Genomic surveillance reveals dynamic shifts in the connectivity of COVID-19 epidemics

Nathaniel L Matteson; Gabriel W Hassler; Ezra Kurzban; Madison A Schwab; Sarah A Perkins; Karthik Gangavarapu; Joshua I Levy; Edyth Parker; David Pride; Abbas Hakim; Peter De Hoff; Willi Cheung; Anelizze Castro-Martinez; Andrea Rivera; Anthony Veder; Ariana Rivera; Cassandra Wauer; Jacqueline Holmes; Jedediah Wilson; Shayla N Ngo; Ashley Plascencia; Elijah S Lawrence; Elizabeth W Smoot; Emily R Eisner; Rebecca Tsai; Marisol Chacón; Nathan A Baer; Phoebe Seaver; Rodolfo A Salido; Stefan Aigner; Toan T Ngo; Tom Barber; Tyler Ostrander; Rebecca Fielding-Miller; Elizabeth H Simmons; Oscar E Zazueta; Idanya Serafin-Higuera; Manuel Sanchez-Alavez; Jose L Moreno-Camacho; Abraham García-Gil; Ashleigh R Murphy Schafer; Eric McDonald; Jeremy Corrigan; John D Malone; Sarah Stous; Seema Shah; Niema Moshiri; Alana Weiss; Catelyn Anderson; Christine M Aceves; Emily G Spencer; Emory C Hufbauer; Justin J Lee; Alison J King; Karthik S Ramesh; Kelly N Nguyen; Kieran Saucedo; Refugio Robles-Sikisaka; Kathleen M Fisch; Steven L Gonias; Amanda Birmingham; Daniel McDonald; Smruthi Karthikeyan; Natasha K Martin; Robert T Schooley; Agustin J Negrete; Horacio J Reyna; Jose R Chavez; Maria L Garcia; Jose M Cornejo-Bravo; David Becker; Magnus Isaksson; Nicole L Washington; William Lee; Richard S Garfein; Marco A Luna-Ruiz Esparza; Jonathan Alcántar-Fernández; Benjamin Henson; Kristen Jepsen; Beatriz Olivares-Flores; Gisela Barrera-Badillo; Irma Lopez-Martínez; José E Ramírez-González; Rita Flores-León; Stephen F Kingsmore; Alison Sanders; Allorah Pradenas; Benjamin White; Gary Matthews; Matt Hale; Ronald W McLawhon; Sharon L Reed; Terri Winbush; Ian H McHardy; Russel A Fielding; Laura Nicholson; Michael M Quigley; Aaron Harding; Art Mendoza; Omid Bakhtar; Sara H Browne; Jocelyn Olivas Flores; Diana G Rincon Rodríguez; Martin Gonzalez Ibarra; Luis C Robles Ibarra; Betsy J Arellano Vera; Jonathan Gonzalez Garcia; Alicia Harvey-Vera; Rob Knight; Louise C Laurent; Gene W Yeo; Joel O Wertheim; Xiang Ji; Michael Worobey; Marc A Suchard; Kristian G Andersen; Abraham Campos-Romero; Shirlee Wohl; Mark Zeller

doi:10.1016/j.cell.2023.11.024

Genomic surveillance reveals dynamic shifts in the connectivity of COVID-19 epidemics

Cell. 2023 Dec 21;186(26):5690-5704.e20. doi: 10.1016/j.cell.2023.11.024. Epub 2023 Dec 14.

Authors

Nathaniel L Matteson¹, Gabriel W Hassler², Ezra Kurzban³, Madison A Schwab³, Sarah A Perkins³, Karthik Gangavarapu⁴, Joshua I Levy³, Edyth Parker³, David Pride⁵, Abbas Hakim⁶, Peter De Hoff⁶, Willi Cheung⁶, Anelizze Castro-Martinez⁷, Andrea Rivera⁸, Anthony Veder⁸, Ariana Rivera⁸, Cassandra Wauer⁸, Jacqueline Holmes⁸, Jedediah Wilson⁸, Shayla N Ngo⁸, Ashley Plascencia⁸, Elijah S Lawrence⁸, Elizabeth W Smoot⁸, Emily R Eisner⁸, Rebecca Tsai⁸, Marisol Chacón⁸, Nathan A Baer⁸, Phoebe Seaver⁸, Rodolfo A Salido⁸, Stefan Aigner⁸, Toan T Ngo⁸, Tom Barber⁸, Tyler Ostrander⁸, Rebecca Fielding-Miller⁹, Elizabeth H Simmons¹⁰, Oscar E Zazueta¹¹, Idanya Serafin-Higuera¹², Manuel Sanchez-Alavez¹³, Jose L Moreno-Camacho¹⁴, Abraham García-Gil¹⁴, Ashleigh R Murphy Schafer¹⁵, Eric McDonald¹⁵, Jeremy Corrigan¹⁵, John D Malone¹⁵, Sarah Stous¹⁵, Seema Shah¹⁵, Niema Moshiri¹⁶, Alana Weiss³, Catelyn Anderson³, Christine M Aceves³, Emily G Spencer³, Emory C Hufbauer³, Justin J Lee³, Alison J King³, Karthik S Ramesh³, Kelly N Nguyen³, Kieran Saucedo³, Refugio Robles-Sikisaka³, Kathleen M Fisch¹⁷, Steven L Gonias¹⁸, Amanda Birmingham¹⁹, Daniel McDonald¹⁹, Smruthi Karthikeyan¹⁹, Natasha K Martin²⁰, Robert T Schooley²⁰, Agustin J Negrete²¹, Horacio J Reyna²¹, Jose R Chavez²¹, Maria L Garcia²¹, Jose M Cornejo-Bravo²², David Becker²³, Magnus Isaksson²³, Nicole L Washington²³, William Lee²³, Richard S Garfein²⁴, Marco A Luna-Ruiz Esparza²⁵, Jonathan Alcántar-Fernández²⁵, Benjamin Henson²⁶, Kristen Jepsen²⁶, Beatriz Olivares-Flores²⁷, Gisela Barrera-Badillo²⁷, Irma Lopez-Martínez²⁷, José E Ramírez-González²⁷, Rita Flores-León²⁷, Stephen F Kingsmore²⁸, Alison Sanders²⁹, Allorah Pradenas²⁹, Benjamin White²⁹, Gary Matthews²⁹, Matt Hale²⁹, Ronald W McLawhon²⁹, Sharon L Reed²⁹, Terri Winbush²⁹, Ian H McHardy³⁰, Russel A Fielding³⁰, Laura Nicholson³⁰, Michael M Quigley³⁰, Aaron Harding³¹, Art Mendoza³¹, Omid Bakhtar³¹, Sara H Browne³², Jocelyn Olivas Flores³³, Diana G Rincon Rodríguez³⁴, Martin Gonzalez Ibarra³⁴, Luis C Robles Ibarra³⁵, Betsy J Arellano Vera³⁶, Jonathan Gonzalez Garcia³⁷, Alicia Harvey-Vera³⁸, Rob Knight³⁹, Louise C Laurent⁷, Gene W Yeo⁴⁰, Joel O Wertheim⁴¹, Xiang Ji⁴², Michael Worobey⁴³, Marc A Suchard⁴⁴, Kristian G Andersen⁴⁵, Abraham Campos-Romero²⁵, Shirlee Wohl³, Mark Zeller⁴⁶

Affiliations

¹ Department of Immunology and Microbiology, Scripps Research, La Jolla, CA, USA. Electronic address: natem@scripps.edu.
² Department of Computational Medicine, University of California, Los Angeles, Los Angeles, CA, USA.
³ Department of Immunology and Microbiology, Scripps Research, La Jolla, CA, USA.
⁴ Department of Biomathematics, David Geffen School of Medicine at UCLA, University of California, Los Angeles, Los Angeles, CA, USA; Department of Immunology and Microbiology, Scripps Research, La Jolla, CA, USA.
⁵ Department of Pathology, University of California, San Diego, La Jolla, CA, USA; Department of Medicine, University of California, San Diego, La Jolla, CA, USA.
⁶ Expedited COVID Identification Environment (EXCITE) Laboratory, Department of Pediatrics, University of California, San Diego, La Jolla, CA, USA; Department of Obstetrics, Gynecology, and Reproductive Sciences, University of California, San Diego, La Jolla, CA, USA; COVID-19 Detection, Investigation, Surveillance, Clinical, and Outbreak Response, California Department of Public Health, Richmond, CA, USA.
⁷ Expedited COVID Identification Environment (EXCITE) Laboratory, Department of Pediatrics, University of California, San Diego, La Jolla, CA, USA; Department of Obstetrics, Gynecology, and Reproductive Sciences, University of California, San Diego, La Jolla, CA, USA; Sanford Consortium of Regenerative Medicine, University of California, San Diego, La Jolla, CA, USA.
⁸ Expedited COVID Identification Environment (EXCITE) Laboratory, Department of Pediatrics, University of California, San Diego, La Jolla, CA, USA.
⁹ Herbert Wertheim School of Public Health and Human Longevity Science, University of California, San Diego, La Jolla, CA, USA; Division of Infectious Disease and Global Public Health, University of California, San Diego, La Jolla, CA, USA.
¹⁰ Academic Affairs, University of California, San Diego, La Jolla, CA, USA.
¹¹ Department of Epidemiology, Secretaria de Salud de Baja California, Tijuana, Baja California, Mexico.
¹² Centro de Diagnostico COVID-19 UABC, Tijuana, Baja California, Mexico.
¹³ Centro de Diagnostico COVID-19 UABC, Tijuana, Baja California, Mexico; Department of Molecular Medicine, Scripps Research, La Jolla, CA, USA.
¹⁴ Clinical Laboratory Department, Salud Digna, A.C, Tijuana, Baja California, Mexico.
¹⁵ County of San Diego Health and Human Services Agency, San Diego, CA, USA.
¹⁶ Department of Computer Science and Engineering, University of California, San Diego, La Jolla, CA, USA.
¹⁷ Department of Obstetrics, Gynecology, and Reproductive Sciences, University of California, San Diego, La Jolla, CA, USA; Center for Computational Biology and Bioinformatics, University of California San Diego, La Jolla, CA, USA.
¹⁸ Department of Pathology, University of California, San Diego, La Jolla, CA, USA.
¹⁹ Department of Pediatrics, University of California, San Diego, La Jolla, CA, USA.
²⁰ Division of Infectious Disease and Global Public Health, University of California, San Diego, La Jolla, CA, USA.
²¹ Facultad de Ciencias de la Salud Universidad Autonoma de Baja California Valle de Las Palmas, Tijuana, Baja California, Mexico.
²² Facultad de Ciencias Quimicas e Ingenieria, Universidad Autonoma de Baja California, Tijuana, Baja California, Mexico.
²³ Helix, San Mateo, CA, USA.
²⁴ Herbert Wertheim School of Public Health and Human Longevity Science, University of California, San Diego, La Jolla, CA, USA.
²⁵ Innovation and Research Department, Salud Digna, A.C, Tijuana, Baja California, Mexico.
²⁶ Institute for Genomic Medicine, University of California, San Diego, La Jolla, CA, USA.
²⁷ Instituto de Diagnóstico y Referencia Epidemiológicos (InDRE), Ciudad de México, CDMX, Mexico.
²⁸ Rady Children's Institute for Genomic Medicine, San Diego, CA, USA.
²⁹ Return to Learn, University of California, San Diego, La Jolla, CA, USA.
³⁰ Scripps Health, La Jolla, San Diego, CA, USA.
³¹ Sharp Healthcare, San Diego, CA, USA.
³² Division of Infectious Disease and Global Public Health, University of California, San Diego, La Jolla, CA, USA; Specialist in Global Health, Encinitas, CA, USA.
³³ Facultad de Ciencias Quimicas e Ingenieria, Universidad Autonoma de Baja California, Tijuana, Baja California, Mexico; University of HealthMx, Tijuana, Baja California, Mexico.
³⁴ University of HealthMx, Tijuana, Baja California, Mexico; Facultad de Medicina, Universidad Xochicalco, Tijuana, Baja California, Mexico.
³⁵ University of HealthMx, Tijuana, Baja California, Mexico; Instituto de Seguridad y Servicios Sociales de los Trabajadores del Estado, Tijuana, Baja California, Mexico.
³⁶ University of HealthMx, Tijuana, Baja California, Mexico; Instituto Mexicano del Seguro Social, Tijuana, Baja California, Mexico.
³⁷ University of HealthMx, Tijuana, Baja California, Mexico; SIMNSA, Tijuana, Baja California, Mexico.
³⁸ University of California, San Diego, La Jolla, CA, USA.
³⁹ Department of Computer Science and Engineering, University of California, San Diego, La Jolla, CA, USA; Department of Pediatrics, University of California, San Diego, La Jolla, CA, USA; Department of Bioengineering, University of California, San Diego, La Jolla, CA, USA.
⁴⁰ Expedited COVID Identification Environment (EXCITE) Laboratory, Department of Pediatrics, University of California, San Diego, La Jolla, CA, USA; Sanford Consortium of Regenerative Medicine, University of California, San Diego, La Jolla, CA, USA; Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA, USA.
⁴¹ Department of Medicine, University of California, San Diego, La Jolla, CA, USA.
⁴² Department of Mathematics, School of Science and Engineering, Tulane University, New Orleans, LA, USA.
⁴³ Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ, USA.
⁴⁴ Department of Human Genetics, University of California, Los Angeles, Los Angeles, CA, USA.
⁴⁵ Department of Immunology and Microbiology, Scripps Research, La Jolla, CA, USA. Electronic address: andersen@scripps.edu.
⁴⁶ Department of Immunology and Microbiology, Scripps Research, La Jolla, CA, USA. Electronic address: zellerm@scripps.edu.

PMID: 38101407
PMCID: PMC10795731 (available on 2024-12-21)
DOI: 10.1016/j.cell.2023.11.024

Abstract

The maturation of genomic surveillance in the past decade has enabled tracking of the emergence and spread of epidemics at an unprecedented level. During the COVID-19 pandemic, for example, genomic data revealed that local epidemics varied considerably in the frequency of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) lineage importation and persistence, likely due to a combination of COVID-19 restrictions and changing connectivity. Here, we show that local COVID-19 epidemics are driven by regional transmission, including across international boundaries, but can become increasingly connected to distant locations following the relaxation of public health interventions. By integrating genomic, mobility, and epidemiological data, we find abundant transmission occurring between both adjacent and distant locations, supported by dynamic mobility patterns. We find that changing connectivity significantly influences local COVID-19 incidence. Our findings demonstrate a complex meaning of "local" when investigating connected epidemics and emphasize the importance of collaborative interventions for pandemic prevention and mitigation.

Keywords: COVID-19; SARS-CoV-2; genomic epidemiology; mobility; phylogenetics; travel restrictions; viral sequencing.

Publication types

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

MeSH terms

COVID-19* / epidemiology
COVID-19* / transmission
COVID-19* / virology
Genomics
Geography
Humans
Infection Control
Pandemics / prevention & control
Public Health
SARS-CoV-2 / genetics

Abstract

Publication types

MeSH terms

Grants and funding