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Compared effects of three oligosaccharides on metabolism of intestinal microflora in rats inoculated with a human faecal flora

Published online by Cambridge University Press:  09 March 2007

Zakia Djouzi
Affiliation:
Laboratoire d'Ecologie et de Physiologie du Système Digestif, Bât, 440, INRA-CRJ, 78352 Jouy en Josas Cedex, France
Claude Andlueux
Affiliation:
Laboratoire d'Ecologie et de Physiologie du Système Digestif, Bât, 440, INRA-CRJ, 78352 Jouy en Josas Cedex, France
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Abstract

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Using germ-free rats inoculated with a human faecal flora (gnotobiotic rats), the effects of three oligosaccharides (β-fructo-oligosaccharides (FOS), β-galacto-oligosaccharides (TOS) and α-gluco-oligosaccharides (GOS)) on intestinal bacterial metabolism were compared. The animals were fed on either a control diet or diets containing 4Og/kg of GOS, FOS or TOS. FOS and TOS were the preferred growth substrates for Bifidobacteria which increased in number by 2 log values in faeces of rats when compared with rats fed on GOS or control diets. Ingestion of TOS specifically induced hydrolysis of the substrate, and did not modify the activity of any other enzymes measured in the caecum. GOS led to a non-specific enzymic induction of β-galactosidase (EC 3.2.1.23), β-glucosidase (EC 3.2.1.21) and α-glucosidase (EC 3.2.1.20) activities whereas β-glucuronidase (EC 3.2.1.31) was lowered. Compared with the control group, FOS and TOS diets led to a significant increase in H2 and CH4 excretion; the GOS diet increased only CH4. Analysis of caecal contents revealed a decrease in pH for all diets compared with controls. Total short-chain fatty acid (SCFA) concentration increased significantly in all groups, but the SCFA profile differed between treatment groups. It was concluded that the three oligosaccharides studied had different effects which may be linked to their chemical structure. Some of these effects may be beneficial to human health

Type
General Nutrition
Copyright
Copyright © The Nutrition Society 1997

References

REFERENCES

Absolonne, J., Jossart, M., Coussement, P. & Roberfoid, M. (1995). Digestive acceptability of oligofructose. First Orafti Research Conference, Proceedings, pp. 135144. Tienen, Belgium:Orafti.Google Scholar
Andrieux, C., Lory, S., Dufour-Lescoat, C., de Baynast, R. & Szylit, O. (1991). Physiological effects of inulin in germ-free rats and in heteroxenic rats inoculated with a human flora. Food Hydrocolloids 5, 4956.CrossRefGoogle Scholar
Beerens, H. (1990). An elective and selective isolation medium for Bifidobacterium spp. Letters in Applied Microbiology 11, 155157.CrossRefGoogle Scholar
Bergman, E. N. (1990). Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiological Reviews 70, 567590.CrossRefGoogle ScholarPubMed
Bond, J. H., Engel, R. R. & Levitt, M. D. (1971). Factors influencing pulmonary methane excretion in man. Journal of Experimental Medicine 133, 572588.CrossRefGoogle ScholarPubMed
Bouhnik, Y., Flourié, B., Ouamé, F., Bisetti, N., Bornet, F. & Rambaud, J. C. (1994). Effets de l'administration prolongée de fructo-oligosaccharides (Actilight®) sur la flore bactérienne colique de l'homme (Effects of chronic fructo-oligosaccharides (Actilight®) ingestion on the human colonic microflora). Gastroentérologie Clinique et Biologique 18, 50A.Google Scholar
Debure, A., Colombel, J. F., Flourié, B., Rautureau, M. & Rambaud, J. C. (1989). Comparaison de l'implantation et de l'activité métabolique d'une flore fécale de rat et d'une flore fécale humaine inoculées chez le rat axénique (Implantation and metabolic activity of rat and human faecal bacterial flora administered to germ-free rats). Gastroentérologie Clinique et Biologique 13, 2531.Google Scholar
Delzenne, N., Kok, N., Fiordalso, M. F., Deboyser, D., Goethals, F. & Roberfroid, M. (1993). Dietary fructooligosaccharides modify lipid metabolism in the rat. American Journal of Clinical Nutrition 57, Suppl. 820.CrossRefGoogle Scholar
De Simone, C., Vesely, R., Bianchi Salvadori, B. & Jirillo, E. (1993). Influence of long term yoghurt consumption in young adults. International Journal of Immunotherapy 7, 205210.Google Scholar
Djouzi, Z., Andrieux, C., Pelenc, V., Somaniba, S., Popot, F., Paul, F., Monsan, P. & Szylit, O. (1995). Degradation and fermentation of α-gluco-oligosaccharides by bacterial strains from human colon: in vitro and in vivo studies in gnotobiotic rats. Journal of Applied Bacteriology 79, 117127.CrossRefGoogle Scholar
Drevon, T. & Bomet, F. (1992). Les fructo-oligosaccharides, Actilight® (Fructo-oligosaccharides, Actilight®). In Sucre, Produits Sucrants, Edulcorants et Substances Glucidiques de Charge dans les Industries Alimentaires. Techniques et Documentation. Collection Sciences et Techniques Agro-Alimentaires. pp. 314337 [Multon, J. L., editor]. Paris: Lavoisier et Apria.Google Scholar
Dropsy, G. & Boy, J. (1965). Détermination de l'ammonitmie (méthode automatique par dialyse) (Ammonia determination in urine). Annales de Biologie Clinique 19, 313318.Google Scholar
Femandes, C. F. & Shahani, K. M. (1990). Anticarcinogenic and immunological properties of dietary lactobacilli. Journal of Food Protection 53, 704710.CrossRefGoogle Scholar
Gibson, G. R., Beatty, E. R., Wang, X. & Cummings, J. H. (1995). Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology 108, 975982.CrossRefGoogle ScholarPubMed
Gilliland, S. E. (1990). Health and nutritional benefits from lactic acid bacteria. FEMS Microbiology Reviews 87, 175188.CrossRefGoogle Scholar
Goldin, B. R. & Gorbach, S. L. (1984). The effect of milk and Lactobacillus feeding on human intestinal bacterial enzyme activity. American journal of Clinical Nutrition 39, 756761.CrossRefGoogle ScholarPubMed
Grimble, G. (1989). Fibre, fermentation, flora and flatus. Gut 30, 613.CrossRefGoogle ScholarPubMed
Hidaka, H., Eida, T., Takizawa, T., Tokunga, T. & Tashiro, Y. (1986). Effects of fructooligosaccharides on intestinal flora and human health. Bifdobacteria Microfora 5, 3750.CrossRefGoogle Scholar
Hidaka, H. & Hirayama, M. (1991). Useful characteristics and commercial applications of fructo-oligosaccharides. Biochemical Society Transactions 19, 561565.CrossRefGoogle ScholarPubMed
Hitchins, A. D. & McDonough, F. E. (1989). Prophylactic and therapeutic aspects of fermented milk. American Journal of Clinical Nutrition 49, 675684.CrossRefGoogle ScholarPubMed
Ito, M., Deguchi, Y., Matsumoto, K., Kimura, M., Onodera, N. & Yajima, T. (1993). Influence of galactooligosaccharides on the human faecal microflora. Journal of Nutritional Science and Vitaminology 39, 635640.CrossRefGoogle Scholar
Ito, M., Deguchi, Y., Miyamori, A., Matsumoto, K., Kikuchi, H., Matsumoto, K., Kobayashi, Y., Yajima, T. & Kan, T. (1990). Effects of administration of galactooligosaccharides on the human faecal microflora, stool weight and abdominal sensation. Microbial Ecology in Health and Disease 3, 285292.CrossRefGoogle Scholar
Kikuchi, H., Andrieux, C., Riottot, M., Bensaada, M., Popot, F., Beaumatin, P. & Szylit, O. (1996). Effect of two levels of transgalactosylated oligosaccharide intake in rats associated with human faecal microflora on bacterial glycolytic activity, end-products of fermentation and bacterial steroid transformation. Journal of Applied Bacteriology 80, 439446.CrossRefGoogle ScholarPubMed
Kikuchi, H., Andrieux, C. & Szylit, O. (1992). Effects of galacto-oligosacharides on bacterial enzymic activities and metabolite production in rats associated with a human flora. Proceedings of the Nutrition Society 51, 7A.Google Scholar
Le Coz, Y., Morel, M. T., Bousseboua, H., Dufour, C. & Szylit, O. (1989). Mise au point d'une chambre respiratoire connectée sur l'isolateur pour la mesure in vivo des gaz de fermentation chez l'animal gnotoxénique (Respiratory chamber associated to isolator for measuring the in vivo production of gas in the gnotobiotic animal). Science et Technologie des Animaux de Laboratoire 14, 3539.Google Scholar
Lupton, J. R. (1995). Short-chain fatty acids and colon tumorigenesis: animal models. In Physiological and Clinical Aspects of Short-Chain Fatty Acids, pp. 308318 [Cummings, J. H., Rombeau, J. L. and Sakata, T., editors]. Cambridge: Cambridge University Press.Google Scholar
Macfarlane, G. T. & Cummings, J. H. (1991). The colonic flora, fermentation and large bowel digestive function. In The Large Intestine: Physiology, Pathophysiology and Disease, pp. 5192[ Phillips, S. F., Pemberton, J. H. and Shorter, R. G., editors]. New York: Raven Press.Google Scholar
Mallett, A. K., Bearne, C. A. & Rowland, I. R. (1989). The influence of incubation pH on the activity of rat and human gut flora enzymes. Journal of Applied Bacteriology 66, 433437.CrossRefGoogle ScholarPubMed
Mallett, A. K., Bearne, C. A., Rowland, I. R., Farthing, M. G. J., Cole, C. B. & Fuller, R. (1987). The use of rats associated with a human faecal flora as a model for studying the effects of diet on the human gut microflora. Journal of Applied Bacteriology 63, 3945.CrossRefGoogle Scholar
Mallet, A. K. & Rowland, I. R. (1988). Factors affecting the gut microflora. In Role of the Gut Flora in Toxicity and Cancer, pp. 347382. London: Academic Press.CrossRefGoogle Scholar
Marteau, P., Pochart, P., Flourié, B., Pellier, P., Santos, L., Desjeux, J. F. & Rambaud, J. C. (1990). Effect of chronic ingestion of fermented dairy product containing Lactobacillus acidophilus and Bijidobacterium bijidum on metabolic activities of the colonic flora in humans. American Journal of Clinical Nutrition 52, 685688.CrossRefGoogle ScholarPubMed
Matsumoto, K., Kobayashi, Y., Tamura, N., Watanabe, T. & Kan, T. (1989). Production of galactooligo-saccharides with β-galactosidase. Denpum Kagaku 36, 123130.Google Scholar
Mitsuoka, T. (1982). Recent trends in research on intestinal flora. Bijidobacteria Microfora 1, 324.CrossRefGoogle Scholar
Mitsuoka, T. (1992). The human gastrointestinal tract. In The Lactic Acid Bacteria in Health and Disease, vol. 1, pp. 69114 [Woods, B. J. B., editor]. London and New York: Elsevier Applied Science.Google Scholar
Mitsuoka, T., Hidaka, H. & Eida, T. (1987). Effect of fructo-oligosaccharides on intestinal microflora. Die Nahrung 31, 427436.CrossRefGoogle ScholarPubMed
Morishita, Y., Knishi, Y., Tanaka, R. & Mutai, M. (1992). The effect of transgalactosylated oligosaccharide (TOS) on the intestinal microflora and the heat resistance of fecal bacteria in rats. Bijidus 6, 1117.Google Scholar
Mutai, M. & Tanaka, R. (1987). Ecology of Bijdobacterium in the human intestinal flora. Bifidobacteria Microfora 6, 3341.CrossRefGoogle Scholar
Nishina, P. M. & Freedland, R. A. (1990). Effects of propionate on lipid biosynthesis in isolated rat hepatocytes. Journal of Nutrition 120, 668675.CrossRefGoogle ScholarPubMed
Oku, T. (1994). Special physiological functions of newly developed mono- and oligosaccharides. In Functional Foods Designer Foods, Pharmufoods, Nutraceuticals, pp. 202218 [Goldberg, I., editor]. New York: Chapman & Hall.CrossRefGoogle Scholar
Roediger, W. E. W. (1980). Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa. Gut 21, 793798.CrossRefGoogle ScholarPubMed
Roediger, W. E. W. (1982). Utilization of nutrients by isolated epithelial cells of rat colon. Gastroenterology 83, 424429.CrossRefGoogle ScholarPubMed
Roland, N., Nugon-Baudon, L. & Rabot, S. (1993). Interactions between the intestinal flora and xenobiotic metabolizing enzymes and their health consequences. World Review of Nutrition and Dietetics 74, 123148.CrossRefGoogle ScholarPubMed
Rowland, I. R. (1988). Factors affecting metabolic activity of the intestinal microflora. Drug Metabolism Reviews 19, 243261.CrossRefGoogle ScholarPubMed
Rowland, I. R. & Tanaka, R. (1993). The effects of transgalactosylated oligosaccharides on gut flora metabolism in rats associated with human faecal microflora. Journal of Applied Bacteriology 74, 667674.CrossRefGoogle ScholarPubMed
Rumney, C. J. & Rowland, I. R. (1992). In vivo and in vitro models of the human colonic flora. Critical Reviews in Food Science and Nutrition 31, 299331.CrossRefGoogle ScholarPubMed
Saavedra, J. M., Bauman, N. A., Oung, I., Perman, J. A. & Yolken, R. H. (1994). Feeding of Bifidobacteriurn bifidum and Streptococcus thennophilus to infants in hospital for prevention of diarrhoea and shedding of rotavirus. Lancet 344, 10461049.CrossRefGoogle ScholarPubMed
Schriffrin, E. J., Rochat, F., Link-Amster, H., Aeschlimann, J. M. & Donnet-Hugues, A. (1995). Immunomodulation of human blood cells following the ingestion of lactic acid bacteria. Journal of Dairy Science 78, 491497.CrossRefGoogle Scholar
Segal, I., Walker, A. R. P., Lord, S. & Cummings, J. H. (1988). Breath methane and large bowel cancer risk in contrasting African populations. Gut 29, 608613.CrossRefGoogle ScholarPubMed
Tamura, Z. (1983). Nutriology of Bifidobacteria. Bijidobacteria Microfora 2, 316.CrossRefGoogle Scholar
Tanaka, R., Takayama, H., Morotomi, M., Kuroshima, T., Ueyama, S., Matsumoto, K., Kuroda, A. & Mutai, M. (1983). Effects of administration of TOS and Bijidobacterium breve 4006 on the human faecal flora. Bijidobacteria Microfora 2, 1724.CrossRefGoogle Scholar
Tokunaga, T., Oku, T. & Hosoya, N. (1986). Influence of chronic intake of new sweetener fructo-oligosaccharide (Neosugar) on growth and gastrointestinal function of the rat. Journal of Nutritional Science and Vitaminology 32, 111121.CrossRefGoogle Scholar
Trexler, P. C. (1959). The use of plastics in the design of isolator systems. Annals of the New York Academy of Sciences 78, 2936.CrossRefGoogle ScholarPubMed
Uchida, K., Nomura, Y. & Takeuchi, N. (1980). Effect of cholic acid, chenodeoxycholic acid, and their related bile acids on cholesterol, phospholipid, and bile acids levels in serum, liver, bile, and faeces of rats. Journal of Biochemistry 87, 187194.CrossRefGoogle ScholarPubMed
Valette, P., Pelenc, V., Djouzi, Z., Andrieux, C., Paul, F., Monsan, P. & Szylit, O. (1993). Bioavailability of new synthesised glucooligosaccharides in the intestinal tract of gnotobiotic rats. Journal of the Science of Food and Agriculture 62, 121127.CrossRefGoogle Scholar
Wang, X. & Gibson, G. R. (1993). Effects of the in vitro fermentation of oligofructose and inulin by bacteria growing in the human large intestine. Journal of Applied Bacteriology 75, 373380.CrossRefGoogle ScholarPubMed
Williams, C. H., Witherly, S. A. & Buddington, R. K. (1994). Influence of dietary neosugar on selected bacterial groups of the human faecal microbiota. Microbial Ecology in Health and Disease 7, 9197.CrossRefGoogle Scholar