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Volume 71, Issue 8

Shiga toxin-producing clonal complex 32, including serotype O145:H28, in the UK and Ireland Open Access

Abstract

Shiga toxin-producing (STEC) O157:H7 has been the most clinically significant STEC serotype in the UK for over four decades. Over the last 10 years we have observed a decrease in STEC O157:H7 and an increase in non-O157 STEC serotypes, such as O145:H28.

Little is known about the microbiology and epidemiology of STEC belonging to CC32 (including O145:H28) in the UK. The aim of this study was to integrate genomic data with patient information to gain a better understanding of the virulence, disease severity, epidemic risk assessment and population structure of this clinically significant clonal complex.

Isolates of belonging to CC32 (=309) in the archives of public health agencies in the UK and Ireland were whole-genome-sequenced, virulence-profiled and integrated with enhanced surveillance questionnaire (ESQ) data, including exposures and disease severity.

Overall, diagnoses of STEC belonging to CC32 (290/309, 94 %) in the UK have increased every year since 2014. Most cases were female (61 %), and the highest proportion of cases belonged to the 0–4 age group (53/211,25 %). The frequency of symptoms of diarrhoea (92 %), abdominal pain (84 %), blood in stool (71 %) and nausea (51 %) was similar to that reported in cases of STEC O157:H7, although cases of STEC CC32 were more frequently admitted to hospital (STEC CC32 48 % vs O157:H7  34 %) and/or developed haemolytic uraemic syndrome (HUS) (STEC CC32 9 % vs O157:H7 4 %).

The majority of STEC isolates (268/290, 92 %) had the / virulence gene combination, most commonly associated with progression to STEC HUS. There was evidence of person-to-person transmission and small, temporally related, geographically dispersed outbreaks, characteristic of foodborne outbreaks linked to nationally distributed products.

We recommend more widespread use of polymerase chain reaction (PCR) for the detection of all STEC serogroups, the development of consistent strategies for the follow-up testing of PCR-positive faecal specimens, the implementation of more comprehensive and standardized collection of epidemiological data, and routine sharing of sequencing data between public health agencies worldwide.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): clonal complex32 , public health surveillance , shiga toxin-producing Escherichia coli O145:H28 and whole-genome sequencing
© 2022 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 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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2022-08-24
2024-05-03
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References

  1. 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]
  2. 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]
  3. 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]
  4. Boisen N, Melton-Celsa AR, Scheutz F, O’Brien AD, Nataro JP. Shiga toxin 2a and eteroaggregative Escherichia coli--a deadly combination. Gut Microbes 2015; 6:272–278 [View Article] [PubMed]
     [Google Scholar]
  5. Cointe A, Birgy A, Mariani-Kurkdjian P, Liguori S, Courroux C et al. Emerging multidrug-resistant hybrid pathotype Shiga toxin-producing Escherichia coli O80 and related strains of clonal complex 165, Europe. Emerg Infect Dis 2018; 24:2262–2269 [View Article] [PubMed]
     [Google Scholar]
  6. Byrne L, Adams N, Jenkins C. Association between Shiga toxin-producing Escherichia coli O157:H7 stx gene subtype and disease severity, England, 2009-2019. Emerg Infect Dis 2020; 26:2394–2400 [View Article] [PubMed]
     [Google Scholar]
  7. Koutsoumanis K, Allende A, Alvarez‐Ordóñez A, Bover‐Cid S et al.EFSA BIOHAZ Panel 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]
  8. Gasser C, Gautier E, Steck A, Siebenmann RE, Oechslin R. Hemolytic-uremic syndrome: bilateral necrosis of the renal cortex in acute acquired hemolytic anemia. Schweiz Med Wochenschr 1955; 85:905–909 [PubMed]
     [Google Scholar]
  9. Obrig TG. Escherichia coli Shiga toxin mechanisms of action in renal disease. Toxins 2010; 2:2769–2794 [View Article] [PubMed]
     [Google Scholar]
  10. Lingwood CA. Verotoxin/globotriaosyl ceramide recognition: angiopathy, angiogenesis and antineoplasia. Biosci Rep 1999; 19:345–354 [View Article] [PubMed]
     [Google Scholar]
  11. Karmali MA, Petric M, Lim C, Fleming PC, Arbus GS et al. The association between idiopathic hemolytic uremic syndrome and infection by verotoxin-producing Escherichia coli. J Infect Dis 1985; 151:775–782 [View Article] [PubMed]
     [Google Scholar]
  12. Butt S, Jenkins C, Godbole G, Byrne L. The epidemiology of shiga toxin-producing Escherichia coli serogroup O157 in england, 2009-2019. Epidemiol Infect 20221–30
     [Google Scholar]
  13. 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: [View Article] [PubMed]
     [Google Scholar]
  14. Simms I, Gilbart VL, Byrne L, Jenkins C, Adak GK et al. Identification of verocytotoxin-producing Escherichia coli O117:H7 in men who have sex with men, England, November 2013 to August 2014. Euro Surveill 2014; 19: [View Article]
     [Google Scholar]
  15. Baker KS, Dallman TJ, Thomson NR, Jenkins C. An outbreak of a rare Shiga-toxin-producing Escherichia coli serotype (O117:H7) among men who have sex with men. Microb Genom 2018; 4: [View Article] [PubMed]
     [Google Scholar]
  16. Dallman T, Cross L, Bishop C, Perry N, Olesen B et al. Whole genome sequencing of an unusual serotype of Shiga toxin-producing Escherichia coli. Emerg Infect Dis 2013; 19:1302–1304 [View Article] [PubMed]
     [Google Scholar]
  17. Olesen B, Jensen C, Olsen KEP, Fussing V, Gerner-Smidt P et al. VTEC O117:K1:H7 a new clonal group of E. coli associated with persistent diarrhoea in Danish travellers. Scand J Infect Dis 2009; 37:288–294 [View Article] [PubMed]
     [Google Scholar]
  18. Rodwell EV, Vishram B, Smith R, Browning L, Smith-Palmer A et al. Epidemiology and genomic analysis of Shiga toxin-producing Escherichia coli clonal complex 165 in the UK. J Med Microbiol 2021; 70: [View Article] [PubMed]
     [Google Scholar]
  19. Bertoldi B, Richardson S, Goodrich-Schneider R, Kurdmongkoltham P, Schneider K. Preventing Foodborne Illness: E. coli "The Big Six [Internet]. University of Florida. https://nifa.usda.gov/sites/default/files/resource/Preventing-Foodborne-Illness-E-coli-the-big-six.pdf
  20. Shridhar PB, Worley JN, Gao X, Yang X, Noll LW et al. Analysis of virulence potential of Escherichia coli O145 isolated from cattle feces and hide samples based on whole genome sequencing. PLOS ONE 2019; 14:e0225057 [View Article] [PubMed]
     [Google Scholar]
  21. Hoyle DV, Keith M, Williamson H, Macleod K, Mathie H et al. Prevalence and epidemiology of Non-O157 Escherichia coli Serogroups O26, O103, O111, and O145 and Shiga toxin gene carriage in Scottish cattle, 2014-2015. Appl Environ Microbiol 2021; 87:e03142-20 [View Article] [PubMed]
     [Google Scholar]
  22. Engelen F, Thiry D, Devleesschauwer B, Mainil J, De Zutter L et al. Occurrence of “gang of five” Shiga toxin-producing Escherichia coli serogroups on Belgian dairy cattle farms by overshoe sampling. Lett Appl Microbiol 2021; 72:415–419 [View Article] [PubMed]
     [Google Scholar]
  23. Projahn M, Lamparter MC, Ganas P, Goehler A, Lorenz-Wright SC et al. Genetic diversity and pathogenic potential of Shiga toxin-producing Escherichia coli (STEC) derived from German flour. Int J Food Microbiol 2021; 347:109197 [View Article] [PubMed]
     [Google Scholar]
  24. Buvens G, Possé B, De Schrijver K, De Zutter L, Lauwers S et al. Virulence profiling and quantification of verocytotoxin-producing Escherichia coli O145:H28 and O26:H11 isolated during an ice cream-related hemolytic uremic syndrome outbreak. Foodborne Pathog Dis 2011; 8:421–426 [View Article] [PubMed]
     [Google Scholar]
  25. Wahl E, Vold L, Lindstedt BA, Bruheim T, Afset JE. Investigation of an Escherichia coli O145 outbreak in a child day-care centre--extensive sampling and characterization of eae- and stx1-positive E. coli yields epidemiological and socioeconomic insight. BMC Infect Dis 2011; 11:238 [View Article] [PubMed]
     [Google Scholar]
  26. Taylor EV, Nguyen TA, Machesky KD, Koch E, Sotir MJ et al. Multistate outbreak of Escherichia coli O145 infections associated with romaine lettuce consumption, 2010. J Food Prot 2013; 76:939–944 [View Article] [PubMed]
     [Google Scholar]
  27. Jenkins C, Ling CL, Ciesielczuk HL, Lockwood J, Hopkins S et al. Detection and identification of bacteria in clinical samples by 16S rRNA gene sequencing: comparison of two different approaches in clinical practice. J Med Microbiol 2012; 61:483–488 [View Article] [PubMed]
     [Google Scholar]
  28. 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]
  29. Dallman TJ, Greig DR, Gharbia SE, Jenkins C. Phylogenetic context of Shiga toxin-producing Escherichia coli serotype O26:H11 in England. Microb Genom 2021; 7:
     [Google Scholar]
  30. Scottish E. coli O157/STEC Reference Laboratory Whole genome sequence typing and analysis of non-O157 STEC [Internet]. Food Standards Scotland; 2020 https://www.foodstandards.gov.scot/downloads/WGS_Typing_and_Analysis_of_Non-O157_STEC_-_Jan_2020_v3.pdf
  31. Joensen KG, Engsbro ALØ, Lukjancenko O, Kaas RS, Lund O et al. Evaluating next-generation sequencing for direct clinical diagnostics in diarrhoeal disease. Eur J Clin Microbiol Infect Dis 2017; 36:1325–1338 [View Article] [PubMed]
     [Google Scholar]
  32. 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]
  33. 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]
  34. 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]
  35. 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]
  36. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD et al. Corrigendum to: IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era. Mol Biol Evol 2020; 37:2461 [View Article] [PubMed]
     [Google Scholar]
  37. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 2019; 47:W256–W259 [View Article] [PubMed]
     [Google Scholar]
  38. Tonkin-Hill G, Lees JA, Bentley SD, Frost SDW, Corander J. Fast hierarchical Bayesian analysis of population structure. Nucleic Acids Res 2019; 47:5539–5549 [View Article] [PubMed]
     [Google Scholar]
  39. Zhou Z, Alikhan NF, Mohamed K, Fan Y, Achtman M. The enterobase user’s guide, with case studies on Salmonella transmissions, Yersinia pestis phylogeny, and Escherichia core genomic diversity. Genome Res 2020; 30:138–152
     [Google Scholar]
  40. Prjibelski A, Antipov D, Meleshko D, Lapidus A, Korobeynikov A. Using SPAdes De Novo Assembler. Curr Protoc Bioinformatics 2020; 70:e102 [View Article] [PubMed]
     [Google Scholar]
  41. Mikheenko A, Prjibelski A, Saveliev V, Antipov D, Gurevich A. Versatile genome assembly evaluation with QUAST-LG. Bioinformatics 2018; 34:i142–i150 [View Article] [PubMed]
     [Google Scholar]
  42. Treangen TJ, Ondov BD, Koren S, Phillippy AM. The Harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol 2014; 15:11 [View Article] [PubMed]
     [Google Scholar]
  43. Kaindama L, Jenkins C, Aird H, Jorgensen F, Stoker K et al. A cluster of Shiga Toxin-producing Escherichia coli O157:H7 highlights raw pet food as an emerging potential source of infection in humans. Epidemiol Infect 2021; 149:e124 [View Article] [PubMed]
     [Google Scholar]
  44. Reeves PR, Liu B, Zhou Z, Li D, Guo D et al. Rates of mutation and host transmission for an Escherichia coli clone over 3 years. PLoS One 2011; 6:e26907 [View Article] [PubMed]
     [Google Scholar]
  45. Eckford S, Grace K, Harris C, Reeves H. UK Veterinary antibiotic Resistance and Sales Surveillance. Internet Veterinary Medicines Directorate; 2013 https://www.gov.uk/government/publications/veterinary-antimicrobial-resistance-and-sales-surveillance-2013
     [Google Scholar]
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Shiga toxin-producing Escherichia coli clonal complex 32, including serotype O145:H28, in the UK and Ireland
J. Med. Microbiol. 71, 001579 (2022); https://doi.org/10.1099/jmm.0.001579
/content/journal/jmm/10.1099/jmm.0.001579
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