An international outbreak of Salmonella enterica serotype Enteritidis linked to eggs from Poland: a microbiological and epidemiological study

Roan Pijnacker, Timothy J. Dallman, Aloys S. L. Tijsma, Gillian Hawkins, Lesley Larkin, Saara M. Kotila, Giusi Amore, Ettore Amato, Pamina M. Suzuki, Sarah Denayer, Sofieke Klamer, Judit Pászti, Jacquelyn McCormick, Hassan Hartman, Gareth J. Hughes, Lin C. T. Brandal, Derek Brown, Joël Mossong, Cecilia Jernberg, Luise MüllerDaniel Palm, Ettore Severi, Joannna Gołębiowska, Blaženka Hunjak, Slawomir Owczarek, Simon le Hello, Patricia Garvey, Kirsten Mooijman, Ingrid H. M. Friesema, Coen van der Weijden, Menno van der Voort, Valentina Rizzi, Eelco Franz, Sophie Bertrand, Martine Brennan, Lynda Browning, Ryan Bruce, Vera Cantaert, Marie Chattaway, John Coia, Sarah Couper, Tjaša Žohar Čretnik, Ondřej Daniel, Anna Maria Dionisi, Laetitia Fabre, Ife Fitz-James, Karolina Florek, Martina Florianová, Eithne Fox, Tatjana Frelih, Eva Grilc, Vera Katalinic Jankovic, Nathalie Jourdan, Renata Karpíšková, Hans van den Kerkhof, Sjoerd Kuiling, Sanja Kurečić Filipović, Valeska Laisnez, Heidi Lange, Niall deLappes, Judith Leblanc, Ida Luzzi, Georgia Mandilara, Henry Mather, Wesley Mattheus, Kassiani Mellou, Deborah Morgan, Elizabeth de Pinna, Catherine Ragimbeau, Margrethe Hovda Røed, Saara Salmenlinna, Robert Smith, Alison Smith-Palmer, Michaela Špačková, Mia Torpdahl, Marija Trkov, Linda Trönnberg, Myrsini Tzani, Lara Utsi, Dariusz Wasyl, Pierre Weicherding

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Background: Salmonella spp are a major cause of food-borne outbreaks in Europe. We investigated a large multi-country outbreak of Salmonella enterica serotype Enteritidis in the EU and European Economic Area (EEA). Methods: A confirmed case was defined as a laboratory-confirmed infection with the outbreak strains of S Enteritidis based on whole-genome sequencing (WGS), occurring between May 1, 2015, and Oct 31, 2018. A probable case was defined as laboratory-confirmed infection with S Enteritidis with the multiple-locus variable-number tandem repeat analysis outbreak profile. Multi-country epidemiological, trace-back, trace-forward, and environmental investigations were done. We did a case-control study including confirmed and probable cases and controls randomly sampled from the population registry (frequency matched by age, sex, and postal code). Odds ratios (ORs) for exposure rates between cases and controls were calculated with unmatched univariable and multivariable logistic regression. Findings: 18 EU and EEA countries reported 838 confirmed and 371 probable cases. 509 (42%) cases were reported in 2016, after which the number of cases steadily increased. The case-control study results showed that cases more often ate in food establishments than did controls (OR 3·4 [95% CI 1·6–7·3]), but no specific food item was identified. Recipe-based food trace-back investigations among cases who ate in food establishments identified eggs from Poland as the vehicle of infection in October, 2016. Phylogenetic analysis identified two strains of S Enteritidis in human cases that were subsequently identified in salmonella-positive eggs and primary production premises in Poland, confirming the source of the outbreak. After control measures were implemented, the number of cases decreased, but increased again in March, 2017, and the increase continued into 2018. Interpretation: This outbreak highlights the public health value of multi-country sharing of epidemiological, trace-back, and microbiological data. The re-emergence of cases suggests that outbreak strains have continued to enter the food chain, although changes in strain population dynamics and fewer cases indicate that control measures had some effect. Routine use of WGS in salmonella surveillance and outbreak response promises to identify and stop outbreaks in the future. Funding: European Centre for Disease Prevention and Control; Directorate General for Health and Food Safety, European Commission; and National Public Health and Food Safety Institutes of the authors' countries (see Acknowledgments for full list).
Original languageEnglish
Pages (from-to)778-786
JournalLancet infectious diseases
Issue number7
Publication statusPublished - 2019

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