Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-22T11:42:41.889Z Has data issue: false hasContentIssue false
  • English
  • Français

Influences of dietary adaptation and source of resistant starch on short-chain fatty acids in the hindgut of rats

Published online by Cambridge University Press:  09 March 2007

Åsa M. Henningsson ,
E. Margareta ,
G. L. Nyman  and
Inger M. E. Björck
Åsa M. Henningsson*
Affiliation:
Applied Nutrition and Food Chemistry, Center for Chemistry and Chemical Engineering, Lund University, P.O. Box 124, SE-221 00 Lund, Sweden
E. Margareta
Affiliation:
Applied Nutrition and Food Chemistry, Center for Chemistry and Chemical Engineering, Lund University, P.O. Box 124, SE-221 00 Lund, Sweden
G. L. Nyman
Affiliation:
Applied Nutrition and Food Chemistry, Center for Chemistry and Chemical Engineering, Lund University, P.O. Box 124, SE-221 00 Lund, Sweden
Inger M. E. Björck
Affiliation:
Applied Nutrition and Food Chemistry, Center for Chemistry and Chemical Engineering, Lund University, P.O. Box 124, SE-221 00 Lund, Sweden
*
*Corresponding author: Dr Åsa M. Henningsson, fax +46 46 222 45 32, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

The effect of adaptation time on the concentration and pattern of short-chain fatty acids (SCFA) formed in the hindgut of rats given resistant starch (RS) in the form of raw potato starch (RPS) or high-amylose maize starch (HAS) was evaluated. Each starchy material was tested in diets containing 100 g indigestible carbohydrate/g DM, and fed for 13, 28 and 42 d. At the end of each period, the content of SCFA was determined in caecum, distal colon and faeces. The caecal concentration of total and individual SCFA increased for both diets with increasing adaptation time. The concentration of butyric acid was higher in the group fed RPS than in that fed HAS at all adaptation times. The caecal proportion of butyric acid was low both in rats fed RPS and HAS (6 and 4 %, respectively) following 13 d of adaptation. However, after 28 d of adaptation, the proportion of butyric acid had increased to 19 % in rats given RPS. A longer adaptation period (42 d) did not increase the proportion of butyric acid further. With HAS, there was also a significant (P<0·01) increase in the proportion of butyric acid with longer adaptation time. However, the increase was much slower and the proportion of butyric acid reached 6 and 8 % after 28 and 42 d respectively. It is concluded that the pattern of SCFA formed from RS in rats is dependent on adaptation time. It cannot be excluded that the different patterns of SCFA reported in the literature for RS may be due to the time of adaptation.

Keywords

Resistant starchFermentationShort-chain fatty acidsButyric acidRats
Type
Research Article
Information
British Journal of Nutrition , Volume 89 , Issue 3 , March 2003 , pp. 319 - 327
Copyright
Copyright © The Nutrition Society 2003

References

Åkerberg, AK, Liljeberg, HG, Granfeldt, YE, Drews, AW & Björck, IM (1998) An in vitro method, based on chewing, to predict resistant starch content in foods allows parallel determination of potentially available starch and dietary fiber. Journal of Nutrition 128, 651–660.CrossRefGoogle Scholar
Annison, G & Topping, DL (1994) Nutritional role of resistant starch: chemical structure vs physiological function. Annual Reviews of Nutrition 14, 297–320.CrossRefGoogle ScholarPubMed
Asp, N-G, Johansson, CG, Hallmer, H & Siljeström, M (1983) Rapid enzymatic assay of insoluble and soluble dietary fiber. Journal of Agricultural and Food Chemistry 31, 476–482.CrossRefGoogle ScholarPubMed
Barnard, JA & Warwick, G (1993) Butyrate rapidly induces growth inhibition and differentiation in HT-29 cells. Cell Growth and Differentiation 4, 495–501.Google ScholarPubMed
Barry, JL, Hoebler, C, Macfarlane, GT, Macfarlane, S, Mathers, JC, Reed, KA, Mortensen, PB, Nordgaard, I, Rowland, IR & Rumney, CJ (1995) Estimation of the fermentability of dietary fibre in vitro: a European interlaboratory study. British Journal of Nutrition 74, 303–322.CrossRefGoogle ScholarPubMed
Berggren, AM, Björck, IM, Nyman, EM & Eggum, BO (1993) Short-chain fatty acid content and pH in caecum of rats given various sources of carbohydrates. Journal of the Science of Food and Agriculture 63, 397–406.CrossRefGoogle Scholar
Berggren, AM, Björck, IM, Nyman, EM & Eggum, BO (1995) Short-chain fatty acid content and pH in caecum of rats fed various sources of starch. Journal of the Science of Food and Agriculture 68, 241–248.CrossRefGoogle Scholar
Bird, AR, Hayakawa, T, Marsono, Y, Gooden, JM, Record, IR, Correll, RL & Topping, DL (2000) Coarse brown rice increases fecal and large bowel short-chain fatty acids and starch but lowers calcium in the large bowel of pigs. Journal of Nutrition 130, 1780–1787.CrossRefGoogle Scholar
Björck, I, Nyman, M, Pedersen, B, Siljeström, M, Asp, N-G & Eggum, BO (1987) Formation of enzyme resistant starch during autoclaving of wheat starch: studies in vitro and in vivo. Journal of Cereal Science 6, 159–172.CrossRefGoogle Scholar
Björck, IME & Siljeström, MA (1992) In-vivo and in-vitro digestibility of starch in autoclaved pea and potato products. Journal of the Science of Food and Agriculture 58, 541–553.CrossRefGoogle Scholar
Bradburn, DM, Mathers, JC, Gunn, A, Burn, J, Chapman, PD & Johnston, ID (1993) Colonic fermentation of complex carbohydrates in patients with familial adenomatous polyposis. Gut 34, 630–636.Google Scholar
Brown, I (1996) Complex carbohydrates and resistant starch. Nutrition Reviews 54, S115–S119.CrossRefGoogle ScholarPubMed
Brown, I, Warhurst, M, Arcot, J, Playne, M, Illman, RJ & Topping, DL (1997) Fecal numbers of bifidobacteria are higher in pigs fed Bifidobacterium longum with a high amylose cornstarch than with a low amylose cornstarch. Journal of Nutrition 127, 1822–1827.CrossRefGoogle ScholarPubMed
Brunsgaard, G, Bach Knudsen, KE & Eggum, BO (1995) The influence of the period of adaptation on the digestibility of diets containing different types of indigestible polysaccharides in rats. British Journal of Nutrition 74, 833–848.Google ScholarPubMed
Caderni, G, Luceri, C, Spagnesi, MT, Giannini, A, Biggeri, A & Dolara, P (1994) Dietary carbohydrates modify azoxymethane-induced intestinal carcinogenesis in rats. Journal of Nutrition 124, 517–523.CrossRefGoogle ScholarPubMed
Cassidy, A, Bingham, SA & Cummings, JH (1994) Starch intake and colorectal cancer risk: an international comparison. British Journal of Cancer 69, 937–942.Google Scholar
Casterline, JLJ, Oles, CJ & Ku, Y (1997) In vitro fermentation of various food fiber fractions. Journal of Agricultural and Food Chemistry 45, 2463–2467.CrossRefGoogle Scholar
Cummings, JH (1997) Short-chain fatty acid enemas in the treatment of distal ulcerative colitis. European Journal of Gastroenterology and Hepatology 9, 149–153.CrossRefGoogle ScholarPubMed
Cummings, JH, Beatty, ER, Kingman, SM, Bingham, SA & Englyst, HN (1996) Digestion and physiological properties of resistant starch in the human large bowel. British Journal of Nutrition 75, 733–747.CrossRefGoogle ScholarPubMed
de Deckere, EA, Kloots, WJ & van Amelsvoort, JM (1995) Both raw and retrograded starch decrease serum triacylglycerol concentration and fat accretion in the rat. British Journal of Nutrition 73, 287–298.CrossRefGoogle ScholarPubMed
De Schrijver, R, Vanhof, K & Van de Ginste, J (1999) Nutrient utilization in rats and pigs fed enzyme resistant starch. Nutrition Research 19, 1349–1361.CrossRefGoogle Scholar
Englyst, HN, Hay, S & Macfarlane, GT (1987) Polysaccharide breakdown by mixed populations of human faecal bacteria. FEMS Microbiology Ecology 45, 163–171.CrossRefGoogle Scholar
Englyst, HN, Kingman, SM & Cummings, JH (1992) Classification and measurement of nutritionally important starch fractions. European Journal of Clinical Nutrition 46, Suppl. 2, S33–S50.Google ScholarPubMed
Ferguson, LR, Tasman-Jones, C, Englyst, H & Harris, PJ (2000) Comparative effects of three resistant starch preparations on transit time and short-chain fatty acid production in rats. Nutrition and Cancer 36, 230–237.Google Scholar
Gallant, DJ, Bouchet, B, Buleon, A & Perez, S (1992) Physical characteristics of starch granules and susceptibility to enzymatic degradation. European Journal of Clinical Nutrition 46, Suppl. 2, S3–S16.Google ScholarPubMed
Gee, JM, Faulks, RM & Johnson, IT (1991) Physiological effects of retrograded, alpha-amylase-resistant cornstarch in rats. Journal of Nutrition 121, 44–49.CrossRefGoogle ScholarPubMed
Hague, A, Elder, DJ, Hicks, DJ & Paraskeva, C (1995) Apoptosis in colorectal tumour cells: induction by the short chain fatty acids butyrate, propionate and acetate and by the bile salt deoxycholate. International Journal of Cancer 60, 400–406.CrossRefGoogle ScholarPubMed
Holdeman, LV, Cato, EP & Moore, WEC (1977) Anaerobic Laboratory Manual, 4th ed., Blackburg, VA: Virginia Polytechnic Institute and State University.Google Scholar
Hylla, S, Gostner, A, Dusel, G, Anger, H, Bartram, HP, Christl, SU, Kasper, H & Scheppach, W (1998) Effects of resistant starch on the colon in healthy volunteers: possible implications for cancer prevention. American Journal of Clinical Nutrition 67, 136–142.CrossRefGoogle Scholar
Kleessen, B, Stoof, G, Proll, J, Schmiedl, D, Noack, J & Blaut, M (1997) Feeding resistant starch affects fecal and cecal microflora and short-chain fatty acids in rats. Journal of Animal Science 75, 2453–2462.CrossRefGoogle ScholarPubMed
Le Blay, G, Michel, C, Blottière, HM & Cherbut, C (1999) Enhancement of butyrate production in the rat caecocolonic tract by long-term ingestion of resistant potato starch. British Journal of Nutrition 82, 419–426.Google Scholar
Lupton, JR & Villalba, N (1988) Fermentation of fiber to short-chain fatty acids: a comparative study with humans, baboons, pigs and rats. FASEB Journal 2, A1201.Google Scholar
Mallett, AK, Bearne, CA, Young, PJ, Rowland, IR & Berry, C (1988) Influence of starches of low digestibility on the rat caecal microflora. British Journal of Nutrition 60, 597–604.CrossRefGoogle ScholarPubMed
Mathers, JC, Smith, H & Carter, S (1997) Dose-response effects of raw potato starch on small-intestinal escape, large-bowel fermentation and gut transit time in the rat. British Journal of Nutrition 78, 1015–1029.CrossRefGoogle ScholarPubMed
Monsma, DJ & Marlett, JA (1995) Rat cecal inocula produce different patterns of short-chain fatty acids than fecal inocula in in vitro fermentations. Journal of Nutrition 125, 2463–2470.Google ScholarPubMed
Moore, WE & Holdeman, LV (1974) Human fecal flora: the normal flora of 20 Japanese-Hawaiians. Applied Microbiology 27, 961–979.CrossRefGoogle ScholarPubMed
Noakes, M, Clifton, PM, Nestel, PJ, Le Leu, R & McIntosh, G (1996) Effect of high-amylose starch and oat bran on metabolic variables and bowel function in subjects with hypertriglyceridemia. American Journal of Clinical Nutrition 64, 944–951.Google Scholar
Nyman, M & Asp, NG (1985) Dietary fibre fermentation in the rat intestinal tract: effect of adaptation period, protein and fibre levels, and particle size. British Journal of Nutrition 54, 635–643.CrossRefGoogle ScholarPubMed
Nyman, M, Asp, NG, Cummings, J & Wiggins, H (1986) Fermentation of dietary fibre in the intestinal tract: comparison between man and rat. British Journal of Nutrition 55, 487–496.CrossRefGoogle Scholar
Olesen, M, Rumessen, JJ & Gudmand-Hoyer, E (1992) The hydrogen breath test in resistant starch research. European Journal of Clinical Nutrition 46, Suppl. 2, S133–S134.Google ScholarPubMed
Perrin, P, Pierre, F, Patry, Y, Champ, M, Berreur, M, Pradal, G, Bornet, F, Meflah, K & Menanteau, J (2001) Only fibres promoting a stable butyrate producing colonic ecosystem decrease the rate of aberrant crypt foci in rats. Gut 48, 53–61.CrossRefGoogle ScholarPubMed
Phillips, J, Muir, JG, Birkett, A, Lu, ZX, Jones, GP, O'Dea, K & Young, GP (1995) Effect of resistant starch on fecal bulk and fermentation-dependent events in humans. American Journal of Clinical Nutrition 62, 121–130.CrossRefGoogle ScholarPubMed
Richardson, AJ, Calder, AG, Stewart, CS & Smith, A (1989) Simultaneous determination of volatile and non-volatile acidic fermentation products of anaerobes by capillary gas chromatography. Letters in Applied Microbiology 9, 5–8.Google Scholar
Roediger, WE (1980) The colonic epithelium in ulcerative colitis: an energy-deficiency disease? Lancet 2, 712–715.Google Scholar
Roediger, WE (1982) Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology 83, 424–429.CrossRefGoogle ScholarPubMed
Sakamoto, J, Nakaji, S, Sugawara, K, Iwane, S & Munakata, A (1996) Comparison of resistant starch with cellulose diet on 1,2-dimethylhydrazineinduced colonic carcinogenesis in rats. Gastroenterology 110, 116–120.Google Scholar
Scheppach, W, Bartram, HP & Richter, F (1995) Role of short-chain fatty acids in the prevention of colorectal cancer. European Journal of Cancer 31A, 1077–1080.CrossRefGoogle ScholarPubMed
Scheppach, W, Fabian, C, Sachs, M & Kasper, H (1988) The effect of starch malabsorption on fecal short-chain fatty acid excretion in man. Scandinavian Journal of Gastroenterology 23, 755–759.CrossRefGoogle ScholarPubMed
Scheppach, W, Sommer, H, Kirchner, T, Paganelli, GM, Bartram, P, Christl, S, Richter, F, Dusel, G & Kasper, H (1992) Effect of butyrate enemas on the colonic mucosa in distal ulcerative colitis. Gastroenterology 103, 51–56.Google Scholar
Schulz, AG, Van Amelsvoort, JM & Beynen, AC (1993) Dietary native resistant starch but not retrograded resistant starch raises magnesium and calcium absorption in rats. Journal of Nutrition 123, 1724–1731.CrossRefGoogle Scholar
Theander, O, Åman P, Westerlund, E, Andersson, R & Pettersson, D (1995) Total dietary fiber determined as neutral sugar residues, uronic acid residues, and Klason lignin (the Uppsala method): collaborative study. Journal of AOAC International 78, 1030–1044.Google Scholar
Thorup, I, Meyer, O & Kristiansen, E (1995) Effect of potato starch, cornstarch and sucrose on aberrant crypt foci in rats exposed to azoxymethane. Anticancer Research 15, 2101–2105.Google Scholar
Topping, DL, Illman, RJ, Clarke, JM, Trimble, RP, Jackson, KA & Marsono, Y (1993) Dietary fat and fiber alter large bowel and portal venous volatile fatty acids and plasma cholesterol but not biliary steroids in pigs. Journal of Nutrition 123, 133–143.CrossRefGoogle Scholar
van Munster, IP, Tangerman, A & Nagengast, FM (1994) Effect of resistant starch on colonic fermentation, bile acid metabolism, and mucosal proliferation. Digestive Diseases and Sciences 39, 834–842.CrossRefGoogle ScholarPubMed
Wang, X, Conway, PL, Brown, IL & Evans, AJ (1999) In vitro utilization of amylopectin and high-amylose maize (Amylomaize) starch granules by human colonic bacteria. Journal of Applied Environmental Microbiology 65, 4848–4854.CrossRefGoogle ScholarPubMed
Weaver, GA, Krause, JA, Miller, TL & Wolin, MJ (1992) Cornstarch fermentation by the colonic microbial community yields more butyrate than does cabbage fiber fermentation; cornstarch fermentation rates correlate negatively with methanogenesis. American Journal of Clinical Nutrition 55, 70–77.CrossRefGoogle ScholarPubMed
Weaver, GA, Tangel, CT, Krause, JA, Parfitt, MM, Jenkins, PL, Rader, JM, Lewis, BA, Miller, TL & Wolin, MJ (1997) Acarbose enhances human colonic butyrate production. Journal of Nutrition 127, 717–723.CrossRefGoogle ScholarPubMed
Whitehead, RH, Young, GP & Bhathal, PS (1986) Effects of short chain fatty acids on a new human colon carcinoma cell line (LIM1215). Gut 27, 1457–1463.CrossRefGoogle ScholarPubMed
Wyatt, GM & Horn, N (1988) Fermentation of resistant food starches by human and rat intestinal bacteria. Journal of the Science of Food and Agriculture 44, 281–288.CrossRefGoogle Scholar
Young, GP, McIntyre, A, Albert, V, Folino, M, Muir, JG & Gibson, PR (1996) Wheat bran suppresses potato starch-potentiated colorectal tumorigenesis at the aberrant crypt stage in a rat model. Gastroenterology 110, 508–514.CrossRefGoogle ScholarPubMed