{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,13]],"date-time":"2026-10-13T22:14:30Z","timestamp":1791929670796,"version":"4.3.4"},"reference-count":90,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,11,9]],"date-time":"2023-11-09T00:00:00Z","timestamp":1699488000000},"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":"Aim<\/jats:title>Campylobacter<\/jats:italic> is the leading bacterial pathogen that causes foodborne illnesses worldwide. Pasture farming is regarded as an important source of agricultural production for small farming communities. Consumer preference for pasture-raised animal products has increased; however, there is a paucity of information on the microbiological quality of pasture-raised poultry products. The purpose of this study was to explore genetic relatedness of thermophilic Campylobacter<\/jats:italic> isolates, to assess antibiotic resistance phenotypically and genotypically, and to screen the presence of virulence determinants of Campylobacter<\/jats:italic> isolates from pasture-raised poultry farms from southeastern United States.<\/jats:p><\/jats:sec>Methods<\/jats:title>Ninety-seven Campylobacter<\/jats:italic> isolates previously identified by Q7 BAX\u00ae<\/jats:sup> System Real-Time PCR were genotyped by multilocus sequence typing (MLST). Campylobacter<\/jats:italic> isolates were then evaluated for their phenotypic antimicrobial susceptibility against nine antimicrobial agents using Sensititre plates. Additionally, Campylobacter<\/jats:italic> isolates were tested for the presence of antimicrobial resistance-associated elements. Furthermore, Campylobacter<\/jats:italic> isolates were screened for the presence of 13 genes encoding putative virulence factors by PCR. These included genes involved in motility (flaA<\/jats:italic> and flhA<\/jats:italic>), adhesion and colonization (cadF<\/jats:italic>, docC<\/jats:italic>, racR<\/jats:italic>, and virB11<\/jats:italic>), toxin production (cdtA<\/jats:italic>, cdtB<\/jats:italic>, cdtC<\/jats:italic>, wlaN<\/jats:italic>, and ceuE<\/jats:italic>) and invasion (ciaB<\/jats:italic> and iamA<\/jats:italic>).<\/jats:p><\/jats:sec>Results<\/jats:title>Among 97 Campylobacter<\/jats:italic> isolates, Campylobacter jejuni<\/jats:italic> (n<\/jats:italic>\u2009=\u200979) and Campylobacter coli<\/jats:italic> (n<\/jats:italic>\u2009=\u200918) were identified. By MLST, C. jejuni<\/jats:italic> isolates were assigned to seven clonal complexes. Among them, ST-353, ST-607 and ST-21 were the most common STs recognized. All C. coli<\/jats:italic> (n<\/jats:italic>\u2009=\u200918) isolates were included in CC-828. Interestingly, eight STs identified were not belonging any previous identified clonal complex. Campylobacter<\/jats:italic> isolates displayed a high resistance rate against tetracycline (81.4%), while a low rate of resistance was observed against macrolides (azithromycin and erythromycin), quinolones and fluoroquinolones (nalidixic acid and ciprofloxacin), aminoglycosides (gentamicin), ketolide (telithromycin), amphenicol (florfenicol) and lincomycin (clindamycin). Thirteen isolates (13.54%) were pan-susceptible to all tested antibiotics, while nine isolates were multi-antimicrobial resistant (MAR; resist to three or more antimicrobial classes). Interestingly, there were no isolates resistant to all antimicrobial classes. Thr86Ile mutation was identified in all quinolones resistant strains. Erythromycin encoding gene (ermB<\/jats:italic>) was identified in 75% of erythromycin resistant isolates. The A2075 mutation was detected in one erythromycin resistant strain, while A2074 could not be identified. The tet<\/jats:italic>O gene was identified in 93.7% of tetracycline resistant isolates and six tetracycline susceptible isolates. In conclusion, the results of this study revealed that Campylobacter<\/jats:italic> isolates from pasture-raised poultry farms showed the ST relatedness to Campylobacter<\/jats:italic> isolates commonly associated with humans, indicating pasture-raised broiler flocks, similar to conventionally-reared broiler flocks, as a potential vector for antibiotic-resistant and pathogenic strains of thermophilic Campylobacter<\/jats:italic> to humans.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fmicb.2023.1271551","type":"journal-article","created":{"date-parts":[[2023,11,11]],"date-time":"2023-11-11T01:25:22Z","timestamp":1699665922000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":11,"title":["Genotypic characterization, antimicrobial susceptibility and virulence determinants of Campylobacter jejuni and Campylobacter coli isolated from pastured poultry farms"],"prefix":"10.3389","volume":"14","author":[{"given":"Amal","family":"Awad","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hung-Yueh","family":"Yeh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hazem","family":"Ramadan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael J.","family":"Rothrock","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,11,9]]},"reference":[{"key":"ref1","first-page":"645","article-title":"Transmission of antibiotic resistance from food animals to humans","volume-title":"Campylobacter","author":"Aarestrup","year":"2008"},{"key":"ref2","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1016\/j.mimet.2005.03.013","article-title":"MAMA-PCR assay for the detection of point mutations associated with high-level erythromycin resistance in Campylobacter jejuni and Campylobacter coli strains","volume":"63","author":"Alonso","year":"2005","journal-title":"J. Microbiol. Methods"},{"key":"ref9001","doi-asserted-by":"publisher","first-page":"4384","DOI":"10.1128\/iai.68.8.4384-4390.2000","article-title":"Involvement of a plasmid in virulence of Campylobacter jejuni 81-176","volume":"68","author":"Bacon","year":"2000","journal-title":"Infect. Immun."},{"key":"ref3","doi-asserted-by":"publisher","first-page":"1447","DOI":"10.3382\/ps\/pey486","article-title":"Prevalence and antimicrobial resistance of Campylobacter from antibiotic-free broilers during organic and conventional processing","volume":"98","author":"Bailey","year":"2019","journal-title":"Poult. Sci."},{"key":"ref9002","doi-asserted-by":"publisher","first-page":"1003","DOI":"10.1046\/j.1365-2672.2003.01926.x","article-title":"PCR detection of seven virulence and toxin genes of Campylobacter jejuni and Campylobacter coli isolates from Danish pigs and cattle and cytolethal distending toxin production of the isolates","volume":"94","author":"Bang","year":"2003","journal-title":"J. Appl. Microbiol."},{"key":"ref4","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1751-0147-43-S1-S37","article-title":"Health and welfare in organic poultry production","volume":"43","author":"Berg","year":"2001","journal-title":"Acta Vet. Scand."},{"key":"ref5","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 Microbiol."},{"key":"ref6","doi-asserted-by":"publisher","first-page":"222","DOI":"10.1016\/j.foodcont.2012.06.044","article-title":"A study of the molecular basis of quinolone and macrolide resistance in a selection of Campylobacter isolates from intensive poultry flocks","volume":"30","author":"Bolton","year":"2013","journal-title":"Food Control"},{"key":"ref7","doi-asserted-by":"publisher","first-page":"645","DOI":"10.1128\/AEM.72.1.645-652.2006","article-title":"Sources of Campylobacter spp. colonizing housed broiler flocks during rearing","volume":"72","author":"Bull","year":"2006","journal-title":"Appl. Environ. Microbiol."},{"key":"ref9003","doi-asserted-by":"publisher","first-page":"527","DOI":"10.1007\/s10482-008-9269-4","article-title":"The detection of hipO gene by real-time PCR in thermophilic Campylobacter spp. with very weak and negative reaction of hippurate hydrolysis","volume":"94","author":"Caner","year":"2008","journal-title":"Antonie Van Leeuwenhoek"},{"key":"ref8","doi-asserted-by":"publisher","first-page":"693","DOI":"10.1590\/s1517-83822013000300005","article-title":"Detection of CDT toxin genes in Campylobacter spp. strains isolated from broiler carcasses and vegetables in S\u00e3o Paulo, Brazil","volume":"44","author":"Carvalho","year":"2013","journal-title":"Braz. J. Microbiol."},{"key":"ref9004","doi-asserted-by":"publisher","first-page":"1353","DOI":"10.1128\/jcm.39.4.1353-1359.2001","article-title":"Molecular characterization of invasive and noninvasive Campylobacter jejuni and Campylobacter coli isolates","volume":"39","author":"Carvalho","year":"2001","journal-title":"J. Clin. Microbiol."},{"key":"ref9","doi-asserted-by":"publisher","first-page":"e37727","DOI":"10.17795\/iji-37727","article-title":"Prevalence of seven virulence genes of Campylobacter jejuni isolated from patients with diarrhea in Rosario, Argentina","volume":"3","author":"Casabonne","year":"2016","journal-title":"Int. J. Inf. Secur."},{"key":"ref10","volume-title":"Campylobacter","year":"2022"},{"key":"ref11","volume-title":"M45: methods for antimicrobial dilution and disk susceptibility testing of infrequently isolated or fastidious bacteria","author":"Hindler","year":"2015"},{"key":"ref12","doi-asserted-by":"publisher","first-page":"2042","DOI":"10.1111\/j.1462-2920.2008.01623.x","article-title":"Campylobacter infection of broiler chickens in a free-range environment","volume":"10","author":"Colles","year":"2008","journal-title":"Environ. Microbiol."},{"key":"ref13","doi-asserted-by":"publisher","first-page":"259","DOI":"10.1016\/j.ijfoodmicro.2009.12.021","article-title":"Comparison of Campylobacter populations isolated from a free-range broiler flock before and after slaughter","volume":"137","author":"Colles","year":"2010","journal-title":"Int. J. Food Microbiol."},{"key":"ref14","doi-asserted-by":"publisher","first-page":"12","DOI":"10.22004\/ag.econ.55972","article-title":"Consumer preferences for pasture-raised animal products: results from Michigan","volume":"39","author":"Conner","year":"2008","journal-title":"J. Food Distrib. Res."},{"key":"ref15","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":"ref16","doi-asserted-by":"publisher","first-page":"5228","DOI":"10.1128\/AEM.00581-10","article-title":"Decreasing trend of overlapping multilocus sequence types between human and chicken Campylobacter jejuni isolates over a decade in Finland","volume":"76","author":"de Haan","year":"2010","journal-title":"Appl. Environ. Microbiol."},{"key":"ref17","doi-asserted-by":"publisher","first-page":"6661","DOI":"10.1128\/AAC.01103-15","article-title":"Constitutive and inducible expression of the rRNA methylase gene erm (B) in Campylobacter","volume":"59","author":"Deng","year":"2015","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref9005","doi-asserted-by":"publisher","first-page":"949","DOI":"10.3201\/eid0809.02-0122","article-title":"Molecular characterization of Campylobacter jejune clones: a basis for epidemiologic investigation","volume":"8","author":"Dingle","year":"2002","journal-title":"Emerg. Infect. Dis."},{"key":"ref18","doi-asserted-by":"publisher","first-page":"3346","DOI":"10.1128\/JCM.39.3.3346-3349.2001","article-title":"Sequence typing confirms that Campylobacter jejuni strains associated with Guillain-Barre and Miller-fisher syndromes are of diverse genetic lineage, serotype, and flagella type","volume":"39","author":"Dingle","year":"2001","journal-title":"J. Clin. Microbiol."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"e0227833","DOI":"10.1371\/journal.pone.0227833","article-title":"Antimicrobial resistance patterns and molecular resistance markers of Campylobacter jejuni isolates from human diarrheal cases","volume":"15","author":"Elhadidy","year":"2020","journal-title":"PLoS One"},{"key":"ref20","doi-asserted-by":"publisher","first-page":"463","DOI":"10.1111\/tbed.13046","article-title":"Molecular epidemiology and antimicrobial resistance mechanisms of Campylobacter coli from diarrhoeal patients and broiler carcasses in Belgium","volume":"66","author":"Elhadidy","year":"2019","journal-title":"Transbound. Emerg. Dis."},{"key":"ref21","doi-asserted-by":"publisher","first-page":"1014","DOI":"10.3389\/fmicb.2018.01014","article-title":"Genetic basis and clonal population structure of antibiotic resistance in Campylobacter jejuni isolated from broiler carcasses in Belgium","volume":"9","author":"Elhadidy","year":"2018","journal-title":"Front. Microbiol."},{"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":"2021","journal-title":"EFSA J."},{"key":"ref23","doi-asserted-by":"publisher","first-page":"350","DOI":"10.1099\/jmm.0.000424","article-title":"Pathogenic potential and genotypic diversity of Campylobacter jejuni: a neglected food-borne pathogen in Brazil","volume":"66","author":"Fraz\u00e3o","year":"2017","journal-title":"J. Med. Microbiol."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1017\/S0043933913000068","article-title":"Control strategies for Campylobacter infection in poultry production","volume":"69","author":"Ghareeb","year":"2013","journal-title":"Worlds Poult. Sci. J."},{"key":"ref25","doi-asserted-by":"publisher","first-page":"181","DOI":"10.1089\/mdr.2013.0110","article-title":"Antimicrobial resistance of Campylobacter jejuni and Campylobacter coli from poultry in Italy","volume":"20","author":"Giacomelli","year":"2014","journal-title":"Microb. Drug Resist."},{"key":"ref26","doi-asserted-by":"publisher","first-page":"3442","DOI":"10.1128\/AAC.48.9.3442-3450.2004","article-title":"Incidence of antibiotic resistance in Campylobacter jejuni isolated in Alberta, Canada, from 1999 to 2002, with special reference to tet (O)-mediated tetracycline resistance","volume":"48","author":"Gibreel","year":"2004","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref27","doi-asserted-by":"publisher","first-page":"3896","DOI":"10.1074\/jbc.275.6.3896","article-title":"Biosynthesis of ganglioside mimics in Campylobacter jejuni OH 4384: identification of the glycosyltransferase genes, enzymatic synthesis of model compounds, and characterization of nanomole amounts by 600-MHz 1H and 13C NMR analysis","volume":"275","author":"Gilbert","year":"2000","journal-title":"J. Biol. Chem."},{"key":"ref28","doi-asserted-by":"publisher","first-page":"84","DOI":"10.1128\/MMBR.00035-10","article-title":"Change is good: variations in common biological mechanisms in the epsilonproteobacterial genera Campylobacter and Helicobacter","volume":"75","author":"Gilbreath","year":"2011","journal-title":"Microbiol. Mol. Biol. Rev."},{"key":"ref29","doi-asserted-by":"publisher","first-page":"699","DOI":"10.1128\/AAC.49.2.699-707.2005","article-title":"Incidence and mechanism of ciprofloxacin resistance in Campylobacter spp. isolated from commercial chicken flocks in the United Kingdom before, during and after fluoroquinolone treatment","volume":"49","author":"Griggs","year":"2005","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref30","doi-asserted-by":"publisher","first-page":"M496","DOI":"10.1111\/j.1750-3841.2010.01747.x","article-title":"Prevalence and characterization of Campylobacter jejuni isolated from pasture flock poultry","volume":"75","author":"Hanning","year":"2012","journal-title":"J. Food Sci."},{"key":"ref31","doi-asserted-by":"publisher","first-page":"31079","DOI":"10.3402\/iee.v6.31079","article-title":"Epidemiology of Campylobacter jejuni infections in Sweden, November 2011\u2013October 2012: is the severity of infection associated with C. jejuni sequence type?","volume":"6","author":"Harvala","year":"2016","journal-title":"Infect. Ecol. Epidemiol."},{"key":"ref32","doi-asserted-by":"publisher","first-page":"82","DOI":"10.1186\/1297-9716-42-82","article-title":"Colonization factors of Campylobacter jejuni in the chicken gut","volume":"42","author":"Hermans","year":"2011","journal-title":"Vet. Res."},{"key":"ref9006","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":"ref33","doi-asserted-by":"publisher","first-page":"407","DOI":"10.1007\/s10142-008-0087-6","article-title":"Genomic differences between Campylobacter jejuni isolates identify surface membrane and flagellar function gene products potentially important for colonizing the chicken intestine","volume":"8","author":"Hiett","year":"2008","journal-title":"Funct. Integr. Genomics"},{"key":"ref34","doi-asserted-by":"publisher","first-page":"e0112421","DOI":"10.1128\/AAC.01124-21","article-title":"Emergence of erythromycin resistance methyltransferases in Campylobacter coli strains in France","volume":"65","author":"Jehanne","year":"2021","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref35","doi-asserted-by":"publisher","first-page":"79","DOI":"10.1093\/jac\/dkq418","article-title":"Contribution of Cme G to antibiotic and oxidative stress resistance in Campylobacter jejuni","volume":"66","author":"Jeon","year":"2011","journal-title":"J. Antimicrob. Chemother."},{"key":"ref36","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":"ref37","doi-asserted-by":"publisher","first-page":"1430","DOI":"10.4315\/0362-028X-73.8.1430","article-title":"Prevalence, antibiograms, and transferable tet (O) plasmid of Campylobacter jejuni and Campylobacter coli isolated from raw chicken, pork, and human clinical cases in Korea","volume":"73","author":"Kim","year":"2010","journal-title":"J. Food Prot."},{"key":"ref9007","doi-asserted-by":"publisher","first-page":"953","DOI":"10.1046\/j.1365-2958.1997.4031771.x","article-title":"Identification and molecular cloning of a gene encoding a fibronectin-binding protein (CadF) from Campylobacter jejuni","volume":"24","author":"Konkel","year":"1997","journal-title":"Mol. Microbiol."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"424","DOI":"10.1089\/fpd.2014.1883","article-title":"Distribution of virulence-associated genes in a selection of Campylobacter isolates","volume":"12","author":"Koolman","year":"2015","journal-title":"Foodborne Pathog. Dis."},{"key":"ref39","doi-asserted-by":"publisher","first-page":"432","DOI":"10.1089\/mdr.2015.0055","article-title":"Characterization of antimicrobial susceptibility and its association with virulence genes related to adherence, invasion, and cytotoxicity in Campylobacter jejuni and Campylobacter coli isolates from animals, meat, and humans","volume":"22","author":"Lapierre","year":"2016","journal-title":"Microb. Drug Resist."},{"key":"ref40","doi-asserted-by":"publisher","first-page":"4358","DOI":"10.1128\/IAI.69.7.4358-4365.2001","article-title":"CdtA, CdtB, and CdtC form a tripartite complex that is required for cytolethal distending toxin activity","volume":"69","author":"Lara-Tejero","year":"2001","journal-title":"Infect. Immun."},{"key":"ref41","doi-asserted-by":"publisher","first-page":"2124","DOI":"10.1128\/aac.46.7.2124-2131.2002","article-title":"CmeABC functions as a multidrug efflux system in Campylobacter jejuni","volume":"46","author":"Lin","year":"2002","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref42","doi-asserted-by":"publisher","first-page":"2902","DOI":"10.4315\/0362-028x-69.12.2902","article-title":"Distribution of Campylobacter genotypes on broilers during slaughter","volume":"69","author":"Lindmark","year":"2006","journal-title":"J. Food Prot."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"501","DOI":"10.1046\/j.1365-2958.2000.02020.x","article-title":"Phase variation of a beta-1,3 galactosyltransferase involved in generation of the ganglioside GM1-like lipo-oligosaccharide of Campylobacter jejuni","volume":"37","author":"Linton","year":"2000","journal-title":"Mol. Microbiol."},{"key":"ref9008","doi-asserted-by":"publisher","first-page":"2568","DOI":"10.1128\/jcm.35.10.2568-2572.1997","article-title":"PCR detection, Identification to species level, and fingerprinting of Campylobacter jejuni and Campylobacter coli direct from diarrheic samples","volume":"35","author":"Linton","year":"1997","journal-title":"J. Clin. Microbiol."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"e00153","DOI":"10.1128\/AAC.00153-19","article-title":"Emerging erm (B)-mediated macrolide resistance associated with novel multidrug resistance genomic islands in Campylobacter","volume":"63","author":"Liu","year":"2019","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"3600","DOI":"10.1128\/AEM.72.5.3600-3607.2006","article-title":"Effect of conventional and organic production practices on the prevalence and antimicrobial resistance of Campylobacter spp. in poultry","volume":"72","author":"Luangtongkum","year":"2006","journal-title":"Appl. Environ. Microbiol."},{"key":"ref46","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1016\/j.ijfoodmicro.2014.04.023","article-title":"Tracking Campylobacter contamination along a broiler chicken production chain from the farm level to retail in China","volume":"181","author":"Ma","year":"2014","journal-title":"Int. J. Food Microbiol."},{"key":"ref9009","doi-asserted-by":"publisher","first-page":"123","DOI":"10.1016\/j.vetmic.2005.10.029","article-title":"PCR detection of virulence-associated genes in Campylobacter jejuni strains with differential ability to invade Caco-2 cells and to colonize the chick gut","volume":"113","author":"M\u00fcller","year":"2006","journal-title":"Vet. Microbiol."},{"key":"ref47","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1186\/s13099-016-0121-5","article-title":"Antimicrobial resistance of Campylobacter isolates from small scale and backyard chicken in Kenya","volume":"8","author":"Nguyen","year":"2016","journal-title":"Gut Pathog."},{"key":"ref48","doi-asserted-by":"publisher","first-page":"468","DOI":"10.1016\/j.ijantimicag.2003.12.008","article-title":"Relative contribution of target gene mutation and efflux to fluoroquinolone and erythromycin resistance, in French poultry and pig isolates of Campylobacter coli","volume":"23","author":"Payot","year":"2004","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref49","doi-asserted-by":"publisher","first-page":"420","DOI":"10.1111\/zph.12247","article-title":"Zoonotic public health hazards in backyard chickens","volume":"63","author":"Pohjola","year":"2016","journal-title":"Zoonoses Public Health"},{"key":"ref50","doi-asserted-by":"publisher","first-page":"1035","DOI":"10.1289\/ehp.10050","article-title":"The persistence of fluoroquinolone-resistant Campylobacter in poultry production","volume":"115","author":"Price","year":"2007","journal-title":"Environ. Health Perspect."},{"key":"ref51","doi-asserted-by":"publisher","first-page":"925","DOI":"10.1089\/mdr.2016.0183","article-title":"Antimicrobial resistance and virulence-associated genes of Campylobacter spp. isolated from raw milk, fish, poultry, and red meat","volume":"23","author":"Raeisi","year":"2017","journal-title":"Microb. Drug Resist."},{"key":"ref52","doi-asserted-by":"publisher","first-page":"108641","DOI":"10.1016\/j.ijfoodmicro.2020.108641","article-title":"Prevalence, genotypic diversity and detection of virulence genes in thermotolerant Campylobacter at different stages of the poultry meat supply chain","volume":"326","author":"Rossler","year":"2020","journal-title":"Int. J. Food Microbiol."},{"key":"ref53","doi-asserted-by":"publisher","first-page":"1791","DOI":"10.3382\/ps\/pey539","article-title":"The application of antibiotics in broiler production and the resulting antibiotic resistance in Escherichia coli: a global overview","volume":"98","author":"Roth","year":"2019","journal-title":"Poult. Sci."},{"key":"ref54","doi-asserted-by":"publisher","first-page":"593","DOI":"10.2134\/jeq2015.07.0366","article-title":"Antibiotic resistance patterns of major zoonotic pathogens from all-natural, antibiotic-free, pasture-raised broiler flocks in the southeastern United States","volume":"45","author":"Rothrock","year":"2016","journal-title":"J. Environ. Qual."},{"key":"ref55","doi-asserted-by":"publisher","first-page":"615","DOI":"10.1099\/jmm.0.45988-0","article-title":"Prevalence of potential virulence markers in polish Campylobacter jejuni and Campylobacter coli isolates obtained from hospitalized children and from chicken carcasses","volume":"54","author":"Rozynek","year":"2005","journal-title":"J. Med. Microbiol."},{"key":"ref56","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1128\/AAC.44.2.267-271.2000","article-title":"Antimicrobial resistance in Campylobacter strains isolated from animals, foods, and humans in Spain in 1997-1998","volume":"44","author":"Saenz","year":"2000","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref57","doi-asserted-by":"publisher","first-page":"168","DOI":"10.3389\/fcimb.2016.00168","article-title":"The cytolethal distending toxin contributes to microbial virulence and disease pathogenesis by acting as a tri-perditious toxin","volume":"6","author":"Scuron","year":"2016","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref58","doi-asserted-by":"publisher","first-page":"1677","DOI":"10.22092\/ari.2021.356400.1837","article-title":"Antibiotic resistance profile and multiple antibiotic resistance index of Campylobacter species isolated from poultry","volume":"76","author":"Shakir","year":"2021","journal-title":"Arch. Razi Inst."},{"key":"ref59","doi-asserted-by":"publisher","first-page":"103751","DOI":"10.1016\/j.fm.2021.103751","article-title":"Epidemiological trends of foodborne Campylobacter outbreaks in the United States of America, 1998\u20132016","volume":"97","author":"Sher","year":"2021","journal-title":"Food Microbiol."},{"key":"ref60","first-page":"69","article-title":"Clinical aspects of Campylobacter infection","volume-title":"Campylobacter","author":"Skirrow","year":"2000"},{"key":"ref61","doi-asserted-by":"publisher","first-page":"e55029","DOI":"10.1371\/journal.pone.0055029","article-title":"Practicalities of using non-local or non-recent multilocus sequence typing data for source attribution in space and time of human campylobacteriosis","volume":"8","author":"Smid","year":"2013","journal-title":"PLoS One"},{"key":"ref62","doi-asserted-by":"publisher","first-page":"103872","DOI":"10.1016\/j.foodqual.2020.103872","article-title":"Consumer perceptions, preferences, and behavior regarding pasture-raised livestock products: a review","volume":"82","author":"Stampa","year":"2020","journal-title":"Food Qual. 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Microbiol."},{"key":"ref65","doi-asserted-by":"publisher","first-page":"1125","DOI":"10.1128\/AAC.47.3.1125-1128.2003","article-title":"PCR restriction fragment length polymorphism analysis for detection of point mutations associated with macrolide resistance in Campylobacter spp","volume":"47","author":"Vacher","year":"2003","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref66","doi-asserted-by":"publisher","first-page":"5649","DOI":"10.1073\/pnas.1503141112","article-title":"Global trends in antimicrobial use in food animals","volume":"112","author":"Van Boeckel","year":"2015","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"ref67","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1089\/fpd.2008.0118","article-title":"Associations among antimicrobial use and antimicrobial resistance of Salmonella spp. isolates from 60 Alberta finishing swine farms","volume":"6","author":"Varga","year":"2009","journal-title":"Foodborne Pathog. Dis."},{"key":"ref68","doi-asserted-by":"publisher","first-page":"61","DOI":"10.14252\/foodsafetyfscj.D-19-00001","article-title":"Current status of Campylobacter food poisoning in Japan","volume":"7","author":"Vetchapitak","year":"2019","journal-title":"Food Saf. (Tokyo)"},{"key":"ref69","doi-asserted-by":"publisher","first-page":"130","DOI":"10.1016\/j.fm.2012.12.003","article-title":"Molecular characterization and antibiotic resistance profiling of Campylobacter isolated from cattle in polish slaughterhouses","volume":"34","author":"Wieczorek","year":"2013","journal-title":"Food Microbiol."},{"key":"ref70","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1016\/j.ijfoodmicro.2015.06.006","article-title":"Comparative analysis of antimicrobial resistance and genetic diversity of Campylobacter from broilers slaughtered in Poland","volume":"210","author":"Wieczorek","year":"2015","journal-title":"Int. J. 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Food Prot."},{"key":"ref74","doi-asserted-by":"publisher","first-page":"192","DOI":"10.1016\/j.micres.2012.11.010","article-title":"Construction, expression, purification and antigenicity of recombinant Campylobacter jejuni flagellar proteins","volume":"168","author":"Yeh","year":"2013","journal-title":"Microbiol. Res."},{"key":"ref75","doi-asserted-by":"publisher","first-page":"270","DOI":"10.1108\/00346650110409092","article-title":"Consumer perception of food risk in chicken meat","volume":"31","author":"Yeung","year":"2001","journal-title":"Nutr. Food Sci."},{"key":"ref76","doi-asserted-by":"publisher","first-page":"48","DOI":"10.1186\/s13099-016-0132-2","article-title":"Molecular epidemiology, virulence determinants and antimicrobial resistance of Campylobacter spreading in retail chicken meat in central China","volume":"8","author":"Zhang","year":"2016","journal-title":"Gut Pathog."},{"key":"ref77","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1016\/j.ijid.2015.11.005","article-title":"A seventeen-year observation of the antimicrobial susceptibility of clinical Campylobacter jejuni and the molecular mechanisms of erythromycin-resistant isolates in Beijing, China","volume":"42","author":"Zhou","year":"2016","journal-title":"Int. J. Infect. Dis."},{"key":"ref78","doi-asserted-by":"publisher","first-page":"549","DOI":"10.2307\/1592894","article-title":"Role of Campylobacter jejuni potential virulence genes in cecal colonization","volume":"45","author":"Ziprin","year":"2001","journal-title":"Avian Dis."},{"key":"ref79","doi-asserted-by":"publisher","first-page":"586","DOI":"10.2307\/1592660","article-title":"The absence of coecal colonization of chicks by a mutant of Campylobacter jejuni not expressing bacterial fibronectin-binding protein","volume":"43","author":"Ziprin","year":"1999","journal-title":"Avian Dis."},{"key":"ref80","doi-asserted-by":"publisher","first-page":"3276","DOI":"10.1128\/JCM.37.10.3276-3280.1999","article-title":"Ciprofloxacin resistance in Campylobacter jejuni isolates: detection of gyrA resistance mutations by mismatch amplification mutation assay PCR and DNA sequence analysis","volume":"37","author":"Zirnstein","year":"1999","journal-title":"J. Clin. 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