Airborne transmission of respiratory viruses

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Abstract

Mechanisms of airborne transmission

The COVID-19 pandemic has highlighted controversies and unknowns about how respiratory pathogens spread between hosts. Traditionally, it was thought that respiratory pathogens spread between people through large droplets produced in coughs and through contact with contaminated surfaces (fomites). However, several respiratory pathogens are known to spread through small respiratory aerosols, which can float and travel in air flows, infecting people who inhale them at short and long distances from the infected person. Wang et al. review recent advances in understanding airborne transmission gained from studying the spread of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infections and other respiratory pathogens. The authors suggest that airborne transmission may be the dominant form of transmission for several respiratory pathogens, including SARS-CoV-2, and that further understanding of the mechanisms underlying infection from the airborne route will better inform mitigation measures. —GKA

Abstract

A Review discusses the scientific basis of and factors controlling airborne transmission of respiratory viruses including coronavirus.

Abstract

BACKGROUND

Exposure to droplets produced in the coughs and sneezes of infected individuals or contact with droplet-contaminated surfaces (fomites) have been widely perceived as the dominant transmission modes for respiratory pathogens. Airborne transmission is traditionally defined as involving the inhalation of infectious aerosols or “droplet nuclei” smaller than 5 μm and mainly at a distance of >1 to 2 m away from the infected individual, and such transmission has been thought to be relevant only for “unusual” diseases. However, there is robust evidence supporting the airborne transmission of many respiratory viruses, including severe acute respiratory syndrome coronavirus (SARS-CoV), Middle East respiratory syndrome (MERS)–CoV, influenza virus, human rhinovirus, and respiratory syncytial virus (RSV). The limitations of traditional views of droplet, fomite, and airborne transmission were illuminated during the COVID-19 pandemic. Droplet and fomite transmission of SARS-CoV-2 alone cannot account for the numerous superspreading events and differences in transmission between indoor and outdoor environments observed during the COVID-19 pandemic. Controversy surrounding how COVID-19 is transmitted and what interventions are needed to control the pandemic has revealed a critical need to better understand the airborne transmission pathway of respiratory viruses, which will allow for better-informed strategies to mitigate the transmission of respiratory infections.

ADVANCES

Respiratory droplets and aerosols can be generated by various expiratory activities. Advances in aerosol measurement techniques, such as aerodynamic and scanning mobility particle sizing, have shown that the majority of exhaled aerosols are smaller than 5 μm, and a large fraction are <1 μm for most respiratory activities, including those produced during breathing, talking, and coughing. Exhaled aerosols occur in multiple size modes that are associated with different generation sites and production mechanisms in the respiratory tract. Although 5 μm has been used historically to distinguish aerosols from droplets, the size distinction between aerosols and droplets should be 100 μm, which represents the largest particle size that can remain suspended in still air for more than 5 s from a height of 1.5 m, typically reach a distance of 1 to 2 m from the emitter (depending on the velocity of airflow carrying the aerosols), and can be inhaled. Aerosols produced by an infected individual may contain infectious viruses, and studies have shown that viruses are enriched in small aerosols (<5 μm). The transport of virus-laden aerosols is affected by the physicochemical properties of aerosols themselves and environmental factors, including temperature, relative humidity, ultraviolet radiation, airflow, and ventilation. Once inhaled, virus-laden aerosols can deposit in different parts of the respiratory tract. Larger aerosols tend to be deposited in the upper airway; however, smaller aerosols, although they can also be deposited there, can penetrate deep into the alveolar region of the lungs. The strong effect of ventilation on transmission, the distinct difference between indoor and outdoor transmission, well-documented long-range transmission, the observed transmission of SARS-CoV-2 despite the use of masks and eye protection, the high frequency of indoor superspreading events of SARS-CoV-2, animal experiments, and airflow simulations provide strong and unequivocal evidence for airborne transmission. Fomite transmission of SARS-CoV-2 has been found to be far less efficient, and droplets are only dominant when individuals are within 0.2 m of each other when talking. Although both aerosols and droplets can be produced by infected individuals during expiratory activities, droplets fall quickly to the ground or surfaces within seconds, leaving an enrichment of aerosols over droplets. The airborne pathway likely contributes to the spread of other respiratory viruses whose transmission was previously characterized as droplet driven. The World Health Organization (WHO) and the US Centers for Disease Control and Prevention (CDC) have officially acknowledged the inhalation of virus-laden aerosols as a main transmission mode in spreading COVID-19 at both short and long ranges in 2021.

OUTLOOK

Airborne transmission of pathogens has been vastly underappreciated, mostly because of an insufficient understanding about the airborne behavior of aerosols and at least partially because of the misattribution of anecdotal observations. Given the lack of evidence for droplet and fomite transmission and the increasingly strong evidence for aerosols in transmitting numerous respiratory viruses, we must acknowledge that airborne transmission is much more prevalent than previously recognized. Given all that we have learned about SARS-CoV-2 infection, the aerosol transmission pathway needs to be reevaluated for all respiratory infectious diseases. Additional precautionary measures must be implemented for mitigating aerosol transmission at both short and long ranges, with particular attention to ventilation, airflows, air filtration, UV disinfection, and mask fit. These interventions are critical tools for ending the current pandemic and preventing future outbreaks.

Phases involved in airborne transmission of respiratory viruses.

Virus-laden aerosols (<100 I1/4m) are first generated by an infected individual through expiratory activities, through which they are exhaled and transported in the environment. They may be inhaled by a potential host to initiate a new infection, provided that they remain infectious. In contrast to droplets (>100 I1/4m), aerosols can linger in air for hours and travel beyond 1 to 2 m from the infected individual who exhales them, causing new infections at both short and long ranges.

CREDIT: N. CARY/ SCIENCE

Abstract

The COVID-19 pandemic has revealed critical knowledge gaps in our understanding of and a need to update the traditional view of transmission pathways for respiratory viruses. The long-standing definitions of droplet and airborne transmission do not account for the mechanisms by which virus-laden respiratory droplets and aerosols travel through the air and lead to infection. In this Review, we discuss current evidence regarding the transmission of respiratory viruses by aerosols—how they are generated, transported, and deposited, as well as the factors affecting the relative contributions of droplet-spray deposition versus aerosol inhalation as modes of transmission. Improved understanding of aerosol transmission brought about by studies of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection requires a reevaluation of the major transmission pathways for other respiratory viruses, which will allow better-informed controls to reduce airborne transmission.

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Aerosol and Surface Stability of SARS-CoV-2 as Compared with SARS-CoV-1

Neeltje van Doremalen, Trenton Bushmaker, Dylan H Morris … (2021)

To the Editor: A novel human coronavirus that is now named severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) (formerly called HCoV-19) emerged in Wuhan, China, in late 2019 and is now causing a pandemic. 1 We analyzed the aerosol and surface stability of SARS-CoV-2 and compared it with SARS-CoV-1, the most closely related human coronavirus. 2 We evaluated the stability of SARS-CoV-2 and SARS-CoV-1 in aerosols and on various surfaces and estimated their decay rates using a Bayesian regression model (see the Methods section in the Supplementary Appendix, available with the full text of this letter at NEJM.org). SARS-CoV-2 nCoV-WA1-2020 (MN985325.1) and SARS-CoV-1 Tor2 (AY274119.3) were the strains used. Aerosols (<5 μm) containing SARS-CoV-2 (105.25 50% tissue-culture infectious dose [TCID50] per milliliter) or SARS-CoV-1 (106.75-7.00 TCID50 per milliliter) were generated with the use of a three-jet Collison nebulizer and fed into a Goldberg drum to create an aerosolized environment. The inoculum resulted in cycle-threshold values between 20 and 22, similar to those observed in samples obtained from the upper and lower respiratory tract in humans. Our data consisted of 10 experimental conditions involving two viruses (SARS-CoV-2 and SARS-CoV-1) in five environmental conditions (aerosols, plastic, stainless steel, copper, and cardboard). All experimental measurements are reported as means across three replicates. SARS-CoV-2 remained viable in aerosols throughout the duration of our experiment (3 hours), with a reduction in infectious titer from 103.5 to 102.7 TCID50 per liter of air. This reduction was similar to that observed with SARS-CoV-1, from 104.3 to 103.5 TCID50 per milliliter (Figure 1A). SARS-CoV-2 was more stable on plastic and stainless steel than on copper and cardboard, and viable virus was detected up to 72 hours after application to these surfaces (Figure 1A), although the virus titer was greatly reduced (from 103.7 to 100.6 TCID50 per milliliter of medium after 72 hours on plastic and from 103.7 to 100.6 TCID50 per milliliter after 48 hours on stainless steel). The stability kinetics of SARS-CoV-1 were similar (from 103.4 to 100.7 TCID50 per milliliter after 72 hours on plastic and from 103.6 to 100.6 TCID50 per milliliter after 48 hours on stainless steel). On copper, no viable SARS-CoV-2 was measured after 4 hours and no viable SARS-CoV-1 was measured after 8 hours. On cardboard, no viable SARS-CoV-2 was measured after 24 hours and no viable SARS-CoV-1 was measured after 8 hours (Figure 1A). Both viruses had an exponential decay in virus titer across all experimental conditions, as indicated by a linear decrease in the log10TCID50 per liter of air or milliliter of medium over time (Figure 1B). The half-lives of SARS-CoV-2 and SARS-CoV-1 were similar in aerosols, with median estimates of approximately 1.1 to 1.2 hours and 95% credible intervals of 0.64 to 2.64 for SARS-CoV-2 and 0.78 to 2.43 for SARS-CoV-1 (Figure 1C, and Table S1 in the Supplementary Appendix). The half-lives of the two viruses were also similar on copper. On cardboard, the half-life of SARS-CoV-2 was longer than that of SARS-CoV-1. The longest viability of both viruses was on stainless steel and plastic; the estimated median half-life of SARS-CoV-2 was approximately 5.6 hours on stainless steel and 6.8 hours on plastic (Figure 1C). Estimated differences in the half-lives of the two viruses were small except for those on cardboard (Figure 1C). Individual replicate data were noticeably “noisier” (i.e., there was more variation in the experiment, resulting in a larger standard error) for cardboard than for other surfaces (Fig. S1 through S5), so we advise caution in interpreting this result. We found that the stability of SARS-CoV-2 was similar to that of SARS-CoV-1 under the experimental circumstances tested. This indicates that differences in the epidemiologic characteristics of these viruses probably arise from other factors, including high viral loads in the upper respiratory tract and the potential for persons infected with SARS-CoV-2 to shed and transmit the virus while asymptomatic. 3,4 Our results indicate that aerosol and fomite transmission of SARS-CoV-2 is plausible, since the virus can remain viable and infectious in aerosols for hours and on surfaces up to days (depending on the inoculum shed). These findings echo those with SARS-CoV-1, in which these forms of transmission were associated with nosocomial spread and super-spreading events, 5 and they provide information for pandemic mitigation efforts.

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SARS-CoV-2 Viral Load in Upper Respiratory Specimens of Infected Patients

Lirong Zou, Feng Ruan, Mingxing Huang … (2020)

To the Editor: The 2019 novel coronavirus (SARS-CoV-2) epidemic, which was first reported in December 2019 in Wuhan, China, and has been declared a public health emergency of international concern by the World Health Organization, may progress to a pandemic associated with substantial morbidity and mortality. SARS-CoV-2 is genetically related to SARS-CoV, which caused a global epidemic with 8096 confirmed cases in more than 25 countries in 2002–2003. 1 The epidemic of SARS-CoV was successfully contained through public health interventions, including case detection and isolation. Transmission of SARS-CoV occurred mainly after days of illness 2 and was associated with modest viral loads in the respiratory tract early in the illness, with viral loads peaking approximately 10 days after symptom onset. 3 We monitored SARS-CoV-2 viral loads in upper respiratory specimens obtained from 18 patients (9 men and 9 women; median age, 59 years; range, 26 to 76) in Zhuhai, Guangdong, China, including 4 patients with secondary infections (1 of whom never had symptoms) within two family clusters (Table S1 in the Supplementary Appendix, available with the full text of this letter at NEJM.org). The patient who never had symptoms was a close contact of a patient with a known case and was therefore monitored. A total of 72 nasal swabs (sampled from the mid-turbinate and nasopharynx) (Figure 1A) and 72 throat swabs (Figure 1B) were analyzed, with 1 to 9 sequential samples obtained from each patient. Polyester flock swabs were used for all the patients. From January 7 through January 26, 2020, a total of 14 patients who had recently returned from Wuhan and had fever (≥37.3°C) received a diagnosis of Covid-19 (the illness caused by SARS-CoV-2) by means of reverse-transcriptase–polymerase-chain-reaction assay with primers and probes targeting the N and Orf1b genes of SARS-CoV-2; the assay was developed by the Chinese Center for Disease Control and Prevention. Samples were tested at the Guangdong Provincial Center for Disease Control and Prevention. Thirteen of 14 patients with imported cases had evidence of pneumonia on computed tomography (CT). None of them had visited the Huanan Seafood Wholesale Market in Wuhan within 14 days before symptom onset. Patients E, I, and P required admission to intensive care units, whereas the others had mild-to-moderate illness. Secondary infections were detected in close contacts of Patients E, I, and P. Patient E worked in Wuhan and visited his wife (Patient L), mother (Patient D), and a friend (Patient Z) in Zhuhai on January 17. Symptoms developed in Patients L and D on January 20 and January 22, respectively, with viral RNA detected in their nasal and throat swabs soon after symptom onset. Patient Z reported no clinical symptoms, but his nasal swabs (cycle threshold [Ct] values, 22 to 28) and throat swabs (Ct values, 30 to 32) tested positive on days 7, 10, and 11 after contact. A CT scan of Patient Z that was obtained on February 6 was unremarkable. Patients I and P lived in Wuhan and visited their daughter (Patient H) in Zhuhai on January 11 when their symptoms first developed. Fever developed in Patient H on January 17, with viral RNA detected in nasal and throat swabs on day 1 after symptom onset. We analyzed the viral load in nasal and throat swabs obtained from the 17 symptomatic patients in relation to day of onset of any symptoms (Figure 1C). Higher viral loads (inversely related to Ct value) were detected soon after symptom onset, with higher viral loads detected in the nose than in the throat. Our analysis suggests that the viral nucleic acid shedding pattern of patients infected with SARS-CoV-2 resembles that of patients with influenza 4 and appears different from that seen in patients infected with SARS-CoV. 3 The viral load that was detected in the asymptomatic patient was similar to that in the symptomatic patients, which suggests the transmission potential of asymptomatic or minimally symptomatic patients. These findings are in concordance with reports that transmission may occur early in the course of infection 5 and suggest that case detection and isolation may require strategies different from those required for the control of SARS-CoV. How SARS-CoV-2 viral load correlates with culturable virus needs to be determined. Identification of patients with few or no symptoms and with modest levels of detectable viral RNA in the oropharynx for at least 5 days suggests that we need better data to determine transmission dynamics and inform our screening practices.

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Temporal dynamics in viral shedding and transmissibility of COVID-19

Xi. He, Eric Lau, Peng Wu … (2020)

We report temporal patterns of viral shedding in 94 patients with laboratory-confirmed COVID-19 and modeled COVID-19 infectiousness profiles from a separate sample of 77 infector-infectee transmission pairs. We observed the highest viral load in throat swabs at the time of symptom onset, and inferred that infectiousness peaked on or before symptom onset. We estimated that 44% (95% confidence interval, 25-69%) of secondary cases were infected during the index cases' presymptomatic stage, in settings with substantial household clustering, active case finding and quarantine outside the home. Disease control measures should be adjusted to account for probable substantial presymptomatic transmission.

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Author and article information

Contributors

Chia C. Wang:

ORCID: https://orcid.org/0000-0003-3214-9937

Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: Project administrationRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Kimberly A. Prather:

ORCID: https://orcid.org/0000-0003-3048-9890

Role: ConceptualizationRole: MethodologyRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Josué Sznitman:

ORCID: https://orcid.org/0000-0001-8217-3842

Role: ConceptualizationRole: Writing - original draftRole: Writing - review & editing

Jose L. Jimenez:

ORCID: https://orcid.org/0000-0001-6203-1847

Role: ConceptualizationRole: InvestigationRole: Writing - review & editing

Seema S. Lakdawala:

ORCID: https://orcid.org/0000-0002-7679-2150

Role: ConceptualizationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Zeynep Tufekci:

ORCID: https://orcid.org/0000-0002-7806-0025

Role: ConceptualizationRole: Writing - review & editing

Linsey C. Marr:

ORCID: https://orcid.org/0000-0003-3628-6891

Role: ConceptualizationRole: InvestigationRole: Writing - review & editing

Journal

Journal ID (nlm-ta): Science

Journal ID (iso-abbrev): Science

Journal ID (publisher-id): science

Journal ID (hwp): science

Title: Science (New York, N.y.)

Publisher: American Association for the Advancement of Science

ISSN (Print): 0036-8075

ISSN (Electronic): 1095-9203

Publication date (Electronic, pub): 27 August 2021

Publication date PMC-release: 27 August 2021

Volume: 373

Issue: 6558

Electronic Location Identifier: eabd9149

Affiliations

[1 ]Aerosol Science Research Center, National Sun Yat-sen University, Kaohsiung, Taiwan 804, Republic of China.

[2 ]Department of Chemistry, National Sun Yat-sen University, Kaohsiung, Taiwan 804, Republic of China.

[3 ]Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA 92037, USA.

[4 ]Department of Biomedical Engineering, Israel Institute of Technology, Haifa 32000, Israel.

[5 ]Department of Chemistry and CIRES, University of Colorado, Boulder, CO 80309, USA.

[6 ]Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15219, USA.

[7 ]School of Information and Department of Sociology, University of North Carolina, Chapel Hill, NC 27599, USA.

[8 ]Department of Civil and Environmental Engineering, Virginia Tech, Blacksburg, VA 24061, USA.

Author notes

[* ]Corresponding author. Email: chiawang@ 123456mail.nsysu.edu.tw (C.C.W.); kprather@ 123456ucsd.edu (K.A.P.)

Author information

Chia C. Wang https://orcid.org/0000-0003-3214-9937

Kimberly A. Prather https://orcid.org/0000-0003-3048-9890

Josué Sznitman https://orcid.org/0000-0001-8217-3842

Jose L. Jimenez https://orcid.org/0000-0001-6203-1847

Seema S. Lakdawala https://orcid.org/0000-0002-7679-2150

Zeynep Tufekci https://orcid.org/0000-0002-7806-0025

Linsey C. Marr https://orcid.org/0000-0003-3628-6891

Article

Publisher ID: abd9149

DOI: 10.1126/science.abd9149

PMC ID: 8721651

PubMed ID: 34446582

SO-VID: e968d51b-ca0c-49d8-a62f-de65e112c985

Copyright © Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution License 4.0 (CC BY).

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This is an open-access article distributed under the terms of the Creative Commons Attribution license, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100008982, National Science Foundation;

Award ID: AGS-1822664

Funded by: FundRef http://dx.doi.org/10.13039/501100008982, National Science Foundation;

Award ID: ECCS 1542100

Funded by: FundRef http://dx.doi.org/10.13039/501100008982, National Science Foundation;

Award ID: ECCS 2025151

Funded by: National Institute of Allergy and Infectious Diseases Center of Excellence in Influenza Research and Surveillance;

Award ID: HHSN272201400007C

Funded by: Ministry of Science and Technology, Taiwan, R.O.C.;

Award ID: MOST 109-2113-M-110-011

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Airborne transmission of respiratory viruses

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Abstract

Mechanisms of airborne transmission

Abstract

Abstract

BACKGROUND

ADVANCES

OUTLOOK

Abstract

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Novel Coronavirus Disease COVID-19

Most cited references 204

Aerosol and Surface Stability of SARS-CoV-2 as Compared with SARS-CoV-1

SARS-CoV-2 Viral Load in Upper Respiratory Specimens of Infected Patients

Temporal dynamics in viral shedding and transmissibility of COVID-19

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