Skip to main content
PMC home page
Journal of the National Medical Association logoLink to Journal of the National Medical Association
. 2006 Oct;98(10):1598–1604.

Evaluation of bone metabolism and bone mass in patients with type-2 diabetes mellitus.

S Gul Oz 1, Gulay Sain Guven 1, Alpaslan Kilicarslan 1, Nursel Calik 1, Yavuz Beyazit 1, Tumay Sozen 1
PMCID: PMC2569751  PMID: 17052049

Abstract

The objectives of this study were to determine whether type-2 diabetes was associated with a higher bone mineral density (BMD) in men and women and to evaluate the differences in mineral metabolism between diabetic and normal subjects by using biochemical bone turnover markers. In this study, 52 patients (37 females/15 males) aged 41-64 with type-2 diabetes mellitus and 48 nondiabetic control subjects (34 females/14 males) were evaluated. In men, BMD was significantly higher in diabetics at the forearm (p <0.05), whereas in women tended to be higher at the hip (p=0.002). Serum osteocalcin (p<0.0001), bone alkaline phosphatase (BAP) (p<0.05) and carboxyterminal telopeptide (CTx) (p<0.05) were higher in the control group than in diabetics. In men, serum osteocalcin (p<0.05) and CTx (p<0.005) and, in women, serum osteocalcin (p<0.0001) and BAP (p<0.05) were lower in diabetic subjects. In conclusion, our findings suggest that although bone formation is decreased in type-2 diabetes, diabetic patients are not susceptible to bone resorption. This low bone turnover can slow the rate of bone loss and cause a higher bone density than expected for their age.

Full text

PDF
1598

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Akin O., Göl K., Aktürk M., Erkaya S. Evaluation of bone turnover in postmenopausal patients with type 2 diabetes mellitus using biochemical markers and bone mineral density measurements. Gynecol Endocrinol. 2003 Feb;17(1):19–29. [PubMed] [Google Scholar]
  2. American Diabetes Association Standards of medical care in diabetes. Diabetes Care. 2005 Jan;28 (Suppl 1):S4–S36. [PubMed] [Google Scholar]
  3. Barrett-Connor E., Holbrook T. L. Sex differences in osteoporosis in older adults with non-insulin-dependent diabetes mellitus. JAMA. 1992 Dec 16;268(23):3333–3337. [PubMed] [Google Scholar]
  4. 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 Apr;80(4):1194–1202. doi: 10.1210/jcem.80.4.7714089. [DOI] [PubMed] [Google Scholar]
  5. Cakatay U., Telci A., Kayali R., Akçay T., Sivas A., Aral F. Changes in bone turnover on deoxypyridinoline levels in diabetic patients. Diabetes Res Clin Pract. 1998 May;40(2):75–79. doi: 10.1016/s0168-8227(98)00025-4. [DOI] [PubMed] [Google Scholar]
  6. Carnevale Vincenzo, Romagnoli Elisabetta, D'Erasmo Emilio. Skeletal involvement in patients with diabetes mellitus. Diabetes Metab Res Rev. 2004 May-Jun;20(3):196–204. doi: 10.1002/dmrr.449. [DOI] [PubMed] [Google Scholar]
  7. Christensen J. O., Svendsen O. L. Bone mineral in pre- and postmenopausal women with insulin-dependent and non-insulin-dependent diabetes mellitus. Osteoporos Int. 1999;10(4):307–311. doi: 10.1007/s001980050232. [DOI] [PubMed] [Google Scholar]
  8. Forsén L., Meyer H. E., Midthjell K., Edna T. H. Diabetes mellitus and the incidence of hip fracture: results from the Nord-Trøndelag Health Survey. Diabetologia. 1999 Aug;42(8):920–925. doi: 10.1007/s001250051248. [DOI] [PubMed] [Google Scholar]
  9. Gallacher S. J., Fenner J. A., Fisher B. M., Quin J. D., Fraser W. D., Logue F. C., Cowan R. A., Boyle I. T., MacCuish A. C. An evaluation of bone density and turnover in premenopausal women with type 1 diabetes mellitus. Diabet Med. 1993 Mar;10(2):129–133. doi: 10.1111/j.1464-5491.1993.tb00029.x. [DOI] [PubMed] [Google Scholar]
  10. Garay-Sevilla M. E., Nava L. E., Malacara J. M., Wróbel K., Wróbel K., Pérez U. Advanced glycosylation end products (AGEs), insulin-like growth factor-1 (IGF-1) and IGF-binding protein-3 (IGFBP-3) in patients with type 2 diabetes mellitus. Diabetes Metab Res Rev. 2000 Mar-Apr;16(2):106–113. doi: 10.3904/kjim.2007.22.3.186. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gregg Edward W., Mangione Carol M., Cauley Jane A., Thompson Theodore J., Schwartz Ann V., Ensrud Kristine E., Nevitt Michael C., Study of Osteoporotic Fractures Research Group Diabetes and incidence of functional disability in older women. Diabetes Care. 2002 Jan;25(1):61–67. doi: 10.2337/diacare.25.1.61. [DOI] [PubMed] [Google Scholar]
  12. Gregorio F., Cristallini S., Santeusanio F., Filipponi P., Fumelli P. Osteopenia associated with non-insulin-dependent diabetes mellitus: what are the causes? Diabetes Res Clin Pract. 1994 Feb;23(1):43–54. doi: 10.1016/0168-8227(94)90126-0. [DOI] [PubMed] [Google Scholar]
  13. Hanley D. A., Brown J. P., Tenenhouse A., Olszynski W. P., Ioannidis G., Berger C., Prior J. C., Pickard L., Murray T. M., Anastassiades T. Associations among disease conditions, bone mineral density, and prevalent vertebral deformities in men and women 50 years of age and older: cross-sectional results from the Canadian Multicentre Osteoporosis Study. J Bone Miner Res. 2003 Apr;18(4):784–790. doi: 10.1359/jbmr.2003.18.4.784. [DOI] [PubMed] [Google Scholar]
  14. Isaia G. C., Ardissone P., Di Stefano M., Ferrari D., Martina V., Porta M., Tagliabue M., Molinatti G. M. Bone metabolism in type 2 diabetes mellitus. Acta Diabetol. 1999 Jun;36(1-2):35–38. doi: 10.1007/s005920050142. [DOI] [PubMed] [Google Scholar]
  15. Jehle P. M., Jehle D. R., Mohan S., Böhm B. O. 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. 1998 Nov;159(2):297–306. doi: 10.1677/joe.0.1590297. [DOI] [PubMed] [Google Scholar]
  16. Kao W. H. Linda, Kammerer Candace M., Schneider Jennifer L., Bauer Richard L., Mitchell Braxton D. Type 2 diabetes is associated with increased bone mineral density in Mexican-American women. Arch Med Res. 2003 Sep-Oct;34(5):399–406. doi: 10.1016/j.arcmed.2002.07.001. [DOI] [PubMed] [Google Scholar]
  17. Khan Aliya A., Brown Jacques P., Kendler David L., Leslie William D., Lentle Brian C., Lewiecki E. Michael, Miller Paul D., Nicholson R. Lawrence, Olszynski Wojciech P., Watts Nelson B. The 2002 Canadian bone densitometry recommendations: take-home messages. CMAJ. 2002 Nov 12;167(10):1141–1145. [PMC free article] [PubMed] [Google Scholar]
  18. Krakauer J. C., McKenna M. J., Buderer N. F., Rao D. S., Whitehouse F. W., Parfitt A. M. Bone loss and bone turnover in diabetes. Diabetes. 1995 Jul;44(7):775–782. doi: 10.2337/diab.44.7.775. [DOI] [PubMed] [Google Scholar]
  19. Levin M. E., Boisseau V. C., Avioli L. V. Effects of diabetes mellitus on bone mass in juvenile and adult-onset diabetes. N Engl J Med. 1976 Jan 29;294(5):241–245. doi: 10.1056/NEJM197601292940502. [DOI] [PubMed] [Google Scholar]
  20. Lunt M., Masaryk P., Scheidt-Nave C., Nijs J., Poor G., Pols H., Falch J. A., Hammermeister G., Reid D. M., Benevolenskaya L. The effects of lifestyle, dietary dairy intake and diabetes on bone density and vertebral deformity prevalence: the EVOS study. Osteoporos Int. 2001;12(8):688–698. doi: 10.1007/s001980170069. [DOI] [PubMed] [Google Scholar]
  21. McNair P., Christensen M. S., Madsbad S., Christiansen C., Transbøl I. Hypoparathyroidism in diabetes mellitus. Acta Endocrinol (Copenh) 1981 Jan;96(1):81–86. doi: 10.1530/acta.0.0960081. [DOI] [PubMed] [Google Scholar]
  22. Meyer H. E., Tverdal A., Falch J. A. Risk factors for hip fracture in middle-aged Norwegian women and men. Am J Epidemiol. 1993 Jun 1;137(11):1203–1211. doi: 10.1093/oxfordjournals.aje.a116622. [DOI] [PubMed] [Google Scholar]
  23. Nicodemus K. K., Folsom A. R., Iowa Women's Health Study Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care. 2001 Jul;24(7):1192–1197. doi: 10.2337/diacare.24.7.1192. [DOI] [PubMed] [Google Scholar]
  24. Okazaki R., Totsuka Y., Hamano K., Ajima M., Miura M., Hirota Y., Hata K., Fukumoto S., Matsumoto T. Metabolic improvement of poorly controlled noninsulin-dependent diabetes mellitus decreases bone turnover. J Clin Endocrinol Metab. 1997 Sep;82(9):2915–2920. doi: 10.1210/jcem.82.9.4258. [DOI] [PubMed] [Google Scholar]
  25. Olmos J. M., Pérez-Castrillón J. L., García M. T., Garrido J. C., Amado J. A., González-Macías J. Bone densitometry and biochemical bone remodeling markers in type 1 diabetes mellitus. Bone Miner. 1994 Jul;26(1):1–8. doi: 10.1016/s0169-6009(08)80157-2. [DOI] [PubMed] [Google Scholar]
  26. Ottenbacher Kenneth J., Ostir Glenn V., Peek M. Kristen, Goodwin James S., Markides Kyriakos S. Diabetes mellitus as a risk factor for hip fracture in mexican american older adults. J Gerontol A Biol Sci Med Sci. 2002 Oct;57(10):M648–M653. doi: 10.1093/gerona/57.10.m648. [DOI] [PubMed] [Google Scholar]
  27. Pedrazzoni M., Ciotti G., Pioli G., Girasole G., Davoli L., Palummeri E., Passeri M. Osteocalcin levels in diabetic subjects. Calcif Tissue Int. 1989 Dec;45(6):331–336. doi: 10.1007/BF02556002. [DOI] [PubMed] [Google Scholar]
  28. Phillips G. B., Tuck C. H., Jing T. Y., Boden-Albala B., Lin I. F., Dahodwala N., Sacco R. L. Association of hyperandrogenemia and hyperestrogenemia with type 2 diabetes in Hispanic postmenopausal women. Diabetes Care. 2000 Jan;23(1):74–79. doi: 10.2337/diacare.23.1.74. [DOI] [PubMed] [Google Scholar]
  29. 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 Nov;29(11):584–591. doi: 10.1055/s-2007-979106. [DOI] [PubMed] [Google Scholar]
  30. Reddy G. K., Stehno-Bittel L., Hamade S., Enwemeka C. S. The biomechanical integrity of bone in experimental diabetes. Diabetes Res Clin Pract. 2001 Oct;54(1):1–8. doi: 10.1016/s0168-8227(01)00273-x. [DOI] [PubMed] [Google Scholar]
  31. Rosato M. T., Schneider S. H., Shapses S. A. Bone turnover and insulin-like growth factor I levels increase after improved glycemic control in noninsulin-dependent diabetes mellitus. Calcif Tissue Int. 1998 Aug;63(2):107–111. doi: 10.1007/s002239900498. [DOI] [PubMed] [Google Scholar]
  32. Rosenbloom A. L. Skeletal and joint manifestations of childhood diabetes. Pediatr Clin North Am. 1984 Jun;31(3):569–589. doi: 10.1016/s0031-3955(16)34607-7. [DOI] [PubMed] [Google Scholar]
  33. Schwartz A. V., Sellmeyer D. E., Ensrud K. E., Cauley J. A., Tabor H. K., Schreiner P. J., Jamal S. A., Black D. M., Cummings S. R., Study of Osteoporotic Features Research Group Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab. 2001 Jan;86(1):32–38. doi: 10.1210/jcem.86.1.7139. [DOI] [PubMed] [Google Scholar]
  34. Schwartz Ann V., Hillier Teresa A., Sellmeyer Deborah E., Resnick Helaine E., Gregg Edward, Ensrud Kristine E., Schreiner Pamela J., Margolis Karen L., Cauley Jane A., Nevitt Michael C. Older women with diabetes have a higher risk of falls: a prospective study. Diabetes Care. 2002 Oct;25(10):1749–1754. doi: 10.2337/diacare.25.10.1749. [DOI] [PubMed] [Google Scholar]
  35. Schwarz P., Sørensen H. A., Momsen G., Friis T., Transbøl I., McNair P. Hypocalcemia and parathyroid hormone responsiveness in diabetes mellitus: a tri-sodium-citrate clamp study. Acta Endocrinol (Copenh) 1992 Mar;126(3):260–263. doi: 10.1530/acta.0.1260260. [DOI] [PubMed] [Google Scholar]
  36. Selby P. L., Shearing P. A., Marshall S. M. Hydroxyproline excretion is increased in diabetes mellitus and related to the presence of microalbuminuria. Diabet Med. 1995 Mar;12(3):240–243. doi: 10.1111/j.1464-5491.1995.tb00465.x. [DOI] [PubMed] [Google Scholar]
  37. Sosa M., Dominguez M., Navarro M. C., Segarra M. C., Hernández D., de Pablos P., Betancor P. Bone mineral metabolism is normal in non-insulin-dependent diabetes mellitus. J Diabetes Complications. 1996 Jul-Aug;10(4):201–205. doi: 10.1016/1056-8727(95)00062-3. [DOI] [PubMed] [Google Scholar]
  38. Stepán J., Havránek T., Formánková J., Skrha J., Skrha F., Pacovský V. Bone isoenzyme of serum alkaline phosphatase in diabetes mellitus. Clin Chim Acta. 1980 Jul 17;105(1):75–81. doi: 10.1016/0009-8981(80)90094-7. [DOI] [PubMed] [Google Scholar]
  39. Stolk R. P., Van Daele P. L., Pols H. A., Burger H., Hofman A., Birkenhäger J. C., Lamberts S. W., Grobbee D. E. Hyperinsulinemia and bone mineral density in an elderly population: The Rotterdam Study. Bone. 1996 Jun;18(6):545–549. doi: 10.1016/8756-3282(96)00079-8. [DOI] [PubMed] [Google Scholar]
  40. Tuominen J. T., Impivaara O., Puukka P., Rönnemaa T. Bone mineral density in patients with type 1 and type 2 diabetes. Diabetes Care. 1999 Jul;22(7):1196–1200. doi: 10.2337/diacare.22.7.1196. [DOI] [PubMed] [Google Scholar]
  41. Verhaeghe J., van Herck E., Visser W. J., Suiker A. M., Thomasset M., Einhorn T. A., Faierman E., Bouillon R. Bone and mineral metabolism in BB rats with long-term diabetes. Decreased bone turnover and osteoporosis. Diabetes. 1990 Apr;39(4):477–482. doi: 10.2337/diab.39.4.477. [DOI] [PubMed] [Google Scholar]
  42. el Miedany Y. M., el Gaafary S., el Baddini M. A. Osteoporosis in older adults with non-insulin-dependent diabetes mellitus: is it sex related? Clin Exp Rheumatol. 1999 Sep-Oct;17(5):561–567. [PubMed] [Google Scholar]

Articles from Journal of the National Medical Association are provided here courtesy of National Medical Association

RESOURCES