COMMENTARY

COVID-19 Data Dives: Why Arguments Against SARS-CoV-2 Aerosol Transmission Don't Hold Water

Jose-Luis Jimenez, PhD

Disclosures

July 30, 2020

Medscape asked top experts to weigh in on the most pressing scientific questions about COVID-19. Check back frequently for more COVID-19 Data Dives, and visit Medscape's Coronavirus Resource Center for complete coverage.

Jose-Luis Jimenez, PhD

I am an aerosol scientist. I have spent a lot of time examining the arguments from some that aerosols play only a very minor role in the transmission of SARS-CoV-2 -- and presenting the evidence that rebuts this claim. A recent article in JAMA argues that aerosols are not an important transmission pathway for SARS-CoV-2. While the article raises good questions, the arguments against aerosols are not consistent with the best science. Here's why I say that:

Aerosol size. Most important, a good understanding of aerosol physics, airflow, and dilution is needed to interpret the behavior of potentially infectious aerosols in complex real-world situations.

Some of the arguments made are based on differences in aerosol and droplet sizes. Both are particles of solid or liquid material in air, with the difference being that aerosols stay suspended for longer times (minutes to hours indoors), while droplets behave ballistically and fall to the ground quickly (in seconds). To be sure, size is the most important property of particles, and because mass increases with the cube of the diameter, the fate and transmission mode of aerosols and droplets change dramatically with size. The authors write, "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."

However, the actual size of droplets that fall to the ground that quickly correspond to sizes larger than 50 μm, so 10 times the size and 1000 (!) times the mass given in the article. This fundamental error has been repeated for decades in guidance from the Centers for Disease Control and Prevention (CDC) and the World Health Organization (WHO) and in medical papers, despite the correct physics having been figured out by Wells in 1934 and the error having been pointed out many times by other scientists.

This video from Ryan Davis, PhD, gives a more accurate picture of the behavior of ~50 μm aerosols in the air. Even at this size, the aerosols do not fall very rapidly to the ground. For aerosols of 5 μm to fall to the ground quickly, as shown in a short animation from the WHO, gravity on Earth would have to be 100 times larger than it is. This happens...on some stars. A 5 μm aerosol can actually stay suspended in air for 30 minutes indoors.

If 5-μm aerosols fell to the ground as stated by the authors and as shown in the WHO's video, we would not have to worry about aerosol (particulate matter) pollution, because a large fraction of it would fall to the ground so quickly. We also would not have to worry about Saharan dust reaching Florida, because much of the dust mass is composed of aerosols in this size range.

The authors further instruct us that "[a]erosols are smaller particles (≤5 μm) that...are small enough and light enough to remain suspended in the air for hours (analogous to pollen)." This is curious, given that pollen ranges in size from 15 to 200 μm. If pollen aerosols, being larger than 5 μm, actually fell to the ground within 1-2 meters, pollen allergies would not be a problem either. But pollination for many plant species would be very difficult too. Relying on medical doctors for advice about aerosols is like relying on me, an aerosol scientist, for medical advice: not a good idea.

Distance vs transmission. Next, the authors posit that "6 feet of separation would not provide protection from aerosols that remain suspended in the air or are carried by currents." This statement does not account for how aerosols spread and dilute.

Exhaled aerosols are most concentrated right in front of the nose and mouth, and get increasingly diluted by air currents with increasing distance.

Think about talking with a smoker (smoke is an aerosol). If you are 1 meter apart, there will be a lot of smoke in between you. There will be much less smoke in the room at the start, although it can build up over time if there is low ventilation.

Now, realize that exhaled respiratory aerosols will behave in the air as the smoke does, except that they are not visible. When talking close to another person, we inhale a fraction of the respiratory aerosols that they exhale (that may contain the virus). If we get farther and farther apart, then the aerosols, like smoke, get diluted and we breathe less of them. Thus naturally distance greatly reduces exposure to respiratory aerosols.

The conversation with a smoker is a qualitative example. But quantitative studies with very detailed physics have been published that estimate exposure to droplets and aerosols in a close proximity situation (often referred to as "close contact," although physical contact is typically not involved).

People often argue that droplets contain more volume, which is correct. However the volume that matters most is not that which is exhaled by the infected person, but that which is inhaled (aerosols) or makes ballistic impact on the eyes, nose, or mouth (droplets) of the susceptible person.

The key result of the study is that, when talking, aerosols overwhelmingly dominate transmission if the distance between the people is greater than 20 cm (8 inches). The ratio of exposure by inhalation of aerosols to impact of droplets is 100 times larger at a distance of 0.5 meters. And that ratio rises to 2000 times greater once the distance increases to 1 meter. Typical US conversational distance is 0.5-1 meter. Droplets have larger volume to begin with, but the aerosols are more finally divided (providing more chances for inhalation) and stay much longer in the air, so that the physics of aerosol and droplet motion overwhelmingly favor aerosol exposure.

Therefore, aerosols probably dominate "close contact" transmission when talking. And talking is the most relevant situation for SARS-CoV-2, which has a major fraction of transmission by asymptomatic and presymptomatic carriers who do not regularly cough. These are the conclusions of a modeling study — it was notably rigorous —using well-established inputs: Newton's laws of motion; the law of gravity; the well-known laws of air drag on moving aerosols; and well-established measurements on the sizes, amounts, and speeds of the expired aerosols. This is not difficult, uncertain physics, such as trying to quantify the expansion of the universe or the mass of neutrinos; it is very well established and tested. Like any scientific study, it has uncertainties, but those are unlikely to reach factors of 100-1000.

For many decades it was thought that tuberculosis was transmitted through droplets and fomites, because transmission seemed to be strongly favored extended "close contact." It was later proven that tuberculosis can only be transmitted through aerosols, highlighting the difficulty of concluding which route may dominate on the basis of an observation of favorable transmission under "close contact."

Some people argue that the clear effectiveness of limiting "close contact" through social distancing to reduce SARS-CoV-2 transmission demonstrates that droplets, which fall to the ground close to the person, are the dominant mode of transmission, and that the same observation disproves aerosols as an important source of infection. The reality is the opposite. That "close contact" is a major mode of transmission of SARS-CoV-2 does not disprove aerosols. Rather, it is some of the best evidence we have that aerosols are important and very likely major.

Long-range transmission. Next, the authors conclude: "the data...are difficult to reconcile with long-range aerosol-based transmission." This I agree with, but long-range, aerosol-based transmission is not something we think is major for SARS-CoV-2 transmission. There is aerosol transmission, but typically with much lower contagiousness than measles, for example. A ballpark estimate is about 20 times less.

Lower infectiousness means that aerosols will infect best at "close contact" when they are most concentrated and one person is inhaling the expired aerosols of the other with the least dilution with room air. Aerosols are less likely to lead to infection at the room scale, but they can do so if we "help" them accumulate and be breathed in (like in the smoke example) with indoor locations, low ventilation, long duration, crowding, talking or singing, and no masks, as in the Skagit Valley Chorale case. We have to accept that talking, and especially singing or shouting, are "aerosol-generating procedures." They do not generate aerosols on the same scale as intubation. But they do so for much longer periods of time, in environments with much lower ventilation than most hospitals, and often without masks. As has been shown for tuberculosis, respiratory aerosol generation in an office was 3000 times less than during intubation, and yet it led to an outbreak with two dozen new infections.

We would expect aerosols to have trouble infecting at very long range, such as through the ventilation system of a commercial building, owing to very high dilution. Long-range infection can probably still happen under very favorable situations, but it is very unlikely to be driving the pandemic. But it is also important to realize that it is hard to identify long-range transmission for a disease unless there are very few cases. For example, if a traveler infected by measles arrives in a city where that disease is not present, several new cases may result. It may then become obvious to the public health investigators that some of the cases can only be explained by long-range transmission. Given the current spread of COVID-19, it is very difficult to make that determination. In addition, diseases like measles almost always present with distinctive symptoms, making the identification of new cases much easier than for COVID-19.

R0. The article goes on to discuss "R naught" (R0), a mathematical term that indicates the average number of new cases expected to stem from a single person. The JAMA authors state that R0 is "quite different from that of viruses that are well known to spread via aerosols such as measles, which has a reproduction number closer to 18."

This argument about R0 is the most repeated argument against aerosols, and it is actually the weakest.

Diseases with very high average R0 are hard to explain without recognizing aerosols as the means of spread. It is difficult for a large number of people to touch the same contaminated surfaces or have extended time to exchange ballistic droplets under many situations. But many people assume that because the average R0 of COVID-19 is much less than that of measles, then SARS-CoV-2 does not transmit through aerosols. There is no basis for that assumption. SARS-CoV-2 is just much less contagious under most circumstances. The authors do acknowledge that possible explanation.

Attack rates. Next, the authors address attack rates, or rates of new infections, relative to contacts of the infected person, which are often relatively low for many infected individuals. They conclude, "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."

This reflects the same misunderstandings discussed above. No clear conclusions about the modes of transmission emerge from that observation. The virus is typically much less contagious than measles. The pattern of low attack rates can be explained by the substantial time it takes to breathe enough exhaled aerosols (dose) to lead to infection. It takes much longer at the room scale than at the scale of "close contact," because of much greater dilution. The broad variability in virus shedding among individuals is also likely be important for explaining this observation.

Importance of superspreading events. Then the authors state, "Proponents of aerosol-based transmission cite well-documented clusters of infections among choir participants, restaurant patrons, and office workers sharing closed indoor spaces. However, based on the reproduction number for SARS-CoV-2...these events appear to be the exception rather than the rule."

Except that these events have been shown to be quite common for SARS-CoV-2, and many researchers think that they are driving the pandemic; see this piece in the New York Times, or this opinion piece on superspreading and the studies linked therein. Two of the studies conclude that 2% of the infected resulted in 20% of the transmission, and that 10% led to 80%. For those subsets, R0 can be estimated as about 20-25. High values that are very difficult to explain without aerosols!

Given such a large fraction of spread through superspreading events, I have to agree with Prof. Donald Milton that these events could prove to be the Achilles' heel of SARS-CoV-2, and that we should focus on identifying their causes and preventing their occurrence. Definitely, the environmental conditions are key: indoor spaces, low ventilation, crowding, long duration, no masks, loud conversation or singing. Perhaps also there are unusual individuals who shed a lot more aerosolized virus than the majority of those infected, and for those individuals the contagiousness does approach that of measles?

Nonaerosol transmission in superspreading events. The authors state that "it is difficult to determine in retrospect all the potential person-to-person interactions that may have happened before, during, and immediately following these events."

Yes, it is difficult. But for the Skagit choir case that we investigated, 53 out of 60 people were infected during a 2.5-hour rehearsal. The choir spokesperson told me, "It is not a highly social group. It is pretty seriously about the singing." Most of the time, choir members were singing in fixed positions, and there was no one within the 1- to 2-meter "landing area" of ballistic droplets in front of the index case.

Members were aware of COVID-19, and reportedly no physical contact between choir members took place. They used hand sanitizer. The index case did not touch the snacks or help distribute the chairs. The index case did visit the restroom, but many members who did not use the restroom were infected.

In any case, fomite transmission appears to be less likely per CDC guidance, while the WHO admits that they do not have direct evidence for it. There was a 15-minute break, during which members talked to "two to three people" on average. Talking between the index case and others "was minimal." Could droplet transmission explain this event? Per the CDC, it would have required “close contact” of at least 15 minutes with 53 people!

Could this choir be an outlier? Well, as we report on our paper, choir cases with high secondary attack rates have also been reported in at least the Netherlands, Austria, Canada, Germany, England, South Korea, and Spain. A similar case in France was just reported. Yet, events like these are being dismissed by what can only be referred to as "contortionist thinking." A scientist interviewed by the New York Times summed it up well: WHO staff members have yet to accept the importance of these case studies and instead have "dreamed up an alternative story" in which an infected person spat on his hands, wiped it on something and "magically" infected numerous other people.

Gatherings of the same size without singing or shouting do not seem to lead to as much spread. This strongly suggests that it is the known higher respiratory aerosol generation during singing that is driving the increased transmission. Although talking results in lower respiratory aerosol generation, it can make up for it with longer time in the same room, low ventilation etc.

PPE. Why is there such a disconnect in the understanding of the role of aerosols in SARS-CoV-2 transmission? Although I do not work in the medical profession, it seems to me that in medicine, the dominant source of information about whether "aerosols" are participating in transmission arises from whether "airborne" personal protective equipment (PPE) and procedures are needed to stop transmission in health care settings. And information about the role of "droplets" being dominant is concluded from whether transmission that can be reasonably well managed with "droplet" PPE and procedures. Physics-based evidence is often dismissed as "theoretical" or "academic."

The relationship of those terms with the physical world seems to be almost completely missing from the interpretation of the PPE evidence. The physics of aerosols and droplets are much more complex and nuanced, and the real behavior of aerosols and droplets does not align with what the different types of PPE protect against.

Although the virus is small (about 0.12 μm), it is encased in larger aerosols containing respiratory fluid or saliva. Although data are scarce, we suspect that aerosols in the range of 1-10 µm produced in speech (not coughing or sneezing) dominate aerosol transmission of SARS-CoV-2. It is often stated than only N95 masks can stop most aerosols. This is true for pollution aerosols, with a typical size of 0.3 µm. But aerosols in the supermicron range are reasonably well filtered by well-worn surgical masks, potentially explaining why "droplet PPE" is quite effective against SARS-CoV-2 transmission in hospitals (as the authors argue may be the case), even if aerosol transmission is one of the main routes.

The authors discuss several studies conducted in hospital environments that examined the effectiveness of N95 vs surgical masks in reducing transmission. Some studies did report that N95 masks provided better protection, while others found no difference. The authors favor the latter studies and take those results as evidence against the importance of aerosol transmission. However, they fail to consider that those masks may not be that different for the supermicron particle size range that is probably most relevant to SARS-CoV-2 transmission, especially when accounting for the imperfect fit of N95 masks for some users in the real world. Additionally, patients with advanced COVID-19 may not release much viable virus in the absence of aerosol-generating procedures. Hospital studies are trying to measure what is probably a small difference in effectiveness, in a "noisy" environment with many confounding effects, which may lead to unclear results.

Demonstration of viable virus in the air. A final argument that is often made by scientists skeptic of the importance of aerosol transmission, including those advising the WHO (although not in this particular paper), is that viable SARS-CoV-2 has not been isolated from the air. A recent preprint claims to have done so, although the details still being debated among virologists.

But capturing viable pathogens from the air is extraordinarily difficult, owing to their low concentrations and their fragility when sampled by the instrumentation. In fact, viable pathogens have never been isolated from room air for either measles or tuberculosis (the latter with many attempts spanning almost a century), two diseases with well-established aerosol transmission. For tuberculosis, only directly sampling patient coughs in an unventilated space 25 times smaller than a typical room has been successful.

It makes no sense to keep demanding definitive proof of viable virus in room air before accepting aerosol transmission of SARS-CoV-2, in the face of mounting evidence supporting this route, the lack of strong arguments against it, and of actually less evidence for the other routes. Especially when the WHO admits that there is actually no direct evidence for fomite transmission of SARS-CoV-2, and large droplet transmission has never been demonstrated directly for SARS-CoV-2 or any other disease. But those are still the accepted routes of transmission, whereas aerosols are still described as much less important.

It appears that absence of (complete) evidence is being taken as evidence of absence, but only for aerosols. This century-old bias is rooted in the history of the field of medical infectious diseases, and in fact we are working with historians to document it.

A Way Forward

As I said at the top, I have spent a lot of time searching for the arguments to counter those who argue that aerosols play at most a very minor role in the transmission of SARS-CoV-2. This JAMA article did a good job of capturing almost all the points offered by these skeptics. And our analysis lays bare the lack of strong arguments against the importance of aerosol transmission for this virus.

The JAMA authors do provide some evidence in favor of aerosols. But in truth, there are many more arguments in favor of aerosols, which would take an article as long as this one to explain. Many of them were laid out in recent papers by Morawska and Milton (with our "group of 36" scientists) and by Prather, Wang, and Schooley. That only a major role for aerosols explains the observed patterns of transmission is a final, powerful argument.

It is unfortunate that key deciding bodies in major health organizations, that have concluded that SARS-CoV-2 does not transmit through the aerosol route, lack researchers with expertise in aerobiology, aerosols, and building science, among other disciplines. In this case, a general lack of awareness can lead to incorrect conclusions.

Going forward, major medical publications should engage aerosol experts to review papers that involve aerosol transport. More important, it is critical that medical researchers collaborate with aerosol researchers and related fields. The fact that the 5 μm error has persisted for decades (and that it is still part of the latest WHO scientific brief as of this writing) shows insufficient communication between fields that are inextricably linked. Although we know enough to strongly suspect that SARS-CoV-2 has a substantial component from aerosol transmission, there is a lot that we do not know and that we need to learn to fight this pandemic, future ones, and other respiratory diseases that also probably have an aerosol component in their transmission. In order to be successful, we need to all work together in the future and break down these barriers.

Author's note: Following publication of the paper discussed in this article, I posted a thread on Twitter about my concerns of flaws in the paper. I contacted JAMA's editors and asked to post a "letter in reply" that would exceed the journal's 500-word limit. As there were many issues to explain to an audience unfamiliar with the fundamentals of aerosol dynamics, the extra length was necessary. In response, I was informed that "because of the volume of submissions related to COVID-19 and the rapid evolution of the pandemic, we are not considering any letters to the editor about any of our COVID-related content." I therefore made the decision to publish this response on Medscape.

Jose-Luis Jimenez, PhD, is a professor in the Department of Chemistry and a Fellow of the Cooperative Institute for Research in the Environmental Sciences (CIRES) at the University of Colorado, Boulder. He is a highly cited researcher, and a fellow of the American Association for Aerosol Research and of the American Geophysical Union. The research of the Jimenez group centers on atmospheric aerosols and aerosol instrumentation. Follow him on Twitter.

Professor Jimenez is extremely grateful to Linsey Marr and Kimberly Prather for reviewing a draft of this text; to them and Lidia Morawska, Don Milton, Julian Tang, Raymond Tellier, Stephanie Dancer, William Bahnfleth, Shelly Miller, Richard Corsi, Catherine Noakes, Giorgio Buonnano, Bill Nazaroff, Atze Boerstra, Jarek Kurnitski, Arsen Melikov, Lydia Bourouiba, and many others for extensive discussions about the transmission of SARS-CoV-2; and to Babak Javid, Saskia Popescu, Eli Perencevich, Angela Rassmussen, Nathalie Dean, and many others for useful discussions about the evidence and arguments that support and not the different transmission routes. The opinions expressed here are the author's own.

Follow Medscape on Facebook, Twitter, Instagram, and YouTube

Comments

3090D553-9492-4563-8681-AD288FA52ACE
Comments on Medscape are moderated and should be professional in tone and on topic. You must declare any conflicts of interest related to your comments and responses. Please see our Commenting Guide for further information. We reserve the right to remove posts at our sole discretion.
Post as:

processing....