Skip to main content

Advertisement

SpringerLink
Log in

Diabetes mellitus and risk of low-energy fracture: a meta-analysis

  • Review
  • Published:
Aging Clinical and Experimental Research Aims and scope Submit manuscript

Abstract

Background

Low-energy fracture risk is significantly increased in diabetes mellitus, the purpose of this article is to systematically evaluate the association between diabetes mellitus and risk for low-energy fracture.

Methods

We conducted a systematic literature search of Medline, Embase, Science Citation Index, Wiley Online Library database through January 2019. Pooled relative risks (RR) with corresponding 95% confidence intervals (95% CI) were calculated with random-effects model to assess the strength of association.

Results

Thirty-seven studies met the inclusion criteria, which included 3,123,382 participants. The pooled RR of any fracture in people with diabetes mellitus was 1.5 (95% CI 1.3–1.8; P < 0.05). The significant association not found in subgroup analysis of prospective design, follow-up period ≥ 10 year (all P > 0.05). The pooled RR of hip fracture in people with diabetes mellitus was 2.0 (95% CI 1.8–2.3; P < 0.05). In addition, subgroup analysis shown higher risk of hip fracture in type 1 diabetes (RR: 5.3). The pooled RR of vertebral fracture with diabetes mellitus was 1.4 (95% CI 0.9–2.2; P = 0.196). Subgroup analysis by type of diabetes showed that the RR of vertebral fracture for patients with unknown-type diabetes was 2.4 (95% CI 1.4–4.0; P < 0.05). Diabetes mellitus was associated with fractures at other sites, and effect estimates was statically significant.

Conclusions

Diabetes mellitus is an independent risk factor for low-energy fracture, and this relationship is more pronounced in hip fracture.

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
Fig. 5

Similar content being viewed by others

References

  1. Johnell O, Kanis JA (2006) An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos Int 17:1726–1733. https://doi.org/10.1007/s00198-006-0172-4

    Article  CAS  Google Scholar 

  2. Jackuliak P, Payer J (2014) Osteoporosis, fractures, and diabetes. Int J Endocrinol 2014:820615. https://doi.org/10.1155/2014/820615

    Article  CAS  Google Scholar 

  3. Janghorbani M, Van Dam RM, Willett WC et al (2007) Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am J Epidemiol 166:495–505. https://doi.org/10.1093/aje/kwm106

    Article  Google Scholar 

  4. Weber DR, Haynes K, Leonard MB et al (2015) Type 1 diabetes is associated with an increased risk of fracture across the life span: a population-based cohort study using The Health Improvement Network (THIN). Diabetes Care 38:1913–1920. https://doi.org/10.2337/dc15-0783

    Article  Google Scholar 

  5. Starup-Linde J, Hygum K, Harsløf T et al (2018) Indications of increased vertebral fracture risk in patients with type 2 diabetes. J Bone Mineral Res 33:182. https://doi.org/10.1002/jbmr.3323

    Article  Google Scholar 

  6. 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. https://doi.org/10.1007/s00198-006-0253-4

    Article  CAS  Google Scholar 

  7. Siris ES, Miller PD, Barrett-Connor E et al (2001) Identification and fracture outcomes of undiagnosed low bone mineral density in postmenopausal women: results from the National Osteoporosis Risk Assessment. JAMA 286:2815–2822. https://doi.org/10.1001/jama.286.22.2815

    Article  CAS  Google Scholar 

  8. Nicodemus KK, Folsom AR, Iowa Women’s Health S (2001) Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care 24:1192–1197. https://doi.org/10.2337/diacare.24.7.1192

    Article  CAS  Google Scholar 

  9. Starup-Linde J, Lykkeboe S, Gregersen S et al (2016) Bone structure and predictors of fracture in type 1 and type 2 diabetes. J Clin Endocrinol Metab 101:928–36. https://doi.org/10.1210/jc.2015-3882

    Article  CAS  Google Scholar 

  10. Zhu K, Hunter M, James A et al (2017) Discordance between fat mass index and body mass index is associated with reduced bone mineral density in women but not in men: the Busselton Healthy Ageing Study. Osteoporos Int 28:259–268. https://doi.org/10.1007/s00198-016-3710-8

    Article  CAS  Google Scholar 

  11. Mastrandrea LD, Wactawski-Wende J, Donahue RP et al (2008) Young women with type 1 diabetes have lower bone mineral density that persists over time. Diabetes Care 31:1729–1735. https://doi.org/10.2337/dc07-2426

    Article  Google Scholar 

  12. Melton LJ, Leibson CL, Achenbach SJ et al (2008) Fracture risk in type 2 diabetes: update of a population-based study. J Bone Mineral Res 23:1334–1342. https://doi.org/10.1359/jbmr.080323

    Article  Google Scholar 

  13. Starup-Linde J, Gregersen S, Vestergaard P (2016) Associations with fracture in patients with diabetes: a nested case-control study. BMJ Open 6:e009686. https://doi.org/10.1136/bmjopen-2015-009686

    Article  Google Scholar 

  14. Dytfeld J, Michalak M (2017) Type 2 diabetes and risk of low-energy fractures in postmenopausal women: meta-analysis of observational studies. Aging Clin Exp Res 29:301–309. https://doi.org/10.1007/s40520-016-0562-1

    Article  Google Scholar 

  15. Vestergaard P, Rejnmark L, Mosekilde L (2009) Diabetes and its complications and their relationship with risk of fractures in type 1 and 2 diabetes. Calcif Tissue Int 84:45–55. https://doi.org/10.1007/s00223-008-9195-5

    Article  CAS  Google Scholar 

  16. Schwartz AV, Sellmeyer DE, Ensrud KE et al (2001) Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab 86:32–38. https://doi.org/10.1210/jcem.86.1.7139

    Article  CAS  Google Scholar 

  17. Janghorbani M, Feskanich D, Willett WC et al (2006) Prospective study of diabetes and risk of hip fracture: the Nurses’ Health Study. Diabetes Care 29:1573–1578. https://doi.org/10.2337/dc06-0440

    Article  Google Scholar 

  18. Korpelainen R, Korpelainen J, Heikkinen J et al (2003) Lifestyle factors are associated with osteoporosis in lean women but not in normal and overweight women: a population-based cohort study of 1222 women. Osteoporos Int 14:34–43. https://doi.org/10.1007/s00198-002-1319-6

    Article  CAS  Google Scholar 

  19. Ahmed LA, Joakimsen RM, Berntsen GK et al (2006) Diabetes mellitus and the risk of non-vertebral fractures: the Tromsø study. Osteoporos Int 17:495–500. https://doi.org/10.1007/s00198-005-0013-x

    Article  Google Scholar 

  20. Shah C, Shah R, Kinra G et al (2015) Risk of fracture in type 2 diabetes mellitus patients: meta-analysis of observational studies. Value Health 18:A601. https://doi.org/10.1016/j.jval.2015.09.2062

    Article  Google Scholar 

  21. Jia P, Bao L, Chen H et al (2017) Risk of low-energy fracture in type 2 diabetes patients: a meta-analysis of observational studies. Osteoporos Int 28:3113–3121. https://doi.org/10.1007/s00198-017-4183-0

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  23. Wang J, You W, Jing Z et al (2016) Increased risk of vertebral fracture in patients with diabetes: a meta-analysis of cohort studies. Int Orthop 40:1299–1307. https://doi.org/10.1007/s00264-016-3146-y

    Article  Google Scholar 

  24. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. http://www.ohri.ca/programs/clinical_epidemiology/oxford.htm

  25. Stang A (2010) Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25:603–605. https://doi.org/10.1007/s10654-010-9491-z

    Article  Google Scholar 

  26. Pignon J-P, Poynard T (1991) Meta-analysis of clinical trials. Gastroenterol Clin Biol 15:229–238. https://doi.org/10.1002/9781118670767.ch13

    Article  CAS  Google Scholar 

  27. Higgins JPT, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558. https://doi.org/10.1002/sim.1186

    Article  Google Scholar 

  28. Egger M, Davey Smith G, Schneider M et al (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ (Clinical research ed) 315:629–634. https://doi.org/10.1136/bmj.315.7109.629

    Article  CAS  Google Scholar 

  29. Willi C, Bodenmann P, Ghali WA et al (2007) Active smoking and the risk of type 2 diabetes: a systematic review and meta-analysis. JAMA 298:2654–2664. https://doi.org/10.1001/jama.298.22.2654

    Article  CAS  Google Scholar 

  30. Meyer HE, Tverdal A, Falch JA (1993) Risk factors for hip fracture in middle-aged Norwegian women and men. Am J Epidemiol 137:1203–1211. https://doi.org/10.1093/oxfordjournals.aje.a116622

    Article  CAS  Google Scholar 

  31. Forsén L, Meyer HE, Midthjell K et al (1999) Diabetes mellitus and the incidence of hip fracture: results from the Nord-Trondelag Health Survey. Diabetologia. https://doi.org/10.1007/s001250051248

    Article  Google Scholar 

  32. Ivers RQ, Cumming RG, Mitchell P et al (2001) Diabetes and risk of fracture: the Blue Mountains Eye Study. Diabetes Care 24:1198–1203. https://doi.org/10.2337/diacare.24.7.1198

    Article  CAS  Google Scholar 

  33. Ottenbacher KJ, Ostir GV, Peek MK et al (2002) Diabetes mellitus as a risk factor for hip fracture in Mexican American older adults. J Gerontol Ser A Biol sci Med Sci 57:M648–M653. https://doi.org/10.1093/gerona/57.10.m648

    Article  Google Scholar 

  34. Strotmeyer ES, Cauley JA, Schwartz AV et al (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 165:1612–1617. https://doi.org/10.1001/archinte.165.14.1612

    Article  Google Scholar 

  35. 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 48:1292–1299. https://doi.org/10.1007/s00125-005-1786-3

    Article  CAS  Google Scholar 

  36. Miao J, Brismar K, Nyrén O et al (2005) Elevated hip fracture risk in type 1 diabetic patients: a population-based cohort study in Sweden. Diabetes Care 28:2850–2855. https://doi.org/10.2337/diacare.28.12.2850

    Article  Google Scholar 

  37. Gerdhem P, Isaksson A, Akesson K et al (2005) Increased bone density and decreased bone turnover, but no evident alteration of fracture susceptibility in elderly women with diabetes mellitus. Osteoporos Int 16:1506–1512. https://doi.org/10.1007/s00198-005-1877-5

    Article  CAS  Google Scholar 

  38. de Liefde II, van der Klift M, de Laet CEDH et al (2005) Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam Study. Osteoporos Int 16:1713–1720. https://doi.org/10.1007/s00198-005-1909-1

    Article  Google Scholar 

  39. Holmberg AH, Johnell O, Nilsson PM et al (2006) Risk factors for fragility fracture in middle age. A prospective population-based study of 33,000 men and women. Osteoporos Int 17:1065–1077. https://doi.org/10.1007/s00198-006-0137-7

    Article  CAS  Google Scholar 

  40. Dobnig H, Piswanger-Sölkner JC, Roth M et al (2006) Type 2 diabetes mellitus in nursing home patients: effects on bone turnover, bone mass, and fracture risk. J Clin Endocrinol Metab 91:3355–3363. https://doi.org/10.1210/jc.2006-0460

    Article  CAS  Google Scholar 

  41. Bonds DE, Larson JC, Schwartz AV et al (2006) Risk of fracture in women with type 2 diabetes: the Women’s Health Initiative Observational Study. J Clin Endocrinol Metab 91:3404–3410. https://doi.org/10.1210/jc.2006-0614

    Article  CAS  Google Scholar 

  42. Lipscombe LL, Jamal SA, Booth GL et al (2007) The risk of hip fractures in older individuals with diabetes: a population-based study. Diabetes Care 30:835–841. https://doi.org/10.2337/dc06-1851

    Article  Google Scholar 

  43. Leslie WD, Lix LM, Prior HJ et al (2007) Biphasic fracture risk in diabetes: a population-based study. Bone 40:1595–1601. https://doi.org/10.1016/j.bone.2007.02.021

    Article  Google Scholar 

  44. Chen H-F, Ho C-A, Li C-Y (2008) Increased risks of hip fracture in diabetic patients of Taiwan: a population-based study. Diabetes Care 31:75–80. https://doi.org/10.2337/dc07-1072

    Article  CAS  Google Scholar 

  45. Sosa M, Saavedra P, Jódar E et al (2009) Bone mineral density and risk of fractures in aging, obese post-menopausal women with type 2 diabetes. The GIUMO Study. Aging Clin Exp Res 21:27–32. https://doi.org/10.1007/bf03324895

    Article  Google Scholar 

  46. Yamamoto M, Yamaguchi T, Yamauchi M et al (2009) Diabetic patients have an increased risk of vertebral fractures independent of BMD or diabetic complications. J Bone Mineral Res 24:702–709. https://doi.org/10.1359/jbmr.081207

    Article  CAS  Google Scholar 

  47. Koh W-P, Wang R, Ang L-W et al (2010) Diabetes and risk of hip fracture in the Singapore Chinese Health Study. Diabetes Care 33:1766–1770. https://doi.org/10.2337/dc10-0067

    Article  Google Scholar 

  48. Fraser L-A, Pritchard J, Ioannidis G et al (2011) Clinical risk factors for fracture in diabetes: a matched cohort analysis. J Clin Densitom 14:416–421. https://doi.org/10.1016/j.jocd.2011.06.007

    Article  Google Scholar 

  49. Strotmeyer ES, Kamineni A, Cauley JA et al (2011) Potential explanatory factors for higher incident hip fracture risk in older diabetic adults. Curr Gerontol Geriatr Res. 2011:979270. https://doi.org/10.1155/2011/979270

    Article  Google Scholar 

  50. Jung JK, Kim HJ, Lee HK et al (2012) Fracture incidence and risk of osteoporosis in female type 2 diabetic patients in Korea. Diabetes Metab J 36:144–150. https://doi.org/10.4093/dmj.2012.36.2.144

    Article  Google Scholar 

  51. Giangregorio LM, Leslie WD, Lix LM et al (2012) FRAX underestimates fracture risk in patients with diabetes. J Bone Mineral Res 27:301–308. https://doi.org/10.1002/jbmr.556

    Article  Google Scholar 

  52. Kilpadi KL, Eldabaje R, Schmitz JE et al (2014) Type 2 diabetes is associated with vertebral fractures in a sample of clinic- and hospital-based Latinos. J Immigr Minor Health 16:440–449. https://doi.org/10.1007/s10903-013-9833-5

    Article  CAS  Google Scholar 

  53. Leslie WD, Aubry-Rozier B, Lamy O et al (2013) TBS (trabecular bone score) and diabetes-related fracture risk. J Clin Endocrinol Metab 98:602–609. https://doi.org/10.1210/jc.2012-3118

    Article  CAS  Google Scholar 

  54. Oei L, Zillikens MC, Dehghan A 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 36:1619–1628. https://doi.org/10.2337/dc12-1188

    Article  CAS  Google Scholar 

  55. Hothersall EJ, Livingstone SJ, Looker HC et al (2014) Contemporary risk of hip fracture in type 1 and type 2 diabetes: a national registry study from Scotland. J Bone Mineral Res 29:1054–1060. https://doi.org/10.1002/jbmr.2118

    Article  Google Scholar 

  56. Liao C-C, Lin C-S, Shih C-C et al (2017) Erratum. Increased risk of fracture and postfracture adverse events in patients with diabetes: two nationwide population-based retrospective cohort studies. Diabetes Care 2014;37:2246–2252. Diabetes Care 40:1134. https://doi.org/10.2337/dc17-er08c

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  58. Majumdar SR, Leslie WD, Lix LM et al (2016) Longer duration of diabetes strongly impacts fracture risk assessment: the Manitoba BMD cohort. J Clin Endocrinol Metab 101:4489–4496. https://doi.org/10.1210/jc.2016-2569

    Article  CAS  Google Scholar 

  59. Looker AC, Eberhardt MS, Saydah SH (2016) Diabetes and fracture risk in older U.S. adults. Bone 82:9–15. https://doi.org/10.1016/j.bone.2014.12.008

    Article  Google Scholar 

  60. Hamilton EJ, Davis WA, Bruce DG et al (2017) Risk and associates of incident hip fracture in type 1 diabetes: the Fremantle Diabetes Study. Diabetes Res Clin Pract 134:153–160. https://doi.org/10.1016/j.diabres.2017.10.011

    Article  Google Scholar 

  61. Holm JP, Jensen T, Hyldstrup L et al (2018) Fracture risk in women with type II diabetes. Results from a historical cohort with fracture follow-up. Endocrine 60:151–158. https://doi.org/10.1007/s12020-018-1564-x

    Article  CAS  Google Scholar 

  62. Furtado S, Rodrigues A, Dias S et al (2019) Self-reported low-energy fractures and associated risk factors in people with diabetes: a national population-based study. Diabetes Res Clin Pract 147:93–101. https://doi.org/10.1016/j.diabres.2018.11.015

    Article  Google Scholar 

  63. Räkel A, Sheehy O, Rahme E et al (2008) Osteoporosis among patients with type 1 and type 2 diabetes. Diabetes Metab 34:193–205. https://doi.org/10.1016/j.diabet.2007.10.008

    Article  Google Scholar 

  64. Sherif E, Aziz M, Elbarbary N et al (2011) Insulin-like growth factor-1 in correlation with bone mineral density among Egyptian adolescents with type 1 diabetes mellitus. Int J Diabetes Dev Ctries 31:104–112. https://doi.org/10.1007/s13410-011-0023-5

    Article  CAS  Google Scholar 

  65. Gilmour J, Colquhoun A, Wu W et al (2018) Type 1 diabetes and bone microarchitecture assessment with trabecular bone score (TBS): a descriptive study. J Clin Densitom. https://doi.org/10.1016/j.jocd.2017.10.022

    Article  Google Scholar 

  66. Starup-Linde J, Vestergaard P (2016) Biochemical bone turnover markers in diabetes mellitus—a systematic review. Bone 82:69–78. https://doi.org/10.1016/j.bone.2015.02.019

    Article  CAS  Google Scholar 

  67. World Health Organization (2019) Classification of diabetes mellitus. World Health Organization. https://apps.who.int/iris/handle/10665/325182

  68. Thrailkill KM, Lumpkin CK, Bunn RC et al (2005) Is insulin an anabolic agent in bone? Dissecting the diabetic bone for clues. Am J Physiol Endocrinol Metab 289:E735–E745. https://doi.org/10.1152/ajpendo.00159.2005

    Article  CAS  Google Scholar 

  69. Starup-Linde J (2013) Diabetes, biochemical markers of bone turnover, diabetes control, and bone. Front Endocrinol 4:21. https://doi.org/10.3389/fendo.2013.00021

    Article  Google Scholar 

  70. Poiana C, Capatina C (2017) Fracture risk assessment in patients with diabetes mellitus. J Clin Densitom 20:432–443. https://doi.org/10.1016/j.jocd.2017.06.011

    Article  Google Scholar 

  71. Ganeko K, Masaki C, Shibata Y et al (2015) Bone aging by advanced glycation end products: a multiscale mechanical analysis. J Dent Res 94:1684–1690. https://doi.org/10.1177/0022034515602214

    Article  CAS  Google Scholar 

  72. Saito M, Marumo K (2010) Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporos Int 21:195–214. https://doi.org/10.1007/s00198-009-1066-z

    Article  CAS  Google Scholar 

  73. Makita Z, Radoff S, Rayfield EJ et al (1991) Advanced glycosylation end products in patients with diabetic nephropathy. N Engl J Med 325:836–842. https://doi.org/10.1056/nejm199109193251202

    Article  CAS  Google Scholar 

  74. Yamamoto M, Yamaguchi T, Yamauchi M et al (2008) Serum pentosidine levels are positively associated with the presence of vertebral fractures in postmenopausal women with type 2 diabetes. J Clin Endocrinol Metab. https://doi.org/10.1210/jc.2007-1270

    Article  Google Scholar 

  75. Gaudio A, Privitera F, Battaglia K et al (2012) Sclerostin levels associated with inhibition of the Wnt/b-catenin signaling and reduced bone turnover in type 2 diabetes mellitus. J Clin Endocrinol Metab 97:3744–3750. https://doi.org/10.1210/jc.2012-1901

    Article  CAS  Google Scholar 

  76. Moayeri A, Mohamadpour M, Mousavi SF et al (2017) Fracture risk in patients with type 2 diabetes mellitus and possible risk factors: a systematic review and meta-analysis. Ther Clin Risk Manag 13:455–468. https://doi.org/10.2147/tcrm.s131945

    Article  Google Scholar 

  77. Shah VN, Shah CS, Snell-Bergeon JK (2015) Type 1 diabetes and risk of fracture: meta-analysis and review of the literature. Diabet Med 32:1134–1142. https://doi.org/10.1111/dme.12734

    Article  CAS  Google Scholar 

  78. Valderrábano RJ, Linares MI (2018) Diabetes mellitus and bone health: epidemiology, etiology and implications for fracture risk stratification. Clin Diabetes Endocrinol 4:9. https://doi.org/10.1186/s40842-018-0060-9

    Article  Google Scholar 

  79. Dheon P, Shah VN (2014) Type 1 diabetes and osteoporosis: a review of literature. Indian J Endocrinol Metab 18:159–165. https://doi.org/10.4103/2230-8210.129105

    Article  Google Scholar 

  80. Campos Pastor MM, López-Ibarra PJ, Escobar-Jiménez F et al (2000) Intensive insulin therapy and bone mineral density in type 1 diabetes mellitus: a prospective study. Osteoporos Int 11:455–459. https://doi.org/10.1007/s001980070114

    Article  CAS  Google Scholar 

  81. Zhukouskaya VV, Eller-Vainicher C, Vadzianava VV et al (2013) Prevalence of morphometric vertebral fractures in patients with type 1 diabetes. Diabetes Care 36:1635–1640. https://doi.org/10.2337/dc12-1355

    Article  CAS  Google Scholar 

  82. Herrera-Rangel AB, Aranda-Moreno C, Mantilla-Ochoa T et al (2015) Influence of the body mass index on the occurrence of falls in patients with type 2 diabetes mellitus. Obes Res Clin Pract 9:522–526. https://doi.org/10.1016/j.orcp.2015.02.006

    Article  Google Scholar 

  83. Armamento-Villareal R, Sadler C, Napoli N et al (2012) Weight loss in obese older adults increases serum sclerostin and impairs hip geometry but both are prevented by exercise training. J Bone Miner Res 27:1215–1221

    Article  CAS  Google Scholar 

  84. Napoli N, Shah K, Waters DL et al (2014) Effect of weight loss, exercise, or both on cognition and quality of life in obese older adults. Am J Clin Nutr 100:189–198

    Article  CAS  Google Scholar 

  85. Hurskainen AR, Virtanen JK, Tuomainen TP et al (2012) Association of serum 25-hydroxyvitamin D with type 2 diabetes and markers of insulin resistance in a general older population in Finland. Diabetes Metab Res Rev 28:418–423. https://doi.org/10.1002/dmrr.2286

    Article  CAS  Google Scholar 

  86. Zhu ZN, Jiang YF, Ding T (2014) Risk of fracture with thiazolidinediones: an updated meta-analysis of randomized clinical trials. Bone 68:115–123. https://doi.org/10.1016/j.bone.2014.08.010

    Article  CAS  Google Scholar 

Download references

Funding

None.

Author information

Authors and Affiliations

  1. Department of Endocrinology, Cangzhou People’s Hospital, No. 7 Qingchi North Avenue, Cangzhou, 061001, China

    Jing Bai & Qian Gao

  2. Department of Orthopedics, Cangzhou People’s Hospital, No. 7 Qingchi North Avenue, Cangzhou, 061001, China

    Chen Wang & Jia Dai

Authors
  1. Jing Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qian Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chen Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jia Dai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jia Dai.

Ethics declarations

Conflict of interest

All authors declare that they have no competing interests.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors.

Informed consent

For this type of study inform consent is not required.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bai, J., Gao, Q., Wang, C. et al. Diabetes mellitus and risk of low-energy fracture: a meta-analysis. Aging Clin Exp Res 32, 2173–2186 (2020). https://doi.org/10.1007/s40520-019-01417-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40520-019-01417-x

Keywords

Search

Navigation