Mechanistic theory predicts the effects of temperature and humidity on inactivation of SARS-CoV-2 and other enveloped viruses

  1. Dylan H Morris  Is a corresponding author
  2. Kwe Claude Yinda
  3. Amandine Gamble
  4. Fernando W Rossine
  5. Qishen Huang
  6. Trenton Bushmaker
  7. Robert J Fischer
  8. M Jeremiah Matson
  9. Neeltje Van Doremalen
  10. Peter J Vikesland
  11. Linsey C Marr
  12. Vincent J Munster
  13. James O Lloyd-Smith  Is a corresponding author
  1. Princeton University, United States
  2. National Institute of Allergy and Infectious Diseases, United States
  3. University of California, Los Angeles, United States
  4. Virginia Tech, United States

Abstract

Ambient temperature and humidity strongly affect inactivation rates of enveloped viruses, but a mechanistic, quantitative theory of these effects has been elusive. We measure the stability of SARS-CoV-2 on an inert surface at nine temperature and humidity conditions and develop a mechanistic model to explain and predict how temperature and humidity alter virus inactivation. We find SARS-CoV-2 survives longest at low temperatures and extreme relative humidities (RH); median estimated virus half-life is >24 hours at 10C and 40% RH, but ~1.5 hours at 27C and 65% RH. Our mechanistic model uses fundamental chemistry to explain why inactivation rate increases with increased temperature and shows a U-shaped dependence on RH. The model accurately predicts existing measurements of five different human coronaviruses, suggesting that shared mechanisms may affect stability for many viruses. The results indicate scenarios of high transmission risk, point to mitigation strategies, and advance the mechanistic study of virus transmission.

Data availability

All code and data needed to reproduce results and figures is archived on Github (https://github.com/dylanhmorris/sars-cov-2-temp-humidity/) and on Zenodo (https://doi.org/10.5281/zenodo.4093264), and licensed for reuse, with appropriate attribution/citation, under a BSD 3-Clause Revised License. This includes all original data generated in the experiments and all data collected and used for meta-analysis.

Article and author information

Author details

  1. Dylan H Morris

    Ecology and Evolutionary Biology, Princeton University, Princeton, United States
    For correspondence
    dhmorris@princeton.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3655-406X
  2. Kwe Claude Yinda

    Virus Ecology Unit, National Institute of Allergy and Infectious Diseases, Hamilton, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Amandine Gamble

    Ecology and Evolutionary Biology, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Fernando W Rossine

    Ecology and Evolutionary Biology, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Qishen Huang

    Civil and Environmental Engineering, Virginia Tech, Blacksburg, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Trenton Bushmaker

    Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, Hamilton, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Robert J Fischer

    Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, Hamilton, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. M Jeremiah Matson

    Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, Hamilton, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Neeltje Van Doremalen

    Laboratory of Virology, National Institute of Allergy and Infectious Diseases, Hamilton, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4368-6359
  10. Peter J Vikesland

    Civil and Environmental Engineering, Virginia Tech, Blacksburg, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Linsey C Marr

    Civil and Environmental Engineering, Virginia Tech, Blacksburg, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. Vincent J Munster

    Laboratory of Virology, National Institute of Allergy and Infectious Diseases, Hamilton, United States
    Competing interests
    The authors declare that no competing interests exist.
  13. James O Lloyd-Smith

    Department of Ecology and Evolutionary Biology, University of California, Los Angeles, Los Angeles, United States
    For correspondence
    jlloydsmith@ucla.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7941-502X

Funding

National Science Foundation (CCF 1917819)

  • Dylan H Morris

Defense Advanced Research Projects Agency (D18AC00031)

  • Amandine Gamble
  • James O Lloyd-Smith

UCLA AIDS Institute and Charity Treks

  • Amandine Gamble
  • James O Lloyd-Smith

National Institute of Allergy and Infectious Diseases (Intramural Research Program)

  • Kwe Claude Yinda
  • Trenton Bushmaker
  • Robert J Fischer
  • M Jeremiah Matson
  • Neeltje Van Doremalen
  • Vincent J Munster

National Science Foundation (DEB-1557022)

  • James O Lloyd-Smith

Strategic Environmental Research and Development Program (RC‐2635)

  • James O Lloyd-Smith

National Science Foundation (CBET-1705653)

  • Qishen Huang
  • Peter J Vikesland
  • Linsey C Marr

National Science Foundation (CBET-2029911)

  • Qishen Huang
  • Peter J Vikesland
  • Linsey C Marr

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. C. Brandon Ogbunugafor, Yale University, United States

Publication history

  1. Received: December 18, 2020
  2. Accepted: February 20, 2021
  3. Accepted Manuscript published: April 27, 2021 (version 1)
  4. Version of Record published: July 13, 2021 (version 2)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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  1. Dylan H Morris
  2. Kwe Claude Yinda
  3. Amandine Gamble
  4. Fernando W Rossine
  5. Qishen Huang
  6. Trenton Bushmaker
  7. Robert J Fischer
  8. M Jeremiah Matson
  9. Neeltje Van Doremalen
  10. Peter J Vikesland
  11. Linsey C Marr
  12. Vincent J Munster
  13. James O Lloyd-Smith
(2021)
Mechanistic theory predicts the effects of temperature and humidity on inactivation of SARS-CoV-2 and other enveloped viruses
eLife 10:e65902.
https://doi.org/10.7554/eLife.65902
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