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Beneficial impact of exercise on bone mass in individuals under calorie restriction: a systematic review and Meta-analysis of randomized clinical trials

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  • Andersen, R. E., T. A. Wadden, and R. J. Herzog. 1997. Changes in bone mineral content in obese dieting women. Metabolism-Clinical and Experimental 46:857–61. doi: 10.1016/S0026-0495(97)90070-6.
  • Azuma, Y., K. Kaji, R. Katogi, S. Takeshita, and A. Kudo. 2000. Tumor necrosis factor-α induces differentiation of and bone resorption by osteoclasts. Journal of Biological Chemistry 275:4858–64. doi: 10.1074/jbc.275.7.4858.
  • Beavers, D. P., K. M. Beavers, R. F. Loeser, N. R. Walton, M. F. Lyles, B. J. Nicklas, S. A. Shapses, J. J. Newman, and S. P. Messier. 2014. The independent and combined effects of intensive weight loss and exercise training on bone mineral density in overweight and obese older adults with osteoarthritis. Osteoarthritis and cartilage 22:726–33. doi: 10.1016/j.joca.2014.04.002.
  • Beavers, K. M., D. P. Beavers, S. B. Martin, A. P. Marsh, M. F. Lyles, L. Lenchik, S. A. Shapses, and B. J. Nicklas. 2017. Change in bone mineral density during weight loss with resistance versus aerobic exercise training in older adults. The Journals of Gerontology: Series A 72 (11):1582–5. doi: 10.1093/gerona/glx048.
  • Beavers, K. M., M. P. Walkup, A. A. Weaver, L. Lenchik, S. B. Kritchevsky, B. J. Nicklas, W. J. Ambrosius, J. Stitzel, T. C. Register, and S. A. Shapses. 2018. Effect of exercise modality during weight loss on bone health in older adults with obesity and cardiovascular disease or metabolic syndrome: a randomized controlled trial. Journal of Bone and Mineral Research 33: 2140–49. doi: 10.1002/jbmr.3555.
  • Bosy‐Westphal, A., W. Later, B. Schautz, M. Lagerpusch, K. Goele, M. Heller, C. C. Glüer, and M. J. Müller. 2011. Impact of intra‐and extra‐osseous soft tissue composition on changes in bone mineral density with weight loss and regain. Obesity 19:1503–10. doi: 10.1038/oby.2011.40.
  • Chao, D., M. A. Espeland, D. Farmer, T. C. Register, L. Lenchik, W. B. Applegate, and W. H. Ettinger. Jr, 2000. Effect of voluntary weight loss on bone mineral density in older overweight women. Journal of the American Geriatrics Society 48 (7):753–9. doi: 10.1111/j.1532-5415.2000.tb04749.x.
  • Daly, R. M., D. W. Dunstan, N. Owen, D. Jolley, J. E. Shaw, and P. Z. Zimmet. 2005. Does high-intensity resistance training maintain bone mass during moderate weight loss in older overweight adults with type 2 diabetes? Osteoporosis International. 16:1703–12. doi: 10.1007/s00198-005-1906-4.
  • Engelke, K., W. Kemmler, D. Lauber, C. Beeskow, R. Pintag, and W. Kalender. 2006. Exercise maintains bone density at spine and hip EFOPS: A 3-year longitudinal study in early postmenopausal women. Osteoporosis International 17:133–42. doi: 10.1007/s00198-005-1938-9.
  • Ensrud, K. E., J. Cauley, R. Lipschutz, and S. R. Cummings. 1997. Weight change and fractures in older women. Archives of Internal Medicine 157 (8):857–63. doi: 10.1001/archinte.1997.00440290041004.
  • Ensrud, K. E., S. K. Ewing, K. L. Stone, J. A. Cauley, P. J. Bowman, S. R. Cummings, and Group, S. o. O. F. R. 2003. Intentional and unintentional weight loss increase bone loss and hip fracture risk in older women. Journal of the American Geriatrics Society 51 (12):1740–7. doi: 10.1046/j.1532-5415.2003.51558.x.
  • Ensrud, K. E., R. L. Fullman, E. Barrett-Connor, J. A. Cauley, M. L. Stefanick, H. A. Fink, C. E. Lewis, and E. Orwoll. 2005. Voluntary weight reduction in older men increases hip bone loss: The osteoporotic fractures in men study. The Journal of Clinical Endocrinology & Metabolism 90:1998–2004. doi: 10.1210/jc.2004-1805.
  • Fassio, A., L. Idolazzi, M. Rossini, D. Gatti, G. Adami, A. Giollo, and O. Viapiana. 2018. The obesity paradox and osteoporosis. Eating and Weight Disorders - Studies on Anorexia, Bulimia and Obesity 23 (3):293–302. doi: 10.1007/s40519-018-0505-2.
  • Fleg, J. L. 2012. Aerobic exercise in the elderly: A key to successful aging. Discovery Medicine 13 (70):223–8.
  • Formiguera, X., and A. Cantón. 2004. Obesity: Epidemiology and clinical aspects. Best Practice & Research Clinical Gastroenterology 18:1125–46. doi: 10.1016/S1521-6918(04)00091-5.
  • Fried, S. K., D. A. Bunkin, and A. S. Greenberg. 1998. Omental and subcutaneous adipose tissues of obese subjects release interleukin-6: Depot difference and regulation by glucocorticoid. Journal of Clinical Endocrinology & Metabolism 83:847–50. doi: 10.1210/jc.83.3.847.
  • Goff, S. L., M. L. Unruh, J. Klingensmith, N. D. Eneanya, C. Garvey, M. J. Germain, and L. M. Cohen. 2019. Advance care planning with patients on hemodialysis: An implementation study. BMC Palliative Care 18 (1):64. doi: 10.1186/s12904-019-0437-2.
  • Hemenway, D., G. A. Colditz, W. C. Willett, M. J. Stampfer, and F. E. Speizer. 1988. Fractures and lifestyle: Effect of cigarette smoking, alcohol intake, and relative weight on the risk of hip and forearm fractures in middle-aged women. American Journal of Public Health 78 (12):1554–8. doi: 10.2105/AJPH.78.12.1554.
  • Higgins, J. P., D. G. Altman, P. C. Gøtzsche, P. Jüni, D. Moher, A. D. Oxman, J. Savović, K. F. Schulz, L. Weeks, and J. A. Sterne. 2011. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ 343 (oct18 2):d5928–d5928., doi: 10.1136/bmj.d5928.
  • Hosny, I. A., H. S. Elghawabi, W. B. F. Younan, A. A. Sabbour, and M. A. M. Gobrial. 2012. Beneficial impact of aerobic exercises on bone mineral density in obese premenopausal women under caloric restriction. Skeletal radiology 41:423–27. doi: 10.1007/s00256-011-1196-1.
  • Jensen, M., D. Ryan, C. Apovian, J. Ard, A. Comuzzie, and K. Donato. 2014. American college of cardiology/American heart association task force on practice guidelines; obesity society. 2013 AHA/ACC/TOS guideline for the management of overweight and obesity in adults: A report of the American college of cardiology/American heart association task force on practice guidelines and the obesity society. Circulation 129:S102–S138. doi: 10.1161/01.cir.0000437739.71477.ee.
  • Jiang, B. C., and D. T. Villareal. 2019. Weight loss-induced reduction of bone mineral density in older adults with obesity. Journal of Nutrition in Gerontology and Geriatrics 38 (1):100–14. doi: 10.1080/21551197.2018.1564721.
  • Jilka, R. 1998. Cytokines, bone remodeling, and estrogen deficiency: A 1998 update. Bone 23 (2):75–81. doi: 10.1016/s8756-3282(98)00077-5.
  • Justesen, J., K. Stenderup, E. Ebbesen, L. Mosekilde, T. Steiniche, and M. Kassem. 2001. Adipocyte tissue volume in bone marrow is increased with aging and in patients with osteoporosis. Biogerontology 2 (3):165–71.
  • Kelleher, J. L., D. P. Beavers, R. M. Henderson, D. Yow, C. Crotts, J. Kiel, B. J. Nicklas, and K. M. Beavers. 2017. Weighted vest use during dietary weight loss on bone health in older adults with obesity. Journal of Osteoporosis and Physical Activity 5 (4):210. doi: 10.4172/2329-9509.1000210.
  • Kemmler, W., K. Engelke, D. Lauber, J. Weineck, J. Hensen, and W. A. Kalender. 2002. Exercise effects on fitness and bone mineral density in early postmenopausal women: 1-year EFOPS results. Medicine & Science in Sports & Exercise 34 (12):2115–23. doi: 10.1097/00005768-200212000-00038.
  • Khosla, S., M. J. Oursler, and D. G. Monroe. 2012. Estrogen and the skeleton. Trends in Endocrinology & Metabolism 23:576–81. doi: 10.1016/j.tem.2012.03.008.
  • Khosla, S., and B. L. Riggs. 2005. Pathophysiology of age-related bone loss and osteoporosis. Endocrinology and Metabolism Clinics of North America 34 (4):1015–30. doi: 10.1016/j.ecl.2005.07.009.
  • Knoke, J. D., and E. Barrett-Connor. 2003. Weight loss: A determinant of hip bone loss in older men and women: The Rancho Bernardo Study. American Journal of Epidemiology 158:1132–8. doi: 10.1093/aje/kwg265.
  • Kreiger, N., J. L. Kelsey, T. R. Holford, and T. O’Connor. 1982. An epidemiologic study of hip fracture in postmenopausal women. American Journal of Epidemiology 116:141–8. doi: 10.1093/oxfordjournals.aje.a113388.
  • Kukuljan, S., C. Nowson, S. Bass, K. Sanders, G. Nicholson, M. Seibel, J. Salmon, and R. Daly. 2009. Effects of a multi-component exercise program and calcium-vitamin-D 3-fortified milk on bone mineral density in older men: A randomised controlled trial. Osteoporosis International 20:1241–51. doi: 10.1007/s00198-008-0776-y.
  • Ma, D., L. Wu, and Z. He. 2013. Effects of walking on the preservation of bone mineral density in perimenopausal and postmenopausal women: A systematic review and meta-analysis. Menopause 20:1216–26. doi: 10.1097/GME.0000000000000100.
  • Marques, E. A., J. Mota, and J. Carvalho. 2012. Exercise effects on bone mineral density in older adults: A meta-analysis of randomized controlled trials. Age 34 (6):1493–515. doi: 10.1007/s11357-011-9311-8.
  • Martyn-St James, M., and S. Carroll. 2009. A meta-analysis of impact exercise on postmenopausal bone loss: The case for mixed loading exercise programmes. British Journal of Sports Medicine 43:898–908. doi: 10.1136/bjsm.2008.052704.
  • Mohamed-Ali, V., S. Goodrick, A. Rawesh, D. Katz, J. Miles, J. Yudkin, S. Klein, and S. Coppack. 1997. Subcutaneous adipose tissue releases interleukin-6, but not tumor necrosis factor-α, in vivo. The Journal of Clinical Endocrinology & Metabolism 82:4196–200. doi: 10.1210/jcem.82.12.4450.
  • Nakata, Y., K. Ohkawara, D. J. Lee, T. Okura, and K. Tanaka. 2008. Effects of additional resistance training during diet-induced weight loss on bone mineral density in overweight premenopausal women. Journal of bone and mineral metabolism 26:172–77. doi: 10.1007/s00774-007-0805-5.
  • Ramsdale, S., and E. Bassey. 1994. Changes in bone mineral density associated with dietary-induced loss of body mass in young women. Clinical Science 87:343–8. doi: 10.1042/cs0870343.
  • Redman, L. M., J. Rood, S. D. Anton, C. Champagne, S. R. Smith, and E. Ravussin. 2008. Calorie restriction and bone health in young, overweight individuals. Archives of internal medicine 168:1859–66. doi: 10.1001/archinte.168.17.1859.
  • Riggs, B. L., L. J. Melton, R. A. Robb, J. J. Camp, E. J. Atkinson, J. M. Peterson, P. A. Rouleau, C. H. McCollough, M. L. Bouxsein, S. Khosla, et al. 2004. Population-based study of age and sex differences in bone volumetric density, size, geometry, and structure at different skeletal sites. Journal of Bone and Mineral Research 19 (12):1945–54. doi: 10.1359/jbmr.040916.
  • Riggs, B. L. 2000. The mechanisms of estrogen regulation of bone resorption. Journal of Clinical Investigation 106:1203–4. doi: 10.1172/JCI11468.
  • Roy, B., M. E. Curtis, L. S. Fears, S. N. Nahashon, and H. M. Fentress. 2016. Molecular mechanisms of obesity-induced osteoporosis and muscle atrophy. Frontiers in Physiology 7:439. doi: 10.3389/fphys.2016.00439.
  • Ryan, A. S., B. J. Nicklas, and K. E. Dennis. 1998. Aerobic exercise maintains regional bone mineral density during weight loss in postmenopausal women. Journal of Applied Physiology 84:1305–10. doi: 10.1152/jappl.1998.84.4.1305.
  • Santanasto, A. J., N. W. Glynn, M. A. Newman, C. A. Taylor, M. M. Brooks, B. H. Goodpaster, and A. B. Newman. 2010. Impact of weight loss on physical function with changes in strength, muscle mass, and muscle fat infiltration in overweight to moderately obese older adults: A randomized clinical trial. Journal of Obesity 10:516–576. doi: 10.1155/2011/516576.
  • Shah, K., R. Armamento‐Villareal, N. Parimi, S. Chode, D. R. Sinacore, T. N. Hilton, N. Napoli, C. Qualls, and D. T. Villareal. 2011a. 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 (12):2851–9. doi: 10.1002/jbmr.475.
  • Shah, M., P. G. Snell, S. Rao, B. Adams‐Huet, C. Quittner, E. H. Livingston, and A. Garg. 2011. High‐volume exercise program in obese bariatric surgery patients: A randomized, controlled trial. Obesity 19 (9):1826–34. doi: 10.1038/oby.2011.172.
  • Shapses, S. A., and D. Sukumar. 2012. Bone metabolism in obesity and weight loss. Annual Review of Nutrition 32 (1):287–309. doi: 10.1146/annurev.nutr.012809.104655.
  • Silverman, N. E., B. J. Nicklas, and A. S. Ryan. 2009. Addition of aerobic exercise to a weight loss program increases BMD, with an associated reduction in inflammation in overweight postmenopausal women. Calcified Tissue International. 84:257–65. doi: 10.1007/s00223-009-9232-z.
  • Smith, A. J., W. R. Phipps, W. Thomas, K. H. Schmitz, and M. S. Kurzer. 2013. The effects of aerobic exercise on estrogen metabolism in healthy premenopausal women. Cancer Epidemiology Biomarkers & Prevention 22 (5):756–64. doi: 10.1158/1055-9965.EPI-12-1325.
  • Soltani, S., G. Hunter, A. Kazemi, and S. Shab-Bidar. 2016. The effects of weight loss approaches on bone mineral density in adults: A systematic review and meta-analysis of randomized controlled trials. Osteoporosis International 27 (9):2655–71. doi: 10.1007/s00198-016-3617-4.
  • Suda, T., N. Takahashi, and T. J. Martin. 1992. Modulation of osteoclast differentiation. Endocrine Reviews 13:66–80. doi: 10.1210/edrv-13-1-66.
  • Svendsen, O. L., C. Hassager, and C. Christiansen. 1993. Effect of an energy-restrictive diet, with or without exercise, on lean tissue mass, resting metabolic rate, cardiovascular risk factors, and bone in overweight postmenopausal women. The American journal of medicine 95:131–140. doi: 10.1016/0002-9343(93)90253-L.
  • Tabata, Y., and Y. Ikada. 1988. Macrophage phagocytosis of biodegradable microspheres composed of L‐lactic acid/glycolic acid homo‐and copolymers. Journal of Biomedical Materials Research 22 (10):837–58. doi: 10.1002/jbm.820221002.
  • Tang, D., R. D. Kamm, C. Yang, J. Zheng, G. Canton, R. Bach, X. Huang, T. S. Hatsukami, J. Zhu, G. Ma, et al. 2014. Image-based modeling for better understanding and assessment of atherosclerotic plaque progression and vulnerability: Data, modeling, validation, uncertainty and predictions. Journal of Biomechanics 47 (4):834–46., doi: 10.1016/j.jbiomech.2014.01.012.
  • Tella, S. H., and J. C. Gallagher. 2014. Prevention and treatment of postmenopausal osteoporosis. The Journal of Steroid Biochemistry and Molecular Biology 142:155–70. doi: 10.1016/j.jsbmb.2013.09.008.
  • Villareal, D. T., S. Chode, N. Parimi, D. R. Sinacore, T. Hilton, R. Armamento-Villareal, N. Napoli, C. Qualls, and K. Shah. 2011. Weight loss, exercise, or both and physical function in obese older adults. New England Journal of Medicine 364:1218–29. doi: 10.1056/NEJMoa1008234.
  • Villareal, D. T., K. Shah, M. R. Banks, D. R. Sinacore, and S. Klein. 2008. Effect of weight loss and exercise therapy on bone metabolism and mass in obese older adults: A one-year randomized controlled trial. The Journal of Clinical Endocrinology & Metabolism 93:2181–7. doi: 10.1210/jc.2007-1473.
  • Warden, S., R. Fuchs, and C. Turner. 2004. Steps for targeting exercise towards the skeleton to increase bone strength. Europa Medicophysica 40 (3):223–32.
  • Weiss, E. P., R. C. Jordan, E. M. Frese, S. G. Albert, and D. T. Villareal. 2017. Effects of weight loss on lean mass, strength, bone, and aerobic capacity. Medicine and Science in Sports and Exercise 49:206. doi: 10.1249/MSS.0000000000001074.
  • Welch, G., C. Wesolowski, S. Zagarins, J. Kuhn, J. Romanelli, J. Garb, and N. Allen. 2011. Evaluation of clinical outcomes for gastric bypass surgery: Results from a comprehensive follow-up study. Obesity Surgery 21 (1):18–28. doi: 10.1007/s11695-009-0069-3.
  • Winters-Stone, K. M., M. C. Leo, and A. Schwartz. 2012. Exercise effects on hip bone mineral density in older, post-menopausal breast cancer survivors are age dependent. Archives of Osteoporosis 7:301–6. doi: 10.1007/s11657-012-0071-6.
  • Wyatt, S. B., K. P. Winters, and P. M. Dubbert. 2006. Overweight and obesity: Prevalence, consequences, and causes of a growing public health problem. J. T. A. j. o. t. m. s 331:166–74.
  • Xiao, C. m., Y. Kang, and Y. C. Zhuang. 2016. Effects of elastic resistance band exercise on postural balance, estrogen, bone metabolism index, and muscle strength of perimenopausal period women. Journal of the American Geriatrics Society 64:1368–70. doi: 10.1111/jgs.14172.
  • Zbranca, E., B. Galusca, and V. Mogos. 2004. Bone mineral densitometry. The importance of BMD in endocrinologist practice. Timisoara Med. J 3:260–7.
  • Zhao, R., M. Zhang, and Q. Zhang. 2017. The effectiveness of combined exercise interventions for preventing postmenopausal bone loss: A systematic review and meta-analysis. Journal of Orthopaedic & Sports Physical Therapy 47:241–51. doi: 10.2519/jospt.2017.6969.
  • Zibellini, J., R. V. Seimon, C. M. Lee, A. A. Gibson, M. S. Hsu, S. A. Shapses, T. V. Nguyen, and A. Sainsbury. 2015. Does diet‐induced weight loss lead to bone loss in overweight or obese adults? A systematic review and meta‐analysis of clinical trials. Journal of Bone and Mineral Research 30 (12):2168–78. doi: 10.1002/jbmr.2564.

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