{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,24]],"date-time":"2026-06-24T14:03:01Z","timestamp":1782309781329,"version":"3.54.5"},"reference-count":109,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2023,5,16]],"date-time":"2023-05-16T00:00:00Z","timestamp":1684195200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Department for Agriculture, Food and the Marine (DAFM)","award":["17F206"],"award-info":[{"award-number":["17F206"]}]},{"name":"Department for Agriculture, Food and the Marine (DAFM)","award":["2018210"],"award-info":[{"award-number":["2018210"]}]},{"name":"Teagasc Walsh Scholarship Scheme","award":["17F206"],"award-info":[{"award-number":["17F206"]}]},{"name":"Teagasc Walsh Scholarship Scheme","award":["2018210"],"award-info":[{"award-number":["2018210"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>The aim of this study was to characterize C. difficile isolates from the farm, abattoir, and retail outlets in Ireland in terms of ribotype and antibiotic resistance (vancomycin, erythromycin, metronidazole, moxifloxacin, clindamycin, and rifampicin) using PCR and E-test methods, respectively. The most common ribotype in all stages of the food chain (including retail foods) was 078 and a variant (RT078\/4). Less commonly reported (014\/0, 002\/1, 049, and 205) and novel (RT530, 547, and 683) ribotypes were also detected, but at lower frequencies. Approximately 72% (26\/36 tested) of the isolates tested were resistant to at least one antibiotic, with the majority of these (65%; 17\/26) displaying a multi-drug (three to five antibiotics) resistant phenotype. It was concluded that ribotype 078, a hypervirulent strain commonly associated with C. difficile infection (CDI) in Ireland, was the most frequent ribotype along the food chain, resistance to clinically important antibiotics was common in C. difficile food chain isolates, and there was no relationship between ribotype and antibiotic resistance profile.<\/jats:p>","DOI":"10.3390\/microorganisms11051296","type":"journal-article","created":{"date-parts":[[2023,5,16]],"date-time":"2023-05-16T02:20:13Z","timestamp":1684203613000},"page":"1296","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Characterization of Food Chain Clostridioides difficile Isolates in Terms of Ribotype and Antimicrobial Resistance"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5641-9498","authenticated-orcid":false,"given":"Pilar","family":"Marcos","sequence":"first","affiliation":[{"name":"Teagasc Food Research Centre, Ashtown, Dublin 15, D15 KN3K Dublin, Ireland"},{"name":"School of Veterinary Medicine, University College Dublin, Belfield, Dublin 4, D04 V1W8 Dublin, Ireland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1354-9839","authenticated-orcid":false,"given":"Aoife","family":"Doyle","sequence":"additional","affiliation":[{"name":"Department of Clinical Microbiology, Trinity College Dublin, Central Pathology Laboratory, St James\u2019s Hospital, Dublin 8, D08 RX0X Dublin, Ireland"},{"name":"Central Veterinary Research Laboratory, Department of Agriculture, Food and the Marine, Backweston, Celbridge, W23 X3PH Kildare, Ireland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paul","family":"Whyte","sequence":"additional","affiliation":[{"name":"School of Veterinary Medicine, University College Dublin, Belfield, Dublin 4, D04 V1W8 Dublin, Ireland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thomas R.","family":"Rogers","sequence":"additional","affiliation":[{"name":"Department of Clinical Microbiology, Trinity College Dublin, Central Pathology Laboratory, St James\u2019s Hospital, Dublin 8, D08 RX0X Dublin, Ireland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"M\u00e1ire","family":"McElroy","sequence":"additional","affiliation":[{"name":"Central Veterinary Research Laboratory, Department of Agriculture, Food and the Marine, Backweston, Celbridge, W23 X3PH Kildare, Ireland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1922-8836","authenticated-orcid":false,"given":"Seamus","family":"Fanning","sequence":"additional","affiliation":[{"name":"UCD-Centre for Food Safety, School of Public Health, Physiotherapy and Sports Science, University College Dublin, Belfield, Dublin 4, D04 V1W8 Dublin, Ireland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5424-5167","authenticated-orcid":false,"given":"Jesus","family":"Frias","sequence":"additional","affiliation":[{"name":"Environmental Sustainability and Health Institute, Technological University Dublin, Grangegorman, Dublin 7, D07 H6K8 Dublin, Ireland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9037-1432","authenticated-orcid":false,"given":"Declan","family":"Bolton","sequence":"additional","affiliation":[{"name":"Teagasc Food Research Centre, Ashtown, Dublin 15, D15 KN3K Dublin, Ireland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,5,16]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1016\/j.anaerobe.2012.09.008","article-title":"Clostridium difficile in young farm animals and slaughter animals in Belgium","volume":"18","author":"Rodriguez","year":"2012","journal-title":"Anaerobe"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1086\/651706","article-title":"Society for Healthcare Epidemiology of America, Infectious Diseases Society of America, Infectious Diseases Society of America. Clinical practice guidelines for Clostridium difficile in adults, 2010 update by the society for healthcare epidemiology of America (SHEA) and the infectious diseases society of America (IDSA)","volume":"31","author":"Cohen","year":"2010","journal-title":"Infect. Control. Hosp. Epidemiol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1086\/521859","article-title":"Antimicrobial-associated risk factors for Clostridium difficile infection","volume":"46","author":"Owens","year":"2008","journal-title":"Clin. Infect. Dis."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1128\/JCM.37.2.461-463.1999","article-title":"PCR targeted to the 16S-23S rRNA gene intergenic spacer region of Clostridium difficile and construction of a library consisting of 116 different PCR ribotypes","volume":"37","author":"Stubbs","year":"1999","journal-title":"J. Clin. Microbiol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1377","DOI":"10.1099\/jmm.0.47714-0","article-title":"Characterization of Clostridium difficile isolates using capillary gel electrophoresis-based PCR ribotyping","volume":"57","author":"Indra","year":"2008","journal-title":"J. Med. Microbiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"692","DOI":"10.3389\/fmicb.2019.00692","article-title":"A Review of Mixed Strain Clostridium difficile Colonization and Infection","volume":"10","author":"Dayananda","year":"2019","journal-title":"Front. Microbiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"721","DOI":"10.1128\/CMR.00127-14","article-title":"Diversity and Evolution in the Genome of Clostridium difficile","volume":"28","author":"Knight","year":"2015","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"E204","DOI":"10.1111\/j.1469-0691.2012.03883.x","article-title":"The undiagnosed cases of Clostridium difficile infection in a whole nation, where is the problem?","volume":"18","author":"Martin","year":"2012","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"388","DOI":"10.1016\/j.jhin.2019.06.003","article-title":"Two-year analysis of Clostridium difficile ribotypes associated with increased severity","volume":"4","author":"Herbert","year":"2019","journal-title":"J. Hosp. Infect."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1007\/978-3-319-72799-8_4","article-title":"Ribotypes and New Virulent Strains Across Europe","volume":"1050","author":"Couturier","year":"2018","journal-title":"Adv. Exp. Med. Biol."},{"key":"ref_11","unstructured":"(2023, January 20). Health Service Executive (HSE)\u2014Health Protection Surveillance Centre (HPSC) Enhanced Surveillance of Clostridioides (Clostridium) difficile Infection in Ireland: Q2 2021 National Report. Available online: https:\/\/www.hpsc.ie\/a-z\/microbiologyantimicrobialresistance\/clostridioidesdifficile\/enhancedsurveillance\/quarterlyreports\/CDINationalReport_Q22022_v2.0_Final.pdf."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/j.vetmic.2016.12.001","article-title":"Subtyping and antimicrobial susceptibility of Clostridium difficile PCR ribotype 078\/126 isolates of human and animal origin","volume":"199","author":"Blanco","year":"2017","journal-title":"Vet. Microbiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"20954","DOI":"10.2807\/1560-7917.ES2014.19.45.20954","article-title":"Whole genome sequencing reveals potential spread of Clostridium difficile between humans and farm animals in the Netherlands, 2002 to 2011","volume":"19","author":"Knetsch","year":"2014","journal-title":"Euro. Surveill."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1016\/j.cmi.2019.10.023","article-title":"Clostridium difficile and One Health","volume":"26","author":"Lim","year":"2020","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1177\/1040638719899081","article-title":"Clostridium (Clostridioides) difficile in animals","volume":"32","author":"Weese","year":"2020","journal-title":"J. Vet. Diagn. Investig. Off. Publ. Am. Assoc. Vet. Lab. Diagn."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Bolton, D., and Marcos, P. (2023). The Environment, Farm Animals and Foods as Sources of Clostridioides difficile Infection in Humans. Foods, 12.","DOI":"10.3390\/foods12051094"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"462","DOI":"10.1111\/jam.13343","article-title":"Presence of Clostridium difficile in pig faecal samples and wild animal species associated with pig farms","volume":"122","author":"Bolea","year":"2017","journal-title":"J. Appl. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1321","DOI":"10.1089\/fpd.2011.0936","article-title":"Clostridium difficile in poultry and poultry meat","volume":"8","author":"Harvey","year":"2011","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1016\/j.vetmic.2011.05.014","article-title":"Epidemiology of Clostridium difficile on a veal farm, prevalence, molecular characterization and tetracycline resistance","volume":"152","author":"Costa","year":"2011","journal-title":"Vet. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"5689","DOI":"10.1128\/AEM.01888-13","article-title":"Prevalence of Gastrointestinal Clostridium difficile Carriage in Australian Sheep and Lambs","volume":"79","author":"Knight","year":"2013","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1111\/j.1863-2378.2012.01540.x","article-title":"Prevalence and genotypic characterization of Clostridium difficile from ruminants in Switzerland","volume":"59","author":"Romano","year":"2012","journal-title":"Zoonoses Public Health"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1016\/j.anaerobe.2014.06.009","article-title":"Clostridium difficile in goats and sheep in Slovenia, characterisation of strains and evidence of age-related shedding","volume":"28","author":"Pate","year":"2014","journal-title":"Anaerobe"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"819","DOI":"10.3201\/eid1505.081071","article-title":"Clostridium difficile in Retail Meat Products, USA, 2007","volume":"15","author":"Songer","year":"2009","journal-title":"Emerg. Infect. Dis."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"5009","DOI":"10.1128\/AEM.00480-09","article-title":"Detection and Enumeration of Clostridium difficile Spores in Retail Beef and Pork","volume":"15","author":"Weese","year":"2009","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"822","DOI":"10.1089\/fpd.2014.1790","article-title":"Characterization of Clostridium difficile isolates from human fecal samples and retail meat from Pennsylvania","volume":"11","author":"Varshney","year":"2014","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"362","DOI":"10.1111\/j.1472-765X.2010.02802.x","article-title":"Detection and characterization of Clostridium difficile in retail chicken","volume":"50","author":"Weese","year":"2010","journal-title":"Lett. Appl. Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1016\/j.fm.2012.03.001","article-title":"Occurrence of toxigenic Clostridium difficile in edible bivalve molluscs","volume":"31","author":"Pasquale","year":"2012","journal-title":"Food Microbiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.ijfoodmicro.2015.05.002","article-title":"Toxigenic Clostridium difficile PCR ribotypes in edible marine bivalve molluscs in Italy","volume":"208","author":"Troiano","year":"2015","journal-title":"Int. J. Food Microbiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1016\/j.ijfoodmicro.2019.03.003","article-title":"Survey, characterization and antimicrobial susceptibility of Clostridium difficile from marine bivalve shellfish of North Adriatic Sea","volume":"298","author":"Agnoletti","year":"2019","journal-title":"Int. J. Food Microbiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"600","DOI":"10.1111\/j.1472-765X.2010.02933.x","article-title":"Clostridium difficile in vegetables, Canada","volume":"51","author":"Metcalf","year":"2010","journal-title":"Lett. Appl. Microbiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1435","DOI":"10.1099\/jmm.0.056358-0","article-title":"Contamination of ready-to-eat raw vegetables with Clostridium difficile, France","volume":"62","author":"Eckert","year":"2013","journal-title":"J. Med. Microbiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1016\/j.anaerobe.2018.10.008","article-title":"Contamination of hospital food with Clostridium difficile in Central Italy","volume":"55","author":"Primavilla","year":"2019","journal-title":"Anaerobe"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"194","DOI":"10.1016\/j.fm.2018.10.017","article-title":"High Clostridium difficile contamination rates of domestic and imported potatoes compared to some other vegetables in Slovenia","volume":"78","author":"Tkalec","year":"2019","journal-title":"Food Microbiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"e02790-18","DOI":"10.1128\/mBio.02790-18","article-title":"A Role for Tetracycline Selection in Recent Evolution of Agriculture-Associated Clostridium difficile PCR Ribotype 078","volume":"10","author":"Dingle","year":"2019","journal-title":"mBio"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1016\/j.ijantimicag.2018.05.013","article-title":"Antimicrobial susceptibility of Clostridium difficile isolated from food and environmental sources in Western Australia","volume":"52","author":"Lim","year":"2018","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"478","DOI":"10.1038\/ajg.2013.4","article-title":"Guidelines for diagnosis, treatment, and prevention of Clostridium difficile infections","volume":"108","author":"Surawicz","year":"2013","journal-title":"Am. J. Gastroenterol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"598","DOI":"10.1038\/s41467-020-14382-1","article-title":"Plasmid-mediated metronidazole resistance in Clostridioides difficile","volume":"11","author":"Boekhoud","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"e1029","DOI":"10.1093\/cid\/ciab549","article-title":"Clinical Practice Guideline by the Infectious Diseases Society of America (IDSA) and Society for Healthcare Epidemiology of America (SHEA) Focused Update Guidelines on Management of Clostridioides difficile Infection in Adults","volume":"5","author":"Johnson","year":"2021","journal-title":"Clin. Infect. Dis."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1007\/978-3-319-72799-8_9","article-title":"Antibiotic Resistances of Clostridium difficile","volume":"1050","author":"Spigaglia","year":"2018","journal-title":"Adv. Exp. Med. Biol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/j.diagmicrobio.2015.05.015","article-title":"A national survey of the molecular epidemiology of Clostridium difficile in Israel, the dissemination of the ribotype 027 strain with reduced susceptibility to vancomycin and metronidazole","volume":"83","author":"Adler","year":"2015","journal-title":"Diagn. Microbiol. Infect. Dis."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"6437","DOI":"10.1128\/AAC.00845-15","article-title":"U.S.-Based National Sentinel Surveillance Study for the Epidemiology of Clostridium difficile-Associated Diarrheal Isolates and Their Susceptibility to Fidaxomicin","volume":"59","author":"Snydman","year":"2015","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"248-e9","DOI":"10.1016\/j.cmi.2014.09.017","article-title":"Pan-European Longitudinal Surveillance of Antibiotic Resistance among Prevalent Clostridium difficile Ribotypes\u2019 Study Group","volume":"21","author":"Freeman","year":"2015","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"2690","DOI":"10.1128\/AAC.00548-13","article-title":"Use of rifamycin drugs and development of infection by rifamycin-resistant strains of Clostridium difficile","volume":"57","author":"Huang","year":"2013","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.anaerobe.2014.08.005","article-title":"In vitro antibiotic susceptibility profile of Clostridium difficile excluding PCR ribotype 027 outbreak strain in Hungary","volume":"30","author":"Terhes","year":"2014","journal-title":"Anaerobe"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"5194","DOI":"10.1128\/AAC.00625-11","article-title":"Comparative susceptibilities to fidaxomicin (OPT-80) of isolates collected at baseline, recurrence, and failure from patients in two phase III trials of fidaxomicin against Clostridium difficile infection","volume":"55","author":"Goldstein","year":"2011","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_46","first-page":"23","article-title":"Recent advances in the understanding of antibiotic resistance in Clostridium difficile infection","volume":"3","author":"Spigaglia","year":"2016","journal-title":"Ther. Adv. Infect. Dis."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1038\/ng.2478","article-title":"Emergence and global spread of epidemic healthcare-associated Clostridium difficile","volume":"45","author":"He","year":"2013","journal-title":"Nat. Genet."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"103781","DOI":"10.1016\/j.fm.2021.103781","article-title":"The prevalence of Clostridioides difficile on farms, in abattoirs and in retail foods in Ireland","volume":"98","author":"Marcos","year":"2021","journal-title":"Food Microbiol."},{"key":"ref_49","unstructured":"European Centre for Disease Prevention and Control (ECDC) (2023, January 20). Laboratory Procedures for Diagnosis and Typing of Human Clostridium difficile Infection; Technical Report. Available online: www.ecdc.europa.eu."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1111\/j.1574-6968.1999.tb13629.x","article-title":"Development of a new PCR-ribotyping method for Clostridium difficile based on ribosomal RNA gene sequencing","volume":"175","author":"Bidet","year":"1999","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.ijantimicag.2012.01.004","article-title":"Treatment failure and recurrence of Clostridium difficile infection following treatment with vancomycin or metronidazole, a systematic review of the evidence","volume":"40","author":"Vardakas","year":"2012","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1086\/596315","article-title":"High frequency of rifampin resistance identified in an epidemic Clostridium difficile clone from a large teaching hospital","volume":"48","author":"Curry","year":"2009","journal-title":"Clin. Infect. Dis."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.anaerobe.2014.04.007","article-title":"Occurrence of Clostridium difficile PCR-ribotype 027 and it\u2019s closely related PCR-ribotype 176 in hospitals in Poland in 2008-2010","volume":"28","author":"Lachowicz","year":"2014","journal-title":"Anaerobe"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"200","DOI":"10.1016\/j.bj.2021.02.007","article-title":"Clinical characteristics associated with the severity of Clostridium [Clostridioides] difficile infection in a tertiary teaching hospital from Mexico","volume":"45","year":"2022","journal-title":"Biomed. J."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"526","DOI":"10.1046\/j.1469-0691.2003.00559.x","article-title":"Antecedent use of fluoroquinolones is associated with resistance to moxifloxacin in Clostridium difficile","volume":"9","author":"Ackermann","year":"2003","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1517","DOI":"10.1592\/phco.23.14.1517.31936","article-title":"Moxifloxacin-induced Clostridium difficile-associated diarrhea","volume":"23","author":"Carroll","year":"2003","journal-title":"Pharmacotherapy"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"2227","DOI":"10.1093\/jac\/dkr292","article-title":"European Study Group on Clostridium difficile (ESGCD) Multidrug resistance in European Clostridium difficile clinical isolates","volume":"66","author":"Spigaglia","year":"2011","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_58","first-page":"158601","article-title":"Clostridium difficile with Moxifloxacin\/Clindamycin Resistance in Vegetables in Ohio, USA, and Prevalence Meta-Analysis","volume":"2014","author":"Ilic","year":"2014","journal-title":"J. Pathog."},{"key":"ref_59","unstructured":"European Committee on Antimicrobial Susceptibility Testing (EUCAST) (2023, March 01). MIC Distribution for Clostridioides Difficie. Available online: https:\/\/mic.eucast.org\/search\/?search%5Bmethod%5D=mic&search%5Bantibiotic%5D=-1&search%5Bspecies%5D=564&search%5Bdisk_content%5D=-1&search%5Blimit%5D=50."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1963","DOI":"10.1128\/JCM.00224-07","article-title":"Prevalence of PCR ribotypes among Clostridium difficile isolates from pigs, calves, and other species","volume":"45","author":"Keel","year":"2007","journal-title":"J. Clin. Microbiol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/j.anaerobe.2018.03.009","article-title":"Presence of Clostridium difficile in poultry and poultry meat in Egypt","volume":"51","author":"Thomas","year":"2018","journal-title":"Anaerobe"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"770","DOI":"10.1016\/j.ijmm.2018.05.006","article-title":"The emergence of Clostridium difficile PCR ribotype 078 in piglets in the Czech Republic clusters with Clostridium difficile PCR ribotype 078 isolates from Germany, Japan and Taiwan","volume":"308","author":"Krutova","year":"2018","journal-title":"Int. J. Med. Microbiol."},{"key":"ref_63","doi-asserted-by":"crossref","unstructured":"Zhang, L.J., Yang, L., Gu, X.X., Chen, P.X., Fu, J.L., and Jiang, H.X. (2019). The first isolation of Clostridium difficile RT078\/ST11 from pigs in China. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0212965"},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Janezic, S., Zidaric, V., Pardon, B., Indra, A., Kokotovic, B., Blanco, J.L., Seyboldt, C., Diaz, C.R., Poxton, I.R., and Perreten, V. (2014). International Clostridium difficile animal strain collection and large diversity of animal associated strains. BMC Microbiol., 14.","DOI":"10.1186\/1471-2180-14-173"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1016\/j.ijid.2020.04.026","article-title":"Molecular epidemiology and antimicrobial resistance of Clostridioides difficile detected in chicken, soil and human samples from Zimbabwe","volume":"96","author":"Berger","year":"2020","journal-title":"Int. J. Infect. Dis."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1016\/j.ijfoodmicro.2010.11.007","article-title":"Prevalence of Clostridium difficile in retailed meat in the Netherlands","volume":"144","author":"Heuvelink","year":"2011","journal-title":"Int. J. Food Microbiol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"778","DOI":"10.1111\/j.1469-0691.2011.03651.x","article-title":"Clostridium difficile in Dutch animals, their presence, characteristics and similarities with human isolates","volume":"18","author":"Koene","year":"2012","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"7591","DOI":"10.1111\/1462-2920.15601","article-title":"Agricultural fertilization with poultry manure results in persistent environmental contamination with the pathogen Clostridioides difficile","volume":"23","author":"Frentrup","year":"2021","journal-title":"Environ. Microbiol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"109032","DOI":"10.1016\/j.ijfoodmicro.2020.109032","article-title":"Prevalence and phylogenetic relationship of Clostridioides difficile strains in fresh poultry meat samples processed in different cutting plants","volume":"339","author":"Heise","year":"2021","journal-title":"Int. J. Food Microbiol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"1080","DOI":"10.1099\/jmm.0.029983-0","article-title":"An investigation of the subtype diversity of clinical isolates of Irish Clostridium difficile ribotypes 027 and 078 by repetitive-extragenic palindromic PCR","volume":"60","author":"Solomon","year":"2011","journal-title":"J. Med. Microbiol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"8515","DOI":"10.1128\/AEM.02185-12","article-title":"Different antibiotic resistance and sporulation properties within multiclonal Clostridium difficile PCR ribotypes 078, 126, and 033 in a single calf farm","volume":"78","author":"Zidaric","year":"2012","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_72","doi-asserted-by":"crossref","unstructured":"Blasi, F., Lovito, C., Albini, E., Bano, L., Dalmonte, G., Drigo, I., Maresca, C., Massacci, F.R., Orsini, S., and Primavilla, S. (2021). Clostridioides difficile in Calves in Central Italy, Prevalence, Molecular Typing, Antimicrobial Susceptibility and Association with Antibiotic Administration. Animals, 11.","DOI":"10.3390\/ani11020515"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1186\/2047-2994-2-14","article-title":"Antimicrobial susceptibility profiles of human and piglet Clostridium difficile PCR-ribotype 078","volume":"2","author":"Keessen","year":"2013","journal-title":"Antimicrob. Resist. Infect. Control."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"513","DOI":"10.3389\/fmicb.2014.00513","article-title":"Genetic relatedness between Japanese and European isolates of Clostridium difficile originating from piglets and their risk associated with human health","volume":"5","author":"Usui","year":"2014","journal-title":"Front. Microbiol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"17218","DOI":"10.1038\/s41598-017-17523-7","article-title":"Surveillance of antibiotic resistance among common Clostridium difficile ribotypes in Hong Kong","volume":"7","author":"Chow","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"2994","DOI":"10.3389\/fmicb.2018.02994","article-title":"Genomic Study of a Clostridium difficile Multidrug Resistant Outbreak-Related Clone Reveals Novel Determinants of Resistance","volume":"9","author":"Isidro","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_77","doi-asserted-by":"crossref","unstructured":"Rahimi, E., Jalali, M., and Weese, J.S. (2014). Prevalence of Clostridium difficile in raw beef, cow, sheep, goat, camel and buffalo meat in Iran. BMC Public Health, 14.","DOI":"10.1186\/1471-2458-14-119"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"817","DOI":"10.3201\/eid1505.081186","article-title":"Clostridium difficile in ready-to-eat salads, Scotland","volume":"15","author":"Bakri","year":"2009","journal-title":"Emerg. Infect. Dis."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1093\/fqsafe\/fyx032","article-title":"Detection of antibiotic resistance toxigenic Clostridium difficile in processed retail lettuce","volume":"2","author":"Han","year":"2018","journal-title":"Food Qual. Saf."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1016\/S2221-1691(15)30156-8","article-title":"Clostridium difficile in ready-to-eat foods in Isfahan and Shahrekord, Iran","volume":"2","author":"Rahimi","year":"2015","journal-title":"Asian Pac. J. Trop. Biomed."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"516","DOI":"10.1016\/j.ijantimicag.2009.09.012","article-title":"Antimicrobial resistance in Clostridium difficile","volume":"34","author":"Huang","year":"2009","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/j.anaerobe.2018.07.007","article-title":"Antimicrobial resistance in large clostridial toxin-negative, binary toxin-positive Clostridium difficile ribotypes","volume":"54","author":"Androga","year":"2018","journal-title":"Anaerobe"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1016\/j.meatsci.2018.01.020","article-title":"The prevalence of Clostridium difficile in cattle and sheep carcasses and the antibiotic susceptibility of isolates","volume":"139","author":"Hampikyan","year":"2018","journal-title":"Meat Sci."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"407","DOI":"10.2478\/jvetres-2020-0052","article-title":"Characterisation and Antibiotic Susceptibility Profile of Clostridioides (Clostridium) Difficile Isolated from Chicken Carcasses","volume":"64","author":"Bingol","year":"2020","journal-title":"J. Vet. Res."},{"key":"ref_85","first-page":"759","article-title":"Prevalence of Clostridium difficile Isolated from Beef and Chicken Meat Products in Turkey","volume":"38","year":"2018","journal-title":"Korean J. Food Sci. Anim. Resour."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"1647","DOI":"10.1128\/AAC.46.6.1647-1650.2002","article-title":"Reassessment of Clostridium difficile susceptibility to metronidazole and vancomycin","volume":"46","author":"Alonso","year":"2002","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1186\/1476-0711-13-21","article-title":"Study of the frequency of Clostridium difficile tcdA, tcdB, cdtA and cdtB genes in feces of Calves in south west of Iran","volume":"13","author":"Doosti","year":"2014","journal-title":"Ann. Clin. Microbiol. Antimicrob."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"e00738-18","DOI":"10.1128\/AEM.00738-18","article-title":"Isolation of toxigenic Clostridium difficile from animal manure and composts being used as biological soil amendments","volume":"84","author":"Dharmasena","year":"2018","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1016\/j.anaerobe.2014.05.012","article-title":"Clostridium perfringens and Clostridium difficile in cooked beef sold in Cote d\u2019Ivoire and their antimicrobial susceptibility","volume":"28","author":"Kouassi","year":"2014","journal-title":"Anaerobe"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1016\/j.fm.2014.03.021","article-title":"Multilocus sequence typing analysis and antibiotic resistance of Clostridium difficile strains isolated from retail meat and humans in Belgium","volume":"42","author":"Rodriguez","year":"2014","journal-title":"Food Microbiol."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1501\/Vetfak_0000002794","article-title":"Detection of Clostridium difficile and toxin genes in samples of modified atmosphere packaged (MAP) minced and cubed beef meat","volume":"64","author":"Atasoy","year":"2017","journal-title":"Ank. \u00dcniversitesi Vet. Fak\u00fcltesi Derg."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"883","DOI":"10.1007\/s10068-018-0318-0","article-title":"Prevalence of Clostridium difficile isolated from various raw meats in Korea","volume":"27","author":"Lee","year":"2018","journal-title":"Food Sci. Biotechnol."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"158","DOI":"10.1186\/s13756-020-00815-5","article-title":"Antimicrobial resistance in Clostridioides (Clostridium) difficile derived from humans, a systematic review and meta-analysis","volume":"9","author":"Sholeh","year":"2020","journal-title":"Antimicrob. Resist. Infect. Control."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1111\/zph.12299","article-title":"Antimicrobial Susceptibility Patterns of Clostridium difficile Isolates from Family Dairy Farms","volume":"64","author":"Bandelj","year":"2017","journal-title":"Zoonoses Public Health"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1016\/j.vetmic.2017.09.010","article-title":"Clostridium difficile in beef cattle farms, farmers and their environment, Assessing the spread of the bacterium","volume":"210","author":"Hakimi","year":"2017","journal-title":"Vet. Microbiol."},{"key":"ref_96","doi-asserted-by":"crossref","unstructured":"Masarikova, M., Simkova, I., Plesko, M., Eretova, V., Krutova, M., and Cizek, A. (2020). The Colonisation of Calves in Czech Large-Scale Dairy Farms by Clonally-Related Clostridioides difficile of the Sequence Type 11 Represented by Ribotypes 033 and 126. Microorganisms, 8.","DOI":"10.3390\/microorganisms8060901"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"1034","DOI":"10.4315\/0362-028X.JFP-14-493","article-title":"Low Prevalence of Clostridium difficile in Slaughter Pigs in Korea","volume":"78","author":"Cho","year":"2015","journal-title":"J. Food Prot."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"2892","DOI":"10.1128\/JCM.02482-09","article-title":"Clostridium difficile isolates resistant to fluoroquinolones in Italy, emergence of PCR ribotype 018","volume":"48","author":"Spigaglia","year":"2010","journal-title":"J. Clin. Microbiol."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"2929","DOI":"10.1128\/AAC.00220-12","article-title":"Antimicrobial-resistant strains of Clostridium difficile from North America","volume":"56","author":"Tenover","year":"2012","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1186\/s13756-020-00765-y","article-title":"The association of a reduced susceptibility to moxifloxacin in causative Clostridium (Clostridioides) difficile strain with the clinical outcome of patients","volume":"9","author":"Krutova","year":"2020","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"704","DOI":"10.5812\/ircmj.5189","article-title":"Antimicrobial susceptibility of Clostridium difficile clinical isolates in Iran","volume":"15","author":"Goudarzi","year":"2013","journal-title":"Iran. Red Crescent Med. J."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"2716","DOI":"10.1128\/AAC.01623-06","article-title":"In vitro activities of 15 antimicrobial agents against 110 toxigenic Clostridium difficile clinical isolates collected from 1983 to 2004","volume":"51","author":"Hecht","year":"2007","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"2813","DOI":"10.1128\/AAC.00342-08","article-title":"Rifampin and rifaximin resistance in clinical isolates of Clostridium difficile","volume":"52","author":"Galang","year":"2008","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"827","DOI":"10.1345\/aph.1K675","article-title":"Rifamycin antibiotics for treatment of Clostridium difficile-associated diarrhea","volume":"42","author":"Garey","year":"2008","journal-title":"Ann. Pharmacother."},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"2161","DOI":"10.1056\/NEJMoa1108789","article-title":"National survey of drug-resistant tuberculosis in China","volume":"366","author":"Zhao","year":"2012","journal-title":"N. Engl. J. Med."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"1347","DOI":"10.3390\/genes6041347","article-title":"Disruption of the Gut Microbiome, Clostridium difficile Infection and the Threat of Antibiotic Resistance","volume":"6","author":"Johanesen","year":"2015","journal-title":"Genes"},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1111\/j.1469-0691.2011.03570.x","article-title":"Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria, An international expert proposal for interim standard definitions for acquired resistance","volume":"18","author":"Magiorakos","year":"2012","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1089\/fpd.2014.1865","article-title":"Multidrug-resistant pathogens in the food supply","volume":"12","author":"Doyle","year":"2015","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"604986","DOI":"10.3389\/fcimb.2020.604986","article-title":"High Prevalence of Multidrug-Resistant Clostridioides difficile Following Extensive Use of Antimicrobials in Hospitalized Patients in Kenya","volume":"10","author":"Mutai","year":"2021","journal-title":"Front. Cell. Infect. Microbiol."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/11\/5\/1296\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:35:46Z","timestamp":1760124946000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/11\/5\/1296"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,5,16]]},"references-count":109,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2023,5]]}},"alternative-id":["microorganisms11051296"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms11051296","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,5,16]]}}}