Identification of domestic reservoirs and common exposures in an emerging lineage of Shiga toxin-producing Escherichia coli O157:H7 in England: a genomic epidemiological analysis

Timothy J. Dallman*, Katri Jalava, Neville Q. Verlander, David Gally, Claire Jenkins, Gauri Godbole, Saheer Gharbia

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

7 Citations (Scopus)

Abstract

Background: The zoonotic pathogen Shiga toxin-producing Escherichia coli (STEC) O157:H7 emerged during the 1980s as a causative agent of foodborne outbreaks associated with haemorrhagic colitis and haemolytic uraemic syndrome, which can be fatal. We investigated the emerging lineage IIc that was causing outbreaks of STEC O157:H7, identified and quantified the domestic and non-domestic reservoirs, and quantified patient exposures across the population of England. Methods: In this genomic epidemiological analysis study, all human STEC O157:H7 lineage IIc (n=925) isolates cultured from faecal specimens submitted to the UK Health Security Agency between June 1, 2015, and Dec 31, 2020, from patients in England in the community or in hospital, were whole-genome sequenced and the genomic population structure was described. Explanatory variables were obtained from microbiological surveillance data and STEC Enhanced Surveillance Questionnaire responses. Ancestral-state reconstruction using patient travel information was used to define domestic and non-domestic clades and transmission dynamics. Exposures for patients infected with isolates from domestic clades were assessed using mixed-effects multinomial univariable and multivariable regression. Findings: Lineage IIc emerged 50 years ago, and subsequent clonal expansions have resolved into six major extant clades. We defined two English domestic clades that emerged during the past 30 years, and four non-domestic clades comprising isolates that infected or were transmitted to patients in England via international travel or the consumption or handling of imported food. Throughout the study period, non-domestic clades contributed approximately twice the number of infections as domestic clades did. Patients infected with domestic IIc clade strains reported more frequent exposure to fresh produce (raw vegetables p=0·012; prepackaged salad p=0·0009), contact with animals (cattle p=0·021), and visits to farms (p=0·0053) than patients infected with strains from other STEC O157:H7 lineages. A multivariable mixed-effects multinomial model confirmed that within the domestic clades, the major risk factors for infection were prepackaged salad (clade 2.3.3, relative risk ratio [RRR] 1·72, 95% CI 1·09–2·72; p=0·019) and visits to farms (clade 2.5.2, RRR 1·98, 1·12–3·52; p=0·020) as fixed effects. Local authority district as a random variable had a strong but variable effect for clades 2.3.3 and 2.5.2. Interpretation: Lineage IIc has emerged as the most prevalent lineage of STEC O157:H7 in England, with a sizeable domestic reservoir. Human infection is associated with the consumption of contaminated fresh produce and contact with domestic livestock. The collection of routine, detailed exposure data on patients who are infected, integrated with high-resolution microbiological typing, enables powerful reframing of our understanding of foodborne disease risk within a One Health context. Funding: National Institute for Health and Care Research Health and UK Health Security Agency.

Original languageEnglish
Pages (from-to)e606-e615
JournalThe Lancet Microbe
Volume3
Issue number8
DOIs
Publication statusPublished - Aug 2022

Bibliographical note

Funding Information:
We gratefully acknowledge the E coli O157 Super-shedding in Cattle and Mitigation of Human Risk (FS101055) project team for the provision of the cattle isolates and the staff of the UK Gastrointestinal Bacteria Reference Unit for the processing of isolates as part of routine surveillance and the UK Gastrointestinal Infections and Food Safety (One Health) Division for the epidemiological and statistical surveillance and for doing enhanced questionnaires. This research was partly funded by the UK National Institute for Health and Care Research (NIHR) Health Protection Research Unit in Gastrointestinal Infections at the University of Liverpool, and the NIHR Health Protection Research Unit in Genomics and Enabling Data at the University of Warwick, in partnership with UK Health Security Agency (UKHSA). The views expressed are those of the authors and not necessarily those of the UK National Health Service, the NIHR, the UK Department of Health, or UKHSA.

Funding Information:
We gratefully acknowledge the E coli O157 Super-shedding in Cattle and Mitigation of Human Risk (FS101055) project team for the provision of the cattle isolates and the staff of the UK Gastrointestinal Bacteria Reference Unit for the processing of isolates as part of routine surveillance and the UK Gastrointestinal Infections and Food Safety (One Health) Division for the epidemiological and statistical surveillance and for doing enhanced questionnaires. This research was partly funded by the UK National Institute for Health and Care Research (NIHR) Health Protection Research Unit in Gastrointestinal Infections at the University of Liverpool, and the NIHR Health Protection Research Unit in Genomics and Enabling Data at the University of Warwick, in partnership with UK Health Security Agency (UKHSA). The views expressed are those of the authors and not necessarily those of the UK National Health Service, the NIHR, the UK Department of Health, or UKHSA.

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

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