Domiciliary Cockroaches as ...(CLEAN Copy) J Arthropod-Borne Dis, June 2018, 12(2): 141–151 AA Adenusi et al.: Domiciliary Cockroaches … 141 http://jad.tums.ac.ir Published Online: June 12, 2018 Original Article Domiciliary Cockroaches as Carriers of Human Intestinal Parasites in Lagos Metropolis, Southwest Nigeria: Implications for Public Health *Adedotun A Adenusi 1, Mary I Akinyemi 2, Dele Akinsanya 3 1Medical Parasitology Unit, Department of Medical Microbiology and Parasitology, College of Medicine, University of Lagos, Idi-Araba, Surulere, Lagos, Nigeria 2Statistics Unit, Department of Mathematics, University of Lagos, Akoka, Lagos, Nigeria 3Department of Zoology, University of Lagos, Akoka, Lagos, Nigeria (Received 7 July 2016; accepted 12 May 2018) Abstract Background: Domiciliary cockroaches are obnoxious pests of significant medical importance. We investigated the prevalence of human intestinal parasites in cockroaches and its attendant public health importance. Methods: Overall, 749 cockroaches (Periplaneta americana, 509, Blattella germanica, 240) caught by trapping from 120 households comprising 3 different housing types in Somolu, Lagos metropolis, southwest Nigeria, in 2015 were screened for human intestinal parasites using standard parasitological techniques. Results: The prevalence of human intestinal parasites in cockroaches was 96.4%. There was no statistically signifi- cant difference (P> 0.05) in parasite prevalences between P. americana (95.7%) and B. germanica (97.9%). Parasite species identified and their prevalence were as follows: Entamoeba histolytica/dispar (44.1%), E. coli (37.8%), Gi- ardia lamblia (18.7%), Cryptosporidium sp. (13.8%), Ascaris lumbricoides (61.3%), Trichuris trichiura (55.8%), hookworms (11.6%), Strongyloides stercoralis (11.7%), Taenia/Echinococcus spp. (10.5%), Enterobius vermicularis (17.2%) and Hymenolepis nana (11.6%). Parasite prevalence and burdens varied with housing type; the prevalence was significantly higher statistically (P< 0.05) in cockroaches from low-cost bungalow, LCB (100%) and low-cost, 2-storey, LC2-S (100%) houses than in medium-cost flats, MCF (81.3%). Parasite burdens were also significantly higher statistically (P< 0.05) in cockroaches from LCB or LC2-S than in cockroaches from MCF. Parasite preva- lences between cockroach gut and body surfaces were not statistically significant (P> 0.05) but mean parasite bur- dens in gut were significantly higher statistically (P< 0.05) than on body surfaces. Conclusion: Cockroaches types carry transmissive stages of human intestinal parasites and may act as reservoirs and potential mechanical vectors for disease transmission. Keywords: Cockroaches, Periplaneta americana, Blattella germanica, Intestinal parasites, Lagos Introduction Cockroaches (Insecta: Blattaria) are insects, which have been in existence since antiquity (1), thriving in so many habitats and con- suming virtually any organic matter, includ- ing fresh and processed human foods, stored products, garbage, and sewage (1, 2). About 4600 described species of cockroaches are distributed worldwide (3). However, only a few of the about 30 synanthropic species are con- sidered as pests in homes, grocery stores, hos- pitals, offices, schools, warehouses and other establishments (4). The American cockroach, Periplaneta americana (Blattaria: Blattidae) and the German cockroach, Blattella german- ica (Blattaria: Blattellidae) are considered two of the most common and notorious cosmo- politan pest species in Nigeria (5) and glob- ally (6-8). Cockroaches are pests of significant med- ical, veterinary and public health importance. Their presence and sight may induce psycho- logical stress, the levels of which tend to be proportional to cockroach size and number (2). They are an important source of potent envi- *Corresponding author: Dr Adedotun A. Adenusi, E-mail: aaadenusi@yahoo.com http://jad.tums.ac.ir/ J Arthropod-Borne Dis, June 2018, 12(2): 141–151 AA Adenusi et al.: Domiciliary Cockroaches … 142 http://jad.tums.ac.ir Published Online: June 12, 2018 ronmental aeroallergens, which provoke al- lergic reactions and exacerbate acute asthma, especially in predisposed atopic individuals (9, 10). Cockroaches contaminate foods to which they have access with their feces and foul-smelling secretions, thereby making them offensive and unsafe for human consumption (1, 2). They also serve as intermediate hosts to a number of helminth parasites of veteri- nary importance, some of which cause debil- itating diseases in domestic animals (2). Although cockroaches have yet, to be in- criminated as biological vectors of human pathogens, their biology - filthy habits, indis- criminate diet, feeding mechanisms and mor- phology, make them vulnerable and suitable, at least, to acquire, mechanically transport and disseminate pathogens. Indeed, a variety of pathogenic and potentially pathogenic bacte- ria, fungi, and parasites have been isolated from body surfaces and/or gut of cockroach- es in domestic, food-handling, and hospital environments (6, 11-14). The potential exists, therefore, for mechanical transmission through physical dislodgement, regurgitation, or fecal pellet deposition onto and/or into exposed hu- man food, which may be, ready-to-eat or im- properly cooked. Although the direct involve- ment of cockroaches in the transmission of parasites to humans remains to be fully estab- lished, their importance in parasite transport and dissemination cannot be underestimated. Intestinal parasitoses are among the most common and widespread diseases of humans globally responsible for considerable morbid- ity and mortality, especially in children, the most vulnerable population (15). They remain a serious threat to public health worldwide, par- ticularly in communities in resource-poor de- veloping countries in the tropics and subtrop- ics where high prevalences are attributable to poverty, poor living conditions, lack of pota- ble water supply, inadequate waste disposal, poor sanitation and environmental hygiene (16). While a few of these parasites require intermediate hosts, many are transmitted by di- rect ingestion of infective cysts, and oocysts (protozoa) or eggs and/or larvae (helminths) in foods (especially fruits and vegetables), water, soil, pica, or on hands so contaminated. The incidence of human intestinal parasi- toses has continued to increase in recent years, in spite of concerted efforts at reduction. More- over, the transmissive/human-infective stages of some of these parasites can survive in the environment for considerable lengths of time. Because cockroaches carry the same patho- gens found in substrates with which they have contact (17), it is plausible that cockroaches, in environments contaminated with parasite cysts, oocysts, eggs and or larvae, may pick up these stages for transport and dissemination. Poor household hygiene and inadequate environmental sanitation provide congenial at- mosphere for cockroach infestation. Somolu, Lagos metropolis, southwest Nigeria, typifies a cosmopolitan setting in a developing econ- omy such as Nigeria, where poor sanitary con- ditions, together with ecology and demogra- phy, provide congenial atmosphere for cock- roach infestation and contact with pathogens. In spite of the above, and the heterogeneity of Somolu in terms of human population and physical infrastructures, and considering the medical and public health importance of cock- roaches, there is yet, no information on prev- alence of human intestinal parasites in domi- ciliary cockroaches from this locality. The objective of this study was to deter- mine and compare prevalences and species composition of human intestinal parasites in cockroaches from different residential build- ings in Somolu, Lagos State, southwest Nigeria. Materials and Methods Study Area The study was carried out between Aug and Nov 2015 in Somolu (geographical co- ordinates, 6°32' N and longitude 3°22' E), a densely populated cosmopolitan area of La- gos metropolis, and headquarters of Somolu http://jad.tums.ac.ir/ J Arthropod-Borne Dis, June 2018, 12(2): 141–151 AA Adenusi et al.: Domiciliary Cockroaches … 143 http://jad.tums.ac.ir Published Online: June 12, 2018 Local Government Area (LGA) of Lagos State, southwest Nigeria. The LGA which has a land size of 11615km2 and a population of 403569 (18) is inhabited predominantly by people of the Yoruba extraction, although all tribes and sub-tribes of the Nigerian nationality and ex- patriates are also resident. Climate in the area is typical of that in the State and is characterized generally by daily temperatures of 24–34 °C and monthly rela- tive humidity of 64–93% during the rainy season, usually from Apr to Oct, and 34– 49% during the dry season from Nov to Mar. Housing Types Houses in Somolu are typical, a mix of old and modern architecture. One hundred and twenty residential buildings were select- ed for the study using a stratified random sam- pling procedure. They comprised 40 each, of buildings classified as low-cost bungalow (LCB), low-cost, 2-storey (LC2-S), and me- dium-cost flat (MCF), based on building ar- chitecture and socio-economic status of resi- dents. Each LCB or LC2-S had between 5 and 7 rooms on either side of a story and each room was occupied by low-income class in- dividual(s)/family who shared the only kitch- en and toilet/bathroom facilities on either side of a story. Each MCF consists of a 3-bed- room apartment with a kitchen and at least one toilet facility, in a semi-detached build- ing inhabited by a medium-income class fam- ily. Inclusion criterion was that no insecticide and/ or trapping device was used to treat cock- roach infestation in the one week prior to the commencement of the study. Advocacy visits were made to residents of selected houses to explain the objective(s) of the study and to seek for their participation, cooperation, and understanding in the execution of the study. Cockroach collection and identification Cockroaches were trapped live, using ster- ile jars baited with pieces of bread soaked in a small amount of beer. The jars, whose in- side upper portions were coated with a thin film of petroleum jelly (Vaseline®) to prevent cockroach escape, were placed indoors at 19:00h and retrieved at 07:00h the next morn- ing, for 1–3 consecutive days. Cockroaches were transported in the jars to the laboratory where they were anaesthetized and killed by exposure to chloroform fume. They were ex- amined under a dissecting microscope and identified to the lowest taxon possible, using standard taxonomic keys (19). They cock- roaches were counted and sorted by capture site (housing type), and the appropriate taxon. Isolation of parasites from cockroach body surface In order to dislodge parasite stages (cysts, oocysts, eggs and/or larvae) from body sur- faces, cockroaches were washed individually by submersion in 5–10ml sterile physiologi- cal saline and vortexing at low speed for 2 min. Cockroaches were removed from wash solutions using sterile forceps, fixed in 70% alcohol for 5min and air-dried at room tem- perature. Wash solutions were centrifuged at 2000g for 5min, supernatants were decanted and the bottom 0.5–1ml processed further us- ing the formol-ether concentration technique (20). The resulting sediment mixed with the bottom 0.5ml was placed on slide, stained with Lugol’s iodine and examined microscopical- ly for human intestinal parasite stages. For the demonstration of Cryptosporidium oocysts, a modified Ziehl-Neelsen staining method (21) was used. Briefly, air-dried smears prepared from processed body surface wash- ings were fixed with methanol and stained with carbol-fuchsin for 30min. Smears were washed with tap water, decolorized with 1% acid alcohol for 1min, washed again with tap water and counter-stained with 1% meth- ylene blue for 1min. Smears were rinsed fi- nally in tap water and air-dried. Cockroach specimens which could not be processed immediately were kept in the freez- er at -4 °C. http://jad.tums.ac.ir/ J Arthropod-Borne Dis, June 2018, 12(2): 141–151 AA Adenusi et al.: Domiciliary Cockroaches … 144 http://jad.tums.ac.ir Published Online: June 12, 2018 Isolation of parasites from cockroach gut Following washing in physiological sa- line, fixing in 70% alcohol and subsequent air-drying, each cockroach was placed in a sterile Petri dish and dissected under a dis- secting microscope using sterile entomologi- cal needles. Whole gut was removed and ho- mogenized in 2–5ml physiological saline. The homogenate was filtered through gauze and centrifuged at 2000g for 5min, following which the supernatant was decanted. The bottom 0.5– 1ml was processed further using the formol- ether concentration technique. The resulting sediment mixed with the bottom 0.5ml was placed on slide, stained with Lugol’s iodine and examined microscopically as described above. Cryptosporidium oocysts were identified following the modified Ziehl-Neelsen stain- ing method described above. Parasite Identification Cysts, oocysts, eggs and/or larvae of hu- man intestinal parasites were identified mi- croscopically using bench aids (22) and their numbers recorded. A cockroach was consid- ered a carrier if any parasite stage was detect- ed in preparations from body surface and/or gut contents. Data analysis Data were input into Microsoft Excel and analyzed using the “R: A Language and En- vironment for Statistical Computing” software package (23). Analysis of variance (ANOVA) was used to test for differences in overall prev- alence of parasites between cockroach spe- cies, in overall burdens of parasites on cock- roach body surfaces and in gut, and in over- all burdens of protozoan and helminth groups of parasites. The Tukey’s HSD test was used for multiple comparisons of overall preva- lences or burdens of protozoan and/or hel- minth parasites between pairs of residential building types. All tests were carried out at 95% significance level; in all cases, a P< 0.05 was considered statistically significant. Results Prevalence of human intestinal parasites by cockroach species Overall, 749 cockroaches comprising two species, P. americana (509) and B. germanica (240) were caught and identified. Human in- testinal parasite stages were identified in 96.4% of the cockroaches (Table 1). There was no statistically significant difference (F-statistic= 2.354, P= 0.125) in overall prevalence of par- asites between P. americana (95.7%) and B. germanica (97.9%). Parasites were more fre- quently isolated from cockroaches trapped from LCB and LC2-S households than in cock- roaches from MCF (81.3%) (Table 1). There was no statistically significant difference (P= 1.00) in prevalence of parasites between cock- roaches from LCB (100%) and LC2-S (100%) households while there were statistically sig- nificant differences in prevalences of parasites between cockroaches from LCB and MCF (P=0.001) and LC2-S and MCF (P=0.001). Species diversity of human intestinal par- asites in cockroaches Eleven human intestinal parasites, com- prising four protozoan and seven helminth species were identified on body surfaces and/ or in gut of cockroaches. The species and their respective prevalences in both P. amer- icana and B. germanica are as follows: E. histolytica/dispar (44.1%), E. coli (37.8%), G. lamblia (18.7%), Cryptosporidium sp. (13.8%), A. lumbricoides (61.3%), T. trichiura (55.8%), hookworms (11.6%), S. stercoralis (11.7%), Taenia/Echinococcus spp. (10.5%), E. ver- micularis (17.2%) and H. nana (11.6%). Prev- alences of these parasite species in P. ameri- cana and B. germanica, trapped from differ- ent housing types are shown in Figs. 1 and 2, respectively. The helminths, A. lumbricoides and T. trichiura, and the protozoans, E. his- tolytica/dispar and E. coli were the four most prevalent species in both species of cock- roaches, across all housing types, save B. http://jad.tums.ac.ir/ J Arthropod-Borne Dis, June 2018, 12(2): 141–151 AA Adenusi et al.: Domiciliary Cockroaches … 145 http://jad.tums.ac.ir Published Online: June 12, 2018 germanica from MCF wherein G. lamblia was the fourth most prevalent species (25.0%). Their respective overall prevalences in P. americana were 59.5%, 56.8%, 43.2% and 36.7% (Fig. 1) while the corresponding overall prevalences in B. germanica were 65.0%, 53.8%, 45.8% and 40.0% (Fig. 2). Prevalence and burden of human intestinal parasites on cockroach body surfaces and in the gut Parasite prevalence in cockroach gut was either a little higher than or identical numeri- cally, to the corresponding prevalence on body surface. The ANOVA test showed no statis- tically significant differences between preva- lences in gut and on body surfaces in P. amer- icana (F= 1.363, P= 0.243), B. germanica (F= 0.344, P= 0.558) or both (F= 1.671, P= 0.196). Overall parasite prevalences were signif- icantly higher statistically with helminths than protozoans in P. americana (93.9% vs. 83.7%, F= 28.25, P= 1.31e-07), B. germanica (97.5% vs. 83.3%, F= 29.38, P= 9.46e-08), or both (95.1% vs. 83.6%, F= 54.52, P= 2.54e-13) and in cockroaches from LCB (P= 0.005), LC2-S (P= 3.45e-07) and MCF (P= 0.0001). Mean parasite burdens/counts in P. ameri- cana (Table 2) and B. germanica (Table 3) varied with cockroach body region, parasite group (protozoa or helminth) and housing type. Highest parasite burdens on cockroach body surfaces and in gut were with the protozoans, E. histolytica/dispar and E. coli and the hel- minths, A. lumbricoides and T. trichiura, over- all and in each housing type (Tables 2, 3). Overall mean parasite burdens in gut were significantly higher statistically than on body surfaces in P. americana (F= 330, P< 2e-16), B. germanica (F= 166.3, P< 2e-16), and both (F= 496, P< 2e-16). Similarly, overall burdens of helminth parasites were signifi- cantly higher statistically than those of pro- tozoan parasites in P. americana (F= 156, P< 2e-16), B. germanica (F =74.89, P< 2e-16), both (F= 229.8, P< 2e-16) and in LCB (P= 0.0001), LC2-S (P= 0.0001) and MCF (P= 0.044). Differences in overall parasite bur- dens were statistically significant between LCB and MCF (P= 0.0001) and LC2-S and MCF (P= 0.0001), but not statistically signif- icant between LCB and LC2-S (P= 0.996). Table 1. Prevalence of human intestinal parasite stages in cockroaches Housing Type Number of cockroaches examined (% parasite +ve) Total Periplaneta americana Blattella germanica LCB 207 (100) 91 (100) 298 (100)a LC2-S 202 (100) 105 (100) 307 (100)a MCF 100 (78.0) 44 (88.6) 144 (81.3)b Total 509 (95.7)a 240 (97.9)a 749 (96.4) *Values with same superscript along the same column or row are not signifi- cantly different statistically at α= 0.05 http://jad.tums.ac.ir/ J Arthropod-Borne Dis, June 2018, 12(2): 141–151 AA Adenusi et al.: Domiciliary Cockroaches … 146 http://jad.tums.ac.ir Published Online: June 12, 2018 Fig. 1. Prevalence of human intestinal parasites in Periplaneta americana from different housing types Fig. 2. Prevalence of human intestinal parasites in Blattella germanica from different housing type http://jad.tums.ac.ir/ J Arthropod-Borne Dis, June 2018, 12(2): 141–151 AA Adenusi et al.: Domiciliary Cockroaches … 147 http://jad.tums.ac.ir Published Online: June 12, 2018 Table 2. Mean parasite burdens in Periplaneta americana cockroaches from houses in Somolu, Lagos, Nigeria Parasite species LCB (N=207) LC2-S (N=202) MCF (N=100) Body surface Gut Total Body surface Gut Total Body surface Gut Total Ascaris lumbricoides 2.2±2.1 4.8±4.2 7.0±6.2 2.3±2.0 4.9±4.2 7.2±6.2 0.9±1.2 1.5±2.0 2.3±3.2 Cryptosporidium sp 0.3±0.8 0.6±1.6 0.9±2.3 0.5±1.1 0.9±2.1 1.3±3.1 0.1±0.3 0.2±0.6 0.2±1.0 Entamoeba coli 1.3±1.7 2.9±3.7 4.2±5.4 1.1±1.6 2.3±3.4 3.3±4.9 0.4±0.9 0.9±1.7 1.3±2.6 Entamoeba histolytica/ dispar 1.4±1.9 3.1±3.8 4.5±5.6 1.7±1.9 3.3±3.8 5.0±5.6 0.5±1.0 0.9±1.8 1.3±2.8 Enterobius vermicularis 0.5±1.1 1.0±2.2 1.5±3.3 0.5±1.2 1.0±2.1 1.5±3.3 0.2±0.6 0.3±1.0 0.4±1.6 Giardia lamblia 0.3±0.9 0.7±1.7 1.0±2.6 0.5±1.0 0.9±2.1 1.4±3.1 0.3±0.6 0.5±1.2 0.8±1.8 Hookworms 0.2±0.6 0.4±1.3 0.6±1.9 0.4±1.0 0.7±1.8 1.0±2.7 0.1±0.4 0.2±0.8 0.2±1.1 Hymenolepis nana 0.3±0.8 0.6±1.5 0.8±2.3 0.3±0.8 0.5±1.5 0.8±2.3 0.1±0.3 0.1±0.6 0.2±0.9 Strongyloides stercoralis 0.2±0.5 0.3±1.0 0.5±1.5 0.2±0.6 0.5±1.2 0.7±1.8 0.0±0.2 0.1±0.6 0.2±0.8 Taenia/Echinococcus sp 0.3±0.8 0.6±1.7 0.8±2.4 0.2±0.7 0.5±1.5 0.5±2.1 0.1±0.5 0.3±1.0 0.4±1.5 Trichuris trichiura 1.9±1.9 3.9±3.8 5.8±5.7 2.2±2.0 4.4±3.8 6.7±5.8 0.7±1.2 1.3±2.0 2.1±3.1 Total 8.8±4.1 18.8±7.5 27.6±11.4 9.7±3.8 19.7±7.0 29.3±10.5 3.3±2.6 6.2±4.6 9.4±7.1 Table 3. Mean parasite burdens in Blattella germanica cockroaches from houses in Somolu, Lagos, Nigeria Parasite species LCB (N=91) LC2-S (N=105) MCF (N=44) Body surface Gut Total Body surface Gut Total Body surface Gut Total Ascaris lumbricoides 2.7±2.2 5.7±4.7 8.4±6.9 2.6±2.0 5.6±4.1 8.3±6.0 1.2±1.5 2.1±2.5 3.3±4.0 Cryptosporidium sp 0.2±0.6 0.3±1.1 0.5±1.7 0.4±1.0 0.8±2.1 1.2±3.0 0.2±0.5 0.3±0.9 0.5±1.4 Entamoeba coli 1.6±1.9 3.4±4.0 4.9±5.8 1.0±1.6 2.1±3.2 3.1±4.7 0.8±1.2 1.2±2.0 2.0±3.2 Entamoeba histolytica/ dispar 1.6±1.8 3.4±4.0 5.0±5.8 1.7±1.8 3.4±3.7 5.0±5.4 0.5±1.0 0.7±1.5 1.2±2.5 Enterobius vermicularis 0.5±1.0 1.0±2.3 1.5±3.3 0.6±1.3 1.1±2.3 1.8±3.5 0.1±0.5 0.2±0.8 0.3±1.2 Giardia lamblia 0.7±1.3 1.4±2.7 2.2±4.0 0.4±1.1 0.9±2.4 1.4±3.5 0.5±0.9 0.8±1.4 1.2±2.2 Hookworms 0.3±0.9 0.5±1.9 0.8±2.8 0.4±1.0 0.9±2.0 1.3±3.0 0.1±0.5 0.2±0.8 0.3±1.2 Hymenolepis nana 0.2±0.7 0.5±1.4 0.7±2.2 0.3±0.9 0.5±1.6 0.8±2.4 0.1±0.3 0.2±0.8 0.3±1.1 Strongyloides stercoralis 0.2±0.6 0.4±1.1 0.6±1.6 0.3±0.7 0.5±1.3 0.8±1.9 0.1±0.4 0.3±1.0 0.4±1.5 Taenia/Echinococcus sp 0.3±0.8 0.7±1.8 1.0±2.6 0.1±0.4 0.2±1.0 0.3±1.4 0.2±0.5 0.4±1.2 0.6±1.6 Trichuris trichiura 1.6±1.9 3.5±3.8 5.1±5.6 2.0±2.0 4.2±3.9 6.3±5.9 0.9±1.2 1.6±2.0 2.5±3.1 Total 9.8±4.8 20.9±9.7 30.7±14.3 9.9±3.2 20.3±6.4 30.2±9.4 4.4±2.6 8.0±4.1 12.4±6.6 Discussion Cockroaches are nuisance pests whose ac- tivities impact negatively on humans. Of great concern to human and public health, is their capability as potential mechanical vectors of pathogens, including parasites. Previous stud- ies from other parts of Nigeria (13, 24, 25) and elsewhere (6, 12, 26) had reported that cock- roaches captured from homes, hostels, hospi- tals, and markets carry an array of human in- testinal parasites. Results of the present study, which show clearly that the two cockroach spe- cies (P. americana and B. germanica) from res- idential buildings in Somolu, Lagos, southwest Nigeria, carry human intestinal parasites on their body surfaces and/or in the gut indicate that concerns over their potential and/or role as mechanical vectors cannot be overlooked. The species of human intestinal parasites recovered from cockroaches in the present study, (E. histolytica/dispar, E. coli, G. lamblia, Cryptosporidium sp. A. lumbricoides, T. trichiura, hookworms, S. stercoralis, Taenia/ Echinococcus spp., H. nana, and E. vermic- ularis) are responsible for a number of disease conditions in man, some of which could be life-threatening. The three major soil-trans- http://jad.tums.ac.ir/ J Arthropod-Borne Dis, June 2018, 12(2): 141–151 AA Adenusi et al.: Domiciliary Cockroaches … 148 http://jad.tums.ac.ir Published Online: June 12, 2018 mitted helminths (A. lumbricoides, T. trichiura, and hookworms) account for a high burden of disease globally and are intimately related with malnutrition, growth stunting and cog- nitive deficits in children (27). Strongyloides stercoralis may cause complicated infections with high case fatality rates due to hyper- infection or dissemination, especially in im- munocompromised individuals (28). Cryptos- poridium sp. and G. lamblia are nowadays, major causes of diarrhoea, especially in chil- dren (29). Entamoeba histolytica causes am- oebiasis, a potentially severe and life-threat- ening disease and the second most common cause of death from parasitic diseases, after malaria (30). Accidental ingestion of Taenia (particularly, T. solium) eggs often results in human neurocysticercosis, the leading cause of preventable epilepsy worldwide and also, a leading cause of deaths from food-borne diseases (31). Species of Echinococcus cause life-threatening chronic diseases with poor prognosis and high fatality rates, if not care- fully managed clinically (32). Parasite species reported in the present study are consistent with those documented in similar studies (13, 24, 25, 33, 34). However, the disparities could be due to differences in the levels of household and environmental hygiene, transmission dynamics between study localities, and in the diagnostic procedure employed. Predominance of A. lumbricoides on body surfaces and/or in the gut of cock- roaches across all different housing types in the present study is in consonance with find- ings from similar studies in other parts of the country (13, 25, 33). This could be due to its predominance in the human population and/or the persistence of its eggs in the environment for months to years (35). Identity of parasite species in cockroach- es from all three housing types indicates that these parasites have equal chances of being acquired by cockroaches, probably because they are endemic in the study area. Differ- ences in individual parasite species burdens between cockroaches from low-cost (LCB or LC2-S) and MCF could then be explicated by the varying levels of hygiene and sanitation in each housing type. Poorer housing and sani- tary conditions, which could predispose to higher parasite contamination, characterize low-cost households. Overwhelming and widespread prevalence (96.4%) of human intestinal parasites in dom- iciliary cockroaches in the present study is singular in Nigeria and is a cause for public health concern. Other studies from Nigeria had reported prevalences of 58.6% in Calabar, Southsouth (25), 67.1% in Owerri, Southeast (33) and 77.5% in Sokoto, Northwest (24). Al-Mayali and Al-Yaqoobi (36) and El- Sherbini and El-Sherbini (34) reported prev- alences of 83.3% and 98% respectively, in Iraq and Egypt. Disparities in prevalences be- tween different studies may be explained by differences in the levels of hygiene and sani- tation between study localities. Identity in the diversity of parasites be- tween P. americana and B. germanica as well as the insignificant statistical differences in their respective prevalences in the cockroach species indicate a uniform distribution of para- site species between the two cockroach spe- cies in the same environment. They also sug- gest that the two cockroach species have equal potential for mechanical transport and possi- bly, consequent dissemination of parasites in the environment. Because pathogens carried by cockroaches are acquired from their immediate environ- ments (37), the human intestinal parasites re- ported herein, were acquired through contact with unhygienic environments. Most of the parasites whose cysts, oocysts, eggs and/or larvae (hookworm: A. duodenale only) were isolated from cockroaches in the present study are transmitted to humans via consumption of food and/or water so contaminated. Since cock- roaches travel indiscriminately between filth and human food, they may be capable of dis- seminating parasite stages (on their body sur- http://jad.tums.ac.ir/ J Arthropod-Borne Dis, June 2018, 12(2): 141–151 AA Adenusi et al.: Domiciliary Cockroaches … 149 http://jad.tums.ac.ir Published Online: June 12, 2018 faces and/or in the gut) through physical dis- lodgement, vomitus and/or feces onto any sub- strate in the environment, including human food and food preparation surfaces. The med- ical and public health implications of this are better imagined. Cysts of E. histolytica and E. dispar are morphologically indistinguishable microscop- ically, so also are the eggs of Echinococcus and Taenia species. Since molecular techniques, which differentiate reliably, cysts of E. his- tolytica from E. dispar (38) and eggs of Echi- nococcus from Taenia species (39, 40) were not employed in the present study, the former was simply identified morphologically as E. histolytica/dispar and the latter as Taenia/ Echinococcus spp. Conclusion Cockroaches (P. americana and B. german- ica) across different housing types in Somolu, Lagos metropolis, Nigeria, transport on their body surfaces and/or in the gut, transmissive stages of human intestinal parasites and thus, may serve as reservoirs and potential mechan- ical vectors for disease transmission. The ex- ceptionally high prevalence of parasites in cockroaches (96.4%) justifies the need for im- provements in existing standards of household hygiene and environmental sanitation in order to minimize cockroach contact with unhygienic sites/substrates from which parasites are ac- quired. Acknowledgements We are grateful to all residents of the dif- ferent houses selected for participation in the study, for their cooperation and understand- ing in the execution of the study. The authors declare no conflict of interests. References 1. Cochran DG (1999) Cockroaches: Their Biology, Distribution and Control. WHO/ CDS/CPC/WHOPES/99.3. World Health Organization, Geneva. 2. Kramer RD, Brenner RJ (2009) Cockroach- es (Blattaria). In: Mullen GR, Durden LA (Eds) Medical and Veterinary Ento- mology, 2nd Edition. Academic Press/ Elsevier Inc., New York, USA, pp. 41– 55. 3. Beccaloni GW (2014) Cockroach Species File Online. Version 5.0/5.0. World Wide Web electronic publication. Available at: http://Cockroach.SpeciesFile.org 4. Rust MK, Reierson DA (2007) Cockroaches. Integrated Pest Management for Home Gardeners and Landscape Professionals. Pest Notes, Publication 7467, Universi- ty of California Agriculture and Natu- ral Resources, California, USA. 5. Anikwe JC, Adetoro FA, Anogwih JA, Makanjuola WA, Kemabonta KA, Akinwande KL (2014) Laboratory and field evaluation of an Indoxacarb Gel bait against two cockroach species (Dictyoptera: Blattellidae, Blattidae) in Lagos, Nigeria. J Econ Entomol. 107 (4): 1639–1642. 6. Hamu H, Debalke S, Zemene E, Birlie B, Mekonnen Z, Yewhalaw D (2014) Iso- lation of intestinal parasites of public health importance from cockroaches (Blattella germanica) in Jimma Town, Southwestern Ethiopia. J Parasitol Res. p. 5. 7. Hashemi-Aghdam SS, Oshaghi MA (2015) A checklist of Iranian cockroaches (Blat- todea) with description of Polyphaga sp. as a new species in Iran. J Arthropod Borne Dis. 9: 161–175. 8. Nazari M, Alipourian Motlagh B, Nasirian H (2016) Toxicity of cypermethrin and chlorpyrifos against German cockroach [Blattella germanica (Blattaria: Blattelli- dae)] strains from Hamadan, Iran. Pak J Biol Sci. 19: 259–264. 9. Jeong KY, Son M, Lee JH, Hong CS, Park http://jad.tums.ac.ir/ http://cockroach.speciesfile.org/ J Arthropod-Borne Dis, June 2018, 12(2): 141–151 AA Adenusi et al.: Domiciliary Cockroaches … 150 http://jad.tums.ac.ir Published Online: June 12, 2018 JW (2015) Allergenic characterization of a novel allergen, homologous to chy- motrypsin, from German cockroach. Al- lergy, Asthma and Immunol Res. 7(3): 283–289. 10. Rabito, FA, Carlson JC, He H, Werth- mann D, Schal C (2017) A single in- tervention for cockroach control reduc- es cockroach exposure and asthma mor- bidity in children. J Allergy Clin Im- munol. 140(2): 565–570. 11. Salehzadeh A, Tavacol P, Mahjub H (2007) Bacterial, fungal and parasitic contam- ination of cockroaches in public hospi- tals of Hamadan, Iran. J Vector Borne Dis. 44: 105–110. 12. Kinfu A, Erko B (2008) Cockroaches as carriers of human intestinal parasites in two localities in Ethiopia. Trans R Soc Trop Med Hyg. 102: 1143–1147. 13. Isaac C, Orue PO, Iyamu MI, Ehiaghe JI, Isaac O (2014) Comparative analysis of pathogenic organisms in cockroach- es from different community settings in Edo State, Nigeria. Korean J Parasitol. 52: 177–181. 14. Sayyad S, Vahabi A, Vahabi B, Sayyadi M, Sahne SH (2016) Investigation of bacteriological infections of the Amer- ican cockroaches in Paveh City, Kerman- shah Province. Mater Sociomed. 28(1): 17–20. 15. Yones DA, Galal LA, Abdallah AM, Za- ghlol KS (2015) Effect of enteric para- sitic infection on serum trace elements and nutritional status in upper Egyptian children. Trop Parasitol. 5(1): 29–35. 16. Sinniah B, Hassan AKR, Sabaridah I, Soe MM, Ibrahim Z, Ali O (2014) Preva- lence of intestinal parasitic infections among communities living in different habitats and its comparison with one hundred and one studies conducted over the past 42 years (1970 to 2013) in Ma- laysia. Trop Biomed. 31(2): 190–206. 17. Ahmad A, Ghosh A, Schal C, Zurek L (2011) Insects in confined swine opera- tions carry a large antibiotic resistant and potentially virulent enterococcal com- munity. BMC Microbiol. 11: 23. 18. Federal Republic of Nigeria (2010) 2006 Population and Housing Census: Pri- ority Table Volume III: Population Distribution by Sex, State, LGA and Senatorial District. National Population Commission, Abuja, Nigeria. 19. Burgess NRH (1993) Cockroaches (Blat- taria). In: Lane RP, Crosskey RW (Eds) Medical Insects and Arachnids. Chap- man and Hall, London, pp. 473–482. 20. WHO (1991) Basic Laboratory Methods in Medical Parasitology. World Health Organization, Geneva. 21. Adegbola RA, Demba E, DeVeer G, Todd J (1994) Cryptosporidium infection in Gambian children less than five years of age. J Trop Med Hyg. 97: 103–107. 22. WHO (1994) Bench Aids for the Diagno- sis of Intestinal Parasites. World Health Organization, Geneva. 23. R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical computing, Vienna, Austria. 24. Bala AY, Sule H (2012) Vectorial poten- tial of cockroaches in transmitting par- asites of medical importance in Arkilla, Sokoto, Nigeria. Niger J Basic Appl Sci. 20(2): 111–115. 25. Etim SE, Okon OE, Akpan PA, Ukpong GI, Oku EE (2013) Prevalence of cock- roaches (Periplanata americana) in households in Calabar: Public health im- plications. J Public Health Epidemiol. 5(3): 149–152. 26. Chamavit P, Sahaisook P, Niamnuy N (2011) The majority of cockroaches from the Samutprakarn Province of Thailand are carriers of parasitic organ- isms. EXCLI J. 10: 218–222. 27. Pullan RL, Smith JL, Jasrasaria R, Booker SJ (2014) Global numbers of infection http://jad.tums.ac.ir/ http://www.ncbi.nlm.nih.gov/pubmed/?term=Isaac%20C%5BAuthor%5D&cauthor=true&cauthor_uid=24850961 http://www.ncbi.nlm.nih.gov/pubmed/?term=Orue%20PO%5BAuthor%5D&cauthor=true&cauthor_uid=24850961 http://www.ncbi.nlm.nih.gov/pubmed/?term=Iyamu%20MI%5BAuthor%5D&cauthor=true&cauthor_uid=24850961 http://www.ncbi.nlm.nih.gov/pubmed/?term=Ehiaghe%20JI%5BAuthor%5D&cauthor=true&cauthor_uid=24850961 http://www.ncbi.nlm.nih.gov/pubmed/?term=Isaac%20O%5BAuthor%5D&cauthor=true&cauthor_uid=24850961 J Arthropod-Borne Dis, June 2018, 12(2): 141–151 AA Adenusi et al.: Domiciliary Cockroaches … 151 http://jad.tums.ac.ir Published Online: June 12, 2018 and disease burden of soil transmitted helminth infections in 2010. Parasit Vec- tors. 7: 37. 28. Henriquez-Camacho C, Gotuzzo E, Eche- varria J, White Jr AC, Terashima A, Samalvides F, Pérez-Molina JA, Plana MN (2016) Ivermectin versus albend- azole or thiabendazole for Strongyloi- des stercoralis infection. Cochrane Da- tabase Syst Rev. 1: CD007745. 29. Osman M, El Safadi D, Cian A, Benam- rouz S, Nourrisson C, Poirier P, Pereira B, Razakandrainibe R, Pinon A, Lambert C, Wawrzyniak I, Dabboussi F, Delbac F, Favennec L, Hamze M, Viscogliosi E, Certad G (2016) Prevalence and risk factors for intestinal protozoan infections with Cryptosporidium, Giardia, Blasto- cystis and Dientamoeba among school- children in Tripoli, Lebanon. PLoS Negl Trop Dis. 10(3): e0004496. 30. Skappak C, Akierman S, Belga S, Novak K, Chadee K, Urbanski SJ, Church D, Beck PL (2014) Invasive amoebiasis: a review of Entamoeba infections high- lighted with case reports. Can J Gas- troenterol Hepatol. 28: 355–359. 31. WHO (2016) Preventable epilepsy: Tae- nia solium infection burdens economies, societies and individuals: A rationale for investment and action. WHO/HTM/ NTD/NZD/2016.1. World Health Or- ganization, Geneva. 32. McManus DP, Gray DJ, Zhang W, Yang Y (2012) Diagnosis, treatment, and man- agement of echinococcosis. BMJ. p. 344. 33. Ajero CMU, Ukaga CN, Ebirim C (2011) The role of cockroaches (Blatta orien- talis and Periplaneta americana) in me- chanical transmission of parasites in households in Owerri, South East Nige- ria. Niger J Parasitol. 32(2): 153–156. 34. El-Sherbini GT, El-Sherbini ET (2011) The role of cockroaches and flies in me- chanical transmission of medical im- portant parasites. J Entomol Nematol. 3: 98–104. 35. WHO (2004) Integrated guide to sanitary parasitology. Regional Office for the Eastern Mediterranean. WHO Regional Centre for Environmental Health Ac- tivities, Document WHO-EM/CEH/121/ E. Amman, Jordan. 36. Al-Mayali HH, Al-yaqoobi MSM (2010) Parasites of cockroach, P. americana (L), in Al-Diwaniya Province, Iraq. J Thi-Qar Sci. 2(3): 93–104. 37. Menasria T, Tine S, Mahcene D, Benam- mar L, Megri R, Boukoucha M, Debabza M (2015) External bacterial flora and antimicrobial susceptibility patterns of Staphylococcus spp. and Pseudomonas spp. isolated from two household cock- roaches, Blattella germanica and Blat- ta orientalis. Biomed Environ Sci. 28 (4): 316–320. 38. Lau YL, Anthony C, Fakhrurrazi SA, Ib- rahim J, Ithoi R, Mahmud R (2013) Re- al-time PCR assay in differentiating En- tamoeba histolytica, Entamoeba dispar and Entamoeba moshkovskii infections in Orang Asli settlements in Malaysia. Parasit Vectors. 6(1): 250. 39. Jimenez JA, Rodriguez S, Moyano LM, Castillo Y, Garcia HH (2010) Differen- tiating Taenia eggs found in human stools - does Ziehl Neelsen staining help? Trop Med Int Health. 15(9): 1077–1081. 40. Salant H, Abbasi I, Hamburger J (2012) The development of a loop-mediated iso- thermal amplification method (LAMP) for Echinococcus granulosus coprode- tection. Am J Trop Med Hyg. 87: 883– 887. http://jad.tums.ac.ir/