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Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam Study.

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Abstract

The aim of this study was to determine the association between type-2 diabetes mellitus (DM), BMD and fractures in 6,655 men and women aged 55 years and over from the Rotterdam Study. We compared subjects with type-2 DM to subjects without DM. Additionally, subset analyses were performed, dividing subjects on the basis of the glucose tolerance test into already treated DM, newly diagnosed DM, impaired glucose tolerance (IGT) and normal glucose tolerance (NGT, reference). Femoral neck and lumbar spine BMD were measured using DEXA. Nonvertebral fracture ascertainment was performed using an automated record system involving GPs and local hospitals. Although subjects with DM had higher BMD, they had an increased nonvertebral fracture risk: hazard ratio (HR) 1.33 (1.00–1.77). In subset analysis, the increased fracture risk appeared restricted to treated DM subjects only: HR 1.69 (1.16–2.46). Subjects with IGT had a higher BMD, but contrary to treated DM, they had a lower fracture risk: HR 0.80 (0.63–1.00). In conclusion, subjects with type-2 DM and IGT both have a higher BMD. Whereas, subjects with IGT have a decreased fracture risk, subjects with DM (primarily those with already established and treated DM) had an increased fracture risk, probably due to long-term complications associated with DM.

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References

  1. Report of the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus (1997). Diabetes Care 20:1183–1197

    PubMed  Google Scholar 

  2. Yano H, Ohya K, Amagasa T (1994) Effects of insulin on in vitro bone formation in fetal rat parietal bone. Endocr J 41:293–300

    CAS  PubMed  Google Scholar 

  3. Mohan S, Richman C, Guo R, Amaar Y, Donahue LR, Wergedal J, Baylink DJ (2003) Insulin-like growth factor regulates peak bone mineral density in mice by both growth hormone-dependent and -independent mechanisms. Endocrinology 144:929–936

    Article  CAS  PubMed  Google Scholar 

  4. Kayath MJ, Tavares EF, Dib SA, Vieira JG (1998) Prospective bone mineral density evaluation in patients with insulin-dependent diabetes mellitus. J Diabetes Complications 12:133–139

    Article  CAS  PubMed  Google Scholar 

  5. Christensen JO, Svendsen OL (1999) Bone mineral in pre- and postmenopausal women with insulin-dependent and non-insulin-dependent diabetes mellitus. Osteoporos Int 10:307–311

    Article  CAS  PubMed  Google Scholar 

  6. Tuominen JT, Impivaara O, Puukka P, Ronnemaa T (1999) Bone mineral density in patients with type 1 and type 2 diabetes. Diabetes Care 22:1196–1200

    CAS  PubMed  Google Scholar 

  7. Bauer DC, Browner WS, Cauley JA, Orwoll ES, Scott JC, Black DM, Tao JL, Cummings SR (1993) Factors associated with appendicular bone mass in older women. The Study of Osteoporotic Fractures Research Group. Ann Intern Med 118:657–665

    CAS  PubMed  Google Scholar 

  8. van Daele PL, Stolk RP, Burger H, Algra D, Grobbee DE, Hofman A, Birkenhager JC, Pols HA (1995) Bone density in non-insulin-dependent diabetes mellitus. The Rotterdam Study. Ann Intern Med 122:409–414

    PubMed  Google Scholar 

  9. Lunt M, Masaryk P, Scheidt-Nave C, Nijs J, Poor G, Pols H, Falch JA, Hammermeister G, Reid DM, Benevolenskaya L, Weber K, Cannata J, O’Neill TW, Felsenberg D, Silman AJ, Reeve J (2001) The effects of lifestyle, dietary dairy intake and diabetes on bone density and vertebral deformity prevalence: the EVOS study. Osteoporos Int 12:688–698

    Article  CAS  PubMed  Google Scholar 

  10. 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

    CAS  PubMed  Google Scholar 

  11. Levin ME, Boisseau VC, Avioli LV (1976) Effects of diabetes mellitus on bone mass in juvenile and adult-onset diabetes. N Engl J Med 294:241–245

    CAS  PubMed  Google Scholar 

  12. Ishida H, Seino Y, Matsukura S, Ikeda M, Yawata M, Yamashita G, Ishizuka S, Imura H (1985) Diabetic osteopenia and circulating levels of vitamin D metabolites in type 2 (noninsulin-dependent) diabetes. Metabolism 34:797–801

    Article  CAS  PubMed  Google Scholar 

  13. Giacca A, Fassina A, Caviezel F, Cattaneo AG, Caldirola G, Pozza G (1988) Bone mineral density in diabetes mellitus. Bone 9:29–36

    Article  CAS  PubMed  Google Scholar 

  14. Weinstock RS, Goland RS, Shane E, Clemens TL, Lindsay R, Bilezikian JP (1989) Bone mineral density in women with type II diabetes mellitus. J Bone Miner Res 4:97–101

    CAS  PubMed  Google Scholar 

  15. Okuno Y, Nishizawa Y, Sekiya K, Hagiwara S, Miki T, Morii H (1991) Total and regional bone mineral content in patients with non-insulin dependent diabetes mellitus. J Nutr Sci Vitaminol (Tokyo) 37 [Suppl]:S43–49

  16. Wakasugi M, Wakao R, Tawata M, Gan N, Koizumi K, Onaya T (1993) Bone mineral density measured by dual energy X-ray absorptiometry in patients with non-insulin-dependent diabetes mellitus. Bone 14:29–33

    Article  CAS  PubMed  Google Scholar 

  17. Sosa M, Dominguez M, Navarro MC, Segarra MC, Hernandez D, de Pablos P, Betancor P (1996) Bone mineral metabolism is normal in non-insulin-dependent diabetes mellitus. J Diabetes Complications 10:201–205

    Article  CAS  PubMed  Google Scholar 

  18. Forsen L, Meyer HE, Midthjell K, Edna TH (1999) Diabetes mellitus and the incidence of hip fracture: results from the Nord-Trondelag Health Survey. Diabetologia 42:920–925

    Article  CAS  PubMed  Google Scholar 

  19. Ivers RQ, Cumming RG, Mitchell P, Peduto AJ (2001) Diabetes and risk of fracture: The Blue Mountains Eye Study. Diabetes Care 24:1198–1203

    CAS  PubMed  Google Scholar 

  20. Nicodemus KK, Folsom AR (2001) Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care 24:1192–1197

    CAS  PubMed  Google Scholar 

  21. Heath H 3rd, Melton LJ 3rd, Chu CP (1980) Diabetes mellitus and risk of skeletal fracture. N Engl J Med 303:567–570

    PubMed  Google Scholar 

  22. Melchior TM, Sorensen H, Torp-Pedersen C (1994) Hip and distal arm fracture rates in peri- and postmenopausal insulin-treated diabetic females. J Intern Med 236:203–208

    CAS  PubMed  Google Scholar 

  23. Hofman A, Grobbee DE, de Jong PT, van den Ouweland FA (1991) Determinants of disease and disability in the elderly: the Rotterdam Elderly Study. Eur J Epidemiol 7:403–422

    Article  CAS  PubMed  Google Scholar 

  24. Klaver CC, Wolfs RC, Vingerling JR, Hofman A, de Jong PT (1998) Age-specific prevalence and causes of blindness and visual impairment in an older population: the Rotterdam Study. Arch Ophthalmol 116:653–658

    CAS  PubMed  Google Scholar 

  25. Diabetes mellitus. Report of a WHO Study Group (1985) World Health Organ Tech Rep Ser 727:1–113

    Google Scholar 

  26. Prevention of diabetes mellitus. Report of a WHO Study Group (1994) World Health Organ Tech Rep Ser 844:1–100

    Google Scholar 

  27. Alberti KG, Zimmet PZ (1998) Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet Med 15:539–553

    Article  CAS  PubMed  Google Scholar 

  28. Burger H, de Laet CE, van Daele PL, Weel AE, Witteman JC, Hofman A, Pols HA (1998) Risk factors for increased bone loss in an elderly population: the Rotterdam Study. Am J Epidemiol 147:871–879

    CAS  PubMed  Google Scholar 

  29. Tripathy D, Carlsson M, Almgren P, Isomaa B, Taskinen MR, Tuomi T, Groop LC (2000) Insulin secretion and insulin sensitivity in relation to glucose tolerance: lessons from the Botnia Study. Diabetes 49:975–980

    CAS  PubMed  Google Scholar 

  30. 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 Physiol 265:E655–659

    CAS  PubMed  Google Scholar 

  31. Stolk RP, Van Daele PL, Pols HA, Burger H, Hofman A, Birkenhager JC, Lamberts SW, Grobbee DE (1996) Hyperinsulinemia and bone mineral density in an elderly population: The Rotterdam Study. Bone 18:545–549

    Article  CAS  PubMed  Google Scholar 

  32. Barrett-Connor E, Kritz-Silverstein D (1996) Does hyperinsulinemia preserve bone? Diabetes Care 19:1388–1392

    CAS  PubMed  Google Scholar 

  33. Schwartz AV, Hillier TA, Sellmeyer DE, Resnick HE, Gregg E, Ensrud KE, Schreiner PJ, Margolis KL, Cauley JA, Nevitt MC, Black DM, Cummings SR (2002) Older women with diabetes have a higher risk of falls: a prospective study. Diabetes Care 25:1749–1754

    PubMed  Google Scholar 

  34. Paul RG, Bailey AJ (1996) Glycation of collagen: the basis of its central role in the late complications of ageing and diabetes. Int J Biochem Cell Biol 28:1297–1310

    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. Wang X, Shen X, Li X, Agrawal CM (2002) Age-related changes in the collagen network and toughness of bone. Bone 31:1–7

    Article  PubMed  Google Scholar 

  37. Modan M, Halkin H, Karasik A, Lusky A (1984) Effectiveness of glycosylated hemoglobin, fasting plasma glucose, and a single post-load plasma glucose level in population screening for glucose intolerance. Am J Epidemiol 119:431–444

    CAS  PubMed  Google Scholar 

  38. Stolk RP, Orchard TJ, Grobbee DE (1995) Why use the oral glucose tolerance test? Diabetes Care 18:1045–1049

    CAS  PubMed  Google Scholar 

  39. Haeckel R, Wosniok W, Raber R, Janka HU (2003) Detecting type 2 diabetes by a single post-challenge blood sample. Clin Chem Lab Med 41:1251–1258

    Article  CAS  PubMed  Google Scholar 

  40. Coustan DR, Widness JA, Carpenter MW, Rotondo L, Pratt DC, Oh W (1986) Should the fifty-gram, one-hour plasma glucose screening test for gestational diabetes be administered in the fasting or fed state? Am J Obstet Gynecol 154:1031–1035

    CAS  PubMed  Google Scholar 

  41. Ruwaard D, Feskens EJ (1993) Diabetes Mellitus. In Ruwaard D, Kramers PGN (eds) (1993) Volksgezondheid Toekomst Verkenning: De Gezondheidstoestand van de Nederlandse bevolking in de periode 1950–2010. Sdu Uitgeverij Plantijnstraat, Den Haag, pp 303–308

    Google Scholar 

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Authors and Affiliations

  1. Department of Internal Medicine, Erasmus Medical Centre, PO Box 1738, 3000 DR, Rotterdam, The Netherlands

    I. I. de Liefde, M. van der Klift, C. E. D. H. de Laet, P. L. A. van Daele & H. A. P. Pols

  2. Department of Epidemiology and Biostatistics, Erasmus Medical Centre, Rotterdam, The Netherlands

    I. I. de Liefde, M. van der Klift, C. E. D. H. de Laet, A. Hofman & H. A. P. Pols

Authors
  1. I. I. de Liefde
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  2. M. van der Klift
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  3. C. E. D. H. de Laet
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  4. P. L. A. van Daele
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  5. A. Hofman
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  6. H. A. P. Pols
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Correspondence to M. van der Klift.

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de Liefde, I.I., van der Klift, M., de Laet, C.E.D.H. et al. Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam Study.. Osteoporos Int 16, 1713–1720 (2005). https://doi.org/10.1007/s00198-005-1909-1

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