Microbiomes of the Built Environment A Research Agenda for Indoor Microbiology, Human Health, and Buildings (2017) / Chapter Skim
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2 Microorganisms in Built Environments: Impacts on Human Health
2 Microorganisms in Built Environments: Impacts on Human Health
Pages 31-90
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From page 31... ...
• There is evidence of a link between exposure to indoor mi croorganisms and the development of respiratory and allergic symptoms, particularly those arising from exposure to micro organisms that flourish in damp indoor settings. • Preliminary evidence suggests that certain microbial exposures, including early-life exposures to diverse microorganisms as sociated with animals, may have beneficial health effects, such as protection from allergy and respiratory symptoms.
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From page 32... ...
This chapter begins by laying the groundwork for understanding how microorganisms found in buildings may influence health. The chapter then addresses, in turn, infection transmission in indoor environments, noninfectious health outcomes associated with indoor microorganisms, and potential benefits of microbial exposures.
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From page 33... ...
separates the indoor and outdoor environments, thus reducing exposure to microorganisms that thrive outdoors and potentially increasing exposure to organisms that thrive indoors. The diversity of the microbiomes of the built environments in which humans live may impact the microbiomes of their bodies.
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. One topic of interest is the nature of nonpathogenic interactions between indoor and human microbiomes.
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Only a handful of studies support a role of these compounds in inflammatory processes when combined with exposure to other microbial components (endotoxin, glucans) (Korkalainen et al., 2017)
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. Sources of Indoor Microbiomes That Are Relevant to Human Health Recent observations suggest that occupants and outdoor microbes enterng buildings through ventilation and tracked in through dust are the i dominant origin of indoor environmental bacteria, particularly those that can be airborne (Adams et al., 2015; Prussin et al., 2015)
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are well documented in the spread of infectious disease, and there is research documenting aerosol transmission of pathogens in different nonresidential indoor environments (Dick et al., 1987; Wong et al., 2010)
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Figure 2-1 illustrates various routes of transmission of infectious agents in the indoor environment. Chapter 3 explores indoor sources and reservoirs of microorganisms in greater detail, but one important pathway for human exposure is inhalation of microorganisms carried or resuspended in room air, as well as microorganisms found in building water systems that become aerosolized.
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Rubella Norovirus Rotavirus Adenovirus Coxsackie virus Influenza Rhinovirus Coronaviruses (Middle East respiratory syndrome [MERS] , severe acute respiratory syndrome [SARS]
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, is capable of amplifying on wetted surfaces such as those that may be found in built environments. In some cases, amplification is facilitated by growth of amoebae in biofilms that may harbor pathogens.
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showed that inhalation of a variety of volatile organic compounds either enhanced lethality or reduced the mice's ability to fight off the inhaled Klebsiella infection. It can be anticipated that many human exposures in the built environment will be complex, and future studies will need to explore in more detail the potentially interacting or modulating effects of combined chemical, physical particulate matter, and microbial exposures on health.
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. In summary, the indoor environment can be a venue for exposure to a variety of infectious agents, including bacteria, protozoa, fungi, and viruses.
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The 2004 IOM report lists a number of health outcomes as having inadequate or insufficient evidence with which to determine whether an association exists, including airflow obstruction (in otherwise healthy persons) , skin symptoms, mucous membrane irritation 2 The term "noninfectious" is used here to represent potential health associations that are not known to be due to specific infection, although conventional clinical testing through pathogen culture methods may not fully consider the breadth of diversity and community structure of indoor microbiomes that has been increasingly characterized.
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From page 44... ...
Evidence existing asthma Development of Limited or Sufficient Evidence Sufficient Evidence asthma Suggestive Evidence Current asthma Not Evaluated Sufficient Evidence Sufficient Evidence Ever-diagnosed asthma Not Evaluated Not Evaluated Sufficient Evidence Bronchitis Not Evaluated Limited or Sufficient Evidence Suggestive Evidence Respiratory infections Not Evaluated Sufficient Evidence Sufficient Evidence Allergic rhinitis Not Evaluated Limited or Sufficient Evidence Suggestive Evidence Eczema Not Evaluated Not Evaluated Sufficient Evidence Common cold Not Evaluated Not Evaluated Limited or Suggestive Evidence Allergy/atopy Not Evaluated Inadequate/ Limited or Insufficient Suggestive Evidence Evidence Hypersensitivity Clinical Evidence Clinical Evidence Clinical Evidence pneumonitis * Evidence judged to be strongly suggestive of causation.
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From page 45... ...
. The rest of this section selectively discusses studies published in the past decade concerning indoor dampness and respiratory or allergic health outcomes, and it addresses the question "Can specific indoor microbial exposures account in part for the adverse respiratory effects of building dampness?
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From page 46... ...
This is the case particularly in susceptible populations such as children and people with preexisting asthma. Association with Asthma Development and Worsening of Asthma Control Living, working, or attending school in damp indoor environments has been associated with onset or worsening and exacerbation of asthsma in children and adults.
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From page 47... ...
Recent evidence suggests that both allergic and nonallergic asthma are more frequent in damp indoor environments. This evidence is important because it suggests that not all of the effects of dampness result from a llergic responses to allergens from microbial and nonmicrobial sources (e.g., allergens on dust mites and cockroaches)
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Fungi are a source of many different components that may have health effects. Allergens and other antigens on indoor fungi are one set of microbial components known to worsen respiratory symptoms in people who have established asthma and are allergic to the specific fungal allergen they inhale.
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More recent publications have implicated damp indoor environments, along with other exposures (e.g., chemicals)
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. V In addition to producing active metabolites or metabolizing chemicals in the indoor environment, the indoor environmental microbiome itself may influence the human microbiome in ways that lead to health effects.
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. However, there are no data to suggest that the indoor environmental microbiome influences the composition or structure of the skin microbiome (Lax et al., 2014)
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and sleep disorders, to changes in neurocognitive or behavioral function. The findings of these studies have prompted investigators to posit that indoor microbial communities may m ediate a portion of the observed associations of brain health outcomes with building characteristics or with other potential microbial sources within or proximal to buildings.
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. Other potential mechanisms by which environmental microbes might influence brain health might not require the ingestion or proliferation of microbes, and they could include responses to airway or skin encounters with microbial components or metabolites.
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In addition to the large literature linking damp buildings, buildings with water damage, and housing in poor repair with respiratory symptoms, some studies also link these conditions to reduction in brain health, with symptoms of headache, nausea, mood disorders, difficulty concentrating, or sleep difficulties (Ansarin et al., 2013; Casas et al., 2013; Chambers et al., 2016; Cox-Ganser et al., 2010, 2011; Faber et al., 2015; Francisco et al., 2016; Jacobs et al., 2015; Oudin et al., 2016; Park et al., 2008, 2017; Schiffman et al., 2005, Shiue, 2015; Singh and Kenney, 2013; Tiesler et al., 2015)
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From page 55... ...
Although an in-depth discussion of outdoor environmental pollution is beyond the scope of this study, air, water, and other materials from the outdoor environment come indoors into built environments. The integration of disparate areas of knowledge that will underpin a clearer understanding of how indoor microbial exposures can lead to health outcomes and how this understanding could lead to practical application will include efforts to clarify the ties between the outdoors and the indoors.
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From page 56... ...
Thus, it is important to conduct studies of indoor microbial effects on neurocognitive outcomes in built environments reflecting a range of socioeconomic circumstances and resources and to incorporate prospective longitudinal studies in future assessments. BENEFICIAL EFFECTS OF MICROBES Over the past two decades, interest in the potentially protective influences of indoor environmental microbes has been stimulated in part by farm community studies (see Box 2-3 and Annex Table 2-2 at the end of this chapter)
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From page 57... ...
. This knowledge has led to the identification of biomarkers that are associated with health benefit and an extensive body of research aimed at understanding the mechanisms of how microbial exposures could benefit human health (Heederik and von Mutius, 2012; Torow and Hornef, 2017; von Mutius, 2016; von Mutius and Vercelli, 2010; Wlasiuk and Vercelli,
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From page 58... ...
This field of research needs many more targeted, longitudinal observational studies and intervention studies in order to pinpoint where beneficial tips into adverse, as well as the reverse, and to build the knowledge base needed to modulate built environments so as to positively impact human health. Association of Microbial Exposures with Protection from Asthma and Respiratory Symptoms While the adverse effects of microorganisms, their components, and their products have well-documented influence on the development, progression, or exacerbation of asthma and allergies (Eggleston et al., 1998; Lai et al., 2015; Quansah et al., 2012)
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From page 59... ...
, but they may help define the components of microbial exposures that are of potential therapeutic benefit for some people. As has been shown with endotoxin, it is likely that various microbial components may be good for some people and bad for others, depending on dose, compartment (whether inhaled or ingested)
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From page 60... ...
Furthermore, it is unknown whether environmental microbial exposures contributed to the reported improvements. While green buildings have repeatedly been cited as an approach to improving health (Allen et al., 2015, 2016; NRC, 2006)
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Connections between the built environment and a number of nonrespiratory health outcomes have been suggested -- including effects on child development, brain health, and mental health -- although less is known about whether these effects are due to exposures to indoor environmental microbes and through which physiologic mechanisms they occur. Beneficial effects on health from exposure to microorganisms in built environments have also been reported, particularly for exposures that occur in early life.
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3. Elucidate the immunologic, physiologic, or other biologic mecha nisms through which microbial exposures in built environments may influence human health.
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Several studies have documented associations between early-life microbial exposures and exposure to diverse microorganisms associated with animals and later protective health effects. Further longitudinal studies of the ef fects of early-life microbial exposures on subsequent child and adult health will be needed to understand these connections more fully.
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Environmental Health Perspectives 124(10)
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2012. The outdoor air pollution and brain health workshop.
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1991. Microbiological agents as health risks in indoor air.
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Indoor Air 24(3)
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2012. Seasonal variations of indoor microbial exposures and their relation to temperature, relative humidity, and air exchange rate.
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. Environmental Health Perspectives 123(10)
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2015. Indoor environmental exposures and exacerbation of asthma: An update to the review by the Institute of Medicine.
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Indoor Air 27(1)
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Indoor Air 17(1)
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2016. Indoor environmental control of tuberculosis and other airborne infec tions.
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Indoor Air 16(3)
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2000. Health effects of mycotoxins in indoor air: A critical review.
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2010. Multiple microbial exposures in the home may protect against asthma or allergy in childhood.
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2007. Airborne bacteria in indoor environments.
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2009. WHO guidelines for indoor air quality: Damp ness and mold.
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: 1 visit, limited resources Chew Three Pre–post Mold (spore Intervention: Reductions N/A Pre- and during et al., uninhabited treatment counts, Removal of in mold and treatment mold and 2006 water- comparison cultures, drywall, carpet, endotoxin endotoxin levels orders damaged PCR insulation, and all pre–post, of magnitudes above homes after analysis, water-damaged but high those in homes without a major glucan) , furnishings levels during severe water damage hurricane endotoxin, cleanup Adequate respirator use (New and PM recommended during Orleans, cleanup Louisiana)
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From page 80... ...
ANNEX TABLE 2-1 Continued 80 Exposure Exposure Asthma Reference Population Study Design Focus Intervention Outcome Outcome Comments Kercsmar 62 2- to RCT Mold scores; Intervention At 6 months, Decreased Low sample size, limited et al., 17-year-old allergen (n = 29) and but not at asthma power 2006 children levels control (n = 33)
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, residents average and in asthma Some retrofitting indoor CO2 health (adults) required as not all 982 ppm renovations worked Reports of health benefits appear fewer in follow-up 81 continued
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ANNEX TABLE 2-1 Continued 82 Exposure Exposure Asthma Reference Population Study Design Focus Intervention Outcome Outcome Comments Mitchell 182 4- to Observational, Indoor Intervention: Reduction Reduction Separate effects of et al., 12-year-old pre–post allergens, Individually in bedroom (45 percent) individual interventions 2012 children with intervention moisture and tailored mold spores in asthma unknown moderate study mold multifaceted and in symptom days Unclear whether mold to severe environmental Alternaria in Children decrease occurred asthma living intervention settled dust with asthma because of intervention in post– plus asthma counselor Hurricane counselor (timing had greater Katrina of introduction of symptom flooded counselor varied)
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intervention versus comparison group in other environmental exposures 83 continued
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ANNEX TABLE 2-1 Continued 84 Exposure Exposure Asthma Reference Population Study Design Focus Intervention Outcome Outcome Comments Colton 31 low- Observational Intervention (n = Green versus Fewer sick Suggested benefits of et al., income comparison 18) : Move from conventional building move to green housing 2014 households of exposures conventional to housing: syndrome need further assessment in rental and health in new buildings Lower PM2.5, symptoms Number of controls housing green versus designed to green NO2, and limit pre–post analysis conventional standards; smoke- nicotine housing, free policies and Fewer including IPM practices reports of among those employed mold, pests, who moved Control 1 (n = 6)
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Workshop on the Indoor Environment and Childhood Asthma as representative and illustrative of asthma management intervention studies in children. SOURCE: Adapted from Gold et al., 2017.
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ANNEX TABLE 2-2 Beneficial Associations of Indoor Microbiota with Asthma or Allergy Outcomes in Selected 86 Studies Using Metagenomics, Molecular Biologic, or Culture Methods to Measure Indoor Environmental Microbiota Microbiota Exposure Source and Protective Adverse Reference Population Study Design Measurement Method Associations Associations Comments Ege et al., 2011 Two European Cross- Mattress dust Less asthma N/A Diversity as studies sectional associated with: outcome has comparing PARSIFAL: screened Greater diversity limitations children on for bacterial DNA with Specific taxa: Families of farms with SSCP* fungi = eurotium, species, but not reference group: penicillium; specific microbes, PARSIFAL GABRIELA: bacterial bacteria = Listeria identified as (n = 489)
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From page 87... ...
followed air and bedroom dust; sensitization, and outdoor air taxon and mode of from birth to bacterial and fungal asthma by age 13 Cladosporium, exposure age 13 culture associated with dust Aspergillus at Culture misses bedroom floor 2–3 months nonculturable taxa dust Tischer et al., 189 children Longitudinal At 3 months of age: Reduced N/A Protective 2016 (Munich, birth cohort Living room floor dust aeroallergen associations may Germany) followed bacterial and fungal sensitization and attenuate with age from birth to diversity assessed with ever wheezing Diversity as age 10 tRFLP*
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From page 88... ...
ANNEX TABLE 2-2 Continued 88 Microbiota Exposure Source and Protective Adverse Reference Population Study Design Measurement Method Associations Associations Comments Stein et al., 60 children Cross- Bedroom and living Reduced asthma N/A Protective 2016 aged 7–14 sectional room dust assessed with increased associations may from the Amish with 16S rRNA V4-5 endotoxin levels be related only to and Hutterite amplicon sequencing; and increased immune activation communities bacterial and microbial diversity in the upper archaeal diversity and Sensitized animals airway compositional structure; protected from Microbial endotoxin levels; animal eosinophilia with organisms likely exposure validation exposure to dust associated with studies from Amish homes bovine animals Birzele et al., 86 school-age Cross- Mattress dust and nasal Reduced asthma N/A Protective 2016 children sectional samples assessed with with diversity/ associations may 454 pyrosequencing richness -- stronger relate not only of 16S rRNA; for dust than for to upper-airway bacterial diversity and nasal mucosal colonization composition based on samples operational taxonomic units (OTUs) Cavaleiro Rufo 858 8- to Cross- Classroom air samples Reduced allergic Higher Culture misses et al., 2017 10-year-old sectional for bacterial and fungal sensitization but sensitization nonculturable taxa children from culture and endotoxin not asthma with with higher air 20 primary measures increased diversity Penicillium spp.
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From page 89... ...
NOTES: GI = gastrointestinal; N/A = not available; SSCP = single-strand conformation polymorphism analysis; tRFLP = terminal restriction fragment length polymorphism. Diversity: small numbers of microbial exposures may be sufficient to stimulate all pattern-recognition receptors.
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