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Microbial Exchange via Fomites and Implications for Human Health

  • Brent StephensEmail author
  • Parham Azimi
  • Megan S. Thoemmes
  • Mohammad Heidarinejad
  • Joseph G. Allen
  • Jack A. Gilbert
Biology and Pollution (G O’Mullan and R Boopathy, Section Editors)
Part of the following topical collections:
  1. Topical Collection on Biology and Pollution

Abstract

Purpose of Review

Fomites are inanimate objects that become colonized with microbes and serve as potential intermediaries for transmission to/from humans. This review summarizes recent literature on fomite contamination and microbial survival in the built environment, transmission between fomites and humans, and implications for human health.

Recent Findings

Applications of molecular sequencing techniques to analyze microbial samples have increased our understanding of the microbial diversity that exists in the built environment. This growing body of research has established that microbial communities on surfaces include substantial diversity, with considerable dynamics. While many microbial taxa likely die or lay dormant, some organisms survive, including those that are potentially beneficial, benign, or pathogenic. Surface characteristics also influence microbial survival and rates of transfer to and from humans. Recent research has combined experimental data, mechanistic modeling, and epidemiological approaches to shed light on the likely contributors to microbial exchange between fomites and humans and their contributions to adverse (and even potentially beneficial) human health outcomes.

Summary

In addition to concerns for fomite transmission of potential pathogens, new analytical tools have uncovered other microbial matters that can be transmitted indirectly via fomites, including entire microbial communities and antibiotic-resistant bacteria. Mathematical models and epidemiological approaches can provide insight on human health implications. However, both are subject to limitations associated with study design, and there is a need to better understand appropriate input model parameters. Fomites remain an important mechanism of transmission of many microbes, along with direct contact and short- and long-range aerosols.

Keywords

Microbiology Built environment Contamination Infectious disease transmission Aerosol Quantitative microbial risk assessment (QMRA) 

Notes

Acknowledgements

BS and JAG were supported by the Alfred P. Sloan Foundation’s program on the Microbiology of the Built Environment (MoBE); BS was supported in part by an ASHRAE New Investigator Award.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflicts of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Nutton V. The seeds of disease: an explanation of contagion and infection from the Greeks to the renaissance. Med Hist. 1983;27:1–34.CrossRefGoogle Scholar
  2. 2.
    Klepeis NE, Nelson WC, Ott WR, Robinson JP, Tsang AM, Switzer P, et al. The National Human Activity Pattern Survey (NHAPS): a resource for assessing exposure to environmental pollutants. J Expo Anal Environ Epidemiol. 2001;11:231–52.CrossRefGoogle Scholar
  3. 3.
    •• 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. This study characterized the longitudinal succession of bacterial communities on indoor surfaces in 7 homes, finding that microbial communities were largely sourced from humans and were identifiable by family. CrossRefGoogle Scholar
  4. 4.
    •• Chase J, Fouquier J, Zare M, Sonderegger DL, Knight R, Kelley ST, et al. Geography and location are the primary drivers of office microbiome composition. mSystems. 2016;1:e00022-16. This study investigated the impacts of a wide variety of parameters including geography, material type, human interaction, location in a room, seasonal variation, and indoor and microenvironmental parameters on bacterial communities in offices. CrossRefGoogle Scholar
  5. 5.
    • Stobnicka A, Gołofit-Szymczak M, Wójcik-Fatla A, Zając V, Korczyńska-Smolec J, Górny RL. Prevalence of human parainfluenza viruses and noroviruses genomes on office fomites. Food Environ Virol. 2018;10:133–40. This study evaluated the potential role of office fomites in respiratory and enteric virus transmission by assessing the occurrence of viruses on 130 surfaces from both open-space and non-open-space rooms in office buildings during a 9-month period. CrossRefGoogle Scholar
  6. 6.
    • Thompson K-A, Bennett AM. Persistence of influenza on surfaces. J Hosp Infect. 2017;95:194–9. This study assessed the viability of five influenza strains seeded on three surfaces over the course of several weeks, finding that viable influenza was recovered from surfaces for up to 2 weeks while influenza genetic material could be detected by PCR for more than 7 weeks. CrossRefGoogle Scholar
  7. 7.
    • Malcolm KC, Caceres SM, Honda JR, Davidson RM, Epperson LE, Strong M, et al. Mycobacterium abscessus displays fitness for fomite transmission. Appl Environ Microbiol. 2017;83.  https://doi.org/10.1128/AEM.00562-17. This article demonstrated M. abscessus growth on surfaces is enhanced in the presence of house dust, surviving desiccation for up to 2 weeks.
  8. 8.
    • Missri L, Smiljkovski D, Prigent G, Lesenne A, Obadia T, Joumaa M, et al. Bacterial colonization of healthcare workers’ mobile phones in the ICU and effectiveness of sanitization. J Occup Environ Hyg. 2018:1–4. This article assessed the prevalence of bacterial colonization of 56 healthcare workers’ mobile phones in an intensive care unit both immediately before and 5 min after sanitization of the phones with bactericidal wipes, finding that colonization with pathogens was frequent but colonization with multi-drug resistant bacteria was rare. Google Scholar
  9. 9.
    •• Smibert OC, Aung AK, Woolnough E, Carter GP, Schultz MB, Howden BP, et al. Mobile phones and computer keyboards: unlikely reservoirs of multidrug-resistant organisms in the tertiary intensive care unit. J Hosp Infect. 2018;99:295–8. This article sampled for a large number of multi-drug resistant organisms (MRDOs) on medical staff personal mobile phones, departmental phones, and ICU keyboards, finding that MRSA was isolated from only two phones and that these fomites appear unlikely to contribute much to hospital-acquired MRDOs. CrossRefGoogle Scholar
  10. 10.
    • Haun N, Hooper-Lane C, Safdar N. Healthcare personnel attire and devices as fomites: a systematic review. Infect Control Hosp Epidemiol. 2016;37:1367–73. This article reviewed a large number of studies that assessed contamination of fomites in healthcare settings and found high variability in contamination rates by fomite type, microbial agent, and sampling and analysis technique. CrossRefGoogle Scholar
  11. 11.
    •• Jackson SS, Harris AD, Magder LS, Stafford KA, Johnson JK, Miller LG, et al. Bacterial burden is associated with increased transmission to health care workers from patients colonized with vancomycin-resistant Enterococcus. Am J Infect Control. 2019;47:13–7. This article found that the bacterial contamination of HCW gloves and gowns was associated with the vancomycin-resistant Enterococcus (VRE) on body sites of patients with VRE, suggesting that ICU patients with a higher bacterial burden were more likely to transmit VREs to HCWs. CrossRefGoogle Scholar
  12. 12.
    •• Hartmann EM, Hickey R, Hsu T, Betancourt Román CM, Chen J, Schwager R, et al. Antimicrobial chemicals are associated with elevated antibiotic resistance genes in the indoor dust microbiome. Environ Sci Technol. 2016;50:9807–15. This article was the first to find an association between antibiotic resistance genes and antimicrobial chemicals in dust samples from indoor environments. CrossRefGoogle Scholar
  13. 13.
    •• 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. This article demonstrated that the loss of microbial diversity on surfaces is correlated with an increase in antibiotic resistance, suggesting there is a need for implementing strategies to restore bacterial diversity in certain built environments. CrossRefGoogle Scholar
  14. 14.
    • Greene C, Vadlamudi G, Eisenberg M, Foxman B, Koopman J, Xi C. Fomite-fingerpad transfer efficiency (pick-up and deposit) of Acinetobacter baumannii—with and without a latex glove. Am J Infect Control. 2015;43:928–34. This article estimated the transfer efficiency of Acinetobacter baumannii with and without latex glove use from the finger pad to a fomite and from a fomite to the finger pad. CrossRefGoogle Scholar
  15. 15.
    • Killingley B, Greatorex J, Digard P, Wise H, Garcia F, Varsani H, et al. The environmental deposition of influenza virus from patients infected with influenza A(H1N1)pdm09: implications for infection prevention and control. J Infect Public Health. 2016;9:278–88. This article used a novel approach to quantify and correlate the amount of virus recovered from the nares of infected subjects with that recovered from their immediate environment in the community and hospital settings. CrossRefGoogle Scholar
  16. 16.
    • Kunkel SA, Azimi P, Zhao H, Stark BC, Stephens B. Quantifying the size-resolved dynamics of indoor bioaerosol transport and control. Indoor Air. 2017;27:977–87. This article used a human respiratory activity simulator to aerosolize two model organisms and measured the abundance of microbes on surfaces and in bioaerosols in multiple locations in an apartment unit operating with different HVAC particle filters, finding that DNA from both organisms was detected under all test conditions in all air samples up to 7 m away from the source, with concentrations decreasing at greater distances from the bioaerosol source and with higher efficiency filters. CrossRefGoogle Scholar
  17. 17.
    •• Reynolds KA, Sexton JD, Pivo T, Humphrey K, Leslie RA, Gerba CP. Microbial transmission in an outpatient clinic and impact of an intervention with an ethanol-based disinfectant. Am J Infect Control. 2019;47:128–32. This article used a novel method to evaluate microbial transmission in an outpatient clinic and the impact of a disinfectant by placing a viral tracer on two fomites at the beginning of the day and tracking its presence throughout the remainder of the day. CrossRefGoogle Scholar
  18. 18.
    • Xiao S, Li Y, Wong T, Hui DSC. Role of fomites in SARS transmission during the largest hospital outbreak in Hong Kong. PLoS One. 2017;12:e0181558. This article used a multi-agent model to predict the distributions of infection risk during the well-known Ward 8A SARS outbreak in 2003 in the Prince of Wales Hospital in Hong Kong, concluding that the SARS coronavirus was most likely spread via a combination of long-range airborne and fomite routes. CrossRefGoogle Scholar
  19. 19.
    • Zhang N, Li Y. Transmission of influenza A in a student office based on realistic person-to-person contact and surface touch behaviour. Int J Environ Res Public Health. 2018;15:1699. This study simulated the transmission of influenza A virus in a graduate student office via three transmission routes, informed by novel data on more than 3500 person-to-person contacts and 127,000 surface touches obtained by video camera recording. CrossRefGoogle Scholar
  20. 20.
    • Greene C, Ceron NH, Eisenberg MC, Koopman J, Miller JD, Xi C, et al. Asymmetric transfer efficiencies between fomites and fingers: impact on model parameterization. Am J Infect Control. 2018;46:620–6. This article used a model of Acinetobacter baumannii to demonstrate the effects that incorrect assumptions for pathogen transfer efficiency between fomites and fingers (and between fingers and fomites) can have on QMRA model predicted results. CrossRefGoogle Scholar
  21. 21.
    • Weir MH, Shibata T, Masago Y, Cologgi DL, Rose JB. Effect of surface sampling and recovery of viruses and non-spore-forming Bacteria on a quantitative microbial risk assessment model for fomites. Environ Sci Technol. 2016;50:5945–52. This article demonstrated the impact that QMRA model inputs can have on model results, including recovery efficiency from several non-porous fomites, fomite material, surface area, recovery tool, and initial fomite concentrations. CrossRefGoogle Scholar
  22. 22.
    • Kutter JS, Spronken MI, Fraaij PL, Fouchier RA, Herfst S. Transmission routes of respiratory viruses among humans. Curr Opin Virol. 2018;28:142–51. This article summarized the state of knowledge of dominant transmission routes for a number of human respiratory viruses and noted that many studies on inter-human transmission routes remain inconclusive. CrossRefGoogle Scholar
  23. 23.
    •• 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. This article found associations between housing characteristics and bacterial and fungal communities in homes of asthmatic children. CrossRefGoogle Scholar
  24. 24.
    • O’Connor GT, Lynch SV, Bloomberg GR, et al. Early-life home environment and risk of asthma among inner-city children. J Allergy Clin Immunol. 2018;141:1468–75. This article found that higher indoor levels of pet or pest allergens in infancy, as well as the abundance of some bacterial taxa, were associated with a lower risk of asthma in a birth cohort of high-risk inner-city children. CrossRefGoogle Scholar
  25. 25.
    Kelley ST, Gilbert JA. Studying the microbiology of the indoor environment. Genome Biol. 2013;14:202.CrossRefGoogle Scholar
  26. 26.
    Konya T, Scott JA. Recent advances in the microbiology of the built environment. Curr Sustain Renew Energy Rep. 2014;1:35–42.Google Scholar
  27. 27.
    Gilbert JA, Stephens B. Microbiology of the built environment. Nat Rev Microbiol. 2018;16:661–70.CrossRefGoogle Scholar
  28. 28.
    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.CrossRefGoogle Scholar
  29. 29.
    Hospodsky D, Qian J, Nazaroff WW, Yamamoto N, Bibby K, Rismani-Yazdi H, et al. Human occupancy as a source of indoor airborne bacteria. PLoS One. 2012;7:e34867.CrossRefGoogle Scholar
  30. 30.
    Qian J, Hospodsky D, Yamamoto N, Nazaroff WW, Peccia J. Size-resolved emission rates of airborne bacteria and fungi in an occupied classroom. Indoor Air. 2012;22:339–51.CrossRefGoogle Scholar
  31. 31.
    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;7:1262–73.CrossRefGoogle Scholar
  32. 32.
    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.CrossRefGoogle Scholar
  33. 33.
    Lax S, Sangwan N, Smith D, et al. Bacterial colonization and succession in a newly opened hospital. Sci Transl Med. 2017;9:eaah6500.CrossRefGoogle Scholar
  34. 34.
    Lai PS, Allen JG, Hutchinson DS, Ajami NJ, Petrosino JF, Winters T, et al. Impact of environmental microbiota on human microbiota of workers in academic mouse research facilities: an observational study. PLoS One. 2017;12:e0180969.CrossRefGoogle Scholar
  35. 35.
    Adams RI, Bateman AC, Bik HM, Meadow JF. Microbiota of the indoor environment: a meta-analysis. Microbiome. 2015;3.  https://doi.org/10.1186/s40168-015-0108-3.
  36. 36.
    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.CrossRefGoogle Scholar
  37. 37.
    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.CrossRefGoogle Scholar
  38. 38.
    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.CrossRefGoogle Scholar
  39. 39.
    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.CrossRefGoogle Scholar
  40. 40.
    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.CrossRefGoogle Scholar
  41. 41.
    Stephens B. What have we learned about the microbiomes of indoor environments? mSystems. 2016;1:e00083-16.CrossRefGoogle Scholar
  42. 42.
    Barberán A, Dunn RR, Reich BJ, Pacifici K, Laber EB, Menninger HL, et al. The ecology of microscopic life in household dust. Proc R Soc B Biol Sci. 2015;282:20151139.CrossRefGoogle Scholar
  43. 43.
    Gibbons SM. The built environment is a microbial wasteland. mSystems. 2016;1:e00033-16.CrossRefGoogle Scholar
  44. 44.
    Dannemiller KC, Mendell MJ, Macher JM, Kumagai K, Bradman A, Holland N, et al. Next-generation DNA sequencing reveals that low fungal diversity in house dust is associated with childhood asthma development. Indoor Air. 2014;24:236–47.CrossRefGoogle Scholar
  45. 45.
    Karvonen AM, Hyvärinen A, Rintala H, Korppi M, Täubel M, Doekes G, et al. Quantity and diversity of environmental microbial exposure and development of asthma: a birth cohort study. Allergy. 2014;69:1092–101.CrossRefGoogle Scholar
  46. 46.
    Lynch SV, Wood RA, Boushey H, 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.CrossRefGoogle Scholar
  47. 47.
    Ege MJ, Mayer M, Normand A-C, Genuneit J, Cookson WOCM, Braun-Fahrländer C, et al. Exposure to environmental microorganisms and childhood asthma. N Engl J Med. 2011;364:701–9.CrossRefGoogle Scholar
  48. 48.
    Stein MM, Hrusch CL, Gozdz J, Igartua C, Pivniouk V, Murray SE, et al. Innate immunity and asthma risk in Amish and Hutterite farm children. N Engl J Med. 2016;375:411–21.CrossRefGoogle Scholar
  49. 49.
    Schuijs MJ, Willart MA, Vergote K, Gras D, Deswarte K, Ege MJ, et al. Farm dust and endotoxin protect against allergy through A20 induction in lung epithelial cells. Science. 2015;349:1106–10.CrossRefGoogle Scholar
  50. 50.
    Gibbons SM, Schwartz T, Fouquier J, Mitchell M, Sangwan N, Gilbert JA, et al. Ecological succession and viability of human-associated microbiota on restroom surfaces. Appl Environ Microbiol. 2015;81:765–73.CrossRefGoogle Scholar
  51. 51.
    Hegarty B, Dannemiller KC, Peccia J. Gene expression of indoor fungal communities under damp building conditions: implications for human health. Indoor Air. 2018;28:548–58.CrossRefGoogle Scholar
  52. 52.
    Hu J, Ben Maamar S, Glawe AJ, Gottel N, Gilbert JA, Hartmann EM. Impacts of indoor surface finishes on bacterial viability. Indoor Air. 2019.  https://doi.org/10.1111/ina.12558.
  53. 53.
    Flores GE, Bates ST, Knights D, Lauber CL, Stombaugh J, Knight R, et al. Microbial biogeography of public restroom surfaces. PLoS One. 2011;6:e28132.CrossRefGoogle Scholar
  54. 54.
    Flores GE, Bates ST, Caporaso JG, Lauber CL, Leff JW, Knight R, et al. Diversity, distribution and sources of bacteria in residential kitchens. Environ Microbiol. 2013;15:588–96.CrossRefGoogle Scholar
  55. 55.
    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.CrossRefGoogle Scholar
  56. 56.
    Kelley ST, Theisen U, Angenent LT, St. Amand A, Pace NR. Molecular analysis of shower curtain biofilm microbes. Appl Environ Microbiol. 2004;70:4187–92.CrossRefGoogle Scholar
  57. 57.
    Adams RI, Lymperopoulou DS, Misztal PK, de Cassia Pessotti R, Behie SW, Tian Y, et al. Microbes and associated soluble and volatile chemicals on periodically wet household surfaces. Microbiome. 2017;5.  https://doi.org/10.1186/s40168-017-0347-6.
  58. 58.
    Yano T, Kubota H, Hanai J, Hitomi J, Tokuda H. Stress tolerance of methylobacterium biofilms in bathrooms. Microbes Environ. 2012.  https://doi.org/10.1264/jsme2.ME12146.
  59. 59.
    Prussin AJ, Garcia EB, Marr LC. Total concentrations of virus and bacteria in indoor and outdoor air. Environ Sci Technol Lett. 2015;150310105417006.Google Scholar
  60. 60.
    Boone S, Gerba C. The occurrence of influenza A virus on household and day care center fomites. J Infect. 2005;51:103–9.CrossRefGoogle Scholar
  61. 61.
    Bright KR, Boone SA, Gerba CP. Occurrence of bacteria and viruses on elementary classroom surfaces and the potential role of classroom hygiene in the spread of infectious diseases. J Sch Nurs. 2010;26:33–41.CrossRefGoogle Scholar
  62. 62.
    Jones EL, Kramer A, Gaither M, Gerba CP. Role of fomite contamination during an outbreak of norovirus on houseboats. Int J Environ Health Res. 2007;17:123–31.CrossRefGoogle Scholar
  63. 63.
    Pappas DE, Hendley JO, Schwartz RH. Respiratory viral RNA on toys in pediatric office waiting rooms. Pediatr Infect Dis J. 2010;29:102–4.CrossRefGoogle Scholar
  64. 64.
    Gralton J, McLaws M-L, Rawlinson WD. Personal clothing as a potential vector of respiratory virus transmission in childcare settings: personal clothing as transmission vector. J Med Virol. 2015;87:925–30.CrossRefGoogle Scholar
  65. 65.
    Butz AM, Fosarelli P, Dick J, Cusack T, Yolken R. Prevalence of rotavirus on high-risk fomites in day-care facilities. Pediatrics. 1993;92:202–5.Google Scholar
  66. 66.
    Soule H, Genoulaz O, Gratacap-Cavallier B, Mallaret MR, Morand P, François P, et al. Monitoring rotavirus environmental contamination in a pediatric unit using polymerase chain reaction. Infect Control Hosp Epidemiol. 1999;20:432–4.CrossRefGoogle Scholar
  67. 67.
    Dowell SF, Simmerman JM, Erdman DD, Wu J-SJ, Chaovavanich A, Javadi M, et al. Severe acute respiratory syndrome coronavirus on hospital surfaces. Clin Infect Dis. 2004;39:652–7.CrossRefGoogle Scholar
  68. 68.
    Boone SA, Gerba CP. The prevalence of human parainfluenza virus 1 on indoor office fomites. Food Environ Virol. 2010;2:41–6.CrossRefGoogle Scholar
  69. 69.
    Ganime AC, Carvalho-Costa FA, Santos M, Costa Filho R, Leite JPG, Miagostovich MP. Viability of human adenovirus from hospital fomites: viability of human adenovirus from fomites. J Med Virol. 2014;86:2065–9.CrossRefGoogle Scholar
  70. 70.
    Khan RM, Al-Dorzi HM, Al Johani S, Balkhy HH, Alenazi TH, Baharoon S, et al. Middle East respiratory syndrome coronavirus on inanimate surfaces: a risk for health care transmission. Am J Infect Control. 2016;44:1387–9.CrossRefGoogle Scholar
  71. 71.
    Weber TP, Stilianakis NI. Inactivation of influenza A viruses in the environment and modes of transmission: a critical review. J Infect. 2008;57:361–73.CrossRefGoogle Scholar
  72. 72.
    Bean B, Moore BM, Sterner B, Peterson LR, Gerding DN, Balfour HH. Survival of influenza viruses on environmental surfaces. J Infect Dis. 1982;146:47–51.CrossRefGoogle Scholar
  73. 73.
    Greatorex JS, Digard P, Curran MD, Moynihan R, Wensley H, Wreghitt T, et al. Survival of influenza A(H1N1) on materials found in households: implications for infection control. PLoS One. 2011;6:e27932.CrossRefGoogle Scholar
  74. 74.
    Mukherjee DV, Cohen B, Bovino ME, Desai S, Whittier S, Larson EL. Survival of influenza virus on hands and fomites in community and laboratory settings. Am J Infect Control. 2012;40:590–4.CrossRefGoogle Scholar
  75. 75.
    Thomas Y, Vogel G, Wunderli W, Suter P, Witschi M, Koch D, et al. Survival of influenza virus on banknotes. Appl Environ Microbiol. 2008;74:3002–7.CrossRefGoogle Scholar
  76. 76.
    Oxford J, Berezin EN, Courvalin P, Dwyer DE, Exner M, Jana LA, et al. The survival of influenza A(H1N1)pdm09 virus on 4 household surfaces. Am J Infect Control. 2014;42:423–5.CrossRefGoogle Scholar
  77. 77.
    Perry KA, Coulliette AD, Rose LJ, Shams AM, Edwards JR, Noble-Wang JA. Persistence of influenza A (H1N1) virus on stainless steel surfaces. Appl Environ Microbiol. 2016;82:3239–45.CrossRefGoogle Scholar
  78. 78.
    McDevitt J, Rudnick S, First M, Spengler J. Role of absolute humidity in the inactivation of influenza viruses on stainless steel surfaces at elevated temperatures. Appl Environ Microbiol. 2010;76:3943–7.CrossRefGoogle Scholar
  79. 79.
    Shaman J, Kohn M. Absolute humidity modulates influenza survival, transmission, and seasonality. Proc Natl Acad Sci. 2009;106:3243–8.CrossRefGoogle Scholar
  80. 80.
    Sakaguchi H, Wada K, Kajioka J, Watanabe M, Nakano R, Hirose T, et al. Maintenance of influenza virus infectivity on the surfaces of personal protective equipment and clothing used in healthcare settings. Environ Health Prev Med. 2010;15:344–9.CrossRefGoogle Scholar
  81. 81.
    Boone SA, Gerba CP. Significance of fomites in the spread of respiratory and enteric viral disease. Appl Environ Microbiol. 2007;73:1687–96.CrossRefGoogle Scholar
  82. 82.
    van Doremalen N, Bushmaker T, Munster VJ. Stability of Middle East respiratory syndrome coronavirus (MERS-CoV) under different environmental conditions. Euro Surveill. 2013;18.Google Scholar
  83. 83.
    Marks LR, Reddinger RM, Hakansson AP. Biofilm formation enhances fomite survival of Streptococcus pneumoniae and Streptococcus pyogenes. Infect Immun. 2014;82:1141–6.CrossRefGoogle Scholar
  84. 84.
    Jones TM, Lutz EA. Environmental survivability and surface sampling efficiencies for Pseudomonas aeruginosa on various fomites. J Environ Health. 2014;76:16–20.Google Scholar
  85. 85.
    CDC. Antibiotic resistance threats in the United States: U.S. Department of Health and Human Services Centers for Disease Control and Prevention; 2013.Google Scholar
  86. 86.
    Davis MF, Iverson SA, Baron P, Vasse A, Silbergeld EK, Lautenbach E, et al. Household transmission of meticillin-resistant Staphylococcus aureus and other staphylococci. Lancet Infect Dis. 2012;12:703–16.CrossRefGoogle Scholar
  87. 87.
    Simões RR, Aires-de-Sousa M, Conceição T, Antunes F, da Costa PM, de Lencastre H. High prevalence of EMRSA-15 in Portuguese public buses: a worrisome finding. PLoS One. 2011;6:e17630.CrossRefGoogle Scholar
  88. 88.
    Conceição T, Diamantino F, Coelho C, de Lencastre H, Aires-de-Sousa M. Contamination of public buses with MRSA in Lisbon, Portugal: a possible transmission route of major MRSA clones within the community. PLoS One. 2013;8:e77812.CrossRefGoogle Scholar
  89. 89.
    Bhoonderowa A, Gookool S, Biranjia-Hurdoyal SD. The importance of mobile phones in the possible transmission of bacterial infections in the community. J Community Health. 2014;39:965–7.CrossRefGoogle Scholar
  90. 90.
    Kanamori H, Rutala WA, Weber DJ. The role of patient care items as a fomite in healthcare-associated outbreaks and infection prevention. Clin Infect Dis. 2017;65:1412–9.CrossRefGoogle Scholar
  91. 91.
    Harris PNA, Ashhurst-Smith C, Berenger SJ, Shoobert A, Ferguson JK. Adhesive tape in the health care setting: another high-risk fomite? Med J Aust. 2011;196:34.CrossRefGoogle Scholar
  92. 92.
    Feldman J, Feldman J, Feldman M. Women doctors’ purses as an unrecognized fomite. Del Med J. 2012;84:277–80.Google Scholar
  93. 93.
    Julian T, Singh A, Rousseau J, Weese J. Methicillin-resistant staphylococcal contamination of cellular phones of personnel in a veterinary teaching hospital. BMC Res Notes. 2012;5:193.CrossRefGoogle Scholar
  94. 94.
    Grimmond T, Neelakanta A, Miller B, Saiyed A, Gill P, Cadnum J, et al. A microbiological study to investigate the carriage and transmission-potential of Clostridium difficile spores on single-use and reusable sharps containers. Am J Infect Control. 2018;46:1154–9.CrossRefGoogle Scholar
  95. 95.
    Mitchell JB, Sifuentes LY, Wissler A, Abd-Elmaksoud S, Lopez GU, Gerba CP. Modelling of ultraviolet light inactivation kinetics of methicillin-resistant Staphylococcus aureus , vancomycin-resistant Enterococcus , Clostridium difficile spores and murine norovirus on fomite surfaces. J Appl Microbiol. 2019;126:58–67.CrossRefGoogle Scholar
  96. 96.
    Reitzel R, Rosenblatt J, Jiang Y, Hachem R, Raad I. Disposable gendine antimicrobial gloves for preventing transmission of pathogens in health care settings. Am J Infect Control. 2014;42:55–9.CrossRefGoogle Scholar
  97. 97.
    Falagas ME, Makris GC. Probiotic bacteria and biosurfactants for nosocomial infection control: a hypothesis. J Hosp Infect. 2009;71:301–6.CrossRefGoogle Scholar
  98. 98.
    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.CrossRefGoogle Scholar
  99. 99.
    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.CrossRefGoogle Scholar
  100. 100.
    Caselli E, Brusaferro S, Coccagna M, Arnoldo L, Berloco F, Antonioli P, et al. Reducing healthcare-associated infections incidence by a probiotic-based sanitation system: a multicentre, prospective, intervention study. PLoS One. 2018;13:e0199616.CrossRefGoogle Scholar
  101. 101.
    Caselli E, Arnoldo L, Rognoni C, D’Accolti M, Soffritti I, Lanzoni L, et al. Impact of a probiotic-based hospital sanitation on antimicrobial resistance and HAI-associated antimicrobial consumption and costs: a multicenter study. Infect Drug Resist. 2019;12:501–10.CrossRefGoogle Scholar
  102. 102.
    Caselli E, Antonioli P, Mazzacane S. Safety of probiotics used for hospital environmental sanitation. J Hosp Infect. 2016;94:193–4.CrossRefGoogle Scholar
  103. 103.
    Tuladhar E, Hazeleger WC, Koopmans M, Zwietering MH, Duizer E, Beumer RR. Transfer of noroviruses between fingers and fomites and food products. Int J Food Microbiol. 2013;167:346–52.CrossRefGoogle Scholar
  104. 104.
    Moore G, Dunnill CW, Wilson APR. The effect of glove material upon the transfer of methicillin-resistant Staphylococcus aureus to and from a gloved hand. Am J Infect Control. 2013;41:19–23.CrossRefGoogle Scholar
  105. 105.
    Koenig DW, Korir-Morrison C, Hoffman DR. Transfer efficiency of Staphylococcus aureus between nitrile exam gloves and nonporous fomites. Am J Infect Control. 2016;44:245–6.CrossRefGoogle Scholar
  106. 106.
    Lopez GU, Kitajima M, Havas A, Gerba CP, Reynolds KA. Evaluation of a disinfectant wipe intervention on fomite-to-finger microbial transfer. Appl Environ Microbiol. 2014;80:3113–8.CrossRefGoogle Scholar
  107. 107.
    Winther B, McCue K, Ashe K, Rubino JR, Hendley JO. Environmental contamination with rhinovirus and transfer to fingers of healthy individuals by daily life activity. J Med Virol. 2007;79:1606–10.CrossRefGoogle Scholar
  108. 108.
    Suwantarat N, Supple LA, Cadnum JL, Sankar T, Donskey CJ. Quantitative assessment of interactions between hospitalized patients and portable medical equipment and other fomites. Am J Infect Control. 2017;45:1276–8.CrossRefGoogle Scholar
  109. 109.
    Sassi HP, Reynolds KA, Pepper IL, Gerba CP. Evaluation of hospital-grade disinfectants on viral deposition on surfaces after toilet flushing. Am J Infect Control. 2018;46:507–11.CrossRefGoogle Scholar
  110. 110.
    Booth CM, Frost G. Potential distribution of viable norovirus post simulated vomiting. J Hosp Infect. 2019;102:304–10.  https://doi.org/10.1016/j.jhin.2019.02.010.CrossRefGoogle Scholar
  111. 111.
    Pitol AK, Bischel HN, Boehm AB, Kohn T, Julian TR. Transfer of enteric viruses adenovirus and Coxsackie virus and bacteriophage MS2 from liquid to human skin. Appl Environ Microbiol. 2018;84.  https://doi.org/10.1128/AEM.01809-18.
  112. 112.
    Haas CN, Rose JB, Gerba CP. Quantitative microbial risk assessment: Haas/quantitative microbial risk assessment; 2014.  https://doi.org/10.1002/9781118910030.CrossRefGoogle Scholar
  113. 113.
    Sze To GN, Chao CYH. Review and comparison between the Wells-Riley and dose-response approaches to risk assessment of infectious respiratory diseases. Indoor Air. 2010;20:2–16.CrossRefGoogle Scholar
  114. 114.
    Nicas M, Jones RM. Relative contributions of four exposure pathways to influenza infection risk. Risk Anal. 2009;29:1292–303.CrossRefGoogle Scholar
  115. 115.
    Nicas M, Sun G. An integrated model of infection risk in a health-care environment. Risk Anal. 2006;26:1085–96.CrossRefGoogle Scholar
  116. 116.
    Jones RM, Masago Y, Bartrand T, Haas CN, Nicas M, Rose JB. Characterizing the risk of infection from Mycobacterium tuberculosis in commercial passenger aircraft using quantitative microbial risk assessment. Risk Anal. 2009;29:355–65.CrossRefGoogle Scholar
  117. 117.
    Jones RM, Adida E. Influenza infection risk and predominate exposure route: uncertainty analysis. Risk Anal. 2011;31:1622–31.CrossRefGoogle Scholar
  118. 118.
    Jones RM, Nicas M. Benchmarking of a Markov multizone model of contaminant transport. Ann Occup Hyg. 2014;58:1018–31.Google Scholar
  119. 119.
    Jones RM, Nicas M. Experimental evaluation of a Markov multizone model of particulate contaminant transport. Ann Occup Hyg. 2014;58:1032–45.Google Scholar
  120. 120.
    Kraay ANM, Hayashi MAL, Hernandez-Ceron N, Spicknall IH, Eisenberg MC, Meza R, et al. Fomite-mediated transmission as a sufficient pathway: a comparative analysis across three viral pathogens. BMC Infect Dis. 2018;18:540.  https://doi.org/10.1186/s12879-018-3425-x.CrossRefGoogle Scholar
  121. 121.
    Sze-To GN, Yang Y, Kwan JKC, Yu SCT, Chao CYH. Effects of surface material, ventilation, and human behavior on indirect contact transmission risk of respiratory infection: effects of different factors on indirect contact risk. Risk Anal. 2014;34:818–30.CrossRefGoogle Scholar
  122. 122.
    Otter JA, Donskey C, Yezli S, Douthwaite S, Goldenberg SD, Weber DJ. Transmission of SARS and MERS coronaviruses and influenza virus in healthcare settings: the possible role of dry surface contamination. J Hosp Infect. 2016;92:235–50.CrossRefGoogle Scholar
  123. 123.
    Lei H, Li Y, Xiao S, Lin C-H, Norris SL, Wei D, et al. Routes of transmission of influenza A H1N1, SARS CoV, and norovirus in air cabin: comparative analyses. Indoor Air. 2018;28:394–403.CrossRefGoogle Scholar
  124. 124.
    Li S, Eisenberg JNS, Spicknall IH, Koopman JS. Dynamics and control of infections transmitted from person to person through the environment. Am J Epidemiol. 2009;170:257–65.CrossRefGoogle Scholar
  125. 125.
    Atkinson MP, Wein LM. Quantifying the routes of transmission for pandemic influenza. Bull Math Biol. 2008;70:820–67.CrossRefGoogle Scholar
  126. 126.
    Xiao S, Tang JW, Hui DS, Lei H, Yu H, Li Y. Probable transmission routes of the influenza virus in a nosocomial outbreak. Epidemiol Infect. 2018;146:1114–22.CrossRefGoogle Scholar
  127. 127.
    Breban R. Role of environmental persistence in pathogen transmission: a mathematical modeling approach. J Math Biol. 2013;66:535–46.CrossRefGoogle Scholar
  128. 128.
    Zhao J, Eisenberg JE, Spicknall IH, Li S, Koopman JS. Model analysis of fomite mediated influenza transmission. PLoS One. 2012;7:e51984.CrossRefGoogle Scholar
  129. 129.
    Canales RA, Reynolds KA, Wilson AM, Fankem SLM, Weir MH, Rose JB, et al. Modeling the role of fomites in a norovirus outbreak. J Occup Environ Hyg. 2019;16:16–26.CrossRefGoogle Scholar
  130. 130.
    Julian TR, Canales RA, Leckie JO, Boehm AB. A model of exposure to rotavirus from nondietary ingestion iterated by simulated intermittent contacts. Risk Anal. 2009;29:617–32.CrossRefGoogle Scholar
  131. 131.
    Nicas M, Best D. A study quantifying the hand-to-face contact rate and its potential application to predicting respiratory tract infection. J Occup Environ Hyg. 2008;5:347–52.CrossRefGoogle Scholar
  132. 132.
    Julian TR, Pickering AJ. A pilot study on integrating videography and environmental microbial sampling to model fecal bacterial exposures in peri-urban Tanzania. PLoS One. 2015;10:e0136158.CrossRefGoogle Scholar
  133. 133.
    Hertzberg VS, Weiss H, Elon L, Si W, Norris SL, The FlyHealthy Research Team. Behaviors, movements, and transmission of droplet-mediated respiratory diseases during transcontinental airline flights. Proc Natl Acad Sci. 2018;115:3623–7.CrossRefGoogle Scholar
  134. 134.
    Smieszek T, Lazzari G, Salathé M. Assessing the dynamics and control of droplet- and aerosol-transmitted influenza using an indoor positioning system. Sci Rep. 2019;9.  https://doi.org/10.1038/s41598-019-38825-y.
  135. 135.
    Herzog AB, Pandey AK, Reyes-Gastelum D, Gerba CP, Rose JB, Hashsham SA. Evaluation of sample recovery efficiency for bacteriophage P22 on fomites. Appl Environ Microbiol. 2012;78:7915–22.CrossRefGoogle Scholar
  136. 136.
    Ganime AC, Leite JPG, de Abreu Corrêa A, Melgaço FG, Carvalho-Costa FA, Miagostovich MP. Evaluation of the swab sampling method to recover viruses from fomites. J Virol Methods. 2015;217:24–7.CrossRefGoogle Scholar
  137. 137.
    Thornley CN, Emslie NA, Sprott TW, Greening GE, Rapana JP. Recurring norovirus transmission on an airplane. Clin Infect Dis. 2011;53:515–20.CrossRefGoogle Scholar
  138. 138.
    Moser MR, Bender TR, Margolis HS, Noble GR, Kendal AP, Ritter DG. An outbreak of influenza aboard a commercial airliner. Am J Epidemiol. 1979;110:1–6.CrossRefGoogle Scholar
  139. 139.
    Knox J, Uhlemann A-C, Miller M, Hafer C, Vasquez G, Vavagiakis P, et al. Environmental contamination as a risk factor for intra-household Staphylococcus aureus transmission. PLoS One. 2012;7:e49900.CrossRefGoogle Scholar
  140. 140.
    Cowling BJ, Ip DKM, Fang VJ, Suntarattiwong P, Olsen SJ, Levy J, et al. Aerosol transmission is an important mode of influenza A virus spread. Nat Commun. 2013;4.  https://doi.org/10.1038/ncomms2922.
  141. 141.
    Lee SS, Wong NS. Probable transmission chains of Middle East respiratory syndrome coronavirus and the multiple generations of secondary infection in South Korea. Int J Infect Dis. 2015;38:65–7.CrossRefGoogle Scholar
  142. 142.
    Dick EC, Jennings LC, Mink KA, Wartgow CD, Inborn SL. Aerosol transmission of rhinovirus colds. J Infect Dis. 1987;156:442–8.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Civil, Architectural, and Environmental EngineeringIllinois Institute of TechnologyChicagoUSA
  2. 2.Environmental Health DepartmentHarvard T.H. Chan School of Public HealthBostonUSA
  3. 3.Department of PediatricsUniversity of California San Diego School of MedicineSan DiegoUSA

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