Hostname: page-component-7c8c6479df-27gpq Total loading time: 0 Render date: 2024-03-29T12:16:19.343Z Has data issue: false hasContentIssue false

Exposure to purified lignan from flaxseed (Linum usitatissimum) alters bone development in female rats

Published online by Cambridge University Press:  09 March 2007

Wendy E. Ward
Affiliation:
Department of Nutritional Sciences, University of Toronto, Toronto, Ontario M5S 3E2, Canada
Yvonne V. Yuan
Affiliation:
School of Nutrition, Ryerson Polytechnic University, Toronto, Ontario M5B 2K3, Canada
Angela M Cheung
Affiliation:
Osteoporosis Program, Department of Medicine, University Health Network & Mount Sinai Hospital, Toronto, Ontario
Lilian U. Thompson*
Affiliation:
Department of Nutritional Sciences, University of Toronto, Toronto, Ontario M5S 3E2, Canada
*
*Corresponding author: Dr Lilian U. Thompson, fax +1 416 978 5882, email lilian.thompson@utoronto.ca
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.

Due to the potential oestrogenic effects of secoisolariciresinol diglycoside (SDG), the mammalian lignan precursor in flaxseed (Linum usitatissimum), we hypothesized that exposure to purified SDG during early life would have a positive effect on developing bone. This present study determined whether exposure to SDG purified from flaxseed during suckling via mother's milk or continuously to adolescence (postnatal day (PND) 50) or adulthood (PND 132) increased bone mineral content (BMC) or bone strength in female rat offspring. Offspring were exposed to basal diet (BD) or one of two doses of SDG (50S, 100S) equivalent to that in a 50 or 100 g flaxseed/kg diet during lactation only or through to PND 50 or 132. At PND 50 and 132, femurs were analysed for BMC by dual energy X-ray absorptiometry and biomechanical strength by a 3-point bending test. Compared with BD group, rats exposed to continuous 50S or 100S diet had stronger femurs at PND 50 without changes in BMC. At PND 132 there were no differences in femur strength despite the fact that continuous exposure to BD resulted in a higher (P<0·05) BMC than rats exposed to 100S during lactation only or to 50S or 100S during lactation through to adulthood. In conclusion, female rat bone is more sensitive to the oestrogen-like action of lignans during early life when endogenous levels of sex hormones are low, but by adulthood the improved bone strength does not persist. Importantly, exposure to purified lignan does not have negative effects on bone strength.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2001

References

Alekel, DL, St. Germain, A, Peterson, CT, Hanson, KB, Stewart, JW & Toshiya, T (2000) Isoflavone-rich soy protein isolate attenuates bone loss in the lumbar spine of perimenopausal women. American Journal of Clinical Nutrition 72, 844852.CrossRefGoogle ScholarPubMed
Anderson, JJ, Ambrose, WW & Garner, SC (1998) Biphasic effects of genistein on bone tissue in the ovariectomized lactating rat model. Proceedings of the Society for Experimental Biology and Medicine 217, 345350.CrossRefGoogle Scholar
Anderson, JJ & Garner, SC (1998) Phytoestrogens and bone. Baillieres Clinics in Endocrinology and Metabolism 12, 543557.CrossRefGoogle ScholarPubMed
Arjmandi, BH, Alekel, L, Hollis, BW, Amin, D, Stacewicz-Sapuntzakis, M, Guo, P & Kukreja, SC (1996) Dietary soybean protein prevents bone loss in an ovariectomized rat model of osteoporosis. Journal of Nutrition 126, 161167.CrossRefGoogle Scholar
Arjmandi, BH, Birnbaum, R, Goyal, NV, Getlinger, MJ, Juma, S, Alekel, L, Hasler, CM, Drum, ML, Hollis, BW & Kukreja, SC (1998) Bone-sparing effect of soy protein in ovarian hormone-deficient rats is related to its isoflavone content. American Journal of Clinical Nutrition 68, Suppl., 1364S1368S.CrossRefGoogle ScholarPubMed
Canadian Council on Animal Care (1984) Guide to the Care and Use of Experimental Animals, Ottawa, Ont.: Institute of Laboratory Animal Resources Commission on Life Sciences.Google Scholar
Cheung, SL, Zhang, SF, Nelson, TL, Warlow, PM & Civitelli, R (1994) Stimulation of human osteoblast differentiation and function by ipriflavone and its metabolites. Calcified Tissue International 55, 356362.CrossRefGoogle Scholar
Draper, CR, Edel, MJ, Dick, IM, Randall, AG, Martin, GB & Prince, RL (1997) Phytoestrogens reduce bone loss and bone resorption in oophorectomized rats. Journal of Nutrition 127, 17951799.CrossRefGoogle ScholarPubMed
Eisman, JA (2000) Genetics of osteoporosis. Endocrine Reviews 20, 788804.CrossRefGoogle Scholar
Fanti, P, Monier-Faugere, MC, Geng, Z, Schmidt, J, Morris, PE, Cohen, D & Malluche, HH (1998) The phytoestrogen genistein reduces bone loss in short-term ovariectomized rats. Osteoporosis International 8, 274281.CrossRefGoogle ScholarPubMed
Gennari, C (1999) Calcitonin, bone-active isoflavones and vitamin D metabolites. Osteoporosis International 2, S81S90.CrossRefGoogle Scholar
Harris, SA, Tau, KR, Turner, RT & Spelsberg, TC (1996) Estrogens and progestins. In Principles of Bone Biology, pp. 510513 [Bilezikian, JP, Raisz, LG and Rodan, GA, editors]. San Diego, CA: Academic Press.Google Scholar
Ishimi, Y, Arai, N, Wang, X, Wu, J, Umegaki, K, Miyaura, C, Takeda, A & Ikegami, S (2000) Difference in effective dosage of genistein on bone and uterus in ovariectomized mice. Biochemical and Biophysical Research Communications 274, 697701.CrossRefGoogle Scholar
Ishimi, Y, Miyaura, C, Ohmura, M, Onoe, Y, Sata, H, Uchiyama, Y, Ito, M, Wang, X, Suda, T & Ikegama, S (1999) Selective effects of genistein, a soybean isoflavone, on B-lymphopoiesis and bone loss caused by estrogen deficiency. Endocrinology 140, 18931900.CrossRefGoogle ScholarPubMed
Johanson, JC, Crenshaw, TD & Benvenuga, NJ (2000) Bone strength is compromised by dietary (n-6) fatty acids independent of bone ash and bone mineral density in newborn pigs. FASEB Journal 14, A38.Google Scholar
Johnston, CJ, Miller, JZ, Slemenda, CW, Reister, TK, Hui, S, Christian, JC & Peacock, M (1992) Calcium supplementation and increases in bone mineral density in children. New England Journal of Medicine 327, 8287.CrossRefGoogle ScholarPubMed
Kuiper, GGJM, Carlsson, B, Grandien, K, Enmark, E, Haggblad, J, Nilsson, S & Gustaffson, J-A (1997) Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 138, 863870.CrossRefGoogle ScholarPubMed
Lonzer, MD, Imrie, R, Rogers, D, Worley, D, Licata, A & Secic, M (1996) Effects of heredity, age, weight, puberty, activity, and calcium intake on bone mineral density in children. Clinical Pediatrics 35, 185189.CrossRefGoogle Scholar
Molgaard, C, Thomsen, BT & Michaelsen, KF (1999) Whole body bone mineral accretion in healthy children and adults. Archives of Diseases in Childhood 81, 1015.CrossRefGoogle Scholar
Ørtoft, G & Oxlund, H (1988) Reduced strength of rat cortical bone after glucocorticoid treatment. Calcified Tissue International 43, 376382.CrossRefGoogle ScholarPubMed
Ørtoft, G, Oxlund, H, Jorgensen, PH & Andreassen, TT (1992) Glucocorticoid treatment of food deprivation counteract the stimulating effect of growth hormone on rat cortical bone strength. Acta Paediatrica 81, 912917.CrossRefGoogle ScholarPubMed
Oxlund, H, Barckman, M, Ørtoft, G & Andreassen, TT (1995) Reduced concentrations of collagen cross-links are associated with reduced strength of bone. Bone 17, 365S371S.CrossRefGoogle ScholarPubMed
Picherit, C, Coxam, V, Bennetau-Pelissero, C, Kati-Coulibaly, S, Davicco, MJ, Lebecque, P & Barlet, JP (2000) Daidzein is more efficient than genistein in preventing ovariectomy-induced bone loss in rats. Journal of Nutrition 130, 16751681.Google ScholarPubMed
Potter, SM, Baum, J-A, Teng, H, Stillman, RJ, Shay, NF & Erdman, JW Jr (1998) Soy protein and isoflavones: their effects on blood lipids and bone density in postmenopausal women. American Journal of Clinical Nutrition 68, Suppl., 1375S1379S.CrossRefGoogle ScholarPubMed
Reeves, PG, Nielsen, FM & Fahey, GC Jr (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. Journal of Nutrition 123, 19391951.CrossRefGoogle Scholar
Rickard, SE, Orcheson, LJ, Seidl, MM, Luyengi, L, Fong, HHS & Thompson, LU (1996) Dose-dependent production of mammalian lignans in rats and in vitro from the purified precursor secoisolariciresinol diglycoside in flaxseed. Journal of Nutrition 126, 20122019.Google ScholarPubMed
Slemenda, CW, Miller, MZ, Hui, SL, Reister, TK & Johnston, CC Jr (1991) Role of physical activity in the development of skeletal mass in children. Journal of Bone and Mineral Research 6, 12271233.CrossRefGoogle ScholarPubMed
Slemenda, CW, Reister, TK, Hui, SL, Miller, JZ, Christian, JC & Johnston, CC Jr (1994) Influences on skeletal mineralization in children and adolescents. Journal of Pediatrics 125, 201207.CrossRefGoogle ScholarPubMed
Teegarden, D, Proulx, WR, Martin, BR, Zhao, J, McCabe, GP, Lyle, RM, Peacock, M, Slemenda, C, Johnston, CC & Weaver, CM (1995) Peak bone mass in young women. Journal of Bone Mineral Research 10, 711715.CrossRefGoogle ScholarPubMed
Tham, DM, Gardner, CD & Haskell, WL (1998) Potential health benefits of dietary phytoestrogens: a review of the clinical, epidemiological, and mechanistic evidence. Journal of Clinical Endocrinology and Metabolism 83, 22232235.Google ScholarPubMed
Thompson, LU, Rickard, SE, Orcheson, LJ & Seidel, MM (1996) Flaxseed and its lignan components reduce mammary tumor growth at a late stage of carcinogenesis. Carcinogenesis 17, 13731376.CrossRefGoogle Scholar
Thompson, LU, Robb, P, Serraino, M & Cheung, F (1991) Mammalian lignan production from various foods. Nutrition and Cancer 16, 4352.CrossRefGoogle ScholarPubMed
Thompson, LU (1998) Experimental studies on lignans and cancer. Baillieres Clinics in Endocrinology and Metabolism 12, 691705.CrossRefGoogle ScholarPubMed
Tou, JCL, Chen, J & Thompson, LU (1998) Flaxseed and its lignan precursor secoisolariciresinol diglycoside affects pregnancy outcome and reproductive development in rats. Journal of Nutrition 128, 18611868.CrossRefGoogle ScholarPubMed
Tou, JCL, Chen, J & Thompson, LU (1999) Dose, timing and duration of flaxseed exposure affect reproductive indices and sex hormone levels in rats. Journal of Toxicology and Environmental Health 56, 555570.CrossRefGoogle ScholarPubMed
Tou, JCL & Thompson, LU (1999) Exposure to flaxseed or its lignan component during different developmental stages influences rat mammary gland structures. Carcinogenesis 20, 18311835.CrossRefGoogle ScholarPubMed
Ward, WE, Jiang, FO & Thompson, LU (2000) Exposure to flaxseed or purified lignan during lactation influences rat mammary gland structures. Nutrition and Cancer 37, 6974.CrossRefGoogle ScholarPubMed
Ward, WE & Thompson, LU (2001) Dietary estrogens of plant and fungal origin: occurrence and exposure. In Handbook of Environmental Chemistry, [Metzler, M, editor]. Heidelberg: Springer-Verlag (In the Press).Google Scholar
Ward, WE, Yuan, YV, Cheung, AM & Thompson, LU (2001) Exposure to flaxseed and its purified lignan reduces bone strength in young but not older male rats. Journal of Toxicology and Environmental Health 63, 5365.CrossRefGoogle Scholar
Weinstein, RS (2000) True strength. Journal of Bone and Mineral Research 15, 621625.CrossRefGoogle ScholarPubMed
Westerlund, KC, Wakley, GK, Evans, GL & Turner, RT (1993) Estrogen does not increase bone formation in growing rats. Endocrinology 133, 29242934.CrossRefGoogle Scholar
Windahl, SH, Norgard, M, Kuiper, GGJM, Gustafsson, J-A & Andersson, G (2000) Cellular distribution of estrogen receptor β in neonatal rat bone. Bone 26, 117121.CrossRefGoogle ScholarPubMed