Abstract
Bariatric surgery may negatively impact bone health. We aimed to compare fracture risk following bariatric surgery by type (malabsorptive, restrictive), or to non-surgical weight loss, or to controls with obesity. We systematically searched four databases from inception until October 2020. We included observational and interventional studies on adults. We screened articles and abstracted data in duplicate and independently and assessed the risk of bias. We conducted random-effects model meta-analyses (Review Manager v5.3), to calculate the relative risk of any or site-specific fracture (CRD42019128536). We identified four trials of unclear-to-high risk of bias and 15 observational studies of fair-to-good quality. Data on fracture risk following bariatric surgery compared to medical weight loss is scarce and limited by the small number of participants. In observational studies, at a mean/median post-operative follow-up > 2 years, the relative risk of any fracture was 45% (p < 0.001) and 61% (p = 0.04) higher following malabsorptive procedures compared to obese controls and restrictive procedures, respectively, with moderate to high heterogeneity. Site-specific relative fracture risk (hip and wrist) was one- to two-folds higher post malabsorptive procedures compared to obese controls or restrictive procedures. The risks of any and of site-specific fracture were not increased following restrictive procedures compared to obese controls. Fracture risk seems to increase following malabsorptive bariatric surgeries, at a mean/median follow-up > 2 years. The risk is not increased with restrictive surgeries. The available evidence has several limitations. A prospective and rigorous long-term follow-up of patients following bariatric surgery is needed for a better assessment of their fracture risk with aging.
Similar content being viewed by others
Abbreviations
- LGB:
-
Laparoscopic gastric banding
- RYGB:
-
Roux-en-Y gastric bypass
- BPD:
-
Biliopancreatic diversion without a duodenal switch
- BPD-DS:
-
Biliopancreatic diversion with a duodenal switch
- SG:
-
Sleeve gastrectomy
- BMD:
-
Bone mineral density
- SR/MAs:
-
Systematic reviews/meta-analyses
- BMI:
-
Body mass index
- ROB:
-
Risk of bias
- NOS:
-
Newcastle-Ottawa Quality Assessment Scale
- RR:
-
Risk ratio
- IMT:
-
Intensive medical therapy
- VBG:
-
Vertical banded gastroplasty
- RCT:
-
Randomized controlled trials
- NRCT:
-
Non-randomized controlled trials
- DM:
-
Diabetes mellitus
- DSS:
-
Diabetes Surgery Study
- STAMPEDE:
-
Surgical Therapy And Medications Potentially Eradicate Diabetes Efficiently
- SOS:
-
Swedish Obesity Study
- aHR:
-
Adjusted hazard ratio
- ICD:
-
International Classification of Disease
References
Brolin RE (2002) Bariatric surgery and long-term control of morbid obesity. JAMA 288:2793–2796
Kwok CS, Pradhan A, Khan MA, Anderson SG, Keavney BD, Myint PK, Mamas MA, Loke YK (2014) Bariatric surgery and its impact on cardiovascular disease and mortality: a systematic review and meta-analysis. Int J Cardiol 173:20–28
Sharples AJ, Mahawar K (2020) Systematic review and meta-analysis of randomised controlled trials comparing Long-term outcomes of Roux-En-Y gastric bypass and sleeve gastrectomy. Obes Surg 30:664–672
Surgery ASfMaB Bariatric surgery procedures. https://asmbs.org/patients/bariatric-surgery-procedures. Accessed 27 Jul 2021
Pucci A, Batterham RL (2019) Mechanisms underlying the weight loss effects of RYGB and SG: similar, yet different. J Endocrinol Invest 42:117–128
Saad R, Habli D, El Sabbagh R, Chakhtoura M (2020) Bone health following bariatric surgery: an update. J Clin Densitom 23(2):165–181
Strain WD, Down S, Brown P, Puttanna A, Sinclair A (2021) Diabetes and frailty: an expert consensus statement on the management of older adults with type 2 diabetes. Diabetes Ther 12:1227–1247
Defeudis G, Mazzilli R, Gianfrilli D, Lenzi A, Isidori AM (2018) The CATCH checklist to investigate adult-onset hypogonadism. J Androl 6:665–679
Cauley JA, Ellenberg SS, Schwartz AV, Ensrud KE, Keaveny TM, Snyder PJ (2021) Effect of testosterone treatment on the trabecular bone score in older men with low serum testosterone. Osteoporos Int. https://doi.org/10.1007/s00198-021-06022-1
Paccou J, Caiazzo R, Lespessailles E, Cortet B (2021) Bariatric surgery and osteoporosis. Calcif Tissue Int. https://doi.org/10.1007/s00223-020-00798-w
Gregory NS (2017) The effects of bariatric surgery on bone metabolism. Endocrinol Metab Clin North Am 46:105–116
Hage MP, El-Hajj Fuleihan G (2014) Bone and mineral metabolism in patients undergoing Roux-en-Y gastric bypass. Osteoporos Int 25:423–439
Patel JJ, Mundi MS, Hurt RT, Wolfe B, Martindale RG (2017) Micronutrient deficiencies after bariatric surgery: an emphasis on vitamins and trace minerals. Nutr Clin Pract 32:471–480
Via MA, Mechanick JI (2017) Nutritional and micronutrient care of bariatric surgery patients: current evidence update. Curr Obes Rep 6:286–296
Gagnon C, Schafer AL (2018) Bone health after bariatric surgery. JBMR Plus 2:121–133
Carlsson LMS, Sjöholm K, Ahlin S et al (2019) Long-term incidence of serious fall-related injuries after bariatric surgery in Swedish obese subjects. Int J Obes 43:933–937
Nguyen TV, Center JR, Eisman JA (2005) Femoral neck bone loss predicts fracture risk independent of baseline BMD. J Bone Miner Res 20:1195–1201
Briot K, Roux C (2013) Corticosteroid-induced osteoporosis. Rev Med Interne 34:315–323
Rachner TD, Coleman R, Hadji P, Hofbauer LC (2018) Bone health during endocrine therapy for cancer. Lancet Diabetes Endocrinol 6:901–910
Ablett AD, Boyle BR, Avenell A (2019) Fractures in adults after weight loss from bariatric surgery and weight management programs for obesity: systematic review and meta-analysis. Obes Surg 29:1327–1342
Marcil G, Bourget-Murray J, Shinde S, Switzer N, Debru E, Church N, Mitchell P, Reso A, Gill RS (2018) The incidence of fractures following bariatric surgery: a systematic review. Int J Surg Open 14:9–14
Zhang Q, Chen Y, Li J, Chen D, Cheng Z, Xu S, Huang Y, Wang Q (2018) A meta-analysis of the effects of bariatric surgery on fracture risk. Obes Rev 19:728–736
Zhang Q, Dong J, Zhou D, Liu F (2020) Comparative risk of fracture for bariatric procedures in patients with obesity: a systematic review and Bayesian network meta-analysis. Int J Surg 75:13–23
Chakhtoura M, Saad R, Habli D, Sabbagh R, Boueiz N (2019) Fracture risk following bariatric surgery: a systematic review and meta-analysis of observational studies. https://www.crd.york.ac.uk/PROSPERO/display_record.php?RecordID=128536. Accessed 27 Jul 2021
GA Wells BS, D O'Connell, J Peterson, V Welch, M Losos, P Tugwell (2019) The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp 2019. Accessed 27 Jul 2021
Higgins JJT, Chandler J, Cumpston M, Tianjing L, Page M, Welch V (2019) Cochrane handbook for systematic reviews of interventions. https://training.cochrane.org/handbook. Accessed 27 Jul 2021
Yu EW, Bouxsein ML, Roy AE, Baldwin C, Cange A, Neer RM, Kaplan LM, Finkelstein JS (2014) Bone loss after bariatric surgery: discordant results between DXA and QCT bone density. J Bone Miner Res 29:542–550
Vilarrasa N, Vilarrasa N, San José P et al (2011) Evaluation of bone mineral density loss in morbidly obese women after gastric bypass: 3-year follow-up. Obes Surg 21:465–472
Ruiz-Tovar J, Oller I, Priego P, Arroyo A, Calero A, Diez M, Zubiaga L, Calpena R (2013) Short- and mid-term changes in bone mineral density after laparoscopic sleeve gastrectomy. Obes Surg 23:861–866
Prevention CfDCa measures of risk. https://www.cdc.gov/csels/dsepd/ss1978/lesson3/section2.html. Accessed 27 Jul 2021
Crawford MR, Pham N, Khan L, Bena JF, Schauer PR, Kashyap SR (2018) Increased bone turnover in type 2 diabtes patients randomized to bariatric surgery versus medical therapy at 5 years. Endocr Pract 24:256–264
Ikramuddin S, Billington CJ, Lee WJ et al (2015) Roux-en-Y gastric bypass for diabetes (the Diabetes Surgery Study): 2-year outcomes of a 5-year, randomised, controlled trial. Lancet Diabetes Endocrinol 3:413–422
Ikramuddin S, Korner J, Lee WJ et al (2018) Lifestyle intervention and medical management with vs without Roux-en-Y gastric bypass and control of hemoglobin A1c, LDL cholesterol, and systolic blood pressure at 5 years in the diabetes surgery study. JAMA 319:266–278
Maghrabi AH, Wolski K, Abood B et al (2015) Two-year outcomes on bone density and fracture incidence in patients with T2DM randomized to bariatric surgery versus intensive medical therapy. Obes 23:2344–2348
Schauer PR, Bhatt DL, Kirwan JP et al (2017) Bariatric surgery versus intensive medical therapy for diabetes - 5-year outcomes. New Eng J Med 376:641–651
Hofso D, Nordstrand N, Johnson LK et al (2010) Obesity-related cardiovascular risk factors after weight loss: a clinical trial comparing gastric bypass surgery and intensive lifestyle intervention. Eur J Endocrinol 163:735–745
Ahlin S, Peltonen M, Sjöholm K et al (2020) Fracture risk after three bariatric surgery procedures in Swedish obese subjects: up to 26 years follow-up of a controlled intervention study. J Intern Med 287:546–557
Guney E, Kisakol G, Ozgen G, Yilmaz C, Yilmaz R, Kabalak T (2003) Effect of weight loss on bone metabolism: comparison of vertical banded gastroplasty and medical intervention. Obes Surg 13:383–388
Muschitz C, Kocijan R, Marterer C, Nia AR, Muschitz GK, Resch H, Pietschmann P (2015) Sclerostin levels and changes in bone metabolism after bariatric surgery. J Clin Endocrinol Metab 100:891–901
Costa TL, Paganotto M, Radominski RB, Kulak CM, Borba VC (2015) Calcium metabolism, vitamin D and bone mineral density after bariatric surgery. Osteoporos Int 26:757–764
Axelsson KF, Werling M, Eliasson B, Szabo E, Näslund I, Wedel H, Lundh D, Lorentzon M (2018) Fracture risk after gastric bypass surgery: a retrospective cohort study. J Bone Miner Res 33:2122–2131
Douglas IJ, Bhaskaran K, Batterham RL, Smeeth L (2015) Bariatric surgery in the United Kingdom: a cohort study of weight loss and clinical outcomes in routine clinical care. PLoS Med 12(12):e1001925
Fashandi AZ, Mehaffey JH, Hawkins RB, Schirmer B, Hallowell PT (2018) Bariatric surgery increases risk of bone fracture. Surg Endosc 32:2650–2655
Javanainen M, Pekkarinen T, Mustonen H, Scheinin T, Leivonen M (2018) Two-year nutrition data in terms of vitamin D, vitamin B12, and albumin after bariatric surgery and long-term fracture data compared with conservatively treated obese patients: a retrospective cohort study. Obes Surg 28:2968–2975
Lalmohamed A, de Vries F, Bazelier MT, Cooper A, van Staa TP, Cooper C, Harvey NC (2012) Risk of fracture after bariatric surgery in the United Kingdom: population based, retrospective cohort study. BMJ 345:e5085
Lu CW, Chang YK, Chang HH, Kuo CS, Huang CT, Hsu CC, Huang KC (2015) Fracture risk after bariatric surgery: a 12-year nationwide cohort study. J Med 94:e2087
O’Keefe KL, Kemmeter PR, Kemmeter KD (2010) Bariatric surgery outcomes in patients aged 65 years and older at an American society for metabolic and bariatric surgery center of excellence. Obes Surg 20:1199–1205
Rousseau C, Jean S, Gamache P, Lebel S, Mac-Way F, Biertho L, Michou L, Gagnon C (2016) Change in fracture risk and fracture pattern after bariatric surgery: nested case-control study. BMJ 354:i3794
Yu EW, Kim SC, Sturgeon DJ, Lindeman KG, Weissman JS (2019) Fracture risk after roux-en-y gastric bypass vs adjustable gastric banding among medicare beneficiaries. JAMA Surg 154:746–753
Yu EWL MP, LandonJ E, Lindeman KG, Kim SC (2017) Fracture risk after bariatric surgery: Roux-en-y gastric bypass versus adjustable gastric banding. J Bone Miner Res 32:1229–1236
Khalid SI, Omotosho PA, Spagnoli A, Torquati A (2020) Association of bariatric surgery with risk of fracture in patients with severe obesity. JAMA Netw 3:e207419–e207419
Paccou J, Martignène N, Lespessailles E, Babykina E, Pattou F, Cortet B, Ficheur G (2020) Gastric bypass but not sleeve gastrectomy increases risk of major osteoporotic fracture: French population-based cohort study. J Bone Miner Res 35:1415–1423
Young MT, Phelan MJ, Nguyen NT (2016) A decade analysis of trends and outcomes of male vs female patients who underwent bariatric surgery. J Am Coll Surg 222:226–231
Torgersen Z, Osmolak A, Forse RA (2014) Sleeve gastrectomy and roux en y gastric bypass: current state of metabolic surgery. Curr Opin Endocrinol Diabetes Obes 21:352–357
Tian S, Zhao D (2018) The effects of bariatric surgery on fracture risk: is there a significant higher risk? Obes Rev 19:1460–1461
Beavers KM, Greene KA, Yu EW (2020) Bone complications of bariatric surgery: updates on sleeve gastrectomy, fractures, and interventions. Eur J Endocrinol 183:R119–R132
Buchwald H, Avidor Y, Braunwald E (2005) Bariatric surgery: a systematic review and meta-analysis. ACC Curr J Rev 14:13–13
Stein E, Silverberg S (2014) Bone loss after bariatric surgery: causes, consequences, and management. Lancet Diabetes Endocrinol 2:165–174
Hofsø D, Hillestad TOW, Halvorsen E, Fatima F, Johnson LK, Lindberg M et al (2021) Bone mineral density and turnover after sleeve gastrectomy and gastric bypass: a randomized controlled trial (Oseberg). J Clin Endocrinol Metab 106:501–511
Tian Z, Fan X-T, Li S-Z, Zhai T, Dong J (2020) Changes in bone metabolism after sleeve gastrectomy versus gastric bypass: a meta-analysis. Obes Surg 30:77–86
Palermo A, Tuccinardi D, Defeudis G, Watanabe M, D’Onofrio L, LauriaPantano A, Napoli N, Pozzilli P, Manfrini S (2016) BMI and BMD: the potential interplay between obesity and bone fragility. Int J Environ Res Pub He 13:544
Lespessailles E, Paccou J, Javier R-M, Thomas T, Cortet B, Committee GS (2019) Obesity, bariatric surgery and fractures. J Clin Endocrinol Metab 104:4756–4768
Compston J, Watts N, Chapurlat R et al (2011) Obesity is not protective against fracture in postmenopausal women: GLOW. Am J Med 124:1043–1050
Johansson H, Kanis JA, Odén A et al (2014) A meta-analysis of the association of fracture risk and body mass index in women. J Bone Miner Res 29:223–233
Reeve J, Loveridge N (2014) The fragile elderly hip: mechanisms associated with age-related loss of strength and toughness. Bone 61:138–148
Kanis JA, McCloskey E (1992) Epidemiology of vertebral osteoporosis. Bone 13:S1–S10
Kanis JA, Johnell O, De Laet C et al (2004) A meta-analysis of previous fracture and subsequent fracture risk. Bone 35:375–382
Nakamura KM, Haglind EGC, Clowes JA, Achenbach SJ, Atkinson EJ, Melton LJ, Kennel KA (2014) Fracture risk following bariatric surgery: a population-based study. Osteoporos Int 25:151–158
Acknowledgements
The work was supported in part by the Fogarty International Center and the Office of Dietary Supplements of the National Institutes of Health (NIH), award number D43 TW009118. The content is solely the responsibility of authors and does not necessarily represent official views of the NIH. The authors thank Miss Aida Farha, Medical Information Specialist, Saab Medical Library at the American University of Beirut—Lebanon, for her assistance in designing comprehensive complex searches of the medical literature and for the provision of select articles. The authors thank Dr. Rawaa Sabbagh for her contribution in the screening process of citations and full texts. The authors also thank the corresponding authors: Dr. Kennel Kurt [68], Dr. Claudia Gagnon [48], and Dr. Peter Hallowell [43], who have replied to their queries by email.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Saad, R.K., Ghezzawi, M., Habli, D. et al. Fracture risk following bariatric surgery: a systematic review and meta-analysis. Osteoporos Int 33, 511–526 (2022). https://doi.org/10.1007/s00198-021-06206-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00198-021-06206-9