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Changes in Bone Turnover Markers after Roux-en-Y Gastric Bypass Versus Sleeve Gastrectomy: a Systematic Review and Meta-Analysis

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Abstract

This systematic review and meta-analysis was performed to compare the alterations in bone turnover markers between SG and RYGB. A literature search was conducted in PubMed, Medline, Scopus, Web of Science, and the Cochrane Central Register of Controlled Trials (CENTRAL) databases to find the studies. There was significant less increment in osteocalcin [WMD =  − 5.98, 95% CI (− 9.30, − 2.47) P < 0.01] and parathyroid hormone (PTH) [WMD =  − 9.59, 95% CI (− 15.02, − 4.16) P < 0.01] in the SG group compared to the RYGB group. No significant differences were seen in change of C-terminal telopeptide of type I collagen (CTX), N-terminal propeptide of type I collagen (PINP), Ca, and 25(OH)-D between SG and RYGB groups. According to our meta-analysis, bone formation markers appear to have more increment following RYGB than SG. This observation is accompanied by a larger increase in PTH after RYGB patients compared to SG patients. PROSPERO: CRD42022308985.

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References

  1. Welbourn R, Hollyman M, Kinsman R, et al. Bariatric Surgery worldwide: baseline demographic description and one-year outcomes from the Fourth IFSO Global Registry Report 2018. Obes Surg. 2019;29(3):782–95.

    Article  PubMed  Google Scholar 

  2. O’Brien PE, Hindle A, Brennan L, et al. 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. 2019;29(1):3–14.

    Article  PubMed  Google Scholar 

  3. Wiggins T, Guidozzi N, Welbourn R, et al. Association of bariatric surgery with all-cause mortality and incidence of obesity-related disease at a population level: a systematic review and meta-analysis. PLoS Med. 2020;17(7):e1003206.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Pereira Chaves, de Holanda N, de Lima Carlos I, et al. Fracture Risk after bariatric surgery: a systematic literature review and meta-analysis. Endocr Pract : official journal of the American College of Endocrinology and the American Association of Clinical Endocrinologists. 2022;28(1):58–69.

    Article  Google Scholar 

  5. Jaruvongvanich V, Vantanasiri K, Upala S, et al. Changes in bone mineral density and bone metabolism after sleeve gastrectomy: a systematic review and meta-analysis. Surg Obes Relat Dis : official journal of the American Society for Bariatric Surgery. 2019;15(8):1252–60.

    Article  Google Scholar 

  6. Stein EM, Silverberg SJ. Bone loss after bariatric surgery: causes, consequences, and management. Lancet Diabetes Endocrinol. 2014;2(2):165–74.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Liu C, Wu D, Zhang JF, et al. Changes in bone metabolism in morbidly obese patients after bariatric surgery: a meta-analysis. Obes Surg. 2016;26(1):91–7.

    Article  PubMed  Google Scholar 

  8. Martin TJ, Seeman E. Bone remodelling: its local regulation and the emergence of bone fragility. Best Pract Res Clin Endocrinol Metab. 2008;22(5):701–22.

    Article  PubMed  Google Scholar 

  9. Vasikaran S, Cooper C, Eastell R, et al. International Osteoporosis Foundation and International Federation of Clinical Chemistry and Laboratory Medicine position on bone marker standards in osteoporosis. Clin Chem Lab Med. 2011;49(8):1271–4.

    Article  CAS  PubMed  Google Scholar 

  10. Tian Z, Fan XT, Li SZ, et al. Changes in bone metabolism after sleeve gastrectomy versus gastric bypass: a meta-analysis. Obes Surg. 2020;30(1):77–86.

    Article  PubMed  Google Scholar 

  11. Gu L, Lin K, Du N, et al. Differences in the effects of laparoscopic sleeve gastrectomy and laparoscopic Roux-en-Y gastric bypass on gut hormones: systematic and meta-analysis. Surg Obes Relat Dis : official journal of the American Society for Bariatric Surgery. 2021;17(2):444–55.

    Article  Google Scholar 

  12. Saad RK, Ghezzawi M, Habli D, et al. Fracture risk following bariatric surgery: a systematic review and meta-analysis. Osteoporo Int : a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA. 2022;33(3):511–26.

    Article  CAS  Google Scholar 

  13. Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ (Clinical research ed). 2021;372:n71.

    PubMed  Google Scholar 

  14. Shea BJ, Reeves BC, Wells G, et al. AMSTAR 2: a critical appraisal tool for systematic reviews that include randomised or non-randomised studies of healthcare interventions, or both. BMJ (Clinical research ed). 2017;358:j4008.

    Article  PubMed  Google Scholar 

  15. Paccou J, Thuillier D, Courtalin M, et al. A comparison of changes in bone turnover markers after gastric bypass and sleeve gastrectomy, and their association with markers of interest. Surg Obes Relat Dis : official journal of the American Society for Bariatric Surgery. 2022;18(3):373–83.

    Article  Google Scholar 

  16. Hofsø D, Hillestad TOW, Halvorsen E, et al. Bone mineral density and turnover after sleeve gastrectomy and gastric bypass: a randomized controlled trial (Oseberg). J Clin Endocrinol Metab. 2021;106(2):501–11.

    Article  PubMed  Google Scholar 

  17. Guerrero-Pérez F, Casajoana A, Gómez-Vaquero C, et al. Changes in bone mineral density in patients with type 2 diabetes after different bariatric surgery procedures and the role of gastrointestinal hormones. Obes Surg. 2020;30(1):180–8.

    Article  PubMed  Google Scholar 

  18. Crawford MR, Pham N, Khan L, et al. Increased bone turnover in type 2 diabetes patients randomized to bariatric surgery versus medical therapy at 5 years. Endocr Pract : official journal of the American College of Endocrinology and the American Association of Clinical Endocrinologists. 2018;24(3):256–64.

    Article  Google Scholar 

  19. Ivaska KK, Huovinen V, Soinio M, et al. Changes in bone metabolism after bariatric surgery by gastric bypass or sleeve gastrectomy. Bone. 2017;95:47–54.

    Article  CAS  PubMed  Google Scholar 

  20. Bredella MA, Greenblatt LB, Eajazi A. Effects of Roux-en-Y gastric bypass and sleeve gastrectomy on bone mineral density and marrow adipose tissue. Bone. 2017;95:85–90.

    Article  PubMed  Google Scholar 

  21. Lancha A, Moncada R, Valentí V, et al. Comparative effects of gastric bypass and sleeve gastrectomy on plasma osteopontin concentrations in humans. Surg Endosc. 2014;28(8):2412–20.

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  23. Morgan EF, Gerstenfeld LC. Chapter 2 - The bone organ system: form and function. In: Dempster DW, Cauley JA, Bouxsein ML, Cosman F, editors. Marcus and Feldman's Osteoporosis (Fifth Edition): Academic Press 2021; 15–35.

  24. Paccou J, Caiazzo R, Lespessailles E, et al. Bariatric surgery and osteoporosis. Calcif Tissue Int. 2022;110(5):576–91.

    Article  CAS  PubMed  Google Scholar 

  25. Mele C, Caputo M, Ferrero A, et al. Bone response to weight loss following bariatric surgery. Front Endocrinol. 2022;13:921353.

    Article  Google Scholar 

  26. Lee CG, Carr MC, Murdoch SJ, et al. Adipokines, inflammation, and visceral adiposity across the menopausal transition: a prospective study. J Clin Endocrinol Metab. 2009;94(4):1104–10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Holick MF. Vitamin D deficiency. N Engl J Med. 2007;357(3):266–81.

    Article  CAS  PubMed  Google Scholar 

  28. Marzullo P, Minocci A, Tagliaferri MA, et al. Investigations of thyroid hormones and antibodies in obesity: leptin levels are associated with thyroid autoimmunity independent of bioanthropometric, hormonal, and weight-related determinants. J Clin Endocrinol Metab. 2010;95(8):3965–72.

    Article  CAS  PubMed  Google Scholar 

  29. Ishii S, Cauley JA, Crandall CJ, et al. Diabetes and femoral neck strength: findings from the Hip Strength Across the Menopausal Transition study. J Clin Endocrinol Metab. 2012;97(1):190–7.

    Article  CAS  PubMed  Google Scholar 

  30. Barzin M, Ebadinejad A, Vahidi F, et al. The mediating role of bariatric surgery in the metabolic relationship between parathyroid hormone and 25-hydroxyvitamin D. Osteoporos Int. 2022;33(12):2585–94. https://doi.org/10.1007/s00198-022-06533-5.

    Article  CAS  PubMed  Google Scholar 

  31. Greenblatt MB, Tsai JN, Wein MN. Bone turnover markers in the diagnosis and monitoring of metabolic bone disease. Clin Chem. 2017;63(2):464–74.

    Article  CAS  PubMed  Google Scholar 

  32. Hindi SM, Vittinghoff E, Schafer AL, et al. Commercial Laboratory Reproducibility of Serum CTX in Clinical Practice. JBMR plus. 2019;3(10):e10225.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Yu EW, Wewalka M, Ding SA, et al. Effects of gastric bypass and gastric banding on bone remodeling in obese patients with type 2 diabetes. J Clin Endocrinol Metab. 2016;101(2):714–22.

    Article  CAS  PubMed  Google Scholar 

  34. Yu EW. Bone metabolism after bariatric surgery. J Bone Miner Res : the official journal of the American Society for Bone and Mineral Research. 2014;29(7):1507–18.

    Article  Google Scholar 

  35. Abegg K, Gehring N, Wagner CA, et al. Roux-en-Y gastric bypass surgery reduces bone mineral density and induces metabolic acidosis in rats. Am J Physiol Regul Integr Comp Physiol. 2013;305(9):R999-r1009.

    Article  CAS  PubMed  Google Scholar 

  36. Khundmiri SJ, Murray RD, Lederer E. PTH and vitamin D. Compr Physiol. 2016;6(2):561–601.

    Article  PubMed  Google Scholar 

  37. Salman MA, 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. 2022;46(4):865–75.

    Article  PubMed  Google Scholar 

  38. Khalid SI, Omotosho PA, Spagnoli A, et al. Association of bariatric surgery with risk of fracture in patients with severe obesity. JAMA Netw Open. 2020;3(6):e207419.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Gagnon C, Schafer AL. Bone health after bariatric surgery. JBMR plus. 2018;2(3):121–33.

    Article  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Obesity Research Center, Research Institute for Endocrine Sciences, Shahid Beheshti University of Medical Sciences, Tehran, 19395-476, Iran

    Amir Ebadinejad, Faranak Ghazy, Maryam Barzin, Majid Valizadeh, Behnaz Abiri & Farhad Hosseinpanah

  2. Isfahan Endocrine and Metabolism Research Center, Isfahan University of Medical Sciences, Isfahan, Iran

    Amirhossein Ramezani Ahmadi

  3. Tehran Obesity Treatment Center, Department of Surgery, Faculty of Medicine, Shahed University, Tehran, Iran

    Alireza Khalaj

Authors
  1. Amir Ebadinejad
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  2. Amirhossein Ramezani Ahmadi
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  3. Faranak Ghazy
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Correspondence to Behnaz Abiri or Farhad Hosseinpanah.

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Key Points

• According to the evidence, bone formation markers appear to have more increment following RYGB than SG.

• No significant differences were seen in change of C-terminal telopeptide of type I collagen (CTX), N-terminal propeptide of type I collagen (PINP), Ca and 25(OH)-D between SG and RYGB groups.

• Patients who undergo metabolic surgery are at risk for accelerated bone loss and may develop bone fragility if not effectively controlled.

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Ebadinejad, A., Ahmadi, A.R., Ghazy, F. et al. Changes in Bone Turnover Markers after Roux-en-Y Gastric Bypass Versus Sleeve Gastrectomy: a Systematic Review and Meta-Analysis. OBES SURG 33, 1259–1269 (2023). https://doi.org/10.1007/s11695-023-06503-8

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