Public health surveillance of multidrug-resistant clones of Neisseria gonorrhoeae in Europe: a genomic survey

<h4>Background</h4> <p>Traditional methods for molecular epidemiology of Neisseria gonorrhoeae are suboptimal. Whole-genome sequencing (WGS) offers ideal resolution to describe population dynamics and to predict and infer transmission of antimicrobial resistance, and can enhance i...

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Main Authors: Harris, SR, Cole, MJ, Spiteri, G, Sánchez-Busó, L, Golparian, D, Jacobsson, S, Goater, R, Abudahab, K, Yeats, CA, Bercot, B, Borrego, MJ, Crowley, B, Stefanelli, P, Tripodo, F, Abad, R, Aanensen, DM, Unemo, M, Euro-Gasp Study Group
Format: Journal article
Language:English
Published: Elsevier 2018
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author Harris, SR
Cole, MJ
Spiteri, G
Sánchez-Busó, L
Golparian, D
Jacobsson, S
Goater, R
Abudahab, K
Yeats, CA
Bercot, B
Borrego, MJ
Crowley, B
Stefanelli, P
Tripodo, F
Abad, R
Aanensen, DM
Unemo, M
Euro-Gasp Study Group,
author_facet Harris, SR
Cole, MJ
Spiteri, G
Sánchez-Busó, L
Golparian, D
Jacobsson, S
Goater, R
Abudahab, K
Yeats, CA
Bercot, B
Borrego, MJ
Crowley, B
Stefanelli, P
Tripodo, F
Abad, R
Aanensen, DM
Unemo, M
Euro-Gasp Study Group,
author_sort Harris, SR
collection OXFORD
description <h4>Background</h4> <p>Traditional methods for molecular epidemiology of Neisseria gonorrhoeae are suboptimal. Whole-genome sequencing (WGS) offers ideal resolution to describe population dynamics and to predict and infer transmission of antimicrobial resistance, and can enhance infection control through linkage with epidemiological data. We used WGS, in conjunction with linked epidemiological and phenotypic data, to describe the gonococcal population in 20 European countries. We aimed to detail changes in phenotypic antimicrobial resistance levels (and the reasons for these changes) and strain distribution (with a focus on antimicrobial resistance strains in risk groups), and to predict antimicrobial resistance from WGS data.</p> <h4>Methods</h4> <p>We carried out an observational study, in which we sequenced isolates taken from patients with gonorrhoea from the European Gonococcal Antimicrobial Surveillance Programme in 20 countries from September to November, 2013. We also developed a web platform that we used for automated antimicrobial resistance prediction, molecular typing (N gonorrhoeae multi-antigen sequence typing [NG-MAST] and multilocus sequence typing), and phylogenetic clustering in conjunction with epidemiological and phenotypic data.</p> <h4>Findings</h4> <p>The multidrug-resistant NG-MAST genogroup G1407 was predominant and accounted for the most cephalosporin resistance, but the prevalence of this genogroup decreased from 248 (23%) of 1066 isolates in a previous study from 2009–10 to 174 (17%) of 1054 isolates in this survey in 2013. This genogroup previously showed an association with men who have sex with men, but changed to an association with heterosexual people (odds ratio=4·29). WGS provided substantially improved resolution and accuracy over NG-MAST and multilocus sequence typing, predicted antimicrobial resistance relatively well, and identified discrepant isolates, mixed infections or contaminants, and multidrug-resistant clades linked to risk groups.</p> <h4>Interpretation</h4> <p>To our knowledge, we provide the first use of joint analysis of WGS and epidemiological data in an international programme for regional surveillance of sexually transmitted infections. WGS provided enhanced understanding of the distribution of antimicrobial resistance clones, including replacement with clones that were more susceptible to antimicrobials, in several risk groups nationally and regionally. We provide a framework for genomic surveillance of gonococci through standardised sampling, use of WGS, and a shared information architecture for interpretation and dissemination by use of open access software.</p>
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spelling oxford-uuid:7895e3b1-c73e-471d-b4a3-fc4c0fe1be6e2022-03-26T20:31:40ZPublic health surveillance of multidrug-resistant clones of Neisseria gonorrhoeae in Europe: a genomic surveyJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:7895e3b1-c73e-471d-b4a3-fc4c0fe1be6eEnglishSymplectic Elements at OxfordElsevier2018Harris, SRCole, MJSpiteri, GSánchez-Busó, LGolparian, DJacobsson, SGoater, RAbudahab, KYeats, CABercot, BBorrego, MJCrowley, BStefanelli, PTripodo, FAbad, RAanensen, DMUnemo, MEuro-Gasp Study Group, <h4>Background</h4> <p>Traditional methods for molecular epidemiology of Neisseria gonorrhoeae are suboptimal. Whole-genome sequencing (WGS) offers ideal resolution to describe population dynamics and to predict and infer transmission of antimicrobial resistance, and can enhance infection control through linkage with epidemiological data. We used WGS, in conjunction with linked epidemiological and phenotypic data, to describe the gonococcal population in 20 European countries. We aimed to detail changes in phenotypic antimicrobial resistance levels (and the reasons for these changes) and strain distribution (with a focus on antimicrobial resistance strains in risk groups), and to predict antimicrobial resistance from WGS data.</p> <h4>Methods</h4> <p>We carried out an observational study, in which we sequenced isolates taken from patients with gonorrhoea from the European Gonococcal Antimicrobial Surveillance Programme in 20 countries from September to November, 2013. We also developed a web platform that we used for automated antimicrobial resistance prediction, molecular typing (N gonorrhoeae multi-antigen sequence typing [NG-MAST] and multilocus sequence typing), and phylogenetic clustering in conjunction with epidemiological and phenotypic data.</p> <h4>Findings</h4> <p>The multidrug-resistant NG-MAST genogroup G1407 was predominant and accounted for the most cephalosporin resistance, but the prevalence of this genogroup decreased from 248 (23%) of 1066 isolates in a previous study from 2009–10 to 174 (17%) of 1054 isolates in this survey in 2013. This genogroup previously showed an association with men who have sex with men, but changed to an association with heterosexual people (odds ratio=4·29). WGS provided substantially improved resolution and accuracy over NG-MAST and multilocus sequence typing, predicted antimicrobial resistance relatively well, and identified discrepant isolates, mixed infections or contaminants, and multidrug-resistant clades linked to risk groups.</p> <h4>Interpretation</h4> <p>To our knowledge, we provide the first use of joint analysis of WGS and epidemiological data in an international programme for regional surveillance of sexually transmitted infections. WGS provided enhanced understanding of the distribution of antimicrobial resistance clones, including replacement with clones that were more susceptible to antimicrobials, in several risk groups nationally and regionally. We provide a framework for genomic surveillance of gonococci through standardised sampling, use of WGS, and a shared information architecture for interpretation and dissemination by use of open access software.</p>
spellingShingle Harris, SR
Cole, MJ
Spiteri, G
Sánchez-Busó, L
Golparian, D
Jacobsson, S
Goater, R
Abudahab, K
Yeats, CA
Bercot, B
Borrego, MJ
Crowley, B
Stefanelli, P
Tripodo, F
Abad, R
Aanensen, DM
Unemo, M
Euro-Gasp Study Group,
Public health surveillance of multidrug-resistant clones of Neisseria gonorrhoeae in Europe: a genomic survey
title Public health surveillance of multidrug-resistant clones of Neisseria gonorrhoeae in Europe: a genomic survey
title_full Public health surveillance of multidrug-resistant clones of Neisseria gonorrhoeae in Europe: a genomic survey
title_fullStr Public health surveillance of multidrug-resistant clones of Neisseria gonorrhoeae in Europe: a genomic survey
title_full_unstemmed Public health surveillance of multidrug-resistant clones of Neisseria gonorrhoeae in Europe: a genomic survey
title_short Public health surveillance of multidrug-resistant clones of Neisseria gonorrhoeae in Europe: a genomic survey
title_sort public health surveillance of multidrug resistant clones of neisseria gonorrhoeae in europe a genomic survey
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