Cited by 605SARS-CoV-2 and COVID-19 ResearchCOVID-19 epidemiological studiesSARS-CoV-2 detection and testing

The DOI matches its Crossref record; 52 of the 54 references it cites were found in a registry or an index, and 2 are not checked yet; none of the 12 sources its claims cite is checked for support yet.

Spread of a SARS-CoV-2 variant through Europe in the summer of 2020

Open access
Hodcroft, Emma B., Zuber, Moira, Nadeau, Sarah, Vaughan, Timothy G., Crawford, Katharine H. D., Althaus, Christian L., Reichmuth, Martina L., Bowen, John E., Walls, Alexandra C., Corti, Davide, Bloom, Jesse D., Veesler, David, Mateo, David, Hernando, Alberto, Comas, Iñaki, González-Candelas, Fernando, SeqCOVID-SPAIN consortium, González-Candelas, Fernando, Goig, Galo Adrian, Chiner-Oms, Álvaro, Cancino-Muñoz, Irving, López, Mariana Gabriela, Torres-Puente, Manuela, Gomez-Navarro, Inmaculada, Jiménez-Serrano, Santiago, Ruiz-Roldán, Lidia, Bracho, María Alma, García-González, Neris, Martínez-Priego, Llúcia, Galán-Vendrell, Inmaculada, Ruiz-Hueso, Paula, De Marco, Griselda, Ferrús, Maria Loreto, Carbó-Ramírez, Sandra, D’Auria, Giuseppe, Coscollá, Mireia, Ruiz-Rodríguez, Paula, Roig-Sena, Francisco Javier, Sanmartín, Isabel, Garcia-Souto, Daniel, Pequeno-Valtierra, Ana, Tubio, Jose M. C., Rodríguez-Castro, Jorge, Rabella, Nuria, Navarro, Ferrán, Miró, Elisenda, Rodríguez-Iglesias, Manuel, Galán-Sanchez, Fátima, Rodriguez-Pallares, Salud, de Toro, María, Escudero, María Bea, Azcona-Gutiérrez, José Manuel, Alberdi, Miriam Blasco, Mayor, Alfredo, García-Basteiro, Alberto L., Moncunill, Gemma, Dobaño, Carlota, Cisteró, Pau, García-de-Viedma, Darío, Pérez-Lago, Laura, Herranz, Marta, Sicilia, Jon, Catalán-Alonso, Pilar, Muñoz, Patricia, Muñoz-Cuevas, Cristina, Rodríguez-Rodríguez, Guadalupe, Alberola-Enguidanos, Juan, Nogueira, Jose Miguel, Camarena, Juan José, Rezusta, Antonio, Tristancho-Baró, Alexander, Milagro, Ana, Martínez-Cameo, Nieves Felisa, Gracia-Grataloup, Yolanda, Martró, Elisa, Bordoy, Antoni E., Not, Anna, Antuori-Torres, Adrián, Benito, Rafael, Algarate, Sonia, Bueno, Jessica, del Pozo, Jose Luis, Boga, Jose Antonio, Castelló-Abietar, Cristián, Rojo-Alba, Susana, Alvarez-Argüelles, Marta Elena, Melon, Santiago, Aranzamendi-Zaldumbide, Maitane, Vergara-Gómez, Andrea, Fernández-Pinero, Jovita, Martínez, Miguel J., Vila, Jordi, Rubio, Elisa, Peiró-Mestres, Aida, Navero-Castillejos, Jessica, Posada, David, Valverde, Diana, Estévez-Gómez, Nuria, Fernandez-Silva, Iria, de Chiara, Loretta, Gallego-García, Pilar, Varela, Nair, Moreno, Rosario, Tirado, Maria Dolores, Gomez-Pinedo, Ulises, Gozalo-Margüello, Mónica, Eliecer-Cano, Maria, Méndez-Legaza, José Manuel, Rodríguez-Lozano, Jesus, Siller, María, Pablo-Marcos, Daniel, Oliver, Antonio, Reina, Jordi, López-Causapé, Carla, Canut-Blasco, Andrés, Hernáez-Crespo, Silvia, Cordón, Maria Luz A., Lecároz-Agara, María-Concepción, Gómez-González, Carmen, Aguirre-Quiñonero, Amaia, López-Mirones, José Israel, Fernández-Torres, Marina, Almela-Ferrer, Maria Rosario, Gonzalo-Jiménez, Nieves, Ruiz-García, Maria Montserrat, Galiana, Antonio, Sanchez-Almendro, Judith, Cilla, Gustavo, Montes, Milagrosa, Piñeiro, Luis, Sorarrain, Ane, Marimón, José María, Gomez-Ruiz, Maria Dolores, López-Hontangas, José Luis, González Barberá, Eva M., Navarro-Marí, José María, Pedrosa-Corral, Irene, Sanbonmatsu-Gámez, Sara, Pérez-González, Carmen, Chamizo-López, Francisco, Bordes-Benítez, Ana, Navarro, David, Albert, Eliseo, Torres, Ignacio, Gascón, Isabel, Torregrosa-Hetland, Cristina Juana, Pastor-Boix, Eva, Cascales-Ramos, Paloma, Fuster-Escrivá, Begoña, Gimeno-Cardona, Concepción, Ocete, María Dolores, Medina-Gonzalez, Rafael, González-Cantó, Julia, Martínez-Macias, Olalla, Palop-Borrás, Begoña, de Toro, Inmaculada, Mediavilla-Gradolph, Maria Concepción, Pérez-Ruiz, Mercedes, González-Recio, Óscar, Gutiérrez-Rivas, Mónica, Simarro-Córdoba, Encarnación, Lozano-Serra, Julia, Robles-Fonseca, Lorena, de Salazar, Adolfo, Viñuela-González, Laura, Chueca, Natalia, García, Federico, Gómez-Camarasa, Cristina, Carvajal, Ana, de la Puente, Raul, Martín-Sánchez, Vicente, Fregeneda-Grandes, Juan-Miguel, Molina, Antonio José, Argüello, Héctor, Fernández-Villa, Tania, Farga-Martí, Maria Amparo, Domínguez-Márquez, Victoria, Costa-Alcalde, José Javier, Trastoy, Rocío, Barbeito-Castiñeiras, Gema, Coira, Amparo, Pérez-del-Molino, María Luisa, Aguilera, Antonio, Planas, Anna M., Soriano, Alex, Fernandez-Cádenas, Israel, Pérez-Tur, Jordi, Marcos, Maria Ángeles, Moreno-Docón, Antonio, Viedma, Esther, Mingorance, Jesús, Galán-Montemayor, Juan Carlos, Parra-Grande, Mónica, Stadler, Tanja, Neher, Richard A.·2021·Nature

Abstract

Following its emergence in late 2019, the spread of SARS-CoV-2 1,2 has been tracked by phylogenetic analysis of viral genome sequences in unprecedented detail 3-5. Although the virus spread globally in early 2020 before borders closed, intercontinental travel has since been greatly reduced. However, travel within Europe resumed in the summer of 2020. Here we report on a SARS-CoV-2 variant, 20E (EU1), that was identified in Spain in early summer 2020 and subsequently spread across Europe. We find no evidence that this variant has increased transmissibility, but instead demonstrate how rising incidence in Spain, resumption of travel, and lack of effective screening and containment may explain the variant's success. Despite travel restrictions, we estimate that 20E (EU1) was introduced hundreds of times to European countries by summertime travellers, which is likely to have undermined local efforts to minimize infection with SARS-CoV-2. Our results illustrate how a variant can rapidly become dominant even in the absence of a substantial transmission advantage in favourable epidemiological settings. Genomic surveillance is critical for understanding how travel can affect transmission of SARS-CoV-2, and thus for informing future containment strategies as travel resumes.

Checked 2026-10-06 · 2 references not checked yet

Overview

Integrity signals

Registry

Crossref · 10.1038/s41586-021-03677-y

Cites

52 of 54 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

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Claims the paper makes

41 Own result · 24 Own interpretation · 11 Own method · 8 Not checked yet · 7 No basis given

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Show all 49 claims

  • It may state two separate claims as one. 38
  • Probably not a substantial claim. 8
42 of 42
  • The authors state this as an assumption.

    Returning tourists have a similar SARS-CoV-2 incidence to the reported provincial incidence in Spain.

    “assuming that returning tourists have a similar incidence”
  • The authors state this as an assumption.

    20E (EU1) spread at the same rate as other variants in the resident countries.

    “This model assumes that 20E (EU1) spread at the same rate as other variants in the resident countries”
  • The authors state this as an assumption.

    The majority of mutations observed in the tree arose once and were carried between countries.

    “it is reasonable to assume that the majority of mutations observed in the tree arose once and were carried (possibly multiple times) between countries.”
  • The authors state this as an assumption.

    Reported provincial incidence in Spain is accurate and representative for the import model.

    “Taking reported incidence in the provinces at face value”
  • The authors state this as an assumption.

    20E (EU1) and non-20E (EU1) variants share a sampling probability.

    “20E (EU1) and non-20E (EU1) variants share a sampling probability”
  • The paper relies on this without support.

    Observed frequencies are subject to variable reporting delays.

    “Observed frequencies are subject to variable reporting delays.”
6 of 6

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Citations

Cites

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Research works printed but not linked: 1

  1. Pearson, C. A. B. et al. Estimates of severity and transmissibility of novel SARS-CoV-2 variant 501Y.V2 in South Africa. Preprint at https://cmmid.github.io/topics/covid19/sa-novel-variant.html (2021).

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Metadata

Authors
Hodcroft, E. B., Zuber, M., Nadeau, S., Vaughan, T. G., Crawford, K. H. D., Althaus, C. L., Reichmuth, M. L., Bowen, J. E., Walls, A. C., Corti, D., Bloom, J. D., Veesler, D., Mateo, D., Hernando, A., Comas, I., González-Candelas, F., SeqCOVID-SPAIN consortium, González-Candelas, F., Goig, G. A., Chiner-Oms, Á., Cancino-Muñoz, I., López, M. G., Torres-Puente, M., Gomez-Navarro, I., Jiménez-Serrano, S., Ruiz-Roldán, L., Bracho, M. A., García-González, N., Martínez-Priego, L., Galán-Vendrell, I., Ruiz-Hueso, P., De Marco, G., Ferrús, M. L., Carbó-Ramírez, S., D’Auria, G., Coscollá, M., Ruiz-Rodríguez, P., Roig-Sena, F. J., Sanmartín, I., Garcia-Souto, D., Pequeno-Valtierra, A., Tubio, J. M. C., Rodríguez-Castro, J., Rabella, N., Navarro, F., Miró, E., Rodríguez-Iglesias, M., Galán-Sanchez, F., Rodriguez-Pallares, S., de Toro, M., Escudero, M. B., Azcona-Gutiérrez, J. M., Alberdi, M. B., Mayor, A., García-Basteiro, A. L., Moncunill, G., Dobaño, C., Cisteró, P., García-de-Viedma, D., Pérez-Lago, L., Herranz, M., Sicilia, J., Catalán-Alonso, P., Muñoz, P., Muñoz-Cuevas, C., Rodríguez-Rodríguez, G., Alberola-Enguidanos, J., Nogueira, J. M., Camarena, J. J., Rezusta, A., Tristancho-Baró, A., Milagro, A., Martínez-Cameo, N. F., Gracia-Grataloup, Y., Martró, E., Bordoy, A. E., Not, A., Antuori-Torres, A., Benito, R., Algarate, S., Bueno, J., del Pozo, J. L., Boga, J. A., Castelló-Abietar, C., Rojo-Alba, S., Alvarez-Argüelles, M. E., Melon, S., Aranzamendi-Zaldumbide, M., Vergara-Gómez, A., Fernández-Pinero, J., Martínez, M. J., Vila, J., Rubio, E., Peiró-Mestres, A., Navero-Castillejos, J., Posada, D., Valverde, D., Estévez-Gómez, N., Fernandez-Silva, I., de Chiara, L., Gallego-García, P., Varela, N., Moreno, R., Tirado, M. D., Gomez-Pinedo, U., Gozalo-Margüello, M., Eliecer-Cano, M., Méndez-Legaza, J. M., Rodríguez-Lozano, J., Siller, M., Pablo-Marcos, D., Oliver, A., Reina, J., López-Causapé, C., Canut-Blasco, A., Hernáez-Crespo, S., Cordón, M. L. A., Lecároz-Agara, M.-C., Gómez-González, C., Aguirre-Quiñonero, A., López-Mirones, J. I., Fernández-Torres, M., Almela-Ferrer, M. R., Gonzalo-Jiménez, N., Ruiz-García, M. M., Galiana, A., Sanchez-Almendro, J., Cilla, G., Montes, M., Piñeiro, L., Sorarrain, A., Marimón, J. M., Gomez-Ruiz, M. D., López-Hontangas, J. L., González Barberá, E. M., Navarro-Marí, J. M., Pedrosa-Corral, I., Sanbonmatsu-Gámez, S., Pérez-González, C., Chamizo-López, F., Bordes-Benítez, A., Navarro, D., Albert, E., Torres, I., Gascón, I., Torregrosa-Hetland, C. J., Pastor-Boix, E., Cascales-Ramos, P., Fuster-Escrivá, B., Gimeno-Cardona, C., Ocete, M. D., Medina-Gonzalez, R., González-Cantó, J., Martínez-Macias, O., Palop-Borrás, B., de Toro, I., Mediavilla-Gradolph, M. C., Pérez-Ruiz, M., González-Recio, Ó., Gutiérrez-Rivas, M., Simarro-Córdoba, E., Lozano-Serra, J., Robles-Fonseca, L., de Salazar, A., Viñuela-González, L., Chueca, N., García, F., Gómez-Camarasa, C., Carvajal, A., de la Puente, R., Martín-Sánchez, V., Fregeneda-Grandes, J.-M., Molina, A. J., Argüello, H., Fernández-Villa, T., Farga-Martí, M. A., Domínguez-Márquez, V., Costa-Alcalde, J. J., Trastoy, R., Barbeito-Castiñeiras, G., Coira, A., Pérez-del-Molino, M. L., Aguilera, A., Planas, A. M., Soriano, A., Fernandez-Cádenas, I., Pérez-Tur, J., Marcos, M. Á., Moreno-Docón, A., Viedma, E., Mingorance, J., Galán-Montemayor, J. C., Parra-Grande, M., Stadler, T., & Neher, R. A.
Affiliations
  • University of Bern (CH)
  • University of Basel (CH)
  • SIB Swiss Institute of Bioinformatics (CH)
  • University of Washington (US)
  • Vir Biotechnology (Switzerland) (CH)
  • Howard Hughes Medical Institute (US)
  • Consejo Superior de Investigaciones Científicas (ES)
  • Universitat de València (ES)
  • Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana (ES)
  • Universitat Autònoma de Barcelona (ES)
  • Hospital de Sant Pau (ES)
  • Hospital Clínic de Barcelona (ES)
  • Hospital General Universitario Gregorio Marañón (ES)
  • Hospital San Pedro de Alcántara (ES)
  • Universidad de Zaragoza (ES)
  • Hospital Universitario Miguel Servet (ES)
  • Hospital Universitari Germans Trias i Pujol (ES)
  • Hospital Clínico Universitario Lozano Blesa (ES)
  • Servicio Gallego de Salud (ES)
  • Universidade de Vigo (ES)
  • Marqués de Valdecilla University Hospital (ES)
  • Health Research Institute of the Balearic Islands (ES)
  • Hospital Universitario Son Espases (ES)
  • Osakidetza (ES)
  • Hospital General Universitario de Elche (ES)
  • Biogipuzkoa Health Research Institute (ES)
  • Instituto de Investigación Biosanitaria de Granada (ES)
  • Hospital Universitario de Gran Canaria Doctor Negrín (ES)
  • INCLIVA Health Research Institute (ES)
  • Hospital General de Elda (ES)
  • Hospital General Universitario De Valencia (ES)
  • Hospital Regional Universitario de Málaga (ES)
  • Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (ES)
  • Hospital General Universitario de Albacete (ES)
  • Universidad de León (ES)
  • Hospital Arnau de Vilanova (ES)
  • Complejo Hospitalario Universitario de Santiago (ES)
  • Hospital Universitario 12 De Octubre (ES)
  • Hospital Universitario La Paz (ES)
  • Hospital Universitario Ramón y Cajal (ES)
  • Hospital Marina Baixa (ES)
Corresponding author
  • Hodcroft, Emma B.
  • Neher, Richard A.
ORCID
Venue
Nature
Published
2021-06-07
Volume
595
Issue
7869
Pages
707-712
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
OpenAlex
W3166766123
Cited by
425
References
47
Citations by year
2026: 12 · 2025: 34 · 2024: 53 · 2023: 80 · 2022: 128 · 2021: 115
FWCI
29.76
Type
journal article
Language
en
Open access
Locations
  • Nature (publishedVersion)
  • PubMed (publishedVersion)
  • edoc (University of Basel) (acceptedVersion)
  • Buleria (Universidad de León) (submittedVersion, cc-by-nc-nd)
  • RePEc: Research Papers in Economics (submittedVersion)
  • Bern Open Repository and Information System (University of Bern) (submittedVersion, other-oa)
  • DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
  • Repository of Digital Objects for Teaching Research and Culture (University of Valencia) (submittedVersion, other-oa)
  • Zaguan (University of Zaragoza Repository) (submittedVersion, cc-by)
Funders
  • National Science Foundation
  • Howard Hughes Medical Institute
  • Burroughs Wellcome Fund
  • Universität Basel
  • Fast Grants
  • European Commission (HORIZON2020, 101003688, COVID-19)
  • Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (196046, 196267)
  • Bundesamt für Gesundheit
  • Eidgenössische Technische Hochschule Zürich
  • Consejo Superior de Investigaciones Científicas
  • Instituto de Salud Carlos III (COV20, COV20/00140)
  • National Institute of General Medical Sciences (R01GM120553)
  • National Institute of Allergy and Infectious Diseases (HHSN272201700059C, COVID-19, DP1AI158186, F30AI149928, R01AI141707)
  • H2020 European Research Council (638553)
Topics
  • Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
  • Physical Sciences › Mathematics › Modeling and Simulation › COVID-19 epidemiological studies
  • Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 detection and testing
Keywords
SARS-CoV-2, COVID-19 pandemic, international travel, viral spread, genomic surveillance, travel restrictions, containment strategies, transmissibility, summer 2020, Europe, Spain
MeSH terms
COVID-19, SARS-CoV-2, Europe, Genotype, Humans, Phylogeny, Seasons, Time Factors, Travel

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