Bugs and drugs: a systems biology approach to characterising the effect of moxidectin on the horse’s faecal microbiome.
Abstract: Anthelmintic treatment is a risk factor for intestinal disease in the horse, known as colic. However the mechanisms involved in the onset of disease post anthelmintic treatment are unknown. The interaction between anthelmintic drugs and the gut microbiota may be associated with this observed increase in risk of colic. Little is known about the interaction between gut microbiota and anthelmintics and how treatment may alter microbiome function. The objectives of this study were: To characterise (1) faecal microbiota, (2) feed fermentation kinetics in vitro and (3) metabolic profiles following moxidectin administration to horses with very low (0 epg) adult strongyle burdens. Objective: Moxidectin will not alter (1) faecal microbiota, (2) feed fermentation in vitro, or, (3) host metabolome. Results: Moxidectin increased the relative abundance of Deferribacter spp. and Spirochaetes spp. observed after 160 h in moxidectin treated horses. Reduced in vitro fibre fermentation was observed 16 h following moxidectin administration in vivo (P = 0.001), along with lower pH in the in vitro fermentations from the moxidectin treated group. Metabolic profiles from urine samples did not differ between the treatment groups. However metabolic profiles from in vitro fermentations differed between moxidectin and control groups 16 h after treatment (R = 0.69, QY = 0.48), and within the moxidectin group between 16 h and 160 h post moxidectin treatment (R = 0.79, QY = 0.77). Metabolic profiles from in vitro fermentations and fermentation kinetics both indicated altered carbohydrate metabolism following in vivo treatment with moxidectin. Conclusions: These data suggest that in horses with low parasite burdens moxidectin had a small but measurable effect on both the community structure and the function of the gut microbiome.
Publication Date: 2020-10-14 PubMed ID: 33499996PubMed Central: PMC7807906DOI: 10.1186/s42523-020-00056-2Google 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.
- 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.
This study investigates the impact of a common anthelmintic drug, moxidectin, on the intestinal microbiome of horses. The results indicate that following treatment with moxidectin, there were changes in both the composition and function of the microbiome, particularly in horses with already low levels of parasites.
Research Objective
- The research aimed to understand the interaction between the anthelmintic drug moxidectin and gut microbiota in horses, particularly in those with low adult strongyle burdens (0 eggs per gram or epg).
- It aimed to determine if moxidectin altered the faecal microbiota, feed fermentation in vitro (in a laboratory setting), or the host’s metabolic process.
Results of the Study
- The research showed that moxidectin increased the relative abundance of Deferribacter spp. and Spirochaetes spp. in the horse’s faecal microbiota after 160 hours of treatment.
- There was a reduction observed in in vitro fibre fermentation about 16 hours after administering moxidectin.
- The pH from in vitro fermentations was lower in the group that received the moxidectin treatment.
- Interestingly, metabolic profiles from urine samples did not show significant differences between the treatment and control groups.
- However, metabolic profiles from in vitro fermentations did vary between the treatment and control groups 16 hours after treatment, and within the treatment group between 16 hours and 160 hours post moxidectin treatment.
- Both metabolic profiles from in vitro fermentations and fermentation kinetics suggested that carbohydrate metabolism was altered following moxidectin treatment.
Conclusion of the Study
- The data suggests that moxidectin has a slight but quantifiable effect on the structure and function of the gut microbiome in horses, especially those with low parasite burdens.
- This suggests that the usage of moxidectin and possibly other anthelmintic drugs can impact the health of horses, potentially increasing the risk of intestinal diseases such as colic.
Cite This Article
APA
Daniels SP, Leng J, Swann JR, Proudman CJ.
(2020).
Bugs and drugs: a systems biology approach to characterising the effect of moxidectin on the horse’s faecal microbiome.
Anim Microbiome, 2(1), 38.
https://doi.org/10.1186/s42523-020-00056-2 Publication
Researcher Affiliations
- School of Equine Management and Science, Royal Agricultural University, Cirencester, Gloucestershire, GL9 6JS, UK. simon.daniels@rau.ac.uk.
- School of Veterinary Medicine, University of Surrey, Guildford, Surrey, GU2 7TE, UK. simon.daniels@rau.ac.uk.
- School of Veterinary Medicine, University of Surrey, Guildford, Surrey, GU2 7TE, UK.
- Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Imperial College London, London, SW7 2AZ, UK.
- School of Veterinary Medicine, University of Surrey, Guildford, Surrey, GU2 7TE, UK.
Conflict of Interest Statement
None.
References
This article includes 60 references
- Peachey LE, Jenkins TP, Cantacessi C. This Gut Ain't Big Enough for Both of Us. Or Is It? Helminth-Microbiota Interactions in Veterinary Species.. Trends Parasitol 2017 Aug;33(8):619-632.
- Cortés A, Peachey LE, Jenkins TP, Scotti R, Cantacessi C. Helminths and microbes within the vertebrate gut - not all studies are created equal.. Parasitology 2019 Sep;146(11):1371-1378.
- Kaneene JB, Miller R, Ross WA, Gallagher K, Marteniuk J, Rook J. Risk factors for colic in the Michigan (USA) equine population.. Prev Vet Med 1997 Apr;30(1):23-36.
- Cohen ND, Gibbs PG, Woods AM. Dietary and other management factors associated with colic in horses.. J Am Vet Med Assoc 1999 Jul 1;215(1):53-60.
- Hillyer MH, Taylor FG, Proudman CJ, Edwards GB, Smith JE, French NP. Case control study to identify risk factors for simple colonic obstruction and distension colic in horses.. Equine Vet J 2002 Jul;34(5):455-63.
- Reid SW, Mair TS, Hillyer MH, Love S. Epidemiological risk factors associated with a diagnosis of clinical cyathostomiasis in the horse.. Equine Vet J 1995 Mar;27(2):127-30.
- Goachet AG, Ricard JM, Jacotot E, Varloud M, Julliand V. Effect of oral administration of anthelmintics on colonic microflora of horses. Proceedings of French Equine Veterinary Association Pau; 2004.
- Peachey LE, Molena RA, Jenkins TP, Di Cesare A, Traversa D, Hodgkinson JE, Cantacessi C. The relationships between faecal egg counts and gut microbial composition in UK Thoroughbreds infected by cyathostomins.. Int J Parasitol 2018 May;48(6):403-412.
- Peachey LE, Castro C, Molena RA, Jenkins TP, Griffin JL, Cantacessi C. Dysbiosis associated with acute helminth infections in herbivorous youngstock - observations and implications.. Sci Rep 2019 Jul 31;9(1):11121.
- Crotch-Harvey L, Thomas LA, Worgan HJ, Douglas JL, Gilby DE, McEwan NR. The effect of administration of fenbendazole on the microbial hindgut population of the horse.. J Equine Sci 2018;29(2):47-51.
- Li RW, Wu S, Li W, Navarro K, Couch RD, Hill D, Urban JF Jr. Alterations in the porcine colon microbiota induced by the gastrointestinal nematode Trichuris suis.. Infect Immun 2012 Jun;80(6):2150-7.
- Taxis TM, Wolff S, Gregg SJ, Minton NO, Zhang C, Dai J, Schnabel RD, Taylor JF, Kerley MS, Pires JC, Lamberson WR, Conant GC. The players may change but the game remains: network analyses of ruminal microbiomes suggest taxonomic differences mask functional similarity.. Nucleic Acids Res 2015 Nov 16;43(20):9600-12.
- Pinu FR, Beale DJ, Paten AM, Kouremenos K, Swarup S, Schirra HJ, Wishart D. Systems Biology and Multi-Omics Integration: Viewpoints from the Metabolomics Research Community.. Metabolites 2019 Apr 18;9(4).
- Pallister T, Jackson MA, Martin TC, Zierer J, Jennings A, Mohney RP, MacGregor A, Steves CJ, Cassidy A, Spector TD, Menni C. Hippurate as a metabolomic marker of gut microbiome diversity: Modulation by diet and relationship to metabolic syndrome.. Sci Rep 2017 Oct 20;7(1):13670.
- Escalona EE, Leng J, Dona AC, Merrifield CA, Holmes E, Proudman CJ, Swann JR. Dominant components of the Thoroughbred metabolome characterised by (1) H-nuclear magnetic resonance spectroscopy: A metabolite atlas of common biofluids.. Equine Vet J 2015 Nov;47(6):721-30.
- Leng J, Proudman C, Darby A, Blow F, Townsend N, Miller A, Swann J. Exploration of the Fecal Microbiota and Biomarker Discovery in Equine Grass Sickness.. J Proteome Res 2018 Mar 2;17(3):1120-1128.
- Lowman RS, Theodorou MK, Hyslop JJ, Dhanoa MS, Cudderford D. Evaluation of in vitro batch culture technique for estimating the in vivo digestability and digestable energy content of equine feeds using equine faeces as a source of microbial inoculum. Anim Feed Sci Technol 1999;80(1):11–27.
- France J, Dhanoa MS, Theodorou MK, Lister SJ, Davies DR, Isac D. A model to interpret gas accumulation profiles associated with in vitro degradation of ruminant feeds. J Theor Biol 1993;163:99–111.
- Leung JM, Graham AL, Knowles SCL. Parasite-Microbiota Interactions With the Vertebrate Gut: Synthesis Through an Ecological Lens.. Front Microbiol 2018;9:843.
- Jenkins TP, Brindley PJ, Gasser RB, Cantacessi C. Helminth Microbiomes - A Hidden Treasure Trove?. Trends Parasitol 2019 Jan;35(1):13-22.
- Walshe N, Duggan V, Cabrera-Rubio R, Crispie F, Cotter P, Feehan O, Mulcahy G. Removal of adult cyathostomins alters faecal microbiota and promotes an inflammatory phenotype in horses.. Int J Parasitol 2019 May;49(6):489-500.
- Kunz IGZ, Reed KJ, Metcalf JL, Hassel DM, Coleman RJ, Hess TM, Coleman SJ. Equine Fecal Microbiota Changes Associated With Anthelmintic Administration.. J Equine Vet Sci 2019 Jun;77:98-106.
- Kreisinger J, Bastien G, Hauffe HC, Marchesi J, Perkins SE. Interactions between multiple helminths and the gut microbiota in wild rodents.. Philos Trans R Soc Lond B Biol Sci 2015 Aug 19;370(1675).
- Berry D, Kuzyk O, Rauch I, Heider S, Schwab C, Hainzl E, Decker T, Müller M, Strobl B, Schleper C, Urich T, Wagner M, Kenner L, Loy A. Intestinal Microbiota Signatures Associated with Inflammation History in Mice Experiencing Recurring Colitis.. Front Microbiol 2015;6:1408.
- Steuer AE, Stewart JC, Barker VD, Adams AA, Nielsen MK. Cytokine and goblet cell gene expression in equine cyathostomin infection and larvicidal anthelmintic therapy.. Parasite Immunol 2020 Jun;42(6):e12709.
- Biddle AS, Black SJ, Blanchard JL. An in vitro model of the horse gut microbiome enables identification of lactate-utilizing bacteria that differentially respond to starch induction.. PLoS One 2013;8(10):e77599.
- Moore-Colyer M, Tuthill P, Bannister I, Daniels S. Growth Rates of Thoroughbred Foals and In Vitro Gut Health Parameters When Fed a Cereal or an All-Fiber Creep Feed.. J Equine Vet Sci 2020 Oct;93:103191.
- Leng J, Walton G, Swann J, Darby A, La Ragione R, Proudman C. "Bowel on the Bench": Proof of Concept of a Three-Stage, In Vitro Fermentation Model of the Equine Large Intestine.. Appl Environ Microbiol 2019 Dec 13;86(1).
- Cooper P, Walker AW, Reyes J, Chico M, Salter SJ, Vaca M, Parkhill J. Patent human infections with the whipworm, Trichuris trichiura, are not associated with alterations in the faecal microbiota.. PLoS One 2013;8(10):e76573.
- Li RW, Li W, Sun J, Yu P, Baldwin RL, Urban JF. The effect of helminth infection on the microbial composition and structure of the caprine abomasal microbiome.. Sci Rep 2016 Feb 8;6:20606.
- Clark A, Sallé G, Ballan V, Reigner F, Meynadier A, Cortet J, Koch C, Riou M, Blanchard A, Mach N. Strongyle Infection and Gut Microbiota: Profiling of Resistant and Susceptible Horses Over a Grazing Season.. Front Physiol 2018;9:272.
- Xu Z, Malmer D, Langille MG, Way SF, Knight R. Which is more important for classifying microbial communities: who's there or what they can do?. ISME J 2014 Dec;8(12):2357-9.
- Brown VE, Rymer C, Agnew RE, Givens I. Relationship between in vitro gas production profiles of forages and in vivo rumen fermentation patterns in beef steers fed those forages. Anim Feed Sci Technol 2002;98(1):13–24.
- Newbold CJ, Ramos-Morales E. Review: Ruminal microbiome and microbial metabolome: effects of diet and ruminant host.. Animal 2020 Mar;14(S1):s78-s86.
- Dougal K, de la Fuente G, Harris PA, Girdwood SE, Pinloche E, Newbold CJ. Identification of a core bacterial community within the large intestine of the horse.. PLoS One 2013;8(10):e77660.
- Julliand V, Grimm P. HORSE SPECIES SYMPOSIUM: The microbiome of the horse hindgut: History and current knowledge.. J Anim Sci 2016 Jun;94(6):2262-74.
- Coles GC, Bauer C, Borgsteede FH, Geerts S, Klei TR, Taylor MA, Waller PJ. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) methods for the detection of anthelmintic resistance in nematodes of veterinary importance.. Vet Parasitol 1992 Sep;44(1-2):35-44.
- Daniels SP, Proudman CJ. Ovicidal efficacy of fenbendazole after treatment of horses naturally infected with cyathostomins.. Vet Parasitol 2016 Aug 30;227:151-6.
- Tyma JF, Epstein KL, Whitfield-Cargile CM, Cohen ND, Giguère S. Investigation of effects of omeprazole on the fecal and gastric microbiota of healthy adult horses.. Am J Vet Res 2019 Jan;80(1):79-86.
- Faul F, Erdfelder E, Lang AG, Buchner A. G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences.. Behav Res Methods 2007 May;39(2):175-91.
- Gokbulut C, Nolan AM, McKellar QA. Plasma pharmacokinetics and faecal excretion of ivermectin, doramectin and moxidectin following oral administration in horses.. Equine Vet J 2001 Sep;33(5):494-8.
- Ellis JM, Hollands T. Accuracy of different methods of estimating the weight of horses.. Vet Rec 1998 Sep 19;143(12):335-6.
- Ellis RJ, Bruce KD, Jenkins C, Stothard JR, Ajarova L, Mugisha L, Viney ME. Comparison of the distal gut microbiota from people and animals in Africa.. PLoS One 2013;8(1):e54783.
- Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. QIIME allows analysis of high-throughput community sequencing data.. Nat Methods 2010 May;7(5):335-6.
- Edgar RC. Search and clustering orders of magnitude faster than BLAST.. Bioinformatics 2010 Oct 1;26(19):2460-1.
- DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB.. Appl Environ Microbiol 2006 Jul;72(7):5069-72.
- Price MN, Dehal PS, Arkin AP. FastTree 2--approximately maximum-likelihood trees for large alignments.. PLoS One 2010 Mar 10;5(3):e9490.
- Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy.. Appl Environ Microbiol 2007 Aug;73(16):5261-7.
- McMurdie PJ, Holmes S. Waste not, want not: why rarefying microbiome data is inadmissible.. PLoS Comput Biol 2014 Apr;10(4):e1003531.
- Lozupone CA, Hamady M, Kelley ST, Knight R. Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities.. Appl Environ Microbiol 2007 Mar;73(5):1576-85.
- Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences.. Nat Biotechnol 2013 Sep;31(9):814-21.
- Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. Metagenomic biomarker discovery and explanation.. Genome Biol 2011 Jun 24;12(6):R60.
- Kyto encyclopaedia of genes and genome (KEGG) orthologs https://www.genome.jp/kegg/pathway.html Accessed May 2019.
- Theodorou MK, Williams BA, Dhaona MS, McAllan AB, France J. A simple gas production method using a pressure transducer to determine the fermentation kinetics of ruminant feeds. Anim Feed Sci Technol 1994;48:185–197.
- Müller CE, von Rosen D, Uden P. Effect of forage conservation method of microbial flora and fermentation pattern in forage and in equine colon and faeces. Livest Sci 2008;119:116–128.
- Lowman RS, Theodorou MK, Longland AC, Cí·¯ord D. A comparison of equine faeces or caecal digesta as sources of inoculum for in vitro fermentation studies using the pressure transducer technique. Anim Sci 1996;62:683.
- Ross GJS. MLP Maximum Likelihood Programme. Oxford: Numerical algorithms group; 1987.
- Gowan AA, Downey G, Esquerre C, O'Donnell CP. Preventing over-fitting in PLS calibration models of near-infrared spectroscopy data using regression coefficients. J Chemother 2010;25(7):375–381.
- Benjamini Y, Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J Roy Stat Soc 1995;57(1):289–300.
- Trygg J, Holmes E, Lundstedt T. Chemometrics in metabonomics.. J Proteome Res 2007 Feb;6(2):469-79.
Citations
This article has been cited 8 times.- Stummer M, Frisch V, Glitz F, Hinney B, Spergser J, Krücken J, Diekmann I, Dimmel K, Riedel C, Cavalleri JV, Rümenapf T, Joachim A, Lyrakis M, Auer A. Presence of Equine and Bovine Coronaviruses, Endoparasites, and Bacteria in Fecal Samples of Horses with Colic.. Pathogens 2023 Aug 15;12(8).
- Boisseau M, Dhorne-Pollet S, Bars-Cortina D, Courtot É, Serreau D, Annonay G, Lluch J, Gesbert A, Reigner F, Sallé G, Mach N. Species interactions, stability, and resilience of the gut microbiota - Helminth assemblage in horses.. iScience 2023 Feb 17;26(2):106044.
- Żak-Bochenek A, Bajzert J, Sambor D, Siwińska N, Szponar B, Łaczmański Ł, Żebrowska P, Czajkowska A, Karczewski M, Chełmońska-Soyta A. Homeostasis of the Intestinal Mucosa in Healthy Horses-Correlation between the Fecal Microbiome, Secretory Immunoglobulin A and Fecal Egg Count.. Animals (Basel) 2022 Nov 10;12(22).
- Simões J, Batista M, Tilley P. The Immune Mechanisms of Severe Equine Asthma-Current Understanding and What Is Missing.. Animals (Basel) 2022 Mar 16;12(6).
- Qi L, Lian CA, Zhu FC, Shi M, He LS. Comparative Analysis of Intestinal Microflora Between Two Developmental Stages of Rimicaris kairei, a Hydrothermal Shrimp From the Central Indian Ridge.. Front Microbiol 2021;12:802888.
- Hu D, Yang J, Qi Y, Li B, Li K, Mok KM. Metagenomic Analysis of Fecal Archaea, Bacteria, Eukaryota, and Virus in Przewalski's Horses Following Anthelmintic Treatment.. Front Vet Sci 2021;8:708512.
- Sallé G, Canlet C, Cortet J, Koch C, Malsa J, Reigner F, Riou M, Perrot N, Blanchard A, Mach N. Integrative biology defines novel biomarkers of resistance to strongylid infection in horses.. Sci Rep 2021 Jul 12;11(1):14278.
- Slater R, Frau A, Hodgkinson J, Archer D, Probert C. A Comparison of the Colonic Microbiome and Volatile Organic Compound Metabolome of Anoplocephala perfoliata Infected and Non-Infected Horses: A Pilot Study.. Animals (Basel) 2021 Mar 9;11(3).
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists