Skip to main content

Advertisement

Log in

Incident type 2 diabetes and hip fracture risk: a population-based matched cohort study

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

Abstract

Summary

There is scarce data on the association between early stages of type 2 diabetes and fracture risk. We report a 20 % excess risk of hip fracture in the first years following disease onset compared to matched non-diabetic patients.

Introduction

Type 2 diabetes mellitus (T2DM) is a chronic disease that affects several target organs. Data on the association between T2DM and osteoporotic fractures is controversial. We estimated risk of hip fracture in newly diagnosed T2DM patients, compared to matched non-diabetic peers.

Methods

We conducted a population-based parallel cohort study using data from the Sistema d’Informació per al Desenvolupament de la Investigació en Atenció Primària (SIDIAP) database. Participants were all newly diagnosed T2DM patients registered in SIDIAP in 2006–2011 (T2DM cohort). Up to two diabetes-free controls were matched to each T2DM participant on age, gender, and primary care practice. Main outcome was incident hip fracture in 2006–2011, ascertained using the tenth edition of the International Classification of Diseases (ICD-10) codes. We used Fine and Gray survival modelling to estimate risk of hip fracture according to T2DM status, accounting for competing risk of death. Multivariate models were adjusted for body mass index, previous fracture, and use of oral corticosteroids.

Results

During the study period (median follow-up 2.63 years), 444/58,483 diabetic patients sustained a hip fracture (incidence rate 2.7/1,000 person-years) compared to 776/113,448 matched controls (2.4/1,000). This is equivalent to an unadjusted (age- and gender-matched) subhazard ratio (SHR) 1.11 [0.99–1.24], and adjusted SHR 1.20 [1.06–1.35]. The adjusted SHR for major osteoporotic and any osteoporotic fractures were 0.95 [0.89–1.01] and 0.97 [0.92–1.02].

Conclusions

Newly diagnosed T2DM patients are at a 20 % increased risk of hip fracture even in early stages of disease, but no for all fractures. More data is needed on the causes for an increased fracture risk in T2DM patients as well as on the predictors of osteoporotic fractures among these patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Soriguer F, Goday A, Bosch-Comas A et al (2012) Prevalence of diabetes mellitus and impaired glucose regulation in Spain: the Di@bet.es Study. Diabetologia 55:88–93

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  2. Curiel MD, García J, Carrasco J (2001) Prevalencia de osteoporosis determinada por densitometría en la población femenina española. Med Clin (Barc) 116:86–88

    Article  Google Scholar 

  3. De Liefde II, van der Klift M, de Laet CEDH, van Daele PL, Hofman A, Pols HAP (2005) Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam Study. Osteoporos Int 16:1713–1720

    Article  PubMed  Google Scholar 

  4. Vestergaard P (2007) Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes—a meta-analysis. Osteoporos Int 18:427–444

    Article  CAS  PubMed  Google Scholar 

  5. 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 

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

    Article  PubMed  Google Scholar 

  7. Forsén L, Meyer HE, Midthjell K, Edna TH (1999) Diabetes mellitus and the incidence of hip fracture: results from the Nord-Trøndelag Health Survey. Diabetologia 42:920–925

    Article  PubMed  Google Scholar 

  8. Blakytny R, Spraul M, Jude EB (2011) Review: The diabetic bone: a cellular and molecular perspective. Int J Low Extrem Wounds 10:16–32

    Article  PubMed  Google Scholar 

  9. Martínez-Laguna D, Nogués-Solán X, Díez-Pérez A, Soria-Castro A, Carbonell-Abella C, Arias-Moliz I, Estrada-Laza P, Prieto-Alhambra D (2013) Riesgo de fractura asociado a los estadios previos al diagnóstico de diabetes mellitus tipo 2: estudio de casos-controles anidados (cohorte DIAFOS). Rev Osteoporos Metab Min 02:73–78

    Article  Google Scholar 

  10. Schwartz AV, Vittinghoff E, Sellmeyer DE et al (2008) Diabetes-related complications, glycemic control, and falls in older adults. Diabetes Care 31:391–396

    Article  PubMed Central  PubMed  Google Scholar 

  11. Kanazawa I, Yamaguchi T, Yamamoto M, Yamauchi M, Yano S, Sugimoto T (2009) Relationships between serum adiponectin levels versus bone mineral density, bone metabolic markers, and vertebral fractures in type 2 diabetes mellitus. Eur J Endocrinol 160:265–273

    Article  CAS  PubMed  Google Scholar 

  12. Kahn SE, Haffner SM, Heise M et al (2006) Glycemic durability of rosiglitazone, metformin, or glyburide monotherapy. N Engl J Med 355:2427–2443

    Article  CAS  PubMed  Google Scholar 

  13. Home PD, Jones NP, Pocock SJ, Beck-Nielsen H, Gomis R, Hanefeld M, Komajda M, Curtis P (2007) Rosiglitazone RECORD study: glucose control outcomes at 18 months. Diabet Med 24:626–634

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  14. Meier C, Kraenzlin ME, Bodmer M, Jick SS, Jick H, Meier CR (2008) Use of thiazolidinediones and fracture risk. Arch Intern Med 168:820–825

    Article  CAS  PubMed  Google Scholar 

  15. García-Gil MDM, Hermosilla E, Prieto-Alhambra D, Fina F, Rosell M, Ramos R, Rodriguez J, Williams T, Van Staa T, Bolíbar B (2011) Construction and validation of a scoring system for the selection of high-quality data in a Spanish population primary care database (SIDIAP). Inform Prim Care 19:135–145

    Google Scholar 

  16. Vinagre I, Mata-Cases M, Hermosilla E, Morros R, Fina F, Rosell M, Castell C, Franch-Nadal J, Bolíbar B, Mauricio D (2012) Control of glycemia and cardiovascular risk factors in patients with type 2 diabetes in primary care in Catalonia (Spain). Diabetes Care 35:774–779

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Prieto-Alhambra D, Premaor MO, Fina Avilés F, Hermosilla E, Martinez-Laguna D, Carbonell-Abella C, Nogués X, Compston JE, Díez-Pérez A (2012) The association between fracture and obesity is site-dependent: a population-based study in postmenopausal women. J Bone Miner Res 27:294–300

    Article  PubMed  Google Scholar 

  18. Premaor MO, Compston JE, Fina Avilés F, Pagès-Castellà A, Nogués X, Díez-Pérez A, Prieto-Alhambra D (2013) The association between fracture site and obesity in men: a population-based cohort study. J Bone Miner Res 28:1771–1777

    Article  PubMed  Google Scholar 

  19. Prieto-Alhambra D, Premaor MO, Avilés FF, Castro AS, Javaid MK, Nogués X, Arden NK, Cooper C, Compston JE, Diez-Perez A (2014) Relationship between mortality and BMI after fracture: a population-based study of men and women aged ≥40 years. J Bone Miner Res 29:1737–1744

    Article  PubMed  Google Scholar 

  20. Pages-Castella A, Carbonell-Abella C, Aviles FF, Alzamora M, Baena-Diez JM, Laguna DM, Nogues X, Diez-Perez A, Prieto-Alhambra D (2012) “Burden of osteoporotic fractures in primary health care in Catalonia (Spain): a population-based study”. BMC Musculoskelet Disord 13:79

    Article  PubMed Central  PubMed  Google Scholar 

  21. Fine JP, Gray RJ (1999) A proportional hazards model for the subdistribution of a competing risk. J Am Stat Assoc 94:496–509

    Article  Google Scholar 

  22. Altman DG, Bland JM (2003) Interaction revisited: the difference between two estimates. BMJ 326:219

    Article  PubMed Central  PubMed  Google Scholar 

  23. Sterne JAC, White IR, Carlin JB, Spratt M, Royston P, Kenward MG, Wood AM, Carpenter JR (2009) Multiple imputation for missing data in epidemiological and clinical research: potential and pitfalls. BMJ 338:b2393

    Article  PubMed Central  PubMed  Google Scholar 

  24. Giangregorio LM, Leslie WD, Lix LM, Johansson H, Oden A, McCloskey E, Kanis JA (2012) FRAX underestimates fracture risk in patients with diabetes. J Bone Miner Res 27:301–308

    Article  PubMed  Google Scholar 

  25. Schwartz AV, Vittinghoff E, Bauer DC et al (2011) Association of BMD and FRAX score with risk of fracture in older adults with type 2 diabetes. JAMA 305:2184–2192

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Melton LJ, Leibson CL, Achenbach SJ, Therneau TM, Khosla S (2008) Fracture risk in type 2 diabetes: update of a population-based study. J Bone Miner Res 23:1334–1342

    Article  PubMed Central  PubMed  Google Scholar 

  27. Viégas M, Costa C, Lopes A, Griz L, Medeiro MA, Bandeira F (2011) Prevalence of osteoporosis and vertebral fractures in postmenopausal women with type 2 diabetes mellitus and their relationship with duration of the disease and chronic complications. J Diabetes Complicat 25:216–221

    Article  PubMed  Google Scholar 

  28. Bonds DE, Larson JC, Schwartz AV, Strotmeyer ES, Robbins J, Rodriguez BL, Johnson KC, Margolis KL (2006) Risk of fracture in women with type 2 diabetes: the Women’s Health Initiative Observational Study. J Clin Endocrinol Metab 91:3404–3410

    Article  CAS  PubMed  Google Scholar 

  29. Coutinho M, Gerstein HC, Wang Y, Yusuf S (1999) The relationship between glucose and incident cardiovascular events. A metaregression analysis of published data from 20 studies of 95,783 individuals followed for 12.4 years. Diabetes Care 22:233–240

    Article  CAS  PubMed  Google Scholar 

  30. DECODE Study Group the EDEG (2001) Glucose tolerance and cardiovascular mortality: comparison of fasting and 2-hour diagnostic criteria. Arch Intern Med 161:397–405

    Article  Google Scholar 

  31. Levitzky YS, Pencina MJ, D’Agostino RB, Meigs JB, Murabito JM, Vasan RS, Fox CS (2008) Impact of impaired fasting glucose on cardiovascular disease: the Framingham Heart Study. J Am Coll Cardiol 51:264–270

    Article  CAS  PubMed  Google Scholar 

  32. Duckworth W, Abraira C, Moritz T et al (2009) Glucose control and vascular complications in veterans with type 2 diabetes. N Engl J Med 360:129–139

    Article  CAS  PubMed  Google Scholar 

  33. Collins TC, Ewing SK, Diem SJ, Taylor BC, Orwoll ES, Cummings SR, Strotmeyer ES, Ensrud KE (2009) Peripheral arterial disease is associated with higher rates of hip bone loss and increased fracture risk in older men. Circulation 119:2305–2312

    Article  PubMed Central  PubMed  Google Scholar 

  34. Sennerby U, Melhus H, Gedeborg R, Byberg L, Garmo H, Ahlbom A, Pedersen NL, Michaëlsson K (2009) Cardiovascular diseases and risk of hip fracture. JAMA 302:1666–1673

    Article  CAS  PubMed  Google Scholar 

  35. Martínez-Laguna D, Soria-Castro A, Carbonell-Abella C, Orozco-López P, Estrada-Laza P, Conesa-García A, Sancho-Almela F, Nogués-Solán X, Díez-Pérez A (2014) P-58: Estudio de incidencia de fracturas por fragilidad registradas en pacientes atendidos en la Atención Primaria de salud. Rev Osteoporos Metab Min 6:36–44

    Google Scholar 

  36. Berry SD, Ngo L, Samelson EJ, Kiel DP (2010) Competing risk of death: an important consideration in studies of older adults. J Am Geriatr Soc 58:783–787

    Article  PubMed Central  PubMed  Google Scholar 

  37. Bolland MJ, Jackson R, Gamble GD, Grey A (2013) Discrepancies in predicted fracture risk in elderly people. BMJ 346:e8669

    Article  PubMed  Google Scholar 

  38. Lind M, Garcia-Rodriguez LA, Booth GL, Cea-Soriano L, Shah BR, Ekeroth G, Lipscombe LL (2013) Mortality trends in patients with and without diabetes in Ontario, Canada and the UK from 1996 to 2009: a population-based study. Diabetologia 56:2601–2608

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

DPA, MKJ, CC, and NKA receive partial support from the Oxford NIHR Musculoskeletal Biomedical Research Unit. DPA is funded by the NIHR Clinician Scientist Award scheme.

Conflicts of interest

Daniel Martinez-Laguna, Cristian Tebe, M Kassim Javaid, Xavier Nogues, Nigel K Arden, Cyrus Cooper, Adolfo Diez-Perez, and Daniel Prieto-Alhambra declare that they have no conflict of interest.

Daniel Prieto-Alhambra has received unrelated research grants from AMGEN and BIOIBERICA S.A.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. Prieto-Alhambra.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 14.2 kb)

ESM 2

(DOCX 13.3 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Martinez-Laguna, D., Tebe, C., Javaid, M.K. et al. Incident type 2 diabetes and hip fracture risk: a population-based matched cohort study. Osteoporos Int 26, 827–833 (2015). https://doi.org/10.1007/s00198-014-2986-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-014-2986-9

Keywords

Navigation