Behaviour of aerosols and their role in the transmission of SARS‐CoV‐2; a scoping review

Summary Covid‐19 has triggered an unprecedented global health crisis. The highly contagious nature and airborne transmission route of SARS‐CoV‐2 virus requires extraordinary measures for its containment. It is necessary to know the behaviour of aerosols carrying the virus to avoid this contagion. This paper describes the behaviour of aerosols and their role in the transmission of SARS‐CoV‐2 according to published models using a scoping review based on the PubMed, Scopus, and WOS databases. From an initial 530 references, 9 papers were selected after applying defined inclusion criteria. The results reinforce the airborne transmission route as a means of contagion of the virus and recommend the use of face masks, extending social distance to more than 2 metres, and natural ventilation of enclosed spaces as preventive measures. These results contribute to a better understanding of SARS‐CoV‐2 and help design effective strategies to prevent its spread.

the virus, which would occur when near an infected person.
Thirdly, through airborne transmission, by inhalation through the upper or lower airways of droplets and smaller particles that are suspended in the air for longer distances and times than droplet transmission. 4 SARS-CoV-2 spreads primarily through the respiratory particles that infected people emit when talking, coughing, breathing, or sneezing, wrapped in mucus or saliva forming droplets. The behaviour of these droplets in the air depends on their size; larger droplets precipitate before evaporating, splashing their nearby environment. 5 When these drops are larger than 5-10 μm in diameter, their emission has a range of 1 metre, so an infected person could infect another healthy person with whom they have close contact. 6 In addition, it can also be spread by coming in contact with the contaminated belongings and environment of an infected person, as the virus can persist on inanimate surfaces for days. 5 At the beginning of the pandemic, this pathway, surface transmission, was considered the main route of spreading of the virus, and airborne transmission was thought unlikely. 4 Consequently, and in the absence of a vaccine or specific treatment for Covid-19, prevention measures focused on mask use, social distancing and confinement, hand hygiene, and disinfection of surfaces. 7 However, the role of aerosols in the transmission of SARS-CoV-2 is increasingly relevant. Aerosols are dispersed liquid or solid particles suspended in the air, which may contain microorganisms, in which case they are called bioaerosols. 5 Aerosols have a size <5 μm and, being smaller and lighter than droplets, do not precipitate in the proximity of the infected person, but can remain in the air for an extended period of time. 8 Respiratory droplets are mainly composed of water with a solid particle inside such as microorganisms. The effect of evaporation, conditioned by relative humidity, temperature, and air speed, causes the droplets to quickly become aerosols up to a certain size, carrying a considerable effective viral load. 9 Aerosols with viral load can directly enter the host's airways by inhalation, thus spreading the disease. 10 Breathing, talking, coughing, and sneezing generate drops and sprays sliding from one individual to another. These actions mainly generate microparticles, except for sneezing, which provokes the emission of large drops with central tendency. 11 The least particleproducing actions are breathing, followed by talking and then coughing. 12 Singing increases emission rates and has been associated with cases of SARS-CoV-2 transmission in enclosed spaces. 13 The emission of particles through the mouth or nose depends on the initial speed with which they are dispatched. A sneeze can expel particles at high speed (about 50 m/s), but these dissipate quickly at a short distance (5 m/s at more than 0.6 m). When speaking, particles are emitted with a lower initial speed (3 m/s), though the airflow field has a range of 1 m (Figure 1). 12 The transmission mode affects whether the infection will be beginning in the upper or lower respiratory tract and, consequently, the severity and evolution of the disease. 10 Small aerosols are more susceptible to being inhaled deep into the lung, which would cause an infection in the alveolar tissues of the lower respiratory tract, while droplets become trapped in the upper respiratory tract. 14 The port of entry of SARS-Cov-2 in humans is the angiotensin-2 converting enzyme, that is present in type II pneumocytes of the lung and hair cells of the nasal membrane. From the biological point of view, airborne transmission of the virus is quite plausible. 12 Between 80% and 90% of the particles emitted in respiratory activities by an infected person are aerosols, with a size less than 1 μm in diameter. 8 In addition, the particles emitted by the cough of an infected person rapidly decrease in diameter, to half of their initial volume due to the loss of water by evaporation. 8 That is, an infected person is surrounded by a nebula of aerosols generated by their own breathing. Studies have described how pathogens are most often found in small particle aerosols (<5 μm in diameter) that are airborne and breathable. 4 Therefore, a large number of infectious particles with viral load circulating the air could be deposited in the nasal airways, and even host exposure can occur hours later and in the absence of the infected person. 8 An aerosol is a particle that is subject to the aerodynamics of the gas in which it is found, so environmental conditions such as humidity, temperature, and ventilation can accelerate the transmission of aerosols, thus contributing to the spread of the disease. 15 Aerosols with a small concentration of the virus, in poorly ventilated spaces, combined with low humidity and high temperature can be highly contagious. 16 There have been cases of transmission between people more than 2 m away in enclosed spaces with little ventilation and after exposure to an infected person for more than 30 min 4 Air conditioning and ventilation mechanisms F I G U R E 1 The emission of particles through the mouth or nose increase the propagation distance of exhaled particles. Heating Ventilation Air Conditioning (HVAC) systems establish recirculation and ventilation circuits that can transport the aerosol from their point of origin to all HVAC areas. Thus, although the particles may reach further, the concentration will be lower due to dilution and filtration. 12 On the other hand, although the main source of aerosols and droplets is the emission by patients themselves, there are other scenarios that can generate infectious particles, such as medical procedures, surgeries, tap water, and toilet flushes. 17

| MATERIALS AND METHODS
A scoping review was conducted following the methodology proposed by Arksey & O'Malley. 19

| Identifying the research question
The research question this review intended to answer was: How do aerosols emitted by respiratory activity behave in ambient air? How might this behaviour affect the transmission of SARS-CoV-2?

| Identifying relevant studies
The PubMed, Scopus, and WOS databases were consulted. In addition, the reference lists of the most relevant articles were consulted.
Search terms related to virus and disease, contaminating particles and route of transmission were selected. The search strategy used was ("Covid-19" OR "SARS-COV-2" OR coronavirus) AND (aerosol OR droplet) AND (ventilation OR "airborne transmission"). The search was conducted between the months of January and February, 2021.

| Study selection
Articles from experimental models describing the behaviour of aerosols in ambient air published between 2020 and 2021, in English or Spanish, were included in the present review. Two reviewers independently checked the references initially obtained in the search.
After eliminating duplicates, the reviewers analysed the title and abstract to select papers according to the inclusion criteria. In case of doubt or disagreement, an attempt was made to make a decision by consensus, with a third researcher intervening when necessary. The shortlisted papers were analysed in full text to identify those that provided relevant information to the research question.

| Charting the data
For data extraction, an analytical-narrative method was followed to synthesise and interpret the information, grouping and reorganising the data by following the key points and main subjects (Arksey & O'Malley, 2005). The data were classified in tables specifically designed for this purpose, in the following sections: authorship, year of publication, model used in the study, measured variables, results, and recommendations. The whole process was carried out independently by two researchers who agreed on the extracted data. The intervention of a third researcher was not necessary to resolve discrepancies.

| Collating, summarising, and reporting the results
The main findings and recommendations were summarised following an analytical-descriptive procedure. The content analysis led to three main subjects: particle behaviour, containment measures, and ventilation.

| RESULTS
Initially, through the electronic search in the databases, 882 references were obtained. After eliminating duplicates, the titles and abstracts were analysed to identify the papers according to the inclusion criteria. The reading and analysis of full texts led to the selection of 9 papers for this review. The selection process is summarised in Figure 2. The main findings of the selected papers are presented in Table 1 and summarized in Figure 3. 20-28

| Behaviour of particles
Infectious aerosols are exhaled by infected people who emit a different number of particles, depending on whether they perform normal breathing or emit a cough or sneeze. 8 According to the results ROBLES-ROMERO ET AL. When considering the high number of people who have the disease but are asymptomatic, the risk of infection in any common space is high. Vuorinen et al. 26 estimated at 100 the number of particles needed in the air for contagion. If the infected person is silent, the particle emission rate is 1248 copies/m, 3 while if they speak they amount to 7.44 million copies/m 3 . 23 When speaking, the emission rate is comparable to that of an individual doing light physical activity. 21 According to Riediker & Tsae, 23

| Preventive measures
The most recommended containment measure is the use of a face mask, since regardless of the type used, it significantly reduces the contagion. 20,22 Bhagat et al. 20 pointed out the protective effect of masks by diverting most of the particles emitted towards the infected person's own body. Feng et al. 22 reinforced this recommendation by stating that even if they are poorly placed and made of low filtration material, they have protective effects against not wearing them.
With regard to social distancing measures, the revised articles established as an effective distance a minimum of 2 m even when wearing a mask, 28 extending it to more than 4 metres in case of cough. 26 In outdoor or ventilated spaces, between 1.6 and 8.2 m is considered a safe interval ( Figure 4). 25 In enclosed spaces, it is difficult to establish a safe range due to the difficulty of controlling influencing variables. It has been identified that an infected person in movement has a protective effect over standing in the same place, since the higher the speed of displacement, the greater the dispersion of aerosols and the lower the concentration. 26 The difference in incidences of contagion varies depending on the characteristics of where social interactions occur and the ca-

| Ventilation
With regard to enclosed spaces, the characteristics of ventilation is the key to reducing the number of infections. Natural ventilation, with doors and windows to the outside, is more effective than Ventilation. Displacement ventilation, which encourages vertical stratification and removal of polluted hot air near the ceiling, appears to be the most effective measure in reducing contagion.
Ventilation that allows extraction of the columns of hot air in upper parts of rooms.
Airflows. Flows within enclosed spaces behave like turbulent. Use of mask to send direct aerosols towards the body of the emitter, reducing the formation of polluting clouds.
Masks are effective in reducing the direct expulsion of bio-aerosols by dragging them into the person's body.

Buonanno et al. 2020
Particle emission rate. The viral load present in asymptomatic people is similar to that of those who present symptoms, so they have the same transmission capacity.
Use of effective protective measures since the contagion capacity of the asymptomatic is similar to the symptomatic. Ventilation.
The emission of particles when speaking resembles the emission that occurs when performing light physical exercise.
Mechanical ventilation in enclosed spaces.
Mechanical ventilation reduces the number of cases that will be caused by an infected person during the period of infection from less than 1 to less than 0.4.

Feng et al. 2020
Aerosol emission distance.
Coughing can send aerosols more than 3 m away if the air is stagnant.
Increase the safety distance in enclosed spaces without ventilation.
Airflows. The wind facilitates the movement and deposition of even large respiratory droplets.
Avoid direct air flows between individuals.
Relative humidity. High relative humidity increases the condensation effect and causes larger infectious droplets to fall earlier.
Increase the relative humidity in enclosed spaces.
Wearing masks. Incorrectly worn face masks also significantly reduce the suspension of contaminated particles.
Use face masks always and under any circumstances.
Use of face protection to reduce the risk of infection.
Concentration in a closed room.
Concentrations in a closed space with an infected person coughing amount to 7.44 million copies/ m 3 , while with normal breathing they represent 1248 copies/m 3 .
Ventilation of enclosed spaces.

Satheesan et al. 2020
Air conditioning systems. Air renewal with the outside and the rates of exhaust airflow have significant effects on the distribution of polluting particles within a mechanically ventilated space.
Renewal with outdoor air in the air conditioning systems of indoor rooms.
Air renewal. The placement of air extraction grilles on top of an infected patient reduces the risk of airborne transmission.
Place infected patients under the air grilles.

Sun et al. 2020
Safety distance.
Safe social distance when speaking should be from 1.6 to 3.0 metres in ventilated or outdoor spaces, and up to 8.2 m in poorly ventilated environments.
Increase social distance as much as possible even in open spaces.

Ventilation.
Decreasing the occupancy of spaces to 50% reduces the infection rate between 20% and 40% in the first 30 min.
Reduce space capacity to 50%.
Safe ventilation of spaces reduces the risk by 40% if occupancy is reduced to 50%.

Vuorinen
Number of particles Estimated number of particles for a contagion = 100. Do not stay in enclosed spaces.
artificial ventilation as it favours that larger particles are deposited earlier, 22 and facilitates the dissolution of polluting aerosols with the clean air of the room. 24 According to their results, Zhao et al. 28 recommended avoiding horizontal aeration flows that transport particles from one person to another. On the contrary Buonanno et al. 21 found that the effectiveness of mechanical ventilation is greater than natural ventilation in spaces visited by an asymptomatic patient, reducing the mean number of cases that will be caused by an infected person during the period of infection, from less than 1 to less than 0.4. According to these authors, if natural ventilation involves a direct flow of air from the infected person to the potential host, the chances of infection are higher. Ventilation.
Coughing sends infectious particles up to 4 m away in enclosed spaces and remain 90 s in the air.
Use suction ventilation from the ceiling.
The speed of movement of the infected reduces the concentration of aerosols by dilution.
Suction ventilation from the ceiling favours the dilution of aerosols and reduces the risk of contagion.

Yao et al. 2020
Humidity and temperature.
Both indoor and outdoor areas of high temperature and low humidity reduce the risk of infection.
Indoor spaces should increase temperature and reduce humidity to reduce the risk of infection.

Use of ozone.
Ozone reduces the existence of the virus in all types of spaces and surfaces.
Use of ozone can help disinfect surfaces and environments.
Adequately ventilate indoor spaces with outdoor air.

Zhao et al. 2020
Aerosol dispersion. Respiratory droplets travel farther in environments with low temperature and high humidity.
Increase the safety distance to more than 2 m in humid and cold environments.
Humidity and temperature.
The number of aerosol particles increases in high temperature and low humidity environments.
Avoid horizontal ventilations to aerate rooms, as these transport particles between people.
Ventilation. 2 m of physical distance are insufficient to eliminate possible droplet contact in cold and humid environments.
The dispersion distance of the droplets increases as the speed of the airflow increases, which can reach 23 m.. As far as artificial ventilation is concerned, one variable to consider is the type of air circulation. The reviewed studies recommend the use of air from the outside and avoiding recirculation of indoor air to reduce the incidence of contagion. 24 Bhagat et al. 20 further described that moving airflows within enclosed spaces behave as turbulent, favouring the redistribution of potential polluting aerosols. Another variable to consider is the situation in which the air extraction device is placed in artificially ventilated rooms. According to the models included in this review, suction grids should preferably be located on the ceiling to be more effective. 20,24,26 Specifically, in inpatient units of Covid-19 patients, Satheesan et al. 24 advised that patients should be placed under the grilles of the ventilation system to increase the suction power of infectious aerosols. Air extraction devices must be located in the highest areas of the rooms, so that the air that has risen due to temperature difference can be extracted. 20 The reviewed studies also identified two other environmental variables that influence the contagion process: temperature and masks. 38,39 The effectiveness of masks is difficult to assess as their filtration capacity depends on the tissue used and whether or not filters are included. 40 In relation to social distance, the reviewed studies support this measure. However, there are differences in the results of previous studies depending on the scenario. In ventilated spaces, if the infected person is at rest, a minimum separation between 1 m, according to WHO, 30 and close to 2 m is recommended 34,41 as long as the infected person wears a face mask. Otherwise, these distances would be insufficient. 42 In the event that the person is in a space without ventilation, the distances must be increased, being difficult to quantify due to the different variables that affect this situation. 43 After reviewing the articles included in this review, ventilation stands out as a protective measure for the control of contagions in Many studies propose natural ventilation as the most effective measure, that is keeping windows and doors open. 8,37 According to Kohanski et al. 12 with three outdoor air renewals per hour in an enclosed space, the risk of contagion is reduced by 95%. If this is not possible, artificial ventilation is the next option, which would depend on the use of air conditioning devices. 44 Evidence recommends placing the ventilation device on the ceiling, directed horizontally with respect to airflow, and just above the patient in a hospital with infected patients. 45 Air recirculation would increase the permanence of aerosols in suspension, raising the risk of infection if there is a person infected in the enclosed space. 46 Borro et al. 47  and 40% relative humidity than at 27°C and 65% relative humidity. 55

| CONCLUSIONS
The present review brings together evidence on the behaviour of aerosols in the air, which will help to better understand the mecha-