FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Microbiome2023; 11(1); 33; doi: 10.1186/s40168-023-01465-6

Longitudinal study of the short- and long-term effects of hospitalisation and oral trimethoprim-sulfadiazine administration on the equine faecal microbiome and resistome.

Abstract: Hospitalisation and antimicrobial treatment are common in horses and significantly impact the intestinal microbiota. Antimicrobial treatment might also increase levels of resistant bacteria in faeces, which could spread to other ecological compartments, such as the environment, other animals and humans. In this study, we aimed to characterise the short- and long-term effects of transportation, hospitalisation and trimethoprim-sulfadiazine (TMS) administration on the faecal microbiota and resistome of healthy equids. In a longitudinal experimental study design, in which the ponies served as their own control, faecal samples were collected from six healthy Welsh ponies at the farm (D0-D13-1), immediately following transportation to the hospital (D13-2), during 7 days of hospitalisation without treatment (D14-D21), during 5 days of oral TMS treatment (D22-D26) and after discharge from the hospital up to 6 months later (D27-D211). After DNA extraction, 16S rRNA gene sequencing was performed on all samples. For resistome analysis, shotgun metagenomic sequencing was performed on selected samples. Hospitalisation without antimicrobial treatment did not significantly affect microbiota composition. Oral TMS treatment reduced alpha-diversity significantly. Kiritimatiellaeota, Fibrobacteres and Verrucomicrobia significantly decreased in relative abundance, whereas Firmicutes increased. The faecal microbiota composition gradually recovered after discontinuation of TMS treatment and discharge from the hospital and, after 2 weeks, was more similar to pre-treatment composition than to composition during TMS treatment. Six months later, however, microbiota composition still differed significantly from that at the start of the study and Spirochaetes and Verrucomicrobia were less abundant. TMS administration led to a significant (up to 32-fold) and rapid increase in the relative abundance of resistance genes sul2, tetQ, ant6-1a, and aph(3")-lb. lnuC significantly decreased directly after treatment. Resistance genes sul2 (15-fold) and tetQ (six-fold) remained significantly increased 6 months later. Oral treatment with TMS has a rapid and long-lasting effect on faecal microbiota composition and resistome, making the equine hindgut a reservoir and potential source of resistant bacteria posing a risk to animal and human health through transmission. These findings support the judicious use of antimicrobials to minimise long-term faecal presence, excretion and the spread of antimicrobial resistance in the environment. Video Abstract.
© 2023. The Author(s).
Get Full Text
Publication Date: 2023-02-27 PubMed ID: 36850017PubMed Central: PMC9969626DOI: 10.1186/s40168-023-01465-6Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Video-Audio Media
  • Journal Article

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 study examines the short and long-term impact of hospitalisation and an antibiotic treatment on the diversity and composition of bacteria in horse faeces, particularly the increase in antibiotic-resistant bacteria. It finds that hospitalisation alone doesn’t significantly alter the faecal bacteria, but the antibiotic treatment causes marked changes that can persist for up to six months, potentially posing a risk to other animals and humans.

Study Design and Process

  • Researchers conducted a longitudinal study observing the effects of transportation, hospitalisation, and trimethoprim-sulfadiazine (TMS) treatment on six healthy Welsh ponies.
  • In this study, ponies served as their own control by collecting faecal samples at various stages: before and after transportation, during hospitalisation with and without TMS treatment, and up to six months following discharge.
  • Researchers extracted DNA for 16S rRNA gene sequencing from all samples to study the microbiota.
  • To study the resistome (set of antibiotic resistance genes), shotgun metagenomic sequencing was performed on selected samples.

Impact of Hospitalisation and Treatment on Microbiota Composition

  • The study did not observe any significant effects on the faecal microbiota composition due to hospitalisation without antimicrobial treatment.
  • However, during the oral TMS treatment, the microbiota alpha-diversity significantly reduced, and the abundances of specific bacterial groups shifted. The populations of Kiritimatiellaeota, Fibrobacteres, and Verrucomicrobia reduced, and Firmicutes increased.
  • Post the discontinuation of the TMS treatment and discharge, the faecal microbiota composition gradually returned closer to pre-treatment state within two weeks. However, microbiota composition was still significantly different from the start even after six months.

Impact on Resistome

  • It was found that TMS treatment led to a sharp and significant increase in the relative abundance of several resistance genes, indicating an increased presence of antibiotic-resistant bacteria.
  • While some resistance genes decreased immediately after treatment stopped, genes like sul2 and tetQ remained significantly increased even six months after treatment.

Implications of the Study

  • The significant long-term increase in antibiotic resistance in the faecal microbiota due to TMS treatment indicates that the horse’s gut can become a reservoir for antibiotic-resistant bacteria, which is a potential health risk.
  • This long-lasting presence of antibiotic-resistant bacteria could pose risks to other animals and humans through transmission.
  • These results highlight the need for careful use of antimicrobials to minimise the long-term presence and spread of antimicrobial resistance in the environment.

Cite This Article

APA
Theelen MJP, Luiken REC, Wagenaar JA, Sloet van Oldruitenborgh-Oosterbaan MM, Rossen JWA, Schaafstra FJWC, van Doorn DA, Zomer AL. (2023). Longitudinal study of the short- and long-term effects of hospitalisation and oral trimethoprim-sulfadiazine administration on the equine faecal microbiome and resistome. Microbiome, 11(1), 33. https://doi.org/10.1186/s40168-023-01465-6

Publication

Microbiome
ISSN: 2049-2618
NlmUniqueID: 101615147
Country: England
Language: English
Volume: 11
Issue: 1
Pages: 33
PII: 33

Researcher Affiliations

Theelen, Mathijs J P
  • Department of Clinical Sciences (Equine Sciences), Faculty of Veterinary Medicine, Utrecht University, Yalelaan 112, 3584, CM, Utrecht, the Netherlands. m.j.p.theelen@uu.nl.
  • Department of Biomolecular Health Sciences (Infectious Diseases and Immunology), Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, 3584, CL, Utrecht, the Netherlands. m.j.p.theelen@uu.nl.
Luiken, Roosmarijn E C
  • Department of Biomolecular Health Sciences (Infectious Diseases and Immunology), Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, 3584, CL, Utrecht, the Netherlands.
Wagenaar, Jaap A
  • Department of Biomolecular Health Sciences (Infectious Diseases and Immunology), Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, 3584, CL, Utrecht, the Netherlands.
  • WHO Collaborating Centre for Reference and Research on Campylobacter and Antimicrobial Resistance from a One Health Perspective/OIE Reference Laboratory for Campylobacteriosis, Yalelaan 1, 3584, CL, Utrecht, the Netherlands.
Sloet van Oldruitenborgh-Oosterbaan, Marianne M
  • Department of Clinical Sciences (Equine Sciences), Faculty of Veterinary Medicine, Utrecht University, Yalelaan 112, 3584, CM, Utrecht, the Netherlands.
Rossen, John W A
  • Department of Medical Microbiology and Infection Prevention, University Medical Center Groningen, University of Groningen, Hanzeplein 1, 9713, GZ, Groningen, the Netherlands.
  • Department of Pathology, University of Utah School of Medicine, 15 North Medical Drive East, Ste #1100, Salt Lake City, Utah, 84112, USA.
Schaafstra, Femke J W C
  • HAS University of Applied Sciences, Onderwijsboulevard 221, 5223, DE, 's-Hertogenbosch, the Netherlands.
  • Department of Population Health Sciences (Farm Animal Health), Faculty of Veterinary Medicine, Utrecht University, Yalelaan 7, 3584, CL, Utrecht, the Netherlands.
van Doorn, David A
  • Department of Clinical Sciences (Equine Sciences), Faculty of Veterinary Medicine, Utrecht University, Yalelaan 112, 3584, CM, Utrecht, the Netherlands.
  • Department of Population Health Sciences (Farm Animal Health), Faculty of Veterinary Medicine, Utrecht University, Yalelaan 7, 3584, CL, Utrecht, the Netherlands.
Zomer, Aldert L
  • Department of Biomolecular Health Sciences (Infectious Diseases and Immunology), Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, 3584, CL, Utrecht, the Netherlands.
  • WHO Collaborating Centre for Reference and Research on Campylobacter and Antimicrobial Resistance from a One Health Perspective/OIE Reference Laboratory for Campylobacteriosis, Yalelaan 1, 3584, CL, Utrecht, the Netherlands.

MeSH Terms

  • Humans
  • Horses
  • Animals
  • Trimethoprim / pharmacology
  • Longitudinal Studies
  • RNA, Ribosomal, 16S / genetics
  • Hospitalization
  • Feces
  • Microbiota / genetics

Conflict of Interest Statement

JR is consulting for IDbyDNA Inc. The other authors declare that they have no competing interests.

References

This article includes 65 references
  1. Costa MC, Weese JS. Understanding the Intestinal Microbiome in Health and Disease.. Vet Clin North Am Equine Pract 2018 Apr;34(1):1-12.
    doi: 10.1016/j.cveq.2017.11.005pubmed: 29402480google scholar: lookup
  2. Theelen MJP, Luiken REC, Wagenaar JA, Sloet van Oldruitenborgh-Oosterbaan MM, Rossen JWA, Zomer AL. The Equine Faecal Microbiota of Healthy Horses and Ponies in The Netherlands: Impact of Host and Environmental Factors.. Animals (Basel) 2021 Jun 12;11(6).
    doi: 10.3390/ani11061762pmc: PMC8231505pubmed: 34204691google scholar: lookup
  3. Costa MC, Arroyo LG, Allen-Vercoe E, Stämpfli HR, Kim PT, Sturgeon A, Weese JS. Comparison of the fecal microbiota of healthy horses and horses with colitis by high throughput sequencing of the V3-V5 region of the 16S rRNA gene.. PLoS One 2012;7(7):e41484.
    doi: 10.1371/journal.pone.0041484pmc: PMC3409227pubmed: 22859989google scholar: lookup
  4. Arnold C, Pilla R, Chaffin K, Lidbury J, Steiner J, Suchodolski J. Alterations in the Fecal Microbiome and Metabolome of Horses with Antimicrobial-Associated Diarrhea Compared to Antibiotic-Treated and Non-Treated Healthy Case Controls.. Animals (Basel) 2021 Jun 17;11(6).
    doi: 10.3390/ani11061807pmc: PMC8235368pubmed: 34204371google scholar: lookup
  5. Costa MC, Stämpfli HR, Arroyo LG, Allen-Vercoe E, Gomes RG, Weese JS. Changes in the equine fecal microbiota associated with the use of systemic antimicrobial drugs.. BMC Vet Res 2015 Feb 3;11:19.
    doi: 10.1186/s12917-015-0335-7pmc: PMC4323147pubmed: 25644524google scholar: lookup
  6. Barr BS, Waldridge BM, Morresey PR, Reed SM, Clark C, Belgrave R, Donecker JM, Weigel DJ. Antimicrobial-associated diarrhoea in three equine referral practices.. Equine Vet J 2013 Mar;45(2):154-8.
    doi: 10.1111/j.2042-3306.2012.00595.xpubmed: 22779907google scholar: lookup
  7. Singh KS, Anand S, Dholpuria S, Sharma JK, Blankenfeldt W, Shouche Y. Antimicrobial resistance dynamics and the one-health strategy: a review. Environ Chem Lett 2021;19(4):2995–3007.
    doi: 10.1007/s10311-021-01238-3google scholar: lookup
  8. Laxminarayan R, Van Boeckel T, Frost I, Kariuki S, Khan EA, Limmathurotsakul D, Larsson DGJ, Levy-Hara G, Mendelson M, Outterson K, Peacock SJ, Zhu YG. The Lancet Infectious Diseases Commission on antimicrobial resistance: 6 years later.. Lancet Infect Dis 2020 Apr;20(4):e51-e60.
    doi: 10.1016/S1473-3099(20)30003-7pubmed: 32059790google scholar: lookup
  9. Collignon PJ, McEwen SA. One Health-Its Importance in Helping to Better Control Antimicrobial Resistance.. Trop Med Infect Dis 2019 Jan 29;4(1).
    doi: 10.3390/tropicalmed4010022pmc: PMC6473376pubmed: 30700019google scholar: lookup
  10. Wright GD. The antibiotic resistome: the nexus of chemical and genetic diversity.. Nat Rev Microbiol 2007 Mar;5(3):175-86.
    doi: 10.1038/nrmicro1614pubmed: 17277795google scholar: lookup
  11. Kim M, Park J, Kang M, Yang J, Park W. Gain and loss of antibiotic resistant genes in multidrug resistant bacteria: One Health perspective.. J Microbiol 2021 Jun;59(6):535-545.
    doi: 10.1007/s12275-021-1085-9pubmed: 33877574google scholar: lookup
  12. Álvarez-Narváez S, Berghaus LJ, Morris ERA, Willingham-Lane JM, Slovis NM, Giguere S, Cohen ND. A Common Practice of Widespread Antimicrobial Use in Horse Production Promotes Multi-Drug Resistance.. Sci Rep 2020 Jan 22;10(1):911.
    doi: 10.1038/s41598-020-57479-9pmc: PMC6976650pubmed: 31969575google scholar: lookup
  13. Urra J, Alkorta I, Lanzén A, Mijangos I, Garbisu C. The application of fresh and composted horse and chicken manure affects soil quality, microbial composition and antibiotic resistance. Appl Soil Ecol 2019;135:73–84.
    doi: 10.1016/j.apsoil.2018.11.005google scholar: lookup
  14. Mitchell S, Bull M, Muscatello G, Chapman B, Coleman NV. The equine hindgut as a reservoir of mobile genetic elements and antimicrobial resistance genes.. Crit Rev Microbiol 2021 Sep;47(5):543-561.
    doi: 10.1080/1040841X.2021.1907301pubmed: 33899656google scholar: lookup
  15. Faubladier C, Chaucheyras-Durand F, da Veiga L, Julliand V. Effect of transportation on fecal bacterial communities and fermentative activities in horses: impact of Saccharomyces cerevisiae CNCM I-1077 supplementation.. J Anim Sci 2013 Apr;91(4):1736-44.
    doi: 10.2527/jas.2012-5720pubmed: 23408806google scholar: lookup
  16. Liu Y, Bailey KE, Dyall-Smith M, Marenda MS, Hardefeldt LY, Browning GF, Gilkerson JR, Billman-Jacobe H. Faecal microbiota and antimicrobial resistance gene profiles of healthy foals.. Equine Vet J 2021 Jul;53(4):806-816.
    doi: 10.1111/evj.13366pubmed: 33030244google scholar: lookup
  17. Knudsen BE, Bergmark L, Munk P, Lukjancenko O, Priemé A, Aarestrup FM, Pamp SJ. Impact of Sample Type and DNA Isolation Procedure on Genomic Inference of Microbiome Composition.. mSystems 2016 Sep-Oct;1(5).
    doi: 10.1128/mSystems.00095-16pmc: PMC5080404pubmed: 27822556google scholar: lookup
  18. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data.. Nat Methods 2016 Jul;13(7):581-3.
    doi: 10.1038/nmeth.3869pmc: PMC4927377pubmed: 27214047google scholar: lookup
  19. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools.. Nucleic Acids Res 2013 Jan;41(Database issue):D590-6.
    doi: 10.1093/nar/gks1219pmc: PMC3531112pubmed: 23193283google scholar: lookup
  20. Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor.. Bioinformatics 2018 Sep 1;34(17):i884-i890.
    doi: 10.1093/bioinformatics/bty560pmc: PMC6129281pubmed: 30423086google scholar: lookup
  21. Clausen PTLC, Aarestrup FM, Lund O. Rapid and precise alignment of raw reads against redundant databases with KMA.. BMC Bioinformatics 2018 Aug 29;19(1):307.
    doi: 10.1186/s12859-018-2336-6pmc: PMC6116485pubmed: 30157759google scholar: lookup
  22. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, Aarestrup FM, Larsen MV. Identification of acquired antimicrobial resistance genes.. J Antimicrob Chemother 2012 Nov;67(11):2640-4.
    doi: 10.1093/jac/dks261pmc: PMC3468078pubmed: 22782487google scholar: lookup
  23. Wood DE, Lu J, Langmead B. Improved metagenomic analysis with Kraken 2.. Genome Biol 2019 Nov 28;20(1):257.
    doi: 10.1186/s13059-019-1891-0pmc: PMC6883579pubmed: 31779668google scholar: lookup
  24. Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: accelerated for clustering the next-generation sequencing data.. Bioinformatics 2012 Dec 1;28(23):3150-2.
    doi: 10.1093/bioinformatics/bts565pmc: PMC3516142pubmed: 23060610google scholar: lookup
  25. Munk P, Knudsen BE, Lukjancenko O, Duarte ASR, Van Gompel L, Luiken REC, Smit LAM, Schmitt H, Garcia AD, Hansen RB, Petersen TN, Bossers A, Ruppé E, Lund O, Hald T, Pamp SJ, Vigre H, Heederik D, Wagenaar JA, Mevius D, Aarestrup FM. Abundance and diversity of the faecal resistome in slaughter pigs and broilers in nine European countries.. Nat Microbiol 2018 Aug;3(8):898-908.
    doi: 10.1038/s41564-018-0192-9pubmed: 30038308google scholar: lookup
  26. R Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2020.
  27. McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data.. PLoS One 2013;8(4):e61217.
    doi: 10.1371/journal.pone.0061217pmc: PMC3632530pubmed: 23630581google scholar: lookup
  28. Oksanen J, Kindt R, Legendre P, O'Hara B, Simpson GL, Solymos P. Vegan community ecology package. R package version 2019;2:5–6.
  29. Wickham H. ggplot2: elegant graphics for data analysis. New York: Springer, Cham; 2016.
  30. Svetnik V, Liaw A, Tong C, Culberson JC, Sheridan RP, Feuston BP. Random forest: a classification and regression tool for compound classification and QSAR modeling.. J Chem Inf Comput Sci 2003 Nov-Dec;43(6):1947-58.
    doi: 10.1021/ci034160gpubmed: 14632445google scholar: lookup
  31. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.. Genome Biol 2014;15(12):550.
    doi: 10.1186/s13059-014-0550-8pmc: PMC4302049pubmed: 25516281google scholar: lookup
  32. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 1995;57(1):289–300.
  33. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing.. J Comput Biol 2012 May;19(5):455-77.
    doi: 10.1089/cmb.2012.0021pmc: PMC3342519pubmed: 22506599google scholar: lookup
  34. von Meijenfeldt FAB, Arkhipova K, Cambuy DD, Coutinho FH, Dutilh BE. Robust taxonomic classification of uncharted microbial sequences and bins with CAT and BAT.. Genome Biol 2019 Oct 22;20(1):217.
    doi: 10.1186/s13059-019-1817-xpmc: PMC6805573pubmed: 31640809google scholar: lookup
  35. Di Pietro R, Arroyo LG, Leclere M, Costa MC. Species-Level Gut Microbiota Analysis after Antibiotic-Induced Dysbiosis in Horses.. Animals (Basel) 2021 Sep 30;11(10).
    doi: 10.3390/ani11102859pmc: PMC8533001pubmed: 34679880google scholar: lookup
  36. Salem SE, Maddox TW, Berg A, Antczak P, Ketley JM, Williams NJ, Archer DC. Variation in faecal microbiota in a group of horses managed at pasture over a 12-month period.. Sci Rep 2018 May 31;8(1):8510.
    doi: 10.1038/s41598-018-26930-3pmc: PMC5981443pubmed: 29855517google scholar: lookup
  37. Stewart HL, Pitta D, Indugu N, Vecchiarelli B, Engiles JB, Southwood LL. Characterization of the fecal microbiota of healthy horses.. Am J Vet Res 2018 Aug;79(8):811-819.
    doi: 10.2460/ajvr.79.8.811pubmed: 30058849google scholar: lookup
  38. Costa MC, Silva G, Ramos RV, Staempfli HR, Arroyo LG, Kim P, Weese JS. Characterization and comparison of the bacterial microbiota in different gastrointestinal tract compartments in horses.. Vet J 2015 Jul;205(1):74-80.
    doi: 10.1016/j.tvjl.2015.03.018pubmed: 25975855google scholar: lookup
  39. Massacci FR, Clark A, Ruet A, Lansade L, Costa M, Mach N. Inter-breed diversity and temporal dynamics of the faecal microbiota in healthy horses.. J Anim Breed Genet 2020 Jan;137(1):103-120.
    doi: 10.1111/jbg.12441pubmed: 31523867google scholar: lookup
  40. O' Donnell MM, Harris HM, Jeffery IB, Claesson MJ, Younge B, O' Toole PW, Ross RP. The core faecal bacterial microbiome of Irish Thoroughbred racehorses.. Lett Appl Microbiol 2013 Dec;57(6):492-501.
    doi: 10.1111/lam.12137pubmed: 23889584google scholar: lookup
  41. Proudman CJ, Hunter JO, Darby AC, Escalona EE, Batty C, Turner C. Characterisation of the faecal metabolome and microbiome of Thoroughbred racehorses.. Equine Vet J 2015 Sep;47(5):580-6.
    doi: 10.1111/evj.12324pubmed: 25041526google scholar: lookup
  42. Schoster A, Mosing M, Jalali M, Staempfli HR, Weese JS. Effects of transport, fasting and anaesthesia on the faecal microbiota of healthy adult horses.. Equine Vet J 2016 Sep;48(5):595-602.
    doi: 10.1111/evj.12479pubmed: 26122549google scholar: lookup
  43. Schmidt A, Möstl E, Wehnert C, Aurich J, Müller J, Aurich C. Cortisol release and heart rate variability in horses during road transport.. Horm Behav 2010 Feb;57(2):209-15.
    doi: 10.1016/j.yhbeh.2009.11.003pubmed: 19944105google scholar: lookup
  44. Enck P, Merlin V, Erckenbrecht JF, Wienbeck M. Stress effects on gastrointestinal transit in the rat.. Gut 1989 Apr;30(4):455-9.
    doi: 10.1136/gut.30.4.455pmc: PMC1434046pubmed: 2714679google scholar: lookup
  45. Rochegüe T, Haenni M, Mondot S, Astruc C, Cazeau G, Ferry T, Madec JY, Lupo A. Impact of Antibiotic Therapies on Resistance Genes Dynamic and Composition of the Animal Gut Microbiota.. Animals (Basel) 2021 Nov 16;11(11).
    doi: 10.3390/ani11113280pmc: PMC8614244pubmed: 34828011google scholar: lookup
  46. Collinet A, Grimm P, Julliand S, Julliand V. Multidimensional Approach for Investigating the Effects of an Antibiotic-Probiotic Combination on the Equine Hindgut Ecosystem and Microbial Fibrolysis.. Front Microbiol 2021;12:646294.
    doi: 10.3389/fmicb.2021.646294pmc: PMC8027512pubmed: 33841371google scholar: lookup
  47. Ransom-Jones E, Jones DL, McCarthy AJ, McDonald JE. The Fibrobacteres: an important phylum of cellulose-degrading bacteria.. Microb Ecol 2012 Feb;63(2):267-81.
    doi: 10.1007/s00248-011-9998-1pubmed: 22213055google scholar: lookup
  48. Derrien M, Vaughan EE, Plugge CM, de Vos WM. Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium.. Int J Syst Evol Microbiol 2004 Sep;54(Pt 5):1469-1476.
    doi: 10.1099/ijs.0.02873-0pubmed: 15388697google scholar: lookup
  49. Lindenberg F, Krych L, Fielden J, Kot W, Frøkiær H, van Galen G, Nielsen DS, Hansen AK. Expression of immune regulatory genes correlate with the abundance of specific Clostridiales and Verrucomicrobia species in the equine ileum and cecum.. Sci Rep 2019 Sep 3;9(1):12674.
    doi: 10.1038/s41598-019-49081-5pmc: PMC6722064pubmed: 31481726google scholar: lookup
  50. Daly K, Proudman CJ, Duncan SH, Flint HJ, Dyer J, Shirazi-Beechey SP. Alterations in microbiota and fermentation products in equine large intestine in response to dietary variation and intestinal disease.. Br J Nutr 2012 Apr;107(7):989-95.
    doi: 10.1017/S0007114511003825pubmed: 21816118google scholar: lookup
  51. Spring S, Bunk B, Spröer C, Schumann P, Rohde M, Tindall BJ, Klenk HP. Characterization of the first cultured representative of Verrucomicrobia subdivision 5 indicates the proposal of a novel phylum.. ISME J 2016 Dec;10(12):2801-2816.
    doi: 10.1038/ismej.2016.84pmc: PMC5148204pubmed: 27300277google scholar: lookup
  52. Ricker N, Trachsel J, Colgan P, Jones J, Choi J, Lee J, Coetzee JF, Howe A, Brockmeier SL, Loving CL, Allen HK. Toward Antibiotic Stewardship: Route of Antibiotic Administration Impacts the Microbiota and Resistance Gene Diversity in Swine Feces.. Front Vet Sci 2020;7:255.
    doi: 10.3389/fvets.2020.00255pmc: PMC7249142pubmed: 32509805google scholar: lookup
  53. Palleja A, Mikkelsen KH, Forslund SK, Kashani A, Allin KH, Nielsen T, Hansen TH, Liang S, Feng Q, Zhang C, Pyl PT, Coelho LP, Yang H, Wang J, Typas A, Nielsen MF, Nielsen HB, Bork P, Wang J, Vilsbøll T, Hansen T, Knop FK, Arumugam M, Pedersen O. Recovery of gut microbiota of healthy adults following antibiotic exposure.. Nat Microbiol 2018 Nov;3(11):1255-1265.
    doi: 10.1038/s41564-018-0257-9pubmed: 30349083google scholar: lookup
  54. Hu Y, Yang X, Qin J, Lu N, Cheng G, Wu N, Pan Y, Li J, Zhu L, Wang X, Meng Z, Zhao F, Liu D, Ma J, Qin N, Xiang C, Xiao Y, Li L, Yang H, Wang J, Yang R, Gao GF, Wang J, Zhu B. Metagenome-wide analysis of antibiotic resistance genes in a large cohort of human gut microbiota.. Nat Commun 2013;4:2151.
    doi: 10.1038/ncomms3151pubmed: 23877117google scholar: lookup
  55. Dunowska M, Morley PS, Traub-Dargatz JL, Hyatt DR, Dargatz DA. Impact of hospitalization and antimicrobial drug administration on antimicrobial susceptibility patterns of commensal Escherichia coli isolated from the feces of horses.. J Am Vet Med Assoc 2006 Jun 15;228(12):1909-17.
    doi: 10.2460/javma.228.12.1909pubmed: 16784384google scholar: lookup
  56. Adams RJ, Mollenkopf DF, Mathys DA, Whittle A, Ballash GA, Mudge M, Daniels JB, Barr B, Wittum TE. Prevalence of extended-spectrum cephalosporin-, carbapenem-, and fluoroquinolone-resistant members of the family Enterobacteriaceae isolated from the feces of horses and hospital surfaces at two equine specialty hospitals.. J Am Vet Med Assoc 2021 Apr 1;258(7):758-766.
    doi: 10.2460/javma.258.7.758pubmed: 33754819google scholar: lookup
  57. Kauter A, Epping L, Ghazisaeedi F, Lübke-Becker A, Wolf SA, Kannapin D, Stoeckle SD, Semmler T, Günther S, Gehlen H, Walther B. Frequency, Local Dynamics, and Genomic Characteristics of ESBL-Producing Escherichia coli Isolated From Specimens of Hospitalized Horses.. Front Microbiol 2021;12:671676.
    doi: 10.3389/fmicb.2021.671676pmc: PMC8085565pubmed: 33936023google scholar: lookup
  58. Bryan J, Leonard N, Fanning S, Katz L, Duggan V. Antimicrobial resistance in commensal faecal Escherichia coli of hospitalised horses.. Ir Vet J 2010 Jun 1;63(6):373-9.
    doi: 10.1186/2046-0481-63-6-373pmc: PMC3113860pubmed: 21851747google scholar: lookup
  59. Schoster A, van Spijk JN, Damborg P, Moodley A, Kirchgaessner C, Hartnack S, Schmitt S. The effect of different antimicrobial treatment regimens on the faecal shedding of ESBL-producing Escherichia coli in horses.. Vet Microbiol 2020 Apr;243:108617.
    doi: 10.1016/j.vetmic.2020.108617pubmed: 32273003google scholar: lookup
  60. Williams A, Christley RM, McKane SA, Roberts VL, Clegg PD, Williams NJ. Antimicrobial resistance changes in enteric Escherichia coli of horses during hospitalisation: resistance profiling of isolates.. Vet J 2013 Jan;195(1):121-6.
    doi: 10.1016/j.tvjl.2012.08.001pubmed: 22967926google scholar: lookup
  61. Johns I, Verheyen K, Good L, Rycroft A. Antimicrobial resistance in faecal Escherichia coli isolates from horses treated with antimicrobials: a longitudinal study in hospitalised and non-hospitalised horses.. Vet Microbiol 2012 Oct 12;159(3-4):381-9.
    doi: 10.1016/j.vetmic.2012.04.010pubmed: 22565010google scholar: lookup
  62. Damborg P, Marskar P, Baptiste KE, Guardabassi L. Faecal shedding of CTX-M-producing Escherichia coli in horses receiving broad-spectrum antimicrobial prophylaxis after hospital admission.. Vet Microbiol 2012 Jan 27;154(3-4):298-304.
    doi: 10.1016/j.vetmic.2011.07.005pubmed: 21820821google scholar: lookup
  63. Alexander TW, Yanke JL, Reuter T, Topp E, Read RR, Selinger BL, McAllister TA. Longitudinal characterization of antimicrobial resistance genes in feces shed from cattle fed different subtherapeutic antibiotics.. BMC Microbiol 2011 Jan 24;11(1):19.
    pmc: PMC3037836pubmed: 21261985doi: 10.1186/1471-2180-11-19google scholar: lookup
  64. Aviv G, Rahav G, Gal-Mor O. Horizontal Transfer of the Salmonella enterica Serovar Infantis Resistance and Virulence Plasmid pESI to the Gut Microbiota of Warm-Blooded Hosts.. mBio 2016 Sep 6;7(5).
    doi: 10.1128/mBio.01395-16pmc: PMC5013300pubmed: 27601577google scholar: lookup
  65. Marbouty M, Cournac A, Flot JF, Marie-Nelly H, Mozziconacci J, Koszul R. Metagenomic chromosome conformation capture (meta3C) unveils the diversity of chromosome organization in microorganisms.. Elife 2014 Dec 17;3:e03318.
    doi: 10.7554/eLife.03318pmc: PMC4381813pubmed: 25517076google scholar: lookup

Citations

This article has been cited 5 times.
  1. Lagounova M, MacNicol JL, Weese JS, Pearson W. The Effect of Dietary Synbiotics in Actively Racing Standardbred Horses Receiving Trimethoprim/Sulfadiazine. Animals (Basel) 2023 Jul 18;13(14).
    doi: 10.3390/ani13142344pubmed: 37508120google scholar: lookup
  2. Prandi I, Bellato A, Nebbia P, Roch-Dupland O, Stella MC, Passarino E, Mauthe von Degerfeld M, Quaranta G, Robino P. Antimicrobial Resistance in Escherichia coli from Hedgehogs (Erinaceus europaeus) Admitted to a Wildlife Rescue Center. Animals (Basel) 2025 Jul 27;15(15).
    doi: 10.3390/ani15152206pubmed: 40804996google scholar: lookup
  3. Rubio-Garcia A, Luiken REC, Marcelino I, Rossen JWA, van Zeijl JH, Wagenaar JA, Zomer AL. Antimicrobial treatment affects the microbiome and resistome of both treated and untreated rehabilitating harbour seals (Phoca vitulina). Anim Microbiome 2025 Jul 23;7(1):77.
    doi: 10.1186/s42523-025-00449-1pubmed: 40702575google scholar: lookup
  4. Bell J, Radial SL, Cuming RS, Trope G, Hughes KJ. Effects of fecal microbiota transplantation on clinical outcomes and fecal microbiota of foals with diarrhea. J Vet Intern Med 2024 Sep-Oct;38(5):2718-2728.
    doi: 10.1111/jvim.17185pubmed: 39266472google scholar: lookup
  5. Rubio-Garcia A, Zomer AL, Guo R, Rossen JWA, van Zeijl JH, Wagenaar JA, Luiken REC. Characterising the gut microbiome of stranded harbour seals (Phoca vitulina) in rehabilitation. PLoS One 2023;18(12):e0295072.
    doi: 10.1371/journal.pone.0295072pubmed: 38051704google scholar: lookup
Subscribe to our newsletter
Join 100,129 horse owners like you who receive our email updates on horse health and nutrition.