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Original article

Vol. 145 No. 3940 (2015)

Cross-border outbreak of Salmonella enterica ssp. enterica serovar Bovismorbificans: multiple approaches for an outbreak investigation in Germany and Switzerland

  • Astrid M Knoblauch
  • Martin W Bratschi
  • Meike K Zuske
  • Denise Althaus
  • Roger Stephan
  • Herbert Hächler
  • Andreas Baumgartner
  • Rita Prager
  • Wolfgang Rabsch
  • Ekkehardt Altpeter
  • Marianne Jost
  • Mirjam Mäusezahl
  • Christoph Hatz
  • Sabine Kiefer
Cite this as:
Swiss Med Wkly. 2015;145:w14182


QUESTION UNDER STUDY: In July 2014, an outbreak of Salmonella enterica ssp. enterica serovar Bovismorbificans was detected in Switzerland. The goal of the outbreak investigation was to rapidly identify and eliminate the contamination source in order to prevent new cases.

METHODS: A case-case study design was applied comprising reported cases of S. Bovismorbificans and cases of other serovars. A trawling questionnaire was administered by telephone interview. Data were collected for 34 cases (20 S. Bovismorbificans and 14 Salmonella spp.) pertaining to food consumption during the 72 hours prior to symptom onset.

RESULTS: A statistically significant association between an S. Bovismorbificans infection and the consumption of ‘salads’ (odds ratio [OR] 14.3, 95% confidence interval [CI] 1.47–138.27) as well as the consumption of ‘sprouts’ (OR 10.6, 95% CI 1.16–97.59) was found. Principal places of consumption of ‘salads’ and ‘sprouts’ in outbreak cases were restaurants in southern Germany (80.0%, 95% CI 56.3%–94.3%). Microbiological analysis in Germany identified S. Bovismorbificans on sprouts, and genotype analysis confirmed that Swiss and German cases shared the same outbreak strain. The contaminated products were removed from the market in Germany, preventing an on-going outbreak.

CONCLUSION: The combination of the applied methods and the collaboration between the two countries proved to be crucial elements of this investigation. A series of sprouts-associated salmonellosis outbreaks underpin the importance of this vegetable as a potential food-borne pathogen carrier.


  1. European Food Safety Authority (EFSA). Zoonoses monitoring: Switzerland: Trends and sources of zoonoses and zoonotic agents in humans, foodstuffs, animals and feedingsstuffs. 2013; Parma: EFSA.
  2. Schmid H, Baumgartner A. Epidemiology of infections with enteric salmonellae in Switzerland with particular consideration of travelling activities. Swiss Med Wkly. 2013;143:w13842.
  3. Tindall BJ, Grimont PA, Garrity GM, Euzeby JP. Nomenclature and taxonomy of the genus Salmonella. Int J Syst Evol Microbiol. 2005;55(Pt 1):521–4.
  4. Guibourdenche M, Roggentin P, Mikoleit M, Fields PI, Bockemuhl J, Grimont PA, et al. Supplement 2003–2007 (No. 47) to the White-Kauffmann-Le Minor scheme. Res Microbiol. 2010;161(1):26–9.
  5. Bundesrecht. Verordnung über die Meldung übertragbarer Krankheiten des Menschen. 1999; Bern: Schweizerische Eidgenossenschaft.
  6. Stafford RJ, McCall BJ, Neill AS, Leon DS, Dorricott GJ, Towner CD, et al. A statewide outbreak of Salmonella Bovismorbificans phage type 32 infection in Queensland. Commun Dis Intell Q Rep. 2002;26(4):568–73.
  7. Gilsdorf A, Jansen A, Alpers K, Dieckmann H, van Treeck U, Hauri AM, et al. A nationwide outbreak of SalmonellaBovismorbificans PT24, Germany, December 2004–March 2005. Euro Surveill. 2005;10(3):pii=2667.
  8. Rimhanen-Finne R, Niskanen T, Lienemann T, Johansson T, Sjoman M, Korhonen T, et al. A nationwide outbreak of Salmonella Bovismorbificans associated with sprouted Alfalfa seeds in Finland, 2009. Zoonoses Public Hlth. 2011;58(8):589–96.
  9. Centers for Disease Control and Prevention (CDC). Multistate outbreak of Salmonella serotype Bovismorbificans infections associated with hummus and tahini - United States, 2011. MMWR Morb Mortal Wkly Rep. 2012;61(46):944–7.
  10. National Reference Laboratory for Enteropathogenic Bacteria and Listeria (NENT), Bundesamt für Gesundheit (BAG). EPIS Alert NENT BAG 060814. 2014; Bern: NENT, BAG.
  11. Heymann DL. Control of communicable diseases manual: 19th edition. 2008. Washington DC: American Public Health Association.
  12. Bundesamt für Gesundheit (BAG). Lebensmittelbedingte Gruppenerkrankungen in der Schweiz. 2012; Bern: BAG.
  13. Miller T, Braun PG, Fehlhaber K, Prager R, Pfeifer Y, Rabsch W. Typing of Salmonella enterica serovar Infantis isolates from 51 outbreaks in Germany between 1974 and 2009 by a novel phage-typing scheme. Epidemiol Infect. 2014;142(1):75–83.
  14. Centers for Disease Control and Prevention (CDC). Standard Operating Procedure for PulseNet PFGE of Escherichia coli O157:H7, Escherichia colinon-O157 (STEC), Salmonella serotypes, Shigella sonnei and Shigella flexneri. 2013; Atlanta: Centers of Disease Control.
  15. Grimont PAD, Weill FX. Antigenic formulae of the Salmonella serovars: 9th edition. 2007; Geneva: World Health Organization Collaborating Centre for Reference and Research on Salmonella, Institut Pasteur.
  16. Liesegang A, Davos D, Balzer JC, Rabsch W, Prager R, Lightfoot D, et al. Phage typing and PFGE pattern analysis as tools for epidemiological surveillance of Salmonella enterica serovar Bovismorbificans infections. Epidemiol Infect. 2002;128(2):119–30.
  17. Landesgesundheitsamt Baden-Württemberg. Infektionsbericht Baden-Württemberg: Meldewoche 34. 2014; Stuttgart: Landesgesundheitsamt Baden-Württemberg.
  18. Van Beneden CA, Keene WE, Strang RA, Werker DH, King AS, Mahon B, et al. Multinational outbreak of Salmonella enterica serotype Newport infections due to contaminated Alfalfa sprouts. JAMA. 1999;281(2):158–62.
  19. Buchholz U, Bernard H, Werber D, Bohmer MM, Remschmidt C, Wilking H, et al. German outbreak of Escherichia coli O104:H4 associated with sprouts. N Engl J Med. 2011;365(19):1763–70.
  20. Gobin M, Launders N, Lane C, Kafatos G, Adak B. National outbreak of Salmonella Java phage type 3b variant 9 infection using parallel case-control and case-case study designs, United Kingdom, July to October 2010. Euro Surveill. 2011;16(47):pii=20023.
  21. Bayer C, Bernard H, Prager R, Rabsch W, Hiller P, Malorny B, et al. An outbreak of Salmonella Newport associated with mung bean sprouts in Germany and the Netherlands, October to November 2011. Euro Surveill. 2014;19(1):pii=20665.
  22. Bundesamt für Lebensmittelsicherheit und Veterinärwesen (BLV), Schnellwarnsystem für Lebens- und Futtermittel (RASFF). Lebensmittelüberwachung: Gutachten zu Sprossen. 2014; Bern: BLV, RASFF.
  23. Robert Koch Institute (RKI). Salmonellose (Salmonellen-Gastroenteritis): RKI-Ratgeber für Ärzte Berlin: RKI; 2011 [cited January 2015]. Available from:
  24. Refsum T, Heir E, Kapperud G, Vardund T, Holstad G. Molecular epidemiology of Salmonella enterica serovar Typhimurium isolates determined by pulsed-field gel electrophoresis: comparison of isolates from avian wildlife, domestic animals, and the environment in Norway. Appl Environ Microbiol. 2002;68(11):5600–6.
  25. Ghosh TS, Patnaik JL, Alden NB, Vogt RL. Internet- versus telephone-based local outbreak investigations. Emerg Infect Dis. 2008;14(6):975–7.
  26. Whelan J, Noel H, Friesema I, Hofhuis A, de Jager CM, Heck M, et al. National outbreak of Salmonella Typhimurium (Dutch) phage-type 132 in the Netherlands, October to December 2009. Euro Surveill. 2010;15(44):pii=19705.
  27. Raguenaud ME, Le Hello S, Salah S, Weill FX, Brisabois A, Delmas G, et al. Epidemiological and microbiological investigation of a large outbreak of monophasic Salmonella Typhimurium 4,5,12:i:- in schools associated with imported beef in Poitiers, France, October 2010. Euro Surveill. 2012;17(40):pii=20289.
  28. Kunwar R, Singh H, Mangla V, Hiremath R. Outbreak investigation: Salmonella food poisoning. Med J Armed Forces India. 2013;69(4):388–91.
  29. Oregon Health Authority. Shotgun hypothesis-generating questionnaire. 2014; Portland: Oregon Health Authority.
  30. Kiefer S, Künzli E, Hatz C. Kompetenzzentrum für epidemiologische Ausbruchsuntersuchungen: Prätest Bericht. 2013; Basel, Zürich: Swiss Tropical and Public Health Institute, Institut für Sozial- und Präventivmedizin der Universität Zürich.
  31. Hächler H, Marti G, Giannini P, Lehner A, Jost M, Beck J, et al. Outbreak of listerosis due to imported cooked ham, Switzerland 2011. Euro Surveill. 2013;18(18):pii=20469.
  32. Inns T, Beasley G, Lane C, Hopps V, Peters T, Pathak K, et al. Outbreak of Salmonella enterica Goldcoast infection associated with whelk consumption, England, June to October 2013. Euro Surveill. 2013;18(49):pii=20654.
  33. Stewart DS, Reineke KF, Ulaszek JM, Tortorello ML. Growth of Salmonelladuring sprouting of alfalfa seeds associated with salmonellosis outbreaks. J Food Prot. 2001;64(5):618–22.
  34. Safranek T, Leschinsky D, Keyser A, O'Keefe A, Timmons T, Holmes S, et al. Outbreak of Salmonella serotype Saintpaul infections associated with eating alfalfa sprouts – United States, 2009. MMWR Morb Mortal Wkly Rep. 2009;58(18):500–3.

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