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Abstract

Diarrhoeagenic (DEC) pathotypes are defined by genes located on mobile genetic elements, and more than one definitive pathogenicity gene may be present in the same strain. In August 2022, UK Health Security Agency (UKHSA) surveillance systems detected an outbreak of hybrid Shiga toxin-producing /enterotoxigenic (STEC–ETEC) serotype O101:H33 harbouring both Shiga toxin () and heat-stable toxin ().

These hybrid strains of DEC are a public health concern, as they are often associated with enhanced pathogenicity. However, little is known about their epidemiology, clinical significance and associated public health burden.

The aim of this study was to describe the microbiology, epidemiology and genomic analysis of this novel hybrid serotype in the context of the STEC–ETEC strains in the UKHSA archive.

From 2014 to 2023, STEC isolated from faecal specimens testing positive for STEC by PCR were sequenced on the NextSeq 1000 short read platform and a subset were selected for long read nanopore sequencing. Genomes were analysed to determine serotype, subtype, DEC pathogenicity genes and antimicrobial resistance determinants.

There were 162 STEC–ETEC strains isolated between 2014 and 2023, of which 117/162 were human clinical isolates and 45 were of food or animal origin. An average of 16 STEC–ETEC strains were identified each year, exhibiting a range of different subtypes, the most common profiles being (=65, 40%) and (=48, 30%). The most common sequence types were ST329 and ST200 (=24 each), and the most frequently detected serotype was O187:H28 (=25). Nine cases of genetically linked STEC–ETEC O101:H33, were detected between 8 August and 21 September 2022. Although the temporal and geographical distribution of the cases was characteristic of a foodborne outbreak, the contaminated vehicle was not identified.

Phylogenetic analysis and long-read sequencing of the outbreak strain provided insight into the stepwise acquisition of and and the evolutionary history of STEC–ETEC pathotypes. The integration of epidemiological data and whole-genome sequencing for routine surveillance of gastrointestinal pathogens is key to understanding the emergence of zoonotic hybrid DEC pathotypes and monitoring foodborne threats to public health.

Funding
This study was supported by the:
  • National Institute for Health Research Health Protection Research Unit (Award 111815)
    • Principal Award Recipient: JenkinsClaire
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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/content/journal/jmm/10.1099/jmm.0.001946
2025-01-22
2026-01-24

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References

  1. Croxen MA, Law RJ, Scholz R, Keeney KM, Wlodarska M et al. Recent advances in understanding enteric pathogenic Escherichia coli. Clin Microbiol Rev 2013; 26:822–880 [View Article] [PubMed]
    [Google Scholar]
  2. Nataro JP, Kaper JB. Diarrheagenic Escherichia coli. Clin Microbiol Rev 1998; 11:142–201 [View Article] [PubMed]
    [Google Scholar]
  3. Kolenda R, Burdukiewicz M, Schierack P. A systematic review and meta-analysis of the epidemiology of pathogenic Escherichia coli of calves and the role of calves as reservoirs for human pathogenic E. coli. Front Cell Infect Microbiol 2015; 5:23 [View Article] [PubMed]
    [Google Scholar]
  4. Jenkins C. Enteroaggregative Escherichia coli. Curr Top Microbiol Immunol 2018; 416:27–50 [View Article] [PubMed]
    [Google Scholar]
  5. Newitt S, MacGregor V, Robbins V, Bayliss L, Chattaway MA et al. Two Linked Enteroinvasive Escherichia coli outbreaks, Nottingham, UK, June 2014. Emerg Infect Dis 2016; 22:1178–1184 [View Article] [PubMed]
    [Google Scholar]
  6. Tozzoli R, Grande L, Michelacci V, Ranieri P, Maugliani A et al. Shiga toxin-converting phages and the emergence of new pathogenic Escherichia coli: a world in motion. Front Cell Infect Microbiol 2014; 4:80 [View Article] [PubMed]
    [Google Scholar]
  7. Hazen TH, Michalski J, Luo Q, Shetty AC, Daugherty SC et al. Comparative genomics and transcriptomics of Escherichia coli isolates carrying virulence factors of both enteropathogenic and enterotoxigenic E. coli. Sci Rep 2017; 7:3513 [View Article] [PubMed]
    [Google Scholar]
  8. Njamkepo E, Fawal N, Tran-Dien A, Hawkey J, Strockbine N et al. Erratum: Global phylogeography and evolutionary history of Shigella dysenteriae type 1. Nat Microbiol 2016; 1:16209 [View Article] [PubMed]
    [Google Scholar]
  9. Koutsoumanis K, Allende A, Alvarez‐Ordóñez A, Bover‐Cid S, Chemaly M et al. Pathogenicity assessment of Shiga toxin‐producing Escherichia coli (STEC) and the public health risk posed by contamination of food with STEC. EFS2 2020; 18:5967 [View Article]
    [Google Scholar]
  10. Kampmeier S, Berger M, Mellmann A, Karch H, Berger P. The 2011 German Enterohemorrhagic Escherichia coli O104:H4 outbreak-the danger is still out there. Curr Top Microbiol Immunol 2018; 416:117–148 [View Article] [PubMed]
    [Google Scholar]
  11. Chattaway MA, Dallman TJ, Gentle A, Wright MJ, Long SE et al. Whole genome sequencing for public health surveillance of Shiga toxin-producing Escherichia coli other than serogroup O157. Front Microbiol 2016; 7:258 [View Article] [PubMed]
    [Google Scholar]
  12. Dallman TJ, Byrne L, Ashton PM, Cowley LA, Perry NT et al. Whole-genome sequencing for national surveillance of Shiga toxin-producing Escherichia coli O157. Clin Infect Dis 2015; 61:305–312 [View Article] [PubMed]
    [Google Scholar]
  13. Dallman T, Ashton P, Schafer U, Jironkin A, Painset A et al. SnapperDB: a database solution for routine sequencing analysis of bacterial isolates. Bioinformatics 2018; 34:3028–3029 [View Article] [PubMed]
    [Google Scholar]
  14. Greig DR, Quinn OI, Rodwell EV, Olonade I, Swift C et al. Genomic analysis of an outbreak of Shiga toxin-producing Escherichia coli O183:H18 in the United Kingdom, 2023. Microb Genom 2024; 10:001243 [View Article] [PubMed]
    [Google Scholar]
  15. Yara DA, Greig DR, Gally DL, Dallman TJ, Jenkins C et al. Comparison of shiga toxin-encoding bacteriophages in highly pathogenic strains of shiga toxin-producing escherichia coli O157:H7 in the UK. Microb Genom 2020; PMCID:e000334–393 [View Article] [PubMed]
    [Google Scholar]
  16. Nyholm O, Halkilahti J, Wiklund G, Okeke U, Paulin L et al. Comparative genomics and characterization of hybrid Shigatoxigenic and enterotoxigenic Escherichia coli (STEC/ETEC) strains. PLoS One 2015; 10:e0135936 [View Article] [PubMed]
    [Google Scholar]
  17. Boxall MD, Day MR, Greig DR, Jenkins C. Antimicrobial resistance profiles of diarrhoeagenic Escherichia coli isolated from travellers returning to the UK, 2015-2017. J Med Microbiol 2020; 69:932–943 [View Article] [PubMed]
    [Google Scholar]
  18. Vishram B, Jenkins C, Greig DR, Godbole G, Carroll K et al. The emerging importance of Shiga toxin-producing Escherichia coli other than serogroup O157 in England. J Med Microbiol 2021; 70:001375 [View Article] [PubMed]
    [Google Scholar]
  19. Love NK, Douglas A, Gharbia S, Hughes H, Morbey R et al. Understanding the impact of the COVID-19 pandemic response on GI infection surveillance trends in England, January 2020-April 2022. Epidemiol Infect 2023; 151:e147 [View Article] [PubMed]
    [Google Scholar]
  20. Lauzi S, Luzzago C, Chiani P, Michelacci V, Knijn A et al. Free-ranging red deer (Cervus elaphus) as carriers of potentially zoonotic Shiga toxin-producing Escherichia coli. Transbound Emerg Dis 2022; 69:1902–1911 [View Article] [PubMed]
    [Google Scholar]
  21. Nüesch-Inderbinen M, Barmettler K, Stevens MJA, Cernela N. Shiga toxin-producing Escherichia coli isolated from hunted wild boar (Sus scrofa) in Switzerland. Schweiz Arch Tierheilkd 2024; 166:131–140 [View Article] [PubMed]
    [Google Scholar]
  22. Bai X, Zhang J, Ambikan A, Jernberg C, Ehricht R et al. Molecular characterization and comparative genomics of clinical hybrid Shiga toxin-producing and enterotoxigenic Escherichia coli (STEC/ETEC) strains in Sweden. Sci Rep 2019; 9:5619 [View Article] [PubMed]
    [Google Scholar]
  23. Nyholm O, Heinikainen S, Pelkonen S, Hallanvuo S, Haukka K et al. Hybrids of Shigatoxigenic and enterotoxigenic Escherichia coli (STEC/ETEC) among human and animal isolates in Finland. Zoonoses Public Health 2015; 62:518–524 [View Article] [PubMed]
    [Google Scholar]
  24. Ji X, Liang B, Sun Y, Zhu L, Zhou B et al. An extended-spectrum beta-lactamase-producing hybrid Shiga-toxigenic and enterotoxigenic Escherichia coli strain isolated from a piglet with diarrheal disease in northeast China. Foodborne Pathog Dis 2020; 17:382–387 [View Article] [PubMed]
    [Google Scholar]
  25. Johura FT, Parveen R, Islam A, Sadique A, Rahim MN et al. Occurrence of hybrid Escherichia coli strains carrying Shiga toxin and heat-stable toxin in livestock of Bangladesh. Front Public Health 2016; 4:287 [View Article] [PubMed]
    [Google Scholar]
  26. Aref N-EM, Abdel-Raheem A-RA, Kamaly HF, Hussien SZ. Clinical and sero-molecular characterization of Escherichia coli with an emphasis on hybrid strain in healthy and diarrheic neonatal calves in Egypt. Open Vet J 2018; 8:351–359 [View Article] [PubMed]
    [Google Scholar]
  27. Martikainen O, Kagambèga A, Bonkoungou IJ, Barro N, Siitonen A et al. Characterization of Shigatoxigenic Escherichia coli strains from Burkina Faso. Foodborne Pathog Dis 2012; 9:1015–1021 [View Article] [PubMed]
    [Google Scholar]
  28. Yang X, Liu Q, Bai X, Hu B, Jiang D et al. High prevalence and persistence of Escherichia coli strains producing Shiga toxin subtype 2k in goat herds. Microbiol Spectr 2022; 10:e0157122 [View Article] [PubMed]
    [Google Scholar]
  29. Yang X, Wu Y, Liu Q, Sun H, Luo M et al. Genomic characteristics of Stx2e-producing Escherichia coli strains derived from humans, animals, and meats. Pathogens 2021; 10:1551 [View Article] [PubMed]
    [Google Scholar]
  30. Dallman TJ, Neuert S, Fernandez Turienzo C, Berin M, Richardson E et al. Prevalence and persistence of antibiotic resistance determinants in the gut of travelers returning to the United Kingdom is associated with colonization by pathogenic Escherichia coli. Microbiol Spectr 2023; 11:e0518522 [View Article] [PubMed]
    [Google Scholar]
  31. Den Ouden A, Greig DR, Rodwell EV, Tripodo F, Olonade I et al. Escherichia coli encoding Shiga toxin subtype Stx2f causing human infections in England, 2015-2022. J Med Microbiol 2023; 72:37294302 [View Article] [PubMed]
    [Google Scholar]
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