Skip to main content

Advertisement

Log in

Alteration of Bone Mineral Density Differs Between Genders in Obese Subjects After Laparoscopic Sleeve Gastrectomy: Bone Morphogenetic Protein 4 May Count

  • Original Contributions
  • Published:
Obesity Surgery Aims and scope Submit manuscript

Abstract

Objective

Laparoscopic sleeve gastrectomy (LSG) has proven to be successful in weight reduction but with potential loss of bone mass. Previous studies indicated that bone morphogenetic protein 4 (BMP4) plays an important role in both bone formation and glucose–lipid metabolism. This study aimed to investigate the changes in bone mineral density (BMD), bone metabolic parameters, and serum BMP4 levels in obese Chinese subjects after LSG.

Methods

Seventy-one obese patients (34 males, age 31.70 ± 9.61 years and 37 females, age 32.80 ± 11.45 years) were enrolled. BMD (at the right hip, femoral neck, and lumbar spine 1–4 (L1–L4)) was measured by dual-energy X-ray absorptiometry, bone metabolic markers, and routine anthropometric/laboratory biochemical parameters at baseline, 3, 6, and 12 months after LSG (abbreviated as 3, 6, and 12 M post-LSG, respectively) were recorded. Serum BMP4 levels were measured by enzyme-linked immunosorbent assay.

Results

LSG led to dramatic weight loss with improved glucose–lipid metabolism in all patients. In females, BMD was significantly decreased at the right hip at all time points studied and at the femoral neck at 6 and 12 M post-LSG (P < 0.05 or P < 0.01). In males, BMD was not significantly changed (all P > 0.05). Intriguingly, serum BMP4 levels were reduced slightly at 3 M post-LSG (P = 0.463) and were significantly at 6 M post-LSG (from 75.51 ± 16.54 to 65.40 ± 10.51 pg/mL, P = 0.048) in females, but unchanged in males (all P > 0.05). Vitamin D and 25-hydroxy vitamin D were increased in males at 12 M post-LSG (all P < 0.05). Osteocalcin was increased in males at all time points studied and in females at 3 and 6 M post-LSG (all P < 0.05). Type I collagen was increased in males at 3 and 6 M post-LSG and in females at all the time points studied (all P < 0.05).

Conclusions

The effect of LSG on BMD differs between genders, decreasing significantly in females while remaining unchanged in males. Moreover, decreased BMP4 levels may partly account for the diminished BMD in obese Chinese female patients after LSG.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Mechanick JI, Kushner RF, Sugerman HJ, et al. American Association of Clinical Endocrinologists, The Obesity Society, and American Society for Metabolic & Bariatric Surgery medical guidelines for clinical practice for the perioperative nutritional, metabolic, and nonsurgical support of the bariatric surgery patient. Obesity. 2009;17 Suppl 1:S1–70. v

    PubMed  Google Scholar 

  2. Ricci C, Gaeta M, Rausa E, et al. Early impact of bariatric surgery on type II diabetes, hypertension, and hyperlipidemia: a systematic review, meta-analysis and meta-regression on 6,587 patients. Obes Surg. 2014;24:522–8.

    Article  PubMed  Google Scholar 

  3. Uebelhart B. Effects of bariatric surgery on bone. Joint Bone Spine: Revue Du Rhumatisme. 2016;83:271–5.

    Article  Google Scholar 

  4. Rodriguez-Carmona Y, Lopez-Alavez FJ, Gonzalez-Garay AG, et al. Bone mineral density after bariatric surgery. A systematic review. Int J Surg. 2014;12:976–82.

    Article  PubMed  Google Scholar 

  5. Ruiz-Tovar J, Oller I, Priego P, et al. Short- and mid-term changes in bone mineral density after laparoscopic sleeve gastrectomy. Obes Surg. 2013;23:861–6.

    Article  PubMed  Google Scholar 

  6. Campanha-Versiani L, Pereira DAG, Ribeiro-Samora GA, 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;27:2129–37.

    Article  PubMed  Google Scholar 

  7. Adamczyk P, Buzga M, Holeczy P, et al. Bone mineral density and body composition after laparoscopic sleeve gastrectomy in men: a short-term longitudinal study. Int J Surg. 2015;23:101–7.

    Article  PubMed  Google Scholar 

  8. Massague J, Chen YG. Controlling TGF-beta signaling. Genes Dev. 2000;14:627–44.

    PubMed  CAS  Google Scholar 

  9. Gustafson B, Hammarstedt A, Hedjazifar S, et al. Restricted adipogenesis in hypertrophic obesity: the role of WISP2, WNT, and BMP4. Diabetes. 2013;62:2997–3004.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Bowers RR, Kim JW, Otto TC, et al. Stable stem cell commitment to the adipocyte lineage by inhibition of DNA methylation: role of the BMP-4 gene. Proc Natl Acad Sci U S A. 2006;103:13022–7.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Gustafson B, Hammarstedt A, Hedjazifar S, et al. BMP4 and BMP antagonists regulate human white and beige adipogenesis. Diabetes. 2015;64:1670–81.

    Article  PubMed  CAS  Google Scholar 

  12. Modica S, Straub LG, Balaz M, et al. Bmp4 promotes a brown to white-like adipocyte shift. Cell Rep. 2016;16:2243–58.

    Article  PubMed  CAS  Google Scholar 

  13. Son JW, Kim MK, Park YM, et al. Association of serum bone morphogenetic protein 4 levels with obesity and metabolic syndrome in non-diabetic individuals. Endocr J. 2011;58:39–46.

    Article  PubMed  CAS  Google Scholar 

  14. Kim MK, Jang EH, Hong OK, et al. Changes in serum levels of bone morphogenic protein 4 and inflammatory cytokines after bariatric surgery in severely obese Korean patients with type 2 diabetes. Int J Endocrinol. 2013;2013:681205.

    PubMed  PubMed Central  Google Scholar 

  15. Verhave J. Weight loss and health status after bariatric surgery in adolescents. N Engl J Med. 2016;374:1989.

    PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  17. Epstein NE. Bariatric bypasses contribute to loss of bone mineral density but reduce axial back pain in morbidly obese patients considering spine surgery. Surg Neurol Int. 2017;8:13.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Gregory NS. The effects of bariatric surgery on bone metabolism. Endocrinol Metab Clin N Am. 2017;46:105–16.

    Article  Google Scholar 

  19. Kao CH, Chen CC, Wang SJ. Normal data for lumbar spine bone mineral content in healthy elderly Chinese: influences of sex, age, obesity and ethnicity. Nucl Med Commun. 1994;15:916–20.

    Article  PubMed  CAS  Google Scholar 

  20. Wang J, Yan D, Hou X, et al. Association of adiposity indices with bone density and bone turnover in the Chinese population. Osteoporos Int. 2017;28:2645–52.

    Article  PubMed  CAS  Google Scholar 

  21. Hsin MC, Huang CK, Tai CM, et al. Case-matched study of the differences in bone mineral density 1 year after 3 different bariatric procedures. Surg Obes Relat Dis. 2015;11:181–5.

    Article  PubMed  Google Scholar 

  22. Biagioni MFG, Mendes AL, Nogueira CR, et al. Bariatric Roux-En-Y gastric bypass surgery: adipocyte proteins involved in increased bone remodeling in humans. Obes Surg. 2017;27:1789–96.

    Article  PubMed  Google Scholar 

  23. Lee WT, Jiang J. The resurgence of the importance of vitamin D in bone health. Asia Pac J Clin Nutr. 2008;17(Suppl 1):138–42.

    PubMed  CAS  Google Scholar 

  24. Kuroyanagi G, Tokuda H, Yamamoto N, et al. Resveratrol amplifies BMP-4-stimulated osteoprotegerin synthesis via p38 MAP kinase in osteoblasts. Mol Med Rep. 2015;12:3849–54.

    Article  PubMed  CAS  Google Scholar 

  25. Christensen GL, Jacobsen ML, Wendt A, et al. Bone morphogenetic protein 4 inhibits insulin secretion from rodent beta cells through regulation of calbindin1 expression and reduced voltage-dependent calcium currents. Diabetologia. 2015;58:1282–90.

    Article  PubMed  CAS  Google Scholar 

  26. Hong OK, Yoo SJ, Son JW, et al. High glucose and palmitate increases bone morphogenic protein 4 expression in human endothelial cells. Korean J Physiol Pharmacol. 2016;20:169–75.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Chattopadhyay T, Singh RR, Gupta S, et al. Bone morphogenetic protein-7 (BMP-7) augments insulin sensitivity in mice with type II diabetes mellitus by potentiating PI3K/AKT pathway. Biofactors. 2017;43:195–209.

    Article  PubMed  CAS  Google Scholar 

  28. Macotela Y, Emanuelli B, Mori MA, et al. Intrinsic differences in adipocyte precursor cells from different white fat depots. Diabetes. 2012;61:1691–9.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Funding

This research was supported by National Natural Science Foundation of China (NSFC 81500650, 81700752).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shen Qu.

Ethics declarations

Competing Interests

The authors declare that they have no conflict of interest.

Additional information

Xingchun Wang and Liang Li are co-first authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, X., Li, L., Zhu, C. et al. Alteration of Bone Mineral Density Differs Between Genders in Obese Subjects After Laparoscopic Sleeve Gastrectomy: Bone Morphogenetic Protein 4 May Count. OBES SURG 28, 3221–3226 (2018). https://doi.org/10.1007/s11695-018-3298-5

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11695-018-3298-5

Keywords

Navigation