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Viewpoint
July 13, 2020

Airborne Transmission of SARS-CoV-2: Theoretical Considerations and Available Evidence

Author Affiliations
  • 1Harvard Medical School and Harvard Pilgrim Health Care Institute, Department of Population Medicine, Boston, Massachusetts
  • 2Department of Medicine, Brigham and Women’s Hospital, Boston, Massachusetts
JAMA. 2020;324(5):441-442. doi:10.1001/jama.2020.12458

The coronavirus disease 2019 (COVID-19) pandemic has reawakened the long-standing debate about the extent to which common respiratory viruses, including the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), are transmitted via respiratory droplets vs aerosols. Droplets are classically described as larger entities (>5 μm) that rapidly drop to the ground by force of gravity, typically within 3 to 6 feet of the source person. Aerosols are smaller particles (≤5 μm) that rapidly evaporate in the air, leaving behind droplet nuclei that are small enough and light enough to remain suspended in the air for hours (analogous to pollen).

Determining whether droplets or aerosols predominate in the transmission of SARS-CoV-2 has critical implications. If SARS-CoV-2 is primarily spread by respiratory droplets, wearing a medical mask, face shield, or keeping 6 feet apart from other individuals should be adequate to prevent transmission. If, however, SARS-CoV-2 is carried by aerosols that can remain suspended in the air for prolonged periods, medical masks would be inadequate (because aerosols can both penetrate and circumnavigate masks), face shields would provide only partial protection (because there are open gaps between the shield and the wearer’s face), and 6 feet of separation would not provide protection from aerosols that remain suspended in the air or are carried by currents.

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    13 Comments for this article
    EXPAND ALL
    Is This All We've Got? A Plea to the Scientific Community
    Adam Collins, MD | VA
    Thanks for this article and the points of view it represents along with supporting references. As an anesthesiologist, I remain interested in the risk presented to healthcare workers, particularly from patient care on patients who are thought to be COVID negative. Tests themselves and the timing of testing will allow a certain percentage of patients to slip by and encounter large numbers of healthcare workers. I'm wondering when we will have current studies that we will consider high quality and why we are still talking about case studies from months ago or studies on other viruses. There have been millions of cases of COVID worldwide, and the information on the risk to healthcare workers should be getting more current and better, not just repackaged. Specifically, the two case reports referenced here (#s 5 and 6) are single cases with heterogenous exposure, heterogeneous PPE and likely lower sensitivity testing than we currently have. The data you cite with respect to low average attack rates in shared living situations probably doesn't necessarily represent the spectrum of possibility. This virus is not average and there is a mix of attack rates from case to case, ranging from zero transmission to superspreader events. The published superspreader events as well as ones I have witnessed in my own hospital indicate that at times it is very easy for CoV-2 to spread to large numbers of people. This happens in churches and restaurants, but also in healthcare environments including those with high grade ventilation, regular cleaning and mandatory use of masks and other standard PPE. Just to give you a sense of what I mean, one patient came in to our hospital and produced a positive PCR test 2 days later. A cluster of 34 new cases developed over the next week.

    How can we get current, high grade evidence on what it takes to keep healthcare workers safe in the workplace? Unless we have better science on this, scarcity of PPE and healthcare economics will drive practices that may turn out to be unsafe.
    CONFLICT OF INTEREST: None Reported
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    Droplets and Aerosols in COVID-19 Transmission
    Michael McAleer, PhD (Econometrics), Queen's | Asia University, Taiwan
    The detailed and informative presentation by expert medical scientists is a significant contribution to recognizing and understanding the spread of the SARS-CoV-2 virus that causes the COVID-19 disease.

    A related comprehensive discussion of the transmission of COVID-19 by droplets and the lighter evaporating aerosols is presented in Jayaweera et al. (2020) (1).  

    It is a salutary lesson that the World Health Organization (WHO) should accept and publicize, in view of their seeming reticence to acknowledge the prevalence of airborne transmission in both confined and open spaces.

    If the virus can be carried by aerosols that remain
    suspended in the air and are carried by currents, it follows that medical masks, ventilators, face shields, and social distancing would not likely be sufficient to provide adequate protection for anyone, let alone health care providers.

    This should be of immense concern to everyone who relies on PPE - that they might not be sufficiently effective in the face of airborne transmissions.

    It is seriously problematic that coughing can lead to secretions of both droplets and aerosols that can travel distances and last for several hours.

    The lack of clinical trials on how COVID-19 and other types of coronaviruses might be contracted is far from reassuring, as COVID-19 seems to be an especially virulent form of coronavirus.

    Airborne transmissions should be of concern to all governments that are opening up their societies and economies, such as allowing transportation on public trains and buses, large sporting and theatrical events, beaches, encouraging tourism, and opening up of restaurants, bars, and cafes.

    The effects of temperature and seasons on the transmission of COVID-19 is as yet unknown because of a lack of clinical and experimental trials, which is another area of research that should be considered seriously.

    Convincing the WHO of the importance of publicizing the importance of airborne transmissions is essential in making the medical fraternity and the general public aware of the importance of significant care and attention in accessing cautionary protective measures.

    Reference

    1. Jayaweera, M., H. Perera, B. Gunawardana and J. Manatunge (2020), Transmission of COVID-19 virus by droplets and aerosols: A critical review on the unresolved dichotomy, Environmental Research, 88, September 2020, published online 2020 June 13.
    doi: 10.1016/j.envres.2020.109819. 
    https://www.sciencedirect.com/science/article/pii/S0013935120307143?via%3Dihub
    CONFLICT OF INTEREST: None Reported
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    Correction of Error on Droplet Aerodynamic Behaviour
    John Murphy, PhD ROH CIH MACE | University of Toronto
    I wish to make a minor observation with respect to the paper by Klompas et al. The 5 μm aerodynamic diameter cut-point for "droplets", above which they are believed to "rapidly drop to the ground by force of gravity, typically within 3 to 6 feet of the source person", is far too low.

    Stoke’s Law predicts the terminal settling velocity of a 5 µm droplet under the influence of gravity in perfectly still air to be on the order of 0.1 centimeter per hour. With such a low settling velocity those droplets would not fall-out
    under force of gravity within 3 to 6 feet of explusion. At 50 µm, the physical diameter at which a droplet would first become visible, it is closer to 6 cm per hour, and similarly would not fall-out within 3 to 6 feet. In fact, the Wells-Riley equation predicts that all non-visible droplets would, under most common indoor and outdoor atmospheric conditions, transform to droplet nuclei. As the authors correctly note, "whether droplets or aerosols predominate in the transmission of SARS-CoV-2 has critical implications."
    CONFLICT OF INTEREST: None Reported
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    Aerosol from Respiratory Support Devices?
    Aiman Tulaimat, MD | Cook County Health
    At our institution, the tough decision is not so much about use of PPE for spontaneously breathing patients but about patients on high flow NC or CPAP. Should they be in negative pressure rooms? Should these rooms have anterooms? And what PPE should we use when we enter these rooms?
    CONFLICT OF INTEREST: None Reported
    Airborne component of transmission is thus proven
    Bruce Davidson, MD, MPH | Pulmonary Medicine
    The authors' analysis is interesting but has several flaws. Thanks to commenter Professor John Murphy of Toronto for explaining that expelled "droplets" are not dichotomous, falling within 6 feet or floating, but within a spectrum, and smaller gobs can dry out and remain airborne like the tiniest readily respirable ones.

    Repeatedly conflating influenza and COVID-19 is erroneous. Human influenza viruses primarily target sialic acid alpha 2,6 receptors on ciliated and mucosal cells abundant in the upper airway. SARS-CoV-2 binds to ACE2 surface proteins found in intact humans in deeper airways and the alveoli. Proximal airway ACE2 surface protein
    is limited to basal layers, not accessible to surface virus (1). This profound difference in accessibility of target cells disallows or at least targets for close scrutiny the authors' repeated analogies to influenza to promote "droplet" transmission and disallow "aerosol" transmission.

    Their analogies are a far too slender reed on which to lean. They claim a SARS-CoV-2 contact infection risk among household members of 10-40%, drawing a contrast with measles! But the household contact infection (i.e., a tuberculin skin test > 10mm) risk for tuberculosis active cases was 35% for high-income countries (such as the USA, where BCG is not administered) in a quite large meta-analysis (2). Most (but not all!) TB infection is believed to be by tiny droplets that clear the pharynx and the vocal cords.

    In fact COVID-19 infects both ways, by bigger and tiny droplets. We should disinfect indoor air with enhanced ventilation, low-dose upper-room germicidal UVC with ceiling fans, and HEPA filtration, depending upon the circumstance. 

    Typhoid and cholera outbreaks were stopped by creating both sewage and water treatment, as well as strict food-handler rules. It's time to stop debating by inference and rely on pathophysiology and public health disease control practice.

    REFERENCES

    1. Hamming I, J Pathol 2004; 203: 631–637
    2. Fox G et al, Eur Respir J 2013;41:140-156
    CONFLICT OF INTEREST: None Reported
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    Finally!
    Erin Wilkes, MD, MSHS, FACEP |
    Finally, someone summarizes the evidence well. Thank you! All great points.

    I would add that given that the virus is novel and spans the full spectrum of respiratory illness (from asymptomatic to ARDS) with transmission possible in both the asymptomatic and pre-symptomatic state, if it was truly airborne in the classic sense (measles), it would have infected the entire world before we even new that it was here, just from the amount of travel between China, the US, and Europe alone. People drastically underestimate how challenging it is to identify a novel virus such as this in the midst
    of flu season in the modern era.

    If only we could get the rest of the medical community and the public to understand this article.

    I know many have criticized the WHO, but I applaud its reluctance to get caught up in poor science with so much at stake, especially in the developing world.
    CONFLICT OF INTEREST: None Reported
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    SARS-CoV-2 Suspension Time
    Andrew Smith |
    “If, however, SARS-CoV-2 is carried by aerosols that can remain suspended in the air for prolonged periods, medical masks would be inadequate (because aerosols can both penetrate and circumnavigate masks)”

    Aerosols are mostly blocked by masks, not just N95, but surgical masks, and many homemade types. This has been documented by many studies. Aerosols can circumnavigate masks, which means that masks may not protect the wearer much. But the rationale for using masks is that they protect others from the wearer, and most aerosols will not circumnavigate masks of the wearer. The masks don’t have to function perfectly to
    reduce greatly the amount of virus that might be exhaled.

    “People infected with SARS-CoV-2 may be producing both droplets and aerosols on a constant basis but most of these emissions are not infecting other people. This pattern seems more consistent with secretions that fall rapidly to the ground within a narrow radius of the infected person rather than with virus-laden aerosols that remain suspended in the air at face level for hours where they can be inhaled by anyone in the vicinity.”

    Particles or droplets in the air exist of course on a continuum. Very small particles may remain suspended in the air for hours, while larger ones may settle in shorter periods, but remain airborne for a long enough period to extend out to a considerable radius. That such particles may spread SARS-CoV-2 is supported by calculations of saliva concentrations that suggest particles < 10 um in diameter (after dehydration) will contain few if any viral copies. Particles of 10 um or larger (even if not technically referred to as an aerosol) may remain suspended for a few minutes. This is certainly enough time to spread some distance from the infected individual, while not remaining in the air for very long. This could explain the much lower R0 compared to the measles virus (MV). The MV may exhibit greater shedding, resulting in more viral copies present in very small aerosol particles. Also, MV may have a lower infectious dose than SARS-CoV-2.
    CONFLICT OF INTEREST: None Reported
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    We Should Not Ignore Small Persistent Particles that Can Travel > 2 meters.
    Joseph Brain, ScD., MA, S.M.in Hyg. | Harvard TH Chan School of Public Health
    The airborne transmission of SARS - CoV - 2 is a critical topic, however we disagree with the authors' conclusion that small persistent aerosols are not involved. Particularly in large spaces where many share the same recycled air, it is dangerous to suggest that these particles are never important and can be ignored. We also fault them for not supporting an adjacent conclusion that UV light can be deployed to prevent this transmission pathway. Reducing persistent infectious aerosols is important. Here are facts that support these conclusions:

    Motion of all airborne particles is size dependent. The magnitude of
    particle displacements are a continuous variable determined by their size, density, and shape. There is no bright line. Although larger particles fall by gravity, as particle size decreases sedimentation rates decrease, while particle diffusion [Brownian movement] displacements increase. Small particles are those more likely to remain airborne longer. Somewhere around 1 micron in size, gravity becomes less important than particle diffusion. These particles stay suspended longer and are thus more persistent. Two meters separation is inadequate to avoid contact and possible airborne transmission by these aerosols. They can travel farther than that, unlike larger droplets. EPA air pollution standards use PM 2.5, particles smaller than 2.5 microns, as a reliable parameter of risk for particles that travel long distances.

    Wet particles evaporate and become smaller; 99.5% of emitted droplets is water. The emphasis on “microdroplets” rather than large droplets is correct and has attracted the attention it deserves. However the concern typically emphasizes sizes coming from humans. They begin as a polydisperse distribution which includes small particles that may persist as well as large particles that settle. We emphasize that larger particles become smaller as they evaporate. Evaporation rates are well described with critical variables being relative humidity, temperature, and convection. The drier the air the faster the evaporation rates. Thus some droplets which might have settled by sedimentation, become smaller aerosols which persist and disperse by movement of ambient air. Water evaporates, however solutes, proteins, and the virus do not.

    Deploy UV technologies to kill SARS - CoV - 19 now. All tools must be deployed to cope with this pandemic such as testing and tracking as well as mask wearing. An effective tool which needs to be used more is the use of ultraviolet light to kill the virus. Considerable data exists using devices already designed and manufactured. They can be deployed in a variety of spaces ranging from large communal rooms in airports and prisons to individual patient rooms in hospitals. These devices are" shovel ready” and affordable. They could be used in classrooms in schools, meat packing factories, and in Walmart stores.

    We appreciate the opportunity to discuss risk mitigation and to promulgate best practices throughout the United States. Only then will we see the progress we need.

    References:

    1. Brain JD, Valberg PA. Deposition of aerosol in the respiratory tract. Am Rev Respir Dis. 1979;120(6):1325‐1373.
    2. Nardell EA, Nathavitharana RR. Airborne spread of SARS-CoV-2 and a potential role for air disinfection. JAMA. 2020. (In Press)
    CONFLICT OF INTEREST: None Reported
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    Flawed Arguments Against Aerosol Transmission
    Jose-Luis Jimenez, PhD | University of Colorado-Boulder
    I am one of the scientists who co-wrote the Morawska & Milton-led letter in Clinical Infectious Diseases making the case for the importance of aerosol transmission (1). 

    The arguments against aerosol transmission by Klompas et al. are seriously flawed. Not a single one of them is strong. JAMA is not accepting responses to their COVID-19 coverage due to the high volume of submissions, so we are preparing a response to be submitted to a different journal.

    In the interest of timeliness, I link here a thread that I have written highlighting the flaws in the article (2),
    with an expanded argument elsewhere (3). I understand that this is unusual, but these are unusual times. The thread format allows for images, videos, links, and more length, which are needed for understanding of the counterarguments.

    Please email me if you feel that my arguments have flaws (and please explain what they are and provide references), or if there are other arguments that you think disprove aerosol transmission of SARS-CoV-2 (and then please explain those arguments and provide references).

    REFERENCES

    1. https://academic.oup.com/cid/article/doi/10.1093/cid/ciaa939/5867798
    2. https://twitter.com/jljcolorado/status/1283668758884581377
    3. www.medscape.com/viewarticle/934837?src=uc_mscpedt&faf=1#vp_6
    CONFLICT OF INTEREST: None Reported
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    Aerosol transmission – Out with the Old, In With the New
    Julian Tang, PhD, MRCP, FRCPath | Respiratory Sciences, University of Leicester, Leicester, UK
    We felt compelled to respond to the Viewpoint by Klompas et al., published on 13 July 2020 in JAMA. There are some myths perpetuated in this Viewpoint, which emanate from firmly entrenched views held by the medical profession among others.

    Aerosol science has moved on from the rigid definitions of the past and some forward thinking is required in light of the current pandemic. Droplets of <5 µm deserve special attention because of their ability to penetrate the alveolar space, but they are just one end of a spectrum of droplet of different sizes, some of which would
    have been originally classified as ‘large’ droplets and yet can actually travel more than 2 m when carried by a jet of air.

    Infections acquired from aerosols are not necessarily as contagious as measles; tuberculosis, for example, has a Ro of up to 4.3 [1], and patients with hantavirus pulmonary syndrome are not contagious. Given the suspected high rate of asymptomatic infection and almost certain role in onward spread of SARS-CoV-2, the Ro for Covid-19 must be a serious underestimate.

    The lack of reports of long-range transmission for SARS-CoV-2, in contrast to measles or chickenpox, does not rule out short-range aerosol transmission of SARS-CoV-2 [2]. Historically it has been difficult to demonstrate long-range transmission of a virus widespread in the community [3].

    The proven capacity of MERS-CoV and SARS-CoV-1 to generate infectious aerosols is a relevant warning about the closely related SARS-CoV-2 [4].

    The recommendation by Klompas et al. for optimizing indoor ventilation is an implicit admission of a role for aerosol transmission of SARS-CoV-2. Increasing air changes would not impact on viral acquisition through direct contact or transmission from large droplets falling onto nearby surfaces.

    The point is not whether aerosol transmission is the dominant mode of transmission but whether it occurs often enough to warrant active mitigation as part of a comprehensive control strategy. From evidence amassed so far, there is more than enough intelligence to trigger a precautionary approach.

    Raymond Tellier (Department of Medicine, McGill University, Montreal, Canada)
    Julian W Tang (Respiratory Sciences, University of Leicester, Leicester, UK)
    Stephanie Dancer (School of Applied Sciences, Edinburgh Napier University, Edinburgh, UK)

    References

    1. Ma Y, Horsburgh CR, White LF, Jenkins HE. Quantifying TB transmission: a systematic review of reproduction number and serial interval estimates for tuberculosis. Epidemiol Infect. 2018;146(12):1478-1494. doi:10.1017/S0950268818001760

    2. Chen W, Zhang N, Wei J, Yen HL, Li Y. Short-range airborne route dominates exposure of respiratory infection during close contact. Build Environ 2020;176:106859. doi.org/10.1016/j.buildenv.2020.106859

    3. Gelfand HM, Posch J. The recent outbreak of smallpox in Meschede, West Germany. Am J Epidemiol. 1971 Apr;93(4):234-7. doi: 10.1093/oxfordjournals.aje.a121251.

    4. Tellier R, Li Y, Cowling BJ, Tang JW. Recognition of aerosol transmission of infectious agents: a commentary. BMC Infect Dis. 2019;19(1):101. doi:10.1186/s12879-019-3707-y
    CONFLICT OF INTEREST: None Reported
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    Interventions Should Be Based on Research on Bioaerosols
    Mary Wilson, MD | University of California San Francisco
    The topic of transmission of SARS-Cov-2 merits attention [1]. The key question is not whether aerosol transmission is the predominant means of transmission but rather whether it contributes to transmission. Depending on the setting – the characteristics of the infected person (e.g., stage of infection, presence of symptoms, other personal characteristics, activities such as shouting, singing, breathing, physical exercise) and the physical environment (e.g., size of the space, ventilation, temperature, humidity, number and density of people), aerosol route may account for none, a little, or a lot of viral transmission. The relative proportion of transmission from droplet, contact with contaminated surfaces and materials, and microdroplets or aerosol is not fixed and will vary depending on the circumstances. Interventions to protect people should be based on the possibility of aerosol spread [2]. Although most transmission may occur from droplets encountered in close proximity (1-2 meters) to an infected individual, some microdroplets may hang in the air outside of this perimeter and result in transmission, especially in crowded indoor spaces with poor ventilation.

    Current approaches to preventing spread – physical distancing, handwashing, and wearing a mask – are all important. These can be supplemented by other means – such as preventing high density gatherings in poorly ventilated indoor spaces and paying more attention to ventilation, air exchanges and use of germicidal UV radiation, to reduce risk of indoor spread.

    1. Morawska L, Milton DK. It is Time to Address Airborne Transmission of COVID-19, Clinical Infectious Diseases, , ciaa939, https://doi.org/10.1093/cid/ciaa939

    2. Rapid Expert Consultation from the National Academies Standing Committee: Rapid Expert Consultation on the Possibility of Bioaerosol Spread of SARS-CoV-2 for the COVID-19 Pandemic (April 1, 2020) https://www.nap.edu/read/25769/chapter/1
    CONFLICT OF INTEREST: None Reported
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    Authors' Response
    Michael Klompas, MD, MPH | Harvard Medical School and Brigham and Women's Hospital, Boston, MA
    We write to express our gratitude for the many thoughtful comments on our paper. Many of the readers’ comments reinforce a primary message of our paper, namely that simply dividing transmission into droplets versus aerosols is overly simplistic. Respiratory emissions include a range of particles in many different sizes, there is no clean-cut point between droplets versus aerosols, and all secretions can play a role in transmission depending upon circumstances.

    As Dr. Wilson eloquently noted in her comments, the relative contributions of fomites vs droplets vs aerosols vary depending upon the infected source’s viral burden, activities (breathing vs
    talking vs coughing), and the environment they occupy (dimensions, ventilation, etc.). We would add to this list the exposed person's proximity to the source person and duration of exposure. These parameters all play a role in determining the overall amount of virus to which people are exposed and thus their risk of infection. Exposure to larger amounts of virus increases the risk of infection, exposure to smaller amounts carries a lower risk of infection. This is presumably why household contacts of an infected person are 6 times more likely to get infected compared to non-household contacts.

    There are multiple ways one can be exposed to larger amounts of virus: if the infected person has a high viral burden, if the source is engaged in activities that generate greater amounts of respiratory secretions (e.g. singing, coughing, or being intubated), if one is close to the source where the density and quantity of virus-laden droplets and aerosols are greatest, if exposure is prolonged because it increases the cumulative dose, and if ventilation is poor because this allows otherwise insignificant amounts of virus-laden aerosols to accumulate. Aligning these factors may account for superspreading events.

    Conversely, the risk of infection is diminished if the infected person has a low viral burden, was only producing a small amount of secretions (e.g. quiet breathing), the duration of exposure was brief, the distance from the infected person was great (because distance can transcend the range of infectious droplets and allow for dilution of virus-laden aerosols over exponentially greater volumes of ambient air), the quality of ventilation good (because refreshing the air dilutes residual virus-laden aerosols), the interaction occurred outside, the source patient was wearing a mask that contained their secretions, and if the exposed person was wearing a high-quality mask because they can block most droplets and some fraction of aerosols leading to a lower net inoculum. Host defenses likely also play a role.

    The bottom line is that transmission risk is a function of many factors. Presenting only part of the equation – such as showing that people can produce aerosols that remain suspended in the air for long periods or that it is possible to recover viral RNA from air samples – can lead to a misleading impression of disease risk and the relative importance of various mitigation strategies. Experimental data on viral dynamics, aerosol behavior, and prevention strategies need to be paired with clinical data on actual infection rates in order to understand their significance. We are sympathetic to the desire to exercise the precautionary principal while we all continue to gather these data but echo the plea in Dr. Collin’s comments for high-grade evidence on what’s truly necessary to prevent actual infections.

    Michael Klompas MD, MPH
    Meghan Baker MD, ScD
    Chanu Rhee MD, MPH
    CONFLICT OF INTEREST: None Reported
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    Misunderstanding of Ventilation
    Mark Mendell, MPH, PhD | California Department of Public Health
    While I commend the authors for their summary of current evidence on transmission of COVID-19, there are 2 important problems with their piece:

    1) ) The question they pose is the wrong one: "Determining whether droplets or aerosols predominate in the transmission of SARS-CoV-2 has critical implications." Their conclusion is then an answer to the wrong question. The question of actual interest is, how much aerosol transmission is occurring? This is what should influence public health decisions.

    (2) They misunderstand the effects of ventilation: ventilation is the introduction of outdoor air into a building, replacing indoor air and
    thus diluting the indoor concentration of contaminants produced indoors.

    The review "finds that aerosol-based transmission appears to be less likely. This result means that six feet of physical distancing, wearing face coverings (either medical masks, cloth masks, or face shields), maintaining hand hygiene, and keeping environments well ventilated should be effective in stopping COVID spread."

    While the authors may understand disease and infection generally, they apparently do not understand that if good indoor ventilation decreases transmission of a disease, this is proof of long-range airborne transmission of the disease by small aerosols. Otherwise ventilation has no effect! Ventilation does not reduce short-range transmission of either large droplets or small aerosols.

    Thus the conclusions and recommendations of this piece, because of these two limitations, unfortunately may obstruct proper attention to possible long-range airborne transmission in this pandemic.
    CONFLICT OF INTEREST: None Reported
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