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Published in: Obesity Surgery 8/2015

01-08-2015 | Original Contributions

Markers of Bone Metabolism in Obese Individuals Undergoing Laparoscopic Sleeve Gastrectomy

Authors: Asja E. Schollenberger, Jaana M. Heinze, Tobias Meile, Andreas Peter, Alfred Königsrainer, Stephan C. Bischoff

Published in: Obesity Surgery | Issue 8/2015

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Abstract

Background

Besides its advantages, bariatric surgery implicates a risk of nutritional deficiencies, which might result in impaired bone metabolism. We assessed the effect of laparoscopic sleeve gastrectomy (LSG) on blood markers of bone metabolism in obese patients during a 3-year observation period.

Methods

In 39 obese patients (29 women, 10 men, mean BMI 51.8 ± 6.8 kg/m2) undergoing LSG, we measured blood concentrations of 25-hydroxyvitamin D (25(OH)D), calcium, parathyroid hormone (PTH), bone alkaline phosphatase (BAP), and N-telopeptides crosslinks (NTx) before LSG and up to 3 years postoperatively. Vitamin D and calcium supplementations were recorded.

Results

LSG caused an excess weight loss (EWL) of 54 ± 20 % after 3 years. Before surgery, we found decreased levels of 25(OH)D and calcium in 80 and 5 % of the subjects, respectively, while increased levels of PTH, BAP, and NTx were found in 39, 28, and 21 %, respectively. Mean levels of NTx and the prevalence of elevated levels of NTx increased within 2 years (p < 0.001 and p < 0.01). Neither mean blood concentrations of 25(OH)D, calcium, PTH, and BAP nor relative prevalence of deficiencies regarding these markers changed during the study period. The supplementation rates of calcium and vitamin D increased postoperatively.

Conclusions

Morbid obesity is associated with pronounced changes of markers of bone metabolism; LSG did neither aggravate nor ameliorate vitamin D metabolism within a 3-year time period, but led to increased bone resorption 2 years postoperatively. Routine supplementation of calcium and vitamin D is not likely sufficient to compensate the obesity-associated deficiencies in bone metabolism.
Literature
1.
go back to reference Sjöström L, Lindroos A, Peltonen M, Sullivan M, Wedel H, et al. Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. N Engl J Med. 2004;351(26):2683–93.PubMedCrossRef Sjöström L, Lindroos A, Peltonen M, Sullivan M, Wedel H, et al. Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. N Engl J Med. 2004;351(26):2683–93.PubMedCrossRef
2.
go back to reference Peterli R, Borbély Y, Kern B, et al. Early results of the Swiss Multicentre Bypass or Sleeve Study (SM-BOSS): a prospective randomized trial comparing laparoscopic sleeve gastrectomy and Roux-en-Y gastric bypass. Ann Surg. 2013;258(5):690–4. discussion 695.PubMedCentralPubMedCrossRef Peterli R, Borbély Y, Kern B, et al. Early results of the Swiss Multicentre Bypass or Sleeve Study (SM-BOSS): a prospective randomized trial comparing laparoscopic sleeve gastrectomy and Roux-en-Y gastric bypass. Ann Surg. 2013;258(5):690–4. discussion 695.PubMedCentralPubMedCrossRef
3.
go back to reference Sjöström L. Review of the key results from the Swedish Obese Subjects (SOS) trial—a prospective controlled intervention study of bariatric surgery. J Intern Med. 2013;273(3):219–34. PMID: 23163728.PubMedCrossRef Sjöström L. Review of the key results from the Swedish Obese Subjects (SOS) trial—a prospective controlled intervention study of bariatric surgery. J Intern Med. 2013;273(3):219–34. PMID: 23163728.PubMedCrossRef
4.
go back to reference Sjöström L, Peltonen M, Jacobson P, et al. Bariatric surgery and long-term cardiovascular events. JAMA. 2012;307(1):56–65.PubMedCrossRef Sjöström L, Peltonen M, Jacobson P, et al. Bariatric surgery and long-term cardiovascular events. JAMA. 2012;307(1):56–65.PubMedCrossRef
5.
go back to reference Saltzman E, Karl JP. Nutrient deficiencies after gastric bypass surgery. Annu Rev Nutr. 2013;33:183–203.PubMedCrossRef Saltzman E, Karl JP. Nutrient deficiencies after gastric bypass surgery. Annu Rev Nutr. 2013;33:183–203.PubMedCrossRef
6.
go back to reference Skroubis G, Kouri N, Mead N, et al. Long-term results of a prospective comparison of Roux-en-Y gastric bypass versus a variant of biliopancreatic diversion in a non-superobese population (BMI 35–50 kg/m(2)). Obes Surg. 2014;24(2):197–204. PMID: 24105406.PubMedCrossRef Skroubis G, Kouri N, Mead N, et al. Long-term results of a prospective comparison of Roux-en-Y gastric bypass versus a variant of biliopancreatic diversion in a non-superobese population (BMI 35–50 kg/m(2)). Obes Surg. 2014;24(2):197–204. PMID: 24105406.PubMedCrossRef
7.
go back to reference Damms-Machado A, Friedrich A, Kramer KM, et al. Pre- and postoperative nutritional deficiencies in obese patients undergoing laparoscopic sleeve gastrectomy. Obes Surg. 2012;22(6):881–9. PMID: 22403000.PubMedCrossRef Damms-Machado A, Friedrich A, Kramer KM, et al. Pre- and postoperative nutritional deficiencies in obese patients undergoing laparoscopic sleeve gastrectomy. Obes Surg. 2012;22(6):881–9. PMID: 22403000.PubMedCrossRef
8.
go back to reference Friedrich AE, Damms-Machado A, Meile T, et al. Laparoscopic sleeve gastrectomy compared to a multidisciplinary weight loss program for obesity—effects on body composition and protein status. Obes Surg. 2013;23(12):1957–65. PMID: 23856991.PubMedCrossRef Friedrich AE, Damms-Machado A, Meile T, et al. Laparoscopic sleeve gastrectomy compared to a multidisciplinary weight loss program for obesity—effects on body composition and protein status. Obes Surg. 2013;23(12):1957–65. PMID: 23856991.PubMedCrossRef
9.
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(1):40–7. PMID: 14742841.PubMedCrossRef Goode LR, Brolin RE, Chowdhury HA, et al. Bone and gastric bypass surgery: effects of dietary calcium and vitamin D. Obes Res. 2004;12(1):40–7. PMID: 14742841.PubMedCrossRef
10.
go back to reference Sinha N, Shieh A, Stein EM, 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.CrossRef Sinha N, Shieh A, Stein EM, 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.CrossRef
11.
go back to reference Vilarrasa N, San José P, García I, 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.PubMedCrossRef Vilarrasa N, San José P, García I, 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.PubMedCrossRef
12.
go back to reference Ruiz-Tovar J, Oller I, Tomas A, et al. Mid-term effects of sleeve gastrectomy on calcium metabolism parameters, vitamin D and parathormone (PTH) in morbid obese women. Obes Surg. 2012;22(5):797–801.PubMedCrossRef Ruiz-Tovar J, Oller I, Tomas A, et al. Mid-term effects of sleeve gastrectomy on calcium metabolism parameters, vitamin D and parathormone (PTH) in morbid obese women. Obes Surg. 2012;22(5):797–801.PubMedCrossRef
13.
go back to reference Pluskiewicz W, Bužga M, Holéczy P, et al. 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. PMID: 22555865.PubMedCentralPubMedCrossRef Pluskiewicz W, Bužga M, Holéczy P, et al. 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. PMID: 22555865.PubMedCentralPubMedCrossRef
14.
go back to reference Ruiz-Tovar J, Oller I, Priego P, et al. Short- and mid-term changes in bone mineral density after laparoscopic sleeve gastrectomy. Obes Surg. 2013;23(7):861–6. PMID: 23315187.PubMedCrossRef Ruiz-Tovar J, Oller I, Priego P, et al. Short- and mid-term changes in bone mineral density after laparoscopic sleeve gastrectomy. Obes Surg. 2013;23(7):861–6. PMID: 23315187.PubMedCrossRef
15.
go back to reference Carrasco F, Basfi-Fer K, Rojas P, et al. Changes in bone mineral density after sleeve gastrectomy or gastric bypass: relationships with variations in vitamin D, ghrelin, and adiponectin levels. Obes Surg. 2014;24(6):877–84. PMID: 24435517.PubMedCrossRef Carrasco F, Basfi-Fer K, Rojas P, et al. Changes in bone mineral density after sleeve gastrectomy or gastric bypass: relationships with variations in vitamin D, ghrelin, and adiponectin levels. Obes Surg. 2014;24(6):877–84. PMID: 24435517.PubMedCrossRef
16.
go back to reference Vix M, Liu K, Diana M, et al. Impact of Roux-en-Y gastric bypass versus sleeve gastrectomy on vitamin D metabolism: short-term results from a prospective randomized clinical trial. Surg Endosc. 2014;28(3):821–6. PMID: 24196556.PubMedCrossRef Vix M, Liu K, Diana M, et al. Impact of Roux-en-Y gastric bypass versus sleeve gastrectomy on vitamin D metabolism: short-term results from a prospective randomized clinical trial. Surg Endosc. 2014;28(3):821–6. PMID: 24196556.PubMedCrossRef
17.
go back to reference Nogués X, Goday A, Peña MJ, et al. Pérdida de masa ósea tras gastrectomía tubular: estudio prospectivo comparativo con el bypass gástrico. Cir Esp. 2010;88(2):103–9.PubMedCrossRef Nogués X, Goday A, Peña MJ, et al. Pérdida de masa ósea tras gastrectomía tubular: estudio prospectivo comparativo con el bypass gástrico. Cir Esp. 2010;88(2):103–9.PubMedCrossRef
18.
go back to reference Buffington W, Cowan S. Vitamin D deficiency in the morbidly obese. Obes Surg. 1993;3(4):421–4. PMID: 10757956.PubMedCrossRef Buffington W, Cowan S. Vitamin D deficiency in the morbidly obese. Obes Surg. 1993;3(4):421–4. PMID: 10757956.PubMedCrossRef
19.
go back to reference Snijder MB, van Dam RM, Visser M, et al. Adiposity in relation to vitamin D status and parathyroid hormone levels: a population-based study in older men and women. J Clin Endocrinol Metab. 2005;90(7):4119–23.PubMedCrossRef Snijder MB, van Dam RM, Visser M, et al. Adiposity in relation to vitamin D status and parathyroid hormone levels: a population-based study in older men and women. J Clin Endocrinol Metab. 2005;90(7):4119–23.PubMedCrossRef
21.
go back to reference Hamoui N, Anthone G, Crookes PF. Calcium metabolism in the morbidly obese. Obes Surg. 2004;14(1):9–12.PubMedCrossRef Hamoui N, Anthone G, Crookes PF. Calcium metabolism in the morbidly obese. Obes Surg. 2004;14(1):9–12.PubMedCrossRef
22.
go back to reference Grethen E, Hill KM, Jones R, et al. Serum leptin, parathyroid hormone, 1,25-dihydroxyvitamin D, fibroblast growth factor 23, bone alkaline phosphatase, and sclerostin relationships in obesity. J Clin Endocrinol Metab. 2012;97(5):1655–62.PubMedCentralPubMedCrossRef Grethen E, Hill KM, Jones R, et al. Serum leptin, parathyroid hormone, 1,25-dihydroxyvitamin D, fibroblast growth factor 23, bone alkaline phosphatase, and sclerostin relationships in obesity. J Clin Endocrinol Metab. 2012;97(5):1655–62.PubMedCentralPubMedCrossRef
23.
go back to reference Kueper MA, Kramer KM, Kirschniak A, et al. Laparoscopic sleeve gastrectomy: standardized technique of a potential stand-alone bariatric procedure in morbidly obese patients. World J Surg. 2008;32(7):1462–5.PubMedCrossRef Kueper MA, Kramer KM, Kirschniak A, et al. Laparoscopic sleeve gastrectomy: standardized technique of a potential stand-alone bariatric procedure in morbidly obese patients. World J Surg. 2008;32(7):1462–5.PubMedCrossRef
24.
25.
go back to reference Pinheiro JC, Bates DM. Mixed-effects models in S and S-PLUS. New York: Springer; 2000.CrossRef Pinheiro JC, Bates DM. Mixed-effects models in S and S-PLUS. New York: Springer; 2000.CrossRef
26.
go back to reference Chang S, Stoll CRT, Song J, et al. The effectiveness and risks of bariatric surgery: an updated systematic review and meta-analysis, 2003–2012. JAMA Surg. 2014;149(3):275–87.PubMedCentralPubMedCrossRef Chang S, Stoll CRT, Song J, et al. The effectiveness and risks of bariatric surgery: an updated systematic review and meta-analysis, 2003–2012. JAMA Surg. 2014;149(3):275–87.PubMedCentralPubMedCrossRef
27.
go back to reference Saif T, Strain GW, Dakin G, et al. Evaluation of nutrient status after laparoscopic sleeve gastrectomy 1, 3, and 5 years after surgery. Surg Obes Relat Dis. 2012;8(5):542–7.PubMedCrossRef Saif T, Strain GW, Dakin G, et al. Evaluation of nutrient status after laparoscopic sleeve gastrectomy 1, 3, and 5 years after surgery. Surg Obes Relat Dis. 2012;8(5):542–7.PubMedCrossRef
28.
go back to reference Hewitt S, Søvik TT, Aasheim ET, et al. Secondary hyperparathyroidism, vitamin D sufficiency, and serum calcium 5 years after gastric bypass and duodenal switch. Obes Surg. 2013;23(3):384–90.PubMedCrossRef Hewitt S, Søvik TT, Aasheim ET, et al. Secondary hyperparathyroidism, vitamin D sufficiency, and serum calcium 5 years after gastric bypass and duodenal switch. Obes Surg. 2013;23(3):384–90.PubMedCrossRef
29.
go back to reference Bruno C, Fulford AD, Potts JR, 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 Endocrinol Metab. 2010;95(1):159–66.PubMedCentralPubMedCrossRef Bruno C, Fulford AD, Potts JR, 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 Endocrinol Metab. 2010;95(1):159–66.PubMedCentralPubMedCrossRef
30.
go back to reference Braghetto I, Davanzo C, Korn O, et al. Scintigraphic evaluation of gastric emptying in obese patients submitted to sleeve gastrectomy compared to normal subjects. Obes Surg. 2009;19(11):1515–21.PubMedCrossRef Braghetto I, Davanzo C, Korn O, et al. Scintigraphic evaluation of gastric emptying in obese patients submitted to sleeve gastrectomy compared to normal subjects. Obes Surg. 2009;19(11):1515–21.PubMedCrossRef
31.
go back to reference Melissas J, Koukouraki S, Askoxylakis J, et al. Sleeve gastrectomy: a restrictive procedure? Obes Surg. 2007;17(1):57–62.PubMedCrossRef Melissas J, Koukouraki S, Askoxylakis J, et al. Sleeve gastrectomy: a restrictive procedure? Obes Surg. 2007;17(1):57–62.PubMedCrossRef
33.
go back to reference Lin E, Armstrong-Moore D, Liang Z, et al. Contribution of adipose tissue to plasma 25-hydroxyvitamin D concentrations during weight loss following gastric bypass surgery. Obesity (Silver Spring). 2011;19(3):588–94.CrossRef Lin E, Armstrong-Moore D, Liang Z, et al. Contribution of adipose tissue to plasma 25-hydroxyvitamin D concentrations during weight loss following gastric bypass surgery. Obesity (Silver Spring). 2011;19(3):588–94.CrossRef
34.
go back to reference Ross PD, Knowlton W. Rapid bone loss is associated with increased levels of biochemical markers. J Bone Miner Res. 1998;13(2):297–302.PubMedCrossRef Ross PD, Knowlton W. Rapid bone loss is associated with increased levels of biochemical markers. J Bone Miner Res. 1998;13(2):297–302.PubMedCrossRef
35.
36.
go back to reference Hedlund LR, Gallagher JC. The effect of age and menopause on bone mineral density of the proximal femur. J Bone Miner Res. 1989;4(4):639–42.PubMedCrossRef Hedlund LR, Gallagher JC. The effect of age and menopause on bone mineral density of the proximal femur. J Bone Miner Res. 1989;4(4):639–42.PubMedCrossRef
37.
go back to reference Nordin BE, Gallagher JC, Aaron JE, et al. Post-menopausal osteopenia and osteoporosis. Front Horm Res. 1975;3:131–49.PubMedCrossRef Nordin BE, Gallagher JC, Aaron JE, et al. Post-menopausal osteopenia and osteoporosis. Front Horm Res. 1975;3:131–49.PubMedCrossRef
38.
go back to reference Clemens JD, Herrick MV, Singer FR, et al. Evidence that serum NTx (collagen-type I N-telopeptides) can act as an immunochemical marker of bone resorption. Clin Chem. 1997;43(11):2058–63.PubMed Clemens JD, Herrick MV, Singer FR, et al. Evidence that serum NTx (collagen-type I N-telopeptides) can act as an immunochemical marker of bone resorption. Clin Chem. 1997;43(11):2058–63.PubMed
39.
go back to reference Scariano JK, Glew RH, Bou-Serhal CE, et al. Serum levels of cross-linked N-telopeptides and aminoterminal propeptides of type I collagen indicate low bone mineral density in elderly women. Bone. 1998;23(5):471–7.PubMedCrossRef Scariano JK, Glew RH, Bou-Serhal CE, et al. Serum levels of cross-linked N-telopeptides and aminoterminal propeptides of type I collagen indicate low bone mineral density in elderly women. Bone. 1998;23(5):471–7.PubMedCrossRef
Metadata
Title
Markers of Bone Metabolism in Obese Individuals Undergoing Laparoscopic Sleeve Gastrectomy
Authors
Asja E. Schollenberger
Jaana M. Heinze
Tobias Meile
Andreas Peter
Alfred Königsrainer
Stephan C. Bischoff
Publication date
01-08-2015
Publisher
Springer US
Published in
Obesity Surgery / Issue 8/2015
Print ISSN: 0960-8923
Electronic ISSN: 1708-0428
DOI
https://doi.org/10.1007/s11695-014-1509-2

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