Priming for welfare: gut microbiota is associated with equitation conditions and behavior in horse athletes.
Abstract: We simultaneously measured the fecal microbiota and multiple environmental and host-related variables in a cohort of 185 healthy horses reared in similar conditions during a period of eight months. The pattern of rare bacteria varied from host to host and was largely different between two time points. Among a suite of variables examined, equitation factors were highly associated with the gut microbiota variability, evoking a relationship between gut microbiota and high levels of physical and mental stressors. Behavioral indicators that pointed toward a compromised welfare state (e.g. stereotypies, hypervigilance and aggressiveness) were also associated with the gut microbiota, reinforcing the notion for the existence of the microbiota-gut-brain axis. These observations were consistent with the microbiability of behaviour traits (> 15%), illustrating the importance of gut microbial composition to animal behaviour. As more elite athletes suffer from stress, targeting the microbiota offers a new opportunity to investigate the bidirectional interactions within the brain gut microbiota axis.
Publication Date: 2020-05-20 PubMed ID: 32433513PubMed Central: PMC7239938DOI: 10.1038/s41598-020-65444-9Google Scholar: Lookup
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- Journal Article
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Summary
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This research investigates the relationship between the gut microbiota (microorganisms living in intestines) and the physical and mental stress levels in 185 healthy horses over an eight months period. The study suggests that changes in gut microbiota may be associated with equitation factors and certain behavioural indicators, implying a possible connection between the gut and animal behavior, and providing new opportunities to explore the interactions within the brain-gut-microbiota axis.
Research Methodology
- The research was conducted on a cohort of 185 healthy horses, reared in similar conditions over a span of eight months.
- Simultaneous measurements were made of the fecal microbiota and multiple environmental and host-related variables.
- The variability pattern of rare bacteria was examined across host to host and between two time points.
Research Findings
- Among many variables examined, equitation factors (training methods, workload, rider’s skill level, and saddle fit) were strongly associated with gut microbiota variability. This reflects a relationship between gut microbiota and high physical and mental stress in horse athletes.
- Behavioural indicators such as hypervigilance, stereotypies, and aggressiveness that suggest a compromised welfare state were prominently linked with gut microbiota. This goes to strengthen the idea of a microbiota-gut-brain axis, where changes in microbiota could impact behaviour.
- Common behavioural traits were found to be dependent on the microbiotal makeup by over 15%, highlighting the substantial role of gut microbial composition in determining animal behaviour.
Research Implications and Future Directions
- The study provides valuable insights for athletes, especially elite ones, as they often suffer from high stress levels. Understanding the interaction between gut microbiota and stress can offer new avenues for stress management practices.
- The research illuminates the bi-directional interactions within the brain-gut-microbiota axis and its effect on animal behavior, which could pave the way for future research in manipulating microbiota to influence behavior and manage stress.
Cite This Article
APA
Mach N, Ruet A, Clark A, Bars-Cortina D, Ramayo-Caldas Y, Crisci E, Pennarun S, Dhorne-Pollet S, Foury A, Moisan MP, Lansade L.
(2020).
Priming for welfare: gut microbiota is associated with equitation conditions and behavior in horse athletes.
Sci Rep, 10(1), 8311.
https://doi.org/10.1038/s41598-020-65444-9 Publication
Researcher Affiliations
- Animal Genetic and Integrative Biology, INRAE, University of Paris-Saclay, AgroParisTech, 78350, Jouy-en-Josas, France. nuria.mach@inrae.fr.
- PRC, INRAE, CNRS, IFCE, University of Tours, 37380, Nouzilly, France.
- Health Science Department, Open University of Catalonia, 08018, Barcelona, Spain.
- Medicine Department, University of Lleida, 25001, Lleida, Spain.
- Animal Genetic and Integrative Biology, INRAE, University of Paris-Saclay, AgroParisTech, 78350, Jouy-en-Josas, France.
- Animal Breeding and Genetics Program, Institute for Research and Technology in Food and Agriculture (IRTA), Torre Marimon, 08140, Caldes de Montbui, Spain.
- Animal Genetic and Integrative Biology, INRAE, University of Paris-Saclay, AgroParisTech, 78350, Jouy-en-Josas, France.
- Department of Population Health and Pathobiology, College of Veterinary Medicine, North Carolina State University, Raleigh, NC, 27607, USA.
- US UMR 1426, INRAE, Genomic platform, 31326, Castanet-Tolosan, France.
- Animal Genetic and Integrative Biology, INRAE, University of Paris-Saclay, AgroParisTech, 78350, Jouy-en-Josas, France.
- University of Bordeaux, INRAE, NutriNeuro UMR 1286, 33076, Bordeaux, France.
- University of Bordeaux, INRAE, NutriNeuro UMR 1286, 33076, Bordeaux, France.
- PRC, INRAE, CNRS, IFCE, University of Tours, 37380, Nouzilly, France.
MeSH Terms
- Animals
- Behavior, Animal
- Biodiversity
- Cohort Studies
- Environment
- Feces / microbiology
- Female
- Gastrointestinal Microbiome / physiology
- Health Status
- Horses / microbiology
- Horses / physiology
- Male
- Phenotype
- Physical Conditioning, Animal
- Sports
Conflict of Interest Statement
The authors declare no competing interests.
References
This article includes 103 references
- Clemente JC, Ursell LK, Parfrey LW, Knight R. The impact of the gut microbiota on human health: an integrative view.. Cell 2012 Mar 16;148(6):1258-70.
- Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour.. Nat Rev Neurosci 2012 Oct;13(10):701-12.
- Mackie RI, Wilkins CA. Enumeration of anaerobic bacterial microflora of the equine gastrointestinal tract.. Appl Environ Microbiol 1988 Sep;54(9):2155-60.
- 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 Vet Res 2012 Nov 27;8:231.
- Venable EB. Effects of Feeding Management on the Equine Cecal Microbiota. J. Equine Vet. Sci. 2017;49:113–121.
- Mach N, Foury A, Kittelmann S, Reigner F, Moroldo M, Ballester M, Esquerré D, Rivière J, Sallé G, Gérard P, Moisan MP, Lansade L. The Effects of Weaning Methods on Gut Microbiota Composition and Horse Physiology.. Front Physiol 2017;8:535.
- 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.
- Shepherd ML, Swecker WS Jr, Jensen RV, Ponder MA. Characterization of the fecal bacteria communities of forage-fed horses by pyrosequencing of 16S rRNA V4 gene amplicons.. FEMS Microbiol Lett 2012 Jan;326(1):62-8.
- 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.
- 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 Vet J 2015 Nov;47(6):641-9.
- 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.
- Dougal K, Harris PA, Edwards A, Pachebat JA, Blackmore TM, Worgan HJ, Newbold CJ. A comparison of the microbiome and the metabolome of different regions of the equine hindgut.. FEMS Microbiol Ecol 2012 Dec;82(3):642-52.
- 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 Jul 3;9(1):9620.
- 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.
- Sugahara H, Odamaki T, Hashikura N, Abe F, Xiao JZ. Differences in folate production by bifidobacteria of different origins.. Biosci Microbiota Food Health 2015;34(4):87-93.
- Ericsson AC, Johnson PJ, Lopes MA, Perry SC, Lanter HR. A Microbiological Map of the Healthy Equine Gastrointestinal Tract.. PLoS One 2016;11(11):e0166523.
- Nedjadi T, Moran AW, Al-Rammahi MA, Shirazi-Beechey SP. Characterization of butyrate transport across the luminal membranes of equine large intestine.. Exp Physiol 2014 Oct;99(10):1335-47.
- Costa MC, Weese JS. Understanding the Intestinal Microbiome in Health and Disease.. Vet Clin North Am Equine Pract 2018 Apr;34(1):1-12.
- Destrez A, Grimm P, Julliand V. Dietary-induced modulation of the hindgut microbiota is related to behavioral responses during stressful events in horses.. Physiol Behav 2019 Apr 1;202:94-100.
- 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 Oct 1;149:159-64.
- Willing B, Vörös A, Roos S, Jones C, Jansson A, Lindberg JE. Changes in faecal bacteria associated with concentrate and forage-only diets fed to horses in training.. Equine Vet J 2009 Dec;41(9):908-14.
- 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.
- Hansen NC, Avershina E, Mydland LT, Næsset JA, Austbø D, Moen B, Måge I, Rudi K. High nutrient availability reduces the diversity and stability of the equine caecal microbiota.. Microb Ecol Health Dis 2015;26:27216.
- Harlow BE, Donley TM, Lawrence LM, Flythe MD. Effect of starch source (corn, oats or wheat) and concentration on fermentation by equine faecal microbiota in vitro.. J Appl Microbiol 2015 Nov;119(5):1234-44.
- 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.
- Al Jassim RA, Andrews FM. The bacterial community of the horse gastrointestinal tract and its relation to fermentative acidosis, laminitis, colic, and stomach ulcers.. Vet Clin North Am Equine Pract 2009 Aug;25(2):199-215.
- Chapman AM. Acute diarrhea in hospitalized horses.. Vet Clin North Am Equine Pract 2009 Aug;25(2):363-80.
- Båverud V, Gustafsson A, Franklin A, Lindholm A, Gunnarsson A. Clostridium difficile associated with acute colitis in mature horses treated with antibiotics.. Equine Vet J 1997 Jul;29(4):279-84.
- Blikslager AT. Colic Prevention to Avoid Colic Surgery: A Surgeon's Perspective.. J Equine Vet Sci 2019 May;76:1-5.
- 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.
- Janabi AHD, Biddle AS, Klein DJ, McKeever KH. The effects of acute strenuous exercise on the faecal microbiota in Standardbred racehorses. Comp. Exerc. Physiol. 2017;13:13–24.
- Almeida ML, Feringer WH Júnior, Carvalho JR, Rodrigues IM, Jordão LR, Fonseca MG, Carneiro de Rezende AS, de Queiroz Neto A, Weese JS, Costa MC, Lemos EG, Ferraz GC. Intense Exercise and Aerobic Conditioning Associated with Chromium or L-Carnitine Supplementation Modified the Fecal Microbiota of Fillies.. PLoS One 2016;11(12):e0167108.
- 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(3):e90730.
- Mach N, Plancade S, Pacholewska A, Lecardonnel J, Rivière J, Moroldo M, Vaiman A, Morgenthaler C, Beinat M, Nevot A, Robert C, Barrey E. Integrated mRNA and miRNA expression profiling in blood reveals candidate biomarkers associated with endurance exercise in the horse.. Sci Rep 2016 Mar 10;6:22932.
- Mach N, Ramayo-Caldas Y, Clark A, Moroldo M, Robert C, Barrey E, López JM, Le Moyec L. Understanding the response to endurance exercise using a systems biology approach: combining blood metabolomics, transcriptomics and miRNomics in horses.. BMC Genomics 2017 Feb 17;18(1):187.
- Ruet A, Lemarchand J, Parias C, Mach N, Moisan MP, Foury A, Briant C, Lansade L. Housing Horses in Individual Boxes Is a Challenge with Regard to Welfare.. Animals (Basel) 2019 Aug 28;9(9).
- Lansade L, Foury A, Reigner F, Vidament M, Guettier E, Bouvet G, Soulet D, Parias C, Ruet A, Mach N, Lévy F, Moisan MP. Progressive habituation to separation alleviates the negative effects of weaning in the mother and foal.. Psychoneuroendocrinology 2018 Nov;97:59-68.
- Metcalf JL, Song SJ, Morton JT, Weiss S, Seguin-Orlando A, Joly F, Feh C, Taberlet P, Coissac E, Amir A, Willerslev E, Knight R, McKenzie V, Orlando L. Evaluating the impact of domestication and captivity on the horse gut microbiome.. Sci Rep 2017 Nov 14;7(1):15497.
- 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 Nov 22;6(1):207.
- Cooper JJ, Albentosa MJ. Behavioural adaptation in the domestic horse: Potential role of apparently abnormal responses including stereotypic behaviour. Livest. Prod. Sci. 2005;92:177–182.
- Henderson AJ. Don't fence me in: managing psychological well being for elite performance horses.. J Appl Anim Welf Sci 2007;10(4):309-29.
- Ninomiya S, Sato S, Sugawara K. Weaving in stabled horses and its relationship to other behavioural traits. Appl. Anim. Behav. Sci. 2007;106:134–143.
- Rothschild D, Weissbrod O, Barkan E, Kurilshikov A, Korem T, Zeevi D, Costea PI, Godneva A, Kalka IN, Bar N, Shilo S, Lador D, Vila AV, Zmora N, Pevsner-Fischer M, Israeli D, Kosower N, Malka G, Wolf BC, Avnit-Sagi T, Lotan-Pompan M, Weinberger A, Halpern Z, Carmi S, Fu J, Wijmenga C, Zhernakova A, Elinav E, Segal E. Environment dominates over host genetics in shaping human gut microbiota.. Nature 2018 Mar 8;555(7695):210-215.
- Bass D, Stentiford GD, Wang HC, Koskella B, Tyler CR. The Pathobiome in Animal and Plant Diseases.. Trends Ecol Evol 2019 Nov;34(11):996-1008.
- de Steenhuijsen Piters WA, Heinonen S, Hasrat R, Bunsow E, Smith B, Suarez-Arrabal MC, Chaussabel D, Cohen DM, Sanders EA, Ramilo O, Bogaert D, Mejias A. Nasopharyngeal Microbiota, Host Transcriptome, and Disease Severity in Children with Respiratory Syncytial Virus Infection.. Am J Respir Crit Care Med 2016 Nov 1;194(9):1104-1115.
- Jovel J, Patterson J, Wang W, Hotte N, O'Keefe S, Mitchel T, Perry T, Kao D, Mason AL, Madsen KL, Wong GK. Characterization of the Gut Microbiome Using 16S or Shotgun Metagenomics.. Front Microbiol 2016;7:459.
- Pollock J, Glendinning L, Wisedchanwet T, Watson M. The Madness of Microbiome: Attempting To Find Consensus "Best Practice" for 16S Microbiome Studies.. Appl Environ Microbiol 2018 Apr 1;84(7).
- Jousset A, Bienhold C, Chatzinotas A, Gallien L, Gobet A, Kurm V, Küsel K, Rillig MC, Rivett DW, Salles JF, van der Heijden MG, Youssef NH, Zhang X, Wei Z, Hol WH. Where less may be more: how the rare biosphere pulls ecosystems strings.. ISME J 2017 Apr;11(4):853-862.
- 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.
- Art T, Lekeux P. Exercise-induced physiological adjustments to stressful conditions in sports horses. Livest. Prod. Sci. 2005;92:101–111.
- Karl JP, Margolis LM, Madslien EH, Murphy NE, Castellani JW, Gundersen Y, Hoke AV, Levangie MW, Kumar R, Chakraborty N, Gautam A, Hammamieh R, Martini S, Montain SJ, Pasiakos SM. Changes in intestinal microbiota composition and metabolism coincide with increased intestinal permeability in young adults under prolonged physiological stress.. Am J Physiol Gastrointest Liver Physiol 2017 Jun 1;312(6):G559-G571.
- Allen JM, Berg Miller ME, Pence BD, Whitlock K, Nehra V, Gaskins HR, White BA, Fryer JD, Woods JA. Voluntary and forced exercise differentially alters the gut microbiome in C57BL/6J mice.. J Appl Physiol (1985) 2015 Apr 15;118(8):1059-66.
- Clark A, Mach N. Exercise-induced stress behavior, gut-microbiota-brain axis and diet: a systematic review for athletes.. J Int Soc Sports Nutr 2016;13:43.
- Rigottier-Gois L. Dysbiosis in inflammatory bowel diseases: the oxygen hypothesis.. ISME J 2013 Jul;7(7):1256-61.
- Albenberg L, Esipova TV, Judge CP, Bittinger K, Chen J, Laughlin A, Grunberg S, Baldassano RN, Lewis JD, Li H, Thom SR, Bushman FD, Vinogradov SA, Wu GD. Correlation between intraluminal oxygen gradient and radial partitioning of intestinal microbiota.. Gastroenterology 2014 Nov;147(5):1055-63.e8.
- Jiang H, Ling Z, Zhang Y, Mao H, Ma Z, Yin Y, Wang W, Tang W, Tan Z, Shi J, Li L, Ruan B. Altered fecal microbiota composition in patients with major depressive disorder.. Brain Behav Immun 2015 Aug;48:186-94.
- Rogers GB, Keating DJ, Young RL, Wong ML, Licinio J, Wesselingh S. From gut dysbiosis to altered brain function and mental illness: mechanisms and pathways.. Mol Psychiatry 2016 Jun;21(6):738-48.
- Kelly JR, Borre Y, O' Brien C, Patterson E, El Aidy S, Deane J, Kennedy PJ, Beers S, Scott K, Moloney G, Hoban AE, Scott L, Fitzgerald P, Ross P, Stanton C, Clarke G, Cryan JF, Dinan TG. Transferring the blues: Depression-associated gut microbiota induces neurobehavioural changes in the rat.. J Psychiatr Res 2016 Nov;82:109-18.
- Bharwani A, Mian MF, Surette MG, Bienenstock J, Forsythe P. Oral treatment with Lactobacillus rhamnosus attenuates behavioural deficits and immune changes in chronic social stress.. BMC Med 2017 Jan 11;15(1):7.
- Hsiao EY, McBride SW, Hsien S, Sharon G, Hyde ER, McCue T, Codelli JA, Chow J, Reisman SE, Petrosino JF, Patterson PH, Mazmanian SK. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders.. Cell 2013 Dec 19;155(7):1451-63.
- Hemmann KE, Koho NM, Vainio OM, Raekallio MR. Effects of feed on plasma leptin and ghrelin concentrations in crib-biting horses.. Vet J 2013 Oct;198(1):122-6.
- Lach G, Schellekens H, Dinan TG, Cryan JF. Anxiety, Depression, and the Microbiome: A Role for Gut Peptides.. Neurotherapeutics 2018 Jan;15(1):36-59.
- Cogan TA, Thomas AO, Rees LE, Taylor AH, Jepson MA, Williams PH, Ketley J, Humphrey TJ. Norepinephrine increases the pathogenic potential of Campylobacter jejuni.. Gut 2007 Aug;56(8):1060-5.
- Lyte M, Vulchanova L, Brown DR. Stress at the intestinal surface: catecholamines and mucosa-bacteria interactions.. Cell Tissue Res 2011 Jan;343(1):23-32.
- Johnson KV, Foster KR. Why does the microbiome affect behaviour?. Nat Rev Microbiol 2018 Oct;16(10):647-655.
- Hemmann K, Ahonen S, Raekallio M, Vainio O, Lohi H. Exploration of known stereotypic behaviour-related candidate genes in equine crib-biting.. Animal 2014 Mar;8(3):347-53.
- Staiger EA, Albright JD, Brooks SA. Genome-wide association mapping of heritable temperament variation in the Tennessee Walking Horse.. Genes Brain Behav 2016 Jun;15(5):514-26.
- Hiippala K, Jouhten H, Ronkainen A, Hartikainen A, Kainulainen V, Jalanka J, Satokari R. The Potential of Gut Commensals in Reinforcing Intestinal Barrier Function and Alleviating Inflammation.. Nutrients 2018 Jul 29;10(8).
- Li XN, Chen L, Luo B, Li X, Wang CY, Zou W, Zhang P, You Y, Tang XQ. Hydrogen sulfide attenuates chronic restrain stress-induced cognitive impairment by upreglulation of Sirt1 in hippocampus.. Oncotarget 2017 Nov 21;8(59):100396-100410.
- Sarrafchi A, Blokhuis HJ. Equine stereotypic behaviors: Causation, occurrence, and prevention. J. Vet. Behav. Clin. Appl. Res. 2013;8:386–394.
- Hemberger S, Pedrolli DB, Stolz J, Vogl C, Lehmann M, Mack M. RibM from Streptomyces davawensis is a riboflavin/roseoflavin transporter and may be useful for the optimization of riboflavin production strains.. BMC Biotechnol 2011 Dec 2;11:119.
- Hanstock TL, Clayton EH, Li KM, Mallet PE. Anxiety and aggression associated with the fermentation of carbohydrates in the hindgut of rats.. Physiol Behav 2004 Sep 15;82(2-3):357-68.
- Chen L, Shen Y, Wang C, Ding L, Zhao F, Wang M, Fu J, Wang H. Megasphaera elsdenii Lactate Degradation Pattern Shifts in Rumen Acidosis Models.. Front Microbiol 2019;10:162.
- Kubasova T, Davidova-Gerzova L, Merlot E, Medvecky M, Polansky O, Gardan-Salmon D, Quesnel H, Rychlik I. Housing Systems Influence Gut Microbiota Composition of Sows but Not of Their Piglets.. PLoS One 2017;12(1):e0170051.
- Martin CR, Osadchiy V, Kalani A, Mayer EA. The Brain-Gut-Microbiome Axis.. Cell Mol Gastroenterol Hepatol 2018;6(2):133-148.
- Carroll CL, Huntington PJ. Body condition scoring and weight estimation of horses.. Equine Vet J 1988 Jan;20(1):41-5.
- Martin-rosset W. Equine Nutrition: INRA nutrient requirements, recommended allowances and feed tables. .
- Martin-Rosset W, Vermorel M, Doreau M, Tisserand JL, Andrieu J. The French horse feed evaluation systems and recommended allowances for energy and protein. Livest. Prod. Sci. 1994;40:37–56.
- Raynaud JP. [Study of the efficiency of a quantitative coproscopic technic for the routine diagnosis and control of parasitic infestations of cattle, sheep, horses and swine].. Ann Parasitol Hum Comp 1970 May-Jun;45(3):321-42.
- Caporaso JG. correspondence QIIME allows analysis of high- throughput community sequencing data Intensity normalization improves color calling in SOLiD sequencing. Nat. Publ. Gr. 2010;7:335–336.
- Rideout JR, He Y, Navas-Molina JA, Walters WA, Ursell LK, Gibbons SM, Chase J, McDonald D, Gonzalez A, Robbins-Pianka A, Clemente JC, Gilbert JA, Huse SM, Zhou HW, Knight R, Caporaso JG. Subsampled open-reference clustering creates consistent, comprehensive OTU definitions and scales to billions of sequences.. PeerJ 2014;2:e545.
- 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.
- Edgar RC. Search and clustering orders of magnitude faster than BLAST.. Bioinformatics 2010 Oct 1;26(19):2460-1.
- Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection.. Bioinformatics 2011 Aug 15;27(16):2194-200.
- Price MN, Dehal PS, Arkin AP. FastTree 2--approximately maximum-likelihood trees for large alignments.. PLoS One 2010 Mar 10;5(3):e9490.
- McMurdie PJ, Holmes S. Phyloseq: a bioconductor package for handling and analysis of high-throughput phylogenetic sequence data.. Pac Symp Biocomput 2012;:235-46.
- Dixon P. VEGAN, a package of R functions for community ecology. J. Veg. Sci. 2003;14:927.
- Lahti L, Shetty S. Tools for microbiome analysis in R. (2017).
- Bates D, Maechler M, Bolker B, Walker S. Fitting Linear Mixed-Effects Models Using lme4. J. Stat. Softw. 2015;67:1–48.
- Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto JM, Bertalan M, Borruel N, Casellas F, Fernandez L, Gautier L, Hansen T, Hattori M, Hayashi T, Kleerebezem M, Kurokawa K, Leclerc M, Levenez F, Manichanh C, Nielsen HB, Nielsen T, Pons N, Poulain J, Qin J, Sicheritz-Ponten T, Tims S, Torrents D, Ugarte E, Zoetendal EG, Wang J, Guarner F, Pedersen O, de Vos WM, Brunak S, Doré J, Antolín M, Artiguenave F, Blottiere HM, Almeida M, Brechot C, Cara C, Chervaux C, Cultrone A, Delorme C, Denariaz G, Dervyn R, Foerstner KU, Friss C, van de Guchte M, Guedon E, Haimet F, Huber W, van Hylckama-Vlieg J, Jamet A, Juste C, Kaci G, Knol J, Lakhdari O, Layec S, Le Roux K, Maguin E, Mérieux A, Melo Minardi R, M'rini C, Muller J, Oozeer R, Parkhill J, Renault P, Rescigno M, Sanchez N, Sunagawa S, Torrejon A, Turner K, Vandemeulebrouck G, Varela E, Winogradsky Y, Zeller G, Weissenbach J, Ehrlich SD, Bork P. Enterotypes of the human gut microbiome.. Nature 2011 May 12;473(7346):174-80.
- Ding T, Schloss PD. Dynamics and associations of microbial community types across the human body.. Nature 2014 May 15;509(7500):357-60.
- Kaufman L, Rousseuw PJ. Finding Groups in Data: An Introduction to Cluster Analysis. Biometrics 1991;47:788.
- Rousseeuw PJ. Silhouettes: A graphical aid to the interpretation and validation of cluster analysis. J. Comput. Appl. Math. 1987;20:53–65.
- Calinski T, Harabasz J. A dendrite method for cluster analysis. Commun. Stat. - Theory Methods. 1974;3:1–27.
- 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.
- Lê Cao KA, González I, Déjean S. integrOmics: an R package to unravel relationships between two omics datasets.. Bioinformatics 2009 Nov 1;25(21):2855-6.
- Clarke KR, Ainsworth M. A method of linking multivariate community structure to environmental variables. Mar. Ecol. Prog. Ser. 1993;92:205–219.
- Witten DM, Tibshirani R, Hastie T. A penalized matrix decomposition, with applications to sparse principal components and canonical correlation analysis.. Biostatistics 2009 Jul;10(3):515-34.
- Difford GF, Plichta DR, Løvendahl P, Lassen J, Noel SJ, Højberg O, Wright AG, Zhu Z, Kristensen L, Nielsen HB, Guldbrandtsen B, Sahana G. Host genetics and the rumen microbiome jointly associate with methane emissions in dairy cows.. PLoS Genet 2018 Oct;14(10):e1007580.
- Pérez P, de los Campos G. Genome-wide regression and prediction with the BGLR statistical package.. Genetics 2014 Oct;198(2):483-95.
- Paulson JN, Stine OC, Bravo HC, Pop M. Differential abundance analysis for microbial marker-gene surveys.. Nat Methods 2013 Dec;10(12):1200-2.
- Ross EM, Moate PJ, Marett LC, Cocks BG, Hayes BJ. Metagenomic predictions: from microbiome to complex health and environmental phenotypes in humans and cattle.. PLoS One 2013;8(9):e73056.
- Ramayo-Caldas Y, Zingaretti L, Popova M, Estellé J, Bernard A, Pons N, Bellot P, Mach N, Rau A, Roume H, Perez-Enciso M, Faverdin P, Edouard N, Ehrlich D, Morgavi DP, Renand G. Identification of rumen microbial biomarkers linked to methane emission in Holstein dairy cows.. J Anim Breed Genet 2020 Jan;137(1):49-59.
Citations
This article has been cited 20 times.- Foury A, Mach N, Ruet A, Lansade L, Moisan MP. Transcriptomic signature related to poor welfare of sport horses.. Compr Psychoneuroendocrinol 2023 Nov;16:100201.
- Homer B, Judd J, Mohammadi Dehcheshmeh M, Ebrahimie E, Trott DJ. Gut Microbiota and Behavioural Issues in Production, Performance, and Companion Animals: A Systematic Review.. Animals (Basel) 2023 Apr 25;13(9).
- Ganda E, Chakrabarti A, Sardi MI, Tench M, Kozlowicz BK, Norton SA, Warren LK, Khafipour E. Saccharomyces cerevisiae fermentation product improves robustness of equine gut microbiome upon stress.. Front Vet Sci 2023;10:1134092.
- 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.
- 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 Dec 19;10(12).
- 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 Oct 3;5(1):1032.
- Colombino E, Raspa F, Perotti M, Bergero D, Vervuert I, Valle E, Capucchio MT. Gut health of horses: effects of high fibre vs high starch diet on histological and morphometrical parameters.. BMC Vet Res 2022 Sep 8;18(1):338.
- Wen X, Luo S, Lv D, Jia C, Zhou X, Zhai Q, Xi L, Yang C. Variations in the fecal microbiota and their functions of Thoroughbred, Mongolian, and Hybrid horses.. Front Vet Sci 2022;9:920080.
- 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 (Basel) 2022 Jun 8;12(12).
- Weinert-Nelson JR, Biddle AS, Williams CA. Fecal microbiome of horses transitioning between warm-season and cool-season grass pasture within integrated rotational grazing systems.. Anim Microbiome 2022 Jun 21;4(1):41.
- Feng Y, Liu D, Liu Y, Yang X, Zhang M, Wei F, Li D, Hu Y, Guo Y. Host-genotype-dependent cecal microbes are linked to breast muscle metabolites in Chinese chickens.. iScience 2022 Jun 17;25(6):104469.
- Lara F, Castro R, Thomson P. Changes in the gut microbiome and colic in horses: Are they causes or consequences?. Open Vet J 2022 Mar-Apr;12(2):242-249.
- Wang Y, Nguyen LH, Mehta RS, Song M, Huttenhower C, Chan AT. Association Between the Sulfur Microbial Diet and Risk of Colorectal Cancer.. JAMA Netw Open 2021 Nov 1;4(11):e2134308.
- Goodman-Davis R, Figurska M, Cywinska A. Gut Microbiota Manipulation in Foals-Naturopathic Diarrhea Management, or Unsubstantiated Folly?. Pathogens 2021 Sep 4;10(9).
- Zhu Y, Wang X, Liu B, Yi Z, Zhao Y, Deng L, Holyoak R, Li J. The Effect of Ryegrass Silage Feeding on Equine Fecal Microbiota and Blood Metabolite Profile.. Front Microbiol 2021;12:715709.
- Mach N, Baranowski E, Nouvel LX, Citti C. The Airway Pathobiome in Complex Respiratory Diseases: A Perspective in Domestic Animals.. Front Cell Infect Microbiol 2021;11:583600.
- Mach N, Moroldo M, Rau A, Lecardonnel J, Le Moyec L, Robert C, Barrey E. Understanding the Holobiont: Crosstalk Between Gut Microbiota and Mitochondria During Long Exercise in Horse.. Front Mol Biosci 2021;8:656204.
- Martin de Bustamante M, Gomez D, MacNicol J, Hamor R, Plummer C. The Fecal Bacterial Microbiota in Horses with Equine Recurrent Uveitis.. Animals (Basel) 2021 Mar 9;11(3).
- Mach N, Lansade L, Bars-Cortina D, Dhorne-Pollet S, Foury A, Moisan MP, Ruet A. Gut microbiota resilience in horse athletes following holidays out to pasture.. Sci Rep 2021 Mar 3;11(1):5007.
- 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 (Basel) 2021 Jan 24;11(2).
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