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

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. NgoAshley 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

Research output: Contribution to journal › Article › peer-review

5 Scopus citations

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.

Original language	English (US)
Pages (from-to)	5690-5704.e20
Journal	Cell
Volume	186
Issue number	26
DOIs	https://doi.org/10.1016/j.cell.2023.11.024
State	Published - Dec 21 2023
Externally published	Yes

Keywords

COVID-19
SARS-CoV-2
genomic epidemiology
mobility
phylogenetics
travel restrictions
viral sequencing

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

Access to Document

10.1016/j.cell.2023.11.024

Cite this

Matteson, N. L., Hassler, G. W., Kurzban, E., Schwab, M. A., Perkins, S. A., Gangavarapu, K., Levy, J. I., Parker, E., Pride, D., Hakim, A., De Hoff, P., Cheung, W., Castro-Martinez, A., Rivera, A., Veder, A., Rivera, A., Wauer, C., Holmes, J., Wilson, J., ... Zeller, M. (2023). Genomic surveillance reveals dynamic shifts in the connectivity of COVID-19 epidemics. Cell, 186(26), 5690-5704.e20. https://doi.org/10.1016/j.cell.2023.11.024

Matteson, NL, Hassler, GW, Kurzban, E, Schwab, MA, Perkins, SA, Gangavarapu, K, Levy, JI, Parker, E, Pride, D, Hakim, A, De Hoff, P, Cheung, W, Castro-Martinez, A, Rivera, A, Veder, A, Rivera, A, Wauer, C, Holmes, J, Wilson, J, Ngo, SN, Plascencia, A, Lawrence, ES, Smoot, EW, Eisner, ER, Tsai, R, Chacón, M, Baer, NA, Seaver, P, Salido, RA, Aigner, S, Ngo, TT, Barber, T, Ostrander, T, Fielding-Miller, R, Simmons, EH, Zazueta, OE, Serafin-Higuera, I, Sanchez-Alavez, M, Moreno-Camacho, JL, García-Gil, A, Murphy Schafer, AR, McDonald, E, Corrigan, J, Malone, JD, Stous, S, Shah, S, Moshiri, N, Weiss, A, Anderson, C, Aceves, CM, Spencer, EG, Hufbauer, EC, Lee, JJ, King, AJ, Ramesh, KS, Nguyen, KN, Saucedo, K, Robles-Sikisaka, R, Fisch, KM, Gonias, SL, Birmingham, A, McDonald, D, Karthikeyan, S, Martin, NK, Schooley, RT, Negrete, AJ, Reyna, HJ, Chavez, JR, Garcia, ML, Cornejo-Bravo, JM, Becker, D, Isaksson, M, Washington, NL, Lee, W, Garfein, RS, Luna-Ruiz Esparza, MA, Alcántar-Fernández, J, Henson, B, Jepsen, K, Olivares-Flores, B, Barrera-Badillo, G, Lopez-Martínez, I, Ramírez-González, JE, Flores-León, R, Kingsmore, SF, Sanders, A, Pradenas, A, White, B, Matthews, G, Hale, M, McLawhon, RW, Reed, SL, Winbush, T, McHardy, IH, Fielding, RA, Nicholson, L, Quigley, MM, Harding, A, Mendoza, A, Bakhtar, O, Browne, SH, Olivas Flores, J, Rincon Rodríguez, DG, Gonzalez Ibarra, M, Robles Ibarra, LC, Arellano Vera, BJ, Gonzalez Garcia, J, Harvey-Vera, A, Knight, R, Laurent, LC, Yeo, GW, Wertheim, JO, Ji, X, Worobey, M, Suchard, MA, Andersen, KG, Campos-Romero, A, Wohl, S & Zeller, M 2023, 'Genomic surveillance reveals dynamic shifts in the connectivity of COVID-19 epidemics', Cell, vol. 186, no. 26, pp. 5690-5704.e20. https://doi.org/10.1016/j.cell.2023.11.024

@article{5601da92f980415d829dfbdd2868315a,

title = "Genomic surveillance reveals dynamic shifts in the connectivity of COVID-19 epidemics",

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",

author = "Matteson, {Nathaniel L.} and Hassler, {Gabriel W.} and Ezra Kurzban and Schwab, {Madison A.} and Perkins, {Sarah A.} and Karthik Gangavarapu and Levy, {Joshua I.} and Edyth Parker and David Pride and Abbas Hakim and {De Hoff}, Peter and Willi Cheung and Anelizze Castro-Martinez and Andrea Rivera and Anthony Veder and Ariana Rivera and Cassandra Wauer and Jacqueline Holmes and Jedediah Wilson and Ngo, {Shayla N.} and Ashley Plascencia and Lawrence, {Elijah S.} and Smoot, {Elizabeth W.} and Eisner, {Emily R.} and Rebecca Tsai and Marisol Chac{\'o}n and Baer, {Nathan A.} and Phoebe Seaver and Salido, {Rodolfo A.} and Stefan Aigner and Ngo, {Toan T.} and Tom Barber and Tyler Ostrander and Rebecca Fielding-Miller and Simmons, {Elizabeth H.} and Zazueta, {Oscar E.} and Idanya Serafin-Higuera and Manuel Sanchez-Alavez and Moreno-Camacho, {Jose L.} and Abraham Garc{\'i}a-Gil and {Murphy Schafer}, {Ashleigh R.} and Eric McDonald and Jeremy Corrigan and Malone, {John D.} and Sarah Stous and Seema Shah and Niema Moshiri and Alana Weiss and Catelyn Anderson and Aceves, {Christine M.} and Spencer, {Emily G.} and Hufbauer, {Emory C.} and Lee, {Justin J.} and King, {Alison J.} and Ramesh, {Karthik S.} and Nguyen, {Kelly N.} and Kieran Saucedo and Refugio Robles-Sikisaka and Fisch, {Kathleen M.} and Gonias, {Steven L.} and Amanda Birmingham and Daniel McDonald and Smruthi Karthikeyan and Martin, {Natasha K.} and Schooley, {Robert T.} and Negrete, {Agustin J.} and Reyna, {Horacio J.} and Chavez, {Jose R.} and Garcia, {Maria L.} and Cornejo-Bravo, {Jose M.} and David Becker and Magnus Isaksson and Washington, {Nicole L.} and William Lee and Garfein, {Richard S.} and {Luna-Ruiz Esparza}, {Marco A.} and Jonathan Alc{\'a}ntar-Fern{\'a}ndez and Benjamin Henson and Kristen Jepsen and Beatriz Olivares-Flores and Gisela Barrera-Badillo and Irma Lopez-Mart{\'i}nez and Ram{\'i}rez-Gonz{\'a}lez, {Jos{\'e} E.} and Rita Flores-Le{\'o}n and Kingsmore, {Stephen F.} and Alison Sanders and Allorah Pradenas and Benjamin White and Gary Matthews and Matt Hale and McLawhon, {Ronald W.} and Reed, {Sharon L.} and Terri Winbush and McHardy, {Ian H.} and Fielding, {Russel A.} and Laura Nicholson and Quigley, {Michael M.} and Aaron Harding and Art Mendoza and Omid Bakhtar and Browne, {Sara H.} and {Olivas Flores}, Jocelyn and {Rincon Rodr{\'i}guez}, {Diana G.} and {Gonzalez Ibarra}, Martin and {Robles Ibarra}, {Luis C.} and {Arellano Vera}, {Betsy J.} and {Gonzalez Garcia}, Jonathan and Alicia Harvey-Vera and Rob Knight and Laurent, {Louise C.} and Yeo, {Gene W.} and Wertheim, {Joel O.} and Xiang Ji and Michael Worobey and Suchard, {Marc A.} and Andersen, {Kristian G.} and Abraham Campos-Romero and Shirlee Wohl and Mark Zeller",

note = "Publisher Copyright: {\textcopyright} 2023 Elsevier Inc.",

year = "2023",

month = dec,

day = "21",

doi = "10.1016/j.cell.2023.11.024",

language = "English (US)",

volume = "186",

pages = "5690--5704.e20",

journal = "Cell",

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number = "26",

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TY - JOUR

T1 - Genomic surveillance reveals dynamic shifts in the connectivity of COVID-19 epidemics

AU - Matteson, Nathaniel L.

AU - Hassler, Gabriel W.

AU - Kurzban, Ezra

AU - Schwab, Madison A.

AU - Perkins, Sarah A.

AU - Gangavarapu, Karthik

AU - Levy, Joshua I.

AU - Parker, Edyth

AU - Pride, David

AU - Hakim, Abbas

AU - De Hoff, Peter

AU - Cheung, Willi

AU - Castro-Martinez, Anelizze

AU - Rivera, Andrea

AU - Veder, Anthony

AU - Rivera, Ariana

AU - Wauer, Cassandra

AU - Holmes, Jacqueline

AU - Wilson, Jedediah

AU - Ngo, Shayla N.

AU - Plascencia, Ashley

AU - Lawrence, Elijah S.

AU - Smoot, Elizabeth W.

AU - Eisner, Emily R.

AU - Tsai, Rebecca

AU - Chacón, Marisol

AU - Baer, Nathan A.

AU - Seaver, Phoebe

AU - Salido, Rodolfo A.

AU - Aigner, Stefan

AU - Ngo, Toan T.

AU - Barber, Tom

AU - Ostrander, Tyler

AU - Fielding-Miller, Rebecca

AU - Simmons, Elizabeth H.

AU - Zazueta, Oscar E.

AU - Serafin-Higuera, Idanya

AU - Sanchez-Alavez, Manuel

AU - Moreno-Camacho, Jose L.

AU - García-Gil, Abraham

AU - Murphy Schafer, Ashleigh R.

AU - McDonald, Eric

AU - Corrigan, Jeremy

AU - Malone, John D.

AU - Stous, Sarah

AU - Shah, Seema

AU - Moshiri, Niema

AU - Weiss, Alana

AU - Anderson, Catelyn

AU - Aceves, Christine M.

AU - Spencer, Emily G.

AU - Hufbauer, Emory C.

AU - Lee, Justin J.

AU - King, Alison J.

AU - Ramesh, Karthik S.

AU - Nguyen, Kelly N.

AU - Saucedo, Kieran

AU - Robles-Sikisaka, Refugio

AU - Fisch, Kathleen M.

AU - Gonias, Steven L.

AU - Birmingham, Amanda

AU - McDonald, Daniel

AU - Karthikeyan, Smruthi

AU - Martin, Natasha K.

AU - Schooley, Robert T.

AU - Negrete, Agustin J.

AU - Reyna, Horacio J.

AU - Chavez, Jose R.

AU - Garcia, Maria L.

AU - Cornejo-Bravo, Jose M.

AU - Becker, David

AU - Isaksson, Magnus

AU - Washington, Nicole L.

AU - Lee, William

AU - Garfein, Richard S.

AU - Luna-Ruiz Esparza, Marco A.

AU - Alcántar-Fernández, Jonathan

AU - Henson, Benjamin

AU - Jepsen, Kristen

AU - Olivares-Flores, Beatriz

AU - Barrera-Badillo, Gisela

AU - Lopez-Martínez, Irma

AU - Ramírez-González, José E.

AU - Flores-León, Rita

AU - Kingsmore, Stephen F.

AU - Sanders, Alison

AU - Pradenas, Allorah

AU - White, Benjamin

AU - Matthews, Gary

AU - Hale, Matt

AU - McLawhon, Ronald W.

AU - Reed, Sharon L.

AU - Winbush, Terri

AU - McHardy, Ian H.

AU - Fielding, Russel A.

AU - Nicholson, Laura

AU - Quigley, Michael M.

AU - Harding, Aaron

AU - Mendoza, Art

AU - Bakhtar, Omid

AU - Browne, Sara H.

AU - Olivas Flores, Jocelyn

AU - Rincon Rodríguez, Diana G.

AU - Gonzalez Ibarra, Martin

AU - Robles Ibarra, Luis C.

AU - Arellano Vera, Betsy J.

AU - Gonzalez Garcia, Jonathan

AU - Harvey-Vera, Alicia

AU - Knight, Rob

AU - Laurent, Louise C.

AU - Yeo, Gene W.

AU - Wertheim, Joel O.

AU - Ji, Xiang

AU - Worobey, Michael

AU - Suchard, Marc A.

AU - Andersen, Kristian G.

AU - Campos-Romero, Abraham

AU - Wohl, Shirlee

AU - Zeller, Mark

PY - 2023/12/21

Y1 - 2023/12/21

N2 - 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.

AB - 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.

KW - COVID-19

KW - SARS-CoV-2

KW - genomic epidemiology

KW - mobility

KW - phylogenetics

KW - travel restrictions

KW - viral sequencing

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UR - http://www.scopus.com/inward/citedby.url?scp=85180565043&partnerID=8YFLogxK

U2 - 10.1016/j.cell.2023.11.024

DO - 10.1016/j.cell.2023.11.024

M3 - Article

C2 - 38101407

AN - SCOPUS:85180565043

SN - 0092-8674

VL - 186

SP - 5690-5704.e20

JO - Cell

JF - Cell

IS - 26

ER -

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

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Keywords

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