HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Janghorbani, M. Articles by Hu, F. Search for Related Content PubMed PubMed Citation Articles by Janghorbani, M. Articles by Hu, F. Social Bookmarking                What's this?

Prospective Study of Diabetes and Risk of Hip Fracture

The Nurses’ Health Study

¹ School of Public Health, Isfahan University of Medical Sciences, Isfahan, Iran
² Channing Laboratory, Brigham and Women’s Hospital and Harvard Medical School, Boston, Massachusetts
³ Department of Nutrition, Harvard School of Public Heath, Boston, Massachusetts

Address correspondence and reprint requests to Prof. M. Janghorbani, School of Public Health, Isfahan University of Medical Sciences, Isfahan, Iran. E-mail: janghorbani{at}yahoo.com

	ABSTRACT

TOP ABSTRACT INTRODUCTION RESEARCH DESIGN AND METHODS RESULTS CONCLUSIONS References

 
OBJECTIVE—The purpose of this study was to determine whether women with type 1 and type 2 diabetes are at higher risk of hip fractures.

RESEARCH DESIGN AND METHODS—A total of 109,983 women aged 34–59 years in 1980 were followed through 2002 for the occurrence of hip fracture. At baseline and through biennial follow-up, women were asked about their history and treatment of diabetes and other potential risk factors for hip fracture.

RESULTS—During 2.22 million person-years of follow-up, 1,398 women had a hip fracture. Compared with women without diabetes, the age-adjusted relative risk (RRs) of hip fracture was 7.1 (95% CI 4.4–11.4) for women with type 1 diabetes and 1.7 (1.4–2.0) for those with type 2 diabetes. After further adjustment for BMI, smoking, physical activity, menopausal status, daily intake of calcium, vitamin D, protein, and postmenopausal hormone use, the multivariate RR of incident hip fracture in individuals with type 1 diabetes compared with individuals without diabetes was 6.4 (3.9–10.3) and with type 2 diabetes was 2.2 (1.8–2.7). The RRs increased with longer duration of type 2 diabetes (3.1 [2.3–4.0] for 12 years compared with no diabetes, P for trend < 0.001) and ever use of insulin.

CONCLUSIONS—These data indicate that both type 1 and type 2 diabetes are associated with an increased risk of hip fracture. The results of this study highlight the need for fracture-prevention strategies in women with diabetes.

Abbreviations: BMD, bone mineral density • NHS, Nurses’ Health Study • SOF, Studies of Osteoporotic Fractures

	INTRODUCTION

TOP ABSTRACT INTRODUCTION RESEARCH DESIGN AND METHODS RESULTS CONCLUSIONS References

 
The role of diabetes as a risk factor for osteoporosis and fracture remains unsettled. Bone mineral density (BMD) appears to be reduced in patients with type 1 diabetes in most (1–4) but not all studies (5,6). There have also been conflicting reports about BMD in patients with type 2 diabetes (3,4,7–18); in some studies BMD was reduced (7,9), whereas in other studies BMD was increased (8,10–12) or unchanged (13–18). Uncertainty also exists about the relationship between diabetes and fracture incidence. Only a few studies have examined the risk of fracture in people with type 1 diabetes (9,14–16,19,20); the risk of hip fracture appeared to be increased in some (9,14,19,20) but not all studies (15,16). Studies of the association between type 2 diabetes and the risk of fracture also demonstrated inconsistent conclusions (4,8,9,11,12,21–25). Several of these studies showed a positive association (12,22–25), whereas others reported no association (4,8,9) or even an inverse relation (11,21). However, most of these studies have been conducted with relatively small numbers of participants, have had limited ability to adjust for potential confounders, or were not able to distinguish between type 1 and type 2 diabetes (24,25). Given the conflicting results in previous studies, we used the large ongoing Nurses’ Health Study (NHS) to examine the risk of hip fracture in women with type 1 or type 2 diabetes.

	RESEARCH DESIGN AND METHODS

TOP ABSTRACT INTRODUCTION RESEARCH DESIGN AND METHODS RESULTS CONCLUSIONS References

 
The NHS is an ongoing cohort that was established in 1976 when 121,701 female registered nurses 30–55 years of age and residing in one of 11 states completed a mailed questionnaire on their health status and on various potential risk factors for diabetes, cancers, cardiovascular disease, and other chronic diseases. Of this cohort, 98% are white. Participants receive follow-up questionnaires biennially to update information on demographic, anthropometric, and lifestyle factors and on newly diagnosed diseases including hip fracture. The follow-up rate still exceeds 90% for every 2-year period. The study was approved by the Human Research Committees at the Harvard School of Public Health and Brigham and Women’s Hospital.

Ascertainment of fracture
Incident cases of hip fracture that occurred before 1 June 2002 were identified from questionnaires mailed to participants biennially after 1980. Although we relied on self-reports of hip fractures, we expected reliable information in a cohort of registered nurses. Validity was demonstrated in a small validation study in which all 30 reported hip fractures were confirmed by medical records (26). Fractures due to major trauma such as a motor vehicle accident were excluded.

Ascertainment of diabetes
Cases of diabetes were identified from baseline and biennial follow-up questionnaires. When women reported that diabetes had been diagnosed by a physician, confirmation was based on responses to a supplementary questionnaire about complications, diagnostic tests, and treatments. Confirmation criteria conformed to guidelines of the National Diabetes Data Group (27) until 1997 and to revised criteria of the American Diabetes Association from 1998 forward (28). A validation study found 98.4% concordance of our nurse participants’ reports of type 2 diabetes with medical records (29). Only women with definite type 1 and type 2 diabetes were considered in this analysis. We estimated duration of diabetes by subtracting the date of diagnosis from the date of last completed questionnaire. We obtained information on drug treatment for diabetes from the supplementary questionnaire. Using the baseline questionnaire, we classified women as having type 1 diabetes if diabetes was first diagnosed at 30 years of age and if they were currently using insulin or were ketosis prone (n = 292). Women whose diabetes was first diagnosed at >30 years of age were classified as having type 2 diabetes (n = 8,348). A total of 6,883 women without diabetes at baseline reported newly diagnosed type 2 diabetes in the biennial follow-up questionnaires.

Covariates
Information on age, body size, smoking status, weight change, alcohol intake, diet and physical activity, family and personal medical history, and postmenopausal hormone therapy was collected at the baseline and through biennial questionnaires. Every 2–4 years, we sent a semiquantitative food frequency questionnaire to the participants, from which we calculated nutrient intake values. Although the NHS cohort started in 1976, this analysis was begun in 1980 (referred to as baseline) when the food frequency questionnaire was first included. We calculated BMI as the ratio of weight in kilograms to the square of height in meters, the latter being assessed at 1976 only. Self-reports of body weight have been highly correlated with technician-measured weights (r = 0.96) (30). Waist and hip circumferences were self-reported in 1986 and 1996. Self-reports of waist and hip circumference have been reasonably correlated with the average of two technician measurements of waist and hip circumference (r = 0.89 for waist and 0.84 for hip) (31). The number of hours of leisure time physical activity per week was assessed in 1986, 1988, 1992, 1994, 1996, 1998, and 2000. Physical activity reported on the questionnaire was highly correlated with activity recorded in diaries (32).

Women who reported diabetes that was not confirmed were excluded from the analyses (n = 842). Participants were also excluded if they did not report their height or weight or reported, at baseline, having any disease or conditions known to affect fracture risk (e.g., cancer other than skin cancer or heart disease and stroke) (n = 10,876). This left a study population of 109,983 women with a mean ± SD age of 56.1 ± 9.4 years.

Analysis
Incidence was expressed as the number of cases of hip fracture per 100,000 person-years of follow-up beginning on the date of completion of the baseline questionnaire in 1980 and continuing until the occurrence of a hip fracture, the date of the last completed follow-up questionnaire, death, or end of follow-up on 1 June 2002, whichever came first. To describe the association between diabetes and risk of hip fracture we used two types of statistical analyses: age-adjusted relative risks (RRs) based on incidence rates and multivariate-adjusted RRs from Cox’s proportional hazard model using the SAS computer package (version 9.0; SAS Institute, Cary, NC). We considered the following covariates in the multivariate-adjusted analyses: current BMI, BMI at age 18, weight change from age 18 to current, waist-to-hip ratio, menopausal status and use of postmenopausal hormones, smoking, physical activity, history of osteoporosis, use of thiazide diuretics, dietary glycemic index, and daily consumption of calcium, vitamin D, protein, retinol, vitamin K, alcohol, and caffeine. To clarify the role of BMI further, we also conducted an analysis including the interaction terms of BMI as a continuous variable with type 2 diabetes in the "full" model.

	RESULTS

TOP ABSTRACT INTRODUCTION RESEARCH DESIGN AND METHODS RESULTS CONCLUSIONS References

 
Differences in distribution of several age-adjusted characteristics among 101,343 (92.1%) women without diabetes, 292 (0.3%) with type 1 diabetes, and 8,348 (7.6%) with type 2 diabetes are shown in Table 1. As expected, women with type 2 diabetes were older; had higher age-adjusted current BMI and at age 18, waist-to-hip ratio, and weight gain; were less likely to be alcohol drinkers; consumed less caffeine; were more likely to use thiazide diuretics and less likely to use postmenopausal hormones; and had slightly lower physical activity than those without diabetes and those with type 1 diabetes. In addition, women with either type of diabetes were less likely than women without diabetes to be users of estrogen. The mean ± SD age of hip fracture was 65.6 ± 8.3 years for nondiabetic subjects, 65.3 ± 7.4 years for type 1 diabetic subjects, and 68.6 ± 7.2 years for type 2 diabetic subjects. Of the 8,348 women with type 2 diabetes, 1,379 (16.5%) reported ever using insulin.

The association between type 2 diabetes and hip fracture was similar among obese and nonobese women (Table 3). Also, in both obese and nonobese women with type 2 diabetes, the risk of fracture increased with increasing duration of diabetes.

	CONCLUSIONS

TOP ABSTRACT INTRODUCTION RESEARCH DESIGN AND METHODS RESULTS CONCLUSIONS References

More studies have examined the effect of type 2 diabetes on bone fracture, also with inconsistent results. Although the SOF found that type 2 diabetes was associated with increased risk of foot (33) and proximal humerus fractures (23), another SOF report suggested an increased risk of hip fracture in women with diabetes not treated with insulin; after adjustment for obesity the RR was 1.6 (95% CI 0.9–2.7) (7). Also, the SOF reported an increased risk of hip and proximal humerus fractures in older women with type 2 diabetes, despite having higher BMD (12). In a case-control study among elderly people in Oslo, there was a nonsignificant increased risk for hip fracture in those with diabetes (34), whereas in a Danish study there was no increased risk in diabetic women treated with insulin compared with the general population (16). Studies in Norway also showed a strong association between diabetes and risk of hip fracture in both women and men, although it was not possible to distinguish between type 1 and type 2 diabetes (14,24). In the Blue Mountains Eye Study, insulin-treated type 2 diabetes but not tablet- or diet-treated type 2 diabetes was associated with an increased risk of fracture (8). At the Mayo Clinic, the risk of ankle fractures was elevated among women with diabetes, but a higher risk for other fracture sites was not found (15). These results, however, were not adjusted for body size or BMD. Melchior et al. (16) found no differences in rates of hip and Colles’ fracture among women with diabetes who were being treated with insulin compared with women without diabetes. In a large cross-sectional study from Rotterdam, women with type 2 diabetes had a lower frequency of self-reported nonspine fracture in the preceding 5 years than women without diabetes (11,35). In this study both men and women with type 2 diabetes had higher mean BMD than subjects without diabetes, even after adjustment for obesity. We found that women with type 2 diabetes had a 2.2 (1.8–2.7) times higher multivariate-adjusted risk of hip fracture than women without diabetes.

The mechanisms whereby diabetes exerts negative effects on fracture risk are not entirely clear. Putative mechanisms include lower BMD, weight loss, metabolic acidosis, and hyperglycemia in type 1 diabetes, whereas vision loss and neuropathy may be of greater importance in type 2 diabetes. Moreover, a link between microvascular complications of type 1 diabetes and long-term bone loss has been reported (36), notably between neuropathy and decreased BMD of the femoral neck (6). Another possible cause of the increased risk of hip fracture in both type 1 and type 2 diabetes is diabetes-related comorbidity (8,37,38), such as diabetic retinopathy, peripheral neuropathy, cerebral stroke, or hypoglycemia, which may increase the risk of falling. The combination of poor bone quality and frequent falls would be expected to increase the risk of fracture independent of BMD.

We found that the incidence of hip fracture was higher in patients with insulin-treated type 2 diabetes than in non–insulin-treated patients. Although we have no direct data on mechanisms, insulin treatment may indicate a more severe disease process rather than be a direct contributor to hip fracture. A higher incidence of hip fracture among insulin-treated patients could be attributable to a younger age at onset, to more difficult metabolic control than in non–insulin-treated type 2 diabetes or to episodes of hypoglycemia. Insulin may have an anabolic effect on bone (28,35), but the role of insulin in fracture risk is uncertain. This role warrants further study.

In this study, duration of type 2 diabetes was associated with the incidence of hip fracture, supporting the results of other studies (8,9), albeit not all studies (20). The strong association with duration may largely explain the substantially greater RR among women with type 1 diabetes. Measures of duration of diabetes are subject to error, and type 2 diabetes remains undiagnosed for years in many individuals; this error would tend to weaken associations with duration and could have accounted for the lack of an apparent relation in some studies.

Obesity is associated with type 2 diabetes and with increased levels of estrogen, which may decrease hip fracture risk among obese women. In addition, obesity provides cushioning for the hip in the event of a fall (7). However, our findings confirm other studies (9) in which type 2 diabetes increased the risk for hip fracture regardless of obesity.

Consistent with previous studies (9,39), we found that women with diabetes were less likely than women without diabetes to use hormone replacement therapy, which has been shown to lower the risk for hip fracture. However, the positive association between diabetes and hip fracture remained, even after adjustment for hormone replacement therapy, and a significant positive association was observed among never users (data not shown).

The strengths of this study include the prospective cohort design, large sample size, long-term follow-up, and detailed information on potential confounding factors, such as weight change, smoking, body size, exogenous estrogen, alcohol consumption, and diet. Selection and information bias were unlikely because of the prospective design and high rate of follow-up. However, the NHS was not undertaken primarily to determine risk factors for fracture. Thus, because there were no measures of BMD, neuromuscular impairment, history of fractures at baseline, family history of fractures, or cognitive impairment we cannot evaluate whether the increased hip fracture risk was mediated by reduced bone mass or by complications of diabetes predisposing to trauma, such as retinopathy, cerebral stroke, and peripheral neuropathy. Hip fracture was based on self-report, although the validity has been shown to be high (26). Because diabetes was determined by self-report and confirmed through a diagnostic supplementary questionnaire, those participants identified as not having diabetes probably included some women with undiagnosed type 2 diabetes. However, these misclassifications would tend to reduce rather than increase the significance of differences between diabetes and hip fracture. Some women with type 2 diabetes may have been misclassified as having type 1 diabetes, and some with late onset type 1 diabetes may have been included in our group of women with type 2 diabetes, but again this could not have accounted for the differences in risk. Another limitation was the fact that study participants were mainly white, and results may not apply to the broader population of women, especially to other racial/ethnic groups.

In summary, our study indicates that women with type 1 or type 2 diabetes are at increased risk for hip fracture. These findings highlight the need for fracture prevention efforts in individuals with diabetes.

	Acknowledgments

 
This work was supported by National Institutes of Health Grants DK58845 and P01CA87969.

We are grateful to Tricia Li for computer technical assistance. This study could not have been conducted without the contribution of the nurses who participated.

	Footnotes

 
The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C Section 1734 solely to indicate this fact.

A table elsewhere in this issue shows conventional and Système International (SI) units and conversion factors for many substances.

Received for publication February 24, 2006. Accepted for publication April 18, 2006.

	References

TOP ABSTRACT INTRODUCTION RESEARCH DESIGN AND METHODS RESULTS CONCLUSIONS References

 

1. Munoz-Torres M, Jodar E, Escobar-Jimenez F, Lopez-Ibarra PJ, Luna JD: Bone mineral density measured by dual X-ray absorptiometry in Spanish patients with insulin-dependent diabetes mellitus. Calcif Tissue Int 58:316–319, 1996[Medline]
   
2. 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 8:399–403, 1998[Medline]
   
3. Jehle PM, Jehle DR, Mohan S, Bohm BO: 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, 1998[Abstract]
   
4. Tuominen JT, Impivaara O, Puukka P, Ronnemaa T: Bone mineral density in patients with type 1 and type 2 diabetes. Diabetes Care 22:1196–1200, 1999[Abstract/Free Full Text]
   
5. Gallacher SJ, Fenner JA, Fisher BM, Quin JD, Fraser WD, Logue FC, Cowan RA, Boyle IT, MacCuish AC: An evaluation of bone density and turnover in premenopausal women with type 1 diabetes mellitus. Diabet Med 10:129–133, 1993[Medline]
   
6. Weber G, Beccaria L, de’Angelis M, Mora S, Galli L, Cazzuffi MA, Turba F, Frisone F, Guarneri MP, Chiumello G: Bone mass in young patients with type I diabetes. Bone Miner 8:23–30, 1990[Medline]
   
7. Cummings SR, Nevitt MC, Browner WS, Stone K, Fox KM, Ensrud KE, Cauley J, Black D, Vogt TM: Risk factors for hip fracture in white women: Study of Osteoporotic Fractures Research Group. N Engl J Med 332:767–773, 1995[Abstract/Free Full Text]
   
8. Ivers RQ, Cumming RG, Mitchell P, Peduto AJ: Diabetes and risk of fracture: the Blue Mountains Eye Study. Diabetes Care 24:1198–1203, 2001[Abstract/Free Full Text]
   
9. Nicodemus KK, Folsom AR: Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care 24:1192–1197, 2001[Abstract/Free Full Text]
   
10. Wakasugi M, Wakao R, Tawata M, Gan N, Koizumi K, Onaya T: Bone mineral density measured by dual energy X-ray absorptiometry in patients with non-insulin-dependent diabetes mellitus. Bone 14:29–33, 1993[Medline]
    
11. Van Daele PLA, Stolk RP, Burger H, Algra D, Grobbee DE, Hofman A, Birkenhagen JC, Pols HA: Bone density in non-insulin-dependent diabetes mellitus. Ann Intern Med 122:409–414, 1995[Abstract/Free Full Text]
    
12. Schwartz AV, Sellmeyer DE, Ensrud KE, Cauley JA, Tabor HK, Schreiner PJ, Birkenhager JC, Pols HA: Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab 86:32–38, 2001[Abstract/Free Full Text]
    
13. Sosa M, Dominguez M, Navarro MC, Segarra MC, Hernandez D, de Pablos P, Betancor P: Bone mineral metabolism is normal in non-insulin-dependent diabetes mellitus. J Diabetes Complications 10:201–205, 1996[Medline]
    
14. Forsen L, Meyer HE, Midthjell K, Edna TH: Diabetes mellitus and the incidence of hip fracture: results from the Nord-Trondelag Health Survey. Diabetologia 42:920–925, 1999[Medline]
    
15. Heath H, Melton LJ, Chu CP: Diabetes mellitus and risk of skeletal fracture. N Engl J Med 303:567–570, 1980[Medline]
    
16. Melchior TM, Sorensen H, Torp-Pedersen C: Hip and distal arm fracture rates in peri- and postmenopausal insulin-treated diabetic females. J Intern Med 236:203–208, 1994[Medline]
    
17. Barrett-Connor E, Holbrook TL: Sex differences in osteoporosis in older adults with non-insulin-dependent diabetes mellitus. JAMA 268:3333–3337, 1992[Abstract]
    
18. Isaia GC, Ardissone P, Di Stefano M, Ferrari D, Martina V, Porta M, Tagliabue M, Molinatti GM: Bone metabolism in type 2 diabetes mellitus. Acta Diabetol 36:35–38, 1999[Medline]
    
19. Miao J, Brismar K, Nyren O, Ugarph-Morawski A, Ye W: Elevated hip fracture risk in type 1 diabetic patients: a population-based cohort study in Sweden. Diabetes Care 28:2850–2855, 2005[Abstract/Free Full Text]
    
20. Vestergaard P, Rejnmark L, Mosekilde L: Relative fracture risk in patients with diabetes mellitus, and the impact of insulin and oral antidiabetic medication on relative fracture risk. Diabetologia 48:1292–1299, 2005[Medline]
    
21. Korpelainen R, Korpelainen J, Heikkinen J, Vaananen K, Keinanen-Kiukaanniemi S: Lifestyle factors are associated with osteoporosis in lean women but not in normal and overweight women: a population-based cohort study of 1,222 women. Osteoporos Int 14:34–43, 2003[Medline]
    
22. Ottenbacher KJ, Ostir GV, Peek MK, Goodwin JS, Markides KS: Diabetes mellitus as a risk factor for hip fracture in Mexican-American older adults. J Gerontol A Biol Sci Med Sci 57:M648–M653, 2002[Abstract/Free Full Text]
    
23. Kelsey JL, Browner WS, Seeley DG, Nevitt MC, Cummings SR: Risk factors for fractures of the distal forearm and proximal humerus: the Study of Osteoporotic Fractures Research Group. Am J Epidemiol 135:477–489, 1992[Abstract/Free Full Text]
    
24. Meyer HE, Tverdal A, Falch JA: Risk factors for hip fracture in middle-aged Norwegian women and men. Am J Epidemiol 137:1203–1211, 1993.[Abstract/Free Full Text]
    
25. Vogt MT, Cauley JA, Tomaino MM, Stone K, Williams JR, Herndon JH: Distal radius fractures in older women: a 10-year follow-up study of descriptive characteristics and risk factors: the study of osteoporotic fractures. J Am Geriatr Soc 50:97–103, 2002[Medline]
    
26. Colditz GA, Martin P, Stampfer MJ, Willett WC, Sampson L, Rosner B, Hennekens CH, Speizer FE: Validation of questionnaire information on risk factors and disease outcomes in a prospective cohort study of women. Am J Epidemiol 123:894–900, 1986[Abstract/Free Full Text]
    
27. National Diabetes Data Group: Classification and diagnosis of diabetes mellitus and other categories of glucose intolerance. Diabetes 28:1039–1057, 1979.[Medline]
    
28. Expert Committee on the Diagnosis and Classification of Diabetes Mellitus: Report of the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus. Diabetes Care 23(Suppl. 1):S4–S19, 2000.
    
29. Manson JE, Rimm EB, Stampfer MJ, Colditz GA, Willett WC, Krolewski AS, Rosner B, Hennekens CH, Speizer FE: Physical activity and incidence of non-insulin-dependent diabetes mellitus in women. Lancet 338:774–778, 1991[Medline]
    
30. Willett W, Stampfer MJ, Bain C, Lipnick R, Speizer FE, Rosner B, Cramer D, Hennekens CH: Cigarette smoking, relative weight, and menopause. Am J Epidemiol 117:651–658, 1983[Abstract/Free Full Text]
    
31. Rimm EB, Stampfer MJ, Colditz GA, Chute CG, Litin LB, Willett WC: Validity of self-reported waist and hip circumferences in men and women. Epidemiology 1:466–473, 1990.[Medline]
    
32. Wolf AM, Hunter DJ, Colditz GA, Manson JE, Stampfer MJ, Corsano KA, Rosner B, Kriska A, Willett WC: Reproducibility and validity of a self-administered physical activity questionnaire. Int J Epidemiol 23:991–999, 1994[Abstract/Free Full Text]
    
33. Seeley DG, Kelsey J, Jergas M, Nevitt MC: Predictors of ankle and foot fractures in older women: the Study of Osteoporotic Fractures Research Group. J Bone Miner Res 11:1347–1355, 1996.[Medline]
    
34. Meyer HE, Henrikson C, Falch JA, Pedersen JI, Tverdal A: Risk factors for hip fracture in a high incidence area: a case-control study from Oslo, Norway. Osteoporosis Int 5:239–246, 1995[Medline]
    
35. Stolk RP, Van Daele PL, Pols HA, Burger H, Hofman A, Birkenhager JC, Lamberts SW, Grobbee DE: Hyperinsulinemia and bone material density in an elderly population: the Rotterdam Study. Bone 18:545–549, 1996[Medline]
    
36. Mathiassen B, Nielsen S, Johansen JS, Hartwell D, Ditzel J, Rodbro P, Christiansen C: Long-term bone loss in insulin-dependent diabetic patients with microvascular complications. J Diabetes Complications 4:145–149, 1990
    
37. Leidig-Bruckner G, Ziegler R: Diabetes mellitus a risk for osteoporosis? Exp Clin Endocrinol Diabetes 109:S493–S514, 2001[Medline]
    
38. Nelson DA, Jacober SJ: Why do older women with diabetes have an increased fracture risk? J Clin Endocrinol Metab 86:29–31, 2001[Free Full Text]
    
39. Keating NL, Cleary PD, Rossi AS, Zaslavsky AM, Ayanian JZ: Use of hormone replacement therapy by postmenopausal women in the United States. Ann Intern Med 130:545–553, 1999.[Abstract/Free Full Text]
    

CiteULike

Del.icio.us

Digg

Reddit

Technorati

This article has been cited by other articles:

				J. L. Fowlkes, R. C. Bunn, L. Liu, E. C. Wahl, H. N. Coleman, G. E. Cockrell, D. S. Perrien, C. K. Lumpkin Jr., and K. M. Thrailkill Runt-Related Transcription Factor 2 (RUNX2) and RUNX2-Related Osteogenic Genes Are Down-Regulated throughout Osteogenesis in Type 1 Diabetes Mellitus Endocrinology, April 1, 2008; 149(4): 1697 - 1704. [Abstract] [Full Text] [PDF]

				M. Monami, B. Cresci, A. Colombini, L. Pala, D. Balzi, F. Gori, V. Chiasserini, N. Marchionni, C. M. Rotella, and E. Mannucci Bone Fractures and Hypoglycemic Treatment in Type 2 Diabetic Patients: A case-control study Diabetes Care, February 1, 2008; 31(2): 199 - 203. [Abstract] [Full Text] [PDF]

				H.-F. Chen, C.-A. Ho, and C.-Y. Li Increased Risks of Hip Fracture in Diabetic Patients of Taiwan: A population-based study Diabetes Care, January 1, 2008; 31(1): 75 - 80. [Abstract] [Full Text] [PDF]

				M. Janghorbani, R. M. Van Dam, W. C. Willett, and F. B. Hu Systematic Review of Type 1 and Type 2 Diabetes Mellitus and Risk of Fracture Am. J. Epidemiol., September 1, 2007; 166(5): 495 - 505. [Abstract] [Full Text] [PDF]

This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Janghorbani, M. Articles by Hu, F. Search for Related Content PubMed PubMed Citation Articles by Janghorbani, M. Articles by Hu, F. Social Bookmarking                What's this?