For Catherine Noakes, a scientist who studies how pathogens move in the built environment, the first few months of the coronavirus pandemic were punctuated with a foreboding sense of frustration.
That frustration was rooted in the readily accepted assumption that COVID-19 was not spreading through the air via microscopic particles called aerosols, but predominantly through larger respiratory droplets expelled among people in close proximity and falling quickly on nearby surfaces.
The World Health Organization (WHO) â€”Â which sets the tone for many nations â€”Â early on denied COVID-19 was spreading through these tiny aerosols suspended in air.
As evidence mounted, alongside pressure from scientists like Noakes, the agency eventually acknowledged the possibility of airborne transmission â€” but continued to downplay its significance in favour of droplets, placing a heavy emphasis on handwashing and disinfecting surfaces instead of more stringent measures.
Then as evidence suggesting the virus behind COVID-19 was primarily airborne grew to be overwhelming, the agency finally admitted in December 2021 that the virus could indeed be spreading via aerosols.
â€œYou can understand it in the early days â€” that we donâ€™t have all the evidence,â€ says Noakes, 46, speaking over a video call in January this year.
â€œSo, we should have been following the precautionary principle: wash your hands, clean your surfaces, keep your air clean. Instead, we just focused on the hands and surfaces because there wasnâ€™t an acceptance of the air mattering.â€
That, according to Noakes and a small band of aerosol scientists, was a critical mistake.
â€˜Confusing the publicâ€™
The WHO position relied on a doctrine that had dominated medical discourse for decades: that a respiratory infection-causing pathogen spreads disease primarily through close contact with an infected individual who sheds large droplets and carries the virus by speaking or coughing, for example.
Some infections, such as tuberculosis and measles, are understood to mainly spread via aerosols, where there isnâ€™t necessarily close contact with a sick person. In other words, airborne infections are traditionally seen as spreading over long distances.
But whether itâ€™s COVID-19, the flu, or other such infections â€” it is not one or the other, it is a continuum of large to tiny particles, says Noakes, a professor of environmental engineering at the University of Leeds in the United Kingdom.
If in the early months of the pandemic there wasnâ€™t much understanding about how this virus transmits, why did the WHO swiftly endorse large-droplet spread from the beginning?
â€œThatâ€™s a good question,â€ says Noakes. â€œWhy?â€ she asks, her hands up in the air.
â€œI mean, it doesnâ€™t make any physical sense whatsoever that the virus can be in large droplets but not small ones,â€ she adds, with an exasperated laugh. â€œI think itâ€™s a lack of understanding of the physics of how these things transmit.â€
For the better part of the last two years,Â Noakes has been educating her government as part of a scientific advisory group shaping the UKâ€™s COVID-19 response. She has evenÂ advised the WHOÂ on controlling building ventilation toÂ prevent the virus from spreading indoors.
She has convinced the UK government to add â€œfresh airâ€ to its COVID-19 campaign, helped formulate the WHOâ€™s belated guidelines on ventilation for control of the virus, and is playing a key role in lobbying for a global paradigm shift in regulatory standards for indoor air, which currently cover pollutants such as carbon monoxide and other chemicals, but not airborne pathogens.
But two years since it declared a global pandemic on March 11, 2020, the WHO â€”Â which remains at the heart of the global health response to the pandemic â€” still hasnâ€™t cleared the air about transmission.
It made a fatal error in undermining aerosol transmission early on and has dithered and delayed in backing it as a major route of transmission since, critics say.
Perhaps the worst part is that the agency has still not taken responsibility for its missteps and said it was wrong about airborne transmission, says Dr Kimberly Prather, an atmospheric chemist and aerosol expert at the University of California San Diego.
â€œYouâ€™re not quite admitting it and still doubling down â€” youâ€™re confusing the public in the midst of a global pandemic. Thatâ€™s not okay.â€
As a result, many more people have likely been infected and died, scientists argue. For Prather, Noakes and others in their niche area of research, it just didnâ€™t have to be this way.
Distinct corner of research
It was February 2020, and the WHO was holding a press conference on a novel coronavirus the world was just about getting to grips with.
Around the 40th minute, the agencyâ€™s Director-General Dr Tedros Adhanom Ghebreyesus described the COVID-causing virus â€” SARS-CoV-2 â€” as airborne. Some minutes later, following a hushed chat with Dr Michael Ryan, executive director of the WHOâ€™s health emergencies programme, Tedros recanted his original statement, apologised for saying â€œairborneâ€ and said he meant to say the virus was spreading through â€œdroplets or respiratory transmissionâ€. He rejected that it was airborne again in early March.
At the end of March 2020, the WHO tweeted: â€œFACT: #COVID19 is NOT airborne.â€
Noakes remembers it well, noting â€œIt was cited many times [by scientists] in 2020 to deny airborne transmission.â€
Alarmed that the WHO effectively ruled out the possibility that COVID-19 was airborne and concerned by the signal that this would send to countries formulating their pandemic response, Noakes, Prather and a few dozen aerosol scientists across the globe quickly organised to challenge this thinking. In an open letter that was eventually signed by 239 experts, they called for the need to address airborne transmission.
This small but vocal crew of scientists, occupying this corner of research and looking at how pathogens spread in the air, had quickly recognised the threat.
After all, they had spent years scrutinising and collecting evidence that suggests common illnesses like the flu, colds and the pathogen RSV (which can cause pneumonia and lung inflammation in infants) can spread through the air via fine aerosol particles.
There is even evidence supporting the spread of virus-laden particles of SARS and MERS â€”Â which belong to the coronavirus family â€”Â via air.
An epidemiological investigation, for example, of a previously mysterious 300-person outbreak in 2003 in a Hong Kong housing complex during the 2002-2004 severe acute respiratory syndrome (SARS) outbreak suggested that after an infected patient with diarrhoea visited a toilet in one apartment building, high concentrations of viral aerosols in the building plumbing were drawn into other apartment bathrooms through floor drains.
Winds then transported the virus-laden air to adjacent buildings tens of metres away, where more people were infected.
A separate study from the same outbreak found that at Hong Kongâ€™s Prince of Wales Hospital, 41 percent (30 of 74 patients) admitted to the ward where a SARS patient was admitted were infected. Most of the infected patients were in the same and adjacent bay while only 18 percent of people in distant bays contracted the disease. All nurses and physicians serving in the ward cared for patients across all bays â€” so if contact with the index case was spread to others through these healthcare workers, then the risk of infection shouldâ€™ve been distributed more evenly among the bays.
Instead, this pattern of infection related to proximity suggests airborne transmission, the researchers concluded, adding that no other known routes of infectious diseases transmission could adequately explain this type of spread.
This kind of detective work, alongside data collected from lab experiments, had long convinced scientists like Noakes that aerosolised particles tend to stick around suspended in the air and due to their diminutive size travel further indoors, versus larger droplets that drop onto people and surfaces quickly.
Given what these aerosol scientists had learned about these other viruses, Noakes and her peers theorised that it was unlikely SARS-CoV-2 would be dramatically different.
Keeping it simple
One can fathom why many scientists and the WHO were sceptical about airborne transmission.
For starters, it is harder to trace and grasp the idea of airborne infections because air as a contagion is, well, invisible, not to mention nebulous, not owned by anybody, and widespread.
When it comes to buildings and their airflows, things can get complicated and investigation more complex, unlike for food and water contaminants, for example, that usually come from a source that is easier to identify.
â€œYouâ€™ve got different sizes of droplets and aerosols and they evaporate differently, and it depends on temperature, ventilation, and peopleâ€™s behaviour. All these things happen,â€ says Noakes. â€œThat makes a really bad public message.â€
Besides, there is the natural human inclination to simplify the complex â€” you want to provide a simple message like COVID-19 is spread mainly through droplets â€” so the directive becomes wash your hands and keep your distance, explains Noakes.
These are also actions that can be managed individually.
But when the enemy is airborne â€”Â say via the simple act of breathing â€“ youâ€™re no longer in control.
The solutions necessary are more onerous and expensive,Â including measures to improve ventilation and air filtration, using medical-grade masks, curbing crowding and reducing time spent indoors. In hospital settings, this mode of spread requires negative pressure isolation rooms.
â€œThat only works when youâ€™ve got a very small number of cases of a disease, but not for these many cases,â€ Noakes says. â€œAnd so, because you canâ€™t apply airborne precautions, if you declare it as a droplet, then maybe you donâ€™t have to [apply them]?â€
â€˜More that the world should be doingâ€™
Calls from Noakes and her peers to address airborne transmission were met with resistance. In fact, they had trouble getting their open letter published.
It was rejected by two prestigious journals, Nature in May 2020 and then The Lancet the following month. (Neither journal offered spokespeople to comment on these decisions).
These rejections were the result of the process of peer review whereby a piece of scholarly work, research or idea is scrutinised by experts in the field. Scientists reviewing the open letter for the journals likely rejected it due to the prevailing view that droplets were the main mode of transmission, said Noakes.
In those days, many countries taking a cue from the WHO were emphasising washing hands and social distancing and not highlighting key interventions like ventilation and mask-wearing.
â€œAt the time, every day counted,â€ Noakes says. â€œIt was very frustrating â€¦ to know that there was more that the world should be doing.â€
That signal from the WHO and certain scientists that COVID-19 wasnâ€™t airborne did a huge amount of damage, notes Dr Deepti Gurdasani, an epidemiologist at Queen Mary University of London in the UK. â€œI really wonder how different things would have been had pretty much all of the world adopted high-grade masks and with the focus on ventilation,â€ she says.
In early July 2020, three months after Noakes and her colleagues made their first attempt, their open letter was published in the journal Clinical Infectious Diseases.
Days later, the WHO softened its position from denial to what Linsey Marr, an expert in airborne transmission of viruses at Virginia Tech in the United States and cosignatory of the open letter, described as â€œgrudging partial acceptanceâ€.
The United Nations agency had finally acknowledged the possibility of aerosol transmission but cautioned further research was needed.
Reaction to the letter was divisive. Some scientists came out swinging against the idea of virus-laden particles in the air.
Noakes recalls how she and her colleagues were even accused of running ventilation companies. â€œItâ€™s complete rubbish, none of us runs a ventilation company,â€ she says, bemused.
But the repudiation from sections of the medical community wasnâ€™t entirely surprising.
â€œDisease transmission has traditionally been the preserve of the medical profession and it felt like there was a dismissal of people from other fields, particularly engineers,â€ says Noakes.
There has been this resistance from people in medical fields, agrees Prather, who says, â€œTheyâ€™ve sort of dismissed our opinions.â€
One of the reasons for that has been the call from certain scientists in the medical field for randomised controlled trials (RCTs), considered a gold standard to measure an interventionâ€™s effect, to back airborne transmission measures.
That makes sense when youâ€™re measuring the effect (if any) of a vaccine or drug â€” because there are so many factors at play â€” but to apply it to airborne transmission measures doesnâ€™t make sense because it is possible to directly measure their impact, Prather said.
â€œIt makes sense that if something filters out 99 percent of aerosols, it will reduce the risk of transmission,â€ adds Gurdasani.
Noakes, who trained as an engineer, hadnâ€™t exactly envisioned a career in public health. But as a post-grad, she got hooked on disease transmission after being roped into a project to understand how UV light could be used to control tuberculosis. This type of research wasnâ€™t a neat engineering problem like, say, understanding how ships sail. Disease transmission is real life; itâ€™s a messy problem. â€œAnything biological has huge uncertainties in it,â€ she says.
In the early 2000s, Noakes started thinking seriously about the airborne transmission of infections that were thought to be spreading via droplets. It was a time when the importance of ventilation and the built environment, through the engineering of spaces with continuous airflow, for example, was remerging in terms of disease control. This renewed focus came about partly as cases of antibiotic-resistant pathogens were on the rise, and the SARS outbreak of 2002-2004 had reinforced the grave risk of worldwide transmission of infectious disease.
Slowly but surely, the evidence of the airborne transmission of many disease-causing viruses had been building. But as 2020 rolled around, and COVID-19 hit the headlines, Noakes and her motley crew of aerosol scientists were still largely seen as outsiders trying to dethrone a centuries-old theory.
â€œI think the evidence for airborne transmission was seen by some as weak and so the messaging was quite light touch,â€ Noakes says.
A medical dogma
Before governments or health authorities could drum up a message to underscore the importance of airborne transmission, they had to be convinced that it was a realistic possibility.
And this is in large part due to the idea ingrained in medical school that droplet transmission is the biggest contributor to the spread of respiratory infections, to counter stigma associated with the concept of miasma (which comes from the Greek word that means â€œto polluteâ€) advocated by the ancient Greek physician Hippocrates. He suspected dirty air was the root cause of diseases â€“ this was before pathogens were even a concept â€“ that attacked multiple people at the same time.
This more-than-two-millennia-old observation, while valid in the sense that it identified air as the common denominator, profoundly undermined the likelihood of an infected individual passing on the disease to another. â€œMiasmatistsâ€ â€” including nursing pioneer Florence Nightingale, who endorsed enhancing ventilation to heal those riddled by infection â€” dominated medical thinking right up until the 20th century.
Then, in 1910, influential American epidemiologist Charles Chapin popularised the notion that infection came not from the environment, but from contact with or proximity to an infected person.
Although diseases like cholera and malaria had by then been tied to other vectors of transmission, the main opposition to Chapinâ€™s assertions came from the entrenched miasmatist mode of thinking. He argued that infection spread was better explained by â€œspray-borneâ€ droplets, freeing practitioners of medicine â€œfrom the specter of infected air â€“ a specter which has pursued the race from the time of Hippocrates.â€
â€œHe advocated that it was mostly droplets that transmitted very close to people â€” and that sort of pushed airborne [transmission] out, particularly for particular things like viruses,â€ Noakes says, explaining that itâ€™s much harder to culture viruses versus bacteria for example, and so people just sort of took Chapin at his word.
He was very dismissive of airborne transmission, and he had a very outsized influence and ended up setting the terms for infectious disease transmission and control that lasted for 100 years, said Virginia Techâ€™s Marr.
Hesitation to say â€˜airborneâ€™
There are also socioeconomic implications of health authorities endorsing airborne transmission, particularly in countries that may not have good mechanical ventilation systems or enough respirators, says Marr: â€œThat is basically what the WHO told us when we were in a meeting with them in early April . I think they were very hesitant to call the disease airborne because it would basically tell these lower-resource settings â€¦ thereâ€™s no hope for you.â€
â€œThatâ€™s where the WHO have struggled â€¦ because they have to give advice that applies to the whole world,â€ says Noakes.
Lidia Morawska, director of the International Laboratory for Air Quality and Health at Queensland University of Technology in Australia and a co-author of the open letter, added that even in richer countries, recognition of airborne transmission would require major investment from governments to, for instance, retrofit schools to improve ventilation.
â€œAdmitting that the virus is airborne, and something has to be done with ventilation, government has to provide guidelines and means for doing this,â€ Morawska says.
The WHOâ€™s reticence in recognising aerosol transmission in 2020 could have also been linked to global supply-chain problems related to the manufacturing of personal protective equipment (PPE), some scientists suggested.
Gurdasani says that perhaps there was a decision taken that acknowledging airborne transmission could have jeopardised mask or PPE supplies for health workers.
â€œI donâ€™t think you should ever change your evidence to match what you want your policy to be. I think you need to be honest with people,â€ she says.
There are past examples of public health messaging creating a misleading impression, motivated by what authorities see as a pragmatic goal.
Messaging by the WHO and the Centers for Disease Control and Prevention (CDC) in the US on tobacco and e-cigarettes, for example, is an example of that, where the messaging has created the impression that all forms of tobacco are equally harmful and e-cigarettes are at least as harmful as cigarettes, said Robert West, a professor and health psychologist at University College London who sits on a committee advising the UK government on behavioural science.
â€œI think their motivation is based on the idea that more nuanced messaging would create an opening that the tobacco industry could exploit to undermine tobacco control more generally,â€ West says. â€œThis has been very contentious and raises an important ethical question about whether there is ever any justification for a public health authority to mislead the public for what it considers to be the benefit of public health.â€
The WHO did not directly respond to questions about airborne SARS-CoV-2 transmission, but said in an email that the agencyâ€™s scientific understanding of SARS-COV-2 continues to evolve.
â€œThe emergence of SARS-CoV-2 Variants of Concern with increased transmissibility â€¦ 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,â€ read the email. â€œWHO is updating its communication materials to reflect this language, and we expect the technical guidance to be reviewed, but our understanding of how the virus spreads and how to protect yourself remain the same.â€
Nevertheless, the initial burst of urgency placed on droplet-led transmission has been enshrined in public minds.
â€œWe spent a lot of our time washing our hands to â€˜Happy Birthdayâ€™ and cleaning surfaces â€¦ and that stuck,â€ says Stephen Reicher, a professor of psychology at the University of St Andrews in Scotland and another member of the UK government advisory committee on behavioural science.
â€œEven when the scientific understanding of COVID changed there was still an inertia because we didnâ€™t work on changing the representation and hence, we were still stuck, being fixated with the old mitigations while underappreciating the new. This was clear from polling â€” people still saw handwashing as more important than opening windows.â€
Superspreader events and research insights
That July 2020 open letter wasnâ€™t quite enough for global health authorities and governments, which needed more proof of this airborne hypothesis. So aerosol scientists peppered across the globe got on with the arduous process of gathering evidence.
Initially, the strongest signals came from so-called superspreader events where a single source infected a disproportionate number of people in an indoor space, situations that would be difficult to explain by only close contact.
One of the first such investigative studies, co-authored by Noakes, Marr, Morawska and others, looked at a two-and-a-half-hour choir practice involving 61 singers in Washington state in the US in May 2020. One person who attended had cold-like symptoms and was later diagnosed with COVID-19 â€” and after, 53 members of the choir were confirmed or strongly suspected to have contracted COVID-19, and two died. Aerosol transmission, the researchers concluded, was the most likely culprit given the precautions taken, including the use of hand sanitiser, no hugging, and no handshakes.
Although ventilation wasnâ€™t a prominent feature in the UK governmentâ€™s original COVID-19 slogan â€œhands, face, spaceâ€, as the evidence mounted on aerosol transmission, the government was listening to Noakes. Around June 2020, as the country saw the lifting of some restrictions, public officials started to encourage opening windows, and in the run-up to Christmas, there was all kinds of messaging around meeting outdoors and ventilating your home. Eventually, by the end of March 2021, â€œfresh airâ€ was added to the official slogan.
â€œThe [UK] government listened to her â€¦ because sheâ€™s been patient. I canâ€™t imagine that sheâ€™s had a normal weekend in two years,â€ said Noakesâ€™s colleague Barbara Evans, professor of public health engineering at the University of Leeds.
The reality of working in public health is that if you do your job well, nobody knows youâ€™re doing it, Evans said, adding that Noakes had previously done considerable work on infection management in hospitals and knew how crucial ventilation was.
â€œThen the COVID crisis sort of suddenly laid bare was how critical it all was. And sheâ€™s been remarkably generous about not saying to a load of people, â€˜I told you so.â€™â€
As the UK government opened the door for people to return to work and school later in 2021, Noakes helped develop a key model to predict how many people were likely to be infected by an asymptomatic but infectious person in those types of indoor settings.
Noakesâ€™s model showed that halving the occupancy of an office could reduce the risk of airborne transmission fourfold.
Her work has also involved modelling to predict the range of droplets and aerosols that are emitted when we breathe, talk and cough to understand how these particles are affected by factors like temperature and humidity and the risk of transmission through different routes â€“ via the air and hands, for example.
Some research insights are easy to implement â€“ such as in winter when itâ€™s cold and windy, ventilating a room with a small opening reduces exposure to the virus, and on a hot, still summer day, a wider opening will get the same result.
Insights have also paved the way for CO2 monitors, for example. When we breathe, we exhale carbon dioxide â€” so higher levels of CO2 in a room are indirect indicators of higher occupancy and lower ventilation. Changes can then be made, for example, to improve ventilation or attendance patterns. With CO2 a proxy for poor ventilation, monitors can be used in enclosed spaces such as classrooms, and the UK government last autumn announced that it would supply all state-funded educational settings with this equipment.
Inequality the difference between life and death
Some months after the slogan change in the UK, the WHO finally acknowledged the importance of aerosol transmission by the end of 2021, in a small update. The WHOâ€™s page on how COVID-19 is transmitted was tweaked to say that apart from droplets, aerosols are also a viable route of spread. There was no big announcement highlighting the change.
â€œTheyâ€™ve never moved to a correct the perception that itâ€™s not airborne,â€ says Marr. â€œHistory will not look upon them kindly.â€
With many countries around the world taking their steer on strategies to manage the pandemic (and other infectious diseases) from the WHO, taking so long to recognise airborne transmission meant many countries didnâ€™t take steps to mitigate this mode of transmission, and sadly that meant more cases and more deaths, said Noakes.
In line with other inequalities, people from deprived areas and households were hit the hardest by this pandemic due to their heavy exposure to the virus, catalysed by the typically overcrowded conditions they live in, the type of work that they do and the type of transport that they take.
In the UK, for instance, these disadvantaged communities tend to have limited access to green space â€” and disproportionately include people from minority backgrounds, who are already more hesitant to get vaccinated. This confluence of factors has meant such communities have been much more likely to be hospitalised, and in turn, die, said Dr Zubaida Haque, executive director of the UK charity The Equality Trust.
â€œThe fact that this is an airborne virus has massive implications,â€ Haque says. â€œFor one, we know that Black and ethnic minority people [in the UK] are much more likely to live in overcrowded housing compared to their white counterparts.â€
Up to one in three Bangladeshi families, about 20 percent of Pakistani families, and roughly 15 percent of Black African groups live in overcrowded housing. People from Chinese and Indian backgrounds score somewhere slightly lower on that scale â€” but itâ€™s still much higher than the rate for white British households, which is 2 percent, Haque explained.
â€œThat means more people in fewer rooms and less space, which means that the virus will spread much quicker. It also means that people canâ€™t self-isolate properly,â€ she says.
â€œYou realise that although weâ€™re all facing the same storm, we werenâ€™t in the same boat. Itâ€™s devastating, right? Inequality in this pandemic has meant the difference between life and death.â€
Ventilation needs the same push as vaccines
Occasionally, Noakes goes back to look at the first paper she worked on back in April 2020 on what was known about transmission and what to expect at the request of the UK government scientific advisory group. â€œNearly everything we said in there is still right â€” some of it has changed because we learned new things about the virus, but the basic principles [of transmission] are all in there,â€ she says.
â€œThough I still couldnâ€™t tell you the exact breakdown of how much transmission happens from the smallest aerosols through to the largest ones, whether itâ€™s close range or far field, but I think Iâ€™m much more confident that inhalation is the major route, no doubt.â€
Prather, meanwhile, wonders how much worse things could have been had she and her peers not poked and prodded the WHO into diluting their hard stance against airborne transmission.
â€œIs there confusion, still?â€ she asks. â€œYes, unfortunately. You know that because when you walk into a business you see hand sanitiser right there front and centre and no oneâ€™s wearing masks. So that tells you the general public doesnâ€™t get it as much as they could or should.â€
And so, two years on, we still donâ€™t have good public insight around airborne transmission, or the vital importance of ventilation. But things are changing â€” and this band of outsiders is determined to provoke a shift in standards in ventilation requirements in line with the transformation in the 1800s, when cities started organising clean water supplies and centralising sewage systems.
That means contending with a legacy of buildings worldwide that donâ€™t just have inadequate ventilation, but fail to meet basic building standards. Then there are others that have been built to conserve energy and prioritise comfort over ventilation, and the hope is that the experience of this pandemic could pave the way for investments in schools, workplaces and homes to improve air quality by revamping the built environment.
â€œI would love to see the same action on ventilation and environment as weâ€™ve seen on pharmaceutical interventions [such as vaccines and drugs],â€ says Noakes.
â€œWe can highlight the benefits, we can highlight the challenges and the complexities of things like ventilation â€¦ but we canâ€™t make it happen,â€ she adds, with an air of resignation.
â€œAnd you know, it would be lovely to say, well, â€˜Letâ€™s solve them all.â€™ But the cost of solving them all is going to be enormous. And somebody has got to decide whoâ€™s going to stump up that money to do it.â€
Still, Noakes is heartened to see ventilation now being increasingly discussed in the mainstream media alongside another challenge facing humanity: the climate crisis. â€œ[Today] there is a widespread recognition that we need to rethink all of our buildings and transport vehicles to not just address climate change,â€ she says, â€œbut also to ensure they provide healthy environments for the people in them.â€