Effects of endocrine and inflammatory changes on markers of bone turnover following Roux-en-Y gastric bypass surgery
Main Article Content
Abstract
Bariatric surgery is associated with increased bone turnover. The mechanisms involved are unclear but may involve nutrition, mechanical unloading, altered secretion of gastrointestinal and adipose hormones and changes in inflammatory status leading to weight loss induced bone loss. We assessed markers of bone turnover in obese adults (F=19, M=1; BMI 46.5 + 7.9 kg/m2) following Roux-en-Y gastric bypass surgery (RYGB), and investigated their relationship to endocrine and inflammatory markers following this procedure. Bone specific alkaline phospatase (BAP) and N-teleopeptide of type I collagen (NTx) were measured as markers of bone formation and resorption, respectively. Repeated measures analysis of variance (ANOVA) was used to evaluate differences over time. Step-wise multiple regression was used to model the contributions of body weight and composition, endocrine and inflammatory markers to bone metabolism (expressed as BAP/NTX). BAP/ NTx declined significantly (p<0.05) within 1 month after surgery and remained low for 12 months post RYGB. Before surgery, glucose (partial R2 = 0.23, p=0.03) and non-esterified fatty acids (FFA) (partial R2 = 0.12, p=0.09) explained 35% of the variance in BAP/NTX (model R2 = 0.35). Twelve months after RYGB, 48% of variance in BAP/NTx was explained by glucose (partial R2 = 0.21, p=0.04), insulin (partial R2 = 0.17, p=0.05) and C-reactive protein (CRP) (partial R2 = 0.10, p=0.09; model R2 =0.48) Changes in body weight and composition were not significantly related to the BAP/NTX ratio 12 months after surgery. In conclusion, the use of BAP/NTx ratio and stepwise regression models can be used to explore the inter-relationships among bone metabolism, endocrine and inflammatory markers following RYGB weight loss induced bone loss over an extended period of persistent weight loss.
Article Details
How to Cite
ROGERS, Tara S et al.
Effects of endocrine and inflammatory changes on markers of bone turnover following Roux-en-Y gastric bypass surgery.
Medical Research Archives, [S.l.], v. 2, n. 2, sep. 2015.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/329>. Date accessed: 16 apr. 2024.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
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Basu A, Devaraj S, Jialal I. 2006. Dietary factors that promote or retard inflammation. Arterioscler Thromb Vasc Biol; 26:995-1001.
Basu R, Peterson J, Rizza R, Khosla S. 2011. Effects of physiological variations in circulating insulin levels on bone turnover in humans. J Clin Endocrinol Metab; 96(5):1450-1455.
Beckman LM, Beckman TR, Earthman CP. 2010. Changes in gastrointestinal hormones and leptin after Roux-en-Y gastric bypass procedure: a review. J Am Diet Assoc; 110:571-584.
Beckman LM, Beckman TR, Sibley SD, Thomas W, Ikramuddin S, Kellogg TA et al. 2011. Changes in gastrointestinal hormones and leptin after Roux-en-Y gastric bypass surgery. J Parenter Enteral Nutr; 35:169-180.
Biagioni MF, Mendes AL, Nogueira CR, Pavia SA, Leite CU, Mazeto GM. 2014. Weight-reducing gastroplasty with Roux-en-Y gastric bypass: impact on vitamin D status and bone remodeling markers. Metab Syndr Related Disord; 12(1):11-15.
Blum M, Harris SS, Must A, Naumova EN, Phillips SM, Rand WM et al. 2003. Leptin, body composition and bone mineral density in pre-menopausal women. Calcif Tissue Int; 73:27-32.
Bruno C, Fulford AD, Potts JR, McClintock R, Jones R, Cacucci BM et al. 2010. Serum markers of bone turnover are increased at six and eighteen months after Roux-en-Y bariatric surgery: correlation with the reduction in leptin. J Clin Endocrinol Metab; 95:159-166.
Brzozowska MM, Sainsbury A, Eisman JA, Baldock PA, Center JR. 2013. Bariatric surgery, bone loss, obesity and possible mechanisms. Obes Rev; 14:52-67.
Campos GM, Rabl C, Peeva S, Ciovica R, Rao M, Schwarz JM et al. 2010. 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 loss. J Gastrointest Surg; 14(1):15-23.
Carrasco F, Ruz M, Rojas P, Csendes A, Rebolledo A, Codeceo J et al. 2009. Changes in bone mineral density, body composition and adiponectin levels in morbidly obese patients after bariatric surgery. Obes Surg; 19:41-46.
Casagrande DS, Repetto G, Mottin CC, Shah J, Pietrobon R, Worni M, Schaan BD. 2012. Changes in bone mineral density in women following one-year gastric bypass surgery. Obes Surg; 22:1287-1292.
Coates PS, Fernstrom JD, Fernstrom MH, Schauer PR, Greenspan SL. 2004. Gastric bypass surgery for morbid obesity leads to an increase in bone turnover and a decrease in bone mass. J Clin Endocrinol Metab; 89:1061-1065.
Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, Nyce MR, Ohannesian JP, Marco CC, McKee LJ, Bauer TL, Caro JF. 1996. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med.; 334:292–295.
Cornish J, Callon KE, Bara U, Lin C, Naot D, Hill BL et al. 2002. Leptin directly regulates bone cell function in vitro and reduces bone fragility in vivo. J Endocrinol; 175:405-415.
Cornish J, Costa JL and Naot D. The bone-fat mass relationship: laboratory studies. IBMS BoneKEy 2009; 6(9):311-322.
Dirksen C, Jorgensen NB, Bojesen-Moller KN, Jacobsen SH, Hansen DL, Worm D et al. 2012. Mechanisms of improved glycemic control under Roux-en-Y gastric bypass. Diabetologia; 55:1890-1901.
Ducy P, Amling M, Takeda S, Priemel M, Schilling AF, Beil FT et al. 2000. Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell; 100:197-207.
El-Kadre LJ, Rocha PR, de Almeida Tinoco AC, Tinoco RC. 2004. Calcium metabolism in pre- and post-menopausal morbidly obese women at baseline and after laproscopic Roux-en-Y gastric bypass. Obes Surg; 14(8):1062-1066.
Folli F, Sabowitz BN, Schwesinger W, Fanti P, Guardado-Mendoza R, Muscogiuri G. 2012. Bariatric surgery and bone disease: from clinical perspective to molecular insights. Int J Obes; 36:1373-1379.
Frederich RC, Hamann A, Anderson S, Lollmann B, Lowell BB, Flier JS. 1995. Leptin levels reflect body lipid content in mice: evidence for diet-induced resistance to leptin action. Nat Med.; 1:1311–1314.
Fulzele K and Clemens TL. 2012. Novel functions for insulin in bone. Bone; 50:452-456.
Gómez JM, Vilarrasa N, Masdevall C, Pujol J, Solano E, Soler J et al. 2009. Regulation of bone mineral density in morbidly obese women: a cross-sectional study in two cohorts before and after bypass surgery. Obes Surg; 19:345-350.
Gómez-Ambrosi J, Rodriguez A, Catalán V, Frühbeck G. 2008. The bone-adipose axis in obesity and weight loss. Obes Surg; 18:1134-1143.
Granado-Lorencio F, Simal-Antón A, Salazar-Mosteiro J, Herrero-Barbudo C, Donoso-Navarro E, Blanco-Navarro I et al. 2010. Time-course changes in bone turnover markers and fat soluble vitamins after obesity surgery. Obes Surg; 20:1524-1529.
Grethen E, Hill KM, Jones R, Cacucci BM, Gupta CE, Acton A et al. 2012. Serum leptin, parathyroid hormone, 1,25 Dihydroxyvitamin D, fibroblast growth factor 23, bone alkaline phosphatase and sclerostin relationships in obesity. J Clin Endocrinol Metab; 97:1655-1662.
Hage MP and Fuleihan GE. 2014. Bone and mineral metabolism in patients undergoing Roux-en-Y gastric bypass. Osteoporos Int; 25:423-439.
Havel PJ. 2004. Update on adipocyte hormones: regulation of energy balance and carbohydrate/lipid metabolism. Diabetes;53 (Supp 1):S143-S151.
Holdstock C, Engström BE, Öhrvall M, Lind L, Sundbom M, Karlsson FA. 2003. Ghrelin and adipose tissue regulatory peptides: effect of gastric bypass surgery in obese humans. J Clin Endocrinol Metab; 88:3177-3183.
Jürimäe J, Kums T, Jürimäe T. 2009. Adipocytokine and ghrelin levels in relation to bone mineral density in physically active older women: longitudinal associations. Eur J Endocrinol; 160:381-385.
Karsenty G and Ferron M. The contribution of bone to whole-organism physiology. 2012. Nature; 481:314-320.
Koroglu BK, Kiris F, Ersoy IH, Sutcu R, Yildiz M, Aksu O et al. 2011. Relationship of leptin, adiponectin and insulin resistance to bone mineral density in type 2 diabetic post-menopausal women. Pol J Endocrinol; 62(5):429-435.
Lancha A, Moncada R, Valentí V, Rodríguez A, Catalán V, Becerril S et al. 2014. Comparative effects of gastric bypass and sleeve gastrectomy on plasma osteopontin concentrations in humans. Surg Endosc 28:2412-2420.
Lee Y, Kim M, Choi K, Kim J, Bae W, Kim S et al. 2011. Relationship between inflammation biomarkers, antioxidant vitamins, and bone mineral density in patients with metabolic syndrome. Nutr Res Pract; 5(2):150-156.
Mahdy T, Atia S, Farid M, Adulatif A. 2008. Effect of Roux-en-Y gastric bypass on bone metabolism in patients with morbid obesity: Mansoura experiences. Obes Surg; 18:1526-1531.
McCormick RK. 2007. Osteoporosis: integrating biomarkers and other diagnostic correlates into the management of bone fragility. Altern Med Rev; 12(2):113-145.
Mechanick JI, Youdim A, Jones DB, Garvey WT, Hurley DL, McMahon MM et al. 2013. Clinical practice guidelines for the perioperative nutritional, metabolic, and nonsurgical support of the bariatric surgery patient- 2013 update: cosponsored by the American Association of Clinical Endocrinologists, the Obesity Society, and the American Society for Metabolic and Bariatric Surgery. Obesity; 21:S1-S27.
Nakamura KM, Haglind EGC, Clowes JA, Achenbach SJ, Atkinson EJ, Melton III LJ, Kennel KA. 2014. Fracture risk following bariatric surgery: a population-based study. Osteoporos Int; 25:151-158.
Raffaelli M, Guidone C. Callari C, Iaconelli A, Bellatone R, Mingrone G. 2014. Effect of gastric bypass versus diet on cardiovascular risk factors. Ann Surg; 259:694-699.
Reid IR. 2010. Fat and bone. Arch Biochem Biophys; 503:20-27.
Riedl M, Vila G, Maier C, Handisurya A, Shakeri-Manesch S, Prager G et al. 20008. Plasma osteopontin increases after bariatric surgery and correlates with markers of bone turnover but not insulin resistance. J Clin Endocrinol Metab; 93:2307-2312.
Schaller G, Aso Y, Schernthaner GH, Kopp HP, Inukai T, Kriwanek S et al. 2009. Increase of osteopontin plasma concentrations after bariatric surgery independent from inflammation and insulin resistance. Obes Surg; 19:351-356.
Schweitzer DH. 2007. Mineral metabolism and bone disease after bariatric surgery and ways to optimize bone health. Obes Surg; 17:1510-1516.
Scibora LM, Ikramuddin S, Buchwald H, Petit MA. 2012. Examining the link between bariatric surgery, bone loss, and osteoporosis: a review of bone density studies. Obes Surg; 22:654-667.
Sinha N, Shieh A, Stein EM, Strain G, Schulman A, Pomp A et al. 2011. Increased PTH and 1,25(OH)(2)D levels associated with increased markers of bone turnover following bariatric surgery. Obesity (Silver Spring); 19(12):2388-2393.
Stein EM, Carrelli A, Young P, Bucovsky M, Zhang C, Schrope B et al. 2013. Bariatric surgery results in cortical bone loss. J Clin Endocrionl Metab; 98:541-549.
Stein EM and Silverberg SJ. 2014. Bone loss after bariatric surgery: causes, consequences, and management. Lancet Diabetes Endocrionol; 2:165-174.
Swarbrick MM, Austrheim-Smith IT, Stanhope KL, Van Loan MD, Ali MR, Wolf BM et al. 2006. Circulating concentrations of high-molecular-weight adiponectin are increased following Roux-en-Y gastric bypass surgery. Diabetologia; 49:2552-2558.
Swarbrick MM, Stanhope KL, Austrheim-Smith IT, Van Loan MD, Ali MR, Wolfe BM, et al. 2008. Longitudinal changes in pancreatic and adipocyte hormones following Roux-en-Y gastric bypass surgery. Diabetologia;51:1901-1911.
Thomsen SB, Rathcke CN, Jorgensen NB, Madsbad S, Vestergaard H. Effects of Roux-en-Y gastric bypass on fasting and post-prandial levels of the inflammatory markers YKL-40 and MCP-1 in patients with type 2 diabetes and glucose tolerant subjects. J Obes 2013; Article ID 361781, 10 pages.
Turner RT, Kalra SP, Wong CP, Philbrick KA, Lindenmaier LB, Boghossian S et al. Peripheral leptin regulates bone formation. J Bone Miner Res 2013; 28(1):22-34.
Valderas JP, Padilla O, Solari S, Escalona M, González G. Feeding and bone turnover in gastric bypass. J Clin Endocrinol Metab 2014; 99:491-497.
Viégas M, Simoes de Vasconcelos R, Neves AP, Diniz ET, Bandeira F. Bariatric surgery and bone metabolism: a systematic review. Arq Bras Endocrinol Metab 2010; 54(2):158-163.
Vilarrasa N, San José P, Garcia I, Gómez-Vaquero C, Miras PM, Ruiz de Gordejuela AG et al. Evaluation of bone mineral density loss in morbidly obese women after gastric bypass: three year follow up. Obes Surg 2011; 21:465-472.
Williams SE. Metabolic bone disease in the bariatric surgery patient. J Obes 2011. Article ID 634614, 9 pages.
Yamauchi M, Sugimoto T, Yamaguchi T, Nakaoka D, Kanzawa M, Yano S et al. Plasma leptin concentrations are associated with bone mineral density and the presence of vertebral fractures in postmenopausal women. Clin Endocrinol 2001; 55:341-347.
Yu EW. Bone metabolism after bariatric surgery. J Bone Miner Res 2014; 29(7):1507-1518.
Basu A, Devaraj S, Jialal I. 2006. Dietary factors that promote or retard inflammation. Arterioscler Thromb Vasc Biol; 26:995-1001.
Basu R, Peterson J, Rizza R, Khosla S. 2011. Effects of physiological variations in circulating insulin levels on bone turnover in humans. J Clin Endocrinol Metab; 96(5):1450-1455.
Beckman LM, Beckman TR, Earthman CP. 2010. Changes in gastrointestinal hormones and leptin after Roux-en-Y gastric bypass procedure: a review. J Am Diet Assoc; 110:571-584.
Beckman LM, Beckman TR, Sibley SD, Thomas W, Ikramuddin S, Kellogg TA et al. 2011. Changes in gastrointestinal hormones and leptin after Roux-en-Y gastric bypass surgery. J Parenter Enteral Nutr; 35:169-180.
Biagioni MF, Mendes AL, Nogueira CR, Pavia SA, Leite CU, Mazeto GM. 2014. Weight-reducing gastroplasty with Roux-en-Y gastric bypass: impact on vitamin D status and bone remodeling markers. Metab Syndr Related Disord; 12(1):11-15.
Blum M, Harris SS, Must A, Naumova EN, Phillips SM, Rand WM et al. 2003. Leptin, body composition and bone mineral density in pre-menopausal women. Calcif Tissue Int; 73:27-32.
Bruno C, Fulford AD, Potts JR, McClintock R, Jones R, Cacucci BM et al. 2010. Serum markers of bone turnover are increased at six and eighteen months after Roux-en-Y bariatric surgery: correlation with the reduction in leptin. J Clin Endocrinol Metab; 95:159-166.
Brzozowska MM, Sainsbury A, Eisman JA, Baldock PA, Center JR. 2013. Bariatric surgery, bone loss, obesity and possible mechanisms. Obes Rev; 14:52-67.
Campos GM, Rabl C, Peeva S, Ciovica R, Rao M, Schwarz JM et al. 2010. 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 loss. J Gastrointest Surg; 14(1):15-23.
Carrasco F, Ruz M, Rojas P, Csendes A, Rebolledo A, Codeceo J et al. 2009. Changes in bone mineral density, body composition and adiponectin levels in morbidly obese patients after bariatric surgery. Obes Surg; 19:41-46.
Casagrande DS, Repetto G, Mottin CC, Shah J, Pietrobon R, Worni M, Schaan BD. 2012. Changes in bone mineral density in women following one-year gastric bypass surgery. Obes Surg; 22:1287-1292.
Coates PS, Fernstrom JD, Fernstrom MH, Schauer PR, Greenspan SL. 2004. Gastric bypass surgery for morbid obesity leads to an increase in bone turnover and a decrease in bone mass. J Clin Endocrinol Metab; 89:1061-1065.
Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, Nyce MR, Ohannesian JP, Marco CC, McKee LJ, Bauer TL, Caro JF. 1996. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med.; 334:292–295.
Cornish J, Callon KE, Bara U, Lin C, Naot D, Hill BL et al. 2002. Leptin directly regulates bone cell function in vitro and reduces bone fragility in vivo. J Endocrinol; 175:405-415.
Cornish J, Costa JL and Naot D. The bone-fat mass relationship: laboratory studies. IBMS BoneKEy 2009; 6(9):311-322.
Dirksen C, Jorgensen NB, Bojesen-Moller KN, Jacobsen SH, Hansen DL, Worm D et al. 2012. Mechanisms of improved glycemic control under Roux-en-Y gastric bypass. Diabetologia; 55:1890-1901.
Ducy P, Amling M, Takeda S, Priemel M, Schilling AF, Beil FT et al. 2000. Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell; 100:197-207.
El-Kadre LJ, Rocha PR, de Almeida Tinoco AC, Tinoco RC. 2004. Calcium metabolism in pre- and post-menopausal morbidly obese women at baseline and after laproscopic Roux-en-Y gastric bypass. Obes Surg; 14(8):1062-1066.
Folli F, Sabowitz BN, Schwesinger W, Fanti P, Guardado-Mendoza R, Muscogiuri G. 2012. Bariatric surgery and bone disease: from clinical perspective to molecular insights. Int J Obes; 36:1373-1379.
Frederich RC, Hamann A, Anderson S, Lollmann B, Lowell BB, Flier JS. 1995. Leptin levels reflect body lipid content in mice: evidence for diet-induced resistance to leptin action. Nat Med.; 1:1311–1314.
Fulzele K and Clemens TL. 2012. Novel functions for insulin in bone. Bone; 50:452-456.
Gómez JM, Vilarrasa N, Masdevall C, Pujol J, Solano E, Soler J et al. 2009. Regulation of bone mineral density in morbidly obese women: a cross-sectional study in two cohorts before and after bypass surgery. Obes Surg; 19:345-350.
Gómez-Ambrosi J, Rodriguez A, Catalán V, Frühbeck G. 2008. The bone-adipose axis in obesity and weight loss. Obes Surg; 18:1134-1143.
Granado-Lorencio F, Simal-Antón A, Salazar-Mosteiro J, Herrero-Barbudo C, Donoso-Navarro E, Blanco-Navarro I et al. 2010. Time-course changes in bone turnover markers and fat soluble vitamins after obesity surgery. Obes Surg; 20:1524-1529.
Grethen E, Hill KM, Jones R, Cacucci BM, Gupta CE, Acton A et al. 2012. Serum leptin, parathyroid hormone, 1,25 Dihydroxyvitamin D, fibroblast growth factor 23, bone alkaline phosphatase and sclerostin relationships in obesity. J Clin Endocrinol Metab; 97:1655-1662.
Hage MP and Fuleihan GE. 2014. Bone and mineral metabolism in patients undergoing Roux-en-Y gastric bypass. Osteoporos Int; 25:423-439.
Havel PJ. 2004. Update on adipocyte hormones: regulation of energy balance and carbohydrate/lipid metabolism. Diabetes;53 (Supp 1):S143-S151.
Holdstock C, Engström BE, Öhrvall M, Lind L, Sundbom M, Karlsson FA. 2003. Ghrelin and adipose tissue regulatory peptides: effect of gastric bypass surgery in obese humans. J Clin Endocrinol Metab; 88:3177-3183.
Jürimäe J, Kums T, Jürimäe T. 2009. Adipocytokine and ghrelin levels in relation to bone mineral density in physically active older women: longitudinal associations. Eur J Endocrinol; 160:381-385.
Karsenty G and Ferron M. The contribution of bone to whole-organism physiology. 2012. Nature; 481:314-320.
Koroglu BK, Kiris F, Ersoy IH, Sutcu R, Yildiz M, Aksu O et al. 2011. Relationship of leptin, adiponectin and insulin resistance to bone mineral density in type 2 diabetic post-menopausal women. Pol J Endocrinol; 62(5):429-435.
Lancha A, Moncada R, Valentí V, Rodríguez A, Catalán V, Becerril S et al. 2014. Comparative effects of gastric bypass and sleeve gastrectomy on plasma osteopontin concentrations in humans. Surg Endosc 28:2412-2420.
Lee Y, Kim M, Choi K, Kim J, Bae W, Kim S et al. 2011. Relationship between inflammation biomarkers, antioxidant vitamins, and bone mineral density in patients with metabolic syndrome. Nutr Res Pract; 5(2):150-156.
Mahdy T, Atia S, Farid M, Adulatif A. 2008. Effect of Roux-en-Y gastric bypass on bone metabolism in patients with morbid obesity: Mansoura experiences. Obes Surg; 18:1526-1531.
McCormick RK. 2007. Osteoporosis: integrating biomarkers and other diagnostic correlates into the management of bone fragility. Altern Med Rev; 12(2):113-145.
Mechanick JI, Youdim A, Jones DB, Garvey WT, Hurley DL, McMahon MM et al. 2013. Clinical practice guidelines for the perioperative nutritional, metabolic, and nonsurgical support of the bariatric surgery patient- 2013 update: cosponsored by the American Association of Clinical Endocrinologists, the Obesity Society, and the American Society for Metabolic and Bariatric Surgery. Obesity; 21:S1-S27.
Nakamura KM, Haglind EGC, Clowes JA, Achenbach SJ, Atkinson EJ, Melton III LJ, Kennel KA. 2014. Fracture risk following bariatric surgery: a population-based study. Osteoporos Int; 25:151-158.
Raffaelli M, Guidone C. Callari C, Iaconelli A, Bellatone R, Mingrone G. 2014. Effect of gastric bypass versus diet on cardiovascular risk factors. Ann Surg; 259:694-699.
Reid IR. 2010. Fat and bone. Arch Biochem Biophys; 503:20-27.
Riedl M, Vila G, Maier C, Handisurya A, Shakeri-Manesch S, Prager G et al. 20008. Plasma osteopontin increases after bariatric surgery and correlates with markers of bone turnover but not insulin resistance. J Clin Endocrinol Metab; 93:2307-2312.
Schaller G, Aso Y, Schernthaner GH, Kopp HP, Inukai T, Kriwanek S et al. 2009. Increase of osteopontin plasma concentrations after bariatric surgery independent from inflammation and insulin resistance. Obes Surg; 19:351-356.
Schweitzer DH. 2007. Mineral metabolism and bone disease after bariatric surgery and ways to optimize bone health. Obes Surg; 17:1510-1516.
Scibora LM, Ikramuddin S, Buchwald H, Petit MA. 2012. Examining the link between bariatric surgery, bone loss, and osteoporosis: a review of bone density studies. Obes Surg; 22:654-667.
Sinha N, Shieh A, Stein EM, Strain G, Schulman A, Pomp A et al. 2011. Increased PTH and 1,25(OH)(2)D levels associated with increased markers of bone turnover following bariatric surgery. Obesity (Silver Spring); 19(12):2388-2393.
Stein EM, Carrelli A, Young P, Bucovsky M, Zhang C, Schrope B et al. 2013. Bariatric surgery results in cortical bone loss. J Clin Endocrionl Metab; 98:541-549.
Stein EM and Silverberg SJ. 2014. Bone loss after bariatric surgery: causes, consequences, and management. Lancet Diabetes Endocrionol; 2:165-174.
Swarbrick MM, Austrheim-Smith IT, Stanhope KL, Van Loan MD, Ali MR, Wolf BM et al. 2006. Circulating concentrations of high-molecular-weight adiponectin are increased following Roux-en-Y gastric bypass surgery. Diabetologia; 49:2552-2558.
Swarbrick MM, Stanhope KL, Austrheim-Smith IT, Van Loan MD, Ali MR, Wolfe BM, et al. 2008. Longitudinal changes in pancreatic and adipocyte hormones following Roux-en-Y gastric bypass surgery. Diabetologia;51:1901-1911.
Thomsen SB, Rathcke CN, Jorgensen NB, Madsbad S, Vestergaard H. Effects of Roux-en-Y gastric bypass on fasting and post-prandial levels of the inflammatory markers YKL-40 and MCP-1 in patients with type 2 diabetes and glucose tolerant subjects. J Obes 2013; Article ID 361781, 10 pages.
Turner RT, Kalra SP, Wong CP, Philbrick KA, Lindenmaier LB, Boghossian S et al. Peripheral leptin regulates bone formation. J Bone Miner Res 2013; 28(1):22-34.
Valderas JP, Padilla O, Solari S, Escalona M, González G. Feeding and bone turnover in gastric bypass. J Clin Endocrinol Metab 2014; 99:491-497.
Viégas M, Simoes de Vasconcelos R, Neves AP, Diniz ET, Bandeira F. Bariatric surgery and bone metabolism: a systematic review. Arq Bras Endocrinol Metab 2010; 54(2):158-163.
Vilarrasa N, San José P, Garcia I, Gómez-Vaquero C, Miras PM, Ruiz de Gordejuela AG et al. Evaluation of bone mineral density loss in morbidly obese women after gastric bypass: three year follow up. Obes Surg 2011; 21:465-472.
Williams SE. Metabolic bone disease in the bariatric surgery patient. J Obes 2011. Article ID 634614, 9 pages.
Yamauchi M, Sugimoto T, Yamaguchi T, Nakaoka D, Kanzawa M, Yano S et al. Plasma leptin concentrations are associated with bone mineral density and the presence of vertebral fractures in postmenopausal women. Clin Endocrinol 2001; 55:341-347.
Yu EW. Bone metabolism after bariatric surgery. J Bone Miner Res 2014; 29(7):1507-1518.