten terminal ileum sctions from right hemicokctomy specimens werenormalcontrols. cryptsin pouch biopsiesand normalcantralshadasimilarpciolabelling indexmeanof78k and 82% (mean values 71-81 and 7 w 3 ) respectiveiy the sides and tips of villi had a significantly greater pclo labellmg indexinthepouch biopstes(72mean. range59-33). compared withnormaicontrols(t7% mean, range 12-20) these resulk demmstiate an expanded proliferatwe epnhelial compartment in ileal pouch mucwhich in contrast to normal terminal ileum involves villous surfaces. considering the frequency and long term natllrs 01 pouchitis. thesefindingssupportthe need for continued pathalogical and clinical assessmentof the ileal mucosa in the neo-rectum of these patients. we, cui, i c talbot, j. m. a. northover signiticant alterations in structure. function and gene expression of mltochondna have been reported in cobrectal turnours. but it $5 not known rf these abnormalities are due to mitochondria1 genetic alteration. in this study, total cellular dna was isolated from 15 l lo rectal carcinomas, 8 adenomas and their adlacent histologically normal mucosa. these dna samples were digested separately with 13 different restriction endonucleases. and then analysed by southern blotting using apurified mtdnaprobe. the restriction fragment pattern oftumourmtdnawas comparedta thatofeorrespondingnormalmucosalmtdna.theseresultsshowedthattherearenalargedeletions. insert~ons, or rearrangements $n turnour mtdna. and no single base changes m the delectable regions in spite of some polymorphic vanations. our results suggest that mtdna changes are unlikely to have a malor role in human colorectal tumoungenesis. hence, alterations in colorectal turnour mitochondria must be dependent upon other mechanisms crescentic colitis: the clinicopathological spectrum of a distinctive endoscopic feature in the sigmoid colon n. a. shepherd, s. gore, s. p. wilkmson oepariments ofnsfopafholcgyand gastreoterol~y, gloucestershre royal hospml, great western road, gloucesfw, crescentic coibs describes an endoscopic appearanc0 of the sigmoid colon charactwised by mucosal swellmg, eqhema and haemorrhagestrictly localised tothecrescentic mucosal folds. in alive yearpericd thisdiagnosiswas made m 34 patrents, representvlg 1 .a% of ail fbeopta endoscopies. there was a male predominance and most plients were middle-aged or elderly. dwerticulosis waspresent m most (82%) but theabnomallf~es wareconfined to the crescentic mucosal folds with sparing of the divenicular onfices. the malorlty of patients presented with a history of bleeding perano. histologically there wasaspectrum of changesvaryingfrommlnorvascularcongestian to florid active inflammatory disease with crypt architectural abnormalities mimicking ulcerative colitis. three patients presenting with crescentc colitis later developed the clinical, endoscopic and histopathological features of distal ulcerative coliitls: two other patients with a history of distal ulcerative colitis were found to have the charaderlstlc changes 01 crescentic colitis only at endoscopy. three cases showed the histological features of mucosai prolapse the findings in thisstudy demonstratethat arelativelyspecificendoscopicfeaturemayexhibit a wide spectrum of pathological changes whilst luminal mucosal inflammation of the sigmoid colon, usually in a5sociat1on wiih diverticuioss. may mimic the pathology of chronic inflammatory bowel disease. asmall propartion of these cases may represenl a strictly locallsed form of chronic ulcerative colitis. of genome and antigen a n various anatomtcal sees the resuns have imolications lor the mechanism of e n t~ of mv into neurons and for mechanisms of transynaptic viral spread neuiopathology, fnstitute of pathology j chow, j tobias.' k co1ston.2t j chambers estrogen is generally considered to maintain bone mass through suppression of bone resorption we have previously demonstrated that administration of pharmacologic doses of estrogen increased bone formation in ovary-intact rats to assess theeffectsof physiological concentrationsol estrogen on boneformatian. estrogen was administered to ovariectamised rats fi n which bone resorption was suppressed by ahprbp. animals receiving exogenous 17p-estradtal (ed (1 wglkg. t o wgikg and 1 w pgkg daily for 17 days) showed a dose-dependent increasemtrabecularbonevolumeaft 9%. 25.8% and43.6% respectively, compared wnhthoseratstreated with ahprbp alone. the increase in bone volume was due to bane formation in e,-treated animals, in which bone resorption had been almost completely suppressed by ahprbp neither ovanectomy. ahprbp nor e,-treatment had asignificanteffecton thevolumeorrateoflormationofcortical bone thus. theiocreasedbonerasorptionwhichis aconsequence 01 estrogen-dellclency entralns lncreased bone formation, whlch masks a slmunaneous reduction in estrogen-dependent bone formation. it thus appears that estrogen maintains bone volume not only through inhibition of bone resorption. but also through stimulation of bone formation. pgs m bone formation m vmo. which may represent a pathway common to bone anabolism that 8s observed !n response to many e""lio"mental5t1m"ll pgf2, was wlthoul effect we found that nodule mductton by pgs occutred early the cunures, belore nodules lntegrln expression e n human bone was examkned by immunohistolqlical stalnmg of edta-decalcrfec and undecalcllned cryostat sections of fracture-and tumour-associated callus dbtalned at surgery and neonatal costochondral )unctions obtained at autopsy. cases were stained wlth a panel of well-charactsnsed monwlonai antibodies against p1-3. el-5 and uvp3 integrios using abc peraxidase and indirect immunofluorescence techniques. osteoclasts stained lor pl , p3. u2 and ovp3 mtegnns. indicating that they express u2p1 nlp-2) and uvp3 (classm vttranectin receptor) ostmblasts stained lor pl, 04 and u5, and osteocytes stained for p l and 05. indicating that ostmblasts express n4pl nlp-4) and m5gl nlp-5. classical fibronectin receotorl and that vlp-4 expression 1s reduced or lost during differentiation to astwcytes j qulnn. n a. athanasau nufield depanment of paihology and bactenotogy, level 4, john radcoffe hospital, oxford, ox3 9du osteoclasts are known to effect bone resorption in inflammation and malignancy but whether other cells of the mononuclear phagocyte system. particularly macrophages and macrophage palykaryons, are similarly capable of pathological bone destruction is uncertain macrophages derived from tumours (human lung camnomas. murine mmw-assmated mammary carcinomas) and inflammatory lesions (munne foreign body granubmas) were cuituredonboneslicesbothin thepresenceandabsenceaf stz slromalcells.theseneoplasticand inflammatory iesions contained a heavy macrophage infiltrate but no giant cells and no calcified tissue. there was superficial roughening ofthebonesurfacebymacrophagesboth inthepresenceandabsenceofst2cellsand.aher t4days. scattered areas of lacunar resorption 8 n co-cultures of macrophages and st2 cells. normal pulmonary tissue macrophagesdid not produce resorption lacunaeunder these conditions. the results show that macrophages alone are capable of atype of low-grade boneresorption and that a subpopuwion of turnour 01 inflammation-assaoated macrophages following specific interaction with slromal cells, can differentiate intocellscapable of the special8sed function of high-grade lacunar bone resorpt1on macrophages may thus directly contribute to the mteolysis associated with metastatic turnours and inflammatory lesms in bone differences in the grade of osteolysis may also account for clinical differences tn the degrees and rate at which pathological bane resorption occurs the george washmgton university medtcal center, washnqton, 0 c , u s a for decades, new technological advances have been hailedor condemnedas representing the extinclion 01 cla~s~cal diagnostic surgical pathology, but so far the reports of the death of our specialty have been grossly exaggerated. indeed, the newtechnologies of the 1990sare seenas aids torathet than replacementsfor careful and intelligent gross and micmscopic examination and interpretation, which havealways remained the 'gold standard" against wnichnewtechniquesaremeasuted thedecade will bemarked by anexplosionof pos5ibilitiesfort155ueas well a5 non-tmue diagnosis, balanced by a shrinkage in both specimen sizes (already evident in breast pathology) and healthcare budgets.thus. thesurgical pathalogist will haveto becometoanevengreaterextentthecomplete physician. in order to beable to choose wiselyand economically from thediagnostic"menu"availab1e. thesurgical pathologist w d also have a greater need than heretofore to be a competent cytopathologist as well, as many of his or her cases will also have fine needle aspiration material and a nuclear grading will assume greater significance o n tumor pathology. finally, the roles of the surgical pathologist ~n both research and patient care (including direct patteoi contact) will require emphasis m order to attract more medical students into our specialhl. womenorthosewithlowgradedisease.this hasledto theviewthathpv 161s~nielatedtocer~1c~l cancer asimple pcr protocol was developed using standards containing 0.1-100 fg of hpv 16 dna in 100 ng of normal human placental ona toestimate levelsaf hpv 16 dnain smearsor biopsies. the quantltativedistribution of hpv 16 dna tn normal and abnormal ~ervlcal epithelium was mapped thmughout 50 loop biopsy and hysterectomy specimens using micro-dissectionand histologyof alternate millimeter slices levels were measured in parallel c~n~c~i smears. preliminaryresuits show a low lwel of hpv 18 dna(equiva1ent to one copy per 100 cells) was usual in women with normal smears or low grade abnormalities replication of hpv 16 dna to a level of one copy or more per cell was limited to areas of cin2~3 which may be very small and to atypical immature metaplasia. the level was reflected ~n the smear aswitch to a high level of hpv 16 dna s a biological and potential diagnostic maherfor high grade precancer. cerv8cal biopsies were stained by the cracker technique to demonstrate agnors. for the purposes of the study, b~opsiesweredividedlntaflvegroups-normal, kallocytosis.cini.cin iiandciniii.usinganiemps/2 hastingan a m s photon framestore a customised image analysls system was created. the image 1s dllated and eroded to close any cavities an outlining procedure locates the agnors and records their mid-pants. from this 11st of midpants themeandistanceofeach agnor'slhreenearest neighboursiscalculated.thlsprocedurescanledoutfor several lelds of view. this study attempts to relate the shape of the associated "mean distance" histograms to the histologlca1 diagnoses in flry cases. primary adenocarcinoma of the cervix: a retrospective clinicopathological study of 55 cases r ananoos, kamta nahar.' alison b,grigg.'s. roberts? sergin m. 1sma11 the patientfen healthy with a tendency togain weight being heronlycomplaint. gynaecological referral revealeda 28 week gestation abdominal mass and bilateral varicose veins. laparotomy, lee oapharedomy, total abdominal hysterectomy and right salpingo-oophorectomy were carried out the len ovarian turnour was cyst~c, smoath surfaced. unilocular,cantainedturbid brownnon-greasycontentsand was22cmln diameter.al0cmsquarearea of lhe lining showed papillary tutmg. and the remainder was smooth. hiatology of these papillary areas revealed a papillomatow proliferative squamous neoplasm with keratinization and mild acute inflammatm. wthout evidence of cytologicalatypia.stromal invasionora benigncysticteratoma.theremainderofthecystshowednat swamous. cuboidal, or low-coiumnar type epithelium with an underlying vaguely endometrial type stroma in minute focl, with occasional small secondary cysts thls unusual squamous neoplasm was diagnosed as a proliferative epbdermoid meglomerularperipolarcell isan epithelial cell snuted atthe vascularpole ofthe glomerulus recently, theexistence of the penpolar cell has been doubted the aims of this study were first, to establish whether the peripolar cell is a m q v e cell type ~n the mammalian kidney. and second, to compare their numbers and morphology in different speces we used scanning electron microscopy to study 1-12 kidneys from each of 11 mammalian species including man. we removed the glomeruli by microdissection and examined a minimum of 20 vascular poles from each kidney penpolar cells were largest and most numerous m goat and sheep kidneys (1w% and 84% of glomerul~) meywerescant~estandsmallest 10 humanand bovinekidneys(6 5% and 11 %).whileaspectsotsome per~polarcells resembled podocytesand otherperipolar cells had features reminiscent of parietal epithelialcells. in each ~pe~ie~wewereabletadistinguishperipolarcellsasaspeciflccellhlpe. weconcludefirst. that theglomerular peripolar cell 1s a unique cell type ~n the mammalian glomerulus, and second. that their morphology and number cystlc renal disease occurs in various forms characterised by dilatation of different pans of the nephron. the morphologoal, clinical and genetic features of these diseases is variable but some animal models have been developed m an attempt to understand the mechanism of cyst formation within the nephron. we describe a polycybtic1.510.ofthe kidneyinthscea-n mousew~hanx-linkedrecessive~mmunodetic,entsyndrome there is progressive cystlc dilatation affecting all parts of the nephron. the cyst lining is composed of a single l a y m c epithelium with focal nuclear crowding and the formation of micropapillary structures. the cystlc epithelial cells show subnuclear vacuolation focal basement membrane thickening is also a feature. there is no signdicant inflammatory infiltrate present within these ktdneys. election rni~roscoptc examination w e a l s that the subnuclear vacdation 1s due to loss of the membrane infoldings at the basal pole of the eplthelial cell wlth flud accumulatlon within the extracellular space. the basement membrane thickening is due to expansion of the lamina dense. the finding of a plycystic kidney lesion on these mice offers an opportunity to investigate the relationship beween the immune system and renal cyst formation. eqthropomtin. a circulating glywprotem, is the principal humoral regulator of elythropoiesis. it 1s produced in the kidney butthe precisecell oforigin iscontroversial. erythropoietin participates in a~1~ssicaif88dbackcontroi system whch attemots to restore oxvaen deiivew lo the tissues. normallv erdhrowiatin is resent in the sbnm at picomolar c6mntrations bui revels may h e up to 1001oid durilg ?&erehkpoxic ;tress. the mechanism linking renal oxygen sensing with erythropoietin synthesis is p o~l y understood but there 1s evidencethat cells of the innsr cortex respond to tissue hypoxia by producing elythropoietln. eryihropoietin geneexpression in the kidney can be detected by northern blot anaiysis within one hour of exposure to hypoxie stimulation. the cellular location of erythropaietin m-nger rnawasdetected inamurine model byinsdu hybridizationemploying radioiabeiled dna probes and autoradiography techniques. tubular cells of the inner renal cortex wbi b identifled as the main site of ervfhropoietin gene transcription. the location oterythropaetm production was confirmed by immunohistochemistry with anti-sera ra4sed to pure recombinam dna-denvea human elythropoetin. the specific antibodies bound oniy lo tubular cell cytoplasm, confirming the tubular location of erythropoiet,n-producing cells. severe reversible acute renal failure and iga nephropathy r jackson, k l. c. mclay unrvemty diws~lon of pathology, giasgow ropl infirmary, castle sireel. glasgow, g4 osf whilst progressive, irreverable renel failure is well known in the evolution of a stgnificant proportion of cases of iga nephropathy, disease-related. reuerstbie, severe deteiioretion in renei function 1s a less well recognized phenomenon. relatively few cases aredocumented in the literatureand these have invariably been associated with m-iw haematuna. renal failure has been largely attributed to a combination of tubular obstruction by red -11 cast~andacutetubularn%crosisthaughttabetheresunof adirecttubulo-toxiceffectof released haemoglobin. in a review of 122 cases of i@ nephropathy we have encountered two cases of this type. the clinical. histological. immunohistochemical and ultrastructural data relating to these cases are presented. on the basis of this evidence and an analysisof the relevant literature. 11 isconcludedthat the accepted pathogenetic hypothesisdnot provide an entirelysatisfactaryexpianationof the phenomenon. itisfurlhersuggested that immunologically mediated injury dfrected at the glameruiar vascular pole and possibly the extraglamerular mesangium could compromise thetubular blood supply and might also lead to haemorrhage into the distal tubule at the macuia densa. scanning electron microscopy (semi when combined with electron microprobe analysis (mpa) 1s an expeditious and accurate method of identitying substances deposited in tissues. we report a case in which these techniques were used to study crystals in a transplanted kidney. the patient presented at age three with vitamin d resistant rickets and fanconi syndrome on the basis of cystlnosis. he gradually went into renal failure and received a kidney transplantfrom hismother. itfunctionedwsiifarafewmonths butthen deterioratedandwas removedone year after transpiantation.afewcrystalswereob~ed by light microscopy ma biopsytakenattwomonths. arepeat biopsy at four months was examined by sem and contained the typical hexagonal cryystais of cystine. the s o i i i sulphur peak obtained with mpa confirmed their elemental compojltion. the hydrophilic nature of the cystlne prevented their identificetion within routine sectionsfor transmission electron microscopy (tem). the hexagonal o~tline of aystaiswas confined to interstiitat macrophages rather than tubular arglomeruiar ceiis. 10 pm frozen sections mounted on carbn pianchets diowed vlsualisation and analysis of the crystal deposits by sem. the use of appropriate processing methods may be crucial m identifying crystal dspasition within pathological specimens. during the 10 year period 7981-90.1 1 new cases of dense deposit disease (m~~b,a"op,olif~=ti"~ giomerulonephritis type ill were diagnow in nonhern ireland. two further known patients developed recurrent disease in renal transplants. the mean age of onset was 14 years (range eight-22 years) with five males and eight females affected. renal function was impaired in 38% patients at presentation which ranged from nephrotic syndrome (55%). nephrilidnephrotc syndrome (15%) and macroscopic haematura with mild protelnuria (15%) lo mild protemuria f microsopic haematuna (15%). serum c 3 was universally low. haw of initial biopsies showed cr-entsusuailyaiatedwith rapidansefrenaifailure. 38% ofpatientsrequired diaiysisatorwithin twomonths of presentation. a further 15% d patmnts developed renal failure within three pars of disease onset of the six patientstranaplanted haw havedaveioped rmrrent diseasin their grafts six patients havenot required dialysisat ameanfoilaw upoffour yearr(ranse0neloeightyears). mhaugh reialweiyuncommon, dense deposit disease isan important causeof renal failure in children and adolescents. we have confirmed that this disease has a poor outlook in terms of renal function with a tendency towards recurrence in grafts a review of 73 renal biopsies from patients with diabetes mellitus. [1981] [1982] [1983] [1984] [1985] [1986] [1987] [1988] [1989] [1990] . showed 45 with diabetic giomeruionephropathyalone, 25 with other renal diseaseand3 with both diabetic giomerulonephropathyand other renal disease. eight with the histologiwl appearances of diabetic nephropathy without known diabetes were alsn identified. clinical details were available on 68 ofthe 73 patients. these showed that in type 1 (insuiin dependent) diabetes (24). most (19) showed diabetic giomeruionephropathy, 2 showed both diabetic glome~lon~phropathy and another diagoaas, and 3 showed aniy another diagnosis in type 2 (non insuiin dependent) diabetes (44). 23 showed diabetic glomerulonephropathy with 20 showing another renal diagnosis without diabetic giombrulonephropathy, and 1 with both diabetic glomeruionephropathy and another diagnosis. 01 6 patients investigated with nodular glomerulosclerosis resembling that seen in diabetes but not known to be diabetic at the time of biopsy, 5 showed abnormal glucose metabolism on investigation and t showed a paraprotein. this review showsthatinpatientswithciinicairenaldiseaseanddiabetesmeliitus,therenaldiseasecannotalways beassumed to be diabetic nephropathy especially ~n type 2 diabetes where a wide range of other renal disease can occur histological findings of diabetic nephropathy may occur in patients before diabetes is diagnosed cllnlwiiy. a j. hawie, r. l. bryan in a biopsyof arenaltransplant. we notedan artmalabnormalitythat wasunrecorded in standard texts. in an arcuate artery. theiewastheappearanceafformation ofanewartery inside theoid, with layersof muscleandelastic fibres that in places resembled an internal elastic lamina. separated from the original internal elastic lamina by loose connective tissue. in a systematic study of 156 consecutive transpiant biopsies and 17 consecut~ve transplant nephrectomies. another six examples of this abnormality were found. these six and the index specimen showed changes cons~stent with chronic vascular rejection. in a systematic study of 28 consecutive nan-transplant renal biopsies showing interstitial nephritis. another example ofthis lesion was found, in a kidney showing chronic interstitial nephntis. thischange isprobablyavmantfom of muscularisation ofthsarteriai intima, isseen in chronlc renal damage, and occurs in transplanted and native kidneys. localised myloidasis ofthe lower genito-unnarytractisararedisease. few studleshaveanempted tocharacterise theamyloidtypeusing immunohistochemicalstains. wereportaseriesofnin~casssinvoivingthebladder(7), lower ureter (1)and penile urethra(1). thesecomprised7 malesand pfemaies with an age ranged 5&79years. nonsof the patients had evidence of systemic amyioidoss. three patients had a past history of lower genito-urinq tract infection and of these, one had repeated instrumentation. one patient had prostatic carcmma the cmmonast presenting wmpiaint washaematuriaand the mostfavouredsurgicaldiagnosiswasa neoplasm. fowpat#ents had repeat biapsiesfor persistent orrecurtentamyloidosiswith atimeintmal ofupto2t yearsfram initial presentation. bght microscopy showed amyloid deposmon throughoutthebiopsies, in lamina propria. muscle. adiposetissueand vessel wails. with a variable giant cell reaction and lymphoplasmacytic infillrate. an abc-immunaperoxidase techniquewas usedwith antibodmsto pcamponent, serum amyioidaprote8n prealbummandkappaand lambda light cham in an attempt to classify the amyloid type. this was found to b e d non-pa. non-prealbumm type. a negative or equivocal reaction was seen for kappa and lambda light chains however, such antibodies may not necessarily be immunoreactive with light chains or fragments of light chains m amyloid deposits. features of bile reflux type gastntis: glandular distmion (branching, "carkscrewmg"). nuclear regeneratwn, intramucosal smooth musclefibresandpaucityof inflammation. helicobacterpylanarganiams werenoted bileacid concentration #n gastrc aspirates collected by endoscopy at the time of biopsy was estimated using an optical densitymethod.gi23casesshowingglandulardistorti~7 hadraisedgasttic bileacidconcentration.m18cases with mahednuclearregeneration6hadraised bileacidsandof 11 case~withinbamucosalsmoothmuxlefibres4 had raised bile acids nine of 12 cases with raised bile acids showed a chronic inflammatory response the histological features of bile reflux type gastritis which correlate best with estimation of bile m gastric juice are glandular branching, "corkscrewing" and intramucosal smooth muscle fibres whereas pauclty of chronlc inflammation does not h pylon was identified in 8 of 12 cases with raised bile acid. aims to compare the bacterial flora of normal and inflamed appendices. and to conelate this with various histological features. to establish the incidence of yeninla infection ~n acute appendicihs !n southampton. methods resectedappendicesweresentheshta histopathologyandal cm portionwasremovedandcultured for aerobic and anaerobic organisma. the remainder was fixed ~n 1 0% buffered formalin and pocessed for rwtine histology results: 38 appendices showed acute ap+endicitis, and 30 were normal. histology there were statistically significant differences between the two groups for the p s e n c e o f faecollfhs (p < 0.01). fibrosis (p < 0.01) and prominent follicles (p < 0 05) -all were more common ~n the normal appendices. microbiology no yer~inia was cultured in enher group. there were statistically significant differences in the number in each group which grew anaerobes and streptococci. anaerobes were more common in the normal group (p < 0.01). and streptococci morecommon in inflamedappendaes(p< 0 05) conclusions. 1.thereisanaiiwed bactenalflora in acute appendicitis. 2 yersinia does not contnbute to acute appendicitis in southampton. 3 faecoliths. fibrosis and prominent follicles are significantly more common in normal appendces le antigen (using cat9-9) a i d type 2 h antigen using a specific moncbnal antiserum. we f w n d a widespread distribution oftype 1 structures in both benign and malignant epnhelium oftheextrahepatic biliarytract and ampulla of vater. type 2 h antigen expression was seen in benign epnhelium and in non-papillary tumoun and ampullary carinomas. lmmunohistochemical detection of tyw 1 blood qrou0 antlqens does not adpear to be ofprwnostlc the majority of cases bearclose relationship to human ulcerativecolitisclinically, endoscopcallyarid i" re-nseto treatment one hundred postmortem iiyerswerestudiedfromconontoptamanns with totalseversul~ataecolitis who were pathogen free and had a histological picture resembling human uicerallve cdhs only 39 iivwere normal in 20 there was a mild penportal chronic inflammation. 16 had extens~ve steatosts, 4 had an appearance resembling chronic active hepatitis and ~n 4 the histology resembled that of sclerosng cholangitja. other hepatic pathologies were s e n in smaller numbers. these changes parallel the itver disease seen in association wlfh "icbrativbcolitisinman. webelievetheconon toptamannprovidesthefirst modelof l i~e r d i~~~~e m u l~e r a t i v e~~l n to allow sturty of the pathogenesis of the enralntestinal manifestations of ulcerative colitis. r-rvolr and ilm-anal anastomosis. pre-and pan-surgical specimens were studied and compared using routine histological and histochemicaltechniqm themalontyofcasssexhibitedan lncreasem chronc lnflammatlon wlth 1 1 n 1 0 or noacute inflammation.the levelsof chronic innammation were found to bemost severe i" those cases which ~~fferedhompouchiti~. morphomstncalanalysisrevealedan~ncreaseincrypt depthtovillousheightration(cdvh) ~n 88% of cases. the cdvh in the pouchitis cases was greater than 8 n the other specimens studied the resuns of m u m histochemical analysis did not show any charactenstic changes occumng. in the cases studied. lectm histochemistry demonstrated an increase an supranuclear staining of the pouches with dba. sea, wfa and wa. which is similar to that fwnd in poximal colon. staining with psa, lca. u f 3 and lta revealed charactenstic changes in binding panem th-may mdjcale changes m tucosylation of certain cellular canponents. certain changes in lectin binding were found to be more sjgnificant in the pouchitis group of cases. the changes in the ra~ewoir mucosa are most irkely to be an adaptive response to the new mtra-lummal environment wlth the acqmdfon of cmain mime chaiacteristics. thereare alsosp~ciftc changes which occur to a greatsrdegree m the cases with wuchits, these may occur as a result of or lead to the occunence of puchms. these resuns may be cryostat sctionshomten patientswith ileal pouches lor extensive colitis, ten distal ulcerative ~olitics and five normal mall intestines were assessed immunohistochemically for macrophages (leu m5 antibody). rfdl gnterdigitating antigen presenting cells). and rfdt (resting macrophages)antigencantainingcellsin lminapropna. result~areexpressbdasape~=~~t=g~~f thetotal. normal small intestine contained a mean 7?4 6% and 8% (ranges 3-9.2-1 1, and 2-13) leu m5. rfdl and rfdt positive ~ell~re~pecl~~elywh~chcontrastswiththoseh~ghervaluesinpouchbiapsies-86%,30%and88%(ranges71-94, 21-52and 7694)respectively. distal ulcerative coilticscontalned increased macrophagenumbers(43.43 and27% for the three antibodies) but have a predominance of the rfdi positive population in contrast to pouchitis patients in whomthe rfd7 positive cells predominate thesefindings demonswate remarkably high macrophagenumbersin pouchitis, howeverthe rfd7 positive sub-populations predominance suggests an aetiologv other than ulcerative colitis for muchitis. margaret balsltis. yah mahida the wide family of cell adhesion molecules (including the subgroups of the immunoglobulin supergene family. the integnn receptors andtheselectins) are involved in controlling interactions between endothella cells and leucacytes !n inflammatory states. this is partly by their influence on adhesion and migration of leucacytes to and through endothellurn. using monoclonal antibodies, we have compared expr~ss~on of the three cell adhesion molecules icam-t (interceiiular adhesion molecule-1). elam-t lendothelial leucocyte adhesion molecule-t and vcam-1 (vascular cell adhesion molecule-t) ~n normal colonic mucosa with muwsa from cases of inflammatory bowel disease. wehavefoundexpressianafthese threemoleculesto beincreased~ninflammatarybaweldiseaseandthis change involvesendothelial cells as well asleucocytes we will dixussthbrelationship between adhesion molecule expression and dlsease actlvlty and posslble therapeutic implications granulomatous enterocolitis associated with therapeutic irradiation 0.6. mangham. k m newbold, s dover the universty of bmmgham department of palhology, sci3ool of m&mi science the medrcal schwl, edggbaslon. chronic radiation-induced entero~olitis 1s a weli recognised complication of radiotherapy for mtra-abdominal or pelvbcmalignancy. the pathological features includepwforatlon. fistula formation. segmental necros~s. and stncture formation. the histologicalfeaturesareessentially lxhaamic in nature. consequent upon the characteristic vascular damage. two case5 of inadtation-induced granulomatous enterocolltis are described ~n which non-caseating epithelcoid granulomas were present ~n the bowel well. to our knowledge. granulomas have not been previously &="bed in radiation coldisor any other formof ixhaemic bowel disease thsgranulomaswere largely confined to the mmosz-associated lymphoid tissue and the draining lymph nodes. naked submucosal granulomas were, however atso present. this distribution is similar to that seen m crohn's disease and tuberculosis. no evidence of these, or any othersystem!c ~r a n " l~r n a t~~~~~n d i t l~n~ was present these cases suppon theview that granulomas in bowel disease are secondary to an tmpaired muwsal bamer to antigens and highlight the non-specifiaty of granulomas m the diaynoscs of inflammatozy bowel diseases between 1 and 5% of crohn's disease patients have involvement of the upper gastrointestlna1 tract the identification of granulomata is normally required to make a specific diagnosts but this may be dinicult in small endoscopic biopsies. we present t o cases where there was a strong suggestion of upper gastrolntestinal crohn's disease with a definitive diagnosis established on more distal invoivbment. four of the biopsies contained granulomata. the remaindershowedeitherpatchy inflammation, local ulceration orvillo~s dtjtmtlon only in aneffort to establish whether crohn's disease biopsies contained specific macrophage or lymphoid populations we applied the~onoclonal antibodies. mt1 (cd43). uchll (cd45ro)). muramidass. mac 387, alpha-1 antltwsin and kpt (cdg8) using immunohistochemistry. theresuns were compared with 6 casesot "on-specific duodenitis orlelunltis crypt-restricted loss of g6pd activity has been used to quantify carcinogen-induced somatic mutation of the xsamples of peripheral nerve (sciatic nerve) of mice from varylng age groups were examlned over the past 8 years. development olage~related penpheral neivefibredegeneraflon was observed among mlce over 18 months age. the spontaneous peripheral nauropathy was characterized by walierlan type degeneratlon. teased nerve flbres from mice of 2 years old showed evidence of swelling of the myelin sheath. fragmentation d myelin into myelin balls or ovoids, with areas of segmental demyellnatlon. light microscopic examination of h 8 e stained sections revealed axonal degeneration, and myelin fragmentation. with vawolation of nerve fibres. on ultrastructural studies. there was evidence of axa-myelin degeneration. axxoplasm showing dark stained bodles suggemng of degenerate mitochondria the myelin sheath a l~o showed disorganization and fragmentation 01 myelin, sometimes with whorl lormatron rithcm the cyroplasm of schwann cetk, wtth evidence of autophagocytosis by schwann ceiis. in some inslancestherawere sgnsofproliferation at schwann cells. nervefibredegeneration affected both non-myelinated and myelmated fibres generally, therewereapparentlygreaternumbers 0fdegeneratenan-myelinated nerrefibres than myelmated nerve fibres. furthermore the numben of degenerate myelinat& nerve fibres were less than in seontaneous peripheral neuopathy in ageing rats (personal obsenat1on) swntaneous peripheral neuropathy of sciat,cnenesmainlyappearedin miceaged 18 manlhsormore, 1s5eenonlvvelyr2rely in mlceof 6 months. younger mice did not show any evidence of this change age-related penpheral nelimpathy is not usually accornpan~~d by any clln,cal 5,gns neur~.9fhology. uhversrty ofiowa, iowa. u s a v~scuiarendothellalcclls(rn)conslitufet~elntertace betweenthe bloodstreamand thetcsske5and pertoormsevetal key roles ~n the development 01 immune and inflammatory responses endothellal cell5 from the braln display slgnlflcantly different momhoiogy from other en. having ilght ]unctlons between them and 2 pauclty at micropinacytolic ves~cles dunng inflammatory conditions of the cns interaction between mlammataly cells and rbb en 8s an initial important event. it 1s known that expression of several adhesion molecules on b r m en is upregulated !n intlammatorycondtti~ns and cytokine-induction ofthese molecules has been investigated however an ~mparlanl mechanism of adheson molecule induction and hence modulation of tmflammatq cell/en binding might beviral infect8onofbrainen wehaveexamined theabilityofmeaslesvirus(human2)andherpes 1 simplex virus to infect cerebral endothelial cells. adhesion of syngenelc splenocytes to both vlrally-infected and mock infected cells was determined using a chromiums1 assay. by 48h of infection with measles yins, cytopathic effect was eadent. and splenocyte adherence was increased to a mean of 138% of the control mock-infected aner 24h mock-infecled expression of the adhesion molecules meca-325 and mala-lon virally-infected cells was determined possible mechanisms for enhancement of adhesion will be discussed and subsequent implications of virus inlectiun of cerebral en ~n relation to homing of inflammatory cells into the brain. ultrastructulal dbsenamns were made on the mechanism and route of innanmatory cell diapedesis through cerebral vessel walls in an experimental model of can~ned~stempervlrusencephalamyel~t~s ~n the hamster migrating monocyies and lymphacyiesextended pseudopodiawhich contacted, indented and adhwedtoendothelwm. they lhen invaded the endnthel12l cells. becoming enveloped by endothelial cytoplasmic processes which re-establishec the continuity of the vascular lining as the migrating cell passed through although mlgratlng cells were frequently seen close to intei endotreiml junctions. they were ever seen wlthln iprctlons. or between adlacent endothelial cellsand therewas noev!denceof opening of mterendothelial tlghtpnmons aherpasslng through the endothel~al layer. cells squeezed through small pores (migration porest in the t h r sub-endothellal basal lamina me present study confirms and extends previous observations on the operation u;#thr the cns of a trans-endothel~al. paraiunclianal route for d8apedesis of mflammatary cells. ireland falbology royal viclona hospital, bcl/asl hi 12 6bl lrrlnrld a sewice for the blochemtcal dlagnosts of lysosamd 8torpge diseases has now been o n operalaon m betlast forslx y n a r~ it currently lids assays available for the measurement 01 16 lysasamal acid hydrolases in plasma. serum. lkwcocvtes. cultured sk8nfibroblasts. amnioticfluld and cultured amniatlccellstordlagnos~s of 20 lysosomalstorage diaurders solar 250 patients have been referred from throughout ireland wtth 53 having a positive diagnosis of these. 18 were diagnosed as being hamozygous for a specific lysosomal enzyme deficiency, 6 were identified as having multiple enzyme acl~ciencies (mucolipidosis type 1111-cell disease) and 29 had heterozygote (carrier) enzyme ibvpis 01 t t v latier. 28 w~i e either parents (obligate hetemrygotes) or siblings of homozygotes and one was a heterozyquti' lor x~lirlhrll recessively inherited fabry's disease. in addttlon. prenatal diagnosis has been performed on 11 motherswithafam,iy hi~toryofi-celldiseaseand/orhurler'ssyndmme.oneofthesepmvedto bepositivefor huller 9 tht' resuiic 01 the biochemical investigations of these cases are presented. high levels of circulating immunoglobulins are common ~n liver dlsbase. in alcohol8c hver disease depos1s of 8mmunaglobullna(lga) have been found in the liver and therenal mesanglum, and werepart acaseof a3oyearoldfemale with a2year history of cardiomyopathy and progressivemuscle weakness anerthe birth of her baby shewas subsequentlyflnedwith apacemaker. clin~cally, therewas sevweweaknessof neck flexors with proximodistal weakness tn both arms and mild weakness of htp flexors. the most stnking weaknesswasin herbreathmg muscles therewas no ptosisorfaaal weakness rellexeswere symmetrical and her plantarswere flexor herckwas normal. aquadriceps musclebiopsy revealed abnormal vanatcon o n fibre diameters affecting bothflbrelypes. occasional pink hyalme ~nclus~ons which stainedforacid phosphataseand wlth pas wwe seen i~i both fibre types electron microscopy showed these i n~l~s i o n~ to cwtsist of aggregates 01 10 nm diameter filamentaenmeshedwithinacentral coreofdenseamorphousmatenal. inotherareastheamorphausmatsnal layas inegutar patches within !he sarcoplasrn mainly at the level of the "z" tine causing disintegration of the sacomere immunoelection microscopy wing collmdai gold showed that the denseamorphous material reacted slrongiyw21 days in ovo and from 3 day hatchlings readily lorm bath fibroblastic and cartilage colonies in vitro. cells within the cartilage colonies are polygonai in morphology, are separated by a relradile exhaceiiuiar matrix and svnthesise catilage specific pmeogiycans and collagens. as shown histochemicelly, biochemically and immunocytochemically. in contrast, adult chicken bone manow does not form cartilage. instead, the cells appear osteoblast-like and synthesise coilagens typical of bone. a. m. fianagan t. j. chambers &wtmment of h~slopatholosy. sl george's hosptal medlcel sch-i, london. sw17 ore osteaclastshavebeensuccessfullygeneratedinculturesofmurinehaemopoisticcells. itwouldbeuseful ifasmila, model were available to analyse the mechanisms of regulatlm of human mteaclast formaim ir normal and pathological states. although the osteoclast is present in reverai neoplastic conditions. it is not known whether it forms part of other haemowietic malignancies, lor example, polycythaemia rubra "era or chrmic lymphatic leuhemia. we used strategies based on our experience with murine osteoclastogenesis. however, we have been unabletogeneratefunctional human osteoclastscapableoiresorbingbone m vrtro. large numbersofmultinucleate cells developed in these cultures mese cells did not show a typical panem of reactivity with asteociast-specific manoclonal antibodies, nor did they bind '251sct but rath@r possessed an antigenic profile characteristic of macmphage polykaryons. it is pecullarthat human tissue fails to support osteoclast generation stnce cells of the other haemopoietic lineages were consistently generated in our cuitures. in murine cunuras it is known that a particular shomal cell type is requtred for osteoclastagen@sis; it is possible therefore that this cell population is spamin adult humantissue.miswouldreflecttheiownumberofosteoc1asts presentinhuman adults comparedto mice elucidation of conditionssuitableforthe generation mthehuman osleoclastm wtrow~ll heldus understand the mechanisms by which it is regulated in health and disease spaceof one year. the other case 1s b middie-agedwoman who &=being affected bythe disease far sevaral years developed separate sarcomas in each lower limb dunng a nine month pwiod. each tumour was treated bv pamal amputation but she died from widespread metastases within one year of the first amputationthe distribution of proline-4-hydroxylase in a range of human tissues shown by a monoclonal antibody, fib 585 s. smlth, p. revell aepariment of mobd anatomy and bone and h m f research unrt, the london hospw medcal cdl€ge, london. e l fib 505. a commercially available monoclonal antibady to the b subunit at the enzyme proiine-4-hydroxyla~ invalved~ntheproductionofcallagen, wasappl'edtaacetonebxedcryostat sect~onsofawiderangeoftissues. in hver, hspatocytesshowedvarying degrsesof labelling with the antibody, along with spindle shapedcells(sscs) in associated connective tissue in both tonsil and lymph node. sscs in the connective tissue were melled with the antibody along with a number of other cells (lymphocytes) within the germinal centres. in addition to this. perivascularcellsand cells intheconnectivetissue iayerimmediatelybelowtheepithelium also labeliedin sections of tonsil. in skin, very few cells in the dermis were positive for pm11ne-4-hydroxylase. as were also only a small numbetof epidermal cells. afew chondrocyteswere marked bythisantibody in artlcularcartilageand intervertebral disc,along withswneostwcytesin bone.manycellsinthepleuraandtheepimysiumof normal~keletalmusclew~e posotive. there was no staining at all in specimens of kidney. in addition to these 'normar tissues, examples of a seminoma, a breast carcinoma and a thymoma were examined. each of the turnours showed fib 585 labeliiw of ssc~withinthestromalt~ssue.theseresultsshowthat fib5b5sele~tivelylabelssscs.whlcharapresumedto be f8brobiasts. in a wide ranged1 both normal and pathological tissues. which produce and maintaln the collagen matnx. proime-4-hydoxylase is an enzyme involved in the pmduction of collagen and demonshahle in the rer of fibroblasts. it may therefore be cmsldered as a possible matker for fibroblasts in tissue sections. we have applied the mouse moncclonal antlbdy fib 505, raised against the $ subunn of prol1ne-4-hydroxylase. to alcohol fixed paramn embeddedsections and acetonefixedcryostat sect~onsolnormal (n = 4) and meumatoid (n = 30) synovia. synoviocytes labelled very strongly, but the distribution vaned between samples. insome, mostsynoviocytes weremahed, whilein others ~nlythedeepiayerofcells wasmitive. it isnot known whether thts dillerence ~n prdine-4-hydroxylase expression is due to the severity and duration of disease. drug treatment or other factors. it is of interest, however, that fib 505 labelling was not wnflned to the type b (fibroblast-llke) synoviocytes and that the more supficlal type a synoviocytes also contained proline-4hydroxylase. spindleshapsdeells i" thesublntlmaleonnectiva tissue were labelledma vanablemanner. inaddltlm to these findings for fibroblastic cells. a small cap of fib 505 posnive cells was seen around lymphoidfollicles. sometimes polansed towards the synovial surface. this enzyme expression by lymphocytes is under further invsstlgatlo". vitronectin 1s an adhesive glycoprotein which shares several functional similarities with fibronectin. it is a major component of extracellular matnx and plays a role in cell-matrix mteradians, monocyte function. and the coagulation and wmplement systems. we have employed a monoclonal antibody to assess the distribution of vironectin in frozen synovial biopsies from patients with rheumatoid arthntis, ostwnhntis. ankylosing spmdyiitis andtraumatic non-inflammato~ control^ (49 cases). lmmunoreactive vltronectin was identified in the synovium. similarto the panem of immunoreactiyefibronectin, itwas located in adensefibrillarpanem surrounding cellsof the synovial lining layer. vitronectin was also associated with fibres throughoutthe sub-intimal connective tissues. being most prolific in fibrotic areas. vltronectin was identified in the sub-endothellal layen of blood vessels. but unlike fibronecttn 11 was not associated with basement membranes. similar distributlon patterns wme observed in all biopsies studied thelocalisation ofvitronectitin in synovial tissues suggestsapossibleroie inanachmmtofcellsto the extracellular matrix and that 11 may be important in the pathophysiology of inflammation and repair manolayercultured articularchondrocytesare known to rapidly losethelrexpressionof collagen typeil.the purpose of this study was to compare the expression of various collagen types in twoand three-dimensional cultures 01 articular chandracytes. in addition. the expression of s-1w protein and its alpha and beta subunits was studied in monolayer cui1ures. bavine articular chondrocytes were isolated by collagenase digestion from ankle joints and cuhured in monolayerandspheroid culturesin dmemwim 10% fcs lmmunocytochemical studieswere performed using the indirect peroxidase technique an monolayers affer methanollethanol (1 1 vlv) fixation and on frozen sections of spheroids. the reaction was scored semi-quantitatively as negative (-), weakly (+) moderately (++) ontha basisofthenumbersafcasesrefsiredtoustottheidentificalionofjointcry~talsintissuesectians, webelieve that calcium pyraphosphatedihydrate(cppd) deposnion disease isbeing underdiagnosed byhistopathologists. a crltical light microscopic reviewof 18cases. all with thediagnosisconfimed bymicroanalysis(energydispersivexrayspectroscopyln thescanning electron microscope, infrared spectroscapywboth) revealed adistinctwefeathery or br"shlikeappearanceinal1suchdeposits.thisfeaturewasapparentat lowpower, whileconvincingvisualisation of crystalswithinthedepositswasdiff~cuneven withanoil immersionobiective.thesignof birehingeneeof cppd crystals is more dificult to demonnrate i" tissue sections than synoviai fluids. due to iactois such as stain. fragmentation and heaping up of crystals, buf it can be more readily assessed in unstained sections or following microincineration of the section. in six of our c a m the deposits were exclusively within bone: demonstration depended on relatiyeunderdecalcification: deposits in this position have not previously been recognised. this study thus provides new information an the histological identdication of cppd deposns in tisues and implies heterogeneity in the pathogenesis of such deposits. in human knee osteoarthrosis (oa) overt unicornpartmental disease is frequently accompanied by a macroscopically normal second cornpartmsm. however. there are a number of light micmscopical changes within the latter which might amount to an "early osteoarthrosis". these are chondrocyte pmliferation and chondrone formation. decreased proteoglycan staining and disruption of the chandra-osseous interface with duplication of the tidemark and resorption ofthe cartilage by chondmclasts. tidemark duplication is also a feature of established oa re~resenti~gadistu~ancedfcabif~cat~oninrone5ofarticularcartilage.slnceslwp~~t~i~~~~ knowncalciumion transponmoleculs.altsrationm~~sstainingpanernand~ntens~tym~grn beanlndexotearlyo~. sl~~protemstamng was studied in the tiblai plateau cartdage of 31 cases: 12 with unicornpartmental oa. 11 with bicompartmental oa and8 controls. lntheianerall chondrocytesgavepositivemembrana and cytoplasmic staining (especially in zones 2 e n d 3 ) , d~u s e w e a k m a t~~c~l s t~~~~~g~~~~~e l , s t~o~g p a r i c e l l~i a~a~d~~t~~-t~~t o~~l s t~i~~~g~~~o~~s 4 a~d 5 . in overt and early oa the orderly malrlcal panem was disrupted with prominent patchy staining around chondrocyte clusters. the significance of the change in the matncal distribution ~n oa is unknown and unlikely lo be related to a disturbance of calcification in zone 5. road, london. wcl m e histogenesis at alveolar son part sarcoma (asps) is still unsenled: nonchromaffin paraganglioma. malignant granular cell myoblastoma, neuml tumour, myogenic tumour. habdomyosarcoma and renin-producing tumoui theories have been proposed lmmunohistochemical studies have yielded discrepant results we recentlyobsewed that the diastase resistant crystalline material in asps was strikingly reactive for vimentin by the immunoperoxidase method on paraffh sections 01 one case. we then studied paraffin sections of seven other cases from our files between 1980 and 1991 ~ by routine light microscopy, immunohistochemistry and electron microscopy all eight cases were reactlve for vimentin. which highlighted the crystalline materlal as in the first case. vanabie numbers of immunoreactlve cells for desmin were found in three. and smooth muscle specific actin in four. all cases showed some reactivity for neuron specific enolase. and seven of the eight cases reacted for s-100 protein. the clinical and pathological lea lure^ of 20 cases of synoviai sarcoma have been reviewed. these tumours are aggressive with a poor prognosis. typically affecting young aduns with a long history before presentation and detinltive diagnosis. a high index of suspicion is required if the diagnosis is not to be missed several features, including age, size. site. histological type (monophasicibiphasic), mitotic actlvity and necms~s have been investigated withaview toestablishing possible prognosticindicators. the bestguideto prognosisis assessment 01 mitotic actlvity. size and histological type dld not affen the outcome. in this study the effecl of subcapsular orchidectomy on skeletal metastases from prostatic carcinoma was studied using bone histomorphomatnc paramsten. twenty-eight patients with bone metastases were studied immediately before and for seven months after orchidectomy. tetracycline labelled bone biopsies were taken from metastases and turnour free areas at the beginning and end of study. sixteen of the 28 patients also underwent o~teocla~t inhibition tor six months using disodium pamidronate (30 mg i.v. weekly for 4 weeks then anemale weekly for five months) to enable differentiation of the skeletal response to castration. histamarphametnc anslysi~ 01 tumour frse bonerevealed adrapin overall bonevolume. histological analysisofmetastasesshawedadecrease m osteoblastic activity but widespread osteoclast mediated ostealysis. tumour regression and manow recolonisation were present in most c~s b s but malignant foci remained in 56% of repeat metastatic biopsies, inducing a typical. lacalised disruption of bone metabolism. it is concluded that orchidectomy causes ostmblastic regression blrt induces increased ostboclast mediated bone destruction, which is most pronounced within metastases. although tumour regression and marrow recolonisation usually occur within metastases, active turnour foci anen perstsf. ( 11) chairman s. g. silverberg, washington theeffectsafoncogeneson thedeveloping nelvoussystem havebeenstudiedinaneuraltransplant system ~ntats, taking advantage of the extraordinary capacity of fetal cns to differentiate in and fully integrate with, the adult host brain. gene transfer tnto tetal brain cells was mediated by in viiro infection with replication-defsctwe retroviral vectors. fetal rat brain suspensions were then stermtaxically injected into the caudoputamen of adult f344 rats.animals carrying transplants exposed in vim lo the polyoma medium tantigen developed endothellal hemangiomas in the graft which often led to fatal cerebral hemorrhage within 13-50 days alter transplantatm lntroductm of the viral sic gene caused astrocytic and mesenchymai tumors affer latency periods of 2 4 months.following infection of fetal donor cells with a vector encoding the v-myc oncogene led to the development of only a single embryonal cns tumor whereas exposure to v-ha-ras and v-myc resulted in the rapbd induction of multiple malignant neoplasms. when injected intracerebrallyinto newborn ratsin vivo, complementation of theseongogenes led 10 the development of malignant hemangioendotheliomas, undinerentiated neural tumors andlor leukmia.oncogene transferthus constitutes a challenging new model to assess the effects of translorm~ng genes on the developing nervous system. since the presentahon of molecular genetic evidence supporting the knudson hypothesis m the eariy 1980s there hasbeen increasing interestinthe ideathatasimilartwo-hit mechanism mayaperateln sporadadlccancers therens now evidencbthatlassofonealleleandretentionottheother~nmutated/wildfarmaccuninsparad~ccalono. lung. renal and breast cancers in breast cancer lossof heterorygoslty(l0h) has been demanstratedfarseveral alleleson chromosomes 1 l p 13q and an the short arm of chromosome 17. loh has also been demonstrated on other chromosomes thegeneral viewisthat loh indicatesthatasuppressorgene may bepresentattheseloct. hawevet in interpreting lohthere 1sdifficulty indetermining when loh becomessignificant because itsincidencevariesfrom 1%700/0 depending on the locus examined. in this presentation, knowledge about loh on chromosome 11 p (and 11 q where a new deletion has been recently discovered), and 17p will be presented and the pathqlenetic significanceand ciinicsl relevanceexamined. lnthe lattercontext anewrapid methodfordetemlnmg alleljc dosage will a l x be described which does not requlre rflp analysis. expelt systems -1.e. computer software that can function as cansuhant, decision support system, or process contr~llerhas undergone a rapid development durlng the past decade. applications to histopathology have gnaw some 2,ocqdiffuse maiignantmesotheliomas(0mm) occurannuailymn. americaat thepresenttime.cumulat~~ely, substantial numbersot lesser-knownfarms of mesothelia1 turnourare also seen, including serous paptllary tumoun of the peritoneum, well differentiatedpapillarymesothellomas and benign cystic mesotheliomas, but incidencedata are not available.the relativeiyfrequent atypical reactive hyperplmasof w o s a membrane add further vanstytothe range of mesothellai lesions which may present diagnostic problems. the expenence of a u.s.-canadian mesotheliomapanel suggests that dmm vs. metastatic carcinomacontinues to bethe commonest mesatheliamarelateddiagnostieehaliengeandthatthedifficunyandalwayssolved bytheappiicationofspecialstains almostas common are le~ions in which the ditferential diagnosiscenters on dmm us. a reactive process (atypicai mesotheliai hyperplasia, fibrous pleurisy) within the laner group it is particulady difflcun lo obtain a strong consensus opinion, andfoilaw-uphasconfirmedthemaiorityopinioninonly69%ofcases. sarcomatousdmmvs.sarcomanosisaiso a notable area of difficuny. most mesothelial lesions tn north amenca. including dmm. are reviewed within a short time of biopsy by a pathologist in a major teaching centre, only a small number (5-10%) being subpct to further scrutiny by a panel or ~n the coune of epidemiological or clinical studies however, many cases resurface later ~n a legal sening when the material and clinl~al information 1s often available. the original diagnosis of the hosoital pathologist 1s usually endaned by the courts. sharon w. weiss llposarcoma is one of the most common forms of son tissue sarcoma and may be divided into several subwes well-differentiated. myxoid. round cali, phmwpha, and dedifferentiated. this presentation will discuss the 1) diagnosticcnteriaof lipblasts2) d8agnosisand behaviorof myxoidround cell iiposarcoma andthe3) behavior and incidence of "dedifferentiation" dwell-differentiated ihposarcoma. the diagnosis of lipsarcoma depends in part on the identdication of lipoblasts or pnmitive fat ceils. since iipoblast-l!ke cdls may be seen m a variety of conditions apart from iiposarcoma, strict diagnostic c!i tma must be applied in identlfving these ceiis. these cells contain a hyperchromatic. indented or scalloped, ecmtnc nucleus set in a cytoplasm containing one or more lipid-nch vacudes. these cells must also occur in an appropriate histaiqic background. vanous lesions which may contain ihpoblast-like cells and which may. therefore, mimic liposarcoma include fat necrosis, fat atrophy, silicone granuloma, signet nng carcinomas or melanomas, and a variety of malignant tumors with fixation artifact. myxold androundcell lipsarcomarepresentthemost commanfarmofsarcomaaccuningmearlytamidadunlifeandare commoniy located #n the region of the mlgh and popitteal fossa. although the designation of "myxold and "raund cely suggest two separateturnortypes. they represnt ends d a common h~stologlcspbctnm. myxaid liposeicoma represents the well differentiated end of the spenrum. whereas round cell represents the pcarly differentiated end.however, transitional or mixed forms ex~st. accounting for confusion as to how such tumors should be classlfled mymd liposarcomas are characterized by nodules of bland stellate or rounded cells set 8 n hyaiuronic aod-rich strama. an intricate plexiform vasculature and numerous lipblasts are easily vdentaed. wlth progression to round celliiposarcomathecellsbecomelarger,moreatypicalandthestromalessmyxaid. lipoblastsaremoredlfticultto find and a plexiform vasculature 1s less apparent. recent work by evans suggests that evaluatlon of myxoidlfound cell ihpasarcomashould includethe percentage of round cell component wdhin atumorsincethisdirectclh/ mtluences prognosis. our policy is to carefully sampk such tmors, submining t section for each centimeter in greatest diameter of the tumor. a rough estimate of the percentage of a round cell component 1s made. we w a r d tumors havinglessthan 1010faroundcellcomponentasgradei.thosehav,ngbetween 1&25% roundcelicomdonent are considered grade 11. whereas those with more than 25% are considered grade 111. well dmerentiated liposarcoma is one of the most common sarcomas accuning m late adult life. characteristically affecting the deep musclesaftheextremities, theretropentonealspace. and the groin, this tumor ischaractenzed by varying amounts of mature fat interspersed with fibrous bands, atypical hyperchromaric spmdledceiis, and lipoblasts. these lesions are considered low grade sarcomas having a high rate of local recurrence but no abilny to metastaslze. recently evans and ammi eial suggested that well-differentiated liposarcomas occurring m the wbcutaneous tissue and muxles of the extremity cause so hnle morbidity that the use of the term "atypical lipma" should be used rather than ihposarcoma. in contrast. well-differentiated liposarcomas in the retropentoneum cause significant morbidihl and pose a significant risk of death from local disease. thus. nearly all pathologists agree that the term "weii differentiated lipasarcoma" should be retained for these tumors ~n the retroperitoneum. however. none of these recent studies have followed a large number of these tumors for a proianged period at time m order to assess the long term behavior and specihcalty risk that such 1es1ons may progresswith time to a higher grade lesions (1.9 dedifferentiate). we have recently completed a follow-up study of 98 cases of well ditferentiated iiposarcoma accurringmthemusc~oftheextremity,retropntoneum,andgroin. inalllmatlonsthenskof local recurrence was high. however,dedifferentiationoccurred~n 33% of casesandwasnotrestnnedtotumors~nanyparticularlacatlon. butcouldbe bestconelatedwiththedurationofthetumor. withmostcasesoccun~ngaflerl0mmoreyean thus. dedifferentiation is not a site-dependent phenomenon, as has previously been suggested. but rather a time dependentphenomenon.anhough thesedatado notneee~~arily indicatethatwe should abandon theterm"atwca1 itpoma" they do indicate the need tor proianged foilow-up of patients wlth wei&-dlfferent,ated ddosarcoma and the small but deflnne risk of dedifferentiation as a long term complication of the disease. key: cord-335382-fk4um9nw authors: farver, carol f.; zander, dani s. title: molecular basis of pulmonary disease date: 2012-08-10 journal: molecular pathology doi: 10.1016/b978-0-12-374419-7.00018-4 sha: doc_id: 335382 cord_uid: fk4um9nw pulmonary pathology includes a large spectrum of both neoplastic and non-neoplastic diseases that affect the lung. many of these are a result of the unusual relationship of the lung with the outside world. every breath that a human takes brings the outside world into the body in the form of infectious agents, organic and inorganic particles, and noxious agents of all types. although the lung has many defense mechanisms to protect itself from these insults, these are not infallible; therefore, lung pathology arises. damage to the lung is particularly important given the role of the lung in the survival of the organism. any impairment of lung function has widespread effects throughout the body, since all organs depend on the lungs for the oxygen they need. pulmonary pathology catalogs the changes in the lung tissues and the mechanisms through which these occur. this chapter presents a review of lung pathology and the current state of knowledge about the pathogenesis of each disease. it suggests that a clear understanding of both morphology and mechanism is required for the development of new therapies and preventive measures. pulmonary pathology includes a large spectrum of both neoplastic and non-neoplastic diseases that affect the lung. many of these are a result of the unusual relationship of the lung with the outside world. every breath that a human takes brings the outside world into the body in the form of infectious agents, organic and inorganic particles, and noxious agents of all types. although the lung has many defense mechanisms to protect itself from these insults, these are not infallible and so lung pathology arises. damage to the lung is particularly important given the role of the lung in the survival of the organism. any impairment of lung function has widespread effects throughout the body, since all organs depend on the lungs for the oxygen they need. pulmonary pathology catalogs the changes in the lung tissues and the mechanisms through which these occur. what follows is a review of lung pathology and the current state of knowledge about the pathogenesis of each disease. we believe that a clear understanding of both morphology and mechanism is required for the development of new therapies and preventive measures. lung cancer is a major cause of morbidity and mortality throughout the world. the most recent estimates available from the surveillance, epidemiology, and end results (seer) program of the national cancer institute are that in 2007 over 213,000 people in the united states were diagnosed with cancer of the lung and bronchus, and over 160,000 will have died due to this disease [1] . however, in the past decade incidence and mortality rates have begun to move in a more positive direction, particularly in men. overall, men show a decline in lung cancer incidence, while in women, although lung cancer rates grew from 1975 through 1998, they stabilized from 1998 through 2004 [2] . similarly, cancer death rates due to lung cancer have declined for men and have slowed for women. although, for women, lung cancer death rates have increased since 1975, the rate of increase has slowed to 0.2% annually from 1995 to 2004 [2] . these trends parallel changes in the prevalence of tobacco smoking, the most important risk factor for development of lung cancer. given the tremendous societal and individual impacts of this disease, it is not surprising that the molecular biology of lung cancer is a major focus of investigation. elucidation of the molecular pathogenesis of these neoplasms has progressed significantly, offering insights into new, targeted therapies, and predictors of prognosis and therapeutic responsiveness. recognition of precursor lesions for some types of lung cancers has been facilitated by our expanded understanding of early molecular changes involved in carcinogenesis. the world health organization (who) classification scheme is the most widely used system for classification of these neoplasms (table 18 .1) [3] . although there are numerous histologic types and subtypes of lung cancers, most of the common malignant epithelial tumors can be grouped into the categories of nonsmall cell lung cancers (nsclcs) and small cell carcinomas (sclcs). nsclcs include adenocarcinomas (acs), squamous cell carcinomas (sqccs), large cell carcinomas, adenosquamous carcinomas, and sarcomatoid carcinomas. sclcs include cases of pure and combined small cell carcinoma. common pulmonary symptoms associated with these tumors include cough, shortness of breath, chest pain or tightness, and hemoptysis (coughing up blood). since some tumors cause airway obstruction, they predispose to pneumonia, which can be an important clue to the existence of a tumor in some patients. constitutional symptoms can include fever, weight loss, and malaise. some neoplasms will declare themselves with symptoms related to local invasion of adjacent structures such as chest wall, nerves, superior vena cava, esophagus, or heart. sclcs are known for early and widespread metastasis and are therefore particularly prone to being discovered through presentations as metastases in distant sites. some tumors are discovered due to pathophysiologic changes triggered by the release of soluble substances from tumor cells. endocrine syndromes due to elaboration of hormones are well recognized, and include cushing syndrome, syndrome of inappropriate antidiuretic hormone, hypercalcemia, carcinoid syndrome, gynecomastia, and others. hypercoagulability commonly occurs with lung cancers, leading to manifestations of venous thrombosis, nonbacterial thrombotic endocarditis, and disseminated intravascular coagulation. hematologic changes can include anemia, granulocytosis, eosinophilia, and other abnormalities. other paraneoplastic syndromes such as clubbing of the fingers, myasthenic syndromes, dermatomyositis/polymyositis, and transverse myelitis are noted in subsets of patients. when lung cancer is suspected, evaluation of the patient includes a thorough clinical, radiologic, and laboratory assessment, with collection of tissue or cytology samples to establish a pathologic diagnosis of malignancy and to classify the tumor type. fiberoptic bronchoscopy is often performed to collect samples for diagnosis. sample types can include transbronchial and endobronchial biopsies, bronchial brushings, bronchial washings, bronchoalveolar lavage samples, and transbronchial needle aspirates. submission of sputum samples for cytologic malignant epithelial tumors examination can provide a diagnosis in some cases, particularly for centrally located tumors such as sqcc and sclc. tumors arising in a peripheral location can also be sampled, in many cases, by fine needle aspiration or core needle biopsy performed under radiologic guidance. if a pleural effusion is present in combination with a lung parenchymal tumor, analysis of the pleural fluid cytology often allows one to establish a diagnosis. pleural biopsy, mediastinoscopy with biopsy, and wedge biopsy can also be performed, depending on the clinical and radiologic findings. for tumors with apparent distant metastasis, biopsy of the metastasis focus can both establish a pathologic diagnosis and determine the stage of the tumor. the prognosis of lung cancers is closely related to tumor stage. for nsclcs, the american joint commission on cancer tnm staging system is widely used (table 18. 2) [4] , and for sclcs, disease is classified as limited (restricted to one hemithorax) or extensive. overall, for lung cancers, the 5-year survival is 13.4% for men and 17.9% for women [5] . an important factor leading to this relatively poor survival is the late stage at which many lung cancers are diagnosed. information from the seer database, from 1996-2003, indicates that 16%, 35%, 42%, and 7% of patients were diagnosed with localized, regional, distant, or unstaged disease, respectively [5] . the corresponding 5-year survival rates are 49.0%, 15.3%, 2.8%, and 8.7%, and 10year survival rates are 37.8%, 10.3%, 1.6%, and 5.1% [5] . for patients with nsclcs, treatment depends on stage and comorbid conditions [6] . surgical resection is the preferred approach to treatment of localized nsclcs, provided there is no medical contraindication to operative intervention. lobectomy or more extensive resection (depending on tumor extent) is usually recommended rather than lesser surgeries, unless other comorbid conditions preclude these procedures. tumor 3 cm in greatest dimension, surrounded by lung or visceral pleura, without bronchoscopic evidence of invasion more proximal than the lobar bronchus t2 tumor with any of the following features of size or extent: > 3 cm in greatest dimension, involves main bronchus ! 2 cm distal to the carina, invades visceral pleura, associated with atelectasis or obstructive pneumonitis that extends to the hilar region but does not involve the entire lung t3 tumor of any size that directly invades the chest wall, diaphragm, mediastinal pleura, parietal pericardium; or lies < 2 cm distal to the carina but without involvement of the carina; or is associated with atelectasis or obstructive pneumonitis of the entire lung t4 tumor of any size that invades the mediastinum, heart, great vessels, trachea, esophagus, vertebral body, carina; or has separate tumor nodule(s) in same lobe; or is associated with a malignant pleural effusion. regional lymph nodes (n) nx regional lymph nodes cannot be assessed n0 no regional lymph node metastasis n1 metastasis in ipsilateral peribronchial and/or ipsilateral hilar lymph nodes, including intrapulmonary nodes involved by direct extension of the primary tumor n2 metastasis in ipsilateral mediastinal and/or subcarinal lymph node(s) n3 metastasis in contralateral mediastinal, contralateral hilar, ipsilateral or contralateral scalene or supraclavicular lymph node(s). mx distant metastasis cannot be assessed m0 no distant metastasis m1 distant metastasis; includes separate tumor nodule(s) in a different lobe. occult t0 n0 m0 stage 0 tis n0 m0 stage ia t1 n0 m0 stage ib t2 n0 m0 stage iia t1 n1 m0 stage iib t2 n1 m0 t3 n0 m0 stage iiia t1 n2 m0 t2 n2 m0 t3 n1 m0 t3 n2 m0 stage iiib any t n3 m0 t4 any intraoperative mediastinal lymph node sampling or dissection is also recommended for accurate pathologic staging and determination of therapy. subsets of patients also benefit from chemotherapy and radiotherapy. for more advanced nsclc and for sclc, chemotherapy and radiotherapy are the primary treatment modalities [6] . rare patients with limited-stage sclcs can be considered for surgical resection with curative intent. development of lung cancer occurs with multiple, complex, stepwise genetic and epigenetic changes involving allelic losses, chromosomal instability and imbalance, mutations in tumor suppressor genes (tsgs) and dominant oncogenes, epigenetic gene silencing through promoter hypermethylation, and aberrant expression of genes participating in control of cell proliferation and apoptosis [7] . there are similarities as well as type-specific differences in the molecular alterations between nsclcs and sclcs, and between sqccs and acs [8] [9] [10] . oncogenes that play a part in the pathogenesis of lung cancer include myc, k-ras (predominantly acs), cyclin d1, bcl2, and erbb family genes such as egfr (epidermal growth factor receptor) (predominantly acs) and her2/neu (predominantly acs) [11, 12] . also, lung cancers often display abnormalities involving tsgs including tp53, rb, p16 ink4a , and new candidate tsgs on the short arm of chromosome 3 (dutt1, fhit, rasff1a, fus-1, bap-1) [11, 13] . as research advances, these lists continue to grow, and as knowledge has expanded about the roles of these genes in carcinogenesis and tumor behavior, new targeted therapeutic agents have been designed to treat this disease ( figure 18 .1 and table 18 .3) [14] . many other agents are under investigation. in cancers, chromosomal regions harboring tsgs and oncogenes are often deleted or amplified. allele loss involving loci in 3p14-23 is a consistent feature of lung cancer pathogenesis [15, 16] . wistuba et al. reported allelic losses of 3p, often multiple and discontinuous, in 96% of the lung cancers studied and in 78% of the precursor lesions [15] . larger segments of allelic loss were noted in most sclcs (91%) and sqccs (95%) than in acs (71%) and preneoplastic/preinvasive lesions [15] . there was allelic loss in the 600-kb 3p21.3 deletion region in 77% of the lung cancers; 70% of the normal or reneoplastic/preinvasive lesions associated with lung cancers; and 49% of the normal, mildly abnormal, or preneoplastic/ preinvasive lesions found in smokers without lung cancer, but no loss was seen in the samples from people who had never smoked [15] . 8p21-23 deletions are also frequent and early events in the pathogenesis of lung carcinomas [17] , and other common alterations include loh at 13q, 17q, 18q, and 22p [16] . allelic losses that are more frequent in sqccs than acs include deletions at 17p13 (tp53), 13q14 (rb), 9p21 (p16 ink4a ), 8p21-23, and several regions of 3p [11, 15, 17, 18] . a recent study utilizing a bacterial artificial chromosome array to perform high-resolution whole genome profiling of sqcc and ac cell lines showed that regions of frequent amplification shared by both types of tumors included 5p; chromosome 7, 8q, 11q13, 19q, and 20q; and common regions of deletion included 3p, 4q, 9p, 10p, 10q; chromosome 18; and chromosome 21 [10] . however, acs appeared to have higher frequencies of deletion of chromosome 6; 8p, 9q, 15q; and chromosome 16 than sqccs, and possess small regions of amplification on chromosomes 12 and 14 not seen in sqccs. chromosome arms 2q and 13q were frequently deleted in ac but amplified in sqcc cell lines. both types of tumors showed deletion of chromosome arm 17p, but it was more frequent in the sqcc cell lines, while amplification of chromosome 17p was more frequent in acs. amplification of chromosome 3q was common to both types of tumors but showed frequent alteration at 3q23-3q26 in the sqcc lines and at 3q22 in the ac lines. inactivation of recessive oncogenes is believed to occur through a two-stage process. it has been suggested that the first allelic inactivation occurs, often via a point mutation, and the second allele is later inactivated by a chromosomal deletion, translocation or other alteration such as methylation of the gene promoter region [19] . inactivating mutations in the tsg tp53, which encodes the p53 protein, are the most frequent mutations in lung cancers. these mutations are found in up to 50% of nsclcs and over 70% of sclcs, and are largely attributable to direct dna damage from cigarette smoke carcinogens [20] . tp53 mutational patterns show a prevalence of g to t transversions in 30% of smokers' lung cancers versus only 12% of lung cancers in nonsmokers [20] . p53 protein is a transcription factor and a key regulator of cell cycle progression; cellular signals induced by dna damage, oncogene expression, or other stimuli trigger p53dependent responses including initiating cell cycle arrest, apoptosis, differentiation, and dna repair [21] . loss of p53 function in tumor cells can result in inappropriate progression through the dysregulated cell cycle checkpoints and permits the inappropriate survival of genetically damaged cells [22] . the p16 ink4a -cyclin d1-cdk4-rb pathway, which plays a central role in controlling the g1 to s phase transition of the cell cycle, is another important tumor suppressor pathway that is often disrupted in lung cancers. it interfaces with the p53 pathway through p14 arf and p21 waf/cip1 . thirty percent to 70% of nsclcs contain mutations of p16 ink4a , including homozygous deletion or point mutations and epigenetic alterations, leading to p16 ink4a inactivation [22] . almost 90% of sclcs and smaller numbers of nsclcs, on the other hand, display loss of rb expression [23] , and mutational mechanisms usually responsible include deletion, nonsense mutations, and splicing abnormalities that lead to truncated rb protein [22] . p16 ink4a leads to hypophosphorylation of the rb protein, which causes arrest of cells in the g1 phase. the active, hypophosphorylated form of rb regulates other cellular proteins including the transcription factors e2f1, e2f2, and e2f3, which are essential for progression through the g1/s phase transition. loss of p16 ink4a protein or increased complexes of cyclin d-cdk4-6 or cyclin e-cdk2 lead to hyperphosphorylation of rb with resultant evasion of cell cycle arrest and progression into s phase [21, 23] . cell cycle progression is inhibited by p21 waf/cip1 through its inhibition of the cyclin complexes. the 10%-30% of nsclcs lacking detectable alterations in p16 ink4a and rb may have abnormalities of cyclin d1 and cdk4, which cause inactivation of the rb pathway [22] . figure 18 .2 provides an overview of the p53 and retinoblastoma (rb) pathways, showing the complex interactions between the components [21] . epigenetic alterations (hypermethylation of the 5 0 cpg island) of tsgs are also frequent occurrences during pulmonary carcinogenesis, and methylation profiles of nsclcs show relationships to smoke exposure, histologic type, and geography. methylation rates of p16 ink4a and apc and the mean methylation index (mi) (a reflection of the overall methylation status) in current or former smokers were significantly higher than in never smokers; the mean mi of tumors was highest in current smokers; methylation rates of apc, cdh13, and rarbeta were significantly higher in acs than in sqccs; methylation rates of mgmt and gstp1 in cases from the united states and australia significantly exceeded those from japanese and taiwanese cases; and no significant gender-related differences in methylation patterns were found [24] . proto-oncogene activation and growth factor signaling are important in pulmonary carcinogenesis. the tyrosine kinase epidermal growth factor receptor (egfr) is frequently mutated in nsclcs, particularly in acs, and the mutational status is important in determining response to tyrosine kinase inhibitors. a related pathway, the phosphoinositide 3-kinase (pi3k)/akt/mammalian target of rapamycin (mtor) pathway, is frequently deregulated in pulmonary carcinogenesis. as reviewed by marinov et al., this pathway has been reported to mediate the effects of several tyrosine kinase receptors, including egfr, c-met, c-kit, and igf-ir, on proliferation and survival in nsclc and sclc [25] . clinical trials are ongoing, investigating the efficacy of the mtor inhibitor rapamycin and its analogues on lung cancer [26] . her2/neu is another related receptor tyrosine kinase that is upregulated in approximately 20%-30% of nsclcs [27, 28] , but unlike the situation with her2/neu-positive breast cancers, treatment with anti-her2/neu antibody (trastuzumab) does not seem to yield comparable benefits for nsclc when used alone or in combination with chemotherapy [28, 29] . point mutations of ras family proto-oncogenes (most often at k-ras codons 12, 13, or 61) are detected in 20%-30% of lung acs and 15%-50% of all nsclcs [22] . although farnesyl transferase inhibitors prevent ras signaling, these agents have not shown significant activity as single-agent therapy in untreated nsclc or relapsed sclc [30] . myc family genes (myc, mycn, and mycl), which play roles in cell cycle regulation, proliferation, and dna synthesis, are more frequently activated in sclcs than in nsclcs, either by gene amplification or by transcriptional dysregulation [22] . vascular endothelial growth factor (vegf) is a homodimeric glycoprotein that is overexpressed in many lung cancers and directly stimulates endothelial cell proliferation, promotes endothelial cell survival in newly formed vessels, and induces proteases involved in the degradation of the extracellular matrix needed for endothelial cell migration [31] . its angiogenic effects are mediated by three receptors: vegfr-1, vegfr-2, and vegfr-3; ligand binding leads to tyrosine kinase activation and activation of the signaling pathways required for angiogenesis [31] . monoclonal antibodies to vegf (bevacizumab) and tyrosine kinase inhibitors to vegfrs have been developed and show promise for treatment of nsclc. a phase iii trial of bevacizumab showed significantly improved overall and progression-free survival when this agent was used in combination with standard first-line chemotherapy in patients with advanced nsclc, and several smallmolecule vegfr tyrosine kinase inhibitors have yielded favorable results in phase i and ii trials in nsclc [32] . micrornas are a recently discovered class of nonprotein-coding, endogenous, small rnas which regulate gene expression by translational repression, mrna cleavage, and mrna decay initiated by mirna-guided rapid deadenylation [33] . some micrornas such as let-7 have been suggested to play roles in carcinogenesis by functioning as oncogenes or tumor suppressors, negatively regulating tsgs and/or genes that control cell differentiation or apoptosis [33] . investigations of the therapeutic potential of micrornas are also under way. in the 2004 version of the who classification scheme, ac is defined as "a malignant epithelial tumour with glandular differentiation or mucin production, showing acinar, papillary, bronchioloalveolar or solid with mucin growth patterns or a mixture of these patterns" [34] . ac has become the most frequent histologic type of lung cancer in parts of the world. it occurs primarily in smokers, but represents the most common type of lung cancer in people who have never smoked and in women. a small subset of these tumors arise in patients with localized scars or diffuse fibrosing lung diseases such as asbestosis and interstitial pneumonia associated with scleroderma [35] . these neoplasms usually arise in the periphery of the lung, and are more likely to invade the pleura and chest wall than other histologic types of lung cancers. radiologic studies can show one or more nodules, ground-glass opacities, or mixed solid and ground-glass lesions. on gross examination, the neoplasms are often solitary gray-white nodules or masses, sometimes with necrosis or cavitation, which pucker the overlying pleura. mucin-producing tumors can have a glistening, gelatinous appearance. other presentations include a pattern of consolidation resembling pneumonia (usually bronchioloalveolar carcinoma) ( figure 18 .3), multiple nodules, diffuse interstitial widening due to lymphangitic spread, endobronchial lesions with submucosal infiltration, and diffuse visceral pleural infiltration and thickening resembling mesothelioma. common histologic patterns displayed by acs include acinar ( figure 18 chapter 18 molecular basis of pulmonary disease mixtures of these patterns are very frequent. less common histologic subtypes include fetal ac, mucinous (colloid) ac, mucinous cystadenocarcinoma, signet ring ac, and clear cell ac [34] . acs usually exhibit differentiation toward clara cells or type ii pneumocytes or, less often, goblet cells. they manifest a range of differentiation extending from very well-differentiated tumors with extensive gland formation and little cytoatypia, to poorly differentiated, solid tumors that cannot be categorized as acs unless one orders a mucin stain (figure 18.7) . however, most examples include readily identifiable glands. invasiveness is reflected by the presence of neoplastic glands that infiltrate through stroma or pleura, stimulating a fibroblastic (desmoplastic) response ( figure 18.4) , or by cells in the lumens of blood vessels or lymphatics. in recent years, atypical adenomatous hyperplasia (aah) has been recognized as a precursor lesion for peripheral pulmonary acs. this lesion is defined as "a localized proliferation of mild to moderately atypical cells lining involved alveoli and, sometimes, respiratory bronchioles, resulting in focal lesions in peripheral part iv molecular pathology of human disease alveolated lung, usually less than 5 mm in diameter and generally in the absence of underlying interstitial inflammation and fibrosis" (figure 18 .8) [36] . aah exists on a histologic continuum with bronchioloalveolar carcinoma (bac), which is defined as an in situ (noninvasive) form of ac, in which the neoplastic cells grow along alveolar septa (lepidic growth) without invasion of stroma or vasculature ( figure 18 .5, figure 18 .6) [34] . most bacs exceed 1 cm in diameter and consist of cells with greater degrees of cytoatypia than aah. although aah is found in approximately 3% of patients without lung cancer at autopsy [37] , it has been reported in 9%-21% of lung resection specimens with all types of primary lung cancer and 16%-35% of lung resection specimens with ac [36] . the progenitor cell for bac and aah is believed to be an epithelial cell located at the junction between the terminal bronchiole and alveolus, termed the bronchioalveolar stem cell [38] . a recently published large-scale study of primary lung acs, using dense single nucleotide polymorphism arrays, described 57 significantly recurrent copy-number alterations in these tumors (table 18 .4) [12] . twenty-six of 39 autosomal chromosome arms showed consistent large-scale copy-number gain or loss, and 31 recurrent focal events, including 24 amplifications and 7 homozygous deletions, were found. although some of the alterations involved regions known to harbor a proto-oncogene or tsg, these genes remain to be identified in some of the other regions affected. amplification of chromosome 14q13.3 was the most common event noted, found in 12% of samples. this region includes nkx2-1, which encodes a lineage-specific transcription factor (thyroid transcription factor-1 [ttf-1]) that activates transcription of target genes including the surfactant proteins, and may be an important proto-oncogene involved in a significant fraction of lung acs. immunohistochemical staining for ttf-1 can be performed to detect expression of this factor in most lung adenocarcinomas, aiding in the determination of the lung as the site of origin of the tumor (figure 18 .9). additional work using small interfering rna (sirna)mediated knockdown of this gene in lung cancer cell lines with amplification led to reductions in tumor cell proliferation, through both decreased cell cycle progression and increased apoptosis, suggesting that gene amplification and overexpression contribute to lung cancer cell proliferation rates and survival [39] . egfr and k-ras mutations are mutually exclusive mutational events in ac of the lung, which suggests the existence of two independent oncogenic pathways [40, 41] . egfr is a receptor tyrosine kinase whose activation by ligand binding leads to activation of cell signaling pathways such as ras/mitogen-activated protein kinase (mapk) and phosphatidylinositol-3-kinase, which in turn propagates signals for proliferation, blocking of apoptosis, differentiation, motility, invasion, and adhesion [21] . tumor-acquired mutations in the tyrosine kinase domain of egfr, often associated with gene amplification, have been found in approximately 5%-10% of nsclcs in the united states, and are associated with ac histology, never-smoker status, east asian ethnicity, and female gender [14, 40, 42] . egfr mutations are frequently in-frame deletions in exon 19, single missense mutations in exon 21, or in-frame duplications/insertions in exon 20, and occasional missense mutations and double mutations can also be detected [40, 43] . egfr mutation has an inverse correlation with methylation of the p16 ink4a gene and sparc (secreted protein acidic and rich in cysteine), an extracellular ca2ã¾-binding glycoprotein associated with the regulation of cell adhesion and growth [41] . egfr status is an important predictor of response to egfr kinase inhibitors: patients with egfr mutations are most likely to have a significant response to egfr tyrosine kinase inhibitor therapy, and egfr amplification and protein overexpression have been reported to correlate with survival after egfr tyrosine kinase inhibitor therapy [14, 44] . k-ras is a member of the ras family of proteins, which function as signal transducers between cell membrane-based growth factor signaling and the mapk pathways [21] . k-ras mutations are associated with smoking, male gender, and poorly differentiated tumors [43] . her2 (also known as egfr2 or erbb2), a member of the egfr family of receptor tyrosine kinases, is mutated in less than 2% of nsclc, and does not occur in tumors with egfr or k-ras mutation [45] . the her2 mutations are in-frame insertions in exon 20 and are significantly more frequent in acs (2.8%), never smokers (3.2%), asian ethnicity (3.9%), and women (3.6%), similar to egfr mutations [45] . alterations in dna methylation appear to be important epigenetic changes in cancer, contributing to chromosomal instability through global hypomethylation, and aberrant gene expression through alterations in the methylation levels at promoter cpg islands [46] . this lesion, which has been defined as a precursor lesion for peripheral pulmonary adenocarcinomas, consists of a wellcircumscribed nodule measuring several millimeters in diameter, in which alveolar septa are lined by mildly moderate atypical cells. epigenetic differences exist between egfr-mediated and k-ras-mediated tumorigenesis, and may interact with the genetic changes. a recent study showed that the probability of having egfr mutation was significantly lower among those with p16 ink4a and cdh13 methylation than in those without, and the methylation index was significantly lower in egfr mutant cases than in wild-type. in contrast, k-ras mutation was significantly higher in p16 ink4a methylated cases than in unmethylated cases, and the methylation index was higher in k-ras mutant cases than in wild-type [47] . sqcc is defined as "a malignant epithelial tumour showing keratinization and/or intercellular bridges that arises from bronchial epithelium," in the who classification scheme [48] . it is a common histologic type of nsclc that is closely linked to cigarette smoking. in most patients, this tumor arises in a mainstem, lobar, or segmental bronchus, producing a central mass on imaging known tumor suppressor genes and proto-oncogenes defined as found in either cosmic30, cgp census31, or other evidence; if there is more than one known proto-oncogene in the region, only one is listed (priority for listing is, in order: known lung adenocarcinoma mutation; known lung cancer mutation; other known mutation (by cosmic frequency); listing in cgp census). @myc is near, but not within, the peak region. ksingle gene deletions previously seen, this study provides new mutations as well. part iv molecular pathology of human disease studies. many of these tumors have an endobronchial component that can cause airway obstruction, leading to postobstructive pneumonia, atelectasis, or bronchiectasis. not infrequently, it is the pneumonia that prompts evaluation of the patient and leads to discovery of the tumor. less often, sqccs develop in the periphery of the lung. gross examination reveals a tan or gray mass that usually arises in a large bronchus and often includes an endobronchial component (figure 18 .10, figure 18 .11). partial or complete airway obstruction can be associated with changes of pneumonia, bronchitis, abscess, bronchiectasis, or atelectasis. necrosis and cavitation are very common in these tumors. involvement of hilar lymph nodes by tan-gray tumor can be visible in some resected specimens. microscopically, the key features of this tumor are its keratinization, sometimes with formation of keratin pearls, and intercellular bridges ( figure 18 .12). as is true of acs, the degree of differentiation of this tumor varies from very well differentiated cases, in which there are abundant keratinization and intercellular bridges and little cytoatypia, to very poorly differentiated cases, in which keratinization and intercellular bridges can be quite inconspicuous and the tumor consists of sheets of large atypical cells with marked cytoatypia and frequent mitoses. however, most cases fall more toward the middle of the spectrum. invasiveness is reflected by the presence of irregular nests and sheets of cells that infiltrate through tissues, stimulating a fibroblastic response, or by cells inside vascular or lymphatic spaces. invasive sqccs are often accompanied by sqcc in situ and dysplasia, their precursor lesions. these lesions arise in the bronchi and may be contiguous with the invasive tumor or exist as one or more separate foci. these precursor lesions can also be observed without coexisting invasive carcinoma. like sqcc, tobacco smoking is the main predisposing factor for sqcc in situ and dysplasia. unlike invasive sqcc, however, these lesions are not invasive-they do not extend through the basement membrane of the bronchial epithelium. grossly, they may be invisible or appear as flat, tan or red discolorations of the bronchial mucosa, or tan wart-like excrescences. microscopically, these lesions encompass a chapter 18 molecular basis of pulmonary disease range of squamous changes that include alterations in the thickness of the bronchial epithelium, the maturational progress of squamous differentiation, cell size, and nuclear characteristics ( figure 18 .13, figure 18 .14) [11, 49] . as dysplasia increases from mild to moderate to severe, the epithelium thickens, and maturation is increasingly impaired. the basilar zone expands with epithelial cell crowding, the intermediate zone shrinks, and there is reduced flattening of the superficial squamous cells. cell size, pleomorphism, and anisocytosis usually increase, and there is coarsening of the chromatin and appearance of nucleoli, nuclear angulations, and folding. in carcinoma in situ, although the epithelium may or may not be thickened and the cell size may be small, medium, or large, there is minimal or no maturation from the base to the superficial aspect, and the atypical nuclear features are present throughout the entire thickness of the epithelium. mitoses appear in the lower third (mild or moderate dysplasia), lower two-thirds (severe dysplasia), or throughout the full thickness of the epithelium (carcinoma in situ). basal cells in the bronchial epithelium are believed to represent the progenitor cells for invasive sqcc, and the sequence of events leading to sqcc is believed to include basal cell hyperplasia, squamous metaplasia, squamous dysplasia, carcinoma in situ, and invasive sqcc (figure 18 .14) [11, [49] [50] [51] . regression of lesions preceding invasive sqcc can occur, particularly the earlier lesions [52] . however, severe dysplasia and carcinoma in situ are associated with a significantly increased probability of developing invasive sqcc in patients followed over time with surveillance bronchoscopy [53] . wistuba and colleagues evaluated sqccs and precursor lesions for loss of heterozygosity (loh) at 10 chromosomal regions (3p12, 3p14.2, 3p14.1-21.3, 3p21, 3p22-24, 3p25, 5q22, 9p21, 13q14 rb, and 17p13 tp53) part iv molecular pathology of human disease frequently deleted in lung cancer and found multiple, sequentially occurring allele-specific molecular changes in separate, apparently clonally independent foci, early in the pathogenesis of sqccs of the lung, suggesting a field cancerization effect [11, 18] . they observed clones of cells with allelic loss at one or more regions in 31% percent of histologically normal epithelium and 42% of specimens with hyperplasia or metaplasia; increasing frequency of loh within clones with increasing histopathologic lesional severity; the most frequent and earliest regions of allelic loss at 3p21, 3p22-24, 3p25, and 9p21; increasing size of the 3p deletions with progressive histologic changes; and tp53 allelic loss in many histologically advanced lesions (dysplasia and cis) [18] . an overview of the sequential molecular events leading to invasive sqcc is shown in figure 18 .14 [11] . large cell carcinoma is an undifferentiated nsclc without light microscopic evidence of squamous or glandular differentiation, although squamous or glandular features may be detectable by ultrastructural examination (figure 18 .15) [54] . histologic subtypes of large cell carcinoma include large cell neuroendocrine carcinoma (lcnec), combined lcnec, basaloid carcinoma, lymphoepithelioma-like carcinoma, clear cell carcinoma, and large cell carcinoma with rhabdoid phenotype [54] . clinical signs and symptoms resemble those of other types of nsclc. most tumors develop as peripheral lung masses, except for basaloid carcinomas, which usually form centrally located masses. histologically, large cell carcinomas consist of sheets and nests of large cells with vesicular nuclei, prominent nucleoli, and moderate or abundant amounts of cytoplasm. lcnecs demonstrate neuroendocrine architectural features and immunohistochemical or ultrastructural evidence of neuroendocrine differentiation. basaloid carcinomas display nests of small, monomorphic, rounded or fusiform tumor cells with little cytoplasm, numerous mitoses, comedo-type necrosis, and hyaline or mucoid stromal degeneration. clear cell carcinoma consists of large tumor cells with clear cytoplasm. precursor lesions are not currently recognized for any of the subtypes of large cell carcinoma. however, basaloid carcinoma is associated with squamous dysplasia in about one-third of cases [54] . large cell carcinomas are poorly differentiated carcinomas that can demonstrate features of ac (most frequent), sqcc, or neuroendocrine differentiation when examined by immunohistochemistry, electron microscopy, or molecular methods [55] . these tumors often demonstrate losses of 1p, 1q, 3p, 6q, 7q, and 17p, and gains of 5q and 7p, more closely resembling acs than other histologic types of lung cancer [56] . common molecular abnormalities include tp53 mutation, c-myc amplification, and p16 promoter hypermethylation, while k-ras mutation is less common [55] . egfr tyrosine kinase domain mutation is not characteristic of large cell carcinomas, and egfrviii (deletion mutations in the extracellular domain of egfr) is uncommon [57, 58] . the major categories of pulmonary neuroendocrine (ne) neoplasms include small cell carcinoma (sclc), large cell neuroendocrine carcinoma (lcnec), typical carcinoid, and atypical carcinoid. sclc and lcnec are high-grade carcinomas, typical carcinoid is a low-grade malignant neoplasm, and atypical carcinoid occupies an intermediate position in the spectrum of biologic aggressiveness. in one large series, the 5-year and 10-year survival rates for typical carcinoid were 87% and 87%, 56% and 35% for atypical carcinoid, 27% and 9% for lcnec, and 9% and 5% for sclc, respectively [59] . by light microscopy, these tumors display ne architectural features including organoid nesting, a trabecular arrangement, rosette formation, and palisading. these patterns are more prominent in carcinoids than in lcnecs and may or may not be visible in individual sclcs. typical carcinoids contain fewer than 2 mitoses per 2 mm 2 (10 hpf) and lack necrosis ( figure 18 .16), while atypical carcinoids show 2-10 mitoses per 2 mm 2 (10 hpf) or necrosis, which is often punctate [60] . sclc consists of small, undifferentiated tumor cells with scant cytoplasm and finely granular chromatin and absent or inconspicuous nucleoli ( figure 18 .17). nuclear molding is characteristic, necrosis is common, and the mitotic rate is typically high, with a mean of over 60 mitoses per 2 mm 2 [61] . combined differences also exist in the characteristics of patients with carcinoids, as compared to patients with sclc and lcnec. patients with carcinoids are typically younger and less likely to smoke than those with sclcs and lcnecs, the vast majority of whom have a current or previous history of tobacco smoking [62, 63] . rare patients with carcinoids have the multiple endocrine neoplasia 1 (men1) syndrome, an association that is not seen with sclcs and lcnecs. in addition, an association with diffuse idiopathic pulmonary neuroendocrine cell hyperplasia (dipnech) has been noted for carcinoids but not for sclcs and lcnecs, leading to classification of dipnech as a preinvasive lesion in the most recent version of the who classification scheme [64] . dipnech is a diffuse proliferation of single cells, small nodules (ne bodies), and linear proliferations of pulmonary ne cells that may reside in the bronchial and/or bronchiolar epithelia ( figure 18 . 19) , and may be accompanied by extraluminal proliferations part iv molecular pathology of human disease (tumorlets and carcinoids) [64] . however, morphologically identifiable precursor lesions for sclc and lcnec have not been established. molecular markers of pulmonary ne tumors include chromogranin a, synaptophysin (figure 18.20) , and n-cam (cd56). these markers are expressed by all categories of ne tumors, with higher frequencies observed in the carcinoids and atypical carcinoids than in small cell and large cell neuroendocrine carcinomas. gastrin-releasing peptide, calcitonin, other peptide hormones, the insulinoma-associated 1 (insm1) promotor and the human achaete-scute homolog-1 (hash1) gene have also been reported as overexpressed by these tumors [65, 66] . thyroid transcription factor-1 (ttf-1) is expressed by 80%-90% of sclcs, 30%-50% of lcnecs, and 0%-70% of carcinoids [67] [68] [69] [70] . sclcs [71] [72] [73] [74] [75] [76] . more than 90% of sclcs and sqccs demonstrate large, often discontinuous segments of allelic loss on chromosome 3p, in areas encompassing multiple candidate tumor suppressor genes, including some of those listed previously [15, 75] . atypical carcinoids show a higher frequency of loh at 3p, 13q, 9p21, and 17p than typical carcinoids, but not as high as the high-grade ne tumors [77] . some typical and atypical carcinoids possess mutations of the multiple endocrine neoplasia 1 (men1) gene on chromosome 11q13 or loh at this locus [78] , while these abnormalities occur with lower frequencies in sclcs and lcnecs, supporting separate pathways of tumorigenesis [79] . men1 encodes for the nuclear protein menin, which is believed to play several roles in tumorigenesis by linking transcription factor function to histone-modification pathways, in part through interacting with the activator-protein-1 family transcription factor jund, modifying it from an oncoprotein into a tumor suppressor protein [80] . oncogenes frequently amplified in sclcs include myc (8q24), mycn (2p24), and mycl1 (1p34), and additional amplified genes that represent candidate oncogenes include the antiapoptotic genes tnfrsf4 (1p36), dad1 (14q11), bcl2l1 (20q11), and bcl2l2 (14q11) [76] . the myc proteins are transcription factors that are important in cell cycle regulation, proliferation, and dna synthesis, and can induce p14 arf , leading to apoptosis through p53 if cellular conditions do not favor proliferation [21] . tsgs are inactivated in the majority of sclcs. eighty percent to 90% of sclcs demonstrate tp53 mutations, as compared to more than 50% of nsclcs, fewer atypical carcinoids, and virtually no typically carcinoids [74, 81] . most of the tp53 mutations in sclcs are missense point mutations that result in a stabilized p53 mutant protein which can be easily detected by immunohistochemistry [71] . p53 protein overexpression occurs frequently in high-grade ne carcinomas, but is unusual in typical carcinoids and intermediate in atypical carcinoids [82, 83] . dysregulation of p53 produces downstream effects on bcl-2 and bax. antiapoptotic bcl-2 predominates over proapoptotic bax in the high-grade ne carcinomas, while the reverse is true for carcinoids [82] . lcnecs resemble sclcs in their high rates of tp53 mutation and predominance of bcl-2 expression over bax expression [84] . alterations compromising the p16 ink4a /cyclin d1/rb pathway of g1 arrest are consistent in high-grade pulmonary ne carcinomas (92%), primarily through loss of rb protein, but are less frequent in atypical carcinoids (59%) and are uncommon in typical carcinoids [23] . mutations in the rb1 gene exist in many sclcs, with associated loss of function of the gene product [71, 74, 85] . in another study, 89% of the ne carcinomas (excluding carcinoids) versus 13% of the non-ne carcinomas exhibited loh and loss of rb-protein expression [86] . the hypophosphorylated form of rb protein functions as a cell cycle regulator for g1 arrest; cyclin d1 overexpression and p16 ink4a loss produce persistent hyperphosphorylation of rb with consequent evasion of cell cycle arrest [23] . recent data also suggest that in sclcs, overexpression of mdm2 (a transcriptional target of p53) or p14 arf loss leads to evasion of cell cycle arrest through the p53 and rb pathway ( figure 18 .2) [71] . the transcription factor e2f-1 appears to play a role in cellular proliferation by activating genes required for s phase entry. e2f-1 product is overexpressed in 92% of sclcs and 50% of lcnecs, and is significantly associated with a high ki67 index and bcl-2:bax ratio >1 [87] . a mediator of the proteasomal degradation of e2f-1, the s phase kinase-associated protein 2 (skp2) f-box protein accumulates in high-grade ne carcinomas (86%), and its overexpression has been associated with advanced stage and nodal metastasis in pulmonary ne tumors [88] . in the high-grade ne tumors, skp2 appears to interact with e2f-1 and stimulate its transcriptional activity toward the cyclin e promoter [87, 88] . telomeres play an important role in the protection of chromosomes against degradation. telomerases, the enzymes that synthesize telomeric dna strands, serve to counterbalance losses of dna during cell divisions. high telomerase activity has been noted in over 80% of sclcs and lcnecs [89] [90] [91] versus 14% or fewer typical carcinoids [91, 92] . expression of human telomerase mrna component (hterc) and human telomerase reverse transcriptase (htert) mrna were reported, respectively, in 58% and 74% of typical carcinoids; and in 100% and 100% of atypical carcinoids, lcnecs and sclcs, and telomere length alterations in lcnecs and sclcs were greater than in typical carcinoids [92] . aberrant methylation of cytosine-guanine (cpg) islands in promoter regions of malignant cells is an important mechanism for silencing of tsgs (epigenetic inactivation). methylation of dna involves the transfer of a methyl group, by a dna methyltransferase, to the cytosine of a cpg dinucleotide [93] . rassf1a is a potential tsg that undergoes epigenetic inactivation in virtually all sclcs and a majority of nsclcs through hypermethylation of its promoter region [94, 95] . ne tumors have lower frequencies of methylation of p16, apc, and cdh13 (h-cadherin) than nsclcs [95] . sclcs have higher frequencies of methylation of rassf1a, cdh1 (e-cadherin), and rarb than carcinoids [95] . promoter methylation of casp8, which encodes the apoptosis-inducing cysteine protease caspase 8, was also found in 35% of sclcs, 18% of carcinoids, and no nsclcs, suggesting that casp8 may function as a tsg in ne lung tumors [96] . although histologically defined precursors for sclc are lacking, a higher incidence of genetic abnormalities is found in the normal or hyperplasic airway epithelium of patients with sclc than nsclc [97] . by extension, it has been suggested that sclc may arise directly from histologically normal or mildly abnormal epithelium, rather than evolving through a sequence of recognizable histologic intermediary changes [11] . relatively little is known about molecular abnormalities in precursors of carcinoids. although carcinoids have been viewed as arising from tumorlets, 11q13 (int-2) allelic imbalance is significantly more common in carcinoids (73%) than in tumorlets (9%), and may represent an early event in carcinoid tumor formation [98] . the int-2 gene lies in close proximity to men1, a tumor suppressor gene frequently mutated in ne tumors [98] . the molecular pathology of dipnech remains to be elucidated. mesenchymal neoplasms included in the who classification scheme (table 18 .1) encompass a spectrum of malignant and benign proliferations that show differentiation along multiple lineages. overall, these tumors are much less common in the lung than are epithelial neoplasms. information about molecular pathogenesis has emerged for some of the mesenchymal neoplasms. pulmonary inflammatory myofibroblastic tumor (imt) is a lesion composed of myofibroblastic cells, collagen, and inflammatory cells that primarily occurs in individuals less than 40 years of age, and is the most common endobronchial mesenchymal lesion in childhood ( figure 18 .21) [99] . synovial sarcoma is usually a soft tissue malignancy, but uncommonly arises in the pleura or the lung and often takes an aggressive course [100] . pulmonary hamartomas are benign neoplasms consisting of mixtures of cartilage, fat, connective tissue, and smooth muscle, which present as coin lesions on chest radiographs and are excised in order to rule out a malignancy ( figure 18 .22). many imts demonstrate clonal abnormalities with rearrangements of chromosome 2p23 and the anaplastic lymphoma kinase (alk) gene [101] . the rearrangements involve fusion of tropomyosin (tpm) n-terminal coiled-coil domains to the alk c-terminal kinase domain, producing two alk fusion genes, tpm4-alk and tpm3-alk, which encode oncoproteins with constitutive kinase activity [102] . like their soft tissue counterparts, more than 90% of pulmonary and pleural synovial sarcomas demonstrate a chromosomal translocation t(x;18) (syt-ssx) [103, 104] . detection of this translocation can be very helpful for confirming the diagnosis of synovial sarcoma in this unusual location. most pulmonary hamartomas show abnormalities of chromosomal bands 6p21, 12q14-15, or other regions [105] , corresponding to mutations of high-mobility group (hmg) proteins, a family of nonhistone chromatin-associated proteins that serve an important role in regulating chromatin architecture and gene expression [106] . malignant mesothelioma (mm) is an uncommon, aggressive tumor arising from mesothelial cells on serosal surfaces, primarily the pleura and peritoneum, and less often the pericardium or tunica vaginalis. the most important risk factor for mm is exposure to the subset of asbestos fibers known as amphiboles (crocidolite and amosite) [107] . the incidence of this tumor in the united states peaked in the early to mid-1990s, and appears to be declining, likely related to decreases in the use of amphiboles since their peak period of importation in the 1960s [107] . these tumors are characterized by long latency periods between asbestos exposure and clinical presentation of the tumor, with a mean of 30-40 years [108] . radiation, a nonasbestos fiber known as erionite, and potentially other processes associated with pleural scarring have also been implicated in the causation of smaller numbers of cases of malignant mesothelioma [108] , and a role for simian virus 40 (sv40) in the genesis of this tumor has been suggested by some, but remains controversial [109, 110] . pleural mm most commonly arises in males over the age of 60. presenting features typically include a hemorrhagic pleural effusion associated with shortness of breath and chest wall pain. weight loss and malaise are common. by the time the tumor is discovered, patients usually have extensive involvement of the pleural surfaces. with progression, the tumor typically invades the lung, chest wall, and diaphragm. lymph node metastasis can cause superior vena caval obstruction, and cardiac tamponade, subcutaneous nodules, and contralateral lung involvement can also occur. from the time of diagnosis, the median survival is 12 months [110] . treatment may include surgery, chemotherapy, radiotherapy, immunotherapy, or other treatments, often in combination [110] . the intent of surgery is usually palliative. whether extrapleural pneumonectomy with chemotherapy and radiotherapy can lead to cure is unclear [111] . new agents are currently under investigation for their potential to improve the life expectancy and quality of life in patients with this aggressive malignancy. gross pathologic features of mm include pleural nodules which grow and coalesce to fill the pleural cavity and form a thick rind around the lung. a firm tan appearance is common, and occasionally the tumor can have a gelatinous consistency (figure 18 .23). extension along the interlobar fissures and invasion into the adjacent lung, diaphragm, and chest wall are characteristic. further spread can occur into the pericardial cavity and around other mediastinal structures, and distant metastases can also develop. histologically, mm manifests a wide variety of histologic patterns. the major histologic categories include epithelioid mesothelioma, sarcomatoid mesothelioma, desmoplastic mesothelioma, and biphasic mesothelioma [108] . epithelioid mesothelioma consists of round, ovoid, or polygonal cells with eosinophilic cytoplasm and nuclei that are usually round with little cytoatypia (figure 18 .24). these cells most often form sheets, tubulopapillary structures, or gland-like arrangements, and some tumors can have a myxoid appearance due to production of large amounts of hyaluronate. sarcomatoid mesothelioma is composed of malignant-appearing spindle cells occasionally accompanied by mature sarcomatous components (osteosarcoma, chondrosarcoma, others). desmoplastic mesothelioma can be a diagnostic challenge due to its frequently bland appearance and resemblance to organizing pleuritis. it consists of variably atypical spindle cells in a dense collagenous matrix ( figure 18 .25). helpful features for separating figure 18 .23 malignant mesothelioma. the tan/white tumor involves the entire pleura surrounding and compressing the underlying parenchyma, which appears congested but relatively unremarkable. chapter 18 molecular basis of pulmonary disease this tumor from organizing pleuritis include invasion of chest wall muscle or adipose tissue and necrosis. biphasic mesotheliomas include both epithelioid and sarcomatoid elements, each comprising at least 10% of the tumor [108] . pathologic diagnosis of mm has been greatly assisted by the expanded availability of antibodies for use in immunohistochemistry [112] . mesothelial differentiation can be supported by immunoreactivity with cytokeratin 5/6, calretinin ( figure 18 .26), hbme-1, d2-40, and other antibodies. histologic distinction of epithelioid mesotheliomas from metastatic acs is a common need in practice, and a panel approach using calretinin and cytokeratin 5/6, with other antibodies reactive with acs (cea, moc-31, ber-ep4, leu m1, b72.3, and others) will usually be successful. electron microscopy can also be helpful in difficult cases by demonstrating long thin microvilli in many mms with an epithelioid component. pan-cytokeratin staining is helpful for supporting a diagnosis of sarcomatoid or desmoplastic mm as opposed to sarcoma, since most (but not all) sarcomas will not stain for pan-cytokeratin. other mesothelial and mesenchymal markers can also be useful for assisting in the differentiation of mm from histologically similar sarcomas. precursor lesions for mm have not been clearly defined from a histologic standpoint, although it is likely that an in situ stage exists [108] . the term atypical mesothelial hyperplasia has been recommended for surface (noninvasive) proliferations of mesothelial cells of uncertain malignant potential [108] . exposure to asbestos fibers is believed to trigger the pathobiological changes leading to the majority of mms. currently, it is believed that asbestos may act as an initiator (genetically) and promoter (epigenetically) in the development of mms [113] . the degree to which tumorigenesis results from direct interactions of the fibers with the mesothelial cells, or through other mechanisms involving oxidative stress (or both), is unresolved [113, 114] . multiple chromosomal alterations are often noted in mms, and inactivation of tsgs plays an important part in the pathogenesis of mm [113] . a variety of genetic abnormalities have been reported including deletions of 1p21-22, 3p21, 4p, 4q, 6q, 9p21, 13q13-14, 14q, and proximal 15q, monosomy 22, and gains of 1q, 5p, 7p, 8q22-24, and 15q22part iv molecular pathology of human disease 25 [108, 115] . the most common genetic abnormality in mm is a deletion in 9p21 encompassing the cdkn2a locus encoding the tumor suppressors p16 ink4a and p14 arf , which participate in the p53 and rb pathways and inhibit cell cycle progression ( figure 18 .2) [113, 116] . recent studies have shown that sv40 large t antigen (present in some mms) inactivates the tsg products rb and p53, raising the possibility that asbestos and sv40 could act as co-carcinogens in mm and suggesting that perturbations of rb-and p53-dependent growth-regulatory pathways may be involved in the pathogenesis of mm [115] . other common findings include inactivating mutations with allelic loss in the tsg neurofibromin 2 (nf2), found at chromosome 22q12 [117] , and inactivation of cdkn2a/p14 arf and gpc3 (another tsg) by promoter methylation [108] . loss of cdkn2a/ p14 arf also results in mdm2-mediated inactivation of p53 [116] . however, in mms, unlike many other epithelial tumors, mutations in the tp53, rb, and ras genes are rare [118] . the wnt signal transduction pathway is also abnormally activated in mms and appears to play a role in pathogenesis [119] . activation of the pathway leads to accumulation of b-catenin in the cytoplasm and its translocation to the nucleus. interactions with tcf/ lef transcription factors promote expression of multiple genes including c-myc and cyclin d. the mechanism of activation does not appear to involve mutations in the b-catenin gene, but may instead involve more upstream components of the pathway, such as the disheveled proteins [119] . recent evidence also suggests that the phosphatidylinositol 3-kinase (pi3-k/akt) pathway is frequently activated in mms, and that inhibition of this pathway can increase sensitivity to a chemotherapeutic agent [120] . the wilms' tumor gene (wt1) is also expressed in most mms, but its role in the pathogenesis of mm is unclear [114] . finally, egfr signaling in mms has recently become a focus of greater attention, and there are some data showing that the egfr is an early cell membrane target of asbestos fibers and is linked to activation of the mapk cascade [113] . unfortunately, a phase ii clinical trial of gefitinib treatment in patients with mms did not show effectiveness, despite egfr overexpression in over 97% of cases [121] . another study found that common egfr mutations conferring sensitivity to gefitinib are not prevalent in human malignant mesothelioma [122] . further investigation continues into new, potentially efficacious agents for the treatment of mm. non-neoplastic pulmonary pathology comprises inflammatory and fibrosing diseases of the conducting airways, alveoli, vessels, and lymphoid tissue. this pathology may be localized or diffuse, may either have an obvious etiology or be idiopathic, and may cause injury that is reparable or irreparable. most importantly, an understanding of non-neoplastic lung pathology plays a vital role in the clinical management of these diseases. this section covers the major types of obstructive and interstitial diseases, the vascular lesions, the pneumonias, the occupational diseases, the major histiocytic conditions, and the most common developmental anomalies. this list does not include all of the non-neoplastic diseases that can affect the lung, but it represents those that are responsible for the majority of illness. also, the conditions highlighted within each of these categories are those about which we best understand the molecular biology of the disease mechanisms. obstructive lung diseases are characterized by a reduction in airflow due to airway narrowing. this airflow reduction occurs, in general, by two basic mechanisms: (i) inflammation and injury of the airway, resulting in obstruction by mucous and cellular debris within and around the airway lumen; and (ii) destruction of the elastin fibers of the alveolar walls, causing loss of elastic recoil and subsequent premature collapse of the airway during the expiratory phase of respiration. there are four major obstructive lung diseases: asthma, emphysema, chronic bronchitis, and bronchiectasis. asthma is a chronic inflammatory disease of the airways that affects more than 150 million people worldwide. the prevalence of disabling asthma has increased over 200% since 1969, ranging from as low as 1% in rural ethiopia to over 20% among children in parts of central and south america [123] . in the united states, asthma affects approximately 8%-10% of the population and is the leading cause of hospitalization among children less than 15 years of age [123] . clinically, the disease is defined as a generalized obstruction of airflow with a reversibility that can occur spontaneously or with therapy. it is characterized by recurrent wheezing, cough, or shortness of breath resulting from airway hyperactivity and mucus hypersecretion. the hyperresponsiveness is a result of acute bronchospasm and can be elicited for diagnostic purposes using histamine or methacholine challenges. the key feature of these symptoms is that they are variable-worse at night or in the early morning, and in some people worse after exercise. it has previously been assumed that these symptoms are separated by intervals of normal physiology. however, evidence is now accumulating that asthma can cause progressive lung impairment due to chronic morphologic changes in the airways. the treatment strategies for this complex disease are myriad. in atopic individuals, allergen avoidance should be the primary therapy. for example, in children, reducing exposure to house dust mites early in life decreases sensitization and the incidence of disease. for those who do develop the disease, avoidance of allergens later in life improves symptom control. established treatments for asthma flairs include inhaled corticosteroids, and short-acting and long-acting b2-adrenoceptor agonists. phosphodiesterase (pde) inhibitors such as theophylline have been used for decades to treat asthmatic bronchoconstriction, but both cardiac and central nervous systems side effects have limited their use. newer pde inhibitors without side effects include non-xanthine drugs such as rofumilast. the pathologic changes to the airways in asthma are very similar to those seen in chronic bronchitis. they consist of a thickened basement membrane with epithelial desquamation, goblet cell hyperplasia, and subepithelial elastin deposition. in the wall of the airway, smooth muscle hypertrophy and submucosal gland hyperplasia are also present ( figure 18 .27). in acute asthma exacerbations, a transmural chronic inflammatory infiltrate with variable amounts of eosinophilia may be present, resulting in epithelial injury and desquamation that can become quite pronounced. one sees clumps of degenerating epithelial cells mixed with mucin in the lumen airway. these aggregates of degenerating cells are referred to as creola bodies and can be seen in expectorated mucin from these patients. also present in these sputum samples are charcot-leyden crystals, rhomboid-shaped structures that represent breakdown products from eosinophil cytoplasmic granules ( figure 18 .28). the changes seen in the walls of these airways represent long-term airway remodeling caused by prolonged inflammation. this remodeling may play a role in the pathophysiology of asthma. the amount of airway remodeling is highly variable from patient to patient, but remodeling has been found even in patients with mild asthma. currently, the effect of the treatment on this chronic pathology is unclear [124] . the pathogenesis of asthma is complex, and most likely involves both genetic and environmental components. most experts now see it as a disease in which an insult initiates a series of events in a genetically susceptible host. no single gene accounts for the familial component of this disease. genetic analysis of these patients reveals a prevalence of specific hla alleles, polymorphisms of fc erib, il-4, and cd14 [125, 126] . asthma can be classified using a number of different schema. most commonly, asthma is divided into two categories: atopic (allergic) and nonatopic (nonallergic). atopic asthma results from an allergic sensitization usually early in life and has its onset in early childhood. nonatopic asthma is late-onset and, though the immunopathology has not been as well studied, probably has similar mechanisms to atopic asthma. although this nosology is convenient for purposes of understanding the mechanisms of the disease, most patients manifest a combination of these two categories with overlapping symptoms. th0 pathogenetic mechanisms of both types encompass a variety of cells and their products. these include airway epithelium, smooth muscle cells, fibroblasts, mast cells, eosinophils, and t-cells. the asthma response includes two phases: an early response comprising an acute bronchospastic event within 15-30 minutes after exposure, and a late response that peaks approximately 4-6 hours and that can have prolonged effects. if one wants to understand this complex response, it is best to divide it into three components: (i) a type 1 hypersensitivity response, (ii) acute and chronic inflammation, and (iii) bronchial hyperactivity. type 1 hypersensitivity in general, human asthma is associated with a predominance of type 2 helper cells with a cd4ã¾ phenotype. these th2-type cells result from the uptake and processing of viral, allergen, and environmental triggers that initiate the episode. the processing includes the presentation of these triggers by the airway dendritic cells to naive t-cells (th0), resulting in their differentiation into populations of th1 and th2. the th2 differentiation is a result of il-10 release by the dendritic cells, and the th2 cells then part iv molecular pathology of human disease further propagate the inflammatory reaction in two ways. first, they release a variety of cytokines such as il-4, il-5, and il-13 that mediate a wide variety of responses. il-4 and il-13 stimulate b-cells and plasma cells to produce ige, which, in turn, stimulates mast cell maturation and the release of multiple mediators, including histamine and leukotrienes. second, these th2 cells secrete il-5 that, together with il-4, also stimulates mast cells to secrete histamine, tryptase, chymase, and the cysteinyl leukotrienes causing the bronchoconstrictor response that occurs rapidly after the exposure to the allergen. il-5 from these lymphocytes also recruits eosinophils to the airways and stimulates the release of the contents of their granules, including eosinophil cationic protein (ecp), major basic protein (mbp), eosinophil peroxidase, and eosinophil-derived neurotoxin. these compounds not only induce the bronchial wall hyperactivity but are also responsible for the increased vascular permeability that produces the transmural edema in the airways. the cells can differentiate into th1 cells as a result of il-12 produced by dendritic cells. these th1 cells produce interferon-gamma (ifn-g), il-2, and lymphotoxin, which play a role in macrophage activation in delayedtype hypersensitivity reactions as seen in diseases such as rheumatoid arthritis and tuberculosis [123] . these th1 cells are predominantly responsible for defense against intracellular organisms and are more prominent in normal airways and in airways of patients with emphysema than in asthmatics. however, in severe forms of asthma, th1 cells are recruited and have the capacity to secrete tumor necrosis factor (tnf)-a and ifn-g, which may lead to the tissue-damaging immune response one sees in these airways (figure 18 .29) [127, 128] . acute and chronic inflammation the role of acute and chronic inflammatory cells, including eosinophils, mast cells, macrophages, and lymphocytes, in asthma is evident in the abundance of these cells in airways, sputum, and bronchoalveolar samples from patients with this disease. the number of eosinophils in the airways correlates with the severity of asthma and the amount of bronchial hyperresponsiveness. proteins released by these cells including ecp, mcp, and eosinophil-derived neurotoxin cause at least some of the epithelial damage seen in the active form of asthma. neutrophils are prominent in the more acute exacerbations of asthma and are probably recruited to these airways by il-8, a potent neutrophil chemoattractant released by airway epithelial cells [123] . these cells also release proteases, reactive oxygen species (ros), and other proinflammatory mediators that, in addition to the epithelial damage, also contribute to the airway destruction and remodeling that occurs in the more chronic forms of this disease. the susceptibility of the epithelium in asthma to this oxidant injury may be increased due to decreased antioxidants such as superoxide dismutase in these lungs [129] . finally, mast cells are activated to release an abundance of mediators through the binding of ige to fceri, high-affinity receptors on their surface. allergens bind to ige molecules and induce a cross-linking of these molecules, leading to activation of the mast cell and release of a number of mediators, most notably histamine, tryptase, and various leukotrienes, including leukotriene d 4 (ltd 4 ), and interact with the smooth muscle to induce contraction and the acute bronchospastic response [130] . allergen bronchial hyperactivity the cornerstone of asthma is the hyperactive response of the airway smooth muscle. the mechanism by which this occurs combines neural pathways and inflammatory pathways. as stated, the inflammatory component of this response comes predominantly from the mast cells. the major neural pathway involved is the nonadrenergic noncholinergic (nanc) system. although cholinergic pathways are responsible for maintaining the airway smooth muscle tone, it is the nanc system that releases bronchoactive tachykinins (substance p and neurokinin a) that bind to nk2 receptors on the smooth muscle and cause the constriction that characterizes the acute asthmatic response [123] . in addition to these acute mechanisms, the airway also undergoes structural alterations to its formed elements. in the mucosa, these changes include goblet cell hyperplasia and basement membrane thickening. within the submucosa and airway wall, increased deposition of collagen and elastic fibers results in fibrosis and elastosis, and both the smooth muscle cells and the submucosal glands undergo hypertrophy and hyperplasia. these irreversible changes are a consequence of chronic inflammatory insults on the airways through mechanisms that include release of fibrosing mediators such tgfb and mitogenic mediators such as epidermal and fibroblast growth factors (egf, fgf). the exact mechanisms by which this occurs are not clearly defined, but the similarity of these factors with those involved in branching morphogenesis of the developing lung has led to a focus on the effect of inflammation on the interaction of the epithelium with the underlying mesenchymal cells [128] . the term chronic obstructive pulmonary disease (copd) applies to emphysema, chronic bronchitis, and bronchiectasis, those diseases in which airflow limitation is usually progressive, but, unlike asthma, not fully reversible [131] . the prevalence of copd worldwide is estimated at 9%-10% in adults over the age of 40 [132] . though there are different forms of copd with different etiologies, the clinical manifestations of the most common forms of the disease are the same. these include a progressive decline in lung function, usually measured as decreased forced expiratory flow in 1 second (fev1), a chronic cough, and dyspnea. emphysema and chronic bronchitis are the most common diseases of copd and are the result of cigarette smoking. as such, they usually exist together in most smokers. chronic bronchitis is defined clinically as a persistent cough with sputum production for at least 3 months in at least 2 consecutive years without any other identifiable cause. patients with chronic bronchitis typically have copious sputum with a prominent cough, more commonly get infections, and typically experience hypercapnia and severe hypoxemia, giving rise to the clinical moniker blue bloater. emphysema is the destruction and permanent enlargement of the air spaces distal to the terminal bronchioles without obvious fibrosis [133] . these patients have only a slight cough, while the overinflation of the lungs is severe, inspiring the term pink puffers. the pathologic features of copd are best understood if one considers the whole of copd as a spectrum of pathology that consists of emphysematous tissue destruction, airway inflammation, remodeling, and obstruction [134] . the lungs of patients with copd usually contain all of these features, but in varying proportions. the pathologic features of chronic bronchitis include mucosal pathology that consists of epithelial inflammation, injury, and regenerative epithelial changes of squamous and goblet cell metaplasia. in addition, the submucosa shows changes of remodeling with smooth muscle hypertrophy and submucosal gland hyperplasia. these changes are responsible for the copious secretions characteristic of this clinical disease, although studies have reported no consistent relationship between these pathologic features of the large airways and the airflow obstruction [135] . the pathology definition of emphysema is an abnormal, permanent enlargement of the airspaces distal to the terminal bronchioles accompanied by destruction of the alveolar walls without fibrosis [133] . the four major pathologic patterns of emphysema are defined by the location of this destruction. these include centriacinar, panacinar, paraseptal, and irregular emphysema. the first two of these are responsible for the overwhelming majority of the clinical disease. centriacinar emphysema (sometimes referred to as centrilobular) represents 95% of the cases and is a result of destruction of alveoli at the proximal and central areas of the pulmonary acinus, including the respiratory bronchioles ( figure 18 .30). it predominantly affects the upper lobes the remaining two types of emphysema, paraseptal and irregular, are rarely associated with clinical disease. in paraseptal emphysema, the damage is to the distal acinus, the area that abuts the pleura at the margins of the lobules. damage in this area may cause spontaneous pneumothoraces, typically in young, thin men [136] . irregular emphysema is tissue destruction and alveolar enlargement that occurs adjacent to scarring, secondary to the enhanced inflammation in the area. though this is a common finding in a scarred lung, it is of little if any clinical significance to the patient. though the emphysema in these lungs plays the dominant role in causing the obstruction, small airway pathology is also present. respiratory bronchiolitis refers to the inflammatory changes found in the distal airways of smokers. these consist of pigmented macrophages filling the lumen and the peribronchiolar airspaces and mild chronic inflammation and fibrosis around the bronchioles (figure 18 .33). the pigment in these macrophages represents the inhaled particulate matter of the cigarette smoke that has been phagocytized by these cells. the macrophages in turn release proteases, which destroy the elastic fibers in the surrounding area, resulting in the loss of elastic recoil and the obstructive symptoms. in general, copd is a result of inflammation of the large airways that produces the airway remodeling characteristic of chronic bronchitis as well as inflammation of the smaller airways that results in the destruction of the adjacent tissue and consequent emphysema. the predominant inflammatory cells involved in this process are the alveolar macrophages, neutrophils, and lymphocytes. the main theories of the pathogenesis of copd support the interaction of airway inflammation with two main systems in the lung: the protease-antiprotease system and the oxidant-antioxidant system. these systems help to protect the lung from the many irritants that enter the lung via the large pulmonary surface area that interfaces with the environment. in the protease-antiprotease system, proteases are produced by a number of cells, including epithelial cells and inflammatory cells that degrade the underlying lung matrix. the most important proteases in the lung are the neutrophil elastases, part of the serine protease family, and the metalloproteinases (mmps) produced predominantly by macrophages. these proteases can be secreted in response to invasion by environmental irritants, most notably infectious agents such as bacteria. in this setting, their role is to enzymatically degrade the organism. however, proteases can also be secreted by both inflammatory and epithelial cells in a normal lung to repair and maintain the underlying lung matrix proteins [137] . to protect the lung from unwanted destruction by these enzymes, the liver secretes antiproteases that circulate in the bloodstream to the lung and inhibit the action of the proteases. in addition, macrophages that secrete mmps also secrete tissue inhibitors of metalloproteinases (timps). a delicate balance of proteases and antiproteases is needed to maintain the integrity of the lung structure. an imbalance that results in a relative excess of proteases (either by overproduction of proteases or underproduction of their inhibitors) leads to tissue destruction and the formation of emphysema. this imbalance occurs in different ways in the two major types of emphysema: centriacinar and panacinar. in centriacinar emphysema, caused primarily by cigarette smoking, there is an overproduction of proteases primarily due to the stimulatory effect of chemicals within the smoke on the neutrophils and macrophages. though the exact mechanism is not completely understood, most studies support that nicotine from the cigarette smoke acts as a chemoattractant, and ros also contained in the smoke, stimulate an increased release of neutrophil elastases and mmps from activated macrophages, leading to the destruction of the elastin in the alveolar spaces [137] . this inflammatory cell activation may come about through the activation of the transcription factor nfkb that leads to tnfa production [132] . in addition, the elastin peptides themselves may attract additional inflammatory cells to further increase the protease secretion and exacerbate the matrix destruction [137] . unlike centriacinar emphysema, panacinar emphysema is most commonly caused by a genetic deficiency of antiproteases, usually due to alpha-1 anti-trypsin (aat) deficiency, a condition that affects approximately 60,000 people in the united states [138] . aat deficiency is due to a defect in the gene that encodes the protein aat, a glycoprotein produced by hepatocytes and the main inhibitor of neutrophil elastase. the affected gene is the serpina1 gene (formerly known as p1), located on the long arm of chromosome 14 (14q31-32.3). the genetic mutations that occur have been categorized into four groups: base substitution, in-frame deletions, frame-shift mutations, and exon deletions. these mutations usually result in misfolding, polymerization, and retention of the aberrant protein within the hepatocytes, leading to decreased circulating levels. aat deficiency is an autosomal codominant disease with over 100 allelic variants, of which the m alleles (m1-m6) are the most common; these alleles produce normal serum levels of a lessactive protein [139] . individuals who manifest the lung disease are usually homozygous for the alleles z or s (zz and ss phenotype) or heterozygous for the 2 m alleles (mz, or sz phenotype) [139] . an aat concentration in plasma of less than 40% of normal confers a risk for emphysema [140] . in individuals with the zz genotype, the activity of aat is approximately one-fifth of normal [141] . the second system in the lung involved in the pathogenesis of emphysema is the oxidant-antioxidant system. as in the protease system, the lung is protected from oxidative stress in the form of ros by antioxidants produced by cells in the lung. ros in the lung include oxygen ions, free radicals, and peroxides. the major antioxidants in the airways are enzymes including catalase, superoxide dismutase (sod), glutathione peroxidase, glutathione s-transferase, xanthine oxidase, and thioredoxin, as well as nonenzymatic antioxidants including glutathione, ascorbate, urate, and bilirubin [142] . the balance of oxidants and antioxidants in the lung prevents damage by ros. however, cigarette smoke increases the production of ros by neutrophils, eosinophils, macrophages, and epithelial cells [143] . evidence that damage to the lung epithelium and matrix is a direct result of ros includes the presence of exhaled h 2 o 2 and 8-isoprostane, decreased plasma antioxidants, and increased plasma and tissue levels of oxidized proteins, including various lipid peroxidation products. in addition to this direct effect, ros may also induce a proinflammatory response that recruits more inflammatory cells to the lung. in animal models, cigarette smoke induces the expression of proinflammatory cytokines such as il-6, il-8, tnfa, and il-1 from macrophages, epithelial cells, and fibroblasts, perhaps through activation of the transcription factor nfkb [144, 145] (figure 18.34) . finally, there is some evidence that cigarette smoke further disturbs the oxidant-antioxidant balance in the lung by depleting antioxidants such as ascorbate and glutathione [132] . bronchiectasis represents the permanent remodeling and dilatation of the large airways of the lung most commonly due to chronic inflammation and recurrent pneumonia. these infections usually occur because airway secretions and entrapped organisms cannot be effectively cleared. this pathology dictates the clinical features of the disease, which include chronic cough with copious secretions and a history of recurrent pneumonia. the five major causes of bronchiectasis are infection, obstruction, impaired mucociliary defenses, impaired systemic immune defenses, and congenital. these may produce either a localized or diffuse form of the disease. localized bronchiectasis is usually due to obstruction of airways by mass lesions or scars from previous injury or infection. diffuse bronchiectasis can result from defects in systemic immune defenses in which either innate or adaptive immunity may be impaired. diseases due to the former include chronic granulomatous disease (cgd), and diseases due to the latter include agammaglobulinemia/hypogammaglobulinemia and severe combined immune deficiencies. defects in the mucociliary defense mechanism that is responsible for physically clearing organisms from the lung may also cause diffuse bronchiectasis. these include ciliary dyskinesias that result in cilia with aberrant ultrastructure and cystic fibrosis (cf). congenital forms of bronchiectasis are rare but do exist. the most common include mounier-kuhn's syndrome and williams-campbell syndrome, the former causing enlargement of the trachea and major bronchi due to loss of bronchial cartilage, and the latter causing diffuse bronchiectasis of the major airways probably due to a genetic defect in the connective tissue [146, 147] . the pathology of bronchiectasis is most dramatically seen at the gross level. one can see dilated airways containing copious amounts of infected secretions and mucous plugs localized either to a segment of the lung or diffusely involving the entire lung as in cystic fibrosis (figure 18.35) . microscopic features include chronic inflammatory changes similar to those of chronic bronchitis but with ulceration of the mucosa and submucosa leading to destruction of the smooth muscle, and elastic in the airway wall and the characteristic dilatation and fibrosis. these enlarged airways contain mucous plugs comprising mucin and abundant degenerating inflammatory cells, a result of infections that establish themselves in these airways following the loss of the mucociliary defense mechanism. bacteria may be found in these plugs, most notably p. aeruginosa. the pathogenetic mechanism of bronchiectasis is complex and depends on the underlying etiology. in general, the initial damage to the bronchial epithelium is due to aberrant mucin (cystic fibrosis), dysfunctional cilia (ciliary dyskinesias), and ineffective immune surveillance (defects in innate and antibody-mediated immunity), leading to a cycle of tissue injury, repair, and remodeling that ultimately destroys the normal airway. the initial event in this cycle usually involves dysfunction of the mucociliary mechanism that inhibits the expulsion from the lungs of organisms and other foreign substances that invade the airways. this may be due to defects in the cilia or the mucin. ciliary defects are found in primary ciliary dyskinesia, a genetically heterogeneous disorder, usually inherited as an autosomal recessive trait that produces immotile cilia with clinical manifestations in the lungs, sinuses, middle ear, male fertility, and organ lateralization [148] . over 250 proteins make up the axoneme of the cilia, but mutations in 2 genes, dnai1 and dnah5, which encode for proteins in the outer dynein arms, most frequently cause this disorder [149] . in cf the main defect affects the mucin. in patients with this autosomal recessive condition, there is a low volume of airway surface liquid (asl) causing sticky mucin that inhibits normal ciliary motion and effective mucociliary clearance of organisms. this is due to a defect in the cystic fibrosis transmembrane conductance regulator (cftr) gene, located on chromosome 7 that encodes a camp-activated channel which regulates the flow of chloride ions in and out of cells and intracellular vacuoles, helping to maintain the osmolality of the mucin. this protein is present predominantly on the apical membrane of the airway epithelial cells, though it is also involved in considerable subapical, intracellular trafficking and recycling during the course of its maturation within these cells. this genetic disease manifests in multiple other organs that depend on chloride ion transport to maintain normal secretions, including the pancreas, intestine, liver, reproductive organs, and sweat glands [150] . the genetic mutations in cf influence the cftr trafficking in the distal compartments of the protein secretary pathway, and various genetic mutations produce different clinical phenotypes of the disease. over 1600 mutations of the cftr gene have been found. however, only four of these mutations occur at a frequency of greater than 1%. these mutations are grouped into five classes according to their functional deficit: group i, cftr is not synthesized; group ii, cftr is inadequately processed; group iii, cftr is not regulated; group iv, cftr shows abnormal conductance; group v, cftr has partially defective production or processing. approximately 70% of cf patients are in group ii and have the same mutation, f508d cftr, a deletion of phenylalanine at codon 508 [154] . in these patients, most of the cftr protein is misfolded and undergoes premature degradation within the endoplasmic reticulum, though a small amount of the cftr protein is present on the apical membrane and does function normally. cf patients may have a combination of genetic mutations from any of the five groups. however, those patients with the most severe disease involving both the lungs and pancreas usually carry at least two mutations from group i, ii, or iii [151] . systemic immune deficiencies cause bronchiectasis through the establishment of persistent infection and inflammation. there are four major categories of immune deficiencies. the first category consists of a number of genetic diseases that cause either agammaglobulinemia or hypogammaglobulinemia. these include xlinked agammaglobulinemia (xla) and common variable immunodeficiency (cvi). xla is caused by a mutation of the bruton's tyrosine kinase (btk) gene that results in the virtual absence of all immunoglobulin isotypes and of circulating b lymphocytes. in cvi there is a marked reduction in igg and iga and/or igm, associated with defective antibody response to protein and polysaccharide antigens. as expected, both of these diseases increase susceptibility to infections from encapsulated bacteria. the second category of immune deficiency is hyper-ige syndrome, a disease with markedly elevated serum ige levels that is characterized by recurrent staphylococcal infections. the third category is chronic granulomatous disease (cgd), a genetically heterogeneous group of disorders that have a defective phagocytic respiratory burst and superoxide production, inhibiting the ability to kill staphylococcus spp. and fungi such as aspergillus spp. finally, severe combined immune deficiency (scid) comprises a group of disorders with abnormal t-cell development and b-cell and/or natural killer cell maturation and function, predisposing these patients to pneumocystis jiroveci and viral infections [152] . after the initial insult, the subsequent steps in the development of bronchiectasis include destruction of the epithelial cells and bronchial wall connective tissue matrix by the proteases and ros secreted by the neutrophils. this proinflammatory milieu is produced by multiple factors. first, infections can persist in these lungs due to defective host immune systems and mechanisms certain organisms have developed to evade these immune defenses. for example, pseudomonas aeruginosa, changes from a nonmucoid to a mucoid variant and also releases virulence factors to protect against phagocytosis [153] . second, in the case of cystic fibrosis, neutrophils are directly recruited by proinflammatory cytokines, such as interleukin-8 (il-8), released from the bronchial epithelial cells as a result of the defective cgft protein [154] . finally, the necrotic cellular debris and other breakdown products act as chemoattractants that recruit more inflammatory cells to the airway wall, further exacerbating the damage. the final phase of the repair and remodeling begins when macrophages invade and recruit fibroblasts that secrete collagen, leading to the fibrosis seen in the pathology. however, in the absence of effective airway clearance mechanisms, these ectatic airways remain a reservoir of infection that continues the cycle of inflammation and tissue destruction. the idiopathic interstitial pneumonias (iips) comprise a group of diffuse infiltrative pulmonary diseases with a similar clinical presentation characterized by dyspnea, restrictive physiology, and bilateral interstitial infiltrates on chest radiography [155] . pathologically, these diseases have characteristic patterns of tissue injury with chronic inflammation and varying amounts of fibrosis. by recognizing these patterns, a pathologist can classify each of these entities and predict prognosis. however, the pathologist cannot establish the etiology, since these pathologic patterns can be seen in multiple clinical settings. the pathologic classification of these diseases, originally defined by liebow and carrington in 1969 [156] , has undergone important revisions over the past 35 years with the latest revision by the american thoracic society/european respiratory society in 2003 [157] . the best known and most prevalent entity of the iips is idiopathic pulmonary fibrosis (ipf), which is known pathologically as usual interstitial pneumonia (uip). uip is a histologic pattern characterized by patchy areas of chronic lymphocytic inflammation with organizing and collagenous type fibrosis. these patients usually present with gradually increasing shortness of breath and a nonproductive cough after having had symptoms for many months or even years. imaging studies usually reveal bilateral, basilar disease with a reticular pattern [155] . therapy begins with corticosteroids, advancing to more cytotoxic drugs such as methotrexate and cytoxan, but most current therapies are not effective in stopping the progression of the disease. the current estimates are that 20/100,000 males and 13/100,000 females have the disease, most of whom progress to respiratory failure and death within 5 years [158] . the pathology is characterized by a leading edge of chronic inflammation with fibroblastic foci that begin in different areas of the lung at different times. these processes produce a variegated pattern of fibrosis, usually referred to as a temporally heterogenous pattern of injury [159] . because it occurs predominantly in the periphery of the lung involving the subpleura and interlobular septae, the gross picture is one of more advanced peripheral and basilar disease (figure 18.36) . the progression from inflammation to fibrosis includes interstitial widening, epithelial injury and sloughing, fibroblastic infiltration, and organizing fibrosis within the characteristic fibroblastic foci. deposition of collagen by fibroblasts occurs in the latter stages of repair. the presence of the abundant collagen produces stiff lungs that are unable to clear the airway secretions, leading to recurrent inflammation of the bronchiolar epithelium with eventual fibrosis and breakdown of the airway structure. this remodeling produces mucousfilled ectatic spaces giving rise to the gross picture of honeycomb spaces, which is seen in the advanced pathology ( figure 18 .36) [160] . theories of the pathogenesis of ipf have evolved over the past decade. early theories favored a primary inflammatory process, while current theories favor the concept that the fibrosis of the lung proceeds independently of inflammatory events and develops from aberrant epithelial and epithelial-mesenchymal responses to injury to the alveolar epithelial cells (aecs) [161] . the aecs consist of two populations: the type 1 pneumocytes and the type 2 pneumocytes. in normal lungs, type 1 pneumocytes line 95% of the alveolar wall, and type 2 pneumocytes line the remaining 5%. however, in lung injury, the type 1 cells, which are exquisitely fragile, undergo cell death, and the type 2 pneumocytes serve as progenitor cells to regenerate the alveolar epithelium [162] . though some studies have suggested that repopulation of the type 2 cells depends on circulating stem cells, this concept remains to be fully proven. according to current concepts, the injury and/or apoptosis of the aecs initiates a cascade of cellular events that produce the scarring in these lungs. studies of aecs in lungs from patients with ipf have shown ultrastructural evidence of cell injury and apoptosis as well as expression of proapoptotic proteins. further, inhibition of this apoptosis by blocking a variety of proapoptotic mechanisms such the fas-fas ligand pathway, angiotensin, and tnfa production, and caspase activation can stop the progression of this fibrosis [163] . the result of the aec injury is the migration, proliferation, and activation of the fibroblasts and myofibroblasts that leads to the formation of the characteristic fibroblastic foci of the uip pathology and the deposition and accumulation of collagen and elastic fibers in the alveoli (figure 18.37 ). this unique pathology may be a result of the increased production of profibrotic factors such as transforming growth factor-a (tgfa) and tgfb, fibroblastic growth factor-2, insulin-like growth factor-1, and platelet-derived growth factor. an alternative pathway might involve overproduction of inhibitors of matrix degradation such as timps (tissue inhibitors of matrix production) [164] . in support of the former mechanism, fibroblasts isolated from the lungs of ipf patients exhibit a profibrotic secretory phenotype [165] . multiple factors, such as environmental particulates, drug or chemical exposures, and viruses may trigger the initial epithelial injury, but genetic factors also play a role. approximately 2%-20% of patients with ipf have a family history of the disease with an inheritance pattern of autosomal dominance with variable penetrance. two genetic mutations have been implicated in this familial form of ipf. one large kindred has been reported with a mutation in the gene encoding surfactant protein c, and six probands have been a b reported with heterozygous mutations in genes htert or htr, encoding telomerase reverse transcriptase and telomerase rna, respectively, resulting in mutant telomerase and short telomeres [166] . adult respiratory distress syndrome (ards) represents a constellation of clinical, radiologic, and physiologic features in patients with acute respiratory failure that can occur after a variety of insults. ards is defined by clinical criteria that include a rapid onset of severe hypoxemia that is refractory to oxygen therapy, the presence of abnormal chest radiographs with evidence of bilateral alveolar filling and collapse, increased pulmonary artery occlusion pressure, and a resistance to improved oxygenation regardless of mechanical ventilation therapy [167] . treatment of ards includes eliminating the underlying cause, protective ventilation strategies that improve oxygenation, and supportive treatment that may include administration of corticosteroids. the pathology of ards is diffuse alveolar damage (dad), whose histologic picture is one of inflammation and fibrosis that diffusely involves all of the structures of the alveolus and is similar throughout the affected areas of the lung [168] . dad is divided into three major phases that follow each other chronologically after the original insult. these are exudative, proliferative, and fibrotic dad. the initial injury primarily involves the epithelium of the alveolar wall and the endothelium in the capillary, causing the destruction and sloughing of the type 1 pneumocytes into the alveolar space and a breakdown of the tight junctions of the endothelium. in combination, these two events result in the loss of the epithelial-endothelial barrier of the alveolus and leakage of plasma from the capillary into the alveolar space. this flooding of the airspace with fluid markedly decreases oxygen exchange and causes the hypoxia that these patients experience. in addition, acute inflammatory changes of the endothelium also cause thrombi to form in vessels, adding to a decreased amount of blood circulating through the lung and further compromising gas exchange. as air is brought into the alveoli, the positive pressure within the alveolar space forces the plasma against the alveolar wall, producing a membranous morphology referred to as hyalin membranes characteristic of the first phase of dad, referred to as exudative dad (figure 18.38) . this initial injury is followed by a sequence of events that represent the lung's efforts to repair itself. first, type 2 pneumocytes undergo hyperplasia and re-epithelialize the alveolar wall after the loss of the type 1 cells. this re-establishes the epithelial barrier and, because these cells secrete surfactant, results in increased surfactant production, which lowers the surface tension of the alveolus and inhibits its collapse. because of the increased numbers of type 2 pneumocytes, this is known as the proliferative phase of dad (figure 18.38) . in the final phase of dad, fibrotic dad, fibroblasts migrate in from the adjacent interstitium to the alveolar space and produce organizing and irreversible fibrosis within both the alveolar space and the interstitium. in addition to this mechanism, fibrosis may also occur in those areas where alveolar walls collapse when surfactant is decreased during the initial insult. the histopathologic picture during this fibrotic phase is one of thickened alveolar septa, intra-alveolar granulation tissue, microcyst formation, and areas of irregular alveolar scarring. in rare cases, these microcysts progress to large cysts, an adult equivalent of bronchopulmonary dysplasia. the cellular events of dad are complex and incompletely understood. in general, the disease can be broken down into two phases. in the first, a large influx of neutrophils and plasma enter the alveolar space. the role the neutrophils play in the initial cellular injury and death is unclear, but it is known that they are necessary for this injury to occur. in addition, clinical studies have shown that within the peripheral blood and bronchoalveolar lavages (bal) of these patients, neutrophils are present along with a myriad of proinflammatory cytokines, such as il-8, il-1, and tgfa, all of which are capable of recruiting them to the lung. also present in these fluids are mediators that recruit fibroblasts such as tgfb. all of these mediators are probably the result of upregulation of nfkb, a proinflammatory transcription factor, in alveolar macrophages. the adherence of neutrophils to the capillary endothelium in the lung occurs through adhesion molecules such as selectin, integrin, and immunoglobulins. neutrophil adherence and subsequent transmigration through the endothelium of the lung capillaries may cause some endothelial damage. however, most speculate that ros and reactive nitrogen chapter 18 molecular basis of pulmonary disease species (rns) secreted by the neutrophils modulate the majority of this injury [169] . this is supported by the finding that patients with ards have products of oxidative damage such as hydrogen peroxide (h 2 o 2 ) in the exhaled breath and myeloperoxidase and oxidized aat in the bal. the cell injury and death of the type 1 pneumocytes most likely occurs via two mechanisms: lipopolysaccharide (lps)-induced caspase-dependent apoptosis and hyperoxia-induced cell death through apoptosis and nonapoptotic mechanisms [170] . in the former, lps, an immunogenic component of the outer membrane of gram-negative bacteria, may trigger innate immune and inflammatory responses via toll-like receptors that bind fas-associated death domain protein and caspase-9, leading to epithelial cell death. in hyperoxia-induced cell death, hyperoxia may induce the expression of angiopoietin 2 (ang2) in lung epithelial cells. ang2 is an angiogenic growth factor that can activate caspase pathways and lead to apoptotic cell death [170] . cell death in ards is not limited to these mechanisms, and further study of many of pathways by which this can occur is needed. lymphangioleiomyomatosis (lam) is a rare systemic disease of women, usually in their reproductive years (average age of 35 years), that is characterized by a proliferation of abnormal smooth muscle cells giving rise to cysts in the lungs, abnormalities in the lymphatics, and abdominal tumors, most notably in the kidneys. in addition to sporadic cases (denoted as s-lam), lam also affects 30% of women with tuberous sclerosis (denoted as tsc-lam), a genetic disorder with variable penetrance associated with seizures, brain tumors, and cognitive impairment [171, 172] . global estimates indicate that tsc-lam may be as much as 5-fold to 10-fold more prevalent than s-lam, though at least some suggest that tsc-lam may have a milder clinical course than s-lam [172] . clinically, lam patients usually present with increasing shortness of breath on exertion, obstructive symptoms, spontaneous pneumothoraces, and chylous effusions or with abdominal masses consisting of either angiomyolipomas and/or lymphangiomyomas. chest imaging studies characteristically reveal hyperinflation with flattened diaphragms and thin-walled cystic changes. mortality at 10 years from the onset of symptoms is 10%-20% [173] . lam appears as small, thin-walled cysts (0.5-5.0 cm) randomly throughout both lungs [174] (figure 18.39) . microscopically, lam lungs contain a diffuse infiltration of smooth muscle cells, predominantly around lymphatics, veins, and venules. most notably, one finds smooth muscle cells in the subpleural with hemosiderin-laden macrophages in the adjacent field, and the macrophages are also seen on bronchoalveolar lavage specimens from these patients. the hemosiderin pigment in these lungs is thought to be secondary to microhemorrhages from the obstruction of the veins ( figure 18 .40) [175] . the smooth muscle cells in lam react to antibodies to hmb-45, a premelanosomal protein. other melanosome-like structures are also found in lam cells, suggesting that these cells have characteristics of both smooth muscle and melanosomes [176] . the lesional cells in lam are smooth muscle-like with both spindled and epithelioid morphology [177] . these cells are the same in both s-lam and tsc-lam part iv molecular pathology of human disease and are a clonal population although they lack other features of malignancy [178] . molecular studies reveal that the abnormal lam cell proliferation is caused by mutations in one of two genes linked to tuberous sclerosis: tuberous sclerosis complex 1 or 2 (tsc1 or tsc2). these two genes control cell growth and differentiation through the akt/mammalian target of rapamycin (mtor) signaling pathway [172] . in this pathway, a growth factor receptor (such as insulin or pdgf receptors) becomes phosphorylated when an appropriate ligand binds, resulting in activation of downstream effectors and ultimately akt. the gene products of tsc1 and tsc2 are hamartin and tuberin, which act as dimers to maintain rheb (a member of the ras family) in a gdp-loaded state via statins, acting as a break to the akt/mtor pathway, thereby retarding protein synthesis and cell growth. in lam cells, loss-of-function mutations in these two genes remove this inhibition, leading to enhanced rheb activation, mtor activation (with raptor), and subsequent phosphorylation of downstream molecules which result in uncontrolled cell growth, angiogenesis, and damage to the lung tissue ( figure 18 .41) [179] . the abnormal proliferation of lam cells is thought to damage the lung through overproduction of matrix metalloproteinases (mmps), which degrade the connective tissue of the lung architecture, destroy the alveolar integrity, and result in cyst formation with air trapping [179] . these destructive capabilities of the lam cells are enhanced by their secretion of the angiogenic factor vegf-c, which is thought to cause the proliferation of lymphatic channels throughout the lung [179] . sarcoidosis is a multisystemic disease that involves the lung in over 90% of the cases [180] . it is most common in the 20-40-year age group and among females. in the united states, african americans are more commonly affected than caucasians [181] . the clinical picture of sarcoidosis is variable, but most patients present with systemic symptoms including fatigue, weight loss, and fever. the most common finding on chest imaging studies is bilateral hilar lymph node enlargement and reticular, reticulonodular, and focal alveolar opacities within the lung parenchyma [182] . pulmonary sarcoidosis is characterized by granulomas which consist of activated histiocytes, called epithelioid histiocytes that form nodules ranging in size from 15-20 microns (figure 18 .42) [183] . unlike infectious granulomas that usually contain areas of central necrosis, the granulomas in pulmonary sarcoidosis are predominantly non-necrotizing [184] . also, the granulomas in sarcoidosis follow a distribution along the lymphatics, which includes the area in the subpleural, along the interlobular septae and around the bronchovascular area containing the bronchiole and branch of the pulmonary artery (figure 18 .42). the granulomas occur much more commonly in the upper lobes, leading to the predominant upper lobe fibrosis and bronchiectasis that can be seen in longstanding sarcoidosis [185] . despite over 50 years of research on sarcoidosis, the etiology remains unknown. most agree that the disease is probably a result of environmental triggers acting on a genetically susceptible host [186, 187] . a genetic basis of sarcoidosis has been suggested by studies that demonstrate familial clustering and racial variation [188, 189] . further, complex inheritance patterns for the disease suggest that more than one gene may be involved [190] . several genes of the major histocompatibility complex (mhc) region of the genome have been implicated. most are clustered on the short arm of chromosome 6 that encompasses the human leukocyte antigen (hla) domain. the hla class i mhc molecules associated with sarcoidosis are the hla-b7 and hla-b8 class i alleles [191, 192] . hla class ii molecules implicated in susceptibility include the hla-dr alleles [193, 194] . genes other than mhc genes thought to regulate the susceptibility to sarcoidosis include those for chemokines such as macrophage inflammatory protein-1a and rantes (ccr5 and ccr3) [195, 196] . environmental factors that have been implicated are those that are aerosolized. therefore, these environmental agents have a mode of entry into the lungs and can cause granulomas in the lung, similar to sarcoidosis. these factors can be divided into two major categories, which include infectious and noninfectious agents. the mycobacteria have been the most extensively studied organisms. however, their role in this disease remains controversial due to the difficulty in identifying them by either culture or histochemical stains in sarcoid tissue. recently, molecular techniques have been able to demonstrate mycobacterial nucleic acid in sarcoid tissue [197, 198] . however, even studies using this technology have not produced consistent results, and the role of these organisms in the disease requires further study. the immune response in sarcoidosis has two major features: (i) the initial event leading to granuloma formation and (ii) the progression of this granulomatous response to either resolution or fibrosis [199] . the formation of the granulomas, triggered by activation of tcells and antigen-presenting dendritic histiocytes, results in a release of proinflammatory cytokines and chemokines, and recruitment, activation, and proliferation of mononuclear cells, predominantly t-cells. these activated t-cells are predominantly cd4-expressing t-helper (th) cells, which release ifn-g and il-2. alveolar macrophages at the site release tnfa, il-12, il-16, and other growth factors. this results in the granuloma formation and alveolitis, the characteristic morphologic features of the disease [200] . the second phase of this immunologic response that leads to either resolution of the disease or persistence of the granulomas and fibrosis is less well characterized. ongoing granuloma formation and inflammation may be a result of the persistent presence of antigens, the excessive synthesis of chemotactic factors, or the part iv molecular pathology of human disease persistence of the mononuclear cells within the granulomas. importantly, the role of the t-cells in these granulomas is to secrete cytokines that attract, stimulate, and ultimately deactivate the fibroblasts that are responsible for the fibrosis that is seen in the chronic disease. the balance between the profibrotic mediators such as tgfb, insulin-like growth factor-i, platelet-derived growth factor (pdgf), and the antifibrotic mediators, such as ifn-g, probably dictates the natural history of sarcoidosis in the lung [201] . genes involved in macrophage-derived cytokines, chemokines, and mediators of fibrosis are all possible candidates for the underlying genetic cause of this complicated disease. pulmonary alveolar proteinosis (pap) is a rare disease of the lungs characterized by accumulation of surfactant in the alveolar spaces. the names alveolar proteinosis, lipoproteinosis, or perhaps most accurately phospholipoproteinosis, apply equally to this entity. pap takes three forms clinically: (i) congenital (2%), (ii) secondary (5%-10%), and (iii) idiopathic or primary (88%-93%) [202] [203] [204] . pap arises in previously healthy adults with the median age at diagnosis of approximately 40 years and a male-to-female ratio of 2.7:1. the clinical presentation is variable and usually includes an insidious onset of slowly progressive dyspnea, a dry cough, and other symptoms of respiratory distress, including fatigue and clubbing. however, almost one-third of patients are asymptomatic and are found clinically by abnormal chest x-rays [205, 206] . the secondary form of pap can be found in patients with environmental exposures, including fine silica, aluminum, titanium dioxide, and kaolin dust [206] . also, secondary pap may be found in patients with malignancies, most commonly hematologic malignancies such as myelogenous leukemia [207, 208] . chest imaging studies in both the idiopathic and secondary forms most commonly show fine, diffuse, feathery nodular infiltrates, centered in the hilar areas, sparing the peripheral regions [206] . on chest computerized tomographs, the infiltrates may have a geometric-type shape, sometimes referred to as crazy paving [209] . the most prominent microscopic feature of both idiopathic and secondary pap is the filling of the alveoli with finely granular period acid-schiff-positive diastaseresistant (pasd) acellular material (figure 18 chapter 18 molecular basis of pulmonary disease material consists of phospholipids (90%); surfactant proteins a, b, c, and d (10%); and carbohydrate (<1%) [210] . alveolar macrophages (ams) with prominent foamy cytoplasm are commonly seen, while alveolar septa are remarkably normal in appearance. in some alveolar spaces there are denser, more solid clumps of pas-d-positive material. definitive pathologic differences between the idiopathic and secondary forms of pap have not been well documented [211, 212] . the etiologies of the two adult forms of pap have been well studied with the most known about the idiopathic variant. theories of the pathogenesis of this form have focused on the abnormal accumulation of the surfactant-like material within the alveolar spaces. since the regulation of surfactant levels in the alveoli depends on appropriate synthesis, recycling, and catabolism, the two opposing hypotheses have included overproduction versus decreased degradation of this material. in normal hosts, surfactant is essential to maintaining the low surface tension needed for proper alveolar inflation and gas exchange. the critical role of maintaining the proper composition and amount of surfactant in the alveoli is performed by two cell types: type 2 pneumocytes and alveolar macrophages [213] . the type 2 pneumocytes synthesize surfactant in the endoplasmic reticulum and golgi, and store it as lamellar bodies [213] , which are then delivered to and fuse with the apical plasma membrane, secreting the surfactant into the airways [214] . catabolism of surfactant is carried out by type 2 pneumocytes and ams. in pap, most evidence suggests that the clearance of surfactant by the am is decreased [203, 215] . the first clue as to the underlying mechanism for this defect in am function came in 1994 when studies revealed that knockout mice deficient in granulocytemacrophage colony-stimulating factor (gm-csf) develop lung lesions similar to those in patients with pap [216] . this rather serendipitous finding prompted explorations centered on the am and the effect diminished gm-csf might have on its cellular functions. subsequent studies from humans with pap revealed an autoimmune mechanism by which a circulating neutralizing antibody to gm-csf blocked its binding to the gm-csf receptor, depressing the effect of gm-csf on the ams [217] [218] [219] . neutralizing antibodies to gm-csf have most often been identified in the idiopathic variant of pap. however, recently these antibodies have also been reported in patients with secondary pap [220] . genes that control many functions in the am are controlled by signaling pathways initiated by gm-csf binding to the am. one pathway is mediated through a transcription factor pu.1 that controls genes involved in surfactant degradation, among other bactericidal functions [221, 222] . another transcription factor, peroxisome-proliferator-activated receptor g (pparg), is also part of a pathway activated by gm-csf. pparg controls the expression of genes involved in intracellular lipid metabolism. ams from patients with pap have a deficiency of this transcription factor, which is correctable by gm-csf therapy [223] . overall, the lack of gm-csf-initiated signaling in ams from patients with pap leads to inhibition of both pparg and pu.1 pathways. this results in decreased surfactant catabolism, intracellular lipid metabolism, and the accumulation of surfactant in the alveoli (figure 18 .44). pulmonary hypertension consists of a group of distinct diseases whose pathology is characterized by abnormal destruction, repair, remodeling, and proliferation of all compartments of the pulmonary vascular tree, including arteries, arterioles, capillaries, and veins. the classification of these diseases has undergone a number of revisions. the most recent revision (in 2003) groups these diseases based on both their pathologic and clinical characteristics [224] . there are five major disease categories in the current classification system: (i) pulmonary arterial hypertension (pah); (ii) pulmonary hypertension with left heart disease; (iii) pulmonary hypertension associated with lung disease and/or hypoxemia; (iv) pulmonary hypertension due to chronic thrombotic and/or embolic disease; and (v) miscellaneous causes, including sarcoidosis, histiocytosis x, and lymphangioleiomyomatosis. the clinical course of most patients with pulmonary hypertension begins with exertional dyspnea, and progresses through chest pain, syncope, increased mean pulmonary artery pressures and, eventually, right heart failure. the rate of this clinical progression varies among patients, from a few months to many years [225] . treatment of these diseases focuses on blocking the mediators involved in the pathogenesis of the diseases. however, current therapies rarely prevent progression of the disease, and lung transplantation provides the only hope for long-term survival. the major group of this classification, pah, can be subdivided into familial pah, idiopathic pah, pah associated with other conditions (such as connective tissue diseases, hiv, congenital heart disease), and pah secondary to drugs and toxins (such as anorexigens, cocaine, and amphetamines). in these diseases, the primary pathology is localized predominantly in the small pulmonary arteries and arterioles. however, two other diseases in this group, pulmonary veno-occlusive disease and pulmonary capillary hemangiomatosis, involve predominantly other components of the pulmonary vasculature, the veins, and the capillaries, respectively. the pathologic changes seen in the pulmonary vessels of these patients primarily reflect injury to and repair of the endothelium. early pathologic changes include medial hypertrophy and intimal fibrosis that narrows and obliterates the vessel lumen. these are followed by remodeling and revascularization, producing a proliferation of abnormal endothelial-lined spaces. these structures are known as plexogenic lesions and are the pathognomonic feature of pah (figure 18.45) . in the most severe pathologic lesions, these abnormal vascular structures become dilated or angiomatoid-like and may develop features of a necrotizing vasculitis with transmural inflammation and fibrinoid necrosis. though the exact pathogenetic mechanism of pah remains unknown, research over the past 10 years has begun to offer some clues. the familial form of pah, with a 2:1 female-to-male prevalence, has an autosomal dominance inheritance pattern with low penetrance. the genetic basis for this has been found to be germline mutations in the gene encoding the bone morphogenetic protein receptor type 2 (bmpr2). these mutations account for approximately 60%-70% of familial pah and 10%-25% of patients with sporadic pah [233] . approximately 140 bmpr2 mutations have been identified in familial pah, each resulting in a loss of receptor function, either through alteration in transcription of the gene through missense, nonsense, or frameshift alterations in the codon or by rna spicing mistakes [226] . the mechanism by which a single mutation to the bmpr2 gene induces vascular smooth muscle proliferation and decreased apoptosis that is not completely understood, but it most likely involves defects in the bmpr2 signaling pathway. bmpr2 is a receptor for a family cytokines (bmps) that are members of the tgfb superfamily of proteins that play a role in the growth and regulation of many cells, including those of the pulmonary vasculature. in the vascular smooth muscle cells of the lung, tgfb signaling causes a proliferation of smooth muscle in pulmonary arterioles, while bmpr2 signaling causes an inhibition of the proliferation of these cells, favoring an apoptotic environment. the bmpr2 signaling occurs through an activation of a receptor complex (bmpr1 and bmpr2) that leads to phosphorylation and activation of a number cytoplasmic mediators, most notably the smad proteins (mothers against decapentaplegic). these smad proteins, especially the smad 1, smad 5, and smad 8 complex with smad 4, translocate to the nucleus where they target gene transcription that induces an antiproliferative effect in the cell. in familial pah, the bmrpr2 gene mutation may lead to insufficient protein product and subsequent decreased protein function, in this case decreased bmpr2 receptor function, decreased smad protein activation, and decreased antiproliferative effects in the vascular smooth muscle cells. the imbalance between the proproliferative effects of the tgfbs and the antiproliferative effects of the bmps results in the formation of the vascular lesions of pah (figure 18 .46) [227, 228] . despite these advances, questions regarding the pathogenesis of pah remain. most notably, why do only 10%-20% of patients with the mutation develop clinical disease? some speculate that genes confer susceptibility but a second hit is required to develop the clinical disease, such as modifier genes or environmental triggers, perhaps drugs or viral infections [227, 229] pulmonary vasculitides present as diffuse pulmonary hemorrhage and are usually caused by one of three major pulmonary vasculitis syndromes: wegener's granulomatosis, churg-strauss syndrome, and microscopic polyangiitis. all three diseases have similar clinical presentations and considerable overlap in their pathologic features as small vessel systemic vasculitides that affect the lung as well as other organs, most notably the kidney. wegener's granulomatosis (wg) is an unusual disease that affects the upper and lower respiratory tract and the kidneys. it usually presents between 40 and 60 years of age and is slightly more common in men than women. the clinical presentation depends on the affected organ, but when the lung is involved, hemoptysis is the major presenting symptom. chest imaging studies may show a variety of patterns, most commonly bilateral ground glass opacities with masses, usually in the lower lobes that may cavitate. immunologic testing of peripheral blood or end organ tissue can be helpful in revealing characteristic immunofluorescent staining patterns for antineutrophilic cytoplasmic antibody (anca), an antibody that targets two substances: proteinase 3 (pr3) and myeloperoxidase (mpo). when present in either the blood or the tissue, the pattern of immunofluorescent staining can be cytoplasmic (canca) or perinuclear (panca). the former pattern is more commonly seen in wegener's granulomatosis, and the latter is more commonly seen in microscopic polyangiitis and churg-strauss syndrome (css). css is a systemic disorder defined by the presence of asthma, peripheral blood eosinophilia, and systemic vasculitis. similar to wg, it usually presents between 40 and 60 years of age, and a clinical diagnosis requires a history of asthma, a peripheral blood eosinophilia, neuropathy, an abnormal chest imaging study, and sinusitis. other organs involved include the heart, the central nervous system, kidneys (though less commonly than wg), gastrointestinal tract, and skin. chest imaging usually shows patchy, multifocal infiltrates; masses and cavitation are rare. laboratory tests reveal positive panca tests in 70% of patients. microscopic polyangiitis (mpa) is similar to both wg and css in that it is a systemic vasculitis that involves the lung and usually presents in the fourth or fifth decade of life. the clinical onset is usually sudden with fever, weight loss, myalgias, and arthralgias. the kidney is the main organ involved, and mpa is the most common cause of pulmonary-renal syndrome. lung involvement occurs in approximately 50% of the patients, and skin and upper respiratory tract are other common sites. similar to wg and css, anca testing is helpful with positive panca in 80% of patients. chest imaging usually shows bilateral infiltrates without masses, similar to css. treatment for all three diseases is immunosuppression with glucocorticoids or cyclophosphamide, and all three usually respond well, although wg has a greater relapse rate after treatment than either css or mpa [230] . the pathology of wg, css, and mpa have overlapping features of an acute and chronic vasculitis that involves medium-and small-sized vessels in the lung. the inflammatory cell infiltrate that destroys the blood vessels is both lymphocytic and neutrophilic, and areas of fibrinoid necrosis are seen. however, in wg, there are characteristic areas of microabscesses that lead to masses of geographic necrosis with basophilia. scattered multinucleated giant cells are present, but no wellformed granulomas are seen. this helps to distinguish it from other vasculitides and infection (figure 18.47) . similarly, the pathology of css has distinguishing features, with the early pathology characterized by an eosinophilic pneumonia with areas of loosely formed granulomas with central necrosis containing degenerating eosinophils (figure 18 .48). the infiltrate is predominantly eosinophils, but neutrophils, lymphocytes, and plasma cells are also present. capillaritis can be seen in wg, csg, and mpa, and all three have hemosiderin deposition present, both within alveolar macrophages and deposited in the connective tissue of the interstitium and the vessel walls. the pathogenesis of these three pulmonary hemorrhage syndromes is similar to the mechanisms of these diseases in the kidney. in general, these diseases in the lung and the kidney represent immune-mediated these lesions are thought to be the early form of the larger areas of geographic necrosis that produces the mass-like nodules found in these lungs. chapter 18 molecular basis of pulmonary disease necrotizing vasculitides that have few or no immune deposits in the vessels but exhibit the presence of anca autoantibodies to myeloperoxidase (mpo) and proteinase 3 (pr3), the components of primary granules of neutrophils. mpa and css are primarily diseases of mpo antibodies, and wg is primarily a disease of pr3 antibodies. the mechanism by which the ancas are induced is not known but may be part of an autoimmune response to environmental exposures early in life. these autoantibodies then inflict damage on the vessels through a mechanism that is not yet completely understood. one theory suggests that circulating ancas bind to pr3 and mpo on the surface of neutrophils and initiate a respiratory burst, degranulation, and apoptosis. ros and proteases are released and inflict endothelial and tissue damage on the adjacent vessel. the anca binding may also induce the release of proinflammatory cytokines and chemokines such as il-1 and tnfa that further contribute to the vascular inflammation. the second theory postulates that circulating immune complexes of excess anca antigen (mpo or pr3) and anca autoantibodies attach to the vascular endothelium and activate complement that results in the chemotaxis and adhesion of inflammatory cells, causing these cells to undergo a respiratory burst and, as in the first theory, release of ros and proteases that cause the vascular endothelial damage. in both theories, it is important to remember that mpo and pr3 are also present in monocytes and that anca autoantibodies may be involved with monocytes in similar ways to release inflammatory mediators [231] . infectious diseases of the lung are a common cause of pulmonary disease given the constant exposure of the lungs to the environment. various organisms are capable of causing these infections, including common viruses and bacteria, as well as more uncommon fungi, parasites, and protozoa. the diagnosis of the specific etiologic agent can be challenging given that most have similar clinical features and many are difficult to identify in the lung tissue. this brief overview of the defense mechanisms the lung uses to protect itself will serve to introduce the pathology of these lung infections. the lung has multiple anatomic mechanisms by which it defends itself against invasion by various pathogens. first, the upper nasal cavities and respiratory tract serve as anatomic barriers to inhaled organisms. the ciliated epithelium and torturous cavities of the sinuses screen large organisms (typically larger than 10 microns). for those particles that venture further down the respiratory tract, the cough reflex that the upper trachea elicits serves to expel them up and out. second, the mucociliary tree of the upper respiratory tract captures organisms that evade these two mechanisms. the bronchial epithelium contains cilia of up to 20 microns in length that extend into the air surface liquid (asl). the asl is a bilayer of 50-100 microns in thickness consisting of a low-viscosity or watery lower layer that is covered by a high-viscosity or gel upper layer secreted by adjacent goblet cells. this sticky upper layer serves to trap organisms, and the coordinated beating of the cilia moves these entrapped invaders up this mucociliary escalator to the larynx, where they can be expectorated. present in the secretions of the large airways and within the surfactant lining the alveolar walls are soluble mediators secreted by various cells. these mediators include lysozyme and lactoferrin, which lyse bacteria and inhibit their growth; the defensins and cathelicidins, small peptides both with microbicidal properties; and surfactant proteins a and d at the alveolar level, which bind to microorganism and enhance phagocytosis and also have direct bactericidal activity [232] . the major cells of the innate immune response of the lung are the alveolar macrophages (am) and the polymorphonuclear leukocytes (pmn). neutrophils phagocytize and destroy bacteria such as s. aureus, s. pneumoniae, and h. influenzae through a respiratory burst that generates nadph oxidase-dependent ros. in some instances, ams may ingest but not kill an organism. this occurs with such organisms as mycobacterium spp., nocardia spp., and legionella spp. because of the ability of these organisms to continue to replicate within part iv molecular pathology of human disease the am, cell-mediated immunity is required for their complete elimination. patients with defects in nadph oxidase are especially prone to respiratory infections by such organisms as s. aureus, nocardia spp. and aspergillus spp. bronchial epithelial cells are important in innate immunity through secretion of cytokines and molecules including il-1, il-5, il-6, il-8, and granulocytemacrophage colony-stimulating factor (gm-csf). these molecules attract macrophages as well as neutrophils and other inflammatory cells to the area to enhance the inflammatory response to the organism [233] . bronchial epithelial cells also serve an important role in recognizing pathogens through patternrecognition receptors (prrs). natural killer (nk) cells are involved in the innate immune response with surface receptors that recognize cells infected with viruses such as rsv, influenza, parainfluenza, and rhinovirus. the nk cells release ifn-g, which recruit other immune cells to add to the antiviral response. dendritic cells are tissue histiocytes positioned around the airways and lymphatics in the lung that recognize pathogens and their antigens and trigger the proliferation and amplification of antigen-specific tcells. this immune response bridges the innate immune response to the adaptive immune responses and is especially important in fungal infections. this mechanism is mediated through toll-like receptors (tlrs) that are able to distinguish pathogens from self-components by triggering cytokine production through nfkb and ap-1 and expressing co-stimulatory molecules necessary for this t-cell activation [234] . for those organisms that evade the basic, innate immunity of the lung, there are adaptive immune mechanisms that encompass both humoral and cellular immune mechanisms. humoral immunity is an important defense against encapsulated bacteria, most notably s. pneumoniae, and for other pyogenic bacteria such as h. influenzae, and staphylococci spp., and resolution of these infections requires the production of igg antibodies to the organisms. cellular immunity is especially important against such respiratory viral infections as influenza, rsv, cmv, varicella, and also against opportunistic infections. these viruses induce a cd4ã¾ and cd8ã¾ t-cell response that clears the lung of these viruses within 8-10 days post infection. granulomas are a common inflammatory response to both pathogens and foreign material. the most notable granulomatous infections in the lung are due to mycobacteria and fungal organisms. activation of cd4ã¾ t-cells by these organisms leads to proliferation and differentiation of these cd4ã¾ t-cells into t-helper-1 cells. the release of ifn-g by the th-1 cells activates lung macrophages to form epithelioid macrophages that have an increased ability to kill the microorganisms and express surface molecules that promote cell-to-cell fusion into giant cells. in addition, activation of these macrophages results in the release of numerous cytokines including ifn-g and tnfa. in patients who are deficient in cd4ã¾ t-cells or ifn-g, granuloma formation is very poor, altering the pathologic picture of these infections. this effect is most obvious in the nontuberculous mycobacterial infections, which have numerous patterns of injury depending on the immune status of their host. pneumonias can be broadly categorized into one of five major clinicopathologic categories, including (i) community-acquired pneumonias (acute and atypical), (ii) nosocomial pneumonias, (iii) aspiration pneumonias and lung abscess, (iv) chronic pneumonias, and (v) pneumonias in immunocompromised hosts. each type presents with a characteristic clinical pattern and may be caused by any of several pathogens so that treatment is many times empiric. the first category comprises community-acquired pneumonias (cap). these represent the majority of the lung infections that receive medical treatment, usually on an outpatient basis, with low (<1%) mortality. patients hospitalized for these infections typically have other comorbidities. the responsible organisms include respiratory syncytial virus (rsv); rhinovirus, parainfluenza, and influenza virus; bacteria, including mycoplasma pneumoniae and rickettsia; and most notably chlamydia pneumonia. chlamydia causes what is termed atypical pneumonia with a clinical course characterized by a progressive onset of fever without chills, a dry cough, and chest imaging that reveals focal infiltrates. acute or typical cap presents abruptly with high fever, chills, productive cough, and radiographs with lobar or segmental consolidation. the most common pathogens are streptococcus pneumoniae, haemophilus influenza, staphylococcus aureus, and moraxella catarrhalis. the second category, nosocomial pneumonias, consists of infections acquired within the hospital or from healthcare associated facilities. these infections are usually found in patients with predisposing risk factors and are a major source of morbidity and mortality, with some studies reporting a mortality range of 20%-50%. the most common risk factors include respiratory ventilation, artificial airways, nasogastric tubes, supine positioning, and medications that alter gastric emptying. the responsible organisms include klebsiella spp., legionella spp., staphylococcus aureus, and pseudomonas aeruginosa. the third category includes aspiration pneumonias and lung abscesses. these infections occur in the setting of patients with aberrant swallow or gag reflexes that allow gastric or oral contents into the airways. the organisms where necrosis and cavity formation occurs include s. aureus, k. pneumoniae, the anaerobic oral flora, and mycobacteria. clinically, these infections may have an acute course with fever and dyspnea or a more insidious course, many times with patients first presenting with lung cavities, empyemas, or necrotizing pneumonias. the fourth category, chronic pneumonias, includes indolent infections that cause a localized mass-like lesion in an otherwise healthy host. nocardia and actinomyces spp. are the most common pathogens, but mycobacteria and fungi may also cause these pneumonias. the fifth category includes pneumonias that occur in the setting of an immunocompromised patient. these include a number of organisms that otherwise would not act as pathogens such as the viruses cmv and hsv, the fungi aspergillosis and pneumocystis pneumonia, and the bacterium mycobacterium avium complex. streptococcus pneumoniae streptococcus pneumoniae, a gram-positive diplococcus also known as pneumococcus or diplococcus pneumonia, is a common cause of bacterial pneumonia in infants and elderly patients, alcoholics, diabetics, and patients with immunosuppression. this pneumonia usually presents abruptly with chills, a cough with rust-colored sputum and pleuritis, with high fevers, tachycardia, and tachypnea. the characteristic gross pathology is a lobar pneumonia that progresses from a red acute phase to a gray organizing phase. a fibrinous pleuritis is common, which eventually organizes to entrap the lung parenchyma in a fibrous capsule [235] . the microscopic examination reveals abundant fibrin, neutrophils, and extravasated red blood cells within the alveolar space and congested capillaries. hemophilus influenzae hemophilus influenzae is a gramnegative bacillus that inhabits the upper respiratory tract and can cause otitis media, epiglottitis, and meningitis, and usually enters the lung through aspiration or hematogenous spread. six serotypes are defined based on their capsular antigens, with type b the most common cause of pneumonias. this type of pneumonia is most commonly found in children or in the elderly with underlying chronic lung disease such as emphysema, cystic fibrosis, bronchiectasis, in patients with hiv infection, or in alcoholics. this bacterial pneumonia is usually preceded by a viral or mycoplasma infection that damages the mucociliary elements in the airways and allows for colonization by h. influenzae. the symptoms include fever; a productive, purulent cough; and myalgias. the incidence of this pneumonia as a common community-acquired pneumonia in children is quite low due to the advent of effective vaccines. however, it is increasing in incidence as a nosocomial infection [236] . like pneumococcal pneumonia, the pathology of h. influenzae pneumonia is in a lobar distribution with a neutrophilic-rich infiltrate and a pleural effusion. necrosis and empyema may occur but are uncommon. staphylococcus aureus staphylococcal pneumonia is caused by staphylococcus aureus, gram-positive cocci that usually spread to the lung through the blood from other infected sites, most often the skin. though a common community pathogen, it is found twice as frequently in pneumonias in hospitalized patients. it often attacks the elderly and patients with cf and arises as a co-infection with influenza viral pneumonia. the clinical course is characterized by high fevers, chills, a cough with purulent bloody sputum, and rapidly progressing dyspnea. the gross pathology commonly reveals an acute bronchopneumonia pattern (figure 18 .49) that may evolve into a necrotizing cavity with congested red/purple lungs and airways that contain a bloody fluid and thick mucoid secretions. the histologic pattern is characterized by a bronchopneumonia that spreads distally from the small airways into to the alveolar spaces (figure 18 .50) to form abscesses that connect with the pleural surface and may result in empyemas. the treatment of this organism has become increasingly problematic due to antibioticresistant strains, most notably methicillin-resistant s. aureus. legionella pneumophila legionella are gram-negative bacilli found predominantly in aquatic habitats such as lakes, rivers, and ponds. standing pools of water from humidifiers and other water outlets may be other sources. approximately 50% of air conditioners contain these bacilli. though 15 serogroups of legionella have been identified, 3 cause the overwhelming majority of human pneumonia. the clinical disease takes two forms: (i) legionnaires' disease, named after the outbreak of pneumonia at the 1976 american legion convention in philadelphia; and (ii) pontiac fever, a self-limiting flu-like disease with nonspecific symptoms. legionella pneumonia presents as a severe infection of the lung with chills and rigors with a nonproductive cough. it can progress rapidly to systemic symptoms of nausea, vomiting, and diarrhea and can lead to renal failure and death without immediate antibiotic therapy. the infected lungs are remarkably red and congested and appear to be distended with fluid. the microscopic picture reveals fibrinopurulent exudates that fill the alveolar space mixed with a necrotic, cellular infiltrate of degenerating neutrophils and monocytes (figure 18 .51). hyaline membranes may form in the periphery of the lesions, and pleural effusions consisting of fibrinoserous exudates are common. pseudomonas aeruginosa pseudomonas aeruginosa is a gram-negative bacillus that is found throughout the environment and in 50% of the airways of hospitalized patients. it usually enters the body through a disruption of the epithelial surface by cuts, burns, or therapeutic devices such as mechanical ventilators or intravascular catheters. pneumonias caused by this organism are usually found in intensive care units of hospitals and burn units, in patients with underlying chronic lung diseases including cystic fibrosis, emphysema, and in patients with prolonged hospitalization. the pathology is necrosis with a bronchopneumonia pattern that usually consists of an area of congestion and hemorrhage that is surrounded by a halo of tan/white consolidation (figure 18.52) . a necrotizing vasculitis with abundant organisms in vessel walls can be seen, and cavitation is common ( figure 18 .53). in treated lungs, healed cavities or pneumatoceles may appear as smooth-walled fibrous cysts. other gram-negative bacilli gram-negative bacilli such as klebsiella pneumoniae, acinetobacter, and various enterobacteriaceae spp. are common nosocomial pathogens. similar to p. aeruginosa, these pathogens colonize the oropharynx and are usually introduced into the lung by inhalation or aspiration of oral contents. the most notable of these is friedlander's pneumonia caused by k. pneumoniae, the most common cause of gramnegative bacterial pneumonia. this typically occurs in men over 40 years of age, usually in the setting of alcoholism, diabetes mellitus, or chronic lung disease. these patients produce large amounts of thick, bloody sputum, a product of the viscous mucopolysaccharide capsule of the organism, and present with severe systemic symptoms of hypotension and generalized weakness. the pathology of these pneumonias is similar to pseudomonas pneumonia with marked cavitation and abundant organisms on microscopic examination. nocardia spp. nocardiosis of the lung is caused by nocardia asteroides, a gram-positive rod found in the soil or organic matter. this infection is most common in immunocompromised adult patients and can be seen in the setting of pulmonary alveolar proteinosis, chronic lung diseases, and mycobacterial and other granulomatous diseases that affect the lung. its clinical course is indolent and usually begins 1-2 weeks before the patient presents for medical therapy. cough is common, often with thick, purulent sputum. in the immunocompromised setting, fever, chills, dyspnea, and hemoptysis are common, and weight loss may occur as the disease progresses. the pathology is remarkable for suppurative abscess formation with multiple cavities filled with green, thick pus. the inflammatory infiltrate consists of neutrophils, macrophages, and abundant necrotic debris with epithelioid histiocytes and giant cells within the wall of the cavity (figure 18 .54). empyema and pleura involvement occur in the majority of cases. mycoplasma and rickettsia pneumonias mycoplasma pneumoniae pneumonia is among the most common infections of the lower respiratory tract and usually occurs in small epidemics in closed populations. it often presents with atypical features of a progressive onset, fever without chills, a dry cough, diffuse crackles on physical examination, and chest imaging studies that reveal patchy interstitial infiltrates. the pathologic features are a result of the attachment of the organisms to the bronchiolar epithelium where they cause epithelial injury and ulcerations through secretion of peroxide [237] . in cases of severe infection, diffuse alveolar damage may be present. chlamydial pneumonia chlamydia spp. causes pneumonia in a variety of clinical settings. chlamydia trachomatis is an infection found predominantly in the postnatal period, chlamydia psittaci is the result of direct transmission from infected birds, including parakeets, parrots, and pigeons. chlamydia pneumoniae is the most common of the three and is a frequent cause of community-acquired pneumonia. it typically causes a very mild or asymptomatic infection with fever, sore throat, and nonproductive cough. the course of this infection may be severe in the elderly. chest imaging studies show alveolar infiltrates, and pleural effusions are present in the majority of cases. the pathology has not been well defined since the infection is usually self-limited. however, in experimental animal models there is a neutrophilic response in the early stages, and an interstitial, peribronchiolar, and perivascular infiltrate of lymphocytes, macrophages, and plasma cells in the latter stages of the infection. mycobacteria, a major cause of lung infections, are nonmotile, aerobic, catalase-producing, acid-fast bacilli. clinically significant lung infections can be caused by m. tuberculosis and by a group of nontuberculous mycobacteria (ntm). the latter group consists of over 100 species, of which three cause the overwhelming majority of pulmonary disease. these are m. avium-intracellulare (m. avium complex), m. kansasii, and m. fortuitum-chelonae. throughout history, tuberculosis (infection with m. tuberculosis) was the major disease caused by these organisms and was responsible for worldwide morbidity and mortality. however, over the past two decades lung diseases caused by ntm have become much more common and now represent the majority of the pulmonary mycobacterial disease. mycobacterium tuberculosis pulmonary tuberculosis is spread by interpersonal contact through aerosolized droplets. once in the alveoli, the bacteria cause a cell-mediated inflammatory response that is capable of inducing granuloma formation and necrosis. as in all infections, the extent of the disease is a function of the host's immune response. the most susceptible part iv molecular pathology of human disease patients are those with certain conditions that include immunosuppression, diabetes, malignancy, renal failure, among others. clinically, an infected patient has a productive cough, fever, and weight loss, and may develop hemoptysis as the cavitation progresses and erodes into the pulmonary vessels. extensive involvement of the lung can produce significant dyspnea and pleuritic chest pain. the pathology of tuberculosis is primarily that of granuloma formation and acute pneumonia. the granulomas are predominantly necrotizing, and the pneumonia usually contains abundant fibrin and neutrophils that fill the alveolar spaces. the gross lesions are referred to as caseous or cheese-like, because of the amount of necrosis present. this caseous material can extend into airways and is commonly coughed up during the active disease. in chronic forms of the disease, the area can undergo fibrosis and involute into a firm, hard scar. there are three major clinicopathologic variants of the disease: (i) primary tuberculosis, (ii) postprimary or reactivation tuberculosis, and (iii) progressive fibrocavitary disease. primary tuberculosis. in this form of the disease, the initial site of infection can be anywhere in the lung, but is usually in the lower lobe or anterior segment of the upper lobe, the areas that receive the most ventilation. the lesion usually consists of a dense consolidation with acute pneumonia and necrotizing granulomas. cavitation may occur, especially in the setting of immunocompromised hosts. from these foci, the organisms may spread through the lymphatics to elsewhere in the lung, the hilar lymph nodes, and the bloodstream, and lay dormant for long periods of time. the combination of the primary site of infection and the involved hilar lymph nodes is known as a ghon complex [238] . postprimary tuberculosis. this form of tuberculosis represents reactivation of old, scarred primary lesions long after the initial insult. the lesion can occur anywhere in the lung where the bacteria from the primary lesion have spread, but is usually apical. it consists of a focus or organizing pneumonia and fibrosis with central caseation. in an active lesion, the typical parenchymal pattern is an acute pneumonia with cavitation that expands to include the surrounding lung with aggregates of granulomas. the controversy surrounding this lesion arises as some evidence suggests that these lesions represent exogenous reinfection. the pathology of reactivation or reinfection may be indistinguishable, although reactivation tuberculosis may appear to arise out of a fibrotic, calcified chronic lesion [239] . progressive fibrocavitary disease. this form of the disease may arise out of either primary or postprimary tuberculosis. however, the latter is the more common scenario. the cavities that develop in this form of the disease begin as a slowly progressive, necrotizing pneumonia with abundant granulomas (figure 18 .55). the active disease may spread through the airways, causing ulceration, necrosis, and fibrosis of the surrounding bronchi and bronchioles. the extension of the disease in this way depends on the host, and patients with depressed immune systems can have large areas of the lung involved with massive pulmonary necrosis. usually, a fibrous capsule develops in the area of the cavitation, although inspissated necrotic material into the adjacent airways remains a continuous source of inflammation that can lead to reinfection and ongoing scarring [240] . nontuberculous mycobacteria the nontuberculous mycobacteria (ntm) are ubiquitous inhabitants of our environment, isolated from soil, fresh and brackish water, house dust, birds, animals, and food, and are increasingly important in causing pulmonary disease. there are currently more than 100 ntm species known. those organisms thought to be pathogenic to the lung include the clinical presentation of these lung infections can vary from minimally symptomatic small lesions discovered by routine radiography to sudden hemoptysis from advanced disease with severe cavitation (table 18 .5). the two most characteristic lesions are those of diffuse infiltrates in an immunocompromised patient, seen most commonly in the hiv-positive population and an viruses most pulmonary infections are due to viruses from four major groups: influenza, parainfluenza, respiratory syncytial virus (rsv), and adenovirus (table 18 .6) [241] . the clinical presentations of these infections have some common features, including insidious onset, nonproductive cough, fever, and chest pain. chest imaging studies usually reveal bilateral, multifocal infiltrates, most without evidence of cavitation or pleural involvement. these infections are mild, self-limiting, and require no more than supportive therapy except in immunocompromised hosts, where the clinical course can be much more serious. also, immunocompromised patients are susceptible to other viruses such as herpesvirus and cytomegalovirus pneumonias, which are not common pathogens in normal hosts [242] . since the 1980s, a subset of pulmonary viral infections has emerged with a much more aggressive clinical course, most notably sars, coronavirus, and hantavirus. these viruses present with systemic symptoms of headache, myalgias, and weakness followed by a deteriorating clinical course with respiratory distress, shock and, in over 50% of the cases, death [243, 244] . therapy for most respiratory viral infections is supportive, although antivirals are available for some viruses, mostly used in the setting of immunocompromised patients. ribavirin, a guanosine analogue, is the main antiviral used for rsv; m2 inhibitors or adamantanes (amantadine and rimantadine) are used against influenza a and neuraminidase inhibitors (oseltamivir and zanamivir) are used against both influenza a and b [245] . cytomegalovirus is treated with ganciclovir, foscarnet, or cidofovir, while herpesvirus is treated with acyclovir [241] . the pathologic patterns of injury for most viruses are similar, making morphologic distinctions among them difficult. however, some characteristic patterns emerge, most notably in those viruses that cause cytopathic changes. influenza, adenovirus, sars, coronavirus, and hantavirus all cause an acute lung injury pattern with diffuse alveolar damage, and in the case of the latter two viruses, evidence of hemorrhage and edema. influenza and adenovirus will also cause a necrotizing bronchiolitis due to their preferential infection of bronchial epithelial cells. finally, some viral infections can be distinguished by their characteristic cytopathic inclusions. adenovirus can be identified by characteristic smudge cells that present in advanced stages of the disease and represent adenovirus particles in the nucleus of an infected cell (figure 18 .56). cytomegalovirus has both nuclear owl's eye inclusions, as well as cytoplasmic inclusions (figure 18 .57). herpesvirus has glassy intranuclear inclusions and can also have multinucleation (figure 18 .58). fungi are larger and more complex than bacteria, and their patterns of injury in the lung are different and in general more destructive. these pathogens are common in our environment and enter the lungs through inhalation. though many fungi are capable of causing pulmonary disease, most only inhabit the lung as colonizers. those of most concern for causing clinical disease include the endemic fungi of north america-histoplasma capsulatum, blastomyces dermatitidis, and coccidioides immitis-and two fungi that are commonly seen in immunocompromised hosts-aspergillus fumigatus and pneumocystis jiroveci. histoplasma capsulatum histoplasma capsulatum is a dimorphic fungus most prevalent in the middle portion of the united states from the great lakes to tennessee. the fungus is present in soil that has been contaminated with guano and other debris by nesting birds, most commonly blackbirds and chickens, and by bats. the organism lives in the environment as spores or conidia and germinates to form hyphae. these structures divide to create the yeast forms, which, when inhaled, induce granuloma formation in the lung. approximately 75% of people have skin tests that are positive for exposure to h. capsulatum, but most exposures do not cause clinical disease. disease typically occurs in people exposed to large amounts of organisms, such as construction workers who move large volumes of dirt or spelunkers who venture into bat-ridden caves. the acute disease has flu-like symptoms which are self-limiting. healed disease may leave behind calcified granulomas in the lung that appear as buckshot on chest imaging studies. the most chronic forms of this disease may slowly progress, giving rise to cavitating and fibrous lesions. in the immunocompromised host, disseminating histoplasmosis can be seen, although reactivation is uncommon [246] . the pathology reveals characteristic necrotizing granulomas distributed around the airways (figure 18 .59), which contain silver-positive yeast forms of 2-4 microns. these granulomas may resolve into scarred nodules, which can calcify and produce the characteristic chest images. cavities may form in the apices with progression of the disease, and the disseminated form of the disease has an abundance of organisms both within macrophages in the lung and throughout many organs in the body. blastomyces dermatitidis blastomyces dermatitidis is also endemic to the middle united states, including the ohio and mississippi river valleys. it is found in wooded terrain, usually during the wet seasons, putting campers and outdoorsmen at risk. the clinical disease takes two forms, cutaneous and systemic, the latter beginning in the lungs through inhalation. the acute pulmonary infection takes a nonspecific form with fever, malaise, and chest pain. imaging studies may show either infiltrates or a mass-like infiltrate. thus, blastomyces infection may mimic other diseases, and the diagnosis may be delayed. some patients go on to chronic disease with cavitation or progressive pulmonary blastomycosis, which manifests as acute respiratory distress syndrome, cavitary lesions, and a poor prognosis [247] . the pathology of blastomyces infection is similar to histoplasmosis with necrotizing granulomas. however, the lesions are larger, showing more neutrophilic necrosis. the organisms are also larger (8-15 microns), with prominent broad-based budding, and are apparent on routine hematoxylin and eosin staining (figure 18 .60). coccidioides immitis coccidioides immitis is found in the semi-arid desert climate of the southwestern united states. the organisms are inhaled as spores, causing an acute disease characterized by fever, chills, chest pain, dyspnea, and hemoptysis. chest imaging studies typically show consolidation and cavitation, and hilar lymphadenopathy is common. reactivation and dissemination are possible in patients with previous infection, whether or not they are immunocompromised patients [248] . the pathology of pulmonary coccidioidomycosis is neutrophilic, suppurative, and granulomatous. the organisms appear as large spherules containing endospores, visible on silver stains. the spherules are 30-100 microns in diameter and the endospores that are released into the surrounding tissue proceed to mature into new spherules (figure 18.61) . as in histoplasmosis, cavitating lesions may have hyphal forms that begin to germinate. aspergillus fumigatus aspergilli are asexual mycelial fungi that are ubiquitous in the environment as airborne aspergillus spores. they are weak pathogens that produce invasive infections predominantly in immunocompromised hosts or in those with significant chronic lung diseases. in tissue, aspergilli form septate hyphae, 3-6 microns in diameter, with characteristic acute-angle, dichotomous branching (figure 18.62) . these organisms affect the lung in three major ways: (i) saprophytic growth in bronchi or pre-existent cavities; (ii) as an allergic or hypersensitivity reaction, predominantly in asthmatics; and (iii) invasive aspergillosis in immunocompromised hosts [249, 250] . as a saprophyte, aspergillus produces surface growths or minute masses of hyphae, usually in bronchiectatic cavities, emphysematous bullae, or scars from previous lung diseases such as tuberculosis or sarcoidosis. the pathology is usually that of a fibrous-walled cavity containing degenerating hyphae (figure 18 .63). in this setting, hyphae do not invade into the lung tissue, but surface erosion of a vascularized cavity may cause hemoptysis. aspergillus causes an immunologic response resulting in mucoid impaction or eosinophilic pneumonia in asthmatics, an entity known as allergic bronchopulmonary aspergillosis (abpa). pathologically, one sees mucoid plugs and superficial erosions of the airways with histiocytic inflammation, with only rare hyphal fragments present. the final form of the disease, invasive pulmonary aspergillosis, is found in severely immunocompromised, neutropenic patients. the hyphae, which disseminate through the blood, invade the blood vessels causing thrombosis, hemorrhage, and infarction to form typical targetoid lesions. this form of the disease has a poor prognosis despite aggressive antifungal therapy. pneumocystis jiroveci the taxonomy of pneumocystis jiroveci (formerly pneumocystis carinii) has changed over the past decade. previously thought to be a protozoan based on the histological characteristics of its trophozoite and cyst life forms, it has recently been placed in the fungal kingdom after ribosomal rna was found to have sequences compatible with the ascomycetous fungi [251] . the inability to culture pneumocystis jiroveci has slowed the understanding of this organism. animal models have helped in defining the antigenic and genotypic differences among the various pneumocystis organisms, which has led to the proposal for species-specific strains, with p. jiroveci found in human infections [252] . the molecular methods used for the typing these species examine a number of gene loci. most importantly, sequence analysis of the thymidylate synthase (ts) and superoxide dismutase (soda) gene loci, the epsp synthase domain of the multifunctional arom gene, and the mitochondrial small subunit ribosomal rna (mtssu rrna) locus have been used to distinguish the various pneumocystis species that infect different mammalian hosts [253] . clinically, p. jiroveci causes disease predominantly in the immunocompromised setting. pneumocystis pneumonia (pcp) has been found during recent times most commonly in the aids population, but prior to this epidemic, it was found in malnourished infants and other severely immunocompromised hosts. because this organism has not been cultured, the diagnosis of pcp continues to be challenging. the clinical characteristics are nonspecific and vary with the patient's immune status. in the hiv population, patients typically develop a subacute onset of progressive dyspnea, a nonproductive cough, malaise, and a low-grade fever. in the non-hiv population, the presentation is more acute, with fulminant respiratory failure associated with cough and fever, and usually requiring mechanical ventilation [254] . chest imaging studies typically show bilateral, symmetric, fine reticular interstitial infiltrates involving the perihilar area, which spread to involve the entire lung. figure 18 .62 aspergillosis. aspergillus fumigatus grows within necrotizing cavities of the lung as branching septated fungal hyphae, as seen on this grocott methenamine silver stain. figure 18 .63 aspergilloma. fungal hyphae from aspergillus fumigatus can colonize chronically inflamed lungs with cavities and may grow to form fungal balls with a dark, green color that are treated by surgical resection, as seen in this case of a lobectomy specimen. treatment is usually with trimethoprim/sulfamethoxazole and intravenous pentamidine. survival is 50%-95% even in severely immunocompromised patients. the life cycle of p. jiroveci consists of three stages: trophozoite, cyst, and sporozoite. the trophozoite form, which adheres to the type 1 epithelium, replicates and enlarges through three precyst stages before maturing into a cyst form that is found in the alveolar space. sporozoites develop within immature cysts through meiosis and mitosis. the mature cyst contains eight haploid sporozoites. the rupture of the cyst wall releases sporozoites into the surrounding environment where they mature into trophozoites. the pathology of the infection is predominantly due to the interaction of the organism with the epithelium. the attachment of the organism to the lung epithelium is via glycoprotein a present on the surface of the organism. the binding of the organism to the type 1 cell occurs via surface receptors on the type 1 cell that include macrophage mannose receptors. these interact with glycoprotein a and activate pathways in the organism that induce genes encoding for pathways that induce mating and proliferation responses, and for the formation of pheromone receptors, transcription factors, and heterotrimeric g-protein subunits [263] . in addition to these genetic effects, the cyst wall contains chitins, polymers, and other substances, in particular, 1,3-glucan, that maintain its integrity and induce the inflammatory response of the host. the 1,3-glucan in the wall of the organism stimulates the release by the macrophages of reactive oxidant species and the generation of potent proinflammatory cytokines, such as tnfa, which bind to the organism and exert a toxic effect. once inside the macrophage, the organism is incorporated into the phagolysosome and degraded. tnfa also directly recruits other inflammatory cells including neutrophils, lymphocytes, and circulating monocytes, and induces the release of il-8 and ifn-g that recruit and activate inflammatory cells [255] . in aggregate, the recruitment of these inflammatory cells and the mediators they release is responsible for the damage to the lung epithelium and endothelium that is seen in this disease [255] . the pathology of pcp has typical and atypical variants. typically, the lung contains a dense interstitial plasma cell pneumonia that expands alveolar walls. the epithelium consists predominantly of type 2 pneumocytes, and the alveolar spaces contain an eosinophilic, frothy exudate, which contains fine, hemoxylin-stained dots that represent a thickening in the cyst wall (figure 18.64) . in this form of the disease, the organisms are abundant and the diagnosis can usually be made by bronchoalveolar lavage. atypical pathologic variants include a necrotizing variant that has a pattern similar to the typical form with exudative alveolar infiltrates, but which undergoes necrosis and cavity formation. these cavities heal into fibrous-walled cysts, similar in gross appearance to those found in pseudomonas pneumonia. a third variant has wellformed granulomas involving the airways, a pattern common to histoplasmosis and tuberculosis. in this form, the organisms are rare and very difficult to find, even with tissue organismal stains. in general, the pathologic pattern of injury depends on the host's immune status, with the typical pathology found in severely immunocompromised hosts as the aids population and the atypical forms found in hosts with immune systems that are less compromised. pulmonary langerhans cell histiocytosis (plch) and erdheim-chester disease are histiocytic diseases that primarily affect the lung. other histiocytic diseases may affect the lung, such as niemann-pick disease, gaucher disease, hermansky-pudlak and rosai-dorfman disease, but these are not considered primarily lung histiocytic diseases. pulmonary langerhans' cell histiocytosis (plch) is a disease of the dendritic histiocytes of the lung referred to as langerhans' cells (lcs). this disease is part of a group of diseases that are characterized by a proliferation of langerhans cells in organs throughout the body that range from a malignant systemic disease as is seen in children [256] to the pulmonary variant that is seen in adolescents and adults. plch is usually the result of inflammatory or neoplastic stimuli in lungs of smokers or in lungs involved by certain neoplasms [257] . chest radiographs from patients with plch usually reveal bilateral nodules, predominantly in the upper lobes, which are worrisome for metastatic disease. treatment involves smoking cessation and steroid therapy. typically, the disease undergoes spontaneous regression. approximately 15%-20% of patients will progress to irreversible end-stage fibrosis [258] . the pathology of plch consists of airway-based lesions with a proliferation of lcs. the early cellular lesions contain a mixture of cells including langerhans' cells, lymphocytes, plasma cells, and eosinophils ( figure 18 .65). though it was previously referred to as eosinophilic granuloma, eosinophils are not the major cell type present, and the lesion is, at best, a loosely formed granuloma. immunohistochemistry reveals the lcs to be diffusely, strongly immunoreactive to s-100 protein and cd1a. ultrastructural analysis reveals intracytoplasmic organelles called birbeck granules, a normal constituent of langerhans' cells, in greater numbers in plch [259] . the pathogenetic mechanisms of plch focus on defects in the homeostasis of dendritic cells (dcs) in the lungs of smokers and the role tobacco smoke may play in stimulating the proliferation of these cells [260] . some studies suggest that stimulation of alveolar macrophages by chemicals in smoke results in secretion of such cytokines as gm-csf, tgfb, and tnfa [261] . in transgenic mice, accumulation of dcs around airways may be a result of excess gm-csf [262] . other theories suggest that cigarette smoke stimulates the secretion of bombesin-like peptide by the neuroendocrine cells in the bronchiolar epithelium and leads to a similar stimulation of alveolar macrophages and a cytokine milieu that promotes the proinflammatory proliferative changes [262] . not all smokers get plch, leading to the suggestion that only smokers with an underlying genetic susceptibility will develop the disease. studies have established that in some cases the lcs in plch are clonal, suggesting that cellular abnormalities must play some part in the pathogenesis of the diseases [263] . to support this, studies have shown genetic mutations and allelic loss of tumor suppressor genes in smokers with plch [264] . the mechanisms by which this proliferation of lcs leads to the destruction of the bronchiolar epithelium and the other observed pathology are unclear. lcs in normal lungs have little ability to interact with t-cells or act as effective antigen-presenting cells, but the lcs of plch have a mature immunophenotype, expressing b7-1 and b7-2, the co-stimulatory molecules needed for lymphostimulatory activity [265] . whether this more mature immune phenotype leads to an unregulated immune response and destruction of the bronchial epithelial cells is not known. however, some studies have shown that bronchiolar epithelial cells may induce the expression of this mature phenotype by secreting cytokines in response to environmental stimulants such as cigarette smoke or viral infections, or by the development of hyperplastic or dysplastic lesions that express new foreign antigens [265] . erdheim-chester disease (ecd) is a systemic non-langerhans' cell histiocytosis of adults that most commonly involves the long bones. involvement of other organs, including the lung, has been reported. lung involvement occurs in approximately 20%-35% of the cases, and the patients usually present with cough, dyspnea, rhonchi, and pleuritic pain. radiographically, the lungs reveal infiltrates in a lymphatic distribution, predominantly upper lobe, with prominent interstitial septal markings that can mimic sarcoidosis [266] [267] [268] [269] [270] [271] [272] . pulmonary involvement by ecd may have an unfavorable prognosis, and the fibrosis that ensues is one of the most frequently reported causes of death [266, 273] . the treatment of ecd is variable with corticosteroids, chemotherapy, surgical resection, and radiation therapy reported [273] . non-langerhans' cell histiocytes of dendritic cell phenotype are the main cells present in this disease. this infiltrate contains foamy histiocytes with scattered giant cells, a scant number of lymphocytes or plasma cells, and some fibroblasts. the histiocytes express cd68 (macrophage antigen) and factor xiiia (dendritic cell antigen), but express s-100 protein weakly or not at all, and do not express cd1a. ultrastructural analysis reveals phagolysosomes, but no birbeck granules are present [273] . this infiltrate that involves the lung is usually present in the pleura and subpleura, within the interlobular septa and around the bronchovascular structures. the remainder of the lung parenchyma is unremarkable, though fibrosis and paracicatricial emphysema can appear in the late stages of the disease [266] . the etiology of ecd is not known, but this rare disease has been established as primarily a macrophage disorder [274] . these histiocytes have abundant phagolysosomes and express the antigen cd1a and are consistent with a phagocytic cell, most likely closely related to alveolar macrophages. the peripheral monocytosis and the proinflammatory cytokine profile that is found in these patients might suggest that the histiocytic infiltrate is a result of systemic monocytic activation and invasion of circulating monocytes into the tissues throughout the body [275] . recently, an ecd patient was successfully treated by an agent toxic to monocytes, supporting the theory that these cells play a part in the disease [275] . alternatively, end organ cytokine production by local inflammatory cells resulting in proliferation and differentiation of resident immature histiocyte populations may produce a similar picture. another interesting observation is that erdheim-chester has been reported to occur in patients with langerhans' cell histiocytosis [276] , which may suggest that this is a disease where macrophages transition between two different phenotypes along the differentiation spectrum of tissue dendritic cells [276] . whether this is a benign or malignant proliferation has not been established. of 5 patients studied, clonality has been demonstrated in 3 by polymerasechain reaction [277] . environmental exposures are a major cause of lung disease and can cause a wide spectrum of both acute and chronic pathology. many organic and inorganic materials can cause lung damage, and because of their similar patterns of injury and long latent periods, it can be difficult to isolate the exact offending agent without a thorough clinical history. the two occupational lung diseases presented here-asbestosis and silicosis-represent pneumoconiosis, which are defined as diseases which result in diffuse parenchymal lung injury due to inhaled inorganic material. both have many pathologic patterns of injury that depend on the amount and length of time of exposure, and both can also cause neoplastic diseases of the lung. asbestos fibers are naturally occurring silicates that are commonly used in construction materials such as cement and insulation and in many textiles. they can be separated into two groups based on their mineralogic characteristics. serpentine fibers, named as such because they are long and curly, include chrysotile asbestos. amphibole fibers, more straight and rodlike, include predominantly amosite and crocidolite asbestos. in the united states most of the asbestos is chrysotile. the amphiboles are more pathogenic and are responsible for most of the neoplastic and non-neoplastic pulmonary diseases associated with asbestos exposure. by definition, asbestosis is bilateral diffuse interstitial fibrosis of the lungs that can be attributed to asbestos exposure. the disease, which mostly affects textile and construction workers, is usually the result of direct exposure over 15-20 years. the latency to clinical disease is inversely proportional to the level of exposure. the symptoms are a gradual onset of shortness of breath, a cough with dry rales at the bases on inspiration, and digital clubbing. in the early disease, the chest x-ray shows basilar disease that begins predominantly as thickening of the subpleural, but progresses as infiltrates and fibrosis that involve the middle zone, eventually leading to thickening of the airways and traction bronchiectasis. the apex of the lung is usually spared. the clinical findings are nonspecific and have considerable overlap with uip, so the diagnosis is usually made only when a history of significant exposure is discovered. the gross picture includes a bilateral lower lobe gray/tan fibrosis with honeycomb changes in late disease. microscopically, asbestosis can cause many patterns of injury in the lung, but the most common is collagenous deposition in the areas of the lymphatics where the fibers are in the highest concentration. these areas include the subpleural, interlobular septae, and around the bronchovascular areas that contain a bronchiole and a branch of the pulmonary artery. hyalinized pleural plaques are a common manifestation of asbestos exposure but are not specific for asbestos and can be found in the absence of pulmonary parenchymal disease. eventually, the fibrosis involves the alveoli beyond the bronchioles and causes distortion of the lung architecture to form remodeled, dilated airspaces similar to those seen in uip. distinguishing this fibrosis from other forms of fibrosing lung disease can be difficult, but the presence of ferruginous bodies, asbestos fibers coated by iron, proteins, and a mucopolysaccharide coat are indicative of significant asbestos exposures and support this diagnosis (figure 18 .66) [278] . figure 18.66 asbestosis. this cytopathologic preparation from a bronchoalveolar lavage specimen illustrates an asbestos fiber coated by an iron-protein-mucopolysaccharide substance and appears as a golden brown, beaded structure known as a ferruginous body. silicosis results from chronic, high-dose exposure to crystalline silica, which consists of silicon and oxygen with trace amounts of other elements, usually iron. the most common silica is quartz, which is present in large amounts in such rocks as granite, shale, and sandstone and is among the more fibrogenic of all silica types. thus, occupations most at risk for silicosis include sandblasting, quarrying, stone dressing, and foundry work where exposure to quartz is high. the disease takes three major clinical and pathologic forms that have different clinical characteristics. simple or nodule silicosis is marked by the presence of fine nodules 1 cm, on chest imaging studies, usually in the upper lobes. patients with this condition are typically asymptomatic, with normal respiratory physiology. the pathology in these lungs reveals discrete, hard nodules that have a green/gray color, centered either on the small airways or in the subpleura. microscopically, these nodules have an early stellate shape that eventually transforms to a more whorled appearance with dustladen macrophages scattered throughout it. polarized light examination reveals weakly birefringent material. complicated pneumoconiosis represents similar pathologic findings only with larger and more circumscribed nodules, which coalesce into a large upper lobe mass, a condition known as progressive, massive fibrosis ( figure 18.67) . these patients are symptomatic with a productive cough and mixed pulmonary function tests with a reduced diffusing capacity as the fibrosis increases. diffuse interstitial fibrosis may occur; however, unlike asbestosis, this pattern is found in pneumoconiosis. when complicated pneumoconiosis is found with rheumatoid nodules in the setting of a patient with rheumatoid arthritis, this is known as caplan's syndrome. the pathogenesis of both asbestosis and silicosis depends upon inflammation and fibrosis caused by the inhaled fibers. in humans, the amount of fiber needed to cause fibrosis varies from person to person. this may be related to a difference in fiber deposition based on the size of the lungs or to the efficacy with which the lung clears these fibers [256] . some studies have also suggested that fiber length determines the amount of pathology. however, this association has not been confirmed in humans for either asbestosis or silicosis. in both diseases, it is known that other factors increase the risk of developing disease. for example, smokers exhibit worse disease than nonsmokers with similar exposures to asbestosis. the mechanism for this effect is unclear, although speculation centers on the inhibition of fiber clearance in smokers. also, it is known that smoking enhances the uptake of fibers by pulmonary epithelial cells and in this way may increase the fibrogenic and inflammatory cytokine production by these cells. the cellular mechanisms by which both asbestos and silica fibers induce the inflammation and fibrosis are mediated predominantly through alveolar macrophages. in the case of silica, it is known that the uptake of these fibers into the alveolar macrophages is by way of a scavenger receptor expressed on the surface of the cell known as marco (macrophage receptor with a collagenous structure). once inside the cells, the fibers activate the release of ros that can lead to cellular and molecular damage through a number of pathways. first, ros can directly cause lipid peroxidation, membrane damage, and dna damage. second, silicainduced free radicals can trigger phosphorylation of cellular proliferation pathways through mitogen-activated protein kinases (mapks), extracellular signal regulated kinases (erks), and p38. these pathways are also involved in the proliferation of fibroblasts in asbestosis and of mesothelial and epithelial cells in the neoplastic diseases associated with the inhalation of these fibers [279] . in addition, these fibers can activate proinflammatory pathways controlled by such transcription factors as nuclear nfkb and activator protein 1 (ap-1). these pathways result in the activation of the early response genes c-fos and c-jun and the release of proinflammatory cytokines such as il-1 as well as fibrogenic factors such tnfa [280] . tnfa plays a prominent role in both diseases, and its regulation has been studied in animal models exposed to silica. it is now known that a transcription factor labeled nuclear factor of activated t-cells (nfat) plays a key role in the regulation of tnfa. figure 18 .67 complicated pneumoconiosis/ progressive massive fibrosis. this sagittal cut section of lung reveals a large gray/black mass that extends from the apex to include the majority of the lung. the patient had a long history as a coal mine worker, and the microscopic sections revealed abundant anthracotic pigment and scarring in this area. binding sites for nfat have been found in the promoter region of the tnfa gene. the mediation of silica-induced tnfa transcription is probably via o 2-but not h 2 o 2 [280, 281] . atresia of the lung represents a premature closure of the airway at any level of the bronchial tree including the lobar, segmental, or subsegmental airways. clinically, these children usually present between 10 and 20 years of age for symptoms of dyspnea, wheezing, recurrent pneumonias, or for incidental findings on a chest imaging study. these lesions are more common in the proximal segmental bronchi, right more often than left. when atresia is associated with anomalies of the vascular supply to the affected airway, the lesion represents a separate, aberrant segment of lung known as a sequestration, either intralobar or extralobar type. the pathology of bronchial atresias and sequestrations represents sequelae of chronic inflammation due to the accumulation of secretions in these blind-end airways. these features consist of cystically dilated airways with mucus and parenchymal fibrosis with honeycomb changes. in intralobar sequestrations (ils), the anomalous vessel is a muscular artery that enters through the pleura from an aortic source, usually from the thoracic area. ils are separate, isolated areas of lung invested with the normal visceral pleura without bronchial or arterial connections (figure 18 .68). extralobar sequestrations (els) are pyramid-shaped accessory pieces of lung that have their own pleura with an artery from the lung but without airway connections. the category of congenital pulmonary cystic diseases represents the majority of congenital pulmonary disease and includes foregut cysts and cystic adenomatoid malformations. foregut cysts include bronchogenic, esophageal, and thymic cysts that form from defects in the foregut branching. clinically, these cysts are usually incidental findings on chest imaging studies, but they can present with complications due to infection or hemorrhage. pathologic features of these cysts include subtle differences that are usually only apparent after microscopic examination. grossly, these cysts usually arise proximally either within the mediastinum (over 50%) or in the proximal regions of the lungs, right more commonly than left, along the esophagus, and rarely within the lung parenchyma or below the diaphragm [282] . microscopically, each cyst contains a simple cuboidal or columnar epithelium, ciliated or nonciliated, that may undergo squamous metaplasia. distinguishing among the three types of cysts requires the presence of other elements. bronchogenic cysts have submucosal glands and/or hyaline cartilage within their walls, and thymic cysts may contain residual thymus. congenital cystic adenomatoid malformations (ccam), now more commonly referred to as congenital pulmonary airway malformations (cpam), are segments of lung with immature airways and alveolar parenchyma. these are usually classified by their predominant cyst size into types 0-4. type 1 cysts, which contain a main large cyst of up to 10 cm, are the most common. these cysts are distinguished from foregut cysts upon the recognition in the cpam of immature alveolar duct-like structures connecting to the surrounding lung parenchyma. this type of cpam is also notable, as it is known to undergo malignant transformation, usually to mucinous bronchioloalveolar cell adenocarcinomas. these anomalies arise due to defects during the various stages of development and are best considered within these developmental stages. the embryonic stage occurs within the first 3-7 weeks of life when the ventral wall of the foregut separates into the trachea and esophagus and branches to form the left and right lungs. the splanchnic mesenchyme that surrounds this foregut forms the vascular and connective tissues of the lungs. defects in this phase result in complete lack of lung development known as pulmonary agenesis and incomplete separation of the trachea and esophagus, causing tracheal-esophageal atresias and fistulas. the pseudoglandular stage, between weeks 7-17 of development, is a time of rapid development of the conducting airways including the bronchi and bronchioles and the expansion of the peripheral lung into the acinar buds. the mesenchymal tissue figure 18 .68 intralobar sequestration. the tan and white mass involving this left lower lobectomy specimen represents chronic pneumonia and fibrosis in the sequestered area of the lung. the dilated airways are features of an endstage fibrosis that is commonly found in this entity. part iv molecular pathology of human disease that surrounds these buds begins to thin, becomes vascularized, and forms the cartilage that surrounds the more proximal branching airways. during the canalicular (week [17] [18] [19] [20] [21] [22] [23] [24] , saccular (weeks [24] [25] [26] [27] [28] [29] [30] [31] [32] [33] [34] [35] [36] [37] [38] , and alveolar (weeks 36 to maturity) stages of development, the acinar buds continue to expand, and the mesenchyme surrounding this continues to thin. during the canalicular stage, the pulmonary vascular bed begins to organize, the distance between the blood in the vascular spaces and the air in the alveoli narrows, and the respiratory epithelium begins to form. the gas exchange unit of the alveolus becomes functional during the saccular stage with further differentiation of the respiratory epithelium to include clara cells, ciliated and nonciliated cells, and type 2 cells with the first production of surfactant occurring during this period. this gas exchange unit continues to mature during the alveolar stage with the growth and septation of the alveoli. this process continues postnatally through 6-8 years of age. the different types of cpams arise at different stages of development. cpams 0, 1, and 2 are a result of defects during the early embryonic and pseudoglandular stages of development, producing pathology with features of primitive alveolar buds and immature and abnormal airway cartilage structures. cpams 3 and 4 result from abnormal formation of the more distal airways and pulmonary parenchyma during the canalicular, saccular, and alveolar phases, causing pathology with immature alveolar, or alveolar simplification with enlarged alveoli [283] . various genetic defects in the pathways that control lung morphogenesis have been associated with these congenital lung diseases. two major transcription factors are responsible for the normal branching morphogenesis. the first, thyroid transcription factor-1 (ttf-1), is a member of the nkx2.1 family of hemeodomain-containing transcription factors. this factor plays a role in the lung epithelial-specific gene expression and proper lung bud development in the embryonic stage, as well as in the maturation of the respiratory epithelium. the second major factor is somatic hedgehog (shh)/gli, expressed by endodermally derived cells and required for branching morphogenesis. the development of the lung bud from the foregut endoderm depends on the appropriate expression of these lung-specific genes at the correct time in development. in the presence of genetic defects, aberrant lung development may occur. for example, mutations of various types in the shh/gli gene have been found to cause tracheoesophageal fistulas, anomalous pulmonary vasculature, and aberrant airway branching. also, deletions in the ttf-1 gene are associated with tracheoesophageal fistulas and a variety of forms of lung dysgenesis [284] . finally, factors present in the surrounding mesenchyme play a role in inducing the proper development of the pulmonary endoderm. a prominent mesenchymal factor in this process is fibroblast growth factor (fgf), which modulates both the proximal and distal lung branching morphogenesis. deletions in this gene may cause lung agenesis and tracheal malformations [284] . surfactant dysfunction disorders represent a heterogenous group of inherited disorders of surfactant metabolism, found predominantly in infants and children. pulmonary surfactant includes both phospholipids and surfactant proteins, designated surfactant proteins a, b, c, and d (sp-a, sp-b, sp-c, sp-d), synthesized and secreted by type 2 cells beginning in the canalicular stage of lung development. damage to type 2 cells during this time period can lead to acquired surfactant deficiencies. however, more commonly these deficiencies are the result of genetic defects of the surfactant proteins themselves. the major diseases are caused by genetic defects in the surfactant protein b (sftpb, chromosome 2p12-p11.2); surfactant protein c (sftpc, chromosome 8p21); and adenosine triphosphate (apt)-binding cassette transporter subfamily a member 3 (abca3, chromosome 16p13.3). defects in sftpb and abca3 have an autosomal recessive inheritance pattern, and defects in sftpc have an autosomal dominant pattern. sp-b deficiency is the most common. it presents at birth with a rapidly progressive respiratory failure and chest imaging studies showing diffuse ground glass infiltrates. the gross pathology in these lungs consists of heavy, red, and congested parenchyma with microscopic features that range from a pap-like pattern to a chronic pneumonitis of infancy (cpi) pattern. in sp-b deficiency, the pap pattern predominates with a histologic picture of cuboidal alveolar epithelium and eosinophilic pas-positive material within the alveolar spaces that appears with disease progression. in the late stages of the disease, the alveolar wall thickens with a chronic inflammatory infiltrate and fibroblasts. this alveolar proteinosis-type pattern of injury can be confirmed with immunohistochemical studies that establish the absence of sp-b within this surfactant-like material. diseases due to abca3 or sftpc deficiency may present within a week of birth or years later; the former has a poor prognosis, but the latter has a more variable prognosis with some patients surviving into adulthood. indeed, sp-c mutations have also been recognized in some families as a cause of interstitial pneumonia and pulmonary fibrosis in adults [285] . the pathology of sp-c deficiency has more cpi features and less proteinosis. in contrast, abca deficiency can have either pap or cpi features, with the former present early in the disease and the latter present in more chronically affected lungs [286] . the sp-b gene (sftpb) is approximately 10 kb in length and is located on chromosome 2. there are over 30 recessive loss-of-function mutations associated with the sftpb gene. however, the most common mutation is a gaa substitution for c in codon 121, found in about 70% of the cases. the lack of sp-b leads to an abnormal proportion of phosphatidylglycerol and an accumulation of a pro-sp-c peptide, leading to the alveolar proteinosis-like pathology. sp-c protein deficiency is due to a defect in the sftpc gene localized to human chromosome 8. there are approximately 35 dominantly expressed mutations in sftpc that result in acute and chronic lung disease. approximately 55% of them arise spontaneously, and the remainder are inherited. the most common mutation is a threonine substitution for isoleucine in codon 73 (i73t), found in 25% of the cases, including both sporadic and inherited disease [287] . this mutation leads to a misfolding of the sp-c protein, which inhibits its progression through the intracellular secretory pathway, usually within the golgi apparatus or the endoplasmic reticulum [288] . the absence of sp-c within the alveolar space causes severe lung disease in mouse models. infants with documented mutated prosp-c protein, the larger primary translation product from which sp-c is proteolytically cleaved, can have respiratory distress syndrome (rds) or cpi. in older individuals, pathologic patterns observed in the lungs with these mutations include nonspecific interstitial pneumonitis (nsip) and uip. in this affected adult population, the pathology and age of disease presentation vary even within familial cohorts, suggesting the involvement of a second hit, perhaps an environmental factor [289] . the abca3 protein is a member of the family of atpdependent transporters, which includes the cftr, and is expressed in epithelial cells. mutation in this gene results in severe respiratory failure that is refractory to surfactant replacement. the cellular basis for the lack of surfactant in patients with this genetic mutation is not known. the presence of abnormal lamellar bodies within the type 2 cells by ultrastructural analysis suggests a disruption in the normal surfactant synthesis and packaging in 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cord-017248-a37t31u1 authors: nan title: alphabetic listing of diseases and conditions date: 2010-05-17 journal: handbook of autopsy practice doi: 10.1007/978-1-59745-127-7_17 sha: doc_id: 17248 cord_uid: a37t31u1 part ii begins with a list of special histologic stains, their for use and their corresponding references. at the end of this list is a procedure for removal of formalin precipitate from tissue sections. diseases. there may also be a list of possible associated conditions. these entities are generally linked pathogenetically to the main disease entry. any asterisk after a related disease indicates that that disorder is also listed as a disease entry. many disease entries will be followed by a three-column table that provides the reader with a listing of the pathologic findings to be expected with the disease as well as the prosection and dissection procedures necessary to demonstrate those findings. it is expected that routine hematoxylin-eosin stains will be done on all sections submitted for histologic examination. special stains will be recommended in the procedures column of the tables, when indicated. any table immediately following the two columns of disease entries always refers to the disease in the right column. prepare smears of undiluted blood. obtain blood for molecular studies for preservation of small intestinal mucosa and for preparation for study under dissecting microscope, see part i, chapter 2. submit sample for histologic study. submit stool for chemical analysis. record weight and submit sample for histologic study. freeze liver for molecular studies record appearance of spine (see also chest roentgenogram). for removal and specimen preparation, see chapter 4. request luxol fast blue stain. for removal and specimen preparation, see chapter 5. below-normal weight in infants. kyphoscoliosis. very low concentrations of cholesterol and decreased triglycerides; serum~-lipoprotein or absent; a.-lipoproteins present. acanthocytosis (spiny red cells). gene mutations (4) . abnormal shape of villi; vacuolation of epithelial cells. fatty stools fatty changes. gene mutations (4) systemic manifestations of malabsorption syndrome* and of vitamin a deficiency. * kyphoscoliosis. axonal degeneration of the spinocerebellar tracts; demyelination of the fasciculus cuneatus and gracilis (2) . possible involvement of posterior columns, pyramidal tracts, and peripheral nerves. atypical retinitis pigmentosa (2) with involvement of macula. angioid streaks (3) . synonym: cerebral abscess. note: for microbiologic study of tissues and abscesses, see part i, chapter 7. include samples for anaerobic culture. it is best to study the brain after fixation but if specimen is examined fresh, aspirate and prepare smears of abscess content. photograph surface and coronal slices of brain. request giemsa stain, gram stain, pas stain, and grocott's methenamine silver stain for fungi. external examination if there is evidence of trauma, see also under "injury, head." prepare roentgenograms of chest and skull. submit for microbiologic study. for removal and specimen preparation, see chapter 4. for microbiologic study, photography, and special stains, see under "note." for exposure of venous sinuses, see chapter 4. sample walls of sinuses for histologic study. for exposure of paranasal sinuses, mastoid cells, and middle ears, see chapter 4. for removal and specimen preparation, see chapter 5. procedures depend on suspected lesions as listed in right-hand column. skin infections in upper half of face. edema of forehead, eyelids, and base of nose, proptosis, and chemosis indicate cerebral venous sinus thrombosis. * trauma; craniotomy wounds. skull fracture and other traumatic lesions. for possible intrathoracic lesions, see below under "other organs." the national transportation safety board (ntsb)* has authority over aircraft wreckage and the legal authority to investigate and to determine the cause of air crashes. (1) the dead are the responsibility of the medical examiner or coroner. local police will seal off the area of the crash. other than for the purpose of determining that death has occurred, no one should be allowed to approach the bodies or any objects until the identification teams and the medical examiner or coroner have taken charge. the sudden influx of bodies after a commercial air carrier accident and the request for speedy identification of the victims would overburden almost any institution. managing such a disaster is eased by writing a contingency plan beforehand. temporary morgue facilities may have to be established near the scene of the crash. refrigerated trucks may serve as storage space. a practical approach is to deal first with those bodies that seem to be the easiest to identify, in order to narrow the field for the more difficult cases. if bodies are scattered, their locations can be referenced to stakes in the ground or spray paint on pavement; only then should these bodies (or parts) and personal effects be collected. for large-scale crashes a locations can be referenced to a string-line grid benchmarked to gps coordinates. records and diagrams of the relative positions of victims are prepared during this phase. if bodies are still within the airplane, their positions are recorded, and photographed. the personnel of the medical examiner or coroner can augmented by d-mort team staffed by forensic pathologists, anthropologists, dentists, morgue technicians, and investigators supplied by the national disaster medical system. ** the airline will provide a list of the passengers and the federal bureau of investigation (fbi) disaster team will make itself available to take and identify fingerprints and aid in the acquisition of other identifying data such as age, race, weight, height, and hair color and style. if dental records can be obtained, this provides one of the most certain methods of identification. a medical history indicating amputations, internal prostheses, or other characteristic surgical interventions or the presence of nephrolithiasis, gallstones, and the like will be helpful. fingerprints (and footprints of babies) should be taken in all instances. wallets with identification cards,jewelry, name tags in clothing, or other personal belongings may provide the fastest tentative identification. the medical examiner may elect to autopsy only the flight crew but not the passengers of an aircraft crash. however, the grossly identifiable fatal injuries should be described, photographed, and x-rayed. this may reveal identifying body changes. if comparison of somatic radiographs, dental records, fingerprints, or photographs do not identify the victim, dna comparison must be considered. burned or fragmented bodies of passengers and the bodies ofcrew members, and particularly the pilots, must have a complete autopsy, including roentgenographic and toxicologic examinations, which must always include alcohol and carbon monoxide determinations. internal examination might reveal a coronary occlusion, or roentgenograms may disclose a bullet as evidence that violence preceded the crash. in some airplane crashes, particularly in light airplane accidents, suicide must be considered. in such cases police investigation is required to determine if the pilot exhibited suicidal ideation in the recent past.. when resources permit, autopsies should be performed on all deceased occupants of aircraft crashes, including passengers, in order to distinguish among blunt impact trauma, smoke inhalation, and flash fires as causes ofdeath, and to answer future questions concerning pain and suffering, intoxication, and sequence of survivorship. after a crash victim has been identified, the coroner or medical examiner will issue a death certificate. if remains of a decedent cannot be found, a judge can, upon petition, declare a passenger dead and sign a death certificate prepared by a medical examiner. *phone # ofntsb command center: 202-314-6000 **phone # of dmort: 800-872-6367. entry should be followed. usually, the circumstances that led to drowning are not apparent from the autopsy findings but can be reconstructed from reports of witnesses and the police. because the reflex drive to seek air is triggered by hypercarbia, not hypoxia, loss of consciousness and drowning can ensue after hyperventilation and breath-holding by experienced swimmers who then drown without a struggle. there are no specific autopsy findings. a search for trauma, including a posterior neck dissection, should be made in all instances. head and cervical injuries may be responsible for loss of consciousness and drowning, usually in individuals diving into shallow water. toxicologic examination as described below for scuba diving accidents is always indicated. with scuba diving fatalities, investigation of the equipment and circumstances is usually more important than the autopsy. scuba fatalities should be studied by or with the aid of diving experts-for instance, members of a diving club or shop (not the one providing the gear used by the decedent) or the u.s. navy. (1) careful investigation of the scene and study of reports of witnesses and the police are essential. the investigation should ascertain the site of diving (currents and other underwater hazards), the estimated depth, the water temperature (exposure to cold), and a description of water clarity. electrocution should be considered if the site has electric underwater cables (see "injury, electric"). cerebral concussion should be considered if explosives were used in the vicinity. knowledge of the method of recovery of the body and the type of resuscitation efforts can aid in the interpretation of apparent wounds. the medical history of the diving victim should be sought, as it may lead to a diagnosis for which the autopsy is typically silent, such as seizure disorder, or may reveal asthma, emphysema, or chronic bronchitis, all of which increase the risk of air trapping and arterial air embolism. although drowning may be the terminal event in some scuba deaths, the investigation should be focused on the adverse environmental and equipment factors that place a capable swimmer at risk of drowning (see "embolism, air" and "sickness, decompression"). because scuba divers risk arterial air embolism if they ascend with a closed glottis, on can attempt to document gas bubbles at autopsy, but their interpretation is problematic: bodies recovered immediately are subjected to resuscitation efforts, which can by themselves produce extra-alveolar air artifacts, and bodies not recovered immediately tend to be found in a putrefied condition, full of postmortem gas. in the remaining cases, the pathologist must consider the potential of introducing artifactual gas bubbles by the forcible retraction of the chest plate and by sawing the calvarium. the following procedures apply primarily to scuba diving accidents. interrogation of witnesses is important; the behavior and complaints of the decedent, if any, might help distinguish between a natural death by heart disease and an unnatural death by air embolism. external examination eyes and ears head (skull and brain) chest blood (from heart and peripheral vessels) heart tracheobronchial tree and lungs a procedures photograph victim as recovered and after removal of wet suit and other diving gear. record condition of clothing and gear. impound all diving equipment for study by experts, particularly scuba tank, breathing hoses, and regulators. residual air in tank should be analyzed. record color of skin (including face, back, soles, palms, and scalp). palpate skin and record presence or absence of crepitation. record extent and character of wounds. prepare histologic specimens. record appearance of face (including oral and nasal cavities) and of ears. prepare roentgenograms. if air embolism must be expected, as in the presence of pneumomediastinum, follow procedures described under "embolism, air." for evaluation of findings, see also above under "note." if decompression sickness (caisson disease) is suspected, also prepare roentgenograms of the elbows, hips, and knees. otoscopic examination. funduscopic examination. save vitreous for possible toxicologic and other studies. for removal of brain, see chapter 4. record contents of arteries of the circle of willis and its major branches and basilar artery. strip dura from base of skull and from calvarium. for removal and specimen preparation, see chapter 4. for demonstration of pneumothorax, see under "pneumothorax". if gas is visible in coronary arteries, photograph. photograph and aspirate gas in heart chambers. submit samples of heart blood and peripheral blood for toxicologic study and drug screen. examine lungs in situ. save bronchial washings for analysis of debris. fresh dissection is recommended. if decompression sickness is suspected, prepare sudan stains from fresh-frozen lung sections. complete toxicologic sampling should be carried out (see chapter 13). record nature of gastric contents. remove neck organs toward end of autopsy. for posterior neck dissection, see chapter 4. incise tongue. for removal, see chapter 4. for removal, see chapter 4. for removal, prosthetic repair, and specimen preparation, see chapter 2. consult roentgenograms. in decompression sickness, fatty change of liver, and ischemic infarctions of many organs. interstitial emphysema. aspiration (see above). trauma to cervical spine. mottled pallor of tongue after air embolism. contusion of tongue after convulsive chewing. nitrogen bubbles in spinal cord arteries may occur after rapid ascent. air embolism;' cerebral edema in decompression sickness. aseptic necroses (infarcts, "dysbaric osteonecrosis"), most often in head of femur, distal femur, and proximal tibia. infarcts indicate repeated hyperbaric exposures. nitrogen bubbles in and about joints and in periosteal vessels ("bends") occur during rapid ascent. related terms: automobile accident; motorcycle accident. note: a visit to the scene can make the interpretation of the autopsy findings easier. the vehicle can also be inspected in a more leisurely fashion at the impound lot. this is particularly useful for correlating patterned injuries with objects in the vehicle. most vehicular crashes occur as intersection crashes or because a vehicle with excessive speed left a curved road. the medical examiner or coroner should gain a basic understanding of the crash mechanism so that informed descriptions can be rendered, e.g., "impact to the b pillar of the decedent's automobile by the front of a pickup truck which failed to stop for a stop sign at an intersection, resulting in a 2-feet intrusion into the cabin; restraint belts not employed; air bag deployed; extrication required which took 15 minutes." police are responsible for determining mechanical and environmental risk factors for the crash and for determining some human risk factors such as suicidal or homicidal intent. the pathologist determines other risk factors for crashes such as heart disease, a history of epilepsy, and intoxication by carbon monoxide, drugs, and alcohol. suicide as a manner of death should be considered when a single-occupant vehicle strikes a bridge abutment or a large tree head-on, with no evidence of evasive action or braking. in such a situation, the standard police traffic investigation should be supplemented of interviews of the victim's family and friends. the ambulance run sheet is an invaluable source of observations that often are not available from the police. this document should be acquired in all instances, even if the paramedics determined that death occurred and did not transport. the basic autopsy procedures are listed below. most traffic victims who die at the scene or who are dead on arrival at the hospital died from neurogenic shock caused by wounds of the head or vertebral column, or from exsanguination from a tom vessel or heart. as such, they have little lividity, and little blood is found in the vehicles. presence ofintense lividity may indicate suffocation or heart disease as a cause of death. if postural asphyxia is suspected, the first responders to the scene should be interviewed to determine the position of the decedent in the vehicle, and the vital signs, ifany, ofthe decedent from the time of the crash to the time of extrication. posterior neck dissection is indicated in these instances. if manifestations of heart disease, intense lividity, and absence oflethal wounds suggest that a crash occurred because the driver was dead, other drivers on the road may have observed that the victim was slumped at the wheel before the crash. the determination of heart attack at the wheel is usually simple, because most such victims realize that something is wrong, and bring the vehicle to a stop at the side of the road, or coast gently into a fixed object. in such instances, damage to the vehicle is minor, and wounds to the decedent are usually trivial. while pattemed wounds can often be matched to objects (see below), patternless wounds usually cannot be visually matched to specific objects, although an opinion can sometimes be given as to what object was struck, based on the direction of motion and position ofthe body with respect to the vehicle. impacts with the a-pillar produce narrow vertical zones of facial laceration and fractures extending from forehead to jaw. tempered glass shatters into small cubes on impact, and leaves so-called "dicing" wounds, which are abraded cuts arranged in a somewhat rectilinear pattern. windshield glass leaves shallow, abraded, vertically oriented cuts on the face or scalp. with pedestrians, the lower extremities are of particular forensic interest, to determine the height and direction of impact from vehicles that left the scene. scalp hair and blood should be collected from such "hit and run" victims and from occupants of a suspect car if police have a question as to which occupant was the driver; these exemplars can be compared to fibers and tissue recovered from the vehicle in question. likewise, foreign material in wounds can sometimes be matched to suspect vehicles, and should be sought and retained as evidence. for pedestrians, the distance between the impact point on the lower extremities and the soles of the feet should be recorded. the legs should be opened to inspect tibial fractures; cortical fractures initiate propagation opposite to the side of impact, where they usually have a pulled-apart appearance, and then splinter the cortex at the side of impact. abrasions are better impact markers than contusions, because subcutaneous blood extravasation can be caused not only by impact to the skin, but also from blood extravasating from underlying fractures. if no cutaneous abrasions or fractures of the leg bones are found, the skin of the legs should be incised to expose contusions. fracture descriptions should include location in the bone (e.g., proximal metaphysis or shaft), whether the fracture is complete or incomplete, and whether the fracture is displaced or distracted. lacerations of intervertebral disks, facet joint capsules, and ligamenta flava should not be loosely termed "fractures." the presence or absence of blood extravasation in soft tissue adjacent to the fractures should be recorded, and its volume estimated if it appears severe enough. venous air embolism from tom dural sinuses cannot be diagnosed without a pre-autopsy chest radiograph or an in situ bubble test. if an x-ray machine is readily available, an anterior-posterior chest radiograph should be obtained in every traffic victim who dies at the scene or after a failed resuscitation attempt. if a hemothorax is suspected, the rib cuts should be placed further lateral and the chest plate reflected so that the internal mammary vessels can be inspected before the chest plate is removed. after measuring and removing the bloody effusion, the underlying serosal surfaces should be inspected for defects. lacerations of the heart and aorta will be obvious. tamponaded lacerations of the aorta, around which the adventitia still holds, must be noted as such. if no lacerations are found at the usual sites, lacerations of the azygous veins must be considered, especially in association with fracture dislocations of the thoracic vertebral column; other sites are the internal mammary arteries, especially with fractures of ribs i and 2 or of the sternum, and intercostal arteries with displaced rib fractures. only after the serosal defect is identified should the organs be removed, because that procedure creates many more holes in the serosa. for that reason, as much information as possible should be gained by in situ observation. the only evidence of concussion of the heart may be a cardiac contusion or a sternal fracture. the usual clinical history suggests cardiovascular instability that is not associated with craniocerebral trauma and which does not respond to the infusion of intravenous volume agents. the autopsy assistant may saw but should not retract the skull cap and remove the brain. the pathologist should observe in situ whether shallow lacerations of the pontomedullary junction with stretching of the midbrain are present. these lesions cannot be distinguished from artifact by examining the brain later. thus, only after appropriate in situ inspection should the pathologist remove the brain. a posterior neck dissection is required if no lethal craniocerebral or cardiovascular trauma is found, or if suffocation is suspected; neck trauma must be ruled out to diagnose suffocation in a traffic fatality. sudden death in a patient with seemingly trivial wounds may be caused by undiagnosed trauma of the craniocervical articulation. a posterior neck dissection is required in these instances. the diagnosis of diffuse axonal injury of the brain in victims with no appreciable survival interval requires that suffocation be ruled out and that no resuscitation from a cardiac arrest has been attempted. clinicians are quick to apply the label "closed head injury" when a victim of a traffic crash has cerebral edema on a computerized axial tomogram of the head, even if no cerebral contusions, scalp contusions, or skull fractures are evident. this may be a misinterpretation, because cerebral edema can be caused by hypoxic encephalopathy made evident after resuscitation from a cardiac arrest, or from hypoxia caused by suffocation. procedures possible or expected findings record presence of lividity. photograph all external wounds; measure all lacerations and any abrasions or contusions with a pattern. collect scalp hair and blood (see below) from victims of hit and run accidents. collect foreign material in wounds. intense lividity and absence of lethal wounds may indicate that the crash occurred because the driver was dead from heart disease or suffocation. wound documentation. patterned injuries often sometimes be matched to objects in or about the vehicle (the most common patterned wound is that from tempered glass; see above under "note"). impact patterns in pedestrians may help to reconstruct the accident. hair and blood of the victim may be matched to transfer evidence on a vehicle suspected of having left the scene. part ii / diseases and conditions internal examination of body cavities heart and great vessels abdomen skull and brain; neck soft tissue compartments at any location prepare roentgenograms of chest is cases with head impact and skull fractures. collect samples for toxicologic study from all victims, including passengers. create pleural window to detect pneumothorax. if blood is seen, examine internal mammary vessels (see under "note"). measure volume of blood in cavity bleeds, and note whether chambers of heart and great vessels are collapsed or filled. record evidence of cardiac contusion, sprain of intracardiac inferior vena cava, laceration of pericardial sac, and fracture of sternum. laceration of heart or great vessels (measure volume of blood). follow routine procedures for dissection of heart and great vessels (see chapter 3) . in situ bubble test to confirm venous air embolism. record evidence of trauma and volume of blood in peritoneal cavity; estimated volume of blood in retroperitoneal soft tissues. autopsy assistant may saw the skull but pathologist should inspect brain in situ and remove it personally. for removal and specimen preparation of brain, see chapter 4. record brain weight. posterior neck dissection is indicated if there is no craniocerebral or cardio-vascular trauma, or if suffocation is suspected. record evidence of trauma and estimate volume of blood. venous air embolism.' evidence of alcohol or drug intoxication. pneumothorax, hemothorax, e.g., after laceration of internal mammary vessels. evidence of significant hemorrhage. indirect evidence of cardiac concussion. evidence of exsanguinating wounds. evidence of cardiovascular disease that may have felled the driver before the crash. in european countries, the concentration is expressed in promille (grams per liter). in the united states, it has become customary to refer to concentration by percentage (grams per deciliter), and values in these units have been written into legislation and included in the uniform vehicle codes. unless qualified, the use of promille or percentage does not indicate whether the result of the analysis is weight/weight, weight/ volume, orvolume/volume. another common way ofexpressing concentration, milligrams per deciliter, has also been used to indicate alcohol concentrations. the method ofexpressing concentration must be clearly specified whenever the alcohol level is mentioned. the desired expression canbe derived from the toxicologic report by using the following equation: i,000~g/ml =100mg/dl =0.10g/dl =21.74 mmolll =1.0 promille =0.10% what is the legal interpretation of alcohol (ethanol) intoxication? objective impairment of driving ability is observed at threshold blood alcohol concentrations of .035-.040 g/dl. as of august 2005 all states and the district of columbia have adopted laws that make it criminal offense for a driver to operate a motor vehicle with a blood alcohol concentration of 0.08 g/ dl or greater. many states have an enhanced penalty for high concentrations such as 0.15 g/dl or above. several states have zero tolerance laws, under which drivers who are minors are legally operating only if their blood alcohol concentration is 0.02 g/dl or less, and in some states, not detectable at all. blood alcohol concentrations obtained at autopsy are valid until putrefaction begins. specimen tubes with sodium fluoride should be used, and the specimen should be stored in the refrigerator. if the air space above the blood samples in the container is large, alcohol can evaporate and a falsely low blood alcohol level can result. putrefactive changes before autopsy or during storage may cause a falsely high blood alcohol concentration. ethanol can be produced in the specimen container; this is more likely in the absence of a preservative. because fluoride inhibits bacteria far more than fungi, higher fluoride concentrations are required for the inhibition of fungal growth (4) . although there is no major difference in the alcohol concentrations ofblood samples from the intact heart chambers and the femoral vessels (5), autopsy samples from pooled blood in the pericardial sac or pleural cavity are unsatisfactory. we therefore recommend that blood be withdrawn from peripheral vessels. is there normal "endogenous" blood alcohol (ethanol) in a living person? blood alcohol concentrations are generally believed to be negligible in the absence of ingested alcohol. "endogenous" ethanol in human blood exists at a concentration of about 0.0002 g/dl, which is below the limit of detection for most methods (6) . first in such a list would be postural asphyxia, for example, in drunks who fall asleep face down. also, depressant drugs in the tricyclic, analgesic, barbiturate, and benzodiazepine classes all potentiate the effect of alcohol (7) . also included in such a list would be infancy and childhood; ischemic heart disease;' chronic bronchitis and emphysema;' other chronic debilitating diseases; poisoning with carbon tetrachloride' or carbon monoxide;' and other causes of hypoxia.' how can one estimate blood alcohol (ethanol) concentrations from vitreous, urine, or tissue alcohol levels and from alcohol in stomach contents? the ratio of serum, plasma, urine, vitreous, and various tissues has been compiled by garriot (8) . the values may vary considerably. for vitreous, the ratios varied from 0.46-1.40. these variations may depend on whether blood alcohol concentrations were increasing or decreasing at the time of death. most other body fluids and tissues showed ranges closer to 1. most urine values were above the blood alcohol concentrations. in another study (9) , the blood/vitreous (bn) ratio in the early absorption phase was 1.29 (range, 0.71-3.71; sd 0.57) and in the late absorption and elimination phase, the bn ratio was 0.89 (range, 0.32-1.28; sd 0.19). blood ethanol concentrations probably can be estimated using b =1.29v for early absorption and b = 0.89v for later phases. a urinelblood ethanol ratio of 1.20 or less indicates that the deceased was in the early absorption phase. how can one use alcohol (ethanol) concentrations in postmortem specimens to estimate the blood alcohol concentration at various times before death? with certain limitations, one can base calculations of this kind on the assumption that the blood alcohol level decreases from its peak at a fairly constant rate of 0.015-q.018g/dl/h until death (10) . if blood is not available, conversion factors (see above) must be used. alcoholics have been reported to metabolize at a rate of up to 0.043 g/dl/h (6) . example: the driver of an automobile drinks at a party until midnight. he leaves his host at about 1:30 a.m. and is involved in a head-on collision at 2:15 a.m. he dies in the emergency room at 6:35 a.m. there are multiple injuries and the patient exsanguinates. the autopsy is done at 1:30 p.m. although this appears quite unlikely, let us assume that no satisfactory blood sample was obtained before death and that no blood or plasma expanders were given. if under such circumstances the alcohol concentration in the vitreous was found to be 0.157 g/dl, what was the alcohol concentration in the blood at the time of the accident? vitreous and blood alcohol concentrations may be assumed to have remained unchanged after death. therefore, the blood alcohol level at the time of death must have been approx 0.157 (vitreous humor alcohol) x 0.89 (conversion factor, see above) = 0.14g/dl. the time interval between the accident (2:15 a.m.) and death (6:35 a.m.) is 4 hand 20 min or 4 1/3 h. if we assume that the decedent was not an alcoholic and that the blood alcohol concentration was decreasing from its peak at a constant rate of 0.015 g/dl/h, then the concentration at the time ofthe accident is estimated to have been 0.14 (concentration at time of death) + (4 1/3 x 0.015) = 0.140 + 0.065 = 0.205 g/dl or 0.2%. the blood alcohol concentration at the time of the accident could have been lower if the victim stopped drinking later than 1h or 1 1/2 h before the accident. in the latter case, the peak alcohol level would have occurred after the accident, reflecting the time to absorb the latest drink. the blood alcohol concentration at the time of the accident could have been lower or higher if the time when the patient stopped drinking, the time of the accident, or the time of the death is uncertain. the blood alcohol concentration at the time of the accident could have been higher if the victim was a chronic alcoholic. the elimination rate in such persons may be as high as 0.040 mg/dl, which would change the figures in our example above to 0.140 + (4 1/3 x .040) =0.140 + 0.173 = 0.313 g/d1 or 0.3%. only rough estimates are possible. first, the peak blood alcohol level must be determined or calculated, as described in the previous paragraphs. tables (see below) are available that relate blood alcohol level to the minimal amounts of whiskey, wine, or beer that must have been consumed (10) . however, tables of this type are often based on the minimum amount of alcohol circulating in the body after specific numbers of drinks; such tables do not yield reliable results if used conversely. furthermore, inasmuch as drinking and elimination of alcohol may take place concomitantly, over a longer period the total amount of alcohol consumed may have been much greater than the tables would indicate. it cannot be lower. according to these tables, 6 pints of ordinary beer or 8 fl oz of whiskey would be the minimal amounts needed to produce a blood alcohol level of about 200 mg/dl in a person weighing 140-180 pounds. the total body alcohol can be calculated from the blood alcohol level by using widmark's formula: average concentration of alcohol in entire body = .68 concentration of alcohol in the blood in a person weighing 70 kg, the blood alcohol concentration would be increased 50 mg/dl (0.05%) by the absorption of 1oz of ethanol (20z of 100-proof whiskey). strength of alcohol is measured in "proof'; absolute alcohol is 200 proof. therefore, in the united states, alcohol content as volume percent is half the proof (for example, 100-proof whiskey contains 50% alcohol by volume). the alcohol content of various beverages is shown in the following table. approximate alcohol content in various beverages t toata from glaister, rentoul e. medical jurisprudence and toxicology, 12th ed. e & s livingstone, edinburgh, 1966 with permission. twithin 1 h after consumption of diluted alcohol (approx 15%) on an empty stomach, assuming body weight of 140-180 pounds (63.6-81.7 kg) reproduced from (11) with permission. *one ounce (about 30ml) of whiskey or 120z (about 355ml) of beer. what is the toxicity of alcohol other than ethanol? in general, the toxicity increases as the number of carbon atoms in the alcohol increases. thus, butyl alcohol is two times as toxic as ethyl alcohol: but isopropyl alcohol is only twothirds as toxic as isobutyl alcohol and one-half as toxic as amyl alcohol. primary alcohols are more toxic than the corresponding secondary isomers (10) . anemia, hemolytic synonyms and related terms: acquired hemolytic anemia; extracorpuscular hemolytic anemia; hereditary hemolytic anemia (hereditary elliptocytosis, pyropoikilocytosis, stomatocytosis. spherocytosis); immunohemolytic anemia; intracor-puscular hemolytic anemia; microangiopathic hemolytic anemia; spur cell anemia. possible associated conditions: disseminated intravascular coagulation;* eclampsia;* glucose-6-phosphatase deficiency (g6pd); hemolytic uremic syndrome;* malignant hypertension; lymphoma* and other malignancies; paroxysmal nocturnal hemo-globinuria; sickle cell disease;*thalassemia;* thrombotic thrombocytopenic purpura.* (see also below under "note.") note: hemolysis also may be caused by conditions such as poisoning with chemicals or drugs, heat injury, snake bite,* or infections or may develop as a transfusion reaction* or be secondary to adenocarcinoma, heart valve prostheses (see below), liver disease (see below), renal disease, or congenital erythropoietic porphyria. * procedures prepare skeletal roentgenograms. jaundice; skin ulcers over malleoli. in young patients: thickening of frontal and parietal bones with loss of outer table ("hairon-end" appearance); paravertebral masses caused by extramedullary hematopoiesis; deformities of metacarpals, metatarsals, and phalanges. osteonecrosis* of femoral heads. remove and place in fixative as early as possible in order to minimize autolysis (alternatively, formalin can be injected in situ; see below). samples should include oxyntic corpus and fundus mucosa. record weights. submit tissue samples for histologic study. record weight of thyroid gland. for removal and specimen preparation, see chapter 4. request luxol fast blue stain. for removal and specimen preparation, see chapter 5. if there is a clinical diagnosis of anemia-related amblyopia, follow procedures described under "amblyopia, nutritional." jaundice. manifestations of malnutrition. * stomatitis with cheilosis and perianal ulcerations due to folic acid deficiency. chronic exfoliative skin disorders. vitiligo. macrocytosis; poikilocytosis; macroovalocytes; hypersegmentation of leukocytes; abnormal platelets. atrophic glossitis with ulcers. pharyngoesophagitis (folic acid deficiency). previous total or subtotal gastrectomy. carcinoma of stomach. autoimmune gastritis (diffuse corporal atrophic gastritis) with intestinal metaplasia. crohn's disease;* sprue;* other chronic inflammatory disorders; jejunal diverticula; intestinal malignancies; fish tapeworm infestation; previous intestinal resection or blind intestinal loop; enteric fistulas. hepatosplenomegaly. alcoholic liver disease. * giant epithelial cells. hyperthyroid goiter; thyroiditis. demyelination of cerebral white matter (in advanced cases). demyelination in posterior and lateral columns of spinal cord, most frequently in thoracic and cervical segments. demyelination of peripheral nerves. retinal hemorrhages; demyelination of optic nerves. hypercellular; megaloblastic. myeloproliferative disorder. brain other organs if mycotic aneurysms are expected and microbiologic studies are intended, follow procedures described below under "aneurysm, mycotic aortic." request verhoeff-van gieson, gram, and grocott's methenamine silver stains. for cerebral arteriography, see chapter 4. if arteriography cannot be carried out, rinse fresh blood gently from base of brain until aneurysm can be identified. record site of rupture and estimated amount of extravascular blood. for paraffin embedding of aneurysms, careful positioning is required. expected findings depend on type of aneurysm. mycotic aneurysms are often multiple and deep in brain substance. berry aneurysms are the most frequent types and often are multiple. most frequent sites are the bifurcations and trifurcations of the circle of willis. saccular atherosclerotic aneurysms are more common than dissecting aneurysms, which are very rare. with congenital cerebral artery aneurysm: coarctation of aorta;* manifestations of hypertension;* and polycystic renal disease. with mycotic aneurysm: infective endocarditis;* pulmonary suppurative processes; and pyemia. aneurysm, dissecting aortic (see "dissection, aortic.") aneurysm, membranous septum of heart note: for general dissection techniques, see chapter 3. most aneurysms ofthe membranous septum probably repre-sent spontaneous closure of a membranous ventricular septal defect by the septalleafiet of the tricuspid valve. aneurysm, mycotic aortic note: (i) collect all tissues that appear to be infected. (2) request aerobic, anaerobic, and fungal cultures. (3) request gram and grocott methenamine silver stains. (4) no special precautions are indicated. (5) no serologic studies are available. (6) this is not a reportable disease. chest and abdominal organs aorta other organs submit blood samples for bacterial culture. en masse removal of adjacent organs is recommended. photograph all grossly identifiable lesions. aspirate material from aneurysm or para-aortic abscess and submit for culture. prepare sections and smears of wall of aneurysm and of aorta distant from aneurysm. request verhoeffvan gieson and gram stains. septicemia and infective endocarditis. * streptococcus, staphylococcus, spirochetes, and salmonella can be found in mycotic aneurysm. para-aortic abscess. septic emboli with infarction or abscess formation. aneurysm, syphilitic aortic part ii / diseases and conditions heart and aorta other organs en masse removal of organs is recommended. for coronary arteriography, see chapter 10. request verhoeff-van gieson stain from sections at different levels of aorta, adjacent great vessels, and coronary arteries. see also under "syphilis." aneurysm usually in ascending aorta. may erode adjacent bone (sternum). syphilitic aortitis may cause intimal wrinkling, narrowing of coronary ostia, and shortening of aortic cusps. disruption of medial elastic fibrils. aortic valvulitis and insufficiency;* syphilitic coronary arteritis; syphilitic myocarditis. external examination aorta prepare chest and abdominal roentgenograms. open aorta along line of blood flow, or bisect into anterior and posterior halves. photograph tear(s). measure bloody effusions in body cavities. measure or estimate amount of blood in mediastinum. request verhoeff-van gieson stain. cutaneous impact trauma. mediastinum widened by hemorrhage in case of tarnponaded dissection. a bleed into a body cavity of less-thanexsanguinating volume should point to an alternate mechanism of death such as neurogenic shock or lethal concussion; a posterior neck dissection may be required in such instances. microscopy may show transmural rupture, false aneurysm, or localized dissection. angiitis (see "arteritis, all types or type unspecified.") angina pectoris note: see under "disease, ischemic heart" and chapter 3. angiokeratoma corporis dittusum (see "disease, fabry's.") angiomatosis, encephalotrigeminal (see "disease, sturge-weber-dimitri.") angiopathy, congophilic cerebral synonyms and related terms: beta amyloid angiopathy due to~-amyloid peptide deposition (~a4) (associated with alzheimer's disease; hereditary cerebral hemorrhage with amyloid angiopathy of dutch type; or sporadic beta amyloid angiopathy); hereditary cerebral amyloid angiopathy, due to deposition of other amyloidogenic proteins such as cystatin c (icelandic type) and others (e.g., transthyretin, gelsolin) (1). procedures possible or expected findings request stains for amyloid, particularly congo red, and thioflavine s (examine with polarized and ultraviolet light, respectively). request immunostain for~a4. some tissue should be kept frozen for biochemical studies. multiple recent cerebral cortical infarctions or small cortical hemorrhages, or both, or massive hemispheric hemorrhages, both recent and old. amyloid deposition in leptomeninges and cortical blood vessels. senile plaques are usually present. in some cases, angiopathy is part of alzheimer's disease. * other organs a prepare material for electron microscopy. electron microscopic study permits definite confirmation of diagnosis. organs and tissues may be minimally affected by amyloidosis. anomaly, coronary artery possible associated conditions: with double outlet right ventricle; persistent truncal artery; tetralogy of fallot;* and transposition of the great arteries.* note: coronary artery between aorta and pulmonary artery, often with flap-valve angulated coronary ostium. coronary artery may communicate with cardiac chamber, coronary sinus, or other cardiac veins, or with mediastinal vessel through pericardial vessel. saccular aneurysm of coronary artery with abnor-mal flow, infective endarteritis of arteriovenous fistula, and myocardial infarction may be present. ifone or both coronary arteries originate from pulmonary trunk, myocardial infarction may be present. heart perform coronary angiography. if infective endarteritis is suspected, submit blood sample for microbiologic study. ectopic origin of coronary arteries or single coronary artery. sudden death. for a detailed description of possible additional findings, see above under "note." anomaly, ebstein's (see "malformation, ebstein's") anorexia nervosa note: sudden death from tachyarrhythmias may occur in advanced cases and thus, autopsy findings may not reveal the immediate cause of death. external examination all organs record height and weight, and prepare photographs to show cachectic features. record abnormalities as listed in righthand column. follow procedures described under "starvation." record weight of endocrine organs and submit samples for histologic study. cachexia, often with preserved breast tissue; hirsutism; dry, scaly, and yellow skin (carotenemia). mild edema may be present. parotid glands may be enlarged. manifestations of starvation.* ovaries tend to be atrophic; other endocrine organs should not show abnormalities. synonyms: cutaneous anthrax; gastrointestinal anthrax; pulmonary (inhalational) anthrax. note: (1) collect all tissues that appear to be infected. this is a reportable disease. bioterrorism must be considered in current cases. external examination and skin blood photograph cutaneous papules, vesicles, and pustules. prepare smears and histologic sections. submit samples for bacteriologic study. submit sample for serologic study. disseminated anthrax infection may occur without skin lesions. edema of neck and anterior chest in nasopharyngeal anthrax. anthrax septicemia. see above under "note." part ii i diseases and conditions lungs gastrointestinal tracts and mesentery neck organs record character and volume of effusions. after sampling for bacteriologic study (see above under "note") perfuse one or both lungs with formalin. extensive sampling for histologic study is indicated. extensive sampling for histologic study is indicated. photograph meningeal hemorrhage in situ. pleural effusions;* hemorrhagic mediastinitis; anthrax pneumonia (inhalational anthrax; woolsorter's disease). histologic sections reveal hemorrhagic necrosis, often with minimal inflammation and gram-positive, spore-forming, encapsulated bacilli. gastrointestinal anthrax with mucosal edema and ulcerations. hemorrhagic mesenteric lymphadenitis. tongue, nasopharynx, and tonsils may be involved. hemorrhagic meningitis (hemorrhage tends to predominate). external examination distal colon and rectum photograph perineum. measure depth of anal pit, if any. dissect distal colon, rectum, and perirectal pelvic organs in situ (as much as possible). search for opening of fistulous tracts from lumen. use roentgenologic study or dissection, or both, to determine course of tract. absence of normally located anus; anal dimple. abnormal termination of the bowel into the trigone of the urinary bladder, the urethra distal to the verumontanum, the posterior wall of the vagina, the vulva, or the perineum. aortitis note: see also under "arteritis" and "aneurysm, ascending aortic." heart and aorta other organs and tissues remove heart with whole length of aorta and adjacent major arteries. record width and circumference of aorta at different levels. describe and photograph appearance of intima and of orifices of coronary arteries and other aortic branches. submit multiple samples for histologic study and request verhoeff-van gieson stain. procedures depend on expected findings or grossly identified abnormalities as listed in right-hand column. secondary aortic atherosclerosis or intimal fibroplasia. widening of aorta; syphilitic aneurysm. * giant cell aortitis; rheumatoid aortitis; syphilitic aortitis; takayasu's arteritis.* manifestations of rheumatoid arthritis, * syphilis,* systemic sclerosis,* hodgkin's lymphoma, and many other diseases associated with vasculitis. external examination brain spine and spinal cord other organs prepare roentgenogram of spine. for removal and specimen preparation, see chapter 4. for removal of spinal cord and specimen preparation, see chapter 4. expose nerve roots. record appearance and photograph spinal cord in situ. submit samples of spinal cord and inflamed tissue for histologic study. request gram, gomori's iron, and grocott's methenamine silver stains. procedures depend on expected findings or grossly identified abnormalities as listed in right-hand column. signs of previous spinal surgery or lumbar puncture (myelography). evidence of previous trauma or previous myelography. cerebral arachnoiditis. fibrous arachnoidal adhesions and loculated cysts. tuberculosis;* syphilis;* fungal or parasitic infection. systemic infection (see above). ascending urinary infection or other manifestations of paraplegia. arch, aortic, interrupted synonym: severe coarctation. note: the basic anomaly is a discrete imperforate region in the aortic arch, with a patent ductal artery joining the descending thoracic aorta. type a interruption is between the left subclavian and ductal arteries; type b between the left subclavian and left common carotid arteries; and type c (rare) between the left common carotid and brachiocephalic (innominate) arteries. for general dissection techniques, see part i, chapter 3. possible associated conditions: bicuspid aortic valve (with type a); di george syndrome* with thymic and parathyroid aplasia (with type b); hypoplasia of ascending aorta (with all types); persistent truncal artery (truncus arteriosus); ventricular septal defect. arrhythmia, cardiac note: see also under "death, sudden cardiac." toxicologic studies may be indicated, for instance, if digitalis toxicity (see "poisoning, digitalis") is suspected. if a cardiac pacemaker had been implanted, the instrument should be tested for malfunction. arteriosclerosis (see "atherosclerosis.") arteritis, all types or type unspecified synonyms and related terms: allergic angiitis and granulomatosis (churg-strauss);* allergic vasculitis; anaphylactoid purpura* and its synonyms; angiitis; buerger's disease;* cranial arteritis; giant cell arteritis;* granulomatous arteritis (angiitis); hypersensitivity angiitis; infectious angiitis; necrotizing arteritis; polyarteritis nodosa;* rheumatic arteritis; rheumatoid arteritis, syphilitic arteritis; takayasu's arteritis;* temporal arteritis; thromboangiitis obliterans; and others (see also below under "note"). note: autopsy procedures depend on (1) the expected type of arteritis, such as giant cell arteritis,* polyarteritis nodosa,* or thromboangiitis obliterans (buerger's disease*); and (2) the nature of suspected associated or underlying disease, such as aortic arch syndrome,* beh~et's syndrome,* cogan's syndrome, degos' disease,* dermatomyositis,* erythema nodosum and multiforme,* goodpasture's syndrome,* polymyositis, rheumatic fever, * rheumatoid arthritis,* syphilis,* and other nonspecific infectious diseases, systemic lupus erythematosus,* systemic sclerosis (scleroderma),* or takayasu's disease. for histologic study of blood vessels, verhoeff-van gieson stain or a similar stain is recommended. temporal and ophthalmic arteritis. arteritis of ciliary and retinal vessels. clinically, polymyalgia. anemia. arteritis, takayasu's synonyms: aortic arch syndrome; pulseless disease. external examination heart, aorta, and adjacent great vessels kidney eyes and optic nerve brain for in situ aortography, clamp distal descending thoracic aorta and neck vessels as distal as possible from takeoff at aortic arch. remove heart together with aorta and long sleeves of neck vessels. for coronary arteriography, see chapter 10 (method designed to show coronary ostia). test competence of aortic valve. open aortic arch anteriorly and measure (with calipers) lumen at origin of great neck vessels. photograph aorta and neck vessels and submit samples for histologic study. request verhoeffvan gieson stain. submit tissue for histologic examination. for removal and specimen preparation, see chapter 5. for removal and specimen preparation, see chapter 4. facial muscular atrophy and pigmentation. narrowing at origin of brachiocephalic arteries. dilated ascending aorta. narrowing of coronary arteries at origins. myocardial infarction. aortic insufficiency. * aortic atherosclerosis. thromboses of brachiocephalic arteries. giant cell arteritis. * diffuse mesangial proliferative glomeulonephritis (1) . atrophy of optic nerve, retina, and iris; cataracts; retinal pigmentation. ischemic lesions. artery, patent ductal synonym: patent ductus arteriosus. note: the basic anomaly is persistent postnatal patency of the ductal artery, usually as an isolated finding (in 75% of cases in infants, and in 95% in adults). it is more common in premature than full-term infants and at high altitudes than at sea level. possible complications in unoperated cases include congestive heart failure, * plexogenic pulmonary hypertension,* ductal artery aneurysm or rupture, fatal pulmonary embolism,* or sudden death. in some conditions, such as aortic atresia* or transposition with an intact ventricular septum,* ductal patency may be necessary for survival. possible associated conditions: atrial or ventricular septal defect;* coarctation ofthe aorta;* conotruncal anomalies; necrotizing enterocolitis in premature infants; postrubella syndrome; and valvular or vascular obstructions. artery, persistent truncal synonym and related terms: type i, pulmonary arteries arise from single pulmonary trunk (in 55%); type 2, pulmonary arteries arise separately but close-by (in 35%); type 3, pulmonary arteries arise separately but distal from one another (in 10%). note: the basic anomaly is a common truncal artery, with truncal valve, giving rise to aorta, pulmonary arteries, and coronary arteries, usually with a ventricular septal defect. interventions include complete rastelli-type repair, with closure of ventricular septal defect, and insertion of valved extracardiac conduit between right ventricle and detached pulmonary arteries. possible associated conditions: absent pulmonary artery (in 15%); atrial septal defect (in 15%); absent ductal artery (in 50%); coronary ostial anomalies (in 40%); di george syndrome;* double aortic arch; extracardiac anomalies (in 25%); interrupted aortic arch* (in 15%); right aortic arch (in 30%); truncal valve insufficiency (uncommon) or stenosis (rare); trun-cal valve with three (in 70%), four (in 20%), or two (in 10%) cusps. heart and great vessels if infective endocarditis is suspected, follow culture procedures for endocardial vegetation described in chapter 10. request verhoeff-van gieson stain. infective endocarditis,* usually of truncal valve. late postoperative conduit obstruction. postoperative late progressive truncal artery dilation with truncal valve insufficiency. hypertensive pulmonary vascular disease. cerebral abscess,* if right-to-ieft-shunt was present. arthritis, all types or type unspecified note: for extra-articular changes, see under the name of the suspected underlying conditions. infectious diseases that may be associated with arthritis include bacillary dysentery, * brucellosis, * gonorrhea, rubella,* syphilis, * tuberculosis, * typhoid fever, * and varicella. * noninfectious diseases in this category include acromegaly,* beh<;et's syndrome,* felty's syndrome,* gout,* rheumatoid arthritis,* and many others, too numerous to mention. remove synovial fluid and prepare smears. submit synovial fluid for microbiologic and chemical study. for removal of joints, prosthetic repair, and specimen preparation, see chapter 2. for removal and specimen preparation, see chapter 5. in the polyarticular variant, facial asymmetry may be noted. rheumatoid factor positive in some cases. pericarditis.* interstitial pneumonitis; pleuritis. (see also under "arthritis, rheumatoid.") lymphadenopathy. splenomegaly. monarthritis or severe, erosive polyarthritis; see also under "arthritis, rheumatoid" and above under "externalexamination and skin." ankylosing spondylitis* may be present. chronic iridocyclitis. see "arthritis, rheumatoid." arthritis, rheumatoid synonyms and related terms: ankylosing spondylitis;* felty's syndrome;* juvenile rheumatoid arthritis* (still's disease); rheumatoid disease; and others. possible associated conditions: amyloidosis;* polymyositis (dermatomyositis*); psoriasis;* sjogren's syndrome;* systemic lupus erythematosus;* systemic vasculitis, and others. subcutaneous rheumatoid nodules on elbows, back, areas overlying ischial and femoral tuberosities, heads of phalangeal and metacarpal bones, and occiput. deformities and subluxation of peripheral joints (see also below under "joints"). subaxial dislocation of cervical spine may be cause of sudden death. pneumothorax;* pleural empyema.* t-cell abnormalities (1) . bacteremia. positive rheumatoid factor. rheumatoid granulomas in myocardium (septum), pericardium, and at base of aortic and mitral valves; constrictive pericarditis;* aortic stenosis;* coronary arteritis. systemic vasculitis (arteritis*). rheumatoid granulomas in pleura and lung (with pneumoconiosis*); bronchopleural fistula; rheumatoid pneumonia with interstitial pulmonary fibrosis and honeycombing; bronchiectasis;* bronchiolitis with cystic changes; pulmonary arteritis. pneumoconiosis* in caplan arthrogryposis (2) may be a primary muscle disease, or it may involve abnormalities of the brain, spinal cord, and/or peripheral nerves. etiologies are numerous, as are the modes of inheritance. critical to making the appropriate diagnosis is the collection of muscles from various sites for routine histology, muscle histochemistry, and electron microscopy. portions of peripheral motor nerves must also be prepared for histology and electron microscopy. abdominal cavity intra-abdominal lymphatic system puncture abdominal cavity and submit fluid for microbiologic study. record volume of exudate or transudate and submit sample for determination of fat and cholesterol content. prior to routine dissection, lymphangiography (see below) may be indicated. possible associated conditions: with pulmonary aspergillosis-bronchiectasis; * bronchocentric granulomatosis;* sarcoidosis;* tuberculosis. * with systemic aspergillosisleukemia;* lymphoma;* and other conditions complicated by immunosuppression (l, 2) . other organs a carefully make multiple parasagittal sections through the unperfused lungs. culture areas of consolidation. if diagnosis was confirmed, perfuse lungs with formalin. prepare histologic sections from walls of cavities, cavity contents, and pneumonic infiltrates. procedures depend on expected findings or grossly identified abnormalities as listed in right-hand column. assault note: all procedures described under "homicide" must be followed. asthma note: spray death* may occur in asthma sufferers from pressurized aerosol bronchodilators. record thickness and position. perfuse one lung with formalin. because mucous plugs may block bronchial tree, attach perfusion apparatus to pulmonary artery or to bronchus and pulmonary artery. monitor perfusion to ensure proper inflation. prepare photograph of fixed cut section. submit samples of pulmonary parenchyma and bronchi for histologic study. request azure-eosin and verhoeff-van gieson stains. record weight and thickness of walls. leave attached to stomach. photograph and submit samples for histologic study. eczema. conjunctival hemorrhages and subcutaneous emphysema may be present after fatal attack. pneumothorax;* mediastinal emphysema. low diaphragm (see below). increased igeconcentrations in fatal asthma; postmortem tryptase determination is of doubtful value in this regard (1) . hypertrophy. low position of diaphragm. hyperinflated lungs. thick-walled bronchi with prominent viscid mucous plugs. typical microscopic inflammatory changes (2) . asthmatic bronchitis with eosinophilic infiltrates. bronchocentric granulomatosis.* pulmonary atherosclerosis with breakup of elastic fibers. paucity of ecosinophils in mucous (6) . cor pulmonale. refl ux esophagitis (3) . peptic ulcer. * pneumatosis of small intestine; emphysema of colon. centrilobular congestion and necrosis. petechial hemorrhages in hypothalamus; necrosis of cerebellar folia; anoxic changes in cortex, globus pallidus, thalamus, sommer's sector of hippocampus, and purkinje cells of cerebellum. suspected changes in anterior hom cells of spinal cord in patients with asthma-associated poliomyelitis-like illness (hopkins syndrome) (4). allergic polyps and other allergic inflammatory changes (5) . increased erythropoiesis. atresia, aortic valvular synonym: aortic atresia; aortic atresia with intact ventricular septum; hypoplastic left heart syndrome. note: the basic anomaly is an imperforate aortic valve, with secondary hypoplasia ofleft-sided chambers and ascending aorta. for possible surgical interventions, see two-stage norwood and modified fontan procedures in chapter 3. possible associated conditions: atrial septal defect* (or patent foramen ovale, usually restrictive); dilatation of myocardial sinusoids thatcommunicate with coronary vessels; dilatation of right atrium, right ventricle, and pulmonary trunk; fibroelastosis ofleft atrial and left ventricular endocardium; hypertrophy of ventricular and atrial walls; hypoplastic left atrium, mitral valve, left ventricle, and ascending aorta; mitral atresia* with minute left ventricle; patent ductal artery (ductus arteriosus); small left ventricle with hypertrophic wall; tubular hypoplasia of aortic arch, with or without discrete coarctation. synonyms and related terms: congenital biliary atresia; extrahepatic biliary atresia; infantile obstructive cholangio-pathy; syndromic (alagille's syndrome) or nonsyndromic paucity of intrahepatic bile ducts ("intrahepatic" biliary atresia). possible associated conditions: alpha]-antitrypsin deficiency;* choledochal cyst;* congenital rubella syndrome;* polysplenia syndrome* (1); small bowel atresia; trisomy 17-18; trisomy 21; turner's syndrome;* viral infections (cytomegalovirus infection;* rubella*). dissect extrahepatic bile ducts in situ or leave hepatoduodenalligament intact for later fixation and sectioning (see below). record appearance and contents of gallbladder and course of cystic duct. in postoperative cases, submit sample of anastomosed hepatic hilar tissue for demonstration of microscopic bile ducts. remove liver with hepatoduodenalligament. prepare horizontal sections through ligament and submit for histologic identification of ducts or duct remnants. prepare frontal slices of liver and sample for histologic study. request pas stain with diastase digestion. procedures depend on expected findings or grossly identified abnormalities as listed in right-hand column. jaundice. congenital rubella and other viral infections. alpha]-antitrypsin deficiency;* defects in bile acid synthesis. chromosomal abnormalities. in atresia of the hepatic duct, the gallbladder will be empty. in isolated atresia of the common bile duct, the gallbladder contains bile but it cannot be squeezed into the duodenum. atresia or hypoplasia of bile duct(s); choledochal cyst(s). biliary drainage created by kasai operation. obliterative cholangiopathy (2) . intrahepatic cholelithiasis; postoperative ascending cholangitis; secondary biliary cirrhosis; giant cell transformation; paucity of intrahepatic bile ducts. pas-positive inclusions in alphal-antitrypsin deficiency.* polysplenia syndrome* (1) with malrotation, situs inversus, preduodenal portal vein, absent inferior vena cava, anomalous hepatic artery supply, and cardiac defects. for other abnormalities outside the biliary tree, see under "possible associated conditions"). nephromegaly (3) . atresia, cardiac valves (see "atresia, aortic valvular," "atresia, mitral valvular," "atresia pulmonary valvular, with intact ventricular septum," "atresia, pulmonary valvular, with ventricular septal defect," and "atresia, tricuspid valvular.") atresia, duodenal possible associated conditions: with membranous obstruction of the duodenum-annular pancreas; atresia of esophagus* with tracheoesophageal fistula; congenital heart disease; cystic fibrosis;* down's syndrome;* hirschsprung's disease; imperforate anus* or other congenital obstructions of the intestinal tract (1); intestinal malrotation; lumbosacral, rib-, and digitllimb anomalies; single umbilical artery; spinal defects; undescended testis (1). see also under "atresia, small intestinal." the basic anomaly is an imperforate pulmonary valve, with a hypoplastic right ventricle. in unoperated cases, ductal closure is the most common cause of death. for possible surgical interventions, see modified blalock-taussig shunt, mod-ified fontan procedure, and pulmonary valvulotomy in chapter 3. for general dissection techniques, see chapter 3. possible associated conditions: dilated myocardial sinusoids that may communicate with epicardial coronary arteries or veins; patent ductal artery (ductus arteriosus); patent oval foramen (foramen orale); tricuspid atresia with minute right ven-tricle; tricuspid stenosis with hypoplastic right ventricle (in 95%); tricuspid insufficiency with dilated right ventricle (in 5%). synonym: tetralogy of fallot with pulmonary atresia. note: the basic anomaly is atresia of the pulmonary valve and ofvariable length ofpulmonary artery, and ventricular septal defect (membranous or outlet type), with overriding aorta, and with pulmonary blood supply from ductal or systemic collateral arteries. for possible surgical interventions, see rastelli-type repair and unifocalization of multiple collateral arteries in chapter 3. possible associated conditions: right ventricular outflow tract a short blind-ended pouch (70%) or absent (30%); atresia of pulmonary artery bifurcation, with nonconfluent pulmonary arteries; right aortic arch (40%); atrial septal defect (50%); persistent left superior vena cava; anomalous pulmonary venous connection; tricuspid stenosis or atresia; complete atrioventricular septal defect; transposed great arteries; double inlet left ventricle; asplenia, polysplenia, or velocardiofacial syndromes; dilated ascending aorta, with aortic insufficiency. related term: jejuno-ileal atresia. possible associated findings: esophageal atresia* with tracheoesophageal fistula; lumbosacral, rib-, or digit/limb anom -alies; undescended testes (l) . note: see also under "atresia, duodena1." fascia lata, blood, or liver these specimens should be collected using aseptic technique for tissue culture for chromosome analysis (see chapter 9) . intestinal tract for mesenteric angiography, see chapter 2. leave mesentery attached to small bowel, particularly to the atretic portion. trisomy 21. multiple atresias; proximal dilatation; volvulus; malrotation; meconium impaction; other evidence of cystic fibrosis. anorectal malformation (l) . annular pancreas (1). atresia, tricuspid valvular note: the basic anomaly is an absent right atrioventricular connection (85%) or imperforate tricuspid valve (15%), with a hypoplastic right ventricle (100%), muscular ventricular septal defect (90%) that is restrictive (85%), and a patent oval atresia, urethral foramen (80%) or secundum atrial septal defect (20%). for possible surgical interventions, see modified fontan or glenn procedures in chapter 3. for general dissection techniques, see chapter 3. possible associated conditions: juxtaposed atrial appendages; large left ventricular valvular orifice; large left ventricular chamber; persistent left superior vena cava; pulmonary atresia; transposition of the great arteries (25%), with aortic co-arctation (35% of those); anomalies of musculoskeletal or digestive systems (20%); down's,* asplenia, or other syndromes. heart aorta and cervical arteries brain if infective endocarditis* is suspected, culture using the method described in chapter 7. for dissection of carotid and vertebral arteries, see chapter 4. for removal and specimen preparation, and cerebral anteriography, see chapter 4. if a foreign body is discovered during a medicolegal autopsy or if the discovery of a foreign body may have medicolegal impli-cations (e.g., presence of a surgical instrument in the abdominal cavity), the rules of the chain of custody apply. for the handling of bullets or bullet fragments, see "injury, firearm." if analysis offoreign material is required, commercial laboratories may be helpful. bolus (see "obstruction, acute airway!') burns note: fatal bums should be reported to the medical examiner's or coroner's office. the questions to be answered by the pathologist depend on whether the incident was accidental, sui-cidal, or homicidal, and whether the victim survivied to be treated in the hospital. a pending death certificate should be issued if the fire and police investigators are not sure of the circumstances at the time of the autopsy. for electrical bums, see under "injury, electrical." for victims who were treated at the hospital, autopsy procedures should be directed toward the discovery or confirmation of the mechanism of death, such as sepsis or pulmonary embolism.* death can be caused primarily by heart disease, with other-wise minor bums and smoke inhalation serving as the trigger that leads to lethal ventricular arrhythmia. because carbon monoxide concentrations are halved approx every 30 min with 100% oxygen therapy, the pathologist must obtain the first clinical laboratory test results for co-hemoglobin. soot can be detected with the naked eye 2 or 3 d after inhalation of smoke. ambulance records should be examined to determine whether a persistent coma might have been caused by hypoxic encephalopathy following resuscitation from cardiac arrest at the scene. admission blood samples should be acquired to test for cohemoglobin and alcohol. this may not have been done in the emergency room. persons suffering from chronic alcoholism succumb to fire deaths more often than persons who do not drink. a very high initial serum alcohol concentration suggests a risk factor for the fire and presence of chronic alcoholism. patients with chronic alcoholism typically are deprived of alcohol when they are in the bum unit and this can cause sudden, presumably cardiac, death,just as it occurs under similarcircum-stances, not complicated by bums. under these circumstances, the heart fails to show major abnormalities. this mode of dying seems to have no relationship to the presence or absence of liver disease. if the body is found dead and charred at the scene, prepare whole body roentgenograms, before and after removal of remanants of clothing. see also under "identification of the body" and "external examination" in chapter 13). one or two fingerpads may yield sufficient ridge detail for identification. if this is not possible, ante-and postmortem somatic and dental radiographs must be compared for identification, or dna comparison must be used. external examination, heart and lungs abdominal cavity and liver see below under "cardiomyopathy, dilated." record volume of ascites. record actual and expected weight of liver. request iron stain. see below under "cardiomyopathy, dilated." alcoholic cirrhosis and alcoholic cardiomyopathy rarely coexist. however, in genetic hemochromatosis,* cirrhosis and heart failure are common findings. cardiomyopathy, dilated (idiopathic, familial, and secondary types) note: for general dissection techniques, see chapter 3. external examination heart other organs and tissues record actual and expected weights. record ventricular thicknesses and valvular circumferences. evaluate relative atrial and ventricular chamber sizes. procedures depend on expected findings or grossly identified abnormalities as listed in right-hand column. note: huntington's disease maps to the short arm of chromosome 4. the gene is widely expressed but of unknown function; it contains a cag repeat sequence, which is expanded (range, 37 to 86) in patients with huntington's disease. a sensitive diag-nostic test is based on the determination of this cag sequence, which can be done on fresh-frozen tissue or blood (1) . in the absence of genetic confirmation, sampling of organs and tissues cannot be excessive because a complex differential diagnosis must be resolved. note: disseminated intravascular coagulation (dic) often is a complication of obstetrical mishaps such as abruptio placentae or amniotic fluid embolism,* or it complicates malignancies (such as adenocarcinomas or leukemia*) or bacterial, viral, and other infections. other conditions such as aortic aneurysm* or hemolytic uremic syndrome* are known causes also. ifthe nature of the underlying disease is known, follow the procedures under the appropriate heading also. note: this is a cause of diarrhea. microscopic colitis is associated with older age; collagenous colitis is associated with female sex (1). the colon is grossly normal but microscopically, increased lymphocytes in the lamina propria and a subepithelial band of collagen is found. if only the lymphocytic infiltrate is found, the term "lymphocytic colitis" or "microscopic colitis" should be applied. a trichrome stain should be ordered in all instances, because the collagen band may be difficult to see without the special stain. i death, anaphylactic synonym: generalized anaphylaxis. note: autopsy should be done as soon as possible after death. neck organs should be removed before embalming. if death is believed to be caused by drug anaphylaxis, inquire about type of drug(s), drug dose, and route of administration (intravenous, intramuscular, and oral or other). this will determine proper sampling procedures-for instance, after penicillin anaphylaxis. allergy to bee stings, wasp stings, fire ants, and certain plants may also be responsible for anaphylaxis. however, envenomation also can be fatal in the absence of anaphylaxis. external examination search for injection sites or sting marks. if such lesions are present, photograph and excise with 5-cm margin. freeze excised tissue at -70â°c for possible analysis. prepare chest roentgenogram. foam in front of mouth and nostrils. swelling of involved tissue. antigen-antibody reaction in involved tissues. antibodies against suspected antigen. laryngeal edema may recede soon after death. foamy edema in trachea and bronchi; diffuse or focal pulmonary distention ("acute emphysema") alternating with collapse; pulmonary edema and congestion; accumulation of eosinophilic leukocytes. eosinophilic leukocytes in red pulp. death, anesthesia-associated. note: there are many possible causes of anesthesiaassociated death that are not drug-related, such as acute airway obstruction* by external compression, aspiration, arrhythmia of a heart not previously known to be diseased, tumor, or an inflammatory process. some ofthe complications are characteristically linked to a specific phase of the anesthesia, and many are not revealed by customary morphologic techniques. the task for the pathologist charged with investigating an anesthesia-associated death is to reconstruct the chain of physiologic events culminating in cessation of vital signs. autopsy morphology plays a supporting role; the main investigations center around the record left by the anesthesiologist, testing of anesthesia equipment, and toxicological testing. a consulting anesthesiologist can divine much more information from the anesthesia and recovery room records than can the pathologist, and can suggest avenues of further investigation. therefore, the most important step in these autopsies is to obtain the anesthesiaassociated records and to secure the consulting services of an independent anesthesiologist. the changes in the vital signs during and after anesthesia will help to focus the investigation toward a cardiac mechanism ofdeath or depression ofbrainstem function as a terminal mechanism. when information is gathered about drugs and chemical agents that have been administered or to which the victim may have had access, the pathologist must keep in mind that some non-medical chemicals and many drugs are known to affect anesthesia. drugs and their metabolic products, additives, stabilizers, impurities, and deterioration products (one of which can be carbon monoxide) may be present and can be identified in postmortem tissues. therefore, all appropriate body fluids and solid tissue should be submitted for toxicological examination. if the anesthetic agent was injected into or near the spinal canal, spinal fluid should be withdrawn from above the injected site into a standard toxicologist's collection tube with fluoride preservative. if the anesthetic agent was injected locally, tissue should be excised around the needle puncture marks at a radius of 2-4 em. serial postmortem analysis of specimens may permit extrapolation to tissue concentration at the time of death. the time interval between drug administration and death sometimes can be calculated from the distribution and ratio ofadministered drugs and their metabolic products. for a review of anesthetic death investigation, see ref. (1) . halothane anesthesia and some other anesthetic agents may cause fulminant hepatitis and hepatic failure. the autopsy procedures suggested under "hepatitis, viral" should be followed. note: for special autopsy procedures in postoperative deaths, see chapter 1. in some instances, procedures described under "death, anesthesia-associated" may be indicated. for a review of investigational procedures and autopsy techniques in operating-room-associated deaths, see ref. (1) . if the autopsy will involve anatomy or dissection techniques that are unfamiliar, the pathologist should not hesitate to invite the surgeon to the autopsy. in patients who develop a cerebral infarction after open heart surgery, arterial air embolism should be considered as a possible cause. the diagnosis often must be based on excluding other causes because the air has been absorbed prior to death. if a patient dies rapidly, the hospital records may be incomplete or scanty. for example, if a patient bleeds to death despite attempted repair of hepatic lacerations, hospital records may not suffice to reach the correct cause-of-death opinion; personal accounts from the surgeon and anesthesiologist may be needed. autopsy data on patients dying following thoracic surgery may be found in ref (2) . d death, restaurant (see "obstruction, acute airway.") death, sniffing and spray related terms: glue sniffing; sudden sniffing death syndrome. note: no anatomic abnormalities will be noted at autopsy. sudden death may occur after cardiac dysrhythmia or respiratory arrest. procedures possible or expected findings lungs brain if poison had been inhaled at the time when death occurred, tie main bronchi. submit lungs in glass container for gas analysis. submit samples of small bronchi for histologic study. for removal and specimen preparation, see chapter 4. submit samples of fresh or frozen brain for toxicologic study. submit samples in glass containers (not plastic) for toxicologic study. trichloroethane, fluorinated refrigerants, and other volatile hydrocarbons are most often involved in the "sudden sniffing death syndrome." spray death may occur in asthma sufferers using pressurized aerosol bronchodilators. freons and related propellants may also be responsible for sudden death. toxic components of glue-such as toluene-accumulate in the brain of glue sniffers. also present in various glues are acetone, aliphatic acetates, cyclohexane, hexane, isopropanol, methylethyl ketone, and methylisobutyl ketone. aerosols may occlude the airway by freezing the larynx. carbon tetrachloride sniffing may cause hepatorenal syndrome (see also under "poisoning, carbon tetrachloride"). death, sudden unexpected, of adult note: medicolegal autopsies are usually indicated, and appropriate procedures should be followed. ifanaphylactic death is suspected, see also under that heading. for all unexpected deaths, the pathologist should learn the circumstances of the death, in order to determine whether the mechanism of death was rapid or slow, and to guide the selection of ancillary tests. whenever paramedics attended a person, the run sheet should be obtained to look for a history of recent drinking or ofchronic alcoholism may be an important clue. the combination of a history ofalcoholism, a negative test for ethanol, and absence ofcardiovascular disease, should suggest alcohol withdrawal as the cause ofa sudden death. the list of"possible or expected findings" below is not complete. for general toxicologic sampling, see chapter 13. possible associated conditions: atrial septal defect;*bicuspid aortic valve;* coarctation,* hypoplasia, or interruption (type a) of aortic arch; coronary artery from main pulmonary artery; right atrial arch; patent ductal artery;* right pulmonary artery from ascending aorta; subaortic stenosis;* tetralogy of fallot;* ventricular septal defect. * (in approx 50% of the cases, one or more of these associated conditions are found.) defect, atrial septal note: the basic anomaly is a defect of the atrial septum, usually at the oval fossa (in 85%). possible complications in unoperated cases include atrial arrhythmias, congestive heart failure; paradoxic embolism; plexogenic pulmonary hypertension â«10%), and pulmonary artery aneurysm. possible surgical interventions include surgical and transcatheter closure of defect. for deficiency, vitamin c synonyms: hypovitaminosis c; scurvy. external examination and skin other organs bones, joints, and soft tissues record extent and character of skin lesions; prepare sections of skin. describe appearance of gums, and prepare sections. record evidence of bleeding. for removal, prosthetic repair, and specimen preparation of bones and joints, see chapter 2. hyperkeratotic hair follicles with perifollicular hemorrhages (posterior thighs, anterior forearms, abdomen); petechiae and ecchymoses (inner and posterior thighs); subcutaneous hemorrhages. gingivitis. in rare instances, gastrointestinal or genitourinary hemorrhages. hemorrhages into muscles and joints. subperiosteal hemorrhages occur primarily in distal femora, proximal humeri, tibiae, and costochondral junctions (scorbutic rosary). deficiency, vitamin d synonyms: hypovitaminosis d; rickets. note: features or rickets may be found in familial hypophosphatemia (vitamin d-resistent rickets; fanconi syndrome). vitreous or blood (serum) other organs prepare skeletal roentgenograms. in infants with suspected rickets, record size of anterior fontanelle and shape of head; state of dentition; and shape of costochondral junctions, wrists, long bones, and spine. submit samples for calcium, magnesium, and phosphate determination. procedures depend on expected findings or grossly identified abnormalities as listed in right-hand column. weigh parathyroid glands and submit samples for histologic study. submit samples of intestine for histologic study. for removal, prosthetic repair, and specimen preparation, see chapter 2. in infantile rickets, diagnostic sites for histologic sampling are costochondral junctions, distal ends of radius and ulna, and proximal ends of tibia and humerus. for adults, see under "osteomalacia." in infants, rachitic changes at costochondral junctions; in adults, osteoporosis* and osteomalacia*-with or without pseudofractures (milkman's syndrome (1) . note: the term spinocerebellar degeneration encompasses a variety of lesions whose classification is controversial. a new approach has come from linkage analysis and molecular biology. for instance, friedreich's ataxia, the classic form of hereditary ataxia, is due to an intronic expansion of a gaa tri-nucleotide repeat. other forms are also identified by their specific gene loci. neuropathologic examination still is important and ample sampling is suggested, which should include cerebral cortex, basal ganglia (caudate nucleus, putamen, and globus pallidus), thalamus, subthalamic nucleus, midbrain (red nucleus and substantia nigra), pons (pontine nuclei), spinal cord (at cer-vical, thoracic, and lumbar levels), optic tract, optic nerves with lateral geniculate nucleus, and sensory and motor peripheral nerves. for removal and specimen preparation, see chapter 5. enlargement of head. poor demarcation between cortex and gelatinous white matter. extensive demyelination and vacuolation of white matter, particularly subcortically. optic atrophy. degeneration, striatonigral (see "atrophy, multiple system.") related term: thirst. note: possible underlying conditions not related to inaccessibility of water include bums, exposure to heat, gastrointestinal diseases, recent paracentesis, renal diseases, and use of diuretic drugs. see also under "disorder, electrolyte(s)." external examination vitreous urine prepare histologic sections of blisters, ulcers, or skin abrasions. submit sample for sodium, chloride, and urea nitrogen determination. skin turgor may be decreased and eyes may be sunken. microscopic changes help to decide whether skin lesions are antemortem or postmortem. sodium concentrations more than 155 meqll, chloride concentrations more than 130 meq/ and urea nitrogen concentrations between 40 and 100 meq/dl indicate dehydration. absence or minimal amount of urine. dementia (see "disease, alzheimer's.") drug abuse, amphetamine(s) note: methamphetamine abuse may be suggested by poor condition of the dentition. methylenedioxymethamphetamine ("ecstasy") abuse is often suggested by friends with whom the decedent was abusing drugs. follow procedures described under "dependence, drug(s)." drug abuse, cocaine note: cocaine is spontaneously hydrolyzed by blood esterases, even after death. however, one of its major metabolite, benzoylecgonine, is routinely identifiable by immunoassay screening tests. when cocaine is abused concurrently with heroin or other depressant drugs, it may be difficult to ascribe deth to a single agent, unless circumstances clearly point to a rapid cardiac mechanism or a slow brainstem depression mechanism. note: if narcotic paraphernalia and samples of the drug itself are found at the scene of the death, they should be submitted for analysis. helpful information about the nature of a drug may be obtained from witnesses. state crime laboratories may provide much assistance. if name of drug is known, see also under "poisoning,..." the slang name of a drug may be insufficient for identification because these names often are used for different compounds at different times of places. opoid narcotics can be injected intravenously, or subcutaneously, or snorted. death may occur with such speed that the bodies may be found with needles and syringes in the veins or clenched in the hands. drug abuse may be associated with a multitude of local (see below) or systemic complications, including malaria* and tetanus. * as stated in chapter 13, for a growing number of analytes, most notably tricyclic antidepressants, peripheral blood is preferred over central blood. peripheral blood is aspirated by percutaneous puncture before autopsy, from the femoral vein or the subclavian vein. the authors prefer the femoral approach in order to avoid any question of artifact in the diagnosis of venous air embolism. it may be pru-dent to add naf to some of the samples. related term: childhood dermatomyositis (or polymyositis) associated with vasculitis; dermatomyositis (or polymyositis) associated with neoplasia or collagen vascular disease; primary idiopathic dermatomyositis; primary idiopathic polymyositis. possible associated conditions: carcinoma (lung, stomach, intestine, and prostate in males; breast, ovary, and uterus in females; miscellaneous sites in both sexes); lymphoma* (rare) and other malignancies (1); lupus erythematosus;* mixed connective tissue disease; progressive systemic sclerosis;* rheumatoid arthritis;* sjogren's syndrome;* and others. vasculitis of childhood polymyositis (dermatomyositis). external examination and skin heart lungs esophagus and gastrointestinal tract photograph grossly involved skin. prepare sections of involved (anterior chest, knuckles, knees) and grossly uninvolved skin and subcutaneous tissue. prepare roentgenograms. submit samples from myocardium for histologic study. perfuse one lung with formalin. submit samples from all segments for histologic study. arteritis* and phlebitis* with thrombosis, fibrosis, and infarctions. steatohepatitis and manifestations of diabetes mellitus* may be found (2) . myositis with muscular atrophy and fibrosis; vasculitis in childhood cases. polyneuropathy (rare) (5). arthritis. diabetes mellitus synonyms: type i (insulin-dependent or juvenile-onset) diabetes mellitus; type ii (insulin-independent or adult onset) diabetes mellitus; secondary diabetes mellitus (e.g., due to drugs or pancreatic disease). note: in infants of diabetic mothers, macrosomia and congenital malformations must be expected. record size and weight of placenta and total weight and length, crown to rump length, and crown to heel length of infant. compare with expected measurements (see part iii). expected histologic finding in-clude hyperpla-sia with relative increase ofb cells of the islands of langerhans with interstitial and peri-insular eosinophilic infiltrates, decid-ual changes of the endometrium, enhanced follicle growth in the ovaries, and leydig cell hyperplasia. possible associated conditions: acanthosis nigricans; acro-megaly;* amyotrophic lateral sclerosis; * ataxia telangiectasia;* fanconi's anemia;* friedreich's ataxia;* gout;* hemochro-matosis; *hyperlipoproteinemia; * hyperthroidism;* obesity;* turner's syndrome;* and many others, too numerous to mention. note: the term "caroli's syndrome" often is used for cases that also show histologic features of congenital he-patic fibrosis or other manifestations of fibropolycystic liver disease,* whereas the name "caroli's disease" refers to idiopathic dilatation of intrahepatic bile ducts, without associated abnormalities. possible associated conditions: choledochal cyst* and related extrahepatic biliary abnormalities (1); congenital hepatic fibrosis; * cysts of kidneys (renal tubular ectasia or medullary sponge kidney; autosomal-recessive polycystic kidney disease, and rarely, autosomal-dominant polycystic kidney disease [2] )* and of pancreas. record volume of effusions. prepare smears of fresh blood or of buffy coat, or make thick-drop preparation. submit sample for xenodiagnosis or animal inoculation and for serologic study. record weight. in chronic chagas' disease, perfuse intact heart with formalin (chapter 3) and slice fixed heart in a frontal plane so as to create anterior and posterior halves. prepare photographs. histologic samples should include conduction system. include several sections of atrial (auricular) walls for histologic study of autonomous ganglia. perfuse at least one lung with formalin. leave affected hollow viscera intact and fill with formalin. cut fixed organs in half, photograph, and cut histologic sections on edge. record liver weight and submit samples for histologic study. record weight. prepare photographs of abnormalities. weigh and examine. prepare histologic sections. for removal and specimen preparation, see chapter 4. autopsy is desirable in suspected cases because the diagnosis can only be firmly established after neuropathologic examination. serologic studies are not available. unfortunately, all tissues (not just the brain and spinal cord) may remain infectious even after prolonged fixation and histologic processing. thus, the autopsy recommendations for most other infectious diseases do not apply here. this is a reportable disease in some states. special precautions are indicated and therefore, the procedures described here should be followed strictly (1) (2) (3) (4) : all persons in the autopsy room must wear disposable long-sleeved gowns, gloves, and masks. contamination of the autopsy table should be prevented by covering it with a disposable, non-permeable plastic sheet. autopsy generally should be restricted to the brain. if organs in the chest or abdomen need to be examined, this is best done in situ. to prevent aerosolization of potentially infectious bone dust, a hood or other protective device should be used while opening the skull with a stryker saw. after completing the autopsy, instruments and other potentially contaminated objects should be autoclaved in a steam autoclave (1 h at 134â°c). porous load is considered more effective than gravity displacement autoclaves. immerse autopsy instruments in distilled water before and during autoclaving, in order to protect them from corrosion. ifno autoclave is available, chemical disinfection (see below) is a satisfactory alternative. disposable items should be put in a container for infectious hospital waste and ultimately incinerated. contaminated objects not suitable for autoclaving (such as the stryker saw) should be soaked with a2nnaoh solution for 1 h (alternatively, 1 nnaoh may be used for 2 h). contaminated surfaces should be thoroughly washed with the same solution. aluminum should be treated for 2 h with a fresh 5% naoci (sodium hypochlorite) solution with at least 20,000 ppm free chloride. wash waters should be collected; if no autoclave is available, 2 n naoh or >4 volumes of 5% sodium hypochlorite bleach should be added to the water and left for a minimum of 2 h before being discarded. before removing the body from the autopsy room, it should be sponged with 5% sodium hypochlorite. to deactivate cjd infectivity, tissue blocks, 5 mm or less in thickness, should be fixed in formalin in a formalin-totissue ratio of at least 20: 1 for at least 48 h and then soaked in concentrated formic acid (95-100%) for i h, followed by another 48 h of formalin fixation. the fixation fluid should be collected and decontaminated, as described earlier for wash water. glassware and tissue carriers should also be decontaminated as previously described. after this deactivation, the tissue blocks can be processed in a routine fashion. at any stage of these procedures, special care must be taken to avoid cuts with potentially contaminated glassware, blades, or other objects. parenteral exposure to potentially contaminated material also should be avoided. remains of patients who have died of the disease should not be accepted for anatomy teaching for students. if specimens are prepared for pathology collections, they should be handled with great caution. morticians and mortuary workers should be warned of possible hazards posed by tissues of patients with transmissible spongiforme encephalopathies; they should be advised about proper use of disinfectants. clinical laboratories that receive autopsy tissues or fluids must be warned about the infectious nature of the material. if possible, decontamination should be done at the site where the autopsy was done. for the shipping of potentially infected material, see chapter 15. increased concentrations of nse (5). spongiforme changes, astrocytosis, neuronal loss, amyloid plaque formation, prp deposition, and proliferation of activated microglia (6). cerebrospinal fluid brain submit sample for neuron-specific enolase (nse). for removal and specimen preparation, see chapter 4 and above under "note." submit fresh-frozen material for confirmation of diagnosis by histoblot technique on protease k-digested frozen tissue or western blot preparations on brain homogenates. immunohistochemical localization ofprp and hla-dr protein on paraffin-embedded tissue is possible. disease, demyelinating (see "degeneration, spongy, of white matter," "encephalomyelitis, all types or type unspecified," "leukodystrophy, globoid cell," "leukodystrophy, sudanophilic," "sclerosis, multiple;' and "sclerosis, schilder's cerebral.") disease, diffuse alveolar synonym: diffuse pulmonary disease. note: autopsy procedures are listed under the more specific diagnoses, such as "hemosiderosis, idiopathic pulmonary," "lipoproteinosis, pulmonary alveolar," "microlithiasis, pulmonary alveolar," "pneumonia, lipoid," and "syndrome, goodpasture's." glycosphingolipid storage in cornea; lens opacities; dilated vessels in conjunctiva and lens; thrombi in blood vessels (5). disease, fibropolycystic, of the liver and biliary tract note: "fibropolycystic disease of the liver and biliary tract" comprises a group of well defined conditions, which may occur together and hence need a collective designation. the conditions include autosomal-recessive (infantile) and auto-somal dominant (adult) polycystic disease of the liver; caroli's disease or syndrome;* choledochal cyst,* congenital hepatic fibro-sis,* multiple biliary microhamartomas, and related disorders. for autopsy procedures, see also under more specific designations. disease, glycogen storage synonyms: andersen's disease or brancher deficiency (glycogenosis, type iv); cori's or forbes' disease (glycogenosis, type ill); cyclic amp dependent kinase (type x); glycogen synthetase deficiency (type 0); hers' disease (glycogenosis, type vi); mcardle's disease (glycogenosis type v); phosphorylase b kinase deficiency (types ixa, b, and c); pompe's disease (glycogenosis, type it); tarui disease (glycogenosis type vii); von gierke's disease (glycogenosis, type ia); x-linked glycogenosis (type vill). note: if the diagnosis had not been confirmed prior to death, samples of liver, skeletal muscle, blood, and fascia (for fibroblast culture, see below) should be snap-frozen for enzyme assay, which will determine the specific deficiency. types ia and b, iii, vi, and hepatic phosphorylase b kinase deficiency (types ixa, b and c) are hepatic-hypoglycemic disorders, whereas types v and vii affect muscle energy processes. type ii also affects the musculature, whereas type iv may cause cirrhosis and death in infancy from extreme hypotonia. determination of type of glycogenosis usually can be based on (i) pattern of glycogen storage in liver, (2) presence or absence of nuclear hyperglycogenation in liver, (3) cytoplasmic lipid in liver, (4) presence or absence of liver cirrhosis, and (5) presence or absence of glycogen and basophilic deposits in skeletal muscles. possible associated conditions: fanconi syndrome* or gout* with type ia glycogenosis; neutropenia, recurrent infections, and crohn's disease with types ib or ie. glycogen primarily in retinal ganglion cells and ciliary muscle. glycogen in sympathetic nerve ganglia and neurons of cranial nerves in type vii. gouty arthritis. disease, graft-versus-host note: this disease occurs most commonly after bone marrow transplantation. the disease has also occurred after transfusion of viable lymphocytes, for example, to patients with cancer or leukemia. * in patients with graft-versus-host disease (gvhd), autopsy also may reveal recurrence of the underlying disease such as leukemia. possible associated conditions: alphal-antitrypsin deficiency;* amyloidosis;* ankylosing spondylitis;* primary sclerosing cholangitis;* sjogren's syndrome. * see also below under "possible or expected findings." note: in many instances, either chronic ulcerative colitis or crohn's disease* had been diagnosed clinically, but sometimes, the distinction is difficult to make, even at autopsy. many features described below occur in chronic ulcerative colitis but some manifestations of crohn's disease or conditions that may occur in all types of inflammatory bowel disease also are listed so that both positive and negative findings can be recorded properly. osteoporosis;* ankylosing spondylitis;* arthritis of peripheral joints; periarthritis; hypertrophic osteoarthropathy;* tendinitis (particularly of ankle and achilles tendons). disease, iron storage (see "hemochromatosis.") related terms: atherosclerotic heart disease. note: the most common anatomic finding at autopsy in subjects older than 30 yr is coronary atherosclerosis. unusual under-lying or associated conditions include chronic aortic stenosis or regurgitation; coronary artery anomalies; coronary artery dissection; coronary embolism; coronary ostial stenosis (due to calcification of aortic sinotubular junction or, rarely, to syphilitic aortitis); coronary vasculitis (for instance, in polyarteritis nodosa* or acute hypersensitivity arteritis); hyperthyroidism,* gastrointestinal hemorrhage; * hypothyroidism, * idiopathic arterial calcification of infancy; intramural coronary amyloidosis; pheochromocytoma, polycythemia vera; * pseudoxanthoma elasticum,* radiationinduced coronary stenosis; severe pulmonary hypertension (with right ventricular ischemia); sickle cell disease;* and others. if bypass surgery had been performed, see "surgery, coronary bypass." macular rash (4). multifocal fibrinopurulent pneumonia with sparing of the bronchi and bronchioles. exudate is rich in phagocytes, fibrin, and karyorrhectic debris. synonym: lyme arthritis note: this infection is caused by the spirochete, borrelia burgdoiferi, which is transmitted from rodents to human by the hard deer ticks, ixodes dammini, 1. ricinus, and others. brain and spinal cord for removal and specimen preparation, see chapter 4. request luxol fast blue stain for myelin. symmetric and zonal demyelination in corpus callosum, anterior commissure, optic chiasm, optic tracts, and white matter of frontal lobes. external examination and skin; oral cavity lungs aorta record distribution of skin lesions and submit tissue samples for histologic study. for preparation of angiograms of the pulmonary arterial and venous vasculature, see chapter 2. if aneurysm or dissection is present, follow procedures described under those headings. telangiectatic (often papular) lesions most commonly found in cheeks, scalp, nasal orifices, oral cavity, ears, neck, shoulders, fingers, toes, and nail beds. cyanosis and clubbing may be prominent. arteriovenous malformations/fistulas. aneurysm; * aortic dissection. * if cirrhosis is present, prepare angiograms of hepatic arteries and veins (chapter 2). photograph and prepare sections of angiomatous lesions. note: parkinson's syndrome is caused by conditions that may simulate parkinson's disease; these include carbon monoxide* and manganese poisoning, corticobasal degeneration, druginduced parkinsonism, huntington's disease, multiple system atrophy,* progressive supranuclear palsy* (steele-richardson-olszewski syndrome), space-occupying lesions (rare), trauma (dementia pugilistica), and causes related to tumors and vascular diseases. brain for removal and specimen preparation, see chapter 4. histologic sections should include midbrain (substantia nigra), upper pons (locus ceruleus), medulla, nucleus basalis (substantia innominata), and basal ganglia. if parkinsonian syndrome was diagnosed, follow procedures described under the name of the suspected underlying condition (see above under "note"). depigmentation of substantia nigra and locus coeruleus; neuronal loss and reactive gliosis; eosinophilic intracytoplasmic inclusion bodies (lewy bodies) in some of the surviving neurons; no significant changes in basal ganglia. disease, pelizaeus-merzbacher synonyms: sudanophilic (orthochromatic) leukodystrophy. brain and spinal cord for removal and specimen preparation, see chapter 4. request luxol fast blueipas stain for myelin and bielschowsky's stain for axons. prepare frozen sections for sudan stain. brain generally atrophic. myelin loss in centrum ovale, cerebellum, and part of brain stem, with a tigroid pattern of residual myelin near vessels. axons are preserved. diffuse gliosis with relatively few lipoid-containing macrophages, compared to the myelin loss. lipoid material stains with sudan. brain and spinal cord for removal and specimen preparation, see chapter 4. request silver stains (bielchowsky or bodian stain). histochemical stains in pick's cells and bodies reveal phosphorylated neurofilaments, ubiquitin, and tubulin. some tissue should be kept frozen for biochemical studies. severe cerebral atrophy, involving primarily frontal and anterior temporal lobes (knifeblade atrophy; walnut brain). microscopically, severe neuronal loss accompanied by astrocytosis. characteristic argyrophilic, intracytoplasmic inclusions (pick's bodies), particularly in hippocampus and swollen, distended "ballooned" neurons (pick's cells). these changes are not always present. external examination, skin, and adipose tissue blood cerebrospinal fluid heart liver and kidneys brain, spinal cord, and peripheral nerves eyes submit sample for determinaion of phytanic acid concentration and for molecular studies. for obtaining a sample, see chapter 7. sample for histologic study. for removal and specimen preparation, see chapter 4. for removal and specimen preparation, see chapter 5. ichthyosis. phytanic acid accumulation in adipose tissues. phytanic acidemia, mutation of phyh or pex 7 (2). increased protein concentrations. cardiomyopathy.* phytanic acid accumulation. axonal neuropathy. retinitis pigmentosa. hypoalphalipoproteinemia. lymphadenopathy with diffuse deposition of cholesterol esters. premature atherosclerotic cardiovascular disease (1). hepatosplenomegaly with foam cells. enlarged tonsils with characteristic orange discoloration. polyneuropathy (2) . in adults, corneal infiltrates. foam cells. request pas stain. in granulomas, bacilli are not always pas positive (2) . section all grossly involved tissues for histologic examination. submit section for electron microscopy. emaciation. hyperpigmentation, particularly of exposed skin and in scars. hyperkeratosis. arthritis involving ankles, knees, shoulders, and wrists. ascites; fibrinous peritonitis. * nodules in peritoneum containing sickle-form particlecontaining cells (spc cells submit sample for determination of sodium, potassium, chloride, glucose, urea nitrogen, and creatinine concentrations. calcium and phosphate concentrations can also be tested. if sample is small, indicate priority for testing. if indicated, submit sample for chemical study. submit tissue samples for histologic study. considerably increased or decreased values for sodium (more than 155 meqll or less than 130 meqll) and chloride (more than 135 meqll or less than 105 meqll) indicate that changes were present before death. for further interpretation, see chapter 8. postmortem electrolyte concentrations are quite unreliable. may be useful for calcium determination. vacuolar nephropathy (vacuolar changes in proximal convoluted tubules) in potassium deficiency (may also occur after infusion of hypertonic solutions). disorder, hemorrhagic (see "coagulation, disseminated intravascular," ''disease, christmas:' ''disease, von willebrand's," "hemophilia," and "purpura,.â�¢â�¢") disorder, inherited, of phagocyte function note: several conditions represent phagocyte function disorders. autopsy procedures for one of these disorders can be found under "disease, chronic granulomatous." consult this entry for other phagocyte function disorders. synonyms and related terms: fabry's disease* (angiokeratoma corporis diffusum); gangliosidosis;* gaucher's disease;* glycogenosis,* type ii; leukodystrophies (krabbe's or globoidcell,* metachromatic leukoencephalopathy*); mucopolysaccharidoses* (hunter, hurler, morquio, and sanfilippo disease); mucolipidosis; niemann pick disease* (type a, b, c, or sphingomyelinase deficiency); neuraminidase deficiency; neuronal ceroid lipofuscinosis (batten's disease or kufs' disease). hypopharyngeal pulsion diverticulum (zenker's diverticulum) at lower margin of inferior constrictor muscle of pharynx. traction diverticulum at midesophagus after an inflammatory process-for instance, tuberculous lymphadenitis. epiphrenic diverticulum may also occur. luxtacardiac or juxtapyloric diverticulum. heterotopic tissue in meckel's diverticulum, with or without peptic ulceration. colonic muscular hypertrophy and stenosis, usually in sigmoid colon. diverticulitis with perforation, fistulas, or peritonitis. * diving (see "accident, diving (skin or scuba).") related terms: dry drowning; fresh-water drowning; near-drowning; salt (sea)-water drowning (see the following table). primary drowning ("immediate drowning") deaths occurring within minutes after immersion, before or without resuscitative measures deaths from hypoxia and acidosis caused by glottal spasm on breath holding. there may be no evidence of water entering stomach or lungs and no appreciable morphologic changes at autopsy. note: the diagnosis is one of exclusion. the pathologist should help the police to determine: i) how did the person (or dead body) get in the water, and 2) why could that person not get out of the water? it is not enough to ask if a person could swim but investigators should find out how well (what strokes did the victim know?) and how far he or she could swim. the inquiry must include the depth of the water and must address hazards such as undertow or underwater debris, and the behavior deaths occurring from within 30 min to several weeks after resuscitation, because of metabolic acidosis, pulmonary edema, or infective or chemical pneumonitis deaths from hypoxia and acidosis caused by obstruction of airway by water related to: hypervolemia hemolysis hyponatremia hypochloremia hyperkalemia of the victim immediately before submerging. deaths of adults in bathtubs and swimming pools are usually from natural, cardiac causes, or they are suicides, unless the victim was drunk. diatom tests (1) have not proven useful in the united states but there is enthusiasm for such tests among european pathologists. the distinction between hyponatremic deaths in fresh water and hypernatremic deaths in salt water derives from experimental studies; in practice, one cannot reliably predict the salinity of the immersion medium from autopsy studies. because many bodies of drowning victims are recovered only after the body floats to the surface, decomposition will often obscure even the nondiagnostic findings such as pleural effusions, which are often associated with drowning. external examination and skin (wounds) organ samples for diatom search serosal surfaces and cavities if identity of drowning victim is not known, record identifying features as described in chapter 13. prepare dental and whole-body roentgenograms. submit tissue samples for histologic study of wounds. inspect inside of hands. collect fingernail scrapings. record appearance and contents of body orifices. record features indicative of drowning. photograph face from front and in profile. take pictures of all injuries, with and without scale and autopsy number. remove vitreous for analysis. if diatom search is intended, clean body thoroughly before dissection to avoid contamination of organs and body fluids with algae and diatoms (see below). submit sample for toxicologic study. sample early during autopsy, before carrying out other dissections. use fresh instruments for removal of specimens to avoid contamination. submit subpleural portion of lung: subcapsular portions of liver, spleen, and kidneys; bone marrow; and brain. store samples in clean glass jars. for technique of diatom detection, see below. record volume of fluid in pleural spaces. photograph petechial hemorrhages. photograph layerwise neck dissection if strangulation* is suspected. open airways posteriorly, and photograph, remove and save mud, algae, and any other material in tracheobronchial tree. record size and weight of lungs. there may be wounds that were inflicted before drowning occurred-for instance, in shipwrecks or vehicular and diving accidents. other wounds may be inflicted after deathfor instance, from ship propellers or marine animals. sometimes, premortem and postmortem wounds can be distinguished histologically. object (hair?) held by hands in cadaveric spasm. cutis anserina and "washerwoman" changes of hands and feet are of no diagnostic help. foreign bodies; semen (see also under "rape"). foam cap over mouth and nose. in the autopsy room, water running from nose and mouth is usually pulmonary edema or water from the stomach. high concentrations of alcohol indicate intoxication (see under "alcoholism and alcohol intoxication"). evidence of alcohol intoxication may be found. diatoms may occur in the liver and in other organs of persons who have died from causes other than drowning. comparison with diatoms in water sample from area of drowning may be helpful. penny-sized or smaller hemorrhages may indicate violent respiratory efforts or merely intense lividity. presence of pleural fluid suggests drowning. for diatom detection (l) , boil 2-5 g oftissue for 10--15 min in 10 rnl of concentrated nitric acid and 0.5 rnl of concentrated sulfuric acid. then, add sodium nitrate in small quantities until the black color of the charred organic matter has been dispelled. it may be necessary to warm the acid-digested material with weak sodium hydroxide, but the material must soon be washed free from alkali to avoid dissolving the diatoms. the diatoms should be washed, concentrated, and stored in distilled water. for examination, allow a drop of the concentrate to evaporate on a slide, and then mount it in a resin of high refractive index. all equipment must be well-cleaned, and distilled water must be used for all solutions. there are several variations and adaptations of this method. drug abuse, amphetamine(s) note: methamphetamine abuse may be suggested by poor condition of the dentition. methylenedioxymethamphetamine ("ecstasy") abuse is often suggested by friends with whom the decedent was abusing drugs. follow procedures described under "dependence, drug(s)." ductus arteriosus, patent (see "artery, patent ductal.") synonyms and related terms. achondroplastic dwarf; asexual dwarf; ateliotic dwarf; micromelic dwarf; normal dwarf; pituitary dwarf; true dwarf; and many other terms, too numerous to mention. external examination bones and joints record height and weight. prepare skeletal roentgenograms. for removal, prosthetic repair, and specimen preparation, see chapter 2. growth retardation. abnormal growth of epiphyseal cartilage with enlargement of metaphysis. long bones and pelvis most commonly affected. cavernous hemangiomas (maffucci's syndrome). see above under "external examination." chondrosarcoma. dyscrasia, plasma cell note: these conditions are characterized by abnormally proliferated b-immunocytes that produce a monoclonal immunoglobulin. multiple myeloma, * plasma cell leukemia, plasma-cytoma, and waldenstrom's macroglobulinemia* as well as heavy-chain diseases and monoclonal gammopathies of unknown type belong to this disease family. amyloidosis* is closely related to these conditions. for autopsy procedures, see under "amyloidosis," "macroglobulinemia," or "multiple myeloma" and under name of condition that may have caused the plasma cell dyscrasia. such conditions include carcinoma (colon, breast, or biliary tract), gaucher's disease,* hyperlipoproteinemia, * infectious or noninfectious chronic inflammatory diseases, and previous cardiac surgery. synonym: shigella dysentery. note: (i) collect all tissues that appear to be infected. blood bowel eyes joints submit sample for culture and for serologic study. submit sample of feces or preferably bloodtinged mucus for culture. if bacteriologic diagnosis has already been confirmed, pin colon on corkboard, photograph, and fix in formalin for histologic study. submit sample of vitreous for study of sodium, potassium, chloride, and urea nitrogen concentrations. for removal and specimen preparation of eyes, see chapter 5. for removal, prosthetic repair, and specimen preparation, see chapter 2. escherichia coli septicemia. colitis with microabscesses; transverse shallow ulcers and hemorrhages, most often in terminal ileum and colon. dehydration* pattern of electrolytes and urea nitrogen. serous arthritis* of knee joints is a late complication. external examination record extent of pigmentation, facial features, and primary and secondary sex characteristics. prepare skeletal roentgenograms. for removal, prosthetic repair, and specimen preparation, see chapter 2. record size of apertures of cranial nerves in base of skull. unilateral skin pigmentation and precocious puberty in females (albright's syndrome), less commonly in males. synonyms and related terms: becker's muscular dystrophy; congenital muscular dystrophy; duchenne's progressive muscular dystrophy; dystrophinopathy; em-ery-dreifuss mucular dystrophy; facioscapulohumeral dystrophy; limb girdle dystrophy; myotonic muscular dystrophy. external examination record pattern of scalp hair. record status of skeletal musculature. obtain sections for histologic examination. dystrophin staining of the sarcolemma is absent in duchenne's muscular dystrophy and patchy in becker's dystrophy. frontal baldness (in myotonic muscular dystrophy). atrophy and wasting of muscles (generalized or local: predominantly distal in myotonic muscular dystrophy). pseudohypertrophy of calf muscles in duchenne's muscular dystrophy. dystrophic changes include variations in fiber size, fiber degeneration and regeneration, peri-and endomysial fibrosis, and fatty replacement of muscle. the liver, especially the right lobe, is the most common site of involvement. secondary infection or calcification may be present. the lung is the second most common site of involvement. fluid and air may be visible on the roentgenogram. cysts may be present in the abdominal cavity, muscles, kidneys, spleen, bones, heart, and brain. eosinophilia. edema, angioneurotic synonym: angioedema. note: possible causes and suggested autopsy procedures are described under "death, anaphylactic." related term: silo-filler's disease. n5%) unless management is poor or unless new, virulent pathogens are introduced by additions to the herd. enzootic pneumonia is also called viral pneumonia because it often begins with an acute respiratory infection with bpiv-3, brsv, or possibly with one or more of several other viruses (adenovirus, bohv-1, reovirus, bovine coronavirus [bcov] , and bovine rhinitis virus). mycoplasmas, notably mycoplasma dispar, mycoplasma bovis, ureaplasma, and possibly chlamydophila, may also be primary agents. following infection with any of these agents, opportunistic bacteria, such as pasteurella multocida, trueperella (arcanobacterium) pyogenes, histophilus somni, mannheimia haemolytica, and escherichia coli, can cause a secondary suppurative bronchopneumonia, the most serious stage of enzootic pneumonia. the pathogenesis of the primary invasion and how it predisposes the host to invasion by the opportunists are poorly understood, but it is likely that there is impairment of pulmonary defense mechanisms. environmental factors, including air quality (poor ventilation), high relative humidity, and animal crowding, have been strongly incriminated. the immune status of the calf also plays an important role in the development and severity of enzootic pneumonia. calves with bovine leukocyte adhesion deficiency (blad), which prevents the migration of neutrophils from the capillaries, are highly susceptible to bronchopneumonia. lesions are variable and depend largely on the agents involved and on the duration of the inflammatory process. in the acute phases, lesions caused by viruses are those of bronchointerstitial pneumonia, which are generally mild and transient, and therefore are seen only sporadically at necropsy. microscopically, the lesions are necrotizing bronchiolitis, necrosis of type i pneumonocytes with hyperplasia of type ii pneumonocytes, and mild interstitial and alveolar edema. in the case of bpiv-3 and brsv infection, intracytoplasmic inclusion bodies and the formation of large multinucleated syncytia, resulting from the fusion of infected bronchiolar and alveolar epithelial cells, can also be observed in the lungs (fig. 9-83) . airway hyperreactivity has been described in calves after brsv infection; however, the significance of this syndrome in relation to enzootic pneumonia of calves is still under investigation. the mycoplasmas also can cause bronchiolitis, bronchiolar and alveolar necrosis, and an interstitial reaction, but in contrast to viral-induced pneumonias, mycoplasmal lesions tend to progress to a chronic stage characterized by striking peribronchiolar lymphoid hyperplasia (cuffing pneumonia). when complicated by secondary bacterial infections (e.g., pasteurella multocida and trueperella pyogenes), viral or mycoplasmal lesions change from a pure bronchointerstitial to a suppurative bronchopneumonia (fig. 9-84) . in late stages of bronchopneumonia, the lungs contain a creamy-mucoid exudate in the airways and later often have pulmonary abscesses and bronchiectasis (see fig. 9-11) . note that the same viruses and mycoplasmas involved in the enzootic pneumonia complex can also predispose cattle to other diseases, such as pneumonic mannheimiosis (mannheimia aspiration pneumonia. aspiration pneumonia is often a devastating sequela to improper gastric tubing of horses, particularly exogenous lipid pneumonia from mineral oil delivered into the trachea in treatment of colic. gross and microscopic lesions are described in detail in the section on aspiration pneumonias of cattle. opportunistic infections. chlamydophila (chlamydia) spp., obligatory intracellular zoonotic pathogens, can cause systemic infection in many mammalian and avian species; in horses, they can also cause keratoconjunctivitis, rhinitis, pneumonia, abortion, polyarthritis, enteritis, hepatitis, and encephalitis. serologic studies suggest that infection without apparent disease is common in horses. horses experimentally infected with chlamydophila psittaci develop mild and transient bronchointerstitial pneumonia. there are unconfirmed reports suggesting a possible association between these organisms and recurrent airway obstruction in horses. detection of chlamydial organisms in affected tissue is not easy and requires special laboratory techniques such as pcr, immunohistochemistry, and fluorescent antibody tests. horses are only sporadically affected with mycobacteriosis (mycobacterium avium complex, mycobacterium tuberculosis, and mycobacterium bovis). the intestinal tract and associated lymph nodes are generally affected, suggesting an oral route of infection with subsequent hematogenous dissemination to the lungs. the tubercles (granulomas) differ from those in ruminants and pigs, being smooth, gray, solid, sarcoma-like nodules without grossly visible caseous necrosis or calcification (efig. 9-14) . microscopically, the tubercles are composed of macrophages, epithelioid cells, and multinucleated giant cells. fibrosis increases with time, accounting in part for the sarcomatous appearance. adenovirus infections occur commonly in arabian foals with combined immunodeficiency (cid), a hereditary lack of b and t lymphocytes. in cases of adenoviral infection, large basophilic or amphophilic inclusions are present in the nuclei of tracheal, bronchial, bronchiolar, alveolar, renal, and intestinal epithelial cells. as it occurs in other species, infection with a unique fungal pathogen known as pneumocystis carinii typically occurs in immunosuppressed or immunoincompetent individuals such as arabian foals with cid (see fig. 9 -20). diagnosis of pneumocystis carinii requires microscopic examination of lungs and special stains. idiopathic interstitial pneumonia. interstitial and bronchointerstitial pneumonias of undetermined cause that can progress to severe pulmonary fibrosis have been reported in foals and young horses. the gross and microscopic lesions are reminiscent of those of bovine pulmonary edema and emphysema or ards. the lungs are notably congested and edematous and microscopically are characterized by necrosis of the bronchiolar epithelium, alveolar edema, hyperplasia of type ii pneumonocytes, and hyaline membranes. the cause of this form of equine interstitial pneumonia is not known, but toxic and particularly viral causes have been proposed. bovine respiratory disease complex (brdc) and acute undifferentiated respiratory disease are general terms often used by clinicians to describe acute and severe bovine respiratory illness of clinically undetermined cause. these terms do not imply any particular type of pneumonia and therefore should not be used in pathology reports. clinically, the brd complex includes bovine enzootic pneumonia (multifactorial etiology); pneumonic mannheimiosis (mannheimia haemolytica); respiratory histophilosis (histophilus somni), previously known as respiratory hemophilosis (haemophilus somnus); mycoplasma bovis; respiratory viral infections, such as infectious bovine 528.e1 chapter 9 respiratory system, mediastinum, and pleurae pneumonic mannheimiosis (shipping fever) is the most important respiratory disease of cattle in north america, particularly in feedlot animals that have been through the stressful marketing and assembly processes. mannheimia haemolytica biotype a, serotype 1 is the etiologic agent most commonly responsible for the severe pulmonary lesions. a few investigators still consider that pasteurella multocida and other serotypes of mannheimia haemolytica are also causes of this disease. even after many years of intense investigation, from the gross lesions to the molecular aspects of the disease, the pathogenesis of pneumonic mannheimiosis remains incompletely understood. experiments have established that mannheimia haemolytica a1 alone is usually incapable of causing disease because it is rapidly cleared by pulmonary defense mechanisms. these findings may explain why mannheimia haemolytica, despite being present in the nasal cavity of healthy animals, only sporadically causes disease. for mannheimia haemolytica to be established as a pulmonary infection, it is first required that stressors impair the defense mechanisms and allow the bacteria to colonize the lung (see section on impairment of defense haemolytica). clinically, enzootic pneumonia is usually mild, but fatal cases are occasionally seen even in farms with optimal health management. pneumonic mannheimiosis (shipping fever). shipping fever (transit fever) is a vague clinical term used to denote acute respiratory diseases that occur in cattle several days or weeks after shipment. the disease is characterized by a severe fibrinous bronchopneumonia, reflecting the fact that death generally occurs early or at an acute stage. because mannheimia haemolytica (formerly pasteurella haemolytica) is most frequently isolated from affected lungs, the names pneumonic mannheimiosis and pneumonic pasteurellosis have been used synonymously. it is known that pneumonic mannheimiosis can occur in animals that have not been shipped and that organisms other than mannheimia haemolytica can cause similar lesions. therefore the term shipping fever should be relinquished in favor of more specific names, such as pneumonic mannheimiosis or respiratory histophilosis. irregular areas of coagulative necrosis are typically bordered by a rim of elongated cells often referred to as oat-shaped cells or oat cells that are degenerating neutrophils mixed with a few alveolar macrophages (see fig. 9 -86). in the early stages of necrosis, there is no evidence of vascular thrombosis, suggesting that necrosis is primarily caused by the cytotoxin of mannheimia haemolytica and is not the result of an ischemic change. the interlobular septa become distended with protein-rich edematous fluid, and the lymphatic vessels contain fibrin thrombi. the trachea and bronchi can have considerable amounts of blood and exudate, which are transported by the mucociliary escalator or coughed up from deep within the lungs, but the walls of the trachea and major bronchi may or may not be involved. because of the necrotizing process, sequelae to pneumonic mannheimiosis can be serious and can include abscesses, encapsulated sequestra (isolated pieces of necrotic lung), chronic pleuritis, fibrous pleural adhesions, and bronchiectasis. clinically, pneumonic mannheimiosis is characterized by a severe toxemia that can kill animals even when considerable parts of the lungs remain functionally and structurally normal. cattle usually become depressed, febrile (104° to 106° f [40° to 41° c]), and anorexic and have a productive cough, encrusted nose, mucopurulent nasal exudate, shallow respiration, or an expiratory grunt. hemorrhagic septicemia. pneumonic mannheimiosis should not be confused with hemorrhagic septicemia (septicemic pasteurellosis) of cattle and water buffalo (bubalus bubalis) caused by inhalation or ingestion of serotypes 6:b and 6:e of pasteurella multocida. this oie-notifiable disease does not occur in north america and currently is reported only from some countries in asia, africa, and recently in germany. in contrast to pneumonic mannheimiosis, in which lesions are always confined to the lower respiratory tract, the bacteria of hemorrhagic septicemia always disseminates hematogenously to other organs. at necropsy, typically, generalized petechiae are present on the serosal surfaces of the intestine, heart, and lungs and in skeletal muscles. superficial and visceral lymph nodes are swollen and hemorrhagic. variable lesions include edematous and hemorrhagic lungs with or without consolidation; hemorrhagic enteritis; blood-tinged fluid in the thorax and abdomen; and subcutaneous edema of the head, neck, and ventral abdomen. bacteria can be cultured from blood, and animals have high fever and die rapidly (100% case fatality). respiratory histophilosis (haemophilosis). respiratory histophilosis is part of the histophilus somni (haemophilus somnus) disease complex, which has at least eight different clinicopathologic forms, each one involving different organs. this complex includes septicemia, encephalitis (known as thrombotic meningoencephalitis [tme]), pneumonia (respiratory histophilosis), pleuritis, myocarditis, arthritis, ophthalmitis, conjunctivitis, otitis, and abortion. the portals of entry for the different forms of histophilosis have not been properly established. the respiratory form of bovine histophilosis is the result of the capacity of the bacterium to induce both suppurative and fibrinous bronchopneumonia (efig. 9-15 ). the latter is in some cases indistinguishable from that of pneumonic mannheimiosis. the pathogenesis of respiratory histophilosis is still poorly understood, and the disease cannot be reproduced consistently by administration of histophilus somni alone. like mannheimia haemolytica, it requires predisposing factors such as stress or a preceding viral infection. histophilus somni is often isolated from the lungs of calves with enzootic pneumonia. the capacity of histophilus somni to cause septicemia and localized infections in the lungs, brain, eyes, ear, heart, mammary gland, male and female genital organs, or placenta is perhaps attributable to specific virulence factors, such as immunoglobulin-binding proteins (igbps) and lipooligosaccharide (los). also, histophilus mechanisms). these stressors include weaning, transport, fatigue, crowding, mixing of cattle from various sources, inclement weather, temporary starvation, and viral infections. horizontal transmission of viruses and mannheimia haemolytica occurs during crowding and transportation of cattle. viruses that most commonly predispose cattle to pneumonic mannheimiosis include bohv-1, bpiv-3, and brsv. once established in the lungs, mannheimia haemolytica causes lesions by means of different virulence factors, which include endotoxin, lipopolysaccharide, adhesins, and outer membrane proteins; however, the most important is probably the production of a leukotoxin (exotoxin), which binds and kills bovine macrophages and neutrophils. the fact that this toxin exclusively affects ruminant leukocytes probably explains why mannheimia haemolytica is a respiratory pathogen in cattle and sheep but not in other species. during mannheimia haemolytica infection, alveolar macrophages, neutrophils, and mast cells release maximum amounts of proinflammatory cytokines, particularly tnf-α, il-1, il-8, adhesion molecules, histamine, and leukotrienes. by locally releasing enzymes and free radicals, leukocytes further contribute to the injury and necrosis of bronchiolar and alveolar cells. the gross lesions of acute and subacute pneumonic mannheimiosis are the prototypic fibrinous bronchopneumonia, with prominent fibrinous pleuritis ( fig. 9-85 and see fig. 9 -72) and pleural effusion. lesions are always cranioventral and usually ventral to a horizontal line through the tracheal bifurcation. the interlobular septa are distended by yellow, gelatinous edema and fibrin. the "marbling" of lobules is the result of intermixing areas of coagulation necrosis, interlobular interstitial edema, and congestion ( fig. 9-86) . microscopically, lung lesions are evident 4 hours after experimental infection in which neutrophils fill the bronchial, bronchiolar, and alveolar spaces. within 24 to 48 hours, the cytotoxic effect of mannheimia haemolytica is manifested by necrosis of individual alveolar cells and fibrin begins to exude into the alveoli from increased permeability of the air-blood barrier. these changes are exacerbated by endothelial swelling, altered platelet function, increased procoagulant activity, and diminished profibrinolytic activity in the lungs. by 72 hours, alveolar macrophages start to appear in the bronchoalveolar space. at this time, large and the pulmonary defense mechanisms. lung lesions are typically those of a chronic bronchopneumonia with numerous well-delineated caseonecrotic nodules (fig. 9-87 and e-fig. 9-16) . microscopically, lesions are quite characteristic and consist of distinct areas of pulmonary necrosis centered on bronchi or bronchioles. the lesion is formed by a core of fine eosinophilic granular debris surrounded by a rim of neutrophils, macrophages, and fibroblasts (see fig. 9-87) . although the origin of the caseonecrotic lesions is under investigation, recent studies incriminate reactive oxygen species (ros) and reactive nitrogen species (rns) as the major contributors for cell injury in the lung. the diagnosis is confirmed by isolation or somni has the ability to undergo structural and antigenic variation, evade phagocytosis by promoting leukocytic apoptosis, inhibit intracellular killing, reduce transferrin concentrations, and induce endothelial apoptosis in the lungs of affected calves. mixed pulmonary infections of histophilus somni, mannheimia haemolytica, pasteurella multocida, trueperella pyogenes, and mycoplasmas are fairly common in calves. mycoplasma bovis pneumonia. mycoplasma bovis is the most common mycoplasma sp. isolated from pneumonic lungs of cattle in europe and north america. pulmonary infection is exacerbated by stress or any other adverse factor (e.g., viral infection) that depresses n control programs for infectious disease. it was eradicated from north america in 1892 and from australia in the 1970s, but it is still enzootic in large areas of africa, asia, and eastern europe. the etiologic agent, mycoplasma mycoides ssp. mycoides small colony type, was the first mycoplasma isolated and is one of the most pathogenic of those that infect domestic animals. natural infection occurs in cattle and asian buffalo. the portal of entry is aerogenous, and infections occur when a susceptible animal inhales infected droplets. the pathogenic mechanisms are still inadequately understood but are suspected to involve toxin and galactan production, unregulated production of tnf-α, ciliary dysfunction, immunosuppression, and immune-mediated vasculitis. vasculitis and thrombosis of pulmonary arteries, arterioles, veins, and lymphatic vessels lead to lobular infarction. the name of the disease is a good indication of the gross lesions. it is a severe, fibrinous bronchopneumonia (pleuropneumonia) similar to that of pneumonic mannheimiosis (see figs. 9-72 and 9-85) but having a more pronounced "marbling" of the lobules because of extensive interlobular edema and lymphatic thrombosis. typically, 60% to 79% of lesions are in the caudal lobes (not cranioventrally), and pulmonary sequestra (necrotic lung encapsulated by connective tissue) are more frequent and larger than pneumonic mannheimiosis. unilateral lesions are common in this disease. microscopically, the appearance again is like that of pneumonic mannheimiosis, except that vasculitis and thrombosis of pulmonary arteries, arterioles, and capillaries are much more obvious and are clearly the major cause of the infarction and thrombosis of lymphatic vessels in interlobular septa. mycoplasma mycoides ssp. mycoides small colony type remains viable in the sequestra for many years, and under stress (e.g., starvation), the fibrous capsule may break down releasing mycoplasma into the airways, thus becoming a source of infection for other animals. clinical signs are those of severe sepsis, including fever, depression, and anorexia followed by severe respiratory signs such as opened-mouth breathing, dyspnea and coughing, and crepitation and pleural friction on thoracic auscultation. vaccination is highly effective in preventing the disease. bovine tuberculosis. tuberculosis is an ancient, communicable, worldwide, chronic disease of human beings and domestic animals. it continues to be a major problem in human beings in underdeveloped countries, and it is on the rise in some industrialized nations, largely because of the immunosuppressive effects of aids, immigration, and movement of infected animals across borders. the world health organization (who) estimates that more than 1 million people die of tuberculosis and 8 million new cases appear each year, mostly in developing countries. mycobacterium tuberculosis is transmitted between human beings, but where unpasteurized milk is consumed, mycobacterium bovis from the milk of cattle with mammary tuberculosis is also an important cause of human tuberculosis. mycobacterium bovis infections have also been reported in a number of domestic and wild mammalian species; in some countries, wildlife reservoirs exist and may act as a source of infection for cattle. bovine tuberculosis is primarily caused by mycobacterium bovis, but infection with mycobacterium tuberculosis, the pathogen of human tuberculosis, and mycobacterium caprae (formerly mycobacterium bovis ssp. caprae/mycobacterium tuberculosis ssp. caprae) can occur sporadically. tuberculosis can be acquired by several routes, but infection of the lungs by inhalation of mycobacterium bovis is the most common in adult cattle, whereas ingestion of infected milk is more predominant in young animals. organisms belonging to the mycobacterium avium complex can also infect cattle, but for infection caused by these organisms, the term atypical mycobacteriosis (not tuberculosis) is currently preferred. immunohistochemical labeling of tissue sections for mycoplasma antigens. mycoplasma bovis is also incriminated in arthritis, otitis, mastitis, abortion, and keratoconjunctivitis. contagious bovine pleuropneumonia. contagious bovine pleuropneumonia is an oie-notifiable disease of historic interest in veterinary medicine because it was the object of early national a b c than 90% of bovine cases, a chronic, moist cough can progress to dyspnea. enlarged tracheobronchial lymph nodes can contribute to the dyspnea by impinging on airways, and the enlargement of caudal mediastinal nodes can compress the caudal thoracic esophagus and cause bloating. interstitial pneumonias. atypical interstitial pneumonia (aip) is a vague clinical term well entrenched in veterinary literature but one that has led to enormous confusion among veterinarians. it was first used to describe acute or chronic forms of bovine pneumonia that did not fit in any of the "classic" forms because of the lack of exudate and lack of productive cough. microscopically, the criteria for diagnosis of aip in cattle were based on the absence of obvious exudate and the presence of edema, interstitial emphysema (see the section on pulmonary emphysema), hyaline membranes, hyperplasia of type ii pneumonocytes, and alveolar fibrosis with interstitial cellular infiltrates. at that time, any pulmonary disease or pulmonary syndrome that had a few of the previously mentioned lesions was traditionally diagnosed as aip, and grouping all these different syndromes together was inconsequential because their etiopathogenesis were then unknown. field and laboratory investigations have demonstrated that most of the bovine syndromes previously grouped under aip have rather different causes and pathogeneses ( fig. 9-88) . furthermore, what was "atypical" in the past has become so common that it is fairly routine nowadays to find "typical cases" of aip. for all these reasons, investigators, largely from britain, proposed that all these syndromes previously clustered into aip should be named according to their specific cause or pathogenesis. the most common bovine syndromes characterized by edema, emphysema, hyaline membranes, and hyperplasia of type ii pneumonocytes include bovine pulmonary edema and emphysema (fog fever), "extrinsic allergic alveolitis" (hypersensitivity pneumonitis), "reinfection syndromes" (hypersensitivity to dictyocaulus sp. or brsv), milk allergy, ingestion of moldy potatoes, paraquat toxicity, toxic silo gases, mycotoxins, and others. acute bovine pulmonary edema and emphysema (fog fever). acute bovine pulmonary edema and emphysema (abpee), known in britain as fog fever (no association with atmospheric conditions), occurs in cattle usually grazing "fog" pastures (i.e., aftermath or foggage, regrowth after a hay or silage has been cut). epidemiologically, abpee usually occurs in adult beef cattle in the fall when there is a change in pasture from a short, dry grass to a lush, green grass. it is generally accepted that l-tryptophan present in the pasture is metabolized in the rumen to 3-methylindole, which in turn is absorbed into the bloodstream and carried to the lungs. mixed function oxidases present in the nonciliated bronchiolar epithelial (club) cells metabolize 3-methylindole into a highly pneumotoxic compound that causes extensive and selective necrosis of bronchiolar cells and type i pneumonocytes (fig. 9-89 and see fig. 9 -88) and increases alveolar permeability, leading to edema, thickening of the alveolar interstitium, and alveolar and interstitial emphysema. 3-methylindole also interferes with the lipid metabolism of type ii pneumonocytes. the gross lesions are those of a diffuse interstitial pneumonia with severe alveolar and interstitial edema and interlobular emphysema (see fig. 9-55, a) . the lungs are expanded, pale, and rubbery in texture, and the lesions are most notable in the caudal lobes. microscopically, the lesions are alveolar and interstitial edema and emphysema, formation of characteristic hyaline membranes within alveoli (see fig. 9-55, b) , and in those animals that survive for several days, hyperplasia of type ii pneumonocytes and alveolar interstitial fibrosis. respiratory infection usually starts when inhaled bacilli reach the alveoli and are phagocytosed by pulmonary alveolar macrophages. if these cells are successful in destroying the bacteria, infection is averted. however, mycobacterium bovis, being a facultative pathogen of the monocytic-macrophage system, may multiply intracellularly, kill the macrophage, and initiate infection. from this first nidus of infection, bacilli spread aerogenously via airways within the lungs and eventually via the lymph vessels to tracheobronchial and mediastinal lymph nodes. the initial focus of infection at the portal of entry (lungs) plus the involvement of regional lymph nodes is termed the primary (ghon) complex of tuberculosis. if the infection is not contained within this primary complex, bacilli disseminate via the lymph vessels to distant organs and other lymph nodes by the migration of infected macrophages. hematogenous dissemination occurs sporadically when a granuloma containing mycobacteria erodes the wall of a blood vessel, causes vasculitis, and allows the granuloma to discharge mycobacteria into the alveolar circulation. if dissemination is sudden and massive, mycobacteria are widely disseminated and numerous small foci of infection develop in many tissues and organs and the process is referred to as miliary tuberculosis (like millet seeds). the host becomes hypersensitive to the mycobacterium, which enhances the cell-mediated immune defenses in early or mild infections but can result in host-tissue destruction in the form of caseous necrosis. the evolution and dissemination of the pulmonary infection are closely regulated by cytokines and tnf-α production by alveolar macrophages. unlike abscesses that tend to grow rather fast, granulomas evolve slowly at the site of infection. the lesion starts with few macrophages and neutrophils ingesting the offending organism, but because mycobacterium organisms are resistant to phagocytosis, infected macrophages eventually die, releasing viable bacteria, lipids, and cell debris. cell debris accumulates in the center of the lesion, whereas viable bacteria and bacterial lipids attract additional macrophages and a few lymphocytes at the periphery of the lesion. some of these newly recruited macrophages are activated by local lymphocytes and become large phagocytic cells with abundant cytoplasm resembling epithelial cells, thus the term epithelioid macrophages. multinucleated giant cells (also macrophages) appear at the edges of the lesion, and finally the entire focus of inflammatory process becomes surrounded by fibroblasts and connective tissue (see fig. 9 -81). it may take weeks or months for a granuloma to be grossly visible. bovine tuberculosis, the prototype for granulomatous pneumonia, is characterized by the presence of a few or many caseated granulomas (see fig. 9 -80). the early gross changes are small foci (tubercles) most frequently seen in the dorsocaudal, subpleural areas. with progression, the lesions enlarge and become confluent with the formation of large areas of caseous necrosis. calcification of the granulomas is a typical finding in bovine tuberculosis. single nodules or clusters occur on the pleura and peritoneum, and this presentation has been termed pearl disease. microscopically, the tubercle is composed of mononuclear cells of various types. in young tubercles, which are noncaseous, epithelioid and langhans' giant cells are at the center, surrounded by lymphocytes, plasma cells, and macrophages. later, caseous necrosis develops at the center, secondary to the effects of cell-mediated hypersensitivity and enclosed by fibrosis at the periphery. acid-fast organisms may be numerous but more often are difficult to find in histologic section or smears. clinically, the signs of tuberculosis relate to the dysfunction of a particular organ system or to general debilitation, reduced milk production, and emaciation. in the pulmonary form, which is more grossly, the postmortem lesions vary from subtle, gray, subpleural foci (granulomatous inflammation) to severe lesions, in which the lungs are firm and heavy and have a "meaty appearance" because of interstitial pneumonia (efig. 9 -17) with type ii pneumonocyte hyperplasia, lymphocytic infiltration, and interstitial fibrosis. characteristically, discrete noncaseous granulomas formed in response to the deposition of antigen-antibody complexes are scattered throughout the lungs. chronic cases of extrinsic allergic alveolitis can eventually progress to diffuse fibrosing alveolitis. clinically, it can be acute or chronic; the latter has a cyclical pattern of exacerbation during winter months. weight loss, coughing, and poor exercise tolerance are clinical features. full recovery can occur if the disease is recognized and treated early. reinfection syndrome. hypersensitivity to reinfection with larvae of dictyocaulus viviparus is another allergic syndrome manifested in the lungs that causes signs and lesions indistinguishable from abpee, with the exception of eosinophils and possibly larvae in the alveolar exudate. the hypersensitivity reaction in the lung causes diffuse alveolar damage and edema, necrosis of type i pneumonocytes, and hyperplasia of type ii pneumonocytes. in the later stages of the disease, there is formation of small granulomas with interstitial infiltrates of mononuclear cells. it has been suggested but not confirmed that emphysema with diffuse proliferative alveolitis and formation of hyaline membranes can also occur sporadically in the late stages of brsv infection in cattle. presumably, this disease shares many similarities with "atypical" infections occasionally seen in children with respiratory syncytial virus (rsv human strain), in which a hypersensitivity to the virus or virus-induced augmentation of the immune response results in hypersensitivity pneumonitis (see fig. 9 -88). brsv infection is also known to enhance hypersensitivity to environmental allergens in cattle. other forms of bovine interstitial pneumonia. inhalation of manure ("pit") gases, such as nitrogen dioxide (no 2 ), hydrogen interstitial cell infiltrates, fibrosis, emphysema acute proliferation phase hyperplasia of type ii pneumonocytes clinically, severe respiratory distress develops within 10 days of the abrupt pasture change, and cattle develop expiratory dyspnea, oral breathing, and evidence of emphysema within the lungs and even subcutaneously along the back. experimentally, reducing ruminal conversion of l-tryptophan to 3-methylindole prevents the development of abpee. a number of other agents cause virtually the same clinical and pathologic syndrome as is seen in abpee. the pathogenesis is assumed to be similar, although presumably other toxic factors are specific for each syndrome. one of these pneumotoxic factors is 4-ipomeanol, which is found in moldy sweet potatoes contaminated with the fungus fusarium solani. mixed function oxidases in the lungs activate 4-ipomeanol into a potent pneumotoxicant capable of producing irreversible oxidative injury to type i pneumonocytes and bronchiolar epithelial cells, presumably through lipoperoxidation of cell membranes. similarly, purple mint (perilla frutescens), stinkwood (zieria arborescens), and rapeseed and kale (brassica species) also cause pulmonary edema, emphysema, and interstitial pneumonia. extrinsic allergic alveolitis. extrinsic allergic alveolitis (hypersensitivity pneumonitis), one of the most common allergic diseases in cattle, is seen mainly in housed adult dairy cows in the winter. this disease shares many similarities with its human counterpart known as farmer's lung, which results from a type iii hypersensitivity reaction to inhaled organic antigens, most commonly microbial spores, mainly of the thermophilic actinomycete, saccharopolyspora rectivirgula (micropolyspora faeni), commonly found in moldy hay. this is followed by an antibody response to inhaled spores and local deposition of antigen-antibody complexes (arthus reaction) in the lungs (see fig. 9 -88). because it affects only a few animals of the herd or the sporadic person working in a farm, it is presumed that intrinsic host factors, such as dysregulation of dendritic cells, t lymphocytes, igg, interleukins, ifn-γ, and surfactant, are involved in the pathogenesis of the disease. chapter 9 respiratory system, mediastinum, and pleurae efigure 9 -17 interstitial pneumonia, adult cow. note meaty appearance of the pulmonary parenchyma and mild edematous distention of the interlobular septa. inset, thick hyaline membranes (arrows) lining hypercellular alveolar walls. hypersensitivity pneumonia was suspected. (courtesy dr. a. lópez, atlantic veterinary college.) gases, inhalation of no 2 (silo gas) also causes bronchiolitis, edema, and interstitial pneumonia and, in survivors, bronchiolitis obliterans ("silo filler's disease"). smoke inhalation resulting from barn or house fires is sporadically seen by veterinarians and pathologists. in addition to skin burns, animals involved in fire accidents suffer extensive thermal injury produced by the heat on the nasal and laryngeal mucosa, and severe chemical irritation caused by inhalation of combustion gases and particles in the lung. animals that survive or are rescued from fires frequently develop nasal, laryngeal, and tracheal edema, and pulmonary hemorrhage and alveolar edema, which are caused by chemical injury to the blood-air barrier or by ards caused by the excessive production of free radicals during the pulmonary inflammatory response (see efig. 9-7) . microscopic examination of the lungs often reveals carbon particles (soot) on mucosal surfaces of the conducting system. verminous pneumonia (dictyocaulus viviparus). pulmonary lesions in parasitic pneumonias vary from interstitial pneumonia caused by migrating larvae to chronic bronchitis from intrabronchial adult parasites, to granulomatous pneumonia, which is caused by dead larvae, aberrant parasites, or eggs of parasites. in many cases, an "eosinophilic syndrome" in the lungs is characterized by infiltrates of eosinophils in the pulmonary interstitium and bronchoalveolar spaces and by blood eosinophilia. atelectasis and emphysema secondary to the obstruction of airways by parasites and mucous secretions are also common findings in parasitic pneumonias. the severity of these lesions relates to the numbers and size of the parasites and the nature of the host reaction, which sometimes includes hypersensitivity reactions (see section on reinfection syndrome). a common general term for all of these diseases is verminous pneumonia, and the adult nematodes are often visible grossly in the airways ( fig. 9-90) . dictyocaulus viviparus is an important pulmonary nematode (lungworm) responsible for a disease in cattle referred to as verminous pneumonia or verminous bronchitis. adult parasites live in the bronchi of cattle, mainly in the caudal lobes, and cause severe bronchial irritation, bronchitis, and pulmonary edema, which in turn are responsible for lobular atelectasis and interstitial emphysema. atelectasis is confined to the lobules of the lungs ventilated by the obstructed bronchi (dorsocaudal). interstitial emphysema (interlobular) is caused by forced expiratory movements against a partially obstructed single bronchus. in addition to the inflammation of bronchial mucosa, bronchoaspiration of larvae and eggs also causes an influx of leukocytes into the bronchoalveolar space (alveolitis). verminous pneumonia is most commonly seen in calves during their first summer grazing pastures that are repeatedly used from year to year, particularly in regions of europe that have a moist cool climate. the parasite can overwinter in pastures, even in climates as cold as canada's, and older animals may be carriers for a considerable length of time. at necropsy, lesions appear as dark or gray, depressed, wedgeshaped areas of atelectasis involving few or many lobules usually along the dorsocaudal aspect of the lungs. on cut surface, edematous foam and mucus mixed with white, slender (up to 80-mm long) nematodes are visible in the bronchi (see fig. 9 -90). in the most severe cases, massive numbers of nematodes fill the bronchial tree. microscopically, the bronchial lumens are filled with parasites admixed with mucus because of goblet cell hyperplasia, and there is squamous metaplasia of the bronchial and bronchiolar epithelium because of chronic irritation. there are also inflammatory infiltrates in the bronchial mucosa; alveolar edema; hyperplasia of balt sulfide (h 2 s), and ammonia (nh 3 ), from silos or sewage can be a serious hazard to animals and human beings. at toxic concentrations, these gases cause necrosis of bronchiolar cells and type i pneumonocytes and fulminating pulmonary edema that causes asphyxiation and rapid death (see fig. 9-60) . like other oxidant secretory granules released by club cells contain several proteins, such as surfactantlike protein, antiinflammatory protein (cc10), and bronchiolar lining proteins. b, ros produced by club cells are also absorbed into capillaries within the lamina propria and are transferred by the circulatory system to pulmonary capillaries where they disrupt the air-blood barrier, causing degeneration and necrosis of type i pneumonocytes. this process leads to leakage of plasma fluid (alveolar edema [pink color]) and extravasation of erythrocytes (alveolar hemorrhage) and neutrophils (inflammation). ingested pneumotoxicants can be metabolized by the liver, leading to release of ros into the circulatory system that then disrupts the air-blood barrier in a similar manner. fig. 9 -77). microscopically, there are focal intraalveolar hemorrhages caused by larvae migrating through the alveolar walls. some larvae admixed with edematous fluid and cellular exudate (including eosinophils) may be visible in bronchioles and alveoli. the alveolar walls are thickened because of edema and a few inflammatory cells. clinical signs include cough and expiratory dyspnea to the point of oral breathing. hydatid cysts, the intermediate stage of echinococcus granulosus, can be found in the lungs and liver and other viscera of sheep and to a lesser extent in cattle, pigs, goats, horses, and human beings. the adult stage is a tapeworm that parasitizes the intestine of canidae. hydatidosis is still an important zoonosis in some countries, and perpetuation of the parasite life cycle results from animals being fed uncooked offal from infected sheep and consumption of uninspected meat. hydatid cysts are generally 5 to 15 cm in diameter, and numerous cysts can be found in the viscera of affected animals ( fig. 9-91 ). each parasitic cyst is filled with clear fluid; numerous daughter cysts attach to the wall, each containing several "brood capsules" with protoscolices inside. hydatid cysts have little clinical significance in animals but are economically important because of carcass condemnation. aspiration pneumonias. the inhalation of regurgitated ruminal contents or iatrogenic deposition of medicines or milk into the trachea can cause severe and often fatal aspiration pneumonia. bland substances, such as mineral oil, may incite only a mild suppurative or histiocytic bronchopneumonia, whereas some "home remedies" or ruminal contents are highly irritating and cause a fibrinous, necrotizing bronchopneumonia. the right cranial lung lobe tends to be more severely affected because the right cranial bronchus is the most cranial branch and enters the ventrolateral aspect of the trachea. however, the distribution may vary when animals aspirate while in lateral recumbency. in some severe cases, pulmonary necrosis can be complicated by infection with saprophytic organisms present in ruminal contents, causing fatal gangrenous pneumonia. aspiration pneumonia should always be considered in animals whose swallowing has been compromised-for example, those with cleft palate or hypocalcemia (milk fever). on the other hand, neurological diseases such as encephalitis (e.g., rabies) or encephalopathy (e.g., lead poisoning) should be investigated in animals in which the cause of aspiration pneumonia could not be caused by persistent immunologic stimuli; hypertrophy and hyperplasia of bronchiolar smooth muscle because of increased contraction and decreased muscle relaxation; and a few eosinophilic granulomas around the eggs and dead larvae. these granulomas, grossly, are gray, noncaseated nodules (2 to 4 mm in diameter) and may be confused with those seen at the early stages of tuberculosis. the clinical signs (coughing) vary with the severity of infection, and severe cases can be confused clinically with interstitial pneumonias. expiratory dyspnea and death can occur with heavy parasitic infestations when there is massive obstruction of airways. a different form of bovine pneumonia, an acute allergic reaction known as reinfection syndrome, occurs when previously sensitized adult cattle are exposed to large numbers of larvae (dictyocaulus viviparus). lesions in this syndrome are those of a hypersensitivity pneumonia as previously described. other lung parasites. ascaris suum is the common intestinal roundworm of pigs; larvae cannot complete their life cycle in calves, but the larvae can migrate through the lungs and cause severe pneumonia and death of calves within 2 weeks of infection. infection is usually acquired from the soil on which infested pigs were previously kept. the gross lesions are a diffuse interstitial pneumonia with hemorrhagic foci, atelectasis, and interlobular edema and it also occurs in canada, europe, australia, and probably elsewhere. this disease has two major clinicopathologic forms: one involves the central nervous system of goat kids and young goats and is characterized by a nonsuppurative leukoencephalomyelitis; the other form involves the joints of adult goats and is characterized by a chronic, nonsuppurative arthritis-synovitis. in addition, infection with cae virus can cause chronic lymphocytic interstitial pneumonia. the lentivirus of cae, caprine arthritis and encephalitis virus (caev), is closely related to visna/maedi virus and, in fact, cross infection with cae virus in sheep has been achieved experimentally. similar to maedi, cae infection presumably occurs during the first weeks of life when the doe transmits the virus to her offspring through infected colostrum or milk. horizontal transmission between infected and susceptible goats via the respiratory route has also been described. after coming into contact with mucosal cells at the portal of entry, the virus is phagocytized by macrophages, which migrate to the regional lymph nodes. infected macrophages are disseminated hematogenously to the central nervous system, joints, lungs, and mammary glands. like maedi, there is some evidence that the recruitment of lymphocytic cells results from dysregulation of cytokine production by infected macrophages and lymphocytes in affected tissues. it can take several months before serum antibodies can be detected in infected goats. grossly, the interstitial pneumonia is diffuse and tends to be most severe in the caudal lobes. the lungs are gray-pink and firm in texture with numerous, 1-to 2-mm, gray-white foci on the cut surface. the tracheobronchial lymph nodes are consistently enlarged. microscopically, the alveolar walls are thickened by lymphocytes and conspicuous hyperplasia of type ii pneumonocytes ( fig. 9-93 ). one important difference between the pneumonias of cae and maedi is that in cae the alveoli are filled with proteinaceous eosinophilic material (alveolar proteinosis), which in electron micrographs has structural features of pulmonary surfactant. the pulmonary form of cae can be mistaken for parasitic pneumonia (muellerius capillaris) because these two diseases have lymphocytic interstitial pneumonia and can coexist in the same goat. explained otherwise. depending on the nature of the aspirated material, histopathologic evaluation generally reveals foreign particles such as vegetable cells, milk droplets, and large numbers of bacteria in bronchi, bronchioles, and alveoli (efig. 9-18 ). vegetable cells and milk typically induce an early neutrophilic response followed by a histiocytic reaction with "foreign body" multinucleated giant cells (see efig. 9-12 ). special stains are used for the microscopic confirmation of aspirated particles in the lung (e.g., pas for vegetable cells and oil red-o for oil or milk droplets). maedi (visna/maedi). maedi is an important, lifelong, and persistent viral disease of sheep and occurs in most countries, except australia and new zealand. maedi means "shortness of breath" in the icelandic language, and it is known as graaff-reinet disease in south africa, zwoegerziekte in the netherlands, la bouhite in france, and ovine progressive pneumonia (opp) in the united states. more recently, the disease has also been referred to as ovine lentivirusinduced lymphoid interstitial pneumonia or simply lymphoid interstitial pneumonia (lip). maedi is caused by visna/maedi virus (vmv), a nononcogenic small ruminant lentivirus (srlv) of the family retroviridae that is antigenically related to the lentivirus causing caprine arthritisencephalitis (cae). seroepidemiologic studies indicate that infection is widespread in the sheep population, yet the clinical disease seems to be rare. the pathogenesis is incompletely understood, but it is known that transmission occurs largely vertically, through ingestion of infected colostrum, and horizontally, via inhalation of infected respiratory secretions. once in the body, the ovine lentivirus causes lifelong infections within monocytes and macrophages, including alveolar and pulmonary intravascular macrophages; clinical signs do not develop until after a long incubation period of 2 years or more. pulmonary lesions at the time of death are severe interstitial pneumonia and failure of the lungs to collapse when the thorax is opened. notable rib imprints, indicators of uncollapsed lungs, are often present on the pleural surface ( fig. 9-92 ). the lungs are pale, mottled, and typically heavy (two or three times normal weight), and the tracheobronchial lymph nodes are enlarged. microscopically, the interstitial pneumonia is characterized by balt hyperplasia and thickening of alveolar walls and peribronchial interstitial tissue by heavy infiltration of lymphocytes, largely t lymphocytes (see fig. 9 -75). recruitment of mononuclear cells into the pulmonary interstitium is presumably the result of sustainable production of cytokines by retrovirus-infected pulmonary macrophages and lymphocytes. hyperplasia of type ii pneumonocytes is not a prominent feature of maedi, likely because in this disease there is no injury to type i pneumonocytes, but there is some alveolar fibrosis and smooth muscle hypertrophy in bronchioles. secondary bacterial infections often cause concomitant bronchopneumonia. enlargement of regional lymph nodes (tracheobronchial) is due to severe lymphoid hyperplasia, primarily of b lymphocytes. the virus can also infect many other tissues, causing nonsuppurative encephalitis (visna), lymphocytic arthritis, lymphofollicular mastitis, and vasculitis. maedi is clinically characterized by dyspnea and an insidious, slowly progressive emaciation despite good appetite. death is inevitable once clinical signs are present, but it may take many months. caprine arthritis-encephalitis. caprine arthritis-encephalitis (cae) is a retroviral disease of goats (small ruminant lentivirus) that has a pathogenesis remarkably similar to that of visna/maedi in sheep. it was first described in the united states in the 1970s, but such as pasteurella multocida, pneumonia may progress to fibrinous or suppurative bronchopneumonia. one might expect some specific evidence pointing to the infectious agents (e.g., large intranuclear inclusion bodies in epithelial cells with adenoviral infection), but this is often not the case, either because examination is seldom done at the acute stage when the lesions are still present or because secondary bacterial infections mask the primary lesions. in the late stages, chronic enzootic pneumonia is characterized by hyperplastic bronchitis, atelectasis, alveolar and peribronchiolar fibrosis, and marked peribronchial lymphoid hyperplasia (cuffing pneumonia). ovine pneumonic mannheimiosis. ovine pneumonic mannheimiosis is one of the most common and economically significant diseases in most areas where sheep are raised. it is caused by mannheimia haemolytica and has a pathogenesis and lesions similar to those of pneumonic mannheimiosis of cattle. colonization and infection of lungs are facilitated by stressors such as changes in weather; handling; deworming; dipping; viral infections such as parainfluenza virus 3 (piv3), respiratory syncytial virus (rsv), and adenovirus; and probably chlamydiae and bordetella parapertussis infections. lesions are characterized by a severe fibrinous bronchopneumonia (cranioventral) with pleuritis ( fig. 9-94 and e-fig. 9-19 ). subacute to chronic cases progress to purulent bronchopneumonia, and sequelae include abscesses and fibrous pleural adhesions. a similar form of pneumonic mannheimiosis has been reported with increased frequency in bighorn sheep. septicemic pasteurellosis. septicemic pasteurellosis, a common ovine disease, is caused by bibersteinia trehalosi (formerly pasteurella trehalosi or mannheimia haemolytica biotype t) in lambs 5 months of age or older or by mannheimia haemolytica (biotype a) in lambs younger than 2 months of age. both organisms are carried in the tonsils and oropharynx of clinically healthy sheep, and under abnormal circumstances (particularly under stress from dietary or environmental changes) bacteria can invade adjacent tissues, enter the bloodstream, and cause septicemia. gross lesions include a distinctive necrotizing pharyngitis and tonsillitis; ulcerative esophagitis (efig. 9-20) ; severe congestion and edema of the lungs; focal hepatic necrosis; and petechiae in the mucosa of the tongue, esophagus, and intestine and particularly in the lungs and pleura. clinically, goats are active and afebrile but progressively lose weight despite normal appetite. the encephalitic or arthritic signs tend to obscure the respiratory signs, which are only evident on exertion. secondary bacterial bronchopneumonia is common in affected animals. bacterial pneumonias. in the past, pasteurella haemolytica was incriminated in four major ovine diseases known as (1) acute ovine pneumonic pasteurellosis (shipping fever), (2) enzootic pneumonia (nonprogressive chronic pneumonia), (3) fulminating septicemia, and (4) mastitis. under the new nomenclature, mannheimia haemolytica is responsible for ovine pneumonia resembling shipping fever in cattle (ovine pneumonic mannheimiosis), septicemia in young lambs (younger than 3 months of age), and ovine enzootic pneumonia and sporadic severe gangrenous mastitis in ewes. bibersteinia (pasteurella) trehalosi (formerly pasteurella haemolytica biotype t) is the agent incriminated in septicemia in lambs 5 to 12 months old. chronic enzootic pneumonia. in sheep, this entity is a multifactorial disease complex that, in contrast to ovine pneumonic mannheimiosis, causes only a mild to moderate pneumonia and it is rarely fatal. it generally affects animals younger than 1 year of age. significant costs associated with chronic enzootic pneumonia include reduction of weight gain, labor costs, veterinary fees, and slaughterhouse waste. the modifier "chronic" is used here to avoid any confusion with pneumonic mannheimiosis ("acute enzootic pneumonia"). it is also sometimes called atypical pneumonia, chronic nonprogressive pneumonia, proliferative pneumonia, or other names. chronic enzootic pneumonia is a clinical epidemiologic term and does not imply a single causal agent but is the result of a combination of infectious, environmental, and managerial factors. the list of infectious agents involved in ovine enzootic pneumonia includes mannheimia haemolytica, pasteurella multocida, parainfluenza virus 3 (pi-3), adenovirus, reovirus, respiratory syncytial virus (rsv), chlamydiae, and mycoplasmas (mycoplasma ovipneumoniae). in the early stages of enzootic pneumonia, a cranioventral bronchointerstitial pneumonia is characterized by moderate thickening of alveolar walls because of hyperplasia of type ii pneumonocytes. in some cases, when lungs are infected with secondary pathogens, viviparus of cattle. as seen in cattle with dictyocaulus viviparus, areas of atelectasis secondary to bronchiolar obstruction are present, particularly along the dorsal caudal aspects of the caudal lung lobes. microscopically, affected lungs are characterized by a catarrhal, eosinophilic bronchitis, with peribronchial lymphoid hyperplasia and smooth muscle hyperplasia of bronchi and bronchioles. bronchioles and alveoli can contain edematous fluid, eosinophils, and parasitic larvae and eggs. microscopic granulomas caused by aspirated eggs can be observed in the distal lung. the clinical signs (cough, moderate dyspnea, and loss of condition) and lesions relate mainly to obstruction of the small bronchi by adult worms and filaria. anemia of undetermined pathogenesis and secondary bacterial pneumonia are common in small ruminants with this parasitic disease. muellerius capillaris. muellerius capillaris, also called the nodular lungworm, occurs in sheep and goats in most areas of the world and is the most common lung parasite of sheep in europe and northern africa. it requires slugs or snails as intermediate hosts. the lesions in sheep are typically multifocal, subpleural nodules that tend to be most numerous in the dorsal areas of the caudal lung lobes ( fig. 9-95, a) . these nodules are soft and hemorrhagic in the early stages but later become gray-green and hard or even calcified. microscopically, a focal, eosinophilic, and granulomatous reaction occurs in the microscopically, the hallmark lesion is a disseminated intravascular thrombosis often with bacterial colonies in the capillaries of affected tissues. the alveolar capillaries contain bacteria and microthrombi, and the alveolar lumens have fibrin and red blood cells. mannheimia haemolytica and bibersteinia trehalosi are readily isolated from many organs. affected animals usually die within a few hours of infection, and these animals only rarely have clinical signs such as dullness, recumbency, and dyspnea. contagious caprine pleuropneumonia. a number of mycoplasma spp., often referred to as the "mycoides cluster," can produce respiratory tract infections in goats; however, only mycoplasma capricolum ssp. capripneumoniae is considered to cause contagious caprine pleuropneumonia. this disease is the goat counterpart of contagious bovine pleuropneumonia in cattle; sheep do not have a corresponding disease. this oie-notifiable disease is important in africa, the middle east, and areas of asia, but it is also seen elsewhere. the gross lesions caused by mycoplasma capricolum ssp. capripneumoniae are similar to those of the bovine disease and consist of a severe, often unilateral fibrinous bronchopneumonia and pleuritis; however, distention of the interlobular septa (which are normally not as well developed in goats as in cattle) and formation of pulmonary sequestra are less obvious than in the bovine disease. clinically, contagious caprine pleuropneumonia is similar to contagious bovine pleuropneumonia, with high morbidity and mortality, fever, cough, dyspnea, and increasing distress and weakness. other small ruminant mycoplasmas. pneumonia, fibrinous polyarthritis, septicemia, meningitis, mastitis, peritonitis, and abortion are possible manifestations of disease caused by mycoplasma mycoides ssp. mycoides large colony type and mycoplasma mycoides ssp. capri. the pathogenicity of other mycoplasmas, such as mycoplasma ovipneumoniae, mycoplasma arginini, and mycoplasma capricolum ssp. capricolum, in sheep and goats is still being defined and specific description of the lesions would be premature. these organisms probably cause disease only in circumstances similar to those for enzootic pneumonia, where host, infectious, and environmental factors create a complex interaction in the pathogenesis of the disease. it has been suggested that igg antibodies directed against ovine mycoplasmal antigens cross-react with ciliary proteins, causing inflammation and ciliary dysfunction, a condition in lambs referred to as coughing syndrome. tuberculosis. although tuberculosis has generally been considered uncommon in sheep and goats, caprine tuberculosis has become a significant disease in areas of spain and europe. mycobacterium caprae (formerly mycobacterium bovis ssp. caprae/mycobacterium tuberculosis ssp. caprae) is the most common cause, but infection with mycobacterium bovis or with the mycobacterium avium complex does occur when the disease is prevalent in other species in the locality. the pulmonary form, similar to that seen in cattle, is characterized by a granulomatous pneumonia with multiple, large, caseous, calcified, and well-encapsulated granulomas scattered throughout the lungs. intralesional acid-fast organisms within macrophages are not as abundant as in bovine tuberculosis. staphylococcus aureus. young sheep (2 to 12 weeks old) are susceptible to staphylococcus aureus septicemia (tick pyemia). this bacterium causes disseminated inflammation and abscesses in the joints, heart, liver, kidneys, and cns, and in the lung it can also produce bronchopneumonia and pulmonary abscesses (efig. 9-21 ). dictyocaulus filaria. dictyocaulus filaria, also called the large lungworm, is a serious, worldwide, parasitic disease of the lungs, most commonly of lambs and goat kids but occurring in adults as well. the life cycle and lesions are similar to those of dictyocaulus epithelial cells spreads rapidly throughout the nasal, tracheal, and bronchial mucosa, with the more severe outbreaks reflecting more involvement of intrapulmonary airways and secondary infection with pasteurella multocida, trueperella (arcanobacterium) pyogenes, or haemophilus spp. although uncommon, human beings infected with swine influenza (h1n1) can transmit the virus to pigs; therefore it is important that veterinarians or workers with influenza-like illness stay away from pig farms. natural transmission of h1n1 and h5n1 from human beings to ferrets (mustela putorius furo) and from human beings to cats and dogs has also been reported. pulmonary lesions caused by influenza virus alone are rarely seen in the postmortem room because this disease has a very low mortality rate unless complicated with secondary bacterial infections. grossly, a copious catarrhal to mucopurulent inflammation extends from the nasal passages to the bronchioles, with the volume of mucus being sufficient to plug small airways and cause a lobular or multilobular atelectasis in the cranioventral regions of the lungs. the appearance can be similar grossly, although not microscopically, to that of mycoplasma hyopneumoniae. fatal cases have severe alveolar and interstitial pulmonary edema. microscopically, the lesions in uncomplicated cases are typical of a virus-induced, necrotizing bronchitis-bronchiolitis, which in severe cases extends into the alveoli as bronchointerstitial pneumonia. it is characterized by necrosis of the bronchial/bronchiolar epithelium, thickening and infiltration of the alveolar wall with mononuclear cells and aggregates of macrophages, neutrophils, mucus, and some necrotic cells within the alveolar lumen. if these changes are extensive enough, the lumen of bronchioles can be occluded by exudate, causing lobular atelectasis. viral antigen can be demonstrated in infected epithelial cells by immunoperoxidase techniques. in the later stages of alveolar inflammation, neutrophils are progressively replaced by intraalveolar macrophages, unless the pneumonia is complicated by secondary bacterial infections. recent serologic surveys indicate that infection is also prevalent in wild pigs. clinically, a sudden onset of fever, nasal discharge, stiffness, labored breathing, weakness or even prostration, followed by painful and often paroxysmal coughing, is seen in animals of all age groups and may affect most of the herd. the outbreak subsides virtually without mortality within 1 or 2 weeks; the clinical appearance is much more alarming than the pathologic changes, unless the pigs have secondary infection with bacteria. infection can be confirmed using pcr in secretions collected with nasal swabs. the most important effect of most outbreaks of influenza is severe weight loss, but pregnant sows may abort or give birth to weak piglets. porcine reproductive and respiratory syndrome. a disease originally named mystery swine disease was first recognized in the united states in 1987. in 1990, it was seen in europe, and the disease now occurs worldwide in most major pig-raising countries. in 1991, dutch investigators isolated a virus as the etiologic agent; porcine reproductive and respiratory syndrome virus (prrsv) is currently classified in the genus arterivirus of the family arteriviridae. as its name implies, prrs is characterized by late-term abortions and stillbirths and respiratory problems. the respiratory form is generally seen in nursery and grow/finish pigs. the pathogenesis has not been completely elucidated, but it is presumed that there is a mucosal portal of entry with virus replication in macrophages of the lymphoid tissue, followed by viremia and finally dissemination of infected macrophages to the lungs and other organs, such as the thymus, liver (kupffer cells), spleen, lymph nodes, and intestine. the pulmonary alveolar and intravascular macrophages are the major targets for prrs virus, which induces apoptosis of these cells. the virus also downregulates the innate immune response by subpleural alveoli where the adults, eggs, and coiled larvae reside ( fig. 9-95, b) . clinical signs are usually not apparent. goats differ from sheep by having diffuse interstitial rather than focal lesions, and the reaction to the parasites seen microscopically varies from almost no lesions to a severe interstitial pneumonia with heavy infiltrates of mononuclear cells in alveolar walls resembling cae or mycoplasmal infections. secondary effects of muellerius capillaris infection in sheep and goats include decreased weight gain and possibly secondary bacterial infections. protostrongylus rufescens. protostrongylus rufescens is a worldwide parasite of sheep, goats, and wild ruminants. it requires an intermediate snail as a host. infection is usually subclinical, but protostrongylus rufescens can be pathogenic for lambs and goat kids and can cause anorexia, diarrhea, weight loss, and mucopurulent nasal discharge. the adult parasite lives in bronchioles as dictyocaulus spp., but it causes pulmonary nodules similar to those of muellerius capillaris. porcine pneumonias are unequivocally a major obstacle for the contemporary swine industry. the incidence, prevalence, and mortality rates of pneumonias in pigs depend on a series of complex, multifactorial interactions. among the most commonly recognized elements linked to porcine pneumonias are the following: • host (age, genetic makeup, immune status) • infectious agents (viruses, bacteria) • environmental determinants (humidity, temperature, ammonia concentrations) • management practices (crowding, mixing of animals, air quality, nutrition, stress) because of the nature of these multifactorial interactions, it will become obvious in the following paragraphs that more often than not a specific type of pneumonia frequently progresses to or coexists with another. the term porcine respiratory disease complex (prdc) has been introduced in clinical practice to describe pigs with signs of respiratory infection involving combined bacterial and viral infections. commonly implicated microbes include porcine reproductive and respiratory syndrome virus (prrsv), swine influenza virus (siv), porcine circovirus 2 (pcv2), porcine respiratory coronavirus (prcov), mycoplasma hyopneumoniae, and pasteurella multocida. swine influenza (swine flu). swine influenza is a highly contagious acute respiratory viral disease of swine that is caused by swine influenza virus (siv), a type a influenza virus of the family orthomyxoviridae. it is generally accepted that swine influenza resulted from adaptation of the type a influenza virus that caused the human influenza pandemic during world war i. the most common subtypes of siv currently circulating in pigs are h1n1, h1n2, and h3n2. swine influenza is enzootic worldwide and is known to infect human beings who are in close contact with sick pigs. in 2009, an outbreak of swine-human influenza (h1n1), presumably transmitted from pigs to human beings, emerged in mexico and rapidly spread to many countries throughout the world. this new "pandemic" was attributed to a triple-reassortant of influenza a virus containing gene segments of swine, eurasian avian, and human strains. human infection with this novel strain affected mainly children and young adults, as well as individuals of any age with an underlying debilitating condition. transmission between influenza-infected and susceptible pigs occurs mainly by aerosol or oral route. siv attaches to and replicates within epithelial cells of the upper respiratory tract; the infection of similar inclusions are occasionally seen in bronchial glandular and renal epithelial cells. the lungs show thickening of the alveolar walls because of hyperplasia of type ii pneumonocytes and interstitial infiltrates of mononuclear cells, peribronchiolar fibrous hyperplasia, and necrotizing bronchitis/bronchiolitis. circovirus can be confirmed in affected tissue by immunohistochemical or pcr techniques. dual infections with pcv2 and prrsv frequently occur in pigs, and secondary infections with pneumocystis carinii are commonly seen in pigs with this coinfection. characteristically, alveoli are filled with a distinctive foamy exudate that contains the organism, which is not visible in h&e-stained sections but is easily demonstrated with gomori's methenamine silver stain (see fig. 9-20) . in human beings, pneumocystis (carinii) jirovecii pneumonia (pneumocystosis) is one of the most common and often fatal complications in aids patients. as in aids patients, abnormal populations of cd4 + and cd8 + t lymphocytes have been incriminated as the underlying mechanism leading to pneumocystosis in foals and pigs. nipah virus. nipah virus belongs to the paramyxoviridae family and shares a genus (henipavirus) with the closely related hendra virus (see section on pneumonias of horses). another emerging zoonotic disease, nipah virus caused a major epidemic with significant human mortality in southeast asia in 1998 and 1999. people handling pigs were primarily affected. similar to hendra virus, fruit bats (flying foxes) act as natural reservoir and are involved in the transmission to pigs by poorly understood mechanisms. in pigs, this virus infects the respiratory system resulting in pneumonia with syncytial cells occurring in the vascular endothelium and in the respiratory epithelium at all levels of the lung. disease is spread to human beings via the respiratory route. human-to-human transmission of this virus has been reported in more recent outbreaks. other viral pneumonias of pigs. porcine respiratory coronavirus (prcov) is sporadically incriminated in pneumonia in pigs. this viral pneumonia is generally mild, and most pigs fully recover if the pneumonia is not complicated with other infections. lesions in the lung are those of bronchointerstitial pneumonia with necrotizing bronchiolitis. interestingly, infections with porcine and other respiratory coronaviruses have been used to investigate the pathogenesis of severe acute respiratory syndrome (sars), an emerging and highly contagious condition in human beings that is attributed to a novel human coronavirus (sars-cov). the relationship between sars-cov and animal coronavirus is still under investigation. other viruses rarely incriminated in porcine respiratory disease complex (prdc) include paramyxovirus, encephalomyocarditis virus, hemagglutinating encephalomyocarditis virus, and adenovirus. petechial hemorrhages in the lung and pulmonary edema may be seen with african swine fever, classical swine fever, and pseudorabies virus infections. porcine enzootic pneumonia. porcine enzootic pneumonia, a highly contagious disease of pigs caused by mycoplasma hyopneumoniae, is grossly characterized by suppurative or catarrhal bronchopneumonia ( fig. 9-96 and efig. 9-23 ). when its worldwide prevalence and deleterious effect on feed conversion are taken into account, this disease is probably the most economically significant respiratory disease of pigs. although an infectious disease, it is very much influenced by immune status and management factors, such as crowding (airspace and floor space), ventilation (air exchange rate), concentrations of noxious gases in the air (ammonia and hydrogen sulfide), relative humidity, temperature fluctuations, and mixing of stock from various sources. it has been demonstrated with inhibiting interferons and deregulates the adaptive immune response, thus interfering with the normal defense mechanisms predisposing pigs to septicemia and bacterial pneumonia. the most common opportunistic organisms are streptococcus suis, salmonella choleraesuis, mycoplasma hyopneumoniae, haemophilus parasuis, bordetella bronchiseptica, pasteurella multocida, and pneumocystis carinii. dual viral infections with prrsv and porcine circovirus 2 (pcv2), siv, and porcine respiratory coronavirus (prcov) are commonly found in pigs, and such coinfections increase the severity of disease. on postmortem examination, pulmonary lesions vary from very mild changes characterized by failure of the lung to collapse when the thorax is opened and the presence of rib imprints (see fig. 9 -74) to severe changes manifested by consolidation of the lung in cases that have been complicated with bacterial pneumonia. tracheobronchial and mediastinal lymph nodes are typically enlarged. microscopically, pulmonary changes are those of interstitial pneumonia characterized by thickening of alveolar walls by infiltrating macrophages and lymphocytes and mild hyperplasia of type ii pneumonocytes. necrotic cells are scattered in the alveolar lumens. unlike some other viral infections, bronchiolar epithelium does not appear to be affected. diagnosis of prrs in tissue collected at necropsy can be confirmed by immunohistochemistry and pcr techniques. infected pigs may become carriers and transmit the infection through body fluids and semen. clinically, prrs in nursery and young growing animals is characterized by sneezing, fever, anorexia, dyspnea, cough, and occasional death. some piglets develop severe cyanosis of the abdomen and ears, which explains why this syndrome was named blue ear disease when first described in europe. porcine circovirus-associated disease. another emerging porcine syndrome, characterized clinically by progressive emaciation in weaned pigs, was originally described in the 1990s in canada, the united states, and europe. since then, it has disseminated to many countries, causing economic devastation in pig farms worldwide. because of the clinical signs and lesions in many organs, this syndrome was named postweaning multisystemic wasting syndrome (pmws). porcine circovirus 2 (pcv2) has been incriminated as the etiologic agent and is a member of the circoviridae family. pcv2 has been associated with a number of syndromes in pigs, including systemic pcv2 infection (the preferred term for pmws because it may also affect mature pigs), pcv2-associated pneumonia, pcv2-associated enteritis, porcine dermatitis and nephropathy syndrome (pdns), pcv2-associated reproductive failure, and, most recently, pcv2-associated cerebellar vasculitis. the diseases caused by pcv2 are now collectively known as porcine circovirus-associated disease (pcvad); the most common manifestations are systemic pcv2 infection (pmws) and pcv2-associated pneumonia as part of the porcine respiratory disease complex. all of these manifestations affect more than one organ, and there is substantial overlap between the syndromes. at necropsy, pigs with systemic pcv2 infection (pmws) and pcv2-associated pneumonia are often in poor body condition, and the most remarkable changes, not considering other possible secondary infections, are enlargement of the superficial and visceral lymph nodes and a mild interstitial pneumonia characterized by failure of the lungs to collapse when the thorax is opened. jaundice is occasionally observed. microscopically, the lymphoid tissues show lymphoid depletion, histiocytic replacement of follicles, and notable proliferation of parafollicular histiocytes, some of which fuse and form syncytial cells (granulomatous lymphadenitis); necrosis of the lymphoid follicles is seen less often. in some cases, large basophilic inclusion bodies are present singly or as grapelike clusters (botryoid inclusions) within the cytoplasm of macrophages, particularly in peyer's patches, spleen, and lymph nodes (efig. 9-22 ). chapter 9 respiratory system, mediastinum, and pleurae peribronchial, bronchiolar, and alveolar interstitium. additional virulence factors include the ability of mycoplasma hyopneumoniae to cause immunosuppression, reduce the phagocytic activity of neutrophils in the lung, and change the chemical composition of mucus. all of these functional alterations can predispose the lung to secondary bacterial infections. the lesions caused by mycoplasma hyopneumoniae start as a bronchointerstitial pneumonia and progress to a suppurative or mucopurulent bronchopneumonia once secondary pathogens are involved (commonly seen at necropsy). in most pigs, gross lesions affect only portions of the cranial lobes, but in more severely affected pigs, lesions involve 50% or more of the cranioventral portions of the lungs (see fig. 9 -96). the affected lungs are dark red in the early stages but have a homogeneous pale-gray ("fish flesh") appearance in the more chronic stages of the disease. on cut surface, exudate can easily be expressed from airways, and depending on the stage of the lesions and secondary infections, the exudate varies from purulent to mucopurulent to mucoid. microscopic lesions are characterized by an influx of macrophages and neutrophils into the bronchi, bronchioles, and alveoli, and with time there is also notable balt hyperplasia (see fig. 9-96, b) . in some cases, accumulation of exudate can be severe enough to cause occlusion of bronchioles and atelectasis of the corresponding lobules. the suppurative bronchopneumonia may be accompanied by a mild fibrinous pleuritis, which is often more severe if other organisms, such as mycoplasma hyorhinis, pasteurella multocida, or actinobacillus pleuropneumoniae, are also involved. abscesses and fibrous pleural adhesions are sequelae of chronic complicated infections. clinically, enzootic pneumonia occurs as a herd problem in two disease forms. a newly acquired infection of a previously clean herd causes disease in all age groups, resulting in acute respiratory distress and low mortality. in a chronically infected herd, the mature animals are immune and clinical signs are usually apparent only in growing pigs at times of particular stress such as at weaning. in such herds, coughing and reduced rate of weight gain are the most notable signs. porcine pasteurellosis. porcine pasteurellosis is an infectious disease complex with unclear pathogenesis that includes primary infections by pasteurella multocida alone (primary pasteurellosis) or, more frequently, after the defense mechanisms are impaired and a secondary bacterium colonizes the lung (porcine pneumonic pasteurellosis). in rare cases, pasteurella multocida causes acutely fatal septicemias in pigs (primary septicemic pasteurellosis). it is important to remember that pasteurella multocida serotypes a and d are both part of the normal nasal flora and are also causative agents of bronchopneumonia, pleuritis, and atrophic rhinitis in pigs. pasteurella multocida is one of the most common secondary pathogens isolated from the lungs of pigs with swine influenza virus (siv), porcine reproductive and respiratory syndrome virus (prrsv), porcine circovirus 2 (pcv2), pseudorabies (suhv-1), classical swine fever (hog cholera), enzootic pneumonia, and porcine pleuropneumonia. secondary infections with pasteurella multocida notably change the early and mild bronchointerstitial reaction of enzootic and viral pneumonias into a severe suppurative bronchopneumonia with multiple abscesses and sometimes pleuritis. the other important role of pasteurella multocida in porcine pneumonias is as a cause of a fulminating, cranioventral, fibrinous bronchopneumonia (pleuropneumonia) after influenza virus infection or stress from inadequate ventilation resulting in high levels of ammonia in the air. the nature of the lesion and the predisposing factors of poor management or coexisting viral infections suggest that fulminating porcine pasteurellosis has a pathogenesis similar to that of pneumonic mannheimiosis of cattle. pharyngitis with subcutaneous cervical edema, fibrinohemorrhagic polyarthritis, and focal lymphocytic pcr that mycoplasma hyopneumoniae is present in the air of infected farms. the causative agent, mycoplasma hyopneumoniae, is a fastidious organism and very difficult to grow; thus the final diagnosis is frequently based on interpretation of lesions alone or supported by ancillary tests to detect this mycoplasma in affected lungs by immunohistochemistry, immunofluorescence, or pcr. the bronchopneumonic lesions of porcine enzootic pneumonia are in most cases mild to moderate, and thus mortality is low unless complicated with secondary pathogens, such as pasteurella multocida, trueperella (arcanobacterium) pyogenes, bordetella bronchiseptica, haemophilus spp., mycoplasma hyorhinis, and other mycoplasmas and ureaplasmas. although the pathogenesis of porcine enzootic pneumonia is not completely elucidated, it is known that mycoplasma hyopneumoniae first adheres to the cilia of the bronchi by means of a unique adhesive protein, produces ciliostasis, and finally colonizes the respiratory system by firmly attaching to the ciliated epithelial cells of the trachea and the bronchi of the cranioventral regions of the lungs. once attached to the respiratory epithelium, it provokes an influx of neutrophils into the tracheobronchial mucosa; causes extensive loss of cilia (deciliation); stimulates an intense hyperplasia of lymphocytes in the balt; and attracts mononuclear cells into the factors have been identified. these factors allow actinobacillus pleuropneumoniae to attach to cells; produce pores in cell membranes; damage capillaries and alveolar walls, resulting in vascular leakage and thrombosis; impair phagocytic function; and elicit failure of clearance mechanisms. the gross lesions in the acute form consist of a fibrinous bronchopneumonia characterized by severe consolidation and a fibrinous exudate on the pleural surface. although all lobes can be affected, a common site is the dorsal area of the caudal lobes. in fact, a large area of fibrinous pleuropneumonia involving the caudal lobe of a pig's lung is considered almost diagnostic for this disease (fig. 9-97) . on cut surface, consolidated lungs have notably dilated interlobular septa and irregular but well-circumscribed areas of necrosis caused by potent cytotoxins produced by actinobacillus pleuropneumoniae. except for the distribution, pulmonary lesions of porcine pleuropneumonia are identical to those of pneumonic mannheimiosis of cattle. the microscopic lesions are also very similar and include areas of coagulative necrosis surrounded by a thick cluster of "streaming (oat-shaped/oat cell) leukocytes" and notable distention of the interlobular septa because of severe edema and lymphatic thrombosis. bronchioles and alveoli are filled with edematous fluid, fibrin, neutrophils, and few macrophages (see fig. 9 -97). pigs with the chronic form have multiple pulmonary abscesses and large (2 to 10 cm) pieces of necrotic lung encapsulated by connective tissue (sequestra)-changes frequently seen in slaughterhouses. interstitial nephritis are also present in porcine pneumonic pasteurellosis. sequelae of porcine pneumonic pasteurellosis include fibrous pleuritis and pericarditis, pulmonary abscesses, so-called sequestra, and usually death. in contrast to ruminants, mannheimia haemolytica is not a respiratory pathogen for pigs, but in some instances, it can cause abortion in sows. porcine pleuropneumonia. porcine pleuropneumonia is a highly contagious, worldwide disease of pigs caused by actinobacillus (haemophilus) pleuropneumoniae (app), which is characterized by a severe, often fatal, fibrinous bronchopneumonia with extensive pleuritis (pleuropneumonia). survivors generally develop notable residual lesions and become carriers of the organisms. porcine pleuropneumonia is an increasingly important cause of acute and chronic pneumonias, particularly in intensively raised pigs (2 to 5 months old). transmission of actinobacillus pleuropneumoniae occurs by the respiratory route, and the disease can be reproduced experimentally by intranasal inoculation of the bacterium. considered a primary pathogen, actinobacillus pleuropneumoniae can sporadically produce septicemia in young pigs and otitis media and otitis interna with vestibular syndrome in weaned pigs. two biovars and 15 serotypes of the organism have been identified; all serotypes can cause the disease, but differences in virulence exist. the pathogenesis is not yet well understood, but specific virulence factors, such as rtx toxins (hemolytic/cytolytic toxins apx i to apx iv), capsular factors, fimbriae and adhesins, lipopolysaccharide, and permeability tuberculosis. tuberculosis is an important disease in domestic and wild pigs that has a much greater prevalence in pigs than in cattle or other domestic mammals in many countries. porcine tuberculosis is attributed to infection with mycobacterium bovis and porcine mycobacteriosis to infection with mycobacterium avium complex. a common scenario in small mixed-farming operations is the diagnosis of avian tuberculosis at the time that pigs are slaughtered, and the source is ingestion of tuberculous chickens or contaminated litter. as would be expected, granulomas are found in the mesenteric, mandibular, and retropharyngeal lymph nodes; to a lesser extent in the intestine, liver, and spleen; and only in rare cases in the lung. the route of infection in pulmonary tuberculosis and mycobacteriosis of pigs is most often hematogenous after oral exposure and intestinal infection. lung lesions are those of a granulomatous pneumonia. the microscopic lesions are basically those of tubercles (granulomas), but the degree of encapsulation, caseation, and calcification varies with the type of mycobacterium, age of the lesion, and host immune response. other bacterial pneumonias of pigs. septicemias in pigs often cause petechial hemorrhages in the lung and pulmonary edema. salmonellae, escherichia coli, and listeria monocytogenes can cause severe interstitial pneumonia in very young animals. salmonella choleraesuis causes a necrotizing fibrinous pneumonia similar to porcine pleuropneumonia, and salmonella typhisuis causes a chronic suppurative bronchopneumonia. in high health herds, actinobacillus suis may cause fibrinohemorrhagic pleuropneumonia and is easily confused with porcine pleuropneumonia. metastrongylosis. metastrongylus apri (elongatus), metastrongylus salmi, and metastrongylus pudendotectus (lungworms) of domestic and feral pigs occur throughout most of the world and require earthworms as intermediate hosts for transmission. the incidence of disease has therefore decreased with development of confinement housing. the importance of pig lungworms is mainly because infection results in growth retardation of the host. clinical signs include coughing because of parasitic bronchitis. the gross lesions, when noticeable, consist of small gray nodules, particularly along the ventral borders of the caudal lobes. the adult worms are grossly visible in bronchi, and microscopically, the parasites cause a catarrhal bronchitis with infiltration of eosinophils and lobular atelectasis ( fig. 9-99) . ascaris suum. the larvae of ascaris suum can cause edema, focal subpleural hemorrhages, and interstitial inflammation (see fig. 9 -77). along their larval migration tracts, hemorrhages also occur in the liver and, after fibrosis, become the large white "milk spots" seen so frequently as incidental findings at necropsy. it has been reported that ascaris suum may cause immunosuppression in severely affected pigs. pigs can be killed if exposed to an overwhelming larval migration. other causes of pneumonia. foreign body granulomatous pneumonia occurs frequently in pigs after inhalation of vegetable material (starch pneumonia), presumably from dusty (nonpelleted) feed. lesions are clinically silent but are often mistaken for other pneumonic processes during inspection at slaughterhouses. microscopically, pulmonary changes are typical of foreign body granulomatous inflammation in which variably sized feed particles are surrounded by macrophages and neutrophils, and often have been phagocytosed by multinucleated giant cells. feed (vegetable) particles appear as thick-walled polygonal cells that stain positive with pas because of their rich carbohydrate (starch) content (see efig. 9-12) . clinically, porcine pleuropneumonia can vary from an acute form with unexpected death and blood-stained froth at the nostrils and mouth to a subacute form characterized by coughing and dyspnea accompanied by clinical signs of sepsis such as high fever, hypoxemia, anorexia, and lethargy (efig. 9-24) . a chronic form is characterized by decreased growth rate and persistent cough. animals that survive often carry the organism in the tonsils, shed the organism, and infect susceptible pigs. haemophilus pneumonia. in addition to glasser's disease characterized by polyserositis (pericarditis, pleuritis, peritonitis, polyarthritis, and meningitis) (efig. 9-25) , some serotypes of haemophilus parasuis (originally haemophilus influenzae suis) can also cause suppurative bronchopneumonia that in severe cases can be fatal. the causal organism, haemophilus parasuis, is usually carried in the nasopharynx of normal pigs and requires abnormal circumstances such as those following stress (weaning and cold weather) or viral infections (swine influenza or pcv2). specific pathogen-free (spf) pigs seem to be particularly susceptible to glasser's disease (arthritis and serositis) but not to pulmonary infection (bronchopneumonia). streptococcal pneumonia. streptococcus suis is a common cause of porcine disease worldwide and a serious zoonosis capable of causing death by septic shock or meningitis and residual deafness in butchers, veterinarians, and pig farmers. typically, streptococcus suis gains entrance to the susceptible young pig through the oropharyngeal mucosa and is carried in the tonsils, nasal mucosa, and mandibular lymph nodes of healthy animals, particularly in survivors of an outbreak. infected sows can abort or vertically transmit the infection to their offspring. some serotypes of streptococcus suis cause neonatal septicemia, and this can result in suppurative meningitis, otitis, arthritis, polyserositis, myocarditis, valvular endocarditis, and embolic pneumonia ( fig. 9-98 ). other serotypes of streptococcus suis can reach the lung by the aerogenous route and cause a suppurative bronchopneumonia, in combination with pasteurella multocida, escherichia coli, or mycoplasma hyopneumoniae, or in combination with actinobacillus pleuropneumoniae, which causes a fibrinous bronchopneumonia. coinfections of streptococcus suis with pcv2 and prrsv are also frequently seen in some farms. gross lesions in the acute stages include serous to catarrhal to mucopurulent nasopharyngitis and conjunctivitis. the lungs are edematous and have a diffuse interstitial pneumonia ( fig. 9 -100) microscopically characterized by necrotizing bronchiolitis, necrosis and exfoliation of pneumonocytes, mild alveolar edema, and, several hours later, thickening of the alveolar walls because of interstitial mononuclear cell infiltrates and hyperplasia of type ii pneumonocytes. secondary infections with bordetella bronchiseptica and mycoplasmas are common and induce life-threatening suppurative bronchopneumonia. the thymus may be small relative to the age of the animal because of viral-induced lymphocytolysis. microscopically, eosinophilic inclusions are present in the epithelial cells of many tissues, in the nuclei or cytoplasm, or in both (see fig. 9 -100). they appear early in the bronchiolar epithelium but are most prominent in the epithelium of the lung, stomach, renal pelvis, and urinary bladder, making these tissues good choices for diagnostic examination. viral inclusions are rarely seen in the later stages of this disease. the suppurative secondary bronchopneumonias often hinder the detection of viral lesions in the lung, particularly because bronchiolar cells containing inclusion bodies exfoliate and mix with the neutrophils recruited by the bacterial infection. distemper virus antigens can be readily demonstrated in infected cells by the immunoperoxidase technique (see fig. 9 -100), which can also be used in skin biopsies for the antemortem diagnosis of canine distemper. distemper virus also has a tendency to affect developing tooth buds and ameloblasts, causing enamel hypoplasia in dogs that recover from infection. of all distemper lesions, demyelinating encephalomyelitis, which develops late, is the most devastating (see chapter 14). sequelae to distemper include the nervous and pneumonic complications mentioned previously and various systemic infections, such as toxoplasmosis and sarcocystosis, because of depressed immunity. persistent viral infection occurs in some dogs that survive the disease, and they may become carriers and the source of infection for other susceptible animals. clinical signs consist of biphasic fever, diarrhea, vomiting, weight loss, mucopurulent oculonasal discharge, coughing, respiratory distress, and possible loss of vision. weeks later, hyperkeratosis of the foot pads ("hard pad") and the nose are observed, along with nervous signs, including ataxia, paralysis, convulsions, or residual myoclonus (muscle twitches, tremors, and "tics"). in general, inflammatory diseases of the lungs are less of a problem in dogs than in food-producing species and can be subdivided in two major groups, infectious and noninfectious pneumonias. "canine infectious respiratory disease" (cird) is the term currently used by clinicians to describe a heterogeneous group of respiratory infections in dogs; these diseases were previously clustered under the name of infectious tracheobronchitis or "kennel cough." cird is the canine counterpart of brd and prd complexes in cattle and pigs, respectively. the most common viruses in cird include canine parainfluenza virus (cpiv), canid herpesvirus 1 (cahv-1), canine adenovirus-2 (cav-2), canine respiratory coronavirus (crcov), canine distemper virus (cdv), and canine influenza virus (civ). bordetella bronchiseptica, streptococcus equi ssp. zooepidemicus, and mycoplasma spp. are the most frequent bacterial isolates in cird. it has been recently recognized that animal shelters are an important source of viral and bacterial infections for dogs and cats. uremia and paraquat toxicity are perhaps the two most notable noninfectious causes of canine respiratory disease. canine distemper. canine distemper is an important and ubiquitous infectious disease of dogs, other canidae, wild felidae, mustelidae, and marine mammals throughout the world. it is caused by a morbillivirus that is antigenically related to the human measles, rinderpest (officially eradicated in 2011), "peste de petit ruminants," and phocine distemper viruses. canine distemper virus (cdv) is transmitted to susceptible puppies through infected body fluids. the virus invades through the upper respiratory tract and conjunctiva, proliferates in regional lymph nodes, becomes viremic, and in dogs with an inadequate antibody response, infects nearly all body tissues (pantropic), particularly the epithelial cells. distemper virus hampers the immune response, downregulates cytokine production, and persists for a long time in some tissues. cdv can target the lungs either directly as a viral pneumonia or indirectly by its immunosuppressive effects rendering the lungs susceptible to secondary bacterial and protozoal infections, or as a coinfection with other viruses such as canine adenovirus-2 and canid herpesvirus 1. 15:292-294, 2003.) inclusion bodies occur within epithelial cells in early lesions. cahv-1 has also been identified as a cause of ulcerative keratoconjunctivitis in older dogs. canine influenza (canine flu). canine influenza is an emerging contagious respiratory infection of dogs that was first described in the united states and subsequently in other countries. it has a high morbidity (close to 100%), but the mortality, as with most other influenza infections, is relatively low (less than 8%). this disease, first diagnosed in greyhounds, is caused by a novel influenza-a virus (canine influenza virus or civ), a mutation from a previously recognized h3n8 strain of equine influenza virus. dog-to-dog transmission does occur and therefore this infection must be distinguished from other viruses of the canine infectious respiratory disease (cird) group. pulmonary lesions are generally mild and transient, but infected dogs are susceptible to secondary bacterial bronchopneumonia. the most relevant lesions in dogs dying unexpectedly from canine influenza are pleural and pulmonary hemorrhages. microscopically, there is necrotizing tracheitis, bronchitis, and bronchiolitis with exudation of neutrophils and macrophages. in severe cases, hemorrhagic interstitial or bronchointerstitial pneumonia may be accompanied by vasculitis and thrombosis. influenza antigen can be demonstrated by immunohistochemistry in airway epithelium and alveolar macrophages. clinically, dogs with canine influenza are lethargic, inappetent, and hyperthermic and frequently cough and show nasal discharge. these signs resemble those seen in dogs with kennel cough or secondary bacterial pneumonia. in addition, there are confirmed cases of canine influenza caused by the porcine h1n1 presumably transmitted from infected pet owners. bacterial pneumonias. dogs generally develop bacterial pneumonias when the pulmonary defense mechanisms have been impaired. pasteurella multocida, streptococcus spp., escherichia coli, klebsiella pneumoniae, and bordetella bronchiseptica can be involved in pneumonia secondary to distemper or after aspiration of gastric contents ( fig. 9-102 and efig. 9-27 ). streptococcus zooepidemicus can cause acute and fatal hemorrhagic pleuropneumonia with canine adenovirus type 2 infection. cav-2 infection is a common but transient contagious disease of the respiratory tract of dogs, causing mild fever, oculonasal discharge, coughing, and poor weight gain. the portal of entry is generally by inhalation of infected aerosols followed by viral replication in the surface cells of the upper respiratory tract, mucous cells of the trachea and bronchi, nonciliated bronchiolar epithelial cells, and type ii pneumonocytes. pulmonary lesions are initially those of bronchointerstitial pneumonia, with necrosis and exfoliation of bronchiolar and alveolar epithelium, edema, and, a few days later, proliferation of type ii pneumonocytes, mild infiltration of neutrophils and lymphocytes in the alveolar interstitium, and hyperplastic bronchitis and bronchiolitis. large basophilic intranuclear viral inclusions are typically seen in bronchiolar and alveolar cells ( fig. 9-101) . infection with cav-2 is clinically mild unless complicated with a secondary bacterial infection or coinfections with other viruses such as distemper virus. experimental work suggests cav-2 reinfection may lead to hyperreactive airways, a nonspecific condition in which the bronchial mucosa becomes highly "responsive" to irritation such as that caused by cold air, gases, or cigarette smoke. however, it is not clear if this outcome is true in natural infections. canid herpesvirus 1. canid herpesvirus 1 (cahv-1) can cause fatal systemic disease in newborn puppies and is probably a contributing factor in "fading puppy syndrome." hypothermia has been suggested as a pivotal component in the pathogenesis of fatal infections in puppies. many dogs are seropositive, suggesting that transient or subclinical infections are more common than realized; the virus remains latent in the trigeminal and other ganglia and can be reactivated after stress, resulting in asymptomatic transmission of cahv-1 virus to offspring via the placenta, thus resulting in abortion or stillbirths. in puppies, cahv-1 causes ulcerative tracheitis, interstitial pneumonia (efig. 9-26) , and focal necrosis and inflammation in the kidneys, liver, and brain. eosinophilic intranuclear aspiration pneumonia starts as an acute necrotizing bronchitis and bronchiolitis caused by aspiration of irritant materials such as gastric acid or a caustic material administered by mouth. the aspirate also contains potentially pathogenic bacteria, and because the mucociliary apparatus is damaged and these bacteria are not removed, they settle into the ventral portions of the lung (from gravity) and provoke a fibrinosuppurative and necrotizing bronchopneumonia. b, bronchoalveolar spaces are filled with neutrophils, macrophages, and bacteria (arrows). h&e stain. inset, large colonies of bacteria (arrows). h&e stain. (courtesy dr. a. lópez, atlantic veterinary college.) a b infection; thus it most frequently affects outdoor and hunting dogs. from the lung, infection is disseminated hematogenously to other organs, mainly bone, skin, brain, and eyes. pulmonary lesions are characterized by multifocal to coalescing pyogranulomatous pneumonia, generally with firm nodules scattered throughout the lungs (fig. 9-103) . microscopically, nodules are pyogranulomas with numerous macrophages (epithelioid cells), some neutrophils, multinucleated giant cells, and thick-walled yeasts (see fig. 9 -35, c). yeasts are 5 to 25 µm in diameter and are much better visualized when they are stained with pas reaction or gomori's methenamine silver stain. nodules can also be present in other tissues, chiefly lymph nodes, skin, spleen, liver, kidneys, bones, testes, prostate, and eyes. this fungus can be easily identified in properly prepared and stained transtracheal washes or lymph node aspirates. clinical signs can reflect involvement of virtually any body tissue; pulmonary effects include cough, decreased exercise tolerance, and terminal respiratory distress. coccidioidomycosis. coccidioidomycosis (san joaquin valley fever), caused by the dimorphic fungus coccidioides immitis, occurs mainly in animals living in arid regions of the southwestern united states, mexico, and central and south america. it is a primary respiratory tract (aerogenous) infection commonly seen at slaughterhouses in clinically normal feedlot cattle. in dogs, coccidioidomycosis also has an aerogenous portal of entry and then a b hemorrhagic pleural effusion in dogs. death is generally a consequence of severe sepsis and septic shock or from β-hemolytic streptococcal bacteremia causing emboli in the lungs, liver, brain, and lymph nodes. the primary source of the infection cannot be determined in most cases. dental disease in dogs may be a source of systemic and pulmonary infection, a concept wellrecognized in human medicine for many years. the role of mycoplasmas in canine pneumonia is still uncertain because these organisms are frequently isolated from normal nasopharyngeal flora. tuberculosis is uncommon in dogs because these animals appear to be quite resistant to infection; most cases occur in immunocompromised dogs or in dogs living with infected human beings. dogs are susceptible to the infection with mycobacterium tuberculosis, mycobacterium bovis, and mycobacterium avium complex, and therefore canine infection presupposes contact with human or animal tuberculosis. the clinicopathologic manifestation is pulmonary after inhalation or alimentary after oral exposure, but in most cases infection is disseminated to lymph nodes and visceral organs. the gross lesions are multifocal, firm nodules with necrotic centers, most often seen in the lungs, lymph nodes, kidneys, and liver. diffuse granulomatous pleuritis and pericarditis with copious serofibrinous or sanguineous effusion are common. microscopically, granulomas are formed by closely packed macrophages but with very little connective tissue. mycotic pneumonias. mycotic pneumonias are serious diseases seen commonly in animals in some regions. there are two main types: those caused by opportunistic fungi and those caused by a group of fungi associated with systemic "deep" mycoses. all of these fungi affect human beings and most domestic animals but are probably not transmitted between species. aspergillosis. opportunistic fungi, such as aspergillus spp. (particularly aspergillus fumigatus), are important in birds, but in domestic animals, they mainly affect immunosuppressed individuals or those on prolonged antibiotic therapy. the pulmonary lesion is a multifocal, nodular, pyogranulomatous, or granulomatous pneumonia. microscopically, there is necrosis and infiltrates of neutrophils, macrophages, and lymphocytes, with proliferation of fibroblasts eventually leading to encapsulation of the granuloma. fungal hyphae are generally visible in the core of the lesion and in the walls of blood vessels. systemic mycoses (dimorphic fungal infections) . systemic (deep) mycoses are caused by blastomyces dermatitidis, histoplasma capsulatum, coccidioides immitis, and cryptococcus neoformans/ cryptococcus gatti (see fig. 9 -35). blastomycosis mainly affects dogs and is discussed here, whereas cryptococcosis is discussed in the section on pneumonias of cats. in contrast to other fungi, such as aspergillus spp., organisms of the systemic mycosis group are all primary pathogens of human beings and animals and thus do not necessarily require a preceding immunosuppression to cause disease. these fungi have virulence factors that favor hematogenous dissemination and evasion of immune and phagocytic responses. systemic dissemination is often exacerbated by the administration of immunosuppressant drugs such as corticosteroids. these fungi are usually detected by cytological evaluation of affected tissues. blastomycosis. blastomycosis occurs in many countries of the north american continent, africa, the middle east, and occasionally in europe. in the united states, it is most prevalent in the atlantic, st. lawrence, and ohio-mississippi river valley states, compared with the mountain-pacific region. blastomyces dermatitidis is a dimorphic fungus (mycelia-yeast) seen mainly in young dogs and occasionally in cats and horses. this fungus is present in the soil, and inhalation of spores is considered the principal route of from the alveolar interstitium associated with larvae or dead worms because little reaction develops to the live adults. crenosoma vulpis. crenosoma vulpis is a lungworm seen commonly in foxes and sporadically in dogs with access to the intermediate hosts-slugs and snails. the adult lungworms live in small bronchi and bronchioles in the caudal lobes, causing eosinophilic and catarrhal bronchitis manifested grossly as gray areas of inflammation and atelectasis. in some animals, crenosoma vulpis causes bronchiolar goblet cell metaplasia and mucous obstruction, resulting in lobular atelectasis due to the valve effect of the mucous plug. eucoleus aerophilus. eucoleus aerophilus (capillaria aerophila) is a nematode parasite typically found in the trachea and bronchi of wild and domestic carnivores. in some cases, this parasite may also involve the nasal passages and sinuses. although generally asymptomatic, some dogs cough because of the local irritation caused by the parasites on the tracheal or bronchial mucosa. paragonimus spp. paragonimus kellicotti in north america and paragonimus westermani in asia are generally asymptomatic fluke infections in fish-eating species. the life cycle involves two intermediate hosts, the first a freshwater snail and the second a freshwater crab or crayfish; in north america, cats and dogs acquire infection by eating crayfish. gross lesions include pleural hemorrhages where the metacercariae migrate into the lungs. later, multifocal eosinophilic pleuritis, and subpleural cysts up to 7 mm long containing pairs of adult flukes, are found along with eosinophilic granulomas around clusters of eggs. like many other parasitic pneumonias, lesions and scars are more frequent in the caudal lobes. pneumothorax can occur if a cyst that communicates with an airway ruptures to the pleural surface. other parasitic infections. angiostrongylus vasorum and dirofilaria immitis are parasites of the pulmonary arteries and right ventricle and, depending on the stage, can produce different forms of pulmonary lesions. adult parasites can cause chronic arteritis that leads to pulmonary hypertension, pulmonary arterial thrombosis, interstitial (eosinophilic) granulomatous pneumonia, pulmonary interstitial fibrosis, congestive right-sided cardiac failure, and eventually caudal vena caval syndrome. other lesions include pleural petechial hemorrhages and, in later stages, diffuse pulmonary hemosiderosis and multifocal pulmonary infarcts. larvae and eggs also cause alveolar injury, thickening of the alveolar walls with eosinophils and lymphocytes (interstitial pneumonia), and multifocal or coalescing granulomas with giant cells (parasitic granulomas). pneumocystis carinii has been reported as a sporadic cause of chronic interstitial pneumonia in dogs with a compromised immune system (see pneumonias of horses; also see fig. 9 -20). aspiration pneumonia. aspiration pneumonia is an important form of pneumonia that occurs in dogs when vomit or regurgitated materials are aspirated into the lungs, or when drugs or radiographic contrast media are accidentally introduced into the airways (efig. 9-28) . as in other animal species, aspiration pneumonia may be unilateral or may more often affect the right cranial lobe ( fig. 9-104 ). the severity of lesions depends very much on the chemical and microbiologic composition of the aspirated material. in general, aspiration in monogastric animals, particularly in dogs and cats, is more severe because of the low ph of the gastric contents (chemical pneumonitis). in severe cases, dogs and cats die rapidly from septic shock and ards (see fig. 9 -63), which is microscopically characterized by diffuse alveolar damage, protein-rich pulmonary edema, neutrophilic alveolitis, and formation of typical hyaline membranes along the alveolar walls (see fig. 9-104 ). in animals that survive the acute stages of aspiration, pulmonary lesions progress to bronchopneumonia. aspiration pneumonia is a common sequela to disseminates systemically to other organs. clinical signs relate to the location of lesions, so there can be respiratory distress, lameness, generalized lymphadenopathy, or cutaneous lesions, among others. the lesions caused by coccidioides immitis consist of focal granulomas or pyogranulomas that can have suppurative or caseated centers. the fungal organisms are readily seen in histologic or cytologic preparation as large (10 to 80 µm in diameter), double-walled, and highly refractile spherules containing numerous endospores (see fig. 9-35, d) . histoplasmosis. histoplasmosis is a systemic infection that results from inhalation and, in dogs, possibly ingestion of another dimorphic fungus, histoplasma capsulatum. histoplasmosis occurs sporadically in dogs and human beings and, to a lesser extent, in cats and horses. bats often eliminate histoplasma capsulatum in the feces, and droppings from bats and birds, particularly pigeons, heavily promote the growth and survival of this fungus in the soil of enzootic areas. pulmonary lesions are grossly characterized by variably sized, firm, poorly encapsulated granulomas and, sometimes, more diffuse involvement of the lungs. microscopically, granulomatous lesions typically have many macrophages filled with small (1 to 3 µm), punctiform, intracytoplasmic, dark oval bodies (yeasts) (see fig. 9 -35, a) that are best demonstrated with pas reaction or gomori's methenamine silver stain. similar nodules or diffuse involvement can be present in other tissues, chiefly lymph nodes, spleen, intestine, and liver. toxoplasmosis. toxoplasmosis is a worldwide disease caused by the obligate intracellular, protozoal parasite toxoplasma gondii. cats and other felidae are the definitive hosts in which the mature parasite divides sexually in the intestinal mucosa. human beings, dogs, cats, and many wild mammals can become intermediate hosts after accidental ingestion of fertile oocysts shed in cat feces or ingestion of undercooked or raw meat containing tissue cysts, and fetuses can be infected transplacentally from an infected dam. in most instances, the parasite infects many cells of different tissues and induces an antibody response (seropositive animals) but does not cause clinical disease. toxoplasmosis is often triggered by immunosuppression, such as that caused by canine distemper virus. toxoplasmosis is characterized by focal necrosis around the protozoan. pulmonary lesions are severe, multifocal necrotizing interstitial pneumonia with notable proliferation of type ii pneumonocytes and infiltrates of macrophages and neutrophils. other lesions in disseminated toxoplasmosis include multifocal necrotizing hepatitis, myocarditis, splenitis, myositis, encephalitis, and ophthalmitis. the parasites appear microscopically as small (3 to 6 µm) basophilic cysts that can be found free in affected tissues or within the cytoplasm of many epithelial cells and macrophages (see efig. 8-8) . similar findings can be seen sporadically in dogs infected with neospora caninum and sarcocystis canis, and immunohistochemistry would be required to differentiate those protozoal organisms from toxoplasma gondii. filaroides hirthi. filaroides hirthi, a lungworm of the alveoli and bronchioles of dogs, has long been known as a cause of mild subclinical infection in large colonies of beagle dogs in the united states. however, it can on occasion cause severe and even fatal disease in individual pets, presumably as a result of immunosuppression. clinical signs may include coughing and terminal respiratory distress. grossly, the lesions are multifocal subpleural nodules, often with a green hue because of eosinophils, scattered throughout the lungs. microscopically, these nodules are eosinophilic granulomas arising 548.e1 chapter 9 respiratory system, mediastinum, and pleurae other pneumonias. idiopathic pulmonary fibrosis is a rare condition of uncertain etiology reported in the west highland white terrier breed that shares similarities with human and feline idiopathic pulmonary fibrosis. microscopically, there is diffuse interstitial pneumonia and progressive alveolar fibrosis with capillary obliteration, hyperplasia of type ii cells, some of which exhibit cellular atypia, and finally hypertrophy and hyperplasia of smooth muscle. the interstitial fibrosis eventually spills over alveolar spaces causing conspicuous intraalveolar fibrosis. although upper respiratory tract infections are common and important in cats, pneumonias are uncommon except when there is immunosuppression or aspiration of gastric contents. viral infections such as feline rhinotracheitis and calicivirus may cause lesions in the lungs, but unless there is secondary invasion by bacteria, they do not usually cause a fatal pneumonia. feline rhinotracheitis. feline rhinotracheitis is an important viral disease of cats caused by the ubiquitous felid herpesvirus 1 (fehv-1). this infection affects primarily young or debilitated cats causing inflammation in the nasal, ocular, and tracheal mucosa and, to a much lesser extent, the lung (see species-specific diseases of the nasal cavity and paranasal sinuses). when lungs are affected, fehv-1 causes bronchointerstitial pneumonia with necrosis of bronchiolar and alveolar epithelium, thickening of the alveolar walls, and extensive permeability edema. eosinophilic intranuclear inclusion bodies may be seen in infected epithelial cells early in infection. feline calicivirus. feline calicivirus (fcv) causes upper respiratory disease, stomatitis, conjunctivitis, and, to a lesser extent, interstitial pneumonia. microscopically, affected lungs exhibit the typical pattern of bronchointerstitial pneumonia with necrotizing bronchiolitis, thickening of alveolar walls, occasionally hyaline membranes, hyperplasia of type ii pneumonocytes, and macrophages admixed with cellular debris in the alveolar lumens. because pulmonary lesions are similar to those caused by fehv-1, isolation or in situ detection is required for final diagnosis. feline infectious peritonitis. feline infectious peritonitis (fip) is caused by fip virus (fipv), a mutated form of feline enteric cleft palate, and in dogs with megaesophagus secondary to either myasthenia gravis or persistent right aortic arch. it is also an important complication of general anesthesia or neurologic diseases affecting laryngeal function. paraquat. paraquat, a broad-spectrum herbicide widely used in gardening and agriculture, can cause severe and often fatal toxic interstitial pneumonia (pneumonitis) in dogs, cats, human beings, and other species. after ingestion or inhalation, this herbicide selectively accumulates in the lung where paraquat toxic metabolites are produced by club (clara) cells. these metabolites promote local release of free radicals in the lung, which causes extensive injury to club cells and to the blood-air barrier, presumably through lipid peroxidation of type i and ii pneumonocytes and alveolar endothelial cells (see fig. 9 -89). paraquat toxicity has been used experimentally as a model of oxidant-induced alveolar injury and pulmonary fibrosis. soon after poisoning, the lungs are heavy, edematous, and hemorrhagic because of extensive necrosis of epithelial and endothelial cells in the alveolar walls. the lungs of animals that survive acute paraquat toxicosis are pale, fail to collapse when the thorax is opened, and have interstitial emphysema, bullous emphysema, and occasionally pneumomediastinum. microscopic findings in the acute and subacute phases include necrosis of type i pneumonocytes, interstitial and alveolar edema, intraalveolar hemorrhages, and proliferation of type ii pneumonocytes. in the chronic stages (4 to 8 weeks later), the lesions are typically characterized by severe interstitial and intraalveolar fibrosis. uremic pneumopathy. uremic pneumonopathy (pneumonitis) is one of the many extrarenal lesions seen in dogs with chronic uremia. lesions are characterized by a combination of pulmonary edema and calcification of vascular smooth muscle and alveolar basement membranes. in severe cases, alveolar calcification prevents lung collapse when the thorax is opened. in the more advanced cases, the lungs appear diffusely distended, pale red or brown in color, and show a rough pleural surface with rib imprints (see fig. 9 -51). on palpation, the pulmonary parenchyma has a typical "gritty" texture because of mineralization of the alveolar and vascular walls, which are best visualized microscopically by using special stains such as von kossa (see fig. 9 -51). because this is not primarily an inflammatory lesion, the term pneumonitis should not be used. fig. 9-63) . a, note that the lungs did not collapse when the thorax was opened (loss of negative pressure) and as a result fill almost the entire thoracic cavity. the cranioventral aspects of the lung are consolidated with hemorrhage. b, alveolar capillary congestion, thick hyaline membranes along the alveolar septa (arrows), and intraalveolar hemorrhage. these microscopic changes are typical of the diffuse alveolar damage seen in lungs with ards. h&e stain. (courtesy dr. a. lópez, atlantic veterinary college.) feline calicivirus has removed chlamydophila felis from its previously overstated importance as a lung pathogen. tuberculosis. cats are susceptible to three types of mycobacterial infections: classic tuberculosis, feline leprosy, and atypical mycobacteriosis. classic tuberculosis in cats is rare and generally caused by mycobacterium bovis and mycobacterium microti but also, to a lesser extent, by mycobacterium tuberculosis. nosocomial tuberculosis (mycobacterium bovis) in cats has been reported with increased frequency. the usual route of infection for feline tuberculosis is oral, through infected rodents/meat or unpasteurized milk, so the granulomatous lesions are mainly in the intestine and mesenteric lymph nodes where they may disseminate through infected phagocytes to other organs. the solid and noncaseated appearance of tuberculous nodules is grossly similar to that of neoplasms, so they must be differentiated from pulmonary neoplasms (e.g., lymphoma). classic tuberculosis with dermal lesions in cats should be differentiated from feline leprosy (localized skin granulomas) caused by mycobacterium lepraemurium and other nonculturable species of acid-fast bacilli. atypical mycobacteriosis is caused by contamination of a skin wound with saprophytic and nonsaprophytic mycobacteria such as those of the mycobacterium avium complex. advances in pcr techniques have notably reduced the time required for etiologic diagnosis of mycobacteriosis in veterinary diagnostic laboratories. cryptococcosis. cryptococcosis (pulmonary cryptococcus neoformans or cryptococcus gatti) is the most frequent systemic mycosis in cats, and lesions are akin to those discussed in the section on mycotic pneumonias of dogs. it occurs worldwide in all species but is diagnosed most frequently in cats, horses, dogs, and human beings. some healthy dogs and cats harbor cryptococcus in the nasal cavity and become asymptomatic carriers. clinical infection may occur in immunocompetent cats and in cats that are immunologically compromised, such as by felv, fiv, malnutrition, or corticosteroid treatment. lesions can occur in nearly any tissue, resulting in a wide c coronavirus (fecv), and is one of a few viral infections of domestic animals that result in pyogranulomatous pneumonia. this disease is microscopically characterized by a vasculitis affecting many tissues and organs ( fig. 9-105) . other viral pneumonias. other viruses sporadically incriminated in feline interstitial pneumonia are cowpox virus (cpxv) and influenza a h1n1. pasteurellae. bacteria from the nasal flora such as pasteurella multocida and pasteurella-like organisms are occasionally associated with secondary bronchopneumonia in cats ( fig. 9-106) . pasteurella multocida also causes otitis media and meningitis, but its role as a respiratory pathogen is mainly associated with pyothorax. interestingly, there are reports of pasteurella multocida pneumonia in older or immunosuppressed human beings acquired through contact with domestic cats. mycoplasmas. mycoplasmas are often isolated from the lungs of cats with pulmonary lesions but are not definitively established as primary pathogens in feline pneumonias. feline pneumonitis. the term feline pneumonitis is a misnomer because the major lesions caused by chlamydophila felis (formerly chlamydia psittaci) are severe conjunctivitis and rhinitis (see species-specific diseases of the nasal cavity and paranasal sinuses). the elucidation of the importance of feline viral rhinotracheitis and organism infects erythrocytes in the erythrocytic stage of disease and multiplies in intravascular macrophages/monocytes, including those in the alveolar capillaries (efig. 9-29) , during the leukocytic stage of disease. aspiration pneumonia. aspiration pneumonias are common in cats as a result of vomiting, regurgitation, dysphagia, or anesthetic complication or after accidental administration of food, oral medicaments, or contrast media into the trachea (iatrogenic). pulmonary lesions are similar to those described for dogs, and the type of lung lesion depends on the chemical and bacterial composition of the aspirated material (see the section on aspiration pneumonia of dogs). feline idiopathic pulmonary fibrosis. feline idiopathic pulmonary fibrosis is a rare, progressive, and fatal disease of cats of uncertain etiology characterized by multifocal fibrotic nodules subpleurally and randomly in the lung making the pleural surface resemble nodular cirrhosis of the liver ( fig. 9-108) . microscopically, the affected alveolar and peribronchiolar interstitium is thickened by excessive fibrosis, abundant deposition of extracellular matrix, and hypertrophy of smooth muscle. some investigators suggest an intrinsic cellular defect in type ii pneumonocytes as the underlying cause. the alveolar walls are diffusely lined by cuboidal hyperplastic type ii pneumonocytes, and the alveolar lumens often contain exfoliated cells and necrotic debris. this feline condition has morphologic features similar to "equine multinodular pulmonary fibrosis" and "cryptogenic pulmonary fibrosis" in human beings. fetal pneumonias. pneumonia is one of the most frequent lesions found in fetuses submitted for postmortem examination, particularly in foals and food-producing animals. because of autolysis, lack of inflation, and the lungs being at various stages of development, fetal lesions are often missed or misdiagnosed. in the nonaerated fetal lung, the bronchoalveolar spaces are filled with a viscous, locally produced fluid known as lung fluid or lung liquid. it has been estimated that an ovine fetus produces approximately 2.5 ml of "lung fluid" per kilogram of body weight per hour. in the variety of clinical signs. however, granulomatous rhinitis, sinusitis, otitis media and interna, pneumonia, ulcerative dermatitis, and meningoencephalitis are most common. the pulmonary lesion in cryptococcosis is a multifocal granulomatous pneumonia and, like those occurring in other internal organs, they are small, gelatinous, white foci. the gelatinous appearance is due to the broad mucous capsule around the yeast (see fig. 9-35, b) . microscopically, lesions contain great numbers of fungal organisms (4 to 10 µm in diameter without the capsule) and only a few macrophages, lymphocytes, and multinucleated giant cells. this thick polysaccharide capsule does not stain well with h&e, and thus there is a large empty space or halo around the yeast. feline lungworm. aelurostrongylus abstrusus, known as feline lungworm, is a parasite that occurs in cats wherever the necessary slug and snail intermediate hosts are found. it can cause chronic respiratory disease with coughing and weight loss and, sometimes, severe dyspnea and death, particularly if there are secondary bacterial infections. the gross lesions are multifocal, amber, and subpleural granulomatous nodules up to 1 cm in diameter throughout the lungs. on incision, these nodules may contain viscous exudate. microscopically, the adult parasites, eggs, and coiled larvae are in the bronchioles and alveoli, where they cause catarrhal bronchiolitis, hyperplasia of submucosal glands, and, later, granulomatous alveolitis, alveolar fibrosis, and fibromuscular hyperplasia ( fig. 9-107) . during routine examination of feline lungs, it is quite common to find fibromuscular hyperplasia in bronchioles and arterioles in otherwise healthy cats. it was alleged in the past that this fibromuscular hyperplasia was a long-term sequela of subclinical infection with aelurostrongylus abstrusus. however, this view has been challenged; thus the pathogenesis and significance of pulmonary fibromuscular hyperplasia in healthy cats remains uncertain. in severe cases, fibromuscular hyperplasia is grossly visible in the lungs as white subpleural nodules. other parasitic pneumonias. toxoplasma gondii, paragonimus kellicotti, and dirofilaria immitis can also affect cats (see the section on parasitic pneumonias of dogs). cytauxzoon felis is an apicomplexan hemoparasite that affects domestic and wild felidae. the diseases that cause fetal pneumonia in farm animals. gross lesions in the lungs are generally undetected, but microscopic lesions include focal necrotizing interstitial pneumonia and focal necrosis in the liver, spleen, or brain. fetal bronchointerstitial pneumonia also occurs in some viral abortions, such as those caused by infectious bovine rhinotracheitis (ibr) virus and bovine parainfluenza virus 3 (bpiv-3) in cattle and equine viral rhinopneumonitis (evr) in horses. fetal pneumonias in dogs and cats are infrequently described, perhaps because aborted puppies and kittens are rarely submitted for postmortem examination. with advancements in molecular biology techniques, the etiologic diagnosis of abortions and their association with pulmonary fetal lesions is rapidly improving. neonatal pneumonias and septicemias. these entities are rather common in newborn animals lacking passive immunity because of the lack of either ingestion or absorption of maternal colostrum (failure of passive transfer or hypogammaglobulinemia). in addition to septicemias causing interstitial pneumonia, farm animals with hypogammaglobulinemia can develop bronchopneumonia by inhalation of bacterial pathogens. these include histophilus somni and pasteurella multocida in calves; streptococcus spp. in foals; and escherichia coli, listeria monocytogenes, and streptococcus suis in pigs. meconium aspiration syndrome. meconium aspiration syndrome (mas) is an important but preventable condition in human babies that originates when amniotic fluid contaminated with meconium is aspirated during labor or immediately after birth. the pathogenesis of mas is basically the same as in those of fetal bronchopneumonia (see fig. 9-109) . fetal hypoxia, a common event during dystocia or prolonged parturition, causes the fetus to relax the anal sphincter and release meconium into the amniotic fluid. aspiration of meconium can occur directly from aspirating contaminated amniotic fluid before delivery (respiratory movements with an open glottis) or immediately after delivery when the meconium lodged in the nasopharynx is carried into the lung with the first breath of air. this latter form of aspiration is prevented in delivery rooms by routine suction of the nasopharynx in meconium-stained babies. mas is well known in human babies, but the occurrence and significance in animals remains largely unknown. mas has been reported in calves, foals, piglets, and puppies. although pulmonary lesions are generally mild and transient, aspiration of meconium can be life-threatening for newborn babies and animals because it typically occurs in compromised neonates already suffering from intrauterine hypoxia and acidosis. neonatal acidosis is known to impair colostrum absorption in calves. common mas sequelae are lobular atelectasis, pulmonary hypertension, and possibly airway hyperreactivity. in the most severe cases of mas, focal (patchy) atelectasis can be observed grossly in the lung, indicating failure of the lungs to be fully aerated because of the mechanical obstruction and the chemical effect of meconium on pulmonary surfactant (see fig. 9 -52). microscopically, meconium and keratin exfoliated from skin of the fetus into the amniotic fluid are present in bronchi, bronchioles, and alveoli and accompanied by mild alveolitis characterized by infiltration of leukocytes followed by alveolar macrophages and occasional giant cells (efig. 9-30) . lung cancer in animals is rare, unlike in human beings, in which the incidence is alarming and continues to be the number one cause of death due to cancer in canada, the united states, and europe. interestingly, prostatic and breast cancers, so much feared by men fetus, this fluid normally moves along the tracheobronchial tree, reaching the oropharynx, where a fraction is swallowed into the gastrointestinal tract, and a small portion is released into the amniotic fluid. at the time of birth, the lung fluid is rapidly reabsorbed from the lungs by alveolar absorption and lymphatic drainage. aspiration of amniotic fluid contaminated with meconium and bacteria from placentitis is the most common route by which microbial pathogens reach the fetal lungs. this form of pneumonia is secondary to fetal hypoxia and acidosis ("fetal distress"), which cause the fetus to relax the anal sphincter, release meconium into the amniotic fluid, and, in the terminal stages, inspire deeply with open glottis, resulting in the aspiration of contaminated fluid ( fig. 9-109 ). gross lesions are only occasionally recognized, but microscopic changes are similar to those of a bronchopneumonia. microscopically, bronchoalveolar spaces contain variable numbers of neutrophils, macrophages, epidermal squames, and pieces of meconium that appear as bright yellow material because of its bile content. in contrast to postnatal bronchopneumonia, lesions in fetuses are not restricted to the cranioventral aspects of the lungs but typically involve all pulmonary lobes. in cattle, brucella abortus and trueperella (arcanobacterium) pyogenes are two of the most common bacteria isolated from the lungs of aborted fetuses. these bacteria are usually present in large numbers in the amniotic fluid of cows with bacterial placentitis. inflammation of the placenta interferes with oxygen exchange between fetal and maternal tissue, and the resultant fetal hypoxia induces the fetus to "breathe" with an open glottis and aspirate the amniotic fluid. aspergillus spp. (mycotic abortion) and ureaplasma diversum cause sporadic cases of placentitis, which results in fetal pneumonia and abortion. in addition to the respiratory route (aspiration), pathogens, such as bacteria and viruses, can also reach the lungs via fetal blood and cause interstitial pneumonia. listeriosis (listeria monocytogenes), salmonellosis (salmonella spp.), and chlamydiosis (chlamydophila abortus [c. psittaci]) are the best known examples of blood-borne primary benign neoplasms of the lungs, such as pulmonary adenomas, are highly unusual in domestic animals. most primary neoplasms are malignant and appear as solitary masses of variable size that, with time, can metastasize to other areas of the lungs and to distant organs. it is sometimes difficult on gross and microscopic examination to differentiate primary lung cancer from pulmonary metastasis resulting from malignant neoplasms elsewhere in the body. it is often difficult to determine the precise topographic origin of a neoplasm within the lungs-for example, whether it originates in the conducting system (bronchogenic carcinoma), transitional system (bronchiolar carcinoma), exchange system (alveolar carcinoma), or bronchial glands (bronchial gland carcinoma). according to the literature, pulmonary carcinomas in animals arise generally from club (clara) cells or type ii pneumonocytes of the bronchioloalveolar region, in contrast to those in human beings, which are mostly bronchogenic. tumors located at the hilus generally arise from major bronchi and tend to be a solitary large mass with occasional small metastasis to the periphery of the lung. in contrast, tumors arising from the bronchioloalveolar region are often multicentric with numerous peripheral metastases in the lung parenchyma. because of histologic architecture and irrespective of the site of origin, many malignant epithelial neoplasms are classified by the all-encompassing term of pulmonary adenocarcinomas. dogs and cats are the species most frequently affected with primary pulmonary neoplasms, largely carcinomas, generally in older animals. the mean age for primary lung tumors is 11 years for dogs and 12 years for cats. pulmonary carcinomas in other domestic animals, except for retrovirus-induced pulmonary carcinoma in sheep, are less common, possibly because fewer farm animals are allowed to reach their natural life span. these neoplasms can be invasive or expansive, vary in color (white, tan, or gray) and texture (soft or firm), and often have areas of necrosis and hemorrhage, which result in a "craterous" or "umbilicate" appearance. this umbilicate appearance is frequently seen in rapidly growing carcinomas in which the center of the tumoral mass undergoes necrosis as a result of ischemia. some lung neoplasms resemble pulmonary consolidation or large granulomas. cats with moderately differentiated neoplasms had significantly longer survival time (median, 698 days) than cats with poorly differentiated neoplasms (median, 75 days). dogs with primary lung neoplasms, grades i, ii, and iii, had survival times of 790, 251, and 5 days, respectively. ovine pulmonary adenocarcinoma (ovine pulmonary carcinoma). ovine pulmonary adenocarcinoma, also known as pulmonary adenomatosis and jaagsiekte (from the south african afrikaans word for "driving sickness"), is a transmissible, retrovirus-induced neoplasia of ovine lungs caused by jaagsiekte sheep retrovirus (jsrv). it occurs in sheep throughout the world, with the notable exception of australia and new zealand; its incidence is high in scotland, south africa, and peru and unknown but probably low in north america. this pulmonary carcinoma behaves very much like a chronic pneumonia, and jsrv shares many epidemiologic similarities with the ovine lentivirus responsible for maedi and the retrovirus responsible for enzootic nasal carcinoma in small ruminants. pulmonary adenomatosis has been transmitted to goats experimentally but is not known to be a spontaneous disease in that species. ovine pulmonary adenocarcinoma affects mainly mature sheep but can occasionally affect young stock. intensive husbandry probably facilitates horizontal transmission by the copious nasal discharge and explains why the disease occurs as devastating epizootics with 5% to 80% mortality when first introduced into a flock. differential diagnosis between maedi and pulmonary adenomatosis can prove difficult because both diseases often coexist in the same flock and women, are a distant second. to say that cigarette smoking is responsible for this epidemic of lung cancer is unnecessary. although dogs have been proposed as valuable "sentinels" for environmental hazards, such as exposure to passive smoking, asbestos, dyes, and insecticides, it is not known if the prevalence of canine lung tumors has increased in geographical areas with high contamination. alterations in genes (oncogenes) and chromosomes and changes in biologically active molecules have been linked to lung cancer in recent years. as with many other forms of cancer, epidemiologic studies indicate that the incidence of pulmonary neoplasms increases with age, but there are still insufficient data to confirm that particular canine or feline breeds have a higher predisposition to spontaneous lung neoplasms. a standard nomenclature of pulmonary neoplasms in domestic animals is lacking, and as a consequence, multiplicity of names and synonyms occur in the veterinary literature. some classifications are based on the primary site, whereas others emphasize more the histomorphologic type. the most common types of benign and malignant pulmonary neoplasms in domestic mammals are listed in box 9-2. clinically, the signs of pulmonary neoplasia vary with the degree of invasiveness, the amount of parenchyma involved, and locations of metastases. signs may be vague, such as cough, lethargy, anorexia, weight loss, and perhaps dyspnea. in addition, paraneoplastic syndromes, such as hypercalcemia, endocrinopathies, and pulmonary hypertrophic osteoarthropathy, have been associated with pulmonary neoplasms. primary neoplasms of the lungs. primary neoplasms of the lungs arise from cells normally present in the pulmonary tissue and can be epithelial or mesenchymal, although the latter are rare. any malignant tumor metastatic from another body location (e.g., osteosarcoma in dogs, uterine carcinoma in cows, and malignant melanoma in horses) box 9-2 classification of pulmonary neoplasms 553.e1 chapter 9 respiratory system, mediastinum, and pleurae abundant cytoplasm containing numerous acidophilic granules, which are positive for pas and for s-100 protein using immunohistochemistry. although this tumor can cause bronchial obstruction and respiratory signs, in most cases, it is an incidental finding in older horses submitted for postmortem examination. lymphomatoid granulomatosis. lymphomatoid granulomatosis is a rare but interesting pulmonary disease of human beings, dogs, cats, and possibly horses and donkeys characterized by nodules or large solid masses in one or more lung lobes. these frequently metastasize to lymph nodes, kidneys, and liver. microscopically, tumors are formed by large pleomorphic mononuclear (lymphomatoid) cells with a high mitotic rate and frequent formation of binucleated or multinucleated cells. tumor cells have a distinct tendency to grow around blood vessels and invade and destroy the vascular walls. lymphomatoid granulomatosis has some resemblance to lymphoma and is therefore also referred to as angiocentric lymphoma; phenotypic marking confirms that neoplastic cells are a mixed population of plasma cells, b and t lymphocytes, and histiocytes. cerebral and cutaneous forms of lymphomatoid granulomatosis have also reported in human beings, dogs, and cats. secondary neoplasms of the lungs. secondary neoplasms of the lungs are all malignant by definition because they are the result of metastasis to the lungs from malignant neoplasms elsewhere. because the pulmonary capillaries are the first filter met by tumor emboli released into the vena cava or pulmonary arteries, secondary neoplasms in the lung are relatively common in comparison to primary ones. also, secondary tumors can be epithelial or mesenchymal in origin. common metastatic tumors of epithelial origin are mammary, thyroid ( fig. 9-111) , and uterine carcinomas. tumors of mesenchymal origin are osteosarcoma ( fig. 9-112, a) ; hemangiosarcoma ( fig. 9-112, b) ; malignant melanoma in dogs; lymphoma in cows, pigs, dogs, and cats ( fig. 9-113) ; and vaccineassociated sarcoma in cats. usually, secondary pulmonary neoplasms are multiple; scattered throughout all pulmonary lobes (hematogenous dissemination); of variable size; and, according to the growth pattern, can be nodular, diffuse, or radiating (efig. 9-31) . the appearance of metastatic neoplasms differs according to the type of neoplasm. for example, dark red cystic nodules containing blood indicate hemangiosarcoma, dark black solid nodules indicate melanoma, and hard solid nodules (white, yellow, or tan color) with bone spicules indicate osteosarcoma. the gross appearances of or in the same animal. death is inevitable after several months of the initial onset of respiratory signs, and a specific humoral immune response to jsrv is undetectable in affected sheep. during the early stages of ovine pulmonary carcinoma, the lungs are enlarged, heavy, and wet and have several firm, gray, variably sized nodules that in some cases can be located in the cranioventral lobes mimicking a bronchopneumonic lesion ( fig. 9-110, a) . in the later stages, the nodules become confluent, and large segments of both lungs are diffusely, but not symmetrically, infiltrated by neoplastic cells. on cross section, edematous fluid and a copious mucoid secretion are present in the trachea and bronchi ( fig. 9-110, b) . microscopically, the nodules consist of cuboidal or columnar epithelial cells lining airways and alveoli and forming papillary or acinar (glandlike) structures (see fig. 9-110, a) . because the cells have been identified ultrastructurally as originating from both type ii alveolar epithelial cells and club (clara) cells, the neoplasm is considered a "bronchioloalveolar" carcinoma. sequelae often include secondary bronchopneumonia, abscesses, and fibrous pleural adhesions. metastases occur to tracheobronchial and mediastinal lymph nodes and, to a lesser extent, to other tissues such as pleura, muscle, liver, and kidneys. neoplastic cells stain strongly positive for jsrv using immunohistochemistry. clinically, ovine pulmonary adenocarcinoma is characterized by a gradual loss of condition, coughing, and respiratory distress, especially after exercise (e.g., herding or "driving"). appetite and temperature are normal, unless there are secondary bacterial infections. an important differentiating feature from maedi (interstitial pneumonia) can be observed if animals with pulmonary adenomatosis are raised by their hind limbs; copious, thin, mucoid fluid, produced by neoplastic cells in the lungs, pours from the nostrils of some animals. carcinoid (neuroendocrine) tumor of the lungs. carcinoid tumor of the lungs is a neoplasm presumably arising from neuroendocrine cells and is sporadically seen in dogs as multiple, large, firm pulmonary masses close to the mainstem bronchi. it has also been reported in the nasal cavity of horses. tumor cells are generally polygonal with finely granular, pale, or slightly eosinophilic cytoplasm. nuclei are small, and mitotic figures are absent or rare. granular cell tumor. granular cell tumor is a rare and locally invasive tumor that has been reported mainly in human beings and older horses. the cell origin of this tumor was thought to be the myoblast, but it is currently presumed to be schwann cells, which are normally present in the bronchovascular bundles of the lung. microscopically, neoplastic cells are large, polyhedron-shaped with metastatic carcinomas are generally similar to the primary neoplasm and sometimes have umbilicated centers. proper diagnoses of pulmonary neoplasms in live animals require history, clinical signs, radiographs, cytologic analysis of bal fluid, and, when necessary, a lung biopsy. identification of a specific lineage of neoplastic cells in biopsy or postmortem specimens is often difficult and requires electron microscopy or immunohistochemical techniques. electron microscopy allows identification of distinctive cellular components such as osmiophilic lamellar phospholipid nephritic bodies in alveolar type ii epithelial cells or melanosomes in melanomas. immunohistochemical staining is also helpful in identifying tumor cells. the thoracic wall, diaphragm, and mediastinum are lined by the parietal pleura, which reflects onto the lungs at the hilum and continues as the visceral pleura, covering the entire surface of the lungs, except at the hilus where the bronchi and blood vessels enter. the space between the parietal and visceral pleura (pleural space) is only minimal and under normal conditions contains only traces of clear fluid, which is a lubricant, and a few exfoliated cells. samples of this fluid are obtained by thoracocentesis, a simple procedure in which a needle is passed into the pleural cavity. volumetric, biochemical, and cytologic changes in this fluid are routinely used in veterinary diagnostics. anomalies 7 congenital defects are rare and generally of little clinical significance. cysts within the mediastinum of dogs and, less often, cats in severe cases, the amount of fluid present in the thoracic cavity can be considerable. for instance, a medium-size dog can have 2 l of fluid, and a cow may accumulate 25 l or more. excessive fluid in the thorax causes compressive atelectasis resulting in respiratory distress (see fig. 9 -54). hydrothorax is most commonly seen in cattle with right-sided heart failure or cor pulmonale (hydrostatic) (efig. 9 -32); dogs with congestive heart failure (hydrostatic), chronic hepatic disease (hepatic hydrothorax) ( fig. 9-114) , or nephrotic syndrome (hypoproteinemia); pigs with mulberry heart disease (increased vascular permeability); and horses with african horse sickness (increased vascular permeability). hemothorax. blood in the thoracic cavity is called hemothorax, but the term has been used for exudate with a sanguineous component. causes include rupture of a major blood vessel as a result of severe thoracic trauma (e.g., hit by car); erosion of a vascular wall by malignant cells or inflammation (e.g., aortitis caused by spirocerca lupi); ruptured aortic aneurysms; clotting defects, including coagulopathies; warfarin toxicity; disseminated intravascular coagulation (consumption coagulopathy); and thrombocytopenia. hemothorax is generally acute and fatal. on gross examination, the thoracic cavity can be filled with blood, and the lungs are partially or completely atelectatic ( fig. 9-115 ). chylothorax. the accumulation of chyle (lymph rich in triglycerides) in the thoracic cavity ( fig. 9-116 ) is a result of the rupture of major lymph vessels, usually the thoracic duct or the right lymphatic duct. the clinical and pathologic effects of chylothorax are similar to those of the other pleural effusions. causes include thoracic neoplasia (the most common cause in human beings but a distant second to idiopathic cases in dogs), trauma, congenital lymph vessel anomalies, lymphangitis, dirofilariasis, and iatrogenic rupture of the thoracic duct during surgery. the source of the leakage of chyle is rarely found at necropsy. when the leakage of chyle occurs in the abdominal cavity, the condition is referred to as chyloabdomen. cytologic and biochemical examination of fluid collected by thoracocentesis typically reveals large numbers of lymphocytes, lipid droplets, few neutrophils in chronic cases, and high triglyceride content. can be large enough to compromise pulmonary function or mimic neoplasia in thoracic radiographs. these cysts may arise from the thymus (thymic branchial cysts), bronchi (bronchogenic cysts), ectopic thyroid tissue (thyroglossal duct cysts), or from remnants of the branchial pouches, and they are generally lined by epithelium and surrounded by a capsule of stromal tissue. anomalies of the thoracic duct cause some cases of chylothorax. pleural calcification. pleural calcification is commonly found in dogs and less often in cats with chronic uremia. lesions appear as linear white streaks in parietal pleura, mainly over the intercostal muscles of the cranial part of the thoracic cavity. the lesions are not functionally significant but indicate a severe underlying renal problem. vitamin d toxicity (hypervitaminosis d) and ingestion of hypercalcemic substances, such as vitamin d analogs, can also cause calcification of the pleura and other organs. pneumothorax. pneumothorax is the presence of air in the thoracic cavity where there should normally be negative pressure to facilitate inspiration. human beings have a complete and strong mediastinum so that pneumothorax is generally unilateral and thus not a serious problem. in dogs, the barrier varies, but in general it is not complete, so often some communication exists between left and right sides. there are two main forms of pneumothorax. in spontaneous (idiopathic) pneumothorax, air leaking into the pleural cavity from the lungs occurs without any known underlying disease or trauma. in secondary pneumothorax, movement of air into the pleural cavity results from underlying pulmonary or thoracic wall disease. the most common causes of secondary pneumothorax in veterinary medicine are penetrating wounds to the thoracic wall, perforated esophagus, iatrogenic trauma to the thorax and lung during a transthoracic lung biopsy or thoracoscopy, tracheal rupture from improper intubation, and rupture of emphysematous bullae or parasitic pulmonary cysts (paragonimus spp.) that communicate with the thoracic cavity. pneumothorax and pneumomediastinum caused by high air pressure (barotrauma) are also well documented in cats after equipment failure during anesthesia. clinical signs of pneumothorax include respiratory distress, and the lesion is simply a collapsed, atelectatic lung. the air is readily reabsorbed from the cavity if the site of entry is sealed. pleural effusion. pleural effusion is a general term used to describe accumulation of any fluid (transudate, modified transudate, exudate, blood, lymph, or chyle) in the thoracic cavity. cytologic and biochemical evaluations of pleural effusions taken by thoracocentesis are helpful in determining the type of effusion and possible pathogenesis. based on protein concentration and total numbers of nucleated cells, pleural effusions are cytologically divided into transudates, modified transudates, and exudates. hydrothorax. when the fluid is serous, clear, and odorless and fails to coagulate when exposed to air, the condition is referred to as hydrothorax (transudate). causes of hydrothorax are the same as those involved in edema formation in other organs: increased hydrostatic pressure (heart failure), decreased oncotic pressure (hypoproteinemia, as in liver disease), alterations in vascular permeability (inflammation), or obstruction of lymph drainage (neoplasia). in cases in which the leakage is corrected, if the fluid is a transudate, it is rapidly reabsorbed. if the fluid persists, it irritates the pleura and causes mesothelial hyperplasia and fibrosis, which thickens the pleura. from a perforated esophagus. chronic injury typically results in serosal fibrosis and tight adhesions between visceral and parietal pleurae (see fig. 9 -71). when extensive, these adhesions can obliterate the pleural space. pleuritis or pleurisy. inflammation of the visceral or parietal pleurae is called pleuritis, and according to the type of exudate, it can be fibrinous, suppurative, granulomatous, hemorrhagic, or a combination of exudates. acute fibrinous pleuritis can progress with time to pleural fibrosis ( fig. 9-117 ). when suppurative pleuritis results in accumulation of purulent exudate in the cavity, the lesion is called pyothorax or thoracic empyema ( fig. 9-118) . clinically, pleuritis causes considerable pain, and in addition, empyema can result in severe toxemia. pleural fibrous adhesions (between parietal and visceral pleura) and fibrosis are the most common sequelae of chronic pleuritis and can significantly interfere with inflation of the lungs. pleuritis can occur as an extension of pneumonia, particularly in fibrinous bronchopneumonias (pleuropneumonia), or it can occur alone, without pulmonary involvement ( fig. 9-119 ). bovine and ovine pneumonic mannheimiosis and porcine and bovine pleuropneumonia are good examples of pleuritis associated with fibrinous bronchopneumonias. polyserositis in pigs and pleural empyema, particularly in cats and horses, are examples of pleural inflammation in pleural tissue is readily susceptible to injury caused by direct implantation of an organism through a penetrating thoracic or diaphragmatic wound; by hematogenous dissemination of infectious organisms in septicemias; or by direct extension from an adjacent inflammatory process, such as in fibrinous bronchopneumonia or in contrast to those with the effusive ("wet") form, in which thoracic involvement is primarily that of a pleural effusion. cytologic evaluation of the effusion typically shows a low to moderate cellularity with degenerated leukocytes, lymphocytes, macrophages, and mesothelial cells, and a pink granular background as a result of the high protein content. pleuritis is also an important problem in horses. nocardia spp. can cause fibrinopurulent pneumonia and pyothorax with characteristic sulfur granules. although mycoplasma felis can be isolated from the respiratory tract of normal horses, it is also isolated from horses with pleuritis and pleural effusion, particularly during the early stages of infection. the portal of entry of this infection is presumably aerogenous, first to the lung and subsequently to the pleura. the pleural surface of the lung is often involved in neoplasms that have metastasized from other organs to the pulmonary parenchyma and ruptured the visceral pleura to seed the pleural cavity. mesothelioma is the only primary neoplasm of the pleura. which involvement of the lungs may not accompany the pleuritis. pleural inflammation is most frequently caused by bacteria, which cause polyserositis reaching the pleura hematogenously. these bacteria include haemophilus parasuis (glasser's disease) (see , streptococcus suis, and some strains of pasteurella multocida in pigs; streptococcus equi ssp. equi and streptococcus equi ssp. zooepidemicus in horses; escherichia coli in calves; and mycoplasma spp. and haemophilus spp. in sheep and goats. contamination of pleural surfaces can be the result of extension of a septic process (e.g., puncture wounds of the thoracic wall and, in cattle, traumatic reticulopericarditis) and ruptured pulmonary abscesses (e.g., trueperella pyogenes). in dogs and cats, bacteria (e.g., nocardia, actinomyces, and bacteroides) can cause pyogranulomatous pleuritis, characterized by accumulation of blood-stained pus ("tomato soup") in the thoracic cavity. this exudate usually contains yellowish flecks called sulfur granules ( fig. 9-120 ), although these are less common in nocardial empyema in cats. many species of bacteria, such as escherichia coli, trueperella pyogenes, pasteurella multocida, and fusobacterium necrophorum, can be present in pyothorax of dogs and cats. these bacteria occur alone or in mixed infections. the pathogenesis of pleural empyema in cats is still debatable, but bite wounds or penetration of foreign material (migrating grass awns) are likely. pyogranulomatous pleuritis with empyema occurs occasionally in dogs, presumably associated with inhaled small plant material and penetrating (migrating) grass awns. because of their physical shape (barbed) and assisted by the respiratory movement, aspirated grass awns can penetrate airways, move through the pulmonary parenchyma, and eventually perforate the visceral pleura causing pyogranulomatous pleuritis. cats with the noneffusive ("dry") form of feline infectious peritonitis (fip) frequently have focal pyogranulomatous pleuritis, mesothelioma is a rare neoplasm of the thoracic, pericardial, and peritoneal mesothelium of human beings that is seen most commonly in calves, in which it can be congenital. in human beings, it has long been associated with inhalation of certain types of asbestos fibers (asbestos mining and ship building) alone or with cigarette smoking as a probable cocarcinogen; no convincing association between the incidence of mesothelioma and exposure to asbestos has been made in domestic animals. in animals, there may be pleural effusion with resulting respiratory distress, cough, and weight loss. mesothelioma initially causes a thoracic effusion, but cytologic diagnosis can be difficult because of the morphologic resemblance of malignant and reactive mesothelial cells. during inflammation, mesothelial cells become reactive and not only increase in number but also become pleomorphic and form multinucleated cells that may be cytologically mistaken for those of a carcinoma. grossly, mesothelioma appears as multiple, discrete nodules or arborescent, spreading growths on the pleural surface ( fig. 9-121) . microscopically, either the mesothelial covering cells or the supporting tissue can be the predominant malignant component, so the neoplasm can microscopically resemble a carcinoma or a sarcoma. figure 9 -120 nocardiosis. a, chronic pleuritis (nocardia asteroides), pleural cavity, cat. the pleural cavity is covered with abundant red-brown ("tomato soup") exudate" (syringe). once considered to be pathognomonic of nocardia spp. infection, it is no longer regarded as being diagnostic of nocardiosis. the fluid contains abundant protein, erythrocytes, granulomatous inflammatory cells, and sulfur granules. b, chronic pleuritis (nocardia asteroides), visceral pleura, dog. the thickened pleura has a granular pink-gray appearance because of granulomatous inflammation and the proliferation of fibrovascular tissue of the pleura. c, chronic pleuritis (nocardia asteroides), dog. the pleura has been thrown up into villous-like projections composed of abundant fibrovascular tissue and granulomatous inflammation. leakage from the neocapillaries of the fibrovascular tissue is responsible for the hemorrhagic appearance of the pleural exudate. h&e stain. d, chronic pleuritis (nocardia asteroides), thoracic cage, parietal pleura, cat. large pieces of exudate, which contain yellow sulfur granules, are present on the thickened pleura. although considered malignant, mesotheliomas rarely metastasize to distant organs. secondary neoplasms of the pleura. secondary tumors may also spread into the visceral and parietal pleura. thymomas are rare neoplasms that grow in the cranial mediastinum of adult or aged dogs, cats, pigs, cattle, and sheep. thymomas are composed of thymic epithelium and lymphocytes (see chapter 13). old age, both in human beings and in animals, is known to be a risk factor for pulmonary infections, but the precise mechanisms involved in this increased susceptibility are still under investigation. some studies have shown that in aged individuals the antibacterial properties provided by surfactant proteins, proinflammatory cytokines, and complement are altered. pulmonary hyperinflation (often referred to as senile emphysema) has been reported as an age-related change in human and canine lungs. other age-related changes described in canine lungs include mineralization of bronchial cartilage, pleural and alveolar fibrosis, and heterotopic bone formation (so-called "pulmonary osteomas"). we thank all pathologists at the atlantic veterinary college, university of prince edward island for providing case material. suggested readings are available at www.expertconsult.com. lung section showing a distended and partially occluded blood vessel (center of figure) containing large granular cells. these large cells are macrophages, and their cytoplasm is filled with myriad merozoites isolation of porcine circoviruslike viruses from pigs with a wasting disease in the usa and europe exercise-induced pulmonary hemorrhage effect of mucociliary transport relies on efficient regulation of ciliary beating epidemiology, diagnosis, and treatment of blastomycosis in dogs and cats canine h3n8 influenza virus infection in dogs and mice failure of respiratory defenses in the pathogenesis of bacterial pneumonia in cattle the respiratory system advances in diagnosis of respiratory diseases of small ruminants canine nasal disease transmission of equine influenza virus to dogs dear jd: bacterial pneumonia in dogs and cats acute respiratory distress syndrome in dogs and cats: a review of clinical findings and pathophysiology inflammatory response to infectious pulmonary injury laryngeal paralysis: a study of 375 cases in a mixed-breed population of horses stem cells of the respiratory tract exudative pleural disease in small animals bovine respiratory disease research pulmonary thromboembolism coccidioidomycosis in dogs and cats: a review cousens c: pathology and pathogenesis of ovine pulmonary adenocarcinoma prognosis factors for survival in cats after removal of a primary lung tumor: 21 cases (1979-1994) the acute respiratory distress syndrome: from mechanism to translation endogenous lipid pneumonia in cats: 24 cases (1985-1998) retroviral infections in sheep and goats: small ruminant lentiviruses and host interaction canine and feline nasal neoplasia the acute respiratory distress syndrome equine respiratory medicine and surgery canine pleural and mediastinal effusions: a retrospective study of 81 cases a review of histiocytic diseases of dogs and cats estimation of nasal shedding and seroprevalence of organisms known to be associated with bovine respiratory disease in australian live export cattle polymicrobial respiratory disease in pigs current state of knowledge on porcine circovirus type 2-associated lesions common and emerging infectious diseases in the animal shelter chronic rhinitis in the cat advances in the understanding of pathogenesis, and diagnosis and therapeutics of feline allergic asthma mannheimia haemolytica and bovine respiratory disease detection of respiratory viruses and bordetella bronchiseptica in dogs with acute respiratory tract infections current perspectives on the diagnosis and epidemiology of mycoplasma hyopneumoniae infection mannheimia haemolytica: bacterialhost interactions in bovine pneumonia acute lung injury review rhodococcus equi: the many facets of a pathogenic actinomycete tumors of the respiratory system key: cord-004879-pgyzluwp authors: nan title: programmed cell death date: 1994 journal: experientia doi: 10.1007/bf02033112 sha: doc_id: 4879 cord_uid: pgyzluwp nan it is widely held that all developmental cell death is of a single type (apoptosis) and that neuronal death is primarily for adjusting the number of neurons in a population to the size of their target field through competition between equals for target-derived factors. we shall draw on our research and on that of others to criticize these views and replace them by the following. at least three types of neuronal death occur, only one of which resembles apoptosis; a neuron can choose between several self-destruct mechanisms depending on the cause of its death. the purpose of the death is to regulate connectivity, not neuron number. competitors for trophic factors are unequal, and many losers have made axonal targeting errors. a neuron's survival and differentiation depend on multiple anterograde and retrograde signals. activity affects retrograde signals and some but not all anterograde ones. the pattern of activity is more important than the overall amount. in rodents, the period of naturally occuring cell death of motoneurons is followed by a period of supersensitivity to axonal injury. thus, in newborn rodents lesion of the facial nerve leads to a rapid degeneration of the injured motoneurons. we have tested whether overexpression, in rive, of the bcl-2 proto-oncogene was capable of preventing death of axotomized motoneurons. to address this question we used transgenic mice whose motoneurons overexpress the bcl-2 protein. one of the two facial nerves of newborn mice was transected on the 2nd-3rd post-natal day. seven days after the lesion, the morphology of the facial nuclei was analyzed. in control mice, and when compared to the intact nucleus, 70 to 80 % of axotomized motoneurons had disappeared. in contrast, in the transgenic animals, the number of motoneurons on the lesioned side remained unchanged when compared to the eontralateral nucleus. furthermore, their axons remained visible up to the distal lesion site. these experiments show that, in rive, motoneurons overexpressing the bcl-2 protein survive after axotomy, and suggest that, in rive, bcl-2 protect neurons from experimentally induced cell death and could be a target for treatment of motoneurons degenerative diseases. messmer s., mattenberger l., sager y., blatter-garin m-c., pometta d., kate a., james r.w. drpt de mrdeeine, drpt. de pharmacologie, div. de neurophysiologie clinique, facult6 de mrdecine, gen~ve. clusterin is a widely expressed glycoprotein, highly conserved across species. numerous functions have been postulated for this protein. the most important are roles in lipid transport, as elusterin is associated with apolipoprotein ai in hdl, complement regulation and tissue remodelling, in particular during cell death and differentiation. using cultures of rat spinal cord neurones (90% neurons and 5-10% non-neuronal cells), we have studied the expression of clusterin and ape e in glutamate-induced neuronal cell death to examine potential roles in lipid management. up-regulation of the two proteins was observed. clusterin and ape e appear in the conditioned medium respectively 15h and 7.5h after incubation with glutamate. control studies, in the presence of a noncompetitive nmda receptor agonist showed the secretion of clusterin and ape e to be diminished by >60%. no up-regulation of either protein was observed in complementary studies with exclusively non-neuronal cell cultures. the cellular origin of the 2 secreted proteins is presently under investigation. programmed cell death and tissue remodelling are consequences of hormonally induced restructuring of the rat ventral prostate after castration and the rat mammary gland after weaning. we used the "differential display"-method (liang and pardee, 1992, science 257:967) to detect and isolate edna fragments whose corresponding rnas are regulated either coincidentally, or in an organ specific fashion during mammary gland involution and postcastrational prostate regression. partial sequencing of 12 clones revealed high, but not absolute homology of 5 fragments with sequences, previously characterized in different biological contexts. these five encode functions which could be anticipated to be important for cell growth and/or programmed cell death, we are presently investigating the functions of several of these transcripts in cell culture and in rive. antisense oligos are being employed in vivo to determine whether these genes contribute to the phenotype of programmed cell death. b epitopes derived from the envelope gp52 glycoprotein (ep3) or from the viral superantigen of mmtv have been incorporated into inert or live vaccines. the inert vaccine consists of purified chimeric proteins which contain the b epitopes alone or fused to multimeric promiscuous t helper epitopes from tetanus toxin. mice were immunized subcutaneously with these chimeric proteins. the live vaccine consists of an avirulent strain of salmonella typhimurium which expresses the mmtv epitopes in the form of chimeric proteins fused to the nucleocapsid protein of hepatitis b virus. this vaccine is given to mice in one oral dose. the level, duration and isotype of the immune response generated by each vaccine have been measured and compared. the level of protection has been investigated by systemically challenging immunized mice with the relzovims. a reduced binding of oxytocin (ot) occurs with aging in some, but not all, areas of the rat brain (arsenijevic et al., experientia 1993, 49, a75) . the candate putamen showed the most impressive loss of ot receptors. two other regions, the hypothalamic ventromedial nucleus (vmh) and the islands of caueja (icj) had also an important deficit of ot binding sites. on the other hand, these two regions were known to be sensitive to sex steroids. in the present work, we treated from 20 month old rats during one month with testosterone propionate (2 #g/kg s.c., once every 3 days) dissolved in oil. three rats of the same age injected with oil only served as controls. we labelled ot receptors throughout the brain of old rats using a 125i-labelled ligand specific for ot receptors. analysis of autoradiograms by an image analyzer revealed that the testosterone treatment increased ot binding sites in the vmh, in the icj, and, to a lesser extent, in the bed nucleus of the stria terminalis, a region also sensitive to sex steroids, by contrast, in the caudate putamen, the disappearance of ot receptors was not compensated. in conclusion, the decrease of ot receptors occurring in vmh and icj with aging can be reversed by administration of gonadal steroids. in contrast, the loss of ot receptors in the striatum appears to depend on another mecanism. vasopressin (avp) receptors are expressed transiently in the facial nucleus during development (tribollet et el., 1991, dev. brain res., 58, 13-24) . avp may therefore play a role in the maturation of neuromuscular connexions in the neonate rat, and possibly in the restanration of these connexions after nerve lesion in the adult. in order to investigate the latter proposition, we have sectionned the facial nerve in adult rats and used quantitative autoradiography to look at avp binding sites in the facial nucleus at various postoperative times. we observed a massive and transient increase of avp binding sites on the operated side. the number of facial avp binding sites reaches a maximum about one week after nerve section, remains stable during 2-3 weeks, then begin to decrease towards control level. the induction of avp receptors is markedly delayed if the proximal stump of the nerve is ligated. to assess whether other motor nuclei would also react to axotomy by up-regulating the expression of avp receptors, we have sectionned the hypoglossal nerve and the sciatic nerve. in both cases, the binding of avp receptor ligand increases massively in the respective motor nuclei, with a time-course similar to that found in the facial nucleus. altogether, our data suggest that central avp could be involved in the process of nerve regeneration. cytotoxic t-cell mediated apoptosis schaerer,e, karapetian,o.,adrian,m. and tschopp,j. inst.de biochimie, univ.de lausanne, 1066 epalinges. an apoptotic cell death mechanism is used by cytolytic t cells (ctl) to lyse appropriate target cells. ctl harbor cytoplasmic storage compartments, containing the lytic protein perforin and serineproteases (granzymes), whose content is released upon target cell interaction. we show that these granules are multivesieular bodies and that degranulation releases these intragranular vesicles (igv) having granzymes, t-cell receptor and yet undefined proteins associated. isolated igvs and perforin induce dna breakdown in target cells within 20 minutes. microscopic analysis demonstrates that igv specifically interact with target cell via the t-cell receptor and that their contents is taken up by the target cell. already 15 min. after interaction, 3 distinct igv proteins are found in the nucleus of the target cell.one of the molecules has been identified to be granzyme a, previously reported to be involved in apoptosis. we propose that lymphocytes transfer apoptosisinducing proteins to the nucleus of the target cells using vesicles as vehicles for delivery. cytotoxic t cells kill their targets by a mechanism involving membranolysis and dna degradation (apoptosis). recently, two sets of proteins have been proposed as dna breakdown-inducing molecules in t cells: granzyme a, b and tia-i. in this study, we cloned and further characterized the tia-i mouse homologue. aa sequence comparison with the human tia-1 showed an overall identity of 93%. devoid of a signal peptide, tia is yet localized to cytotoxic granules, probably targeted via a gly-tyr-motif. as tia-i, its mouse homolcgue contains three rnabinding domains. expression of tia during development shows a very strong signal in the brain and weaker signals in thymus, heart and other organs. during embryonic development several structures that contribute to organogenesis form transiently and are later eliminated by apoptosis. this pattern of tia expression could indicate its involvement in apoptosis. prostate involution occurs after castration in rats and is associated with the death by apoptosis of a large fraction of the epithelial cells. we have isolated several genes from a prostate involution bacteriophage lambda library using differential screening methods. among these clones, one d~monstrated an especially strong signal when used as a probe against northern blots of prostate mlhna obtained before, and at different times after castration. this gene is down-regulated after castration by 40-fold within 5 days. intramuscular injection of a testosterone depot resulted in complete restoration of expression within 24 hours. upon sequencing it became apparent that this clone has a high degree of homology to a known ndah dehydrogenase encoded in mitochondrial dna. the clone failed to hybridize to any transcripts from rat organs other than prostate. we are now in the process of isolating the htm~n hc~olog to this gene for use as a biomarker in study of benign hyperplasia and developing carcinoma. this gene is a possible indicator for testosterone-independent cell populations or of cells lacking ftl~ctional testosterone receptor. during the first three postnatal weeks the rat lung undergoes the last two developmental stages, the phase of alveolarization and the phase of microvascular maturation. the latter involves a decrease of the connective tissue mass in the alveolar septa and a merging of the two capillary layers to a single one. speculating that programmed cell death may play a role during this remodeling, we searched for the presence of apoptotie cells in rat lungs between days 10 and 24. lung paraffin sections were treated with y-terminal transferase, digoxigenin-dutp, and anti-digoxigeninfluorescein-f(ab)-fragments, and the number of fluorescent nuclei was compared between sections at different days. while the number of apoptotie ceils was low until the end of the second week and at day 24, we observed an about eight fold increase of fluorescent nuclei towards the end of the third week. we conclude that programmed cell death is involved in the structural maturation of the lung. brunner, a., wallrapp, ch., pollack, i, twardzik, t. and schneuwly, s. lehrstuhl genetik, biozentrum universit~t w~rzburg, mutants in the giant lens (g/l) gene show a strong disturbance in ommatidial development. in the absence of any gene product, additional phetoreceptors, cone cells and pigment cells develop. opposite effects can be seen in flies in which the gene product of the giant lens gene can be ectopically expressed by heat shock. a second very typical phenotype is the disturbance of photoreceptor axon guidance. molecular analysis of gil shows that it encodes a secreted protein of 444aa containing three evolutionary conserved cystein-motives very similar to egf-like repeats. we propose that gil functions as a secreted signal, most likely a lateral inhibitor for the development of specific cell fates and that gil, either directly or indirectly, is involved in targeting photoreceptor axons into the brain. the decrease in cellularity during scar establishment is mediated through apoptosis desmouliere, a., redard, m., darby, i., and g. gabbiani department of pathology, cmu, 1 rue michel server, 1211 gen~ve 4 dudng the healing of an open wound, granulation tissue formation is characterized by replication and accumulation of fibroblastic cells, many of which acquire morphological and biochemical features of smooth muscle cells and have been named myofibroblasts (sch0rch et el., histology for pathologists, t992). as the wound evolves into a scar, there is an important decrease in ceuuladty, including disappearance of myofibroblasts. the question adses as to which process is responsible for myofibroblast disappearance. during a previous investigation on the expression of (z-smooth muscle actin in myofibroblasts, we have obsewed that in late phases of wound healing, many of myofibroblasts show signs of apoptosis end suggested that this type of cell death is responsible for the disappearance of myofibroblasts (darby et al., lab. invest. 63:21, 1990) . we have tested this hypothesis by means of electron microscopy and morphometry and by in situ end-labeling of fragmented dna (wijsman et al., j. histochem. cytochem. 41:7, t 993) . our results show that the number of apoptotic cells increases as the wound closes and suggest that this may be the mechanism for the disappearance of myofibroblasts as well as for the evolution of granulation tissue into a scar. (supported by the swiss national science foundation, grant n~ s01-16 r. jaggl, a. marti and b. jehn. universit~t bern, akef, tiefenaustr. 120, 3004 bern at weaning the mammary gland undergoes a reductive remodelling process (involution) which is associated with the cessation of milk protein gene expression and apoptosis of milk-produclng epithelial cells. this process can be reversed by returning the pups to the mother within 1 day. elevated nuclear protein kinase a (pka) activity was observed from one day post-lactation, paralleled by increased c-los, junb, ]und and to a lesser extent c-]un mrna levels. ap-1 dna binding activity was transiently induced and the ap-1 complex was shown to consist principally of cfos/jund. oct-1 dna binding activity and oct-1 protein were gradually lost from the gland over the first four days of involution, whereas oct-1 m_rna levels remained unchanged. comparing nuclear extracts from normal mammary glands with nuclear extracts from glands which had been cleared of all epithelial cells three weeks after birth revealed that pka activation, ap-1 induction and oct-1 inactivation are all dependent on the presence of the epithelial compartment. the increased fos/jtm expression and the inactivation of oct-1 may be consequences of the increased pka activity. when involution is reversed, both, pica activity and ap-1 dna binding activity (and fos andjun mrna levels) are reduced to basal levels. our data suggests a role for pka and ap-1 on progranlmed cell death of manlnmry epithelial ceils. bcl-2~ does not require membrane attachment for its survival activity c. borner*, i. martinout, c. mattmann*, m. irmler*, e. sch&rrer*, j.-c. martinou-j-, and j. tschopp*. * institute of biochemistry, university of lausanne, 1066 epalinges, 1 institute of molecular biology, glaxo inc.,1228 plan los ouates. 8cl-2(z is a mitochondrial or perinuclear-associated oncoprotein that prolongs the life span of a variety of cell types by interfering with programmed cell death. how it exerts this activity is unknown but it is believed that membrane attachment is required. to identify critical regions in bcl-2o~ for subcellular localization and survival activity, we created by site-directed mutagenesis, various mutations in regions which are most conserved between the different bcl-2 species. we show here that membrane attachment is not required for the survival activity of bcl-2o< a truncation mutant of bcl-2(z lacking the last 33 amino acids (t3) including the hydrophobic domain is soluble, yet fully active in blocking apoptosis of sympathetic neurons induced by ngf deprivation or l929 fibroblasts induced by tnfc~ treatment. we further provide evidence for a putative functional region in bcl-2 which lies in the conserved domains 4 and 5 upstream of the hydrophobic cooh terminal tail. the breakdown of nuclear dna is considered to be a hallmark of apoptosis. we previously identified the perinuclear membrane localized dnase i as the endonuclease involved in the formation of oligonucleosomal-sized fragments (dna ladder). it is not clear how the nuclease is activated and has access to the dna. we show that in thymocytes induced to undergo apoptosis, lamin breakdown preceded dna laddering. by transfeeting hela cells with a constitutively active cdc2 mutant, nuclear envelope breakdown and typical apoptotic features (ehromatin condensation) were observed. moreover, co-transfection with cdc2 mutant and dnase i led to dna degradation. we propose that apoptosis can be induced by wrongly timed and hence abortive mitosis leading to uncontrolled nuclear membrane disintegration. s02-01 s02-04 platelet-derived growth factor (pdgf) is thought to play an active role in fibrosing diseases. bronchiolitis obliterans-organizing pneumonia (boop) is a condition characterized by intraluminal proliferation of connective tissue inside distal air spaces. to evaluate pdgf expression in boop we performed immunohistoehemistry on lung biopsies from 20 patients and 10 controls free of fibrosis. sedal sections were stained with an antibody against either pdgf or the monoeyte/macrophage marker cd68, in both groups the pdgf ~9 cells were essentially tissue macrophages. using point counting to measure volume fraction (vv) , pdgf-pesitive cells represented 4.65+1.63% (mean+sd) of the volume occupied by lung tissue in the boop cases, and 2,12+0.65% in the controls (!0<0,001). similarily, 10.73+4.69% of the lung tissue was occupied by cd68 e~ macrophages in the boop cases, compared to 5.37:~3.73% in the controls (p