In early April, I wrote a long post covering all the science I could find about aerosols and droplets. The basic summary was that this is an area of medicine with lots of misconceptions, poor assumptions, and incomplete science. There was good evidence that previous coronaviruses were spread by aerosols. There was good evidence that influenza is spread by aerosols. Overall, it seemed very likely that SARS-CoV-2 or COVID-19 was being spread by aerosols, but the science was pretty weak. There is still a lot we don’t know, but as I update the evidence 6 months later, it is pretty clear that aerosols play an important, and unfortunately still widely ignored, role in the transmission of COVID-19.
Dispelling some misconceptions
There are still many who argue strongly against the role of aerosols in transmission of COVID-19. In general, I think these arguments clash with science and have significant logical inconsistencies. Before getting to the evidence that COVID-19 is spread by aerosols, let’s dispel a few widely held misconceptions.
COVID-19 has a low Ro
One main argument against aerosol spread points to the Ro, with the assumption that airborne diseases will always spread easily, and therefore have a high Ro. The argument is often framed as, “this disease doesn’t look like measles, and therefore cannot possibly be airborne.” This is bad logic, as infectivity and mechanism of transmission are separate concepts. Some pathogens require higher numbers to reliably cause infections, which will result in a lower Ro no matter how the infection is transmitted. “While many airborne infections are highly contagious, this is not, strictly speaking, part of the definition.” (Tellier 2019)
The logic here is clearly faulty. The argument being used has the basic format: “X is a Y. Z is not like X. Therefore Z cannot be a Y.” This is somewhat like saying “a horse is a mammal, therefore that dog cannot be a mammal because they don’t look the same.”
This logic is especially problematic in the context of aerosol spread because there are other diseases with good evidence of aerosol spread, such as influenza, that look nothing like measles, but a lot like COVID-19. In fact, the prototypical airborne pathogen is tuberculosis, and tuberculosis has an Ro between 1-3 (exactly like COVID-19). (Ma 2018)
Furthermore, the statement that ‘COVID looks nothing like measles’ is probably untrue. On average, disease transmission is low, but if you look at super-spreaders, COVID-19 starts to look a lot like measles.
Therefore, the arguments based on Ro are both illogical and inconsistent with science. If anything, the Ro of COVID-19 looks exactly like other known airborne diseases (such as tuberculosis), and so this would be an argument in favour of airborne spread.
Most transmission is short distance
The equally fallacious corollary to the Ro argument is that “if COVID-19 is transmitted through aerosols, we should see a lot of infections occurring over long distances”. Although it is true that aerosols will disperse much further than droplets, it is faulty logic to define the mode of transmission by the distance of transmission. The concentration of infectious particles falls dramatically with distance, even when those infectious particles are carried by aerosols. They are spread out through 3 dimensional space, and therefore decrease exponentially with distance. Although aerosols can transmit disease over long distances, they are much more likely to transmit disease over a short distance. (Chen 2020)
This illogical step is so ingrained in the infectious diseases literature that most studies just assume droplet spread if there was close contact. This illogical assumption undermines a great deal of the existing infectious disease literature.
As an interesting historical analogy, for decades it was thought that tuberculosis was transmitted through droplets and fomites, because it occurred most often after close contact. We now know that tuberculosis can only be transmitted through aerosols. (Jimenez 2020)
The existing science refutes the assumption that close contact suggests droplet spread. At the typical conversational distance of about 1 meter, exposure to aerosols is about 2000 times greater than exposure to droplets. (Chen 2020)
The bottom line is that short range disease transmission is definitely consistent with aerosol transmission, and distance cannot be used to define mode of transmission.
So why don’t we see a lot of long range transmission of COVID-19? The primary explanation is simple dilution. The further you are from a patient, the more dilute aerosols become. Risk of aerosol transmission drops off dramatically with increasing distance.
The importance of dilution of aerosols is evident in everyday life. You can smell cigarette smoke when you are standing 8 meters away from a smoker, but it is nothing like the obnoxious fumes present if you were standing right next to them. Similarly, cigarette smoke is much worse indoors than out. Imagine each smoke molecule as a virus. You are obviously at much higher risk 1 meter away than you are at 8 meters. (But that doesn’t make smoke a droplet.)
Dilution doesn’t prevent exposure to the virus, but it makes it less probable. With dilution of aerosols, the primary driver of infection is the intrinsic infectivity of the pathogen. If infection occurs after exposure to only a few viral particles, we should expect to see more long range transmission despite the dilution. If larger exposures are required, we will see fewer infections. This is the primary difference between measles and COVID-19.
One final note about long range transmission: we really don’t know how common it is in COVID-19. Identification of long range transmission is incredibly difficult unless there are a very small number of cases. With a small outbreak of measles cases, it is easier to determine exactly where individuals were, and identify airborne transmission. For the vast majority of COVID-19 cases, we do not know how the individual became ill, and so could easily be overlooking long range transmission (especially when the possibility of aerosol transmission is dismissed out of hand in some circles). In fact, there seems to be pretty good evidence of long range transmission in many of the super-spreader events discussed below.
Our current approach is working
Another argument occasionally used to dismiss aerosols as a mode of transmission is that our current PPE approach seems to be working in hospitals. First, I would point out that healthcare workers are contracting COVID-19 at a rate that is far higher than the general population, so this argument is pretty weak. Furthermore, as will be explored further below, there are many other factors that significantly dilute aerosols in most hospitals, like excellent ventilation, good distancing, and masking of both patients and providers. Although not quite as good as N95s, well fitting surgical masks will still filter out as much as 80% of infectious aerosols. (Makison Booth 2013) Combined with the low infectivity of SARS-CoV-2, these factors keep us relatively safe even when we stubbornly ignore the science that suggests aerosols are very important in the transmission of COVID-19.
Many of the arguments against the aerosol spread of COVID-19 rely on incorrect assumptions about particle size. I went into this at length in the first post, so won’t repeat myself here. The basic summary is that particles of sizes that many articles refer to as droplets actually remain airborne for prolonged periods, and are therefore better classified as aerosols for the purposes of transmission. Just be careful when reading articles, because many don’t define these terms. When I use the term aerosol here, I am referring to any droplet that remains suspended in the air for longer that a few seconds, whatever the size, because that is the feature that matters for infection control.
The lack of definitive proof
Some of the arguments against aerosol transmission simply assume droplet transmission and demand “definitive proof” for aerosol transmission. I won’t attempt a treatise on the philosophy of science here, but that is an unreasonable bar.
One version of this argument states that viable SARS-CoV-2 has never been isolated from the air, and therefore we cannot definitively prove airborne transmission. This demand is unreasonable. Measles and tuberculosis are both known to be airborne, and no one has been able to isolate viable pathogens for either from the air. (Jimenez 2020) Furthermore, this is probably an outdated argument, as multiple studies actually have identified viable SARS-CoV-2 in the air. (Lednicky 2020; Santarpia 2020a)
The specifics of whether or not viable virus has been cultured from air samples is irrelevant. The point is that unfair standards are being used when comparing aerosols and droplets. There is no definitive proof that SARS-CoV-2 spreads through large droplets. (Jimenez 2020) It is crazy to require such stringent proof of aerosol transmission, while simultaneously just assuming droplet transmission is occurring. The same standards must be required for both claims. We are unlikely to have ‘definitive proof’ of either claim. Our decisions must be made based on the preponderance of the evidence.
There is good evidence that COVID-19 spreads through aerosols
Although there is no “smoking gun”, the evidence that COVID-19 spreads through aerosols is relatively strong. Below I outline the various converging areas of science that convince me that aerosols are a major route of SARS-CoV-2 transmission.
The animal data is not perfect, but suggests aerosol spread. Animal studies definitely show that SARS-COV-2 can be transmitted ‘through the air’, but most of these studies have done an inadequate job of distinguishing between aerosols and droplets. (Richard 2020; Sia 2020)
In the original post, I discussed research in ferrets that pretty definitely showed that influenza can be spread through aerosols. A similar study has now been replicated using both SARS-CoV1 and SARS-CoV-2. Healthy ferrets were placed in a cage that was above infected ferrets (as droplets should not rise against gravity) and the cages were connected with pipes that had a series of 90 degree bends (as droplets should not make the turns). In the SARS-CoV-1 pairings, all 4 healthy ferrets subsequently tested positive. In the SARS-CoV-2 pairings, 2 of the 4 ferrets tested positive. Thus, the infection spread through the air, around corners, and against gravity, which is inconsistent with droplet transmission, but describes aerosol transmission perfectly. However, the set-up is somewhat artificial, as there were high air flow rates between the cages. It would have been more convincing if they were left with relatively stagnant air. (Kutter 2020) (It is amazing to me that for such a controversial and important subject, this experiment has not been replicated.)
In a similar study in mice, SARS-CoV-2 was transmitted through aerosols, but required longer exposures than transmission by close contact. (Bao 2020) As discussed above, long range aerosol transmission should require longer exposure as the total viral exposure per time is lower.
Although there is no perfect study, the animal studies certainly suggest COVID-19 is aerosol spread.
The strongest evidence for aerosol transmission of COVID-19 is probably the epidemiologic data. Everyone knows about “super-spreader” events at this point. These cases are so common that most aren’t subject to scientific reporting. Every week, we hear news reports of gatherings that led to very large numbers of new infections. Although it is essentially impossible to prove the route of transmission during these events, this type of large scale transmission has always been assumed to be airborne in the past, and that certainly makes the most sense.
There are too many examples to cover them all, but let’s review a few. The most famous example is probably the choir practice that occurred in Skagit County, Washington in March 2020. 61 people attended a choir practice on March 10th, one of whom had COVID-19. Of the remaining 60, 52 (87%) subsequently contracted the disease (32 were confirmed by PCR and the rest diagnosed clinically). The chairs in the room were only 6-10 inches apart, but most people were further than a few meters from the index patient for most, if not all, of the night. COVID-19 was already a known entity at the time, so some precautions were in place (mostly in keeping with droplet/contact spread). There was no reported physical contact between any of the attendees and most attendees left immediately after the practice. Although the exact mechanism of transmission cannot be confirmed, the incredibly high attack rate simply doesn’t make sense with contact or droplet spread, and the pattern looks exactly like other airborne diseases. (Hamner 2020; Jimenez 2020)
A similar case occurred after an asymptomatic individual took a 50 minute bus ride to and from a religious ceremony, and then developed cough, fever, and chills the evening after the event. Of the 68 individuals on the bus, 24 (35%) were diagnosed with COVID-19. The passengers didn’t change seats or move during the ride, and the infections were relatively evenly spread throughout the bus – a pattern more consistent with airborne spread than droplet. A second bus to the same event acted as a ‘control’ and no passengers were diagnosed with COVID-19. The authors conclude that this event provides “very strong evidence of aerosol transmission”. (Shen 2020)
An outbreak in an office building in Korea paints a similar picture. On March 9, they identified a cluster of cases from the building and closed it down. Testing was offered to everyone, and 1,143 (99.8%) accepted. The pattern of exposure again seems to suggest aerosol spread. The outbreak was centered on the 11th floor. Of individuals from other floors who would have been exposed to droplet/contact spread in the lobby and elevators, 3 individuals (0.3%) tested positive for COVID-19. On the 11th floor, 94 individuals (44%) tested positive. The 11th floor is divided in half, but with shared bathrooms, elevators, and lobby. The vast majority of positives were from half of the floor, but on that side the positives are equally distributed, in a pattern more suggestive of aerosol spread than droplet spread, although we don’t know exactly how individuals interacted. The ventilation of the building is not described. (Park 2020)
I find these epidemiologic reports incredibly enlightening. They are clearly indirect evidence. They rely on numerous assumptions. However, on a whole, they seem to provide relatively strong support for the concept that COVID-19 is transmitted through aerosols. There are many more reports of super-spreader outbreaks than I can cover, but they all suggest the same thing: aerosols transmission of COVID-19. (Cai 2020, Li 2020, Almilaji 2020; Bays 2020; Günther 2020; Wallace 2020; Charlotte 2020)
The superspreaders highlight an important issue with COVID-19: the risk of transmission is not evenly distributed. Many infected individuals will not spread the disease at all. One modelling study estimated that 10% of patients are responsible for 80% of disease transmission. (Endo 2020) Another study suggests that 8% of infected individuals are responsible for 60% of secondary cases, while 70% of infected people don’t pass the disease on to anyone else. (Laxminarayan 2020) Another epidemiologic study from Hong Kong reached similar conclusions: 19% of people were responsible for 80% of transmission. (Adam 2020)
The uneven distribution of disease transmission is why simply comparing the Ro among diseases can be misleading, and why many people have heard of “k” or the dispersion factor as a second essential concept. (Kupferschmidt 2020) If instead of looking at population averages, you focus on the smaller number of individuals who are spreading the disease widely, COVID-19 starts to look a lot more like a classic airborne disease.
As I discussed above, the infectivity and mode of transmission are different concepts. The number of people being infected does not prove the mechanism of transmission. However, these super-spreader events are very difficult to explain based on droplet transmission, but easy to explain based on aerosols.
The transmission pattern of COVID-19 may be the strongest indication that aerosols play a significant role in the spread of disease.
Ventilation as a risk factor
Poor ventilation is widely accepted as a risk factor for COVID-19. That being said, with the exception of a few case reports, I haven’t found any studies specifically linking ventilation to the spread of SARS-CoV-2.
Ventilation is a known risk factor for many similar viruses. Inadequate ventilation was identified as a risk factor for the transmission of SARS. (Li 2005) A systematic review found that there is “strong and sufficient evidence to demonstrate the association between ventilation, air movements in buildings and the transmission/spread of infectious diseases such as measles, tuberculosis, chickenpox, influenza, smallpox and SARS.” (Li 2007) Poor ventilation in college dorms has also been associated with increases in seasonal acute respiratory illnesses. (Zhu 2020)
By definition, droplets fall rapidly to the ground and therefore are basically unaffected by ventilation. If ventilation impacts disease transmission, it is strong evidence that the disease is spread by aerosols, as aerosols are the only vector significantly altered by ventilation. This simple fact seems to be overlooked by many governing bodies, resulting in conflicting recommendations. For example, the WHO states that COVID-19 is only spread through droplets but simultaneously emphasizes the need for ventilation in the control of the disease. That doesn’t make sense.
Ventilation is important in the spread of SARS-CoV-1. Ventilation is important in the spread of seasonal respiratory illnesses, which include numerous other coronaviruses. Ventilation really only impacts aerosols, and so this is strong evidence that aerosol transmission is important in the spread of these diseases. We have no reason to believe that the transmission of SARS-CoV-2 is different from these other coronaviruses, so although the evidence is indirect, it again suggests that COVID-19 is transmitted through aerosols.
Indoors versus outdoors
The spread of COVID-19 is more likely in indoors settings. In a review of 318 COVID-19 outbreaks in China, all 318 occurred in an indoor setting. (Qian 2020) A similar study from Japan looked at 110 cases among 11 clusters, and the odds of transmission in an indoor setting was 19 times higher than in an outdoor setting, and the odds of a super-spreader even was 33 times higher indoors than outdoors. (Nishiura 2020) (This ratio will be partly explained by the fact that large gatherings are more likely to occur in indoor settings. It would be interesting to see a study adjust for this fact.)
The preponderance of indoor spread cannot be easily explained if transmission is occurring through droplets. Droplets fall to the ground rapidly, and therefore are mostly unaffected by dilution and breezes in the outdoor setting. The rapid fall of droplets does not provide sufficient time for ultraviolet light to inactivate the virus. When someone sneezes next to you, the chance of a droplet contacting your mucous membranes is unchanged whether you are inside or out. Droplets should be equally infectious indoors and out. In fact, droplets should probably be more infectious outdoors, because masks are more frequently worn inside than out. The fact that COVID-19 transmission occurs so much more frequently in indoor settings is further evidence of the importance of aerosols.
Sadly, the one type of research we need most is also the type of research that is most lacking. (Perhaps limited by the stubborn insistence from some circles that COVID-19 is only spread through droplets). How do infection rates vary with different forms of PPE? Unfortunately, as far as I can tell, no one has done studies directly comparing hospitals or countries that are routinely practicing under airborne precautions to those that are not. However, as I previously discussed, there is lots of evidence that healthcare workers are contracting COVID-19 far more often than they should be. There was also some evidence that suggests much lower rates of healthcare worker infections in hospitals that are routinely using N95s or PAPRs. (Koh 2020; Liu 2020) If this holds true, it is yet another line of evidence that COVID-19 spreads through aerosols.
This is not a topic I have seen widely discussed, but droplet production is strongly associated with symptoms (coughing and sneezing). Asymptomatic individuals produce far fewer droplets. The fact that asymptomatic spread is clearly playing an important role in COVID-19 is another line of evidence that suggests aerosols are an important mechanism of transmission.
As I reviewed in the initial post, we have known from very early on that SARS-CoV-2 can be found in airborne samples, can survive in aerosols, and can be found in places like air ducts that can’t be reached by droplets. (Guo 2020, Santarpia 2020b, Ong 2020, Liu 2020; Van Doremalen 2020; Fears 2020) Furthermore, some studies have specifically identified viable virus in the air more than 2 meters from the patient. (Lednicky 2020) This data is weak, but parallels all the other lines of evidence that together make it very clear that aerosols are involved in the transmission of COVID-19.
When are aerosols formed?
“Aerosol generating procedures” have probably received far too much attention. As I covered in the original aerosol post, aerosols are generated by talking, and are produced in much larger quantities when patients are coughing, have high minute ventilations, or airway collapse. (Tellier 2009; Asadi 2019; Morawska 2006; Fiegel 2006; Wilson 2020) A study measuring aerosol generation while talking concludes that “there is a substantial probability that normal speaking causes airborne virus transmission in confined environments.” (Stadnytskyi 2020) Another study found viable SARS-CoV-2 in the air more than 2 meters from patients in hospital rooms, again leading the authors to conclude that “patients with respiratory manifestations of COVID-19 produce aerosols in the absence of aerosol-generating procedures that contain viable SARS-CoV-2, and these aerosols may serve as a source of transmission of the virus”. (Lednicky 2020) Intubation is one of the highest risk procedures we perform, but a single cough produces as many as 500 times more aerosols than the act of intubation. (Brown 2020)
Aerosols are constantly present. The focus on only a handful of procedures is a dangerous distraction. Inserting a urinary catheter was associated with an increased risk of contracting SARS (RR 5.00 95% CI 2.44-1.023). (Loeb 2004) Being present during an ECG (OR 3.52) and inserting a peripheral IV (RR 3.24) were also associated with an increased rate of transmission of SARS. (Loeb 2004; Raboud 2010) None of these activities are “aerosol generating” but all were found to be high risk.
When combined with the fact that healthcare workers are contracting COVID at a much higher rate than the general population, this data tells us that we need to change our approach. Choosing PPE based on procedures doesn’t seem to be well supported by science. We need to acknowledge the importance of aerosols in all patients, and be particularly wary of coughing and respiratory distress.
Management of aerosols
Hopefully everyone is convinced that we need to take aerosols seriously. I cannot cover every aspect of the science of aerosol management. There are already many experts publishing extensively on the topic, and I think we should just listen to them. (For example, read anything by Jose-Luis Jimenez or Shelly Miller, among many others.) However, the news that COVID-19 is spread through aerosols seems to provoke such pessimistic reactions that I want to briefly cover what it means for management.
First of all, the fact that COVID-19 is aerosol spread makes me very optimistic. Looking at the state of the world in November 2020, it is pretty clear that we are failing in our attempts to manage this disease. If we were already doing everything in our power to fight this pandemic, it would be incredibly depressing. However, the fact that we have been completely ignoring the important role that aerosols are playing in the spread of this disease means that we have an opportunity to improve. That is excellent news.
Thankfully, there are a lot of basic, low cost interventions that anyone can implement, even if major medical institutions choose to ignore this science. Avoid crowded places. Avoid close proximity to others. Avoid poorly ventilated environments. When meeting with others, do it outdoors as much as possible. If you need to be indoors or in close contact with others, do so for as short as possible. Wear a mask when indoors (including vehicles and other enclosed spaces) and avoid misguided souls who aren’t wearing masks. Refrain from activities that significantly increase aerosols production, such as singing, loud talking, or heavy breathing (exercise) in indoor environments. If you have to be in an enclosed space with someone (such as in a car), open the windows to increase ventilation.
The current suggestions, such as physical distancing and mask wearing are good, but they aren’t enough. They remain necessary, but aren’t sufficient. The fact that SARS-CoV-2 is aerosol spread shouldn’t stop any of our current efforts. Instead, we should be looking at the extra precautions we can add to stem the spread of this disease.
Ventilation and filtration
Most “super-spreader” or large transmission events have occurred in indoor settings. The simple public health measure of reducing large indoor gatherings is essential in combating COVID-19. However, the shutdown of indoor venues has had a significant impact on many people’s lives. We need to open businesses, but we need to do so safely. Similarly, those of us working in healthcare who are confined indoors with sick COVID patients also need to be kept safe. A focus on ventilation is essential.
I will not pretend to be an expert on ventilation. There are many aspects to consider, but the most basic is ensuring adequate air exchanges, so that contaminated air is sufficiently replaced with fresh air. The CDC recommends 6-12 air changes per hour and a minimum of 12 is generally required for hospital negative pressure rooms. (CDC 2019; Li 2007) However, the efficacy of ventilation is dependent on the number of people in the room. A better metric may be liters exchanged per second per person (L/p/s) – which measures the same airflow, but adjusts for the number of people in the space (and therefore the total number of aerosols being produced). Recommendations target at least 10 L/s/p, but ideally 20-25 L/s/p to prevent aerosol spread of COVID-19. (REHVA 2020)
One problem is that ventilation is difficult for the average person to assess. If my local barbeque joint is full of conspiracy theorists who refuse to wear masks, the decision is easy to shop somewhere else. However, how am I supposed to know whether a restaurant has adequate ventilation? One interesting proposal is to use carbon dioxide levels as a surrogate measure of adequate ventilation. The concept is well described in this article. There are cheap (approximately $150) CO2 monitors that could give us a real time indication of ventilation. The ambient concentration of carbon dioxide is about 410 parts per million. A concentration above approximately 800 that is an indication that you are rebreathing exhaled air and therefore other people’s aerosols. (Rudnik 2003) It is not a perfect surrogate. Filtration could effectively remove all aerosols, but leave the CO2 level unchanged. However, it is a reasonable concept that could potentially increase the safety of indoor dining dramatically. (To be clear, although this is a promising theory, there is no evidence that these monitors actually decrease transmission, but they might be worth trying. The potential return on investment is massive.)
Air filtration also makes sense. I have seen many claims that suggest that the excellent filtration in modern aircraft is the primary reason we have seen so few outbreaks on airplanes. I have not reviewed the evidence on filtration specifically, but again there are many experts to guide us if we are willing to accept aerosol spread and ask for their help.
If you want more information, there are some very in depth reviews on ventilation, filtration, and indoor air flow patterns that can get you started. (Lipinski 2020; Jayaweera 2020)
Upper room UV light
Germicidal ultraviolet light is another interesting topic on which I have barely scratched the surface. Using a tuberculosis model and animal testing, upper room UV light was show to decrease the rate of infection by approximately 80% in a simulated hospital setting. (Mphaphlele 2015) Laboratory studies have indicated that UV light is effective at inactivating both SARS and influenza, so it should theoretically work against COVID-19 as well. (Darnell 2004; McDevitt 2012) Interestingly, high intensity ultraviolet light has been suggested to manage measles outbreaks as far back as 1978. (Riley 1978) There is also a CDC/NIOSH guideline on ultraviolet germicidal irradiation for the management of tuberculosis in healthcare settings. I do not yet know the science well enough to know where and when UV light should be implemented, but once we accept that evidence that aerosols are important in the spread of COVID-19, it is another potential tool at our disposal.
The role of masks in reducing the transmission of COVID-19 is a massive topic that will need its own blog post in the future. However, the acknowledgement of aerosol transmission of COVID-19 does necessitate at least a few comments about the role of masks.
Although it is true that N95s filter more aerosols than surgical masks, it is a misconception that surgical masks are useless against aerosols. A well fitting surgical mask will filter the majority of the larger (>1 micron) aerosols that are thought to be transmitting COVID-19. (Jimenez 2020; Shakya 2017; Makison Booth 2013) In one study of live patients with acute respiratory illnesses, surgical masks were shown to block 100% of seasonal coronavirus droplets and aerosols, although the efficacy was lower for other viruses. (Leung 2020)
Surgical masks are not 100% effective, but that doesn’t make them ineffective. Remember, the concentration of aerosols drops dramatically with distance. When combined with decent ventilation and the relatively low infectivity of SARS-CoV-2, an 80% effective surgical mask may be enough for most situations (and is certainly better than no mask).
Of course, the fact that COVID-19 is aerosol spread means that N95s are going to be important in high risk scenarios, especially in health care. It still isn’t clear exactly when N95s are needed, but the rate of infections in healthcare workers indicates that we probably should be using them more often than we currently are.
Unfortunately, the N95 is a limited resource. In an ideal world, we would use N95s for all patients with suspected COVID-19. That was our approach to SARS and MERS. Unfortunately, the world in 2020 is not ideal, and the supply of PPE is not endless. The appropriate response to this problem is to acknowledge that COVID-19 is aerosol spread and ensure that healthcare workers have appropriate PPE. That should be an absolute top priority for all hospitals and all levels of government. However, in the meantime, we have to decide what to do with our limited supply.
There are no perfect answers. In many places, people are wearing the same N95 for entire shifts, day after day. Many places are reusing or reprocessing N95s that are designed to be disposable. The evidence that this is safe is scant, at best.
I think the science of aerosols can guide us. All patients are producing aerosols, so we need to abandon the outdated ‘aerosol generating procedure’ paradigm. However, we must also acknowledge that, although healthcare workers are getting sick far more than they should be, the absolute rate is still low. By now, we have all been exposed to SARS-CoV-2 while not wearing an N95, but very few of us actually contracted the virus. The infectivity of SARS-CoV-2 is relatively low. Surgical masks, although imperfect, are still pretty good. Hospitals generally have excellent ventilation. Brief patient encounters keep our total aerosol exposure low, and when we are in patient rooms, a small amount of physical distancing significantly decreases aerosol exposure.
These factors combine to mean that, for the average patient, a surgical mask and “droplet precautions” may be adequate. It will not be perfect. The occasional healthcare worker will still get sick, but the rate will be very low. Although I don’t think any healthcare worker should get sick at work, this small risk is probably much better than the risk we would face after running out of N95s.
So how should we decide when to wear an N95? The aerosol generating procedure paradigm doesn’t work. Procedures don’t produce aerosols, patients do. However, the factors discussed above provide a framework that can guide our decisions. Aerosols are most concentrated close to the patient. Coughing patients and those in respiratory distress produce far more aerosols. Total exposure is correlated with time.
Therefore, if I have a patient in respiratory distress, and I have to spend a long time in close contact with the patient (such as while placing a central line), I will definitely wear full airborne PPE, whether or not there is technically an ‘aerosol generating procedure’ occurring. However, for a 3 minute assessment of a patient with mild coryza, most of which I can do from across the room, the risk is low enough that I will wear droplet precautions and preserve those precious N95s for when I truly need them.
Putting it together
Almost everyone now admits that aerosols play a role in the transmission of SARS-CoV-2, even in the absence of aerosol generating procedures. However, many still debate or downplay the magnitude of aerosol transmission. Based on this extensive review of the literature, I think it is very clear that aerosols play a considerable role in the transmission of COVID-19, and that we are unlikely to prevail against this pandemic unless we acknowledge that fact.
The arguments against aerosol transmission are logically fallacious and conflict with available science. The Ro of a disease does not define its mechanism of transmission, but even if it did, the Ro of COVID-19 is very similar to that of the prototypical airborne disease of tuberculosis. Aerosol transmission is much more likely to occur over short distances, but even if aerosol transmission was defined by long distance spread, there are countless super-spread events that seem to fit the mold.
Many lines of research all support the important role of aerosols in the transmission of COVID-19. There is animal data that strongly suggests airborne spread. The epidemiology of super-spreaders is explained far better by aerosol than droplet transmission. The role of ventilation in preventing disease transmission suggests aerosols. The fact that infections predominantly occur indoors suggests aerosol spread. Presymptomatic transmission suggests aerosols. The preponderance of the evidence is clearly on the side of aerosol transmission.
In contrast, there is almost no evidence for droplet transmission. That claim has not been based on science. It is based on opinion and historical medical momentum. The conversation about aerosols and droplets has been rather biased from the outset. Many refuse to acknowledge the possibility of aerosol transmission unless there is definitive proof, but simultaneously accept droplet transmission, which has even less evidence than aerosols.
This table from Jose-Luis Jimenez provides a nice summary of the many types of evidence, and demonstrates that the evidence for aerosol spread is far stronger than the evidence for any other type of transmission.
We are repeating old mistakes, but with worse consequences. In conversations about COVID-19, measles is held up as the prototypical example of an airborne illness. Ironically, we had this same debate about measles, and tuberculosis before that. This article about measles from 1985 states that “most public health authorities believe that the primary mode of transmission is by large respiratory droplets which remain suspended in air for short time intervals. Successful transmission in this manner requires close contact between susceptible individuals and a source patient, usually within 1 m (3 ft).” (Bloch 1985) Sound familiar? The evidence for this claim was essentially identical to the evidence currently being used to claim that COVID-19 is only spread through droplets.
We can no longer keep our heads in the sand. The evidence is clear. Aerosols play a significant role in the transmission of COVID-19.
I think this is a good development. Currently, we are losing the battle. However, the fact that we have been ignoring the science around aerosols means that we have a path forward. If we start to manage aerosol transmission appropriately, there is a chance we can get this pandemic under control.
The basic steps forward are simple. We need to continue following the current recommendations about physical distancing, hand washing, and masks. In addition, we need to be cognizant of the factors that drive aerosol spread: crowds and long times spent in poorly ventilated environments. We need to acknowledge the limitations of the current approach. There is no such thing as a ‘2 meter rule’ – the farther apart the better. We will need to improve our indoor spaces, with a focus on ventilation, filtration, and potentially ultraviolet light decontamination systems.
These are still relatively blunt tools. A key aspect of disease transmission in COVID-19 is the existence of super-spreaders. The majority of secondary cases arise from a relatively small number of individuals. This is clearly a feature of aerosol spread, and our focus on droplets and contact have left us blind to the root causes of this phenomenon. We understand some of the basics (varying viral load, varying aerosol emission, and circumstances that increase aerosol exposure), but too much is still unknown. We need effective interventions to stop these super-spreader outbreaks, and the path to those interventions lies with accepting that aerosol spread is important in the transmission of COVID-19.
Addressing this problem in healthcare settings will be more difficult. We should aim for an adequate supply of PPE, so that all encounters with patients suspected of COVID-19 can be performed with appropriate aerosols precautions. In the meantime, we will have to think carefully about the factors that increase risk. We need to abandon the ‘aerosol generating procedure’ paradigm, as all COVID-19 patients produce aerosols. We need to focus on patients with respiratory complaints, and prioritise providers that need to spend prolonged periods at the bedside.
Aerosol transmission plays a very important role in the spread of COVID-19. It is essential that we acknowledge the science on this issue if we are going to have any success against this pandemic.
The idea that COVID-19 is spread by aerosols is not a fringe position I made up while wearing a tinfoil hat. Here are some other reviews on the topic you can read.
Fennelly KP. Particle sizes of infectious aerosols: implications for infection control. Lancet Respir Med. 2020 Sep;8(9):914-924. doi: 10.1016/S2213-2600(20)30323-4. Epub 2020 Jul 24. PMID: 32717211 [free full text]
- “The studies reviewed in this paper consistently show that humans produce infectious aerosols in a wide range of particle sizes”
- “Data are accumulating that severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the virus that causes COVID-19, is transmitted by both small and large particle aerosols”
- “These data suggest that health-care workers should be protected from these potentially infectious aerosols when working in close proximity to patients.”
- An open letter to the WHO from 239 scientists
- “Studies by the signatories and other scientists have demonstrated beyond any reasonable doubt that viruses are released during exhalation, talking, and coughing in microdroplets small enough to remain aloft in air and pose a risk of exposure at distances beyond 1–2 m from an infected individual”
- “We are concerned that the lack of recognition of the risk of airborne transmission of COVID-19 and the lack of clear recommendations on the control measures against the airborne virus will have significant consequences”
Prather KA, Wang CC, Schooley RT. Reducing transmission of SARS-CoV-2 Science. 2020; 368(6498):1422-1424. [free full text]
- “A large proportion of the spread of coronavirus disease 2019 (COVID-19) appears to be occurring through airborne transmission of aerosols produced by asymptomatic individuals during breathing and speaking.”
- “Aerosol transmission of viruses must be acknowledged as a key factor leading to the spread of infectious respiratory diseases. Evidence suggests that SARS-CoV-2 is silently spreading in aerosols exhaled by highly contagious infected individuals with no symptoms.”
Public Health Agency of Canada Evidence Brief
- “The available empirical and modeled evidence indicates there is some risk of SARS-CoV-2 virus laden aerosol and droplet dispersion at distances beyond two meters, while epidemiological evidence implicates airborne transmission of SARS-CoV-2 to have occurred in some indoor settings”
If you think there is good scientific evidence for droplet transmission, important studies that I have missed, or any problems with this article, please comment below. The goal of performing an extensive review of the literature is to find the answer that is most likely to be true. I don’t care whether COVID-19 is droplet or aerosol spread. I care that we use the best available science to guide our actions, and will happily adjust as new data becomes available.
Adam DC, Wu P, Wong JY, et al. Clustering and superspreading potential of SARS-CoV-2 infections in Hong Kong Nat Med. 2020; 26(11):1714-1719.
Almilaji O, Thomas P. Air recirculation role in the infection with COVID-19, lessons learned from Diamond Princess cruise ship. medRxiv 2020;2020.07.08.20148775.
Asadi S, Wexler AS, Cappa CD, Barreda S, Bouvier NM, Ristenpart WD. Aerosol emission and superemission during human speech increase with voice loudness. Sci Rep. 2019;9(1):2348. Published 2019 Feb 20. doi:10.1038/s41598-019-38808-z PMID: 30787335
Bao L, Gao H, Deng W, Lv Q, Yu H, Liu M, Yu P, Liu J, Qu Y, Gong S, Lin K, Qi F, Xu Y, Li F, Xiao C, Xue J, Song Z, Xiang Z, Wang G, Wang S, Liu X, Zhao W, Han Y, Wei Q, Qin C. 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 Jul 23;222(4):551-555. doi: 10.1093/infdis/jiaa281. PMID: 32444876
Bays DJ, Nguyen MH, Cohen SH, Waldman S, Martin CS, Thompson GR, Sandrock C, Tourtellotte J, Pugashetti JV, Phan C, Nguyen HH, Warner GY, Penn BH. Investigation of Nosocomial SARS-CoV-2 Transmission from Two Patients to Health Care Workers Identifies Close Contact but not Airborne Transmission Events. Infect Control Hosp Epidemiol. 2020 Jul 3:1-22. doi: 10.1017/ice.2020.321. Epub ahead of print. PMID: 32618530
Bloch AB, Orenstein WA, Ewing WM, Spain WH, Mallison GF, Herrmann KL, Hinman AR. Measles outbreak in a pediatric practice: airborne transmission in an office setting. Pediatrics. 1985 Apr;75(4):676-83. PMID: 3982900
Brown J, Gregson FKA, Shrimpton A, Cook TM, Bzdek BR, Reid JP, Pickering AE. A quantitative evaluation of aerosol generation during tracheal intubation and extubation. Anaesthesia. 2020 Oct 6:10.1111/anae.15292. doi: 10.1111/anae.15292. Epub ahead of print. PMID: 33022093
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 Jun;26(6):1343-1345. doi: 10.3201/eid2606.200412. Epub 2020 Jun 17. PMID: 32163030
CDC 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.https://espanol.cdc.gov/infectioncontrol/pdf/guidelines/environmentalguidelines-P.pdf
Charlotte N. High Rate of SARS-CoV-2 Transmission due to Choir Practice in France at the Beginning of the COVID-19 Pandemic [Internet]. Epidemiology; 2020. Available from: http://medrxiv.org/lookup/doi/10.1101/2020.07.19.20145326
Chen W, Zhang N, Wei J, Yen H, Li Y. Short-range airborne route dominates exposure of respiratory infection during close contact Building and Environment. 2020; 176:106859-.
Darnell ME, Subbarao K, Feinstone SM, Taylor DR. Inactivation of the coronavirus that induces severe acute respiratory syndrome, SARS-CoV Journal of Virological Methods. 2004; 121(1):85-91.
Guo ZD, Wang ZY, Zhang SF, et al. Aerosol and Surface Distribution of Severe Acute Respiratory Syndrome Coronavirus 2 in Hospital Wards, Wuhan, China, 2020 [published online ahead of print, 2020 Apr 10]. Emerg Infect Dis. 2020;26(7):10.3201/eid2607.200885. doi:10.3201/eid2607.200885 PMID: 32275497
Endo A; Centre for the Mathematical Modelling of Infectious Diseases COVID-19 Working Group, Abbott S, Kucharski AJ, Funk S. Estimating the overdispersion in COVID-19 transmission using outbreak sizes outside China. Wellcome Open Res. 2020 Jul 10;5:67. doi: 10.12688/wellcomeopenres.15842.3. PMID: 32685698; PMCID: PMC7338915.
Fears SC, Klimstra WB, Duprex P, Hartman A, Weaver SC, Plante KS, et al. Persistence of severe acute respiratory syndrome coronavirus 2 in aerosol suspensions. Emerg Infect Dis. 2020 Sep. https://doi.org/10.3201/eid2609.201806
Fiegel J, Clarke R, Edwards DA. Airborne infectious disease and the suppression of pulmonary bioaerosols. Drug Discov Today. 2006;11(1-2):51–57. doi:10.1016/S1359-6446(05)03687-1 PMID: 16478691
Guenther, Thomas and Czech-Sioli, Manja and Indenbirken, Daniela and Robitailles, Alexis and Tenhaken, Peter and Exner, Martin and Ottinger, Matthias and Fischer, Nicole and Grundhoff, Adam and Brinkmann, Melanie, Investigation of a superspreading event preceding the largest meat processing plant-related SARS-Coronavirus 2 outbreak in Germany (July 17, 2020). Available at SSRN: https://ssrn.com/abstract=3654517 or http://dx.doi.org/10.2139/ssrn.3654517
Hamner L, Dubbel P, Capron I, et al. High SARS-CoV-2 Attack Rate Following Exposure at a Choir Practice — Skagit County, Washington, March 2020. MMWR Morb Mortal Wkly Rep 2020;69:606–610. DOI: http://dx.doi.org/10.15585/mmwr.mm6919e6
Jayaweera M, Perera H, Gunawardana B, Manatunge J. Transmission of COVID-19 virus by droplets and aerosols: A critical review on the unresolved dichotomy. Environ Res. 2020 Sep;188:109819. doi: 10.1016/j.envres.2020.109819. Epub 2020 Jun 13. PMID: 32569870
Jimenez JL. COVID-19 Data Dives: Why Arguments Against SARS-CoV-2 Aerosol Transmission Don’t Hold Water – Medscape – Jul 30, 2020. Available at: https://www.medscape.com/viewarticle/934837?src=uc_mscpedt&faf=1#vp_1
Koh FH, Tan MG, Chew MH. The fight against COVID-19: disinfection protocol and turning over of CleanSpace® HALO™ in a Singapore Hospital. Updates Surg. 2020 Jun;72(2):311-313. doi: 10.1007/s13304-020-00809-3. Epub 2020 May 27. PMID: 32462609
Kupferschmidt K. Why do some COVID-19 patients infect many others, whereas most don’t spread the virus at all? Science. 2020; [article]
Kutter JS, de Meulder D, Bestebroer TM, et al. SARS-CoV and SARS-CoV-2 are transmitted through the air between ferrets over more than one meter distance. bioRxiv 2020;2020.10.19.345363. Preprint: https://www.biorxiv.org/content/10.1101/2020.10.19.345363v1.article-metrics
Laxminarayan R, Wahl B, Dudala SR, et al. Epidemiology and transmission dynamics of COVID-19 in two Indian states. Science 2020;eabd7672.
Lednicky JA, Lauzardo M, Fan ZH, Jutla A, Tilly TB, Gangwar M, Usmani M, Shankar SN, Mohamed K, Eiguren-Fernandez A, Stephenson CJ, Alam M, Elbadry MA, Loeb JC, Subramaniam K, Waltzek TB, Cherabuddi K, Morris JG Jr, Wu CY. Viable SARS-CoV-2 in the air of a hospital room with COVID-19 patients. medRxiv [Preprint]. 2020 Aug 4:2020.08.03.20167395. doi: 10.1101/2020.08.03.20167395. Update in: Int J Infect Dis. 2020 Sep 16;: PMID: 32793914
Leung NHL, Chu DKW, Shiu EYC, Chan KH, McDevitt JJ, Hau BJP, Yen HL, Li Y, Ip DKM, Peiris JSM, Seto WH, Leung GM, Milton DK, Cowling BJ. Respiratory virus shedding in exhaled breath and efficacy of face masks. Nat Med. 2020 May;26(5):676-680. doi: 10.1038/s41591-020-0843-2. Epub 2020 Apr 3. Erratum in: Nat Med. 2020 May 27;: PMID: 32371934
Li Y, Huang X, Yu IT, Wong TW, Qian H. Role of air distribution in SARS transmission during the largest nosocomial outbreak in Hong Kong. Indoor Air. 2005 Apr;15(2):83-95. doi: 10.1111/j.1600-0668.2004.00317.x. PMID: 15737151
Li Y, Leung GM, Tang JW, Yang X, Chao CY, Lin JZ, Lu JW, Nielsen PV, Niu J, Qian H, Sleigh AC, Su HJ, Sundell J, Wong TW, Yuen PL. Role of ventilation in airborne transmission of infectious agents in the built environment – a multidisciplinary systematic review. Indoor Air. 2007 Feb;17(1):2-18. doi: 10.1111/j.1600-0668.2006.00445.x. PMID: 17257148
Li Y, Qian H, Hang J, et al. Evidence for probable aerosol transmission of SARS-CoV-2 in a poorly ventilated restaurant. medRxiv 2020;2020.04.16.20067728.
Lipinski T, Ahmad D, Serey N, Jouhara H. Review of ventilation strategies to reduce the risk of disease transmission in high occupancy buildings International Journal of Thermofluids. 2020; 7-8:100045-.
Liu M, Cheng SZ, Xu KW, Yang Y, Zhu QT, Zhang H, Yang DY, Cheng SY, Xiao H, Wang JW, Yao HR, Cong YT, Zhou YQ, Peng S, Kuang M, Hou FF, Cheng KK, Xiao HP. Use of personal protective equipment against coronavirus disease 2019 by healthcare professionals in Wuhan, China: cross sectional study. BMJ. 2020 Jun 10;369:m2195. doi: 10.1136/bmj.m2195. PMID: 32522737
Liu Y, Yu ZN, et al. Aerodynamic Characteristics and RNA Concentration of SARS-CoV-2 Aerosol in Wuhan Hospitals during COVID-19 Outbreak. 2020. Preprint, not peer reviewed, here.
Loeb M, McGeer A, Henry B, et al. SARS among critical care nurses, Toronto. Emerg Infect Dis. 2004;10(2):251–255. doi:10.3201/eid1002.030838 PMID: 15030692
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 Sep;146(12):1478-1494. doi: 10.1017/S0950268818001760. Epub 2018 Jul 4. PMID: 29970199
Makison Booth C, Clayton M, Crook B, Gawn JM. Effectiveness of surgical masks against influenza bioaerosols. J Hosp Infect. 2013 May;84(1):22-6. doi: 10.1016/j.jhin.2013.02.007. Epub 2013 Mar 14. PMID: 23498357
McDevitt JJ, Rudnick SN, Radonovich LJ. Aerosol Susceptibility of Influenza Virus to UV-C Light Appl. Environ. Microbiol.. 2012; 78(6):1666-1669.
Morawska L. Droplet fate in indoor environments, or can we prevent the spread of infection?. Indoor Air. 2006;16(5):335–347. doi:10.1111/j.1600-0668.2006.00432.x PMID: 16948710
Mphaphlele M, Dharmadhikari AS, Jensen PA, Rudnick SN, van Reenen TH, Pagano MA, Leuschner W, Sears TA, Milonova SP, van der Walt M, Stoltz AC, Weyer K, Nardell EA. Institutional Tuberculosis Transmission. Controlled Trial of Upper Room Ultraviolet Air Disinfection: A Basis for New Dosing Guidelines. Am J Respir Crit Care Med. 2015 Aug 15;192(4):477-84. doi: 10.1164/rccm.201501-0060OC. PMID: 25928547
Nielsen, P. V., & Liu, L. (2020). The influence of air distribution on droplet infection and airborne cross infection. Department of Civil Engineering, Aalborg University. DCE Technical Memorandum No. 77 Available at: https://vbn.aau.dk/ws/portalfiles/portal/332256833/The_influence_of_air_distribution_on_droplet_infection_and_airborne_cross_infection.pdf
Nishiura H, Oshitani H, Kobayashi T, et al. Closed environments facilitate secondary transmission of coronavirus disease 2019 (COVID-19) [Internet]. Epidemiology; 2020. Available from: http://medrxiv.org/lookup/doi/10.1101/2020.02.28.20029272
Ong SWX, Tan YK, Chia PY, 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
Prather KA, Wang CC, Schooley RT. Reducing transmission of SARS-CoV-2 Science. 2020; 368(6498):1422-1424. Available here: https://science.sciencemag.org/content/368/6498/1422
Qian H, Miao T, Liu L, Zheng X, Luo D, Li Y. Indoor transmission of SARS-CoV-2. Indoor Air. 2020 Oct 31. doi: 10.1111/ina.12766. Epub ahead of print. PMID: 33131151
Raboud J, Shigayeva A, McGeer A, et al. Risk factors for SARS transmission from patients requiring intubation: a multicentre investigation in Toronto, Canada. PLoS One. 2010;5(5):e10717. Published 2010 May 19. doi:10.1371/journal.pone.0010717 PMID: 20502660
REHVA. REHVA COVID-19 guidance document. How to operate HVAC and other building service systems to prevent the spread of the coronavirus (SARS-CoV-2) disease (COVID-19) in workplaces. November 17, 2020. Available at: https://www.rehva.eu/fileadmin/user_upload/REHVA_COVID-19_guidance_document_V4_23112020_V2.pdf
Richard M, Kok A, de Meulder D, Bestebroer TM, Lamers MM, Okba NMA, Fentener van Vlissingen M, Rockx B, Haagmans BL, Koopmans MPG, Fouchier RAM, Herfst S.
Riley EC, Murphy G, Riley RL. Airborne spread of measles in a suburban elementary school. Am J Epidemiol. 1978 May;107(5):421-32. doi: 10.1093/oxfordjournals.aje.a112560. PMID: 665658.
SARS-CoV-2 is transmitted via contact and via the air between ferrets. Nat Commun. 2020 Jul 8;11(1):3496. doi: 10.1038/s41467-020-17367-2. PMID: 32641684
Rudnick SN, Milton DK. Risk of indoor airborne infection transmission estimated from carbon dioxide concentration. Indoor Air. 2003 Sep;13(3):237-45. doi: 10.1034/j.1600-0668.2003.00189.x. PMID: 12950586
Santarpia JL, Herrera VL, Rivera DN, et al. The Infectious Nature of Patient-Generated SARS-CoV-2 Aerosol [Internet]. Infectious Diseases (except HIV/AIDS); 2020. Available from: http://medrxiv.org/lookup/doi/10.1101/2020.07.13.20041632
Santarpia JL, Rivera DN, et al. Transmission Potential of SARS-CoV-2 in Viral Shedding Observed at the University of Nebraska Medical Center. 2020. Preprint here.
Shakya KM, Noyes A, Kallin R, Peltier RE. Evaluating the efficacy of cloth facemasks in reducing particulate matter exposure. J Expo Sci Environ Epidemiol. 2017 May;27(3):352-357. doi: 10.1038/jes.2016.42. Epub 2016 Aug 17. PMID: 27531371.
Shen Y, Li C, Dong H, Wang Z, Martinez L, Sun Z, Handel A, Chen Z, Chen E, Ebell MH, Wang F, Yi B, Wang H, Wang X, Wang A, Chen B, Qi Y, Liang L, Li Y, Ling F, Chen J, Xu G. Community Outbreak Investigation of SARS-CoV-2 Transmission Among Bus Riders in Eastern China. JAMA Intern Med. 2020 Sep 1:e205225. doi: 10.1001/jamainternmed.2020.5225. Epub ahead of print. PMID: 32870239
Sia SF, Yan LM, Chin AWH, Fung K, Choy KT, Wong AYL, Kaewpreedee P, Perera RAPM, Poon LLM, Nicholls JM, Peiris M, Yen HL. Pathogenesis and transmission of SARS-CoV-2 in golden hamsters. Nature. 2020 Jul;583(7818):834-838. doi: 10.1038/s41586-020-2342-5. Epub 2020 May 14. PMID: 32408338
Stadnytskyi V, Bax CE, Bax A, Anfinrud P. The airborne lifetime of small speech droplets and their potential importance in SARS-CoV-2 transmission. Proc Natl Acad Sci U S A. 2020 Jun 2;117(22):11875-11877. doi: 10.1073/pnas.2006874117. Epub 2020 May 13. PMID: 32404416
Tellier R. Aerosol transmission of influenza A virus: a review of new studies. J R Soc Interface. 2009;6 Suppl 6(Suppl 6):S783–S790. doi:10.1098/rsif.2009.0302.focus PMID: 19773292
Tellier R, Li Y, Cowling BJ, Tang JW. Recognition of aerosol transmission of infectious agents: a commentary. BMC Infect Dis. 2019 Jan 31;19(1):101. doi: 10.1186/s12879-019-3707-y. PMID: 30704406
van Doremalen N, Bushmaker T, Morris DH, Holbrook MG, Gamble A, Williamson BN, Tamin A, Harcourt JL, Thornburg NJ, Gerber SI, Lloyd-Smith JO, de Wit E, Munster VJ. 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. doi: 10.1056/NEJMc2004973. Epub 2020 Mar 17. PMID: 32182409; PMCID: PMC7121658.
Wallace M, Hagan L, Curran KG, et al. COVID-19 in correctional and detention facilities—United States, February–April 2020. MMWR Morb Mortal Wkly Rep 2020; 69: 587–90.
Wei J, Li Y. Airborne spread of infectious agents in the indoor environment. Am J Infect Control. 2016 Sep 2;44(9 Suppl):S102-8. doi: 10.1016/j.ajic.2016.06.003. PMID: 27590694
Yu IT, Xie ZH, Tsoi KK, Chiu YL, Lok SW, Tang XP, Hui DS, Lee N, Li YM, Huang ZT, Liu T, Wong TW, Zhong NS, Sung JJ. Why did outbreaks of severe acute respiratory syndrome occur in some hospital wards but not in others? Clin Infect Dis. 2007 Apr 15;44(8):1017-25. doi: 10.1086/512819. Epub 2007 Mar 9. PMID: 17366443
Zhang R, Li Y, Zhang AL, Wang Y, Molina MJ. Identifying airborne transmission as the dominant route for the spread of COVID-19. Proc Natl Acad Sci U S A. 2020 Jun 30;117(26):14857-14863. doi: 10.1073/pnas.2009637117. Epub 2020 Jun 11. Erratum in: Proc Natl Acad Sci U S A. 2020 Oct 13;117(41):25942-25943. PMID: 32527856
Zhu S, Jenkins S, Addo K, Heidarinejad M, Romo SA, Layne A, Ehizibolo J, Dalgo D, Mattise NW, Hong F, Adenaiye OO, Bueno de Mesquita JP, Albert BJ, Washington-Lewis R, German J, Tai S, Youssefi S, Milton DK, Srebric J. Ventilation and laboratory confirmed acute respiratory infection (ARI) rates in college residence halls in College Park, Maryland. Environ Int. 2020 Apr;137:105537. doi: 10.1016/j.envint.2020.105537. Epub 2020 Feb 3. PMID: 32028176