1887

Microbial Genomics logo

Volume 7, Issue 6

Phylogenetic context of Shiga toxin-producing serotype O26:H11 in England Open Access

Abstract

The increasing use of PCR for the detection of gastrointestinal pathogens in hospital laboratories in England has improved the detection of Shiga toxin-producing (STEC), and the diagnosis of haemolytic uraemic syndrome (HUS). We aimed to analyse the microbiological characteristics and phylogenetic relationships of STEC O26:H11, clonal complex (CC) 29, in England to inform surveillance, and to assess the threat to public health. There were 502 STEC belonging to CC29 isolated between 2014 and 2019, of which 416 were from individual cases. The majority of isolates belonged to one of three major sequence types (STs), ST16 (=37), ST21 (=350) and ST29 (=24). ST16 and ST29 were mainly isolated from cases reporting recent travel abroad. Within ST21, there were three main clades associated with domestic acquisition. All three domestic clades had Shiga toxin subtype gene () profiles associated with causing severe clinical outcomes including STEC-HUS, specifically either , or . Isolates from the same patient, same household or same outbreak with an established source for the most part fell within 5-SNP single linkage clusters. There were 19 5-SNP community clusters, of which six were travel-associated and one was an outbreak of 16 cases caused by the consumption of contaminated salad leaves. Of the remaining 12 clusters, 9/12 were either temporally or geographically related or both. Exposure to foodborne STEC O26:H11 ST21 capable of causing severe clinical outcomes, including STEC-HUS, is an emerging risk to public health in England. The lack of comprehensive surveillance of this STEC serotype is a concern, and there is a need to expand the implementation of methods capable of detecting STEC in local hospital settings.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): foodborne outbreaks , public health , Shiga toxin-producing Escherichia coliO26:H11 , surveillance and whole genome sequencing
Funding
This study was supported by the:
  • National Institute Health Research (Award 111815)
    • Principle Award Recipient: TimothyJ Dallman
© Crown copyright 2021
  • This information is licensed under the Open Government Licence 3.0. 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.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000551
2021-03-24
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/mgen/7/6/mgen000551.html?itemId=/content/journal/mgen/10.1099/mgen.0.000551&mimeType=html&fmt=ahah

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. Taylor CM, White RH, Winterborn MH, Rowe B. Haemolytic-Uraemic syndrome: clinical experience of an outbreak in the West Midlands. Br Med J 1986; 292:1513–1516 [View Article][PubMed]
     [Google Scholar]
  3. 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]
  4. Jenkins C, Evans J, Chart H, Willshaw GA, Frankel G. Escherichia coli serogroup O26-a new look at an old adversary. J Appl Microbiol 2008; 104:14–25 [View Article][PubMed]
     [Google Scholar]
  5. Smith HW, Linggood MA. The transmissible nature of enterotoxin production in a human enteropathogenic strain of Escherichia coli. J Med Microbiol 1971; 4:301–305 [View Article][PubMed]
     [Google Scholar]
  6. Scotland SM, Smith HR, Willshaw GA, Rowe B. Vero cytotoxin production in strain of Escherichia coli is determined by genes carried on bacteriophage. Lancet 1983; 2:216 [View Article][PubMed]
     [Google Scholar]
  7. Bielaszewska M, Mellmann A, Bletz S, Zhang W, Köck R et al. Enterohemorrhagic Escherichia coli O26:H11/H-: a new virulent clone emerges in Europe. Clin Infect Dis 2013; 56:1373–1381 [View Article][PubMed]
     [Google Scholar]
  8. Ogura Y, Gotoh Y, Itoh T, Sato MP, Seto K et al. Population structure of Escherichia coli O26 : H11 with recent and repeated stx2 acquisition in multiple lineages. Microb Genom 2017; 3: [View Article][PubMed]
     [Google Scholar]
  9. Gerber A, Karch H, Allerberger F, Verweyen HM, Zimmerhackl LB. Clinical course and the role of Shiga toxin-producing Escherichia coli infection in the hemolytic-uremic syndrome in pediatric patients, 1997-2000, in Germany and Austria: a prospective study. J Infect Dis 2002; 186:493–500 [View Article][PubMed]
     [Google Scholar]
  10. Brooks JT, Sowers EG, Wells JG, Greene KD, Griffin PM et al. Non-O157 Shiga toxin-producing Escherichia coli infections in the United States, 1983-2002. J Infect Dis 2005; 192:1422–1429 [View Article][PubMed]
     [Google Scholar]
  11. Pollock KG, Bhojani S, Beattie TJ, Allison L, Hanson M et al. Highly virulent Escherichia coli O26, Scotland. Emerg Infect Dis 2011; 17:1777–1779 [View Article][PubMed]
     [Google Scholar]
  12. Buvens G, Pierard D. Virulence profiling and disease association of verocytotoxin-producing Escherichia coli O157 and non-O157 isolates in Belgium. Foodborne Pathog Dis 2012; 9:530–535 [View Article][PubMed]
     [Google Scholar]
  13. Delannoy S, Mariani-Kurkdjian P, Bonacorsi S, Liguori S, Fach P. Characteristics of emerging human-pathogenic Escherichia coli O26:H11 strains isolated in France between 2010 and 2013 and carrying the stx2d gene only. J Clin Microbiol 2015; 53:486–492 [View Article][PubMed]
     [Google Scholar]
  14. Caron E, Crepin VF, Simpson N, Knutton S, Garmendia J et al. Subversion of actin dynamics by EPEC and EHEC. Curr Opin Microbiol 2006; 9:40–45 [View Article][PubMed]
     [Google Scholar]
  15. Pearce MC, Jenkins C, Vali L, Smith AW, Knight HI et al. Temporal shedding patterns and virulence factors of Escherichia coli serogroups O26, O103, O111, O145, and O157 in a cohort of beef calves and their dams. Appl Environ Microbiol 2004; 70:1708–1716 [View Article][PubMed]
     [Google Scholar]
  16. Leomil L, Pestana de Castro AF, Krause G, Schmidt H, Beutin L. Characterization of two major groups of diarrheagenic Escherichia coli O26 strains which are globally spread in human patients and domestic animals of different species. FEMS Microbiol Lett 2005; 249:335–342 [View Article][PubMed]
     [Google Scholar]
  17. Krüger A, Lucchesi PM, Sanso AM, Etcheverría AI, Bustamante AV et al. Genetic characterization of Shiga toxin-producing Escherichia coli O26:H11 strains isolated from animal, food, and clinical samples. Front Cell Infect Microbiol 2015; 5:74 [View Article][PubMed]
     [Google Scholar]
  18. Shakerian A, Rahimi E, Emad P. Vegetables and restaurant salads as a reservoir for shiga toxigenic Escherichia coli: distribution of virulence factors, O-Serogroups, and antibiotic resistance properties. J Food Prot 2016; 79:1154–1160 [View Article][PubMed]
     [Google Scholar]
  19. Ross CM, Rapp D, Cave VM, Brightwell G. Prevalence of Shiga toxin-producing Escherichia coli in pasture-based dairy herds. Lett Appl Microbiol 2019; 68:112–119 [View Article][PubMed]
     [Google Scholar]
  20. Moran-Gilad J, Rokney A, Danino D, Ferdous M, Alsana F et al. Real-time genomic investigation underlying the public health response to a Shiga toxin-producing Escherichia coli O26:H11 outbreak in a nursery. Epidemiol Infect 2017; 145:2998–3006 [View Article][PubMed]
     [Google Scholar]
  21. Scavia G, Gianviti A, Labriola V, Chiani P, Maugliani A et al. A case of haemolytic uraemic syndrome (HUS) revealed an outbreak of Shiga toxin-2-producing Escherichia coli O26:H11 infection in a nursery, with long-lasting shedders and person-to-person transmission, Italy 2015. J Med Microbiol 2018; 67:775–782 [View Article][PubMed]
     [Google Scholar]
  22. Chapman PA, Siddons CA, Zadik PM, Jewes L. An improved selective medium for the isolation of Escherichia coli O157. J Med Microbiol 1991; 35:107–110 [View Article][PubMed]
     [Google Scholar]
  23. Byrne L, Vanstone GL, Perry NT, Launders N, Adak GK et al. Epidemiology and microbiology of Shiga toxin-producing Escherichia coli other than serogroup O157 in England, 2009-2013. J Med Microbiol 2014; 63:1181–1188 [View Article][PubMed]
     [Google Scholar]
  24. Caprioli A, Tozzi AE, Rizzoni G, Karch H. Non-O157 Shiga toxin-producing Escherichia coli infections in Europe. Emerg Infect Dis 1997; 3:578–579 [View Article][PubMed]
     [Google Scholar]
  25. Schmidt H, Geitz C, Tarr PI, Frosch M, Karch H. Non-O157:H7 pathogenic Shiga toxin-producing Escherichia coli: phenotypic and genetic profiling of virulence traits and evidence for clonality. J Infect Dis 1999; 179:115–123 [View Article][PubMed]
     [Google Scholar]
  26. Terajima J, Iyoda S, Ohnishi M, Watanabe H. Shiga toxin (verotoxin)-producing Escherichia coli in Japan. Microbiol Spectr 2014; 2: [View Article][PubMed]
     [Google Scholar]
  27. Carroll KJ, Harvey-Vince L, Jenkins C, Mohan K, Balasegaram S. The epidemiology of Shiga toxin-producing Escherichia coli infections in the South East of England: November 2013-March 2017 and significance for clinical and public health. J Med Microbiol 2019; 68:930–939 [View Article][PubMed]
     [Google Scholar]
  28. Jenkins C, Dallman TJ, Grant KA. Impact of whole genome sequencing on the investigation of food-borne outbreaks of Shiga toxin-producing Escherichia coli serogroup O157:H7, England, 2013 to 2017. Euro Surveill 2019; 24: [View Article]
     [Google Scholar]
  29. 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]
  30. 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]
  31. 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]
  32. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article][PubMed]
     [Google Scholar]
  33. 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]
  34. Li H, Durbin R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 2010; 26:589–595 [View Article][PubMed]
     [Google Scholar]
  35. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The sequence Alignment/Map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article][PubMed]
     [Google Scholar]
  36. 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]
  37. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article][PubMed]
     [Google Scholar]
  38. Joensen KG, Tetzschner AM, Iguchi A, Aarestrup FM, Scheutz F. Rapid and easy in silico serotyping of Escherichia coli isolates by use of whole-genome sequencing data. J Clin Microbiol 2015; 53:2410–2426 [View Article][PubMed]
     [Google Scholar]
  39. Tewolde R, Dallman T, Schaefer U, Sheppard CL, Ashton P et al. Most: a modified MLST typing tool based on short read sequencing. PeerJ 2016; 4:e2308 [View Article][PubMed]
     [Google Scholar]
  40. European Food Safety Authority (ESFA) Pathogenicity assessment of Shiga toxin‐producing Escherichia coli (STEC) and the public health risk posed by contamination of food with STEC. EFSA Journal 2020; 18:5967
     [Google Scholar]
  41. Byrne L, Adams N, Jenkins C. Association between Shiga Toxin-Producing Escherichia coli O157:H7 stx Severity, England, 2009-2019. Emerg Infect Dis 2020; 26:2394–2400 [View Article][PubMed]
     [Google Scholar]
  42. Byrne L, Jenkins C, Launders N, Elson R, Adak GK. The epidemiology, microbiology and clinical impact of Shiga toxin-producing Escherichia coli in England, 2009-2012. Epidemiol Infect 2015; 143:3475–3487 [View Article][PubMed]
     [Google Scholar]
  43. Werber D, Fruth A, Liesegang A, Littmann M, Buchholz U et al. A multistate outbreak of Shiga toxin-producing Escherichia coli O26:H11 infections in Germany, detected by molecular subtyping surveillance. J Infect Dis 2002; 186:419–422 [View Article][PubMed]
     [Google Scholar]
  44. Ethelberg S, Smith B, Torpdahl M, Lisby M, Boel J et al. Outbreak of non-O157 Shiga toxin-producing Escherichia coli infection from consumption of beef sausage. Clin Infect Dis 2009; 48:e78–e81 [View Article][PubMed]
     [Google Scholar]
  45. Jones G, Lefèvre S, Donguy MP, Nisavanh A, Terpant G et al. Outbreak of Shiga toxin-producing Escherichia coli (STEC) O26 paediatric haemolytic uraemic syndrome (HUS) cases associated with the consumption of soft raw cow’s milk cheeses, France, March to May 2019. Euro Surveill 2019; 24: [View Article]
     [Google Scholar]
  46. 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][PubMed]
     [Google Scholar]
  47. 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]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000551
Loading
Phylogenetic context of Shiga toxin-producing Escherichia coli serotype O26:H11 in England
M Gen 7, 000551 (2021); https://doi.org/10.1099/mgen.0.000551
/content/journal/mgen/10.1099/mgen.0.000551
/content/journal/mgen/10.1099/mgen.0.000551
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error