1887

Access Microbiology open research platform logo

Volume 5, Issue 5

Shiga toxin-producing (STEC) and atypical enteropathogenic (aEPEC) in Swedish retail wheat flour Open Access

Abstract

Wheat flour has been identified as the source of multiple outbreaks of gastrointestinal disease caused by shiga toxin-producing (STEC). We have investigated the presence and genomic characteristics of STEC and related atypical enteropathogenic (aEPEC) in 200 bags of Swedish-produced retail wheat flour, representing 87 products and 25 brands. Samples were enriched in modified tryptone soya broth (mTSB) and screened with real-time PCR targeting , and , and the serogroups O157, O121 and O26. Isolation was performed by immunomagnetic separation (IMS) for suspected STEC/aEPEC O157, O121 and O26, and by screening pools of colonies for other STEC. Real-time PCR after enrichment revealed 12 % of samples to be positive for shiga toxin genes ( and/or ) and 11 % to be positive for intimin (). Organic production, small-scale production or whole grain did not significantly influence shiga toxin gene presence or absence in a generalized linear mixed model analysis. Eight isolates of STEC were recovered, all of which were intimin-negative. Multiple serotype/sequence type/shiga toxin subtype combinations that have also been found in flour samples in other European countries were recovered. Most STEC types recovered were associated with sporadic cases of STEC among humans in Sweden, but no types known to have caused outbreaks or severe cases of disease (i.e. haemolytic uraemic syndrome) were found. The most common finding was O187:H28 ST200 with , with possible links to cervid hosts. Wildlife associated with crop damage is a plausible explanation for at least some of the surprisingly high frequency of STEC in wheat flour.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): cereals , EHEC , food microbiology , food safety , foodborne infections , genomics , One Health and zoonosis
Funding
This study was supported by the:
  • The Elsa and Ivar Sandberg Foundation
    • Principle Award Recipient: RobertSoderlund
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/acmi/10.1099/acmi.0.000577.v3
2023-05-03
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/acmi/5/5/acmi000577.v3.html?itemId=/content/journal/acmi/10.1099/acmi.0.000577.v3&mimeType=html&fmt=ahah

References

  1. Gyles CL. Shiga toxin-producing Escherichia coli: an overview. J Anim Sci 2007; 85:E45–62 [View Article] [PubMed]
     [Google Scholar]
  2. Mele C, Remuzzi G, Noris M. Hemolytic uremic syndrome. Semin Immunopathol 2014; 36:399–420 [View Article] [PubMed]
     [Google Scholar]
  3. Persad AK, LeJeune JT. Animal reservoirs of Shiga Toxin-producing Escherichia coli . Microbiol Spectr 2014; 2:EHEC–0027 [View Article] [PubMed]
     [Google Scholar]
  4. Pires SM, Majowicz S, Gill A, Devleesschauwer B. Global and regional source attribution of Shiga toxin-producing Escherichia coli infections using analysis of outbreak surveillance data. Epidemiol Infect 2019; 147:e236 [View Article] [PubMed]
     [Google Scholar]
  5. Anonymous Microbiological surveillance of ehec (Mikrobiologisk övervakning av ehec) Public Health Agency of Sweden 2020-2022. n.d https://www.folkhalsomyndigheten.se/mikrobiologi-laboratorieanalyser/mikrobiella-och-immunologiska-overvakningsprogram/fordjupad-information/overvakning-av-ehec/
  6. EFSA Panel on Biological Hazards (BIOHAZ) Scientific Opinion on VTEC‐seropathotype and scientific criteria regarding pathogenicity assessment. EFS2 2013; 11: [View Article]
     [Google Scholar]
  7. Trabulsi LR, Keller R, Tardelli Gomes TA. Typical and atypical enteropathogenic Escherichia coli . Emerg Infect Dis 2002; 8:508–513 [View Article] [PubMed]
     [Google Scholar]
  8. Hu J, Torres AG. Enteropathogenic Escherichia coli: foe or innocent bystander?. Clin Microbiol Infect 2015; 21:729–734 [View Article] [PubMed]
     [Google Scholar]
  9. Söderlund R, Hurel J, Jinnerot T, Sekse C, Aspán A et al. Genomic comparison of Escherichia coli serotype O103:H2 isolates with and without verotoxin genes: implications for risk assessment of strains commonly found in ruminant reservoirs. Infect Ecol Epidemiol 2016; 6:30246 [View Article] [PubMed]
     [Google Scholar]
  10. Neil KP, Biggerstaff G, MacDonald JK, Trees E, Medus C et al. A novel vehicle for transmission of Escherichia coli O157:H7 to humans: multistate outbreak of E. coli O157:H7 infections associated with consumption of ready-to-bake commercial prepackaged cookie dough--United States, 2009. Clin Infect Dis 2012; 54:511–518 [View Article] [PubMed]
     [Google Scholar]
  11. Crowe SJ, Bottichio L, Shade LN, Whitney BM, Corral N et al. Shiga Toxin-producing E. coli infections associated with flour. N Engl J Med 2017; 377:2036–2043 [View Article] [PubMed]
     [Google Scholar]
  12. Morton V, Cheng JM, Sharma D, Kearney A. An outbreak of Shiga toxin-producing Escherichia coli O121 infections associated with flour—Canada, 2016–2017†. Can Commun Dis Rep 2017; 43:154–155 [View Article]
     [Google Scholar]
  13. Vasser M, Barkley J, Miller A, Gee E, Purcell K et al. Notes from the field: Multistate outbreak of Escherichia coli O26 infections linked to raw flour - United States, 2019. MMWR Morb Mortal Wkly Rep 2021; 70:600–601 [View Article] [PubMed]
     [Google Scholar]
  14. Gieraltowski L, Schwensohn C, Meyer S, Eikmeier D, Medus C et al. Notes from the field: multistate outbreak of Escherichia coli O157:H7 infections linked to dough mix - United States, 2016. MMWR Morb Mortal Wkly Rep 2017; 66:88–89 [View Article] [PubMed]
     [Google Scholar]
  15. Anonymous Rappel de pizzas surgelees Fraîch’up Buitoni: Buitoni; 2022 https://live-72196-food-buitoni-france.pantheonsite.io/fr/rappel-de-pizzas-surgelees-fraichup-buitoni/
  16. Anonymous Santé publique France - Cas graves de syndrome hémolytique et urémique (SHU) chez l’enfant: retrait - rappel préventif de lots de pizzas surgelées Fraîch’Up de la marque Buitoni en raison d’une possible contamination par la bactérie Escherichia coli O26: Santé publique France; 2022 https://www.santepubliquefrance.fr/presse/2022/cas-graves-de-syndrome-hemolytique-et-uremique-shu-chez-l-enfant-retrait-rappel-preventif-de-lots-de-pizzas-surgelees-fraich-up-de-la-marque
  17. Mäde D, Geuthner A-C, Imming R, Wicke A. Detection and isolation of Shiga-Toxin producing Escherichia coli in flour in Germany between 2014 and 2017. J Consum Prot Food Saf 2017; 12:245–253 [View Article]
     [Google Scholar]
  18. Kindle P, Nüesch-Inderbinen M, Cernela N, Stephan R. Detection, isolation, and characterization of Shiga Toxin-producing Escherichia coli in flour. J Food Prot 2019; 82:164–167 [View Article] [PubMed]
     [Google Scholar]
  19. Boss R, Hummerjohann J. Whole genome sequencing characterization of Shiga Toxin-producing Escherichia coli isolated from flour from Swiss retail markets. J Food Prot 2019; 82:1398–1404 [View Article] [PubMed]
     [Google Scholar]
  20. Zhang H, Yamamoto E, Murphy J, Carrillo C, Hardie K et al. Microbiological survey of wheat flour sold at retail in Canada, 2018 to 2019. J Food Prot 2021; 84:647–654 [View Article] [PubMed]
     [Google Scholar]
  21. Perelle S, Dilasser F, Grout J, Fach P. Detection by 5’-nuclease PCR of Shiga-toxin producing Escherichia coli O26, O55, O91, O103, O111, O113, O145 and O157:H7, associated with the world’s most frequent clinical cases. Mol Cell Probes 2004; 18:185–192 [View Article] [PubMed]
     [Google Scholar]
  22. Perelle S, Dilasser F, Grout J, Fach P. Detection of Escherichia coli serogroup O103 by real-time polymerase chain reaction. J Appl Microbiol 2005; 98:1162–1168 [View Article] [PubMed]
     [Google Scholar]
  23. Nielsen EM, Andersen MT. Detection and characterization of verocytotoxin-producing Escherichia coli by automated 5’ nuclease PCR assay. J Clin Microbiol 2003; 41:2884–2893 [View Article] [PubMed]
     [Google Scholar]
  24. Joensen KG, Tetzschner AMM, 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]
  25. Joensen KG, Scheutz F, Lund O, Hasman H, Kaas RS et al. Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli . J Clin Microbiol 2014; 52:1501–1510 [View Article] [PubMed]
     [Google Scholar]
  26. Larsen MV, Cosentino S, Rasmussen S, Friis C, Hasman H et al. Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol 2012; 50:1355–1361 [View Article] [PubMed]
     [Google Scholar]
  27. Martínez-Castillo A, Muniesa M. Implications of free Shiga toxin-converting bacteriophages occurring outside bacteria for the evolution and the detection of Shiga toxin-producing Escherichia coli . Front Cell Infect Microbiol 2014; 4:46 [View Article] [PubMed]
     [Google Scholar]
  28. Berghofer LK, Hocking AD, Miskelly D, Jansson E. Microbiology of wheat and flour milling in Australia. Int J Food Microbiol 2003; 85:137–149 [View Article] [PubMed]
     [Google Scholar]
  29. De Angelis M, Minervini F, Siragusa S, Rizzello CG, Gobbetti M. Wholemeal wheat flours drive the microbiome and functional features of wheat sourdoughs. Int J Food Microbiol 2019; 302:35–46 [View Article] [PubMed]
     [Google Scholar]
  30. 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]
  31. 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]
  32. Mitchell MC. Scottish wild deer as a potential source of human pathogenic non-O157 Shiga toxin producing Escherichia coli STEC: Edinburgh Napier University; 2021
     [Google Scholar]
  33. Flink C, Nyberg K. Occurrence of Campylobacter spp., Salmonella spp. and shiga toxin-producing Escherichia coli in inline milk filters from Swedish dairy farms. J Food Saf 2020; 40:
     [Google Scholar]
  34. 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]
  35. Nishida R, Nakamura K, Taniguchi I, Murase K, Ooka T et al. The global population structure and evolutionary history of the acquisition of major virulence factor-encoding genetic elements in Shiga toxin-producing Escherichia coli O121:H19. Microb Genom 2021; 7:12 [View Article] [PubMed]
     [Google Scholar]
  36. European food safety A, European centre for disease P, control The European Union One Health 2021 zoonoses report. EFSA J 2022; 20:12 [View Article]
     [Google Scholar]
  37. Gilbertsson I. Bevattning av spannmål – en ekonomisk analys / Irrigation of cereals – an economic analysis; MSc thesis No.1199 Uppsala: Swedish University of Agricultural Sciences; 2019
     [Google Scholar]
  38. Ländell G. The Swedish Board of Agriculture / Statistics Sweden: Viltskador i lantbruksgrödor 2020 (Wildlife crop damage 2020): The Swedish Board of Agriculture / Statistics Sweden; 2. https://jordbruksverket.se/5.2de76dfa17a6bda55987f54e.html#h-17avspannmalsarealenvarviltskadad
  39. Anonymous BfR opinion No 004/2020: Escherichia coli in flour – sources, risks and prevention. Bundesinstitut für Risikobewertung; 2020
  40. Gill A, McMahon T, Dussault F, Petronella N. Shiga toxin-producing Escherichia coli survives storage in wheat flour for two years. Food Microbiol 2020; 87:103380 [View Article] [PubMed]
     [Google Scholar]
  41. Espinosa L, Gray A, Duffy G, Fanning S, McMahon BJ. A scoping review on the prevalence of Shiga-toxigenic Escherichia coli in wild animal species. Zoonoses Public Health 2018; 65:911–920 [View Article] [PubMed]
     [Google Scholar]
  42. Menichetti L, Touzot L, Elofsson K, Hyvönen R, Kätterer T et al. Interactions between a population of fallow deer (Dama dama), humans and crops in a managed composite temperate landscape in southern Sweden: Conflict or opportunity?. PLoS One 2019; 14:e0215594 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/acmi/10.1099/acmi.0.000577.v3
Loading
Shiga toxin-producing Escherichia coli (STEC) and atypical enteropathogenic E. coli (aEPEC) in Swedish retail wheat flour
Access Microbiology 5, 000577.v3 (2023); https://doi.org/10.1099/acmi.0.000577.v3
/content/journal/acmi/10.1099/acmi.0.000577.v3
/content/journal/acmi/10.1099/acmi.0.000577.v3
Loading

Data & Media loading...

Supplements

Supplementary material 1

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