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Effects of Gastric Bypass and Sleeve Gastrectomy on Bone Mineral Density and Bone Turnover Markers: A Systematic Review and Meta-Analysis

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Abstract

Background

There is a growing interest in the post-operative bone-related effects of bariatric surgery. However, little is known about the comparative effects of the most commonly performed bariatric procedures, namely Roux-en-Y gastric bypass (RYGB) and sleeve gastrectomy (SG).

Objectives

To systematically assess the differences in areal bone mineral density (aBMD) and biochemical and hormonal markers of bone metabolism among patients undergoing RYGB and SG.

Methods

We conducted a systematic review and meta-analysis of studies aBMD at different sites, as well as bone-specific alkaline phosphatase (BALP), 25-OH-vitamin D, calcium and parathyroid hormone (PTH) after RYGB and SG.

Results

Fourteen studies were included (717 patients, 50.63% in the RYGB arm). Based on data collected at 1 year, 2 years and > 2 years, there were no significant differences in aBMD measurements at the total hip, lumbar spine, femoral neck, and the whole body with no statistical heterogeneity among different comparisons. Patients in the RYGB group showed significantly higher concentrations of BALP at 1 year (SMD = 0.52, 95%CI, 0.23–0.81, p = 0.0004) and PTH at > 2 years of follow-up (SMD = 0.68, 95%CI, 0.31–1.05, p = 0.0003) compared to the SG group.

Conclusion

There were no significant differences in aBMD measurements at the hip, lumbar spine, femoral neck, and the total body following RYGB and SG procedures. However, BALP and PTH concentrations were significantly higher after RYGB surgeries compared to SG. Attention should be paid to patients undergoing RYGB to prevent the expected skeletal fragility over time.

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References

  1. O’Brien PE, Hindle A, Brennan L, Skinner S, Burton P, Smith A et al (2019) Long-term outcomes after bariatric surgery: a systematic review and meta-analysis of weight loss at 10 or more years for all bariatric procedures and a single-centre review of 20-year outcomes after adjustable gastric banding. Obes Surg 29(1):3–14

    Article  Google Scholar 

  2. Maciejewski ML, Arterburn DE, Van Scoyoc L, Smith VA, Yancy WS, Weidenbacher HJ et al (2016) Bariatric surgery and long-term durability of weight loss. JAMA Surg 151(11):1046–1055

    Article  Google Scholar 

  3. International Federation for the Surgery of Obesity and Metabolic Disorders (IFSO) (2019) 5th IFSO Global Registry Report. United Kingdom.

  4. Ahlin S, Peltonen M, Sjöholm K, Anveden Å, Jacobson P, Andersson-Assarsson JC 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(5):546–557. https://doi.org/10.1111/joim.13020

    Article  CAS  PubMed  Google Scholar 

  5. Paccou J, Martignène N, Lespessailles E, Babykina E, Pattou F, Cortet B et al (2020) Gastric bypass but not sleeve gastrectomy increases risk of major osteoporotic fracture: French population-based cohort study. J Bone Miner Res 35(8):1415–1423

    Article  CAS  Google Scholar 

  6. Jaruvongvanich V, Vantanasiri K, Upala S, Ungprasert P (2019) Changes in bone mineral density and bone metabolism after sleeve gastrectomy: a systematic review and meta-analysis. Surg Obesity Related Dis 15(8):1252–1260

    Article  Google Scholar 

  7. Ko BJ, Myung SK, Cho KH, Park YG, Kim SG, Kim do H et al. (2016) Relationship between Bariatric surgery and bone mineral density: a meta-analysis. Obesity Surg 26(7):1414–1421. https://doi.org/10.1007/s11695-015-1928-8.

  8. Moher D, Liberati A, Tetzlaff J, Altman DG, Group P (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ (Clinical research ed). 339:b2535-b. https://doi.org/10.1136/bmj.b2535.

  9. Wells GA, Shea B, O’Connell D, Peterson J, Welch V, Losos M et al (2000) The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Oxford.

  10. Higgins JP, Altman DG, Sterne JA (2011) Assessing risk of bias in included studies. In: Higgins JPT, Green S (eds). Cochrane handbook for systematic reviews of interventions, Version 510: The Cochrane Collaboration, Available online at: http://www.handbook.cochrane.org.

  11. Egger M, Smith GD, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109):629–634

    Article  CAS  Google Scholar 

  12. Lu C, Li Z, Yang J, Feng L, Wang C, Shi Q (2020) Variations in Irisin, bone mineral density, bone mineral content, and body composition after Laparoscopic Bariatric procedures in obese adults. J Clin Densitometry Official J Int Soc Clin Densitometry 23(2):244–253. https://doi.org/10.1016/j.jocd.2019.05.002

    Article  Google Scholar 

  13. Luhrs AR, Davalos G, Lerebours R, Yoo J, Park C, Tabone L et al (2020) Determining changes in bone metabolism after bariatric surgery in postmenopausal women. Surg Endosc 34(4):1754–1760. https://doi.org/10.1007/s00464-019-06922-8

    Article  PubMed  Google Scholar 

  14. 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(9):2968–2975

    Article  Google Scholar 

  15. Ivaska KK, Huovinen V, Soinio M, Hannukainen JC, Saunavaara V, Salminen P et al (2017) Changes in bone metabolism after bariatric surgery by gastric bypass or sleeve gastrectomy. Bone 95:47–54

    Article  CAS  Google Scholar 

  16. Coupaye M, Breuil MC, Rivière P, Castel B, Bogard C, Dupré T et al (2013) Serum vitamin D increases with weight loss in obese subjects 6 months after Roux-en-Y gastric bypass. Obes Surg 23(4):486–493. https://doi.org/10.1007/s11695-012-0813-y

    Article  PubMed  Google Scholar 

  17. Bredella MA, Greenblatt LB, Eajazi A, Torriani M, Elaine WY (2017) Effects of Roux-en-Y gastric bypass and sleeve gastrectomy on bone mineral density and marrow adipose tissue. Bone 95:85–90

    Article  Google Scholar 

  18. Ieong K, Ardila-Gatas J, Yang J, Zhang X, Tsui ST, Spaniolas K et al (2020) Bone mineral density changes after bariatric surgery. Surgical Endoscopy, pp 1–8.

  19. Maghrabi AH, Wolski K, Abood B, Licata A, Pothier C, Bhatt DL et al (2015) Two-year outcomes on bone density and fracture incidence in patients with T2DM randomized to bariatric surgery versus intensive medical therapy. Obesity 23(12):2344–2348

    Article  Google Scholar 

  20. Carrasco F, Basfi-Fer K, Rojas P, Valencia A, Csendes A, Codoceo J et al (2014) Changes in bone mineral density after sleeve gastrectomy or gastric bypass: relationships with variations in vitamin D, ghrelin, and adiponectin levels. Obes Surg 24(6):877–884

    Article  Google Scholar 

  21. Carrasco F, Basfi-Fer K, Rojas P, Csendes A, Papapietro K, Codoceo J et al (2018) Calcium absorption may be affected after either sleeve gastrectomy or Roux-en-Y gastric bypass in premenopausal women: a 2-y prospective study. Am J Clin Nutr 108(1):24–32

    Article  Google Scholar 

  22. Hsin M-C, Huang C-K, Tai C-M, Yeh L-R, Kuo H-C, Garg A (2015) A case-matched study of the differences in bone mineral density 1 year after 3 different bariatric procedures. Surg Obesity Related Dis 11(1):181–185

    Article  Google Scholar 

  23. Tan HC, Tan MZ-W, Tham KW, Pasupathy S, Eng AKH, Ganguly S et al (2015) One year changes in QCT and DXA bone densities following bariatric surgery in a multiethnic Asian cohort. Osteoporosis Sarcopenia 1(2):115–120.

  24. Brzozowska MM, Tran T, Bliuc D, Jorgensen J, Talbot M, Fenton-Lee D et al (2021) Roux-en-Y gastric bypass and gastric sleeve surgery result in long term bone loss. Int J Obes 45(1):235–246

    Article  CAS  Google Scholar 

  25. Cadart O, Degrandi O, Barnetche T, Mehsen-Cetre N, Monsaingeon-Henry M, Pupier E et al (2020) Long-term effects of Roux-en-Y gastric bypass and sleeve gastrectomy on bone mineral density: a 4-year longitudinal study. Obes Surg 30(9):3317–3325

    Article  CAS  Google Scholar 

  26. Guerrero-Pérez F, Casajoana A, Gómez-Vaquero C, Virgili N, López-Urdiales R, Hernández-Montoliu L et al (2020) Changes in bone mineral density in patients with Type 2 Diabetes after different Bariatric surgery procedures and the role of gastrointestinal hormones. Obes Surg 30(1):180–188. https://doi.org/10.1007/s11695-019-04127-5

    Article  PubMed  Google Scholar 

  27. 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(2):501–511

    Article  Google Scholar 

  28. Muschitz C, Kocijan R, Marterer C, Nia AR, Muschitz GK, Resch H et al (2015) Sclerostin levels and changes in bone metabolism after bariatric surgery. J Clin Endocrinol Metab 100(3):891–901

    Article  CAS  Google Scholar 

  29. Nogués X, Goday A, Peña MJ, Benaiges D, de Ramón M, Crous X et al (2010) Bone mass loss after sleeve gastrectomy: a prospective comparative study with gastric bypass. Cirugia Espanola 88(2):103–109. https://doi.org/10.1016/j.ciresp.2010.04.008

    Article  PubMed  Google Scholar 

  30. Vilarrasa N, de Gordejuela AGR, Gómez-Vaquero C, Pujol J, Elio I, San José P et al (2013) Effect of bariatric surgery on bone mineral density: comparison of gastric bypass and sleeve gastrectomy. Obes Surg 23(12):2086–2091

    Article  Google Scholar 

  31. Fu R, Holmer HK (2015) AHRQ methods for effective health care. Change score or follow-up score? An empirical evaluation of the impact of choice of mean difference estimates. Rockville (MD): Agency for Healthcare Research and Quality (US).

  32. Mônaco-Ferreira DV, Leandro-Merhi VA, Aranha NC, Brandalise A, Brandalise NA (2018) Metabolic changes up to 10 years after gastric bypass. Obes Surg 28(6):1636–1642

    Article  Google Scholar 

  33. Blom-Høgestøl IK, Mala T, Kristinsson JA, Brunborg C, Gulseth HL, Eriksen EF (2020) Changes in bone quality after Roux-en-Y gastric bypass: a prospective cohort study in subjects with and without type 2 diabetes. Bone 130:115069.

  34. Krez AN, Stein EM (2020) The skeletal consequences of bariatric surgery. Curr Osteoporos Rep 18(3):262–272

    Article  Google Scholar 

  35. Yu EW, Bouxsein ML, Putman MS, Monis EL, Roy AE, Pratt JS et al (2015) Two-year changes in bone density after Roux-en-Y gastric bypass surgery. J Clin Endocrinol Metab 100(4):1452–1459. https://doi.org/10.1210/jc.2014-4341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Shanbhogue VV, Støving RK, Frederiksen KH, Hanson S, Brixen K, Gram J et al (2017) Bone structural changes after gastric bypass surgery evaluated by HR-pQCT: a two-year longitudinal study. Eur J Endocrinol 176(6):685–693. https://doi.org/10.1530/eje-17-0014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Demeter S, Leslie WD, Lix L, MacWilliam L, Finlayson GS, Reed M (2007) The effect of socioeconomic status on bone density testing in a public health-care system. Osteoporosis International: a Journal Established as Result of Cooperation Between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 18(2):153–158. https://doi.org/10.1007/s00198-006-0212-0

    Article  CAS  Google Scholar 

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Acknowledgements

This research would not have been possible without the exceptional support of our colleagues Mohamed Gamal Qassem, Usama Shaker Mohamed, Alaa Helal, Ahmed Abdelrahman Mahmoud, Feras Aljarad, Ahmed Nashaat, Ahmed Dorra, and Ahmed Abdalla. Their enthusiasm, knowledge and efforts have been an inspiration and kept our work on track, and the generosity and expertise of all of them have improved this study in innumerable ways.

Author information

Authors and Affiliations

  1. General Surgery Department, Kasralainy School of Medicine, Cairo University, Cairo, Egypt

    Mohamed AbdAlla Salman

  2. General Surgery Department, Sunderland Royal Hospital, Sunderland, Tyne and Wear, UK

    Mohammed Aradaib

  3. Internal Medicine Department, Kasr Alainy Faculty of Medicine, Cairo University, Cairo, Egypt

    Ahmed Salman

  4. General Surgery Department Department, National Hepatology and Tropical Medicine Research Institute, Cairo, Egypt

    Ahmed Elewa

  5. General Surgery Department, Great Western Hospital, NHS Foundation Trust, Swindon, UK

    Mohamed Tourky

  6. Gastroenterology and Hepatology Department, National Hepatology and Tropical Medicine Research Institute, Cairo, Egypt

    Hossam El-Din Shaaban

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  1. Mohamed AbdAlla Salman
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Correspondence to Mohamed AbdAlla Salman.

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Appendix 1

Appendix 1

The search process used in the PubMed database.

#1 "bariatric" OR "bariatric surgery" OR "gastric bypass" OR "bypass" OR "gastric sleeve" OR "sleeve gastrectomy".

#2 "bone" OR "mineral density" OR "bone mineral density" OR "fracture".

#3 "vitamin D" OR "vit D" OR "25(OH)D" "PTH" OR "calcium".

#4 #1 AND #2 OR #3.

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Salman, M.A., Aradaib, M., Salman, A. et al. Effects of Gastric Bypass and Sleeve Gastrectomy on Bone Mineral Density and Bone Turnover Markers: A Systematic Review and Meta-Analysis. World J Surg 46, 865–875 (2022). https://doi.org/10.1007/s00268-021-06429-1

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