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Body Weight/Composition and Weight Change: Effects on Bone Health

  • Sue A. ShapsesEmail author
  • Mariana Cifuentes
Chapter
Part of the Nutrition and Health book series (NH)

Abstract

A low body weight in older individuals is a major risk factor for fracture, and the maintenance of weight can prevent bone loss. Notwithstanding the above, newer information shows that obesity alters bone quality and is not always protective against osteoporosis and fracture, as previously thought. Weight reduction will have a different impact on bone, depending on the amount and whether it is involuntary or voluntary. Although mechanisms regulating bone loss are uncertain, it is clear that the method to achieve voluntary weight reduction (through different diets, medication, or increasing levels of activity) will determine the bone response. In addition, extreme weight loss due to bariatric surgery leads to bone loss and the long-term implications are discussed. Finally, alterations in bone quality and strength parameters due to weight reduction and regain suggest that bone lost is not recovered.

Keywords

Body composition Body weight Bone Fracture risk Weight loss 

Notes

Acknowledgements

Supported by NIH-AG12161. We would like to thank Brian Chang, BS, for his careful review and editorial assistance in preparing this manuscript.

References

  1. 1.
    Flegal KM, Carroll MD, Kit BK, Ogden CL. Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999–2010. JAMA. 2012;307(5):491–7.PubMedGoogle Scholar
  2. 2.
    Must A, Jacques PF, Dallal GE, Bajema CJ, Dietz WH. Long-term morbidity and mortality of overweight adolescents. A follow-up of the Harvard Growth Study of 1922 to 1935. N Engl J Med. 1922;327(19):1350–5.Google Scholar
  3. 3.
    Goulding A, Jones IE, Taylor RW, Williams SM, Manning PJ. Bone mineral density and body composition in boys with distal forearm fractures: a dual-energy x-ray absorptiometry study. J Pediatr. 2001;139(4):509–15.PubMedGoogle Scholar
  4. 4.
    Holmberg AH, Johnell O, Nilsson PM, Nilsson J, Berglund G, Akesson K. Risk factors for fragility fracture in middle age. A prospective population-based study of 33,000 men and women. Osteoporos Int. 2006;17(7):1065–77.PubMedGoogle Scholar
  5. 5.
    Shapses SA, Sukumar D. Bone metabolism in obesity and weight loss. Annu Rev Nutr. 2012;32:287–309.PubMedCentralPubMedGoogle Scholar
  6. 6.
    Albala C, Yanez M, Devoto E, Sostin C, Zeballos L, Santos JL. Obesity as a protective factor for postmenopausal osteoporosis. Int J Obes Relat Metab Disord. 1996;20(11):1027–32.PubMedGoogle Scholar
  7. 7.
    Cifuentes M, Johnson MA, Lewis RD, Heymsfield SB, Chowdhury HA, Modlesky CM, et al. Bone turnover and body weight relationships differ in normal-weight compared with heavier postmenopausal women. Osteoporos Int. 2003;14(2):116–22.PubMedCentralPubMedGoogle Scholar
  8. 8.
    Reid IR, Ames R, Evans MC, Sharpe S, Gamble G, France JT, et al. Determinants of total body and regional bone mineral density in normal postmenopausal women—a key role for fat mass. J Clin Endocrinol Metab. 1992;75(1):45–51.PubMedGoogle Scholar
  9. 9.
    Sukumar D, Schlussel Y, Riedt CS, Gordon C, Stahl T, Shapses SA. Obesity alters cortical and trabecular bone density and geometry in women. Osteoporos Int. 2011;22(2):635–45.PubMedCentralPubMedGoogle Scholar
  10. 10.
    Nielson CM, Marshall LM, Adams AL, Leblanc ES, Cawthon PM, Ensrud K, et al. BMI and fracture risk in older men: the osteoporotic fractures in men study (MrOS). J Bone Miner Res. 2011;26(3):496–502.PubMedCentralPubMedGoogle Scholar
  11. 11.
    Premaor MO, Pilbrow L, Tonkin C, Parker RA, Compston J. Obesity and fractures in postmenopausal women. J Bone Miner Res. 2010;25(2):292–7.PubMedGoogle Scholar
  12. 12.
    Bjorntorp P. The regulation of adipose tissue distribution in humans. Int J Obes Relat Metab Disord. 1996;20(4):291–302.PubMedGoogle Scholar
  13. 13.
    Pedersen SB, Hansen PS, Lund S, Andersen PH, Odgaard A, Richelsen B. Identification of oestrogen receptors and oestrogen receptor mRNA in human adipose tissue. Eur J Clin Invest. 1996;26(4):262–9.PubMedGoogle Scholar
  14. 14.
    Shiraki M, Ito H, Fujimaki H, Higuchi T. Relation between body size and bone mineral density with special reference to sex hormones and calcium regulating hormones in elderly females. Endocrinol Jpn. 1991;38(4):343–9.PubMedGoogle Scholar
  15. 15.
    Bell NH, Epstein S, Greene A, Shary J, Oexmann MJ, Shaw S. Evidence for alteration of the vitamin D-endocrine system in obese subjects. J Clin Invest. 1985;76(1):370–3.PubMedCentralPubMedGoogle Scholar
  16. 16.
    Bolland MJ, Grey AB, Ames RW, Horne AM, Gamble GD, Reid IR. Fat mass is an important predictor of parathyroid hormone levels in postmenopausal women. Bone. 2006;38(3):317–21.PubMedGoogle Scholar
  17. 17.
    Pitroda AP, Harris SS, Dawson-Hughes B. The association of adiposity with parathyroid hormone in healthy older adults. Endocrine. 2009;36(2):218–23.PubMedCentralPubMedGoogle Scholar
  18. 18.
    Wortsman J, Matsuoka LY, Chen TC, Lu Z, Holick MF. Decreased bioavailability of vitamin D in obesity. Am J Clin Nutr. 2000;72(3):690–3.PubMedGoogle Scholar
  19. 19.
    Drincic AT, Armas LA, Van Diest EE, Heaney RP. Volumetric dilution, rather than sequestration best explains the low vitamin D status of obesity. Obesity (Silver Spring). 2012;20(7):1444–8.Google Scholar
  20. 20.
    Rajakumar K, de Las HJ, Chen TC, Lee S, Holick MF, Arslanian SA. Vitamin D status, adiposity, and lipids in black American and Caucasian children. J Clin Endocrinol Metab. 2011;96(5):1560–7.PubMedCentralPubMedGoogle Scholar
  21. 21.
    Blum M, Dallal GE, Dawson-Hughes B. Body size and serum 25 hydroxy vitamin D response to oral supplements in healthy older adults. J Am Coll Nutr. 2008;27(2):274–9.PubMedCentralPubMedGoogle Scholar
  22. 22.
    Scragg R, Holdaway I, Singh V, Metcalf P, Baker J, Dryson E. Serum 25-hydroxyvitamin D3 is related to physical activity and ethnicity but not obesity in a multicultural workforce. Aust N Z J Med. 1995;25(3):218–23.PubMedGoogle Scholar
  23. 23.
    Klein KO, Larmore KA, de Lancey E, Brown JM, Considine RV, Hassink SG. Effect of obesity on estradiol level, and its relationship to leptin, bone maturation, and bone mineral density in children. J Clin Endocrinol Metab. 1998;83(10):3469–75.PubMedGoogle Scholar
  24. 24.
    De SM, Farello G, Palumbo M, Gentile T, Ciuffreda M, Olioso P, et al. Growth charts, growth velocity and bone development in childhood obesity. Int J Obes Relat Metab Disord. 1995;19(12):851–7.Google Scholar
  25. 25.
    Goulding A, Taylor RW, Jones IE, McAuley KA, Manning PJ, Williams SM. Overweight and obese children have low bone mass and area for their weight. Int J Obes Relat Metab Disord. 2000;24(5):627–32.PubMedGoogle Scholar
  26. 26.
    Woo DG, Lee BY, Lim D, Kim HS. Relationship between nutrition factors and osteopenia: effects of experimental diets on immature bone quality. J Biomech. 2009;42(8):1102–7.PubMedGoogle Scholar
  27. 27.
    Patsch JM, Kiefer FW, Varga P, Pail P, Rauner M, Stupphann D, et al. Increased bone resorption and impaired bone microarchitecture in short-term and extended high-fat diet-induced obesity. Metabolism. 2011;60(2):243–9.PubMedGoogle Scholar
  28. 28.
    Cao JJ, Sun L, Gao H. Diet-induced obesity alters bone remodeling leading to decreased femoral trabecular bone mass in mice. Ann N Y Acad Sci. 2010;1192:292–7.PubMedGoogle Scholar
  29. 29.
    Ducher G, Bass SL, Naughton GA, Eser P, Telford RD, Daly RM. Overweight children have a greater proportion of fat mass relative to muscle mass in the upper limbs than in the lower limbs: implications for bone strength at the distal forearm. Am J Clin Nutr. 2009;90(4):1104–11.PubMedGoogle Scholar
  30. 30.
    Pollock NK, Laing EM, Baile CA, Hamrick MW, Hall DB, Lewis RD. Is adiposity advantageous for bone strength? A peripheral quantitative computed tomography study in late adolescent females. Am J Clin Nutr. 2007;86(5):1530–8.PubMedGoogle Scholar
  31. 31.
    Pollock NK, Bernard PJ, Gutin B, Davis CL, Zhu H, Dong Y. Adolescent obesity, bone mass, and cardiometabolic risk factors. J Pediatr. 2011;158(5):727–34.PubMedCentralPubMedGoogle Scholar
  32. 32.
    Dimitri P, Wales JK, Bishop N. Fat and bone in children: differential effects of obesity on bone size and mass according to fracture history. J Bone Miner Res. 2010;25(3):527–36.PubMedGoogle Scholar
  33. 33.
    Dimitri P, Bishop N, Walsh JS, Eastell R. Obesity is a risk factor for fracture in children but is protective against fracture in adults: a paradox. Bone. 2012;50(2):457–66.PubMedGoogle Scholar
  34. 34.
    Rana AR, Michalsky MP, Teich S, Groner JI, Caniano DA, Schuster DP. Childhood obesity: a risk factor for injuries observed at a level-1 trauma center. J Pediatr Surg. 2009;44(8):1601–5.PubMedCentralPubMedGoogle Scholar
  35. 35.
    Goulding A, Jones IE, Taylor RW, Piggot JM, Taylor D. Dynamic and static tests of balance and postural sway in boys: effects of previous wrist bone fractures and high adiposity. Gait Posture. 2003;17(2):136–41.PubMedGoogle Scholar
  36. 36.
    Cole ZA, Harvey NC, Kim M, Ntani G, Robinson SM, Inskip HM, et al. Increased fat mass is associated with increased bone size but reduced volumetric density in pre pubertal children. Bone. 2012;50(2):562–7.PubMedCentralPubMedGoogle Scholar
  37. 37.
    Nguyen TV, Howard GM, Kelly PJ, Eisman JA. Bone mass, lean mass, and fat mass: same genes or same environments? Am J Epidemiol. 1998;147(1):3–16.PubMedGoogle Scholar
  38. 38.
    Sigurdsson G, Halldorsson BV, Styrkarsdottir U, Kristjansson K, Stefansson K. Impact of genetics on low bone mass in adults. J Bone Miner Res. 2008;23(10):1584–90.PubMedGoogle Scholar
  39. 39.
    Brown LB, Streeten EA, Shapiro JR, McBride D, Shuldiner AR, Peyser PA, et al. Genetic and environmental influences on bone mineral density in pre- and post-menopausal women. Osteoporos Int. 2005;16(12):1849–56.PubMedCentralPubMedGoogle Scholar
  40. 40.
    Dawson-Hughes B, Shipp C, Sadowski L, Dallal G. Bone density of the radius, spine, and hip in relation to percent of ideal body weight in postmenopausal women. Calcif Tissue Int. 1987;40(6):310–4.PubMedGoogle Scholar
  41. 41.
    van der Voort DJ, Geusens PP, Dinant GJ. Risk factors for osteoporosis related to their outcome: fractures. Osteoporos Int. 2001;12(8):630–8.PubMedGoogle Scholar
  42. 42.
    Burckhardt P, Wynn E, Krieg MA, Bagutti C, Faouzi M. The effects of nutrition, puberty and dancing on bone density in adolescent ballet dancers. J Dance Med Sci. 2011;15(2):51–60.PubMedGoogle Scholar
  43. 43.
    Waldron-Lynch F, Murray BF, Brady JJ, McKenna MJ, McGoldrick A, Warrington G, et al. High bone turnover in Irish professional jockeys. Osteoporos Int. 2010;21(3):521–5.PubMedGoogle Scholar
  44. 44.
    Galusca B, Zouch M, Germain N, Bossu C, Frere D, Lang F, et al. Constitutional thinness: unusual human phenotype of low bone quality. J Clin Endocrinol Metab. 2008;93(1):110–7.PubMedGoogle Scholar
  45. 45.
    Zhang HC, Kushida K, Atsumi K, Kin K, Nagano A. Effects of age and menopause on spinal bone mineral density in Japanese women: a ten-year prospective study. Calcif Tissue Int. 2002;70(3):153–7.PubMedGoogle Scholar
  46. 46.
    Ravn P, Cizza G, Bjarnason NH, Thompson D, Daley M, Wasnich RD, et al. 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. J Bone Miner Res. 1999;14(9):1622–7.PubMedGoogle Scholar
  47. 47.
    De Laet C, Kanis JA, Oden A, Johanson H, Johnell O, Delmas P, et al. Body mass index as a predictor of fracture risk: a meta-analysis. Osteoporos Int. 2005;16(11):1330–8.PubMedGoogle Scholar
  48. 48.
    Espallargues M, Sampietro-Colom L, Estrada MD, Sola M, Del RL, Setoain J, et al. Identifying bone-mass-related risk factors for fracture to guide bone densitometry measurements: a systematic review of the literature. Osteoporos Int. 2001;12(10):811–22.PubMedGoogle Scholar
  49. 49.
    El MA, Rezqi A, Mounach A, Achemlal L, Bezza A, Ghozlani I. Systematic vertebral fracture assessment in asymptomatic postmenopausal women. Bone. 2013;52(1):176–80.Google Scholar
  50. 50.
    Corbeil P, Simoneau M, Rancourt D, Tremblay A, Teasdale N. Increased risk for falling associated with obesity: mathematical modeling of postural control. IEEE Trans Neural Syst Rehabil Eng. 2001;9(2):126–36.PubMedGoogle Scholar
  51. 51.
    Spaine LA, Bollen SR. ‘The bigger they come …’: the relationship between body mass index and severity of ankle fractures. Injury. 1996;27(10):687–9.PubMedGoogle Scholar
  52. 52.
    Douchi T, Yamamoto S, Oki T, Maruta K, Kuwahata R, Yamasaki H, et al. Difference in the effect of adiposity on bone density between pre- and postmenopausal women. Maturitas. 2000;34(3):261–6.PubMedGoogle Scholar
  53. 53.
    Lindsay R, Cosman F, Herrington BS, Himmelstein S. Bone mass and body composition in normal women. J Bone Miner Res. 1992;7(1):55–63.PubMedGoogle Scholar
  54. 54.
    Chen Z, Lohman TG, Stini WA, Ritenbaugh C, Aickin M. Fat or lean tissue mass: which one is the major determinant of bone mineral mass in healthy postmenopausal women? J Bone Miner Res. 1997;12(1):144–51.PubMedGoogle Scholar
  55. 55.
    Grabowski DC, Ellis JE. High body mass index does not predict mortality in older people: analysis of the Longitudinal Study of Aging. J Am Geriatr Soc. 2001;49(7):968–79.PubMedGoogle Scholar
  56. 56.
    Muruganandan S, Roman AA, Sinal CJ. Adipocyte differentiation of bone marrow-derived mesenchymal stem cells: cross talk with the osteoblastogenic program. Cell Mol Life Sci. 2009;66(2):236–53.PubMedGoogle Scholar
  57. 57.
    Abdallah BM, Kassem M. New factors controlling the balance between osteoblastogenesis and adipogenesis. Bone. 2012;50(2):540–5.PubMedGoogle Scholar
  58. 58.
    Kang S, Bennett CN, Gerin I, Rapp LA, Hankenson KD, Macdougald OA. Wnt signaling stimulates osteoblastogenesis of mesenchymal precursors by suppressing CCAAT/enhancer-binding protein alpha and peroxisome proliferator-activated receptor gamma. J Biol Chem. 2007;282(19):14515–24.PubMedGoogle Scholar
  59. 59.
    Gimble JM, Zvonic S, Floyd ZE, Kassem M, Nuttall ME. Playing with bone and fat. J Cell Biochem. 2006;98(2):251–66.PubMedGoogle Scholar
  60. 60.
    Margolis KL, Ensrud KE, Schreiner PJ, Tabor HK. Body size and risk for clinical fractures in older women. Study of Osteoporotic Fractures Research Group. Ann Intern Med. 2000;133(2):123–7.PubMedGoogle Scholar
  61. 61.
    Kawai M, Rosen CJ. PPARgamma: a circadian transcription factor in adipogenesis and osteogenesis. Nat Rev Endocrinol. 2010;6(11):629–36.PubMedCentralPubMedGoogle Scholar
  62. 62.
    Bazelier MT, de Vries F, Vestergaard P, Herings RM, Gallagher AM, Leufkens HG, et al. Risk of fracture with thiazolidinediones: an individual patient data meta-analysis. Front Endocrinol (Lausanne). 2013;4:11.Google Scholar
  63. 63.
    Verma S, Rajaratnam JH, Denton J, Hoyland JA, Byers RJ. Adipocytic proportion of bone marrow is inversely related to bone formation in osteoporosis. J Clin Pathol. 2002;55(9):693–8.PubMedCentralPubMedGoogle Scholar
  64. 64.
    Kim M, Kim C, Choi YS, Kim M, Park C, Suh Y. Age-related alterations in mesenchymal stem cells related to shift in differentiation from osteogenic to adipogenic potential: implication to age-associated bone diseases and defects. Mech Ageing Dev. 2012;133(5):215–25.PubMedGoogle Scholar
  65. 65.
    Bethel M, Srour EF, Kacena MA. Hematopoietic cell regulation of osteoblast proliferation and differentiation. Curr Osteoporos Rep. 2011;9(2):96–102.PubMedCentralPubMedGoogle Scholar
  66. 66.
    Bredella MA, Torriani M, Ghomi RH, Thomas BJ, Brick DJ, Gerweck AV, et al. Vertebral bone marrow fat is positively associated with visceral fat and inversely associated with IGF-1 in obese women. Obesity (Silver Spring). 2011;19(1):49–53.Google Scholar
  67. 67.
    Thorsen K, Nordstrom P, Lorentzon R, Dahlen GH. The relation between bone mineral density, insulin-like growth factor I, lipoprotein (a), body composition, and muscle strength in adolescent males. J Clin Endocrinol Metab. 1999;84(9):3025–9.PubMedGoogle Scholar
  68. 68.
    Wake DJ, Strand M, Rask E, Westerbacka J, Livingstone DE, Soderberg S, et al. Intra-adipose sex steroid metabolism and body fat distribution in idiopathic human obesity. Clin Endocrinol (Oxf). 2007;66(3):440–6.Google Scholar
  69. 69.
    Sowers MF, Kshirsagar A, Crutchfield MM, Updike S. Joint influence of fat and lean body composition compartments on femoral bone mineral density in premenopausal women. Am J Epidemiol. 1992;136(3):257–65.PubMedGoogle Scholar
  70. 70.
    Salamone LM, Glynn N, Black D, Epstein RS, Palermo L, Meilahn E, et al. Body composition and bone mineral density in premenopausal and early perimenopausal women. J Bone Miner Res. 1995;10(11):1762–8.PubMedGoogle Scholar
  71. 71.
    Blain H, Vuillemin A, Teissier A, Hanesse B, Guillemin F, Jeandel C. Influence of muscle strength and body weight and composition on regional bone mineral density in healthy women aged 60 years and over. Gerontology. 2001;47(4):207–12.PubMedGoogle Scholar
  72. 72.
    Taaffe DR, Cauley JA, Danielson M, Nevitt MC, Lang TF, Bauer DC, et al. Race and sex effects on the association between muscle strength, soft tissue, and bone mineral density in healthy elders: the Health, Aging, and Body Composition Study. J Bone Miner Res. 2001;16(7):1343–52.PubMedGoogle Scholar
  73. 73.
    Kirchengast S, Peterson B, Hauser G, Knogler W. Body composition characteristics are associated with the bone density of the proximal femur end in middle- and old-aged women and men. Maturitas. 2001;39(2):133–45.PubMedGoogle Scholar
  74. 74.
    Coin A, Sergi G, Beninca P, Lupoli L, Cinti G, Ferrara L, et al. Bone mineral density and body composition in underweight and normal elderly subjects. Osteoporos Int. 2000;11(12):1043–50.PubMedGoogle Scholar
  75. 75.
    Cohen A, Dempster DW, Recker RR, Lappe JM, Zhou H, Zwahlen A, et al. Abdominal fat is associated with lower bone formation and inferior bone quality in healthy premenopausal women: a transiliac bone biopsy study. J Clin Endocrinol Metab. 2013;98(6):2562–72.PubMedCentralPubMedGoogle Scholar
  76. 76.
    Junior IF, Cardoso JR, Christofaro DG, Codogno JS, de Moraes AC, Fernandes RA. The relationship between visceral fat thickness and bone mineral density in sedentary obese children and adolescents. BMC Pediatr. 2013;13:37.PubMedCentralPubMedGoogle Scholar
  77. 77.
    Bhupathiraju SN, Dawson-Hughes B, Hannan MT, Lichtenstein AH, Tucker KL. Centrally located body fat is associated with lower bone mineral density in older Puerto Rican adults. Am J Clin Nutr. 2011;94(4):1063–70.PubMedCentralPubMedGoogle Scholar
  78. 78.
    Lu H, Fu X, Ma X, Wu Z, He W, Wang Z, et al. Relationships of percent body fat and percent trunk fat with bone mineral density among Chinese, black, and white subjects. Osteoporos Int. 2011;22(12):3029–35.PubMedGoogle Scholar
  79. 79.
    Russell M, Mendes N, Miller KK, Rosen CJ, Lee H, Klibanski A, et al. Visceral fat is a negative predictor of bone density measures in obese adolescent girls. J Clin Endocrinol Metab. 2010;95(3):1247–55.PubMedCentralPubMedGoogle Scholar
  80. 80.
    Hla MM, Davis JW, Ross PD, Wasnich RD, Yates AJ, Ravn P, et al. A multicenter study of the influence of fat and lean mass on bone mineral content: evidence for differences in their relative influence at major fracture sites. Early Postmenopausal Intervention Cohort (EPIC) Study Group. Am J Clin Nutr. 1996;64(3):354–60.PubMedGoogle Scholar
  81. 81.
    Takata S, Ikata T, Yonezu H. Characteristics of bone mineral density and soft tissue composition of obese Japanese women: application of dual-energy X-ray absorptiometry. J Bone Miner Metab. 1999;17(3):206–10.PubMedGoogle Scholar
  82. 82.
    Riggs BL, O’Fallon WM, Muhs J, O’Connor MK, Kumar R, Melton III LJ. Long-term effects of calcium supplementation on serum parathyroid hormone level, bone turnover, and bone loss in elderly women. J Bone Miner Res. 1998;13(2):168–74.PubMedGoogle Scholar
  83. 83.
    Zemel MB, Shi H, Greer B, Dirienzo D, Zemel PC. Regulation of adiposity by dietary calcium. FASEB J. 2000;14(9):1132–8.PubMedGoogle Scholar
  84. 84.
    Carruth BR, Skinner JD. The role of dietary calcium and other nutrients in moderating body fat in preschool children. Int J Obes Relat Metab Disord. 2001;25(4):559–66.PubMedGoogle Scholar
  85. 85.
    Skinner ML, Simpson JA, Buchholz AC. Dietary and total calcium intakes are associated with lower percentage total body and truncal fat in young, healthy adults. J Am Coll Nutr. 2011;30(6):484–90.PubMedGoogle Scholar
  86. 86.
    Heaney RP, Davies KM, Barger-Lux MJ. Calcium and weight: clinical studies. J Am Coll Nutr. 2002;21(2):152S–5.PubMedGoogle Scholar
  87. 87.
    Shapses SA, Heshka S, Heymsfield SB. Effect of calcium supplementation on weight and fat loss in women. J Clin Endocrinol Metab. 2004;89(2):632–7.PubMedCentralPubMedGoogle Scholar
  88. 88.
    Shi H, Dirienzo D, Zemel MB. Effects of dietary calcium on adipocyte lipid metabolism and body weight regulation in energy-restricted aP2-agouti transgenic mice. FASEB J. 2001;15(2):291–3.PubMedGoogle Scholar
  89. 89.
    Xue B, Moustaid N, Wilkison WO, Zemel MB. The agouti gene product inhibits lipolysis in human adipocytes via a Ca2+-dependent mechanism. FASEB J. 1998;12(13):1391–6.PubMedGoogle Scholar
  90. 90.
    Tremblay A, Gilbert JA. Human obesity: is insufficient calcium/dairy intake part of the problem? J Am Coll Nutr. 2011;30(5 Suppl 1):449S–53.PubMedGoogle Scholar
  91. 91.
    Yanovski JA, Parikh SJ, Yanoff LB, Denkinger BI, Calis KA, Reynolds JC, et al. Effects of calcium supplementation on body weight and adiposity in overweight and obese adults: a randomized trial. Ann Intern Med. 2009;150(12):821–6.PubMedCentralPubMedGoogle Scholar
  92. 92.
    Chen M, Pan A, Malik VS, Hu FB. Effects of dairy intake on body weight and fat: a meta-analysis of randomized controlled trials. Am J Clin Nutr. 2012;96(4):735–47.PubMedCentralPubMedGoogle Scholar
  93. 93.
    Zhu W, Cai D, Wang Y, Lin N, Hu Q, Qi Y, et al. Calcium plus vitamin D3 supplementation facilitated fat loss in overweight and obese college students with very-low calcium consumption: a randomized controlled trial. Nutr J. 2013;12:8.PubMedCentralPubMedGoogle Scholar
  94. 94.
    Sneve M, Figenschau Y, Jorde R. Supplementation with cholecalciferol does not result in weight reduction in overweight and obese subjects. Eur J Endocrinol. 2008;159(6):675–84.PubMedGoogle Scholar
  95. 95.
    Zittermann A, Frisch S, Berthold HK, Gotting C, Kuhn J, Kleesiek K, et al. Vitamin D supplementation enhances the beneficial effects of weight loss on cardiovascular disease risk markers. Am J Clin Nutr. 2009;89(5):1321–7.PubMedGoogle Scholar
  96. 96.
    Gallagher JC, Sai A, Templin T, Smith L. Dose response to vitamin D supplementation in postmenopausal women: a randomized trial. Ann Intern Med. 2012;156(6):425–37.PubMedGoogle Scholar
  97. 97.
    Shapses SA, Sukumar D, Schneider SH, Schlussel Y, Sherrell RM, Field MP, et al. Vitamin D supplementation and calcium absorption during caloric restriction: a randomized double-blind trial. Am J Clin Nutr. 2013;97(3):637–45.PubMedCentralPubMedGoogle Scholar
  98. 98.
    Shapses SA, Manson JE. Vitamin D and prevention of cardiovascular disease and diabetes: why the evidence falls short. JAMA. 2011;305(24):2565–6.PubMedCentralPubMedGoogle Scholar
  99. 99.
    Ji GR, Yao M, Sun CY, Li ZH, Han Z. BsmI, TaqI, ApaI and FokI polymorphisms in the vitamin D receptor (VDR) gene and risk of fracture in Caucasians: a meta-analysis. Bone. 2010;47(3):681–6.PubMedGoogle Scholar
  100. 100.
    Vandevyver C, Wylin T, Cassiman JJ, Raus J, Geusens P. Influence of the vitamin D receptor gene alleles on bone mineral density in postmenopausal and osteoporotic women. J Bone Miner Res. 1997;12(2):241–7.PubMedGoogle Scholar
  101. 101.
    Grundberg E, Brandstrom H, Ribom EL, Ljunggren O, Mallmin H, Kindmark A. Genetic variation in the human vitamin D receptor is associated with muscle strength, fat mass and body weight in Swedish women. Eur J Endocrinol. 2004;150(3):323–8.PubMedGoogle Scholar
  102. 102.
    Avenell A, Richmond PR, Lean ME, Reid DM. Bone loss associated with a high fibre weight reduction diet in postmenopausal women. Eur J Clin Nutr. 1994;48(8):561–6.PubMedGoogle Scholar
  103. 103.
    Chao D, Espeland MA, Farmer D, Register TC, Lenchik L, Applegate WB, et al. Effect of voluntary weight loss on bone mineral density in older overweight women. J Am Geriatr Soc. 2000;48(7):753–9.PubMedGoogle Scholar
  104. 104.
    Fogelholm GM, Sievanen HT, Kukkonen-Harjula TK, Pasanen ME. Bone mineral density during reduction, maintenance and regain of body weight in premenopausal, obese women. Osteoporos Int. 2001;12(3):199–206.PubMedGoogle Scholar
  105. 105.
    Ricci TA, Heymsfield SB, Pierson Jr RN, Stahl T, Chowdhury HA, Shapses SA. Moderate energy restriction increases bone resorption in obese postmenopausal women. Am J Clin Nutr. 2001;73(2):347–52.PubMedGoogle Scholar
  106. 106.
    Shapses SA, Von Thun NL, Heymsfield SB, Ricci TA, Ospina M, Pierson Jr RN, et al. Bone turnover and density in obese premenopausal women during moderate weight loss and calcium supplementation. J Bone Miner Res. 2001;16(7):1329–36.PubMedGoogle Scholar
  107. 107.
    Jensen LB, Quaade F, Sorensen OH. Bone loss accompanying voluntary weight loss in obese humans. J Bone Miner Res. 1994;9(4):459–63.PubMedGoogle Scholar
  108. 108.
    Pritchard JE, Nowson CA, Wark JD. Bone loss accompanying diet-induced or exercise-induced weight loss: a randomised controlled study. Int J Obes Relat Metab Disord. 1996;20(6):513–20.PubMedGoogle Scholar
  109. 109.
    Ramsdale SJ, Bassey EJ. Changes in bone mineral density associated with dietary-induced loss of body mass in young women. Clin Sci (Lond). 1994;87(3):343–8.Google Scholar
  110. 110.
    Ryan AS, Nicklas BJ, Dennis KE. Aerobic exercise maintains regional bone mineral density during weight loss in postmenopausal women. J Appl Physiol. 1998;84(4):1305–10.PubMedGoogle Scholar
  111. 111.
    Salamone LM, Cauley JA, Black DM, Simkin-Silverman L, Lang W, Gregg E, et al. Effect of a lifestyle intervention on bone mineral density in premenopausal women: a randomized trial. Am J Clin Nutr. 1999;70(1):97–103.PubMedGoogle Scholar
  112. 112.
    Svendsen OL, Hassager C, Christiansen C. 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. Am J Med. 1993;95(2):131–40.PubMedGoogle Scholar
  113. 113.
    Van Loan MD, Keim NL. Influence of cognitive eating restraint on total-body measurements of bone mineral density and bone mineral content in premenopausal women aged 18-45 y: a cross-sectional study. Am J Clin Nutr. 2000;72(3):837–43.PubMedGoogle Scholar
  114. 114.
    Bolotin HH. Inaccuracies inherent in dual-energy X-ray absorptiometry in vivo bone mineral densitometry may flaw osteopenic/osteoporotic interpretations and mislead assessment of antiresorptive therapy effectiveness. Bone. 2001;28(5):548–55.PubMedGoogle Scholar
  115. 115.
    Tothill P, Avenell A. Errors in dual-energy X-ray absorptiometry of the lumbar spine owing to fat distribution and soft tissue thickness during weight change. Br J Radiol. 1994;67(793):71–5.PubMedGoogle Scholar
  116. 116.
    Kanis JA, McCloskey EV, Johansson H, Oden A, Strom O, Borgstrom F. Development and use of FRAX in osteoporosis. Osteoporos Int. 2010;21 Suppl 2:S407–13.PubMedGoogle Scholar
  117. 117.
    Talbott SM, Cifuentes M, Dunn MG, Shapses SA. Energy restriction reduces bone density and biomechanical properties in aged female rats. J Nutr. 2001;131(9):2382–7.PubMedCentralPubMedGoogle Scholar
  118. 118.
    Cheng XG, Lowet G, Boonen S, Nicholson PH, Van der PG, Dequeker J. Prediction of vertebral and femoral strength in vitro by bone mineral density measured at different skeletal sites. J Bone Miner Res. 1998;13(9):1439–43.PubMedGoogle Scholar
  119. 119.
    Ensrud KE, Lipschutz RC, Cauley JA, Seeley D, Nevitt MC, Scott J, et al. Body size and hip fracture risk in older women: a prospective study. Study of Osteoporotic Fractures Research Group. Am J Med. 1997;103(4):274–80.PubMedGoogle Scholar
  120. 120.
    Langlois JA, Mussolino ME, Visser M, Looker AC, Harris T, Madans J. Weight loss from maximum body weight among middle-aged and older white women and the risk of hip fracture: the NHANES I epidemiologic follow-up study. Osteoporos Int. 2001;12(9):763–8.PubMedGoogle Scholar
  121. 121.
    Hawkins J, Cifuentes M, Pleshko NL, Ambia-Sobhan H, Shapses SA. Energy restriction is associated with lower bone mineral density of the tibia and femur in lean but not obese female rats. J Nutr. 2010;140(1):31–7.PubMedCentralPubMedGoogle Scholar
  122. 122.
    Sukumar D, Ambia-Sobhan H, Zurfluh R, Schlussel Y, Stahl TJ, Gordon CL, et al. Areal and volumetric bone mineral density and geometry at two levels of protein intake during caloric restriction: a randomized, controlled trial. J Bone Miner Res. 2011;26(6):1339–48.PubMedCentralPubMedGoogle Scholar
  123. 123.
    Valdimarsson T, Lofman O, Toss G, Strom M. Reversal of osteopenia with diet in adult coeliac disease. Gut. 1996;38(3):322–7.PubMedCentralPubMedGoogle Scholar
  124. 124.
    Robbins J, Hirsch C, Whitmer R, Cauley J, Harris T. The association of bone mineral density and depression in an older population. J Am Geriatr Soc. 2001;49(6):732–6.PubMedGoogle Scholar
  125. 125.
    Michelson D, Stratakis C, Hill L, Reynolds J, Galliven E, Chrousos G, et al. Bone mineral density in women with depression. N Engl J Med. 1996;335(16):1176–81.PubMedGoogle Scholar
  126. 126.
    Hannan MT, Felson DT, Dawson-Hughes B, Tucker KL, Cupples LA, Wilson PW, et al. Risk factors for longitudinal bone loss in elderly men and women: the Framingham Osteoporosis Study. J Bone Miner Res. 2000;15(4):710–20.PubMedGoogle Scholar
  127. 127.
    Nguyen TV, Sambrook PN, Eisman JA. Bone loss, physical activity, and weight change in elderly women: the Dubbo Osteoporosis Epidemiology Study. J Bone Miner Res. 1998;13(9):1458–67.PubMedGoogle Scholar
  128. 128.
    Ensrud KE, Cauley J, Lipschutz R, Cummings SR. Weight change and fractures in older women. Study of Osteoporotic Fractures Research Group. Arch Intern Med. 1997;157(8):857–63.PubMedGoogle Scholar
  129. 129.
    Mussolino ME, Looker AC, Madans JH, Langlois JA, Orwoll ES. Risk factors for hip fracture in white men: the NHANES I Epidemiologic Follow-up Study. J Bone Miner Res. 1998;13(6):918–24.PubMedGoogle Scholar
  130. 130.
    Bales CW, Ritchie CS. Sarcopenia, weight loss, and nutritional frailty in the elderly. Annu Rev Nutr. 2002;22:309–23.PubMedGoogle Scholar
  131. 131.
    Wing RR, Hill JO. Successful weight loss maintenance. Annu Rev Nutr. 2001;21:323–41.PubMedGoogle Scholar
  132. 132.
    Vestergaard P, Borglum J, Heickendorff L, Mosekilde L, Richelsen B. Artifact in bone mineral measurements during a very low calorie diet: short-term effects of growth hormone. J Clin Densitom. 2000;3(1):63–71.PubMedGoogle Scholar
  133. 133.
    Goldstein SA, Elwyn DH. The effects of injury and sepsis on fuel utilization. Annu Rev Nutr. 1989;9:445–73.PubMedGoogle Scholar
  134. 134.
    Ricci TA, Chowdhury HA, Heymsfield SB, Stahl T, Pierson Jr RN, Shapses SA. Calcium supplementation suppresses bone turnover during weight reduction in postmenopausal women. J Bone Miner Res. 1998;13(6):1045–50.PubMedGoogle Scholar
  135. 135.
    Jensen LB, Kollerup G, Quaade F, Sorensen OH. Bone minerals changes in obese women during a moderate weight loss with and without calcium supplementation. J Bone Miner Res. 2001;16(1):141–7.PubMedGoogle Scholar
  136. 136.
    Borghi L, Schianchi T, Meschi T, Guerra A, Allegri F, Maggiore U, et al. Comparison of two diets for the prevention of recurrent stones in idiopathic hypercalciuria. N Engl J Med. 2002;346(2):77–84.PubMedGoogle Scholar
  137. 137.
    Jackson RD, Lacroix AZ, Gass M, Wallace RB, Robbins J, Lewis CE, et al. Calcium plus vitamin D supplementation and the risk of fractures. N Engl J Med. 2006;354(7):669–83.PubMedGoogle Scholar
  138. 138.
    Riedt CS, Cifuentes M, Stahl T, Chowdhury HA, Schlussel Y, Shapses SA. Overweight postmenopausal women lose bone with moderate weight reduction and 1 g/day calcium intake. J Bone Miner Res. 2005;20(3):455–63.PubMedCentralPubMedGoogle Scholar
  139. 139.
    Mason C, Xiao L, Imayama I, Duggan CR, Bain C, Foster-Schubert KE, et al. Effects of weight loss on serum vitamin D in postmenopausal women. Am J Clin Nutr. 2011;94(1):95–103.PubMedCentralPubMedGoogle Scholar
  140. 140.
    Ribot C, Tremollieres F, Pouilles JM, Bonneu M, Germain F, Louvet JP. Obesity and postmenopausal bone loss: the influence of obesity on vertebral density and bone turnover in postmenopausal women. Bone. 1987;8(6):327–31.PubMedGoogle Scholar
  141. 141.
    Rosen CJ, Morrison A, Zhou H, Storm D, Hunter SJ, Musgrave K, et al. Elderly women in northern New England exhibit seasonal changes in bone mineral density and calciotropic hormones. Bone Miner. 1994;25(2):83–92.PubMedGoogle Scholar
  142. 142.
    Rapuri PB, Kinyamu HK, Gallagher JC, Haynatzka V. Seasonal changes in calciotropic hormones, bone markers, and bone mineral density in elderly women. J Clin Endocrinol Metab. 2002;87(5):2024–32.PubMedGoogle Scholar
  143. 143.
    Storm D, Eslin R, Porter ES, Musgrave K, Vereault D, Patton C, et al. Calcium supplementation prevents seasonal bone loss and changes in biochemical markers of bone turnover in elderly New England women: a randomized placebo-controlled trial. J Clin Endocrinol Metab. 1998;83(11):3817–25.PubMedGoogle Scholar
  144. 144.
    Fleischer J, Stein EM, Bessler M, Della BM, Restuccia N, Olivero-Rivera L, et al. The decline in hip bone density after gastric bypass surgery is associated with extent of weight loss. J Clin Endocrinol Metab. 2008;93(10):3735–40.PubMedCentralPubMedGoogle Scholar
  145. 145.
    Johnson JM, Maher JW, Samuel I, Heitshusen D, Doherty C, Downs RW. Effects of gastric bypass procedures on bone mineral density, calcium, parathyroid hormone, and vitamin D. J Gastrointest Surg. 2005;9(8):1106–10.PubMedGoogle Scholar
  146. 146.
    Sinha N, Shieh A, Stein EM, Strain G, Schulman A, Pomp A, et al. Increased PTH and 1.25(OH)(2)D levels associated with increased markers of bone turnover following bariatric surgery. Obesity (Silver Spring). 2011;19(12):2388–93.Google Scholar
  147. 147.
    Bergqvist AG, Schall JI, Stallings VA, Zemel BS. Progressive bone mineral content loss in children with intractable epilepsy treated with the ketogenic diet. Am J Clin Nutr. 2008;88(6):1678–84.PubMedGoogle Scholar
  148. 148.
    Reddy ST, Wang CY, Sakhaee K, Brinkley L, Pak CY. Effect of low-carbohydrate high-protein diets on acid-base balance, stone-forming propensity, and calcium metabolism. Am J Kidney Dis. 2002;40(2):265–74.PubMedGoogle Scholar
  149. 149.
    Willi SM, Oexmann MJ, Wright NM, Collop NA, Key Jr LL. The effects of a high-protein, low-fat, ketogenic diet on adolescents with morbid obesity: body composition, blood chemistries, and sleep abnormalities. Pediatrics. 1998;101(1 Pt 1):61–7.PubMedGoogle Scholar
  150. 150.
    Clifton P. Effects of a high protein diet on body weight and comorbidities associated with obesity. Br J Nutr. 2012;108 Suppl 2:S122–9.PubMedGoogle Scholar
  151. 151.
    Foster GD, Wyatt HR, Hill JO, Makris AP, Rosenbaum DL, Brill C, et al. Weight and metabolic outcomes after 2 years on a low-carbohydrate versus low-fat diet: a randomized trial. Ann Intern Med. 2010;153(3):147–57.PubMedCentralPubMedGoogle Scholar
  152. 152.
    Friedman AN, Ogden LG, Foster GD, Klein S, Stein R, Miller B, et al. Comparative effects of low-carbohydrate high-protein versus low-fat diets on the kidney. Clin J Am Soc Nephrol. 2012;7(7):1103–11.PubMedCentralPubMedGoogle Scholar
  153. 153.
    Sebastian A. Dietary protein content and the diet’s net acid load: opposing effects on bone health. Am J Clin Nutr. 2005;82(5):921–2.PubMedGoogle Scholar
  154. 154.
    Frassetto L, Morris Jr RC, Sebastian A. Long-term persistence of the urine calcium-lowering effect of potassium bicarbonate in postmenopausal women. J Clin Endocrinol Metab. 2005;90(2):831–4.PubMedGoogle Scholar
  155. 155.
    Maurer M, Riesen W, Muser J, Hulter HN, Krapf R. Neutralization of Western diet inhibits bone resorption independently of K intake and reduces cortisol secretion in humans. Am J Physiol Renal Physiol. 2003;284(1):F32–40.PubMedGoogle Scholar
  156. 156.
    Bushinsky DA. Dysregulation of the calcium, phosphorus, parathyroid hormone, and vitamin D axis: what are the causes and risks? Am J Kidney Dis. 2001;37(6):1310–2.PubMedGoogle Scholar
  157. 157.
    Gotfredsen A, Westergren HH, Andersen T. Influence of orlistat on bone turnover and body composition. Int J Obes Relat Metab Disord. 2001;25(8):1154–60.PubMedGoogle Scholar
  158. 158.
    Ryan AS, Treuth MS, Hunter GR, Elahi D. Resistive training maintains bone mineral density in postmenopausal women. Calcif Tissue Int. 1998;62(4):295–9.PubMedGoogle Scholar
  159. 159.
    Villareal DT, Fontana L, Weiss EP, Racette SB, Steger-May K, Schechtman KB, et al. Bone mineral density response to caloric restriction-induced weight loss or exercise-induced weight loss: a randomized controlled trial. Arch Intern Med. 2006;166(22):2502–10.PubMedGoogle Scholar
  160. 160.
    Villareal DT, Shah K, Banks MR, Sinacore DR, Klein S. Effect of weight loss and exercise therapy on bone metabolism and mass in obese older adults: a one-year randomized controlled trial. J Clin Endocrinol Metab. 2008;93(6):2181–7.PubMedCentralPubMedGoogle Scholar
  161. 161.
    Silverman NE, Nicklas BJ, Ryan AS. Addition of aerobic exercise to a weight loss program increases BMD, with an associated reduction in inflammation in overweight postmenopausal women. Calcif Tissue Int. 2009;84(4):257–65.PubMedCentralPubMedGoogle Scholar
  162. 162.
    Redman LM, Rood J, Anton SD, Champagne C, Smith SR, Ravussin E. Calorie restriction and bone health in young, overweight individuals. Arch Intern Med. 2008;168(17):1859–66.PubMedCentralPubMedGoogle Scholar
  163. 163.
    Shah K, Armamento-Villareal R, Parimi N, Chode S, Sinacore DR, Hilton TN, et al. 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. J Bone Miner Res. 2011;26(12):2851–9.PubMedCentralPubMedGoogle Scholar
  164. 164.
    Villareal DT, Chode S, Parimi N, Sinacore DR, Hilton T, Armamento-Villareal R, et al. Weight loss, exercise, or both and physical function in obese older adults. N Engl J Med. 2011;364(13):1218–29.PubMedCentralPubMedGoogle Scholar
  165. 165.
    Scibora LM, Ikramuddin S, Buchwald H, Petit MA. Examining the link between bariatric surgery, bone loss, and osteoporosis: a review of bone density studies. Obes Surg. 2012;22(4):654–67.PubMedGoogle Scholar
  166. 166.
    Lee WJ, Wang W, Lee YC, Huang MT, Ser KH, Chen JC. Laparoscopic mini-gastric bypass: experience with tailored bypass limb according to body weight. Obes Surg. 2008;18(3):294–9.PubMedGoogle Scholar
  167. 167.
    Shukla AP, Moreira M, Dakin G, Pomp A, Brillon D, Sinha N, et al. Medical versus surgical treatment of type 2 diabetes: the search for level 1 evidence. Surg Obes Relat Dis. 2012;8(4):476–82.PubMedGoogle Scholar
  168. 168.
    Vilarrasa N, San JP, Garcia I, Gomez-Vaquero C, Miras PM, de Gordejuela AG, et al. Evaluation of bone mineral density loss in morbidly obese women after gastric bypass: 3-year follow-up. Obes Surg. 2011;21(4):465–72.PubMedGoogle Scholar
  169. 169.
    Goode LR, Brolin RE, Chowdhury HA, Shapses SA. Bone and gastric bypass surgery: effects of dietary calcium and vitamin D. Obes Res. 2004;12(1):40–7.PubMedGoogle Scholar
  170. 170.
    Lalmohamed A, de Vries F, Bazelier MT, Cooper A, van Staa TP, Cooper C, et al. Risk of fracture after bariatric surgery in the United Kingdom: population based, retrospective cohort study. BMJ. 2012;345:e5085.PubMedCentralPubMedGoogle Scholar
  171. 171.
    Ybarra J, Sanchez-Hernandez J, Gich I, De LA, Rius X, Rodriguez-Espinosa J, et al. Unchanged hypovitaminosis D and secondary hyperparathyroidism in morbid obesity after bariatric surgery. Obes Surg. 2005;15(3):330–5.PubMedGoogle Scholar
  172. 172.
    Hultin H, Edfeldt K, Sundbom M, Hellman P. Left-shifted relation between calcium and parathyroid hormone in obesity. J Clin Endocrinol Metab. 2010;95(8):3973–81.PubMedGoogle Scholar
  173. 173.
    Coates PS, Fernstrom JD, Fernstrom MH, Schauer PR, Greenspan SL. Gastric bypass surgery for morbid obesity leads to an increase in bone turnover and a decrease in bone mass. J Clin Endocrinol Metab. 2004;89(3):1061–5.PubMedGoogle Scholar
  174. 174.
    Avgerinos DV, Leitman IM, Martinez RE, Liao EP. Evaluation of markers for calcium homeostasis in a population of obese adults undergoing gastric bypass operations. J Am Coll Surg. 2007;205(2):294–7.PubMedGoogle Scholar
  175. 175.
    Jin J, Robinson AV, Hallowell PT, Jasper JJ, Stellato TA, Wilhem SM. Increases in parathyroid hormone (PTH) after gastric bypass surgery appear to be of a secondary nature. Surgery. 2007;142(6):914–20.PubMedGoogle Scholar
  176. 176.
    Stein EM, Carrelli A, Young P, Bucovsky M, Zhang C, Schrope B, et al. Bariatric surgery results in cortical bone loss. J Clin Endocrinol Metab. 2013;98(2):541–9.PubMedCentralPubMedGoogle Scholar
  177. 177.
    Pluskiewicz W, Buzga M, Holeczy P, Bortlik L, Smajstrla V, Adamczyk P. Bone mineral changes in spine and proximal femur in individual obese women after laparoscopic sleeve gastrectomy: a short-term study. Obes Surg. 2012;22(7):1068–76.PubMedCentralPubMedGoogle Scholar
  178. 178.
    Shapses SA. Is bone loss after gastric bypass surgery associated with the extent of weight loss? Nat Clin Pract Endocrinol Metab. 2009;5(2):80–1.PubMedCentralPubMedGoogle Scholar
  179. 179.
    Folli F, Sabowitz BN, Schwesinger W, Fanti P, Guardado-Mendoza R, Muscogiuri G. Bariatric surgery and bone disease: from clinical perspective to molecular insights. Int J Obes (Lond). 2012;36(11):1373–9.Google Scholar
  180. 180.
    Brzozowska MM, Sainsbury A, Eisman JA, Baldock PA, Center JR. Bariatric surgery, bone loss, obesity and possible mechanisms. Obes Rev. 2013;14(1):52–67.PubMedGoogle Scholar
  181. 181.
    Milliken LA, Going SB, Lohman TG. Effects of variations in regional composition on soft tissue measurements by dual-energy X-ray absorptiometry. Int J Obes Relat Metab Disord. 1996;20(7):677–82.PubMedGoogle Scholar
  182. 182.
    Yu EW, Thomas BJ, Brown JK, Finkelstein JS. Simulated increases in body fat and errors in bone mineral density measurements by DXA and QCT. J Bone Miner Res. 2012;27(1):119–24.PubMedGoogle Scholar
  183. 183.
    Liu G, Peacock M, Eilam O, Dorulla G, Braunstein E, Johnston CC. Effect of osteoarthritis in the lumbar spine and hip on bone mineral density and diagnosis of osteoporosis in elderly men and women. Osteoporos Int. 1997;7(6):564–9.PubMedGoogle Scholar
  184. 184.
    Rizzoli R, Slosman D, Bonjour JP. The role of dual energy X-ray absorptiometry of lumbar spine and proximal femur in the diagnosis and follow-up of osteoporosis. Am J Med. 1995;98(2A):33S–6.PubMedGoogle Scholar
  185. 185.
    Hansen KE, Binkley N, Blank RD, Krueger DC, Christian RC, Malone DG, et al. An atlas improves interobserver agreement regarding application of the ISCD vertebral body exclusion criteria. J Clin Densitom. 2007;10(4):359–64.PubMedGoogle Scholar
  186. 186.
    VonThun N, Sukumar D, Heymsfield S, Shapses S. Weight reduction followed by regain in postmenopausal women only partially attenuates bone loss: a two year case control trial. Obesity. 2011;19:S113.Google Scholar
  187. 187.
    Villalon KL, Gozansky WS, Van Pelt RE, Wolfe P, Jankowski CM, Schwartz RS, et al. A losing battle: weight regain does not restore weight loss-induced bone loss in postmenopausal women. Obesity (Silver Spring). 2011;19(12):2345–50.Google Scholar
  188. 188.
    Waters DL, Vawter R, Qualls C, Chode S, Armamento-Villareal R, Villareal DT. Long-term maintenance of weight loss after lifestyle intervention in frail, obese older adults. J Nutr Health Aging. 2013;17(1):3–7.PubMedCentralPubMedGoogle Scholar
  189. 189.
    Hinton PS, Rector RS, Linden MA, Warner SO, Dellsperger KC, Chockalingam A, et al. Weight-loss-associated changes in bone mineral density and bone turnover after partial weight regain with or without aerobic exercise in obese women. Eur J Clin Nutr. 2012;66(5):606–12.PubMedCentralPubMedGoogle Scholar
  190. 190.
    Meyer HE, Tverdal A, Selmer R. Weight variability, weight change and the incidence of hip fracture: a prospective study of 39,000 middle-aged Norwegians. Osteoporos Int. 1998;8(4):373–8.PubMedGoogle Scholar
  191. 191.
    Fogelholm M, Sievanen H, Heinonen A, Virtanen M, Uusi-Rasi K, Pasanen M, et al. Association between weight cycling history and bone mineral density in premenopausal women. Osteoporos Int. 1997;7(4):354–8.PubMedGoogle Scholar
  192. 192.
    Bogden JD, Kemp FW, Huang AE, Shapses SA, Ambia-Sobhan H, Jagpal S, et al. Bone mineral density and content during weight cycling in female rats: effects of dietary amylase-resistant starch. Nutr Metab (Lond). 2008;5:34.Google Scholar
  193. 193.
    Gozansky WS, Van Pelt RE, Jankowski CM, Schwartz RS, Kohrt WM. Protection of bone mass by estrogens and raloxifene during exercise-induced weight loss. J Clin Endocrinol Metab. 2005;90(1):52–9.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Department of Nutritional SciencesRutgers UniversityNew BrunswickUSA
  2. 2.Institute of Nutrition and Food Technology INTAUniversidad de ChileSantiagoChile

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