About this Journal Submit a Manuscript Table of Contents
Evidence-Based Complementary and Alternative Medicine
Volume 2012 (2012), Article ID 921684, 11 pages
http://dx.doi.org/10.1155/2012/921684
Research Article

Effects of Extracts from Trifolium medium L. and Trifolium pratense L. on Development of Estrogen Deficiency-Induced Osteoporosis in Rats

1Department of Pharmacology, Medical University of Silesia, Katowice, Jagiellońska 4, 41-200 Sosnowiec, Poland
2Department of Pharmacognosy with Medicinal Plant Unit, Medical University of Lublin, Chodźki 1, 20-093 Lublin, Poland

Received 13 July 2012; Revised 28 September 2012; Accepted 28 September 2012

Academic Editor: HuanBiao Mo

Copyright © 2012 Urszula Cegieła et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. V. S. Lagari and S. Levis, “Phytoestrogens and bone health,” Current Opinion in Endocrinology, Diabetes and Obesity, vol. 17, no. 6, pp. 546–553, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. T. Oseni, R. Patel, J. Pyle, and V. C. Jordan, “Selective estrogen receptor modulators and phytoestrogens,” Planta Medica, vol. 74, no. 13, pp. 1656–1665, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. G. Zgórka, “Studies on phytoestrogenic and nonphytoestrogenic compounds in Trifolium incarnatum L. and other clover species using pressurized liquid extraction and high performance column liquid chromatography with photodiode-array and fluorescence detection,” Journal of AOAC International, vol. 94, no. 1, pp. 22–31, 2011. View at Scopus
  4. T. Sabudak and N. Guler, “Trifolium L.—a review on its phytochemical and pharmacological profile,” Phytotherapy Research, vol. 23, no. 3, pp. 439–446, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. J. T. Coon, M. H. Pittler, and E. Ernst, “Trifolium pratense isoflavones in the treatment of menopausal hot flushes: a systematic review and meta-analysis,” Phytomedicine, vol. 14, no. 2-3, pp. 153–159, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. S. E. Geller, L. P. Shulman, R. B. van Breemen et al., “Safety and efficacy of black cohosh and red clover for the management of vasomotor symptoms: a randomized controlled trial,” Menopause, vol. 16, no. 6, pp. 1156–1166, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. C. del Giorno, A. M. da Fonseca, V. R. Bagnoli, J. S. de Assis, J. M. Soares Jr., and E. C. Baracat, “Effects of Trifolium pratense on the climacteric and sexual symptoms in postmenopausal women,” Revista da Associação Médica Brasileira, vol. 56, no. 5, pp. 558–562, 2010. View at Scopus
  8. M. Lipovac, P. Chedraui, C. Gruenhut et al., “The effect of red clover isoflavone supplementation over vasomotor and menopausal symptoms in postmenopausal women,” Gynecological Endocrinology, vol. 28, no. 3, pp. 203–207, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. N. Panay, “Taking an integrated approach: managing women with phytoestrogens,” Climacteric, vol. 14, supplement 2, pp. 2–7, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. T. M. Knudson Schult, K. E. Ensrud, T. Blackwell, B. Ettinger, R. Wallace, and J. A. Tice, “Effect of isoflavones on lipids and bone turnover markers in menopausal women,” Maturitas, vol. 48, no. 3, pp. 209–218, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. C. M. Weaver, B. R. Martin, G. S. Jackson et al., “Antiresorptive effects of phytoestrogen supplements compared with estradiol or risedronate in postmenopausal women using 41Ca methodology,” The Journal of Clinical Endocrinology and Metabolism, vol. 94, no. 10, pp. 3798–3805, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. P. B. Clifton-Bligh, R. J. Baber, G. R. Fulcher, M. L. Nery, and T. Moreton, “The effect of isoflavones extracted from red clover (Rimostil) on lipid and bone metabolism,” Menopause, vol. 8, no. 4, pp. 259–265, 2001. View at Scopus
  13. C. Atkinson, J. E. Compston, N. E. Day, M. Dowsett, and S. A. Bingham, “The effects of phytoestrogen isoflavones on bone density in women: a double-blind, randomized, placebo-controlled trial,” The American Journal of Clinical Nutrition, vol. 79, no. 2, pp. 326–333, 2004. View at Scopus
  14. F. Occhiuto, R. De Pasquale, G. Guglielmo et al., “Effects of phytoestrogenic isoflavones from red clover (Trifolium pratense L.) on experimental osteoporosis,” Phytotherapy Research, vol. 21, no. 2, pp. 130–134, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. P. G. Adaikan, B. Srilatha, and A. J. Wheat, “Efficacy of red clover isoflavones in the menopausal rabbit model,” Fertility and Sterility, vol. 92, no. 6, pp. 2008–2013, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Kawakita, F. Marotta, Y. Naito et al., “Effect of an isoflavones-containing red clover preparation and alkaline supplementation on bone metabolism in ovariectomized rats,” Clinical Interventions in Aging, vol. 4, no. 1, pp. 91–100, 2009. View at Scopus
  17. G. Zgórka, “Pressurized liquid extraction versus other extraction techniques in micropreparative isolation of pharmacologically active isoflavones from Trifolium L. species,” Talanta, vol. 79, no. 1, pp. 46–53, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. F. A. Bisby, J. L. Zarucchi, B. D. Schrire, Y. R. Roskov, and R. J. White, Eds., ILDIS World Database of Legumes, 5th edition, 2000, LegumeWeb service, http://www.ildis.org.
  19. L. Zoric, L. Merkulov, J. Lukovic, and P. Boza, “Comparative analysis of qualitative anatomical characters of Trifolium L. (Fabaceae) and their taxonomic implications: preliminary results,” Plant Systematics and Evolution, vol. 298, no. 1, pp. 205–219, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. C. H. Turner and D. B. Burr, “Basic biomechanical measurements of bone: a tutorial,” Bone, vol. 14, no. 4, pp. 595–608, 1993. View at Publisher · View at Google Scholar · View at Scopus
  21. E. K. Stürmer, D. Seidlová-Wuttke, S. Sehmisch et al., “Standardized bending and breaking test for the normal and osteoporotic metaphyseal tibias of the rat: effect of estradiol, testosterone, and raloxifene,” Journal of Bone and Mineral Research, vol. 21, no. 1, pp. 89–96, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. J. Folwarczna, B. Nowińska, L. Śliwiński, M. Pytlik, U. Cegieła, and A. Betka, “Fenoterol did not enhance glucocorticoid-induced skeletal changes in male rats,” Acta Biochimica Polonica, vol. 58, no. 3, pp. 313–319, 2011. View at Scopus
  23. G. M. Kiebzak, R. Smith, C. C. Gundberg, J. C. Howe, and B. Sacktor, “Bone status of senescent male rats: chemical, morphometric, and mechanical analysis,” Journal of Bone and Mineral Research, vol. 3, no. 1, pp. 37–45, 1988. View at Scopus
  24. M. Pytlik, J. Folwarczna, and W. Janiec, “Effects of doxycycline on mechanical properties of bones in rats with ovariectomy-induced osteopenia,” Calcified Tissue International, vol. 75, no. 3, pp. 225–230, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. U. Cegieła, M. Pytlik, and W. Janiec, “Effects of α-escin on histomorphometrical parameters of long bones in rats with experimental post-steroid osteopenia,” Polish Journal of Pharmacology, vol. 52, no. 1, pp. 33–37, 2000. View at Scopus
  26. J. Folwarczna, L. Śliwiński, U. Cegieła et al., “Raloxifene similarly affects the skeletal system of male and ovariectomized female rats,” Pharmacological Reports, vol. 59, no. 3, pp. 349–358, 2007. View at Scopus
  27. A. Pfitscher, E. Reiter, and A. Jungbauer, “Receptor binding and transactivation activities of red clover isoflavones and their metabolites,” Journal of Steroid Biochemistry and Molecular Biology, vol. 112, no. 1–3, pp. 87–94, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. D. F. Ma, L. Q. Qin, P. Y. Wang, and R. Katoh, “Soy isoflavone intake increases bone mineral density in the spine of menopausal women: meta-analysis of randomized controlled trials,” Clinical Nutrition, vol. 27, no. 1, pp. 57–64, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. D. F. Ma, L. Q. Qin, P. Y. Wang, and R. Katoh, “Soy isoflavone intake inhibits bone resorption and stimulates bone formation in menopausal women: meta-analysis of randomized controlled trials,” European Journal of Clinical Nutrition, vol. 62, no. 2, pp. 155–161, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. J. Liu, S. C. Ho, Y. X. Su, W. Q. Chen, C. X. Zhang, and Y. M. Chen, “Effect of long-term intervention of soy isoflavones on bone mineral density in women: a meta-analysis of randomized controlled trials,” Bone, vol. 44, no. 5, pp. 948–953, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. E. Ricci, S. Cipriani, F. Chiaffarino, M. Malvezzi, and F. Parazzini, “Soy isoflavones and bone mineral density in perimenopausal and postmenopausal western women: a systematic review and meta-analysis of randomized controlled trials,” Journal of Women's Health, vol. 19, no. 9, pp. 1609–1617, 2010. View at Publisher · View at Google Scholar · View at Scopus
  32. K. Taku, M. K. Melby, N. Nishi, T. Omori, and M. S. Kurzer, “Soy isoflavones for osteoporosis: an evidence-based approach,” Maturitas, vol. 70, no. 4, pp. 333–338, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. G. G. C. Kuhnle, H. A. Ward, A. Vogiatzoglou et al., “Association between dietary phyto-oestrogens and bone density in men and postmenopausal women,” The British Journal of Nutrition, vol. 106, no. 7, pp. 1063–1069, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. C. Castelo-Branco and M. J. Cancelo Hidalgo, “Isoflavones: effects on bone health,” Climacteric, vol. 14, no. 2, pp. 204–211, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. D. Somjen, S. Katzburg, F. Kohen, B. Gayer, and E. Livne, “Daidzein but not other phytoestrogens preserves bone architecture in ovariectomized female rats in vivo,” Journal of Cellular Biochemistry, vol. 103, no. 6, pp. 1826–1832, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. A. K. Gautam, B. Bhargavan, A. M. Tyagi et al., “Differential effects of formononetin and cladrin on osteoblast function, peak bone mass achievement and bioavailability in rats,” The Journal of Nutritional Biochemistry, vol. 22, no. 4, pp. 318–327, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. H. Ha, H. Y. Lee, J. H. Lee et al., “Formononetin prevents ovariectomy-induced bone loss in rats,” Archives of Pharmacal Research, vol. 33, no. 4, pp. 625–632, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. J. J. B. Anderson, W. W. Ambrose, and S. C. Garner, “Biphasic effects of genistein on bone tissue in the ovariectomized, lactating rat model,” Proceedings of the Society for Experimental Biology and Medicine, vol. 217, no. 3, pp. 345–350, 1998. View at Scopus
  39. P. Fanti, M. C. Monier-Faugere, Z. Geng et al., “The phytoestrogen genistein reduces bone loss in short-term ovariectomized rats,” Osteoporosis International, vol. 8, no. 3, pp. 274–281, 1998. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Bitto, B. P. Burnett, F. Polito et al., “Effects of genistein aglycone in osteoporotic, ovariectomized rats: a comparison with alendronate, raloxifene and oestradiol,” British Journal of Pharmacology, vol. 155, no. 6, pp. 896–905, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. L. Śliwiński, J. Folwarczna, B. Nowińska et al., “A comparative study of the effects of genistein, estradiol and raloxifene on the murine skeletal system,” Acta Biochimica Polonica, vol. 56, no. 2, pp. 261–270, 2009. View at Scopus
  42. A. Bitto, H. Marini, B. P. Burnett et al., “Genistein aglycone effect on bone loss is not enhanced by supplemental calcium and vitamin D3: a dose ranging experimental study,” Phytomedicine, vol. 18, no. 10, pp. 879–886, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. M. Tezval, S. Sehmisch, D. Seidlová-Wuttke et al., “Changes in the histomorphometric and biomechanical properties of the proximal femur of ovariectomized rat after treatment with the phytoestrogens genistein and equol,” Planta Medica, vol. 76, no. 3, pp. 235–240, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Sehmisch, M. Erren, L. Kolios et al., “Effects of isoflavones equol and genistein on bone quality in a rat osteopenia model,” Phytotherapy Research, vol. 24, supplement 2, pp. S168–S174, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Sehmisch, J. Uffenorde, S. Maehlmeyer et al., “Evaluation of bone quality and quantity in osteoporotic mice—the effects of genistein and equol,” Phytomedicine, vol. 17, no. 6, pp. 424–430, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Mathey, J. Mardon, N. Fokialakis et al., “Modulation of soy isoflavones bioavailability and subsequent effects on bone health in ovariectomized rats: the case for equol,” Osteoporosis International, vol. 18, no. 5, pp. 671–679, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. J. Folwarczna, M. Zych, J. Burczyk, H. Trzeciak, and H. I. Trzeciak, “Effects of natural phenolic acids on the skeletal system of ovariectomized rats,” Planta Medica, vol. 75, no. 15, pp. 1567–1572, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Folwarczna, M. Zych, and H. I. Trzeciak, “Effects of curcumin on the skeletal system in rats,” Pharmacological Reports, vol. 62, no. 5, pp. 900–909, 2010. View at Scopus
  49. K. D. R. Setchell, N. M. Brown, and E. Lydeking-Olsen, “The clinical importance of the metabolite equol—a clue to the effectiveness of soy and its isoflavones,” The Journal of Nutrition, vol. 132, no. 12, pp. 3577–3584, 2002. View at Scopus
  50. J. P. Yuan, J. H. Wang, and X. Liu, “Metabolism of dietary soy isoflavones to equol by human intestinal microflora—implications for health,” Molecular Nutrition and Food Research, vol. 51, no. 7, pp. 765–781, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. K. M. Shedd-Wise, D. L. Alekel, H. Hofmann et al., “The soy isoflavones for reducing bone loss study: 3-Yr effects on pQCT bone mineral density and strength measures in postmenopausal women,” Journal of Clinical Densitometry, vol. 14, no. 1, pp. 47–57, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Yamaguchi, Y. L. Lai, S. Uchiyama, and T. Nakagawa, “Oral administration of phytocomponent p-hydroxycinnamic acid prevents bone loss in ovariectomized rats,” Molecular and Cellular Biochemistry, vol. 311, no. 1-2, pp. 31–36, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Folwarczna, M. Pytlik, M. Zych et al., “Effects of caffeic and chlorogenic acids on bone mechanical properties in female rats,” Bone, vol. 50, supplement 1, p. S158, 2012.
  54. S. C. Manolagas, “From estrogen-centric to aging and oxidative stress: a revised perspective of the pathogenesis of osteoporosis,” Endocrine Reviews, vol. 31, no. 3, pp. 266–300, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. V. Coxam, “Current data with inulin-type fructans and calcium, targeting bone health in adults,” The Journal of Nutrition, vol. 137, supplement 11, pp. 2527S–2533S, 2007. View at Scopus
  56. S. Takahara, T. Morohashi, T. Sano, A. Ohta, S. Yamada, and R. Sasa, “Fructooligosaccharide consumption enhances femoral bone volume and mineral concentrations in rats,” The Journal of Nutrition, vol. 130, no. 7, pp. 1792–1795, 2000. View at Scopus
  57. S. Pelletier, G. F. Tremblay, G. Bélanger et al., “Forage nonstructural carbohydrates and nutritive value as affected by time of cutting and species,” Agronomy Journal, vol. 102, no. 5, pp. 1388–1398, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. W. S. Branham, S. L. Dial, C. L. Moland et al., “Phytoestrogens and mycoestrogens bind to the rat uterine estrogen receptor,” The Journal of Nutrition, vol. 132, no. 4, pp. 658–664, 2002. View at Scopus
  59. J. E. Burdette, J. Liu, D. Lantvit et al., “Trifolium pratense (red clover) exhibits estrogenic effects in vivo in ovariectomized Sprague-Dawley rats,” The Journal of Nutrition, vol. 132, no. 1, pp. 27–30, 2002. View at Scopus
  60. D. Shor, T. Sathyapalan, S. L. Atkin, and N. J. Thatcher, “Does equol production determine soy endocrine effects?” European Journal of Nutrition, vol. 51, no. 4, pp. 389–398, 2012. View at Publisher · View at Google Scholar · View at Scopus
  61. L. Gu, S. E. House, R. L. Prior et al., “Metabolic phenotype of isoflavones differ among female rats, pigs, monkeys, and women,” The Journal of Nutrition, vol. 136, no. 5, pp. 1215–1221, 2006. View at Scopus
  62. G. Leclercq, P. de Cremoux, P. This, and Y. Jacquot, “Lack of sufficient information on the specificity and selectivity of commercial phytoestrogens preparations for therapeutic purposes,” Maturitas, vol. 68, no. 1, pp. 56–64, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. W. Wuttke, H. Jarry, and D. Seidlová-Wuttke, “Isoflavones-Safe food additives or dangerous drugs?” Ageing Research Reviews, vol. 6, no. 2, pp. 150–188, 2007. View at Publisher · View at Google Scholar · View at Scopus