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Practical Indicators for Risk of Airborne Transmission in Shared Indoor Environments and Their Application to COVID-19 Outbreaks

  • Z. Peng
    Z. Peng
    Dept. of Chemistry and CIRES, University of Colorado, Boulder, Colorado 80309, United States
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    Orcidhttps://orcid.org/0000-0002-6823-452X
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  • A.L. Pineda Rojas
    A.L. Pineda Rojas
    CIMA, UMI-IFAECI/CNRS, FCEyN, Universidad de Buenos Aires─UBA/CONICET, Buenos Aires C1428EGA, Argentina
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  • E. Kropff
    E. Kropff
    Leloir Institute─IIBBA/CONICET, CBA, Buenos Aires C1405BWE, Argentina
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  • W. Bahnfleth
    W. Bahnfleth
    Dept. of Architectural Engineering, The Pennsylvania State University, University Park, Pennsylvania 16802, United States
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  • G. Buonanno
    G. Buonanno
    Dept. of Civil and Mechanical Engineering, University of Cassino and Southern Lazio, Cassino 03043, Italy
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  • S.J. Dancer
    S.J. Dancer
    Dept. of Microbiology, NHS Lanarkshire, Glasgow, Scotland G75 8RG, U.K.
    School of Applied Sciences, Edinburgh Napier University, Edinburgh, Scotland EH11 4BN, U.K.
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  • J. Kurnitski
    J. Kurnitski
    REHVA Technology and Research Committee, Tallinn University of Technology, Tallinn 19086, Estonia
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  • Y. Li
    Y. Li
    Dept. of Mechanical Engineering, The University of Hong Kong, Hong Kong 999077, China
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  • M.G.L.C. Loomans
    M.G.L.C. Loomans
    Dept. of the Built Environment, Eindhoven University of Technology, Eindhoven 5612 AZ, The Netherlands
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  • L.C. Marr
    L.C. Marr
    Dept. of Civil and Environmental Engineering, Virginia Tech, Blacksburg, Virginia 24061, United States
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    Orcidhttps://orcid.org/0000-0003-3628-6891
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  • L. Morawska
    L. Morawska
    International Laboratory for Air Quality and Health, Queensland University of Technology, Brisbane, Queensland 4001, Australia
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    Orcidhttps://orcid.org/0000-0002-0594-9683
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  • W. Nazaroff
    W. Nazaroff
    Dept. of Civil and Environmental Engineering, University of California, Berkeley, California 94720, United States
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    Orcidhttps://orcid.org/0000-0001-5645-3357
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  • C. Noakes
    C. Noakes
    School of Civil Engineering, University of Leeds, Leeds LS2 9JT, U.K.
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  • X. Querol
    X. Querol
    Institute of Environmental Assessment and Water Research, IDAEA, Spanish Research Council, CSIC, Barcelona 08034, Spain
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  • C. Sekhar
    C. Sekhar
    Dept. of the Built Environment, National University of Singapore , 117566 Singapore
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  • R. Tellier
    R. Tellier
    Dept. of Medicine, McGill University and McGill University Health Centre, Montreal, Québec H4A 3J1, Canada
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  • T. Greenhalgh
    T. Greenhalgh
    Nuffield Dept. of Primary Care Health Sciences, University of Oxford, Oxford OX2 6GG, U.K.
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  • L. Bourouiba
    L. Bourouiba
    The Fluid Dynamics of Disease Transmission Laboratory, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, United States
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  • A. Boerstra
    A. Boerstra
    REHVA (Federation of European Heating, Ventilation and Air Conditioning Associations), BBA Binnenmilieu, The Hague 2501 CJ, The Netherlands
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  • J.W. Tang
    J.W. Tang
    Dept. of Respiratory Sciences, University of Leicester, Leicester LE1 7RH, U.K.
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  • S.L. Miller
    S.L. Miller
    Dept. of Mechanical Engineering, University of Colorado, Boulder, Colorado 80309, United States
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    Orcidhttps://orcid.org/0000-0002-1967-7551
  • , and 
  • J.L. Jimenez*
    J.L. Jimenez
    Dept. of Chemistry and CIRES, University of Colorado, Boulder, Colorado 80309, United States
    *Email: [email protected]
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    Orcidhttps://orcid.org/0000-0001-6203-1847
Cite this: Environ. Sci. Technol. 2022, 56, 2, 1125–1137
Publication Date (Web):January 5, 2022
https://doi.org/10.1021/acs.est.1c06531

Copyright © 2022 American Chemical Society. This publication is licensed under

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Abstract

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Some infectious diseases, including COVID-19, can undergo airborne transmission. This may happen at close proximity, but as time indoors increases, infections can occur in shared room air despite distancing. We propose two indicators of infection risk for this situation, that is, relative risk parameter (Hr) and risk parameter (H). They combine the key factors that control airborne disease transmission indoors: virus-containing aerosol generation rate, breathing flow rate, masking and its quality, ventilation and aerosol-removal rates, number of occupants, and duration of exposure. COVID-19 outbreaks show a clear trend that is consistent with airborne infection and enable recommendations to minimize transmission risk. Transmission in typical prepandemic indoor spaces is highly sensitive to mitigation efforts. Previous outbreaks of measles, influenza, and tuberculosis were also assessed. Measles outbreaks occur at much lower risk parameter values than COVID-19, while tuberculosis outbreaks are observed at higher risk parameter values. Because both diseases are accepted as airborne, the fact that COVID-19 is less contagious than measles does not rule out airborne transmission. It is important that future outbreak reports include information on masking, ventilation and aerosol-removal rates, number of occupants, and duration of exposure, to investigate airborne transmission.

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KEYWORDS:

Synopsis

A model of airborne disease transmission through shared-room air is shown to explain literature outbreaks and can help guide mitigations.

Introduction

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Some respiratory infections can be transmitted through the airborne pathway in which aerosol particles (<100 μm) are shed by infected individuals and inhaled by others, causing disease in susceptible individuals. (1−4) It is widely accepted that measles, tuberculosis, and chickenpox are transmitted in this way, (5,6) and acceptance is growing that this is a major and potentially the dominant transmission mode of COVID-19. (7−13) There is substantial evidence that smallpox, (14) influenza, (3) SARS, (15) MERS, (6) and rhinovirus (16) are also transmitted via inhalation of aerosols.
There are three airborne transmission scenarios of interest in which infectious and susceptible people: (a) are in close proximity to each other (<1–2 m), so-called “short-range airborne transmission,” with overlapping breathing zones, (17) which is effectively mitigated by physical distancing; (b) are sharing air in the same room, that is, “shared-room airborne;” and (c) are not sharing a room, far apart in a very large room, or even in different buildings as in the Amoy Gardens SARS outbreak, called “longer-distance airborne transmission.” (15) Often (b) and (c) are lumped together under “long-range transmission,” but in Scenario (c) transport of pathogen-containing air is more complex, so that the approximation of well-mixed air is less valid. It is thus useful to separate these scenarios given the substantial differences in the risk of these situations and actions needed to abate the risk of transmission.
Airborne diseases vary widely in transmissibility, but all of them are most easily transmitted in a short range because of the higher concentration of pathogen-containing aerosols close to the infected person. For SARS-CoV-2, a pathogen of initially moderate infectivity (more recently increased by some variants such as Delta or Omicron), many instances have been reported implicating transmission in shared indoor spaces. Indeed, multiple outbreaks of COVID-19 have been reported in crowded spaces that were relatively poorly ventilated and that were shared by many people for periods of half an hour or longer. Examples include choir rehearsals, (11) religious services, (18) buses, (19) workshop rooms, (19) restaurants, (4,20) and gyms, (21) among others. There are only a few documented cases of longer-distance transmission of SARS-CoV-2, in buildings. (22−24) However, cases of longer-distance transmission are harder to detect as they require contact tracing teams to have sufficient data to connect cases together and rule out infection acquired elsewhere. Historically, it was only possible to prove longer-distance transmission in the complete absence of community transmission (e.g., ref (14)).
Being able to quickly assess the risk of infection for a wide variety of indoor environments is of utmost importance given the impact of the continuing pandemic (and the risk of future pandemics) on so many aspects of life in almost every country of the world. We urgently need to improve the safety of the air that we breathe across a range of environments including child-care facilities, kindergartens, schools, colleges, shops, offices, homes, eldercare facilities, factories, public and private transportation, restaurants, gyms, libraries, cinemas, concert halls, places of worship, and mass outdoor events across different climates and socio-economic conditions. There is limited evidence to specify to minimum ventilation rates required to mitigate airborne transmission in buildings. (25) However, data from COVID-19 outbreaks consistently show that a large fraction of buildings worldwide have very low ventilation rates despite the requirements set in national building standards. A host of policy questions─from how to safely reopen schools to how to prevent transmission in high-risk occupational settings─require accurate quantification of the multiple interacting variables that influence airborne infection risk.
Qualitative guidance to reduce the risk of airborne transmission has been published. (26−28) Different mathematical models have been proposed to help manage risk of airborne transmission, (29,30) and several models have been adapted to COVID-19. (31−34) It is important to define quantitative infection risk criteria for different spaces and types of events to more effectively manage the pandemic. (35) Such criteria could then be used by authorities and policy makers to assist in deciding which activities are permitted under what conditions, so as to limit infection risk across a society. To our knowledge, no such quantitative criteria have been proposed. In addition, often recommendations are complex and vague, for example, “reduce duration and density of occupancy and increase ventilation.” However, it is not clear how to combine the different measures together (e.g., is half the duration equivalent to doubling the ventilation?), and it is also not clear what level of mitigation is sufficient to reduce outbreak probability to a low level.
Here, we use a box model to estimate the viral aerosol concentration indoors and combine it with the Wells–Riley infection model. (29) The combined model is used to derive two quantitative risk parameters that allow comparing the relative risk of transmission in different situations when sharing room air. We explore the trends in infections observed in outbreaks of COVID-19 and other diseases as a function of these parameters. Finally, we use the parameters to quantify a graphical display of the relative risk of different situations and mitigation options.

Materials and Methods

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Box Model of Infection

The box model considers a single enclosed space in which virus-containing aerosols are assumed to be rapidly uniformly mixed compared with the time spent by the occupants in the space. This assumption is approximately applicable in many outbreaks, but there are some exceptions such as rooms where clear directional flow causes transmission. (18,20) Infection in close proximity (overlapping breathing zones) is not included. The mathematical notation used in the paper is summarized in Table S1. The mass balance equation is first written in terms of c, the concentration of infectious quanta in the air in the enclosed space (units of quanta m–3). Compared with a model written in terms of aerosol or viral particle concentrations, c has the advantage of implicitly including effects such as the deposition efficiency of the aerosol particles in the lungs of a susceptible person, as well as the efficiency with which such deposited particles may cause infection, the multiplicity of infection, and so on. The balance of quanta in the space can be written as:
(1)
where Ep is the emission rate of quanta into the indoor air from an infected person present in the space (quanta/h); fe is the penetration efficiency of virus-carrying particles through masks or face coverings for exhalation (which takes into account the impact of whether the infector wears a face covering); V is the volume of the space; λ0 is the first-order rate of removal of quanta by ventilation with outdoor air (h–1); λcle is the removal of quanta by air cleaning devices (e.g., recirculated air with filtering, germicidal UV, portable air cleaners, etc.); λdec is the infectivity decay rate of the virus; λdep is the deposition rate of airborne virus-containing particles onto surfaces, which is in theory size-dependent but not treated in a size-resolved manner in this study. Ep is a critical parameter that depends strongly on the disease, and it can be estimated with a forward model based on aerosol emission rates and pathogen concentration in saliva and respiratory fluid (32,36) or by fitting a model such as the one used here to real transmission events. (11,32)
This equation can be solved analytically or numerically for specific situations. Given the enormous number of possible situations, and given the prevalence of outbreaks resulting from events where air is shared for a significant period of time, we consider a simplified situation where the presence of all occupants is stable and continuous. Writing λ = λ0 + λcle + λdec + λdep for simplicity leads to a steady-state infectious quanta concentration of:
(2)
Under the assumption of no infectious quanta at the beginning of the event, a multiplicative factor, rss, can be applied for events too short to approximately reach steady state (see Section S1 for details) to correct the deviation of the quanta concentration averaged over the event (cavg) from that at the steady state:
(3)
Because the goal is to analyze outbreaks, we assume that only a single infectious person is present in the space, which is thought to be applicable to the outbreaks analyzed below. This allows calculation of the probability of infection, conditional to one infectious person being present. The model can also be formulated to calculate the absolute probability of infection, if we assume that the probability of an infectious person being present reflects the prevalence of a disease at a given location and time (e.g., refs (31,37)).
The infectious dose inhaled by a susceptible person present in the space (n) is expressed in quanta (one quantum is defined as the infectious dose corresponding to a probability of infection of 1 – 1/e) below:
(4)
where fi is the penetration efficiency of virus-carrying particles through masks or face coverings for inhalation (which takes into account the effect of the fraction of occupants wearing face coverings) (see the description of eq 1 for the definition of the other penetration efficiency used in this paper, i.e., fe); B is the breathing volumetric flow rate of susceptible persons; D is the duration of exposure, assumed to be the same for all the susceptible persons. Substituting:
(5)
The number of expected secondary infections increases monotonically with increasing n. For an individual susceptible person, by definition of an infectious quantum, the probability of infection is: (29)
(6)
For low values of n, the use of the Taylor expansion for an exponential allows approximating P as:
(7)
The total number of secondary infections expected, which may also be regarded as the effective reproduction number (Re) in a given situation, is then:
(8)
where Nsus is the number of susceptible individuals present, which is generally lower than the number of occupants because of vaccination or immunity from past infection. All the outbreaks studied here occurred before COVID-19 vaccines became available. Thus, the number of secondary infections increases linearly with n at lower values and nonlinearly at higher values. We retain the simplified form to define and calculate the risk parameters but use eq 6 for fitting the outbreak results in Figure 1b.

Figure 1

Figure 1. (a) Number of secondary cases vs. the risk parameter H and (b) attack rate vs. the relative risk parameter Hr for outbreaks of COVID-19, tuberculosis, influenza, and measles reported in the literature. A stronger outbreak in this figure refers to (i) more secondary infections, (ii) a higher attack rate, and (iii) a more infectious index case than typical outbreaks. The fitted trend line of attack rate as a function of Hr and its estimated uncertainty range (5th and 95th percentiles) are also shown in (b). All of the outbreaks investigated here involve the original variants of the virus. A variant twice as contagious (Ep0 × 2) should shift the fitted line to the left by a factor of two and displace the points of individual outbreaks upward.

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Risk Parameters for Airborne Infection

We define the relative risk parameter, Hr, and the risk parameter, H, for airborne infection in a shared space. The purpose of Hr and H is to capture the dependency of P and Nsi, respectively, on the parameters that define an event in a given space, in particular those parameters that can be controlled to reduce the risk of shared-room airborne transmission. To better capture the controllable actions, Ep and B were split into factors that can and cannot be controlled. Ep can be expressed as the product Ep0 × rE where Ep0 and rE are, respectively, the quanta shedding rate of an infectious person resting and only orally breathing (no vocalization), which takes into account the amount of virus shedded, the infectivity of each virus shed, and the susceptibility of the person who became infected; and the shedding rate enhancement factor relative to Ep0 for an activity with a certain degree of vocalization and physical intensity (see Table S2a for details). B can be expressed as B0 × rB, where B0 and rB are the average volumetric breathing rate of a sedentary susceptible person (under the assumption of the same size of all age groups) and the relative breathing rate enhancement factor (vs B0) for an activity with a certain physical intensity and for a certain age group (see Table S2b for details). Ep0 is uncertain, likely highly variable across the population, and variable over time during the period of infectiousness. (32,36,38) It may also increase due to new virus variants such as the SARS-CoV-2 Delta and Omicron variants, that are more contagious, assuming that the increased contagiousness is due to increased viral emission or reduced infectious dose (both of which would increase the quanta emission rate). (39,40) We note that some variants could in principle also increase transmissibility by lengthening the period of infectiousness for a given person, which by itself would not increase the quanta emission rate in a given situation. B0 is relatively well known and varies with a susceptible person’s age, sex, and body weight, in addition to the physical activity level. rE and rB are less uncertain than Ep0 and are functions of the specific physical and vocalization activities. (32,36,41) Thus, they are useful in capturing the quantitative impact of specific controllable factors. There could be factors beyond those considered here that lead to variation of viral emissions, such as the respiratory effort of patients with breathing disorders, such as emphysema or asthma. (42) Such factors can be incorporated into updated tables and computations from the model in the future.
Then P can be expressed as a function of Ep0, B0, and the product of the other controllable factors as:
(9)
Where Hr is the relative risk parameter:
(10)
It has a unit of h2 m–3, which indicates the increase of risk with duration (h), the inverse of the ventilation rate expressed as air changes per hour (1/h–1 = h), and the inverse of the volume of the space (1/m3). The other parameters such as the effect of masking are dimensionless. Hr includes the relative increase of the emission with activity (rE), but not the quanta emission rate by a resting and orally breathing infector (Ep0). This allows using the same risk parameters for different diseases, which will naturally separate in the graphs according to their transmissibility. The four terms that make up λ may vary in relative importance for different diseases and conditions. λdec ∼ 1.1 h–1 (43) has been reported for COVID-19. λdec depends on temperature and relative humidity. (44,45) λdep depends on the particle size and the geometry and airflow in a given space. Respiratory particle sizes in the range from 1–5 μm are thought to play a role in aerosol transmission of COVID-19, because of a combination of high emission rates by activities such as talking (46) and low deposition rates. λdep for a typical furnished indoor space spans 0.2–2 h–1 over this size range, with faster deposition for larger particles. (47) λ0 varies from ∼12 h–1 for airborne infection isolation rooms, (48) ∼6 h–1 for laboratories, ∼0.5 h–1 for residences, (49) ∼1 h–1 for offices, (1,50) and ∼2 h–1 for classrooms. (50,51) Limited ventilation data are available for many semipublic spaces such as shops, restaurants, and bars or transportation. λcle can vary from 0, if such systems are not in use, to several h–1 for adequately sized systems. Ventilation with clean outdoor air will be important in most situations, while virus decay and deposition likely contribute but are more uncertain for COVID-19, based on current information. In particular, the size distribution of aerosols containing infectious viruses is uncertain.
We consider a worst-case scenario where rates of deposition and infectivity decay are small compared with ventilation and air cleaning and can therefore be neglected. This also allows using the same relative risk parameter to compare different airborne diseases. This yields:
(11)
Hr can be recast as:
(12)
where:
(13)
Assuming that all of the people present in a space are susceptible to infection, L is equivalent to the ventilation plus air cleaning rate per person present in the space, (typically expressed in liters s–1 person–1 in standards and guidelines such as from refs (52−54)). If some fraction of the people present are immune to the disease, then L is larger than the corresponding personal ventilation rate in the guidance. While this recasting will be useful to persons familiar with ventilation guidelines, we keep the form in eq 11 for most further analyses, because the number of people allowed in a space is one of the critical variables that can be examined with this relative risk parameter.
We insert eq 9 into eq 8 and obtain
(14)
where we define the risk parameter
(15)
When there is only one infector present and n is small, H is proportional to Nsi, that is, the outbreak size. When it is unknown whether an infector is present, H is an approximate indicator of the absolute probability of infection (Pa), because the expected value of the number of infectors (Ni) is the product of the number of occupants (N) and probability of an occupant being infectious, a measure of prevalence of infectious individuals in local population (ηI), as shown below:
(16)
The precise estimation of ηI is complex for several reasons. Most transmission may be associated with those infected with high viral loads, (55,56) as many infected individuals may not shed virus into the air. (38) Also much spread is by individuals with few or no symptoms who may not know that they are infected; (57) however, a fraction of symptomatic infectious individuals are typically in isolation. There is also significant variation in viral load and infectivity during the course of the disease. (58) For these reasons, it is very difficult to determine ηI precisely based on test data. For a situation with multiple potential infectors present (e.g., a COVID-19 ward in a hospital), the risk parameters should be multiplied by the number of infectors.
For the analysis later in the paper that does not involve the activity type or face covering choice (and thus does not involve rE, rB, fe, or fi), we define another parameter (H′), which is closely related to H:
(17)
This parameter only captures the characteristics of susceptible individuals’ presence in the indoor space, not of their behavior.

Results

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Value of the Risk Parameters for Documented Outbreaks of COVID-19

An important advantage of the simple risk parameters is that their values can be calculated for outbreaks that are documented in the scientific literature. Values for documented COVID-19 outbreaks are shown in Table 1 (rE and rB are estimated based on the likely types of activities in each case, (32,36,41) see Table S2 for typical values). Also included are values for outbreaks documented in the literature for tuberculosis and measles, which are widely accepted to transmit through the air, and an influenza outbreak that was clearly due to airborne transmission. We have included all the outbreaks known to us for which sufficient information was available to estimate airborne infection risk. Most public health investigations so far in this pandemic have neglected to report ventilation rates, the volume of the space, filter and air cleaner efficiencies, and other building science details, and thus, their airborne risk cannot be estimated. It is important that future outbreak reports include this information, to allow expanding our knowledge of the circumstances conducive to airborne transmission of different diseases.
Table 1. Parameters for Outbreaks Documented in the Literature, but Missing Parameters Could Not Be Calculated from the Information Given in the Literature References
diseaseoutbreak (reference)rE relative shedding rate factorrB relative breathing rate factorD (h)NsusV (m3)λ0 (h–1)L (L s–1 person–1)rssH (persons h2 m–3)H′ (persons h2 m–3)Hr (h2 m–3)attack rate (%)number of secondary cases
COVID-19Guangzhou restaurant (4)9.3a11.220970.670.90.311.10.110.054459
big bus outbreak (59)113.346604.71.70.940.500.500.011178
small bus outbreak (59)11117228.93.20.890.0770.0770.0045122
Skagit choir (11)85b2.5c2.5608100.72.60.53300.140.58753
call center (60)30d1821663064.90.98130.450.0624494
aircraft (61)50e11119f60211818.40.170.446312
slaughterhouse (62)4.3g5h8 30000.53 0.77  0.08326 
Berlin choir (63)85b2.5c2.5 12000.17 0.19  0.4991 
Berlin school 1 (63)114.5 1808.3 0.97  0.002910 
Berlin school 2 (63)111.5 15010 0.93  0.000936 
Israel school (64)5.7i1.1j4.5 1502.7 0.92  0.143 
Germany meeting (63)1.7k12 1701.2 0.62  0.01217 
tuberculosisoffice (65)1.7k116067  7.11l116.30.164027
hospital (66)1.9m1.7n1800252006131l12037.54.8287
influenzaaircrafte (67)5014.3291680.50.450.59440.881.58625
measlesschool (29)111048  150 (7.6)o1l0.0190.0190.00045225
school (29),p113031  170 (5.5)o1l0.050.050.0016237
physician’s office (68)111122501.26.90.420.0170.0170.0014334
a

Footnotes: choice of parameters for specific cases. Talking during half of the time and half normal/half loud talking assumed.

b

Light exercise - loudly speaking.

c

Light intensity for 61- <71 years.

d

Resting - loudly speaking.

e

Estimate for coughing. The value is the product of rE for resting - speaking and the ratio of the average expired aerosol counts for coughing and talking. (69)

f

Only the business class cabin is considered.

g

Moderate exercise - oral breathing.

h

Moderate intensity for all age groups.

i

Standing - speaking for the infectious teacher.

j

Sedentary/passive for students aged 12–18.

k

Resting - speaking during 1/3 of the time assumed.

l

Event long enough for the assumption of unity for rss.

m

Half resting - oral breathing/half light exercise - oral breathing assumed.

n

Half sedentary/passive/half light intensity assumed.

o

Ventilation rate per susceptible person. The number in parentheses is for the ventilation rate per occupant, estimated based on a teacher-to-student ratio of 11.3% for Monroe County, NY (according to National Center for Education Statistics Common Core of Data (https://nces.ed.gov/ccd/)).

p

Scaled to the single-infector condition.

We see that the COVID-19 outbreaks that have been documented span ∼2.5 orders of magnitude range of the risk parameter H ∼ 0.09–30 persons h2 m–3. Numbers of secondary cases of these outbreaks generally increase with H (Figure 1a). Aiming to maintain values far below the threshold of 0.05 persons h2 m–3 should help reduce outbreaks.
Hr correlates well with the attack rates for the outbreaks reported in Table 1 (Figure 1b, Hr can be calculated for more reported outbreaks than H because the number of susceptible occupants is needed for the calculation of H, but not for that of Hr). COVID-19 outbreaks are observed for Hr > 0.001 h2 m–3, and thus, indoor activities should be limited to conditions below this value during the pandemic whenever possible.
A trend line can be fitted to the attack rate vs Hr with the Box/Wells–Riley model based on eq 9 (Figure 1b), with the fitting parameter being Ep0, that is, the basic quanta shedding rate (when breathing only, no vocalization). A best-fit Ep0 of 18.6 quanta h–1 was obtained (with B0 = 0.288 m3 h–1 assumed for all occupants for simplicity). When the uncertainties of Hr and attack rates are considered, the uncertainty of Ep0 can also be estimated through Monte Carlo uncertainty propagation, described in detail in Section S2. The 5th and 95th percentiles of the Ep0 values are 8.4 and 48.1 quanta h–1, respectively. This range is higher than that suggested by Buonanno et al. (2 quanta h–1), (32,36) but overlapping with the uncertainty range provided by those authors. Note that outbreaks are typically only observed for individuals with higher quanta emission rates; many infected individuals have low emission rates, and the risk in those situations will be lower than that estimated here. (32,36) The attack rates estimated according to this trend line have a high correlation with the actual attack rates (r2 = 0.90; Figure S1). Given the small size of the dataset of Hr and attack rates, we cross-validate this fitting by the leave-one-out method. (70) The 12 values of Ep0 obtained in the cross validation have maximum and mean relative absolute deviations of 20 and 6%, respectively, from the best-fit value, showing the robustness of the fitting.
Close alignment supports the dominant shared-room airborne character of these COVID-19 outbreaks. If the outbreaks had major components of other transmission modes (e.g., fomite or close-range transmission), we would expect a dependence on other parameters not considered here and overall much lower correlation with the risk parameters. Nevertheless, it can be observed that the attack rates of the outbreaks at low Hr (∼0.01 h2 m–3 or lower) are higher than the fitted curve. This can be due to several factors, including (i) other transmission routes (e.g., short-range airborne transmission, for which the risk cannot be well captured by the model in this study and can still be significant at low Hr) or (ii) the detection of only outlier cases of long-range airborne transmission resulting from the variability of Ep0 (e.g., cases where the infector’s actual quanta emission rate was extremely high), as the other cases may have too few secondary infections to be documented in the literature.

Effect of Building Parameters vs. Human Activities

The type of activity performed in each case (captured by the product of rE and rB) contributes substantially to the difference in H between these cases. When human activities are not taken into account, the parameter H′ only spans a narrow range of 0.09–0.56 person h2 m–3. This is probably due to similar per-person ventilation rates in many public indoor spaces (on the order of a few liter s–1 person–1) (52) and similar lengths of common events (in hours).
Similar to H, the variation in the values of Hr for the outbreaks in Table 1 is also largely determined by rE and rB. If they are not taken into account, Hr for all outbreaks would vary in the narrow range of 0.001 to ∼0.01 h2 m–3, as V and λ0 are building characteristics and D, as discussed above, is usually in hours. This implies that, in the presence of a single infector, reducing vocalization and/or physical intensity levels of the indoor activity is a very effective way to lower the infection risk of susceptible individuals. Reducing the event length can also help, while reducing occupancy cannot in this case, as shown by eq 10.
It is possible that some of the most visible outbreaks are associated with super-emitter individuals, who shed virus particles at higher rates than others. (42,71−73) If that is the case, the actual Hr values at which significant transmission starts to appear in the presence of individuals that are not super emitters may be higher than those determined here. However, if super-emitters are important, so will be their contribution to total spread, and thus one should try to reduce the risk to reduce the probability of such events occurring.

Values of the Risk Parameters for Outbreaks of Other Airborne Diseases

In Table 1 and Figure 1, we also include a few reported indoor outbreaks of three other diseases with significant airborne transmission, that is, tuberculosis, influenza, and measles. For outbreaks to have a similar number of secondary cases or attack rate, H or Hr needs to be higher for tuberculosis and influenza and lower for measles than that for COVID-19 (Figure 1). Note that many of the children present in the measles outbreak were vaccinated, but the risk parameter framework can still be applied by considering the number of susceptible children present. This difference is mainly due to differences in Ep0 (lower for tuberculosis and influenza and higher for measles; Figure 1b). A higher Ep0 for measles may indicate a larger amount of airborne measles virus in breath or a steeper dose–response curve for the measles virus than SARS-CoV-2, or both. A novel disease as contagious as measles would make almost any indoor situation prone to superspreading. On the other hand, tuberculosis and influenza are less contagious. Tuberculosis transmission is propagated because untreated infected people remain contagious for years. (74) The influenza outbreak occurred in an airplane without ventilation with the index case constantly coughing and represents an extreme for this disease. (67) Most influenza patients are thought to emit significantly less virus. (75) More discussions about quanta emission rates of different diseases can be found elsewhere. (36,76)
Given that both the measles and tuberculosis pathogens are widely accepted as airborne, the intermediate risk profile for COVID-19 in Figure 1b is not inconsistent with airborne transmission, contrary to frequently made arguments. (77,78) Contagiousness of a disease does not necessarily indicate the transmission route. (79) Airborne diseases can vary in their contagiousness depending on parameters such as the amount of virus shed, the survival of the virus in the air, the dose–response relationship for infection, and other parameters. The only fundamental requirement is that transmission needs to be sufficient for the disease to survive as such, something COVID-19 has had no trouble with so far.

Graphical Representation of Relative Risks of Different Situations

When it is not known whether infectors are present at an indoor event, all occupants must be considered possible infectors. We assume that the probability of an occupant being infectious is the same as the fraction of infectious people in the local population (ηI). H indicates the risk of an outbreak. Consequently, the risk also depends on the number of occupants in addition to the vocalization level, event duration, ventilation, and mask wearing. Jones et al. (26) estimated the dependency of the infection risk on these factors and tabulated it in a manner similar to Table 2. However, they only did so qualitatively. Having defined H as a risk parameter, we can assess the risk more quantitatively based on H values (as well as contact times allowed until outbreak risk is significant (H = 0.05 persons h2 m–3) and attack rates) under different conditions (Table 2). Although the actual risk also depends on ηI and the choice of the threshold for high risk (red cells in Table 2) is subjective, the risk parameter (H value) in Table 2 seems to vary in a smaller range than the corresponding table in the study by Jones et al. (26) We also show that being outdoors (with much better ventilation than indoors) has a greater expected benefit than they estimated.
Table 2. (a) Values of the Airborne Infection Risk Parameter (H, in Persons h2 m–3), (b) Exposure Times Corresponding to H = 0.05 Persons h2 m–3, and (c) Predicted Attack Rates with 0.1% Infectious People in Local Population for (Equivalent) Shared-Room Airborne Transmission under Different Conditions in the Similar Format of Figure 3 of ref (25).a
a

An additional type of activity (“heavy exercise”) is included. Table S3 details the specific choices of the conditions in Table 2. Note that these specifications can be changed as needed, which is easy to implement in the COVID-19 Aerosol Transmission Estimator (Figure S2). Color of a cell varies (a) with H value from green (0 persons h2 m–3) via yellow (0.05 persons h2 m–3) to red (≥0.5 persons h2 m–3), (b) with exposure time from red (0.1 h) via yellow (1 h) to green (10 h), and (c) with predicted attack rate from green (0) via yellow (0.0001) to red (0.001). The selection of the colors in Table 2a was based on the following considerations: (i) no risk (H = 0 persons h2 m–3) for green; (ii) no documented outbreaks when H < 0.05 persons h2 m–3 (Figure 1a) (thus 0.05 persons h2 m–3 for yellow); (iii) outbreaks with significant numbers of secondary infections when H ≥ 0.5 persons h2 m–3 (Figure 1a) (thus red). For that in Table 2b, relatively simple numbers are chosen for the thresholds that correspond to the thresholds for H in Table 2a. As probability of infection is given in Table 2c, its colors are chosen based on the personal risk tolerance of the authors. Note that significant uncertainties remain in the parameters for the table (which are for the wild-type SARS-CoV-2) and that the colors should be interpreted in relative terms. These tables are available in the online transmission risk estimator, and all of their aspects can be modified depending on specific situations and preferences.

Note that, although occupancy has no impact on the attack rate if an infector is present, occupancy affects the risk in two ways when the presence of infector(s) is unknown, that is, (i) the probability of the presence of an infector in a certain locality and (ii) the size (number of secondary cases) of the outbreak if it occurs. Therefore, lowering occupancy has double benefits.

Risk Evaluation for Indoor Spaces with Prepandemic and Mitigation Scenarios

Values of the risk parameter H for some typical public spaces under prepandemic conditions are tabulated in Table S4 and shown in Figure 2. H in all prepandemic settings is on the order of 0.05 persons h2 m–3 or higher, implying a significant risk of outbreak during the pandemic (Figure 2a). Often, ventilation rates may be lower than official guidance due to many factors including malfunction, lack of maintenance, or attempts to save energy. (80) Substandard ventilation, coupled with poor air distribution, substantially increases the risk and size of an outbreak through shared-room airborne transmission (Figure 2a,b). This is consistent with observations that indicate that COVID-19 outbreaks are disproportionately observed in poorly ventilated environments, which are specifically spaces with little to no added outdoor air or adequately filtered air. (81) However, H and Hr of all of the prepandemic spaces are in a regime highly sensitive to mitigation efforts (Figure 2a,b). Therefore, mitigation measures such as increasing ventilation or air cleaning, reducing voice volume when speaking, reducing occupancy, shortening duration of occupancy, and mask wearing are required to reduce the risk of transmission in similar settings (Table S4). With mitigation measures implemented, H in these settings can be lowered to the order of 0.01 persons h2 m–3, low enough to avoid major outbreaks (Figure 2a). Particularly, for hospital general examination room, a high-risk setting where there can be coughing infectors emitting quanta at a high rate, a combination of an improvement of ventilation rate to 6 h–1, application of higher efficiency air filters, a halved duration, and a requirement of fit-tested N95 respirators can lower the attack rate from ∼90% to negligible (Figure 2c). Use of high-quality masks (e.g., N95/FFP3) that fit well is highly effective as a mitigation measure.

Figure 2

Figure 2. (a and b) Same format as Figure 1, but for COVID-19 only. Also shown are the H and Hr values for several common indoor situations (both prepandemic and pandemic) listed in Table S4. The H values for the cases with prepandemic settings except for a lower occupancy and the H and Hr values for the ASHRAE standard cases (52) (not other cases or outbreaks) with prepandemic settings except for a lower ventilation rate are shown for comparison. The standalone legend box is for (a) and (b) only. (c) Approximately multiplicative effects of various mitigation measures for the hospital general examination room case are also shown as an example.

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Calculation of Risk Parameters for Specific Situations

The calculation of H, H′, and Hr for specific situations of interest has been implemented in the COVID-19 aerosol transmission estimator, which is freely available online. (31) The estimator is a series of spreadsheets that implement the same aerosol transmission model described by Miller et al. (11) It allows the user to make a copy into an online Google spreadsheet or download it as a Microsoft Excel file for adaptation to the situations of interest to each user. The model can be used to estimate the risk of specific situations, to explore the reduction in transmission because of different control measures (e.g., increased ventilation, masking, etc.), and to understand aerosol transmission modeling for incorporation into more complex models. The model also allows the estimation of the average CO2 concentration during an activity, as an additional indicator of indoor risk, and to facilitate the investigation of the relationship between infection risk and CO2 concentrations. (37,82) A screenshot of the estimator is shown in Figure S2.
In addition, a sheet allows recalculating Table 2 in this paper for sets of parameters different from those used here (and shown in Table S2).

Discussion

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We have explored the relationship between airborne infection transmission when sharing indoor spaces with distance between occupants greater than their breathing zones and the parameters of the space using a box/Wells–Riley model. We have derived an expression for the number of secondary infections and isolated the controllable terms in this expression in two airborne transmission risk parameters, H and Hr.
We find a consistent relationship, with increasing attack rate in the known COVID-19 outbreaks, as the value of Hr increases. This provides some confidence that airborne transmission is important in these outbreaks and that the models used here capture the key processes important for airborne transmission.
Outbreaks have been observed when Hr is on the order of 0.001 h2 m–3 and higher. A criterion based on Hr (e.g., Hr > 0.01 or 0.1 h2 m3, depending on available contact tracing resources) can also be used to determine if an occupant of an indoor space is a “close contact” of an identified infector in the same space through the shared-room air airborne transmission (note that this criterion does not apply to close contacts at risk of infection through short-range (<2 m) airborne transmission). The lowest H for the major COVID-19 outbreaks in indoor settings reported in the literature is ∼0.1 person h2 m–3. Note that all the outbreaks investigated here concern the early to mid-2020 variants of SARS-CoV-2, and a variant twice as contagious as those should reduce the tolerable values of the parameters by about a factor of 2. H can be orders of magnitude higher for the superspreading events where most attendees were infected (e.g., the Skagit Valley choir rehearsal). (11) However, if human activity-dependent factors are not taken into account, H′ for all the outbreaks discussed in this paper is ∼0.1–0.5 person h2 m–3. H′ values for public indoor spaces usually fall in or near this range primarily due to similar per-person ventilation rates and public event durations. Substandard ventilation, coupled with poor air distribution, is associated with substantial increases in the risk of outbreak. However, all of the prepandemic example spaces analyzed are in a regime in which they are highly sensitive to mitigation efforts.
The relative risk of COVID-19 infection falls between that of two well-known airborne diseases: the more transmissible measles and the less transmissible tuberculosis. This shows that the fact that COVID-19 is less transmissible than measles does not rule out airborne transmission. These risk parameters can be applied to other airborne diseases, if outbreaks are characterized in this framework. This approach may be useful in the design and renovation of building systems. For a novel disease that was as transmissible as measles, it would be very difficult to make any indoor activities safe aside from highly effective/protective vaccination.
Our analysis shows that mitigation measures to limit shared-room airborne transmission are needed in most indoor spaces whenever COVID-19 is spreading in a community. Among effective measures are reducing vocalization, avoiding intense physical activities, shortening the duration of occupancy, reducing the number of occupants, wearing high-quality well-fitting masks, increasing ventilation, improving ventilation effectiveness, and applying additional virus removal measures (such as HEPA filtration and UVGI disinfection). The use of multiple “layers of protection” is needed in many situations, while a single measure (e.g., masking) may not be able to reduce risk to low levels. We have shown that combinations of some or all of these measures are able to lower H close to 0.01 person h2 m–3, so that the expected number of secondary cases is substantially lower than 1 even in the presence of an infectious person, hence would be likely to avoid major outbreaks.

Supporting Information

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The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.est.1c06531.

  • Derivation of the factor accounting for the deviation from the steady state, details of Monte Carlo uncertainty propagation for the fitting of attack rates vs Hr, evaluation of the fitting in Figure 1b, rE and rB for different vocalization and physical intensity levels, details of the conditions for Table 2, details of the setting in Figure 2, and screenshot of the COVID-19 Aerosol Transmission Estimator (PDF)

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Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

Author Information

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  • Corresponding Author
  • Authors
    • Z. Peng - Dept. of Chemistry and CIRES, University of Colorado, Boulder, Colorado 80309, United States;  Orcidhttps://orcid.org/0000-0002-6823-452X
    • A.L. Pineda Rojas - CIMA, UMI-IFAECI/CNRS, FCEyN, Universidad de Buenos Aires─UBA/CONICET, Buenos Aires C1428EGA, Argentina
    • E. Kropff - Leloir Institute─IIBBA/CONICET, CBA, Buenos Aires C1405BWE, Argentina
    • W. Bahnfleth - Dept. of Architectural Engineering, The Pennsylvania State University, University Park, Pennsylvania 16802, United States
    • G. Buonanno - Dept. of Civil and Mechanical Engineering, University of Cassino and Southern Lazio, Cassino 03043, Italy
    • S.J. Dancer - Dept. of Microbiology, NHS Lanarkshire, Glasgow, Scotland G75 8RG, U.K.;  School of Applied Sciences, Edinburgh Napier University, Edinburgh, Scotland EH11 4BN, U.K.
    • J. Kurnitski - REHVA Technology and Research Committee, Tallinn University of Technology, Tallinn 19086, Estonia
    • Y. Li - Dept. of Mechanical Engineering, The University of Hong Kong, Hong Kong 999077, China
    • M.G.L.C. Loomans - Dept. of the Built Environment, Eindhoven University of Technology, Eindhoven 5612 AZ, The Netherlands
    • L.C. Marr - Dept. of Civil and Environmental Engineering, Virginia Tech, Blacksburg, Virginia 24061, United States;  Orcidhttps://orcid.org/0000-0003-3628-6891
    • L. Morawska - International Laboratory for Air Quality and Health, Queensland University of Technology, Brisbane, Queensland 4001, Australia;  Orcidhttps://orcid.org/0000-0002-0594-9683
    • W. Nazaroff - Dept. of Civil and Environmental Engineering, University of California, Berkeley, California 94720, United States;  Orcidhttps://orcid.org/0000-0001-5645-3357
    • C. Noakes - School of Civil Engineering, University of Leeds, Leeds LS2 9JT, U.K.
    • X. Querol - Institute of Environmental Assessment and Water Research, IDAEA, Spanish Research Council, CSIC, Barcelona 08034, Spain
    • C. Sekhar - Dept. of the Built Environment, National University of Singapore , 117566 Singapore
    • R. Tellier - Dept. of Medicine, McGill University and McGill University Health Centre, Montreal, Québec H4A 3J1, Canada
    • T. Greenhalgh - Nuffield Dept. of Primary Care Health Sciences, University of Oxford, Oxford OX2 6GG, U.K.
    • L. Bourouiba - The Fluid Dynamics of Disease Transmission Laboratory, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, United States
    • A. Boerstra - REHVA (Federation of European Heating, Ventilation and Air Conditioning Associations), BBA Binnenmilieu, The Hague 2501 CJ, The Netherlands
    • J.W. Tang - Dept. of Respiratory Sciences, University of Leicester, Leicester LE1 7RH, U.K.
    • S.L. Miller - Dept. of Mechanical Engineering, University of Colorado, Boulder, Colorado 80309, United States;  Orcidhttps://orcid.org/0000-0002-1967-7551
  • Notes
    The authors declare no competing financial interest.

    This paper has been previously submitted to medRxiv, a preprint server for Health Sciences. The preprint can be cited as: Z.P., A.L.P.R., E.K., W.B., G.B., S.J.D., J.K., Y.L., M.G.L.C.L., L.C.M., L.M., W.N., C.N., X.Q., C.S., R.T., T.G., L.B., A.B., J.W.T., S.L.M., J.L.J. Practical Indicators for Risk of Airborne Transmission in Shared Indoor Environments and their Application to COVID-19 Outbreaks. 2021, medRxiv. https://www.medrxiv.org/content/10.1101/2021.04.21.21255898 (accessed November 22, 2021).

Acknowledgments

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Z.P. and J.L.J. were partially supported by NSF AGS-1822664. T.G. was supported by ESRC ES/V010069/1. L.B. acknowledges CIHR and Fields, and NSF.

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    Because the detection of SARS-CoV-2 RNA in aerosols but failure to isolate viable (infectious) virus are commonly reported, there is substantial controversy whether severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) can be transmitted through aerosols. This conundrum occurs because common air samplers can inactivate virions through their harsh collection processes. We sought to resolve the question whether viable SARS-CoV-2 can occur in aerosols using VIVAS air samplers that operate on a gentle water vapor condensation principle. Air samples collected in the hospital room of 2 COVID-19 patients, 1 ready for discharge and the other newly admitted, were subjected to RT-qPCR and virus culture. The genomes of the SARS-CoV-2 collected from the air and isolated in cell culture were sequenced. Viable SARS-CoV-2 was isolated from air samples collected 2 to 4.8 m away from the patients. The genome sequence of the SARS-CoV-2 strain isolated from the material collected by the air samplers was identical to that isolated from the newly admitted patient. Ests. of viable viral concns. ranged 6-74 TCID50 units/L of air. Patients with respiratory manifestations of COVID-19 produce aerosols in the absence of aerosol-generating procedures that contain viable SARS-CoV-2, and these aerosols may serve as a source of transmission of the virus.
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  9. 9
    National Academies of Sciences, Engineering; Medicine; Others. Airborne Transmission of SARS-CoV-2: Proceedings of a Workshop in Brief; The National Academies Press: Washington, DC 2020.
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    There is no corresponding record for this reference.
  10. 10
    Prather, K. A.; Marr, L. C.; Schooley, R. T.; McDiarmid, M. A.; Wilson, M. E.; Milton, D. K. Airborne Transmission of SARS-CoV-2. Science 2020, 370, 303– 304,  DOI: 10.1126/science.abf0521
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    Airborne transmission of SARS-CoV-2
    Sills, Jennifer; Prather, Kimberly A.; Marr, Linsey C.; Schooley, Robert T.; McDiarmid, Melissa A.; Wilson, Mary E.; Milton, Donald K.
    Science (Washington, DC, United States) (2020), 370 (6514), 303-304CODEN: SCIEAS; ISSN:1095-9203. (American Association for the Advancement of Science)
    A review. There is overwhelming evidence that inhalation of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) represents a major transmission route for coronavirus disease 2019 (COVID-19). There is an urgent need to harmonize discussions about modes of virus transmission across disciplines to ensure the most effective control strategies and provide clear and consistent guidance to the public. To do so, we must clarify the terminol. to distinguish between aerosols and droplets using a size threshold of 100μm, not the historical 5μm. This size more effectively separates their aerodynamic behavior, ability to be inhaled, and efficacy of interventions. Viruses in aerosols (smaller than 100μm) can remain suspended in the air for many seconds to hours, like smoke, and be inhaled. They are highly concd. near an infected person, so they can infect people most easily in close proximity. But aerosols contg. infectious virus (2) can also travel more than 2 m and accumulate in poorly ventilated indoor air, leading to superspreading events. Individuals with COVID-19, many of whom have no symptoms, release thousands of virus-laden aerosols and far fewer droplets when breathing and talking. Thus, one is far more likely to inhale aerosols than be sprayed by a droplet, and so the balance of attention must be shifted to protecting against airborne transmission.
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  11. 11
    Miller, S. L.; Nazaroff, W. W.; Jimenez, J. L.; Boerstra, A.; Buonanno, G.; Dancer, S. J.; Kurnitski, J.; Marr, L. C.; Morawska, L.; Noakes, C. Transmission of SARS-CoV-2 by Inhalation of Respiratory Aerosol in the Skagit Valley Chorale Superspreading Event. Indoor Air 2021, 31, 314– 323,  DOI: 10.1111/ina.12751
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    11
    Transmission of SARS-CoV-2 by inhalation of respiratory aerosol in the Skagit Valley Chorale superspreading event
    Miller, Shelly L.; Nazaroff, William W.; Jimenez, Jose L.; Boerstra, Atze; Buonanno, Giorgio; Dancer, Stephanie J.; Kurnitski, Jarek; Marr, Linsey C.; Morawska, Lidia; Noakes, Catherine
    Indoor Air (2021), 31 (2), 314-323CODEN: INAIE5; ISSN:1600-0668. (Wiley-Blackwell)
    During the 2020 COVID-19 pandemic, an outbreak occurred following attendance of a symptomatic index case at a weekly rehearsal on 10 March of the Skagit Valley Chorale (SVC). After that rehearsal, 53 members of the SVC among 61 in attendance were confirmed or strongly suspected to have contracted COVID-19 and two died. Transmission by the aerosol route is likely; it appears unlikely that either fomite or ballistic droplet transmission could explain a substantial fraction of the cases. It is vital to identify features of cases such as this to better understand the factors that promote superspreading events. Based on a conditional assumption that transmission during this outbreak was dominated by inhalation of respiratory aerosol generated by one index case, we use the available evidence to infer the emission rate of aerosol infectious quanta. We explore how the risk of infection would vary with several influential factors: ventilation rate, duration of event, and deposition onto surfaces. The results indicate a best-est. emission rate of 970 ± 390 quanta/h. Infection risk would be reduced by a factor of two by increasing the aerosol loss rate to 5 h-1 and shortening the event duration from 2.5 to 1 h.
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    Greenhalgh, T.; Jimenez, J. L.; Prather, K. A.; Tufekci, Z.; Fisman, D.; Schooley, R. Ten Scientific Reasons in Support of Airborne Transmission of SARS-CoV-2. Lancet 2021, 397, 1603– 1605,  DOI: 10.1016/S0140-6736(21)00869-2
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    Ten scientific reasons in support of airborne transmission of SARS-CoV-2
    Greenhalgh, Trisha; Jimenez, Jose L.; Prather, Kimberly A.; Tufekci, Zeynep; Fisman, David; Schooley, Robert
    Lancet (2021), 397 (10285), 1603-1605CODEN: LANCAO; ISSN:0140-6736. (Elsevier Ltd.)
    Heneghan and colleagues' systematic review, funded by WHO, published in March, 2021, as a preprint, states: "The lack of recoverable viral culture samples of SARS-CoV-2 prevents firm conclusions to be drawn about airborne transmission" (F1000Research 2021; published online March 24. https://doi.org/10.12688/f1000research.52091.1 (preprint). This conclusion, and the wide circulation of the review's findings, is concerning because of the public health implications. In this report, ten streams of evidence that collectively support the hypothesis that SARS-CoV-2 is transmitted primarily by the airborne route is presented. The authors propose that it is a scientific error to use lack of direct evidence of SARS-CoV-2 in some air samples to cast doubt on airborne transmission while overlooking the quality and strength of the overall evidence base. There is consistent, strong evidence that SARS-CoV-2 spreads by airborne transmission. Although other routes can contribute, we believe that the airborne route is likely to be dominant. The public health community should act accordingly and without further delay.
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    Tang, J. W.; Marr, L. C.; Li, Y.; Dancer, S. J. Covid-19 Has Redefined Airborne Transmission. BMJ 2021, 373, n913,  DOI: 10.1136/bmj.n913
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    Gelfand, H. M.; Posch, J. The Recent Outbreak of Smallpox in Meschede, West Germany. Am. J. Epidemiol. 1971, 93, 234– 237,  DOI: 10.1093/oxfordjournals.aje.a121251
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    The recent outbreak of smallpox in Meschede, West Germany
    Gelfand H M; Posch J
    American journal of epidemiology (1971), 93 (4), 234-7 ISSN:0002-9262.
    There is no expanded citation for this reference.
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    Yu, I. T. S.; Li, Y.; Wong, T. W.; Tam, W.; Chan, A. T.; Lee, J. H. W.; Leung, D. Y. C.; Ho, T. Evidence of Airborne Transmission of the Severe Acute Respiratory Syndrome Virus. N. Engl. J. Med. 2004, 350, 1731– 1739,  DOI: 10.1056/NEJMoa032867
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    Evidence of airborne transmission of the severe acute respiratory syndrome virus
    Yu, Ignatius T. S.; Li, Yuguo; Wong, Tze Wai; Tam, Wilson; Chan, Andy T.; Lee, Joseph H. W.; Leung, Dennis Y. C.; Ho, Tommy
    New England Journal of Medicine (2004), 350 (17), 1731-1739CODEN: NEJMAG; ISSN:0028-4793. (Massachusetts Medical Society)
    BACKGROUND: There is uncertainty about the mode of transmission of the severe acute respiratory syndrome (SARS) virus. We analyzed the temporal and spatial distributions of cases in a large community outbreak of SARS in Hong Kong and examd. the correlation of these data with the three-dimensional spread of a virus-laden aerosol plume that was modeled using studies of airflow dynamics. METHODS: We detd. the distribution of the initial 187 cases of SAWS in the Amoy Gardens housing complex in 2003 according to the date of onset and location of residence. We then studied the assocn. between the location (building, floor, and direction the apartment unit faced) and the probability of infection using logistic regression. The spread of the airborne, virus-laden aerosols generated by the index patient was modeled with the use of airflow-dynamics studies, including studies performed with the use of computational fluid-dynamics and multizone modeling. RESULTS: The curves of the epidemic suggested a common source of the outbreak. All but 5 patients lived in seven buildings (A to G), and the index patient and more than half the other patients with SAWS (99 patients) lived in building E. Residents of the floors at the middle and upper levels in building E were at a significantly higher risk than residents on lower floors; this finding is consistent with a rising plume of contaminated warm air in the air shaft generated from a middle-level apartment unit. The risks for the different units matched the virus concns. predicted with the use of multizone modeling. The distribution of risk in buildings B, C, and D corresponded well with the three-dimensional spread of virus-laden aerosols predicted with the use of computational fluid-dynamics modeling. CONCLUSIONS: Airborne spread of the virus appears to explain this large community outbreak of SARS, and future efforts at prevention and control must take into consideration the potential for airborne spread of this virus.
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    Dick, E. C.; Jennings, L. C.; Mink, K. A.; Wartgow, C. D.; Inborn, S. L. Aerosol Transmission of Rhinovirus Colds. J. Infect. Dis. 1987, 156, 442– 448,  DOI: 10.1093/infdis/156.3.442
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    Aerosol transmission of rhinovirus colds
    Dick E C; Jennings L C; Mink K A; Wartgow C D; Inhorn S L
    The Journal of infectious diseases (1987), 156 (3), 442-8 ISSN:0022-1899.
    Rhinovirus infections may spread by aerosol, direct contact, or indirect contact involving environmental objects. We examined aerosol and indirect contact in transmission of rhinovirus type 16 colds between laboratory-infected men (donors) and susceptible men (recipients) who played cards together for 12 hr. In three experiments the infection rate of restrained recipients (10 [56%] of 18), who could not touch their faces and could only have been infected by aerosols, and that of unrestrained recipients (12[67%] of 18), who could have been infected by aerosol, by direct contact, or by indirect fomite contact, was not significantly different (chi 2 = 0.468, P = .494). In a fourth experiment, transmission via fomites heavily used for 12 hr by eight donors was the only possible route of spread, and no transmissions occurred among 12 recipients (P less than .001 by two-tailed Fisher's exact test). These results suggest that contrary to current opinion, rhinovirus transmission, at least in adults, occurs chiefly by the aerosol route.
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    Chen, W.; Zhang, N.; Wei, J.; Yen, H.-L.; Li, Y. Short-Range Airborne Route Dominates Exposure of Respiratory Infection during Close Contact. Build. Environ. 2020, 176, 106859  DOI: 10.1016/j.buildenv.2020.106859
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    Katelaris, A. L.; Wells, J.; Clark, P.; Norton, S.; Rockett, R.; Arnott, A.; Sintchenko, V.; Corbett, S.; Bag, S. K. Epidemiologic Evidence for Airborne Transmission of SARS-CoV-2 during Church Singing, Australia, 2020. Emerg. Infect. Dis. 2021, 27, 1677– 1680,  DOI: 10.3201/eid2706.210465
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    Epidemiologic Evidence for Airborne Transmission of SARS-CoV-2 during Church Singing, Australia, 2020
    Katelaris Anthea L; Wells Jessica; Clark Penelope; Norton Sophie; Rockett Rebecca; Arnott Alicia; Sintchenko Vitali; Corbett Stephen; Bag Shopna K
    Emerging infectious diseases (2021), 27 (6), 1677-1680 ISSN:.
    An outbreak of severe acute respiratory syndrome coronavirus 2 infection occurred among church attendees after an infectious chorister sang at multiple services. We detected 12 secondary case-patients. Video recordings of the services showed that case-patients were seated in the same section, up to 15 m from the primary case-patient, without close physical contact, suggesting airborne transmission.
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  19. 19
    Shen, Y.; Li, C.; Dong, H.; Wang, Z.; Martinez, L.; Sun, Z.; Handel, A.; Chen, Z.; Chen, E.; Ebell, M. H.; Wang, F.; Yi, B.; Wang, H.; Wang, X.; Wang, A.; Chen, B.; Qi, Y.; Liang, L.; Li, Y.; Ling, F.; Chen, J.; Xu, G. Community Outbreak Investigation of SARS-CoV-2 Transmission Among Bus Riders in Eastern China. JAMA Intern. Med. 2020, 180, 1665– 1671,  DOI: 10.1001/jamainternmed.2020.5225
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    Community outbreak investigation of SARS-CoV-2 transmission among bus riders in Eastern China
    Shen, Ye; Li, Changwei; Dong, Hongjun; Wang, Zhen; Martinez, Leonardo; Sun, Zhou; Handel, Andreas; Chen, Zhiping; Chen, Enfu; Ebell, Mark H.; Wang, Fan; Yi, Bo; Wang, Haibin; Wang, Xiaoxiao; Wang, Aihong; Chen, Bingbing; Qi, Yanling; Liang, Lirong; Li, Yang; Ling, Feng; Chen, Junfang; Xu, Guozhang
    JAMA Internal Medicine (2020), 180 (12), 1665-1671CODEN: JIMACF; ISSN:2168-6114. (American Medical Association)
    Importance Evidence of whether severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the virus that causes coronavirus disease 2019 (COVID-19), can be transmitted as an aerosol (ie, airborne) has substantial public health implications. Objective To investigate potential transmission routes of SARS-CoV-2 infection with epidemiol. evidence from a COVID-19 outbreak. Design, setting, and participants This cohort study examd. a community COVID-19 outbreak in Zhejiang province. On Jan. 19, 2020, 128 individuals took 2 buses (60 [46.9%] from bus 1 and 68 [53.1%] from bus 2) on a 100-min round trip to attend a 150-min worship event. The source patient was a passenger on bus 2. We compared risks of SARS-CoV-2 infection among at-risk individuals taking bus 1 (n = 60) and bus 2 (n = 67 [source patient excluded]) and among all other individuals (n = 172) attending the worship event. We also divided seats on the exposed bus into high-risk and low-risk zones according to the distance from the source patient and compared COVID-19 risks in each zone. In both buses, central air conditioners were in indoor recirculation mode. Main outcomes and measures SARS-CoV-2 infection was confirmed by reverse transcription polymerase chain reaction or by viral genome sequencing results. Attack rates for SARS-CoV-2 infection were calcd. for different groups, and the spatial distribution of individuals who developed infection on bus 2 was obtained. Results Of the 128 participants, 15 (11.7%) were men, 113 (88.3%) were women, and the mean age was 58.6 years. On bus 2, 24 of the 68 individuals (35.3% [including the index patient]) received a diagnosis of COVID-19 after the event. Meanwhile, none of the 60 individuals in bus 1 were infected. Among the other 172 individuals at the worship event, 7 (4.1%) subsequently received a COVID-19 diagnosis. Individuals in bus 2 had a 34.3% (95% CI, 24.1%-46.3%) higher risk of getting COVID-19 compared with those in bus 1 and were 11.4 (95% CI, 5.1-25.4) times more likely to have COVID-19 compared with all other individuals attending the worship event. Within bus 2, individuals in high-risk zones had moderately, but nonsignificantly, higher risk for COVID-19 compared with those in the low-risk zones. The absence of a significantly increased risk in the part of the bus closer to the index case suggested that airborne spread of the virus may at least partially explain the markedly high attack rate obsd. Conclusions and relevance In this cohort study and case investigation of a community outbreak of COVID-19 in Zhejiang province, individuals who rode a bus to a worship event with a patient with COVID-19 had a higher risk of SARS-CoV-2 infection than individuals who rode another bus to the same event. Airborne spread of SARS-CoV-2 seems likely to have contributed to the high attack rate in the exposed bus. Future efforts at prevention and control must consider the potential for airborne spread of the virus.
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    Kwon, K. S.; Park, J. I.; Park, Y. J.; Jung, D. M.; Ryu, K. W.; Lee, J. H. Evidence of Long-Distance Droplet Transmission of SARS-CoV-2 by Direct Air Flow in a Restaurant in Korea. J. Korean Med. Sci. 2020, 35, e415  DOI: 10.3346/jkms.2020.35.e415
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    Evidence of long-distance droplet transmission of SARS-COV-2 by direct air flow in a restaurant in Korea
    Kwon, Keun-Sang; Park, Jung-Im; Park, Young Joon; Jung, Don-Myung; Ryu, Ki-Wahn; Lee, Ju-Hyung
    Journal of Korean Medical Science (2020), 35 (46), e415CODEN: JKMSEH; ISSN:1598-6357. (Korean Academy of Medical Sciences)
    The transmission mode of severe acute respiratory syndrome coronavirus 2 is primarily known as droplet transmission. However, a recent argument has emerged about the possibility of airborne transmission. On June 17, there was a coronavirus disease 2019 (COVID-19) outbreak in Korea assocd. with long distance droplet transmission. The epidemiol. investigation was implemented based on personal interviews and data collection on closed-circuit television images, and cell phone location data. The epidemic investigation support system developed by the Korea Disease Control and Prevention Agency was used for contact tracing. At the restaurant considered the site of exposure, air flow direction and velocity, distances between cases, and movement of visitors were investigated. A total of 3 cases were identified in this outbreak, and max. air flow velocity of 1.2 m/s was measured between the infector and infectee in a restaurant equipped with ceiling-type air conditioners. The index case was infected at a 6.5 m away from the infector and 5 min exposure without any direct or indirect contact. Droplet transmission can occur at a distance greater than 2 m if there is direct air flow from an infected person. Therefore, updated guidelines involving prevention, contact tracing, and quarantine for COVID-19 are required for control of this highly contagious disease.
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    Jang, S.; Han, S. H.; Rhee, J. Y. Cluster of Coronavirus Disease Associated with Fitness Dance Classes, South Korea. Emerg. Infect. Dis. 2020, 26, 1917– 1920,  DOI: 10.3201/eid2608.200633
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    21
    Cluster of coronavirus disease associated with fitness dance classes, South Korea
    Jang, Sukbin; Han, Si Hyun; Rhee, Ji-Young
    Emerging Infectious Diseases (2020), 26 (8), 1917-1920CODEN: EIDIFA; ISSN:1080-6059. (Centers for Disease Control and Prevention)
    During 24 days in Cheonan, South Korea, 112 persons were infected with severe acute respiratory syndrome coronavirus 2 assocd. with fitness dance classes at 12 sports facilities. Intense phys. exercise in densely populated sports facilities could increase risk for infection. Vigorous exercise in confined spaces should be minimized during outbreaks.
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    Eichler, N.; Thornley, C.; Swadi, T.; Devine, T.; McElnay, C.; Sherwood, J.; Brunton, C.; Williamson, F.; Freeman, J.; Berger, S.; Ren, X.; Storey, M.; de Ligt, J.; Geoghegan, J. L. Transmission of Severe Acute Respiratory Syndrome Coronavirus 2 during Border Quarantine and Air Travel, New Zealand (Aotearoa). Emerg. Infect. Dis. 2021, 27, 1274– 1278,  DOI: 10.3201/eid2705.210514
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    22
    Transmission of severe acute respiratory syndrome coronavirus 2 during border quarantine and air travel, New Zealand (Aotearoa)
    Eichler, Nick; Thornley, Craig; Swadi, Tara; Devine, Tom; McElnay, Caroline; Sherwood, Jillian; Brunton, Cheryl; Williamson, Felicity; Freeman, Josh; Berger, Sarah; Ren, Xiaoyun; Storey, Matt; de Ligt, Joep; Geoghegan, Jemma L.
    Emerging Infectious Diseases (2021), 27 (5), 1274-1278CODEN: EIDIFA; ISSN:1080-6059. (Centers for Disease Control and Prevention)
    The strategy in New Zealand (Aotearoa) to eliminate coronavirus disease requires that international arrivals undergo managed isolation and quarantine and mandatory testing for severe acute respiratory syndrome coronavirus 2. Combining genomic and epidemiol. data, we investigated the origin of an acute case of coronavirus disease identified in the community after the patient had spent 14 days in managed isolation and quarantine and had 2 neg. test results. By combining genomic sequence anal. and epidemiol. investigations, we identified a multibranched chain of transmission of this virus, including on international and domestic flights, as well as a probable case of aerosol transmission without direct person-to-person contact. These findings show the power of integrating genomic and epidemiol. data to inform outbreak investigations.
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    Nissen, K.; Krambrich, J.; Akaberi, D.; Hoffman, T.; Ling, J.; Lundkvist, Å.; Svensson, L.; Salaneck, E. Long-Distance Airborne Dispersal of SARS-CoV-2 in COVID-19 Wards. Sci. Rep. 2020, 10, 19589,  DOI: 10.1038/s41598-020-76442-2
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    Long-distance airborne dispersal of SARS-CoV-2 in COVID-19 wards
    Nissen, Karolina; Krambrich, Janina; Akaberi, Dario; Hoffman, Tove; Ling, Jiaxin; Lundkvist, Aake; Svensson, Lennart; Salaneck, Erik
    Scientific Reports (2020), 10 (1), 19589CODEN: SRCEC3; ISSN:2045-2322. (Nature Research)
    Abstr.: Evidence suggests that SARS-CoV-2, as well as other coronaviruses, can be dispersed and potentially transmitted by aerosols directly or via ventilation systems. We therefore investigated ventilation openings in one COVID-19 ward and central ducts that expel indoor air from three COVID-19 wards at Uppsala University Hospital, Sweden, during Apr. and May 2020. Swab samples were taken from individual ceiling ventilation openings and surfaces in central ducts. Samples were subsequently subjected to rRT-PCR targeting the N and E genes of SARS-CoV-2. Central ventilation HEPA filters, located several stories above the wards, were removed and portions analyzed in the same manner. In two subsequent samplings, SARS-CoV-2 N and E genes were detected in seven and four out of 19 room vents, resp. Central ventilation HEPA exhaust filters from the ward were found pos. for both genes in three samples. Corresponding filters from two other, adjacent COVID-19 wards were also found pos. Infective ability of the samples was assessed by inoculation of susceptible cell cultures but could not be detd. in these expts. Detection of SARS-CoV-2 in central ventilation systems, distant from patient areas, indicate that virus can be transported long distances and that droplet transmission alone cannot reasonably explain this, esp. considering the relatively low air change rates in these wards. Airborne transmission of SARS-CoV-2 must be taken into consideration for preventive measures.
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    Hwang, S. E.; Chang, J. H.; Oh, B.; Heo, J. Possible Aerosol Transmission of COVID-19 Associated with an Outbreak in an Apartment in Seoul, South Korea, 2020. Int. J. Infect. Dis. 2021, 104, 73– 76,  DOI: 10.1016/j.ijid.2020.12.035
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    24
    Possible aerosol transmission of COVID-19 associated with an outbreak in an apartment in Seoul, South Korea, 2020
    Hwang, Seo Eun; Chang, Je Hwan; Oh, Bumjo; Heo, Jongho
    International Journal of Infectious Diseases (2021), 104 (), 73-76CODEN: IJIDF3; ISSN:1201-9712. (Elsevier Ltd.)
    Scientists have strongly implied that aerosols could be the plausible cause of coronavirus disease-2019 (COVID-19) transmission; however, aerosol transmission remains controversial. We investigated the epidemiol. relationship among infected cases on a recent cluster infection of COVID-19 in an apartment building in Seoul, South Korea. All infected cases were found along two vertical lines of the building, and each line was connected through a single air duct in the bathroom for natural ventilation. Our investigation found no other possible contact between the cases than the airborne infection through a single air duct in the bathroom. The virus from the first infected case can be spread to upstairs and downstairs through the air duct by the (reverse) stack effect, which explains the air movement in a vertical shaft. This study suggests aerosol transmission, particularly indoors with insufficient ventilation, which is underappreciated.
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    Li, Y.; Leung, G. M.; Tang, J. W.; Yang, X.; Chao, C. Y. H.; Lin, J. Z.; Lu, J. W.; Nielsen, P. V.; Niu, J.; Qian, H.; Sleigh, A. C.; Su, H.-J. J.; Sundell, J.; Wong, T. W.; Yuen, P. L. Role of Ventilation in Airborne Transmission of Infectious Agents in the Built Environment - a Multidisciplinary Systematic Review. Indoor Air 2007, 17, 2– 18,  DOI: 10.1111/j.1600-0668.2006.00445.x
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    Role of ventilation in airborne transmission of infectious agents in the built environment - a multidisciplinary systematic review
    Li Y; Leung G M; Tang J W; Yang X; Chao C Y H; Lin J Z; Lu J W; Nielsen P V; Niu J; Qian H; Sleigh A C; Su H-J J; Sundell J; Wong T W; Yuen P L
    Indoor air (2007), 17 (1), 2-18 ISSN:0905-6947.
    There have been few recent studies demonstrating a definitive association between the transmission of airborne infections and the ventilation of buildings. The severe acute respiratory syndrome (SARS) epidemic in 2003 and current concerns about the risk of an avian influenza (H5N1) pandemic, have made a review of this area timely. We searched the major literature databases between 1960 and 2005, and then screened titles and abstracts, and finally selected 40 original studies based on a set of criteria. We established a review panel comprising medical and engineering experts in the fields of microbiology, medicine, epidemiology, indoor air quality, building ventilation, etc. Most panel members had experience with research into the 2003 SARS epidemic. The panel systematically assessed 40 original studies through both individual assessment and a 2-day face-to-face consensus meeting. Ten of 40 studies reviewed were considered to be conclusive with regard to the association between building ventilation and the transmission of airborne infection. There is strong and sufficient evidence to demonstrate the association between ventilation, air movements in buildings and the transmission/spread of infectious diseases such as measles, tuberculosis, chickenpox, influenza, smallpox and SARS. There is insufficient data to specify and quantify the minimum ventilation requirements in hospitals, schools, offices, homes and isolation rooms in relation to spread of infectious diseases via the airborne route. PRACTICAL IMPLICATION: The strong and sufficient evidence of the association between ventilation, the control of airflow direction in buildings, and the transmission and spread of infectious diseases supports the use of negatively pressurized isolation rooms for patients with these diseases in hospitals, in addition to the use of other engineering control methods. However, the lack of sufficient data on the specification and quantification of the minimum ventilation requirements in hospitals, schools and offices in relation to the spread of airborne infectious diseases, suggest the existence of a knowledge gap. Our study reveals a strong need for a multidisciplinary study in investigating disease outbreaks, and the impact of indoor air environments on the spread of airborne infectious diseases.
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  26. 26
    Jones, N. R.; Qureshi, Z. U.; Temple, R. J.; Larwood, J. P. J.; Greenhalgh, T.; Bourouiba, L. Two Metres or One: What Is the Evidence for Physical Distancing in Covid-19?. BMJ 2020, 370, m3223  DOI: 10.1136/bmj.m3223
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    Morawska, L.; Tang, J. W.; Bahnfleth, W.; Bluyssen, P. M.; Boerstra, A.; Buonanno, G.; Cao, J.; Dancer, S.; Floto, A.; Franchimon, F.; Haworth, C.; Hogeling, J.; Isaxon, C.; Jimenez, J. L.; Kurnitski, J.; Li, Y.; Loomans, M.; Marks, G.; Marr, L. C.; Mazzarella, L.; Melikov, A. K.; Miller, S.; Milton, D. K.; Nazaroff, W.; Nielsen, P. V.; Noakes, C.; Peccia, J.; Querol, X.; Sekhar, C.; Seppänen, O.; Tanabe, S.-I.; Tellier, R.; Tham, K. W.; Wargocki, P.; Wierzbicka, A.; Yao, M. How Can Airborne Transmission of COVID-19 Indoors Be Minimised?. Environ. Int. 2020, 142, 105832  DOI: 10.1016/j.envint.2020.105832
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    27
    How can airborne transmission of COVID-19 indoors be minimized?
    Morawska, Lidia; Tang, Julian W.; Bahnfleth, William; Bluyssen, Philomena M.; Boerstra, Atze; Buonanno, Giorgio; Cao, Junji; Dancer, Stephanie; Floto, Andres; Franchimon, Francesco; Haworth, Charles; Hogeling, Jaap; Isaxon, Christina; Jimenez, Jose L.; Kurnitski, Jarek; Li, Yuguo; Loomans, Marcel; Marks, Guy; Marr, Linsey C.; Mazzarella, Livio; Melikov, Arsen Krikor; Miller, Shelly; Milton, Donald K.; Nazaroff, William; Nielsen, Peter V.; Noakes, Catherine; Peccia, Jordan; Querol, Xavier; Sekhar, Chandra; Seppanen, Olli; Tanabe, Shin-ichi; Tellier, Raymond; Tham, Kwok Wai; Wargocki, Pawel; Wierzbicka, Aneta; Yao, Maosheng
    Environment International (2020), 142 (), 105832CODEN: ENVIDV; ISSN:0160-4120. (Elsevier Ltd.)
    During the rapid rise in COVID-19 illnesses and deaths globally, and notwithstanding recommended precautions, questions are voiced about routes of transmission for this pandemic disease. Inhaling small airborne droplets is probable as a third route of infection, in addn. to more widely recognized transmission via larger respiratory droplets and direct contact with infected people or contaminated surfaces. While uncertainties remain regarding the relative contributions of the different transmission pathways, we argue that existing evidence is sufficiently strong to warrant engineering controls targeting airborne transmission as part of an overall strategy to limit infection risk indoors. Appropriate building engineering controls include sufficient and effective ventilation, possibly enhanced by particle filtration and air disinfection, avoiding air recirculation and avoiding overcrowding. Often, such measures can be easily implemented and without much cost, but if only they are recognized as significant in contributing to infection control goals. We believe that the use of engineering controls in public buildings, including hospitals, shops, offices, schools, kindergartens, libraries, restaurants, cruise ships, elevators, conference rooms or public transport, in parallel with effective application of other controls (including isolation and quarantine, social distancing and hand hygiene), would be an addnl. important measure globally to reduce the likelihood of transmission and thereby protect healthcare workers, patients and the general public.
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  28. 28
    Bond, T. C.; Bosco-Lauth, A.; Farmer, D. K.; Francisco, P. W.; Pierce, J. R.; Fedak, K. M.; Ham, J. M.; Jathar, S. H.; VandeWoude, S. Quantifying Proximity, Confinement, and Interventions in Disease Outbreaks: A Decision Support Framework for Air-Transported Pathogens. Environ. Sci. Technol. 2021, 55, 2890– 2898,  DOI: 10.1021/acs.est.0c07721
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    28
    Quantifying Proximity, Confinement, and Interventions in Disease Outbreaks: A Decision Support Framework for Air-Transported Pathogens
    Bond, Tami C.; Bosco-Lauth, Angela; Farmer, Delphine K.; Francisco, Paul W.; Pierce, Jeffrey R.; Fedak, Kristen M.; Ham, Jay M.; Jathar, Shantanu H.; VandeWoude, Sue
    Environmental Science & Technology (2021), 55 (5), 2890-2898CODEN: ESTHAG; ISSN:0013-936X. (American Chemical Society)
    The inability to communicate how infectious diseases are transmitted in human environments has triggered avoidance of interactions during the COVID-19 pandemic. We define a metric, Effective ReBreathed Vol. (ERBV), that encapsulates how infectious pathogens, including SARS-CoV-2, transport in air. ERBV separates environmental transport from other factors in the chain of infection, allowing quant. comparisons among situations. Particle size affects transport, removal onto surfaces, and elimination by mitigation measures, so ERBV is presented for a range of exhaled particle diams.: 1, 10, and 100μm. Pathogen transport depends on both proximity and confinement. If interpersonal distancing of 2 m is maintained, then confinement, not proximity, dominates rebreathing after 10-15 min in enclosed spaces for all but 100μm particles. We analyze strategies to reduce this confinement effect. Ventilation and filtration reduce person-to-person transport of 1μm particles (ERBV1) by 13-85% in residential and office situations. Deposition to surfaces competes with intentional removal for 10 and 100μm particles, so the same interventions reduce ERBV10 by only 3-50%, and ERBV100 is unaffected. Prior knowledge of size-dependent ERBV would help identify transmission modes and effective interventions. This framework supports mitigation decisions in emerging situations, even before other infectious parameters are known.
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    Riley, E. C.; Murphy, G.; Riley, R. L. Airborne Spread of Measles in a Suburban Elementary School. Am. J. Epidemiol. 1978, 107, 421– 432,  DOI: 10.1093/oxfordjournals.aje.a112560
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    Airborne spread of measles in a suburban elementary school
    Riley E C; Murphy G; Riley R L
    American journal of epidemiology (1978), 107 (5), 421-32 ISSN:0002-9262.
    A measles epidemic in a modern suburban elementary school in upstate New York in spring, 1974, is analyzed in terms of a model which provides a basis for apportioning the chance of infection from classmates sharing the same home room, from airborne organisms recirculated by the ventilating system, and from exposure in school buses. The epidemic was notable because of its explosive nature and its occurrence in a school where 97% of the children had been vaccinated. Many had been vaccinated at less than one year of age. The index case was a girl in second grade who produced 28 secondary cases in 14 different classrooms. Organisms recirculated by the ventilating system were strongly implicated. After two subsequent generations, 60 children had been infected, and the epidemic subsided. From estimates of major physical and biologic factors, it was possible to calculate that the index case produced approximately 93 units of airborne infection (quanta) per minute. The epidemic pattern suggested that the secondaries were less infectious by an order of magnitude. The exceptional infectiousness of the index case, inadequate immunization of many of the children, and the high percentage of air recirculated throughout the school, are believed to account for the extent and sharpness of the outbreak.
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    Noakes, C. J.; Sleigh, P. A. Mathematical Models for Assessing the Role of Airflow on the Risk of Airborne Infection in Hospital Wards. J. R. Soc. Interface. 2009, 6 Suppl 6, S791,  DOI: 10.1098/rsif.2009.0305.focus
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    Jimenez, J. L.; Peng, Z. COVID-19 Aerosol Transmission Estimator https://tinyurl.com/covid-estimator (accessed Mar 26, 2021).
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    Buonanno, G.; Morawska, L.; Stabile, L. Quantitative Assessment of the Risk of Airborne Transmission of SARS-CoV-2 Infection: Prospective and Retrospective Applications. Environ. Int. 2020, 145, 106112  DOI: 10.1016/j.envint.2020.106112
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    Quantitative assessment of the risk of airborne transmission of SARS-CoV-2 infection: Prospective and retrospective applications
    Buonanno, G.; Morawska, L.; Stabile, L.
    Environment International (2020), 145 (), 106112CODEN: ENVIDV; ISSN:0160-4120. (Elsevier Ltd.)
    Airborne transmission is a recognized pathway of contagion; however, it is rarely quant. evaluated. The numerous outbreaks that have occurred during the SARS-CoV-2 pandemic are putting a demand on researchers to develop approaches capable of both predicting contagion in closed environments (predictive assessment) and analyzing previous infections (retrospective assessment). This study presents a novel approach for quant. assessment of the individual infection risk of susceptible subjects exposed in indoor microenvironments in the presence of an asymptomatic infected SARS-CoV-2 subject. The application of a Monte Carlo method allowed the risk for an exposed healthy subject to be evaluated or, starting from an acceptable risk, the max. exposure time. We applied the proposed approach to four distinct scenarios for a prospective assessment, highlighting that, in order to guarantee an acceptable risk of 10-3 for exposed subjects in naturally ventilated indoor environments, the exposure time could be well below one hour. Such max. exposure time clearly depends on the viral load emission of the infected subject and on the exposure conditions; thus, longer exposure times were estd. for mech. ventilated indoor environments and lower viral load emissions. The proposed approach was used for retrospective assessment of documented outbreaks in a restaurant in Guangzhou (China) and at a choir rehearsal in Mount Vernon (USA), showing that, in both cases, the high attack rate values can be justified only assuming the airborne transmission as the main route of contagion. Moreover, we show that such outbreaks are not caused by the rare presence of a superspreader, but can be likely explained by the co-existence of conditions, including emission and exposure parameters, leading to a highly probable event, which can be defined as a "superspreading event".
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  33. 33
    Lelieveld, J.; Helleis, F.; Borrmann, S.; Cheng, Y.; Drewnick, F.; Haug, G.; Klimach, T.; Sciare, J.; Su, H.; Pöschl, U. Model Calculations of Aerosol Transmission and Infection Risk of COVID-19 in Indoor Environments. Int. J. Environ. Res. Public Health 2020, 17, 8114,  DOI: 10.3390/ijerph17218114
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    Model Calculations of Aerosol Transmission and Infection Risk of COVID-19 in indoor environments
    Lelieveld, Jos; Helleis, Frank; Borrmann, Stephan; Cheng, Yafang; Drewnick, Frank; Haug, Gerald; Klimach, Thomas; Sciare, Jean; Su, Hang; Poeschl, Ulrich
    International Journal of Environmental Research and Public Health (2020), 17 (21), 8114CODEN: IJERGQ; ISSN:1660-4601. (MDPI AG)
    The role of aerosolized SARS-CoV-2 viruses in airborne transmission of COVID-19 has been debated. The aerosols are transmitted through breathing and vocalization by infectious subjects. Some authors state that this represents the dominant route of spreading, while others dismiss the option. Here we present an adjustable algorithm to est. the infection risk for different indoor environments, constrained by published data of human aerosol emissions, SARS-CoV-2 viral loads, infective dose and other parameters. We evaluate typical indoor settings such as an office, a classroom, choir practice, and a reception/party. Our results suggest that aerosols from highly infective subjects can effectively transmit COVID-19 in indoor environments. This "highly infective" category represents approx. 20% of the patients who tested pos. for SARS-CoV-2. We find that "super infective" subjects, representing the top 5-10% of subjects with a pos. test, plus an unknown fraction of less-but still highly infective, high aerosol-emitting subjects-may cause COVID-19 clusters (>10 infections). In general, active room ventilation and the ubiquitous wearing of face masks (i.e., by all subjects) may reduce the individual infection risk by a factor of five to ten, similar to high-vol., high-efficiency particulate air (HEPA) filtering. A particularly effective mitigation measure is the use of high-quality masks, which can drastically reduce the indoor infection risk through aerosols.
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    Jones, B.; Sharpe, P.; Iddon, C.; Hathway, E. A.; Noakes, C. J.; Fitzgerald, S. Modelling Uncertainty in the Relative Risk of Exposure to the SARS-CoV-2 Virus by Airborne Aerosol Transmission in Well Mixed Indoor Air. Build. Environ. 2021, 191, 107617  DOI: 10.1016/j.buildenv.2021.107617
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    34
    Modelling uncertainty in the relative risk of exposure to the SARS-CoV-2 virus by airborne aerosol transmission in well mixed indoor air
    Jones Benjamin; Sharpe Patrick; Iddon Christopher; Hathway E Abigail; Noakes Catherine J; Fitzgerald Shaun
    Building and environment (2021), 191 (), 107617 ISSN:0360-1323.
    We present a mathematical model and a statistical framework to estimate uncertainty in the number of SARS-CoV-2 genome copies deposited in the respiratory tract of a susceptible person, [Formula: see text] , over time in a well mixed indoor space. By relating the predicted median [Formula: see text] for a reference scenario to other locations, a Relative Exposure Index (REI) is established that reduces the need to understand the infection dose probability but is nevertheless a function of space volume, viral emission rate, exposure time, occupant respiratory activity, and room ventilation. A 7 h day in a UK school classroom is used as a reference scenario because its geometry, building services, and occupancy have uniformity and are regulated. The REI is used to highlight types of indoor space, respiratory activity, ventilation provision and other factors that increase the likelihood of far field ( [Formula: see text] m) exposure. The classroom reference scenario and an 8 h day in a 20 person office both have an [Formula: see text] and so are a suitable for comparison with other scenarios. A poorly ventilated classroom (1.2 l s(-1) per person) has [Formula: see text] suggesting that ventilation should be monitored in classrooms to minimise far field aerosol exposure risk. Scenarios involving high aerobic activities or singing have [Formula: see text] ; a 1 h gym visit has a median [Formula: see text] , and the Skagit Choir superspreading event has [Formula: see text] . Spaces with occupancy activities and exposure times comparable to those of the reference scenario must preserve the reference scenario volume flow rate as a minimum rate to achieve [Formula: see text] , irrespective of the number of occupants present.
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  35. 35
    Han, E.; Tan, M. M. J.; Turk, E.; Sridhar, D.; Leung, G. M.; Shibuya, K.; Asgari, N.; Oh, J.; García-Basteiro, A. L.; Hanefeld, J.; Cook, A. R.; Hsu, L. Y.; Teo, Y. Y.; Heymann, D.; Clark, H.; McKee, M.; Legido-Quigley, H. Lessons Learnt from Easing COVID-19 Restrictions: An Analysis of Countries and Regions in Asia Pacific and Europe. Lancet 2020, 396, 1525– 1534,  DOI: 10.1016/S0140-6736(20)32007-9
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    Lessons learnt from easing COVID-19 restrictions: an analysis of countries and regions in Asia Pacific and Europe
    Han, Emeline; Tan, Melisa Mei Jin; Turk, Eva; Sridhar, Devi; Leung, Gabriel M.; Shibuya, Kenji; Asgari, Nima; Oh, Juhwan; Garcia-Basteiro, Alberto L.; Hanefeld, Johanna; Cook, Alex R.; Hsu, Li Yang; Teo, Yik Ying; Heymann, David; Clark, Helen; McKee, Martin; Legido-Quigley, Helena
    Lancet (2020), 396 (10261), 1525-1534CODEN: LANCAO; ISSN:0140-6736. (Elsevier Ltd.)
    The COVID-19 pandemic is an unprecedented global crisis. Many countries have implemented restrictions on population movement to slow the spread of severe acute respiratory syndrome coronavirus 2 and prevent health systems from becoming overwhelmed; some have instituted full or partial lockdowns. However, lockdowns and other extreme restrictions cannot be sustained for the long term in the hope that there will be an effective vaccine or treatment for COVID-19. Governments worldwide now face the common challenge of easing lockdowns and restrictions while balancing various health, social, and economic concerns. To facilitate cross-country learning, this Health Policy paper uses an adapted framework to examine the approaches taken by nine high-income countries and regions that have started to ease COVID-19 restrictions: five in the Asia Pacific region (ie, Hong Kong [Special Administrative Region], Japan, New Zealand, Singapore, and South Korea) and four in Europe (ie, Germany, Norway, Spain, and the UK). This comparative anal. presents important lessons to be learnt from the experiences of these countries and regions. Although the future of the virus is unknown at present, countries should continue to share their experiences, shield populations who are at risk, and suppress transmission to save lives.
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    Buonanno, G.; Stabile, L.; Morawska, L. Estimation of Airborne Viral Emission: Quanta Emission Rate of SARS-CoV-2 for Infection Risk Assessment. Environ. Int. 2020, 141, 105794  DOI: 10.1016/j.envint.2020.105794
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    Estimation of airborne viral emission: Quanta emission rate of SARS-CoV-2 for infection risk assessment
    Buonanno, G.; Stabile, L.; Morawska, L.
    Environment International (2020), 141 (), 105794CODEN: ENVIDV; ISSN:0160-4120. (Elsevier Ltd.)
    Airborne transmission is a pathway of contagion that is still not sufficiently investigated despite the evidence in the scientific literature of the role it can play in the context of an epidemic. While the medical research area dedicates efforts to find cures and remedies to counteract the effects of a virus, the engineering area is involved in providing risk assessments in indoor environments by simulating the airborne transmission of the virus during an epidemic. To this end, virus air emission data are needed. Unfortunately, this information is usually available only after the outbreak, based on specific reverse engineering cases. In this work, a novel approach to est. the viral load emitted by a contagious subject on the basis of the viral load in the mouth, the type of respiratory activity (e.g. breathing, speaking, whispering), respiratory physiol. parameters (e.g. inhalation rate), and activity level (e.g. resting, standing, light exercise) is proposed. The results showed that high quanta emission rates (>100 quanta h-1) can be reached by an asymptomatic infectious SARS-CoV-2 subject performing vocalization during light activities (i.e. walking slowly) whereas a symptomatic SARS-CoV-2 subject in resting conditions mostly has a low quanta emission rate (<1 quantum h-1). The findings in terms of quanta emission rates were then adopted in infection risk models to demonstrate its application by evaluating the no. of people infected by an asymptomatic SARS-CoV-2 subject in Italian indoor microenvironments before and after the introduction of virus containment measures. The results obtained from the simulations clearly highlight that a key role is played by proper ventilation in containment of the virus in indoor environments.
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    Peng, Z.; Jimenez, J. L. Exhaled CO2 as a COVID-19 Infection Risk Proxy for Different Indoor Environments and Activities. Environ. Sci. Technol. Lett. 2021, 8, 392– 397,  DOI: 10.1021/acs.estlett.1c00183
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    Exhaled CO2 as a COVID-19 Infection Risk Proxy for Different Indoor Environments and Activities
    Peng, Zhe; Jimenez, Jose L.
    Environmental Science & Technology Letters (2021), 8 (5), 392-397CODEN: ESTLCU; ISSN:2328-8930. (American Chemical Society)
    CO2 is co-exhaled with aerosols contg. SARS-CoV-2 by COVID-19-infected people and can be used as a proxy of SARS-CoV-2 concns. indoors. Indoor CO2 measurements by low-cost sensors hold promise for mass monitoring of indoor aerosol transmission risk for COVID-19 and other respiratory diseases. We derive anal. expressions of CO2-based risk proxies and apply them to various typical indoor environments. The relative infection risk in a given environment scales with excess CO2 level, and thus, keeping CO2 as low as feasible in a space allows optimization of the protection provided by ventilation. The CO2 level corresponding to a given abs. infection risk varies by >2 orders of magnitude for different environments and activities. Although large uncertainties, mainly from virus exhalation rates, are still assocd. with infection risk ests., our study provides more specific and practical recommendations for low-cost CO2-based indoor infection risk monitoring.
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    Ma, J.; Qi, X.; Chen, H.; Li, X.; Zhang, Z.; Wang, H.; Sun, L.; Zhang, L.; Guo, J.; Morawska, L.; Grinshpun, S. A.; Biswas, P.; Flagan, R. C.; Yao, M. COVID-19 Patients in Earlier Stages Exhaled Millions of SARS-CoV-2 per Hour. Clin. Infect. Dis. 2021, 72, e652– e654,  DOI: 10.1093/cid/ciaa1283
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    Coronavirus disease 2019 patients in earlier stages exhaled millions of severe acute respiratory syndrome coronavirus 2 per hour
    Ma, Jianxin; Qi, Xiao; Chen, Haoxuan; Li, Xinyue; Zhang, Zheng; Wang, Haibin; Sun, Lingli; Zhang, Lu; Guo, Jiazhen; Morawska, Lidia; Grinshpun, Sergey A.; Biswas, Pratim; Flagan, Richard C.; Yao, Maosheng
    Clinical Infectious Diseases (2021), 72 (10), e652-e654CODEN: CIDIEL; ISSN:1537-6591. (Oxford University Press)
    Coronavirus disease 2019 (COVID-19) patients exhaled millions of severe acute respiratory syndrome coronavirus 2 RNA copies per h, which plays an important role in COVID-19 transmission. Exhaled breath had a higher pos. rate (26.9%, n = 52) than surface (5.4%, n = 242) and air (3.8%, n = 26) samples.
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    Volz, E.; Mishra, S.; Chand, M.; Barrett, J. C.; Johnson, R.; Geidelberg, L.; Hinsley, W. R.; Laydon, D. J.; Dabrera, G.; O’Toole, Á.; Amato, R.; Ragonnet-Cronin, M.; Harrison, I.; Jackson, B.; Ariani, C. V.; Boyd, O.; Loman, N. J.; McCrone, J. T.; Gonçalves, S.; Jorgensen, D.; Myers, R.; Hill, V.; Jackson, D. K.; Gaythorpe, K.; Groves, N.; Sillitoe, J.; Kwiatkowski, D. P.; COVID-19 Genomics UK (COG-UK) consortium; Flaxman, S.; Ratmann, O.; Bhatt, S.; Hopkins, S.; Gandy, A.; Rambaut, A.; Ferguson, N. M. Assessing Transmissibility of SARS-CoV-2 Lineage B.1.1.7 in England. Nature 2021, 593, 266– 269,  DOI: 10.1038/s41586-021-03470-x
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    Assessing transmissibility of SARS-CoV-2 lineage B.1.1.7 in England
    Volz, Erik; Mishra, Swapnil; Chand, Meera; Barrett, Jeffrey C.; Johnson, Robert; Geidelberg, Lily; Hinsley, Wes R.; Laydon, Daniel J.; Dabrera, Gavin; O'Toole, Aine; Amato, Robert; Ragonnet-Cronin, Manon; Harrison, Ian; Jackson, Ben; Ariani, Cristina V.; Boyd, Olivia; Loman, Nicholas J.; McCrone, John T.; Goncalves, Sonia; Jorgensen, David; Myers, Richard; Hill, Verity; Jackson, David K.; Gaythorpe, Katy; Groves, Natalie; Sillitoe, John; Kwiatkowski, Dominic P.; Flaxman, Seth; Ratmann, Oliver; Bhatt, Samir; Hopkins, Susan; Gandy, Axel; Rambaut, Andrew; Ferguson, Neil M.
    Nature (London, United Kingdom) (2021), 593 (7858), 266-269CODEN: NATUAS; ISSN:0028-0836. (Nature Portfolio)
    The SARS-CoV-2 lineage B.1.1.7, designated variant of concern (VOC) 202012/01 by Public Health England, was first identified in the UK in late summer to early autumn 2020. Whole-genome SARS-CoV-2 sequence data collected from community-based diagnostic testing for COVID-19 show an extremely rapid expansion of the B.1.1.7 lineage during autumn 2020, suggesting that it has a selective advantage. Changes in VOC frequency inferred from genetic data correspond closely to changes inferred by S gene target failures (SGTF) in community-based diagnostic PCR testing. Anal. of trends in SGTF and non-SGTF case nos. in local areas across England shows that B.1.1.7 has higher transmissibility than non-VOC lineages, even if it has a different latent period or generation time. The SGTF data indicate a transient shift in the age compn. of reported cases, with cases of B.1.1.7 including a larger share of under 20-yr-olds than non-VOC cases. We estd. time-varying reprodn. nos. for B.1.1.7 and co-circulating lineages using SGTF and genomic data. The best-supported models did not indicate a substantial difference in VOC transmissibility among different age groups, but all analyses agreed that B.1.1.7 has a substantial transmission advantage over other lineages, with a 50-100% higher reprodn. no.
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  40. 40
    Kidd, M.; Richter, A.; Best, A.; Cumley, N.; Mirza, J.; Percival, B.; Mayhew, M.; Megram, O.; Ashford, F.; White, T.; Moles-Garcia, E.; Crawford, L.; Bosworth, A.; Atabani, S. F.; Plant, T.; McNally, A. S-Variant SARS-CoV-2 Lineage B1.1.7 Is Associated with Significantly Higher Viral Loads in Samples Tested by Thermo Fisher Taq Path RT-qPCR. J. Infect. Dis. 2021, 223, 1666,  DOI: 10.1093/infdis/jiab082
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    S-variant SARS-CoV-2 lineage B1.1.7 is associated with significantly higher viral load in samples tested by taqpath polymerase chain reaction
    Kidd, Michael; Richter, Alex; Best, Angus; Cumley, Nicola; Mirza, Jeremy; Percival, Benita; Mayhew, Megan; Megram, Oliver; Ashford, Fiona; White, Thomas; Moles-Garcia, Emma; Crawford, Liam; Bosworth, Andrew; Atabani, Sowsan F.; Plant, Tim; McNally, Alan
    Journal of Infectious Diseases (2021), 223 (10), 1666-1670CODEN: JIDIAQ; ISSN:1537-6613. (Oxford University Press)
    A SARS-CoV-2 variant B1.1.7 contg. mutation Δ69/70 has spread rapidly in the United Kingdom and shows an identifiable profile in ThermoFisher TaqPath RT-qPCR, S gene target failure (SGTF). We analyzed recent test data for trends and significance. Linked cycle threshold (Ct) values for respiratory samples showed that a low Ct for ORF1ab and N were clearly assocd. with SGTF. Significantly more SGTF samples had higher inferred viral loads between 1 x 107 and 1 x 108. Our that patient whose samples exhibit the SGTF profile are more likely to have high viral loads, which may explain higher infectivity and rapidity of spread.
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    EPA. Chapter 6─Inhalation Rates. In Exposure Factors Handbook; U.S. Environmental Protection Agency, 2011.
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    Edwards, D. A.; Ausiello, D.; Salzman, J.; Devlin, T.; Langer, R.; Beddingfield, B. J.; Fears, A. C.; Doyle-Meyers, L. A.; Redmann, R. K.; Killeen, S. Z.; Maness, N. J.; Roy, C. J. Exhaled Aerosol Increases with COVID-19 Infection, Age, and Obesity. Proc. Natl. Acad. Sci. U. S. A. 2021, 118, e2021830118  DOI: 10.1073/pnas.2021830118
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    Exhaled aerosol increases with COVID-19 infection, age, and obesity
    Edwards, David A.; Ausiello, Dennis; Salzman, Jonathan; Devlin, Tom; Langer, Robert; Beddingfield, Brandon J.; Fears, Alyssa C.; Doyle-Meyers, Lara A.; Redmann, Rachel K.; Killeen, Stephanie Z.; Maness, Nicholas J.; Roy, Chad J.
    Proceedings of the National Academy of Sciences of the United States of America (2021), 118 (8), e2021830118CODEN: PNASA6; ISSN:0027-8424. (National Academy of Sciences)
    COVID-19 transmits by droplets generated from surfaces of airway mucus during processes of respiration within hosts infected by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) virus. We studied respiratory droplet generation and exhalation in human and nonhuman primate subjects with and without COVID-19 infection to explore whether SARS-CoV-2 infection, and other changes in physiol. state, translate into observable evolution of nos. and sizes of exhaled respiratory droplets in healthy and diseased subjects. In our observational cohort study of the exhaled breath particles of 194 healthy human subjects, and in our exptl. infection study of eight nonhuman primates infected, by aerosol, with SARS-CoV-2, we found that exhaled aerosol particles vary between subjects by three orders of magnitude, with exhaled respiratory droplet no. increasing with degree of COVID-19 infection and elevated BMI-years. We obsd. that 18% of human subjects (35) accounted for 80% of the exhaled bioaerosol of the group (194), reflecting a superspreader distribution of bioaerosol analogous to a classical 20:80 superspreader of infection distribution. These findings suggest that quant. assessment and control of exhaled aerosol may be crit. to slowing the airborne spread of COVID-19 in the absence of an effective and widely disseminated vaccine.
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    van Doremalen, N.; Bushmaker, T.; Morris, D. H.; Holbrook, M. G.; Gamble, A.; Williamson, B. N.; Tamin, A.; Harcourt, J. L.; Thornburg, N. J.; Gerber, S. I.; Lloyd-Smith, J. O.; de Wit, E.; Munster, V. J. Aerosol and Surface Stability of SARS-CoV-2 as Compared with SARS-CoV-1. N. Engl. J. Med. 2020, 382, 1564– 1567,  DOI: 10.1056/NEJMc2004973
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    Aerosol and Surface Stability of SARS-CoV-2 as Compared with SARS-CoV-1
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    The New England journal of medicine (2020), 382 (16), 1564-1567 ISSN:.
    There is no expanded citation for this reference.
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    Chan, K. H.; Peiris, J. S. M.; Lam, S. Y.; Poon, L. L. M.; Yuen, K. Y.; Seto, W. H. The Effects of Temperature and Relative Humidity on the Viability of the SARS Coronavirus. Adv. Virol. 2011, 2011, 734690  DOI: 10.1155/2011/734690
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    The Effects of Temperature and Relative Humidity on the Viability of the SARS Coronavirus
    Chan K H; Peiris J S Malik; Lam S Y; Poon L L M; Yuen K Y; Seto W H
    Advances in virology (2011), 2011 (), 734690 ISSN:.
    The main route of transmission of SARS CoV infection is presumed to be respiratory droplets. However the virus is also detectable in other body fluids and excreta. The stability of the virus at different temperatures and relative humidity on smooth surfaces were studied. The dried virus on smooth surfaces retained its viability for over 5 days at temperatures of 22-25°C and relative humidity of 40-50%, that is, typical air-conditioned environments. However, virus viability was rapidly lost (>3 log(10)) at higher temperatures and higher relative humidity (e.g., 38°C, and relative humidity of >95%). The better stability of SARS coronavirus at low temperature and low humidity environment may facilitate its transmission in community in subtropical area (such as Hong Kong) during the spring and in air-conditioned environments. It may also explain why some Asian countries in tropical area (such as Malaysia, Indonesia or Thailand) with high temperature and high relative humidity environment did not have major community outbreaks of SARS.
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    Dabisch, P.; Schuit, M.; Herzog, A.; Beck, K.; Wood, S.; Krause, M.; Miller, D.; Weaver, W.; Freeburger, D.; Hooper, I.; Green, B.; Williams, G.; Holland, B.; Bohannon, J.; Wahl, V.; Yolitz, J.; Hevey, M.; Ratnesar-Shumate, S. The Influence of Temperature, Humidity, and Simulated Sunlight on the Infectivity of SARS-CoV-2 in Aerosols. Aerosol Sci. Technol. 2021, 55, 142– 153,  DOI: 10.1080/02786826.2020.1829536
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    The influence of temperature, humidity, and simulated sunlight on the infectivity of SARS-CoV-2 in aerosols
    Dabisch, Paul; Schuit, Michael; Herzog, Artemas; Beck, Katie; Wood, Stewart; Krause, Melissa; Miller, David; Weaver, Wade; Freeburger, Denise; Hooper, Idris; Green, Brian; Williams, Gregory; Holland, Brian; Bohannon, Jordan; Wahl, Victoria; Yolitz, Jason; Hevey, Michael; Ratnesar-Shumate, Shanna
    Aerosol Science and Technology (2021), 55 (2), 142-153CODEN: ASTYDQ; ISSN:0278-6826. (Taylor & Francis, Inc.)
    Recent evidence suggests that respiratory aerosols may play a role in the spread of SARS-CoV-2 during the ongoing COVID-19 pandemic. The authors' lab. has previously demonstrated that simulated sunlight inactivated SARS-CoV-2 in aerosols and on surfaces. In the present study, the authors extend these findings to include the persistence of SARS-CoV-2 in aerosols across a range of temp., humidity, and simulated sunlight levels using an environmentally controlled rotating drum aerosol chamber. The results demonstrate that temp., simulated sunlight, and humidity are all significant factors influencing the persistence of infectious SARS-CoV-2 in aerosols, but that simulated sunlight and temp. have a greater influence on decay than humidity across the range of conditions tested. The time needed for a 90% decrease in infectious virus ranged from 4.8 min at 40°C, 20% relative humidity, and high intensity simulated sunlight representative of noon on a clear day on the summer solstice at 40°N latitude, to greater than two hours under conditions representative of those expected indoors or at night. These results suggest that the persistence of infectious SARS-CoV-2 in naturally occurring aerosols may be affected by environmental conditions, and that aerosolized virus could remain infectious for extended periods of time under some environmental conditions. The present study provides a comprehensive dataset on the influence of environmental parameters on the survival of SARS-CoV-2 in aerosols that can be utilized, along with data on viral shedding from infected individuals and the inhalational infectious dose, to inform future modeling and risk assessment efforts.
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    Johnson, G. R.; Morawska, L.; Ristovski, Z. D.; Hargreaves, M.; Mengersen, K.; Chao, C. Y. H.; Wan, M. P.; Li, Y.; Xie, X.; Katoshevski, D.; Corbett, S. Modality of Human Expired Aerosol Size Distributions. J. Aerosol Sci. 2011, 42, 839– 851,  DOI: 10.1016/j.jaerosci.2011.07.009
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    Modality of human expired aerosol size distributions
    Johnson, G. R.; Morawska, L.; Ristovski, Z. D.; Hargreaves, M.; Mengersen, K.; Chao, C. Y. H.; Wan, M. P.; Li, Y.; Xie, X.; Katoshevski, D.; Corbett, S.
    Journal of Aerosol Science (2011), 42 (12), 839-851CODEN: JALSB7; ISSN:0021-8502. (Elsevier Ltd.)
    An essential starting point when investigating the potential role of human expired aerosols in the transmission of disease is to gain a comprehensive knowledge of the expired aerosol generation process, including the aerosol size distribution, the various droplet prodn. mechanisms involved and the corresponding sites of prodn. within the respiratory tract. In order to approach this level of understanding we have integrated the results of two different investigative techniques spanning 3 decades of particle size from 700 nm to 1 mm, presenting a single composite size distribution, and identifying the most prominent modes in that distribution. We link these modes to specific sites of origin and mechanisms of prodn. The data for this were obtained using the Aerodynamic Particle Sizer (APS) covering the range 0.7≤d≤20 μm and Droplet Deposition Anal. (DDA) covering the range d≥20 μm. In the case of speech three distinct droplet size distribution modes were identified with count median diams. at 1.6, 2.5 and 145 μm. In the case of voluntary coughing the modes were located at 1.6, 1.7 and 123 μm. The modes are assocd. with three distinct processes: one occurring deep in the lower respiratory tract, another in the region of the larynx and a third in the upper respiratory tract including the oral cavity. The first of these, the Bronchiolar Fluid Film Burst (BFFB or B) mode contains droplets produced during normal breathing. The second, the Laryngeal (L) mode is most active during voicing and coughing. The third, the Oral (O) cavity mode is active during speech and coughing. The no. of droplets and the vol. of aerosol material assocd. with each mode of aerosol prodn. during speech and coughing is presented. The size distribution is modeled as a tri-modal lognormal distribution dubbed the Bronchiolar/Laryngeal/Oral (B.L.O.) tri-modal model.
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    Thatcher, T. L.; Lai, A. C. K.; Moreno-Jackson, R.; Sextro, R. G.; Nazaroff, W. W. Effects of Room Furnishings and Air Speed on Particle Deposition Rates Indoors. Atmos. Environ. 2002, 36, 1811– 1819,  DOI: 10.1016/S1352-2310(02)00157-7
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    Effects of room furnishings and air speed on particle deposition rates indoors
    Thatcher, Tracy L.; Lai, Alvin C. K.; Moreno-Jackson, Rosa; Sextro, Richard G.; Nazaroff, William W.
    Atmospheric Environment (2002), 36 (11), 1811-1819CODEN: AENVEQ; ISSN:1352-2310. (Elsevier Science Ltd.)
    Particle deposition to surfaces plays an important role in detg. exposure to indoor particles; however, the effect of furnishings and air speed on these rates has not been well characterized. Expts. were performed in an isolated room (vol. = 14.2 m3) using 3 different indoor furnishing levels (bare, carpeted, fully furnished) and 4 different air flow conditions. Deposition loss rates were detd. by generating a short burst of polydispersed particles, then measuring size-resolved (0.5-10 μm) concn. decay rate using an aerodynamic particle sizer. Increasing the surface area from bare (35 m2 nominal surface area) to fully furnished (12 m2 addnl. surface area) increased the deposition loss rate by as much as a factor of 2.6; largest increase was obsd. for the smallest particles. Increasing the mean air speed from <5 to 19 cm/s by increasing fan speed, increased the deposition rate for all particle sizes by factors of 1.3-2.4, with larger particles exhibiting greater effects than smaller particles. The significant effect of particle size and room conditions on deposition loss rates argues against using a single, first-order loss-rate coeff. to represent deposition for integrated mass measurements (PM2.5 or PM10).
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    Nazaroff, W. W. Residential Air-Change Rates: A Critical Review. Indoor Air 2021, 31, 282– 313,  DOI: 10.1111/ina.12785
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    Residential air-change rates: A critical review
    Nazaroff William W
    Indoor air (2021), 31 (2), 282-313 ISSN:.
    Air-change rate is an important parameter influencing residential air quality. This article critically assesses the state of knowledge regarding residential air-change rates, emphasizing periods of normal occupancy. Cumulatively, about 40 prior studies have measured air-change rates in approximately 10,000 homes using tracer gases, including metabolic CO2 . The central tendency of the air-change rates determined in these studies is reasonably described as lognormal with a geometric mean of 0.5 h(-1) and a geometric standard deviation of 2.0. However, the geometric means of individual studies vary, mainly within the range 0.2-1 h(-1) . Air-change rates also vary with time in residences. Factors influencing the air-change rate include weather (indoor-outdoor temperature difference and wind speed), the leakiness of the building envelope, and, when present, operation of mechanical ventilation systems. Occupancy-associated factors are also important, including window opening, induced exhaust from flued combustion, and use of heating and cooling systems. Empirical and methodological challenges remain to be effectively addressed. These include clarifying the time variation of air-change rates in residences during occupancy and understanding the influence of time-varying air-change rates on tracer-gas measurement techniques. Important opportunities are available to improve understanding of air-change rates and interzonal flows as factors affecting the source-to-exposure relationships for indoor air pollutants.
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    Batterman, S.; Su, F.-C.; Wald, A.; Watkins, F.; Godwin, C.; Thun, G. Ventilation Rates in Recently Constructed U.S. School Classrooms. Indoor Air 2017, 27, 880– 890,  DOI: 10.1111/ina.12384
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    Ventilation rates in recently constructed U.S. school classrooms
    Batterman S; Su F-C; Wald A; Watkins F; Godwin C; Thun G
    Indoor air (2017), 27 (5), 880-890 ISSN:.
    Low ventilation rates (VRs) in schools have been associated with absenteeism, poorer academic performance, and teacher dissatisfaction. We measured VRs in 37 recently constructed or renovated and mechanically ventilated U.S. schools, including LEED and EnergyStar-certified buildings, using CO2 and the steady-state, build-up, decay, and transient mass balance methods. The transient mass balance method better matched conditions (specifically, changes in occupancy) and minimized biases seen in the other methods. During the school day, air change rates (ACRs) averaged 2.0±1.3 hour(-1) , and only 22% of classrooms met recommended minimum ventilation rates. HVAC systems were shut off at the school day close, and ACRs dropped to 0.21±0.19 hour(-1) . VRs did not differ by building type, although cost-cutting and comfort measures resulted in low VRs and potentially impaired IAQ. VRs were lower in schools that used unit ventilators or radiant heating, in smaller schools and in larger classrooms. The steady-state, build-up, and decay methods had significant limitations and biases, showing the need to confirm that these methods are appropriate. Findings highlight the need to increase VRs and to ensure that energy saving and comfort measures do not compromise ventilation and IAQ.
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    ASHRAE Ventilation for Acceptable Indoor Air Quality. ANSI/ASHRAE Standard 62.1–2019; ANSI/ASHRAE 2019.
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    ASHRAE ASHRAE Position Document on Infectious Aerosols; American Society of Heating, Refrigerating and Air-Conditioning Engineers 2020.
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    REHVA How to Operate HVAC and Other Building Service Systems to Prevent the Spread of the Coronavirus (SARS-CoV-2) Disease (COVID-19) in Workplaces; Federation of European Heating, Ventilation and Air Conditioning Associations 2020.
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    Chen, P. Z.; Bobrovitz, N.; Premji, Z.; Koopmans, M.; Fisman, D. N.; Gu, F. X. Heterogeneity in Transmissibility and Shedding SARS-CoV-2 via Droplets and Aerosols. Elife 2021, 10, e65774  DOI: 10.7554/eLife.65774
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    Heterogeneity in transmissibility and shedding SARS-CoV-2 via droplets and aerosols
    Chen, Paul Z.; Bobrovitz, Niklas; Premji, Zahra; Koopmans, Marion; Fisman, David N.; Gu, Frank X.
    eLife (2021), 10 (), e65774CODEN: ELIFA8; ISSN:2050-084X. (eLife Sciences Publications Ltd.)
    Background: Which virol. factors mediate overdispersion in the transmissibility of emerging viruses remains a long-standing question in infectious disease epidemiol. Methods: Here, we use systematic review to develop a comprehensive dataset of respiratory viral loads (rVLs) of SARS-CoV-2, SARS-CoV-1 and influenza A(H1N1)pdm09. We then comparatively meta-analyze the data and model individual infectiousness by shedding viable virus via respiratory droplets and aerosols. Results: The analyses indicate heterogeneity in rVL as an intrinsic virol. factor facilitating greater overdispersion for SARS-CoV-2 in the COVID-19 pandemic than A(H1N1)pdm09 in the 2009 influenza pandemic. For COVID-19, case heterogeneity remains broad throughout the infectious period, including for pediatric and asymptomatic infections. Hence, many COVID-19 cases inherently present minimal transmission risk, whereas highly infectious individuals shed tens to thousands of SARS-CoV-2 virions/min via droplets and aerosols while breathing, talking and singing. Coughing increases the contagiousness, esp. in close contact, of symptomatic cases relative to asymptomatic ones. Infectiousness tends to be elevated between 1 and 5 days post- symptom onset. Conclusions: Intrinsic case variation in rVL facilitates overdispersion in the transmissibility of emerging respiratory viruses. Our findings present considerations for disease control in the COVID- 19 pandemic as well as future outbreaks of novel viruses. Funding: Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant program, NSERC Senior Industrial Research Chair program and the Toronto COVID-19 Action Fund.
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    Yang, Q.; Saldi, T. K.; Gonzales, P. K.; Lasda, E.; Decker, C. J.; Tat, K. L.; Fink, M. R.; Hager, C. R.; Davis, J. C.; Ozeroff, C. D.; Muhlrad, D.; Clark, S. K.; Fattor, W. T.; Meyerson, N. R.; Paige, C. L.; Gilchrist, A. R.; Barbachano-Guerrero, A.; Worden-Sapper, E. R.; Wu, S. S.; Brisson, G. R.; McQueen, M. B.; Dowell, R. D.; Leinwand, L.; Parker, R.; Sawyer, S. L. Just 2% of SARS-CoV-2–positive Individuals Carry 90% of the Virus Circulating in Communities. Proc. Natl. Acad. Sci. U. S. A. 2021, 118, e2104547118  DOI: 10.1073/pnas.2104547118
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    Just 2% of SARS-CoV-2-positive individuals carry 90% of the virus circulating in communities
    Yang, Qing; Saldi, Tassa K.; Gonzales, Patrick K.; Lasda, Erika; Decker, Carolyn J.; Tat, Kimngan L.; Fink, Morgan R.; Hager, Cole R.; Davis, Jack C.; Ozeroff, Christopher D.; Muhlrad, Denise; Clark, Stephen K.; Fattor, Will T.; Meyerson, Nicholas R.; Paige, Camille L.; Gilchrist, Alison R.; Barbachano-Guerrero, Arturo; Worden-Sapper, Emma R.; Wu, Sharon S.; Brisson, Gloria R.; McQueen, Matthew B.; Dowell, Robin D.; Leinwand, Leslie; Parker, Roy; Sawyer, Sara L.
    Proceedings of the National Academy of Sciences of the United States of America (2021), 118 (21), e2104547118CODEN: PNASA6; ISSN:0027-8424. (National Academy of Sciences)
    We analyze data from the fall 2020 pandemic response efforts at the University of Colorado Boulder, where more than 72,500 saliva samples were tested for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) using qRT-PCR. All samples were collected from individuals who reported no symptoms assocd. with COVID-19 on the day of collection. From these, 1,405 pos. cases were identified. The distribution of viral loads within these asymptomatic individuals was indistinguishable from what has been previously obsd. in symptomatic individuals. Regardless of symptomatic status, ∼50% of individuals who test pos. for SARS-CoV-2 seem to be in noninfectious phases of the disease, based on having low viral loads in a range from which live virus has rarely been isolated. We find that, at any given time, just 2% of individuals carry 90% of the virions circulating within communities, serving as viral 'supercarriers' and possibly also superspreaders.
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    Wu, S. L.; Mertens, A. N.; Crider, Y. S.; Nguyen, A.; Pokpongkiat, N. N.; Djajadi, S.; Seth, A.; Hsiang, M. S.; Colford, J. M.; Reingold, A.; Arnold, B. F.; Hubbard, A.; Benjamin-Chung, J. Substantial Underestimation of SARS-CoV-2 Infection in the United States. Nat. Commun. 2020, 11, 4507,  DOI: 10.1038/s41467-020-18272-4
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    Substantial underestimation of SARS-CoV-2 infection in the United States
    Wu, Sean L.; Mertens, Andrew N.; Crider, Yoshika S.; Nguyen, Anna; Pokpongkiat, Nolan N.; Djajadi, Stephanie; Seth, Anmol; Hsiang, Michelle S.; Colford Jr., John M.; Reingold, Art; Arnold, Benjamin F.; Hubbard, Alan; Benjamin-Chung, Jade
    Nature Communications (2020), 11 (1), 4507CODEN: NCAOBW; ISSN:2041-1723. (Nature Research)
    Accurate ests. of the burden of SARS-CoV-2 infection are crit. to informing pandemic response. Confirmed COVID-19 case counts in the U.S. do not capture the total burden of the pandemic because testing has been primarily restricted to individuals with moderate to severe symptoms due to limited test availability. Here, the authors use a semi-Bayesian probabilistic bias anal. to account for incomplete testing and imperfect diagnostic accuracy. The authors est. 6454,951 cumulative infections compared to 721,245 confirmed cases (1.9% vs. 0.2% of the population) in the United States as of Apr. 18, 2020. Accounting for uncertainty, the no. of infections during this period was 3 to 20 times higher than the no. of confirmed cases. 86% (simulation interval: 64-99%) of this difference is due to incomplete testing, while 14% (0.3-36%) is due to imperfect test accuracy. The approach can readily be applied in future studies in other locations or at finer spatial scale to correct for biased testing and imperfect diagnostic accuracy to provide a more realistic assessment of COVID-19 burden.
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    Jones, T. C.; Biele, G.; Mühlemann, B.; Veith, T.; Schneider, J.; Beheim-Schwarzbach, J.; Bleicker, T.; Tesch, J.; Schmidt, M. L.; Sander, L. E.; Kurth, F.; Menzel, P.; Schwarzer, R.; Zuchowski, M.; Hofmann, J.; Krumbholz, A.; Stein, A.; Edelmann, A.; Corman, V. M.; Drosten, C. Estimating Infectiousness throughout SARS-CoV-2 Infection Course. Science 2021, 373, eabi5273  DOI: 10.1126/science.abi5273
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    Ou, C.; Hu, S.; Luo, K.; Yang, H.; Hang, J.; Cheng, P.; Hai, Z.; Xiao, S.; Qian, H.; Xiao, S.; Jing, X.; Xie, Z.; Ling, H.; Liu, L.; Gao, L.; Deng, Q.; Cowling, B. J.; Li, Y. Insufficient Ventilation Led to a Probable Long-Range Airborne Transmission of SARS-CoV-2 on Two Buses. Build. Environ. 2022, 207, 108414  DOI: 10.1016/j.buildenv.2021.108414
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    Insufficient ventilation led to a probable long-range airborne transmission of SARS-CoV-2 on two buses
    Ou Cuiyun; Yang Hongyu; Hang Jian; Ling Hong; Hu Shixiong; Luo Kaiwei; Gao Lidong; Cheng Pan; Xiao Shenglan; Li Yuguo; Hai Zheng; Jing Xinping; Xie Zhengshen; Xiao Shanliang; Qian Hua; Liu Li; Deng Qihong; Cowling Benjamin J; Li Yuguo
    Building and environment (2022), 207 (), 108414 ISSN:0360-1323.
    Uncertainty remains on the threshold of ventilation rate in airborne transmission of SARS-CoV-2. We analyzed a COVID-19 outbreak in January 2020 in Hunan Province, China, involving an infected 24-year-old man, Mr. X, taking two subsequent buses, B1 and B2, in the same afternoon. We investigated the possibility of airborne transmission and the ventilation conditions for its occurrence. The ventilation rates on the buses were measured using a tracer-concentration decay method with the original driver on the original route. We measured and calculated the spread of the exhaled virus-laden droplet tracer from the suspected index case. Ten additional passengers were found to be infected, with seven of them (including one asymptomatic) on B1 and two on B2 when Mr. X was present, and one passenger infected on the subsequent B1 trip. B1 and B2 had time-averaged ventilation rates of approximately 1.7 and 3.2 L/s per person, respectively. The difference in ventilation rates and exposure time could explain why B1 had a higher attack rate than B2. Airborne transmission due to poor ventilation below 3.2 L/s played a role in this two-bus outbreak of COVID-19.
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    Park, S. Y.; Kim, Y. M.; Yi, S.; Lee, S.; Na, B. J.; Kim, C. B.; Kim, J. I.; Kim, H. S.; Kim, Y. B.; Park, Y.; Huh, I. S.; Kim, H. K.; Yoon, H. J.; Jang, H.; Kim, K.; Chang, Y.; Kim, I.; Lee, H.; Gwack, J.; Kim, S. S.; Kim, M.; Kweon, S.; Choe, Y. J.; Park, O.; Park, Y. J.; Jeong, E. K. Coronavirus Disease Outbreak in Call Center, South Korea. Emerg. Infect. Dis. 2020, 26, 1666– 1670,  DOI: 10.3201/eid2608.201274
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    Coronavirus disease outbreak in call center, South Korea
    Park, Shin Young; Kim, Young-Man; Yi, Seonju; Lee, Sangeun; Na, Baeg-Ju; Kim, Chang Bo; Kim, Jung-il; Kim, Hea Sook; Kim, Young Bok; Park, Yoojin; Huh, In Sil; Kim, Hye Kyung; Yoon, Hyung Jun; Jang, Hanaram; Kim, Kyungnam; Chang, Yeonhwa; Kim, Inhye; Lee, Hyeyoung; Gwack, Jin; Kim, Seong Sun; Kim, Miyoung; Kweon, Sanghui; Choe, Young June; Park, Ok; Park, Young Joon; Jeong, Eun Kyeong
    Emerging Infectious Diseases (2020), 26 (8), 1666-1670CODEN: EIDIFA; ISSN:1080-6059. (Centers for Disease Control and Prevention)
    We describe the epidemiol. of a coronavirus disease (COVID-19) outbreak in a call center in South Korea. We obtained information on demog. characteristics by using standardized epidemiol. investigation forms. We performed descriptive analyses and reported the results as frequencies and proportions for categoric variables. Of 1,143 persons who were tested for COVID-19, a total of 97 (8.5%, 95% CI 7.0%-10.3%) had confirmed cases. Of these, 94 were working in an 11th-floor call center with 216 employees, translating to an attack rate of 43.5% (95% CI 36.9%-50.4%). The household secondary attack rate among symptomatic case-patients was 16.2% (95% CI 11.6%- 22.0%). Of the 97 persons with confirmed COVID-19, only 4 (1.9%) remained asymptomatic within 14 days of quarantine, and none of their household contacts acquired secondary infections. Extensive contact tracing, testing all contacts, and early quarantine blocked further transmission and might be effective for contg. rapid outbreaks in crowded work settings.
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    Khanh, N. C.; Thai, P. Q.; Quach, H.-L.; Thi, N.-A. H.; Dinh, P. C.; Duong, T. N.; Mai, L. T. Q.; Nghia, N. D.; Tu, T. A.; Quang, L. N.; Quang, T. D.; Nguyen, T.-T.; Vogt, F.; Anh, D. D. Transmission of SARS-CoV 2 During Long-Haul Flight. Emerg. Infect. Dis. 2020, 26, 2617– 2624,  DOI: 10.3201/eid2611.203299
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    Transmission of SARS-CoV-2 during long-haul flight
    Khanh, Nguyen Cong; Thai, Pham Quang; Quach, Ha-Linh; Thi, Ngoc-Anh Hoang; Dinh, Phung Cong; Duong, Tran Nhu; Mai, Le Thi Quynh; Nghia, Ngu Duy; Tu, Tran Anh; Quang, La Ngoc; Quang, Tran Dai; Nguyen, Trong-Tai; Vogt, Florian; Anh, Dang Duc
    Emerging Infectious Diseases (2020), 26 (11), 2617-2624CODEN: EIDIFA; ISSN:1080-6059. (Centers for Disease Control and Prevention)
    To assess the role of in-flight transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the authors investigated a cluster of cases among passengers on a 10-h com. flight. Affected persons were passengers, crew, and their close contacts. The authors traced 217 passengers and crew to their final destinations and interviewed, tested, and quarantined them. Among the 16 persons in whom SARS-CoV-2 infection was detected, 12 (75%) were passengers seated in business class along with the only symptomatic person (attack rate 62%). Seating proximity was strongly assocd. with increased infection risk (risk ratio 7.3, 95% CI 1.2-46.2). The authors found no strong evidence supporting alternative transmission scenarios. In-flight transmission that probably originated from 1 symptomatic passenger caused a large cluster of cases during a long flight. Guidelines for preventing SARS-CoV-2 infection among air passengers should consider individual passengers' risk for infection, the no. of passengers traveling, and flight duration.
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    Günther, T.; Czech-Sioli, M.; Indenbirken, D.; Robitaille, A.; Tenhaken, P.; Exner, M.; Ottinger, M.; Fischer, N.; Grundhoff, A.; Brinkmann, M. M. SARS-CoV-2 Outbreak Investigation in a German Meat Processing Plant. EMBO Mol. Med. 2020, 12, e13296  DOI: 10.15252/emmm.202013296
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    SARS-CoV-2 outbreak investigation in a German meat processing plant
    Guenther, Thomas; Czech-Sioli, Manja; Indenbirken, Daniela; Robitaille, Alexis; Tenhaken, Peter; Exner, Martin; Ottinger, Matthias; Fischer, Nicole; Grundhoff, Adam; Brinkmann, Melanie M.
    EMBO Molecular Medicine (2020), 12 (12), e13296CODEN: EMMMAM; ISSN:1757-4684. (Wiley-Blackwell)
    We describe a multifactorial investigation of a SARS-CoV-2 outbreak in a large meat processing complex in Germany. Infection event timing, spatial, climate and ventilation conditions in the processing plant, sharing of living quarters and transport, and viral genome sequences were analyzed. Our results suggest that a single index case transmitted SARS-CoV-2 to co-workers over distances of more than 8 m, within a confined work area in which air is constantly recirculated and cooled. Viral genome sequencing shows that all cases share a set of mutations representing a novel sub-branch in the SARS-CoV-2 C20 clade. We identified the same set of mutations in samples collected in the time period between this initial infection cluster and a subsequent outbreak within the same factory, with the largest no. of confirmed SARS-CoV-2 cases in a German meat processing facility reported so far. Our results indicate climate conditions, fresh air exchange rates, and airflow as factors that can promote efficient spread of SARS-CoV-2 via long distances and provide insights into possible requirements for pandemic mitigation strategies in industrial workplace settings.
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    Kriegel, M.; Buchholz, U.; Gastmeier, P.; Bischoff, P.; Abdelgawad, I.; Hartmann, A. Predicted Infection Risk for Aerosol Transmission of SARS-CoV-2. medRxiv 2020,  DOI: 10.1101/2020.10.08.20209106 .
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    Stein-Zamir, C.; Abramson, N.; Shoob, H.; Libal, E.; Bitan, M.; Cardash, T.; Cayam, R.; Miskin, I. A Large COVID-19 Outbreak in a High School 10 Days after Schools’ Reopening, Israel, May 2020. Eurosurveillance 2020, 25, 1– 5,  DOI: 10.2807/1560-7917.ES.2020.25.29.2001352
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    A large COVID-19 outbreak in a high school 10 days after schools' reopening, Israel, May 2020
    Stein-Zamir, Chen; Abramson, Nitza; Shoob, Hanna; Libal, Erez; Bitan, Menachem; Cardash, Tanya; Cayam, Refael; Miskin, Ian
    Eurosurveillance (2020), 25 (29), 1-5CODEN: EUROGD; ISSN:1560-7917. (European Centre for Disease Prevention and Control)
    On 13 March 2020, Israel's government declared closure of all schools. Schools fully reopened on 17 May 2020. Ten days later, a major outbreak of COVID-19 occurred in a high school. The 1st case was registered on 26 May, the 2nd on 27 May. They were not epidemiol. linked. Testing of the complete school community revealed 153 students (attack rate: 13.2%) and 25 staff members (attack rate: 16.6%) who were COVID-19 pos.
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    Nardell, E. A.; Keegan, J.; Cheney, S. A.; Etkind, S. C. Airborne Infection: Theoretical Limits of Protection Achievable by Building Ventilation. Am. Rev. Respir. Dis. 1991, 144, 302– 306,  DOI: 10.1164/ajrccm/144.2.302
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    Airborne infection. Theoretical limits of protection achievable by building ventilation
    Nardell E A; Keegan J; Cheney S A; Etkind S C
    The American review of respiratory disease (1991), 144 (2), 302-6 ISSN:0003-0805.
    Of 67 office workers 27 (40%) had documented tuberculin skin test conversions after an estimated 4-wk exposure to a coworker with cavitary tuberculosis. Worker complaints for more than 2 yr before the tuberculosis exposure prompted investigations of air quality in the building before and after the tuberculosis exposure. Carbon dioxide concentrations in many parts of the building were found to be above recommended levels, indicating suboptimal ventilation with outdoor air. We applied a mathematical model of airborne transmission to the data to assess the role of building ventilation and other transmission factors. We estimated that ventilation with outside air averaged about 15 feet 3/min (cfm) per occupant, the low end of acceptable ventilation, corresponding to CO2 levels of about 1,000 ppm. The model predicted that at 25 cfm per person 18 workers would have been infected (a 33% reduction) and at 35 cfm, a level considered optimal for comfort, that 13 workers would have been infected (an additional 19% reduction). Further increases in outdoor air ventilation would be impractical and would have resulted in progressively smaller increments in protection. According to the model, the index case added approximately 13 infectious doses (quanta) per hour (qph) to the office air during the exposure period, 10 times the average infectiousness reported in a large series of tuberculosis cases. Further modeling predicted that as infectiousness rises, ventilation would offer progressively less protection. We conclude that outdoor air ventilation that is inadequate for comfort may contribute to airborne infection but that the protection afforded to building occupants by ventilation above comfort levels may be inherently limited, especially when the level of exposure to infection is high.
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    Gammaitoni, L.; Nucci, M. C. Using a Mathematical Model to Evaluate the Efficacy of TB Control Measures. Emerg. Infect. Dis. 1997, 3, 335– 342,  DOI: 10.3201/eid0303.970310
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    Using a mathematical model to evaluate the efficacy of TB control measures
    Gammaitoni L; Nucci M C
    Emerging infectious diseases (1997), 3 (3), 335-42 ISSN:1080-6040.
    We evaluated the efficacy of recommended tuberculosis (TB) infection control measures by using a deterministic mathematical model for airborne contagion. We examined the percentage of purified protein derivative conversions under various exposure conditions, environmental controlstrategies, and respiratory protective devices. We conclude that environmental control cannot eliminate the risk for TB transmission during high-risk procedures; respiratory protective devices, and particularly high-efficiency particulate air masks, may provide nearly complete protection if used with air filtration or ultraviolet irradiation. Nevertheless, the efficiency of these control measures decreases as the infectivity of the source case increases. Therefore, administrative control measures (e.g., indentifying and isolating patients with infectious TB) are the most effective because they substantially reduce the rate of infection.
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    Moser, M. R.; Bender, T. R.; Margolis, H. S.; Noble, G. R.; Kendal, A. P.; Ritter, D. G. An Outbreak of Influenza Aboard a Commercial Airliner. Am. J. Epidemiol. 1979, 110, 1– 6,  DOI: 10.1093/oxfordjournals.aje.a112781
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    An outbreak of influenza aboard a commercial airliner
    Moser M R; Bender T R; Margolis H S; Noble G R; Kendal A P; Ritter D G
    American journal of epidemiology (1979), 110 (1), 1-6 ISSN:0002-9262.
    A jet airliner with 54 persons aboard was delayed on the ground for three hours because of engine failure during a takeoff attempt. Most passengers stayed on the airplane during the delay. Within 72 hours, 72 per cent of the passengers became ill with symptoms of cough, fever, fatigue, headache, sore throat and myalgia. One passenger, the apparent index case, was ill on the airplane, and the clinical attack rate among the others varied with the amount of time spent aboard. Virus antigenically similar to A/Texas/1/77(H3N2) was isolated from 8 of 31 passengers cultured, and 20 of 22 ill persons tested had serologic evidence of infection with this virus. The airplane ventilation system was inoperative during the delay and this may account for the high attack rate.
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    Remington, P. L.; Hall, W. N.; Davis, I. H.; Herald, A.; Gunn, R. A. Airborne Transmission of Measles in a Physician’s Office. JAMA 1985, 253, 1574– 1577,  DOI: 10.1001/jama.1985.03350350068022
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    Airborne transmission of measles in a physician's office
    Remington P L; Hall W N; Davis I H; Herald A; Gunn R A
    JAMA (1985), 253 (11), 1574-7 ISSN:0098-7484.
    An unusual outbreak of measles occurred in 1982 in a pediatrician's office in Muskegon, Mich. Three children, who had arrived at the office 60 to 75 minutes after a child with measles had departed, developed measles. Using a model based on airborne transmission, it is estimated that the index patient was producing 144 units of infection (quanta) per minute while in the office. Characteristics such as coughing, increased warm air recirculation, and low relative humidity may have increased the likelihood of transmission. Adequate immunization of all patients and staff, respiratory isolation and prompt care of all suspected cases, and adequate fresh-air ventilation should decrease the risk of airborne transmission of measles in this setting. Airborne transmission may occur more often than previously suspected, a possibility that should be considered when evaluating current measles control strategies.
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    Wilson, N. M.; Marks, G. B.; Eckhardt, A.; Clarke, A. M.; Young, F. P.; Garden, F. L.; Stewart, W.; Cook, T. M.; Tovey, E. R. The Effect of Respiratory Activity, Non-Invasive Respiratory Support and Facemasks on Aerosol Generation and Its Relevance to COVID-19. Anaesthesia 2021, 76, 1465,  DOI: 10.1111/anae.15475
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    The effect of respiratory activity, non-invasive respiratory support and facemasks on aerosol generation and its relevance to COVID-19
    Wilson, N. M.; Marks, G. B.; Eckhardt, A.; Clarke, A. M.; Young, F. P.; Garden, F. L.; Stewart, W.; Cook, T. M.; Tovey, E. R.
    Anaesthesia (2021), 76 (11), 1465-1474CODEN: ANASAB; ISSN:0003-2409. (Wiley-Blackwell)
    Respirable aerosols (< 5 μm in diam.) present a high risk of SARS-CoV-2 transmission. Guidelines recommend using aerosol precautions during aerosol-generating procedures, and droplet (> 5 μm) precautions at other times. However, emerging evidence indicates respiratory activities may be a more important source of aerosols than clin. procedures such as tracheal intubation. We aimed to measure the size, total no. and vol. of all human aerosols exhaled during respiratory activities and therapies. We used a novel chamber with an optical particle counter sampling at 100 l.min-1 to count and size-fractionate close to all exhaled particles (0.5-25 μm). We compared emissions from ten healthy subjects during six respiratory activities (quiet breathing; talking; shouting; forced expiratory manoeuvres; exercise; and coughing) with three respiratory therapies (high-flow nasal oxygen and single or dual circuit non-invasive pos. pressure ventilation). Activities were repeated while wearing facemasks. When compared with quiet breathing, exertional respiratory activities increased particle counts 34.6-fold during talking and 370.8-fold during coughing (p < 0.001). High-flow nasal oxygen 60 at l.min-1 increased particle counts 2.3-fold (p = 0.031) during quiet breathing. Single and dual circuit non-invasive respiratory therapy at 25/10 cm. H2O with quiet breathing increased counts by 2.6-fold and 7.8-fold, resp. (both p < 0.001). During exertional activities, respiratory therapies and facemasks reduced emissions compared with activities alone. Respiratory activities (including exertional breathing and coughing) which mimic respiratory patterns during illness generate substantially more aerosols than non-invasive respiratory therapies, which conversely can reduce total emissions. We argue the risk of aerosol exposure is underappreciated and warrants widespread, targeted interventions.
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    Milton, D. K.; Fabian, M. P.; Cowling, B. J.; Grantham, M. L.; McDevitt, J. J. Influenza Virus Aerosols in Human Exhaled Breath: Particle Size, Culturability, and Effect of Surgical Masks. PLoS Pathog. 2013, 9, e1003205  DOI: 10.1371/journal.ppat.1003205
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    Influenza virus aerosols in human exhaled breath: particle size, culturability, and effect of surgical masks
    Milton, Donald K.; Patricia Fabian, M.; Cowling, Benjamin J.; Grantham, Michael L.; McDevitt, James J.
    PLoS Pathogens (2013), 9 (3), e1003205CODEN: PPLACN; ISSN:1553-7374. (Public Library of Science)
    The CDC recommends that healthcare settings provide influenza patients with facemasks as a means of reducing transmission to staff and other patients, and a recent report suggested that surgical masks can capture influenza virus in large droplet spray. However, there is minimal data on influenza virus aerosol shedding, the infectiousness of exhaled aerosols, and none on the impact of facemasks on viral aerosol shedding from patients with seasonal influenza. We collected samples of exhaled particles (one with and one without a facemask) in two size fractions ("coarse">5 μm, "fine" ≤5 μm) from 37 volunteers within 5 days of seasonal influenza onset, measured viral copy no. using quant. RT-PCR, and tested the fine-particle fraction for culturable virus. Fine particles contained 8.8 (95% CI 4.1 to 19) fold more viral copies than did coarse particles. Surgical masks reduced viral copy nos. in the fine fraction by 2.8 fold (95% CI 1.5 to 5.2) and in the coarse fraction by 25 fold (95% CI 3.5 to 180). Overall, masks produced a 3.4 fold (95% CI 1.8 to 6.3) redn. in viral aerosol shedding. Correlations between nasopharyngeal swab and the aerosol fraction copy nos. were weak (r = 0.17, coarse; r = 0.29, fine fraction). Copy nos. in exhaled breath declined rapidly with day after onset of illness. Two subjects with the highest copy nos. gave culture pos. fine particle samples. Surgical masks worn by patients reduce aerosols shedding of virus. The abundance of viral copies in fine particle aerosols and evidence for their infectiousness suggests an important role in seasonal influenza transmission. Monitoring exhaled virus aerosols will be important for validation of exptl. transmission studies in humans.
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    Lindsley, W. G.; Noti, J. D.; Blachere, F. M.; Thewlis, R. E.; Martin, S. B.; Othumpangat, S.; Noorbakhsh, B.; Goldsmith, W. T.; Vishnu, A.; Palmer, J. E.; Clark, K. E.; Beezhold, D. H. Viable Influenza A Virus in Airborne Particles from Human Coughs. J. Occup. Environ. Hyg. 2015, 12, 107– 113,  DOI: 10.1080/15459624.2014.973113
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    Viable Influenza A Virus in Airborne Particles from Human Coughs
    Lindsley, William G.; Noti, John D.; Blachere, Francoise M.; Thewlis, Robert E.; Martin, Stephen B.; Othumpangat, Sreekumar; Noorbakhsh, Bahar; Goldsmith, William T.; Vishnu, Abhishek; Palmer, Jan E.; Clark, Karen E.; Beezhold, Donald H.
    Journal of Occupational and Environmental Hygiene (2015), 12 (2), 107-113CODEN: JOEHA2; ISSN:1545-9624. (Taylor & Francis, Inc.)
    Patients with influenza release aerosol particles contg. the virus into their environment. However, the importance of airborne transmission in the spread of influenza is unclear, in part because of a lack of information about the infectivity of the airborne virus. The purpose of this study was to det. the amt. of viable influenza A virus that was expelled by patients in aerosol particles while coughing. Sixty-four symptomatic adult volunteer outpatients were asked to cough 6 times into a cough aerosol collection system. Seventeen of these participants tested pos. for influenza A virus by viral plaque assay (VPA) with confirmation by viral replication assay (VRA). Viable influenza A virus was detected in the cough aerosol particles from 7 of these 17 test subjects (41%). Viable influenza A virus was found in the smallest particle size fraction (0.3 μm to 8 μm), with a mean of 142 plaque-forming units (SD 215) expelled during the 6 coughs in particles of this size. These results suggest that a significant proportion of patients with influenza A release small airborne particles contg. viable virus into the environment. Although the amts. of influenza A detected in cough aerosol particles during our expts. were relatively low, larger quantities could be expelled by influenza patients during a pandemic when illnesses would be more severe. Our findings support the idea that airborne infectious particles could play an important role in the spread of influenza.
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    Yan, J.; Grantham, M.; Pantelic, J.; Bueno de Mesquita, P. J.; Albert, B.; Liu, F.; Ehrman, S.; Milton, D. K.; EMIT Consortium Infectious Virus in Exhaled Breath of Symptomatic Seasonal Influenza Cases from a College Community. Proc. Natl. Acad. Sci. U. S. A. 2018, 115, 1081– 1086,  DOI: 10.1073/pnas.1716561115
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    Infectious virus in exhaled breath of symptomatic seasonal influenza cases from a college community
    Yan, Jing; Grantham, Michael; Pantelic, Jovan; Bueno de Mesquita, P. Jacob; Albert, Barbara; Liu, Fengjie; Ehrman, Sheryl; Milton, Donald K.
    Proceedings of the National Academy of Sciences of the United States of America (2018), 115 (5), 1081-1086CODEN: PNASA6; ISSN:0027-8424. (National Academy of Sciences)
    Little is known about the amt. and infectiousness of influenza virus shed into exhaled breath. This contributes to uncertainty about the importance of airborne influenza transmission. We screened 355 symptomatic volunteers with acute respiratory illness and report 142 cases with confirmed influenza infection who provided 218 paired nasopharyngeal (NP) and 30-min breath samples (coarse >5-μm and fine ≤5-μm fractions) on days 1-3 after symptom onset. We assessed viral RNA copy no. for all samples and cultured NP swabs and fine aerosols. We recovered infectious virus from 52 (39%) of the fine aerosols and 150 (89%) of the NP swabs with valid cultures. The geometric mean RNA copy nos. were 3.8 × 104/30-min fine-, 1.2 × 104/30-min coarse-aerosol sample, and 8.2 × 108 per NP swab. Fine- and coarse-aerosol viral RNA were pos. assocd. with body mass index and no. of coughs and neg. assocd. with increasing days since symptom onset in adjusted models. Fine-aerosol viral RNA was also pos. assocd. with having influenza vaccination for both the current and prior season. NP swab viral RNA was pos. assocd. with upper respiratory symptoms and neg. assocd. with age but was not significantly assocd. with fine- or coarse-aerosol viral RNA or their predictors. Sneezing was rare, and sneezing and coughing were not necessary for infectious aerosol generation. Our observations suggest that influenza infection in the upper and lower airways are compartmentalized and independent.
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    Tiemersma, E. W.; van der Werf, M. J.; Borgdorff, M. W.; Williams, B. G.; Nagelkerke, N. J. D. Natural History of Tuberculosis: Duration and Fatality of Untreated Pulmonary Tuberculosis in HIV Negative Patients: A Systematic Review. PLoS One 2011, 6, e17601  DOI: 10.1371/journal.pone.0017601
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    Natural history of tuberculosis: duration and fatality of untreated pulmonary tuberculosis in HIV negative patients: a systematic review
    Tiemersma, Edine W.; van der Werf, Marieke J.; Borgdorff, Martien W.; Williams, Brian G.; Nagelkerke, Nico J. D.
    PLoS One (2011), 6 (4), e17601CODEN: POLNCL; ISSN:1932-6203. (Public Library of Science)
    Background: The prognosis, specifically the case fatality and duration, of untreated tuberculosis is important as many patients are not correctly diagnosed and therefore receive inadequate or no treatment. Furthermore, duration and case fatality of tuberculosis are key parameters in interpreting epidemiol. data. Methodol. and Principal Findings: To est. the duration and case fatality of untreated pulmonary tuberculosis in HIV neg. patients we reviewed studies from the pre-chemotherapy era. Untreated smear-pos. tuberculosis among HIV neg. individuals has a 10-yr case fatality variously reported between 53% and 86%, with a weighted mean of 70%. Ten-year case fatality of culture-pos. smear-neg. tuberculosis was nowhere reported directly but can be indirectly estd. to be approx. 20%. The duration of tuberculosis from onset to cure or death is approx. 3 years and appears to be similar for smear-pos. and smear-neg. tuberculosis. Conclusions: Current models of untreated tuberculosis that assume a total duration of 2 years until self-cure or death underestimate the duration of disease by about one year, but their case fatality ests. of 70% for smear-pos. and 20% for culture-pos. smear-neg. tuberculosis appear to be satisfactory.
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  • Abstract

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    Figure 1

    Figure 1. (a) Number of secondary cases vs. the risk parameter H and (b) attack rate vs. the relative risk parameter Hr for outbreaks of COVID-19, tuberculosis, influenza, and measles reported in the literature. A stronger outbreak in this figure refers to (i) more secondary infections, (ii) a higher attack rate, and (iii) a more infectious index case than typical outbreaks. The fitted trend line of attack rate as a function of Hr and its estimated uncertainty range (5th and 95th percentiles) are also shown in (b). All of the outbreaks investigated here involve the original variants of the virus. A variant twice as contagious (Ep0 × 2) should shift the fitted line to the left by a factor of two and displace the points of individual outbreaks upward.

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    Figure 2

    Figure 2. (a and b) Same format as Figure 1, but for COVID-19 only. Also shown are the H and Hr values for several common indoor situations (both prepandemic and pandemic) listed in Table S4. The H values for the cases with prepandemic settings except for a lower occupancy and the H and Hr values for the ASHRAE standard cases (52) (not other cases or outbreaks) with prepandemic settings except for a lower ventilation rate are shown for comparison. The standalone legend box is for (a) and (b) only. (c) Approximately multiplicative effects of various mitigation measures for the hospital general examination room case are also shown as an example.

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      Community outbreak investigation of SARS-CoV-2 transmission among bus riders in Eastern China
      Shen, Ye; Li, Changwei; Dong, Hongjun; Wang, Zhen; Martinez, Leonardo; Sun, Zhou; Handel, Andreas; Chen, Zhiping; Chen, Enfu; Ebell, Mark H.; Wang, Fan; Yi, Bo; Wang, Haibin; Wang, Xiaoxiao; Wang, Aihong; Chen, Bingbing; Qi, Yanling; Liang, Lirong; Li, Yang; Ling, Feng; Chen, Junfang; Xu, Guozhang
      JAMA Internal Medicine (2020), 180 (12), 1665-1671CODEN: JIMACF; ISSN:2168-6114. (American Medical Association)
      Importance Evidence of whether severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the virus that causes coronavirus disease 2019 (COVID-19), can be transmitted as an aerosol (ie, airborne) has substantial public health implications. Objective To investigate potential transmission routes of SARS-CoV-2 infection with epidemiol. evidence from a COVID-19 outbreak. Design, setting, and participants This cohort study examd. a community COVID-19 outbreak in Zhejiang province. On Jan. 19, 2020, 128 individuals took 2 buses (60 [46.9%] from bus 1 and 68 [53.1%] from bus 2) on a 100-min round trip to attend a 150-min worship event. The source patient was a passenger on bus 2. We compared risks of SARS-CoV-2 infection among at-risk individuals taking bus 1 (n = 60) and bus 2 (n = 67 [source patient excluded]) and among all other individuals (n = 172) attending the worship event. We also divided seats on the exposed bus into high-risk and low-risk zones according to the distance from the source patient and compared COVID-19 risks in each zone. In both buses, central air conditioners were in indoor recirculation mode. Main outcomes and measures SARS-CoV-2 infection was confirmed by reverse transcription polymerase chain reaction or by viral genome sequencing results. Attack rates for SARS-CoV-2 infection were calcd. for different groups, and the spatial distribution of individuals who developed infection on bus 2 was obtained. Results Of the 128 participants, 15 (11.7%) were men, 113 (88.3%) were women, and the mean age was 58.6 years. On bus 2, 24 of the 68 individuals (35.3% [including the index patient]) received a diagnosis of COVID-19 after the event. Meanwhile, none of the 60 individuals in bus 1 were infected. Among the other 172 individuals at the worship event, 7 (4.1%) subsequently received a COVID-19 diagnosis. Individuals in bus 2 had a 34.3% (95% CI, 24.1%-46.3%) higher risk of getting COVID-19 compared with those in bus 1 and were 11.4 (95% CI, 5.1-25.4) times more likely to have COVID-19 compared with all other individuals attending the worship event. Within bus 2, individuals in high-risk zones had moderately, but nonsignificantly, higher risk for COVID-19 compared with those in the low-risk zones. The absence of a significantly increased risk in the part of the bus closer to the index case suggested that airborne spread of the virus may at least partially explain the markedly high attack rate obsd. Conclusions and relevance In this cohort study and case investigation of a community outbreak of COVID-19 in Zhejiang province, individuals who rode a bus to a worship event with a patient with COVID-19 had a higher risk of SARS-CoV-2 infection than individuals who rode another bus to the same event. Airborne spread of SARS-CoV-2 seems likely to have contributed to the high attack rate in the exposed bus. Future efforts at prevention and control must consider the potential for airborne spread of the virus.
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    20. 20
      Kwon, K. S.; Park, J. I.; Park, Y. J.; Jung, D. M.; Ryu, K. W.; Lee, J. H. Evidence of Long-Distance Droplet Transmission of SARS-CoV-2 by Direct Air Flow in a Restaurant in Korea. J. Korean Med. Sci. 2020, 35, e415  DOI: 10.3346/jkms.2020.35.e415
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      Evidence of long-distance droplet transmission of SARS-COV-2 by direct air flow in a restaurant in Korea
      Kwon, Keun-Sang; Park, Jung-Im; Park, Young Joon; Jung, Don-Myung; Ryu, Ki-Wahn; Lee, Ju-Hyung
      Journal of Korean Medical Science (2020), 35 (46), e415CODEN: JKMSEH; ISSN:1598-6357. (Korean Academy of Medical Sciences)
      The transmission mode of severe acute respiratory syndrome coronavirus 2 is primarily known as droplet transmission. However, a recent argument has emerged about the possibility of airborne transmission. On June 17, there was a coronavirus disease 2019 (COVID-19) outbreak in Korea assocd. with long distance droplet transmission. The epidemiol. investigation was implemented based on personal interviews and data collection on closed-circuit television images, and cell phone location data. The epidemic investigation support system developed by the Korea Disease Control and Prevention Agency was used for contact tracing. At the restaurant considered the site of exposure, air flow direction and velocity, distances between cases, and movement of visitors were investigated. A total of 3 cases were identified in this outbreak, and max. air flow velocity of 1.2 m/s was measured between the infector and infectee in a restaurant equipped with ceiling-type air conditioners. The index case was infected at a 6.5 m away from the infector and 5 min exposure without any direct or indirect contact. Droplet transmission can occur at a distance greater than 2 m if there is direct air flow from an infected person. Therefore, updated guidelines involving prevention, contact tracing, and quarantine for COVID-19 are required for control of this highly contagious disease.
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    21. 21
      Jang, S.; Han, S. H.; Rhee, J. Y. Cluster of Coronavirus Disease Associated with Fitness Dance Classes, South Korea. Emerg. Infect. Dis. 2020, 26, 1917– 1920,  DOI: 10.3201/eid2608.200633
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      Cluster of coronavirus disease associated with fitness dance classes, South Korea
      Jang, Sukbin; Han, Si Hyun; Rhee, Ji-Young
      Emerging Infectious Diseases (2020), 26 (8), 1917-1920CODEN: EIDIFA; ISSN:1080-6059. (Centers for Disease Control and Prevention)
      During 24 days in Cheonan, South Korea, 112 persons were infected with severe acute respiratory syndrome coronavirus 2 assocd. with fitness dance classes at 12 sports facilities. Intense phys. exercise in densely populated sports facilities could increase risk for infection. Vigorous exercise in confined spaces should be minimized during outbreaks.
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    22. 22
      Eichler, N.; Thornley, C.; Swadi, T.; Devine, T.; McElnay, C.; Sherwood, J.; Brunton, C.; Williamson, F.; Freeman, J.; Berger, S.; Ren, X.; Storey, M.; de Ligt, J.; Geoghegan, J. L. Transmission of Severe Acute Respiratory Syndrome Coronavirus 2 during Border Quarantine and Air Travel, New Zealand (Aotearoa). Emerg. Infect. Dis. 2021, 27, 1274– 1278,  DOI: 10.3201/eid2705.210514
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      Transmission of severe acute respiratory syndrome coronavirus 2 during border quarantine and air travel, New Zealand (Aotearoa)
      Eichler, Nick; Thornley, Craig; Swadi, Tara; Devine, Tom; McElnay, Caroline; Sherwood, Jillian; Brunton, Cheryl; Williamson, Felicity; Freeman, Josh; Berger, Sarah; Ren, Xiaoyun; Storey, Matt; de Ligt, Joep; Geoghegan, Jemma L.
      Emerging Infectious Diseases (2021), 27 (5), 1274-1278CODEN: EIDIFA; ISSN:1080-6059. (Centers for Disease Control and Prevention)
      The strategy in New Zealand (Aotearoa) to eliminate coronavirus disease requires that international arrivals undergo managed isolation and quarantine and mandatory testing for severe acute respiratory syndrome coronavirus 2. Combining genomic and epidemiol. data, we investigated the origin of an acute case of coronavirus disease identified in the community after the patient had spent 14 days in managed isolation and quarantine and had 2 neg. test results. By combining genomic sequence anal. and epidemiol. investigations, we identified a multibranched chain of transmission of this virus, including on international and domestic flights, as well as a probable case of aerosol transmission without direct person-to-person contact. These findings show the power of integrating genomic and epidemiol. data to inform outbreak investigations.
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    23. 23
      Nissen, K.; Krambrich, J.; Akaberi, D.; Hoffman, T.; Ling, J.; Lundkvist, Å.; Svensson, L.; Salaneck, E. Long-Distance Airborne Dispersal of SARS-CoV-2 in COVID-19 Wards. Sci. Rep. 2020, 10, 19589,  DOI: 10.1038/s41598-020-76442-2
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      23
      Long-distance airborne dispersal of SARS-CoV-2 in COVID-19 wards
      Nissen, Karolina; Krambrich, Janina; Akaberi, Dario; Hoffman, Tove; Ling, Jiaxin; Lundkvist, Aake; Svensson, Lennart; Salaneck, Erik
      Scientific Reports (2020), 10 (1), 19589CODEN: SRCEC3; ISSN:2045-2322. (Nature Research)
      Abstr.: Evidence suggests that SARS-CoV-2, as well as other coronaviruses, can be dispersed and potentially transmitted by aerosols directly or via ventilation systems. We therefore investigated ventilation openings in one COVID-19 ward and central ducts that expel indoor air from three COVID-19 wards at Uppsala University Hospital, Sweden, during Apr. and May 2020. Swab samples were taken from individual ceiling ventilation openings and surfaces in central ducts. Samples were subsequently subjected to rRT-PCR targeting the N and E genes of SARS-CoV-2. Central ventilation HEPA filters, located several stories above the wards, were removed and portions analyzed in the same manner. In two subsequent samplings, SARS-CoV-2 N and E genes were detected in seven and four out of 19 room vents, resp. Central ventilation HEPA exhaust filters from the ward were found pos. for both genes in three samples. Corresponding filters from two other, adjacent COVID-19 wards were also found pos. Infective ability of the samples was assessed by inoculation of susceptible cell cultures but could not be detd. in these expts. Detection of SARS-CoV-2 in central ventilation systems, distant from patient areas, indicate that virus can be transported long distances and that droplet transmission alone cannot reasonably explain this, esp. considering the relatively low air change rates in these wards. Airborne transmission of SARS-CoV-2 must be taken into consideration for preventive measures.
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    24. 24
      Hwang, S. E.; Chang, J. H.; Oh, B.; Heo, J. Possible Aerosol Transmission of COVID-19 Associated with an Outbreak in an Apartment in Seoul, South Korea, 2020. Int. J. Infect. Dis. 2021, 104, 73– 76,  DOI: 10.1016/j.ijid.2020.12.035
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      Possible aerosol transmission of COVID-19 associated with an outbreak in an apartment in Seoul, South Korea, 2020
      Hwang, Seo Eun; Chang, Je Hwan; Oh, Bumjo; Heo, Jongho
      International Journal of Infectious Diseases (2021), 104 (), 73-76CODEN: IJIDF3; ISSN:1201-9712. (Elsevier Ltd.)
      Scientists have strongly implied that aerosols could be the plausible cause of coronavirus disease-2019 (COVID-19) transmission; however, aerosol transmission remains controversial. We investigated the epidemiol. relationship among infected cases on a recent cluster infection of COVID-19 in an apartment building in Seoul, South Korea. All infected cases were found along two vertical lines of the building, and each line was connected through a single air duct in the bathroom for natural ventilation. Our investigation found no other possible contact between the cases than the airborne infection through a single air duct in the bathroom. The virus from the first infected case can be spread to upstairs and downstairs through the air duct by the (reverse) stack effect, which explains the air movement in a vertical shaft. This study suggests aerosol transmission, particularly indoors with insufficient ventilation, which is underappreciated.
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    25. 25
      Li, Y.; Leung, G. M.; Tang, J. W.; Yang, X.; Chao, C. Y. H.; Lin, J. Z.; Lu, J. W.; Nielsen, P. V.; Niu, J.; Qian, H.; Sleigh, A. C.; Su, H.-J. J.; Sundell, J.; Wong, T. W.; Yuen, P. L. Role of Ventilation in Airborne Transmission of Infectious Agents in the Built Environment - a Multidisciplinary Systematic Review. Indoor Air 2007, 17, 2– 18,  DOI: 10.1111/j.1600-0668.2006.00445.x
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      25
      Role of ventilation in airborne transmission of infectious agents in the built environment - a multidisciplinary systematic review
      Li Y; Leung G M; Tang J W; Yang X; Chao C Y H; Lin J Z; Lu J W; Nielsen P V; Niu J; Qian H; Sleigh A C; Su H-J J; Sundell J; Wong T W; Yuen P L
      Indoor air (2007), 17 (1), 2-18 ISSN:0905-6947.
      There have been few recent studies demonstrating a definitive association between the transmission of airborne infections and the ventilation of buildings. The severe acute respiratory syndrome (SARS) epidemic in 2003 and current concerns about the risk of an avian influenza (H5N1) pandemic, have made a review of this area timely. We searched the major literature databases between 1960 and 2005, and then screened titles and abstracts, and finally selected 40 original studies based on a set of criteria. We established a review panel comprising medical and engineering experts in the fields of microbiology, medicine, epidemiology, indoor air quality, building ventilation, etc. Most panel members had experience with research into the 2003 SARS epidemic. The panel systematically assessed 40 original studies through both individual assessment and a 2-day face-to-face consensus meeting. Ten of 40 studies reviewed were considered to be conclusive with regard to the association between building ventilation and the transmission of airborne infection. There is strong and sufficient evidence to demonstrate the association between ventilation, air movements in buildings and the transmission/spread of infectious diseases such as measles, tuberculosis, chickenpox, influenza, smallpox and SARS. There is insufficient data to specify and quantify the minimum ventilation requirements in hospitals, schools, offices, homes and isolation rooms in relation to spread of infectious diseases via the airborne route. PRACTICAL IMPLICATION: The strong and sufficient evidence of the association between ventilation, the control of airflow direction in buildings, and the transmission and spread of infectious diseases supports the use of negatively pressurized isolation rooms for patients with these diseases in hospitals, in addition to the use of other engineering control methods. However, the lack of sufficient data on the specification and quantification of the minimum ventilation requirements in hospitals, schools and offices in relation to the spread of airborne infectious diseases, suggest the existence of a knowledge gap. Our study reveals a strong need for a multidisciplinary study in investigating disease outbreaks, and the impact of indoor air environments on the spread of airborne infectious diseases.
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    26. 26
      Jones, N. R.; Qureshi, Z. U.; Temple, R. J.; Larwood, J. P. J.; Greenhalgh, T.; Bourouiba, L. Two Metres or One: What Is the Evidence for Physical Distancing in Covid-19?. BMJ 2020, 370, m3223  DOI: 10.1136/bmj.m3223
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      Morawska, L.; Tang, J. W.; Bahnfleth, W.; Bluyssen, P. M.; Boerstra, A.; Buonanno, G.; Cao, J.; Dancer, S.; Floto, A.; Franchimon, F.; Haworth, C.; Hogeling, J.; Isaxon, C.; Jimenez, J. L.; Kurnitski, J.; Li, Y.; Loomans, M.; Marks, G.; Marr, L. C.; Mazzarella, L.; Melikov, A. K.; Miller, S.; Milton, D. K.; Nazaroff, W.; Nielsen, P. V.; Noakes, C.; Peccia, J.; Querol, X.; Sekhar, C.; Seppänen, O.; Tanabe, S.-I.; Tellier, R.; Tham, K. W.; Wargocki, P.; Wierzbicka, A.; Yao, M. How Can Airborne Transmission of COVID-19 Indoors Be Minimised?. Environ. Int. 2020, 142, 105832  DOI: 10.1016/j.envint.2020.105832
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      27
      How can airborne transmission of COVID-19 indoors be minimized?
      Morawska, Lidia; Tang, Julian W.; Bahnfleth, William; Bluyssen, Philomena M.; Boerstra, Atze; Buonanno, Giorgio; Cao, Junji; Dancer, Stephanie; Floto, Andres; Franchimon, Francesco; Haworth, Charles; Hogeling, Jaap; Isaxon, Christina; Jimenez, Jose L.; Kurnitski, Jarek; Li, Yuguo; Loomans, Marcel; Marks, Guy; Marr, Linsey C.; Mazzarella, Livio; Melikov, Arsen Krikor; Miller, Shelly; Milton, Donald K.; Nazaroff, William; Nielsen, Peter V.; Noakes, Catherine; Peccia, Jordan; Querol, Xavier; Sekhar, Chandra; Seppanen, Olli; Tanabe, Shin-ichi; Tellier, Raymond; Tham, Kwok Wai; Wargocki, Pawel; Wierzbicka, Aneta; Yao, Maosheng
      Environment International (2020), 142 (), 105832CODEN: ENVIDV; ISSN:0160-4120. (Elsevier Ltd.)
      During the rapid rise in COVID-19 illnesses and deaths globally, and notwithstanding recommended precautions, questions are voiced about routes of transmission for this pandemic disease. Inhaling small airborne droplets is probable as a third route of infection, in addn. to more widely recognized transmission via larger respiratory droplets and direct contact with infected people or contaminated surfaces. While uncertainties remain regarding the relative contributions of the different transmission pathways, we argue that existing evidence is sufficiently strong to warrant engineering controls targeting airborne transmission as part of an overall strategy to limit infection risk indoors. Appropriate building engineering controls include sufficient and effective ventilation, possibly enhanced by particle filtration and air disinfection, avoiding air recirculation and avoiding overcrowding. Often, such measures can be easily implemented and without much cost, but if only they are recognized as significant in contributing to infection control goals. We believe that the use of engineering controls in public buildings, including hospitals, shops, offices, schools, kindergartens, libraries, restaurants, cruise ships, elevators, conference rooms or public transport, in parallel with effective application of other controls (including isolation and quarantine, social distancing and hand hygiene), would be an addnl. important measure globally to reduce the likelihood of transmission and thereby protect healthcare workers, patients and the general public.
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    28. 28
      Bond, T. C.; Bosco-Lauth, A.; Farmer, D. K.; Francisco, P. W.; Pierce, J. R.; Fedak, K. M.; Ham, J. M.; Jathar, S. H.; VandeWoude, S. Quantifying Proximity, Confinement, and Interventions in Disease Outbreaks: A Decision Support Framework for Air-Transported Pathogens. Environ. Sci. Technol. 2021, 55, 2890– 2898,  DOI: 10.1021/acs.est.0c07721
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      Quantifying Proximity, Confinement, and Interventions in Disease Outbreaks: A Decision Support Framework for Air-Transported Pathogens
      Bond, Tami C.; Bosco-Lauth, Angela; Farmer, Delphine K.; Francisco, Paul W.; Pierce, Jeffrey R.; Fedak, Kristen M.; Ham, Jay M.; Jathar, Shantanu H.; VandeWoude, Sue
      Environmental Science & Technology (2021), 55 (5), 2890-2898CODEN: ESTHAG; ISSN:0013-936X. (American Chemical Society)
      The inability to communicate how infectious diseases are transmitted in human environments has triggered avoidance of interactions during the COVID-19 pandemic. We define a metric, Effective ReBreathed Vol. (ERBV), that encapsulates how infectious pathogens, including SARS-CoV-2, transport in air. ERBV separates environmental transport from other factors in the chain of infection, allowing quant. comparisons among situations. Particle size affects transport, removal onto surfaces, and elimination by mitigation measures, so ERBV is presented for a range of exhaled particle diams.: 1, 10, and 100μm. Pathogen transport depends on both proximity and confinement. If interpersonal distancing of 2 m is maintained, then confinement, not proximity, dominates rebreathing after 10-15 min in enclosed spaces for all but 100μm particles. We analyze strategies to reduce this confinement effect. Ventilation and filtration reduce person-to-person transport of 1μm particles (ERBV1) by 13-85% in residential and office situations. Deposition to surfaces competes with intentional removal for 10 and 100μm particles, so the same interventions reduce ERBV10 by only 3-50%, and ERBV100 is unaffected. Prior knowledge of size-dependent ERBV would help identify transmission modes and effective interventions. This framework supports mitigation decisions in emerging situations, even before other infectious parameters are known.
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      Riley, E. C.; Murphy, G.; Riley, R. L. Airborne Spread of Measles in a Suburban Elementary School. Am. J. Epidemiol. 1978, 107, 421– 432,  DOI: 10.1093/oxfordjournals.aje.a112560
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      Airborne spread of measles in a suburban elementary school
      Riley E C; Murphy G; Riley R L
      American journal of epidemiology (1978), 107 (5), 421-32 ISSN:0002-9262.
      A measles epidemic in a modern suburban elementary school in upstate New York in spring, 1974, is analyzed in terms of a model which provides a basis for apportioning the chance of infection from classmates sharing the same home room, from airborne organisms recirculated by the ventilating system, and from exposure in school buses. The epidemic was notable because of its explosive nature and its occurrence in a school where 97% of the children had been vaccinated. Many had been vaccinated at less than one year of age. The index case was a girl in second grade who produced 28 secondary cases in 14 different classrooms. Organisms recirculated by the ventilating system were strongly implicated. After two subsequent generations, 60 children had been infected, and the epidemic subsided. From estimates of major physical and biologic factors, it was possible to calculate that the index case produced approximately 93 units of airborne infection (quanta) per minute. The epidemic pattern suggested that the secondaries were less infectious by an order of magnitude. The exceptional infectiousness of the index case, inadequate immunization of many of the children, and the high percentage of air recirculated throughout the school, are believed to account for the extent and sharpness of the outbreak.
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      Noakes, C. J.; Sleigh, P. A. Mathematical Models for Assessing the Role of Airflow on the Risk of Airborne Infection in Hospital Wards. J. R. Soc. Interface. 2009, 6 Suppl 6, S791,  DOI: 10.1098/rsif.2009.0305.focus
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      Jimenez, J. L.; Peng, Z. COVID-19 Aerosol Transmission Estimator https://tinyurl.com/covid-estimator (accessed Mar 26, 2021).
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      Buonanno, G.; Morawska, L.; Stabile, L. Quantitative Assessment of the Risk of Airborne Transmission of SARS-CoV-2 Infection: Prospective and Retrospective Applications. Environ. Int. 2020, 145, 106112  DOI: 10.1016/j.envint.2020.106112
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      Quantitative assessment of the risk of airborne transmission of SARS-CoV-2 infection: Prospective and retrospective applications
      Buonanno, G.; Morawska, L.; Stabile, L.
      Environment International (2020), 145 (), 106112CODEN: ENVIDV; ISSN:0160-4120. (Elsevier Ltd.)
      Airborne transmission is a recognized pathway of contagion; however, it is rarely quant. evaluated. The numerous outbreaks that have occurred during the SARS-CoV-2 pandemic are putting a demand on researchers to develop approaches capable of both predicting contagion in closed environments (predictive assessment) and analyzing previous infections (retrospective assessment). This study presents a novel approach for quant. assessment of the individual infection risk of susceptible subjects exposed in indoor microenvironments in the presence of an asymptomatic infected SARS-CoV-2 subject. The application of a Monte Carlo method allowed the risk for an exposed healthy subject to be evaluated or, starting from an acceptable risk, the max. exposure time. We applied the proposed approach to four distinct scenarios for a prospective assessment, highlighting that, in order to guarantee an acceptable risk of 10-3 for exposed subjects in naturally ventilated indoor environments, the exposure time could be well below one hour. Such max. exposure time clearly depends on the viral load emission of the infected subject and on the exposure conditions; thus, longer exposure times were estd. for mech. ventilated indoor environments and lower viral load emissions. The proposed approach was used for retrospective assessment of documented outbreaks in a restaurant in Guangzhou (China) and at a choir rehearsal in Mount Vernon (USA), showing that, in both cases, the high attack rate values can be justified only assuming the airborne transmission as the main route of contagion. Moreover, we show that such outbreaks are not caused by the rare presence of a superspreader, but can be likely explained by the co-existence of conditions, including emission and exposure parameters, leading to a highly probable event, which can be defined as a "superspreading event".
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    33. 33
      Lelieveld, J.; Helleis, F.; Borrmann, S.; Cheng, Y.; Drewnick, F.; Haug, G.; Klimach, T.; Sciare, J.; Su, H.; Pöschl, U. Model Calculations of Aerosol Transmission and Infection Risk of COVID-19 in Indoor Environments. Int. J. Environ. Res. Public Health 2020, 17, 8114,  DOI: 10.3390/ijerph17218114
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      Model Calculations of Aerosol Transmission and Infection Risk of COVID-19 in indoor environments
      Lelieveld, Jos; Helleis, Frank; Borrmann, Stephan; Cheng, Yafang; Drewnick, Frank; Haug, Gerald; Klimach, Thomas; Sciare, Jean; Su, Hang; Poeschl, Ulrich
      International Journal of Environmental Research and Public Health (2020), 17 (21), 8114CODEN: IJERGQ; ISSN:1660-4601. (MDPI AG)
      The role of aerosolized SARS-CoV-2 viruses in airborne transmission of COVID-19 has been debated. The aerosols are transmitted through breathing and vocalization by infectious subjects. Some authors state that this represents the dominant route of spreading, while others dismiss the option. Here we present an adjustable algorithm to est. the infection risk for different indoor environments, constrained by published data of human aerosol emissions, SARS-CoV-2 viral loads, infective dose and other parameters. We evaluate typical indoor settings such as an office, a classroom, choir practice, and a reception/party. Our results suggest that aerosols from highly infective subjects can effectively transmit COVID-19 in indoor environments. This "highly infective" category represents approx. 20% of the patients who tested pos. for SARS-CoV-2. We find that "super infective" subjects, representing the top 5-10% of subjects with a pos. test, plus an unknown fraction of less-but still highly infective, high aerosol-emitting subjects-may cause COVID-19 clusters (>10 infections). In general, active room ventilation and the ubiquitous wearing of face masks (i.e., by all subjects) may reduce the individual infection risk by a factor of five to ten, similar to high-vol., high-efficiency particulate air (HEPA) filtering. A particularly effective mitigation measure is the use of high-quality masks, which can drastically reduce the indoor infection risk through aerosols.
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    34. 34
      Jones, B.; Sharpe, P.; Iddon, C.; Hathway, E. A.; Noakes, C. J.; Fitzgerald, S. Modelling Uncertainty in the Relative Risk of Exposure to the SARS-CoV-2 Virus by Airborne Aerosol Transmission in Well Mixed Indoor Air. Build. Environ. 2021, 191, 107617  DOI: 10.1016/j.buildenv.2021.107617
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      Modelling uncertainty in the relative risk of exposure to the SARS-CoV-2 virus by airborne aerosol transmission in well mixed indoor air
      Jones Benjamin; Sharpe Patrick; Iddon Christopher; Hathway E Abigail; Noakes Catherine J; Fitzgerald Shaun
      Building and environment (2021), 191 (), 107617 ISSN:0360-1323.
      We present a mathematical model and a statistical framework to estimate uncertainty in the number of SARS-CoV-2 genome copies deposited in the respiratory tract of a susceptible person, [Formula: see text] , over time in a well mixed indoor space. By relating the predicted median [Formula: see text] for a reference scenario to other locations, a Relative Exposure Index (REI) is established that reduces the need to understand the infection dose probability but is nevertheless a function of space volume, viral emission rate, exposure time, occupant respiratory activity, and room ventilation. A 7 h day in a UK school classroom is used as a reference scenario because its geometry, building services, and occupancy have uniformity and are regulated. The REI is used to highlight types of indoor space, respiratory activity, ventilation provision and other factors that increase the likelihood of far field ( [Formula: see text] m) exposure. The classroom reference scenario and an 8 h day in a 20 person office both have an [Formula: see text] and so are a suitable for comparison with other scenarios. A poorly ventilated classroom (1.2 l s(-1) per person) has [Formula: see text] suggesting that ventilation should be monitored in classrooms to minimise far field aerosol exposure risk. Scenarios involving high aerobic activities or singing have [Formula: see text] ; a 1 h gym visit has a median [Formula: see text] , and the Skagit Choir superspreading event has [Formula: see text] . Spaces with occupancy activities and exposure times comparable to those of the reference scenario must preserve the reference scenario volume flow rate as a minimum rate to achieve [Formula: see text] , irrespective of the number of occupants present.
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      Han, E.; Tan, M. M. J.; Turk, E.; Sridhar, D.; Leung, G. M.; Shibuya, K.; Asgari, N.; Oh, J.; García-Basteiro, A. L.; Hanefeld, J.; Cook, A. R.; Hsu, L. Y.; Teo, Y. Y.; Heymann, D.; Clark, H.; McKee, M.; Legido-Quigley, H. Lessons Learnt from Easing COVID-19 Restrictions: An Analysis of Countries and Regions in Asia Pacific and Europe. Lancet 2020, 396, 1525– 1534,  DOI: 10.1016/S0140-6736(20)32007-9
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      Lessons learnt from easing COVID-19 restrictions: an analysis of countries and regions in Asia Pacific and Europe
      Han, Emeline; Tan, Melisa Mei Jin; Turk, Eva; Sridhar, Devi; Leung, Gabriel M.; Shibuya, Kenji; Asgari, Nima; Oh, Juhwan; Garcia-Basteiro, Alberto L.; Hanefeld, Johanna; Cook, Alex R.; Hsu, Li Yang; Teo, Yik Ying; Heymann, David; Clark, Helen; McKee, Martin; Legido-Quigley, Helena
      Lancet (2020), 396 (10261), 1525-1534CODEN: LANCAO; ISSN:0140-6736. (Elsevier Ltd.)
      The COVID-19 pandemic is an unprecedented global crisis. Many countries have implemented restrictions on population movement to slow the spread of severe acute respiratory syndrome coronavirus 2 and prevent health systems from becoming overwhelmed; some have instituted full or partial lockdowns. However, lockdowns and other extreme restrictions cannot be sustained for the long term in the hope that there will be an effective vaccine or treatment for COVID-19. Governments worldwide now face the common challenge of easing lockdowns and restrictions while balancing various health, social, and economic concerns. To facilitate cross-country learning, this Health Policy paper uses an adapted framework to examine the approaches taken by nine high-income countries and regions that have started to ease COVID-19 restrictions: five in the Asia Pacific region (ie, Hong Kong [Special Administrative Region], Japan, New Zealand, Singapore, and South Korea) and four in Europe (ie, Germany, Norway, Spain, and the UK). This comparative anal. presents important lessons to be learnt from the experiences of these countries and regions. Although the future of the virus is unknown at present, countries should continue to share their experiences, shield populations who are at risk, and suppress transmission to save lives.
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      Buonanno, G.; Stabile, L.; Morawska, L. Estimation of Airborne Viral Emission: Quanta Emission Rate of SARS-CoV-2 for Infection Risk Assessment. Environ. Int. 2020, 141, 105794  DOI: 10.1016/j.envint.2020.105794
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      Estimation of airborne viral emission: Quanta emission rate of SARS-CoV-2 for infection risk assessment
      Buonanno, G.; Stabile, L.; Morawska, L.
      Environment International (2020), 141 (), 105794CODEN: ENVIDV; ISSN:0160-4120. (Elsevier Ltd.)
      Airborne transmission is a pathway of contagion that is still not sufficiently investigated despite the evidence in the scientific literature of the role it can play in the context of an epidemic. While the medical research area dedicates efforts to find cures and remedies to counteract the effects of a virus, the engineering area is involved in providing risk assessments in indoor environments by simulating the airborne transmission of the virus during an epidemic. To this end, virus air emission data are needed. Unfortunately, this information is usually available only after the outbreak, based on specific reverse engineering cases. In this work, a novel approach to est. the viral load emitted by a contagious subject on the basis of the viral load in the mouth, the type of respiratory activity (e.g. breathing, speaking, whispering), respiratory physiol. parameters (e.g. inhalation rate), and activity level (e.g. resting, standing, light exercise) is proposed. The results showed that high quanta emission rates (>100 quanta h-1) can be reached by an asymptomatic infectious SARS-CoV-2 subject performing vocalization during light activities (i.e. walking slowly) whereas a symptomatic SARS-CoV-2 subject in resting conditions mostly has a low quanta emission rate (<1 quantum h-1). The findings in terms of quanta emission rates were then adopted in infection risk models to demonstrate its application by evaluating the no. of people infected by an asymptomatic SARS-CoV-2 subject in Italian indoor microenvironments before and after the introduction of virus containment measures. The results obtained from the simulations clearly highlight that a key role is played by proper ventilation in containment of the virus in indoor environments.
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      Peng, Z.; Jimenez, J. L. Exhaled CO2 as a COVID-19 Infection Risk Proxy for Different Indoor Environments and Activities. Environ. Sci. Technol. Lett. 2021, 8, 392– 397,  DOI: 10.1021/acs.estlett.1c00183
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      Exhaled CO2 as a COVID-19 Infection Risk Proxy for Different Indoor Environments and Activities
      Peng, Zhe; Jimenez, Jose L.
      Environmental Science & Technology Letters (2021), 8 (5), 392-397CODEN: ESTLCU; ISSN:2328-8930. (American Chemical Society)
      CO2 is co-exhaled with aerosols contg. SARS-CoV-2 by COVID-19-infected people and can be used as a proxy of SARS-CoV-2 concns. indoors. Indoor CO2 measurements by low-cost sensors hold promise for mass monitoring of indoor aerosol transmission risk for COVID-19 and other respiratory diseases. We derive anal. expressions of CO2-based risk proxies and apply them to various typical indoor environments. The relative infection risk in a given environment scales with excess CO2 level, and thus, keeping CO2 as low as feasible in a space allows optimization of the protection provided by ventilation. The CO2 level corresponding to a given abs. infection risk varies by >2 orders of magnitude for different environments and activities. Although large uncertainties, mainly from virus exhalation rates, are still assocd. with infection risk ests., our study provides more specific and practical recommendations for low-cost CO2-based indoor infection risk monitoring.
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      Ma, J.; Qi, X.; Chen, H.; Li, X.; Zhang, Z.; Wang, H.; Sun, L.; Zhang, L.; Guo, J.; Morawska, L.; Grinshpun, S. A.; Biswas, P.; Flagan, R. C.; Yao, M. COVID-19 Patients in Earlier Stages Exhaled Millions of SARS-CoV-2 per Hour. Clin. Infect. Dis. 2021, 72, e652– e654,  DOI: 10.1093/cid/ciaa1283
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      Coronavirus disease 2019 patients in earlier stages exhaled millions of severe acute respiratory syndrome coronavirus 2 per hour
      Ma, Jianxin; Qi, Xiao; Chen, Haoxuan; Li, Xinyue; Zhang, Zheng; Wang, Haibin; Sun, Lingli; Zhang, Lu; Guo, Jiazhen; Morawska, Lidia; Grinshpun, Sergey A.; Biswas, Pratim; Flagan, Richard C.; Yao, Maosheng
      Clinical Infectious Diseases (2021), 72 (10), e652-e654CODEN: CIDIEL; ISSN:1537-6591. (Oxford University Press)
      Coronavirus disease 2019 (COVID-19) patients exhaled millions of severe acute respiratory syndrome coronavirus 2 RNA copies per h, which plays an important role in COVID-19 transmission. Exhaled breath had a higher pos. rate (26.9%, n = 52) than surface (5.4%, n = 242) and air (3.8%, n = 26) samples.
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      Volz, E.; Mishra, S.; Chand, M.; Barrett, J. C.; Johnson, R.; Geidelberg, L.; Hinsley, W. R.; Laydon, D. J.; Dabrera, G.; O’Toole, Á.; Amato, R.; Ragonnet-Cronin, M.; Harrison, I.; Jackson, B.; Ariani, C. V.; Boyd, O.; Loman, N. J.; McCrone, J. T.; Gonçalves, S.; Jorgensen, D.; Myers, R.; Hill, V.; Jackson, D. K.; Gaythorpe, K.; Groves, N.; Sillitoe, J.; Kwiatkowski, D. P.; COVID-19 Genomics UK (COG-UK) consortium; Flaxman, S.; Ratmann, O.; Bhatt, S.; Hopkins, S.; Gandy, A.; Rambaut, A.; Ferguson, N. M. Assessing Transmissibility of SARS-CoV-2 Lineage B.1.1.7 in England. Nature 2021, 593, 266– 269,  DOI: 10.1038/s41586-021-03470-x
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      Assessing transmissibility of SARS-CoV-2 lineage B.1.1.7 in England
      Volz, Erik; Mishra, Swapnil; Chand, Meera; Barrett, Jeffrey C.; Johnson, Robert; Geidelberg, Lily; Hinsley, Wes R.; Laydon, Daniel J.; Dabrera, Gavin; O'Toole, Aine; Amato, Robert; Ragonnet-Cronin, Manon; Harrison, Ian; Jackson, Ben; Ariani, Cristina V.; Boyd, Olivia; Loman, Nicholas J.; McCrone, John T.; Goncalves, Sonia; Jorgensen, David; Myers, Richard; Hill, Verity; Jackson, David K.; Gaythorpe, Katy; Groves, Natalie; Sillitoe, John; Kwiatkowski, Dominic P.; Flaxman, Seth; Ratmann, Oliver; Bhatt, Samir; Hopkins, Susan; Gandy, Axel; Rambaut, Andrew; Ferguson, Neil M.
      Nature (London, United Kingdom) (2021), 593 (7858), 266-269CODEN: NATUAS; ISSN:0028-0836. (Nature Portfolio)
      The SARS-CoV-2 lineage B.1.1.7, designated variant of concern (VOC) 202012/01 by Public Health England, was first identified in the UK in late summer to early autumn 2020. Whole-genome SARS-CoV-2 sequence data collected from community-based diagnostic testing for COVID-19 show an extremely rapid expansion of the B.1.1.7 lineage during autumn 2020, suggesting that it has a selective advantage. Changes in VOC frequency inferred from genetic data correspond closely to changes inferred by S gene target failures (SGTF) in community-based diagnostic PCR testing. Anal. of trends in SGTF and non-SGTF case nos. in local areas across England shows that B.1.1.7 has higher transmissibility than non-VOC lineages, even if it has a different latent period or generation time. The SGTF data indicate a transient shift in the age compn. of reported cases, with cases of B.1.1.7 including a larger share of under 20-yr-olds than non-VOC cases. We estd. time-varying reprodn. nos. for B.1.1.7 and co-circulating lineages using SGTF and genomic data. The best-supported models did not indicate a substantial difference in VOC transmissibility among different age groups, but all analyses agreed that B.1.1.7 has a substantial transmission advantage over other lineages, with a 50-100% higher reprodn. no.
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      Kidd, M.; Richter, A.; Best, A.; Cumley, N.; Mirza, J.; Percival, B.; Mayhew, M.; Megram, O.; Ashford, F.; White, T.; Moles-Garcia, E.; Crawford, L.; Bosworth, A.; Atabani, S. F.; Plant, T.; McNally, A. S-Variant SARS-CoV-2 Lineage B1.1.7 Is Associated with Significantly Higher Viral Loads in Samples Tested by Thermo Fisher Taq Path RT-qPCR. J. Infect. Dis. 2021, 223, 1666,  DOI: 10.1093/infdis/jiab082
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      S-variant SARS-CoV-2 lineage B1.1.7 is associated with significantly higher viral load in samples tested by taqpath polymerase chain reaction
      Kidd, Michael; Richter, Alex; Best, Angus; Cumley, Nicola; Mirza, Jeremy; Percival, Benita; Mayhew, Megan; Megram, Oliver; Ashford, Fiona; White, Thomas; Moles-Garcia, Emma; Crawford, Liam; Bosworth, Andrew; Atabani, Sowsan F.; Plant, Tim; McNally, Alan
      Journal of Infectious Diseases (2021), 223 (10), 1666-1670CODEN: JIDIAQ; ISSN:1537-6613. (Oxford University Press)
      A SARS-CoV-2 variant B1.1.7 contg. mutation Δ69/70 has spread rapidly in the United Kingdom and shows an identifiable profile in ThermoFisher TaqPath RT-qPCR, S gene target failure (SGTF). We analyzed recent test data for trends and significance. Linked cycle threshold (Ct) values for respiratory samples showed that a low Ct for ORF1ab and N were clearly assocd. with SGTF. Significantly more SGTF samples had higher inferred viral loads between 1 x 107 and 1 x 108. Our that patient whose samples exhibit the SGTF profile are more likely to have high viral loads, which may explain higher infectivity and rapidity of spread.
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      Edwards, D. A.; Ausiello, D.; Salzman, J.; Devlin, T.; Langer, R.; Beddingfield, B. J.; Fears, A. C.; Doyle-Meyers, L. A.; Redmann, R. K.; Killeen, S. Z.; Maness, N. J.; Roy, C. J. Exhaled Aerosol Increases with COVID-19 Infection, Age, and Obesity. Proc. Natl. Acad. Sci. U. S. A. 2021, 118, e2021830118  DOI: 10.1073/pnas.2021830118
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      Exhaled aerosol increases with COVID-19 infection, age, and obesity
      Edwards, David A.; Ausiello, Dennis; Salzman, Jonathan; Devlin, Tom; Langer, Robert; Beddingfield, Brandon J.; Fears, Alyssa C.; Doyle-Meyers, Lara A.; Redmann, Rachel K.; Killeen, Stephanie Z.; Maness, Nicholas J.; Roy, Chad J.
      Proceedings of the National Academy of Sciences of the United States of America (2021), 118 (8), e2021830118CODEN: PNASA6; ISSN:0027-8424. (National Academy of Sciences)
      COVID-19 transmits by droplets generated from surfaces of airway mucus during processes of respiration within hosts infected by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) virus. We studied respiratory droplet generation and exhalation in human and nonhuman primate subjects with and without COVID-19 infection to explore whether SARS-CoV-2 infection, and other changes in physiol. state, translate into observable evolution of nos. and sizes of exhaled respiratory droplets in healthy and diseased subjects. In our observational cohort study of the exhaled breath particles of 194 healthy human subjects, and in our exptl. infection study of eight nonhuman primates infected, by aerosol, with SARS-CoV-2, we found that exhaled aerosol particles vary between subjects by three orders of magnitude, with exhaled respiratory droplet no. increasing with degree of COVID-19 infection and elevated BMI-years. We obsd. that 18% of human subjects (35) accounted for 80% of the exhaled bioaerosol of the group (194), reflecting a superspreader distribution of bioaerosol analogous to a classical 20:80 superspreader of infection distribution. These findings suggest that quant. assessment and control of exhaled aerosol may be crit. to slowing the airborne spread of COVID-19 in the absence of an effective and widely disseminated vaccine.
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      van Doremalen, N.; Bushmaker, T.; Morris, D. H.; Holbrook, M. G.; Gamble, A.; Williamson, B. N.; Tamin, A.; Harcourt, J. L.; Thornburg, N. J.; Gerber, S. I.; Lloyd-Smith, J. O.; de Wit, E.; Munster, V. J. Aerosol and Surface Stability of SARS-CoV-2 as Compared with SARS-CoV-1. N. Engl. J. Med. 2020, 382, 1564– 1567,  DOI: 10.1056/NEJMc2004973
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      Aerosol and Surface Stability of SARS-CoV-2 as Compared with SARS-CoV-1
      van Doremalen Neeltje; Bushmaker Trenton; Holbrook Myndi G; Williamson Brandi N; de Wit Emmie; Munster Vincent J; Morris Dylan H; Gamble Amandine; Tamin Azaibi; Harcourt Jennifer L; Thornburg Natalie J; Gerber Susan I; Lloyd-Smith James O
      The New England journal of medicine (2020), 382 (16), 1564-1567 ISSN:.
      There is no expanded citation for this reference.
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      Chan, K. H.; Peiris, J. S. M.; Lam, S. Y.; Poon, L. L. M.; Yuen, K. Y.; Seto, W. H. The Effects of Temperature and Relative Humidity on the Viability of the SARS Coronavirus. Adv. Virol. 2011, 2011, 734690  DOI: 10.1155/2011/734690
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      The Effects of Temperature and Relative Humidity on the Viability of the SARS Coronavirus
      Chan K H; Peiris J S Malik; Lam S Y; Poon L L M; Yuen K Y; Seto W H
      Advances in virology (2011), 2011 (), 734690 ISSN:.
      The main route of transmission of SARS CoV infection is presumed to be respiratory droplets. However the virus is also detectable in other body fluids and excreta. The stability of the virus at different temperatures and relative humidity on smooth surfaces were studied. The dried virus on smooth surfaces retained its viability for over 5 days at temperatures of 22-25°C and relative humidity of 40-50%, that is, typical air-conditioned environments. However, virus viability was rapidly lost (>3 log(10)) at higher temperatures and higher relative humidity (e.g., 38°C, and relative humidity of >95%). The better stability of SARS coronavirus at low temperature and low humidity environment may facilitate its transmission in community in subtropical area (such as Hong Kong) during the spring and in air-conditioned environments. It may also explain why some Asian countries in tropical area (such as Malaysia, Indonesia or Thailand) with high temperature and high relative humidity environment did not have major community outbreaks of SARS.
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      Dabisch, P.; Schuit, M.; Herzog, A.; Beck, K.; Wood, S.; Krause, M.; Miller, D.; Weaver, W.; Freeburger, D.; Hooper, I.; Green, B.; Williams, G.; Holland, B.; Bohannon, J.; Wahl, V.; Yolitz, J.; Hevey, M.; Ratnesar-Shumate, S. The Influence of Temperature, Humidity, and Simulated Sunlight on the Infectivity of SARS-CoV-2 in Aerosols. Aerosol Sci. Technol. 2021, 55, 142– 153,  DOI: 10.1080/02786826.2020.1829536
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      The influence of temperature, humidity, and simulated sunlight on the infectivity of SARS-CoV-2 in aerosols
      Dabisch, Paul; Schuit, Michael; Herzog, Artemas; Beck, Katie; Wood, Stewart; Krause, Melissa; Miller, David; Weaver, Wade; Freeburger, Denise; Hooper, Idris; Green, Brian; Williams, Gregory; Holland, Brian; Bohannon, Jordan; Wahl, Victoria; Yolitz, Jason; Hevey, Michael; Ratnesar-Shumate, Shanna
      Aerosol Science and Technology (2021), 55 (2), 142-153CODEN: ASTYDQ; ISSN:0278-6826. (Taylor & Francis, Inc.)
      Recent evidence suggests that respiratory aerosols may play a role in the spread of SARS-CoV-2 during the ongoing COVID-19 pandemic. The authors' lab. has previously demonstrated that simulated sunlight inactivated SARS-CoV-2 in aerosols and on surfaces. In the present study, the authors extend these findings to include the persistence of SARS-CoV-2 in aerosols across a range of temp., humidity, and simulated sunlight levels using an environmentally controlled rotating drum aerosol chamber. The results demonstrate that temp., simulated sunlight, and humidity are all significant factors influencing the persistence of infectious SARS-CoV-2 in aerosols, but that simulated sunlight and temp. have a greater influence on decay than humidity across the range of conditions tested. The time needed for a 90% decrease in infectious virus ranged from 4.8 min at 40°C, 20% relative humidity, and high intensity simulated sunlight representative of noon on a clear day on the summer solstice at 40°N latitude, to greater than two hours under conditions representative of those expected indoors or at night. These results suggest that the persistence of infectious SARS-CoV-2 in naturally occurring aerosols may be affected by environmental conditions, and that aerosolized virus could remain infectious for extended periods of time under some environmental conditions. The present study provides a comprehensive dataset on the influence of environmental parameters on the survival of SARS-CoV-2 in aerosols that can be utilized, along with data on viral shedding from infected individuals and the inhalational infectious dose, to inform future modeling and risk assessment efforts.
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      Johnson, G. R.; Morawska, L.; Ristovski, Z. D.; Hargreaves, M.; Mengersen, K.; Chao, C. Y. H.; Wan, M. P.; Li, Y.; Xie, X.; Katoshevski, D.; Corbett, S. Modality of Human Expired Aerosol Size Distributions. J. Aerosol Sci. 2011, 42, 839– 851,  DOI: 10.1016/j.jaerosci.2011.07.009
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      Modality of human expired aerosol size distributions
      Johnson, G. R.; Morawska, L.; Ristovski, Z. D.; Hargreaves, M.; Mengersen, K.; Chao, C. Y. H.; Wan, M. P.; Li, Y.; Xie, X.; Katoshevski, D.; Corbett, S.
      Journal of Aerosol Science (2011), 42 (12), 839-851CODEN: JALSB7; ISSN:0021-8502. (Elsevier Ltd.)
      An essential starting point when investigating the potential role of human expired aerosols in the transmission of disease is to gain a comprehensive knowledge of the expired aerosol generation process, including the aerosol size distribution, the various droplet prodn. mechanisms involved and the corresponding sites of prodn. within the respiratory tract. In order to approach this level of understanding we have integrated the results of two different investigative techniques spanning 3 decades of particle size from 700 nm to 1 mm, presenting a single composite size distribution, and identifying the most prominent modes in that distribution. We link these modes to specific sites of origin and mechanisms of prodn. The data for this were obtained using the Aerodynamic Particle Sizer (APS) covering the range 0.7≤d≤20 μm and Droplet Deposition Anal. (DDA) covering the range d≥20 μm. In the case of speech three distinct droplet size distribution modes were identified with count median diams. at 1.6, 2.5 and 145 μm. In the case of voluntary coughing the modes were located at 1.6, 1.7 and 123 μm. The modes are assocd. with three distinct processes: one occurring deep in the lower respiratory tract, another in the region of the larynx and a third in the upper respiratory tract including the oral cavity. The first of these, the Bronchiolar Fluid Film Burst (BFFB or B) mode contains droplets produced during normal breathing. The second, the Laryngeal (L) mode is most active during voicing and coughing. The third, the Oral (O) cavity mode is active during speech and coughing. The no. of droplets and the vol. of aerosol material assocd. with each mode of aerosol prodn. during speech and coughing is presented. The size distribution is modeled as a tri-modal lognormal distribution dubbed the Bronchiolar/Laryngeal/Oral (B.L.O.) tri-modal model.
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      Thatcher, T. L.; Lai, A. C. K.; Moreno-Jackson, R.; Sextro, R. G.; Nazaroff, W. W. Effects of Room Furnishings and Air Speed on Particle Deposition Rates Indoors. Atmos. Environ. 2002, 36, 1811– 1819,  DOI: 10.1016/S1352-2310(02)00157-7
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      Effects of room furnishings and air speed on particle deposition rates indoors
      Thatcher, Tracy L.; Lai, Alvin C. K.; Moreno-Jackson, Rosa; Sextro, Richard G.; Nazaroff, William W.
      Atmospheric Environment (2002), 36 (11), 1811-1819CODEN: AENVEQ; ISSN:1352-2310. (Elsevier Science Ltd.)
      Particle deposition to surfaces plays an important role in detg. exposure to indoor particles; however, the effect of furnishings and air speed on these rates has not been well characterized. Expts. were performed in an isolated room (vol. = 14.2 m3) using 3 different indoor furnishing levels (bare, carpeted, fully furnished) and 4 different air flow conditions. Deposition loss rates were detd. by generating a short burst of polydispersed particles, then measuring size-resolved (0.5-10 μm) concn. decay rate using an aerodynamic particle sizer. Increasing the surface area from bare (35 m2 nominal surface area) to fully furnished (12 m2 addnl. surface area) increased the deposition loss rate by as much as a factor of 2.6; largest increase was obsd. for the smallest particles. Increasing the mean air speed from <5 to 19 cm/s by increasing fan speed, increased the deposition rate for all particle sizes by factors of 1.3-2.4, with larger particles exhibiting greater effects than smaller particles. The significant effect of particle size and room conditions on deposition loss rates argues against using a single, first-order loss-rate coeff. to represent deposition for integrated mass measurements (PM2.5 or PM10).
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      Residential air-change rates: A critical review
      Nazaroff William W
      Indoor air (2021), 31 (2), 282-313 ISSN:.
      Air-change rate is an important parameter influencing residential air quality. This article critically assesses the state of knowledge regarding residential air-change rates, emphasizing periods of normal occupancy. Cumulatively, about 40 prior studies have measured air-change rates in approximately 10,000 homes using tracer gases, including metabolic CO2 . The central tendency of the air-change rates determined in these studies is reasonably described as lognormal with a geometric mean of 0.5 h(-1) and a geometric standard deviation of 2.0. However, the geometric means of individual studies vary, mainly within the range 0.2-1 h(-1) . Air-change rates also vary with time in residences. Factors influencing the air-change rate include weather (indoor-outdoor temperature difference and wind speed), the leakiness of the building envelope, and, when present, operation of mechanical ventilation systems. Occupancy-associated factors are also important, including window opening, induced exhaust from flued combustion, and use of heating and cooling systems. Empirical and methodological challenges remain to be effectively addressed. These include clarifying the time variation of air-change rates in residences during occupancy and understanding the influence of time-varying air-change rates on tracer-gas measurement techniques. Important opportunities are available to improve understanding of air-change rates and interzonal flows as factors affecting the source-to-exposure relationships for indoor air pollutants.
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    50. 50
      Persily, A. K.; Gorfain, J.; Brunner, G. Survey of Ventilation Rates in Office Buildings. Build. Res. Inf. 2006, 34, 459– 466,  DOI: 10.1080/09613210600809128
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      Batterman, S.; Su, F.-C.; Wald, A.; Watkins, F.; Godwin, C.; Thun, G. Ventilation Rates in Recently Constructed U.S. School Classrooms. Indoor Air 2017, 27, 880– 890,  DOI: 10.1111/ina.12384
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      Ventilation rates in recently constructed U.S. school classrooms
      Batterman S; Su F-C; Wald A; Watkins F; Godwin C; Thun G
      Indoor air (2017), 27 (5), 880-890 ISSN:.
      Low ventilation rates (VRs) in schools have been associated with absenteeism, poorer academic performance, and teacher dissatisfaction. We measured VRs in 37 recently constructed or renovated and mechanically ventilated U.S. schools, including LEED and EnergyStar-certified buildings, using CO2 and the steady-state, build-up, decay, and transient mass balance methods. The transient mass balance method better matched conditions (specifically, changes in occupancy) and minimized biases seen in the other methods. During the school day, air change rates (ACRs) averaged 2.0±1.3 hour(-1) , and only 22% of classrooms met recommended minimum ventilation rates. HVAC systems were shut off at the school day close, and ACRs dropped to 0.21±0.19 hour(-1) . VRs did not differ by building type, although cost-cutting and comfort measures resulted in low VRs and potentially impaired IAQ. VRs were lower in schools that used unit ventilators or radiant heating, in smaller schools and in larger classrooms. The steady-state, build-up, and decay methods had significant limitations and biases, showing the need to confirm that these methods are appropriate. Findings highlight the need to increase VRs and to ensure that energy saving and comfort measures do not compromise ventilation and IAQ.
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      ASHRAE Ventilation for Acceptable Indoor Air Quality. ANSI/ASHRAE Standard 62.1–2019; ANSI/ASHRAE 2019.
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      ASHRAE ASHRAE Position Document on Infectious Aerosols; American Society of Heating, Refrigerating and Air-Conditioning Engineers 2020.
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      REHVA How to Operate HVAC and Other Building Service Systems to Prevent the Spread of the Coronavirus (SARS-CoV-2) Disease (COVID-19) in Workplaces; Federation of European Heating, Ventilation and Air Conditioning Associations 2020.
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      Chen, P. Z.; Bobrovitz, N.; Premji, Z.; Koopmans, M.; Fisman, D. N.; Gu, F. X. Heterogeneity in Transmissibility and Shedding SARS-CoV-2 via Droplets and Aerosols. Elife 2021, 10, e65774  DOI: 10.7554/eLife.65774
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      Heterogeneity in transmissibility and shedding SARS-CoV-2 via droplets and aerosols
      Chen, Paul Z.; Bobrovitz, Niklas; Premji, Zahra; Koopmans, Marion; Fisman, David N.; Gu, Frank X.
      eLife (2021), 10 (), e65774CODEN: ELIFA8; ISSN:2050-084X. (eLife Sciences Publications Ltd.)
      Background: Which virol. factors mediate overdispersion in the transmissibility of emerging viruses remains a long-standing question in infectious disease epidemiol. Methods: Here, we use systematic review to develop a comprehensive dataset of respiratory viral loads (rVLs) of SARS-CoV-2, SARS-CoV-1 and influenza A(H1N1)pdm09. We then comparatively meta-analyze the data and model individual infectiousness by shedding viable virus via respiratory droplets and aerosols. Results: The analyses indicate heterogeneity in rVL as an intrinsic virol. factor facilitating greater overdispersion for SARS-CoV-2 in the COVID-19 pandemic than A(H1N1)pdm09 in the 2009 influenza pandemic. For COVID-19, case heterogeneity remains broad throughout the infectious period, including for pediatric and asymptomatic infections. Hence, many COVID-19 cases inherently present minimal transmission risk, whereas highly infectious individuals shed tens to thousands of SARS-CoV-2 virions/min via droplets and aerosols while breathing, talking and singing. Coughing increases the contagiousness, esp. in close contact, of symptomatic cases relative to asymptomatic ones. Infectiousness tends to be elevated between 1 and 5 days post- symptom onset. Conclusions: Intrinsic case variation in rVL facilitates overdispersion in the transmissibility of emerging respiratory viruses. Our findings present considerations for disease control in the COVID- 19 pandemic as well as future outbreaks of novel viruses. Funding: Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant program, NSERC Senior Industrial Research Chair program and the Toronto COVID-19 Action Fund.
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    56. 56
      Yang, Q.; Saldi, T. K.; Gonzales, P. K.; Lasda, E.; Decker, C. J.; Tat, K. L.; Fink, M. R.; Hager, C. R.; Davis, J. C.; Ozeroff, C. D.; Muhlrad, D.; Clark, S. K.; Fattor, W. T.; Meyerson, N. R.; Paige, C. L.; Gilchrist, A. R.; Barbachano-Guerrero, A.; Worden-Sapper, E. R.; Wu, S. S.; Brisson, G. R.; McQueen, M. B.; Dowell, R. D.; Leinwand, L.; Parker, R.; Sawyer, S. L. Just 2% of SARS-CoV-2–positive Individuals Carry 90% of the Virus Circulating in Communities. Proc. Natl. Acad. Sci. U. S. A. 2021, 118, e2104547118  DOI: 10.1073/pnas.2104547118
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      Just 2% of SARS-CoV-2-positive individuals carry 90% of the virus circulating in communities
      Yang, Qing; Saldi, Tassa K.; Gonzales, Patrick K.; Lasda, Erika; Decker, Carolyn J.; Tat, Kimngan L.; Fink, Morgan R.; Hager, Cole R.; Davis, Jack C.; Ozeroff, Christopher D.; Muhlrad, Denise; Clark, Stephen K.; Fattor, Will T.; Meyerson, Nicholas R.; Paige, Camille L.; Gilchrist, Alison R.; Barbachano-Guerrero, Arturo; Worden-Sapper, Emma R.; Wu, Sharon S.; Brisson, Gloria R.; McQueen, Matthew B.; Dowell, Robin D.; Leinwand, Leslie; Parker, Roy; Sawyer, Sara L.
      Proceedings of the National Academy of Sciences of the United States of America (2021), 118 (21), e2104547118CODEN: PNASA6; ISSN:0027-8424. (National Academy of Sciences)
      We analyze data from the fall 2020 pandemic response efforts at the University of Colorado Boulder, where more than 72,500 saliva samples were tested for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) using qRT-PCR. All samples were collected from individuals who reported no symptoms assocd. with COVID-19 on the day of collection. From these, 1,405 pos. cases were identified. The distribution of viral loads within these asymptomatic individuals was indistinguishable from what has been previously obsd. in symptomatic individuals. Regardless of symptomatic status, ∼50% of individuals who test pos. for SARS-CoV-2 seem to be in noninfectious phases of the disease, based on having low viral loads in a range from which live virus has rarely been isolated. We find that, at any given time, just 2% of individuals carry 90% of the virions circulating within communities, serving as viral 'supercarriers' and possibly also superspreaders.
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    57. 57
      Wu, S. L.; Mertens, A. N.; Crider, Y. S.; Nguyen, A.; Pokpongkiat, N. N.; Djajadi, S.; Seth, A.; Hsiang, M. S.; Colford, J. M.; Reingold, A.; Arnold, B. F.; Hubbard, A.; Benjamin-Chung, J. Substantial Underestimation of SARS-CoV-2 Infection in the United States. Nat. Commun. 2020, 11, 4507,  DOI: 10.1038/s41467-020-18272-4
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      Substantial underestimation of SARS-CoV-2 infection in the United States
      Wu, Sean L.; Mertens, Andrew N.; Crider, Yoshika S.; Nguyen, Anna; Pokpongkiat, Nolan N.; Djajadi, Stephanie; Seth, Anmol; Hsiang, Michelle S.; Colford Jr., John M.; Reingold, Art; Arnold, Benjamin F.; Hubbard, Alan; Benjamin-Chung, Jade
      Nature Communications (2020), 11 (1), 4507CODEN: NCAOBW; ISSN:2041-1723. (Nature Research)
      Accurate ests. of the burden of SARS-CoV-2 infection are crit. to informing pandemic response. Confirmed COVID-19 case counts in the U.S. do not capture the total burden of the pandemic because testing has been primarily restricted to individuals with moderate to severe symptoms due to limited test availability. Here, the authors use a semi-Bayesian probabilistic bias anal. to account for incomplete testing and imperfect diagnostic accuracy. The authors est. 6454,951 cumulative infections compared to 721,245 confirmed cases (1.9% vs. 0.2% of the population) in the United States as of Apr. 18, 2020. Accounting for uncertainty, the no. of infections during this period was 3 to 20 times higher than the no. of confirmed cases. 86% (simulation interval: 64-99%) of this difference is due to incomplete testing, while 14% (0.3-36%) is due to imperfect test accuracy. The approach can readily be applied in future studies in other locations or at finer spatial scale to correct for biased testing and imperfect diagnostic accuracy to provide a more realistic assessment of COVID-19 burden.
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      Jones, T. C.; Biele, G.; Mühlemann, B.; Veith, T.; Schneider, J.; Beheim-Schwarzbach, J.; Bleicker, T.; Tesch, J.; Schmidt, M. L.; Sander, L. E.; Kurth, F.; Menzel, P.; Schwarzer, R.; Zuchowski, M.; Hofmann, J.; Krumbholz, A.; Stein, A.; Edelmann, A.; Corman, V. M.; Drosten, C. Estimating Infectiousness throughout SARS-CoV-2 Infection Course. Science 2021, 373, eabi5273  DOI: 10.1126/science.abi5273
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      Ou, C.; Hu, S.; Luo, K.; Yang, H.; Hang, J.; Cheng, P.; Hai, Z.; Xiao, S.; Qian, H.; Xiao, S.; Jing, X.; Xie, Z.; Ling, H.; Liu, L.; Gao, L.; Deng, Q.; Cowling, B. J.; Li, Y. Insufficient Ventilation Led to a Probable Long-Range Airborne Transmission of SARS-CoV-2 on Two Buses. Build. Environ. 2022, 207, 108414  DOI: 10.1016/j.buildenv.2021.108414
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      Insufficient ventilation led to a probable long-range airborne transmission of SARS-CoV-2 on two buses
      Ou Cuiyun; Yang Hongyu; Hang Jian; Ling Hong; Hu Shixiong; Luo Kaiwei; Gao Lidong; Cheng Pan; Xiao Shenglan; Li Yuguo; Hai Zheng; Jing Xinping; Xie Zhengshen; Xiao Shanliang; Qian Hua; Liu Li; Deng Qihong; Cowling Benjamin J; Li Yuguo
      Building and environment (2022), 207 (), 108414 ISSN:0360-1323.
      Uncertainty remains on the threshold of ventilation rate in airborne transmission of SARS-CoV-2. We analyzed a COVID-19 outbreak in January 2020 in Hunan Province, China, involving an infected 24-year-old man, Mr. X, taking two subsequent buses, B1 and B2, in the same afternoon. We investigated the possibility of airborne transmission and the ventilation conditions for its occurrence. The ventilation rates on the buses were measured using a tracer-concentration decay method with the original driver on the original route. We measured and calculated the spread of the exhaled virus-laden droplet tracer from the suspected index case. Ten additional passengers were found to be infected, with seven of them (including one asymptomatic) on B1 and two on B2 when Mr. X was present, and one passenger infected on the subsequent B1 trip. B1 and B2 had time-averaged ventilation rates of approximately 1.7 and 3.2 L/s per person, respectively. The difference in ventilation rates and exposure time could explain why B1 had a higher attack rate than B2. Airborne transmission due to poor ventilation below 3.2 L/s played a role in this two-bus outbreak of COVID-19.
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    60. 60
      Park, S. Y.; Kim, Y. M.; Yi, S.; Lee, S.; Na, B. J.; Kim, C. B.; Kim, J. I.; Kim, H. S.; Kim, Y. B.; Park, Y.; Huh, I. S.; Kim, H. K.; Yoon, H. J.; Jang, H.; Kim, K.; Chang, Y.; Kim, I.; Lee, H.; Gwack, J.; Kim, S. S.; Kim, M.; Kweon, S.; Choe, Y. J.; Park, O.; Park, Y. J.; Jeong, E. K. Coronavirus Disease Outbreak in Call Center, South Korea. Emerg. Infect. Dis. 2020, 26, 1666– 1670,  DOI: 10.3201/eid2608.201274
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      Coronavirus disease outbreak in call center, South Korea
      Park, Shin Young; Kim, Young-Man; Yi, Seonju; Lee, Sangeun; Na, Baeg-Ju; Kim, Chang Bo; Kim, Jung-il; Kim, Hea Sook; Kim, Young Bok; Park, Yoojin; Huh, In Sil; Kim, Hye Kyung; Yoon, Hyung Jun; Jang, Hanaram; Kim, Kyungnam; Chang, Yeonhwa; Kim, Inhye; Lee, Hyeyoung; Gwack, Jin; Kim, Seong Sun; Kim, Miyoung; Kweon, Sanghui; Choe, Young June; Park, Ok; Park, Young Joon; Jeong, Eun Kyeong
      Emerging Infectious Diseases (2020), 26 (8), 1666-1670CODEN: EIDIFA; ISSN:1080-6059. (Centers for Disease Control and Prevention)
      We describe the epidemiol. of a coronavirus disease (COVID-19) outbreak in a call center in South Korea. We obtained information on demog. characteristics by using standardized epidemiol. investigation forms. We performed descriptive analyses and reported the results as frequencies and proportions for categoric variables. Of 1,143 persons who were tested for COVID-19, a total of 97 (8.5%, 95% CI 7.0%-10.3%) had confirmed cases. Of these, 94 were working in an 11th-floor call center with 216 employees, translating to an attack rate of 43.5% (95% CI 36.9%-50.4%). The household secondary attack rate among symptomatic case-patients was 16.2% (95% CI 11.6%- 22.0%). Of the 97 persons with confirmed COVID-19, only 4 (1.9%) remained asymptomatic within 14 days of quarantine, and none of their household contacts acquired secondary infections. Extensive contact tracing, testing all contacts, and early quarantine blocked further transmission and might be effective for contg. rapid outbreaks in crowded work settings.
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      Khanh, N. C.; Thai, P. Q.; Quach, H.-L.; Thi, N.-A. H.; Dinh, P. C.; Duong, T. N.; Mai, L. T. Q.; Nghia, N. D.; Tu, T. A.; Quang, L. N.; Quang, T. D.; Nguyen, T.-T.; Vogt, F.; Anh, D. D. Transmission of SARS-CoV 2 During Long-Haul Flight. Emerg. Infect. Dis. 2020, 26, 2617– 2624,  DOI: 10.3201/eid2611.203299
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      Transmission of SARS-CoV-2 during long-haul flight
      Khanh, Nguyen Cong; Thai, Pham Quang; Quach, Ha-Linh; Thi, Ngoc-Anh Hoang; Dinh, Phung Cong; Duong, Tran Nhu; Mai, Le Thi Quynh; Nghia, Ngu Duy; Tu, Tran Anh; Quang, La Ngoc; Quang, Tran Dai; Nguyen, Trong-Tai; Vogt, Florian; Anh, Dang Duc
      Emerging Infectious Diseases (2020), 26 (11), 2617-2624CODEN: EIDIFA; ISSN:1080-6059. (Centers for Disease Control and Prevention)
      To assess the role of in-flight transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the authors investigated a cluster of cases among passengers on a 10-h com. flight. Affected persons were passengers, crew, and their close contacts. The authors traced 217 passengers and crew to their final destinations and interviewed, tested, and quarantined them. Among the 16 persons in whom SARS-CoV-2 infection was detected, 12 (75%) were passengers seated in business class along with the only symptomatic person (attack rate 62%). Seating proximity was strongly assocd. with increased infection risk (risk ratio 7.3, 95% CI 1.2-46.2). The authors found no strong evidence supporting alternative transmission scenarios. In-flight transmission that probably originated from 1 symptomatic passenger caused a large cluster of cases during a long flight. Guidelines for preventing SARS-CoV-2 infection among air passengers should consider individual passengers' risk for infection, the no. of passengers traveling, and flight duration.
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      Günther, T.; Czech-Sioli, M.; Indenbirken, D.; Robitaille, A.; Tenhaken, P.; Exner, M.; Ottinger, M.; Fischer, N.; Grundhoff, A.; Brinkmann, M. M. SARS-CoV-2 Outbreak Investigation in a German Meat Processing Plant. EMBO Mol. Med. 2020, 12, e13296  DOI: 10.15252/emmm.202013296
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      SARS-CoV-2 outbreak investigation in a German meat processing plant
      Guenther, Thomas; Czech-Sioli, Manja; Indenbirken, Daniela; Robitaille, Alexis; Tenhaken, Peter; Exner, Martin; Ottinger, Matthias; Fischer, Nicole; Grundhoff, Adam; Brinkmann, Melanie M.
      EMBO Molecular Medicine (2020), 12 (12), e13296CODEN: EMMMAM; ISSN:1757-4684. (Wiley-Blackwell)
      We describe a multifactorial investigation of a SARS-CoV-2 outbreak in a large meat processing complex in Germany. Infection event timing, spatial, climate and ventilation conditions in the processing plant, sharing of living quarters and transport, and viral genome sequences were analyzed. Our results suggest that a single index case transmitted SARS-CoV-2 to co-workers over distances of more than 8 m, within a confined work area in which air is constantly recirculated and cooled. Viral genome sequencing shows that all cases share a set of mutations representing a novel sub-branch in the SARS-CoV-2 C20 clade. We identified the same set of mutations in samples collected in the time period between this initial infection cluster and a subsequent outbreak within the same factory, with the largest no. of confirmed SARS-CoV-2 cases in a German meat processing facility reported so far. Our results indicate climate conditions, fresh air exchange rates, and airflow as factors that can promote efficient spread of SARS-CoV-2 via long distances and provide insights into possible requirements for pandemic mitigation strategies in industrial workplace settings.
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      Kriegel, M.; Buchholz, U.; Gastmeier, P.; Bischoff, P.; Abdelgawad, I.; Hartmann, A. Predicted Infection Risk for Aerosol Transmission of SARS-CoV-2. medRxiv 2020,  DOI: 10.1101/2020.10.08.20209106 .
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      Stein-Zamir, C.; Abramson, N.; Shoob, H.; Libal, E.; Bitan, M.; Cardash, T.; Cayam, R.; Miskin, I. A Large COVID-19 Outbreak in a High School 10 Days after Schools’ Reopening, Israel, May 2020. Eurosurveillance 2020, 25, 1– 5,  DOI: 10.2807/1560-7917.ES.2020.25.29.2001352
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      A large COVID-19 outbreak in a high school 10 days after schools' reopening, Israel, May 2020
      Stein-Zamir, Chen; Abramson, Nitza; Shoob, Hanna; Libal, Erez; Bitan, Menachem; Cardash, Tanya; Cayam, Refael; Miskin, Ian
      Eurosurveillance (2020), 25 (29), 1-5CODEN: EUROGD; ISSN:1560-7917. (European Centre for Disease Prevention and Control)
      On 13 March 2020, Israel's government declared closure of all schools. Schools fully reopened on 17 May 2020. Ten days later, a major outbreak of COVID-19 occurred in a high school. The 1st case was registered on 26 May, the 2nd on 27 May. They were not epidemiol. linked. Testing of the complete school community revealed 153 students (attack rate: 13.2%) and 25 staff members (attack rate: 16.6%) who were COVID-19 pos.
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      Nardell, E. A.; Keegan, J.; Cheney, S. A.; Etkind, S. C. Airborne Infection: Theoretical Limits of Protection Achievable by Building Ventilation. Am. Rev. Respir. Dis. 1991, 144, 302– 306,  DOI: 10.1164/ajrccm/144.2.302
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      Airborne infection. Theoretical limits of protection achievable by building ventilation
      Nardell E A; Keegan J; Cheney S A; Etkind S C
      The American review of respiratory disease (1991), 144 (2), 302-6 ISSN:0003-0805.
      Of 67 office workers 27 (40%) had documented tuberculin skin test conversions after an estimated 4-wk exposure to a coworker with cavitary tuberculosis. Worker complaints for more than 2 yr before the tuberculosis exposure prompted investigations of air quality in the building before and after the tuberculosis exposure. Carbon dioxide concentrations in many parts of the building were found to be above recommended levels, indicating suboptimal ventilation with outdoor air. We applied a mathematical model of airborne transmission to the data to assess the role of building ventilation and other transmission factors. We estimated that ventilation with outside air averaged about 15 feet 3/min (cfm) per occupant, the low end of acceptable ventilation, corresponding to CO2 levels of about 1,000 ppm. The model predicted that at 25 cfm per person 18 workers would have been infected (a 33% reduction) and at 35 cfm, a level considered optimal for comfort, that 13 workers would have been infected (an additional 19% reduction). Further increases in outdoor air ventilation would be impractical and would have resulted in progressively smaller increments in protection. According to the model, the index case added approximately 13 infectious doses (quanta) per hour (qph) to the office air during the exposure period, 10 times the average infectiousness reported in a large series of tuberculosis cases. Further modeling predicted that as infectiousness rises, ventilation would offer progressively less protection. We conclude that outdoor air ventilation that is inadequate for comfort may contribute to airborne infection but that the protection afforded to building occupants by ventilation above comfort levels may be inherently limited, especially when the level of exposure to infection is high.
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      Gammaitoni, L.; Nucci, M. C. Using a Mathematical Model to Evaluate the Efficacy of TB Control Measures. Emerg. Infect. Dis. 1997, 3, 335– 342,  DOI: 10.3201/eid0303.970310
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      Using a mathematical model to evaluate the efficacy of TB control measures
      Gammaitoni L; Nucci M C
      Emerging infectious diseases (1997), 3 (3), 335-42 ISSN:1080-6040.
      We evaluated the efficacy of recommended tuberculosis (TB) infection control measures by using a deterministic mathematical model for airborne contagion. We examined the percentage of purified protein derivative conversions under various exposure conditions, environmental controlstrategies, and respiratory protective devices. We conclude that environmental control cannot eliminate the risk for TB transmission during high-risk procedures; respiratory protective devices, and particularly high-efficiency particulate air masks, may provide nearly complete protection if used with air filtration or ultraviolet irradiation. Nevertheless, the efficiency of these control measures decreases as the infectivity of the source case increases. Therefore, administrative control measures (e.g., indentifying and isolating patients with infectious TB) are the most effective because they substantially reduce the rate of infection.
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      Moser, M. R.; Bender, T. R.; Margolis, H. S.; Noble, G. R.; Kendal, A. P.; Ritter, D. G. An Outbreak of Influenza Aboard a Commercial Airliner. Am. J. Epidemiol. 1979, 110, 1– 6,  DOI: 10.1093/oxfordjournals.aje.a112781
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      An outbreak of influenza aboard a commercial airliner
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      American journal of epidemiology (1979), 110 (1), 1-6 ISSN:0002-9262.
      A jet airliner with 54 persons aboard was delayed on the ground for three hours because of engine failure during a takeoff attempt. Most passengers stayed on the airplane during the delay. Within 72 hours, 72 per cent of the passengers became ill with symptoms of cough, fever, fatigue, headache, sore throat and myalgia. One passenger, the apparent index case, was ill on the airplane, and the clinical attack rate among the others varied with the amount of time spent aboard. Virus antigenically similar to A/Texas/1/77(H3N2) was isolated from 8 of 31 passengers cultured, and 20 of 22 ill persons tested had serologic evidence of infection with this virus. The airplane ventilation system was inoperative during the delay and this may account for the high attack rate.
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      Remington, P. L.; Hall, W. N.; Davis, I. H.; Herald, A.; Gunn, R. A. Airborne Transmission of Measles in a Physician’s Office. JAMA 1985, 253, 1574– 1577,  DOI: 10.1001/jama.1985.03350350068022
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      Airborne transmission of measles in a physician's office
      Remington P L; Hall W N; Davis I H; Herald A; Gunn R A
      JAMA (1985), 253 (11), 1574-7 ISSN:0098-7484.
      An unusual outbreak of measles occurred in 1982 in a pediatrician's office in Muskegon, Mich. Three children, who had arrived at the office 60 to 75 minutes after a child with measles had departed, developed measles. Using a model based on airborne transmission, it is estimated that the index patient was producing 144 units of infection (quanta) per minute while in the office. Characteristics such as coughing, increased warm air recirculation, and low relative humidity may have increased the likelihood of transmission. Adequate immunization of all patients and staff, respiratory isolation and prompt care of all suspected cases, and adequate fresh-air ventilation should decrease the risk of airborne transmission of measles in this setting. Airborne transmission may occur more often than previously suspected, a possibility that should be considered when evaluating current measles control strategies.
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      Wilson, N. M.; Marks, G. B.; Eckhardt, A.; Clarke, A. M.; Young, F. P.; Garden, F. L.; Stewart, W.; Cook, T. M.; Tovey, E. R. The Effect of Respiratory Activity, Non-Invasive Respiratory Support and Facemasks on Aerosol Generation and Its Relevance to COVID-19. Anaesthesia 2021, 76, 1465,  DOI: 10.1111/anae.15475
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      The effect of respiratory activity, non-invasive respiratory support and facemasks on aerosol generation and its relevance to COVID-19
      Wilson, N. M.; Marks, G. B.; Eckhardt, A.; Clarke, A. M.; Young, F. P.; Garden, F. L.; Stewart, W.; Cook, T. M.; Tovey, E. R.
      Anaesthesia (2021), 76 (11), 1465-1474CODEN: ANASAB; ISSN:0003-2409. (Wiley-Blackwell)
      Respirable aerosols (< 5 μm in diam.) present a high risk of SARS-CoV-2 transmission. Guidelines recommend using aerosol precautions during aerosol-generating procedures, and droplet (> 5 μm) precautions at other times. However, emerging evidence indicates respiratory activities may be a more important source of aerosols than clin. procedures such as tracheal intubation. We aimed to measure the size, total no. and vol. of all human aerosols exhaled during respiratory activities and therapies. We used a novel chamber with an optical particle counter sampling at 100 l.min-1 to count and size-fractionate close to all exhaled particles (0.5-25 μm). We compared emissions from ten healthy subjects during six respiratory activities (quiet breathing; talking; shouting; forced expiratory manoeuvres; exercise; and coughing) with three respiratory therapies (high-flow nasal oxygen and single or dual circuit non-invasive pos. pressure ventilation). Activities were repeated while wearing facemasks. When compared with quiet breathing, exertional respiratory activities increased particle counts 34.6-fold during talking and 370.8-fold during coughing (p < 0.001). High-flow nasal oxygen 60 at l.min-1 increased particle counts 2.3-fold (p = 0.031) during quiet breathing. Single and dual circuit non-invasive respiratory therapy at 25/10 cm. H2O with quiet breathing increased counts by 2.6-fold and 7.8-fold, resp. (both p < 0.001). During exertional activities, respiratory therapies and facemasks reduced emissions compared with activities alone. Respiratory activities (including exertional breathing and coughing) which mimic respiratory patterns during illness generate substantially more aerosols than non-invasive respiratory therapies, which conversely can reduce total emissions. We argue the risk of aerosol exposure is underappreciated and warrants widespread, targeted interventions.
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      Milton, D. K.; Fabian, M. P.; Cowling, B. J.; Grantham, M. L.; McDevitt, J. J. Influenza Virus Aerosols in Human Exhaled Breath: Particle Size, Culturability, and Effect of Surgical Masks. PLoS Pathog. 2013, 9, e1003205  DOI: 10.1371/journal.ppat.1003205
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      Influenza virus aerosols in human exhaled breath: particle size, culturability, and effect of surgical masks
      Milton, Donald K.; Patricia Fabian, M.; Cowling, Benjamin J.; Grantham, Michael L.; McDevitt, James J.
      PLoS Pathogens (2013), 9 (3), e1003205CODEN: PPLACN; ISSN:1553-7374. (Public Library of Science)
      The CDC recommends that healthcare settings provide influenza patients with facemasks as a means of reducing transmission to staff and other patients, and a recent report suggested that surgical masks can capture influenza virus in large droplet spray. However, there is minimal data on influenza virus aerosol shedding, the infectiousness of exhaled aerosols, and none on the impact of facemasks on viral aerosol shedding from patients with seasonal influenza. We collected samples of exhaled particles (one with and one without a facemask) in two size fractions ("coarse">5 μm, "fine" ≤5 μm) from 37 volunteers within 5 days of seasonal influenza onset, measured viral copy no. using quant. RT-PCR, and tested the fine-particle fraction for culturable virus. Fine particles contained 8.8 (95% CI 4.1 to 19) fold more viral copies than did coarse particles. Surgical masks reduced viral copy nos. in the fine fraction by 2.8 fold (95% CI 1.5 to 5.2) and in the coarse fraction by 25 fold (95% CI 3.5 to 180). Overall, masks produced a 3.4 fold (95% CI 1.8 to 6.3) redn. in viral aerosol shedding. Correlations between nasopharyngeal swab and the aerosol fraction copy nos. were weak (r = 0.17, coarse; r = 0.29, fine fraction). Copy nos. in exhaled breath declined rapidly with day after onset of illness. Two subjects with the highest copy nos. gave culture pos. fine particle samples. Surgical masks worn by patients reduce aerosols shedding of virus. The abundance of viral copies in fine particle aerosols and evidence for their infectiousness suggests an important role in seasonal influenza transmission. Monitoring exhaled virus aerosols will be important for validation of exptl. transmission studies in humans.
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      Lindsley, W. G.; Noti, J. D.; Blachere, F. M.; Thewlis, R. E.; Martin, S. B.; Othumpangat, S.; Noorbakhsh, B.; Goldsmith, W. T.; Vishnu, A.; Palmer, J. E.; Clark, K. E.; Beezhold, D. H. Viable Influenza A Virus in Airborne Particles from Human Coughs. J. Occup. Environ. Hyg. 2015, 12, 107– 113,  DOI: 10.1080/15459624.2014.973113
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      Viable Influenza A Virus in Airborne Particles from Human Coughs
      Lindsley, William G.; Noti, John D.; Blachere, Francoise M.; Thewlis, Robert E.; Martin, Stephen B.; Othumpangat, Sreekumar; Noorbakhsh, Bahar; Goldsmith, William T.; Vishnu, Abhishek; Palmer, Jan E.; Clark, Karen E.; Beezhold, Donald H.
      Journal of Occupational and Environmental Hygiene (2015), 12 (2), 107-113CODEN: JOEHA2; ISSN:1545-9624. (Taylor & Francis, Inc.)
      Patients with influenza release aerosol particles contg. the virus into their environment. However, the importance of airborne transmission in the spread of influenza is unclear, in part because of a lack of information about the infectivity of the airborne virus. The purpose of this study was to det. the amt. of viable influenza A virus that was expelled by patients in aerosol particles while coughing. Sixty-four symptomatic adult volunteer outpatients were asked to cough 6 times into a cough aerosol collection system. Seventeen of these participants tested pos. for influenza A virus by viral plaque assay (VPA) with confirmation by viral replication assay (VRA). Viable influenza A virus was detected in the cough aerosol particles from 7 of these 17 test subjects (41%). Viable influenza A virus was found in the smallest particle size fraction (0.3 μm to 8 μm), with a mean of 142 plaque-forming units (SD 215) expelled during the 6 coughs in particles of this size. These results suggest that a significant proportion of patients with influenza A release small airborne particles contg. viable virus into the environment. Although the amts. of influenza A detected in cough aerosol particles during our expts. were relatively low, larger quantities could be expelled by influenza patients during a pandemic when illnesses would be more severe. Our findings support the idea that airborne infectious particles could play an important role in the spread of influenza.
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      Yan, J.; Grantham, M.; Pantelic, J.; Bueno de Mesquita, P. J.; Albert, B.; Liu, F.; Ehrman, S.; Milton, D. K.; EMIT Consortium Infectious Virus in Exhaled Breath of Symptomatic Seasonal Influenza Cases from a College Community. Proc. Natl. Acad. Sci. U. S. A. 2018, 115, 1081– 1086,  DOI: 10.1073/pnas.1716561115
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      Infectious virus in exhaled breath of symptomatic seasonal influenza cases from a college community
      Yan, Jing; Grantham, Michael; Pantelic, Jovan; Bueno de Mesquita, P. Jacob; Albert, Barbara; Liu, Fengjie; Ehrman, Sheryl; Milton, Donald K.
      Proceedings of the National Academy of Sciences of the United States of America (2018), 115 (5), 1081-1086CODEN: PNASA6; ISSN:0027-8424. (National Academy of Sciences)
      Little is known about the amt. and infectiousness of influenza virus shed into exhaled breath. This contributes to uncertainty about the importance of airborne influenza transmission. We screened 355 symptomatic volunteers with acute respiratory illness and report 142 cases with confirmed influenza infection who provided 218 paired nasopharyngeal (NP) and 30-min breath samples (coarse >5-μm and fine ≤5-μm fractions) on days 1-3 after symptom onset. We assessed viral RNA copy no. for all samples and cultured NP swabs and fine aerosols. We recovered infectious virus from 52 (39%) of the fine aerosols and 150 (89%) of the NP swabs with valid cultures. The geometric mean RNA copy nos. were 3.8 × 104/30-min fine-, 1.2 × 104/30-min coarse-aerosol sample, and 8.2 × 108 per NP swab. Fine- and coarse-aerosol viral RNA were pos. assocd. with body mass index and no. of coughs and neg. assocd. with increasing days since symptom onset in adjusted models. Fine-aerosol viral RNA was also pos. assocd. with having influenza vaccination for both the current and prior season. NP swab viral RNA was pos. assocd. with upper respiratory symptoms and neg. assocd. with age but was not significantly assocd. with fine- or coarse-aerosol viral RNA or their predictors. Sneezing was rare, and sneezing and coughing were not necessary for infectious aerosol generation. Our observations suggest that influenza infection in the upper and lower airways are compartmentalized and independent.
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      Tiemersma, E. W.; van der Werf, M. J.; Borgdorff, M. W.; Williams, B. G.; Nagelkerke, N. J. D. Natural History of Tuberculosis: Duration and Fatality of Untreated Pulmonary Tuberculosis in HIV Negative Patients: A Systematic Review. PLoS One 2011, 6, e17601  DOI: 10.1371/journal.pone.0017601
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      Natural history of tuberculosis: duration and fatality of untreated pulmonary tuberculosis in HIV negative patients: a systematic review
      Tiemersma, Edine W.; van der Werf, Marieke J.; Borgdorff, Martien W.; Williams, Brian G.; Nagelkerke, Nico J. D.
      PLoS One (2011), 6 (4), e17601CODEN: POLNCL; ISSN:1932-6203. (Public Library of Science)
      Background: The prognosis, specifically the case fatality and duration, of untreated tuberculosis is important as many patients are not correctly diagnosed and therefore receive inadequate or no treatment. Furthermore, duration and case fatality of tuberculosis are key parameters in interpreting epidemiol. data. Methodol. and Principal Findings: To est. the duration and case fatality of untreated pulmonary tuberculosis in HIV neg. patients we reviewed studies from the pre-chemotherapy era. Untreated smear-pos. tuberculosis among HIV neg. individuals has a 10-yr case fatality variously reported between 53% and 86%, with a weighted mean of 70%. Ten-year case fatality of culture-pos. smear-neg. tuberculosis was nowhere reported directly but can be indirectly estd. to be approx. 20%. The duration of tuberculosis from onset to cure or death is approx. 3 years and appears to be similar for smear-pos. and smear-neg. tuberculosis. Conclusions: Current models of untreated tuberculosis that assume a total duration of 2 years until self-cure or death underestimate the duration of disease by about one year, but their case fatality ests. of 70% for smear-pos. and 20% for culture-pos. smear-neg. tuberculosis appear to be satisfactory.
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      Bueno de Mesquita, P. J.; Noakes, C. J.; Milton, D. K. Quantitative Aerobiologic Analysis of an Influenza Human Challenge-transmission Trial. Indoor Air 2020, 30, 1189– 1198,  DOI: 10.1111/ina.12701
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      Quantitative aerobiologic analysis of an influenza human challenge-transmission trial
      Bueno de Mesquita, Paul Jacob; Noakes, Catherine J.; Milton, Donald K.
      Indoor Air (2020), 30 (6), 1189-1198CODEN: INAIE5; ISSN:1600-0668. (Wiley-Blackwell)
      Despite evidence that airborne transmission contributes to influenza epidemics, limited knowledge of the infectiousness of human influenza cases hinders pandemic preparedness. We used airborne viral source strength and indoor CO2 monitoring from the largest human influenza challenge-transmission trial (EMIT: Evaluating Modes of Influenza Transmission, ClinicalTrials.gov no. NCT01710111) to compute an airborne infectious dose generation rate q = 0.11 (95% CI 0.088, 0.12)/h and calc. the quantity of airborne virus per infectious dose σ = 1.4E + 5 RNA copies/quantum (95% CI 9.9E + 4, 1.8E + 5). We then compared these calcd. values to available data on influenza airborne infectious dose from several previous studies, and applied the values to dormitory room environments to predict probability of transmission between roommates. Transmission risk from typical, moderately to severely symptomatic influenza cases is dramatically decreased by exposure redn. via increasing indoor air ventilation. The minority of cases who shed the most virus (ie, supershedders) may pose great risk even in well-ventilated spaces. Our modeling method and estd. infectiousness provide a ground work for (a) epidemiol. studies of transmission in non-exptl. settings and (b) evaluation of the extent to which airborne exposure control strategies could limit transmission risk.
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      Mikszewski, A.; Stabile, L.; Buonanno, G.; Morawska, L. The Airborne Contagiousness of Respiratory Viruses: A Comparative Analysis and Implications for Mitigation. Geosci. Front. 2021, 101285,  DOI: 10.1016/j.gsf.2021.101285
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      Conly, J.; Seto, W. H.; Pittet, D.; Holmes, A.; Chu, M.; Hunter, P. R.; on behalf of the WHO Infection Prevention and Control Research and Development Expert Group for COVID-19; Conly, J.; Cookson, B.; Pittet, D.; Holmes, A.; Chu, M.; Voss, A.; Levin, A. S. S.; Seto, W. H.; Kalisvar, M.; Fisher, D.; Gobat, N.; Hunter, P. R.; Sobsey, M.; Schwaber, M. J.; Tomczyk, S.; Ling, M. L. Use of Medical Face Masks versus Particulate Respirators as a Component of Personal Protective Equipment for Health Care Workers in the Context of the COVID-19 Pandemic. Antimicrob. Resist. Infect. Control 2020, 9, 126,  DOI: 10.1186/s13756-020-00779-6
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      Use of medical face masks versus particulate respirators as a component of personal protective equipment for health care workers in the context of the COVID-19 pandemic
      Conly John; Seto W H; Pittet Didier; Holmes Alison; Chu May; Hunter Paul R
      Antimicrobial resistance and infection control (2020), 9 (1), 126 ISSN:.
      Currently available evidence supports that the predominant route of human-to-human transmission of the SARS-CoV-2 is through respiratory droplets and/or contact routes. The report by the World Health Organization (WHO) Joint Mission on Coronavirus Disease 2019 (COVID-19) in China supports person-to-person droplet and fomite transmission during close unprotected contact with the vast majority of the investigated infection clusters occurring within families, with a household secondary attack rate varying between 3 and 10%, a finding that is not consistent with airborne transmission. The reproduction number (R0) for the SARS-CoV-2 is estimated to be between 2.2-2.7, compatible with other respiratory viruses associated with a droplet/contact mode of transmission and very different than an airborne virus like measles with a R0 widely cited to be between 12 and 18. Based on the scientific evidence accumulated to date, our view is that SARS-CoV-2 is not spread by the airborne route to any significant extent and the use of particulate respirators offers no advantage over medical masks as a component of personal protective equipment for the routine care of patients with COVID-19 in the health care setting. Moreover, prolonged use of particulate respirators may result in unintended harms. In conjunction with appropriate hand hygiene, personal protective equipment (PPE) used by health care workers caring for patients with COVID-19 must be used with attention to detail and precision of execution to prevent lapses in adherence and active failures in the donning and doffing of the PPE.
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      Klompas, M.; Baker, M. A.; Rhee, C. Airborne Transmission of SARS-CoV-2: Theoretical Considerations and Available Evidence. JAMA 2020, 324, 441– 442,  DOI: 10.1001/jama.2020.12458
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      Airborne transmission of SARS-CoV-2
      Klompas, Michael; Baker, Meghan A.; Rhee, Chanu
      JAMA, the Journal of the American Medical Association (2020), 324 (5), 441-442CODEN: JAMAAP; ISSN:1538-3598. (American Medical Association)
      This article describes about the airborne transmission of SARS-CoV-2.
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      Tang, J. W.; Bahnfleth, W. P.; Bluyssen, P. M.; Buonanno, G.; Jimenez, J. L.; Kurnitski, J.; Li, Y.; Miller, S.; Sekhar, C.; Morawska, L.; Marr, L. C.; Melikov, A. K.; Nazaroff, W. W.; Nielsen, P. V.; Tellier, R.; Wargocki, P.; Dancer, S. J. Dismantling Myths on the Airborne Transmission of Severe Acute Respiratory Syndrome Coronavirus-2 (SARS-CoV-2). J. Hosp. Infect. 2021, 110, 89– 96,  DOI: 10.1016/j.jhin.2020.12.022
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      Dismantling myths on the airborne transmission of severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2)
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      The Journal of hospital infection (2021), 110 (), 89-96 ISSN:.
      The coronavirus disease 2019 (COVID-19) pandemic has caused untold disruption throughout the world. Understanding the mechanisms for transmission of severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) is key to preventing further spread, but there is confusion over the meaning of 'airborne' whenever transmission is discussed. Scientific ambivalence originates from evidence published many years ago which has generated mythological beliefs that obscure current thinking. This article collates and explores some of the most commonly held dogmas on airborne transmission in order to stimulate revision of the science in the light of current evidence. Six 'myths' are presented, explained and ultimately refuted on the basis of recently published papers and expert opinion from previous work related to similar viruses. There is little doubt that SARS-CoV-2 is transmitted via a range of airborne particle sizes subject to all the usual ventilation parameters and human behaviour. Experts from specialties encompassing aerosol studies, ventilation, engineering, physics, virology and clinical medicine have joined together to produce this review to consolidate the evidence for airborne transmission mechanisms, and offer justification for modern strategies for prevention and control of COVID-19 in health care and the community.
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      Chan, W. R.; Li, X.; Singer, B. C.; Pistochini, T.; Vernon, D.; Outcault, S.; Sanguinetti, A.; Modera, M. Ventilation Rates in California Classrooms: Why Many Recent HVAC Retrofits Are Not Delivering Sufficient Ventilation. Build. Environ. 2020, 167, 106426  DOI: 10.1016/j.buildenv.2019.106426
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      Rudnick, S. N.; Milton, D. K. Risk of Indoor Airborne Infection Transmission Estimated from Carbon Dioxide Concentration. Indoor Air 2003, 13, 237– 245,  DOI: 10.1034/j.1600-0668.2003.00189.x
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      Risk of indoor airborne infection transmission estimated from carbon dioxide concentration
      Rudnick, S. N.; Milton, D. K.
      Indoor Air (2003), 13 (3), 237-245CODEN: INAIE5; ISSN:0905-6947. (Blackwell Publishing Ltd.)
      The Wells-Riley equation, used to model the risk of indoor airborne transmission of infectious diseases such as tuberculosis, is sometimes problematic because it assumes steady-state conditions and requires measurement of outdoor air supply rates, which are frequently difficult to measure and often vary over time. An alternative equation was derived which avoids these problems by detg. the fraction of inhaled air which was exhaled previously by someone in the building (re-breathed fraction) using CO2 concn. as a marker for exhaled-breath exposure. A non-steady state version of the Wells-Riley equation was also derived which is esp. useful in poorly ventilated environments when outdoor air supply rates are assumed const. A relationship between av. no. of secondary cases infected by each primary case in a building and exposure to exhaled breath was derived, demonstrating there is likely an achievable crit. re-breathed fraction of indoor air below which airborne propagation of common respiratory infections and influenza will not occur.
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    • Derivation of the factor accounting for the deviation from the steady state, details of Monte Carlo uncertainty propagation for the fitting of attack rates vs Hr, evaluation of the fitting in Figure 1b, rE and rB for different vocalization and physical intensity levels, details of the conditions for Table 2, details of the setting in Figure 2, and screenshot of the COVID-19 Aerosol Transmission Estimator (PDF)


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