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Bariatric Surgery and Bone Loss: Do We Need to Be Concerned?

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Abstract

Despite significant improvement in weight and comorbid conditions, there is growing evidence that bariatric surgery may exert a negative effect on the skeleton. This review has focused on the impact of bariatric surgery on bone health, with the concern that bariatric surgery may increase skeletal fragility and fracture risk by accelerating bone loss. We have highlighted studies evaluating changes in bone metabolism after three commonly performed bariatric procedures including laparoscopic adjustable gastric banding, Roux-en-Y gastric bypass surgery and increasingly popular sleeve gastrectomy. This review has also discussed some of the technical issues faced in measuring bone in obese populations and during dynamic weight loss. There is limited evidence regarding potential mechanisms for the reported observations of increased bone turnover and/or bone loss after bariatric surgery. We have reviewed the evidence surrounding potential factors affecting bone health in bariatric patients such as rapid weight loss per se, nutritional deficiencies, effects of fat-derived adipokines and gut-derived appetite-regulatory hormones. Future prospective long-term cohort studies are needed to define how to quantify bone loss in individuals with obesity, particularly following massive weight loss, and for how long the bone changes continue. These studies will help clarify any negative clinical consequences of these changes, including future fracture risk in this unique group of patients.

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References

  1. World Health Organization (WHO). Obesity: preventing and managing the global epidemic. Report of a WHO consultation. World Health Organization Technical Report Series 894. Geneva: WHO; 2000.

  2. Fontaine KR, Redden DT, Wang CX, Westfall AO, Allison DB. Years of life lost due to obesity. JAMA J Am Med Assoc. 2003;289(2):187–93.

    Google Scholar 

  3. Rosmond R, Lapidus L, Marin P, Bjorntorp P. Mental distress, obesity and body fat distribution in middle-aged men. Obes Res. 1996;4(3):245–52.

    CAS  PubMed  Google Scholar 

  4. Christou NV. Impact of obesity and bariatric surgery on survival. World J Surg. 2009;33(10):2022–7.

    PubMed  Google Scholar 

  5. Buchwald H, Oien DM. Metabolic/bariatric surgery worldwide 2011. Obes Surg. 2013;23(4):427–36.

    PubMed  Google Scholar 

  6. Albala C, Yanez M, Devoto E, Sostin C, Zeballos L, Santos JL. Obesity as a protective factor for postmenopausal osteoporosis. Int J Obes. 1996;20(11):1027–32.

    CAS  Google Scholar 

  7. 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 Endocr Metab. 1992;75(1):45–51.

    CAS  PubMed  Google Scholar 

  8. Rosen CJ, Klibanski A. Bone, fat, and body composition: evolving concepts in the pathogenesis of osteoporosis. Am J Med. 2009;122(5):409–14.

    CAS  PubMed  Google Scholar 

  9. Hsu YH, Venners SA, Terwedow HA, Feng Y, Niu TH, Li ZP, et al. Relation of body composition, fat mass, and serum lipids to osteoporotic fractures and bone mineral density in Chinese men and women. Am J Clin Nutr. 2006;83(1):146–54.

    CAS  PubMed  Google Scholar 

  10. 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. 2000;24(5):627–32.

    CAS  Google Scholar 

  11. 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.

    CAS  PubMed  Google Scholar 

  12. Grethen E, McClintock R, Gupta CE, Jones R, Cacucci BM, Diaz D, et al. Vitamin D and hyperparathyroidism in obesity. J Clin Endocrinol Metabol. 2011;96(5):1320–6.

    CAS  Google Scholar 

  13. Hammoud AO, Gibson M, Peterson CM, Meikle AW, Carrell DT. Impact of male obesity on infertility: a critical review of the current literature. Fertil Steril. 2008;90(4):897–904.

    PubMed  Google Scholar 

  14. Khosla S. Minireview: the OPG/RANKL/RANK system. Endocrinology. 2001;142(12):5050–5.

    CAS  PubMed  Google Scholar 

  15. Gilsanz V, Chalfant J, Mo AO, Lee DC, Dorey FJ, Mittelman SD. Reciprocal relations of subcutaneous and visceral fat to bone structure and strength. J Clin Endocrinol Metabol. 2009;94(9):3387–93.

    CAS  Google Scholar 

  16. 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 Metabol. 2010;95(3):1247–55.

    CAS  Google Scholar 

  17. 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.

    CAS  PubMed Central  PubMed  Google Scholar 

  18. Papakitsou EF, Margioris AN, Dretakis KE, Trovas G, Zoras U, Lyritis G, et al. Body mass index (BMI) and parameters of bone formation and resorption in postmenopausal women. Maturitas. 2004;47(3):185–93.

    CAS  PubMed  Google Scholar 

  19. Reid IR. Relationships between fat and bone. Osteoporos Int. 2008;19(5):595–606.

    CAS  PubMed  Google Scholar 

  20. Meunier P, Aaron J, Edouard C, Vignon G. Osteoporosis and the replacement of cell populations of the marrow by adipose tissue. A quantitative study of 84 iliac bone biopsies. Clin Orthop Relat Res. 1971;80:147–54.

    CAS  PubMed  Google Scholar 

  21. Sekiya I, Larson BL, Vuoristo JT, Cui JG, Prockop DJ. Adipogenic differentiation of human adult stem cells from bone marrow stroma (MSCs). J Bone Miner Res. 2004;19(2):256–64.

    CAS  PubMed  Google Scholar 

  22. Schellinger D, Lin CS, Hatipoglu HG, Fertikh D. Potential value of vertebral proton MR spectroscopy in determining bone weakness. Am J Neuroradiol. 2001;22(8):1620–7.

    CAS  PubMed  Google Scholar 

  23. Compston J. Obesity and bone. Current Osteoporos Rep. 2013;11(1):30–5.

    Google Scholar 

  24. Flynn J, Foley S, Jones G. Can BMD assessed by DXA at age 8 predict fracture risk in boys and girls during puberty? An eight-year prospective study. J Bone Miner Res. 2007;22(9):1463–7.

    PubMed  Google Scholar 

  25. 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.

    PubMed  Google Scholar 

  26. Johansson H, Kanis JA, Oden A, McCloskey E, Chapurlat RD, Christiansen C, et al. A meta-analysis of the association of fracture risk and body mass index in women. J Bone Miner Res. 2014;29(1):223–33.

    Google Scholar 

  27. Compston JE, Watts NB, Chapurlat R, Cooper C, Boonen S, Greenspan S, et al. Obesity is not protective against fracture in postmenopausal women: GLOW. Am J Med. 2011;124(11):1043–50.

    PubMed  Google Scholar 

  28. Korenkov M. Bariatric surgery. Contrib Nephrol. 2006;151:243–53.

    PubMed  Google Scholar 

  29. Kuzmak LI. A preliminary-report on a silicone gastric banding for obesity. Clin Nutr. 1986;5:73–7.

    Google Scholar 

  30. Melissas J, Koukouraki S, Askoxylakis J, Stathaki M, Daskalakis M, Perisinakis K, et al. Sleeve gastrectomy—a restrictive procedure? Obes Surg. 2007;17(1):57–62.

    PubMed  Google Scholar 

  31. de Jong JR, van Ramshorst B, Gooszen HG, Smout AJ, Tiel-Van Buul MM. Weight loss after laparoscopic adjustable gastric banding is not caused by altered gastric emptying. Obes Surg. 2009;19(3):287–92.

    PubMed  Google Scholar 

  32. Madan AK, Harper JL, Tichansky DS. Techniques of laparoscopic gastric bypass: on-line survey of American Society for Bariatric Surgery practicing surgeons. Surg Obes Relat Dis. 2008;4(2):166–72.

    PubMed  Google Scholar 

  33. le Roux CW, Aylwin SJB, Batterham RL, Borg CM, Coyle F, Prasad V, et al. Gut hormone profiles following bariatric surgery favor an anorectic state, facilitate weight loss, and improve metabolic parameters. Ann Surg. 2006;243(1):108–14.

    PubMed Central  PubMed  Google Scholar 

  34. Borg CM, le Roux CW, Ghatei MA, Bloom SR, Patel AG, Aylwin SJB. Progressive rise in gut hormone levels after Roux-en-Y gastric bypass suggests gut adaptation and explains altered satiety. Brit J Surg. 2006;93(2):210–5.

    CAS  PubMed  Google Scholar 

  35. Dixon AFR, le Roux CW, Ghatei MA, Bloom SR, McGee TL, Dixon JB. Pancreatic polypeptide meal response may predict gastric band-induced weight loss. Obes Surg. 2011;21(12):1906–13.

    PubMed  Google Scholar 

  36. Buchwald H, Avidor Y, Braunwald E, Jensen MD, Pories W, Fahrbach K, et al. Bariatric surgery: a systematic review and meta-analysis. JAMA, J Am Med Assoc. 2004;292(14):1724–37.

    CAS  Google Scholar 

  37. O’Brien PE, MacDonald L, Anderson M, Brennan L, Brown WA. Long-term outcomes after bariatric surgery: fifteen-year follow-up of adjustable gastric banding and a systematic review of the bariatric surgical literature. Ann Surg. 2013;257(1):87–94.

    PubMed  Google Scholar 

  38. Committee ACI. Updated position statement on sleeve gastrectomy as a bariatric procedure. Surg Obes Relat Dis. 2012;8(3):e21–6.

    Google Scholar 

  39. Schneider BE, Mun EC. Surgical management of morbid obesity. Diabetes Care. 2005;28(2):475–80.

    PubMed  Google Scholar 

  40. Blackburn G. Solutions in weight control: lessons from gastric surgery. Am J Clin Nutr. 2005;82(1):248s–52s.

    CAS  PubMed  Google Scholar 

  41. Everson G, Kelsberg G, Nashelsky J. How effective is gastric bypass for-weight loss? J Fam Practice. 2004;53(11):914-+.

    Google Scholar 

  42. Heneghan HM, Meron-Eldar S, Brethauer SA, Schauer PR, Young JB. Effect of bariatric surgery on cardiovascular risk profile. Am J Cardiol. 2011;108(10):1499–507.

    PubMed  Google Scholar 

  43. Giusti V, Gasteyger C, Suter M, Heraief E, Gaillard RC, Burckhardt P. Gastric banding induces negative bone remodelling in the absence of secondary hyperparathyroidism: potential role of serum C telopeptides for follow-up. Int J Obes. 2005;29(12):1429–35.

    CAS  Google Scholar 

  44. Pugnale N, Giusti V, Suter M, Zysset E, Heraief E, Gaillard RC, et al. Bone metabolism and risk of secondary hyperparathyroidism 12 months after gastric banding in obese pre-menopausal women. Int J Obes. 2003;27(1):110–6.

    CAS  Google Scholar 

  45. von Mach MA, Stoeckli R, Bilz S, Kraenzlin M, Langer I, Keller U. Changes in bone mineral content after surgical treatment of morbid obesity. Metabolism. 2004;53(7):918–21.

    Google Scholar 

  46. Smith FJ, Holman CDJ, Moorin RE, Fletcher DR. Incidence of bariatric surgery and postoperative outcomes: a population-based analysis in Western Australia. Med J Aust. 2008;189(4):198–202.

    PubMed  Google Scholar 

  47. Kehagias I, Spyropoulos C, Karamanakos S, Kalfarentzos F. Efficacy of sleeve gastrectomy as sole procedure in patients with clinically severe obesity (BMI </=50 kg/m(2)). Surg Obes Relat Dis. 2013;9(3):363–9.

    PubMed  Google Scholar 

  48. Nogues X, Goday A, Pena MJ, Benaiges D, de Ramon M, Crous X, et al. Bone mass loss after sleeve gastrectomy: a prospective comparative study with gastric bypass. Cir Espan. 2010;88(2):103–9.

    Google Scholar 

  49. 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.

    PubMed Central  PubMed  Google Scholar 

  50. Ruiz-Tovar J, Oller I, Priego P, Arroyo A, Calero A, Diez M, et al. Short- and mid-term changes in bone mineral density after laparoscopic sleeve gastrectomy. Obes Surg. 2013;23(7):861–6.

    PubMed  Google Scholar 

  51. Silverberg SJ, Shane E, Delacruz L, Dempster DW, Feldman F, Seldin D, et al. Skeletal disease in primary hyperparathyroidism. J Bone Miner Res. 1989;4(3):283–91.

    CAS  PubMed  Google Scholar 

  52. Fleischer J, Stein EM, Bessler M, Della Badia M, 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 Endocr Metab. 2008;93(10):3735–40.

    CAS  PubMed Central  PubMed  Google Scholar 

  53. 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.

    CAS  PubMed  Google Scholar 

  54. Ott MT, Fanti P, Malluche HH, Ryo UY, Whaley FS, Strodel WE, et al. Biochemical-evidence of metabolic bone-disease in women following roux-Y gastric bypass for morbid-obesity. Obes Surg. 1992;2(4):341–8.

    PubMed  Google Scholar 

  55. 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 Endocr Metab. 2004;89(3):1061–5.

    CAS  PubMed  Google Scholar 

  56. 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.

    PubMed  Google Scholar 

  57. Johnson JM, Maher JW, DeMaria EJ, Downs RW, Wolfe LG, Kellum JM. The long-term effects of gastric bypass on vitamin D metabolism. Ann Surg. 2006;243(5):701–5.

    PubMed Central  PubMed  Google Scholar 

  58. Carrasco F, Ruz M, Rojas P, Csendes A, Rebolledo A, Codoceo J, et al. Changes in bone mineral density, body composition and adiponectin levels in morbidly obese patients after bariatric surgery. Obes Surg. 2009;19(1):41–6.

    PubMed  Google Scholar 

  59. Kaulfers AMD, Bean JA, Inge TH, Dolan LM, Kalkwarf HJ. Bone loss in adolescents after bariatric surgery. Pediatrics. 2011;127(4):E956–61.

    PubMed Central  PubMed  Google Scholar 

  60. Bruno C, Fulford AD, Potts JR, McClintock R, Jones R, Cacucci BM, et al. Serum markers of bone turnover are increased at six and 18 months after Roux-En-Y bariatric surgery: correlation with the reduction in leptin. J Clin Endocr Metab. 2010;95(1):159–66.

    CAS  PubMed Central  PubMed  Google Scholar 

  61. Mahdy T, Atia S, Farid M, Adulatif A. Effect of Roux-en Y gastric bypass on bone metabolism in patients with morbid obesity: mansoura experiences. Obes Surg. 2008;18(12):1526–31.

    PubMed  Google Scholar 

  62. Valderas JP, Velasco S, Solari S, Liberona Y, Viviani P, Maiz A, et al. Increase of bone resorption and the parathyroid hormone in postmenopausal women in the long-term after Roux-en-Y gastric bypass. Obes Surg. 2009;19(8):1132–8.

    PubMed  Google Scholar 

  63. Vilarrasa N, Gomez JM, Elio I, Gomez-Vaquero C, Masdevall C, Pujol J, et al. Evaluation of bone disease in morbidly obese women after gastric bypass and risk factors implicated in bone loss. Obes Surg. 2009;19(7):860–6.

    PubMed  Google Scholar 

  64. Stein EM, Carrelli A, Young P, Bucovsky M, Zhang C, Schrope B, et al. Bariatric surgery results in cortical bone loss. J Clin Endocrinol Metabol. 2013;98(2):541–9.

    CAS  Google Scholar 

  65. Casagrande DS, Repetto G, Mottin CC, Shah J, Pietrobon R, Worni M, et al. Changes in bone mineral density in women following 1-year gastric bypass surgery. Obes Surg. 2012;22(8):1287–92.

    PubMed  Google Scholar 

  66. 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.

    PubMed  Google Scholar 

  67. Vilarrasa N, San Jose P, 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.

    PubMed  Google Scholar 

  68. Zwintscher NP, Azarow KS, Horton JD, Newton CR, Martin MJ. The increasing incidence of adolescent bariatric surgery. J Pediatr Surg. 2013;48(12):2401–7.

    PubMed  Google Scholar 

  69. Boza C, Viscido G, Salinas J, Crovari F, Funke R, Perez G. Laparoscopic sleeve gastrectomy in obese adolescents: results in 51 patients. Surg Obes Relat Dis. 2012;8(2):133–7 (discussion 7–9).

    PubMed  Google Scholar 

  70. Balsa JA, Botella-Carretero JI, Peromingo R, Zamarron I, Arrieta F, Munoz-Malo T, et al. Role of calcium malabsorption in the development of secondary hyperparathyroidism after biliopancreatic diversion. J Endocrinol Invest. 2008;31(10):845–50.

    CAS  PubMed  Google Scholar 

  71. Balsa JA, Botella-Carretero JI, Peromingo R, Caballero C, Munoz-Malo T, Villafruela JJ, et al. Chronic increase of bone turnover markers after biliopancreatic diversion is related to secondary hyperparathyroidism and weight loss. Relation with bone mineral density. Obes Surg. 2010;20(4):468–73.

    PubMed  Google Scholar 

  72. Compston JE, Vedi S, Gianetta E, Watson G, Civalleri D, Scopinaro N. Bone histomorphometry and vitamin D status after biliopancreatic bypass for obesity. Gastroenterology. 1984;87(2):350–6.

    CAS  PubMed  Google Scholar 

  73. Compston JE, Vedi S, Ledger JE, Webb A, Gazet JC, Pilkington TR. Vitamin D status and bone histomorphometry in gross obesity. Am J Clin Nutr. 1981;34(11):2359–63.

    CAS  PubMed  Google Scholar 

  74. Marceau P, Biron S, Lebel S, Marceau S, Hould FS, Simard S, et al. Does bone change after biliopancreatic diversion? J Gastrointest Surg. 2002;6(5):690–8.

    PubMed  Google Scholar 

  75. Ammann P, Rizzoli R. Bone strength and its determinants. Osteoporosis Int. 2003;14:S13–8.

    Google Scholar 

  76. Lewiecki EM. Bone densitometry and vertebral fracture assessment. Current Osteoporo Rep. 2010;8(3):123–30.

    Google Scholar 

  77. Tothill P, Laskey MA, Orphanidou CI, van Wijk M. Anomalies in dual energy X-ray absorptiometry measurements of total-body bone mineral during weight change using lunar, hologic and norland instruments. Brit J Radiol. 1999;72(859):661–9.

    CAS  PubMed  Google Scholar 

  78. Van Loan MD, Johnson HL, Barbieri TF. Effect of weight loss on bone mineral content and bone mineral density in obese women. Am J Clin Nutr. 1998;67(4):734–8.

    PubMed  Google Scholar 

  79. 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.

    CAS  PubMed  Google Scholar 

  80. 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.

    PubMed  Google Scholar 

  81. Evans EM, Mojtahedi MC, Kessinger RB, Misic MM. Simulated change in body fatness affects Hologic QDR 4500A whole body and central DXA bone measures. J Clin Densitom. 2006;9(3):315–22.

    PubMed  Google Scholar 

  82. Svendsen OL, Haarbo J, Hassager C, Christiansen C. Accuracy of measurements of body composition by dual-energy X-ray absorptiometry in vivo. Am J Clin Nutr. 1993;57(5):605–8.

    CAS  PubMed  Google Scholar 

  83. Madsen OR, Jensen JEB, Sorensen OH. Validation of a dual energy X-ray absorptiometer: measurement of bone mass and soft tissue composition. Eur J Appl Physiol O. 1997;75(6):554–8.

    CAS  Google Scholar 

  84. Bolotin HH. DXA in vivo BMD methodology: an erroneous and misleading research and clinical gauge of bone mineral status, bone fragility, and bone remodelling. Bone. 2007;41(1):138–54.

    CAS  PubMed  Google Scholar 

  85. Tothill P. Dual-energy X-ray absorptiometry measurements of total-body bone mineral during weight change. J Clin Densitom. 2005;8(1):31–8.

    PubMed  Google Scholar 

  86. Binkley N, Krueger D, Vallarta-Ast N. An overlying fat panniculus affects femur bone mass measurement. J Clin Densitom. 2003;6(3):199–204.

    PubMed  Google Scholar 

  87. Yu EW, Bouxsein M, Roy AE, Baldwin C, Cange A, Neer RM, et al. Bone loss after bariatric surgery: Discordant results between DXA and QCT bone density. J Bone Miner Res. 2013. doi:10.1002/jbmr.2063.

  88. Center JR, White CP. Obesity: bariatric surgery, weight loss and bone. Nat Rev Endocrinol. 2013;9(11):630–2.

    PubMed  Google Scholar 

  89. Gilsanz V. Bone density in children: a review of the available techniques and indications. Eur J Radiol. 1998;26(2):177–82.

    CAS  PubMed  Google Scholar 

  90. Petit MA, Beck TJ, Shults J, Zemel BS, Foster BJ, Leonard MB. Proximal femur bone geometry is appropriately adapted to lean mass in overweight children and adolescents. Bone. 2005;36(3):568–76.

    PubMed  Google Scholar 

  91. Wetzsteon RJ, Petit MA, Macdonald HM, Hughes JM, Beck TJ, Mckay HA. Bone structure and volumetric BMD in overweight children: a longitudinal study. J Bone Miner Res. 2008;23(12):1946–53.

    PubMed  Google Scholar 

  92. Siu WS, Qin L, Leung KS. pQCT bone strength index may serve as a better predictor than bone mineral density for long bone breaking strength. J Bone Miner Metab. 2003;21(5):316–22.

    PubMed  Google Scholar 

  93. Madsen OR, Jensen JE, Sorensen OH. Validation of a dual energy X-ray absorptiometer: measurement of bone mass and soft tissue composition. Eur J Appl Physiol Occup Physiol. 1997;75(6):554–8.

    CAS  PubMed  Google Scholar 

  94. Olbers T, Bjorkman S, Lindroos A, Maleckas A, Lonn L, Sjostrom L, et al. Body composition, dietary intake, and energy expenditure after laparoscopic Roux-en-y gastric bypass and laparoscopic vertical banded gastroplasty—a randomized clinical trial. Ann Surg. 2006;244(5):715–22.

    PubMed Central  PubMed  Google Scholar 

  95. 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.

    CAS  PubMed  Google Scholar 

  96. Xanthakos SA. Nutritional Deficiencies in Obesity and After Bariatric Surgery. Pediatr Clin N Am. 2009;56(5):1105-+.

    Google Scholar 

  97. Ernst B, Thurnheer M, Schmid SM, Schultes B. Evidence for the necessity to systematically assess micronutrient status prior to bariatric surgery. Obes Surg. 2009;19(1):66–73.

    PubMed  Google Scholar 

  98. De Prisco C, Levine SN. Metabolic bone disease after gastric bypass surgery for obesity. Am J Med Sci. 2005;329(2):57–61.

    PubMed  Google Scholar 

  99. Compher CW, Badellino KO, Boullata JI. Vitamin D and the bariatric surgical patient: a review. Obes Surg. 2008;18(2):220–4.

    PubMed  Google Scholar 

  100. Manco M, Calvani M, Nanni G, Greco AV, Iaconelli A, Gasbarrini G, et al. Low 25-hydroxyvitamin D does not affect insulin sensitivity in obesity after bariatric surgery. Obes Res. 2005;13(10):1692–700.

    CAS  PubMed  Google Scholar 

  101. El-Kadre LJ, Rocha PR, de Almeida Tinoco AC, Tinoco RC. Calcium metabolism in pre- and postmenopausal morbidly obese women at baseline and after laparoscopic Roux-en-Y gastric bypass. Obes Surg. 2004;14(8):1062–6.

    PubMed  Google Scholar 

  102. Carlin AM, Rao DS, Yager KM, Genaw JA, Parikh NJ, Szymanski W. Effect of gastric bypass surgery on vitamin D nutritional status. Surg Obes Relat Dis. 2006;2(6):638–42.

    PubMed  Google Scholar 

  103. Ybarra J, Sanchez-Hernandez J, Gich I, De Leiva A, 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.

    PubMed  Google Scholar 

  104. Youssef Y, Richards WO, Sekhar N, Kaiser J, Spagnoli A, Abumrad N, et al. Risk of secondary hyperparathyroidism after laparoscopic gastric bypass surgery in obese women. Surg Endosc. 2007;21(8):1393–6.

    CAS  PubMed  Google Scholar 

  105. 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.

    CAS  PubMed  Google Scholar 

  106. Rizzoli R, Eisman JA, Norquist J, Ljunggren O, Krishnarajah G, Lim SK, et al. Risk factors for vitamin D inadequacy among women with osteoporosis: an international epidemiological study. Int J Clin Pract. 2006;60(8):1013–9.

    CAS  PubMed  Google Scholar 

  107. Parfitt AM, Podenphant J, Villanueva AR, Frame B. Metabolic bone-disease with and without osteomalacia after intestinal-bypass surgery—a bone histomorphometric study. Bone. 1985;6(4):211–20.

    CAS  PubMed  Google Scholar 

  108. Al-Shoha A, Qiu SJ, Palnitkar S, Rao DS. Osteomalacia with bone marrow fibrosis due to severe vitamin D deficiency after a gastrointestinal bypass operation for severe obesity. Endocr Pract. 2009;15(6):528–33.

    PubMed  Google Scholar 

  109. Aarts EO, Janssen IMC, Berends FJ. The gastric sleeve: losing weight as fast as micronutrients? Obes Surg. 2011;21(2):207–11.

    PubMed Central  PubMed  Google Scholar 

  110. Nadler EP, Youn HA, Ren CJ, Fielding GA. An update on 73 US obese pediatric patients treated with laparoscopic adjustable gastric banding: comorbidity resolution and compliance data. J Pediatr Surg. 2008;43(1):141–6.

    PubMed  Google Scholar 

  111. Mechanick JI, Youdim A, Jones DB, Garvey WT, Hurley DL, McMahon MM, et al. Clinical practice guidelines for the perioperative nutritional, metabolic, and nonsurgical support of the bariatric surgery patient–2013 update: cosponsored by American Association of Clinical Endocrinologists, The Obesity Society, and American Society for Metabolic & Bariatric Surgery. Obesity (Silver Spring). 2013;21(Suppl 1):S1–27.

    CAS  PubMed Central  PubMed  Google Scholar 

  112. Heaney RP. Functional indices of vitamin D status and ramifications of vitamin D deficiency. Am J Clin Nutr. 2004;80(6):1706s–9s.

    CAS  PubMed  Google Scholar 

  113. Skroubis G, Sakellaropoulos G, Pouggouras K, Mead N, Nikiforidis G, Kalfarentzos F. Comparison of nutritional deficiencies after Roux-en-Y gastric bypass and after biliopancreatic diversion with Roux-en-Y gastric bypass. Obes Surg. 2002;12(4):551–8.

    PubMed  Google Scholar 

  114. Dolan K, Hatzifotis M, Newbury L, Lowe N, Fielding G. A clinical and nutritional comparison of biliopancreatic diversion with and without duodenal switch. Ann Surg. 2004;240(1):51–6.

    PubMed Central  PubMed  Google Scholar 

  115. Conigrave AD, Brown EM, Rizzoli R. Dietary protein and bone health: roles of amino acid-sensing receptors in the control of calcium metabolism and bone homeostasis. Annual Rev Nutr. 2008;28:131–55.

    CAS  Google Scholar 

  116. Munger RG, Cerhan JR, Chiu BC. Prospective study of dietary protein intake and risk of hip fracture in postmenopausal women. Am J Clin Nutr. 1999;69(1):147–52.

    CAS  PubMed  Google Scholar 

  117. Kerstetter JE, Mitnick ME, Gundberg CM, Caseria DM, Ellison AF, Carpenter TO, et al. Changes in bone turnover in young women consuming different levels of dietary protein. J Clin Endocrinol Metabol. 1999;84(3):1052–5.

    CAS  Google Scholar 

  118. Kerstetter JE, O’Brien KO, Insogna KL. Dietary protein, calcium metabolism, and skeletal homeostasis revisited. Am J Clin Nutr. 2003;78(3 Suppl):584S–92S.

    CAS  PubMed  Google Scholar 

  119. Huang Z, Himes JH, McGovern PG. Nutrition and subsequent hip fracture risk among a national cohort of white women. Am J Epidemiol. 1996;144(2):124–34.

    CAS  PubMed  Google Scholar 

  120. Kerstetter JE, O’Brien KO, Caseria DM, Wall DE, Insogna KL. The impact of dietary protein on calcium absorption and kinetic measures of bone turnover in women. J Clin Endocrinol Metabol. 2005;90(1):26–31.

    CAS  Google Scholar 

  121. Heber D, Greenway FL, Kaplan LM, Livingston E, Salvador J, Still C, et al. Endocrine and nutritional management of the post-bariatric surgery patient: an Endocrine Society Clinical Practice Guideline. J Clin Endocrinol Metabol. 2010;95(11):4823–43.

    CAS  Google Scholar 

  122. Ilich JZ, Kerstetter JE. Nutrition in bone health revisited: a story beyond calcium. J Am Coll Nutr. 2000;19(6):715–37.

    CAS  PubMed  Google Scholar 

  123. Westerterp-Plantenga MS, Lemmens SG, Westerterp KR. Dietary protein—its role in satiety, energetics, weight loss and health. Br J Nutr. 2012;108(Suppl 2):S105–12.

    CAS  PubMed  Google Scholar 

  124. Oh KW, Lee WY, Rhee EJ, Baek KH, Yoon KH, Kang MI, et al. The relationship between serum resistin, leptin, adiponectin, ghrelin levels and bone mineral density in middle-aged men. Clin Endocrinol. 2005;63(2):131–8.

    CAS  Google Scholar 

  125. Zhao LJ, Liu YJ, Liu PY, Hamilton J, Recker RR, Deng HW. Relationship of obesity with osteoporosis. J Clin Endocr Metab. 2007;92(5):1640–6.

    CAS  PubMed Central  PubMed  Google Scholar 

  126. Karsenty G, Oury F. The central regulation of bone mass, the first link between bone remodeling and energy metabolism. J Clin Endocr Metab. 2010;95(11):4795–801.

    CAS  PubMed  Google Scholar 

  127. Wong IPL, Driessler F, Khor EC, Shi YC, Hormer B, Nguyen AD, et al. Peptide YY regulates bone remodeling in mice: a link between gut and skeletal biology. PLoS ONE. 2012;7(7):e40038.

    CAS  PubMed Central  PubMed  Google Scholar 

  128. Baldock PA, Lee NJ, Driessler F, Lin S, Allison S, Stehrer B, et al. Neuropeptide Y knockout mice reveal a central role of NPY in the coordination of bone mass to body weight. PLoS ONE. 2009;4(12):e8415.

    PubMed Central  PubMed  Google Scholar 

  129. Pieribone VA, Brodin L, Friberg K, Dahlstrand J, Soderberg C, Larhammar D, et al. Differential expression of mRNAs for neuropeptide Y-related peptides in rat nervous tissues: possible evolutionary conservation. J Neurosci Off J Soc Neurosci. 1992;12(9):3361–71.

    CAS  Google Scholar 

  130. Parker SL, Balasubramaniam A. Neuropeptide Y Y2 receptor in health and disease. Br J Pharmacol. 2008;153(3):420–31.

    CAS  PubMed Central  PubMed  Google Scholar 

  131. Batterham RL, Cohen MA, Ellis SM, Le Roux CW, Withers DJ, Frost GS, et al. Inhibition of food intake in obese subjects by peptide YY3-36. N Engl J Med. 2003;349(10):941–8.

    CAS  PubMed  Google Scholar 

  132. Olivan B, Teixeira J, Bose M, Bawa B, Chang T, Summe H, et al. Effect of weight loss by diet or gastric bypass surgery on peptide YY(3-36) levels. Ann Surg. 2009;249(6):948–53.

    PubMed Central  PubMed  Google Scholar 

  133. Valderas JP, Irribarra V, Boza C, de la Cruz R, Liberona Y, Acosta AM, et al. Medical and surgical treatments for obesity have opposite effects on peptide YY and appetite: a prospective study controlled for weight loss. J Clin Endocr Metab. 2010;95(3):1069–75.

    CAS  PubMed  Google Scholar 

  134. Bose M, Machineni S, Olivan B, Teixeira J, McGinty JJ, Bawa B, et al. Superior appetite hormone profile after equivalent weight loss by gastric bypass compared to gastric banding. Obesity. 2010;18(6):1085–91.

    CAS  PubMed Central  PubMed  Google Scholar 

  135. Boey D, Lin S, Enriquez RF, Lee NJ, Slack K, Couzens M, et al. PYY transgenic mice are protected against diet-induced and genetic obesity. Neuropeptides. 2008;42(1):19–30.

    CAS  PubMed  Google Scholar 

  136. Wortley KE, Garcia K, Okamoto H, Thabet K, Anderson KD, Shen V, et al. Peptide YY regulates bone turnover in rodents. Gastroenterology. 2007;133(5):1534–43.

    CAS  PubMed  Google Scholar 

  137. Yuzuriha H, Inui A, Asakawa A, Ueno N, Kasuga M, Meguid MM, et al. Gastrointestinal hormones (anorexigenic peptide YY and orexigenic ghrelin) influence neural tube development. Faseb J. 2007;21(9):2108–12.

    CAS  PubMed  Google Scholar 

  138. Misra M, Miller KK, Tsai P, Gallagher K, Lin A, Lee N, et al. Elevated peptide YY levels in adolescent girls with anorexia nervosa. J Clin Endocr Metab. 2006;91(3):1027–33.

    CAS  PubMed  Google Scholar 

  139. Utz AL, Lawson EA, Misra M, Mickley D, Gleysteen S, Herzog DB, et al. Peptide YY (PYY) levels and bone mineral density (BMD) in women with anorexia nervosa. Bone. 2008;43(1):135–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  140. Russell M, Stark J, Nayak S, Miller KK, Herzog DB, Klibanski A, et al. Peptide YY in adolescent athletes with amenorrhea, eumenorrheic athletes and non-athletic controls. Bone. 2009;45(1):104–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  141. Scheid JL, Toombs RJ, Ducher G, Gibbs JC, Williams NI, De Souza MJ. Estrogen and peptide YY are associated with bone mineral density in premenopausal exercising women. Bone. 2011;49(2):194–201.

    CAS  PubMed  Google Scholar 

  142. Hansen L, Deacon CF, Orskov C, Holst JJ. Glucagon-like peptide-1-(7-36)amide is transformed to glucagon-like peptide-1-(9-36)amide by dipeptidyl peptidase IV in the capillaries supplying the L cells of the porcine intestine. Endocrinology. 1999;140(11):5356–63.

    CAS  PubMed  Google Scholar 

  143. Gutzwiller JP, Goke B, Drewe J, Hildebrand P, Ketterer S, Handschin D, et al. Glucagon-like peptide-1: a potent regulator of food intake in humans. Gut. 1999;44(1):81–6.

    CAS  PubMed Central  PubMed  Google Scholar 

  144. Naslund E, Barkeling B, King N, Gutniak M, Blundell JE, Holst JJ, et al. Energy intake and appetite are suppressed by glucagon-like peptide-1 (GLP-1) in obese men. Int J Obes Relat Metab Disord J Int Assoc Study Obes. 1999;23(3):304–11.

    CAS  Google Scholar 

  145. Toft-Nielsen MB, Damholt MB, Madsbad S, Hilsted LM, Hughes TE, Michelsen BK, et al. Determinants of the impaired secretion of glucagon-like peptide-1 in type 2 diabetic patients. J Clin Endocrinol Metabol. 2001;86(8):3717–23.

    CAS  Google Scholar 

  146. Ranganath LR, Beety JM, Morgan LM, Wright JW, Howland R, Marks V. Attenuated GLP-1 secretion in obesity: cause or consequence? Gut. 1996;38(6):916–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  147. Feinle C, Chapman IM, Wishart J, Horowitz M. Plasma glucagon-like peptide-1 (GLP-1) responses to duodenal fat and glucose infusions in lean and obese men. Peptides. 2002;23(8):1491–5.

    CAS  PubMed  Google Scholar 

  148. Shak JR, Roper J, Perez-Perez GI, Tseng CH, Francois F, Gamagaris Z, et al. The effect of laparoscopic gastric banding surgery on plasma levels of appetite-control, insulinotropic, and digestive hormones. Obes Surg. 2008;18(9):1089–96.

    PubMed Central  PubMed  Google Scholar 

  149. Ram E, Vishne T, Diker D, Gal-Ad I, Maayan R, Lerner I, et al. Impact of gastric banding on plasma ghrelin, growth hormone, cortisol, DHEA and DHEA-S levels. Obes Surg. 2005;15(8):1118–23.

    PubMed  Google Scholar 

  150. Korner J, Inabnet W, Febres G, Conwell IM, McMahon DJ, Salas R, et al. Prospective study of gut hormone and metabolic changes after adjustable gastric banding and Roux-en-Y gastric bypass. Int J Obes (Lond). 2009;33(7):786–95.

    CAS  PubMed Central  Google Scholar 

  151. Bose M, Machineni S, Olivan B, Teixeira J, McGinty JJ, Bawa B, et al. Superior appetite hormone profile after equivalent weight loss by gastric bypass compared to gastric banding. Obesity (Silver Spring). 2010;18(6):1085–91.

    CAS  PubMed Central  PubMed  Google Scholar 

  152. Usinger L, Hansen KB, Kristiansen VB, Larsen S, Holst JJ, Knop FK. Gastric emptying of orally administered glucose solutions and incretin hormone responses are unaffected by laparoscopic adjustable gastric banding. Obes Surg. 2011;21(5):625–32.

    PubMed  Google Scholar 

  153. Peterli R, Wolnerhanssen B, Peters T, Devaux N, Kern B, Christoffel-Courtin C, et al. Improvement in glucose metabolism after bariatric surgery: comparison of laparoscopic Roux-en-Y gastric bypass and laparoscopic sleeve gastrectomy: a prospective randomized trial. Ann Surg. 2009;250(2):234–41.

    PubMed  Google Scholar 

  154. Valderas JP, Irribarra V, Rubio L, Boza C, Escalona M, Liberona Y, et al. Effects of sleeve gastrectomy and medical treatment for obesity on glucagon-like peptide 1 levels and glucose homeostasis in non-diabetic subjects. Obes Surg. 2011;21(7):902–9.

    PubMed  Google Scholar 

  155. Laferrere B, Teixeira J, McGinty J, Tran H, Egger JR, Colarusso A, et al. Effect of weight loss by gastric bypass surgery versus hypocaloric diet on glucose and incretin levels in patients with type 2 diabetes. J Clin Endocr Metab. 2008;93(7):2479–85.

    CAS  PubMed Central  PubMed  Google Scholar 

  156. Campos GM, Rabl C, Peeva S, Ciovica R, Rao M, Schwarz JM, et al. Improvement in peripheral glucose uptake after gastric bypass surgery is observed only after substantial weight loss has occurred and correlates with the magnitude of weight lost. J Gastrointest Surg. 2010;14(1):15–22.

    PubMed Central  PubMed  Google Scholar 

  157. Yamada C, Yamada Y, Tsukiyama K, Yamada K, Udagawa N, Takahashi N, et al. The murine glucagon-like peptide-1 receptor is essential for control of bone resorption. Endocrinology. 2008;149(2):574–9.

    CAS  PubMed  Google Scholar 

  158. Nuche-Berenguer B, Moreno P, Esbrit P, Dapia S, Caeiro JR, Cancelas J, et al. Effect of GLP-1 treatment on bone turnover in normal, type 2 diabetic, and insulin-resistant states. Calcified Tissue Int. 2009;84(6):453–61.

    CAS  Google Scholar 

  159. Inui A, Asakawa A, Bowers CY, Mantovani G, Laviano A, Meguid MM, et al. Ghrelin, appetite, and gastric motility: the emerging role of the stomach as an endocrine organ. Faseb J. 2004;18(3):439–56.

    CAS  PubMed  Google Scholar 

  160. Cummings DE, Purnell JQ, Frayo RS, Schmidova K, Wisse BE, Weigle DS. A preprandial rise in plasma ghrelin levels suggests a role in meal initiation in humans. Diabetes. 2001;50(8):1714–9.

    CAS  PubMed  Google Scholar 

  161. Nijhuis J, van Dielen FMH, Buurman WA, Greve JWM. Ghrelin, leptin and insulin levels after restrictive surgery: a 2-year follow-up study. Obes Surg. 2004;14(6):783–7.

    PubMed  Google Scholar 

  162. Bohdjalian A, Langer FB, Shakeri-Leidenmuhler S, Gfrerer L, Ludvik B, Zacherl J, et al. Sleeve gastrectomy as sole and definitive bariatric procedure: 5-year results for weight loss and ghrelin. Obes Surg. 2010;20(5):535–40.

    PubMed  Google Scholar 

  163. Geloneze B, Tambascia MA, Pilla VF, Geloneze SR, Repetto EM, Pareja JC. Ghrelin: a gut-brain hormone: effect of gastric bypass surgery. Obes Surg. 2003;13(1):17–22.

    PubMed  Google Scholar 

  164. Morinigo R, Casamitjana R, Moize V, Lacy AM, Delgado S, Gomis R, et al. Short-term effects of gastric bypass surgery on circulating ghrelin levels. Obes Res. 2004;12(7):1108–16.

    PubMed  Google Scholar 

  165. Stoeckli R, Chanda R, Langer I, Keller U. Changes of body weight and plasma ghrelin levels after gastric banding and gastric bypass. Obes Res. 2004;12(2):346–50.

    CAS  PubMed  Google Scholar 

  166. Faraj M, Havel PJ, Phelis S, Blank D, Sniderman AD, Cianflone K. Plasma acylation-stimulating protein, adiponectin, leptin, and ghrelin before and after weight loss induced by gastric bypass surgery in morbidly obese subjects. J Clin Endocr Metab. 2003;88(4):1594–602.

    CAS  PubMed  Google Scholar 

  167. Holdstock C, Engstrom BE, Ohrvall M, Lind L, Sundbom M, Karlsson FA. Ghrelin and adipose tissue regulatory peptides: effect of gastric bypass surgery in obese humans. J Clin Endocr Metab. 2003;88(7):3177–83.

    CAS  PubMed  Google Scholar 

  168. Vendrell J, Broch M, Vilarrasa N, Molina A, Gomez JM, Gutierrez C, et al. Resistin, adiponectin, ghrelin, leptin, and proinflammatory cytokines: relationships in obesity. Obes Res. 2004;12(6):962–71.

    CAS  PubMed  Google Scholar 

  169. Ohlsson C, Bengtsson BA, Isaksson OG, Andreassen TT, Slootweg MC. Growth hormone and bone. Endocr Rev. 1998;19(1):55–79.

    CAS  PubMed  Google Scholar 

  170. Wang DH, Hu YS, Du JJ, Hu YY, Zhong WD, Qin WJ. Ghrelin stimulates proliferation of human osteoblastic TE85 cells via NO/cGMP signaling pathway. Endocrine. 2009;35(1):112–7.

    CAS  PubMed  Google Scholar 

  171. Fukushima N, Hanada R, Teranishi H, Fukue Y, Tachibana T, Ishikawa H, et al. Ghrelin directly regulates bone formation. J Bone Miner Res. 2005;20(5):790–8.

    CAS  PubMed  Google Scholar 

  172. Biver E, Salliot C, Combescure C, Gossec L, Hardouin P, Legroux-Gerot I, et al. Influence of adipokines and ghrelin on bone mineral density and fracture risk: a systematic review and meta-analysis. J Clin Endocrinol Metabol. 2011;96(9):2703–13.

    CAS  Google Scholar 

  173. Nouh O, Abd Elfattah MM, Hassouna AA. Association between ghrelin levels and BMD: a cross sectional trial. Gynecol Endocrinol Off J Int Soc Gynecol Endocrinol. 2012;28(7):570–2.

    CAS  Google Scholar 

  174. Misra M, Miller KK, Stewart V, Hunter E, Kuo K, Herzog DB, et al. Ghrelin and bone metabolism in adolescent girls with anorexia nervosa and healthy adolescents. J Clin Endocr Metab. 2005;90(9):5082–7.

    CAS  PubMed  Google Scholar 

  175. Weiss LA, Langenberg C, Barrett-Connor E. Ghrelin and bone: is there an association in older adults?: the Rancho Bernardo study. J Bone Miner Res. 2006;21(5):752–7.

    CAS  PubMed  Google Scholar 

  176. Yokota T, Meka CS, Medina KL, Igarashi H, Comp PC, Takahashi M, et al. Paracrine regulation of fat cell formation in bone marrow cultures via adiponectin and prostaglandins. J Clin Invest. 2002;109(10):1303–10.

    CAS  PubMed Central  PubMed  Google Scholar 

  177. Holdstock C, Engstrom BE, Ohrvall M, Lind L, Sundbom M, Karlsson FA. Ghrelin and adipose tissue regulatory peptides: effect of gastric bypass surgery in obese humans. J Clin Endocrinol Metabol. 2003;88(7):3177–83.

    CAS  Google Scholar 

  178. Diez JJ, Iglesias P. The role of the novel adipocyte-derived hormone adiponectin in human disease. Eur J Endocrinol. 2003;148(3):293–300.

    CAS  PubMed  Google Scholar 

  179. Matsubara M, Maruoka S, Katayose S. Inverse relationship between plasma adiponectin and leptin concentrations in normal-weight and obese women. Eur J Endocrinol. 2002;147(2):173–80.

    CAS  PubMed  Google Scholar 

  180. Abbenhardt C, McTiernan A, Alfano CM, Wener MH, Campbell KL, Duggan C, et al. Effects of individual and combined dietary weight loss and exercise interventions in postmenopausal women on adiponectin and leptin levels. J Intern Med. 2013;274(2):163–75.

    CAS  PubMed Central  PubMed  Google Scholar 

  181. Luo XH, Guo LJ, Xie H, Yuan LQ, Wu XP, Zhou HD, et al. Adiponectin stimulates RANKL and inhibits OPG expression in human osteoblasts through the MAPK signaling pathway. J Bone Miner Res. 2006;21(10):1648–56.

    CAS  PubMed  Google Scholar 

  182. Wang Y, Lam KSL, Xu JY, Lu G, Xu LY, Cooper GJS, et al. Adiponectin inhibits cell proliferation by interacting with several growth factors in an oligomerization-dependent manner. J Biol Chem. 2005;280(18):18341–7.

    CAS  PubMed  Google Scholar 

  183. Yamauchi T, Kamon J, Waki H, Terauchi Y, Kubota N, Hara K, et al. The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat Med. 2001;7(8):941–6.

    CAS  PubMed  Google Scholar 

  184. Friedman JM, Halaas JL. Leptin and the regulation of body weight in mammals. Nature. 1998;395(6704):763–70.

    CAS  PubMed  Google Scholar 

  185. Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, Nyce MR, et al. Serum immunoreactive leptin concentrations in normal-weight and obese humans. N Engl J Med. 1996;334(5):292–5.

    CAS  PubMed  Google Scholar 

  186. Williams KW, Scott MM, Elmquist JK. From observation to experimentation: leptin action in the mediobasal hypothalamus. Am J Clin Nutr. 2009;89(3):985s–90s.

    CAS  PubMed Central  PubMed  Google Scholar 

  187. Zabrocka L, Raczynska S, Goyke E, Sledzinski Z, Swierczynski J. BMI is the main determinant of the circulating leptin in women after vertical banded gastroplasty. Obes Res. 2004;12(3):505–12.

    PubMed  Google Scholar 

  188. Ram E, Vishne T, Maayan R, Lerner I, Weizman A, Dreznik Z, et al. The relationship between BMI, plasma leptin, insulin and proinsulin before and after laparoscopic adjustable gastric banding. Obes Surg. 2005;15(10):1456–62.

    PubMed  Google Scholar 

  189. Edwards C, Hindle AK, Fu S, Brody F. Downregulation of leptin and resistin expression in blood following bariatric surgery. Surg Endosc. 2011;25(6):1962–8.

    PubMed  Google Scholar 

  190. Ducy P, Amling M, Takeda S, Priemel M, Schilling AF, Beil FT, et al. Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell. 2000;100(2):197–207.

    CAS  PubMed  Google Scholar 

  191. Thomas T, Burguera B. Is leptin the link between fat and bone mass? J Bone Miner Res. 2002;17(9):1563–9.

    CAS  PubMed  Google Scholar 

  192. Whipple T, Sharkey N, Demers L, Williams N. Leptin and the skeleton. Clin Endocrinol. 2002;57(6):701–11.

    CAS  Google Scholar 

  193. Steppan CM, Crawford DT, Chidsey-Frink KL, Ke HZ, Swick AG. Leptin is a potent stimulator of bone growth in ob/ob mice. Regul Pept. 2000;92(1–3):73–8.

    CAS  PubMed  Google Scholar 

  194. Burguera B, Hofbauer LC, Thomas T, Gori F, Evans GL, Khosla S, et al. Leptin reduces ovariectomy-induced bone loss in rats. Endocrinology. 2001;142(8):3546–53.

    CAS  PubMed  Google Scholar 

  195. Hamrick MW, Della-Fera MA, Choi YH, Pennington C, Baile CA. Leptin treatment induces loss of bone marrow adipocytes and increases bone formation in leptin-deficient ob/ob mice. J Bone Miner Res. 2005;20(6):994–1001.

    CAS  PubMed  Google Scholar 

  196. Takeda S, Elefteriou F, Levasseur R, Liu X, Zhao L, Parker KL, et al. Leptin regulates bone formation via the sympathetic nervous system. Cell. 2002;111(3):305–17.

    CAS  PubMed  Google Scholar 

  197. Baldock PA, Allison S, McDonald MM, Sainsbury A, Enriquez RF, Little DG, et al. Hypothalamic regulation of cortical bone mass: opposing activity of Y2 receptor and leptin pathways. J Bone Miner Res. 2006;21(10):1600–7.

    CAS  PubMed  Google Scholar 

  198. Baldock PA, Sainsbury A, Allison S, Lin EJD, Couzens M, Boey D, et al. Hypothalamic control of bone formation: distinct actions of leptin and Y2 receptor pathways. J Bone Miner Res. 2005;20(10):1851–7.

    CAS  PubMed  Google Scholar 

  199. Welt CK, Chan JL, Bullen J, Murphy R, Smith P, DePaoli AM, et al. Recombinant human leptin in women with hypothalamic amenorrhea. N Engl J Med. 2004;351(10):987–97.

    CAS  PubMed  Google Scholar 

  200. Simha V, Zerwekh JE, Sakhaee K, Garg A. Effect of subcutaneous leptin replacement therapy on bone metabolism in patients with generalized lipodystrophy. J Clin Endocr Metab. 2002;87(11):4942–5.

    CAS  PubMed  Google Scholar 

  201. Farooqi IS, Matarese G, Lord GM, Keogh JM, Lawrence E, Agwu C, et al. Beneficial effects of leptin on obesity, T cell hyporesponsiveness, and neuroendocrine/metabolic dysfunction of human congenital leptin deficiency. J Clin Invest. 2002;110(8):1093–103.

    CAS  PubMed Central  PubMed  Google Scholar 

  202. Chan JL, Mantzoros CS. Role of leptin in energy-deprivation states: normal human physiology and clinical implications for hypothalamic amenorrhoea and anorexia nervosa. Lancet. 2005;366(9479):74–85.

    CAS  PubMed  Google Scholar 

  203. Scatena M, Liaw L, Giachelli CM. Osteopontin: a multifunctional molecule regulating chronic inflammation and vascular disease. Arterioscler Thromb Vasc Biol. 2007;27(11):2302–9.

    CAS  PubMed  Google Scholar 

  204. Reinholt FP, Hultenby K, Oldberg A, Heinegard D. Osteopontin—a possible anchor of osteoclasts to bone. Proc Natl Acad Sci USA. 1990;87(12):4473–5.

    CAS  PubMed Central  PubMed  Google Scholar 

  205. Calvo MS, Eyre DR, Gundberg CM. Molecular basis and clinical application of biological markers of bone turnover. Endocr Rev. 1996;17(4):333–68.

    CAS  PubMed  Google Scholar 

  206. Ferron M, Hinoi E, Karsenty G, Ducy P. Osteocalcin differentially regulates beta cell and adipocyte gene expression and affects the development of metabolic diseases in wild-type mice. Proc Natl Acad Sci USA. 2008;105(13):5266–70.

    CAS  PubMed Central  PubMed  Google Scholar 

  207. Hofbauer LC, Schoppet M. Clinical implications of the osteoprotegerin/RANKL/RANK system for bone and vascular diseases. JAMA, J Am Med Assoc. 2004;292(4):490–5.

    CAS  Google Scholar 

  208. Ducy P, Desbois C, Boyce B, Pinero G, Story B, Dunstan C, et al. Increased bone formation in osteocalcin-deficient mice. Nature. 1996;382(6590):448–52.

    CAS  PubMed  Google Scholar 

  209. Lee NK, Sowa H, Hinoi E, Ferron M, Ahn JD, Confavreux C, et al. Endocrine regulation of energy metabolism by the skeleton. Cell. 2007;130(3):456–69.

    CAS  PubMed Central  PubMed  Google Scholar 

  210. Lee NK, Karsenty G. Reciprocal regulation of bone and energy metabolism. J Musculoskelet Neuron Interact. 2008;8(4):351.

    CAS  Google Scholar 

  211. Fernandez-Real JM, Izquierdo M, Ortega F, Gorostiaga E, Gomez-Ambrosi J, Moreno-Navarrete JM, et al. The relationship of serum osteocalcin concentration to insulin secretion, sensitivity, and disposal with hypocaloric diet and resistance training. J Clin Endocrinol Metabol. 2009;94(1):237–45.

    CAS  Google Scholar 

  212. Saleem U, Mosley TH Jr, Kullo IJ. Serum osteocalcin is associated with measures of insulin resistance, adipokine levels, and the presence of metabolic syndrome. Arterioscler Thromb Vasc Biol. 2010;30(7):1474–8.

    CAS  PubMed Central  PubMed  Google Scholar 

  213. Pittas AG, Harris SS, Eliades M, Stark P, Dawson-Hughes B. Association between serum osteocalcin and markers of metabolic phenotype. J Clin Endocrinol Metabol. 2009;94(3):827–32.

    CAS  Google Scholar 

  214. Alfadda AA, Masood A, Shaik SA, Dekhil H, Goran M. Association between osteocalcin, metabolic syndrome, and cardiovascular risk factors: role of total and undercarboxylated osteocalcin in patients with type 2 diabetes. Int J Endocrinol. 2013;2013:197519.

    PubMed Central  PubMed  Google Scholar 

  215. Booth SL, Centi A, Smith SR, Gundberg C. The role of osteocalcin in human glucose metabolism: marker or mediator? Nat Rev Endocrinol. 2013;9(1):43–55.

    CAS  PubMed  Google Scholar 

  216. Merlotti D, Gennari L, Dotta F, Lauro D, Nuti R. Mechanisms of impaired bone strength in type 1 and 2 diabetes. Nutr Metabol Cardiovasc Dis NMCD. 2010;20(9):683–90.

    CAS  Google Scholar 

  217. Schwetz V, Pieber T, Obermayer-Pietsch B. The endocrine role of the skeleton: background and clinical evidence. Eur J Endocrinol. 2012;166(6):959–67.

    CAS  PubMed  Google Scholar 

  218. van Bezooijen RL, Roelen BA, Visser A, van der Wee-Pals L, de Wilt E, Karperien M, et al. Sclerostin is an osteocyte-expressed negative regulator of bone formation, but not a classical BMP antagonist. J Exp Med. 2004;199(6):805–14.

    PubMed Central  PubMed  Google Scholar 

  219. Li X, Ominsky MS, Niu QT, Sun N, Daugherty B, D’Agostin D, et al. Targeted deletion of the sclerostin gene in mice results in increased bone formation and bone strength. J Bone Miner Res. 2008;23(6):860–9.

    PubMed  Google Scholar 

  220. Loots GG, Kneissel M, Keller H, Baptist M, Chang J, Collette NM, et al. Genomic deletion of a long-range bone enhancer misregulates sclerostin in Van Buchem disease. Genome Res. 2005;15(7):928–35.

    CAS  PubMed Central  PubMed  Google Scholar 

  221. Baron R, Rawadi G. Targeting the Wnt/beta-catenin pathway to regulate bone formation in the adult skeleton. Endocrinology. 2007;148(6):2635–43.

    CAS  PubMed  Google Scholar 

  222. Almeida M, Han L, Bellido T, Manolagas SC, Kousteni S. Wnt proteins prevent apoptosis of both uncommitted osteoblast progenitors and differentiated osteoblasts by beta-catenin-dependent and -independent signaling cascades involving Src/ERK and phosphatidylinositol 3-kinase/AKT. J Biol Chem. 2005;280(50):41342–51.

    CAS  PubMed  Google Scholar 

  223. Semenov M, Tamai K, He X. SOST is a ligand for LRP5/LRP6 and a Wnt signaling inhibitor. J Biol Chem. 2005;280(29):26770–5.

    CAS  PubMed  Google Scholar 

  224. Sutherland MK, Geoghegan JC, Yu C, Turcott E, Skonier JE, Winkler DG, et al. Sclerostin promotes the apoptosis of human osteoblastic cells: a novel regulation of bone formation. Bone. 2004;35(4):828–35.

    CAS  PubMed  Google Scholar 

  225. Beighton P, Barnard A, Hamersma H, van der Wouden A. The syndromic status of sclerosteosis and van Buchem disease. Clin Genet. 1984;25(2):175–81.

    CAS  PubMed  Google Scholar 

  226. Brunkow ME, Gardner JC, Van Ness J, Paeper BW, Kovacevich BR, Proll S, et al. Bone dysplasia sclerosteosis results from loss of the SOST gene product, a novel cystine knot-containing protein. Am J Human Genet. 2001;68(3):577–89.

    CAS  Google Scholar 

  227. Felson DT, Zhang Y, Hannan MT, Anderson JJ. Effects of weight and body mass index on bone mineral density in men and women: the Framingham study. J Bone Miner Res. 1993;8(5):567–73.

    CAS  PubMed  Google Scholar 

  228. Schoenau E, Frost HM. The “muscle-bone unit” in children and adolescents. Calcif Tissue Int. 2002;70(5):405–7.

    CAS  PubMed  Google Scholar 

  229. Robling AG, Niziolek PJ, Baldridge LA, Condon KW, Allen MR, Alam I, et al. Mechanical stimulation of bone in vivo reduces osteocyte expression of Sost/sclerostin. J Biol Chem. 2008;283(9):5866–75.

    CAS  PubMed  Google Scholar 

  230. Lin C, Jiang X, Dai Z, Guo X, Weng T, Wang J, et al. Sclerostin mediates bone response to mechanical unloading through antagonizing Wnt/beta-catenin signaling. J Bone Miner Res. 2009;24(10):1651–61.

    CAS  PubMed  Google Scholar 

  231. Gaudio A, Pennisi P, Bratengeier C, Torrisi V, Lindner B, Mangiafico RA, et al. Increased sclerostin serum levels associated with bone formation and resorption markers in patients with immobilization-induced bone loss. J Clin Endocrinol Metabol. 2010;95(5):2248–53.

    CAS  Google Scholar 

  232. Armamento-Villareal R, Sadler C, Napoli N, Shah K, Chode S, Sinacore DR, et al. Weight loss in obese older adults increases serum sclerostin and impairs hip geometry but both are prevented by exercise training. J Bone Miner Res. 2012;27(5):1215–21.

    CAS  PubMed Central  PubMed  Google Scholar 

  233. McClung MR, Grauer A, Boonen S, Bolognese MA, Brown JP, Diez-Perez A, et al. Romosozumab in postmenopausal women with low bone mineral density. N Engl J Med. 2014;370(5):412–20.

    Google Scholar 

  234. Nakamura KM, Haglind EG, Clowes JA, Achenbach SJ, Atkinson EJ, Melton LJ, 3rd, et al. Fracture risk following bariatric surgery: a population-based study. Osteopor International : a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA. 2013.

  235. 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. Br Med J. 2012;345.

  236. Goldner WS, O’Dorisio TM, Dillon JS, Mason EE. Severe metabolic bone disease as a long-term complication of obesity surgery. Obes Surg. 2002;12(5):685–92.

    PubMed  Google Scholar 

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Conflict of interest

Malgorzata Monika Brzozowska, Amanda Sainsbury, John A. Eisman, Paul A. Baldock, and Jacqueline R. Center declare that they have no conflict of interest.

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Authors and Affiliations

  1. Garvan Institute of Medical Research, Darlinghurst, NSW, Australia

    Malgorzata Monika Brzozowska, John A. Eisman, Paul A. Baldock & Jacqueline R. Center

  2. The Boden Institute of Obesity, Nutrition, Exercise & Eating Disorders, The University of Sydney, Sydney, NSW, Australia

    Amanda Sainsbury

  3. School of Medical Sciences, University of New South Wales, Kensington, NSW, Australia

    Amanda Sainsbury

  4. St Vincent’s Hospital Medical School, Darlinghurst, NSW, Australia

    John A. Eisman & Jacqueline R. Center

  5. School of Medicine, University of New South Wales, Kensington, NSW, Australia

    John A. Eisman, Paul A. Baldock & Jacqueline R. Center

  6. School of Medicine, University of Notre Dame, Sydney, NSW, Australia

    John A. Eisman

  7. Clinical School, St Vincent’s Hospital, Darlinghurst, NSW, Australia

    Paul A. Baldock

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  1. Malgorzata Monika Brzozowska
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  2. Amanda Sainsbury
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  3. John A. Eisman
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  5. Jacqueline R. Center
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Correspondence to Jacqueline R. Center.

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Brzozowska, M.M., Sainsbury, A., Eisman, J.A. et al. Bariatric Surgery and Bone Loss: Do We Need to Be Concerned?. Clinic Rev Bone Miner Metab 12, 207–227 (2014). https://doi.org/10.1007/s12018-014-9162-9

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