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Salmonellosis remains the second most common zoonosis in the European Union despite a long-term decreasing trend. However, this trend has been reported to have stagnated in recent years, particularly for serotype Enteritidis (SE).


To describe temporal changes in the incidence of SE human infections, and in its associated factors between 2006 and 2019. In addition, we aim to determine which factors influenced the stagnated trend seen in recent years.


Data on culture-confirmed SE human infections from national surveillance registries in the Netherlands and Belgium between 2006 and 2019 were analysed using multivariable negative-binomial regression models with restricted cubic splines.


SE incidence was significantly higher in summer and autumn than winter, in persons aged 0–4 years and 5–14 years than in persons ≥ 60 years, and increased with increasing proportions of travel-related and resistant SE infections. SE incidence decreased significantly in both countries until 2015, followed by an increasing trend, which was particularly pronounced in the Netherlands. Potential SE outbreaks in both countries and invasive infections in the Netherlands also increased after 2015.


The increase in potential outbreaks and invasive infections since 2015 may partially explain the observed reversal of the decreasing trend. While these results provide insights into the possible causes of this trend reversal, attention should also be given to factors known to influence SE epidemiology at primary (animal) production and pathogen genomic levels.


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  1. European Food Safety AuthorityEuropean Centre for Disease Prevention and Control. The European Union One Health 2019 Zoonoses Report. EFSA J. 2021;19(2):e06406. PMID: 33680134 
  2. World Health Organization (WHO). Salmonella (non-typhoidal). Geneva: WHO; 20 Feb 2018. Available from: https://www.who.int/news-room/fact-sheets/detail/salmonella-(non-typhoidal).
  3. Acheson D,, Hohmann EL. Nontyphoidal salmonellosis. Clin Infect Dis. 2001;32(2):263-9.  https://doi.org/10.1086/318457  PMID: 11170916 
  4. Mughini-Gras L, Pijnacker R, Duijster J, Heck M, Wit B, Veldman K, et al. Changing epidemiology of invasive non-typhoid Salmonella infection: a nationwide population-based registry study. Clin Microbiol Infect. 2020;26(7):941.e9-.e14.
  5. Nationaal Referentie Centrum voor Salmonella & Shigell. 2020. Jaarverslag 2020. [Annual report]. Sciensano: Brussels; Jun 2021. Dutch. Available from: https://nrchm.wiv-isp.be/nl/ref_centra_labo/salmonella_shigella/Rapporten/Salmonella%202020.pdf
  6. Issenhuth-Jeanjean S, Roggentin P, Mikoleit M, Guibourdenche M, de Pinna E, Nair S, et al. Supplement 2008-2010 (no. 48) to the White-Kauffmann-Le Minor scheme. Res Microbiol. 2014;165(7):526-30.  https://doi.org/10.1016/j.resmic.2014.07.004  PMID: 25049166 
  7. Dekker JP, Frank KM. Salmonella, Shigella, and yersinia. Clin Lab Med. 2015;35(2):225-46.  https://doi.org/10.1016/j.cll.2015.02.002  PMID: 26004640 
  8. Dougan G, Baker S. Salmonella enterica serovar Typhi and the pathogenesis of typhoid fever. Annu Rev Microbiol. 2014;68(1):317-36.  https://doi.org/10.1146/annurev-micro-091313-103739  PMID: 25208300 
  9. European Food Safety Authority and European Centre for Disease Prevention and Control. The community summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in the European Union in 2008. EFSA J. 2010;8(1).
  10. European Food Safety AuthorityEuropean Centre for Disease Prevention and Control. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food‐borne outbreaks in 2012. EFSA J. 2014;12(2).
  11. European Food Safety AuthorityEuropean Centre for Disease Prevention and Control. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016. EFSA J. 2017;15(12):e05077. PMID: 32625371 
  12. Koutsoumanis K, Allende A, Alvarez-Ordóñez A, Bolton D, Bover-Cid S, Chemaly M, et al. Salmonella control in poultry flocks and its public health impact. EFSA J. 2019;17(2):e05596. PMID: 32626222 
  13. Kuehn BM. Salmonella cases traced to egg producers: findings trigger recall of more than 500 million eggs. JAMA. 2010;304(12):1316.  https://doi.org/10.1001/jama.2010.1330  PMID: 20858872 
  14. Doorduyn Y, Van Den Brandhof WE, Van Duynhoven YTHP, Wannet WJB, Van Pelt W. 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. Epidemiol Infect. 2006;134(3):617-26.  https://doi.org/10.1017/S0950268805005406  PMID: 16638166 
  15. Jajere SM. A review of Salmonella enterica with particular focus on the pathogenicity and virulence factors, host specificity and antimicrobial resistance including multidrug resistance. Vet World. 2019;12(4):504-21.  https://doi.org/10.14202/vetworld.2019.504-521  PMID: 31190705 
  16. van Pelt W, de Wit MA, Wannet WJ, Ligtvoet EJ, Widdowson MA, van Duynhoven YT. Laboratory surveillance of bacterial gastroenteric pathogens in The Netherlands, 1991-2001. Epidemiol Infect. 2003;130(3):431-41.  https://doi.org/10.1017/S0950268803008392  PMID: 12825727 
  17. Mughini-Gras L, Heck M, van Pelt W. Increase in reptile-associated human salmonellosis and shift toward adulthood in the age groups at risk, the Netherlands, 1985 to 2014. Euro Surveill. 2016;21(34):30324.  https://doi.org/10.2807/1560-7917.ES.2016.21.34.30324  PMID: 27589037 
  18. van Duijkeren E, Wannet WJ, Houwers DJ, van Pelt W. Serotype and phage type distribution of salmonella strains isolated from humans, cattle, pigs, and chickens in the Netherlands from 1984 to 2001. J Clin Microbiol. 2002;40(11):3980-5.  https://doi.org/10.1128/JCM.40.11.3980-3985.2002  PMID: 12409362 
  19. Statistics Netherlands (CBS). The Hague. [Accessed: 20 Sep 2022]. Available from: https://www.cbs.nl/en.
  20. Van Goethem N, Van Den Bossche A, Ceyssens P-J, Lajot A, Coucke W, Vernelen K, et al. Coverage of the national surveillance system for human Salmonella infections, Belgium, 2016-2020. PLoS One. 2021;16(8):e0256820.  https://doi.org/10.1371/journal.pone.0256820  PMID: 34437638 
  21. Directorate General Statistics - Statistics Belgium (Statbel). Brussels. [Accessed: 20 Sep 2022]. Available from: https://statbel.fgov.be/en
  22. May M. Regression Modelling Strategies with Applications to Linear Models, Logistic Regression, and Survival Analysis. Int J Epidemiol. 2002;31(3):699-700.  https://doi.org/10.1093/ije/31.3.699 
  23. European Food Safety Authority and European Centre for Disease Prevention and Control (EFSA and ECDC). The European Union One Health 2018 Zoonoses Report. EFSA J. 2019;17(12):e05926. PMID: 32626211 
  24. Ekdahl K, de Jong B, Wollin R, Andersson Y. Travel-associated non-typhoidal salmonellosis: geographical and seasonal differences and serotype distribution. Clin Microbiol Infect. 2005;11(2):138-44.  https://doi.org/10.1111/j.1469-0691.2004.01045.x  PMID: 15679488 
  25. Mughini-Gras L, Enserink R, Friesema I, Heck M, van Duynhoven Y, van Pelt W. Risk factors for human salmonellosis originating from pigs, cattle, broiler chickens and egg laying hens: a combined case-control and source attribution analysis. PLoS One. 2014;9(2):e87933.  https://doi.org/10.1371/journal.pone.0087933  PMID: 24503703 
  26. Al-Mashhadani M, Hewson R, Vivancos R, Keenan A, Beeching NJ, Wain J, et al. Foreign travel and decreased ciprofloxacin susceptibility in Salmonella enterica infections. Emerg Infect Dis. 2011;17(1):123-5.  https://doi.org/10.3201/eid1701.100999  PMID: 21192872 
  27. de Jong B, Ekdahl K. The comparative burden of salmonellosis in the European Union member states, associated and candidate countries. BMC Public Health. 2006;6(1):4.  https://doi.org/10.1186/1471-2458-6-4  PMID: 16403230 
  28. Rodríguez I, Rodicio MR, Guerra B, Hopkins KL. Potential international spread of multidrug-resistant invasive Salmonella enterica serovar enteritidis. Emerg Infect Dis. 2012;18(7):1173-6.  https://doi.org/10.3201/eid1807.120063  PMID: 22709653 
  29. European Centre for Disease Prevention and Control (ECDC). Joint rapid outbreak assessment: Multi-country outbreak of Salmonella Enteritidis infections linked to Polish eggs. Stockholm: ECDC; 2017. Available from: https://www.ecdc.europa.eu/en/publications-data/joint-rapid-outbreak-assessment-multi-country-outbreak-salmonella-enteritidis-0
  30. Rijksinstituut voor Volksgezondheid en Milieu (RIVM). Staat van Zoönosen 2020. [State of zoonoses 2020]. Bilthoven: RIVM; 2021.
  31. Nationaal Referentie Centrum voor Salmonella. Jaarverslag 2019. [Annual report 2019]. Sciensano: Brussels. Jun 2020. Dutch. Available from: https://nrchm.wiv-isp.be/nl/ref_centra_labo/salmonella_shigella/Rapporten/Jaarverslag%20Salm%20Shig%202019_NL.pdf

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