Abstract
Background
Based on a rat model of human relatively high exposure to cigarette smoke, this study aimed to estimate whether Epimedium pubescen flavonoid (EPF) may prevent a smoke-induced decrease in bone mineral density (BMD) and weakening of the biomechanical properties of bone.
Methods
Fifty male Wistar rats were randomized into five groups: controls, passively smoking groups and passively smoking rats administered EPF at three dosage levels (75, 150 or 300 mg/kg/day) in drinking water for 4 months. A rat model of passive cigarette smoking was prepared by breeding male rats in a cigarette-smoking box for 4 months. Bone metabolic makers, BMD and biomechanical properties of the femoral distal end and femoral diaphysis were examined.
Results
Exposure to cigarette smoke decreased the BMD, affected bone turnover (inhibited bone formation and stimulated its resorption) and weakened the biomechanical properties of the femur at its distal end and diaphysis. EPF supplementation during cigarette smoke exposure prevented the decrease in BMD, accelerated bone turnover and weakened the biomechanical properties of bone.
Conclusion
Our data suggest that EPF supplementation can prevent the adverse effects of smoke exposure on BMD and biomechanical properties by inhibiting bone turnover and preventing bone resorption, and in this way it can decrease the risk of bone fractures.
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References
Coleman AL, Seitzman RL, Cummings SR, Yu F, Cauley JA, Ensrud KE, Stone KL, Hochberg MC, Pedula KL, Thomas EL. Study of Osteoporotic Fractures Research Group. The association of smoking and alcohol use with age-related macular degeneration in the oldest old: the Study of Osteoporotic Fractures. Am J Ophthalmol. 2010;149:160–9.
Giampietro PF, McCarty C, Mukesh B, McKiernan F, Wilson D, Shuldiner A, Liu J, LeVasseur J, Ivacic L, Kitchner T, Ghebranious N. The role of cigarette smoking and statins in the development of postmenopausal osteoporosis: a pilot study utilizing the Marshfield Clinic Personalized Medicine Cohort. Osteoporos Int. 2010;21:467–77.
Bjarnason NH, Nielsen TF, Jørgensen HL, Christiansen C. The influence of smoking on bone loss and response to nasal estradiol. Climacteric. 2009;12:59–65.
Jenkins MR, Denison AV. Smoking status as a predictor of hip fracture risk in postmenopausal women of northwest Texas. Prev Chronic Dis. 2008;5:A09.
Wong PK, Christie JJ, Wark JD. The effects of smoking on bone health. Clin Sci (Lond). 2007;113:233–41.
Donzé J, Ruffieux C, Cornuz J. Determinants of smoking and cessation in older women. Age Ageing. 2007;36:53–7.
Oncken C, Prestwood K, Kleppinger A, Wang Y, Cooney J, Raisz L. Impact of smoking cessation on bone mineral density in postmenopausal women. J Womens Health (Larchmt). 2006;15:1141–50.
Bernaards CM, Twisk JW, Snel J, van Mechelen W, Lips P, Kemper HC. Smoking and quantitative ultrasound parameters in the calcaneus in 36-year-old men and women. Osteoporos Int. 2004;15:735–41.
Kanis JA, Johnell O, Oden A, Johansson H, De Laet C, Eisman JA, Fujiwara S, Kroger H, McCloskey EV, Mellstrom D, Melton LJ, Pols H, Reeve J, Silman A, Tenenhouse A. Smoking and fracture risk: a meta-analysis. Osteoporos Int. 2005;16:155–62.
Law MR, Hackshaw AK. A meta-analysis of cigarette smoking, bone mineral density and risk of hip fracture, recognition of a major effect. BMJ. 1997;315:841–6.
Ward KD, Klesges RC. A meta-analysis of the effects of cigarette smoking on bone mineral density. Calcif Tissue Int. 2001;68:259–70.
Lorentzon M, Mellstrom D, Haug E, Ohlsson C. Smoking is associated with lower bone mineral density and reduced cortical thickness in young men. J Clin Endocrinol Metab. 2007;92:497–503.
Qin L, Zhang G, Hung WY, Shi Y, Leung K, Yeung HY, Leung P. Phytoestrogen-rich herb formula “XLGB” prevents OVX-induced deterioration of musculoskeletal tissues at the hip in old rats. J Bone Miner Metab. 2005;23:55–61.
Qian G, Zhang X, Lu L, Wu X, Li S, Meng J. Regulation of Cbfa1 expression by total flavonoids of Herba epimedii. Endocr J. 2006;53:87–94.
An SJ, Li T, Li E. Effect of kidney-tonifying herbs on ovary function and bone mass in postmenopausal women. Chin J Osteoporosis. 2000;6:55–9 (Chinese).
Maehira F, Miyagi I, Kawano N, Kawano M, Shinjoh S. Tobacco smoke exposure alters cholestryl esterase activities and causes accumulation of cholesteryl esters in the rat aorta. J Clin Biochem Nutr. 1995;18:145–55.
Epping-Jordan MP, Watkins SS, Koob GF, Markou A. Dramatic decreases in brain reward function during nicotine withdrawal. Nature. 1998;393:76–9.
Deyhim F, Stoecker BJ, Brusewitz GH, Devareddy L, Arjmandi BH. Dried plum reverses bone loss in an osteopenic rat model of osteoporosis. Menopause. 2005;12:755–62.
Brzóska MM, Majewska K, Moniuszko-Jakoniuk J. Mechanical properties of femoral diaphysis and femoral neck of female rats chronically exposed to various levels of cadmium. Calcif Tissue Int. 2005;76:287–98.
Brzóska MM, Majewska K, Moniuszko-Jakoniuk J. Weakness in the mechanical properties of femur of growing female rats exposed to cadmium. Arch Toxicol. 2005;79:519–30.
Follet H, Boivin G, Rumelhart C, Meunier PJ. The degree of mineralization is a determinant of bone strength: a study on human calcanei. Bone. 2004;34:783–9.
César-Neto JB, Benatti BB, Manzi FR, Sallum EA, Sallum AW, Nociti FH. The influence of cigarette smoke inhalation on bone density. A radiographic study in rats. Braz Oral Res. 2005;19:47–51.
Ajiro Y, Tokuhashi Y, Matsuzaki H, Nakajima S, Ogawa T. Impact of passive smoking on the bones of rats. Orthopedics. 2010;33:90–5.
Hapidin H, Othman F, Soelaiman IN, Shuid AN, Luke DA, Mohamed N. Negative effects of nicotine on bone-resorbing cytokines and bone histomorphometric parameters in male rats. J Bone Miner Metab. 2007;25:93–8.
Cornuz J, Feskanich D, Willett WC, Colditz GA. Smoking, smoking cessation, and risk of hip fracture in women. Am J Med. 1999;106:311–4.
Akhter MP, Lund AD, Gairola CG. Bone biomechanical property deterioration due to tobacco smoke exposure. Calcif Tissue Int. 2005;77:319–26.
Meng FH, Li YB, Xiong ZL, Jiang ZM, Li FM. Osteoblastic proliferative activity of Epimedium brevicornum Maxim. Phytomedicine. 2005;12:189–93.
Zhang G, Qin L, Hung WY, Shi YY, Leung PC, Yeung HY, Leung KS. Flavonoids derived from herbal Epimedium brevicornum Maxim prevent OVX-induced osteoporosis in rats independent of its enhancement in intestinal calcium absorption. Bone. 2006;38:818–25.
Zhang G, Qin L, Shi Y. Epimedium-derived phytoestrogen flavonoids exert beneficial effect on preventing bone loss in late postmenopausal women: a 24-month randomized, double-blind and placebo-controlled trial. J Bone Miner Res. 2007;22:1072–9.
Zhao J, Ohba S, Shinkai M, Chung UI, Nagamune T. Icariin induces osteogenic differentiation in vitro in a BMP- and Runx2-dependent manner. Biochem Biophys Res Commun. 2008;369:444–8.
Nian H, Ma MH, Nian SS, Xu LL. Antiosteoporotic activity of icariin in ovariectomized rats. Phytomedicine. 2009;16:320–6.
Chen KM, Ge BF, Ma HP, Liu XY, Bai MH, Wang Y. Icariin, a flavonoid from the herb Epimedium enhances the osteogenic differentiation of rat primary bone marrow stromal cells. Pharmazie. 2005;60:939–42.
Sugimoto E, Yamaguchi M. Anabolic effect of genistein in osteoblastic MC3T3-E1 cells. Int J Mol Med. 2000;5:515–20.
Yamaguchi M, Sugimoto E. Stimulatory effect of genistein and daidzein on protein synthesis in osteoblastic MC3T3-E1 cells: activation of aminoacyl-t-RNA synthetase. Mol Cell Biochem. 2000;214:97–102.
Acknowledgments
This study was supported by grants from the National Natural Science Foundation of China (no. 30300396), the Provincial Science Foundation of Hunan (no. 09JJ3048), the Provincial Development and Reform Commission Project of Hunan (2007-896), the graduate degree thesis Innovation Foundation of Hunan Province (CX-2010B102) and National Clinical Key Department Construction Projects of China. The kind help of Prof. Hong Shen with preparing the paper is appreciated.
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The authors have no conflicts of interest related to the contents of this manuscript.
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S. Gao and H. Liu contributed equally to this work.
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Gao, Sg., Liu, H., Li, Kh. et al. Effect of Epimedium pubescen flavonoid on bone mineral density and biomechanical properties of femoral distal end and femoral diaphysis of passively smoking male rats. J Orthop Sci 17, 281–288 (2012). https://doi.org/10.1007/s00776-012-0207-y
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DOI: https://doi.org/10.1007/s00776-012-0207-y