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Home / Equine Research Bank / Microorganisms / Genomic Analysis of Clostridioides difficile Recovered from ...
Microorganisms2023; 11(7); doi: 10.3390/microorganisms11071743

Genomic Analysis of Clostridioides difficile Recovered from Horses in Western Australia.

Abstract: Clostridioides difficile poses an ongoing threat as a cause of gastrointestinal disease in humans and animals. Traditionally considered a human healthcare-related disease, increases in community-associated C. difficile infection (CDI) and growing evidence of inter-species transmission suggest a wider perspective is required for CDI control. In horses, C. difficile is a major cause of diarrhoea and life-threatening colitis. This study aimed to better understand the epidemiology of CDI in Australian horses and provide insights into the relationships between horse, human and environmental strains. A total of 752 faecal samples from 387 Western Australian horses were collected. C. difficile was isolated from 104 (30.9%) horses without gastrointestinal signs and 19 (37.8%) with gastrointestinal signs. Of these, 68 (55.3%) harboured one or more toxigenic strains, including C. difficile PCR ribotypes (RTs) 012 (n = 14), 014/020 (n = 10) and 087 (n = 7), all prominent in human infection. Whole-genome analysis of 45 strains identified a phylogenetic cluster of 10 closely related C. difficile RT 012 strains of equine, human and environmental origin (0-62 SNP differences; average 23), indicating recent shared ancestry. Evidence of possible clonal inter-species transmission or common-source exposure was identified for a subgroup of three horse and one human isolates, highlighting the need for a One Health approach to C. difficile surveillance.
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Publication Date: 2023-07-03 PubMed ID: 37512915PubMed Central: PMC10386058DOI: 10.3390/microorganisms11071743Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research article studies the impact of Clostridioides difficile infection (CDI) in horses in West Australia and links this to human and environmental strains of the disease. It uncovers potential trans-species transmission of the disease and highlights the need for a holistic, One Health approach in CDI surveillance.

Overview of the Study

  • The research was conducted to gain insight into the epidemiology of CDI in Australian horses and the relationship between horse, human, and environmental strains of the disease.
  • Clostridioides difficile is a bacterium that can cause gastrointestinal diseases in humans and animals. In horses, it’s a significant cause of diarrhoea and severe colitis.
  • Traditionally, CDI has been considered a health issue associated primarily with humans, but a rise in community-associated infections and evidence of cross-species transmission suggest a broader perspective is needed.

Methodology and Findings

  • The researchers collected 752 faecal samples from 387 horses in Western Australia for the study. They found CDI in 30.9% of horses without gastrointestinal issues and 37.8% with such issues.
  • Out of the infected horses, 55.3% harbored one or more toxigenic strains of CDI. Some of these strains, including Clostridioides difficile PCR ribotypes (RTs) 012, 014/020, and 087, are also prevalent in human infections.
  • Whole-genome analysis was performed on 45 strains, and close relations were found between 10 of these CDI RT 012 strains, from horses, humans, and environmental sources, indicating a shared recent ancestry.

Conclusion and Recommendations

  • The study found evidence of possible clonal inter-species transmission or common-source exposure in a subgroup of three horse and one human isolates. This highlights the potential for CDI transmission between different species and from common environmental sources.
  • The study thus underscores the need for a comprehensive “One Health” approach to CDI surveillance that considers human, animal, and environmental health collectively. Such a perspective could help improve control measures for CDI and enhance our understanding of its transmission mechanisms.

Cite This Article

APA
Hain-Saunders NMR, Knight DR, Bruce M, Byrne D, Riley TV. (2023). Genomic Analysis of Clostridioides difficile Recovered from Horses in Western Australia. Microorganisms, 11(7). https://doi.org/10.3390/microorganisms11071743

Publication

Microorganisms
ISSN: 2076-2607
NlmUniqueID: 101625893
Country: Switzerland
Language: English
Volume: 11
Issue: 7

Researcher Affiliations

Hain-Saunders, Natasza M R
  • Centre for Biosecurity, and One Health, Harry Butler Institute, Murdoch University, Murdoch, WA 6150, Australia.
Knight, Daniel R
  • School of Biomedical Sciences, The University of Western Australia, Queen Elizabeth II Medical Centre, Nedlands, WA 6009, Australia.
  • PathWest Laboratory Medicine, Department of Microbiology, Queen Elizabeth II Medical Centre, Nedlands, WA 6009, Australia.
Bruce, Mieghan
  • Centre for Biosecurity, and One Health, Harry Butler Institute, Murdoch University, Murdoch, WA 6150, Australia.
  • School of Veterinary Medicine, Murdoch University, Murdoch, WA 6150, Australia.
Byrne, David
  • School of Veterinary Medicine, Murdoch University, Murdoch, WA 6150, Australia.
Riley, Thomas V
  • Centre for Biosecurity, and One Health, Harry Butler Institute, Murdoch University, Murdoch, WA 6150, Australia.
  • School of Biomedical Sciences, The University of Western Australia, Queen Elizabeth II Medical Centre, Nedlands, WA 6009, Australia.
  • PathWest Laboratory Medicine, Department of Microbiology, Queen Elizabeth II Medical Centre, Nedlands, WA 6009, Australia.
  • School of Medical and Health Sciences, Edith Cowan University, Joondalup, WA 6027, Australia.

Grant Funding

  • APP1138257 / National Health and Medical Research Council
  • Research and Innovation Strategic Scholarship / Murdoch University

Conflict of Interest Statement

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

References

This article includes 64 references
  1. Ofori E, Ramai D, Dhawan M, Mustafa F, Gasperino J, Reddy M. Community-acquired Clostridium difficile: Epidemiology, ribotype, risk factors, hospital and intensive care unit outcomes, and current and emerging therapies.. J. Hosp. Infect. 2018;99:436–442.
    doi: 10.1016/j.jhin.2018.01.015pubmed: 29410012google scholar: lookup
  2. Feuerstadt P, Theriault N, Tillotson G. The burden of CDI in the United States: A multifactorial challenge.. BMC Infect. Dis. 2023;23:132.
    doi: 10.1186/s12879-023-08096-0pmc: PMC9990004pubmed: 36882700google scholar: lookup
  3. . Antibiotic Resistance Threats in the United States.. .
  4. Keel M.K, Songer J.G. The comparative pathology of Clostridium difficile-associated disease.. Vet. Path. 2006;43:225–240.
    doi: 10.1354/vp.43-3-225pubmed: 16672570google scholar: lookup
  5. Shen A. Clostridium difficile toxins: Mediators of inflammation.. J. Innate Immun. 2012;4:149–158.
    doi: 10.1159/000332946pmc: PMC3388264pubmed: 22237401google scholar: lookup
  6. Lyerly D.M, Lockwood D.E, Richardson S.H, Wilkins T.D. Biological activities of toxins A and B of Clostridium difficile.. Infect. Immun. 1982;35:1147–1150.
    doi: 10.1128/iai.35.3.1147-1150.1982pmc: PMC351167pubmed: 7068215google scholar: lookup
  7. Kuehne S.A, Cartman S.T, Heap J.T, Kelly M.L, Cockayne A, Minton N.P. The role of toxin A and toxin B in Clostridium difficile infection.. Nature 2010;467:711–713.
    doi: 10.1038/nature09397pubmed: 20844489google scholar: lookup
  8. Buddle J.E, Fagan R.P. Pathogenicity and virulence of Clostridioides difficile.. Virulence 2023;14:2150452.
    doi: 10.1080/21505594.2022.2150452pmc: PMC9815241pubmed: 36419222google scholar: lookup
  9. Weese J.S. Clostridium (Clostridioides) difficile in animals.. J. Vet. Diagn. Investig. Off. Publ. Am. Assoc. Vet. Lab. Diagn. Inc. 2020;32:213–221.
    doi: 10.1177/1040638719899081pmc: PMC7081495pubmed: 31904312google scholar: lookup
  10. Knight D.R, Riley T.V. Genomic delineation of zoonotic origins of Clostridium difficile.. Front. Public Health 2019;7:164.
    doi: 10.3389/fpubh.2019.00164pmc: PMC6595230pubmed: 31281807google scholar: lookup
  11. Knetsch C.W, Connor T, Mutreja A, van Dorp S.M, Sanders I, Browne H, Harris D, Lipman L, Keessen E.C, Corver J. Whole genome sequencing reveals potential spread of Clostridium difficile between humans and farm animals in the Netherlands, 2002 to 2011.. Eurosurveillance 2014;19:30–41.
    doi: 10.2807/1560-7917.ES2014.19.45.20954pmc: PMC4518193pubmed: 25411691google scholar: lookup
  12. Loo V.G, Brassard P, Miller M.A. Household transmission of Clostridium difficile to family members and domestic pets.. Infect. Control. Hosp. Epidemiol. 2016;37:1342.
    doi: 10.1017/ice.2016.178pubmed: 27767004google scholar: lookup
  13. Redding L.E, Habing G.G, Tu V, Bittinger K.L, O’Day J, Pancholi P, Wang S.-H, Alexander A, Kelly B.J, Weese J.S. Infrequent intrahousehold transmission of Clostridioides difficile between pet owners and their pets.. Zoonoses Public Health 2023;70:341–351.
    doi: 10.1111/zph.13032pmc: PMC10175142pubmed: 36779297google scholar: lookup
  14. Diab S.S, Rodriguez-Bertos A, Uzal F.A. Pathology and diagnostic criteria of Clostridium difficile enteric infection in horses.. Vet. Pathol. 2013;50:1028–1036.
    doi: 10.1177/0300985813489039pubmed: 23686768google scholar: lookup
  15. Båverud V, Gustafsson A, Franklin A, Aspán A, Gunnarsson A. Clostridium difficile: Prevalence in horses and environment, and antimicrobial susceptibility.. Equine Vet. J. 2003;35:465–471.
    doi: 10.2746/042516403775600505pubmed: 12875324google scholar: lookup
  16. Thean S, Elliott B, Riley T.V. Clostridium difficile in horses in Australia—A preliminary study.. J. Med. Microbiol. 2011;60:1188–1192.
    doi: 10.1099/jmm.0.030908-0pubmed: 21436371google scholar: lookup
  17. Weese J.S, Staempfli H.R, Prescott J.F. A prospective study of the roles of Clostridium difficile and enterotoxigenic Clostridium perfringens in equine diarrhoea.. Equine Vet. J. 2001;33:403–409.
    doi: 10.2746/042516401776249534pubmed: 11469775google scholar: lookup
  18. Shaughnessy M, Snider T, Sepulveda R, Boxrud D, Cebelinski E, Jawahir S, Holzbauer S, Johnston B, Smith K, Bender J. Prevalence and molecular characteristics of Clostridium difficile in retail meats, food-producing and companion animals, and humans in Minnesota.. J. Food Prot. 2018;81:1635–1642.
    doi: 10.4315/0362-028X.JFP-18-104pubmed: 30198756google scholar: lookup
  19. Schoster A, Staempfli H.R. Epidemiology and antimicrobial resistance in Clostridium difficile with special reference to the horse.. Curr. Clin. Microbiol. Rep. 2016;3:32–41.
    doi: 10.1007/s40588-016-0029-3google scholar: lookup
  20. . Racing Australia Annual Report 2020.. .
  21. . Horse Meat Production.. .
  22. Lim S.C, Knight D.R, Moono P, Foster N.F, Riley T.V. Clostridium difficile in soil conditioners, mulches and garden mixes with evidence of a clonal relationship with historical food and clinical isolates.. Environ. Microbiol. Rep. 2020;12:672–680.
    doi: 10.1111/1758-2229.12889pubmed: 32975368google scholar: lookup
  23. Brazier J.S. Role of the laboratory in investigations of Clostridium difficile diarrhea.. Clin. Infect. Dis. 1993;16:228–233.
    doi: 10.1093/clinids/16.Supplement_4.S228pubmed: 8324124google scholar: lookup
  24. Lim S.C, Foster N.F, Elliott B, Riley T.V. High prevalence of Clostridium difficile on retail root vegetables, Western Australia.. J. Appl. Microbiol. 2018;124:585–590.
    doi: 10.1111/jam.13653pubmed: 29193458google scholar: lookup
  25. . Methods for Antimicrobial Susceptibility Testing of Anaerobic Bacteria, Seventh Edition.. .
  26. . Breakpoint Tables for Interpretation of MICs and Zone Diameters, Version 13.0.. 2023.
  27. . Assessment Report, Dificlir Fidaxomicin.. .
  28. O’Connor J.R, Galang M.A, Sambol S.P, Hecht D.W, Vedantam G, Gerding D.N, Johnson S. Rifampin and rifaximin resistance in clinical isolates of Clostridium difficile.. Antimicrob. Agents Chemother. 2008;52:2813–2817.
    doi: 10.1128/AAC.00342-08pmc: PMC2493101pubmed: 18559647google scholar: lookup
  29. . Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Third Informational Supplement.. 2013.
  30. Griffiths D, Fawley W, Kachrimanidou M, Bowden R, Crook D.W, Fung R, Golubchik T, Harding R.M, Jeffery K.J, Jolley K.A. Multilocus sequence typing of Clostridium difficile.. J. Clin. Microbiol. 2010;48:770–778.
    doi: 10.1128/JCM.01796-09pmc: PMC2832416pubmed: 20042623google scholar: lookup
  31. Altschul S.F, Gish W, Miller W, Myers E.W, Lipman D.J. Basic local alignment search tool.. J. Mol. Biol. 1990;215:403–410.
    doi: 10.1016/S0022-2836(05)80360-2pubmed: 2231712google scholar: lookup
  32. Harris S.R. SKA: Split Kmer analysis toolkit for bacterial genomic epidemiology.. bioRxiv 2018:453142.
    doi: 10.1101/453142google scholar: lookup
  33. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: An online tool for phylogenetic tree display and annotation.. Nucleic Acids Res. 2021;49:W293–W296.
    doi: 10.1093/nar/gkab301pmc: PMC8265157pubmed: 33885785google scholar: lookup
  34. Wick R.R, Judd L.M, Gorrie C.L, Holt K.E. Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads.. PLoS Comput. Biol. 2017;13:e1005595.
    doi: 10.1371/journal.pcbi.1005595pmc: PMC5481147pubmed: 28594827google scholar: lookup
  35. Wick R.R, Schultz M.B, Zobel J, Holt K.E. Bandage: Interactive visualization of de novo genome assemblies.. Bioinformatics 2015;31:3350–3352.
    doi: 10.1093/bioinformatics/btv383pmc: PMC4595904pubmed: 26099265google scholar: lookup
  36. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki E.P, Zaslavsky L, Lomsadze A, Pruitt K.D, Borodovsky M, Ostell J. NCBI prokaryotic genome annotation pipeline.. Nucleic Acids Res. 2016;44:6614–6624.
    doi: 10.1093/nar/gkw569pmc: PMC5001611pubmed: 27342282google scholar: lookup
  37. Arndt D, Grant J.R, Marcu A, Sajed T, Pon A, Liang Y, Wishart D.S. PHASTER: A better, faster version of the PHAST phage search tool.. Nucleic Acids Res. 2016;44:16–21.
    doi: 10.1093/nar/gkw387pmc: PMC4987931pubmed: 27141966google scholar: lookup
  38. Fawley W.N, Knetsch C.W, MacCannell D.R, Harmanus C, Du T, Mulvey M.R, Paulick A, Anderson L, Kuijper E.J, Wilcox M.H. Development and validation of an internationally-standardized, high-resolution capillary gel-based electrophoresis PCR-ribotyping protocol for Clostridium difficile.. PLoS ONE 2015;10:e0118150.
    doi: 10.1371/journal.pone.0118150pmc: PMC4332677pubmed: 25679978google scholar: lookup
  39. Weese J.S, Rousseau J, Deckert A, Gow S, Reid-Smith R.J. Clostridium difficile and methicillin-resistant Staphylococcus aureus shedding by slaughter-age pigs.. BMC Vet. Res. 2011;7:41.
    doi: 10.1186/1746-6148-7-41pmc: PMC3162498pubmed: 21791057google scholar: lookup
  40. Medina-Torres C.E, Weese J.S, Staempfli H.R. Validation of a commercial enzyme immunoassay for detection of Clostridium difficile toxins in feces of horses with acute diarrhea.. J. Vet. Intern. Med. 2010;24:628–632.
    doi: 10.1111/j.1939-1676.2010.00506.xpubmed: 20384955google scholar: lookup
  41. Connor M.C, McGrath J.W, McMullan G, Marks N, Fairley D.J. Development of an optimized broth enrichment culture medium for the isolation of Clostridium difficile.. Anaerobe 2018;54:92–99.
    doi: 10.1016/j.anaerobe.2018.08.006pubmed: 30118894google scholar: lookup
  42. Dharmasena M, Jiang X. Improving culture media for the isolation of Clostridium difficile from compost.. Anaerobe 2018;51:1–7.
    doi: 10.1016/j.anaerobe.2018.03.002pubmed: 29518533google scholar: lookup
  43. Blanco J.L, Álvarez-Pérez S, García M.E. Is the prevalence of Clostridium difficile in animals underestimated?. Vet. J. 2013;197:694–698.
    doi: 10.1016/j.tvjl.2013.03.053pubmed: 23911042google scholar: lookup
  44. Weese J.S, Avery B.P, Rousseau J, Reid-Smith R.J. Detection and enumeration of Clostridium difficile spores in retail beef and pork.. Appl. Environ. Microbiol. 2009;75:5009.
    doi: 10.1128/AEM.00480-09pmc: PMC2725490pubmed: 19525267google scholar: lookup
  45. Lawley T.D, Clare S, Deakin L.J, Goulding D, Yen J.L, Raisen C, Brandt C, Lovell J, Cooke F, Clark T.G. Use of purified Clostridium difficile spores to facilitate evaluation of health care disinfection regimens.. Appl. Environ. Microbiol. 2010;76:6895–6900.
    doi: 10.1128/AEM.00718-10pmc: PMC2953018pubmed: 20802075google scholar: lookup
  46. Rodriguez C, Taminiau B, Brévers B, Avesani V, Van Broeck J, Leroux A.A, Amory H, Delmée M, Daube G. 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;172:309–317.
    doi: 10.1016/j.vetmic.2014.05.013pubmed: 24894133google scholar: lookup
  47. Schoster A, Staempfli H.R, Arroyo L.G, Reid-Smith R.J, Janecko N, Shewen P.E, Weese J.S. Longitudinal study of Clostridium difficile and antimicrobial susceptibility of Escherichia coli in healthy horses in a community setting.. Vet. Microbiol. 2012;159:364–370.
    doi: 10.1016/j.vetmic.2012.04.006pubmed: 22554764google scholar: lookup
  48. Bandelj P, Blagus R, Briski F, Frlic O, Vergles Rataj A, Rupnik M, Ocepek M, Vengust M. Identification of risk factors influencing Clostridium difficile prevalence in middle-size dairy farms.. Vet. Res. 2016;47:41.
    doi: 10.1186/s13567-016-0326-0pmc: PMC4788955pubmed: 26968527google scholar: lookup
  49. He M, Sebaihia M, Lawley T.D, Stabler R.A, Dawson L.F, Martin M.J, Holt K.E, Seth-Smith H.M.B, Quail M.A, Rance R. Evolutionary dynamics of Clostridium difficile over short and long time scales.. Proc. Natl. Acad. Sci. USA 2010;107:7527–7532.
    doi: 10.1073/pnas.0914322107pmc: PMC2867753pubmed: 20368420google scholar: lookup
  50. Brouwer M.S.M, Roberts A.P, Hussain H, Williams R.J, Allan E, Mullany P. Horizontal gene transfer converts non-toxigenic Clostridium difficile strains into toxin producers.. Nat. Commun. 2013;4:2601.
    doi: 10.1038/ncomms3601pmc: PMC3826655pubmed: 24131955google scholar: lookup
  51. Natarajan M, Walk S.T, Young V.B, Aronoff D.M. A clinical and epidemiological review of non-toxigenic Clostridium difficile.. Anaerobe 2013;22:1–5.
    doi: 10.1016/j.anaerobe.2013.05.005pmc: PMC3729612pubmed: 23727391google scholar: lookup
  52. Gerding D.N, Sambol S.P, Johnson S. Non-toxigenic Clostridioides (Formerly Clostridium) difficile for prevention of C. difficile infection: From bench to bedside back to bench and back to bedside.. Front. Microbiol. 2018;9:1700.
    doi: 10.3389/fmicb.2018.01700pmc: PMC6070627pubmed: 30093897google scholar: lookup
  53. Sambol S.P, Skinner A.M, Serna-Perez F, Owen B, Gerding D.N, Johnson S. Effective colonization by nontoxigenic Clostridioides difficile REA strain M3 (NTCD-M3) spores following treatment with either Fidaxomicin or Vancomycin.. Microbiol. Spectr. 2023;11:e0051723.
    doi: 10.1128/spectrum.00517-23pmc: PMC10100807pubmed: 36975811google scholar: lookup
  54. Knight D.R, Squire M.M, Collins D.A, Riley T.V. Genome analysis of Clostridium difficile PCR ribotype 014 lineage in Australian pigs and humans reveals a diverse genetic repertoire and signatures of long-range interspecies Transmission.. Front. Microbiol. 2016;7:2138.
    doi: 10.3389/fmicb.2016.02138pmc: PMC5225093pubmed: 28123380google scholar: lookup
  55. Moono P, Lim S.C, Riley T.V. High prevalence of toxigenic Clostridium difficile in public space lawns in Western Australia.. Sci. Rep. 2017;7:41196.
    doi: 10.1038/srep41196pmc: PMC5286503pubmed: 28145453google scholar: lookup
  56. Hong S, Putsathit P, George N, Hemphill C, Huntington P.G, Korman T.M, Kotsanas D, Lahra M, McDougall R, Moore C.V. Laboratory-based surveillance of Clostridium difficile infection in Australian health care and community settings, 2013 to 2018.. J. Clin. Microbiol. 2020;58:e01552-20.
    doi: 10.1128/JCM.01552-20pmc: PMC7587093pubmed: 32848038google scholar: lookup
  57. Collins D.A, Riley T.V. Clostridium difficile in Asia: Opportunities for One Health management.. Trop. Med. Infect. Dis. 2019;4:7.
    doi: 10.3390/tropicalmed4010007pmc: PMC6473466pubmed: 30597880google scholar: lookup
  58. Freeman J, Vernon J, Morris K, Nicholson S, Todhunter S, Longshaw C, Wilcox M.H. Pan-European longitudinal surveillance of antibiotic resistance among prevalent Clostridium difficile ribotypes.. Clin. Microbiol. Infect. 2015;21:248.e9–248.e16.
    doi: 10.1016/j.cmi.2014.09.017pubmed: 25701178google scholar: lookup
  59. Weese J.S, Slovis N, Rousseau J. Clostridioides (Clostridium) difficile in neonatal foals and mares at a referral hospital.. J. Vet. Intern. Med. 2021;35:1140–1146.
    doi: 10.1111/jvim.16094pmc: PMC7995440pubmed: 33656757google scholar: lookup
  60. Lee Y.-R, Lee K, Byun J.-W, Kim H, So B, Ku B.-K, Kim H.-Y, Moon B.-Y. Prevalence, genetic characteristics, and antimicrobial resistance of Clostridioides difficile isolates from horses in Korea.. Anaerobe 2023;80:102700.
    doi: 10.1016/j.anaerobe.2023.102700pubmed: 36716814google scholar: lookup
  61. Knight D.R, Kullin B, Androga G.O, Barbut F, Eckert C, Johnson S, Spigaglia P, Tateda K, Tsai P.J, Riley T.V. Evolutionary and genomic insights into Sequence Type 11: A diverse zoonotic and antimicrobial-resistant lineage of global One Health importance.. mBio 2019;10:e00446-19.
    doi: 10.1128/mBio.00446-19pmc: PMC6469969pubmed: 30992351google scholar: lookup
  62. Janezic S, Garneau J.R, Monot M. Comparative Genomics of Clostridium difficile.. 2018.
    pubmed: 0
  63. Imwattana K, Kiratisin P, Riley T.V, Knight D.R. Genomic basis of antimicrobial resistance in non-toxigenic Clostridium difficile in Southeast Asia.. Anaerobe 2020;66:102290.
    doi: 10.1016/j.anaerobe.2020.102290pubmed: 33137436google scholar: lookup
  64. Hardefeldt L.Y, Gilkerson J.R, Billman-Jacobe H, Stevenson M.A, Thursky K, Bailey K.E, Browning G.F. Barriers to and enablers of implementing antimicrobial stewardship programs in veterinary practices.. J. Vet. Intern. Med. 2018;32:1092–1099.
    doi: 10.1111/jvim.15083pmc: PMC5980358pubmed: 29573053google scholar: lookup

Citations

This article has been cited 5 times.
  1. Petry S, Tapprest J, Maillard K, Barbut F, Duquesne F, Kozak S, Foucher N, Bernez-Romand M, Bridoux L, Poquet I. Clostridioides difficile in equidae necropsied in Northwestern France, between 2019 and 2021. Microbiol Spectr 2026 Feb 3;14(2):e0216525.
    doi: 10.1128/spectrum.02165-25pubmed: 41467783google scholar: lookup
  2. Hardefeldt L, Thomas K, Page S, Norris J, Browning G, El Hage C, Stewart A, Gilkerson J, Muscatello G, Verwilghen D, van Galen G, Bauquier J, Cuming R, Reynolds B, Whittaker C, Wilkes E, Clulow J, Burden C, Begg L. Antimicrobial prescribing guidelines for horses in Australia. Aust Vet J 2025 Dec;103(12):781-889.
    doi: 10.1111/avj.70003pubmed: 40903020google scholar: lookup
  3. Hain-Saunders NMR, Knight DR, Harvey A, Bruce M, Hampson BA, Riley TV. Clostridioides difficile in feral horse populations in Australia. Appl Environ Microbiol 2025 May 21;91(5):e0211424.
    doi: 10.1128/aem.02114-24pubmed: 40172204google scholar: lookup
  4. Alexiou S, Diakou A, Kachrimanidou M. The Role of Clostridioides difficile Within the One Health Framework: A Review. Microorganisms 2025 Feb 16;13(2).
    doi: 10.3390/microorganisms13020429pubmed: 40005794google scholar: lookup
  5. Hain-Saunders N, Knight DR, Bruce M, Riley TV. Complete genome sequences of toxigenic Clostridioides difficile isolated from Australian feral horses. Microbiol Resour Announc 2024 Dec 12;13(12):e0108624.
    doi: 10.1128/mra.01086-24pubmed: 39576097google scholar: lookup
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