Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Bariatric Surgery

Bone mineral density in young adults 5 to 11 years after adolescent metabolic and bariatric surgery for severe obesity compared to peers

Abstract

Objective

Metabolic and bariatric surgery (MBS) is associated with decreased bone mineral density (BMD) in adults. The long-term impact of MBS during adolescence on BMD is unknown. We report bone health status 5 to 11 years after Roux-en-Y gastric bypass (RYGB) and vertical sleeve gastrectomy (VSG) from the Teen-LABS study cohort.

Methods

Between 2016 and 2022, BMD was measured by dual energy x-ray absorptiometry (DXA) in 106 young adults who had undergone MBS as adolescents. Volumetric BMD by peripheral quantitative computed tomography was measured on a subset. Ninety-one controls who had not undergone MBS were recruited for comparison.

Results

In cases (RYGB: mean age 26.8 ± 1.9 years, mean BMI 42.1 ± 9.9 kg/m2, VSG: mean age 25.1 ± 2.1 years, mean BMI 37.1 ± 8.4 kg/m2), compared to controls (mean age 26.5 ± 2.7 years, mean BMI 40.2 ± 8.7 kg/m2) (age p < 0.001, BMI p = 0.02), adjusted mean DXA-BMD (g/cm2) of the RYGB (n = 58) and VSG (n = 48) groups were lower at the hip (−10.0% and −6.3%), femoral neck (−9.6% and −5.7%) and ultra-distal radius (−7.9% and −7.0%; all p < 0.001), respectively. DXA-BMD did not differ between RYGB and VSG groups. Trabecular volumetric BMD at the radius and tibia were lower in the RYGB (−30% and −26%) and VSG (−15% and −14%) groups compared to the control group (p < 0.001). Greater time since MBS was associated with lower BMD Z-scores at the hip (p = 0.05) and femoral neck (p = 0.045). Percent change in body mass index (BMI) from baseline or in the first year after MBS were not associated with bone measures at a median of 9.3 years post MBS.

Conclusion

BMD, especially of the hip and femoral neck, was lower in young adults who underwent MBS during adolescence compared to matched peers who had not undergone MBS. BMD Z-scores of the femoral neck were inversely associated with time since MBS but were not associated with BMI change.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Adjusted mean dual energy x-ray absorptiometry (DXA) outcomes for metabolic and bariatric surgery groups and matched controls.
Fig. 2: Adjusted mean peripheral quantitative computed tomography (pQCT) outcomes for metabolic and bariatric surgery groups and matched controls.

Similar content being viewed by others

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Michalsky MP, Inge TH, Jenkins TM, Xie C, Courcoulas A, Helmrath M, et al. Cardiovascular Risk Factors After Adolescent Bariatric Surgery. Pediatrics. 2018;141:e20172485.

    Article  PubMed  Google Scholar 

  2. Stanford FC, Mushannen T, Cortez P, Campoverde Reyes KJ, Lee H, Gee DW, et al. Comparison of short and long-term outcomes of metabolic and bariatric surgery in adolescents and adults. Front Endocrinol (Lausanne). 2020;11:157.

    Article  PubMed  Google Scholar 

  3. Ryder JR, Xu P, Inge TH, Xie C, Jenkins TM, Hur C, et al. Thirty-year risk of cardiovascular disease events in adolescents with severe obesity. Obesity (Silver Spring). 2020;28:616–23.

    Article  PubMed  Google Scholar 

  4. Kim J, Nimeri A, Khorgami Z, El Chaar M, Lima AG, Vosburg RW. Metabolic bone changes after bariatric surgery: 2020 update, American Society for Metabolic and Bariatric Surgery Clinical Issues Committee position statement. Surg Obes Relat Dis. 2021;17:1–8.

    Article  PubMed  Google Scholar 

  5. Beamish AJ, Harper ER, Järvholm K, Janson A, Olbers T. Long-term outcomes following adolescent metabolic and bariatric surgery. J Clin Endocrinol Metab. 2023;108:2184–92.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Casagrande DS, Repetto G, Mottin CC, Shah J, Pietrobon R, Worni M, et al. Changes in bone mineral density in women following 1-year gastric bypass surgery. Obes Surg. 2012;22:1287–92.

    Article  PubMed  Google Scholar 

  7. 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. J Clin Endocrinol Metab. 2015;100:1452–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Fleischer J, Stein EM, Bessler M, Della Badia M, Restuccia N, et al. The decline in hip bone density after gastric bypass surgery is associated with extent of weight loss. J Clin Endocrinol Metab. 2008;93:3735–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. J Clin Endocrinol Metab. 2018;103:4104–12.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Lindeman KG, Rushin CC, Cheney MC, Bouxsein ML, Hutter MM, Yu EW. Bone density and trabecular morphology at least 10 years after gastric bypass and gastric banding. J Bone Miner Res. 2020;35:2132–42.

    Article  CAS  PubMed  Google Scholar 

  11. Reyes ML, Hernandez M, Samso C, Palma MP, Escobar R, Holmgren LJ. Quality of life assessment (PedsQL) in children at risk of disuse osteoporosis: Decreases of appendicular bone mineral density is associated to a greater body pain. Bone. 2007;40:S73–S.

    Google Scholar 

  12. Ebadinejad A, Ahmadi AR, Ghazy F, Barzin M, Khalaj A, Valizadeh M, et al. Changes in bone turnover markers after roux-en-y gastric bypass versus sleeve gastrectomy: a systematic review and meta-analysis. Obes Surg. 2023;33:1259–69.

    Article  PubMed  Google Scholar 

  13. Hofsø D, Hillestad TOW, Halvorsen E, Fatima F, Johnson LK, Lindberg M, et al. Bone mineral density and turnover after sleeve gastrectomy and gastric bypass: a randomized controlled trial (oseberg). J Clin Endocrinol Metab. 2021;106:501–11.

    Article  PubMed  Google Scholar 

  14. Raoof M, Näslund 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.

    Article  PubMed  Google Scholar 

  15. Ieong K, Ardila-Gatas J, Yang J, Zhang X, Tsui ST, Spaniolas K, et al. Bone mineral density changes after bariatric surgery. Surg Endosc. 2021;35:4763–70.

    Article  PubMed  Google Scholar 

  16. Sperb LF, Leotti VB, Silveiro SP, de Azevedo MJ, Viana LV. Long-term changes in bone density and bone metabolism after gastric bypass surgery: a retrospective cohort study. Obes Surg. 2023;33:911–9.

    Article  PubMed  Google Scholar 

  17. de Holanda NCP, Baad VMA, Bezerra LR, de Lima SKM, Filho JM, de Holanda Limeira CC, et al. Secondary hyperparathyroidism, bone density, and bone turnover after bariatric surgery: differences between roux-en-y gastric bypass and sleeve gastrectomy. Obes Surg. 2021;31:5367–75.

    Article  PubMed  Google Scholar 

  18. Paccou J, Tsourdi E, Meier C, Palermo A, Pepe J, Body JJ, et al. Bariatric surgery and skeletal health: A narrative review and position statement for management by the European Calcified Tissue Society (ECTS). Bone. 2022;154:116236.

    Article  PubMed  Google Scholar 

  19. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Yu EW, Lee MP, Landon JE, Lindeman KG, Kim SC. Fracture risk after bariatric surgery: Roux-en-Y gastric bypass versus adjustable gastric banding. J Bone Miner Res. 2017;32:1229–36.

    Article  PubMed  Google Scholar 

  21. Robinson DE, Douglas I, Tan GD, Delmestri A, Judge A, Cooper C, et al. Bariatric surgery increases the rate of major fracture: self-controlled case series study in UK Clinical Practice Research Datalink. J Bone Miner Res. 2021;36:2153–61.

    Article  PubMed  Google Scholar 

  22. Khalid SI, Omotosho PA, Spagnoli A, Torquati A. Association of bariatric surgery with risk of fracture in patients with severe obesity. JAMA Netw Open. 2020;3:e207419.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Ahlin S, Peltonen M, Sjöholm K, Anveden Å, Jacobson P, Andersson-Assarsson JC, et al. 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. 2020;287:546–57.

    Article  CAS  PubMed  Google Scholar 

  24. Kaulfers AM, Bean JA, Inge TH, Dolan LM, Kalkwarf HJ. Bone loss in adolescents after bariatric surgery. Pediatrics. 2011;127:e956–61.

    Article  PubMed  PubMed Central  Google Scholar 

  25. 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.

    Article  CAS  PubMed  Google Scholar 

  26. Järvholm K, Janson A, Peltonen M, Neovius M, Gronowitz E, Engström M, et al. Metabolic and bariatric surgery versus intensive non-surgical treatment for adolescents with severe obesity (AMOS2): a multicentre, randomised, controlled trial in Sweden. Lancet Child Adolesc Health. 2023;7:249–60.

    Article  PubMed  Google Scholar 

  27. Misra M, Singhal V, Carmine B, Bose A, Kelsey MM, Stanford FC, et al. Bone outcomes following sleeve gastrectomy in adolescents and young adults with obesity versus non-surgical controls. Bone. 2020;134:115290.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Mitchell DM, Singhal V, Animashaun A, Bose A, Carmine B, Stanford FC, et al. Skeletal effects of sleeve gastrectomy in adolescents and young adults: a 2-year longitudinal study. J Clin Endocrinol Metab. 2023;108:847–57.

    Article  PubMed  Google Scholar 

  29. Nimmala S, Kaur S, Singhal V, Mitchell DM, Stanford FC, Bouxsein ML, et al. Changes in sex steroids and enteric peptides after sleeve gastrectomy in youth in relation to changes in bone parameters. J Clin Endocrinol Metab. 2022;107:e3747–e58.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Xanthakos SA, Khoury JC, Inge TH, Jenkins TM, Modi AC, Michalsky MP, et al. Nutritional risks in adolescents after bariatric surgery. Clin Gastroenterol Hepatol. 2020;18:1070–81.e5.

    Article  CAS  PubMed  Google Scholar 

  31. Inge TH, Courcoulas AP, Jenkins TM, Michalsky MP, Helmrath MA, Brandt ML, et al. Weight loss and health status 3 years after bariatric surgery in adolescents. N Engl J Med. 2016;374:113–23.

    Article  CAS  PubMed  Google Scholar 

  32. Craig CL, Marshall AL, Sjostrom M, Bauman AE, Booth ML, Ainsworth BE, et al. International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc. 2003;35:1381–95.

    Article  PubMed  Google Scholar 

  33. Wadhwa R, Kumar M, Talegaonkar S, Vohora D. Serotonin reuptake inhibitors and bone health: A review of clinical studies and plausible mechanisms. Osteoporos Sarcopenia. 2017;3:75–81.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Lespessailles E, Toumi H. Proton Pump Inhibitors and Bone Health: An Update Narrative Review. Int J Mol Sci. 2022;23:10733.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Monadi M, Javadian Y, Cheraghi M, Heidari B, Amiri M. Impact of treatment with inhaled corticosteroids on bone mineral density of patients with asthma: related with age. Osteoporos Int. 2015;26:2013–8.

    Article  CAS  PubMed  Google Scholar 

  36. Tian Z, Fan X-T, Li S-Z, Zhai T, Dong J. Changes in bone metabolism after sleeve gastrectomy versus gastric bypass: a meta-analysis. Obes Surg. 2020;30:77–86.

    Article  PubMed  Google Scholar 

  37. Chaves Pereira de Holanda N, de Lima Carlos I, Chaves de Holanda Limeira C, Cesarino de Sousa D, Serra de Lima Junior FA, Telis de Vilela Araújo A, et al. Fracture risk after bariatric surgery: a systematic literature review and meta-analysis. Endocr Pract. 2022;28:58–69.

    Article  PubMed  Google Scholar 

  38. Saad RK, Ghezzawi M, Habli D, Alami RS, Chakhtoura M. Fracture risk following bariatric surgery: a systematic review and meta-analysis. Osteoporos Int. 2022;33:511–26.

    Article  CAS  PubMed  Google Scholar 

  39. Wren TA, Shepherd JA, Kalkwarf HJ, Zemel BS, Lappe JM, Oberfield S, et al. Racial disparity in fracture risk between white and nonwhite children in the United States. J Pediatr. 2012;161:1035–40.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Stattin K, Höijer J, Hållmarker U, Baron JA, Larsson SC, Wolk A, et al. Fracture risk across a wide range of physical activity levels, from sedentary individuals to elite athletes. Bone. 2021;153:116128.

    Article  CAS  PubMed  Google Scholar 

  41. Vandewalle S, Taes Y, Van Helvoirt M, Debode P, Herregods N, Ernst C, et al. Bone size and bone strength are increased in obese male adolescents. J Clin Endocrinol Metab. 2013;98:3019–28.

    Article  CAS  PubMed  Google Scholar 

  42. Leonard MB, Zemel BS, Wrotniak BH, Klieger SB, Shults J, Stallings VA, et al. Tibia and radius bone geometry and volumetric density in obese compared to non-obese adolescents. Bone. 2015;73:69–76.

    Article  PubMed  Google Scholar 

  43. Yu EW, Bouxsein ML, Roy AE, Baldwin C, Cange A, Neer RM, et al. Bone loss after bariatric surgery: discordant results between DXA and QCT bone density. J Bone Miner Res. 2014;29:542–50.

    Article  CAS  PubMed  Google Scholar 

  44. Hernández-Martínez A, Veras L, Boppre G, Soriano-Maldonado A, Oliveira J, Diniz-Sousa F, et al. Changes in volumetric bone mineral density and bone quality after Roux-en-Y gastric bypass: A meta-analysis with meta-regression. Obes Rev. 2022;23:e13479.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Huber FA, Singhal V, Tuli S, Becetti I, Lopez Lopez AP, Bouxsein ML, et al. Two-year Skeletal Effects of Sleeve Gastrectomy in Adolescents with Obesity Assessed with Quantitative CT and MR Spectroscopy. Radiology. 2023;307:e223256.

    Article  PubMed  Google Scholar 

  46. Evans EM, Mojtahedi MC, Kessinger RB, Misic MM. Simulated change in body fatness affects Hologic QDR 4500A whole body and central DXA bone measures. J Clin Densitom. 2006;9:315–22.

    Article  PubMed  Google Scholar 

  47. Jain RK, Vokes T. Visceral adipose tissue is negatively associated with bone mineral density in NHANES 2011-2018. J Endocr Soc. 2023;7:bvad008.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Russell M, Mendes N, Miller KK, Rosen CJ, Lee H, Klibanski A, et al. Visceral fat is a negative predictor of bone density measures in obese adolescent girls. J Clin Endocrinol Metab. 2010;95:1247–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Gállego Suárez C, Singer BH, Gebremariam A, Lee JM, Singer K. The relationship between adiposity and bone density in U.S. children and adolescents. PLoS One. 2017;12:e0181587.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Silva BC, Bilezikian JP. Parathyroid hormone: anabolic and catabolic actions on the skeleton. Curr Opin Pharmacol. 2015;22:41–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Pratt JSA, Browne A, Browne NT, Bruzoni M, Cohen M, Desai A, et al. ASMBS pediatric metabolic and bariatric surgery guidelines, 2018. Surg Obes Relat Dis. 2018;14:882–901.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors gratefully acknowledge the commitment of the participants in the Teen-LABS study and study personnel.

Funding

Funding

This study was conducted as a cooperative agreement and funded by the National Institute of Diabetes and Digestive and Kidney Diseases (U01 DK072493, UM1 DK072493 and UM1 DK095710). The research was also supported in part by the National Center for Advancing Translational Sciences of the National Institutes of Health (Award Number UL1 TR001425). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Author information

Authors and Affiliations

Authors

Contributions

Halley Wasserman, MD, MS was involved in the study design, review of the DXA and pQCT scans, interpretation of the results, drafting and revising this manuscript and approval of the submitted manuscript. Todd Jenkins was responsible for the statistical analysis and creation of the tables and figures. He helped obtain funding for this work. He was involved in revising this manuscript and approval of the submitted manuscript. Thomas Inge was involved in obtaining funding for this work, study design, interpretation of results, revising this manuscript and approval of the submitted manuscript. Justin Ryder, PhD was involved in the study design, interpretation of results, revising this manuscript and approval of the submitted manuscript. Marc Michalsky, MD, MBA was involved in the data collection, interpretation of results, revising this manuscript and approval of the submitted manuscript. Stephanie Sisley, MD was involved in data collection, interpretation of results, revising this manuscript and approval of the submitted manuscript. Changchun Xie, PhD was involved in the interpretation of results, revising this manuscript and approval of the submitted manuscript. Heidi J. Kalkwarf, PhD was involved in the study design, review of DXA and pQCT scans, data analysis, interpretation of results, drafting and revising this manuscript and approval of the submitted manuscript.

Corresponding author

Correspondence to Halley Wasserman.

Ethics declarations

Competing interests

HW – Nothing to disclose. TJ – Nothing to disclose. TI – Consultant for Mediflix and receives author royalties from Wolters Kluwer for UpToDate chapter contribution. JR – Receives a donation of drug and placebo for a clinical trial from Boehringer Ingelheim. MM – Intuitive Surgical, Inc (educational honorarium), Intuitive Surgical, Inc (stock ownership – relationship terminated), Lilly USA, LLC (Pediatric Obesity Advisory Board ad hoc member). SS – Consultant for Rhythm Pharmaceuticals. CX – Nothing to disclose. HJK - Nothing to disclose.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wasserman, H., Jenkins, T., Inge, T. et al. Bone mineral density in young adults 5 to 11 years after adolescent metabolic and bariatric surgery for severe obesity compared to peers. Int J Obes 48, 575–583 (2024). https://doi.org/10.1038/s41366-023-01453-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41366-023-01453-8

Search

Quick links