Clinical Infectious Diseases INVITED COMMENTARY It Is Time to Address Airborne Transmission of Coronavirus Disease 2019 (COVID-19) Lidia Morawska1 and Donald K. Milton2 1International Laboratory for Air Quality and Heath, WHO Collaborating Centre, Queensland University of Technology, 2 George Street, Brisbane, QLD 4001 Australia, and 2Institute for Applied Environmental Health, University of Maryland School of Public Health, College Park, Maryland, USA Downloaded from https://academic.oup.com/cid/advance-article/doi/10.1093/cid/ciaa939/5867798 by guest on 15 November 2020 Keywords. airborne transmission; airborne infection spread; coronavirus; COVID-19; SARS-CoV-2 virus. We appeal to the medical community transmission was the most likely mech- on hand washing, maintaining social and to the relevant national and inter- anism explaining the spatial pattern of distancing, and droplet precautions. Most national bodies to recognize the potential infections [6]. Retrospective analysis has public health organizations, including the for airborne spread of coronavirus dis- shown the same for severe acute respira- World Health Organization (WHO) [16], ease 2019 (COVID-19). There is signifi- tory syndrome coronavirus 2 (SARS- do not recognize airborne transmission cant potential for inhalation exposure to CoV-2) [7–10]. In particular, a study in except for aerosol-generating procedures viruses in microscopic respiratory drop- their review of records from a Chinese performed in healthcare settings. Hand lets (microdroplets) at short to medium restaurant observed no evidence of direct washing and social distancing are ap- distances (up to several meters, or room or indirect contact between the 3 parties propriate but, in our view, insufficient to scale), and we are advocating for the use [10]. In their review of video records from provide protection from virus-carrying of preventive measures to mitigate this the restaurant, they observed no evidence respiratory microdroplets released into route of airborne transmission. of direct or indirect contact between the the air by infected people. This problem Studies by the signatories and other 3 parties. Many studies conducted on the is especially acute in indoor or enclosed scientists have demonstrated beyond any spread of other viruses, including respira- environments, particularly those that are reasonable doubt that viruses are released tory syncytial virus (RSV) [11], Middle crowded and have inadequate ventilation during exhalation, talking, and coughing East Respiratory Syndrome Coronavirus [17] relative to the number of occupants in microdroplets small enough to remain (MERS-CoV) [8], and influenza [2, 4], and extended exposure periods (as graph- aloft in air and pose a risk of exposure at show that viable airborne viruses can be ically depicted in Figure 1). For example, distances beyond 1–2 m from an infected exhaled [2] and/or detected in the in- airborne transmission appears to be the individual ([1–4]). For example, at typical door environment of infected patients only plausible explanation for several indoor air velocities [5], a 5-μm droplet [11, 12]. This poses the risk that people superspreading events investigated that will travel tens of meters, much greater sharing such environments can poten- occurred under such conditions [10], and than the scale of a typical room, while tially inhale these viruses, resulting in others where recommended precautions settling from a height of 1.5 m to the infection and disease. There is every related to direct droplet transmissions floor. Several retrospective studies con- reason to expect that SARS-CoV-2 be- were followed. ducted after the severe acute respiratory haves similarly, and that transmission The evidence is admittedly incom- syndrome coronavirus 1 (SARS-CoV-1) via airborne microdroplets [10, 13] is an plete for all the steps in COVID-19 epidemic demonstrated that airborne important pathway. Viral RNA associated microdroplet transmission, but it is simi- with droplets <5 μm has been detected larly incomplete for the large droplet in air [14], and the virus has been shown and fomite modes of transmission. The Received 26 June 2020; editorial decision 30 June 2020; to maintain infectivity in droplets of this airborne transmission mechanism op- accepted 6 July 2020; published online July 6, 2020. size [9]. Other viruses have been shown erates in parallel with the large droplet Correspondence: L. Morawska, Australia (l.morawska@ qut.edu.au). to survive equally well, if not better, in and fomite routes [16] that are now the Clinical Infectious Diseases® 2020;XX(XX):1–4 aerosols compared to droplets on a sur- basis of guidance. Following the precau- © The Author(s) 2020. Published by Oxford University Press for face [15]. tionary principle, we must address every the Infectious Diseases Society of America. All rights reserved. For permissions, e-mail: [email protected]. The current guidance from numerous potentially important pathway to slow DOI: 10.1093/cid/ciaa939 international and national bodies focuses the spread of COVID-19. The measures INVITED COMMENTARY • CID 2020:XX (XX XXXX) • 1 may think that they are fully protected by adhering to the current recommenda- tions, but in fact, additional airborne interventions are needed for further re- duction of infection risk. This matter is of heightened signifi- cance now, when countries are reopening following lockdowns: bringing people back to workplaces and students back to schools, colleges, and universities. Downloaded from https://academic.oup.com/cid/advance-article/doi/10.1093/cid/ciaa939/5867798 by guest on 15 November 2020 We hope that our statement will raise awareness that airborne transmission of COVID-19 is a real risk and that con- trol measures, as outlined above, must be added to the other precautions taken, to reduce the severity of the pandemic and save lives. Supplementary Data Supplementary materials are available at Clinical Infectious Diseases online. Consisting of data provided by the authors to benefit the reader, the posted materials are not copyedited and are the sole responsibility of the authors, so ques- tions or comments should be addressed to the corresponding author. Figure 1. Distribution of respiratory microdroplets in an indoor environment with (A) inadequate ventilation and (B) adequate ventilation. Notes Acknowledgment. Together with the authors, 239 scientists support this Commentary, and that should be taken to mitigate airborne Ventilating, and Air-Conditioning their affiliations and contact details are listed in transmission risk include: Engineers) and REHVA (the Federation the Supplementary Data. The following scientists contributed to for- of European Heating, Ventilation and Air mulating this commentary. Linsey C. Marr, • Provide sufficient and effective venti- Conditioning Associations) have already William Bahnfleth, Jose-Luis Jimenez, Yuguo lation (supply clean outdoor air, min- provided guidelines based on the existing Li, William W. Nazaroff, Catherine Noakes, Chandra Sekhar, Julian Wei-Tze Tang, Raymond imize recirculating air) particularly evidence of airborne transmission. The Tellier, Philomena M. Bluyssen, Atze Boerstra, in public buildings, workplace envir- measures that we propose offer more Giorgio Buonanno, Junji Cao, Stephanie onments, schools, hospitals, and aged benefits than potential downsides, even if J. Dancer, Francesco Franchimon, Charles care homes. they can only be partially implemented. Haworth, Jaap Hogeling, Christina Isaxon, Jarek Kurnitski, Marcel Loomans, Guy B. Marks, • Supplement general ventilation with It is understood that there is not as yet Livio Mazzarella, Arsen Krikor Melikov, Shelly airborne infection controls such as universal acceptance of airborne trans- Miller, Peter V. Nielsen, Jordan Peccia, Xavier local exhaust, high efficiency air filtra- mission of SARS-CoV2; but in our col- Querol, Olli Seppänen, Shin-ichi Tanabe, Kwok Wai Tham, Pawel Wargocki, Aneta Wierzbicka, tion, and germicidal ultraviolet lights. lective assessment there is more than Maosheng Yao. • Avoid overcrowding, particularly in enough supporting evidence so that the The following scientists reviewed the docu- public transport and public buildings. precautionary principle should apply. In ment. Jonathan Abbatt, John Adgate, Alireza Afshari, Kang-Ho Ahn, Francis Allard, Joseph order to control the pandemic, pending Allen, Celia Alves, Meinrat O. Andreae, Isabella Such measures are practical and often the availability of a vaccine, all routes of Annesi-Maesano, Ahmet Arısoy, Andrew P. Ault, can be easily implemented; many are transmission must be interrupted. Gwi-Nam Bae, Gabriel Bekö, Scott C. Bell, not costly. For example, simple steps We are concerned that the lack of rec- Allan Bertram, Mahmood Bhutta, Seweryn Bialasiewicz, Merete Bilde, Tami Bond, Joseph such as opening both doors and win- ognition of the risk of airborne trans- Brain, Marianna Brodach, David M. Broday, dows can dramatically increase air flow mission of COVID-19 and the lack of Guangyu Cao, Christopher D. Cappa, Annmarie rates in many buildings. For mechanical clear recommendations on the control Carlton, Paul K. S. Chan, Christopher Chao, Kuan-Fu Chen, Qi Chen, Qingyan Chen, David systems, organizations such as ASHRAE measures against the airborne virus will Cheong, Per Axcel Clausen, Ross Crawford, Derek (the American Society of Heating, have significant consequences: people Clements-Croome, Geo Clausen, Ian Clifton, 2 • CID 2020:XX (XX XXXX)