Nutrition Research
Volume 30, Issue 6 , Pages 427-434 , June 2010

Butyrylated starch increases large bowel butyrate levels and lowers colonic smooth muscle contractility in rats

  • Balazs H. Bajka

      Affiliations

    • CSIRO Preventative Health National Research Flagship, Food and Nutritional Sciences, Adelaide, South Australia 5000, Australia
    • Discipline of Physiology, The School of Molecular & Biomedical Sciences, The University of Adelaide, South Australia 5000, Australia
    • ,
  • Julie M. Clarke

      Affiliations

    • CSIRO Preventative Health National Research Flagship, Food and Nutritional Sciences, Adelaide, South Australia 5000, Australia
    • ,
  • David. L. Topping

      Affiliations

    • CSIRO Preventative Health National Research Flagship, Food and Nutritional Sciences, Adelaide, South Australia 5000, Australia
    • ,
  • Lynne Cobiac

      Affiliations

    • Department of Nutrition and Dietetics, School of Medicine, Flinders University, South Australia 5042, Australia
    • ,
  • Mahinda Y. Abeywardena

      Affiliations

    • CSIRO Preventative Health National Research Flagship, Food and Nutritional Sciences, Adelaide, South Australia 5000, Australia
    • ,
  • Glen S. Patten

      Affiliations

    • CSIRO Preventative Health National Research Flagship, Food and Nutritional Sciences, Adelaide, South Australia 5000, Australia
    • Corresponding Author InformationCorresponding author. CSIRO Food and Nutritional Sciences, Kintore Avenue, PO Box 10041, Adelaide BC 5000, Australia. Tel.: +61 8 8303 8956; fax: +61 8 8303 8899.

Received 15 April 2010 ,Revised 6 June 2010 ,Accepted 7 June 2010.

References 

  1. Cummings JH, Macfarlane GT. The control and consequences of bacterial fermentation in the human colon. J Appl Bacteriol. 1991;70:443–459
  2. Topping DL, Clifton PM. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol Rev. 2001;81:1031–1064
  3. Brouns F, Kettlitz B, Arrigoni E. Resistant starch and the “butyrate revolution”. Trends Food Sci Technol. 2002;13:251–261
  4. Andoh A, Tsujikawa T, Fujiyama Y. Role of dietary fiber and short-chain fatty acids in the colon. Curr Pharm Des. 2003;9:347–358
  5. Sakata T. Stimulatory effect of short-chain fatty acids on epithelial cell proliferation in the rat intestine: a possible explanation for trophic effects of fermentable fibre, gut microbes and luminal trophic factors. Br J Nutr. 1987;58:95–103
  6. Levy P, Robin H, Bertrand F, Kornprobst M, Capeau J. Butyrate-treated colonic Caco-2 cells exhibit defective integrin-mediated signaling together with increased apoptosis and differentiation. J Cell Physiol. 2003;197:336–347
  7. Kien CL, Blauwiekel R, Bunn JY, Jetton TL, Frankel WL, Holst JJ. Cecal infusion of butyrate increases intestinal cell proliferation in piglets. J Nutr. 2007;137:916–922
  8. Yajima T. Contractile effect of short-chain fatty acids on the isolated colon of the rat. J Physiol (Lond). 1985;368:667–678
  9. Rondeau MP, Meltzer K, Michel KE, McManus CM, Washabau RJ. Short chain fatty acids stimulate feline colonic smooth muscle contraction. J Feline Med Surg. 2003;5:167–173
  10. Mitsui R, Ono S, Karaki S, Kuwahara A. Neural and non-neural mediation of propionate-induced contractile responses in the rat distal colon. Neurogastroenterol Motil. 2005;17:585–594
  11. Yajima T, Kojima K, Tohyama K, Mutai M. Alteration in sensitivity of transmural electrical response to propionate in rat colon after chronic luminal infusion of short-chain fatty acids. Life Sci. 1983;32:1073–1079
  12. Annison G, Illman RJ, Topping DL. Acetylated, propionylated or butyrylated starches raise large bowel short-chain fatty acids preferentially when fed to rats. J Nutr. 2003;133:3523–3528
  13. Bajka BH, Topping DL, Cobiac L, Clarke JM. Butyrylated starch is less susceptible to enzymic hydrolysis and increases large-bowel butyrate more than high-amylose maize starch in the rat. Br J Nutr. 2006;96:276–282
  14. Clarke JM, Bird AR, Topping DL, Cobiac L. Excretion of starch and esterified short-chain fatty acids by ileostomy subjects after the ingestion of acylated starches. Am J Clin Nutr. 2007;86:1146–1151
  15. Bajka BH, Clarke JM, Cobiac L, Topping DL. Butyrylated starch protects colonocyte DNA against dietary protein-induced genetic damage in rats. Carcinogenesis. 2008;29:2167–2174
  16. National Health and Medical Research Council, Australian Research Council and The Australian Vice-Chancellors' Committee . Australian code of practice for the care and use of animals for scientific purposes. 7th ed.. 2004;http://wwwnhmrcgovau/publications/synopses/ea16synhtm
  17. Australian Government, National Health and Medical Research Council . Guidelines to promote the well being of animals used for scientific purposes: the assessment and alleviation of pain and distress in research animals. Expert Working Group of the Animal Welfare Committee of the NH&MRC. 2008;(print). http://www.nhmrc.gov.au
  18. Murase M, Kimura Y, Nagata Y. Determination of portal short-chain fatty acids in rats fed various dietary fibers by capillary gas chromatography. J Chromatogr B Biomed Appl. 1995;664:415–420
  19. Patten GS, Head RJ, Abeywardena MY, McMurchie EJ. An apparatus to assay opioid activity in the infused lumen of the intact isolated guinea pig ileum. J Pharmacol Toxicol Methods. 2001;45:39–46
  20. Patten GS, Abeywardena MY, McMurchie EJ, Jahangiri A. Dietary fish oil increases acetylcholine- and eicosanoid-induced contractility of isolated rat ileum. J Nutr. 2002;132:2506–2513
  21. Patten GS, Adams MJ, Dallimore JA, Rogers PF, Topping DL, Abeywardena MY. Restoration of depressed prostanoid-induced ileal contraction in spontaneously hypertensive rats by dietary fish oil. Lipids. 2005;40:69–79
  22. Kurjak M, Sattler D, Schusdziarra V, Allescher HD. Characterization of prejunctional and postjunctional muscarinic receptors of the ascending reflex contraction of the ileum. J Pharmacol Exp Ther. 1999;290:893–900
  23. Sugimori S, Kadowaki M, Yoneda S, Yamanouchi M, Nakano H, Takaki M. New method for evaluating intestinal contractions in guinea pig by curve fitting. Dig Dis Sci. 2000;45:136–144
  24. Clarke JM, Topping DL, Bird AR, Young GP, Cobiac L. Effects of high-amylose maize starch and butyrylated high-amylose maize starch on azoxymethane-induced intestinal cancer in rats. Carcinogenesis. 2008;29:2190–2194
  25. Ichikawa H, Sakata T. Effect of L-lactic acid, short-chain fatty acids, and pH in cecal infusate on morphometric and cell kinetic parameters of rat cecum. Dig Dis Sci. 1997;42:1598–1610
  26. Gibson PR, Kilias D, Rosella O, Day JM, Abbott M, Finch CF, et al. Effect of topical butyrate on rectal epithelial kinetics and mucosal enzyme activities. Clin Sci. 1998;94:671–676
  27. Ichikawa H, Shineha R, Satomi S Sakata T. Gastric or rectal instillation of short-chain fatty acids stimulates epithelial cell proliferation of small and large intestine in rats. Dig Dis Sci. 2002;47:1141–1146
  28. Martin LJ, Dumon HJ, Lecannu G, Champ MM. Potato and high-amylose maize starches are not equivalent producers of butyrate for the colonic mucosa. Br J Nutr. 2000;84:689–696
  29. Stark A, Nyska A, Madar Z. Metabolic and morphometric changes in small and large intestine in rats fed high-fiber diets. Toxicol Pathol. 1996;24:166–171
  30. Squires PE, Rumsey RD, Edwards CA, Read NW. Effect of short-chain fatty acids on contractile activity and fluid flow in rat colon in vitro. Am J Physiol. 1992;262:G813–G817
  31. Cherbut C, Ferrier L, Roze C, Anini Y, Blottiere H, Lecannu G, et al. Short-chain fatty acids modify colonic motility through nerves and polypeptide YY release in the rat. Am J Physiol. 1998;275:G1415–G1422
  32. Binder HJ, Mehta P. Short-chain fatty acids stimulate active sodium and chloride absorption in vitro in the rat distal colon. Gastroenterology. 1989;96:989–996
  33. Dass NB, John AK, Bassil AK, Crumbley CW, Shehee WR, Maurio FP, et al. The relationship between the effects of short-chain fatty acids on intestinal motility in vitro and GPR43 receptor activation. Neurogastroenterol Motil. 2007;19:66–74
  34. Depoortere I, Van Assche G, Thijs T, Geboes K, Peeters TL. Differential changes in ACh-, motilin-, substance P-, and K(+)-induced contractility in rabbit colitis. Am J Physiol Gastrointest Liver Physiol. 1999;277:G61–G68
  35. Maggi CA, Patacchini R, Santicioli P, Giuliani S, Turini D, Barbanti G, et al. Human isolated small intestine: motor responses of the longitudinal muscle to field stimulation and exogenous neuropeptides. Naunyn Schmiedebergs Arch Pharmacol. 1989;339:415–423
  36. Mohajer B, Ma TY. Eicosanoids and the small intestine. Prostaglandins Other Lipid Mediat. 2000;61:125–143
  37. Frantzides CT, Lianos EA, Wittmann D, Greenwood B, Edmiston CE. Prostaglandins and modulation of small bowel myoelectric activity. Am J Physiol. 1992;262:G488–G497
  38. Haschke G, Schafer H, Diener M. Effect of butyrate on membrane potential, ionic currents and intracellular Ca2+ concentration in cultured rat myenteric neurones. Neurogastroenterol Motil. 2002;14:133–142
  39. Masliah C, Cherbut C, Bruley des Varannes S, Barry JL, Dubois A, et al. Short-chain fatty acids do not alter jejunal motility in man. Dig Dis Sci. 1992;37:193–197
  40. Cuche G, Cuber JC, Malbert CH. Ileal short-chain fatty acids inhibit gastric motility by a humoral pathway. Am J Physiol Gastrointest Physiol. 2000;279:G925–G930
  41. Fukumoto S, Tatewaki M, Yamada T, Fujimiya M, Mantyh C, Voss M, et al. Short-chain fatty acids stimulate colonic transit via intraluminal 5-HT release in rats. Am J Physiol Regul Integr Comp Physiol. 2003;284:R1269–R1276
  42. Grider JR, Piland BE. The peristaltic reflex induced by short-chain fatty acids is mediated by sequential release of 5-HT and neuronal CGRP but not BDNF. Gastroenterology. 2008;135:1163–1167
  43. Vanhoutvin SA, Troost FJ, Kilkens TO, Lindsay PJ, Hamer HM, Jonkers DM, et al. The effects of butyrate enemas on visceral perception in healthy volunteers. Neurogastroenterol Motil. 2009;21:952–958
  44. Patten GS, Conlon MA, Bird AR, Adams MJ, Topping DL, Abeywardena MY. Interactive effects of dietary resistant starch and fish oil on short chain fatty acid production and agonist-induced contractility in young rats. Dig Dis Sci. 2006;51:254–261
  45. Grider JR, Foxx-Orenstein AE. Mediators and regulation of peristalsis. Curr Opin Gastroenterol. 1999;15:22–25
  46. Martinolle JP, Garcia-Villar R, Fioramonti J. Bueno. Altered contractility of circular and longitudinal muscle in TNBS-inflamed guinea pig ileum. Am J Physiol Gastrointest Liver Physiol. 1997;272:G1258–G1267
  47. Wells RW, Blennerhassett MG. Divergent changes to muscarinic and serotonergic signalling following colitis. Gut. 2005;54:1699–1706

PII: S0271-5317(10)00101-6

doi: 10.1016/j.nutres.2010.06.003

Nutrition Research
Volume 30, Issue 6 , Pages 427-434 , June 2010

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