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Edition 28 - General Edition

Fomite Transmission Among Respiratory Viruses and the Importance of Low-level Surface Disinfection

By Timothy L. Wiemken

Citation

Wiemken, TL. Fomite transmission among respiratory viruses and the importance of low-level surface disinfection. Harvard Public Health Review. 2021; 28.

Fomite transmission among respiratory viruses and the importance of low-level surface disinfection

Abstract

Background

Many different respiratory viruses cause substantial morbidity and mortality worldwide. The impact of these viruses on human health is not well understood since diagnostic testing is uncommon, available tests have modest diagnostic accuracy, and therapies are rare. This leaves infection prevention our primary resource for reduction in morbidity and mortality due to these viruses.

Main Body

A practical approach to prevention of respiratory virus transmission is to institute protections to reduce the risk from all sources of potential transmission. This approach is called the “swiss cheese model” and is often considered the cornerstone of quality. Although mask use has been given a great deal of discussion for respiratory virus prevention, the role of surfaces and indirect contact transmission through fomites has been largely ignored despite a great deal of supporting evidence. Fomite transmission even more critical, as it is tightly interconnected with both droplet and airborne routes. Two major interventions for prevention of indirect contact from fomites include hand hygiene and surface disinfection. Given the difficulty in monitoring and ensuring compliance with hand hygiene, the importance of surface disinfection has been deemed more and more critical over the past decade. Nevertheless, a major bottleneck with surface disinfection as a transmission reduction intervention is that it is a “momentary event’, and microorganisms rapidly recontaminate the environment after traditional disinfection approaches. One improvement to these surface disinfection interventions may be to add continuously acting disinfectants or antimicrobial surface coatings to compatible surfaces. These are products that have bactericidal or bacteriostatic activity for an extended period of time. Several of these products exist, but only a few have shown effectiveness in interventional studies against a variety of pathogens.

Conclusion

During a time when SARS-CoV-2 is ravaging the world, when influenza viruses decimate populations annually, and countless other respiratory viruses cause significant morbidity, ensuring the most effective prevention interventions are both socially accepted and evidence-based is critical. Our approaches to respiratory virus transmission reduction must be all-encompassing if we wish to truly break the chain of transmission. This includes ensuring environmental hygiene through surface disinfection.

Background

Respiratory viruses cause substantial morbidity and mortality worldwide, with influenza alone resulting in up to 650,000 deaths each year (1). As of December 2020, a new respiratory virus, Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) has led to a pandemic with over 73 million infections and more than 1.6 million deaths (2). Several other viruses also cause human respiratory infection, including parainfluenza virus, respiratory syncytial virus (RSV), human metapneumovirus, other ‘seasonal’ coronavirus (e.g. coronaviruses 229E, NL63, OC43, and HKU1), rhinovirus, enterovirus, adenovirus, and bocavirus. The impact of these viruses on human health is not well studied since diagnostic testing is uncommon, available tests have modest diagnostic accuracy, and therapies are essentially non-existent (with the exception of influenza) – the latter limiting the clinical utility of knowing that one of these viruses is present in the management of symptomatic patients. This leaves infection prevention our primary resource for reduction in morbidity and mortality due to these viruses.

Main text

Respiratory virus infection is likely to result from all three major modes of transmission: contact (direct or indirect), droplets, and aerosols (3). However, we do not have a strong evidence base for our understanding of transmission and prevention of these viruses. This lack of knowledge is underscored by the wide variability of transmission-based prevention measures outlined by the Centers for Disease Control and Prevention (CDC) in hospital settings – variability even for the same organism (4). For example, adenovirus pneumonia, a lower respiratory tract infection, is documented as needing droplet precautions, but upper respiratory infection, or other lower respiratory infections (exacerbation of chronic bronchitis or acute bronchitis) are not specifically mentioned. This results in a recommendation for transmission prevention under “respiratory infectious diseases not covered elsewhere” – suggesting that only standard precautions are needed. The lack of specific published evidence for transmission prevention of this virus results in confusing guidance, which may lead to difficulty in implementing prevention interventions in practice. Further, this may erode trust in those attempting to implement interventions if said interventions compete with one another. A more practical approach is to institute protections to reduce the risk from all major sources of potential transmission. This approach is called the “swiss cheese model” and is often considered the cornerstone of quality (5, 6). In healthcare, this approach led to the consideration that ‘bundles’ of interventions may be the most effective approach for infection prevention in most settings.

 

This bundled intervention approach is a necessity, as all three transmission modalities are likely common for all respiratory viruses (3, 7). This probability is often conflated with the ‘primary’ mode of transmission – the mechanism by which ‘most’ infections occur. Since a primary mode of transmission is nearly impossible to define outside of controlled laboratory experiments non-generalizable to community health settings, public health policy must focus on interventions to control all potential transmission modalities. The reality is that multifaceted interventions are necessary to curb the spread of nearly all transmissible infectious agents. Differentiating the likelihood of various modes is often more of an academic exercise than a public health necessity in many situations.

Of these three modes of transmission, droplet and aerosol routes are regularly discussed in the field of respiratory viruses and have dominated nearly all prevention discussions with respect to SARS-CoV-2 (8, 9). Nonetheless, a significant body of evidence exists with respect to environmental longevity of respiratory viruses and their potential for indirect transmission via fomites (10-30). Despite this longstanding knowledge, there is often limited consideration for the importance of these inanimate surfaces in respiratory virus transmission prevention. This is exemplified by the occasional minimization of transmission due to fomites in SARS-CoV-2 (31) despite the fact that it may be possible to capture this organism on surfaces more readily than in the air (11), surface contamination is very common (8, 11, 32), and infectious virus appears to persist longer on surfaces than in aerosols (8). Even recently, the CDC has reduced the importance of surface transmission and hand hygiene, an elementary mistake in situations of high public health importance. Fomite transmission is a critical concept since it is not possible to decouple these transmission mechanisms given that contact transmission is tightly interconnected with both droplet and airborne routes. If a particle can be released from an individual via droplets or aerosols and the pathogen contained within the particle can remain infectious on a surface for any amount of time, contact transmission via indirect routes has more than a reasonable potential to occur.

 

The difficulty in decoupling these transmission modalities results in limited direct evidence for both modes. This issue can be solved through well controlled human-laboratory studies, however. For example, human challenge studies with respiratory viruses result in an ideal scenario to study transmission via various routes. These studies are extremely expensive and difficulty to accomplish and require specific biological safety units which allow infected subjects to stay and be cared for on a 24-hour basis until they are deemed no longer infected. National funding for these studies should be strongly considered to facilitate evidence-based guidance for the next pandemic.

 

These points drive an argument for policy changes during public health disasters concerning transmissible infectious diseases. When the interventions are simple there should be mandatory multimodal approaches for intervention as without this, not only do our approaches falter, but political agendas may contaminate our ability to protect the public.

 

Hand hygiene and low-level surface disinfection are the two primary interventions for reducing transmission risks from fomites, both of which are known to have poor compliance in healthcare settings and are therefore likely to be of poor compliance in the community as well (33, 34).  Given the difficulty in monitoring and ensuring compliance with hand hygiene, the importance of surface disinfection has been deemed more and more critical over the past decade (34). Without question, disinfection is a vital component of our multifaceted approach to limit transmission of respiratory viruses. Nevertheless, a major bottleneck with surface disinfection as a transmission reduction intervention is that it is a “momentary event’, and microorganisms rapidly recontaminate the environment after traditional disinfection approaches (35). This means that surfaces need to be disinfected efficaciously with some regularity, a task which is often difficult to implement in practice. Many interventions have been studied to improve cleaning and disinfection processes, ranging from monitoring and feedback (36) to ready-to-use cleaner/disinfectant combinations (37), but limitations remain. Self-disinfecting surfaces have been suggested as potential additive interventions, but most have not proven their cost-benefit to date (38).

 

Yet another improvement to our surface disinfection interventions may be to add continuously acting disinfectants or antimicrobial surface coatings to compatible surfaces. Several of these products exist, but only a few have shown effectiveness in interventional studies against a variety of pathogens (39-42). Antimicrobial coatings may be advocated as part of an environmental hygiene bundle along with traditional cleaning and disinfection procedures (e.g. daily and terminal cleaning/disinfection of patient rooms). Antimicrobial coatings will also reduce bioburden on surfaces other than the traditional “high touch” areas which are the focus of traditional cleaning and disinfection programs (43). These other surfaces are not often considered as major reservoirs for pathogens. However, risk is a continuum, not a binary event. Therefore, all surfaces touched by individuals may pose a risk for infection, not simply high touch areas near direct patient care activities. The actual risk of acquisition of an infection from a fomite will vary based on the same factors (infectious dose, individuals immunological state, etc.) as risks from direct person-to-person transmission. Antimicrobial coatings may help ensure that these largely ignored surfaces are maintaining a low microbial bioburden, further reducing fomite transmission risks. Antimicrobial coatings may be bacteriostatic or bactericidal, although the end product is one that has some form of ability to maintain pathogen inactivation over some time – in some cases up to 90-days post application. These products do not eliminate the need for regular disinfection activities. Further, they must withstand repeated scrubbing with other cleaners and disinfectants. With only recent movement by the United States Environmental Protection Agency (EPA) to develop testing methodologies to document the efficacy for antimicrobial surface coatings (44), it may be some time before these products are readily available or recommended in US national guidance.

 

Regardless, these new technologies do show promise for improving our approach to low-level surface disinfection into the future (39-42) and continue to be active areas of research with a great deal of promising data (45, 46).

Conclusions

During a time when SARS-CoV-2 is ravaging the world, when influenza viruses decimate populations annually, and countless other respiratory viruses cause significant morbidity, ensuring the most effective prevention interventions are both socially accepted and evidence-based is critical.  Further, the importance of implementing and supporting these interventions far outweighs the need to immediately understand the intricacies of transmission modalities, which likely vary substantially from setting to setting. Our approaches to respiratory virus transmission reduction must be all-encompassing if we wish to truly break the chain of transmission. This includes ensuring environmental hygiene through surface disinfection.

Abbreviations

CDC: Centers for Disease Control and Prevention

 

EPA: Environmental Protection Agency

 

RSV: Respiratory Syncytial Virus

 

SARS-CoV-2: Severe Acute Respiratory Syndrome Coronavirus 2

Availability of Data and Materials

Data sharing is not applicable to this article as no datasets were generated or analyzed during the current study.

References

  1. World Health Organization. Influenza (Seasonal) [updated November 6, 2018. Available from: https://www.who.int/news-room/fact-sheets/detail/influenza-(seasonal).
  2. University JH. Coronavirus Resource Center 2020 [Available from: https://coronavirus.jhu.edu/map.html.
  3. Kutter JS, Spronken MI, Fraaij PL, Fouchier RA, Herfst S. Transmission routes of respiratory viruses among humans. Current opinion in virology. 2018;28:142-51.
  4. Siegel JD, Rhinehart E, Jackson M, Chiarello L, Health Care Infection Control Practices Advisory C. 2007 Guideline for Isolation Precautions: Preventing Transmission of Infectious Agents in Health Care Settings. Am J Infect Control. 2007;35(10 Suppl 2):S65-164.
  5. O’Connor T, Papanikolaou V, Keogh I. Safe surgery, the human factors approach. Surgeon. 2010;8(2):93-5.
  6. Reason JT. Human error. Cambridge England ; New York: Cambridge University Press; 1990. xv, 302 p. p.
  7. Wilson NM, Norton A, Young FP, Collins DW. Airborne transmission of severe acute respiratory syndrome coronavirus-2 to healthcare workers: a narrative review. Anaesthesia. 2020;75(8):1086-95.
  8. van Doremalen N, Bushmaker T, Morris DH, Holbrook MG, Gamble A, Williamson BN, et al. Aerosol and Surface Stability of SARS-CoV-2 as Compared with SARS-CoV-1. N Engl J Med. 2020;382(16):1564-7.
  9. Liu Y, Ning Z, Chen Y, Guo M, Liu Y, Gali NK, et al. Aerodynamic analysis of SARS-CoV-2 in two Wuhan hospitals. Nature. 2020;582(7813):557-60.
  10. Kampf G, Todt D, Pfaender S, Steinmann E. Persistence of coronaviruses on inanimate surfaces and their inactivation with biocidal agents. J Hosp Infect. 2020;104(3):246-51.
  11. Ong SWX, Tan YK, Chia PY, Lee TH, Ng OT, Wong MSY, et al. Air, Surface Environmental, and Personal Protective Equipment Contamination by Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) From a Symptomatic Patient. JAMA. 2020;323(16):1610-2.
  12. 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(3):235-50.
  13. 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(4):423-5.
  14. Pastorino B, Touret F, Gilles M, de Lamballerie X, Charrel RN. Prolonged Infectivity of SARS-CoV-2 in Fomites. Emerg Infect Dis. 2020;26(9):2256-7.
  15. Perry KA, Coulliette AD, Rose LJ, Shams AM, Edwards JR, Noble-Wang JA. Persistence of Influenza A (H1N1) Virus on Stainless Steel Surfaces. Applied and environmental microbiology. 2016;82(11):3239-45.
  16. Phan LT, Sweeney DM, Maita D, Moritz DC, Bleasdale SC, Jones RM. Respiratory viruses in the patient environment. Infect Control Hosp Epidemiol. 2020;41(3):259-66.
  17. Poirier C, Luo W, Majumder MS, Liu D, Mandl KD, Mooring TA, et al. The role of environmental factors on transmission rates of the COVID-19 outbreak: an initial assessment in two spatial scales. Scientific reports. 2020;10(1):17002.
  18. Ren SY, Wang WB, Hao YG, Zhang HR, Wang ZC, Chen YL, et al. Stability and infectivity of coronaviruses in inanimate environments. World J Clin Cases. 2020;8(8):1391-9.
  19. 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(2):133-40.
  20. Thompson KA, Bennett AM. Persistence of influenza on surfaces. J Hosp Infect. 2017;95(2):194-9.
  21. Vanessa dos Santos da Silva J, Henrique de Mello M, Staggemeier R, Henzel A, Rigotto C, Spilki FR. Adenovirus presence in surfaces and equipment from ambulatories, internship units, and operating rooms in a Brazilian hospital. Am J Infect Control. 2014;42(6):693-4.
  22. Weber TP, Stilianakis NI. Inactivation of influenza A viruses in the environment and modes of transmission: a critical review. J Infect. 2008;57(5):361-73.
  23. Asadi S, Gaaloul Ben Hnia N, Barre RS, Wexler AS, Ristenpart WD, Bouvier NM. Influenza A virus is transmissible via aerosolized fomites. Nature communications. 2020;11(1):4062.
  24. Bean B, Moore BM, Sterner B, Peterson LR, Gerding DN, Balfour HH, Jr. Survival of influenza viruses on environmental surfaces. J Infect Dis. 1982;146(1):47-51.
  25. Bin SY, Heo JY, Song MS, Lee J, Kim EH, Park SJ, et al. Environmental Contamination and Viral Shedding in MERS Patients During MERS-CoV Outbreak in South Korea. Clin Infect Dis. 2016;62(6):755-60.
  26. Biryukov J, Boydston JA, Dunning RA, Yeager JJ, Wood S, Reese AL, et al. Increasing Temperature and Relative Humidity Accelerates Inactivation of SARS-CoV-2 on Surfaces. mSphere. 2020;5(4).
  27. Boone SA, Gerba CP. The occurrence of influenza A virus on household and day care center fomites. J Infect. 2005;51(2):103-9.
  28. Wilson AM, Reynolds KA, Canales RA. Estimating the effect of hand hygiene compliance and surface cleaning timing on infection risk reductions with a mathematical modeling approach. Am J Infect Control. 2019;47(12):1453-9.
  29. Kramer A, Schwebke I, Kampf G. How long do nosocomial pathogens persist on inanimate surfaces? A systematic review. BMC Infect Dis. 2006;6:130.
  30. 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(1):540.
  31. Goldman E. Exaggerated risk of transmission of COVID-19 by fomites. Lancet Infect Dis. 2020;20(8):892-3.
  32. Guo Z-D, Wang Z-Y, Zhang S-F, Li X, Li L, Li C, et al. Aerosol and Surface Distribution of Severe Acute Respiratory Syndrome Coronavirus 2 in Hospital Wards, Wuhan, China, 2020. Emerging Infectious Diseases. 2020;26(7):1583-91.
  33. Centers for Disease Control and Prevention. Hand Hygiene in Healthcare Settings, Show me the science [Available from: https://www.cdc.gov/handhygiene/science/index.html.
  34. Carling P. Methods for assessing the adequacy of practice and improving room disinfection. Am J Infect Control. 2013;41(5 Suppl):S20-5.
  35. Hardy KJ, Gossain S, Henderson N, Drugan C, Oppenheim BA, Gao F, et al. Rapid recontamination with MRSA of the environment of an intensive care unit after decontamination with hydrogen peroxide vapour. J Hosp Infect. 2007;66(4):360-8.
  36. Dumigan DG, Boyce JM, Havill NL, Golebiewski M, Balogun O, Rizvani R. Who is really caring for your environment of care? Developing standardized cleaning procedures and effective monitoring techniques. Am J Infect Control. 2010.
  37. Wiemken TL, Curran DR, Pacholski EB, Kelley RR, Abdelfattah RR, Carrico RM, et al. The value of ready-to-use disinfectant wipes: compliance, employee time, and costs. Am J Infect Control. 2014;42(3):329-30.
  38. Weber DJ, Rutala WA. Self-disinfecting surfaces: review of current methodologies and future prospects. Am J Infect Control. 2013;41(5 Suppl):S31-5.
  39. Ellingson KD, Pogreba-Brown K, Gerba CP, Elliott SP. Impact of a Novel Antimicrobial Surface Coating on Health Care-Associated Infections and Environmental Bioburden at 2 Urban Hospitals. Clin Infect Dis. 2020;71(8):1807-13.
  40. Tamimi AH, Carlino S, Gerba CP. Long-term efficacy of a self-disinfecting coating in an intensive care unit. Am J Infect Control. 2014;42(11):1178-81.
  41. Rutala WA, Gergen MF, Sickbert-Bennett EE, Anderson DJ, Weber DJ, Program CDCPE. Antimicrobial activity of a continuously active disinfectant against healthcare pathogens. Infect Control Hosp Epidemiol. 2019;40(11):1284-6.
  42. Schmidt MG, Fairey SE, Attaway HH. In situ evaluation of a persistent disinfectant provides continuous decontamination within the clinical environment. Am J Infect Control. 2019;47(6):732-4.
  43. Beggs C, Knibbs LD, Johnson GR, Morawska L. Environmental contamination and hospital-acquired infection: factors that are easily overlooked. Indoor air. 2014.
  44. United States Environmental Protection Agency. USEPA, Office of Pesticide Programs (OPP), Antimicrobials Division (AD); Interim Guidance – Expedited Review for Products Adding Residual Efficacy Claims [Available from: https://beta.regulations.gov/docket/EPA-HQ-OPP-2020-0529/document.
  45. Ikner LA, Beck V, Gundy PM, Gerba CP. Continuously Active Antimicrobial Coating Remains Effective After Multiple Contamination Events. medRxiv. 2020:2020.09.07.20188607.
  46. Ikner LA, Torrey JR, Gundy PM, Gerba CP. A Continuously Active Antimicrobial Coating effective against Human Coronavirus 229E. medRxiv. 2020:2020.05.10.20097329.

About the Author

Timothy L Wiemken

Timothy L Wiemken, PhD MPH FAPIC FSHEA CIC, is an Associate Professor, at the Saint Louis University School of Medicine, Department of Internal Medicine and Division of Infectious Diseases, Allergy, and Immunology. 

He is also Director of Data Science and Epidemiology, Institute for Vaccine Science and Policy; Director, Infectious Diseases Epidemiology, SSM Saint Louis University Hospital; and Director, Systems Infection Prevention Center. 

Dr. Wiemken is a consultant for Allied Biosciences, Medline Industries, and Avadim Health.

He may be reached at timothy.wiemken@health.slu.edu