1887
Systematic Review Open Access
Like 0

Abstract

Introduction

Food-borne disease outbreak investigations use epidemiological, microbiological and food chain evidence to identify the implicated food and inform risk management actions.

Aims

We used Shiga toxin-producing (STEC) as a model pathogen to investigate the success of outbreak strain isolation from food or environmental samples during outbreak investigations, and examined the factors influencing the chance of isolation.

Methods

We searched for reports of food-borne STEC outbreak investigations worldwide in peer-reviewed and grey literature in line with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines.

Results

We found a total of 223 outbreaks suitable for inclusion. Food and/or environmental samples were available for testing in 137 investigations, and the outbreak strain was isolated in 94 (42%) of investigations. We found no significant effect of STEC serovar or size of outbreak on likelihood of successful outbreak strain isolation. Isolation success ranged across different implicated commodities from 86% for beef-related outbreaks to 50% for salads and leafy greens. In 20% of outbreaks with samples available for testing, an additional STEC strain was isolated alongside the outbreak strain and in 6.6%, only an alternative STEC strain was isolated. Risk management action was taken on epidemiological evidence alone in 21 incidents.

Conclusion

The principal reasons why the outbreak strain was not isolated were lack of sample availability and methodological issues concerned with laboratory isolation. We recommend strategies that could improve the likelihood of isolation including the rapid collection of samples based on epidemiological intelligence.

Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2024.29.49.2400193
2024-12-05
2024-12-12
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2024.29.49.2400193
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/29/49/eurosurv-29-49-3.html?itemId=/content/10.2807/1560-7917.ES.2024.29.49.2400193&mimeType=html&fmt=ahah

References

  1. Word Health Organisation (WHO). Estimating the burden of foodborne diseases. Geneva: WHO. [Accessed: Oct 2023]. Available from: https://www.who.int/activities/estimating-the-burden-of-foodborne-diseases
  2. Word Health Organisation (WHO). Foodborne disease outbreaks: guidelines for investigation and control. 1st ed. Geneva: WHO; 2008. ISBN: 978-92-4-154722-2. Available from: https://www.who.int/publications/i/item/9789241547222
  3. Gormley FJ, Little CL, Rawal N, Gillespie IA, Lebaigue S, Adak GK. A 17-year review of foodborne outbreaks: describing the continuing decline in England and Wales (1992-2008). Epidemiol Infect. 2011;139(5):688-99.  https://doi.org/10.1017/S0950268810001858  PMID: 20696086 
  4. World Health Organization (WHO) & Food and Agriculture Organization of the United Nations (FAO). Shiga toxin-producing Escherichia coli (STEC) and food: attribution, characterization, and monitoring: report. Geneva: WHO; 2018. ISBN: 9789241514279‎. Available from: https://iris.who.int/handle/10665/272871
  5. Caprioli A, Morabito S, Brugère H, Oswald E. Enterohaemorrhagic Escherichia coli: emerging issues on virulence and modes of transmission. Vet Res. 2005;36(3):289-311.  https://doi.org/10.1051/vetres:2005002  PMID: 15845227 
  6. Majowicz SE, Scallan E, Jones-Bitton A, Sargeant JM, Stapleton J, Angulo FJ, et al. Global incidence of human Shiga toxin-producing Escherichia coli infections and deaths: a systematic review and knowledge synthesis. Foodborne Pathog Dis. 2014;11(6):447-55.  https://doi.org/10.1089/fpd.2013.1704  PMID: 24750096 
  7. Gillespie IA, O’Brien SJ, Adak GK, Cheasty T, Willshaw G. Foodborne general outbreaks of Shiga toxin-producing Escherichia coli O157 in England and Wales 1992-2002: where are the risks? Epidemiol Infect. 2005;133(5):803-8.  https://doi.org/10.1017/S0950268805004486  PMID: 16181498 
  8. Adams NL, Byrne L, Smith GA, Elson R, Harris JP, Salmon R, et al. Shiga toxin-producing Escherichia coli O157, England and Wales, 1983-2012. Emerg Infect Dis. 2016;22(4):590-7.  https://doi.org/10.3201/eid2204.151485  PMID: 26982243 
  9. Jaros P, French N, Benschop J, Soboleva T, Campbell D. Use of epidemiological evidence in investigations of foodborne disease outbreaks. MPI Technical Paper No: 2016/33. Wellington: Ministry for Primary Industries, Manatū Ahu Matua; 2016. ISBN: 978-1-77665-301-0. Available from: https://www.mpi.govt.nz/dmsdocument/12675/direct
  10. Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group. Reprint--preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Phys Ther. 2009;89(9):873-80.  https://doi.org/10.1093/ptj/89.9.873  PMID: 19723669 
  11. 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(6):930-9.  https://doi.org/10.1099/jmm.0.000970  PMID: 30994441 
  12. Schaffzin JK, Coronado F, Dumas NB, Root TP, Halse TA, Schoonmaker-Bopp DJ, 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(2):283-9.  https://doi.org/10.1017/S0950268811000719  PMID: 21554779 
  13. 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.  https://doi.org/10.1017/S095026881900116X  PMID: 31364563 
  14. Kintz E, Byrne L, Jenkins C, McCARTHY N, Vivancos R, Hunter P. Outbreaks of Shiga toxin-producing Escherichia coli linked to sprouted seeds, salad, and leafy greens: a systematic review. J Food Prot. 2019;82(11):1950-8.  https://doi.org/10.4315/0362-028X.JFP-19-014  PMID: 31638410 
  15. Sodha SV, Lynch M, Wannemuehler K, Leeper M, Malavet M, Schaffzin J, et al. Multistate outbreak of Escherichia coli O157:H7 infections associated with a national fast-food chain, 2006: a study incorporating epidemiological and food source traceback results. Epidemiol Infect. 2011;139(2):309-16.  https://doi.org/10.1017/S0950268810000920  PMID: 20429971 
  16. Bradley KK, Williams JM, Burnsed LJ, Lytle MB, McDermott MD, Mody RK, et al. Epidemiology of a large restaurant-associated outbreak of Shiga toxin-producing Escherichia coli O111:NM. Epidemiol Infect. 2012;140(9):1644-54.  https://doi.org/10.1017/S0950268811002329  PMID: 22117135 
  17. Byrne L, Adams N, Glen K, Dallman TJ, Kar-Purkayastha I, Beasley G, et al. Epidemiological and microbiological investigation of an outbreak of severe disease from Shiga toxin-producing Escherichia coli O157 infection associated with consumption of a slaw garnish. J Food Prot. 2016;79(7):1161-8.  https://doi.org/10.4315/0362-028X.JFP-15-580  PMID: 27357035 
  18. Centres for Disease Control and Prevention (CDC). 2014 E. coli outbreak linked to raw clover sprouts. Atlanta: CDC; 2014. Available from: ttps://archive.cdc.gov/#/details?url=https://www.cdc.gov/ecoli/2014/o121-05-14/index.html
  19. 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(4):1800346.  https://doi.org/10.2807/1560-7917.ES.2019.24.4.1800346  PMID: 30696532 
  20. King LA, Nogareda F, Weill FX, Mariani-Kurkdjian P, Loukiadis E, Gault G, et al. Outbreak of Shiga toxin-producing Escherichia coli O104:H4 associated with organic fenugreek sprouts, France, June 2011. Clin Infect Dis. 2012;54(11):1588-94.  https://doi.org/10.1093/cid/cis255  PMID: 22460976 
  21. Launders N, Byrne L, Adams N, Glen K, Jenkins C, Tubin-Delic D, et al. Outbreak of Shiga toxin-producing E. coli O157 associated with consumption of watercress, United Kingdom, August to September 2013. Euro Surveill. 2013;18(44):20624.  https://doi.org/10.2807/1560-7917.ES2013.18.44.20624  PMID: 24183803 
  22. Mikhail AFW, Jenkins C, Dallman TJ, Inns T, Douglas A, Martín AIC, 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(2):187-96.  https://doi.org/10.1017/S0950268817002874  PMID: 29248018 
  23. Friesema I, Sigmundsdottir G, van der Zwaluw K, Heuvelink A, Schimmer B, de Jager C, et al. An international outbreak of Shiga toxin-producing Escherichia coli O157 infection due to lettuce, September-October 2007. Euro Surveill. 2008;13(50):19065.  https://doi.org/10.2807/ese.13.50.19065-en  PMID: 19087865 
  24. Sharapov UM, Wendel AM, Davis JP, Keene WE, Farrar J, Sodha S, et al. Multistate outbreak of Escherichia coli O157:H7 infections associated with consumption of fresh spinach: United States, 2006. J Food Prot. 2016;79(12):2024-30.  https://doi.org/10.4315/0362-028X.JFP-15-556  PMID: 28221950 
  25. Ferguson DD, Scheftel J, Cronquist A, Smith K, Woo-Ming A, Anderson E, et al. Temporally distinct Escherichia coli 0157 outbreaks associated with alfalfa sprouts linked to a common seed source--Colorado and Minnesota, 2003. Epidemiol Infect. 2005;133(3):439-47.  https://doi.org/10.1017/S0950268804003589  PMID: 15962550 
  26. Wu FM, Beuchat LR, Wells JG, Slutsker L, Doyle MP, Swaminathan B. Factors influencing the detection and enumeration of Escherichia coli O157:H7 on alfalfa seeds. Int J Food Microbiol. 2001;71(1):93-9.  https://doi.org/10.1016/S0168-1605(01)00559-1  PMID: 11764897 
  27. Trmčić A, Ralyea R, Meunier-Goddik L, Donnelly C, Glass K, D’Amico D, et al. Consensus categorization of cheese based on water activity and pH-A rational approach to systemizing cheese diversity. J Dairy Sci. 2017;100(1):841-7.  https://doi.org/10.3168/jds.2016-11621  PMID: 27816245 
  28. Gaulin C, Ramsay D, Catford A, Bekal S. Escherichia coli O157:H7 Outbreak associated with the consumption of beef and veal tartares in the province of Quebec, Canada, in 2013. Foodborne Pathog Dis. 2015;12(7):612-8.  https://doi.org/10.1089/fpd.2014.1919  PMID: 25974740 
  29. Jenkins C, Dallman TJ, Launders N, Willis C, Byrne L, Jorgensen F, et al. Public health investigation of two outbreaks of Shiga toxin-producing Escherichia coli O157 associated with consumption of watercress. Appl Environ Microbiol. 2015;81(12):3946-52.  https://doi.org/10.1128/AEM.04188-14  PMID: 25841005 
  30. Gieraltowski L, Schwensohn C, Meyer S, Eikmeier D, Medus C, Sorenson A, 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(3):88-9.  https://doi.org/10.15585/mmwr.mm6603a6  PMID: 28125572 
  31. Yeni F, Yavaş S, Alpas H, Soyer Y. Most common foodborne pathogens and mycotoxins on fresh produce: a review of recent outbreaks. Crit Rev Food Sci Nutr. 2016;56(9):1532-44.  https://doi.org/10.1080/10408398.2013.777021  PMID: 26583913 
/content/10.2807/1560-7917.ES.2024.29.49.2400193
Loading

Data & Media loading...

Supplementary data

Submit comment
Close
Comment moderation successfully completed
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