Genomics-informed responses in the elimination of COVID-19 in Victoria, Australia: an observational, genomic epidemiological study.


Journal

The Lancet. Public health
ISSN: 2468-2667
Titre abrégé: Lancet Public Health
Pays: England
ID NLM: 101699003

Informations de publication

Date de publication:
08 2021
Historique:
received: 01 05 2021
revised: 26 05 2021
accepted: 01 06 2021
pubmed: 13 7 2021
medline: 5 8 2021
entrez: 12 7 2021
Statut: ppublish

Résumé

A cornerstone of Australia's ability to control COVID-19 has been effective border control with an extensive supervised quarantine programme. However, a rapid recrudescence of COVID-19 was observed in the state of Victoria in June, 2020. We aim to describe the genomic findings that located the source of this second wave and show the role of genomic epidemiology in the successful elimination of COVID-19 for a second time in Australia. In this observational, genomic epidemiological study, we did genomic sequencing of all laboratory-confirmed cases of COVID-19 diagnosed in Victoria, Australia between Jan 25, 2020, and Jan 31, 2021. We did phylogenetic analyses, genomic cluster discovery, and integrated results with epidemiological data (detailed information on demographics, risk factors, and exposure) collected via interview by the Victorian Government Department of Health. Genomic transmission networks were used to group multiple genomic clusters when epidemiological and genomic data suggested they arose from a single importation event and diversified within Victoria. To identify transmission of emergent lineages between Victoria and other states or territories in Australia, all publicly available SARS-CoV-2 sequences uploaded before Feb 11, 2021, were obtained from the national sequence sharing programme AusTrakka, and epidemiological data were obtained from the submitting laboratories. We did phylodynamic analyses to estimate the growth rate, doubling time, and number of days from the first local infection to the collection of the first sequenced genome for the dominant local cluster, and compared our growth estimates to previously published estimates from a similar growth phase of lineage B.1.1.7 (also known as the Alpha variant) in the UK. Between Jan 25, 2020, and Jan 31, 2021, there were 20 451 laboratory-confirmed cases of COVID-19 in Victoria, Australia, of which 15 431 were submitted for sequencing, and 11 711 met all quality control metrics and were included in our analysis. We identified 595 genomic clusters, with a median of five cases per cluster (IQR 2-11). Overall, samples from 11 503 (98·2%) of 11 711 cases clustered with another sample in Victoria, either within a genomic cluster or transmission network. Genomic analysis revealed that 10 426 cases, including 10 416 (98·4%) of 10 584 locally acquired cases, diagnosed during the second wave (between June and October, 2020) were derived from a single incursion from hotel quarantine, with the outbreak lineage (transmission network G, lineage D.2) rapidly detected in other Australian states and territories. Phylodynamic analyses indicated that the epidemic growth rate of the outbreak lineage in Victoria during the initial growth phase (samples collected between June 4 and July 9, 2020; 47·4 putative transmission events, per branch, per year [1/years; 95% credible interval 26·0-85·0]), was similar to that of other reported variants, such as B.1.1.7 in the UK (mean approximately 71·5 1/years). Strict interventions were implemented, and the outbreak lineage has not been detected in Australia since Oct 29, 2020. Subsequent cases represented independent international or interstate introductions, with limited local spread. Our study highlights how rapid escalation of clonal outbreaks can occur from a single incursion. However, strict quarantine measures and decisive public health responses to emergent cases are effective, even with high epidemic growth rates. Real-time genomic surveillance can alter the way in which public health agencies view and respond to COVID-19 outbreaks. The Victorian Government, the National Health and Medical Research Council Australia, and the Medical Research Future Fund.

Sections du résumé

BACKGROUND
A cornerstone of Australia's ability to control COVID-19 has been effective border control with an extensive supervised quarantine programme. However, a rapid recrudescence of COVID-19 was observed in the state of Victoria in June, 2020. We aim to describe the genomic findings that located the source of this second wave and show the role of genomic epidemiology in the successful elimination of COVID-19 for a second time in Australia.
METHODS
In this observational, genomic epidemiological study, we did genomic sequencing of all laboratory-confirmed cases of COVID-19 diagnosed in Victoria, Australia between Jan 25, 2020, and Jan 31, 2021. We did phylogenetic analyses, genomic cluster discovery, and integrated results with epidemiological data (detailed information on demographics, risk factors, and exposure) collected via interview by the Victorian Government Department of Health. Genomic transmission networks were used to group multiple genomic clusters when epidemiological and genomic data suggested they arose from a single importation event and diversified within Victoria. To identify transmission of emergent lineages between Victoria and other states or territories in Australia, all publicly available SARS-CoV-2 sequences uploaded before Feb 11, 2021, were obtained from the national sequence sharing programme AusTrakka, and epidemiological data were obtained from the submitting laboratories. We did phylodynamic analyses to estimate the growth rate, doubling time, and number of days from the first local infection to the collection of the first sequenced genome for the dominant local cluster, and compared our growth estimates to previously published estimates from a similar growth phase of lineage B.1.1.7 (also known as the Alpha variant) in the UK.
FINDINGS
Between Jan 25, 2020, and Jan 31, 2021, there were 20 451 laboratory-confirmed cases of COVID-19 in Victoria, Australia, of which 15 431 were submitted for sequencing, and 11 711 met all quality control metrics and were included in our analysis. We identified 595 genomic clusters, with a median of five cases per cluster (IQR 2-11). Overall, samples from 11 503 (98·2%) of 11 711 cases clustered with another sample in Victoria, either within a genomic cluster or transmission network. Genomic analysis revealed that 10 426 cases, including 10 416 (98·4%) of 10 584 locally acquired cases, diagnosed during the second wave (between June and October, 2020) were derived from a single incursion from hotel quarantine, with the outbreak lineage (transmission network G, lineage D.2) rapidly detected in other Australian states and territories. Phylodynamic analyses indicated that the epidemic growth rate of the outbreak lineage in Victoria during the initial growth phase (samples collected between June 4 and July 9, 2020; 47·4 putative transmission events, per branch, per year [1/years; 95% credible interval 26·0-85·0]), was similar to that of other reported variants, such as B.1.1.7 in the UK (mean approximately 71·5 1/years). Strict interventions were implemented, and the outbreak lineage has not been detected in Australia since Oct 29, 2020. Subsequent cases represented independent international or interstate introductions, with limited local spread.
INTERPRETATION
Our study highlights how rapid escalation of clonal outbreaks can occur from a single incursion. However, strict quarantine measures and decisive public health responses to emergent cases are effective, even with high epidemic growth rates. Real-time genomic surveillance can alter the way in which public health agencies view and respond to COVID-19 outbreaks.
FUNDING
The Victorian Government, the National Health and Medical Research Council Australia, and the Medical Research Future Fund.

Identifiants

pubmed: 34252365
pii: S2468-2667(21)00133-X
doi: 10.1016/S2468-2667(21)00133-X
pmc: PMC8270762
pii:
doi:

Types de publication

Journal Article Observational Study Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e547-e556

Commentaires et corrections

Type : ErratumIn

Informations de copyright

Copyright © 2021 The Author(s). Published by Elsevier Ltd. This is an Open Access article under the CC BY-NC-ND 4.0 license. Published by Elsevier Ltd.. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests All authors declare no competing interests.

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Auteurs

Courtney R Lane (CR)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia.

Norelle L Sherry (NL)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia.

Ashleigh F Porter (AF)

Department of Microbiology and Immunology, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia.

Sebastian Duchene (S)

Department of Microbiology and Immunology, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia.

Kristy Horan (K)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia.

Patiyan Andersson (P)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia.

Mathilda Wilmot (M)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia.

Annabelle Turner (A)

Victorian Department of Health, Melbourne, VIC, Australia.

Sally Dougall (S)

Victorian Department of Health, Melbourne, VIC, Australia.

Sandra A Johnson (SA)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia.

Michelle Sait (M)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia.

Anders Gonçalves da Silva (A)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia; Doherty Applied Microbial Genomics, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia.

Susan A Ballard (SA)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia.

Tuyet Hoang (T)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia.

Timothy P Stinear (TP)

Doherty Applied Microbial Genomics, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia; Department of Microbiology and Immunology, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia.

Leon Caly (L)

Victorian Infectious Diseases Reference Laboratory, Royal Melbourne Hospital at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia.

Vitali Sintchenko (V)

Centre for Infectious Diseases and Microbiology Public Health, Westmead Hospital, Sydney, NSW, Australia; Sydney Medical School, The University of Sydney, Sydney, NSW, Australia.

Rikki Graham (R)

Public Health Microbiology, Forensic and Scientific Services, Queensland Department of Health, Brisbane, QLD, Australia.

Jamie McMahon (J)

Public Health Microbiology, Forensic and Scientific Services, Queensland Department of Health, Brisbane, QLD, Australia.

David Smith (D)

Department of Microbiology, PathWest Laboratory Medicine, QEII Medical Centre, Perth, WA, Australia; School of Medicine, University of Western Australia, Perth, WA, Australia.

Lex Ex Leong (LE)

Public Health Laboratory, Microbiology and Infectious Diseases, SA Pathology, Adelaide, SA, Australia.

Ella M Meumann (EM)

Territory Pathology, Royal Darwin Hospital, Darwin, NT, Australia; Global and Tropical Health Division, Menzies School of Health Research, Charles Darwin University, Darwin, NT, Australia.

Louise Cooley (L)

Royal Hobart Hospital, Hobart, TAS, Australia; School of Medicine, University of Tasmania, Hobart, TAS, Australia.

Benjamin Schwessinger (B)

Research Biology School, Australian National University, Canberra, ACT, Australia.

William Rawlinson (W)

Virology Research Laboratory, Serology and Virology Division, NSW Health Pathology, Prince of Wales Hospital, Sydney, NSW, Australia.

Sebastiaan J van Hal (SJ)

Department of Infectious Disease and Microbiology, Royal Prince Alfred Hospital, Sydney, NSW, Australia.

Nicola Stephens (N)

School of Medicine, University of Tasmania, Hobart, TAS, Australia.

Mike Catton (M)

Victorian Infectious Diseases Reference Laboratory, Royal Melbourne Hospital at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia.

Clare Looker (C)

Victorian Department of Health, Melbourne, VIC, Australia.

Simon Crouch (S)

Victorian Department of Health, Melbourne, VIC, Australia.

Brett Sutton (B)

Victorian Department of Health, Melbourne, VIC, Australia.

Charles Alpren (C)

Victorian Department of Health, Melbourne, VIC, Australia.

Deborah A Williamson (DA)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia; Department of Microbiology and Immunology, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia; Victorian Infectious Diseases Reference Laboratory, Royal Melbourne Hospital at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia; Department of Microbiology, Royal Melbourne Hospital, Melbourne, VIC, Australia.

Torsten Seemann (T)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia; Doherty Applied Microbial Genomics, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia.

Benjamin P Howden (BP)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia; Doherty Applied Microbial Genomics, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia; Department of Microbiology and Immunology, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia. Electronic address: bhowden@unimelb.edu.au.

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