Skip to main content
SpringerLink
Log in

Osteopenia in insulin-dependent diabetes mellitus; prevalence and aspects of pathophysiology

  • Original Article
  • Published:
Journal of Endocrinological Investigation Aims and scope Submit manuscript

Abstract

The objective was to evaluate the prevalence and severity of osteopenia in patients with uncomplicated insulin-dependent diabetes mellitus (IDDM) and to obtain more information on the pathophysiology of diabetic osteopenia. In 35 patients with uncomplicated IDDM (21 men and 14 women; age 37.6±9.9 yr; duration of disease 8.5±3.5 years) bone mineral density was measured by dual energy X-ray absorptiometry (DEXA). In addition, markers of bone formation [plasma insulin-like growth factor I (IGF-I), serum alkaline phosphatase (ALP), serum bone alkaline phosphatase (BAP) and serum osteocalcin] and bone resorption [urinary excretion of calcium and of the cross-linked N-telopeptide of type 1 collagen, both corrected for the excretion of creatinine] were measured in the diabetic patients and in 33 healthy controls, matched for sex, age, height, weight and body mass index (BMI). In 67% of the diabetic men and 57% of the diabetic women osteopenia of the femoral neck and/or the lumbar spine (T-value ≤−1 SD) was present. Fourteen percent of the male patients, but none of the female patients, met the criteria for osteoporosis (T-value ≤−2.5 SD). In the whole group of diabetic patients the mean plasma IGF-I level tended to be lower (p<0.10) as compared to that in the controls. In the diabetic patients with femoral neck osteopenia, the mean plasma IGF-I level was significantly lower (p<0.05) than in those without osteopenia at this site. There were no differences in the mean serum ALP, BAP and osteocalcin levels between the diabetic patients and the controls, nor between the diabetic patients with and without femoral neck osteopenia. Considering only the male diabetic patients, significantly lower mean plasma IGF-I (−26%), serum ALP (−24%) and serum osteocalcin (−38%) levels were present in the patients with femoral neck osteopenia than in those without osteopenia at this site, suggesting lowered bone formation. The bone resorption markers were similar in all (sub)groups of diabetic patients and not different between diabetic patients and controls. Bone mineral density (BMD) did not correlate with plasma levels of glycosylated hemoglobin (HbA1c). BMD values were not related to any of the bone resorption or formation markers, except for plasma IGF-I both in the femoral neck (r=+0.38, p=0.026) and the lumbar spine (r=+0.34, p=0.043). Our data demonstrate that at least in male patients with IDDM, osteopenia is the consequence of a lowered bone formation with a predominance of bone resorption over formation.

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. Piepkorn B., Kann P., Forst T., Andreas J., Pfützner A., Beyer J. Bone mineral density and bone metabolism in diabetes mellitus. Horm. Metab. Res. 1997, 29: 584–591.

    Article  CAS  PubMed  Google Scholar 

  2. Munoz-Torres M., Jódar E., Escobar-Jiménez F., López-Ibarra P., Luna J. Bone mineral density measured by dual x-ray absorptiometry in Spanish patients with insulin-dependent diabetes mellitus. Calcif. Tissue Int. 1996, 58: 316–319.

    Article  CAS  PubMed  Google Scholar 

  3. Forst T., Pfützner A., Kann P., Schehler B., Lobmann R., Schäfer H., Andreas J., Bockisch A., Beyer J. Peripheral osteopenia in adult patients with insulindependent diabetes mellitus. Diabet. Med. 1995, 12: 874–879.

    Article  CAS  PubMed  Google Scholar 

  4. Compston J., Smith E., Matthews C., Schofield P. Whole body composition and regional bone mass in women with insulin-dependent diabetes mellitus. Clin. Endocrinol. (Oxf.) 1994, 41: 289–293.

    Article  CAS  Google Scholar 

  5. Kayath M., Dib S., Vieire J. Prevalence and magnitude of osteopenia associated with insulin-dependent diabetes mellitus. J. Diabetes Complications 1994, 8: 97–104.

    Article  CAS  PubMed  Google Scholar 

  6. Buysschaert M., Cauwe F., Jamart J., Brichant C., De Coster P., Magnan A., Donckier J. Proximal femur density in type 1 diabetic patients. Diabet. Metab. 1992, 18: 32–37.

    CAS  Google Scholar 

  7. Goliat E., Ostrowski K., Marusza W., Lipinska A., Przedlacki J. Bone loss in insulin-dependent diabetes mellitus patients without diabetic nephropathy. Diabetologia 1997, 40 (Suppl. 1): A 579, abstract 2276.

    Google Scholar 

  8. Koeva L., Bohchelian H., Klisarova A., Pranchev L., Svrakova L. Bone changes in patients with insulin-dependent (type 1) diabetes mellitus. Diabetologia 1997, 40 (Suppl. 1): A 579, abstract 2277.

    Google Scholar 

  9. Gallacher S., Fenner J., Fisher B., Quin J., Fraser W., Logue F., Cowan R., Boyle I., MacCuish A. An evaluation of bone density and turnover in premenopausal women with type 1 Diabetes Mellitus. Diabet. Med. 1993, 10: 129–133.

    Article  CAS  PubMed  Google Scholar 

  10. Olmos J., Pérez-Castrillón J., Carcía M, Garrido J., Amado J., Gonzáles-Marcías J. Bone densitometry and biochemical bone remodeling markers in type 1 diabetes mellitus. Bone Miner. 1994, 26: 1–8.

    Article  CAS  PubMed  Google Scholar 

  11. Wientraub S., Eisenberg D., Tardiman R., Weissman S., Salama R. Is diabetic osteoporosis due to microangiopathy? Lancet 1980, ii: 983.

    Article  Google Scholar 

  12. Kelsey J., Browner W., Seely D., Nevitt M., Cummings S. Risk factors for fractures of the distal forearm and proximal humerus. Am. J. Epidemiol. 1992, 135: 477–489.

    CAS  PubMed  Google Scholar 

  13. Seeley D., Kelsey J., Jergas M., Nevitt M. Predictors of ankle and foot fractures in older women. J. Bone Miner. Res. 1996, 11: 1347–1355.

    Article  CAS  PubMed  Google Scholar 

  14. Van Hoof H., Swinkels L., Stevenhagen J., van den Bergh H., Ross H., Benraad Th. Advantages of paper chromatography as a preparative step in the assay of 1,25 dihydroxyvitamin D. J. Chromatogr. 1993, 621: 33–39.

    Article  PubMed  Google Scholar 

  15. De Leeuw I., Mulkens N., Vertommen J., Abs R. A histo-morphometric study on the trabecular bone of diabetic subjects. Diabetologia 1976, 12: 385–386.

    Google Scholar 

  16. Cohen H., Donnelly T., Fogelman I., Beastall G., Smith L., Gardner M., Fyffe J., Jenkins A., MacCuish A., Manderson W. Assessment of skeletal metabolism in diabetes. Proceedings on International Symposium on Osteoporosis, Jerusalem, Israel, 1981, p. 105.

    Google Scholar 

  17. Seino Y., Ishida H. Diabetic osteopenia: Pathophysiology and clinical aspects. Diabetes Metab. Rev. 1985, 1: 21–35.

    Google Scholar 

  18. Kream B., Smith M., Canalis E., Raisz L. Characterization of the effect of insulin on collagen synthesis in fetal rat bone. Endocrinology 1985, 1: 296–302.

    Article  Google Scholar 

  19. Auwerx J., Dequeker J., Bouillon R., Guesens P., Nijs J. Mineral metabolism and bone mass at peripheral and axial skeleton in Diabetes Mellitus. Diabetes 1988, 37: 8–12.

    Article  CAS  PubMed  Google Scholar 

  20. McNair P., Madsbad S., Christiansen C., Christensen M., Faber O., Binder C., Transbøl I. Bone loss in Diabetes: effects of metabolic state. Diabetologia 1979, 17: 283–286.

    Article  CAS  PubMed  Google Scholar 

  21. Nyomba B., Bouillon R., Bidingija M., Kandjingu K., De Moor P. Vitamin D metabolites and their binding protein in adult diabetic patients. Diabetes 1986, 35: 911-915.

    Article  CAS  PubMed  Google Scholar 

  22. Bouillon R., Bex M., Van Herck E., Laureys J., Dooms L., Lesaffre E., Ravussin E. Influence of age, sex, and insulin on osteoblast function: osteoblast dysfunction in diabetes mellitus. J. Clin. Endocrinol. Metab. 1995, 80: 1194–1202.

    CAS  PubMed  Google Scholar 

  23. Bell J., Thompson C., Brown A., Dandona P. Total alkaline phosphatase and quantitative isoenzyme analysis in diabetes mellitus. Ann. Clin. Biochem. 1988; 25 (Suppl.): 93S–94S.

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  25. Rico H., Hernandez E., Cabranes J., Gomez-Castresana F. Suggestion of a deficient osteoblastic function in diabetes mellitus: the possible cause of osteopenia in diabetics. Calcif. Tissue Int. 1989, 45: 71–73.

    Article  CAS  PubMed  Google Scholar 

  26. Guarneri M., Weber G., Gallia P., Chiumello G. Effect of insulin treatment on osteocalcin levels in diabetic children an adolescents. J. Endocrinol. Invest. 1993, 16: 505–509.

    CAS  PubMed  Google Scholar 

  27. Sayinalp S., Gedik O., Koray Z. Increasing serum osteocalcin after glycemic control in diabetic men. Calcif. Tissue Int. 1995, 57: 422–425.

    Article  CAS  PubMed  Google Scholar 

  28. Ljunghall S., Johansson A., Burmon P., Kampe O., Lindh E., Karlsson F. Low plasma levels of IGF-I in male patients with idiopathic osteoporosis. J. Int. Med. Res. 1992, 232: 59–64.

    Article  CAS  Google Scholar 

  29. Umpierrez G., Zlatev T., Spanheimer R. Correction of altered collagen metabolism in diabetic animals with insulin therapy. Matrix 1989, 9: 336–342.

    Article  CAS  PubMed  Google Scholar 

  30. Umpierrez G., Goldstein S., Phillips L., Spanheimer R. Nutritional and hormonal regulation of articular collagen production in diabetic animals. Diabetes 1989, 38: 758–763.

    Article  CAS  PubMed  Google Scholar 

  31. Amiel S., Sherwin R., Hintz R., Gertner J., Press C., Tamborlane W. Effect of diabetes and its control on insulin-like growth factors in the young subject with type 1 diabetes. Diabetes 1984, 33: 1175–1179.

    Article  CAS  PubMed  Google Scholar 

  32. Brenner R., Riemenschneider B., Blum W., Mörike M., Teller W., Pirsig W., Heinze E. Defective stimulation of proliferation and collagen biosynthesis of human bone cells by serum from diabetic patients. Acta Endocrinol. (Copenh.) 1992, 127: 509–514.

    CAS  Google Scholar 

  33. Bouillon R. Diabetic bone disease: low turnover osteoporosis related to decreased IGF-I production. Verh. K. Acad. Geneeskd. Belg. 1992, 54: 365–391.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Endocrinology, University Hospital Nijmegen, P.O. Box 9101, 6500 HB, Nijmegen, The Netherlands

    S. A. G. Kemink M.D., A. R. M. M. Hermus & A. G. H. Smals

  2. Department of Internal Medicine, University Hospital Nijmegen, Nijmegen, The Netherlands

    J. A. Lutterman

  3. Department of Chemical Endocrinology, University Hospital Nijmegen, Nijmegen, The Netherlands

    L. M. J. W. Swinkels

Authors
  1. S. A. G. Kemink M.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. R. M. M. Hermus
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. L. M. J. W. Swinkels
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. A. Lutterman
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. G. H. Smals
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Supported by a grant from the Diabetes Fonds Nederland

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kemink, S.A.G., Hermus, A.R.M.M., Swinkels, L.M.J.W. et al. Osteopenia in insulin-dependent diabetes mellitus; prevalence and aspects of pathophysiology. J Endocrinol Invest 23, 295–303 (2000). https://doi.org/10.1007/BF03343726

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF03343726

Key-words

Search

Navigation