Title

耐力運動與飲食控制型塑骨骼系統之骨代謝與能量代謝觀

Translated Titles

The Skeleton Modeled by Endurance Exercise and Dietary Manipulation: A Perspective from the Interaction between Bone Metabolism and Energy Metabolism

DOI

10.3966/102472972015034801001

Authors

黃滄海(Tsang-Hai Huang)

Key Words

骨鈣素 ; 胰島素 ; 骨品質 ; 骨密度 ; osteocalcin ; insulin ; bone quality ; bone density

PublicationName

體育學報

Volume or Term/Year and Month of Publication

48卷1期(2015 / 03 / 01)

Page #

1 - 17

Content Language

繁體中文

Chinese Abstract

在傳統的觀念中,骨頭對身體所提供的功能包括:保護腦/臟器、儲存礦物質、支撐身體、作為執行各種運動時的槓桿系統以及造血。近年來,骨生物學最新的發現指出,骨頭不再只是激素調節過程中的接受者,實際上,骨頭可被視為一器官看待,並具有主動調節能量代謝反應(包括:血糖調控)的能力。胰島素已被證實會進一步作用在造骨細胞上的胰島素受器,而其下游反應除了直接促成造骨細胞分泌骨鈣素之外,同時也會間接促進蝕骨細胞進行骨吸收作用而釋出存放於骨基質中的骨鈣素。經研究證實,羧化不完全的骨鈣素會刺激胰臟的β細胞分泌更多的胰島素,因而使得血糖調降的過程更有效率。耐力運動及飲食控制(例如:熱量限制)為具有減重以及促進能量代謝敏感性的行為改變方式,然而,這兩種介入方式經常伴隨有較低骨頭質量及較小骨頭尺寸的現象,因此,常被認為對骨骼健康沒有正面助益。本文旨在整合骨頭可被視為內分泌器官的新知與傳統已知的骨代謝調節機制,針對耐力運動及飲食控制所導致的低骨量及較小骨尺寸提供一嶄新的觀點,文中論述亦包含骨代謝與能量代謝兩者之間的交互作用。耐力運動和飲食控制除了和較低的骨量或骨尺寸有關之外,實際上,這兩種介入方式所改善的代謝特徵(例如:較低的發炎反應或向下調節的氧化壓力)反而對長期的骨代謝而言是有助益的。同時,本文亦針對骨密度學測量方法以及骨品質指標的有效性進行論述,藉以闡明耐力運動及飲食控制對骨健康的影響。

English Abstract

Traditionally, well-known functions of bones include protecting brain/internal organs, serving as a reservoir of mineral, supporting body, providing leverage system for various movements and producing blood cells. Recently novel findings suggest that bone is not only a tissue served as a recipient of hormonal inputs but also an organ actively mediating energy metabolism, which includes blood sugar regulation. Insulin has been verified to act through insulin receptor (IR) located on osteoblast, and the downstream reactions of osteoblast IR which would directly stimulate the secretion of osteocalcin from osteoblast as well as indirectly up-regulate the bone resorption released osteocalcin from bone matrix. And, it is the undercarboxylated osteocalcin further stimulating insulin secretion from β-cell of pancreas and enhancing the efficiency of blood glucose down-regulation. Endurance exercise and dietary manipulations (e.g caloric restriction) are behavioral modifications, which have well-proven efficiencies in body weight reduction and also in promoting energy metabolic sensitivity. However, the effects of those two interventions frequently accompany with lower bone mass as well as smaller bone sizes. Hence, endurance exercise and caloric restriction have been considered not beneficial for bone health. The first purpose of the current review was to integrate the new knowledge of bone serving as an endocrine organ with traditional bone regulating mechanisms. Then, we provided a brand-new opinion with regard to endurance exercise and dietary manipulations caused low bone mass as well as smaller bone size. Discussions of interactions between bone metabolism and energy metabolism were included. In spite of correlating with lower bone mass/size, endurance exercise and dietary manipulation actually ameliorate the metabolism profile (e.g. lower inflammatory response, down-regulated oxidative stress) which would further benefit to bone metabolism. In addition, arguments regarding the validity of densitometric measurements and bone quality were also included to elucidate the effects of endurance exercise and dietary manipulations on bone health.

Topic Category 社會科學 > 體育學
Reference
  1. Alfadda, A. A.,Masood, A.,Shaik, S. A.,Dekhil, H.,Goran, M.(2013).Association between osteocalcin, metabolic syndrome, and cardiovascular risk factors: Role of total and undercarboxylated osteocalcin in patients with type 2 diabetes.International Journal of Endocrinology
  2. Atalay, S.,Elci, A.,Kayadibi, H.,Onder, C. B.,Aka, N.(2012).Diagnostic utility of osteocalcin, undercarboxylated osteocalcin, and alkaline phosphatase for osteoporosis in premenopausal and postmenopausal women.Annals of Laboratory Medicine,32,23-30.
  3. Bennell, K. L.,Malcolm, S. A.,Khan, K. M.,Thomas, S. A.,Reid, S. J.,Brukner, P. D.,Wark, J. D.(1997).Bone mass and bone turnover in power athletes, endurance athletes, and controls: A 12-month longitudinal study.Bone,20,477-484.
  4. Bluher, M.,Michael, M. D.,Peroni, O. D.,Ueki, K.,Carter, N.,Kahn, B. B.,Kahn, C. R.(2002).Adipose tissue selective insulin receptor knockout protects against obesity and obesity-related glucose intolerance.Developmental Cell,3,25-38.
  5. Blum, M.,Harris, S. S.,Must, A.,Naumova, E. N.,Phillips, S. M.,Rand, W. M.,Dawson-Hughes, B.(2003).Leptin, body composition and bone mineral density in premenopausal women.Calcified Tissue International,73,27-32.
  6. Boulé, N. G.,Haddad, E.,Kenny, G. P.,Wells, G. A.,Sigal, R. J.(2001).Effects of exercise on glycemic control and body mass in type 2 diabetes mellitus: A meta-analysis of controlled clinical trials.Journal of the American Medical Association,286,1218-1227.
  7. Boulé, N. G.,Weisnagel, S. J.,Lakka, T. A.,Tremblay, A.,Bergman, R. N.,Rankinen, T.,Bouchard, C.(2005).Effects of exercise training on glucose homeostasis: The HERITAGE family study.Diabetes Care,28,108-114.
  8. Bozzini, C. E.,Champin, G.,Alippi, R. M.,Bozzini, C.(2011).Bone mineral density and bone strength from the mandible of chronically protein restricted rats.Acta Odontologica Latinoamericana,24,223-228.
  9. Brahm, H.,Strom, H.,Piehl-Aulin, K.,Mallmin, H.,Ljunghall, S.(1997).Bone metabolism in endurance trained athletes: A comparison to population-based controls based on DXA, SXA, quantitative ultrasound, and biochemical markers.Calcified Tissue International,61,448-454.
  10. Bruning, J. C.,Michael, M. D.,Winnay, J. N.,Hayashi, T.,Horsch, D.,Accili, D.,Kahn, C. R.(1998).A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without altering glucose tolerance.Molecular cell,2,559-569.
  11. Bullo, M.,Moreno-Navarrete, J. M.,Fernandez-Real, J. M.,Salas-Salvado, J.(2012).Total and undercarboxylated osteocalcin predict changes in insulin sensitivity and beta cell function in elderly men at high cardiovascular risk.American Journal of Clinical Nutrition,95,249-255.
  12. Burghardt, A. J.,Issever, A. S.,Schwartz, A. V.,Davis, K. A.,Masharani, U.,Majumdar, S.,Link, T. M.(2010).High-resolution peripheral quantitative computed tomographic imaging of cortical and trabecular bone microarchitecture in patients with type 2 diabetes mellitus.Journal of Clinical Endocrinology and Metabolism,95,5045-5055.
  13. Burrows, M.,Nevill, A. M.,Bird, S.,Simpson, D.(2003).Physiological factors associated with low bone mineral density in female endurance runners.British Journal of Sports Medicine,37,67-71.
  14. Camporez, J. P.,Jornayvaz, F. R.,Lee, H. Y.,Kanda, S.,Guigni, B. A.,Kahn, M.,Shulman, G. I.(2013).Cellular mechanism by which estradiol protects female ovariectomized mice from high-fat diet-induced hepatic and muscle insulin resistance.Endocrinology,154,1021-1028.
  15. Cao, J. J.(2011).Effects of obesity on bone metabolism.Journal of Orthopaedic Surgery and Research,6,30-36.
  16. Chaudhary, S. B.,Liporace, F. A.,Gandhi, A.,Donley, B. G.,Pinzur, M. S.,Lin, S. S.(2008).Complications of ankle fracture in patients with diabetes.Journal of the American Academy Orthopaedic Surgeons,16,159-170.
  17. Colman, R. J.,Beasley, T. M.,Allison, D. B.,Weindruch, R.(2012).Skeletal effects of long-term caloric restriction in rhesus monkeys.Age,34,1133-1143.
  18. Cooper, L. A.,Joy, E. A.(2005).Osteoporosis in a female cross-country runner with femoral neck stress fracture.Current Sports Medicine Reports,4,321-322.
  19. Dalsky, G. P.,Stocke, K. S.,Ehsani, A. A.,Slatopolsky, E.,Lee, W. C.,Birge, S. J., Jr.(1988).Weight-bearing exercise training and lumbar bone mineral content in postmenopausal women.Annals of Internal Medicine,108,824-828.
  20. Davicco, M. J.,Horcajada-Molteni, M. N.,Gaumet-Meunier, N.,Lebecque, P.,Coxam, V.,Barlet, J. P.(1999).Endurance training and bone metabolism in middle-aged rats.Mechanisms of Ageing and Development,109,83-96.
  21. Devlin, M. J.,Cloutier, A. M.,Thomas, N. A.,Panus, D. A.,Lotinun, S.,Pinz, I.,Bouxsein, M. L.(2010).Caloric restriction leads to high marrow adiposity and low bone mass in growing mice.Journal of Bone and Mineral Research,25,2078-2088.
  22. Dumortier, M.,Brandou, F.,Perez-Martin, A.,Fedou, C.,Mercier, J.,Brun, J. F.(2003).Low intensity endurance exercise targeted for lipid oxidation improves body composition and insulin sensitivity in patients with the metabolic syndrome.Diabetes and Metabolism,29,509-518.
  23. Duncan, C. S.,Blimkie, C. J.,Cowell, C. T.,Burke, S. T.,Briody, J. N.,Howman-Giles, R.(2002).Bone mineral density in adolescent female athletes: Relationship to exercise type and muscle strength.Medicine and Science in Sports and Exercise,34,286-294.
  24. Fallon, K. E.,Fallon, S. K.,Boston, T.(2001).The acute phase response and exercise: court and field sports.British Journal of Sports Medicine,35,170-173.
  25. Felson, D. T.,Zhang, Y.,Hannan, M. T.,Anderson, J. J.(1993).Effects of weight and body mass index on bone mineral density in men and women: the Framingham study.Journal of Bone and Mineral Research,8,567-573.
  26. Ferron, M.,Wei, J.,Yoshizawa, T.,Del Fattore, A.,DePinho, R. A.,Teti, A.,Karsenty, G.(2010).Insulin signaling in osteoblasts integrates bone remodeling and energy metabolism.Cell,142,296-308.
  27. Friedman, J. M.,Halaas, J. L.(1998).Leptin and the regulation of body weight in mammals.Nature,395,763-770.
  28. Frost, H. M.(1987).Bone "mass" and the "mechanostat": A proposal.Anatamical Record,219,1-9.
  29. Frost, H. M.(1997).Obesity, and bone strength and "mass": A tutorial based on insights from a new paradigm.Bone,21,211-214.
  30. Fulzele, K.,Riddle, R. C.,DiGirolamo, D. J.,Cao, X.,Wan, C.,Chen, D.,Clemens, T. L.(2010).Insulin receptor signaling in osteoblasts regulates postnatal bone acquisition and body composition.Cell,142,309-319.
  31. Gaffney-Stomberg, E.,Cao, J. J.,Lin, G. G.,Wulff, C. R.,Murphy, N. E.,Young, A. J.,Pasiakos, S. M.(2014).Dietary protein level and source differentially affect bone metabolism, strength, and intestinal calcium transporter expression during ad libitum and food-restricted conditions in male rats.Journal of Nutrition,144,821-829.
  32. Goulding, A.,Taylor, R. W.,Jones, I. E.,McAuley, K. A.,Manning, P. J.,Williams, S. M.(2000).Overweight and obese children have low bone mass and area for their weight.International Journal of Obesity and Related Metabolic Disorders,24,627-632.
  33. Hamann, C.,Goettsch, C.,Mettelsiefen, J.,Henkenjohann, V.,Rauner, M.,Hempel, U.,Hofbauer, L. C.(2011).Delayed bone regeneration and low bone mass in a rat model of insulin-resistant type 2 diabetes mellitus is due to impaired osteoblast function.American Journal of Physiology: Endocrinology and Metabolism,301,1220-1228.
  34. Hamann, C.,Kirschner, S.,Gunther, K. P.,Hofbauer, L. C.(2012).Bone, sweet bone-osteoporotic fractures in diabetes mellitus.Nature Reviews Endocrinology,8,297-305.
  35. Hamrick, M. W.,Ding, K. H.,Ponnala, S.,Ferrari, S. L.,Isales, C. M.(2008).Caloric restriction decreases cortical bone mass but spares trabecular bone in the mouse skeleton: implications for the regulation of bone mass by body weight.Journal of Bone and Mineral Research,23,870-878.
  36. Hind, K.,Truscott, J. G.,Evans, J. A.(2006).Low lumbar spine bone mineral density in both male and female endurance runners.Bone,39,880-885.
  37. Hinoi, E.,Gao, N.,Jung, D. Y.,Yadav, V.,Yoshizawa, T.,Myers, M. G., Jr.,Karsenty, G.(2008).The sympathetic tone mediates leptin's inhibition of insulin secretion by modulating osteocalcin bioactivity.Journal of Cell Biology,183,1235-1242.
  38. Hinton, P. S.,Rector, R. S.,Linden, M. A.,Warner, S. O.,Dellsperger, K. C.,Chockalingam, A.,Thomas, T. R.(2012).Weight-loss-associated changes in bone mineral density and bone turnover after partial weight regain with or without aerobic exercise in obese women.European Journal of Clinical Nutrition,66,606-612.
  39. Hofbauer, L. C.,Brueck, C. C.,Singh, S. K.,Dobnig, H.(2007).Osteoporosis in patients with diabetes mellitus.Journal of Bone and Mineral Research,22,1317-1328.
  40. Hotamisligil, G. S.,Arner, P.,Caro, J. F.,Atkinson, R. L.,Spiegelman, B. M.(1995).Increased adipose tissue expression of tumor necrosis factor-alpha in human obesity and insulin resistance.Journal of Clinical Investigation,95,2409-2415.
  41. Hsu, Y. H.,Venners, S. A.,Terwedow, H. A.,Feng, Y.,Niu, T.,Li, Z.,Xu, X.(2006).Relation of body composition, fat mass, and serum lipids to osteoporotic fractures and bone mineral density in Chinese men and women.American Journal of Clinical Nutrition,83,146-154.
  42. Huang, T. H.,Chang, F. L.,Lin, S. C.,Liu, S. H.,Hsieh, S. S.,Yang, R. S.(2008).Endurance treadmill running training benefits the biomaterial quality of bone in growing male wistar rats.Journal of Bone and Mineral Metabolism,26,350-357.
  43. Huang, T. H.,Lewis, J. L.,Lin, H. S.,Kuo, L. T.,Mao, S. W.,Tai, Y. S.,Yang, R. S.(2014).A methionine-restricted diet and endurance exercise decrease bone mass and extrinsic strength but increase intrinsic strength in growing male rats.Journal of Nutrition,144,621-630.
  44. Huang, T. H.,Lin, S. C.,Chang, F. L.,Hsieh, S. S.,Liu, S. H.,Yang, R. S.(2003).Effects of different exercise modes on mineralization, structure, and biomechanical properties of growing bone.Journal of Applied Physiology,95,300-307.
  45. Jurimae, T.,Soot, T.,Jurimae, J.(2005).Relationships of anthropometrical parameters and body composition with bone mineral content or density in young women with different levels of physical activity.Journal of Physiological Anthropology and Applied Human Science,24,579-587.
  46. Karsenty, G.,Ferron, M.(2012).The contribution of bone to whole-organism physiology.Nature,481,314-320.
  47. Kawai, M.,de Paula, F. J.,Rosen, C. J.(2012).New insights into osteoporosis: The bone-fat connection.Journal of Internal Medicine,272,317-329.
  48. Kemmler, W.,Engelke, K.,Baumann, H.,Beeskow, C.,von Stengel, S.,Weineck, J.,Kalender, W. A.(2006).Bone status in elite male runners.European Journal of Applied Physiology,96,78-85.
  49. Kemmler, W.,Lauber, D.,Weineck, J.,Hensen, J.,Kalender, W.,Engelke, K.(2004).Benefits of 2 years of intense exercise on bone density, physical fitness, and blood lipids in early postmenopausal osteopenic women: Results of the erlangen fitness osteoporosis prevention study (EFOPS).Archives of Internal Medicine,164,1084-1091.
  50. Khan, K.(2001).Physical activity and bone health.Champaign, IL:Human Kinetics.
  51. Knapp, K. M.,Welsman, J. R.,Hopkins, S. J.,Fogelman, I.,Blake, G. M.(2012).Obesity increases precision errors in dual-energy X-ray absorptiometry measurements.Journal of Clinical Densitometry,15,315-319.
  52. Lacombe, J.,Karsenty, G.,Ferron, M.(2013).In vivo analysis of the contribution of bone resorption to the control of glucose metabolism in mice.Molecular Metabolism,2,498-504.
  53. Lane, M. A.,Black, A.,Handy, A. M.,Shapses, S. A.,Tilmont, E. M.,Kiefer, T. L.,Roth, G. S.(2001).Energy restriction does not alter bone mineral metabolism or reproductive cycling and hormones in female rhesus monkeys.Journal of Nutrition,131,820-827.
  54. Lee, N. K.,Sowa, H.,Hinoi, E.,Ferron, M.,Ahn, J. D.,Confavreux, C.,Karsenty, G.(2007).Endocrine regulation of energy metabolism by the skeleton.Cell,130,456-469.
  55. Levinger, I.,Jerums, G.,Stepto, N. K.,Parker, L.,Serpiello, F. R.,McConell, G. K.,Seeman, E..The effect of acute exercise on undercarboxylated osteocalcin and insulin sensitivity in obese men.Journal of Bone and Mineral Research
  56. Levinger, I.,Zebaze, R.,Jerums, G.,Hare, D. L.,Selig, S.,Seeman, E.(2011).The effect of acute exercise on undercarboxylated osteocalcin in obese men.Osteoporosis Internaltional,22,1621-1626.
  57. Liu, J. J.,Toy, W. C.,Wong, M. D.,Tan, C. S.,Tavintharan, S.,Wong, M. S.,Lim, S. C.(2013).Elevated undercarboxylated and reduced carboxylated osteocalcin are associated with metabolic syndrome in middle age Asian females.Experimental and Clinical Endocrinology and Diabetes,121,329-333.
  58. Liu, Z.,Aronson, J.,Wahl, E. C.,Liu, L.,Perrien, D. S.,Kern, P. A.,Lumpkin, C. K., Jr.(2007).A novel rat model for the study of deficits in bone formation in type-2 diabetes.Acta Orthopaedica,78,46-55.
  59. Mardon, J.,Habauzit, V.,Trzeciakiewicz, A.,Davicco, M. J.,Lebecque, P.,Mercier, S.,Coxam, V.(2008).Influence of high and low protein intakes on age-related bone loss in rats submitted to adequate or restricted energy conditions.Calcified Tissue International,82,373-382.
  60. Mattson, M. P.(2012).Evolutionary aspects of human exercise-born to run purposefully.Ageing Research Reviews,11,347-352.
  61. Mattusch, F.,Dufaux, B.,Heine, O.,Mertens, I.,Rost, R.(2000).Reduction of the plasma concentration of C-reactive protein following nine months of endurance training.International Journal of Sports Medicine,21,21-24.
  62. Molfino, A.,Cascino, A.,Conte, C.,Ramaccini, C.,Rossi Fanelli, F.,Laviano, A.(2010).Caloric restriction and L-carnitine administration improves insulin sensitivity in patients with impaired glucose metabolism.Journal of Parenteral and Enteral Nutrition,34,295-299.
  63. Nguyen, T. V.,Sambrook, P. N.,Eisman, J. A.(1998).Bone loss, physical activity, and weight change in elderly women: the Dubbo Osteoporosis Epidemiology Study.Journal of Bone and Mineral Research,13,1458-1467.
  64. NIH Consensus Development Panel on Osteoporosis Prevention, Diagonosis, and Therapy(2001).Osteoporosis prevention, diagnosis, and therapy.Journal of the American Medical Association,285,785-795.
  65. Nowak, A.,Straburzynska-Lupa, A.,Kusy, K.,Zielinski, J.,Felsenberg, D.,Rittweger, J.,Pilaczynska-Szczesniak, L.(2010).Bone mineral density and bone turnover in male masters athletes aged 40-64.Aging Male,13,133-141.
  66. Oberhauser, F.,Schulte, D. M.,Faust, M.,Gudelhofer, H.,Hahn, M.,Muller, N.,Laudes, M.(2012).Weight loss due to a very low calorie diet differentially affects insulin sensitivity and interleukin-6 serum levels in nondiabetic obese human subjects.Hormone and metabolic research,44,465-470.
  67. Petit, M. A.,Paudel, M. L.,Taylor, B. C.,Hughes, J. M.,Strotmeyer, E. S.,Schwartz, A. V.,Osteoporotic Fractures in Men (MrOs) Study Group(2010).Bone mass and strength in older men with type 2 diabetes: The osteoporotic fractures in men study.Journal of Bone and Mineral Research,25,285-291.
  68. Poehlman, E. T.,Toth, M. J.,Gardner, A. W.(1995).Changes in energy balance and body composition at menopause: A controlled longitudinal study.Annals of Internal Medicine,123,673-675.
  69. Polgreen, L. E.,Jacobs, D. R., Jr.,Nathan, B. M.,Steinberger, J.,Moran, A.,Sinaiko, A. R.(2012).Association of osteocalcin with obesity, insulin resistance, and cardiovascular risk factors in young adults.Obesity,20,2194-2201.
  70. Pradhan, A. D.,Manson, J. E.,Rifai, N.,Buring, J. E.,Ridker, P. M.(2001).C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus.Journal of the American Medical Association,286,327-334.
  71. Raichlen, D. A.,Polk, J. D.(2013).Linking brains and brawn: Exercise and the evolution of human neurobiology.Proceeding of the Royal Society B: Biological Sciences,280,20122250-20122258.
  72. Ravn, P.,Cizza, G.,Bjarnason, N. H.,Thompson, D.,Daley, M.,Wasnich, R. D.,Christiansen, C.(1999).Low body mass index is an important risk factor for low bone mass and increased bone loss in early postmenopausal women: Early postmenopausal intervention cohort EPIC study group.Journal of Bone and Mineral Research,14,1622-1627.
  73. Reid, I. R.(2002).Relationships among body mass, its components, and bone.Bone,31,547-555.
  74. Ren, J.(2004).Leptin and hyperleptinemia - from friend to foe for cardiovascular function.Journal of Endocrinology,181,1-10.
  75. Retzepi, M.,Donos, N.(2010).The effect of diabetes mellitus on osseous healing.Clinical Oral Implants Research,21,673-681.
  76. Samjoo, I. A.,Safdar, A.,Hamadeh, M. J.,Raha, S.,Tarnopolsky, M. A.(2013).The effect of endurance exercise on both skeletal muscle and systemic oxidative stress in previously sedentary obese men.Nutrition and Diabetes,3
  77. Schafer, A. L.,Sellmeyer, D. E.,Schwartz, A. V.,Rosen, C. J.,Vittinghoff, E.,Palermo, L.,Black, D. M.(2011).Change in undercarboxylated osteocalcin is associated with changes in body weight, fat mass, and adiponectin: Parathyroid hormone (1-84) or alendronate therapy in postmenopausal women with osteoporosis (the PaTH study).Journal of Clinical Endocrinology and Metabolism,96,1982-1989.
  78. Scofield, K. L.,Hecht, S.(2012).Bone health in endurance athletes: runners, cyclists, and swimmers.Current Sports Medicine Reports,11,328-334.
  79. Shah, K.,Armamento-Villareal, R.,Parimi, N.,Chode, S.,Sinacore, D. R.,Hilton, T. N.,Villareal, D. T.(2011).Exercise training in obese older adults prevents increase in bone turnover and attenuates decrease in hip bone mineral density induced by weight loss despite decline in bone-active hormones.Journal of Bone and Mineral Research,26,2851-2859.
  80. Shapses, S. A.,Sukumar, D.(2012).Bone metabolism in obesity and weight loss.Annual Review of Nutrition,32,287-309.
  81. Shen, C. L.,Zhu, W.,Gao, W.,Wang, S.,Chen, L.,Chyu, M. C.(2013).Energy-restricted diet benefits body composition but degrades bone integrity in middle-aged obese female rats.Nutrition Research,33,668-676.
  82. Sherk, V. D.,Malone, S. P.,Bemben, M. G.,Knehans, A. W.,Palmer, I. J.,Bemben, D. A.(2011).Leptin, fat mass, and bone mineral density in healthy pre-and postmenopausal women.Journal of Clinical Densitometry,14,321-325.
  83. Speakman, J. R.,Mitchell, S. E.(2011).Caloric restriction.Molecular Aspects of Medicne,32,159-221.
  84. Sukumar, D.,Ambia-Sobhan, H.,Zurfluh, R.,Schlussel, Y.,Stahl, T. J.,Gordon, C. L.,Shapses, S. A.(2011).Areal and volumetric bone mineral density and geometry at two levels of protein intake during caloric restriction: A randomized, controlled trial.Journal of Bone and Mineral Research,26,1339-1348.
  85. Takeda, S.,Kobayashi, Y.,Park, J. H.,Ezawa, I.,Omi, N.(2012).Effect of different intake levels of dietary protein and physical exercise on bone mineral density and bone strength in growing male rats.Journal of Nutritional Science and Vitaminology,58,240-246.
  86. Villareal, D. T.,Chode, S.,Parimi, N.,Sinacore, D. R.,Hilton, T.,Armamento-Villareal, R.,Shah, K.(2011).Weight loss, exercise, or both and physical function in obese older adults.New England Journal of Medicine,364,1218-1229.
  87. Villareal, D. T.,Fontana, L.,Weiss, E. P.,Racette, S. B.,Steger-May, K.,Schechtman, K. B.,Holloszy, J. O.(2006).Bone mineral density response to caloric restriction-induced weight loss or exercise-induced weight loss: A randomized controlled trial.Archives of Internal Medicine,166,2502-2510.
  88. Villareal, D. T.,Shah, K.,Banks, M. R.,Sinacore, D. R.,Klein, S.(2008).Effect of weight loss and exercise therapy on bone metabolism and mass in obese older adults: A one-year randomized controlled trial.Journal of Clinical Endocrinology and Metabolism,93,2181-2187.
  89. Weitzmann, M. N.,Pacifici, R.(2006).Estrogen deficiency and bone loss: An inflammatory tale.Journal of Clinical Investigation,116,1186-1194.
  90. Wellen, K. E.,Hotamisligil, G. S.(2005).Inflammation, stress, and diabetes.Journal of Clinical Investigation,115,1111-1119.
  91. Wellen, K. E.,Hotamisligil, G. S.(2003).Obesity-induced inflammatory changes in adipose tissue.Journal of Clinical Investigation,112,1785-1788.
  92. Westerbeek, Z. W.,Hepple, R. T.,Zernicke, R. F.(2008).Effects of aging and caloric restriction on bone structure and mechanical properties.The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences,63,1131-1136.
  93. Yasui, T.,Uemura, H.,Tomita, J.,Miyatani, Y.,Yamada, M.,Miura, M.,Irahara, M.(2006).Association of serum undercarboxylated osteocalcin with serum estradiol in pre-, peri- and early post-menopausal women.Journal of Endocrinological Investigation,29,913-918.
  94. Yoo, E. J.,Jun, T. W.,Hawkins, S. A.(2010).The effects of a walking exercise program on fall-related fitness, bone metabolism, and fall-related psychological factors in elderly women.Research in Sports Medicine,18,236-250.
  95. Yu, E. W.,Bouxsein, M. L.,Roy, A. E.,Baldwin, C.,Cange, A.,Neer, R. M.,Finkelstein, J. S.(2014).Bone loss after bariatric surgery: Discordant results between DXA and QCT bone density.Journal of Bone and Mineral Research,29,542-550.
  96. Zerath, E.,Holy, X.,Douce, P.,Guezennec, C. Y.,Chatard, J. C.(1997).Effect of endurance training on postexercise parathyroid hormone levels in elderly men.Medicine and Science in Sports Exercise,29,1139-1145.