{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T02:16:59Z","timestamp":1790043419845,"version":"4.0.1"},"reference-count":44,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2025,12,6]],"date-time":"2025-12-06T00:00:00Z","timestamp":1764979200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100018688","name":"Korea Disease Control and Prevention Agency","doi-asserted-by":"crossref","award":["2022-ER2103-01"],"award-info":[{"award-number":["2022-ER2103-01"]}],"id":[{"id":"10.13039\/100018688","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100018688","name":"Korea Disease Control and Prevention Agency","doi-asserted-by":"crossref","award":["2024-ER2103-00"],"award-info":[{"award-number":["2024-ER2103-00"]}],"id":[{"id":"10.13039\/100018688","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Antibiotics"],"abstract":"<jats:p>Background\/Objectives:  Clostridioides difficile is an anaerobic Gram-positive bacterium and a leading cause of healthcare-associated diarrhea. In this study, C. difficile strains isolated from human patients with diarrhea and companion dogs in South Korea were compared to reveal the potential transmission between different hosts. Methods: A total of 304 C. difficile strains were isolated, including 217 human isolates and 87 dog isolates. The strains were characterized for antimicrobial susceptibility and genotypic features, including antimicrobial resistant genes and toxin genes. In addition, comparative genomic analyses were performed to investigate their genetic relatedness. Results: Although antimicrobial susceptibility test revealed no significant difference in overall resistance, human isolates had higher resistance to moxifloxacin and cefotetan, while dog isolates showed slightly higher resistance to clindamycin and ampicillin. Resistance to vancomycin (3.7%), rifampin (8.3%), and chloramphenicol (0.9%) was observed only in human isolates. Toxin genes (tcdA and tcdB) were found in 57.1% of human isolates and 43.7% of dog isolates, while binary toxin genes (cdtA and cdtB) were detected only in isolates from humans. Multilocus sequence typing (MLST) analysis identified 34 sequence types (STs) in human isolates and 16 in dog isolates. Among them, 15 STs were detected in the isolates from both origins; notably, ST203 and ST42 were the predominant taxa that were equally derived from humans and dogs. Although tcdA and tcdB have not been previously reported in ST203, they were detected in 7 out of 34 ST203 isolates. The whole genomes of 36 representative isolates belonging to ST42 and ST203 were classified according to the STs of the source origin. Conclusions: These results indicate that similar C. difficile strain populations are present in both humans and companion dogs, which is compatible with interspecies dissemination or circulation of shared strain populations, and may also reflect host adaptation.<\/jats:p>","DOI":"10.3390\/antibiotics14121231","type":"journal-article","created":{"date-parts":[[2025,12,8]],"date-time":"2025-12-08T08:21:43Z","timestamp":1765182103000},"page":"1231","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Comparative Relatedness of Clostridioides difficile Strains Isolated from Humans and Companion Dogs in South Korea"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1373-9256","authenticated-orcid":false,"given":"Joo Yeol","family":"Kim","sequence":"first","affiliation":[{"name":"Division of Biotechnology, Jeonbuk National University, Iksan 54596, Republic of Korea"},{"name":"Advanced Institute of Environment and Bioscience, Jeonbuk National University, Iksan 54596, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Su Min","family":"Kwak","sequence":"additional","affiliation":[{"name":"Division of Biotechnology, Jeonbuk National University, Iksan 54596, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0009-9921-4386","authenticated-orcid":false,"given":"Jae Hong","family":"Jeong","sequence":"additional","affiliation":[{"name":"Division of Biotechnology, Jeonbuk National University, Iksan 54596, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jae Young","family":"Oh","sequence":"additional","affiliation":[{"name":"Division of Biotechnology, Jeonbuk National University, Iksan 54596, Republic of Korea"},{"name":"Advanced Institute of Environment and Bioscience, Jeonbuk National University, Iksan 54596, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1620-4916","authenticated-orcid":false,"given":"Kwang-Won","family":"Seo","sequence":"additional","affiliation":[{"name":"College of Veterinary Medicine, Chungbuk National University, Cheongju 28644, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dongheui","family":"An","sequence":"additional","affiliation":[{"name":"Seegene Medical Foundation, Seoul 04805, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0348-5440","authenticated-orcid":false,"given":"Dokyun","family":"Kim","sequence":"additional","affiliation":[{"name":"Department of Laboratory Medicine and Research Institute of Bacterial Resistance, Gangnam Severance Hospital, Yonsei University College of Medicine, Seoul 06273, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9290-897X","authenticated-orcid":false,"given":"Seok Hoon","family":"Jeong","sequence":"additional","affiliation":[{"name":"Department of Laboratory Medicine and Research Institute of Bacterial Resistance, Gangnam Severance Hospital, Yonsei University College of Medicine, Seoul 06273, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chang-Ki","family":"Kim","sequence":"additional","affiliation":[{"name":"Seoul Clinical Laboratories, Yongin 16954, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7831-5905","authenticated-orcid":false,"given":"Kwang Jun","family":"Lee","sequence":"additional","affiliation":[{"name":"Division of Zoonotic and Vector Borne Disease Research, National Institute of Health, Cheongju 28159, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4422-9312","authenticated-orcid":false,"given":"Jong-Chan","family":"Chae","sequence":"additional","affiliation":[{"name":"Division of Biotechnology, Jeonbuk National University, Iksan 54596, Republic of Korea"},{"name":"Advanced Institute of Environment and Bioscience, Jeonbuk National University, Iksan 54596, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,12,6]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"100560","DOI":"10.4292\/wjgpt.v16.i1.100560","article-title":"Comprehensive review of Clostridium difficile infection: Epidemiology, diagnosis, prevention, and treatment","volume":"16","author":"Wang","year":"2025","journal-title":"World J. Gastrointest. Pharmacol. Ther."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"200","DOI":"10.14218\/JTG.2024.00022","article-title":"Clostridioides difficile Infection: A Review of Emerging Practices for Infection Treatment and Prevention of Recurrence","volume":"2","author":"Darkow","year":"2024","journal-title":"J. Transl. Gastroenterol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1335","DOI":"10.1111\/apt.17975","article-title":"Review article: The epidemiology and management of Clostridioides difficile infection\u2014A clinical update","volume":"59","author":"Clarke","year":"2024","journal-title":"Aliment. Pharmacol. Ther."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Salvarani, F.M., Oliveira, H.G.d.S., and Uzal, F.A. (2025). Clostridioides difficile in Animal Inflammatory Bowel Disease: A One Health Perspective on Emerging Zoonotic Threats. Microorganisms, 13.","DOI":"10.3390\/microorganisms13061233"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1111\/zph.13032","article-title":"Infrequent intrahousehold transmission of Clostridioides difficile between pet owners and their pets","volume":"70","author":"Redding","year":"2023","journal-title":"Zoonoses Public Health"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"3077","DOI":"10.1093\/jac\/dkab231","article-title":"Mechanisms of antibiotic resistance of Clostridioides difficile","volume":"76","author":"Wickramage","year":"2021","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1016\/j.jgar.2024.07.006","article-title":"Antimicrobial susceptibilities, resistance mechanisms and molecular characteristics of toxigenic Clostridioides difficile isolates in a large teaching hospital in Chongqing, China","volume":"38","author":"Dang","year":"2024","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"e2525252","DOI":"10.1001\/jamanetworkopen.2025.25252","article-title":"Antibiotic use and the risk of hospital-onset Clostridioides difficile infection","volume":"8","author":"Gilboa","year":"2025","journal-title":"JAMA Netw. Open"},{"key":"ref_9","first-page":"280","article-title":"Clostridioides difficile infection: An update","volume":"32","author":"Salvati","year":"2024","journal-title":"Infez. Med."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Alam, M.Z., and Madan, R. (2024). Clostridioides difficile Toxins: Host Cell Interactions and Their Role in Disease Pathogenesis. Toxins, 16.","DOI":"10.3390\/toxins16060241"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.mib.2021.10.018","article-title":"Regulation of Clostridioides difficile toxin production","volume":"65","author":"Majumdar","year":"2022","journal-title":"Curr. Opin. Microbiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"ofad040","DOI":"10.1093\/ofid\/ofad040","article-title":"Clostridioides difficile binary toxin binding component increases virulence in a hamster model","volume":"10","author":"Simpson","year":"2023","journal-title":"Open Forum Infect. Dis."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Markovska, R., Dimitrov, G., Gergova, R., and Boyanova, L. (2023). Clostridioides difficile, a New \u201cSuperbug\u201d. Microorganisms, 11.","DOI":"10.3390\/microorganisms11040845"},{"key":"ref_14","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."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Alexiou, S., Diakou, A., and Kachrimanidou, M. (2025). The Role of Clostridioides difficile Within the One Health Framework: A Review. Microorganisms, 13.","DOI":"10.3390\/microorganisms13020429"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Abad-Fau, A., Sevilla, E., Mart\u00edn-Burriel, I., Moreno, B., and Bolea, R. (2023). Update on commonly used molecular typing methods for Clostridioides difficile. Microorganisms, 11.","DOI":"10.3390\/microorganisms11071752"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Sch\u00fcler, M.A., Riedel, T., Overmann, J., Daniel, R., and Poehlein, A. (2024). Comparative genome analyses of clinical and non-clinical Clostridioides difficile strains. Front. Microbiol., 15.","DOI":"10.3389\/fmicb.2024.1404491"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Li, C., Heuler, J., Zhu, D., Meng, X., Chakraborty, S., Harmanus, C., Wang, S., Peng, Z., Smits, W.K., and Wu, A. (2024). Genomic and phenotypic characterization of a Clostridioides difficile strain of the epidemic ST37 type from China. Front. Cell. Infect. Microbiol., 14.","DOI":"10.3389\/fcimb.2024.1412408"},{"key":"ref_19","first-page":"000590","article-title":"A multisite genomic epidemiology study of Clostridioides difficile infections in the USA supports differential roles of healthcare versus community spread for two common strains","volume":"7","author":"Young","year":"2021","journal-title":"Microb. Genom."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"102317","DOI":"10.1016\/j.anaerobe.2020.102317","article-title":"Dogs are carriers of Clostridioides difficile lineages associated with human community-acquired infections","volume":"67","author":"Lindberg","year":"2021","journal-title":"Anaerobe"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Hernandez, B.G., Vinithakumari, A.A., Sponseller, B., Tangudu, C., and Mooyottu, S. (2020). Prevalence, colonization, epidemiology, and public health significance of Clostridioides difficile in companion animals. Front. Vet. Sci., 7.","DOI":"10.3389\/fvets.2020.512551"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"102539","DOI":"10.1016\/j.anaerobe.2022.102539","article-title":"Genetic and phenotypic characteristics of Clostridium (Clostridioides) difficile from canine, bovine, and pediatric populations","volume":"74","author":"Redding","year":"2022","journal-title":"Anaerobe"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Alves, F., Castro, R., Pinto, M., Nunes, A., Pomba, C., Oliveira, M., Silveira, L., Gomes, J.P., and Oleastro, M. (2023). Molecular epidemiology of Clostridioides difficile in companion animals: Genetic overlap with human strains and public health concerns. Front. Public Health, 10.","DOI":"10.3389\/fpubh.2022.1070258"},{"key":"ref_24","first-page":"793","article-title":"Toxin gene profiles and antimicrobial resistance of Clostridioides difficile infection: A single tertiary care center study in Iran","volume":"13","author":"Sholeh","year":"2021","journal-title":"Iran. J. Microbiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1017\/ice.2020.383","article-title":"Inpatient fluoroquinolone use in Veterans\u2019 Affairs hospitals is a predictor of Clostridioides difficile infection due to fluoroquinolone-resistant ribotype 027 strains","volume":"42","author":"Silva","year":"2021","journal-title":"Infect. Control Hosp. Epidemiol."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Hur, B.A., Hardefeldt, L.Y., Verspoor, K.M., Baldwin, T., and Gilkerson, J.R. (2020). Describing the antimicrobial usage patterns of companion animal veterinary practices; free text analysis of more than 4.4 million consultation records. PLoS ONE, 15.","DOI":"10.1371\/journal.pone.0230049"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Wen, G.-L., Li, S.-H., Qin, Z., Yang, Y.-J., Bai, L.-X., Ge, W.-B., Liu, X.-W., and Li, J.-Y. (2022). Isolation, molecular typing, and antimicrobial resistance of Clostridium difficile in dogs and cats in Lanzhou City of Northwest China. Front. Vet. Sci., 9.","DOI":"10.3389\/fvets.2022.1032945"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Sholeh, M., Beig, M., Kouhsari, E., Rohani, M., Katouli, M., and Badmasti, F. (2025). Global insights into the genome dynamics of Clostridioides difficile associated with antimicrobial resistance, virulence, and genomic adaptations among clonal lineages. Front. Cell. Infect. Microbiol., 14.","DOI":"10.3389\/fcimb.2024.1493225"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1093\/infdis\/jiab294","article-title":"Genomic analysis of Clostridioides difficile in two regions of the United States reveals a diversity of strains and limited transmission","volume":"225","author":"Pecora","year":"2022","journal-title":"J. Infect. Dis."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Hussain, H., Nubgan, A., Rodr\u00edguez, C., Imwattana, K., Knight, D.R., Parthala, V., Mullany, P., and Goh, S. (2024). Removal of mobile genetic elements from the genome of Clostridioides difficile and the implications for the organism\u2019s biology. Front. Microbiol., 15.","DOI":"10.3389\/fmicb.2024.1416665"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Tickler, I.A., Goering, R.V., and Tenover, F.C. (2025). History and evolution of the hypervirulent Clostridioides difficile ribotype 027 lineage. Microorganisms, 13.","DOI":"10.3390\/microorganisms13102376"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Chankhamhaengdecha, S., Hadpanus, P., Aroonnual, A., Ngamwongsatit, P., Chotiprasitsakul, D., Chongtrakool, P., and Janvilisri, T. (2013). Evaluation of multiplex PCR with enhanced spore germination for detection of Clostridium difficile from stool samples of hospitalized patients. BioMed Res. Int., 2013.","DOI":"10.1155\/2013\/875437"},{"key":"ref_33","unstructured":"Clinical and Laboratory Standards Institute (CLSI) (2024). Performance Standards for Antimicrobial Susceptibility Testing, CLSI. [34th ed.]. CLSI Supplement M100."},{"key":"ref_34","unstructured":"The European Committee on Antimicrobial Susceptibility Testing (EUCAST) (2023). Breakpoint Tables for Interpretation of MICs and Zone Diameters, Version 13.0, EUCAST."},{"key":"ref_35","doi-asserted-by":"crossref","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":"ref_36","doi-asserted-by":"crossref","unstructured":"Wick, R.R., Judd, L.M., Gorrie, C.L., and Holt, K.E. (2017). Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput. Biol., 13.","DOI":"10.1371\/journal.pcbi.1005595"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"3691","DOI":"10.1093\/bioinformatics\/btv421","article-title":"Roary: Rapid large-scale prokaryote pan-genome analysis","volume":"31","author":"Page","year":"2015","journal-title":"Bioinformatics"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"2068","DOI":"10.1093\/bioinformatics\/btu153","article-title":"Prokka: Rapid prokaryotic genome annotation","volume":"30","author":"Seemann","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1009","DOI":"10.1093\/bioinformatics\/btr039","article-title":"Easyfig: A genome comparison visualizer","volume":"27","author":"Sullivan","year":"2011","journal-title":"Bioinformatics"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1093\/molbev\/msu300","article-title":"IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies","volume":"32","author":"Nguyen","year":"2015","journal-title":"Mol. Biol. Evol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1093\/bioinformatics\/btl529","article-title":"Interactive Tree of Life (iTOL): An online tool for phylogenetic tree display and annotation","volume":"23","author":"Letunic","year":"2007","journal-title":"Bioinformatics"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Hyatt, D., Chen, G.L., LoCascio, P.F., Land, M.L., Larimer, F.W., and Hauser, L.J. (2010). Prodigal: Prokaryotic gene recognition and translation initiation site identification. BMC Bioinform., 11.","DOI":"10.1186\/1471-2105-11-119"},{"key":"ref_43","first-page":"e000166","article-title":"chewBBACA: A complete suite for gene-by-gene schema creation and strain identification","volume":"4","author":"Silva","year":"2018","journal-title":"Microb. Genom."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1395","DOI":"10.1101\/gr.232397.117","article-title":"GrapeTree: Visualization of core genomic relationships among 100,000 bacterial pathogens","volume":"28","author":"Zhou","year":"2018","journal-title":"Genome Res."}],"container-title":["Antibiotics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-6382\/14\/12\/1231\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,12,10]],"date-time":"2025-12-10T05:25:03Z","timestamp":1765344303000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-6382\/14\/12\/1231"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,12,6]]},"references-count":44,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2025,12]]}},"alternative-id":["antibiotics14121231"],"URL":"https:\/\/doi.org\/10.3390\/antibiotics14121231","relation":{},"ISSN":["2079-6382"],"issn-type":[{"value":"2079-6382","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,12,6]]}}}