Outbreak of sexually transmitted, extensively drug-resistant Shigella sonnei in the UK, 2021–22: a descriptive epidemiological study

Outbreak Control Team

doi:10.1016/S1473-3099(22)00370-X

Outbreak of sexually transmitted, extensively drug-resistant Shigella sonnei in the UK, 2021–22: a descriptive epidemiological study

Outbreak Control Team

Research output: Contribution to journal › Article › peer-review

53 Citations (Scopus)

Abstract

Background: Shigellosis, traditionally a foodborne and waterborne infection, causes substantial morbidity globally. It is now a leading cause of sexually transmitted gastroenteritis among gay, bisexual, and other men who have sex with men (MSM). We describe an ongoing outbreak of extensively drug-resistant (XDR) Shigella sonnei in the UK. Methods: Routine laboratory surveillance (Second Generation Surveillance System, Gastrointestinal Data Warehouse) identified an exceedance of S sonnei clade 5 in England, first detected in September, 2021. Cases within this clade were subsequently reported from Scotland, Wales, and Northern Ireland. Confirmed cases in this outbreak were defined as individuals diagnosed with S sonnei clade 5 in the UK, with a specimen date between Sept 1, 2021, and Feb 9, 2022, who were genomically confirmed as part of a ten-single nucleotide polymorphism (SNP) linkage cluster. We used whole-genome sequencing with SNP typing to identify genomic clusters and antimicrobial-resistance determinants, analysing cases across the UK. We collected demographic, epidemiological, and clinical data from people infected with S sonnei clade 5 in England using questionnaires (standard and bespoke outbreak questionnaires). We used descriptive summary statistics to characterise cases. Findings: 72 cases (70 [97%] male, median age 34 years [IQR 27–39]) belonging to the ten-SNP single linkage cluster of S sonnei clade 5 were identified between Sept 4, 2021, and Feb 9, 2022. Isolates were predominantly XDR, with 66 (92%) of 72 harbouring bla_CTX-M-27, a plasmid-mediated gene for production of extended-spectrum β-lactamases (ESBLs). Of 33 cases with clinical data, 19 (58%) received antibiotics and eight (24%) were hospitalised. 21 (78%) of 27 cases with completed bespoke outbreak questionnaires were HIV-negative MSM taking HIV pre-exposure prophylaxis (PrEP) who reported sexual contacts in the UK and Europe within the incubation period. Interpretation: We highlight the rapid dissemination of XDR ESBL-producing S sonnei in sexual networks of MSM. We recommend strengthening shigella testing where clinically indicated, antimicrobial-resistance surveillance, and integrated health promotion messaging among all MSM, including PrEP users, to reduce the burden of shigellosis. Funding: National Institute for Health Research Health Protection Research Unit in Gastrointestinal Infections at the University of Liverpool in partnership with the UK Health Security Agency.

Original language	English
Pages (from-to)	1503-1510
Number of pages	8
Journal	The Lancet Infectious Diseases
Volume	22
Issue number	10
DOIs	https://doi.org/10.1016/S1473-3099(22)00370-X
Publication status	Published - Oct 2022

Bibliographical note

Funding Information:
We thank all colleagues involved in the Outbreak Control Team, including UKHSA Health Protection Teams, microbiology diagnostic laboratories in the National Health Service, British HIV Association, and British Association of Sexual Health and HIV, and the patients who participated in case interviews. We also thank the National Institute for Health Research (NIHR) Health Protection Research Unit (HPRU) in Gastrointestinal Infections at the University of Liverpool who partly funded the study in partnership with the UK Health Security Agency. CJ and DRG are affiliated with the NIHR HPRU in Gastrointestinal Infections.

Funding Information:
We thank all colleagues involved in the Outbreak Control Team, including UKHSA Health Protection Teams, microbiology diagnostic laboratories in the National Health Service, British HIV Association, and British Association of Sexual Health and HIV, and the patients who participated in case interviews. We also thank the National Institute for Health Research (NIHR) Health Protection Research Unit (HPRU) in Gastrointestinal Infections at the University of Liverpool who partly funded the study in partnership with the UK Health Security Agency. CJ and DRG are affiliated with the NIHR HPRU in Gastrointestinal Infections.

Publisher Copyright:
© 2022 Published by Elsevier Ltd. This is an Open Access article under the CC BY 4.0 license

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10.1016/S1473-3099(22)00370-X

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@article{bdb8f61aa76f40adb80f5ff690f0e9c4,

title = "Outbreak of sexually transmitted, extensively drug-resistant Shigella sonnei in the UK, 2021–22: a descriptive epidemiological study",

abstract = "Background: Shigellosis, traditionally a foodborne and waterborne infection, causes substantial morbidity globally. It is now a leading cause of sexually transmitted gastroenteritis among gay, bisexual, and other men who have sex with men (MSM). We describe an ongoing outbreak of extensively drug-resistant (XDR) Shigella sonnei in the UK. Methods: Routine laboratory surveillance (Second Generation Surveillance System, Gastrointestinal Data Warehouse) identified an exceedance of S sonnei clade 5 in England, first detected in September, 2021. Cases within this clade were subsequently reported from Scotland, Wales, and Northern Ireland. Confirmed cases in this outbreak were defined as individuals diagnosed with S sonnei clade 5 in the UK, with a specimen date between Sept 1, 2021, and Feb 9, 2022, who were genomically confirmed as part of a ten-single nucleotide polymorphism (SNP) linkage cluster. We used whole-genome sequencing with SNP typing to identify genomic clusters and antimicrobial-resistance determinants, analysing cases across the UK. We collected demographic, epidemiological, and clinical data from people infected with S sonnei clade 5 in England using questionnaires (standard and bespoke outbreak questionnaires). We used descriptive summary statistics to characterise cases. Findings: 72 cases (70 [97%] male, median age 34 years [IQR 27–39]) belonging to the ten-SNP single linkage cluster of S sonnei clade 5 were identified between Sept 4, 2021, and Feb 9, 2022. Isolates were predominantly XDR, with 66 (92%) of 72 harbouring blaCTX-M-27, a plasmid-mediated gene for production of extended-spectrum β-lactamases (ESBLs). Of 33 cases with clinical data, 19 (58%) received antibiotics and eight (24%) were hospitalised. 21 (78%) of 27 cases with completed bespoke outbreak questionnaires were HIV-negative MSM taking HIV pre-exposure prophylaxis (PrEP) who reported sexual contacts in the UK and Europe within the incubation period. Interpretation: We highlight the rapid dissemination of XDR ESBL-producing S sonnei in sexual networks of MSM. We recommend strengthening shigella testing where clinically indicated, antimicrobial-resistance surveillance, and integrated health promotion messaging among all MSM, including PrEP users, to reduce the burden of shigellosis. Funding: National Institute for Health Research Health Protection Research Unit in Gastrointestinal Infections at the University of Liverpool in partnership with the UK Health Security Agency.",

author = "{Outbreak Control Team} and Hannah Charles and Mateo Prochazka and Katie Thorley and Adam Crewdson and Greig, {David R.} and Claire Jenkins and Anais Painset and Helen Fifer and Lynda Browning and Paul Cabrey and Robert Smith and Daniel Richardson and Laura Waters and Katy Sinka and Gauri Godbole and Helen Corkin and Asha Abrahams and Holly LeBlond and Janice Lo and Amelia Holgate and John Saunders and Gunveer Plahe and Amoolya Vusirikala and Freddy Green and Mike King and Rediat Tewolde and Andrew Jajja",

note = "Funding Information: We thank all colleagues involved in the Outbreak Control Team, including UKHSA Health Protection Teams, microbiology diagnostic laboratories in the National Health Service, British HIV Association, and British Association of Sexual Health and HIV, and the patients who participated in case interviews. We also thank the National Institute for Health Research (NIHR) Health Protection Research Unit (HPRU) in Gastrointestinal Infections at the University of Liverpool who partly funded the study in partnership with the UK Health Security Agency. CJ and DRG are affiliated with the NIHR HPRU in Gastrointestinal Infections. Funding Information: We thank all colleagues involved in the Outbreak Control Team, including UKHSA Health Protection Teams, microbiology diagnostic laboratories in the National Health Service, British HIV Association, and British Association of Sexual Health and HIV, and the patients who participated in case interviews. We also thank the National Institute for Health Research (NIHR) Health Protection Research Unit (HPRU) in Gastrointestinal Infections at the University of Liverpool who partly funded the study in partnership with the UK Health Security Agency. CJ and DRG are affiliated with the NIHR HPRU in Gastrointestinal Infections. Publisher Copyright: {\textcopyright} 2022 Published by Elsevier Ltd. This is an Open Access article under the CC BY 4.0 license",

year = "2022",

month = oct,

doi = "10.1016/S1473-3099(22)00370-X",

language = "English",

volume = "22",

pages = "1503--1510",

journal = "The Lancet Infectious Diseases",

issn = "1473-3099",

publisher = "Elsevier Ltd.",

number = "10",

}

TY - JOUR

T1 - Outbreak of sexually transmitted, extensively drug-resistant Shigella sonnei in the UK, 2021–22

T2 - a descriptive epidemiological study

AU - Outbreak Control Team

AU - Charles, Hannah

AU - Prochazka, Mateo

AU - Thorley, Katie

AU - Crewdson, Adam

AU - Greig, David R.

AU - Jenkins, Claire

AU - Painset, Anais

AU - Fifer, Helen

AU - Browning, Lynda

AU - Cabrey, Paul

AU - Smith, Robert

AU - Richardson, Daniel

AU - Waters, Laura

AU - Sinka, Katy

AU - Godbole, Gauri

AU - Corkin, Helen

AU - Abrahams, Asha

AU - LeBlond, Holly

AU - Lo, Janice

AU - Holgate, Amelia

AU - Saunders, John

AU - Plahe, Gunveer

AU - Vusirikala, Amoolya

AU - Green, Freddy

AU - King, Mike

AU - Tewolde, Rediat

AU - Jajja, Andrew

N1 - Funding Information: We thank all colleagues involved in the Outbreak Control Team, including UKHSA Health Protection Teams, microbiology diagnostic laboratories in the National Health Service, British HIV Association, and British Association of Sexual Health and HIV, and the patients who participated in case interviews. We also thank the National Institute for Health Research (NIHR) Health Protection Research Unit (HPRU) in Gastrointestinal Infections at the University of Liverpool who partly funded the study in partnership with the UK Health Security Agency. CJ and DRG are affiliated with the NIHR HPRU in Gastrointestinal Infections. Funding Information: We thank all colleagues involved in the Outbreak Control Team, including UKHSA Health Protection Teams, microbiology diagnostic laboratories in the National Health Service, British HIV Association, and British Association of Sexual Health and HIV, and the patients who participated in case interviews. We also thank the National Institute for Health Research (NIHR) Health Protection Research Unit (HPRU) in Gastrointestinal Infections at the University of Liverpool who partly funded the study in partnership with the UK Health Security Agency. CJ and DRG are affiliated with the NIHR HPRU in Gastrointestinal Infections. Publisher Copyright: © 2022 Published by Elsevier Ltd. This is an Open Access article under the CC BY 4.0 license

PY - 2022/10

Y1 - 2022/10

N2 - Background: Shigellosis, traditionally a foodborne and waterborne infection, causes substantial morbidity globally. It is now a leading cause of sexually transmitted gastroenteritis among gay, bisexual, and other men who have sex with men (MSM). We describe an ongoing outbreak of extensively drug-resistant (XDR) Shigella sonnei in the UK. Methods: Routine laboratory surveillance (Second Generation Surveillance System, Gastrointestinal Data Warehouse) identified an exceedance of S sonnei clade 5 in England, first detected in September, 2021. Cases within this clade were subsequently reported from Scotland, Wales, and Northern Ireland. Confirmed cases in this outbreak were defined as individuals diagnosed with S sonnei clade 5 in the UK, with a specimen date between Sept 1, 2021, and Feb 9, 2022, who were genomically confirmed as part of a ten-single nucleotide polymorphism (SNP) linkage cluster. We used whole-genome sequencing with SNP typing to identify genomic clusters and antimicrobial-resistance determinants, analysing cases across the UK. We collected demographic, epidemiological, and clinical data from people infected with S sonnei clade 5 in England using questionnaires (standard and bespoke outbreak questionnaires). We used descriptive summary statistics to characterise cases. Findings: 72 cases (70 [97%] male, median age 34 years [IQR 27–39]) belonging to the ten-SNP single linkage cluster of S sonnei clade 5 were identified between Sept 4, 2021, and Feb 9, 2022. Isolates were predominantly XDR, with 66 (92%) of 72 harbouring blaCTX-M-27, a plasmid-mediated gene for production of extended-spectrum β-lactamases (ESBLs). Of 33 cases with clinical data, 19 (58%) received antibiotics and eight (24%) were hospitalised. 21 (78%) of 27 cases with completed bespoke outbreak questionnaires were HIV-negative MSM taking HIV pre-exposure prophylaxis (PrEP) who reported sexual contacts in the UK and Europe within the incubation period. Interpretation: We highlight the rapid dissemination of XDR ESBL-producing S sonnei in sexual networks of MSM. We recommend strengthening shigella testing where clinically indicated, antimicrobial-resistance surveillance, and integrated health promotion messaging among all MSM, including PrEP users, to reduce the burden of shigellosis. Funding: National Institute for Health Research Health Protection Research Unit in Gastrointestinal Infections at the University of Liverpool in partnership with the UK Health Security Agency.

AB - Background: Shigellosis, traditionally a foodborne and waterborne infection, causes substantial morbidity globally. It is now a leading cause of sexually transmitted gastroenteritis among gay, bisexual, and other men who have sex with men (MSM). We describe an ongoing outbreak of extensively drug-resistant (XDR) Shigella sonnei in the UK. Methods: Routine laboratory surveillance (Second Generation Surveillance System, Gastrointestinal Data Warehouse) identified an exceedance of S sonnei clade 5 in England, first detected in September, 2021. Cases within this clade were subsequently reported from Scotland, Wales, and Northern Ireland. Confirmed cases in this outbreak were defined as individuals diagnosed with S sonnei clade 5 in the UK, with a specimen date between Sept 1, 2021, and Feb 9, 2022, who were genomically confirmed as part of a ten-single nucleotide polymorphism (SNP) linkage cluster. We used whole-genome sequencing with SNP typing to identify genomic clusters and antimicrobial-resistance determinants, analysing cases across the UK. We collected demographic, epidemiological, and clinical data from people infected with S sonnei clade 5 in England using questionnaires (standard and bespoke outbreak questionnaires). We used descriptive summary statistics to characterise cases. Findings: 72 cases (70 [97%] male, median age 34 years [IQR 27–39]) belonging to the ten-SNP single linkage cluster of S sonnei clade 5 were identified between Sept 4, 2021, and Feb 9, 2022. Isolates were predominantly XDR, with 66 (92%) of 72 harbouring blaCTX-M-27, a plasmid-mediated gene for production of extended-spectrum β-lactamases (ESBLs). Of 33 cases with clinical data, 19 (58%) received antibiotics and eight (24%) were hospitalised. 21 (78%) of 27 cases with completed bespoke outbreak questionnaires were HIV-negative MSM taking HIV pre-exposure prophylaxis (PrEP) who reported sexual contacts in the UK and Europe within the incubation period. Interpretation: We highlight the rapid dissemination of XDR ESBL-producing S sonnei in sexual networks of MSM. We recommend strengthening shigella testing where clinically indicated, antimicrobial-resistance surveillance, and integrated health promotion messaging among all MSM, including PrEP users, to reduce the burden of shigellosis. Funding: National Institute for Health Research Health Protection Research Unit in Gastrointestinal Infections at the University of Liverpool in partnership with the UK Health Security Agency.

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U2 - 10.1016/S1473-3099(22)00370-X

DO - 10.1016/S1473-3099(22)00370-X

M3 - Article

C2 - 35809593

AN - SCOPUS:85138530282

SN - 1473-3099

VL - 22

SP - 1503

EP - 1510

JO - The Lancet Infectious Diseases

JF - The Lancet Infectious Diseases

IS - 10

ER -

Outbreak of sexually transmitted, extensively drug-resistant Shigella sonnei in the UK, 2021–22: a descriptive epidemiological study

Abstract

Bibliographical note

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