Advertisement

Discordant pattern of peripheral fractures in diabetes: a meta-analysis on the risk of wrist and ankle fractures

  • T. Vilaca
  • J. Walsh
  • R. Eastell
Original Article

Abstract

Summary

To clarify if the peripheral microarchitectural abnormalities described in diabetics have clinical consequences, we evaluated the risk of wrist and ankle fractures. The meta-analysis resulted in an increase in the risk of ankle fractures and a decrease in wrist fractures risk, suggesting that microarchitecture may not be the major fracture determinant.

Introduction

There is evidence for an increase in the risk of hip fractures in diabetes (both in type 1 and 2), but the risk is not established for other skeletal sites. Microarchitecture evaluations have reported a decrease in volumetric bone mineral density and an increase in cortical porosity at the radius and tibia. To investigate if there is a clinical consequence for these microarchitectural abnormalities, we performed a systematic review and meta-analysis on the risk of ankle and wrist fractures in diabetes.

Methods

Medline and Embase were searched using the terms ‘diabetes mellitus’, ‘fracture’, ‘ankle’, ‘radius’ and ‘wrist’. Relative risks and 95% confidence intervals were calculated using random effects model.

Results

For ankle fractures, six studies were selected including 2,137,223 participants and 15,395 fractures. For wrist fractures, 10 studies were eligible with 2,773,222 subjects and 39,738 fractures. The studies included men and women, ages 20 to 109 years for the wrist and 27 to 109 years for the ankle. The vast majority of subjects had type 2 diabetes.

Diabetes was associated with an increase in the risk of ankle fractures (RR 1.30 95%CI 1.15–1.48) and a decrease in wrist fractures (RR 0.85 95%CI 0.77-0.95). In the studies that reported body mass index (BMI), the mean values were 10% higher in the diabetic groups than controls.

Conclusion

The risk of fractures is increased in diabetes at the ankle and decreased at the wrist. The same pattern is observed in obesity. Although bone microarchitectural features are different in obesity and diabetes, the epidemiology of peripheral fractures is similar in both diseases suggesting that microarchitecture may not be the major determinant of peripheral fractures in these populations.

Keywords

Ankle fractures Bone Diabetes Wrist fractures 

Notes

Compliance with ethical standards

Conflicts of interest

None.

Supplementary material

198_2018_4717_MOESM1_ESM.docx (14 kb)
ESM 1 (DOCX 13 kb)

References

  1. 1.
    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(4):427–444CrossRefPubMedCentralGoogle Scholar
  2. 2.
    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(5):495–505CrossRefPubMedCentralGoogle Scholar
  3. 3.
    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(9):3404–3410CrossRefPubMedCentralGoogle Scholar
  4. 4.
    Napoli N, Strotmeyer ES, Ensrud KE, Sellmeyer DE, Bauer DC, Hoffman AR, Dam TTL, Barrett-Connor E, Palermo L, Orwoll ES, Cummings SR, Black DM, Schwartz AV (2014) Fracture risk in diabetic elderly men: the MrOS study. Diabetologia 57(10):2057–2065CrossRefPubMedCentralGoogle Scholar
  5. 5.
    Strotmeyer ES, Cauley JA, Schwartz AV, Nevitt MC, Resnick HE, Bauer DC, Tylavsky FA, de Rekeneire N, Harris TB, Newman AB (2005) Nontraumatic fracture risk with diabetes mellitus and impaired fasting glucose in older white and black adults: the health, aging, and body composition study. Arch Intern Med 165(14):1612–1617CrossRefPubMedCentralGoogle Scholar
  6. 6.
    Petit MA, Paudel ML, Taylor BC, Hughes JM, Strotmeyer ES, Schwartz AV, Cauley JA, Zmuda JM, Hoffman AR, Ensrud KE, Osteoporotic Fractures in Men (MrOs) Study Group (2010) Bone mass and strength in older men with type 2 diabetes: the osteoporotic fractures in men study. J Bone Miner Res 25(2):285–291CrossRefPubMedCentralGoogle Scholar
  7. 7.
    Fan Y, Wei F, Lang Y, Liu Y (2015) Diabetes mellitus and risk of hip fractures: a meta-analysis. Osteoporos IntGoogle Scholar
  8. 8.
    Dytfeld J, Michalak M (2016) Type 2 diabetes and risk of low-energy fractures in postmenopausal women: meta-analysis of observational studies. Aging Clin Exp ResGoogle Scholar
  9. 9.
    Shah VN, Shah CS, Snell-Bergeon JK (2015) Type 1 diabetes and risk of fracture: meta-analysis and review of the literature. Diabet Med 32(9):1134–1142CrossRefPubMedCentralGoogle Scholar
  10. 10.
    Pan H, Wu N, Yang T, He W (2014) Association between bone mineral density and type 1 diabetes mellitus: a meta-analysis of cross-sectional studies. Diabetes Metab Res Rev 30(7):531–542CrossRefPubMedCentralGoogle Scholar
  11. 11.
    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(6):1619–1628CrossRefPubMedCentralGoogle Scholar
  12. 12.
    Schwartz AV, Vittinghoff E, Bauer DC, Hillier TA, Strotmeyer ES, Ensrud KE, Donaldson MG, Cauley JA, Harris TB, Koster A, Womack CR, Palermo L, Black DM, Study of Osteoporotic Fractures (SOF) Research Group, Osteoporotic Fractures in Men (MrOS) Research Group, Health, Aging, and Body Composition (Health ABC) Research Group (2011) Association of BMD and FRAX score with risk of fracture in older adults with type 2 diabetes. JAMA 305(21):2184–2192CrossRefPubMedCentralGoogle Scholar
  13. 13.
    Ogurtsova K, da Rocha Fernandes JD, Huang Y, Linnenkamp U, Guariguata L, Cho NH, Cavan D, Shaw JE, Makaroff LE (2017) IDF diabetes atlas: global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Res Clin Pract 128:40–50CrossRefGoogle Scholar
  14. 14.
    Johnell O, Kanis JA (2006) An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos Int 17(12):1726–1733CrossRefPubMedCentralGoogle Scholar
  15. 15.
    Walsh JS, Vilaca T (2017) Obesity, type 2 diabetes and bone in adults. Calcif Tissue Int 100(5):528–535CrossRefPubMedCentralGoogle Scholar
  16. 16.
    Shanbhogue VV, Hansen S, Frost M, Jorgensen NR, Hermann AP, Henriksen JE et al (2016) Compromised cortical bone compartment in type 2 diabetes mellitus patients with microvascular disease. Eur J Endocrinol 174(2):115–124CrossRefPubMedCentralGoogle Scholar
  17. 17.
    Shanbhogue VV, Hansen S, Frost M, Jorgensen NR, Hermann AP, Henriksen JE et al (2015) Bone geometry, volumetric density, microarchitecture, and estimated bone strength assessed by HR-pQCT in adult patients with type 1 diabetes mellitus. J Bone Miner ResGoogle Scholar
  18. 18.
    Burghardt AJ, Issever AS, Schwartz AV, Davis KA, Masharani U, Majumdar S, Link TM (2010) High-resolution peripheral quantitative computed tomographic imaging of cortical and trabecular bone microarchitecture in patients with type 2 diabetes mellitus. J Clin Endocrinol Metab 95(11):5045–5055CrossRefPubMedCentralGoogle Scholar
  19. 19.
    Patsch JM, Burghardt AJ, Yap SP, Baum T, Schwartz AV, Joseph GB, Link TM (2013) Increased cortical porosity in type 2 diabetic postmenopausal women with fragility fractures. J Bone Miner Res 28(2):313–324CrossRefPubMedCentralGoogle Scholar
  20. 20.
    Paccou J, Ward KA, Jameson KA, Dennison EM, Cooper C, Edwards MH (2016) Bone microarchitecture in men and women with diabetes: the importance of cortical porosity. Calcif Tissue Int 98(5):465–473CrossRefPubMedCentralGoogle Scholar
  21. 21.
    PRISMA-TRANSPARENT REPORTING of SYSTEMATIC REVIEWS and META-ANALYSES http://www.prisma-statement.org2016 [PRISMA is an evidence-based minimum set of items for reporting in systematic reviews and meta-analyses.]
  22. 22.
    Wells GA, Shea B, O'Connell D, Peterson J, Welch V, Losos M, et al The Newcastle-Ottawas scale (NOS) for assessing the quality of non randomised studies in meta-analysis http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp2014
  23. 23.
    Greenland S (1987) Quantitative methods in the review of epidemiologic literature. Epidemiol Rev 9:1–30CrossRefGoogle Scholar
  24. 24.
    Ivers RQ, Cumming RG, Mitchell P, Peduto AJ (2001) Diabetes and risk of fracture: the Blue Mountains Eye Study. Diabetes Care 24(7):1198–1203CrossRefPubMedCentralGoogle Scholar
  25. 25.
    Schwartz AV, Sellmeyer DE, Ensrud KE, Cauley JA, Tabor HK, Schreiner PJ, Jamal SA, Black DM, Cummings SR, Study of Osteoporotic Features Research Group (2001) Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab 86(1):32–38CrossRefPubMedCentralGoogle Scholar
  26. 26.
    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(7):1065–1077CrossRefPubMedCentralGoogle Scholar
  27. 27.
    Taylor AJ, Gary LC, Arora T, Becker DJ, Curtis JR, Kilgore ML, Morrisey MA, Saag KG, Matthews R, Yun H, Smith W, Delzell E (2011) Clinical and demographic factors associated with fractures among older Americans. Osteoporos Int 22(4):1263–1274CrossRefPubMedCentralGoogle Scholar
  28. 28.
    Pritchard JM, Giangregorio LM, Ioannidis G, Papaioannou A, Adachi JD, Leslie WD (2012) Ankle fractures do not predict osteoporotic fractures in women with or without diabetes. Osteoporos Int 23(3):957–962CrossRefPubMedCentralGoogle Scholar
  29. 29.
    Wallander M, Axelsson KF, Nilsson AG, Lundh D, Lorentzon M (2017) Type 2 diabetes and risk of hip fractures and non-skeletal fall injuries in the elderly: a study from the fractures and fall injuries in the elderly cohort (FRAILCO). J Bone Miner Res 32(3):449–460CrossRefPubMedCentralGoogle Scholar
  30. 30.
    Gerdhem P, Isaksson A, Akesson K, Obrant KJ (2005) Increased bone density and decreased bone turnover, but no evident alteration of fracture susceptibility in elderly women with diabetes mellitus. Osteoporos Int 16(12):1506–1512CrossRefPubMedCentralGoogle Scholar
  31. 31.
    de L II, van der Klift M, de Laet CE, van Daele PL, Hofman A, Pols HA (2005) Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam study. Osteoporos Int 16(12):1713–1720CrossRefGoogle Scholar
  32. 32.
    Leslie WD, Derksen SA, Metge C, Lix LM, Salamon EA, Steiman PW et al (2005) Demographic risk factors for fracture in First Nations people. Can J Public Health 96(Suppl 1):S45–S50PubMedPubMedCentralGoogle Scholar
  33. 33.
    Harness NG, Funahashi T, Dell R, Adams AL, Burchette R, Chen X, Greene D (2012) Distal radius fracture risk reduction with a comprehensive osteoporosis management program. J Hand Surg Am 37(8):1543–1549CrossRefPubMedCentralGoogle Scholar
  34. 34.
    Keegan TH, Kelsey JL, Sidney S, Quesenberry CP Jr (2002) Foot problems as risk factors of fractures. Am J Epidemiol 155(10):926–931CrossRefPubMedCentralGoogle Scholar
  35. 35.
    Greenfield DM, Eastell R (2001) Risk factors for ankle fracture. Osteoporos Int 12(2):97–103CrossRefPubMedCentralGoogle Scholar
  36. 36.
    Giannini S, Chiarello E, Persiani V, Luciani D, Cadossi M, Tedesco G (2013) Ankle fractures in elderly patients. Aging Clin Exp Res 25(Suppl 1):S77–S79CrossRefPubMedCentralGoogle Scholar
  37. 37.
    Stein EM, Liu XS, Nickolas TL, Cohen A, Thomas V, McMahon DJ et al (2011) Abnormal microarchitecture and stiffness in postmenopausal women with ankle fractures. J Clin Endocrinol Metab 96(7):2041–2048CrossRefPubMedCentralGoogle Scholar
  38. 38.
    Nellans KW, Kowalski E, Chung KC (2012) The epidemiology of distal radius fractures. Hand Clin 28(2):113–125CrossRefPubMedCentralGoogle Scholar
  39. 39.
    Melton LJ 3rd, Christen D, Riggs BL, Achenbach SJ, Muller R, van Lenthe GH et al (2010) Assessing forearm fracture risk in postmenopausal women. Osteoporos Int 21(7):1161–1169CrossRefPubMedCentralGoogle Scholar
  40. 40.
    Caffarelli C, Alessi C, Nuti R, Gonnelli S (2014) Divergent effects of obesity on fragility fractures. Clin Interv Aging 9:1629–1636PubMedPubMedCentralGoogle Scholar
  41. 41.
    Evans AL, Paggiosi MA, Eastell R, Walsh JS (2015) Bone density, microstructure and strength in obese and normal weight men and women in younger and older adulthood. J Bone Miner Res 30(5):920–928CrossRefPubMedCentralGoogle Scholar
  42. 42.
    Conway B, Miller RG, Costacou T, Fried L, Kelsey S, Evans RW, Orchard TJ (2010) Temporal patterns in overweight and obesity in type 1 diabetes. Diabet Med 27(4):398–404CrossRefPubMedCentralGoogle Scholar
  43. 43.
    Nilsson AG, Sundh D, Johansson L, Nilsson M, Mellstrom D, Rudang R et al (2017) Type 2 diabetes mellitus is associated with better bone microarchitecture but lower bone material strength and poorer physical function in elderly women: a population-based study. J Bone Miner Res 32(5):1062–1071CrossRefPubMedCentralGoogle Scholar
  44. 44.
    Samelson EJ, Demissie S, Cupples LA, Zhang X, Xu H, Liu CT, Boyd SK, McLean RR, Broe KE, Kiel DP, Bouxsein ML (2018) Diabetes and deficits in cortical bone density, microarchitecture, and bone size: Framingham HR-pQCT study. J Bone Miner Res 33(1):54–62CrossRefPubMedCentralGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2018

Authors and Affiliations

  1. 1.Academic Unit of Bone MetabolismUniversity of SheffieldSheffieldUK
  2. 2.Metabolic Bone CentreNorthern General HospitalSheffieldEngland

Personalised recommendations