- Dr Jonathan Fluxman
Its not only about social distancing: the importance of airborne spread of Covid-19
Updated: Jul 25, 2020
The spread of Covid-19 is generally not well understood, in particular the way it spreads indoors by means of airborne micro-droplets, so called aerosol spread. This has major implications for how we respond to the pandemic, as lockdown is being eased and people are starting to mix together again in significant numbers as they return to work and public spaces. This article discusses airborne transmission in detail and emphasises that an awareness of all of the risk factors for spread is important if we are to keep safe, especially in enclosed indoor spaces.
It should be noted that there is still disagreement over the role of aerosol spread of Covid-19, which is explored in detail in a companion article here. However the evidence is now very convincing that this type of spread plays a major role in indoor transmission.
3. Routes of infection
4. Dose of infection, time and distance
6. Close contact
7. Speaking + graphic
8. Laughing, shouting and singing
9. Coughing and sneezing
10. Aerosol rich environment + videos
11. Exercise and work of breathing
12. Asymptomatic spread
13. Spread in the home
15. Toilets and bathrooms
16. Shops and supermarkets
17. Indoor sports
18. Restaurants and chefs + graphic
19. Pubs and bars
20. Workplaces and offices + graphic
21. "Covid-safe" return to work
22. Walking, running and cycling
23. Outdoor sport
24. Public transport
25. Taxis and minicabs
26. Security guards
27. Face coverings
29. Risk factors + graphic
30. Risk factor chart
Official advice rightly says social distancing is very important to prevent the spread of Covid-19. But there are other important things which are not being done, in particular to minimise aerosol transmission, which puts the public and working people at risk. We need to know the different ways Covid-19 can spread, in order to better protect ourselves, our families and our communities.
In any situation the risk of getting infected with Covid-19 depends on:
Anyone can be infected; asymptomatic spread is common
The distance you are from other people
The number of people in any given place
The amount of time you spend near to them
What activity people are doing while in the space, eg sitting quietly, talking loudly, or coughing.
The size of the space you and others are in
The ventilation and airflow in the space you are in
Are people wearing face covering or mask?
Surface spread by touching.
Think about all these risk factors whenever you leave home, when you go shopping, when you travel, and when you’re at work. An easy way to remember them is this:
And Do Not Talk Aloud So Very Much Sam.
This document looks at all these risk factors in detail, so please read on if you want all the detail and the evidence. It considers how they apply to a variety of daily activities, places and occupations. There are two appendices at the end with colour-coded risk factors, as a visual summary.
Covid-19 is spread by people, but the risks factors for spread, in the home, in the local community and at work are not well understood. Official advice and therefore public understanding of practical measures to reduce transmission is more or less limited to social distancing and handwashing. There has been recent advice about wearing face coverings, which seems to be growing in emphasis, but the messaging has been contradictory and confusing for people. There is an urgent need for a better understanding of routes of spread of Covid-19 so that people can make rational, well informed decisions during their day-to-day activities.
Professor Erin Bromage has written an excellent, clear and practical article (*) which provides a framework for this understanding, which underlines the fact that it is not only about social distancing, as important as that measure is. This article looks at Professor Bromage’s paper, and a number of other issues and scenarios. There is added urgency to this, given that lockdown, which has stopped exponential spread of the virus, is being progressively eased by the UK government. However there is still a worryingly high rate of ongoing daily transmission. Many people therefore feel this is premature, and unsafe, but it is happening. The more informed we are therefore, the better we will be able to judge for ourselves the risks involved in doing what we are being asked to do, be it go back to work, or send our children back to school, and the better we will be able to demand the things we need to keep us safe. Unfortunately, official guidance about how to “be Covid safe” when returning to work is lacking is important respects, crucially with regard to preventing aerosol spread of Covid-19, which is a major route of viral transmission indoors. There are still gaps in our knowledge, including transmission risks in children, and the scenarios discussed here illustrate risk factors rather than provide fool-proof answers. It is written at a time when Covid-19 has devastated this country, and there is tragically still a long way still to go. The absence of widespread testing in the UK means there is no certainty about the level of infection in our communities, but it seems clear that it is still high, the best estimates are between 2,300 and 4,300 a day as of 20 June (42). This has not changed materially for the last 2-3 weeks, so the R0 value is near one and exceeded one in the north west of the country recently (35). There have also been recent outbreaks in Leicester and in meat processing plants in Yorkshire and Wales. The fact of high ongoing transmission, and that asymptomatic spread is common means that our decision-making needs to assume that anyone we encounter is potentially infectious, and that there is more to staying safe than just keeping our distance from other people.
** Data from Independent SAGE up to 2 July:
* “The risks - know them – avoid them” by Erin Bromage, Professor of Biology and Comparative Immunology at Massachusetts Dartmouth University. A number of sections of the paper have been included here. All statements of fact have been checked and referenced. The full article is here: https://www.erinbromage.com/post/the-risks-know-them-avoid-them. All other material has also been checked and referenced. References are numbered in brackets and listed in Appendix 1.
3. Routes of infection
The coronavirus (also called SARS-CoV2 and Covid -19) spreads from one person to others in four main ways:
Respiratory spread by live virus particles contained in tiny droplets which are breathed out by an infected person, and which mostly fall to the ground within about 2m. But things like coughing and sneezing can project droplets a lot further.
Respiratory spread by viral particles which are suspended in the air (aerosols) which can lead to infection in enclosed spaces. (1) (4) See also figure 1 below.
By direct contact with someone who is infected, such as shaking hands and then touching your mouth, nose or eyes, or by hugging or kissing,
By touching surfaces which have live virus on them and then touching your mouth, nose or eyes (so called fomite spread).
Droplet spread is the major route of spread when people are near to one another, while aerosol spread is important in in enclosed and confined spaces. Fomite spread is important in situations where there is a lot of traffic of people, and many touch surfaces, such as public transport.
4. Dose of infection
As Professor Bromage explains, in order to get infected you need to be exposed to an infectious dose of the virus. We don’t have the evidence for Covid-19 itself, but from infectious dose studies with other coronaviruses, it appears that relatively small doses may be needed to get infected, as we know Covid-19 spreads very easily. Experts estimate that between a hundred to a few thousand virus particles are enough to cause infection; we can therefore use a figure of about 1000 infectious viral particles as an estimate. (2) (3) This still needs to be confirmed, but we can use that number to demonstrate how infection can occur. Infection could therefore occur through 1000 or more infectious viral particles inhaled in one breath or from rubbing your eye, or 100 viral particles inhaled with each breath over 10 breaths, or 10 viral particles with 100 breaths.
Time spent near someone who is infected
So it is not only the amount of virus you are exposed to but also the time you spend in an environment which contains virus. For example, if you share an indoor office all day with someone who is infectious, you can get infected even if you sit 4 or 5m away, as you will be breathing in small numbers of viruses over several hours which can add up to more than the 1000 particles infection threshold.
Distance from the infected person – social distancing
The 2m rule works because most of the virus is contained in droplets which fall to the ground nearby after being breathed out by an infectious person, so a short encounter with someone who is infected 2m away is very unlikely to expose you to enough virus to get infected. (see figure 1 below) Social distancing will protect you during a brief indoor exposure to an infected person because there is not enough time to achieve the infectious viral dose when you are standing 2 metres apart. Social distancing works outside because the wind and the infinite outdoor space dilutes and disperses the virus particles, preventing us from breathing in enough particles to get infected. However social distancing does not work if you are in an enclosed space with an infected person for a longer period of time, due to aerosol spread of the virus.
WHAT PEOPLE ARE DOING IS ALSO IMPORTANT
5. Breathing quietly
As Professor Bromage says, most of the respiratory droplets breathed out are low velocity and fall to the ground quickly. Due to the low exhalation force with each breath, droplets from the lower respiratory areas (which contain much more virus, compared with the upper airway) are not expelled, and the droplets released from breathing therefore only contain low levels of virus.
We don't have information for Covid-19 yet, but studies of the influenza virus have shown that a person infected with influenza breathes out up to 33 infectious viral particles per minute (1). If we assume, say, 20 viral particles are released each minute into the environment, even if every virus ended up getting absorbed (which is very unlikely, because that means that every virus ends up inside the airways or mucous membranes and penetrates into cells and replicates), to get infected you would need to be in that environment for 50 minutes (1000 viral particles divided by 20 per minute = 50 minutes). So, a short period of time in the same space with an infected person who is breathing quietly, is low risk for infection. This risk can be lowered further by wearing a face covering.
6. A “close contact”
Public Health England (PHE), for the purposes of contact tracing, i.e. contacting people who might have become infected by someone known to have the virus, defines close contact as involving either face to face contact or spending more than 15 minutes within 2 metres of an infected person (Ref 5). The exposure to virus x time formula is the basis of contact tracing. From the above we can see this time period is about right, as long as that person is breathing normally. Speaking, laughing, coughing etc however, would make the time period for infection potentially much shorter – see below.
This increases the release of respiratory droplets significantly, due to the greater respiratory effort, and the louder the speech the greater the number of droplets emitted. So it could only take a few minutes talking to someone face to face in an enclosed space to get infected.
In fact, speech droplets generated by asymptomatic carriers of SARS-CoV-2 talking normally, are increasingly considered to be a likely mode of disease transmission. (see later section about spread in a call centre in Korea). Highly sensitive laser light- scattering observations have revealed that loud speech can emit thousands of oral fluid droplets per second, and in a few people tens of thousands (so called “super-emitters”). In a closed, stagnant air environment, they disappear (by dehydration and disintegration) after a few minutes. This means that there is a substantial probability that normal speaking causes airborne virus transmission in confined environments. (4) These aerosolised microdroplets can be thought about like the odour of perfume, which can be smelled some distance away when the particles enter the nose.
Figure 1 Spread of Covid-19 by droplets and aerosols (with thanks to the One Heart Clinic https://www.oneheartclinic.com/) Aerosols are created when talking, shouting, laughing, singing, exercising as well as when coughing and sneezing.
Researchers in one paper estimated that a person standing and speaking in a room could release up to 114 infectious doses of virus per hour. (45)
8. Laughing and shouting
If an infected person laughs or shouts (or sings – see below), even more release of virus occurs, because deep breathing occurs and a much greater volume of air and force is involved in expelling the air when laughing or shouting. So if you are in an enclosed space with someone doing these things, you could become infected quite quickly, even if you are more than 2m away. This is why gatherings are so dangerous for spread, especially when they involve alcohol, which disinhibits behaviour, in addition to the natural tendency to talk loudly, laugh etc while we are with friends and family.
Similarly, singing produces respiratory droplets extremely well. Deep-breathing while singing and the greater force used in expelling the air through the vocal chords releases much more virus into the surrounding air and these travel throughout the space occupied by that person.
Professor Bromage points to the experience of a community choir in Washington in the US (6) as an example of the dangers of singing in enclosed spaces with others. Even though people were aware of the virus and took steps to minimize transfer of virus; e.g. they avoided the usual handshakes and hugs hello, there was hand sanitiser at the door, people also brought their own music to avoid sharing. Social distancing was apparently not rigorously followed during the practice session. The organisers also told choir members prior to the session that anyone experiencing symptoms should stay home. The choir sang for 2 ½ hours, inside an enclosed rehearsal hall which was roughly the size of a volleyball court (about 160 square meters). One person with cold-like symptoms infected most of the people in attendance. The long period of time of exposure, the enclosed space and the forceful breathing from singing by everyone ensured that people were exposed to enough virus for infection to take place. Over a period of 4 days, 53 of the 61 choir members became infected, and two died.
9. Coughing and sneezing
Coughs and sneezes expel thousands of droplets at high speed from the mouth and nose; some of the droplets can travel as far as 8 meters. Sneezing may produce as many as 40,000 droplets at speeds over 100mph, while coughing can produce up to 3000 droplets (7), at slower but still high speeds relative to breathing So both can project virus easily across a room in a short time. The viral loads may be very high: one study calculated that there are on average about 7 million Covid-19 virus particles per ml of oral fluid. (4). Each cough can generate 1ml or more of fluid, therefore potentially very high numbers of viral particles could be expelled with each cough or sneeze (8). Not all of these are likely to be infectious but being in an enclosed space with someone coughing for a period of time is high risk.
After a sneeze the largest droplets rapidly settle onto surfaces within 1 to 2 m away from the person. These are infectious if touched and transferred to the face by someone else. The smaller and evaporating droplets are trapped in the turbulent puff cloud, remain suspended, and, over the course of seconds to a few minutes, can travel the dimensions of a room and land up to 6 to 8 m away (9).
Again, the reason many more virus particles generated by coughing and sneezing is because of the respiratory effort involved: they involve taking a deep breath and then expelling a large volume of air rapidly with great force. Due to the very high exhalation force and large volume of breath expelled, viral particles from the lower respiratory areas (which contain more virus, compared with the upper airway) are expelled into the air.
If you are face-to-face with a person who is coughing or sneezing, and that person do so straight at you, you will receive many times the infectious dose of virus. But even not directed at you, many aerosolised virus particles hang in the air, filling the room with infectious viral particles, creating an "aerosol rich environment". All you have to do is enter that room within a few minutes of the person who has been coughing/sneezing and stay there for a period of time and you may inhale enough virus to establish an infection.
Sneezing is not common with Covid-19 but coughing is and it can be frequent and persistent. This is one reason why it is so important for infected people to isolate at home. It is also why if we are out and about and feel we’re about to cough or sneeze we should turn away from anyone else and cough or sneeze into a tissue, or into our elbow across our mouth and nose to reduce amount of virus being projected into the air around us. Remember you may feel fine but still be an asymptomatic carrier of the virus and we know that people can be very infectious in the day or two before they get symptoms. So do your utmost to control coughing and sneezing when other people are around, even if you feel fine, especially in enclosed spaces.
10. Aerosol rich environments
The concept of an "aerosol rich environment" is important to bear in mind in terms of risk. An infected person will create this in any enclosed space with poor ventilation. The smaller the space, and the longer the time this person spends in the space, the greater the amount of aerosolised virus there will be in the room air. If this person engages in any activity which generates a high output of virus, such as coughing, laughing, singing or exercising, the greater the amount of circulating virus there will be in the room. Such aerosol rich environments are high risk for spread.
These two video clips, from Japan and the US, demonstrate this quite well, and how important ventilation is in enclosed spaces:
https://youtu.be/vBvFkQizTT4 (whole video is good, see 4min 20 secs in particular)
11. Exercising and work of breathing
We have seen how the effort involved in breathing determines how much virus infected people project into the air around them. If we think about it the effort involved in breathing also determines how much air we breathe in. When we're breathing quietly we take in about 0.5 litres (500ml) of air with each breath from a radius approximately 10 cm from our mouths. (41) So with heavy breathing, say when we are doing physically demanding work, or exercising in an indoor gym, we take in much bigger volumes of air, around 3 or 4 litres with each breath. The rate of breathing also goes up from about 15 breaths per minute at rest to 40 or more breaths per minute during exercise. This means that we will draw in air from a bigger radius around our mouth with each breath and the amount of air breathed in will be much greater per minute (15 x 0.5 L = 7.5 L/min with quiet breathing, and 40 x 4.0 L = 160 L/min with hard work or exercise). So if the space has airborne virus in it, it is pretty clear that exercising will quickly draw in large amounts of virus and make infection likely in a short space of time.
If someone coughs, sneezes or is laughing loudly near you and you are in an enclosed space, holding your breath and quickly moving away will reduce the amount of virus you breathe in, although you may get virus on you hands, face and clothes. There is evidence with the influenza virus that breathing in aerosolised virus goes deep into the lungs to the alveoli (air sacs) because the viral particles are so small, and causes more severe disease in the lower respiratory tract as opposed to in the upper respiratory tract with larger droplet spread. (43)
12. Asymptomatic spread
High viral loads of SARS-CoV-2 have been detected in oral fluids of Covid-19 positive patients including asymptomatic people (4). A study in Nature Medicine showed that nearly half (44%) of the infections in a group of 94 people in Guangdong, China, were from people who were shedding the virus 2-3 days before they had symptoms. (10)
In another study of people living in the Italian village of Vó, in which about 80% of the population were tested twice within two weeks, 43% the population were found to be asymptomatically infected, showing no symptoms over the observation period of two weeks, while viral loads were equivalent in symptomatic and asymptomatic patients (Ref 11)
This has potentially very important consequences for the timing of measures to contain the virus both at an individual level and a community or population level: The authors of the Guangdong study state, “Significant presymptomatic transmission would probably reduce the effectiveness of control measures that are initiated (at) symptom onset, such as isolation, contact tracing and enhanced hygiene or use of face masks for symptomatic persons”.
PLACES AND ACTIVITIES
13. In the home
Most infections occur within households according to the WHO. In early March Dr Mike Ryan, executive director of the WHO's health emergencies program said "If you look, most cases …are in family clusters. That's been driving the epidemic." (14)
Spread within households is very common – a study in March in Wuhan in China (15) estimates 30% of household contacts will get infected. However not everyone was tested, only those showing symptoms, so the rate may have been higher. Another study (as yet not peer reviewed) in Guangzhou in China showed a lower rate 20%, with people over 60 being most at risk and those under 20 less so (16).
These high rates are not surprising: a household member contracts the virus in the community or school or work and brings it into the house where sustained close contact between household members occurs as part of normal every day family life. There is also sharing of kitchen and bathroom areas increasing fomite (by touching surfaces) spread. As we have seen a lot of transmission can occur before symptoms develop in the index case in the household. This makes it difficult to avoid spread in households by isolating, as this is obviously done only when symptoms arise. The Guangzhou study found that isolation of the infected person following the onset of symptoms, the infection rate reduced by about a third.
It is not clear what the housing conditions were in these studies, nor the socio-economic status of the subjects.
Once symptoms start, the person should ideally stay in one room, away from everyone, as much as possible, wear a face mask if around others and use a separate bathroom if possible. Personal items such as dishes, towels and bedding should not be shared. Household members who wash the laundry of the patient should wear disposable gloves and avoid contact with the items as much as possible.
However, isolation of the infected person is often difficult or impossible in poorer, deprived communities, where there is overcrowding (which is sometimes severe with several people living in one or two rooms), and sharing of kitchen and toilet and bathroom facilities with other people or families in multiple occupancy households.
Detailed self-isolation instructions are needed for example provided by Public Health England (PHE) (17) [these are out of date however - they do not include wearing of a face covering]. The advice from the European Centre for Disease Control (ECDC) is more comprehensive (18). It may be useful to discuss an isolation plan for all family members prior to any infection coming in the household and involve neighbours and relatives, for example possibly moving out vulnerable elderly family members if isolation measures in the house would be very difficult. However, for many families there is not much they can do and they remain at risk.
15. Toilets and bathrooms
As Professor Bromage says bathrooms have a lot of high touch surfaces, eg door handles, taps, sinks; and fomite (surfaces and materials) transfer risk in this environment can be high. It is advisable to personalise towels and wash cloths. Windows should be kept open in bathrooms to clear any aerosolised virus. Treat public bathrooms, which also have stalls with doors and locks, with extra caution due to lots of people using them.
Electric hand driers (*) have been shown to be potentially hazardous. Research published in 2014 concluded "Jet air and warm air dryers result in increased bacterial aerosolization when drying hands. These results suggest that air dryers may be unsuitable for use in healthcare settings, as they may facilitate microbial cross-contamination via airborne dissemination to the environment or bathroom visitors." (37) The high speed air currents pick up virus from people's hands (handwashing is often not 100% effective) and circulate it in the confined space of bathroom areas, which often lack adequate ventilation. This evidence has been presented several times to SAGE and Public Health England in April and May (38) (39) but the government has yet to recommend people stop using electric hand driers.
(*) With thanks to Dr Charlotte Fowler, a doctor of 27 years working as a senior consultant in a large central London teaching hospital. Dr Fowler has organised a petition to the Health Secretary about the government's lack of action to stop the use of hand driers. See here: http://www.change.org/StopCOVID19aerosols-SHUTDOWNelectrichanddryers
16. Corner shops and grocery stores
A lot of these have narrow aisles making social distancing impossible. As long as no-one is coughing, sneezing or shouting, the risk is probably low if the time spent in the shop is short. However if the shop has several people in it and if you spend some time shopping in the enclosed space of the shop, risk is higher. Shopkeepers and their staff are at relatively high risk due to the high footfall each day in shops and their being in the enclosed space for many hours. Several shopworkers are known to have died from Covid-19 and the true number is probably higher than the reported cases (19). Sales and retail assistants have twice the death rate of the general population according to recent ONS figures. (20) Ventilation will help but many shops don’t have this. The wearing of face coverings by everyone, customers and staff, is an important measure to reduce transmission.
These are safer than in the early days of the pandemic with panic buying and crowding at entrances prior to opening. There is now organised queuing outside and many only allow a limited number of people in at any one time. Supermarkets are also large indoor spaces with ventilation. However they are not risk-free as distancing is still not possible all the time in the aisles, and there is as yet no requirement on customers to wear a face covering before entering the store. Without these, coughing, sneezing, laughing etc will spread virus in the aisles potentially infecting others. Staff in supermarkets are at increased risk however; as they encounter many customers while working all day.
17. Indoor sports
Professor Bromage highlights how indoor team sports can be hazardous, as shown by a super-spreader event in Canada during a curling competition in early March. Even though it is in a large indoor space, curling brings players in close contact with each other in a cool environment, with heavy breathing for an extended period of time. This particular tournament resulted in 24 of the 72 people becoming infected. (21)
Individual indoor sports are less hazardous but it does depend on the number of players present, the size of the indoor space, the air ventilation and time spent playing. High energy games like squash in enclosed spaces are high risk.
Gyms and fitness centres would also appear to be high risk. There is a lot of high energy activity with deep breathing, both in terms of producing lots of virus and in terms of breathing in lots of air which may contain virus while exercising. Heavy exercise will result in volumes of air being breathed in and out, of about 20 times that of quiet breathing. There is also a lot of shared equipment and fomite spread is an obvious additional risk. Social distancing, even if successfully implemented, will not be sufficiently protective. One or two asymptomatic carriers who are working out vigorously could spread the virus throughout the gym space if this is enclosed without proper ventilation involving sufficient fresh air air exchanges per hour. Gym sessions are also usually a minimum of 30 minutes, often longer, so prolonged exposure time in an "aerosol rich environment" is another risk factor.
A report of an outbreak of Covid-19 in a restaurant in Guangzhou in late January and early February (22) is very instructive, demonstrating spread of the virus from a single asymptomatic carrier in a restaurant environment. The seating arrangements are shown in figure 2 below. The infected person (A1) had dinner with 9 friends. During the meal, which took about an hour, the asymptomatic carrier released low-levels of virus into the air from breathing. Airflow, from various airflow vents, was from right to left. The tables were about 1 metre apart. About half the people at the infected person's table became sick over the next seven days. 75% of the people on the adjacent downwind table became infected. Two of the 7 people on the upwind table were infected (probably by turbulent airflow). No one at tables E or F became infected, they were out of the main airflow from the air conditioner on the right to the exhaust fan on the left of the room.
Figure 2. Seating at Guangzhou restaurant showing location of index case and those subsequently infected.This is one part of a larger space which had another air conditioning unit.
Chefs are at high risk.
It should be noted that in the recent ONS figures, chefs have one of the highest death rates from Covid-19: three and a half times that of the average. Likely factors include working in the enclosed environment of the restaurant kitchen for long hours, inadequate ventilation, a very busy, high energy environment with a lot of footfall of staff and customers in and out. Restaurant kitchens are clearly a high risk environment at present in the UK.
19. Pubs and bars
From 4th July people will be able to visit pubs and bars as the government further eases lockdown. It has also reduced the social distancing rules from 2m to "1m plus". "One-metre plus" involves keeping one metre apart, plus wearing face covering, sitting side to side rather than face to face and increased use of hand sanitiser. This is worrying: maintaining distancing will be difficult, face coverings are impractical, and pubs and bars are often noisy with lots of laughing and raised voices. People will naturally turn to one another when speaking. Alcohol also disinhibits behaviour, people are therefore less likely to observe precautions. Furthermore, airborne spread is likely as pubs and bars are often not well ventilated, and government advice says merely windows and doors should be opened frequently "when possible". There have been outbreaks of Covid-19 reported in Florida in several bars which had opened up after lockdown, necessitating their closure again. Fifteen people in one group became infected after visiting a bar on 6 June. (40)
20. Workplaces and offices
Another very informative and very thorough study was of an outbreak in a call centre in early March in Seoul, South Korea (see figure 3 below). (23) A single infected employee worked on the 11th floor of a building; that floor had 216 employees. Employees did not generally move between floors, and they did not have an in-house restaurant for meals. Over the period of a week, 94 of those people became infected (43.5%: the blue chairs in figure 3). Three other people on different floors were also infected. Note how one side of the office was mainly infected, but there were others at some distance away on the other side, who also became infected. While the number of people infected by different routes, i.e. respiratory droplets, aerosol or fomite transmission (door handles, shared water coolers, elevator buttons etc.) is unknown, this shows that being in an enclosed space, in a crowded office environment and sharing the same air for a prolonged period is very high risk for exposure and infection. Interestingly, even though there was interaction with other people on different floors of the building in elevators and the lobby, the outbreak was almost entirely limited to a single floor, which indicates that the duration of interaction (or contact) was likely the main reason for further spread. This clearly has major implications for office working while the rate of infection in the community is high, or unknown, as in the UK at present.
The follow up of patients during the study was also meticulous and showed other interesting findings. Eight of the 97 people infected were asymptomatic at the time of testing, four of whom developed symptoms later in the 2 week follow up monitoring period. All the household contacts of patients with confirmed infections were also investigated, tested, and monitored for 14 days after testing positive, regardless of symptoms. Of 225 household contacts infections occurred in 34 household members who had contact with symptomatic case-patients, i.e. a “secondary attack rate” of 16.2%. None of the 17 household members of the asymptomatic case-patients developed symptoms or tested positive after 14 days of quarantine, underlining the importance of finding asymptomatic carriers early who can then effectively isolate from other family members.
The authors concluded that “Extensive contact tracing, testing all contacts and early quarantine blocked further transmission….”
Figure 3. Floor plan of the 11th floor of building X, site of a coronavirus disease outbreak in Seoul, South Korea, 2020. Blue colouring indicates the seating places of persons with confirmed infection.
21. Government guidance on return to work in offices
While parts of this guidance is sensible and helpful, such as risk assessments, home working when possible and cleaning and sanitising of the workplace to prevent fomite spread, there are some serious omissions from the guidance. In particular there is almost no consideration of aerosol spread of Covid-19 and the related issues of (a) time spent in potentially infectious environments and (b) the need for effective ventilation. The guidance is overly reliant on social distancing, and pays very little regard to the role and technical requirements of ventilation to prevent transmission of infection (32). The advice on the benefits of wearing face coverings is particularly disappointing – they are described as “marginally beneficial as a precautionary measure”. However this may change as it appears the government is increasingly keen on face coverings as a measure to mitigate risk when easing lockdown.
It appears that the aim of reducing transmission of infection has been set aside in the guidance for some work areas. The guidance for offices and contact centres (33) in the section for workplaces and workstations states the “Objective: To maintain social distancing between individuals when they are at their workstations”, whereas for meetings it says “Objective: To reduce transmission due to face-to-face meetings and maintain social distancing in meetings.” Should the objective not be to reduce transmission everywhere and at all times? The guidance also advises back-to-back and side-to-side seating arrangements “Only where it is not possible to move workstations further apart”. As the call centre in Seoul outbreak shows all too clearly, 2m distancing and sitting back-to-back will not to prevent spread within an enclosed space occupied over several hours.
22. Outdoors: pedestrians, bike riders and runners
The risk of getting infected by other people outdoors is low. From first principles it is reasonable to assume that few viral particles will successfully transfer from one person to another, as the time of the encounter is very short (a few seconds), and any virus particles will be widely dispersed in the open air. If distancing is observed and both people are wearing face masks the risks are even lower.
An article in Vox in 24 April 2020 quoted a virologist at Columbia University, Angela Rasmussen, as follows, “The risks of virus transmissibility in the air outdoors is likely quite low ….., although this risk hasn’t been definitively measured. Outside, things like sunlight, wind, rain, ambient temperature, and humidity can affect virus infectivity and transmissibility, so while we can’t say there’s zero risk, it’s likely low unless you are engaging in activities as part of a large crowd (such as a protest). Solitary outdoor exercise is likely low-risk.” (24)
People exercising by running or cycling will be breathing more deeply so if they are infected, they will project more virus into the air around them. Their relative speed to a passer-by however is high, so the encounter time is very short. Coughing, sneezing and spitting (especially after “hawking”) are high risk if the person does this near you and you then walk through the “plume” they have just produced as you pass them. Such actions should be actively discouraged and runners and cyclists should like everyone keep to the 2m rule when passing from behind or in front.
The viral load produced, encounter time, distance between people and air circulation are the important factors to consider. Outdoors these are very favourable most of the time. Social distancing is still important and wearing a face covering also reduces risk.
23. Outdoor sports
Individual sports like tennis and golf are low risk for the reasons described above. Careful physical distancing is important though, given that players may be breathing heavily at times.
Team sports however are potentially hazardous as players come into close contact with team mates and opponents, and if anyone is infected there is risk of transmission due to heavy breathing from exertion and close physical contact.
Mass outdoor sporting events before lockdown involving thousands of spectators were very hazardous. The Cheltenham Gold Cup horse racing event in mid-March here in the UK, and the football match in Milan on 19 February were probably “super-spreader” events. Both were outdoors, but the large crowds of people, in close contact, engaging in excitable behaviour, all facilitated spread, and underline how being outdoors on its own is not enough to protect people from infection. The Milan football match has been likened to a “biological bomb” and is thought to have contributed significantly to the dreadful death toll in northern Italy.
24. Public transport
This is a known high risk for spread of respiratory infections among passengers, due to overcrowding, multiple touch surfaces, enclosed spaces with little ventilation, and prolonged journey times. A study in 2009 showed recent bus or tram use within five days of symptom onset was associated with an almost six-fold increased risk of consulting a GP for an acute respiratory illness. (25) Public transport and healthcare settings are common sources of contact between infected individuals and other people.
The TUC calculated in 2018 that average commuting times for working people on public transport are well over two hours each day by rail, an hour and 40 mins by tube and an hour and 20 minutes by bus each day. Strikingly, it also found that BAME workers had longer commutes by about 10 mins each day. (26)
Transport staff are also at significant risk due to encountering very large numbers of people each day. The recent ONS figures showed that bus and coach drivers have 2.5 times the average death rate from Covid-19. At least 33 bus drivers have died of Covid-19 in London; and many are unhappy about safety measures. One stated “We are in a capsule with all that Covidy air circulating around us.” (27) This underlines the point that social distancing alone will not make public transport safe; the enclosed space is inherently risky even with a small number of passengers at any one time. The government’s advice on social distancing in public transport lacks clarity, is advisory only and appears to seek to weaken the 2m rule (which is being questioned, it appears to enable more businesses to open), stating “… (try) to keep 2 metres away from people, where possible, as a precaution. However, this is not a rule and the science is complex.” (28) [page 8 Guidance for Transport Operators]. As of 15 June wearing a face covering on public transport is now mandatory which is a welcome measure. Face coverings will reduce spread, as would keeping open all windows on buses and trains. The same is true of taxis, minicabs and coaches – all passengers and drivers should wear face coverings and all windows should be left open.
Station staff are also at risk from encountering large numbers of people. There are disturbing reports of a woman working at a Victoria Station in London who apparently died of Covid-19 after being spat at by a member of the public. (29)
Official advice on improving ventilation is mentioned in the government’s guidance, for transport operators, as follows: “Organisations should consider how to increase ventilation and air flow. Where possible, transport operators and businesses should ensure that a fresh air supply is consistently flowing through vehicles, carriages, transport hubs and office buildings.” The advice lacks any detail however of the technical requirements for effective ventilation for this highly infectious pathogen, as well as lacking clear direction or requirement for compliance. There is also no mention in the advice of journey times. Overall the guidance will not reliably lead to safe conditions for travel on public transport.
25. Taxis and minicabs
These are high risk, because of the small enclosed space occupied by the driver and passenger/s. This is underlined by the recent ONS figures, which showed that male taxi and minicab drivers, and chauffeurs had 3.5 times the average death rate from Covid-19. Very many cab drivers are from Black or Asian communities, who have suffered 2-4 times the death rate of whites from the disease. There are numerous media reports of the tragic deaths of drivers, some of whom felt they had to keep working to support their families. Some cab companies are introducing screens between drivers and passengers, and some firms have policies that passengers must sit at the rear in the seat opposite the driver. Official advice about travel in taxis emphasises social distancing, and facing away from other people in queues where that is not possible. It also warns of fomite spread from touch surfaces. However there is the same poor advice about face coverings as in the other guidance and there is no mention of ventilation. Keeping all the windows open is an important protective measure in all cabs. The taxi firm Uber have recently introduced a “no mask, no ride” policy for passengers, which is to be welcomed.
26. Security guards
Men working as security guards have a shockingly high death rate from Covid-19, i.e. 4.5 times the average, the highest of all job categories. It is not entirely clear why, but they have several known risk factors: many are from also Black or Asian, they are exposed to a lot of passers-by at the entrances and inside shops and other premises all day, they spend long periods indoors in enclosed spaces with lots of members of the public, and they may need to have close contact with other people when carrying out their duties. There are reports of security guards being threatened by being spat and coughed at by members of the public. Strict social distancing for security guards would seem to be important therefore, and once again wearing a face covering will limit spread from infectious people. Some security guards have been given face shields to counter the spitting hazard.
27. Face coverings
Face coverings work because they reduce aerosol spread by trapping the tiny droplets containing virus as they leave the mouth and before they evaporate and the viral particles become suspended in the air, i.e. aerosolise. A recent paper in the Annals of Internal Medicine states, “Cloth does not stop isolated virions (virus particles). However, most virus transmission occurs via larger particles in secretions, whether aerosol (<5 µm) or droplets (>5 µm), which are generated directly by speaking, eating, coughing, and sneezing; aerosols are also created when water evaporates from smaller droplets, which become aerosol-sized droplet nuclei. The point is not that some particles can penetrate but that some particles are stopped, particularly in the outward direction. Every virus-laden particle retained in a mask is not available to hang in the air as an aerosol or fall to a surface to be later picked up by touch.” (34) The paper goes on to say, in the fight against this deadly pandemic every tool we have should be used.
Each day it seems there is a new paper demonstrating the effectiveness and importance of face coverings for the general public. This recent paper from Zhang et al in the Proceedings of the National Academy of Sciences states, “…airborne transmission is highly virulent and represents the dominant route to spread the disease. By analyzing the trend and mitigation measures in Wuhan, China, Italy, and New York City, from January 23 to May 9, 2020, we illustrate that the impacts of mitigation measures are discernable from the trends of the pandemic. Our analysis reveals that the difference with and without mandated face covering represents the determinant in shaping the pandemic trends in the three epicenters. This protective measure alone significantly reduced the number of infections, that is, by over 78,000 in Italy from April 6 to May 9 and over 66,000 in New York City from April 17 to May 9. Other mitigation measures, such as social distancing implemented in the United States, are insufficient by themselves in protecting the public. We conclude that wearing of face masks in public corresponds to the most effective means to prevent interhuman transmission, and this inexpensive practice, in conjunction with simultaneous social distancing, quarantine, and contact tracing, represents the most likely fighting opportunity to stop the COVID-19 pandemic.” (36)
Government advice about face coverings has unfortunately been confusing and contradictory. For several weeks the government declined to recommend their use for the public, stating evidence for their effectiveness was weak, and they were concerned that people would not follow other important control measures like social distancing if they wore masks. The advice changed when the prime minister said on 30 April “I do think face coverings will be useful. Both for epidemiological reasons but, also, for giving people confidence that they can go back to work”, and 2 weeks later face coverings were incorporated into official advice on return to work in various sectors of the economy. They have now been made mandatory on public transport as of 15 June. What is worrying now however is that arguments are being made that the use of face coverings will make it safe to reduce social distancing from 2m to 1.5m or even 1m.
This contradictory and changing advice is very regrettable as it makes it difficult for the public to have confidence in face coverings as an essential public health measure to keep us all safe. This can be seen by the generally low level of face covering wearing by the general public when they are out and about.
The aerosol route of spread of Covid-19 needs to gain wider recognition as a matter of urgency. If we are going to successfully combat the pandemic we must all adopt additional measures like face coverings and avoid high risk environments like enclosed indoor spaces with poor ventilation, until much less virus is circulating in the community and we have an efficient test, track, isolate and support system in the country.
Social distancing rules protect you from exposure during brief indoor encounters with infected people, and from outdoor exposures. Indoors, there is not enough time to achieve the infectious viral load when you are standing 2m apart for short periods of time, and outdoors the open air dilutes viral load to a negligible number, and the effects of sunlight, heat, and humidity on viral survival, all serve to minimize the risk when outside.
Covid-19 transmission is mostly an indoor phenomenon. A study (not yet peer reviewed) of outbreaks of Covid-19 involving 318 small clusters of cases showed all but one occurred indoors (31). Most were in the home or involved public transport. Sharing indoor space is the common factor, which is why measures to deal with aerosol spread are so important, which means face masks and proper ventilation, alongside avoiding crowded enclosed spaces.
Rely on your own judgement: assess each situation according to the risk factors described here (see colour charts in appendix 2) and if you think there is risk don’t take yourself or your family into that environment.
29. RISK FACTORS FOR SPREAD OF COVID-19
30. RISK FACTOR CHART
32. For example: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6072925/