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. Issue Editors' Note: Microbial Challenges in the Built Environment Tuesday, September 20, 2022 Author: Charles Haas and Vivian Loftness On average, individuals spend 87 percent of their time indoors (Klepeis et al. 2001). Therefore, human exposures in this environment need to be characterized to determine where, how, and how much intervention is needed to reduce risks. While the focus here is on microbial exposure, indoor exposure to chemicals (Li et al. 2019), including secondary organics produced by indoor reaction (Yang and Waring 2016) and radioactive isotopes (e.g., radon) (Field et al. 2006), is also important. There is a long history of reported adverse health effects associated with microorganisms or their metabolites in the indoor environment (Nag 2019). Yet over the past decade—starting well before the SARS-CoV-2 outbreak in late 2019—there has been an explosion of scholarship with respect to the indoor microbiome (figure 1). There is clear evidence for adverse effects of diverse microbial pathogens in the indoor environment (table 1). Human exposure can result from either inhalation or fomites (i.e., individuals touching contaminated surfaces and then transferring pathogens to the nose, mouth, or eyes). These pathogens include human corona-viruses such as SARS (severe acute respiratory syndrome) and MERS (Middle East respiratory syndrome). National Academies Consensus Report In 2017 a committee of the National Academies of Sciences, Engineering, and Medicine produced a consensus report summarizing the state of knowledge of the microbiome of the indoor environment and identifying research needs (NASEM 2017). It was recognized that the indoor environment represents a highly coupled ecosystem of human and other inhabitants (including animals, pets, and insects), engineered building systems, and microbial communities (figure 2). In addition to pathogens, noninfectious diseases or syndromes, some of which may be mediated by microbial metabolites or fragments from organisms whose growth is promoted by permissive conditions (e.g., humidity or temperature) in buildings, are of concern. The committee found strong evidence of association among the follow-ing (although mechanisms are mostly not certain): upper respiratory tract symptoms wheezing coughing shortness of breath development of asthma exacerbation of asthma hypersensitivity pneumonitis. The dynamics of the indoor microbiome are influenced by complex processes, both intrinsic to a building and due to exchanges with external environments, as illustrated in figure 3. Not shown in this figure are important sources of pathogens resulting from aerosolization of any water from indoor sources such as humidifiers (Tyndall et al. 1995) and showers (Hamilton et al. 2019). The 2017 committee identified 12 priority research areas under the following five themes: Characterize interrelationships among microbial communities and built environment systems of air, water, surfaces, and occupants. Assess the influences of the built environment and indoor microbial exposures on the composition and function of the human microbiome, on human functional responses, and on human health outcomes. Explore nonhealth impacts of interventions to manipulate microbial communities. Advance the tools and research infrastructure for addressing microbiome–built environment questions. Translate research into practice. Significance in Light of Covid-19 The covid-19 pandemic and consideration of means of transmission have increased attention to the role of the indoor environment in disease transmission. The provision of clean water and adequate sanitation is recognized as one of the greatest 20th century engineering advances (Constable and Somerville 2003). In light of the pandemic, it has been argued that improvement in indoor air quality is now an urgent engineering need for the control of respiratory infectious diseases (Morawska et al. 2021). For SARS-CoV-2, the aerosol route of transmission may be the dominant (Tellier 2022)—though not exclusive (Kraay et al. 2021)—one. Recognition of the importance of this route for covid-19 transmission was initially handicapped by a misunderstanding of how suspended particles behave in the indoor environment (Randall et al. 2021). However, for other organisms, fomite or droplet routes may be more significant (Kraay et al. 2018), so the control of fomite risks from touched surfaces cannot be neglected. In This Issue The aim of this issue is to outline problems associated with the microbiome in the built environment and to review approaches to address them, toward enhanced design, engineering, and operation of more healthful indoor air in the future. Stating the Problems The first several articles state the problems. Brent Stephens, Kyle Bibby, and Karen Dannemiller begin by discussing the impacts of covid-19 on understanding microbial and viral exposures in the built environment. They introduce strategies for measuring viral disease prevalence in wastewater, building dust, air, and on surfaces, and call for the expansion of both random population and individual testing, while recognizing associated costs, inconvenience, and differing data resolution requirements, among other factors. Erica Hartmann then looks at engineering and design factors as well as the role of urban development in healthful built environments. There are important considerations in the possible benefits of outdoor versus indoor air; effective filtration and correct use of cleaning products are relevant, as are impacts on energy use and cost. The creation of healthful built environments requires mindful attention to design, maintenance, energy demands, and equity. The third article, “Estimating Indoor Microbial Risks as Applied to Covid-19,” presents the application of quantitative microbial risk assessment (QMRA) as an invaluable approach to hazard identification, dose response, exposure assessment, and risk characterization of respiratory pathogens. Advances are needed to better account for population heterogeneity and incorporate dose-response models in disease transmission models. Exploring Solutions The next series of articles consider solutions to microbial challenges in the built environment. Active air interventions are discussed by Jelena Srebric and Don Milton as “an important mechanism for reducing risks of [airborne] infection transmission.” The authors explain the utility and challenges of ventilation, filtration (including portable devices), and germicidal ultraviolet light. They also call for “significant investment” to develop and test technologies, standards and certification for them, research to better understand the link between interventions and health outcomes, and policies that support improved residential ventilation. Andrew Persily and Jeffrey Siegel highlight standards and actions to improve ventilation performance, which is as critical as handwashing, face masks, vaccination, and distancing. They point out the need to “recognize the large amount of variation between buildings and their ventilation systems, which directly relate to what can and should be done in a given building.” The authors also cite the utility of CO2 monitoring, operations and maintenance, and the need for research to inform updated standards. Hooman Parhizkar, Alen Mahic´, and Kevin Van Den Wymelenberg affirm the importance of ventilation standards and HVAC operating scenarios to control disease transmission risk. They used a reference building for their risk-energy decision support platform to calculate risk of disease transmission taking into account current ventilation standards, air exchange rates, relative humidity values, and associated energy consumption. Looking ahead, they write that “Future energy codes, ventilation standards, and HVAC system operational and maintenance guidelines would all benefit from a concurrent understanding of how key indoor air variables implicate annual energy use and airborne disease transmission risks.” The built environment includes water-related structures, whose water-generated microbiomes can affect public health. Kerry Hamilton and Timothy Bartrand present an extensive and detailed table, ordered by level of public health risk, of microenvironment-associated water microbiomes—from medical devices to cooling towers, showerheads, fountains, pools and hot tubs, and ice machines, among others. For each they summarize primary exposure routes, public health significance, data and knowledge gaps, and best practices in management, with relevant citations throughout. In an article titled “Microbial Surface Transmission in the Built Environment and Management Methods,” Amanda Wilson, Diane Gold, and Paloma Beamer discuss fomite transmission of respiratory and other pathogens (including C. difficile and Staphylococcus). They acknowledge the role of human behavior not only in pathogen transmission but also in an over-zealous approach to surface cleaning that “leads to fewer interactions…with…nonharmful microorganisms that aid in immune system development.” Infection control methods should protect nonharmful microorganisms, encourage proper use of cleaning chemicals, and prioritize layered engineering strategies (e.g., proper ventilation and air filtration, use of UV light). Building on the topic of beneficial microorganisms, Megan Thoemmes, Sarah Allard, and Jack Gilbert distinguish between “pets and pests,” and caution that “People now come into contact with a smaller subset of diverse organisms that are important not only for immune development but also for the reduction of pathogen abundance indoors.” They envision “a future where microbial biocontrol can be engineered into building materials…to provide surfaces that both actively reduce the emergence and persistence of dangerous pathogens and create immune-activating exposure to decrease the incidence of chronic immune disease.” Looking Ahead The pandemic highlighted significant inequities in microbial exposure and health, and to prepare for future public health challenges, responsible engineering practice requires consideration of these as much as standards, ventilation performance, filtration, and -other engineering approaches. Diane Gold, Tyra B-ryant--Stephens, Elizabeth Matsui, and Lee Ann Kahlor review the specific problems due to covid-19—such as amplified poverty, housing instability, more crowding (as individuals lost jobs or their own homes and moved in with extended family)—and their role in increased respiratory infection incidence, morbidity, and mortality. Given the historical practices that created the present-day state of US housing and neighborhoods, the authors call for systemic changes as well as community engagement, respectful research -methods, more effective risk communication, and improved housing quality. In the final article, Robert Dunn and Megan Thoemmes explain humans’ unconscious and conscious awareness of microbes. The former is represented in “the extraordinary sophistication” of the immune system; the latter is comparatively recent and lacks the capacity to distinguish between harmful and beneficial microbes. Loss of exposure to the latter is associated with problems of gut health, skin health, and even mental health. Their point is that “in the long term people need to understand how to manage the microbiomes of daily life in more sophisticated ways to favor beneficial species, ignore benign species, and strategically target problem species.” Conclusion This timely issue of The Bridge conveys some of the breadth of the challenges and potential solutions to microbiomes in the built environment. It is also clear that much is still to be learned. Advances in the application of tools of molecular biology to the indoor microbiome (Gilbert and Stephens 2018) will enhance understanding of the fate, transport, proliferation, and impacts of microorganisms indoors and the role of exchanges with outdoor environments. Based on such knowledge and the incorporation of risk assessment, engineering interventions for risk reduction can be better designed. The covid-19 pandemic has been a wake-up call to the engineering community and society. The articles in these pages illustrate some paths forward to better prepare for future such challenges. To design, construct, operate, and maintain more healthful buildings, a multidisciplinary program of fundamental, applied, and translational research is necessary, and it should involve federal, local, and nongovernmental funding sources to address the challenges posed in this issue. Acknowledgments We appreciate the time and effort of the following experts enlisted to evaluate the articles in this issue: Gary Adamkiewicz, Elizabeth Anderson, Bill Bahnfleth, Heather Bischel, Nadine Borduas-Dedekind, Jonathan Burkhardt, José Guillermo Cedeño Laurent, David Coil, Richard Corsi, Peter DeCarlo, Curtis Donskey, Tim Julian, Sarah Kantrowitz, Scott Kelley, Kerry -Kinney, Mark LeChevallier, Ken Martinez, Pawel Misztal, Keeve Nachman, William Nazaroff, Paula Olsiewski, Jordan Peccia, Michael Poulsen, Caitlin Proctor, and Pawel Wargocki. And we are most grateful for the extraordinary efforts of Managing Editor Cameron Fletcher in working with us to assemble this issue. References Constable G, Somerville B. 2003. A Century of Innovation: Twenty Engineering Achievements That Transformed Our Lives. Washington: Joseph Henry Press. Field RW, Krewski D, Lubin JH, Zielinski JM, Alavanja M, Catalan VS, Klotz JB, Létourneau EG, Lynch CF, Lyon JL, and 6 others. 2006. An overview of the North American residential radon and lung cancer case-control studies. Toxicology and Environmental Health A 69(7):599–631. Gilbert JA, Stephens B. 2018. Microbiology of the built environment. Nature Reviews Microbiology 16:661–70. Hamilton KA, Hamilton MT, Johnson W, Jjemba P, Bukhari Z, LeChevallier M, Haas CN, Gurian PL. 2019. Risk-based critical concentrations of Legionella pneumophila for indoor residential water uses. Environmental Science & Technology 53(8):4528–41. Klepeis NE, Nelson WC, Ott WR, Robinson JP, Tsang AM, Switzer P, Behar JV, Hern SC, Engelmann WH. 2001. The National Human Activity Pattern Survey (NHAPS): A resource for assessing exposure to environmental pollutants. Exposure Science & Environmental Epidemiology 11(3):231–52. Kraay ANM, Hayashi MAL, Berendes DM, Sobolik JS, Leon JS, Lopman BA. 2021. Risk for fomite-mediated transmission of SARS-CoV-2 in child daycares, schools, nursing homes, and offices. Emerging Infectious Diseases 27(4):1229–31. Kraay ANM, Hayashi MAL, Hernandez-Ceron N, Spicknall IH, Eisenberg MC, Meza R, Eisenberg JNS. 2018. Fomite-mediated transmission as a sufficient pathway: A comparative analysis across three viral pathogens. BMC Infectious Diseases 18(1):540. Li L, Arnot JA, Wania F. 2019. How are humans exposed to organic chemicals released to indoor air? Environmental Science & Technology 53(19):11276–84. Morawska L, Allen J, Bahnfleth W, Bluyssen PM, Boerstra A, Buonanno G, Cao J, Dancer SJ, Floto A, Franchimon F, and 29 others. 2021. A paradigm shift to combat indoor respiratory infection. Science 372(6543):689–91. Nag PK. 2019. Sick building syndrome and other building-related illnesses. In: Nag PK, Office Buildings: Health, Safety, and Environment, pp. 53–103. Springer Nature Singapore. NASEM [National Academies of Science, Engineering, and Medicine]. 2017. Microbiomes of the Built Environment: A Research Agenda for Indoor Microbiology, Human Health, and Buildings. Washington: National Academies Press. Randall K, Ewing ET, Marr LC, Jimenez JL, Bourouiba L. 2021. How did we get here: What are droplets and aerosols and how far do they go? A historical perspective on the transmission of respiratory infectious diseases. Interface Focus 11:10. Tellier R. 2022. COVID-19: The case for aerosol transmission. Interface Focus 12(2):20210072. Tyndall RL, Lehman ES, Bowman EK, Milton DK, Barbaree JM. 1995. Home humidifiers as a potential source of exposure to microbial pathogens, endotoxins, and allergens. Indoor Air 5(3):171–78. Yang Y, Waring MS. 2016. Secondary organic aerosol formation initiated by a-terpineol ozonolysis in indoor air. Indoor Air 26(6):939–52.  We were members of the committee, as were the following contributors to this issue: Jack Gilbert, Diane Gold, and Andrew Persily.  There were other outcomes for which insufficient or inconsistent evidence was available. About the Author:Charles Haas (NAE) is the LD Betz Professor of Environmental Engineering, Drexel University. Vivian Loftness is Paul Mellon University Professor of Architecture, Carnegie Mellon University.