Aerosol transmission of SARS-CoV-2? Evidence, prevention and control

Song Tang, Yixin Mao, Rachael M Jones, Qiyue Tan, John S Ji, Na Li, Jin Shen, Yuebin Lv, Lijun Pan, Pei Ding, Xiaochen Wang, Youbin Wang, C Raina MacIntyre, Xiaoming Shi, Song Tang, Yixin Mao, Rachael M Jones, Qiyue Tan, John S Ji, Na Li, Jin Shen, Yuebin Lv, Lijun Pan, Pei Ding, Xiaochen Wang, Youbin Wang, C Raina MacIntyre, Xiaoming Shi

Abstract

As public health teams respond to the pandemic of coronavirus disease 2019 (COVID-19), containment and understanding of the modes of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) transmission is of utmost importance for policy making. During this time, governmental agencies have been instructing the community on handwashing and physical distancing measures. However, there is no agreement on the role of aerosol transmission for SARS-CoV-2. To this end, we aimed to review the evidence of aerosol transmission of SARS-CoV-2. Several studies support that aerosol transmission of SARS-CoV-2 is plausible, and the plausibility score (weight of combined evidence) is 8 out of 9. Precautionary control strategies should consider aerosol transmission for effective mitigation of SARS-CoV-2.

Keywords: Airborne transmission; COVID-19; Hospital; Mask; Precaution; Respiratory protection.

Conflict of interest statement

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Copyright © 2020 The Authors. Published by Elsevier Ltd.. All rights reserved.

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References

    1. Asadi S., Bouvier N., Wexler A.S., Ristenpart W.D. The coronavirus pandemic and aerosols: does COVID-19 transmit via expiratory particles? Aerosol Sci. Technol. 2020;54:635–638.
    1. Bai Y., Yao L., Wei T., et al. Presumed asymptomatic carrier transmission of COVID-19. JAMA. 2020
    1. Bao L., Gao H., Deng W., et al. Transmission of severe acute respiratory syndrome coronavirus 2 via close contact and respiratory droplets among human angiotensin-converting enzyme 2 mice. J. Infect. Dis. 2020;222:551–555.
    1. Blachere F.M., Lindsley W.G., Pearce T.A., et al. Measurement of airborne influenza virus in a hospital emergency department. Clin. Infect. Dis.: Off. Publ. Infect. Dis. Soc. Am. 2009;48:438–440.
    1. Bonifait L., Charlebois R., Vimont A., et al. Detection and quantification of airborne norovirus during outbreaks in healthcare facilities. Clin. Infect. Dis.: Off. Publ. Infect. Dis. Soc. Am. 2015;61:299–304.
    1. Bourouiba L. Turbulent gas clouds and respiratory pathogen emissions: potential implications for reducing transmission of COVID-19. JAMA. 2020
    1. Brankston G., Gitterman L., Hirji Z., Lemieux C., Gardam M. Transmission of influenza A in human beings. Lancet. Infect. Dis. 2007;7:257–265.
    1. Buonanno G., Stabile L., Morawska L. Estimation of airborne viral emission: quanta emission rate of SARS-CoV-2 for infection risk assessment. Environ. Int. 2020;141
    1. Cai J., Sun W., Huang J., Gamber M., Wu J., He G. Indirect virus transmission in cluster of COVID-19 cases, Wenzhou, China, 2020. Emerg. Infect. Dis. 2020;26:1343–1345.
    1. Campell A. Government of Ontario; Canada: 2006. SARS Commission Final Report: Spring of Fear.
    1. CDC, 2020. Interim Infection Prevention and Control Recommendations for Patients with Suspected or Confirmed Coronavirus Disease 2019 (COVID-19) in Healthcare Settings. (Accessed April 1, 2020, at .
    1. Chan J.F., Yuan S., Zhang A.J., et al. Surgical mask partition reduces the risk of non-contact transmission in a golden Syrian hamster model for Coronavirus Disease 2019 (COVID-19) Clin. Infect. Dis.: Off. Publ. Infect. Dis. Soc. Am. 2020
    1. Chen Y., Wang A., Yi B., et al. The epidemiological characteristics of infection in close contacts of COVID-19 in Ningbo city. Chinese J. Epidemiol. 2020;41
    1. Chia P.Y., Coleman K.K., Tan Y.K., et al. Detection of air and surface contamination by SARS-CoV-2 in hospital rooms of infected patients. Nat. Commun. 2020;11:2800.
    1. Chin A., Chu J., Perera M., et al. Stability of SARS-CoV-2 in different environmental conditions. The Lancet Microbe. 2020;1(1)
    1. Chowdhury R., Maranas C.D. Biophysical characterization of the SARS-CoV2 spike protein binding with the ACE2 receptor explains increased COVID-19 pathogenesis. bioRxiv. 2020;2020(03):30.015891.
    1. Chu C.M., Cheng V.C., Hung I.F., et al. Viral load distribution in SARS outbreak. Emerg. Infect. Dis. 2005;11:1882–1886.
    1. Coleman K.K., Sigler W.V. Airborne influenza A virus exposure in an elementary school. Sci. Rep. 2020;10:1859.
    1. Cook T.M. Personal protective equipment during the COVID-19 pandemic – a narrative review. Anaesthesia. 2020
    1. Cowling B.J., Leung G.M. Epidemiological research priorities for public health control of the ongoing global novel coronavirus (2019-nCoV) outbreak. Euro Surveill.: Bull. Europeen sur les maladies transmissibles = European Commun. Dis. Bull. 2020;2
    1. de Wit E., van Doremalen N., Falzarano D., Munster V.J. SARS and MERS: recent insights into emerging coronaviruses. Nat. Rev. Microbiol. 2016;14:523–534.
    1. Deng W., Bao L., Gao H., et al. Ocular conjunctival inoculation of SARS-CoV-2 can cause mild COVID-19 in Rhesus macaques. bioRxiv. 2020;2020(03):13.990036.
    1. Dhand R., Li J. Coughs and sneezes: their role in transmission of respiratory viral infections, including SARS-CoV-2. Am. J. Respir. Crit. Care Med. 2020
    1. Dietz Leslie, Horve Patrick F., Coil David A., Fretz Mark, Eisen Jonathan A., Van Den Wymelenberg Kevin, Gilbert Jack A. 2019 Novel coronavirus (COVID-19) pandemic: built environment considerations to reduce transmission. mSystems. 2019;5(2) doi: 10.1128/mSystems.00245-20.
    1. Ding, Z., Qian, H., Xu, B., et al. 2020. Toilets dominate environmental detection of SARS-CoV-2 virus in a hospital. medRxiv 2020:2020.04.03.20052175.
    1. ECDC, 2020. Q & A on COVID-19: 4. What is the mode of transmission? How (easily) does it spread? (Accessed March 31, 2020, at .
    1. Fabian P., McDevitt J.J., DeHaan W.H., et al. Influenza virus in human exhaled breath: an observational study. PLoS ONE. 2008;3
    1. Fears Alyssa C., Klimstra William B., Duprex Paul, Hartman Amy, Weaver Scott C., Plante Kenneth S., Mirchandani Divya, Plante Jessica Ann, Aguilar Patricia V., Fernández Diana, Nalca Aysegul, Totura Aysegul, Dyer David, Kearney Brian, Lackemeyer Matthew, Bohannon J. Kyle, Johnson Reed, Garry Robert F., Reed Doug S., Roy Chad J. Persistence of severe acute respiratory syndrome coronavirus 2 in aerosol suspensions. Emerg. Infect. Dis. 2020;26(9) doi: 10.3201/eid2609.201806.
    1. Feigin R.D., Baker C.J., Herwaldt L.A., Lampe R.M., Mason E.O., Whitney S.E. Epidemic meningococcal disease in an elementary-school classroom. N. Engl. J. Med. 1982;307:1255–1257.
    1. Francisco, P.W., Emmerich, S.J., 2014. ASHRAE Position Document on Airborne Infectious Diseases.
    1. Guan W.J., Ni Z.Y., Hu Y., et al. Clinical characteristics of coronavirus disease 2019 in China. N. Engl. J. Med. 2020
    1. Guo Z.-D., Wang Z.-Y., Zhang S.-F., et al. Aerosol and surface distribution of severe acute respiratory syndrome coronavirus 2 in hospital wards, Wuhan, China, 2020. Emerg. Infect. Dis. J. 2020;26:1583.
    1. Holshue M.L., DeBolt C., Lindquist S., et al. First Case of 2019 Novel Coronavirus in the United States. N. Engl. J. Med. 2020;382:929–936.
    1. Jeong Hye Won, Kim Se-Mi, Kim Hee-Sung, Kim Young-Il, Kim Jun Hyoung, Cho Jun Yeon, Kim Sun-hyung, Kang Hyeran, Kim Seong-Gyu, Park Su-Jin, Kim Eun-Ha, Choi Young Ki. Viable SARS-CoV-2 in various specimens from COVID-19 patients. Clin. Microbiol. Infect. 2020 doi: 10.1016/j.cmi.2020.07.020.
    1. Jiang, Y., Wang, H., Chen, Y., et al., 2020. Clinical Data on Hospital Environmental Hygiene Monitoring and Medical Staffs Protection during the Coronavirus Disease 2019 Outbreak. medRxiv 2020.02.25.20028043; doi:.
    1. Johnson D., Lynch R., Marshall C., Mead K., Hirst D. Aerosol generation by modern flush toilets. Aerosol Sci. Technol.: J. Am. Assoc. Aerosol Res. 2013;47:1047–1057.
    1. Jones R.M., Brosseau L.M. Aerosol transmission of infectious disease. J. Occup. Environ. Med. 2015;57:501–508.
    1. Keene C.H. Airborne contagion and air hygiene. William firth wells. J. Sch. Health. 1955;25:249.
    1. Khare P., Marr L.C. Simulation of vertical concentration gradient of influenza viruses in dust resuspended by walking. Indoor Air. 2015;25:428–440.
    1. Kim Y.I., Kim S.G., Kim S.M., et al. Infection and rapid transmission of SARS-CoV-2 in ferrets. Cell Host Microbe. 2020;27(704–9)
    1. Knight V. Viruses as agents of airborne contagion. Ann. N. Y. Acad. Sci. 1980;353:147–156.
    1. Kurnitski, J., Boerstra, A., Franchimon, F., Mazzarella, L., Hogeling, J., Hovorka, F., 2020. REHVA COVID-19 guidance document , March 17, 2020 (updates will follow as necessary) How to operate and use building services in order to prevent the spread of the coronavirus disease (COVID-19) virus (SARS-CoV-2) in workplaces. 2020, 1–6.
    1. Lee N., Hui D., Wu A., et al. A major outbreak of severe acute respiratory syndrome in Hong Kong. N. Engl. J. Med. 2003;348:1986–1994.
    1. Letko M., Marzi A., Munster V. Functional assessment of cell entry and receptor usage for SARS-CoV-2 and other lineage B betacoronaviruses. Nat. Microbiol. 2020;5:562–569.
    1. Leung N.H.L., Chu D.K.W., Shiu E.Y.C., et al. Respiratory virus shedding in exhaled breath and efficacy of face masks. Nat. Med. 2020
    1. Li Y., Duan S., Yu I.T., Wong T.W. Multi-zone modeling of probable SARS virus transmission by airflow between flats in Block E, Amoy Gardens. Indoor Air. 2005;15:96–111.
    1. Li Y.Y., Wang J.X., Chen X. Can a toilet promote virus transmission? From a fluid dynamics perspective. Phys. fluids. 2020;32
    1. Liu Y., Ning Z., Chen Y., et al. Aerodynamic analysis of SARS-CoV-2 in two Wuhan hospitals. Nature. 2020;582:557–560.
    1. Liu L., Wei J., Li Y., Ooi A. Evaporation and dispersion of respiratory droplets from coughing. Indoor Air. 2017;27:179–190.
    1. Lopman B., Gastanaduy P., Park G.W., Hall A.J., Parashar U.D., Vinje J. Environmental transmission of norovirus gastroenteritis. Curr. Opin. Virol. 2012;2:96–102.
    1. Lu J., Gu J., Li K., et al. COVID-19 outbreak associated with air conditioning in restaurant, Guangzhou, China, 2020. Emerg. Infect. Dis. 2020;26:1628–1631.
    1. Lukassen S., Chua R.L., Trefzer T., et al. SARS-CoV-2 receptor ACE2 and TMPRSS2 are predominantly expressed in a transient secretory cell type in subsegmental bronchial branches. bioRxiv. 2020;2020(03):13.991455.
    1. Ma Q.X., Shan H., Zhang H.L., Li G.M., Yang R.M., Chen J.M. Potential utilities of mask-wearing and instant hand hygiene for fighting SARS-CoV-2. J. Med. Virol. 2020
    1. Marks P.J., Vipond I.B., Regan F.M., Wedgwood K., Fey R.E., Caul E.O. A school outbreak of Norwalk-like virus: evidence for airborne transmission. Epidemiol. Infect. 2003;131:727–736.
    1. Miller, S.L., Nazaroff, W.W., Jimenez, J.L., et al.,2020. Transmission of SARS-CoV-2 by inhalation of respiratory aerosol in the Skagit Valley Chorale superspreading event. 2020:2020.06.15.20132027.
    1. Milton D.K., Fabian M.P., Cowling B.J., Grantham M.L., McDevitt J.J. Influenza virus aerosols in human exhaled breath: particle size, culturability, and effect of surgical masks. PLoS Pathog. 2013;9
    1. MHLW, 2020. Q & A on coronavirus 2019 (COVID-19): How does human to human transmission of the novel coronavirus (2019-nCOV) happen? (Accessed March 14, 2020, at .
    1. MOH, 2020. Clarifications on Misinformation regarding COVID-19. 2020. (Accessed April 1, 2020, at .
    1. Morawska L., Johnson G., Ristovski Z., Hargreaves M., Mengersen K., Corbett S. Size distribution and sites of origin of droplets expelled from the human respiratory tract during expiratory activities. J. Aerosol Sci. 2009;40:256–269.
    1. Moriarty L.F., Plucinski M.M., Marston B.J., et al. Public health responses to COVID-19 outbreaks on cruise ships - worldwide, february-march 2020. MMWR Morb. Mortal. Wkly Rep. 2020;69:347–352.
    1. Moser M.R., Bender T.R., Margolis H.S., Noble G.R., Kendal A.P., Ritter D.G. An outbreak of influenza aboard a commercial airliner. Am. J. Epidemiol. 1979;110:1–6.
    1. Mubareka S., Lowen A.C., Steel J., Coates A.L., Garcia-Sastre A., Palese P. Transmission of influenza virus via aerosols and fomites in the guinea pig model. J. Infect. Dis. 2009;199:858–865.
    1. Mustaffa-Babjee A., Ibrahim A.L., Khim T.S. A case of human infection with Newcastle disease virus. Southeast Asian J. Trop. Med. Public Health. 1976;7:622–624.
    1. National Academies of Sciences E, Medicine, 2020. Rapid Expert Consultation on the Possibility of Bioaerosol Spread of SARS-CoV-2 for the COVID-19 Pandemic (April 1, 2020). The National Academies Press, Washington, DC.
    1. NHC, 2020. Diagnosis and treatment plan of COVID-19 (trial version 7). (in Chinese) (Accessed March 3, 2020, at .
    1. Ong S.W.X., Tan Y.K., Chia P.Y., 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
    1. Oran D.P., Topol E.J. Prevalence of asymptomatic SARS-CoV-2 infection: a narrative review. Ann. Intern. Med. 2020
    1. Parienta D., Morawska L., Johnson G.R., et al. Theoretical analysis of the motion and evaporation of exhaled respiratory droplets of mixed composition. J. Aerosol Sci. 2011;42:1–10.
    1. Paules C.I., Marston H.D., Fauci A.S. Coronavirus infections—more than just the common cold. JAMA. 2020;323:707–708.
    1. Ratnesar-Shumate S., Williams G., Green B., et al. Simulated sunlight rapidly inactivates SARS-CoV-2 on surfaces. J. Infect. Dis. 2020;222:214–222.
    1. Read, R., 2020. A choir decided to go ahead with rehearsal. Now dozens of members have COVID-19 and two are dead. 2020. (Accessed April 13, 2020, at ).
    1. Rothe C., Schunk M., Sothmann P., et al. Transmission of 2019-nCoV infection from an asymptomatic contact in Germany. N. Engl. J. Med. 2020;382:970–971.
    1. REHVA, 2020. REHVA COVID-19 guidance document, April 3, 2020. (Accessed March 17, 2020, at .
    1. Santarpia J.L., Rivera D.N., Herrera V.L., et al. Aerosol and surface contamination of SARS-CoV-2 observed in quarantine and isolation care. Sci. Rep. 2020;10:12732.
    1. Setti L., Passarini F., De Gennaro G., et al. SARS-Cov-2RNA found on particulate matter of Bergamo in Northern Italy: First evidence. Environ. Res. 2020;188
    1. Shen Y., Li C., Dong H., et al. Airborne transmission of COVID-19: epidemiologic evidence from two outbreak investigations. ResearchGate. 20202020
    1. Sia S.F., Yan L.M., Chin A.W.H., et al. Pathogenesis and transmission of SARS-CoV-2 in golden hamsters. Nature. 2020
    1. Siegel J.D., Rhinehart E., Jackson M., Chiarello L. 2007 Guideline for isolation precautions: preventing transmission of infectious agents in health care settings. Am. J. Infect. Control. 2007;35:S65–S164.
    1. Smith, J.C., Sheltzer, J.M., 2020. Cigarette smoke triggers the expansion of a subpopulation of respiratory epithelial cells that express the SARS-CoV-2 receptor ACE2. bioRxiv 2020:2020.03.28.013672.
    1. Smither S.J., Eastaugh L.S., Findlay J.S., Lever M.S. Experimental aerosol survival of SARS-CoV-2 in artificial saliva and tissue culture media at medium and high humidity. Emerging Microbes Infect. 2020;9:1415–1417.
    1. Somsen G.A., van Rijn C., Kooij S., Bem R.A., Bonn D. Small droplet aerosols in poorly ventilated spaces and SARS-CoV-2 transmission. Lancet Respir. Med. 2020;8:658–659.
    1. Stadnytskyi V., Bax C.E., Bax A., Anfinrud P. The airborne lifetime of small speech droplets and their potential importance in SARS-CoV-2 transmission. PNAS. 2020;117:11875–11877.
    1. Tan L., Kang X., Zhang B., et al. A special case of COVID-19 with long duration of viral shedding for 49 days. medRxiv. 2020;2020(03) 22.20040071.
    1. Tellier R., Li Y., Cowling B.J., Tang J.W. Recognition of aerosol transmission of infectious agents: a commentary. BMC Infect. Dis. 2019;19:101.
    1. van Doremalen, N., Bushmaker, T., Morris, D., et al., 2020. Aerosol and surface stability of HCoV-19 (SARS-CoV-2) compared to SARS-CoV-1. medRxiv 2020:2020.03.09.20033217.
    1. Wang J., Du G. COVID-19 may transmit through aerosol. Ir. J. Med. Sci. 2020:1–2.
    1. Wei J., Li Y. Enhanced spread of expiratory droplets by turbulence in a cough jet. Build. Environ. 2015;93:86–96.
    1. WHO, 2020. WHO Coronavirus Disease (COVID-19) Dashboard. 2020. (Accessed July 30, 2020, at ).
    1. WHO, 2020. Q&A on coronaviruses (COVID-19) : Is COVID-19 airborne? (Accessed March 9, 2020, at .
    1. WHO, 2020. Q&A: How is COVID-19 transmitted? What do we know about aerosol transmission? (Accessed July 9, 2020, at .
    1. Wölfel R., Corman V.M., Guggemos W., et al. Virological assessment of hospitalized patients with COVID-2019. Nature. 2020;581:465–469.
    1. Wong B.C., Lee N., Li Y., et al. Possible role of aerosol transmission in a hospital outbreak of influenza. Clin. Infect. Dis.: Off. Publ. Infect. Dis. Soc. Am. 2010;51:1176–1183.
    1. Wrapp D., Wang N., Corbett K.S., et al. Cryo-EM structure of the 2019-nCoV spike in the prefusion conformation. Science. 2020;367:1260–1263.
    1. Wu, Z., Zhang, D., Lei, Y., 2012. An outbreak of norovirus in school transmitted by aerosol. Chinese Journal of School Health 33, 244–5. (in Chinese).
    1. Wu, W., Li, Y., Wei, Z., et al., 2020. Investigation and analysis on characteristics of a cluster of COVID-19 associated with exposure in a department store in Tianjin. Chinese Journal of Epidemiology 41, 489–93. (in Chinese).
    1. Xiao S., Li Y., Sung M., Wei J., Yang Z. A study of the probable transmission routes of MERS-CoV during the first hospital outbreak in the Republic of Korea. Indoor Air. 2018;28:51–63.
    1. Xie C., Jiang L., Huang G., et al. Comparison of different samples for 2019 novel coronavirus detection by nucleic acid amplification tests. Int. J. Infect. Dis. 2020;93:264–267.
    1. Xu H., Zhong L., Deng J., et al. High expression of ACE2 receptor of 2019-nCoV on the epithelial cells of oral mucosa. Int. J. Oral Sci. 2020;12:8.
    1. Yang W., Elankumaran S., Marr L.C. Concentrations and size distributions of airborne influenza A viruses measured indoors at a health centre, a day-care centre and on aeroplanes. J. R. Soc. Interface. 2011;8:1176–1184.
    1. Yu I.T., Li Y., Wong T.W., et al. Evidence of airborne transmission of the severe acute respiratory syndrome virus. N. Engl. J. Med. 2004;350:1731–1739.
    1. Zhang X., Ji Z., Yue Y., Liu H., Wang J. Infection risk assessment of COVID-19 through aerosol transmission: a case study of South China seafood market. Environ. Sci. Technol. 2020
    1. Zhang R., Li Y., Zhang A.L., Wang Y., Molina M.J. Identifying airborne transmission as the dominant route for the spread of COVID-19. Proc. Natl. Acad. Sci. USA. 2020;117:14857–14863.
    1. Zhou F., Yu T., Du R., et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet (London, England) 2020;395:1054–1062.
    1. Zietsman M., Phan L.T., Jones R.M. Potential for occupational exposures to pathogens during bronchoscopy procedures. J. Occup. Environ. Hygiene. 2019;16:707–716.
    1. Zou L., Ruan F., Huang M., et al. SARS-CoV-2 viral load in upper respiratory specimens of infected patients. N. Engl. J. Med. 2020;382:1177–1179.

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