Genomic epidemiology reveals multiple introductions of SARS-CoV-2 from mainland Europe into Scotland

Ana da Silva Filipe; James G. Shepherd; Thomas Williams; Joseph Hughes; Elihu Aranday-Cortes; Patawee Asamaphan; Shirin Ashraf; Carlos Balcazar; Kirstyn Brunker; Alasdair Campbell; Stephen Carmichael; Chris Davis; Rebecca Dewar; Michael D. Gallagher; Rory Gunson; Verity Hill; Antonia Ho; Ben Jackson; Edward James; Natasha Jesudason; Natasha Johnson; E. Carol McWilliam Leitch; Kathy Li; Alasdair MacLean; Daniel Mair; David A. McAllister; John T. McCrone; Sarah E. McDonald; Martin P. McHugh; A. Keith Morris; Jenna Nichols; Marc Niebel; Kyriaki Nomikou; Richard J. Orton; Áine O’Toole; Massimo Palmarini; Benjamin J. Parcell; Yasmin A. Parr; Andrew Rambaut; Stefan Rooke; Sharif Shaaban; Rajiv Shah; Joshua B. Singer; Katherine Smollett; Igor Starinskij; Lily Tong; Vattipally B. Sreenu; Elizabeth Wastnedge; Matthew T. G. Holden; David L. Robertson; Kate Templeton; Emma C. Thomson

doi:10.1038/s41564-020-00838-z

Genomic epidemiology reveals multiple introductions of SARS-CoV-2 from mainland Europe into Scotland

Ana da Silva Filipe, James G. Shepherd, Thomas Williams, Joseph Hughes, Elihu Aranday-Cortes, Patawee Asamaphan, Shirin Ashraf, Carlos Balcazar, Kirstyn Brunker, Alasdair Campbell, Stephen Carmichael, Chris Davis, Rebecca Dewar, Michael D. Gallagher, Rory Gunson, Verity Hill, Antonia Ho, Ben Jackson, Edward James, Natasha JesudasonNatasha Johnson, E. Carol McWilliam Leitch, Kathy Li, Alasdair MacLean, Daniel Mair, David A. McAllister, John T. McCrone, Sarah E. McDonald, Martin P. McHugh, A. Keith Morris, Jenna Nichols, Marc Niebel, Kyriaki Nomikou, Richard J. Orton, Áine O’Toole, Massimo Palmarini, Benjamin J. Parcell, Yasmin A. Parr, Andrew Rambaut, Stefan Rooke, Sharif Shaaban, Rajiv Shah, Joshua B. Singer, Katherine Smollett, Igor Starinskij, Lily Tong, Vattipally B. Sreenu, Elizabeth Wastnedge, , Matthew T. G. Holden, David L. Robertson, Kate Templeton, Emma C. Thomson (Lead / Corresponding author)

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Abstract

Coronavirus disease 2019 (COVID-19) was first diagnosed in Scotland on 1 March 2020. During the first month of the outbreak, 2,641 cases of COVID-19 led to 1,832 hospital admissions, 207 intensive care admissions and 126 deaths. We aimed to identify the source and number of introductions of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) into Scotland using a combined phylogenetic and epidemiological approach. Sequencing of 1,314 SARS-CoV-2 viral genomes from available patient samples enabled us to estimate that SARS-CoV-2 was introduced to Scotland on at least 283 occasions during February and March 2020. Epidemiological analysis confirmed that early introductions of SARS-CoV-2 originated from mainland Europe (the majority from Italy and Spain). We identified subsequent early outbreaks in the community, within healthcare facilities and at an international conference. Community transmission occurred after 2 March, 3 weeks before control measures were introduced. Earlier travel restrictions or quarantine measures, both locally and internationally, would have reduced the number of COVID-19 cases in Scotland. The risk of multiple reintroduction events in future waves of infection remains high in the absence of population immunity.

Original language	English
Pages (from-to)	112-122
Number of pages	11
Journal	Nature Microbiology
Volume	6
Issue number	1
Early online date	21 Dec 2020
DOIs	https://doi.org/10.1038/s41564-020-00838-z
Publication status	Published - Jan 2021

Keywords

SARS-CoV-2
Viral epidemiology

ASJC Scopus subject areas

Microbiology
Immunology
Applied Microbiology and Biotechnology
Genetics
Microbiology (medical)
Cell Biology

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10.1038/s41564-020-00838-z

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da Silva Filipe, A., Shepherd, J. G., Williams, T., Hughes, J., Aranday-Cortes, E., Asamaphan, P., Ashraf, S., Balcazar, C., Brunker, K., Campbell, A., Carmichael, S., Davis, C., Dewar, R., Gallagher, M. D., Gunson, R., Hill, V., Ho, A., Jackson, B., James, E., ... Thomson, E. C. (2021). Genomic epidemiology reveals multiple introductions of SARS-CoV-2 from mainland Europe into Scotland. Nature Microbiology, 6(1), 112-122. https://doi.org/10.1038/s41564-020-00838-z

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title = "Genomic epidemiology reveals multiple introductions of SARS-CoV-2 from mainland Europe into Scotland",

abstract = "Coronavirus disease 2019 (COVID-19) was first diagnosed in Scotland on 1 March 2020. During the first month of the outbreak, 2,641 cases of COVID-19 led to 1,832 hospital admissions, 207 intensive care admissions and 126 deaths. We aimed to identify the source and number of introductions of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) into Scotland using a combined phylogenetic and epidemiological approach. Sequencing of 1,314 SARS-CoV-2 viral genomes from available patient samples enabled us to estimate that SARS-CoV-2 was introduced to Scotland on at least 283 occasions during February and March 2020. Epidemiological analysis confirmed that early introductions of SARS-CoV-2 originated from mainland Europe (the majority from Italy and Spain). We identified subsequent early outbreaks in the community, within healthcare facilities and at an international conference. Community transmission occurred after 2 March, 3 weeks before control measures were introduced. Earlier travel restrictions or quarantine measures, both locally and internationally, would have reduced the number of COVID-19 cases in Scotland. The risk of multiple reintroduction events in future waves of infection remains high in the absence of population immunity.",

keywords = "SARS-CoV-2, Viral epidemiology",

author = "{da Silva Filipe}, Ana and Shepherd, {James G.} and Thomas Williams and Joseph Hughes and Elihu Aranday-Cortes and Patawee Asamaphan and Shirin Ashraf and Carlos Balcazar and Kirstyn Brunker and Alasdair Campbell and Stephen Carmichael and Chris Davis and Rebecca Dewar and Gallagher, {Michael D.} and Rory Gunson and Verity Hill and Antonia Ho and Ben Jackson and Edward James and Natasha Jesudason and Natasha Johnson and {McWilliam Leitch}, {E. Carol} and Kathy Li and Alasdair MacLean and Daniel Mair and McAllister, {David A.} and McCrone, {John T.} and McDonald, {Sarah E.} and McHugh, {Martin P.} and Morris, {A. Keith} and Jenna Nichols and Marc Niebel and Kyriaki Nomikou and Orton, {Richard J.} and {\'A}ine O{\textquoteright}Toole and Massimo Palmarini and Parcell, {Benjamin J.} and Parr, {Yasmin A.} and Andrew Rambaut and Stefan Rooke and Sharif Shaaban and Rajiv Shah and Singer, {Joshua B.} and Katherine Smollett and Igor Starinskij and Lily Tong and Sreenu, {Vattipally B.} and Elizabeth Wastnedge and Holden, {Matthew T. G.} and Robertson, {David L.} and Kate Templeton and Thomson, {Emma C.}",

note = "Funding Information: We thank all staff at the Scottish NHS virology laboratories who provided samples for sequencing, as well as the global researchers who shared genome data on GISAID (https://www.gisaid.org). We thank R. Kuo, T. Regan and A. Warr (The Roslin Institute, University of Edinburgh) for sequencing reagents, and S. Arkison for server maintenance. The study was funded by the Medical Research Council (MRC) core award (MC UU 1201412), a Wellcome Trust Collaborator Award (206298/Z/17/Z – for the ARTIC Network), and a Wellcome Trust Award (204802/Z/16/Z). COG-UK is supported by funding from the MRC part of UK Research and Innovation (UKRI), the National Institute of Health Research (NIHR) and Genome Research Limited, operating as the Wellcome Sanger Institute. The Cloud Infrastructure for Microbial Bioinformatics is funded by the MRC through grant MR/L015080/1. Publisher Copyright: {\textcopyright} 2020, The Author(s), under exclusive licence to Springer Nature Limited.",

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doi = "10.1038/s41564-020-00838-z",

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da Silva Filipe, A, Shepherd, JG, Williams, T, Hughes, J, Aranday-Cortes, E, Asamaphan, P, Ashraf, S, Balcazar, C, Brunker, K, Campbell, A, Carmichael, S, Davis, C, Dewar, R, Gallagher, MD, Gunson, R, Hill, V, Ho, A, Jackson, B, James, E, Jesudason, N, Johnson, N, McWilliam Leitch, EC, Li, K, MacLean, A, Mair, D, McAllister, DA, McCrone, JT, McDonald, SE, McHugh, MP, Morris, AK, Nichols, J, Niebel, M, Nomikou, K, Orton, RJ, O’Toole, Á, Palmarini, M, Parcell, BJ, Parr, YA, Rambaut, A, Rooke, S, Shaaban, S, Shah, R, Singer, JB, Smollett, K, Starinskij, I, Tong, L, Sreenu, VB, Wastnedge, E, Holden, MTG, Robertson, DL & Templeton, K & Thomson, EC 2021, 'Genomic epidemiology reveals multiple introductions of SARS-CoV-2 from mainland Europe into Scotland', Nature Microbiology, vol. 6, no. 1, pp. 112-122. https://doi.org/10.1038/s41564-020-00838-z

TY - JOUR

T1 - Genomic epidemiology reveals multiple introductions of SARS-CoV-2 from mainland Europe into Scotland

AU - da Silva Filipe, Ana

AU - Shepherd, James G.

AU - Williams, Thomas

AU - Hughes, Joseph

AU - Aranday-Cortes, Elihu

AU - Asamaphan, Patawee

AU - Ashraf, Shirin

AU - Balcazar, Carlos

AU - Brunker, Kirstyn

AU - Campbell, Alasdair

AU - Carmichael, Stephen

AU - Davis, Chris

AU - Dewar, Rebecca

AU - Gallagher, Michael D.

AU - Gunson, Rory

AU - Hill, Verity

AU - Ho, Antonia

AU - Jackson, Ben

AU - James, Edward

AU - Jesudason, Natasha

AU - Johnson, Natasha

AU - McWilliam Leitch, E. Carol

AU - Li, Kathy

AU - MacLean, Alasdair

AU - Mair, Daniel

AU - McAllister, David A.

AU - McCrone, John T.

AU - McDonald, Sarah E.

AU - McHugh, Martin P.

AU - Morris, A. Keith

AU - Nichols, Jenna

AU - Niebel, Marc

AU - Nomikou, Kyriaki

AU - Orton, Richard J.

AU - O’Toole, Áine

AU - Palmarini, Massimo

AU - Parcell, Benjamin J.

AU - Parr, Yasmin A.

AU - Rambaut, Andrew

AU - Rooke, Stefan

AU - Shaaban, Sharif

AU - Shah, Rajiv

AU - Singer, Joshua B.

AU - Smollett, Katherine

AU - Starinskij, Igor

AU - Tong, Lily

AU - Sreenu, Vattipally B.

AU - Wastnedge, Elizabeth

AU - Holden, Matthew T. G.

AU - Robertson, David L.

AU - Templeton, Kate

AU - Thomson, Emma C.

N1 - Funding Information: We thank all staff at the Scottish NHS virology laboratories who provided samples for sequencing, as well as the global researchers who shared genome data on GISAID (https://www.gisaid.org). We thank R. Kuo, T. Regan and A. Warr (The Roslin Institute, University of Edinburgh) for sequencing reagents, and S. Arkison for server maintenance. The study was funded by the Medical Research Council (MRC) core award (MC UU 1201412), a Wellcome Trust Collaborator Award (206298/Z/17/Z – for the ARTIC Network), and a Wellcome Trust Award (204802/Z/16/Z). COG-UK is supported by funding from the MRC part of UK Research and Innovation (UKRI), the National Institute of Health Research (NIHR) and Genome Research Limited, operating as the Wellcome Sanger Institute. The Cloud Infrastructure for Microbial Bioinformatics is funded by the MRC through grant MR/L015080/1. Publisher Copyright: © 2020, The Author(s), under exclusive licence to Springer Nature Limited.

PY - 2021/1

Y1 - 2021/1

N2 - Coronavirus disease 2019 (COVID-19) was first diagnosed in Scotland on 1 March 2020. During the first month of the outbreak, 2,641 cases of COVID-19 led to 1,832 hospital admissions, 207 intensive care admissions and 126 deaths. We aimed to identify the source and number of introductions of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) into Scotland using a combined phylogenetic and epidemiological approach. Sequencing of 1,314 SARS-CoV-2 viral genomes from available patient samples enabled us to estimate that SARS-CoV-2 was introduced to Scotland on at least 283 occasions during February and March 2020. Epidemiological analysis confirmed that early introductions of SARS-CoV-2 originated from mainland Europe (the majority from Italy and Spain). We identified subsequent early outbreaks in the community, within healthcare facilities and at an international conference. Community transmission occurred after 2 March, 3 weeks before control measures were introduced. Earlier travel restrictions or quarantine measures, both locally and internationally, would have reduced the number of COVID-19 cases in Scotland. The risk of multiple reintroduction events in future waves of infection remains high in the absence of population immunity.

AB - Coronavirus disease 2019 (COVID-19) was first diagnosed in Scotland on 1 March 2020. During the first month of the outbreak, 2,641 cases of COVID-19 led to 1,832 hospital admissions, 207 intensive care admissions and 126 deaths. We aimed to identify the source and number of introductions of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) into Scotland using a combined phylogenetic and epidemiological approach. Sequencing of 1,314 SARS-CoV-2 viral genomes from available patient samples enabled us to estimate that SARS-CoV-2 was introduced to Scotland on at least 283 occasions during February and March 2020. Epidemiological analysis confirmed that early introductions of SARS-CoV-2 originated from mainland Europe (the majority from Italy and Spain). We identified subsequent early outbreaks in the community, within healthcare facilities and at an international conference. Community transmission occurred after 2 March, 3 weeks before control measures were introduced. Earlier travel restrictions or quarantine measures, both locally and internationally, would have reduced the number of COVID-19 cases in Scotland. The risk of multiple reintroduction events in future waves of infection remains high in the absence of population immunity.

KW - SARS-CoV-2

KW - Viral epidemiology

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DO - 10.1038/s41564-020-00838-z

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SN - 2058-5276

VL - 6

SP - 112

EP - 122

JO - Nature Microbiology

JF - Nature Microbiology

IS - 1

ER -

Genomic epidemiology reveals multiple introductions of SARS-CoV-2 from mainland Europe into Scotland

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Keywords

ASJC Scopus subject areas

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Author Correction: Genomic epidemiology reveals multiple introductions of SARS-CoV-2 from mainland Europe into Scotland (Nature Microbiology, (2021), 6, 1, (112-122), 10.1038/s41564-020-00838-z)

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