Microarchitectural aspects of increased bone fragility in individuals with type 2 diabetes
N/A
Abstract
Type 2 diabetes (T2DM) is a common noncommunicable disease that represents one of the leading public health problems worldwide. An increased risk of fractures, particularly fractures of the femoral neck, has been recognized as one of the complications of diabetes. However, fracture risk assessment in individuals with T2DM remains challenging because the results of densitometric measurements are unreliable in these individuals. Namely, individuals with T2DM often have a T-score that is identical to or better than that in individuals without T2DM. Various research groups have conducted basic and clinical analyses of cortical or trabecular microarchitecture of the distal radius, tibia, or femoral neck. The methodology and results of these studies are heterogeneous, and a definitive conclusion on the state of bone microarchitecture in individuals with T2DM is still lacking. Therefore, the aim of our study was to summarize the results of previously conducted studies of bone microarchitecture in individuals with T2DM and draw conclusions on the state of bone microarchitecture in individuals with T2DM. It is difficult to observe any changes in trabecular bone microarchitecture unless individuals with T2DM have developed microvascular or macrovascular complications; in that case, the results of the studies indicate that trabecular bone microarchitecture is significantly worse than that in individuals without T2DM.
References
1. Khan MAB, Hashim MJ, King JK, Govender RD, Mustafa H, Al Kaabi J. Epidemiology of type 2 diabetes–global burden of disease and forecasted trends. Journal of epidemiology and global health. 2020;10(1):107.
2. East M, Africa N. IDF diabetes atlas. diabetes. 2017;20:79.
3. DIJABETES Z, BIJI R. Incidencija i mortalitet od dijabetesa u Srbiji.
4. Collaboration ERF. Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: a collaborative meta-analysis of 102 prospective studies. The lancet. 2010;375(9733):2215-22.
5. Yau JW, Rogers SL, Kawasaki R, Lamoureux EL, Kowalski JW, Bek T, et al. Global prevalence and major risk factors of diabetic retinopathy. Diabetes care. 2012;35(3):556-64.
6. Tesfaye S, Selvarajah D. Advances in the epidemiology, pathogenesis and management of diabetic peripheral neuropathy. Diabetes/metabolism research and reviews. 2012;28:8-14.
7. Gulcelik NE, Bayraktar M, Caglar O, Alpaslan M, Karakaya J. Mortality after hip fracture in diabetic patients. Exp Clin Endocrinol Diabetes. 2011;119(7):414-8.
8. Ivers RQ, Cumming RG, Mitchell P, Peduto AJ. Diabetes and risk of fracture: the Blue Mountains Eye Study. Diabetes care. 2001;24(7):1198-203.
9. Valderrábano RJ, Linares MI. Diabetes mellitus and bone health: epidemiology, etiology and implications for fracture risk stratification. Clinical diabetes and endocrinology. 2018;4:1-8.
10. Panula J, Pihlajamäki H, Mattila VM, Jaatinen P, Vahlberg T, Aarnio P, et al. Mortality and cause of death in hip fracture patients aged 65 or older-a population-based study. BMC musculoskeletal disorders. 2011;12(1):1-6.
11. Dubey A, Aharonoff GB, Zuckerman JD, Koval KJ. The effects of diabetes on outcome after hip fracture. Bulletin (Hospital for Joint Diseases (New York, NY)). 2000;59(2):94-8.
12. Karagiannis A, Papakitsou E, Dretakis K, Galanos A, Megas P, Lambiris E, et al. Mortality rates of patients with a hip fracture in a southwestern district of Greece: ten-year follow-up with reference to the type of fracture. Calcified tissue international. 2006;78:72-7.
13. Schwartz AV, Hillier TA, Sellmeyer DE, Resnick HE, Gregg E, Ensrud KE, et al. Older women with diabetes have a higher risk of falls: a prospective study. Diabetes care. 2002;25(10):1749-54.
14. van Daele PL, Stolk RP, Burger H, Algra D, Grobbee DE, Hofman A, et al. Bone density in non-insulin-dependent diabetes mellitus: the Rotterdam Study. Annals of internal medicine. 1995;122(6):409-14.
15. Rakic V, Davis W, Chubb S, Islam F, Prince R, Davis T. Bone mineral density and its determinants in diabetes: the Fremantle Diabetes Study. Diabetologia. 2006;49:863-71.
16. Tebé C, Martínez-Laguna D, Carbonell-Abella C, Reyes C, Moreno V, Diez-Perez A, et al. The association between type 2 diabetes mellitus, hip fracture, and post-hip fracture mortality: a multi-state cohort analysis. Osteoporosis International. 2019;30:2407-15.
17. Vestergaard P, Rejnmark L, Mosekilde L. Diabetes and its complications and their relationship with risk of fractures in type 1 and 2 diabetes. Calcified tissue international. 2009;84:45-55.
18. Fan Y, Wei F, Lang Y, Liu Y. Diabetes mellitus and risk of hip fractures: a meta-analysis. Osteoporosis International. 2016;27:219-28.
19. Dede AD, Tournis S, Dontas I, Trovas G. Type 2 diabetes mellitus and fracture risk. Metabolism. 2014;63(12):1480-90.
20. Forsen L, Meyer H, Midthjell K, Edna T-H. Diabetes mellitus and the incidence of hip fracture: results from the Nord-Trøndelag Health Survey. Diabetologia. 1999;42:920-5.
21. Melton III LJ, Leibson CL, Achenbach SJ, Therneau TM, Khosla S. Fracture risk in type 2 diabetes: update of a population‐based study. Journal of Bone and Mineral Research. 2008;23(8):1334-42.
22. Bonds DE, Larson JC, Schwartz AV, Strotmeyer ES, Robbins J, Rodriguez BL, et al. Risk of fracture in women with type 2 diabetes: the Women’s Health Initiative Observational Study. The Journal of clinical endocrinology & metabolism. 2006;91(9):3404-10.
23. Schousboe JT, Morin SN, Kline GA, Lix LM, Leslie WD. Differential risk of fracture attributable to type 2 diabetes mellitus according to skeletal site. Bone. 2022;154:116220.
24. Shah VN, Shah CS, Snell‐Bergeon JK. Type 1 diabetes and risk of fracture: meta‐analysis and review of the literature. Diabetic Medicine. 2015;32(9):1134-42.
25. Miao J, Brismar K, Nyrén O, Ugarph-Morawski A, Ye W. Elevated hip fracture risk in type 1 diabetic patients: a population-based cohort study in Sweden. Diabetes care. 2005;28(12):2850-5.
26. Janghorbani M, Van Dam RM, Willett WC, Hu FB. Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. American journal of epidemiology. 2007;166(5):495-505.
27. Lee RH, Sloane R, Pieper C, Lyles KW, Adler RA, Van Houtven C, et al. Glycemic control and insulin treatment alter fracture risk in older men with type 2 diabetes mellitus. Journal of Bone and Mineral Research. 2019;34(11):2045-51.
28. Leanza G, Maddaloni E, Pitocco D, Conte C, Palermo A, Maurizi AR, et al. Risk factors for fragility fractures in type 1 diabetes. Bone. 2019;125:194-9.
29. Shanbhogue VV, Hansen S, Frost M, Jørgensen NR, Hermann AP, Henriksen JE, et al. Compromised cortical bone compartment in type 2 diabetes mellitus patients with microvascular disease. European journal of endocrinology. 2016;174(2):115-24.
30. Burghardt AJ, Issever AS, Schwartz AV, Davis KA, Masharani U, Majumdar S, et al. High-resolution peripheral quantitative computed tomographic imaging of cortical and trabecular bone microarchitecture in patients with type 2 diabetes mellitus. The Journal of Clinical Endocrinology & Metabolism. 2010;95(11):5045-55.
31. Patsch JM, Burghardt AJ, Yap SP, Baum T, Schwartz AV, Joseph GB, et al. Increased cortical porosity in type 2 diabetic postmenopausal women with fragility fractures. Journal of bone and mineral research. 2013;28(2):313-24.
32. Osima M, Kral R, Borgen TT, Høgestøl IK, Joakimsen RM, Eriksen EF, et al. Women with type 2 diabetes mellitus have lower cortical porosity of the proximal femoral shaft using low-resolution CT than nondiabetic women, and increasing glucose is associated with reduced cortical porosity. Bone. 2017;97:252-60.
33. Samakkarnthai P, Sfeir JG, Atkinson EJ, Achenbach SJ, Wennberg PW, Dyck PJ, et al. Determinants of bone material strength and cortical porosity in patients with type 2 diabetes mellitus. The Journal of Clinical Endocrinology & Metabolism. 2020;105(10):e3718-e29.
34. Nilsson AG, Sundh D, Johansson L, Nilsson M, Mellström D, Rudäng R, et al. 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. Journal of Bone and Mineral Research. 2017;32(5):1062-71.
35. Karim L, Moulton J, Van Vliet M, Velie K, Robbins A, Malekipour F, et al. Bone microarchitecture, biomechanical properties, and advanced glycation end-products in the proximal femur of adults with type 2 diabetes. Bone. 2018;114:32-9.
36. Hunt HB, Torres AM, Palomino PM, Marty E, Saiyed R, Cohn M, et al. Altered tissue composition, microarchitecture, and mechanical performance in cancellous bone from men with type 2 diabetes mellitus. Journal of Bone and Mineral Research. 2019;34(7):1191-206.
37. Heilmeier U, Cheng K, Pasco C, Parrish R, Nirody J, Patsch J, et al. Cortical bone laminar analysis reveals increased midcortical and periosteal porosity in type 2 diabetic postmenopausal women with history of fragility fractures compared to fracture-free diabetics. Osteoporosis International. 2016;27:2791-802.
38. Wölfel EM, Jähn-Rickert K, Schmidt FN, Wulff B, Mushumba H, Sroga GE, et al. Individuals with type 2 diabetes mellitus show dimorphic and heterogeneous patterns of loss in femoral bone quality. Bone. 2020;140:115556.
39. Cirovic A, Vujacic M, Petrovic B, Cirovic A, Zivkovic V, Nikolic S, et al. Vascular Complications in Individuals with Type 2 Diabetes Mellitus Additionally Increase the Risk of Femoral Neck Fractures Due to Deteriorated Trabecular Microarchitecture. Calcif Tissue Int. 2022;110(1):65-73.
40. Cirovic A, Jadzic J, Djukic D, Djonic D, Zivkovic V, Nikolic S, et al. Increased Cortical Porosity, Reduced Cortical Thickness, and Reduced Trabecular and Cortical Microhardness of the Superolateral Femoral Neck Confer the Increased Hip Fracture Risk in Individuals with Type 2 Diabetes. Calcif Tissue Int. 2022;111(5):457-65.