Abstract
Wrinkling is a ubiquitous surface phenomenon in many biological tissues and is believed to play an important role in arterial health. As arteries are highly nonlinear, anisotropic, multilayered composite systems, it is necessary to investigate wrinkling incorporating these material characteristics. Several studies have examined surface wrinkling mechanisms with nonlinear isotropic material relationships. Nevertheless, wrinkling associated with anisotropic constitutive models such as Ogden–Gasser–Holzapfel (OGH), which is suitable for soft biological tissues, and in particular arteries, still requires investigation. Here, the effects of OGH parameters such as fibers’ orientation, stiffness, and dispersion on the onset of wrinkling, wrinkle wavelength and amplitude are elucidated through analysis of a bilayer system composed of a thin, stiff neo-Hookean membrane and a soft OGH substrate subjected to compression. Critical contractile strain at which wrinkles occur is predicted using both finite element analysis and analytical linear perturbation approach. Results suggest that besides stiffness mismatch, anisotropic features associated with fiber stiffness and distribution might be used in natural layered systems to adjust wrinkling and subsequent folding behaviors. Further analysis of a bilayer system with fibers in the (x–y) plane subjected to compression in the x direction shows a complex dependence of wrinkling strain and wavelength on fiber angle, stiffness, and dispersion. This behavior is captured by an approximation utilizing the linearized anisotropic properties derived from OGH model. Such understanding of wrinkling in this artery wall-like system will help identify the role of wrinkling mechanisms in biological artery in addition to the design of its synthetic counterparts.
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Acknowledgements
L.P. gratefully acknowledges the support of the Department of Surgery, University of Chicago. N.N., E.T., and S.V. acknowledge support from NSF-1824708 and NIH R56-HL142743-01. S.V. acknowledges support from NSF-1561789. N.N. acknowledges funding from NIH-T32 #HL098036. L.D. gratefully acknowledges the partial support of the following grants: (1) PRIN 2017 20177TTP3S and H2020 FET Proactive project NEUROFIBERS, (2) The Italian MIUR with the “Departments of Excellence” Grant L. 232/2016, (3) ARS01-01384-PROSCAN. L.D. also acknowledges the participation to the NIH R56-HL142743-01 grant although without financial support from it. We are grateful to Simon Watkins and the personnel at the Center for Biological Imaging at the University of Pittsburgh for assistance with imaging. This research was supported in part by the University of Pittsburgh Center for Research Computing through the resources provided.
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Appendices
Appendix 1: Perturbation analysis for wrinkling in neo-Hookean/Ogden–Gasser–Holzapfel Bilayer
Summary of notations
Symbols | Notation meaning |
---|---|
L | Length of the bilayer |
H, h | Substrate and film thicknesses |
\(\lambda _x=\lambda _1, \lambda _2, \lambda _3\) | Applied stretch in x, y, z directions, respectively |
\(\delta\) | Perturbation amplitude |
\(\alpha\) | Parameter determined in the eigenvalue analysis |
\(\lambda , k\) | Wavelength and wave number: \(k=\frac{2\pi }{\lambda }\) |
\(\epsilon\) | The applied strain: \(\epsilon = \frac{\Delta L}{L}\) |
\(\epsilon _{\mathrm{w}}\) | Critical wrinkling strain |
\(k_1\), \(k_2\) | Fiber stiffness, fiber nonlinearity parameter |
\(\kappa\), \(\theta\) | Fiber dispersion, orientation |
\(L_i\) | Unit vector of the direction of the \(i\hbox {th}\) fiber family |
\(\sigma , P,S, N\) | Cauchy, first and second Piola–Kirchhoff, nominal stresses |
F, C, B | Deformation gradient, right and left Cauchy–Green tensor |
\(I_1, I_{4ii}=L_i^{\mathrm{T}}CL_i\) | Invariants of the Cauchy–Green tensor |
\(\mu _{\mathrm{f}}, \mu _{\mathrm{s}}\) | Shear modulus of film and substrate matrix |
\(u_{\mathrm{f}}, v_{\mathrm{f}}, u_{\mathrm{s}}, v_{\mathrm{s}}\) | Displacement in the film and substrate |
Bifurcation of a thin, stiff neo-Hookean layer on an OGH substrate
A bilayer composed of a thin, stiff incompressible neo-Hookean film attached to a soft, incompressible OGH substrate is subjected to compression as shown in Fig. 15.
Assume that the deformation is plane strain and uniform with the deformation state described in Eq. 8.
where (X, Y) are coordinates in the undeformed configuration and (x, y) are the corresponding coordinates in the current configuration. \(\lambda _x\) is the lateral stretch in the x direction.
Consider the perturbation of this homogeneous deformation state with the generic forms of perturbation shown in Eq. 9 for the case of incompressibility (Sun et al. 2012):
where \(\delta<< 1\) is the perturbation amplitude parameter. \(k=\frac{2\pi }{\lambda }\) is the wrinkle wave number, \(\lambda\) is the undeformed-configurational wavelength of the perturbation. \(\alpha\) is a parameter to be determined from the equilibrium condition. p is the hydrostatic pressure for incompressible solids. \(p_0, p_1\) are to be determined from boundary conditions.
The deformation state of each layer in the bilayer due to the above perturbation is a linear combination of each layer ’s eigenmodes when each layer is considered separately and is subjected to the same perturbation. Therefore, in the followings, we first will consider the perturbation of each layer individually. A linear combination of the obtained eigenmodes will then be used to construct the deformation state of each layer in the bilayer system. Continuity conditions at the interface between the two layers and boundary conditions at the free surface are used next to construct an eigenvalue problem to determine the critical onset of wrinkling. Finally, the critical wrinkling strain is determined by numerically solving the resulting eigenvalue problem.
1.1 Analysis of eigenmodes of the neo-Hookean film
The analysis of eigenmodes of a neo-Hookean layer has been carried out in Sun et al. (2012), Cao and Hutchinson (2012), Stewart et al. (2016). Specifically, consider the neo-Hookean strain energy density function given in Eq. 10:
First Piola–Kirchhoff stress can be determined from this strain energy function by taking the derivative with respect to the deformation gradients F and taking into account the hydrostatic pressure due to incompressibility, specifically:
Note that the deformation gradient can be determined from Eq. (9) for the perturbation state. Specifically,
Note that this prescribed deformation gradient already satisfies the incompressibility constraint \(\hbox {det}(F)=1+O(\delta ^2)\).
The first invariant \(I_1\) is the trace of the left Cauchy–Green tensor \(B=F^{\mathrm{T}} F\), which is:
and
With the consideration of incompressibility \(\hbox {det}(F)=1\) or \(F_{11}F_{22}-F_{12}F_{21}=1\), the inverse of the deformation gradient \(F^{-1}\) becomes:
Hence,
Note that for a more compact form, Eq. 16 can be written in the matrix form which can be easily derived from the second Piola Kirchhoff stress \(S=2 \frac{\partial W_{\mathrm{NH}}}{\partial C}\). Specifically,
which are consistent with the stresses using index notations in Eq. 16.
Substituting Eq. 12 into Eq. 16, the calculations result in the following formulae for first Piola–Kirchhoff stress:
The zeroth order (\(\delta =0\)) solution is obtained from Eq. 18, and from the boundary condition for the single layer \(P_{22}^{0}=0\), it is shown that \(p_0=\frac{2\mu _{\mathrm{f}}}{\lambda _x^2}\)
Substituting the stresses into the two following equilibrium equations, the following 2 equations are obtained:
which leads to:
From the first part of Eq. 20, \(p_1=-4\pi \mu _{\mathrm{f}} \alpha \lambda _x^3 (1-\alpha ^2)\). Substituting this \(p_1\) into the second part of Eq. 20 yields a fourth-order equation of \(\alpha\): \(4\pi \mu _{\mathrm{f}} (\lambda _x^4\alpha ^2-1)(1-\alpha ^2)=0\). Solving this equation gives four solutions of \(\alpha\) and hence 4 pairs of solutions \(\left( \alpha _i, p_i\right)\) corresponding with 4 eigenvalues: \(\alpha =1, \alpha =-1, \alpha =1/\lambda _x^2, \alpha =-1/\lambda _x^2\). Substituting each pair of solutions into Eqs. (9) and (18) provides an eigenmode and its stress state for the single neo-Hookean layer subjected to perturbation. Specifically, from Eq. (9), \(\left( u_{fi},v_{fi}\right) , i=\overline{1,4}\) are obtained for the deformation where \(u=x-\lambda _x X, v=y-Y/\lambda _x\). From Eq. (18), tangential and normal tractions \(N_{fi_{21}}, N_{fi_{22}}, i=\overline{1,4}\) are obtained from the nominal stresses, respectively. Nominal stress is determined as \(N= P^{\mathrm{T}}\).
1.2 Analysis of eigenmodes of the OGH substrate
Consider the OGH substrate with the strain energy density function given in Eq. 21.
where the invariant \(I_\mathrm{4mm}=L_{\mathrm{m}}.(C L_{\mathrm{m}})\), \(L_{\mathrm{m}}\) is the unit direction of the fiber family m th, \(C=F^{\mathrm{T}}F\) is the right Cauchy Green tensor.
With the same approach as in Sect. 1.1, the first Piola–Kirchhoff stress can be determined by taking the derivative of the energy with respect to the deformation gradient.
or from the second Piola–Kirchhoff stress S:
where the second Piola–Kirchhoff stress is:
Thus, the first Piola–Kirchhoff stress becomes:
With the given deformation gradient in Eq. (9), components of the first Piola–Kirchhoff stress corresponding to the OGH layer are specified in Eq. 25. Hence, from the zeroth-order solution with the boundary condition \(P_{22}^{0}=0\), \(p_0\) is determined.
Substituting these stresses into the two equilibrium equations (in Eq. 19) and applying the same solution method as in Sect. 1.1, a fourth-order equation in terms of \(\alpha\) is again obtained. Hence, 4 pairs of solutions \(\left( \alpha _i, p_i\right)\) are determined. However, for the substrate, as the undulation dies down as \(Y \rightarrow -\infty\), only 2 solutions with positive values of \(\alpha\) are used to construct eigenmodes for the substrate. Specifically, from Eq. (9), \(\left( u_{si},v_{si}\right) , i=\overline{1,2}\) are obtained for the deformation where \(u=x-\lambda _x X, v=y-Y/\lambda _x\). From Eq. (25), tangential and normal tractions \(N_{si_{21}}, N_{si_{22}}, i=\overline{1,2}\) are obtained from the nominal stresses, respectively. Nominal stress is determined as \(N= P^{\mathrm{T}}\).
Note that for a neo-Hookean layer, the 4 eigenvalues \(\alpha\) are all real values. However, solving the fourth-order equation of eigenvalues \(\alpha\) for the OGH substrate can result in complex solutions. If the eigenvalues \(\alpha\) for the OGH substrate are complex, the four eigenvalues will correspond to two pairs of complex conjugate. As the undulation must vanish when \(Y \rightarrow -\infty\), the pair of complex conjugate with the positive real part is chosen for constructing the eigenmodes for the substrate. Actually, as this is a pair of conjugate eigenvalues \(\alpha\), only one is needed. With this eigenvalue, it is straightforward to compute \(\left( u_{\mathrm{si}},v_{\mathrm{si}}\right)\) and \(N_{{{\text{si}}_{{21}} }} ,N_{{{\text{si}}_{{22}} }}\) which are the corresponding deformation and stresses. As \(\alpha\) is a complex value, these deformation and stress fields are also complex. The real parts and the complex parts of the fields are used now to construct the 2 eigenmodes of the OGH substrate.
Due to the cumbersome formulae, all the calculations for the stresses, equilibrium equations, and eigenvalue problems are implemented in Matlab.
1.3 Linear combination of eigenmodes for the bilayer system
Recall: \(\left( u_{fi},v_{fi}\right) , i=\overline{1,4}\) and \(N_{fi_{21}}, N_{fi_{22}}, i=\overline{1,4}\) as the deformation and stresses, respectively, associated with 4 eigenmodes of the neo-Hookean layer. \(\left( u_{si},v_{si}\right) , i=\overline{1,2}\) and \(N_{si_{21}}, N_{si_{22}}, i=\overline{1,2}\) as the deformation and nominal stresses, respectively, associated with 2 eigenmodes of the OGH layer.
For a bilayer composed of a neo-Hookean film attached to an OGH substrate subjected to the perturbation in Eq. 9, the deformation in each layer is a linear combination of its eigenmodes. In other words, the deformation in the neo-Hookean film can be written as:
The deformation in the OGH substrate can be written as:
where \(A_1,A_2,A_3,A_4,A_5,A_6\) are constant parameters.
1.4 Continuity and boundary conditions—eigenvalue problem for critical strain
At the interface between the film and the substrate, \(Y=0\), continuity in displacements and tractions are enforced which can be written as follows:
At the stress-free face \(Y=h\) of the neo-Hookean film, two boundary conditions for tractions are obtained:
1.5 Critical wrinkling strain determination
By substituting the linear combinations in Eqs. 26, 27 into the system of continuity and boundary conditions in Eqs. 28 and 29, a system of the following forms is obtained:
The critical wrinkling strain, which is minimized over all kh is determined from the nonlinear equations \(\det (F)=0\). This is solved numerically in Matlab.
Appendix 2: Linearization of OGH model for material properties
Figure 16 plots the prediction of \(\frac{{(kh)}^2}{\epsilon _{\mathrm{w}}}\) ratio for bilayers of a neo-Hookean film bonded to an OGH substrate.
When the fiber stiffness \(k_1=0\), the substrate becomes neo-Hookean. The ratio approaches the value of 4 for \(\mu _{\mathrm{f}}>> \mu _{\mathrm{s}}\), which is demonstrated in Fig. 16 for the mismatch modulus ratio \(\mu _{\mathrm{f}}/\mu _{\mathrm{s}}=1000\). At lower mismatch ratio, the value of \(\frac{{(kh)}^2}{\epsilon _{\mathrm{w}}}\) is slightly less than 4. Specifically, with a mismatch modulus ratio \(\mu _{\mathrm{f}}/\mu _{\mathrm{s}}\) of 100 as considered in this paper, \(\frac{{(kh)}^2}{\epsilon _{\mathrm{w}}} \sim 3.7\). When fiber stiffness is nonzero, the renormalization of the substrate stiffness must change the effective value of the substrate stiffness and lead to deviations of this ratio from the constant value. At low fiber stiffness \(k_1/\mu _{\mathrm{s}}=2, k_1/\mu _{\mathrm{s}}=5\), the ratio remains constant around the value of the corresponding neo-Hookean bilayer with the same modulus mismatch \(\mu _{\mathrm{f}}/\mu _{\mathrm{s}}=100\). For higher fiber stiffness \(k_1/\mu _{\mathrm{s}}=10\), the ratio shows some deviations from this constant trend, especially at high values of fiber angle \(\theta\). Note that as angle \(\theta\) increases, the transverse direction y also has higher stiffness. The deviation, therefore, might be attributed to the effect of orthotropic material properties associated with OGH model which become more significant as fibers are stiffer and oriented in the transverse (y) direction. These properties are derived through linearization as follows.
Ogden–Gasser–Holzapfel substrate with strain energy density function:
where \(C=F^{\mathrm{T}}F\) is the right Cauchy–Green tensor, F is the deformation gradient, \(L_i\) is the unit vector of the orientation of the \(i\hbox {th}\) fiber family. Here, \(N=2\) corresponds to two fiber families.
The second Piola–Kirchhoff stress:
Cauchy stress for incompressible case:
where \(B=FF^{\mathrm{T}}\) is the left Cauchy Green tensor.
For two family fibers lying in x–y plane: \(L_1=[c, s, 0]^{\mathrm{T}}, L_2=[c, -s, 0]^{\mathrm{T}}, c=\cos (\theta ), s=\sin (\theta )\) where \(\theta\) is the fiber angle with respect to x-axis.
1.1 Determine longitudinal moduli and Poisson’s ratios
Consider a block made of OGH material being subjected to tension in one direction and free to expand in the other two directions. The deformation gradient F, left Cauchy–Green tensor B, right Cauchy–Green tensor C are described as follows:
where the three stretch ratios are related by incompressibility restriction: \(\lambda _1\lambda _2\lambda _3=1\). Other quantities in Eq. (33) for computing Cauchy stresses become:
Substituting Eqs. (34–40) into Eq. (33), three components of Cauchy stresses for the block being pulled in one direction:
1.1.1 Stretching along the x direction to determine \(E_x, \nu _{xy}, \nu _{xz}\)
Note that the block is pulled in x direction and is free to expand in y and z directions, therefore:
thus, using \(\lambda _3=\frac{1}{\lambda _1\lambda _2}\), they can be written:
Consider small deformation regime, the strains are small and their high order terms can be neglected. Thus, the following approximations can be used to approximate the stresses:
Substituting the approximations in Eq. (44) into Eq. (43), the stresses become:
since \(\sigma _{22}=0\), so we have:
Note that we are pulling in the x direction, so this ratio between the two strains gives the Poisson’s ratio \(\nu _{xy}\). It can be seen that for the case of isotropic material, i.e., \(k_1=0\) or \(\kappa =1/3\), this ratio is equal to 0.5 which is the Poisson’s ratio of isotropic incompressible material.
By substituting \(\epsilon _2\) in terms of \(\epsilon _1\) into \(\sigma _{11}\), we have:
The longitudinal modulus in the x-direction, thus, can be obtained:
Again, for \(k_1=0\) or \(\kappa =1/3\), this modulus reduces to \(E_x=6\mu\) which is the Young modulus value of isotropic, incompressible material.
Note that:
1.1.2 Stretching along the y direction to determine \(E_y, \nu _{yx}, \nu _{yz}\)
With the same approach, the modulus \(E_y\) in y-direction and Poisson’s ratio \(\nu _{yx}\) can be derived by subjecting the block to the tension in y-direction. Specifically,
Thus:
The Poisson’s ratio \(\nu _{yx}\) is therefore,
And the modulus \(E_y\):
The Poisson’s ratio \(\nu _{yz}\) is:
1.1.3 Pulling in the z direction to determine \(E_z, \nu _{zx}, \nu _{zy}\)
When the block is subjected to tension in z direction and is free to expand in x, y directions, the stress state becomes:
Using \(\lambda _2=\frac{1}{\lambda _1\lambda _3}\), Eq. (33) becomes:
Using small deformation approximations:
Substituting Eq. (58) into Eq. (57):
Therefore, the Poisson’s ratio \(\nu _{zx}\) is:
The modulus \(E_z\) is:
Poisson’s ratio \(\nu _{zy}\)
1.2 Apply simple shear stress \(\sigma _{xy}\) to determine shear modulus \(G_{xy}\)
The deformation gradient and all related quantities to compute stress state in this loading case are:
Other quantities in Eq. (50) for computing Cauchy stresses.
Neglecting high order term of \(\gamma\), the shear stress \(\sigma _{xy}\) in Eq. (33) becomes:
Thus, the shear stress \(G_{xy}\) becomes:
With similar approach, the shear moduli \(G_{xz}\), \(G_{yz}\) can also be determined. For fiber plane (x–y), these shear moduli are equal to the value of isotropic case \(G_{yz}=G_{xz}=2\mu\).
Figure 17 illustrates how the longitudinal (\(E_x\)) and transverse (\(E_y\)) stiffnesses vary with respect to the fiber angle \(\theta\) at two values of fiber stiffness \(k_1/\mu _{\mathrm{s}}=5\) and \(k_1/\mu _{\mathrm{s}}=2\).
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Nguyen, N., Nath, N., Deseri, L. et al. Wrinkling instabilities for biologically relevant fiber-reinforced composite materials with a case study of Neo-Hookean/Ogden–Gasser–Holzapfel bilayer. Biomech Model Mechanobiol 19, 2375–2395 (2020). https://doi.org/10.1007/s10237-020-01345-0
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DOI: https://doi.org/10.1007/s10237-020-01345-0