{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T18:56:36Z","timestamp":1792004196441,"version":"4.4.0"},"reference-count":88,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,6,6]],"date-time":"2023-06-06T00:00:00Z","timestamp":1686009600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:sec><jats:title>Introduction<\/jats:title><jats:p>Whole genome sequencing (WGS) is increasingly used for characterizing foodborne pathogens and it has become a standard typing technique for surveillance and research purposes. WGS data can help assessing microbial risks and defining risk mitigating strategies for foodborne pathogens, including <jats:italic>Salmonella enterica<\/jats:italic>.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>To test the hypothesis that (combinations of) different genes can predict the probability of infection [P(inf)] given exposure to a certain pathogen strain, we determined P(inf) based on invasion potential of 87 <jats:italic>S. enterica<\/jats:italic> strains belonging to 15 serovars isolated from animals, foodstuffs and human patients, in an <jats:italic>in vitro<\/jats:italic> gastrointestinal tract (GIT) model system. These genomes were sequenced with WGS and screened for genes potentially involved in virulence. A random forest (RF) model was applied to assess whether P(inf) of a strain could be predicted based on the presence\/absence of those genes. Moreover, the association between P(inf) and biofilm formation in different experimental conditions was assessed.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results and Discussion<\/jats:title><jats:p>P(inf) values ranged from 6.7E-05 to 5.2E-01, showing variability both among and within serovars. P(inf) values also varied between isolation sources, but no unambiguous pattern was observed in the tested serovars. Interestingly, serovars causing the highest number of human infections did not show better ability to invade cells in the GIT model system, with strains belonging to other serovars displaying even higher infectivity. The RF model did not identify any virulence factor as significant P(inf) predictors. Significant associations of P(inf) with biofilm formation were found in all the different conditions for a limited number of serovars, indicating that the two phenotypes are governed by different mechanisms and that the ability to form biofilm does not correlate with the ability to invade epithelial cells. Other omics techniques therefore seem more promising as alternatives to identify genes associated with P(inf), and different hypotheses, such as gene expression rather than presence\/absence, could be tested to explain phenotypic virulence [P(inf)].<\/jats:p><\/jats:sec>","DOI":"10.3389\/fmicb.2023.1184387","type":"journal-article","created":{"date-parts":[[2023,6,6]],"date-time":"2023-06-06T16:46:43Z","timestamp":1686070003000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":17,"title":["Assessing phenotypic virulence of Salmonella enterica across serovars and sources"],"prefix":"10.3389","volume":"14","author":[{"given":"Sara","family":"Petrin","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lucas","family":"Wijnands","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elisa","family":"Beninc\u00e0","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lapo","family":"Mughini-Gras","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ellen H. M.","family":"Delfgou-van Asch","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laura","family":"Villa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Massimiliano","family":"Orsini","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carmen","family":"Losasso","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"John E.","family":"Olsen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lisa","family":"Barco","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,6,6]]},"reference":[{"key":"ref1","volume-title":"FastQC: a quality control tool for high throughput sequence data.","author":"Andrews","year":"2010"},{"key":"ref2","doi-asserted-by":"publisher","first-page":"977","DOI":"10.1111\/1462-2920.12351","article-title":"A unique megaplasmid contributes to stress tolerance and pathogenicity of an emergent S. Enterica serovar infantis strain","volume":"16","author":"Aviv","year":"2014","journal-title":"Environ. Microbiol."},{"key":"ref3","doi-asserted-by":"publisher","first-page":"455","DOI":"10.1089\/cmb.2012.0021","article-title":"SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing","volume":"19","author":"Bankevich","year":"2012","journal-title":"J. Comput. Biol."},{"key":"ref02","doi-asserted-by":"publisher","first-page":"508","DOI":"10.1111\/j.1758-2229.2011.00242.x","article-title":"Intestinal and chronic infections: Salmonella lifestyles in hostile environments","volume":"3","author":"B\u00e4umler","year":"2011","journal-title":"Environ. Microbiol. Rep."},{"key":"ref4","author":"Berk","year":"2008"},{"key":"ref5","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1471-2180-9-237\/FIGURES\/2","article-title":"Genomic and phenotypic variation in epidemic-spanning S. Enterica serovar enteritidis isolates","volume":"9","author":"Betancor","year":"2009","journal-title":"BMC Microbiol."},{"key":"ref6","doi-asserted-by":"publisher","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","article-title":"Trimmomatic: a flexible trimmer for Illumina sequence data","volume":"30","author":"Bolger","year":"2014","journal-title":"Bioinformatics"},{"key":"ref7","doi-asserted-by":"publisher","first-page":"503","DOI":"10.1099\/0022-1317-49-6-503","article-title":"Comparative study of the invasiveness of Salmonella serotypes typhimurium, Choleraesuis and Dublin for Caco-2 cells, HEp-2 cells and rabbit ileal epithelia","volume":"49","author":"Bolton","year":"2000","journal-title":"J. Med. Microbiol."},{"key":"ref8","doi-asserted-by":"publisher","first-page":"833","DOI":"10.1016\/J.TIFS.2021.10.030","article-title":"Food chain information in the European pork industry: where are we?","volume":"118","author":"Bonardi","year":"2021","journal-title":"Trends Food Sci. Technol."},{"key":"ref9","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1038\/nmeth.3176","article-title":"Fast and sensitive protein alignment using DIAMOND","volume":"12","author":"Buchfink","year":"2015","journal-title":"Nat. Methods"},{"key":"ref10","doi-asserted-by":"publisher","first-page":"2101174","DOI":"10.2807\/1560-7917.ES.2022.27.38.2101174\/CITE\/PLAINTEXT","article-title":"Changing epidemiology of Salmonella enteritidis human infections in the Netherlands and Belgium, 2006 to 2019: a registry-based population study","volume":"27","author":"Chanam\u00e8-Pinedo","year":"","journal-title":"Eur. Secur."},{"key":"ref11","doi-asserted-by":"publisher","first-page":"109850","DOI":"10.1016\/j.ijfoodmicro.2022.109850","article-title":"Sources and trends of human salmonellosis in Europe, 2015-2019: an analysis of outbreak data","volume":"379","author":"Chanam\u00e8-Pinedo","year":"","journal-title":"Int. J. Food Microbiol."},{"key":"ref12","doi-asserted-by":"publisher","first-page":"D325","DOI":"10.1093\/nar\/gki008","article-title":"VFDB: a reference database for bacterial virulence factors","volume":"33","author":"Chen","year":"2005","journal-title":"Nucleic Acids Res."},{"key":"ref13","doi-asserted-by":"publisher","first-page":"1368","DOI":"10.3389\/fmicb.2019.01368","article-title":"Embracing diversity: differences in virulence mechanisms, disease severity, and host adaptations contribute to the success of nontyphoidal Salmonella as a foodborne pathogen","volume":"10","author":"Cheng","year":"2019","journal-title":"Front. Microbiol."},{"key":"ref14","doi-asserted-by":"publisher","first-page":"144","DOI":"10.3201\/EID2501.181103","article-title":"New multidrug-resistant Salmonella enterica serovar Anatum clone, Taiwan, 2015\u20132017","volume":"25","author":"Chiou","year":"2019","journal-title":"Emerg. Infect. Dis."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"2124","DOI":"10.1080\/22221751.2020.1821582","article-title":"Genomic epidemiology of emerging ESBL-producing Salmonella Kentucky blaCTX-M-14b in Europe","volume":"9","author":"Coipan","year":"2020","journal-title":"Emerg. Microbes. Infect."},{"key":"ref16","doi-asserted-by":"publisher","first-page":"e12916","DOI":"10.1111\/JFS.12916","article-title":"Description of control programmes for Salmonella in pigs in Europe. Progress to date?","volume":"41","author":"Correia-Gomes","year":"2021","journal-title":"J Food Saf"},{"key":"ref09","doi-asserted-by":"publisher","first-page":"e00066","DOI":"10.1128\/mSphere.00066-17","article-title":"Cooperation of adhesin alleles in Salmonella-host tropism","volume":"2","author":"De Masi","year":"2017","journal-title":"Msphere"},{"key":"ref17","doi-asserted-by":"publisher","first-page":"8914","DOI":"10.4081\/ijfs.2021.8914","article-title":"Assessment of contamination of Salmonella spp. in imported black pepper and sesame seed and Salmonella inactivation by gamma irradiation","volume":"10","author":"D\u2019Oca","year":"2021","journal-title":"Ital J Food Saf"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"59","DOI":"10.5772\/67189","article-title":"Salmonella fimbriae: what is the clue to their hairdo?","volume-title":"Current Topics in Salmonella and Salmonellosis","author":"Dufresne","year":"2017"},{"key":"ref20","doi-asserted-by":"publisher","first-page":"21","DOI":"10.2903\/SP.EFSA.2017.EN-1353","article-title":"Multi-country outbreak of Salmonella enteritidis infections linked to polish eggs","volume":"14","year":"2017","journal-title":"EFSA Support. Publ"},{"key":"ref21","doi-asserted-by":"publisher","first-page":"e06971","DOI":"10.2903\/J.EFSA.2021.6971","article-title":"The European Union one health 2020 zoonoses report","volume":"19","year":"","journal-title":"EFSA J."},{"key":"ref22","doi-asserted-by":"publisher","first-page":"e06406","DOI":"10.2903\/j.efsa.2021.6406","article-title":"The European Union one health 2019 zoonoses report","volume":"19","year":"","journal-title":"EFSA J."},{"key":"ref19","volume-title":"Surveillance Atlas of Infectious Diseases","year":"2022"},{"key":"ref23","doi-asserted-by":"publisher","first-page":"198","DOI":"10.1097\/00005792-199105000-00004","article-title":"Human infection with Salmonella Dublin","volume":"70","author":"Fang","year":"1991","journal-title":"Medicine"},{"key":"ref24","doi-asserted-by":"publisher","first-page":"1211","DOI":"10.1038\/ng.3644","article-title":"Distinct Salmonella enteritidis lineages associated with enterocolitis in high-income settings and invasive disease in low-income settings","volume":"48","author":"Feasey","year":"2016","journal-title":"Nat. Genet."},{"key":"ref25","doi-asserted-by":"publisher","first-page":"e00591-15","DOI":"10.1128\/AEM.00591-19\/SUPPL_FILE\/AEM.00591-19-S0001.PDF","article-title":"Worldwide epidemiology of Salmonella serovars in animal-based foods: a meta-analysis","volume":"85","author":"Ferrari","year":"2019","journal-title":"Appl. Environ. Microbiol."},{"key":"ref26","doi-asserted-by":"publisher","first-page":"553","DOI":"10.1080\/01621459.1983.10478008","article-title":"A method for comparing two hierarchical clusterings","volume":"78","author":"Fowlkes","year":"1983","journal-title":"J. Am. Stat. Assoc."},{"key":"ref27","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1146\/annurev.cellbio.17.1.53","article-title":"Salmonella interactions with host cells: type III secretion at work","volume":"17","author":"Gal\u00e1n","year":"2001","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"ref28","doi-asserted-by":"publisher","first-page":"3718","DOI":"10.1093\/bioinformatics\/btv428","article-title":"Dendextend: an R package for visualizing, adjusting and comparing trees of hierarchical clustering","volume":"31","author":"Galili","year":"2015","journal-title":"Bioinformatics"},{"key":"ref29","doi-asserted-by":"publisher","first-page":"460","DOI":"10.1001\/JAMA.1949.62910070003007B","article-title":"SEROUS ARTHRITIS OF THE KNEE JOINT: report of a case caused by Salmonella Typhosa and Salmonella Montevideo in a child","volume":"141","author":"Gordon","year":"1949","journal-title":"J. Am. Med. Assoc."},{"key":"ref30","doi-asserted-by":"publisher","first-page":"1072","DOI":"10.1093\/bioinformatics\/btt086","article-title":"QUAST: quality assessment tool for genome assemblies","volume":"29","author":"Gurevich","year":"2013","journal-title":"Bioinformatics"},{"key":"ref31","doi-asserted-by":"publisher","first-page":"e0161225","DOI":"10.1371\/JOURNAL.PONE.0161225","article-title":"Genomic and evolutionary analysis of two Salmonella enterica serovar Kentucky sequence types isolated from bovine and poultry sources in North America","volume":"11","author":"Haley","year":"2016","journal-title":"PLoS One"},{"key":"ref32","doi-asserted-by":"publisher","first-page":"625","DOI":"10.1111\/j.1349-7006.1993.tb02022.x","article-title":"Changes of proliferative activity and phenotypes in spontaneous differentiation of a colon cancer cell line","volume":"84","author":"Hara","year":"1993","journal-title":"Jpn. J. Cancer Res."},{"key":"ref33","doi-asserted-by":"publisher","first-page":"1083","DOI":"10.1089\/FPD.2011.0862\/ASSET\/IMAGES\/LARGE\/FIGURE1.JPEG","article-title":"Molecular epidemiological investigation of a diffuse outbreak caused by Salmonella enterica serotype Montevideo isolates in Osaka prefecture, Japan","volume":"8","author":"Harada","year":"2011","journal-title":"Foodborne Pathog. Dis."},{"key":"ref34","doi-asserted-by":"publisher","first-page":"e000269","DOI":"10.1099\/MGEN.0.000269","article-title":"Global phylogenomics of multidrug-resistant Salmonella enterica serotype Kentucky ST198","volume":"5","author":"Hawkey","year":"2019","journal-title":"Microb Genom"},{"key":"ref35","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1136\/bmj.326.7385.357","article-title":"Short and long term mortality associated with foodborne bacterial gastrointestinal infections: registry based study commentary: matched cohorts can be useful","volume":"326","author":"Helms","year":"2003","journal-title":"BMJ"},{"key":"ref01","doi-asserted-by":"publisher","first-page":"275","DOI":"10.1046\/j.1365-2958.1999.01345.x","article-title":"The genetic basis of tetrathionate respiration in Salmonella Typhimurium","volume":"32","author":"Hensel","year":"1999","journal-title":"Mol. Microbiol."},{"key":"ref05","doi-asserted-by":"publisher","first-page":"539","DOI":"10.1099\/jmm.0.05510-0","article-title":"Frequency and polymorphism of sopE in isolates of Salmonella Enterica belonging to the ten most prevalent serotypes in England and Wales","volume":"53","author":"Hopkins","year":"2004","journal-title":"J. Med. Microbiol."},{"key":"ref36","doi-asserted-by":"publisher","first-page":"503","DOI":"10.1089\/FPD.2008.0144","article-title":"Comparison of genetic and physiological properties of Salmonella enterica isolates from chickens reveals one major difference between serovar Kentucky and other serovars","volume":"6","author":"Joerger","year":"2009","journal-title":"Response Acid."},{"key":"ref37","doi-asserted-by":"publisher","first-page":"272","DOI":"10.1308\/147870804588","article-title":"Septic arthritis of the knee by Salmonella Montevideo","volume":"86","author":"Katsoulis","year":"2004","journal-title":"Ann. R. Coll. Surg. Engl."},{"key":"ref010","doi-asserted-by":"publisher","first-page":"2597","DOI":"10.1128\/jcm.28.12.2597-2601.1990","article-title":"Outbreak of Salmonella Typhimurium infection traced to contaminated chocolate and caused by a strain lacking the 60-megadalton virulence plasmid","volume":"28","author":"Kapperud","year":"1990","journal-title":"J. Clin. Microbiol."},{"key":"ref38","first-page":"214","article-title":"Bacteremia due to Salmonella enterica Serotype Montevideo producing plasmid-mediated AmpC \u03b2-lactamase (DHA-1)","volume":"34","author":"Kim","year":"2004","journal-title":"Ann. Clin. Lab. Sci."},{"key":"ref39","doi-asserted-by":"publisher","first-page":"e05898","DOI":"10.2903\/J.EFSA.2019.5898","article-title":"Whole genome sequencing and metagenomics for outbreak investigation, source attribution and risk assessment of food-borne microorganisms","volume":"17","author":"Koutsoumanis","year":"","journal-title":"EFSA J."},{"key":"ref40","doi-asserted-by":"publisher","first-page":"e05596","DOI":"10.2903\/J.EFSA.2019.5596","article-title":"Salmonella control in poultry flocks and its public health impact","volume":"17","author":"Koutsoumanis","year":"","journal-title":"EFSA J."},{"key":"ref41","doi-asserted-by":"publisher","first-page":"3182","DOI":"10.3389\/FMICB.2018.03182\/BIBTEX","article-title":"Phenotypic prediction: linking in vitro virulence to the genomics of 59 Salmonella enteric strains","volume":"10","author":"Kuijpers","year":"2019","journal-title":"Front. Microbiol."},{"key":"ref42","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/srep46232","article-title":"Pathogenic traits of Salmonella Montevideo in experimental infections in vivo and in vitro","volume":"7","author":"Lalsiamthara","year":"2017","journal-title":"Sci. Rep."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"2200314","DOI":"10.2807\/1560-7917.ES.2022.27.15.2200314","article-title":"Investigation of an international outbreak of multidrug-resistant monophasic Salmonella typhimurium associated with chocolate products, EU\/EEA and United Kingdom, February to April 2022","volume":"27","author":"Larkin","year":"2022","journal-title":"Eur. Secur."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"395","DOI":"10.3389\/fmicb.2013.00395","article-title":"The global establishment of a highly-fluoroquinolone resistant Salmonella enterica serotype Kentucky ST198 strain","volume":"4","author":"le Hello","year":"2013","journal-title":"Front. Microbiol."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"675","DOI":"10.1093\/INFDIS\/JIR409","article-title":"International spread of an epidemic population of Salmonella enterica serotype Kentucky ST198 resistant to ciprofloxacin","volume":"204","author":"le Hello","year":"2011","journal-title":"J. Infect. Dis."},{"key":"ref46","doi-asserted-by":"publisher","first-page":"e160","DOI":"10.1017\/S0950268821001230","article-title":"The challenging task to select Salmonella target serovars in poultry: the Italian point of view","volume":"149","author":"Leati","year":"2021","journal-title":"Epidemiol. Infect."},{"key":"ref47","doi-asserted-by":"publisher","first-page":"e01122-19","DOI":"10.1128\/AAC.01122-19\/SUPPL_FILE\/AAC.01122-19-SD001.XLSX","article-title":"Emergence of multidrug-resistant Salmonella enterica serovar Goldcoast strains in Taiwan and international spread of the ST358 clone","volume":"63","author":"Liao","year":"2019","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref48","doi-asserted-by":"publisher","first-page":"104597","DOI":"10.1016\/J.AMSU.2022.104597","article-title":"Outbreak of monophasic Salmonella typhimurium sequence type 34 linked to chocolate products","volume":"82","author":"Lund","year":"2022","journal-title":"Ann. Med. Surg."},{"key":"ref49","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12864-020-6588-y","article-title":"Comparative genomic analysis reveals high intra-serovar plasticity within Salmonella Napoli isolated in 2005-2017","volume":"21","author":"Mastrorilli","year":"2020","journal-title":"BMC Genomics"},{"key":"ref50","doi-asserted-by":"publisher","first-page":"e0126883","DOI":"10.1371\/JOURNAL.PONE.0126883","article-title":"Genomic comparison of the closely-related S. Enterica serovars enteritidis, Dublin and Gallinarum","volume":"10","author":"Matthews","year":"2015","journal-title":"PLoS One"},{"key":"ref51","doi-asserted-by":"publisher","first-page":"2249","DOI":"10.1007\/s10096-014-2180-1","article-title":"Characterization of the emerging clinically-relevant multidrug-resistant S. Enterica serotype 4,[5],12:i:- (monophasic variant of S. Typhimurium) clones","volume":"33","author":"Mour\u00e3o","year":"2014","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref52","doi-asserted-by":"publisher","first-page":"941.e9","DOI":"10.1016\/j.cmi.2019.11.015","article-title":"Changing epidemiology of invasive non-typhoid Salmonella infection: a nationwide population-based registry study","volume":"26","author":"Mughini-Gras","year":"2020","journal-title":"Clin. Microbiol. Infect."},{"key":"ref53","first-page":"21","article-title":"Acute myocarditis precipitated by Salmonella Montevideo infection: a case report","volume":"93","author":"O\u2019Connor","year":"2000","journal-title":"Ir. Med. J."},{"key":"ref54","doi-asserted-by":"publisher","first-page":"e0003611","DOI":"10.1371\/journal.pntd.0003611","article-title":"Signatures of adaptation in human invasive Salmonella typhimurium ST313 populations from sub-Saharan Africa","volume":"9","author":"Okoro","year":"2015","journal-title":"PLoS Negl. Trop. Dis."},{"key":"ref55","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1016\/J.IJFOODMICRO.2011.05.013","article-title":"Pathogenic potential of Salmonella typhimurium DT104 following sequential passage through soil, packaged fresh-cut lettuce and a model gastrointestinal tract","volume":"148","author":"Oliveira","year":"2011","journal-title":"Int. J. Food Microbiol."},{"key":"ref56","doi-asserted-by":"publisher","first-page":"887","DOI":"10.1089\/FPD.2014.1773\/ASSET\/IMAGES\/LARGE\/FIGURE2.JPEG","article-title":"An outbreak of multiple serotypes of Salmonella in New Zealand linked to consumption of contaminated tahini imported from Turkey","volume":"11","author":"Paine","year":"2014","journal-title":"Foodborne Pathog. Dis."},{"key":"ref57","doi-asserted-by":"publisher","first-page":"428","DOI":"10.1089\/fpd.2017.2403","article-title":"Health outcomes from multidrug-resistant Salmonella infections in high-income countries: a systematic review and Meta-analysis","volume":"15","author":"Parisi","year":"2018","journal-title":"Foodborne Pathog. Dis."},{"key":"ref58","doi-asserted-by":"publisher","first-page":"821679","DOI":"10.3389\/FMICB.2022.821679\/FULL","article-title":"Effect of pH and salinity on the ability of Salmonella serotypes to form biofilm","volume":"13","author":"Petrin","year":"2022","journal-title":"Front. Microbiol."},{"key":"ref59","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1016\/J.PROFOO.2016.02.085","article-title":"Phenotypic behavior of 35 Salmonella enterica serovars compared to epidemiological and genomic data","volume":"7","author":"Pielaat","year":"2016","journal-title":"Procedia Food Sci"},{"key":"ref012","first-page":"323","article-title":"Enterocyte-like differentiation and polarization of the human colon carcinoma cell line Caco-2 in culture","volume":"47","author":"Pinto","year":"1983","journal-title":"Biol. Cell."},{"key":"ref08","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12864-019-5809-8","article-title":"Association of Salmonella virulence factor alleles with intestinal and invasive serovars","volume":"20","author":"Rakov","year":"2019","journal-title":"BMC genomics"},{"key":"ref03","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1146\/annurev-micro-091014-104108","article-title":"The pyromaniac inside you: Salmonella metabolism in the host gut","volume":"69","author":"Rivera-Ch\u00e1vez","year":"2015","journal-title":"Annu. Rev. Microbiol."},{"key":"ref60","unstructured":"Boston, MAPBCRStudio: Integrated Development for R. RStudio2021"},{"key":"ref61","doi-asserted-by":"publisher","first-page":"498","DOI":"10.1016\/j.tim.2009.08.008","article-title":"Life in the inflamed intestine, Salmonella style","volume":"17","author":"Santos","year":"2009","journal-title":"Trends Microbiol."},{"key":"ref62","doi-asserted-by":"publisher","first-page":"2059","DOI":"10.4315\/JFP-21-096","article-title":"A review of significant European foodborne outbreaks in the last decade","volume":"84","author":"Sarno","year":"2021","journal-title":"J. Food Prot."},{"key":"ref63","doi-asserted-by":"publisher","first-page":"889","DOI":"10.3389\/FMICB.2020.00889\/BIBTEX","article-title":"Source attribution study of sporadic Salmonella Derby cases in France","volume":"11","author":"S\u00e9vellec","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref64","doi-asserted-by":"publisher","first-page":"811","DOI":"10.1007\/S00203-011-0719-4\/FIGURES\/3","article-title":"In vitro and in vivo pathogenicity of Salmonella enteritidis clinical strains isolated from North America","volume":"193","author":"Shah","year":"2011","journal-title":"Arch. Microbiol."},{"key":"ref65","doi-asserted-by":"publisher","first-page":"793","DOI":"10.1046\/j.1365-2958.2002.02802.x","article-title":"Genetic analysis of Salmonella enteritidis biofilm formation: critical role of cellulose","volume":"43","author":"Solano","year":"2002","journal-title":"Mol. Microbiol."},{"key":"ref66","doi-asserted-by":"publisher","first-page":"46","DOI":"10.1007\/S002030000236","article-title":"Virulent strains of Salmonella enteritidis disrupt the epithelial barrier of Caco-2 and HEp-2 cells","volume":"175","author":"Solano","year":"2001","journal-title":"Arch. Microbiol."},{"key":"ref67","doi-asserted-by":"publisher","first-page":"20040","DOI":"10.2807\/ESE.16.50.20040-EN\/CITE\/PLAINTEXT","article-title":"Outbreak of Salmonella Montevideo associated with a dietary food supplement flagged in the rapid alert system for food and feed (RASFF) in Germany, 2010","volume":"16","author":"St\u00f6cker","year":"2011","journal-title":"Eur. Secur."},{"key":"ref06","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0045245","volume-title":"A naturally occurring single nucleotide polymorphism in the Salmonella SPI-2 type III effector srfH\/sseI controls early extraintestinal dissemination","author":"Thornbrough","year":"2012"},{"key":"ref68","doi-asserted-by":"publisher","first-page":"1065","DOI":"10.1017\/S0950268805004085","article-title":"Sesame seed products contaminated with Salmonella: three outbreaks associated with tahini","volume":"133","author":"Unicomb","year":"2005","journal-title":"Epidemiol. Infect."},{"key":"ref69","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1017\/S0950268899004379","article-title":"Host adapted serotypes of Salmonella enterica","volume":"125","author":"Uzzau","year":"2000","journal-title":"Epidemiol. Infect."},{"key":"ref70","doi-asserted-by":"publisher","first-page":"236","DOI":"10.2307\/2282967","article-title":"Hierarchical grouping to optimize an objective function","volume":"58","author":"Ward","year":"1963","journal-title":"J. Am. Stat. Assoc."},{"key":"ref71","doi-asserted-by":"publisher","first-page":"1139","DOI":"10.3389\/FMICB.2017.01139","article-title":"Quantification of Salmonella survival and infection in an in vitro model of the human intestinal tract as proxy for foodborne pathogens","volume":"8","author":"Wijnands","year":"2017","journal-title":"Front. Microbiol."},{"key":"ref72","doi-asserted-by":"publisher","first-page":"645","DOI":"10.1111\/j.0006-341X.2000.00645.x","article-title":"A note on robust variance estimation for cluster-correlated data","volume":"56","author":"Williams","year":"2000","journal-title":"Biometrics"},{"key":"ref73","doi-asserted-by":"publisher","first-page":"847","DOI":"10.1016\/J.FM.2009.05.007","article-title":"Assessment of the microbiological safety of edible dried seeds from retail premises in the United Kingdom with a focus on Salmonella spp","volume":"26","author":"Willis","year":"2009","journal-title":"Food Microbiol."},{"key":"ref74","doi-asserted-by":"publisher","first-page":"e02303-18","DOI":"10.1128\/mBio.02303-18","article-title":"Salmonella enterica phylogeny based on whole-genome sequencing reveals two new clades and novel patterns of horizontally acquired genetic elements","volume":"9","author":"Worley","year":"2018","journal-title":"mBio"},{"key":"ref75","doi-asserted-by":"publisher","first-page":"6812","DOI":"10.1128\/AEM.00497-10\/ASSET\/F46595C5-D370-4902-B986-FAD659877B36\/ASSETS\/GRAPHIC\/ZAM9991014220004.JPEG","article-title":"Differential phenotypic diversity among epidemic-spanning S. Enteritidis serovar enteritidis isolates from humans or animals","volume":"76","author":"Yim","year":"2010","journal-title":"Appl. Environ. Microbiol."},{"key":"ref76","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1016\/J.JIAC.2018.07.003","article-title":"Isolation of Salmonella enterica serovar Agona strains and their similarities to strains derived from a clone caused a serovar shift in broilers","volume":"25","author":"Yokoyama","year":"2019","journal-title":"J. Infect. Chemother."},{"key":"ref07","doi-asserted-by":"publisher","first-page":"8754","DOI":"10.1038\/ncomms9754","article-title":"Allelic variation contributes to bacterial host specificity","volume":"6","author":"Yue","year":"2015","journal-title":"Nat. Commun."},{"key":"ref04","doi-asserted-by":"publisher","first-page":"419","DOI":"10.3389\/fmicb.2013.00419","article-title":"Allelic variation in Salmonella: an underappreciated driver of adaptation and virulence","volume":"4","author":"Yue","year":"2014","journal-title":"Front. Microbiol."},{"key":"ref011","doi-asserted-by":"publisher","first-page":"138","DOI":"10.1101\/gr.251678.119","article-title":"The EnteroBase user\u2019s guide, with case studies on Salmonella transmissions, Yersinia pestis phylogeny, and Escherichia core genomic diversity","volume":"30","author":"Zhou","year":"2020","journal-title":"Genome Res."}],"container-title":["Frontiers in Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2023.1184387\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,6,6]],"date-time":"2023-06-06T16:46:53Z","timestamp":1686070013000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2023.1184387\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,6,6]]},"references-count":88,"alternative-id":["10.3389\/fmicb.2023.1184387"],"URL":"https:\/\/doi.org\/10.3389\/fmicb.2023.1184387","relation":{},"ISSN":["1664-302X"],"issn-type":[{"value":"1664-302X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,6,6]]},"article-number":"1184387"}}