Skip to main content
Top
Published in: Current Osteoporosis Reports 6/2019

01-12-2019 | Diabetes | Bone and Diabetes (A Schwartz and P Vestergaard, Section Editors)

Effects of Diabetes on Bone Material Properties

Authors: Sashank Lekkala, Erik A. Taylor, Heather B. Hunt, Eve Donnelly

Published in: Current Osteoporosis Reports | Issue 6/2019

Login to get access

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.
Literature
1.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
2.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
4.
go back to reference 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.CrossRef 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.CrossRef
5.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
6.
go back to reference Starup-Linde J, Frost M, Vestergaard P, Abrahamsen B. Epidemiology of fractures in diabetes. Calcif Tissue Int. Elsevier Inc. 2017;100:109–21.PubMedCrossRef Starup-Linde J, Frost M, Vestergaard P, Abrahamsen B. Epidemiology of fractures in diabetes. Calcif Tissue Int. Elsevier Inc. 2017;100:109–21.PubMedCrossRef
8.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
9.
go back to reference 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. 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.
10.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
11.
go back to reference •• 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. •• 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.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
13.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
14.
go back to reference Tang SY, Zeenath U, Vashishth D. Effects of non-enzymatic glycation on cancellous bone fragility. Bone. 2007;40:1144–51.PubMedCrossRef Tang SY, Zeenath U, Vashishth D. Effects of non-enzymatic glycation on cancellous bone fragility. Bone. 2007;40:1144–51.PubMedCrossRef
15.
go back to reference 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. 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.
16.
go back to reference Keenan HA, Maddaloni E. Bone Microarchitecture in type 1 diabetes: it is complicated. Curr Osteoporos Rep Springer US. 2016;14:351–8.CrossRef Keenan HA, Maddaloni E. Bone Microarchitecture in type 1 diabetes: it is complicated. Curr Osteoporos Rep Springer US. 2016;14:351–8.CrossRef
17.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
18.
go back to reference 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.CrossRef 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.CrossRef
19.
go back to reference • 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. PubMedCrossRef • 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. PubMedCrossRef
20.
go back to reference 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. 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.
21.
go back to reference 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.CrossRef 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.CrossRef
22.
go back to reference •• 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.PubMedCrossRef •• 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.PubMedCrossRef
23.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
24.
go back to reference 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.CrossRef 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.CrossRef
25.
go back to reference Lenzen S. The mechanisms of alloxan- and streptozotocin-induced diabetes. Diabetologia. 2008;51:216–26.PubMedCrossRef Lenzen S. The mechanisms of alloxan- and streptozotocin-induced diabetes. Diabetologia. 2008;51:216–26.PubMedCrossRef
26.
go back to reference •• 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.PubMedCrossRef •• 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.PubMedCrossRef
27.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
28.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
29.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
30.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
31.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
32.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
33.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
34.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
35.
go back to reference 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. 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.
36.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
37.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
38.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
39.
go back to reference 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. 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.
40.
go back to reference Epstein PN, Overbeek PA, Means AR. Calmodulin-induced early-onset diabetes in transgenic mice. Cell. 1989;58:1067–73.PubMedCrossRef Epstein PN, Overbeek PA, Means AR. Calmodulin-induced early-onset diabetes in transgenic mice. Cell. 1989;58:1067–73.PubMedCrossRef
41.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
42.
go back to reference Lecka-Czernik B. Safety of antidiabetic therapies on bone. Clin Rev Bone Miner Metab. 2013;11:49–58.PubMedCrossRef Lecka-Czernik B. Safety of antidiabetic therapies on bone. Clin Rev Bone Miner Metab. 2013;11:49–58.PubMedCrossRef
43.
go back to reference •• 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. CrossRef •• 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. CrossRef
44.
go back to reference 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. 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.
45.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
46.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
47.
go back to reference •• 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.PubMedCrossRef •• 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.PubMedCrossRef
48.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
49.
go back to reference 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.CrossRef 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.CrossRef
50.
go back to reference 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.CrossRef 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.CrossRef
51.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
52.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
53.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
54.
go back to reference 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. 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.
55.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
56.
go back to reference 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. 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.
57.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
58.
go back to reference Clark JB, Palmer CJ, Shaw WN. The diabetic Zucker fatty rat. Proc Soc Exp Biol Med. 1983;173:68–75.PubMedCrossRef Clark JB, Palmer CJ, Shaw WN. The diabetic Zucker fatty rat. Proc Soc Exp Biol Med. 1983;173:68–75.PubMedCrossRef
59.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
60.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
61.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
62.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
63.
go back to reference 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. 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.
64.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
65.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
66.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
67.
go back to reference Ealey KN, Fonseca D, Archer MC, Ward WE. Bone abnormalities in adolescent leptin-deficient mice. Regul Pept. 2006;136:9–13.PubMedCrossRef Ealey KN, Fonseca D, Archer MC, Ward WE. Bone abnormalities in adolescent leptin-deficient mice. Regul Pept. 2006;136:9–13.PubMedCrossRef
68.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
69.
go back to reference 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. 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.
70.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
71.
go back to reference Kutscher CL, Miller M, Schmalbach NL. Renal deficiency associated with diabetes insipidus in the SWR/J mouse. Physiol Behav. 1975;14:815–8.PubMedCrossRef Kutscher CL, Miller M, Schmalbach NL. Renal deficiency associated with diabetes insipidus in the SWR/J mouse. Physiol Behav. 1975;14:815–8.PubMedCrossRef
72.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
73.
go back to reference 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.CrossRef 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.CrossRef
74.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
75.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
76.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
77.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
Metadata
Title
Effects of Diabetes on Bone Material Properties
Authors
Sashank Lekkala
Erik A. Taylor
Heather B. Hunt
Eve Donnelly
Publication date
01-12-2019
Publisher
Springer US
Published in
Current Osteoporosis Reports / Issue 6/2019
Print ISSN: 1544-1873
Electronic ISSN: 1544-2241
DOI
https://doi.org/10.1007/s11914-019-00538-6

Other articles of this Issue 6/2019

Current Osteoporosis Reports 6/2019 Go to the issue

Cancer-induced Musculoskeletal Diseases (E Keller and J Sterling, Section Editors)

Bone Health in Men with Prostate Cancer: Review Article

Muscle and Bone (L Bonewald and M Hamrick, Section Editors)

Exosomes and Extracellular RNA in Muscle and Bone Aging and Crosstalk

Kidney and Bone (I Salusky and T Nickolas, Section Editors)

Bone Health in Glomerular Kidney Disease

Bone Marrow and Adipose Tissue (G Duque and B Lecka-Czernik, Section Editors)

The Regulation of Marrow Fat by Vitamin D: Molecular Mechanisms and Clinical Implications