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Identification of a constitutive law for trabecular bone samples under remodeling in the framework of irreversible thermodynamics

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Abstract

We construct in the present paper constitutive models for bone remodeling based on micromechanical analyses at the scale of a representative unit cell (RUC) including a porous trabecular microstructure. The time evolution of the microstructure is simulated as a surface remodeling process by relating the surface growth remodeling velocity to a surface driving force incorporating a (surface) Eshelby tensor. Adopting the framework of irreversible thermodynamics, a 2D constitutive model based on the setting up of the free energy density and a dissipation potential is identified from FE simulations performed over a unit cell representative of the trabecular architecture obtained from real bone microstructures. The static and evolutive effective properties of bone at the scale of the RUC are obtained by combining a methodology for the evaluation of the average kinematic and static variables over a prototype unit cell and numerical simulations with controlled imposed first gradient rates. The formulated effective growth constitutive law at the scale of the homogenized set of trabeculae within the RUC is of viscoplastic type and relates the average growth strain rate to the homogenized stress tensor. The postulated model includes a power law function of an effective stress chosen to depend on the first and second stress invariants. The model coefficients are calibrated from a set of virtual testing performed over the RUC subjected to a sequence of loadings. Numerical simulations show that overall bone growth does not show any growth kinematic hardening. The obtained results quantify the strength and importance of different types of external loads (uniaxial tension, simple shear, and biaxial loading) on the overall remodeling process and the development of elastic deformations within the RUC.

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Abbreviations

\(\mathbf{C}\) :

Tensor of effective elastic moduli

\(\overline{\mathbf{D}} \) :

Average rate of deformation tensor

\(\overline{\mathbf{D}} _\mathrm{e} \) :

Average elastic rate of deformation tensor

\(\overline{\mathbf{D}} _\mathrm{g} \) :

Average rate of growth tensor

\(\mathbf{E}\left( x \right) \) :

Average kinematic first gradient tensors

\(E_x,E_y\) :

Effective homogenized moduli in x, y, respectively

\({\varvec{\varepsilon }}\) :

Classical infinitesimal strain tensor

\(\overline{{{\varvec{\upvarepsilon }} }_\mathrm{e} } ,\overline{{{\varvec{\upvarepsilon }}}_\mathrm{g}}\) :

A average elastic and growth tensors (small strain)

\(\mathbf{f}_{\mathrm{S}} \) :

Surface force field

\({\tilde{\mathbf{F}}}\) :

Surface deformation gradient

\({\tilde{\mathbf{F}}}_\mathbf{a}\) :

Surface accommodation mapping

\({\tilde{\mathbf{F}}}_{\mathrm{g}}\) :

Surface growth mapping

\(\mathbf{g}_\mathrm{a} \) :

Acceleration due to gravity

\(\mathbf{I}_\mathrm{S} \) :

Surface identity tensor

J :

Jacobean of the total deformation gradient

\(\tilde{J}_{\mathrm{a}}, \tilde{J}_{\mathrm{g}}\) :

Determinants of the accommodation and growth tensors

\({J}_{1}, {J}_{2}\),:

First and second invariants of the applied stress

\(\mathbf{K}\) :

Curvature tensor of the surface

\(\tilde{K}\) :

Constant measuring the rate of surface adaptation

\(\overline{\mathbf{L}} _\mathrm{g} \) :

Average growth velocity gradient

\(\mathbf{N}\) :

Unit normal vector

\(\overline{{\dot{p}}} _\mathrm{g} \) :

Effective growth strain rate (second invariant of \(\overline{\mathbf{D}} _\mathrm{g} )\)

\({R}_{\mathrm{g}}\) :

Isotropic hardening

\({\tilde{\mathbf{T}}}\) :

Surface nominal stress

\(\mathbf{u}=\left( {u_x ,u_y } \right) \) :

Displacement vector in 2D

\(U_{{\mathrm{RUC}}}\) :

Strain energy over the unit cell

\(V_{{\mathrm{RUC}}} =\left| \Omega \right| \) :

Volume of the RUC

\(\mathbf{V}\) :

Total velocity field

\({\tilde{\mathbf{V}}}_{\mathrm{g}} \) :

Surface growth velocity field

\(v_{xy},v_{yx}\) :

In-plane effective Poisson’s ratios

\(W^{\mathrm{S}}\) :

Surface energy density

\(\mathbf{X}_{\mathrm{g}}\) :

Growth position

\(\varphi ^{*}\) :

Dissipation potential

\(\rho _{\mathrm{S}} \) :

Surface density of nutrients

\({r\rho }^{\mathrm{eff}}\) :

Effective density

\(\dot{\rho }^{\mathrm{eff}}\) :

Rate of effective density

\(\sigma ^{\mathrm{eq}}\) :

Equivalent stress

\({{\varvec{\upsigma }} }^{\mathrm{ext}}\) :

Applied stress tensor

\(\sigma ^{\mathrm{g}}\) :

Growth threshold corresponding to the minimal effective stress

\(\tilde{{\varvec{\Sigma }}}_{a}\) :

Surface Eshelby stress

\(\Gamma ^{{\mathrm{S}}}\) :

Rate of mass surface growth

\(\Omega _{\mathrm{g}} \) :

The scalar growth potential

\(\alpha ,\beta ,K,N\) :

Four material parameters of the constitutive growth model

\(\psi _\mathrm{e} \) :

Elastic part of the free energy density

\(\psi _\mathrm{g} \) :

Growth part of the free energy density

References

  1. Ambrosi, D., Mollica, F.: On the mechanics of a growing tumor. Int. J. Eng. Sci. 40, 1297–1316 (2002)

    Article  MathSciNet  MATH  Google Scholar 

  2. Brynk, T., Hellmich, C., Fritsch, A., Zysset, P., Eberhardsteiner, J.: Experimental poromechanics of trabecular bone strength: role of Terzaghi’s effective stress and of tissue level stress fluctuations. J. Biomech. 44(3), 501–8 (2010)

    Article  Google Scholar 

  3. Carter, D.R.: Mechanical loading histories and cortical bone remodeling. Calcif. Tissue Int. 36(Suppl 1), S19S24 (1984)

    Google Scholar 

  4. Carter, D., Hayes, W.: The compressive behavior of bone as a two-phase porous structure. J. Bone Joint Surg. 59, 954–962 (1977)

    Article  Google Scholar 

  5. Cowin, S., Van Buskirk, W.C.: Surface bone remodeling induced by a medullary pin. J. Biomech. 12(4), 269–76 (1979)

    Article  Google Scholar 

  6. Cowin, S.C., Hegedus, D.H.: Bone remodeling I: theory of adaptive elasticity. J. Elast. 6, 313–325 (1976)

    Article  MathSciNet  MATH  Google Scholar 

  7. Crockett, J.C., Rogers, M.J., Coxon, F.P., Hocking, L.J., Helfrich, M.H.: Bone remodeling at a glance. J. Cell Sci. 124, 991–998 (2011)

    Article  Google Scholar 

  8. Drozdov, A.D.: Volumetric growth of viscoelastic solids. Mech. Solids 25, 99–106 (1990)

    Google Scholar 

  9. Entov, V.M.: Mechanical model of scoliosis. Mech. Solids 18, 199–206 (1983)

    Google Scholar 

  10. Epstein, M., Maugin, G.A.: Thermomechanics of volumetric growth in uniform bodies. Int. J. Plast. 16, 951–978 (2000)

    Article  MATH  Google Scholar 

  11. Ganghoffer, J.F.: Mechanical modeling of growth considering domain variation—part II: volumetric and surface growth involving Eshelby tensors. J. Mech. Phys. Solids 58(9), 1434–1459 (2010)

    Article  ADS  MATH  Google Scholar 

  12. Ganghoffer, J.F.: A contribution to the mechanics and thermodynamics of surface growth, application to bone remodeling. Int. J. Eng. Sci. 50(1), 166–191 (2012)

    Article  MathSciNet  Google Scholar 

  13. Ganghoffer, J.F.: A kinematically and thermodynamically consistent volumetric growth model based on the stress-free configuration. Int. J. Solids Struct. 50, 3446–3459 (2013)

    Article  Google Scholar 

  14. Ganghoffer, J.F., Haussy, B.: Mechanical modeling of growth considering domain variation. Part I: Constitutive framework. Int. J. Solids Struct. 42(15), 4311–4337 (2005)

    Article  MATH  Google Scholar 

  15. Ganghoffer, J.F., Sokolowski, J.: A micromechanical approach to volumetric and surface growth in the framework of shape optimization. Int. J. Eng. Sci. 74, 207–226 (2014)

    Article  MathSciNet  Google Scholar 

  16. Goda, I., Ganghoffer, J.F.: Identification of couple-stress moduli of vertebral trabecular bone based on the 3D internal architectures. J. Mech. Behav. Biomed. Mater. 51, 99–118 (2015)

    Article  Google Scholar 

  17. Goda, I., Ganghoffer, J.F., Maurice, G.: Combined bone internal and external remodeling based on Eshelby stress. Int. J. Solids Struct. 94–95, 138–157 (2016)

    Article  Google Scholar 

  18. Goda, I., Rahouadj, R., Ganghoffer, J.-F., Kerdjoudj, H., Siad, L.: 3D couple-stress moduli of porous polymeric biomaterials using \(\mu \)CT image stack and FE characterization. Int. J. Eng. Sci. 100, 25–44 (2016)

    Article  MathSciNet  Google Scholar 

  19. Hadjidakis, D.J., Androulakis, I.I.: Bone remodeling. Ann. N. Y. Acad. Sci. 1092, 385–396 (2006)

    Article  ADS  Google Scholar 

  20. Halgrin, J., Chaari, F., Markiewicz, É.: On the effect of marrow in the mechanical behavior and crush response of trabecular bone. J. Mech. Behav. Biomed. Mater. 5, 231–237 (2012)

    Article  Google Scholar 

  21. Hellmich, C., Ulm, F.: Drained and undrained poroelastic properties of healthy and pathological bone: a poro-micromechanical investigation. Transp. Porous Media 58, 243–268 (2005)

    Article  Google Scholar 

  22. Hill, R.: Elastic properties of reinforced solids: some theoretical considerations. J. Mech. Phys. Solids 11, 357–372 (1963)

    Article  ADS  MATH  Google Scholar 

  23. Hsu, F.-H.: The influences of mechanical loads on the form of a growing elastic body. J. Biomech. 1, 303–311 (1968)

    Article  Google Scholar 

  24. Humphrey, J.D., Rajagopal, K.R.: A constrained mixture model for growth and remodeling of soft tissues. Math. Models Methods Appl. Sci. 12(3), 407–430 (2002)

    Article  MathSciNet  MATH  Google Scholar 

  25. Khosla, S., Westendorf, J.J., Oursler, M.J.: Oursler Building bone to reverse osteoporosis and repair fractures. J. Clin. Investig. 118, 421–428 (2008)

    Article  Google Scholar 

  26. Lacroix, D.: Computational methods in the modeling of scaffolds for tissue engineering. In: Geris, L. (ed.) Computational Modeling in Tissue Engineering, pp. 107–126. Springer, Berlin (2013)

    Google Scholar 

  27. Lemaitre, J., Chaboche, J.L.: Mécanique des matériaux solides. Dunod, Paris (2009)

    Google Scholar 

  28. Linde, F., Hvid, I., Madsen, F.: The effect of specimen geometry on the mechanical behaviour of trabecular bone specimens. J. Biomech. 25(4), 359–368 (1992)

    Article  Google Scholar 

  29. Louna, Z., Goda, I., Ganghoffer, J.F., Benhadid, S.: Formulation of an effective growth response of trabecular bone based on micromechanical analyses at the trabecular level. Arch. Appl. Mech. 87(3), 457–477 (2017)

    Article  ADS  Google Scholar 

  30. Lubarda, V.A., Hoger, A.: On the mechanics of solids with a growing mass. Int. J. Solids Struct. 39, 4627–4664 (2002)

    Article  MATH  Google Scholar 

  31. McNamara, L.M., Prendergast, P.J.: Bone remodelling algorithms incorporating both strain and microdamage stimuli. J. Biomech. 40, 1381–1391 (2007)

    Article  Google Scholar 

  32. Morgan, E., Keaveny, T.: Dependence of yield strain of human trabecular bone on anatomic site. J. Biomech. 34, 569–577 (2001)

    Article  Google Scholar 

  33. Olivares, L., Lacroix, D.: Computational methods in the modeling of scaffolds for tissue engineering. In: Geris, L. (ed.) Computational Modeling in Tissue Engineering, pp. 107–126. Springer, Berlin (2013)

    Google Scholar 

  34. Prendergast, P.J., Taylor, D.: Prediction of bone adaptation using damage accumulation. J. Biomech. 27, 1067–1076 (1994)

    Article  Google Scholar 

  35. Raisz, L.G.: Physiology and pathophysiology of bone remodeling. Clin. Chem. 45, 1353–1358 (1999)

    Google Scholar 

  36. Rajagopal, K.R.: Multiple natural configurations in continuum mechanics. Report 6, Institute Computational and Applied Mechanics (1995)

  37. Rajagopal, K.R., Srinivasa, A.R.: Mechanics of the inelastic behavior of materials. Part I: theoretical underpinnings. Int. J. Plast. 14, 945–967 (1998)

    Article  MATH  Google Scholar 

  38. Rodriguez, E.K., Hoger, A., McCullogh, A.D.: Stress-dependent finite growth in soft elastic tissues. J. Biomech. 27(4), 455–467 (1994)

    Article  Google Scholar 

  39. Skalak, R.: Growth as a finite displacement field. In: Carlsson, D.E., Shield, R.T. (eds.) Proceedings of the IUTAM Symposium on Finite Elasticity, Martinus Nijhoff, The Hague, pp. 347–355 (1981)

  40. Skalak, R., Farrow, D.A., Hoger, A.: Kinematics of surface growth. J. Math. Biol. 35, 869–907 (1997)

    Article  MathSciNet  MATH  Google Scholar 

  41. Stein, A.A.: The deformation of a rod of growing biological material under longitudinal compression. J. Appl. Math. Mech. 59, 139–146 (1995)

    Article  ADS  MathSciNet  Google Scholar 

  42. Taber, L.A.: Biomechanics of growth, remodeling, and morphogenesis. Appl. Mech. Rev. 48, 487 (1995)

    Article  ADS  Google Scholar 

  43. Thompson, D.W.: On Growth and Form, 2nd edn. Dover, Mineola (1992)

    Book  Google Scholar 

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Correspondence to Jean-François Ganghoffer.

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Communicated by Andreas Öchsner.

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Louna, Z., Goda, I. & Ganghoffer, JF. Identification of a constitutive law for trabecular bone samples under remodeling in the framework of irreversible thermodynamics. Continuum Mech. Thermodyn. 30, 529–551 (2018). https://doi.org/10.1007/s00161-018-0619-9

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