Airborne Transmission - Once Again!

 

I thought I would take time for a rare celebration on this blog.  Most of my writing is about probabilities and uncertain outcomes. In many cases I am responding to the same tired arguments from people who don’t understand science, biology, medicine or psychiatry. Those positions generally result in some political attacks based on that lack of understanding or some specific political agenda. The position I am referring today is the airborne transmission of viruses. Although it seems like a straightforward scientific issue it has led to as much controversy as any psychiatric topic. Despite a significant amount of literature out there on airborne spread, there has been nothing but resistance to the concept.

Nowhere was the resistance more evident than the advent of the current SARS-CoV-2 pandemic. Initially the message was that the virus was spread by fomites or intermediate size droplets that fall within a few feet following a cough or a sneeze.  Accordingly, social distancing at more than a few feet, decontaminating hands and surfaces were recommended to counter this mechanism of transmission. Many experts claim that most respiratory viruses with very few exceptions are transmitted this way. Those same experts claim that airborne transmission of viruses in smaller droplets travelling much longer distances was controversial at best. All of those conflicting ideas led to recommendations for no masks in February of 2020 followed by recommendations for masks in the next two months.  The mask recommendations occurred in the context of widespread shortages of personal protective equipment (PPE) for health care workers.   

I posted my qualifications on the matter (2 Avian Influenza Task Forces earlier in this century, being subjected to multiple respiratory virus epidemics at work despite rigorous hand washing, and studying the available engineering and viral data, and lengthy discussions with HVAC experts) and began to write about it on this blog.  My perspective is clearly that respiratory viruses are airborne and therefore will not be stopped by handwashing alone, that there are clearly engineering approaches to stop respiratory viruses that will work much better than just handwashing, and that there should be a major research and development effort on environmental designs to minimize and even stop respiratory viruses in homes and public building. In fact, as I type this I have selected a UVC device to be installed in my home HVAC system and it will probably be installed in the next month or two.  Many of those posts on this blog can be found here or by using the search term “airborne” in the search box.

The victory lap today occurs with a press release from the CDC today that I consider a bombshell in terms of the airborne transmission concept.  The press release is a quick read but it highlights why surface contamination is unlikely to be a significant factor:

“Quantitative microbial risk assessment (QMRA) studies have been conducted to understand and characterize the relative risk of SARS-CoV-2 fomite transmission and evaluate the need for and effectiveness of prevention measures to reduce risk. Findings of these studies suggest that the risk of SARS-CoV-2 infection via the fomite transmission route is low, and generally less than 1 in 10,000, which means that each contact with a contaminated surface has less than a 1 in 10,000 chance of causing an infection.”

And further:

“The principal mode by which people are infected with SARS-CoV-2 is through exposure to respiratory droplets carrying infectious virus.”

This information has been slowly presented over the course of the past several months.  For example, Dr. Fauci mentioned on several news outlets that cleaning all of the mail and groceries was not necessary because it was not considered a main route of transmission. A logical inference from that statement is why there is a concern about any surfaces at all unless there is a person with a known infection close by.  And by extension, if surface contamination is not that much of a problem why the concern about accidentally touching your face?  As Dr. Fauci typically states we now have the science behind the transmission and the recommendations can be adapted to the new findings.

The CDC press release does not come right out and say airborne transmission.  They continue to say respiratory droplets are the predominate mode of spread and the old document on respiratory droplets says nothing about differentiating between moderate sized droplets that typically fall to the ground within a 6-foot radius of where they are generated or airborne droplets that are lighter, spread past 6 feet from the generation site and remain suspended for longer periods of time.

Some of the comments on the press release have been much more definitive. The only reference to this post has a good timeline on the airborne controversy and this quote from atmospheric chemist Jose-Luis Jimenez: “If we took half the effort that’s being given to disinfection, and we put it on ventilation, that will be huge.”  In the same reference Germany has invested a half billion dollars in improving ventilation and indoor air quality.

Overall, it appears that the CDC is slowly coming around to the idea that respiratory viruses are transmitted via airborne routes, but some resistance is still evident in the press release they link to an earlier non-descript respiratory droplet transmission document.  There are many potential advantages to fully backing the airborne transmission concept (in addition to the available science).  Research and development is at the top of the list. In an early blogpost, I pointed out that UV decontamination was routine in buildings when I was a kid in a small town in northern Wisconsin.  The currently available UVC is much safer and very effective for killing airborne biological particles. From a clinical trials perspective, deployment of these systems on a large scale and following the number of respiratory infections in facilities with and without the technology seems like a fairly basic experiment.

It is also interesting to consider the resistance. There is undoubtedly politics in science and that can be a factor. There may be a medical intervention bias. In other words, we need some magical intervention like a vaccine, antiviral medication, or general polypharmaceutical modality that can either cure or prevent the excessive morbidity and mortality from respiratory viruses.  The track record there is some wins and many losses.  Every year various populations around the world are subjected to significant effects from flu-like illness that are nowhere as lethal as SARS-CoV-2.  Remarkably – everyone accepts this state of affairs until a more lethal virus comes around and affects a larger group of people.  There is politics as usual leading to irrational attitudes about viruses and physical interventions.  The appropriate environmental interventions may make mask refusers irrelevant at some point in the future.

The bottom line of today’s release is good news for all of the airborne virus crowd and I definitely consider myself in that crowd. I would still like to see the CDC modify their position on transmission in respiratory droplets and I think that is coming.  But most of all, I would like to see us get serious about using environmental measures to limit the exposure and spread of all respiratory viruses including the current one that has killed far more Americans than any influenza epidemic since 1918.

 

George Dawson, MD, DFAPA

 

References:

1:  Lewis D. Why indoor spaces are still prime COVID hotspots. Nature. 2021 Apr;592(7852):22-25. doi: 10.1038/d41586-021-00810-9. PMID: 33785914.

2: Dietrich WL, Bennett JS, Jones BW, Hosni MH. Laboratory Modeling of SARS-CoV-2 Exposure Reduction Through Physically Distanced Seating in Aircraft Cabins Using Bacteriophage Aerosol — November 2020. MMWR Morb Mortal Wkly Rep. ePub: 14 April 2021. DOI: http://dx.doi.org/10.15585/mmwr.mm7016e1

3: Greenhalgh T, Jimenez JL, Prather KA, Tufekci Z, Fisman D, Schooley R. Ten scientific reasons in support of airborne transmission of SARS-CoV-2.  The Lancet (online).  Published 4/15/2021. https://doi.org/10.1016/S0140-6736(21)00869-2  Current link

4: Tang JW, Bahnfleth WP, Bluyssen PM, Buonanno G, Jimenez JL, Kurnitski J, Li Y, Miller S, Sekhar C, Morawska L, Marr LC, Melikov AK, Nazaroff WW, Nielsen PV, Tellier R, Wargocki P, Dancer SJ. Dismantling myths on the airborne transmission of severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2). J Hosp Infect. 2021 Apr;110:89-96. doi: 10.1016/j.jhin.2020.12.022.  Current Link

Airborne Transmission Denial Dies Hard ........

I started this post as I left a staff meeting today on containing the coronoavirus. We had a similar meeting 2 months ago and at that point I added that there was airborne transmission of the virus.  The only comment I got was a condescending remark about how we don't know much about airborne transmission and we need to wait and see and blah, bah, blah. It was "as if" I did not know what I was talking about or any of the surrounding controversy.  To my surprise the same people today were sold on airborne transmission. They were even interested in HVAC issues and negative pressure rooms – all of the stuff I have been studying for 20 years.  Nobody mentioned UVC or air filtration.  I decided just to keep my mouth shut. Just like I usually do when politics seems to be the priority rather than science.  But the good news was undeniable.  Airborne transmission has much greater acceptance than it did prior to the current pandemic and there are clear reasons for it.

That staff meeting is a small part of a larger landscape of what airborne transmission advocates like me have been talking about for decades or longer.  Back in the days when I was working in an outdated building that had an HVAC system that was designed to contain heat rather than provide fresh air to dilute and remove airborne pathogens – I routinely observed the effects of this approach on myself and my coworkers.  Upper respiratory infections were endemic.  If one person came into that building with a severe form of a respiratory virus – most people got it. I can recall coming down with an acute flu-like illness one morning at work and getting ill so quickly and severely that I was barely able to make it home due to the cognitive effects.  I was close to delirium.

When you are in medical facilities, the party line is always “wash your hands”. I got the respiratory infections if I washed my hands 20 times a day or a hundred times a day.  The pandemic equivalent of that advice has been “don’t touch your face”.  But it is apparently safe to eat food that has been contaminated with SARS-CoV-2 because the virus is not infectious via gastrointestinal pathways.  The expert opinion is really based on the lack of evidence that eating food or touching food packaging is associated with SARS-CoV-2 infections.  We hear about the virus being infectious through the eyes and nose. It could be rubbed into the eyes from the face or into the nose by nose picking – but how common is that?  Certainly, washing your hands and not touching your face along with physical distancing at 6 feet seem like common sense rules.  But is that going to protect you?

I have never felt like any of those measures was enough and this week a letter came out pointing out the evidence for airborne transmission of respiratory viruses in general and for SARS-CoV-2 in particular.  I was pleased to see Dr. Milton as a co-author of this statement.  I have been reading his work for 20 years on airborne viruses in buildings of different design including the viruses that have been detected both in the air and the occupants of the building. This paper is a brief commentary specific to SARS-CoV-2 with a couple of generalities about airborne viruses and it is signed by 239 scientists who support it. 

   

The commentary starts out as an appeal to the medical community to recognize the potential for airborne spread of COVID-19.  Airborne transmission is defined as the release of droplets containing viral particles during breathing, coughing, sneezing, and any type of vocalization.  There is no doubt this happens. A distribution of droplet particle sizes occurs.  The larger droplets at a typical velocity settle out of the air in shorter distances typically in about 2 meters or 6 feet. The smaller droplets can travel much longer distances.  The authors cite an example of a 5 µm droplet at an original height of 1.5 meters and expelled at a typical indoor velocity travelling for “tens of meters” before it falls to the floor. This is typical airborne transmission and it will obviously not be contained by hand washing or physical distancing.

The authors on to describe some of the well-known scenarios where COVID-19 was transmitted despite no observed direct or indirect contact among the parties where the transmission occurred by video recordings.  They go on to cite other experiments demonstrating that several viruses (influenza, Middle East Respiratory Syndrome coronavirus (MERS-CoV), and respiratory syncytial virus (RSV) can all be spread by airborne routes. Although they don’t go into a lot of technical detail in the commentary, respiratory viruses are exhaled in normal tidal breathing.  The distribution and velocity of exhaled droplets will vary based on the way they are generated.  Infective viral RNA in small (5 µm) droplets from COVID-19 has been detected.

The critical sentence from this document follows:

“Hand washing and social distancing are appropriate, but in our view, insufficient to provide protection from virus carrying respiratory microdroplets released into the air by infected people.”

The is really a landmark statement from this group of experts. In my opinion it revolutionizes the approach not only to this virus but all respiratory viruses.  They all have access to the same type of spread and many have already been shown to have permeated heating and ventilation systems.  One of the main differences is virulence of the virus.  For example, smallpox or variola virus can cause an infection from the inhalation of a single viral particle (6).  Adenovirus, a much more common respiratory virus can cause an infection by the inhalation of as little as 6 viral particles (3).  Although adenovirus is potentially a flu-like respiratory virus, the main initiative at preventing the associated morbidity and mortality occurs in the military where a vaccination is used. The SARS-CoV-2 infections dose has been estimated to be about 280 particles – but the authors of one study suggest it is in the same ballpark of influenza virus and in that paper suggest that the amount of virus leading to infection in volunteers may be twice the amount of the aerosolized virus (5).

The main implication of airborne spread is that sustained inhalation of COVID-19 in poorly ventilated spaces of just being indoors increases risk of transmission. People who are coughing, sneezing, singing or engaged in any activity that results in forceful exhalation will expel small droplets at higher rates of speed and they will remain airborne for a longer period of time and travel much greater distances than the current suggested social distancing of 6 feet. 

To reduce the airborne transmission risk they have straightforward recommendations to avoid overcrowding (every additional person in the room is generating airborne droplets), have adequate ventilation, and supplement these measure with additions like HEPA filtration, germicidal UVC light, and exhausting room air rather than recirculating it. I can recall getting into an argument at one of my Avian Influenza Task Force meetings about a fast way to change the hospital ventilation system in the event of an influx of avian influenza patients.  Recall that the hospital was designed to retain heat by recirculating room air rather than exhausting it – like modern hospital rooms.  At the time, the counterargument was that it was just too expensive to build negative airflow rooms to prevent the flu virus from leaving the room with medical staff caring for the patients.  Most hospital rooms, even the ones I worked in that were built in the 1960s, had windows to the outside.  How difficult would it be to fit these windows with exhaust fans to the exterior of the hospital? 

This consideration is important now that there are political initiatives to reopen schools and other public places.  The ventilation systems of all of these places should be looked at and that assessment incorporated into the overall decision about how safe they are to open.  Further, there should be a systematic approach to how safe buildings are in general from the perspective of transmission of respiratory viruses.  A prospective approach that looks at how buildings in temperate climates need to be designed to minimize the spread of respiratory viruses needs to be a long term goal.  

It took a virus with heightened mortality and morbidity to raise awareness that physical measures rather than any available medication may be the best way to contain respiratory viruses.  Airborne transmission of respiratory virus denial dies hard - but hopefully it is being put to rest once and for all.  That should be a continued priority for everyone and momentum we cannot afford to lose.

George Dawson, MD, DFAPA

References:

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

2:  Erin Bromage.  The Risks - Know Them - Avoid Them.  Erin Bromage COVID-19 Musings.  May 16, 2020.  Link

3:  Yezli S, Otter JA. Minimum Infective Dose of the Major Human Respiratory and Enteric Viruses Transmitted Through Food and the Environment. Food Environ Virol. 2011;3(1):1–30. doi: 10.1007/s12560-011-9056-7. Epub 2011 Mar 16. PMCID: PMC7090536.

4:    Nicas, M., Hubbard, A. E., Jones, R. M., & Reingold, A. L. (2004). The Infectious Dose of Variola (Smallpox) Virus. Applied Biosafety, 9(3), 118–127. https://doi.org/10.1177/153567600400900302

5:  Schröder I. COVID-19: A Risk Assessment Perspective. J Chem Health Saf. 2020;acs.chas.0c00035. Published 2020 May 11. doi:10.1021/acs.chas.0c00035

Previous Airborne Transmission Posts from this Blog:

SARS-CoV-2 Is An Airborne Virus?

Viruses Are In The Air - Protection From Airborne Viruses

Hand Washing

New Twist On An Old Method To Kill The Flu Virus

Is It Time To Quarantine Air Travelers?


Supplementary:

This statement from a recent Nature article:

"But this conclusion is not popular with some experts because it goes against decades of thinking about respiratory infections. Since the 1930s, public-health researchers and officials have generally discounted the importance of aerosols — droplets less than 5 micrometres in diameter — in respiratory diseases such as influenza."

from:  Dyani Lewis.  Mounting evidence suggests coronavirus is airborne — but health advice has not caught up.  Link.



Graphics Credit:

Graphic at the top is from Reference 1 based on the following CC License.  This is an Open Access article distributed under the terms of the Creative Commons Attribution- NonCommercial-NoDerivs licence (http://creativecommons.org/licenses/by-nc-nd/4.0/),

SARS-CoV-2 is an Airborne Virus?

I thought I would say something more about airborne viruses. They have been a hobby of mine for some time.  The first time I heard about how easily the current coronavirus was spreading I thought “this is an airborne virus”. But then there were the usual protests. Some scientists came out and said that coronavirus requires “droplet” precautions rather than “airborne” precautions. The common definition is that droplets are large enough settle out quickly. They may touch you directly if you are close enough but a lot of what droplets do is settle on surfaces. That leads to surface contamination and spread of the virus.  Airborne viruses can travel longer distances within smaller droplets. An even more unique characteristic is that airborne viruses are released with normal expiration. No coughing, sneezing, or shouting is necessary. Just normal breathing can release airborne respiratory viruses into the air in the smallest droplet fraction.

An easy way to conceptualize airborne viral spread is to look at the distribution of particles occurring with every breath. They can range in size from 200 µm on the large end to less than 5 µm on the lower end. Experiments can be done to show how aerosols of these particle sizes spread through a room. Naturalistic experiments can also look at how these are all spread through hospitals, airplanes, and other natural settings. By looking at those patterns and the distance involved as well as any other paths that could lead to transmission – a determination can be made about whether or not a viruses “airborne” or not.

The second issue is whether or not live infectious virus is spread by these droplets. In many cases that has been limitation in the experiments. Direct evidence of viral spread at a distance requires culture of the virus or a bioassay that shows the samples have a cytopathic (killing) effect on live cells. Indirect evidence is typically by PCR where the available nucleic acid is amplified and assayed.  In researching this topic, I found early literature that documented numerous respiratory viruses in ventilation systems of buildings. That research was possible because nobody knew how to capture and culture the virus samples until that time. The other technical issue is air sampling. Certain air sampling devices do not allow for adequate virus detection. There is a technical report recently that showed of a total of four commonly used air sampling devices only one allowed virus to be identified or cultured. These technical constraints have led to a lot of confusion about whether a particular virus is airborne or not.

A practical definition of an airborne virus is one that is exhaled during normal breathing can travel a distance in small droplets (less than 5 µm) and create infection by landing on mucosal surfaces, facial services, or the lining of the nasopharynx, oropharynx, or lungs.  In that case you don’t have to be in the presence of anyone coughing or sneezing. You don’t have to touch any contaminated surfaces. You don’t have to touch your face. You just have to breathe contaminated air. It is entirely possible that you can walk through a cloud of airborne virus and not be aware of how it got there. A common example is walking down the hallway after a crowd of people have walked through some of them carrying the virus. Once you know about airborne viruses it gives you an entirely different perspective on social distancing.  Airborne particles can easily transverse the longest dimension of typical rooms. The distance of 6 feet suggested in typical social distancing guidelines is not nearly far enough.

In a previous post I highlighted an experiment by Donald K. Milton where he designed a machine to sample flu viruses in a natural setting. Research subjects breathed normally and their expired air was sampled for influenza virus. Influenza virus was recovered from 89% of the nasopharyngeal swabs and 39% of the fine aerosol sample defined as droplets less than or equal to 5 µm and greater than 0.05 µm. There was no coughing or sneezing during the collection.. That is proof that influenza virus is airborne.

A recent experiment carried out at the University of Nebraska Medical Center (3) in their bio containment and quarantine units showed that in addition to abundant surface contamination by SARS-CoV-2 the virus was also present in hallway air samples, in areas where only aerosol deposits could reach, and personal air samplers carried by staff.  The virus was detected by PCR analysis as well as culture in some cases. The authors concluded that this was definite evidence of an airborne virus and that facilities treating patients with SARS-CoV-2 should use airborne precautions. This paper is currently undergoing peer review and is on a preprint server.

The technical aspects of aerosol fractionation and dispersion is a subject best addressed in the engineering literature. The best paper I could find on the subject (4) had a goal of studying the dispersion characteristics of exhaled droplets in a ventilated room. The engineering goals are to find out what physical parameters affect the dispersion rate and hopefully lead to better indoor environments. The experimental paradigm looked at a room that was 5 x 4 x 3 m (L x W x H) and ventilated by a downward airflow from the ceiling. Aerosols were injected into this room and the following distance and trajectory along with trajectory time was calculated for the fractional droplets. As expected droplets with larger diameters (110-115 µm) fell at a faster rate and traveled a much shorter distance than the smaller diameter fraction. Droplet dispersion was studied under a number of physical conditions including different airflow, different temperatures, different relative humidity, and the original exhaled initial velocity.

The 0.1, 1.0, and 10 µm droplets covered horizontal distance of 5 m or the entire length of the room. Droplets in the range of 50 to 200 µm cover distances ranging from 0.5 to 4 m.  This study has numerous excellent graphs about varying conditions and how droplets in different fractions are dispersed. The reader is referred to the original reference to review all those conditions. The bottom line for me was it is clear that airborne droplets in the 0.1 to 10 µm range are commonly seen in exhaled air and easily covered distance in this experiment of 5 m or (for Americans) 16.4 feet. That is well beyond social distancing recommendations it explains why this virus continues to spread. Within the past week I have seen clips of New Yorkers in congested subway cars.  Any asymptomatic SARS-CoV-2 carriers in those cars are expelling virus into the air just by tidal volume breathing.  Coughing and sneezing is not required. It would be very good if you covered your cough or sneeze but when your mouth is not covered and you are a symptomatic or asymptomatic carrier you are exhaling viral particles.

The relevance of this virus being airborne cannot be underestimated. It is a substantial part of the reason behind social distancing and stay-at-home orders. It is the reason for the new recommendation to wear masks in public and the various explanations being given for those masks. The absolute best approach is to not have any close social contact until this pandemic is over. I am very concerned about my colleagues and fellow healthcare workers who have inadequate personal protective equipment (PPE). The expectation is that they will continue to take care of the very ill patients with COVID-19. Every effort must be made to make sure they have adequate protection. 

In my particular specialty, all psychiatrists should have access to electronic interviewing at this point. As I pointed out in my earlier posts, I am used to talking people for 30 to 60 minutes at time. Some of those evaluations are 90 minutes in duration. During that time the patient may be coughing or sneezing but for the most part they are breathing and engaged in normal interview conversation. My office is smaller than the room described in the droplet dispersion experiment. By the end of one interview, the smallest fraction of exhaled droplets is dispersed throughout the room. Any viral particles in that fraction can lead to infection.

All health care workers in these environments need immediate protection by the implementation of airborne precautions. I am hopeful that as more people become aware of the airborne route of transmission that it will lead to more caution on the part of the public and the social distancing and staying at home and away from this kind of transmission will make more sense. In the future we need to design indoor environments that can minimize this type of transmission. There is too little innovation in the role of the physical environment in airborne transmission of infectious illness.

I hope the added cost will be looked at in terms of the total cost of illnesses caused by respiratory viruses every year with the recognition that they can still cause devastating pandemics.

George Dawson, MD, DFAPA


References:


1: Lei H, Li Y, Xiao S, Lin CH, Norris SL, Wei D, Hu Z, Ji S. Routes of transmission of influenza A H1N1, SARS CoV, and norovirus in air cabin: Comparative analyses. Indoor Air. 2018 May;28(3):394-403. doi: 10.1111/ina.12445. Epub 2018 Jan 6. PubMed PMID: 29244221. 

2: Yu IT, Li Y, Wong TW, Tam W, Chan AT, Lee JH, Leung DY, Ho T. Evidence of airborne transmission of the severe acute respiratory syndrome virus. N Engl J Med. 2004 Apr 22;350(17):1731-9. PubMed PMID: 15102999.

3: Santarpia et al. (2020) Transmission potential of SARS-CoV-2 in viral shedding observed at the University of Nebraska Medical Center. Retrieved from https://www.medrxiv.org/content/10.1101/2020.03.23.20039446v2.

4: Chen C, Zhao B. Some questions on dispersion of human exhaled droplets in ventilation room: answers from numerical investigation. Indoor Air. 2010 Apr;20(2):95-111. doi: 10.1111/j.1600-0668.2009.00626.x. Epub 2009 Sep 24. PubMed PMID: 20002792.

5: Li, Y., Huang, X., Yu, I.T.S., Wong, T.W. and Qian, H. (2005), Role of air distribution in SARS transmission during the largest nosocomial outbreak in Hong Kong. Indoor Air, 15: 83-95. doi:10.1111/j.1600-0668.2004.00317.x

6: Carl Heneghan, Jon Brassey, Tom Jefferson. SARS-CoV-2 viral load and the severity of COVID-19.  March 26, 2020.  Link

7:  National Research Council 2020. Rapid Expert Consultation on the Possibility of Bioaerosol Spread of SARS-CoV-2 for the COVID-19 Pandemic (April 1, 2020). Washington, DC: The National Academies Press. https://doi.org/10.17226/25769.

"While the current SARS-CoV-2 specific research is limited, the results of available studies are consistent with aerosolization of virus from normal breathing."

8: Pan M, Bonny TS, Loeb J, Jiang X, Lednicky JA, Eiguren-Fernandez A, Hering S, Fan ZH, Wu CY. Collection of Viable Aerosolized Influenza Virus and Other Respiratory Viruses in a Student Health Care Center through Water-Based Condensation Growth. mSphere. 2017 Oct 11;2(5). pii: e00251-17. doi: 10.1128/mSphere.00251-17. eCollection 2017 Sep-Oct. PubMed PMID: 29034325.

9: Lu J, Gu J, Li K, Xu C, Su W, Lai Z, et al. COVID-19 outbreak associated with air conditioning in restaurant, Guangzhou, China, 2020. Emerg Infect Dis. 2020 Jul [date cited]. https://doi.org/10.3201/eid2607.200764

Graphics Credit:

Graphic is from Shutterstock per their standard agreement.