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. Author manuscript; available in PMC: 2017 Aug 1.
Published in final edited form as: J Mech Behav Biomed Mater. 2016 Apr 22;61:554–566. doi: 10.1016/j.jmbbm.2016.04.024

On the accuracy and fitting of transversely isotropic material models

Yuan Feng a,b,*, Ruth J Okamoto c, Guy M Genin c,d,e, Philip V Bayly c,d,e
PMCID: PMC4917463  NIHMSID: NIHMS780875  PMID: 27136091

Abstract

Fiber reinforced structures are central to the form and function of biological tissues. Hyperelastic, transversely isotropic material models are used widely in the modeling and simulation of such tissues. Many of the most widely used models involve strain energy functions that include one or both pseudo-invariants (I4 or I5) to incorporate energy stored in the fibers. In a previous study we showed that both of these invariants must be included in the strain energy function if the material model is to reduce correctly to the well-known framework of transversely isotropic linear elasticity in the limit of small deformations. Even with such a model, fitting of parameters is a challenge. Here, by evaluating the relative roles of I4 and I5 in the responses to simple loadings, we identify loading scenarios in which previous models accounting for only one of these invariants can be expected to provide accurate estimation of material response, and identify mechanical tests that have special utility for fitting of transversely isotropic constitutive models. Results provide guidance for fitting of transversely isotropic constitutive models and for interpretation of the predictions of these models.

Keywords: Biological material, Anisotropic material, Constitutive behavior, Transversely isotropic constitutive model

1. Introduction

Fiber-reinforced structure is typical of many soft biological tissues, including skeletal muscle (Morrow et al., 2010), myocardium (Humphrey, 2002; Taber, 2004), brain stem (Ning et al., 2006), white matter (Feng et al., 2013), ligament and tendon (Dourte et al., 2008; Lake et al., 2010; Thomopoulos and Genin, 2012; Weiss et al., 1996). To understand the mechanical behavior of these soft biological tissues, reliable material models are needed. Here, we focus on transversely isotropic hyperelastic models for such tissues. The constitutive properties are described by a strain energy function ψ, which is a function of certain measures of deformation (Spencer, 1984), some of which (I1, I2, I3) are invariant under arbitrary rotations and others of which (I4, I5) are invariant under rotations about the fiber axis. The most general strain energy function form for a transversely isotropic material contains all of the five invariants (Taber, 2004):

ψ=ψ(I1,I2,I3,I4,I5). (1)

It is common to separate the strain energy function into two parts: the strain energy of the isotropic base material ψisotropic and the strain energy associated with the anisotropic fiber components ψanisotropic (Feng et al., 2013; Horgan and Saccomandi, 2005; Merodio and Ogden, 2003a,b, 2005; Murphy, 2013; Pierce et al., 2013; Qiu and Pence, 1997; Swedberg et al., 2014):

ψ=ψisotropic(I1,I2,I3)+ψanisotropic(I4,I5). (2)

A broad range of forms have been proposed for ψ (Table 1). Most proposed ψanisotropic terms are expressed as a function of only one invariant, either with I4 or I5. Polignone and Horgan (1993) originally proposed a general quadratic form in terms of I4 for ψanisotropic. Following this idea, many studies have focused on the strain energy function with variations of the form. Notably, the ψanisotropic term considering tension-only fibers (e.g. I4−1) is of primary interest for many biological applications such as ligaments and tendon tissues (Horgan and Saccomandi, 2005; Murphy, 2013). We study here the quadratic form of Qiu and Pence (1997), F(I4) = μγ(I4−1)2/2, which we term the F(I4) model in which μ is a modulus that also appears in the isotropic part of ψ and γ is a dimensionless scaling factor. To study the effect of I5, we evaluate the second term of the model of Feng et al. (2013), G(I5¯)=μϕI5¯/2, in which ϕ is a dimensionless scaling factor and I5¯=I5¯I4¯2, where the overbar indicates a variable related to the distortional component of the deformation gradient, as described in detail in Section 2. We term this the G(I5) model, and note that many other forms for the role of I5 have been proposed (Horgan and Saccomandi, 2005; Merodio and Ogden, 2005; Murphy, 2013).

Table 1.

A summary of incompressible, transversely isotropic, hyperelastic models.a

ψisotropic ψanisotropic Volumetric termb
Spencer (1984) μTtr(ε2)
2(μLμT)Aε2A+12β(AεA)2
12λ(trε)2
Polignone and Horgan (1993)c
μ2(I13)
μ2a(I522I5+1)
Weiss et al. (1996)
C1(I¯13)+C2(I¯23)
C3(exp(I¯43)I¯4)
Qiu and Pence (1997)
μ2(I13)
μγ2(I41)2
Taber (2004)
b1eb2(I13)
b3(I41)m
Merodio and Ogden (2005)
μ2(I13)
μγ2(I51)2
Horgan and Saccomandi (2005)d
μ2(I13)
{μIJmI((I41)+JmIln(1I41JmI))μI2JmIIln(1(I41)2JmII)μII2JmIIIln(1(I51)2JmIII)
Schröder et al. (2005)
α1I1J13+α2I2J13α3ln(J)+α4(I3α5+1I3α52)
α6(I5I1I4+I2)+α7I4α8J13+α9(I1I4I5)+α10I4α11
Lu and Zhang (2005)e
12k4(β22)+k2exp(c(λ¯1)2)+12k3(β11)
k12(J1)2
Ning et al. (2006)
C10(I¯13)
θ2(I4¯1)2
1D(J1)2
Velardi et al. (2006)
2μα2(λ1α+λ2α+λ3α3)
2kμα2(I4α/2+I4α/43)
λ1λ2λ3 = 1
Gasser et al. (2006)
μ2(I¯13)
k12k2[exp{k2[κI¯1+(13κ)I¯41]2}1]
Chatelin et al. (2012)
C10(I¯13)+C01(I¯23)
Wfibersd(I¯4)
12KlnJ2
Feng et al. (2013)
μ2(I¯13)
μζ2(I4¯1)2+μϕ2I5¯
κ2(J1)2
Destrade et al. (2015); Horgan and Murphy (2015); Murphy (2013)d
μT2[α(I13)+(1α)(I23)]
{μTμL2(2I4I51)+EL+μT4μL8(I41)2μTμL2(2I4I51)+EL+μT4μL32(I51)2μTμL2(2I4I51)+EL+μT4μL16(I41)(I51)
Swedberg et al. (2014)
μ2(I13)
c12c2(exp(c2(λ1)2)1)
f
a

In the incompressible case the isochoric invariants I1¯, I2¯, I4¯, I5¯ are effectively equal to I1, I2, I4, I5. We keep the original form of each strain energy function.

b

Explicit volumetric term is shown here if it is written out specifically in the original references.

c

The invariant I5 in the formulation corresponds to the definition of I4 in this paper.

d

Strain energy function is composed of one of the forms of ψanisotropic.

e

The formulation used a multiplicative decomposition of the deformation that factor out the volumetric strain and fiber stretch. λ¯=J1/3λ, β1=1λ4C2NNβ2=λJtrCλJλC2NN.

f

μlnI3+κ2(ln(I5I1I4+I2I42(mv0)e4m(λ1)))2.

Both Feng et al. (2013) and Murphy (2013) noted that both anisotropic invariants I4 and I5 are needed in the strain energy function to correctly describe tensile and shear moduli differences in the small strain regime. Models containing only a F(I4) or G(I5) term cannot capture this behavior. Both Murphy (2013) and Feng et al. (2013) proposed the form:

ψ=μ2(I13)+H(I4,I5). (3)

Note that Destrade et al. (2013) also showed at least three invariants are needed to model the transversely isotropic materials (Destrade et al., 2013). Here, we study the model of Feng et al. (2013), with H(I4,I5)=μζ(I4 ¯1)2/2+μϕI5¯. We term this the H(I4, I5) model.

Fitting hyperelastic models to experimental data is crucial in material characterization (Ogden et al., 2004). To estimate the model parameters, it is necessary to gain an understanding of model behaviors in commonly used experimental test such as biaxial and shear tests. Thus, an analysis of canonical large deformations in those standard tests is warranted to identify the tests that are most useful in characterizing the dependence of constitutive response on these invariants.

In this article, we study the mechanical responses of the F(I4), G(I5¯), and H(I4, I5) models. Our goal is to answer two questions. First, under what circumstances can F(I4) and G(I5¯) provide adequate models of material behavior, despite being unable to model linear elastic transversely isotropic material behavior? Second, what mechanical loading tests best emphasize the independent roles of I4 and I5¯ in material behavior, and are therefore best suited to fitting of model parameters? In the following, we study the influence of the two anisotropic invariants under different loading conditions, and develop insights into the experiments that can best fit model parameters.

2. Material model

Defining X as the position vector of a material particle in the undeformed configuration and x as its position vector in the deformed configuration, then the deformation gradient is F=xX. The corresponding right and left Cauchy–Green deformation tensors are C = FTF, b = FFT. The corresponding principal invariants are (Holzapfel, 2000; Spencer, 1984):

I1=tr(C),I2=12[(tr(C))2tr(C2)],andI3=det(C)=J2, (4)

where J = det F is the volume ratio between the deformed and undeformed configurations. Let A be the unit vector of the fiber direction, then two additional “anisotropic” invariants (or pseudo-invariants) I4 and I5, invariant under rotations about A, are introduced to describe the effects of fiber reinforcement (Spencer, 1984):

I4=A·CA,I5=A·C2A. (5)

The deformed fiber unit vector is a = FA. Its magnitude represents the fiber stretch λ=I4. Using the general form of the strain energy function of Eq. (1), the Cauchy stress is given by

σ=2J1[ψ1b+ψ2(I1bb2)+I3ψ3I+ψ4aa+ψ5(aba+aba)], (6)

where ψi = ∂ψ/∂Ii (i = 1, 2, 3, 4, 5), and I is the identity tensor.

If we align fiber direction A with x1 in a (x1, x2, x3) Cartesian frame (Fig. 1), then I4 = C11 and I5=C112+C122+C132. Thus I5 contains information not only about fiber stretch, but also about fiber shearing (Merodio and Ogden, 2005). To isolate and characterize the fiber shear information, the fiber stretch component can be subtracted from I5 (Feng et al., 2013; see also: Taber (2004)):

I5=C122+C132=I5I42. (7)

Fig. 1.

Fig. 1

Basic model of a transversely isotropic material in Cartesian coordinates. Vector A indicates the fiber direction in the reference configuration. The plane of symmetry is perpendicular to x1.

This definition of I5 is similar to the corresponding invariant used by Taber (2004), who described the fiber reinforcement effect in terms of Lagrange strain E. Thus, the fiber reinforcing model function H(I4, I5) can be expressed as H(I4,I5). If we rewrite the general form of Eq. (1) in terms of I5, then the Cauchy stress of ψ=ψ(I1,I2,I3,I4,I5) is

σ=2J1[ψ1b+ψ2(I1bb2)+I3ψ3I+(ψ42ψ5)aa+ψ5(aba+aba)], (8)

where ψi = ∂ψ/∂Ii (i = 1, 2, 3, 4), ψ5=ψ/I5, and I is the identity tensor.

We consider the simple incompressible, transversely isotropic model with the strain energy function of Feng et al. (2013):

ψ=μ2[(I13)+ζ(I41)2+ϕI5]. (9)

This model is proposed as the simplest that captures anisotropy in tension and shear in small deformations (Feng et al., 2013; Namani et al., 2012). In this model, μ is the isotropic shear modulus in a Neo Hookean strain energy function ψisotropic, and ζ and ϕ are dimensionless scaling parameters related to fiber stretch and shear. Fibers are assumed to bear load in compression as well as tension. When ϕ = 0, the model reduces to the F(I4) model.

Eqs. (8) and (9) yield the Cauchy stress:

σ=pI+μb+2μ[(ζϕ)I4ζ]aa+μϕ(aba+baa), (10)

where p is an arbitrary hydrostatic stress according to the incompressibility condition J = 1.

For numerical simulations of nearly incompressible material behavior, it is convenient to decompose the deformation gradient into distortional and dilatational components F¯=J1/3F. The decoupled right and left Cauchy–Green deformation tensors are C¯=F¯TF¯, b=FF¯T. The corresponding modified principal invariants and pesudo-invariants are

I¯1=tr(C¯)=J23I1,I¯2=12[(tr(C¯))2tr(C¯2)]=J43I2,I¯4=AC¯A=J23I4,I¯5=AC¯2A=J43I5,I¯5=I¯5I¯42=J43I5 (11)

For nearly incompressible material, a decoupled form of strain energy function is used:

ψ¯=μ2[(I¯13)+ζ(I¯41)2+ϕI5¯]+U(J), (12)

where the volumetric term U(J)=κ2(J1)2 is the penalty term used to enforce near-incompressibility.

Use Eqs. (8) and (12) the corresponding Cauchy stress in terms of decoupled invariants is

σ=[κ(J1)2μJ1(16I¯ 1+ζ3I¯4(I¯41)+ϕ3I5¯)]I+μJ1b¯+2μJ1[(ζϕ)I¯4ζ]a¯a¯+μϕJ1(a¯b¯a¯+b¯a¯a¯),

where a¯=J1/3a and b¯=J2/3b. Note that in numerical implementation, the decoupled formulations are only applicable to incompressible materials. As for compressible material, the coupled form is recommended to prevent possible unrealistic results (Nolan et al., 2014; Sansour, 2008).

3. Responses to simple loadings

3.1. Uniaxial and biaxial loadings

Tensile (Babaei et al., 2015a,b; Jacquemoud et al., 2007; Tan et al., 2005) and biaxial mechanical tests (Sacks, 2000; Sacks, 1999) are widely used to characterize soft biological tissues. In this section, the response of a uniaxial deformation parallel (Fig. 2a) or perpendicular (b) to the fiber direction is studied. The biaxial response (Fig. 2c) of the model is also studied. If the unit vector of the fiber direction A is given as A = x1, the deformation gradient F and Cauchy stress σ are given in matrix form

[Fij]=[λ1000λ2000λ3],[σij]=[σ11000σ22000σ33] (14)

where λi, i = 1, 2, 3, are the principal stretches. In the incompressible case, we have

λ1λ2λ3=1. (15)

Fig. 2.

Fig. 2

Simple deformation of a transversely isotropic material: (a) uniaxial deformation along the fiber direction; (b) uniaxial deformation perpendicular to the fiber direction; (c) biaxial deformation. (d) simple shear in the fiber direction; (e) simple shear transverse to the fiber direction; (f) general simple shear in (x1, x2) plane with shear angle θ with respect to x1 axis. λ1, λ2 are the stretch ratios, k is the magnitude of shear displacement, the cube has a unit length of 1 for each side.

The pseudo-invariants based on Eqs. (5) and (7) are

I4=λ12,I5=λ14,I5=0, (16)

where I5=0 indicates no shear deformation. From Eq. (8), the Cauchy stress components are

{σ11=μλ12(2ζλ122ζ+1)pσ22=μλ22pσ33=μλ32p. (17)

where p is the Lagrange multiplier constraining the material incompressibility.

3.1.1. Uniaxial loading in the fiber direction

In the case of uniaxial load in the fiber direction, σ22 = σ33 = 0, with Eqs. (15)–(17), we have

λ2=λ3=λ112,p=μλ1. (18)

The non-zero Cauchy stress component σ11 (Fig. 3a) is

σ11=μλ12(2ζλ122ζ+1)μλ1. (19)
Fig. 3.

Fig. 3

Uniaxial stress response. (a) σ11 vs. fiber stretch λ1, and (b) fiber stretch λ2 vs. λ1 when the material is under uniaxial deformation parallel to the fiber direction. (c) σ22 vs. fiber stretch λ2, and (d) fiber stretch λ1 vs.λ2 when the material is under uniaxial loading transverse to the fiber direction. The shear anisotropy parameter ϕ does not affect the stress response in these cases. The model responses for ζ =0.1 and ζ =1 are very close. An interval of [1/λmax, λmax ] is adopted for x-axis in all the plots with λmax =1.5.

From Eq. (19), we can observe that in uniaxial loading, the Cauchy stress is related to stretch by the shear modulus μ and the parameter ζ associated with the fiber stretch pseudo-invariant I4. The parameter ϕ which is associated with I5 does not affect the Cauchy stress in uniaxial loading. The uniaxial response is a strong function of ζ (Fig. 3a), but the stretch ratios in the plane of isotropy (λ2 and λ3), which are constrained by incompressibility (Eq. (18)), are independent of the material parameters (Fig. 3b).

3.1.2. Uniaxial loading transverse to the fiber direction

When uniaxial loading is applied along the x2 axis, we have σ11 = σ33 = 0. With Eqs. (15)–(17)

p=μλ12(2ζλ122ζ+1)=μλ32. (20)

Under the incompressibility condition λ1λ2λ3 = 1, the relationship between stretch ratios λ1 and λ2 can be obtained from Eq. (20)

λ2=1λ122ζλ122ζ+1. (21)

The non-zero Cauchy stress component σ22 is

σ22=μ(λ221λ12λ22). (22)

A numerical solution is obtained from Eqs. (21) and (22) (Fig. 3c and d).

3.1.3. Biaxial loading in the (x1, x2) plane

Taber (2004) presented an analytical solution for biaxial stretch of a transversely isotropic material. Following his approach, the response of the planar biaxial stretch of the transversely isotropic material of Eq. (9), with fibers along the x1 axis, is

[σij]=[μ(λ122ζλ12+2ζλ141λ12λ22)000μ(λ221λ12λ22)0000] (23)

The stress-stretch curves for equibiaxial stretch (Fig. 4a and b) reveal that the stress perpendicular to the fiber direction is not affected by fiber reinforcement. This is useful in equibiaxial calibration experiments because the material parameters ζ and μ can be determined by probing the stresses σ11 and σ22.

Fig. 4.

Fig. 4

(a) σ11and (b) σ22 vs. fiber stretch λ1 = λ2, when the material is under equal biaxial deformation. An interval of [1/λmax, λmax ] is adopted for x-axis in all the plots with λmax =1.5.

Note that because, in all the above analyses, the model responses when ζ =0.1 and ζ =1 are qualitatively very similar, we use only ζ ={0, 1, 10} for illustration in the following analyses.

3.2. Shear deformations

For homogeneous shear deformation, we denote the amount of shear as the displacement magnitude k imposed on the top of a sheared unit cube. For transversely isotropic materials, the shearing deformation can be separated into (i) shear in the plane of isotropy ((x2, x3) plane) and (ii) shear in the plane perpendicular to the plane of isotropy ((x1, x2) plane). For the transversely isotropic material in Eq. (9), when shear deformation is in the plane of isotropy, I4 = I5 = 1. In this case, the fiber reinforcement effect is minimum; the material behaves like Neo Hookean material. The shear stress σ23 = μk, and the strain energy function in terms of k is ψ^(k)=μ2k2. In this study, we focus on the analyses of shear deformation in a plane perpendicular to the plane of isotropy. Shearing in the direction of fibers (Fig. 2d), transverse to the fibers (e), and in an arbitrary direction in the (x1, x2) plane (f) with incompressibility constraint are analyzed. A condition of plane strain in the (x1, x2) plane is assumed for simplicity.

3.2.1. Simple shear displacement in a fiber plane

When shear deformation is produced by imposing a displacement k in the fiber direction (Fig. 2d), the deformation gradient tensor F and Cauchy–Green tensor C are

[Fij]=[1k0010001],[Cij]=[1k0kk2+10001]. (24)

The corresponding pseudo-invariants I4 and I5 are

I4=1,I5=1+k2,I5=k2. (25)

The corresponding Cauchy stress components are

[σij]=μ[2k23(2ϕ+1)k(ϕ+1)0k(ϕ+1)k23(2ϕ+1)000k23(2ϕ+1)]. (26)

The stress response as a function of k is shown in Fig. 5. We observe that ζ does not affect the Cauchy stress, which indicates that the fibers are not stretched when the shearing displacement is imposed in the fiber direction. However I5 still captures the shearing information when k is nonzero. ϕ affects all the Cauchy stress components.

Fig. 5.

Fig. 5

Stress response to simple shear displacement parallel to the fiber direction for ϕ=0, ϕ=1, and ϕ=10. The parameter ζ, which is related to the fiber stretch, does not influence the response. The shear stress complies with the linear response of the Neo Hookean material when ϕ=0.

If also under a plane stress condition (σ33 = 0), the Cauchy stress tensor σ is

[σij]=μ[k2(2ϕ+1)k(ϕ+1)0k(ϕ+1)0 0000]. (27)

If the strain energy function is written in terms of k (Eqs. (4), (9) and (25))

ψ^(k)=μ2k2(1+ϕ), (28)

then

σ12=ψ^(k)k. (29)

From Eqs. (27) and (28), we observe that: (i) σ11, σ22 and σ33 are even functions of k; (ii) σ12 is an odd function of k; (iii) the parameter ζ, which governs stresses due to fiber stretch, is not included in either the stress response or the strain energy change. Only the parameter ϕ affects the stress response.

3.2.2. Simple shear displacement transverse to the fiber direction

When the simple shear deformation is imposed with displacement transverse to the fiber (Fig. 2e), the deformation gradient tensor F and Cauchy–Green tensor C are

[Fij]=[100k10001],[Cij]=[k2+1k0k10001]. (30)

The corresponding pseudo-invariants I4 and I5 are

I4=k2+1,I5=(k2+1)2+k2,I5=k2. (31)

We observe that if the amount of shear k>0 and I4>1, the fibers are stretched. Also, I5 is nonzero only when k is nonzero. Based on Eq. (8), the Cauchy stress is

[σij]=μ·[k23(2ζk2+2ϕ4ζ+1)k(2ζk2+ϕ+1)0k(2ζk2+ϕ+1)2k23(2ζk2+2ϕζ+1)000k23(2ζk2+2ϕ+2ζ+1)]. (32)

The stress response as a function of k is shown in Fig. 6.

Fig. 6.

Fig. 6

Stress response to simple shear displacement transverse to the fiber direction for ζ =0, ζ =1, and ζ =10. (a) ϕ=1, and (b) ϕ=10.

If plane stress condition is assumed (σ33 = 0), the Cauchy stress tensor σ is

[σij]=μ[2ζk2k(2ζk2+ϕ+1)0k(2ζk2+ϕ+1)k2(2ζk2+2ϕ+1)0000], (33)

If the strain energy function is written in terms of k (Eqs. (4), (9) and (31))

ψ^(k)=μ2k2(1+ϕ+ζk2), (34)

then

σ12=ψ^(k)k. (35)

From Eqs. (33) and (34), we observe that: (i) σ11, σ22 and σ33 are even functions of k; (ii) σ12 is an odd function of k; (iii) both ζ and ϕ are included in the stress and strain energy term.

3.2.3. General simple shear in the (x1; x2))plane

If simple shear is applied in the (x1; x2) plane, with shearing direction in an angle θ to the x1 axis (Fig. 2f), then we set up the material coordinates (x¯1,x¯2,x¯3) following (Horgan and Saccomandi, 2005; Merodio and Ogden, 2005; Qiu and Pence, 1997):

{x¯1=cosθx1+sinθx2x¯2=sinθx1+cosθx2x¯3=x3, (36)

where the shearing direction is parallel to x¯1 axis. The deformation gradient F, and the right Cauchy-Green tensor C in the coordinates (x¯1,x¯2,x¯3) are the same as Eq. (24). Using Eq. (36) to transform F and C into (x1; x2; x3) coordinates

[Fij]=[1ksinθcosθkcos2θ0ksin2θ1+ksinθcosθ0001],[Cij]=[k2sin2θksin2θ+1kcos2θk2sinθcosθ0kcos2θk2sinθcosθkcos2θ+ksin2θ+10001]. (37)

The pseudo-invariants are

I4=k2sin2θksin2θ+1,I5=(kcos2θk2sinθcosθ)2+(k 2sin2θksin2θ+1)2,I5=(kcos2θk2sinθcosθ)2. (38)

It is easy to verify that I5=C1220, which captures the shearing information when k is nonzero(Merodio and Ogden, 2005). I5 increases with k when θ is 0, π4, 3π8, (Fig. 7). When θ is π8, I5 is a concave function, with an inflection point at k = 1. The normalized Cauchy stress in terms of material parameters ζ and ϕ and the shearing direction θ is shown in Appendix A. A plot of the Cauchy stress components σ11, σ22, σ33 and σ12 against the amount of shear k with θ=π4 and 3π8 shows that the stress response could be non-monotonic (Fig. 8 and Fig. 9). The stress responses are monotonic when ζ is 0 or 1 and ϕ is 1. However, when ζ and ϕ become larger, especially when ζ=ϕ=10, the non-monotonic effect appears in all stress components. The nonzero components of Cauchy stress tensor in plane stress condition are also shown in Appendix A.

Fig. 7.

Fig. 7

I5 vs. k when shearing direction angle θ with respect to x1 is 0, π8, π4, 3π8. I5 is the same when θ is 0 and π2.

Fig. 8.

Fig. 8

Stress response to in-plane shear displacement with shearing direction θ=π/4, for ζ =0, ζ =1, and ζ =10. (a) ϕ=1, and (b) ϕ=10.

Fig. 9.

Fig. 9

Stress response of in-plane shear displacement with shearing direction θ=3π/8, for ζ =0, ζ =1, and ζ =10. (a) ϕ=1, and (b) ϕ=10.

4. Example of data fitting

Transversely isotropic material models have been applied to study ligament and tendon tissues which have distinct fiber directions (Dourte et al., 2008; Henninger et al., 2015; Lake et al., 2010). Many tensile and biaxial tests have been done (Davis and De Vita, 2012; Henninger et al., 2015; Szczesny et al., 2012). Typical tests such as stretch along the fiber direction are usually of primary interest for ligaments and tendons. Therefore, we used data from uniaxial stretch of tendon to show the model behavior with one of the anisotropic invariants.

As an example of fitting the model of Feng et al. (2013), we fit the mechanical tests of Davis and De Vita (2012), who applied uniaxial stretch along the fiber direction of rat tail tendon fascicles. The tensile test is similar to Fig. 2a. A fitting of the data from the uniaxial stretch provides a first estimate of μ=107.66 MPa, and ζ=0.91 (Fig. 10).

Fig. 10.

Fig. 10

Experimental and fitted data of rat tail tendon fascicles under tensile loading along the fiber direction.

5. Discussion

5.1. Anisotropic behavior

The stress responses when the material is stretched transverse and parallel to the fiber direction (Fig. 11a, b) confirms the fiber reinforcement effect when ζ>0. The shear stress increases in a nonlinear fashion when the material is sheared transverse to the fiber direction (Fig. 11c, d). Inspection of the shear stress component σ12 in Eqs. (26) and (32) shows that the shear stresses in the two cases (shear displacement parallel or perpendicular to the fiber direction) differs by 2ζk3. Thus anisotropic behavior under finite shear is partly a result of fiber stretch, analogous to the Poynting effect.

Fig. 11.

Fig. 11

Illustration of the anisotropic behavior of the model: stress vs. stretch ratio for (a) ζ=1 and (b) ζ=10 when the material is stretched transverse/parallel to the fiber direction; and comparison of shear stress in simple shear for (c) ζ=10, ϕ=1 and (d) ζ=1, ϕ=10 when the material is sheared transverse/parallel to the fiber direction.

5.2. Strengths and limitations of transversely isotropic constitutive models

5.2.1. Uniaxial stretch in the fiber direction

Using the F(I4) model Qiu and Pence (1997) showed that when the material is loaded along fiber direction

(σ11)I4=μλ12(2γλ122γ+1)μλ1. (39)

Using a strain energy function analogous to the G(I5) model, Merodio and Ogden (2005) showed that when loaded in tension along fiber direction

(σ11)I5=μλ12(4γλ164γλ12+1)μλ1. (40)

Eq. (39) is identical with Eq. (19) ( I5 is unaffected by fiber stretch). Similar results were also observed in a transversely isotropic model with F(I4) only, proposed by Horgan and Saccomandi (2005). In Eq. (40), it is clear that I5 contributes to the uniaxial response, σ11.

5.2.2. Uniaxial stretch transverse to the fiber direction

The relation between fiber stretch λ1 and λ2 in Eq. (21) is seen in the F(I4) model and the G(I5) model, from which

(λ2)I5=1λ124γλ164γλ12+1. (41)

Both the F(I4) and G(I5) models have limited shortening along the fiber direction (λ1 in Fig. 3d) when stretching infinitely perpendicular to the fiber direction (λ2 in Fig. 3d). The asymptotic behavior of the H(I4; I5) model is the same as that of the F(I4) model.

5.2.3. Simple shear displacement in the fiber direction

In plane stress conditions, when ϕ = 0 the Cauchy stress tensor for the H(I4; I5) model is identical to that of the F(I4) model. If ϕ>0, each stress component is larger than that of the F(I4) model. By comparing the stress response with those from the G(I5) model:

[σij]I5=μ[k2+4γk2(1+k2)k+2γk30k+2γk300000], (42)

we observe that the magnitudes of both σ11 and σ12 increase monotonically as k increases (σ11 is an even function and σ12 is an odd function). In Eqs. (26) and (28), we observe that the stress components and strain energy function are only related to ϕ, the parameter characterizing fiber matrix interaction. Similarly, in the G(I5) model, all stress components contain γ (Eq. (42)) which is the parameter related with fiber shear.

5.2.4. Simple shear displacement transverse to fiber direction

Similar to the case of simple shear in fiber direction, the Cauchy stress is the same when ϕ=0 but larger when ϕ>0, compared to the F(I4) model, due to fiber-matrix interactions. If we compare with the Cauchy stress tensor in a similar analysis with respect to the G(I5) model:

[σij]I5=μ[4γk2(k4+4k2+3)k+2γk3(2k4+9k2+9)0k+2γk3(2k4+9k2+9)k2+4γk4(k4+5k2+6)0000], (43)

then, for plane stress, we see from Eqs. (33) and (43) that for both models: (i) σ11; σ22 and σ33 are even functions; (ii) σ12 is an odd function; (iii) σ11, σ22, and σ12 increase monotonically as k increases. However, if not in plane stress, neither σ11 nor σ22 are monotonic (Fig. 6), due to the negative term involving ζ.

5.2.5. Simple shear displacement in an arbitrary direction

Analysis of I4, I5, and C12 with respect to k and θ has been performed by Merodio and Ogden (2005). One difference worth noting is that when the fiber direction θ = π/8, I5 is convex (Merodio and Ogden, 2005) and I5 is concave (Fig. 7) with respect to k. This illustrates the interaction between I4 and I5 when in general shear deformation. The current model confirms that differences in the direction of shear displacement can have a large influence on the stress responses (Figs. 8 and 9). A similar effect was also presented in the G(I5) model presented by Merodio and Ogden (2005). When ϕ = 0, the Cauchy stress components in Eqs. (A.5)–(A.7) are identical to the F(I4) model, but larger when ϕ>0. Compared with the results of arbitrary shear from the G(I5) model, we observe a similar pattern of σ11, σ22, and σ12 with respect to k.

5.3. Effect of anisotropic invariants in different loading conditions and implications for mechanical tests

To characterize transversely isotropic materials, it is usually necessary to estimate model parameters via mechanical tests. Although inverse methods can be used to estimate model parameters, a straightforward estimate of the model parameters via fitting experiment data is still desirable (Zhang et al., 2015). We examined the effect of each invariant by comparing the stress components from Eq. (9) to the responses of the model lacking one of the anisotropic invariants (I4 or I5):

σerrμ=1μ(σI4I5σomittingI4orI5), (44)

The corresponding mechanical tests that are best to capture the invariant and model parameters are discussed.

5.3.1. Effect of I4 and implications for model fitting

In both uniaxial and equal biaxial tensile tests, we observe that all the stress components are only affected by parameter ζ. If the I4 term was omitted, for uniaxial stretch along the fiber direction and equal biaxial stretch, the error of σ would be the same (Eqs. (19) and (23)):

σ11errμ=2μζλ12(λ121), (45)

In simple shear deformation when fiber is along the fiber direction, we observe that the stress components are not affected by I4. However, if the shear deformation is transverse to the fiber direction in the plane of (x1; x2), omitting I4 can cause error. The error depends linearly on ζ and is a non-linear function of the shear deformation, k (Eq. (32)):

[σijerr]μ=ζ[2k23(k22)2k302k32k23(2k21)000k23(k2+1)]. (46)

Thus, when estimating the parameter ζ, or any parameters scaling the I4 invariant, uniaxial or biaxial stretch tests are sensible.

5.3.2. Effect of I5 and implications for model fitting

The effects of I5 in shear are captured by the modified invariant I5. If I5 is not included in the model, and shear parallel to the fiber direction, the error of stress is proportional to both the parameter ϕ and the shear amplitude, k (Eq. (26)):

[σijerr]μ=ϕ[4k23k0k2k230002k23]. (47)

Similar analysis can be applied to simple shear deformation transverse to the fiber direction, and an analytical solution of the stress error in terms of parameter ϕ can be obtained from Eq. (32):

[σijerr]μ=ϕ[2k23k0k4k230002k23]. (48)

With respect to estimating parameter ϕ, considering Eq. (26), it is recommended to use shear tests parallel to the fiber direction for data fitting.

5.3.3. Remarks on mechanical testing

In estimating the five parameters of the general transversely isotropic material form (Eq. (1)), Criscione et al. (2001) developed a novel invariant sets separating physical attributes of strain. These mutually orthogonal invariants provide a unique advantage in the experimental determination of the energy functions (Criscione et al., 2001, 2000, 2002). In this study, the specific strain energy form of Eq. (9) has only three parameters. We have shown that under uniaxial loading, either along, or perpendicular to the fiber direction, or during equibiaxial stretch, only the invariant I4 is needed to model the material behavior. In shear deformation parallel to the fiber direction, only the invariant I5 is needed to model the material behavior. Therefore, each individual parameter can be fitted separately using different mechanical testing methods. However, in shear deformation transverse to the fiber direction, both fiber stretch and fiber–matrix interactions are involved, and both invariants are needed to describe the model behavior, as they are when shear deformation is in an arbitrary direction in the (x2; x3) plane.

6. Conclusions

In this study, we explored the response to large deformations of a transversely isotropic model with both I4 and I5 invariants. A comparison of the model behavior to that of transversely isotropic models with only I4 invariant showed similar responses to stretch parallel or perpendicular to the fiber direction. However, the model with both invariants showed distinctly different behavior under shear deformation.

Analytical solutions exhibited clear nonlinear anisotropic behavior in both stretch and shear deformation. The material model exhibited the expected increase in tensile stiffness in the fiber direction, as well as a larger shear modulus when sheared in the plane containing fibers, relative to shear in the plane of isotropy. Nonlinear stiffening was seen for shear displacement perpendicular to the fiber direction. This behavior is useful for modeling and simulations of many soft biological tissues such as brain white matter, muscle, and tendon.

Analytical solutions of the model with both I4 and I5 invariants indicated that individual parameters, such as ζ and ϕ, could be characterized separately by tensile and shear tests. Typical mechanical testing procedures such as biaxial (Sacks, 2000; Sacks, 1999), rheometric (Hrapko et al., 2008) or shear testing (Namani et al., 2012; Rashid et al., 2013) can be utilized to characterize the parameters for specific soft tissues with transversely isotropic behavior. Parameter fitting based on data acquired from these mechanical tests can be used for first approximation of the model parameters. Although some simple mechanical tests can be fully modeled using only one invariant, loading conditions such as shear transverse to the fiber direction can be described only if both are included.

Acknowledgments

The authors would like to thank Dr. Larry A. Taber, Dr. Barna Szabo, Dr. Yunfei Shi, Dr. Spencer Lake, and Dr. Chunghao Lee for helpful discussions. We acknowledge support from Jiangsu Province (Grant BK20140356, YF), the Chinese National Natural Science Foundation (Grant 61503267, YF), the SRF for ROCS, SEM (Grant K511701515, YF), the NIH (Grants R01 NS055951 (PVB) and R01 HL109505 (GMG)), the NIH and NSF jointly though grant NSF U01 EB016422 (GMG), the NSF (Grant CMMI-1332433, PVB), and the Chinese Ministry of Education through a Changjiang Scholar Award (GMG).

Appendix A

The Cauchy stress components of the general simple shear in the (x1; x2) plane can be obtained from Eqs. (8) and (38). We normalized each stress component with respect to shear modulus μ. With short-handed notations c = cos θ, s = sin θ for simplicity, the corresponding normalized Cauchy stress components are

σ11μ=ζ(2(ksc1)2(k2s22ksc)23(k2s22ksc)(k2s22ksc+1)k2(s21))+ϕ(2(ksc1)2(k2s22ksc+1)23(k2sc+2(s21)k)2+2(ksc1)(k3sck2+3ksc1))+k262ksck22(2s21) (A.1)
σ22μ=ζ(23(k2s22ksc)(k2s22ksc+1)+2k2s4(k2s22ksc))+ϕ(23(k2sc+k(2s21))22k2s4(k2s22ksc+1)+2ks2(k2s2+3s21))+23k2s2+k23(s21)+2ksc (A.2)
σ33μ=2ζ3((k22(c2s2)+2ksck22)(k22(c2s2)+2ksck221))2ϕ3(k2sck(c2s2))2k23 (A.3)
σ12μ=2ks2(ksc1)(k2s22ksc)ζ+ϕ(ks2(k3sck2+3ksc1)+k(ksc1)(k2s2+3s21)2ks2(ksc1)(k2s22ksc+1))+k2sck(2s21) (A.4)

With plane stress condition (σ33 = 0), the nonzero components of Cauchy stress tensor σ are

σ11μ=2ζ(ksc1)2(k2s22ksc)+ϕ(2(ksc1)2(k2s22ksc+1)+2(ksc1)(k3sck2+3ksc1))k2(s21)2ksc (A.5)
σ12μ=k2sck(2s21)+2ks2ζ(ksc1)(k2s22ksc)+ϕ(ks2(k3sck2+3ksc1)+k(ksc1)(k2s2+3s21)2ks2(ksc1(k2s22ksc+1))) (A.6)
σ22μ=ζ(2k2s4(k2s22ksc))+ϕ(2k2s4(k2s22ksc+1)+2k2s2(k2s2+3s21))+k2s2+2ksc (A.7)

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