It was 24 January, the day before Chinese New Year. A family of four, recently travelled from Wuhan to Guangzhou, were enjoying lunch in a busy, airconditioned fifth-floor restaurant.
Later that day, one of them developed a fever and cough. They went to hospital, and were diagnosed with COVID-19. Within two weeks, four other members of their family, along with five other individuals who dined at the restaurant that fateful lunchtime, had also been diagnosed.
But the infected individuals at the other tables had had no direct contact with the index patient during lunch, nor had they had contact with anyone else infected with COVID-19 in the days before and after their diagnosis. The one thing connecting them all was the cool air blown from an airconditioning unit on the wall, which circulated the air across three tables, including the middle table where the index patient sat and ate.
A study of this outbreak, published in late April, was the first to describe possible airborne spread of SARS-CoV-2, where the transmission couldn’t easily be attributed to direct contact, larger droplets from a sneeze or cough, or contaminated surfaces.
Since then, there has been an at-times heated debate about airborne transmission of COVID-19 that has played out not just among scientists but in scientific institutions, on social media and the front pages of newspapers.
At stake was an effective public health response to the pandemic: if airborne transmission of COVID-19 was in fact of equal concern with surface and droplet transmission, failure to account for that would leave a gaping hole in health defences. Airborne transmission has implications for advice on physical distancing, mask-wearing, on PPE provision for healthcare workers, on ventilation systems in public spaces, even on building design.
But uncertainty around this question is evident in the reluctance of organisations such as the World Health Organisation, US Centers for Disease Control and governments to explicitly address airborne transmission in their communication about the virus. And the urgency of the situation is revealed by initiatives such as the open letter to the WHO, signed by 239 scientists from around the world on 6 July, calling on WHO and other health organisations to recognize the potential for airborne spread of COVID-19.
The challenge in getting a clear answer to the question of what role airborne transmission plays in the spread of COVID-19 is that it’s essentially impossible to do a randomised controlled trial to study it, says Professor Lidia Morawska, an expert on air quality and aerosol science at the Queensland University of Technology. “Therefore, we need to rely mainly on prospective studies, particularly in hospitals where we know that there’s a source, we know that there are infected people, and therefore we conduct the sampling in the air, on the surfaces and so on,” Morawska says. “And we find the virus in the air.” Then there are the case studies, such as the Chinese restaurant outbreak, the choir practice outbreak, and the bus trip.
Part of the issue stems from confusion about what is meant by “airborne”, says Associate Professor Hassan Vally, infectious disease epidemiologist at LaTrobe University. “Droplet spread means that you project out a large droplet that is big enough that it falls to the ground, and so that’s why you have that distance of 1.5 metres,” he says. “But when we talk about airborne transmission, we’re talking about transmission that’s occurring in these smaller droplets that don’t fall to the ground – they can stay suspended in the air.”
Moreover, these smaller droplets can remain suspended for a long time, and preserve enough live virus that they could potentially infect someone who inhales them.
This leads to a second point of confusion, which is terminology: what are droplets, what are aerosols, and what is the difference?
Morawska says in the world of aerosol science, the term aerosol describes liquid or solid particles of any size, suspended in a gaseous medium such as air. A droplet specifically refers to a liquid particle. There are no size limits set on a droplet in aerosol science, but “in medical sciences aerosol is small, droplet is big,” she says.
If so, where is the line drawn between the two? Again, Morawska says medical science seems to have picked an arbitrary cut-off point between the two, of five micrometres. The issue at stake is: when is a droplet (or large aerosol) large enough to fall to the ground?
There’s not a lot of research on this, but Morawska says particles that remain suspended in the air seem to range from around 1-10 micrometres in size, and these small droplets or aerosols able to linger in air currents potentially for hours without falling to the floor.
The other issue with these smaller droplets is their source. Larger droplets, such as those expelled with a cough or sneeze, or generated during very excited speech, tend to be generated from the mouth, says Morawska, where there isn’t as much virus. “What research on this virus had been showing is that the highest viral load is in the smallest size of particles [from] deep in the lung, not from the mouth,” she says.
The third question then is: how far do these small aerosols spread? From early in the pandemic, the public health advice has been to maintain a distance of 1-2 metres – depending on which country you’re in – to avoid encountering infectious particles from another person. That distance was based on research done in the 1930s by W. F. Wells, an “Instructor in Sanitary Science” at the Harvard School of Public Health, whose experiment suggested that most droplets that came from people’s mouths during coughs and sneezes succumbed to gravity within around 3 feet – just shy of 1 metre. But those experiments didn’t – and probably couldn’t, given the technology of the day – look at the much smaller particles that are now causing concern: the ones that are ejected during normal speech and even breathing.
Dr Manouk Abkarian, a researcher at the Center for Structural Biology at the University of Montpellier in France, and the French National Centre for Scientific Research, and colleagues recently used laser light to study air movement during speech, to see how far these tiny particles might travel.
They discovered that exhaled air travels half a metre in just a fraction of a second, but air expelled by the plosive sounds of speech – the consonants p or b, for example – quickly spreads to at least 1 metre, and multiple plosives in a sentence can propel that air beyond two metres in what they describe as a “train of puffs”. Those puffs could also carry invisible, virus-laden particles in the 1-10 micrometre range.
“When someone sneezes on you, it’s pretty visible,” Abkarian says. “But if someone tells you, ‘pass me the pepper, please’, you are not thinking that you are putting yourself in danger.”
Abkarian’s work suggests there was no magical barrier at the 1 or even 2 metre point, where these potential infectious particles cease to become a threat. “It’s telling you that there are no simple rules,” he says. “If you give a distance, you have to give a time.”
Given the accumulation of evidence from laboratory experiments and case studies, Vally believes there’s now no question that, under some circumstances, SARS-CoV-2 can be aerosolised and can be transmitted via air.
But this is just one half of the puzzle. The other, and perhaps more contentious question, is whether airborne transmission is an important route of transmission in this pandemic.
Some evidence for that comes from observations of the seasonality of COVID-19, says Dr Julian Druce, head of the Virus Identification Laboratory at the Doherty Institute in Melbourne.
The peaks and troughs of a respiratory virus over the course of a year can give clues about its main routes of transmission. For example, the influenza virus is largely a winter event, because people are forced indoors, bringing them into closer proximity to each other, so there is more opportunity for droplet or aerosol – both airborne – transmission.
In contrast, the common cold is generally a year-round phenomenon, albeit with an increase during winter. “That suggests there’s fomites – as in things we touch: surfaces, door handles, tram rails etc,” Druce says. “People have just blown their nose and then their goop goes onto whatever that surface is because they’ve been manipulating a gunky tissue.”
But with COVID-19, which is yet to hit its first official birthday, that pattern hasn’t clearly revealed itself. “With a new virus, we don’t yet have a picture of seasonality, [of] what’s the natural cycle of this virus.”
There are early signs of seasonality that does imply greater spread when people are in close proximity, and there is more opportunity for airborne transmission. The virus surged in Europe in January and February during their winter, but its first peak in Australia – during late summer and early autumn – wasn’t nearly as significant as the second peak that hit Victoria during winter.
“Similarly in Europe in summer, they relaxed their restrictions and lived with it, though they had it pretty much under control,” Druce says. “But it’s now started getting a little bit cooler and it’s going badly out of control.” It suggests the virus is not only spread by fomites on surfaces, but by airborne routes.
It all comes down to probability, he says. What is the probability that a droplet will carry enough live virus to be a threat, the probability that that droplet will be inhaled by another person, the probability that a virus will find a cell in that person’s respiratory tract, and the probability that the virus will engage with the receptor on that cell surface and enter the cell?
“Probably nine times out of 10 you inhale a virus and it gets on the sticky mucus, and to all intents and purposes that’s pretty thick to a virus, and it doesn’t penetrate to get to the cell,” he says. “It’s all about those dynamics that link to transmissibility.”
If there is a reasonable probability that virus-laden aerosols can hang around in air currents for hours, what does that mean for indoor environments? It’s a big enough concern that among the 239 scientists who signed the open letter pleading with health organisations to acknowledge airborne transmission were a number of experts on indoor air quality and the built environment. Professor Richard de Dear, head of the Indoor Environmental Quality Lab at the University of Sydney, was one of them.
Something struck de Dear about the Chinese restaurant case study. The amount of outside air being introduced into the restaurant’s airconditioning system was very low – as little as 1 litre per second per person: around one-tenth of what would normally be expected.
“It was a very busy day in the restaurant’s calendar, so they had high levels of occupancy and low levels of ventilation, and that’s probably the worst combination,” he says. The air-conditioning system was also a split-system, which essentially blows air over a large cooling coil. But the air was simply recirculated from inside the restaurant, with very little fresh air being introduced.
“They were just projecting air outwards across the ceiling of the space, hitting the baffle wall and then air was coming back through the tables and back into the unit,” de Dear says. Three tables were in line with that single unit, and the middle one was occupied by the index patient.
If airborne transmission is possible – and de Dear is convinced the evidence points to that – it has major implications for airconditioning and building design. “The obvious changes will be the density of occupants: just how many people you can cram into an office floor, the number of square metres you have to allocate to each occupant,” he says.
He also argues it will be the death knell for what’s called “activity-based workplace design”, or what many know as “hot-desking” or “hotelling”: “That whole concept is completely redundant now; the way we organise space is going to have to change.” That workplace structure is unlikely to be missed, de Dear says, as survey after survey suggests most workers hate it. It may be that pandemics push office design back towards individual offices, more people working from home, and more virtual meetings. But it also means rethinking airconditioning and air-flow patterns, and moving back to natural ventilation using windows. None of this is easy, or cheap.
Which might explain why public health authorities and governments are increasingly emphasising the importance of mask-wearing. “The reason why the masks are encouraged – and they’re encouraged very loudly – is because this is personal responsibility,” Morawska says. “But a new paradigm of designing buildings and operating them? This is something which is really big.”