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Effects of Diabetes on Bone Material Properties

Current Osteoporosis Reports volume 17, pages 455–464 (2019)Cite this article

Abstract

Purpose of Review

Individuals with type 1 and type 2 diabetes mellitus (T1DM, T2DM) have an increased risk of bone fracture compared to non-diabetic controls that is not explained by differences in BMD, BMI, or falls. Thus, bone tissue fracture resistance may be reduced in individuals with DM. The purpose of this review is to summarize work that analyzes the effects of T1DM and T2DM on bone tissue compositional and mechanical properties.

Recent Findings

Studies of clinical T2DM specimens revealed increased mineralization and advanced glycation endproduct (AGE) concentrations and significant relationships between mechanical performance and composition of cancellous bone. Specifically, in femoral cancellous tissue, compressive stiffness and strength increased with mineral content; and post-yield properties decreased with AGE concentration. In addition, cortical resistance to in vivo indentation (bone material strength index) was lower in patients with T2DM vs. age-matched non-diabetic controls, and this resistance decreased with worsening glycemic control. Recent studies on patients with T1DM and history of a prior fragility fracture found greater mineral content and concentrations of AGEs in iliac trabecular bone and correspondingly stiffer, harder bone at the nanosacle.

Summary

Recent observational data showed greater AGE and mineral content in surgically retrieved bone from patients with T2DM vs. non-DM controls, consistent with reduced bone remodeling. Limited data on human T1DM bone tissue also showed higher mineral and AGE content in patients with prior fragility fractures compared to non-DM and non-fracture controls.

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References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Vestergaard P. Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes - a meta-analysis. Osteoporos Int. 2007;18:427–44.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  2. Janghorbani M, Van Dam RM, Willett WC, Hu FB. Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am J Epidemiol. 2007;166:495–505.

    PubMed  Article  PubMed Central  Google Scholar 

  3. Shah VN, Carpenter RD, Ferguson VL, Schwartz AV. Bone health in type 1 diabetes. Curr Opin Endocrinol Diabetes Obes. 2018;25:231–6.

    PubMed  Article  PubMed Central  Google Scholar 

  4. Schwartz AV, Vittinghoff E, Bauer DC, Hillier TA, Strotmeyer ES, Ensrud KE, et al. Association of BMD and FRAX score with risk of fracture in older adults with type 2 diabetes. JAMA - J Am Med Assoc. 2011;305:2184–92.

    CAS  Article  Google Scholar 

  5. 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. J Clin Endocrinol Metab. 2006;91:3404–10.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  6. Starup-Linde J, Frost M, Vestergaard P, Abrahamsen B. Epidemiology of fractures in diabetes. Calcif Tissue Int. Elsevier Inc. 2017;100:109–21.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  7. Schwartz AV. Epidemiology of fractures in type 2 diabetes. Bone. 2016;82:2–8.

    PubMed  Article  Google Scholar 

  8. Hough FS, Pierroz DD. Cooper C, Ferrari SL, IOF CSA Bone and Diabetes Working Group _. Mechanisms in endocrinology: mechanisms and evaluation of bone fragility in type 1 diabetes mellitus. Eur J Endocrinol. 2016;174:R127–38.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  9. Napoli N, Chandran M, Pierroz DD, Abrahamsen B, Schwartz AV, Ferrari SL. Mechanisms of diabetes mellitus-induced bone fragility. Nat Rev Endocrinol. Nat Publ Group. 2017;13:208–19.

    CAS  Google Scholar 

  10. Shanbhogue VV, Mitchell DM, Rosen CJ, Bouxsein ML. Type 2 diabetes and the skeleton: new insights into sweet bones. Lancet Diabetes Endocrinol. 2016;4:159–73.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  11. •• Hunt H, Torres A, Palomino P, 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. J Bone Miner Res. 2019; This study relating compositional and mechanical properties found increased pentosidine and mineralization in men with T2DM, and showed that high concentrations of AGEs can increase fragility, especially for T2DM patients with low BV/TV.

  12. Saito M, Fujii K, Mori Y, Marumo K. Role of collagen enzymatic and glycation induced cross-links as a determinant of bone quality in spontaneously diabetic WBN/Kob rats. Osteoporos Int. 2006;17:1514–23.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  13. Vashishth D, Gibson GJ, Khoury JI, Schaffler MB, Kimura J, Fyhrie DP. Influence of nonenzymatic glycation on biomechanical properties of cortical bone. Bone. 2001;28:195–201.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  14. Tang SY, Zeenath U, Vashishth D. Effects of non-enzymatic glycation on cancellous bone fragility. Bone. 2007;40:1144–51.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  15. Yamagishi S-I. Role of advanced glycation end products (AGEs) and receptor for AGEs (RAGE) in vascular damage in diabetes. EXG. 2011;46:217–24.

    CAS  Google Scholar 

  16. Keenan HA, Maddaloni E. Bone Microarchitecture in type 1 diabetes: it is complicated. Curr Osteoporos Rep Springer US. 2016;14:351–8.

    Article  Google Scholar 

  17. 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. J Bone Miner Res. 2017;32:1062–71.

    PubMed  Article  PubMed Central  Google Scholar 

  18. Kalaitzoglou E, Popescu I, Bunn RC, Fowlkes JL, Thrailkill KM. Effects of type 1 diabetes on osteoblasts, osteocytes, and osteoclasts. Curr Osteoporos Rep. Springer US. 2016;14:310–9.

    Article  Google Scholar 

  19. • Hygum K, Starup-Linde J, Harsløf T, Vestergaard P, Langdahl BL. Diabetes mellitus, a state of low bone turnover-a systematic review and meta-analysis. Eur J Endocrinol. 2017;176:R137–57 This extensive review of biochemical markers of bone formation and resorption in diabetes and found that low bone turnover is observed in both T1DM and T2DM conditions.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  20. Zhukouskaya VV, Eller-Vainicher C, Shepelkevich AP, Dydyshko Y, Cairoli E, Chiodini I. Bone health in type 1 diabetes: focus on evaluation and treatment in clinical practice. J Endocrinol Invest. Springer International Publishing. 2015;38:941–50.

    CAS  Google Scholar 

  21. Hamann C, Kirschner S, Günther KP, Hofbauer LC. Bone, sweet bone - osteoporotic fractures in diabetes mellitus. Nat Rev Endocrinol Nature Publishing Group. 2012;8:297–305.

    CAS  Article  Google Scholar 

  22. •• Farlay D, Armas LAG, Gineyts E, Akhter MP, Recker RR, Boivin G. Nonenzymatic glycation and degree of mineralization are higher in bone from fractured patients with type 1 diabetes mellitus. J Bone Miner Res. 2016;31:190–5 This is the only study to our knowledge to have assessed compositional properties in patients with T1DM and found increased AGE accumulation in patients with T1DM.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  23. Fleischli JG, Laughlin TJ, Lavery LA, Shah B, Lanctot D, Agrawal CM, et al. The effects of diabetes mellitus on the material properties of human metatarsal bones. J Foot Ankle Surg. 1998;37:195–8.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  24. Fleischli JG, Laughlin TJ, Athanasiou K, Lanctot DR, Lavery L, Wang X, et al. Effect of diabetes mellitus on the material properties of the distal tibia. J Am Podiatr Med Assoc. 2014;96:91–5.

    Article  Google Scholar 

  25. Lenzen S. The mechanisms of alloxan- and streptozotocin-induced diabetes. Diabetologia. 2008;51:216–26.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  26. •• Fajardo RJ, Karim L, Calley VI, Bouxsein ML. A review of rodent models of type 2 diabetic skeletal fragility. J Bone Miner Res. 2014;29:1025–40 This extensive review discusses the effect of T2DM on the skeletal phenotype of different rodent models.

    PubMed  PubMed Central  Article  Google Scholar 

  27. Paschalis EP, Verdelis K, Doty SB, Boskey AL, Mendelsohn R, Yamauchi M. Spectroscopic characterization of collagen cross-links in bone. J Bone Miner Res. 2001;16:1821–8.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  28. Oliveira Limirio PHJ, Da Rocha HA, De Morais RB, Hiraki KRN, Balbi APC, Soares PBF, et al. Influence of hyperbaric oxygen on biomechanics and structural bone matrix in type 1 diabetes mellitus rats. PLoS ONE. 2018;13.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  29. Bozkurt O, Bilgin MD, Evis Z, Pleshko N, Severcan F. Early alterations in bone characteristics of type I diabetic rat femur: a Fourier transform infrared (FT-IR) imaging study. Appl Spectrosc. 2016;70:2005–15.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  30. Donmez BO, Unal M, Ozdemir S, Ozturk N, Oguz N, Akkus O. Effects of losartan treatment on the physicochemical properties of diabetic rat bone. J Bone Miner Metab. 2017;35:161–70.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  31. Silva MJ, Brodt MD, Lynch MA, McKenzie JA, Tanouye KM, Nyman JS, et al. Type 1 diabetes in young rats leads to progressive trabecular bone loss, cessation of cortical bone growth, and diminished whole bone strength and fatigue life. J Bone Miner Res. 2009;24:1618–27.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  32. Mansur SA, Mieczkowska A, Bouvard B, Flatt PR, Chappard D, Irwin N, et al. Stable incretin mimetics counter rapid deterioration of bone quality in type 1 diabetes mellitus. J Cell Physiol. 2015;230:3009–18.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  33. Mieczkowska A, Mansur SA, Irwin N, Flatt PR, Chappard D, Mabilleau G. Alteration of the bone tissue material properties in type 1 diabetes mellitus: a Fourier transform infrared microspectroscopy study. Bone. 2015;76:31–9.

    PubMed  Article  PubMed Central  Google Scholar 

  34. Facchini DM, Yuen VG, Battell ML, McNeill JH, Grynpas MD. The effects of vanadium treatment on bone in diabetic and non-diabetic rats. Bone. 2006;38:368–77.

    CAS  PubMed  Article  Google Scholar 

  35. Makowski AJ, Patil CA, Mahadevan-Jansen A, Nyman JS. Polarization control of Raman spectroscopy optimizes the assessment of bone tissue. J Biomed Opt International Society for Optics and Photonics. 2013;18:055005.

    Google Scholar 

  36. Taylor EA, Lloyd AA, Salazar-Lara C, Donnelly E. Raman and Fourier transform infrared (FT-IR) mineral to matrix ratios correlate with physical chemical properties of model compounds and native bone tissue. Appl Spectrosc. 2017;71:2404–10.

    CAS  PubMed  Article  Google Scholar 

  37. Nyman JS, Even JL, Jo CH, Herbert EG, Murry MR, Cockrell GE, et al. Increasing duration of type 1 diabetes perturbs the strength-structure relationship and increases brittleness of bone. Bone. 2011;48:733–40.

    PubMed  Article  PubMed Central  Google Scholar 

  38. Zhang H, Gan L, Zhu X, Wang J, Han L, Cheng P, et al. Moderate-intensity 4 mT static magnetic fields prevent bone architectural deterioration and strength reduction by stimulating bone formation in streptozotocin-treated diabetic rats. Bone. 2018;107:36–44.

    PubMed  Article  Google Scholar 

  39. Rubin MR, Paschalis EP, Poundarik A, Sroga GE, McMahon DJ, Gamsjaeger S, et al. Correction: advanced glycation endproducts and bone material properties in type 1 diabetic mice. PLoS ONE. 2016;11:1–14.

    Google Scholar 

  40. Epstein PN, Overbeek PA, Means AR. Calmodulin-induced early-onset diabetes in transgenic mice. Cell. 1989;58:1067–73.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  41. Thrailkill KM, Lumpkin CK, Bunn RC, Kemp SF, Fowlkes JL. Is insulin an anabolic agent in bone? Dissecting the diabetic bone for clues. Am J Physiol Endocrinol Metab. 2005;289:E735–45.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  42. Lecka-Czernik B. Safety of antidiabetic therapies on bone. Clin Rev Bone Miner Metab. 2013;11:49–58.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  43. •• 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. Elsevier. 2018;114:32–9 This is the first study to examine compositional and mechanical properties of bone from humans with T2DM and found reduced resistance to creep indentation in cortical bone from patients with T2DM.

    CAS  Article  Google Scholar 

  44. Bucknell A, King KB, Oren TW, Botolin S, Williams A. Arthroplasty in veterans: analysis of cartilage, bone, serum, and synovial fluid reveals differences and similarities in osteoarthritis with and without comorbid diabetes. J Rehabil Res Dev. 2012;48:1195.

    Google Scholar 

  45. Pritchard JM, Papaioannou A, Tomowich C, Giangregorio LM, Atkinson SA, Beattie KA, et al. Bone mineralization is elevated and less heterogeneous in adults with type 2 diabetes and osteoarthritis compared to controls with osteoarthritis alone. Bone. Elsevier Inc. 2013;54:76–82.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  46. Manavalan JS, Cremers S, Dempster DW, Zhou H, Dworakowski E, Kode A, et al. Circulating osteogenic precursor cells in type 2 diabetes mellitus. J Clin Endocrinol Metab. 2012;97:3240–50.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  47. •• Farr JN, Drake MT, Amin S, Melton LJ, McCready LK, Khosla S. In vivo assessment of bone quality in postmenopausal women with type 2 diabetes. J Bone Miner Res. 2014;29:787–95 This comprehensive assessment of geometric and microarchitectural properties in women with T2DM demonstrated that bone material strength index decreased with 10-year HbA1c.

    PubMed  PubMed Central  Article  Google Scholar 

  48. Furst JR, Bandeira LC, Fan WW, Agarwal S, Nishiyama KK, Mcmahon DJ, et al. Advanced glycation endproducts and bone material strength in type 2 diabetes. J Clin Endocrinol Metab. 2016;101:2502–10.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  49. Arnold M, Zhao S, Ma S, Giuliani F, Hansen U, Cobb JP, et al. Microindentation – a tool for measuring cortical bone stiffness? Bone Jt Res. 2017;6:542–9.

    CAS  Article  Google Scholar 

  50. Poundarik AA, Wu PC, Evis Z, Sroga GE, Ural A, Rubin M, et al. A direct role of collagen glycation in bone fracture. J Mech Behav Biomed Mater. 2015;50:82–92.

    Article  Google Scholar 

  51. Karim L, Tang SY, Sroga GE, Vashishth D. Differences in non-enzymatic glycation and collagen cross-links between human cortical and cancellous bone. Osteoporos Int. 2013;24:2441–7.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  52. Schmidt FN, Zimmermann EA, Campbell GM, Sroga GE, Püschel K, Amling M, et al. Assessment of collagen quality associated with non-enzymatic cross-links in human bone using Fourier-transform infrared imaging. Bone. 2017;97:243–51.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  53. Willett TL, Sutty S, Gaspar A, Avery N, Grynpas M. In vitro non-enzymatic ribation reduces post-yield strain accommodation in cortical bone. Bone. Elsevier Inc. 2013;52:611–22.

    PubMed  Article  PubMed Central  Google Scholar 

  54. Marin C, Papantonakis G, Sels K, Van Lenthe GH, Falgayrac G, Vangoitsenhoven R, et al. Unraveling the compromised biomechanical performance of type 2 diabetes- and Roux-en-Y gastric bypass bone by linking mechanical-structural and physico-chemical properties. Sci Rep Springer US. 2018;8:1–12.

    Google Scholar 

  55. Ionova-Martin SS, Wade JM, Tang S, Shahnazari M, Ager JW, Lane NE, et al. Changes in cortical bone response to high-fat diet from adolescence to adulthood in mice. Osteoporos Int. 2011;22:2283–93.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  56. Kerckhofs G, Durand M, Vangoitsenhoven R, Marin C, Van Der Schueren B, Carmeliet G, et al. Changes in bone macro-and microstructure in diabetic obese mice revealed by high resolution microfocus X-ray computed tomography. Sci Rep Nature Publishing Group. 2016;6:1–13.

    Google Scholar 

  57. Ionova-Martin SS, Do SH, Barth HD, Szadkowska M, Porter AE, Ager JW, et al. Reduced size-independent mechanical properties of cortical bone in high-fat diet-induced obesity. Bone. Elsevier Inc. 2010;46:217–25.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  58. Clark JB, Palmer CJ, Shaw WN. The diabetic Zucker fatty rat. Proc Soc Exp Biol Med. 1983;173:68–75.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  59. Fu C, Zhang X, Ye F, Yang J. High insulin levels in KK-Ay diabetic mice cause increased cortical bone mass and impaired trabecular micro-structure. Int J Mol Sci. 2015;16:8213–26.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  60. Reinwald S, Peterson RG, Allen MR, Burr DB. Skeletal changes associated with the onset of type 2 diabetes in the ZDF and ZDSD rodent models. Am J Physiol Endocrinol Metab. 2009;296:E765–74.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  61. Prisby RD, Swift JM, Bloomfield SA, Hogan HA, Delp MD. Altered bone mass, geometry and mechanical properties during the development and progression of type 2 diabetes in the Zucker diabetic fatty rat. J Endocrinol. 2008;199:379–88.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  62. Pereira M, Gohin S, Lund N, Hvid A, Smitham PJ, Oddy MJ, et al. Sclerostin does not play a major role in the pathogenesis of skeletal complications in type 2 diabetes mellitus. Osteoporos Int Osteoporosis International. 2017;28:309–20.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  63. Hamann C, Goettsch C, Mettelsiefen J, Henkenjohann V, Rauner M, Hempel U, et al. Delayed bone regeneration and low bone mass in a rat model of insulin-resistant type 2 diabetes mellitus is due to impaired osteoblast function. Am J Physiol Metab. 2011;301:E1220–8.

    CAS  Google Scholar 

  64. Xu F, Dong Y, Huang X, Li M, Qin L, Ren Y, et al. Decreased osteoclastogenesis, osteoblastogenesis and low bone mass in a mouse model of type 2 diabetes. Mol Med Rep. 2014;10:1935–41.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  65. Hunt HB, Pearl JC, Diaz DR, King KB, Donnelly E. Bone tissue collagen maturity and mineral content increase with sustained hyperglycemia in the KK-Ay murine model of type 2 diabetes. J Bone Miner Res. 2018;33:921–9.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  66. Takagi S, Miura T, Yamashita T, Ando N, Nakao H, Ishihara E, et al. Characteristics of diabetic osteopenia in KK-Ay diabetic mice. Biol Pharm Bull. 2012;35:438–43.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  67. Ealey KN, Fonseca D, Archer MC, Ward WE. Bone abnormalities in adolescent leptin-deficient mice. Regul Pept. 2006;136:9–13.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  68. Williams GA, Callon KE, Watson M, Costa JL, Ding Y, Dickinson M, et al. Skeletal phenotype of the leptin receptor-deficient db/db mouse. J Bone Miner Res. 2011;26:1698–709.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  69. Huang L, You YK, Zhu TY, Zheng LZ, Huang XR, Chen HY, et al. Validity of leptin receptor-deficiency (db/db) type 2 diabetes mellitus mice as a model of secondary osteoporosis. Sci Rep Nature Publishing Group. 2016;6:1–7.

    Google Scholar 

  70. Kim JH, Sen Ś, Avery CS, Simpson E, Chandler P, Nishina PM, et al. Genetic analysis of a new mouse model for non-insulin-dependent diabetes. Genomics. 2001;74:273–86.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  71. Kutscher CL, Miller M, Schmalbach NL. Renal deficiency associated with diabetes insipidus in the SWR/J mouse. Physiol Behav. 1975;14:815–8.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  72. Hammond MA, Gallant MA, Burr DB, Wallace JM. Nanoscale changes in collagen are reflected in physical and mechanical properties of bone at the microscale in diabetic rats. Bone. Elsevier Inc. 2013;60:26–32.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  73. Creecy A, Uppuganti S, Merkel AR, O’Neal D, Makowski AJ, Granke M, et al. Changes in the fracture resistance of bone with the progression of type 2 diabetes in the ZDSD rat. Calcif Tissue Int Springer US. 2016;99:289–301.

    CAS  Article  Google Scholar 

  74. Creecy A, Uppuganti S, Unal M, Clay Bunn R, Voziyan P, Nyman JS. Low bone toughness in the TallyHO model of juvenile type 2 diabetes does not worsen with age. Bone. Elsevier Inc. 2018;110:204–14.

    PubMed  PubMed Central  Article  Google Scholar 

  75. Gallant MA, Brown DM, Organ JM, Allen MR, Burr DB. Reference-point indentation correlates with bone toughness assessed using whole-bone traditional mechanical testing. Bone. Elsevier Inc. 2013;53:301–5.

    PubMed  Article  Google Scholar 

  76. Igarashi C, Maruyama T, Ezawa I, Takei I, Saruta T. WBN/Kob rat: a new model of spontaneous diabetes, osteopenia and systemic hemosiderin deposition. Bone Miner. 1994;27:133–44.

    CAS  PubMed  Article  Google Scholar 

  77. Devlin MJ, Van Vliet M, Motyl K, Karim L, Brooks DJ, Louis L, et al. Early-onset type 2 diabetes impairs skeletal acquisition in the male TALLYHO/JngJ mouse. Endocrinology. 2014;155:3806–16.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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Funding

Funding for this work was provided in part by NIH K01 AR064314 to ED.

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Affiliations

  1. Department of Materials Science and Engineering, Cornell University, Ithaca, NY, USA

    Sashank Lekkala, Heather B. Hunt & Eve Donnelly

  2. Sibley School of Mechanical and Aerospace Engineering, Cornell University, Ithaca, NY, USA

    Erik A. Taylor

  3. Research Division, Hospital for Special Surgery, New York, NY, USA

    Eve Donnelly

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  1. Sashank Lekkala
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  2. Erik A. Taylor
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Correspondence to Eve Donnelly.

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Sashank Lekkala, Erik A. Taylor, Heather B. Hunt, and Eve Donnelly declare no conflict of interest.

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Lekkala, S., Taylor, E.A., Hunt, H.B. et al. Effects of Diabetes on Bone Material Properties. Curr Osteoporos Rep 17, 455–464 (2019). https://doi.org/10.1007/s11914-019-00538-6

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Keywords

  • Bone material properties
  • Type 1 diabetes mellitus (T1DM)
  • Type 2 diabetes mellitus (T2DM)
  • Advanced glycation end products (AGEs)
  • Diabetic murine models
  • In vitro glycation