Abstract
Background
The prevalence of overweight and obesity is increasing dramatically worldwide. As a consequence, bariatric surgery for morbid obesity is in constant development. Although bariatric surgery has proven its efficiency at achieving weight loss and correcting comorbidities, it may cause vitamin deficiencies and subsequent complications. The goal of this review is to assess the impact of obesity surgery on bone metabolism and to analyze the underlying mechanisms and relationships with adipokines. Our review focuses on gastric banding, vertical banded gastroplasty, and gastric bypass.
Methods
The articles were located via PubMed database, using the key words “bariatric surgery,” “weight loss,” “bone loss,” and “bone metabolism” and published until May 2006.
Results
Five main studies were reviewed concerning gastric banding and six concerning Roux-en-Y gastric bypass. An early increase in bone markers (formation and resorption) is constantly found, prevailing on bone resorption, and resulting in early bone loss.
Conclusion
According to the few studies available, bone loss frequently occurs after bariatric surgery and particularly in a more pronounced way after gastric bypass, but its clinical significance is still under discussion. In addition, the physiopathology of these changes remains unclear, but could implicate adipokines such as leptin and adiponectin.
Similar content being viewed by others
References
Ogden CL, Carroll MD, Curtin LR, et al. Prevalence of overweight and obesity in the United States, 1999–2004. JAMA 2006;295:1549–55.
James PT. Obesity: the worldwide epidemic. Clin Dermatol 2004;22:276–80.
Sjostrom L, Lindroos AK, Peltonen M, et al. Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. N Engl J Med 2004;351:2683–93.
Craig BM, Tseng DS. Cost-effectiveness of gastric bypass for severe obesity. Am J Med 2002;113:491–8.
Sampalis JS, Liberman M, Auger S, et al. The impact of weight reduction surgery on health-care costs in morbidly obese patients. Obes Surg 2004;14:939–47.
Shah M, Simha V, Garg A. Review: long-term impact of bariatric surgery on body weight, comorbidities, and nutritional status. J Clin Endocrinol Metab 2006;91:4223–31.
Ducy P, Amling M, Takeda S, et al. Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell 2000;100:197–207.
Elefteriou F, Ducy P. Control of body mass by leptin occurs through the sympathetic nervous system. Med Sci (Paris) 2003;19:391–3.
Lenchik L, Register TC, Hsu FC, et al. Adiponectin as a novel determinant of bone mineral density and visceral fat. Bone 2003;33:646–51.
Chapin BL, LeMar HJ Jr, Knodel DH, et al. Secondary hyperparathyroidism following biliopancreatic diversion. Arch Surg 1996;131:1048–52.
Compston JE, Horton LW, Laker MF, et al. Bone disease after jejuno-ileal bypass for obesity. Lancet 1978;2:1–4.
Compston JE, Vedi S, Gianetta E, et al. Bone histomorphometry and vitamin D status after biliopancreatic bypass for obesity. Gastroenterology 1984;87:350–6.
Marceau P, Biron S, Lebel S, et al. Does bone change after biliopancreatic diversion? J Gastrointest Surg 2002;6:690–8.
Newbury L, Dolan K, Hatzifotis M, et al. Calcium and vitamin D depletion and elevated parathyroid hormone following biliopancreatic diversion. Obes Surg 2003;13:893–5.
Shaker JL, Norton AJ, Woods MF, et al. Secondary hyperparathyroidism and osteopenia in women following gastric exclusion surgery for obesity. Osteoporos Int 1991;1:177–81.
Slater GH, Ren CJ, Siegel N, et al. Serum fat-soluble vitamin deficiency and abnormal calcium metabolism after malabsorptive bariatric surgery. J Gastrointest Surg 2004;8:48–55.
Vage V, Solhaug JH, Berstad A, et al. Jejunoileal bypass in the treatment of morbid obesity: a 25-year follow-up study of 36 patients. Obes Surg 2002;12:312–8.
Vage V, Gjesdal CG, Eide GE, et al. Bone mineral density in females after jejunoileal bypass: a 25-year follow-up study. Obes Surg 2004;14:305–12.
Cundy T, Evans MC, Kay RG, et al. Effects of vertical-banded gastroplasty on bone and mineral metabolism in obese patients. Br J Surg 1996;83:1468–72.
Giusti V, Gasteyger C, Suter M, et al. Gastric banding induces negative bone remodelling in the absence of secondary hyperparathyroidism: potential role of serum C telopeptides for follow-up. Int J Obes (Lond) 2005;29:1429–35.
Guney E, Kisakol G, Ozgen G, et al. Effect of weight loss on bone metabolism: comparison of vertical banded gastroplasty and medical intervention. Obes Surg 2003;13:383–8.
Pugnale N, Giusti V, Suter M, et al. Bone metabolism and risk of secondary hyperparathyroidism 12 months after gastric banding in obese pre-menopausal women. Int J Obes Relat Metab Disord 2003;27:110–6.
Strauss BJ, Marks SJ, Growcott JP, et al. Body composition changes following laparoscopic gastric banding for morbid obesity. Acta Diabetol 2003;40(Suppl 1):S266–9.
Coates PS, Fernstrom JD, Fernstrom MH, et al. Gastric bypass surgery for morbid obesity leads to an increase in bone turnover and a decrease in bone mass. J Clin Endocrinol Metab 2004;89:1061–5.
Goode LR, Brolin RE, Chowdhury HA, et al. Bone and gastric bypass surgery: effects of dietary calcium and vitamin D. Obes Res 2004;12:40–7.
Johnson JM, Maher JW, Samuel I, et al. Effects of gastric bypass procedures on bone mineral density, calcium, parathyroid hormone, and vitamin D. J Gastrointest Surg 2005;9:1106–10.
Johnson JM, Maher JW, DeMaria EJ, et al. The long-term effects of gastric bypass on vitamin D metabolism. Ann Surg 2006;243:701–4.
Ott MT, Fanti P, Malluche HH, et al. Biochemical evidence of metabolic bone disease in women following Roux-Y gastric bypass for morbid obesity. Obes Surg 1992;2:341–8.
von Mach MA, Stoeckli R, Bilz S, et al. Changes in bone mineral content after surgical treatment of morbid obesity. Metabolism 2004;53:918–21.
De PC, Levine SN. Metabolic bone disease after gastric bypass surgery for obesity. Am J Med Sci 2005;329:57–61.
Colquitt J, Clegg A, Sidhu M, et al. Surgery for morbid obesity. Cochrane Database Syst Rev 2003;CD003641.
Sahota O, Mundey MK, San P, et al. The relationship between vitamin D and parathyroid hormone: calcium homeostasis, bone turnover, and bone mineral density in postmenopausal women with established osteoporosis. Bone 2004;35:312–9.
Buchwald H, Buchwald JN. Evolution of operative procedures for the management of morbid obesity 1950–2000. Obes Surg 2002;12:705–17.
Liel Y, Edwards J, Shary J, et al. The effects of race and body habitus on bone mineral density of the radius, hip, and spine in premenopausal women. J Clin Endocrinol Metab 1988;66:1247–50.
Mazess RB, Barden HS, Drinka PJ, et al. Influence of age and body weight on spine and femur bone mineral density in U.S. white men. J Bone Miner Res 1990;5:645–52.
Orozco P, Nolla JM. Associations between body morphology and bone mineral density in premenopausal women. Eur J Epidemiol 1997;13:919–24.
Bell NH, Epstein S, Greene A, et al. Evidence for alteration of the vitamin D-endocrine system in obese subjects. J Clin Invest 1985;76:370–3.
Bastounis EA, Karayiannakis AJ, Syrigos K, et al. Sex hormone changes in morbidly obese patients after vertical banded gastroplasty. Eur Surg Res 1998;30:43–7.
Teitelman M, Grotegut CA, Williams NN, et al. The impact of bariatric surgery on menstrual patterns. Obes Surg 2006;16:1457–63.
Karsenty G. Convergence between bone and energy homeostases: leptin regulation of bone mass. Cell Metab 2006;4:341–8.
Elefteriou F, Ahn JD, Takeda S, et al. Leptin regulation of bone resorption by the sympathetic nervous system and CART. Nature 2005;434:514–20.
Ahima RS. Metabolic actions of adipocyte hormones: focus on adiponectin. Obesity (Silver Spring) 2006;14(Suppl 1):9S–15S.
Luo XH, Guo LJ, Yuan LQ, et al. Adiponectin stimulates human osteoblasts proliferation and differentiation via the MAPK signaling pathway. Exp Cell Res 2005;309:99–109.
Luo XH, Guo LJ, Xie H, et al. Adiponectin stimulates RANKL and inhibits OPG expression in human osteoblasts through the MAPK signaling pathway. J Bone Miner Res 2006;21:1648–56.
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;67:734–8.
Tothill P, Hannan WJ, Cowen S, et al. Anomalies in the measurement of changes in total-body bone mineral by dual-energy X-ray absorptiometry during weight change. J Bone Miner Res 1997;12:1908–21.
Tothill P, Laskey MA, Orphanidou CI, et al. Anomalies in dual energy X-ray absorptiometry measurements of total-body bone mineral during weight change using Lunar, Hologic and Norland instruments. Br J Radiol 1999;72:661–69.
Andersen RE, Wadden TA, Herzog RJ. Changes in bone mineral content in obese dieting women. Metabolism 1997;46:857–61.
Gotfredsen A, Westergren HH, Andersen T. Influence of orlistat on bone turnover and body composition. Int J Obes Relat Metab Disord 2001;25:1154–60.
Ricci TA, Heymsfield SB, Pierson RN Jr, et al. Moderate energy restriction increases bone resorption in obese postmenopausal women. Am J Clin Nutr 2001;73:347–52.
De Laet C, Kanis JA, Oden A, et al. Body mass index as a predictor of fracture risk: a meta-analysis. Osteoporos Int 2005;16:1330–8.
Johnell O, Kanis JA, Oden A, et al. Predictive value of BMD for hip and other fractures. J Bone Miner Res 2005;20:1185–94.
Acknowledgment
We would like to thank Stacie Chat-Yung, MS, RD for her assistance with editing and translation in English.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wucher, H., Ciangura, C., Poitou, C. et al. Effects of Weight Loss on Bone Status after Bariatric Surgery: Association Between Adipokines and Bone Markers. OBES SURG 18, 58–65 (2008). https://doi.org/10.1007/s11695-007-9258-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11695-007-9258-0