Elastic properties of woven bone: effect of mineral content and collagen fibrils orientation
- 332 Downloads
- 2 Citations
Abstract
Woven bone is a type of tissue that forms mainly during fracture healing or fetal bone development. Its microstructure can be modeled as a composite with a matrix of mineral (hydroxyapatite) and inclusions of collagen fibrils with a more or less random orientation. In the present study, its elastic properties were estimated as a function of composition (degree of mineralization) and fibril orientation. A self-consistent homogenization scheme considering randomness of inclusions’ orientation was used for this purpose. Lacuno-canalicular porosity in the form of periodically distributed void inclusions was also considered. Assuming collagen fibrils to be uniformly oriented in all directions led to an isotropic tissue with a Young’s modulus \(E = 1.90\) GPa, which is of the same order of magnitude as that of woven bone in fracture calluses. By contrast, assuming fibrils to have a preferential orientation resulted in a Young’s modulus in the preferential direction of 9–16 GPa depending on the mineral content of the tissue. These results are consistent with experimental evidence for woven bone in foetuses, where collagen fibrils are aligned to a certain extent.
Keywords
Woven bone Multiscale micromechanical model Homogenization Mineral contentNotes
Acknowledgments
This work was supported by grant DPI2014-58233-P from the Ministerio de Economía y Competitividad (Spain).
References
- Beno T, Yoon Y, Cowin S, Fritton SP (2006) Estimation of bone permeability using accurate microstructural measurements. J Biomech 39(13):2378–2387CrossRefGoogle Scholar
- Benveniste Y (1990) Some remarks on three micromechanical models in composite media. J Appl Mech T ASME 57(2):474–476CrossRefGoogle Scholar
- Bonfield W, Li E (1967) Anisotropy of nonelastic flow in bone. J Appl Phys 38:2450–2455CrossRefGoogle Scholar
- Brighton C, Hunt R (1986) Histochemical localization of calcium in the fracture callus with potassium pyroantimonate: possible role of chondrocyte mitochondrial calcium in callus calcification. J Bone Joint Surg Am 68–A(5):703–715CrossRefGoogle Scholar
- Brighton C, Hunt R (1997) Early histologic and ultrastructural changes in microvessels of periosteal callus. J Orthop Trauma 11(4):244–253CrossRefGoogle Scholar
- Buckwalter J, Glimcher M, Cooper R, Recker R (1995) Bone biology. Part I: structure, blood supply, cells, matrix, and mineralization. J Bone Joint Surg Am 77(8):1256–1275CrossRefGoogle Scholar
- Bunge H (1982) Texture analysis in materials science: mathematical methods. Butterworths, DaytonGoogle Scholar
- Chou P, Carleone J, Hsu C (1972) Elastic constants of layered media. J Compos Mater 6(1):80–93CrossRefGoogle Scholar
- Cowin S (1999) Bone poroelasticity. J Biomech 32:217–238CrossRefGoogle Scholar
- Cowin S, Yang G, Mehrabadi M (1999) Bounds on the effective anisotropic elastic constants. J Elast 57(1):1–24MathSciNetCrossRefMATHGoogle Scholar
- Crolet J, Aoubiza B, Meunier A (1993) Compact bone: numerical simulation of mechanical characteristics. J Biomech 26(6):677–687CrossRefGoogle Scholar
- Currey J (1969) The relationship between the stiffness and the mineral content of bone. J Biomech 2:477–480CrossRefGoogle Scholar
- Cusack S, Miller A (1979) Determination of the elastic constants of collagen by brillouin light scattering. J Mol Biol 135:39–51CrossRefGoogle Scholar
- Deuerling J, Yue W, Espinoza Orías A, Roeder R (2009) Specimen-specific multi-scale model for the anisotropic elastic constants of human cortical bone. J Biomech 42(13):2061–2067CrossRefGoogle Scholar
- Dong X, Guo X (2006) Prediction of cortical bone elastic constants by a two-level micromechanical model using a generalized self-consistent method. J Biomech Eng T ASME 128(3):309–316CrossRefGoogle Scholar
- Eshelby J (1957) The determination of the elastic field of an ellipsoidal inclusion, and related problems. Proc R Soc Lond Ser A 241(1226):376–396MathSciNetCrossRefMATHGoogle Scholar
- Farlay D, Panczer G, Rey C, Delmas P, Boivin G (2010) Mineral maturity and crystallinity index are distinct characteristics of bone mineral. J Bone Miner Metab 28:433–445CrossRefGoogle Scholar
- Ferrari M, Johnson G (1989) Effective elasticities of short-fiber composites with arbitrary orientation distribution. Mech Mater 8(1):67–73CrossRefGoogle Scholar
- Fritsch A, Hellmich C (2007) ’Universal’ microstructural patterns in cortical and trabecular, extracellular and extravascular bone materials: micromechanics-based prediction of anisotropic elasticity. J Theor Biol 244(4):597–620CrossRefGoogle Scholar
- Fritsch A, Dormieux L, Hellmich C (2006) Porous polycrystals built up by uniformly and axisymmetrically oriented needles: homogenization of elastic properties. CR Mec 334:151–157CrossRefMATHGoogle Scholar
- Fritsch A, Hellmich C, Young P (2013) Micromechanics-derived scaling relations for poroelasticity and strength of brittle porous polycrystals. J Appl Mech 80(020):905Google Scholar
- Frost H (1989a) The biology of fracture healing. An overview for clinicians. Part I. Clin Orthop Relat Res 248:283–293Google Scholar
- Frost H (1989b) The biology of fracture healing. An overview for clinicians. Part II. Clin Orthop Relat Res 248:294–309Google Scholar
- García-Aznar J, Rueberg T, Doblaré M (2005) A bone remodelling model coupling microdamage growth and repair by 3D BMU-activity. Biomech Model Mechanobiol 4:147–167CrossRefGoogle Scholar
- García-Rodríguez J (2014) Modelo de remodelación de callo óseo de fractura de fémur humano. PhD thesis, Universidad de Sevilla, Seville, SpainGoogle Scholar
- Gardner T, Stoll T, Marks L, Mishra S, Knothe Tate M (2000) The influence of mechanical stimulus on the pattern of tissue differentiation in a long bone fracture—a FEM study. J Biomech 33(4):415–425CrossRefGoogle Scholar
- Geoffrey H (1972) The biochemistry and physiology of bone, vol 1. Academic Press, New YorkGoogle Scholar
- Ghanbari J, Naghdabadi R (2009) Nonlinear hierarchical multiscale modeling of cortical bone considering its nanoscale microstructure. J Biomech 42(10):1560–1565CrossRefGoogle Scholar
- Gong J, Arnold J, Cohn S (1964) Composition of trabecular and cortical bone. Anat Rec 149:325–332CrossRefGoogle Scholar
- Grant C, Brockwell D, Radford S, Thomson N (2009) Tuning the elastic modulus of hydrated collagen fibrils. Biophys J 97:2985–2992CrossRefGoogle Scholar
- Hashin Z (1968) Assessment of the self-consistent scheme approximation. J Compos Mater 2:284–300CrossRefGoogle Scholar
- Hellmich C, Ulm FJ (2002) Micromechanical model for ultrastructural stiffness of mineralized tissues. J Eng Mech ASCE 128(8):898–908CrossRefGoogle Scholar
- Hellmich C, Barthélémy JF, Dormieux L (2004) Mineral-collagen interactions in elasticity of bone ultrastructure—a continuum micromechanics approach. Eur J Mech A Solid 23(5):783–810CrossRefMATHGoogle Scholar
- Hernandez C, Beaupré G, Keller T, Carter D (2001a) The influence of bone volume fraction and ash fraction on bone strength and modulus. Bone 29(1):74–78CrossRefGoogle Scholar
- Hernandez C, Beaupré G, Marcus R, Carter D (2001b) A theoretical analysis of the contributions of remodeling space, mineralization, and bone balance to changes in bone mineral density during alendronate treatment. Bone 29(6):511–516CrossRefGoogle Scholar
- Hernandez C, Majeska R, Schaffler M (2004) Osteocyte density in woven bone. Bone 35(5):1095–1099CrossRefGoogle Scholar
- Hill R (1965) A self consistent mechanics of composite materials. J Mech Phys Sol 13:213–222CrossRefGoogle Scholar
- Hunt R (2016) Material interaction varies bone strength: mammals.http://www.asknature.org/strategy/6bc0469baa23a29a6b5f9eb6febb75a8. Accessed 10 Mar 2016
- Jackson S, Cartwright A, Lewis D (1978) The morphology of bone mineral crystals. Calcif Tissue Int 25:217–222CrossRefGoogle Scholar
- Katz J (1968) Hard tissue as a composite material—I. Bounds on the elastic behavior. J Biomech 4:455–473CrossRefGoogle Scholar
- Kotha S, Guzelsu N (2007) Tensile behavior of cortical bone: dependence of organic matrix material properties on bone mineral content. J Biomech 40(1):36–45CrossRefGoogle Scholar
- Lees S, Heeley J, Cleary P (1979) A study of some properties of a sample of bovine cortical bone using ultrasound. Calcif Tissue Int 29(2):107–117CrossRefGoogle Scholar
- Leong P, Morgan E (2008) Measurement of fracture callus material properties via nanoindentation. Acta Biomater 4:1569–1575CrossRefGoogle Scholar
- Martínez-Reina J, Domínguez J, García-Aznar J (2011) Effect of porosity and mineral content on the elastic constants of cortical bone: a multiscale approach. Biomech Model Mechanobiol 10(3):309–322CrossRefGoogle Scholar
- McKibbin B (1978) The biology of fracture healing in long bones. J Bone Joint Surg Br 60 B(2):150–162Google Scholar
- Mitchel B, Burr D (1988) Stiffness of compact bone. effect of porosity and density. J Biomech 21:13–16CrossRefGoogle Scholar
- Mora-Macías J (2016) Biomechanics of bone transport: in vivo, ex vivo and numerical characterization. PhD thesis, Universidad de Sevilla, Seville, SpainGoogle Scholar
- Mora-Macías J, Reina-Romo E, Domínguez J (2016) Model of the distraction callus tissue behavior during bone transport based in experiments in vivo. J Mech Behav Biomed Mater 61:419–430CrossRefGoogle Scholar
- Nemat-Nasser S, Hori M (1999) Micromechanics: overall properties of heterogeneous materials. Elsevier, AmsterdamMATHGoogle Scholar
- Parfitt A (1987) Bone remodeling and bone loss: understanding the pathophysiology of osteoporosis. Clin Obstet Gynecol 30(4):789–811CrossRefGoogle Scholar
- Pettermann H, Böhm H, Rammerstorfer F (1997) Some direction-dependent properties of matrix-inclusion type composites with given reinforcement orientation distributions. Compos Part B Eng 28(3):253–265CrossRefGoogle Scholar
- Porter D (2004) Pragmatic multiscale modelling of bone as a natural hybrid nanocomposite. Mat Sci Eng A Struct 365(1–2):38–45CrossRefGoogle Scholar
- Remaggi F, Canè V, Palumbo C, Ferretti M (1998) Histomorphometric study on the osteocyte lacuno-canalicular network in animals of different species. I. Woven-fibered and parallel-fibered bones. Ital J Anat Embryol 103(4):145–155Google Scholar
- Rho J, Kuhn-Spearing L, Zioupos P (1998) Mechanical properties and the hierarchical structure of bone. Med Eng Phys 20:92–102CrossRefGoogle Scholar
- Sasaki N, Matsushima N, Ikawa T, Yamamura H, Fukuda A (1989) Orientation of bone mineral and its role in the anisotropic mechanical properties of bone transverse anisotropy. J Biomech 22:157–164CrossRefGoogle Scholar
- Sevostianov I, Kachanov M (2000) Impact of the porous microstructure on the overall elastic properties of the osteonal cortical bone. J Biomech 33(7):881–888CrossRefGoogle Scholar
- Sfeir C, Ho C, Doll B et al (2005) Fracture repair. In: Lieberman J, Friedlaender G (eds) Bone regeneration and repair. Humana Press Inc, Totowa, pp 21–43CrossRefGoogle Scholar
- Smith J (1960) Collagen fibre patterns in mammalian bone. J Anat 94(3):329–344Google Scholar
- Su X, Feng Q, Cui F, Zhu X (1997) Microstructure and micromechanical properties of the mid-diaphyses of human fetal femurs. Connect Tissue Res 36(3):271–286CrossRefGoogle Scholar
- Su X, Sun K, Cui F, Landis W (2003) Organization of apatite crystals in human woven bone. Bone 32(2):150–162CrossRefGoogle Scholar
- Tiburtius S, Schrof S, Molnár F, Varga P, Peyrin F, Grimal Q, Raum K, Gerisch A (2014) On the elastic properties of mineralized turkey leg tendon tissue: multiscale model and experiment. Biomech Model Mechanobiol 13(5):1003–1023CrossRefGoogle Scholar
- Vetter A, Epari D, Seidel R, Schell H, Fratzl P, Duda G, Weinkamer R (2010) Temporal tissue patterns in bone healing of sheep. J Orthop Res 28(11):1440–1447CrossRefGoogle Scholar
- Vetter A, Liu Y, Witt F et al (2011) The mechanical heterogeneity of the hard callus influences local tissue strains during bone healing: a finite element study based on sheep experiments. J Biomech 44(3):517–523CrossRefGoogle Scholar
- Wang L, Fritton S, Cowin S, Weinbaum S (1999) Fluid pressure relaxation depends upon osteonal microstructure: modeling of an oscillatory bending experiment. J Biomech 32:663–672CrossRefGoogle Scholar
- Wen H, Cui F, Feng Q, Li H, Zhu X (1995) Microstructural investigation of the early external callus after diaphyseal fractures of human long bone. J Struct Biol 114(2):115–122CrossRefGoogle Scholar
- Yang G, Kabel J, Van Rietbergen B, Odgaard A, Huiskes R, Cowin S (1998) Anisotropic Hooke’s law for cancellous bone and wood. J Elast 53(2):125–146CrossRefMATHGoogle Scholar
- Yoon Y, Cowin S (2008a) An estimate of anisotropic poroelastic constants of an osteon. Biomech Model Mechanobiol 7(1):13–26CrossRefGoogle Scholar
- Yoon Y, Cowin S (2008b) The estimated elastic constants for a single bone osteonal lamella. Biomech Model Mechanobiol 7(1):1–11CrossRefGoogle Scholar
- Yoon Y, Yang G, Cowin S (2002) Estimation of the effective transversely isotropic elastic constants of a material from known values of the material’s orthotropic elastic constants. Biomech Model Mechanobiol 1(1):83–93CrossRefGoogle Scholar
- Zhang D, Cowin S (1994) Oscillatory bending of a poroelastic beam. J Mech Phys Solids 42:1575–1599MathSciNetCrossRefMATHGoogle Scholar
- Zhang D, Weinbaum S, Cowin S (1998) Estimates of the peak pressure in bone pore water. J Biomech Eng 120:697–703CrossRefGoogle Scholar
- Zhou H, Shen V, Dempster D, Lindsay R (2001) Continuous parathyroid hormone and estrogen administration increases vertebral cancellous bone volume and cortical width in the estrogen-deficient rat. J Bone Miner Res 16:1300–1307CrossRefGoogle Scholar