Dispersal patterns and influence of air travel during the global expansion of SARS-CoV-2 variants of concern

Houriiyah Tegally; Eduan Wilkinson; Joseph L-H Tsui; Monika Moir; Darren Martin; Anderson Fernandes Brito; Marta Giovanetti; Kamran Khan; Carmen Huber; Isaac I Bogoch; James Emmanuel San; Jenicca Poongavanan; Joicymara S Xavier; Darlan da S Candido; Filipe Romero; Cheryl Baxter; Oliver G Pybus; Richard J Lessells; Nuno R Faria; Moritz U G Kraemer; Tulio de Oliveira

doi:10.1016/j.cell.2023.06.001

Dispersal patterns and influence of air travel during the global expansion of SARS-CoV-2 variants of concern

Cell. 2023 Jul 20;186(15):3277-3290.e16. doi: 10.1016/j.cell.2023.06.001. Epub 2023 Jun 7.

Authors

Houriiyah Tegally¹, Eduan Wilkinson², Joseph L-H Tsui³, Monika Moir², Darren Martin⁴, Anderson Fernandes Brito⁵, Marta Giovanetti⁶, Kamran Khan⁷, Carmen Huber⁸, Isaac I Bogoch⁹, James Emmanuel San¹⁰, Jenicca Poongavanan², Joicymara S Xavier¹¹, Darlan da S Candido¹², Filipe Romero¹², Cheryl Baxter², Oliver G Pybus¹³, Richard J Lessells¹⁰, Nuno R Faria¹⁴, Moritz U G Kraemer¹⁵, Tulio de Oliveira¹⁶

Affiliations

¹ Centre for Epidemic Response and Innovation (CERI), School of Data Science and Computational Thinking, Stellenbosch University, Stellenbosch, South Africa; KwaZulu-Natal Research Innovation and Sequencing Platform (KRISP), Nelson R. Mandela School of Medicine, University of KwaZulu-Natal, Durban, South Africa. Electronic address: houriiyah.tegally@gmail.com.
² Centre for Epidemic Response and Innovation (CERI), School of Data Science and Computational Thinking, Stellenbosch University, Stellenbosch, South Africa.
³ Department of Biology, University of Oxford, Oxford, UK.
⁴ Wellcome Centre for Infectious Diseases Research in Africa (CIDRI-Africa), Cape Town, South Africa; Institute of Infectious Disease and Molecular Medicine, University of Cape Town, Cape Town, South Africa.
⁵ Instituto Todos pela Saúde, São Paulo, São Paulo, Brazil.
⁶ Laboratorio de Flavivirus, Fundacao Oswaldo Cruz, Rio de Janeiro, Brazil; Laboratório de Genética Celular e Molecular, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil; Department of Science and Technology for Humans and the Environment, University of Campus Bio-Medico di Roma, Rome, Italy.
⁷ BlueDot, Toronto, ON, Canada; Department of Medicine, Division of Infectious Diseases, University of Toronto, Toronto, ON, Canada.
⁸ BlueDot, Toronto, ON, Canada.
⁹ Department of Medicine, Division of Infectious Diseases, University of Toronto, Toronto, ON, Canada.
¹⁰ KwaZulu-Natal Research Innovation and Sequencing Platform (KRISP), Nelson R. Mandela School of Medicine, University of KwaZulu-Natal, Durban, South Africa.
¹¹ Centre for Epidemic Response and Innovation (CERI), School of Data Science and Computational Thinking, Stellenbosch University, Stellenbosch, South Africa; Universidade Federal de Minas Gerais, Belo Horizonte, Brazil; Institute of Agricultural Sciences, Universidade Federal dos Vales do Jequitinhonha e Mucuri, Unaí, Brazil.
¹² MRC Centre for Global Infectious Disease Analysis and Department of Infectious Disease Epidemiology, Jameel Institute, School of Public Health, Imperial College London, London, UK.
¹³ Department of Biology, University of Oxford, Oxford, UK; Pandemic Sciences Institute, University of Oxford, Oxford, UK; Department of Pathobiology and Population Sciences, Royal Veterinary College London, London, UK.
¹⁴ Department of Biology, University of Oxford, Oxford, UK; MRC Centre for Global Infectious Disease Analysis and Department of Infectious Disease Epidemiology, Jameel Institute, School of Public Health, Imperial College London, London, UK; Departamento de Moléstias Infecciosas e Parasitárias e Instituto de Medicina Tropical da Faculdade de Medicina, Universidade de São Paulo, São Paulo, Brazil.
¹⁵ Department of Biology, University of Oxford, Oxford, UK; Pandemic Sciences Institute, University of Oxford, Oxford, UK. Electronic address: moritz.kraemer@biology.ox.ac.uk.
¹⁶ Centre for Epidemic Response and Innovation (CERI), School of Data Science and Computational Thinking, Stellenbosch University, Stellenbosch, South Africa; KwaZulu-Natal Research Innovation and Sequencing Platform (KRISP), Nelson R. Mandela School of Medicine, University of KwaZulu-Natal, Durban, South Africa; Department of Global Health, University of Washington, Seattle, WA, USA. Electronic address: tulio@sun.ac.za.

Abstract

The Alpha, Beta, and Gamma SARS-CoV-2 variants of concern (VOCs) co-circulated globally during 2020 and 2021, fueling waves of infections. They were displaced by Delta during a third wave worldwide in 2021, which, in turn, was displaced by Omicron in late 2021. In this study, we use phylogenetic and phylogeographic methods to reconstruct the dispersal patterns of VOCs worldwide. We find that source-sink dynamics varied substantially by VOC and identify countries that acted as global and regional hubs of dissemination. We demonstrate the declining role of presumed origin countries of VOCs in their global dispersal, estimating that India contributed <15% of Delta exports and South Africa <1%-2% of Omicron dispersal. We estimate that >80 countries had received introductions of Omicron within 100 days of its emergence, associated with accelerated passenger air travel and higher transmissibility. Our study highlights the rapid dispersal of highly transmissible variants, with implications for genomic surveillance along the hierarchical airline network.

Keywords: SARS-CoV-2; genomics; global dispersal; mobility; phylogenetics; phylogeography; travel; variants.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Air Travel*
COVID-19*
Humans
Phylogeny
SARS-CoV-2

Supplementary concepts

SARS-CoV-2 variants

Abstract

Publication types

MeSH terms

Supplementary concepts

Grants and funding