Skip to main content

Advertisement

SpringerLink
Log in

Bone metabolism and the 10-year probability of hip fracture and a major osteoporotic fracture using the country-specific FRAX algorithm in men over 50 years of age with type 2 diabetes mellitus: a case–control study

  • Original Article
  • Published:
Clinical Rheumatology Aims and scope Submit manuscript

Abstract

The aim of the study was to evaluate the 10-year probability of hip fracture and a major osteoporotic fracture using the FRAX algorithm, vitamin D status, bone mineral density (BMD), and biochemical markers of bone turnover in men over 50 years of age with type 2 diabetes mellitus (T2DM). We estimated FRAX-predicted 10-year fracture probability, levels of 25-hydroxyvitamin D (25-OH-D), markers of bone turnover, and bone mineral density at the L1–L4 (lumbar spine (LS)) and femur neck (FN) in 68 men with T2DM and compared these with an age-matched group (n = 68). The mean (range) age of the T2DM group was 61.4 (51–78) years. The prevalence of hypovitaminosis D (25-OH-D <75 nmol/L) was 59 %. The mean (range) FRAX hip fracture and FRAX major osteoporotic fracture was 0.7 (0–2.8) and 3.2 (0–8.5) %, respectively. BMD at the FN (0.974 vs. 0.915 g/cm2, p = 0.008) and LS (1.221 vs. 1.068 g/cm2, p < 0.001) was significantly higher in the T2DM cohort as compared to the healthy age-matched males. 25-OH-vitamin D (67.7 vs.79.8 nmol/L, p < 0.001), crosslaps (0.19 vs. 0.24 μg/L, p = 0.004), and osteocalcin (13.3 vs. 15.7 μg/L, p = 0.004) were significantly lower in the T2DM group. There was no difference in FRAX-related fracture probability between the two groups. Acknowledging the limitations of our study size, we suggest that the increased BMD in T2DM and the noninclusion of T2DM as a secondary risk factor in the FRAX algorithm may be probable explanations for the discordance between literature-observed and FRAX-related fracture probabilities.

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

Similar content being viewed by others

References

  1. Schwartz AV (2003) Diabetes mellitus: does it affect bone? Calcif Tissue Int 73:515–519

    Article  CAS  PubMed  Google Scholar 

  2. Inzerillo AM, Epstein S (2004) Osteoporosis and diabetes mellitus. Rev Endocr Metab Disord 5:261–268

    Article  PubMed  Google Scholar 

  3. Leidig-Bruckner G, Ziegler R (2001) Diabetes mellitus—a risk for osteoporosis? Exp Clin Endocrinol Diabetes 109:S493–S514

    Article  CAS  PubMed  Google Scholar 

  4. de Liefde II, van der Klift M, de Laet CE et al (2005) Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam Study. Osteoporos Int 16(12):1713–20

    Article  PubMed  Google Scholar 

  5. Strotmeyer ES, Cauley JA, Schwartz AV et al (2005) Nontraumatic fracture risk with diabetes mellitus and impaired fasting glucose in older white and black adults: the health, aging, and body composition study. Arch Intern Med 165:1612–7

    Article  PubMed  Google Scholar 

  6. Schwartz AV, Vittinghoff E, Bauer DC et al (2011) Association of BMD and FRAX score with risk of fracture in older adults with type 2 diabetes. JAMA 305:2184–92

    Article  CAS  PubMed  Google Scholar 

  7. Janghorbani M, Van Dam RM, Willett 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 

  8. Lipscombe LL, Jamal SA, Booth GL, Hawker GA (2007) The risk of hip fractures in older individuals with diabetes: a population-based study. Diabetes Care 30:835–41

    Article  PubMed  Google Scholar 

  9. Einhorn TA, Boskey AL, Gundberg CM, Vigorita VJ, Devlin VJ, Beyer MM (1988) The mineral and mechanical properties of bone in chronic experimental diabetes. J Orthop Res 6:317–323

    Article  CAS  PubMed  Google Scholar 

  10. Akune T, Ogata N, Hoshi K et al (2002) Insulin receptor substrate-2 maintains predominance of anabolic function over catabolic function of osteoblasts. J Cell Biol 159:147–156

    Article  CAS  PubMed  Google Scholar 

  11. Ogata N, Chikazu D, Kubota N et al (2000) Insulin receptor substrate-1 in osteoblast is indispensable for maintaining bone turnover. J Clin Invest 105:935–943

    Article  CAS  PubMed  Google Scholar 

  12. Fulzele K, Riddle RC, DiGirolamo DJ et al (2010) Insulin receptor signaling in osteoblasts regulates postnatal bone acquisition and body composition. Cell 142:309–319

    Article  CAS  PubMed  Google Scholar 

  13. Thomas DM, Hards DK, Rogers SD, Ng KW, Best JD (1996) Insulin receptor expression in bone. J Bone Miner Res 11:1312–1320

    Article  CAS  PubMed  Google Scholar 

  14. Wergedal JE, Baylink DJ (1984) Characterization of cells isolated and cultured from human bone. Proc Soc Exp Biol Med 176:60–69

    Article  CAS  PubMed  Google Scholar 

  15. Canalis EM, Dietrich JW, Maina DM, Raisz LG (1977) Hormonal control of bone collagen synthesis in vitro. Effects of insulin and glucagon. Endocrinology 100:668–674

    Article  CAS  PubMed  Google Scholar 

  16. Canalis E (1983) Effect of hormones and growth factors on alkaline phosphatase activity and collagen synthesis in cultured rat calvariae. Metabolism 32:14–20

    Article  CAS  PubMed  Google Scholar 

  17. Hahn TJ, Westbrook SL, Sullivan TL, Goodman WG, Halstead LR (1988) Glucose transport in osteoblast-enriched bone explants: characterization and insulin regulation. J Bone Miner Res 3:359–365

    Article  CAS  PubMed  Google Scholar 

  18. Thomas DM, Udagawa N, Hards DK et al (1998) Insulin receptor expression in primary and cultured osteoclast-like cells. Bone 23:181–186

    Article  CAS  PubMed  Google Scholar 

  19. Bouillon R, Bex M, Van Herck E et al (1995) Influence of age, sex, and insulin on osteoblast function: osteoblast dysfunction in diabetes mellitus. J Clin Endocrinol Metab 80:1194–1202

    Article  CAS  PubMed  Google Scholar 

  20. Jehle PM, Jehle DR, Mohan S, Böhm BO (1998) Serum levels of insulin-like growth factor system components and relationship to bone metabolism in type 1 and type 2 diabetes mellitus patients. J Endocrinol 159:297–306

    Article  CAS  PubMed  Google Scholar 

  21. Moller DE, Flier JS (1997) Insulin resistance—mechanisms, syndromes, and implications. N Engl J Med 325:938–948

    Google Scholar 

  22. Reid IR, Evans MC, Cooper GJ, Ames RW, Stapleton J (1993) Circulating insulin levels are related to bone density in normal postmenopausal women. Am J Physio 265:E655–E659

    CAS  Google Scholar 

  23. Smythe HA (1987) Osteoarthritis, insulin and bone density. J Rheumatol 14:91–93

    PubMed  Google Scholar 

  24. Haffner SM, Bauer RL (1993) The association of obesity and glucose and insulin concentrations with bone density in premenopausal and postmenopausal women. Metabolism 42:735–738

    Article  CAS  PubMed  Google Scholar 

  25. Sambrook PN, Eisman JA, Pocock NA, Jenkins AB (1988) Serum insulin and bone density in normal subjects. J Rheumatol 15:1415–1417

    CAS  PubMed  Google Scholar 

  26. Plymate SR, Matej LA, Jones RE, Friedl KE (1988) Inhibition of sex hormone-binding globulin production in the human hepatoma (Hep G2) cell line by insulin and prolactin. J Clin Endocrinol Metab 67:460–464

    Article  CAS  PubMed  Google Scholar 

  27. Birkeland KI, Hanssen KF, Torjesen PA, Vaaler S (1993) Level of sex hormone-binding globulin is positively correlated with insulin sensitivity in men with type 2 diabetes. J Clin Endocrinol Metab 76:275–278

    Article  CAS  PubMed  Google Scholar 

  28. Preziosi P, Barrett-Connor E, Papoz L (1993) Interrelation between plasma sex hormone-binding globulin and plasma insulin in healthy adult women: the telecom study. J Clin Endocrinol Metab 76:283–287

    Article  CAS  PubMed  Google Scholar 

  29. Peiris AN, Stagner JI, Plymate SR, Vogel RL, Heck M, Samols E (1993) Relationship of insulin secretory pulses to sex hormone-binding globulin in normal men. J Clin Endocrinol Metab 76:279–282

    Article  CAS  PubMed  Google Scholar 

  30. Lindsay R (1991) Why do oestrogens prevent bone loss? Baillieres Clin Obstet Gynaecol 5:837–852

    Article  CAS  PubMed  Google Scholar 

  31. Conover CA, Ronk M, Lombana F, Powell DR (1996) Insulin-like growth factor-binding protein-1 expression in cultured human bone cells: regulation by insulin and glucocorticoid. Endocrinology 137:3295–3301

    Article  CAS  PubMed  Google Scholar 

  32. Suzuki K, Miyakoshi N, Tsuchida T, Kasukawa Y, Sato K, Itoi E (2003) Effects of combined treatment of insulin and human parathyroid hormone(1-34) on cancellous bone mass and structure in streptozotocin-induced diabetic rats. Bone 33:108–114

    Article  CAS  PubMed  Google Scholar 

  33. Williams JP, Blair HC, McDonald JM et al (1997) Regulation of osteoclastic bone resorption by glucose. Biochem Biophys Res Commun 235:646–651

    Article  CAS  PubMed  Google Scholar 

  34. Hofbauer LC, Brueck CC, Singh SK, Dobnig H (2007) Osteoporosis in patients with diabetes mellitus. J Bone Miner Res 22:1317–1328

    Article  CAS  PubMed  Google Scholar 

  35. Vashishth D, Gibson GJ, Khoury JI, Schaffler MB, Kimura J, Fyhrie DP (2001) Influence of nonenzymatic glycation on biomechanical properties of cortical bone. Bone 28:195–201

    Article  CAS  PubMed  Google Scholar 

  36. Saito M, Fujii K, Mori Y, Marumo K (2006) Role of collagen enzymatic and glycation induced cross-links as a determinant of bone quality in spontaneously diabetic WBN/Kob rats. Osteoporos Int 17:1514–1523

    Article  CAS  PubMed  Google Scholar 

  37. D’Erasmo E, Pisani D, Ragno A, Raejntroph N, Vecci E, Acca M (1999) Calcium homeostasis during oral glucose load in healthy women. Horm Metab Res 31:271–273

    Article  PubMed  Google Scholar 

  38. Okazaki R, Totsuka Y, Hamano K et al (1997) Metabolic improvement of poorly controlled noninsulin-dependent diabetes mellitus decreases bone turnover. J Clin Endocrinol Metab 82:2915–2920

    Article  CAS  PubMed  Google Scholar 

  39. Scragg R, Holdaway I, Singh V, Metcalf P, Baker J, Dryson E (1995) Serum 25-hydroxyvitamin D3 levels decreased in impaired glucose tolerance and diabetes mellitus. Diabetes Res Clin Pract 27:181–188

    Article  CAS  PubMed  Google Scholar 

  40. Baynes KC, Boucher BJ, Feskens EJ, Kromhout D (1997) Vitamin D, glucose tolerance and insulinaemia in elderly men. Diabetologia 40:344–347

    Article  CAS  PubMed  Google Scholar 

  41. http://www.shef.ac.uk/FRAX/. Accessed 08 Dec 2012

  42. Krakauer JC, McKenna MJ, Buderer NF et al (1995) Bone loss and bone turnover in diabetes. Diabetes 44:775–82

    Article  CAS  PubMed  Google Scholar 

  43. Dobnig H, Piswanger-Solkner JC, Roth M (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  CAS  PubMed  Google Scholar 

  44. Achemlal L, Tellal S, Rkiouak F (2005) Bone metabolism in male patients with type 2 diabetes. Clin Rheumatol 24:493–496

    Article  PubMed  Google Scholar 

  45. Fardellone P, Sebert JL, Bouraya M et al (1991) [Evaluation of the calcium content of diet by frequential self-questionnaire]. Rev Rhum Mal Osteoartic 58:99–103

    CAS  PubMed  Google Scholar 

  46. Dawson-Hughes B, Heaney RP, Holick MF, Lips P, Meunier PJ, Vieth R (2005) Estimates of optimal vitamin D status. Osteoporos Int 16:713–716

    Article  CAS  PubMed  Google Scholar 

  47. Bhattoa HP, Nagy E, More C et al (2013) Prevalence and seasonal variation of hypovitaminosis D and its relationship to bone metabolism in healthy Hungarian men over 50 years of age: the HunMen Study. Osteoporos Int 24:179–186

    Article  CAS  PubMed  Google Scholar 

  48. Schwartz AV, Hillier TA, Sellmeyer DE et al (2002) Older women with diabetes have a higher risk of falls: a prospective study. Diabetes Care 25:1749–1754

    Article  PubMed  Google Scholar 

  49. Petit MA, Paudel ML, Taylor BC (2010) Bone mass and strength in older men with type 2 diabetes: the osteoporotic fractures in men study. J Bone Miner Res 25:285–291

    Article  PubMed  Google Scholar 

  50. Giangregorio LM, Leslie WD, Lix LM et al (2012) FRAX underestimates fracture risk in patients with diabetes. J Bone Miner Res 27:301–308

    Article  PubMed  Google Scholar 

  51. Ford ES, Ajani UA, McGuire LC, Liu S (2005) Concentrations of serum vitamin D and the metabolic syndrome among U.S. adults. Diabetes Care 28:1228–30

    Article  CAS  PubMed  Google Scholar 

  52. Yaturu S, Davis J (2011) Prevalence of decreased vitamin D Levels is high among veterans with diabetes and/or CKD. ISRN Endocrinol 2011:109458

    PubMed  Google Scholar 

Download references

Acknowledgments

This work is supported by the OTKA 105073 research grant (H.P.B.) and the TÁMOP 4.2.1./B-09/1/KONV-2010-0007 project (H.P.B, E.K., A.B, G.P., P.A-S., M.K.), which is implemented through the New Hungary Development Plan, co-financed by the European Union and the European Social Fund.

Disclosures

None.

Author information

Authors and Affiliations

  1. Department of Laboratory Medicine, Medical and Health Science Center, University of Debrecen, Nagyerdei krt. 98, 4032, Debrecen, Hungary

    Harjit P. Bhattoa, Ugo Onyeka, Edit Kalina & Peter Antal-Szalmas

  2. Regional Osteoporosis Center, Department of Obstetrics and Gynecology, Medical and Health Science Center, University of Debrecen, Debrecen, Hungary

    Harjit P. Bhattoa & Adam Balogh

  3. 1st Department of Internal Medicine, Medical and Health Science Center, University of Debrecen, Debrecen, Hungary

    Gyorgy Paragh & Miklos Kaplar

Authors
  1. Harjit P. Bhattoa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ugo Onyeka
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Edit Kalina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Adam Balogh
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gyorgy Paragh
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Peter Antal-Szalmas
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Miklos Kaplar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Harjit P. Bhattoa.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bhattoa, H.P., Onyeka, U., Kalina, E. et al. Bone metabolism and the 10-year probability of hip fracture and a major osteoporotic fracture using the country-specific FRAX algorithm in men over 50 years of age with type 2 diabetes mellitus: a case–control study. Clin Rheumatol 32, 1161–1167 (2013). https://doi.org/10.1007/s10067-013-2254-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10067-013-2254-y

Keywords

Search

Navigation