{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,29]],"date-time":"2026-10-29T17:13:21Z","timestamp":1793294001158,"version":"4.5.0"},"reference-count":29,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2024,5,28]],"date-time":"2024-05-28T00:00:00Z","timestamp":1716854400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Institut Pasteur (Paris, France)"},{"name":"Sant\u00e9 Publique France (Saint Maurice, France)"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Clostridium perfringens (C. perfringens) is an anaerobic, spore-forming Gram-positive rod responsible for necrotizing gangrene, bacteremia in patients with cancer or gastrointestinal tract infection. C. perfringens virulence is due in large part to toxin production. In 2014, a new enterotoxin, BEC (binary enterotoxin of Clostridium perfringens) encoded by becA and becB genes, distinct from enterotoxin (CPE) encoded by the cpe gene, has been described. BEC-producing strains can be causative agents of acute gastroenteritis in humans. We present herein the case of a 64-year-old man who presented to the emergency department of Toulouse University Hospital with pneumonia and septic shock, without digestive symptoms. Blood cultures showed C. perfringens bacteremia and despite appropriate antibiotic treatment the patient passed away 7 h after admission. The characterization of the strain by whole genome sequencing revealed the presence of typical genes of C. perfringens: plc gene (alpha-toxin, phospholipase C) and pfoA (theta-toxin, perfringolysine). Surprisingly, this strain also harbored becA and becB genes encoding the recently described BEC toxin. Interestingly, alpha-toxin typing of our isolate and other published BEC isolates showed that they belonged to different PLC subtypes, confirming the high genetic diversity of these strains. To our knowledge, it is the first clinical case reporting bacteremia due to a BEC-producing C. perfringens isolate.<\/jats:p>","DOI":"10.3390\/microorganisms12061095","type":"journal-article","created":{"date-parts":[[2024,5,28]],"date-time":"2024-05-28T13:32:55Z","timestamp":1716903175000},"page":"1095","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Binary Enterotoxin Producing Clostridium perfringens Isolated in Blood Cultures: Case Report and Review of the Literature"],"prefix":"10.3390","volume":"12","author":[{"given":"Linda","family":"Ben Sa\u00efd","sequence":"first","affiliation":[{"name":"Department of Microbiology, Toulouse University Hospital, 31059 Toulouse, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9670-3274","authenticated-orcid":false,"given":"Laure","family":"Diancourt","sequence":"additional","affiliation":[{"name":"National Reference Center for Anaerobic Bacteria and Botulism, Institut Pasteur, Universit\u00e9 Paris Cit\u00e9, 75015 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4175-3394","authenticated-orcid":false,"given":"Audrey","family":"Rabeau","sequence":"additional","affiliation":[{"name":"Department of Thoracic Oncology, Toulouse University Hospital, 31000 Toulouse, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Virginie","family":"Gallet","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Toulouse University Hospital, 31059 Toulouse, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5490-4238","authenticated-orcid":false,"given":"Gauthier","family":"Delvallez","sequence":"additional","affiliation":[{"name":"National Reference Center for Anaerobic Bacteria and Botulism, Institut Pasteur, Universit\u00e9 Paris Cit\u00e9, 75015 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marion","family":"Grare","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Toulouse University Hospital, 31059 Toulouse, France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,5,28]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"723","DOI":"10.1080\/21505594.2021.1886777","article-title":"Pathogenicity and virulence of Clostridium perfringens","volume":"12","author":"Gohari","year":"2021","journal-title":"Virulence"},{"key":"ref_2","first-page":"ytac488","article-title":"Gas in the myocardium: A fatal presentation of Clostridium perfringens: A case report","volume":"7","author":"Khan","year":"2023","journal-title":"Eur. Heart J."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1016\/j.jiac.2019.07.019","article-title":"Clinical features of Clostridium bacteremia in cancer patients: A case series review","volume":"26","author":"Yamamoto","year":"2020","journal-title":"J. Infect. Chemother."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"e936329","DOI":"10.12659\/AJCR.936329","article-title":"Clostridium perfringens and Escherichia coli Bacteremia in a patient with acute obstructive suppurative cholangitis: A case report and review of the literature","volume":"23","author":"Zhang","year":"2022","journal-title":"Am. J. Case Rep."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"91","DOI":"10.3947\/ic.2016.48.2.91","article-title":"Anaerobic bacteremia: Impact of inappropriate therapy on mortality","volume":"48","author":"Kim","year":"2016","journal-title":"Infect. Chemother."},{"key":"ref_6","first-page":"1795","article-title":"Two cases of liver abscess caused by Clostridium perfringens after transcatheter arterial chemoembolization","volume":"40","author":"Oshima","year":"2013","journal-title":"Gan Kagaku Ryoho"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"4397","DOI":"10.3748\/wjg.v21.i14.4397","article-title":"Clostridium perfringens infection after transarterial chemoembolization for large hepatocellular carcinoma","volume":"21","author":"Li","year":"2015","journal-title":"World J. Gastroenterol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1016\/j.anaerobe.2018.04.011","article-title":"Expansion of the Clostridium perfringens toxin-based typing scheme","volume":"53","author":"Rood","year":"2018","journal-title":"Anaerobe"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"2390","DOI":"10.1128\/IAI.01759-14","article-title":"BEC, a novel enterotoxin of Clostridium perfringens found in human clinical isolates from acute gastroenteritis outbreaks","volume":"82","author":"Yonogi","year":"2014","journal-title":"Infect. Immun."},{"key":"ref_10","unstructured":"Comit\u00e9 de l\u2019Antibiogramme de la Soci\u00e9t\u00e9 Fran\u00e7aise de Microbiologie (2023, June 18). Recommendations CA-SFM\/EUCAST 2022. Available online: https:\/\/www.sfm-microbiologie.org\/wp-content\/uploads\/2022\/05\/CASFM2022_V1.0.pdf."},{"key":"ref_11","first-page":"137","article-title":"Detection of toxigenic clostridia","volume":"216","author":"Popoff","year":"2003","journal-title":"Methods Mol. Biol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"3813","DOI":"10.1128\/JCM.00983-14","article-title":"Lumbar discitis caused by Clostridium perfringens","volume":"52","author":"Lotte","year":"2014","journal-title":"J. Clin. Microbiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"500","DOI":"10.1016\/j.ygeno.2013.07.011","article-title":"AlienTrimmer: A tool to quickly and accurately trim off multiple short contaminant sequence from high-throughput sequencing reads","volume":"102","author":"Criscuolo","year":"2013","journal-title":"Genomics"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1089\/cmb.2012.0021","article-title":"SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing","volume":"19","author":"Bankevich","year":"2012","journal-title":"J. Comput. Biol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"7060","DOI":"10.1128\/AEM.01486-12","article-title":"A wide variety of Clostridium perfringens type A food-borne isolates that carry a chromosomal cpe gene belong to one multilocus sequence typing cluster","volume":"78","author":"Xiao","year":"2012","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"102473","DOI":"10.1016\/j.anaerobe.2021.102473","article-title":"Clonal diversity of Clostridium perfringens human clinical isolates with various toxin gene profiles based on multilocus sequence typing and alpha-toxin (PLC) typing","volume":"72","author":"Aung","year":"2021","journal-title":"Anaerobe"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1007\/s15010-012-0389-4","article-title":"Population-based assessment of the incidence, risk factors, and outcomes of anaerobic bloodstream infections","volume":"41","author":"Ngo","year":"2013","journal-title":"Infection"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"102202","DOI":"10.1016\/j.anaerobe.2020.102202","article-title":"Clinical relevance of Clostridium bacteremia: An 8-year retrospective study","volume":"63","author":"Stabler","year":"2020","journal-title":"Anaerobe"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1016\/j.jinf.2008.06.018","article-title":"Epidemiology of Clostridium species bacteremia in Calgary, Canada, 2000\u20132006","volume":"57","author":"Leal","year":"2008","journal-title":"J. Infect."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1305","DOI":"10.1007\/s10096-022-04491-8","article-title":"Epidemiology, aetiology and clinical characteristics of clostridial bacteremia: A 6-year population-based observationnal study of 386 patients","volume":"41","author":"Sarasoja","year":"2022","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"584","DOI":"10.1093\/clind\/24.4.584","article-title":"The clinical significance of blood cultures in the 1990s: A prospective comprehensive evaludation of the microbiology, epidemiology, and outcome of bacteremia and fungemia in adults","volume":"24","author":"Weinstein","year":"1997","journal-title":"Clin. Infect. Dis."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"102207","DOI":"10.1016\/j.anaerobe.2020.102207","article-title":"Epidemiology and Microbiological features of anaerobic bacteremia in two French University Hospital","volume":"64","author":"Dumont","year":"2020","journal-title":"Anaerobe"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1007\/s10096-008-0487-5","article-title":"Pronostic factors and impact of antibiotherapy in 117 cases of anaerobic bacteremia","volume":"27","author":"Robert","year":"2008","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1413","DOI":"10.1086\/516355","article-title":"Clinical significance and outcome of anaerobic bacteremia","volume":"26","author":"Salonen","year":"1998","journal-title":"Clin. Infect. Dis."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"859","DOI":"10.1128\/JCM.02859-14","article-title":"Four foodborne disease outbreaks caused by a new type of enterotoxin-producing Clostridium perfringens","volume":"53","author":"Monma","year":"2015","journal-title":"J. Clin. Microbiol."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Matsuda, A., Aung, M.S., Urushibara, N., Kawaguchiya, M., Sumi, A., Nakamura, M., Horino, Y., Ito, M., Habadera, S., and Kobayashi, N. (2019). Prevalence and genetic diversity of toxin genes in clinical isolates of Clostridium perfringens: Coexistence of alpha-toxin variant and binary enterotoxin genes (bec\/cpile). Toxins, 11.","DOI":"10.3390\/toxins11060326"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Kiu, R., Sim, K., Shaw, A., Cornwell, E., Pickard, D., Kroll, J.S., and Hall, L.J. (2019). Genomic analysis of Clostridium perfringens BEC\/CPILE-positive, toxinotype D and E strains isolated from healthy children. Toxins, 11.","DOI":"10.3390\/toxins11090543"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Ueda, K., Kawahara, K., Kimoto, N., Yamaguchi, Y., Yamada, K., Oki, H., Yoshida, T., Matsuda, S., Matsumoto, Y., and Motooka, D. (2022). Analysis of the complete genome sequences of Clostridium perfringens strains harbouring the binary enterotoxin BEC gene and comparative genomics of pCP13-like family plasmids. BMC Genom., 23.","DOI":"10.1186\/s12864-022-08453-4"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1016\/j.jhin.2022.05.011","article-title":"One-day prevalence of asymptomatic carriage of toxigenic and non-toxigenic Clostridioides difficile in 10 French hospitals","volume":"129","author":"Candela","year":"2022","journal-title":"J. Hosp. Infect."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/12\/6\/1095\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:49:44Z","timestamp":1760107784000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/12\/6\/1095"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,5,28]]},"references-count":29,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2024,6]]}},"alternative-id":["microorganisms12061095"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms12061095","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,5,28]]}}}