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The specificity of the interaction with intestinal bacterial fermentation by prebiotics determines their physiological efficacy

Published online by Cambridge University Press:  14 December 2007

Jan Van Loo
Jan Van Loo*
Affiliation:
ORAFTI, Aandorenstraat 1, B3300 Tienen, Belgium
*
Corresponding author: Dr J. Van Loo, fax +32 16 801359, email [email protected]
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Abstract

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The concept of prebiotic food ingredients is an important recent development in nutrition. The concept has attracted a great deal of attention, and many food ingredients (mainly dietary carbohydrates) have been claimed to be ‘prebiotic’. It is emphasised that in order to be called prebiotic, a compound should be: (1) non-digestible; (2) fermentable; (3) fermentable in a selective way. These properties should be demonstrated in human volunteers in at least two independent dietary intervention trials. On the basis of published and unpublished results, it is shown in the present paper that the way in which a prebiotic influences intestinal fermentation is the key to its physiological properties. This statement is illustrated mainly by considering an established group of prebiotics, the β(2–1) fructans. These linear molecules show a strong discontinuity in physicochemical properties as the chains become longer. The β(2–1) fructans with a chain length of up to ten monomer units are very soluble and are particularly ‘bifidogenic’. Longer chains (ten to sixty-five monomer units) are poorly soluble in water, they have less pronounced bifidogenic properties, and they are fermented more slowly. It was observed that a combination of short-chain and long-chain fructans (Synergy1) is physiologically (for example, increasing mineral absorption, suppressing carcinogenesis, modulating lipid metabolism, etc) more active than the individual fractions. A possible mechanism is described in the present review. From an in-depth overview of the literature it is confirmed that for prebiotic action, the ‘selectivity principle’ for intestinal fermentation is determinative for the type and for the efficiency of physiological activity. It is confirmed that prebiotics act through their influence on intestinal fermentation.

Keywords

PrebioticsIntestinal fermentationColonic bacteriaInulin
Type
Research Article
Information
Nutrition Research Reviews , Volume 17 , Issue 1 , June 2004 , pp. 89 - 98
Copyright
Copyright © The Author 2004

References

Alles, MS, De Roos, NM, Backx, JC, van de Lisdonk, E & Hautvast, J (1997) Consumption of fructo-oligosaccharides does not affect blood glucose and serum lipids in patients with type 2 diabetes. American Journal of Clinical Nutrition, 69, 64–69.CrossRefGoogle Scholar
Baeten, J (1999) Invloed van inuline-type fructanen op de darmflora : simulaties door middel van in vitro batchfermentaties met fecale slurry (On the influence of inulin-type fructans on the intestinal flora simulations by means of in vitro batch fermentations with faecal slurry). Thesis Vrije Universiteit Brussel, Brussels, Belgium.Google Scholar
Barrangou, R, Altermann, E, Hutkins, R, Cano, R & Klaenhammer, TR (2003) Functional and comparative genomic analyses of an operon involved in fructooligosaccharide utilization by Lactobacillus acidophilus. Proceedings of the National Academy of Sciences USA 100, 8957–8962.CrossRefGoogle ScholarPubMed
Brighenti, F, Casiraghi, MC, Canzi, E & Ferrari, A (1999) Effect of consumption of a ready-to-eat breakfast cereal containing inulin on the intestinal milieu and blood lipids in healthy male volunteers. European Journal of Clinical Nutrition 53, 726–733.CrossRefGoogle ScholarPubMed
Buddington, KK, Donahoo, JB & Buddington, RK (2002) Dietary oligofructose and inulin protect mice from enteric and systemic pathogens and tumor inducers. Journal of Nutrition 132, 472–477.CrossRefGoogle ScholarPubMed
Cashman, K (2003) Prebiotics and calcium bioavailability. Current Issues of Intestinal Microbiology 4, 21–32.Google ScholarPubMed
Cherbut, C, Salvador, V, Barry, J-LDF & Delort-Laval, J (1991) Dietary fibre effects on intestinal transit in man: involvement of their physicochemical and fermentative properties. Food Hydrocolloids 5, 15–22.CrossRefGoogle Scholar
Coudray, C, Bellanger, J, Castiglia-Delavaud, C, Remesy, C, Vermorel, M & Rayssiguier, Y (1997) Effect of soluble or partly soluble dietary fibres supplementation on absorption and balance of calcium, magnesium, iron and zinc in healthy young men. European Journal of Clinical Nutrition 51, 375–380.CrossRefGoogle ScholarPubMed
Coudray, C, Bellanger, J, Vermorel, M, Sinaud, S, Wils, D, Feillet-Coudray, C, Brandolini, M, Bouteloup-Demange, C & Rayssiguier, Y (2003 a) Two polyol, low digestible carbohydrates improve the apparent absorption of magnesium but not of calcium in healthy young men. Journal of Nutrition 133, 90–93.CrossRefGoogle Scholar
Coudray, C, Tressol, JC, Gueux, E & Rayssiguier, Y (2003 b) Effects of inulin-type fructans of different chain length and type of branching on intestinal absorption and balance of calcium and magnesium in rats. European Journal of Nutrition 42, 91–98.CrossRefGoogle ScholarPubMed
Cummings, JH, Christie, S & Cole, T (2001) A study of fructooligosaccharides in the prevention of travellers' diarrhoea. Alimentary Pharmacology and Therapeutics 15, 1139–1145.CrossRefGoogle Scholar
Cummings, JH, Rombeau, JL & Sakata, T (1995) Physiological and Clinical Aspects of Short-Chain Fatty Acids. Cambridge UK: Cambridge University Press.Google Scholar
Davidson, MH & Maki, KC (1999) Effects of dietary inulin on serum lipids. Journal of Nutrition 129, 1474S–1477S.CrossRefGoogle ScholarPubMed
Delzenne, N, Aertssens, J, Verplaetse, H, Roccaro, M & Roberfroid, M (1995) Effect of fermentable fructo-oligosaccharides on mineral, nitrogen and energy digestive balance in the rat. Life Sciences 57, 1579–1587.CrossRefGoogle ScholarPubMed
Den Hond, EM, Geypens, BJ & Ghoos, YF (1997) Effect of long chain chicory inulin on bowel habit and transit time in constipated persons. Nutrition Research 20, 731–736.CrossRefGoogle Scholar
Djouzi, Z & Andrieux, C (1997) Compared effects of three oligosaccharides on metabolism of intestinal microflora in rats inoculated with a human faecal flora. British Journal of Nutrition 78, 313–324.CrossRefGoogle ScholarPubMed
Ellegard, L, Andersson, H & Bosaeus, I (1997) Inulin and oligofructose do not influence the absorption of cholesterol, or the excretion of cholesterol, Ca, Mg, Zn, Fe, or bile acids but increases energy excretion in ileostomy subjects. European Journal of Clinical Nutrition 51, 1–5.CrossRefGoogle ScholarPubMed
Femia, AP, Luceri, C, Dolara, P, Giannini, A, Biggeri, A, Salvadori, M, Clune, Y, Collins, KJ, Paglierani, M & Caderni, G (2002) Antitumorigenic activity of the prebiotic inulin enriched with oligofructose in combination with the probiotics Lactobacillus rhamnosus and Bifidobacterium lactis on azoxymethane-induced colon carcinogenesis in rats. Carcinogenesis 23, 1953–1960.CrossRefGoogle ScholarPubMed
Gibson, GR, Beatty, ER, Wang, X & Cummings, JH (1995) Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology 108, 975–982.CrossRefGoogle ScholarPubMed
Gibson, GR & Roberfroid, MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. Journal of Nutrition 125, 1401–1412.CrossRefGoogle ScholarPubMed
Griffin, IJ, Davila, PM & Abrams, SA (2002) Non-digestible oligosaccharides and calcium absorption in girls with adequate calcium intakes. British Journal of Nutrition 87 Suppl. 2, S187–S191.CrossRefGoogle ScholarPubMed
Harmsen, H, Raangs, G, Franks, A, Wildeboeer-Veloo, A & Welling, G (2002) The effect of the prebiotic inulin and the probiotic Bifidobacterium longum on the fecal microflora of healthy volunteers measured by FISH and DGGE. Microbial Ecology in Health and Disease 14, 211–219.CrossRefGoogle Scholar
Hopkins, M, Cummings, J & Macfarlane, G (1998) Inter-species differences in maximum specific growth rates and cell yield of bifidobacteria cultured on oligosaccharides and other simple carbohydrate sources. Journal of Applied Microbiology 85, 381–386.CrossRefGoogle Scholar
Jackson, KG, Taylor, GR, Clohessy, AM & Williams, CM (1999) The effect of the daily intake of inulin on fasting lipid, insulin and glucose concentrations in middle-aged men and women. British Journal of Nutrition 82, 23–30.CrossRefGoogle ScholarPubMed
Kelly-Quagliana, KA, Nelson, PD & Buddington, RK (2003) Dietary oligofructose and inulin modulate immune functions in mice. Nutrition Research 23, 257–267.CrossRefGoogle Scholar
Klinder, A, Gietl, E, Hughes, R, Jonkers, N, Karlsson, P, McGlyn, H, Pistoli, S, Tuohy, K, Rafter, J, Rowland, I, Van Loo, J & Pool-Zobel, B (2003) Gut fermentation products of chicory inulin-derived prebiotics inhibit markers of tumor progression in human colon tumor cells. Proceedings of the 2nd meeting of Frontiers in Cancer Prevention Research.Google Scholar
Kok, NN, Morgan, LM, Williams, CM, Roberfroid, MB, Thissen, JP & Delzenne, NM (1998) Insulin, glucagon-like peptide 1, glucose-dependent insulinotropic polypeptide and insulin-like growth factor I as putative mediators of the hypolipidemic effect of oligofructose in rats. Journal of Nutrition 128, 1099–1103.CrossRefGoogle ScholarPubMed
Letexier, D, Diraison, F & Beylot, M (2003) Addition of inulin to a moderately high-carbohydrate diet reduces hepatic lipogenesis and plasma triacylglycerol concentrations in humans. American Journal of Clinical Nutrition 77, 559–564.CrossRefGoogle ScholarPubMed
Marchessault, R (1980) Conformation and crystalline structure of (2–1)-beta-D-fructofuranan (inulin). Canadian Journal of Chemistry 58, 2415–2422.CrossRefGoogle Scholar
Newton, D, Cummings, JH, Macfarlane, S & Macfarlane, G (1998) Growth of a human intestinal Desulfovibrio desulfuricans in continuous cultures containing defined populations of saccharolytic and amino acid fermenting bacteria. Journal for Applied Microbiology 85, 371–380.CrossRefGoogle ScholarPubMed
Ohta, A, Motohashi, Y, Ohtsuki, M, Hirayama, M, Adachi, T & Sakuma, K (1998) Dietary fructooligosaccharides change the concentration of calbindin-D9k differently in the mucosa of the small and large intestine of rats. Journal of Nutrition 128, 934–939.CrossRefGoogle ScholarPubMed
Pedersen, AA, Sandstrom, B & Van Amelsvoort, JMM (1997) The effect of ingestion of inulin on blood lipids and gastrointestinal symptoms in healthy females. British Journal of Nutrition 78, 215–222.CrossRefGoogle ScholarPubMed
Pereira, DI & Gibson, GR (2002) Effects of consumption of probiotics and prebiotics on serum lipid levels in humans. Critical Reviews in Biochemistry and Molecular Biology 37, 259–281.CrossRefGoogle ScholarPubMed
Pierre, F, Perrin, P, Champ, M, Bornet, F, Meflah, K & Menanteau, J (1997) Short-chain fructo-oligosaccharides reduce the occurrence of colon tumors and develop gut-associated lymphoid tissue in Min mice. Cancer Research 57, 225–228.Google ScholarPubMed
Reddy, BS, Hamid, R & Rao, CV (1997) Effect of dietary oligofructose and inulin on colonic preneoplastic aberrant crypt foci inhibition. Carcinogenesis 18, 1371–1374.CrossRefGoogle ScholarPubMed
Roberfroid, MB, Van Loo, JA & Gibson, GR (1998) The bifidogenic nature of chicory inulin and its hydrolysis products. Journal of Nutrition 128, 11–19.CrossRefGoogle ScholarPubMed
Swanson, KS, Grieshop, CM, Flickinger, EA, Bauer, LL, Wolf, BW, Chow, JM, Garleb, KA, Williams, JA & Fahey, GC (2002) Fructooligosaccharides and Lactobacillus acidophilus modify bowel function and protein catabolites excreted by healthy humans. Journal of Nutrition 132, 3042–3050.CrossRefGoogle ScholarPubMed
Tahiri, M, Tressol, JC, Arnaud, J, Bornet, F, Bouteloup-Demange, C, Feillet-Coudray, C, Ducros, V, Pepin, D, Brouns, F, Rayssiguier, AM & Coudray, C (2001) Five-week intake of short-chain fructo-oligosaccharides increases intestinal absorption and status of magnesium in postmenopausal women. Journal of Bone Mineralisation Research 16, 2152–2160.CrossRefGoogle ScholarPubMed
Tahiri, M, Tressol, JC, Arnaud, J, Bornet, FR, Bouteloup-Demange, C, Feillet-Coudray, C, Brandolini, M, Ducros, V, Pepin, D, Brouns, F, Roussel, AM, Rayssiguier, Y & Coudray, C (2003) Effect of short-chain fructooligosaccharides on intestinal calcium absorption and calcium status in postmenopausal women: a stable-isotope study. Amercian Journal of Clinical Nutrition 77, 449–457.CrossRefGoogle ScholarPubMed
Taper, HS, Delzenne, NM & Roberfroid, MB (1997) Growth inhibition of transplantable mouse tumors by non-digestible carbohydrates. International Journal of Cancer Research 71, 1109–1112.3.0.CO;2-5>CrossRefGoogle ScholarPubMed
Taper, HS, Lemort, C & Roberfroid, MB (1998) Inhibition effect of dietary inulin and oligofructose on the growth of transplantable mouse tumor. Anticancer Research 18, 4123–4126.Google ScholarPubMed
Tuohy, K, Finlay, RK, Wynne, AG & Gibson, GR (2001) A human volunteer study on the prebiotic effects of HP-inulin – faecal bacteria enumerated using fluorescent in situ hybridisation (FISH). Anaerobe 7, 113–118.CrossRefGoogle Scholar
van den Heuvel, EG, Muys, T, van Dokkum, W & Schaafsma, G (1999) Oligofructose stimulates calcium absorption in adolescents. American Journal of Clinical Nutrition 69, 544–548.CrossRefGoogle ScholarPubMed
van den Heuvel, EG, Schaafsma, G, Muys, T & van Dokkum, W (1998) Nondigestible oligosaccharides do not interfere with calcium and nonheme-iron absorption in young, healthy men. American Journal of Clinical Nutrition 67, 445–451.CrossRefGoogle Scholar
van Dokkum, W, Wezendonk, B, Srikumar, TS & van den Heuvel, EG (1999) Effect of nondigestible oligosaccharides on large-bowel functions, blood lipid concentrations and glucose absorption in young healthy male subjects. European Journal of Clinical Nutrition 53, 1–7.CrossRefGoogle ScholarPubMed
Van Loo, J, Cummings, J, Delzenne, N, Englyst, H, Franck, A, Hopkins, M, Kok, N, Macfarlane, G, Newton, D, Quigley, M, Roberfroid, M, van Vliet, T & van den Heuvel, E (1999) Functional food properties of non-digestible oligosaccharides: a consensus report from the ENDO project (DGXII AIRII-CT94–1095). British Journal of Nutrition 81, 121–132.Google ScholarPubMed
Van Loo, J & Jonkers, N (2001) Evaluation in human volunteers of the potential anticarcinogenic activities of novel nutritional concepts: prebiotics probiotics and synbiotics (the SYNCAN project). Nutrition and Metabolic Cardiovascular Disease 11, 87–93.Google ScholarPubMed
Van Loo, J, Coussement, P, De Leenheer, L, Hoebregs, H & Smits, G (1995) On the presence of inulin and oligofructose as natural ingredients in the western diet. Critical Reviews in Food Science and Nutrition 35, 525–552.CrossRefGoogle ScholarPubMed
van Vliet, T (1997) A Double Blind Placebo Controlled, Parallel Trial on the Effect of Oligofructose Intake on Serum Lipids in Male Volunteers. TNO Report V 97.874. Zeist The Netherlands: TNO.Google Scholar
Verghese, M, Rao, DR, Chawan, CB & Shackelford, L (2002 a) Dietary inulin suppresses azoxymethane-induced preneoplastic aberrant crypt foci in mature Fisher 344 rats. Journal of Nutrition 132, 2804–2808.CrossRefGoogle ScholarPubMed
Verghese, M, Rao, DR, Chawan, CB, Williams, LL & Shackelford, L (2002 b) Dietary inulin suppresses azoxymethane-induced aberrant crypt foci and colon tumors at the promotion stage in young Fisher 344 rats. Journal of Nutrition 132, 2809–2813.CrossRefGoogle ScholarPubMed
Verghese, M, Walker, LT, Shackelford, L, Chawan, CB & Van Loo, J (2003) Inhibitory effects of non-digestible carbohydrates of different chain lengths on AOM-induced aberrant crypt foci in Fisher 344 rats. Proceedings of the 2nd meeting of Frontiers in Cancer Prevention Research.Google Scholar
Wang, X & Gibson, GR (1993) Effects of the in vitro fermentation of oligofructose and inulin by bacteria growing in the human large intestine. Journal of Applied Bacteriology 75, 373–380.CrossRefGoogle ScholarPubMed
Younes, H, Coudray, C, Bellanger, J, Demigne, C, Rayssiguier, Y & Remesy, C (2001) Effects of two fermentable carbohydrates (inulin and resistant starch) and their combination on calcium and magnesium balance in rats. British Journal of Nutrition 86, 479–485.CrossRefGoogle ScholarPubMed