{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,26]],"date-time":"2026-09-26T10:39:17Z","timestamp":1790419157473,"version":"4.1.0"},"reference-count":55,"publisher":"Microbiology Society","issue":"4","license":[{"start":{"date-parts":[[2021,4,22]],"date-time":"2021-04-22T00:00:00Z","timestamp":1619049600000},"content-version":"unspecified","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2021,4,22]]},"abstract":"Food-borne outbreak investigation currently relies on the time-consuming and challenging bacterial isolation from food, to be able to link food-derived strains to more easily obtained isolates from infected people. When no food isolate can be obtained, the source of the outbreak cannot be unambiguously determined. Shotgun metagenomics approaches applied to the food samples could circumvent this need for isolation from the suspected source, but require downstream strain-level data analysis to be able to accurately link to the human isolate. Until now, this approach has not yet been applied outside research settings to analyse real food-borne outbreak samples. In September 2019, a \n \n Salmonella<\/jats:ext-link>\n <\/jats:named-content>\n <\/jats:italic> outbreak occurred in a hotel school in Bruges, Belgium, affecting over 200 students and teachers. Following standard procedures, the Belgian National Reference Center for human salmonellosis and the National Reference Laboratory for \n \n Salmonella<\/jats:ext-link>\n <\/jats:named-content>\n <\/jats:italic> in food and feed used conventional analysis based on isolation, serotyping and MLVA (multilocus variable number tandem repeat analysis) comparison, followed by whole-genome sequencing, to confirm the source of the contamination over 2\u2009weeks after receipt of the sample, which was freshly prepared tartar sauce in a meal cooked at the school. Our team used this outbreak as a case study to deliver a proof of concept for a short-read strain-level shotgun metagenomics approach for source tracking. We received two suspect food samples: the full meal and some freshly made tartar sauce served with this meal, requiring the use of raw eggs. After analysis, we could prove, without isolation, that \n \n Salmonella<\/jats:ext-link>\n <\/jats:named-content>\n <\/jats:italic> was present in both samples, and we obtained an inferred genome of a \n \n Salmonella enterica<\/jats:ext-link>\n <\/jats:named-content>\n <\/jats:italic> subsp. \n \n enterica<\/jats:ext-link>\n <\/jats:named-content>\n <\/jats:italic> serovar Enteritidis that could be linked back to the human isolates of the outbreak in a phylogenetic tree. These metagenomics-derived outbreak strains were separated from sporadic cases as well as from another outbreak circulating in Europe at the same time period. This is, to our knowledge, the first \n \n Salmonella<\/jats:ext-link>\n <\/jats:named-content>\n <\/jats:italic> food-borne outbreak investigation uniquely linking the food source using a metagenomics approach and this in a fast time frame.<\/jats:p>","DOI":"10.1099\/mgen.0.000547","type":"journal-article","created":{"date-parts":[[2021,4,7]],"date-time":"2021-04-07T17:19:19Z","timestamp":1617815959000},"source":"Crossref","is-referenced-by-count":26,"title":["Application of a strain-level shotgun metagenomics approach on food samples: resolution of the source of a Salmonella food-borne outbreak"],"prefix":"10.1099","volume":"7","author":[{"given":"Florence E.","family":"Buytaers","sequence":"first","affiliation":[{"name":"Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium"},{"name":"Transversal Activities in Applied Genomics, Sciensano, Brussels, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Assia","family":"Saltykova","sequence":"additional","affiliation":[{"name":"Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium"},{"name":"Transversal Activities in Applied Genomics, Sciensano, Brussels, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7122-1578","authenticated-orcid":false,"given":"Wesley","family":"Mattheus","sequence":"additional","affiliation":[{"name":"National Reference Center for Salmonella and Shigella spp., Sciensano, Brussels, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bavo","family":"Verhaegen","sequence":"additional","affiliation":[{"name":"National Reference Laboratory for Salmonella and Food-Borne Infections, Food-Borne Pathogens, Sciensano, Brussels, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nancy H. C.","family":"Roosens","sequence":"additional","affiliation":[{"name":"Transversal Activities in Applied Genomics, Sciensano, Brussels, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kevin","family":"Vanneste","sequence":"additional","affiliation":[{"name":"Transversal Activities in Applied Genomics, Sciensano, Brussels, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Valeska","family":"Laisnez","sequence":"additional","affiliation":[{"name":"Agentschap Zorg en Gezondheid, Brussels, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2572-6540","authenticated-orcid":false,"given":"Na\u00efma","family":"Hammami","sequence":"additional","affiliation":[{"name":"Agentschap Zorg en Gezondheid, Brussels, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brigitte","family":"Pochet","sequence":"additional","affiliation":[{"name":"Federal Agency for the Security of the Food Chain, Brussels, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vera","family":"Cantaert","sequence":"additional","affiliation":[{"name":"Federal Agency for the Security of the Food Chain, Brussels, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2169-4588","authenticated-orcid":false,"given":"Kathleen","family":"Marchal","sequence":"additional","affiliation":[{"name":"Department of Genetics, University of Pretoria, Pretoria, South Africa"},{"name":"Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium"},{"name":"Department of Information Technology, IDlab, IMEC, Ghent University, Ghent, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sarah","family":"Denayer","sequence":"additional","affiliation":[{"name":"National Reference Laboratory for Salmonella and Food-Borne Infections, Food-Borne Pathogens, Sciensano, Brussels, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4198-4133","authenticated-orcid":false,"given":"Sigrid C.J.","family":"De Keersmaecker","sequence":"additional","affiliation":[{"name":"Transversal Activities in Applied Genomics, Sciensano, Brussels, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"345","reference":[{"key":"R1","article-title":"EFSA and ECDC technical report on the collection and analysis of whole genome sequencing data from food\u2010borne pathogens and other relevant microorganisms isolated from human, animal, food, feed and food\/feed environmental samples in the joint ECDC\u2010EFSA molecular typing database. EFSA Support Publ [Internet]. 2019;16(5). Available from: http:\/\/doi.wiley.com\/10.2903\/sp.efsa.2019.EN-1337"},{"key":"R2","doi-asserted-by":"publisher","DOI":"10.1099\/jmm.0.45687-0"},{"key":"R3","article-title":"Commission regulation (EC) no 2073\/2005 of 15 November 2005 on microbiological criteria for foodstuffs","volume":"2005","journal-title":"Off J Eur Union"},{"key":"R4","article-title":"The European Union one health 2018 zoonoses report","volume":"17","year":"2019","journal-title":"EFSA J"},{"key":"R5","doi-asserted-by":"publisher","DOI":"10.3390\/microorganisms8121861"},{"key":"R6","volume-title":"Lessons Learned from the 2011 Outbreak of Shiga Toxin-Producing Escherichia coli (STEC) O104:H4 in Sprouted Seeds, Commission Staff Working Document (https:\/\/ec.europa.eu\/food\/sites\/food\/files\/safety\/docs\/biosafety-crisis-cswd_lessons_learned_en.pdf)","year":"2011"},{"key":"R7","doi-asserted-by":"publisher","DOI":"10.1016\/j.trac.2017.06.001"},{"key":"R8","doi-asserted-by":"publisher","DOI":"10.1089\/fpd.2019.2636"},{"key":"R9","doi-asserted-by":"publisher","DOI":"10.20506\/rst.35.1.2419"},{"key":"R10","doi-asserted-by":"publisher","DOI":"10.1038\/nrg.2017.88"},{"key":"R11","doi-asserted-by":"publisher","DOI":"10.2903\/j.efsa.2019.5898"},{"key":"R12","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.02601-15"},{"key":"R13","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0167870"},{"key":"R14","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.01144-17"},{"key":"R15","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.00078-16"},{"key":"R16","doi-asserted-by":"publisher","DOI":"10.3390\/ijms21165688"},{"key":"R17","doi-asserted-by":"publisher","DOI":"10.3390\/microorganisms8081191"},{"key":"R18","article-title":"ISO 6579-1:2017 Microbiology of the Food Chain \u2013 Horizontal Method for the Detection, Enumeration and Serotyping of Salmonella \u2013 Part 1: Detection of Salmonella spp","year":"2017"},{"key":"R19","article-title":"Scientific opinion on the evaluation of molecular typing methods for major food-borne microbiological hazards and their use for attribution modelling, outbreak investigation and scanning surveillance: part 1 (evaluation of methods and applications)","volume":"11","year":"2013","journal-title":"EFSA J"},{"key":"R20","volume-title":"Use of Whole Genome Sequencing (WGS) of Food-borne Pathogens for Public Health Protection","year":"2014"},{"key":"R21","doi-asserted-by":"publisher","DOI":"10.1016\/j.cmi.2016.11.012"},{"key":"R22","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2019.01591"},{"key":"R23","doi-asserted-by":"publisher","DOI":"10.1016\/j.cofs.2016.04.004"},{"key":"R24","doi-asserted-by":"publisher","DOI":"10.1038\/nmeth.3444"},{"key":"R25","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.02577-16"},{"key":"R26","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.02340-17"},{"key":"R27","volume-title":"Voedselvergiftigingen in Belgie Jaaroverzicht 2019 (https:\/\/www.sciensano.be\/sites\/default\/files\/jaarverslagboekje_vti2019_nl2020.pdf)","year":"2020"},{"key":"R28","volume-title":"Centre National de R\u00e9f\u00e9rence Salmonella & Shigella Rapport Annuel 2019 (https:\/\/nrchm.wiv-isp.be\/fr\/centres_ref_labo\/salmonella_et_shigella_spp\/Rapports\/Salmonella+Shigella 2019.pdf)","year":"2020"},{"key":"R29","article-title":"Communiqu\u00e9 de presse de l\u2019Agence R\u00e9gionale \u201cZorg en Gezondheid\u201d et de l\u2019Agence F\u00e9d\u00e9rale pour la S\u00e9curit\u00e9 de la Cha\u00eene Alimentaire: r\u00e9sultats de l\u2019enqu\u00eate sur le foyer de salmonelles l\u2019\u00e9cole h\u00f4teli\u00e8re Spermalie Bruges","year":"2019"},{"key":"R30","doi-asserted-by":"publisher","DOI":"10.1016\/S1473-3099(19)30047-7"},{"key":"R31","volume-title":"Joint ECDC-EFSA Rapid Outbreak Assessment: Multi-Country Outbreak of Salmonella enteritidis Infections Linked to Eggs, fourth update","year":"2020"},{"key":"R32","doi-asserted-by":"publisher","DOI":"10.1007\/s00253-013-5234-x"},{"key":"R33","year":"2010"},{"key":"R34","doi-asserted-by":"publisher","DOI":"10.2903\/j.efsa.2014.3784"},{"key":"R35","doi-asserted-by":"publisher","DOI":"10.1186\/s13059-019-1891-0"},{"key":"R36","doi-asserted-by":"publisher","DOI":"10.1371\/annotation\/b84e1af7-c127-45c3-be22-76abd977600f"},{"key":"R37","doi-asserted-by":"publisher","DOI":"10.1186\/s13059-020-02014-2"},{"key":"R38","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btu641"},{"key":"R39","doi-asserted-by":"publisher","DOI":"10.1089\/cmb.2012.0021"},{"key":"R40","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btt086"},{"key":"R41","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0147101"},{"key":"R42","doi-asserted-by":"publisher","DOI":"10.1093\/jac\/dks261"},{"key":"R43","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2019.00362"},{"key":"R44","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msy096"},{"key":"R45","doi-asserted-by":"publisher","DOI":"10.1093\/oxfordjournals.molbev.a040023"},{"key":"R46","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkw290"},{"key":"R47","doi-asserted-by":"publisher","DOI":"10.1128\/AAC.00419-13"},{"key":"R48","doi-asserted-by":"publisher","DOI":"10.1016\/j.foodres.2018.09.014"},{"key":"R49","doi-asserted-by":"publisher","DOI":"10.1001\/jama.2013.3231"},{"key":"R50","doi-asserted-by":"publisher","DOI":"10.1186\/s13059-015-0677-2"},{"key":"R51","article-title":"ISO\/DIS 23418 Microbiology of the Food Chain \u2013 Whole Genome Sequencing for Typing and Genomic Characterization of Foodborne Bacteria \u2013 General Requirements and Guidance","year":"2021"},{"key":"R52","doi-asserted-by":"publisher","DOI":"10.1186\/s12864-020-6592-2"},{"key":"R53","year":"2015"},{"key":"R54","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msaa015"},{"key":"R55","article-title":"What\u2019s in my pot? Real-time species identification on the MinION","author":"Juul","year":"2015","journal-title":"bioRxiv"}],"container-title":["Microbial Genomics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.microbiologyresearch.org\/content\/journal\/mgen\/10.1099\/mgen.0.000547?crawler=true&mimetype=application\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,12,15]],"date-time":"2023-12-15T04:25:59Z","timestamp":1702614359000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.microbiologyresearch.org\/content\/journal\/mgen\/10.1099\/mgen.0.000547"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,4,22]]},"references-count":55,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2021,4,22]]}},"URL":"https:\/\/doi.org\/10.1099\/mgen.0.000547","relation":{},"ISSN":["2057-5858"],"issn-type":[{"value":"2057-5858","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,4,22]]}}}