{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T03:17:14Z","timestamp":1792725434184,"version":"4.5.0"},"reference-count":51,"publisher":"Oxford University Press (OUP)","issue":"6","license":[{"start":{"date-parts":[[2023,6,10]],"date-time":"2023-06-10T00:00:00Z","timestamp":1686355200000},"content-version":"vor","delay-in-days":9,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001801","name":"University of Western Australia","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100001801","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000925","name":"National Health and Medical Research Council","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000925","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2023,6,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:sec>\n                  <jats:title>Aims<\/jats:title>\n                  <jats:p>To investigate the prevalence, molecular type, and antimicrobial susceptibility of Clostridioides difficile in the environment in Vietnam, where little is known about C. difficile.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Methods and results<\/jats:title>\n                  <jats:p>Samples of pig faeces, soils from pig farms, potatoes, and the hospital environment were cultured for C. difficile. Isolates were identified and typed by polymerase chain reaction (PCR) ribotyping. The overall prevalence of C. difficile contamination was 24.5% (68\/278). Clostridioides difficile was detected mainly in soils from pig farms and hospital soils, with 70%\u2013100% prevalence. Clostridioides difficile was isolated from 3.4% of pig faecal samples and 5% of potato surfaces. The four most prevalent ribotypes (RTs) were RTs 001, 009, 038, and QX574. All isolates were susceptible to metronidazole, fidaxomicin, vancomycin, and amoxicillin\/clavulanate, while resistance to erythromycin, tetracycline, and moxifloxacin was common in toxigenic strains. Clostridioides difficile RTs 001A+B+CDT\u2013 and 038A\u2013B\u2013CDT\u2013 were predominantly multidrug resistant.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Conclusions<\/jats:title>\n                  <jats:p>Environmental sources of C. difficile are important to consider in the epidemiology of C. difficile infection in Vietnam, however, contaminated soils are likely to be the most important source of C. difficile. This poses additional challenges to controlling infections in healthcare settings.<\/jats:p>\n               <\/jats:sec>","DOI":"10.1093\/jambio\/lxad118","type":"journal-article","created":{"date-parts":[[2023,6,10]],"date-time":"2023-06-10T03:02:45Z","timestamp":1686366165000},"source":"Crossref","is-referenced-by-count":15,"title":["Environmental contamination with <i>Clostridioides<\/i> (<i>Clostridium<\/i>) <i>difficile<\/i> in Vietnam"],"prefix":"10.1093","volume":"134","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1128-6425","authenticated-orcid":false,"given":"Peng An","family":"Khun","sequence":"first","affiliation":[{"name":"School of Biomedical Sciences, The University of Western Australia , Nedlands 6009, Western Australia , Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Long Duc","family":"Phi","sequence":"additional","affiliation":[{"name":"Thai Binh University of Medicine and Pharmacy , Thai Binh 410000 , Vietnam"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huong Thi Thu","family":"Bui","sequence":"additional","affiliation":[{"name":"Thai Binh General Hospital , Thai Binh 410000 , Vietnam"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nguyen Thi","family":"Bui","sequence":"additional","affiliation":[{"name":"Ninh Binh Women and Children\u2019s Hospital , Ninh Binh 430000 , Vietnam"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Quyen Thi Huyen","family":"Vu","sequence":"additional","affiliation":[{"name":"Ninh Binh Women and Children\u2019s Hospital , Ninh Binh 430000 , Vietnam"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Luong Duy","family":"Trinh","sequence":"additional","affiliation":[{"name":"Ninh Binh Women and Children\u2019s Hospital , Ninh Binh 430000 , Vietnam"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6754-9290","authenticated-orcid":false,"given":"Deirdre A","family":"Collins","sequence":"additional","affiliation":[{"name":"School of Medical and Health Sciences, Edith Cowan University , Joondalup 6027, Western Australia , Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1351-3740","authenticated-orcid":false,"given":"Thomas V","family":"Riley","sequence":"additional","affiliation":[{"name":"School of Biomedical Sciences, The University of Western Australia , Nedlands 6009, Western Australia , Australia"},{"name":"School of Medical and Health Sciences, Edith Cowan University , Joondalup 6027, Western Australia , Australia"},{"name":"Medical, Molecular and Forensic Sciences, Murdoch University , Murdoch 6150, Western Australia , Australia"},{"name":"Department of Microbiology, PathWest Laboratory Medicine , Nedlands 6009, Western Australia , Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2023,6,9]]},"reference":[{"key":"2023062712551035100_bib1","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":"2023062712551035100_bib2","doi-asserted-by":"crossref","first-page":"476","DOI":"10.1007\/BF01962596","article-title":"Laboratory diagnosis of Clostridium difficile-associated diarrhoea","volume":"7","author":"Bowman","year":"1988","journal-title":"Eur J Clin Microbiol Infect Dis"},{"key":"2023062712551035100_bib3","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1016\/j.fm.2018.08.012","article-title":"A review of Clostridioides [Clostridium] difficile occurrence through the food chain","volume":"77","author":"Candel-Perez","year":"2019","journal-title":"Food Microbiol"},{"key":"2023062712551035100_bib4","doi-asserted-by":"crossref","DOI":"10.15620\/cdc:82532","volume-title":"Antibiotic resistance threats in the United States","author":"Centers for Disease Control and Prevention (CDC)","year":"2019"},{"key":"2023062712551035100_bib5","doi-asserted-by":"crossref","first-page":"1359","DOI":"10.1001\/jamainternmed.2013.7056","article-title":"Epidemiology of community-associated Clostridium difficile infection, 2009 through 2011","volume":"173","author":"Chitnis","year":"2013","journal-title":"JAMA Intern Med"},{"key":"2023062712551035100_bib6","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/j.nmni.2017.04.006","article-title":"Prevalence and molecular epidemiology of Clostridium difficile infection in Indonesia","volume":"18","author":"Collins","year":"2017","journal-title":"New Microbes New Infect"},{"key":"2023062712551035100_bib7","first-page":"149","volume-title":"Determination of infection rates and some molecular epidemiological characteristics of toxin gene carried Clostridium difficile strains isolated from patients with diarrhea after antibiotic treatment in four hospitals in Hanoi (2013\u20132015)","author":"Duong","year":"2017"},{"key":"2023062712551035100_bib8","doi-asserted-by":"crossref","first-page":"1094","DOI":"10.1128\/JCM.03321-15","article-title":"Evaluation of luminex xTAG gastrointestinal pathogen panel assay for detection of multiple diarrheal pathogens in fecal samples in Vietnam","volume":"54","author":"Duong","year":"2016","journal-title":"J Clin Microbiol"},{"key":"2023062712551035100_bib9","author":"EUCAST","year":"2021"},{"key":"2023062712551035100_bib10","doi-asserted-by":"crossref","first-page":"248.e249","DOI":"10.1016\/j.cmi.2014.09.017","article-title":"Pan-European longitudinal surveillance of antibiotic resistance among prevalent Clostridium difficile ribotypes","volume":"21","author":"Freeman","year":"2015","journal-title":"Clin Microbiol Infect"},{"key":"2023062712551035100_bib11","first-page":"196","volume-title":"Characteristics of epidemiology, clinical manifestation, and risk factors of Clostridium difficile infection among adult patients with diarrhoea in bach mai hospital from 2013 to 2017","author":"Giang","year":"2020"},{"key":"2023062712551035100_bib12","doi-asserted-by":"crossref","first-page":"1320","DOI":"10.1056\/NEJMoa1910215","article-title":"Trends in U.S. burden of Clostridioides difficile infection and outcomes","volume":"382","author":"Guh","year":"2020","journal-title":"N Engl J Med"},{"key":"2023062712551035100_bib13","doi-asserted-by":"crossref","first-page":"624","DOI":"10.4315\/0362-028X.JFP-12-330","article-title":"Longitudinal study of Clostridium difficile and methicillin-resistant Staphylococcus aureus associated with pigs from weaning through to the end of processing","volume":"76","author":"Hawken","year":"2013","journal-title":"J Food Prot"},{"key":"2023062712551035100_bib14","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1128\/jcm.00893-22","article-title":"A white colony-producing Clostridioides difficile ribotype 020 strain","volume":"61","author":"Imwattana","year":"2023","journal-title":"J Clin Microbiol"},{"key":"2023062712551035100_bib15","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1016\/j.anaerobe.2019.03.008","article-title":"High prevalence and diversity of tcdA-negative and tcdB-positive, and non-toxigenic, Clostridium difficile in Thailand","volume":"57","author":"Imwattana","year":"2019","journal-title":"Anaerobe"},{"key":"2023062712551035100_bib16","doi-asserted-by":"crossref","first-page":"102550","DOI":"10.1016\/j.anaerobe.2022.102550","article-title":"Clostridioides (Clostridium) difficile in children with diarrhoea in Vietnam","volume":"74","author":"Khun","year":"2022","journal-title":"Anaerobe"},{"key":"2023062712551035100_bib17","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":"2023062712551035100_bib18","doi-asserted-by":"crossref","first-page":"2213","DOI":"10.1093\/jac\/dkw124","article-title":"Clostridium difficile clade 5 in Australia: antimicrobial susceptibility profiling of PCR ribotypes of human and animal origin","volume":"71","author":"Knight","year":"2016","journal-title":"J Antimicrob Chemother"},{"key":"2023062712551035100_bib19","doi-asserted-by":"crossref","first-page":"164","DOI":"10.3389\/fpubh.2019.00164","article-title":"Genomic delineation of zoonotic origins of Clostridium difficile","volume":"7","author":"Knight","year":"2019","journal-title":"Front Public Health"},{"key":"2023062712551035100_bib20","first-page":"2138","article-title":"Genome analysis of Clostridium difficile PCR ribotype 014 lineage in Australian pigs and humans reveals a diverse genetic repertoire and signatures of long-range interspecies transmission","volume":"7","author":"Knight","year":"2016","journal-title":"Front Microbiol"},{"key":"2023062712551035100_bib21","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1128\/AEM.03032-14","article-title":"Nationwide surveillance study of Clostridium difficile in Australian neonatal pigs shows high prevalence and heterogeneity of PCR ribotypes","volume":"81","author":"Knight","year":"2015","journal-title":"Appl Environ Microbiol"},{"key":"2023062712551035100_bib22","doi-asserted-by":"crossref","first-page":"2630","DOI":"10.1128\/AEM.03951-12","article-title":"Cross-sectional study reveals high prevalence of Clostridium difficile non-PCR ribotype 078 strains in Australian veal calves at slaughter","volume":"79","author":"Knight","year":"2013","journal-title":"Appl Environ Microbiol"},{"key":"2023062712551035100_bib23","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.anaerobe.2016.06.008","article-title":"Reclassification of Clostridium difficile as Clostridioides difficile (Hall and O\u2019Toole 1935) Prevot 1938","volume":"40","author":"Lawson","year":"2016","journal-title":"Anaerobe"},{"key":"2023062712551035100_bib24","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1128\/AAC.00296-20","article-title":"Antimicrobial susceptibilities of Clostridium difficile isolates from 12 Asia-Pacific countries in 2014 and 2015","volume":"64","author":"Lew","year":"2020","journal-title":"Antimicrob Agents Chemother"},{"key":"2023062712551035100_bib25","doi-asserted-by":"crossref","first-page":"1156","DOI":"10.1111\/jam.15408","article-title":"Whole-genome sequencing links Clostridium (Clostridioides) difficile in a single hospital to diverse environmental sources in the community","volume":"133","author":"Lim","year":"2022","journal-title":"J Appl Microbiol"},{"key":"2023062712551035100_bib26","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1111\/jam.13653","article-title":"High prevalence of Clostridium difficile on retail root vegetables, Western Australia","volume":"124","author":"Lim","year":"2018","journal-title":"J Appl Microbiol"},{"key":"2023062712551035100_bib27","doi-asserted-by":"crossref","first-page":"41196","DOI":"10.1038\/srep41196","article-title":"High prevalence of toxigenic Clostridium difficile in public space lawns in Western Australia","volume":"7","author":"Moono","year":"2017","journal-title":"Sci Rep"},{"key":"2023062712551035100_bib28","doi-asserted-by":"crossref","first-page":"256","DOI":"10.1016\/j.anaerobe.2009.09.006","article-title":"Varied prevalence of Clostridium difficile in an integrated swine operation","volume":"15","author":"Norman","year":"2009","journal-title":"Anaerobe"},{"key":"2023062712551035100_bib29","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":"O\u2019Connor","year":"2008","journal-title":"Antimicrob Agents Chemother"},{"key":"2023062712551035100_bib30","doi-asserted-by":"crossref","first-page":"2459","DOI":"10.1007\/s10096-021-04311-5","article-title":"Antimicrobial resistance in Clostridioides difficile","volume":"40","author":"O\u2019Grady","year":"2021","journal-title":"Eur J Clin Microbiol Infect Dis"},{"key":"2023062712551035100_bib31","doi-asserted-by":"crossref","first-page":"102065","DOI":"10.1016\/j.anaerobe.2019.06.018","article-title":"High prevalence of Clostridium difficile in soil, mulch and lawn samples from the grounds of Western Australian hospitals","volume":"60","author":"Perumalsamy","year":"2019","journal-title":"Anaerobe"},{"key":"2023062712551035100_bib32","first-page":"165","article-title":"Evaluation of the BD Max Cdiff assay for the detection of toxigenic Clostridium difficile in human stool specimens","volume":"47","author":"Putsathit","year":"2015","journal-title":"Pathology (Phila)"},{"key":"2023062712551035100_bib33","doi-asserted-by":"crossref","first-page":"108408","DOI":"10.1016\/j.vetmic.2019.108408","article-title":"Molecular epidemiology of Clostridium difficile isolated from piglets","volume":"237","author":"Putsathit","year":"2019","journal-title":"Vet Microbiol"},{"key":"2023062712551035100_bib34","doi-asserted-by":"crossref","first-page":"e00170","DOI":"10.1128\/JCM.00170-18","article-title":"High prevalence of toxigenic and nontoxigenic Clostridium difficile strains in Malaysia","volume":"56","author":"Riley","year":"2018","journal-title":"J Clin Microbiol"},{"key":"2023062712551035100_bib35","doi-asserted-by":"crossref","first-page":"526","DOI":"10.1038\/nrmicro2164","article-title":"Clostridium difficile infection: new developments in epidemiology and pathogenesis","volume":"7","author":"Rupnik","year":"2009","journal-title":"Nat Rev Microbiol"},{"key":"2023062712551035100_bib36","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1071\/HI12057","article-title":"Role of the hospital environment in disease transmission, with a focus on Clostridium difficile","volume":"18","author":"Rutala","year":"2013","journal-title":"Healthcare Infect"},{"key":"2023062712551035100_bib37","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":"2023062712551035100_bib38","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":"2023062712551035100_bib39","first-page":"299","article-title":"Clostridium difficile infection in humans and piglets: a \u2018One Health\u2019 opportunity","volume":"365","author":"Squire","year":"2013","journal-title":"Curr Top Microbiol Immunol"},{"key":"2023062712551035100_bib40","doi-asserted-by":"crossref","first-page":"780","DOI":"10.1016\/j.ajic.2018.12.013","article-title":"Hospital-associated Clostridium difficile infection and reservoirs within the hospital environment","volume":"47","author":"Srinivasa","year":"2019","journal-title":"Am J Infect Control"},{"key":"2023062712551035100_bib41","doi-asserted-by":"crossref","DOI":"10.2807\/1560-7917.ES.2020.25.16.1900479","article-title":"Clostridioides difficile in national food surveillance, Slovenia, 2015 to 2017","volume":"25","author":"Tkalec","year":"2020","journal-title":"Eurosurveillance"},{"key":"2023062712551035100_bib42","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1016\/j.anaerobe.2016.06.002","article-title":"Zoonotic potential of the Clostridium difficile RT078 family in Taiwan","volume":"41","author":"Tsai","year":"2016","journal-title":"Anaerobe"},{"key":"2023062712551035100_bib43","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/j.anaerobe.2016.11.004","article-title":"Survival and prevalence of Clostridium difficile in manure compost derived from pigs","volume":"43","author":"Usui","year":"2017","journal-title":"Anaerobe"},{"key":"2023062712551035100_bib44","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1111\/j.1469-0691.2008.01992.x","article-title":"Infection control measures to limit the spread of Clostridium difficile","volume":"14","author":"Vonberg","year":"2008","journal-title":"Clin Microbiol Infect"},{"key":"2023062712551035100_bib45","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1016\/j.livsci.2007.09.008","article-title":"A survey of manure management on pig farms in northern Vietnam","volume":"112","author":"Vu","year":"2007","journal-title":"Livest Sci"},{"key":"2023062712551035100_bib46","volume-title":"Performance Standards for Antimicrobial Susceptibility Testing: Seventh Informational Supplement M100-S30","author":"Weinstein","year":"2020"},{"key":"2023062712551035100_bib47","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1071\/HI15003","article-title":"The emergence of community-acquired Clostridium difficile in an Australian hospital","volume":"20","author":"Wozniak","year":"2015","journal-title":"Healthcare Infect"},{"key":"2023062712551035100_bib48","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/j.ijmm.2016.02.002","article-title":"Potentially hypervirulent Clostridium difficile PCR ribotype 078 lineage isolates in pigs and possible implications for humans in Taiwan","volume":"306","author":"Wu","year":"2016","journal-title":"Int J Med Microbiol"},{"key":"2023062712551035100_bib49","doi-asserted-by":"crossref","first-page":"e0212965","DOI":"10.1371\/journal.pone.0212965","article-title":"The first isolation of Clostridium difficile RT078\/ST11 from pigs in China","volume":"14","author":"Zhang","year":"2019","journal-title":"PLoS One"},{"key":"2023062712551035100_bib50","doi-asserted-by":"crossref","DOI":"10.1186\/s12866-020-01757-z","article-title":"The molecular characters and antibiotic resistance of Clostridioides difficile from economic animals in China","volume":"20","author":"Zhang","year":"2020","journal-title":"BMC Microbiol"},{"key":"2023062712551035100_bib51","doi-asserted-by":"crossref","first-page":"2244","DOI":"10.1080\/22221751.2021.2005453","article-title":"Comparative genomic and transmission analysis of Clostridioides difficile between environmental, animal, and clinical sources in China","volume":"10","author":"Zhou","year":"2021","journal-title":"Emerg Microbes Infect"}],"container-title":["Journal of Applied Microbiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/jambio\/advance-article-pdf\/doi\/10.1093\/jambio\/lxad118\/50565760\/lxad118.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jambio\/article-pdf\/134\/6\/lxad118\/50722248\/lxad118.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jambio\/article-pdf\/134\/6\/lxad118\/50722248\/lxad118.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,6,27]],"date-time":"2023-06-27T12:58:12Z","timestamp":1687870692000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jambio\/article\/doi\/10.1093\/jambio\/lxad118\/7193377"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,6,1]]},"references-count":51,"journal-issue":{"issue":"6","published-print":{"date-parts":[[2023,6,1]]}},"URL":"https:\/\/doi.org\/10.1093\/jambio\/lxad118","relation":{},"ISSN":["1365-2672"],"issn-type":[{"value":"1365-2672","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2023,6]]},"published":{"date-parts":[[2023,6,1]]},"article-number":"lxad118"}}