1. An international outbreak of Salmonella enterica serotype Enteritidis linked to eggs from Poland: a microbiological and epidemiological study
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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 Müller, Daniel 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, Graduate School, AII - Infectious diseases, National Institute for Public Health and the Environment [Bilthoven] (RIVM), Public Health England [London], Netherlands Food and Consumer Product Safety Authority (NVWA), Health Protection Scotland, European Centre for Disease Prevention and Control [Stockholm, Sweden] (ECDC), European Food Safety Authority (EFSA), European Commission [Brussels], Sciensano [Bruxelles], Réseau International des Instituts Pasteur (RIIP), National Centre for Epidemiology (NCE), Norwegian Institute of Public Health [Oslo] (NIPH), NHS Greater Glasgow and Clyde, Laboratoire National de Santé [Luxembourg] (LNS), Public Health Agency of Sweden, Statens Serum Institut [Copenhagen], Independent Author, Croatian Institute of Public Health [Zagreb] (CIPH), Istituto Superiore di Sanità (ISS), Institut Pasteur [Paris] (IP), Health Protection Surveillance Centre (HPSC), UMR 212 EME 'écosystèmes marins exploités' (EME), Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Montpellier (UM), School of Chemistry [Southampton, UK], University of Southampton, Department of Infectious, Centre National de Référence - National Reference Center Escherichia coli, Shigella et Salmonella (CNR-ESS), Institut de Veille Sanitaire (INVS), Stobhill Hospital, Durrell Institute of Conservation and Ecology, University of Kent [Canterbury], Department of Microbiology, National Veterinary Research Institute [Pulawy, Pologne] (NVRI), This study received funding from the European Centre for Disease Prevention and Control, the Directorate General for Health and Food Safety of the European Commission, and the following national public health and food safety institutes: the National Institute for Public Health and the Environment (Netherlands), Public Health England, Health Protection Scotland, the National Institute for Public Health (Sciensano, Belgium), National Centre for Epidemiology (Hungary), the Norwegian Institute for Public Health, the National Health Laboratory (Luxembourg), the Public Health Agency of Sweden, Statens Serum Institut (Denmark), the Croatian Institute of Public Health, Instituto Superiore di Sanità (Italy), Institut Pasteur (France), Health Protection Surveillance Centre (Ireland), the Netherlands Food and Consumer Product Safety Authority, the Chief Veterinary Inspectorate (Poland), the Scottish Salmonella, Shigella, and Clostridium difficile Reference Laboratory, and the European Union Reference Laboratory for Salmonella (Netherlands). VR and GA are employed with the European Food Safety Authority (EFSA) in its BIOCONTAM Unit that provides scientific and administrative support to EFSA's scientific activities in the area of microbiological risk assessment. PMS and EA are employed with the European Commission at the Directorate-General for Health and Food Safety. The positions and opinions presented in this Article are those of the authors alone and are not intended to represent the views or scientific works of the European Commission or EFSA., International Outbreak Investigation Team 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, Sanja Kurečić Filipović, Ife Fitz-James, Karolina Florek, Martina Florianová, Eithne Fox, Tatjana Frelih, Eva Grilc, Vera Katalinic Jankovic, Nathalie Jourdan, Renata Karpíšková, Hans van den Kerkhof, Katalin Krisztalovics, Sjoerd Kuiling, 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., European Centre for Disease Prevention and Control (ECDC), Istituto Superiore di Sanita [Rome], Institut Pasteur [Paris], and Université de Montpellier (UM)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Institut de Recherche pour le Développement (IRD)
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Male ,0301 basic medicine ,Serotype ,Salmonella ,medicine.medical_specialty ,Eggs ,Population ,Serogroup ,medicine.disease_cause ,Disease Outbreaks ,03 medical and health sciences ,0302 clinical medicine ,Environmental health ,Epidemiology ,medicine ,Humans ,Life Science ,030212 general & internal medicine ,education ,2. Zero hunger ,education.field_of_study ,Whole Genome Sequencing ,biology ,business.industry ,Public health ,Outbreak ,biology.organism_classification ,Food safety ,[SDV.MP.BAC]Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology ,3. Good health ,Europe ,Epidemiologic Studies ,[SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology ,030104 developmental biology ,Infectious Diseases ,Salmonella enteritidis ,Salmonella enterica ,Case-Control Studies ,[SDV.MP.VIR]Life Sciences [q-bio]/Microbiology and Parasitology/Virology ,Female ,Salmonella Food Poisoning ,Poland ,business - Abstract
Summary 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).
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- 2019
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