Skip to main content
SpringerLink
Log in

Markers of Bone Metabolism in Obese Individuals Undergoing Laparoscopic Sleeve Gastrectomy

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

Abstract

Background

Besides its advantages, bariatric surgery implicates a risk of nutritional deficiencies, which might result in impaired bone metabolism. We assessed the effect of laparoscopic sleeve gastrectomy (LSG) on blood markers of bone metabolism in obese patients during a 3-year observation period.

Methods

In 39 obese patients (29 women, 10 men, mean BMI 51.8 ± 6.8 kg/m2) undergoing LSG, we measured blood concentrations of 25-hydroxyvitamin D (25(OH)D), calcium, parathyroid hormone (PTH), bone alkaline phosphatase (BAP), and N-telopeptides crosslinks (NTx) before LSG and up to 3 years postoperatively. Vitamin D and calcium supplementations were recorded.

Results

LSG caused an excess weight loss (EWL) of 54 ± 20 % after 3 years. Before surgery, we found decreased levels of 25(OH)D and calcium in 80 and 5 % of the subjects, respectively, while increased levels of PTH, BAP, and NTx were found in 39, 28, and 21 %, respectively. Mean levels of NTx and the prevalence of elevated levels of NTx increased within 2 years (p < 0.001 and p < 0.01). Neither mean blood concentrations of 25(OH)D, calcium, PTH, and BAP nor relative prevalence of deficiencies regarding these markers changed during the study period. The supplementation rates of calcium and vitamin D increased postoperatively.

Conclusions

Morbid obesity is associated with pronounced changes of markers of bone metabolism; LSG did neither aggravate nor ameliorate vitamin D metabolism within a 3-year time period, but led to increased bone resorption 2 years postoperatively. Routine supplementation of calcium and vitamin D is not likely sufficient to compensate the obesity-associated deficiencies in bone metabolism.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Sjöström L, Lindroos A, Peltonen M, Sullivan M, Wedel H, et al. Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. N Engl J Med. 2004;351(26):2683–93.

    Article  PubMed  Google Scholar 

  2. Peterli R, Borbély Y, Kern B, et al. Early results of the Swiss Multicentre Bypass or Sleeve Study (SM-BOSS): a prospective randomized trial comparing laparoscopic sleeve gastrectomy and Roux-en-Y gastric bypass. Ann Surg. 2013;258(5):690–4. discussion 695.

    Article  PubMed Central  PubMed  Google Scholar 

  3. Sjöström L. Review of the key results from the Swedish Obese Subjects (SOS) trial—a prospective controlled intervention study of bariatric surgery. J Intern Med. 2013;273(3):219–34. PMID: 23163728.

    Article  PubMed  Google Scholar 

  4. Sjöström L, Peltonen M, Jacobson P, et al. Bariatric surgery and long-term cardiovascular events. JAMA. 2012;307(1):56–65.

    Article  PubMed  Google Scholar 

  5. Saltzman E, Karl JP. Nutrient deficiencies after gastric bypass surgery. Annu Rev Nutr. 2013;33:183–203.

    Article  CAS  PubMed  Google Scholar 

  6. Skroubis G, Kouri N, Mead N, et al. Long-term results of a prospective comparison of Roux-en-Y gastric bypass versus a variant of biliopancreatic diversion in a non-superobese population (BMI 35–50 kg/m(2)). Obes Surg. 2014;24(2):197–204. PMID: 24105406.

    Article  PubMed  Google Scholar 

  7. Damms-Machado A, Friedrich A, Kramer KM, et al. Pre- and postoperative nutritional deficiencies in obese patients undergoing laparoscopic sleeve gastrectomy. Obes Surg. 2012;22(6):881–9. PMID: 22403000.

    Article  PubMed  Google Scholar 

  8. Friedrich AE, Damms-Machado A, Meile T, et al. Laparoscopic sleeve gastrectomy compared to a multidisciplinary weight loss program for obesity—effects on body composition and protein status. Obes Surg. 2013;23(12):1957–65. PMID: 23856991.

    Article  PubMed  Google Scholar 

  9. Goode LR, Brolin RE, Chowdhury HA, et al. Bone and gastric bypass surgery: effects of dietary calcium and vitamin D. Obes Res. 2004;12(1):40–7. PMID: 14742841.

    Article  CAS  PubMed  Google Scholar 

  10. Sinha N, Shieh A, Stein EM, et al. Increased PTH and 1.25(OH)(2)D levels associated with increased markers of bone turnover following bariatric surgery. Obesity (Silver Spring). 2011;19(12):2388–93.

    Article  CAS  Google Scholar 

  11. Vilarrasa N, San José P, García I, et al. Evaluation of bone mineral density loss in morbidly obese women after gastric bypass: 3-year follow-up. Obes Surg. 2011;21(4):465–72.

    Article  PubMed  Google Scholar 

  12. Ruiz-Tovar J, Oller I, Tomas A, et al. Mid-term effects of sleeve gastrectomy on calcium metabolism parameters, vitamin D and parathormone (PTH) in morbid obese women. Obes Surg. 2012;22(5):797–801.

    Article  PubMed  Google Scholar 

  13. Pluskiewicz W, Bužga M, Holéczy P, et al. Bone mineral changes in spine and proximal femur in individual obese women after laparoscopic sleeve gastrectomy: a short-term study. Obes Surg. 2012;22(7):1068–76. PMID: 22555865.

    Article  PubMed Central  PubMed  Google Scholar 

  14. 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(7):861–6. PMID: 23315187.

    Article  PubMed  Google Scholar 

  15. Carrasco F, Basfi-Fer K, Rojas P, et al. Changes in bone mineral density after sleeve gastrectomy or gastric bypass: relationships with variations in vitamin D, ghrelin, and adiponectin levels. Obes Surg. 2014;24(6):877–84. PMID: 24435517.

    Article  PubMed  Google Scholar 

  16. Vix M, Liu K, Diana M, et al. Impact of Roux-en-Y gastric bypass versus sleeve gastrectomy on vitamin D metabolism: short-term results from a prospective randomized clinical trial. Surg Endosc. 2014;28(3):821–6. PMID: 24196556.

    Article  PubMed  Google Scholar 

  17. Nogués X, Goday A, Peña MJ, et al. Pérdida de masa ósea tras gastrectomía tubular: estudio prospectivo comparativo con el bypass gástrico. Cir Esp. 2010;88(2):103–9.

    Article  PubMed  Google Scholar 

  18. Buffington W, Cowan S. Vitamin D deficiency in the morbidly obese. Obes Surg. 1993;3(4):421–4. PMID: 10757956.

    Article  PubMed  Google Scholar 

  19. Snijder MB, van Dam RM, Visser M, et al. Adiposity in relation to vitamin D status and parathyroid hormone levels: a population-based study in older men and women. J Clin Endocrinol Metab. 2005;90(7):4119–23.

    Article  CAS  PubMed  Google Scholar 

  20. Grethen E, McClintock R, Gupta CE, et al. Vitamin D and hyperparathyroidism in obesity. J Clin Endocrinol Metab. 2011;96(5):1320–6.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Hamoui N, Anthone G, Crookes PF. Calcium metabolism in the morbidly obese. Obes Surg. 2004;14(1):9–12.

    Article  PubMed  Google Scholar 

  22. Grethen E, Hill KM, Jones R, et al. Serum leptin, parathyroid hormone, 1,25-dihydroxyvitamin D, fibroblast growth factor 23, bone alkaline phosphatase, and sclerostin relationships in obesity. J Clin Endocrinol Metab. 2012;97(5):1655–62.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Kueper MA, Kramer KM, Kirschniak A, et al. Laparoscopic sleeve gastrectomy: standardized technique of a potential stand-alone bariatric procedure in morbidly obese patients. World J Surg. 2008;32(7):1462–5.

    Article  PubMed  Google Scholar 

  24. Runkel N, Colombo-Benkmann M, Hüttl TP, et al. Bariatric surgery. Dtsch Arztebl Int. 2011;108(20):341–6.

    PubMed Central  PubMed  Google Scholar 

  25. Pinheiro JC, Bates DM. Mixed-effects models in S and S-PLUS. New York: Springer; 2000.

    Book  Google Scholar 

  26. Chang S, Stoll CRT, Song J, et al. The effectiveness and risks of bariatric surgery: an updated systematic review and meta-analysis, 2003–2012. JAMA Surg. 2014;149(3):275–87.

    Article  PubMed Central  PubMed  Google Scholar 

  27. Saif T, Strain GW, Dakin G, et al. Evaluation of nutrient status after laparoscopic sleeve gastrectomy 1, 3, and 5 years after surgery. Surg Obes Relat Dis. 2012;8(5):542–7.

    Article  PubMed  Google Scholar 

  28. Hewitt S, Søvik TT, Aasheim ET, et al. Secondary hyperparathyroidism, vitamin D sufficiency, and serum calcium 5 years after gastric bypass and duodenal switch. Obes Surg. 2013;23(3):384–90.

    Article  PubMed  Google Scholar 

  29. Bruno C, Fulford AD, Potts JR, et al. Serum markers of bone turnover are increased at six and 18 months after Roux-en-Y bariatric surgery: correlation with the reduction in leptin. J Clin Endocrinol Metab. 2010;95(1):159–66.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  30. Braghetto I, Davanzo C, Korn O, et al. Scintigraphic evaluation of gastric emptying in obese patients submitted to sleeve gastrectomy compared to normal subjects. Obes Surg. 2009;19(11):1515–21.

    Article  PubMed  Google Scholar 

  31. Melissas J, Koukouraki S, Askoxylakis J, et al. Sleeve gastrectomy: a restrictive procedure? Obes Surg. 2007;17(1):57–62.

    Article  PubMed  Google Scholar 

  32. Blum M, Dolnikowski G, Seyoum E, et al. Vitamin D(3) in fat tissue. Endocrine. 2008;33(1):90–4.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Lin E, Armstrong-Moore D, Liang Z, et al. Contribution of adipose tissue to plasma 25-hydroxyvitamin D concentrations during weight loss following gastric bypass surgery. Obesity (Silver Spring). 2011;19(3):588–94.

    Article  CAS  Google Scholar 

  34. Ross PD, Knowlton W. Rapid bone loss is associated with increased levels of biochemical markers. J Bone Miner Res. 1998;13(2):297–302.

    Article  CAS  PubMed  Google Scholar 

  35. Wu X, Li H, Xie H, et al. Age-related bone turnover markers and osteoporotic risk in native Chinese women. BMC Endocr Disord. 2014;14(1):8.

    Article  PubMed Central  PubMed  Google Scholar 

  36. Hedlund LR, Gallagher JC. The effect of age and menopause on bone mineral density of the proximal femur. J Bone Miner Res. 1989;4(4):639–42.

    Article  CAS  PubMed  Google Scholar 

  37. Nordin BE, Gallagher JC, Aaron JE, et al. Post-menopausal osteopenia and osteoporosis. Front Horm Res. 1975;3:131–49.

    Article  CAS  PubMed  Google Scholar 

  38. Clemens JD, Herrick MV, Singer FR, et al. Evidence that serum NTx (collagen-type I N-telopeptides) can act as an immunochemical marker of bone resorption. Clin Chem. 1997;43(11):2058–63.

    CAS  PubMed  Google Scholar 

  39. Scariano JK, Glew RH, Bou-Serhal CE, et al. Serum levels of cross-linked N-telopeptides and aminoterminal propeptides of type I collagen indicate low bone mineral density in elderly women. Bone. 1998;23(5):471–7.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Ruth Volland from the Pediatric Clinical Trial Unit of the Department of Pediatrics and Adolescents Medicine at the University Hospital Cologne, Germany, for her help regarding the statistical analysis of the data. Furthermore, we thank Maria Seitzer from the Department of General, Visceral, and Transplant Surgery of the University Hospital of Tuebingen, Germany - she supported us in the laboratory measurements of NTx. This work was supported by the “Competence Network of Obesity,” research group “Obesity and the gastrointestinal tract”, coordinated by SCB and funded by the Federal Ministry of Education and Research, Germany (No. FKZ 01GI0843). The sponsor had no influence on the study design, analysis, and interpretation of data, as well as in the writing of the manuscript.

Conflict of Interest

Asja E. Schollenberger, Jaana M. Heinze, Tobias Meile, Andreas Peter, Alfred Königsrainer, and Stephan C. Bischoff declare that they have no conflict of interest.

Statement of Informed Consent

Informed consent was obtained from all individual participants included in the study.

Statement of Human Rights

All procedures performed in studies involving human participants were in accordance with the ethical standard of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Author information

Authors and Affiliations

  1. Department of Nutritional Medicine, University of Hohenheim, Fruwirthstraße 12, 70593, Stuttgart, Germany

    Asja E. Schollenberger, Jaana M. Heinze & Stephan C. Bischoff

  2. Department of General, Visceral, and Transplant Surgery, University Hospital of Tuebingen, Hoppe-Seyler-Straße 3, 72076, Tuebingen, Germany

    Asja E. Schollenberger, Tobias Meile & Alfred Königsrainer

  3. Department of Internal Medicine, University Hospital of Tuebingen, Otfried-Mueller-Straße 10, 72076, Tuebingen, Germany

    Andreas Peter

Authors
  1. Asja E. Schollenberger
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jaana M. Heinze
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tobias Meile
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Andreas Peter
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alfred Königsrainer
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Stephan C. Bischoff
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stephan C. Bischoff.

Additional information

The work has been performed at the Department of General, Visceral, and Transplant Surgery of the University Hospital of Tuebingen, Tuebingen, Germany.

Registration: at clinicaltrials.gov (No. NCT01344525)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schollenberger, A.E., Heinze, J.M., Meile, T. et al. Markers of Bone Metabolism in Obese Individuals Undergoing Laparoscopic Sleeve Gastrectomy. OBES SURG 25, 1439–1445 (2015). https://doi.org/10.1007/s11695-014-1509-2

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11695-014-1509-2

Keywords

Search

Navigation