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1 Maturitas 63 (2009) Contents lists available at ScienceDirect Maturitas journal homepage: Review The role of physical activity in the prevention of osteoporosis in postmenopausal women An update Natalie M. Schmitt a, Jochen Schmitt b, Martina Dören c, a Public Health Department Sächsische Schweiz Osterzgebirge, Dippoldiswalde, Germany b Section of Epidemiology and Health Services Research, Department of Dermatology, Technische Universität Dresden, Germany c Clinical Research Center of Women s Health, Charité-Berlin Medical School, Berlin, Germany article info abstract Article history: Received 10 January 2009 Received in revised form 2 March 2009 Accepted 6 March 2009 Keywords: Bone mineral density Exercise Osteoporosis Physical activity Postmenopause Context and objective: Osteoporosis causes an increase in bone fragility. Its clinical significance mainly refers to (hip) fractures secondary to (low or moderate) trauma. In Europe and North America about 6% of men and 21% of women aged years are classified to have osteoporosis. Although it is well accepted that exercise is essential for the management of osteoporosis, the exact role of physical activity in the primary and secondary prevention of osteoporotic fractures is still controversial. Methods: The MEDLINE database and reference lists of selected publications were systematically searched for randomized controlled trials and prospective cohort studies, respectively, published since January 2000 regarding the association of physical activity and osteoporosis in postmenopausal women. Results: Two prospective cohort studies indicate the clinical relevance of this association by showing an inverse relationship between physical activity and the risk of hip fracture. There is convincing evidence that physical activity effectively slows bone loss in postmenopausal women in a dose-dependent manner. Exercise programs may increase bone mineral density. Conclusion: In order to maximize the goals of public health most effective, individually adapted, intense, high impact exercise programs are needed. However, they may be complicated to communicate and adherence on the population level may be hard to achieve. These programs must be weighed against popular and applicable existing programs (e.g. aerobic classes, Tai Chi, and walking) which appear to be easier to adhere to but appear to be less effective in the prevention of osteoporotic fractures in the individual postmenopausal women Elsevier Ireland Ltd. All rights reserved. Contents 1. Introduction Methods Results Discussion Clinical implications Limitations of the evidence Need for additional research Conclusion Conflict of interest Funding References Introduction Corresponding author at: Charité-Universitätsmedizin Berlin, Campus Benjamin Franklin, Hindenburgdamm 30, D Berlin, Germany. Tel.: ; fax: address: martina.doeren@charite.de (M. Dören). Due to the increase in life expectancy disorders prevalent in postmenopausal women are becoming more and more important. Osteoporosis is a disease characterised by compromised bone mass and strength, resulting in an increase in bone fragility [1]. It is largely /$ see front matter 2009 Elsevier Ireland Ltd. All rights reserved. doi: /j.maturitas

2 N.M. Schmitt et al. / Maturitas 63 (2009) diagnosed through quantitative assessment of bone mineral density (BMD), a major determinant of bone strength [1,2]. The level of BMD in later life is a function of the maximum bone mass attained in early adulthood and of subsequent age-related bone loss, which starts after entering the fourth decade of life and accelerates in early postmenopausal years in women [3 5]. The clinical significance and (economic) burden of osteoporosis mainly refers to hip fractures and fractures of the forearm, the proximal humerus and vertebrae secondary to low to moderate trauma in postmenopausal women [1,6]. Worldwide, approximately 200 million women suffer from osteoporosis [6]. Approximately 6% of men and 21% of women aged years are classified as having osteoporosis in Europe and North America [1]. Women may change their patterns of physical activity throughout their lifespan. The engagement in physical activity depends on various factors such as general health, body mass index, smoking status, and socioeconomic position. Existing low level physical activity has been shown to be associated with the risk of fractures [6]. To be beneficial to bone health, high impact exercise is more important than the focus on endurance, a critical factor in the prevention of cardiovascular diseases [5,7]. Interventions and exercise programs targeting women in the perimenopausal period may be most effective in achieving maintenance of physical activity through the critical years of bone loss in the early postmenopausal years [8,9]. Although it is well accepted that exercise forms an integral component in the management of osteoporosis [1], the exact role of physical activity in the primary and secondary prevention of osteoporotic fractures (i.e. the clinical significant consequence of the disease) is still controversial [6]. Long-term data on the prevention of osteoporosis is scarce. Relevant reviews of the topic did not include any studies from the last decade. In addition, the low quality of included studies was noted [10]. One important review by Bonaiuti et al. meta-analysed the results of a complex range of randomized controlled trials (RCTs) regarding the association between exercise and osteoporosis in postmenopausal women published from 1966 to The authors concluded that all prescribed exercise programs, including aerobic exercise, resistance exercises or walking are effective at 1 year or more in slowing loss of BMD. (Fast) walking is recommended as the best prevention and treatment strategy for osteoporosis in postmenopausal women as it is most similar to activities of daily living and may produce the greatest compliance. The authors could not retrieve studies to show any effect of exercise for the prevention of fractures. In addition, it is unclear whether the effects of exercise on bone last after discontinuation [10]. The present review of prior publications on the association between physical activity and osteoporosis in postmenopausal women summarizes the literature since January We aim to provide an update on the beneficial value of types of exercise regimens for the prevention of osteoporosis and its consequences. 2. Methods A multi-step strategy was used to identify all relevant articles. We used overlapping search strategies including systematic electronic searches (MEDLINE using the MeSH terms exercise, physical activity, and osteoporosis ) and hand search of the reference lists of all included articles. We limited the systematic search to female adults and to core clinical journals in English language dating from January 2000 to October We focussed on RCTs and prospective cohort studies, which provided data on the association of exercise and or physical activity and osteoporosis, respectively. The abstracts were screened and full-text articles retrieved if abstracts provided essential information upon our objectives. Abstracts and articles were reviewed by three authors (NS, MD, JS). Publications were eligible for inclusion if any information (primary or secondary data, literature review of publications) on the effects of physical activity on the bone mass and strength in postmenopausal women was presented. 3. Results Seven publications were included in this literature review, three of which report on RCT [4,11,12], one on a controlled though not randomized clinical trial [13], and three on prospective cohort studies [7,14,15]. Six studies exclusively evaluated postmenopausal women [4,7,12 15] whereas one included both men and women and only presents limited data on the subgroup of postmenopausal women [11]. Tables 1 and 2 summarize major details on the characteristics, participants, and results. Milliken et al. [12] conducted a trial on depressive symptoms, body weight, and bone mass density in 320 postmenopausal women exercising for 1 year. Participants were stratified by use of hormone replacement therapy (HRT) and randomized to supervised exercise vs control group. Unfortunately, the authors did not provide enough details on the type, intensity, and duration of the exercise program to estimate its appropriateness for prevention of loss of BMD. All participants were supplemented with 800 mg calcium. Exercise had a positive effect on BMD in postmenopausal women. However, a statistically significant effect of exercise was present only on the hip and not on the lumbar spine. This could be possibly explained by the type of exercise program. Although this is an important, its relevance for public health practice is limited by the missing information on the relevant characteristics of the exercise program. Interestingly, depressive symptoms explained a greater proportion of the variability of BMD than exercise in this trial. Chan et al. [4] reported on a smaller RCT (n = 132) with a design similar to the aforementioned trial [12]. The exercise group performed 5 sessions Tai Chi Chun per week. The characteristics of Tai Chi Chun were described as low-impact, weight bearing exercise with slow and smooth movements at constant speed, an exercise regularly practiced by older women in Hong Kong. After 1 year the authors did not observe any statistically significant differences in bone loss in the lumbar spine and proximal femur or incident fractures between control group and exercise group. The differences for these outcomes between the two groups were very small and the had adequate power to show clinically relevant differences. We believe that the observed differences in BMD of the distal tibia are clinically less important as fractures of this bone are not typically related to osteoporosis in postmenopausal women. The RCT by de Jong et al. [11] suggested that aerobic fitness, muscle strength, and the use of bisphosphonates were independently associated with an increase in BMD in a population with an increased risk for osteoporosis (i.e. patients with rheumatoid arthritis). This included both men and women and menopausal status was not reported. The fact that the results of this were robust after adjustment for age and sex suggests that the results are relevant for postmenopausal women. However, the data should be interpreted with caution, because the pathophysiology of bone loss in rheumatoid arthritis may be distinctly different from the one related to changes associated to the changes after menopause. Additionally, the generalizability of the results from this RCT to a lower risk population still needs further investigation. Unlike the studies described above which evaluated the effects of common or not further specified exercise programs, Kemmler et al. [13] aimed to design an optimal program targeted at the prevention of osteoporosis in early postmenopausal women. The program was designed and supervised by an interdisciplinary team including

3 36 N.M. Schmitt et al. / Maturitas 63 (2009) Table 1 Study characteristics, research question, and description of participants of included studies. Reference Study type Study duration; geographical region Research question relevant to this review Number of participants; mean (SD) age (years); ethnicity Milliken et al. [12] RCT 12 months; US What are the effects of exercise on BMD in postmenopausal women? Chan et al. [4] RCT 12 months; Hong What is the effect of supervised Kong exercise on the prevention of early postmenopausal bone loss? de Jong et al. [11] RCT 24 months; the Netherlands Kemmler et al. [13] Non-RCT 26 months; Germany Feskanich et al. [7] Prospective cohort 12 years; 11 US states Robbins et al. [15] Kerschan-Schindl et al. [14] Prospective cohort Prospective cohort Is a long-term, high-intensity, weight-bearing exercise program able to prevent the loss of BMD in patients with rheumatoid arthritis? What is the effect of intense exercise on BMD in early postmenopausal women? What is the relationship between walking, leisure time activity and the risk of hip fracture? 7.6 years (mean); US What are the risk factors of hip fracture in postmenopausal women? 9.7(1.0) years mean What is the effect of a nonprogressive (SD); Austria home exercise program in women with a history of postmenopausal fractures and low bone mass? n = 320; 55.6 (4.8); not reported n = 132; 54.0 (3.5); Chinese n = 309 men and women; n.r.; median 54; 25th, 75th percentile: 46,61 eg, 45,62 cg; not reported n = 137; 55.5 (3.2) eg, 55.9 (3.1) cg; not reported n = 61,200; n.r.; range: years; 98% white n = 10,750 (BMD); n.r.; range: years; n.r.; multiethnic n = 19 eg, n = 6 cg; 65.3 (5.6) eg, 60.4 (4.6) cg; not reported SD: standard deviation; n.r.: not reported; eg: exercise group; cg: control group; RCT: randomized controlled trial; BMD: bone mineral density. Table 2 Description of the variable physical activity, outcome parameters, follow-up rate, and results of included studies. Reference Description of physical activity Outcome measurements Follow-up rate Major findings Milliken et al. [12] Chan et al. [4] de Jong et al. [11] Kemmler et al. [13] Feskanich et al. [7] Robbins, 2007 [15] Kerschan-Schindl, 2000 [14] 1 year supervised exercise training program; quantified by cumulative amount of weight lifted during the 1-year exercise program; no further details reported 5 supervised Tai Chi Chun exercise sessions à 45 min per week 2 supervised high-intensity (weight bearing and impact loading) exercise sessions à 75 min per week 2 supervised group sessions à min + 2 non-supervised individual home training sessions à 25 min per week (warm-up, endurance, jumping, strength and flexibility training) 4 assessments (questionnaire): 7 activities, 11 duration categories; calculation of mean MET-h/wk Self-reported, measured as METs Partly supervised home exercise program minimum 3 20 min per week (focusing on flexibility, posture, coordination) BMD: DXA of lumbar spine, femoral neck, greater trochanter BMD: (1) DXA of lumbar spine, proximal femur; (2) QCT of distal tibia; fractures BMD: DXA of total hip and lumbar spine BMD: (1) DXA of lumbar spine, proximal femur, forearm; (2) QCT of lumbar spine Serum makers of bone turnover (osteocalcin, bone resorption from serum cross-links) Self-reported incident hip fracture due to low or moderate trauma Self-reported hip fractures, confirmed by review of medical records BMD: DXA of lumbar spine, femoral neck; X-rays of vertebral column; fractures 83% Statistically significant exercise effect on BMD of trochanter and femoral neck, not on lumbar spine; cumulative amount of weight lifted during the 1-year exercise program statistically significantly predicts BMD changes of greater trochanter 81% eg; 83% cg DXA: no statistically significant difference in bone loss between eg and cg; QCT: rate of bone density loss (%) significantly higher in cg ( 1,58) compared to eg ( 0,61); fractures: 3 cg, 1 eg 91% Multivariate analyses: use of bisphosphonates, increase in muscle strength and increase in aerobic fitness are associated with an increase in hip BMD; similar results after adjustment for age and sex 58% eg; 65% cg Statistically significant exercise effects: DXA spine: +0,7% eg, 2,3% cg; DXA hip: 0,3% eg, 1,7% cg; QCT: density decrease in metabolically more active trabecular bone cortical compartments; no difference in BMD of forearm and in serum makers between eg and cg Not reported; 576,518 person-years Not reported Physical activity is inversely associated with risk of hip fracture: 55% lower risk of hip fracture when 24 MET-h/wk vs < 3 MET-h/wk; decline in risk in a dose-dependent manner; risk of hip fracture increased linearly (statistically significant) with increasing reduction of activity Physical activity is an independent predictor of hip fracture 37% eg No statistically significant difference in BMD between cg and eg; vertebral fractures: 0 cg, 6 eg; non-vertebral fractures: 3 cg, 9 eg eg: exercise group; cg: control group; RCT: randomized controlled trial; BMD: bone mineral density; DXA: dual-energy X-ray absorptiometry; QCT: quantitative computed tomography; METs: metabolic equivalent tasks (a MET is the ratio of work metabolic rate to a standard resting metabolic rate of kj/kg per hour [25]); e.g. walking at an average pace: MET score of 3; h/wk: hours per week.

4 N.M. Schmitt et al. / Maturitas 63 (2009) health physicists, sport scientists, and physicians. The exercise program was evaluated in a non-randomized controlled trial in a total of 137 women, 86 of which were allocated to the exercise group and 51 to the control group (according to patients preferences). Another advantage of the is the long duration of 26 months. All women were individually supplemented to ensure intake of 1.5 g calcium and 500 IU cholecalciferol, so that the exercise effect was not obscured by insufficient calcium and vitamin D intake. Exercise effectively prevented bone mass loss in the lumbar spine and hip (dual-energy X-ray absorptiometry measurement). In the spine, even an increase in BMD could be achieved in the exercise group, whereas women in the control group significantly lost bone mass in the hip and lumbar spine. In the control group the decrease in BMD was much higher in the metabolically more active trabecular bone than in the cortical compartments (quantitative computed tomography measurement). The relationship between walking, leisure time activity, and the risk of hip fracture was prospectively investigated in a subgroup of the Nurses Health Study in 61,200 postmenopausal, predominantly Caucasian women without hip fractures at baseline [7]. Physical activity was assessed using a questionnaire and quantified by metabolic equivalent tasks (METs)-hours per week. Other than in the RCTs, the primary outcome was not BMD but incident hip fracture due to low or moderate trauma, a highly relevant (clinical) event. The data suggest that physical activity prevents hip fractures in a dose-dependent manner. Body mass index, HRT, smoking, diet, and calcium/vitamin D intake the major other known determinants of osteoporosis in postmenopausal women only slightly confounded the relationship between physical activity and risk of hip fracture. Walking also significantly decreased the risk of hip fracture. The faster the pace, the higher the preventive effect of walking. Although the generalizability to higher risk and non- Caucasian populations might be limited we believe that this by Feskanich et al. is highly relevant for public health. Another large prospective cohort by Robbins et al. [15] replicated the finding that physical activity is an independent predictor of hip fracture in postmenopausal women. This component of the Women s Health Initiative, however, aimed to develop an algorithm to predict the risk of hip fractures and only offers limited information on the detailed role of physical activity in the prevention of osteoporotic fractures. Kerschan-Schindl et al. [14] evaluated the effect of a nonprogressive exercise program which had been shown to delay bone loss in postmenopausal women with and without reduced BMD. The included postmenopausal women at risk for recurrent fractures. Only 19 women participated in the home exercise program for a mean follow-up of 10 years (control group: n = 6). The authors did not observe any statistically significant differences in BMD or osteoporotic fractures between the exercise and control group. Methodological limitations of this include low follow-up rate (36% in the exercise group), insufficient power, and evidence of insufficient compliance of participants. Other studies of higher quality focussing on women with a history of postmenopausal fractures and low bone mass are critically important to fill the research gap in this relevant population. 4. Discussion 4.1. Clinical implications The early postmenopause is a period in which fast bone loss in women s lifespan occurs. Effective interventions should target perimenopausal women in order to maintain physical activity into the critical postmenopausal years of life at least [4,8]. Eveninlater life initiation of physical activity can reduce fracture risk, but it must be maintained in order to preserve its benefits on bone health [7]. As physical activity seems to stimulate bone accretion in a dose-dependent manner with a low threshold (active living), the intensity of physical activity is one important determinant in the prevention of osteoporosis [5,7,16]. Based on risk estimates of the Nurses Health Study, 23% (42%) of the hip fractures in the age group years may be prevented by exercising at 9 MET-h/wk or higher (24 MET-h/wk or higher) [7]. On the other hand, walking has already been proven suitable for lowering fracture risk and the rate of bone loss [7,17,18], so that we agree with the recommendation by Bonaiuti et al. that fast walking is an adequate tool in the prevention of osteoporosis [10]. This review focuses on the effect of physical activity on osteoporosis. We want to point out, that the positive implications of exercising go far beyond: prevention of falls through improvements in muscle strength, balance and posture control, increase in fitness and quality of life, decrease in pain intensity and frequency at the spine, prevention of age-related decline in levels of vitamin D (outdoor activity) [19], prevention of cardiovascular diseases, cancer and depression etc [4,7,12,13,20]. These highly important issues were beyond the scope of our review. However, the risk and significance of sport accidents and injuries should not be neglected in the subpopulation of older women. In addition, increases in physical activity in combination with body weight loss may show detrimental effects on BMD [21]. The risks and benefits of lowimpact exercise with slow and smooth movements [4] should be weighed against more active programs including jumping and aerobics [13] in the individual woman. The characteristics of physical activity and exercise programs determine their effect on BMD and the prevention of osteoporotic fractures on the individual and on the population level. In low-risk women the specific improvement of muscle strength and aerobic fitness without weight- or impactbearing components do not seem to be effective in increasing BMD [22]. The specifically tailored supervised exercise program developed by Kemmler et al. [13] which showed a significant impact on bone density may be regarded as a best practice example of effective prevention of BMD loss in early postmenopausal women Limitations of the evidence It should be remembered that the assessment of physical activity largely depended on self-reports in the studies elected for this review. Although MET is an accepted methodology to capture physical activity and appears to be the gold standard, only a minority of studies are available to provide insights into the issue of this review. Furthermore, poor adherence to effective training programs [5,9,10,13] expose the problem that obviously it is very difficult to maintain a life style optimal for bone health in daily life for many women. Self-management programs including education on osteoporosis and its prevention, covering promotion of behavioural strategies for maximizing bone health, may play a critical role in the development of lasting behaviour changes (e.g. engagement in tailored exercise programs) in postmenopausal women [20]. Finally, the value of BMD may be questionable. In some studies, BMD is assessed in skeletal sites without clinical relevance, e.g. in the tibia where osteoporotic fractures do not typically occur [4]. There is evidence that exercise directed at strengthening the back muscles reduce the risk of vertebral fractures, but not via an increase in BMD [23]. When compared with other fractures frequently occurring in postmenopausal women, morbidity, mortality and costs generated by hip fractures range highest [11]. In addition, the prediction of fractures in postmenopausal women is not improved by BMD measurements at multiple sites [1]. Thus, existing recommendations on the preference of BMD measurements in the hip must be promoted in order to increase comparability of results [1,2,11].

5 38 N.M. Schmitt et al. / Maturitas 63 (2009) Need for additional research The separate analysis of the association between bone status and physical activity in pre- and postmenopausal women which can be observed in the literature most likely hides the complexity of the issue. Due to lack of good-quality, long-term studies, it is still not proven whether exercise intervention programs decrease the risk of hip fractures. A more comprehensive approach in the investigation of the effects of physical activity on bone mineral density and bone strength throughout women s lifespan is urgently needed. It is one scenario for which long-term prospective cohort studies with hard endpoints (incident hip fractures vs BMD) appear to be more informative to understand the complex relationship than RCTs. Future research should consider combining the advantages of RCT and prospective cohort studies for the research question of interest e.g. by specifically training a randomly selected subgroup of a large cohort for several months followed by long-term observation of osteoporotic fractures and regular assessment of physical activity and other causal factors for osteoporosis. Effective strategies identifying women at high risk of osteoporosis who would thus benefit most from exercise programs or more comprehensive interventions (diet, smoking and outdoor activity) is critically important in order to reduce the great public health burden of osteoporosis. 5. Conclusion Based on few and not entirely comparable studies discussed in this review moderate or high intensity physical activity appears to exert site-specific beneficial effects on BMD. Individually tailored, intense, high impact exercise programs [13] may be most effective to maximize the goals of public health to prevent osteoporosis and consecutive adverse outcomes. However, high cost, low practicability, and limited applicability in routine prevention and care may limit the appropriateness of this approach. Popular and more easily applicable existing programs (e.g. aerobic classes, Tai Chi, and walking) seem less effective in the prevention of osteoporotic fractures in postmenopausal women based on the studies included in this review [24]. Conflict of interest The authors declare that there is no conflict of interest. Funding There has not been any funding related to this. References [1] Kanis JA, Burlet N, Cooper C, et al. European guidance for the diagnosis and management of osteoporosis in postmenopausal women. Osteoporos Int 2008;19: [2] Genant HK, Cooper C, Poor G, et al. Interim report and recommendations of the World Health Organization Task-Force for Osteoporosis. Osteoporos Int 1999;10: [3] Beitz R, Dören M. Physical activity and postmenopausal health. J Br Menopause Soc 2004;10:70 4. [4] Chan K, Qin L, Lau M. A randomized, prospective of the effect of Tai Chi Chun exercise on bone mineral density in postmenopausal women. Arch Phys Med Rehabil 2004;85: [5] Stear SJ, Prentice A, Jones SC, Cole TJ. Effect of calcium and exercise intervention on the bone mineral status of y-old adolescent girls. Am J Clin Nutr 2003;77: [6] Lane NE. Epidemiology, etiology, and diagnosis of osteoporosis. Am J Obstet Gynecol 2006;194:S3 11. [7] Feskanich D, Willett W, Colditz G. Walking and leisure-time activity and risk of hip fracture in postmenopausal women. JAMA 2002;288: [8] Evenson KR, Wilcox S, Pettinger M, et al. Vigorous leisure activity through women s adult life. Am J Epidemiol 2002;156: [9] Heinonen A, Kannus P, Sievänen H, et al. Randomised controlled trial of effect of high-impact exercise on selected risk factors for osteoporotic fractures. Lancet 1996;348: [10] Bonaiuti D, Shea B, Iovine R, et al. Exercise for preventing and treating osteoporosis in postmenopausal women (review). In: The Cochrane Database of Systematic Reviews. Oxford: The Cochrane Library; 2002, issue 2 (Art. No.: CD000333). [11] de Jong Z, Munneke M, Lems WF. Slowing of bone loss in patients with rheumatoid arthritis by long-term high-intensity exercise. Arthritis Rheum 2004;50: [12] Milliken LA, Wilhelmy J, Martin CJ. Depressive symptoms and changes in body weight exert independent and site-specific effects on bone in postmenopausal women exercising for 1 year. J Gerontol 2006;61A: [13] Kemmler W, Lauber D, Weineck J, Hensen J, Kalender W, Engelke K. Benefits of 2 years of intense exercise on bone density, physical fitness, and blood lipids in early postmenopausal osteopenic women. Arch Intern Med 2004;164: [14] Kerschan-Schindl K, Uher E, Kainberger F, Kaider A, Ghanem A-H, Preisinger E. Long-term home exercise program: effect in women at high risk of fracture. Arch Phys Med Rehabil 2000;81: [15] Robbins J, Aragaki AK, Kooperberg C, et al. Factors associated with 5-year risk of hip fracture in postmenopausal women. JAMA 2007;298: [16] Greendale GA, Huang M-H, Wang Y, Finkelstein JS, Danielson ME, Sternfeld B. Sport and home physical activity are independently associated with bone density. Med Sci Sports Exerc 2003;35: [17] Krall EA, Dawson-Hughes B. Walking is related to bone density and rates of bone loss. Am J Med 1994;96:20 6. [18] Nelson ME, Fisher EC, Dilmanian FA, Dallal GE, Evans WJ. A 1-y walking program and increased dietary calcium in postmenopausal women: effects on bone. Am J Clin Nutr 1991;53: [19] Scragg R, Camargo Jr CA. Frequency of leisure-time physical activity and serum 25-hydroxyvitamin D levels in the US population: results from the Third National Health and Nutrition Examination Survey. Am J Epidemiol 2008;168: [20] Alp A, Kanat E, Yurtkuran M. Efficacy of a self-management program for osteoporotic subjects. Am J Phys Med Rehabil 2007;86: [21] Salamone LM, Cauley JA, Black DM, et al. Effect of a lifestyle intervention on bone mineral density in premenopausal women: a randomized trial. Am J Clin Nutr 1999;70: [22] Häkkinen A, Sokka T, Kotaniemi A, Hannonen P. A randomized two-year of the effects of dynamic strength training on muscle strength, disease activity, functional capacity, and bone mineral density in early rheumatoid arthritis. Arthritis Rheum 2001;44: [23] Sinaki M, Itoi E, Wahner HW, et al. Stronger back muscles reduce the incidence of vertebral fractures: a prospective 10 year follow-up of postmenopausal women. Bone 2003;30: [24] Kelley GA. Exercise and regional bone mineral density in postmenopausal women: a meta-analytic review of randomized trials. Am J Phys Med Rehabil 1998;77: [25] Ainsworth BE, Haskell WL, Leon AS, et al. Compendium of physical activities: classification of energy costs of human physical activities. Med Sci Sports Exerc 1993;25:71 80.

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