Abstract
Objectives
Little is known about the long-term skeletal impact of bariatric procedures, particularly the increasingly commonly performed gastric sleeve surgery (GS). We examined bone density (BMD) change following three types of bariatric surgery Roux-en-Y gastric bypass (RYGB), GS and laparoscopic adjustable gastric banding (LAGB), compared with diet, over 36 months.
Methods
Non-randomized, prospective study of participants with severe obesity (n = 52), undergoing weight-loss interventions: RYGB (n = 7), GS (n = 21), LAGB (n = 11) and diet (n = 13). Measurements of calciotropic indices, gut hormones (fasting and post prandial) peptide YY (PYY), glucagon-like peptide 1 (GLP1) and adiponectin together with dual-X-ray absorptiometry and quantitative computed tomography scans were performed thorough the study.
Results
All groups lost weight during the first 12 months. Despite weight stability from 12 to 36 months and supplementation of calcium and vitamin D, there was progressive bone loss at the total hip (TH) over 36 months in RYGB −14% (95% CI: −12, −17) and GS −9% (95% CI: −7, −10). In RYGB forearm BMD also declined over 36 months −9% (95% CI: −6, −12) and LS BMD declined over the first 12 months −7% (95% CI: −3, −12). RYGB and GS groups experienced significantly greater bone loss until 36 months than LAGB and diet groups, which experienced no significant BMD loss. These bone losses remained significant after adjustment for weight loss and age. RYGB and GS procedures resulted in elevated postprandial PYY, adiponectin and bone turnover markers up to 36 months without such changes among LAGB and diet participants.
Conclusions
RYGB and GS but not LAGB resulted in ongoing TH bone loss for three postoperative years. For RYGB, bone loss was also observed at LS and non-weight-bearing forearms. These BMD changes were independent of weight and age differences. We, therefore, recommend close monitoring of bone health following RYGB and GS surgeries.
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References
Arterburn DE, Olsen MK, Smith VA, Livingston EH, Van Scoyoc L, Yancy WS Jr., et al. Association between bariatric surgery and long-term survival. JAMA. 2015;313:62–70.
Sjostrom L, Peltonen M, Jacobson P, Sjostrom CD, Karason K, Wedel H, et al. Bariatric surgery and long-term cardiovascular events. JAMA. 2012;307:56–65.
Angrisani L, Santonicola A, Iovino P, Vitiello A, Zundel N, Buchwald H, et al. Bariatric surgery and endoluminal procedures: IFSO Worldwide Survey 2014. Obes Surg. 2017;27:2279–89.
Maciejewski ML, Arterburn DE, Van Scoyoc L, Smith VA, Yancy WS Jr., Weidenbacher HJ, et al. Bariatric surgery and long-term durability of weight loss. JAMA Surg. 2016;151:1046–55.
Nogues X, Goday A, Pena MJ, Benaiges D, de Ramon M, Crous X, et al. Bone mass loss after sleeve gastrectomy: a prospective comparative study with gastric bypass. Cir Espan. 2010;88:103–9.
Pluskiewicz W, Buzga M, Holeczy P, Bortlik L, Smajstrla V, Adamczyk P. Bone mineral changes in spine and proximal femur in individual obese women after laparoscopic sleeve gastrectomy: a short-term study. Obes Surg. 2012;22:1068–76.
Giusti V, Gasteyger C, Suter M, Heraief E, Gaillard RC, Burckhardt P. Gastric banding induces negative bone remodelling in the absence of secondary hyperparathyroidism: potential role of serum C telopeptides for follow-up. Int J Obesity. 2005;29:1429–35.
Pugnale N, Giusti V, Suter M, Zysset E, Heraief E, Gaillard RC, et al. Bone metabolism and risk of secondary hyperparathyroidism 12 months after gastric banding in obese pre-menopausal women. Int J Obesity. 2003;27:110–6.
Fleischer J, Stein EM, Bessler M, Della Badia M, Restuccia N, Olivero-Rivera L, et al. The decline in hip bone density after gastric bypass surgery is associated with extent of weight loss. JCEM. 2008;93:3735–40.
Muschitz C, Kocijan R, Marterer C, Nia AR, Muschitz GK, Resch H, et al. Sclerostin levels and changes in bone metabolism after bariatric surgery. JCEM. 2015;100:891–901.
Yu EW, Bouxsein ML, Putman MS, Monis EL, Roy AE, Pratt JS, et al. Two-year changes in bone density after Roux-en-Y gastric bypass surgery. JCEM. 2015;100:1452–9.
Lindeman KG, Greenblatt LB, Rourke C, Bouxsein ML, Finkelstein JS, Yu EW. Longitudinal 5-year evaluation of bone density and microarchitecture after Roux-en-Y gastric bypass surgery. JCEM. 2018;103:4104–12.
Raoof M, Naslund I, Rask E, Szabo E. Effect of gastric bypass on bone mineral density, parathyroid hormone and vitamin D: 5 years follow-up. Obes Surg. 2016;26:1141–5.
Hsin MC, Huang CK, Tai CM, Yeh LR, Kuo HC, Garg A. A case-matched study of the differences in bone mineral density 1 year after 3 different bariatric procedures. Surg Obes Relat Dis. 2015;11:181–5.
Maghrabi AH, Wolski K, Abood B, Licata A, Pothier C, Bhatt DL, et al. Two-year outcomes on bone density and fracture incidence in patients with T2DM randomized to bariatric surgery versus intensive medical therapy. Obesity. 2015;23:2344–8.
Frederiksen KD, Hanson S, Hansen S, Brixen K, Gram J, Jorgensen NR, et al. Bone structural changes and estimated strength after gastric bypass surgery evaluated by HR-pQCT. Calcif Tissue Int. 2016;98:253–62.
Carrasco F, Ruz M, Rojas P, Csendes A, Rebolledo A, Codoceo J, et al. Changes in bone mineral density, body composition and adiponectin levels in morbidly obese patients after bariatric surgery. Obes Surg. 2009;19:41–6.
Vilarrasa N, Gomez JM, Elio I, Gomez-Vaquero C, Masdevall C, Pujol J, et al. Evaluation of bone disease in morbidly obese women after gastric bypass and risk factors implicated in bone loss. Obes Surg. 2009;19:860–6.
Stein EM, Carrelli A, Young P, Bucovsky M, Zhang C, Schrope B, et al. Bariatric surgery results in cortical bone loss. JCEM. 2013;98:541–9.
Blom-Hogestol IK, Mala T, Kristinsson JA, Brunborg C, Gulseth HL, Eriksen EF. Changes in bone quality after Roux-en-Y gastric bypass: a prospective cohort study in subjects with and without type 2 diabetes. Bone. 2020;130:115069.
Vilarrasa N, San Jose P, Garcia I, Gomez-Vaquero C, Miras PM, de Gordejuela AG, et al. Evaluation of bone mineral density loss in morbidly obese women after gastric bypass: 3-year follow-up. Obes Surg. 2011;21:465–72.
Cadart O, Degrandi O, Barnetche T, Mehsen-Cetre N, Monsaingeon-Henry M, Pupier E. et al. Long-term effects of Roux-en-Y gastric bypass and sleeve gastrectomy on bone mineral density: a 4-year longitudinal study. Obes Surg. 2020;30:3317–25.
Luhrs AR, Davalos G, Lerebours R, Yoo J, Park C, Tabone L, et al. Determining changes in bone metabolism after bariatric surgery in postmenopausal women. Surg Endosc. 2020;34:1754–60.
Bredella MA, Greenblatt LB, Eajazi A, Torriani M, Yu EW. Effects of Roux-en-Y gastric bypass and sleeve gastrectomy on bone mineral density and marrow adipose tissue. Bone. 2017;95:85–90.
Muschitz C, Kocijan R, Haschka J, Zendeli A, Pirker T, Geiger C, et al. The impact of vitamin D, calcium, protein supplementation, and physical exercise on bone metabolism after bariatric. Surgery: The BABS Study. JBMR. 2016;31:672–82.
Brzozowska MM, Sainsbury A, Eisman JA, Baldock PA, Center JR. Bariatric surgery, bone loss, obesity and possible mechanisms. Obes Rev. 2013;14:52–67.
Batterham RL, Bloom SR. The gut hormone peptide YY regulates appetite. Ann Ny Acad Sci. 2003;994:162–8.
Rigamonti AE, Agosti F, Compri E, Giunta M, Marazzi N, Muller EE, et al. Anorexigenic postprandial responses of PYY and GLP1 to slow ice cream consumption: preservation in obese adolescents, but not in obese adults. Eur J Endocrinol. 2013;168:429–36.
Bruno C, Fulford AD, Potts JR, McClintock R, Jones R, Cacucci BM, 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. JCEM. 2010;95:159–66.
Crawford MR, Pham N, Khan L, Bena JF, Schauer PR, Kashyap SR. Increased bone turnover in type 2 diabetes patients randomized to bariatric surgery versus medical therapy at 5 years. Endocr Pract. 2018;24:256–64.
Beamish AJ, Gronowitz E, Olbers T, Flodmark CE, Marcus C, Dahlgren J. Body composition and bone health in adolescents after Roux-en-Y gastric bypass for severe obesity. Pediatr Obes. 2017;12:239–46.
Schauer PR, Bhatt DL, Kirwan JP, Wolski K, Aminian A, Brethauer SA, et al. Bariatric surgery versus intensive medical therapy for diabetes - 5-year outcomes. NEJM. 2017;376:641–51.
Parrott J, Frank L, Rabena R, Craggs-Dino L, Isom KA, Greiman L. American society for metabolic and bariatric surgery integrated health nutritional guidelines for the surgical weight loss patient 2016 update: micronutrients. Surg Obes Relat Dis. 2017;13:727–41.
Shanbhogue VV, Stoving RK, Frederiksen KH, Hanson S, Brixen K, Gram J, et al. Bone structural changes after gastric bypass surgery evaluated by HR-pQCT: a two-year longitudinal study. Eur J Endocrinol. 2017;176:685–93.
Rousseau C, Jean S, Gamache P, Lebel S, Mac-Way F, Biertho L, et al. Change in fracture risk and fracture pattern after bariatric surgery: nested case-control study. BMJ. 2016;354:i3794.
Lu CW, Chang YK, Chang HH, Kuo CS, Huang CT, Hsu CC, et al. Fracture risk after bariatric surgery: a 12-year nationwide cohort study. Medicine. 2015;94:e2087.
Nakamura KM, Haglind EG, Clowes JA, Achenbach SJ, Atkinson EJ, Melton LJ 3rd, et al. Fracture risk following bariatric surgery: a population-based study. Osteoporosis INT. 2014;25:151–8.
Axelsson KF, Werling M, Eliasson B, Szabo E, Naslund I, Wedel H, et al. Fracture risk after gastric bypass surgery: a retrospective cohort study. JBMR. 2018;12:2122–31.
Yu EW, Kim SC, Sturgeon DJ, Lindeman KG, Weissman JS. Fracture risk after Roux-en-Y gastric bypass vs adjustable gastric banding among medicare beneficiaries. JAMA Surg. 2019;154:746–53.
Schauer PR, Kashyap SR, Wolski K, Brethauer SA, Kirwan JP, Pothier CE, et al. Bariatric surgery versus intensive medical therapy in obese patients with diabetes. NEJM. 2012;366:1567–76.
Blom-Hogestol IK, Mala T, Kristinsson JA, Brunborg C, Gulseth HL, Eriksen EF. Changes in bone quality after Roux-en-Y gastric bypass: a prospective cohort study in subjects with and without type 2 diabetes. Bone. 2019;130:115069.
Goode LR, Brolin RE, Chowdhury HA, Shapses SA. Bone and gastric bypass surgery: effects of dietary calcium and vitamin D. Obes Res. 2004;12:40–7.
Luhrs AR, Davalos G, Lerebours R, Yoo J, Park C, Tabone L, et al. Determining changes in bone metabolism after bariatric surgery in postmenopausal women. Surg Endosc. 2019;34:1754–60.
Guerrero-Perez F, Casajoana A, Gomez-Vaquero C, Virgili N, Lopez-Urdiales R, Hernandez-Montoliu L, et al. Changes in bone mineral density in patients with type 2 diabetes after different bariatric surgery procedures and the role of gastrointestinal hormones. Obes Surg. 2019;30:180–8.
Yu EW, Bouxsein M, Roy AE, Baldwin C, Cange A, Neer RM, et al. Bone loss after bariatric surgery: discordant results between DXA and QCT bone density. JBMR. 2013;29:542–50.
Crawford MR, Pham N, Khan L, Bena JF, Schauer PR, Kashyap SR. Increased bone turnover in type 2 diabetes patients randomized to bariatric surgery vs. medical therapy at 5 years. Endocr Pract. 2017;24:256–64.
Schollenberger AE, Heinze JM, Meile T, Peter A, Konigsrainer A, Bischoff SC. Markers of bone metabolism in obese individuals undergoing laparoscopic sleeve gastrectomy. Obes Surg. 2015;25:1439–45.
Ott MT, Fanti P, Malluche HH, Ryo UY, Whaley FS, Strodel WE, et al. Biochemical-evidence of metabolic bone-disease in women following Roux-Y gastric bypass for morbid-obesity. Obes Surg. 1992;2:341–8.
Yousseif A, Emmanuel J, Karra E, Millet Q, Elkalaawy M, Jenkinson AD, et al. Differential effects of laparoscopic sleeve gastrectomy and laparoscopic gastric bypass on appetite, circulating acyl-ghrelin, peptide YY3-36 and active GLP-1 levels in non-diabetic humans. Obes Surg. 2014;24:241–52.
Ramon JM, Salvans S, Crous X, Puig S, Goday A, Benaiges D, et al. Effect of Roux-en-Y gastric bypass vs sleeve gastrectomy on glucose and gut hormones: a prospective randomised trial. J Gastrointest Surg. 2012;16:1116–22.
Canales BK, Schafer AL, Shoback DM, Carpenter TO. Gastric bypass in obese rats causes bone loss, vitamin D deficiency, metabolic acidosis, and elevated peptide YY. Surg Obes Relat Dis. 2014;10:878–84.
Yu EW, Wewalka M, Ding SA, Simonson DC, Foster K, Holst JJ, et al. Effects of gastric bypass and gastric banding on bone remodeling in obese patients with type 2 diabetes. JCEM. 2015;101:714–22.
Woelnerhanssen B, Peterli R, Steinert RE, Peters T, Borbely Y, Beglinger C. Effects of postbariatric surgery weight loss on adipokines and metabolic parameters: comparison of laparoscopic Roux-en-Y gastric bypass and laparoscopic sleeve gastrectomy–a prospective randomized trial. Surg Obes Relat Dis. 2011;7:561–8.
Trakhtenbroit MA, Leichman JG, Algahim MF, Miller CC 3rd, Moody FG, Lux TR, et al. Body weight, insulin resistance, and serum adipokine levels 2 years after 2 types of bariatric surgery. Am J Med. 2009;122:435–42.
Diker D, Vishne T, Maayan R, Weizman A, Vardi P, Dreznik Z, et al. Impact of gastric banding on plasma adiponectin levels. Obes Surg. 2006;16:1057–61.
Luo XH, Guo LJ, Xie H, Yuan LQ, Wu XP, Zhou HD, et al. Adiponectin stimulates RANKL and inhibits OPG expression in human osteoblasts through the MAPK signaling pathway. JBMR. 2006;21:1648–56.
Biver E, Salliot C, Combescure C, Gossec L, Hardouin P, Legroux-Gerot I, et al. Influence of adipokines and ghrelin on bone mineral density and fracture risk: a systematic review and meta-analysis. JCEM. 2011;96:2703–13.
Acknowledgements
The authors thank the nurses of the Clinical Research Facility, including Srs Lynne Schofield, Vanessa Travers and Ashley Douglas and all the volunteers who participated in the study.
Funding
National Health and Medical Research Council (NHMRC) Scholarship for MMB.
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Study design: JRC, PAB, MMB, JAE, NP, CPW, JJ, MT, DFL. Study conduct: MMB. Data collection: MMB, CPW, JJ, MT, DFL, AH. Data analysis: TT, JRC, DB, MMB, CPW, WC, TVN. Data interpretation: TT, JRC, MMB, PAB, DB, JAE, TVN, CPW, AH. Drafting manuscript: M.B. Revising manuscript content: MMB, JRC, TT, CPW, PAB, JAE. Approving final version of manuscript: all authors. JRC and TT take responsibility for the integrity of the data analysis.
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TT, DB, WC, AH, TVN and PAB have no competing of interests to report. MMB, JJ, AV, CPW, NP, DF-L, JAE and JRC disclosed relevant financial interests outside this body of work. MMB has received a honorarium for educational talk from Astra Zeneca. JJ has received honorarium for educational talk from GORE company. MT has received consulting support from Gore, Medtronic, Ethicon Endosurgery, Olympus and MSD. AV has received a honorarium for educational talk from Astra Zeneca. CPW received consulting and research support from Amgen. N.P received consulting and research support from Amgen. DF-L received consulting support from Medtronic. JRC has received honoraria for educational talks and/or been on Advisory boards from Amgen and Theramex/Teva. JAE received consulting and research support from Amgen, Eli Lilly, Merck Sharp and Dohme and Novartis. This does not alter our adherence to JBMR policies on sharing data and materials.
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Brzozowska, M.M., Tran, T., Bliuc, D. et al. Roux-en-Y gastric bypass and gastric sleeve surgery result in long term bone loss. Int J Obes 45, 235–246 (2021). https://doi.org/10.1038/s41366-020-00660-x
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DOI: https://doi.org/10.1038/s41366-020-00660-x
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