key: cord-333950-e0hd3iuu
authors: Maillard, Jean-Yves; Bloomfield, Sally F.; Courvalin, Patrice; Essack, Sabiha Y.; Gandra, Sumanth; Gerba, Charles P.; Rubino, Joseph R.; Scott, Elizabeth A.
title: Reducing antibiotic prescribing and addressing the global problem of antibiotic resistance by targeted hygiene in the home and everyday life settings: A Position Paper
date: 2020-04-18
journal: Am J Infect Control
DOI: 10.1016/j.ajic.2020.04.011
sha: 
doc_id: 333950
cord_uid: e0hd3iuu

Antimicrobial resistance (AMR) continues to threaten global health. Although global and national AMR action plans are in place, infection prevention and control is primarily discussed in the context of healthcare facilities with home and everyday life settings barely addressed. As seen with the recent global SARS-CoV-2 pandemic, everyday hygiene measures can play an important role in containing the threat from infectious microorganisms. This position paper has been developed following a meeting of global experts in London, 2019. It presents evidence that home and community settings are important for infection transmission and also the acquisition and spread of AMR. It also demonstrates that the targeted hygiene approach offers a framework for maximizing protection against colonization and infections, thereby reducing antibiotic prescribing and minimizing selection pressure for the development of antibiotic resistance. If combined with the provision of clean water and sanitation, targeted hygiene can reduce the circulation of resistant bacteria in homes and communities, regardless of a country's Human Development Index (overall social and economic development). Achieving a reduction of AMR strains in healthcare settings requires a mirrored reduction in the community. The authors call upon national and international policy makers, health agencies and healthcare professionals to further recognize the importance of targeted hygiene in the home and everyday life settings for preventing and controlling infection, in a unified quest to tackle AMR.

The global impact is already profound and expected to intensify, particularly among the poorest nations. 3, 4 The main driver is overuse and misuse of antibiotics in medicine and agriculture including unregulated over-the-counter sales, while global spread of resistant bacteria or resistance genes is attributed to poor infection prevention and control in healthcare facilities, and sub-optimal hygiene and sanitation in communities, confounded by poor infrastructure and weak governance. 5 In the US, between 80-90% of the volume of human antibiotic use occurs in the outpatient setting, with nearly 50% considered to be inappropriate or unnecessary. 6 Without prompt action, it is estimated that rates of AMR to commonly-used antibiotics could exceed 40-60% in some countries by 2030, 7 and by 2050, around 10 million people could die each year as a result of resistance to antibiotics and other antimicrobial agents. 8 Almost 9

million of these will be in Africa and Asia. 8 In 2015, an alliance of the WHO, the Food and Agriculture Organization of the United Nations interventions." 9 The GAP emphasizes the need for society-wide engagement, with a clear focus on "prevention first." 9 One of the five strategic objectives is a reduction in the incidence of infection through improved sanitation, hygiene, and infection prevention. 9 At least 120 countries have finalized national action plans, with the plans of more than 60 other countries under development. 10 What is striking is that the GAP and national plans discuss infection prevention and control primarily in the context of healthcare facilities. (See https://www.who.int/antimicrobialresistance/national-action-plans/library/en/). By contrast, the latest 2019 UK national action plan, which sets out a 20-year vision 11 and a 5-year plan 12 for how the UK will contribute to controlling AMR by 2040, offers guidelines on infection prevention in healthcare settings, but also highlights the role of the community, noting that, when it comes to infections in the community, the public have a huge part to play. 12 

In recent years, demographic changes and changes in health service structure mean that the number of people living in the community needing special care, because they are at greater risk of infection, has significantly increased. The largest proportion of these are the elderly, who generally have reduced immunity to infection which is often exacerbated by other illnesses like diabetes and malignant illnesses. A decrease in immunity usually starts from 50 years old.

Other infection-susceptible groups include the very young, patients recently discharged from hospital, and family members with invasive devices such as catheters, as well as those whose immune competence is impaired as a result of chronic and degenerative illnesses (including HIV/AIDS) or because they are receiving immunosuppressant drugs or other therapies.

Immunosuppressed individuals are often also on other medications such as antibiotics, to help protect them from infection but can further increase susceptibility to infections such as Clostridium difficile.

Home and everyday life settings provide multiple opportunities for spread of infection.

Everyday life settings include locations where normally there is no mandated hygiene policy as is typically found in clinical and educational settings; for example: work places, public transport, gyms, child day-care facilities, and shopping centers.

Poor hygiene is considered a major factor in the transmission of community-based infections, including gastrointestinal (GI) and respiratory tract (RT) infections such as colds and influenza, and skin infections caused by S. aureus. 14 For the elderly, communal living environments, combined with problems of fecal incontinence, create an environment in which enteric and foodborne pathogens are easily spread. As a result, the incidence of salmonellosis and

Campylobacter diarrhea appears to be higher among the elderly in these situations.

More vulnerable 'at risk' members of society are now being looked after outside hospital settings. For example, in Germany, it is estimated that approximately three quarters of all people in need of care are currently being cared for at home. 15 In the community the immunocompromised are also at risk from opportunistic pathogens such as E. coli, Klebsiella spp., and Pseudomonas aeruginosa, which are considered as hospital related. 15 The key steps in preventing the spread of infection, known as breaking the chain of infection, are the same regardless of setting. In the home, pathogens may have been brought home from hospital settings or enter the home via colonized or infected people, pets/domestic animals, or through contaminated food and water. 15, 16 Pathogens and other microbes are shed constantly from these sources, with rapid transmission around the home mainly via hands, hand and food contact surfaces, cleaning utensils and in the air ( Figure 1 ). 15 respectively. For Campylobacter, counts of >100 and >1000 were isolated from 5 and 1.7%

respectively. This is a concern, since it is estimated that 80% of Salmonella infections originate in the home, 32 and a UK study detected Campylobacter spp. in 56% of chilled retail chickens, with 7% of samples containing >1000 colony forming units (CFU)/g of skin. 33 The infectious dose of Campylobacter is estimated at <500 CFU. 34 Chaidez et al. 35 demonstrated that the risk of Salmonella transmission from cleaning cloths via hands to mouth was far higher than the guideline levels for acceptable risk.

Since most pathogenic organisms die relatively rapidly, particularly on dry surfaces, the greatest risk of human exposure presents immediately after shedding from an infected or contaminated source. However some species, including S. aureus, E. coli, and other organisms such as fungal species, rhinovirus, and norovirus can survive for long periods even on dry surfaces. 36 Audit studies suggest that some Gram-negative organisms can form permanent reservoirs or secondary sources of contamination, particularly where moisture is present such as in sinks and drains, kitchen cleaning cloths and sponges. 37 44 The dose also depends on host susceptibility and mode of entry, and may be lower for at-risk groups in the community such as children, the elderly, and people with compromised immunity. 44 Although care of increasing numbers of patients in the community, including at home can help alleviate over-burdened health systems, it can be undermined by inadequate infection control in the home and urgent focus is now needed on infection transmission in homes and community settings in addition to healthcare settings.

Although multidrug-resistant (MDR) bacteria (i.e. bacteria that have acquired resistance to at least one agent in three or more antimicrobial classes) are typically hospital-acquired, 50 Since 2000, we have seen the emergence of new "community acquired" strains of MRSA (CA-MRSA). While healthcare-associated strains are mainly a risk to vulnerable people, for CA-MRSA, any family member is at risk and it is more prevalent among children and young adults where they cause infections of cuts, wounds and abrasions. US experience suggests the risk is greatest among those engaging skin-to-skin contact activities and contact with contaminated objects such as towels, sheets and sports equipment. Transmission is common in settings such as prisons, schools and sports teams. 42 A study assessing the transmission of CA-MRSA in a university in the US, found multidrug resistant USA300 responsible for diseases including necrotizing pneumonia, severe sepsis and necrotizing fasciitis, on common touch surfaces at the university, student homes and local community settings. This suggests transfer between different locations within the community. 61 Enterobacterales are a common cause of community-associated infections, including urinary tract infections and bacteremia as well as gastrointestinal infections. 51 67 Kitchen sponges not only act as reservoirs of microorganisms, but also as disseminators over domestic surfaces, which can lead to cross-contamination of hands and food, which is considered a main cause of foodborne disease outbreaks.

Carbapenem-resistant Enterobacteriaceae (CRE) are also on the rise globally, but, to date, most CRE infections in the US and Europe have been healthcare-associated. 68, 70 Although data from Asia is sparse, carbapenemases have been found in bacteria recovered from drinking water in India and in food-producing animals in China. 69, 71, 72 In European studies during the 1990s, vancomycin-resistant enterococci (VRE) were detected in the stools of healthy volunteers. [73] [74] [75] [76] [77] However, rates of VRE, carbapenem resistance in Acinetobacter infections, and MDR P.

aeruginosa are thought to be low in individuals living in the community. 51 Overall, the evidence suggests that MDR strains of bacteria, like any other strains of bacteria, can enter the home or other settings via people who are infected or colonized or via contaminated food and can be spread to other members of the family via hands and contaminated surfaces.

If implemented effectively, home and everyday life hygiene has the potential to reduce rates of infection and the need for antibiotic prescriptions, thereby reducing the selective pressure for the development and subsequent dissemination of resistance. 15 Microbiological data 14, 15 suggest that the surfaces that are most often responsible for spread of harmful microbes, at key moments include the hands themselves, hand contact surfaces, food contact surfaces, and cleaning cloths and other cleaning items ( Figure 2 ). These surfaces are referred to as critical surfaces or critical control points. Clothing, household linen, toilets, sinks and bath surfaces may also contribute to establishing a chain of infection, however, the risks associated with these surfaces are typically lower as they rely on the hands and other "chain links" to disseminate infectious microbes to cause human exposure. 

An important aspect of targeted hygiene is hygienic cleaning -as opposed to visible cleaningto break the chain of infection. This is achieved using hygiene procedures (products plus process) to reduce pathogenic microorganisms on critical surfaces to a level where they are no longer harmful to health -thereby preventing ongoing spread. 15, 84 Several methods exist to achieve such reduction in potential pathogens: mechanical/physical removal using dry wiping, soap or detergent-based cleaning together with adequate rinsing, inactivation or eradication using a disinfectant on hard surfaces or an alcohol-based sanitizer on the hands, or a physical process such as heating (to ≥60°C/140°F) or ultraviolet treatment. Most frequently, a combination of these approaches is likely to be used. 15, 84 When developing hygiene procedures aimed at breaking the chain of infection, the goal should be to ensure that each procedure is appropriate to its intended use. In recent years, risk modelling has been developed in order to achieve this. 80 Quantitative Microbial Risk Assessment (QMRA) was originally developed for ensuring water quality and is increasingly being used to develop infection prevention control strategies in other settings, including healthcare. 85, 86 QMRA is a scientifically-validated approach that uses published data to model the chain of infection and estimate safe residual level of contamination at critical points in the chain. 84 , 87 This information is then used to estimate the log reduction required to reduce contamination to a safe level. Based on these estimates, tests modelling use conditions can be used to develop effective hygiene procedures to achieve the required reduction. The approach is set out in more detail by Bloomfield et al. 84 In the past, recommendations on selection of hygiene procedures for home and everyday life were based on the health status of family members, and it is still argued by some that disinfectants should only be used in situations where people are infected or at increased risk of infection. 87 Although there is data to show that hygiene is important in preventing transmission of MRSA colonization and infection in the domestic environment, further investigation is required to demonstrate the full extent to which poor home hygiene may contribute to the burden of foodborne infection associated with antibiotic resistant strains.

Quantifying the impact of hygiene on the burden of infection in home and everyday life is challenging because of the large population sizes required to generate significant results, and difficulties in conducting studies involving multiple interventions. Most data have been generated from single intervention studies -primarily hand hygiene -where meta-analyses show a positive impact on GI and RT infections. [91] [92] [93] Children who attend day-care centers have significantly more infections than those who do not.

The most common are RT and GI infections, and the risk of otitis media is almost twice that of children remaining at home. 94 Studies in day-care centers and schools in which hand hygiene was combined with cleaning and/or disinfection of environmental surfaces indicate a positive impact on illness rates and reduction in the use of antibiotics. [94] [95] [96] [97] In an intervention study 96 reduction of antibiotic prescriptions for RT infections in a group who used hand sanitizers compared with a control group. 98 Another 2018 intervention study 99 found that children were prescribed antibiotics for significantly fewer weeks in day care centers using specific disinfecting products and cleaning protocols than centers that continued to use their standard procedures and products (RR=0.68 [95% CI 0.54, 0.86]; p=0.001) -a relative risk reduction of almost onethird.

To the best of our knowledge, only one study on the impact of targeted hygiene in the home has been conducted. 100 This study, conducted among low-income communities in Cape Town, South Africa, evaluated the impact of hygiene education alone and education in combination with hand washing with soap at critical times, bathing at least three times a week, cleaning/disinfecting household surfaces at critical times, and proper waste disposal. 100 QMRA is also now being used to estimate the impact of hygiene interventions on infection in community settings. 102 Haas et al. 103 

Concern has been expressed as to whether expanding use of microbicidal products, in the home and everyday life may contribute to the rise in AMR. 105 Sub-lethal levels of microbicides can induce stress on bacterial cells, causing expression of mechanisms that reduce the biocide concentration at the bacterial target site further and allow the bacterial cell to repair. 106, 107 These include overexpression of an efflux system, membrane regulatory changes, and changes in membrane permeability and composition. 107 These same mechanisms can produce changes in the susceptibility profile to unrelated antimicrobials. 107 In other words, the use of microbicides may cross-select for antibiotic resistance and be associated with reduced antibiotic susceptibility to clinically significant levels (recently reviewed by Maillard 107 ).

Factors inherent to the microbicide (i.e. concentration, formulation, mechanism of action), the microorganisms (i.e. type/strain, metabolism, resistance mechanisms), and product usage (e.g.

concentration, exposure time), all impact on product efficacy. 107 Decreases in efficacy, for example, following shorter contact time or product dilution, will lead to bacterial survivalantimicrobial damage caused by a sub-lethal concentration of a microbicide is likely to be repairable. 107 A number of expert reports commissioned in the last 10 years have highlighted laboratory studies linking microbicide use with reduced antibiotic susceptibility. However, these reports conclude that there is little evidence for this effect occurring in real-life clinical practice, and have called for further research into whether microbicide use influences antibiotic resistance in the community. 108-111 Rutala et al. (2000) found that the frequency of occurrence of antibiotic resistance in environmental isolates from homes was much lower than for clinical isolates from a hospital intensive care unit and an outpatient setting where there was routine extensive use of antibiotics. 112 Two studies were carried out to investigate whether antibiotic resistant strains were more likely to be found in homes where antibacterial products were used, compared with homes where they were not. 113, 114 Samples were collected from houses in the USA and UK of 30 users and nonusers of antibacterials. Susceptibility tests against antibiotics and antibacterial agents (triclosan, pine oil, BAC and para-chloro-meta-xylenol) were carried out on the bacteria isolated. The authors concluded that there was no evidence that antibiotic resistant strains occurred more frequently in user homes compared with non-user homes. A 1-year study by Aiello et al (2005) also showed that household use of antibacterial cleaning products was not a significant risk factor for occurrence of antibiotic resistant isolates from hands. 115 Despite more than 20 years of research, there is still no conclusive resolution to the question of whether and to what extent; microbicides might contribute to AMR in clinical practice. In light of laboratory data, which indicates that microbicide-induced AMR is biologically plausible for some types of microbicides, it is concluded that use of microbicides needs to be prudent and appropriate and that the products containing them must be used at recommended concentrations and with the appropriate contact time.

Targeted hygiene works to ensure that use of disinfectants and hand sanitizers (i.e. microbicides used at the correct concentration and contact time) are confined to situations where there is identifiable risk of spread of harmful microorganisms, ensuring that they play an essential role in tackling AMR. The need for antibiotic prescribing may in fact increase if disinfectants and hand sanitizers are not used as indicated, due to the increased risk of infection and survival of bacteria bearing AMR determinants. These could potentially spread to other areas in the home and on into the community. It is important to note also that preventing viral infections as well as bacterial infections, such as those that cause respiratory and GI infections, can also have a role in reducing AMR as this will eliminate the potential for mis-prescribing or misuse of antibiotics.

In In 2015, an estimated 663 million people around the world were drinking from unimproved water sources, and 2.4 billion had no access to improved sanitation -the vast majority of these were in Sub-Saharan Africa and South Asia. 119 It is estimated that 2.3 billion people lack the use of sanitation facilities which are not shared with other households, 120 42 As with studies conducted in HICs, the highest levels of contamination in LMICs are typically found in moist locations such as kitchen sponges and dishcloths. [122] [123] [124] The key question, however, is whether, and to what extent, the incidence and levels of potentially harmful pathogens (and thus infection risks) are higher in homes without access to adequate water and sanitation.

Sinclair and Gerba 124 monitored fecal coliforms, total coliforms, E. coli and heterotrophic plate count bacteria on household surfaces in 8 homes that had improved latrines (i.e. a pour-flush latrine) in a rural village of Cambodia, and compared the results with similar data from homes in the US 38 and Japan. 39 Fecal coliform levels in Cambodia were found to be highest in moist locations such as the plastic ladle used for sink water, the toilet seat surface, and the cutting board surface. 124 For E. coli, the mean log CFU per 4 cm 2 ranged from 0.5 to 4.0, with highest counts found on the top of the squat toilet, the wash basin, and the floor around the toilet.

Fecal coliform levels were 100-fold higher on these surfaces in Cambodia than on equivalent surfaces in the US and Japanese studies.

In LMICs, due to a lack of basic sanitation, good hand hygiene is of vital importance. 116 Globally, it has been estimated that only 19% of the population washes its hands with soap after contact with excreta. 93 Observations show that hand washing with soap is undertaken in an ad hoc manner, 116 with many households having no access to handwashing facilities. 125 Unsurprisingly, studies in LMICs have reported high levels of fecal indicator bacteria on the hands of household members, [126] [127] [128] with one study correlating presence of fecal contamination on the hands with the prevalence of gastrointestinal and respiratory symptoms within the household. 126 A Cochrane review showed that improving hand washing practices probably reduces diarrhea episodes in child day-care centers in both high income countries and among communities living in low to middle income countries by as much as 30%. 92

The evidence set out in this paper suggests that, if combined with measures ensuring clean water and adequate sanitation, targeted hygiene practices in home and everyday life settings could make a significant contribution to tackling AMR through infection prevention and a consequential reduction in antibiotic prescribing. This is true in all areas of the world including low-income countries.

Additionally, the evidence suggests that hygiene promotion would contribute to preventing the transmission of resistant bacteria from the home and everyday life settings, into healthcare settings, and back into the community. Further research is still needed to evaluate the extent to which this might occur, especially in communities in low income countries.

To be effective, hygiene interventions need to consider all aspects that are likely to affect the outcome. This includes a reduction of antibiotics from the food chain and the environment, improved hygiene education and availability of appropriate products as well as the provision of clean water and improved sanitation.

Based on these findings, the authors of this paper issue a call to action to national and international health policy makers, health agencies, and healthcare professionals to give greater recognition to the importance of hygiene in the home and everyday life and development and promotion or more effective codes of practice for hygiene in the home and everyday life as part of national action plans to tackle AMR. Although the precise impact of hygiene on transmission of infection between community and healthcare settings needs further investigation, it is important to recognise, that reducing the need for antibiotic prescribing and the circulation of AMR strains in healthcare settings cannot be achieved without also reducing circulation of infections and AMR strains in the community. We cannot allow hygiene in home and everyday life settings to become the weak link in the chain.

The development of this position paper was supported by an educational grant from Reckitt

Benckiser who fund the activity of the Global Hygiene Council. Medical writing support was provided by the medical communications agency, Spink, which runs the secretariat for the GHC. 

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