Building upon current knowledge and techniques of indoor microbiology to construct the next era of theory into microorganisms, health, and the built environment

Abstract

In the constructed habitat in which we spend up to 90% of our time, architectural design influences occupants’ behavioral patterns, interactions with objects, surfaces, rituals, the outside environment, and each other. Within this built environment, human behavior and building design contribute to the accrual and dispersal of microorganisms; it is a collection of fomites that transfer microorganisms; reservoirs that collect biomass; structures that induce human or air movement patterns; and space types that encourage proximity or isolation between humans whose personal microbial clouds disperse cells into buildings. There have been recent calls to incorporate building microbiology into occupant health and exposure research and standards, yet the built environment is largely viewed as a repository for microorganisms which are to be eliminated, instead of a habitat which is inexorably linked to the microbial influences of building inhabitants. Health sectors have re-evaluated the role of microorganisms in health, incorporating microorganisms into prevention and treatment protocols, yet no paradigm shift has occurred with respect to microbiology of the built environment, despite calls to do so. Technological and logistical constraints often preclude our ability to link health outcomes to indoor microbiology, yet sufficient study exists to inform the theory and implementation of the next era of research and intervention in the built environment. This review presents built environment characteristics in relation to human health and disease, explores some of the current experimental strategies and interventions which explore health in the built environment, and discusses an emerging model for fostering indoor microbiology rather than fearing it.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1

References

  1. 1.

    Tognotti E. Lessons from the History of Quarantine, from Plague to Influenza A. Emerging Infectious Dis J. 2013;19:254.

  2. 2.

    Best M, Neuhauser D. Ignaz Semmelweis and the birth of infection control. Qual Saf Health Care. 2004;13:233–4.

  3. 3.

    Lister J. On the antiseptic principle in the practice of surgery. Br Med J. 1867;2:246–8.

  4. 4.

    Tomes NJ. American Attitudes toward the Germ Theory of Disease: Phyllis Allen Richmond Revisited. J Hist Med. 1997;52:17–50.

  5. 5.

    Smith KA. Louis pasteur, the father of immunology? Front Immunol. 2012;3:68.

  6. 6.

    Evans AS. Causation and disease: the Henle-Koch postulates revisited. Yale J Biol Med. 1976;49:175–95.

  7. 7.

    Riva MA, Benedetti M, Cesana G. Pandemic fear and literature: observations from Jack London’s The Scarlet Plague. Emerg Infect Dis. 2014;20:1753–7.

  8. 8.

    Mathur P. Hand hygiene: back to the basics of infection control. Indian J Med Res. 2011;134:611–20.

  9. 9.

    Teigen PM. Legislating fear and the public health in gilded age Massachusetts. J Hist Med Allied Sci. 2007;62:141–70.

  10. 10.

    Stewart GT. Limitations of the germ theory. Lancet. 1968;1:1077–81.

  11. 11.

    Gause GF. The struggle for existence. Williams & Wilkins Co., Baltimore, Maryland, 1934.

  12. 12.

    Hungate RE. Further experiments on cellulose digestion by the protozoa in the rumen of cattle. Biol Bull. 1943;84:157–63.

  13. 13.

    McFall-Ngai MJ, Ruby EG. Symbiont recognition and subsequent morphogenesis as early events in an animal-bacterial mutualism. Science. 1991;254:1491–4.

  14. 14.

    Dunlap PV, McFall-Ngai MJ. Initiation and control of the bioluminescent symbiosis between photobacterium leiognathi and leiognathid fish. Ann N Y Acad Sci. 1987;503:269–83.

  15. 15.

    Adair KL, Douglas AE. Making a microbiome: the many determinants of host-associated microbial community composition. Curr Opin Microbiol. 2017;35:23–9.

  16. 16.

    Robinson CJ, Bohannan BJM, Young VB. From structure to function: the ecology of host-associated microbial communities. Microbiol Mol Biol Rev. 2010;74:453–76.

  17. 17.

    Knoop KA, Gustafsson JK, McDonald KG, Kulkarni DH, Coughlin PE, McCrate S, et al. Microbial antigen encounter during a preweaning interval is critical for tolerance to gut bacteria. Sci Immunol. 2017;2:eaao1314.

  18. 18.

    Prokopakis E, Vardouniotis A, Kawauchi H, Scadding G, Georgalas C, Hellings P, et al. The pathophysiology of the hygiene hypothesis. Int J Pediatr Otorhinolaryngol. 2013;77:1065–71.

  19. 19.

    Liu AH. Revisiting the hygiene hypothesis for allergy and asthma. J Allergy Clin Immunol. 2015;136:860–5.

  20. 20.

    Vandegrift R, Bateman AC, Siemens KN, Nguyen M, Green JL, Van Den Wymelenberg KG, et al. Cleanliness in context: reconciling hygiene with a modern microbial perspective. Microbiome. 2017;5:76.

  21. 21.

    Scudellari M. News feature: cleaning up the hygiene hypothesis. Proc Natl Acad Sci USA. 2017;114:1433–6.

  22. 22.

    Rook GAW, Brunet LR. Microbes, immunoregulation, and the gut. Gut. 2005;54:317–20.

  23. 23.

    Buffie CG, Bucci V, Stein RR, McKenney PT, Ling L, Gobourne A, et al. Precision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile. Nature. 2015;517:205–8.

  24. 24.

    Surawicz CM, McFarland LV, Greenberg RN, Rubin M, Fekety R, Mulligan ME, et al. The search for a better treatment for recurrent Clostridium difficile disease: use of high-dose vancomycin combined with Saccharomyces boulardii. Clin Infect Dis. 2000;31:1012–7.

  25. 25.

    Na X, Kelly C. Probiotics in Clostridium difficile infection. J Clin Gastroenterol. 2011;45(Suppl):S154–8.

  26. 26.

    Lawley TD, Clare S, Walker AW, Stares MD, Connor TR, Raisen C, et al. Targeted restoration of the intestinal microbiota with a simple, defined bacteriotherapy resolves relapsing Clostridium difficile disease in mice. PLoS Pathog. 2012;8:e1002995.

  27. 27.

    Lau CS, Chamberlain RS. Probiotics are effective at preventing Clostridium difficile-associated diarrhea: a systematic review and meta-analysis. Int J Gen Med. 2016;9:27–37.

  28. 28.

    Mora M, Mahnert A, Koskinen K, Pausan MR, Oberauner-Wappis L, Krause R, et al. Microorganisms in confined habitats: microbial monitoring and control of intensive care units, operating rooms, cleanrooms and the international space station. Front Microbiol. 2016;7:1573.

  29. 29.

    Adams RI, Bateman AC, Bik HM, Meadow JF. Microbiota of the indoor environment: a meta-analysis. Microbiome. 2015;3:49.

  30. 30.

    NASEM. Microbiomes of the Built Environment. National Academies Press, Washington, DC, 2017.

  31. 31.

    Gilbert JA, Stephens B. Microbiology of the built environment. Nat Rev Microbiol. 2018;16:661–70.

  32. 32.

    Gomez-Silvan C, Leung MHY, Grue KA, Kaur R, Tong X, Lee PKH, et al. A comparison of methods used to unveil the genetic and metabolic pool in the built environment. Microbiome. 2018;6:71.

  33. 33.

    Nazaroff WW. Embracing microbes in exposure science. J Expo Sci Environ Epidemiol. 2019;29:1–10.

  34. 34.

    Kembel SW, Jones E, Kline J, Northcutt D, Stenson J, Womack AM, et al. Architectural design influences the diversity and structure of the built environment microbiome. ISME J. 2012;6:1469–79.

  35. 35.

    Adams RI, Lymperopoulou D. Lessons learned when looking for non-neutral ecological processes in the built environment: the bacterial and fungal microbiota of shower tiles. bioRxiv. 2018: 413773. https://doi.org/10.1101/413773.

  36. 36.

    Givehchi R, Maestre JP, Bi C, Wylie D, Xu Y, Kinney KA, et al. Quantitative filter forensics with residential HVAC filters to assess indoor concentrations. Indoor Air. 2019;29:390–402.

  37. 37.

    Emerson JB, Keady PB, Clements N, Morgan EE, Awerbuch J, Miller SL, et al. High temporal variability in airborne bacterial diversity and abundance inside single-family residences. Indoor Air. 2017;27:576–86.

  38. 38.

    Green JL. Can bioinformed design promote healthy indoor ecosystems? Indoor Air. 2014;24:113–5.

  39. 39.

    Brown GZ, Kline J, Mhuireach G, Northcutt D, Stenson J. Making microbiology of the built environment relevant to design. Microbiome. 2016;4:6.

  40. 40.

    Thaler DS. Toward a microbial Neolithic revolution in buildings. Microbiome. 2016;4:14.

  41. 41.

    Yong E. For healthier buildings, just add bacteria? ideas.ted.com. 2017. https://ideas.ted.com/for-healthier-buildings-just-add-bacteria/ (Accessed 19 Feb 2019).

  42. 42.

    Purcell AT. The relationship between buildings and behaviour. Build Environ. 1987;22:215–32.

  43. 43.

    Dunn RR, Fierer N, Henley JB, Leff JW, Menninger HL. Home life: factors structuring the bacterial diversity found within and between homes. PLoS ONE. 2013;8:e64133.

  44. 44.

    Kembel SW, Meadow JF, O’Connor TK, Mhuireach G, Northcutt D, Kline J, et al. Architectural design drives the biogeography of indoor bacterial communities. PLoS ONE. 2014;9:e87093.

  45. 45.

    Meadow JF, Altrichter AE, Kembel SW, Moriyama M, O’Connor TK, Womack AM, et al. Bacterial communities on classroom surfaces vary with human contact. Microbiome. 2014;2:7.

  46. 46.

    Hsu T, Joice R, Vallarino J, Abu-Ali G, Hartmann EM, Shafquat A, et al. Urban transit system microbial communities differ by surface type and interaction with humans and the environment. mSystems 2016; 1. https://doi.org/10.1128/mSystems.00018-16.

  47. 47.

    Karkman A, Lehtimäki J, Ruokolainen L. The ecology of human microbiota: dynamics and diversity in health and disease. Ann N Y Acad Sci. 2017;1399:78–92.

  48. 48.

    Adams RI, Bhangar S, Pasut W, Arens EA, Taylor JW, Lindow SE, et al. Chamber bioaerosol study: outdoor air and human occupants as sources of indoor airborne microbes. PLoS ONE. 2015;10:e0128022.

  49. 49.

    Ross AA, Doxey AC, Neufeld JD. The skin microbiome of cohabiting couples. mSystems. 2017;2:e00043–17.

  50. 50.

    Meadow JF, Altrichter AE, Bateman AC, Stenson J, Brown GZ, Green JL, et al. Humans differ in their personal microbial cloud. PeerJ. 2015;3:e1258.

  51. 51.

    Lax S, Smith DP, Hampton-Marcell J, Owens SM, Handley KM, Scott NM, et al. Longitudinal analysis of microbial interaction between humans and the indoor environment. Science. 2014;345:1048–52.

  52. 52.

    Luongo JC, Barberán A, Hacker-Cary R, Morgan EE, Miller SL, Fierer N. Microbial analyses of airborne dust collected from dormitory rooms predict the sex of occupants. Indoor Air. 2017;27:338–44.

  53. 53.

    Marineli F, Tsoucalas G, Karamanou M, Androutsos G, Mary Mallon. (1869–1938) and the history of typhoid fever. Ann Gastroenterol Hepatol. 2013;26:132–4.

  54. 54.

    Franzosa EA, Huang K, Meadow JF, Gevers D, Lemon KP, Bohannan BJM, et al. Identifying personal microbiomes using metagenomic codes. Proc Natl Acad Sci USA. 2015;112:E2930–8.

  55. 55.

    Meadow JF, Altrichter AE, Kembel SW, Kline J, Mhuireach G, Moriyama M, et al. Indoor airborne bacterial communities are influenced by ventilation, occupancy, and outdoor air source. Indoor Air. 2014;24:41–8.

  56. 56.

    Dannemiller KC, Gent JF, Leaderer BP, Peccia J. Influence of housing characteristics on bacterial and fungal communities in homes of asthmatic children. Indoor Air. 2016;26:179–92.

  57. 57.

    Wood R, Morrow C, Ginsberg S, Piccoli E, Kalil D, Sassi A, et al. Quantification of shared air: a social and environmental determinant of airborne disease transmission. PLoS ONE. 2014;9:e106622.

  58. 58.

    Andrews JR, Morrow C, Walensky RP, Wood R. Integrating social contact and environmental data in evaluating tuberculosis transmission in a South African township. J Infect Dis. 2014;210:597–603.

  59. 59.

    Salathé M, Kazandjieva M, Lee JW, Levis P, Feldman MW, Jones JH. A high-resolution human contact network for infectious disease transmission. Proc Natl Acad Sci USA. 2010;107:22020–5.

  60. 60.

    Borgo B, Mostafavi M. Microbial Air Quality in a 50-year-old Middle School. In: 2007 SACNAS. Society for the Advancement of Chicanos and Native Americans in Science, Kansas City, Missouri, 2007, pp 1–6.

  61. 61.

    Hayleeyesus SF, Manaye AM. Microbiological quality of indoor air in university libraries. Asian Pac J Trop Biomed. 2014;4:S312–7.

  62. 62.

    Virtanen M, Terho K, Oksanen T, Kurvinen T, Pentti J, Routamaa M, et al. Patients with infectious diseases, overcrowding, and health in hospital staff. Arch Intern Med. 2011;171:1296–8.

  63. 63.

    Clements A, Halton K, Graves N, Pettitt A, Morton A, Looke D, et al. Overcrowding and understaffing in modern health-care systems: key determinants in meticillin-resistant Staphylococcus aureus transmission. Lancet Infect Dis. 2008;8:427–34.

  64. 64.

    Bick JA. Infection control in jails and prisons. Clin Infect Dis. 2007;45:1047–55.

  65. 65.

    Tschudin-Sutter S, Carroll KC, Tamma PD, Sudekum ML, Frei R, Widmer AF, et al. Impact of toxigenic Clostridium difficile colonization on the risk of subsequent C. difficile Infection in intensive care unit patients. Infect Control Hosp Epidemiol. 2015;36:1324–9.

  66. 66.

    Yakob L, Riley TV, Paterson DL, Clements ACA. Clostridium difficile exposure as an insidious source of infection in healthcare settings: an epidemiological model. BMC Infect Dis. 2013;13:376.

  67. 67.

    Chaudhury H, Mahmood A, Valente M. The use of single patient rooms versus multiple occupancy rooms in acute care environments. coalition for health environments research, 2005. https://www.healthdesign.org/sites/default/files/use_of_single_patient_rooms_v_multiple_occ._rooms-acute_care.pdf.

  68. 68.

    Bodin Danielsson C, Chungkham HS, Wulff C, Westerlund H. Office design’s impact on sick leave rates. Ergonomics. 2014;57:139–47.

  69. 69.

    Pejtersen JH, Feveile H, Christensen KB, Burr H. Sickness absence associated with shared and open-plan offices–a national cross sectional questionnaire survey. Scand J Work Environ Health. 2011;37:376–82.

  70. 70.

    Ridenhour BJ, Braun A, Teyrasse T, Goldsman D. Controlling the spread of disease in schools. PLoS ONE. 2011;6:e29640.

  71. 71.

    Dill-McFarland KA, Tang Z-Z, Kemis JH, Kerby RL, Chen G, Palloni A, et al. Close social relationships correlate with human gut microbiota composition. Sci Rep. 2019;9:703.

  72. 72.

    Jansen TR. When preschool is in a nursing home. The Atlantic 2016. https://www.theatlantic.com/education/archive/2016/01/the-preschool-inside-a-nursing-home/424827/ Accessed 2 Jan 2019.

  73. 73.

    Seidel J, Valenzano DR. The role of the gut microbiome during host ageing. F1000Res. 2018;7:1086.

  74. 74.

    Odamaki T, Kato K, Sugahara H, Hashikura N, Takahashi S, Xiao J-Z, et al. Age-related changes in gut microbiota composition from newborn to centenarian: a cross-sectional study. BMC Microbiol. 2016;16:90.

  75. 75.

    Dimidi E, Christodoulides S, Scott SM, Whelan K. Mechanisms of action of probiotics and the gastrointestinal microbiota on gut motility and constipation. Adv Nutr. 2017;8:484–94.

  76. 76.

    Wampach L, Heintz-Buschart A, Hogan A, Muller EEL, Narayanasamy S, Laczny CC, et al. Colonization and succession within the human gut microbiome by archaea, bacteria, and microeukaryotes during the first year of life. Front Microbiol. 2017;8:738.

  77. 77.

    Inoue R, Nishio A, Fukushima Y, Ushida K. Oral treatment with probiotic Lactobacillus johnsonii NCC533 (La1) for a specific part of the weaning period prevents the development of atopic dermatitis induced after maturation in model mice, NC/Nga. Br J Dermatol. 2007;156:499–509.

  78. 78.

    Fujimura KE, Demoor T, Rauch M, Faruqi AA, Jang S, Johnson CC, et al. House dust exposure mediates gut microbiome Lactobacillus enrichment and airway immune defense against allergens and virus infection. Proc Natl Acad Sci USA. 2014;111:805–10.

  79. 79.

    Orsmark-Pietras C, James A, Konradsen JR, Nordlund B, Söderhäll C, Pulkkinen V, et al. Transcriptome analysis reveals upregulation of bitter taste receptors in severe asthmatics. Eur Respir J. 2013;42:65–78.

  80. 80.

    Mortaz E, Adcock IM, Folkerts G, Barnes PJ, Paul Vos A, Garssen J. Probiotics in the management of lung diseases. Mediators Inflamm. 2013;2013:751068.

  81. 81.

    Pellaton C, Nutten S, Thierry A-C, Boudousquié C, Barbier N, Blanchard C, et al. Intragastric and intranasal administration of Lactobacillus paracasei NCC2461 modulates allergic airway inflammation in mice. Int J Inflam. 2012;2012:686739.

  82. 82.

    Le Noci V, Guglielmetti S, Arioli S, Camisaschi C, Bianchi F, Sommariva M, et al. Modulation of pulmonary microbiota by antibiotic or probiotic aerosol therapy: a strategy to promote immunosurveillance against lung metastases. Cell Rep. 2018;24:3528–38.

  83. 83.

    Rutala WA, Weber DJ. Surface disinfection: should we do it? J Hosp Infect. 2001;48(Suppl A):S64–8.

  84. 84.

    Vincent M, Hartemann P, Engels-Deutsch M. Antimicrobial applications of copper. Int J Hyg Environ Health. 2016;219:585–91.

  85. 85.

    Fahimipour AK, Hartmann EM, Siemens A, Kline J, Levin DA, Wilson H, et al. Daylight exposure modulates bacterial communities associated with household dust. Microbiome. 2018;6:175.

  86. 86.

    Dannemiller KC, Weschler CJ, Peccia J. Fungal and bacterial growth in floor dust at elevated relative humidity levels. Indoor Air. 2017;27:354–63.

  87. 87.

    Vandegrift R, Ishaq SL, Kline J, Fahimipour A, Stenson J, Crowley R, et al. Shut the front door: seasonal patterns in window operation drive fungal and bacterial community dissimilarity between indoor and outdoor air. In: The 15th Conference of the International Society of Indoor Air Quality & Climate (ISIAQ). International Society of Indoor Air Quality & Climate, p 2.

  88. 88.

    Gibbons SM. The built environment is a microbial wasteland. mSystems. 2016;1:e00033–16.

  89. 89.

    Otter JA, French GL. Survival of nosocomial bacteria and spores on surfaces and inactivation by hydrogen peroxide vapor. J Clin Microbiol. 2009;47:205–7.

  90. 90.

    Kramer A, Schwebke I, Kampf G. How long do nosocomial pathogens persist on inanimate surfaces? A systematic review. BMC Infect Dis. 2006;6:130.

  91. 91.

    Smith SM, Eng RH, Padberg FT Jr. Survival of nosocomial pathogenic bacteria at ambient temperature. J Med. 1996;27:293–302.

  92. 92.

    Gil F, Lagos-Moraga S, Calderón-Romero P, Pizarro-Guajardo M, Paredes-Sabja D. Updates on Clostridium difficile spore biology. Anaerobe. 2017;45:3–9.

  93. 93.

    Ng TW, Chan PY, Chan TT, Wu H, Lai KM. Skin squames contribute to ammonia and volatile fatty acid production from bacteria colonizing in air-cooling units with odor complaints. Indoor Air. 2017;28:258–65.

  94. 94.

    Hospodsky D, Yamamoto N, Nazaroff WW, Miller D, Gorthala S, Peccia J. Characterizing airborne fungal and bacterial concentrations and emission rates in six occupied children’s classrooms. Indoor Air. 2015;25:641–52.

  95. 95.

    Lopez GU, Gerba CP, Tamimi AH, Kitajima M, Maxwell SL, Rose JB. Transfer efficiency of bacteria and viruses from porous and nonporous fomites to fingers under different relative humidity conditions. Appl Environ Microbiol. 2013;79:5728–34.

  96. 96.

    Marinella MA, Pierson C, Chenoweth C. The stethoscope. A potential source of nosocomial infection? Arch Intern Med. 1997;157:786–90.

  97. 97.

    Brooks B, Olm MR, Firek BA, Baker R, Geller-McGrath D, Reimer SR, et al. The developing premature infant gut microbiome is a major factor shaping the microbiome of neonatal intensive care unit rooms. Microbiome. 2018;6:112.

  98. 98.

    Chemaly RF, Simmons S, Dale CJr, Ghantoji SS, Rodriguez M, Gubb J, et al. The role of the healthcare environment in the spread of multidrug-resistant organisms: update on current best practices for containment. Ther Adv Infect Dis. 2014;2:79–90.

  99. 99.

    Joseph A. The impact of the environment on infections in healthcare facilities. Center for Health Design, Concord, California, 2006.

  100. 100.

    Jump RLP, Pultz MJ, Donskey CJ. Vegetative Clostridium difficile survives in room air on moist surfaces and in gastric contents with reduced acidity: a potential mechanism to explain the association between proton pump inhibitors and C. difficile-associated diarrhea? Antimicrob Agents Chemother. 2007;51:2883–7.

  101. 101.

    Hoeksma P, Aarnink A, Ogink N. Effect of temperature and relative humidity on the survival of airborne bacteria. Wageningen UR Livestock Research, 2015. https://library.wur.nl/WebQuery/wurpubs/fulltext/348736.

  102. 102.

    Zhao Y, Aarnink AJA, Dijkman R, Fabri T, de Jong MCM, Groot Koerkamp PWG. Effects of temperature, relative humidity, absolute humidity, and evaporation potential on survival of airborne Gumboro vaccine virus. Appl Environ Microbiol. 2012;78:1048–54.

  103. 103.

    Tang JW. The effect of environmental parameters on the survival of airborne infectious agents. J R Soc Interface. 2009;6(Suppl 6):S737–46.

  104. 104.

    Górny RL, Gołofit-Szymczak M, Cyprowski M, Stobnicka A, Ławniczek-Wałczyk A. Effect of electrical charges on potential of fibers for transport of microbial particles in dry and humid air. J Aerosol Sci. 2018;116:66–82.

  105. 105.

    Hegarty B, Dannemiller K, Peccia J. Gene expression of indoor fungal communities under damp building conditions: implications for human health. Indoor Air. 2018;28:548–58.

  106. 106.

    Pessi A-M, Suonketo J, Pentti M, Kurkilahti M, Peltola K, Rantio-Lehtimäki A. Microbial growth inside insulated external walls as an indoor air biocontamination source. Appl Environ Microbiol. 2002;68:963–7.

  107. 107.

    Wu T, Täubel M, Holopainen R, Viitanen A-K, Vainiotalo S, Tuomi T, et al. Infant and adult inhalation exposure to resuspended biological particulate matter. Environ Sci Technol. 2018;52:237–47.

  108. 108.

    Hyytiäinen HK, Jayaprakash B, Kirjavainen PV, Saari SE, Holopainen R, Keskinen J, et al. Crawling-induced floor dust resuspension affects the microbiota of the infant breathing zone. Microbiome. 2018;6:25.

  109. 109.

    Frankel M, Hansen EW, Madsen AM. Effect of relative humidity on the aerosolization and total inflammatory potential of fungal particles from dust-inoculated gypsum boards. Indoor Air. 2014;24:16–28.

  110. 110.

    Lowen AC, Mubareka S, Steel J, Palese P. Influenza virus transmission is dependent on relative humidity and temperature. PLoS Pathog. 2007;3:1470–6.

  111. 111.

    Wolkoff P. Indoor air humidity, air quality, and health - An overview. Int J Hyg Environ Health. 2018;221:376–90.

  112. 112.

    Taylor S, Hugentobler W. Is low indoor humidity a driver for healthcare-associated infections? In: Proceedings, Indoor Air 2016. International Society of Indoor Air Quality and Climate, 2016. https://www.isiaq.org/docs/Papers/Paper340.pdf.

  113. 113.

    Davis RE, Dougherty E, McArthur C, Huang QS, Baker MGCold. dry air is associated with influenza and pneumonia mortality in Auckland, New Zealand. Influenza Other Respi Viruses. 2016;10:310–3.

  114. 114.

    Frankel M, Bekö G, Timm M, Gustavsen S, Hansen EW, Madsen AM. Seasonal variations of indoor microbial exposures and their relation to temperature, relative humidity, and air exchange rate. Appl Environ Microbiol. 2012;78:8289–97.

  115. 115.

    Dannemiller KC, Weschler CJ, Peccia J. Fungal and bacterial growth in floor dust at elevated relative humidity levels. Indoor Air. 2017;27:354–63.

  116. 116.

    Khare P, Marr LC. Simulation of vertical concentration gradient of influenza viruses in dust resuspended by walking. Indoor Air. 2015;25:428–40.

  117. 117.

    Ahmed T, Usman M, Scholz M. Biodeterioration of buildings and public health implications caused by indoor air pollution. Indoor Built Environ. 2017;27:752–65.

  118. 118.

    Pasanen A-L, Juutinen T, Jantunen MJ, Kalliokoski P. Occurrence and moisture requirements of microbial growth in building materials. Int Biodeterior Biodegradation. 1992;30:273–83.

  119. 119.

    Kuhn DM, Ghannoum MA. Indoor mold, toxigenic fungi, and Stachybotrys chartarum: infectious disease perspective. Clin Microbiol Rev. 2003;16:144–72.

  120. 120.

    Kettleson EM, Adhikari A, Vesper S, Coombs K, Indugula R, Reponen T. Key determinants of the fungal and bacterial microbiomes in homes. Environ Res. 2015;138:130–5.

  121. 121.

    Mendell MJ, Macher JM, Kumagai K. Measured moisture in buildings and adverse health effects: a review. Indoor Air. 2018;28:488–99.

  122. 122.

    Kanchongkittiphon W, Mendell MJ, Gaffin JM, Wang G, Phipatanakul W. Indoor environmental exposures and exacerbation of asthma: an update to the 2000 review by the Institute of Medicine. Environ Health Perspect. 2015;123:6–20.

  123. 123.

    Kotay S, Chai W, Guilford W, Barry K, Mathers AJ. 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. Appl Environ Microbiol. 2017;83:e03327–16.

  124. 124.

    Falkinham JO 3rd, Iseman MD, de Haas P, van Soolingen D. Mycobacterium avium in a shower linked to pulmonary disease. J Water Health. 2008;6:209–13.

  125. 125.

    Thomson R, Tolson C, Carter R, Coulter C, Huygens F, Hargreaves M. Isolation of nontuberculous mycobacteria (NTM) from household water and shower aerosols in patients with pulmonary disease caused by NTM. J Clin Microbiol. 2013;51:3006–11.

  126. 126.

    Kline S, Cameron S, Streifel A, Yakrus MA, Kairis F, Peacock K, et al. An outbreak of bacteremias associated with Mycobacterium mucogenicum in a hospital water supply. Infect Control Hosp Epidemiol. 2004;25:1042–9.

  127. 127.

    Kool JL, Bergmire-Sweat D, Butler JC, Brown EW, Peabody DJ, Massi DS, et al. Hospital characteristics associated with colonization of water systems by Legionella and risk of nosocomial legionnaires’ disease: a cohort study of 15 hospitals. Infect Control Hosp Epidemiol. 1999;20:798–805.

  128. 128.

    Borella P, Montagna MT, Romano-Spica V, Stampi S, Stancanelli G, Triassi M, et al. Legionella infection risk from domestic hot water. Emerg Infect Dis. 2004;10:457–64.

  129. 129.

    Dade-Robertson M, Keren-Paz A, Zhang M, Kolodkin-Gal I. Architects of nature: growing buildings with bacterial biofilms. Microb Biotechnol. 2017;10:1157–63.

  130. 130.

    Grumbein S, Minev D, Tallawi M, Boettcher K, Prade F, Pfeiffer F, et al. Hydrophobic properties of biofilm-enriched hybrid mortar. Adv Mater. 2016;28:8138–43.

  131. 131.

    Hesnawi R, Dahmani K, Al-Swayah A, Mohamed S, Mohammed SA. Biodegradation of municipal wastewater with local and commercial bacteria. Procedia Engineering. 2014;70:810–4.

  132. 132.

    Mikkonen A, Li T, Vesala M, Saarenheimo J, Ahonen V, Kärenlampi S, et al. Biofiltration of airborne VOCs with green wall systems-Microbial and chemical dynamics. Indoor Air. 2018;28:697–707.

  133. 133.

    Russell JA, Hu Y, Chau L, Pauliushchyk M, Anastopoulos I, Anandan S, et al. Indoor-biofilter growth and exposure to airborne chemicals drive similar changes in plant root bacterial communities. Appl Environ Microbiol. 2014;80:4805–13.

  134. 134.

    Waring MS. How well do potted plants or bio-walls clean the indoor air of organic gases? October 17–18, 2016. http://nas-sites.org/builtmicrobiome/files/2016/07/Michael-Waring-FOR-POSTING.pdf.

  135. 135.

    Ponsoni K, Raddi MSG. Indoor air quality related to occupancy at an airconditioned public building. Braz Arch Biol Technol. 2010;53:99–103.

  136. 136.

    Sadar JS. Through the healing glass: shaping the modern body through glass architecture, 1925–35. Routledge, New York, 2016.

  137. 137.

    Himmelfarb P, Scott A, Thayer PS. Bactericidal activity of a broad-spectrum illumination source. Appl Microbiol. 1970;19:1013–4.

  138. 138.

    The Duty on Glass. Lancet. 1845;45:214–6.

  139. 139.

    Møller KI, Kongshoj B, Philipsen PA, Thomsen VO, Wulf HC. How Finsen’s light cured lupus vulgaris. Photodermatol Photoimmunol Photomed. 2005;21:118–24.

  140. 140.

    Hobday RA. Sunlight therapy and solar architecture. Med Hist. 1997;41:455–72.

  141. 141.

    Hobday RA, Dancer SJ. Roles of sunlight and natural ventilation for controlling infection: historical and current perspectives. J Hosp Infect. 2013;84:271–82.

  142. 142.

    Bazzoni CB. The destruction of bacteria through the action of light. Am J Public Health. 1914;4:975–92.

  143. 143.

    Ward HM. The action of light on bacteria. Lancet. 1893;141:383.

  144. 144.

    Downing AMW, Blunt TP III. Researches on the effect of light upon Bacteria and other organisms. Proc R Soc Lond. 1878;26:488–500.

  145. 145.

    Medeiros AB, de A, Enders BC, Lira ALBDC. The Florence Nightingale’s Environmental Theory: A Critical. Analysis. Esc Anna Nery. 2015;19:518–24.

  146. 146.

    Nightingale F. Notes on Hospitals. Longman, Green, Longman, Roberts, and Green, London, 1863.

  147. 147.

    Kundsin RB. Architectural design and indoor microbial pollution. Oxford University Press, New York, 1988.

  148. 148.

    Stone A (ed.). Proceedings of the Twenty-Seventh Annual Convention of the American Institute of Architects. Inland Architect Press, Chicago, Illinois, 1893.

  149. 149.

    Chynoweth P. Progressing the rights to light debate – Part 1: a review of current practice. Structural Survey. 2004;22:131–7.

  150. 150.

    Hessling M, Spellerberg B, Hoenes K. Photoinactivation of bacteria by endogenous photosensitizers and exposure to visible light of different wavelengths - a review on existing data. FEMS Microbiol Lett. 2017;364:fnw270.

  151. 151.

    Fonseca MJ, Tavares F. The bactericidal effect of sunlight. Am Biol Teach. 2011;73:548–52.

  152. 152.

    Besaratinia A, Yoon J-I, Schroeder C, Bradforth SE, Cockburn M, Pfeifer GP. Wavelength dependence of ultraviolet radiation-induced DNA damage as determined by laser irradiation suggests that cyclobutane pyrimidine dimers are the principal DNA lesions produced by terrestrial sunlight. FASEB J. 2011;25:3079–91.

  153. 153.

    Goldman RP, Travisano M. Experimental evolution of ultraviolet radiation resistance in Escherichia coli. Evolution. 2011;65:3486–98.

  154. 154.

    Takada A, Matsushita K, Horioka S, Furuichi Y, Sumi Y. Bactericidal effects of 310 nm ultraviolet light-emitting diode irradiation on oral bacteria. BMC Oral Health. 2017;17:96.

  155. 155.

    Dai T, Vrahas MS, Murray CK, Hamblin MR. Ultraviolet C irradiation: an alternative antimicrobial approach to localized infections? Expert Rev Anti Infect Ther. 2012;10:185–95.

  156. 156.

    Oppezzo OJ. Contribution of UVB radiation to bacterial inactivation by natural sunlight. J Photochem Photobiol B. 2012;115:58–62.

  157. 157.

    de Sousa DL, Lima RA, Zanin IC, Klein MI, Janal MN, Duarte S. Effect of twice-daily blue light treatment on matrix-rich biofilm development. PLoS ONE. 2015;10:e0131941.

  158. 158.

    Maclean M, Anderson JG, MacGregor SJ, White T, Atreya CD. A new proof of concept in bacterial reduction: antimicrobial action of violet-blue light (405 nm) in ex vivo stored plasma. J Blood Transfus. 2016;2016:2920514.

  159. 159.

    Deng Y, Yao J, Wang X, Guo H, Duan D. Transcriptome sequencing and comparative analysis of Saccharina japonica (Laminariales, Phaeophyceae) under blue light induction. PLoS ONE. 2012;7:e39704.

  160. 160.

    Ondrusch N, Kreft J. Blue and red light modulates SigB-dependent gene transcription, swimming motility and invasiveness in Listeria monocytogenes. PLoS ONE. 2011;6:e16151.

  161. 161.

    Sandhu BS, Singh CK. Relationship of sunlight and humidity on the virulence of street rabies virus in saliva. Indian J Anim Sci. 2009;79:24–5.

  162. 162.

    Patra V, Byrne SN, Wolf P. The skin microbiome: is it affected by uv-induced immune suppression? Front Microbiol. 2016;7:1235.

  163. 163.

    Prescott SL, Larcombe D-L, Logan AC, West C, Burks W, Caraballo L, et al. The skin microbiome: impact of modern environments on skin ecology, barrier integrity, and systemic immune programming. World Allergy Organ J. 2017;10:29.

  164. 164.

    Hartmann B, Benson M, Junger A, Quinzio L, Röhrig R, Fengler B, et al. Computer keyboard and mouse as a reservoir of pathogens in an intensive care unit. J Clin Monit Comput. 2004;18:7–12.

  165. 165.

    Daylight modeling | WELL Standard. https://standard.wellcertified.com/light/daylight-modeling. Accessed 27 Feb 2019.

  166. 166.

    Daylight | U.S. Green Building Council. https://www.usgbc.org/credits/healthcare/v4-draft/eqc-0. Accessed 27 Feb 2019.

  167. 167.

    Sehulster L, Chinn RYW, Arduino MJ, Carpenter J, Donlan R, Ashford D, et al. Guidelines for environmental infection control in health-care facilities. Centers for Disease Control and Prevention, 2003. https://francais.cdc.gov/mmwr/preview/mmwrhtml/rr5210a1.htm?mobile=nocontent.

  168. 168.

    Lateef F. Hospital design for better infection control. J Emerg Trauma Shock. 2009;2:175–9.

  169. 169.

    Magill SS, Edwards JR, Bamberg W, Beldavs ZG, Dumyati G, Kainer MA, et al. Multistate point-prevalence survey of health care–associated infections. N Engl J Med. 2014;370:1198–208.

  170. 170.

    Jacob JT, Kasali A, Steinberg JP, Zimring C, Denham ME. The role of the hospital environment in preventing healthcare-associated infections caused by pathogens transmitted through the air. Health Environ Res. Design J. 2013;7:74–98.

  171. 171.

    Dancer SJ. Controlling hospital-acquired infection: focus on the role of the environment and new technologies for decontamination. Clin Microbiol Rev. 2014;27:665–90.

  172. 172.

    Donskey CJ. Does improving surface cleaning and disinfection reduce health care-associated infections? Am J Infect Control. 2013;41:S12–9.

  173. 173.

    Kwan SE, Shaughnessy RJ, Hegarty B, Haverinen-Shaughnessy U, Peccia J. The reestablishment of microbial communities after surface cleaning in schools. J Appl Microbiol. 2018;125:897–906.

  174. 174.

    La Duc MT, Dekas A, Osman S, Moissl C, Newcombe D, Venkateswaran K. Isolation and characterization of bacteria capable of tolerating the extreme conditions of clean room environments. Appl Environ Microbiol. 2007;73:2600–11.

  175. 175.

    Salter SJ, Cox MJ, Turek EM, Calus ST, Cookson WO, Moffatt MF, et al. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol. 2014;12:87.

  176. 176.

    Boyce JM, Havill NL, Dumigan DG, Golebiewski M, Balogun O, Rizvani R. Monitoring the effectiveness of hospital cleaning practices by use of an adenosine triphosphate bioluminescence assay. Infect Control Hosp Epidemiol. 2009;30:678–84.

  177. 177.

    Dharan S, Mourouga P, Copin P, Bessmer G, Tschanz B, Pittet D. Routine disinfection of patients’ environmental surfaces. Myth or reality?. J Hosp Infect. 1999;42:113–7.

  178. 178.

    Dancer SJ. Hospital cleaning in the 21st century. Eur J Clin Microbiol Infect Dis. 2011;30:1473–81.

  179. 179.

    Ramphal L, Suzuki S, McCracken IM, Addai A. Improving hospital staff compliance with environmental cleaning behavior. Proc. 2014;27:88–91.

  180. 180.

    Garcia dos Santos A Jr, Menis Ferreira A, Rigotti MA, Ribeiro dos Santos F, Ribeiro Furlan MC, de Andrade D. Efficiency evaluation of the cleaning and disinfection of surfaces in a primary health center. Texto Contexto Enferm. 2018;27:e3720017.

  181. 181.

    Xu C, Liu L. Personalized ventilation: one possible solution for airborne infection control in highly occupied space? Indoor Built Environ. 2018;27:873–6.

  182. 182.

    Memarzadeh F. Literature Review: Room Ventilation and Airborne Disease Transmission. Am Soc Healthcare Eng. 2013. http://www.ashe.org/management_monographs/pdfs/mg2013Memarzadeh.pdf.

  183. 183.

    Atkinson EBJ, Chartier Y, Pessoa-Silva CL, Jensen P, Li Y, Seto W-H. Natural Ventilation for Infection Control in Health-Care Settings. World Health Organization, 2009. https://www.who.int/water_sanitation_health/publications/natural_ventilation.pdf.

  184. 184.

    Adams RI, Miletto M, Taylor JW, Bruns TD. Dispersal in microbes: fungi in indoor air are dominated by outdoor air and show dispersal limitation at short distances. ISME J. 2013;7:1460.

  185. 185.

    Carlton EJ, Barton K, Shrestha PM, Humphrey J, Newman LS, Adgate JL, et al. Relationships between home ventilation rates and respiratory health in the Colorado Home Energy Efficiency and Respiratory Health (CHEER) study. Environ Res. 2019;169:297–307.

  186. 186.

    Arvanitakis G, Temmerman R, Spök A. Development and use of microbial-based cleaning products (MBCPs): current issues and knowledge gaps. Food Chem Toxicol. 2018;116:3–9.

  187. 187.

    Spök A, Klade M. Environmental, health and legal aspects of cleaners containing living microbes as active ingredients. 2009.http://www.tb-klade.at/wp-content/uploads/2015/06/IFZ-EWP-3-2010.pdf.

  188. 188.

    Pérez-Pantoja D, Donoso R, Junca H, González B, Pieper DH. Phylogenomics of Aerobic Bacterial Degradation ofAromatics. In: Rojo F (ed). Aerobic Utilization of Hydrocarbons, Oils and Lipids. Cham: Springer; 2016.

  189. 189.

    Vandini A, Temmerman R, Frabetti A, Caselli E, Antonioli P, Balboni PG, et al. Hard surface biocontrol in hospitals using microbial-based cleaning products. PLoS ONE. 2014;9:e108598.

  190. 190.

    Caselli E, D’Accolti M, Vandini A, Lanzoni L, Camerada MT, Coccagna M, et al. Impact of a probiotic-based cleaning intervention on the microbiota ecosystem of the hospital surfaces: focus on the resistome remodulation. PLoS ONE. 2016;11:e0148857.

  191. 191.

    Nordengrün M, Michalik S, Völker U, Bröker BM, Gómez-Gascón L. The quest for bacterial allergens. Int J Med Microbiol. 2018;308:738–50.

  192. 192.

    Simon-Nobbe B, Denk U, Pöll V, Rid R, Breitenbach M. The spectrum of fungal allergy. Int. Arch. Allergy Immunol. 2008;145:58–86.

  193. 193.

    Araki A, Kawai T, Eitaki Y, Kanazawa A, Morimoto K, Nakayama K, et al. Relationship between selected indoor volatile organic compounds, so-called microbial VOC, and the prevalence of mucous membrane symptoms in single family homes. Sci Total Environ. 2010;408:2208–15.

  194. 194.

    Daisey JM, Angell WJ, Apte MG. Indoor air quality, ventilation and health symptoms in schools: an analysis of existing information. Indoor Air. 2003;13:53–64.

  195. 195.

    Sundell J, Levin H, Nazaroff WW, Cain WS, Fisk WJ, Grimsrud DT, et al. Ventilation rates and health: multidisciplinary review of the scientific literature. Indoor Air. 2011;21:191–204.

  196. 196.

    Simons E, Hwang S-A, Fitzgerald EF, Kielb C, Lin S. The impact of school building conditions on student absenteeism in Upstate New York. Am J Public Health. 2010;100:1679–86.

  197. 197.

    CDC. Asthma. Centers for Disease Control and Prevention | National Center for Health Statistics. 2019. https://www.cdc.gov/nchs/fastats/asthma.htm. Accessed 6 Feb 2019.

  198. 198.

    Hsu J, Qin X, Beavers SF, Mirabelli MC. Asthma-related school absenteeism, morbidity, and modifiable factors. Am J Prev Med. 2016;51:23–32.

  199. 199.

    Nunes C, Pereira AM, Morais-Almeida M. Asthma costs and social impact. Asthma Research and Practice. 2016;3:1.

  200. 200.

    Ciaccio CE, Barnes C, Kennedy K, Chan M, Portnoy J, Rosenwasser L. Home dust microbiota is disordered in homes of low-income asthmatic children. J Asthma. 2015;52:873–80.

  201. 201.

    Lynch SV, Wood RA, Boushey H, Bacharier LB, Bloomberg GR, Kattan M, et al. Effects of early-life exposure to allergens and bacteria on recurrent wheeze and atopy in urban children. J Allergy Clin Immunol. 2014;134:593–601.e12.

  202. 202.

    Hooks KB, O’Malley MA. Dysbiosis and its discontents. MBio. 2017;8:01492–17.

  203. 203.

    Chu W-L, Tneh S-Y, Ambu S. A survey of airborne algae and cyanobacteria within the indoor environment of an office building in Kuala Lumpur, Malaysia. Grana. 2013;52:207–20.

  204. 204.

    Bernstein IL, Safferman RS. Viable algae in house dust. Nature. 1970;227:851–2.

  205. 205.

    Böbel TS, Hackl SB, Langgartner D, Jarczok MN, Rohleder N, Rook GA, et al. Less immune activation following social stress in rural vs. urban participants raised with regular or no animal contact, respectively. Proc Natl Acad Sci USA. 2018;115:5259–64.

  206. 206.

    Rintala H, Pitkäranta M, Täubel M. Chapter 4 - Microbial Communities Associated with House Dust. In: Laskin AI, Sariaslani S, Gadd GM (eds). Advances in applied microbiology. Academic Press, 2012, pp 75–120.

  207. 207.

    Heederik D, von Mutius E. Does diversity of environmental microbial exposure matter for the occurrence of allergy and asthma? J Allergy Clin Immunol. 2012;130:44–50.

  208. 208.

    Vestergaard DV, Holst GJ, Basinas I, Elholm G, Schlünssen V, Linneberg A, et al. Pig Farmers’ homes harbor more diverse airborne bacterial communities than pig stables or suburban homes. Front Microbiol. 2018;9:870.

  209. 209.

    Cardona C, Lax S, Larsen P, Stephens B, Hampton-Marcell J, Edwardson CF, et al. Environmental sources of bacteria differentially influence host-associated microbial dynamics. mSystems. 2018;3:e00052-18.

  210. 210.

    McDonald D, Ackermann G, Khailova L, Baird C, Heyland D, Kozar R, et al. Extreme dysbiosis of the microbiome in critical illness. mSphere. 2016;1:e00199-16.

  211. 211.

    Brooks B, Firek BA, Miller CS, Sharon I, Thomas BC, Baker R, et al. Microbes in the neonatal intensive care unit resemble those found in the gut of premature infants. Microbiome. 2014;2:1.

  212. 212.

    Lax S, Sangwan N, Smith D, Larsen P, Handley KM, Richardson M, et al. Bacterial colonization and succession in a newly opened hospital. Sci Transl Med. 2017;9:eaah6500.

  213. 213.

    Parkinson AJ. The Arctic Human Health Initiative: a legacy of the International Polar Year 2007–9. Int J Circumpolar Health. 2013;72:21655.

  214. 214.

    Barker SF, Packer M, Scales PJ, Gray S, Snape I, Hamilton AJ. Pathogen reduction requirements for direct potable reuse in Antarctica: evaluating human health risks in small communities. Sci Total Environ. 2013;461–2:723–33.

  215. 215.

    Jin J-S, Touyama M, Yamada S, Yamazaki T, Benno Y. Alteration of a human intestinal microbiota under extreme life environment in the Antarctica. Biol Pharm Bull. 2014;37:1899–906.

  216. 216.

    Venkateswaran K, Vaishampayan P, Cisneros J, Pierson DL, Rogers SO, Perry J. International Space Station environmental microbiome - microbial inventories of ISS filter debris. Appl Microbiol Biotechnol. 2014;98:6453–66.

  217. 217.

    Phelan M. Why fungi adapt so well to life in space | Scienceline. Scienceline. 2018. https://scienceline.org/2018/03/fungi-love-to-grow-in-outer-space/. Accessed 10 Feb 2019.

  218. 218.

    Crucian BE, Choukèr A, Simpson RJ, Mehta S, Marshall G, Smith SM, et al. Immune system dysregulation during spaceflight: potential countermeasures for deep space exploration missions. Front Immunol. 2018;9:1437.

  219. 219.

    Wilson N. A Microbial Hitchhiker’s Guide to the Galaxy: researchers race to understand effects of deep space on microbiome. Bioscience. 2019;69:5–11.

  220. 220.

    Voorhies AA, Lorenzi HA. The challenge of maintaining a healthy microbiome during long-duration space missions. Front Astronomy Space Stations. 2016;3:23.

  221. 221.

    Romsdahl J, Blachowicz A, Chiang AJ, Singh N, Stajich JE, Kalkum M, et al. Characterization of Aspergillus niger Isolated from the International Space Station. mSystems. 2018;3:e00112-18.

  222. 222.

    Mahnert A, Moissl-Eichinger C, Zojer M, Bogumil D, Mizrahi I, Rattei T, et al. Man-made microbial resistances in built environments. Nat Commun. 2019;10:968.

  223. 223.

    Leung MHY, Wilkins D, Li EKT, Kong FKF, Lee PKH. Indoor-air microbiome in an urban subway network: diversity and dynamics. Appl Environ Microbiol. 2014;80:6760–70.

  224. 224.

    Be NA, Thissen JB, Fofanov VY, Allen JE, Rojas M, Golovko G, et al. Metagenomic analysis of the airborne environment in urban spaces. Microb Ecol. 2015;69:346–55.

  225. 225.

    Haahtela T, Holgate S, Pawankar R, Akdis CA, Benjaponpitak S, Caraballo L, et al. The biodiversity hypothesis and allergic disease: world allergy organization position statement. World Allergy Organ J. 2013;6:3.

  226. 226.

    Kim K, DuPont HL, Pickering LK. Outbreaks of diarrhea associated with Clostridium difficile and its toxin in day-care centers: evidence of person-to-person spread. J Pediatr. 1983;102:376–82.

  227. 227.

    Delmée M, Verellen G, Avesani V, Francois G. Clostridium difficile in neonates: serogrouping and epidemiology. Eur J Pediatr. 1988;147:36–40.

  228. 228.

    Rusin P, Maxwell S, Gerba C. Comparative surface-to-hand and fingertip-to-mouth transfer efficiency of gram-positive bacteria, gram-negative bacteria, and phage. J Appl Microbiol. 2002;93:585–92.

  229. 229.

    Ziskind G. Particle resuspension from surfaces: revisited and re-evaluated. Rev Chem Eng. 2006;22:1–123.

  230. 230.

    Jou J, Ebrahim J, Shofer FS, Hamilton KW, Stern J, Han JH, et al. Environmental transmission of Clostridium difficile: association between hospital room size and C. difficile Infection. Infect Control Hosp Epidemiol. 2015;36:564–8.

  231. 231.

    Freedberg DE, Salmasian H, Cohen B, Abrams JA, Larson EL. Receipt of antibiotics in hospitalized patients and risk for Clostridium difficile infection in subsequent patients who occupy the same bed. JAMA Intern Med. 2016;176:1801–8.

  232. 232.

    Lowe TM, Chan PP. tRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Res. 2016;44:W54–7.

  233. 233.

    Kim H-Y, Estes CR, Duncan AG, Wade BD, Cleary FC, Lloyd CR, et al. Real-time detection of microbial contamination. IEEE Eng Med Biol Mag. 2004;23:122–9.

  234. 234.

    Fahimipour AK, Ben Mamaar S, McFarland AG, Blaustein RA, Chen J, Glawe AJ, et al. Antimicrobial chemicals associate with microbial function and antibiotic resistance indoors. mSystems. 2018;3:e00200-18.

  235. 235.

    Emerson JB, Adams RI, Román CMB, Brooks B, Coil DA, Dahlhausen K, et al. Schrödinger’s microbes: Tools for distinguishing the living from the dead in microbial ecosystems. Microbiome. 2017;5:86.

  236. 236.

    Klein AM, Bohannan BJM, Jaffe DA, Levin DA, Green JL. Molecular evidence for metabolically active bacteria in the atmosphere. Front Microbiol. 2016;7:772.

  237. 237.

    Nocker A, Cheung C-Y, Camper AK. Comparison of propidium monoazide with ethidium monoazide for differentiation of live vs. dead bacteria by selective removal of DNA from dead cells. J Microbiol Methods. 2006;67:310–20.

  238. 238.

    Gao M, Ahern J, Koshland CP. Perceived built environment and health-related quality of life in four types of neighborhoods in Xi’an, China. Health Place. 2016;39:110–5.

  239. 239.

    Miller JD, Sun M, Gilyan A, Roy J, Rand TG. Inflammation-associated gene transcription and expression in mouse lungs induced by low molecular weight compounds from fungi from the built environment. Chem Biol Interact. 2010;183:113–24.

  240. 240.

    Perlman RL. Mouse models of human disease: an evolutionary perspective. Evol Med Public Health. 2016;2016:170–6.

  241. 241.

    Dai D, Prussin AJ,2nd, Marr LC, Vikesland PJ, Edwards MA, Pruden A. Factors shaping the human exposome in the built environment: opportunities for engineering control. Environ Sci Technol. 2017;51:7759–74.

  242. 242.

    Jiang C, Wang X, Li X, Inlora J, Wang T, Liu Q, et al. Dynamic human environmental exposome revealed by longitudinal personal monitoring. Cell. 2018;175:277–91.e31.

  243. 243.

    Stucki AO, Stucki JD, Hall SRR, Felder M, Mermoud Y, Schmid RA, et al. A lung-on-a-chip array with an integrated bio-inspired respiration mechanism. Lab Chip. 2015;15:1302–10.

  244. 244.

    Cho S, Yoon J-Y. Organ-on-a-chip for assessing environmental toxicants. Curr Opin Biotechnol. 2017;45:34–42.

  245. 245.

    Arnold C. Rethinking sterile: the hospital microbiome. Environ Health Perspect. 2014;122:A182–7.

Download references

Acknowledgements

The authors appreciate the efforts of Dr. Roo Vandegrift, Sam Velasquez, Jeff Kline, Fiona Curliss, and Paul Ward in reviewing this manuscript. The authors would also like to thank Mira Zimmerman, Delaney Hetrick, and Julia May for their graphical contributions. This work was funded by grants from the Alfred P. Sloan Foundation to the Biology and the Built Environment Center at the University of Oregon.

Author information

SLI conceived of scope, and contributed to writing and editing. PFH and SL contributed to literature review, writing, and editing. GAM, LD, MF, KVDW, and GM contributed to editing.

Correspondence to Suzanne L. Ishaq.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Keywords

  • Biomonitoring
  • Dermal exposure
  • Disease
  • Environmental monitoring
  • Epidemiology
  • Personal exposure