Microstructural fatigue fracture behavior of glycated cortical bone.
Cortical bone
Critical energy release rate
Fatigue fracture
Glycation
Phase field fracture
Journal
Medical & biological engineering & computing
ISSN: 1741-0444
Titre abrégé: Med Biol Eng Comput
Pays: United States
ID NLM: 7704869
Informations de publication
Date de publication:
Nov 2023
Nov 2023
Historique:
received:
15
01
2023
accepted:
29
07
2023
medline:
23
10
2023
pubmed:
16
8
2023
entrez:
15
8
2023
Statut:
ppublish
Résumé
The current study aims to simulate fatigue microdamage accumulation in glycated cortical bone with increased advanced glycation end-products (AGEs) using a phase field fatigue framework. We link the material degradation in the fracture toughness of cortical bone to the high levels of AGEs in this tissue. We simulate fatigue fracture in 2D models of cortical bone microstructure extracted from human tibias. The results present that the mismatch between the critical energy release rate of microstructural features (e.g., osteons and interstitial tissue) can alter crack initiation and propagation patterns. Moreover, the high AGEs content through the increased mismatch ratio can cause the activation or deactivation of bone toughening mechanisms under cyclic loading. The fatigue fracture simulations also show that the lifetime of diabetic cortical bone samples can be dependent on the geometry of microstructural features and the mismatch ratio between the features. Additionally, the results indicate that the trapped cracks in cement lines in the diabetic cortical microstructure can prevent further crack growth under cyclic loading. The present findings show that alterations in the materials heterogeneity of microstructural features can change the fatigue fracture response, lifetime, and fragility of cortical bone with high AGEs contents. Cortical bone models are created from microscopy images taken from the cortical cross-section of human tibias. Increased glycation contents in the cortical bone sample can change the crack growth trajectories.
Identifiants
pubmed: 37582979
doi: 10.1007/s11517-023-02901-3
pii: 10.1007/s11517-023-02901-3
doi:
Substances chimiques
Glycation End Products, Advanced
0
Glycopyrrolate
V92SO9WP2I
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3021-3034Subventions
Organisme : National Science Foundation
ID : CMMI-2143422
Commentaires et corrections
Type : ErratumIn
Informations de copyright
© 2023. International Federation for Medical and Biological Engineering.
Références
Acevedo C, Stadelmann VA, Pioletti DP, Alliston T, Ritchie RO (2018) Fatigue as the missing link between bone fragility and fracture. Nature Biomed Eng 2(2):62–71
doi: 10.1038/s41551-017-0183-9
Lodge CJ, Sha S, Yousef ASE, MacEachern C (2020) Stress fractures in the young adult hip. J Orthop Trauma 34(2):95–100
doi: 10.1016/j.mporth.2020.01.006
Iwamoto J, Takeda T (2003) Stress fractures in athletes: review of 196 cases. J Orthop Sci 8(3):273–278
pubmed: 12768465
doi: 10.1007/s10776-002-0632-5
Meurman K, Elfving S (1980) Stress fracture in soldiers: a multifocal bone disorder. a comparative radiological and scintigraphic study. Radiology 134(2):483–487
pubmed: 7352236
doi: 10.1148/radiology.134.2.7352236
Breer S, Krause M, Marshall RP, Oheim R, Amling M, Barvencik F (2012) Stress fractures in elderly patients. Int Orthop 36(12):2581–2587
pubmed: 23138969
pmcid: 3508041
doi: 10.1007/s00264-012-1708-1
Carpintero P, Berral FJ, Baena P, Garcia-Frasquet A, Lancho JL (1997) Delayed diagnosis of fatigue fractures in the elderly. Am J Sports Med 25(5):659–662
pubmed: 9302472
doi: 10.1177/036354659702500512
Colopy S, Benz-Dean J, Barrett J, Sample S, Lu Y, Danova N et al (2004) Response of the osteocyte syncytium adjacent to and distant from linear microcracks during adaptation to cyclic fatigue loading. Bone 35(4):881–891
pubmed: 15454095
doi: 10.1016/j.bone.2004.05.024
Burr DB, Forwood MR, Fyhrie DP, Martin RB, Schaffler MB, Turner CH (1997) Bone microdamage and skeletal fragility in osteoporotic and stress fractures. J Bone Mineral Res 12(1):6–15
doi: 10.1359/jbmr.1997.12.1.6
Seref-Ferlengez Z, Kennedy OD, Schaffler MB (2015) Bone microdamage, remodeling and bone fragility: how much damage is too much damage? BoneKEy reports 4
Nyman JS, Makowski AJ (2012) The contribution of the extracellular matrix to the fracture resistance of bone. Current osteoporos Rep 10(2):169–177
doi: 10.1007/s11914-012-0101-8
Vashishth D (2009) Advanced glycation end-products and bone fractures. Ibms Bonekey 6(8):268
pubmed: 27158323
pmcid: 4856156
doi: 10.1138/20090390
Karim L, Bouxsein ML (2016) Effect of type 2 diabetes-related non-enzymatic glycation on bone biomechanical properties. Bone 82:21–27
pubmed: 26211993
doi: 10.1016/j.bone.2015.07.028
Collier T, Nash A, Birch H, De Leeuw N (2018) Effect on the mechanical properties of type i collagen of intra-molecular lysine-arginine derived advanced glycation end-product cross-linking. J Biomech 67:55–61
pubmed: 29254633
pmcid: 5773075
doi: 10.1016/j.jbiomech.2017.11.021
Merlo K, Aaronson J, Vaidya R, Rezaee T, Chalivendra V, Karim L (2020) In vitro-induced high sugar environments deteriorate human cortical bone elastic modulus and fracture toughness. J Orthop Res 38(5):972–983
pubmed: 31793028
doi: 10.1002/jor.24543
Saito M, Mori S, Mashiba T, Komatsubara S, Marumo K (2008) Collagen maturity, glycation induced-pentosidine, and mineralization are increased following 3-year treatment with incadronate in dogs. Osteoporos Int 19(9):1343–1354
pubmed: 18373056
doi: 10.1007/s00198-008-0585-3
Tang S, Vashishth D (2010) Non-enzymatic glycation alters microdamage formation in human cancellous bone. Bone 46(1):148–154
pubmed: 19747573
doi: 10.1016/j.bone.2009.09.003
Nguyen HQ, Nguyen TNT, Pham TQD, Nguyen VD, Tran XV, Dao TT (2021) Crack propagation in the tibia bone within total knee replacement using the extended finite element method. Appl Sci 11(10):4435
doi: 10.3390/app11104435
Kahla RB, Barkaoui A, Merzouki T (2018) Age-related mechanical strength evolution of trabecular bone under fatigue damage for both genders: Fracture risk evaluation. J Mech Behav Biomed Mater 84:64–73
pubmed: 29751273
doi: 10.1016/j.jmbbm.2018.05.006
Hambli R, Hattab N (2013) Application of neural network and finite element method for multiscale prediction of bone fatigue crack growth in cancellous bone. Multiscale Computer Modeling in Biomechanics and Biomedical Engineering 3–30
Waanders D, Janssen D, Miller MA, Mann KA, Verdonschot N (2009) Fatigue creep damage at the cement-bone interface: an experimental and a micro-mechanical finite element study. J Biomech 42(15):2513–2519
pubmed: 19682690
pmcid: 2783955
doi: 10.1016/j.jbiomech.2009.07.014
Nguyen TT, Yvonnet J, Zhu QZ, Bornert M, Chateau C (2015) A phase field method to simulate crack nucleation and propagation in strongly heterogeneous materials from direct imaging of their microstructure. Eng Fract Mech 139:18–39
doi: 10.1016/j.engfracmech.2015.03.045
Remmers JJ, de Borst R, Needleman A (2008) The simulation of dynamic crack propagation using the cohesive segments method. J Mech Phys Solids 56(1):70–92
doi: 10.1016/j.jmps.2007.08.003
Moës N, Dolbow J, Belytschko T (1999) A finite element method for crack growth without remeshing. Int J Num Methods Eng 46(1):131–150
doi: 10.1002/(SICI)1097-0207(19990910)46:1<131::AID-NME726>3.0.CO;2-J
Ghorashi SS, Valizadeh N, Mohammadi S, Rabczuk T (2015) T-spline based xiga for fracture analysis of orthotropic media. Comput Struct 147:138–146
doi: 10.1016/j.compstruc.2014.09.017
Natarajan S, Annabattula RK, Martínez-Pañeda E et al (2019) Phase field modelling of crack propagation in functionally graded materials. Compos Part B: Eng 169:239–248
doi: 10.1016/j.compositesb.2019.04.003
Ambati M, Gerasimov T, De Lorenzis L (2015) Phase-field modeling of ductile fracture. Comput Mech 55(5):1017–1040
doi: 10.1007/s00466-015-1151-4
Miehe C, Hofacker M, Welschinger F (2010) A phase field model for rate-independent crack propagation: robust algorithmic implementation based on operator splits. Comput Methods Appl Mech Eng 199(45–48):2765–2778
doi: 10.1016/j.cma.2010.04.011
Wu JY, Nguyen VP, Nguyen CT, Sutula D, Bordas S, Sinaie S (2018) Phase field modeling of fracture. Advances in applied mechancis: multi-scale theory and computation 52
de Borst R, Verhoosel CV (2016) Gradient damage vs phase-field approaches for fracture: similarities and differences. Comput Methods Appl Mech Eng 312:78–94
doi: 10.1016/j.cma.2016.05.015
Goswami S, Anitescu C, Chakraborty S, Rabczuk T (2020) Transfer learning enhanced physics informed neural network for phase-field modeling of fracture. Theor Appl Fract Mech 106:102447
doi: 10.1016/j.tafmec.2019.102447
Msekh MA, Cuong N, Zi G, Areias P, Zhuang X, Rabczuk T (2018) Fracture properties prediction of clay/epoxy nanocomposites with interphase zones using a phase field model. Eng Fract Mech 188:287–299
doi: 10.1016/j.engfracmech.2017.08.002
Maghami E, Moore JP, Josephson TO, Najafi AR (2022) Damage analysis of human cortical bone under compressive and tensile loadings. Comput Methods Biomech Biomed Eng 25(3):342–357
doi: 10.1080/10255842.2021.2023135
Josephson TO, Moore JP, Maghami E, Freeman TA, Najafi AR (2022) Computational study of the mechanical influence of lacunae and perilacunar zones in cortical bone microcracking. J Mech Behav Biomed Mater 126:105029
pubmed: 34971951
doi: 10.1016/j.jmbbm.2021.105029
Maghami E, Josephson TO, Moore JP, Rezaee T, Freeman TA, Karim L et al (2021) Fracture behavior of human cortical bone: role of advanced glycation end-products and microstructural features. J Biomech 125:110600
pubmed: 34246065
doi: 10.1016/j.jbiomech.2021.110600
Maghami E, Pejman R, Najafi AR (2021) Fracture micromechanics of human dentin: a microscale numerical model. J Mech Behav Biomed Mater 114:104171
pubmed: 33218927
doi: 10.1016/j.jmbbm.2020.104171
Nguyen L, Stoter S, Baum T, Kirschke J, Ruess M, Yosibash Z et al (2017) Phase-field boundary conditions for the voxel finite cell method: surface-free stress analysis of ct-based bone structures. Int J Numer Methods Biomed Eng 33(12):e2880
doi: 10.1002/cnm.2880
Maghami E, Najafi AR (2022) Influence of age-related changes on crack growth trajectories and toughening mechanisms in human dentin. Dent Mater 38(11):1789–1800
pubmed: 36184336
doi: 10.1016/j.dental.2022.09.009
Wu C, Fang J, Zhang Z, Entezari A, Sun G, Swain MV et al (2020) Fracture modeling of brittle biomaterials by the phase-field method. Eng Fract Mech 224:106752
doi: 10.1016/j.engfracmech.2019.106752
Pinto DC, Pace ED (2015) A silver-stain modification of standard histological slide preparation for use in anthropology analyses. J Forensic Sci 60(2):391–398
pubmed: 25583347
doi: 10.1111/1556-4029.12697
Gustafsson A, Khayyeri H, Wallin M, Isaksson H (2019) An interface damage model that captures crack propagation at the microscale in cortical bone using xfem. J Mech Behav Biomed Mater 90:556–565
pubmed: 30472565
doi: 10.1016/j.jmbbm.2018.09.045
Saffar KP, Najafi AR, Moeinzadeh MH, Sudak LJ (2013) A finite element study of crack behavior for carbon nanotube reinforced bone cement. World J Mech 3(5A):13–21
doi: 10.4236/wjm.2013.35A003
Abdel-Wahab AA, Maligno AR, Silberschmidt VV (2012) Micro-scale modelling of bovine cortical bone fracture: analysis of crack propagation and microstructure using x-fem. Comput Mater Sci 52(1):128–135
doi: 10.1016/j.commatsci.2011.01.021
Fan Z, Swadener J, Rho J, Roy M, Pharr G (2002) Anisotropic properties of human tibial cortical bone as measured by nanoindentation. J Orthop Res 20(4):806–810
pubmed: 12168671
doi: 10.1016/S0736-0266(01)00186-3
Fratzl P, Gupta H, Paschalis E, Roschger P (2004) Structure and mechanical quality of the collagen-mineral nano-composite in bone. J Mater Chem 14(14):2115–2123
doi: 10.1039/B402005G
Giner E, Belda R, Arango C, Vercher-Martínez A, Tarancón JE, Fuenmayor FJ (2017) Calculation of the critical energy release rate gc of the cement line in cortical bone combining experimental tests and finite element models. Eng Fract Mech 184:168–182
doi: 10.1016/j.engfracmech.2017.08.026
Brown CU, Yeni YN, Norman TL (2000) Fracture toughness is dependent on bone location–a study of the femoral neck, femoral shaft, and the tibial shaft. J Biomed Mater Res: Off J Soc Biomater Jpn Soc Biomater 49(3):380–389
doi: 10.1002/(SICI)1097-4636(20000305)49:3<380::AID-JBM11>3.0.CO;2-W
Tang S, Vashishth D (2011) The relative contributions of non-enzymatic glycation and cortical porosity on the fracture toughness of aging bone. J Biomech 44(2):330–336
pubmed: 21056419
doi: 10.1016/j.jbiomech.2010.10.016
Bourdin B, Francfort GA, Marigo JJ (2008) The variational approach to fracture. J Elast 91(1–3):5–148
doi: 10.1007/s10659-007-9107-3
Kristensen PK, Martínez-Pañeda E (2020) Phase field fracture modelling using quasi-newton methods and a new adaptive step scheme. Theor Appl Fract Mech 107:102446
doi: 10.1016/j.tafmec.2019.102446
Alessi R, Vidoli S, De Lorenzis L (2018) A phenomenological approach to fatigue with a variational phase-field model: the one-dimensional case. Eng Fract Mech 190:53–73
doi: 10.1016/j.engfracmech.2017.11.036
Carrara P, Ambati M, Alessi R, De Lorenzis L (2020) A framework to model the fatigue behavior of brittle materials based on a variational phase-field approach. Comput Methods Appl Mech Eng 361:112731
doi: 10.1016/j.cma.2019.112731
Burr DB (2019) Changes in bone matrix properties with aging. Bone 120:85–93
pubmed: 30315999
doi: 10.1016/j.bone.2018.10.010
Li J, Gong H (2021) Fatigue behavior of cortical bone: a review. Acta Mech Sinica 37(3):516–526
Varvani-Farahani A, Najmi H (2010) A damage assessment model for cadaveric cortical bone subjected to fatigue cycles. Int J Fatigue 32(2):420–427
doi: 10.1016/j.ijfatigue.2009.08.002
Taylor D (2018) Observations on the role of fracture mechanics in biology and medicine. Eng Fract Mech 187:422–430
doi: 10.1016/j.engfracmech.2018.01.002
Wegst UG, Bai H, Saiz E, Tomsia AP, Ritchie RO (2015) Bioinspired structural materials. Nature Mater 14(1):23–36
Carter D, Hayes WC, Schurman DJ (1976) Fatigue life of compact bone–ii. effects of microstructure and density. J Biomech 9(4):211-218
pubmed: 1262355
doi: 10.1016/0021-9290(76)90006-3
Poundarik AA, Wu PC, Evis Z, Sroga GE, Ural A, Rubin M et al (2015) A direct role of collagen glycation in bone fracture. J Mech Behav Biomed Mater 52:120–130
pubmed: 26530231
pmcid: 4651854
doi: 10.1016/j.jmbbm.2015.08.012
Carando S, Barbos MP, Ascenzi A, Boyde A (1989) Orientation of collagen in human tibial and fibular shaft and possible correlation with mechanical properties. Bone 10(2):139–142
pubmed: 2765311
doi: 10.1016/8756-3282(89)90012-4
Mischinski S, Ural A (2013) Interaction of microstructure and microcrack growth in cortical bone: a finite element study. Comput Methods Biomech Biomed Eng 16(1):81–94
doi: 10.1080/10255842.2011.607444
Budyn E, Hoc T, Jonvaux J (2008) Fracture strength assessment and aging signs detection in human cortical bone using an x-fem multiple scale approach. Comput Mech 42(4):579–591
doi: 10.1007/s00466-008-0283-1
Li S, Abdel-Wahab A, Demirci E, Silberschmidt VV (2014) Fracture process in cortical bone: X-fem analysis of microstructured models. In: Fracture phenomena in nature and technology Springer, pp 43–55