Skip to main content

Advertisement

SpringerLink
Log in

Epidemiology and Antimicrobial Resistance in Clostridium difficile With Special Reference to the Horse

  • Bacteriology (N Borel, Section Editor)
  • Published:
Current Clinical Microbiology Reports Aims and scope Submit manuscript

Abstract

Clostridium difficile is an important gastrointestinal pathogen in humans and animals. Disease occurs after intestinal colonization with toxigenic strains of C. difficile and subsequent proliferation due to disturbances of the microbiota. Several animal species can be affected, but mainly pigs and horses, and occasionally dogs, develop clinical disease. Pathogenesis appears to be similar in animals and humans. Initially, this disease was mainly considered to be a nosocomial infection after antimicrobial exposure; now, it often has a community onset without prior antimicrobial exposure. Therefore, reservoirs of C. difficile including animal feces, food, and the environment have recently been investigated. The bacterium has been isolated from the feces of healthy individuals from several species, including domestic and wild animals. Molecular types isolated from animals correlate with human ones, suggesting that animals could serve as an important reservoir. The use of antimicrobials appears associated with infection patterns and resistance profiles of C. difficile.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Hall IC, O’toole E. Intestinal flora in new-borin infants—with a description of a new pathogenic anaerobe, Bacillus difficilis. Am J Dis Child. 1935;49:390–402.

    Article  Google Scholar 

  2. George RH, Symonds JM, Dimock F, Brown JD, Arabi Y, Shinagawa N, et al. Identification of Clostridium difficile as a cause of pseudomembranous colitis. Brit Med J. 1978;1:695–5.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  3. Alvarez-Perez S, Blanco JL, Bouza E, Alba P, Gibert X, Maldonado J, et al. Prevalence of Clostridium difficile in diarrhoeic and non-diarrhoeic piglets. Vet Microbiol. 2009;137:302–5. Two-hundred samples from 40 zoo animal species were investigated and showed a C. difficile prevalence of 3.5 % among zoo animals, 57 % of which were ribotype 078, an important hypervirulent human strain. This suggests zoo animals as a potential source of C. difficile for humans. The high level of resistance to fluorquinolones and the unstable metronidazole-resistant strain detected were also of concern.

  4. Weese JS, Staempfli HR, Prescott JF. A prospective study of the roles of clostridium difficile and enterotoxigenic Clostridium perfringens in equine diarrhoea. Equine Vet J. 2001;33:403–9.

    Article  CAS  PubMed  Google Scholar 

  5. Bauer MP, Kuijper EJ. Potential sources of Clostridium difficile in human infection. Infect Dis Clin North Am. 2015;29:29–35.

    Article  PubMed  Google Scholar 

  6. Beaugerie L, Flahault A, Barbut F, Atlan P, Lalande V, Cousin P, et al. Antibiotic-associated diarrhoea and Clostridium difficile in the community. Alimen Pharmacol Ther. 2003;17:905–12.

    Article  CAS  Google Scholar 

  7. Bauer MP, Notermans DW, van Benthem BHB, Brazier JS, Wilcox MH, Rupnik M, et al. Clostridium difficile infection in Europe: a hospital-based survey. Lancet. 2011;377:63–73.

    Article  PubMed  Google Scholar 

  8. Arroyo LG, Kruth SA, Willey BM, Staempfli HR, Low DE, Weese JS. PCR ribotyping of Clostridium difficile isolates originating from human and animal sources. J Med Microbiol. 2005;54:163–6.

    Article  CAS  PubMed  Google Scholar 

  9. Costa MC, Stampfli HR, Arroyo LG, Pearl DL, Weese JS. Epidemiology of Clostridium difficile on a veal farm: prevalence, molecular characterization and tetracycline resistance. Vet Microbiol. 2011;152:379–84.

    Article  CAS  PubMed  Google Scholar 

  10. Koene MG, Mevius D, Wagenaar JA, Harmanus C, Hensgens MP, Meetsma AM, et al. Clostridium difficile in Dutch animals: their presence, characteristics and similarities with human isolates. Clin Microbiol Infect. 2011;18:778–84.

    Article  PubMed  Google Scholar 

  11. Rodriguez-Palacios A, Pickworth C, Loerch S, LeJeune JT. Transient fecal shedding and limited animal-to-animal transmission of Clostridium difficile by naturally infected finishing feedlot cattle. Appl Environ Microbiol. 2011;77:3391–7.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. Rupnik M. Is Clostridium difficile-associated infection a potentially zoonotic and foodborne disease? Clin Microbiol Infect. 2007;13:457–9.

    Article  CAS  PubMed  Google Scholar 

  13. Lyerly DM, Saum KE, MacDonald DK, Wilkins TD. Effects of Clostridium difficile toxins given intragastrically to animals. Infect Immun. 1985;47:349–52.

    PubMed Central  CAS  PubMed  Google Scholar 

  14. Songer JG. Bacterial phospholipases and their role in virulence. Trends Microbiol. 1997;5:156–61.

    Article  CAS  PubMed  Google Scholar 

  15. Borriello SP, Vale T, Brazier JS, Hyde S, Chippeck E. Evaluation of a commercial enzyme immunoassay kit for the detection of Clostridium difficile toxin A. Europ J Clin Microbiol Infect Dis. 1992;11:360–3.

    Article  CAS  PubMed  Google Scholar 

  16. Barbut F, Lalande V, Burghoffer B, Thien HV, Grimprel E, Petit JC. Prevalence and genetic characterization of toxin A variant strains of Clostridium difficile among adults and children with diarrhea in France. J Clin Microbiol. 2002;40:2079–83.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Magdesian KG, Dujowich M, Madigan JE, Hansen LM, Hirsh DC, Jang SS. Molecular characterization of Clostridium difficile isolates from horses in an intensive care unit and association of disease severity with strain type. J Am Vet Med Assoc. 2006;228:751–5.

    Article  PubMed  Google Scholar 

  18. Arroyo LG, Staempfli H, Weese JS. Molecular analysis of Clostridium difficile isolates recovered from horses with diarrhea. Vet Microbiol. 2007;120:179–83.

    Article  CAS  PubMed  Google Scholar 

  19. Ossiprandi MC, Buttrini M, Bottarelli E, Zerbini L. Preliminary molecular analysis of Clostridium difficile isolates from healthy horses in northern Italy. Comp Immunol Microbiol Infect Dis. 2010;33:25–9.

    Article  Google Scholar 

  20. Kato H, Kato N, Watanabe K, Iwai N, Nakamura H, Yamamoto T, et al. Identification of toxin A-negative, toxin B-positive Clostridium difficile by PCR. J Clin Microbiol. 1998;36:2178–82.

    PubMed Central  CAS  PubMed  Google Scholar 

  21. Brazier JS, Stubbs SL, Duerden BI. Prevalence of toxin A negative/B positive Clostridium difficile strains. J Hosp Infect. 1999;42:248–9.

    CAS  PubMed  Google Scholar 

  22. Alfa MJ, Kabani A, Lyerly D, Moncrief S, Neville LM, Al-Barrak A, et al. Characterization of a toxin A-negative, toxin B-positive strain of Clostridium difficile responsible for a nosocomial outbreak of Clostridium difficile-associated diarrhea. J Clin Microbiol. 2000;38:2706–14.

    PubMed Central  CAS  PubMed  Google Scholar 

  23. 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;41:1118–25.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  24. Shin BM, Kuak EY, Yoo SJ, Shin WC, Yoo HM. Emerging toxin A-B+ variant strain of Clostridium difficile responsible for pseudomembranous colitis at a tertiary care hospital in Korea. Diagnostic Microbiol Infect Dis. 2008;60:333–7.

    Article  CAS  Google Scholar 

  25. Popoff MR, Rubin EJ, Gill DM, Boquet P. Actin-specific ADP-ribosyltransferase produced by a Clostridium difficile strain. Infect Immun. 1988;56:2299–306.

    PubMed Central  CAS  PubMed  Google Scholar 

  26. Perelle S, Gibert M, Bourlioux P, Corthier G, Popoff MR. Production of a complete binary toxin (actin-specific ADP-ribosyltransferase) by Clostridium difficile CD196. Infect Immun. 1997;65:1402–7.

    PubMed Central  CAS  PubMed  Google Scholar 

  27. Rupnik M, Wilcox MH, Gerding DN. Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nature reviews Microbiol. 2009;7:526–36.

    Article  CAS  Google Scholar 

  28. Mulvey MR. Hypervirulent Clostridium difficile Strains in Hospitalized Patients, Canada. Emerg Infect Dis. 2010;16:678–81.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Weese JS, Staempfli HR, Prescott JF. Survival of Clostridium difficile and its toxins in equine feces: implications for diagnostic test selection and interpretation. J Vet Diagnostic Invest. 2000;12:332–6.

    Article  CAS  Google Scholar 

  30. Bengualid V, Umesh KC, Alapati J, Berger J. Clostridium difficile at a community hospital in the Bronx, New York: incidence prevalence and risk factors from 2006 to 2008. Am J Infect Control. 2011;39:183–7.

    Article  PubMed  Google Scholar 

  31. Eyre DW, Cule ML, Wilson DJ, Griffiths D, Vaughan A, O’Connor L, et al. Diverse sources of C. difficile infection identified on whole-genome sequencing. New England J Med. 2013;369:1195–205. This study showed that transmission of Clostridium difficile from patient to patient in a hospital only occurred in few cases. Sequencing technologies showed that most consecutive C. difficile infections were due to different strains from differing sources, suggesting that incoming patients and visitation animals could be an important source of C. difficile in hospitals.

  32. Keessen EC, Gaastra W, Lipman LJ. Clostridium difficile infection in humans and animals, differences and similarities. Vet Microbiol. 2011;153:205–17.

    Article  CAS  PubMed  Google Scholar 

  33. Hensgens MP, Keessen EC, Squire MM, Riley TV, Koene MG, de Boer E, et al. Clostridium difficile infection in the community: a zoonotic disease? Clin Microbiol Infect. 2012;18:635–45.

    Article  CAS  PubMed  Google Scholar 

  34. Janezic S, Zidaric V, Pardon B, Indra A, Kokotovic B, Blanco JL, et al. International Clostridium difficile animal strain collection and large diversity of animal associated strains. BMC Microbiol. 2014;14:173. Although PCR ribotype 078 is often reported as the major animal-associated C. difficile ribotype, the variability of strains in pigs and other animal hosts is substantial. Most common human PCR ribotypes (014, 020, and 002) are also among the most prevalent animal-associated C. difficile strains worldwide. The widespread dissemination of toxigenic C. difficile , as well as the considerable overlap in strain distribution between species, furthers concerns about interspecies, including zoonotic, transmission of this critically important pathogen.

  35. McDonald LC, Killgore GE, Thompson A, Owens Jr RC, Kazakova SV, Sambol SP, et al. An epidemic, toxin gene-variant strain of Clostridium difficile. New England J Med. 2005;353:2433–41.

    Article  CAS  Google Scholar 

  36. Goorhuis A, Bakker D, Corver J, Debast SB, Harmanus C, Notermans DW, et al. Emergence of Clostridium difficile infection due to a new hypervirulent strain, polymerase chain reaction ribotype 078. Clin Infect Dis. 2008;47:1162–70.

    Article  CAS  PubMed  Google Scholar 

  37. Walker AS, Eyre DW, Wyllie DH, Dingle KE, Griffiths D, Shine B, et al. Relationship between bacterial strain type, host biomarkers, and mortality in Clostridium difficile infection. Clin Infect Dis. 2013;56:1589–600.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. Rodriguez-Palacios A, Ilic S, LeJeune JT. Clostridium difficile with Moxifloxacin/Clindamycin resistance in vegetables in Ohio, USA, and prevalence meta-analysis. J Pathogens. 2014;2014:158601.

    Article  CAS  Google Scholar 

  39. Weese JS, Toxopeus L, Arroyo L. Clostridium difficile associated diarrhoea in horses within the community: predictors, clinical presentation and outcome. Equine Vet J. 2006;38:185–8.

    Article  CAS  PubMed  Google Scholar 

  40. Baverud V, Gustafsson A, Franklin A, Aspan A, Gunnarsson A. Clostridium difficile: prevalence in horses and environment, and antimicrobial susceptibility. Equine Vet J. 2003;35:465–71.

    Article  CAS  PubMed  Google Scholar 

  41. McNamara SE, Abdujamilova N, Somsel P, Gordoncillo MJ, DeDecker JM, Bartlett PC. Carriage of Clostridium difficile and other enteric pathogens among a 4-H avocational cohort. Zoonoses Public Health. 2011;58:192–9.

    Article  CAS  PubMed  Google Scholar 

  42. Medina-Torres CE, Weese JS, Staempfli HR. Prevalence of Clostridium difficile in horses. Vet Microbiol. 2011;152:212–5.

    Article  PubMed  Google Scholar 

  43. Schoster A, Arroyo LG, Staempfli HR, Shewen PE, Weese JS. Presence and molecular characterization of Clostridium difficile and Clostridium perfringens in intestinal compartments of healthy horses. BMC Vet Res. 2012;8:94.

    Article  PubMed Central  PubMed  Google Scholar 

  44. Schoster A, Staempfli HR, Arroyo LG, Reid-Smith RJ, Janecko N, Shewen PE, et al. Longitudinal study of Clostridium difficile and antimicrobial susceptibility of Escherichia coli in healthy horses in a community setting. Vet Microbiol. 2012;159:364–70.

    Article  CAS  PubMed  Google Scholar 

  45. Schoster A, Arroyo LG, Staempfli HR, Weese JS. Comparison of microbial populations in the small intestine, large intestine and feces of healthy horses using terminal restriction fragment length polymorphism. BMC Res Notes. 2013;6:91.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  46. Costa MC, Silva G, Ramos RV, Staempfli HR, Arroyo LG, Kim P, et al. Characterization and comparison of the bacterial microbiota in different gastrointestinal tract compartments in horses. Vet J. 2015;205:74–80.

    Article  CAS  PubMed  Google Scholar 

  47. Schoster A, Staempfli HR, Abrahams M, Jalali M, Weese JS, Guardabassi L. Effect of a Probiotic on Prevention of Diarrhea and Clostridium difficile and Clostridium perfringens shedding in foals. J Vet Intern Med. 2015;29:925–31.

    Article  CAS  PubMed  Google Scholar 

  48. Alvarez-Perez S, Blanco JL, Martinez-Nevado E, Pelaez T, Harmanus C, Kuijper E, et al. 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;169:218–22.

    Article  CAS  PubMed  Google Scholar 

  49. Rodriguez-Palacios A, Stampfli HR, Duffield T, Peregrine AS, Trotz-Williams LA, Arroyo LG, et al. Clostridium difficile PCR ribotypes in calves, Canada. Emerg Infect Dis. 2006;12:1730–6.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  50. Zidaric V, Pardon B, Dos Vultos T, Deprez P, Brouwer MS, Roberts AP, et al. 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;78:8515–22.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  51. 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;18:621–5. Horses admitted to veterinary hospitals appeared to be colonized irrespective of the reason for hospitalization. Antimicrobial resistance to more than one antimicrobial was common. One hundred percent were resistant to gentamicin and ceftiofur, antimicrobials commonly used in equine medicine. No metronidazole or vancomycin resistance was identified.

    Article  CAS  PubMed  Google Scholar 

  52. Post KW, Jost BH, Songer JG. Evaluation of a test for Clostridium difficile toxins A and B for the diagnosis of neonatal swine enteritis. J Vet Diagnostic Invest. 2002;14:258–9.

    Article  Google Scholar 

  53. Susick EK, Putnam M, Bermudez DM, Thakur S. Longitudinal study comparing the dynamics of Clostridium difficile in conventional and antimicrobial free pigs at farm and slaughter. Vet Microbiol. 2012;157:172–8.

    Article  CAS  PubMed  Google Scholar 

  54. 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;14:325–7.

    Article  CAS  PubMed  Google Scholar 

  55. Indra A, Lassnig H, Baliko N, Much P, Fiedler A, Huhulescu S, et al. Clostridium difficile: a new zoonotic agent? Wien Klin Wochenschr. 2009;121:91–5.

    Article  PubMed  Google Scholar 

  56. 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.

    Article  PubMed Central  PubMed  Google Scholar 

  57. Keel K, Brazier JS, Post KW, Weese S, Songer JG. Prevalence of PCR ribotypes among Clostridium difficile isolates from pigs, calves, and other species. J Clin Microbiol. 2007;45:1963–4.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  58. Knetsch CW, Connor TR, Mutreja A, van Dorp SM, Sanders IM, Browne HP, et al. Whole genome sequencing reveals potential spread of Clostridium difficile between humans and farm animals in the Netherlands, 2002 to 2011. Euro Surveillance. 2014;19:20954. Most recently, almost identical strains have been isolated from pig farmers and their respective pigs, further strengthening the suggestion that C. difficile can be transmitted from animals to humans; however, a common environmental source could not be ruled out entirely.

  59. Metcalf D, Avery BP, Janecko N, Matic N, Reid-Smith R, Weese JS. Clostridium difficile in seafood and fish. Anaerobe. 2011;17:85–6.

    Article  PubMed  Google Scholar 

  60. Metcalf DS, Costa MC, Dew WMV, Weese JS. Clostridium difficile in vegetables, Canada. Letters Appl Microbiol. 2010;51:600–2.

    Article  CAS  Google Scholar 

  61. Metcalf D, Reid-Smith RJ, Avery BP, Weese JS. Prevalence of Clostridium difficile in retail pork. Can Vet J. 2010;51:873–6.

    PubMed Central  PubMed  Google Scholar 

  62. Harvey RB, Norman KN, Andrews K, Norby B, Hume ME, Scanlan CM, et al. Clostridium difficile in retail meat and processing plants in Texas. J Vet Diagnostic Invest. 2011;23:807–11.

    Article  Google Scholar 

  63. Songer JG, Trinh HT, Killgore GE, Thompson AD, McDonald LC, Limbago BM. Clostridium difficile in retail meat products, USA, 2007. Emerg Infect Dis. 2009;15:819–21.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  64. 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;42:166–71.

    Article  CAS  PubMed  Google Scholar 

  65. Rahimi E, Jalali M, Weese JS. Prevalence of Clostridium difficile in raw beef, cow, sheep, goat, camel and buffalo meat in Iran. BMC Public Health. 2014;14:119.

    Article  PubMed Central  PubMed  Google Scholar 

  66. Weese JS, Finley R, Reid-Smith RR, Janecko N, Rousseau J. Evaluation of Clostridium difficile in dogs and the household environment. Epidemiol Infect. 2010;138:1100–4.

    Article  CAS  PubMed  Google Scholar 

  67. Weese JS, Staempfli HR, Prescott JF. Isolation of environmental Clostridium difficile from a veterinary teaching hospital. J Vet Diagnostic Invest. 2000;12:449–52.

    Article  CAS  Google Scholar 

  68. Lefebvre SL, Reid-Smith R, Boerlin P, Weese JS. Evaluation of the risks of shedding Salmonellae and other potential pathogens by therapy dogs fed raw diets in Ontario and Alberta. Zoonoses Public Health. 2008;55:470–80.

    Article  CAS  PubMed  Google Scholar 

  69. Weese JS, Rousseau J, Arroyo L. Bacteriological evaluation of commercial canine and feline raw diets. Can Vet J. 2005;46:513–6.

    PubMed Central  PubMed  Google Scholar 

  70. Borriello SP. Pathogenesis of Clostridium difficile infection. J Antimicrob Chemother. 1998;41(Suppl C):13–9.

    Article  CAS  PubMed  Google Scholar 

  71. Larson HE, Borriello SP. Quantitative study of antibiotic-induced susceptibility to Clostridium difficile enterocecitis in hamsters. Antimicrob Agents Chemother. 1990;34:1348–53.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  72. Leffler DA, Lamont JT. Clostridium difficile infection. New England J Med. 2015;372:1539–48.

    Article  CAS  Google Scholar 

  73. Jones RL, Adney WS, Shideler RK. Isolation of Clostridium difficile and detection of cytotoxin in the feces of diarrheic foals in the absence of antimicrobial treatment. J Clin Microbiol. 1987;25:1225–7.

    PubMed Central  CAS  PubMed  Google Scholar 

  74. Jones RL. Diagnostic procedures for isolation and characterization of Clostridium difficile associated with enterocolitis in foals. J Vet Diagnostic Invest. 1989;1:84–6.

    Article  CAS  Google Scholar 

  75. Baverud V, Franklin A, Gunnarsson A, Gustafsson A, Hellander-Edman A. Clostridium difficile associated with acute colitis in mares when their foals are treated with erythromycin and rifampicin for Rhodococcus equi pneumonia. Equine Vet J. 1998;30:482–8.

    Article  CAS  PubMed  Google Scholar 

  76. Uzal FA, Diab SS, Blanchard P, Moore J, Anthenill L, Shahriar F, et al. Clostridium perfringens type C and Clostridium difficile co-infection in foals. Vet Microbiol. 2012;156:395–402.

    Article  CAS  PubMed  Google Scholar 

  77. Jones RL, Adney WS, Alexander AF, Shideler RK, Traub-Dargatz JL. Hemorrhagic necrotizing enterocolitis associated with Clostridium difficile infection in four foals. J Am Vet Med Assoc. 1988;193:76–9.

    CAS  PubMed  Google Scholar 

  78. Madewell BR, Tang YJ, Jang S, Madigan JE, Hirsh DC, Gumerlock PH, et al. Apparent outbreaks of Clostridium difficile-associated diarrhea in horses in a veterinary medical teaching hospital. J Vet Diagnostic Invest. 1995;7:343–6.

    Article  CAS  Google Scholar 

  79. Chapman AM. Acute diarrhea in hospitalized horses. Vet Clin N Am Equine. 2009;25:363–80.

    Article  Google Scholar 

  80. Baverud V. Clostridium difficile infections in animals with special reference to the horse. a review. Vet Q. 2002;24:203–19.

    Article  CAS  PubMed  Google Scholar 

  81. Baverud V, Gustafsson A, Franklin A, Lindholm A, Gunnarsson A. Clostridium difficile associated with acute colitis in mature horses treated with antibiotics. Equine Vet J. 1997;29:279–84.

    Article  CAS  PubMed  Google Scholar 

  82. Gohari IM, Arroyo L, Macinnes JI, Timoney JF, Parreira VR, Prescott JF. Characterization of Clostridium perfringens in the feces of adult horses and foals with acute enterocolitis. Can J Vet Res. 2014;78:1–7.

    PubMed Central  PubMed  Google Scholar 

  83. Slovis, N.M., Elam, J., Estrada, M. and Leutenegger, C.M. (2013) Infectious agents associated with diarrhoea in neonatal foals in central Kentucky: A comprehensive molecular study. Equine Vet J.

  84. Frederick J, Giguere S, Sanchez LC. Infectious agents detected in the feces of diarrheic foals: a retrospective study of 233 cases (2003–2008). J Vet Intern Med. 2009;23:1254–60.

    Article  CAS  PubMed  Google Scholar 

  85. Arroyo LG, Weese JS, Staempfli HR. Experimental Clostridium difficile enterocolitis in foals. J Vet Intern Med. 2004;18:734–8.

    Article  PubMed  Google Scholar 

  86. Gustafsson A, Baverud V, Gunnarsson A, Pringle J, Franklin A. Study of faecal shedding of Clostridium difficile in horses treated with penicillin. Equine Vet J. 2004;36:180–2.

    Article  CAS  PubMed  Google Scholar 

  87. Diab SS, Rodriguez-Bertos A, Uzal FA. Pathology and diagnostic criteria of Clostridium difficile enteric infection in horses. Vet Pathol. 2013;50:1028–36.

    Article  CAS  PubMed  Google Scholar 

  88. Gustafsson A, Baverud V, Gunnarsson A, Rantzien MH, Lindholm A, Franklin A. The association of erythromycin ethylsuccinate with acute colitis in horses in Sweden. Equine Vet J. 1997;29:314–8.

    Article  CAS  PubMed  Google Scholar 

  89. Magdesian KG, Hirsh DC, Jang SS, Hansen LM, Madigan JE. Characterization of Clostridium difficile isolates from foals with diarrhea: 28 cases (1993–1997). J Am Vet Med Assoc. 2002;220:67–73.

    Article  CAS  PubMed  Google Scholar 

  90. Deneve C, Delomenie C, Barc MC, Collignon A, Janoir C. Antibiotics involved in Clostridium difficile-associated disease increase colonization factor gene expression. J Med Microbiol. 2008;57:732–8.

    Article  CAS  PubMed  Google Scholar 

  91. Baverud V. Clostridium difficile diarrhea: infection control in horses. Vet Clinics North Am Equine. 2004;20:615–30.

    Article  Google Scholar 

  92. Rodriguez C, Taminiau B, Brevers B, Avesani V, Van Broeck J, Leroux A, et al. Faecal microbiota characterisation of horses using 16 rdna barcoded pyrosequencing, and carriage rate of clostridium difficile at hospital admission. BMC Microbiol. 2015;15:181. This is the first study to evaluate the composition of the microbiota of horses in relation to C. difficile carriage. Only two horses were positive for C. difficile and displayed a decreased bacterial richness; however, none of the horses developed diarrhea.

  93. Elinav E, Planer D, Gatt ME. Prolonged ileus as a sole manifestation of pseudomembranous enterocolitis. Intern J Colorect Dis. 2004;19:273–6.

    Article  Google Scholar 

  94. Keel MK, Songer JG. The comparative pathology of Clostridium difficile-associated disease. Vet Pathol. 2006;43:225–40.

    Article  CAS  PubMed  Google Scholar 

  95. Diab SS, Songer G, Uzal FA. Clostridium difficile infection in horses: a review. Vet Microbiol. 2013;167:42–9.

    Article  CAS  PubMed  Google Scholar 

  96. Arroyo LG. Potential role of Clostridium difficile as a cause of duodenitis-proximal jejunitis in horses. J Med Microbiol. 2006;55:605–8.

    Article  PubMed  Google Scholar 

  97. Braun M, Herholz C, Straub R, Choisat B, Frey J, Nicolet J, et al. Detection of the ADP-ribosyltransferase toxin gene (cdtA) and its activity in Clostridium difficile isolates from Equidae. FEMS Microbiol Letters. 2000;184:29–33.

    Article  CAS  Google Scholar 

  98. Songer JG. The emergence of Clostridium difficile as a pathogen of food animals. Animal Health Res Rev. 2004;5:321–6.

    Article  Google Scholar 

  99. Kiss D, Bilkei G. A new periparturient disease in Eastern Europe, Clostridium difficile causes postparturient sow losses. Theriogenol. 2005;63:17–23.

    Article  CAS  Google Scholar 

  100. Rodriguez-Palacios A, Stampfli HR, Stalker M, Duffield T, Weese JS. Natural and experimental infection of neonatal calves with Clostridium difficile. Vet Microbiol. 2007;124:166–72.

    Article  PubMed  Google Scholar 

  101. Crook DW, Walker AS, Kean Y, Weiss K, Cornely OA, Miller MA, et al. Fidaxomicin versus vancomycin for Clostridium difficile infection: meta-analysis of pivotal randomized controlled trials. Clin Infect Dis. 2012;55 Suppl 2:S93–103.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  102. Staempfli HR, Prescott JF, Carman RJ, McCutcheon LJ. Use of bacitracin in the prevention and treatment of experimentally-induced idiopathic colitis in horses. Can J Vet Res. 1992;56:233–6.

    PubMed Central  CAS  PubMed  Google Scholar 

  103. Rodriguez C, Taminiau B, Brevers B, Avesani V, Van Broeck J, Leroux AA, et al. Carriage and acquisition rates of Clostridium difficile in hospitalized horses, including molecular characterization, multilocus sequence typing and antimicrobial susceptibility of bacterial isolates. Vet Microbiol. 2014;172:309–17.

    Article  CAS  PubMed  Google Scholar 

  104. Baverud V, Gunnarsson A, Karlsson M, Franklin A. Antimicrobial susceptibility of equine and environmental isolates of Clostridium difficile. Microb Drug Resist. 2004;10:57–63.

    Article  CAS  PubMed  Google Scholar 

  105. Silva RO, Ribeiro MG, Palhares MS, Borges AS, Maranhao RP, Silva MX, et al. Detection of A/B toxin and isolation of Clostridium difficile and Clostridium perfringens from foals. Equine Vet J. 2013;45:671–5.

    Article  CAS  PubMed  Google Scholar 

  106. Jang SS, Hansen LM, Breher JE, Riley DA, Magdesian KG, Madigan JE, et al. Antimicrobial susceptibilities of equine isolates of Clostridium difficile and molecular characterization of metronidazole-resistant strains. Clin Infect Dis. 1997;25 Suppl 2:S266–7.

    Article  CAS  PubMed  Google Scholar 

  107. Weese JS. Investigation of antimicrobial use and the impact of antimicrobial use guidelines in a small animal veterinary teaching hospital: 1995–2004. J Am Vet Med Assoc. 2006;228:553–8.

    Article  PubMed  Google Scholar 

  108. Delmee M, Avesani V. Correlation between serogroup and susceptibility to chloramphenicol, clindamycin, erythromycin, rifampicin and tetracycline among 308 isolates of Clostridium difficile. J Antimicrob Chemother. 1988;22:325–31.

    Article  CAS  PubMed  Google Scholar 

  109. Post KW, Songer JG. Antimicrobial susceptibility of Clostridium difficile isolated from neonatal pigs with enteritis. Anaerobe. 2004;10:47–50.

    Article  CAS  PubMed  Google Scholar 

  110. Pituch H, Obuch-Woszczatynski P, Wultanska D, Meisel-Mikolajczyk F, Luczak M. A survey of metronidazole and vancomycin resistance in strains of Clostridium difficile isolated in Warsaw, Poland. Anaerobe. 2005;11:197–9.

    Article  CAS  PubMed  Google Scholar 

  111. Pereira JB, Farragher TM, Tully MP, Jonathan Cooke J. Association between Clostridium difficile infection and antimicrobial usage in a large group of English hospitals. British J Clin Pharmacol. 2014;77:896–903.

    Article  Google Scholar 

  112. Floch MH, Walker WA, Sanders ME, Nieuwdorp M, Kim AS, Brenner DA, et al. Recommendations for Probiotic Use-2015 Update: Proceedings and Consensus Opinion. J Clin Gastroenterol. 2015;49 Suppl 1:S69–73.

    Article  PubMed  Google Scholar 

  113. Aas J, Gessert CE, Bakken JS. Recurrent Clostridium difficile colitis: case series involving 18 patients treated with donor stool administered via a nasogastric tube. Clin Infect Dis. 2003;36:580–5.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Vetsuisse Faculty, Equine Department, University of Zurich, Winterthurerstrasse 260, 8057, Zurich, Switzerland

    Angelika Schoster

  2. Ontario Veterinary College, Department of Clinical Studies, University of Guelph, Guelph, ON, N1G2W1, Canada

    Henry Staempfli

Authors
  1. Angelika Schoster
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Henry Staempfli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Angelika Schoster.

Ethics declarations

Conflict of Interest

The authors have no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Additional information

This article is part of the Topical Collection on Bacteriology

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schoster, A., Staempfli, H. Epidemiology and Antimicrobial Resistance in Clostridium difficile With Special Reference to the Horse. Curr Clin Micro Rpt 3, 32–41 (2016). https://doi.org/10.1007/s40588-016-0029-3

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40588-016-0029-3

Keywords

Search

Navigation