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Biomechanics of Soft Tissues
Biomechanics of Soft Tissues
Principles and Applications

Edited by
Adil Al-Mayah
CRC Press
Taylor & Francis Group
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Boca Raton, FL 33487-2742

© 2018 by Taylor & Francis Group, LLC

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 Contents

Preface................................................................................................. vii
Editor ....................................................................................................ix
Contributors .........................................................................................xi

1 Mechanical Characteristics of Soft Tissues .................................. 1

Adil Al-Mayah
2 Mechanical Investigations of Biological Tissues Using
Tensile Loading and Indentation ................................................ 27
Wanis Nafo and Adil Al-Mayah
3 Magnetic Resonance Elastography ............................................. 55
Deirdre M. McGrath
4 Biomechanics of Cancer .............................................................. 95
Homeyra Pourmohammadali, Mohammad Kohandel,
and Sivabal Sivaloganathan
5 Biomechanical Modeling Applications in Image-Guided
Radiotherapy .............................................................................. 117
Michael Velec and Kristy K. Brock
6 3D Ultrasound-Guided Interventions ...................................... 145
Aaron Fenster, Jessica Rodgers, Justin Michael, and Derek Gillies
Index .................................................................................................. 169

v
 Preface

The emerging paradigm of incorporating images and biomechanical properties of soft

tissues has a proven potential as an integral part of the advancement of several medi-
cal applications, including image-guided radiotherapy and surgery, brachytherapy,
and diagnostics. The subject of Biomechanics of Soft Tissues has been addressed in a
number of journal papers and conferences, in addition to anatomical site-specific books.
However, the urgent need for better understanding of the subject requires references
that cover a wide scope of mechanical principles, properties, and applications.
This book starts by introducing the basics of soft tissue structures and the fundamentals
of biomechanics using linear elastic, hyperelastic, viscoelastic, and poroelastic-modeling
approaches (Chapter 1). To provide a quantitative sense of modeling parameters, this
chapter also includes a list of mechanical parameters of human tissues. This chapter is
followed by presenting different testing methods to measure these parameters (Chapter 2)
where widely used direct mechanical tensile loading and indentation-testing methods are
presented. The analytical procedures of these techniques are illustrated, in addition to
application examples of soft tissue investigations. Chapter 3 presents the technique of
elastography as an image-based method to measure mechanical properties of tissues.
This chapter paves the way for some medical applications of soft tissue biomechanics.
Chapter 4 discusses the role of biomechanical forces that are applied to cancer cells on
cancer progression, tumor development, and consequently treatment. Specific attention
was paid for biomechanics role on the therapeutic strategies in controlling cancer pro-
gression and the effects of some of the common chemotherapy drugs on biomechanics of
cancer. Chapter 5 presents a unique integration of soft tissue biomechanics and imaging
to address the challenging task of deformable image registration (DIR). It starts with a
brief description of biomechanical-based DIR techniques developed in several anatomical
sites. This is followed by an illustration of the role of biomechanical DIR in reducing geo-
metric and dosimetric uncertainties in radiotherapy, improving the design of treatment,
and augmenting our understanding of response to several clinical scenarios. Chapter 6
focuses on ultrasound-guided soft tissue interventions where a number of state-of-the-art
technologies are presented. This chapter provides an excellent view of the potential ideas
to incorporate soft tissue biomechanics to address a number of challenges associated with
soft tissue deformation.

vii
viii Preface

The combined medical and engineering expertise of contributors makes this

book an excellent source of information and ideas for both engineering and medical
professionals as challenges and expanding knowledge of different disciplines necessi-
tate the adoption of the “diplomacy of knowledge” to expand collaboration and share
ideas. This book provides medical professionals an insight into a wealth of modeling
approaches, testing techniques, and mechanical characteristics that are frequently used
by engineers. On the other hand, the presented medical applications provide engineers
with a glimpse of amazing medical practices and encourage them to expand their roles
in the medical field.
 Editor

Professor Adil Al-Mayah is a member of the engineering school at the University of

Waterloo, Waterloo, Ontario, Canada. He has done cutting-edge research integrating
mechanics into imaging to accurately localize cancer tumors for radiotherapy
applications. This technique has been successfully applied to different anatomical
systems, including lungs, liver, head-and-neck, breast, and prostrate. He has an excellent
publication record in top tier journals, refereed conferences, abstracts and presentations,
invited talks, book chapters, and patents.

ix
 Contributors

Adil Al-Mayah Derek Gillies

Department of Civil and Environmental Robarts Research Institute
Engineering The University of Western Ontario
Mechanical and Mechatronics and
Engineering (Cross appointment) Department of Medical Biophysics
University of Waterloo The University of Western Ontario
Waterloo, Ontario, Canada London, Ontario, Canada

Mohammad Kohandel
Kristy K. Brock Department of Applied Mathematics
Department of Imaging Physics University of Waterloo
The University of Texas M.D. Anderson Waterloo, Ontario, Canada
Cancer Center
Houston, Texas Deirdre M. McGrath
NIHR Nottingham Biomedical Research
Centre
Aaron Fenster Radiological Sciences
Robarts Research Institute Queens Medical Centre
The University of Western Ontario Nottingham, NG7 2UH, United Kingdom
and
Biomedical Engineering Graduate Justin Michael
Program Robarts Research Institute
The University of Western Ontario The University of Western Ontario
and and
Department of Medical Biophysics Biomedical Engineering Graduate
The University of Western Ontario Program
London, Ontario, Canada The University of Western Ontario
London, Ontario, Canada

xi
xii Contributors

Wanis Nafo Sivabal Sivaloganathan

Department of Civil and Environmental Department of Applied Mathematics
Engineering University of Waterloo
University of Waterloo Waterloo, Ontario, Canada
Waterloo, Ontario, Canada
and
Homeyra Pourmohammadali Center for Mathematical Medicine
Department of Applied Mathematics Fields Institute for Research in
University of Waterloo Mathematical Sciences
Waterloo, Ontario, Canada Toronto, Ontario, Canada

Jessica Rodgers Michael Velec

Robarts Research Institute Techna Institute and Princess Margaret
The University of Western Ontario Cancer Centre
and University Health Network
Biomedical Engineering Graduate Toronto, Canada
Program
The University of Western Ontario
London, Ontario, Canada
 1
Mechanical
Characteristics
of Soft Tissues
1.1 Introduction ...............................................................1
General • Source of Mechanical Response in
Soft Tissues • General Mechanical Behavior
1.2 Linear Elasticity ........................................................ 3
Model Description • Elastic Properties of Human
Tissues
1.3 Hyperelasticity .......................................................... 6
Model Description • Hyperelastic Properties
of Human Tissues
1.4 Viscoelasticity .......................................................... 11
Model Description • Viscoelastic Properties
of Human Tissues
1.5 Poroelasticity ............................................................15
Model Description • Poroelastic Investigations
of Human Tissues
1.6 Isotropy and Homogeneity of Tissues ..................18
Adil Al-Mayah 1.7 Conclusion ................................................................21

1.1 Introduction
1.1.1 General
Soft tissues are defined as the tissues that support and connect body structures. They
include skin, muscles, fat, tendons, ligaments, blood vessels, nerves, cartilages, and
other tissue matrices. In some cases, they are simply defined as body tissues that
exclude hard tissues such as bones, teeth, and nails. As bones, a major component of
nonsoft tissues, represent 12%–15% of the human body mass, it can be concluded that

1
2 Biomechanics of Soft Tissues

most of the human body is composed of soft tissues. Soft tissues are known for high
flexibility and soft mechanical properties, differentiating them from mineralized stiff
tissues, such as bones (Holzapfel 2001).

1.1.2 Source of Mechanical Response in Soft Tissues

Modeling biological phenomena and material behavior can be performed at the atomic,
molecular, microscopic, and macroscopic scales. The mechanical response of tissues can
be well addressed at the macroscopic scale of biological modeling and to a limited extent at
the microscopic (multicellular) scale. Therefore, these scales will be the focus of this section.
At the cellular level, each cell consists of a cellular membrane, cytoplasm, and
nucleus. The membrane and structural cytoplasmic component, known as the cytoskel-
eton, are the main contributors to the structural performance of cells. The membrane
separates the intra- and extracellular environments and plays a role in the interaction
between these two environments. The cytoskeleton provides structural integrity of cells.
It consists of three types of filaments: (1) actin (8 nm diameter), (2) an intermediate rope-
like structure (10 nm diameter), and (3) microtubules (25 nm diameter). Actin filaments
are stiffer in extension than microtubules but they rupture at a much lower extension.
The intermediate filaments exhibit an intermediate extensional stiffness at lower exten-
sions, but they can sustain much larger extensions than the other two types of filaments
while exhibiting a nonlinearly stiffening response. The microtubules are long cylinders
that exhibit high bending stiffness compared to other filaments.
At the tissue level, typical tissues consist of three main components: (1) epithelial,
(2) stromal, and (3) mesenchymal cells. Epithelium is one of the four basic animal tissues
along with connective, muscle, and nervous tissues. It is composed of packed epithelial
cells arranged in varying numbers of layers that line the body cavities and surfaces and
form glands. Epithelial tissues’ main functions include protection and secretion. The
epithelial cells are attached to each other at many locations through adherence junc-
tions, tight junctions, and spot-like adhesion (desmosomes). These epithelial cells rest
on a membrane through a keratin-based cytoskeleton and adhesion-based junctions
(hemidesmosomes). The thin semipermeable membrane separates the epithelium from
the stroma. The stroma is a loose connective tissue that may rest on layers of muscles
or bones. It is composed of extracellular matrix (ECM), blood vessels, nerves, and lym-
phatic vessels. The ECM consists of a scaffolding of fibers, such as collagen and elastin,
embedded in a mixture of water and glycoproteins, and is of particular interest in terms
of mechanical performance.
Collagen represents the main structural component of hard and soft tissues in ani-
mals, and is responsible for the mechanical performance and strength of many ele-
ments of the human body, including blood vessels, tendons, and bones (Fung 1993).
Interestingly, Fung (1993) compared its role to the role of steel in the advancement of
many aspects of our civilization. Therefore, the performance of many soft tissues can
be attributed to their collagen fiber content. In addition, the high water content of soft
tissues plays a vital role in their mechanical behavior due to its incompressibility and
viscous nature, which contribute to viscoelastic and poroelastic performance.
Mechanical Characteristics of Soft Tissues 3

1.1.3 General Mechanical Behavior

Soft tissues have a complex structure that is generally described as a “nonlinear, inelas-
tic, heterogeneous, anisotropic character that varies from point to point, from time to
time and from individual to individual” (Humphrey 2003). For example, the generalized
stress–strain curve of a soft tissue under a simple stretching load with a constant load-
ing rate exhibits three main regions before rupture, depending on the intensity of the
applied load. Generally, it shows a linear behavior under low loading with low stiffness,
which becomes nonlinear as load increases. As the applied load increases further, a lin-
ear behavior with high stiffness is observed.
Changing the rate of loading can alter this behavior, reflecting the time-dependent
characteristics of soft tissues. Therefore, different mechanical models have been devel-
oped to capture the behavior of soft tissues under loading. These models include elastic
(linear), hyperelastic (nonlinear elasticity), viscoelastic (time-dependent), and poro-
elastic (biphasic) types. Each model has its own applications, spanning from assess-
ment of organ’s deformation to drug distribution inside the tissues. The details of the
required outcomes of these models may necessitate sophisticated material properties.
For example, for soft tissues experiencing little deformation during regular physiologi-
cal activities, linear elastic properties are sufficient. However, hyperelastic properties are
recommended for accurate estimation of organ deformation when large deformation
is expected. In addition, viscoelastic and poroelastic properties are required for time-
dependent and multiphasic tissue responses.
Furthermore, materials can generally be characterized according to their homogene-
ity (location-dependent properties) and isotropy (direction-dependent properties). To
provide a better understanding of isotropy and homogeneity, these concepts will be dis-
cussed using a linear elasticity model as an illustrative example.

1.2 Linear Elasticity

1.2.1 Model Description
Linear elastic models have been widely used to characterize the behavior of soft tissues,
as they have for many other tissues such as metals. They may not provide a full repre-
sentation of material behavior because it is limited to a low-load level. However, their
popularity in mechanical modeling of soft tissues is due to their simplicity. In addition,
these models are sufficient for a number of modeling aspects of organ deformation, as in
the case of deformable image registration for image-guided interventions where regular
physiological deformation of some organs is small. However, it is not a favored model
in applications where large deformation is expected, such as traumatic automotive and
sport incidents.
The applied load and the corresponding deformation data can be established
using tensile, compressive, or indentation-testing methods. For a sample with a
cross-sectional area of A and length L and subjected to a uniaxial tensile loading
of P, the force is often translated into a stress (σ), which is the ratio of the applied
load to the cross-sectional area (i.e., σ = P/A). In addition, the deformation (ΔL) is
4 Biomechanics of Soft Tissues

Stress Tension Compression

θ
Stress
E = tan(θ) =
Strain
εx
ν=− ε
y y
Strain
x
(a) (b) (c)
p
Δl Shear (τ)

p p
τ K=
l G= ΔV/V
Δl/l
p

(d) (e)

FIGURE 1.1 (a) Stress–strain plot of elastic material under (b) tensile and (c) compression
loads where the tangent of the plot represents the modulus of elasticity, and the negative ratio
of lateral to longitudinal strains is the Poisson’s ratio, (d) rotational deformation caused by
shear, and (e) volumetric deformation under equal pressure loading. (With kind permission
from Taylor & Francis: Imaging in Medical Diagnosis and Therapy 2013, 85–94, Al-Mayah, A.
and Brock, K.)

represented by a strain (ε), which is the ratio of the length change to the original
length (i.e., ε = ΔL/L), as illustrated in Figure 1.1a–c.
The slope of the stress–strain curve is called the elastic modulus (E = σ/ε), often known
as Young’s modulus (Figure 1.1a). In addition, the compressibility factor represented by
Poisson’s ratio (ν) is the second parameter required to describe the material’s behavior
that can be calculated as the negative ratio of the transverse strain (εx) to the longitudi-
nal strain (εy) in the direction of the applied load (ν =− εx/εy). In some cases, mechanical
properties of tissues are reported in terms of shear modulus (G), which represents the
ratio of the shear stress (τ) to the shear strain represented by the angular deformation of
the distorted shape (≈ Δl/l), as shown in Figure 1.1d. The shear modulus can be written in
terms of the elastic modulus and Poisson’s ratio, where G = 0.5E/(1 + ν). In other cases, a
material experiences volumetric changes (ΔV) because of equal pressures applied from
all directions, as shown in Figure 1.1e. The bulk modulus (K = p/(ΔV/V) is used in this
case, where (K = E/[3(1−2ν)].

1.2.2 Elastic Properties of Human Tissues

Linear elastic properties of some human soft tissues are listed in Table 1.1. Although
most of the soft tissue properties reported in the literature are ex vivo, and are often
Mechanical Characteristics of Soft Tissues 5

TABLE 1.1 Elastic Modulus of Different Human Soft Tissues

Tissue Testing Method Average Elastic Modulus (kPa) Reference
Brain MRE 12.9 kPa white matter Uffmann et al. 2004
15.2 kPa gray matter
Arteries (coronary) Uniaxial tensile 1480–1550 kPa healthy Karimi et al. 2013
(ex vivo) 3770–4530 kPa atherosclerotic
Ascending thoracic Uniaxial tensile 2982 kPa healthy Jarrahi et al. 2016
aorta (ex vivo) 7641 kPa Marfan syndrome
Breast MRE 17.1–23.5 kPa fat Van Houten et al. 2003
24.2–30.3 kPa fibroglandular
Esophagus Ultrasonography and 4.9–13.6 kPa Takeda et al. 2002
manometry
Liver USE 0.64–1.08 kPa (liver) Yeh et al. 2002
3–12.1 kPa (tumor)
1.11–4.93 kPa (fibrosis)
Indentation 270 kPa Carter et al. 2001
Aspiration 6.0 kPa Muller et al. 2009
Aspiration 20 kPa (long term) Nava et al. 2008
60 kPa (instantaneous)
Liver with fibrosis Transient elastography 7.2–18.2 kPa Marcellin et al. 2009
Elastography 2.8–16.5 kPa (stage 0–2) Corpechot et al. 2006
6.8–69.1 kPa (stage 3,4)
Prostate with PBH Sonoelastography 24.1 kPa peripheral Zhang et al. 2014
32.2 kPa transitional
Parotid gland USE 26 kPa (healthy) Wierzbicka et al. 2013
146.6 kPa (malignant)
88.7 kPa (benign)
Thyroid cancer Compression 45 kPa Lyshchik et al. 2005

Note: MRE = magnetic resonance elastography, USE = ultrasonic elastography.

animal tissue properties, efforts have been made to report human and in vivo tissue
properties. Different testing methods were used, including direct mechanical tensile and
indentation tests, in addition to image-based elastography. More details on these meth-
ods will be presented in the upcoming chapters 2 and 3. The investigated parameters
include the elastic modulus (E) or shear modulus (G), and Poisson’s ratio (ν); however,
the elastic modulus is one of the most widely reported measurements. Although, soft
tissues are mostly incompressible or nearly incompressible (ν ≤ 0.5), some investigations
have reported Poisson’s ratio values. For example, Lai-Fook and Hyatt (2000) experi-
mentally measured Poisson’s ratio for lung parenchyma, in addition to the shear modu-
lus. They found that Poisson’s ratio was age related and increased from 0.41 to 0.45 as age
increased. In addition, the effective shear modulus of human lungs (in vivo), measured
using MR elastography, was affected by the volume of inflation (G = 3.45 kPa at residual
volume, and 10.75 kPa at the total lung capacity) (Mariappan et al. 2011).
Significant variations are observed among the reported data, even when looking at the
same organs. However, this is expected with the range of different individuals, testing
methods and procedures, and load/strain ranges applied across studies. For example,
6 Biomechanics of Soft Tissues

Stress Region I: Region II: Region III:

Large deformation under Increasing stiffness Highest stiffness

lower load Nonlinear Linear
Regular physiological Wavy collagen fibers Fiber stretching
activities Fiber recruitment
Linear or nearly linear
Wavy collagen fibers
Fibers alignment

E = Stress/Strain

Strain (or stretch ratio)

FIGURE 1.2 General nonlinear behavior of soft tissues stretched under a constant loading rate.

the modulus of elasticity is load/strain dependent, as shown in Figure 1.2; however, few
details have been provided in some papers.

1.3 Hyperelasticity
1.3.1 Model Description
Many materials perform nonlinearly under loading, as characterized by the nonlin-
ear stress–strain (or stress–stretch ratio) relationship. Typical nonlinear stress–strain
relationships of hyperelastic material combine three regions, as shown in Figure 1.2. In
the first region (Region I), the tissue experiences large deformation under relatively low
loading (low stiffness) in a linear or nearly linear pattern attributed to the removal of
waves of collagen fibers in relaxed tissues. Most of the typical physiological activities are
within this region. This is followed by a nonlinear region (Region II) with an increas-
ing stiffness due to the initial recruitment of stiff collagen fibers. As the load further
increases (Region III), the tissue exhibits a stiffer behavior that is mainly characterized
by a linear stress–strain relationship as stiff fibers are stretched and actively participate
in carrying the applied load.
Different approaches have been proposed to capture this nonlinear material perfor-
mance, reaching back to 1847, when Wertheim showed a nonlinear stress–strain relation-
ship of animal tissues that deviated from the linear elastic Hooke’s law. This was formulated
by direct nonlinear stress–strain equations or through the use of strain-energy functions.
More direct nonlinear equations have been proposed (Fung 1993), as listed in Table 1.2;
however, they were not intended to represent three-dimensional (3D) stress states (Fung
1993). Regardless of their long history, these equations are not widely used in soft-tissue
characterization.
On other hand, strain-energy or potential-energy functions (W) are widely used to
capture a wide range of elastic finite deformation. These models are applied to rubber
Mechanical Characteristics of Soft Tissues 7

TABLE 1.2 Nonlinear Stress–Strain Energy Function

Used to Model Biological Tissues
Reference Model
Wertheim (1847) ε 2 = a σ 2 + bσ
Morgan (1960) ε = a σn
Kendedi et al. (1964) σ = k ε d , σ = B ( e mε − 1 )
Ridge and Wright (1964) ε = C + k σb, ε = x + ylogσ
Hoeltzel et al. (1992) σ = α( ε − εs )β

and rubber-like materials, also known as hyperelastic materials or Green elastic material
(named after Green in 1839), where they are characterized as incompressible or nearly
incompressible materials (i.e., Poisson’s ratio ν ≈ 0.5). This works well for most soft tis-
sues because of their incompressibility nature associated with their high water content.
The strain-energy function (W) represents a measure of energy stored in a material due
to the applied strain. The relationship between the strain-energy function and the mate-
rial deformation is represented by the stretch ratios in principle directions (λ1, λ2, and λ3).
Three strain invariants (I1, I2, and I3) are used to represent the stretches, as shown in
Equation 1.1. These strain invariants are the same regardless of the applied coordinate
system.

I 1 = λ12 + λ 22 + λ32

I 2 = λ12 λ 22 + λ 22 λ32 + λ32 λ12 (1.1)

I 3 = λ12 λ 22 λ32

For incompressible materials, the value of the third invariant (I3) is 1.

Different energy functions have been developed to capture the performance of hyper-
elastic materials. Given a wide variation of soft tissue responses to mechanical loading,
the efficiency of each of these energy functions depends on its ability to capture the full
behavior of the material with a minimum number of parameters. In other words, if the
proposed model results fit with the experimental data of a material subjected to a spe-
cific loading, the model is considered efficient to predict the material behavior under this
specified loading condition. Reviews on some of these models can be found in Martins
et al. (2006) and Boyce and Arruda (2000). Some of the popular hyperelastic models
used in biomechanical modeling are briefly described below:
1. Mooney–Rivlin model is an early model that was used to capture the nonlinear
behavior of rubber-like materials (Martins et al. 2006). It is known for its high
accuracy, especially for cases in the median range of strain (200%–250%). The
strain energy function is

W = C10 ( I 1 − 3) + C01( I 2 − 3) (1.2)

where C10 and C01 are material constants in stress units (e.g., N/mm2).
8 Biomechanics of Soft Tissues

2. Polynomial model was proposed by Rivlin as an extension of the Mooney–Rivlin

model. The model is proposed in a form of polynomial series as follows:
∞
W= ∑C ( I − 3) ( I
i , j =0
ij 1
i
2 − 3) j (1.3)

where Cij is a material parameter.

3. Neo–Hookean model considers only the first term of the Rivlin model. It is suitable
for modeling small strains of 150%. It has been widely used in modeling biologi-
cal tissues because of its accuracy in capturing material behavior under different
loading (Marckmann and Verron 2006). In addition, it is recognized for its sim-
plicity because only one parameter is required.

W = C10 ( I 1 − 3) (1.4)

4. Yeoh model uses higher order terms of I1 or I2 to account for a wider spectrum of
deformation. Adding a higher order of I1 was shown to accurately model large
deformation loading cases. In addition, the effect of I2 on the accuracy of mate-
rial characteristics was also minimal. Therefore, the Yeoh model focuses on
three orders of I1 only, as illustrated in Equation 1.5 for incompressible material
models:

WYeoh = C10 ( I 1 − 3) + C 20 ( I 1 − 3) 2 + C 30 ( I 1 − 3)3 (1.5)

5. Arruda and Boyce model considers higher order terms for incompressible
materials:
5

∑ λC ( I − 3 )
i
W =µ i
2 i −2
i
1
i
(1.6)
i =1

where C1 = 1/ 2 , C 2 =
= 1/ 20 , C 3 11
=/1050, C 4 19/7000, C 5 = 519/673750, λ is the
locking stretch ratio (unitless), and μ is known as the initial shear modulus.
6. Ogden model uses principal stretches in the strain-energy function instead of the
strain invariants used in other models (Ogden 1984). This model has been used to
model large deformation cases:
n
Wo = ∑ αµ ( λ
i =1
i

i
αi
1 + λ α2 i + λ3αi − 3 ) (1.7)

where μi (stress units) and αi (unitless) are real numbers representing material
parameters, whereas (n) is a positive integer.
7. Veronda–Westmann model has been used to model incompressible materials:

(
WVW = C1 e α(I1 −3) − 1 − C 2( I 2 − 3) ) (1.8)
Mechanical Characteristics of Soft Tissues 9

where:
C1 and C2 are material constants with stress units
α is a unitless parameter

8. Fung model (Fung 1975) is an exponential pseudostrain energy function ( ρ0W ) ,

described as follows:
C  (a1ε2x +a2 ε2y + 2 a4 εx ε y ) (a1ε2x +a2 εz2 + 2 a4 εx εz ) (a1εz2 +a2 ε2y + 2 a4 εz ε y ) 
ρ0W = e +e +e  (1.9)
2  
where:
εx, εy , and εz are strain components
c, a1, a2, and a4 are material constants
Although this model was introduced in the biomechanics literature several decades ago,
its implementation into finite element (FE) simulations has been limited. The key bar-
riers to numerical implementations are inherent numerical instability and convergence
(Sun et al. 2005).
Although most hyperelastic models are isotropic, some anisotropic models with dif-
ferent degrees of anisotropy have been introduced, including transversely isotropic
(Humphrey et al. 1990a, b; Weiss et al. 1996; Gardiner and Weiss 2001) and orthotropic
(Tong and Fung 1976; Chew et al. 1986; Fung 1993; Criscione et al. 2003) models. However,
the numerical convergence problem is a barrier for using these in numerical modeling
(Sun et al. 2005).

1.3.2 Hyperelastic Properties of Human Tissues

A nonlinear stress–strain relationship has been reported for different organ tissues.
Zeng et al. (1987) experimentally investigated the mechanical properties of excised
human lung tissues using biaxial loading. A nonlinear hyperelastic model was applied
to characterize the nonlinear stress–strain relationship. Similar behavior was observed
by Budday et al. (2017) in their extensive investigation of ex vivo human brain tissues,
where shear, tension, and compression tests were conducted to investigate hyperelastic
properties of different brain regions. The experimental data fit well with the modified
one-term Ogden strain-energy function by comparison with other energy functions
such as Neo–Hookean, Mooney–Rivlin, Demiray, and Gent. The properties varied
among different brain regions and testing methods as reported in Table 1.3.
Similar variations were also reported among different regions of the breast, as
reported by Samani and Plewes (2004), and among different types of breast cancers
(O’Hagan and Samani 2009), including ductal carcinoma in situ, invasive mucous
carcinoma, invasive lobular carcinoma, and low-, medium-, and high-grade inva-
sive ductal carcinomas. It was clearly shown that cancerous tissue parameters were
larger than healthy tissues in some cases by as much as two orders of larger magnitude
(O’Hagan and Samani 2009). Table 1.3 provides a sample of hyperelastic properties and
models of human tissues.
10 Biomechanics of Soft Tissues

TABLE 1.3 Human Tissue Hyperelastic Parameters

Hyperelastic Model and Parameters Testing Method Reference

Brain

W = C10 ( I 1 − 3 ) + C 30 ( I 1 − 3 )
3 Aspiration test Schiavone
(in vivo) et al. 2009
C10 = 0.24 kPa, C30 = 3.42 kPa
ψ Ogden = 2µ/α 2 ( λ1α + λ 2α + λ 3α − 3 ) Tension, compression, Budday et al.
Parameter range represents different regions of brain: and shear (ex vivo) 2017
μ = 0.33 to 1.06 kPa, α = −22.0 to −24.6 (shear test)
μ = 0.33 to 1.16 kPa, α = −25.6 to −38.9 (tension test)
μ = 0.47 to 1.63 kPa, α = −11.4 to −16.5 (compression test)

Breast
W = ∑ i + J =1Cij ( I 1 − 3 ) ( I 2 − 3 )
N i j Indentation + Inverse Samani and
FEM Plewes 2004
(C10 = 0.31, C01 = 0.30, C11 = 2.25, C20 = 3.80, C02 = 4.72) kPa
(adipose)
(C10 = 0.33, C01 = 0.28, C11 = 4.49, C20 = 7.72, C02 = 9.45) ×
10−4 kPa (fibroglandular)

Lungs
C  (a1ε2x +a2 ε2y +2 a4 εx ε y ) (a1ε2x +a2 εz2 +2 a4 εx εz ) (a1εz2 +a2 ε2y +2 a4 εz ε y )  Biaxial tensile Zeng et al.
ρ0W = e +e +e
2  

(ex vivo) 1987

𝑐 = 11.8 𝑔/𝑐𝑚, a1 = 0.43, a2 = 0.56, a4 = 0.32

C ( εI12 +βI 2 ) Gao et al.
ρ0W = e 2006
2∆
C dyn
= 3.06 ± 0.84 K . 2 , α = 4.47 ± 1.94, β = −4.2 ± 2.55
∆ cm
Liver

 −2   −2  K
2 Aspiration test + Nava et al.
W = C10  I 3 3 I 1 − 3  + C 20  I 3 3 I 1 − 3  + 0 ( I 3 − 1)
2
Inverse FEM 2008
    2
    (in vivo)
C10 = 9.85 kPa, C20 = 26.29 kPa, K0 = 104 kPa
Liver capsule Inflation test Brunon et al.
W = C 20 ( I 1 − 3 ) one-term polynomial model 2011
2

C20 = 114 ± 40 kPa

W = a e ( 1 ) − 1 Exponential model (Demiray)

b I −3
 
a = 71 ± 29 kPa, b = 1.8 ± 0.5 kPa
1
I 1 = λ12 + λ 22 + 2 2
λ1 λ 2
Mechanical Characteristics of Soft Tissues 11

1.4 Viscoelasticity
1.4.1 Model Description
In previous linear elastic and hyperelastic modeling sections, the time element was not
considered as a contributing factor to the mechanical behavior of soft tissues. However,
duration and rate of loading (force/unit time) affect the mechanical behavior of soft
tissues given their high-fluid (viscous) content. Depending on the application of the
mechanical properties of soft tissues, there is a debate on the importance of this factor.
However, most of this debate focuses on the significance of including the time factor and
not on the intrinsic characteristic of tissues.
Figure 1.3 illustrates the time-dependent response of pure elastic, pure viscous, and
viscoelastic materials, which combines pure elastic and pure viscous responses. The
differences in response can be recognized in the loading and unloading stages. The load-
ing and unloading response of elastic material is independent of time. This is clearly
demonstrated by the immediate response of these materials to both loading and unloading
conditions. During loading, the load is instantaneously transferred to the material.
Similarly, the material responds to unloading immediately after the load is removed.
However, viscous material responses at the loading stage are a function of time. In this
case, time is needed to transfer the full load to the material, often referred to as a velocity
of deformation. In addition, the material is deformed permanently, even after the load
is removed during unloading stage. On the other hand, viscoelastic material responses
are a mixture of pure elastic and viscous responses, where deformation is a function of
time during both the loading and unloading conditions. However, unlike pure viscous
materials, the strain drops suddenly after the load removal in the unloading stage, but
requires time to fully recover and return to its original configuration. Given their pat-
tern of loading response, viscoelastic materials are modeled using spring and dashpot to
model the elastic and viscoelastic response, respectively.
The time-dependent response of viscoelastic materials can be divided into different
types: creep, relaxation, strain-rate, and hysteresis, as shown in Figure 1.4. In creep,
under a constant load, the material continues to experience deformation (strain) over
time. On the other hand, the material relaxes when it is subjected to a constant deforma-
tion as stress drops. In addition, the response of the material to loading is dependent

Elastic Viscous Viscoelastic

Unloading
Unloading Unloading
Strain (ε)

Strain (ε)
Strain (ε)

(a) Time (t) (b) Time (t) (c) Time (t)

FIGURE 1.3 Time-dependent response of (a) elastic, (b) viscous, and (c) viscoelastic materials.
12 Biomechanics of Soft Tissues

Strain

Stress
Stress

Time Time Strain

(a) Relaxation (b) Creep (c) Hysteresis

FIGURE 1.4 (a) Stress–time behavior of a viscoelastic material under two constant strain levels,
(b) strain–time behavior of a viscoelastic material subjected to two constant stress levels, and
(c) Hysteresis of stress–strain plot of a viscoelastic material under cyclic loading. (With kind per-
mission from Taylor & Francis: Imaging in Medical Diagnosis and Therapy 2013, 85–94, Al-Mayah,
A. and Brock, K.)

on the duration of the applied load as it is capable of carrying higher loads under faster
strain application (i.e., higher strain rate). Therefore, the strain/loading rate is often
reported with viscoelastic material properties. In hysteresis, the viscoelastic material
dissipates energy when it is subjected to loading–unloading cycles where the loading
path is different from that of unloading.
There are three types of viscoelasticity: (1) linear, (2) quasi-linear, and (3) nonlinear.
Linear viscoelasticity is used in a wide range of applications due to its simplicity; hence,
it is the focus of this section. Linear viscoelastic models generally include a solid-related
characteristic (e.g., spring), in addition to the fluid component (e.g., damper or dashpot).
Different arrangements and numbers of these components have been proposed to create a
number of viscoelastic models. Some of these common models are presented here, includ-
ing Maxwell, Kelvin–Voigt, and standard linear solid (Zener model), as listed in Table 1.4.
The Maxwell model is the simplest model, where it consists of a spring and a dashpot
arranged alongside each other. Therefore, both spring and dashpot are subjected to the
same load. It accurately predicts the relaxation response, but not the creep response, as
described by

1 dσ σ
ε = ε s + ε d = + (1.10)
E dt η
where:
dεs dε dε
ε s = , ε d = d , and ε =
dt dt dt
εs and εd are spring and dashpot strains, respectively, produced by the applied
stress (σ)
E and η are the spring and dashpot constants, respectively

In the Kelvin–Voigt model, both spring and dashpot are subjected to the same displace-
ment due to their parallel arrangement. It is worth mentioning that the Kelvin–Voigt
model shows a unique relaxation response to a rigid body in sudden loading because the
dashpot does not move under sudden loading. It is well suited to the prediction of creep.
The stress is calculated by
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