Opinion | Why Covid's Airborne Transmission Was Acknowledged So Late - The New York Times

Guest Essay

May 7, 2021

By Zeynep Tufekci

Dr. Tufekci is a contributing Opinion writer who has extensively examined the Covid-19 pandemic.

This article has been updated.

A few sentences have shaken a century of science.

A week ago, more than a year after the World Health Organization declared that we face a pandemic, a page on its website titled “Coronavirus Disease (Covid-19): How Is It Transmitted?” got a seemingly small update.

The agency’s response to that question had been that “current evidence suggests that the main way the virus spreads is by respiratory droplets” — which are expelled from the mouth and quickly fall to the ground — “among people who are in close contact with each other.”

The revised response still emphasizes transmission in close contact but now says it may be via aerosols — smaller respiratory particles that can float — as well as droplets. It also adds a reason the virus can also be transmitted “in poorly ventilated and/or crowded indoor settings,” saying this is because “aerosols remain suspended in the air or travel farther than 1 meter.”

The change didn’t get a lot of attention. There was no news conference, no big announcement.

Then, on Friday, the Centers for Disease Control and Prevention also updated its guidance on Covid-19, clearly saying that inhalation of these smaller particles is a key way the virus is transmitted, even at close range, and put it on top of its list of how the disease spreads.

There was no news conference by the C.D.C. either.

But these latest shifts challenge key infection control assumptions that go back a century, putting a lot of what went wrong last year in context. They may also signal one of the most important advancements in public health during this pandemic.

If the importance of aerosol transmission had been accepted early, we would have been told from the beginning that it was much safer outdoors, where these small particles disperse more easily, as long as you avoid close, prolonged contact with others. We would have tried to make sure indoor spaces were well ventilated, with air filtered as necessary. Instead of blanket rules on gatherings, we would have targeted conditions that can produce superspreading events: people in poorly ventilated indoor spaces, especially if engaged over time in activities that increase aerosol production, like shouting and singing. We would have started using masks more quickly, and we would have paid more attention to their fit, too. And we would have been less obsessed with cleaning surfaces.

Our mitigations would have been much more effective, sparing us a great deal of suffering and anxiety.

Since the pandemic is far from over, with countries like India facing devastating surges, we need to understand both why this took so long to come about and what it will mean.

*

Initially, SARS-CoV-2 was seen as a disease spread by respiratory droplets, except in rare cases of aerosol transmission during medical procedures like intubation. Countertops, boxes and other possible fomites — contaminated surfaces — were seen as a threat because if we touched them after droplets fell on them, it was believed the virus could make its way to our hands, then our noses, eyes or mouths.

The implications of this were illustrated when I visited New York City in late April — my first trip there in more than a year.

A giant digital billboard greeted me at Times Square, with the message “Protecting yourself and others from Covid-19. Guidance from the World Health Organization.”

First, “Hygiene” flashed, urging me to wash my hands, “practice respiratory hygiene,” avoid touching my face and wear a mask when necessary. Next, “Social distancing” told me to avoid close contact with people (illustrated by people separated by one meter), avoid shaking hands and stay home if unwell. Then “Medical help” advised me to follow local medical protocols.

I was stunned that the final instruction was “Stay informed.”

That billboard neglected the clearest epidemiological pattern of this pandemic: The vast majority of transmission has been indoors, sometimes beyond a range of three or even six feet. The superspreading events that play a major role in driving the pandemic occur overwhelmingly, if not exclusively, indoors.

The billboard had not a word about ventilation, nothing about opening windows or moving activities outdoors, where transmission has been rare and usually only during prolonged and close contact. (Ireland recently reported 0.1 percent of Covid-19 cases were traced to outdoor transmission.)

The omission is not surprising. Throughout the pandemic, the W.H.O. was slow to accept the key role that infectious particles small enough to float could be playing.

Mary-Louise McLaws, an epidemiologist at the University of New South Wales in Sydney, Australia, and a member of the W.H.O. committees that craft infection prevention and control guidance, wanted all this examined but knew the stakes made it harder to overcome the resistance. She told The Times last year, “If we started revisiting airflow, we would have to be prepared to change a lot of what we do.” She said it was a very good idea, but she added, “It will cause an enormous shudder through the infection control society.”

This assumption that these larger droplets that can travel only a few feet are the main way the disease spreads is one of the key reasons the W.H.O. and the C.D.C. didn’t recommend masks at first. Why bother if one can simply stay out of their range? After the C.D.C. recommended masks in April 2020, the W.H.O. shifted last June, but it first suggested ordinary people generally wear masks if physical distancing could not be maintained, and still said health care workers performing screenings in the community did not need to wear masks if they could stay that single meter away from patients. The W.H.O. last updated its mask guidance in December but continued to insist that mask use indoors was not necessary if people could remain separated by that mere meter — this time conceding that if ventilation might not be adequate, masks should be worn indoors, regardless of distancing.

In contrast, if the aerosols had been considered a major form of transmission, in addition to distancing and masks, advice would have centered on ventilation and airflow, as well as time spent indoors. Small particles can accumulate in enclosed spaces, since they can remain suspended in the air and travel along air currents. This means that indoors, three or even six feet, while helpful, is not completely protective, especially over time.

To see this misunderstanding in action, look at what’s still happening throughout the world. In India, where hospitals have run out of supplemental oxygen and people are dying in the streets, money is being spent on fleets of drones to spray anti-coronavirus disinfectant in outdoor spaces. Parks, beaches and outdoor areas keep getting closed around the world. This year and last, organizers canceled outdoor events for the National Cherry Blossom Festival in Washington, D.C. Cambodian customs officials advised spraying disinfectant outside vehicles imported from India. The examples are many.

Meanwhile, many countries allowed their indoor workplaces to open but with inadequate aerosol protections. There was no attention to ventilation, installing air filters as necessary or even opening windows when possible, more to having people just distancing three or six feet, sometimes not requiring masks beyond that distance, or spending money on hard plastic barriers, which may be useless at best. (Just this week, President Biden visited a school where students were sitting behind plastic shields.)

This occurred throughout the world in the past year. The United States has been a bit better, but the C.D.C. did not really accept aerosol transmission until October, though still relegating it to a secondary role until its change on Friday, which put the risk infection from inhaling these tiny particles first on its list of means of transmission.

*

The scientific wrangling, resistance and controversy that prevented a change in guidance stem from a century of mistaken assumptions whose roots go back to the origins of germ theory of disease in the 19th century.

Until germ theory became established in the 19th century, many people believed that deadly diseases like cholera were caused by miasma — stinking fumes from organic or rotting material. It wasn’t easy to persuade people that creatures so small that they could not be seen in a seemingly innocent glass of water could be claiming so many lives.

This was a high-stakes fight: Getting the transmission mechanisms of a disease wrong can lead to mitigations that not only are ineffective but also make things worse. During the 19th century, fearing miasma, Londoners worked hard to direct their stinky sewers into the nearby Thames River, essentially spreading cholera even more.

But clear evidence doesn’t easily overturn tradition or overcome entrenched feelings and egos. John Snow, often credited as the first scientific epidemiologist, showed that a contaminated well was responsible for a 1854 London cholera epidemic by removing the suspected pump’s handle and documenting how the cases plummeted afterward. Many other scientists and officials wouldn’t believe him for 12 years, when the link to a water source showed up again and became harder to deny. (He died years earlier.)

Similarly, when the Hungarian physician Ignaz Semmelweis realized the importance of washing hands to protect patients, he lost his job and was widely condemned by disbelieving colleagues. He wasn’t always the most tactful communicator, and his colleagues resented his brash implication that they were harming their patients (even though they were). These doctors continued to kill their patients through cross-contamination for decades, despite clear evidence showing how death rates had plummeted in the few wards where midwives and Dr. Semmelweis had succeeded in introducing routine hand hygiene. He ultimately died of an infected wound.

Disentangling causation is difficult, too, because of confusing correlations and conflations. Terrible smells frequently overlap with unsanitary conditions that can contribute to ill health, and in mid-19th-century London, death rates from cholera were higher in parts of the city with poor living conditions.

Along the way to modern public health shaped largely by the fight over germs, a theory of transmission promoted by the influential public health figure Charles Chapin took hold.

Dr. Chapin asserted in the early 1900s that respiratory diseases were most likely spread at close range by people touching bodily fluids or ejecting respiratory droplets, and did not allow for the possibility that such close-range infection could occur by inhaling small floating particles others emitted. He was also concerned that belief in airborne transmission, which he associated with miasma theories, would make people feel helpless and drop their guard against contact transmission. This was a mistake that would haunt infection control for the next century and more.

In modern medical parlance, respiratory transmission routes are divided between the larger droplets, associated with diseases that spread at close distance, and the smaller aerosols (sometimes also called droplet nuclei), associated with diseases like measles that we know can spread at long distance and are usually highly contagious. Indeed, studies showing that respiratory diseases spread more easily in proximity to infected people seemingly confirmed the role of droplets.

It was in this context in early 2020 that the W.H.O. and the C.D.C. asserted that SARS-CoV-2 was transmitted primarily via these heavier, short-range droplets, and provided guidance accordingly.

But from the beginning, the way the disease was spreading around the world did not fit this theory well. In February 2020, after an infected person was found to have boarded the cruise ship Diamond Princess, hundreds of people trapped on board for weeks were infected, including 567 of the 2,666 passengers, who were largely confined to their rooms and delivered food by masked personnel — hard to explain solely with droplet-driven transmission. (Hitoshi Oshitani, a Japanese virologist who played an important role in his country’s response to the epidemic, said it was this ship outbreak that helped convince him this was airborne — and it’s why Japan planned around airborne transmission assumptions from as early as February 2020.)

Then there were the many superspreader events around the world that defied droplet explanations. In March 2020 in Mount Vernon, Wash., 61 pandemic-aware people showed up to a choir practice and sang with some distance between them in a large space, were provided hand sanitizer and left the doors open, reducing the need for people to touch the handles. But 53 of them were confirmed or strongly suspected to have contracted Covid-19 anyway, and two died. Long-distance transmission was being documented as well: One study from China in April 2020, clearly documenting transmission from beyond one meter, had video evidence showing the initially infected person had not come very close to those he infected, and there were no common surfaces touched.

Epidemiological studies and examples kept pouring in, too, all of them showing that Covid-19 was spreading primarily indoors and clusters were concentrated in poorly ventilated spaces. And when outdoor transmission did occur, it was often when people were in prolonged close contact, talking or yelling, as with construction workers on the same site.

The disease was also greatly overdispersed, sometimes being not very contagious and other times dramatically so. Large-scale studies showed that more than 70 percent of infected people did not transmit to any other person, while as few as 5 percent may be responsible for 80 percent of transmissions through superspreading events. Despite databases documenting thousands of indoor superspreader incidents, I’m not aware of a single confirmed outdoor-only case of superspreading.

None of this could be explained easily if the disease were “primarily transmitted between people through respiratory droplets and contact routes,” as the W.H.O. had said, since those larger, heavier particles would behave the same indoors as outdoors, would be largely indifferent to ventilation and would not be conducive to so much superspreading.

Finally, it was clear from early on that people who weren’t yet sick or coughing or sneezing — which produce a lot more droplets — were transmitting and that things correlated with aerosol emissions like talking, yelling and singing were associated with many of the outbreaks.

Amid the growing evidence, in July, hundreds of scientists signed an open letter urging the public health agencies, especially the W.H.O., to address airborne transmission of the coronavirus.

That month, after the open letter, the W.H.O. updated its guidance to say that “short-range aerosol transmission” from infected people in poorly ventilated spaces over time “cannot be ruled out” but went on to say that “the detailed investigations of these clusters suggest that droplet and fomite transmission could also explain human-to-human transmission within these clusters” and that close contact could still be the reason, “especially if hand hygiene was not performed and masks were not used when physical distancing was not maintained.”

Evidence kept accumulating. Transmission was documented in adjacent rooms in a quarantine hotel where people never interacted. Several hospital workers were proved to have been infected despite strict contact and droplet precautions. Viable virus was found in air samples from hospital rooms of Covid-19 patients who hadn’t had aerosol-generating procedures and in an air sample from an infected person’s car. The virus was found in exhaust vents in hospitals, and ferrets in cages connected only via shared air infected each other. And so on.

There were quibbles with each study: Was the sampled virus infective enough? (It is hard to catch the viruses from the air without destroying them.) Could some fomite connection have been missed? Still, it kept getting harder to deny the role of aerosols as a major factor.

Last October, the C.D.C. published updated guidance acknowledging airborne transmission, but as a secondary route under some circumstances, until it acknowledged airborne transmission as crucial on Friday. And the W.H.O. kept inching forward in its public statements, most recently a week ago.

*

Linsey Marr, a professor of engineering at Virginia Tech who made important contributions to our understanding of airborne virus transmission before the pandemic, pointed to two key scientific errors — rooted in a lot of history — that explain the resistance, and also opened a fascinating sociological window into how science can get it wrong and why.

First, Dr. Marr said, the upper limit for particles to be able to float is actually 100 microns, not five microns, as generally thought. The incorrect five-micron claim may have come about because earlier scientists conflated the size at which respiratory particles could reach the lower respiratory tract (important for studying tuberculosis) with the size at which they remain suspended in the air.

Dr. Marr said that if you inhale a particle from the air, it’s an aerosol. She agreed that droplet transmission by a larger respiratory particle is possible, if it lands on the eye, for example, but biomechanically, she said, nasal transmission faces obstacles, since nostrils point downward and the physics of particles that large makes it difficult for them to move up the nose. And in lab measurements, people emit far more of the easier-to-inhale aerosols than the droplets, she said, and even the smallest particles can be virus laden, sometimes more so than the larger ones, seemingly because of how and where they are produced in the respiratory tract.

Second, she said, proximity is conducive to transmission of aerosols as well because aerosols are more concentrated near the person emitting them. In a twist of history, modern scientists have been acting like those who equated stinky air with disease, by equating close contact, a measure of distance, only with the larger droplets, a mechanism of transmission, without examination.

Since aerosols also infect at close range, measures to prevent droplet transmission — masks and distancing — can help dampen transmission for airborne diseases as well. However, this oversight led medical people to circularly assume that if such measures worked at all, droplets must have played a big role in their transmission.

Other incorrect assumptions thrived. For example, in July, right after the letter by the hundreds of scientists challenging the droplet paradigm, Reuters reported that Dr. John Conly, who chairs a key W.H.O. infection prevention working group, said that there would be many more cases if the virus was airborne and asked, “Would we not be seeing, like, literally billions of cases globally?” He made similar claims last month. And he is not the only member of that group to assert this, a common assumption in the world of infection control well into 2021.

However, Dr. Marr pointed out, there are airborne diseases, like measles, that are highly contagious and others, like tuberculosis, that are not. Moreover, while SARS-CoV-2 is certainly not as infectious as measles on average, it can be highly infectious in the superspreading events driving the pandemic.

Many respiratory viruses carried by aerosols survive better in colder environments and lower relative humidity, Dr. Marr said, again fitting the pattern of outbreaks around the world, for example, in many meatpacking plants. Plus, some activities produce more aerosols — talking, yelling, singing, exercising — also fitting the pattern of outbreaks globally.

Why did it take so long to understand all this?

*

One reason is that our institutions weren’t necessarily set up to deal with what we faced. For example, the W.H.O.’s Infection Prevention and Control (I.P.C.) global unit primarily concentrates on health care facilities. Many of the experts they enlisted to form the Covid-19 I.P.C. Guidance Development Group were hospital-focused, and some of them specialized in antibiotic-resistant bacterial infections that can spread wildly in health care facilities when medical personnel fail to regularly wash their hands. So this focus made sense in a prepandemic world. Hospitals employ trained health care workers and are fairly controlled, well-defined settings, with different considerations from those of a pandemic across many environments in the real world. Further, in some countries like the United States, they tend to have extensive engineering controls to dampen infections, involving aggressive air-exchange standards, almost like being outdoors. This is the opposite of modern office and even residential buildings, which tend to be more sealed for energy efficiency. In such a medical environment, hand hygiene is a more important consideration, since ventilation is taken care of.

Another dynamic we’ve seen is something that is not unheard-of in the history of science: setting a higher standard of proof for theories that challenge conventional wisdom than for those that support it.

As part of its assessment of the virus’s spread, the W.H.O. asked a group of scientists last fall to review the evidence on transmission of the coronavirus. When reviewing airborne transmission, the group focused mostly on studies of air samples, especially if live virus was captured from the air, which, as mentioned above, is extremely hard. By that criterion, airborne transmission of the measles virus, which is undisputed, would not be accepted because no one has cultivated that pathogen from room air. That’s also true of tuberculosis. And while scientists, despite the difficulties, had managed to capture viable SARS-CoV-2 in three studies that I’m aware of, the review noted that the virus was detected only intermittently in general, disputed whether the captured live virus was infective enough and ultimately said it could not reach “firm conclusions over airborne transmission.” The lead author and another senior member of the research group previously said they believed transmission was driven by droplets.

The skepticism about airborne transmission is at odds with the acceptance of droplet transmission. Dr. Marr and Joseph Allen, the director of the Healthy Buildings program and an associate professor at Harvard’s T.H. Chan School of Public Health, told me that droplet transmission has never been directly demonstrated. Since Dr. Chapin, close-distance transmission has been seen as proof of droplets unless disproved through much effort, as was finally done for tuberculosis.

Another key problem is that, understandably, we find it harder to walk things back. It is easier to keep adding exceptions and justifications to a belief than to admit that a challenger has a better explanation.

The ancients believed that all celestial objects revolved around the earth in circular orbits. When it became clear that the observed behavior of the celestial objects did not fit this assumption, those astronomers produced ever-more-complex charts by adding epicycles — intersecting arcs and circles — to fit the heavens to their beliefs.

In a contemporary example of this attitude, the initial public health report on the Mount Vernon choir case said that it may have been caused by people “sitting close to one another, sharing snacks and stacking chairs at the end of the practice,” even though almost 90 percent of the people there developed symptoms of Covid-19. Shelly Miller, an aerosol expert at the University of Colorado Boulder, was so struck by the incident that she initiated a study with a team of scientists, documenting that the space was less full than usual, allowing for increased distance, that nobody reported touching anyone else, that hand sanitizer was used and that only three people who had arrived early arranged the chairs. There was no spatial pattern to the transmission, implicating airflows, and there was nobody within nine feet in front of the first known case, who had mild symptoms.

Galileo is said to have murmured, “And yet it moves,” after he was forced to recant his theory that the earth moved around the sun. Scientists who studied bioaerosols could only say, “And yet it floats.”

*

So much of what we have done throughout the pandemic — the excessive hygiene theater and the failure to integrate ventilation and filters into our basic advice — has greatly hampered our response. Some of it, like the way we underused or even shut down outdoor space, isn’t that different from the 19th-century Londoners who flushed the source of their foul air into the Thames and made the cholera epidemic worse.

Righting this ship cannot be a quiet process — updating a web page here, saying the right thing there. The proclamations that we now know are wrong were so persistent and so loud for so long.

It’s true that as the evidence piled on, there was genuine progress and improvement, especially as of late. Even before the change in language last week, for example, the W.H.O. published helpful guides on ventilation, first in July and updating it in March. Recently, though the organization’s documents have lagged, more of its officials have started giving advice compatible with aerosol transmission, emphasizing things like close mask fit — which matters little for droplet transmission — and ventilation — which matters even less. All this is good, but nowhere near enough to change the regulations and policy bundles that had already been put in place around the world.

And the progress we’ve made might lead to an overhaul in our understanding of many other transmissible respiratory diseases that take a terrible toll around the world each year and could easily cause other pandemics.

So big proclamations require probably even bigger proclamations to correct, or the information void, unnecessary fears and misinformation will persist, damaging the W.H.O. now and in the future.

Scientists have responded. In just the past few weeks, there has been a flood of articles published about airborne transmission in leading medical journals. Dr. Marr and other scientists told me the situation was very difficult until recently, as the droplet dogma reigned. I co-wrote one of those papers, published in The Lancet last month, arguing that aerosols may be the predominant mode of transmission for SARS-CoV-2, a step farther.

I’ve seen our paper used in India to try to reason through aerosol transmission and the necessary mitigations. I’ve heard of people in India closing their windows after hearing that the virus is airborne, likely because they were not being told how to respond. Plus, there are important questions for what this means for higher-risk settings, like medical facilities.

The W.H.O. needs to address these fears and concerns, treating it as a matter of profound change, so other public health agencies and governments, as well as ordinary people, can better adjust.

The past year has revealed how crucial the agency is, despite being hampered by chronic underfunding, lack of independence and attempts to turn it into a political football by big powers. Like other public health organizations, many of its dedicated staff members work tirelessly under difficult conditions to safeguard health around the world. Maintaining its credibility is essential not just for the rest of this terrible pandemic but in the future.

It needs to begin a campaign proportional to the importance of all this, announcing, “We’ve learned more, and here’s what’s changed, and here’s how we can make sure everyone understands how important this is.” That’s what credible leadership looks like. Otherwise, if a web page is updated in the forest without the requisite fanfare, how will it matter?