Advertisement

Digestive Diseases and Sciences

, Volume 51, Issue 2, pp 254–261 | Cite as

Interactive Effects of Dietary Resistant Starch and Fish Oil on Short-Chain Fatty Acid Production and Agonist-Induced Contractility in Ileum of Young Rats

  • Glen S. PattenEmail author
  • Michael A. Conlon
  • Anthony R. Bird
  • Michael J. Adams
  • David L. Topping
  • Mahinda Y. Abeywardena
Motility

Abstract

We have shown independently that dietary fiber and n−3 fatty acids can affect gut function. This study investigated the interactive effects of resistant starch (RS) (as high amylose maize starch [HAMS]) and tuna fish oil on ileal contractility. Four-week-old male Sprague Dawley rats were fed 4 diets that contained 100 g/kg fat as sunflower oil or tuna fish oil, with 10% fiber supplied as α -cellulose or HAMS for 6 weeks. Fish oil feeding led to higher ileal n-3 fatty acid levels (mainly as DHA) and higher agonist-induced maximal contractility with an RS effect noted for carbachol. HAMS-containing diets resulted in lower colonic pH and higher total short-chain fatty acids (SCFA), but not for butyrate with fish oil. Low prostanoid responses in young rats were enhanced by fish oil independent of RS. The order of muscarinic receptor subtype responses were different compared to older rats; fish oil feeding altered the sensitivity of the M1 receptor subtype. Although little interactive effects were demonstrated, these data suggest developmental changes in ileal receptor systems with independent effects of RS and fish oil on some bowel properties in juvenile rats.

Key Words

resistant starch fish oil SCFA young rats ileal contractility muscarinic prostanoid 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Topping DL, Clifton PM: Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol Rev 81:1031–1064, 2001PubMedGoogle Scholar
  2. 2.
    Henningsson AM, Margareta E, Nyman GL, Bjorck ME: Influences of dietary adaptation and source of resistant starch on short-chain fatty acids in the hindgut of rats. Br J Nutr 89:319–327, 2003CrossRefPubMedGoogle Scholar
  3. 3.
    von Engelhardt W, Bartels J, Kirschberger S, zu Duttingdorf M, Busche R: Role of short-chain fatty acids in the hind gut. Vet Q 20(Suppl 3):S52–S59, 1998PubMedGoogle Scholar
  4. 4.
    Gil A: Polyunsaturated fatty acids and inflammatory diseases. Biomed Pharmacother 56:388–396, 2002CrossRefPubMedGoogle Scholar
  5. 5.
    Shimizu T, Igarashi J, Ohtuka Y, Ogushi S, Kaneko K, Yamashiro Y: Effects of n-3 polyunsaturated fatty acids and vitamin E on colonic mucosal leukotriene generation, lipid peroxidation, and microcirculation in rats with experimental colitis. Digestion 63:49–54, 2001CrossRefPubMedGoogle Scholar
  6. 6.
    Singer P, Wirth M: Can n-3 PUFA reduce cardiac arrhythmias? Results of a clinical trial. Prost Leukot Essent Fatty Acids 71:153–159, 2004Google Scholar
  7. 7.
    Stulnig TM: Immunomodulation by polyunsaturated fatty acids: mechanism and effects. Int Archiv Allergy Immunol 132:310–321, 2003Google Scholar
  8. 8.
    Hashimoto M, Hossain S, Yamasaki H, Yazawa K, Masumura S: Effects of eicosapentaenoic acid and docosahexaenoic acid on plasma membrane fluidity of aortic endothelial cells. Lipids 34:1297–1304, 1999PubMedGoogle Scholar
  9. 9.
    Vasandani C, Kafrouni AI, Caronna A, et al.: Upregulation of hepatic LDL transport by n-3 fatty acids in LDL receptor knockout mice. J Lipid Res 43:772–784, 2002PubMedGoogle Scholar
  10. 10.
    Patten GS, Bird RB, Topping DL, Abeywardena MY: Effects of convenience rice congee supplemented diets on guinea pig whole animal and gut growth, caecal digesta SCFA and in vitro. ileal contractility. Asia Pac J Clin Nutr 13:92–100, 2004PubMedGoogle Scholar
  11. 11.
    Patten GS, Bird AR, Topping DL, Abeywardena MY: Dietary fish oil alters the sensitivity of guinea pig ileum to electrically driven contractions and 8-iso.-PGE2. Nutr Res 22:1413–1426, 2002CrossRefGoogle Scholar
  12. 12.
    Patten GS, Abeywardena MY, McMurchie EJ, Jahangiri A: Dietary fish oil increases acetylcholine- and eicosanoid-induced contractility of isolated rat ileum. J Nutr 132:2506–2513, 2002PubMedGoogle Scholar
  13. 13.
    Muir JG, O'Dea K: Validation of an in vitro. assay for predicting the amount of starch that escapes digestion in the small intestines of humans. Am J Clin Nutr 57:540–546, 1993PubMedGoogle Scholar
  14. 14.
    Patten GS, Adams JA, Dallimore JA, Abeywardena MY: Depressed prostanoid-induced contractility of gut in spontaneously hypertensive rats (SHR) not affected by level of dietary fat. J Nutr 134:2924–2929, 2004PubMedGoogle Scholar
  15. 15.
    Coleman LJ, Landstrom EK, Royle PJ, Bird AR, McIntosh GH: A diet containing alpha-cellulose and fish oil reduces aberrant crypt foci formation and modulates other possible markers for colon cancer risk in azoxymethane-treated rats. J Nutr 132:2312–2318, 2002PubMedGoogle Scholar
  16. 16.
    Conlon MA, Bird AR: Interactions of dietary fibre and resistant starch with oil on genetic damage in the rat colon. Asia Pac J Clin Nutr 12:S54, 2003PubMedGoogle Scholar
  17. 17.
    Shimizu T, Fujii T, Suzuki R, et al.: Effects of highly purified eicosapentaenoic acid on erythrocyte fatty acid composition and leukocyte and colonic mucosa leukotriene B4 production in children with ulcerative colitis. J Pediatr Gastroenterol Nutr 37:581–585, 2003PubMedGoogle Scholar
  18. 18.
    Nakanishi S, Kataoka K, Kuwahara T, Ohnishi Y: Effects of high amylose maize starch and Clostridium butyricum. on metabolism in colonic microbiota and formation of azoxymethane-induced aberrant crypt foci in the rat colon. Microbiol Immunol 47:951–958, 2003PubMedGoogle Scholar
  19. 19.
    NHMRC Australian code of practice for the care and use of animals for scientific purposes, 6th ed. 1997, Canberra, ACT, 2601, published by the Australian GovernmentGoogle Scholar
  20. 20.
    Reeves PG, Nielson FH, Fahey GC: AIN-93 diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123:1939–1951, 1993PubMedGoogle Scholar
  21. 21.
    Muir JG, Birkett A, Brown I, Jones G, O'Dea K: Food processing and maize variety affects the amount of starch escaping digestion in the small intestine. Am J Clin Nutr 61:82–89, 1995PubMedGoogle Scholar
  22. 22.
    Patten GS, Head RJ, Abeywardena MY, McMurchie EJ: An apparatus to assay opioid activity in the perfused lumen of the intact isolated ileum. J Pharmacol Toxicol Meth 45:39–46, 2001CrossRefGoogle Scholar
  23. 23.
    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 40:69–79, 2004Google Scholar
  24. 24.
    Kendall CW, Emam A, Augustin LS, Jenkins DJ: Resistant starch and health. J AOAC Int 87:769–774, 2004PubMedGoogle Scholar
  25. 25.
    Scheppach W, Weiler F: The butyrate story: old wine in new bottles. Curr Opin Clin Nutr Metab Care 7:563–567, 2004PubMedGoogle Scholar
  26. 26.
    McManus CM, Michel KE, Simon DM, Wahabau RJ: Effect of short-chain fatty acids on contraction of smooth muscle in the canine colon. Am J Vet Res 63:295–300, 2002PubMedGoogle Scholar
  27. 27.
    Rondeau MP, Meltzer K, Michel KE, McManus CM, Washabau RJ: Short chain fatty acids stimulate feline colonic smooth muscle contraction. J Feline Med Surg 5:167–173, 2003CrossRefPubMedGoogle Scholar
  28. 28.
    Cherbut C: Motor effects of short-chain fatty acids and lactate in the gastrointestinal tract. Proc Nutr Soc 62:95–99, 2003CrossRefPubMedGoogle Scholar
  29. 29.
    Le Poul E, Loison C, Struyf S, et al.: Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation. J Biol Chem 278:25481–25489, 2003CrossRefPubMedGoogle Scholar
  30. 30.
    Sales ME, Sterin-Borda L, Rodriguez M, Borda ES: Intracellular signals coupled to different rat ileal muscarinic receptor subtypes. Cell Signal 9:373–378, 1997CrossRefPubMedGoogle Scholar
  31. 31.
    Del Castillo IC, Alvarez JG, Freedman SD, et al.: Docosahexaenoic acid selectively augments muscarinic stimulation of epithelial Cl secretion. J Surg Res 110:338–343, 2003CrossRefPubMedGoogle Scholar
  32. 32.
    Farkas E, de Wilde MC, Kiliaan AJ, Luiten PG: Systemic effects of dietary n-3 PUFA supplementation accompanying changes in CNS parameters in cerebral hypoperfusion. Ann NY Acad Sci 977:77–86, 2002PubMedGoogle Scholar
  33. 33.
    Zhang L: Muscarinic receptors in developing rat colon. Eur J Pharmacol 304:211–219, 1996CrossRefPubMedGoogle Scholar
  34. 34.
    Ehlert FJ, Sawyer GW, Esqueda EE: Contractile role of M2 and M3 muscarinic receptors in gastrointestinal smooth muscle. Life Sci 64:387–394, 1999CrossRefPubMedGoogle Scholar
  35. 35.
    Oyachi N, Lakshmanan J, Ahanya SN, Bassiri MD, Atkinson JB, Ross MG: Development of ovine fetal ileal motility: role of muscarinic receptor subtypes. Am J Obstet Gynecol 189:953–957, 2003CrossRefPubMedGoogle Scholar
  36. 36.
    Unno T, Inaba T, Ohashi H, Takewaki T, Komori S: Role of Ca2+ mobilization on muscarinic receptor-mediated membrane depolarization in guinea pig ileal smooth muscle cells. Jpn J Pharmacol 84:431–437, 2000CrossRefPubMedGoogle Scholar
  37. 37.
    Duchen K, Bjorksten B: Polyunsaturated n-3 fatty acids and the development of atopic disease. Lipids 36:1033–1042, 2001PubMedGoogle Scholar
  38. 38.
    Oddy WH, de Klerk NH, Kendall GE, Mihrshahi S, Peat JK: Ratio of omega-6 to omega-3 fatty acids and childhood asthma. J Asthma 41:319–326, 2004PubMedGoogle Scholar
  39. 39.
    Prescott SL, Calder PC: N-3 polyunsaturated fatty acids and allergic disease. Curr Opin Clin Nutr Metab Care 7:123–129, 2004PubMedGoogle Scholar
  40. 40.
    Nelson TL, Hickey MS: Acute changes in dietary omega-3 fatty acid intake lowers soluble interleukin-6 receptor in healthy adult normal weight and overweight males. Cytokine 26: 195–201, 2004CrossRefPubMedGoogle Scholar
  41. 41.
    Alpigiani MG, Ravera G, Buzzanca C, Devescovi R, Fiore P, Iester A: The use of n-3 fatty acids in chronic juvenile arthritis. Pediatr Med Chir 18:387–390, 1996PubMedGoogle Scholar
  42. 42.
    James MJ, Proudman SM, Cleland LG: Dietary n-3 fats as adjunctive therapy in a prototypic inflammatory disease: issues and obstacles for use in rheumatoid arthritis. Prost Leukot Essent Fatty Acids 68:399–405, 2003Google Scholar
  43. 43.
    Stoney RM, Woods RK, Hosking CS, Hill DJ, Abramson MJ, Thien FCK: Maternal breast milk long-chain n-3 fatty acids are associated with increased risk of atopy in breastfed infants. Clin Exp Allergy 34:194–200, 2004CrossRefPubMedGoogle Scholar
  44. 44.
    Bhatnagar D, Durrington PN: Omega-3 fatty acids: their role in the prevention and treatment of atherosclerosis related risk factors and complications. Int J Clin Pract 57:305–314, 2003PubMedGoogle Scholar
  45. 45.
    Roynette CE, Calder PC, Dupertuis YM, Pichard C: n-3 Polyunsaturated fatty acids and colon cancer prevention. Clin Nutr 23:139–151, 2004PubMedGoogle Scholar
  46. 46.
    Geerling BJ, Stockbrugger RW, Brummer RJ: Nutrition and inflammatory bowel disease: an update. Scand J Gastroenterol Suppl 230:95–105, 1999PubMedGoogle Scholar
  47. 47.
    Moreau NM, Champ MM, Goupry SM, et al.: Resistant starch modulates in vivo colonic butyrate uptake and its oxidation in rats with dextran sulfate sodium-induced colitis. J Nutr 134:593–600, 2004Google Scholar
  48. 48.
    Ling SC, Griffiths AM: Nutrition in inflammatory bowel disease. Curr Opin Nutr Metab Care 3:339–344, 2000Google Scholar
  49. 49.
    Belluzzi A: n−3 Fatty acids for the treatment of inflammatory bowel disease. Proc Nutr Soc 61:391–395, 2002CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science + Business Media, Inc. 2006

Authors and Affiliations

  • Glen S. Patten
    • 1
    • 2
    Email author
  • Michael A. Conlon
    • 1
  • Anthony R. Bird
    • 1
  • Michael J. Adams
    • 1
  • David L. Topping
    • 1
  • Mahinda Y. Abeywardena
    • 1
  1. 1.CSIRO Health Sciences and NutritionAdelaideAustralia
  2. 2.AdelaideAustralia

Personalised recommendations