U.S. flag

An official website of the United States government

NCBI Bookshelf. A service of the National Library of Medicine, National Institutes of Health.

Cover of FAQ: Microbiology of Built Environments

FAQ: Microbiology of Built Environments

Report on an American Academy of Microbiology Colloquium held in Washington, DC, in September 2015

, Ph.D.

Author Information and Affiliations
Washington (DC): American Society for Microbiology; .

ABSTRACT

Built environments are the structures that humans create to shelter from the outdoors and provide spaces for living, working, playing, and getting places. Along with humans, pets, pests, and house plants, built environments house a range of microbes. Preliminary studies indicate that indoor spaces have distinct microbial communities, influenced by building materials, ventilation and airflow, moisture, and human and animal activity. The Academy convened a colloquium on September 9, 2015 to examine the role of complex microbial ecosystems found in built environments, including their effects on building chemistry and human health. Studying the microbiology of built environments can change the ways we design, build, operate, occupy, and clean our indoor spaces.

Front Matter

The American Academy of Microbiology (Academy) is the honorific branch of the American Society for Microbiology (ASM), a non-profit scientific society with nearly 40,000 members. Fellows of the Academy have been elected by their peers in recognition of their outstanding contributions to the microbial sciences. Through its colloquia program, the Academy draws on the expertise of these fellows to address critical issues in the microbial sciences.

This report is based on the deliberations of experts who gathered for a full day to discuss a series of questions developed by the steering committee regarding the role of complex microbial ecosystems found in built environments. This report has been reviewed by all participants, and every effort has been made to ensure that the information is accurate and complete. The contents reflect the views of the participants and are not intended to reflect official positions of the Academy or ASM.

The Academy acknowledges Karen MacKavanagh for her assistance in editing this report. Additionally the Academy thanks Chelsie Geyer, Ph.D. for her assistance on this project.

Contents of the report may be distributed further so long as the authorship of the Academy is acknowledged and this disclaimer is included.

BOARD OF GOVERNORS, AMERICAN ACADEMY OF MICROBIOLOGY

Michele S. Swanson, Ph.D., Chair University of Michigan

Martin J. Blaser, M.D. New York University

Donald A. Bryant, Ph.D. Pennsylvania State University

Nancy Craig, Ph.D. John Hopkins University

Terence Dermody, M.D. Vanderbilt University

Stan Fields, Ph.D. University of Washington

Gerry Fink, Ph.D. Massachusetts Institute of Technology

James M. Hughes, M.D. Emory University

Steven Lindow, Ph.D. University of California, Berkeley

Margaret McFall-Ngai, Ph.D. University of Wisconsin-Madison

Mary Ann Moran, Ph.D. University of Georgia

Graham C. Walker, Ph.D. Massachusetts Institute of Technology

COLLOQUIUM STEERING COMMITTEE

Joan W. Bennett, Ph.D., Chair Rutgers University

Paula Olsiewski, Ph.D. Alfred P. Sloan Foundation

Lutgarde Raskin, Ph.D. University of Michigan

PARTICIPANTS

Martin J. Blaser, M.D. New York University

Maria Gloria Dominguez-Bello, Ph.D. New York University

Jack Gilbert, Ph.D. University of Chicago, Argonne National Laboratory

Vincent Hill, Ph.D. U.S. Centers for Disease Control and Prevention

Vito Ilacqua, Ph.D. U.S. Environmental Protection Agency

Bruce Hamilton, Ph.D. National Science Foundation

Elliott Horner, PhD UL Environment

Jeff Kline University of Oregon

Shelly Miller, Ph.D. University of Colorado, Boulder

Edward Nardell, M.D. Harvard School of Public Health

Aino Nevalainen, Ph.D. National Institute for Health and Welfare, Finland

Gary Roselle, M.D. Cincinnati Veteran Affairs Medical Center

Michael Schmidt, Ph.D. Medical University of South Carolina

Julie Segre, Ph.D. National Institutes of Health

Jeffrey Siegel, Ph.D. University of Toronto

Michele S. Swanson, Ph.D. University of Michigan

John Taylor, Ph.D. University of California, Berkeley

ACADEMY STAFF

Marina Moses, MS, DrPH Director

Virginia Dolen Program Manager

Daniel Peniston Colloquium and Public Outreach Program Assistant

1. What are built environments and why are these ecosystems important to study?

Built environments are central to our daily lives. Found in areas ranging from rural to urban, they are the structures that humans create to shelter from the outdoors and provide spaces for living, working, playing, and getting places. They are our homes, offices, schools, hospitals, long-term care and specialized nursing facilities, commercial and retail establishments, airplanes, trains, buses, and subway stations, our cars, and even the space station—indoor spaces designed with different forms, functions, and organization to host particular human needs.

Box Icon

Box

Key terms used throughout text.

These spaces are far from inanimate. Humans, pets, pests, and house plants reside in built environments, and all are associated with a range of microbes, tiny organisms that cannot be seen by the unaided human eye. In fact, the number of microbial cells associated with human bodies is greater than the number of human cells that our bodies contain (Turnbaugh et al. 2007). While people may think of microbes as “bad,” most are not. Many microorganisms help keep pathogens at bay and drive critical functions in our bodies, such as digestion.

Sources of microbial bioaerosols in the built environment may include humans; pets; plants; plumbing systems; heating, ventilation, and air-conditioning systems; mold; resuspension of settled dust; and outdoor air

Figure

Sources of microbial bioaerosols in the built environment may include humans; pets; plants; plumbing systems; heating, ventilation, and air-conditioning systems; mold; resuspension of settled dust; and outdoor air. The green and red dots represent microorganisms (more...)

When humans mingle in the built environment, we share microorganisms with each other and our surrounding space. Microbes are sloughed off with skin cells and dirt; passed through hugs, handshakes, and saliva; and flushed into plumbing systems and carried to septic systems, sewers, and sewage treatment plants. They are on surfaces, in the air, in our tap water, and in the wastewater we create—nearly everywhere. Given such ubiquity and the knowledge that people in the developed world spend more than 90% of their time indoors (Klepeis and Nelson 2001), it is important to understand what types of microorganisms reside in the built environment, how these microbes interact with humans, and how they might impact human health and the economy. Some microbes are pathogenic, particularly to people with compromised immune systems. Others have impacts that we are only just beginning to understand.

With global climate change, we are likely to reexamine how we design and operate the built environment. In doing so, we would be prudent to examine impacts on indoor microbial ecosystems and their effects on human health, comfort, and satisfaction.

2. What microbes are found in built environments?

Trillions of microorganisms contribute to the built environment microbiome, comprising thousands of different species, ranging from single-celled organisms such as bacteria and archaea to microbes with cell structures that are more similar to cells of plants and animals, such as protozoa, fungi, and algae (Adams et al. 2015; Kelly and Gilbert 2013; Konya and Scott 2014; Stephens et al. 2015). In addition, viruses are abundant in these diverse communities of microbes. Since we know little about how they contribute to the built environment microbiome, we do not address them in this report but acknowledge that their importance should be studied.

To identify potential impacts of microbes on people and structures within the built environment, it is important to characterize the biogeography of the microbial community. Which microbes are present? In what numbers? Are the microbes alive or dead, and if alive, how active are they? What kinds of microbial products or metabolites can be found, and what factors drive their concentrations? One of the problems that we face is that the different microbial populations in these communities are quite difficult to quantify given current methods and costs and their variability over time and in space. Nevertheless, this task has been made somewhat easier by developments in molecular biology over the past two to three decades.

The development of DNA sequencing techniques has facilitated the study of microbes in their natural habitat.

Analysis of microbes

Historically, scientists have studied microbial populations by collecting samples and growing the microbes in specialized media in a laboratory. In some studies, “xenobiotic” substances, such as drugs or pollutants, are introduced to the media to better understand their effects on microbes. Analysis of microbes in culture has provided a wealth of information on metabolically active microorganisms. Scientists have learned about relationships between outdoor and indoor microbes and the behavior of microbes found in the indoor air, on indoor surfaces, and in plumbing and ventilation systems. While cultures can be used to model microbial behavior in the indoor environment, this method provides information only on species for which we have identified suitable culture conditions. In addition, the community dynamics between organisms—including competition for resources—can be quite different in a petri dish or flask than out in the built environment, with its multiple ecological niches.

The development of DNA sequencing techniques has facilitated the study of microbes in their natural habitat. Scientists now are able to extract genetic material from microbial cells in a sample taken directly from its natural environment and identify the order of nucleotides within strands of DNA or RNA. Specific nucleotide patterns often can be hallmarks of particular taxa or biological activities. Sequencing does not provide information on the metabolic state of microbes but has allowed microbiologists to identify thousands of new microbial species, many of which were unknown to traditional science (Hugenholz et al. 1998).

Buildings are extremely diverse in form, organization, materials, occupancy, and schedule…

Scientists often examine variations associated with a single “marker” gene present in all species. Microbial ecologists frequently use the 16S ribosomal RNA gene sequence to screen for the presence and relative abundance of different bacterial and archaeal species (Hugenholz et al. 1998; Knight et al. 2012). Likewise, fungi can be analyzed using the ribosomal internal transcribed spacer (ITS) region (Schoch et al. 2012). While this approach is efficient, samples can become biased by the process of amplifying (producing numerous copies of) the gene of interest to allow for analysis (Pinto and Raskin 2012).

Shotgun metagenomic sequencing has become one of the more common sequencing methods. This process examines random genomic DNA fragments extracted directly from the entire microbial community. Like targeted marker gene analysis, this method can effectively identify which microbial taxa are present and estimate their abundance. Metagenomics enables the reassembly of entire genomes, allowing for the assessment of the genetic function potential of organisms. While this is at least an order of magnitude more expensive than marker gene analysis, it provides considerably more data and has far greater potential to generate new knowledge. Fortunately, advances in sequencing technology and computing power are reducing the costs (Kelly and Gilbert 2013).

Sampling microbes

Sample collection and processing also influence the number, type, and viability of the microbes studied from the built environment (Hoisington et al. 2014). Collection capacity and efficiency of different tools can vary dramatically. Swabs, for example, are used to efficiently collect surface microbes from small areas and hard-to-reach places, while vacuums can collect samples from larger areas that include porous surfaces or surfaces that are diffi-cult to “swab” (e.g., carpets). The number of microbes obtained using a swab depends on the degree of sample adhesion. In contrast, the number and viability of microbes obtained by a vacuum are determined by the amount of air passing through the air filter and the resistance of microbes to desiccation from the air flow. For aerosol samples, the type and characteristics of the sampler affect the particle size that can be collected and hence the type of microbes, since different microbes vary greatly in size (Morrow et al. 2012).

Contamination of samples can be a challenge. The mere presence of humans during sample collection and laboratory analysis can impact samples, as humans are constantly shedding microbes with skin cells. Equipment also can cause contamination. For example, gene sequencers may have carryover effects from one series of analyses to the next (Salter et al. 2014).

Equally challenging for investigations in the micro-biology of the built environment is study design. Buildings are extremely diverse in form, organization, materials, occupancy, and schedule, with complex interactions among elements. Studies range in scale from whole buildings to lab-scale models of spaces in order to control for these sources of variation.

As the study of microbes in the built environment progresses, it will be critical to recognize and minimize methodological biases and articulate study designs. Investigators will need to document techniques used more explicitly; moreover, the sampling methods should be standardized so that results from one study can be compared to another (Ramos and Stephens 2014). It would be useful to develop validated consensus standards and protocols for sample collection, processing, and analysis (Morrow et al. 2012) and identify the concentration, type, and location of pathogens that warrant concern and/or disinfection.

Colonization patterns

Despite methodological limitations, we are beginning to understand some of the basic factors that influence the number and type of microbes found in the built environment and confirm some of the conclusions of earlier culture studies. Preliminary studies indicate that indoor spaces have distinct microbial communities. Buildings share many species with the outdoor environment but contain specific taxa that thrive indoors and are more abundant inside than outside (Barberán et al. 2015).

Where do microbes in the indoor microbiome come from? Some come from initial building materials and are brought in by workers during building construction; many others come from building occupants and environmental sources. Humans contribute microbes through loss of skin cells, as well as gut, nasal, oral, and vaginal fluids and semen, while pets contribute through loss of skin, fur, saliva, and feces. Even house plants and fish tanks contribute microbes. The water from centralized drinking water treatment facilities contains microbes that are dispersed when we shower, flush the toilet, and run the dishwasher (Pinto et al. 2012). Outdoor air carries microbes through windows, doors, and ventilation systems, while humans and pets track in microbe-laden soil as well as pollen and dust trapped in clothes and fur. The food that we bring into our homes also contains microbes (Montville and Mathews 2005). And although we don’t like to think about it, insect or rodent pests may introduce additional microbes (Kelly and Gilbert 2013).

Once inside the built environment, microbes are transported through air, water, or the contact of occupants with each other and indoor surfaces. Individual cells or groups of cells may be dispersed multiple times or settle and then thrive, lie dormant, or perish depending on local conditions.

Coughing and sneezing send microbes onto airborne droplets

Figure

Coughing and sneezing send microbes onto airborne droplets.

The kinds of bacteria found in the built environment are related to the occupancy and activity patterns of people, plants, and pets in the building and in individual spaces. The greater the traffic, the more exuberant and varied the activity, the greater the microbial biomass and diversity. Moreover, the organization of spaces in the built environment—how they are juxtaposed—shapes the microbiomes present (Kembel et al. 2014). Given the limitless number of ways that we inhabit buildings, it is not surprising that bacteria vary from building to building and room to room (see Table 1) (Adams et al. 2014; Kelly and Gilbert 2013). In fact, the bacterial “signature” of a building is so distinct that it can be used to predict the sex ratio of human occupants or the presence or absence of a cat or dog (Barberán et al. 2015). When an occupant moves to a new house, it may take only a few days for his or her unique bacterial microbiome to reestablish in a new location (Lax et al. 2014).

Table 1.. Signature microbes of various built environments.

Table 1.

Signature microbes of various built environments.

In contrast, fungi present in the built environment are strongly influenced by the presence of water and the composition of outdoor fungi (Adams et al. 2013). Common fungi include molds such as Aspergillus, Alternaria, Cladosporium, and Penicillium and wood-degrading fungi such as Stereum, Trametes, Phlebia, and Ganoderma, as well as fungi associated with humans such as Candida, a common yeast associated with skin and mucous membranes. Fungal populations tend to vary primarily by moisture level, climate, and region, with significant regional variation across the United States (Barberán et al. 2015).

Ventilation and airflow play a key role in determining the number and type of microbes present in the built environment. Rooms with natural ventilation through windows and doors have a higher abundance of outdoor fungi and bacteria than those that have sealed windows and mechanical ventilation (Kembel et al. 2012; Meadow et al. 2014). Smaller, older residential structures also tend to have higher relative leakage through walls and around window and door areas than larger, newer structures (Chan et al. 2005). Heating, ventilation, and air conditioning (HVAC) systems filter out some airborne microbes.

Warm temperatures and high moisture tend to promote microbial growth within the built environment (Tang 2009). Microbes thrive in restrooms and kitchens—in sinks, on showerheads and shower curtains, and in and around toilets (Feazel et al. 2009). These areas may become microbial hotspots due to the damp microhabitat and the introduction of specific microbes from food, gastrointestinal and vaginal sources, and the water system (Adams et al. 2014). Leaks and condensation from faulty building construction also may cause moisture accumulation and microbial growth.

Floods lead to extensive microbial growth, carrying “outdoor” microbes and nutrients inside. After Hurricane Katrina, the Centers for Disease Control and Prevention (CDC) estimated that 43% of homes in the New Orleans area were colonized with large, visible colonies of mold (CDC 2006). In Boulder, Colorado, scientists found that air in flooded homes had three times more fungal DNA than did air from nonflooded homes. Moreover, the influence of flooding on the microbiome persisted even after the relative humidity returned to baseline and residents removed flood-damaged material and renovated the damaged rooms (Emerson et al. 2015).

Mold in a New Orleans building after Hurricane Katrina

Figure

Mold in a New Orleans building after Hurricane Katrina.

The properties of materials in the built environment also affect microbial growth (Ramos and Stevens 2014). Wood, metal, plaster, and concrete all have different physical and chemical properties of varying appeal to microbes. More-porous materials provide microhabitats for microbes and the opportunity to store moisture. For example, scientists have found that plaster is particularly susceptible to fungal growth after flooding (Anderson et al. 2011). Copper is less prone to colonization and as a result is often the material of choice in hospital design (Mehtar et al. 2008). In fact, laboratory tests show that copper alloys even work as antimicrobials (Michels et al. 2015).

Ventilation and airflow play a key role in determining the number and type of microbes present in the built environment.

Microbial colonization is impacted by cleaning. In the process of cleaning, we remove dust and associated microbes as well as some of the substances on which they live. Chemicals, high temperatures, or UV radiation are used to disinfect surfaces. The more frequently and thoroughly we clean, the less opportunity for microbial buildup on materials and the lower the microbial biomass (Adams et al. 2013; Dunn et al. 2013; Medrano-Félix et al. 2011). Even house walls may be reservoirs for microbial communities, because occupants are less likely to wash walls than floors (Ruiz-Calderon et al. 2016). Hand sanitation is equally important. Proper handwashing and adherence to cleaning protocols minimize the spread of infectious agents in health care settings but may also kill noninfectious microbes (Boyce and Pittet 2002).

Evolution of microbes

Built environments have the capacity to drive the evolution of new microbial species and functions. Unique physical and chemical conditions, and interactions between indoor species, place selective pressures on microbes that ultimately can alter their genetic makeup (Martin et al. 2015). Microbes generate new functions through gene duplication and other mechanisms, as well as coopting functions from other organisms through symbiosis or gene transfer (Eisen 2009). Some of the many new organisms identified in recent years may have evolved in response to the diversified habitats of the built environment (Lax and Gilbert 2015).

3. How does microbial metabolism affect the chemistry of built environments?

Fungi, bacteria, and other heterotrophic microbes break down organic compounds to produce the energy they need for growth and reproduction. When microbes grow on building materials, the result is decomposition and decay. Left unchecked over time, decomposition may undermine the structural integrity of building materials, especially wood, often with catastrophic results. Sadly, we have seen this all too frequently in recent years with the collapse of wood-fortified balconies and decks (Van Derbeken et al. 2015).

Microbes are part of the fine particulate matter in indoor air. Spores and mycelial fragments not only originate from outdoors but are dispersed by fungi and some bacteria (e.g., actinomycetes) growing indoors. Airborne concentrations vary in time and space, reaching 1,000 spores per cubic meter, even in “clean” buildings with no visible mold (Baxter et al. 2005; Nevalainen et al. 2015). Cell fragments, compounds from decomposed materials, and dead microorganisms further contribute to the particle load of indoor air.

Image

Figure

Microbial decomposition in a wood support contributed to the catastrophic collapse of a balcony in Berkeley, CA

Microbes produce a number of additional products that become part of the built environment. Of particular interest and concern are beta-glucans, endotoxins, mycotoxins, and volatile organic compounds (VOCs). In the built environment, these compounds frequently attach to dust particles.

Just as microbes vary in the built environment, so will their metabolic products. VOC, toxin, and glucan production are all influenced by microbe interactions with other organisms as well as the properties of growth substrates. By monitoring the in situ state and developing model systems to study microbial biochemical processes and interactions more closely, scientists can continue to build on our understanding of microbial metabolites in the built environment.

4. How do microbes in the built environment affect human health?

Specific causal links between ill health and indoor microbiomes are difficult to make (Mendell et al. 2011). It is almost impossible to separate the effects of microbes from each other and from those of other stressors such as dust and nonmicrobial volatiles; moreover, we have limited information on human exposure to microbes or microbial by-products (Husman 1996). There are neither uniform diagnostic criteria nor clear-cut biomarkers, and diagnostic categories for health effects are viewed with skepticism by many scientists and physicians. Nevertheless, the apparent association between poor health and mold exposure has led to many postulates that mycotoxins, mold VOCs, and/or other mold metabolites might cause the array of reported symptoms. Despite the lack of consensus about the health risks associated with exposure to molds and their metabolites, experts recommend that fungal proliferation indoors should be prevented or minimized.

Microbes are part of the fine particulate matter in indoor air.

Some of the closest associations between the indoor microbiome and poor health have been documented in moldy buildings that host actinomycetes and fungi, including Penicillium, Aspergillus, and Cladosporium (Pestka et al. 2008). Epidemiological studies have linked these environments to respiratory irritation, allergies, and asthma, as well as secondary respiratory infections caused by bacteria and viruses. Nonspecific symptoms also have been documented, such as headaches and tiredness (Institute of Medicine 2004; Mendell et al. 2011; World Health Organization 2009).

In rare instances, indoor microbiomes have been associated with hypersensitivity pneumonitis. This condition tends to occur in occupational situations such as in greenhouses or mushroom houses, where small biological particles are inhaled and become lodged in the lung. Hypersensitivity pneumonitis is more commonly seen in farming communities, where it is often called farmer’s lung (Husman 1996).

Disease has also been associated with building water systems—areas where Legionella bacteria and other opportunistic plumbing pathogens can thrive (Falkinham et al. 2015). When Legionella bacteria are aerosolized in water droplets and inhaled, they may grow and cause Legionnaires’ disease, a form of pneumonia, or a milder flu-like illness, Pontiac fever. According to the CDC, Legionnaires’ disease results in an estimated 8,000 to 18,000 hospitalizations per year in the United States (http://www.cdc.gov/legionella/fastfacts.html). Recent large outbreaks of disease caused by Legionella highlight the importance of maintaining potable water systems and process water. In the summer of 2015, an outbreak linked to a hotel cooling tower in the Bronx was related to 133 reported cases of Legionnaires’ disease and 16 deaths (http://www.nyc.gov/html/doh/html/diseases/cdlegi.shtml).

Legionella bacteria may thrive in poorly maintained cooling towers

Figure

Legionella bacteria may thrive in poorly maintained cooling towers.

Bacteria associated with fecal matter also present health problems indoors. Enterococci, for example, can pass between people, and from colonized surfaces to people, if sanitary measures such as hand-washing and surface cleaning are not performed. Exposure can lead to infection, particularly if the bacteria get into wounds or the bloodstream. Minimizing the spread of enterococci and other microbes is a particular issue at day care centers and elder care facilities, where diaper changing and bedpan use are common (Hodgeson et al. 2000).

Image

Figure

Legionella bacteria in lung tissue

The negative health impacts of opportunistic pathogenic microbes in hospitals are a particular concern and warrant careful consideration during building design and operation. When patients come to the hospital, they may introduce new or additional disease-causing microbes to the building. These may be transmitted through person-to-person contact, person-to-equipment-to-person contact, or sneezing, coughing, vomiting, and diarrhea. Many hospital patients have compromised or underdeveloped immune systems which confer a heightened risk of infection. In 2002, 1.7 million patients in the United States, or 5% of those admitted to hospitals, contracted hospital-acquired infections, contributing to 99,000 deaths (Klevens et al. 2007). A third of these infections were attributed to lapses in proper cleanliness protocols.

Within the hospital, a patient’s treatment has a strong impact on the microbiome and health outcomes. Antimicrobial medications are used to combat infectious disease. Particular care, however, must be taken with antibiotics. Repeated or incomplete use, particularly for the wrong reason (e.g., as therapy for viral infections), may promote antibiotic-resistant populations of microbes. Further, chemotherapy and radiation can make cancer patients more susceptible to infectious disease by damaging bone marrow cells. With fewer bone marrow cells, the patient has a more difficult time producing the white blood cells needed to combat microbial infection.

Patients in proximity to point sources of pathogenic microbes in a hospital are more likely to come in contact with pathogens and become sick. In the absence of proper barriers, hospital construction and renovation can contribute to airborne mold spores and an increase in the number of infections, including fungal pulmonary infections by Zygomycetes and Aspergillus (Kanamori et al. 2015). Further, patients may have an increased risk of acquiring infections from antibioitic-resistant bacteria (e.g., methicillin-resistant Staphylococcus aureus, vancomycin-resistant Enterococcus, Clostridium difficile, and Acinetobacter) if they occupy a room previously occupied by an infected or colonized patient (Weber and Rutala 2013).

With so many unknowns associated with the transmission of microbes in hospitals and the high stakes at hand, the Alfred P. Sloan Foundation has funded the Hospital Microbiome Project (http://hospitalmicrobiome.com). This project is studying the composition of surface, air, water, and human microbial conditions at a newly constructed University of Chicago hospital before and after the introduction of patients, health care workers, and staff. As the project proceeds, scientists hope to learn where microbes originate, where they thrive, and how they establish themselves, in order to improve patient health outcomes.

Microbiologist Jack Gilbert Swabs the floor in a new hospital room to collect microbial samples at the new University of Chicago hospital

Figure

Microbiologist Jack Gilbert Swabs the floor in a new hospital room to collect microbial samples at the new University of Chicago hospital.

5. Is there such a thing as a healthy indoor microbiome?

Of the 1 to 10 million species of microbes on the planet, scientists estimate that only 1% cause disease (Proctor 2014). The remainder contribute to ecosystems in ways that we are only just beginning to understand. In the human gut, for example, there are microbes that are critical for digestion and produce vitamins, antimicrobials, and neurotransmitters (LeBlanc et al. 2013; Lyte 2013). Thus, it is logical to ask if indoor microbial communities can produce conditions that can influence positive health outcomes in occupants.

We currently don’t have an answer. We don’t even have a good definition for a “healthy” indoor micro-biome. However, there are two ways to think about healthy microbiomes—how we can avoid harmful microbiomes and how we can encourage well-being. More is understood on the first of these.

Scientists agree that it is best to avoid unhealthy systems that build up problematic microorganisms associated with disease. This can be done in part through the appropriate design and operation of buildings. For example, architects can design buildings with room partitions or other physical structures that control foot traffic and some airborne microbe transmission. Engineers can ensure that buildings have an optimal air exchange rate and control relative humidity within heating and cooling zones. By keeping the relative humidity lower than 30%, microbial growth can be limited. Windows let in sunlight, which impacts some microbes, as well as outdoor air, increasing air exchange in the building. However, such turnover is beneficial only in areas and at times with good outdoor air quality and needs to be avoided during periods of air pollution.

In addition, we can design and maintain plumbing systems to minimize microbial colonization. Pipe systems should avoid dead zones that allow water to stagnate and develop biofilms that can allow Legionella, Pseudomonas, and mycobacteria to thrive. Water in water heaters can be heated to a high temperature to suppress microbial contamination (Falkinham et al. 2015). Moreover, we can minimize localized moisture problems by detecting and fixing plumbing leaks rapidly, including the pinhole leaks common in older copper pipes. Water meters can be used in residential structures to identify leaks when all water in the building is shut off.

Proper care should be taken to remove reservoirs of dust and mold when they occur. This entails cleaning or replacing dirty HVAC filters, cleaning HVAC ducting, removing and replacing rotten wood from buildings, or getting rid of resident bird populations. By removing drop ceilings, we can eliminate dead spaces that accumulate dust, as well as porous tile material on which microbes are often found (Hodgeson et al. 2000). Such work can minimize the dispersal of pathogenic microbes but will undoubtedly remove many “good” microbes as well.

HVAC filters can help trap microbes but must be cleaned or replaced frequently

Figure

HVAC filters can help trap microbes but must be cleaned or replaced frequently.

Hospitals routinely take extra precautions to minimize the spread of disease-causing microbes. Surfaces are cleaned frequently, and rooms include stations to facilitate handwashing. Air streams may be more thoroughly scrubbed for fungal or bacterial propagules, or rooms may be pressurized to keep pathogens out or depressurized to prevent the escape of highly infectious microbes. In some cases, hospitals irradiate the upper portions of rooms with ultraviolet germicidal (UV-C) radiation to kill the microbes above 6.5 feet. As air circulates within the room, part of the microbial load is killed (First et al. 2005).

We also can encourage healthy coexistence with microbes by promoting development and maintenance of effective immune systems and healthy microbiomes. There is still much to learn in this area, but scientists recognize that somewhat paradoxically, exposure to bacteria, viruses, and parasites can help us build immunity that enables us to combat infection. The antimicrobial soaps, antimicrobial wipes, and antimicrobial surfaces that we often use, particularly those containing triclosan, may be doing us more harm than good (Bertelsen et al. 2012; Halden 2014).

Exposure to certain microbes is particularly important in early childhood, when the immune system is still developing. Infants, for example, are less likely to develop asthma and allergies if they live in a house with a dog—and its distinct microbial communities—than in a house without a dog (Ownby et al. 2002; von Mutius and Vercelli 2010). When mice were fed lactobacilli from dogs, their immune system improved (Fujimura et al. 2014). Exposure to farm animals during pregnancy and early childhood also decreases the risk for allergies (Holbreich et al. 2012). Endotoxins in farm dust may work to protect lung epithelial cells (Schuijs et al. 2015).

Infants who grow up exposed to dog microbes are less likely to develop asthma and allergies

Figure

Infants who grow up exposed to dog microbes are less likely to develop asthma and allergies.

The type of childbirth also influences the microbial inoculation of children. During vaginal deliveries, babies are colonized by the mother’s vaginal and intestinal microbes. When cesarean deliveries are performed, this inoculation is bypassed and the baby’s first microbial contact is with the room microbiome. For cesarean newborns, this translates to a wholly different complement of microbes, including many skin bacteria and some potential pathogens (e.g., Staphylococcus and Acinetobacter) (Dominguez-Bello et al. 2010). Although scientists are only beginning to explore possible links between immune system development and health outcomes, they have noted an increased incidence of childhood asthma, allergic rhinitis, and obesity in children delivered by cesarean section (Mueller et al. 2015; Renz-Polster et al. 2005).

To increase our understanding of the “healthy” micro-biome in the built environment, we must expand our epidemiologic knowledge. These studies are challenging—investigators need to understand the time, concentration, and route of exposure to microbes and their byproducts, as well as the dose response. It is also important to characterize building factors that may moderate disease so that associations between the built environment and disease can be elucidated (Luongo et al. 2015). As we conduct these studies, it will be important to evaluate risk across socioeconomic groups, age groups, and regions and to bear in mind the energy and carbon costs associated with any change in building design and operation.

6. How do we foster collaborations among scientists who study the built environment using different paradigms?

Assessing indoor microbiomes and identifying links to building design and operation and health outcomes are extremely complex and require expertise from many disciplines. Microbial ecologists, building engineers, architects, public and occupational health experts, and medical doctors all bring specific knowledge, tools, and approaches to the table that can enhance each other’s research.

How do we foster collaboration? At the most basic level, we can provide grants as incentive. Funders can recommend or mandate interdisciplinary collaboration in providing financial support for research projects. We also can provide opportunities for investigators to connect and exchange ideas. By organizing cross-disciplinary sessions or workshops at conferences and/ or providing travel funding for investigators to attend conferences outside of their disciplines, conference organizers can encourage investigators to expand their conversations and explore joint objectives.

Image MicrobiologyBuiltEnvironments-fig10

Scientists can build Internet platforms to share research findings, protocols, ideas, presentation materials, and data. The microBEnet, a project funded by the Alfred P. Sloan Foundation and run out of the lab of Jonathan Eisen at the University of California, Davis, is a particularly useful resource. Users have access to blogs, simple guides, and social media groups, and they can share slides and videos on the microbiology of the built environment (www.microbe.net). Another useful resource is the mVOC database, which provides an excellent platform to exchange information on VOC emissions from bacteria and fungi. Users can find and share information on VOC structures, signature VOCs of particular microbes, and compound target pathways as well as basic information on microbial VOCs (Lemfack et al. 2014; http://bioinformatics.charite.de/smvoc/).

Communication between investigators also can be improved through the use of standardized and complete metadata. For this purpose, the Genomics Standards Consortium has recently developed an MIxS-BE package defining specific metadata terms associated specifically with studies of the built environment (Glass et al. 2014). Regulatory and investigative bodies such as the U.S. Environmental Protection Agency, the U.S. Food and Drug Administration, the U.S. Department of Agriculture, the Centers for Disease Control and Prevention, and their respective counterparts across the globe should be consulted and encouraged to contribute to discussions on data collection and reduction.

7. Will studying microbiology of built environments change the ways we design, build, operate, occupy, and clean our indoor spaces?

Yes, changes are certainly possible as we strengthen our knowledge of the built environment microbiome, its determinants, and health impacts. The common attitude that all microbes are “bad” needs moderating. The better the public understands known risks and suspected benefits of microbes, the more willing people will be to alter the way in which they clean, occupy, and use buildings. Towards this end, we must ensure that information is transparent and widely communicated using nontechnical language and consistent use of terms.

Changes in building design and construction may be more difficult.

Changes in building design and construction may be more difficult. Widespread adoption of new practices will take policy support and mandated changes in building codes. Experts can facilitate this process by working with policymakers to show how research supports the need for change. Whenever possible, the dialogue should engage existing professional communities and companies with related interests. Obvious allies are the Green Building Council, the American Institute of Architects, the Center for Health Design, the American Society of Heating, Refrigerating and Air-Conditioning Engineers (ASHRAE), building scientists/engineers, companies that design hospitals, and those that focus on building sensors and biohazard rooms.

Documented case studies of exemplary buildings and practices and any potential cost savings can facilitate the adoption of sound practices. Forward-looking architects should be enlisted to serve as spokespeople for smart design. Research findings can be used to inform existing standards, such as the WELL Building Standard (http://delos.com/about/well-building-standard/) or the Leadership in Energy and Environmental Design (LEED) standard (http://www.usgbc.org/leed).

References

  • Adams RI, Bateman AC, Bik HM, and JF Meadow. 2015. Microbiota of the indoor environment: a meta-analysis. Microbiome 3:49. doi: 10​.1186/s40168-015-0108-3. [PMC free article: PMC4604073] [PubMed: 26459172]
  • Adams RI, Milleto M, Taylor JW, and TD Bruns. 2013. Dispersal in microbes: fungi in indoor air are dominated by outdoor air and show dispersal limitation at short distances. The ISME Journal 7(7):1262–1273. doi: 10​.1038/ismej.2013.28. [PMC free article: PMC3695294] [PubMed: 23426013]
  • Adams RI, Milleto M, Taylor JW, and TD Bruns. 2014. Airborne bacterial communities in residences: similarities and differences with fungi. PLoS One 9(3):e91283. doi: 10​.1371/journal.pone.0091283. [PMC free article: PMC3946336] [PubMed: 24603548]
  • Anderson B, Frisvad JC, Sondergaard I, Rasmussen IS, and LS Larsen. 2011. Associations between fungal species and water-damaged building materials. Applied and Environmental Microbiology 77(12):4180–4188. doi: 10​.1128/AEM.02513-10. [PMC free article: PMC3131638] [PubMed: 21531835]
  • Barberán A, Dunn RR, Reich BJ, Pacifici K, Laber EB, Menninger HL, Morton JM, Henley JB, Leff JW, Miller SL, and N Fierer. 2015. The ecology of microscopic life in household dust. Proceedings. Biological Sciences/The Royal Society 282(1814). doi: 10​.1098/rspb.2015.1139. [PMC free article: PMC4571696] [PubMed: 26311665]
  • Baxter DM, Perkins JL, McGhee CR, and JM Seltzer. 2005. A regional comparison of mold spore concentrations outdoors and inside “clean” and “mold contaminated” Southern California buildings. Journal of Occupational and Environmental Hygiene 2:8–18. doi: 10​.1080/15459620590897523. [PubMed: 15764519]
  • Bertelsen RJ, Longnecker MP, Løvik M, Calafat AM, Carlsen KH, London SJ, and KC Lødrup Carlsen. 2012. Triclosan exposure and allergic sensitization in Norwegian children. Allergy 68(1):84–91. doi: 10​.1111/all.12058. [PMC free article: PMC3515701] [PubMed: 23146048]
  • Boyce JM, and D Pittet. 2002. Guidelines for hand hygiene in health-care settings: recommendations of the Healthcare Infection Control Practices Advisory Committee and the HICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force. Infection Control and Hospital Epidemiology 23(12):S3–S40. doi: 10​.1086/503164. [PubMed: 12515399]
  • Centers for Disease Control and Prevention. 2006. Health concerns associated with mold in water-damaged homes after Hurricanes Katrina and Rita—New Orleans area, Louisiana, October 2005. MMWR. Morbidity and Mortality Weekly Report 55(2):41–44. [PubMed: 16424858]
  • Chan WR, Nazaroff WW, Price PN, Sohn MD, and AJ Gadgil. 2005. Analyzing a database of residential air leakage in the United States. Atmospheric Environment 39:3445–3455. doi: 10​.1016/j.atmosenv.2005.01.062.
  • Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, and R Knight. 2010. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proceedings of the National Academy of Sciences of the United States of America 107(26):11971–11975. doi: 10​.1073/pnas.1002601107. [PMC free article: PMC2900693] [PubMed: 20566857]
  • Dunn RR, Fierer N, Henley JB, Leff JW, and ML Menninger. 2013. Home life: factors structuring the bacterial diversity found within and between homes. PLoS One 8(5):e64133. doi: 10​.1371/journal.pone.0064133. [PMC free article: PMC3661444] [PubMed: 23717552]
  • Eisen JA. 2009. Genomic evolvability and the origin of novelty: studying the past, interpreting the present, and predicting the future, p 230–251. In Relman DA, Hamburg MA, Choffness ER, and A Mack (ed), Microbial evolution and co-adaptation: a tribute to the life and scientific legacies of Joshua Lederberg. The National Academies Press, Washington, DC.
  • Emerson JB, Keady PB, Brewer TE, Clements N, Morgan EE, Awerbuch J, Miller SL, and N Fierer. 2015. Impacts of flood damage on airborne bacteria and fungi in homes after the 2013 Colorado Front Range flood. Environmental Science and Technology 49(5):2675–2684. doi: 10​.1021/es503845j. [PubMed: 25643125]
  • Falkinham JO, III, Hilborn ED, Arduino MJ, Pruden A, and MA Edwards. 2015. Epidemiology and ecology of opportunistic premise plumbing pathogens: Legionella pneumophila, Mycobacterium avium, and Pseudomonas aeruginosa. Environmental Health Perspectives 123:749–758. doi: 10​.1289/ehp.1408692. [PMC free article: PMC4529011] [PubMed: 25793551]
  • Feazel LM, Baumgartner LK, Peterson KL, Frank DN, Harris JK, and NR Pace. 2009. Opportunistic pathogens enriched in shower-head biofilms. Proceedings of the National Academy of Sciences of the United States of America 106:16393–16399. doi: 10​.1073/pnas.0908446106. [PMC free article: PMC2752528] [PubMed: 19805310]
  • First MW, Weker RA, Yasui S, and EA Nardell. 2005. Monitoring human exposures to upper-room germicidal ultraviolet irradiation. Journal of Occupational and Environmental Hygiene 2:285–292. doi: 10​.1080/15459620590952224. [PubMed: 15848970]
  • Fog Nielsen K. 2003. Mycotoxin production by indoor molds. Fungal Genetics and Biology 39(2):103–117. doi: 10​.1016/S1087-1845(03)00026-4. [PubMed: 12781669]
  • Fujimura KE, Demoor T, Rauch M, Faruqi AA, Jang S, Johnson CC, Boushey HA, Zoratti E, Ownby D, Lukacs NW, and SV Lynch. 2014. House dust exposure mediates gut microbiome Lactobacillus enrichment and airway immune defense against allergens and virus infection. Proceedings of the National Academy of Sciences of the United States of America 111(2):805–810. doi: 10​.1073/pnas.1310750111. [PMC free article: PMC3896155] [PubMed: 24344318]
  • Glass EM, Dribinsky Y, Yilmaz P, Levin H, Pelt RV, Wendel D, Wilke A, Eisen JA, Huse S, Shipanova A, Sogin M, Stajich J, Knight R, Meyer F, and LM Schriml. 2014. MIxS-BE: a MIxS extension defining a minimum information standard for sequence data from the built environment. The ISME Journal 8:1–3. doi: 10​.1038/ismej.2013.176. [PMC free article: PMC3869023] [PubMed: 24152717]
  • Halden RU. 2014. On the need and speed of regulating triclosan and triclocarban in the United States. Environmental Science and Technology 48:3603–3611. doi: 10​.1021/es500495p. [PMC free article: PMC3974611] [PubMed: 24588513]
  • Herrmann A. 2010. The chemistry and biology of volatiles. Wiley, Chichester, United Kingdom.
  • Hodgeson M, Brodt W, Henderson D, Loftness V, McCrone R, Roselle G, Rosenfeld A, Woods J, and R Wright. 2000. Needs and opportunities for improving the health, safety and productivity of medical research facilities. Environmental Health Perspectives 108(Suppl 6):1003–1008. [PMC free article: PMC1240232] [PubMed: 11124125]
  • Hoisington AJ, Maestre JP, King MD, Siegel JA, and KA Kinney. 2014. Impact of sampler selection on the characterization of the indoor microbiome via high-throughput sequencing. Building and Environment 80:274–282. doi: 10​.1016/j.buildenv.2014.04.021.
  • Holbreich M, Genuneit J, Weber J, Braun-Fahrländer C, Waser M, and E von Mutius. 2012. Amish children living in northern Indiana have a very low prevalence of allergic sensitization. The Journal of Allergy and Clinical Immunology 129(6):1671–1673. doi: 10​.1016/j.jaci.2012.03.016. [PubMed: 22513133]
  • Horner WE, and JD Miller. 2003. Microbial volatile organic compounds with emphasis on those arising from filamentous fungal contaminants of buildings. ASHRAE Transactions 109:215–231.
  • Hugenholz P; Goebel BM, and NR Pace. 1998. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. Journal of Bacteriology 180(18):4765–4774. [PMC free article: PMC107498] [PubMed: 9733676]
  • Husman T. 1996. Health effects of indoor-air microorganisms. Scandinavian Journal of Work, Environment, and Health 223:5–13. [PubMed: 8685674]
  • Institute of Medicine. 2004. Damp indoor spaces and health. The National Academies, Institute of Medicine, Washington, DC. [PubMed: 25009878]
  • Kanamori H, Rutala WA, Sickbert-Bennett EE, and DJ Weber. 2015. Review of fungal outbreaks and infection prevention in healthcare settings during construction and renovation. Clinical Infectious Diseases 61:433–444. doi: 10​.1093/cid/civ297. [PubMed: 25870328]
  • Kelly ST, and JA Gilbert. 2013. Studying the microbiology of the indoor environment. Genome Biology 14:202. doi: 10​.1186/gb-2013-14-2-202. [PMC free article: PMC3663111] [PubMed: 23514020]
  • Kembel SW, Jones E, Kline J, Northcutt D, Stetson J, Womack AM, Bohannan BJ, Brown GZ, and JL Green. 2012. Architectural design influences the diversity and structure of the built environment microbiome. The ISME Journal 6:1469–1479. doi: 10​.1038/ismej.2011.211. [PMC free article: PMC3400407] [PubMed: 22278670]
  • Kembel SW, Meadow JF, O'Connor TK, Mhuireach G, Northcutt D, Kline J, Moriyama M, Brown GZ, Bohannan BJM, and JL Green. 2014. Architectural design drives the biogeography of indoor bacterial communities. PLoS One 9(1):e87093. doi: 10​.1371/journal.pone.0087093. [PMC free article: PMC3906134] [PubMed: 24489843]
  • Klepeis NE, and WC Nelson. 2001. The National Human Activity Pattern Survey (NHAPS): a resource for assessing exposure to environmental pollutants. Journal of Exposure Analysis and Environmental Epidemiology 11(3):231–252. doi: 10​.1038/sj.jea.7500165. [PubMed: 11477521]
  • Klevens RM, Edwards JR, Richards CL, Jr, Horan TC, Gaynes RP, Pollock DA, and DM Cardo. 2007. Estimating health care-associated infections and deaths in U.S. hospitals, 2002. Public Health Reports 122:160–166. [PMC free article: PMC1820440] [PubMed: 17357358]
  • Knight R, Jansson J, Field D, Fierer N, Desai N, Fuhrman JA, Hugenholtz P, van der Lelie D, Meyer F, Stevens R, Bailey M, Gordon JI, Kowalchuk GA, and JA Gilbert. 2012. Unlocking the potential of metagenomics through replicated experimental design. Nature Biotechnology 30(6):513–520. doi: 10​.1038/nbt.2235. [PMC free article: PMC4902277] [PubMed: 22678395]
  • Konya T, and JA Scott. 2014. Recent advances in the microbiology of the built environment. Current Sustainable/Renewable Energy Reports 1(2):35–42. doi: 10​.1007/s40518-014-0007-4.
  • Korpi, A, Jarnberg J, and AL Pasanen. 2009. Microbial volatile organic compounds. Critical Reviews in Toxicology 39:139–193. doi: 10​.1080/10408440802291497. [PubMed: 19204852]
  • Lax S, and JA Gilbert. 2015. Hospital-associated microbiota and implications for nosocomial infections. Trends in Molecular Medicine 21:427–432. doi: 10​.1016/j.molmed.2015.03.005. [PubMed: 25907678]
  • Lax S, Smith DP, Hampton-Marcell J, Owens SM, Handley KM, Scott NM, Gibbons SM, Larsen P, Shogan BD, Weiss S, Metcalf JL, Ursell LK, Vázquez-Baeza Y, Van Treuren W, Hasan NA, Gibson MK, Colwell R, Dantas G, Knight R, and JA Gilbert. 2014. Longitudinal analysis of microbial interaction between humans and the indoor environment. Science 345(6200):1048–1052. doi: 10​.1126/science.1254529. [PMC free article: PMC4337996] [PubMed: 25170151]
  • LeBlanc JG, Milani C, de Giori GS, Sesma F, van Sinderen D, and M Ventura. 2013. Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Current Opinion in Biotechnology 24(2):160–168. doi: 10​.1016/j.copbio.2012.08.005. [PubMed: 22940212]
  • Lemfack MC, Nickel J, Dunkel M, Preissner R, and B Piechulla. 2014. mVOC: a database of microbial volatiles. Nucleic Acids Research 42(1):D744–D748. doi: 10​.1093/nar/gkt1250. [PMC free article: PMC3964988] [PubMed: 24311565]
  • Luongo JC, Fennelly KP, Keen JA, Zhai ZJ, Jones BW, and SL Miller. 2015. Role of mechanical ventilation in the airborne transmission of infectious agents in buildings. Indoor Air. doi: 10​.1111/ina.12267. [PMC free article: PMC7165552] [PubMed: 26562748]
  • Lyte M. 2013. Microbial endocrinology in the microbiome-gut-brain axis: how bacterial production and utilization of neurochemicals influence behavior. PLoS Pathogens 9(11):e1003726. doi: 10​.1371/journal.ppat.1003726. [PMC free article: PMC3828163] [PubMed: 24244158]
  • Martin LJ, Adams RI, Bateman A, Bik HM, Hawks J, Hird SM, Hughes D, Kembel SW, Kinney K, Kolokotronis SO, Levy G, McClain C, Meadow JF, Medina RF, Mhuireach GW, Moreau CS, Munshi-South J, Nichols LM, Palmer C, Popova L, Schal C, Täubel M, Trautwein M, Ugalde JA, and RR Dunn. 2015. Evolution of the indoor biome. Trends in Ecology and Evolution 30(4):223–232. doi: 10​.1016/j.tree.2015.02.001. [PubMed: 25770744]
  • Meadow JF, Altrichter AE, Kembel SW, Kline J, Mhuireach G, Moriyama M, Northcutt D, O'Connor TK, Womack AM, Brown GZ, Green JL, and BJ Bohannan. 2014. Indoor air bacterial communities are influenced by ventilation, occupancy, and outdoor air source. Indoor Air 24(1):41–48. doi: 10​.1111/ina.12047. [PMC free article: PMC4285785] [PubMed: 23621155]
  • Medrano-Félix A, Martínez C, Castro-del Campo N, León-Félix J, Peraza-Garay F, Gerba CP, and C Chaidez. 2011. Impact of prescribed cleaning and disinfectant use on microbial contamination in the home. Journal of Applied Microbiology 110(2):463–471. doi: 10​.1111/j.1365-2672.2010.04901.x. [PubMed: 21143709]
  • Mehtar S, Wiid I, and SD Todorov. 2008. The antimicrobial activity of copper and copper alloys against nosocomial pathogens and Mycobacterium tuberculosis isolated from healthcare facilities in the Western Cape: an in-vitro study. The Journal of Hospital Infection 68:45–51. doi: 10​.1016/j.jhin.2007.10.009. [PubMed: 18069086]
  • Mendell MJ, Mirer AG, Cheung K, Tong M, and J Douwes. 2011. Respiratory and allergic health effects of dampness, mold, and dampness-related agents: a review of the epidemiologic evidence. Environmental Health Perspectives 119(6):748–756. doi: 10​.1289/ehp.1002410. [PMC free article: PMC3114807] [PubMed: 21269928]
  • Michels HT, Keevil CW, Salgado CD, and MG Schmidt. 2015. From laboratory research to a clinical trial: copper alloy surfaces kill bacteria and reduce hospital-acquired infections. HERD 9:64–79. doi: 10​.1177/1937586715592650. [PMC free article: PMC4561453] [PubMed: 26163568]
  • Montville TJ, and KR Matthews. 2005. Food microbiology: an introduction. ASM Press, Washington, DC.
  • Morrow JB, Downey AS, Peccia J. 2012. Challenges in microbial sampling in the indoor environment: workshop report summary. NIST technical note 1737. National Institute of Standards and Technology, Gaithersburg, MD.
  • Mueller NT, Whyatt R, Hoepner L, Oberfield S, Dominguez-Bello MG, Widen EM, Hassoun A, Perera F, and A Rundle. 2015. Prenatal exposure to antibiotics, cesarean section and risk of childhood obesity. International Journal of Obesity 39(4):665–670. doi: 10​.1038/ijo.2014.180. [PMC free article: PMC4390478] [PubMed: 25298276]
  • Nevalainen A, Täubel M, and A Hyvärinen. 2015. Indoor fungi: companions and contaminants. Indoor Air 25:125–156. doi: 10​.1111/ina.12182. [PubMed: 25601374]
  • Ownby DR, Johnson CC, and EL Peterson. 2002. Exposure to dogs and cats in the first year of life and risk of allergic sensitization at 6 to 7 years of age. JAMA 288(8):963–972. doi: 10​.1001/jama.288.8.963. [PubMed: 12190366]
  • Pestka JJ, Yike I, Dearborn DG, Ward MD, and JR Harkema. 2008. Stachybotrys chartarum, trichothecene mycotoxins, and damp building-related illness: new insights into a public health enigma. Toxicological Sciences 104(1):4–26. doi: 10​.1093/toxsci/kfm284. [PubMed: 18007011]
  • Pinto AJ, and L Raskin. 2012. PCR biases distort bacterial and archaeal community structure in pyrosequencing datasets. PLoS One 7(8):e43093. doi: 10​.1371/journal.pone.0043093. [PMC free article: PMC3419673] [PubMed: 22905208]
  • Pinto AJ, Xi C, and L Raskin. 2012. Bacterial community structure in the drinking water microbiome is governed by filtration processes. Environmental Science and Technology 46(16):8851–8859. doi: 10​.1021/es302042t. [PubMed: 22793041]
  • Proctor L. 2014. Overview of the NIH Human Microbiome Project. Presentation at the AAAS Symposium Microbiomes of the Built Environment, 27 March 2014, Washington, DC.
  • Ramos T, and B Stephens. 2014. Tools to improve built environment data collection for indoor microbial ecology investigations. Building and Environment 81:243–257. doi: 10​.1016/j.buildenv.2014.07.004.
  • Renz-Polster H, David MR, Buist AS, Vollmer WM, O'Connor EA, Fraser EA, and MA Wall. 2005. Caesarean section delivery and the risk of allergic disorders in childhood. Clinical and Experimental Allergy 35(11):1466–1472. doi: 10​.1111/j.1365-2222.2005.02356.x. [PubMed: 16297144]
  • Ruiz-Calderon JF, Cavallin H, Song SJ, Novoselac A, Pericchi LR, Hernandez JN, Rios R, Branch OH, Pereira H, Paulino LC, Blaser MJ, Knight R, and MG Dominguez-Bello. 2016. Walls talk: microbial biogeography of homes spanning urbanization. Science Advances 2:e1501061. doi: 10​.1126/sciadv.1501061. [PMC free article: PMC4758746] [PubMed: 26933683]
  • Salter SJ, Cox MJ, Turek EM, Calus ST, Cook-son WO, Moffatt MF, Turner P, Parkhill J, Loman NJ, and AW Walker. 2014. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biology 12(1):87. doi: 10​.1186/s12915-014-0087-z. [PMC free article: PMC4228153] [PubMed: 25387460]
  • Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, and Fungal Barcoding Consortium. 2012. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proceedings of the National Academy of Sciences of the United States of America 109(16):6241–6246. doi: 10​.1073/pnas.1117018109. [PMC free article: PMC3341068] [PubMed: 22454494]
  • Schuijs MJ, Willart MA, Vergote K, Gras D, Deswarte K, Ege MJ, Madeira FB, Beyaert R, van Loo G, Bracher F, von Mutius E, Chanez P, Lambrecht BN, and H Hammad. 2015. Farm dust and endotoxin protect against allergy through A20 induction in lung epithelial cells. Science 349(6252):1106–1110. doi: 10​.1126/science.aac6623. [PubMed: 26339029]
  • Stephens B, Adams RI, Bhangar S, Bibby K, and MS Waring. 2015. From commensalism to mutualism: integrating the microbial ecology, building science, and indoor air communities to advance research on the indoor microbiome. Indoor Air 25:1–3. doi: 10​.1111/ina.12167. [PubMed: 25594131]
  • Tang JW. 2009. The effect of environmental parameters on the survival of airborne infectious agents. Journal of the Royal Society, Interface/the Royal Society 6(Suppl 6):S737–S746. doi: 10​.1098/rsif.2009.0227.focus. [PMC free article: PMC2843949] [PubMed: 19773291]
  • Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett C, Knight R, and JI Gordon. 2007. The human microbiome project: exploring the microbial part of ourselves in a changing world. Nature 449(7164):804–810. doi: 10​.1038/nature06244. [PMC free article: PMC3709439] [PubMed: 17943116]
  • Van Derbeken J, Lee HK, Aleaziz H, and K Alexander. 16 June 2015. 6 dead, 7 hurt in Berkeley balcony collapse. San Francisco Chronicle, San Francisco, CA.
  • von Mutius E, and D Vercelli. 2010. Farm living: effects on childhood asthma and allergy. Nature Reviews in Immunology 10(12):861–868. doi: 10​.1038/nri2871. [PubMed: 21060319]
  • Weber, DJ, and WA Rutala. 2013. Understanding and preventing transmission of healthcare-associated pathogens due to the contaminated hospital environment. Infection Control and Hospital Epidemiology 34(5):449–452. doi: 10​.1086/670223. [PubMed: 23571359]
  • World Health Organization. 2009. WHO guidelines for indoor air quality: dampness and mould. WHO Regional Office for Europe, Copenhagen, Denmark. [PubMed: 23785740]
Copyright 2016 American Academy of Microbiology.

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Bookshelf ID: NBK519802PMID: 30176129DOI: 10.1128/AAMCol.Sept.2015