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Abstract

Purpose. This study describes the epidemiology of Shiga toxin-producing Escherichia coli (STEC) infections in a population in the South East of England.

Methods. From 1 November 2013 to 31 March 2017 participating diagnostic laboratories reported Shiga toxin gene (stx) positive real-time PCR results to local public health teams. Stx positive faecal samples/isolates were referred to the Gastrointestinal Bacteria Reference Unit (GBRU) for confirmation by culture and typing by whole genome sequencing (WGS). Key clinical information was collected by public health teams.

Results/Key findings. Altogether, 548 faecal specimens (420 were non-travel associated) were stx positive locally, 535 were submitted to the GBRU. STEC were isolated from 42 %, confirmed by stx PCR in 21 % and 37 % were PCR negative. The most common non-travel associated STEC serogroups were O157, O26, O146 and O91. The annualized incidence of confirmed STEC infections (PCR or culture) was 5.8 per 100 000. The ratio of O157 to non-O157 STEC serogroups was 1:7. The annualized incidence of non-O157 haemolytic uraemic syndrome-associated Escherichia coli (HUSEC) strains was 0.4 per 100 000. Bloody diarrhoea was reported by 58 % of cases infected with E. coli O157, 33 % of cases infected with non-O157 HUSEC strains and 12 % of other lower risk non-O157 strains. Overall, 76 % of non-O157 HUSEC isolates possessed the eae virulence gene.

Conclusions. HUSEC including serogroup O157 were uncommon and more likely to cause bloody diarrhoea than other STEC. The routine use of stx PCR testing can influence clinical management. Understanding the local epidemiology facilitates a proportionate public health response to STEC, based on clinical and microbiological characteristics including stx subtype(s).

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/content/journal/jmm/10.1099/jmm.0.000970
2019-04-17
2020-01-29
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References

  1. Gyles CL. Shiga toxin-producing Escherichia coli: an overview. J Anim Sci 2007;85:E45–E62 [CrossRef]
    [Google Scholar]
  2. 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 [CrossRef]
    [Google Scholar]
  3. Schaffzin JK, Coronado F, Dumas NB, Root TP, Halse TA et al. Public health approach to detection of non-O157 Shiga toxin-producing Escherichia coli: summary of two outbreaks and laboratory procedures. Epidemiol Infect 2012;140:283–289 [CrossRef]
    [Google Scholar]
  4. Gould LH, Bopp C, Strockbine N, Atkinson R, Baselski V et al. Centers for disease control and prevention (CDC). Recommendations for diagnosis of Shiga toxin–producing Escherichia coli infections by clinical laboratories. MMWR Recomm Rep 2009;58:1–14
    [Google Scholar]
  5. Johnson KE, Thorpe CM, Sears CL. The emerging clinical importance of non-O157 Shiga toxin–producing Escherichia coli. Clin Infect Dis 2006;43:1587–1595
    [Google Scholar]
  6. Hoefer D, Hurd S, Medus C, Cronquist A, Hanna S et al. Laboratory practices for the identification of Shiga toxin-producing Escherichia coli in the United States, FoodNet sites, 2007. Foodborne Pathog Dis 2011;8:555–560 [CrossRef]
    [Google Scholar]
  7. 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 [CrossRef]
    [Google Scholar]
  8. EFSA Panel on Biological Hazards (BIOHAZ) Scientific opinion on VTEC-seropathotype and scientific criteria regarding pathogenicity assessment. EFSA J 2013;11:3138 [CrossRef]
    [Google Scholar]
  9. Gould LH, Mody RK, Ong KL, Clogher P, Cronquist AB et al. Increased recognition of non-O157 Shiga toxin-producing Escherichia coli infections in the United States during 2000–2010: epidemiologic features and comparison with E. coli O157 infections. Foodborne Pathog Dis 2013;10:453–460 [CrossRef]
    [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 [CrossRef]
    [Google Scholar]
  11. Pihkala N, Bauer N, Eblen D, Evans P et al.Risk Profile for Pathogenic Non-O157 Shiga toxin-producing Escherichia coli (non-O157 STEC) Office of Public Health Science Office of Policy and Program Development Food Safety and Inspection Service United States Department of Agriculture; 2012
  12. Karmali MA, Mascarenhas M, Shen S, Ziebell K, Johnson S et al. Association of genomic O island 122 of Escherichia coli EDL 933 with verocytotoxin-producing Escherichia coli seropathotypes that are linked to epidemic and/or serious disease. J Clin Microbiol 2003;41:4930–4940 [CrossRef]
    [Google Scholar]
  13. de Boer RF, Ferdous M, Ott A, Scheper HR, Wisselink GJ et al. Assessing the public health risk of Shiga toxin-producing Escherichia coli by use of a rapid diagnostic screening algorithm. J Clin Microbiol 2015;53:1588–1598 [CrossRef]
    [Google Scholar]
  14. Scheutz F. Taxonomy meets public health: the case of Shiga toxin-producing Escherichia coli. Microbiol Spectrum 2014;2: [CrossRef]
    [Google Scholar]
  15. Brandal LT, Wester AL, Lange H, Løbersli I, Lindstedt BA et al. Shiga toxin-producing Escherichia coli infections in Norway, 1992–2012: characterization of isolates and identification of risk factors for haemolytic uremic syndrome. BMC Infect Dis 2015;15:324 [CrossRef]
    [Google Scholar]
  16. De Rauw K, Buyl R, Jacquinet S, Piérard D. Risk determinants for the development of typical haemolytic uremic syndrome in Belgium and proposition of a new virulence typing algorithm for Shiga toxin-producing Escherichia coli. Epidemiol Infect 2018;1–5 [CrossRef]
    [Google Scholar]
  17. 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 [CrossRef]
    [Google Scholar]
  18. Istituto Superiore di SanitIdentification and characterization of Verocytotoxin-producing Escherichia coli (VTEC) by Real Time PCR amplification of the main virulence genes and the genes associated with the serogroups mainly associated with severe human infections EU Reference Laboratory for E. coli, Department of Veterinary Public Health and Food Safety Unit of Foodborne Zoonoses;
  19. Jenkins C, Lawson AJ, Cheasty T, Willshaw GA. Assessment of a real-time PCR for the detection and characterization of verocytotoxigenic Escherichia coli. J Med Microbiol 2012;61:1082–1085 [CrossRef]
    [Google Scholar]
  20. The VTEC operational manual Operational guidance for HPA staff dealing with cases and incidents of VTEC infection. https://www.gov.uk/government/publications/vero-cytotoxin-producing-escherichia-coli-operational-guidelines-for-public-health-management
  21. Dean AG, Arner TG, Sunki GG, Friedman R, Lantinga M et al.Epi Info™, a database and statistics program for public health professionals Atlanta, GA, USA: CDC; 2011
  22. Nüesch-Inderbinen M, Morach M, Cernela N, Althaus D, Jost M et al. Serotypes and virulence profiles of Shiga toxin-producing Escherichia coli strains isolated during 2017 from human infections in Switzerland. Int J Med Microbiol 2018
    [Google Scholar]
  23. Fakhouri F, Zuber J, Frémeaux-Bacchi V, Loirat C. Haemolytic uraemic syndrome. The Lancet in press 2017;390:681–696 [CrossRef]
    [Google Scholar]
  24. Kawano K, Okada M, Haga T, Maeda K, Goto Y. Relationship between pathogenicity for humans and stx genotype in Shiga toxin-producing Escherichia coli serotype O157. Eur J Clin Microbiol Infect Dis 2008;27:227–232 [CrossRef]
    [Google Scholar]
  25. Friedrich AW, Bielaszewská M, Zhang WL, Pulz M, Kuczius T et al. Escherichia coli harboring Shiga toxin 2 gene variants: frequency and association with clinical symptoms. J Infect Dis 2002;185:74–84 [CrossRef]
    [Google Scholar]
  26. Eklund M, Leino K, Siitonen A. Clinical Escherichia coli strains carrying stx genes: stx variants and stx-positive virulence profiles. J Clin Microbiol 2002;40:4585–4593 [CrossRef]
    [Google Scholar]
  27. Persson S, Olsen KEP, Ethelberg S, Scheutz F. Subtyping method for Escherichia coli Shiga toxin (verocytotoxin) 2 variants and correlations to clinical manifestations. J Clin Microbiol 2007;45:2020–2024 [CrossRef]
    [Google Scholar]
  28. Tam C, Viviani L, Adak B, Bolton E, Dodds J et al. The second study of infectious intestinal disease in the community (IID2 study). Final report. Food standards agency. 2012;http://researchonline.lshtm.ac.uk/21041/1/711-1-1393_IID2_FINAL_REPORT.pdf
  29. Tam CC, O'Brien SJ, Tompkins DS, Bolton FJ, Berry L et al. Changes in causes of acute gastroenteritis in the United Kingdom over 15 years: microbiologic findings from 2 prospective, population-based studies of infectious intestinal disease. Clin Infect Dis 2012;54:1275–1286 [CrossRef]
    [Google Scholar]
  30. Rice T, Quinn N, Sleator RD, Lucey B. Changing diagnostic methods and increased detection of verotoxigenic Escherichia coli, Ireland. Emerg Infect Dis 2016;22:1656–1657 [CrossRef]
    [Google Scholar]
  31. Annual Report of the National VTEC Reference Laboratory (VTEC NRL) 2015; Dublin: Public Health Laboratory, Health Services Executive;
  32. van Duynhoven YT, Friesema IH, Schuurman T, Roovers A, van Zwet AA et al. Prevalence, characterisation and clinical profiles of Shiga toxin-producing Escherichia coli in the Netherlands. Clin Microbiol Infect 2008;14:437–445 [CrossRef]
    [Google Scholar]
  33. EFSA (European Food Safety Authority) and ECDC (European Centre for Disease Prevention and Control) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016. EFSA J 2017;15:5077
    [Google Scholar]
  34. Centers for Disease Control and Prevention (CDC) National STEC Surveillance Annual Report, 2015 Atlanta, Georgia: US Department of Health and Human Services, CDC; 2017
    [Google Scholar]
  35. Feng PCH, Delannoy S, Lacher DW, Bosilevac JM, Fach P et al. Shiga toxin-producing serogroup O91 Escherichia coli strains isolated from food and environmental samples. Appl Environ Microbiol 2017;83:e01231–17 [CrossRef]
    [Google Scholar]
  36. Monaghan AM, Byrne B, McDowell D, Carroll AM, McNamara EB et al. Characterization of farm, food, and clinical shiga toxin-producing Escherichia coli (STEC) O113. Foodborne Pathog Dis 2012;9:1088–1096 [CrossRef]
    [Google Scholar]
  37. Martinez-Castillo A, Quirós P, Navarro F, Miró E, Muniesa M. Shiga toxin 2-encoding bacteriophages in human fecal samples from healthy individuals. Appl Environ Microbiol 2013;79:4862–4868 [CrossRef]
    [Google Scholar]
  38. Urdahl AM, Solheim HT, Vold L, Hasseltvedt V, Wasteson Y. Shiga toxin-encoding genes (stx genes) in human faecal samples. APMIS 2013;121:202–210 [CrossRef]
    [Google Scholar]
  39. McAuliffe G, Bissessor L, Williamson D, Moore S, Wilson J et al. Use of the EntericBio Gastro Panel II in a diagnostic microbiology laboratory: challenges and opportunities. Pathology 2017;49:419–422 [CrossRef]
    [Google Scholar]
  40. Harrington SM, Buchan BW, Doern C, Fader R, Ferraro MJ et al. Multicenter evaluation of the BD max enteric bacterial panel PCR assay for rapid detection of Salmonella spp., Shigella spp., Campylobacter spp. (C. jejuni and C. coli), and Shiga toxin 1 and 2 genes. J Clin Microbiol 2015;53:1639–1647 [CrossRef]
    [Google Scholar]
  41. Freedman SB, Xie J, Neufeld MS, Hamilton WL, Hartling L et al. Shiga toxin-producing Escherichia coli infection, antibiotics, and risk of developing hemolytic uremic syndrome: a meta-analysis. Clin Infect Dis 2016;62:1251–1258 [CrossRef]
    [Google Scholar]
  42. McFarland N, Bundle N, Jenkins C, Godbole G, Mikhail A et al. Recurrent seasonal outbreak of an emerging serotype of Shiga toxin-producing Escherichia coli (STEC O55:H7 Stx2a) in the south west of England, July 2014 to September 2015. Euro Surveill 2017;22:30610 [CrossRef]
    [Google Scholar]
  43. Lin A, Sultan O, Lau HK, Wong E, Hartman G et al. O serogroup specific real time PCR assays for the detection and identification of nine clinically relevant non-O157 STECs. Food Microbiol 2011;28:478–483 [CrossRef]
    [Google Scholar]
  44. Woods TA, Mendez HM, Ortega S, Shi X, Marx D et al. Development of 11-Plex MOL-PCR assay for the rapid screening of samples for Shiga toxin-producing Escherichia coli. Front Cell Infect Microbiol 2016;6:92 [CrossRef]
    [Google Scholar]
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