Abstract
Summary
This cross-sectional study assessed cortical bone properties via impact microindentation in adults with normoglycemia, prediabetes, and early-stage T2D. Bone material strength index was stable across the glycemia categories in whites but it declined in blacks. Blacks may be more susceptible than whites to impaired cortical bone properties in early diabetes.
Introduction
Individuals with long-standing type 2 diabetes (T2D) have altered cortical bone material properties as determined by impact microindentation. This cross-sectional study was done to determine whether altered cortical bone material properties could be detected in adults with prediabetes or early-stage T2D.
Methods
Men and postmenopausal women aged ≥ 50 years with no diabetes (50 white, 6 black), prediabetes (75 white, 13 black), and T2D of ≤ 5 years duration (24 white and 16 black) had assessments of bone material strength index (BMSi) by impact microindentation, trabecular bone score (TBS), and bone mineral density (BMD) by DXA and the advanced glycation end product, urine pentosidine.
Results
The association between glycemia category and BMSi differed by race (interaction p = 0.037). In the whites, BMSi did not differ across the glycemia categories, after adjustment for age, sex, and BMI (no diabetes 76.3 ± 1.6 (SEM), prediabetes 77.2 ± 1.3, T2D 76.2 ± 2.5, ANCOVA p = 0.887). In contrast, in the blacks, BMSi differed (ANCOVA p = 0.020) and was significantly lower in subjects with T2D than in those with prediabetes (p < 0.05) and no diabetes (p < 0.05) (mean ± SEM BMSi in no diabetes 86.0 ± 4.3, prediabetes 91.0 ± 3.2, and T2D 71.6 ± 2.9). Neither TBS nor urine pentosidine differed significantly across the glycemia categories in either whites or blacks.
Conclusions
These findings suggest different associations of glycemia with cortical bone material properties in blacks and whites, with blacks possibly being more susceptible to impaired cortical bone properties than whites in early diabetes. A larger study is needed to verify these observations.
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References
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
Hu F, Jiang C, Shen J, Tang P, Wang Y (2012) Preoperative predictors for mortality following hip fracture surgery: a systematic review and meta-analysis. Injury 43:676-685
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
Malgo F, Hamdy NAT, Papapoulis SE, Appelman-Dijkstra NM (2015) Bone material strength by microindentation in vivo is decreased in patients with fragility fractures independently of bone mineral density. J Clin Endocrinol Metab 100:2039-2945
Rozental TD, Walley KC, Demissie S, Caksa S, Martinez-Betancourt A, Parker AM, Tsai JN, Yu EW, Bouxsein ML (2018) Bone material strength index as measured by impact microindentation in postmenopausal women with distal radius and hip fractures. J Bone Miner Res 33(4):621–626
Rudang R, Zoulakis M, Sundh D, Brisby H, Diez-Perez A, Johansson L, Mellstrom D, Darelid A, Lorentzon M (2016) Bone material strength is associated with areal BMD but not with prevalent fractures in older women. Osteoporos Int 27(4):1585–1592
Leslie WD, Aubry-Rozier B, Lamy O, Hans D (2013) TBS (trabecular bone score) and diabetes-related fracture risk. J Clin Endocrinol Metab 98(2):602–609
Silva BC, Leslie WD, Resch H, Lamy O, Lesnyak O, Binkley N, McCloskey EV, Kanis JA, Bilezikian JP (2014) Trabecular bone score: a noninvasive analytical method based upon the DXA image. J Bone Miner Res 29(3):518–530
McCloskey EV, Oden A, Harvey NC, Leslie WD, Hans D, Johansson H, Barkmann R, Boutroy S, Brown J, Chapurlat R et al (2016) A meta-analysis of trabecular bone score in fracture risk prediction and its relationship to FRAX. J Bone Miner Res 31(5):940–948
Farr JN, Drake MT, Amin S, Melton LJ 3rd, McCready LK, Khosla S (2014) In vivo assessment of bone quality in postmenopausal women with type 2 diabetes. J Bone Miner Res 29(4):787–795
Nilsson AG, Sundh D, Johansson L, Nilsson M, Mellstrom D, Rudang R, Zoulakis M, Wallander M, Darelid A, Lorentzon M (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):1062–1071
Furst JR, Bandeira LC, Fan WW, Agarwal S, Nishiyama KK, McMahon DJ, Dworakowski E, Jiang H, Silverberg SJ, Rubin MR (2016) Advanced glycation endproducts and bone material strength in type 2 diabetes. J Clin Endocrinol Metab 101(6):2502–2510
Bailey AJ, Paul RG, Knott L (1998) Mechanisms of maturation and ageing of collagen. Mech Ageing Dev 106(1–2):1–56
Knott L, Bailey AJ (1998) Collagen cross-links in mineralizing tissues: a review of their chemistry, function, and clinical relevance. Bone 22(3):181–187
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(2):195–214
Wang X, Shen X, Li X, Agrawal CM (2002) Age-related changes in the collagen network and toughness of bone. Bone 31(1):1–7
Vashishth D (2009) Advanced glycation end-products and bone fractures. IBMS BoneKEy 6:268–278
Hunt HB, Torres AM, Palomino PM, Marty E, Saiyed R, Cohn M, Jo J, Warner S, Sroga GE, King KB, Lane JM, Vashishth D, Hernandez CJ, Donnelly E (2019) Altered tissue composition, microarchitecture, and mechanical performance in cancellous bone from men with type 2 diabetes mellitus. J Bone Miner Res. https://doi.org/10.1002/jbmr.3711
Schwartz AV, Garnero P, Hillier TA, Sellmeyer DE, Strotmeyer ES, Feingold KR, Resnick HE, Tylavsky FA, Black DM, Cummings SR, Harris TB, Bauer DC, for the Health, Aging, and Body Composition Study (2009) Pentosidine and increased fracture risk in older adults with type 2 diabetes. J Clin Endocrinol Metab 94(7):2380–2386
Yamamoto M, Yamaguchi T, Yamauchi M, Yano S, Sugimoto T (2008) Serum pentosidine levels are positively associated with the presence of vertebral fractures in postmenopausal women with type 2 diabetes. J Clin Endocrinol Metab 93(3):1013–1019
American Diabetes Association Clinical Practice Guidelines (2015) Diabetes Care 38(Supplement 1):S1-S94
White J, Harris SS, Dallal GE, Dawson-Hughes B (2003) Precision of single vs bilateral hip bone mineral density scans. J Clin Densitom 6(2):159–162
Vazquez E, Song LY, Dawson-Hughes B (2004) Precision of bone mineral density scans at the proximal tibia in osteoarthritic subjects. J Clin Densitom 7(4):364–367
Pothuaud L, Carceller P, Hans D (2008) Correlations between grey-level variations in 2D projection images (TBS) and 3D microarchitecture: applications in the study of human trabecular bone microarchitecture. Bone 42(4):775–787
Washburn RA, Smith KW, Jette AM, Janney CA (1993) The Physical Activity Scale for the Elderly (PASE): development and evaluation. J Clin Epidemiol 46(2):153–162
Yu EW, 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(2):673–679
Uppuganti S, Granke M, Manhard MK, Does MD, Perrien DS, Lee DH, Nyman JS (2017) Differences in sensitivity to microstructure between cyclic- and impact-based microindentation of human cortical bone. J Orthop Res 35(7):1442–1452
Looker AC, Eberhardt MS, Saydah SH (2016) Diabetes and fracture risk in older U.S. adults. Bone 82:9–15
Ma L, Oei L, Jiang L, Estrada K, Chen H, Wang Z, Yu Q, Zillikens MC, Gao X, Rivadeneira F (2012) Association between bone mineral density and type 2 diabetes mellitus: a meta-analysis of observational studies. Eur J Epidemiol 27(5):319–332
Funding
This work was supported by the NIH (National Institute of Arthritis and Musculoskeletal and Skin Diseases (NIAMS) R21 AR069922-01 to BD-H and by the U.S. Department of Agriculture, under agreement no. 58-1950-0-014).
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Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the authors and do not necessarily reflect the view of the National Institutes of Health or the U.S. Department of Agriculture.
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Mary Bouxsein serves on the Scientific Advisory Board of ActiveLife Scientific. The other authors have no conflicts to disclose.
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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The protocol was approved by the Tufts Medical Center-Tufts University Institutional Review Board, and written informed consent was obtained from each subject.
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Dawson-Hughes, B., Bouxsein, M. & Shea, K. Bone material strength in normoglycemic and hyperglycemic black and white older adults. Osteoporos Int 30, 2429–2435 (2019). https://doi.org/10.1007/s00198-019-05140-1
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DOI: https://doi.org/10.1007/s00198-019-05140-1