Comparison of Fecal Microbiota of Horses Suffering from Atypical Myopathy and Healthy Co-Grazers.
Abstract: Equine atypical myopathy (AM) is caused by hypoglycin A (HGA) and methylenecyclopropylglycine (MCPG) intoxication resulting from the ingestion of seeds or seedlings of some Acer tree species. Interestingly, not all horses pasturing in the same toxic environment develop signs of the disease. In other species, it has been shown that the intestinal microbiota has an impact on digestion, metabolism, immune stimulation and protection from disease. The objective of this study was to characterize and compare fecal microbiota of horses suffering from AM and healthy co-grazers. Furthermore, potential differences in fecal microbiota regarding the outcome of diseased animals were assessed. This prospective observational study included 59 horses with AM (29 survivors and 30 non-survivors) referred to three Belgian equine hospitals and 26 clinically healthy co-grazers simultaneously sharing contaminated pastures during spring and autumn outbreak periods. Fresh fecal samples (rectal or within 30 min of defecation) were obtained from all horses and bacterial taxonomy profiling obtained by 16S amplicon sequencing was used to identify differentially distributed bacterial taxa between AM-affected horses and healthy co-grazers. Fecal microbial diversity and evenness were significantly (p < 0.001) higher in AM-affected horses as compared with their non-affected co-grazers. The relative abundance of families Ruminococcaceae, Christensenellaceae and Akkermansiaceae were higher (p ≤ 0.001) whereas those of the Lachnospiraceae (p = 0.0053), Bacteroidales (p < 0.0001) and Clostridiales (p = 0.0402) were lower in horses with AM, especially in those with a poor prognosis. While significant shifts were observed, it is still unclear whether they result from the disease or might be involved in the onset of disease pathogenesis.
Publication Date: 2021-02-15 PubMed ID: 33672034PubMed Central: PMC7919468DOI: 10.3390/ani11020506Google Scholar: Lookup
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Summary
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This research explores the differences in intestinal bacteria between horses suffering from Atypical Myopathy (AM) – a disease caused by plant toxins, and their healthy counterparts sharing the same environment. It was found that there are significant differences in bacterial composition, which might be a contributing factor to the onset or progression of the disease.
Study Objective and Design
- The main objective of the study was to examine the fecal microbiota of horses which were suffering from AM and compare it with the horses in similar environments but were healthy, known as ‘co-grazers’.
- A secondary aim was to identify potential differences in intestinal bacteria which may be associated with the outcome of the disease, distinguishing between survivors and non-survivors.
- The study was observational and prospective, observing the horses’ conditions and their fecal microbiota over time and in a natural environment, as opposed to experimenting in a lab setup.
Methodology
- The test subjects included 59 horses with AM and 26 healthy ones, all of which shared contaminated pastures.
- Fresh fecal samples were collected from all the horses, either directly (rectal collection) or within 30 minutes of defecation.
- These samples were then processed using 16S amplicon sequencing, a technology that allows researchers to identify and profile bacterial species based on their genetic material.
- The diversity and evenness of microbial populations in the samples were calculated and compared between the AM-affected horses and the healthy co-grazers.
Findings
- The researchers found higher microbial diversity and evenness in horses suffering from AM compared to the healthy horses. This suggests that AM affected horses had a larger variety of different types of bacteria and a more balanced distribution of these types.
- Specific bacterial families – namely, Ruminococcaceae, Christensenellaceae, and Akkermansiaceae were found to be more abundant in the feces of AM-affected horses, while the families Lachnospiraceae, Bacteroidales, and Clostridiales were less abundant – especially in horses with a poor disease prognosis.
Conclusion
- While clear differences in fecal microbiota composition were observed between AM-affected horses and healthy ones, it’s unclear whether these alterations are a result or a cause of the disease. It’s possible that changes in the gut bacteria may have allowed the horse’s system to better metabolize the toxic plants, preventing its harmful effects, or it might be a consequence of the disease process itself.
Cite This Article
APA
Wimmer-Scherr C, Taminiau B, Renaud B, van Loon G, Palmers K, Votion D, Amory H, Daube G, Cesarini C.
(2021).
Comparison of Fecal Microbiota of Horses Suffering from Atypical Myopathy and Healthy Co-Grazers.
Animals (Basel), 11(2).
https://doi.org/10.3390/ani11020506 Publication
Researcher Affiliations
- Equine Clinical Department, Faculty of Veterinary Medicine, Bât. B41, Sart Tilman, University of Liège, 4000 Liège, Belgium.
- Fundamental and Applied Research for Animals & Health (FARAH), Faculty of Veterinary Medicine, Sart Tilman, University of Liège, 4000 Liège, Belgium.
- Fundamental and Applied Research for Animals & Health (FARAH), Faculty of Veterinary Medicine, Sart Tilman, University of Liège, 4000 Liège, Belgium.
- Department of Food Sciences-Microbiology, Faculty of Veterinary Medicine, University of Liège, Avenue de Cureghem 10, Bât. B43b, 4000 Liège, Belgium.
- Fundamental and Applied Research for Animals & Health (FARAH), Faculty of Veterinary Medicine, Sart Tilman, University of Liège, 4000 Liège, Belgium.
- Department of Functional Sciences, Pharmacology and Toxicology, Faculty of Veterinary Medicine, Bât. B41, Sart Tilman, University of Liège, 4000 Liège, Belgium.
- Large Animal Internal Medicine, Gent University, 9820 Gent, Belgium.
- De Morette Equine Clinic, 1730 Asse, Belgium.
- Fundamental and Applied Research for Animals & Health (FARAH), Faculty of Veterinary Medicine, Sart Tilman, University of Liège, 4000 Liège, Belgium.
- Equine Clinical Department, Faculty of Veterinary Medicine, Bât. B41, Sart Tilman, University of Liège, 4000 Liège, Belgium.
- Fundamental and Applied Research for Animals & Health (FARAH), Faculty of Veterinary Medicine, Sart Tilman, University of Liège, 4000 Liège, Belgium.
- Fundamental and Applied Research for Animals & Health (FARAH), Faculty of Veterinary Medicine, Sart Tilman, University of Liège, 4000 Liège, Belgium.
- Department of Food Sciences-Microbiology, Faculty of Veterinary Medicine, University of Liège, Avenue de Cureghem 10, Bât. B43b, 4000 Liège, Belgium.
- Equine Clinical Department, Faculty of Veterinary Medicine, Bât. B41, Sart Tilman, University of Liège, 4000 Liège, Belgium.
- Fundamental and Applied Research for Animals & Health (FARAH), Faculty of Veterinary Medicine, Sart Tilman, University of Liège, 4000 Liège, Belgium.
Grant Funding
- 0000 / Service Public de Wallonie
- FSR 2020 / Université de Liège
Conflict of Interest Statement
The authors declare no conflict of interest.
References
This article includes 81 references
- Votion D.-M., François A.-C., Kruse C., Renaud B., Farinelle A., Bouquieaux M.-C., Marcillaud-Pitel C., Gustin P.. Answers to the Frequently Asked Questions Regarding Horse Feeding and Management Practices to Reduce the Risk of Atypical Myopathy.. Animals 2020;10:365.
- Votion D.-M., Serteyn D.. Equine Atypical Myopathy: A Review.. Vet. J. 2008;178:185–190.
- Votion D.-M., Linden A., Delguste C., Amory H., Thiry E., Engels P., van Galen G., Navet R., Sluse F., Serteyn D.. Atypical Myopathy in Grazing Horses: A First Exploratory Data Analysis.. Vet. J. 2009;180:77–87.
- Unger L., Nicholson A., Jewitt E.M., Gerber V., Hegeman A., Sweetman L., Valberg S.. Hypoglycin A Concentrations in Seeds of Acer Pseudoplatanus Trees Growing on Atypical Myopathy-Affected and Control Pastures.. J. Vet. Intern. Med. 2014;28:1289–1293.
- Baise E., Habyarimana J.A., Amory H., Boemer F., Douny C., Gustin P., Marcillaud-Pitel C., Patarin F., Weber M., Votion D.-M.. Samaras and Seedlings of Acer Pseudoplatanus Are Potential Sources of Hypoglycin A Intoxication in Atypical Myopathy without Necessarily Inducing Clinical Signs.. Equine Vet. J. 2016;48:414–417.
- Bochnia M., Sander J., Ziegler J., Terhardt M., Sander S., Janzen N., Cavalleri J.-M., Zuraw A., Wensch-Dorendorf M., Zeyner A.. Detection of MCPG Metabolites in Horses with Atypical Myopathy.. PLoS ONE 2019;14:e0211698.
- Van Galen G., Marcillaud Pitel C., Saegerman C., Patarin F., Amory H., Baily J.D., Cassart D., Gerber V., Hahn C., Harris P.. European Outbreaks of Atypical Myopathy in Grazing Equids (2006–2009): Spatiotemporal Distribution, History and Clinical Features: Outbreaks of Atypical Myopathy: Spatiotemporal Distribution, History and Clinical Features.. Equine Vet. J. 2012;44:614–620.
- González-Medina S., Ireland J.L., Piercy R.J., Newton J.R., Votion D.M.. Equine Atypical Myopathy in the UK: Epidemiological Characteristics of Cases Reported from 2011 to 2015 and Factors Associated with Survival.. Equine Vet. J. 2017;49:746–752.
- Fabius L.S., Westermann C.M.. Evidence-Based Therapy for Atypical Myopathy in Horses.. Equine Vet. Educ. 2018;30:616–622.
- Dunkel B., Ryan A., Haggett E., Knowles E.J.. Atypical Myopathy in the South-East of England: Clinicopathological Data and Outcome in Hospitalised Horses.. Equine Vet. Educ. 2020;32:90–95.
- Krägeloh T., Cavalleri J.M.V., Ziegler J., Sander J., Terhardt M., Breves G., Cehak A.. Identification of Hypoglycin A Binding Adsorbents as Potential Preventive Measures in Co-Grazers of Atypical Myopathy Affected Horses.. Equine Vet. J. 2018;50:220–227.
- Bochnia M., Ziegler J., Sander J., Uhlig A., Schaefer S., Vollstedt S., Glatter M., Abel S., Recknagel S., Schusser G.F.. Hypoglycin A Content in Blood and Urine Discriminates Horses with Atypical Myopathy from Clinically Normal Horses Grazing on the Same Pasture.. PLoS ONE 2015;10:e0136785.
- Venable E.B., Bland S.D., McPherson J.L., Francis J.. Role of the Gut Microbiota in Equine Health and Disease.. Anim. Front. 2016;6:43–49.
- Jandhyala S.M., Talukdar R., Subramanyam C., Vuyyuru H., Sasikala M., Reddy D.N.. Role of the Normal Gut Microbiota.. World J. Gastroenterol. WJG 2015;21:8787.
- Kamada N., Seo S.-U., Chen G.Y., Núñez G.. Role of the Gut Microbiota in Immunity and Inflammatory Disease.. Nat. Rev. Immunol. 2013;13:321–335.
- Carding S., Verbeke K., Vipond D.T., Corfe B.M., Owen L.J.. Dysbiosis of the Gut Microbiota in Disease.. Microb. Ecol. Health Dis. 2015;26:26191.
- Costa M.C., Arroyo L.G., Allen-Vercoe E., Stämpfli H.R., Kim P.T., Sturgeon A., Weese J.S.. 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.
- Milinovich G.J., Klieve A.V., Pollitt C.C., Trott D.J.. Microbial Events in the Hindgut During Carbohydrate-Induced Equine Laminitis.. Vet. Clin. North. Am. Equine Pract. 2010;26:79–94.
- Elzinga S.E., Weese J.S., Adams A.A.. Comparison of the Fecal Microbiota in Horses With Equine Metabolic Syndrome and Metabolically Normal Controls Fed a Similar All-Forage Diet.. J. Equine Vet. Sci. 2016;44:9–16.
- Jevit M.J.. Microflora of the Equine Gut and Its Ramifications on the Development of Laminitis; A Comparison of Fecal and Cecal Diversity and Illumina and Roche 454 Sequencers.. Master’s Thesis. Duquesne University; Pittsburgh, PA, USA: 2016.
- 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;17:1120.
- Stewart H.L., Southwood L.L., Indugu N., Vecchiarelli B., Engiles J.B., Pitta D.. Differences in the Equine Faecal Microbiota between Horses Presenting to a Tertiary Referral Hospital for Colic Compared with an Elective Surgical Procedure.. Equine Vet. J. 2019;51:336–342.
- Dai Z.-L., Zhang J., Wu G., Zhu W.-Y.. Utilization of Amino Acids by Bacteria from the Pig Small Intestine.. Amino acids 2010;39:1201–1215.
- Dai Z.-L., Wu G., Zhu W.-Y.. Amino Acid Metabolism in Intestinal Bacteria: Links between Gut Ecology and Host Health.. Front. Biosci. 2011;16:1768–1786.
- Davila A.-M., Blachier F., Gotteland M., Andriamihaja M., Benetti P.-H., Sanz Y., Tomé D.. Re-Print of “Intestinal Luminal Nitrogen Metabolism: Role of the Gut Microbiota and Consequences for the Host.”. Pharmacol. Res. 2013;69:114–126.
- Melde K., Jackson S., Bartlett K., Sherratt H.S.A., Ghisla S.. Metabolic Consequences of Methylenecyclopropylglycine Poisoning in Rats.. Biochem. J. 1991;274:395–400.
- Stewart H.L., Pitta D., Indugu N., Vecchiarelli B., Engiles J.B., Southwood L.L.. Characterization of the Fecal Microbiota of Healthy Horses.. Am. J. Vet. Res. 2018;79:811–819.
- Westermann C.M., Dorland L., Votion D.M., de Sain-van der Velden M.G.M., Wijnberg I.D., Wanders R.J.A., Spliet W.G.M., Testerink N., Berger R., Ruiter J.P.N.. Acquired Multiple Acyl-CoA Dehydrogenase Deficiency in 10 Horses with Atypical Myopathy.. Neuromuscul. Disord. 2008;18:355–364.
- Boemer F., Detilleux J., Cello C., Amory H., Marcillaud-Pitel C., Richard E., van Galen G., van Loon G., Lefère L., Votion D.-M.. Acylcarnitines Profile Best Predicts Survival in Horses with Atypical Myopathy.. PLoS ONE 2017;12:e0182761.
- Cerri S., Taminiau B., Lusancay A.H., Lecoq L., Amory H., Daube G., Cesarini C.. Effect of Oral Administration of Omeprazole on the Microbiota of the Gastric Glandular Mucosa and Feces of Healthy Horses.. J. Vet. Intern. Med. 2020;34:2727–2737.
- Schloss P.D., Westcott S.L., Ryabin T., Hall J.R., Hartmann M., Hollister E.B., Lesniewski R.A., Oakley B.B., Parks D.H., Robinson C.J.. Introducing Mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities.. AEM 2009;75:7537–7541.
- Rognes T., Flouri T., Nichols B., Quince C., Mahé F.. VSEARCH: A Versatile Open Source Tool for Metagenomics.. PeerJ 2016;4:e2584.
- . SILVA Ribosomal RNA Gene Database Project: Improved Data Processing and Web-Based Tools | Nucleic Acids Research | Oxford Academic.. [(accessed on 11 December 2020)].
- Morris E.K., Caruso T., Buscot F., Fischer M., Hancock C., Maier T.S., Meiners T., Müller C., Obermaier E., Prati D.. Choosing and Using Diversity Indices: Insights for Ecological Applications from the German Biodiversity Exploratories.. Ecol. Evol. 2014;4:3514–3524.
- Chao A.. A New Statistical Approach for Assessing Compositional Similarity Based on Incidence and Abundance Data.. Ecol. Lett. 2005;8:148–159.
- Excoffier L., Smouse P.E., Quattro J.M.. Analysis of Molecular Variance Inferred from Metric Distances among DNA Haplotypes: Application to Human Mitochondrial DNA Restriction Data.. Genetics 1992;131:479–491.
- Schoster A., Staempfli H.R., Guardabassi L.G., Jalali M., Weese J.S.. Comparison of the Fecal Bacterial Microbiota of Healthy and Diarrheic Foals at Two and Four Weeks of Life.. BMC Vet. Res. 2017;13:144.
- 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.
- Steelman S.M., Chowdhary B.P., Dowd S., Suchodolski J., Janečka J.E.. 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;8:231.
- Bailey S.R., Adair H.S., Reinemeyer C.R., Morgan S.J., Brooks A.C., Longhofer S.L., Elliott J.. Plasma Concentrations of Endotoxin and Platelet Activation in the Developmental Stage of Oligofructose-Induced Laminitis.. Vet. Immunol. and Immunopathol. 2009;129:167–173.
- 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 Vet. Res. 2021;17:11.
- Milinovich G.J., Trott D.J., Burrell P.C., Croser E.L., Al Jassim R.A., Morton J.M., Van Eps A.W., Pollitt C.C.. Fluorescence in Situ Hybridization Analysis of Hindgut Bacteria Associated with the Development of Equine Laminitis.. Environ. Microbiol. 2007;9:2090–2100.
- Woodmansey E.J.. Intestinal Bacteria and Ageing.. J. Appl. Microbiol. 2007;102:1178–1186.
- Dougal K., de la Fuente G., Harris P.A., Girdwood S.E., Pinloche E., Geor R.J., Nielsen B.D., Schott H.C., Elzinga S., Newbold C.J.. 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.
- Theelen M., Wagenaar M., van Oldruitenborgh-Oosterbaan M.M.S., Rossen J.W.A., Schaafstra F.J., Van Doorn D.A., Zomer A.L.. Short- and Long-Term Effect of Hospitalization and Oral Trimethoprim-Sulfadiazine Administration on the Equine Faecal Microbiome; Proceedings of the ECEIM Online Congress 2020; 20 November 2020.. .
- Schoster A., Mosing M., Jalali M., Staempfli H.R., Weese J.S.. Effects of Transport, Fasting and Anaesthesia on the Faecal Microbiota of Healthy Adult Horses.. Equine Vet. J. 2016;48:595–602.
- Brandt K., Hinrichs U., Glitz F., Landes E., Schulze C., Deegen E., Pohlenz J., Coenen M.. Atypische Myoglobinurie Der Weidepferde.. Pferdeheilkunde 1997;13:27–34.
- Julliand V., Grimm P.. HORSE SPECIES SYMPOSIUM: The Microbiome of the Horse Hindgut: History and Current Knowledge1.. J. Anim. Sci. 2016;94:2262–2274.
- Li Y., Zhang K., Liu Y., Li K., Hu D., Wronski T.. Community Composition and Diversity of Intestinal Microbiota in Captive and Reintroduced Przewalski’s Horse (Equus Ferus Przewalskii). Front. Microbiol. 2019;10:1821.
- Edwards J.E., Shetty S.A., van den Berg P., Burden F., van Doorn D.A., Pellikaan W.F., Dijkstra J., Smidt H.. Multi-Kingdom Characterization of the Core Equine Fecal Microbiota Based on Multiple Equine (Sub) Species.. Anim. Microbiome 2020;2:1–16.
- Kauter A., Epping L., Semmler T., Antao E.-M., Kannapin D., Stoeckle S.D., Gehlen H., Lübke-Becker A., Günther S., Wieler L.H.. The Gut Microbiome of Horses: Current Research on Equine Enteral Microbiota and Future Perspectives.. Anim. Microbiome 2019;1:14.
- Peris-Bondia F., Latorre A., Artacho A., Moya A., D’Auria G.. The Active Human Gut Microbiota Differs from the Total Microbiota.. PLoS ONE 2011;6:e22448.
- Costa M.C., Silva G., Ramos R.V., Staempfli H.R., Arroyo L.G., Kim P., Weese J.S.. Characterization and Comparison of the Bacterial Microbiota in Different Gastrointestinal Tract Compartments in Horses.. The Vet. J. 2015;205:74–80.
- Roediger W.E.W.. The Colonic Epithelium in Ulcerative Colitis: An Energy-Deficiency Disease?. Lancet 1980;316:712–715.
- Conlon M.A., Bird A.R.. The Impact of Diet and Lifestyle on Gut Microbiota and Human Health.. Nutrients 2014;7:17–44.
- Cockburn D.W., Koropatkin N.M.. Polysaccharide Degradation by the Intestinal Microbiota and Its Influence on Human Health and Disease.. J. Mol. Biol. 2016;428:3230–3252.
- Fava F., Gitau R., Griffin B.A., Gibson G.R., Tuohy K.M., Lovegrove J.A.. The Type and Quantity of Dietary Fat and Carbohydrate Alter Faecal Microbiome and Short-Chain Fatty Acid Excretion in a Metabolic Syndrome ‘at-Risk’ Population.. Int J. Obes. 2013;37:216–223.
- Ferrario C., Statello R., Carnevali L., Mancabelli L., Milani C., Mangifesta M., Duranti S., Lugli G.A., Jimenez B., Lodge S.. How to Feed the Mammalian Gut Microbiota: Bacterial and Metabolic Modulation by Dietary Fibers.. Front. Microbiol. 2017;8.
- Daly K., Proudman C.J., Duncan S.H., Flint H.J., Dyer J., Shirazi-Beechey S.P.. 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.
- Britton R.A., Young V.B.. Interaction between the Intestinal Microbiota and Host in Clostridium Difficile Colonization Resistance.. Trends Microbiol. 2012;20:313–319.
- Meehan C.J., Beiko R.G.. A Phylogenomic View of Ecological Specialization in the Lachnospiraceae, a Family of Digestive Tract-Associated Bacteria.. Genome Biol. Evol. 2014;6:703–713.
- Mandal M., Olson D.J., Sharma T., Vadlamudi R.K., Kumar R.. Butyric Acid Induces Apoptosis by Up-Regulating Bax Expression via Stimulation of the c-Jun N-Terminal Kinase/Activation Protein-1 Pathway in Human Colon Cancer Cells.. Gastroenterology 2001;120:71–78.
- Nepelska M., Cultrone A., Béguet-Crespel F., Le Roux K., Doré J., Arulampalam V., Blottière H.M.. Butyrate Produced by Commensal Bacteria Potentiates Phorbol Esters Induced AP-1 Response in Human Intestinal Epithelial Cells.. PLoS ONE 2012;7:e52869.
- Hess J.. AP-1 Subunits: Quarrel and Harmony among Siblings.. J. Cell Sci. 2004;117:5965–5973.
- Waters J.L., Ley R.E.. The Human Gut Bacteria Christensenellaceae Are Widespread, Heritable, and Associated with Health.. BMC Biol. 2019;17:83.
- Alemán J.O., Bokulich N.A., Swann J.R., Walker J.M., De Rosa J.C., Battaglia T., Costabile A., Pechlivanis A., Liang Y., Breslow J.L.. Fecal Microbiota and Bile Acid Interactions with Systemic and Adipose Tissue Metabolism in Diet-Induced Weight Loss of Obese Postmenopausal Women.. J. Transl. Med. 2018;16:244.
- Goodrich J.K., Waters J.L., Poole A.C., Sutter J.L., Koren O., Blekhman R., Beaumont M., Van Treuren W., Knight R., Bell J.T.. Human Genetics Shape the Gut Microbiome.. Cell 2014;159:789–799.
- Dougal K., Harris P.A., Edwards A., Pachebat J.A., Blackmore T.M., Worgan H.J., Newbold C.J.. Changes in the Total Fecal Bacterial Population in Individual Horses Maintained on a Restricted Diet Over 6 Weeks.. Front. Microbiol. 2017;8.
- Biddle A.S., Tomb J.-F., Fan Z.. Microbiome and Blood Analyte Differences Point to Community and Metabolic Signatures in Lean and Obese Horses.. Front. Vet. Sci. 2018;5.
- Belzer C., Vos W.M. de. Microbes inside—from Diversity to Function: The Case of Akkermansia.. ISME J. 2012;6:1449–1458.
- Swidsinski A., Dorffel Y., Loening-Baucke V., Theissig F., Ruckert J.C., Ismail M., Rau W.A., Gaschler D., Weizenegger M., Kuhn S.. Acute Appendicitis Is Characterised by Local Invasion with Fusobacterium Nucleatum/Necrophorum.. Gut 2011;60:34–40.
- Swidsinski A., Loening-Baucke V., Herber A.. Mucosal Flora in Crohn’s Disease and Ulcerative Colitis—an Overview.. J. Physiol. Pharmacol. 2009;60(Suppl. 6):61–71.
- Zhang H., DiBaise J.K., Zuccolo A., Kudrna D., Braidotti M., Yu Y., Parameswaran P., Crowell M.D., Wing R., Rittmann B.E.. Human Gut Microbiota in Obesity and after Gastric Bypass.. Proc. Natl. Acad. Sci. USA. 2009;106:2365–2370.
- Png C.W., Lindén S.K., Gilshenan K.S., Zoetendal E.G., McSweeney C.S., Sly L.I., McGuckin M.A., Florin T.H.J.. Mucolytic Bacteria With Increased Prevalence in IBD Mucosa Augment In Vitro Utilization of Mucin by Other Bacteria.. Am. J. Gastroenterol. 2010;105:2420–2428.
- Wang L., Christophersen C.T., Sorich M.J., Gerber J.P., Angley M.T., Conlon M.A.. Low Relative Abundances of the Mucolytic Bacterium Akkermansia Muciniphila and Bifidobacterium Spp. in Feces of Children with Autism.. Appl. Environ. Microbiol. 2011;77:6718–6721.
- Sonoyama K., Fujiwara R., Takemura N., Ogasawara T., Watanabe J., Ito H., Morita T.. Response of Gut Microbiota to Fasting and Hibernation in Syrian Hamsters.. AEM 2009;75:6451–6456.
- Shin N.-R., Lee J.-C., Lee H.-Y., Kim M.-S., Whon T.W., Lee M.-S., Bae J.-W.. An Increase in the Akkermansia Spp. Population Induced by Metformin Treatment Improves Glucose Homeostasis in Diet-Induced Obese Mice.. Gut 2014;63:727–735.
- Votion D.-M.. The Story of Equine Atypical Myopathy: A Review from the Beginning to a Possible End.. Int. Sch. Res. Not. 2012;2012:1–14.
- Dai Z.-L., Li X.-L., Xi P.-B., Zhang J., Wu G., Zhu W.-Y.. Metabolism of Select Amino Acids in Bacteria from the Pig Small Intestine.. Amino Acids 2012;42:1597–1608.
- Dougal K., Harris P.A., Edwards A., Pachebat J.A., Blackmore T.M., Worgan H.J., Newbold C.J.. A Comparison of the Microbiome and the Metabolome of Different Regions of the Equine Hindgut.. FEMS Microbiol. Ecol. 2012;82:642–652.
- Arumugam M., Raes J., Pelletier E., Le Paslier D., Yamada T., Mende D.R., Fernandes G.R., Tap J., Bruls T., Batto J.-M.. Enterotypes of the Human Gut Microbiome.. Nature 2011;473:174–180.
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