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

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. +187 more·2021·Nature
DOI 10.1038/s41586-021-03677-y
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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.

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

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Crossref · 10.1038/s41586-021-03677-y

Cites

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Statistics

Nothing to recompute.

Claims the paper makes

0 of 12 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    Norway and Iceland seem to have had only a small number of introductions over the summer that led to substantial further spread.

    “Norway and Iceland, for example, seem to have only a small number of introductions over the summer that led to substantial further spread.”
    Quote in the paperNot a substantial claim
  • Findingown data

    Switzerland, the Netherlands, and the United Kingdom have sampled sequences corresponding to many independent introductions that include most major genotypes observed in Spain.

    “In contrast, countries like Switzerland, the Netherlands, or the United Kingdom have sampled sequences that correspond to a large number of independent introductions that include most major genotypes observed in Spain.”
    Quote in the paperSubstantial claim
  • Findingown data

    Most basal genotypes have been observed both in Spain and many other countries, suggesting repeated exports.

    “Most basal genotypes have been observed both in Spain and a large number of other countries, suggesting repeated exports.”
    Quote in the paperSubstantial claim
  • Findingown data

    Sequences from Hong Kong, Australia, New Zealand, and Singapore, presumably exported from Europe, were first detected between mid-August and mid-October.

    “Sequences from Hong Kong, Australia, New Zealand, and Singapore, presumably exports from Europe, were first detected between mid-August and mid-October (see Supplementary Table I).”
    Quote in the paperNot a substantial claim
  • Findingown data

    ELISA dose-response curves were indistinguishable for the SARS-CoV-2 2PS and 2P A222V D614G S ectodomain trimers.

    “The dose-response curves were indistinguishable for the SARS-CoV-2 2PS and the SARS-CoV-2 2P A222V D614G S ectodomain trimers (observed by ELISA, Fig. ED3a-d)”
    Quote in the paperSubstantial claim
  • May combine two claims. 38
  • Classified as probably not a substantial claim. 8

  • May combine two claims.

    Findingown data

    20E (EU1) harbors substantial diversity, and most major genotypes have been observed in many European countries.

    “The tree indicates that 20E (EU1) harbors substantial diversity and most major genotypes have been observed in many European countries.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    In Fig. ED4a, the majority of sequences from Norway and Iceland fall into one sector, while the remainder are singletons or very small clusters that have not spread.

    “In Fig. ED4a, the majority of sequences from these countries fall into one sector, the remainder are singletons or very small clusters that have not spread.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    During July and August 2020, Spain had higher per capita incidence than most other European countries, and 20E (EU1) was much more prevalent in Spain than elsewhere.

    “Throughout July and August 2020, Spain had a higher per capita incidence than most other European countries (see Fig ED5) and 20E (EU1) was much more prevalent in Spain then elsewhere, suggesting Spain as likely origin of most 20E (EU1) introductions to other countries.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Lentiviral particles with A222V mutant spike had slightly higher titers than those without, mean 1.3-fold higher, but the difference was not statistically significant after p24 normalization.

    “Lentiviral particles with the A222V mutant spike had slightly higher titers than those without (mean 1.3-fold higher), although the difference was not statistically significant after normalization by p24 concentration (Fig. ED3e-h).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    20E (EU1) first rose in frequency in Spain, reaching about 50% prevalence within a month of first detection and then 80%.

    “20E (EU1) first rose in frequency in Spain, jumping to around 50% prevalence within a month of the first sequence being detected before rising to 80%.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingcitation

    S:N439K occurs in two larger clusters across Europe and arose several times independently.

    “S:N439K is present in two larger clusters found across Europe 19 and arose several times independently.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [19] Thomson, E. C. et al. Circulating SARS-CoV-2 spike N439K variants maintain fitness while evading antibody-mediated immunity. Cell 184, 1171–1187 (2021). source

      Not checked in the free run.

  • May combine two claims.

    Findingreasoning

    About 320 introductions into Germany and 90 into Switzerland are expected.

    “Similarly, for Germany and Switzerland we would expect around 320 and 90 introductions of 20E (EU1), respectively.”
    Quote in the paperSubstantial claim
    • The authors state this as an assumption: Returning tourists have a similar SARS-CoV-2 incidence to the reported provincial incidence in Spain.
    • The authors state this as an assumption: Reported provincial incidence in Spain is accurate and representative for the import model.

  • May combine two claims.

    Findingown data

    There is some evidence that 20E (EU1) was growing faster than other variants in August, although there is little data to inform estimates of its effective reproductive number in July and it differs little from the prior.

    “While there is little data to inform estimates of R e for 20E (EU1) in July and it differs little from the prior, there is some evidence that 20E (EU1) was growing faster than other variants in August.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    A novel variant, 20E (EU1), carrying the S:A222V mutation on a S:D614G background emerged in early summer and was common in most countries with recent sequences.

    “A novel variant (orange; 20E (EU1)) with mutation S:A222V on a S:D614G background emerged in early summer and is common in most countries with recent sequences.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingown data

    There were a small number of larger transmission chains with more than 53 transmissions (20 across all data sets), which are not shown in the histograms.

    “There were also a small number of larger transmission chains including more than 53 transmissions (20 across all data sets) which are not shown in the histograms.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    After normalizing by p24 concentration, the difference in titer between A222V and D614G decreased from 1.28-fold to 1.14-fold, and the p-value increased to 0.16.

    “After p24 normalization, the titer difference shrinks fom 1.28 to 1.14 fold, increasing the p-value to 0.16.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingnone given

    Confirmed SARS-CoV-2 cases in Spain rose from about 10 per 100k per week in early July to 100 in late August, while case numbers remained low in most of Europe.

    “The number of confirmed SARS-CoV-2 cases in Spain rose from around 10 cases per 100k inhabitants per week in early July to 100 in late August, while case numbers remained low in most of Europe during this time.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingreasoning

    The peak in August in the Swiss analysis was larger under the 'min' definition than under the 'max' definition, consistent with a more conservative definition of a cluster requiring more onward transmission.

    “Notably, the peak in August in the Swiss analysis is larger under the 'min' definition (f) than under the 'max' definition (e), consistent with a more conservative definition of a cluster which would then require more onward transmission.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingcitation

    From 1 June to 30 September 2020, the Swiss FOPH reported 23,199 confirmed SARS-CoV-2 cases; 14,583 (62.9%) provided exposure information; 3,304 (22.7%) reported exposure abroad and 136 (0.9%) named Spain.

    “From 1 June 2020 to 30 September 2020, the Swiss Federal Office of Public Health (FOPH) reported 23,199 confirmed SARS-CoV-2 cases.14,583 (62.9%) cases provided information about their likely place of exposure and country of infection in a clinical registration form.Of these, 3,304 (22.7%) reported an exposure abroad and 136 (0.9%) named Spain as the country of infection.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Findingown data

    After sub-sampling, the 20E (EU1) cluster within the Nextstrain build contains 5,145 sequences, 3,369 of which are unique.

    “After sub-sampling, the 20E (EU1) cluster within the Nextstrain build contains 5,145 sequences, 3,369 of which are unique (accounting for Ns).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingnone given

    Switzerland reported 131 infections in travel returnees, while the model predicts 130.

    “Switzerland reported 131 infections in travel returnees, while the model predicts 130.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Travel resumed quickly and peaked during July and August.

    “Travel resumed quickly and peaked during July and August, see Fig. 3.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    The A222V substitution in the spike protein did not substantially affect antigenic properties or replication of pseudotyped lentiviruses.

    “The substitution A222V in spike has no substantial effect on antigenic properties (a-d) and replication of pseudotyped lentiviruses (e-h).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    In Europe, there were 206 singletons of 20E (EU1), representing 46% of all 20E (EU1) introductions.

    “In Europe, we see 206 20E (EU1) singletons (46% of all 20E (EU1) introductions).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationown data

    Initial introductions of 20E (EU1) likely originated from Spain, but cases outside Spain surpassed those in Spain in late September, and later cross-border transmissions likely originated in other countries.

    “While initial introductions of the variant likely originated from Spain, 20E (EU1) cases outside of Spain surpassed those in Spain in late September and later cross-border transmissions likely originated in other countries (see Fig ED5 B).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisenone given

    Mutations between positions 180 and 220 in N occur in almost every major lineage, and no evidence suggests important phenotypic consequences.

    “Different mutations between positions 180 and 220 in N are observed in almost every major lineage and we are not aware of any evidence suggesting that these mutations have important phenotypic consequence.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Residue S477 is near the receptor binding site and forms part of the epitope recognized by the S2E12 and C102 neutralizing antibodies.

    “Residue S477 is close to the receptor binding site (Fig ED2) and part of the epitope recognized by the S2E12 and C102 neutralizing antibodies 17,18 .”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [17] Barnes, C. O. et al. SARS-CoV-2 neutralizing antibody structures inform therapeutic strategies. Nature 588, 682–687 (2020). source

      Not checked in the free run.

    • cites [18] Tortorici, M. A. et al. Ultrapotent human antibodies protect against SARS-CoV-2 challenge via multiple mechanisms. Science 370, 950–957 (2020). source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    Despite sampling limitations, Fig. ED4a shows that most major genotypes in the cluster were distributed to multiple countries, suggesting identical genotypes were introduced into many countries.

    “Despite limitations in sampling, Fig. ED4a clearly shows that most major genotypes in this cluster were distributed to multiple countries, suggesting that identical genotypes were introduced into many countries .”
    Quote in the paperSubstantial claim
    • The authors state this as an assumption: The majority of mutations observed in the tree arose once and were carried between countries.

  • May combine two claims.

    Interpretationreasoning

    The variant initially spread among agricultural workers in Aragon and Catalonia, then moved into the local population and traveled to the Valencia Region and the rest of Spain.

    “The variant seems to have initially spread among agricultural workers in Aragon and Catalonia, then moved into the local population, where it was able to travel to the Valencia Region and on to the rest of the country.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationreasoning

    Countries where 20E (EU1) was rare (Belgium, France, Czech Republic) have seen similarly rapid increases, suggesting the rise was not driven by any particular lineage and that 20E (EU1) has no substantial difference in transmissibility.

    “However, countries where 20E (EU1) was rare (Belgium, France, Czech Republic, Fig. ED1) have seen similarly rapid increases, suggesting that this rise was not driven by any particular lineage and that 20E (EU1) has no substantial difference in transmissibility.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    The rapid increase of 20E (EU1) frequency slowed or stopped in most countries after summer travel and did not fully replace other variants, consistent with import-driven dynamics with little or no competitive advantage.

    “The fact that the rapid increase of the frequency of 20E (EU1) slowed or stopped in most countries after the summer travel period and didn't fully replace other variants is consistent with import driven dynamics with little or no competitive advantage.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    The smallest branches shown in the tree equal 1 mutation.

    “Though the jitter means branch lengths should be interpreted with caution, the smallest branches shown in the tree equal to 1 mutation.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Study design and conductreasoning

    Particularly for countries other than the UK, the full circulating diversity of the variant is probably not captured, so intermediate transmissions cannot be ruled out.

    “It is important to remember that, particularly for countries other than the UK, the full circulating diversity of the variant is probably not being captured, thus intermediate transmissions cannot be ruled out.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationown data

    Countries like Norway and Iceland had relatively few clusters, with one or two large clusters dominating, suggesting that a small number of introductions dominated 20E (EU1) circulation.

    “Countries like Norway and Iceland have relatively few clusters, with one or two large clusters dominating, suggesting a small number of introductions dominated 20E (EU1) circulation.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Study design and conductnone given

    The Expi293F cells used are not in the database of commonly misidentified cell lines.

    “They are not in the database of commonly misidentified cell lines.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationown data

    Countries with small (1-4 fold) and large (8-12 fold) discrepancies tend to visit distinct destinations in Spain, suggesting that underestimation of incidence in travel returnees is determined by destination and behavior.

    “Countries with small (1-4 fold) and large (8-12 fold) discrepancies tend to visit distinct destinations in Spain, see Figs.ED6 and ED7(c-e), further suggesting that underestimation of incidence in travel returnees is determined by destination and behavior.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim. May combine two claims.

    Study design and conductreasoning

    Selection based on three nucleotide substitutions excludes sequences with no coverage or reversions at those positions, but similarity-based sampling identifies these and nearby sequences.

    “This selection will exclude any sequences with no coverage or reversions at these positions, but the similarity-based sampling during the Nextstrain run will identify these, as well as any other nearby sequences, and incorporate them into the dataset.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductown data

    Problematic sequences were excluded because of high intra-sample variation, wrong dates, and over-divergence.

    “Further, we excluded several problematic sequences due to high intra-sample variation, wrong dates, and over-divergence (divergence values are implausible given the provided dates).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationreasoning

    Travel precautions such as quarantine should in principle have prevented spread of SARS-CoV-2 infections acquired abroad, but in practice failed to have the desired effect.

    “Travel precautions such as quarantine should in principle have prevented spread of SARS-CoV-2 infections acquired abroad, but in practice failed to have the desired effect.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationown data

    Countries like the UK and Denmark showed many clusters of varying size, indicating multiple introductions that led to onward spread.

    “Countries like the UK and Denmark, on the other hand, show many clusters of varying size, indicating multiple introductions that led to onward spread.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    While a slight transmission advantage cannot be ruled out, most of 20E (EU1) spread is explained by epidemiological factors.

    “While we cannot rule out that 20E (EU1) has a slight transmission advantage compared to other variants circulating at the time, most of its spread is explained by epidemiological factors.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    In the case of 20E (EU1), transmissibility, immune evasion, and clinical properties do not seem to have changed substantially.

    “In case of 20E (EU1) none of these seem to have changed substantially, making it an important example of how travel combined with large regional differences in prevalence can lead to substantial rapid shifts in the variant distribution without a dramatic transmission advantage.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    In high incidence settings, travel alone cannot explain a rapid rise in frequency, and the dynamics point to a bona fide transmission advantage.

    “In such a high incidence setting, travel alone cannot explain a rapid rise in frequency and the dynamics points to a bona fide transmission advantage.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    The experiment displayed represents two independent experiments.

    “The experiment shown is representative of two independent experiments.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Study design and conductown data

    The tree allows inference of lower bounds for the number of introductions to each country and identification of plausible origins of those introductions.

    “This tree allows us to infer lower bounds for the number of introductions to each country, and to identify plausible origins of those introductions.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    The association of 20E (EU1) with particular demographics will decay rapidly, and with it any associated increased transmission inferred by phylodynamics.

    “Such association with particular demographics will decay rapidly and with it any associated increased transmission inferred by phylodynamics.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductnone given

    The Expi293F cells used for protein production were not authenticated or tested for mycoplasma contamination.

    “Gibco (Fisher) Expi293F Cells were used for protein production and have not been authenticated or tested for mycoplasma contamination.”
    Quote in the paperNot a substantial claim
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

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • The decline in the number of cases by June, 2020 led governments in Europe to rescind control measures and to encourage a return to life as usual, which led to another wave of infections in September, 2020.

    “the decline in the number of cases by June, 2020 led governments in Europe to rescind control measures and to encourage a return to life as usual, especially in the context of Europe's upcoming summer holidays; this relaxing of control measures led to another wave of infections in countries across Europe in September, 2020.”

    From The Lancet Commission on lessons for the future from the COVID-19 pandemic (2022) · cites this paper as [180]

Cites

Flagged first, then by citations

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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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
Publisher
Springer Science and Business Media LLC
Published
2021-06-07
Volume
595
Issue
7869
Pages
707-712
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
DOI
10.1038/s41586-021-03677-y
OpenAlex
W3166766123
Semantic Scholar
2469490cde7d14d5793b659c17202c99169479ec
Cited by
425
References
47
Citations by year
2026: 12 · 2025: 34 · 2024: 53 · 2023: 80 · 2022: 128 · 2021: 115 · 2020: 3
FWCI
29.76
Type
journal article
Language
en
Open access
Licence
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

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-06.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-06.

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