The dynamics of SARS-CoV-2 infectivity with changes in aerosol microenvironment

Jonathan P Reid; Henry P Oswin; Allen E Haddrell; Mara Otero Fernandez; Jiang-han Tian; Tom Hilditch; Dan A Hardy; Jamie F S Mann; Tristan A Cogan; Darryl J Hill; Adam Finn; Andrew D Davidson

doi:10.1073/pnas.2200109119

The dynamics of SARS-CoV-2 infectivity with changes in aerosol microenvironment

Jonathan P Reid^*
, Henry P Oswin
, Allen E Haddrell^*
, Mara Otero Fernandez
, Jiang-han Tian
, Tom Hilditch
, Dan A Hardy
, Jamie F S Mann
, Tristan A Cogan
, Darryl J Hill
, Adam Finn
, Andrew D Davidson^*

^*Corresponding author for this work

Research output: Contribution to journal › Article (Academic Journal) › peer-review

158 Citations (Scopus)

246 Downloads (Pure)

Abstract

Understanding the factors that influence the airborne survival of viruses such as severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in aerosols is important for identifying routes of transmission and the value of various mitigation strategies for preventing transmission. We present measurements of the stability of SARS-CoV-2 in aerosol droplets (∼5 to 10 µm equilibrated radius) over timescales spanning 5 s to 20 min using an instrument to probe survival in a small population of droplets (typically 5 to 10) containing ∼1 virus/droplet. Measurements of airborne infectivity change are coupled with a detailed physicochemical analysis of the airborne droplets containing the virus. A decrease in infectivity to ∼10% of the starting value was observable for SARS-CoV-2 over 20 min, with a large proportion of the loss occurring within the first 5 min after aerosolization. The initial rate of infectivity loss was found to correlate with physical transformation of the equilibrating droplet; salts within the droplets crystallize at relative humidities (RHs) below 50%, leading to a near-instant loss of infectivity in 50 to 60% of the virus. However, at 90% RH, the droplet remains homogenous and aqueous, and the viral stability is sustained for the first 2 min, beyond which it decays to only 10% remaining infectious after 10 min. The loss of infectivity at high RH is consistent with an elevation in the pH of the droplets, caused by volatilization of CO2 from bicarbonate buffer within the droplet. Four different variants of SARS-CoV-2 were compared and found to have a similar degree of airborne stability at both high and low RH.

Original language	English
Article number	e2200109119
Number of pages	11
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	119
Issue number	27
Early online date	28 Jun 2022
DOIs	https://doi.org/10.1073/pnas.2200109119
Publication status	Published - 5 Jul 2022

Bibliographical note

Funding Information:
ACKNOWLEDGMENTS. This work was funded by the National Institute for Health Research-UK Research and Innovation (UKRI) rapid COVID-19 call, the Elizabeth Blackwell Institute for Health Research, the University of Bristol, and the Medical Research Council. Additionally, this work was supported by funding from the PROTECT COVID-19 National Core Study on transmission and environment, managed by the Health and Safety Executive on behalf of Her Majesty’s Government. A.E.H. and M.O.-F. received funding from the Biotechnology and Biological Sciences Research Council, Project BB/T011688/1. A.D.D. is a member of the G2P-UK National Virology consortium funded by the Medical Research Council/UKRI (Grant MR/W005611/1) that supplied SARS-CoV-2 variants. H.P.O. is supported by funding from the Defence Science and Technology Laboratory and the Engineering and Physical Sciences Research Council. We also thank Robert Alexander for his contributions to discussions on aerosol pH.

Publisher Copyright:
Copyright © 2022 the Author(s).

Research Groups and Themes

Physical & Theoretical

Keywords

Aerosolized Particles and Droplets/chemistry
COVID-19/transmission
Humans
Humidity
Hydrogen-Ion Concentration
SARS-CoV-2/isolation & purification

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8084 - MRC CiC - Reid -EBI
Reid, J. P. (Principal Investigator)
1/06/20 → 28/02/21
Project: Research
A Transformative Technology Platform for Interrogating Airborne Adaptation of Respiratory Pathogens
Reid, J. P. (Principal Investigator)
1/05/20 → 31/07/21
Project: Research

The investigation of the dynamics of exhaled respiratory aerosols
Tian, J.-H. (Author), Reid, J. (Supervisor), 1 Oct 2024
Student thesis: Doctoral Thesis › Doctor of Philosophy (PhD)

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Reid, J. P., Oswin, H. P., Haddrell, A. E., Otero Fernandez, M., Tian, J., Hilditch, T., Hardy, D. A., Mann, J. F. S., Cogan, T. A., Hill, D. J., Finn, A., & Davidson, A. D. (2022). The dynamics of SARS-CoV-2 infectivity with changes in aerosol microenvironment. Proceedings of the National Academy of Sciences of the United States of America, 119(27), Article e2200109119. https://doi.org/10.1073/pnas.2200109119

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title = "The dynamics of SARS-CoV-2 infectivity with changes in aerosol microenvironment",

abstract = "Understanding the factors that influence the airborne survival of viruses such as severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in aerosols is important for identifying routes of transmission and the value of various mitigation strategies for preventing transmission. We present measurements of the stability of SARS-CoV-2 in aerosol droplets (∼5 to 10 µm equilibrated radius) over timescales spanning 5 s to 20 min using an instrument to probe survival in a small population of droplets (typically 5 to 10) containing ∼1 virus/droplet. Measurements of airborne infectivity change are coupled with a detailed physicochemical analysis of the airborne droplets containing the virus. A decrease in infectivity to ∼10\% of the starting value was observable for SARS-CoV-2 over 20 min, with a large proportion of the loss occurring within the first 5 min after aerosolization. The initial rate of infectivity loss was found to correlate with physical transformation of the equilibrating droplet; salts within the droplets crystallize at relative humidities (RHs) below 50\%, leading to a near-instant loss of infectivity in 50 to 60\% of the virus. However, at 90\% RH, the droplet remains homogenous and aqueous, and the viral stability is sustained for the first 2 min, beyond which it decays to only 10\% remaining infectious after 10 min. The loss of infectivity at high RH is consistent with an elevation in the pH of the droplets, caused by volatilization of CO2 from bicarbonate buffer within the droplet. Four different variants of SARS-CoV-2 were compared and found to have a similar degree of airborne stability at both high and low RH.",

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note = "Funding Information: ACKNOWLEDGMENTS. This work was funded by the National Institute for Health Research-UK Research and Innovation (UKRI) rapid COVID-19 call, the Elizabeth Blackwell Institute for Health Research, the University of Bristol, and the Medical Research Council. Additionally, this work was supported by funding from the PROTECT COVID-19 National Core Study on transmission and environment, managed by the Health and Safety Executive on behalf of Her Majesty{\textquoteright}s Government. A.E.H. and M.O.-F. received funding from the Biotechnology and Biological Sciences Research Council, Project BB/T011688/1. A.D.D. is a member of the G2P-UK National Virology consortium funded by the Medical Research Council/UKRI (Grant MR/W005611/1) that supplied SARS-CoV-2 variants. H.P.O. is supported by funding from the Defence Science and Technology Laboratory and the Engineering and Physical Sciences Research Council. We also thank Robert Alexander for his contributions to discussions on aerosol pH. Publisher Copyright: Copyright {\textcopyright} 2022 the Author(s).",

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Reid, JP , Oswin, HP , Haddrell, AE, Otero Fernandez, M, Tian, J, Hilditch, T, Hardy, DA, Mann, JFS , Cogan, TA , Hill, DJ , Finn, A & Davidson, AD 2022, 'The dynamics of SARS-CoV-2 infectivity with changes in aerosol microenvironment', Proceedings of the National Academy of Sciences of the United States of America, vol. 119, no. 27, e2200109119. https://doi.org/10.1073/pnas.2200109119

TY - JOUR

T1 - The dynamics of SARS-CoV-2 infectivity with changes in aerosol microenvironment

AU - Reid, Jonathan P

AU - Oswin, Henry P

AU - Haddrell, Allen E

AU - Otero Fernandez, Mara

AU - Tian, Jiang-han

AU - Hilditch, Tom

AU - Hardy, Dan A

AU - Mann, Jamie F S

AU - Cogan, Tristan A

AU - Hill, Darryl J

AU - Finn, Adam

AU - Davidson, Andrew D

N1 - Funding Information: ACKNOWLEDGMENTS. This work was funded by the National Institute for Health Research-UK Research and Innovation (UKRI) rapid COVID-19 call, the Elizabeth Blackwell Institute for Health Research, the University of Bristol, and the Medical Research Council. Additionally, this work was supported by funding from the PROTECT COVID-19 National Core Study on transmission and environment, managed by the Health and Safety Executive on behalf of Her Majesty’s Government. A.E.H. and M.O.-F. received funding from the Biotechnology and Biological Sciences Research Council, Project BB/T011688/1. A.D.D. is a member of the G2P-UK National Virology consortium funded by the Medical Research Council/UKRI (Grant MR/W005611/1) that supplied SARS-CoV-2 variants. H.P.O. is supported by funding from the Defence Science and Technology Laboratory and the Engineering and Physical Sciences Research Council. We also thank Robert Alexander for his contributions to discussions on aerosol pH. Publisher Copyright: Copyright © 2022 the Author(s).

PY - 2022/7/5

Y1 - 2022/7/5

N2 - Understanding the factors that influence the airborne survival of viruses such as severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in aerosols is important for identifying routes of transmission and the value of various mitigation strategies for preventing transmission. We present measurements of the stability of SARS-CoV-2 in aerosol droplets (∼5 to 10 µm equilibrated radius) over timescales spanning 5 s to 20 min using an instrument to probe survival in a small population of droplets (typically 5 to 10) containing ∼1 virus/droplet. Measurements of airborne infectivity change are coupled with a detailed physicochemical analysis of the airborne droplets containing the virus. A decrease in infectivity to ∼10% of the starting value was observable for SARS-CoV-2 over 20 min, with a large proportion of the loss occurring within the first 5 min after aerosolization. The initial rate of infectivity loss was found to correlate with physical transformation of the equilibrating droplet; salts within the droplets crystallize at relative humidities (RHs) below 50%, leading to a near-instant loss of infectivity in 50 to 60% of the virus. However, at 90% RH, the droplet remains homogenous and aqueous, and the viral stability is sustained for the first 2 min, beyond which it decays to only 10% remaining infectious after 10 min. The loss of infectivity at high RH is consistent with an elevation in the pH of the droplets, caused by volatilization of CO2 from bicarbonate buffer within the droplet. Four different variants of SARS-CoV-2 were compared and found to have a similar degree of airborne stability at both high and low RH.

AB - Understanding the factors that influence the airborne survival of viruses such as severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in aerosols is important for identifying routes of transmission and the value of various mitigation strategies for preventing transmission. We present measurements of the stability of SARS-CoV-2 in aerosol droplets (∼5 to 10 µm equilibrated radius) over timescales spanning 5 s to 20 min using an instrument to probe survival in a small population of droplets (typically 5 to 10) containing ∼1 virus/droplet. Measurements of airborne infectivity change are coupled with a detailed physicochemical analysis of the airborne droplets containing the virus. A decrease in infectivity to ∼10% of the starting value was observable for SARS-CoV-2 over 20 min, with a large proportion of the loss occurring within the first 5 min after aerosolization. The initial rate of infectivity loss was found to correlate with physical transformation of the equilibrating droplet; salts within the droplets crystallize at relative humidities (RHs) below 50%, leading to a near-instant loss of infectivity in 50 to 60% of the virus. However, at 90% RH, the droplet remains homogenous and aqueous, and the viral stability is sustained for the first 2 min, beyond which it decays to only 10% remaining infectious after 10 min. The loss of infectivity at high RH is consistent with an elevation in the pH of the droplets, caused by volatilization of CO2 from bicarbonate buffer within the droplet. Four different variants of SARS-CoV-2 were compared and found to have a similar degree of airborne stability at both high and low RH.

KW - Aerosolized Particles and Droplets/chemistry

KW - COVID-19/transmission

KW - Humans

KW - Humidity

KW - Hydrogen-Ion Concentration

KW - SARS-CoV-2/isolation & purification

U2 - 10.1073/pnas.2200109119

DO - 10.1073/pnas.2200109119

M3 - Article (Academic Journal)

C2 - 35763573

SN - 0027-8424

VL - 119

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 27

M1 - e2200109119

ER -

The dynamics of SARS-CoV-2 infectivity with changes in aerosol microenvironment

Abstract

Bibliographical note

Research Groups and Themes

Keywords

Access to Document

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Projects

8084 - MRC CiC - Reid -EBI

A Transformative Technology Platform for Interrogating Airborne Adaptation of Respiratory Pathogens

Student theses

The investigation of the dynamics of exhaled respiratory aerosols

Cite this