{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,8]],"date-time":"2026-10-08T02:22:27Z","timestamp":1791426147972,"version":"4.3.3"},"reference-count":105,"publisher":"Springer Science and Business Media LLC","issue":"2","license":[{"start":{"date-parts":[[2021,4,23]],"date-time":"2021-04-23T00:00:00Z","timestamp":1619136000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"},{"start":{"date-parts":[[2021,4,23]],"date-time":"2021-04-23T00:00:00Z","timestamp":1619136000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Trop Anim Health Prod"],"published-print":{"date-parts":[[2021,5]]},"DOI":"10.1007\/s11250-021-02728-w","type":"journal-article","created":{"date-parts":[[2021,4,23]],"date-time":"2021-04-23T05:02:48Z","timestamp":1619154168000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":38,"title":["Vaccination against pathogenic clostridia in animals: a review"],"prefix":"10.1007","volume":"53","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1254-3777","authenticated-orcid":false,"given":"Lida","family":"Abdolmohammadi Khiav","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6960-8557","authenticated-orcid":false,"given":"Azadeh","family":"Zahmatkesh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,4,23]]},"reference":[{"key":"2728_CR1","doi-asserted-by":"publisher","first-page":"282","DOI":"10.1016\/j.meegid.2016.03.020","volume":"40","author":"M Alimolaei","year":"2016","unstructured":"Alimolaei, M., Golchin, M., and Daneshvar, H., 2016. Oral immunization of mice against Clostridium perfringens epsilon toxin with a Lactobacillus casei vector vaccine expressing epsilon toxoid, Infection, Genetics and Evolution, 40, 282-287","journal-title":"Infection, Genetics and Evolution"},{"key":"2728_CR2","doi-asserted-by":"publisher","first-page":"681","DOI":"10.1292\/jvms.60.681","volume":"60","author":"K Amimoto","year":"1998","unstructured":"Amimoto, K. et al., 1998. The protective effect of Clostridium novyi type B alpha-toxoid against challenge with spores in guinea pigs, Journal of Veterinary Medical Science, 60, 681-685","journal-title":"Journal of Veterinary Medical Science"},{"key":"2728_CR3","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1292\/jvms.64.67","volume":"64","author":"K Amimoto","year":"2002","unstructured":"Amimoto, K. et al., 2002. Protective effect of Clostridium septicum alpha-toxoid vaccine against challenge with spores in guinea pigs, Journal of Veterinary Medical Science, 64, 67-69","journal-title":"Journal of Veterinary Medical Science"},{"key":"2728_CR4","doi-asserted-by":"publisher","first-page":"1198","DOI":"10.1099\/mic.0.2006\/002287-0","volume":"153","author":"K Amimoto","year":"2007","unstructured":"Amimoto, K. et al., 2007. A novel toxin homologous to large clostridial cytotoxins found in culture supernatant of Clostridium perfringens type C, Microbiology, 153, 1198-1206","journal-title":"Microbiology"},{"key":"2728_CR5","first-page":"31","volume":"32","author":"M Ardehali","year":"1976","unstructured":"Ardehali, M., and Darakhshan, H., 1976. Production and standardization of polyvalent Clostridium perfringens vaccine in Iran, Developments in biological standardization, 32, 31-34","journal-title":"Developments in biological standardization"},{"key":"2728_CR6","first-page":"41","volume":"29","author":"M Ardehali","year":"1977","unstructured":"Ardehali, M., and Darakhshan, H., 1977. Production and standarization of polyvalent Clostridium perfringens vaccine in Iran, Archives of Razi Institute, 29, 41-45","journal-title":"Archives of Razi Institute"},{"issue":"35","key":"2728_CR7","first-page":"23","volume":"34","author":"M Ardehali","year":"1984","unstructured":"Ardehali, M., Darakhshan, H., and Moosawi, M., 1984. Production and standardization of Clostridium oedematiens vaccine in Iran, Archives of Razi Institute, 34,35, 23-26","journal-title":"Archives of Razi Institute"},{"key":"2728_CR8","first-page":"137","volume":"64","author":"M Ardehali","year":"1986","unstructured":"Ardehali, M., Darakhshan, H., and Moosawi, M., 1986. Mass production and standardization of Clostridium oedematiens vaccine against black disease (infectious necrotic hepatitis) of sheep, Developments in biological standardization, 64, 137-140","journal-title":"Developments in biological standardization"},{"key":"2728_CR9","doi-asserted-by":"publisher","first-page":"7904","DOI":"10.1128\/IAI.69.12.7904-7910.2001","volume":"69","author":"MM Awad","year":"2001","unstructured":"Awad, M.M. et al., 2001. Synergistic effects of alpha-toxin and perfringolysin O in Clostridium perfringens-mediated gas gangrene, Infection and Immunity, 69, 7904-7910","journal-title":"Infection and Immunity"},{"key":"2728_CR10","first-page":"226","volume":"8","author":"P Aziminia","year":"2016","unstructured":"Aziminia, P., Pilehchian-Langroudi, R., and Esmaeilnia, K., 2016. Cloning and expression of Clostridium perfringens type D vaccine strain epsilon toxin gene in E. coli as a recombinant vaccine candidate, Iranian Journal of Microbiology, 8, 226-231","journal-title":"Iranian Journal of Microbiology"},{"key":"2728_CR11","doi-asserted-by":"publisher","first-page":"1","DOI":"10.4102\/ojvr.v83i1.1136","volume":"83","author":"F Bakhshi","year":"2016","unstructured":"Bakhshi, F., Langroudi, R.P., and Eimani, B.G., 2016. Enhanced expression of recombinant beta toxin of Clostridium perfringens type B using a commercially available Escherichia coli strain, Onderstepoort Journal of Veterinary Research, 83, 1-4","journal-title":"Onderstepoort Journal of Veterinary Research"},{"key":"2728_CR12","first-page":"161","volume":"51","author":"L Baldassi","year":"1985","unstructured":"Baldassi, L. et al., 1985. Observa\u00e7\u00f5es sobre a incid\u00eancia de gangrena gasosa e carb\u00fanculo sintom\u00e1tico durante 10 anos, 1970-79, no estado de S\u00e3o Paulo, Biol\u00f3gico, S\u00e3o Paulo, 51, 161-165","journal-title":"Biol\u00f3gico, S\u00e3o Paulo"},{"key":"2728_CR13","doi-asserted-by":"publisher","first-page":"552","DOI":"10.1093\/occmed\/kqm110","volume":"57","author":"D Baxter","year":"2007","unstructured":"Baxter, D., 2007. Active and passive immunity, vaccine types, excipients and licensing, Occupational Medicine, 57, 552\u2013556.","journal-title":"Occupational Medicine"},{"key":"2728_CR14","first-page":"15","volume":"69","author":"Z Bozorgkhoo","year":"2014","unstructured":"Bozorgkhoo, Z. et al., 2014. Molecular cloning of Clostridium septicum vaccine strain alpha toxin gene in E. coli, Archives of Razi Institute, 69, 15-20","journal-title":"Archives of Razi Institute"},{"key":"2728_CR15","doi-asserted-by":"publisher","first-page":"985","DOI":"10.1099\/0022-1317-51-11-985","volume":"51","author":"J Brazier","year":"2002","unstructured":"Brazier, J. et al., 2002. Isolation and identification of Clostridium spp. from infections associated with the injection of drugs: experiences of a microbiological investigation team, Journal of Medical Microbiology, 51, 985-989","journal-title":"Journal of Medical Microbiology"},{"key":"2728_CR16","doi-asserted-by":"publisher","first-page":"221","DOI":"10.1111\/mmi.12469","volume":"91","author":"GP Carter","year":"2014","unstructured":"Carter, G.P. et al., 2014. Regulation of toxin production in the pathogenic clostridia, Molecular Microbiology, 91, 221-231","journal-title":"Molecular Microbiology"},{"key":"2728_CR17","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1016\/j.anaerobe.2011.10.001","volume":"18","author":"C Coursodon","year":"2012","unstructured":"Coursodon, C. et al., 2012. TpeL-producing strains of Clostridium perfringens type A are highly virulent for broiler chicks, Anaerobe, 18, 117-121","journal-title":"Anaerobe"},{"key":"2728_CR18","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1128\/iai.38.1.21-26.1982","volume":"38","author":"SJ Cryz Jr","year":"1982","unstructured":"Cryz Jr, S. J., Furer, E., and Germanier, R., 1982. Effect of chemical and heat inactivation on the antigenicity and immunogenicity of Vibrio cholerae, Infection and Immunology, 38, 21\u201326","journal-title":"Infection and Immunology"},{"key":"2728_CR19","doi-asserted-by":"publisher","first-page":"4003","DOI":"10.1016\/j.vaccine.2013.05.063","volume":"31","author":"SPF da Costa","year":"2013","unstructured":"da Costa, S.P.F. et al., 2013. Protection against avian necrotic enteritis after immunisation with NetB genetic or formaldehyde toxoids, Vaccine, 31, 4003-4008","journal-title":"Vaccine"},{"key":"2728_CR20","first-page":"106","volume":"7","author":"FA Daryaei","year":"2017","unstructured":"Daryaei, F.A., Langroudi, R.P., and Golestani Eimani, B., 2017. Production and Evaluation of a New Recombinant Cloning Vector for the Clostridium novyi Type B Vaccine Strain Alpha Toxin Gene, EC Microbiology, 7, 106-111","journal-title":"EC Microbiology"},{"key":"2728_CR21","doi-asserted-by":"publisher","first-page":"140","DOI":"10.1016\/j.molimm.2015.12.001","volume":"70","author":"S Das","year":"2016","unstructured":"Das, S. et al., 2016. Generation and characterization of recombinant bivalent fusion protein r-Cpib for immunotherapy against Clostridium perfringens beta and iota toxemia, Molecular Immunology, 70, 140-148","journal-title":"Molecular Immunology"},{"key":"2728_CR22","doi-asserted-by":"publisher","first-page":"3139","DOI":"10.1016\/j.vaccine.2014.04.006","volume":"32","author":"O Dhungyel","year":"2014","unstructured":"Dhungyel, O., Hunter, J., and Whittington, R., 2014. Footrot vaccines and vaccination, Vaccine, 32, 3139\u20133146","journal-title":"Vaccine"},{"key":"2728_CR23","doi-asserted-by":"publisher","first-page":"85","DOI":"10.21608\/jcvr.2015.37191","volume":"9","author":"A El-sify","year":"2015","unstructured":"El-sify, A., 2015. A review on Clostridium perfringens toxins with special reference to Beta 2 toxin, Journal of Current Veterinary Research, 9, 85-100","journal-title":"Journal of Current Veterinary Research"},{"key":"2728_CR24","unstructured":"Fathi Nahafi, M. et al., 2014. Bioinformatics identification, cloning and partial purification of antigenic regions of Clostridium novyi alpha toxin for immunization. 12th International congress of Immunology & Allergy of Iran, 2014"},{"key":"2728_CR25","unstructured":"Fathi Najafi, M. et al., 1398. Induction of alpha toxin production and reduction of time of cultivation of Clostridium novyi for vaccine production, Proceedings of the twentieth congress of Microbiology, Kerman, 1398"},{"issue":"3","key":"2728_CR26","first-page":"385","volume":"75","author":"M Fathi Najafi","year":"2020","unstructured":"Fathi Najafi, M., Rahman Mashhadi, M., and Hemmaty, M., 2020. Effectiveness of Chitosan Nanoparticles in Development of Pentavalent Clostridial Toxoid Vaccine in Terms of Clinical Pathology Elements and Immunological Responses, Archives of Razi Institute, 75, 3, 385-395","journal-title":"Archives of Razi Institute"},{"key":"2728_CR27","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-019-50683-2","volume":"9","author":"MKC Felix","year":"2019","unstructured":"Felix, M.K.C. et al., 2019. Inactivated alpha toxin from Clostridium novyi type B in nano-emulsion protect partially protects Swiss mice from lethal alpha toxin challenge, Scientific Reports, 9, 1-9","journal-title":"Scientific Reports"},{"key":"2728_CR28","doi-asserted-by":"publisher","first-page":"381","DOI":"10.1080\/03079457.2015.1129663","volume":"45","author":"SP Fernandes da Costa","year":"2016","unstructured":"Fernandes da Costa, S.P. et al., 2016. Variable protection against experimental broiler necrotic enteritis after immunization with the C-terminal fragment of Clostridium perfringens alpha-toxin and a non-toxic NetB variant, Avian Pathology, 45, 381-388","journal-title":"Avian Pathology"},{"key":"2728_CR29","doi-asserted-by":"publisher","first-page":"5200","DOI":"10.1128\/IAI.00534-06","volume":"74","author":"DJ Fisher","year":"2006","unstructured":"Fisher, D.J. et al., 2006. Dissecting the contributions of Clostridium perfringens type C toxins to lethality in the mouse intravenous injection model, Infection and Immunity, 74, 5200-5210","journal-title":"Infection and Immunity"},{"key":"2728_CR30","doi-asserted-by":"crossref","unstructured":"Fortier, L.-C., 2017. The contribution of bacteriophages to the biology and virulence of pathogenic clostridia. In: Advances in Applied Microbiology, (Elsevier, 169-200)","DOI":"10.1016\/bs.aambs.2017.05.002"},{"key":"2728_CR31","doi-asserted-by":"publisher","first-page":"73","DOI":"10.3390\/toxins8030073","volume":"8","author":"JC Freedman","year":"2016","unstructured":"Freedman, J.C., Shrestha, A., and McClane, B.A., 2016. Clostridium perfringens enterotoxin: action, genetics, and translational applications, Toxins, 8, 73","journal-title":"Toxins"},{"key":"2728_CR32","doi-asserted-by":"publisher","first-page":"5500","DOI":"10.1016\/j.vaccine.2012.06.050","volume":"30","author":"J Frey","year":"2012","unstructured":"Frey, J. et al., 2012. Cytotoxin CctA, a major virulence factor of Clostridium chauvoei conferring protective immunity against myonecrosis, Vaccine, 30, 5500-5505","journal-title":"Vaccine"},{"key":"2728_CR33","doi-asserted-by":"publisher","first-page":"32","DOI":"10.1186\/1746-6148-10-32","volume":"10","author":"E Goossens","year":"2014","unstructured":"Goossens, E. et al., 2014. Clostridium perfringens strains from bovine enterotoxemia cases are not superior in in vitro production of alpha toxin, perfringolysin O and proteolytic enzymes, BMC Veterinary Research, 10, 32","journal-title":"BMC Veterinary Research"},{"key":"2728_CR34","doi-asserted-by":"publisher","first-page":"52","DOI":"10.1186\/s13567-016-0336-y","volume":"47","author":"E Goossens","year":"2016","unstructured":"Goossens, E. et al., 2016. The C-terminal domain of Clostridium perfringens alpha toxin as a vaccine candidate against bovine necrohemorrhagic enteritis, Veterinary Research, 47, 52","journal-title":"Veterinary Research"},{"key":"2728_CR35","doi-asserted-by":"crossref","unstructured":"Granum, P.E., Whitaker, J.R., and Skjelkv\u00e5le, R., 1981. Trypsin activation of enterotoxin from Clostridium perfringens type A fragmentation and some physicochemical properties, Biochimica et Biophysica Acta (BBA)-Protein Structure, 668, 325-332","DOI":"10.1016\/0005-2795(81)90165-3"},{"key":"2728_CR36","first-page":"1741","volume":"5","author":"A Haghroosta","year":"2014","unstructured":"Haghroosta, A. et al., 2014. Study on efficiency of blackleg vaccine in cattle in Khuzestan. province, Iran, Research Journal of Pharmaceutical, Biological and Chemical Sciences, 5, 1741-1746","journal-title":"Biological and Chemical Sciences"},{"key":"2728_CR37","doi-asserted-by":"publisher","first-page":"243","DOI":"10.1016\/j.anaerobe.2004.04.006","volume":"10","author":"PJ Hauer","year":"2004","unstructured":"Hauer, P.J., Yeary, T.J., and Rosenbusch, R.F., 2004. Cloning and molecular characterization of the beta toxin (phospholipase C) gene of Clostridium haemolyticum, Anaerobe, 10, 243-254","journal-title":"Anaerobe"},{"key":"2728_CR38","doi-asserted-by":"publisher","first-page":"91","DOI":"10.1093\/intimm\/dxy071","volume":"31","author":"K Hosomi","year":"2019","unstructured":"Hosomi, K. et al., 2019. Development of a bivalent food poisoning vaccine: augmented antigenicity of the C-terminus of Clostridium perfringens enterotoxin by fusion with the B subunit of Escherichia coli Shiga toxin 2, International Immunology, 31, 91-100","journal-title":"International Immunology"},{"key":"2728_CR39","doi-asserted-by":"publisher","first-page":"933","DOI":"10.1038\/nnano.2013.254","volume":"8","author":"C-MJ Hu","year":"2013","unstructured":"Hu, C-M.J. et al., 2013. Nanoparticle-detained toxins for safe andeffective vaccination. Nature Nanotechnology, 8, 933-938","journal-title":"Nature Nanotechnology"},{"key":"2728_CR40","volume-title":"Preparation and evaluation of Improved blackleg and hemorrhagic septicemia vaccine","author":"AR Jabbari","year":"2008","unstructured":"Jabbari, A.R. et al., 2008. Preparation and evaluation of Improved blackleg and hemorrhagic septicemia vaccine,"},{"key":"2728_CR41","doi-asserted-by":"publisher","first-page":"621","DOI":"10.1111\/1348-0421.12198","volume":"58","author":"Z Jiang","year":"2014","unstructured":"Jiang, Z. et al., 2014. Induction of potential protective immunity against enterotoxemia in calves by single or multiple recombinant Clostridium perfringens toxoids, Microbiology and Immunology, 58, 621-627","journal-title":"Microbiology and Immunology"},{"key":"2728_CR42","doi-asserted-by":"crossref","first-page":"1515","DOI":"10.2460\/ajvr.1977.38.10.1515","volume":"38","author":"K Kennedy","year":"1977","unstructured":"Kennedy, K. et al., 1977. Vaccination of cattle and sheep with a combined Clostridium perfringens types C and D toxoid, American Journal of Veterinary Research, 38, 1515-1517","journal-title":"American Journal of Veterinary Research"},{"key":"2728_CR43","doi-asserted-by":"publisher","first-page":"943","DOI":"10.1128\/IAI.01267-08","volume":"77","author":"CL Kennedy","year":"2009","unstructured":"Kennedy, C.L. et al., 2009. Pore-forming activity of alpha-toxin is essential for Clostridium septicum-mediated myonecrosis, Infection and Immunity, 77, 943-951","journal-title":"Infection and Immunity"},{"key":"2728_CR44","doi-asserted-by":"publisher","first-page":"e26","DOI":"10.1371\/journal.ppat.0040026","volume":"4","author":"AL Keyburn","year":"2008","unstructured":"Keyburn, A.L. et al., 2008. NetB, a new toxin that is associated with avian necrotic enteritis caused by Clostridium perfringens, PLoS Pathogens, 4, e26","journal-title":"PLoS Pathogens"},{"key":"2728_CR45","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1051\/vetres\/2009069","volume":"41","author":"AL Keyburn","year":"2010","unstructured":"Keyburn, A.L. et al., 2010. Association between avian necrotic enteritis and Clostridium perfringens strains expressing NetB toxin, Veterinary Research, 41, 1-8","journal-title":"Veterinary Research"},{"key":"2728_CR46","doi-asserted-by":"publisher","first-page":"54","DOI":"10.1186\/1297-9716-44-54","volume":"44","author":"AL Keyburn","year":"2013","unstructured":"Keyburn, A.L. et al., 2013. Vaccination with recombinant NetB toxin partially protects broiler chickens from necrotic enteritis, Veterinary Research, 44, 54","journal-title":"Veterinary Research"},{"key":"2728_CR47","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41426-018-0144-8","volume":"7","author":"R Kiu","year":"2018","unstructured":"Kiu, R., and Hall, L.J., 2018. An update on the human and animal enteric pathogen Clostridium perfringens, Emerging Microbes & Infections, 7, 1-15","journal-title":"Emerging Microbes & Infections"},{"key":"2728_CR48","doi-asserted-by":"publisher","first-page":"359","DOI":"10.1016\/S0378-1135(00)00256-X","volume":"76","author":"A Kojima","year":"2000","unstructured":"Kojima, A. et al., 2000. Cloning and expression of a gene encoding the flagellin of Clostridium chauvoei, Veterinary Microbiology, 76, 359-372","journal-title":"Veterinary Microbiology"},{"key":"2728_CR49","doi-asserted-by":"publisher","first-page":"566","DOI":"10.1637\/10826-032314-Reg.1","volume":"58","author":"CA Lancto","year":"2014","unstructured":"Lancto, C.A. et al., 2014. A noncytolytic \u03b1 toxin recombinant protein protects turkeys against Clostridium septicum challenge, Avian Diseases, 58, 566-571","journal-title":"Avian Diseases"},{"key":"2728_CR50","first-page":"297","volume":"68","author":"R Langroudi","year":"2013","unstructured":"Langroudi, R., and Jabbari, A., 2013. Production of Braxy vaccine by fermenter and enriched culture media, Journal of Veterinary Research, 68, 297-304","journal-title":"Journal of Veterinary Research"},{"key":"2728_CR51","first-page":"43","volume":"67","author":"R Langroudi","year":"2012","unstructured":"Langroudi, R., Jabbari, A., and Shoshtari, M., 2012. Large scale production of blackleg vaccine by fermenter and enriched culture medium in Iran, Archives of Razi Institute, 67, 43-49","journal-title":"Archives of Razi Institute"},{"key":"2728_CR52","doi-asserted-by":"publisher","first-page":"3295","DOI":"10.1016\/j.vaccine.2013.04.061","volume":"31","author":"RP Langroudi","year":"2013","unstructured":"Langroudi, R.P., Shamsara, M., and Aghaiypour, K., 2013. Expression of Clostridium perfringens epsilon-beta fusion toxin gene in E. coli and its immunologic studies in mouse, Vaccine, 31, 3295-3299","journal-title":"Vaccine"},{"key":"2728_CR53","doi-asserted-by":"publisher","first-page":"341","DOI":"10.3390\/toxins8110341","volume":"8","author":"J Li","year":"2016","unstructured":"Li, J., Uzal, F.A., and McClane, B.A., 2016. Clostridium perfringens sialidases: potential contributors to intestinal pathogenesis and therapeutic targets, Toxins, 8, 341","journal-title":"Toxins"},{"key":"2728_CR54","doi-asserted-by":"publisher","first-page":"192","DOI":"10.1016\/j.fm.2010.03.020","volume":"28","author":"M Lindstr\u00f6m","year":"2011","unstructured":"Lindstr\u00f6m, M. et al., 2011. Novel insights into the epidemiology of Clostridium perfringens type A food poisoning, Food Microbiology, 28, 192-198","journal-title":"Food Microbiology"},{"key":"2728_CR55","doi-asserted-by":"publisher","first-page":"6125","DOI":"10.1016\/j.vaccine.2010.07.046","volume":"28","author":"FC Lobato","year":"2010","unstructured":"Lobato, F.C. et al., 2010. Potency against enterotoxemia of a recombinant Clostridium perfringens type D epsilon toxoid in ruminants, Vaccine, 28, 6125-6127","journal-title":"Vaccine"},{"key":"2728_CR56","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1080\/0379450310001636255","volume":"33","author":"A Lovland","year":"2004","unstructured":"Lovland, A. et al., 2004. Maternal vaccination against subclinical necrotic enteritis in broilers, Avian Pathology, 33, 81-90","journal-title":"Avian Pathology"},{"key":"2728_CR57","first-page":"103","volume":"10","author":"H Mamandi","year":"2019","unstructured":"Mamandi, H., Golestani Eimani, B., and Pilehchian Langroudi, R., 2019. Cloning of Tpel Gene of Clostridium perfringens in E. coli, Modares Journal of Biotechnology, 10, 103-107","journal-title":"Modares Journal of Biotechnology"},{"key":"2728_CR58","doi-asserted-by":"publisher","first-page":"617","DOI":"10.1016\/0163-7258(80)90031-5","volume":"10","author":"JL McDonel","year":"1980","unstructured":"McDonel, J.L., 1980. Clostridium perfringens toxins (type a, b, c, d, e), Pharmacology & Therapeutics, 10, 617-655","journal-title":"Pharmacology & Therapeutics"},{"key":"2728_CR59","doi-asserted-by":"publisher","first-page":"6235","DOI":"10.1074\/jbc.M310752200","volume":"279","author":"B Metz","year":"2004","unstructured":"Metz, B. et al., 2004. Identification of formaldehyde-induced modifications in proteins: reactions with model peptides, Journal of Biological Chemistry, 279, 6235\u20136243","journal-title":"Journal of Biological Chemistry"},{"key":"2728_CR60","doi-asserted-by":"publisher","first-page":"363","DOI":"10.1016\/j.anaerobe.2012.01.004","volume":"18","author":"A Milach","year":"2012","unstructured":"Milach, A. et al., 2012. Production and characterization of Clostridium perfringens recombinant \u03b2 toxoid, Anaerobe, 18, 363-365","journal-title":"Anaerobe"},{"key":"2728_CR61","first-page":"415","volume":"53","author":"W Moore","year":"1968","unstructured":"Moore, W., 1968. Solidified media suitable for the cultivation of Clostridium novyi type B, Microbiology, 53, 415-423","journal-title":"Microbiology"},{"issue":"39","key":"2728_CR62","first-page":"83","volume":"38","author":"M Moosawi","year":"1988","unstructured":"Moosawi, M., 1988. Production and standardization two types of clostridial - vaccines for sheep and cattle, Archives of Razi Institute, 38,39, 83-88","journal-title":"Archives of Razi Institute"},{"key":"2728_CR63","doi-asserted-by":"publisher","first-page":"22816","DOI":"10.1038\/srep22816","volume":"6","author":"GMSG Moreira","year":"2016","unstructured":"Moreira, G.M.S.G. et al., 2016. Immunogenicity of a trivalent recombinant vaccine against Clostridium perfringens alpha, beta, and epsilon toxins in farm ruminants, Scientific Reports, 6, 22816","journal-title":"Scientific Reports"},{"key":"2728_CR64","doi-asserted-by":"crossref","unstructured":"Nagahama, M., Oda, M., and Kobayashi, K., 2012. Glycosylating Toxin of Clostridium perfringens. Glycosylation, 2012, IntechOpen,","DOI":"10.5772\/48112"},{"key":"2728_CR65","doi-asserted-by":"publisher","first-page":"340","DOI":"10.1111\/1348-0421.12036","volume":"57","author":"M Nagahama","year":"2013","unstructured":"Nagahama, M. et al., 2013. A recombinant carboxy-terminal domain of alpha-toxin protects mice against Clostridium perfringens, Microbiology and Immunology, 57, 340-345","journal-title":"Microbiology and Immunology"},{"key":"2728_CR66","doi-asserted-by":"publisher","first-page":"396","DOI":"10.3390\/toxins7020396","volume":"7","author":"M Nagahama","year":"2015","unstructured":"Nagahama, M. et al., 2015. Recent insights into Clostridium perfringens beta-toxin, Toxins, 7, 396-406","journal-title":"Toxins"},{"key":"2728_CR67","doi-asserted-by":"publisher","first-page":"275","DOI":"10.1002\/9781118728291.ch23","volume-title":"Infectious necrotic hepatitis, Clostridial Diseases of Animals","author":"M Navarro","year":"2016","unstructured":"Navarro, M., and Uzal, F.A., 2016. Infectious necrotic hepatitis, Clostridial Diseases of Animals. 1st ed. Ames, IA: Wiley Blackwell, 275-279","edition":"1"},{"key":"2728_CR68","doi-asserted-by":"publisher","first-page":"78","DOI":"10.1016\/j.anaerobe.2019.02.011","volume":"56","author":"P Nicholson","year":"2019","unstructured":"Nicholson, P. et al., 2019. Production of neutralizing antibodies against the secreted Clostridium chauvoei toxin A (CctA) upon blackleg vaccination, Anaerobe, 56, 78-87","journal-title":"Anaerobe"},{"key":"2728_CR69","doi-asserted-by":"publisher","first-page":"1219","DOI":"10.3906\/biy-1507-121","volume":"40","author":"NG Noshahri","year":"2016","unstructured":"Noshahri, N.G. et al., 2016. Identification and cloning of highly epitopic regions of Clostridium novyi alpha toxin, Turkish Journal of Biology, 40, 1219-1226","journal-title":"Turkish Journal of Biology"},{"key":"2728_CR70","doi-asserted-by":"publisher","first-page":"5268","DOI":"10.3390\/toxins7124880","volume":"7","author":"M Oda","year":"2015","unstructured":"Oda, M. et al., 2015. Membrane-binding mechanism of Clostridium perfringens alpha-toxin, Toxins, 7, 5268-5275","journal-title":"Toxins"},{"key":"2728_CR71","doi-asserted-by":"publisher","first-page":"743","DOI":"10.1136\/bmj.1.5175.743","volume":"1","author":"HJ Parish","year":"1960","unstructured":"Parish, H. J. and Cannon, D. A., 1960. Staphylococcal infection: antitoxic immunity, British Medical Journal, 1, 743\u2013747","journal-title":"British Medical Journal"},{"key":"2728_CR72","unstructured":"Pilehchian, R., Moosawi, M., and Ardehali, M., 2002. Large scale cultivation of C. Chauvoei (blackleg) vaccine by fermenter. Proceedings of the the 3rd international Iran and Russia conference, Moscow, 2002, 18-20"},{"key":"2728_CR73","doi-asserted-by":"publisher","first-page":"4602","DOI":"10.1111\/j.1742-4658.2011.08145.x","volume":"278","author":"MR Popoff","year":"2011","unstructured":"Popoff, M.R., 2011. Epsilon toxin: a fascinating pore-forming toxin, The FEBS Journal, 278, 4602-4615","journal-title":"The FEBS Journal"},{"key":"2728_CR74","doi-asserted-by":"crossref","unstructured":"Ramadan, N.M. et al., 2020. Oral immunization of broilers with chitosan nano-encapsulated extracellular and cell wall proteins of necrotic enteritis-induced Clostridium perfringens, bioRxiv, 1-36","DOI":"10.1101\/2020.10.23.351817"},{"key":"2728_CR75","unstructured":"Roberts, D.S., 2000. Multicomponent clostridial vaccines using saponin adjuvants. 2000, Google Patents,"},{"key":"2728_CR76","first-page":"311","volume-title":"Gas Gangrene","author":"M Robertson","year":"1943","unstructured":"Robertson, M., and Keppie, J., 1943. Gas Gangrene. Active Immunisation by means of concentrated toxoids, Lancet, 311-314"},{"key":"2728_CR77","doi-asserted-by":"publisher","first-page":"295","DOI":"10.1080\/03079457.2016.1158781","volume":"45","author":"JI Rood","year":"2016","unstructured":"Rood, J.I., Keyburn, A.L., and Moore, R.J., 2016. NetB and necrotic enteritis: the hole movable story, Avian Pathology, 45, 295-301","journal-title":"Avian Pathology"},{"key":"2728_CR78","doi-asserted-by":"crossref","unstructured":"Rossi, A. et al., 2018. Temporal evolution of anti-Clostridium antibody responses in sheep after vaccination with polyvalent Clostridial vaccines. Veterinary Immunology and Immunopathology, 46-51","DOI":"10.1016\/j.vetimm.2018.06.010"},{"key":"2728_CR79","first-page":"39","volume":"30","author":"A Rostami","year":"2016","unstructured":"Rostami, A. et al., 2016. Design and expression of a chimeric vaccine candidate for avian necrotic enteritis, Protein Engineering, Design and Selection, 30, 39-45","journal-title":"Protein Engineering, Design and Selection"},{"key":"2728_CR80","doi-asserted-by":"publisher","first-page":"4152","DOI":"10.1016\/j.vaccine.2013.06.094","volume":"31","author":"FM Salvarani","year":"2013","unstructured":"Salvarani, F.M. et al., 2013. Vaccination with recombinant Clostridium perfringens toxoids \u03b1 and \u03b2 promotes elevated antepartum and passive humoral immunity in swine, Vaccine, 31, 4152-4155","journal-title":"Vaccine"},{"key":"2728_CR81","doi-asserted-by":"crossref","unstructured":"Sargison, N., 2009. Sheep flock health: a planned approach, (John Wiley & Sons)","DOI":"10.1002\/9781444302592"},{"key":"2728_CR82","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1016\/j.anaerobe.2005.10.002","volume":"12","author":"YS Sawires","year":"2006","unstructured":"Sawires, Y.S., and Songer, J.G., 2006. Clostridium perfringens: insight into virulence evolution and population structure, Anaerobe, 12, 23-43","journal-title":"Anaerobe"},{"key":"2728_CR83","doi-asserted-by":"publisher","first-page":"495","DOI":"10.1128\/IAI.00838-09","volume":"78","author":"S Sayeed","year":"2010","unstructured":"Sayeed, S., Li, J., and McClane, B.A., 2010. Characterization of virulence plasmid diversity among Clostridium perfringens type B isolates, Infection and Immunity, 78, 495-504","journal-title":"Infection and Immunity"},{"key":"2728_CR84","doi-asserted-by":"publisher","first-page":"25173","DOI":"10.1074\/jbc.271.41.25173","volume":"271","author":"J Selzer","year":"1996","unstructured":"Selzer, J. et al., 1996. Clostridium novyi \u03b1-toxin-catalyzed incorporation of GlcNAc into Rho subfamily proteins, Journal of Biological Chemistry, 271, 25173-25177","journal-title":"Journal of Biological Chemistry"},{"key":"2728_CR85","first-page":"107","volume":"73","author":"P Seyed Sayyah","year":"2018","unstructured":"Seyed Sayyah, P., Golestani Eimani, B., and Pilehchian Langroudi, R., 2018. Cloning of Clostridium perfringens Iota toxin gene in Escherichia coli, Archives of Razi Institute, 73, 107-111","journal-title":"Archives of Razi Institute"},{"key":"2728_CR86","doi-asserted-by":"publisher","first-page":"10284","DOI":"10.1021\/bi000436r","volume":"39","author":"LA Shepard","year":"2000","unstructured":"Shepard, L.A. et al., 2000. The mechanism of pore assembly for a cholesterol-dependent cytolysin: formation of a large prepore complex precedes the insertion of the transmembrane \u03b2-hairpins, Biochemistry, 39, 10284-10293","journal-title":"Biochemistry"},{"key":"2728_CR87","doi-asserted-by":"crossref","unstructured":"Shimizu, T. et al., 2002. Complete genome sequence of Clostridium perfringens, an anaerobic flesh-eater, Proceedings of the National Academy of Sciences, 99, 996-1001","DOI":"10.1073\/pnas.022493799"},{"key":"2728_CR88","doi-asserted-by":"crossref","unstructured":"Skarin, H., and Segerman, B., 2014. Plasmidome interchange between Clostridium botulinum, Clostridium novyi and Clostridium haemolyticum converts strains of independent lineages into distinctly different pathogens, PloS One, 9","DOI":"10.1371\/journal.pone.0107777"},{"key":"2728_CR89","doi-asserted-by":"publisher","first-page":"216","DOI":"10.1128\/CMR.9.2.216","volume":"9","author":"JG Songer","year":"1996","unstructured":"Songer, J.G., 1996. Clostridial enteric diseases of domestic animals, Clinical Microbiology Reviews, 9, 216","journal-title":"Clinical Microbiology Reviews"},{"key":"2728_CR90","doi-asserted-by":"publisher","first-page":"141","DOI":"10.5897\/AJMR2017.8507","volume":"12","author":"H Sori","year":"2018","unstructured":"Sori, H. et al., 2018. Evaluation of safety and immunogenicity of combined blackleg and hemorrhagic septicemia vaccine, African Journal of Microbiology Research, 12, 141-146","journal-title":"African Journal of Microbiology Research"},{"key":"2728_CR91","doi-asserted-by":"publisher","first-page":"333","DOI":"10.1111\/j.1574-695X.1999.tb01302.x","volume":"24","author":"S Springer","year":"1999","unstructured":"Springer, S., and Selbitz, H.-J., 1999. The control of necrotic enteritis in sucking piglets by means of a Clostridium perfringens toxoid vaccine, FEMS Immunology & Medical Microbiology, 24, 333-336","journal-title":"FEMS Immunology & Medical Microbiology"},{"key":"2728_CR92","doi-asserted-by":"publisher","first-page":"254","DOI":"10.1016\/j.anaerobe.2011.11.001","volume":"18","author":"DL Stevens","year":"2012","unstructured":"Stevens, D.L., Aldape, M.J., and Bryant, A.E., 2012. Life-threatening clostridial infections, Anaerobe, 18, 254-259","journal-title":"Anaerobe"},{"key":"2728_CR93","first-page":"1469","volume":"4","author":"A Taherian Fard","year":"2010","unstructured":"Taherian Fard, A. et al., 2010. Cloning and expression of C-terminal of Clostridium perfringens type A enterotoxin and its biological activity, African Journal of Microbiology Research, 4, 1469-1474","journal-title":"African Journal of Microbiology Research"},{"key":"2728_CR94","doi-asserted-by":"publisher","first-page":"247","DOI":"10.3390\/toxins9080247","volume":"9","author":"M Takehara","year":"2017","unstructured":"Takehara, M. et al., 2017. Cellular entry of Clostridium perfringens iota-toxin and Clostridium botulinum C2 toxin, Toxins, 9, 247","journal-title":"Toxins"},{"issue":"2","key":"2728_CR95","doi-asserted-by":"publisher","first-page":"211","DOI":"10.1007\/s00253-006-0465-8","volume":"72","author":"K Terpe","year":"2006","unstructured":"Terpe, K., 2006. Overview of bacterial expression systems for heterologous protein production: from molecular and biochemical fundamentals to commercial systems. Applied Microbiology and Biotechnology, 72(2), 211-22","journal-title":"Applied Microbiology and Biotechnology"},{"key":"2728_CR96","doi-asserted-by":"publisher","first-page":"214","DOI":"10.1637\/10421-101512-Reg.1","volume":"57","author":"AJ Thachil","year":"2013","unstructured":"Thachil, A.J. et al., 2013. Vaccination of turkeys with Clostridium septicum bacterin-toxoid: evaluation of protection against clostridial dermatitis, Avian Diseases, 57, 214-219","journal-title":"Avian Diseases"},{"key":"2728_CR97","doi-asserted-by":"publisher","first-page":"3235","DOI":"10.1128\/iai.56.12.3235-3240.1988","volume":"56","author":"RK Tweten","year":"1988","unstructured":"Tweten, R.K., 1988. Nucleotide sequence of the gene for perfringolysin O (theta-toxin) from Clostridium perfringens: significant homology with the genes for streptolysin O and pneumolysin, Infection and Immunity, 56, 3235-3240","journal-title":"Infection and Immunity"},{"key":"2728_CR98","doi-asserted-by":"publisher","first-page":"233","DOI":"10.4049\/jimmunol.55.3.233","volume":"55","author":"AA Tytell","year":"1947","unstructured":"Tytell, A.A., and Logan, M.A., 1947. Immunization of humans and animals with gas gangrene toxoids, Journal of Immunology (Baltimore, Md.: 1950), 55, 233-244","journal-title":"Journal of Immunology (Baltimore, Md.: 1950)"},{"key":"2728_CR99","doi-asserted-by":"publisher","first-page":"24","DOI":"10.2174\/1875414701003020024","volume":"2","author":"F Uzal","year":"2010","unstructured":"Uzal, F. et al., 2010. Toxins involved in mammalian veterinary diseases, Open Toxinology Journal, 2, 24\u201342","journal-title":"Open Toxinology Journal"},{"key":"2728_CR100","doi-asserted-by":"publisher","first-page":"361","DOI":"10.2217\/fmb.13.168","volume":"9","author":"FA Uzal","year":"2014","unstructured":"Uzal, F.A. et al., 2014. Towards an understanding of the role of Clostridium perfringens toxins in human and animal disease, Future Microbiology, 9, 361-377","journal-title":"Future Microbiology"},{"key":"2728_CR101","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1186\/1297-9716-44-45","volume":"44","author":"S Verherstraeten","year":"2013","unstructured":"Verherstraeten, S. et al., 2013. The synergistic necrohemorrhagic action of Clostridium perfringens perfringolysin and alpha toxin in the bovine intestine and against bovine endothelial cells, Veterinary Research, 44, 45","journal-title":"Veterinary Research"},{"key":"2728_CR102","doi-asserted-by":"publisher","first-page":"2","DOI":"10.1186\/1297-9716-42-2","volume":"42","author":"EM Vilei","year":"2011","unstructured":"Vilei, E.M. et al., 2011. Genetic and functional characterization of the NanA sialidase from Clostridium chauvoei, Veterinary Research, 42, 2","journal-title":"Veterinary Research"},{"key":"2728_CR103","doi-asserted-by":"publisher","first-page":"e00019","DOI":"10.1128\/mBio.00019-13","volume":"4","author":"X-X Yan","year":"2013","unstructured":"Yan, X.-X. et al., 2013. Structural and functional analysis of the pore-forming toxin NetB from Clostridium perfringens, MBio, 4, e00019-00013","journal-title":"MBio"},{"key":"2728_CR104","doi-asserted-by":"publisher","first-page":"525","DOI":"10.3390\/toxins11090525","volume":"11","author":"NE Zaragoza","year":"2019","unstructured":"Zaragoza, N.E. et al., 2019. Vaccine Production to Protect Animals Against Pathogenic Clostridia, Toxins, 11, 525","journal-title":"Toxins"},{"key":"2728_CR105","doi-asserted-by":"publisher","first-page":"5459","DOI":"10.1016\/j.vaccine.2011.05.059","volume":"29","author":"J Zeng","year":"2011","unstructured":"Zeng, J. et al., 2011. Potential protective immunogenicity of recombinant Clostridium perfringens \u03b1\u2013\u03b22\u2013\u03b21 fusion toxin in mice, sows and cows, Vaccine, 29, 5459-5466","journal-title":"Vaccine"}],"container-title":["Tropical Animal Health and Production"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s11250-021-02728-w.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s11250-021-02728-w\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s11250-021-02728-w.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,4,9]],"date-time":"2025-04-09T08:52:46Z","timestamp":1744188766000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s11250-021-02728-w"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,4,23]]},"references-count":105,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2021,5]]}},"alternative-id":["2728"],"URL":"https:\/\/doi.org\/10.1007\/s11250-021-02728-w","relation":{},"ISSN":["0049-4747","1573-7438"],"issn-type":[{"value":"0049-4747","type":"print"},{"value":"1573-7438","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,4,23]]},"assertion":[{"value":"8 July 2020","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"12 April 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"23 April 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The manuscript does not contain clinical studies or patient data.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval"}},{"value":"All the authors approved the final manuscript.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent to participate"}},{"value":"All the authors consented the final manuscript.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare no competing interests.","order":5,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}}],"article-number":"284"}}