Integrated Nutraceutical – Nutritional Approaches to Address Equine Leaky Gut Syndrome

Authors

  • Michael Ivan Lindinger The Nutraceutical Alliance

DOI:

https://doi.org/10.30564/vsr.v1i1.1057

Abstract

Many of the nutrients beneficial for intestinal health are present in normal foods, but their normal daily intake may be too low to exert optimum effects on intestinal barrier function and immune status. Evidence from laboratory and farm production animals strongly supports dietary supplementation with additional nutrients and nutraceuticals, however research in horses remains scarce and inconclusive. Careful consideration of the outcome desired for horses in care, together with the types of nutraceuticals available, is needed to develop effective strategies for maintenance of healthy intestinal barrier function and for treatment of various leaky gut syndromes in horses. This review presents these issues in the context of what is known about the effects of nutraceutical-type nutrients on the mammalian (including equine) g.i. tract and intestinal microbiome with the aim of providing suggestions for the equine situation.

Keywords:

Horse, Gastro-intestinal tract, Intestinal epithelial cells, Microbiome, Amino acids, Beta-glucans, Probiotics, Prebiotics

References

[1] Stewart AS, Pratt-Phillips S, Gonzalez LM. Alterations in intestinal permeability: the role of the “leaky gut” in health and disease. J Eq Vet Sci, 2017, 52: 10 – 22. DOI:https://doi.org/10.1016/j.jevs.2017.02.009

[2] Pastorelli L, De Salvo C, Mercado JR, Vecchi M, Pizarro TT. Central role of the gut epithelial barrier in the pathogenesis of chronic intestinal inflammation: lessons learned from animal models and human genetics. Front Immunol, 2013, 4: 280. DOI:https://doi.org/10.3389/fimmu.2013.00280

[3] Michielan A, D'Incà R. Intestinal permeability in inflammatory bowel disease: pathogenesis, clinical evaluation, and therapy of leaky gut. Integrat Mediators Inflamm, 2015, 2015: 628157. DOI:https://doi.org/10.1155/2015/628157

[4] Uzal FA, Diab SS. Gastritis, enteritis, and colitis in horses. Vet Clin North Am Equine Pract, 2015, 31(2): 337-358. DOI:https://doi.org/10.1016/j.cveq.2015.04.006

[5] Mathers JC. Nutrient regulation of intestinal proliferation and apoptosis. Proc Nutr Soc, 1998, 57: 219–223. DOI:https://doi.org/10.1079/PNS19980035

[6] Ohland CL, MacNaughton WK. Probiotic bacteria and intestinal epithelial barrier function. Am J Physiol Gastrointest Liver Physiol, 2010, 298: G807–G819. DOI:https://doi.org/10.1152/ajpgi.00243.2009

[7] Rao JN, Wang JY. Luminal nutrients in health and microbes in gut mucosal growth. In: Regulation of Gastrointestinal Mucosal Growth. NCBI Bookshelf. San Rafael (CA): Morgan & Claypool Life Sciences, 2010.

[8] Schoster A, Weese JS, Guardabassi L. Probiotic use in horses - what is the evidence for their clinical efficacy? J Vet Intern Med, 2014. 28(6): 1640-1652. DOI:https://doi.org/10.1111/jvim.12451

[9] Weser E, Babbitt J, Hoban M, Vandeventer A. Intestinal adaptation: different growth responses to disaccharides compared with monosaccharides in rat small bowel. Gastroenterology 1986, 91: 1521–1527.

[10] Weser E. Nutritional aspects of malabsorption: short gut adaptation. Clin Gastroenterol 1983, 12: 443–461.

[11] Finnie IA, Dwarakanath AD, Taylor BA, Rhodes JM. Colonic mucin synthesis is increased by sodium butyrate. Gut, 1995, 36: 93–99.

[12] Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, Brummer RJ. Review article: the role of butyrate on colonic function. Aliment Pharmacol Ther, 2008, 27: 104–119.DOI:https://doi.org/10.1111/j.1365-2036.2007.03562.x

[13] Zheng L, Kelly CJ, Battista KD, Schaefer R, Lanis JM, Alexeev EE, Wang RX, Onyiah JC, Kominsky DJ, Colgan SP. Microbial-derived butyrate promotes epithelial barrier function through IL-10 receptor−dependent repression of claudin-2. J Immunol, 2017, 199(8): 2976-2984. DOI:https://doi.org/10.4049/jimmunol.1700105

[14] Fedriko V, Bostick RM, Flanders WD, Long Q, Sidelnikov E, Shaukat A, Daniel CR, Rutherford RE, Woodard JJ. Effects of vitamin D and calcium on proliferation and differentiation in normal colon mucosa: a randomized clinical trial. Cancer Epidemiol Biomarkers Prev, 2009, 18(11): 2933-2941. DOI:https://doi.org/10.1158/1055-9965

[15] Uni Z, Zaiger G, Gal-Garber O, Pines M, Rozenboim I, Reifen R. Vitamin A deficiency interferes with proliferation and maturation of cells in the chicken small intestine. Br Poult Sci, 2000, 41: 410–415. DOI:https://doi.org/10.1080/10408398.2016.1160362

[16] Zanoni JN, Fernandes PRV. Cell proliferation of the ileum intestinal mucosa of diabetic rats treated with ascorbic acid. Biocell, 2008, 32: 163–168.

[17] Fürst P, Pogan K, Stehle P. L-glutamine dipeptides in clinical nutrition. Nutrition, 1997, 13: 731-737.

[18] Watford M. L-glutamine metabolism and function in relation to proline synthesis and the safety of L-glutamine and proline supplementation. J Nutr, 2008. 138(10): 2003S-2007S. DOI:https://doi.org/10.1093/jn/138.10.2003S

[19] Wu G, Wu Z, Dai Z, Yang Y, Wang W, Liu C, Wang B, Wang J, Yin Y. Dietary requirements of "nutritionally non-essential amino acids" by animals and humans. Amino Acids, 2013, 44(4): 1107-1113. DOI:https://doi.org/10.1007/s00726-012-1444-2

[20] Zuhl MN, Lanphere KR, Kravitz L, Mermier CM, Schneider S, Dokladny K, Moseley PL. 2014. Effects of oral glutamine supplementation on exercise-induced gastrointestinal permeability and tight junction protein expression. J Appl Physiol, 2014, 116: 183–191. DOI:https://doi.org/10.1152/japplphysiol.00646.2013

[21] Kuhn KS, Schuhmann K, Stehle P, Darmaun D, Fürst P. Determination of L-glutamine in muscle protein facilitates accurate assessment of proteolysis and de novo synthesis-derived endogenous L-glutamine production. Am. J. Clin. Nutr. 1999, 70(4): 484-489. DOI:https://doi.org/10.1093/ajcn/70.4.484

[22] van der Schoor SR, Schierbeek H, Bet PM, Vermeulen MJ, Lafeber HN, van Goudoever JB, van Elburg RM. Majority of dietary L-glutamine is utilized in first pass in preterm infants. Pediatr. Res.2010, 67(2): 194-199. DOI:https://doi.org/10.1203/PDR.0b013e3181c34609

[23] Blachier F, Boutry C, Bos C, Tomé D. Metabolism and functions of L-glutamate in the epithelial cells of the small and large intestines. Am. J. Clin. Nutr. 2009, 90(3): 814S-821S. DOI:https://doi.org/10.3945/ajcn.2009.27462S

[24] Wu G, Wu Z, Dai Z, Yang Y, Wang W, Liu C, Wang B, Wang J, Yin Y. Dietary requirements of "nutritionally non-essential amino acids" by animals and humans. Amino Acids, 2013. 44(4): 1107-1113. DOI:https://doi.org/10.1007/s00726-012-1444-2

[25] Watford M. L-glutamine metabolism and function in relation to proline synthesis and the safety of L-glutamine and proline supplementation. J. Nutr. 2008, 138(10): 2003S-2007S DOI:https://doi.org/10.1093/jn/138.10.2003S

[26] Domeneghini C, Di Giancamillo A, Bosi G, Arrighi S. Can nutraceuticals affect the structure of intestinal mucosa? Qualitative and quantitative microanatomy in L-glutamine diet-supplemented weaning piglets. Vet. Res. Commun, 2006,. 30: 331-342. DOI:https://doi.org/10.3382/ps.2009-00415

[27] Larson SD, Li J, Chung DH, Evers BM. Molecular mechanisms contributing to L-glutamine-mediated intestinal cell survival. Am J Physiol Gastrointest Liver Physiol, 2007. 293(6):G1262-G1271. DOI:https://doi.org/10.1152/ajpgi.00254.2007

[28] dos Santos Rd, Viana ML, Generoso SV, Arantes RE, Davisson Correia MI, Cardoso VN. Glutamine supplementation decreases intestinal permeability and preserves gut mucosa integrity in an experimental mouse model. JPEN J Parenter Enteral Nutr, 2010. 34(4):408-13. DOI:https://doi.org/10.1177/0148607110362530

[29] Ruth MR, Field CJ. The immune modifying effects of amino acids on gut-associated lymphoid tissue. J Anim Sci Biotechnol, 2013, 4(1): 27. DOI:https://doi.org/10.1186/2049-1891-4-27

[30] Wang B, Wu G, Zhou Z, Dai Z, Sun Y, Ji Y, Li W, Wang W, Liu C, Han F, Wu Z. Glutamine and intestinal barrier function. Amino Acids 2015. 47(10): 2143-2154. DOI:https://doi.org/10.1007/s00726-014-1773-4

[31] Hirschfield JS, Kern F. Protein starvation and the small intestine. Incorporation of orally and intraperitoneally administered 1-leucine 4, 5-3H into intestinal mucosal protein of protein deprived rats. J Clin Invest, 1969. 48: 1224–1229.

[32] Reeds PJ, Burrin DG. Glutamine and the bowel. J Nutr, 2001. 131: 2505S–2508S. DOI:https://doi.org/10.1093/jn/131.9.2505S

[33] Gismondo MR, Drago L, Fassina MC, Vaghi I, Abbiati R, Grossi E. Immunostimulating effect of oral glutamine. Dig Dis Sci. 1998, 43(8): 1752-4.

[34] Naomoto Y, Yamatsuji T, Shigemitsu K, Ban H, Nakajo T, Shirakawa Y, Motok T, Kobayashi M, Gunduz M, Tanaka N. Rational role of amino acids in intestinal epithelial cells. Rational role of amino acids in intestinal epithelial cells (Review).Int J Mol Med. 2005. 16(2): 201-4.

[35] Tannus AF, Darmaun D, Ribas DF, Oliveira JE, Marchini JS. Glutamine supplementation does not improve protein synthesis rate by the jejunal mucosa of the malnourished rat. Nutr Res, 2009. 29: 596–601. DOI:https://doi.org/10.1016/j.nutres.2009.06.009

[36] Viana ML, dos Santos RG, Generoso SV, Arantes RM, Correia MI, Cardoso VN. Pretreatment with arginine preserves intestinal barrier integrity and reduces bacterial translocation in mice. Nutrition, 2010. 26(2): 218-223. DOI:https://doi.org/10.1016/j.nut.2009.04.005

[37] Quirino IE, Correia MI, Cardoso VN. The impact of arginine on bacterial translocation in an intestinal obstruction model in rats. Clin Nutr. 2007. 26(3): 335-40. DOI:https://doi.org/10.1016/j.clnu.2006.12.007

[38] Pires W, Veneroso CE, Wanner SP, Pacheco DAS, Vaz GC, Amorim FT, Tonoli C, Soares DD, Coimbra CC. Association Between Exercise-Induced Hyperthermia and Intestinal Permeability: A Systematic Review. Sports Med. 2017, 47(7): 1389-1403. DOI:https://doi.org/10.1007/s40279-016-0654-2

[39] Gobert AP1, Cheng Y, Akhtar M, Mersey BD, Blumberg DR, Cross RK, Chaturvedi R, Drachenberg CB, Boucher JL, Hacker A, Casero RA Jr, Wilson KT. Protective role of arginase in a mouse model of colitis.J Immunol. 2004, 173(3): 2109-17. DOI:https://doi.org/10.4049/jimmunol.173.3.2109

[40] Singh K, Gobert AP, Coburn LA, Barry DP, Allaman M, Asim M, Luis PB, Schneider C, Milne GL, Boone HH, Shilts MH, Washington MK, Das SR, Piazuelo MB, Wilson KT.

[41] Dietary Arginine Regulates Severity of Experimental Colitis and Affects the Colonic Microbiome.Front Cell Infect Microbiol. 2019, 9: 66. DOI:https://doi.org/10.3389/fcimb.2019.00066

[42] Madden HP, Breslin RJ, Wasserkrug HL, Efron G, Barbul A.Stimulation of T cell immunity by arginine enhances survival in peritonitis. J Surg Res. 1988, 44(6): 658-63.

[43] Gianotti L, Alexander JW, Pyles T, Fukushima R. Arginine-supplemented diets improve survival in gut-derived sepsis and peritonitis by modulating bacterial clearance. The role of nitric oxide. Ann Surg. 1993, 217(6): 644-53. DOI:https://doi.org/10.1097/00000658-199306000-00006

[44] Wang X, Qiao S, Yin Y, Yue L, Wang Z, Wu G. A deficiency or excess of dietary threonine reduces protein synthesis in jejunum and skeletal muscle of young pigs. J Nutr. 2007, 137(6): 1442-6. DOI:https://doi.org/10.1093/jn/137.6.1442

[45] Munasinghe LL, Robinson JL, Harding SV, Brunton JA, Bertolo RF. Protein synthesis in mucin-producing tissues is conserved when dietary threonine is limiting in piglets. J Nutr. 2017. 147(2): 202-210. DOI:https://doi.org/10.3945/jn.116.236786

[46] Law GK, Bertolo RF, Adjiri-Awere A, Pencharz PB, Ball RO. Adequate oral threonine is critical for mucin production and gut function in neonatal piglets. Am J Physiol Gastrointest Liver Physiol. 2007, 292(5): G1293-301. DOI:https://doi.org/10.1152/ajpgi.00221.2006

[47] Mao X, Zeng X, Qiao S, Wu G, Li D Specific roles of threonine in intestinal mucosal integrity and barrier function. Front Biosci (Elite Ed). 2011, 3: 1192-200.

[48] Johansson ME, Hansson GC. Immunological aspects of intestinal mucus and mucins. Nat Rev Immunol. 2016. 16(10): 639-49. DOI:https://doi.org/10.1038/nri.2016.88

[49] Gaudichon C, Bos C, Morens C, Petzke KJ, Mariotti F, Everwand J, Benamouzig R, Daré S, Tomé D, Metges CC. Ileal losses of nitrogen and amino acids in humans and their importance to the assessment of amino acid requirements Gastroenterology. 2002, 123(1): 50-9. DOI:https://doi.org/10.1053/gast.2002.34233

[50] Wu G. Amino acids: metabolism, functions, and nutrition. Amino Acids. 2009. 37(1): 1-17. DOI:https://doi.org/10.1007/s00726-009-0269-0

[51] Trevisi P, Corrent E, Mazzoni M, Messori S, Priori D, Gherpelli Y, Simongiovanni A, Bosi P. Effect of added dietary threonine on growth performance, health, immunity and gastrointestinal function of weaning pigs with differing genetic susceptibility to Escherichia coli infection and challenged with E. coli K88ac. J Anim Physiol Anim Nutr (Berl). 2015. 99(3): 511-20. DOI:https://doi.org/10.1111/jpn.12216

[52] Chen YP, Cheng YF, Li XH, Yang WL, Wen C, Zhuang S, Zhou YM. Effects of threonine supplementation on the growth performance, immunity, oxidative status, intestinal integrity, and barrier function of broilers at the early age. Poult Sci. 2017. 96(2): 405-413. DOI:https://doi.org/10.3382/ps/pew240

[53] Effect of supplemental L-threonine on mucin 2 gene expression and intestine mucosal immune and digestive enzymes activities of laying hens in environments with high temperature and humidity.Azzam MM, Zou XT, Dong XY, Xie P.Poult Sci. 2011. 90(10): 2251-6. DOI:https://doi.org/10.3382/ps.2011-01574

[54] Coenen M, Mößeler A, Vervuert I. Fermentative gases in breath indicate that inulin and starch start to be degraded by microbial fermentation in the stomach and small intestine of the horse in contrast to pectin and cellulose. J Nutr 2006. 136:2108S–110S. DOI:https://doi.org/10.1093/jn/136.7.2108S

[55] Ratajczak W, Rył A, Mizerski A, Walczakiewicz K, Sipak O, Laszczyńska M. Immunomodulatory potential of gut microbiome-derived short-chain fatty acids (SCFAs). Acta Biochim Pol. 2019. 66(1): 1-12. DOI:https://doi.org/10.18388/abp.2018_2648

[56] Suagee-Bedore JK, Wagner AL, Girard ID. Feeding DigestaWell® buffer to horses alters the effects of starch intake on blood pH, lipopolysaccharide, and interleukin-1b. J Equine Vet Sci, 2018. 61: 36-45. DOI:https://doi.org/10.1016/j.jevs.2017.11.006

[57] Bienenstock J, Kunze W, Forsythe P. Microbiota and the gut-brain axis. Nutr Rev, 2015, 73 Suppl 1: 28-31. DOI:https://doi.org/10.1093/nutrit/nuv019

[58] 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, 99(10): 1335-47. DOI:https://doi.org/10.1113/expphysiol.2014.077982

[59] Hatayama H, Iwashita J, Kuwajima A, Abe T. The short chain fatty acid, butyrate, stimulates MUC2 mucin production in the human colon cancer cell line, LS174T. Biochem Biophys Res Commun, 2007. 356: 599–603. DOI:https://doi.org/10.1016/j.bbrc.2007.03.025

[60] Waller AP, Heigenhauser GJ, Geor RJ, Spriet LL, Lindinger MI. Fluid and electrolyte supplementation after prolonged moderate intensity exercise enhances muscle glycogen resynthesis in Standardbred horses. J Appl Physiol, 2009, 106: 91–100 DOI:https://doi.org/10.1152/japplphysiol.90783.2008

[61] Sadet-Bourgeteau S, Philippeau C, Julliand V. Effect of concentrate feeding sequence on equine hindgut fermentation parameters. Animal, 2017, 11(7): 1146-1152. DOI:https://doi.org/10.1017/S1751731116002603

[62] Doehlert DC, Moore WR. Composition of oat bran and flour prepared by three different mechanisms of dry milling. Cereal Chemistry, 1997, 74(4): 403 - 406. DOI:https://doi.org/10.1094/CCHEM.1997.74.4.403

[63] Knudsen KE, Jensen BB, Hansen I. Oat bran but not a beta-glucan-enriched oat fraction enhances butyrate production in the large intestine of pigs. J Nutr. 1993 Jul. 123(7): 1235-47. DOI:https://doi.org/10.1093/jn/123.7.1235

[64] Sadiq Butt M, Tahir-Nadeem M, Khan MK, Shabir R, Butt MS. Oat: unique among the cereals. Eur J Nutr. 2008, 47(2): 68-79. DOI:https://doi.org/10.1007/s00394-008-0698-7

[65] Rieder A, Samuelsen AB. Do cereal mixed-linked β-glucans possess immune-modulating activities ?Mol Nutr Food Res. 2012, 56(4): 536-47. DOI:https://doi.org/10.1002/mnfr.201100723

[66] Nie Y, Lin Q, Luo F. Effects of Non-Starch Polysaccharides on Inflammatory Bowel Disease. Int J Mol Sci. 2017, 18(7). pii: E1372. DOI:https://doi.org/10.3390/ijms18071372

[67] McFarlin BK, Carpenter KC, Davidson T, McFarlin MA. Baker's yeast beta glucan supplementation increases salivary IgA and decreases cold/flu symptomatic days after intense exercise. J Diet Suppl. 2013, 10(3): 171-83. DOI:https://doi.org/10.3109/19390211.2013.820248

[68] Stier H, Ebbeskotte V, Gruenwald J. Immune-modulatory effects of dietary yeast deta-1,3/1,6-D-glucan. Nutr J. 2014, 13: 38. DOI:https://doi.org/10.1186/1475-2891-13-38

[69] Wasser SP. Medicinal mushrooms as a source of antitumor and immunomodulating polysaccharides. Appl Microbiol Biotechnol, 2002, 60(3): 258-274. DOI:https://doi.org/10.1007/s00253-002-1076-7

[70] Soltanian S, Stuyven E, Cox E, Sorgeloos P, Bossier P. Beta-glucans as immunostimulant in vertebrates and invertebrates. Crit Rev Microbiol. 2009, 35(2): 109-38. DOI:https://doi.org/10.1080/10408410902753746

[71] Samuelsen AB, Schrezenmeir J, Knutsen SH. Effects of orally administered yeast-derived beta-glucans: a review. Mol Nutr Food Res. 2014, 58(1): 183-93. DOI:https://doi.org/10.1002/mnfr.201300338

[72] Chen SN, Chang CS, Chen S, Soni M. Subchronic toxicity and genotoxicity studies of Antrodia mushroom β-glucan preparation. Regul Toxicol Pharmacol. 2018, 92: 429-438. DOI:https://doi.org/10.1016/j.yrtph.2017.12.022

[73] Chen SN, Nan FH, Chen S, Wu JF, Lu CL, Soni MG. Safety assessment of mushroom β-glucan: subchronic toxicity in rodents and mutagenicity studies. Food Chem Toxicol, 2011, 49(11): 2890-2898. DOI:https://doi.org/10.1016/j.fct.2011.08.007

[74] Vine DF, Charman SA, Gibson PR, Sinclair AJ, Porter CJ. Effect of dietary fatty acids on the intestinal permeability of marker drug compounds in excised rat jejunum. J Pharm Pharmacol, 2002. 54(6): 809-819. DOI:https://doi.org/10.1211/0022357021779159

[75] Xiao G, Tang L, Yuan F, Zhu W, Zhang S, Liu Z, Geng Y, Qiu X, Zhang Y, Su L. Eicosapentaenoic acid enhances heat stress-impaired intestinal epithelial barrier function in Caco-2 cells. PLoS One, 2013. 8(9): e73571 DOI:https://doi.org/10.1371/journal.pone.0073571

[76] Kunisawa J, Hashimoto E, Inoue A, Nagasawa R, Suzuki Y, Ishikawa I, Shikata S, Arita M, Aoki J, Kiyono H. Regulation of intestinal IgA responses by dietary palmitic acid and its metabolism. J Immunol. 2014, 193(4): 1666-71. DOI:https://doi.org/10.4049/jimmunol.1302944

[77] Turner D, Steinhart AH, Griffiths AM. Omega 3 fatty acids (fish oil) for maintenance of remission in ulcerative colitis. Cochrane Database Syst Rev, 2007, 18(3): CD006443. DOI:https://doi.org/10.1002/14651858.CD006443.pub2

[78] Miura S, Tsuzuki Y, Hokari R, Ishii H. Modulation of intestinal immune system by dietary fat intake: relevance to Crohn's disease. J Gastroenterol Hepatol. 1998, 13(12): 1183-90.

[79] Chen H, Qiu S, Gan J, Li Z, Nirasawa S, Yin L.New insights into the antioxidant activity and components in crude oat oil and soybean oil. J Food Sci Technol. 2016, 53(1): 808-15. DOI:https://doi.org/10.1007/s13197-015-1991-0

[80] Bergamo P, Gogliettino M, Palmieri G, Cocca E, Maurano F, Stefanile R, Balestrieri M, Mazzarella G, David C, Rossi M. Conjugated linoleic acid protects against gliadin-induced depletion of intestinal defenses. Mol Nutr Food Res. 2011, 55 Suppl 2: S248-56. DOI:https://doi.org/10.1002/mnfr.201100295

[81] Serizawa H, Miura S, Imaeda H, Tanaka S, Kimura H, Tsuzuki Y, Jing-Yang H, Toda K, Hamada Y, Tsuchiya M, Ishii H. Reversal of altered intestinal mucosal immunity in rats fed elemental diet by supplementation of oleic acid. J Gastroenterol Hepatol. 1996, 11(9): 811-8.

[82] Park JH, Grandjean CJ, Hart MH, Baylor JM, Vanderhoof JA. Effects of dietary linoleic acid on mucosal adaptation after small bowel resection. Digestion. 1989, 44(2): 57-65. DOI:https://doi.org/10.1159/000199893

[83] Jenkins AP, Thompson RP. Does the fatty acid profile of dietary fat influence its trophic effect on the small intestinal mucosa? Gut. 1993, 34(3): 358-64.DOI:https://doi.org/10.1136/gut.34.3.358

[84] 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. DOI:https://doi.org/10.1371/journal.pone.0041484

[85] Garrett LA, Brown R, Poxton IR. A comparative study of the intestinal microbiota of healthy horses and those suffering from equine grass sickness. Vet Microbiol, 2002, 87: 81–88.

[86] Milinovich GJ, Trott DJ, Burrell PC, Croser EL, Al Jassim RA, Morton JM, van Eps AW, Pollitt CC. Fluorescence in situ hybridization analysis of hindgut bacteria associated with the development of equine laminitis. Environ Microbiol, 2007, 9: 2090–2100. DOI:https://doi.org/10.1111/j.1462-2920.2007.01327.x

[87] Costa MC, Weese JS. Understanding the intestinal microbiome in health and disease. Vet Clin North Am Equine Pract, 2018, 34(1): 1-12 DOI:https://doi.org/10.1016/j.cveq.2017.11.005

[88] Ericsson AC, Johnson PJ, Lopes MA, Perry SC, Lanter HR. (2016) AA, Bamba T, Sasaki M. A microbiological map of the healthy equine gastrointestinal tract. PLoS ONE 2016. 11(11): e0166523. DOI:https://doi.org/10.1371/journal.pone.0166523

[89] Grimm P, Philippeau C, Julliand V. Faecal parameters as biomarkers of the equine hindgut microbial ecosystem under dietary fiber change. Animal, 2017, 11(7): 1136-1145. DOI:https://doi.org/10.1017/S1751731116002779

[90] Greenwood-Van Meerveld B, Johnson AC, Grundy D. Gastrointestinal physiology and function. Handb Exp Pharmacol, 2017. 239: 1-16. DOI:https://doi.org/10.1007/164_2016_118

[91] 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 Vet Res, 2015, 11: 19. DOI:https://doi.org/10.1186/s12917-015-0335-7

[92] Andrade ME, Araújo RS, de Barros PA, Soares AD, Abrantes FA, Generoso Sde V, Fernandes SO, Cardoso VN. The role of immunomodulators on intestinal barrier homeostasis in experimental models. Clin Nutr, 2015, 34(6): 1080-1087. DOI:https://doi.org/10.1016/j.clnu.2015.01.012

[93] Rao RK, Samak G. Protection and restitution of gut barrier by probiotics: nutritional and clinical implications. Curr Nutr Food Sci, 2013, 9: 99e107.

[94] Souza TC, Zacarías MF, Silva AM, Binetti A, Reinheimer J, Nicoli JR, Vinderola G. Cell viability and immunostimulating and protective capacities of Bifidobacterium longum 51A are differentially affected by technological variables in fermented milks. J Appl Micriobiol, 2012, 112(6): 1184–1192. DOI:https://doi.org/10.1111/j.1365-2672.2012.05280.x

[95] Yun B, Minyu Song |M, Park DJ, Oh S. Beneficial effect of Bifidobacterium longum ATCC 15707 on survival rate of clostridium difficile infection in mice. Korean J Food Sci Anim Resour, 2017. 37(3): 368–375. DOI:https://doi.org/10.5851/kosfa.2017.37.3.368

[96] Philippe D, Heupel E, Blum-Sperisen S, Riedel CU.Treatment with Bifidobacterium bifidum 17 partially protects mice from Th1-driven inflammation in a chemically induced model of colitis. Int J Food Microbiol. 2011, 149(1): 45-9. DOI:https://doi.org/10.1016/j.ijfoodmicro.2010.12.020

[97] Jang SE, Hyam SR, Han MJ, Kim SY, Lee BG, Kim DH. Lactobacillus brevis G-101 ameliorates colitis in mice by inhibiting NF-κB, MAPK and AKT pathways and by polarizing M1 macrophages to M2-like macrophages. J Appl Microbiol, 2013, 115(3): 888-896. DOI:https://doi.org/10.1111/jam.12273

[98] Ueno N, Fujiya M, Segawa S, Nata T, Moriichi K, Tanabe H, Mizukami Y, Kobayashi N, Ito K, Kohgo Y. Heat-killed body of Lactobacillus brevis SBC8803 ameliorates intestinal injury in a murine model of colitis by enhancing the intestinal barrier function. Inflamm Bowel Dis, 2011, 17: 2235e50. DOI:https://doi.org/10.1002/ibd.21597

[99] Shiou S-R, Yu Y, Guo Y, He S-M, Mziray-Andrew CH, Hoenig J, Sun J, Petrof EO, Claud EC. Synergistic protection of combined probiotic conditioned media against neonatal necrotizing enterocolitis-like intestinal injury. PLoS One, 2013, 8: 1e12. DOI:https://doi.org/10.1371/journal.pone.0065108

[100] Mennigen R, Nolte K, Rijcken E, Utech M, Loeffler B, Senninger N, Bruewer M.Probiotic mixture VSL#3 protects the epithelial barrier by maintaining tight junction protein expression and preventing apoptosis in a murine model of colitis. Am J Physiol Gastrointest Liver Physiol. 2009, 296(5): G1140-9. DOI:https://doi.org/10.1152/ajpgi.90534.2008

[101] Peys E, Varghese J, Suresh P, Vandenkerckhove J, Van hemel J, Chaniyilparampu RN, Sas B. Effects of Bacillus subtilis ‘PB6’ (ATCC - PTA 6737) on Clostridium difficile associated diarrhea (CDAD) and inflammatory bowel disease (IBD) in animal models. Am J Infectious Diseases, 2007, 3(4): 255-266. DOI:https://doi.org/10.3844/ajidsp.2007.255.266

[102] Selvam R, Maheswari P, Kavitha P, Ravichandran M, Sas B, Ramchand CN. Effect of Bacillus subtilis PB6, natural probiotic on colon mucosal inflammation and plasma cytokines levels in inflammatory bowel disease. Indian J Biochem Biophys. 2009, 46(1): 79-85.

[103] Abudabos AM. Bacillus subtilis PB6 based-probiotic (CloSTATTM) improves intestinal morphological and microbiological status of broiler chickens under Clostridium perfringens challenge. Int J Agric Biol, 2013, 15(6): 978-982.

[104] Jayaraman S, Thangavel G, Kurian H, Mani R, Mukkalil R, Chirakkal H. Bacillus subtilis PB6 improves intestinal health of broiler chickens challenged with Clostridium perfringens-induced necrotic enteritis. Poult Sci. 2013, 92(2): 370-374. DOI:https://doi.org/10.3382/ps.2012-02528

[105] Hu L, Peng X, Chen H, Yan C, Liu Y, Xu Q, Fang Z, Lin Y, Xu S, Feng B, Li J, Wu, Che L. Effects of intrauterine growth retardation and Bacillus subtilis PB6 supplementation on growth performance, intestinal development and immune function of piglets during the suckling period. Eur J Nutr. 2017, 56(4): 1753-1765. DOI:https://doi.org/10.1007/s00394-016-1223-z

[106] Diab SS, Songer G, Uzal FA. Clostridium difficile infection in horses: a review. Vet Microbiol, 2013, 167(1-2): 42-49 DOI:https://doi.org/10.1016/j.vetmic.2013.03.032

[107] Burke MA, Moore SA. Bacillus subtilis strain PB6 demonstrates growth inhibition toward equine-specific bacterial pathogens. J. Eq Vet Sci. 2017, 58: 84-88.DOI:https://doi.org/10.1016/j.jevs.2017.08.016

[108] EFSA 2009. SCIENTIFIC OPINION Safety and efficacy of the product ColiCure (Escherichia coli) as a feed additive for horses. The EFSA Journal, 2009, 989, 1-14.DOI:https://doi.org/10.2903/j.efsa.2009.989

[109] Rakowska R, Sadowska A, Dybkowska E, Świderski F. Spent yeast as natural source of functional food additives. Rocz Panstw Zakl Hig. 2017, 68(2): 115-121.

[110] Generoso SV, Viana M, Santos R, Martins FS, Machado JA, Arantes RM, Nicoli JR, Correia MI, Cardoso VN. Saccharomyces cerevisiae strain UFMG 905 protects against bacterial translocation, preserves gut barrier integrity and stimulates the immune system in a murine intestinal obstruction model. Arch Microbiol, 2010, 192(6): 477-484.DOI:https://doi.org/10.1007/s00203-010-0574-8

[111] Generoso SV, Viana ML, Santos RG, Arantes RM, Martins FS, Nicoli JR, Machado JA, Correia MI, Cardoso VN. Protection against increased intestinal permeability and bacterial translocation induced by intestinal obstruction in mice treated with viable and heat-killed Saccharomyces boulardii. Eur J Nutr. 2011, 50(4): 261-9. DOI:https://doi.org/10.1007/s00394-010-0134-7

[112] Martins FS, Vieira AT, Elian SD, Arantes RM, Tiago FC, Sousa LP, Araújo HR, Pimenta PF, Bonjardim CA, Nicoli JR, Teixeira MM. Inhibition of tissue inflammation and bacterial translocation as one of the protective mechanisms of Saccharomyces boulardii against Salmonella infection in mice. Microbes Infect. 2013, 15(4): 270-279. DOI:https://doi.org/10.1016/j.micinf.2012.12.007

[113] Desrochers AM, Dolente BA, Roy MF, Boston R, Carlisle S. Efficacy of Saccharomyces boulardii for treatment of horses with acute enterocolitis. J Am Vet Med Assoc. 2005, 227(6): 954-959.

[114] Boyle AG, Magdesian KG, Durando MM, Gallop R, Sigdel S. Saccharomyces boulardii viability and efficacy in horses with antimicrobial-induced diarrhoea. Vet Rec. 2013, 172(5): 128 DOI:https://doi.org/10.1136/vr.100833

[115] 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 diet. J Anim Sci. 2002, 80: 2600–2609. DOI:https://doi.org/10.2527/2002.80102600x

[116] 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. DOI:https://doi.org/10.2527/jas.2008-1602

[117] Schoster A. Probiotic use in equine gastrointestinal disease. Vet Clin North Am Equine Pract. 2018, 34(1): 13-24. DOI:https://doi.org/10.1016/j.cveq.2017.11.004

[118] Shanahan F. A commentary on the safety of probiotics. Gastroenterol Clin North Am. 2012, 41: 869–876. DOI:https://doi.org/10.1016/j.gtc.2012.08.006

[119] Parraga ME, Spier SJ, Thurmond M, Hirsh D. A clinical trial of probiotic administration for prevention of Salmonella shedding in the postoperative period in horses with colic. J Vet Intern Med. 1997, 11:36–41. DOI:https://doi.org/10.1016/j.gtc.2012.08.006

Downloads

Issue

Article Type

Articles