Microbial Exchange via Fomites and Implications for Human Health
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.
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.
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.
KeywordsMicrobiology Built environment Contamination Infectious disease transmission Aerosol Quantitative microbial risk assessment (QMRA)
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.
Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance
- 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.•• 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.• 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.• 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.• 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.• 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.•• 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.• 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.•• 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.•• 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.•• 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.• 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.• 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.• 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.•• 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.• 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.• 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.• 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.• 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.• 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.•• 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.• 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
- 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
- 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.
- 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.
- 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.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.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
- 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
- 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
- 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.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
- 92.Feldman J, Feldman J, Feldman M. Women doctors’ purses as an unrecognized fomite. Del Med J. 2012;84:277–80.Google Scholar
- 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
- 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.
- 118.Jones RM, Nicas M. Benchmarking of a Markov multizone model of contaminant transport. Ann Occup Hyg. 2014;58:1018–31.Google Scholar
- 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
- 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.
- 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.