Skip to main content
Top
Published in: Obesity Surgery 1/2008

01-01-2008 | Research Article

Effects of Weight Loss on Bone Status after Bariatric Surgery: Association Between Adipokines and Bone Markers

Authors: Hélène Wucher, Cécile Ciangura, Christine Poitou, Sébastien Czernichow

Published in: Obesity Surgery | Issue 1/2008

Login to get access

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.
Literature
1.
go back to reference Ogden CL, Carroll MD, Curtin LR, et al. Prevalence of overweight and obesity in the United States, 1999–2004. JAMA 2006;295:1549–55.PubMedCrossRef Ogden CL, Carroll MD, Curtin LR, et al. Prevalence of overweight and obesity in the United States, 1999–2004. JAMA 2006;295:1549–55.PubMedCrossRef
3.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
4.
go back to reference Craig BM, Tseng DS. Cost-effectiveness of gastric bypass for severe obesity. Am J Med 2002;113:491–8.PubMedCrossRef Craig BM, Tseng DS. Cost-effectiveness of gastric bypass for severe obesity. Am J Med 2002;113:491–8.PubMedCrossRef
5.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
6.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
7.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
8.
go back to reference Elefteriou F, Ducy P. Control of body mass by leptin occurs through the sympathetic nervous system. Med Sci (Paris) 2003;19:391–3. Elefteriou F, Ducy P. Control of body mass by leptin occurs through the sympathetic nervous system. Med Sci (Paris) 2003;19:391–3.
9.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
10.
go back to reference Chapin BL, LeMar HJ Jr, Knodel DH, et al. Secondary hyperparathyroidism following biliopancreatic diversion. Arch Surg 1996;131:1048–52.PubMed Chapin BL, LeMar HJ Jr, Knodel DH, et al. Secondary hyperparathyroidism following biliopancreatic diversion. Arch Surg 1996;131:1048–52.PubMed
11.
go back to reference Compston JE, Horton LW, Laker MF, et al. Bone disease after jejuno-ileal bypass for obesity. Lancet 1978;2:1–4.PubMedCrossRef Compston JE, Horton LW, Laker MF, et al. Bone disease after jejuno-ileal bypass for obesity. Lancet 1978;2:1–4.PubMedCrossRef
12.
go back to reference Compston JE, Vedi S, Gianetta E, et al. Bone histomorphometry and vitamin D status after biliopancreatic bypass for obesity. Gastroenterology 1984;87:350–6.PubMed Compston JE, Vedi S, Gianetta E, et al. Bone histomorphometry and vitamin D status after biliopancreatic bypass for obesity. Gastroenterology 1984;87:350–6.PubMed
13.
go back to reference Marceau P, Biron S, Lebel S, et al. Does bone change after biliopancreatic diversion? J Gastrointest Surg 2002;6:690–8.PubMedCrossRef Marceau P, Biron S, Lebel S, et al. Does bone change after biliopancreatic diversion? J Gastrointest Surg 2002;6:690–8.PubMedCrossRef
14.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
15.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
16.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
17.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
18.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
19.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
20.
go back to reference 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.CrossRef 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.CrossRef
21.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
22.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
23.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
24.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
25.
go back to reference 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.PubMed 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.PubMed
26.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
27.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
28.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
29.
go back to reference 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.CrossRef 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.CrossRef
30.
go back to reference De PC, Levine SN. Metabolic bone disease after gastric bypass surgery for obesity. Am J Med Sci 2005;329:57–61.CrossRef De PC, Levine SN. Metabolic bone disease after gastric bypass surgery for obesity. Am J Med Sci 2005;329:57–61.CrossRef
31.
go back to reference Colquitt J, Clegg A, Sidhu M, et al. Surgery for morbid obesity. Cochrane Database Syst Rev 2003;CD003641. Colquitt J, Clegg A, Sidhu M, et al. Surgery for morbid obesity. Cochrane Database Syst Rev 2003;CD003641.
32.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
33.
go back to reference Buchwald H, Buchwald JN. Evolution of operative procedures for the management of morbid obesity 1950–2000. Obes Surg 2002;12:705–17.PubMedCrossRef Buchwald H, Buchwald JN. Evolution of operative procedures for the management of morbid obesity 1950–2000. Obes Surg 2002;12:705–17.PubMedCrossRef
34.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
35.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
36.
go back to reference Orozco P, Nolla JM. Associations between body morphology and bone mineral density in premenopausal women. Eur J Epidemiol 1997;13:919–24.PubMedCrossRef Orozco P, Nolla JM. Associations between body morphology and bone mineral density in premenopausal women. Eur J Epidemiol 1997;13:919–24.PubMedCrossRef
37.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
38.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
39.
go back to reference Teitelman M, Grotegut CA, Williams NN, et al. The impact of bariatric surgery on menstrual patterns. Obes Surg 2006;16:1457–63.PubMedCrossRef Teitelman M, Grotegut CA, Williams NN, et al. The impact of bariatric surgery on menstrual patterns. Obes Surg 2006;16:1457–63.PubMedCrossRef
40.
go back to reference Karsenty G. Convergence between bone and energy homeostases: leptin regulation of bone mass. Cell Metab 2006;4:341–8.PubMedCrossRef Karsenty G. Convergence between bone and energy homeostases: leptin regulation of bone mass. Cell Metab 2006;4:341–8.PubMedCrossRef
41.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
42.
go back to reference Ahima RS. Metabolic actions of adipocyte hormones: focus on adiponectin. Obesity (Silver Spring) 2006;14(Suppl 1):9S–15S. Ahima RS. Metabolic actions of adipocyte hormones: focus on adiponectin. Obesity (Silver Spring) 2006;14(Suppl 1):9S–15S.
43.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
44.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
45.
go back to reference 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.PubMed 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.PubMed
46.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
47.
go back to reference 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.PubMed 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.PubMed
48.
go back to reference Andersen RE, Wadden TA, Herzog RJ. Changes in bone mineral content in obese dieting women. Metabolism 1997;46:857–61.PubMedCrossRef Andersen RE, Wadden TA, Herzog RJ. Changes in bone mineral content in obese dieting women. Metabolism 1997;46:857–61.PubMedCrossRef
49.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
50.
go back to reference 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.PubMed 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.PubMed
51.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
52.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
Metadata
Title
Effects of Weight Loss on Bone Status after Bariatric Surgery: Association Between Adipokines and Bone Markers
Authors
Hélène Wucher
Cécile Ciangura
Christine Poitou
Sébastien Czernichow
Publication date
01-01-2008
Publisher
Springer-Verlag
Published in
Obesity Surgery / Issue 1/2008
Print ISSN: 0960-8923
Electronic ISSN: 1708-0428
DOI
https://doi.org/10.1007/s11695-007-9258-0

Other articles of this Issue 1/2008

Obesity Surgery 1/2008 Go to the issue