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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
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
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,
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
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
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).
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)
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.
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
1.4 Viscoelasticity
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.
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
TABLE 1.4 Linear Viscoelastic Models
Model Configuration Creep Function Relaxation Function

Maxwell
Deformation
Force
t0 Time
t0 Time t1
Kelvin–Voigt
Deformation
Force
t0 Time t1 t0 Time
Standard linear solid E2 η Deformation

(Maxwell form)
Force
E1
t0 Time t1 t0 Time
Source: Al-Mayah, A. and Brock, K. 2013. Imaging in Medical Diagnosis and Therapy, CRC Press,
Taylor & Francis Group, Boca Raton, FL, 85–94.
d εd
σ = σs + σd = E εs + η (1.11)
dt
where:
εs and εd are spring and dashpot strains, respectively
E and η are the spring and dashpot constants, respectively
As for the standard linear solid model using the Maxwell form, the following relation-
ship is applied:
dε E2  η dσ 
=  + σ − E1 ε  (1.12)
dt η ( E1 + E 2 )  E 2 dt 
where E1 and E2 are the spring constants aligned and parallel to the dashpot, respectively,
as shown in Table 1.4.
1.4.2 Viscoelastic Properties of Human Tissues

Different studies have applied viscoelastic properties to model soft tissues. The reported
constants are normally the spring (E) and dashpot (μ) constants. However, in some
cases, a shear modulus (Sinkus et al. 2005; Klatt et al. 2007) and a complex elastic modu-
lus representing the frequency-dependent modulus of elasticity (Zhang et al. 2008) have
also been reported.
A wide range of human tissues have been investigated to find viscoelastic properties.
Among the most widely studied are brain tissues. This is mainly related to the fact that
brain tissues experience a number of time-dependent large deformations, mostly associ-
ated with the fluid movement. Some of these deformations are slow, such as those associ-
ated with hydrocephalus, and convolutional development (Franceschini et al. 2006), in
addition to surgery induced deformation. Other deformations are large and fast, such
as traumatic injuries. Therefore, viscoelastic properties are required for time-dependent
reactions. These properties are addressed in a simple linear viscoelastic form (Klatt et al.
2007; Green et al. 2008; Zhang et al. 2011) and poroviscoelastic form (Franceschini
et al. 2006; Mehrabian and Abousleiman 2011). Similar investigations have been con-
ducted on other human soft tissues, including the breast (Krouskop et al. 1998; Sinkus
et al. 2005), liver (Klatt et al. 2007; Asbach et al. 2008), lung (Zhang et al. 2008), and
prostate (Krouskop et al. 1998).
A sample of linear viscoelastic parameters of human tissues is listed in Table 1.5.
TABLE 1.5 Human Tissue Viscoelastic Parameters
Tissue Testing Method Parameters Reference

Brain MRE (in vivo) μ1 = 0.84 kPa, μ2 = 2.03 kPa, Klatt et al. 2007
η = 6.7 Pa s
Zener_ μ1, μ2 shear modulus
Breast + pathologies MRE (in vivo) G = 0.87 kPa, η = 0.55 Pa s Sinkus et al. 2005
Voigt model
G = 2.9 kPa, η = 2.4 Pa s Cancer
G = 1.3 kPa, η = 2.1 Pa s
Fibroadenoma
G = 1.2 kPa, η = 0.8 kPa
Mastopathy
Liver MRE (in vivo) μ1 = 1.36 kPa, μ2 = 1.86 kPa, Klatt et al. 2007
η = 5.5 Pa s
Zener_ μ1, μ2 shear modulus
Liver with fibrosis MRE (in vivo) E1 = 1.16 kPa, E2 = 1.97 kPa, Asbach et al. 2008
η = 7.3 Pa s
Lung Tension (ex vivo) E = 6.8 kPa, R = 3.1 kPa s, Dolhnikoff et al. 1998
η = 0.072 with airways
E = 9.6 kPa, R = 4.0 kPa s
η = 0.062 without airways
E = 74 kPa, R = 3.5 kPa s total
(R = resistance, η = 0.075
hysteresivity tissue damping/
elastance)
Prostate Sonoelastography + E* = 15.9 kPa, η = 3.61 kPa sα, Zhang et al. 2008
compression test α = 0.2154 healthy
(in vivo + histology) E* = 40.4 kPa, η = 8.65 kPa sα,
α = 0.2247 cancerous
(Kelvin–Voigt model)
σ(t ) = E0 ε( t ) + ηD α [ ε( t ) ]
E* (complex Young’s modulus) is a frequency-dependent Young’s modulus.

In the aforementioned elasticity, hyperelasticity, and viscoelasticity models, a mate-

rial has been considered as uniphase solid and its response to external loads or defor-
mation is modeled as a lumped relationship. Although this assumption is a sufficient
representation to capture mechanical behavior of soft tissues, it does not fully cover
some applications where the biphases model is needed as in the case of drug-distribution
investigations. This biphasic model is based on the fact that soft tissues contain a high
percentage of water, occupying a large percentage of its total volume in spaces that may
be referred to as pores.
1.5 Poroelasticity
The structure of soft tissues is generally considered biphasic, consisting of a porous solid
phase and a fluid phase. Therefore, a poroelastic model has been used to model tissues.
As the solid plays a major role in load-carrying capacity of the porous materials, differ-
ent important functions are attributed to the fluid constituent in tissues. These functions
include transport of nutrients from the vascular system to cells, removal of waste from
cells, preventing friction in cartilage, and drug delivery and distribution, in addition
to its role in load transfer. In general, poroelastic material behavior is similar to that of
viscoelastic materials where it experiences creep under a constant stress and relaxation
under constant strain steps.
Poroelastic theory was developed to model soil consolidation in 1923 and 1925 by
Terzaghi (Terzaghi 1925), who assumed a one-dimensional (1D) consolidation case and
incompressible solid and fluid constituents. The 1D assumption was adopted by assum-
ing the soil as a laterally confined material, thus experiencing only uniaxial deforma-
tions. On the basis of the incompressibility assumption, deformation of soil under
compression is mainly caused by the rearrangement of particles and not by the com-
pression of solid particles and pore fluid. In other words, in saturated soil, the volume
change of a material can occur only by the net flow of fluid out of pores. This assumption
provides a good approximation for the behavior of highly incompressible soft soils such
as clay and sands, where compressibility of stiff solid particles is negligible as compared
to that of the whole porous material.
Biot (1941) further developed the poroelastic theory, presenting a 3D theory of lin-
ear elastic deformation of porous media, taking into account the compressibility of the
constituents. In the year between 1955 and 1973, Biot proposed further developments
by including an anisotropic case, dynamic response, and nonlinear elasticity. Verruijt
(1969) extended the formulation of this theory to soil mechanics problems. In addi-
tion, Rice and Cleary (1976) reformulated the theory in terms of drained and undrained
behavior, and fluid-filled porous materials.
Another approach was proposed to model poroelastic material using the theory of
mixtures. This approach is based on diffusion models developed using fluid and ther-
modynamics principles (Truesdell and Toupin 1960; Bowen 1980), where each constit-
uent has a number of specified characteristics, including a spatial frame, a density, a
body force, and internal energy. According to this theory, chemical reactions between
material constituents are possible, unlike Biot’s theory. Although each of the theories
has its own application in soft tissue modeling, Cowin and Cardoso (2012) used some
of Biot’s poroelastic concepts in the mixture theory to model interstitial tissue growth.
A good review of poroelastic theory development and fundamentals can be found in
Detournay and Cheng (1993).
As Terzaghi and Biot’s theories created a scientific revolution in the geotechni-
cal field (de Boer, 1999), they have a great potential to generate a revolution in the
field of biomechanics and related medical applications. This can be attributed to
the nature of tissues that have a number of common soil characteristics, in that the
mechanical behavior of tissues is controlled not only by the solid-phase response,
but also by fluids and their movement in and out of the pores. At the instant of
loading, the poroelastic material behaves as an elastic solid controlled by shear or
elastic modulus of the matrix. This is followed by the fluid flow that continues until
equilibrium is reached between the internal fluid pressure and external environ-
ment. The pore fluid contributes to the tissue’s mechanical behavior by increasing
stiffness through pore pressure, and to deformation by its movement within and out
of the tissues.
Two scenarios of fluid movement inside the porous media are considered: (1) drained
and (2) undrained conditions. In the drained conditions, the pores are assumed to be
connected with each other allowing the fluid to move out under loading, and there-
fore the pore pressure is zero. On the other hand, under the undrained condition, the
pores are not connected, and the fluid stays within the pore and contributes to carrying
the pressure exerted by external loading. It is worth noting that the fluid contribution
to tissue deformation is more pronounced when it flows out of the tissue in drained
conditions.
In addition, the response of porous materials can be considered at both macrome-
chanical (continuum) and micromechanical levels. The macromechanical approach
describes the overall behavior of a material without describing the contributions of
individual constituents by using bulk material properties of K, Ku, and α, represent-
ing the bulk modulus of drained elastic solid, the undrained bulk modulus, and the
Biot’s coefficient, respectively. The Biot’s coefficient is the ratio of the gained (or lost)
fluid volume of an element to the total volume change of that element when pore
pressure is allowed to return to its original state. On the other hand, the microme-
chanical approach takes the behavior of individual components of a material into
consideration
Two strain components are considered to model porous materials behavior: (1) solid
and (2) fluid phase-related strains. The well-known solid-related strain (εij) is often
small and it is positive for extension. The fluid strain component (ζ) represents the fluid
content variation (positive for gain of fluid), which is the variation of fluid volume per
unit volume of porous material. In the continuum model, Biot’s theory assumes a lin-
ear relationship between the applied stress (σij, p) and strains (εij, ζ), in addition to the
elastic assumption (i.e., full reversibility of deformation) (Detournay and Cheng 1993).
To express these parameters in terms of material constants such as K, Ku, and α, the fol-
lowing relationships have been used:
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my expressions of gratitude.” Mr. Goupil spoke rather deliberately
and seemed to choose his words with care. “That your telegram
received no response is a matter of extreme regret. Yet, when I
inform you that it never reached me, you will, of a certainty,
exonerate me from discourtesy, Mr. Laurie.”
“Why, surely,” agreed Laurie eagerly. “We had already found out
that the telegram was delivered to the wrong person, sir.”
“Ah! Is it so? But doubtless!” Mr. Goupil paused and nodded
several times. “Allow me, please, the explanation of certain ever-to-
be-regretted circumstances. You must know, then, that after the
death of my excellent and never-to-be-forgotten wife I was plunged
in sorrow. You, sir, have never lost a beloved wife—but, no, no, of a
certainty you have not!” Mr. Goupil laughed at himself heartily before
he went on. “Very well. To pursue. In my sorrow I returned to the
country of my birth for a visit, to France, to Moissac, where live many
of my relations. But, sir, one does not elude Sorrow by crossing the
ocean! No, no, it is here!” Mr. Goupil struck himself twice on the
chest. “Soon I return, sir, yet in the brief period of my absence the
harm has been done!” He paused with dramatic effect.
“Indeed,” said Ned sympathetically, yet puzzled.
“Yes, sir, for although I am absent but five months, yet when I
return a so horrible deed has been perpetrated in my name.”
“Indeed.” It was Laurie’s turn this time. Mr. Goupil’s large
countenance depicted the utmost dejection, but only for a moment.
“In my absence,” he went on, brightening, “my lawyer, in whose
hands all my affairs of person were left, learned of the terms of the
will of my late wife’s mother. The will says that at the death of my late
wife the property in this so quaint town occupied by my dear sister-
in-law shall revert. Thereupon, stupid that he was, my lawyer
proceeds to write to my sister-in-law to that effect. The rest, sir, you
know. Yet this lamentable news reached me but three days ago!
‘What,’ asks this lawyer, ‘will you do with this property in Orstead,
New York?’
“‘What property do you speak of?’ I ask him. He tells me then. I am
overcome. I am frantic. ‘Imbecile!’ I shout. ‘What have you done?’ I
come at once by the fastest of trains. I am here!”
“That—that was very nice of you,” faltered Laurie, keeping his
eyes carefully away from Ned.
“Nice! But what else to be done? For nothing at all would I have
had it so happen, and so I hasten to make amends, to offer
apologies to my dear wife’s sister, to you, sir, to correct a so great
mistake!”
“Certainly,” assented Laurie hurriedly. “Of course. But what I don’t
understand is why the letter that Miss Comfort wrote to you didn’t
reach you, sir.”
Mr. Goupil made a gesture of despair. “I will explain it also. My
dear sister-in-law made a mistake of the address. I saw the letter. It
was wrong. I—but wait!” Mr. Goupil drew forth a handsome card-
case, selected of the contents, and reached forward. Laurie took the
card and read:
Chicago Sioux City Des Moines
GOUPIL-MacHENRY COMPANY
Stocks Bonds Investments
514–520 Burlington Bldg., Sioux City, Ia.
Members of the
Chicago Stock Exchange
“You see?” pursued Mr. Goupil. “My dear sister-in-law made the
mistake regrettable. She addressed the letter to the ‘Goupil
Machinery Company.’ There is none.”
“I see,” said Laurie, enlightened, as he passed the engraved card
to Ned. “This MacHenry is your partner, sir?”
“Of a certainty. Adam MacHenry he is, a gentleman of Scottish
birth, but now, like me, William Goupil, a citizen of the United States,
sir.”
“Oh! Well, but look here, Mr. Goupil. Miss Comfort must have had
your initials wrong, too, then, for—”
“Ah, another misfortune! Attend, please. My name is Alphonse
Guillaume Goupil. Yes. Very well. When I am in this country but a
very short time I find that Alphonse is the name of all waiters in all
hotels everywhere I go. I put aside Alphonse then. I am Guillaume
Goupil. Then I become prosperous. I enter into business. Many do
not know how to pronounce my first name, and that is not well. So I
then spell it the American way. To-day I am William Goupil, American
citizen!”
“That explains why the telegram didn’t get to you,” said Laurie.
“Well, the whole thing’s been a sort of—of—”
“Sort of a comedy of errors,” suggested Ned.
Mr. Goupil seized on the phrase with enthusiasm. “Yes, yes, a
comedy of errors! You’ll say so! A comedy of errors of a certainty,
beyond a matter of a doubt! But now, at last, it is finis. All is
satisfactorily arranged. You shall hear. First, then, I offered my dear
sister-in-law a nice home in Sioux City, but no, she must stay here
where it has been her home and her people’s home for so long a
time. Also”—Mr. Goupil laughed enjoyably—“also, Mr. Laurie, she
fears the Indians! But at last it is arranged. In the fall she will return
to her house. By then it will be a place worthy of the sister of my dear
and greatly lamented wife. To-morrow I shall give orders, oh, many
orders! You shall see. It will be—” Mr. Goupil raised his eyes
ecstatically—“magnificent!”
“Well, that certainly is great,” said Laurie. “I can’t tell you how
pleased I—we both are, Mr. Goupil.”
Mr. Goupil bowed again, but without arising, and smiled his own
pleasure. “I shall ask you to believe, Mr. Laurie, that never did I
suspect that my dear sister-in-law was in any need of assistance.
But now I understand. It shall be arranged. From now on—” He
waved a hand grandly. Words would have said far less.
He arose. Laurie arose. Ned arose. Mr. Goupil bowed. Laurie and
Ned bowed.
“Once more, Mr. Laurie, I thank you for your kindness to my dear
sister-in-law. I thank also your so noble brother. I shall be in Orstead
for several days and it will give me great pleasure to see you again.
We shall meet, yes?”
“Of a certainty,” answered Laurie, with no thought of impertinence.
“To-morrow, perhaps, at Miss Comfort’s, sir. We are going there in
the morning to say good-by to her.”
“Excellent! Until the morning, then.” Mr. Goupil bowed. Laurie
bowed. Ned bowed. Mr. Goupil placed his derby in place, gave it an
admonishing tap, smiled pleasantly once more, and was gone.
Laurie closed the door after him and leaned weakly against it.
“If anything else happens to-night,” he sighed, “I’ll go batty!”
CHAPTER XXV
THE MARVELOUS CATCH
W ednesday afternoon, and the hands of the clock in the tower of

the Congregational Church, seen distantly over the tops of the
trees, pointed to eighteen minutes before three.
Ideal weather for Class day, hot in the sun, pleasantly warm in the
shade, with a very blue sky trimmed around the edges with puffs of
creamy-white clouds. An ideal day, too, for the big game, with plenty
of heat to make muscles responsive and no wind to deflect the ball
from its long, arching course. Kind, as well, to the wearers of pretty,
light dresses, with whom the stands were liberally sprinkled,
mothers, sisters, cousins and aunts of the important-looking
graduates. Dark-blue pennants and pennants of maroon and white
drooped against their staffs save when a moment of frenzy set them
swirling above the sloping stands.
The game was three innings old, and the black score-board
behind the back-stop held six big round naughts. Those three
innings had not been devoid of interest, however, even if neither
team had tallied. Nervousness and over-anxiety had filled at least
two of them with breathless moments. In the first and second
Farview had placed men on bases; in the second Hillman’s had got
Pat Browne as far as third. There had been errors by both sides, and
more than one case of poor judgment. Nate Beedle, pitching for the
home team, and Luders, for the visitors, had been in hot water much
of the time. Yet each had survived, and now, at the beginning of the
fourth inning, with Farview coming to bat, the game was still to be
won or lost.
Laurie had been through some bad moments. For the first two
innings he and Nate had not worked together very smoothly. They
had had a half-hour of practice before an early dinner, during which
Nate had coached the new catcher and Laurie had mastered signals.
Later, Cas Bennett had given Laurie the “dope” on the Farview
batters. He was still giving it between innings, for Laurie’s mind was
in no condition to memorize. By the beginning of the third inning ten
Farview players had come to the plate, and at least ten times Nate
had refused Laurie’s signal. Of course Laurie had known that Nate
was right and that he was wrong, but it had all been mighty
confusing and disconcerting. Added to that was the continuing dread
of throwing badly to second. He could peg the ball to first unerringly
enough, or to third, but the long heave across the width of the
diamond terrorized him. Once when he should have thrown to Lew
Cooper that fear of misfortune held his hand, and Hillman’s had
groaned as a Farview runner slid unchallenged to the bag. Save for
that occasion a throw to second had not been called for, and the test
was still ahead of him. For the rest, Laurie had done well enough. He
had dropped the delivery more times than he cared to recall, but had
escaped without penalty. Once the ball had got past him entirely and
bounded against the back-stop, but, fortunately, the bases had been
empty. During the first of the third he and Nate had come to
understand each other better, and constant reiteration by Cas had
finally impressed Laurie with the foibles of the enemy batsmen. Now,
at the beginning of the fourth, he breathed easier and found himself
sustained by a measure of confidence. His throw to second, before
the first of the enemy stepped into the box, was straight, hard, and
knee-high.
Farview began with a scratch hit to the left field that took an
unexpected bound away from Frank Brattle’s ready glove. Followed
a screaming two-bagger that placed the first runner on third. Only a
smart throw-in by Lee Murdock prevented a tally then and there. The
tally came later, however, and a second followed close behind it.
Nate passed a batter and filled the bases. Then a pretty sacrifice fly
to short right moved the runners up, and Farview cheered her first
score. Nate struck out the subsequent batter. Then came a rolling
grounder to Cooper and Lew scraped it up and, with all the time in
the world, threw low to first. By the time Tom Pope had turned
around about three times looking for the ball that he had stopped but
not caught, the runner on third had scored, the batsman was safe,
and the chap from second was half-way between third and the plate.
Tom shot the ball home; Laurie got it, held it, and swung downward.
There was an instant’s confusion of dust and sound, and the umpire
swung his mask upward and out.
Two runs for Farview.
Farview clung to that lead until the sixth, but could not add to it. In
her half of the fourth Hillman’s got Captain Dave as far as second,
but Murdock’s fly to left made the third out. In the fifth the opposing
pitcher struck out Laurie and Nate and kindly allowed Cooper to pop
a fly to third baseman.
In the sixth things began to happen, all at once and on all sides.
Farview started the trouble by hitting through short-stop for a base.
Nate pitched ten deliveries before the next batsman at last fouled out
to first baseman. Then came an attempted sacrifice. The batsman
laid down the ball scarcely two feet from the plate, and the runner on
first was off. Laurie dashed his mask aside, scooped up the trickling
sphere, stepped forward, and sped it to second. The throw was
perfect, and Pope got the runner. Hillman’s applauded delightedly,
and from the Blue’s bench came the approving voice of the coach,
“Good work, Turner!” Laurie, accepting his mask from a Farview
batsman, reflected that maybe nothing was nearly as bad as you
pictured it beforehand, and remembered with surprise that in making
the throw he had not consciously thought a thing about it; hadn’t
hoped he would make it or feared that he wouldn’t; had simply
picked up the ball and plugged it across the diamond! Exit the
bugaboo!
With two down, however, Farview refused to yield the inning.
Instead, she poked a hit across second base and another past third
and so added another tally. That seemed to distress Nate Beedle
unnecessarily, and he proceeded to pass the next batsman. And
after that, with two gone and two strikes and one ball on the
succeeding aspirant, he pitched three more balls in succession and
passed him, too! Very suddenly the bases were full, and the game
seemed about to go glimmering. And at that moment George
Pemberton and the scrub catcher strode off around the first base
stand, and if the visiting crowd hadn’t been making such a ridiculous
noise the thud of ball against mitten might have been heard from
back there.
Nate was, in baseball parlance, “as high as a kite.” His first effort
against the new batsman was a ball that Laurie only stopped by
leaping two feet from the ground. Laurie walked half-way to the
pitcher’s box, amid the exultant howls of a joyous foe, shook the ball
in Nate’s face, and savagely told him to take his time. Laurie was
angry just then. Nate was snappy and told Laurie to “go on back and
quit beefing! I’ll get him!” Laurie signaled for a high ball; the batter
“ate up” low ones. Nate hesitated, shook his head. Laurie called for
one close in then. Nate wound up and stepped forward. The result
was a wide one that made the score two balls and no strikes. On the
bench Mr. Mulford was watching with sharp eyes. Nate followed with
a fast ball that was struck at too late. Laurie’s heart retreated down
his throat again. Once more he signaled a high one. This time Nate
made no demur, but the ball failed to go over. A substitute detached
himself from the group on the bench and sped around the stand.
Laurie, holding the ball, glanced toward the coach. He got the
expected sign. Nate, too, saw, and began to pull at his glove.
Captain Dave joined him at the mound. Nate looked gloomy and
mutinous. Then George Pemberton came into sight, paused an
instant at the bench, and strode toward the box.
Hillman’s cheered and Farview jeered. Nate went to the bench
with hanging head. As he tossed the ball to the relief pitcher Laurie
saw Mr. Mulford pull Nate to a seat beside him and put a big arm
over the sorrowful one’s shoulders. Then George Pemberton was
pitching his warm-up balls, and Laurie was devoutly hoping that they
weren’t samples of what he would offer later. They were, but Laurie
didn’t know it then, for, with three balls and but one strike on him, the
over-eager Farview third baseman struck at George’s first offering
and got it. The bases emptied, and red legs streaked for the plate.
But far out in deep center field Lee Murdock cast one last look over
his shoulder, turned, and pulled down the fly, and Hillman’s let loose
with a sound that was half a groan of relief and half a yell of joy!
With the score 3 to 0 against her, Hillman’s pulled up even in the
last of the sixth. Craig Jones worked a pass; Tom Pope sacrificed
him neatly to second; and Captain Dave, functioning perfectly at last
in the rôle of clean-up batter, hit for two bases, and both Cooper and
Jones scored. Pat Browne was safe on a fielder’s choice, Dave
going out at third. Brattle hit safely, and Murdock was passed. The
bags were all occupied, and the home team’s cohorts roared
exultantly and waved blue banners in air. And Laurie came to bat.
I’d like immensely to tell how Laurie knocked a home run or even a
single, but truth compels me to state that he did nothing of the sort.
He swung twice at good ones and missed them, and ended by
swinging a third time at a very poor one. It remained for Pemberton
to deliver the hit and, perhaps because he was a proverbially poor
batter and wasn’t feared one bit by Mr. Luders, he selected the
second delivery and jabbed it straight at the young gentleman’s
head. Luders put up a defensive hand. The ball tipped it and
bounded toward second. Three players ran for it. By the time short-
stop had got it, Pemberton was galloping up to first, and Pat Browne
had slid in a cloud of dust across the plate. A moment later Brattle
was caught off second, and the trouble was over for the time.
The seventh began with the score 3 to 3, but it wouldn’t have
remained there long if George Pemberton had been allowed to pitch
the inning through. George was even wilder than he had indicated.
He couldn’t find the plate at all. Four successive balls put a Farview
batter on first. One strike, a foul back of the plate that Laurie missed
by inches only, and four more balls put another runner on bases.
Laurie begged, counseled, threatened. George nodded agreeably
and still sent them in anywhere but at the expected spot. When he
had pitched one strike and two balls to the third man up, Coach
Mulford gave the “high sign” and George, not at all regretfully, it
seemed, dropped the ball and gave way to Orville Croft.
Somehow Croft came through unpunished. There were no more
passes, for Croft put the ball over the base nicely, but there were so
many near-hits that Laurie’s heart was in his mouth almost every
minute. If the Hillman’s fielders hadn’t worked like a set of young
professionals in that inning awful things would certainly have befallen
the Blue. The infield showed real ball playing, and thrice what
seemed a safe hit was spoiled. Farview got the first of her runners to
third, but he finally died there when Captain Dave dived to the base-
line and scooped up a ball that was on its way to deep left.
For Hillman’s the last of the seventh made good its reputation. It
was the lucky seventh, and no mistake about it. Luck put Cooper on
first when Luders slanted a slow curve against his ribs, and luck
decreed that the red-legged short-stop should drop the ball a minute
later when Cooper took advantage of Jones’s slam to third. Perhaps
luck had something to do with the pass handed to Pope, too, but it
certainly didn’t altogether govern Captain Dave’s second long hit that
sent in Cooper and Jones and put Hillman’s in a veritable seventh
heaven—I almost wrote “inning”—of delight!
That hit ended Luders’s usefulness. He issued another pass, got
himself into a hole with Frank Brattle, and was derricked, a sandy-
haired youth named Clay succeeding him. Clay disposed of Brattle
very neatly, Murdock flied out to short-stop, and again Laurie failed
to deliver the hit that was, he felt certain, somewhere inside him.
Laurie brought the lucky seventh to a close by knocking a weak
grounder to first baseman.
Hillman’s visioned victory and was joyous and noisy when the
eighth began, but after the first Farview batsman had lined out
Croft’s first offering for two bases the joy paled and the noise
noticeably subsided. And when the next red-legged batter had hit for
a single it began to dawn on the Hillman’s supporters that possibly
the old adage to the effect that he who laughs last laughs best might
be true. Hillman’s pitching staff was exhausted, and if Croft went the
way of Beedle and Pemberton—and he gave every indication of
doing so—the only way the Blue would get the game would be as a
gift from Farview! The Maroon and White took to Croft as a duck
takes to water. He didn’t have much except a couple of slow curves.
His fast one wasn’t exceptionally fast, and it generally failed to locate
the plate. Those slow curves pleased the Farview batsmen
immensely. Even the tail-end of their list found no trouble in hitting
them. Laurie, watching the man on first as a cat watches a mouse,
saw more than a runner who might steal second; he saw a victory
fading into defeat.
Croft worked two strikes on the next man, and then again came
the dread sound of wood against leather. This time, though, the ball
arched high and Cooper, racing back, got under it, and there was
one down. The runner on third had no chance to score, or thought
so. Then, when Captain Dave had talked briefly but earnestly to
Croft, that youth promptly issued one more base on balls, and the
sacks were filled, and defeat loomed large on the horizon. One
down, the bases full, and Croft going the way of the others! Laurie’s
gaze wondered to the bench and Coach Mulford. And then, since to
have looked at the bench at all without seeing it would have been
impossible, he glimpsed the round, anxious, earnest countenance of
Kewpie Proudtree. Laurie’s heart jumped out of place for possibly
the twentieth time that afternoon, and he called to Captain Dave.
The game was held up while captain and catcher conferred.
Finally Dave hurried across and hailed the coach. Another
conference followed, while Farview clamored for the contest to go
on. Then Mr. Mulford waved his hand at Croft, and Kewpie, very
much surprised but apparently not at all overwhelmed, walked into
the diamond, pulling on his glove.
There was a moment of silent amazement. Then Farview went
delirious with delighted amusement. The Farview stand almost
rocked with the laughter that emanated from it, laughter that came as
a relief to strained nerves and was indulged in freely. Hillman’s,
recovering from its first instant of amazement, cheered valiantly, and,
cheering, took hope. After all, it might well be that the chubby
Proudtree would prove no worse than Croft. It was even possible
that he might be an improvement on that youth. Meanwhile Farview
laughed until tears came and Laurie and Kewpie met midway of
mound and plate.
“Go slow, Kewpie,” said Laurie, “and follow the signals. Take all
the time you can; hear? Waiting may worry them. Keep your nerve,
son, no matter what happens. Just pretend that you’re pitching to me
in practice.”
“Sure,” agreed Kewpie complacently. “Don’t worry about me, Nod.
Let’s go!”
One down and three on, a hit meaning two runs! It was a tough
situation that Kewpie faced. But Kewpie seemed totally unworried.
Laurie saw and marveled. His own heart was thumping inside him
like a small sledge-hammer. He wondered if Kewpie was faking that
unconcern and would presently go to pieces like the others, letting in
an avalanche of runs!
But Kewpie was right. Laurie needn’t have worried about him.
Kewpie was magnificent, if a boy of Kewpie’s size and proportions
can ever be magnificent! He was as slow as cold molasses, yes, and
his delivery elicited more amusement from the enemy, but he struck
out with apparent ease the first batsman who faced him, caused the
next man to foul out to Captain Dave, and fanned the third!
When that last of the enemy waved through empty air and then
cast his bat from him venomously, Hillman’s loved Kewpie Proudtree
with a deep and fervid passion. Hillman’s said so. Hillman’s rose
from stand and greensward and cheered his name to the blue
afternoon sky and howled and yelled and went crazy generally. And
Kewpie moved smilingly back to the bench to submit to the hugs of
his companions.
There was no scoring for the Blue in the last of the eighth, for Clay
was master of the situation.
Then Farview started her half of the ninth with desperation written
large on every countenance. Kewpie, the unhurried, returned to his
job. He disposed of the Farview pitcher with four deliveries and then
faced the head of the list. That he would survive that inning without
misadventure was too much to hope for. The misadventure came
when the Farview center fielder slammed a ball into left field and got
two bases. Kewpie looked, or so Laurie though, a little surprised and
a little grieved, but he didn’t allow his emotions to affect his pitching.
He fooled the next man twice with his out-drop and finally finished
him with a slow ball that the batter struck at too soon. Hillman’s
shouted, waved, and prepared to go home.
But the end was not yet. Up came the Farview captain, and he
made it plain to Laurie at once that he wasn’t to be caught with
trifles. He demanded good ones. If he didn’t get them he wouldn’t
swing. He didn’t say all this in words, of course, but he looked it and
showed it by calmly watching Kewpie’s first offering drop by him, a
scant inch beyond the outer corner of the plate. In the end, he had
his way. There was something that suited him, and he accepted it
and drove it down third base line, scoring the man on second and
placing himself on third when the throw went to the plate. Those who
had wandered toward the exits reconsidered and stayed their steps.
With a runner on third the score might yet be tied.
The Farview right fielder had not yet made a hit, but that to
Laurie’s thinking made him the more dangerous, and Laurie worked
very carefully. Kewpie answered the first signal with a straight one
over the center of the plate, and it went for a strike. The next was
also over the center, but too high. Then again Kewpie failed. One
and two now. The runner on third was dashing up and down the
path, and the coachers were yipping like mad. Kewpie, however
remained surprisingly calm. To show how calm he was he sent in a
drop that scored a second strike for him, and the blue pennants
waved triumphantly. Laurie called for the same thing again, but this
time the batter did not offer at it; the score was two and three, and
Laurie’s heart sank. The next must be good. He placed his hands out
and called imploringly:
“Right into the old mitt, Kewpie! Make it good!”
And Kewpie made it good, and, since it was good, unmistakably
good, the Farview youth swung against it with all his might.
But he hit under it, and the ball went up and up in the sunlight
almost straight above the plate. Cries arose from all sides, a
confusing bedlam of warning, entreaty, command. Laurie dashed his
mask behind him, stared upward into the blue, saw the gray sphere
poised overhead, turned and stepped back, looked again, again
retreated. He was under it now—almost. One step further toward the
back-stop—
Then Nemesis took a hand, or sought to. Laurie’s backward
placed foot found the discarded mask. He strove to retain his
balance but could not and fell backward to the ground. The mask
described a curve and landed yards away. Laurie’s feet flew
heavenward. His hands were stretched wide. Then his startled gaze
saw a new danger. Right above him was the ball, falling straight for
his face. Nothing save pure instinct, the instinct that causes one to
fend off a blow, brought his hands up before him. It was, however,
not so much instinct as baseball training that brought them there
palms upward. And, beyond any doubt, it was training that caused
his fingers to close convulsively about the round object that landed
with a loud smack in the hollow of his old brown mitten!
The Graduation Ball was over, and as the twins walked homeward
with Polly and Mae twelve o’clock struck from the tower of the
Congregational Church across the park. There was a big round
moon riding high in the heavens, and the June night was warm and
scented. Mae was to spend the night with Polly, and so the four kept
together across Walnut Street and past the Starling house where, on
the second floor, one lighted window proclaimed the presence of
Bob. Even as Ned proposed a discreet hail, the light behind the
shade went out.
“It was a lovely dance, wasn’t it?” asked Polly. Laurie, beside her,
assented. “It’s been a perfectly gorgeous day,” added Polly. “All of it.
It was such fun this morning at Miss Comfort’s. And that Mr. Goupil is
a darling duck, isn’t he? And, oh, won’t it be perfectly corking next
fall, Laurie, when we have the boat for our own? Think of the good
times we can have! It was wonderful of Miss Comfort to think of it.”
“Bet you anything,” chuckled Laurie, “she’ll wish herself back
there. Dare say she won’t be able to sleep on shore again after a
summer on the rolling deep!”
Polly laughed. “She’s a dear, isn’t she? And, Laurie, didn’t
everything turn out beautifully this spring? Think how we ‘reclaimed’
Kewpie and—”
“Heard Kewpie’s latest? He told Ned and me before supper that he
might not be able to play football next fall because he didn’t want to
risk hurting his pitching arm! He’s a rare bird, that Kewpie!”
“Oh, he must play football! But he will, of course. Wasn’t he
splendid this afternoon? And—and weren’t you splendid, too? I just
shrieked and shrieked when you made that perfectly wonderful catch
and saved the game!”
“I didn’t save the game,” answered Laurie. “I dare say that fellow
would have struck out in another minute. Anyhow, Kewpie says he
would have!”
“But Kewpie doesn’t know, and if he had made a hit it would have
tied the score at least. Anyhow, your catch was absolutely
marvelous. Every one says so.”
A short silence followed. Then Laurie said resolutely: “Look here, I
guess you might as well know the truth about that, Polly. I didn’t
really make that catch.”
“Why, what do you mean? I saw you make it!”
“Yes, I know, but—well you see, I didn’t intend to do it. I saw that
ball coming down straight for the end of my nose, and I just put my
hands up to ward it off. Of course every one thinks I’m a regular
wonder, but I’m not. It was just an accident. I—I haven’t told any one
but Ned—and you.”
“That doesn’t spoil it a bit,” declared Polly. “You did catch the ball,
didn’t you? And if you’d just been trying to keep it from hitting you
you wouldn’t have really caught it, would you?”
“That’s what Ned said,” mused Laurie. “Hanged if I know!”
“Ned’s perfectly right,” responded Polly emphatically.
“Of course I am,” said Ned as he and Mae joined them before the
door of the little shop. “But what is it this time?”
“Never mind,” said Polly. “You can ask Laurie.”
“He probably won’t tell me,” said Ned gloomily. “He hates to say
I’m right about anything. Gee, Polly, it seems funny to think that I
won’t see this place again for three months.”
“It’s horrid,” answered Polly, and Mae murmured agreement. “Still,
I suppose three months won’t seem awfully long. And you will write,
won’t you?”
“Certainly will,” asserted Ned. “And don’t you forget to. But we’ll
see you both in the morning. We don’t get away until eleven twenty-
two. Thanks for coming to the dance.”
“Thanks for asking us,” said Polly, her hand on the door. “Good
night. Good night, Laurie. We’ve had a lovely time.”
“Same here,” said Laurie as he tugged at Ned’s sleeve.
Ned joined him at the edge of the sidewalk, and they took their
caps off and bowed in the manner of Mr. Goupil.
“Beneath yon moon’s effulgent light—”
“We, Nid and Nod, wish you Good Night!”
Transcriber’s Notes:
Except for the frontispiece, illustrations have been moved to
follow the text that they illustrate, so the page number of the
illustration may not match the page number in the List of
Illustrations.
Printer’s, punctuation and spelling inaccuracies were silently
corrected.
Archaic and variable spelling has been preserved.
Variations in hyphenation and compound words have been
preserved.
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Textbook Biomechanics of Soft Tissues Principles and Applications First Edition Al Mayah Ebook All Chapter PDF

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Biomechanics of Soft Tissues :

Principles and Applications First

Biomechanical aspects of soft tissues 1st Edition Loret

Sarcomas of Bone and Soft Tissues in Children and

Soft Computing and Its Applications Volumes One and Two

PRINCIPLES OF MACROECONOMICS 5E Ben Bernanke Et Al

Soft Computing Applications Proceedings of the 8th

Soft Computing Applications: Proceedings of the 6th

Soft Computing Applications: Proceedings of the 7th

Fibre optics : principles and advanced practices Second

© 2018 by Taylor & Francis Group, LLC

No claim to original U.S. Government works

Printed on acid-free paper

International Standard Book Number-13: 978-1-4987-6622-7 (Hardback)

and the CRC Press Web site at

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

The emerging paradigm of incorporating images and biomechanical properties of soft

The combined medical and engineering expertise of contributors makes this

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

Adil Al-Mayah Derek Gillies

Wanis Nafo Sivabal Sivaloganathan

Jessica Rodgers Michael Velec

1.1.2 Source of Mechanical Response in Soft Tissues

1.1.3 General Mechanical Behavior

1.2 Linear Elasticity

Stress Tension Compression

1.2.2 Elastic Properties of Human Tissues

TABLE 1.1 Elastic Modulus of Different Human Soft Tissues

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

Stress Region I: Region II: Region III:

Large deformation under Increasing stiffness Highest stiffness

Strain (or stretch ratio)

TABLE 1.2 Nonlinear Stress–Strain Energy Function

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

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

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

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

where Cij is a material parameter.

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

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

1.3.2 Hyperelastic Properties of Human Tissues

TABLE 1.3 Human Tissue Hyperelastic Parameters

Hyperelastic Model and Parameters Testing Method Reference

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

C20 = 114 ± 40 kPa

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

Elastic Viscous Viscoelastic

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

Time Time Strain

TABLE 1.4 Linear Viscoelastic Models

Model Configuration Creep Function Relaxation Function

Standard linear solid E2 η Deformation

1.4.2 Viscoelastic Properties of Human Tissues

TABLE 1.5 Human Tissue Viscoelastic Parameters

Tissue Testing Method Parameters Reference

E* (complex Young’s modulus) is a frequency-dependent Young’s modulus.

In the aforementioned elasticity, hyperelasticity, and viscoelasticity models, a mate-

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