Skip to main content

Advertisement

SpringerLink
Log in

Diabetes mellitus and risk of hip fractures: a meta-analysis

  • Original Article
  • Published:
Osteoporosis International Aims and scope Submit manuscript

Abstract

Summary

This meta-analysis revealed that diabetic adults had a twofold greater risk of hip fractures compared with non-diabetic populations, and this association was more pronounced in type 1 diabetes.

Introduction

The relationship between diabetes mellitus and risk of hip fracture yielded conflicting results. We conducted a meta-analysis to investigate the association between diabetes mellitus and the risk of hip fractures based on observational studies.

Methods

We conducted a systematic literature search of PubMed and Embase databases through May 2015. We selected cohort and case–control studies providing at least age-adjusted risk ratio (RR) and corresponding 95 % confidence intervals (CI) of hip fractures among diabetic and non-diabetic subjects. Moreover, we pooled the female-to-male RR of hip fractures from studies that reported gender-specific risk estimate in a single study.

Results

Twenty-one studies involving 82,293 hip fracture events among 6,995,272 participants were identified. Diabetes mellitus was associated with an increased risk of hip fractures (RR 2.07; 95 % CI 1.83–2.33) in a random effects model. Subgroup analysis indicated that excess risk of hip fracture was more pronounced in type 1 diabetes (RR 5.76; 95 % CI 3.66–9.07) than that in type 2 diabetes (RR 1.34; 95 % CI 1.19–1.51). The pooled female-to-male RR of hip fractures was 1.09 (95 % CI 0.93–1.28).

Conclusions

Individuals with diabetes mellitus have an excessive risk of hip fractures, and this relationship is more pronounced in type 1 diabetes. The association between diabetes and hip fracture risk is similar in men and women.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Kanis JA, Oden A, McCloskey EV, Johansson H, Wahl DA, Cooper C (2012) A systematic review of hip fracture incidence and probability of fracture worldwide. Osteoporos Int 23:2239–56

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Cooper C, Cole ZA, Holroyd CR, Earl SC, Harvey NC, Dennison EM et al (2011) Secular trends in the incidence of hip and other osteoporotic fractures. Osteoporos Int 22:1277–88

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Gulcelik NE, Bayraktar M, Caglar O, Alpaslan M, Karakaya J (2011) Mortality after hip fracture in diabetic patients. Exp Clin Endocrinol Diabetes 119:414–8

    Article  PubMed  CAS  Google Scholar 

  4. Kannegaard PN, van der Mark S, Eiken P, Abrahamsen B (2010) Excess mortality in men compared with women following a hip fracture. National analysis of comedications, comorbidity and survival. Age Ageing 39:203–9

    Article  PubMed  Google Scholar 

  5. Bertram M, Norman R, Kemp L, Vos T (2011) Review of the long-term disability associated with hip fractures. Inj Prev 17:365–70

    Article  PubMed  Google Scholar 

  6. Reistetter TA, Graham JE, Deutsch A, Markello SJ, Granger CV, Ottenbacher KJ (2011) Diabetes comorbidity and age influence rehabilitation outcomes after hip fracture. Diabetes Care 34:1375–7

    Article  PubMed  PubMed Central  Google Scholar 

  7. Lee YK, Koo KH (2013) Osteoporotic hip fracture in the elderly patients: physicians’ views. J Korean Med Sci 28:976–7

    Article  PubMed  PubMed Central  Google Scholar 

  8. Whiting DR, Guariguata L, Weil C, Shaw J (2011) IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res Clin Pract 94:311–21

    Article  PubMed  Google Scholar 

  9. Mayne D, Stout NR, Aspray TJ (2010) Diabetes, falls and fractures. Age Ageing 39:522–5

    Article  PubMed  Google Scholar 

  10. Nicodemus KK, Folsom AR (2001) Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care 24:1192–7

    Article  PubMed  CAS  Google Scholar 

  11. Janghorbani M, Feskanich D, Willett WC, Hu F (2006) Prospective study of diabetes and risk of hip fracture: the Nurses’ Health Study. Diabetes Care 29:1573–8

    Article  PubMed  Google Scholar 

  12. Holmberg AH, Johnell O, Nilsson PM, Nilsson J, Berglund G, Akesson K (2006) Risk factors for fragility fracture in middle age. A prospective population-based study of 33,000 men and women. Osteoporos Int 17:1065–77

    Article  PubMed  CAS  Google Scholar 

  13. Dobnig H, Piswanger-Solkner JC, Roth M, Obermayer-Pietsch B, Tiran A, Strele A et al (2006) Type 2 diabetes mellitus in nursing home patients: effects on bone turnover, bone mass, and fracture risk. J Clin Endocrinol Metab 91:3355–63

    Article  PubMed  CAS  Google Scholar 

  14. 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 42:920–5

    Article  PubMed  CAS  Google Scholar 

  15. Ahmed LA, Joakimsen RM, Berntsen GK, Fonnebo V, Schirmer H (2006) Diabetes mellitus and the risk of non-vertebral fractures: the Tromso study. Osteoporos Int 17:495–500

    Article  PubMed  Google Scholar 

  16. Schwartz AV, Sellmeyer DE, Ensrud KE, Cauley JA, Tabor HK, Schreiner PJ et al (2001) Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab 86:32–8

    Article  PubMed  CAS  Google Scholar 

  17. Meyer HE, Tverdal A, Falch JA (1993) Risk factors for hip fracture in middle-aged Norwegian women and men. Am J Epidemiol 137:1203–11

    PubMed  CAS  Google Scholar 

  18. Vestergaard P, Rejnmark L, Mosekilde L (2005) Relative fracture risk in patients with diabetes mellitus, and the impact of insulin and oral antidiabetic medication on relative fracture risk. Diabetologia 48:1292–9

    Article  PubMed  CAS  Google Scholar 

  19. Miao J, Brismar K, Nyren O, Ugarph-Morawski A, Ye W (2005) Elevated hip fracture risk in type 1 diabetic patients: a population-based cohort study in Sweden. Diabetes Care 28:2850–5

    Article  PubMed  Google Scholar 

  20. Ivers RQ, Cumming RG, Mitchell P, Peduto AJ (2001) Diabetes and risk of fracture: The Blue Mountains Eye Study. Diabetes Care 24:1198–203

    Article  PubMed  CAS  Google Scholar 

  21. Ottenbacher KJ, Ostir GV, Peek MK, Goodwin JS, Markides KS (2002) Diabetes mellitus as a risk factor for hip fracture in mexican american older adults. J Gerontol A Biol Sci Med Sci 57:M648–53

    Article  PubMed  Google Scholar 

  22. de L, II, van der Klift M, de Laet CE, van Daele PL, Hofman A, Pols HA. Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam Study. Osteoporos Int. 2005;16:1713–20.

  23. Janghorbani M, Van Dam RM, Willett WC, Hu FB (2007) Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am J Epidemiol 166:495–505

    Article  PubMed  Google Scholar 

  24. Leslie WD, Lix LM, Prior HJ, Derksen S, Metge C, O’Neil J (2007) Biphasic fracture risk in diabetes: a population-based study. Bone 40:1595–601

    Article  PubMed  Google Scholar 

  25. Lipscombe LL, Jamal SA, Booth GL, Hawker GA (2007) The risk of hip fractures in older individuals with diabetes: a population-based study. Diabetes Care 30:835–41

    Article  PubMed  Google Scholar 

  26. Chen HF, Ho CA, Li CY (2008) Increased risks of hip fracture in diabetic patients of Taiwan: a population-based study. Diabetes Care 31:75–80

    Article  PubMed  CAS  Google Scholar 

  27. Koh WP, Wang R, Ang LW, Heng D, Yuan JM, Yu MC (2010) Diabetes and risk of hip fracture in the Singapore Chinese Health Study. Diabetes Care 33:1766–70

    Article  PubMed  PubMed Central  Google Scholar 

  28. Strotmeyer ES, Kamineni A, Cauley JA, Robbins JA, Fried LF, Siscovick DS et al (2011) Potential explanatory factors for higher incident hip fracture risk in older diabetic adults. Curr Gerontol Geriatr Res 2011:979270

    Article  PubMed  PubMed Central  Google Scholar 

  29. Giangregorio LM, Leslie WD, Lix LM, Johansson H, Oden A, McCloskey E et al (2012) FRAX underestimates fracture risk in patients with diabetes. J Bone Miner Res 27:301–8

    Article  PubMed  Google Scholar 

  30. Oei L, Zillikens MC, Dehghan A, Buitendijk GH, Castano-Betancourt MC, Estrada K et al (2013) High bone mineral density and fracture risk in type 2 diabetes as skeletal complications of inadequate glucose control: the Rotterdam Study. Diabetes Care 36:1619–28

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Hothersall EJ, Livingstone SJ, Looker HC, Ahmed SF, Cleland S, Leese GP et al (2014) Contemporary risk of hip fracture in type 1 and type 2 diabetes: a national registry study from Scotland. J Bone Miner Res 29:1054–60

    Article  PubMed  PubMed Central  Google Scholar 

  32. Martinez-Laguna D, Tebe C, Javaid MK, Nogues X, Arden NK, Cooper C et al (2015) Incident type 2 diabetes and hip fracture risk: a population-based matched cohort study. Osteoporos Int 26:827–33

    Article  PubMed  CAS  Google Scholar 

  33. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D et al (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 283:2008–12

    Article  PubMed  CAS  Google Scholar 

  34. Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med 151:264–9, W64

    Article  PubMed  Google Scholar 

  35. Wells G, Shea B, O’Connell D, Peterson J, Welch V, Losos M, et al. The Newcastle–Ottawa Scale (NOS) for assessing the quality if nonrandomized studies in meta-analyses. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp (accessed October 1, 2014).

  36. Higgins JPT, Green S, Editors. Cochrane handbook for systematic reviews of interventions version 5.1.0 [updated March 2011]: the Cochrane collaboration; 2011.

  37. DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7:177–88

    Article  PubMed  CAS  Google Scholar 

  38. Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50:1088–101

    Article  PubMed  CAS  Google Scholar 

  39. Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–34

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. de Ferranti SD, de Boer IH, Fonseca V, Fox CS, Golden SH, Lavie CJ et al (2014) Type 1 diabetes mellitus and cardiovascular disease: a scientific statement from the American Heart Association and American Diabetes Association. Circulation 130:1110–30

    Article  PubMed  Google Scholar 

  41. Engelgau MM, Geiss LS, Saaddine JB, Boyle JP, Benjamin SM, Gregg EW et al (2004) The evolving diabetes burden in the United States. Ann Intern Med 140:945–50

    Article  PubMed  Google Scholar 

  42. Tang X, Liu G, Kang J, Hou Y, Jiang F, Yuan W et al (2013) Obesity and risk of hip fracture in adults: a meta-analysis of prospective cohort studies. PLoS One 8:e55077

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Khalil N, Sutton-Tyrrell K, Strotmeyer ES, Greendale GA, Vuga M, Selzer F et al (2011) Menopausal bone changes and incident fractures in diabetic women: a cohort study. Osteoporos Int 22:1367–76

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Vestergaard P (2009) Bone metabolism in type 2 diabetes and role of thiazolidinediones. Curr Opin Endocrinol Diabetes Obes 16:125–31

    Article  PubMed  CAS  Google Scholar 

  45. Carnevale V, Romagnoli E, D’Erasmo L, D’Erasmo E (2014) Bone damage in type 2 diabetes mellitus. Nutr Metab Cardiovasc Dis 24:1151–7

    Article  PubMed  CAS  Google Scholar 

  46. de Waard EA, van Geel TA, Savelberg HH, Koster A, Geusens PP, van den Bergh JP (2014) Increased fracture risk in patients with type 2 diabetes mellitus: an overview of the underlying mechanisms and the usefulness of imaging modalities and fracture risk assessment tools. Maturitas 79:265–74

    Article  PubMed  Google Scholar 

Download references

Conflicts of interest

Yu Fan, Feifei Wei, Yakun Lang, and Yingzhao Liu declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Institute of Molecular Biology and Translational Medicine, The Affiliated People’s Hospital, Jiangsu University, Zhenjiang, Jiangsu, People’s Republic of China, 212002

    Y. Fan, F. Wei & Y. Lang

  2. Department of Endocrinology, The Affiliated People’s Hospital, Jiangsu University, No. 8 Dianli Road, Zhenjiang, Jiangsu, People’s Republic of China, 212002

    Y. Liu

Authors
  1. Y. Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F. Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Y. Lang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Y. Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Y. Liu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 71 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fan, Y., Wei, F., Lang, Y. et al. Diabetes mellitus and risk of hip fractures: a meta-analysis. Osteoporos Int 27, 219–228 (2016). https://doi.org/10.1007/s00198-015-3279-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-015-3279-7

Keywords

Search

Navigation