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Short-chain fatty acid formation in the hindgut of rats fed native and fermented oat fibre concentrates

Published online by Cambridge University Press:  08 March 2007

Adele M. Lambo-Fodje*
Affiliation:
Division of Applied Nutrition and Food Chemistry, Department of Food Technology, Engineering and Nutrition, Center for Chemistry and Chemical Engineering, Lund University, PO Box 124, SE-221 00, Lund, Sweden
Rickard öste
Affiliation:
Division of Applied Nutrition and Food Chemistry, Department of Food Technology, Engineering and Nutrition, Center for Chemistry and Chemical Engineering, Lund University, PO Box 124, SE-221 00, Lund, Sweden
Margareta E. G.-L. Nyman
Affiliation:
Division of Applied Nutrition and Food Chemistry, Department of Food Technology, Engineering and Nutrition, Center for Chemistry and Chemical Engineering, Lund University, PO Box 124, SE-221 00, Lund, Sweden
*
*Corresponding author: Dr Adele M. Lambo-Fodje, fax +46 46 222 45 32, email [email protected]
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Abstract

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The formation of SCFA in rats fed fermented oat fibre concentrates was compared with that of rats fed native oat fibre concentrate. The cultures used were lactic acid bacteria consisting of Lactobacillus bulgaricus and Streptococcus thermophilus (V2), the exopolysaccharide-producing strain Pediococcus damnosus 2.6 (Pd) and L. reuteri (Lr). The materials were incorporated into test diets yielding a concentration of indigestible carbohydrates of 80g/kg (dry weight). Rats fed the V2-fermented fibre-concentrate diet yielded higher caecal and distal concentrations of acetic acid (p<0·01) than rats fed the native fibre concentrate. All the fermented fibre concentrates resulted in a higher propionic acid concentration in the distal colon (p<0·05), while rats fed Pd-fermented fibre concentrate resulted in lower concentration of butyric acid (p<0·05,p <0·01) in all parts of the hindgut as compared with rats fed the native fibre concentrates. Butyrate concentrations ranged between 5–11μmol/g (distal colon) and 6–8;μmol/g (13d faeces). Higher proportions of acetic acid (p<0·05; p<0·01) were observed in the caecum of rats fed the fermented fibre concentrates. Rats fed Pd- and Lr-fermented fibre concentrates produced higher proportions of propionic acid (p<0·05; p<0·01) in the caecum. Changes in SCFA formation in the caecum, distal colon and faeces of rats fed the fermented samples compared with the native sample indicate that these microbes probably survive in the hindgut and that modification of the microflora composition with fermented foods is possible. This may be important for the gastrointestinal flora balance in relation to colonic diseases.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2006

References

Association of Official Analytical Chemists Official Methods of Analysis of AOAC, 13th ed., Washington DC: Association of Official Analytical Chemists. 1980Google Scholar
Axelsson, LLactic acid bacteria: classification and physiology. In Lactic Acid Bacteria: Microbiology and Functional Aspects, 2nd ed., S, Salminen and A von, WrightNew York: Marcel Dekker. 1998 pp.172Google Scholar
Battock, M & Azam-Ali, SFermented fruits and vegetables. FAO Agricultural Services Bulletin, Rome: FAO. 1998 no.134Google Scholar
Berggren, AM, Björck, IM, Nyman, EM & Eggum, BOShortchain fatty acid content and pH in caecum of rats given various sources of carbohydrates. J Sci Food Agric (1993) 63 397406.CrossRefGoogle Scholar
Bianchi-Salvadori, B, Gotti, M, Brughera, F & Ponlinelli, UÉtude sur les variations de la flora lactique et bifide intestinal par rapport a l'administration des cellules lactiques du yaourt (Study on the variations of intestinal lactic acid bacteria and bifidobacteria flora as a result of the administration of lactic acid bacteria of yoghurt). Lait 571/572, 1978 1742.CrossRefGoogle Scholar
Björck, I, Nyman, M, Pedersen, B, Siljeström, M, Asp, N-G & Eggum, BOFormation of enzyme resistant starch during autoclaving of wheat starch: studies in vitro and in vivo. J Cereal Sci (1987) 6 159172.CrossRefGoogle Scholar
Björck, IME & Siljeström, MAIn-vivo and in-vitro digestibility of starch in autoclaved peas and potato products. J Sci Food Agric (1992) 58 541553.CrossRefGoogle Scholar
Brunsgaard, G, Bach Knudsen, KE & Eggum, BOThe influence of the period of adaptation on the digestibility of diets containing different types of indigestible polysaccharides in rats. Br J Nutr (1995) 74 833848.Google ScholarPubMed
Bufill, JAColorectal cancer: evidence for distinct genetic categories based on proximal or distal tumour location. Ann Int Med (1990) 113 779788.CrossRefGoogle ScholarPubMed
Casas, IA & Dobrogosz, WJValidation of the probiotic concept: Lactobacillus reuteri confers broad-spectrum protection against disease in humans and animals. Microb Ecol Health Dis (2000) 12 247285.Google Scholar
Casterline, JL Jr, Oles, CJ & Ku, YIn vitro fermentation of various foods fibre fractions. J Agric Food Chem (1997) 45 24632467.CrossRefGoogle Scholar
Cummings, JHShort-chain fatty acid enemas in the treatment of distal ulcerative colitis. Eur J Gastroenterol Hepatol (1997) 9 149153.CrossRefGoogle ScholarPubMed
Delzenne, N, Aertssens, J, Verplaetse, H, Roccaro, M & Roberfroid, MEffect of fermentable fructo-oligosaccharides on mineral, nitrogen and energy digestive balance in the rat. Life Sci (1995) 57 15791587.CrossRefGoogle ScholarPubMed
De Man, JC, Rogosa, M & Sharpe, MEA medium for the cultivation of lactobacilli. J Appl Microbiol (1960) 23 130135.Google Scholar
Dueñas-Chasco, MT,Rodríguez-Carvajal, MA, Mateo, PT, Franco- Rodríguez, G, Esparteo, JL, Irastorza-Iribas, A & Gil-Serrano, AMStructural analysis of the exopolysaccharide produced by Pediococcus damnosus 2.6. Carbohydr Res (1997) 303 453458.CrossRefGoogle ScholarPubMed
Eastwood, MDiet, fiber and colorectal disease. In The Large Intestine: Physiology, Pathophysiology, and Disease, pp.209222SF, Philips, JH, Pemberton and RG, Shorter editors]. New York: Raven Press Ltd. 1991Google Scholar
Edwards, CInteractions between nutrition and the intestinal microflora. Proc Nutr Soc (1993) 52 375382.CrossRefGoogle ScholarPubMed
Folkenberg, DM, Dejmek, P, Skriver, A & Ipsen, RRelation between sensory texture properties and exopolysaccharide distribution in set and in stirred yoghurts produced with different starter cultures. J Texture Studies (2005) 36 174189.CrossRefGoogle Scholar
Fujisawa, T, Taeshima, T & Mitsuoka, TLactobacilli in human faeces. Biosci Microflora (1996) 15 6975.CrossRefGoogle Scholar
Gamet, L, Daviaud, D, Denis-Pouxviel, C, Remesy, C & Murat, JCEffects of short-chain fatty acids on growth and differentiation of the human colon-cancer cell line HT29. Int J Cancer (1992) 52 286289.CrossRefGoogle ScholarPubMed
Goodlad, JS & Mathers, JCDigestion of complex carbohydrates and large bowel fermentation in rats fed on raw and cooked peas. Br J Nutr (1992) 67 475488.CrossRefGoogle ScholarPubMed
Hague, A, Elder, DJ, Hicks, DJ & Paraskeva, CApoptosis in colorectal tumour cells: induction by the short-chain fatty acids butyrate, propionate and acetic acid and by bile salt deoxycholate. Int J Cancer (1995) 60 400406.CrossRefGoogle ScholarPubMed
Hallert, C, Björck, I, Nyman, M, Pousette, A, Grännö, C & Svensson, HIncreasing fecal butyrate in ulcerative colitis patients by diet: controlled pilot study. Inflamm Bowel Dis (2003) 9 116121.CrossRefGoogle ScholarPubMed
Hargrove, HE & Alford, JAGrowth rate and feed efficiency of rats fed yoghurt and other fermented milks. J Dairy Sci (1978) 61 1119.CrossRefGoogle Scholar
Henningsson, ÅM, Nyman, EM & Björck, IMContent of shortchain fatty acids in the hindgut of rats fed processed bean (Phaseolus vulgaris) flours varying in distribution and content of indigestible carbohydrates. Br J Nutr (2001) 86 379389.CrossRefGoogle ScholarPubMed
Holdeman, LV, Cato, EP & Moore, WECAnaerobe Laboratory Manual, 4th ed.,Blacksburg VA: Southern Printing. 1977Google Scholar
Holt, PR, Mokuolu, AO, Distler, P, Liu, T & Reddy, BSRegional distribution of carcinogen-induced colonic neoplasia in the rat. Nutr Cancer (1996) 25 129135.CrossRefGoogle ScholarPubMed
Immerstrand, T An evaluation of the probiotic potential of Pediococcus damnosus 2.6. Masters Thesis, Lund University. Department of Biotechnology, 2005Google Scholar
Karppinen, S, Liukkonen, K, Aura, AM, Forssell, P & Poutanen, KIn vitro fermentation of polysaccharides of rye, wheat, oat bran and inulin by human faecal bacteria. J Sci Food Agric (2000) 80 14691476.3.0.CO;2-A>CrossRefGoogle Scholar
Konstantakos, AK, Siu, IM, Pretlow, TG, Stellato, TA & Pretlow, TPHuman aberrant crypt foci with carcinoma in situ from a patient with sporadic colon cancer. Gastroenterology (1996) 111 772777.CrossRefGoogle ScholarPubMed
Lambo, MA, Ö ste, R & Nyman, EG-LMDietary fibre in fermented oat and barley b-glucan rich concentrates. Food Chem (2005) 89 283293.CrossRefGoogle Scholar
Levrat, MA, Behr, SR, Rémésy, C & Demigné, CEffects of soyabean fibre on caecal digestion in rats previously adapted to a fibre-free diet. J Nutr (1991) 121 672678.CrossRefGoogle Scholar
Lindgren, SE & Dobrogosz, WJAntagonistic activities of lactic acid bacteria in food and feed fermentations. FEMS Microbiol Rev (1990) 87 149164.CrossRefGoogle Scholar
Macfarlane, GT & Macfarlane, SHuman colonic microbiota: ecology, physiology and metabolic potential of intestinal bacteria. Scand J Gastroenterol (1997) 222 Suppl.,39.CrossRefGoogle ScholarPubMed
McIntyre, A, Gibson, PR & Young, GPButyrate production from dietary fibre and protection against large bowel cancer in a rat model. Gut (1993) 34 386391.CrossRefGoogle ScholarPubMed
Mårtensson, O, Biörklund, M, Lambo, MA, Dueñas-Chasco, M, Irastorza, A, Holst, O, Norin, E, Welling, G, Öste, R, Önning, GFermented, ropy, oat-based products reduce cholesterol levels and stimulate the bifidobacteria flora in humans. Nutr Res (2005) 25 413513.CrossRefGoogle Scholar
Mårtensson, O, Öste, R & Holst, OTexture promoting capacity and EPS formation by lactic acid bacteria in three oat-based nondairy media. Eur Food Res Technol (2002a) 214 232236.CrossRefGoogle Scholar
Mårtensson, O, Staaf, J, Dueñas-Chasco, M, Irastorza, A, Öste, R & Holst, OA fermented ropy non-dairy oat product based on the exopolysaccharide-producing strain Pediococcus damnosus 2.6. Adv Food Sci (2002b) 24 411.Google Scholar
Mathers, JC, Smith, H & Carter, SDose-response effects of raw potato starch on small-intestinal escape, large bowel fermentation and gut transit time in the rat. Br J Nutr (1997) 78 10151029.CrossRefGoogle ScholarPubMed
Mitsuoka, TThe human gastrointestinal tract. In The Lactic Acid Bacteria: The Lactic Acid Bacteria in Health and Disease, vol.1, pp.69114BJB, WoodNew York: Elsevier Applied Science. 1992Google Scholar
Mitsuoka, TIntestinal flora and human health. Asia Pac J Clin Nutr (1996) 5 29.Google ScholarPubMed
Mortensen, FV, Nielsen, H, Mulvany, MJ & Hessov, IShort chain fatty acids dilate isolated human colonic resistance arteries. Gut (1990) 31 13911394.CrossRefGoogle ScholarPubMed
Nagengast, FM, Hectors, MP, Buys, WA & van Tongeren, JHInhibition of secondary bile acid formation in the large intestine by lactulose in healthy subjects of two different age groups. Eur J Clin Invest (1988) 18 5661.CrossRefGoogle ScholarPubMed
Nakajima, H, Suzuki, Y, Kaizu, H & Hirota, TCholesterol lowering activity of ropy fermented milk. J Food Sci (1992) 6 13271329.CrossRefGoogle Scholar
Nilsson, U & Nyman, MShort-chain fatty acid formation in the hindgut of rats fed oligosaccharides varying in monomeric composition, degree of polymerisation and solubility. Br J Nutr (2005) 94 705713.CrossRefGoogle ScholarPubMed
Nyman, M & Asp, NGDietary fibre fermentation in the rat intestinal tract: effect of adaptation period, protein andfibre levels, and particle size. Br J Nutr (1985) 54 635643.CrossRefGoogle ScholarPubMed
Ozadali, F, Glatz, BA & Glatz, CEFed-batch fermentation with and without on-line extraction for propionic and acetic acid production by Propionibacterium acidipropionici. Appl Microbiol Biotechnol (1996) 44 710716.Google ScholarPubMed
Pedrosa, MC, Golner, BB, Goldin, BR, Barakat, S, Dallal, GE & Russei, RMSurvival of yoghurt-cotaining organisms and Lactobacillus grasseri (ADH) and their effect on bacterial enzyme activity in the gastrointestinal tract of healthy and hypochlorhydric elderly subjects. Am J Clin Nutr (1995) 61 353359.CrossRefGoogle ScholarPubMed
Perrin, P, Pierre, F, Patry, Y, Champ, M, Berreur, M, Pradal, G, Bornet, F, Meflah, K & Menanteau, JOnly fibres promoting a stable butyrate producing colonic ecosystem decrease the rate of aberrant crypt foci in rats. Gut (2001) 48 5361.CrossRefGoogle ScholarPubMed
Pretlow, TP, Barrow, BJ, Ashton, WS, O'Riordan, MA, Pretlow, TG, Jurcisek, JA & Stellato, TAAberrant crypts: putative preneoplastic foci in human colonic mucosa. Cancer Res (1991) 51 15641567.Google ScholarPubMed
Pretlow, TP, O'Riordan, MA, Somich, GA, Amini, SB & Pretlow, TGAberrant crypts correlate with tumor incidence in F344 rats treated with azoxymethane and phytate. Carcinogenesis (1992) 13 15091512.CrossRefGoogle ScholarPubMed
Ricciardi, A, Parente, E & Clementi, FA simple method for the screening of lactic acid bacteria for the production of exopolysaccharide in liquid media. Biotechnol Tech (1994) 11 271275.CrossRefGoogle Scholar
Richardson, AJ, Calder, AG, Stewart, CS & Smith, ASimultaneous determination of volatile and non-volatile acidic fermentation products of anaerobes by capillary gas chromatography. Lett Appl Microbiol (1989) 9 58.CrossRefGoogle Scholar
Robertson, JA, Ryden, P, Botham, RL, Reading, S, Gibson, G & Ring, SGStructural properties of diet-derived polysaccharides and their influence on butyrate production during fermentation. Lebensmittel-Wissenschaft Technol (2001) 34 567573.CrossRefGoogle Scholar
Roediger, WEUtilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology (1982) 83 424429.CrossRefGoogle ScholarPubMed
Ruppin, H, Bar-Meir, S, Soergel, KH, Wood, CM & Schmitt, MG JrAbsorption of short-chain fatty acids by the colon. Gastroenterology (1980) 78 15001507.CrossRefGoogle ScholarPubMed
Scheppach, W, Bartram, HP & Richter, FRole of short-chain fatty acids in the prevention of colorectal cancer. Eur J Cancer (1995) 31A, 10771080.CrossRefGoogle Scholar
Scheppach, W, Luehrs, H & Menzel, TBeneficial health effects of low-digestible carbohydrate consumption. Br J Nutr (2001) 85 Suppl.1S23S30.CrossRefGoogle ScholarPubMed
Scheppach, W, Sommer, H, Kirchner, T, Paganelli, GM, Bartram, P, Christi, S, Richter, F, Dusel, G & Kasper, HEffect of butyrate enemas on the colonic mucosa in distal ulcerative colitis. Gastroenterology (1992) 103 5156.CrossRefGoogle ScholarPubMed
Shivapurkar, N, Tang, ZC & Alabaster, OThe effects of highrisk and low-risk diets on aberrant crypt and colonic tumour formation in F344 rats. Carcinogenesis (1997) 13 887890.CrossRefGoogle Scholar
Sutherland, IWNovel and established applications of microbial polysaccharides. Trends Biotechnol (1998) 16 4146.CrossRefGoogle ScholarPubMed
Theander, O, Å man, P, Westerlund, E, Andersson, R & Pettersson, DTotal dietary fibre determination as neutral sugar residues, uronic acids residues and Klason lignin (the Uppsala method): collaborative study. J Assoc Off Anal Chemists Int (1995) 78 10301044.Google ScholarPubMed
Thorup, I, Meyer, O & Kristiansen, EEffect of potato starch, cornstarch and sucrose on aberrant crypt foci in rats exposed to azoxymethane. Anticancer Res (1995) 15 21012105.Google ScholarPubMed
Tsukahara, T, Koyama, H, Okada, M & Ushida, KStimulation of butyrate production by gluconic acid in batch culture of pig caecal digesta and identification of butyrate-producing bacteria. J Nutr (2002) 132 22292234.CrossRefGoogle ScholarPubMed
Tulung, B, Rémésy, C & Demigné, CSpecific effects of guar gum or gum arabic on adaptation of caecal digestion to high fibre diets in the rat. J Nutr (1987) 117 15561561.CrossRefGoogle ScholarPubMed
van Geel-Schutten, GH, Faber, EJ, Ten Brink, B, Kamerling, JP, Vliegenthart, JFG & Dijkhuizen, LBiochemical and structural characterisation of the glucan and fructan exopolysaccharides synthesised by the Lactobacillus reuteri wild-type strain and by mutant strains. Appl Environ Microbiol (1999) 65 30083014.CrossRefGoogle Scholar
Whitehead, RH, Young, GP & Bhathal, PSEffects of shortchain fatty acids on a new human colon carcinoma cell line (LIM1215). Gut (1986) 27 14571463.CrossRefGoogle Scholar
Wolever, TM, Spadafora, P & Eshuis, HInteraction between colonic acetate and propionate in humans. Am J Clin Nut (1991) 53 681687.CrossRefGoogle ScholarPubMed
Wright, RS, Anderson, JW & Bridges, SRPropionate inhibits hepatocyte lipid synthesis. Proc Soc Exp Biol Med (1990) 195 2629.CrossRefGoogle ScholarPubMed
Yajima, TContractile effect of short-chain fatty acids on the isolated colon of the rat. J Physiol (1985) 368 667678.CrossRefGoogle ScholarPubMed
Young, GP, McIntyre, A, Albert, V, Folino, M, Muir, JG & Gibson, PRWheat bran suppresses potato starch-potentiated colorectal tumorigenesis at the aberrant crypt stage in a rat model. Gastroenterology (1996) 110 508514.CrossRefGoogle ScholarPubMed