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Bioavailability of isoflavone phytoestrogens in postmenopausal women consuming soya milk fermented with probiotic bifidobacteria

Published online by Cambridge University Press:  08 March 2007

Dimitri Tsangalis
Affiliation:
Food Safety Authenticity and Quality Unit, Victoria University, Werribee Campus, Victoria, Australia
Gisela Wilcox*
Affiliation:
Clinical Nutrition and Metabolism Unit & Monash University, Department of Medicine, Monash Medical Centre,Clayton, Victoria, Australia
Nagendra P. Shah
Affiliation:
School of Molecular Sciences, Victoria University, Werribee Campus, Victoria, Australia
Lily Stojanovska
Affiliation:
School of Biomedical Sciences, Victoria University, St Albans Campus, Victoria, Australia
*
*Corresponding author: Dr Gisela Wilcox, fax +61 3 9594 6370, email [email protected]
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Abstract

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We investigated the effects of consuming an isoflavone aglycone-enriched soya milk containing viable bifidobacteria on urinary isoflavone excretion and percentage recovery. Sixteen postmenopausal women were randomly divided into two groups to consume either fermented or non-fermented soya milk. Each group participated in a double-blind, crossover study with three 14 d supplementation periods, separated by a 14 d washout. Subjects ingested three daily dosages of isoflavone via the soya milk and collected four 24 h pooled urine specimens per supplementation period. Soya milks were prepared with soya protein isolate and soya germ, followed by fermentation with bifidobacteria. Isoflavone levels were quantified using HPLC. Non-fermented soya milks at 20, 40 and 80 mg isoflavone/200 ml contained 10 %, 9 % and 7 % aglycone, respectively, with their fermented counterparts containing 69 %, 57 % and 36 % aglycone (P<0·001). A trend to a greater percentage urinary recovery of daidzein and glycitein was observed among women consuming fermented soya milk at a dosage of 40 mg isoflavone (P=0·13). A distinct linear dose response for the fermented soya milk group (R2=0·9993) compared with the non-fermented group (R2=0·8865) suggested less interindividual variation in isoflavone absorption. However, total urinary isoflavone excretion was similar for both groups (P>0·05), with urinary isoflavone recovery at approximately 31 %. Increasing the isoflavone dosage correlated positively with its urinary excretion, but urinary percentage recovery of isoflavone was inversely related to dosage level. Hence, a modest dosage ranging from 20 to 30 mg/d may provide the most bioavailable source of isoflavone, regardless of whether it is via an aglycone-rich fermented soya milk or a glucoside-rich soya milk.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2005

References

Albright, SC, Winston, WL & Zappe, C (1999) Data Analysis and Decision Making with Microsoft Excel. Pacific Grove, CA: Brooks/Cole Publishing Company.Google Scholar
Anderson, JW, Johnstone, BM & Cook-Newell, ME (1995) Meta-analysis of the effects of soy protein intake on serum lipids. N Eng J Med 333, 276282.CrossRefGoogle ScholarPubMed
Ballongue, J (1993) Bifidobacteria and probiotic action. In Lactic Acid Bacteria pp. 519587 [Salminen, S, von Wright, A] New York: Marcel Dekker.Google Scholar
Brzezinski, A & Debi, A (1999) Phytoestrogens: the "natural" selective estrogen receptor modulators? Eur J Obstet Gynaecol 85, 4751.CrossRefGoogle ScholarPubMed
Cassidy, A (1996) Physiological effects of phyto-oestrogens in relation to cancer and other human health risks. Proc Nutr Soc 55, 399417.CrossRefGoogle ScholarPubMed
Day, AJ, DuPont, MSRidley, S, Rhodes, M, Rhodes, MJ, Morgan, MR & Williamson, G (1998) Deglycosylation of flavonoid and isoflavonoid glycosides by human small intestine and liver beta-glucosidase activity. FEBS Lett 436, 7175.CrossRefGoogle ScholarPubMed
De Mann, JC, Rogosa, M & Sharpe, ME (1960) A medium for the cultivation of lactobacilli. J Appl Bacteriol 23, 130135.CrossRefGoogle Scholar
Franke, AA & Custer, LJ (1994) High-performance liquid chromatography assay of isoflavonoids and coumesterol from human urine. J Chromatog B 662, 4760.CrossRefGoogle Scholar
Gomes, AMP & Malcata, FX (1999) Bifidobacterium spp. and Lactobacillus acidophilus: biological, biochemical, technological and therapeutical properties relevant for use as probiotics. Trends Food Sci Technol 10, 139157.CrossRefGoogle Scholar
Heinonen, SM, Wähälä, K & Adlercreutz, H (2002) Metabolism of isoflavones in human subjects. Phytochem Rev 1, 175182.CrossRefGoogle Scholar
Hendrich, S (2002) Bioavailability of isoflavones. J Chromatog B 777, 203210.CrossRefGoogle ScholarPubMed
Hendrich, S, Hu, J, Zheng, YL, Lee, SO, Verbruggen, M & Murphy, PA (2001) Comparative bioavailability of isoflavone aglycone and glucosides in women. Fourth International Symposium on the Role of Soy in Preventing and Treating Chronic Disease. San Diego, CA, November 4–7.Google Scholar
Hou, JW, Yu, RC & Chou, CC (2000) Changes in some components of soya milk during fermentation with bifidobacteria. Food Res Int 33, 393397.CrossRefGoogle Scholar
Hutchins, AM, Slavin, JL & Lampe, JW (1995) Urinary isoflavonoid phytoestrogen and lignan excretion after consumption of fermented and unfermented soy products. J Amer Diet Assoc 95, 545551.CrossRefGoogle ScholarPubMed
Izumi, T, Piskula, MK, Osawa, S, Obata, A, Tobe, K, Saito, M, Kataoka, S, Kubota, Y & Kikuchi, M (2000) Soy isoflavone aglycones are absorbed faster and in higher amounts than their glucosides in humans. J Nutr 130, 16951699.CrossRefGoogle ScholarPubMed
Joannou, GE, Kelly, GE, Reeder, AY, Waring, M & Nelson, C (1995) A urinary profile study of dietary phytoestrogens. The identification and mode of metabolism of new isoflavonoids. J Steroid Biochem Mol Biol 54, 167185.CrossRefGoogle ScholarPubMed
Kamaly, KM (1997) Bifidobacteria fermentation of soybean milk. Food Res Int 30, 675682.CrossRefGoogle Scholar
Kelly, GE, Nelson, C, Waring, MA, Joannou, GE & Reeder, AY (1993) Metabolites of dietary (soya) isoflavones in human urine. Clin Chim Acta 223, 922.CrossRefGoogle ScholarPubMed
King, RA & Bignell, CM (2000) Concentrations of isoflavone phytoestrogens and their glucosides in Australian soya beans and soya foods. Aus J Nutr Diet 57, 7078.Google Scholar
King, RA & Bursill, DB (1998) Plasma and urinary kinetics of the isoflavones daidzein and genistein after a single soy meal in humans. Am J Clin Nutr 67, 867872.CrossRefGoogle ScholarPubMed
Kudou, S, Fleury, Y & Welti, D (1991) Malonyl isoflavone glycosides in soybean seeds (Glycine Max merrill). Agric Biol Chem 55, 22272233.Google Scholar
Kurzer, MS (2000) Hormonal effects of soy isoflavones: studies in premenopausal and postmenopausal women. J Nutr 130, 660S661S.CrossRefGoogle ScholarPubMed
Lampe, JW, Karr, SC, Hutchins, AM & Slavin, JL (1998) Urinary equol excretion with a soy challenge: influence of habitual diet. Proc Soc Exp Biol Med 217, 335339.CrossRefGoogle ScholarPubMed
Lee, HP, Gourley, L, Duffy, SW, Esteve, J, Lee, J & Day, NE (1991) Dietary effects on breast cancer risk in Singapore. Lancet 337, 11971200.CrossRefGoogle ScholarPubMed
Lu, L-JW & Anderson, KE (1998) Sex and long-term soy diets affect the metabolism and excretion of soy isoflavones in humans. Am J Clin Nutr 68, 1500S1504S.CrossRefGoogle Scholar
Lu, L-JW, Lin, SN, Grady, JJ, Nagamani, M & Anderson, KE (1996) Altered kinetics and extent of urinary daidzein and genistein excretion in women during chronic soya exposure. Nutr Cancer 26, 289302.CrossRefGoogle ScholarPubMed
Markiewicz, L, Garey, J, Adlercreutz, H & Gurpide, E (1993) In vitro bioassays of non-steroidal phytoesrogens. J Steroid Biochem Mol Biol 45, 399405.CrossRefGoogle Scholar
Masai, T, Wada, K, Hayakawa, K, Yoshihara, I & Mitsuoka, T (1987) Effects of soybean oligosaccharides on human intestinal flora and metabolic activities. Japan J Bacteriol 42, 313.Google Scholar
Mayr, U, Butsch, A & Schneider, S (1992) Validation of two in vitro test systems for estrogenic activities with zearalenone, phytoestrogens and cereal extracts. Toxicology 74, 135149.CrossRefGoogle ScholarPubMed
Mitsuoka, T (1984) Taxonomy and ecology of bifidobacteria. Bifidobacteria Microflora 1, 1128.CrossRefGoogle Scholar
Murphy, PA, Song, T, Buseman, G, Barua, K, Beecher, GR, Trainer, D & Holden, V (1999) Isoflavones in retail and institutional soy foods. J Agric Food Chem 47, 26972704.CrossRefGoogle ScholarPubMed
Orrhage, K & Nord, CE (2000) Bifidobacteria and lactobacilli in human health. Drugs Exp Clin Res 26, 95111.Google ScholarPubMed
Playne, MJ (2002) The health benefits of probiotics. Food Aust 54, 7174.Google Scholar
Richelle, M, Pridmore-Merten, S, Bodenstab, S, Enslen, M & Offord, EA (2002) Hydrolysis of isoflavone glycosides to aglycones by β-glycosidase does not alter plasma and urine isoflavone pharmacokinetics in postmenopausal women. J Nutr 132, 25872592.CrossRefGoogle Scholar
Rowland, IR, Wiseman, H, Sanders, TAB, Adlercreutz, H & Bowey, EA (2000) Interindividual variation in metabolism of soy isoflavones and lignans: influence of habitual diet on equol production by the gut microflora. Nutr Cancer 36, 2732.CrossRefGoogle ScholarPubMed
Setchell, KDR (1995) Non-steroidal estrogens of dietary origin: possible roles in health and disease, metabolism and physiological effects. Proc Nutr Soc NZ 20, 121.Google Scholar
Setchell, KDR & Cassidy, A (1999) Dietary isoflavones: biological effects and relevance to human health. J Nutr 129, 758S767S.CrossRefGoogle ScholarPubMed
Setchell, KDR, Borriello, SP, Hulme, P, Kirk, DN & Axelson, M (1984) Non-steroidal estrogens of dietary origin: possible roles in hormone-dependent disease. Am J Clin Nutr 40, 569578.CrossRefGoogle ScholarPubMed
Setchell, KDR, Brown, NM, Desai, PZimmer-Nechemias, LWolfe, BE, Brashear, WT, kirschner, AS, Cassidy, A & Heubi, VE (2001) Bioavailability of pure isoflavones in healthy humans and analysis of commercial soy isoflavone supplements. J Nutr 131, 1362S1375S.CrossRefGoogle ScholarPubMed
Setchell, KDR, Brown, NM, Zimmer-Nechemias, L, Brasheas, WT, Wolfe, BE, Krischner, AS & Heubi, JE (2002) Evidence for the lack of absorption of soy isoflavone glycosides in humans, supporting the crucial role of intestinal metabolism for bioavailability. Amer J Clin Nutr 76, 447453.CrossRefGoogle ScholarPubMed
Setchell, KDR, Maynard-Brown, N, Desai, PB, Zimmer-Nechemias, L, Wolfe, B, Jakate, AS, Creutzinger, V & Heubi, VE (2003) Bioavailability, disposition, and dose-response effects of soy isoflavones when consumed by healthy women at physiologically typical dietary intakes. J Nutr 133, 10271035.CrossRefGoogle ScholarPubMed
Slavin, JL, Karr, SC, Hutchins, AM & Lampe, JW (1998) Influence of soybean processing, habitual diet, and soy dose on urinary isoflavonoid excretion. Amer J Clin Nutr 68, 1492S1495S.CrossRefGoogle ScholarPubMed
Tsangalis, D & Shah, NP (2004) Metabolism of oligosaccharides and aldehydes and production of organic acids in soya milk by probiotic bifidobacteria. Int J Food Sci Technol 39, 541554.CrossRefGoogle Scholar
Tsangalis, D, Ashton, JF, McGill, AEJShah, NP (2002) Enzymic transformation of isoflavone phytoestrogens in soya milk by β-glucosidase-producing bifidobacteria. J Food Sci 67, 31043113.CrossRefGoogle Scholar
Tsangalis, D, Ashton, JFMcGill, AEJShah, NP (2003) Biotransformation of isoflavones by bifidobacteria in fermented soya milk supplemented with D-glucose and L-cysteine. J Food Sci 68, 623631.CrossRefGoogle Scholar
Tsangalis, D, Ashton, JF, Stojanovska, L, Wilcox, G & Shah, NP (2004) Development of an isoflavone aglycone enriched soya milk using soy germ, soy protein isolate and bifidobacteria. Food Res Int 37, 301312.CrossRefGoogle Scholar
Turner, NJ, Thomson, BM & Shaw, IC (2003) Bioactive isoflavones in functional foods: the importance of gut microflora on bioavailability. Nutr Rev 61, 204213.CrossRefGoogle ScholarPubMed
Xu, X, Harris, KS, Wang, H-J, Murphy, PA & Hendrich, S (1995) Bioavailability of soybean isoflavones depends upon gut microflora in women. J Nutr 125, 23072315.CrossRefGoogle ScholarPubMed
Xu, X, Wang, H-J, Murphy, PA, Cook, L & Hendrich, S (1994) Daidzein is a more bioavailable soya milk isoflavone than is genistein in adult women. J Nutr 124, 825832.CrossRefGoogle Scholar
Zhang, Y, Hendrich, S & Murphy, PA (2003) Glucuronides are the main isoflavone metabolites in women. J Nutr 133, 399404.CrossRefGoogle ScholarPubMed
Zhang, Y, Wang, G-J, Song, TT, Murphy, PA & Hendrich, S (2001) Urinary disposition of the soybean isoflavones daidzein, genistein and glycitein among humans with moderate fecal isoflavone degradation activity (erratum). J Nutr 131, 147148.Google Scholar