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Serum levels of bone resorption markers are decreased in patients with type 2 diabetes

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Abstract

Previous studies of bone turnover markers in diabetes are limited, and the results are conflicting. Our aim was to evaluate differences in bone turnover markers and i-PTH between T2DM and non-diabetes subjects. Cross-sectional study including 133 subjects (78 T2DM, 55 without diabetes). BMD were measured by dual X-ray absorptiometry. Bone turnover markers were determined in serum. Serum levels of bone resorption markers (CTX and TRAP5b) were lower in T2DM compared with non-diabetes subjects. There were no differences in bone formation markers. i-PTH serum levels were lower in T2DM: 38.35 ± 18.20 pg/ml versus 50.22 ± 18.99 pg/ml, P < 0.05. TRAP5b and CTX were positively correlated with i-PTH (CTX: r = 0.443, P < 0.001; TRAP5b: r = 0.180, P = 0.047). There was an inverse relationship between TRAP5b levels and diabetes duration (r = −0.269, P = 0.021). T2DM patients have lower levels of bone resorption markers, and i-PTH compared with subjects without diabetes. Lower levels of PTH may induce a low turnover state as reflected by lower levels of bone resorption markers, and this situation may influence the higher risk of fracture of T2DM.

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Abbreviations

BMD:

Bone mineral density

T2DM:

Type 2 diabetes mellitus

AGEs:

Advanced end-glycation products

OC:

Osteocalcin

SD:

Standard deviation

BAP:

Bone-specific alkaline phosphatase

BTM:

Bone turnover markers

References

  1. Janghorbani M, Van Dam RM, Willet WC, Hu FB (2007) Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am J Epidemiol 166:495–505

    Article  PubMed  Google Scholar 

  2. Majima T, Komatsu Y, Yamada T, Koike Y, Shigemoto M, Takagi C, Hatanaka I, Nakao K (2005) Decreased bone mineral density at the distal radius, but not al the lumbar spine or the femoral neck, in Japanese type 2 diabetic patients. Osteoporos Int 16:907–913

    Article  PubMed  CAS  Google Scholar 

  3. Bridges MJ, Moochala SH, Barbour J, Kelly CA (2005) Influence of diabetes on peripheral bone mineral density in men: a controlled study. Acta Diabetol 42:82–86

    Article  PubMed  CAS  Google Scholar 

  4. Dobnig H, Piswanger-Solkner JC, Roth M, Obermayer-Pietsch B, Tiran A, Strele A, Maier E, Maritschnegg P, Sieberer C, Fahrleitner-Pammer A (2006) Type 2 diabetes mellitus in nursing home patients: effects on bone turnover bone mass, and fracture risk. J Clin Endocrinol Metab 91:3355–3363

    Article  PubMed  CAS  Google Scholar 

  5. Schwartz AV, Sellmeyer DE, Ensrud KE, Cauley JA, Tabor HK, Schreiner PJ, Jamal SA, Black DM, Cummings SR (2001) Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab 86:32–38

    Article  PubMed  CAS  Google Scholar 

  6. Vestegaard P, Rejnmark L, Mosekilde L (2005) Relative fracture risk in patients with diabetes mellitus, and the impact of insulin and oral antidiabetic medication on relative fracture risk. Diabetolologia 48:1292–1299

    Article  Google Scholar 

  7. Yamamoto M, Yamaguchi T, Yamauchi M, Kaji H, Sugimoto T (2009) Diabetic patients have an increased risk of vertebral fractures independent of BMD or diabetic complications. J Bone Miner Res 24:702–709

    Article  PubMed  CAS  Google Scholar 

  8. Gerdhem P, Isaksson A, Akesson K, Obrant KJ (2005) Increased bone density and decreased bone turnover, but no evident alteration of fracture susceptibility in elderly women with diabetes mellitus. Osteoporos Int 16:1506–1512

    Article  PubMed  CAS  Google Scholar 

  9. Hernandez CJ, Tang SY, Baumbach BM, Hwu PB, Sakkee AN, van der Ham F, DeGroot J, Bank RA, Keaveny TM (2005) Trabecular microfracture and the influence of piridinum and non-enzymatic glycation-mediated collagen crosslinks. Bone 37:825–832

    Article  PubMed  CAS  Google Scholar 

  10. De Liefde II, van der Klift M, de Laet C, van Daele PL, Hofman A, Pols HA (2005) Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam study. Osteoporos Int 16:1713–1720

    Article  PubMed  Google Scholar 

  11. Vasilkova O, Mokhort T, Sharshakova T, Hayashida N, Takamura N (2011) Leptin is an independent determinant of bone mineral density in men with type 2 diabetes mellitus. Acta Diabetol Feb 16. [Epub ahead of print]

  12. Li YM, Schilling T, Benisch P, Zeck S, Meissner-Weigl J, Schneider D, Limbert C, Seufert J, Kassem M, Schütze N, Jakob F, Ebert R (2007) Effects of high glucose on mesenchymal stem cell proliferation and differentiation. Biochem Biophys Res Commun 363:209–215

    Article  PubMed  CAS  Google Scholar 

  13. Wittrant Y, Gorin Y, Woodruff K, Horn D, Abboud HE, Mohan S, Abboud-Werner S (2008) High d(+)glucose concentration inhibits RANKL-induced osteoclastogenesis. Bone 42:1122–1130

    Article  PubMed  CAS  Google Scholar 

  14. Rosato MT, Schneider SH, Shapses SA (1998) Bone turnover and insulin-like growth factor I levels increase after improved glycemic control in noninsulin-dependent diabetes mellitus. Calcif Tissue Int 63:107–111

    Article  PubMed  CAS  Google Scholar 

  15. Takizawa M, Suzuki K, Matsubayashi T, Kikuyama M, Suzuki H, Takahashi K, Katsuta H, Mitsuhashi J, Nishida S, Yamaguchi S, Yoshimoto K, Itagaki E, Ishida H (2008) Increased bone resorption may play a crucial role in the occurrence of osteopenia in patients with type 2 diabetes: possible involvement of accelerated polyol pathway in its pathogenesis. Diabetes Res Clin Pract 82:119–126

    Article  PubMed  CAS  Google Scholar 

  16. Oz SG, Guven GS, Kilicarslan A, Calik N, Beyazit Y, Sozen T (2006) Evaluation of bone metabolism and bone mass in patients with type-2 diabetes mellitus. J Natl Med Assoc 98:1598–1604

    PubMed  Google Scholar 

  17. Achemlal L, Tellal S, Rkiouak F, Nouijai A, Bezza A, Derouiche ELM, Ghafir D, El Maghraoui A (2005) Bone metabolism in male patients with type 2 diabetes. Clin Rheumatol 24:493–496

    Article  PubMed  Google Scholar 

  18. Suzuki K, Kurose T, Takizawa M, Maruyama M, Ushikawa K, Kikuyama M, Sugimoto C, Seino Y, Nagamatsu S, Ishida H (2005) Osteoclastic function is accelerated in male patients with type 2 diabetes mellitus: the preventive role of osteoclastogenesis inhibitory factor/osteoprotegerin (OCIF/OPG) on the decrease of bone mineral density. Diabetes Res Clin Pract 68:117–125

    Article  PubMed  CAS  Google Scholar 

  19. Finkelstein JS, Sowers M, Greendale GA, Lee ML, Neer RM, Cauley JA, Ettinger B (2002) Ethnic variation in bone turnover in pre- and early perimenopausal women: effects of anthropometric and lifestyle factors. J Clin Endocrinol Metab 87:3051–3056

    Article  PubMed  CAS  Google Scholar 

  20. Capoglu I, Ozkan A, Ozkan B, Umudum Z (2008) Bone turnover markers in patients with type 2 diabetes and their correlation with glycosylated haemoglobin levels. J Int Med Res 36:1392–1398

    PubMed  CAS  Google Scholar 

  21. Inaba M, Okuno S, Nagasue K, Otoshi T, Kurioka Y, Maekawa K, Kumeda Y, Imanishi Y, Ishimura E, Ohta T, Morii H, Kim M, Nishizawa Y (2001) Impaired secretion of parathyroid hormone is coherent to diabetic hemodialyzed patients. Am J Kidney Dis 38:S139–S142

    Article  PubMed  CAS  Google Scholar 

  22. Tsuchida T, Sato K, Miyañoshi N, Abe T, Kudo T, Tamura Y, Kasukawa Y, Suzuki K (2000) Histomorphometric evaluation of the recovering effect on human parathyroid hormone (1–34) on bone structure and turnover in streptozotocin-induced diabetic rats. Calcif Tissue Int 66:229–233

    Article  PubMed  CAS  Google Scholar 

  23. Pedrazzoni M, Ciotti G, Pioli G, Girasole G, Davoli L, Palummeri E, Passeri M (1989) Osteocalcin levels in diabetic subjects. Calcif Tissue Int 45:331–336

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Bone Metabolic Unit (RETICEF), Endocrinology Division, Hospital Universitario San Cecilio, Av. Dr. Oloriz 16, 18012, Granada, Spain

    Rebeca Reyes-García, Pedro Rozas-Moreno, Antonia García-Martín, Mariela Varsavsky, Maria Dolores Avilés-Perez & Manuel Muñoz-Torres

  2. Endocrinology Division, Hospital General de Ciudad Real, Ciudad Real, Spain

    Pedro Rozas-Moreno & Gema López-Gallardo

Authors
  1. Rebeca Reyes-García
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  2. Pedro Rozas-Moreno
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  3. Gema López-Gallardo
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  4. Antonia García-Martín
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  5. Mariela Varsavsky
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  6. Maria Dolores Avilés-Perez
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  7. Manuel Muñoz-Torres
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Correspondence to Manuel Muñoz-Torres.

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Reyes-García, R., Rozas-Moreno, P., López-Gallardo, G. et al. Serum levels of bone resorption markers are decreased in patients with type 2 diabetes. Acta Diabetol 50, 47–52 (2013). https://doi.org/10.1007/s00592-011-0347-0

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  • DOI: https://doi.org/10.1007/s00592-011-0347-0

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