Download PDF Microbiomes of the Built Environment September 15, 2022 Volume 52 Issue 3 The covid-19 pandemic suddenly directed awareness to potential health impacts of the built environment of everyday living – schools, dwellings, offices, public buildings, and other spaces. This issue explores the “microbiome” of the built environment in the postpandemic reality in terms of ventilation performance, filtration, understanding and quantification of transmission risk, protection of “benign” microbes, and the important role of equity, among others. Microbial Surface Transmission in the Built Environment and Management Methods Monday, September 19, 2022 Author: Amanda M. Wilson, Diane R. Gold, and Paloma I. Beamer An understanding of pathogen transmission is necessary to effectively protect the built—and human—microbiome. The early widespread concern during the covid-19 pandemic about surface transmission of the disease has waned. There was only one confirmed case, to our knowledge, of surface transmission: a susceptible elderly person used a toothpick after touching a contaminated elevator button (Xie et al. 2020). The dominant transmission route of current variants of covid-19 is airborne (Miller et al. 2021), but the potential risk of surface transmission—sometimes referred to as “fomite” (a surface capable of harboring pathogens) transmission (Boone and Gerba 2007)—is not zero. Anything in the air can end up on a surface and hands, leading to possible hand-to-mucosa transmission, given receptors in the mucosa of the nose, upper airways, and mouth (Prü 2022). Covid-19 transmission risk from a single touch with a contaminated surface is estimated at less than 1/10,000 (Pitol and Julian 2021; Wilson et al. 2021a), but the fomite transmission route is important for other pathogens and was even recognized historically. As early as the 17th century, the British intentionally gave blankets used by smallpox patients to Native Americans to infect them as a form of biological warfare (Patterson and Runge 2002). Transmission Methods and Factors Fomites can lead to infection via pathogen contact with an opening in the body (e.g., open wound, facial mucosal membrane). An infected individual can transfer a bodily fluid containing an infectious pathogen to their hand and (i) to others’ hands and eventually fomites or (ii) directly to fomites. These are then touched by susceptible individuals, who may then touch a facial mucosal membrane and/or contaminate other surfaces within hours (Reynolds et al. 2016). For respiratory pathogens, transmission may be via sputum, saliva, or nasal mucus (Adenaiye et al. 2021); for fecal-oral pathogens, the concern may be hand contamination from feces or vomit (Donskey 2010; Phan et al. 2018). Risk of contamination spread depends in part on the survivability of organisms and the frequency with which individuals touch their face, surfaces, or others’ hands. The risk of contamination spread also depends on the survivability of organisms (Casanova et al. 2010); the frequency with which individuals touch their face (Nicas and Best 2008), fomites (Beamer et al. 2012), or others’ hands (Jones et al. 2020); and transfer efficiency (the fraction of pathogens transferred to or from hands during a hand-to-fomite contact) (King et al. 2020). Examples of fecal-oral pathogens that pose fomite transmission risks are norovirus (Kraay et al. 2018), vancomycin-resistant Enterococci (Tacconelli and Cataldo 2008), and Clostridioides difficile (C. difficile) (Weber et al. 2013). For respiratory pathogens, an infected individual may aerosolize pathogens via sneezing, breathing, talking, coughing, singing, or playing a musical instrument (Coleman et al. 2022; Dhand and Li 2020; Fabian et al. 2008; He et al. 2021; Noti et al. 2012). While some infections (e.g., tuberculosis) are contracted strictly via inhalation, many respiratory viruses, such as rhino-virus (e.g., the “common cold”) or influenza A, can be transmitted via the upper airways, with receptors for the viruses in the mucosa (Jacobs et al. 2013; Richard et al. 2020), making surface transmission more theoretically relevant if aerosols containing these pathogens deposit on fomites that are then touched. Computational research has demonstrated that reduced airborne concentrations due to source control (e.g., via infected individuals’ mask use) can reduce fomite transmission (Wilson et al. 2021b) and that airflow patterns can influence deposition patterns on fomites and thus pathogen accruement on hands (King et al. 2015; Wilson et al. 2021c). The risks that fomites pose in this case depend, again, on the rates at which aerosols are produced and deposit on surfaces and the survivability of airborne pathogens on surfaces. Another factor influencing the importance of pathogens transmitted via surfaces is virulence versus pathogenicity. Some organisms (e.g., norovirus, SARS-CoV-2, rotavirus) are pathogenic in nonimmuno-compromised hosts; others (e.g., C. difficile, Pseudomonas aeruginosa, Staphylococcus aureus) are opportunistic, meaning they may be more pathogenic in compromised hosts relative to healthy nonelderly hosts. This can change the impact of fomite transmission of organisms like C. difficile by environment; for example, such transmission is of significant concern in healthcare settings with immunocompromised hosts. Survivability and factors that affect spatial spread are crucial to evaluating fomite transmission since environmental persistence influences environmental spread. Survivability factors such as temperature and humidity (Lin and Marr 2020; Marr et al. 2019) can affect transfer efficiency (Lopez et al. 2013). The concentrations of pathogens emitted from infected individuals are also a key consideration; a pathogen with a fast environmental decay rate could nonetheless pose meaningful risk if generated and introduced to the environment in large quantities. Importance of Human Behaviors Aside from environment survivability, human behavior is a key factor in characterizing risks posed by fomites, as even the most contaminated surface may pose little risk if it is rarely touched. Frequency of surface touches has a positive linear relationship with microbial bioburden on surfaces (Adams et al. 2017), suggesting surface cleaning and hands-free design as invaluable ways to reduce risk. Activity pattern studies of fomite exposures to microbial (and chemical) contaminants, to inform risk assessments, demonstrate that human interactions with fomites are frequent. For example, even older children may make over 1000 hand-to-surface contacts in an hour (Beamer et al. 2012). Hand-to-face contact data have been collected for children and adults (Beamer et al. 2012; Nicas and Best 2008) taking account of potential gender differences (or lack thereof) (Beamer et al. 2012; Zhang et al. 2020), and the influence of environment type (indoor vs. outdoor setting; Tsou et al. 2018) and masked vs. unmasked (Lucas et al. 2020). Most of the data on hand-to-surface frequency for adults have been collected in the context of healthcare surfaces and healthcare worker hand hygiene (King et al. 2021; Phan et al. 2018; Smith et al. 2012). Such studies have been used to identify and define high-touch surfaces for prioritization in cleaning and disinfection protocols (Huslage et al. 2010) with careful selection of cleaning agents to reduce chemically induced health challenges. In office settings, studies have explored the role of hand dominance and social networks in fomite transmission (Zhang et al. 2018, 2020). More data on hand-to-nasal orifices and hand-to-eye contacts and their duration for children and adults are needed to advance fomite transmission microbial risk assessment capabilities. Infection Control Methods and Impacts Controlling transmission is increasingly important for pathogens that are more commonly transmitted via fomites, especially those with antimicrobial resistance, the “overlooked pandemic” (Laxminarayan 2022). A traditional control approach has been cleaning and disinfection. But while the intention is to reduce the presence of pathogens, this approach also affects overall microbial communities on surfaces, with potential human health impacts, raising a recent question, Are we too clean?, particularly in home settings when no one is sick. Protecting Nonharmful Microorganisms The “hygiene hypothesis” is that decreases in infections and simultaneous increases in autoimmune and allergic diseases are related: reduction of microbes in environments leads to fewer interactions not only with pathogens but also with “old friends,” non-harmful microorganisms that aid in immune system development (Frew 2019). Evidence for this was observed in a study of Amish and Hutterite children: the Amish children, who worked more directly with animals, had lower rates of asthma and more diverse microbial communities in dust in their homes (Ober et al. 2017; Stein et al. 2016). Differences in microbial communities in dust between urban and rural environments (Shan et al. 2020) and between indoors and outdoors have also been reported (Barberán et al. 2015). Studies have been used to identify and define high-touch surfaces for prioritization in cleaning and disinfection protocols. Other beneficial microbiome health relationships include the skin microbiome vis-à-vis atopic dermatitis (Lynde et al. 2016), and the gut microbiome’s role in preventing infection from Helicobacter pylori (a risk factor for gastric cancer; Wroblewski et al. 2010) and C. difficile as well as its potential effects on irritable bowel syndrome and cardiovascular diseases (Shreiner et al. 2015). Health Impacts of Chemical Disinfection Further potential consequences of surface cleaning and disinfection include inhalation and dermal exposures to cleaning and disinfection chemicals, increasing health risks such as asthma, especially in occupational settings where cleaning and disinfection is frequent, such as in health care (Arif and Delclos 2012; Dumas et al. 2021), although some have demonstrated that these risks can be relatively low (Weber et al. 2016). When using cleaning and disinfection products, wipes instead of sprays can help reduce the aerosolization and inhalation of chemicals. Proper use of chemicals (e.g., observing recommended contact times) is also important to achieve effective microbial reductions. Disinfectants and sanitizers registered with the US Environmental Protection Agency should be considered rather than products without evaluated efficacy data. The “more is better” rule does not apply to cleaning and disinfection. The “more is better” rule does not apply to cleaning and disinfection. Targeted surface hygiene approaches have been proposed that can be tailored to the virulence and primary routes of a pathogen, by, for example, focusing on high-touch surfaces (Huslage et al. 2010) or specific moments (e.g., right after cooking with raw meat) to guide cleaning and disinfection (Bloomfield 2019). Engineering Strategies Engineering strategies can also be used to control fomite transmission. They may include proper ventilation and air filtration (Morawska et al. 2020), use of ultraviolet light (Kovach et al. 2017), and incorporation of antimicrobial materials such as silver-impregnated fabrics (Gerba et al. 2016) and copper materials (Bryce et al. 2022). For all types of transmission routes, engineering controls are more effective and reliable than those that are administrative or related to the use of personal protective equipment (Sehgal and Milton 2021). The latter methods may involve cleaning and disinfection, hand hygiene compliance, or glove use, all of which rely on consistent human behaviors in order to be effective. Ideally, multiple controls with rigorous protocols should be layered to enhance infection control. We note, however, that time, personnel, products, and resources to effect multiple controls may not be equally available. Inequities may place greater infection burdens on low-income and/or marginalized communities with limited financial, communal, or geographical access to necessary infrastructure, resources, and technologies. Conclusion While likely not a primary route for covid-19 transmission, fomites are important for a number of other pathogens of concern. Layered strategies are needed to control fomite transmission routes, including engineering controls (e.g., ventilation and air filtration to reduce the settling of pathogens on surfaces), fomite cleaning and disinfection, and hand hygiene. Strategies for targeted hygiene are recommended to reduce potential negative health effects from exposure to cleaning and disinfection chemicals and the unnecessary removal of beneficial and nonharmful microorganisms. Acknowledgments Wilson was funded by a University of Health -Sciences Career Development Award. Gold was supported, in part, by the Harvard Chan School NIEHS Center for Environmental Health (NIEHS P30-ES000002). Beamer and Wilson are supported by the Southwest Environmental Health Sciences Center (NIEHS P30 ES006694). This article’s contents are solely the responsibility of the authors and do not necessarily represent the official views of the National Institutes of Health. References Adams CE, Smith J, Watson V, Robertson C, Dancer SJ. 2017. Examining the association between surface bio-burden and frequently touched sites in intensive care. Hospital Infection 95(1):76–80. 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Scientific Reports 10(1):10457.  USEPA Pesticide Registration (https://www.epa.gov/pesticide-registration)  For a discussion of inequities in access to effective infection control, see Gold et al. (2022) in this issue. About the Author:Amanda Wilson is an assistant professor and Paloma Beamer a professor, Department of Community, Environment, & Policy, Mel and Enid Zuckerman College of Public Health, University of Arizona, Tucson. Diane Gold is a professor, Department of Environmental Health, Harvard T.H. Chan School of Public Health, and Channing Division of Network Medicine, Brigham and Women’s Hospital, Harvard Medical School.