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Supplementation of difructose anhydride III enhanced elevation of plasma equol concentrations and lowered plasma total cholesterol in isoflavone-fed rats

Published online by Cambridge University Press:  19 February 2008

Akiko Tamura ,
Megumi Nishimukai ,
Norihiro Shigematsu  and
Hiroshi Hara
Akiko Tamura
Affiliation:
Research Institute, FANCL Co., 12-13 Kamishinano Totsuka-Ku, Yokohama 244-0806, Japan Division of Applied Bioscience, Graduate School of Agriculture, Hokkaido University Kita-9 Nisi-9 Kita-Ku, Sapporo 060-8589, Japan
Megumi Nishimukai
Affiliation:
Division of Applied Bioscience, Graduate School of Agriculture, Hokkaido University Kita-9 Nisi-9 Kita-Ku, Sapporo 060-8589, Japan
Norihiro Shigematsu
Affiliation:
Research Institute, FANCL Co., 12-13 Kamishinano Totsuka-Ku, Yokohama 244-0806, Japan
Hiroshi Hara*
Affiliation:
Division of Applied Bioscience, Graduate School of Agriculture, Hokkaido University Kita-9 Nisi-9 Kita-Ku, Sapporo 060-8589, Japan
*
*Corresponding author: Dr Hiroshi Hara, fax +81 11 706 2504, email [email protected]
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Abstract

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Equol, a derivative of daidzein produced by enterobacteria, has greater activity as a phyto-oestrogen compared with daidzein. Difructose anhydride III (DFAIII) is a newly manufactured non-digestible disaccharide with unique fermentation properties. The present study evaluated the prebiotic effects of DFAIII on equol production and on plasma cholesterol concentrations related to the changes in equol production. We compared plasma equol concentrations at 10.00 and 18.00 hours and faecal isoflavone excretion in three groups of seven rats (male Wistar-ST strain, 6 weeks old) fed a basal diet or a DFAIII or fructooligosaccharide (15/g diet) diet containing 1g soya isoflavone/g diet for 20d. Equol concentrations in the DFAIII group were higher than in the control and fructooligosaccharides groups, especially in the later phase of the light period (18.00 hours) throughout the experiment. Daizein and genistein concentrations did not change between the diet groups. The faecal ratios of equol:daidzein were very high in all groups, but the ratios were higher in the DFAIII group than the control and fructooligosaccharide groups on day 3, and this tendency continued throughout the experiment. On day 20, the plasma total cholesterol concentration was lowest in the DFAIII group. Additionally, the cholesterol concentrations were inversely correlated to plasma equol concentration in all the rats. In conclusion, DFAIII efficiently enhanced plasma equol concentrations, which may be associated with an increase in equol production and a decrease in equol degradation by enterobacteria. Higher plasma equol concentrations may contribute to the hypocholesterolaemic effect of DFAIII feeding.

Keywords

Difructose anhydride IIIFructooligosaccharidesEquolTotal cholesterol
Type
Research Article
Information
British Journal of Nutrition , Volume 96 , Issue 3 , September 2006 , pp. 442 - 449
Copyright
Copyright © The Nutrition Society 2006

References

Afsana, K, Shiga, K, Ishizuka, S & Hara, H (2003) Ingestion of an indigestible saccharide, difructose anhydride III, partially prevents the tannic acid-induced suppression of iron absorption in rats. J Nutr 133, 3553–3560.CrossRefGoogle ScholarPubMed
Akaza, H, Miyanaga, N, Takashima, N (2004) Comparisons of percent equol producers between prostate cancer patients and controls: case-controlled studies of isoflavones in Japanese, Korean and American residents. Jpn J Clin Oncol 34, 86–89.CrossRefGoogle ScholarPubMed
Ali, AA, Velasquez, MT, Hansen, CT, Mohamed, AI & Bhathena, SJ (2004) Effects of soybean isoflavones, probiotics, and their interactions on lipid metabolism and endocrine system in an animal model of obesity and diabetes. J Nutr Biochem 15, 583–590.CrossRefGoogle Scholar
Atkinson, C, Berman, S, Humbert, O & Lampe, JW (2004) In vitro incubation of human feces with daidzein and antibiotics suggests interindividual differences in the bacteria responsible for equol production. J Nutr 134, 596–599.CrossRefGoogle ScholarPubMed
Blair, RM, Appt, SE, Bennetau-Pelissero, C, Clarkson, TB, Anthony, MS, Lamothe, V & Potter, SM (2002) Dietary soy and soy isoflavones have gender-specific effects on plasma lipids and isoflavones in golden Syrian f(1)b hybrid hamsters. J Nutr 132, 3585–3591.CrossRefGoogle ScholarPubMed
Bonorden, MJ, Greany, KA, Wangen, KE, Phipps, WR, Feirtag, J, Adlercreutz, H & Kurzer, MS (2004) Consumption of Lactobacillus acidophilus and Bifidobacterium longum do not alter urinary equol excretion and plasma reproductive hormones in premenopausal women. Eur J Clin Nutr 58, 1635–1642.CrossRefGoogle Scholar
Horn-Ross, PL, John, EM, Canchola, AJ, Stewart, SL & Lee, MM (2003) Phytoestrogen intake and endometrial cancer risk. J Natl Cancer Inst 95, 1158–1164.CrossRefGoogle ScholarPubMed
Kawakami, Y, Tsurugasaki, W, Yoshida, Y, Igarashi, Y, Nakamura, S & Osada, K (2004) Regulative actions of dietary soy isoflavone on biological antioxidative system and lipid metabolism in rats. J Agric Food Chem 52, 1764–1768.CrossRefGoogle ScholarPubMed
King, RA (1998) Daidzein conjugates are more bioavailable than genistein conjugates in rats. Am J Clin Nutr 68, 1496S–1499S.CrossRefGoogle ScholarPubMed
Kirk, EA, Sutherland, P, Wang, SA, Chait, A & LeBoeuf, RC (1998) Dietary isoflavones reduce plasma cholesterol and atherosclerosis in C57B/ mice but not LDL receptor-deficient mice. J Nutr 128, 954–959.CrossRefGoogle Scholar
Mathey, J, Puel, C, Kati-Coulibaly, S, Bennetau-Pelissero, C, Davicco, MJ, Lebecque, P, Horcajada, MN & Coxam, V (2004) Fructooligosaccharides maximize bone-sparing effects of soy isoflavone-enriched diet in the ovariectomized rat. Calcif Tissue Int 75, 169–179.CrossRefGoogle ScholarPubMed
Meyer, BJ, Larkin, TA, Owen, AJ, Astheimer, LB, Tapsell, LC & Howe, PR (2004) Limited lipid-lowering effects of regular consumption of whole soybean foods. Ann Nutr Metab 48, 67–78.CrossRefGoogle ScholarPubMed
Minamida, K, Shiga, K, Sujaya, IN, Sone, T, Yokota, A, Hara, H, Asano, K & Tominta, F (2005) Effects of difructose anhydride III (DFA III) administration on rat intestinal microbiota. J Biosci Bioeng 99, 230–236.CrossRefGoogle ScholarPubMed
Minamida, K, Sujaya, N, Tamura, A, Shigematsu, N, Sone, T, Yokota, A, Asano, K, Benno, Y & Tomita, F (2004) The effects of Di-D-fructofuranose-1,2′:2,3′-dianhydride (DFA III) administration on human intestinal microbiota. J Biosci Bioeng 98, 244–250.CrossRefGoogle Scholar
Mitamura, R, Hara, H, Aoyama, Y & Chiji, H (2002) Supplemental feeding of difructose anhydride III restores calcium absorption impaired by ovariectomy in rats. J Nutr 132, 3387–3393.Google ScholarPubMed
Nettleton, JA, Greany, KA, Thomas, W, Wangen, KE, Adlercreutz, H & Kurzer, MS (2004) Plasma phytoestrogens are not altered by probiotic consumption in postmenopausal women with and without a history of breast cancer. J Nutr 134, 1998–2003.CrossRefGoogle Scholar
Nettleton, JA, Greany, KA, Thomas, W, Wangen, KE, Adlercreutz, H & Kurzer, MS (2005) The effect of soy consumption on the urinary 2:16-hydroxyestrone ratio in postmenopausal women depends on equol production status but is not influenced by probiotic consumption. J Nutr 135, 603–608.CrossRefGoogle Scholar
Ohta, A, Uehara, M, Sakai, K, Takasaki, M, Adlercreutz, H, Morohashi, T & Ishimi, Y (2002) A combination of dietary fructooligosaccharides and isoflavone conjugates increases femoral bone mineral density and equol production in ovariectomized mice. J Nutr 132, 2048–2054.CrossRefGoogle ScholarPubMed
Rowland, I, Faughnan, M, Hoey, L, Wahala, K, Williamson, G & Cassidy, A (2003) Bioavailability of phyto-oestrogens. Br J Nutr 89, S45–S58.CrossRefGoogle ScholarPubMed
Setchell, KD, Brown, NM & Lydeking-Olsen, E (2002) The clinical importance of the metabolite equol – a clue to the effectiveness of soy and its isoflavones. J Nutr 132, 3577–3584.CrossRefGoogle Scholar
Setchell, KD & Cassidy, A (1999) Dietary isoflavones: biological effects and relevance to human health. J Nutr 129, 758S–767S.CrossRefGoogle ScholarPubMed
Setchell, KD & Lydeking-Olsen, E (2003) Dietary phytoestrogens and their effect on bone: evidence from in vitro and in vivo, human observational, and dietary intervention studies. Am J Clin Nutr 78, 593S–609S.CrossRefGoogle Scholar
Song, T, Lee, SO, Murphy, PA & Hendrich, S (2003) Soy protein with or without isoflavones, soy germ and soy germ extract, and daidzein lessen plasma cholesterol levels in golden Syrian hamsters. Exp Biol Med 228, 1063–1068.CrossRefGoogle ScholarPubMed
Steer, TE, Johnson, IT, Gee, JM & Gibson, GR (2003) Metabolism of the soybean isoflavone glycoside genistin in vitro by human gut bacteria and the effect of prebiotics. Br J Nutr 90, 635–642.CrossRefGoogle ScholarPubMed
Stone-Dorshow, T & Levitt, MD (1987) Gaseous response to ingestion of a poorly absorbed fructo-oligosaccharide sweetener. Am J Clin Nutr 46, 61–65.CrossRefGoogle ScholarPubMed
Suzuki, T, Hara, H, Kasai, T & Tomita, F (1998) Effects of difructose anhydride III on calcium absorption in small and large intestines of rats. Biosci Biotechnol Biochem 62, 837–841.CrossRefGoogle ScholarPubMed
Tamura, M, Hirayama, K, Itoh, K, Suzuki, H & Shinohara, K (2002) Effects of rice starch-isoflavone diet or potato starch-isoflavone diet on plasma isoflavone, plasma lipids, cecal enzyme activity, and composition of fecal microflora in adult mice. J Nutr Sci Vitaminol. 48, 225–229.CrossRefGoogle ScholarPubMed
Tamura, M, Ohnishi-Kameyama, M & Shinohara, K (2004a) Lactobacillus gasseri: effects on mouse intestinal flora enzyme activity and isoflavonoids in the caecum and plasma. Br J Nutr 92, 771–776.CrossRefGoogle ScholarPubMed
Tamura, A, Shiomi, T, Shigematsu, N, Tomita, F & Hara, H (2003) Evidence suggesting that difructose anhydride III is an indigestible and low fermentable sugar during the early stage after ingestion in humans. J Nutr Sci Vitaminol 49, 422–427.CrossRefGoogle ScholarPubMed
Tamura, A, Shiomi, T, Tamaki, N, Shigematsu, N, Tomita, F & Hara, H (2004b) Comparative effect of repeated ingestion of difructose anhydride III and palatinose on the induction of gastrointestinal symptoms in humans. Biosci Biotechnol Biochem 68, 1882–1887.CrossRefGoogle ScholarPubMed
Uehara, M, Ohta, A, Sakai, K, Suzuki, K, Watanabe, S & Adlercreutz, H (2001) Dietary fructooligosaccharides modify intestinal bioavailability of a single dose of genistein and daidzein and affect their urinary excretion and kinetics in blood of rats. J Nutr 131, 787–795.CrossRefGoogle ScholarPubMed
Ueno, T, Uchiyama, S & Kikuchi, N (2002) The role of intestinal bacteria on biological effects of soy isoflavones in humans. J Nutr 132, 594S.Google Scholar
Uesugi, T, Toda, T, Tsuji, K & Ishida, H (2001) Comparative study on reduction of bone loss and lipid metabolism abnormality in ovariectomized rats by soy isoflavones, daidzin, genistin, and glycitin. Biol Pharm Bull 24, 368–372.CrossRefGoogle ScholarPubMed
Wangen, KE, Duncan, AM, Xu, X & Kurzer, MS (2001) Soy isoflavones improve plasma lipids in normocholesterolemic and mildly hypercholesterolemic postmenopausal women. Am J Clin Nutr 73, 225–231.CrossRefGoogle ScholarPubMed
Yousef, MI, Kamel, KI, Esmail, AM & Baghdadi, HH (2004) Antioxidant activities and lipid lowering effects of isoflavone in male rabbits. Food Chem Toxicol 42, 1497–1503.CrossRefGoogle ScholarPubMed
Zafar, TA, Weaver, CM, Jones, K, Moore, DR 2nd & Barnes, S (2004) Inulin effects on bioavailability of soy isoflavones and their calcium absorption enhancing ability. J Agric Food Chem 52, 2827–2831.CrossRefGoogle ScholarPubMed