1887
  1. Home
  2. Eurosurveillance
  3. Volume 29, Issue 10, 07/Mar/2024
  4. Article
Outbreaks Open Access
Like 0
Download

Abstract

In September 2022, the Public Health Agency of Sweden observed an increase in domestic Typhimurium cases through the Swedish electronic notification system, and an outbreak strain was identified with whole genome sequencing. Overall, 109 cases with symptom onset between 17 September and 24 November 2022 were reported from 20 of 21 Swedish regions. The median age of cases was 52 years (range 4–87 years) and 62% were female. A case–control study found cases to be associated with consumption of rocket salad (adjusted odds ratio (aOR) = 4.9; 95% confidence interval (CI): 2.4–10, p value < 0.001) and bagged mixed salad (aOR = 4.0; 95% CI: 1.9–8.1, p value < 0.001). Trace-back, supported by Finnish authorities who identified the Swedish outbreak strain in a Finnish cluster during the same time period, identified rocket salad, cultivated, pre-washed and pre-packed in Sweden as the likely source of the outbreak. No microbiological analyses of rocket salad were performed. Our investigation indicates that bagged leafy greens such as rocket salad, regardless of pre-washing procedures in the production chain, may contain and cause outbreaks, posing a health risk to consumers. We emphasise the need for primary producers of leafy greens to identify possible contamination points to prevent outbreaks.

© Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2024.29.10.2300299
2024-03-07
2024-11-21
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2024.29.10.2300299
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/29/10/eurosurv-29-10-3.html?itemId=/content/10.2807/1560-7917.ES.2024.29.10.2300299&mimeType=html&fmt=ahah

References

  1. European Centre for Disease Prevention and Control (ECDC). Salmonellosis - Annual Epidemiological Report for 2021. Stockholm: ECDC; Dec 2022. Available from: https://www.ecdc.europa.eu/sites/default/files/documents/SALM_AER_2021.pdf
  2. Sveriges Riksdag. Socialdepartementet. Smittskyddslag (2004:168). [Infectious Disease Act (2004:168)]. Stockholm: Sveriges Riksdag; 2004. Swedish. Available from: https://www.riksdagen.se/sv/dokument-och-lagar/dokument/svensk-forfattningssamling/smittskyddslag-2004168_sfs-2004-168/
  3. Public Health Agency of Sweden (PHAS). Salmonella – Sjukdomsstatistik. [Salmonella – Disease Statistics]. Stockholm: PHAS [Accessed: 22 Nov 2023]. Swedish. Available from: https://www.folkhalsomyndigheten.se/folkhalsorapportering-statistik/statistik-a-o/sjukdomsstatistik/salmonellainfektion?tab=tab-report
  4. Pires SM, Vieira AR, Hald T, Cole D. Source attribution of human salmonellosis: an overview of methods and estimates. Foodborne Pathog Dis. 2014;11(9):667-76.  https://doi.org/10.1089/fpd.2014.1744  PMID: 24885917 
  5. European Food Safety AuthorityEuropean Centre for Disease Prevention and Control. The European Union One Health 2021 Zoonoses Report. EFSA J. 2022;20(12):e07666. PMID: 36524203 
  6. EFSA Panel on Biological Hazards (BIOHAZ) Panel. Scientific Opinion on the risk posed by pathogens in food of non-animal origin. Part 1 (outbreak data analysis and risk ranking of food/pathogen combinations). EFSA J. 2013;11(1):3025.  https://doi.org/10.2903/j.efsa.2013.3025 
  7. EFSA Panel on Biological Hazards (BIOHAZ). Scientific Opinion on the risk posed by pathogens in food of non-animal origin. Part 2 (Salmonella and Norovirus in leafy greens eaten raw as salads). EFSA J. 2014;12(3):3600.
  8. Swedish Food Agency (SFA). Riksmaten vuxna 2010-11 – Livsmedels- och näringsintag bland vuxna i Sverige. [Riksmaten adults 2010-11 – Intake of food and nutrients among adults in Sweden]. Uppsala: SFA; Sep 2012. Swedish. Available from: https://www.livsmedelsverket.se/matvanor-halsa--miljo/matvanor---undersokningar/riksmaten-2010-11---vuxna
  9. Keene B The Use of Binomial Probabilities in Outbreak Investigations. 7th Association of Public Health Laboratories (APHL) 7th Annual OutbreakNet Meeting; Sep 2011, Long Beach, United States. Available from: https://www.aphl.org/conferences/proceedings/Documents/2011/PulseNet-OutbreakNet/017-Kenne.pdf
  10. Grimont PAD, Weill F-X. Antigenic formulae of the Salmonella serovars. Paris: WHO Collaborating Centre for Reference and Research on Salmonella; 2007. Available from: https://www.pasteur.fr/sites/default/files/veng_0.pdf
  11. Achtman M, Zhou Z, Alikhan NF, Tyne W, Parkhill J, Cormican M, et al. Genomic diversity of Salmonella enterica -The UoWUCC 10K genomes project. Wellcome Open Res. 2021;5:223.  https://doi.org/10.12688/wellcomeopenres.16291.2  PMID: 33614977 
  12. Alikhan NF, Zhou Z, Sergeant MJ, Achtman M. A genomic overview of the population structure of Salmonella. PLoS Genet. 2018;14(4):e1007261.  https://doi.org/10.1371/journal.pgen.1007261  PMID: 29621240 
  13. Zhou Z, Alikhan NF, Mohamed K, Fan Y, Agama Study Group, Achtman M. The EnteroBase user’s guide, with case studies on Salmonella transmissions, Yersinia pestis phylogeny, and Escherichia core genomic diversity. Genome Res. 2020;30(1):138-52.  https://doi.org/10.1101/gr.251678.119  PMID: 31809257 
  14. Zhang S, Yin Y, Jones MB, Zhang Z, Deatherage Kaiser BL, Dinsmore BA, et al. Salmonella serotype determination utilizing high-throughput genome sequencing data. J Clin Microbiol. 2015;53(5):1685-92.  https://doi.org/10.1128/JCM.00323-15  PMID: 25762776 
  15. Feldgarden M, Brover V, Gonzalez-Escalona N, Frye JG, Haendiges J, Haft DH, et al. AMRFinderPlus and the Reference Gene Catalog facilitate examination of the genomic links among antimicrobial resistance, stress response, and virulence. Sci Rep. 2021;11(1):12728.  https://doi.org/10.1038/s41598-021-91456-0  PMID: 34135355 
  16. Salipante SJ, Hall BG. Inadequacies of minimum spanning trees in molecular epidemiology. J Clin Microbiol. 2011;49(10):3568-75.  https://doi.org/10.1128/JCM.00919-11  PMID: 21849692 
  17. Strassle PD, Gu W, Bruce BB, Gould LH. Sex and age distributions of persons in foodborne disease outbreaks and associations with food categories. Epidemiol Infect. 2019;147:e200.  https://doi.org/10.1017/S0950268818003126  PMID: 31364541 
  18. Kays R, Davidson SC, Berger M, Bohrer G, Fiedler W, Flack A, et al. The Movebank system for studying global animal movement and demography. Methods Ecol Evol. 2022;13(2):419-31.  https://doi.org/10.1111/2041-210X.13767 
  19. Palmgren H, Aspán A, Broman T, Bengtsson K, Blomquist L, Bergström S, et al. Salmonella in black-headed gulls (Larus ridibundus); prevalence, genotypes and influence on Salmonella epidemiology. Epidemiol Infect. 2006;134(3):635-44.  https://doi.org/10.1017/S0950268805005261  PMID: 16238820 
  20. MacDonald E, Einöder-Moreno M, Borgen K, Thorstensen Brandal L, Diab L, Fossli Ø, et al. National outbreak of Yersinia enterocolitica infections in military and civilian populations associated with consumption of mixed salad, Norway, 2014. Euro Surveill. 2016;21(34):30321.  https://doi.org/10.2807/1560-7917.ES.2016.21.34.30321  PMID: 27588690 
  21. Nygård K, Lassen J, Vold L, Andersson Y, Fisher I, Löfdahl S, et al. Outbreak of Salmonella Thompson infections linked to imported rucola lettuce. Foodborne Pathog Dis. 2008;5(2):165-73.  https://doi.org/10.1089/fpd.2007.0053  PMID: 18361685 
  22. Vestrheim DF, Lange H, Nygård K, Borgen K, Wester AL, Kvarme ML, et al. Are ready-to-eat salads ready to eat? An outbreak of Salmonella Coeln linked to imported, mixed, pre-washed and bagged salad, Norway, November 2013. Epidemiol Infect. 2016;144(8):1756-60.  https://doi.org/10.1017/S0950268815002769  PMID: 26586305 
  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. Söderström A, Lindberg A, Andersson Y. EHEC O157 outbreak in Sweden from locally produced lettuce, August-September 2005. Euro Surveill. 2005;10(9):E050922.1. PMID: 16788234 
  25. Barratt J, Ahart L, Rice M, Houghton K, Richins T, Cama V, et al. Genotyping Cyclospora cayetanensis from multiple outbreak clusters with an emphasis on a cluster linked to bagged salad mix-United States, 2020. J Infect Dis. 2022;225(12):2176-80.  https://doi.org/10.1093/infdis/jiab495  PMID: 34606577 
  26. McKerr C, Adak GK, Nichols G, Gorton R, Chalmers RM, Kafatos G, et al. An outbreak of Cryptosporidium parvum across England & Scotland associated with consumption of fresh pre-cut salad leaves, May 2012. PLoS One. 2015;10(5):e0125955.  https://doi.org/10.1371/journal.pone.0125955  PMID: 26017538 
  27. Swedish Food Agency (SFA). Bevattningsvatten. [Irrigation water]. Uppsala: SFA; 2019. Swedish. Available from: https://www.livsmedelsverket.se/globalassets/publikationsdatabas/rapporter/2019/s-2019-nr-02---bevattningsvatten.pdf
  28. Sant’Ana AS, Barbosa MS, Destro MT, Landgraf M, Franco BD. Growth potential of Salmonella spp. and Listeria monocytogenes in nine types of ready-to-eat vegetables stored at variable temperature conditions during shelf-life. Int J Food Microbiol. 2012;157(1):52-8.  https://doi.org/10.1016/j.ijfoodmicro.2012.04.011  PMID: 22561064 
  29. Koukkidis G, Haigh R, Allcock N, Jordan S, Freestone P. Salad leaf juices enhance Salmonella growth, colonization of fresh produce, and virulence. Appl Environ Microbiol. 2016;83(1):e02416-16. https://doi.org/10.1128/AEM.02416-16  PMID: 27864173 
  30. Pezzuto A, Belluco S, Losasso C, Patuzzi I, Bordin P, Piovesana A, et al. Effectiveness of washing procedures in reducing Salmonella enterica and Listeria monocytogenes on a raw leafy green vegetable (Eruca vesicaria). Front Microbiol. 2016;7:1663.  https://doi.org/10.3389/fmicb.2016.01663  PMID: 27812356 
  31. Huang J, Luo Y, Zhou B, Zheng J, Nou X. Growth and survival of Salmonella enterica and Listeria monocytogenes on fresh-cut produce and their juice extracts: Impacts and interactions of food matrices and temperature abuse conditions. Food Control. 2019;100(6):300-4.  https://doi.org/10.1016/j.foodcont.2018.12.035 
  32. de Frias AJ, Luo Y, Zhou B, Turner ER, Millner PD, Nou X. Minimizing pathogen growth and quality deterioration of packaged leafy greens by maintaining optimum temperature in refrigerated display cases with doors. Food Control. 2018;92:488-95.  https://doi.org/10.1016/j.foodcont.2018.05.024 
  33. Swedish Food Agency (SFA). Avsvalning och förvaring. [Cooling and storage]. Uppsala: SFA. [Accessed: 4 Apr 2023]. Swedish. Available from: https://www.livsmedelsverket.se/livsmedel-och-innehall/tillagning-och-forvaring/avsvalning-forvaring
  34. Marklinder IM, Lindblad M, Eriksson LM, Finnson AM, Lindqvist R. Home storage temperatures and consumer handling of refrigerated foods in Sweden. J Food Prot. 2004;67(11):2570-7.  https://doi.org/10.4315/0362-028X-67.11.2570  PMID: 15553644 
  35. Mogren L, Windstam S, Boqvist S, Vågsholm I, Söderqvist K, Rosberg AK, et al. The hurdle approach-a holistic concept for controlling food safety risks associated with pathogenic bacterial contamination of leafy green vegetables. A review. Front Microbiol. 2018;9:1965.  https://doi.org/10.3389/fmicb.2018.01965  PMID: 30197634 
Outbreak of Salmonella Typhimurium linked to Swedish pre-washed rocket salad, Sweden, September to November 2022
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Karolina+Fischerstr%C3%B6m&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Fischerström Karolina</a>, <a href="/search?value1=Rikard+Dryselius&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Dryselius Rikard</a>, <a href="/search?value1=Mats+Lindblad&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Lindblad Mats</a>, <a href="/search?value1=Sharon+K%C3%BChlmann-Berenzon&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Kühlmann-Berenzon Sharon</a>, <a href="/search?value1=Nadja+Karamehmedovic&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Karamehmedovic Nadja</a>, <a href="/search?value1=Stefan+B%C3%B6rjesson&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Börjesson Stefan</a>, <a href="/search?value1=Nasanin+Hashemi&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Hashemi Nasanin</a>, <a href="/search?value1=Ingrid+Gunn&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Gunn Ingrid</a>, <a href="/search?value1=Ann-Mari+Gustavsson&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Gustavsson Ann-Mari</a>, <a href="/search?value1=Nilla+Lindroos&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Lindroos Nilla</a>, <a href="/search?value1=Joanna+Nederby-%C3%96hd&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Nederby-Öhd Joanna</a>, <a href="/search?value1=Micael+Widerstr%C3%B6m&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Widerström Micael</a>, <a href="/search?value1=Ruska+Rimhanen-Finne&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Rimhanen-Finne Ruska</a>, <a href="/search?value1=Anni+Vainio&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Vainio Anni</a>, <a href="/search?value1=Moa+Rehn&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Rehn Moa</a></span>. Outbreak of Salmonella Typhimurium linked to Swedish pre-washed rocket salad, Sweden, September to November 2022. <a href="/content/ecdc">Euro Surveill.</a> 2024;29(10):pii=2300299. <a href="https://doi.org/10.2807/1560-7917.ES.2024.29.10.2300299" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2024.29.10.2300299</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 05 Jun 2023;&nbsp;&nbsp; <span class="generated">Accepted</span>: 04 Dec 2023 </span> </p>
/content/10.2807/1560-7917.ES.2024.29.10.2300299
/content/10.2807/1560-7917.ES.2024.29.10.2300299
Loading

Data & Media loading...

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