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

Roan Pijnacker (1) , Timothy Dallman (2) , Aloys Tijsma (3) , Gillian Hawkins (4) , Lesley Larkin (2) , Saara Kotila (5) , Giusi Amore (6) , Ettore Amato (7) , Pamina Suzuki (7) , Sarah Denayer (8) , Sofieke Klamer (8) , Judit Pászti (9) , Jacquelyn Mccormick (2) , Hassan Hartman (2) , Gareth J Hughes (2) , Lin C.T Brandal (10) , Derek Brown (11) , Joel Mossong (12) , Cecilia Jernberg (13) , Luise Müller (14) , Daniel Palm (5) , Ettore Severi (5) , Joannna Gołębiowska (15) , Blaženka Hunjak (16) , Slawomir Owczarek (17) , Simon Le Hello (18) , Patricia Garvey (19) , Kirsten Mooijman (7) , Ingrid Friesema (1) , Coen van Der Weijden (3) , Menno van Der Voort (3) , Valentina Rizzi (6) , Eelco Franz (1) , Sophie Bertrand (20) , Martine Brennan , Lynda Brown (21) , Ryan Bruce , Vera Cantaert , Marie Chattaway , John Coia , Sarah Couper , Tjaša Žohar Čretnik , Daniel Daniel , Anna Maria Dionisi (22) , Laetitia Fabre (23) , Ife Fitz-James , Karolina Florek , Martina Florianová , Eithne Fox , Tatjana Frelih , Eva Grilc , Vera Katalinic Jankovic , Nathalie Jourdan (24) , Renata Karpíšková , Hans van den Kerkhof , Sjoerd Kuiling , Sanja Kurečić Filipović , Valeska Laisnez , Heidi Lange , Niall Delappes , Judit Leblanc , Ida Luzzi (22) , Georgia Mandilara , Henry Mather (25) , Wesley Mattheus , Kassiani Mellou , Deborah Morgan , Elizabeth de Pinna (2) , Catherine Ragimbeau , Margrethe Hovda Røed , Saara Salmenlinna , Robert Smith (26) , Alison Palm , Michaela Špačková , Mia Torpdahl , Marija Trkov , Lin Trönnberg , Myrsini Tzani , Lara Utsi , Dariusz Wasyl (27) , Pierre Weicherding

1 RIVM - National Institute for Public Health and the Environment [Bilthoven]
2 Public Health England [London]
3 NVWA - Netherlands Food and Consumer Product Safety Authority
4 Health Protection Scotland
5 ECDC - European Centre for Disease Prevention and Control
6 EFSA - European Food Safety Authority
7 European Commission [Brussels]
8 Sciensano [Bruxelles]
9 National Centre for Epidemiology (NCE)
10 NIPH - Norwegian Institute of Public Health [Oslo]
11 NHS Greater Glasgow and Clyde
12 LNS - Laboratoire National de Santé [Luxembourg]
13 Public Health Agency of Sweden
14 Statens Serum Institut [Copenhagen]
15 Independent Author
16 CIPH - Croatian Institute of Public Health [Zagreb]
17 Istituto Superiore di Sanita [Rome]
18 IP - Institut Pasteur [Paris]
19 HPSC - Health Protection Surveillance Centre
20 EME - UMR 212 EME "écosystèmes marins exploités"
21 School of Chemistry [Southampton, UK]
22 Department of Infectious
23 CNR-ESS - Centre National de Référence - National Reference Center Escherichia coli, Shigella et Salmonella
24 INVS - Institut de Veille Sanitaire
25 Stobhill Hospital
26 Durrell Institute of Conservation and Ecology
27 Department of Microbiology

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.

Domains: Life Sciences [q-bio]; Microbiology and Parasitology; Virology; Life Sciences [q-bio]; Microbiology and Parasitology; Bacteriology; Life Sciences [q-bio]; Microbiology and Parasitology

Roan Pijnacker, Timothy Dallman, Aloys Tijsma, Gillian Hawkins, Lesley Larkin, et al.. An international outbreak of Salmonella enterica serotype Enteritidis linked to eggs from Poland: a microbiological and epidemiological study. The Lancet Infectious Diseases, 2019, 19 (7), pp.778-786. ⟨10.1016/S1473-3099(19)30047-7⟩. ⟨hal-02152665⟩