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Volume 10, Issue 5

Genomic analysis of an outbreak of Shiga toxin-producing O183:H18 in the United Kingdom, 2023 Open Access

Abstract

In June 2023, UKHSA surveillance systems detected an outbreak of severe gastrointestinal symptoms caused by a rare serotype of Shiga toxin-producing , STEC O183:H18. There were 26 cases aged 6 months to 74 years (42 % cases were aged 0–9 years), distributed across the UK with onset dates range between 22 May 2023 and 4 July 2023. The epidemiological and food chain investigations were inconclusive, although meat products made from beef mince were implicated as a potential vehicle. The outbreak strain belonged to sequence type (ST) 657 and harboured a Shiga toxin () subtype located on a prophage that was unique in the UKHSA -encoding bacteriophage database. Plasmid encoded, putative virulence genes , , , and were detected, however, the established STEC virulence genes involved in attachment to the gut mucosa ( and ) were absent. The acquisition of across the global population structure of ST657 appeared to correspond with the presence of , , , and . During the outbreak investigation, we used long read sequencing to characterise the plasmid and prophage content of this atypical STEC, to look for evidence to explain its recent emergence. Although we were unable to determine source and transmission route of the outbreak strain, the genomic analysis revealed potential clues as to how novel strains for STEC evolve. With the implementation of PCR capable of detecting all STEC, and genome sequencing for typing and virulence profiling, we have the tools to enable us to monitor the changing landscape of STEC. Improvements in the standardised collection of epidemiological data and trace-back strategies within the food industry, will ensure we have a surveillance system capable of alerting us to emerging threats to public health.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): genomic epidemiology , outbreak , Shiga toxin-producing Escherichia coli , surveillance and whole genome sequencing
Funding
This study was supported by the:
  • National Institute for Health Research Health Protection Research Unit (Award 111815)
    • Principle Award Recipient: ClaireJenkins
© 2024 Crown Copyright
  • 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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2024-05-21
2025-04-18
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References

  1. 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]
  2. Wirth T, Falush D, Lan R, Colles F, Mensa P et al. Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 2006; 60:1136–1151 [View Article] [PubMed]
     [Google Scholar]
  3. 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]
  4. Lindsey RL, Prasad A, Feldgarden M, Gonzalez-Escalona N, Kapsak C et al. Identification and characterization of ten Escherichia coli strains encoding novel Shiga toxin 2 subtypes, Stx2n as well as Stx2j, Stx2m, and Stx2o, in the United States. Microorganisms 2023; 11:2561 [View Article] [PubMed]
     [Google Scholar]
  5. Stevens MP, Frankel GM. The locus of enterocyte effacement and associated virulence factors of enterohemorrhagic Escherichia coli. Microbiol Spectr 2014; 2:EHEC–0007 [View Article] [PubMed]
     [Google Scholar]
  6. Dallman T, Smith GP, O’Brien B, Chattaway MA, Finlay D et al. Characterization of a verocytotoxin-producing enteroaggregative Escherichia coli serogroup O111:H21 strain associated with a household outbreak in Northern Ireland. J Clin Microbiol 2012; 50:4116–4119 [View Article] [PubMed]
     [Google Scholar]
  7. Frank C, Milde-Busch A, Werber D. Results of surveillance for infections with Shiga toxin-producing Escherichia coli (STEC) of serotype O104:H4 after the large outbreak in Germany, July to December 2011. Euro Surveill 2014; 19:20760 [View Article]
     [Google Scholar]
  8. 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: [View Article]
     [Google Scholar]
  9. Jenkins C, Byrne L, Vishram B, Sawyer C, Balasegaram S et al. Shiga toxin-producing Escherichia coli haemolytic uraemic syndrome (STEC-HUS): diagnosis, surveillance and public-health management in England. J Med Microbiol 2020; 69:1034–1036 [View Article] [PubMed]
     [Google Scholar]
  10. Byrne L, Kaindama L, Bentley M, Jenkins C, Aird H et al. Investigation into a national outbreak of STEC O157:H7 associated with frozen beef burgers, UK, 2017. Epidemiol Infect 2020; 148:e215 [View Article] [PubMed]
     [Google Scholar]
  11. Wilson D, Dolan G, Aird H, Sorrell S, Dallman TJ et al. Farm-to-fork investigation of an outbreak of Shiga toxin-producing Escherichia coli O157. Microb Genom 2018; 4:e000160 [View Article] [PubMed]
     [Google Scholar]
  12. Jenkins C, Bird PK, Wensley A, Wilkinson J, Aird H et al. Outbreak of STEC O157:H7 linked to a milk pasteurisation failure at a dairy farm in England, 2019. Epidemiol Infect 2022; 150:e114 [View Article] [PubMed]
     [Google Scholar]
  13. Treacy J, Jenkins C, Paranthaman K, Jorgensen F, Mueller-Doblies D et al. Outbreak of Shiga toxin-producing Escherichia coli O157:H7 linked to raw drinking milk resolved by rapid application of advanced pathogen characterisation methods, England, August to October 2017. Euro Surveill 2019; 24:1800191 [View Article] [PubMed]
     [Google Scholar]
  14. Gobin M, Hawker J, Cleary P, Inns T, Gardiner D et al. National outbreak of Shiga toxin-producing Escherichia coli O157:H7 linked to mixed salad leaves, United Kingdom, 2016. Euro Surveill 2018; 23:17-00197 [View Article] [PubMed]
     [Google Scholar]
  15. Mikhail AFW, Jenkins C, Dallman TJ, Inns T, Douglas A et al. An outbreak of Shiga toxin-producing Escherichia coli O157:H7 associated with contaminated salad leaves: epidemiological, genomic and food trace back investigations. Epidemiol Infect 2018; 146:187–196 [View Article] [PubMed]
     [Google Scholar]
  16. Adams NL, Byrne L, Smith GA, Elson R, Harris JP et al. Shiga toxin-producing Escherichia coli O157, England and Wales, 1983-2012. Emerg Infect Dis 2016; 22:590–597 [View Article] [PubMed]
     [Google Scholar]
  17. Byrne L, Dallman TJ, Adams N, Mikhail AFW, McCarthy N et al. Highly pathogenic clone of Shiga Toxin-producing Escherichia coli O157:H7, England and Wales. Emerg Infect Dis 2018; 24:2303–2308 [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. Butt S, Allison L, Vishram B, Greig DR, Aird H et al. Epidemiological investigations identified an outbreak of Shiga toxin-producing Escherichia coli serotype O26:H11 associated with pre-packed sandwiches. Epidemiol Infect 2021; 149:e178 [View Article] [PubMed]
     [Google Scholar]
  20. Ashton PM, Perry N, Ellis R, Petrovska L, Wain J et al. Insight into Shiga toxin genes encoded by Escherichia coli O157 from whole genome sequencing. PeerJ 2015; 3:e739 [View Article] [PubMed]
     [Google Scholar]
  21. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25:1754–1760 [View Article] [PubMed]
     [Google Scholar]
  22. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. Genome project data processing subgroup. The sequence alignment/map format and Samtools. Bioinformatics 2009 Aug; PMCID:2078–2079 [View Article] [PubMed]
     [Google Scholar]
  23. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K et al. The genome analysis toolkit: a mapreduce framework for analyzing next-generation DNA sequencing data. Genome Res 2010; 20:1297–1303 [View Article] [PubMed]
     [Google Scholar]
  24. 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]
  25. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using gubbins. Nucleic Acids Res 2015; 43:e15 [View Article] [PubMed]
     [Google Scholar]
  26. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 2020; 37:1530–1534 [View Article] [PubMed]
     [Google Scholar]
  27. Greig DR, Jenkins C, Gharbia SE, Dallman TJ. Analysis of a small outbreak of Shiga toxin-producing Escherichia coli O157:H7 using long-read sequencing. Microb Genom 2021; 7: [View Article]
     [Google Scholar]
  28. Kolmogorov M, Yuan J, Lin Y, Pevzner PA. Assembly of long, error-prone reads using repeat graphs. Nat Biotechnol 2019; 37:540–546 [View Article] [PubMed]
     [Google Scholar]
  29. Vaser R, Sović I, Nagarajan N, Šikić M. Fast and accurate de novo genome assembly from long uncorrected reads. Genome Res 2017; 27:737–746 [View Article] [PubMed]
     [Google Scholar]
  30. Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 2018; 34:3094–3100 [View Article] [PubMed]
     [Google Scholar]
  31. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 2014; 9:e112963 [View Article] [PubMed]
     [Google Scholar]
  32. Hunt M, Silva ND, Otto TD, Parkhill J, Keane JA et al. Circlator: automated circularization of genome assemblies using long sequencing reads. Genome Biol 2015; 16:294 [View Article]
     [Google Scholar]
  33. Shaaban S, Cowley LA, McAteer SP, Jenkins C, Dallman TJ et al. Evolution of a zoonotic pathogen: investigating prophage diversity in enterohaemorrhagic Escherichia coli O157 by long-read sequencing. Microb Genom 2016; 2:e000096 [View Article] [PubMed]
     [Google Scholar]
  34. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624 [View Article] [PubMed]
     [Google Scholar]
  35. Gilchrist CLM, Chooi YH. clinker & clustermap.js: automatic generation of gene cluster comparison figures. Bioinformatics 2021; 37:2473–2475 [View Article] [PubMed]
     [Google Scholar]
  36. Ondov BD, Treangen TJ, Melsted P, Mallonee AB, Bergman NH et al. Mash: fast genome and metagenome distance estimation using MinHash. Genome Biol 2016; 17:132 [View Article] [PubMed]
     [Google Scholar]
  37. Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 2011; 12:402 [View Article] [PubMed]
     [Google Scholar]
  38. Butt S, Smith-Palmer A, Shand A, McDonald E, Allison L et al. Evidence of on-going transmission of Shiga toxin-producing Escherichia coli O157:H7 following a foodborne outbreak. Epidemiol Infect 2021; 149:e147 [View Article] [PubMed]
     [Google Scholar]
  39. Ooka T, Tokuoka E, Furukawa M, Nagamura T, Ogura Y et al. Human gastroenteritis outbreak associated with Escherichia albertii, Japan. Emerg Infect Dis 2013; 19:144–146 [View Article] [PubMed]
     [Google Scholar]
  40. Buchholz U, Bernard H, Werber D, Böhmer MM, Remschmidt C et al. German outbreak of Escherichia coli O104:H4 associated with sprouts. N Engl J Med 2011; 365:1763–1770 [View Article] [PubMed]
     [Google Scholar]
  41. Rodwell EV, Greig DR, Godbole G, Jenkins C. Clinical and public health implications of increasing notifications of LEE-negative Shiga toxin-producing Escherichia coli in England, 2014-2022. J Med Microbiol 2024; 73: [View Article]
     [Google Scholar]
  42. Dallman TJ, Ashton PM, Byrne L, Perry NT, Petrovska L et al. Applying phylogenomics to understand the emergence of Shiga-toxin-producing Escherichia coli O157:H7 strains causing severe human disease in the UK. Microb Genom 2015; 1:e000029 [View Article]
     [Google Scholar]
  43. Yara DA, Greig DR, Gally DL, Dallman TJ, Jenkins C. Comparison of Shiga toxin-encoding bacteriophages in highly pathogenic strains of Shiga toxin-producing Escherichia coli O157:H7 in the UK. Microb Genom 2020; 6:e000334 [View Article]
     [Google Scholar]
  44. Greig DR, Mikhail AFW, Dallman TJ, Jenkins C. Analysis Shiga toxin-encoding bacteriophage in a rare strain of Shiga Toxin-producing Escherichia coli O157:H7 stx2a/stx2c. Front Microbiol 2020; 11:577658 [View Article] [PubMed]
     [Google Scholar]
  45. Jenkins C, Perry NT, Godbole G, Gharbia S. Evaluation of chromogenic selective agar (CHROMagar STEC) for the direct detection of Shiga toxin-producing Escherichia coli from faecal specimens. J Med Microbiol 2020; 69:487–491 [View Article] [PubMed]
     [Google Scholar]
  46. 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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Genomic analysis of an outbreak of Shiga toxin-producing Escherichia coli O183:H18 in the United Kingdom, 2023
M Gen 10, 001243 (2024); https://doi.org/10.1099/mgen.0.001243
/content/journal/mgen/10.1099/mgen.0.001243
/content/journal/mgen/10.1099/mgen.0.001243
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