Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-24T01:31:10.318Z Has data issue: false hasContentIssue false

Content of short-chain fatty acids in the hindgut of rats fed processed bean (Phaseolus vulgaris) flours varying in distribution and content of indigestible carbohydrates

Published online by Cambridge University Press:  09 March 2007

Åsa M. Henningsson*
Affiliation:
Applied Nutrition and food Chemistry, Center for Chemistry and Chemical Engineering, Lund University, PO Box 124, SE-221 00 Lund, Sweden
E. Margareta
Affiliation:
Applied Nutrition and food Chemistry, Center for Chemistry and Chemical Engineering, Lund University, PO Box 124, SE-221 00 Lund, Sweden
G. L. Nyman
Affiliation:
Applied Nutrition and food Chemistry, Center for Chemistry and Chemical Engineering, Lund University, PO 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, PO Box 124, SE-221 00 Lund, Sweden
*
*Corresponding author: Åsa Hennungsson, 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.

Red kidney beans (Phaseolus vulgaris) processed to differ in distribution and content of indigestible carbohydrates were used to study hindgut fermentability and production of short-chain fatty acids (SCFA). Bean flours with low or high content of resistant starch (RS), mainly raw and physically-inaccessible starch, were obtained by milling the beans before or after boiling. Flours containing retrograded starch and with a high or low content of oligosaccharides were prepared by autoclaving followed by freeze-drying with or without the boiling water. Six diets were prepared from these flours yielding a total concentration of indigestible carbohydrates of 90 or 120 g/kg (dry weight basis). The total fermentability of the indigestible carbohydrates was high with all diets (80–87 %). Raw and physically-inaccessible starch was more readily fermented than retrograded starch (97–99 % v. 86–95 %; P<0·05). Non-starch glucans were fermented to a lesser extent than RS, but the fermentability was higher (P<0·05) in the case of autoclaved (50–54 %) than boiled beans (37–41 %). The distribution between acetic, propionic and butyric acid in the caecum was similar for all diets, with a comparatively high percentage of butyric acid (approximately 18). However, with diets containing the high amounts of RS, the butyric acid concentration was significantly higher in the distal colon than in the proximal colon (P=0·009 and P=0·047 for the high- and low-level diets respectively), whereas it remained constant, or decreased along the colon in the case of the other diets. Furthermore, the two diets richest in RS also promoted the highest percentages of butyric acid in the distal colon (24 and 17 v. 12 and 12–16 for the high- and low-level diets respectively).

Type
Research Article
Copyright
Copyright © The Nutrition Society 2001

References

Aring;kerberg, 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, 651660.Google Scholar
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, 476482.CrossRefGoogle ScholarPubMed
Association of Official Analytical Chemists (1984) Official Methods of Analysis, 14th ed., Washington DC: AOAC.Google Scholar
Bach Knudsen, KE & Canibe, N (1993) Changes in pig plasma lipids to dietary cholesterol, source and level of dietary fibre and caecal infusion of propionate. In COST 92 Metabolic and Physiological Aspects of Dietary Fibre in Food – Mechanisms of Action of Dietary Fibre on Lipid and Cholesterol Metabolism. Proceedings of a Workshop Held in Carry le Route-Marseille, France, 1993, pp. 123130 [Lairon, D, editor]. Luxemburg: Commission of the European Communities.Google Scholar
Barry, IL, Hoebler, C, Macfarlane, GT, Macfarlane, S, Mathers, IC, 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, 303322.CrossRefGoogle ScholarPubMed
Beaulieu, KE & McBurney, MI (1992) Changes in pig serum lipids, nutrient digestibility and sterol excretion during cecal infusion of propionate. Journal of Nutrition 122, 241245.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, 397406.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, 17801787.CrossRefGoogle Scholar
Björck, I, Nyman, M & Asp, N-G (1984) Extrusion cooking and dietary fiber: effects on dietary fiber content and on degradation in the rat intestinal tract. Cereal Chemistry 61, 174179.Google 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, 159172.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, 541553.CrossRefGoogle Scholar
Breuer, RI, Buto, SK, Christ, ML, Bean, J, Vernia, P, Paoluzi, P, Di Paolo, MC & Caprilli, R (1991) Rectal irrigation with short-chain fatty acids for distal ulcerative colitis. Preliminary report. Digestive Diseases and Sciences 36, 185187.CrossRefGoogle ScholarPubMed
Brighenti, F, Testolin, G, Canzi, E, Ferrari, A, Wolever, TMS, Ciappellano, S, Porrini, M & Simonetti, P (1989) Influence of long-term feeding of different purified dietaty fibers on the volatile fatty acid (VFA) profile, pH and fiber-degrading activity of the cecal contents in rats. Nutrition Research 9, 761772.CrossRefGoogle Scholar
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, 18221827.CrossRefGoogle ScholarPubMed
Bufill, JA (1990) Colorectal cancer: evidence for distinct genetic categories based on proximal or distal tumor location. Annals of Internal Medicine 113, 779788.CrossRefGoogle ScholarPubMed
Campbell, JM, Fahey, GC Jr & Wolf, BW (1997) Selected indigestible oligosaccharides affect large bowel mass, cecal and fecal short-chain fatty acids, pH and microflora in rats. Journal of Nutrition 127, 130136.CrossRefGoogle ScholarPubMed
Chen, WJ, Anderson, JW & Jennings, D (1984) Propionate may mediate the hypocholesterolemic effects of certain soluble plant fibers in cholesterol-fed rats. Proceedings of the Society for Experimental Biology and Medicine 175, 215218.CrossRefGoogle ScholarPubMed
Cheng, BO, Trimble, RP, Illman, RJ, Stone, BA & Topping, DL (1987) Comparative effects of dietary wheat bran and its morphological components (aleurone and pericarp–seed coat) on volatile fatty acid concentrations in the rat. British Journal of Nutrition 57, 6976.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, 733747.CrossRefGoogle ScholarPubMed
Cummings, JH & Englyst, HN (1987) Fermentation in the human large intestine and the available substrates. American Journal of Clinical Nutrition 45, 12431255.CrossRefGoogle ScholarPubMed
Cummings, JH, Roberfroid, MB, Andersson, H, Barth, C, Ferro-Luzzi, A, Ghoos, Y, Gibney, M, Hermonsen, K, James, WP, Korver, O, Lairon, D, Pascal, G & Voragen, AG (1997) A new look at dietary carbohydrate: chemistry, physiology and health. Paris Carbohydrate Group. European Journal of Clinical Nutrition 51, 417423.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, S33S50.Google ScholarPubMed
Ferguson, MJ & Jones, GP (2000) Production of short-chain fatty acids following in vitro fermentation of saccharides, saccharide esters, fructo-oligosaccharides, starches, modified starches and non-starch polysaccharides. Journal of the Science of Food and Agriculture 80, 166170.3.0.CO;2-K>CrossRefGoogle Scholar
Goodlad, JS & Mathers, JC (1990) Large bowel fermentation in rats given diets containing raw peas (Pisum sativum). British Journal of Nutrition 64, 569587.CrossRefGoogle ScholarPubMed
Granfeldt, Y, Björck, I, Drews, A & Tovar, J (1992) An in vitro procedure based on chewing to predict metabolic response to starch in cereal and legume products. European Journal of Clinical Nutrition 46, 649660.Google Scholar
Guillemot, F, Colombel, JF, Neut, C, Verplanck, N, Lecomte, M, Romond, C, Paris, JC & Cortot, A (1991) Treatment of diversion colitis by short-chain fatty acids. Prospective and double-blind study. Diseases of the Colon and Rectum 34, 861864.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, 400406.CrossRefGoogle ScholarPubMed
Hague, A & Paraskeva, C (1995) The short-chain fatty acid butyrate induces apoptosis in colorectal tumour cell lines. European Journal of Cancel Prevention 4, 359364.CrossRefGoogle ScholarPubMed
Hara, H, Saito, Y, Nagata, M, Tsuji, M, Yamamoto, K & Kiriyama, S (1994) Artificial fiber complexes composed of cellulose and guar gum or psyllium may be better sources of soluble fiber for rats than comparable fiber mixtures. Journal of Nutrition 124, 12381247.CrossRefGoogle ScholarPubMed
Holt, PR, Mokuolu, AO, Distler, P, Liu, T & Reddy, BS (1996) Regional distribution of carcinogen-induced colonic neoplasia in the rat. Nutrition and Cancer 25, 129135.CrossRefGoogle ScholarPubMed
Hoover, R & Sosulski, FW (1991) Composition, structure, functionality, and chemical modification of legume starches: a review. Canadian Journal of Physiology and Pharmacology 69, 7992.CrossRefGoogle ScholarPubMed
Kapadia, SA, Raimundo, AH, Grimble, GK, Aimer, P & Silk, DB (1995) Influence of three different fiber-supplemented enteral diets on bowel function and short-chain fatty acid production. Journal of Parenteral and Enteral Nutrition 19, 6368.CrossRefGoogle ScholarPubMed
Key, FB & Mathers, JC (1993) Complex carbohydrate digestion and large bowel fermentation in rats given wholemeal bread and cooked haricot beans (Phaseolus vulgaris) fed in mixed diets. British Journal of Nutrition 69, 497509.CrossRefGoogle ScholarPubMed
Key, FB & Mathers, JC (1995) Digestive adaptations of rats given white bread and cooked haricot beans (Phaseolus vulgaris): large-bowel fermentation and digestion of complex carbohydrates. British Journal of Nutrition 74, 393406.CrossRefGoogle ScholarPubMed
Livesey, G (1992) The energy values of dietary fibre and sugar alcohols for man. Nutrition Research Reviews 5, 6184.CrossRefGoogle ScholarPubMed
McBurney, MI & Thompson, LU (1987) Effect of human faecal inoculum on in vitro fermentation variables. British Journal of Nutrition 58, 233243.CrossRefGoogle ScholarPubMed
McBurney, MI & Thompson, LU (1989) Effect of human faecal donor on in vitro fermentation variables. Scandinavian Journal of Gastroenterology 24, 359367.CrossRefGoogle ScholarPubMed
Macfarlane, GT & Cummings, JH (1995) Microbiological aspects of the production of short-chain fatty acids in the large bowel. In Physiological Aspects of Short Chain Fatty Acids, pp. 87105. [Cummings, JH, Rombeau, JL and Sakata, T, editors]. Cambridge: Cambridge University Press.Google Scholar
McIntyre, A, Gibson, PR & Young, GP (1993) Butyrate production from dietary fibre and protection against large bowel cancer in a rat model. Gut 34, 386391.CrossRefGoogle ScholarPubMed
Martin, LJM, Dumon, HJW & Champ, MMJ (1998) Production of short-chain fatty acids from resistant starch in a pig model. Journal of the Science of Food and Agriculture 77, 7180.3.0.CO;2-H>CrossRefGoogle Scholar
Nygaard Johansen, H, Glitsø, V & Bach Knudsen, KE (1996) Influence of extraction solvent and temperature on the quantitative determination of oligosaccharides from plant materials by high-performance liquid chromatography. Journal of Agricultural and Food Chemistry 44, 14701474.CrossRefGoogle Scholar
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, 487496.CrossRefGoogle Scholar
Nyman, M, Schweizer, TF, Pålsson, K-E & Asp, N-G (1991) Effects of processing on fermentation of dietary fibre in vegetables by rats. Lebensmittel-Wissenschaft und-Technologie 24, 433441.Google Scholar
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, 121130.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, 58.CrossRefGoogle Scholar
Roediger, WE (1982) Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology 83, 424429.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, 5156.CrossRefGoogle ScholarPubMed
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, 17241731.CrossRefGoogle Scholar
Shetty, PS & Kurpad, AV (1986) Increasing starch intake in the human diet increases fecal bulking. American Journal of Clinical Nutrition 43, 210212.CrossRefGoogle ScholarPubMed
Siavoshian, S, Segain, JP, Kornprobst, M, Bonnet, C, Cherbut, C, Galmiche, JP & Blottiere, HM (2000) Butyrate and trichostatin A effects on the proliferation/differentiation of human intestinal epithelial cells: induction of cyclin D3 and p21 expression. Gut 46, 507514.CrossRefGoogle ScholarPubMed
Steinhart, AH, Hiruki, T, Brzezinski, A & Baker, JP (1996) Treatment of left-sided ulcerative colitis with butyrate enemas: a controlled trial. Alimentary Pharmacology and Therapeutics 10, 729736.CrossRefGoogle ScholarPubMed
Svanberg, M, Gustafsson, K, Suortti, T & Nyman, M (1995) Molecular weight distribution, measured by HPSEC, and viscosity of water-soluble dietary fiber in carrots following different types of processing. Journal of Agriculture and Food Chemistry 43, 8388.CrossRefGoogle Scholar
Svanberg, M, Sourtti, T & Nyman, M (1997) Physicochemical changes in dietary fiber of green beans after repeated microwave treatments. Journal of Food Science 62, 10061010.CrossRefGoogle Scholar
Svanberg, M, Suortti, T & Nyman, M (1999) Intestinal degradation of dietary fibre in green beans–effects of microwave treatments. International Journal of Food Science and Nutrition 50, 245253.Google ScholarPubMed
Theander, O, Åman P, Westerlund, E, Anderssson, 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 the Association of Official Analytical Chemists International 78, 10301044.Google ScholarPubMed
Titgemeyer, EC, Bourquin, LD, Fahey, GC Jr & Garleb, KA (1991) Fermentability of various fiber sources by human fecal bacteria in vitro. American Journal of Clinical Nutrition 53, 14181424.CrossRefGoogle ScholarPubMed
Todesco, T, Rao, AV, Bosello, O & Jenkins, DJ (1991) Propionate lowers blood glucose and alters lipid metabolism in healthy subjects. American Journal of Clinical Nutrition 54, 860865.CrossRefGoogle ScholarPubMed
Topping, DL, Illman, RJ & Trimble, RP (1985) Volatile fatty acid concentrations in rats fed diets containing gum arabic and cellulose separately and as a mixture. Nutrition Reports International 32, 809814.Google Scholar
Venter, CS, Vorster, HH & Cummings, JH (1990) Effects of dietary propionate on carbohydrate and lipid metabolism in healthy volunteers. American Journal of Gastroenterology 85, 549553.Google ScholarPubMed
Vernia, P, Marcheggiano, A, Caprilli, R, Frieri, G, Corrao, G, Valpiani, D, Di Paolo, MC, Paoluzi, P & Torsoli, A (1995) Short-chain fatty acid topical treatment in distal ulcerative colitis. Alimentary Pharmacology and Therapeutics 9, 309313.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, 14571463.CrossRefGoogle ScholarPubMed
Wolever, TM, Spadafora, P & Eshuis, H (1991) Interaction between colonic acetate and propionate in humans. American Journal of Clinical Nutrition 53, 681687.CrossRefGoogle ScholarPubMed
Wright, RS, Anderson, JW & Bridges, SR (1990) Propionate inhibits hepatocyte lipid synthesis. Proceedings of the Society for Experimental Biology and Medicine 195, 2629.CrossRefGoogle ScholarPubMed