Clostridioides (Clostridium) Difficile in Food-Producing Animals, Horses and Household Pets: A Comprehensive Review
Abstract
:1. Introduction
2. The Evolutionary History of Clostridioides (Clostridium) difficile (C. difficile) Detection in Animals and the Natural Environment
3. The Microorganism and Pathogenesis of C. difficile Infection (CDI)
4. C. Difficile in Food-Producing Animals
4.1. C. Difficile in Food-Producing Animals: Swine
4.2. Food-Producing Animals: Cattle
4.3. Food-Producing Animals: Poultry
4.4. Food-Producing Animals: Sheep and Goats
5. C. difficile in Horses
6. C. Difficile in Household Pets: Dogs and Cats
7. Epidemiology—C. difficile Polymerase Chain Reaction (PCR) Ribotypes in Animals in Europe
8. Diagnosis
8.1. C. Difficile Isolation—Anaerobic Stool Culture
8.2. Characterization of C. Difficile Strains
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- Detection of PaLoc genes and CDT locus Genes by Polymerase Chain Reaction
- -
- Multilocus sequence typing (MLST)
- -
- PCR ribotyping
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- Toxinotyping
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- Whole-genome sequencing (WGS)
9. Control of C. Difficile—Prevention
10. Future Perspectives
Author Contributions
Funding
Conflicts of Interest
References
- Oren, A.; Rupnik, M. Clostridium difficile and Clostridioides difficile: Two validly published and correct names. Anaerobe 2018, 52, 125–126. [Google Scholar] [CrossRef]
- Knight, D.R.; Elliott, B.; Chang, B.J.; Perkins, T.T.; Riley, T.V. Diversity and Evolution in the Genome of Clostridium difficile. Clin. Microbiol. Rev. 2015, 28, 721–741. [Google Scholar] [CrossRef] [Green Version]
- Martin, J.S.; Monaghan, T.M.; Wilcox, M.H. Clostridium difficile infection: epidemiology, diagnosis and understanding transmission. Nat. Rev. Gastroenterol. Hepatol. 2016, 13, 206–216. [Google Scholar] [CrossRef] [Green Version]
- Lawson, P.A.; Citron, D.M.; Tyrrell, K.L.; Finegold, S.M. Reclassification of Clostridium difficile as Clostridioides difficile (Hall and O’Toole 1935) Prevot 1938. Anaerobe 2016, 40, 95–99. [Google Scholar] [CrossRef]
- Bartlett, J.G. Clostridium difficile: history of its role as an enteric pathogen and the current state of knowledge about the organism. Clin. Infect. Dis. 1994, 18 (Suppl. S4), S265–S272. [Google Scholar] [CrossRef]
- Borriello, S.P.; Wilcox, M.H. Clostridium difficile infections of the gut: the unanswered questions. J. Antimicrob. Chemother. 1998, 41 (Suppl. SC), 67–69. [Google Scholar] [CrossRef] [Green Version]
- Carter, G.P.; Rood, J.I.; Lyras, D. The role of toxin A and toxin B in Clostridium difficile-associated disease: Past and present perspectives. Gut Microbes 2010, 1, 58–64. [Google Scholar] [CrossRef] [Green Version]
- Voth, D.E.; Ballard, J.D. Clostridium difficile toxins: mechanism of action and role in disease. Clin. Microbiol. Rev. 2005, 18, 247–263. [Google Scholar] [CrossRef] [Green Version]
- Davies, A.H.; Roberts, A.K.; Shone, C.C.; Acharya, K.R. Super toxins from a super bug: structure and function of Clostridium difficile toxins. Biochem. J. 2011, 436, 517–526. [Google Scholar] [CrossRef] [Green Version]
- Modi, N.; Gulati, N.; Solomon, K.; Monaghan, T.; Robins, A.; Sewell, H.F.; Mahida, Y.R. Differential binding and internalization of Clostridium difficile toxin A by human peripheral blood monocytes, neutrophils and lymphocytes. Scand. J. Immunol. 2011, 74, 264–271. [Google Scholar] [CrossRef]
- Donaldson, M.T.; Palmer, J.E. Prevalence of Clostridium perfringens enterotoxin and Clostridium difficile toxin A in feces of horses with diarrhea and colic. J. Am. Vet. Med. Assoc. 1999, 215, 358–361. [Google Scholar]
- Hawken, P.; Weese, J.S.; Friendship, R.; Warriner, K. Longitudinal study of Clostridium difficile and Methicillin-resistant Staphylococcus aureus associated with pigs from weaning through to the end of processing. J. Food Prot. 2013, 76, 624–630. [Google Scholar] [CrossRef]
- Rodriguez, C.; Taminiau, B.; Van Broeck, J.; Avesani, V.; Delmee, M.; Daube, G. Clostridium difficile in young farm animals and slaughter animals in Belgium. Anaerobe 2012, 18, 621–625. [Google Scholar] [CrossRef]
- Songer, J.G.; Uzal, F.A. Clostridial enteric infections in pigs. J. Vet. Diagn. Invest. 2005, 17, 528–536. [Google Scholar] [CrossRef] [Green Version]
- Songer, J.G.; Anderson, M.A. Clostridium difficile: an important pathogen of food animals. Anaerobe 2006, 12, 1–4. [Google Scholar] [CrossRef]
- Rupnik, M.; Songer, J.G. Clostridium difficile: its potential as a source of foodborne disease. Adv. Food Nutr. Res. 2010, 60, 53–66. [Google Scholar]
- Rodriguez-Palacios, A.; Borgmann, S.; Kline, T.R.; LeJeune, J.T. Clostridium difficile in foods and animals: history and measures to reduce exposure. Anim. Health Res. Rev. 2013, 14, 11–29. [Google Scholar] [CrossRef] [Green Version]
- Kuijper, E.J.; Coignard, B.; Tull, P. Emergence of Clostridium difficile-associated disease in North America and Europe. Clin. Microbiol. Infect. 2006, 12 (Suppl. S6), 2–18. [Google Scholar] [CrossRef] [Green Version]
- Bauer, M.P.; Notermans, D.W.; van Benthem, B.H.; Brazier, J.S.; Wilcox, M.H.; Rupnik, M.; Monnet, D.L.; van Dissel, J.T.; Kuijper, E.J. Clostridium difficile infection in Europe: a hospital-based survey. Lancet 2011, 377, 63–73. [Google Scholar] [CrossRef]
- Yaeger, M.; Funk, N.; Hoffman, L. A survey of agents associated with neonatal diarrhea in Iowa swine including Clostridium difficile and porcine reproductive and respiratory syndrome virus. J. Vet. Diagn. Invest. 2002, 14, 281–287. [Google Scholar] [CrossRef] [Green Version]
- Keel, M.K.; Songer, J.G. The attachment, internalization, and time-dependent, intracellular distribution of Clostridium difficile toxin A in porcine intestinal explants. Vet. Pathol. 2011, 48, 369–380. [Google Scholar] [CrossRef]
- Keessen, E.C.; Hopman, N.E.; van Leengoed, L.A.; van Asten, A.J.; Hermanus, C.; Kuijper, E.J.; Lipman, L.J. Evaluation of four different diagnostic tests to detect Clostridium difficile in piglets. J. Clin. Microbiol. 2011, 49, 1816–1821. [Google Scholar] [CrossRef] [Green Version]
- Hammitt, M.C.; Bueschel, D.M.; Keel, M.K.; Glock, R.D.; Cuneo, P.; DeYoung, D.W.; Reggiardo, C.; Trinh, H.T.; Songer, J.G. A possible role for Clostridium difficile in the etiology of calf enteritis. Vet. Microbiol. 2008, 127, 343–352. [Google Scholar] [CrossRef]
- Goorhuis, A.; Bakker, D.; Corver, J.; Debast, S.B.; Harmanus, C.; Notermans, D.W.; Bergwerff, A.A.; Dekker, F.W.; Kuijper, E.J. Emergence of Clostridium difficile infection due to a new hypervirulent strain, polymerase chain reaction ribotype 078. Clin. Infect. Dis. 2008, 47, 1162–1170. [Google Scholar] [CrossRef] [Green Version]
- Debast, S.B.; van Leengoed, L.A.; Goorhuis, A.; Harmanus, C.; Kuijper, E.J.; Bergwerff, A.A. Clostridium difficile PCR ribotype 078 toxinotype V found in diarrhoeal pigs identical to isolates from affected humans. Environ. Microbiol. 2009, 11, 505–511. [Google Scholar] [CrossRef]
- Indra, A.; Lassnig, H.; Baliko, N.; Much, P.; Fiedler, A.; Huhulescu, S.; Allerberger, F. Clostridium difficile: A new zoonotic agent? Wien. Klin. Wochenschr. 2009, 121, 91–95. [Google Scholar] [CrossRef]
- Zidaric, V.; Zemljic, M.; Janezic, S.; Kocuvan, A.; Rupnik, M. High diversity of Clostridium difficile genotypes isolated from a single poultry farm producing replacement laying hens. Anaerobe 2008, 14, 325–327. [Google Scholar] [CrossRef]
- Knetsch, C.W.; Connor, T.R.; Mutreja, A.; van Dorp, S.M.; Sanders, I.M.; Browne, H.P.; Harris, D.; Lipman, L.; Keessen, E.C.; Corver, J.; et al. Whole genome sequencing reveals potential spread of Clostridium difficile between humans and farm animals in the Netherlands, 2002 to 2011. Euro. Surveill. 2014, 19, 20954. [Google Scholar] [CrossRef]
- Knetsch, C.W.; Kumar, N.; Forster, S.C.; Connor, T.R.; Browne, H.P.; Harmanus, C.; Sanders, I.M.; Harris, S.R.; Turner, L.; Morris, T.; et al. Zoonotic Transfer of Clostridium difficile Harboring Antimicrobial Resistance between Farm Animals and Humans. J. Clin. Microbiol. 2018, 56. [Google Scholar] [CrossRef] [Green Version]
- Krutova, M.; Zouharova, M.; Matejkova, J.; Tkadlec, J.; Krejci, J.; Faldyna, M.; Nyc, O.; Bernardy, J. The emergence of Clostridium difficile PCR ribotype 078 in piglets in the Czech Republic clusters with Clostridium difficile PCR ribotype 078 isolates from Germany, Japan and Taiwan. Int. J. Med. Microbiol. 2018, 308, 770–775. [Google Scholar] [CrossRef]
- Arroyo, L.G.; Kruth, S.A.; Willey, B.M.; Staempfli, H.R.; Low, D.E.; Weese, J.S. PCR ribotyping of Clostridium difficile isolates originating from human and animal sources. J. Med. Microbiol. 2005, 54, 163–166. [Google Scholar] [CrossRef]
- Wu, Y.C.; Lee, J.J.; Tsai, B.Y.; Liu, Y.F.; Chen, C.M.; Tien, N.; Tsai, P.J.; Chen, T.H. Potentially hypervirulent Clostridium difficile PCR ribotype 078 lineage isolates in pigs and possible implications for humans in Taiwan. Int. J. Med. Microbiol. 2016, 306, 115–122. [Google Scholar] [CrossRef]
- Norman, K.N.; Harvey, R.B.; Scott, H.M.; Hume, M.E.; Andrews, K.; Brawley, A.D. Varied prevalence of Clostridium difficile in an integrated swine operation. Anaerobe 2009, 15, 256–260. [Google Scholar] [CrossRef]
- Hopman, N.E.; Oorburg, D.; Sanders, I.; Kuijper, E.J.; Lipman, L.J. High occurrence of various Clostridium difficile PCR ribotypes in pigs arriving at the slaughterhouse. Vet. Q 2011, 31, 179–181. [Google Scholar] [CrossRef] [Green Version]
- Keessen, E.C.; Gaastra, W.; Lipman, L.J. Clostridium difficile infection in humans and animals, differences and similarities. Vet. Microbiol. 2011, 153, 205–217. [Google Scholar] [CrossRef]
- Al Saif, N.; Brazier, J.S. The distribution of Clostridium difficile in the environment of South Wales. J. Med. Microbiol. 1996, 45, 133–137. [Google Scholar] [CrossRef] [Green Version]
- McBee, R.H. Intestinal Flora of Some Antarctic Birds and Mammals. J. Bacteriol. 1960, 79, 311–312. [Google Scholar]
- Hafiz, S.; Oakley, C.L. Clostridium difficile: isolation and characteristics. J. Med. Microbiol. 1976, 9, 129–136. [Google Scholar] [CrossRef] [Green Version]
- Dabard, J.; Dubos, F.; Martinet, L.; Ducluzeau, R. Experimental reproduction of neonatal diarrhea in young gnotobiotic hares simultaneously associated with Clostridium difficile and other Clostridium strains. Infect. Immun. 1979, 24, 7–11. [Google Scholar]
- Jones, M.A.; Hunter, D. Isolation of Clostridium difficile from pigs. Vet. Rec. 1983, 112, 253. [Google Scholar] [CrossRef]
- Hunter, D.; Bellhouse, R.; Baker, K.B. Clostridium difficile isolated from a goat. Vet. Rec. 1981, 109, 291–292. [Google Scholar] [CrossRef]
- Princewell, T.J.; Agba, M.I. Examination of bovine faeces for the isolation and identification of Clostridium species. J. Appl. Bacteriol. 1982, 52, 97–102. [Google Scholar] [CrossRef]
- Ehrich, M.; Perry, B.D.; Troutt, H.F.; Dellers, R.W.; Magnusson, R.A. Acute diarrhea in horses of the Potomac River area: examination for clostridial toxins. J. Am. Vet. Med. Assoc. 1984, 185, 433–435. [Google Scholar]
- Jones, R.L.; Adney, W.S.; Alexander, A.F.; Shideler, R.K.; Traub-Dargatz, J.L. Hemorrhagic necrotizing enterocolitis associated with Clostridium difficile infection in four foals. J. Am. Vet. Med. Assoc. 1988, 193, 76–79. [Google Scholar]
- Magdesian, K.G.; Hirsh, D.C.; Jang, S.S.; Hansen, L.M.; Madigan, J.E. Characterization of Clostridium difficile isolates from foals with diarrhea: 28 cases (1993–1997). J. Am. Vet. Med. Assoc. 2002, 220, 67–73. [Google Scholar] [CrossRef]
- Weber, A.; Kroth, P.; Heil, G. Domestic animals as excreters of Clostridium difficile. Dtsch. Med. Wochenschr. 1988, 113, 1617–1618. [Google Scholar]
- Frazier, K.S.; Herron, A.J.; Hines, M.E., II; Gaskin, J.M.; Altman, N.H. Diagnosis of enteritis and enterotoxemia due to Clostridium difficile in captive ostriches (Struthio camelus). J. Vet. Diagn. Invest. 1993, 5, 623–625. [Google Scholar] [CrossRef] [Green Version]
- French, E.; Rodriguez-Palacios, A.; LeJeune, J.T. Enteric bacterial pathogens with zoonotic potential isolated from farm-raised deer. Foodborne Pathog. Dis. 2010, 7, 1031–1037. [Google Scholar] [CrossRef]
- Bandelj, P.; Trilar, T.; Racnik, J.; Zadravec, M.; Pirs, T.; Avbersek, J.; Micunovic, J.; Ocepek, M.; Vengust, M. Zero prevalence of Clostridium difficile in wild passerine birds in Europe. FEMS Microbiol. Lett. 2011, 321, 183–185. [Google Scholar] [CrossRef] [Green Version]
- Bandelj, P.; Trilar, T.; Blagus, R.; Ocepek, M.; Rousseau, J.; Weese, J.S.; Vengust, M. Prevalence and molecular characterization of Clostridium difficile isolated from European Barn Swallows (Hirundo rustica) during migration. BMC Vet. Res. 2014, 10, 40. [Google Scholar] [CrossRef] [Green Version]
- Alvarez-Perez, S.; Blanco, J.L.; Martinez-Nevado, E.; Pelaez, T.; Harmanus, C.; Kuijper, E.; Garcia, M.E. Shedding of Clostridium difficile PCR ribotype 078 by zoo animals, and report of an unstable metronidazole-resistant isolate from a zebra foal (Equus quagga burchellii). Vet. Microbiol. 2014, 169, 218–222. [Google Scholar] [CrossRef]
- Firth, C.; Bhat, M.; Firth, M.A.; Williams, S.H.; Frye, M.J.; Simmonds, P.; Conte, J.M.; Ng, J.; Garcia, J.; Bhuva, N.P.; et al. Detection of zoonotic pathogens and characterization of novel viruses carried by commensal Rattus norvegicus in New York City. MBio 2014, 5, e01914–e01933. [Google Scholar] [CrossRef] [Green Version]
- Thakur, S.; Sandfoss, M.; Kennedy-Stoskopf, S.; DePerno, C.S. Detection of Clostridium difficile and Salmonella in feral swine population in North Carolina. J. Wildl. Dis. 2011, 47, 774–776. [Google Scholar] [CrossRef] [Green Version]
- Bojesen, A.M.; Olsen, K.E.; Bertelsen, M.F. Fatal enterocolitis in Asian elephants (Elephas maximus) caused by Clostridium difficile. Vet. Microbiol. 2006, 116, 329–335. [Google Scholar] [CrossRef]
- Silva, R.O.; D’Elia, M.L.; de Magalhaes Soares, D.F.; Cavalcanti, A.R.; Leal, R.C.; Cavalcanti, G.; Pereira, P.L.; Lobato, F.C. Clostridium difficile-associated diarrhea in an ocelot (Leopardus pardalis). Anaerobe 2013, 20, 82–84. [Google Scholar] [CrossRef]
- Pasquale, V.; Romano, V.J.; Rupnik, M.; Dumontet, S.; Ciznar, I.; Aliberti, F.; Mauri, F.; Saggiomo, V.; Krovacek, K. Isolation and characterization of Clostridium difficile from shellfish and marine environments. Folia. Microbiol. 2011, 56, 431–437. [Google Scholar] [CrossRef]
- Baverud, V.; Gustafsson, A.; Franklin, A.; Aspan, A.; Gunnarsson, A. Clostridium difficile: prevalence in horses and environment, and antimicrobial susceptibility. Equine. Vet. J. 2003, 35, 465–471. [Google Scholar] [CrossRef]
- Weese, J.S.; Peregrine, A.S.; Armstrong, J. Occupational health and safety in small animal veterinary practice: Part II—Parasitic zoonotic diseases. Can. Vet. J. 2002, 43, 799–802. [Google Scholar]
- Rupnik, M.; Widmer, A.; Zimmermann, O.; Eckert, C.; Barbut, F. Clostridium difficile toxinotype V, ribotype 078, in animals and humans. J. Clin. Microbiol. 2008, 46, 2146. [Google Scholar] [CrossRef] [Green Version]
- Bauer, M.P.; Kuijper, E.J. Potential sources of Clostridium difficile in human infection. Infect. Dis Clin. North. Am. 2015, 29, 29–35. [Google Scholar] [CrossRef]
- Janezic, S.; Ocepek, M.; Zidaric, V.; Rupnik, M. Clostridium difficile genotypes other than ribotype 078 that are prevalent among human, animal and environmental isolates. BMC Microbiol. 2012, 12, 48. [Google Scholar] [CrossRef] [Green Version]
- Suzuki, S.; Ohnishi, M.; Kawanishi, M.; Akiba, M.; Kuroda, M. Investigation of a plasmid genome database for colistin-resistance gene mcr-1. Lancet Infect. Dis. 2016, 16, 284–285. [Google Scholar] [CrossRef] [Green Version]
- Zhu, D.; Sorg, J.A.; Sun, X. Clostridioides difficile Biology: Sporulation, Germination, and Corresponding Therapies for C. difficile Infection. Front. Cell Infect. Microbiol. 2018, 8, 29. [Google Scholar] [CrossRef] [Green Version]
- Meessen-Pinard, M.; Sekulovic, O.; Fortier, L.C. Evidence of in vivo prophage induction during Clostridium difficile infection. Appl. Environ. Microbiol. 2012, 78, 7662–7670. [Google Scholar] [CrossRef] [Green Version]
- Crobach, M.J.T.; Vernon, J.J.; Loo, V.G.; Kong, L.Y.; Pechine, S.; Wilcox, M.H.; Kuijper, E.J. Understanding Clostridium difficile Colonization. Clin. Microbiol. Rev. 2018, 31. [Google Scholar] [CrossRef] [Green Version]
- Claro, T.; Daniels, S.; Humphreys, H. Detecting Clostridium difficile spores from inanimate surfaces of the hospital environment: which method is best? J. Clin. Microbiol. 2014, 52, 3426–3428. [Google Scholar] [CrossRef] [Green Version]
- Sun, X.; Savidge, T.; Feng, H. The enterotoxicity of Clostridium difficile toxins. Toxins 2010, 2, 1848–1880. [Google Scholar] [CrossRef] [Green Version]
- Lyras, D.; O’Connor, J.R.; Howarth, P.M.; Sambol, S.P.; Carter, G.P.; Phumoonna, T.; Poon, R.; Adams, V.; Vedantam, G.; Johnson, S.; et al. Toxin B is essential for virulence of Clostridium difficile. Nature 2009, 458, 1176–1179. [Google Scholar] [CrossRef]
- Popoff, M.R.; Rubin, E.J.; Gill, D.M.; Boquet, P. Actin-specific ADP-ribosyltransferase produced by a Clostridium difficile strain. Infect. Immun. 1988, 56, 2299–2306. [Google Scholar]
- Barbut, F.; Decre, D.; Lalande, V.; Burghoffer, B.; Noussair, L.; Gigandon, A.; Espinasse, F.; Raskine, L.; Robert, J.; Mangeol, A.; et al. Clinical features of Clostridium difficile-associated diarrhoea due to binary toxin (actin-specific ADP-ribosyltransferase)-producing strains. J. Med. Microbiol. 2005, 54, 181–185. [Google Scholar] [CrossRef] [Green Version]
- Songer, J.G.; Jones, R.; Anderson, M.A.; Barbara, A.J.; Post, K.W.; Trinh, H.T. Prevention of porcine Clostridium difficile-associated disease by competitive exclusion with nontoxigenic organisms. Vet. Microbiol. 2007, 124, 358–361. [Google Scholar] [CrossRef]
- Songer, J.G. Clostridia as agents of zoonotic disease. Vet. Microbiol. 2010, 140, 399–404. [Google Scholar] [CrossRef]
- Tonna, I.; Welsby, P.D. Pathogenesis and treatment of Clostridium difficile infection. Postgrad. Med. J. 2005, 81, 367–369. [Google Scholar] [CrossRef]
- Poutanen, S.M.; Simor, A.E. Clostridium difficile-associated diarrhea in adults. CMAJ 2004, 171, 51–58. [Google Scholar] [CrossRef] [Green Version]
- Al-Barrak, A.; Embil, J.; Dyck, B.; Olekson, K.; Nicoll, D.; Alfa, M.; Kabani, A. An outbreak of toxin A negative, toxin B positive Clostridium difficile-associated diarrhea in a Canadian tertiary-care hospital. Can. Commun. Dis. Rep. 1999, 25, 65–69. [Google Scholar]
- Van den Berg, R.J.; Claas, E.C.; Oyib, D.H.; Klaassen, C.H.; Dijkshoorn, L.; Brazier, J.S.; Kuijper, E.J. Characterization of toxin A-negative, toxin B-positive Clostridium difficile isolates from outbreaks in different countries by amplified fragment length polymorphism and PCR ribotyping. J. Clin. Microbiol. 2004, 42, 1035–1041. [Google Scholar] [CrossRef] [Green Version]
- Squire, M.M.; Carter, G.P.; Mackin, K.E.; Chakravorty, A.; Noren, T.; Elliott, B.; Lyras, D.; Riley, T.V. Novel molecular type of Clostridium difficile in neonatal pigs, Western Australia. Emerg. Infect. Dis. 2013, 19, 790–792. [Google Scholar] [CrossRef]
- Moono, P.; Foster, N.F.; Hampson, D.J.; Knight, D.R.; Bloomfield, L.E.; Riley, T.V. Clostridium difficile Infection in Production Animals and Avian Species: A Review. Foodborne Pathog. Dis. 2016, 13, 647–655. [Google Scholar] [CrossRef] [Green Version]
- Arruda, P.H.; Madson, D.M.; Ramirez, A.; Rowe, E.; Lizer, J.T.; Songer, J.G. Effect of age, dose and antibiotic therapy on the development of Clostridium difficile infection in neonatal piglets. Anaerobe 2013, 22, 104–110. [Google Scholar] [CrossRef]
- Buffie, C.G.; Bucci, V.; Stein, R.R.; McKenney, P.T.; Ling, L.; Gobourne, A.; No, D.; Liu, H.; Kinnebrew, M.; Viale, A.; et al. Precision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile. Nature 2015, 517, 205–208. [Google Scholar] [CrossRef] [Green Version]
- Kim, E.K.; Sheetz, K.H.; Bonn, J.; DeRoo, S.; Lee, C.; Stein, I.; Zarinsefat, A.; Cai, S.; Campbell, D.A., Jr.; Englesbe, M.J. A statewide colectomy experience: The role of full bowel preparation in preventing surgical site infection. Ann. Surg. 2014, 259, 310–314. [Google Scholar] [CrossRef]
- Weese, J.S.; Wakeford, T.; Reid-Smith, R.; Rousseau, J.; Friendship, R. Longitudinal investigation of Clostridium difficile shedding in piglets. Anaerobe 2010, 16, 501–504. [Google Scholar] [CrossRef]
- Warriner, K.; Xu, C.; Habash, M.; Sultan, S.; Weese, S.J. Dissemination of Clostridium difficile in food and the environment: Significant sources of C. difficile community-acquired infection? J. Appl. Microbiol. 2017, 122, 542–553. [Google Scholar] [CrossRef]
- Songer, J.G.; Trinh, H.T.; Killgore, G.E.; Thompson, A.D.; McDonald, L.C.; Limbago, B.M. Clostridium difficile in retail meat products, USA, 2007. Emerg. Infect. Dis. 2009, 15, 819–821. [Google Scholar] [CrossRef]
- Thakur, S.; Putnam, M.; Fry, P.R.; Abley, M.; Gebreyes, W.A. Prevalence of antimicrobial resistance and association with toxin genes in Clostridium difficile in commercial swine. Am. J. Vet. Res. 2010, 71, 1189–1194. [Google Scholar] [CrossRef] [Green Version]
- Susick, E.K.; Putnam, M.; Bermudez, D.M.; Thakur, S. Longitudinal study comparing the dynamics of Clostridium difficile in conventional and antimicrobial free pigs at farm and slaughter. Vet. Microbiol. 2012, 157, 172–178. [Google Scholar] [CrossRef]
- Keessen, E.C.; Donswijk, C.J.; Hol, S.P.; Hermanus, C.; Kuijper, E.J.; Lipman, L.J. Aerial dissemination of Clostridium difficile on a pig farm and its environment. Environ. Res. 2011, 111, 1027–1032. [Google Scholar] [CrossRef]
- Burt, S.A.; Siemeling, L.; Kuijper, E.J.; Lipman, L.J. Vermin on pig farms are vectors for Clostridium difficile PCR ribotypes 078 and 045. Vet. Microbiol. 2012, 160, 256–258. [Google Scholar] [CrossRef]
- Van Dorp, S.M.; de Greeff, S.C.; Harmanus, C.; Sanders, I.; Dekkers, O.M.; Knetsch, C.W.; Kampinga, G.A.; Notermans, D.W.; Kuijper, E.J. Ribotype 078 Clostridium difficile infection incidence in Dutch hospitals is not associated with provincial pig farming: Results from a national sentinel surveillance, 2009–2015. PLoS ONE 2017, 12, e0189183. [Google Scholar] [CrossRef] [Green Version]
- Noren, T.; Johansson, K.; Unemo, M. Clostridium difficile PCR ribotype 046 is common among neonatal pigs and humans in Sweden. Clin. Microbiol. Infect. 2014, 20, O2–O6. [Google Scholar] [CrossRef] [Green Version]
- Avbersek, J.; Janezic, S.; Pate, M.; Rupnik, M.; Zidaric, V.; Logar, K.; Vengust, M.; Zemljic, M.; Pirs, T.; Ocepek, M. Diversity of Clostridium difficile in pigs and other animals in Slovenia. Anaerobe 2009, 15, 252–255. [Google Scholar] [CrossRef]
- Schneeberg, A.; Neubauer, H.; Schmoock, G.; Baier, S.; Harlizius, J.; Nienhoff, H.; Brase, K.; Zimmermann, S.; Seyboldt, C. Clostridium difficile genotypes in piglet populations in Germany. J. Clin. Microbiol. 2013, 51, 3796–3803. [Google Scholar] [CrossRef] [Green Version]
- Koene, M.G.; Mevius, D.; Wagenaar, J.A.; Harmanus, C.; Hensgens, M.P.; Meetsma, A.M.; Putirulan, F.F.; van Bergen, M.A.; Kuijper, E.J. Clostridium difficile in Dutch animals: their presence, characteristics and similarities with human isolates. Clin. Microbiol. Infect. 2012, 18, 778–784. [Google Scholar] [CrossRef] [Green Version]
- Rodriguez-Palacios, A.; Stampfli, H.R.; Duffield, T.; Peregrine, A.S.; Trotz-Williams, L.A.; Arroyo, L.G.; Brazier, J.S.; Weese, J.S. Clostridium difficile PCR ribotypes in calves, Canada. Emerg Infect. Dis. 2006, 12, 1730–1736. [Google Scholar] [CrossRef]
- Colloff, A.D.; Scholes, S.F. Idiopathic necrotising enteritis in a dairy calf. Vet. Rec. 2004, 155, 374. [Google Scholar]
- Costa, M.C.; Stampfli, H.R.; Arroyo, L.G.; Pearl, D.L.; Weese, J.S. Epidemiology of Clostridium difficile on a veal farm: prevalence, molecular characterization and tetracycline resistance. Vet. Microbiol. 2011, 152, 379–384. [Google Scholar] [CrossRef]
- Houser, B.A.; Soehnlen, M.K.; Wolfgang, D.R.; Lysczek, H.R.; Burns, C.M.; Jayarao, B.M. Prevalence of Clostridium difficile toxin genes in the feces of veal calves and incidence of ground veal contamination. Foodborne Pathog. Dis. 2012, 9, 32–36. [Google Scholar] [CrossRef]
- Magistrali, C.F.; Maresca, C.; Cucco, L.; Bano, L.; Drigo, I.; Filippini, G.; Dettori, A.; Broccatelli, S.; Pezzotti, G. Prevalence and risk factors associated with Clostridium difficile shedding in veal calves in Italy. Anaerobe 2015, 33, 42–47. [Google Scholar] [CrossRef]
- Zidaric, V.; Pardon, B.; Dos Vultos, T.; Deprez, P.; Brouwer, M.S.; Roberts, A.P.; Henriques, A.O.; Rupnik, M. Different antibiotic resistance and sporulation properties within multiclonal Clostridium difficile PCR ribotypes 078, 126, and 033 in a single calf farm. Appl. Environ. Microbiol. 2012, 78, 8515–8522. [Google Scholar] [CrossRef] [Green Version]
- Pirs, T.; Ocepek, M.; Rupnik, M. Isolation of Clostridium difficile from food animals in Slovenia. J. Med. Microbiol. 2008, 57, 790–792. [Google Scholar] [CrossRef]
- Romano, V.; Albanese, F.; Dumontet, S.; Krovacek, K.; Petrini, O.; Pasquale, V. Prevalence and genotypic characterization of Clostridium difficile from ruminants in Switzerland. Zoonoses Public Health 2012, 59, 545–548. [Google Scholar] [CrossRef]
- Schneeberg, A.; Neubauer, H.; Schmoock, G.; Grossmann, E.; Seyboldt, C. Presence of Clostridium difficile PCR ribotype clusters related to 033, 078 and 045 in diarrhoeic calves in Germany. J. Med. Microbiol. 2013, 62, 1190–1198. [Google Scholar] [CrossRef]
- Bandelj, P.; Harmanus, C.; Blagus, R.; Cotman, M.; Kuijper, E.J.; Ocepek, M.; Vengust, M. Quantification of Clostridioides (Clostridium) difficile in feces of calves of different age and determination of predominant Clostridioides difficile ribotype 033 relatedness and transmission between family dairy farms using multilocus variable-number tandem-repeat analysis. BMC Vet. Res. 2018, 14, 298. [Google Scholar]
- Uzal, F.A.; Senties-Cue, C.G.; Rimoldi, G.; Shivaprasad, H.L. Non-Clostridium perfringens infectious agents producing necrotic enteritis-like lesions in poultry. Avian Pathol. 2016, 45, 326–333. [Google Scholar] [CrossRef] [Green Version]
- Shivaprasad, H.L. Hepatitis associated with Clostridium difficile in an ostrich chick. Avian Pathol. 2003, 32, 57–62. [Google Scholar] [CrossRef] [Green Version]
- Simango, C. Prevalence of Clostridium difficile in the environment in a rural community in Zimbabwe. Trans. R Soc. Trop. Med. Hyg. 2006, 100, 1146–1150. [Google Scholar] [CrossRef]
- Simango, C.; Mwakurudza, S. Clostridium difficile in broiler chickens sold at market places in Zimbabwe and their antimicrobial susceptibility. Int. J. Food Microbiol. 2008, 124, 268–270. [Google Scholar] [CrossRef]
- Legaria, M.C.; Lumelsky, G.; Rosetti, S. Clostridium difficile-associated diarrhea from a general hospital in Argentina. Anaerobe 2003, 9, 113–116. [Google Scholar] [CrossRef]
- Rupnik, M.; Kato, N.; Grabnar, M.; Kato, H. New types of toxin A-negative, toxin B-positive strains among Clostridium difficile isolates from Asia. J. Clin. Microbiol. 2003, 41, 1118–1125. [Google Scholar] [CrossRef] [Green Version]
- Huang, H.; Wu, S.; Wang, M.; Zhang, Y.; Fang, H.; Palmgren, A.C.; Weintraub, A.; Nord, C.E. Clostridium difficile infections in a Shanghai hospital: antimicrobial resistance, toxin profiles and ribotypes. Int J. Antimicrob. Agents 2009, 33, 339–342. [Google Scholar] [CrossRef]
- Balassiano, I.T.; Yates, E.A.; Domingues, R.M.; Ferreira, E.O. Clostridium difficile: a problem of concern in developed countries and still a mystery in Latin America. J. Med. Microbiol. 2012, 61, 169–179. [Google Scholar] [CrossRef]
- Abdel-Glil, M.Y.; Thomas, P.; Schmoock, G.; Abou-El-Azm, K.; Wieler, L.H.; Neubauer, H.; Seyboldt, C. Presence of Clostridium difficile in poultry and poultry meat in Egypt. Anaerobe 2018, 51, 21–25. [Google Scholar] [CrossRef]
- De Boer, E.; Zwartkruis-Nahuis, A.; Heuvelink, A.E.; Harmanus, C.; Kuijper, E.J. Prevalence of Clostridium difficile in retailed meat in the Netherlands. Int. J. Food Microbiol. 2011, 144, 561–564. [Google Scholar] [CrossRef]
- Rodriguez, C.; Taminiau, B.; Avesani, V.; Van Broeck, J.; Delmee, M.; Daube, G. Multilocus sequence typing analysis and antibiotic resistance of Clostridium difficile strains isolated from retail meat and humans in Belgium. Food Microbiol. 2014, 42, 166–171. [Google Scholar] [CrossRef]
- Lund, B.M.; Peck, M.W. A possible route for foodborne transmission of Clostridium difficile? Foodborne Pathog. Dis. 2015, 12, 177–182. [Google Scholar] [CrossRef] [Green Version]
- Hussain, I.; Borah, P.; Sharma, R.K.; Rajkhowa, S.; Rupnik, M.; Saikia, D.P.; Hasin, D.; Deka, N.K.; Barkalita, L.M.; Nishikawa, Y.; et al. Molecular characteristics of Clostridium difficile isolates from human and animals in the North Eastern region of India. Mol. Cell. Probes 2016, 30, 306–311. [Google Scholar] [CrossRef]
- Diab, S.S.; Songer, G.; Uzal, F.A. Clostridium difficile infection in horses: a review. Vet. Microbiol. 2013, 167, 42–49. [Google Scholar] [CrossRef] [Green Version]
- Worsley, M.A. Infection control and prevention of Clostridium difficile infection. J. Antimicrob. Chemother. 1998, 41 (Suppl. SC), 59–66. [Google Scholar] [CrossRef] [Green Version]
- Baverud, V. Clostridium difficile diarrhea: infection control in horses. Vet. Clin. North. Am. Equine Pract 2004, 20, 615–630. [Google Scholar] [CrossRef]
- Magdesian, K.G.; Leutenegger, C.M. Real-time PCR and typing of Clostridium difficile isolates colonizing mare-foal pairs. Vet. J. 2011, 190, 119–123. [Google Scholar] [CrossRef]
- Keel, M.K.; Songer, J.G. The distribution and density of Clostridium difficile toxin receptors on the intestinal mucosa of neonatal pigs. Vet. Pathol. 2007, 44, 814–822. [Google Scholar] [CrossRef] [Green Version]
- Schoster, A.; Arroyo, L.G.; Staempfli, H.R.; Shewen, P.E.; Weese, J.S. Presence and molecular characterization of Clostridium difficile and Clostridium perfringens in intestinal compartments of healthy horses. BMC Vet. Res. 2012, 8, 94. [Google Scholar] [CrossRef] [Green Version]
- Esfandiari, Z.; Weese, S.; Ezzatpanah, H.; Jalali, M.; Chamani, M. Occurrence of Clostridium difficile in seasoned hamburgers and seven processing plants in Iran. BMC Microbiol. 2014, 14, 283. [Google Scholar] [CrossRef] [Green Version]
- Medina-Torres, C.E.; Weese, J.S.; Staempfli, H.R. Prevalence of Clostridium difficile in horses. Vet. Microbiol. 2011, 152, 212–215. [Google Scholar] [CrossRef]
- Kecerova, Z.; Cizek, A.; Nyc, O.; Krutova, M. Clostridium difficile isolates derived from Czech horses are resistant to enrofloxacin; cluster to clades 1 and 5 and ribotype 033 predominates. Anaerobe 2019, 56, 17–21. [Google Scholar] [CrossRef]
- Stone, N.E.; Sidak-Loftis, L.C.; Sahl, J.W.; Vazquez, A.J.; Wiggins, K.B.; Gillece, J.D.; Hicks, N.D.; Schupp, J.M.; Busch, J.D.; Keim, P.; et al. More than 50% of Clostridium difficile Isolates from Pet Dogs in Flagstaff, USA, Carry Toxigenic Genotypes. PLoS ONE 2016, 11, e0164504. [Google Scholar] [CrossRef] [Green Version]
- Lefebvre, S.L.; Arroyo, L.G.; Weese, J.S. Epidemic Clostridium difficile strain in hospital visitation dog. Emerg. Infect. Dis. 2006, 12, 1036–1037. [Google Scholar] [CrossRef]
- Stull, J.W.; Brophy, J.; Weese, J.S. Reducing the risk of pet-associated zoonotic infections. CMAJ 2015, 187, 736–743. [Google Scholar] [CrossRef] [Green Version]
- Marks, S.L.; Kather, E.J.; Kass, P.H.; Melli, A.C. Genotypic and phenotypic characterization of Clostridium perfringens and Clostridium difficile in diarrheic and healthy dogs. J. Vet. Intern. Med. 2002, 16, 533–540. [Google Scholar] [CrossRef]
- Clooten, J.; Kruth, S.; Arroyo, L.; Weese, J.S. Prevalence and risk factors for Clostridium difficile colonization in dogs and cats hospitalized in an intensive care unit. Vet. Microbiol. 2008, 129, 209–214. [Google Scholar] [CrossRef]
- Hensgens, M.P.; Keessen, E.C.; Squire, M.M.; Riley, T.V.; Koene, M.G.; de Boer, E.; Lipman, L.J.; Kuijper, E.J. Clostridium difficile infection in the community: A zoonotic disease? Clin. Microbiol. Infect. 2012, 18, 635–645. [Google Scholar] [CrossRef] [Green Version]
- Wetterwik, K.J.; Trowald-Wigh, G.; Fernstrom, L.L.; Krovacek, K. Clostridium difficile in faeces from healthy dogs and dogs with diarrhea. Acta Vet. Scand. 2013, 55, 23. [Google Scholar] [CrossRef] [Green Version]
- Cave, N.J.; Marks, S.L.; Kass, P.H.; Melli, A.C.; Brophy, M.A. Evaluation of a routine diagnostic fecal panel for dogs with diarrhea. J. Am. Vet. Med. Assoc. 2002, 221, 52–59. [Google Scholar] [CrossRef]
- Madewell, B.R.; Bea, J.K.; Kraegel, S.A.; Winthrop, M.; Tang, Y.J.; Silva, J., Jr. Clostridium difficile: A survey of fecal carriage in cats in a veterinary medical teaching hospital. J. Vet. Diagn. Invest. 1999, 11, 50–54. [Google Scholar] [CrossRef] [Green Version]
- Rodriguez, C.; Avesani, V.; Taminiau, B.; Van Broeck, J.; Brevers, B.; Delmee, M.; Daube, G. Investigation of Clostridium difficile interspecies relatedness using multilocus sequence typing, multilocus variable-number tandem-repeat analysis and antimicrobial susceptibility testing. Vet. J. 2015, 206, 349–355. [Google Scholar] [CrossRef] [Green Version]
- Rabold, D.; Espelage, W.; Abu Sin, M.; Eckmanns, T.; Schneeberg, A.; Neubauer, H.; Mobius, N.; Hille, K.; Wieler, L.H.; Seyboldt, C.; et al. The zoonotic potential of Clostridium difficile from small companion animals and their owners. PLoS ONE 2018, 13, e0193411. [Google Scholar] [CrossRef]
- Janezic, S.; Rupnik, M. Development and Implementation of Whole Genome Sequencing-Based Typing Schemes for Clostridioides difficile. Front. Public Health 2019, 7, 309. [Google Scholar] [CrossRef]
- Lemee, L.; Bourgeois, I.; Ruffin, E.; Collignon, A.; Lemeland, J.F.; Pons, J.L. Multilocus sequence analysis and comparative evolution of virulence-associated genes and housekeeping genes of Clostridium difficile. Microbiology 2005, 151, 3171–3180. [Google Scholar] [CrossRef] [Green Version]
- Janezic, S.; Zidaric, V.; Pardon, B.; Indra, A.; Kokotovic, B.; Blanco, J.L.; Seyboldt, C.; Diaz, C.R.; Poxton, I.R.; Perreten, V.; et al. International Clostridium difficile animal strain collection and large diversity of animal associated strains. BMC Microbiol. 2014, 14, 173. [Google Scholar] [CrossRef] [Green Version]
- Rupnik, M.; Wilcox, M.H.; Gerding, D.N. Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat. Rev. Microbiol. 2009, 7, 526–536. [Google Scholar] [CrossRef]
- Rene, P.; Frenette, C.P.; Schiller, I.; Dendukuri, N.; Brassard, P.; Fenn, S.; Loo, V.G. Comparison of eight commercial enzyme immunoassays for the detection of Clostridium difficile from stool samples and effect of strain type. Diagn. Microbiol. Infect. Dis. 2012, 73, 94–96. [Google Scholar] [CrossRef]
- Tenover, F.C.; Baron, E.J.; Peterson, L.R.; Persing, D.H. Laboratory diagnosis of Clostridium difficile infection can molecular amplification methods move us out of uncertainty? J. Mol. Diagn. 2011, 13, 573–582. [Google Scholar] [CrossRef]
- Jang, S.S.; Hansen, L.M.; Breher, J.E.; Riley, D.A.; Magdesian, K.G.; Madigan, J.E.; Tang, Y.J.; Silva, J., Jr.; Hirsh, D.C. Antimicrobial susceptibilities of equine isolates of Clostridium difficile and molecular characterization of metronidazole-resistant strains. Clin. Infect. Dis 1997, 25 (Suppl. S2), S266–S267. [Google Scholar] [CrossRef] [Green Version]
- George, W.L.; Sutter, V.L.; Citron, D.; Finegold, S.M. Selective and differential medium for isolation of Clostridium difficile. J. Clin. Microbiol. 1979, 9, 214–219. [Google Scholar]
- Wilson, K.H.; Kennedy, M.J.; Fekety, F.R. Use of sodium taurocholate to enhance spore recovery on a medium selective for Clostridium difficile. J. Clin. Microbiol. 1982, 15, 443–446. [Google Scholar]
- Peterson, L.R.; Kelly, P.J.; Nordbrock, H.A. Role of culture and toxin detection in laboratory testing for diagnosis of Clostridium difficile-associated diarrhea. Eur J. Clin. Microbiol. Infect. Dis 1996, 15, 330–336. [Google Scholar] [CrossRef]
- Delmee, M. Laboratory diagnosis of Clostridium difficile disease. Clin. Microbiol. Infect. 2001, 7, 411–416. [Google Scholar] [CrossRef] [Green Version]
- Griffiths, D.; Fawley, W.; Kachrimanidou, M.; Bowden, R.; Crook, D.W.; Fung, R.; Golubchik, T.; Harding, R.M.; Jeffery, K.J.; Jolley, K.A.; et al. Multilocus sequence typing of Clostridium difficile. J. Clin. Microbiol. 2010, 48, 770–778. [Google Scholar] [CrossRef] [Green Version]
- Bidet, P.; Barbut, F.; Lalande, V.; Burghoffer, B.; Petit, J.C. Development of a new PCR-ribotyping method for Clostridium difficile based on ribosomal RNA gene sequencing. FEMS Microbiol. Lett. 1999, 175, 261–266. [Google Scholar] [CrossRef]
- Stubbs, S.L.; Brazier, J.S.; O’Neill, G.L.; Duerden, B.I. PCR targeted to the 16S-23S rRNA gene intergenic spacer region of Clostridium difficile and construction of a library consisting of 116 different PCR ribotypes. J. Clin. Microbiol. 1999, 37, 461–463. [Google Scholar]
- Rupnik, M.; Avesani, V.; Janc, M.; von Eichel-Streiber, C.; Delmee, M. A novel toxinotyping scheme and correlation of toxinotypes with serogroups of Clostridium difficile isolates. J. Clin. Microbiol. 1998, 36, 2240–2247. [Google Scholar]
- Centers for Disease Control and Prevention. Available online: https://www.cdc.gov/pulsenet/ (accessed on 12 September 2019).
- Fenner, L.; Widmer, A.F.; Goy, G.; Rudin, S.; Frei, R. Rapid and reliable diagnostic algorithm for detection of Clostridium difficile. J. Clin. Microbiol. 2008, 46, 328–330. [Google Scholar] [CrossRef] [Green Version]
- Kramer, A.; Schwebke, I.; Kampf, G. How long do nosocomial pathogens persist on inanimate surfaces? A systematic review. BMC Infect. Dis. 2006, 6, 130. [Google Scholar] [CrossRef] [Green Version]
- Merrigan, M.; Venugopal, A.; Mallozzi, M.; Roxas, B.; Viswanathan, V.K.; Johnson, S.; Gerding, D.N.; Vedantam, G. Human hypervirulent Clostridium difficile strains exhibit increased sporulation as well as robust toxin production. J. Bacteriol. 2010, 192, 4904–4911. [Google Scholar] [CrossRef] [Green Version]
- Robinson, C.D.; Auchtung, J.M.; Collins, J.; Britton, R.A. Epidemic Clostridium difficile strains demonstrate increased competitive fitness compared to nonepidemic isolates. Infect. Immun. 2014, 82, 2815–2825. [Google Scholar] [CrossRef] [Green Version]
- Kink, J.A.; Williams, J.A. Antibodies to recombinant Clostridium difficile toxins A and B are an effective treatment and prevent relapse of C. difficile-associated disease in a hamster model of infection. Infect. Immun. 1998, 66, 2018–2025. [Google Scholar]
- Arruda, P.H.; Madson, D.M.; Ramirez, A.; Rowe, E.W.; Songer, J.G. Bacterial probiotics as an aid in the control of Clostridium difficile disease in neonatal pigs. Can. Vet. J. 2016, 57, 183–188. [Google Scholar]
- Schoster, A.; Staempfli, H.R.; Abrahams, M.; Jalali, M.; Weese, J.S.; Guardabassi, L. Effect of a probiotic on prevention of diarrhea and Clostridium difficile and Clostridium perfringens shedding in foals. J. Vet. Intern. Med. 2015, 29, 925–931. [Google Scholar] [CrossRef] [Green Version]
- Toothaker, R.D.; Elmer, G.W. Prevention of clindamycin-induced mortality in hamsters by Saccharomyces boulardii. Antimicrob. Agents Chemother. 1984, 26, 552–556. [Google Scholar] [CrossRef] [Green Version]
- Staempfli, H.R.; Prescott, J.F.; Carman, R.J.; McCutcheon, L.J. Use of bacitracin in the prevention and treatment of experimentally-induced idiopathic colitis in horses. Can. J. Vet. Res. 1992, 56, 233–236. [Google Scholar]
- Allo, M.; Silva, J., Jr.; Fekety, R.; Rifkin, G.D.; Waskin, H. Prevention of clindamycin-induced colitis in hamsters by Clostridium sordellii antitoxin. Gastroenterology 1979, 76, 351–355. [Google Scholar] [CrossRef]
- Ghose, C.; Kelly, C.P. The prospect for vaccines to prevent Clostridium difficile infection. Infect. Dis. Clin. North. Am. 2015, 29, 145–162. [Google Scholar] [CrossRef]
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Kachrimanidou, M.; Tzika, E.; Filioussis, G. Clostridioides (Clostridium) Difficile in Food-Producing Animals, Horses and Household Pets: A Comprehensive Review. Microorganisms 2019, 7, 667. https://doi.org/10.3390/microorganisms7120667
Kachrimanidou M, Tzika E, Filioussis G. Clostridioides (Clostridium) Difficile in Food-Producing Animals, Horses and Household Pets: A Comprehensive Review. Microorganisms. 2019; 7(12):667. https://doi.org/10.3390/microorganisms7120667
Chicago/Turabian StyleKachrimanidou, Melina, Eleni Tzika, and George Filioussis. 2019. "Clostridioides (Clostridium) Difficile in Food-Producing Animals, Horses and Household Pets: A Comprehensive Review" Microorganisms 7, no. 12: 667. https://doi.org/10.3390/microorganisms7120667