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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).
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Publication Date: 2023-02-27 PubMed ID: 36850017PubMed Central: PMC9969626DOI: 10.1186/s40168-023-01465-6Google 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 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.

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Citations

This article has been cited 1 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
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