Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-18T10:23:02.765Z Has data issue: false hasContentIssue false
  • English
  • Français

Influence of soya-based infant formula consumption on isoflavone and gut microflora metabolite concentrations in urine and on faecal microflora composition and metabolic activity in infants and children

Published online by Cambridge University Press:  09 March 2007

Leane Hoey ,
Ian R. Rowland ,
Antony S. Lloyd ,
Don B. Clarke  and
Helen Wiseman
Leane Hoey
Affiliation:
Northern Ireland Centre for Food and Health, University of Ulster, Coleraine BT52 1SA, UK
Ian R. Rowland
Affiliation:
Northern Ireland Centre for Food and Health, University of Ulster, Coleraine BT52 1SA, UK
Antony S. Lloyd
Affiliation:
Central Science Laboratory (CSL), Department for Environment, Food and Rural Affairs (DEFRA), Sand Hutton, York Y041 1LZ, UK
Don B. Clarke
Affiliation:
Central Science Laboratory (CSL), Department for Environment, Food and Rural Affairs (DEFRA), Sand Hutton, York Y041 1LZ, UK
Helen Wiseman*
Affiliation:
Nutrition, Food and Health Research Centre, Department of Nutrition and Dietetics, King's College London, Franklin-Wilkins Building, 150 Stamford Street, London SE1 9NN, UK
*
*Corresponding author: Dr Helen Wiseman, fax +44 20 7848 4185, email Helen.Wiseman@kcl.ac.uk
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

The urinary excretion of soya isoflavones and gut microflora metabolites was investigated in infants and children who had been fed soya-based infant formulas in early infancy. These infants and children were compared with cows'-milk formula-fed controls, to determine at what age gut microflora metabolism of daidzein to equol and/or O-desmethylangolensin (O-DMA) was established, and whether exposure to isoflavones in early infancy influences their metabolism at a later stage of development. Sixty infants and children (aged 4 months–7 years) participated in the study; thirty in each of the soya and control groups. There were four age groups. These were: 4–6 months (seven in the soya group and seven in the control group); 7–12 months (seven in the soya group and nine in the control group); 1–3 years (six in the soya group and eight in the control group); 3–7 years (ten in the soya group and six in the control group). Urine samples were collected to measure isoflavonoids by MS, and faecal samples were collected to measure gut-health-related bacterial composition, by fluorescent in situ hybridisation with oligonucleotide probes, and metabolic activity. A soya challenge (typically a soya yoghurt alternative product containing 4·8g soya protein and on average 22mg total isoflavones) was given to control-group infants (>6 months) and children, and also to soya-group children that were no longer consuming soya, to determine their ability to produce equol and/or O-DMA. Urinary genistein, daidzein and glycitein were detected in all infants (4–6 months) fed soya-based infant formula; O-DMA was detected in 75% of infants but equol was detected in only 25%. In the controls (4–6 months), urinary isoflavonoids were very low or not detected. In the older age groups (7 months–7 years), O-DMA was found in the urine samples of 75% of the soya group and 50% of the controls, after the soya challenge. Equol excretion was detected in 19% of the soya-group infants and children, and in only 5% of the controls. However, in the oldest (3–7 years) children, the proportion excreting O-DMA and equol was similar in both groups. Faecal bacterial numbers for bifidobacteria (P<0·001), bacteroides and clostridia (P<0·05) were significantly lower for the soya group compared with the control group. There appears to be no lasting effect of early-life isoflavone exposure on isoflavone metabolism.

Keywords

Soya isoflavone metabolismEquolSoya-based infant formulaGut bacterial microflora
Type
Research Article
Information
British Journal of Nutrition , Volume 91 , Issue 4 , April 2004 , pp. 607 - 616
Copyright
Copyright © The Nutrition Society 2004

References

Adlercreutz, H (2002) Phyto-oestrogens and cancer. Lancet Oncol 3, 32–41.CrossRefGoogle ScholarPubMed
Adlercreutz, H, Fotsis, T, Bannwart, C, Wahala, K, Brunow, G & Hase, T (1991) Isotope dilution gas chromatographic-mass spectrometric method for the determination of lignans and isoflavonoids in human urine, including identification of genistein. Clinica Chimica Acta 119, 263–278.CrossRefGoogle Scholar
Arora, A, Nair, NG & Strasburg, GM (1998) Antioxidant activities of isoflavones and their biological metabolites in a liposomal system. Arch Biochem Biophys 356, 133–141.CrossRefGoogle Scholar
Badger, TM, Ronis, MJ, Hakkak, R, Rowlands, JC & Korourian, S (2002) The health consequences of early soya consumption. J Nutr 132, 559S–565S.Google Scholar
Barnes, S (2001) Oestrogens and their promiscuous receptors: confronting reality. Biochem Soc Trans 29, 231–236.Google Scholar
Committee on Toxicity of Chemicals in Food, Consumer Products and the Environment (1996) Levels of Plant Oestrogens in the Diets of Infants and Toddlers. London, UK: MAFF.Google Scholar
Committee on Toxicity of Chemicals in Food, Consumer Products and the Environment (1998) Levels of Plant Oestrogens in the Diets of Infants and Toddlers. London, UK: MAFF.Google Scholar
Coward, L, Barnes, NC, Setchell, KDR & Barnes, S (1993) Genistein, daidzein and their β-glycoside conjugates: antitumor isoflavones in soyabean foods from American and Asian diets. J Agric Food Chem 41, 1961–1967.CrossRefGoogle Scholar
Gangolli, SD & Rowland, IR (1999) Role of gastrointestinal flora in the metabolic and toxicological activities of xenobiotics. In General and Applied Toxicology, pp. 561–576 [Marrs, TC, Syverson, T and Ballantyne, B, editors]. London: Macmillan Publisher Ltd.Google Scholar
Gibson, GR & Roberfroid, MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125, 1401–1412.CrossRefGoogle ScholarPubMed
Harmsen, HJM, Gibson, GR, Elfferich, P, Raangs, GC, Wildeboer-Veloo, AC, Argaiz, A, Roberfroid, MB & Welling, GW (1999) Comparison of viable cell counts and fluorescence in situ hybridization using specific rRNA-based probes for the quantification of human fecal bacteria. FEMS Microbiol Lett 183, 125–129.Google Scholar
Heavey, P & Rowland, I (1999) The gut microflora of the developing infant: microbiology and metabolism. Microb Ecol Health Dis 11, 75–83.Google Scholar
Hodgson, JM, Croft, KD, Puddey, IB, Mori, TA & Beilin, LJ (1996) Soybean isoflavonoids and their metabolic products inhibit in vitro lipoprotein oxidation in serum. J Nutr Biochem 7, 664–669.CrossRefGoogle Scholar
Ingram, D, Sanders, K, Kolybaba, M & Lopez, D (1997) Case control study of phyto-estrogens and breast cancer. Lancet 350, 990–994.CrossRefGoogle ScholarPubMed
Irvine, CH, Shand, N, Fitzpatrick, MG & Alexander, SL (1998 a) Daily intake and urinary excretion of genistein and daidzein in infants fed soy- or dairy-based infant formulas. Am J Clin Nutr 68, 1462S–1465S.Google Scholar
Irvine, CHG, Fitzpatrick, MG & Setchell, KDR (1998 b) Phytoestrogens in soy-based infant foods: concentrations, daily intake and possible biological effects. Proc Soc Exp Biol Med 217, 247–253.Google Scholar
Jenkins, DJA, Kendall, CWC, Garsetti, M et al. , (2000) Effect of soy protein foods on low-density lipoprotein oxidation and ex vivo sex hormone activity – a controlled crossover trial. Metabolism 49, 537–543.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, 335–339.CrossRefGoogle ScholarPubMed
Lampe, JW, Skor, HE, Li, S, Wahala, K, Howald, WN & Chen, C (2001) Wheat bran and soy protein feeding do not alter urinary excretion of the isoflavone equol in premenopausal women. J Nutr 131, 740–744.CrossRefGoogle Scholar
Lepage, G & Roy, CC (1986) Direct transesterification of all classes of lipid in a one step reaction. J Lipid Res 27, 114–120.Google Scholar
Lu, LJ, Broemeling, LD, Marshall, MV & Ramanujam, VM (1995) A simplified method to quantify isoflavones in commercial soybean diets and human urine after legume consumption. Cancer Epidemiol Biomarkers Prev 4, 497–503.Google ScholarPubMed
Markiewicz, L, Garey, J, Adlercreutz, H & Gurpide, E (1993) In vitro bioassays of non-steroidal phytoestrogens. J Steroid Biochem 45, 399–405.Google Scholar
Mendez, MA, Anthony, MS & Arab, L (2002) Soy-based formulae and infant growth and development. J Nutr 132, 2127–2130.Google Scholar
Mitchell, JH, Gardner, PT, McPhail, DB, Morrice, PC, Collins, AR & Duthie, GG (1998) Antioxidant efficacy of phytoestrogens in chemical and biological model systems. Arch Biochem Biophys 360, 142–148.CrossRefGoogle ScholarPubMed
Morton, MS, Wilcox, G, Wahlqvist, M & Griffiths, K (1994) Determination of lignans and isoflavonoids in human female plasma following dietary supplementation. J Endocrinol 142, 251–259.Google Scholar
Murphy, PA, Song, T, Buseman, G & Barua, K (1997) Isoflavones in soy-based infant formulas. J Agric Food Chem 45, 4635–4638.CrossRefGoogle Scholar
Rowland, I, Faughnan, M, Hoey, L, Wahala, K, Williamson, G & Cassidy, A (2003) Bioavailability of phyto-oestrogens. Br J Nutr 89, Suppl., S45–S58.Google Scholar
Rowland, IR (1992) Metabolic interaction in the gut. In Probiotics: the Scientific Basis, pp. 29–53 [Fuller, R, edotor]. London: Chapman and Hall.CrossRefGoogle Scholar
Rowland, IR, Mallett, AK & Wise, A (1985) The effect of diet on the mammalian gut flora and its metabolic activities. Crit Rev Toxicol 16, 31–103.Google Scholar
Rowland, IR, Wiseman, H, Sanders, TAB, Adlercreuz, 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, 27–32.CrossRefGoogle ScholarPubMed
Setchell, KDR, Brown, NM, Desai, PB, Zimmer-Nechemias, L, Wolfe, B, Jakate, AS, Creutzinger, V & Heubi, JE (2003 a) Bioavailability, disposition and dose-response effects of soy isoflavones when consumed by healthy women at physiologically typical dietary intakes. J Nutr 133, 1027–1035.Google Scholar
Setchell, KDR, Brown, NM & Lydeking-Olsen, E (2002 a) The clinical importance of the metabolite equol - a clue to the effectiveness of soy and its isoflavones. J Nutr 132, 3577–3584.Google Scholar
Setchell, KDR, Brown, NM, Zimmer-Nechemias, L, Brashear, WT, Wolfe, BE, Kirschner, AS & Heubi, JE (2002 b) Evidence for lack of absorption of soy isoflavone glycosides in humans, supporting the crucial role of intestinal metabolism for bioavailability. Am J Clin Nutr 76, 447–453.CrossRefGoogle ScholarPubMed
Setchell, KDR & Cassidy, A (1999) Dietary isoflavones: biological effects and relevance to human health. J Nutr 129, 758S–767S.CrossRefGoogle ScholarPubMed
Setchell, KDR, Faughnan, MS, Avades, T et al. , (2003 b) Comparing the pharmacokinetics of daidzein and genistein with the use of 13C-labeled tracers in premenopausal women. Am J Clin Nutr 77, 411–419.CrossRefGoogle ScholarPubMed
Setchell, KDR, Nechemias, L, Cai, J & Heubi, JE (1997) Exposure of infants to phytoestrogens from soy-based infant formula. Lancet 350, 23–27.Google Scholar
Setchell, KDR, Zimmer-Nechemias, L, Cai, J & Heubi, JE (1998) Isoflavone content of infant formulas and the metabolic fate of these phytoestrogens in early life. Am J Clin Nutr 68, 1453S–1461S.Google Scholar
Solorzano, L (1969) Determination of ammonia in natural waters by the phenol-hypochlorite method. Limnol Oceanogr 14, 799–801.Google Scholar
Tikkanen, MJ, Wahala, K, Ojala, S, Vihma, V & Adlercreutz, H (1998) Effect of soybean intake on low density lipoprotein (LDL) oxidation resistance. Proc Natl Acad Sci USA 95, 3106–3110.Google Scholar
Visek, WJ (1978) Diet and cell growth modulation by ammonia. Am J Clin Nutr 31, S216–S220.Google Scholar
Wang, HJ & Murphy, PA (1994) Isoflavone content in commercial soybean foods. J Agric Food Chem 42, 1666–1673.CrossRefGoogle Scholar
Watanabe, S, Yamaguchi, M, Sobue, T, Takahashi, T, Miura, T, Arai, Y, Mazur, W, Wahala, K & Adlercreutz, H (1998) Pharmacokinetics of soyabean isoflavones in plasma, urine and feces of men after ingestion of 60g baked soybean powder (kinako). J Nutr 128, 1710–1715.Google Scholar
Wise, A, Mallet, AK & Rowland, IR (1982) Dietary fibre, bacterial metabolism and toxicity of nitrate in rat. Xenobiotica 12, 111–118.Google Scholar
Wiseman, H (2000) The therapeutic potential of phytoestrogens. Expert Opin Investig Drugs 9, 1829–1840.Google Scholar
Wiseman, H, Casey, K, Clarke, DB, Barnes, KA & Bowey, E (2002) Isoflavone aglycon and glucoconjugate content of high- and low-soy U.K. foods used in nutritional studies. J Agric Food Chem 50, 1404–1410.Google Scholar
Wiseman, H, O'Reilly, JD, Adlercreutz, H, Mallet, AI, Bowey, EA, Rowland, IR & Sanders, TA (2000) Isoflavone phytoestrogens consumed in soy decrease F 2 -isoprostane concentrations and increase resistance of low-density lipoprotein to oxidation in humans. Am J Clin Nutr 72, 395–400.CrossRefGoogle ScholarPubMed