Summary¹

People’s desire to understand the environments in which they live is a natural one. People spend most of their time in spaces and structures designed, built, and managed by humans, and it is estimated that people in developed countries now spend 90 percent of their lives indoors. As people move from homes to workplaces, traveling in cars and on transit systems, microorganisms are continually with and around them. These microorganisms reside outdoors in soil and water and coexist indoors where people live and work. They are found in and on pets, plants, and rodents; in water; in dirt tracked indoors on shoes; and in the air that enters buildings. Microorganisms also live on human skin and in systems such as the digestive tract, and the human-associated microbes that are shed, along with the human behaviors that affect their transport and removal, make significant contributions to the diversity of the indoor microbiome. What microorganisms are people exposed to in these indoor settings? What factors control their abundance, diversity, persistence, and other community characteristics? What effects could these organisms have on the health of human occupants and on such other factors as degradation of building materials?

The characteristics of “healthy” indoor environments cannot yet be defined, nor do microbial, clinical, and building researchers yet understand how to modify features of indoor environments—such as building ventilation systems and the chemistry of building materials—in ways that would have predictable impacts on microbial communities to promote health and

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¹ This Summary does not include references. Citations for the findings presented in this Summary appear in subsequent chapters of the report.

prevent disease. The factors that affect the environments within buildings, the ways in which building characteristics influence the composition and function of indoor microbial communities, and the ways in which these microbial communities relate to human health and well-being are extraordinarily complex and can be explored only as a dynamic, interconnected ecosystem by engaging the fields of microbial biology and ecology, chemistry, building science,² and human physiology.

This Consensus Study Report reviews both what is known about the intersection of these disciplines and how new tools may facilitate advances in understanding the ecosystem of built environments, indoor microbiomes, and effects on human health and well-being. The report provides a vision of a future in which indoor microbial communities are better understood, and built environments can be designed and operated to improve human health. To advance this vision, the report offers a research agenda to generate the information needed so that stakeholders with an interest in understanding the impacts of built environments will be able to make more informed decisions.³ The key terms used in the report are defined in Box S-1.

EFFECTS OF INDOOR MICROORGANISMS ON HUMAN HEALTH

More is understood about transmission of infectious microorganisms than about noninfectious health impacts. Concern about diseases spreading from person to person inside buildings and in enclosed spaces is longstanding, and the increasing prevalence of hospital-associated infections further motivates the desire to understand how humans are exposed to disease-causing microorganisms and how the microbial agents associated with infection and disease move through, live, evolve, and die within a building. It is well established that humans can become sick after being exposed to infectious microorganisms indoors (e.g., live virus on a doorknob or in the air, or bacteria such as Legionella in water systems), although variations in human responses are common: microbial exposures may cause adverse health effects in one person while having minor or no effects in another.

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² The report uses the term “building science” to refer to the field of knowledge that focuses on understanding physical and operational aspects of buildings and building systems and the impacts on performance; the term “building scientist” is used to refer to a broad range of integrated technical disciplines, including scientists, engineers, and architects who study this area.

³ The study was sponsored by the Alfred P. Sloan Foundation, the National Aeronautics and Space Administration, the National Institutes of Health, and the U.S. Environmental Protection Agency, which asked the National Academies of Sciences, Engineering, and Medicine to convene a committee to address these multidimensional issues. In addition, the Gordon and Betty Moore Foundation supported travel awards for one of the committee’s data-gathering workshops.

Microorganisms that are living and active in an indoor setting can also produce metabolites that may impact health. Metabolites of gut bacteria have been more well-characterized than those of indoor environmental bacteria or fungi, and further characterization of those metabolites and their influence on health will be needed. Exposure to a “dead” microbe or its component pieces, such as proteins and cell wall components of bacteria or fungi, also may cause irritant and allergic or nonallergic immune responses. Furthermore, humans participate with the indoor microbiome in a cycle of exposure, uptake, and shedding, interactions that can impact human health in myriad ways that remain imperfectly understood.

On the other hand, certain microorganisms, microbial compounds, and microbial communities are associated with beneficial health effects in ways that researchers are working to elucidate. Studies of exposure to “farm-type” microbiomes suggest, for instance, that children who grow up on farms in contact with livestock have a lower risk of developing asthma. Likewise, in urban U.S. settings, some studies suggest that exposure to dogs

or to certain microbes early in life may protect against later allergic disease. Current research is investigating how these early-life microbial exposures correlate with subsequent health outcomes. Another line of investigation involves examining whether microorganisms in the built environment influence the populations of microorganisms on and in humans, such as on skin or in the gastrointestinal tract, and correlating such microbiome–microbiome interactions with health impacts. The difficulty of disentangling these pathways is compounded by the role of additional factors that can influence health and human behavior.

Questions remain as to whether favorable health outcomes are due to exposures to specific microbes, exposures to a greater diversity of microbes, the stages of life at which exposures occur, or other factors. Nor, beyond general advantages of moisture management and other practices, do researchers understand how characteristics of the built environment contribute to these favorable relationships. Nonetheless, advancing knowledge raises the possibility that future interventions to affect microbial communities in the built environment might be used both to reduce the risk of unfavorable outcomes and to promote beneficial or healthful outcomes. To develop effective interventions, researchers will need not only to define pathways that are relevant to human health but also to elucidate their mechanisms of action. Current findings provide a foundation for future directions in research that can yield this knowledge.

OTHER EFFECTS OF MICROORGANISMS

Interest in studying indoor microbial environments is also spurred by the desire to optimize energy performance and incorporate “green design” features into buildings while ensuring that the buildings maintain occupants’ comfort and health. Managing microorganisms indoors may reduce biodegradation of building materials and finishes or reduce biofilm fouling to minimize energy losses. Achieving these objectives entails trade-offs. Increasing the temperature of water in building water heaters and pipes to a level that impedes growth of microorganisms can result in higher energy costs and an increased risk of scalding, or it may have limited effectiveness in inactivating certain microbes. Increased flow of outdoor air into buildings has been linked to occupant health and comfort and can promote exposure to a greater diversity of microorganisms, but it increases the energy consumption for building heating and cooling. Greater outdoor air ventilation also may increase occupants’ exposure to allergens or other pollutants of outdoor origin. A better understanding of building design and use will yield a fuller understanding of the interplay among buildings, microbes, and humans.

RELATIONSHIP OF BUILDING CHARACTERISTICS TO INDOOR MICROBIAL COMMUNITIES

The composition and viability of indoor microbial communities are determined largely by characteristics of the buildings they inhabit, including the availability of water and nutrients for growth and survival; the buildings’ occupants; and the external environment. These relationships affect microbial transport and removal and influence the formation and composition of indoor microbial reservoirs in air and water and on surfaces.

Air can enter buildings as a result of natural ventilation, such as through open windows; mechanical ventilation, such as through a heating, ventilation, and air conditioning (HVAC) system; or leakage into a building through uncontrolled infiltration through the building’s envelope. When air enters buildings in a controlled manner via designed natural and mechanical ventilation systems, it can be filtered to remove particles of various sizes. A number of microorganisms fall into size ranges that can be captured by air filtration systems currently used in buildings, affecting the degree to which indoor microbial composition mimics or differs from that of the outdoor environment. However, the most commonly used filtration systems do not remove all microorganisms, nor do they remove gaseous contaminants, including the metabolic products from some microbes. Moreover, not only do microbes enter buildings through ventilation systems; these systems can also serve as microbial reservoirs, in part as a result of the presence of condensation. How HVAC systems are operated and maintained, the proportions of air drawn from outdoors or recirculated from occupied spaces, and whether systems include mechanisms to remove moisture all link the properties of HVAC systems with effects on indoor microbial communities.

Water systems serve as microbial reservoirs, and the development of microbial communities is affected by the composition of water piped into a building, as well as leaks, condensation, and the existence of other moisture sources. Although a building may appear to be dry, isolated locations of moisture can support microbial growth and activity. Microbes also may persist under arid conditions—for example, as spores.

Human behaviors contribute to how water impacts the indoor microbiome. Such practices as water temperature selection, occupant control of thermostats, whether toilets are flushed with the lid open or closed, and how indoor humidity levels are controlled can influence the development and maintenance of microbial communities. Moisture from the air that becomes adsorbed onto building surfaces or absorbed into materials can be an important anchor for indoor microbial communities, as can the availability of nutrients. It is also important to note that the role of humans in built environments varies. In addition to widely differing ages, health status, occupant density, and behaviors that facilitate or impede the trans-

port and resuspension of indoor microorganisms, different occupants (e.g., homeowners versus renters; facilities managers versus office workers) vary in their ability to control or maintain features of the built environment.

TOOLS THAT FACILITATE ANALYSIS

To make targeted changes in built environments that positively impact microbial communities, building designers and managers and material scientists will need robust data on the relationships among the multiple factors relevant to microbiomes in the built environment. As noted, the existing base of research is starting to provide information that connects building characteristics with the composition and function of indoor microbial communities, while ongoing research is exploring associations with health and other outcomes. To move from research to application, it will be necessary to determine more fully the public health relevance of the relationships among built environments, indoor microbiomes, and humans, as well as how to demonstrate causal relationships in a clinically relevant framework. Although better quantitative information on microbial exposures is likely to be part of this framework, efforts to expand this knowledge face a number of technical and practical challenges.

Studies on the impacts associated with indoor microbiomes will need to use a variety of tools and data collection strategies to capture the dynamics involved. These tools include sensors to measure and monitor such building characteristics as temperature, moisture, and airflow. Identification tools for characterizing which microorganisms are in a sample collected from a given built environment (e.g., a sample taken from an air filtration system, a showerhead, or a carpet) need to be coupled to those that describe microbial functions (e.g., cellulose degradation, mycotoxin production, antibiotic production, production of immunosuppressants, or biofilm formation). Growing microbial samples in culture remains one technique for understanding whether the organisms collected in a building are viable. Since relatively few microorganisms can be cultured, “omics” technologies, including genomics, proteomics, and metabolomics,⁴ have become increasingly important tools for moving research forward by providing a means to assess the composition, structure, and function of microbial communities. The detection of microbial products such as volatiles, toxins, or other microbial metabolites also may yield markers to provide exposure and

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⁴ Metagenomics is the study of the collections of genes present in a sample, which can be used to help identify the particular microorganisms a sample contains. Proteomics (measurement of the collection of proteins) and metabolomics (measurement of the collection of chemical metabolites) yield information on what the microorganisms were doing when the sample was collected and thus help provide a snapshot of the microorganisms’ activity.

outcome data, although further development of techniques for measuring indoor microbial metabolites and development of biomarkers of human exposure will be important.

Despite the advantages these tools provide for characterizing microbial communities, persistent challenges hinder progress in understanding the interconnections among buildings, microorganisms, and health. When applied to built environment samples, sufficiently deep metagenomics sequencing is required to obtain resolution of community composition and abundance⁵ at the species level, and many published reports provide less precise resolution. Advances in other “omics” areas, including the research infrastructure for sharing and analyzing data, are needed to provide fuller information on microbial activities within sampled communities. In addition, improved quantitative data on human exposures to microbes and evidence connecting indoor microbial activity to effects in humans will be needed to strengthen links between exposures and clinically relevant health outcomes. Scientists also need to be aware of the effects of sample collection and handling on downstream data and on the assumptions and limitations associated with the analytic methods that underpin “omics” tools. These tools rely on statistical methods to make sense of large amounts of data. For example, data from metagenomic analysis of a sample are in the form of many pieces of DNA from many different organisms, both living and dead. To assign the organisms in the sample to specific taxonomic groups requires comparing these pieces of DNA with databases to identify their similarities to reference genomes associated with specific microbial species. Researchers also may lack sufficient cultured representatives. Different theoretical assumptions can be made about how best to cluster these pieces of DNA into taxonomic units, which in turn can affect the microbial groups that are identified as being present. Understanding the assumptions associated with “omics” tools and improving ways to compare or standardize the results they produce would enable better comparisons across studies conducted by different groups.

There are additional challenges to facilitating cross-study comparisons. The research community has identified the need for a core set of building, environment, and occupant data to collect when studying indoor microbiomes; however, these elements (and the level of detail required) are not yet fully defined or agreed upon. Further work is needed on how to achieve a reasonable balance between collecting sufficiently detailed information and

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⁵ Relative abundance of a microorganism in a sample refers to the percentage of that type of microorganism that was identified compared with the total microorganisms identified in that sample. Absolute abundance, on the other hand, reflects the actual number of that microorganism that was in the substrate (surface, air, water, or bulk material) in the built environment from which the sample was collected. Several technical challenges arise in obtaining such data from samples.

the time and cost involved. The absence of a core of best practices and standardized dataset parameters creates challenges for comparing results across studies. The ability to draw larger conclusions will require multidisciplinary collaborations and consensus.

MOVING TOWARD PRACTICAL APPLICATION

An important aspect of this report is its emphasis on how future interventions in built environments may someday be able to change indoor microbiomes in ways that promote health, and on what practical steps can be taken to generate the data needed to support the development, assessment, and eventual implementation of these interventions. Relevant types of interventions include those focused on changes to characteristics of buildings, such as ventilation rates, air and water filtration efficiencies, and maintenance schedules. Other potential interventions need to take into account the effects of chemicals in indoor cleaning products, how human behaviors affect the use and effectiveness of such chemicals (e.g., cleaning frequency and methods), and the design and use of existing and novel building materials (e.g., materials designed to have antimicrobial properties).

One way in which scientists are trying to understand these complex relationships is by applying models that represent inputs and outflows of building environment and microbiological systems and that capture the relationships among these components; models that can help predict the effects when one or more factors are changed and generate information to inform the development of future interventions. One example is models of building airflow and contaminant dispersion, which can provide insight into how interventions are likely to impact microbial concentrations and transport in a building. Box S-2 lists knowledge gaps that need to be filled to support such efforts to move from research to practical application.

New data connecting the built environment, microbial communities, and human health could help inform building science and public health decision making. Nevertheless, it is important to remember that policy decisions will not be made in a vacuum. Given the data generated by future research, policy makers and others are likely to take into account additional considerations, including the economic and noneconomic costs of potential interventions, such as the burden of microbial illnesses, energy costs, and the possibility of unintended health effects. Models for designing and assessing built environment interventions will need to incorporate these important dimensions.

Additional challenges may also be associated with built environment interventions, health effects, or access for those in substandard housing who are of lower socioeconomic status. For example, people of low socioeconomic status, relative to those who are better off, may lack access to

information about the interactions between microbes and the built environment and may have more limited ability to make changes to their built environments, even when such guidance is available. A number of key dimensions, currently understudied, need to be informed by the social and behavioral sciences, such as effective communication about the results of scientific research on indoor environments; guidance in such areas as cleaning and maintenance practices; strategies for engaging with relevant sectors of the public, including owners, occupants, facilities managers, and others; and efforts to foster behavior changes where appropriate.

VISION FOR THE FUTURE: MICROBIOME-INFORMED BUILT ENVIRONMENTS

The built environment interacts with the indoor microbiome in multiple ways that impact humans. Microbial exchange between indoors and outdoors, microbial growth and persistence in indoor settings, and human exposures to indoor microbial communities are affected by building design, operation, and maintenance. Research that focuses only on one microbe, on a specific aspect of building design, or on a single human health outcome will not be sufficient to understand these multifactorial relationships. As noted earlier, integrating approaches from multiple disciplines and bodies of knowledge is essential to improve understanding of these relationships and apply the knowledge gleaned. In general, improved understanding of indoor environments holds promise that in the future, buildings can support a more productive, healthier population.

In this report’s vision, future built environments will be informed by improved knowledge about the indoor microbiome. Researchers and building practitioners will have reached a deeper understanding of the effects of indoor microbial communities on human health. Detailed information about the growth, establishment, and evolution of indoor microbiomes and how these microbial communities relate to building characteristics, as well as greater insight into human exposures and responses, will be known.

New technologies will support building operation and maintenance. Examples include sensors to detect water penetration, filtration performance, occupant density, and air quality. Some of these technologies will require further development, while others are currently on the market but are not widely used in practice. Increased utilization of sensing and monitoring technologies can be coupled with a fuller understanding of microbial and environmental connections between the indoors and outdoors and what benefits these connections may provide. Where appropriate, this understanding can be incorporated into building design and operation. It may be hoped that a more purposeful approach to managing buildings and their microbiomes reflected in this vision for the future will result in building

occupants who are more informed about and engaged in improving their indoor environments.

RESEARCH AGENDA

Gaining sufficient understanding of the relationships among microbial, physical, chemical, and human elements that contribute to the built environment and translating this knowledge into improved building design and operation is a long-term goal that will not be achieved quickly or easily. Its accomplishment will likely require partnerships among federal agencies, public entities, and private corporations. Steps that would fill the knowledge gaps identified in Box S-2 and advance progress toward this ultimate goal are reflected in the research agenda presented in Box S-3. The priorities the committee recommends for inclusion in this agenda build on current research, as well as on the questions and potential research directions presented throughout the report. They highlight steps that can be taken in generating the knowledge necessary to fully understand how microbiomes in built environments impact human health and what can be done to ensure that buildings and their occupants are, and remain, healthy into the future.

This research agenda reflects a need for significant additional research and tool and infrastructure development to sustain this field; will require time and support to accomplish; and is broad enough that many partners will need to be involved. Agencies such as the National Institute of Standards and Technology (NIST), the National Institutes of Health (NIH), the National Science Foundation (NSF), the U.S. Department of Energy (DOE), and the U.S. Environmental Protection Agency (EPA) can support, develop, and implement the foundational tools, data, and standards needed to support the field. Given the many types of built environments, occupants, and impacts, agencies including EPA, the General Services Administration (GSA), NIH, the U.S. Centers for Disease Control and Prevention (CDC), the U.S. Department of Defense (DOD), the U.S. Department of Housing and Urban Development (HUD), the U.S. Department of Veterans Affairs (VA), and others may pursue their own interests in exploring microbiome–built environment interactions—for example, health in public housing or in military facilities, vehicles, ships, and submarines. Specialized resources available to such agencies as the National Aeronautics and Space Administration (NASA), including the International Space Station, can provide laboratories in which to test hypotheses, given the close control over environmental features of these resources and the tradition of using such resources as experimental stations. Communities of practice, such as in the indoor air quality and HVAC fields, can follow these developments as they move closer to practical application. Further engagement of such disciplines as materials science and the social and behavioral sciences

can result in significant contributions to these efforts. The integration of expertise across these many communities will be critical to achieving the vision of microbiome-informed design, operation, and maintenance of built environments.