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. Engineering and Design Factors for Healthful Built Environments Tuesday, September 20, 2022 Author: Erica M. Hartmann Healthful built environments require attention to design, energy consumption, air exchange, maintenance, and equity. In Maslow’s hierarchy, shelter is a physiological need, humans’ most fundamental requirement, and the basis of safety. People expect built environments to protect them not only from harsh elements like extreme weather but also from less visible threats, such as pathogens and toxic chemicals. The engineering challenge of meeting these expectations increases in complexity following the complexity of the demands: It is relatively easy to build a structure that provides shade from the sun, somewhat more complicated to also keep out the rain, and much more sophisticated engineering approaches are needed to protect occupants from air or waterborne pathogens. Moreover, it is extremely challenging to achieve all of these without exposing the occupants to potentially harmful chemicals. Role of Urban Development and Engineering in Pathogen Spread Host-pathogen interactions are a function of evolution and ecology, an intricate dance involving pathogen virulence, host resistance, and third-party species that can act as reservoirs or be the victim of “spillover” (Harvell 2004). As with many natural phenomena, human activities have accelerated the rate of new disease outbreaks (Harvell 2004). Urban Development The historical transition from a nomadic lifestyle to agrarian civilizations with domesticated livestock increased the transfer of microorganisms—-including viral, bacterial, and fungal pathogens—between humans and other animals (Piret and Boivin 2020; van Schaik 2022). More recently, increased population density, changes in land use, and rapid global travel have exacerbated the spread of infectious disease, increasing the frequency and magnitude of pandemics (Mankiewicz et al. 2021; Piret and Boivin 2020). Once introduced to humans, pathogens can spread via several routes—including water, air, surfaces (fomites), or close physical contact with other building occupants—all of which are facilitated by various aspects of modern civilization. Thus, the structure and interconnectedness of urban areas and buildings can affect the number and frequency of transmission events. Engineering and Building Design Although high-density urban areas favor the transmission of communicable disease, smart engineering can help protect residents from exposure. Among the earliest examples of engineering approaches to impede the spread of pathogens are water distribution and sanitation systems (Montgomery and Elimelech 2007). Indeed, access to water and sanitation through engineered systems can effectively eradicate waterborne diseases. However, even today access to clean water is not universal, and creative engineering and design solutions are needed to overcome obstacles to the development, adoption, and maintenance of urban and other water treatment systems (Montgomery and Elimelech 2007; Piret and Boivin 2020; Tulchinsky 2018, chapter 5). Even where clean water is available, design can facilitate adoption of best practices. For example, in hospitals proper placement of sinks makes healthcare workers more likely to adhere to hand hygiene guidelines and not use sinks for disposal of food or beverages, reducing the spread of hospital-acquired infection and the development of biofilms that can harbor pathogens (Grabowski et al. 2018; Zellmer et al. 2015). Thus, building design plays an important role in encouraging good behavior and preventing the spread of pathogens. The ongoing covid pandemic has emphasized the importance of airborne pathogen transmission. Sanitation, hand hygiene, and disinfection all remain essential practices, but engineering controls and building design are also critical in limiting exposure (Mankiewicz et al. 2021; Piscitelli et al. 2022). Physical and Chemical Controls and Side Effects Indoor versus Outdoor Air Quality Ventilation is emerging as one of the most valuable tools for maintaining healthy built environments (in this issue, see Persily and Siegel). Increased ventilation is associated with decreased covid transmission as well as higher productivity in workers and lower absenteeism in students (Leung 2015; Persily 2015; Piscitelli et al. 2022). Regardless of the exact mechanism underlying these effects, increasing air exchange rates is almost universally considered to positively impact occupant health. The use of outdoor air as a diluent for contaminant-laden, CO2-rich indoor air is predicated on good outdoor air quality. In some areas, outdoor air should not be directly introduced because of the presence of contaminants, especially particulate matter (PM) and oxidants (Leung 2015). Yet even with the potential for high PM, outdoor air quality is often vastly better than indoor air quality by other metrics, including concentrations of volatile organic chemicals (VOCs) (Liu et al. 2018). The structure and interconnectedness of urban areas and buildings can affect the number and frequency of pathogen transmission events. Local conditions play an important role in determining outdoor air quality. Concerns include levels of PM, nitrogen and sulfur oxides (NOx, SOx), ozone, biological contaminants (viruses, bacteria, fungi, pollen), and VOCs (e.g., benzene) (Jones 1999; Leung 2015; Mankiewicz et al. 2021). Notably, many of these pollutants can be far worse indoors than out, as they have important indoor sources. For example, PM and combustion byproducts are released during activities such as cooking, in which case the focus should be on exhausting cooking fumes rather than increasing overall ventilation (Jones 1999; Leung 2015). The nature and chemistry of contaminants may differ depending on whether they originated indoors or out. For example, bacteria carried in from outdoor air are much less likely to be human-associated than bacteria originating from indoor sources (i.e., occupants) (Leung 2015; Prussin and Marr 2015). Filtration Regardless of whether the source is indoors or out, the same strategies for improving indoor air quality apply. PM, biological matter, and ozone can be removed via filtration (Persily 2015). However, care needs to be exercised in selecting the most appropriate filter and in maintaining and changing filters. Under suboptimal conditions, filters may become a source of pollutants if organic matter is allowed to accumulate and react with ozone, thereby releasing volatile byproducts (Zhang et al. 2011). The same is true of adsorbents, which can be used to remove VOCs but can also become a source of VOCs if not properly maintained (Zhang et al. 2011). Filtration technologies should be evaluated on their ability not only to remove a pollutant of interest but also to generate clean air. As ozone is highly reactive, one alternative to filtration is increased ventilation. While a high ventilation rate might increase introduction of ozone from outdoor air, it concomitantly removes rapidly generated reactants and products (NASEM 2022). Thus, the introduction of ozone as a contaminant from outdoor air is most problematic at low ventilation rates. Many of the products generated by ozone result from uncontrolled reaction with skin lipids (Liu et al. 2021). Smart use of catalysts could efficiently decompose ozone without generating unwanted byproducts. Highly reactive chemical systems, like ozone, plasma, or photocatalytic oxidation, have intentionally been introduced to air purifiers with the goal of degrading organic contaminants. While these technologies may be effective at reducing a specific contaminant of concern, anything involving highly reactive chemistries may release byproducts like secondary or gaseous oxidation products, NOx, and ultrafine particles (Afshari et al. 2020; Zhang et al. 2011). Some air cleaners (e.g., electrostatic precipitators) also unintentionally generate ozone. These technologies can similarly release unintended harmful byproducts (Afshari et al. 2020). In light of these phenomena, technologies should be evaluated not only on their ability to remove a pollutant of interest but also to generate clean air. Research Needed A major challenge to evaluating technologies on this basis is that the definition of “clean” air is nebulous. One possible criterion might be that technologies not create harmful byproducts, although this does not guarantee that the resultant air poses a lower risk to occupant health. Overall, the health impacts of air cleaning technologies are unclear. Well-designed, rigorous real-world studies are needed to elucidate both the effects of air cleaning on air composition and subsequent impacts on human health and the mechanisms underlying these effects (Cheek et al. 2021; Liu et al. 2022). Such studies are especially necessary as there are no indoor air standards—in contrast to, for example, drinking water or outdoor air—to provide an objective metric. Surface Cleaning Surface cleaning is also an important element of building maintenance and an essential practice for the elimination of fomite transmission. However, many cleaning products incorporate VOCs and semi-VOCs that can act as irritants and have long-term negative health effects (Velazquez et al. 2019). Additionally, many surface cleaning products and technologies rely on oxidation, which can result in the formation of unintended harmful byproducts and oxidants, as discussed for air purifiers (Velazquez et al. 2019; Wang et al. 2020). Although problematic in terms of air quality, oxidative cleaning strategies (e.g., peroxide or peracetic acid) are often preferred over other antimicrobials (e.g., -triclosan and quaternary ammonium compounds) because of their broad spectrum of efficacy and lower tendency to promote the development of resistance (Velazquez et al. 2019). While antimicrobials play a pivotal role in treating and preventing human diseases, their efficacy and utility are jeopardized by overuse, including in agriculture (van Schaik 2022; Velazquez et al. 2019). Unnecessary use of antimicrobials can also promote resistance to clinically relevant drugs (van Schaik 2022; Velazquez et al. 2019), exacerbating the already dire global challenge of treating infections (Murray et al. 2022). More targeted cleaning strategies, such as cleaning products specifically aimed at viruses or moisture control for mold problems, rather than broad-spectrum antimicrobials, may alleviate some of these issues. Energy, Equity, and Other Considerations Human-induced climate change can increase conditions that lead to poor outdoor air quality and by extension indoor air quality. It behooves everyone to be mindful of energy consumption and carbon footprint in designing healthy built environments (Leung 2015). While increasing ventilation and filtration undoubtedly benefit building occupants, they increase the already massive energy demand required to heat and cool buildings (Mankiewicz et al. 2021). For comfort, outdoor air must be conditioned: heated or cooled, humidified or dehumidified. Thus, increasing outdoor air intake may not be economical. Similarly, high--efficiency filters require more energy to circulate air than their lower-efficiency counterparts. Increased energy demands are accompanied by increased costs, which may be prohibitive in some cases. Additionally, interventions like retrofits or portable air purifiers are expensive and thus not equitably accessible (Cheek et al. 2021; Lamplugh et al. 2020). Conversely, a singular focus on energy efficiency, as in the case of passive houses, neglects the health of building occupants. Providing equal, affordable access to clean air—whether “clean” is defined based on concentrations of contaminants or health endpoints—is essential from a social justice perspective, acknowledging that marginalized communities disproportionately experience poor air quality (Demetillo et al. 2020; Van Horne et al. 2022). Moreover, in terms of disease prevention, experiences with clean water yield important lessons: without equal access, diseases persist (Montgomery and Elimelech 2007). Finally, even when all economic and access concerns are addressed, personal preference or aesthetic considerations may prevent uptake. Wherever possible, the best way to improve air quality is to remove the source of contaminants, by, for example, using alternative, less toxic solvents or removing unnecessary or potentially harmful ingredients from personal care products. However, in occupational settings, if the replacement is more difficult to use, workers may opt to continue using the more toxic substance (Lamplugh et al. 2019). Similarly, noise levels may influence the use of air handlers or purifiers (Afshari et al. 2020). Creating Healthful Built Environments Building design should address health (Persily 2015). To build adequately protective environments, all of the above considerations need to be taken into account, and conflicting demands (e.g., controlling exposure to pathogens without increasing exposure to harmful chemicals or expanding carbon footprint) need to be resolved. At the very least, all these demands have clear and measurable outcomes: specific pathogens or chemicals to be avoided and energy targets to be met. Conflicting demands—e.g., controlling exposure Increasingly, expectations are shifting from illness prevention to a more proactive approach to health and well-being. Buildings of the future will be expected to provide shade from the sun and allow for appropriate daylighting to promote mental health; filter out UV radiation to prevent cancer and allow sufficient UV exposure for vitamin D production; prevent the spread of infectious disease and allow for early-life microbial exposures that mitigate the later development of allergies, asthma, and other auto-immune disorders (Mankiewicz et al. 2021); and do all this while being carbon and energy negative, potentially by harvesting solar energy. The design of healthful built environments entails teasing apart the nuances of these exposures and integrating them in building design and operation as well as neighborhood planning and urban development (Green 2014; Mankiewicz et al. 2021; van Schaik 2022). Maintenance will avoid the use of chemicals with negative impacts on human and environmental health. Energy demands associated with these design and operation practices will be met through more sustainable practices in architecture and energy generation. Healthful built environments will also aim to counter health disparities and promote equity. Conclusion While the ability to design structures that offer protection from harm is improving, more information is needed about how to build environments that promote health. The development of “green” and “well” building standards is a good start (Mankiewicz et al. 2021; Persily 2015). In addition, for building maintenance and cleaning, manufacturers are moving away from traditional harsh chemicals, particularly antimicrobials, and exploring the use of alternative products and cleaning strategies, including temperature and humidity control, which may have a larger impact on pathogen survival than cleaning (Hu et al. 2022; Velazquez et al. 2019). Also encouraging, market pressures are increasing for organic or “natural” ingredients in personal care products as consumers shy away from synthetic additives like antimicrobials and preservatives (Mordor Intelligence 2022). This shift in manufacturing could help with source control, effectively eliminating some organic contaminants. By taking a holistic approach, balancing all aspects of indoor environmental quality and critically reevaluating building operations and product use, healthful built environments are possible. References Afshari A, Ekberg L, Forejt L, Mo J, Rahimi S, Siegel J, Chen W, Wargocki P, Zurami S, Zhang J. 2020. Electrostatic precipitators as an indoor air cleaner: A literature review. -Sustainability 12:8774. Cheek E, Guercio V, Shrubsole C, Dimitroulopoulou S. 2021. Portable air purification: Review of impacts on indoor air quality and health. Science of the Total Environment 766:142585. Demetillo MAG, Navarro A, Knowles KK, Fields KP, Geddes JA, Nowlan CR, Janz SJ, Judd LM, Al-Saadi J, Sun K, and 3 others. 2020. Observing nitrogen dioxide air pollution inequality using high-spatial-resolution remote sensing measurements in Houston, Texas. Environmental Science & Technology 54:9882–95. Grabowski M, Lobo JM, Gunnell B, Enfield K, Carpenter R, Barnes L, Mathers AJ. 2018. Characterizations of handwashing sink activities in a single hospital medical intensive care unit. Hospital Infection 100:e115–22. Green JL. 2014. Can bioinformed design promote healthy indoor ecosystems? Indoor Air 24:113–15. Harvell D. 2004. Ecology and evolution of host-pathogen interactions in nature. American Naturalist 164:S1–5. Hu J, Shuai W, Sumner JT, Moghadam AA, Hartmann EM. 2022. Clinically relevant pathogens on surfaces display differences in survival and transcriptomic response in relation to probiotic and traditional cleaning strategies. bioRxiv:2022.2001.2011.475867. Jones AP. 1999. Indoor air quality and health. Atmospheric Environment 33:4535–64. Lamplugh A, Harries M, Xiang F, Trinh J, Hecobian A, -Montoya LD. 2019. Occupational exposure to volatile organic compounds and health risks in Colorado nail salons. Environmental Pollution 249:518–26. Lamplugh A, Nguyen A, Montoya LD. 2020. Optimization of VOC removal using novel, low-cost sorbent sinks and active flows. Building and Environment 176:106784. Leung DYC. 2015. Outdoor-indoor air pollution in urban environment: Challenges and opportunity. Frontiers in Environmental Science 2:69. Liu Y, Misztal PK, Xiong J, Tian Y, Arata C, Nazaroff WW, Goldstein AH. 2018. Detailed investigation of ventilation rates and airflow patterns in a northern California residence. Indoor Air 28:572–84. Liu Y, Misztal PK, Arata C, Weschler CJ, Nazaroff WW, -Goldstein AH. 2021. Observing ozone chemistry in an occupied residence. Proceedings of the National Academy of Sciences 118(6):e2018140118. Liu S, Wu R, Zhu Y, Wang T, Fang J, Xie Y, Yuan N, Xu H, Song X, Huang W. 2022. The effect of using personal-level indoor air cleaners and respirators on biomarkers of cardio-respiratory health: A systematic review. Environment International 158:106981. Mankiewicz PMS, Ciardullo CAIA, Theodoridis A, Hénaff EP, Dyson A. 2021. Indoor environmental parameters: Considering measures of microbial ecology in the characterization of indoor air quality, pp. 1–13. Atlanta: American Society of Heating, Refrigeration and Air-Conditioning Engineers. Montgomery MA, Elimelech M. 2007. Water and sanitation in developing countries: Including health in the equation. Environmental Science & Technology 41:17–24. Mordor Intelligence. 2022. Organic Personal Care Products Market: Growth, Trends, Covid-19 Impact, and Forecasts (2022–2027). Hyderabad. Murray CJL, Ikuta KS, Sharara F, Swetschinski L, Robles Aguilar G, Gray A, Han C, Bisignano C, Rao P, Wool E, and 130 others. 2022. Global burden of bacterial anti-microbial resistance in 2019: A systematic analysis. The Lancet 399:629–55. NASEM [National Academies of Sciences, Engineering, and Medicine]. 2022. Why Indoor Chemistry Matters. -Washington: National Academies Press. Persily A. 2015. Challenges in developing ventilation and indoor air quality standards: The story of ASHRAE S-tandard 62. Building and Environment 91:61–69. Persily AK, Siegel JA. 2022. Improving ventilation performance in response to the pandemic. The Bridge 52(3):38–41. Piret J, Boivin G. 2020. Pandemics throughout history. -Frontiers in Microbiology 11:631736. Piscitelli P, Miani A, Setti L, De Gennaro G, Rodo X, -Artinano B, Vara E, Rancan L, Arias J, Passarini F, and 16 others. 2022. The role of outdoor and indoor air quality in the spread of SARS-CoV-2: Overview and recommendations by the research group on COVID-19 and particulate matter (RESCOP commission). Environmental Research 211:113038. Prussin AJ 2nd, Marr LC. 2015. Sources of airborne micro-organisms in the built environment. Microbiome 3:78. Tulchinsky TH. 2018. Case Studies in Public Health. -Cambridge MA: Academic Press. Van Horne YO, Alcala CS, Peltier RE, Quintana PJE, Seto E, Gonzales M, Johnston JE, Montoya LD, Quiros-Alcala L, Beamer PI. 2022. An applied environmental justice framework for exposure science. Exposure Science & Environmental Epidemiology. van Schaik W. 2022. Baas Becking meets One Health. Nature Microbiology 7:482–83. Velazquez S, Griffiths W, Dietz L, Horve P, Nunez S, Hu JL, Shen JX, Fretz M, Bi CY, Xu Y, and 3 others. 2019. From one species to another: A review on the interaction between chemistry and microbiology in relation to cleaning in the built environment. Indoor Air 29:880–94. Wang Z, Kowal SF, Carslaw N, Kahan TF. 2020. Photolysis-driven indoor air chemistry following cleaning of hospital wards. Indoor Air 30:1241–55. Zellmer C, Blakney R, Van Hoof S, Safdar N. 2015. Impact of sink location on hand hygiene compliance for Clostridium difficile infection. American Journal of Infection Control 43:387–89. Zhang Y, Mo J, Li Y, Sundell J, Wargocki P, Zhang J, Little JC, Corsi R, Deng Q, Leung MHK, and 4 others. 2011. Can commonly-used fan-driven air cleaning technologies improve indoor air quality? A literature review. Atmospheric Environment 45:4329–43.  Spillover occurs when there is close contact between humans and nonhuman hosts. About the Author:Erica Hartmann is an associate professor, Department of Civil and Environmental Engineering, Northwestern University.