Significance

There is still much to be understood about the factors influencing the ecology and epidemiology of COVID-19. In particular, whether environmental variation is likely to drive seasonal changes in SARS-CoV-2 transmission dynamics is largely unknown. We investigate the effects of the environment on SARS-CoV-2 transmission rates across the United States and then incorporate the most important environmental parameters into an epidemiological model. We show that temperature and population density can be important factors in transmission but only in the absence of mobility-restricting policy measures, although particularly strong policy measures may be required to mitigate the highest population densities. Our findings improve our understanding of the drivers of COVID-19 transmission and highlight areas in which policy decisions can be proactive.

Abstract

As COVID-19 continues to spread across the world, it is increasingly important to understand the factors that influence its transmission. Seasonal variation driven by responses to changing environment has been shown to affect the transmission intensity of several coronaviruses. However, the impact of the environment on severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) remains largely unknown, and thus seasonal variation remains a source of uncertainty in forecasts of SARS-CoV-2 transmission. Here we address this issue by assessing the association of temperature, humidity, ultraviolet radiation, and population density with estimates of transmission rate (R). Using data from the United States, we explore correlates of transmission across US states using comparative regression and integrative epidemiological modeling. We find that policy intervention (“lockdown”) and reductions in individuals’ mobility are the major predictors of SARS-CoV-2 transmission rates, but, in their absence, lower temperatures and higher population densities are correlated with increased SARS-CoV-2 transmission. Our results show that summer weather cannot be considered a substitute for mitigation policies, but that lower autumn and winter temperatures may lead to an increase in transmission intensity in the absence of policy interventions or behavioral changes. We outline how this information may improve the forecasting of COVID-19, reveal its future seasonal dynamics, and inform intervention policies.

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Data Availability

No new data are released as part of this paper, all external datasets used are publicly available, described in Materials and Methods and referenced. Outputs from our Bayesian model runs are available on Figshare (https://doi.org/10.6084/m9.figshare.14696841.v1) and code to reproduce our analyses are available on Zenodo (https://doi.org/10.5281/zenodo.4884696). Code to download and combine external datasets and reproduce our full analysis pipeline is also available in our team’s GitHub repository (https://www.github.com/pearselab/tyrell).

Acknowledgments

This work was funded by Natural Environment Research Council Grant NE/V009710/1 and by the Imperial College COVID-19 Research Fund. W.D.P. and the W.D.P. laboratory are also funded by NSF Grants ABI-1759965 and EF-1802605.

Supporting Information

Appendix (PDF)

References

1
P. Zhou et al., A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature 579, 270–273 (2020).
2
Y. Liu, A. A. Gayle, A. Wilder-Smith, J. Rocklöv, The reproductive number of COVID-19 is higher compared to SARS coronavirus. J. Trav. Med. 27, taaa021 (2020).
3
M. Mesel-Lemoine et al., A human coronavirus responsible for the common cold massively kills dendritic cells but not monocytes. J. Virol. 86, 7577–7587 (2012).
4
A. J. Smit et al., Winter is coming: A Southern Hemisphere perspective of the environmental drivers of SARS-CoV-2 and the potential seasonality of COVID-19. Int. J. Environ. Res. Publ. Health 17, 5634 (2020).
5
M. Xie, Q. Chen, Insight into 2019 novel coronavirus — An updated interim review and lessons from SARS-CoV and MERS-CoV. Int. J. Infect. Dis. 94, 119–124 (2020).
6
A. C. Lowen, S. Mubareka, J. Steel, P. Palese, Influenza virus transmission is dependent on relative humidity and temperature. PLoS Pathog. 3, 1470–1476 (2007).
7
A. C. Lowen, J. Steel, Roles of humidity and temperature in shaping influenza seasonality. J. Virol. 88, 7692–7695 (2014).
8
J. Tan et al., An initial investigation of the association between the SARS outbreak and weather: With the view of the environmental temperature and its variation. J. Epidemiol. Community Health 59, 186–192 (2005).
9
K. H. Chan et al., The effects of temperature and relative humidity on the viability of the SARS coronavirus. Adv. Virol. 2011, 734690 (2011).
10
N. van Doremalen, T. Bushmaker, V. J. Munster, Stability of middle east respiratory syndrome coronavirus (MERS-CoV) under different environmental conditions. Euro Surveill. 18, 20590 (2013).
11
D. Schoeman, B. C. Fielding, Coronavirus envelope protein: Current knowledge. Virol. J. 16, 69 (2019).
12
C. J. Carlson, J. D. Chipperfield, B. M. Benito, R. J. Telford, R. B. O’Hara, Species distribution models are inappropriate for COVID-19. Nat. Ecol. Evol. 4, 770–771 (2020).
13
C. J. Carlson, A. C. R. Gomez, S. Bansal, S. J. Ryan, Misconceptions about weather and seasonality must not misguide COVID-19 response. Nat. Commun. 11, 4312 (2020).
14
H. M. Korevaar et al., Quantifying the impact of US state non-pharmaceutical interventions on COVID-19 transmission. medRxiv [Preprint] (2020). https://doi.org/10.1101/2020.06.30.20142877 (Accessed 10 August 2020).
15
J. Rocklöv, H. Sjödin, High population densities catalyze the spread of COVID-19. J. Trav. Med. 27, taaa038 (2020).
16
N. Afshordi, B. Holder, M. Bahrami, D. Lichtblau, Diverse local epidemics reveal the distinct effects of population density, demographics, climate, depletion of susceptibles, and intervention in the first wave of COVID-19 in the United States. medRxiv [Preprint] (2020). https://doi.org/10.1101/2020.06.30.20143636 (Accessed 8 February 2021).
17
M. B. Araujo, B. Naimi, Spread of SARS-CoV-2 Coronavirus likely to be constrained by climate. medRxiv {preprint] (2020). https://doi.org/10.1101/2020.03.12.20034728 (Accessed 7 April 2020).
18
R. E. Baker, W. Yang, G. A. Vecchi, C. J. E. Metcalf, B. T. Grenfell, Susceptible supply limits the role of climate in the early SARS-CoV-2 pandemic. Science 369, 315–319 (2020).
19
Q. Bukhari, Y. Jameel, Will coronavirus pandemic diminish by summer? SSRN [Preprint] (2020). https://doi.org/10.2139/ssrn.3556998 (Accessed 10 April 2020).
20
B. Chen et al., Roles of meteorological conditions in COVID-19 transmission on a worldwide scale. medRxiv [Preprint] (2020). https://doi.org/10.1101/2020.03.16.20037168 (Accessed 8 July 2020).
21
W. Luo et al., The role of absolute humidity on transmission rates of the COVID-19 outbreak. medRxiv [Preprint] (2020). https://doi.org/10.1101/2020.02.12.20022467 (Accessed 10 April 2020).
22
Y. Ma et al., Effects of temperature variation and humidity on the death of COVID-19 in Wuhan, China. Sci. Total Environ. 724, 138226 (2020).
23
C. Merow, M. C. Urban, Seasonality and uncertainty in global COVID-19 growth rates. Proc. Natl. Acad. Sci. U.S.A. 117, 27456–27464 (2020).
24
M. M. Sajadi et al., Temperature, humidity, and latitude analysis to estimate potential spread and seasonality of coronavirus disease 2019 (COVID-19). JAMA Netw. Open 3, e2011834 (2020).
25
Y. Yao et al., No association of COVID-19 transmission with temperature or UV radiation in Chinese cities. Eur. Respir. J. 55, 2000517 (2020).
26
D. S. Candido et al., Evolution and epidemic spread of SARS-Cov-2 in Brazil. Science 369, 1255–1260 (2020).
27
R. Laxminarayan et al., Epidemiology and transmission dynamics of COVID-19 in two Indian states. Science 370, 691–697 (2020).
28
M. Aghaali, G. Kolifarhood, R. Nikbakht, H. M. Saadati, S. S. H. Nazari, Estimation of the serial interval and basic reproduction number of COVID-19 in Qom, Iran, and three other countries: A data-driven analysis in the early phase of the outbreak. Transbound. Emerg. Dis. 67, 2860–2868 (2020).
29
National Research Council, “Linkages between climate, ecosystems, and infectious disease” in Under the Weather: Climate, Ecosystems, and Infectious Disease, National Research Council, Ed. (National Academies Press, 2001), pp. 20–44.
30
S. M. Kissler, C. Tedijanto, E. Goldstein, Y. H. Grad, M. Lipsitch, Projecting the transmission dynamics of SARS-CoV-2 through the postpandemic period. Science 368, 860–868 (2020).
31
P. G. T. Walker et al., “The global impact of COVID-19 and strategies for mitigation and suppression” (Report 12, Imperial College COVID-19 Response Team, 2020).
32
J. Wang et al., Impact of temperature and relative humidity on the transmission of COVID-19: A modeling study in China and the United States. BMJ Open, 11, e043863 (2021).
33
J. D. Chipperfield, B. M. Benito, R. B. O’Hara, R. J. Telford, C. J. Carlson, On the inadequacy of species distribution models for modelling the spread of SARS-CoV-2: Response to Araújo and Naimi. EcoEvoRxiv [Preprint] (2020). https://doi.org/10.32942/osf.io/mr6pn (Accessed 7 April 2020).
34
S. Flaxman et al., Estimating the effects of non-pharmaceutical interventions on COVID-19 in Europe. Nature 584, 257–261 (2020).
35
T. A. Mellan et al., “Estimating COVID-19 cases and reproduction number in Brazil” (Technical Rep. 21, Imperial College COVID-19 Response Team, 2020).
36
M. A. C. Vollmer et al., Report 20: Using mobility to estimate the transmission intensity of COVID-19 in Italy: A subnational analysis with future scenarios. medRxiv [Preprint] (2020). https://doi.org/10.1101/2020.05.05.20089359 (Accessed 10 September 2020).
37
H. J. T. Unwin et al., State-level tracking of COVID-19 in the United States. Nat. Commun. 11, 6189 (2020).
38
Google LLC, Google COVID-19 community mobility reports. https://www.google.com/covid19/mobility/. Accessed 20 December 2020.
39
D. H. Morris et al., The effect of temperature and humidity on the stability of SARS-CoV-2 and other enveloped viruses. bioRxiv [Preprint] (2020). https://doi.org/10.1101/2020.10.16.341883 (Accessed 23 October 2020).
40
J. Shaman, V. E. Pitzer, C. Viboud, B. T. Grenfell, M. Lipsitch, Absolute humidity and the seasonal onset of influenza in the continental United States. PLoS Biol. 8, e1000316 (2010).
41
H. Qian, T. Miao, L. Liu, X. Zheng, D. Luo, Y. Li, Indoor transmission of SARS-CoV-2. Indoor Air 31, 639–645 (2020).
42
J. L. Nguyen, J. Schwartz, D. W. Dockery, The relationship between indoor and outdoor temperature, apparent temperature, relative humidity, and absolute humidity. Indoor Air 24, 103–112 (2014).
43
A. B. Asumadu-Sakyi et al., The relationship between indoor and outdoor temperature in warm and cool seasons in houses in Brisbane, Australia. Energy Build. 191, 127–142 (2019).
44
M. G. Just, L. M. Nichols, R. R. Dunn, Human indoor climate preferences approximate specific geographies. R. Soc. Open Sci. 6, 180695 (2019).
45
C. Poirier et al., The role of environmental factors on transmission rates of the COVID-19 outbreak: An initial assessment in two spatial scales. Sci. Rep. 10, 17002 (2020).
46
E. Javan, S. J. Fox, L. A. Meyers, Probability of current COVID-19 outbreaks in all US counties. medRxiv [Preprint] (2020). https://doi.org/10.1101/2020.04.06.20053561 (Accessed 23 June 2020).
47
G. Neofotistos, E. Kaxiras, Modeling the Covid-19 pandemic response of the US states. medRxiv [Preprint] (2020). https://doi.org/10.1101/2020.06.24.20138982 (Accessed 12 August 2020).
48
C. I. Jarvis et al., Quantifying the impact of physical distance measures on the transmission of COVID-19 in the UK. BMC Med. 18, 124 (2020).
49
H. Lau et al., The positive impact of lockdown in Wuhan on containing the COVID-19 outbreak in China. J. Trav. Med. 27, 1–7 (2020).
50
K. Prem, A. R. Cook, M. Jit, Projecting social contact mactrices in 152 countries using contact surveys and demographic data. PLoS Comput. Biol. 13, e1005697 (2017).
51
R Core Team, R: A Language and Environment for Statistical Computing, version 3.6.3. https://www.r-project.org/. Accessed 29 February 2020.
52
Center for International Earth Science Information Network, Gridded population of the world, version 4 (GPWv4): Population density, revision 11. https://doi.org/10.7927/H49C6VHW. Accessed 10 July 2020.
53
Copernicus Climate Change Service, Essential climate variables for assessment of climate variability from 1979 to present. https://cds.climate.copernicus.eu/cdsapp#!/dataset/ecv-for-climate-change. Accessed 5 October 2020.
54
J. Shaman, M. Kohn, Absolute humidity modulates influenza survival, transmission, and seasonality. Proc. Natl. Acad. Sci. U.S.A. 106, 3243–3248 (2009).
55
U. Schulzweida, Data from “CDO user guide, version 1.9.8”. https://doi.org/10.5281/zenodo.3539275. Accessed 27 August 2020.
56
Global Administrative Areas, GADM database of global administrative areas, version 3.6. https://www.gadm.org. Accessed 30 September 2020.
57
R. Verity et al., Estimates of the severity of coronavirus disease 2019: A model-based analysis. Lancet Infect. Dis. 20, 669–677 (2020).
58
Stan Development Team, RStan: The R interface to Stan, version 2.21.2. mc-stan.org/. Accessed 27 July 2020.

Information & Authors

Information

Published in

The cover image for PNAS Vol.118; No.25
Proceedings of the National Academy of Sciences
Vol. 118 | No. 25
June 22, 2021
PubMed: 34103391

Classifications

Data Availability

No new data are released as part of this paper, all external datasets used are publicly available, described in Materials and Methods and referenced. Outputs from our Bayesian model runs are available on Figshare (https://doi.org/10.6084/m9.figshare.14696841.v1) and code to reproduce our analyses are available on Zenodo (https://doi.org/10.5281/zenodo.4884696). Code to download and combine external datasets and reproduce our full analysis pipeline is also available in our team’s GitHub repository (https://www.github.com/pearselab/tyrell).

Submission history

Published online: June 8, 2021
Published in issue: June 22, 2021

Keywords

  1. SARS-CoV-2
  2. transmission
  3. climate
  4. seasonality
  5. epidemiology

Acknowledgments

This work was funded by Natural Environment Research Council Grant NE/V009710/1 and by the Imperial College COVID-19 Research Fund. W.D.P. and the W.D.P. laboratory are also funded by NSF Grants ABI-1759965 and EF-1802605.

Notes

This article is a PNAS Direct Submission.

Authors

Affiliations

Department of Life Sciences, Imperial College London, Ascot SL5 7PY, United Kingdom;
Department of Mathematics, Imperial College London, London SW7 2AZ, United Kingdom;
Amanda S. Gallinat2
Department of Biology, Utah State University, Logan, UT 84322;
Ecology Center, Utah State University, Logan, UT 84322;
Department of Biology, Utah State University, Logan, UT 84322;
Ecology Center, Utah State University, Logan, UT 84322;
Department of Biology, Utah State University, Logan, UT 84322;
Ecology Center, Utah State University, Logan, UT 84322;
MRC Centre for Global Infectious Disease Analysis, Imperial College London, London W2 1PG, United Kingdom
MRC Centre for Global Infectious Disease Analysis, Imperial College London, London W2 1PG, United Kingdom
MRC Centre for Global Infectious Disease Analysis, Imperial College London, London W2 1PG, United Kingdom
Lorenzo Cattarino3
MRC Centre for Global Infectious Disease Analysis, Imperial College London, London W2 1PG, United Kingdom
MRC Centre for Global Infectious Disease Analysis, Imperial College London, London W2 1PG, United Kingdom
Department of Life Sciences, Imperial College London, Ascot SL5 7PY, United Kingdom;
William D. Pearse1 [email protected]
Department of Life Sciences, Imperial College London, Ascot SL5 7PY, United Kingdom;
Department of Biology, Utah State University, Logan, UT 84322;
Ecology Center, Utah State University, Logan, UT 84322;

Notes

1
To whom correspondence may be addressed. Email: [email protected] or [email protected].
Author contributions: T.P.S., L.C., I.D., M.T., and W.D.P. designed research; T.P.S., A.S.G., S.P.K., M.S., H.J.T.U., and W.D.P. performed research; T.P.S., S.F., H.J.T.U., O.J.W., C.W., L.C., I.D., M.T., and W.D.P. analyzed data; and T.P.S., S.F., A.S.G., S.P.K., M.S., H.J.T.U., O.J.W., C.W., L.C., I.D., M.T., and W.D.P. wrote the paper.
2
S.F., A.S.G., S.P.K., M.S., H.J.T.U., O.J.W., and C.W. contributed equally to this work.
3
L.C., I.D., and M.T. contributed equally to this work.

Competing Interests

The authors declare no competing interest.

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    Temperature and population density influence SARS-CoV-2 transmission in the absence of nonpharmaceutical interventions
    Proceedings of the National Academy of Sciences
    • Vol. 118
    • No. 25

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