Skip to main content
Top
Published in: Obesity Surgery 7/2017

01-07-2017 | Original Contributions

Bariatric Roux-En-Y Gastric Bypass Surgery: Adipocyte Proteins Involved in Increased Bone Remodeling in Humans

Authors: Maria Fernanda G Biagioni, Adriana L Mendes, Célia Regina Nogueira, Celso V Leite, Loraine Gollino, Gláucia MFS Mazeto

Published in: Obesity Surgery | Issue 7/2017

Login to get access

Abstract

Purpose

Bariatric surgery has been associated with bone remodeling changes. The action of adipokines on the expression of receptor activator of nuclear factor kappa β ligand (RANKL) and osteoprotegerin (OPG) and on an increase in sclerostin could be related to these changes.

Materials and Methods

This study aimed to assess the repercussions of weight loss, fat mass (FM), and fat-free mass (FFM) loss and biochemical and hormonal changes on bone remodeling markers after Roux-en-Y gastric bypass (RYGB). Anthropometric data, parathyroid hormone (PTH), bone-specific alkaline phosphatase (BSAP), collagen type 1 C-telopeptide (CTX), 25-hydroxy vitamin D (25-OH-VitD), leptin, adiponectin, RANKL, OPG, and sclerostin of 30 menstruating women were measured preoperatively (Pre), and 3, 12, and 24 months (m) after RYGB.

Results

Leptin (34.4 (14.7; 51.9) vs. 22.5 (1.9; 52.7) ng/mL) and OPG (3.6 (1.1; 11.5) vs. 3.4 (1.5; 6) pmol/L) decreased, and adiponectin (7.4 (1.7; 18.4) vs. 13.8 (3.0; 34.6) μg/mL), CTX (0.2 (0.1; 2.2) vs. 0.6 (0.4; 6.0) ng/mL), RANKL (0.1 (0.0; 0.5) vs. 0.3 (0.0; 2.0) pmol/L), and sclerostin (21.7 (3.2; 75.1) vs. 34.8 (6.4; 80.5) pmol/L) increased after 3 m. BSAP increased after 12 m (10.1 (5.4; 18.9) vs. 13.9 (6.9; 30.2) μg/mL) (p < 0.005). CTX correlated positively with adiponectin at 24 m and inversely with leptin Pre; OPG at 3 m; weight, FM, FFM, and leptin at 24 m. RANKL correlated directly with weight at 3 m. Sclerostin correlated inversely with weight Pre and FM at 3 m. BSAP correlated negatively with 25-OH-VitD at 12 m, and positively with PTH at 24 m.

Conclusions

RYGB induced weight loss, and biochemical, hormonal, and body composition changes are associated with higher bone remodeling.
Literature
2.
go back to reference Mechanick JI, Kushner RF, Sugerman HJ, et al. American Association of Clinical Endocrinologists, the Obesity Society, and American Society for Metabolic & Bariatric Surgery medical guidelines for clinical practice for the perioperative nutritional, metabolic, and nonsurgical support of the bariatric surgery patient. Endocr Pract. 2008;14(Suppl 1):1–83.CrossRefPubMed Mechanick JI, Kushner RF, Sugerman HJ, et al. American Association of Clinical Endocrinologists, the Obesity Society, and American Society for Metabolic & Bariatric Surgery medical guidelines for clinical practice for the perioperative nutritional, metabolic, and nonsurgical support of the bariatric surgery patient. Endocr Pract. 2008;14(Suppl 1):1–83.CrossRefPubMed
3.
go back to reference Ricci C, Gaeta M, Rausa E, et al. Early impact f bariatric surgery on type II diabetes, hipertension, and hyperlipidemia: a systematic review, meta-analysis and meta-regression on 6.587 patients. Obes Surg. 2014;24:522–8.CrossRefPubMed Ricci C, Gaeta M, Rausa E, et al. Early impact f bariatric surgery on type II diabetes, hipertension, and hyperlipidemia: a systematic review, meta-analysis and meta-regression on 6.587 patients. Obes Surg. 2014;24:522–8.CrossRefPubMed
4.
5.
go back to reference Stemmer K, Bielohuby M, Grayson BE, et al. Roux-en-Y gastric bypass surgery but not vertical sleeve gastrectomy decreases bone mass in male rats. Endocrinology. 2013;154:2015–24.CrossRefPubMedPubMedCentral Stemmer K, Bielohuby M, Grayson BE, et al. Roux-en-Y gastric bypass surgery but not vertical sleeve gastrectomy decreases bone mass in male rats. Endocrinology. 2013;154:2015–24.CrossRefPubMedPubMedCentral
6.
go back to reference Stein EM, Silverberg SJ. Bone loss after bariatric surgery: causes. Consequences and Management Lancet Diabetes Endocrinol. 2014;2(2):165–74.CrossRefPubMed Stein EM, Silverberg SJ. Bone loss after bariatric surgery: causes. Consequences and Management Lancet Diabetes Endocrinol. 2014;2(2):165–74.CrossRefPubMed
7.
go back to reference Yu EW, Bouxsein ML, Putman MS, et al. Two-year changes in bone density after Roux-en-Y gastric bypass surgery. J Clin Endocrinol Metab. 2015;100(4):1452–9.CrossRefPubMedPubMedCentral Yu EW, Bouxsein ML, Putman MS, et al. Two-year changes in bone density after Roux-en-Y gastric bypass surgery. J Clin Endocrinol Metab. 2015;100(4):1452–9.CrossRefPubMedPubMedCentral
8.
go back to reference Liu C, Wu D, Zhang J, et al. Changes in bone metabolism in morbidly obese patients after bariatric surgery: a meta-analysis. Obes Surg. 2016;26(1):91–7.CrossRefPubMed Liu C, Wu D, Zhang J, et al. Changes in bone metabolism in morbidly obese patients after bariatric surgery: a meta-analysis. Obes Surg. 2016;26(1):91–7.CrossRefPubMed
10.
go back to reference Karefylakis C, Näslund I, Edholm D, et al. Vitamin D status 10 years after primary gastric bypass: gravely high prevalence of hypovitaminosis D and raised PTH levels. Obes Surg. 2014;24(3):343–8.CrossRefPubMed Karefylakis C, Näslund I, Edholm D, et al. Vitamin D status 10 years after primary gastric bypass: gravely high prevalence of hypovitaminosis D and raised PTH levels. Obes Surg. 2014;24(3):343–8.CrossRefPubMed
11.
go back to reference Hage MP, El-Hajj FG. Bone and mineral metabolism in patients undergoing Roux-en-Y gastric bypass. Osteoporosis Int. 2014;25:423–39.CrossRef Hage MP, El-Hajj FG. Bone and mineral metabolism in patients undergoing Roux-en-Y gastric bypass. Osteoporosis Int. 2014;25:423–39.CrossRef
12.
go back to reference Butte NF, Brandt ML, Wong WW, et al. Energetic adaptations persist after bariatric surgery in severely obese adolescents. Obesity (Silver Spring). 2015;23(3):591–601.CrossRefPubMedCentral Butte NF, Brandt ML, Wong WW, et al. Energetic adaptations persist after bariatric surgery in severely obese adolescents. Obesity (Silver Spring). 2015;23(3):591–601.CrossRefPubMedCentral
13.
go back to reference Luo XH, Guo LJ, Xie H, et al. Adiponectin stimulates RANKL and inhibits OPG expression in human osteoblastos through the MAPK signalling pathway. J Bone Miner Res. 2006;21:1648–56.CrossRefPubMed Luo XH, Guo LJ, Xie H, et al. Adiponectin stimulates RANKL and inhibits OPG expression in human osteoblastos through the MAPK signalling pathway. J Bone Miner Res. 2006;21:1648–56.CrossRefPubMed
14.
go back to reference Nakamichi Y, Udagawa N, Kobayashi Y, et al. Osteoprotegerin reduces the serum level of receptor activator of NF-ΚB ligand derived from osteoblasts. J Immunol. 2007;178:192–200.CrossRefPubMed Nakamichi Y, Udagawa N, Kobayashi Y, et al. Osteoprotegerin reduces the serum level of receptor activator of NF-ΚB ligand derived from osteoblasts. J Immunol. 2007;178:192–200.CrossRefPubMed
15.
go back to reference Elissondo N, Rosso LG, Maidana P, et al. Adiponectina: una adipocitoquina con múltiples funciones protectoras. Acta Bioquím Clín Latinoam. 2008;42(1):17–33. Elissondo N, Rosso LG, Maidana P, et al. Adiponectina: una adipocitoquina con múltiples funciones protectoras. Acta Bioquím Clín Latinoam. 2008;42(1):17–33.
17.
18.
19.
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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
20.
go back to reference Muschitz C, Kocijan R, Marterer C, et al. Sclerostin levels and changes in bone metabolism after bariatric surgery. J Clin Endocrinol Metab. 2015;100(3):891–901.CrossRefPubMed Muschitz C, Kocijan R, Marterer C, et al. Sclerostin levels and changes in bone metabolism after bariatric surgery. J Clin Endocrinol Metab. 2015;100(3):891–901.CrossRefPubMed
21.
go back to reference Wijenayaka AR, Kogawa M, Lim HP, et al. Sclerostin stimulates osteocyte support of osteoclast activity by a RANKL-dependent pathway. PLoS One. 2011;6:e25900.CrossRefPubMedPubMedCentral Wijenayaka AR, Kogawa M, Lim HP, et al. Sclerostin stimulates osteocyte support of osteoclast activity by a RANKL-dependent pathway. PLoS One. 2011;6:e25900.CrossRefPubMedPubMedCentral
22.
go back to reference Atkins GJ, Rowe PS, Lim HP, et al. Sclerostin is a locally acting regulator of late-osteoblast/preosteocyte differentiation and regulates mineralization through a MEPE-ASARM-dependent mechanism. J Bone Miner Res. 2011;26:1425–36.CrossRefPubMedPubMedCentral Atkins GJ, Rowe PS, Lim HP, et al. Sclerostin is a locally acting regulator of late-osteoblast/preosteocyte differentiation and regulates mineralization through a MEPE-ASARM-dependent mechanism. J Bone Miner Res. 2011;26:1425–36.CrossRefPubMedPubMedCentral
23.
24.
go back to reference Lewiecki EM. Sclerostin: a novel target for intervention in the treatment of osteoporosis. Discov Med. 2011;12(65):263–73.PubMed Lewiecki EM. Sclerostin: a novel target for intervention in the treatment of osteoporosis. Discov Med. 2011;12(65):263–73.PubMed
25.
go back to reference Dovjak P, Dorfer S, Föger-Samwald U, et al. Serum levels of sclerostin and dickkopf-1: effects of age, gender and fracture status. Gerontology. 2014;60:493–501.CrossRefPubMed Dovjak P, Dorfer S, Föger-Samwald U, et al. Serum levels of sclerostin and dickkopf-1: effects of age, gender and fracture status. Gerontology. 2014;60:493–501.CrossRefPubMed
26.
go back to reference Eriksen EF. Commentary on sclerostin deficiency is linked to altered bone composition. J Bone Miner Res. 2014;29(10):2141–3.CrossRefPubMed Eriksen EF. Commentary on sclerostin deficiency is linked to altered bone composition. J Bone Miner Res. 2014;29(10):2141–3.CrossRefPubMed
27.
go back to reference Fleischer J, Stein EM, Bessler M, et al. The decline in hip bone density after gastric bypass surgery is associated with extent of weight loss. J Clin Endocrinol Metab. 2008;93(10):3735–40.CrossRefPubMedPubMedCentral Fleischer J, Stein EM, Bessler M, et al. The decline in hip bone density after gastric bypass surgery is associated with extent of weight loss. J Clin Endocrinol Metab. 2008;93(10):3735–40.CrossRefPubMedPubMedCentral
28.
go back to reference Gannagé-Yared MH, Yaghi C, Habre B, et al. Osteoprotegerin in relation to body weight, lipid parameters insulin sensitivity, adipocytokines, and C-reactive protein in obese and non-obese young individuals: results from both cross-sectional and interventional study. Eur J Endocrinol. 2008;158(3):353–9.CrossRefPubMed Gannagé-Yared MH, Yaghi C, Habre B, et al. Osteoprotegerin in relation to body weight, lipid parameters insulin sensitivity, adipocytokines, and C-reactive protein in obese and non-obese young individuals: results from both cross-sectional and interventional study. Eur J Endocrinol. 2008;158(3):353–9.CrossRefPubMed
29.
go back to reference Wroblewski E, Swidnicka-Siergiejko A, Hady HR, et al. Variation in blood levels of hormones in obese patients following weight reduction induced by endoscopic and surgical bariatric therapies. Cytokine. 2016;77:56–62.CrossRefPubMed Wroblewski E, Swidnicka-Siergiejko A, Hady HR, et al. Variation in blood levels of hormones in obese patients following weight reduction induced by endoscopic and surgical bariatric therapies. Cytokine. 2016;77:56–62.CrossRefPubMed
30.
go back to reference Mechanick JI, Youdim A, Jones DB, 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. Endocr Pract. 2013;19(2):337–72.CrossRefPubMedPubMedCentral Mechanick JI, Youdim A, Jones DB, 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. Endocr Pract. 2013;19(2):337–72.CrossRefPubMedPubMedCentral
31.
go back to reference Viégas M, Vasconcelos RS, Neves AP, et al. Bariatric surgery and bone metabolism: a systematic review. Arq Bras Endocrinol Metabol. 2010;54(2):158–63.CrossRefPubMed Viégas M, Vasconcelos RS, Neves AP, et al. Bariatric surgery and bone metabolism: a systematic review. Arq Bras Endocrinol Metabol. 2010;54(2):158–63.CrossRefPubMed
32.
go back to reference Vasconcelos RS, Viégas M, Marques TF, et al. Factors associated with secondary hyperparathyroidism in premenopausal women undergoing Roux-en-Y gastric bypass for the treatment of obesity. Arq Bras Endocrinol Metabol. 2010;54(2):233–8.CrossRefPubMed Vasconcelos RS, Viégas M, Marques TF, et al. Factors associated with secondary hyperparathyroidism in premenopausal women undergoing Roux-en-Y gastric bypass for the treatment of obesity. Arq Bras Endocrinol Metabol. 2010;54(2):233–8.CrossRefPubMed
33.
34.
go back to reference Carrasco F, Basfi-fer K, Rpjas 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;24:877–84.CrossRefPubMed Carrasco F, Basfi-fer K, Rpjas 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;24:877–84.CrossRefPubMed
35.
go back to reference Register TC, Divers J, Bowden DW, et al. Relationships between serum adiponectin and bone density, adiposity and calcified atherosclerotic plaque in the African American-Diabetes Heart Study. J Clin Endocrinol Metab. 2013 May;98(5):1916–22.CrossRefPubMedPubMedCentral Register TC, Divers J, Bowden DW, et al. Relationships between serum adiponectin and bone density, adiposity and calcified atherosclerotic plaque in the African American-Diabetes Heart Study. J Clin Endocrinol Metab. 2013 May;98(5):1916–22.CrossRefPubMedPubMedCentral
36.
go back to reference Balsa JA, Lafuente C, Gómez-Martín JM, et al. The role of serum osteoprotegerin and receptor–activator of nuclear factor-κB ligand in metabolic bone disease of women after obesity surgery. J Bone Miner Metab. 2015;1-7 Balsa JA, Lafuente C, Gómez-Martín JM, et al. The role of serum osteoprotegerin and receptor–activator of nuclear factor-κB ligand in metabolic bone disease of women after obesity surgery. J Bone Miner Metab. 2015;1-7
37.
go back to reference Elias E, Casselbrant A, Werling M, et al. Bone mineral density and expression of vitamin D receptor-dependent calcium uptake mechanisms in the proximal small intestine after bariatric surgery. Br J Surg. 2014;101(12):1566–75. doi:10.1002/bjs.9626.CrossRefPubMed Elias E, Casselbrant A, Werling M, et al. Bone mineral density and expression of vitamin D receptor-dependent calcium uptake mechanisms in the proximal small intestine after bariatric surgery. Br J Surg. 2014;101(12):1566–75. doi:10.​1002/​bjs.​9626.CrossRefPubMed
38.
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. doi:10.1210/jc.2009-0265.CrossRefPubMed 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. doi:10.​1210/​jc.​2009-0265.CrossRefPubMed
39.
go back to reference Biagioni MFG, Mendes AL, Nogueira CR, et al. Weight-reducing gastroplasty with Roux-en-Y gastric bypass: impact on vitamin D status and bone remodeling markers. Metab Syndr Relat Disord. 2014;12(1):11–5.CrossRefPubMed Biagioni MFG, Mendes AL, Nogueira CR, et al. Weight-reducing gastroplasty with Roux-en-Y gastric bypass: impact on vitamin D status and bone remodeling markers. Metab Syndr Relat Disord. 2014;12(1):11–5.CrossRefPubMed
40.
go back to reference Oshima K, Nampei A, Matsuda M, et al. Adiponectin increases bone mass by suppressing osteoclast and activating osteoblast. Biochem Biophys Res Commun. 2005;331(2):520–6.CrossRefPubMed Oshima K, Nampei A, Matsuda M, et al. Adiponectin increases bone mass by suppressing osteoclast and activating osteoblast. Biochem Biophys Res Commun. 2005;331(2):520–6.CrossRefPubMed
41.
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(4):646–51.CrossRefPubMed Lenchik L, Register TC, Hsu FC, et al. Adiponectin as a novel determinant of bone mineral density and visceral fat. Bone. 2003;33(4):646–51.CrossRefPubMed
42.
go back to reference Aguirre L, Napoli N, Waters D, et al. Increasing adiposity is associated with higher adipokine levels and lower bone mineral density in obese older adults. J Clin Endocrinol Metab. 2014;99(9):3290–7.CrossRefPubMedPubMedCentral Aguirre L, Napoli N, Waters D, et al. Increasing adiposity is associated with higher adipokine levels and lower bone mineral density in obese older adults. J Clin Endocrinol Metab. 2014;99(9):3290–7.CrossRefPubMedPubMedCentral
43.
go back to reference Naot D, Cornish J. Cytokines and hormones that contribute to the positive association between fat and bone. Front Endocrinol. 2014;5:70.CrossRef Naot D, Cornish J. Cytokines and hormones that contribute to the positive association between fat and bone. Front Endocrinol. 2014;5:70.CrossRef
44.
go back to reference Carrasco F, Ruz M, Rojas P, 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.CrossRefPubMed Carrasco F, Ruz M, Rojas P, 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.CrossRefPubMed
45.
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;95:159–66.CrossRefPubMed 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;95:159–66.CrossRefPubMed
46.
go back to reference Prado WL, Piano A, Lazaretti-Castro M, et al. Relationship between bone mineral density, leptin and insulin concentration in Brazilian obese adolescents. J Bone Miner Metab. 2009;27:613–9.CrossRefPubMed Prado WL, Piano A, Lazaretti-Castro M, et al. Relationship between bone mineral density, leptin and insulin concentration in Brazilian obese adolescents. J Bone Miner Metab. 2009;27:613–9.CrossRefPubMed
47.
go back to reference Thomas T, Burguera B. Is leptin the link between fat and bone mass? J Bone Miner Res. 2002;17:1563–9.CrossRefPubMed Thomas T, Burguera B. Is leptin the link between fat and bone mass? J Bone Miner Res. 2002;17:1563–9.CrossRefPubMed
48.
go back to reference Walicka M, Czerwińska E, Tałałaj M, et al. Influence of weight reduction on leptin concentration and bone mineral density in patients with morbid obesity before and 6 months after bariatric surgery. Endokrynologia Polska. 2009;60(2):97–102.PubMed Walicka M, Czerwińska E, Tałałaj M, et al. Influence of weight reduction on leptin concentration and bone mineral density in patients with morbid obesity before and 6 months after bariatric surgery. Endokrynologia Polska. 2009;60(2):97–102.PubMed
49.
go back to reference Mohiti-Ardekani J, Soleymani-Salehabadi H, et al. Relationships between serum adipocyte hormones (adiponectin, leptin, resistin), bone mineral density and bone metabolic markers in osteoporosis patients. J Bone Miner Metab. 2014;32(4):400–4.CrossRefPubMed Mohiti-Ardekani J, Soleymani-Salehabadi H, et al. Relationships between serum adipocyte hormones (adiponectin, leptin, resistin), bone mineral density and bone metabolic markers in osteoporosis patients. J Bone Miner Metab. 2014;32(4):400–4.CrossRefPubMed
51.
go back to reference Zhang R, Oyajobi BO, Harris SE, et al. Wnt/β-catenin signaling activates bone morphogenetic protein 2 expression in osteoblasts. Bone. 2013;52(1):145–56.CrossRefPubMed Zhang R, Oyajobi BO, Harris SE, et al. Wnt/β-catenin signaling activates bone morphogenetic protein 2 expression in osteoblasts. Bone. 2013;52(1):145–56.CrossRefPubMed
52.
go back to reference Yamauchi T, Kamon J, Waki H, et al. The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat Med. 2001;7:941–6.CrossRefPubMed Yamauchi T, Kamon J, Waki H, et al. The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat Med. 2001;7:941–6.CrossRefPubMed
53.
go back to reference Wang Y, Lam KS, Xu JY, et al. Adiponectin inhibits cell proliferation by interacting with several growth factors in an oligomerization-dependent manner. J Biol Chem. 2005;280:18341–7.CrossRefPubMed Wang Y, Lam KS, Xu JY, et al. Adiponectin inhibits cell proliferation by interacting with several growth factors in an oligomerization-dependent manner. J Biol Chem. 2005;280:18341–7.CrossRefPubMed
54.
go back to reference Schoenau E. Bone mass increase in puberty: what makes it happen? Horm Res Paediatr. 2006;65(2):2–10.CrossRef Schoenau E. Bone mass increase in puberty: what makes it happen? Horm Res Paediatr. 2006;65(2):2–10.CrossRef
55.
56.
go back to reference Van Bezooijen RL, Svensson JP, Eefting D, et al. Wnt but not BMP signaling is involved in the inhibitory action of sclerostin on BMP-stimulated bone formation. J Bone Miner Res. 2007;22(1):19–28.CrossRefPubMed Van Bezooijen RL, Svensson JP, Eefting D, et al. Wnt but not BMP signaling is involved in the inhibitory action of sclerostin on BMP-stimulated bone formation. J Bone Miner Res. 2007;22(1):19–28.CrossRefPubMed
57.
go back to reference Schwartz AV, Johnson KC, Kahn SE, et al. Effect of 1 year of an intentional weight loss intervention on bone mineral density in type 2 diabetes: results from the look AHEAD randomized trial. J Bone Miner Res. 2012;27(3):619–27.CrossRefPubMedPubMedCentral Schwartz AV, Johnson KC, Kahn SE, et al. Effect of 1 year of an intentional weight loss intervention on bone mineral density in type 2 diabetes: results from the look AHEAD randomized trial. J Bone Miner Res. 2012;27(3):619–27.CrossRefPubMedPubMedCentral
58.
go back to reference Bellido T. Summary—osteocyte control of bone formation via Sost/sclerostin. J Musculoskelet Neuronal Interact. 2006;6(4):360–3. Bellido T. Summary—osteocyte control of bone formation via Sost/sclerostin. J Musculoskelet Neuronal Interact. 2006;6(4):360–3.
59.
go back to reference Granado-Lorencio F, Simal-Antón A, Salazar-Mosteiro J, et al. Time-course changes in bone turnover markers and fat-soluble vitamins after obesity surgery. Obes Surg. 2010;20:1524–9.CrossRefPubMed Granado-Lorencio F, Simal-Antón A, Salazar-Mosteiro J, et al. Time-course changes in bone turnover markers and fat-soluble vitamins after obesity surgery. Obes Surg. 2010;20:1524–9.CrossRefPubMed
60.
go back to reference Villareal RA, Sadler C, Napoli N, et al. Weight loss in obese older adults increases serum sclerostin and impairs hip geometry but both are prevented by exercise training. Bone Miner Res. 2012;27(5):1215–21.CrossRef Villareal RA, Sadler C, Napoli N, et al. Weight loss in obese older adults increases serum sclerostin and impairs hip geometry but both are prevented by exercise training. Bone Miner Res. 2012;27(5):1215–21.CrossRef
61.
go back to reference Muschitz C, Kocijan R, Haschka J, et al. The impact of vitamin D, calcium, protein supplementation, and physical exercise on bone metabolism after bariatric surgery: the BABS study. J Bone Miner Res. 2016;31(3):672–82.CrossRefPubMed Muschitz C, Kocijan R, Haschka J, et al. The impact of vitamin D, calcium, protein supplementation, and physical exercise on bone metabolism after bariatric surgery: the BABS study. J Bone Miner Res. 2016;31(3):672–82.CrossRefPubMed
62.
go back to reference Deitel M, Greenstein R. Editorial: recommendations for reporting weight loss. Obes Surg. 2003;13:159–60.CrossRefPubMed Deitel M, Greenstein R. Editorial: recommendations for reporting weight loss. Obes Surg. 2003;13:159–60.CrossRefPubMed
Metadata
Title
Bariatric Roux-En-Y Gastric Bypass Surgery: Adipocyte Proteins Involved in Increased Bone Remodeling in Humans
Authors
Maria Fernanda G Biagioni
Adriana L Mendes
Célia Regina Nogueira
Celso V Leite
Loraine Gollino
Gláucia MFS Mazeto
Publication date
01-07-2017
Publisher
Springer US
Published in
Obesity Surgery / Issue 7/2017
Print ISSN: 0960-8923
Electronic ISSN: 1708-0428
DOI
https://doi.org/10.1007/s11695-017-2546-4

Other articles of this Issue 7/2017

Obesity Surgery 7/2017 Go to the issue