Skip to main content Accessibility help
×
Home

A beef-associated outbreak of Salmonella Typhimurium DT104 in The Netherlands with implications for national and international policy

  • M. KIVI (a1) (a2), A. HOFHUIS (a1), D. W. NOTERMANS (a1), W. J. B. WANNET (a1), M. E. O. C. HECK (a1), A. W. VAN DE GIESSEN (a1), Y. T. H. P. VAN DUYNHOVEN (a1), O. F. J. STENVERS (a3), A. BOSMAN (a1) (a2) and W. VAN PELT (a1)...

Summary

A ten-fold increase in Salmonella Typhimurium DT104 cases in The Netherlands during September–November 2005 prompted an outbreak investigation. A population-based matched case-control study included 56 cases and 100 controls. Risk factors for infection were consumption of a pre-processed raw beef product (odds ratio 4·2, 95% confidence interval 1·5–12·0) and of food from mobile caterers (odds ratio 4·9, 95% confidence interval 1·1–22·1). Bacterial molecular typing established a link with another DT104 outbreak in Denmark caused by beef from a third European country. The incriminated beef was traced in The Netherlands and sampling yielded DT104 of the outbreak-associated molecular type. We concluded that this outbreak was caused by imported contaminated beef. Consumers should be informed about presence of raw meat in pre-processed food products. Optimal utilization of international networks and testing and traceability of foodstuffs has the potential to prevent foodborne infections.

    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      A beef-associated outbreak of Salmonella Typhimurium DT104 in The Netherlands with implications for national and international policy
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      A beef-associated outbreak of Salmonella Typhimurium DT104 in The Netherlands with implications for national and international policy
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      A beef-associated outbreak of Salmonella Typhimurium DT104 in The Netherlands with implications for national and international policy
      Available formats
      ×

Copyright

Corresponding author

*Author for correspondence: Dr M. Kivi, Centre for Infectious Disease Epidemiology, National Institute for Public Health and the Environment (RIVM), PO Box 1, 3720BA, Bilthoven, The Netherlands. (Email: marten.kivi@rivm.nl)

References

Hide All
1. Helms, M, Ethelberg, S, Molbak, K. International Salmonella Typhimurium DT104 infections, 1992–2001. Emerging Infectious Diseases 2005; 11: 859867.
2. Glynn, MK, et al. Emergence of multidrug-resistant Salmonella enterica serotype Typhimurium DT104 infections in the United States. New England Journal of Medicine 1998; 338: 13331338.
3. Molbak, K, et al. An outbreak of multidrug-resistant, quinolone-resistant Salmonella enterica serotype Typhimurium DT104. New England Journal of Medicine 1999; 341: 14201425.
4. White, DG, et al. The isolation of antibiotic-resistant salmonella from retail ground meats. New England Journal of Medicine 2001; 345: 11471154.
5. Talbot, EA, Gagnon, ER, Greenblatt, J. Common ground for the control of multidrug-resistant salmonella in ground beef. Clinical Infectious Diseases 2006; 42: 14551462.
6. Dechet, AM, et al. Outbreak of multidrug-resistant Salmonella enterica serotype Typhimurium definitive type 104 infection linked to commercial ground beef, Northeastern United States, 2003–2004. Clinical Infectious Diseases 2006; 42: 747752.
7. Davies, A, et al. An outbreak of Salmonella Typhimurium DT104 food poisoning associated with eating beef. Communicable Disease Report Review 1996; 6: R159162.
8. Isakbaeva, E, et al. Salmonella Typhimurium DT104 outbreak linked to imported minced beef, Norway, October–November 2005. Eurosurveillance 2005; 10(11).
9. Cody, SH, et al. Two outbreaks of multidrug-resistant Salmonella serotype Typhimurium DT104 infections linked to raw-milk cheese in Northern California. Journal of the American Medical Association 1999; 281: 18051810.
10. Villar, RG, et al. Investigation of multidrug-resistant Salmonella serotype Typhimurium DT104 infections linked to raw-milk cheese in Washington State. Journal of the American Medical Association 1999; 281: 18111816.
11. Andersson, Y, et al. Salmonella Typhimurium outbreak in Sweden from contaminated jars of helva (or halva). Eurosurveillance 2001; 5(29).
12. Horby, PW, et al. A national outbreak of multi-resistant Salmonella enterica serovar Typhimurium definitive phage type (DT) 104 associated with consumption of lettuce. Epidemiology and Infection 2003; 130: 169178.
13. Doorduyn, Y, et al. Risk factors for Salmonella Enteritidis and Typhimurium (DT104 and non-DT104) infections in the Netherlands: predominant roles for raw eggs in Enteritidis and sandboxes in Typhimurium infections. Epidemiology and Infection 2006; 134: 617626.
14. Wall, PG, et al. A case control study of infection with an epidemic strain of multiresistant Salmonella Typhimurium DT104 in England and Wales. Communicable Disease Report Review 1994; 4: R130135.
15. Helms, M, et al. Excess mortality associated with antimicrobial drug-resistant Salmonella Typhimurium. Emerging Infectious Diseases 2002; 8: 490495.
16. Varma, JK, et al. Antimicrobial-resistant nontyphoidal salmonella is associated with excess bloodstream infections and hospitalizations. Journal of Infectious Diseases 2005; 191: 554561.
17. de Wit, MA, et al. Sensor, a population-based cohort study on gastroenteritis in the Netherlands: incidence and etiology. American Journal of Epidemiology 2001; 154: 666674.
18. de Wit, MA, et al. A population-based longitudinal study on the incidence and disease burden of gastroenteritis and campylobacter and salmonella infection in four regions of the Netherlands. European Journal of Epidemiology 2000; 16: 713718.
19. van Pelt, W, et al. Laboratory surveillance of bacterial gastroenteric pathogens in the Netherlands, 1991–2001. Epidemiology and Infection 2003; 130: 431441.
20. van Pelt, W. Explosive increase of multiresistant Salmonella Typhimurium DT104 in 2001 in the Netherlands. Eurosurveillance 2001; 5(50).
21. van Duijkeren, E, et al. Serotype and phage type distribution of salmonella strains isolated from humans, cattle, pigs, and chickens in the Netherlands from 1984 to 2001. Journal of Clinical Microbiology 2002; 40: 39803985.
22. Notermans, DW, et al. Sharp increase of infections with Salmonella serotype Typhimurium DT104 in the Netherlands [in Dutch]. Nederlandse Tijdschrift voor Geneeskunde 2005; 149: 29922994.
23. Kivi, M, et al. Large outbreak of Salmonella Typhimurium DT104, the Netherlands, September–November 2005. Eurosurveillance 2005; 10(12).
24. Widdowson, MA, et al. Automated, laboratory-based system using the internet for disease outbreak detection, the Netherlands. Emerging Infectious Diseases 2003; 9: 10461052.
25. Gatto, AJ, et al. Distribution of molecular subtypes within Salmonella enterica serotype Enteritidis phage type 4 and S. Typhimurium definitive phage type 104 in nine European countries, 2000–2004: Results of an international multi-centre study. Epidemiology and Infection 2006; 134: 729736.
26. Lindstedt, BA, et al. DNA fingerprinting of Salmonella enterica subsp. enterica serovar Typhimurium with emphasis on phage type DT104 based on variable number of tandem repeat loci. Journal of Clinical Microbiology 2003; 41: 14691479.
27. Mevius, DJ, Pellicaan, C, van Pelt, W (eds) MARAN 2004: Monitoring of antimicrobial resistance and antibiotic usage in animals in the Netherlands in 2004. The Netherlands: VANTURES, the Veterinary Antibiotic Usage and Resistance Surveillance Working Group, 2005.
28. The European Parliament and the Council of the European Union. Regulation EC/178/2002. Official Journal of the European Communities 2002; L31: 124.
29. The European Parliament and the Council of the European Union. Regulation EC/853/2004. Official Journal of the European Union 2004; L226: 2282.
30. The European Parliament and the Council of the European Union. Regulation EC/1760/2000. Official Journal of the European Union 2000; L204: 110.
31. The European Parliament and the Council of the European Union. Regulation EC/1825/2000. Official Journal of the European Union 2000; L216: 812.
32. Ethelberg, S. Salmonellosis outbreak linked to carpaccio made from imported raw beef, Denmark, June–August 2005. Eurosurveillance 2005; 10(9).
33. Doorduyn, Y, et al. Shiga toxin-producing Escherichia coli (STEC) O157 outbreak, the Netherlands, September–October 2005. Eurosurveillance 2006; 11(7–8).
34. van Kreijl, CF, Knaap, AGAC, van Raaij, JMA (eds) Our food, our health: Healthy diet and safe food in the Netherlands. Bilthoven, the Netherlands: National Institute for Public Health and the Environment, 2006.
35. Netherlands Ministry of Justice. Commodities act order on preparation and handling of food [in Dutch]. Staatsblad van het Koninkrijk der Nederlanden 1992; 678.
36. The European Parliament and the Council of the European Union. Regulation EC/2160/2003. Official Journal of the European Union 2003; L325: 115.
37. Naugle, AL, et al. Food safety and inspection service regulatory testing program for Escherichia coli O157:H7 in raw ground beef. Journal of Food Protection 2005; 68: 462468.
38. The European Parliament and the Council of the European Union. Regulation EC/2073/2005. Official Journal of the European Union 2005; L338: 126.
39. The European Parliament and the Council of the European Union. Regulation EC/1831/2003. Official Journal of the European Union 2003; L268: 2943.

Related content

Powered by UNSILO

A beef-associated outbreak of Salmonella Typhimurium DT104 in The Netherlands with implications for national and international policy

  • M. KIVI (a1) (a2), A. HOFHUIS (a1), D. W. NOTERMANS (a1), W. J. B. WANNET (a1), M. E. O. C. HECK (a1), A. W. VAN DE GIESSEN (a1), Y. T. H. P. VAN DUYNHOVEN (a1), O. F. J. STENVERS (a3), A. BOSMAN (a1) (a2) and W. VAN PELT (a1)...

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.