{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,26]],"date-time":"2026-09-26T10:39:22Z","timestamp":1790419162960,"version":"4.1.0"},"reference-count":39,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2019,11,25]],"date-time":"2019-11-25T00:00:00Z","timestamp":1574640000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"ERANET ANIHWA","award":["ANIBOTNET Project"],"award-info":[{"award-number":["ANIBOTNET Project"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>We report a botulism outbreak in Charolais cattle fed with wheat flour contaminated by Clostridium botulinum type C and the management of the outbreak at each step from the clinical suspicion to the cleaning and disinfection operations. Diagnosis was based on typical suggestive clinical signs and detection of C. botulinum type C using real-time PCR in samples collected from three young affected bulls. All young exposed bulls and cows (18 animals) eventually died, but three young bulls and one cow were recovering when it was decided to euthanize them. C. botulinum type C was detected in the liver of these four animals. Analysis of the ration components demonstrated that wheat flour, wheat, and the mill used to make flour were positive for C. botulinum type C. A dead cat positive for C. botulinum type C was discovered in the silo where wheat grain was stored and was considered the source of contamination. The cat\u2019s entire body was found mummified, well preserved, and not rotting in the silo. Specific measures, in particular, vaccination of the rest of the herd and cleaning and disinfection operations, were implemented to prevent any recurrence of the outbreak. The presence of wild animal carcasses in feed harboring anaerobic conditions like silage, in particular during harvesting, are known to be at risk for the initiation of a botulism outbreak. This outbreak is a reminder that the presence of an animal carcass in feed, regardless of the kind of feed and whenever the contamination occurs, either during harvesting or storage, is sufficient to induce a botulism outbreak.<\/jats:p>","DOI":"10.3390\/ani9121025","type":"journal-article","created":{"date-parts":[[2019,11,25]],"date-time":"2019-11-25T05:52:58Z","timestamp":1574661178000},"page":"1025","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":19,"title":["A Case Report of a Botulism Outbreak in Beef Cattle Due to the Contamination of Wheat by a Roaming Cat Carcass: From the Suspicion to the Management of the Outbreak"],"prefix":"10.3390","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1970-3801","authenticated-orcid":false,"given":"Caroline","family":"Le Mar\u00e9chal","sequence":"first","affiliation":[{"name":"ANSES, Laboratoire de Ploufragan\u2014Plouzan\u00e9, Unit\u00e9 Hygi\u00e8ne et Qualit\u00e9 des Produits Avicoles et Porcins, BP 53, 22440 Ploufragan, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Olivier","family":"Hulin","sequence":"additional","affiliation":[{"name":"Cabinet V\u00e9t\u00e9rinaire de Bletterans, 16, Rue de la Demi-Lune, 39140 Bletterans, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5384-0589","authenticated-orcid":false,"given":"Sabrina","family":"Mac\u00e9","sequence":"additional","affiliation":[{"name":"ANSES, Laboratoire de Ploufragan\u2014Plouzan\u00e9, Unit\u00e9 Hygi\u00e8ne et Qualit\u00e9 des Produits Avicoles et Porcins, BP 53, 22440 Ploufragan, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"C\u00e9cile","family":"Chuzeville","sequence":"additional","affiliation":[{"name":"GDS 71, Loche, 99 Rue des Grands Crus, 71000 M\u00e2con, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sandra","family":"Rouxel","sequence":"additional","affiliation":[{"name":"ANSES, Laboratoire de Ploufragan\u2014Plouzan\u00e9, Unit\u00e9 Hygi\u00e8ne et Qualit\u00e9 des Produits Avicoles et Porcins, BP 53, 22440 Ploufragan, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Typhaine","family":"Po\u00ebzevara","sequence":"additional","affiliation":[{"name":"ANSES, Laboratoire de Ploufragan\u2014Plouzan\u00e9, Unit\u00e9 Hygi\u00e8ne et Qualit\u00e9 des Produits Avicoles et Porcins, BP 53, 22440 Ploufragan, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christelle","family":"Mazuet","sequence":"additional","affiliation":[{"name":"National Reference Center for Anaerobic Bacteria and Botulism, Pasteur Institute, 25-28 rue du Docteur Roux, 75724 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fran\u00e7oise","family":"Pozet","sequence":"additional","affiliation":[{"name":"Laboratoire D\u00e9partemental d\u2019Analyses du Jura, 59 Rue du Vieil H\u00f4pital, 39800 Poligny, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eric","family":"Sellal","sequence":"additional","affiliation":[{"name":"Agrivalys 71, 267 Rue des \u00c9pinoches, 71000 M\u00e2con, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laure","family":"Martin","sequence":"additional","affiliation":[{"name":"ANSES, Laboratoire de Ploufragan\u2014Plouzan\u00e9, Unit\u00e9 Hygi\u00e8ne et Qualit\u00e9 des Produits Avicoles et Porcins, BP 53, 22440 Ploufragan, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alain","family":"Viry","sequence":"additional","affiliation":[{"name":"Laboratoire D\u00e9partemental d\u2019Analyses du Jura, 59 Rue du Vieil H\u00f4pital, 39800 Poligny, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christine","family":"Rubbens","sequence":"additional","affiliation":[{"name":"Direction D\u00e9partementale de la Protection des Populations de la Sa\u00f4ne et Loire, 71 Rue Jean Mac\u00e9, 71000 M\u00e2con, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marianne","family":"Chemaly","sequence":"additional","affiliation":[{"name":"ANSES, Laboratoire de Ploufragan\u2014Plouzan\u00e9, Unit\u00e9 Hygi\u00e8ne et Qualit\u00e9 des Produits Avicoles et Porcins, BP 53, 22440 Ploufragan, France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2019,11,25]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Uzal, F.A., Songer, J.G., Prescott, J.F., and Popoff, M.R. (2016). Botulism. Clostridial Diseases in Animals, Wiley. Chapter 26.","DOI":"10.1002\/9781118728291"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Peck, M.W., Smith, T.J., Anniballi, F., Austin, J.W., Bano, L., Bradshaw, M., Cuervo, P., Cheng, L.W., Derman, Y., and Dorner, B.G. (2017). Historical Perspectives and Guidelines for Botulinum Neurotoxin Subtype Nomenclature. Toxins, 9.","DOI":"10.3390\/toxins9010038"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"3120","DOI":"10.1128\/AEM.07568-11","article-title":"Neurotoxin gene profiling of Clostridium botulinum types C and D native to different countries within Europe","volume":"78","author":"Woudstra","year":"2012","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"523","DOI":"10.1177\/104063870301500603","article-title":"Determination of the median toxic dose of type C botulinum toxin in lactating dairy cows","volume":"15","author":"Moeller","year":"2003","journal-title":"J. Vet. Diagn. Investig."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1016\/j.anaerobe.2017.08.004","article-title":"Identification and characterization of Clostridium botulinum group III field strains by matrix-assisted laser desorption-ionization time-of-flight mass spectrometry (MALDI-TOF MS)","volume":"48","author":"Bano","year":"2017","journal-title":"Anaerobe"},{"key":"ref_6","unstructured":"European Commission Office SDME 08\/96 Commission, L.E. (2006). Tetanus and botulism in animals. Clostridial in Medical, Veterinary and Food Microbiology\u2014Diagnosis and Typing, EU Publications."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1016\/j.vetmic.2009.07.023","article-title":"Characterization of the D\/C mosaic neurotoxin produced by Clostridium botulinum associated with bovine botulism in Japan","volume":"140","author":"Nakamura","year":"2010","journal-title":"Vet. Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1017\/S0950268808000939","article-title":"Type C bovine botulism outbreak due to carcass contaminated non-acidified silage","volume":"137","author":"Myllykoski","year":"2009","journal-title":"Epidemiol. Infect."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"29","DOI":"10.19182\/remvt.7659","article-title":"Fr\u00e9quence au S\u00e9n\u00e9gal du botulisme animal d\u2019origine hydrique","volume":"22","author":"Doutre","year":"1969","journal-title":"Rev. D\u2019\u00c9levage M\u00e9decine V\u00e9t\u00e9rinaire Pays Trop."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"3477","DOI":"10.1017\/S0950268817002382","article-title":"A large outbreak of bovine botulism possibly linked to a massive contamination of grass silage by type D\/C Clostridium botulinum spores on a farm with dairy and poultry operations","volume":"145","author":"Relun","year":"2017","journal-title":"Epidemiol. Infect."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"212","DOI":"10.1016\/j.vetmic.2017.07.022","article-title":"A bovine botulism outbreak associated with a suspected cross-contamination from a poultry farm","volume":"208","author":"Souillard","year":"2017","journal-title":"Vet. Microbiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1177\/104063870001200511","article-title":"Fatal Clostridium botulinum toxicosis in eleven Holstein cattle fed round bale barley haylage","volume":"12","author":"Kelch","year":"2000","journal-title":"J. Vet. Diagn. Investig."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"S183","DOI":"10.1089\/bsp.2012.0076","article-title":"The workshop on animal botulism in Europe","volume":"11","author":"Skarin","year":"2013","journal-title":"Biosecur. Bioterror."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"204","DOI":"10.1177\/104063870001200302","article-title":"Type C botulism in dairy cattle from feed contaminated with a dead cat","volume":"12","author":"Galey","year":"2000","journal-title":"J. Vet. Diagn. Investig."},{"key":"ref_15","unstructured":"(2019, November 22). Legifrance Le Service Public de la Diffusion du Droit. Available online: https:\/\/www.legifrance.gouv.fr\/affichTexte.do?cidTexte=JORFTEXT000027831750&categorieLien=id."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Le Marechal, C., Fourour, S., Ballan, V., Rouxel, S., Souillard, R., and Chemaly, M. (2018). Detection of Clostridium botulinum group III in environmental samples from farms by real-time PCR using four commercial DNA extraction kits. BMC Res. Notes, 11.","DOI":"10.1186\/s13104-018-3549-5"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Vanhomwegen, J., Berthet, N., Mazuet, C., Guigon, G., Vallaeys, T., Stamboliyska, R., Dubois, P., Kennedy, G.C., Cole, S.T., and Caro, V. (2013). Application of high-density DNA resequencing microarray for detection and characterization of botulinum neurotoxin-producing clostridia. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0067510"},{"key":"ref_18","unstructured":"AFSSA (2002). Rapport sur le Botulisme d\u2019Origine Aviaire et Bovine, AFSSA."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"S191","DOI":"10.1089\/bsp.2012.0089","article-title":"Management of animal botulism outbreaks: From clinical suspicion to practical countermeasures to prevent or minimize outbreaks","volume":"11","author":"Anniballi","year":"2013","journal-title":"Biosecur. Bioterror."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1016\/j.anaerobe.2015.09.007","article-title":"Evidence for a natural humoral response in dairy cattle affected by persistent botulism sustained by non-chimeric type C strains","volume":"36","author":"Bano","year":"2015","journal-title":"Anaerobe"},{"key":"ref_21","first-page":"95","article-title":"Concerning 7 cases of bovine botulism C of feline origin: Epidemiological and pathogenical hypotheses","volume":"71","author":"Joubert","year":"1969","journal-title":"Bull. Soc. Sci. Vet. Med. Comp. Lyon"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"143","DOI":"10.17221\/5854-VETMED","article-title":"Descriptive study of botulism in an Austrian dairy herd: A case report","volume":"57","author":"Kummel","year":"2012","journal-title":"Vet. Med."},{"key":"ref_23","first-page":"609","article-title":"An outbreak of botulism among ruminants in connection with ensilage feeding","volume":"21","author":"Fjolstad","year":"1969","journal-title":"Nord. Vet."},{"key":"ref_24","first-page":"513","article-title":"Etude d\u2019un foyer de botulisme bovin d\u00fb \u00e0 Clostridium botulinum C","volume":"88","author":"Prevot","year":"1955","journal-title":"Ann. L\u2019Institut Pasteur Microbiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1128\/aem.41.1.179-183.1981","article-title":"Persistence of Clostridium botulinum type B on a cattle farm after an outbreak of botulism","volume":"41","author":"Notermans","year":"1981","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_26","first-page":"210","article-title":"Presumptive diagnosis of Clostridium botulinum type D intoxication in a herd of feedlot cattle","volume":"42","author":"Heider","year":"2001","journal-title":"Can. Vet. J."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/j.anaerobe.2018.11.003","article-title":"Type C botulism outbreak in feedlot cattle fed contaminated corn silage","volume":"55","author":"Guizelini","year":"2019","journal-title":"Anaerobe"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"881","DOI":"10.1016\/j.vetmic.2012.11.009","article-title":"Improved detection methods by genetic and immunological techniques for botulinum C\/D and D\/C mosaic neurotoxins","volume":"162","author":"Nakamura","year":"2013","journal-title":"Vet. Microbiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"320","DOI":"10.1111\/j.1863-2378.2007.01070.x","article-title":"Optimization of polymerase chain reaction for detection of Clostridium botulinum type C and D in bovine samples","volume":"54","author":"Prevot","year":"2007","journal-title":"Zoonoses Public Health"},{"key":"ref_30","first-page":"238","article-title":"Another outbreak of botulism in cattle","volume":"87","author":"Berg","year":"1975","journal-title":"Nor. Vet."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"438","DOI":"10.1136\/vr.156.14.438","article-title":"Clinical findings and treatment of 30 cattle with botulism","volume":"156","author":"Braun","year":"2005","journal-title":"Vet. Rec."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"5406","DOI":"10.1128\/JCM.42.11.5406-5408.2004","article-title":"Natural Clostridium botulinum type C toxicosis in a group of cats","volume":"42","author":"Elad","year":"2004","journal-title":"J. Clin. Microbiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1136\/vr.155.4.111","article-title":"Association between Key-Gaskell syndrome and infection by Clostridium botulinum type C\/D","volume":"155","author":"Nunn","year":"2004","journal-title":"Vet. Rec."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"558","DOI":"10.1136\/vr.124.21.558","article-title":"Type C botulism in cattle being fed ensiled poultry litter","volume":"124","author":"Neill","year":"1989","journal-title":"Vet. Rec."},{"key":"ref_35","unstructured":"Le Mar\u00e9chal, C., Rouxel, S., Balaine, L., Po\u00ebz\u00e9vara, T., Ballan, V., Chemaly, M., Le Bouquin, S., and Souillard, R. (2017, January 5\u20136). Evaluation de la contamination du fumier suite \u00e0 un \u00e9pisode de botulisme aviaire. Proceedings of the 12\u00e8mes Journ\u00e9es de la Recherche Avicole et Palmip\u00e8des \u00e0 Foie Gras, Tours, France."},{"key":"ref_36","unstructured":"Smith, L.D.S. (1977). Botulism: The Organisms, Its Toxins, the Disease, Charles C Thomas Publisher."},{"key":"ref_37","first-page":"50","article-title":"Clostridium botulinum type C toxin infection in broiler farms in North West Germany","volume":"92","author":"Schettler","year":"1979","journal-title":"Berl. M\u00fcnchener Tier\u00e4rztliche Wochenschr."},{"key":"ref_38","unstructured":"Eklund, M.W., and Dowell, V.R. (1987). Control of botulism in poultry flocks. Avian Botulism: An International Perspective, Charles C. Thomas."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1016\/j.anaerobe.2011.12.013","article-title":"Visceral botulism at dairy farms in Schleswig Holstein, Germany\u2014Prevalence of Clostridium botulinum in feces of cows, in animal feeds, in feces of the farmers, and in house dust","volume":"18","author":"Kruger","year":"2011","journal-title":"Anaerobe"}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/9\/12\/1025\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T13:37:14Z","timestamp":1760189834000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/9\/12\/1025"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,11,25]]},"references-count":39,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2019,12]]}},"alternative-id":["ani9121025"],"URL":"https:\/\/doi.org\/10.3390\/ani9121025","relation":{},"ISSN":["2076-2615"],"issn-type":[{"value":"2076-2615","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,11,25]]}}}