In This Issue
Microbiomes of the Built Environment
September 15, 2022 Volume 52 Issue 3
The covid-19 pandemic suddenly directed awareness to potential health impacts of the built environment of everyday living – schools, dwellings, offices, public buildings, and other spaces. This issue explores the “microbiome” of the built environment in the postpandemic reality in terms of ventilation performance, filtration, understanding and quantification of transmission risk, protection of “benign” microbes, and the important role of equity, among others.

Microenvironment-Associated Water Microbiomes and Priorities for Public Health Research

Tuesday, September 20, 2022

Author: Kerry A. Hamilton and Timothy Bartrand

Research and data are needed to improve understanding of water-related microbiomes in buildings to reduce disease outbreaks and enhance public health.

A “microenvironment” is the immediate small-scale environment of a structure or organism (or part of it), as distinct from the larger environment, and can create niches for microbial growth.1,2 Differentiating the relative risks between microenvironments in buildings is critical to ranking intervention strategies that will reduce public health risks while promoting a healthy indoor microbiome.

In this article, we highlight water microenvironments that are important from a public health perspective to (i) identify key microenvironments and microbiomes that affect public health risks, (ii) provide a qualitative assessment of the relative risk posed by water microenvironments in buildings, and (iii) identify data gaps that will inform research priorities and risk management efforts.

Water-Related Microbiomes in Buildings

As recognized in the “One Water” construct,3 water systems are a continuum connecting water sources—surface waters, groundwaters, sea-water, and brackish water (for desalination) or greywater/wastewater (for reuse)—to treatment, distribution, detention, and use in building water systems, points of use, drains, collection systems, and wastewater treatment systems. The micro-environment-associated water microbiome in buildings—plumbing systems, points of use, and features such as drains—is influenced by, but distinct from, the microbiome in other parts of the system (e.g., heating, air conditioning, ventilation).

The diversity of systems and sources points to (and data support) a wide variety of water-related microbial communities in buildings. Understanding and managing the water-related microbiome therefore require substantial data collection and synthesis.

Table 1 summarizes the water-related microbiome for key microenvironments in buildings. For 15 micro-environments it characterizes primary exposure route(s), public health significance, key microbiome characteristics and microbial community details where available, qualitative risk evaluation/priorities, data and knowledge gaps, and best management practices.

  • In terms of public health significance, disease outbreaks vary by microenvironment; they include SARS-CoV-2, norovirus, and Legionnaire’s disease, and have been associated with Clostridium difficile, Mycobacterium species, and Staphylococcus bacteria, among others.
  • Qualitative risk evaluation/priorities are designated as follows: low = unlikely to pose a nontrivial public health risk; medium = poses a nontrivial risk under some “typical” conditions or during periods of operational deficiency; high = likely to cause a nontrivial public health risk under routine operating conditions; uncertain = considerable unknown factors present challenges to designation.
  • Cited studies discuss examples of water-related microbiome characteristics and are only a sampling of the many relevant studies conducted to date.

Analysis, Key Data and Knowledge Gaps, and Research Priorities

Microenvironments are generally recognized as important because of their potential to harbor pathogens and promote their growth and because they are associated with exposures of public health consequence. We assign them a qualitative risk and priority based on their association with adverse health impacts. However, that assessment does not account for impacts on infrastructure or other non-health-related implications of the water-related microbiome. That qualification notwithstanding, the risk and priority assessments presented in table 1 can guide future data collection efforts and, equally importantly, analysis and meta-analysis of microbiome data related to priority microenvironments.

We offer the following conclusions and suggestions for measures to support progress in this important area for public health.

  • Research is needed on ways to reduce uncertainties and mitigate risks associated with understudied and/or unregulated water system microenvironments such as the unpressurized portion of showers and other shower components, bathroom drains, decorative water features, and fountains; heating, ventilation, and air conditioning systems including condensate, humidifiers, and misters; cooling towers; point-of-use devices; and certain medical devices.
  • Increased study is needed to (i) better understand the aerosol inhalation route of exposure resulting from water fixtures, systems, and/or devices; and (ii) devise more effective controls and barriers that reduce the occurrence of respiratory pathogens in building water supplies and associated accessories.
  • Improved methods for investigating microbial ecology in situ in the environment can improve understanding of disease transmission routes, prioritize microorganisms for further focus, and identify novel control strategies.
  • Use of genomic tools (e.g., whole genome sequencing) to link infections to sources can aid in identifying and prioritizing water microbiome–associated hazards.4
  • Making additional (typically non-fecal-oral) waterborne illnesses (e.g., nontuberculous mycobacteria) notifiable can increase awareness of micro-environment roles in disease.
  • To reduce public health risk in buildings, it is essential to develop, maintain, and monitor water management plans.

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Vertes A, Hitchins V, Phillips KS. 2012. Analytical challenges of microbial biofilms on medical devices. Analytical Chemistry 84(9):3858–66.

Hoogenkamp MA, Brandt BW, de Soet JJ, Crielaard W. 2020. An in-vitro dynamic flow model for translational research into dental unit water system biofilms. -Microbiological Methods 171:105879.

Paulson C, Stephens LS, Broley W. 2017. Blueprint for One Water (Project #4660). Alexandria VA: Water Research Foundation. ISBN 978-1-60573-274-9.

Constantinides B, Chau KK, Quan TP, Rodger G, -Andersson MI, Jeffery K, Lipworth S, Gweon HS, Peniket A, Pike G, and 9 others. 2020. Genomic surveillance of Escherichia coli and Klebsiella spp. in hospital sink drains and patients. Microbial Genomics 6(7).

Costa D, Mercier A, Gravouil K, Lesobre J, Delafont V, Bousseau A, Verdon J, Imbert C. 2015. Pyrosequencing analysis of bacterial diversity in dental unit waterlines. Water Research 81:223–31.

Sommerstein R, Schreiber PW, Diekema DJ, Edmond MB, Hasse B, Marschall J, Sax H. 2017. Mycobacterium chimaera outbreak associated with heater-cooler devices: Piecing the puzzle together. Infection Control & Hospital Epidemiology 38(1):103–08.

Tsao HF, Scheikl U, Herbold C, Indra A, Walochnik J, Horn M. 2019. The cooling tower water microbiota: -Seasonal dynamics and co-occurrence of bacterial and protist phylotypes. Water Research 159:464–79.

Paniagua AT, Paranjape K, Hu M, Bédard E, Faucher SP. 2020. Impact of temperature on Legionella pneumophila, its protozoan host cells, and the microbial diversity of the biofilm community of a pilot cooling tower. Science of the Total Environment 712:136131.

Paranjape K, Bédard E, Whyte LG, Ronholm J, Prévost M, Faucher SP. 2020. Presence of Legionella spp. in cooling towers: The role of microbial diversity, Pseudomonas, and continuous chlorine application. Water Research 169:115252.

Hamilton KA, Prussin AJ, Ahmed W, Haas CN. 2018. Outbreaks of Legionnaires’ disease and Pontiac fever 2006–2017. Current Environmental Health Reports 5(2):263–71.

Yao W, Gallagher DL, Dietrich AM. 2020. An overlooked route of inhalation exposure to tap water constituents for children and adults: Aerosolized aqueous minerals from ultrasonic humidifiers. Water Research X 9:100060.

Hull NM, Reens AL, Robertson CE, Stanish LF, Harris JK, Stevens MJ, Frank DN, Kotter C, Pace NR. 2015. Molecular analysis of single room humidifier bacteriology. Water Research 69:318–27.

Tyndall RL, Lehman ES, Bowman EK, Milton DK, -Barbaree JM. 1995. Home humidifiers as a potential source of exposure to microbial pathogens, endotoxins, and allergens. Indoor Air 5(3):171–78.

Proctor CR, Gächter M, Kötzsch S, Rölli F, Sigrist R, Walser JC, Hammes F. 2016. Biofilms in shower hoses: Choice of pipe material influences bacterial growth and communities. Environmental Science Water Research & Technology 2(4):670–82.

Gebert MJ, Delgado-Baquerizo M, Oliverio AM, -Webster TM, Nichols LM, Honda JR, Chan ED, Adjemian J, Dunn RR, Fierer N. 2018. Ecological analyses of -Mycobacteria in showerhead biofilms and their relevance to human health. mBio 9(5):e01614–18.

Collins S, Stevenson D, Bennet A, Walker J. 2017. Occurrence of Legionella in UK household showers. International Journal of Hygiene & Environmental Health 220(2 Pt B):401–06.

Kotay S, Chai W, Guilford W, Barry K, Mathers AJ. 2017. Spread from the sink to the patient: In situ study using green fluorescent protein (GFP)-expressing Escherichia coli to model bacterial dispersion from hand-washing sink-trap reservoirs. Applied & Environmental Microbiology 83(8):e03327-16.

Withey Z, Goodall T, MacIntyre S, Gweon HS. 2021. Characterization of communal sink drain communities of a university campus. Environmental DNA 3(5):901–11.

Kotay SM, Parikh HI, Barry K, Gweon HS, Guilford W, Carroll J, Mathers AJ. 2020. Nutrients influence the dynamics of Klebsiella pneumoniae carbapenemase producing enterobacterales in transplanted hospital sinks. Water Research 176:115707.

Kotay SM, Donlan RM, Ganim C, Barry K, Christensen BE, Mathers AJ. 2019. Droplet- rather than aerosol-mediated dispersion is the primary mechanism of bacterial transmission from contaminated hand-washing sink traps. Applied & Environmental Microbiology 85(2):e01997-18.

Modrzewska BD, Bartnicka M, Blaszkowska J. 2019. Microbially contaminated water in urban fountains as a hidden source of infections. CLEAN Soil, Air, Water 47(8):1800322.

Smith SS, Ritger K, Samala U, Black SR, Okodua M, Miller L, Kozak-Muiznieks NA, Hicks LA, Steinheimer C, Ewaidah S, and 2 others. 2015. Legionellosis outbreak associated with a hotel fountain. Open Forum Infectious Diseases 2(4).

Hlavsa MC, Aluko SK, Miller AD, Person J, Gerdes ME, Lee S, Laco JP, Hannapel EJ, Hill VR. 2021. Outbreaks associated with treated recreational water: United States, 2015–2019. Morbidity & Mortality Weekly Report 70(20):733–38.

van Veldhoven K, Keski-Rahkonen P, Barupal DK, -Villanueva CM, Font-Ribera L, Scalbert A, Bodinier B, Grimalt JO, Zwiener C, Vlaanderen J, Portengen L. 2018. Effects of exposure to water disinfection by-products in a swimming pool: A metabolome-wide association study. Environment International 111:60–70.

Shuai X, Sun Y, Meng L, Zhou Z, Zhu L, Lin Z, Chen H. 2021. Dissemination of antibiotic resistance genes in swimming pools and implication for human skin. Science of the Total Environment 794:148693.

Sawabe T, Suda W, Ohshima K, Hattori M, Sawabe T. 2016. First microbiota assessments of children’s -paddling pool waters evaluated using 16S rRNA gene-based -metagenome analysis. Infection & Public Health 9(3):362–65.

Casanovas-Massana A, Blanch AR. 2013. Characterization of microbial populations associated with natural swimming pools. International Journal of Hygiene & Environmental Health 216(2):132–37.

Brandi G, Sisti M, Paparini A, Gianfranceschi G, -Schiavano GF, De Santi M, Santoni D, Magini V, Romano--Spica V. 2007. Swimming pools and fungi: An environmental epidemiology survey in Italian indoor swimming facilities. International Journal of Environmental Health Research 17(3):197–206.

Firuzi P, Asl Hashemi A, Samadi Kafil H, Gholizadeh P, Aslani H. 2020. Comparative study on the microbial quality in the swimming pools disinfected by the ozone-chlorine and chlorine processes in Tabriz, Iran. Environmental Monitoring & Assessment 192(8):516.

Bédard E, Laferrière C, Charron D, Lalancette C, -Renaud C, Desmarais N, Déziel E, Prévost M. 2015. Post-outbreak investigation of Pseudomonas aeruginosa faucet contamination by quantitative polymerase chain reaction and environmental factors affecting positivity. Infection -Control & Hospital Epidemiology 36(11):1337–43.

Zhang C, Qin K, Struewing I, Buse H, Santo Domingo J, Lytle D, Lu J. 2021. The bacterial community diversity of bathroom hot tap water was significantly lower than that of cold tap and shower water. Frontiers in Microbiology 12:625324.

Liu R, Yu Z, Guo H, Liu M, Zhang H, Yang M. 2012. Pyrosequencing analysis of eukaryotic and bacterial communities in faucet biofilms. Science of the Total Environment 435-36:124–31.

De Sotto R, Tang R, Bae S. 2020. Biofilms in premise plumbing systems as a double-edged sword: Microbial community composition and functional profiling of biofilms in a tropical region. Water & Health 18(2):172–85.

Goldstein RR, Kleinfelter L, He X, Micallef SA, George A, Gibbs SG, Sapkota AR. 2017. Higher prevalence of coagulase-negative staphylococci carriage among reclaimed water spray irrigators. Science of the Total Environment 595:35–40.

Garner E, Davis BC, Milligan E, Micallef SA, George A, Gibbs SG, Sapkota AR. 2021. Next generation sequencing approaches to evaluate water and wastewater quality. Water Research 194:116907.

Garner E, Organiscak M, Dieter L, Shingleton C, Haddix M, Joshi S, Pruden A, Ashbolt NJ, Medema G, Hamilton KA. 2021. Towards risk assessment for antibiotic resistant pathogens in recycled water: A systematic review and summary of research needs. Environmental Microbiology 23(12):7355–72.

Garner E, McLain J, Bowers J, Engelthaler DM, Edwards MA, Pruden A. 2018. Microbial ecology and water chemistry impact regrowth of opportunistic pathogens in full-scale reclaimed water distribution systems. Environmental Science & Technology 52(16):9056–68.

Gomez-Alvarez V, Pfaller S, Pressman JG, Wahman DG, Revetta RP. 2016. Resilience of microbial communities in a simulated drinking water distribution system sub-jected to disturbances: Role of conditionally rare taxa and potential implications for antibiotic-resistant bacteria. Environmental Science: Water Research & Technology 2(4):645–57.

Pinto AJ, Schroeder J, Lunn M, Sloan W, Raskin L. 2014. Spatial-temporal survey and occupancy-abundance model-ing to predict bacterial community dynamics in the drinking water microbiome. mBio 5(3):e01135-14.

Bautista-de los Santos QM, Schroeder JL, Sevillano--Rivera MC, Sungthong R, Ijaz UZ, Sloan WT, Pinto AJ. 2016. Microbial communities in full-scale drinking water distribution systems: A meta-analysis. Environmental -Science: Water Research & Technology 2:631–44.

Potgieter S, Pinto A, Sigudu M, Du Preez H, Ncube E, Venter S. 2018. Long-term spatial and temporal microbial community dynamics in a large-scale drinking water distribution system with multiple disinfectant regimes. Water Research 139:406–19.

Rhoads WJ, Ji P, Pruden A, Edwards MA. 2015. Water heater temperature set point and water use patterns influence Legionella pneumophila and associated micro-organisms at the tap. Microbiome 3:67.

Vosloo S, Huo L, Chauhan U, Cotto I, Gincley B, -Vilardi KJ, Yoon B, Pieper KJ, Stubbins A, Pinto AJ. 2022. Systematic recovery of building plumbing-associated -microbial communities after extended periods of altered water demand during the COVID-19 pandemic. -medRxiv, Jan 18.

Buse HY, Morris BJ, Gomez-Alvarez V, Szabo JG, Hall JS. 2020. Legionella diversity and spatiotemporal variation in the occurrence of opportunistic pathogens within a large building water system. Pathogens 9(7):567.

van Heijnsbergen E, Schalk JA, Euser SM, Brandsema PS, den Boer JW, de Roda Husman AM. 2015. Confirmed and potential sources of Legionella reviewed. Environmental Science & Technology 49:4797−815.

Lou M, Liu S, Gu C, Hu H, Tang Z, Zhang Y, Xu C, Li F. 2021. The bioaerosols emitted from toilet and wastewater treatment plant: A literature review. Environmental Science & Pollution Research 28(3):2509–21.

Leone C, Dharmasena M, Tang C, DiCaprio E, Ma Y, Araud E, Bolinger H, Rupprom K, Yeargin T, Li J, and 5 others. 2018. Prevalence of human noroviruses in commercial food establishment bathrooms. Food Protection 81(5):719–28.

Abney SE, Bright KR, McKinney J, Ijaz MK, Gerba CP. 2021. Toilet hygiene: Review and research needs. Applied Microbiology 131(6):2705–14.

Li Y, Duan S, Yu ITS, Wong TW. 2005. Multi-zone model-ing of probable SARS virus transmission by airflow between flats in Block E, Amoy Gardens. Indoor Air 15(2):96–111.

Flores GE, Bates ST, Knights D, Lauber CL, Stombaugh J, Knight R, Fierer N. 2011. Microbial biogeography of public restroom surfaces. PLoS One 6(11):e28132.

Mkrtchyan HV, Russell CA, Wang N, Cutler RR. 2013. Could public restrooms be an environment for bacterial resistomes? PLoS One 8(1):e54223.

Vardoulakis S, Espinoza Oyarce DA, Donner E. 2022. Transmission of COVID-19 and other infectious diseases in public washrooms: A systematic review. Science of the Total Environment 803:149932.

Parsons SA. 2000. The effect of domestic ion-exchange water softeners on the microbiological quality of drinking water. Water Research 34(8):2369–75.

Alfredo K, Lin J, Islam A, Wang ZW. 2020. Impact of activated carbon block point-of-use filters on chloraminated water quality. AWWA Water Science 2(3):e1180.

Reasoner DJ, Blannon JC, Geldreich EE. 1987. Microbiological characteristics of third-faucet point-of-use devices. American Water Works Association 79(10):60–66.

USGS. 2019. Water-use terminology. Online at water-use-terminology.

* Qualitative risk evaluation/priorities: Low = unlikely to pose a nontrivial public health risk; Medium = poses a nontrivial risk under some “typical” conditions or during periods of operational deficiency; High = likely to cause a nontrivial public health risk under routine operating conditions; Uncertain = considerable unknown factors present challenges to designation.

** Self-supplied water use = water withdrawn from a ground- or surface-water source by a user rather than being obtained from a public supply.56

About the Author:Kerry Hamilton is an assistant professor, School of Sustainable Engineering and the Built Environment, and Biodesign Center for Environmental Health Engineering, Arizona State University. Timothy Bartrand is executive director, Environmental Science, Policy, and Research Institute.