We further elucidated the contribution of airborne transmission to the COVID-19 outbreak by comparing the trends and mitigation measures during the pandemic worldwide and by considering the virus transmission routes (Fig. 4). Face covering prevents both airborne transmission by blocking atomization and inhalation of virus-bearing aerosols and contact transmission by blocking viral shedding of droplets. On the other hand, social distancing, quarantine, and isolation, in conjunction with hand sanitizing, minimize contact (direct and indirect) transmission but do not protect against airborne transmission. With social distancing, quarantine, and isolation in place worldwide and in the United States since the beginning of April, airborne transmission represents the only viable route for spreading the disease, when mandated face covering is not implemented. Similarly, airborne transmission also contributes dominantly to the linear increase in the infection prior to the onset of mandated face covering in Italy and NYC (Fig. 2 B and C and SI Appendix, Fig. S1). Hence, the unique function of face covering to block atomization and inhalation of virus-bearing aerosols accounts for the significantly reduced infections in China, Italy, and NYC (Figs. 1–3), indicating that airborne transmission of COVID-19 represents the dominant route for infection.
<img class=”highwire-fragment fragment-image” alt=”Fig. 4.” src=”https://www.pnas.org/content/pnas/early/2020/06/10/2009637117/F4.medium.gif” width=”440″ height=”176″/>
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Transmission of COVID-19. Human atomization of viruses arises from coughing or sneezing of an infected person, producing virus-containing droplets (>5 μm) and aerosols (<5 μm). Virus transmission from person to person occurs through direct/indirect contact and airborne aerosol/droplet routes. Large droplets mainly settle out of air to cause person/object contamination, while aerosols are efficiently dispersed in air. Direct and airborne transmissions occur in short range and extended distance/time, respectively. Inhaled airborne viruses deposit directly into the human respiration tract.
Recent measurements identified SARS-Cov-2 RNA on aerosols in Wuhan’s hospitals (18) and outdoor in northern Italy (21), unraveling the likelihood of indoor and outdoor airborne transmission. Within an enclosed environment, virus-bearing aerosols from human atomization are readily accumulated, and elevated levels of airborne viruses facilitate transmission from person to person. Transmission of airborne viruses in open air is subject to dilution, although virus accumulation still occurs due to stagnation under polluted urban conditions (7, 22). Removal of virus-bearing particles from human atomization via deposition is strongly size dependent, with the settling velocities ranging from 2.8 × 10−5 m⋅s−1 to 1.4 × 10−3 m⋅s−1 for the sizes of 1 and 10 μm, respectively (7). For comparison, typical wind velocity is about 1 m⋅s−1 to 3 m⋅s−1 indoors (23) and is ∼1 m⋅s−1 horizontally and 0.1 m⋅s−1 vertically in stable air (7, 22). Under those indoor and outdoor conditions, the residence time of virus-bearing aerosols reaches hours, due to air mixing (7).
We also examined ambient conditions relevant to the outbreaks in Wuhan, Italy, and NYC. The initial outbreak of COVID-19 in Wuhan coincided with the winter haze season in China (7, 22), during which high levels of PM2.5 were prevalent in air (SI Appendix, Figs. S2 and S3). On the other hand, the daily average PM2.5 concentrations were much lower during the outbreaks in Rome, Italy, and in NYC (SI Appendix, Fig. S2). The airborne transmission pathways (i.e., indoor or outdoor) as well as the effects of ambient PM2.5 levels on virus transmission may be variable among urban cities. For example, the winter haze conditions in China likely exacerbated outdoor virus spreading (24, 25), because of low UV radiation, air stagnation (lacking ventilation on the city scale), and low temperature (7, 22). Also, there may exist a synergetic effect of simultaneous exposure to the virus and PM2.5 to enhance the infectivity, severity, and fatalities of the disease (14, 26). In addition, nascent virus-bearing aerosols produced from human atomization likely undergo transformation in air, including coagulation with ambient preexisting PM and/or growth on a time scale of a few hours in typical urban air (27⇓–29). Such transformation, as recently documented on coarse PM in Italy (21), may mitigate virus inactivation (9, 12), by providing a medium to preserve its biological properties and elongating its lifetimes. However, key questions remain concerning transformation and transmission of virus-bearing aerosols from human atomization in air. Specifically, what are the impacts of transformation of human-atomized aerosols on viral surviving and infectivity in air?
While the humidity effect on viral surviving is uncertain (3, 9), the conditions during the outbreaks in Wuhan, Rome, and NYC correspond to high RH yet low absolute humidity because of low temperature (SI Appendix, Fig. S3). Early experimental work (9) showed remarkable survival for the analogous coronavirus MERS-CoV at the RH level characteristic of the COVID-19 outbreaks in Wuhan, Rome, and NYC. For comparison, indoor temperature and RH typically range from 21 °C to 27 °C and 20 to 70%, respectively (23).
Of particular importance are the considerations that render airborne SARS-CoV-2 the most efficient among all transmission routes. Even with normal nasal breathing, inhalation of virus-bearing aerosols results in deep and continuous deposition into the human respiratory tract, and this transmission route typically requires a low dose (8). Also, airborne viruses have great mobility and sufficiently long surviving time for dispersion (9, 12), and residents situated in densely populated environments are highly vulnerable. In addition, nascent micrometer-size aerosols produced from coughing/sneezing of infected people have the potential of containing many viruses, particularly for asymptomatic carriers (16).
Future research is critically needed to assess the transmission, transformation, and dispersion of virus-bearing aerosols from human atomization under different environmental conditions, as well as the related impacts on virus infectivity. It is equally important to understand human atomization of airborne viruses: What are the number and size distributions of nascent aerosols as well as the viral load per particle from coughing/sneezing? It is also imperative to evaluate human inhalation of airborne viruses: How are aerosols deposited along the respiratory tract, and what is the minimum dose of airborne viruses required for infection? It is also important to evaluate the performance of face masks to quantify the efficiency to filtrate airborne viruses relevant to human atomization and inhalation. Elucidation of these mechanisms requires an interdisciplinary effort.