Abstract
Summary
The effects of bariatric surgery on skeletal health are poorly understood. We found that bariatric surgery patients are more prone to fracture when compared to the general population. While further studies of fracture risk in this population are needed, bone health should be discussed in bariatric surgery clinics.
Introduction
Bariatric surgery is an increasingly common treatment for medically complicated obesity. Adverse skeletal changes after bariatric surgery have been reported, but their clinical importance remains unknown. We hypothesized that bariatric surgery patients are at increased risk of fracture.
Methods
We conducted a historical cohort study of fracture incidence among 258 Olmsted County, Minnesota, residents who underwent a first bariatric surgery in 1985–2004. Relative fracture risk was expressed as standardized incidence ratios (SIRs), while potential risk factors were evaluated by hazard ratios (HR) obtained from a time-to-fracture regression model.
Results
The mean (±SD) body mass index at bariatric surgery was 49.0 ± 8.4 kg/m2, with an average age of 44 ± 10 years and 82 % (212) females. Gastric bypass surgery was performed in 94 % of cases. Median follow-up was 7.7 years (range, 6 days to 25 years), during which 79 subjects experienced 132 fractures. Relative risk for any fracture was increased 2.3-fold (95 % confidence interval (CI), 1.8–2.8) and was elevated for a first fracture at the hip, spine, wrist, or humerus (SIR, 1.9; 95 % CI, 1.1–2.9), as well as for a first fracture at any other site (SIR, 2.5; 95 % CI, 2.0–3.2). Better preoperative activity status was associated with a lower age-adjusted risk (HR, 0.4; 95 % CI, 0.2–0.8) while prior fracture history was not associated with postoperative fracture risk.
Conclusions
Bariatric surgery, which is accompanied by substantial biochemical, hormonal, and mechanical changes, is associated with an increased risk of fracture.
Similar content being viewed by others
References
Centers for Disease Control and Prevention (2011) Overweight and obesity. http://www.cdc.gov/obesity. Accessed 2 Jan 2013
Sjostrom L, Lindroos AK, Peltonen M, Torgerson J, Bouchard C, Carlsson B, Dahlgren S, Larsson B, Narbro K, Sjostrom CD, Sullivan M, Wedel H (2004) Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. N Engl J Med 351:2683–2693
Adams TD, Gress RE, Smith SC, Halverson RC, Simper SC, Rosamond WD, Lamonte MJ, Stroup AM, Hunt SC (2007) Long-term mortality after gastric bypass surgery. N Engl J Med 357:753–761
American Society for Metabolic and Bariatric Surgery (2010) Fact sheet: metabolic and bariatric surgery. http://asmbs.org/ Accessed November 11 2011
Berarducci A, Haines K, Murr MM (2009) Incidence of bone loss, falls, and fractures after Roux-en-Y gastric bypass for morbid obesity. Appl Nurs Res 22:35–41
Abu-Lebdeh HS, Paat JJ (2010) Are post bariatric surgery fractures different from fractures in severely obese subjects? In IOF World Congress on Osteoporosis. Florence, Italy
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
Tice JA, Karliner L, Walsh J, Petersen AJ, Feldman MD (2008) Gastric banding or bypass? A systematic review comparing the two most popular bariatric procedures. Am J Med 121:885–893
Dixon JB, Strauss BJ, Laurie C, O’Brien PE (2007) Changes in body composition with weight loss: obese subjects randomized to surgical and medical programs. Obesity (Silver Spring) 15:1187–1198
von Mach MA, Stoeckli R, Bilz S, Kraenzlin M, Langer I, Keller U (2004) Changes in bone mineral content after surgical treatment of morbid obesity. Metabolism 53:918–921
Shapses SA, Sukumar D (2012) Bone metabolism in obesity and weight loss. Annu Rev Nutr 32:287–309
Shah M, Simha V, Garg A (2006) Review: long-term impact of bariatric surgery on body weight, comorbidities, and nutritional status. J Clin Endocrinol Metab 91:4223–4231
De Prisco C, Levine SN (2005) Metabolic bone disease after gastric bypass surgery for obesity. Am J Med Sci 329:57–61
Mosekilde L, Melsen F, Hessov I, Christensen MS, Lund BJ, Lund BI, Sorensen OH (1980) Low serum levels of 1.25-dihydroxyvitamin D and histomorphometric evidence of osteomalacia after jejunoileal bypass for obesity. Gut 21:624–631
Collazo-Clavell ML, Jimenez A, Hodgson SF, Sarr MG (2004) Osteomalacia after Roux-en-Y gastric bypass. Endocr Pract 10:195–198
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
Fleischer J, Stein EM, Bessler M, Della Badia M, Restuccia N, Olivero-Rivera L, McMahon DJ, Silverberg SJ (2008) The decline in hip bone density after gastric bypass surgery is associated with extent of weight loss. J Clin Endocrinol Metab 93:3735–3740
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
Johnson JM, Maher JW, Samuel I, Heitshusen D, Doherty C, Downs RW (2005) Effects of gastric bypass procedures on bone mineral density, calcium, parathyroid hormone, and vitamin D. J Gastrointest Surg 9:1106–1110, discussion 1110–1101
Carrasco F, Ruz M, Rojas P, Csendes A, Rebolledo A, Codoceo J, Inostroza J, Basfi-Fer K, Papapietro K, Rojas J, Pizarro F, Olivares M (2009) Changes in bone mineral density, body composition and adiponectin levels in morbidly obese patients after bariatric surgery. Obes Surg 19:41–46
Belle S (2005) The NIDDK bariatric surgery clinical research consortium (LABS). Surg Obes Relat Dis 1:145–147
Rocca WA, Yawn BP, St Sauver JL, Grossardt BR, Melton LJ 3rd (2012) History of the Rochester Epidemiology Project: half a century of medical records linkage in a US population. Mayo Clin Proc 87:1202–1213
Melton LJ 3rd (1997) The threat to medical-records research. N Engl J Med 337:1466–1470
Melton LJ 3rd, Crowson CS, O’Fallon WM (1999) Fracture incidence in Olmsted County, Minnesota: comparison of urban with rural rates and changes in urban rates over time. Osteoporos Int 9:29–37
Melton LJ 3rd, Alothman KI, Khosla S, Achenbach SJ, Oberg AL, Zincke H (2003) Fracture risk following bilateral orchiectomy. J Urol 169:1747–1750
Mackey DC, Lui LY, Cawthon PM, Bauer DC, Nevitt MC, Cauley JA, Hillier TA, Lewis CE, Barrett-Connor E, Cummings SR (2007) High-trauma fractures and low bone mineral density in older women and men. JAMA 298:2381–2388
Cox DR (1953) Some simple approximate tests for Poisson variates. Biometrika 40:354–360
Kaplan EL, Meier P (1958) Non-parametric estimation from incomplete observations. J Am Stat Assoc 53:457–481
Kalbfleisch JD, Prentice RL (eds) (1980) The statistical analysis of failure time data. Wiley, New York
Therneau TM, Grambsch PM (2000) Modeling survival data: extending the Cox model. Springer, New York
Firth D (1993) Bias reduction of maximum likelihood estimates. Biometrika 80:27–38
De Laet C, Kanis JA, Oden A, Johanson H, Johnell O, Delmas P, Eisman JA, Kroger H, Fujiwara S, Garnero P, McCloskey EV, Mellstrom D, Melton LJ 3rd, Meunier PJ, Pols HA, Reeve J, Silman A, Tenenhouse A (2005) Body mass index as a predictor of fracture risk: a meta-analysis. Osteoporos Int 16:1330–1338
Compston JE, Watts NB, Chapurlat R, Cooper C, Boonen S, Greenspan S, Pfeilschifter J, Silverman S, Diez-Perez A, Lindsay R, Saag KG, Netelenbos JC, Gehlbach S, Hooven FH, Flahive J, Adachi JD, Rossini M, LaCroix AZ, Roux C, Sambrook PN et al (2011) Obesity is not protective against fracture in postmenopausal women: GLOW. Am J Med 124:1043–1050
Premaor MO, Pilbrow L, Tonkin C, Parker RA, Compston J (2010) Obesity and fractures in postmenopausal women. J Bone Miner Res 25:292–297
Nielson CM, Marshall LM, Adams AL, LeBlanc ES, Cawthon PM, Ensrud K, Stefanick ML, Barrett-Connor E, Orwoll ES, for the Osteoporotic Fractures in Men Study Research G (2011) BMI and fracture risk in older men: The Osteoporotic Fractures in Men Study (MrOS). J Bone Miner Res 26:496–502
Bruno C, Fulford AD, Potts JR, McClintock R, Jones R, Cacucci BM, Gupta CE, Peacock M, Considine RV (2010) Serum markers of bone turnover are increased at 6 and 18 months after Roux-en-Y bariatric surgery: correlation with the reduction in leptin. J Clin Endocrinol Metab 95:159–166
Riedt CS, Brolin RE, Sherrell RM, Field MP, Shapses SA (2006) True fractional calcium absorption is decreased after Roux-en-Y gastric bypass surgery. Obesity (Silver Spring) 14:1940–1948
Hewitt S, Sovik TT, Aasheim ET, Kristinsson J, Jahnsen J, Birketvedt GS, Bohmer T, Eriksen EF, Mala T (2013) Secondary hyperparathyroidism, vitamin D sufficiency, and serum calcium 5 years after gastric bypass and duodenal switch. Obes Surg 23:384–390
Pramyothin P, Biancuzzo RM, Lu Z, Hess DT, Apovian CM, Holick MF (2011) Vitamin D in adipose tissue and serum 25-hydroxyvitamin D after roux-en-Y gastric bypass. Obesity (Silver Spring) 19:2228–2234
Beckman LM, Earthman CP, Thomas W, Compher CW, Muniz J, Horst RL, Ikramuddin S, Kellogg TA, Sibley SD (2013) Serum 25(OH) vitamin D concentration changes after roux-en-y gastric bypass surgery. Obesity (Silver Spring) (in press)
Carlin AM, Rao DS, Yager KM, Parikh NJ, Kapke A (2009) Treatment of vitamin D depletion after Roux-en-Y gastric bypass: a randomized prospective clinical trial. Surg Obes Relat Dis 5:444–449
Ricci TA, Heymsfield SB, Pierson RN Jr, Stahl T, Chowdhury HA, Shapses SA (2001) Moderate energy restriction increases bone resorption in obese postmenopausal women. Am J Clin Nutr 73:347–352
Rosen CJ, Klibanski A (2009) Bone, fat, and body composition: evolving concepts in the pathogenesis of osteoporosis. Am J Med 122:409–414
Reid IR (2008) Relationships between fat and bone. Osteoporos Int 19:595–606
Gomez-Ambrosi J, Rodriguez A, Catalan V, Fruhbeck G (2008) The bone-adipose axis in obesity and weight loss. Obes Surg 18:1134–1143
Weyer C, Funahashi T, Tanaka S, Hotta K, Matsuzawa Y, Pratley RE, Tataranni PA (2001) Hypoadiponectinemia in obesity and type 2 diabetes: close association with insulin resistance and hyperinsulinemia. J Clin Endocrinol Metab 86:1930–1935
Pories WJ, MacDonald KG Jr, Flickinger EG, Dohm GL, Sinha MK, Barakat HA, May HJ, Khazanie P, Swanson MS, Morgan E et al (1992) Is type II diabetes mellitus (NIDDM) a surgical disease? Ann Surg 215:633–642, discussion 643
Sukumar D, Ambia-Sobhan H, Zurfluh R, Schlussel Y, Stahl TJ, Gordon CL, Shapses SA (2011) Areal and volumetric bone mineral density and geometry at two levels of protein intake during caloric restriction: a randomized, controlled trial. J Bone Miner Res 26:1339–1348
St Sauver JL, Grossardt BR, Leibson CL, Yawn BP, Melton LJ 3rd, Rocca WA (2012) Generalizability of epidemiological findings and public health decisions: an illustration from the Rochester Epidemiology Project. Mayo Clin Proc 87:151–160
Acknowledgments
We would like to thank Dr. Michael Sarr for providing the database of all patients completing a bariatric surgery procedure at Mayo Clinic between 1985 and 2004. This study was supported in part by the Division of Endocrinology, Mayo Clinic, Rochester, and P01-AG-04875 from the National Institute on Aging and made possible by the Rochester Epidemiology Project (R01-AG-034676 from the National Institute on Aging), US Public Health Service. The content of this manuscript is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
Conflicts of interest
None.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Nakamura, K.M., Haglind, E.G.C., Clowes, J.A. et al. Fracture risk following bariatric surgery: a population-based study. Osteoporos Int 25, 151–158 (2014). https://doi.org/10.1007/s00198-013-2463-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00198-013-2463-x