Skip to main content

Advertisement

Log in

The Effect of Exercise for the Prevention of Bone Mass After Bariatric Surgery: a Systematic Review and Meta-analysis

  • Review
  • Published:
Obesity Surgery Aims and scope Submit manuscript

A Correction to this article was published on 25 January 2022

This article has been updated

Abstract

We aimed to assess if exercise applied after bariatric surgery (BS) improves bone mineral density (BMD) compared to usual care. Systematic search was conducted up to January 2021. Effect measures were determined using standardized mean difference (SMD) with 95% confidence interval (CI). Certainty evidence was assessed according to GRADE. Four clinical trials encompassing 340 patients were included. Exercise induced a positive BMD effect at total hip (SMD = 0.37 [95% CI 0.02, 0.71]; very low certainty evidence), femoral neck (SMD = 0.63 [95% CI 0.19, 1.06]; low certainty evidence), lumbar spine (SMD = 0.41 [95% CI 0.19, 0.62]; low certainty evidence), and 1/3 radius (SMD = 0.58 [95% CI 0.19, 0.97]; low certainty evidence). Exercise undertaken after BS seems to induce a positive effect on BMD.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price includes VAT (France)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Change history

References

  1. Puzziferri N, Roshek TB 3rd, Mayo HG, Gallagher R, Belle SH, Livingston EH. Long-term follow-up after bariatric surgery: a systematic review. JAMA. 2014;312(9):934–42. https://doi.org/10.1001/jama.2014.10706.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Gagnon C, Schafer AL. Bone health after bariatric surgery. JBMR Plus. 2018;2(3):121–33. https://doi.org/10.1002/jbm4.10048.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Schafer AL, Kazakia GJ, Vittinghoff E, Stewart L, Rogers SJ, Kim TY, et al. Effects of gastric bypass surgery on bone mass and microarchitecture occur early and particularly impact postmenopausal women. J Bone Miner Res. 2018;33(6):975–86. https://doi.org/10.1002/jbmr.3371.

    Article  PubMed  Google Scholar 

  4. Zhang Q, Dong J, Zhou D, Liu F. Comparative risk of fracture for bariatric procedures in patients with obesity: a systematic review and Bayesian network meta-analysis. Int J Surg. 2020;75:13–23. https://doi.org/10.1016/j.ijsu.2020.01.018.

    Article  PubMed  Google Scholar 

  5. Hansen S, Jørgensen NR, Hermann AP, Støving RK. Continuous decline in bone mineral density and deterioration of bone microarchitecture 7 years after Roux-en-Y gastric bypass surgery. Eur J Endocrinol. 2020;182(3):303–11. https://doi.org/10.1530/eje-19-0741.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. 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(11):4104–12. https://doi.org/10.1210/jc.2018-01496.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Raoof M, Näslund I, Rask E, Szabo E. Bone mineral density, parathyroid hormone, and vitamin D after gastric bypass surgery: a 10-year longitudinal follow-up. Obes Surg. 2020;30(12):4995–5000. https://doi.org/10.1007/s11695-020-04912-7.

    Article  PubMed  PubMed Central  Google Scholar 

  8. 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(5):546–57. https://doi.org/10.1111/joim.13020.

    Article  CAS  PubMed  Google Scholar 

  9. Harvey N, Dennison E, Cooper C. Osteoporosis: impact on health and economics. Nat Rev Rheumatol. 2010;6(2):99–105. https://doi.org/10.1038/nrrheum.2009.260.

    Article  PubMed  Google Scholar 

  10. 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(9):2279–89. https://doi.org/10.1007/s11695-017-2666-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Ramos A, Kow L, Brown W, Welbourn R, Dixon J, Kinsman R, et al. Fifth IFSO global registry report—2019. Obes Surg. 2019;29(3):782–95.

    Article  PubMed  Google Scholar 

  12. Paccou J, Caiazzo R, Lespessailles E, Cortet B. Bariatric surgery and osteoporosis. Calcif Tissue Int. 2021. https://doi.org/10.1007/s00223-020-00798-w.

    Article  PubMed  Google Scholar 

  13. Mechanick JI, Apovian C, Brethauer S, Timothy Garvey W, Joffe AM, Kim J, et al. Clinical practice guidelines for the perioperative nutrition, metabolic, and nonsurgical support of patients undergoing bariatric procedures—2019 update: cosponsored by American Association of Clinical Endocrinologists/American College of Endocrinology, The Obesity Society, American Society for Metabolic and Bariatric Surgery, Obesity Medicine Association, and American Society of Anesthesiologists. Obesity (Silver Spring). 2020;28(4):O1-o58. https://doi.org/10.1002/oby.22719.

    Article  Google Scholar 

  14. Liu Y, Côté MM, Cheney MC, Lindeman KG, Rushin CC, Hutter MM, et al. Zoledronic acid for prevention of bone loss in patients receiving bariatric surgery. Bone Rep. 2021;14:100760. https://doi.org/10.1016/j.bonr.2021.100760.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Beavers KM, Beavers DP, Fernandez AZ, Greene KA, Swafford AA, Weaver AA, et al. Risedronate use to attenuate bone loss following sleeve gastrectomy: results from a pilot randomized controlled trial. Clin Obes. 2021;11(6):e12487. https://doi.org/10.1111/cob.12487.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Schafer AL. Vitamin D and intestinal calcium transport after bariatric surgery. J Steroid Biochem Mol Biol. 2017;173:202–10. https://doi.org/10.1016/j.jsbmb.2016.12.012.

    Article  CAS  PubMed  Google Scholar 

  17. Carlin AM, Rao DS, Yager KM, Parikh NJ, Kapke A. Treatment of vitamin D depletion after Roux-en-Y gastric bypass: a randomized prospective clinical trial. Surg Obes Relat Dis. 2009;5(4):444–9. https://doi.org/10.1016/j.soard.2008.08.004.

    Article  PubMed  Google Scholar 

  18. Sugiyama T, Kim YT, Oda H. Letter to the editor: skeletal fragility following bariatric surgery: a mechanistic insight. J Clin Endocrinol Metab. 2016;101(5):L66–7. https://doi.org/10.1210/jc.2016-1652.

    Article  PubMed  Google Scholar 

  19. Guadalupe-Grau A, Fuentes T, Guerra B, Calbet JA. Exercise and bone mass in adults. Sports Med. 2009;39(6):439–68. https://doi.org/10.2165/00007256-200939060-00002.

    Article  PubMed  Google Scholar 

  20. Villareal DT, Chode S, Parimi N, Sinacore DR, Hilton T, Armamento-Villareal R, et al. Weight loss, exercise, or both and physical function in obese older adults. N Engl J Med. 2011;364(13):1218–29. https://doi.org/10.1056/NEJMoa1008234.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Murai IH, Roschel H, Dantas WS, Gil S, Merege-Filho C, de Cleva R, et al. Exercise mitigates bone loss in women with severe obesity after Roux-en-Y gastric bypass: a randomized controlled trial. J Clin Endocrinol Metab. 2019;104(10):4639–50. https://doi.org/10.1210/jc.2019-00074.

    Article  PubMed  Google Scholar 

  22. Diniz-Sousa F, Veras L, Boppre G, Sa-Couto P, Devezas V, Santos-Sousa H, et al. The effect of an exercise intervention program on bone health after bariatric surgery: a randomized controlled trial. J Bone Miner Res. 2021;36(3):489–99. https://doi.org/10.1002/jbmr.4213.

    Article  CAS  PubMed  Google Scholar 

  23. Page MJ, Moher D, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. PRISMA 2020 explanation and elaboration: updated guidance and exemplars for reporting systematic reviews. BMJ. 2021;372:n160. https://doi.org/10.1136/bmj.n160.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Gomez-Bruton A, Montero-Marín J, González-Agüero A, Gómez-Cabello A, García-Campayo J, Moreno LA, et al. Swimming and peak bone mineral density: a systematic review and meta-analysis. J Sports Sci. 2018;36(4):365–77. https://doi.org/10.1080/02640414.2017.1307440.

    Article  PubMed  Google Scholar 

  25. Dimai HP. Use of dual-energy X-ray absorptiometry (DXA) for diagnosis and fracture risk assessment; WHO-criteria, T- and Z-score, and reference databases. Bone. 2017;104:39–43. https://doi.org/10.1016/j.bone.2016.12.016.

    Article  PubMed  Google Scholar 

  26. Kohrt WM, Bloomfield SA, Little KD, Nelson ME, Yingling VR. American College of Sports Medicine Position Stand: physical activity and bone health. Med Sci Sports Exerc. 2004;36(11):1985–96. https://doi.org/10.1249/01.mss.0000142662.21767.58.

    Article  PubMed  Google Scholar 

  27. 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. J Bone Miner Res. 2016;31(3):672–82. https://doi.org/10.1002/jbmr.2707.

    Article  CAS  PubMed  Google Scholar 

  28. Moeyaert M, Maggin D, Verkuilen J. Reliability, validity, and usability of data extraction programs for single-case research designs. Behav Modif. 2016;40(6):874–900. https://doi.org/10.1177/0145445516645763.

    Article  PubMed  Google Scholar 

  29. Wan X, Wang W, Liu J, Tong T. Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Med Res Methodol. 2014;14:135. https://doi.org/10.1186/1471-2288-14-135.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Higgins JPT, Tianjing L, Deeks JJ. Chapter 6. Choosing effect measures and computing estimates of effect. In: Higgins JPT, Thomas J, Chandler J, Cumpston M, Li T, Page MJ, Welch VA, editors. Cochrane handbook for systematic reviews of interventions. 2nd ed. Chichester: John Wiley & Sons; 2019. p. 143–76.

    Chapter  Google Scholar 

  31. da Costa BR, Nüesch E, Rutjes AW, Johnston BC, Reichenbach S, Trelle S, et al. Combining follow-up and change data is valid in meta-analyses of continuous outcomes: a meta-epidemiological study. J Clin Epidemiol. 2013;66(8):847–55. https://doi.org/10.1016/j.jclinepi.2013.03.009.

    Article  PubMed  Google Scholar 

  32. Sterne JAC, Savović J, Page MJ, Elbers RG, Blencowe NS, Boutron I, et al. RoB 2: a revised tool for assessing risk of bias in randomised trials. BMJ. 2019;366:l4898. https://doi.org/10.1136/bmj.l4898.

    Article  PubMed  Google Scholar 

  33. Sterne JA, Hernán MA, Reeves BC, Savović J, Berkman ND, Viswanathan M, et al. ROBINS-I: a tool for assessing risk of bias in non-randomised studies of interventions. BMJ. 2016;355:i4919. https://doi.org/10.1136/bmj.i4919.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Cohen J. Statistical power analysis for the behavioral sciences. 2nd ed. New York: Lawrence Erlbaum Associates; 1988. p. 20–7.

    Google Scholar 

  35. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21(11):1539–58. https://doi.org/10.1002/sim.1186.

    Article  PubMed  Google Scholar 

  36. Deeks JJ, Higgins JPT, Altman DG, et al. Chapter 10 Analysing data and undertaking meta-analyses. In: Higgins JPT, Thomas J, Chandler J, Cumpston M, Li T, Page MJ, Welch VA, editors., et al., Cochrane handbook for systematic reviews of interventions. 2nd ed. Chichester: John Wiley & Sons; 2019. p. 257–84.

    Google Scholar 

  37. Sterne JA, Sutton AJ, Ioannidis JP, Terrin N, Jones DR, Lau J, et al. Recommendations for examining and interpreting funnel plot asymmetry in meta-analyses of randomised controlled trials. BMJ. 2011;343:d4002. https://doi.org/10.1136/bmj.d4002.

    Article  PubMed  Google Scholar 

  38. Sedgwick P, Marston L. How to read a funnel plot in a meta-analysis. BMJ. 2015;351:h4718. https://doi.org/10.1136/bmj.h4718.

    Article  PubMed  Google Scholar 

  39. Schünemann H, Brożek J, Guyatt G, Oxman A (editors). GRADE handbook for grading quality of evidence and strength of recommendations. Updated October 2013. The GRADE Working Group, 2013. Available from: https://gdt.gradepro.org/app/handbook/handbook.html. Accessed 6 Dec 2021.

  40. Schünemann HJ, Higgins JPT, Vist GE, et al. Chapter 14. Completing ‘summary of findings’ tables and grading the certainty of the evidence. In: Higgins JPT, Thomas J, Chandler J, Cumpston M, Li T, Page MJ, Welch VA, editors., et al., Cochrane handbook for systematic reviews of interventions. 2nd ed. Chichester: John Wiley & Sons; 2019. p. 375–99.

    Chapter  Google Scholar 

  41. Schünemann HJ, Vist GE, Higgins JPT, et al. Chapter 15. Interpreting results and drawing conclusions. In: Higgins JPT, Thomas J, Chandler J, Cumpston M, Li T, Page MJ, Welch VA, editors., et al., Cochrane handbook for systematic reviews of interventions. 2nd ed. Chichester: John Wiley & Sons; 2019. p. 403–31.

    Chapter  Google Scholar 

  42. Campanha-Versiani L, Pereira DAG, Ribeiro-Samora GA, Ramos AV, de Sander Diniz MFH, De Marco LA, et al. The effect of a muscle weight-bearing and aerobic exercise program on the body composition, muscular strength, biochemical markers, and bone mass of obese patients who have undergone gastric bypass surgery. Obes Surg. 2017;27(8):2129–37. https://doi.org/10.1007/s11695-017-2618-5.

    Article  PubMed  Google Scholar 

  43. Rodriguez-Carmona Y, Lopez-Alavez FJ, Gonzalez-Garay AG, Solis-Galicia C, Melendez G, Serralde-Zuniga AE. Bone mineral density after bariatric surgery. A systematic review. Int J Surg. 2014;12(9):976–82. https://doi.org/10.1016/j.ijsu.2014.08.002.

    Article  PubMed  Google Scholar 

  44. Melton LJ 3rd, Achenbach SJ, Atkinson EJ, Therneau TM, Amin S. Long-term mortality following fractures at different skeletal sites: a population-based cohort study. Osteoporos Int. 2013;24(5):1689–96. https://doi.org/10.1007/s00198-012-2225-1.

    Article  PubMed  Google Scholar 

  45. Yu EW. Bone metabolism after bariatric surgery. J Bone Miner Res. 2014;29(7):1507–18. https://doi.org/10.1002/jbmr.2226.

    Article  PubMed  Google Scholar 

  46. Vainionpää A, Korpelainen R, Leppaluoto J, Jamsa T. Effects of high-impact exercise on bone mineral density: a randomized controlled trial in premenopausal women. Osteoporos Int. 2005;16(2):191–7. https://doi.org/10.1007/s00198-004-1659-5.

    Article  PubMed  Google Scholar 

  47. Kato T, Terashima T, Yamashita T, Hatanaka Y, Honda A, Umemura Y. Effect of low-repetition jump training on bone mineral density in young women. J Appl Physiol (1985). 2006;100(3):839–43. https://doi.org/10.1152/japplphysiol.00666.2005.

    Article  Google Scholar 

  48. Niu K, Ahola R, Guo H, Korpelainen R, Uchimaru J, Vainionpaa A, et al. Effect of office-based brief high-impact exercise on bone mineral density in healthy premenopausal women: the Sendai Bone Health Concept Study. J Bone Miner Metab. 2010;28(5):568–77. https://doi.org/10.1007/s00774-010-0163-6.

    Article  PubMed  Google Scholar 

  49. Allison SJ, Folland JP, Rennie WJ, Summers GD, Brooke-Wavell K. High impact exercise increased femoral neck bone mineral density in older men: a randomised unilateral intervention. Bone. 2013;53(2):321–8. https://doi.org/10.1016/j.bone.2012.12.045.

    Article  PubMed  Google Scholar 

  50. Pellikaan P, Giarmatzis G, Vander Sloten J, Verschueren S, Jonkers I. Ranking of osteogenic potential of physical exercises in postmenopausal women based on femoral neck strains. PLoS ONE. 2018;13(4):e0195463. https://doi.org/10.1371/journal.pone.0195463.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Daly RM, Dalla Via J, Duckham RL, Fraser SF, Helge EW. Exercise for the prevention of osteoporosis in postmenopausal women: an evidence-based guide to the optimal prescription. Braz J Phys Ther. 2019;23(2):170–80. https://doi.org/10.1016/j.bjpt.2018.11.011.

    Article  PubMed  Google Scholar 

  52. Martyn-St James M, Carroll S. Progressive high-intensity resistance training and bone mineral density changes among premenopausal women: evidence of discordant site-specific skeletal effects. Sports Med. 2006;36(8):683–704. https://doi.org/10.2165/00007256-200636080-00005.

    Article  PubMed  Google Scholar 

  53. Reid IR. Short-term and long-term effects of osteoporosis therapies. Nat Rev Endocrinol. 2015;11(7):418–28. https://doi.org/10.1038/nrendo.2015.71.

    Article  CAS  PubMed  Google Scholar 

  54. Black DM, Delmas PD, Eastell R, Reid IR, Boonen S, Cauley JA, et al. Once-yearly zoledronic acid for treatment of postmenopausal osteoporosis. N Engl J Med. 2007;356(18):1809–22. https://doi.org/10.1056/NEJMoa067312.

    Article  CAS  PubMed  Google Scholar 

  55. Axelsson KF, Werling M, Eliasson B, Szabo E, Naslund I, Wedel H, et al. Fracture risk after gastric bypass surgery: a retrospective cohort study. J Bone Miner Res. 2018;33(12):2122–31. https://doi.org/10.1002/jbmr.3553.

    Article  PubMed  Google Scholar 

  56. Adil MT, Jain V, Rashid F, Al-Taan O, Whitelaw D, Jambulingam P. Meta-analysis of the effect of bariatric surgery on physical function. Br J Surg. 2018;105(9):1107–18. https://doi.org/10.1002/bjs.10880.

    Article  CAS  PubMed  Google Scholar 

  57. Marshall S, Mackay H, Matthews C, Maimone IR, Isenring E. Does intensive multidisciplinary intervention for adults who elect bariatric surgery improve post-operative weight loss, co-morbidities, and quality of life? A systematic review and meta-analysis. Obes Rev. 2020;21(7):e13012. https://doi.org/10.1111/obr.13012.

    Article  PubMed  Google Scholar 

  58. Carretero-Ruiz A, Olvera-Porcel MDC, Cavero-Redondo I, Álvarez-Bueno C, Martínez-Vizcaíno V, Ferrer-Márquez M, et al. Effects of exercise training on weight loss in patients who have undergone bariatric surgery: a systematic review and meta-analysis of controlled trials. Obes Surg. 2019;29(10):3371–84. https://doi.org/10.1007/s11695-019-04096-9.

    Article  PubMed  Google Scholar 

  59. Zhang Y, Coello PA, Guyatt GH, Yepes-Nuñez JJ, Akl EA, Hazlewood G, et al. GRADE guidelines: 20. Assessing the certainty of evidence in the importance of outcomes or values and preferences-inconsistency, imprecision, and other domains. J Clin Epidemiol. 2019;111:83–93. https://doi.org/10.1016/j.jclinepi.2018.05.011.

    Article  PubMed  Google Scholar 

  60. Ioannidis JP, Evans SJ, Gøtzsche PC, O’Neill RT, Altman DG, Schulz K, et al. Better reporting of harms in randomized trials: an extension of the CONSORT statement. Ann Intern Med. 2004;141(10):781–8. https://doi.org/10.7326/0003-4819-141-10-200411160-00009.

    Article  PubMed  Google Scholar 

  61. Crisp AH, Verlengia R, Ravelli MN, Junior IR, de Oliveira MRM. Changes in physical activities and body composition after Roux-Y gastric bypass surgery. Obes Surg. 2018;28(6):1665–71. https://doi.org/10.1007/s11695-017-3074-y.

    Article  PubMed  Google Scholar 

  62. Groen VA, van de Graaf VA, Scholtes VA, Sprague S, van Wagensveld BA, Poolman RW. Effects of bariatric surgery for knee complaints in (morbidly) obese adult patients: a systematic review. Obes Rev. 2015;16(2):161–70. https://doi.org/10.1111/obr.12236.

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

Florêncio Diniz-Sousa was supported by the FCT (grant SFRH/BD/117622/2016), Giorjines Boppre was supported by the FCT (grant SFRH/BD/146976/2019), Lucas Veras was supported by the FCT (grant UI/BD/150673/2020), and Alba Hernández-Martínez was supported by the Plan Propio, Gerty Cori program from the University of Almería, Spain.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Florêncio Diniz-Sousa.

Ethics declarations

Ethical Approval

For this type of study, formal consent is not required.

Informed Consent

Informed consent does not apply.

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

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

Key Points

• Exercise applied after BS may improve BMD compared to usual medical care.

• Exercise effect size was small at TH and LS, and moderate at FN and 1/3 radius.

• Strength of evidence was low at FN, LS, and 1/3 radius and very low at TH.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 13 KB)

Supplementary file2 (XLSX 15 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Diniz-Sousa, F., Boppre, G., Veras, L. et al. The Effect of Exercise for the Prevention of Bone Mass After Bariatric Surgery: a Systematic Review and Meta-analysis. OBES SURG 32, 912–923 (2022). https://doi.org/10.1007/s11695-021-05873-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11695-021-05873-1

Keywords

Navigation