Whole-genome sequencing to delineate Mycobacterium tuberculosis outbreaks: a retrospective observational study

Tuberculosis incidence in the UK has risen in the past decade. Disease control depends on epidemiological data, which can be difficult to obtain. Whole-genome sequencing can detect microevolution within Mycobacterium tuberculosis strains. We aimed to estimate the genetic diversity of related M tuber...

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Veröffentlicht in:The Lancet infectious diseases Jg. 13; H. 2; S. 137 - 146
Hauptverfasser: Walker, Timothy M, Ip, Camilla LC, Harrell, Ruth H, Evans, Jason T, Kapatai, Georgia, Dedicoat, Martin J, Eyre, David W, Wilson, Daniel J, Hawkey, Peter M, Crook, Derrick W, Parkhill, Julian, Harris, David, Walker, A Sarah, Bowden, Rory, Monk, Philip, Smith, E Grace, Peto, Tim EA
Format: Journal Article
Sprache:Englisch
Veröffentlicht: London Elsevier Ltd 01.02.2013
Lancet Publishing Group
Elsevier Limited
Elsevier Science ;, The Lancet Pub. Group
Schlagworte:
Bacterial diseases
Biological and medical sciences
Cluster Analysis
Community-Acquired Infections - epidemiology
Community-Acquired Infections - microbiology
Confidence Intervals
Cross-Sectional Studies
Deoxyribonucleic acid
Disease control
Disease Outbreaks - classification
DNA
Genetic diversity
Genetic Linkage
Genome, Bacterial - genetics
Households
Human bacterial diseases
Humans
Infectious Disease
Infectious diseases
Longitudinal Studies
Medical research
Medical sciences
Mutation Rate
Mycobacterium tuberculosis
Mycobacterium tuberculosis - genetics
Observational studies
Outbreaks
Polymorphism, Single Nucleotide
Retrospective Studies
Sequence Analysis, DNA
Tandem Repeat Sequences
Tuberculosis
Tuberculosis and atypical mycobacterial infections
Tuberculosis, Pulmonary - epidemiology
Tuberculosis, Pulmonary - microbiology
Tuberculosis, Pulmonary - transmission
United Kingdom - epidemiology
United Kingdom
Europe
British Isles
Epidemic
Nucleotide sequence
Mycobacterial infection
Epidemiology
Infection
Tuberculosis
Mycobacterium tuberculosis
Mycobacteriales
Bacteriosis
Mycobacteriaceae
Bacteria
Actinomycetes
Genome
Sequencing
ISSN:1473-3099, 1474-4457, 1474-4457
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Abstract Tuberculosis incidence in the UK has risen in the past decade. Disease control depends on epidemiological data, which can be difficult to obtain. Whole-genome sequencing can detect microevolution within Mycobacterium tuberculosis strains. We aimed to estimate the genetic diversity of related M tuberculosis strains in the UK Midlands and to investigate how this measurement might be used to investigate community outbreaks. In a retrospective observational study, we used Illumina technology to sequence M tuberculosis genomes from an archive of frozen cultures. We characterised isolates into four groups: cross-sectional, longitudinal, household, and community. We measured pairwise nucleotide differences within hosts and between hosts in household outbreaks and estimated the rate of change in DNA sequences. We used the findings to interpret network diagrams constructed from 11 community clusters derived from mycobacterial interspersed repetitive-unit–variable-number tandem-repeat data. We sequenced 390 separate isolates from 254 patients, including representatives from all five major lineages of M tuberculosis. The estimated rate of change in DNA sequences was 0·5 single nucleotide polymorphisms (SNPs) per genome per year (95% CI 0·3–0·7) in longitudinal isolates from 30 individuals and 25 families. Divergence is rarely higher than five SNPs in 3 years. 109 (96%) of 114 paired isolates from individuals and households differed by five or fewer SNPs. More than five SNPs separated isolates from none of 69 epidemiologically linked patients, two (15%) of 13 possibly linked patients, and 13 (17%) of 75 epidemiologically unlinked patients (three-way comparison exact p<0·0001). Genetic trees and clinical and epidemiological data suggest that super-spreaders were present in two community clusters. Whole-genome sequencing can delineate outbreaks of tuberculosis and allows inference about direction of transmission between cases. The technique could identify super-spreaders and predict the existence of undiagnosed cases, potentially leading to early treatment of infectious patients and their contacts. Medical Research Council, Wellcome Trust, National Institute for Health Research, and the Health Protection Agency.
AbstractList Tuberculosis incidence in the UK has risen in the past decade. Disease control depends on epidemiological data, which can be difficult to obtain. Whole-genome sequencing can detect microevolution within Mycobacterium tuberculosis strains. We aimed to estimate the genetic diversity of related M tuberculosis strains in the UK Midlands and to investigate how this measurement might be used to investigate community outbreaks. In a retrospective observational study, we used Illumina technology to sequence M tuberculosis genomes from an archive of frozen cultures. We characterised isolates into four groups: cross-sectional, longitudinal, household, and community. We measured pairwise nucleotide differences within hosts and between hosts in household outbreaks and estimated the rate of change in DNA sequences. We used the findings to interpret network diagrams constructed from 11 community clusters derived from mycobacterial interspersed repetitive-unit-variable-number tandem-repeat data. We sequenced 390 separate isolates from 254 patients, including representatives from all five major lineages of M tuberculosis. The estimated rate of change in DNA sequences was 0.5 single nucleotide polymorphisms (SNPs) per genome per year (95% CI 0.3-0.7) in longitudinal isolates from 30 individuals and 25 families. Divergence is rarely higher than five SNPs in 3 years. 109 (96%) of 114 paired isolates from individuals and households differed by five or fewer SNPs. More than five SNPs separated isolates from none of 69 epidemiologically linked patients, two (15%) of 13 possibly linked patients, and 13 (17%) of 75 epidemiologically unlinked patients (three-way comparison exact p<0.0001). Genetic trees and clinical and epidemiological data suggest that super-spreaders were present in two community clusters. Whole-genome sequencing can delineate outbreaks of tuberculosis and allows inference about direction of transmission between cases. The technique could identify super-spreaders and predict the existence of undiagnosed cases, potentially leading to early treatment of infectious patients and their contacts. Medical Research Council, Wellcome Trust, National Institute for Health Research, and the Health Protection Agency.
Tuberculosis incidence in the UK has risen in the past decade. Disease control depends on epidemiological data, which can be difficult to obtain. Whole-genome sequencing can detect microevolution within Mycobacterium tuberculosis strains. We aimed to estimate the genetic diversity of related M tuberculosis strains in the UK Midlands and to investigate how this measurement might be used to investigate community outbreaks. Methods: In a retrospective observational study, we used Illumina technology to sequence M tuberculosis genomes from an archive of frozen cultures. We characterised isolates into four groups: cross-sectional, longitudinal, household, and community. We measured pairwise nucleotide differences within hosts and between hosts in household outbreaks and estimated the rate of change in DNA sequences. We used the findings to interpret network diagrams constructed from 11 community clusters derived from mycobacterial interspersed repetitive-unitavariable-number tandem-repeat data.
Summary Background Tuberculosis incidence in the UK has risen in the past decade. Disease control depends on epidemiological data, which can be difficult to obtain. Whole-genome sequencing can detect microevolution within Mycobacterium tuberculosis strains. We aimed to estimate the genetic diversity of related M tuberculosis strains in the UK Midlands and to investigate how this measurement might be used to investigate community outbreaks. Methods In a retrospective observational study, we used Illumina technology to sequence M tuberculosis genomes from an archive of frozen cultures. We characterised isolates into four groups: cross-sectional, longitudinal, household, and community. We measured pairwise nucleotide differences within hosts and between hosts in household outbreaks and estimated the rate of change in DNA sequences. We used the findings to interpret network diagrams constructed from 11 community clusters derived from mycobacterial interspersed repetitive-unit–variable-number tandem-repeat data. Findings We sequenced 390 separate isolates from 254 patients, including representatives from all five major lineages of M tuberculosis . The estimated rate of change in DNA sequences was 0·5 single nucleotide polymorphisms (SNPs) per genome per year (95% CI 0·3–0·7) in longitudinal isolates from 30 individuals and 25 families. Divergence is rarely higher than five SNPs in 3 years. 109 (96%) of 114 paired isolates from individuals and households differed by five or fewer SNPs. More than five SNPs separated isolates from none of 69 epidemiologically linked patients, two (15%) of 13 possibly linked patients, and 13 (17%) of 75 epidemiologically unlinked patients (three-way comparison exact p<0·0001). Genetic trees and clinical and epidemiological data suggest that super-spreaders were present in two community clusters. Interpretation Whole-genome sequencing can delineate outbreaks of tuberculosis and allows inference about direction of transmission between cases. The technique could identify super-spreaders and predict the existence of undiagnosed cases, potentially leading to early treatment of infectious patients and their contacts. Funding Medical Research Council, Wellcome Trust, National Institute for Health Research, and the Health Protection Agency.
Tuberculosis incidence in the UK has risen in the past decade. Disease control depends on epidemiological data, which can be difficult to obtain. Whole-genome sequencing can detect microevolution within Mycobacterium tuberculosis strains. We aimed to estimate the genetic diversity of related M tuberculosis strains in the UK Midlands and to investigate how this measurement might be used to investigate community outbreaks. In a retrospective observational study, we used Illumina technology to sequence M tuberculosis genomes from an archive of frozen cultures. We characterised isolates into four groups: cross-sectional, longitudinal, household, and community. We measured pairwise nucleotide differences within hosts and between hosts in household outbreaks and estimated the rate of change in DNA sequences. We used the findings to interpret network diagrams constructed from 11 community clusters derived from mycobacterial interspersed repetitive-unit–variable-number tandem-repeat data. We sequenced 390 separate isolates from 254 patients, including representatives from all five major lineages of M tuberculosis. The estimated rate of change in DNA sequences was 0·5 single nucleotide polymorphisms (SNPs) per genome per year (95% CI 0·3–0·7) in longitudinal isolates from 30 individuals and 25 families. Divergence is rarely higher than five SNPs in 3 years. 109 (96%) of 114 paired isolates from individuals and households differed by five or fewer SNPs. More than five SNPs separated isolates from none of 69 epidemiologically linked patients, two (15%) of 13 possibly linked patients, and 13 (17%) of 75 epidemiologically unlinked patients (three-way comparison exact p<0·0001). Genetic trees and clinical and epidemiological data suggest that super-spreaders were present in two community clusters. Whole-genome sequencing can delineate outbreaks of tuberculosis and allows inference about direction of transmission between cases. The technique could identify super-spreaders and predict the existence of undiagnosed cases, potentially leading to early treatment of infectious patients and their contacts. Medical Research Council, Wellcome Trust, National Institute for Health Research, and the Health Protection Agency.
Background Tuberculosis incidence in the UK has risen in the past decade. Disease control depends on epidemiological data, which can be difficult to obtain. Whole-genome sequencing can detect microevolution withinMycobacterium tuberculosisstrains. We aimed to estimate the genetic diversity of relatedM tuberculosisstrains in the UK Midlands and to investigate how this measurement might be used to investigate community outbreaks. Methods In a retrospective observational study, we used Illumina technology to sequenceM tuberculosisgenomes from an archive of frozen cultures. We characterised isolates into four groups: cross-sectional, longitudinal, household, and community. We measured pairwise nucleotide differences within hosts and between hosts in household outbreaks and estimated the rate of change in DNA sequences. We used the findings to interpret network diagrams constructed from 11 community clusters derived from mycobacterial interspersed repetitive-unit-variable-number tandem-repeat data. Findings We sequenced 390 separate isolates from 254 patients, including representatives from all five major lineages ofM tuberculosis. The estimated rate of change in DNA sequences was 0·5 single nucleotide polymorphisms (SNPs) per genome per year (95% CI 0·3-0·7) in longitudinal isolates from 30 individuals and 25 families. Divergence is rarely higher than five SNPs in 3 years. 109 (96%) of 114 paired isolates from individuals and households differed by five or fewer SNPs. More than five SNPs separated isolates from none of 69 epidemiologically linked patients, two (15%) of 13 possibly linked patients, and 13 (17%) of 75 epidemiologically unlinked patients (three-way comparison exact p<0·0001). Genetic trees and clinical and epidemiological data suggest that super-spreaders were present in two community clusters. Interpretation Whole-genome sequencing can delineate outbreaks of tuberculosis and allows inference about direction of transmission between cases. The technique could identify super-spreaders and predict the existence of undiagnosed cases, potentially leading to early treatment of infectious patients and their contacts. Funding Medical Research Council, Wellcome Trust, National Institute for Health Research, and the Health Protection Agency.
Tuberculosis incidence in the UK has risen in the past decade. Disease control depends on epidemiological data, which can be difficult to obtain. Whole-genome sequencing can detect microevolution within Mycobacterium tuberculosis strains. We aimed to estimate the genetic diversity of related M tuberculosis strains in the UK Midlands and to investigate how this measurement might be used to investigate community outbreaks.BACKGROUNDTuberculosis incidence in the UK has risen in the past decade. Disease control depends on epidemiological data, which can be difficult to obtain. Whole-genome sequencing can detect microevolution within Mycobacterium tuberculosis strains. We aimed to estimate the genetic diversity of related M tuberculosis strains in the UK Midlands and to investigate how this measurement might be used to investigate community outbreaks.In a retrospective observational study, we used Illumina technology to sequence M tuberculosis genomes from an archive of frozen cultures. We characterised isolates into four groups: cross-sectional, longitudinal, household, and community. We measured pairwise nucleotide differences within hosts and between hosts in household outbreaks and estimated the rate of change in DNA sequences. We used the findings to interpret network diagrams constructed from 11 community clusters derived from mycobacterial interspersed repetitive-unit-variable-number tandem-repeat data.METHODSIn a retrospective observational study, we used Illumina technology to sequence M tuberculosis genomes from an archive of frozen cultures. We characterised isolates into four groups: cross-sectional, longitudinal, household, and community. We measured pairwise nucleotide differences within hosts and between hosts in household outbreaks and estimated the rate of change in DNA sequences. We used the findings to interpret network diagrams constructed from 11 community clusters derived from mycobacterial interspersed repetitive-unit-variable-number tandem-repeat data.We sequenced 390 separate isolates from 254 patients, including representatives from all five major lineages of M tuberculosis. The estimated rate of change in DNA sequences was 0.5 single nucleotide polymorphisms (SNPs) per genome per year (95% CI 0.3-0.7) in longitudinal isolates from 30 individuals and 25 families. Divergence is rarely higher than five SNPs in 3 years. 109 (96%) of 114 paired isolates from individuals and households differed by five or fewer SNPs. More than five SNPs separated isolates from none of 69 epidemiologically linked patients, two (15%) of 13 possibly linked patients, and 13 (17%) of 75 epidemiologically unlinked patients (three-way comparison exact p<0.0001). Genetic trees and clinical and epidemiological data suggest that super-spreaders were present in two community clusters.FINDINGSWe sequenced 390 separate isolates from 254 patients, including representatives from all five major lineages of M tuberculosis. The estimated rate of change in DNA sequences was 0.5 single nucleotide polymorphisms (SNPs) per genome per year (95% CI 0.3-0.7) in longitudinal isolates from 30 individuals and 25 families. Divergence is rarely higher than five SNPs in 3 years. 109 (96%) of 114 paired isolates from individuals and households differed by five or fewer SNPs. More than five SNPs separated isolates from none of 69 epidemiologically linked patients, two (15%) of 13 possibly linked patients, and 13 (17%) of 75 epidemiologically unlinked patients (three-way comparison exact p<0.0001). Genetic trees and clinical and epidemiological data suggest that super-spreaders were present in two community clusters.Whole-genome sequencing can delineate outbreaks of tuberculosis and allows inference about direction of transmission between cases. The technique could identify super-spreaders and predict the existence of undiagnosed cases, potentially leading to early treatment of infectious patients and their contacts.INTERPRETATIONWhole-genome sequencing can delineate outbreaks of tuberculosis and allows inference about direction of transmission between cases. The technique could identify super-spreaders and predict the existence of undiagnosed cases, potentially leading to early treatment of infectious patients and their contacts.Medical Research Council, Wellcome Trust, National Institute for Health Research, and the Health Protection Agency.FUNDINGMedical Research Council, Wellcome Trust, National Institute for Health Research, and the Health Protection Agency.
Author Bowden, Rory
Ip, Camilla LC
Evans, Jason T
Harrell, Ruth H
Walker, A Sarah
Parkhill, Julian
Eyre, David W
Walker, Timothy M
Smith, E Grace
Kapatai, Georgia
Crook, Derrick W
Peto, Tim EA
Dedicoat, Martin J
Wilson, Daniel J
Harris, David
Hawkey, Peter M
Monk, Philip
Author_xml – sequence: 1
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  surname: Walker
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  email: timothy.walker@ndm.ox.ac.uk
  organization: Nuffield Department of Medicine, John Radcliffe Hospital, University of Oxford, Oxford, UK
– sequence: 2
  givenname: Camilla LC
  surname: Ip
  fullname: Ip, Camilla LC
  organization: Department of Statistics, University of Oxford, Oxford, UK
– sequence: 3
  givenname: Ruth H
  surname: Harrell
  fullname: Harrell, Ruth H
  organization: West Midlands Public Health Laboratory, Health Protection Agency, Heart of England NHS Foundation Trust, Birmingham, UK
– sequence: 4
  givenname: Jason T
  surname: Evans
  fullname: Evans, Jason T
  organization: West Midlands Public Health Laboratory, Health Protection Agency, Heart of England NHS Foundation Trust, Birmingham, UK
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  surname: Kapatai
  fullname: Kapatai, Georgia
  organization: West Midlands Public Health Laboratory, Health Protection Agency, Heart of England NHS Foundation Trust, Birmingham, UK
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  surname: Dedicoat
  fullname: Dedicoat, Martin J
  organization: Heartlands Hospital and Birmingham Chest Clinic, Heart of England NHS Foundation Trust, Birmingham, UK
– sequence: 7
  givenname: David W
  surname: Eyre
  fullname: Eyre, David W
  organization: Nuffield Department of Medicine, John Radcliffe Hospital, University of Oxford, Oxford, UK
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  givenname: Daniel J
  surname: Wilson
  fullname: Wilson, Daniel J
  organization: Nuffield Department of Medicine, John Radcliffe Hospital, University of Oxford, Oxford, UK
– sequence: 9
  givenname: Peter M
  surname: Hawkey
  fullname: Hawkey, Peter M
  organization: West Midlands Public Health Laboratory, Health Protection Agency, Heart of England NHS Foundation Trust, Birmingham, UK
– sequence: 10
  givenname: Derrick W
  surname: Crook
  fullname: Crook, Derrick W
  organization: Nuffield Department of Medicine, John Radcliffe Hospital, University of Oxford, Oxford, UK
– sequence: 11
  givenname: Julian
  surname: Parkhill
  fullname: Parkhill, Julian
  organization: Wellcome Trust Sanger Institute, Genome Campus, Hinxton, Cambridge, UK
– sequence: 12
  givenname: David
  surname: Harris
  fullname: Harris, David
  organization: Wellcome Trust Sanger Institute, Genome Campus, Hinxton, Cambridge, UK
– sequence: 13
  givenname: A Sarah
  surname: Walker
  fullname: Walker, A Sarah
  organization: Nuffield Department of Medicine, John Radcliffe Hospital, University of Oxford, Oxford, UK
– sequence: 14
  givenname: Rory
  surname: Bowden
  fullname: Bowden, Rory
  organization: Department of Statistics, University of Oxford, Oxford, UK
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  givenname: Philip
  surname: Monk
  fullname: Monk, Philip
  organization: Health Protection Agency, County Hall, Glenfield, Leicester, UK
– sequence: 16
  givenname: E Grace
  surname: Smith
  fullname: Smith, E Grace
  organization: West Midlands Public Health Laboratory, Health Protection Agency, Heart of England NHS Foundation Trust, Birmingham, UK
– sequence: 17
  givenname: Tim EA
  surname: Peto
  fullname: Peto, Tim EA
  organization: Nuffield Department of Medicine, John Radcliffe Hospital, University of Oxford, Oxford, UK
BackLink http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=26902745$$DView record in Pascal Francis
https://www.ncbi.nlm.nih.gov/pubmed/23158499$$D View this record in MEDLINE/PubMed
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Issue 2
Keywords Epidemic
Nucleotide sequence
Mycobacterial infection
Epidemiology
Infection
Tuberculosis
Mycobacterium tuberculosis
Mycobacteriales
Bacteriosis
Mycobacteriaceae
Bacteria
Actinomycetes
Genome
Sequencing
Language English
License http://creativecommons.org/licenses/by/4.0
CC BY 4.0
Copyright © 2013 Elsevier Ltd. All rights reserved.
This work is licensed under a Creative Commons Attribution 4.0 International License, which allows reusers to distribute, remix, adapt, and build upon the material in any medium or format, so long as attribution is given to the creator. The license allows for commercial use.
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ObjectType-Feature-2
content type line 14
content type line 23
ObjectType-Article-2
ObjectType-Feature-1
These authors also contributed equally
These authors contributed equally
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PublicationTitle The Lancet infectious diseases
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Snippet Tuberculosis incidence in the UK has risen in the past decade. Disease control depends on epidemiological data, which can be difficult to obtain. Whole-genome...
Summary Background Tuberculosis incidence in the UK has risen in the past decade. Disease control depends on epidemiological data, which can be difficult to...
Background Tuberculosis incidence in the UK has risen in the past decade. Disease control depends on epidemiological data, which can be difficult to obtain....
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StartPage 137
SubjectTerms Bacterial diseases
Biological and medical sciences
Cluster Analysis
Community-Acquired Infections - epidemiology
Community-Acquired Infections - microbiology
Confidence Intervals
Cross-Sectional Studies
Deoxyribonucleic acid
Disease control
Disease Outbreaks - classification
DNA
Genetic diversity
Genetic Linkage
Genome, Bacterial - genetics
Households
Human bacterial diseases
Humans
Infectious Disease
Infectious diseases
Longitudinal Studies
Medical research
Medical sciences
Mutation Rate
Mycobacterium tuberculosis
Mycobacterium tuberculosis - genetics
Observational studies
Outbreaks
Polymorphism, Single Nucleotide
Retrospective Studies
Sequence Analysis, DNA
Tandem Repeat Sequences
Tuberculosis
Tuberculosis and atypical mycobacterial infections
Tuberculosis, Pulmonary - epidemiology
Tuberculosis, Pulmonary - microbiology
Tuberculosis, Pulmonary - transmission
United Kingdom - epidemiology
Title Whole-genome sequencing to delineate Mycobacterium tuberculosis outbreaks: a retrospective observational study
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https://dx.doi.org/10.1016/S1473-3099(12)70277-3
https://www.ncbi.nlm.nih.gov/pubmed/23158499
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Volume 13
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