DOI QR코드

DOI QR Code

Fermented soybeans by Rhizopus oligosporus reduce femoral bone loss in ovariectomized rats

  • 투고 : 2014.01.16
  • 심사 : 2014.02.19
  • 발행 : 2014.10.01

초록

BACKGROUND/OBJECTIVES: Soy isoflavones are structurally similar to estrogen and bind to estrogen receptors, suggesting that they exhibit estrogenic activities; therefore, they are referred to as phytoestrogens. Fermentation may affect the bioavailability of isoflavones altering soy isoflavone glycosides in the form of aglycones. Thus, this study investigated the effects of fermented soybeans by Rhizopus oligosporus on bone metabolism in both young rats as a pilot test and in ovariectomized (ovx) old rats as a model of menopause. MATERIALS/METHODS: In the pilot test, a total of 24 seven-week-old female Sprague-Dawley (SD) rats were fed one of three diets for a period of four weeks: casein, unfermented soybean product, or fermented soybean product by R. oligosporus. In the ovx rat model, 20-week-old SD rats weighing 260-290 g underwent either sham-operation (n = 10) or bilateral ovariectomy (n = 30) and were then fed the AIN-93M diet for one week. Thereafter, rats were fed sham-casein, ovx-casein, ovx-soybean, or ovx-fermented soybean diet for five weeks. After decapitation, femoral bones were isolated and preserved in 9% formalin for assessment of bone mineral density (BMD), bone mineral content (BMC), and bone-breaking strength (BBS). RESULTS: Ovx rats showed significantly increased weight gain and decreased uterine wet weight. Of particular interest, ovx rats fed fermented soybeans showed increased uterine wet weights compared to control rats. Fermented soybean diet caused a significant increase in plasma 17-${\beta}$ estradiol concentrations in young rats, and 17-${\beta}$ estradiol levels were enhanced in ovx rats to match those of sham-operated ones. Significantly lower femoral BMD and BMC were observed in ovx rats compared to sham-operated controls, whereas bone areas did not differ statistically among the groups. In addition, BBS tended to be increased in ovx rats fed soybeans and fermented soybeans. CONCLUSIONS: Supplementation of fermented soybeans could have preventive and therapeutic effects against osteoporosis in postmenopausal women.

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참고문헌

  1. Maskarinec G, Singh S, Meng L, Franke AA. Dietary soy intake and urinary isoflavone excretion among women from a multiethnic population. Cancer Epidemiol Biomarkers Prev 1998;7:613-9.
  2. Taku K, Umegaki K, Sato Y, Taki Y, Endoh K, Watanabe S. Soy isoflavones lower serum total and LDL cholesterol in humans: a meta-analysis of 11 randomized controlled trials. Am J Clin Nutr 2007;85:1148-56. https://doi.org/10.1093/ajcn/85.4.1148
  3. Sehmisch S, Uffenorde J, Maehlmeyer S, Tezval M, Jarry H, Stuermer KM, Stuermer EK. Evaluation of bone quality and quantity in osteoporotic mice--the effects of genistein and equol. Phytomedicine 2010;17:424-30. https://doi.org/10.1016/j.phymed.2009.10.004
  4. Choi JS, Kwon TW, Kim JS. Isoflavone contents in some varieties of soybean. Food Sci Biotechnol 1996;5:167-9.
  5. Izumi T, Piskula MK, Osawa S, Obata A, Tobe K, Saito M, Kataoka S, Kubota Y, Kikuchi M. Soy isoflavone aglycones are absorbed faster and in higher amounts than their glucosides in humans. J Nutr 2000;130:1695-9. https://doi.org/10.1093/jn/130.7.1695
  6. Hutchins AM, Slavin JL, Lampe JW. Urinary isoflavonoid phytoestrogen and lignan excretion after consumption of fermented and unfermented soy products. J Am Diet Assoc 1995;95:545-51. https://doi.org/10.1016/S0002-8223(95)00149-2
  7. Wang HJ, Murphy PA. Mass balance study of isoflavones during soybean processing. J Agric Food Chem 1996;44:2377-83. https://doi.org/10.1021/jf950535p
  8. Nout MJ, Rombouts FM. Recent developments in tempeh research. J Appl Bacteriol 1990;69:609-33. https://doi.org/10.1111/j.1365-2672.1990.tb01555.x
  9. Setchell KD, Clerici C, Lephart ED, Cole SJ, Heenan C, Castellani D, Wolfe BE, Nechemias-Zimmer L, Brown NM, Lund TD, Handa RJ, Heubi JE. S-equol, a potent ligand for estrogen receptor beta, is the exclusive enantiomeric form of the soy isoflavone metabolite produced by human intestinal bacterial flora. Am J Clin Nutr 2005;81:1072-9. https://doi.org/10.1093/ajcn/81.5.1072
  10. Adlercreutz H, Hamalainen E, Gorbach S, Goldin B. Dietary phytooestrogens and the menopause in Japan. Lancet 1992;339:1233. https://doi.org/10.1016/0140-6736(92)91174-7
  11. Ingram D, Sanders K, Kolybaba M, Lopez D. Case-control study of phyto-oestrogens and breast cancer. Lancet 1997;350:990-4. https://doi.org/10.1016/S0140-6736(97)01339-1
  12. Anderson JJ, Garner SC. The effects of phytoestrogens on bone. Nutr Res 1997;17:1617-32. https://doi.org/10.1016/S0271-5317(97)00156-5
  13. Setchell KD, Cassidy A. Dietary isoflavones: biological effects and relevance to human health. J Nutr 1999;129:758S-767S. https://doi.org/10.1093/jn/129.3.758S
  14. Kuiper GG, Lemmen JG, Carlsson B, Corton JC, Safe SH, van der Saag PT, van der Burg B, Gustafsson JA. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 1998;139:4252-63. https://doi.org/10.1210/endo.139.10.6216
  15. Gil-Izquierdo A, Penalvo JL, Gil JI, Medina S, Horcajada MN, Lafay S, Silberberg M, Llorach R, Zafrilla P, Garcia-Mora P, Ferreres F. Soy isoflavones and cardiovascular disease epidemiological, clinical and -omics perspectives. Curr Pharm Biotechnol 2012;13:624-31. https://doi.org/10.2174/138920112799857585
  16. Atkinson C, Compston JE, Day NE, Dowsett M, Bingham SA. The effects of phytoestrogen isoflavones on bone density in women: a double-blind, randomized, placebo-controlled trial. Am J Clin Nutr 2004;79:326-33. https://doi.org/10.1093/ajcn/79.2.326
  17. Arjmandi BH, Alekel L, Hollis BW, Amin D, Stacewicz-Sapuntzakis M, Guo P, Kukreja SC. Dietary soybean protein prevents bone loss in an ovariectomized rat model of osteoporosis. J Nutr 1996; 126:161-7. https://doi.org/10.1093/jn/126.1.161
  18. Harrison E, Adjei A, Ameho C, Yamamoto S, Kono S. The effect of soybean protein on bone loss in a rat model of postmenopausal osteoporosis. J Nutr Sci Vitaminol (Tokyo) 1998;44:257-68. https://doi.org/10.3177/jnsv.44.257
  19. Arjmandi BH, Getlinger MJ, Goyal NV, Alekel L, Hasler CM, Juma S, Drum ML, Hollis BW, Kukreja SC. Role of soy protein with normal or reduced isoflavone content in reversing bone loss induced by ovarian hormone deficiency in rats. Am J Clin Nutr 1998;68: 1358S-1363S. https://doi.org/10.1093/ajcn/68.6.1358S
  20. Nagata C, Shimizu H, Takami R, Hayashi M, Takeda N, Yasuda K. Soy product intake and serum isoflavonoid and estradiol concentrations in relation to bone mineral density in postmenopausal Japanese women. Osteoporos Int 2002;13:200-4. https://doi.org/10.1007/s001980200014
  21. Mei J, Yeung SS, Kung AW. High dietary phytoestrogen intake is associated with higher bone mineral density in postmenopausal but not premenopausal women. J Clin Endocrinol Metab 2001; 86:5217-21. https://doi.org/10.1210/jcem.86.11.8040
  22. Horiuchi T, Onouchi T, Takahashi M, Ito H, Orimo H. Effect of soy protein on bone metabolism in postmenopausal Japanese women. Osteoporos Int 2000;11:721-4. https://doi.org/10.1007/s001980070072
  23. Ho SC, Chan SG, Yi Q, Wong E, Leung PC. Soy intake and the maintenance of peak bone mass in Hong Kong Chinese women. J Bone Miner Res 2001;16:1363-9. https://doi.org/10.1359/jbmr.2001.16.7.1363
  24. Somekawa Y, Chiguchi M, Ishibashi T, Aso T. Soy intake related to menopausal symptoms, serum lipids, and bone mineral density in postmenopausal Japanese women. Obstet Gynecol 2001;97:109-15. https://doi.org/10.1016/S0029-7844(00)01080-2
  25. Potter SM, Baum JA, Teng H, Stillman RJ, Shay NF, Erdman JW Jr. Soy protein and isoflavones: their effects on blood lipids and bone density in postmenopausal women. Am J Clin Nutr 1998;68: 1375S-1379S. https://doi.org/10.1093/ajcn/68.6.1375S
  26. Devareddy L, Khalil DA, Smith BJ, Lucas EA, Soung do Y, Marlow DD, Arjmandi BH. Soy moderately improves microstructural properties without affecting bone mass in an ovariectomized rat model of osteoporosis. Bone 2006;38:686-93. https://doi.org/10.1016/j.bone.2005.10.024
  27. Zhao Q, Liu X, Zhang L, Shen X, Qi J, Wang J, Qian N, Deng L. Bone selective protective effect of a novel bone-seeking estrogen on trabecular bone in ovariectomized rats. Calcif Tissue Int 2013;93:172-83. https://doi.org/10.1007/s00223-013-9739-1
  28. Cho SH, Choi SW, Choi YS, Kim HJ, Park YH, Bae YC, Lee WJ. Effect of ethanol extract of safflower seed on bone loss in ovariectomized rat. Food Sci Biotechnol 2007;16:392-7.
  29. Deurveilher S, Seary ME, Semba K. Ovarian hormones promote recovery from sleep deprivation by increasing sleep intensity in middle-aged ovariectomized rats. Horm Behav 2013;63:566-76. https://doi.org/10.1016/j.yhbeh.2013.02.011
  30. Ferretti M, Bertoni L, Cavani F, Benincasa M, Sena P, Carnevale G, Zavatti M, Viesti VD, Zanoli P, Palumbo C. Structural and histomorphometric evaluations of ferutinin effects on the uterus of ovariectomized rats during osteoporosis treatment. Life Sci 2012; 90:161-8. https://doi.org/10.1016/j.lfs.2011.11.001
  31. Ferretti M, Bertoni L, Cavani F, Zavatti M, Resca E, Carnevale G, Benelli A, Zanoli P, Palumbo C. Influence of ferutinin on bone metabolism in ovariectomized rats. II: role in recovering osteoporosis. J Anat 2010;217:48-56. https://doi.org/10.1111/j.1469-7580.2010.01242.x
  32. Hertrampf T, Schleipen B, Offermanns C, Velders M, Laudenbach U, Diel P. Comparison of the bone protective effects of an isoflavone-rich diet with dietary and subcutaneous administrations of genistein in ovariectomized rats. Toxicol Lett 2009;184:198-203. https://doi.org/10.1016/j.toxlet.2008.11.006

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