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Comparison of fracture risk between type 1 and type 2 diabetes: a comprehensive real-world data

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Abstract

Summary

Population-based cohort study of 6,548,784 Korean subjects demonstrates that the risk of fracture was higher in patients with diabetes than in nondiabetic subjects. Furthermore, patients with type 1 diabetes were associated with a higher risk of fracture than patients with type 2 diabetes for all measurement sites.

Introduction

Diabetes mellitus is associated with increased fracture risk. Although the pathophysiologic effect on bone metabolism differs according to the type of diabetes, a higher risk of fracture in patients with diabetes than in nondiabetic patients has been consistently demonstrated. Considering the ever-increasing number of patients with diabetes, we aimed to provide updated information on whether this phenomenon remains valid in real-world settings by using large-scale population datasets.

Methods

We conducted a retrospective longitudinal study using data from the Korean National Health Insurance Service dataset of preventive health check-ups between January 2009 and December 2016. The hazard ratios were calculated for any fracture, vertebral fracture, and hip fracture and were analyzed according to the presence and type of diabetes. Among 10,585,818 subjects, 6,548,784 were eligible for the analysis (2418 patients with type 1 diabetes mellitus [T1DM] and 506,208 patients with type 2 diabetes mellitus [T2DM]).

Results

The mean follow-up duration (in years) was 7.0 ± 1.3 for subjects without diabetes, 6.4 ± 2.0 for those with T1DM, and 6.7 ± 1.7 for T2DM. Patients with T1DM had a higher incidence rate for all types of fractures per 1000 person-years. The fully adjusted hazard ratios (HRs) for any fracture, vertebral fracture, and hip fracture were higher in T1DM than in T2DM (1.37 [95% confidence interval (CI): 1.23–1.52] for any fracture, 1.33 [95% CI: 1.09–1.63] for vertebral fracture, and 1.99 [95% CI: 1.56–2.53] for hip fracture).

Conclusions

In this large-scale population analysis, diabetes was associated with a higher risk of all types of fractures. Patients with T1DM had a higher risk of fracture than those with T2DM for all measurement sites, and hip fractures had the highest risk. Therefore, fracture prevention training for patients with diabetes is advisable.

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Data availability

The datasets used and analyzed during the study are available from the corresponding author on reasonable request.

References

  1. Whiting DR, Guariguata L, Weil C, Shaw JJDr, Practice C (2011) IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. 94 (3):311-321

  2. Kweon S, Kim Y, Jang MJ, Kim Y, Kim K, Choi S, Chun C, Khang YH, Oh K (2014) Data resource profile: the Korea National Health and Nutrition Examination Survey (KNHANES). Int J Epidemiol 43(1):69–77. https://doi.org/10.1093/ije/dyt228

    Article  PubMed  PubMed Central  Google Scholar 

  3. Bae JC (2018) Trends of diabetes epidemic in Korea. Diabetes Metab J 42(5):377–379. https://doi.org/10.4093/dmj.2018.0194

    Article  PubMed  PubMed Central  Google Scholar 

  4. 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):1612–1617. https://doi.org/10.1001/archinte.165.14.1612

    Article  PubMed  Google Scholar 

  5. Poiana C, Capatina C (2017) Fracture risk assessment in patients with diabetes mellitus. J Clin Densitom 20(3):432–443. https://doi.org/10.1016/j.jocd.2017.06.011

  6. Napoli N, Chandran M, Pierroz DD, Abrahamsen B, Schwartz AV, Ferrari SL (2017) Mechanisms of diabetes mellitus-induced bone fragility. Nat Rev Endocrinol 13(4):208–219. https://doi.org/10.1038/nrendo.2016.153

    Article  CAS  PubMed  Google Scholar 

  7. Yamamoto M, Yamaguchi T, Yamauchi M, Kaji H, Sugimoto T (2009) Diabetic patients have an increased risk of vertebral fractures independent of BMD or diabetic complications. J Bone Miner Res 24(4):702–709. https://doi.org/10.1359/jbmr.081207

  8. Schwartz AV, Sellmeyer DE, Ensrud KE, Cauley JA, Tabor HK, Schreiner PJ, Jamal SA, Black DM, Cummings SR (2001) Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab 86(1):32–38. https://doi.org/10.1210/jcem.86.1.7139

    Article  CAS  PubMed  Google Scholar 

  9. Miao J, Brismar K, Nyrén 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(12):2850–2855. https://doi.org/10.2337/diacare.28.12.2850

    Article  PubMed  Google Scholar 

  10. Rathmann W, Kostev K (2015) Fracture risk in patients with newly diagnosed type 2 diabetes: a retrospective database analysis in primary care. J Diabetes Complicat 29(6):766–770. https://doi.org/10.1016/j.jdiacomp.2015.05.007

    Article  Google Scholar 

  11. Neumann T, Sämann A, Lodes S, Kästner B, Franke S, Kiehntopf M, Hemmelmann C, Lehmann T, Müller UA, Hein G, Wolf G (2011) Glycaemic control is positively associated with prevalent fractures but not with bone mineral density in patients with type 1 diabetes. Diabet Med 28(7):872–875. https://doi.org/10.1111/j.1464-5491.2011.03286.x

  12. Shanbhogue VV, Hansen S, Frost M, Jørgensen NR, Hermann AP, Henriksen JE, Brixen K (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 Res 30(12):2188–2199. https://doi.org/10.1002/jbmr.2573

  13. Leslie WD, Rubin MR, Schwartz AV, Kanis JA (2012) Type 2 diabetes and bone. J Bone Miner Res 27(11):2231–2237. https://doi.org/10.1002/jbmr.1759

  14. 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):5045–5055. https://doi.org/10.1210/jc.2010-0226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. 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(7):1292–1299. https://doi.org/10.1007/s00125-005-1786-3

    Article  CAS  PubMed  Google Scholar 

  16. 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):427–444. https://doi.org/10.1007/s00198-006-0253-4

  17. 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):495–505. https://doi.org/10.1093/aje/kwm106

    Article  PubMed  Google Scholar 

  18. 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(2):301–309. https://doi.org/10.1007/s40520-016-0562-1

    Article  PubMed  Google Scholar 

  19. Kim MK, Han K, Kim HS, Park YM, Kwon HS, Yoon KH, Lee SH (2017) Cholesterol variability and the risk of mortality, myocardial infarction, and stroke: a nationwide population-based study. Eur Heart J 38(48):3560–3566. https://doi.org/10.1093/eurheartj/ehx585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Lee YH, Han K, Ko SH, Ko KS, Lee KU (2016) Data analytic process of a nationwide population-based study using national health information database established by National Health Insurance Service. Diabetes Metab J 40(1):79–82. https://doi.org/10.4093/dmj.2016.40.1.79

    Article  PubMed  PubMed Central  Google Scholar 

  21. Cheol Seong S, Kim YY, Khang YH, Heon Park J, Kang HJ, Lee H, Do CH, Song JS, Hyon Bang J, Ha S, Lee EJ, Ae Shin S (2017) Data resource profile: the national health information database of the National Health Insurance Service in South Korea. Int J Epidemiol 46(3):799–800. https://doi.org/10.1093/ije/dyw253

    Article  PubMed  Google Scholar 

  22. Lee YB, Han K, Kim B, Jun JE, Lee SE, Ahn J, Kim G, Jin SM, Kim JH (2019) Risk of end-stage renal disease from chronic kidney disease defined by decreased glomerular filtration rate in type 1 diabetes: a comparison with type 2 diabetes and the effect of metabolic syndrome. Diabetes Metab Res Rev 35(8):e3197. https://doi.org/10.1002/dmrr.3197

    Article  PubMed  Google Scholar 

  23. Lee YB, Han K, Kim B, Jin SM, Lee SE, Jun JE, Ahn J, Kim G, Kim JH (2019) High proportion of adult cases and prevalence of metabolic syndrome in type 1 diabetes mellitus population in Korea: a nationwide study. Diabetes Metab J 43(1):76–89. https://doi.org/10.4093/dmj.2018.0048

    Article  PubMed  Google Scholar 

  24. Noh J, Han KD, Ko SH, Ko KS, Park CY (2017) Trends in the pervasiveness of type 2 diabetes, impaired fasting glucose and co-morbidities during an 8-year-follow-up of nationwide Korean population. Sci Rep 7:46656. https://doi.org/10.1038/srep46656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Agarwal DP (2002) Cardioprotective effects of light-moderate consumption of alcohol: a review of putative mechanisms. Alcohol Alcohol 37(5):409–415. https://doi.org/10.1093/alcalc/37.5.409

  26. Lee SR, Choi EK, Rhee TM, Lee HJ, Lim WH, Kang SH, Han KD, Cha MJ, Cho Y, Oh IY, Oh S (2016) Evaluation of the association between diabetic retinopathy and the incidence of atrial fibrillation: a nationwide population-based study. Int J Cardiol 223:953–957. https://doi.org/10.1016/j.ijcard.2016.08.296

    Article  PubMed  Google Scholar 

  27. Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, Fruchart JC, James WP, Loria CM, Smith SC Jr (2009) Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 120(16):1640–1645. https://doi.org/10.1161/circulationaha.109.192644

    Article  CAS  PubMed  Google Scholar 

  28. Kim MK, Lee WY, Kang JH, Kang JH, Kim BT, Kim SM, Kim EM, Suh SH, Shin HJ, Lee KR, Lee KY, Lee SY, Lee SY, Lee SK, Lee CB, Chung S, Jeong IK, Hur KY, Kim SS, Woo JT (2014) 2014 clinical practice guidelines for overweight and obesity in Korea. Endocrinol Metab (Seoul) 29(4):405–409. https://doi.org/10.3803/EnM.2014.29.4.405

  29. Yang S, Nguyen ND, Center JR, Eisman JA, Nguyen TV (2014) Association between hypertension and fragility fracture: a longitudinal study. Osteoporos Int 25(1):97–103. https://doi.org/10.1007/s00198-013-2457-8

  30. Oei L, Zillikens MC, Dehghan A, Buitendijk GH, Castaño-Betancourt MC, Estrada K, Stolk L, Oei EH, van Meurs JB, Janssen JA, Hofman A, van Leeuwen JP, Witteman JC, Pols HA, Uitterlinden AG, Klaver CC, Franco OH, Rivadeneira F (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):1619–1628. https://doi.org/10.2337/dc12-1188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Nielson CM, Marshall LM, Adams AL, LeBlanc ES, Cawthon PM, Ensrud K, Stefanick ML, Barrett-Connor E, Orwoll ES (2011) BMI and fracture risk in older men: the osteoporotic fractures in men study (MrOS). Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research 26(3):496–502. https://doi.org/10.1002/jbmr.235

    Article  Google Scholar 

  32. Tanaka S, Kuroda T, Saito M, Shiraki M (2013) Overweight/obesity and underweight are both risk factors for osteoporotic fractures at different sites in Japanese postmenopausal women. Osteoporos Int 24(1):69–76. https://doi.org/10.1007/s00198-012-2209-1

  33. Fraser LA, Pritchard J, Ioannidis G, Giangegorio LM, Adachi JD, Papaioannou A, Leslie WD (2011) Clinical risk factors for fracture in diabetes: a matched cohort analysis. J Clin Densitom 14(4):416–421. https://doi.org/10.1016/j.jocd.2011.06.007

  34. 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(4):495–500. https://doi.org/10.1007/s00198-005-0013-x

  35. 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(1):45–55. https://doi.org/10.1007/s00223-008-9195-5

    Article  CAS  PubMed  Google Scholar 

  36. Hothersall EJ, Livingstone SJ, Looker HC, Ahmed SF, Cleland S, Leese GP, Lindsay RS, McKnight J, Pearson D, Philip S, Wild SH, Colhoun HM (2014) Contemporary risk of hip fracture in type 1 and type 2 diabetes: a national registry study from Scotland. J Bone Miner Res 29(5):1054–1060. https://doi.org/10.1002/jbmr.2118

  37. Sellmeyer DE, Civitelli R, Hofbauer LC, Khosla S, Lecka-Czernik B, Schwartz AV (2016) Skeletal metabolism, fracture risk, and fracture outcomes in type 1 and type 2 diabetes. Diabetes 65(7):1757–1766. https://doi.org/10.2337/db16-0063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. LeRoith D, Biessels GJ, Braithwaite SS, Casanueva FF, Draznin B, Halter JB, Hirsch IB, McDonnell ME, Molitch ME, Murad MH, Sinclair AJ (2019) Treatment of diabetes in older adults: an endocrine society* clinical practice guideline. J Clin Endocrinol Metab 104(5):1520–1574. https://doi.org/10.1210/jc.2019-00198

    Article  PubMed  PubMed Central  Google Scholar 

  39. Terada M, Inaba M, Yano Y, Hasuma T, Nishizawa Y, Morii H, Otani S (1998) Growth-inhibitory effect of a high glucose concentration on osteoblast-like cells. Bone 22(1):17–23. https://doi.org/10.1016/s8756-3282(97)00220-2

    Article  CAS  PubMed  Google Scholar 

  40. 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):1134–1142. https://doi.org/10.1111/dme.12734

  41. Schwartz AV, Margolis KL, Sellmeyer DE, Vittinghoff E, Ambrosius WT, Bonds DE, Josse RG, Schnall AM, Simmons DL, Hue TF, Palermo L, Hamilton BP, Green JB, Atkinson HH, O'Connor PJ, Force RW, Bauer DC (2012) Intensive glycemic control is not associated with fractures or falls in the ACCORD randomized trial. Diabetes Care 35(7):1525–1531. https://doi.org/10.2337/dc11-2184

    Article  PubMed  PubMed Central  Google Scholar 

  42. Hofbauer LC, Brueck CC, Singh SK, Dobnig H (2007) Osteoporosis in patients with diabetes mellitus. J Bone Miner Res 22(9):1317–1328. https://doi.org/10.1359/jbmr.070510

  43. Bonjour JP, Chevalley T (2014) Pubertal timing, bone acquisition, and risk of fracture throughout life. Endocr Rev 35(5):820–847. https://doi.org/10.1210/er.2014-1007

    Article  CAS  PubMed  Google Scholar 

  44. Huber A, Menconi F, Corathers S, Jacobson EM, Tomer Y (2008) Joint genetic susceptibility to type 1 diabetes and autoimmune thyroiditis: from epidemiology to mechanisms. Endocr Rev 29(6):697–725. https://doi.org/10.1210/er.2008-0015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Wirth CD, Blum MR, da Costa BR, Baumgartner C, Collet TH, Medici M, Peeters RP, Aujesky D, Bauer DC, Rodondi N (2014) Subclinical thyroid dysfunction and the risk for fractures: a systematic review and meta-analysis. Ann Intern Med 161(3):189–199. https://doi.org/10.7326/m14-0125

    Article  PubMed  PubMed Central  Google Scholar 

  46. Lee RH, Sloane R, Pieper C, Lyles KW, Adler RA, Van Houtven C, LaFleur J, Colón-Emeric C (2018) Clinical fractures among older men with diabetes are mediated by diabetic complications. J Clin Endocrinol Metab 103(1):281–287. https://doi.org/10.1210/jc.2017-01593

    Article  PubMed  Google Scholar 

  47. Kim BY, Won JC, Lee JH, Kim HS, Park JH, Ha KH, Won KC, Kim DJ, Park KS (2019) Diabetes fact sheets in Korea, 2018: an appraisal of current status. Diabetes Metab J 43(4):487–494. https://doi.org/10.4093/dmj.2019.0067

    Article  PubMed  PubMed Central  Google Scholar 

  48. Majumdar SR, Leslie WD, Lix LM, Morin SN, Johansson H, Oden A, McCloskey EV, Kanis JA (2016) Longer duration of diabetes strongly impacts fracture risk assessment: the Manitoba BMD cohort. J Clin Endocrinol Metab 101(11):4489–4496. https://doi.org/10.1210/jc.2016-2569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Ivers RQ, Cumming RG, Mitchell P, Peduto AJ (2001) Diabetes and risk of fracture: the Blue Mountains Eye Study. Diabetes Care 24(7):1198–1203. https://doi.org/10.2337/diacare.24.7.1198

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was performed using a database from the National Health Insurance Service, and the results do not necessarily represent the opinion of the National Health Insurance Service.

This study was made possible through the research support program of the Division of Endocrinology and Metabolism, College of Medicine, the Catholic University of Korea. We would like to express our gratitude to Professor Soon Jip Yoo, the head of the division, who made this research possible.

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Authors and Affiliations

  1. Division of Endocrinology and Metabolism, Department of Internal Medicine, Seoul St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea

    J. Ha, C. Jeong & M.I. Kang

  2. Department of Statistics and Actuarial Science, Soongsil University, Seoul, Republic of Korea

    K.-D. Han

  3. Division of General Internal Medicine, Department of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, Republic of Korea

    Y. Lim

  4. Division of Endocrinology and Metabolism, Department of Internal Medicine, Yeouido St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea

    M.K. Kim, H.-S. Kwon, K.-H. Song & K.-H. Baek

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Correspondence to K.-H. Baek.

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The study was approved by the Institutional Review Board of the Catholic Medical Center (No. KC20ZISI0291). The need for informed consent was waived by the review board because all data provided by the NHIS to researchers were deidentified.

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Ha, J., Jeong, C., Han, KD. et al. Comparison of fracture risk between type 1 and type 2 diabetes: a comprehensive real-world data. Osteoporos Int 32, 2543–2553 (2021). https://doi.org/10.1007/s00198-021-06032-z

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