Masking out air sharing
The effectiveness of masks in preventing the transmission of severe acute respiratory syndrome coronavirus 2 has been debated since the beginning of the COVID-19 pandemic. One important question is whether masks are effective despite the forceful expulsion of respiratory matter during coughing and sneezing. Cheng et al. convincingly show that most people live in conditions in which the airborne virus load is low. The probability of infection changes nonlinearly with the amount of respiratory matter to which a person is exposed. If most people in the wider community wear even simple surgical masks, then the probability of an encounter with a virus particle is even further limited. In indoor settings, it is impossible to avoid breathing in air that someone else has exhaled, and in hospital situations where the virus concentration is the highest, even the best-performing masks used without other protective gear such as hazmat suits will not provide adequate protection.
Science, abg6296, this issue p. 1439
Abstract
Airborne transmission by droplets and aerosols is important for the spread of viruses. Face masks are a well-established preventive measure, but their effectiveness for mitigating severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) transmission is still under debate. We show that variations in mask efficacy can be explained by different regimes of virus abundance and are related to population-average infection probability and reproduction number. For SARS-CoV-2, the viral load of infectious individuals can vary by orders of magnitude. We find that most environments and contacts are under conditions of low virus abundance (virus-limited), where surgical masks are effective at preventing virus spread. More-advanced masks and other protective equipment are required in potentially virus-rich indoor environments, including medical centers and hospitals. Masks are particularly effective in combination with other preventive measures like ventilation and distancing.
Airborne transmission is one of the main pathways for the transmission of respiratory viruses, including the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) (1). Wearing face masks has been widely advocated to mitigate transmission. Masks are thought to protect people in two ways: (i) source control, reducing the emission and spread of respiratory viruses through airborne droplets and aerosols, and (ii) wearer protection, reducing the inhalation of airborne respiratory viruses.
The effectiveness of masks, however, is still under debate. Compared with N95 or FFP2 respirators, which have very low particle penetration rates (~5%), surgical and similar masks exhibit higher and more variable penetration rates (~30 to 70%) (2, 3). Given the large number of particles emitted upon respiration and especially upon sneezing or coughing (4), the number of respiratory particles that may penetrate masks is substantial, which is one of the main reasons for doubts about their efficacy in preventing infections. Moreover, randomized clinical trials have shown inconsistent or inconclusive results, with some studies reporting only a marginal benefit or no effect of mask use (5, 6). Thus, surgical and similar masks are often considered to be ineffective. On the other hand, observational data show that regions or facilities with a higher percentage of the population wearing masks have better control of COVID-19 (7тАУ9). So how are we to explain these contrasting results and apparent inconsistencies?
In this work, we develop a quantitative model of airborne virus exposure that can explain these contrasting results and provide a basis for quantifying the efficacy of face masks. We show that mask efficacy strongly depends on airborne virus abundance. On the basis of direct measurements of SARS-CoV-2 in air samples and population-level infection probabilities, we find that the virus abundance in most environments is sufficiently low for masks to be effective in reducing airborne transmission.
When evaluating the effectiveness of masks, we want to understand and quantify their effect on the infection probability, Pinf. Assuming that every inhaled single virus (virion) has the same chance to infect a person, Pinf can be calculated by a single-hit model of infectionPinf=1тИТ1тИТPsingleNv(1)where Psingle represents the infection probability for a single virus and Nv represents the total number of viruses to which the person is exposed (10). For airborne transmission, the infection probability Pinf for a given time period can be plotted as a function of inhaled virus number, Nv.
Figure 1 illustrates the dependence of Pinf on Nv based on the single-hit model (Eq. 1) and scaled by the median infectious dose IDv,50 at which the probability of infection is 50% (10). It shows a highly nonlinear sensitivity of Pinf to changes in Nv. Accordingly, the same percentage of change of Nv may lead to different changes in Pinf depending on the absolute level of Nv. In a virus-rich regime, where Nv is much higher than IDv,50 (Fig. 1, A and B), Pinf is close to unity and is not sensitive to changes in Nv. In this case, wearing a mask may not suffice to prevent infection. In a virus-limited regime, where Nv is close to or lower than IDv,50, however, Pinf strongly varies with Nv, and reducing Nv by wearing a mask will lead to a substantial reduction in the infection probability (Fig. 1, C and D). Thus, we need to determine the regime of airborne virus abundance to understand mask efficacy.
(A to D) The solid curves represent the infection probability (Pinf) as a function of inhaled virus number (Nv) scaled by median infectious dose IDv,50 at which Pinf = 50%. In the virus-rich regime [(A) and (B)], the concentration of airborne viruses is so high that both the numbers of viruses inhaled with and without masks (Nv,mask, Nv) are much higher than IDv,50, and Pinf remains close to ~1 even if masks are used. In the virus-limited regime [(C) and (D)], Nv and Nv,mask are close to or lower than IDv,50, and Pinf decreases substantially when masks are used, even if the masks cannot prevent the inhalation of all respiratory particles. In (B) and (D), the red dots represent respiratory particles containing viruses, and the open green circles represent respiratory particles without viruses. Man icon used in (B) and (D) was made by Tinu CA from www.freeicons.io, distributed under CC-BY 3.0.
Respiratory particles, including aerosol particles and larger droplets, can carry viruses and are often used to visualize the transmission of airborne viruses (4). Taking a representative average of respiratory activity (11), we find that a person typically emits a total number of ~3 ├Ч 106 particles during a 30-min period (supplementary text, section S1.1). This very large number implies that indoor environments are usually in a respiratory particleтАУrich regime. Surgical masks with particle collection efficiencies of ~50% cannot prevent the release of millions of particles per person and their inhalation by others (see green dots in Fig. 1, B and D). In other words, the human-emitted respiratory particle number is so high that we cannot avoid inhaling particles generated by another person, even when wearing a surgical mask. If every respiratory particle were to contain one or more viruses, indoor environments would often be in a virus-rich regime because the median infectious dose IDv,50 for respiratory diseases is typically on the order of a few tens to thousands of viruses (12тАУ14).
But, does a respiratory particleтАУrich regime actually imply a respiratory virusтАУrich regime? To answer this question, we investigated characteristic virus distributions in both exhaled air samples and indoor air samples including coronaviruses (HCoV-NL63, -OC43, -229E, and -HKU1), influenza viruses (A and B), rhinoviruses, and SARS-CoV-2 (supplementary text, section S1). We find that usually just a minor fraction of exhaled respiratory particles contains viruses. In contrast to the high number of emitted respiratory particles, the number of viruses in 30-min samples of exhaled air (Nv,30,ex) are typically low, with mean values of ~53 for coronaviruses (HCoV-NL63, -OC43, -229E, and -HKU1), ~38 for influenza viruses (A and B), and ~96 for rhinoviruses (11) (supplementary text, section S1.2, and Fig. 2). Figure 2, A and B, shows the infection probabilities obtained by inserting the number of exhaled viruses (Nv,30,ex) for the number of potentially inhaled viruses (Nv,30), assuming a characteristic infectious dose of IDv,50 = 100 or 1000 viruses, respectively (12тАУ14). For SARS-CoV-2 in various medical centers, we obtained mean values of Nv,30 in the range of ~1 to ~600 (15тАУ18) (supplementary text, section S1.3), which correspond to Pinf values in the range of ~0.1% to 10% for IDv,50 = 1000 and ~1% to 100% for IDv,50 = 100. The wide range of Nv,30/ IDv,50 and Pinf values demonstrate that both virus-limited and virus-rich conditions can occur in indoor environments.
(A and B) Individual infection probabilities (Pinf) plotted against inhaled virus number (Nv) scaled by characteristic median infectious doses of IDv,50 = 100 or 1000 viruses, respectively. The colored data points represent the mean numbers of viruses inhaled during a 30-min period in different medical centers in China, Singapore, and the US, according to measurement data of exhaled coronavirus, influenza virus, and rhinovirus numbers (blue circles) (11) and of airborne SARS-CoV-2 number concentrations (red symbols) (15тАУ18), respectively. The error bars represent one geometric standard deviation. (C) Population-average infection probability (Pinf,pop) curves assuming lognormal distributions of Nv with different standard deviations of ╧Г = 0, 1, and 2, respectively. The x axis represents the mean value of log(Nv/IDv,50). The shaded area indicates the level of basic population-average infection probability, Pinf,pop,0, for SARS-CoV-2, as calculated from the basic reproduction number for COVID-19 and estimated values of average duration of infectiousness and daily number of contacts.
The high variabilities of Nv,30 and Pinf shown in Fig. 2, A and B, are consistent with the wide distribution of viral load observed in respiratory tract fluids (19) and need to be considered for estimating population-average infection probabilities, Pinf,pop (supplementary text, section S4). For this purpose, we modeled Nv for SARS-CoV-2 as lognormally distributed with standard deviations (╧Г) in the range of ~1 to 2 on the basis of recently reported distributions of the viral load of SARS-CoV-2 in respiratory fluids (19) (supplementary text, section S4). As shown in Fig. 2C, the population-average infection probabilities with ╧Г > 0 are higher than in the case of uniform exposure (╧Г = 0) in the virus-limited regime at Pinf,pop < ~50%. In other words, when the population-average infection probability is in the virus-limited regime with Pinf,pop,0 < 0.5 (Fig. 2C), a broader distribution (larger ╧Г) implies an increase in the fraction of transmission events under virus-rich conditions (e.g., superspreader events), which leads to a reduction of overall mask efficacy.
The basic reproduction number for COVID-19 (R0 тЙИ 2 to 4) (20) can be related to a basic population-average infection probability, Pinf,pop,0, through R0 = Pinf,pop,0 ├Ч c ├Ч d (21). With the average duration of infectiousness (d тЙИ 10 days) and average daily numbers of human contacts (c тЙИ 10 to 25 contacts per day) (22, 23), we obtain estimates in the range of ~0.8% to ~4% for Pinf,pop,0, as indicated by the shaded area in Fig. 2C. The low levels of Pinf,pop,0 indicate a widespread prevalence of virus-limited conditions.
Different regimes of abundance are relevant not only for the distinction of respiratory particles and viruses, but also for different types of viruses. For example, viruses with higher transmissibilityтАФi.e., those with higher loads and rates of emission and exhalation, greater environmental persistence, or lower IDv,50тАФmay result in a virus-rich regime and lead to higher basic reproduction numbers, as observed for measles and other highly infectious diseases. Our analysis shows that the levels of Pinf and R0 can vary widely for different viruses. This means that aerosol transmission does not necessarily lead to a measles-like high R0 and that relatively low values of Pinf and R0 do not rule out airborne transmission. On the basis of the scaling with IDv,50, the curves shown in Figs. 1 to 3 can easily be applied to assess the efficacy of masks and other preventive measures against new and more-infectious mutants of SARS-CoV-2, such as B.1.1.7.