Science Leads the Future
Knowing that an invisible, infectious virus may be lingering in the air of a stuffy room is an unsettling thing.
But even more unsettling is not knowing it could be there.
At the beginning of the COVID-19 pandemic, much of the world was unaware the SARS-CoV-2 coronavirus could be transmitted through the air. Following public health guidance, we dutifully washed our hands and kept our distance; some of us disinfected surfaces and even our groceries.
But the coronavirus was not just transmitted through short-range droplets emitted through coughing or sneezing.
Aerosol and atmospheric scientists from around the world were the first to sound the alarm on airborne transmission of coronavirus: Fine aerosol particles carrying the virus could linger and accumulate in the air for minutes to hours. Anyone sharing the space—even if they were farther away than the social distancing standard of 2 meters (6 feet)—could be at risk for inhaling these infected air particles.
But even before we began masking and avoiding crowded spaces, bad indoor air quality was already responsible for millions of deaths and debilitating health issues. And though we spend 90% of our time indoors, there is generally a lack of appreciation and awareness of the importance of the air around us. The composition of our indoor air matters to our health, whether it contains novel coronavirus or pollutants. But unlike outdoor air, the quality of the air we breathe indoors is not regulated.
If water is contaminated, we can still purchase bottled water, said Lidia Morawska, a physicist at Queensland University of Technology in Australia who runs an air quality lab specializing in airborne particulate matter. “But we have absolutely no choice on air we breathe. And we breathe continuously: If we stopped breathing for 3 minutes, we’ll die. That’s the importance of indoor air quality,” she said.
The revelation that COVID-19 can spread through the air could provide the attention and momentum needed to clear our indoor air for good. Some countries, such as Taiwan, already have regulations addressing indoor air quality. Others, such as Finland, are pursuing a holistic strategy involving health care and educational outreach as well as standards for managing air quality in indoor environments. In March 2022, the Biden administration launched the Clean Air in Buildings Challenge, calling on building owners and operators to adopt key strategies for improving indoor air quality as part of a broader strategy for reducing the spread of COVID-19.
Heightening interest in indoor air quality could save millions of lives—and prepare us for the next airborne pandemic.
“You know, it’s really too bad [awareness] took so long to get here,” said Linsey Marr, an expert on airborne transmission of viruses at Virginia Polytechnic Institute and State University. “But at the same time…I thought it would take a generation, I thought it would take 30 years for us to come this far if there had not been a pandemic.”
Aerosol Scientists Sound the Alarm
At the beginning of the pandemic in 2020, most public health agencies, including the World Health Organization (WHO), did not recognize airborne transmission—aerosol particles laden with infectious agents that can travel over long distances and time through the air—as a viable route for spreading COVID-19. Instead, the focus was on mitigating risk from large respiratory droplets that, expelled by coughs or sneezes, would fall quickly to the ground, leading to recommendations for handwashing and physical distancing.
But for many aerosol and atmospheric scientists, airborne transmission was not only a possibility but also the most likely explanation for the pattern of spread.
Superspreader events, such as the rehearsal of the Skagit Valley Chorale outside of Seattle, showed infections that could not be explained by close contact alone. Another well-documented case of COVID-19 spreading over long distances, through a poorly ventilated restaurant in Guangzhou, China, even included video recordings showing no close contact between infected people.
In addition, poorly ventilated indoor spaces, such as prisons and nursing homes, seemed to experience the worst outbreaks, whereas the likelihood of COVID-19 transmission was far lower outdoors than in.
“It was like, ‘Why, of course, it’s so obvious that it’s airborne,’” said Shelly Miller, an air pollution specialist and environmental engineer at the University of Colorado Boulder. “We were just flabbergasted that this was not something to be considered seriously.”
In the decades before COVID-19, researchers had demonstrated that viruses could be released, spread, and linger in aerosols for far longer and farther than was considered by health officials. “I think it was obvious to me and my colleagues because we understand the physics of airborne particles,” said Miller, lead author of the Skagit Valley Chorale study. “The particles don’t care what organism” they are—be it a fungus, bacterium, or novel coronavirus.
Before the pandemic, for example, Morawska carried around her own carbon dioxide meter to keep informed about the quality of the air surrounding her. “It’s so small it fits into any handbag I have,” she said. If someone was sick at a family gathering or in a staff meeting, she could ensure they were in a well-ventilated area and positioned where their exhaled air would not flow toward others. She would also mask up when she herself was ill.
“In reality, we knew that respiratory viruses such as SARS-CoV-2 spread through the air because they’re emitted from our respiratory activities—mouth, nose—when we speak, when we breathe, when we do anything else,” said Morawska, who has been an adviser on air quality to WHO since 1990. “There was really no disagreement, no question marks amongst scientists about this before the pandemic.”
However, finding direct evidence linking infected aerosols to disease spread is difficult, said Yuguo Li, a researcher of building environments at the University of Hong Kong and editor in chief of the journal Indoor Air.
For direct evidence, you would need to prove at least three things, said Li, who is part of the Lancet COVID-19 Commission. First, you need to show that someone infected breathed out aerosols. Second, you need to show that the aerosols in the space had sufficient viable virus in them. And third, you need to show that someone inhaled them and got infected. Even if all the mechanistic steps of transmission make sense, they are each difficult to prove.
“It’s difficult to get direct evidence [for airborne transmission] every time after this occurs,” Li said. “You cannot trace back the wind in your backyard 100 years ago.”
But there was still enough evidence to follow the precautionary principle for preventive action in the face of uncertainty. Li wondered: Are we going to wait around for definitive evidence when we know enough to take reasonable actions?
Throwing Caution to the Wind
In early March 2020, the director-general of WHO announced to the world that the coronavirus is not airborne. The organization had convened a committee to figure out how the virus is transmitted and how to prevent it, said Jose-Luis Jimenez, a chemist and aerosol expert at the University of Colorado Boulder, noting that the committee had six experts on handwashing and zero on airborne transmission. At the end of March 2020, the WHO tweeted “FACT: #COVID19 is NOT airborne.”
For Morawska, this was a turning point and a realization that something had to be done.
Over the course of 3 days—“I realized time is a factor”—Morawska brought together a group of 36 scientists who signed a petition with the aim of convincing health authorities that the current scientific understanding was different from what WHO was saying.
“Experts were in agreement,” Morawska said, “that this virus, like any other respiratory virus, spreads through the air. It was the disagreement between public health authorities, who were basically spreading misinformation, and experts from many different areas, which were trying to correct this.”
The letter initially led to conversations with WHO but no further action.
“They yell at us, basically. They think we’re like the 5G [conspiracy] people,” said Jimenez, who was part of the group of 36. “They still meet with us, but they don’t take us seriously.”
The letter, signed by 239 aerosol and atmospheric scientists, was published in July 2020. Shortly after, WHO held a press conference acknowledging airborne transmission as a possibility, albeit with disclaimers that such spread is relatively rare.
“But the significance of this was that 3 months were lost, [a] critical 3 months, which means that public health authorities around the world didn’t do anything about their own transmission,” Morawska said.
Further, the letter was not widely accepted by the medical community, Marr said, likely because there weren’t many medical doctors who signed it. There are only a few experts in the world who study both viruses and air.
But consensus continued to slowly build, and scientific evidence for COVID-19 airborne transmission has only grown. Following a National Academy of Sciences workshop in August 2020, Marr, along with Kim Prather and Jimenez, published an article in Science saying that SARS-CoV-2 is airborne. Afterward, the Centers for Disease Control and Prevention (CDC) started changing its tune about the possibility of airborne transmission, Marr said.
It was only in the spring of 2021 that airborne transmission of coronavirus became more widely accepted when three major medical journals—the Lancet, the BMJ, and the Journal of the American Medical Association—published articles about its importance and the accumulating evidence.
When asked for comment, a spokesperson for WHO wrote in an email in late April 2022 that “the terms used to describe transmission of SARS-CoV-2 have differed across scientific disciplines over the course of the pandemic. WHO has been communicating about the risk of all modes of transmission of SARS-CoV-2 including aerosols since the early stages of the pandemic. Our scientific understanding of SARS-CoV-2 continues to evolve. The emergence of SARS-CoV-2 Variants of Concern with increased transmissibility and greater binding affinity to the host entry receptor, ACE2, highlights the need to reiterate the risk of transmission of SARS-CoV-2, including airborne transmission at both short- and long-ranges, depending on the settings.”
“The consensus of COVID aerosol transmission comes out in a very sad manner, with more and more people dying,” Li said. “This is an unfortunate, natural experiment with our life.”
Communicating the Latest Science
Because it was difficult for scientists to publish their results, Twitter became a way to reach people and learn what evidence was missing.
Jimenez became glued to Twitter starting in March 2020. There, he shared information, built a community of scientists, and debated skeptics. “I probably spent a third of my working time on that,” Jimenez said. By the time he took a break in July 2021, he was “exhausted.” But then the Omicron variant hit, and he returned to high-intensity engagement.
He was also able to make the latest COVID-19 information more accessible, tweeting in both English and Spanish, a language that had fewer experts available to communicate crucial information.
“In some respects, it seems that the public got to this answer quicker than parts of the infection control community,” said William Nazaroff, an air quality engineer at the University of California, Berkeley and former editor in chief of Indoor Air. “It wasn’t that hard to persuade people that this really is airborne. You could use a mask, stay away from overly crowded, poorly ventilated conditions, and the public got that faster than some parts of the scientific community.”
Overturning Public Health Dogma
Part of the reason it was so hard and took so long for COVID-19 to be accepted as airborne by the medical community was a “default assumption” that diseases generally did not travel through the air, Marr said.
“It’s in textbooks that these types of diseases are spread by large droplets that spray onto someone’s eyes, nostrils, or lips, and it was just kind of accepted…without thinking about the mechanisms or the fundamental science behind that,” said Marr.
This long-standing dogma is a problem of history, Jimenez said—ancient history. The Greek physician Hippocrates believed that dirty air—miasma—was the root of illness, a view that persisted for more than 2 millennia. In 1910, influential epidemiologist Charles Chapin, with the aid of germ theory, popularized the idea that infection came from contact or droplet transmission. Since then, droplet transmission has become the dominant view.
Before the pandemic, only a handful of respiratory illnesses—tuberculosis, measles, and chicken pox—were accepted as having airborne transmission.
“There was so much resistance to the idea that flus and colds even are airborne,” said Marr, who coauthored a review of other respiratory viruses that could be transmitted through the air and whose research focused on flu transmission before the pandemic. But in addition to rethinking COVID-19 transmission, “I think that’s turning now, too, maybe.”
“We’ve had a bit of a pendulum swing,” agreed Nazaroff.
“The state of understanding and what we learned through experience with COVID is in some ways surprising,” explained Nazaroff, who has done research on the airborne spread of treatment-resistant tuberculosis. “It almost seems self-evident that a respiratory infection…is emitted from somebody who is infectious and then inhaled by a susceptible person as the primary mode of transmission.”
Every time we talk, cough, sneeze, or breathe, we emit particles of respiratory secretions and saliva in a wide range of sizes, from less than a micrometer to more than 100 micrometers in diameter. If there are pathogens in our respiratory system, they could hitch a ride on these particles and be transmitted.
Larger particles, responding readily to gravity, fall quickly to the ground close to the source, within about 2 meters. Smaller particles (aerosols) can remain aloft for minutes to hours, buoyed by air currents, before eventually falling to the ground if the air remains motionless. These aerosols are responsible for airborne transmission and can occur at short range (within 2 meters), where they are most easily transmitted because of higher concentrations of pathogen-containing particles; at long ranges (within a shared room); or even at longer ranges (even in different buildings).
It has been difficult to dislodge public health conceptions of which respiratory particles could be aerosolized. Medical textbooks, for example, considered anything larger than 5 micrometers to be a droplet that falls to the ground quickly, Marr said. But that number was the result of a 60-year-old scientific misunderstanding that, like a virus, propagated until it was established as medical dogma. The research evidence shows that much larger particles (50–100 micrometers) can remain airborne, particularly if there are ambient air currents, and can be carried more than 2 meters. Though there is no definitive cutoff for how large a particle needs to be to be considered a droplet, the threshold is closer to 100 micrometers, and many factors (such as how quickly it was expelled and the speed, temperature, and humidity of the surrounding airflow) can affect its ability to remain suspended.
Another hurdle was that the public health community had “a different way of gaining an understanding of a complex process,” Nazaroff said. For them, the gold standard is a randomized controlled trial that compares randomly assigned participants receiving an intervention to another group without it, “whereas from a physical science perspective, if I can show A goes to B goes to C goes to D goes to E goes to F—then I can connect A and F and I’m persuaded.”
Approaches from public health and different research disciplines have value, scientists said. “I hope the pandemic has brought more attention to this and to the importance of interdisciplinary and multidisciplinary collaborations to understand this,” said Marr.
Health officials also may have been reluctant to declare COVID-19 as airborne because it would shift responsibility from the individual, Morawska said. If COVID-19 were transmitted only through droplets or close contact, health was in the realm of individual responsibility: If you got sick, it was because you did not get vaccinated, wash your hands properly, or wear a mask. But if the virus could linger and spread in the air we all breathe, then the government and public health agencies needed to do something more systematic and costly.
Finally, in December 2021, without announcement or fanfare, WHO quietly changed its website guidelines to acknowledge that COVID-19 could be spread by airborne transmission, marking the first time the public health organization described the coronavirus as “airborne” and a reversal of its firm declaration to the contrary at the start of pandemic.
“Science is a complex, messy business at the frontier,” Nazaroff said. “It’s a human endeavor, so there are people’s egos and ambitions at stake. In a way it’s too bad, but it’s also not surprising. We’re all human actors as scientists, and we bring our strengths and our weaknesses to the enterprise.”
Jimenez gave a different perspective. “This is one of the biggest errors in the history of public health. They don’t want to admit it.”
Indoor Air Quality Is Essential
The pandemic has brought into sharp focus the importance of the air indoors, where most of us spend most of our lives. Indoor air quality problems were all around us before the pandemic and will linger long after if we do not do anything about them.
“When you look at how many contaminants are in the average house in the U.S. and Europe, it’s comparable to Mexico City outdoors on a really bad day,” said Jimenez.
Close to 4 million people are estimated to die prematurely each year because of the health effects of indoor air pollution. Poor air quality indoors is linked to a litany of health issues, including allergies, asthma, lung diseases, and cardiovascular diseases. It is also linked to absenteeism and poorer cognitive performance.
Our indoor air is not just a reflection of outdoor air getting in. Although pollution from the great outdoors can enter buildings, most of the pollutants arise from within. We may regularly produce combustion by-products like carbon monoxide, particulate matter, and smoke from our heating or cooking sources. In addition, personal care and cleaning products release all sorts of organic compounds; some building and furniture materials release formaldehyde.
There are natural pollutants as well, such as radon (a carcinogen), mold, pet dander, and dust. And as COVID-19 has taught us, aerosols in the air can also carry infectious agents.
Climate change, as usual, may make things worse. Worse and longer allergy seasons and worsening wildfires increase the amount of pollen, smoke, and soot making their way indoors. Carbon dioxide, which we release with every exhalation, accumulates indoors at levels found to be harmful to cognition.
Fortunately, we already have the know-how to dramatically improve indoor air quality.
Technological advances like more sensitive tests to detect virus loads in respiratory fluid allowed aerosol scientists to make measurements they couldn’t do routinely just 2 decades ago, Nazaroff said. Having said that, “I don’t think there’s any new, amazing technology that’s just gonna zap the pathogens out,” said Marr. “I think we can get a huge amount of benefit by better implementing the basic things we know about ventilation and filtration.”
Improving ventilation in a building can be as simple as opening a window, which increases airflow and dilutes any virus or pollutants. Air filters and air cleaners can be effective at reducing the amount of contaminant in the air.
For pathogens, including coronavirus, ultraviolet (UV) light treatment is an effective disinfectant, Morawska said. “There’s a lot of discussion about this aspect now because this technology has been known for a long time, for over 80 years. And it’s been used effectively in many places, particularly in health care.”
In an editorial for Indoor Air, Nazaroff articulated four principles expressed in 12 words for achieving good indoor air: Minimize indoor emissions. Keep it dry. Ventilate well. Protect against outdoor pollution.
“What’s standing in the way is a greater appreciation of the importance of clean air, and then the second is money, of course,” Marr said.
Building a Cleaner Future for Indoor Air
COVID-19 might give us the momentum needed to make long-term systemic changes and investments for improving our indoor air. “A big possibility, too early to say, is…that the experience with COVID will raise the profile of indoor air quality problems more generally,” said Nazaroff.
“When there’s not a pandemic, we still have indoor air quality problems, we still have toxic chemicals in our environment, we still have combustion sources. We still have formaldehyde, we still have flu,” said Miller. “There are all of these indoor air quality problems that we’ve been trying to solve for decades, that now we have the obvious attention of most of the public and the scientific community to say, ‘Wow, I can’t believe we’ve been overlooking indoor air.’”
“It’s not SARS-CoV-2 which is on my mind because this will pass,” Morawska said. “It is the future of infection transmission.… That’s why the time is now to put the regulations in place while we are still going through this. That’s why I and all the other scientists have put in all the work we can do towards this.”
In an editorial published in Science in May 2021, Morawska, along with many other experts, proposed a “paradigm shift” in how we combat indoor respiratory infection with building engineering solutions and public health policies.
Jimenez noted that the editorial echoed a call for better ventilation made in 1945 by William Wells, a pioneer of aerosol transmission. “Now, in 2021…well, we said the same thing, almost the same words: Ventilation has been neglected.”
The design of future buildings should support different ventilation strategies, Morawska said. “Future designs would take into account human health from all aspects of indoor air quality and energy as well.”
And we need more than just updated building codes, which establish minimum requirements, Miller said. “What happens with building codes as minimum is everyone just builds to the minimum. So the building is sort of minimally crappy.”
Instead, updated environmental legislation is needed, like what we already have for water and outdoor air quality to protect public health by setting health-based standards requiring the “best available control technology” to reach them, Miller said.
“What I’m stressing as much as possible now is that countries need national indoor air quality standards,” Morawska said.
Having standards means enforcing those standards, which in turn means making measurements, which is more complex and costly for indoor air than outdoor air, said Morawska. “It’s much more complex, but not impossible.”
Fortunately, many modern buildings are already equipped with sensors to detect carbon dioxide levels, which can be used as a proxy for ventilation and human-emitted pollutants. Though these sensors are used for HVAC (heating, ventilating, and air-conditioning) systems, such technologies could be implemented for measuring air quality.
In the United States, there is no government entity at either the state or federal level that is clearly responsible for the air quality of our indoor spaces, Nazaroff said. “Outdoor air is undoubtedly a shared resource. We all contribute to its pollution. But no one of us can fix it. Our indoor air has a more complex and nuanced balance between who’s responsible for it.”
Researchers are cautiously optimistic.
“The greatest success story in history for indoor air pollution has been the shift in smoking behavior,” Nazaroff said. Through a multifaceted approach of new rules, changes in social behavior, increased health awareness, and a generational shift, he said, “we’re now in a very different place than we were 30 years ago. And that gives me hope.”
Places like Finland, Sweden, South Korea, and Taiwan already have legislation for indoor air quality or ventilation. And the Clean Air in Buildings Challenge highlights recommendations and resources for improving ventilation and indoor air quality, as well as serving as a call to action for reducing risks related to airborne contaminants indoors.
“This is probably the most significant step which I’ve seen so far, and this hopefully will give other countries direction,” Morawska said.
Pollutants and infectious diseases will remain a lingering threat in our indoor air long after the current pandemic peters out. But COVID-19 may have changed how we see, cherish, and protect the air we breathe.
“I worry that people have a short attention span, but it feels like we’re potentially on the cusp of an indoor air revolution,” Marr said.
—Richard J. Sima (@richardsima), Science Writer