Abstract
Summary
This study aimed to evaluate bone mineral density (BMD), trabecular microarchitecture, and proximal hip geometry in diabetic postmenopausal women, where BMD alone cannot reflect bone strength adequately. We found significantly lower trabecular bone score and BMD at the distal radius and total forearm in diabetic subjects compared to controls.
Purpose
The limitations resulting from the exclusive assessment of bone mineral density (BMD) in people with diabetes can lead to underestimation of microarchitectural and geometric changes, both of which play an essential role in the fracture risk. Therefore, we aimed to evaluate BMD, trabecular bone score (TBS), and hip structural analysis (HSA) in diabetic type-2 post-menopausal women and compare them with healthy postmenopausal subjects.
Methods
BMD was assessed at the lumbar spine, femoral sites, distal radius, and total forearm using dual-energy X-ray absorptiometry (DXA); TBS was measured based on DXA images using the software at the same region of interest as the BMD measurements; geometric assessment at the proximal femur was performed by the HSA program.
Results
A total of 348 ambulatory type-2 diabetic postmenopausal women and 539 healthy postmenopausal women were enrolled. TBS and BMD at the distal radius and total forearm were significantly (P value < 0.05) lower in cases compared to controls after age and body mass index (BMI) adjustment. In addition, degraded bone microarchitecture was significantly (P value < 0.05) more prevalent in diabetic subjects than in non-diabetic controls after adjusting for age and BMI. A number of geometric indices of the proximal hip were significantly lower in the controls than in those with diabetes (P-value < 0.05).
Conclusion
This study may highlight the utility of the TBS and BMD at the distal radius and total forearm in subjects with type-2 diabetes mellitus, where the BMD at central sites may not adequately predict fracture risk.
Similar content being viewed by others
Data availability
The authors confirm that the data supporting the findings of this study are available and can be requested from the corresponding author upon reasonable request.
References
World Health Organization. Noncommunicable diseases: progress monitor 2022. Available at https://apps.who.int/iris/bitstream/handle/10665/353048/9789240047761-eng.pdf. Accessed 22 Dec 2022
Zhou B, Lu Y, Hajifathalian K, Bentham J, Di Cesare M, Danaei G et al (2016) Worldwide trends in diabetes since 1980: a pooled analysis of 751 population-based studies with 4· 4 million participants. Lancet 387(10027):1513–1530
Sun H, Saeedi P, Karuranga S, Pinkepank M, Ogurtsova K, Duncan BB et al (2022) IDF Diabetes atlas: global, regional and country-level diabetes prevalence estimates for 2021 and projections for 2045. Diabetes Res Clin Pract 183:109119
Wild S, Roglic G, Green A, Sicree R, King H (2004) Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 27(5):1047–1053
Luisa Isidro M, Ruano B (2010) Bone disease in diabetes. Curr Diabetes Rev 6(3):144–155
Zheng Y, Ley SH, Hu FB (2018) Global aetiology and epidemiology of type 2 diabetes mellitus and its complications. Nat Rev Endocrinol 14(2):88–98
Dede AD, Tournis S, Dontas I, Trovas G (2014) Type 2 diabetes mellitus and fracture risk. Metabolism 63(12):1480–1490
Moayeri A, Mohamadpour M, Mousavi SF, Shirzadpour E, Mohamadpour S, Amraei M (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
Ma L, Oei L, Jiang L, Estrada K, Chen H, Wang Z et al (2012) Association between bone mineral density and type 2 diabetes mellitus: a meta-analysis of observational studies. Eur J Epidemiol 27(5):319–332
Link TM, Majumdar S (2004) Current diagnostic techniques in the evaluation of bone architecture. Curr Osteoporos Rep 2(2):47–52
Bonnick SL (2007) Hsa: Beyond bmd with dxa. Bone 41(1):S9–S12
Brandi ML (2009) Microarchitecture, the key to bone quality. Rheumatology 48(suppl_4):iv3–iv8
Leslie WD, Rubin MR, Schwartz AV, Kanis JA (2012) Type 2 diabetes and bone. J Bone Miner Res 27(11):2231–2237
Feng X (2009) Chemical and biochemical basis of cell-bone matrix interaction in health and disease. Curr Chem Biol 3(2):189–196
Bonds DE, Larson JC, Schwartz AV, Strotmeyer ES, Robbins J, Rodriguez BL et al (2006) Risk of fracture in women with type 2 diabetes: the Women’s Health Initiative Observational Study. J Clin Endocrinol Metab 91(9):3404–3410
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 Complications 25(4):216–221
Freeman R (2007) Are blood glucose levels affected by menopause? Menopause 14(3):350–351
Ren Y, Zhang M, Liu Y, Sun X, Wang B, Zhao Y et al (2019) Association of menopause and type 2 diabetes mellitus. Menopause 26(3):325–330
Igase M, Kohara K, Tabara Y, Nagai T, Ochi N, Kido T et al (2012) Low-dose rosuvastatin improves the functional and morphological markers of atherosclerosis in asymptomatic postmenopausal women with dyslipidemia. Menopause 19(12):1294–1299
Blümel JE, Fica J, Chedraui P, Mezones-Holguin E, Zuñiga MC, Witis S et al (2016) Sedentary lifestyle in middle-aged women is associated with severe menopausal symptoms and obesity. Menopause 23(5):488–493
Zhou H, Guo Z-r, Yu L-g, Hu X-s, Xu B-h, Liu H-b et al (2010) Evidence on the applicability of the ATPIII, IDF and CDS metabolic syndrome diagnostic criteria to identify CVD and T2DM in the Chinese population from a 6.3-year cohort study in mid-eastern China. Diabetes Res Clin Pract 90(3):319–25
Ja K (2007) Assessment of osteoporosis at the primary health care level. WHO Collaborating Centre for Metabolic Bone Diseases. WHO Collaborating Centre for Metabolic Bone Diseases. Available at https://frax.shef.ac.uk/FRAX/pdfs/WHO_Technical_Report.pdf. Accessed 22 Dec 2022
Harvey N, Glüer C, Binkley N, McCloskey E, Brandi M-L, Cooper C et al (2015) Trabecular bone score (TBS) as a new complementary approach for osteoporosis evaluation in clinical practice. Bone 78:216–224
Ho-Pham L, Nguyen T (2019) Association between trabecular bone score and type 2 diabetes: a quantitative update of evidence. Osteoporos Int 30(10):2079–2085
Baleanu F, Bergmann P, Hambye AS, Dekelver C, Iconaru L, Cappelle SI et al (2019) Assessment of bone quality with trabecular bone score in type 2 diabetes mellitus: a study from the FRISBEE cohort. Int J Clin Pract 73(5):e13347
Rianon N, Ambrose CG, Buni M, Watt G, Reyes-Ortiz C, Lee M et al (2018) Trabecular bone score is a valuable addition to bone mineral density for bone quality assessment in older Mexican American women with type 2 diabetes. J Clin Densitom 21(3):355–359
Zhukouskaya V, Ellen-Vainicher C, Gaudio A, Privitera F, Cairoli E, Ulivieri F et al (2016) The utility of lumbar spine trabecular bone score and femoral neck bone mineral density for identifying asymptomatic vertebral fractures in well-compensated type 2 diabetic patients. Osteoporos Int 27:49–56
Lin Y-C, Wu J, Kuo S-F, Cheung Y-C, Sung C-M, Fan C-M et al (2020) Vertebral fractures in type 2 diabetes patients: utility of trabecular bone score and relationship with serum bone turnover biomarkers. J Clin Densitom 23(1):37–43
Beck TJ, Broy SB (2015) Measurement of hip geometry—technical background. J Clin Densitom 18(3):331–337
Beck TJ (2007) Extending DXA beyond bone mineral density: understanding hip structure analysis. Curr Osteoporos Rep 5(2):49–55
Shuhart CR, Yeap SS, Anderson PA, Jankowski LG, Lewiecki EM, Morse LR et al (2019) Executive summary of the 2019 ISCD position development conference on monitoring treatment, DXA cross-calibration and least significant change, spinal cord injury, peri-prosthetic and orthopedic bone health, transgender medicine, and pediatrics. J Clin Densitom 22(4):453–471
Gautam KP, Cherian KE, Kapoor N, Thomas N, Paul TV (2022) Utility and validation of bone mineral density measurements at forearm in predicting trabecular microarchitecture and central-site osteoporosis in aging Indian postmenopausal women—a promising surrogate? Aging Med 5(1):30–37
Lewiecki EM, Binkley N, Morgan SL, Shuhart CR, Camargos BM, Carey JJ et al (2016) Best practices for dual-energy X-ray absorptiometry measurement and reporting: International Society for Clinical Densitometry Guidance. J Clin Densitom 19(2):127–140
Silva BC, Broy SB, Boutroy S, Schousboe JT, Shepherd JA, Leslie WD (2015) Fracture risk prediction by non-BMD DXA measures: the 2015 ISCD official positions part 2: trabecular bone score. J Clin Densitom 18(3):309–330
Mirzaei A, Jahed SA, Nojomi M, Rajaei A, Zabihiyeganeh M (2018) A study of the value of trabecular bone score in fracture risk assessment of postmenopausal women. Taiwan J Obstet Gynecol 57(3):389–393
Broy SB, Cauley JA, Lewiecki ME, Schousboe JT, Shepherd JA, Leslie WD (2015) Fracture risk prediction by non-BMD DXA measures: the 2015 ISCD official positions part 1: hip geometry. J Clin Densitom 18(3):287–308
Majima T, Komatsu Y, Yamada T, Koike Y, Shigemoto M, Takagi C et al (2005) Decreased bone mineral density at the distal radius, but not at the lumbar spine or the femoral neck, in Japanese type 2 diabetic patients. Osteoporos Int 16(8):907–913
Anaforoglu I, Nar-Demirer A, Bascil-Tutuncu N, Ertorer ME (2009) Prevalence of osteoporosis and factors affecting bone mineral density among postmenopausal Turkish women with type 2 diabetes. J Diabetes Complicat 23(1):12–17
Sharifi F, Ahmadimoghadam N, Mousavinasab N (2006) The relationship between type 2 diabetes mellitus and bone density in postmenopausal women. Int J Endocrinol Metab 4(3):117–122
Yu E, Putman MS, Derrico N, Abrishamanian-Garcia G, Finkelstein JS, Bouxsein ML (2015) Defects in cortical microarchitecture among African-American women with type 2 diabetes. Osteoporos Int 26:673–679
Samelson EJ, Demissie S, Cupples LA, Zhang X, Xu H, Liu CT et al (2018) Diabetes and deficits in cortical bone density, microarchitecture, and bone size: Framingham HR-pQCT study. J Bone Miner Res 33(1):54–62
Burghardt AJ, Issever AS, Schwartz AV, Davis KA, Masharani U, Majumdar S et al (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
Ho-Pham L, Chau P, Do A, Nguyen H, Nguyen T (2018) Type 2 diabetes is associated with higher trabecular bone density but lower cortical bone density: the Vietnam Osteoporosis Study. Osteoporos Int 29:2059–2067
Garg R, Chen Z, Beck T, Cauley JA, Wu G, Nelson D et al (2012) Hip geometry in diabetic women: Implications for fracture risk. Metabolism 61(12):1756–1762
Bonaccorsi G, Fila E, Messina C, Maietti E, Ulivieri FM, Caudarella R et al (2017) Comparison of trabecular bone score and hip structural analysis with FRAX® in postmenopausal women with type 2 diabetes mellitus. Aging Clin Exp Res 29(5):951–957
Tripto-Shkolnik L, Vered I, Peltz-Sinvani N, Kowal D, Goldshtein I (2021) Bone mineral density of the 1/3 radius refines osteoporosis diagnosis, correlates with prevalent fractures, and enhances fracture risk estimates. Endocr Pract 27(5):408–412
Park C-H, Min K-B, Min J-Y, Kim DH, Seo KM, Kim D-K (2021) Strong association of type 2 diabetes with degenerative lumbar spine disorders. Sci Rep 11(1):16472
Vazquez C, Luca B, Cardenas J, Sanchez A, Montoya T, Labeira P et al (2021) Obesity in postmenopausal women: Causes, prevalence and specific risks: role of decreased. Adv Obes Weight Manag Control 11:155–157
Paul J, Devarapalli V, Johnson JT, Cherian KE, Jebasingh FK, Asha HS et al (2021) Do proximal hip geometry, trabecular microarchitecture, and prevalent vertebral fractures differ in postmenopausal women with type 2 diabetes mellitus? A cross-sectional study from a teaching hospital in southern India. Osteoporos Int 32(8):1585–1593
Bonaccorsi G, Messina C, Cervellati C, Maietti E, Medini M, Rossini M et al (2018) Fracture risk assessment in postmenopausal women with diabetes: comparison between DeFRA and FRAX tools. Gynecol Endocrinol 34(5):404–408
Kim JH, Choi HJ, Ku EJ, Kim KM, Kim SW, Cho NH et al (2015) Trabecular bone score as an indicator for skeletal deterioration in diabetes. J Clin Endocrinol Metab 100(2):475–482
Hamilton CJ, Jamal SA, Beck TJ, Khaled AS, Adachi JD, Brown JP et al (2013) Evidence for impaired skeletal load adaptation among Canadian women with type 2 diabetes mellitus: insight into the BMD and bone fragility paradox. Metabolism 62(10):1401–1405
Bonaccorsi G, Fila E, Messina C, Maietti E, Ulivieri FM, Caudarella R et al (2017) Comparison of trabecular bone score and hip structural analysis with FRAX® in postmenopausal women with type 2 diabetes mellitus. Aging Clin Exp Res 29:951–957
Acknowledgements
The authors would like to thank Dr. Nasrin Shokrpour for editorial assistance.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Consent to participate
All participants in the study were fully informed about the goals, cooperation, benefits, and potential harms of the study and completed the ethical consent forms.
Statement of human and animal rights
All procedures performed in studies involving human participants were in accordance with the ethical standards of The Human Ethics Committee of Shiraz University of Medical Sciences with the approval code of IR.SUMS.REC.1401.281 and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.
Conflicts of interest
None.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Naseri, A., Shojaeefard, E., Bakhshayeshkaram, M. et al. Hip structural analysis, trabecular bone score, and bone mineral density in post-menopausal women with type-2 diabetes mellitus: a multi-center cross-sectional study in the south of Iran. Arch Osteoporos 18, 98 (2023). https://doi.org/10.1007/s11657-023-01310-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11657-023-01310-1