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June 1, 2020

Airborne Spread of SARS-CoV-2 and a Potential Role for Air Disinfection

Author Affiliations
  • 1Brigham and Women’s Hospital, Division of Global Health Equity, Harvard Medical School, Boston, Massachusetts
  • 2Beth Israel Deaconess Medical Center, Division of Infectious Diseases, Harvard Medical School, Boston, Massachusetts
JAMA. 2020;324(2):141-142. doi:10.1001/jama.2020.7603

An April 2, 2020, expert consultation from the National Academies of Sciences, Engineering, and Medicine to the White House Office of Science and Technology Policy concluded that available studies are consistent with the potential aerosol spread of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), not only through coughing and sneezing, but by normal breathing.1 This response to a White House request for a rapid review of the literature likely contributed to the recommendation from the US Centers for Disease Control and Prevention (CDC) that healthy persons wear nonmedical face coverings, when in public, to reduce virus spread from undiagnosed infectious cases.

Although clear evidence of person-to-person airborne transmission of SARS-CoV-2 has not been published, an airborne component of transmission is likely based on other respiratory viruses such as SARS, Middle East respiratory syndrome, and influenza. While air sampling for SARS-CoV-2, in a clinical setting, has demonstrated detectable viral RNA, the extent of transmission resulting from airborne particles relative to large respiratory droplets, directly and on surfaces, is not yet known. But if fitted N95 respirators can be justified as a prudent precaution against airborne infection for health care workers with regular exposure to patients with novel coronavirus 2019 (COVID-19) and nonmedical face coverings justified to be worn in public to reduce aerosol spread, should not air disinfection be deployed in intensive care units, emergency departments, waiting rooms, and ambulatory clinics? This approach may be especially important to prevent spread from asymptomatic persons with infection, who may be sources of transmission in selected public settings.

Other than natural or mechanical ventilation, only 2 practical methods of air disinfection exist: room air cleaners (ie, using filters, UV, or other means of disinfection) and upper-room germicidal UV (GUV) fixtures (see eFigure in the Supplement). For effective air disinfection, ventilation with 6 to 12 room air changes per hour is recommended by the CDC.2 This can be achieved with natural ventilation under favorable outdoor conditions and by mechanical ventilation systems designed for such high-flow rates—but at high operating costs when intake air must be heated or cooled and dehumidified. Portable room air cleaners may be a potential solution, but depending on room volume, their specified clean air delivery rates generally add too few equivalent air changes per hour to provide adequate protection against airborne infection. In contrast, commercially available upper-room GUV air disinfection (with an effective rate of air mixing) has been shown, in clinical settings, to reduce airborne tuberculosis transmission by 80%, equivalent to adding 24 room air changes per hour.3

In resource-limited settings, where air disinfection depends on natural ventilation, upper-room GUV may be increasingly important as windows are closed due to use of ductless air conditioners in response to global warming and severe outdoor air pollution. In resource-rich settings, upper-room GUV can be retrofitted into most areas with sufficient ceiling height. GUV technology is effective against viruses that have been tested, including influenza and SARS-CoV-1.4,5

Direct whole-room GUV is also used for room surface disinfection in unoccupied rooms (eg, between infectious patients), and GUV devices are being used to decontaminate respirators used for COVID-19 patient care. Although not its primary purpose, and as yet unproven experimentally, upper-room GUV in occupied rooms could possibly also reduce infectious virus settling on surfaces, and through 24/7 low-level reflected GUV exposure from the upper room, possibly accelerate virus inactivation on surfaces in the lower room. However, these additional beneficial effects require evidence from rigorously conducted studies.

Conventional thinking has been that person-to-person airborne spread of viral respiratory pathogens is the exception, although the term airborne has not been used uniformly. As defined by Wells and Riley in 1937, true airborne transmission is by infectious droplet nuclei, that is, the 1 to 5 μm dried residua of larger respiratory droplets that stop settling, buoyed by ordinary room air currents, and able to spread far beyond the trajectory of larger respiratory droplets that tend to settle within a meter or so of the infectious source. But other experts classify as airborne the direct spread of larger respiratory droplets from an infectious source to the eyes, nose, or mouth of another person, without the intermediary of transfer by hands or fomites. Recent modeling of cough- and sneeze-generated aerosol suggest the potential for projecting large respiratory droplets well beyond 2 m, but that is not droplet nuclei transmission.6 Although many respiratory viruses are transmitted by all 3 pathways, direct and indirect contact with respiratory droplets, and inhalation of droplet nuclei, there are important differences between infections that are predominantly spread by larger respiratory droplets and those that are occasionally or usually spread as suspended droplet nuclei. Among those important differences are the interventions likely to interrupt airborne transmission, including fit-tested respirators (not surgical masks) for personal protection and air disinfection.

During the relatively short-lived 2003 SARS pandemic, airborne spread of infection on airplanes and in apartment buildings in Hong Kong was documented, the latter associated with aerosol generated by faulty plumbing systems, and virus in stool was thought to play a role in airborne transmission. A cluster of COVID-19 cases at the Hong Mei House, another Hong Kong apartment building, may also have been related to faulty plumbing and a fecal source of viral aerosol.7 Among 3 reported aircraft-associated SARS-CoV-1 transmission events, 1 symptomatic passenger diagnosed with laboratory-confirmed disease was presumed to have infected 22 persons of whom 8 were seated in the 3 rows in front of the index case.8 There have been a number of clusters of COVID-19 clusters, all associated with group settings, but that alone does not define the mode of transmission. An especially concerning cluster in the US was the 2 ½-hour choir rehearsal in Washington State, after which 45 of 60 members in attendance were diagnosed with COVID-19 or had compatible symptoms, including 3 hospitalizations and 2 deaths.9 Choir members with respiratory symptoms were asked not to attend, and none were known to be present. While large droplet spread surely accounted for some transmission, the extent of spread associated with singing as a possible source of enhanced aerosolization makes airborne spread highly suspect.

Since the influenza A(H1N1) epidemic in 2009, research on viral transmission has accelerated. Airborne spread of influenza A virus been shown to occur routinely in the ferret model, and highly controversial research has shown specific genetic mutations associated with airborne transmission of H5N1 avian influenza. In an epidemiological analysis of influenza A transmission among 782 people, the airborne route was estimated to account for half of all cases.10 The potential for SARS, MERS, and influenza to spread via airborne droplet nuclei is no longer in doubt. As emphasized in the recent National Academy of Medicine consultation to the White House, it is time to address the potential for airborne SARS-CoV-2 transmission.1

Given the ongoing risks of SARS-CoV-2 infection among health care workers, some hospitals are considering deployment of commercially available upper-room GUV air disinfection, although no published studies have demonstrated efficacy and GUV systems are not currently recommended in the infection prevention guidelines from the CDC or the World Health Organization. Upper-room GUV systems must be installed and maintained following evidence-based guidelines. Priority areas for air disinfection might be waiting rooms, emergency departments, intensive care units, bronchoscopy and endoscopy rooms, and other sites where aerosol is generated. COVID-19 will not likely be the last pandemic. Management of the current crisis and preparation for future respiratory viral pathogens should include consideration of the use of upper-room GUV to help mitigate airborne transmission.

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Article Information

Corresponding Author: Edward A. Nardell, MD, Brigham and Women’s Hospital, Division of Global Health Equity, Harvard Medical School, 75 Francis St, Boston, MA 02115 (enardell@bwh.harvard.edu).

Published Online: June 1, 2020. doi:10.1001/jama.2020.7603

Conflict of Interest Disclosures: Dr Nardell has been supported entirely by research and implementation grants from the National Institutes of Health (NIH) and the United States Agency for International Development (USAID). Relevant to this commentary, Dr Nardell has consulted on a voluntary basis with the World Health Organization, USAID, Illuminating Engineering Society, and the National Academies of Sciences, Engineering, and Medicine. He has not served as a paid consultant and has no current or past commercial interest in any air disinfection technologies or related products. Dr Nathavitharana reports receipt of grants from NIH and the National Institute of Allergy and Infectious Diseases.

References
1.
Fineberg  HV.  Rapid Expert Consultation on SARS-CoV-2 Viral Shedding and Antibody Response for the COVID-19 Pandemic (April 8, 2020). National Academies of Science, Engineering, and Medicine; 2020.
2.
Centers for Disease Control and Prevention. Guidelines for Environmental Infection Control in Health-Care Facilities. US Dept of Health and Human Services Centers for Disease Control and Prevention. 2003. Updated July 2019. Accessed May 28, 2020. https://espanol.cdc.gov/infectioncontrol/pdf/guidelines/environmental-guidelines-P.pdf
3.
Mphaphlele  M, Dharmadhikari  AS, Jensen  PA,  et al.  Institutional tuberculosis transmission controlled trial of upper room ultraviolet air disinfection: a basis for new dosing guidelines.   Am J Respir Crit Care Med. 2015;192(4):477-484. doi:10.1164/rccm.201501-0060OCPubMedGoogle ScholarCrossref
4.
Darnell  ME, Subbarao  K, Feinstone  SM, Taylor  DR.  Inactivation of the coronavirus that induces severe acute respiratory syndrome, SARS-CoV.   J Virol Methods. 2004;121(1):85-91. doi:10.1016/j.jviromet.2004.06.006PubMedGoogle ScholarCrossref
5.
McDevitt  JJ, Rudnick  SN, Radonovich  LJ.  Aerosol susceptibility of influenza virus to UV-C light.   Appl Environ Microbiol. 2012;78(6):1666-1669. doi:10.1128/AEM.06960-11PubMedGoogle ScholarCrossref
6.
Bourouiba  L.  Turbulent gas clouds and respiratory pathogen emissions: potential implications for reducing transmission of COVID-19.   JAMA. 2020;323(18):1837-1838. doi:10.1001/jama.2020.4756PubMedGoogle Scholar
7.
Graham  B. Virus spread that’s left scientists baffled. Daily Examiner. Published March 11, 2020. Accessed May 28, 2020. https://www.dailyexaminer.com.au/news/virus-spread-thats-left-scientists-baffled/3965731/
8.
Yu  IT, Li  Y, Wong  TW,  et al.  Evidence of airborne transmission of the severe acute respiratory syndrome virus.   N Engl J Med. 2004;350(17):1731-1739. doi:10.1056/NEJMoa032867PubMedGoogle ScholarCrossref
9.
Waldrop  T, Toropin  K, Sutton  J. 2 Dead from coronavirus, 45 ill after March choir rehearsal. Published (updated) April 2, 2020. Accessed May 28, 2020. www.cnn.com/2020/04/01/us/washington-choir-practice-coronavirus-deaths/index.html
10.
Cowling  BJ, Ip  DK, Fang  VJ,  et al.  Aerosol transmission is an important mode of influenza A virus spread.   Nat Commun. 2013;4:1935. doi:10.1038/ncomms2922PubMedGoogle ScholarCrossref
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    6 Comments for this article
    EXPAND ALL
    Application of Upper Room GUV in Large Quarantine Centres During COVID-19 pandemic
    Rahul Narang, MBBS, MD, PhD | Professor Microbiology, Mahatma Gandhi Institute of Medical Sciences, Sevagram, District Wardha, Maharashtra, India
    I read the article by Nardell and Nathavitharana with interest. The authors have suggested use of upper room GUV in selected public settings for prevention of airborne infection especially from asymptomatic COVID-19 subjects. The pandemic is fast evolving in India and other resource-limited countries where use of upper room GUV can be more pertinent. These countries are also facing limited availability of PPE including the extended use of N95 respirators after decontamination. Such measures may lead to lower efficacy of PPE and can be tacked by installing upper room GUV that will not only reduce the SARS-CoV-2 but also Mycobacterium tuberculosis, as many patients may be co-infected with both the agents. This will also have role to play in large quarantine centres. In India, as the number of COVID-19 cases is increasing rapidly due to movement of migrant workers, more facilities with large occupancy will be required to quarantine such cases. The situation may worsen after monsoon season sets in. Cities like Mumbai are converting large covered spaces into quarantine areas. In such spaces also the viral load can be reduced by using exhaust fans and upper room GUV while the circulation of air will be maintained by ceiling fans commonly used in India.
    CONFLICT OF INTEREST: None Reported
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    A Simple Custom Could Prevent Spread of SARS-CoV-2
    Koichi Tsunoda, MD, PhD. | National Hospital Organization Tokyo Medical Center
    There are many transmission mechanisms to spread SARS-CoV-2 that should be taken into account. While air sampling for SARS-CoV-2, in a clinical setting, has demonstrated detectable viral RNA, the extent of transmission resulting from airborne particles relative to large respiratory droplets, directly and on surfaces, is not yet known. These authors have concluded that management of the current crisis and preparation for future respiratory viral pathogens should include consideration of the use of upper-room GUV to help mitigate airborne transmission (1). We want to recommend additional measures.

    When people cough and sneeze, they can propel aerosol particles over a
    distance of 8 meters (2), spray tiny drops of infected saliva fall to the ground and floor within seconds. Viral shedding in stool could be a potential route of transmission (3). We walk on the ground and step on the floor in toilet stalls with shoes and the virus can be spread via the tiny droplets that can infect you. Medical staff wear shoe covers for preventing spread of the virus onto the soles of their shoes all over the floor. The greatest threat really lies on the ground and floors.

    Most secondary infections occurred in the household has reported (4). We are concerned about infections acquired at home. In Japan, there is a simple custom of removing shoes at the entryway of a house or apartment before walking indoors to prevent floor moisture due to the hot and humid climate, a practice which greatly reduces the risk of bringing in virus attached to the soles of the shoes and spread of COVID-19 at home. Virus on the floor can become re-aerosolized and enter the air we breathe, which might increase infection risk. Also, wearing outdoor shoes increases risk to children crawling around on the floor at home. That virus can remain on synthetic materials used in shoes for as long as five days has been mentioned (5).

    To reduce the infection of COVID-19, first wipe the dirt off shoes on the doormat and then dip the shoes into tray or box containing 0.5% sodium hypochlorite and water or bleach to sterilize them at the entryway (6). Then take off or wipe the shoes and enter the house (7). It is an easy solution; removing and/or disinfecting the shoes is a very simple custom during a pandemic that could be one of the precautions to save yourself and your family.

    Koichi Tsunoda MD, PhD. & Mihiro Takazawa
    National Hospital Organization Tokyo Medical Center

    References

    1. Nardell EA, Nathavitharana RR. Airborne Spread of SARS-CoV-2 and a Potential Role for Air Disinfection. JAMA. Published online June 01, 2020.

    2. Bourouiba L. IMAGES IN CLINICAL MEDICINE. A Sneeze. N Engl J Med. 2016 Aug 25;375(8):e15.

    3. S. W. X. Ong, 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, March 4, 2020

    4. Sun K, Viboud C. Impact of contact tracing on SARS-CoV-2 transmission. Lancet
    Infect Dis. 2020 Apr 27.

    5.van Doremalen N, Bushmaker T, Morris DH, et al. Aerosol and Surface Stability of SARS-CoV-2 as Compared with SARS-CoV-1. N Engl J Med. 2020 Apr 16;382(16):1564-1567.

    6. https://www.cdc.gov/vhf/ebola/pdf/cleaning-handwashing-5percent-liquid-bleach.pdf

    7. https://www.cdc.gov/vhf/ebola/hcp/ppetraining/n95respirator_gown/doffing_19.html
    CONFLICT OF INTEREST: None Reported
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    Bipolar Air Ionization Another Potentially Viable Option
    Kent Moore, MD, DDS | Charlotte Oral Surgery
    The authors may not be aware that bipolar plasma ionization may offer another excellent and practical option for management of ambient environmental air. These units have been installed in large medical centers around the world including (but not limited to) Cleveland Clinic, John's Hopkins, Boston Children's, and Atrium (1,2).

    References

    1. https://www.businessinsider.com/bipolar-ionization-could-be-a-secret-weapon-against-covid-19-2020-4

    2. https://globalplasmasolutions-my.sharepoint.com/:p:/p/chris_mauro/EUQ9KTbzkYBDmKQpcoydXwkBz-SMOU8h6N9Y4QmMAqRHLg?e=7faTrw
    CONFLICT OF INTEREST: None Reported
    Airborne vs Surface Contact Spread
    Andrea Vila, MD, Infectious diseases | Hospital Italiano de Mendoza
    I read the article by Nardell and Nathavitharana with interest. Studies that attribute transmission of SARS-coV-2 to air conditioning have not evaluated highly relevant situations such as the use of public toilets. Such a situation could explain some cases in the setting of restaurants and other common places. It seems reasonable to keep focusing on measures of surface hygiene and social distance, before recommending expensive and unproven methods that have been designed to kill airborne pathogens.
    CONFLICT OF INTEREST: None Reported
    Ozone (O3) and a Potential Role for Air Disinfection in Airborne Spread of SARS-CoV-2.
    John Semple, MD, MSc, FRCSC, FACS | University of Toronto
    In the recent “Viewpoint” Nardell and Nathavitharana describe the growing concern regarding the potential for person-to-person airborne transmission of SARS-CoV-2 (1). Although there is no published evidence of documented airborne transmission they present a credible list of examples where sources of transmission in public settings are consistent with the potential for aerosol spread of severe acute respiratory syndrome coronavirus (2). Depending on the pathogen’s route, transmission of viral diseases in indoor settings can potentially be controlled through various procedures including the use of personal protective equipment (1).
    Logically, they argue that if airborne transmission is a real concern and “fitted
    N95 respirators are justified as a prudent precaution against airborne infection for health care workers with exposure to patients with novel coronavirus 2019 (COVID-19) and nonmedical face coverings are justified to be worn in public to reduce aerosol spread, should not air disinfection be deployed in intensive care units, emergency departments, waiting rooms, and ambulatory clinics?” (1). 

    Their subsequent description of notable air disinfectants, however, focuses on UV fixtures (specifically upper-room germicidal UV (GUV)) and the mechanics of effective in-door ventilation but somehow omits the significant role ozone (O3) has in this area. Ozone is a known natural disinfecting agent for which there is a considerable body of research that specifically highlights ozone efficacy in the control of airborne and surface viruses (2, 3). The reactivity of O3 is through oxidation or peroxidation and generation of free radicals, giving rise to a cascade of reactions like peroxidation of lipids leading to changes in membrane permeability. In viruses, the O3 damages the viral capsid and upsets the reproductive cycle by disrupting the virus-to-cell contact with peroxidation (4,5).

    Currently there are no air treatment strategies available for inactivating airborne COVID-19 due to the lack of approved protocols. Both UV light, ozone and disinfecting agents have been tested for other types of airborne phage and virus inactivation (4,5) but none have led to the establishment of standardized air treatment protocols (3).

    We agree with the authors that there needs to be a focus and recommendations from the World Health Organization and the CDC for transmission prevention guidelines in relation to air borne infections for air disinfection in priority areas in health care where aerosol is generated. Management of the current crisis should include a strategy for the use of all disinfecting agents including both O3 and UV in evidence-based guidelines for airborne transmission treatment going forward.

    References:

    1. Nardell EA, Nathavitharana RR. Airborne Spread of SARS-CoV-2 and a Potential Role for Air Disinfection. JAMA. 2020;324(2):141–142. doi:10.1001/jama.2020.7603
    2. Tseng C, Li C. Inactivation of surface viruses by gaseous ozone. J Environ Health. 2008;70(10):56-62.
    3. Dubuis ME, Dumont-Leblond N, Laliberté C, et al. Ozone efficacy for the control of airborne viruses: Bacteriophage and norovirus models. PLoS One. 2020;15(4):e0231164. Published 2020 Apr 10. doi:10.1371/journal.pone.0231164
    4. Weber TP, Stilianakis NI. Inactivation of influenza A viruses in the environment and modes of transmission: a critical review. J Infect. 2008;57(5):361-373. doi:10.1016/j.jinf.2008.08.013
    5. Semple JL, Moore GWK. High Levels of Ambient Ozone (O3) May Impact COVID-19 in High Altitude Mountain Environments [published online ahead of print, 2020 Jun 30]. R
    CONFLICT OF INTEREST: None Reported
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    Citation
    Brett Snodgrass, M.D. | Private Practice
    The authors provide presumably useful information, but no direct citation to the critical work of Wells and Riley: 

    “As defined by Wells and Riley in 1937, true airborne transmission is by infectious droplet nuclei, that is, the 1 to 5 μm dried residua of larger respiratory droplets that stop settling, buoyed by ordinary room air currents, and able to spread far beyond the trajectory of larger respiratory droplets that tend to settle within a meter or so of the infectious source.”

    The JAMA Editor-in-Chief and other interviewers have referenced the distinction between droplet and airborne transmission in multiple
    podcasts and interviews and made some suggestion that the distinction is not dichotomous but occurs along a spectrum.

    If this work by Wells and Riley creates the definitional standard of “airborne transmission” by small drops of fluid in the air, then citation to their work could be useful for readers and appears useful in educating physicians about the distinction between large drop and small airborne drop transmission. Can the authors or editors please provide the citation?
    CONFLICT OF INTEREST: None Reported
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