Bone intrinsic material and compositional properties in postmenopausal women diagnosed with long-term Type-1 diabetes.

The incidence of diabetes mellitus and the associated complications are growing worldwide, affecting the patients' quality of life and exerting a considerable burden on health systems. Yet, the increase in fracture risk in type 1 diabetes (T1D) patients is not fully captured by bone mineral density (BMD), leading to the hypothesis that alterations in bone quality are responsible for the increased risk. Material/compositional properties are important aspects of bone quality, yet information on human bone material/compositional properties in T1D is rather sparse. The purpose of the present study is to measure both the intrinsic material behaviour by nanoindentation, and material compositional properties by Raman spectroscopy as a function of tissue age and microanatomical location (cement lines) in bone tissue from iliac crest biopsies from postmenopausal women diagnosed with long-term T1D (N = 8), and appropriate sex-, age-, BMD- and clinically-matched controls (postmenopausal women; N = 5). The results suggest elevation of advanced glycation endproducts (AGE) content in the T1D and show significant differences in mineral maturity / crystallinity (MMC) and glycosaminoglycan (GAG) content between the T1D and control groups. Furthermore, both hardness and modulus by nanoindentation are greater in T1D. These data suggest a significant deterioration of material strength properties (toughness) and compositional properties in T1D compared with controls.

[1]  P. Milovanović,et al.  Osteocyte apoptosis and cellular micropetrosis signify skeletal aging in type 1 diabetes. , 2023, Acta biomaterialia.

[2]  J. Nyman,et al.  Effect of ribose incubation on physical, chemical, and mechanical properties of human cortical bone. , 2023, Journal of the mechanical behavior of biomedical materials.

[3]  B. Gludovatz,et al.  Dimorphic Mechanisms of Fragility in Diabetes Mellitus: the Role of Reduced Collagen Fibril Deformation , 2022, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[4]  J. Nyman,et al.  Causative or associative: A critical review of the role of advanced glycation end-products in bone fragility. , 2022, Bone.

[5]  O. Akkus,et al.  Raman spectroscopy–based water measurements identify the origin of MRI T2 signal in human articular cartilage zones and predict histopathologic score , 2021, Journal of biophotonics.

[6]  Xiangcheng Sun Glucose detection through surface-enhanced Raman spectroscopy: A review. , 2021, Analytica chimica acta.

[7]  M. Djuric,et al.  Bone quality analysis of jaw bones in individuals with type 2 diabetes mellitus—post mortem anatomical and microstructural evaluation , 2021, Clinical Oral Investigations.

[8]  R. Recker,et al.  Organic matrix quality discriminates between age- and BMD-matched fracturing versus non-fracturing post-menopausal women: A pilot study. , 2019, Bone.

[9]  D. Burr,et al.  Estrogen depletion alters mineralization regulation mechanisms in an ovariectomized monkey animal model. , 2019, Bone.

[10]  O. Akkus,et al.  Raman spectroscopy-based water content is a negative predictor of articular human cartilage mechanical function. , 2019, Osteoarthritis and cartilage.

[11]  J. Nyman,et al.  Manipulating the Amount and Structure of the Organic Matrix Affects the Water Compartments of Human Cortical Bone , 2019, JBMR plus.

[12]  A. Schwartz,et al.  Bone health in type 1 diabetes , 2018, Current opinion in endocrinology, diabetes, and obesity.

[13]  Jean X. Jiang,et al.  Age‐Related Deterioration of Bone Toughness Is Related to Diminishing Amount of Matrix Glycosaminoglycans (GAGs) , 2018, JBMR plus.

[14]  Kamila Kochan,et al.  Raman and infrared spectroscopy of carbohydrates: A review. , 2017, Spectrochimica acta. Part A, Molecular and biomolecular spectroscopy.

[15]  M. V. D. van der Meulen,et al.  Understanding Bone Strength Is Not Enough , 2017, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[16]  K. Klaushofer,et al.  Vibrational spectroscopic techniques to assess bone quality , 2017, Osteoporosis International.

[17]  R. Recker,et al.  Intrinsic material property differences in bone tissue from patients suffering low-trauma osteoporotic fractures, compared to matched non-fracturing women. , 2017, Bone.

[18]  A. Schwartz,et al.  Mechanisms of diabetes mellitus-induced bone fragility , 2017, Nature Reviews Endocrinology.

[19]  J. Nyman,et al.  Tissue-Level Mechanical Properties of Bone Contributing to Fracture Risk , 2016, Current Osteoporosis Reports.

[20]  Alexander J. Makowski,et al.  Changes in the Fracture Resistance of Bone with the Progression of Type 2 Diabetes in the ZDSD Rat , 2016, Calcified Tissue International.

[21]  D. Vashishth,et al.  Advanced Glycation Endproducts and Bone Material Properties in Type 1 Diabetic Mice , 2016, PloS one.

[22]  F. Glorieux,et al.  Aging Versus Postmenopausal Osteoporosis: Bone Composition and Maturation Kinetics at Actively‐Forming Trabecular Surfaces of Female Subjects Aged 1 to 84 Years , 2016, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[23]  R. Recker,et al.  Nonenzymatic Glycation and Degree of Mineralization Are Higher in Bone From Fractured Patients With Type 1 Diabetes Mellitus , 2016, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[24]  P. Fratzl,et al.  Osmotically driven tensile stress in collagen-based mineralized tissues. , 2015, Journal of the mechanical behavior of biomedical materials.

[25]  M. Buehler,et al.  Influence of cross-link structure, density and mechanical properties in the mesoscale deformation mechanisms of collagen fibrils , 2015, Journal of the mechanical behavior of biomedical materials.

[26]  J. Snell-Bergeon,et al.  Type 1 diabetes and risk of fracture: meta‐analysis and review of the literature , 2015, Diabetic medicine : a journal of the British Diabetic Association.

[27]  Alexander J. Makowski,et al.  Identifying Novel Clinical Surrogates to Assess Human Bone Fracture Toughness , 2015, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[28]  W. R. Thompson,et al.  The dependences of osteocyte network on bone compartment, age, and disease , 2015, Bone Research.

[29]  P. Fratzl,et al.  Fragility of Bone Material Controlled by Internal Interfaces , 2015, Calcified Tissue International.

[30]  J. Nyman,et al.  Changes in skeletal collagen cross-links and matrix hydration in high- and low-turnover chronic kidney disease , 2015, Osteoporosis International.

[31]  Shu-Wei Chang,et al.  Osmotic pressure induced tensile forces in tendon collagen , 2015, Nature Communications.

[32]  Ozan Akkus,et al.  Molecular spectroscopic identification of the water compartments in bone. , 2014, Bone.

[33]  R. Recker,et al.  Transmenopausal Changes in Trabecular Bone Quality , 2014, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[34]  Qianjin Feng,et al.  An ultrasound study of altered hydration behaviour of proteoglycan-degraded articular cartilage , 2013, BMC Musculoskeletal Disorders.

[35]  H. Malluche,et al.  Low-energy fractures without low T-scores characteristic of osteoporosis: a possible bone matrix disorder. , 2013, The Journal of bone and joint surgery. American volume.

[36]  J. Kanis,et al.  Standardized nomenclature, symbols, and units for bone histomorphometry: A 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee , 2013, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[37]  P. Fratzl,et al.  Bone material properties in premenopausal women with idiopathic osteoporosis , 2012, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[38]  Susannah P. Fritton,et al.  Alterations in the osteocyte lacunar-canalicular microenvironment due to estrogen deficiency. , 2012, Bone.

[39]  D. Towler,et al.  Arterial calcification and bone physiology: role of the bone–vascular axis , 2012, Nature Reviews Endocrinology.

[40]  Philip Kollmannsberger,et al.  How Linear Tension Converts to Curvature: Geometric Control of Bone Tissue Growth , 2012, PloS one.

[41]  W. R. Thompson,et al.  Perlecan/Hspg2 Deficiency Alters the Pericellular Space of the Lacunocanalicular System Surrounding Osteocytic Processes in Cortical Bone , 2010, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[42]  David M Maahs,et al.  Epidemiology of type 1 diabetes. , 2010, Endocrinology and metabolism clinics of North America.

[43]  Sonja Gamsjaeger,et al.  Cortical bone composition and orientation as a function of animal and tissue age in mice by Raman spectroscopy. , 2010, Bone.

[44]  J. Dunlop,et al.  Two stages in three-dimensional in vitro growth of tissue generated by osteoblastlike cells , 2010, Biointerphases.

[45]  R. Recker,et al.  Use of FTIR Spectroscopic Imaging to Identify Parameters Associated With Fragility Fracture , 2009, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[46]  D. Burr,et al.  Changes in non-enzymatic glycation and its association with altered mechanical properties following 1-year treatment with risedronate or alendronate , 2009, Osteoporosis International.

[47]  Eve Donnelly,et al.  Effects of tissue age on bone tissue material composition and nanomechanical properties in the rat cortex. , 2009, Journal of biomedical materials research. Part A.

[48]  Anil T Ahuja,et al.  Compromised Bone Marrow Perfusion in Osteoporosis , 2008, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[49]  Peter Fratzl,et al.  The effect of geometry on three-dimensional tissue growth , 2008, Journal of The Royal Society Interface.

[50]  P. Fratzl,et al.  Three-dimensional growth behavior of osteoblasts on biomimetic hydroxylapatite scaffolds. , 2007, Journal of biomedical materials research. Part A.

[51]  D. Vashishth,et al.  Effects of non-enzymatic glycation on cancellous bone fragility. , 2007, Bone.

[52]  P. Vestergaard,et al.  Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes—a meta-analysis , 2007, Osteoporosis International.

[53]  Paul Roschger,et al.  Biomimetic mineral-organic composite scaffolds with controlled internal architecture , 2005, Journal of materials science. Materials in medicine.

[54]  D. Donley,et al.  Bone mineral and collagen quality in iliac crest biopsies of patients given teriparatide: new results from the fracture prevention trial. , 2005, The Journal of clinical endocrinology and metabolism.

[55]  S. Vannucci,et al.  Advanced glycation end products and RAGE: a common thread in aging, diabetes, neurodegeneration, and inflammation. , 2005, Glycobiology.

[56]  R. McCreery,et al.  Raman Spectroscopy for Chemical Analysis: McCreery/Raman Spectroscopy , 2005 .

[57]  J. Eisman,et al.  Bone Resorption and Osteoporotic Fractures in Elderly Men: The Dubbo Osteoporosis Epidemiology Study , 2004, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[58]  A. Boskey,et al.  Bone Fragility and Collagen Cross‐Links , 2004, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[59]  Himadri S. Gupta,et al.  Structure and mechanical quality of the collagen–mineral nano-composite in bone , 2004 .

[60]  S. Coppersmith,et al.  Spectroscopically Determined Collagen Pyr/deH-DHLNL Cross-Link Ratio and Crystallinity Indices Differ Markedly in Recombinant Congenic Mice with Divergent Calculated Bone Tissue Strength , 2003, Connective tissue research.

[61]  J. Baynes,et al.  Role of the Maillard Reaction in Aging of Tissue Proteins , 1998, The Journal of Biological Chemistry.

[62]  J. Díez,et al.  Epidemiology of fractures of the proximal femur associated with osteoporosis in Barcelona, Spain , 1989, Calcified Tissue International.

[63]  J. Currey,et al.  The relationship between the stiffness and the mineral content of bone. , 1969, Journal of biomechanics.

[64]  Ozan Akkus,et al.  Shortwave-infrared Raman spectroscopic classification of water fractions in articular cartilage ex vivo , 2018, Journal of biomedical optics.

[65]  L. Hiebert Proteoglycans and Diabetes. , 2017, Current pharmaceutical design.

[66]  Philip Kollmannsberger,et al.  Geometry as a Factor for Tissue Growth: Towards Shape Optimization of Tissue Engineering Scaffolds , 2013, Advanced healthcare materials.

[67]  J. Nyman,et al.  The influence of water removal on the strength and toughness of cortical bone. , 2006, Journal of biomechanics.