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      Longitudinal bone, muscle and adipose tissue changes in physically active subjects – sex differences during adolescence and maturity

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          Abstract

          Objectives:

          To explore changes in bone, muscle and adipose tissue composition in athletes with high physical activity levels at different stages of life.

          Methods:

          Thigh MRIs were acquired at baseline and 2-year follow-up for 20 young (16±1 years) and 20 mature (46±5 years) athletes (10 males, 10 females, respectively). Longitudinal changes in cross-sectional areas (CSAs) of femoral bone, quadriceps muscle, and thigh subcutaneous (SCF) and intermuscular (IMF) adipose tissue were evaluated.

          Results:

          Adolescent males displayed significant muscle (+5.0%, 95%CI: 0.8, 9.2) and bone growth (+2.9%, 95%CI: 1.3, 4.5), whereas adolescent females did not (muscle: +0.8%, 95%CI: -2.2, 3.8; bone: +1.9%, 95%CI: -2.1, 5.6). Adolescent and mature females showed significant SCF increases (+11.0%, 95%CI: 0.9, 21.1 and +6.0%, 95%CI: 0.6, 11.4, respectively), whereas adolescent and mature males did not (+7.2%, 95%CI: -8.0, 22.5 and +1.5%, 95%CI: -9.7, 11.8, respectively). Muscle and bone changes were highly correlated in adolescent males (r=0.66), mature males (r=0.75) and mature females (r=0.68) but not in adolescent females (r=-0.11).

          Conclusions:

          The results suggest sex-specific patterns of age-related change in bone, muscle and adipose tissue, and tight coupling of bone and muscle growth. Sex-specific bone-muscle-adipose tissue relationships may have implications for understanding sex differences in fracture risk.

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          Most cited references36

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          Pathogenesis of bone fragility in women and men.

          Ego Seeman (2002)
          There is no one cause of bone fragility; genetic and environmental factors play a part in development of smaller bones, fewer or thinner trabeculae, and thin cortices, all of which result in low peak bone density. Material and structural strength is maintained in early adulthood by remodelling; the focal replacement of old with new bone. However, as age advances less new bone is formed than resorbed in each site remodelled, producing bone loss and structural damage. In women, menopause-related oestrogen deficiency increases remodelling, and at each remodelled site more bone is resorbed and less is formed, accelerating bone loss and causing trabecular thinning and disconnection, cortical thinning and porosity. There is no equivalent midlife event in men, though reduced bone formation and subsequent trabecular and cortical thinning do result in bone loss. Hypogonadism contributes to bone loss in 20-30% of elderly men, and in both sexes hyperparathyroidism secondary to calcium malabsorption increases remodelling, worsening the cortical thinning and porosity and predisposing to hip fractures. Concurrent bone formation on the outer (periosteal) cortical bone surface during ageing partly compensates for bone loss and is greater in men than in women, so internal bone loss is better offset in men. More women than men sustain fractures because their smaller skeleton incurs greater architectural damage and adapts less effectively by periosteal bone formation. The structural basis of bone fragility is determined before birth, takes root during growth, and gains full expression during ageing in both sexes.
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            Leptin and the sympathetic connection of fat to bone.

            Loss of body weight is associated with bone loss, and body weight gain is associated with increased bone formation. The molecular mechanisms linking body weight, body composition, and bone density are now better understood. Lean mass is likely to have a significant, local effect on bone modeling and remodeling through mechanotransduction pathways. In contrast to the local regulation of bone formation and resorption by muscle-derived stimuli, peripheral body fat appears to influence bone mass via secretion of systemic, endocrine factors that link body weight to bone density even in non-weight bearing regions (e.g., the forearm). The cytokine-like hormone leptin, which is secreted by fat cells, is an important candidate molecule linking changes in body composition with bone formation and bone resorption. Increases in body fat increase leptin levels and stimulate periosteal bone formation through its direct anabolic effects on osteoblasts, and through central (CNS) effects including the stimulation of the GH-IGF-1 axis and suppression of neuropeptide Y, a powerful inhibitor of bone formation. Stimulation of beta2-adrenergic receptors through central (hypothalamic) leptin receptors does, however, increase remodeling of trabecular bone, resulting in a lower cancellous bone volume that may be better adapted to a concomitantly larger cortical bone compartment. These findings suggest that body weight and body fat can regulate bone mass and structure through molecular pathways that are independent of load-bearing. Furthermore, pharmacological manipulation of the signaling pathways activated by leptin may have significant potential for the treatment and prevention of bone loss.
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              The Bone-Muscle Relationship in Men and Women

              Muscle forces are a strong determinant of bone structure, particularly during the process of growth and development. The gender divergence in the bone-muscle relationship becomes strongly evident during adolescence. In females, growth is characterized by increased estrogen levels and increased mass and strength of bone relative to that of muscle, whereas in men, increases in testosterone fuel large increases in muscle, resulting in muscle forces that coincide with a large growth in bone dimensions and strength. In adulthood, significant age-related losses are observed for both bone and muscle tissues. Large decrease in estrogen levels in women appears to diminish the skeleton's responsiveness to exercise more than in men. In contrast, the aging of the muscle-bone axis in men is a function of age related declines in both hormones. In addition to the well-known age related changes in the mechanical loading of bone by muscle, newer studies appear to provide evidence of age- and gender-related variations in molecular signaling between bone and muscle that are independent of purely mechanical interactions. In summary, gender differences in the acquisition and age-related loss in bone and muscle tissues may be important for developing gender-specific strategies for using exercise to reduce bone loss with aging.
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                Author and article information

                Journal
                J Musculoskelet Neuronal Interact
                J Musculoskelet Neuronal Interact
                Journal of Musculoskeletal & Neuronal Interactions
                International Society of Musculoskeletal and Neuronal Interactions (Greece )
                1108-7161
                September 2016
                : 16
                : 3
                : 237-246
                Affiliations
                [1 ]Institute of Anatomy, Paracelsus Medical University Salzburg & Nuremburg, Salzburg, Austria
                [2 ]School of Allied Health, La Trobe University, Bundoora, Victoria, Australia
                [3 ]Julius Wolff Institute, Charité-Universitätsmedizin Berlin, Centre for Sports Science and Sports Medicine Berlin, Germany
                [4 ]Department of Radiology, Charité-Universitätsmedizin Berlin, Germany
                [5 ]Chondrometrics GmbH, Ainring, Germany
                Author notes
                Corresponding author: Dr Adam G. Culvenor, Institute of Anatomy, Paracelsus Medical University, Strubergasse 21, A5020 Salzburg, AUSTRIA E-mail: adam.culvenor@ 123456pmu.ac.at
                Article
                JMNI-16-237
                5114346
                27609038
                59271b35-d2a3-44bd-ae65-449091fbae1a
                Copyright: © Journal of Musculoskeletal and Neuronal Interactions

                This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-Share Alike 3.0 Unported, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 28 April 2016
                Categories
                Original Article

                knee,adolescence,muscle,adiposity,bonemized mice,bone metabolic marker

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