{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,13]],"date-time":"2026-07-13T18:28:44Z","timestamp":1783967324874,"version":"3.55.0"},"reference-count":42,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,8,4]],"date-time":"2023-08-04T00:00:00Z","timestamp":1691107200000},"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:p><jats:italic>Campylobacter jejuni<\/jats:italic> is the most frequent cause of bacterial gastroenteritis; therefore, the characteristics of its epidemiology must be continuously investigated to support possible mitigating measures. This is particularly important when evaluating representative strains from the world's leading chicken meat exporter, Brazil. We evaluated a panel of 14 virulence genes in 359 strains of <jats:italic>C. jejuni<\/jats:italic> isolated from chilled broiler carcasses in Brazil. The genes were classified into five virulence categories (B: biofilm\/motility; SS: secretion\/cytotoxicity system; CI: invasion\/colonization; GB: Guillain-Barr\u00e9; and AE: adaptation to stress). The percentage of strains with stress adaptation genes (86.07%) indicates the ability to survive in unfavorable environments; in addition, the strains showed a risk of causing infections in humans due to the frequency of the hcp gene (97.77%). Genes related to Guillain-Barre syndrome (GBS) in 77.44% of strains are an additional concern, which must be monitored. The gene panel showed the presence of 124 virulence profiles. Individual analyses by carcass, slaughter establishment, and municipalities in which they were located showed high index variabilities (I.Var.) of 0.82, 0.87, and 0.78, respectively. Georeferencing indicated the state of Paran\u00e1 as a hotspot for virulent strains. Higher levels of isolation and multi-virulence were identified in the summer, which is hot and humid in Brazil. Together, our results showed that the studied strains are a potential danger to public health and that there is an urgent need for their surveillance and the adoption of control measures, especially in the state of Paran\u00e1.<\/jats:p>","DOI":"10.3389\/fmicb.2023.1220579","type":"journal-article","created":{"date-parts":[[2023,8,4]],"date-time":"2023-08-04T12:16:57Z","timestamp":1691151417000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":2,"title":["Multi-virulence of Campylobacter jejuni carried by chicken meat in Brazil"],"prefix":"10.3389","volume":"14","author":[{"given":"Phelipe Augusto Borba Martins","family":"Peres","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Roberta Torres","family":"de Melo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paulo Marcel","family":"Armendaris","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fabiano","family":"Barreto","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tiago Follmann","family":"Perin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ana Laura","family":"Grazziotin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guilherme Paz","family":"Monteiro","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ana Beatriz Garcez","family":"Buiatte","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eliane Pereira","family":"Mendon\u00e7a","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eduarda Cristina Alves","family":"Lourenzatto","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Artur Slompo Muniz","family":"Bicalho","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marcelo de Vito","family":"Filho","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daise Aparecida","family":"Rossi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,8,4]]},"reference":[{"key":"B1","unstructured":"Relat\u00f3rio Anual 2023, 20232023"},{"key":"B2","doi-asserted-by":"publisher","first-page":"20","DOI":"10.1556\/EuJMI.2.2012.1.4","article-title":"Analysis of Campylobacter jejuni isolates of various sources for loci associated with Guillain-Barr\u00e9 syndrome","volume":"2","author":"Amon","year":"2012","journal-title":"Eur. J. Microbiol. Immunol"},{"key":"B3","doi-asserted-by":"publisher","first-page":"174","DOI":"10.1016\/j.micpath.2007.01.005","article-title":"Comparative analysis of cytolethal distending toxin (cdt) genes among Campylobacter jejuni, C. coli and C. fetus strains","volume":"42","author":"Asakura","year":"2007","journal-title":"Microb Pathog"},{"key":"B4","doi-asserted-by":"publisher","first-page":"459","DOI":"10.1016\/j.anaerobe.2011.06.010","article-title":"Chemotactic behavior of Campylobacter spp. in function of different temperatures (37 C and 42 C)","volume":"17","author":"Baserisalehi","year":"2011","journal-title":"Anaerobe"},{"key":"B5","doi-asserted-by":"publisher","first-page":"25","DOI":"10.2436\/20.1501.01.132","article-title":"Genes coding for virulence determinants of Campylobacter jejuni in human clinical and cattle isolates from Alberta, Canada, and their potential role in colonization of poultry","volume":"14","author":"Biswas","year":"2011","journal-title":"Int Microbiol"},{"key":"B6","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1016\/j.fm.2014.11.017","article-title":"Campylobacter virulence and survival factors","volume":"48","author":"Bolton","year":"2015","journal-title":"Food microbiology"},{"key":"B7","doi-asserted-by":"publisher","first-page":"551","DOI":"10.1038\/s41579-018-0037-9","article-title":"Campylobacter jejuni: collective components promoting a successful enteric lifestyle","volume":"16","author":"Burnham","year":"2019","journal-title":"Nat. Rev. Microbiol"},{"key":"B8","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1080\/09674845.2017.1291205","article-title":"Towards understanding clinical Campylobacter infection and its transmission: time for a different approach?","volume":"74","author":"Casey","year":"2017","journal-title":"Br. J. Biomed. Sci"},{"key":"B9","unstructured":"Preliminary Incidence and Trends of Infections with Pathogens Transmitted Commonly Through Food \u2014 Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 2016\u20132019 MMWR Morb Mortal2019"},{"key":"B10","doi-asserted-by":"publisher","first-page":"3583","DOI":"10.1128\/AEM.02491-07","article-title":"Comparison of Campylobacter populations in wild geese with those in starlings and free-range poultry on the same farm","volume":"74","author":"Colles","year":"2008","journal-title":"Appl. Environ. Microbiol"},{"key":"B11","doi-asserted-by":"publisher","first-page":"e00072","DOI":"10.1128\/CMR.00072-18","article-title":"Pathogenomics of emerging Campylobacter species","volume":"32","author":"Costa","year":"2019","journal-title":"Clin. Microbiol. Rev"},{"key":"B12","doi-asserted-by":"publisher","first-page":"345","DOI":"10.1099\/jmm.0.05056-0","article-title":"Prevalence of 11 pathogenic genes of Campylobacter jejuni by PCR in strains isolated from humans, poultry meat and broiler and bovine faeces","volume":"52","author":"Datta","year":"2003","journal-title":"J. Med. Microbiol"},{"key":"B13","unstructured":"Update and Review of Control Options for Campylobacter in Broilers At Primary Production, EFSA Journal2020"},{"key":"B14","doi-asserted-by":"publisher","first-page":"1475","DOI":"10.1099\/00221287-148-5-1475","article-title":"Quorum sensing in Campylobacter jejuni: detection of a luxS encoded signalling molecule","volume":"148","author":"Elvers","year":"2012","journal-title":"Microbiology."},{"key":"B15","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1016\/j.vetmic.2004.04.004","article-title":"Correlation between invasion of Caco-2 eukaryotic cells and colonization ability in the chick gut in Campylobacter jejuni","volume":"2","author":"H\u00e4nel","year":"2004","journal-title":"Vet. Microbiol"},{"key":"B16","doi-asserted-by":"publisher","first-page":"1026","DOI":"10.3201\/eid2006.130635","article-title":"Identification of possible virulence marker from Campylobacter jejuni isolates","volume":"20","author":"Harrison","year":"2014","journal-title":"Emerg. Infect. Dis"},{"key":"B17","doi-asserted-by":"publisher","first-page":"6535","DOI":"10.1128\/IAI.68.12.6535-6541.2000","article-title":"Campylobacter jejuni cytolethal distending toxin mediates release of interleukin-8 from intestinal epithelial cells","volume":"68","author":"Hickey","year":"2000","journal-title":"Infect. Immun"},{"key":"B18","unstructured":"Microbiology of Food and Animal Feeding Stuffs \u2013 Horizontal Method for Detection and Enumeration of Campylobacter spp. \u2013 Part 1: Detection Method (ISO 10272-1, 2006)2017"},{"key":"B19","doi-asserted-by":"publisher","first-page":"2","DOI":"10.1016\/j.chom.2010.06.012","article-title":"Type VI secretion: not just for pathogenesis anymore","volume":"8","author":"Jani","year":"2010","journal-title":"Cell Host. Microbe"},{"key":"B20","doi-asserted-by":"publisher","first-page":"687","DOI":"10.1128\/CMR.00006-15","article-title":"Global epidemiology of Campylobacter infection","volume":"28","author":"Kaakoush","year":"2015","journal-title":"Clin. Microbiol. Rev"},{"key":"B21","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3390\/microorganisms7100433","article-title":"Comparative analysis of aerotolerance, antibiotic resistance, and virulence gene prevalence in Campylobacter jejuni isolates from retail raw chicken and duck meat in South Korea","volume":"7","author":"Kim","year":"2019","journal-title":"Microorganisms"},{"key":"B22","doi-asserted-by":"publisher","first-page":"531","DOI":"10.3390\/microorganisms8040531","article-title":"Virulence traits of inpatient Campylobacter jejuni isolates, and a transcriptomic approach to identify potential genes maintaining intracellular survival","volume":"8","author":"Kov\u00e1cs","year":"2020","journal-title":"Microorganisms"},{"key":"B23","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1128\/aem.46.1.165-170.1983","article-title":"Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods","volume":"46","author":"Krumperman","year":"1983","journal-title":"Appl. Environ. Microbiol"},{"key":"B24","doi-asserted-by":"publisher","first-page":"S116","DOI":"10.1016\/j.ijfoodmicro.2010.06.024","article-title":"Evidence of broiler meat contamination with post-disinfection strains of Campylobacter jejuni from slaughterhouse","volume":"145","author":"Kudirkiene","year":"2011","journal-title":"Int. J. Food Microbiol"},{"key":"B25","doi-asserted-by":"publisher","first-page":"1269","DOI":"10.1128\/JCM.00017-17","article-title":"Whole-genome sequencing in epidemiology of Campylobacter jejuni infections","volume":"55","author":"Llarena","year":"2017","journal-title":"J. Clin. Microbiol"},{"key":"B26","unstructured":"Instru\u00e7\u00e3o Normativa n\u00b0 20, de 21 de outubro de 2016. Brasil, 20162016"},{"key":"B27","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1016\/j.ijmm.2005.08.003","article-title":"Detection of cdtA, cdtB, and cdtC genes in Campylobacter jejuni by multiplex PCR","volume":"296","author":"Mart\u00ednez","year":"2006","journal-title":"Int. J. Med. Microbiol"},{"key":"B28","doi-asserted-by":"publisher","first-page":"489","DOI":"10.1016\/j.fm.2019.03.009","article-title":"Evolution of Campylobacter jejuni of poultry origin in Brazil","volume":"82","author":"Melo","year":"2019","journal-title":"Food Microbiol"},{"key":"B29","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2017.01332","article-title":"Intrinsic and extrinsic aspects on Campylobacter jejuni biofilms","author":"Melo","year":"2017","journal-title":"Front. Microbiol"},{"key":"B30","doi-asserted-by":"publisher","first-page":"227","DOI":"10.1016\/j.foodcont.2013.02.032","article-title":"Campylobacter jejuni strains isolated from chicken meat harbour several virulence factors and represent a potential risk to humans","volume":"33","author":"Melo","year":"2013","journal-title":"Food Control"},{"key":"B31","doi-asserted-by":"publisher","DOI":"10.1186\/s12862-015-0447-5","article-title":"Within-host evolution decreases virulence in an opportunistic bacterial pathogen","author":"Mikonranta","year":"2015","journal-title":"BMC Evol. Biol"},{"key":"B32","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fmicb.2018.00408","article-title":"Whole genome sequencing and multiplex qPCR methods to identify Campylobacter jejuni encoding cst-II or cst-III sialyltransferase","volume":"9","author":"Neal-McKinney","year":"2018","journal-title":"Front. Microbiol"},{"key":"B33","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1007\/s12571-012-0230-z","article-title":"The risk of transfer of foodborne bacterial hazards in Turkey through the consumption of meat; risk ranking of muscle foods with the potential to transfer Campylobacter spp","volume":"5","author":"Omurtag","year":"2013","journal-title":"Food Secur."},{"key":"B34","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2017.00354","article-title":"Genome reduction for niche association in Campylobacter hepaticus, a cause of spotty liver disease in poultry","author":"Petrovska","year":"2017","journal-title":"Front. Cell Infect. Microbiol"},{"key":"B35","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fcimb.2012.00022","article-title":"LuxS and quorum-sensing in Campylobacter","volume":"2","author":"Plummer","year":"2012","journal-title":"Front. Cellular Infect. Microbiol"},{"key":"B36","doi-asserted-by":"publisher","first-page":"2242","DOI":"10.1007\/s00284-021-02478-w","article-title":"Prevalence of Campylobacter spp. in chicken carcasses in slaughterhouses from south of Brazil","volume":"78","author":"Rodrigues","year":"2021","journal-title":"Curr. Microbiol"},{"key":"B37","doi-asserted-by":"publisher","first-page":"531","DOI":"10.1016\/j.tim.2010.09.001","article-title":"What is type VI secretion doing in all those bugs?","volume":"18","author":"Schwarz","year":"2010","journal-title":"Trends Microbiol"},{"key":"B38","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s13099-020-00357-6","article-title":"Distribution of genes related to Type 6 secretion system and lipooligosaccharide that induced ganglioside mimicry among Campylobacter jejuni isolated from human diarrhea in Thailand","volume":"12","author":"Serichantalergs","year":"2020","journal-title":"Gut. Pathog"},{"key":"B39","doi-asserted-by":"publisher","first-page":"182","DOI":"10.1016\/j.molimm.2019.04.016","article-title":"Immunogenicity and protective efficacy of mucosal delivery of recombinant hcp of Campylobacter jejuni Type VI secretion system (T6SS) in chickens","volume":"111","author":"Singh","year":"2019","journal-title":"Mol. Immunol"},{"key":"B40","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s13104-019-4201-8","article-title":"Virulence of a T6SS Campylobacter jejuni chicken isolate from North Romania","volume":"12","author":"Ungureanu","year":"2019","journal-title":"BMC Res. Notes"},{"key":"B41","doi-asserted-by":"publisher","first-page":"717","DOI":"10.1016\/S0140-6736(16)00339-1","article-title":"Guillain-barre syndrome","volume":"388","author":"Willison","year":"2016","journal-title":"The Lancet"},{"key":"B42","doi-asserted-by":"publisher","first-page":"768","DOI":"10.4315\/0362-028X-69.4.768","article-title":"Adherenceto and invasion of human intestinal epithelial cells by Campylobacter jejuni and Campylobacter coli isolates from retail meat products","volume":"69","author":"Zheng","year":"2006","journal-title":"J. Food Prot"}],"container-title":["Frontiers in Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2023.1220579\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,8,4]],"date-time":"2023-08-04T12:17:03Z","timestamp":1691151423000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2023.1220579\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,8,4]]},"references-count":42,"alternative-id":["10.3389\/fmicb.2023.1220579"],"URL":"https:\/\/doi.org\/10.3389\/fmicb.2023.1220579","relation":{},"ISSN":["1664-302X"],"issn-type":[{"value":"1664-302X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,8,4]]},"article-number":"1220579"}}