Secondary Osteoporosis and Its Associated Fractures in Postmenopausal Women with Diabetes_Chinese Journal of Evidence-Based Medicine

Authors：

WANG Xiaoping ¹ ,  DING Hongliu ²

1. Shanghai First People’s Hospital, Shanghai Jiaotong University, Shanghai 200080, China2. Meyers Primary Care Institute, University of Massachusetts Medical School, Worcester, MA 01605, USA;

Corresponding author：

DING Hongliu, Email: hlding@hotmail.com

Keywords：

Diabetes; Osteoporosis; Fracture; Analysis of correlation

DOI：

10.7507/1672-2531.20080121

Video：

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Objective 　Secondary osteoporosis is very common in patients with primary osteoporosis. Diabetes is a known cause of secondary osteoporosis. While type I diabetes has been clearly linked with diabetic osteoporosis, the effect of type II diabetes on bone health is controversial.
Methods 　In the present study, we investigated the associations between type II diabetes and osteoporosis as well as fractures at different skeletal sites in Women’s Health Initiative participants.
Results 　Common risk factors such as age, race, BMI, HRT use, and the history of fractures were significantly associated with osteoporosis and fractures in this study population. Diabetic women appeared to have a decreased risk of osteoporosis although it no longer remained significant after adjusting for other risk factors (crude HR=0.78, 95%CI 0.61 to 0.99; adjusted HR=0.93, 95%CI 0.73 to 1.19). The impact of diabetes on fractures varied at different body sites. There was a significant increase of risk of hip fracture (HR=2.54, 95%CI 1.14 to 5.66), but not spine fracture (HR=1.71, 95%CI 0.81 to 3.60) and arm fracture (HR=0.92, 95%CI 0.48 to 1.76) among the women with diabetes. Although the overall risk of fractures in diabetic women did not differ significantly from non-diabetic women (HR=1.37, 95%CI 0.89 to 2.09), the difference had a two-fold increase and was statistically significant after 2,000 days (HR=2.01, 95%CI 1.21 to 3.35), indicating a different hazard at different stages of diabetes.
Conclusion 　Our findings suggest that type II diabetes may not be clearly associated with osteoporosis, it increases a site-specific fracture risk at least in the hip. In addition, the overall fracture risk appears to increase in a time-dependent manner.

Citation： WANG Xiaoping,DING Hongliu. Secondary Osteoporosis and Its Associated Fractures in Postmenopausal Women with Diabetes. Chinese Journal of Evidence-Based Medicine, 2008, 08(7): 517-524. doi: 10.7507/1672-2531.20080121 Copy

1.	National Osteoporosis Foundation: available at http://www.nof.org/osteoporosis/diseasefacts.htm. Accessed: January 11, 2008.
2.	Cooper C. Epidemiology of osteoporosis. Osteoporos Int, 1999, 9(Suppl 2): S2-8.
3.	Stein E & Shane E. Secondary osteoporosis. Endocrinology and Metabolism Clinics of North America, 2003, 1: 115-134.
4.	Tuominen JT, Impivaara O, Puukka P, et al. Bone mineral density in patients with type 1 and type 2 diabetes. Diabetes Care, 1999, 22: 1196-1200.
5.	McNair P, Christiansen C, Christensen MS, et al. Development of bone mineral loss in insulin-treated diabetes: a 112 years follow-up study in sixty patients. Eur J Clin Invest, 1981, 11: 55-59.
6.	Forst T, Pfutzner A, Kann P, et al. Peripheral osteopenia in adult patients with insulin-dependent diabetes mellitus. Diabetes Med, 1995, 12: 874-879.
7.	Buysschaert M, Cauwe F, Jamart J, et al. Proximal femur density in type 1 and 2 diabetic patients. Diabetes Metab, 1992, 18: 32-37.
8.	Hui SL, Epstein S, Johnston Jr CC. A prospective study of bone mass in patients with type I diabetes. J Clin Endocrinol Metab, 1985, 60: 74-80.
9.	Miazgowski T, Czekalski S. A 2-year follow-up study on bone mineral density and markers of bone turnover in patients with long-standing insulin-dependent diabetes mellitus. Osteoporos Int, 1998, 8: 399-403.
10.	Mathiassen B, Nielsen S, Johansen JS, et al. Long-term bone loss in insulin-dependent diabetic patients with microvascular complications. J Diabetes Complications, 1990, 4: 145-149.
11.	Levin ME, BoisseauVC, Avioli LV. Effects of diabetes mellitus on bone mass in juvenile and adult-onset diabetes. N Engl J Med, 1976, 294: 241-245.
12.	Gregorio F, Cristallini S, Santeusanio F, et al. Osteopenia associated with non-insulindependent diabetes mellitus: What are the causes? Diabetes Res Clin Pract, 1994, 23: 43-54.
13.	Krakauer JC, McKenna MJ, Buderer NF, et al. Bone loss and bone turnover in diabetes. Diabetes, 1995, 44: 775-782.
14.	Kao CH, TsouCT, Chen CC, et al. Bone mineral density in patients with noninsulin-dependent diabetes mellitus by dual photon absorptiometry. Nucl Med Commun, 1993, 14: 373-377.
15.	Wakasugi M, Wakao R, Tawata M, et al. Bone mineral density measured by dual energy x-ray absorptiometry in patients with non-insulindependent diabetes mellitus. Bone, 1993, 14: 29-33.
16.	Okuno Y, Nishizawa Y, Sekiya K, et al. Total and regional bone mineral content in patients with non-insulin-dependent diabetes mellitus. J Nutr Sci Vitaminol (Tokyo), 1991, 37(suppl): S43-S49.
17.	van Daele PL, Stolk RP, Burger H, et al. Bone density 518 A. V. Schwartz: Diabetes and Bone in non-insulin-dependent diabetes mellitus. The Rotterdam Study. Ann Intern Med, 1995, 122: 409-414.
18.	Hampson G, Evans C, Petitt RJ, et al. Bone mineral density, collagen type 1 alpha 1 genotypes and bone turnover in premenopausal women with diabetes mellitus. Diabetologia, 1998, 41: 1314-1320.
19.	Bauer DC, Browner WS, Cauley JA, et al. Factors associated with appendicular bone mass in older women. The Study of Osteoporotic Fractures Research Group. Ann Intern Med, 1993, 118: 657-665.
20.	Orwoll ES, Bauer DC, Vogt TM, et al. Axial bone mass in older women. Study of Osteoporotic Fractures Research Group. Ann Intern Med, 1996, 124: 187-196.
21.	Barrett-Connor E, Holbrook TL. Sex differences in osteoporosis in older adults with non-insulin-dependent diabetes mellitus. JAMA, 1992, 268: 3333-3337.
22.	Isaia GC, Ardissone P, Di Stefano M, et al. Bone metabolism in type 2 diabetes mellitus. Acta Diabetol, 1999, 36: 35-38.
23.	Schwartz AV, Sellmeyer DE, Ensrud KE, et al. Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab, 2001, 86: 32-38.
24.	Nicodemus KK, Folsom AR. Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care, 2001, 24: 1192-1197.
25.	Forsen L, Meyer HE, Midthjell K, et al. Diabetes mellitus and the incidence of hip fracture: results from the Nord-Trondelag Health Survey. Diabetologia, 1999, 42: 920-925.
26.	Meyer HE, Tverdal A, Falch JA. Risk factors for hip fracture in middle-aged Norwegian women and men. Am J Epidemiol, 1993, 137: 1203-1211.
27.	Ottenbacher KJ, Ostir GV, Peek MK, et al. Diabetes mellitus as a risk factor for hip fracture in Mexican American older adults. J Gerontol A Biol Sci Med Sci, 2002, 57: M648-653.
28.	Keegan TH, Kelsey JL, Sidney S, et al. Foot problems as risk factors of fractures. Am J Epidemiol, 2002, 155: 926-931.
29.	Majima T, Komatsu Y, Yamada T, et al. Decreased bone mineral density at the distal radius, but not at lumbar spine or the femoral neck, in Japanese type 2 diabetic patients. Osteoporosis Int, 2005, 16: 907-913.
30.	Schwartz AV, Hillier TA, Sellmeyer DE, et al. Older women with diabetes have a higher risk of falls: a prospective study. Diabetes Care, 2002, 25(10):1749-1754.
31.	Haffner SM, Bauer RL. The association of obesity and glucose and insulin concentrations with bone density in premenopausal and postmenopausal women. Metabolism, 1993, 42: 735-738.
32.	Reid IR, Evans MC, Cooper GJ, et al. Circulating insulin levels are related to bone density in normal postmenopausal women. Am J Physiol, 1993, 265: E655-659.
33.	Stolk RP, van Daele PL, Pols HA, et al. Hyperinsulinemia and bone mineral density in an elderly population: The Rotterdam Study. Bone, 1996, 18: 545-549.
34.	Barrett-Connor E, Kritz-Silverstein D. Does hyperinsulinemia preserve bone? Diabetes Care, 1996, 19: 1388–1392.

1. National Osteoporosis Foundation: available at http://www.nof.org/osteoporosis/diseasefacts.htm. Accessed: January 11, 2008.
2. Cooper C. Epidemiology of osteoporosis. Osteoporos Int, 1999, 9(Suppl 2): S2-8.
3. Stein E & Shane E. Secondary osteoporosis. Endocrinology and Metabolism Clinics of North America, 2003, 1: 115-134.
4. Tuominen JT, Impivaara O, Puukka P, et al. Bone mineral density in patients with type 1 and type 2 diabetes. Diabetes Care, 1999, 22: 1196-1200.
5. McNair P, Christiansen C, Christensen MS, et al. Development of bone mineral loss in insulin-treated diabetes: a 112 years follow-up study in sixty patients. Eur J Clin Invest, 1981, 11: 55-59.
6. Forst T, Pfutzner A, Kann P, et al. Peripheral osteopenia in adult patients with insulin-dependent diabetes mellitus. Diabetes Med, 1995, 12: 874-879.
7. Buysschaert M, Cauwe F, Jamart J, et al. Proximal femur density in type 1 and 2 diabetic patients. Diabetes Metab, 1992, 18: 32-37.
8. Hui SL, Epstein S, Johnston Jr CC. A prospective study of bone mass in patients with type I diabetes. J Clin Endocrinol Metab, 1985, 60: 74-80.
9. Miazgowski T, Czekalski S. A 2-year follow-up study on bone mineral density and markers of bone turnover in patients with long-standing insulin-dependent diabetes mellitus. Osteoporos Int, 1998, 8: 399-403.
10. Mathiassen B, Nielsen S, Johansen JS, et al. Long-term bone loss in insulin-dependent diabetic patients with microvascular complications. J Diabetes Complications, 1990, 4: 145-149.
11. Levin ME, BoisseauVC, Avioli LV. Effects of diabetes mellitus on bone mass in juvenile and adult-onset diabetes. N Engl J Med, 1976, 294: 241-245.
12. Gregorio F, Cristallini S, Santeusanio F, et al. Osteopenia associated with non-insulindependent diabetes mellitus: What are the causes? Diabetes Res Clin Pract, 1994, 23: 43-54.
13. Krakauer JC, McKenna MJ, Buderer NF, et al. Bone loss and bone turnover in diabetes. Diabetes, 1995, 44: 775-782.
14. Kao CH, TsouCT, Chen CC, et al. Bone mineral density in patients with noninsulin-dependent diabetes mellitus by dual photon absorptiometry. Nucl Med Commun, 1993, 14: 373-377.
15. Wakasugi M, Wakao R, Tawata M, et al. Bone mineral density measured by dual energy x-ray absorptiometry in patients with non-insulindependent diabetes mellitus. Bone, 1993, 14: 29-33.
16. Okuno Y, Nishizawa Y, Sekiya K, et al. Total and regional bone mineral content in patients with non-insulin-dependent diabetes mellitus. J Nutr Sci Vitaminol (Tokyo), 1991, 37(suppl): S43-S49.
17. van Daele PL, Stolk RP, Burger H, et al. Bone density 518 A. V. Schwartz: Diabetes and Bone in non-insulin-dependent diabetes mellitus. The Rotterdam Study. Ann Intern Med, 1995, 122: 409-414.
18. Hampson G, Evans C, Petitt RJ, et al. Bone mineral density, collagen type 1 alpha 1 genotypes and bone turnover in premenopausal women with diabetes mellitus. Diabetologia, 1998, 41: 1314-1320.
19. Bauer DC, Browner WS, Cauley JA, et al. Factors associated with appendicular bone mass in older women. The Study of Osteoporotic Fractures Research Group. Ann Intern Med, 1993, 118: 657-665.
20. Orwoll ES, Bauer DC, Vogt TM, et al. Axial bone mass in older women. Study of Osteoporotic Fractures Research Group. Ann Intern Med, 1996, 124: 187-196.
21. Barrett-Connor E, Holbrook TL. Sex differences in osteoporosis in older adults with non-insulin-dependent diabetes mellitus. JAMA, 1992, 268: 3333-3337.
22. Isaia GC, Ardissone P, Di Stefano M, et al. Bone metabolism in type 2 diabetes mellitus. Acta Diabetol, 1999, 36: 35-38.
23. Schwartz AV, Sellmeyer DE, Ensrud KE, et al. Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab, 2001, 86: 32-38.
24. Nicodemus KK, Folsom AR. Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care, 2001, 24: 1192-1197.
25. Forsen L, Meyer HE, Midthjell K, et al. Diabetes mellitus and the incidence of hip fracture: results from the Nord-Trondelag Health Survey. Diabetologia, 1999, 42: 920-925.
26. Meyer HE, Tverdal A, Falch JA. Risk factors for hip fracture in middle-aged Norwegian women and men. Am J Epidemiol, 1993, 137: 1203-1211.
27. Ottenbacher KJ, Ostir GV, Peek MK, et al. Diabetes mellitus as a risk factor for hip fracture in Mexican American older adults. J Gerontol A Biol Sci Med Sci, 2002, 57: M648-653.
28. Keegan TH, Kelsey JL, Sidney S, et al. Foot problems as risk factors of fractures. Am J Epidemiol, 2002, 155: 926-931.
29. Majima T, Komatsu Y, Yamada T, et al. Decreased bone mineral density at the distal radius, but not at lumbar spine or the femoral neck, in Japanese type 2 diabetic patients. Osteoporosis Int, 2005, 16: 907-913.
30. Schwartz AV, Hillier TA, Sellmeyer DE, et al. Older women with diabetes have a higher risk of falls: a prospective study. Diabetes Care, 2002, 25(10):1749-1754.
31. Haffner SM, Bauer RL. The association of obesity and glucose and insulin concentrations with bone density in premenopausal and postmenopausal women. Metabolism, 1993, 42: 735-738.
32. Reid IR, Evans MC, Cooper GJ, et al. Circulating insulin levels are related to bone density in normal postmenopausal women. Am J Physiol, 1993, 265: E655-659.
33. Stolk RP, van Daele PL, Pols HA, et al. Hyperinsulinemia and bone mineral density in an elderly population: The Rotterdam Study. Bone, 1996, 18: 545-549.
34. Barrett-Connor E, Kritz-Silverstein D. Does hyperinsulinemia preserve bone? Diabetes Care, 1996, 19: 1388–1392.

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