Current Understanding of Equine Gut Dysbiosis and Microbiota Manipulation Techniques: Comparison with Current Knowledge in Other Species.
- Journal Article
- Review
Summary
The article reviews the current understanding of horses’ intestinal microbiota, its role in various conditions, and the impact of various influencing factors. It also explores effective techniques to manipulate gut microbiota in horses for preventative or therapeutic use.
Importance of Intestinal Microbiota in Horses
The researchers stress the significant role that gut bacteria play in a horse’s overall health and metabolism. The gut microbiota assists in food digestion and absorption, produces vitamins, and competes with harmful bacteria to maintain a healthy gut environment.
- Various factors, including age, diet, antibiotic use, and geographic location, influence the composition of this microbiota.
- High variability of fecal microbiota in horses makes it difficult to establish a clear definition for dysbiosis (an imbalance or maladaptation of the gut microbiota).
- While a clear cause-effect relationship between gut dysbiosis in horses and diseases hasn’t yet been proven, research suggests a potential link between dysbiosis and conditions such as colitis and asthma.
Techniques to Manipulate Gut Microbiota
The article explores several ways to modify a horse’s gut microbiota. The efficacy of these techniques is currently under investigation as promising tools to prevent or treat diseases like antibiotic-induced colitis.
- Prebiotics, substances that generate beneficial gut bacteria, can be used to influence the composition of the intestinal microbiota.
- Probiotics, or live bacteria and yeasts, can be administered to horses to positively affect the gut environment.
- Fecal microbiota transplantation, transferring fecal bacteria from a healthy donor horse to a recipient, is another potential method to restore a balanced gut microbiota.
Future Research Scope
The review emphasizes the need for more research on the microbial ecosystem in a horse’s gut, especially its links to health and disease. It also calls for better techniques to detect dysbiosis and more effective microbiota manipulation methods, which will be invaluable for managing various health conditions in horses.
Cite This Article
Publication
Researcher Affiliations
- Department of Veterinary Biomedical Sciences, Université de Montréal, Saint-Hyacinthe, QC J2S 2M2, Canada.
- Department of Clinical Sciences, Université de Montréal, Saint-Hyacinthe, QC J2S 2M2, Canada.
- Department of Clinical Sciences, Université de Montréal, Saint-Hyacinthe, QC J2S 2M2, Canada.
- Department of Veterinary Biomedical Sciences, Université de Montréal, Saint-Hyacinthe, QC J2S 2M2, Canada.
Conflict of Interest Statement
References
- Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T. A human gut microbial gene catalogue established by metagenomic sequencing.. Nature 2010;464:59–65.
- Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome.. Nature 2012;486:207–214.
- Gill SR, Pop M, DeBoy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, Gordon JI, Relman DA, Fraser-Liggett CM, Nelson KE. Metagenomic Analysis of the Human Distal Gut Microbiome.. Science 2006;312:1355–1359.
- Dave M, Higgins PD, Middha S, Rioux KP. The human gut microbiome: Current knowledge, challenges, and future directions.. Transl. Res. 2012;160:246–257.
- Marchesi JR, Ravel J. The vocabulary of microbiome research: A proposal.. Microbiome 2015;3:31.
- Frati F, Salvatori C, Incorvaia C, Bellucci A, Di Cara G, Marcucci F, Esposito S. The Role of the Microbiome in Asthma: The Gut–Lung Axis.. Int. J. Mol. Sci. 2019;20:123.
- Goulet O. Potential role of the intestinal microbiota in programming health and disease.. Nutr. Rev. 2015;73((Suppl. 1)):32–40.
- Martin-Gallausiaux C, Marinelli L, Blottière HM, Larraufie P, Lapaque N. SCFA: Mechanisms and functional importance in the gut.. Proc. Nutr. Soc. 2021;80:37–49.
- Hou K, Wu ZX, Chen XY, Wang JQ, Zhang D, Xiao C, Zhu D, Koya JB, Wei L, Li J. Microbiota in health and diseases.. Signal Transduct. Target. Ther. 2022;7:135.
- Fong W, Li Q, Yu J. Gut microbiota modulation: A novel strategy for prevention and treatment of colorectal cancer.. Oncogene 2020;39:4925–4943.
- Liu X, Cao S, Zhang X. Modulation of Gut Microbiota–Brain Axis by Probiotics, Prebiotics, and Diet.. J. Agric. Food Chem. 2015;63:7885–7895.
- Martínez-González AE, Andreo-Martínez P. Prebiotics, probiotics and fecal microbiota transplantation in autism: A systematic review.. Rev. Psiquiatr. Salud. Ment. 2020;13:150–164.
- Costa MC, Weese JS. Understanding the Intestinal Microbiome in Health and Disease.. Veter. Clin. N. Am. Equine Pract. 2018;34:1–12.
- Di Pietro R, Arroyo LG, Leclere M, Costa MC. Species-Level Gut Microbiota Analysis after Antibiotic-Induced Dysbiosis in Horses.. Animals 2021;11:2859.
- Costa MC, Weese JS. The equine intestinal microbiome.. Anim. Health Res. Rev. 2012;13:121–128.
- Ericsson AC, Johnson PJ, Lopes MA, Perry SC, Lanter HR. A Microbiological Map of the Healthy Equine Gastrointestinal Tract.. PLoS ONE 2016;11:e0166523.
- Julliand V, Grimm P. HORSE SPECIES SYMPOSIUM: The microbiome of the horse hindgut: History and current knowledge.. J. Anim. Sci. 2016;94:2262–2274.
- Gilroy R, Leng J, Ravi A, Adriaenssens EM, Oren A, Baker D, La Ragione RM, Proudman C, Pallen MJ. Metagenomic investigation of the equine faecal microbiome reveals extensive taxonomic diversity.. PeerJ 2022;10:e13084.
- Daly K, Stewart CS, Flint HJ, Shirazi-Beechey SP. Bacterial diversity within the equine large intestine as revealed by molecular analysis of cloned 16S rRNA genes.. FEMS Microbiol. Ecol. 2001;38:141–151.
- Argenzio R, Southworth M, Stevens CE, Hume ID, Argenzio RA, Lowe JE, Stevens CE. Sites of organic acid production and absorption in the equine gastrointestinal tract.. Am. J. Physiol. Content. 1974;226:1043–1050.
- Belkaid Y, Hand TW. Role of the Microbiota in Immunity and inflammation.. Cell 2014;157:121–141.
- Schamberger GP, Diez-Gonzalez F. Selection of recently isolated colicinogenic Escherichia coli strains inhibitory to Escherichia coli O157:H7.. J. Food Prot. 2002;65:1381–1387.
- Allam-Ndoul B, Castonguay-Paradis S, Veilleux A. Gut Microbiota and Intestinal Trans-Epithelial Permeability.. Int. J. Mol. Sci. 2020;21:6402.
- Di Mauro A, Neu J, Riezzo G, Raimondi F, Martinelli D, Francavilla R, Indrio F. Gastrointestinal function development and microbiota.. Ital. J. Pediatr. 2013;39:15.
- Sommer F, Bäckhed F. The gut microbiota—Masters of host development and physiology.. Nat. Rev. Microbiol. 2013;11:227–238.
- Peng L, Li ZR, Green RS, Holzmanr IR, Lin J. Butyrate Enhances the Intestinal Barrier by Facilitating Tight Junction Assembly via Activation of AMP-Activated Protein Kinase in Caco-2 Cell Monolayers.. J. Nutr. 2009;139:1619–1625.
- 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;49:489–500.
- Mach N, Ruet A, Clark A, Bars-Cortina D, Ramayo-Caldas Y, Crisci E, Pennarun S, Dhorne-Pollet S, Foury A, Moisan MP. Priming for welfare: Gut microbiota is associated with equitation conditions and behavior in horse athletes.. Sci. Rep. 2020;10:8311.
- Bulmer LS, Murray JA, Burns NM, Garber A, Wemelsfelder F, McEwan NR, Hastie PM. High-starch diets alter equine faecal microbiota and increase behavioural reactivity.. Sci. Rep. 2019;9:18621.
- Plancade S, Clark A, Philippe C, Helbling JC, Moisan MP, Esquerré D, Le Moyec L, Robert C, Barrey E, Mach N. Unraveling the effects of the gut microbiota composition and function on horse endurance physiology.. Sci. Rep. 2019;9:9620.
- Julliand V, Grimm P. The Impact of Diet on the Hindgut Microbiome.. J. Equine Veter. Sci. 2017;52:23–28.
- Garber A, Hastie P, Murray JA. Factors Influencing Equine Gut Microbiota: Current Knowledge.. J. Equine Veter. Sci. 2020;88:102943.
- Hesta M, Costa M. How Can Nutrition Help with Gastrointestinal Tract–Based Issues?. Veter. Clin. N. Am. Equine Pract. 2021;37:63–87.
- Muhonen S, Connysson M, Lindberg JE, Julliand V, Bertilsson J, Jansson A. Effects of crude protein intake from grass silage-only diets on the equine colon ecosystem after an abrupt feed change1.. J. Anim. Sci. 2008;86:3465–3472.
- Muhonen S, Julliand V, Lindberg JE, Bertilsson J, Jansson A. Effects on the equine colon ecosystem of grass silage and haylage diets after an abrupt change from hay1.. J. Anim. Sci. 2009;87:2291–2298.
- Fernandes KA, Kittelmann S, Rogers CW, Gee EK, Bolwell CF, Bermingham EN, Thomas DG. Faecal microbiota of forage-fed horses in New Zealand and the population dynamics of microbial communities following dietary change.. PLoS ONE 2014;9:e112846.
- 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;107:989–995.
- Zhu Y, Wang X, Deng L, Chen S, Zhu C, Li J. Effects of Pasture Grass, Silage, and Hay Diet on Equine Fecal Microbiota.. Animals 2021;11:1330.
- Warzecha CM, Coverdale JA, Janecka JE, Leatherwood JL, Pinchak WE, Wickersham TA, McCann JC. Influence of short-term dietary starch inclusion on the equine cecal microbiome.. J. Anim. Sci. 2017;95:5077–5090.
- Al Jassim RA, Andrews FM. The bacterial community of the horse gastrointestinal tract and its relation to fermentative acidosis, laminitis, colic, and stomach ulcers.. Veter. Clin. N. Am. Equine Pract. 2009;25:199–215.
- Destrez A, Grimm P, Cézilly F, Julliand V. Changes of the hindgut microbiota due to high-starch diet can be associated with behavioral stress response in horses.. Physiol. Behav. 2015;149:159–164.
- Han H, Yi B, Zhong R, Wang M, Zhang S, Ma J, Yin Y, Yin J, Chen L, Zhang H. From gut microbiota to host appetite: Gut microbiota-derived metabolites as key regulators.. Microbiome 2021;9:162.
- van de Wouw M, Schellekens H, Dinan TG, Cryan JF. Microbiota-Gut-Brain Axis: Modulator of Host Metabolism and Appetite.. J. Nutr. 2017;147:727–745.
- Lyte M, Chapel A, Lyte JM, Ai Y, Proctor A, Jane JL, Phillips GJ. Resistant Starch Alters the Microbiota-Gut Brain Axis: Implications for Dietary Modulation of Behavior.. PLoS ONE 2016;11:e0146406.
- Proudman C, Darby A, Escalona E. Faecal Microbiome of the Thoroughbred Racehorse and Its Response to Dietary Amylase Supplementation.. Equine Veter. J. 2014;46:35.
- Proudman CJ, Hunter JO, Darby AC, Escalona EE, Batty C, Turner C. Characterisation of the faecal metabolome and microbiome of Thoroughbred racehorses.. Equine Veter. J. 2015;47:580–586.
- Earing JE, Durig AC, Gellin GL, Lawrence LM, Flythe MD. Bacterial Colonization of the Equine Gut; Comparison of Mare and Foal Pairs by PCR-DGGE.. Adv. Microbiol. 2012;2:79–86.
- Costa MC, Stämpfli HR, Allen-Vercoe E, Weese JS. Development of the faecal microbiota in foals.. Equine Veter. J. 2016;48:681–688.
- Husso A, Jalanka J, Alipour MJ, Huhti P, Kareskoski M, Pessa-Morikawa T, Iivanainen A, Niku M. The composition of the perinatal intestinal microbiota in horse.. Sci. Rep. 2020;10:441.
- Quercia S, Freccero F, Castagnetti C, Soverini M, Turroni S, Biagi E, Rampelli S, Lanci A, Mariella J, Chinellato E. Early colonisation and temporal dynamics of the gut microbial ecosystem in Standardbred foals.. Equine Veter. J. 2019;51:231–237.
- Faubladier C, Sadet-Bourgeteau S, Philippeau C, Jacotot E, Julliand V. Molecular monitoring of the bacterial community structure in foal feces pre- and post-weaning.. Anaerobe 2014;25:61–66.
- Lindenberg F, Krych L, Kot W, Fielden J, Frøkiær H, van Galen G, Nielsen DS, Hansen AK. Development of the equine gut microbiota.. Sci. Rep. 2019;9:14427.
- Mach N, Foury A, Kittelmann S, Reigner F, Moroldo M, Ballester M, Esquerré D, Rivière J, Sallé G, Gérard P. The Effects of Weaning Methods on Gut Microbiota Composition and Horse Physiology.. Front. Physiol. 2017;8:535.
- Dougal K, de la Fuente G, Harris PA, Girdwood SE, Pinloche E, Geor RJ, Nielsen BD, Schott HC, Elzinga S, Newbold CJ. Characterisation of the Faecal Bacterial Community in Adult and Elderly Horses Fed a High Fibre, High Oil or High Starch Diet Using 454 Pyrosequencing.. PLoS ONE 2014;9:e87424.
- Biagi E, Nylund L, Candela M, Ostan R, Bucci L, Pini E, Nikkïla J, Monti D, Satokari R, Franceschi C. Through Ageing, and Beyond: Gut Microbiota and Inflammatory Status in Seniors and Centenarians.. PLoS ONE 2010;5:e10667.
- 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;8:8510.
- Antwis RE, Lea JMD, Unwin B, Shultz S. Gut microbiome composition is associated with spatial structuring and social interactions in semi-feral Welsh Mountain ponies.. Microbiome 2018;6:207.
- Ang L, Vinderola G, Endo A, Kantanen J, Jingfeng C, Binetti A, Burns P, Qingmiao S, Suying D, Zujiang Y. Gut Microbiome Characteristics in feral and domesticated horses from different geographic locations.. Commun. Biol. 2022;5:172.
- Arnold CE, Pilla R, Chaffin MK, Leatherwood JL, Wickersham TA, Callaway TR, Lawhon SD, Lidbury JA, Steiner JM, Suchodolski JS. The effects of signalment, diet, geographic location, season, and colitis associated with antimicrobial use or Salmonella infection on the fecal microbiome of horses.. J. Veter. Intern. Med. 2021;35:2437–2448.
- Ayoub C, Arroyo LG, Renaud D, Weese JS, Gomez DE. Fecal Microbiota Comparison Between Healthy Teaching Horses and Client-Owned Horses.. J. Equine Veter. Sci. 2022;118:104105.
- Kaiser-Thom S, Hilty M, Axiak S, Gerber V. The skin microbiota in equine pastern dermatitis: A case-control study of horses in Switzerland.. Veter- Dermatol. 2021;32:646-e172.
- Pagan JD, Harris P, Brewster-Barnes T, Duren SE, Jackson SG. Exercise affects digestibility and rate of passage of all-forage and mixed diets in thoroughbred horses.. J. Nutr. 1998;128((Suppl. 12)):2704S–2707S.
- de Almeida MLM, Feringer WH, Carvalho JRG, Rodrigues IM, Jordão LR, Fonseca MG, de Rezende ASC, Neto AdQ, Weese JS, da Costa MC. Intense Exercise and Aerobic Conditioning Associated with Chromium or L-Carnitine Supplementation Modified the Fecal Microbiota of Fillies.. PLoS ONE 2016;11:e0167108.
- Janabi A, Biddle A, Klein D, McKeever K. The effects of acute strenuous exercise on the faecal microbiota in Standardbred racehorses.. Comp. Exerc. Physiol. 2017;13:13–24.
- Le Moyec L, Robert C, Triba MN, Billat VL, Mata X, Schibler L, Barrey E. Protein Catabolism and High Lipid Metabolism Associated with Long-Distance Exercise Are Revealed by Plasma NMR Metabolomics in Endurance Horses.. PLoS ONE 2014;9:e90730.
- Mach N, Plancade S, Pacholewska A, Lecardonnel J, Rivière J, Moroldo M, Vaiman A, Morgenthaler C, Beinat M, Nevot A. Integrated mRNA and miRNA expression profiling in blood reveals candidate biomarkers associated with endurance exercise in the horse.. Sci. Rep. 2016;6:22932.
- Scheiman J, Luber JM, Chavkin TA, MacDonald T, Tung A, Pham LD, Wibowo MC, Wurth RC, Punthambaker S, Tierney BT. Meta-omics analysis of elite athletes identifies a performance-enhancing microbe that functions via lactate metabolism.. Nat. Med. 2019;25:1104–1109.
- 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 Veter. J. 2016;48:595–602.
- Perry E, Cross TWL, Francis JM, Holscher HD, Clark SD, Swanson KS. Effect of Road Transport on the Equine Cecal Microbiota.. J. Equine Veter. Sci. 2018;68:12–20.
- 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 supplementation1.. J. Anim. Sci. 2013;91:1736–1744.
- Jalanka-Tuovinen J, Salonen A, Nikkilä J, Immonen O, Kekkonen R, Lahti L, Palva A, de Vos WM. Intestinal microbiota in healthy adults: Temporal analysis reveals individual and common core and relation to intestinal symp-toms.. PLoS ONE 2011;6:e23035.
- 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 2021;11:1807.
- 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 Veter. J. 2013;45:154–158.
- Harlow BE, Lawrence LM, Flythe MD. Diarrhea-associated pathogens, lactobacilli and cellulolytic bacteria in equine feces: Responses to antibiotic challenge.. Veter. Microbiol. 2013;166:225–232.
- 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 Veter. Res. 2015;11:19.
- Liepman RS, Swink JM, Habing GG, Boyaka PN, Caddey B, Costa M, Gomez DE, Toribio RE. Effects of Intravenous Antimicrobial Drugs on the Equine Fecal Microbiome.. Animals 2022;12:1013.
- Gomez D, Toribio R, Caddey B, Costa M, Vijan S, Dembek K. Longitudinal effects of oral administration of antimicrobial drugs on fecal microbiota of horses.. J. Veter. Intern. Med. 2023;37:2562–2572.
- Liepman R.S. Alterations in the Fecal Microbiome of Healthy Horses in Response to Antibiotic Treatment. The Ohio State University. 2015. [(accessed on 20 April 2023)]. Available online: https://etd.ohiolink.edu/apexprod/rws_olink/r/1501/10?clear=10&p10_accession_num=osᐩ004228.
- Dethlefsen L, Relman DA. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation.. Proc. Natl. Acad. Sci. USA 2011;108((Suppl. 1)):4554–4561.
- Pilla R, Gaschen FP, Barr JW, Olson E, Honneffer J, Guard BC, Blake AB, Villanueva D, Khattab MR, AlShawaqfeh MK. Effects of metronidazole on the fecal microbiome and metabolome in healthy dogs.. J. Veter. Intern. Med. 2020;34:1853–1866.
- Di Pietro R, Arroyo LG, Leclere M, Costa M. Effects of concentrated fecal microbiota transplant on the equine fecal microbiota after antibiotic-induced dysbiosis.. Can. J. Vet. Res. 2023;87:85–96.
- Uchida-Fujii E, Niwa H, Senoh M, Kato H, Kinoshita Y, Mita H, Ueno T. Clostridioides difficile infection in thoroughbred horses in Japan from 2010 to 2021.. Sci. Rep. 2023;13:13099.
- Russell SL, Gold MJ, Willing BP, Thorson L, McNagny KM, Finlay BB. Perinatal antibiotic treatment affects murine microbiota, immune responses and allergic asthma.. Gut Microbes 2013;4:158–164.
- Pitter G, Ludvigsson JF, Romor P, Zanier L, Zanotti R, Simonato L, Canova C. Antibiotic exposure in the first year of life and later treated asthma, a population based birth cohort study of 143,000 children.. Eur. J. Epidemiol. 2016;31:85–94.
- Principi N, Esposito S. Antibiotic administration and the development of obesity in children.. Int. J. Antimicrob. Agents. 2016;47:171–177.
- Whitfield-Cargile CM, Chamoun-Emanuelli AM, Cohen ND, Richardson LM, Ajami NJ, Dockery HJ. Differential effects of selective and non-selective cyclooxygenase inhibitors on fecal microbiota in adult horses.. PLoS ONE 2018;13:e0202527.
- Kunz IG, Reed KJ, Metcalf JL, Hassel DM, Coleman RJ, Hess TM, Coleman SJ. Equine Fecal Microbiota Changes Associated With Anthelmintic Administration.. J. Equine Veter. Sci. 2019;77:98–106.
- Sirois R. Ph. D. Thesis. Smith College; Northampton, MA, USA: 2013. Comparison of the Fecal Microbiota of Horses before and after Treatment for Parasitic Helminths: Massively Parallel Sequenc-ing of the V4 Region of the 16S Ribosomal RNA Gene.
- 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:e41484.
- Zakia LS, Gomez DE, Caddey BB, Boerlin P, Surette MG, Arroyo LG. Direct and culture-enriched 16S rRNA sequencing of cecal content of healthy horses and horses with typhlocolitis.. PLoS ONE 2023;18:e0284193.
- Weese JS, Holcombe SJ, Embertson RM, Kurtz KA, Roessner HA, Jalali M, Wismer SE. Changes in the faecal microbiota of mares precede the development of post partum colic.. Equine Veter. J. 2015;47:641–649.
- Elzinga SE, Weese JS, Adams AA. Comparison of the Fecal Microbiota in Horses with Equine Metabolic Syndrome and Metabolically Normal Controls Fed a Similar All-Forage Diet.. J. Equine Veter. Sci. 2016;44:9–16.
- Ayoub C, Arroyo LG, MacNicol JL, Renaud D, Weese JS, Gomez DE. Fecal microbiota of horses with colitis and its association with laminitis and survival during hospitalization.. J. Veter. Intern. Med. 2022;36:2213–2223.
- McKinney CA, Oliveira BCM, Bedenice D, Paradis MR, Mazan M, Sage S, Sanchez A, Widmer G. The fecal microbiota of healthy donor horses and geriatric recipients undergoing fecal microbial transplantation for the treatment of diarrhea.. PLoS ONE 2020;15:e0230148.
- McKinney CA, Bedenice D, Pacheco AP, Oliveira BCM, Paradis MR, Mazan M, Widmer G. Assessment of clinical and microbiota responses to fecal microbial transplantation in adult horses with diarrhea.. PLoS ONE 2021;16:e0244381.
- Arroyo LG, Rossi L, Santos BP, Gomez DE, Surette MG, Costa MC. Luminal and Mucosal Microbiota of the Cecum and Large Colon of Healthy and Diarrheic Horses.. Animals 2020;10:1403.
- Pereira GQ, Gomes LA, Santos IS, Alfieri AF, Weese JS, Costa MC. Fecal microbiota transplantation in puppies with canine parvovirus infection.. J. Veter. Intern. Med. 2018;32:707–711.
- Gomez DE, Arroyo LG, Schoster A, Renaud DL, Kopper JJ, Dunkel B, Byrne D, Toribio RE. Diagnostic approaches, aetiological agents and their associations with short-term survival and laminitis in horses with acute diarrhoea admitted to referral institutions.. Equine Veter. J. 2023:1–11.
- Uzal FA, Navarro MA, Asin J, Henderson EE. Clostridial Diseases of Horses: A Review.. Vaccines 2022;10:318.
- Zakia LS, MacNicol JL, Borges AS, Yu S, Boerlin P, Gomez DE, Surette MG, Arroyo LG. Fecal prevalence of Clostridium innocuum DNA in healthy horses and horses with colitis.. Anaerobe 2023;79:102681.
- Steelman SM, Chowdhary BP, Dowd S, Suchodolski J, Janečka JE. Pyrosequencing of 16S rRNA genes in fecal samples reveals high diversity of hindgut microflora in horses and potential links to chronic laminitis.. BMC Veter. Res. 2012;8:231.
- Leclere M, Costa MC. Fecal microbiota in horses with asthma.. J. Veter. Intern. Med. 2020;34:996–1006.
- Coleman MC, Whitfield-Cargile CM, Madrigal RG, Cohen ND. Comparison of the microbiome, metabolome, and lipidome of obese and non-obese horses.. PLoS ONE 2019;14:e0215918.
- Roth P, Stanley J, Chamoun-Emanuelli A, Whitfield-Cargile C, Coleman M. Fecal extract from obese horses induces an inflammatory response by murine macrophages in vitro.. Am. J. Veter. Res. 2022;83:419–425.
- Górniak W, Cholewińska P, Szeligowska N, Wołoszyńska M, Soroko M, Czyż K. Effect of Intense Exercise on the Level of Bacteroidetes and Firmicutes Phyla in the Digestive System of Thoroughbred Racehorses.. Animals 2021;11:290.
- Costa M, Di Pietro R, Bessegatto JA, Pereira PFV, Stievani FC, Gomes RG, Lisbôa JAN, Weese JS. Evaluation of changes in microbiota after fecal microbiota transplantation in 6 diarrheic horses.. Can. Vet. J. 2021;62:1123–1130.
- Costa M, Silva G, Ramos R, Staempfli H, Arroyo L, Kim P, Weese J. Characterization and comparison of the bacterial microbiota in different gastrointestinal tract compartments in horses.. Veter. J. 2015;205:74–80.
- Roediger WE. The Colonic Epithelium in Ulcerative Colitis: An Energy-Deficiency Disease?. Lancet 1980;316:712–715.
- Corrêa-Oliveira R, Fachi JL, Vieira A, Sato FT, Vinolo MAR. Regulation of immune cell function by short-chain fatty acids.. Clin. Transl. Immunol. 2016;5:e73.
- Ze X, Le Mougen F, Duncan SH, Louis P, Flint HJ. Some are more equal than others.. Gut Microbes 2013;4:236–240.
- Metcalf JL, Song SJ, Morton JT, Weiss S, Seguin-Orlando A, Joly F, Feh C, Taberlet P, Coissac E, Amir A. Evaluating the impact of domestication and captivity on the horse gut microbiome.. Sci. Rep. 2017;7:15497.
- Rodriguez C, Taminiau B, Brévers B, Avesani V, Van Broeck J, Leroux A, Gallot M, Bruwier A, Amory H, Delmée M. Faecal microbiota characterisation of horses using 16 rdna barcoded pyrosequencing, and carriage rate of clostridium difficile at hospital admission.. BMC Microbiol. 2015;15:181.
- Shin NR, Whon TW, Bae JW. Proteobacteria: Microbial signature of dysbiosis in gut microbiota.. Trends Biotechnol. 2015;33:496–503.
- Gomez D, Arroyo L, Costa M, Viel L, Weese J. Characterization of the Fecal Bacterial Microbiota of Healthy and Diarrheic Dairy Calves.. J. Veter. Intern. Med. 2017;31:928–939.
- Devkota S, Wang Y, Musch MW, Leone V, Fehlner-Peach H, Nadimpalli A, Antonopoulos DA, Jabri B, Chang EB. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10−/− mice.. Nature 2012;487:104–108.
- Chaucheyras-Durand F, Sacy A, Karges K, Apper E. Gastro-Intestinal Microbiota in Equines and Its Role in Health and Disease: The Black Box Opens.. Microorganisms 2022;10:2517.
- Trompette A, Gollwitzer ES, Yadava K, Sichelstiel AK, Sprenger N, Ngom-Bru C, Blanchard C, Junt T, Nicod LP, Harris NL. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis.. Nat. Med. 2014;20:159–166.
- Park T, Cheong H, Yoon J, Kim A, Yun Y, Unno T. Comparison of the Fecal Microbiota of Horses with Intestinal Disease and Their Healthy Counterparts.. Veter. Sci. 2021;8:113.
- Magne F, Gotteland M, Gauthier L, Zazueta A, Pesoa S, Navarrete P, Balamurugan R. The Firmicutes/Bacteroidetes Ratio: A Relevant Marker of Gut Dysbiosis in Obese Patients?. Nutrients 2020;12:1474.
- Schwiertz A, Taras D, Schäfer K, Beijer S, Bos NA, Donus C, Hardt PD. Microbiota and SCFA in Lean and Overweight Healthy Subjects.. Obesity 2010;18:190–195.
- Alshawaqfeh MK, Wajid B, Minamoto Y, Markel M, Lidbury JA, Steiner JM, Serpedin E, Suchodolski JS. A dysbiosis index to assess microbial changes in fecal samples of dogs with chronic inflammatory enteropathy.. FEMS Microbiol. Ecol. 2017;93:fix136.
- Sung CH, Marsilio S, Chow B, Zornow KA, Slovak JE, Pilla R, Lidbury JA, Steiner JM, Park SY, Hong MP. Dysbiosis index to evaluate the fecal microbiota in healthy cats and cats with chronic enteropathies.. J. Feline Med. Surg. 2022;24:e1–e12.
- Zmora N, Suez J, Elinav E. You are what you eat: Diet, health and the gut microbiota.. Nat. Rev. Gastroenterol. Hepatol. 2019;16:35–56.
- Bibbò S, Ianiro G, Giorgio V, Scaldaferri F, Masucci L, Gasbarrini A, Cammarota G. The role of diet on gut microbiota composition.. Eur. Rev. Med. Pharmacol. Sci. 2016;20:4742–4749.
- Beam A, Clinger E, Hao L. Effect of Diet and Dietary Components on the Composition of the Gut Microbiota.. Nutrients 2021;13:2795.
- Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PD. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics.. Nat. Rev. Gastroenterol. Hepatol. 2017;14:491–502.
- Klaenhammer TR, Kleerebezem M, Kopp MV, Rescigno M. The impact of probiotics and prebiotics on the immune system.. Nat. Rev. Immunol. 2012;12:728–734.
- Ganguly N, Bhattacharya S, Sesikeran B, Nair G, Ramakrishna B, Sachdev H, Batish V, Kanagasabapathy A, Muthuswamy V, Kathuria S. ICMR-DBT Guidelines for Evaluation of Probiotics in Food.. Indian J. Med. Res. 2011;134:22–25.
- Berreta A, Kopper J. Equine Probiotics-What Are They, Where Are We and Where Do We Need to Go?. J. Equine Veter. Sci. 2022;115:104037.
- Berreta A, Burbick CR, Alexander T, Kogan C, Kopper JJ. Microbial Variability of Commercial Equine Probiotics.. J. Equine Veter. Sci. 2021;106:103728.
- Weese JS, Martin H. Assessment of commercial probiotic bacterial contents and label accuracy.. Can. Vet. J. 2011;52:43–46.
- Schoster A, Guardabassi L, Staempfli HR, Abrahams M, Jalali M, Weese JS. The longitudinal effect of a multi-strain probiotic on the intestinal bacterial microbiota of neonatal foals.. Equine Veter. J. 2016;48:689–696.
- Tanabe S, Suzuki T, Wasano Y, Nakajima F, Kawasaki H, Tsuda T, Nagamine N, Tsurumachi T, Sugaya K, Akita H. Anti-inflammatory and Intestinal Barrier–protective Activities of Commensal Lactobacilli and Bifidobacteria in Thoroughbreds: Role of Probiotics in Diarrhea Prevention in Neonatal Thoroughbreds.. J. Equine Sci. 2014;25:37–43.
- Schoster A, Staempfli H, Abrahams M, Jalali M, Weese J, Guardabassi L. Effect of a probiotic on prevention of diarrhea and Clostridium difficile and Clostridium perfringens shedding in foals.. J. Veter. Intern. Med. 2015;29:925–931.
- Weese JS, Rousseau J. Evaluation of Lactobacillus pentosus WE7 for prevention of diarrhea in neonatal foals.. J. Am. Veter. Med. Assoc. 2005;226:2031–2034.
- Czerucka D, Piche T, Rampal P. Review article: Yeast as probiotics–Saccharomyces boulardii.. Aliment. Pharmacol. Ther. 2007;26:767–778.
- Grimm P, Combes S, Pascal G, Cauquil L, Julliand V. Dietary composition and yeast/microalgae combination supplementation modulate the microbial ecosystem in the caecum, colon and faeces of horses.. Br. J. Nutr. 2020;123:372–382.
- Jouany JP, Medina B, Bertin G, Julliand V. Effect of live yeast culture supplementation on hindgut microbial communities and their polysaccharidase and glycoside hydrolase activities in horses fed a high-fiber or high-starch diet.. J. Anim. Sci. 2009;87:2844–2852.
- Boyle AG, Magdesian KG, Gallop R, Sigdel S, Durando MM. Saccharomyces boulardii viability and efficacy in horses with antimicrobial-induced diarrhoea.. Veter. Rec. 2013;172:128.
- Desrochers AM, Dolente BA, Roy MF, Boston R, Carlisle S. Efficacy of Saccharomyces boulardii for treatment of horses with acute enterocolitis.. J. Am. Veter. Med. Assoc. 2005;227:954–959.
- Harlow BE, Lawrence LM, Harris PA, Aiken GE, Flythe MD. Exogenous lactobacilli mitigate microbial changes associated with grain fermentation (corn, oats, and wheat) by equine fecal microflora ex vivo.. PLoS ONE 2017;12:e0174059.
- Murray JAMD, Brown S, O’Shaughnessy P, Monteiro A, Warren H, Hastie PM. Effect of Live Yeast Culture Supplementation on Fibrolytic and Saccharolytic Bacterial Populations in the Feces of Horses Fed a High-Fiber or High-Starch Diet.. J. Equine Veter. Sci. 2017;51:41–45.
- Taran F, Gobesso A, Gonzaga I, Françoso R, Centini T, Moreira C, Silva L. Effects of different amounts of Saccharomyces cerevisiae supplementation on apparent digestibility and faecal parameters in horses fed high-roughage and high-concentrate diets.. Livest. Sci. 2016;186:29–33.
- Medina B, Girard ID, Jacotot E, Julliand V. Effect of a preparation of Saccharomyces cerevisiae on microbial profiles and fermentation patterns in the large intestine of horses fed a high fiber or a high starch diet1.. J. Anim. Sci. 2002;80:2600–2609.
- Garber A, Hastie PM, Farci V, McGuinness D, Bulmer L, Alzahal O, Murray JMD. The effect of supplementing pony diets with yeast on 2. The faecal microbiome.. Animal 2020;14:2493–2502.
- Perricone V, Sandrini S, Irshad N, Comi M, Lecchi C, Savoini G, Agazzi A. The Role of Yeast Saccharomyces cerevisiae in Supporting Gut Health in Horses: An Updated Review on Its Effects on Digestibility and Intestinal and Fecal Microbiota.. Animals 2022;12:3475.
- Mach N, Midoux C, Leclercq S, Pennarun S, Le Moyec L, Rué O, Robert C, Sallé G, Barrey E. Mining the equine gut metagenome: Poorly-characterized taxa associated with cardiovascular fitness in endurance athletes.. Commun. Biol. 2022;5:1032.
- Sheridan PO, Al Odat M, Scott KP. Establishing genetic manipulation for novel strains of human gut bacteria.. Microbiome Res. Rep. 2023;2:1.
- Shoaf K, Mulvey GL, Armstrong GD, Hutkins RW. Prebiotic galactooligosaccharides reduce adherence of enteropathogenic Escherichia coli to tissue culture cells.. Infect. Immun. 2006;74:6920–6928.
- Monteagudo-Mera A, Rastall RA, Gibson GR, Charalampopoulos D, Chatzifragkou A. Adhesion mechanisms mediated by probiotics and prebiotics and their potential impact on human health.. Appl. Microbiol. Biotechnol. 2019;103:6463–6472.
- Tuniyazi M, He J, Guo J, Li S, Zhang N, Hu X, Fu Y. Changes of microbial and metabolome of the equine hindgut during oligofructose-induced laminitis.. BMC Veter. Res. 2021;17:11.
- Ford T, McAdams ZL, Townsend KS, Martin LM, Johnson PJ, Ericsson AC. Effect of Sugar Beet Pulp on the Composition and Predicted Function of Equine Fecal Microbiota.. Biology 2023;12:1254.
- Paßlack N, Vahjen W, Zentek J. Impact of Dietary Cellobiose on the Fecal Microbiota of Horses.. J. Equine Veter. Sci. 2020;91:103106.
- Glatter M, Borewicz K, Bogert BvD, Wensch-Dorendorf M, Bochnia M, Greef JM, Bachmann M, Smidt H, Breves G, Zeyner A. Modification of the equine gastrointestinal microbiota by Jerusalem artichoke meal supplementation.. PLoS ONE 2019;14:e0220553.
- Bachmann M, Glatter M, Bochnia M, Wensch-Dorendorf M, Greef JM, Breves G, Zeyner A. In Vitro Gas Production from Batch Cultures of Stomach and Hindgut Digesta of Horses Adapted to a Prebiotic Dose of Fructooligosaccharides and Inulin.. J. Equine Veter. Sci. 2020;90:103020.
- Boshuizen B, de Vega CVM, De Maré L, de Meeûs C, de Oliveira JE, Hosotani G, Gansemans Y, Deforce D, Van Nieuwerburgh F, Delesalle C. Effects of Aleurone Supplementation on Glucose-Insulin Metabolism and Gut Microbiome in Untrained Healthy Horses.. Front. Veter. Sci. 2021;8:642809.
- Saeidi E, Yarahmadi HM, Fakhraei J, Mojahedi S. Effect of Feeding Fructooligosaccharides and Enterococcus faecium and Their Interaction on Digestibility, Blood, and Immune Parameters of Adult Horses.. J. Equine Veter. Sci. 2021;99:103410.
- McGilloway M, Manley S, Aho A, Heeringa KN, Whitacre L, Lou Y, Squires EJ, Pearson W. Dietary Fermentation Product of Aspergillus Oryzae Prevents Increases in Gastrointestinal Permeability (‘Leaky Gut’) in Horses Undergoing Combined Transport and Exercise.. Animals 2023;13:951.
- MacNicol JL, Renwick S, Ganobis CM, Allen-Vercoe E, Weese JS, Pearson W. The influence of a probiotic/prebiotic supplement on microbial and metabolic parameters of equine cecal fluid or fecal slurry in vitro.. J. Anim. Sci. 2023;101:skad034.
- Adams VJ, LeBlanc N, Penell J. Results of a Clinical Trial Showing Changes to the Faecal Microbiome in Racing Thoroughbreds after Feeding a Nutritional Supplement.. Veter. Sci. 2023;10:27.
- Lucassen A, Hankel J, Finkler-Schade C, Osbelt L, Strowig T, Visscher C, Schuberth HJ. Feeding a Saccharomyces cerevisiae Fermentation Product (Olimond BB) Does Not Alter the Fecal Microbiota of Thoroughbred Racehorses.. Animals 2022;12:1496.
- Lindenberg FC, Lützhøft DO, Krych L, Fielden J, Kot W, Frøkiær H, van Galen G, Nielsen DS, Hansen AK. An Oligosaccharide Rich Diet Increases Akkermansia spp. Bacteria in the Equine Microbiota.. Front. Microbiol. 2021;12:666039.
- Cehak A, Krägeloh T, Zuraw A, Kershaw O, Brehm R, Breves G. Does prebiotic feeding affect equine gastric health? A study on the effects of prebiotic-induced gastric butyric acid production on mucosal integrity of the equine stomach.. Res. Veter. Sci. 2019;124:303–309.
- Bachmann M, Glatter M, Bochnia M, Greef JM, Breves G, Zeyner A. Degradation of Monosaccharides, Disaccharides, and Fructans in the Stomach of Horses Adapted to a Prebiotic Dose of Fructooligosaccharides and Inulin.. J. Equine Veter. Sci. 2021;105:103731.
- Wambacq WA, van Doorn DA, Rovers-Paap PM, Ducatelle R, Vlaminck L, Lourenço M, Hesta M. Dietary supplementation of micro-encapsulated sodium butyrate in healthy horses: Effect on gut histology and immunohistochemistry parameters.. BMC Veter. Res. 2020;16:121.
- Febvre HP, Rao S, Gindin M, Goodwin NDM, Finer E, Vivanco JS, Lu S, Manter DK, Wallace TC, Weir TL. PHAGE Study: Effects of Supplemental Bacteriophage Intake on Inflammation and Gut Microbiota in Healthy Adults.. Nutrients 2019;11:666.
- Hsu BB, Gibson TE, Yeliseyev V, Liu Q, Lyon L, Bry L, Silver PA, Gerber GK. Dynamic Modulation of the Gut Microbiota and Metabolome by Bacteriophages in a Mouse Model.. Cell Host Microbe. 2019;25:803–814.e5.
- Hvas CL, Dahl Jørgensen SM, Jørgensen SP, Storgaard M, Lemming L, Hansen MM, Erikstrup C, Dahlerup JF. Fecal Microbiota Transplantation Is Superior to Fidaxomicin for Treatment of Recurrent Clostridium difficile Infection.. Gastroenterology 2019;156:1324–1332.e3.
- Cammarota G, Masucci L, Ianiro G, Bibbò S, Dinoi G, Costamagna G, Sanguinetti M, Gasbarrini A. Randomised clinical trial: Faecal microbiota transplantation by colonoscopy vs. vancomycin for the treatment of recurrent Clostridium difficile infection.. Aliment. Pharmacol. Ther. 2015;41:835–843.
- de Bustamante MM, Plummer C, MacNicol J, Gomez D. Impact of Ambient Temperature Sample Storage on the Equine Fecal Microbiota.. Animals 2021;11:819.
- Kopper JJ, Alexander TL, Kogan CJ, Berreta AR, Burbick CR. In Vitro Evaluation of the Effect of Storage at −20 °C and Proximal Gastrointestinal Conditions on Viability of Equine Fecal Microbiota Transplant.. J. Equine Veter. Sci. 2021;98:103360.
- Mullen KR, Yasuda K, Divers TJ, Weese JS. Equine faecal microbiota transplant: Current knowledge, proposed guidelines and future directions.. Equine Veter. Educ. 2018;30:151–160.
- Costa M, Di Pietro R, Arantes J, Ratté M, Leclère M, Arroyo L. Bacterial Viability in Different Preparation Protocols of Fecal Microbiota Transplantation Solution.. J. Veter. Intern. Med. 2022;36:2282–2454.
- Wilson BC, Vatanen T, Cutfield WS, O’Sullivan JM. The Super-Donor Phenomenon in Fecal Microbiota Transplantation.. Front. Cell. Infect. Microbiol. 2019;9:2.
- Kinoshita Y, Niwa H, Uchida-Fujii E, Nukada T, Ueno T. Simultaneous Daily Fecal Microbiota Transplantation Fails to Prevent Metronidazole-Induced Dysbiosis of Equine Gut Microbiota.. J. Equine Veter. Sci. 2022;114:104004.
- Laustsen L, Edwards JE, Hermes GDA, Lúthersson N, van Doorn DA, Okrathok S, Kujawa TJ, Smidt H. Free Faecal Water: Analysis of Horse Faecal Microbiota and the Impact of Faecal Microbial Transplantation on Symptom Severity.. Animals 2021;11:2776.
- Quattrini C, Bozorgmanesh R, Egli P, Magdesian K. Fecal microbiota transplant for treatment of diarrhea in adult hospitalized horses—111 cases (2013–2018). Open Veter. J. 2023;13:1135–1140.
- Weingarden AR, Treiger O, Ulsh L, Limketkai B, Goldenberg D, Okafor P, Sonu I, Stollman N, Neshatian L. Delivery of Fecal Material to Terminal Ileum Is Associated with Long-Term Success of Fecal Microbiota Transplantation.. Dig. Dis. Sci. 2023;68:2006–2014.
- Gough E, Shaikh H, Manges AR. Systematic review of intestinal microbiota transplantation (fecal bacteriotherapy) for recurrent clostridium difficile infection.. Clin. Infect. Dis. 2011;53:994–1002.