11
Biomechanics of Soft Tissue
Roger C. Haut
The human body is composed of four primary
groups of tissues: (1) Epithelial tissues are char-
acterized by having cells closely joined one to
another and found on free surfaces of the body.
(2) Muscle tissues are characterized by the high
degree of contractility of their cells or fibers.
Their primary function is to move the skeleton.
(3) Nervous tissues are composed of cells spe-
cialized in the properties of irritability and
conductility. (4) Connective tissues are those in
which the cells are separated by large amounts
of extracellular materials.
Tissues are combined in the body to form
organs. Organs are defined as structures com-
posed of two or more tissues integrated in such
a manner as to perform certain functions. The
heart, for example, has its chambers lined with
a special epithelium, its walls are primarily
muscle, and there are connective tissues present
in numerous forms.
Connective tissues represent wide-ranging
types, both in their variety and distribution. They
are all characterized, however, by large amounts
of extracellular material. Their functions are as
varied as the tissues themselves. These tissues
bind, support, and protect the human body and
its vital organs. Structural integrity and function
of vital organs are adversely affected when
connective tissue surrounding them is damaged.
Connective tissues give us the strength to resist
mechanical forces, and provide a recognizable
shape that persists in the face of these forces. 1
The connective tissues can be classified by
their extracellular constituents. Connective
tissue proper is subdivided into loose, dense, or
228
A. M. Nahum et al. (eds.), Accidental Injury
© Springer Science+Business Media New York 2002
regular. Loose connective tissue is widely dis-
tributed. For example, it is found in the walls of
blood vessels, surrounding muscles as fascia,
and in the lung parenchyma. Dense connective
tissues contain essentially the same elements as
loose connective tissue, but there are fewer cells.
This type of tissue is found in skin, many parts
of the urinary ducts, digestive organs, and blood
vessels. The strom as and capsules of the internal
organs, e.g., kidney and liver, are dense connec-
tive tissues that are responsible for maintain-
ing the structural integrity of organs against
mechanical forces. Other body components,
having primarily mechanical functions, are com-
posed almost exclusively of connective tissue
with few cells called regular connective tissue.
Bone tissue forms the greater part of the skele-
ton. Tendons and ligaments have a parallel
arrangement of the extracellular components
that allow these tissues to transmit tensile loads.
All connective tissues are, in fact, complex
fiber-reinforced composite materials. The
mechanical properties of soft connective tissues
depend on the properties and organization of
collagen fibers in association with elastin fibers,
which are embedded in a hydrated matrix of
proteoglycans. The constitution of each connec-
tive tissue is tuned to perform a specific func-
tion. Ligaments provide mechanical stability to
joints. The function of tendons is to transmit
tensile forces to bone via a muscle. A blood
vessel has to distend in response to a pulse wave,
and subsequently recoil to contribute to the
propulsion of blood. Skin is a soft connective
tissue that supports internal organs and protects
11. Biomechanics of Soft Tissue 229

the body from abrasions, blunt impact, cutting, Collagen

and penetration, while at the same time allow-
ing considerable mobility. The articular surfaces
of diarthrodial joints are covered with a 1- to 5-
mm layer of connective tissue, called articular
cartilage. The primary functions of the cartilage
are (1) to spread loads across joints and in so
doing to minimize contact stress, and (2) to allow
relative movement of the opposing surfaces with
minimum friction and wear. Impact trauma to
the body can cause excessive distortions of
connective tissues leading to organ dysfunction.
Collagen is a fibrous protein that provides soft
connective tissues with tensile strength.
Collagen molecules are synthesized by fibrob-
lastic cells as large precursors (procollagen),
which are then secreted and cleaved extracel-
lularly to become collagen.2 More than a dozen
different types of collagen have been isolated. 3
The most common collagen is type I. This
molecule consists of three polypeptide chains,
each coiled in a left-handed helix3 with approx-
imately 100 amino acids (Fig.1l.1). The three a
chains are combined in a right-handed triple
helix that gives the collagen molecule a rodlike
shape. The length of the molecule is about

Amino acid sequence

gly -'-y- gly-pro-hypro- gly-,-y

Triple helix of amino acid chains

Tropocollagen molecule

-===;:;:;===~ :L15A
~_
3,IXXlA
.,l
Quarter stagger arrangement of molecules

Banded pattern resulting from overlap and hole zones

111111111111111
INTRAMOLECULAR CROSSLINK

INT(RMOlECUlAR CROSSlINKS

==~'" M

~~:~========~:
M.-------.Wllll"q...,M
TENDON

fibrobla.t. woveform
crimp ~rvcture membrane
~i I I I
15A 35A 100-200 A 500-50001 50-300JI 1OO-500Jl
SIZE SCALE

FIGURE 11.1. Schematic representation of the molecular arrangement of collagen in the fiber bundle of rat
tail tendon. (From Haut. 8 )
230 R.c. Haut

280nm, and its diameter is about 1.5nmY
Almost two-thirds of the collagen molecule
consists of three amino acids; glycine (33 %),
proline (15%), and hydroxyproline (15%).5
Every third amino acid in each a. chain is
glycine, and this repetitive sequence is essential
for the proper formation of the triple helix.
Glycine enhances the stability of the molecule
by forming hydrogen bonds among the three
chains of the superhelix. Hydroxyproline and
proline form hydrogen bonds, or hydrogen-
bonded water bridges, between specific groups
on the chains. Type III collagen is thought to be
an immature form of type I because of its high
concentration in young or healing connective
tissues. 3 Type II collagen is unique to cartilage.
Soon after being expressed into the extracel-
lular space, collagen molecules are arranged in
a quaternary structure. Crosslinks are formed
between molecules and are essential to the
aggregation at the fibril level. The crosslinks
derive mainly from four lysine and hydroxyly-
sine residues, one at each end of the helical
region and one in each telopeptide region. 61t is
the crosslinked character of the collagen fibrils
that gives strength to connective tissues. Nimni
and Harkness3 provide a detailed description of
the inter- and intrachain crosslinks in collagen.
The degree of covalent crosslinking in collagen
is altered during maturation. 7 Dietary lathyro-
gens can inhibit crosslinking by inhibiting the
action of the enzyme lysyl oxidase. Some under-
standing of the role of covalent crosslinking
on mechanical strength has been gained with
lathyritic agents. 8,9
The mechanical properties of collagen are
fibrils.15 The tensile modulus of collagen
depends on age and the degree of maturation.8
At an early age the modulus is approximately
400 megapascals (MPa), and it increases to
approximately 600MPa at maturity. The "com-
puted" modulus depends on the length of spec-
imen being tested. 16 One study, based on x-ray
diffraction, indicated that the collagen mole-
cule is stiffer than a collagen fibril or a tendon
(Fig. 11.2)Y
Deformation of RIT up to 2% to 3% strain
has been found reversible with no mechanical
damage. ll Above approximately 4 % strain,
permanent damage has been observed in the
collagen fiber with a reduction of its tensile
modulus and irreversible disruption of the
crimp waveform of its fibrils. ll ,15 Kastelic and
Baerl8 have discussed the mechanism of tensile
yielding and failure of RTT collagen fibers
using electron microscopy and small angle x-
ray (SAX) diffraction. A slight broadening of
the SAX pattern and signs of limited intrafib-
rillar slip are observed in the first yield region.
More significant damage is observed in the
second yield region. At fracture the fiber seems
to separate into filaments averaging 10~.Im in
diameter. 19
It appears that resistance to intrafibrillar slip
in the collagen fiber starts with maturation con-
current with the appearance of "yield" behav-
ior. The resistance increases with age, as does
20

-
0

often determined in experiments on tendon 0

0
and ligaments, where it appears as parallel II
•
-•
a. 0 0

. • 0
oriented fibrils. lO The tensile response of a :E 0

collagen fiber from rat-tail tendon (RTT) at • 0

0
0
0
0
10 0
low strain is associated with straightening of c(
0 0
0 0
crimped collagen fibrils ll ,12 and their shear .......... 0
0
interaction with the hydrated matrix. 13 Kastelic IL. 0
0
0
et aP4 showed that the crimp angles in individ- 0
0
ual collagen fibrils varies radially across the 000
fiber bundle, leading to a sequential uncrimp-
1 2 3 4 5 6
ing of fibrils with deformation. Subsequent to
the "toe" response is a linear region followed FIGURE 11.2. Comparison of the stress-strain curves
by yield and failure regions. The linear region is for a collagen molecule (.), a collagen fibril (0), and
thought due to elastic deformations of collagen a tendon (0). (From Sasaki and OdajimaY)
11. Biomechanics of Soft Tissue
the apparent modulus of the yield region. When
exposed to dietary lathrogens, resistance of col-
lagen to intrafibrillar slip is compromised.8The
tensile strength of collagen from RTf varies
from approximately 50 to 100MPa, depending
on the degree of maturation. 8 Failure strains
vary from approximately 11 % to 18% for the
mature fiber. Failure strain increases with ageY
In contrast, Betsch and Baer lO document
decreasing failure strains with age. The mor-
phology of the collagen fibril structure is criti-
cal in determining its tensile strength,z° The
greatest contribution to the tensile strength of
a collagen fibril is its connectivity. In numerous
diseases collagen fibril connectivity is inter-
rupted and tensile strength of the connective
tissue is significantly decreased.
Studies also show that tensile strength and
failure strain of collagen significantly depend
on strain rate. 21 Tensile strength and failure
strain are approximately 108MPa and 18%,
respectively, at 720%/s compared to 61 MPa
and 14.7% at 3.6%/s?
Elastin
Elastin is another major protein of connective
tissues. It is normally present at significant
levels in blood vessels, the lungs, and skin. The
collagen content of the human Achilles tendon
is about 20 times that of elastin, while in liga-
mentum tlavum of the spine the elastin content
is about five times that of collagen. Like colla-
gen, glycine accounts for about one-third of
the total amino acids of elastin. The contents
of proline and hydroxyproline are much lower
in elastin than collagen. The fundamental
polypeptide chain in elastin is tropoelastin,z2
Assembly of multiple tropoelastin molecules
gives elastin its characteristic elastic properties.
Critical in the assembly is the formation of
crosslinks between tropoelastin molecules.
Allysine residues react nonenzymically with
lysine residues for the characteristic crosslink. 23
Each chain forms a fibrillar structure composed
of alternating segments of crosslinked regions
and structures termed "oiled coils," which may
be stretched from 2 to 2.5 times the length of
relaxed molecules.
231
It is recognized that elastin provides elastic-
ity to connective tissues, but its exact role is
not well understood. The function of elastin
is dependent on its configuration and relative
content in a given material. 24 It is important to
note that in most tissues it is not the content of
elastin alone that dictates mechanics, but rather
its organization relative to collagen. While the
mechanical properties of collagen are typically
estimated from those of RTf, no such pure
form exists for elastin. Human and bovine
aorta and bovine ligamentum nuchae are the
most common sources of elastin fibers. Aortas
contain approximately 40% elastin by dry
weight, while ligamentum nuchae contains 78%
to 83% elastin. 25 Ligamentum nuchae yields a
modulus of approximately 0.3 MPa,z6,27 Carton
et al28 conducted experiments on individual
elastin fibers after dissection from the ligamen-
tum nuchae of the ox. They found a linear
tension-strain curve to approximately 120%
strain. Hass 29 reports a modulus of 3 MPa for
elastin. Jenkins and Little25 used formic acid
to remove collagen from bovine ligamentum
nuchae and showed that the stress-strain curve
of elastin is essentially linear and displayed
minimal time dependency (Fig. 11.3). Minns
and Steven30 conducted tensile experiments at
five stages in the development of fetal bovine
ligamentum nuchae. Strips tested to failure
suggest that the strain at failure decreases from
approximately 280% to 220% at birth. The
tensile stress at failure remained constant until
birth at approximately 1.4MPa. Mature elastin
fibers can be strained to approximately 130%
at lOMPa before failure,z8
Matrix of Proteoglycans
The matrix in which collagen and elastin fibers
are embedded is composed of proteoglycan
aggregates formed from three molecular
species: proteoglycan subunits, hyaluronic acid,
and link protein.31 In its formation each com-
ponent appears separately in the matrix. Pro-
teoglycan subunits noncovalently bind to a
single hyaluronate chain. Link protein is then
incorporated and appears to stabilize the
bond between prot eo glycan subunits and
232
25
2.0
ca
D.
~ 1.5
U)
U)
W
a:: 1.0
I-
U)
o 10 20 30 40 50
STRAIN, %
hyaluronate. The proteoglycan subunit consists
of chondroitin sulfate, keratin sulfate, and pos-
sibly dermatin sulfate covalently attached to
the protein core. These glycosaminoglycans are
linear polymers of sugar residues with a disac-
charide repeating unit. Chondroitin sulfate,
for example, is composed of 40 to 60 repeating
units, is 20,000 to 30,000 in molecular weight,
and ranges in length from about 40 to 60nm.
The hyaluronic acid chains that form the fila-
mentous backbone of proteoglycan aggregates
vary greatly in size, ranging from 200,000 to
over 2 million in molecular weight and from 50
to over 5,OOOnm in length. A proteoglycan
subunit may have 100 chondroitin sulfate
chains attached to a protein core 200,000 in
molecular weight and 200nm in length. The
proteoglycan subunit can be 2 to 3 million in
molecular weight. A proteoglycan aggregate
containing 100 such proteoglycan subunits
would be over 200 million in molecular weight.
In tissues such as cartilage, the proteoglycan
aggregates are effectively immobilized within
a fibrous network. 32 In addition, they are
hydrophilic because glycosaminoglycan mole-
cules contain a high density of negatively
charged groups, which gives rise to imbalance
in the concentration of freely diffusible
electrolytes.
R.c. Haut
FIGURE 11.3. Experimental data from
ligamentum nuchae showing the nearly
linear tensile response of elastin.
(Adapted from Jenkins and Little. 25 )
60 70
Proteoglycans also seem to playa major bio-
logic role in structure of collagen. Collagen
fibrillogenesis, in vivo, may be controlled by
a feedback system whereby the stress history
on fibroblastic cells determines the synthesis
of specific glycosaminoglycans.33 The impor-
tance of two common sulfate-containing
glycosaminoglycans is evident from in vitro
studies. These have shown that in the presence
of chondroitin sulfate, fine fibrils are formed,
while in derma tin sulfate fibrillogenesis is
retarded and relatively large fibrils are
formed. 34,35 Connective tissues that require high
tensile strength usually contain large diameter
collagen fibrils, while those whose primary
function is low-load creep resistance have a
larger proportion of small diameter fibrils?3 In
tendon there is clear evidence of specific inter-
actions between collagen and the matrix of pro-
teoglycans, whereas interactions in cartilage
are probably less specific, involving entrapment
and excluded volumes. 36
The role played by the matrix of proteogly-
cans in the mechanical properties of connective
tissue is not presently well understood. The
matrix comprises only a small fraction of most
connective tissues. This noncollagenous compo-
nent appears partly responsible for the cohe-
sion of tendon fibers?7 Proteoglycan-based
11. Biomechanics of Soft Tissue
filaments are shown attached to collagen at spe-
cific polar locations and interconnecting colla-
gen fibrils. 38 Kronick and Sacks39 have shown
no significant effects of proteoglycan extraction
on the static mechanical properties of biologic
tissues. Other studies suggest the matrix pro-
vides a viscous lubrication between individual
fibrils of collagen.37,40,41 Viscoelastic properties
of numerous tissues have been associated with
the interaction of collagen with the surround-
ing matrix. 42 The matrix in RTI has been
modeled as viscoelastic with a time-dependent
shear modulus. 15 The modulus of the matrix at
3 months of age is approximately 0.1 MPa and
is found to increase 15-fold at maturity. The
complex shear modulus of purified solutions
of proteoglycan monomers and aggregates is
approximately 0.01 MPa at concentrations
similar to that in cartilage. 43 The shear viscosity
is dependent on concentration and shear rate,
being approximately 1.0 pascal-second (Pa-s) at
typical concentrations. Using viscometric flow
measurements on high concentrations of puri-
fied proteoglycan solutions,44 investigators
find that collagen in a collagen-proteoglycan
mixture enhances molecular interactions by
increasing the entanglement interactions
and/or the strength of interaction, while pro-
teoglycans act to reduce the number and/or
strength of molecular interactions.45
Tensile failure studies suggest that the matrix
may help stabilize the collagen fibril at high
rates of loading. 18,21,46,47 On the other hand,
enzymatic digestion studies indicate that the
sensitivity of tissue strength to strain rate is not
directly related to the content of matrix pro-
teoglycans. 48 Lanir49 suggests the kinematics of
collagen and elastin fiber reorientation under
tensile load is determined by the matrix com-
ponent. Hurschler et al50 suggested a similar
matrix effect after studies measured positive
hydrostatic pressures within the ligament
during tensile stretch. 51 These data are sup-
ported by others showing a gross exudation of
tissue fluid during tensile stretch of ligaments
and tendons. 52-54 Interestingly, however, a math-
ematical model of the ligament that includes
a matrix exhibits a negative pressure during
tensile stretch of the ligament. 55 Atkinson et al 56
presents a theoretical model of a collagen sub-
233
fascicle that does exhibit a positive pressure
gradient during tensile stretch. The study sug-
gests a "wringing-out" of tissue fluids during
extension of helically wound fibrils within this
collagen substructure. The model analysis
suggests hydrostatic pressure developed in
the matrix of tissue proteoglycans helps deter-
mine the rate-sensitive properties of soft
tissues. Thus, it is hypothesized that the degree
of hydration help determine the viscoelastic
properties of soft connective tissues.57,58
Ligaments and Tendons
Ligaments and tendons are dense connective
tissues known as parallel-fibered collagenous
tissues. The role of ligament, which connects
bone to bone, is to augment the mechanical
stability of joints and control joint motion. The
function of tendon is to attach muscle to bone
and transmit tensile loads, thereby producing
joint motion. Like other connective tissues,
tendons and ligaments consist of only a few
cells (fibroblasts) and an abundant extracellu-
lar matrix. The content of collagen is slightly
higher in tendons than in ligaments. 59 The
content of elastin varies between ligaments,
depending on function. While ligaments from
the knee, for example, contain small amounts
of elastin, spinal ligaments typically contain
greater amounts of elastin. 60 While the ratio
of collagen to elastin is 1: 2 in ligamentum
flavum,61 the interspinous ligament is predomi-
nantly collagen. 60 These differences in constitu-
tion and organization of collagen and elastin in
various spinal ligaments are reflected in their
mechanical properties (Fig. 11.4).
The nonlinear, stiffening response of liga-
ments is due to the structural responses of col-
lagen and elastin in the matrix of proteoglycans.
Bundles of collagen measuring approximately
20/.lm in width have a characteristic crimp
that varies between ligaments depending on
their particular function. 62 Elastin fibers appear
straight and in close association with collagen.6o
Tensile studies on bone-ligament-bone
preparations have shown nonuniform strain
patterns with large strains existing near inser-
tions into bone. 63 ,64 This has led to structural-
234
FORCE, N
600 .--------------------------------,
500
400
300
200
100
o~~~~--.---------~-.------~
o 1 2 3
DEFORMATION. mm
based models in which crimp angles in collagen
vary down the length of the ligament.65 During
quasi-static tensile deformation, the 20-J..lm-
wide bundles of crimped collagen sequentially
straighten and bear load. 62 The current concept
is that elastin fibers bear load first. Assuming
that the crimp angles in collagen are normally
distributed,66 tensile loads in the early "toe"
region are due to tensile deformation of elastin
fibers and the percentage of the collagen fibers
that have straightened (Fig. 11.5). Structural-
based models have been proposed for soft con-
nective tissues that incorporate the uncrimping
of collagen during tensile stretch. 67-72
The tensile modulus of the human patellar
tendon (PT) varies between investigators: 288
± 18MPa73 and 415 ± 31 MPa.74 The tensile
modulus of human digitorus tendons is approx-
imately 600 MPa. 75 Pintar et aF6 documented
the mechanical properties of various human
lumbar ligaments from specimens ranging from
31 to 80 years of age. The modulus of the
human anterior cruciate ligament (ACL) is 111
± 26MPa for young specimens (16-26 years)
R.c. Haut
FIGURE 11.4. Tensile responses of
the human posterior longitudinal
ligament (PLL), the anterior longi-
tudinal ligament (ALL), and the
ligamentum flavum (LF) showing
the changes due to the content and
organization of collagen and elastin.
(Adapted from Panjabi et aflO)
decreasing continuously to 65 ± 24 MPa for
older specimens (48-86 years).77 Another study
shows this same trend with age. 78 The tensile
properties of tendons have also been found to
depend on age in other studies. 75 ,79 A decrease
in the extractability of collagen with pepsin
has been correlated with a decrease in tensile
modulus of the canine PT with increasing age. 80
Biochemical analyses indicate that these age-
related changes correlate with a decrease in
collagen synthesis and reducible crosslinks
in collagen.81 Immobilization causes a marked
decrease in the modulus of ligaments, while
exercise has a more limited positive effect. 82
When isolated collagen fibers are loaded,
damage is reported at strains above approxi-
mately 4%.11 However, for whole ligaments and
tendons the linear response can extend above
20%. Studies, however, have shown failure of
some fine collagen fibers can go undetected in
macroscopic tests. Scanning electron micro-
graphs of ligaments stretched into the linear
region show ruptured collagen fibers at loads
one-half the maximum (Fig. 11.6).83,84 Near the
11. Biomechanics of Soft Tissue 235

end of the linear region sequential failure of a appear to fail at different points along the
few stretched bundles develops and the process length of the ligament, producing the classic
gradually progresses until the ultimate load of "mop-end" appearance. 77 Panjabi et als5
the structure. Throughout this process the liga- showed that ligaments stretched to 80% of their
ment may visually appear intact. Fiber bundles failure strain exhibit a significant increase in
compliance that may yield a joint laxity.
Some microstructural models of ligaments
and tendons incorporate failure mecha-
nisms. 5o,s6,s7 These models suggest that collagen
I I I I
I I I I fibers fail sequentially as strain reaches approx-
I I I I imately 10%. These data compare favorably
I I I I
with experimental data. 88 A more general
I I I I
elastin k)aded, I I I I model of soft connective tissuess9 is interesting
I • I
collagen
unaimping
"tin loaded, I I
in that it includes uncrimping of collagen and
1811 collagen loaded I ela,tin
tome coftagen Ioeded el.ltin loaded,
Ioeded.
lome collagen fails
stretching and breaking of fibers, while taking
I account of fiber volume fraction, fiber and
matrix properties, fiber orientation, and matrix
I
resistance to fiber reorientation during tissue
I stretch.
I The tensile strength and failure strain for the
I human ACL from young specimens aged 16 to
26 years, is 37.8 ± 9.3MPa and 44.3% ± 8.5%,
respectively.73 In a structural sense the ultimate
load and elongation is 1,725 ± 269N. Woo et ars
documented that for young specimens (22-35
years), the ultimate load is 2,160 ± 157N and
dependent on orientation of the knee prepara-
tion with respect to normal anatomy. The
STRAIN tensile failure properties of other human knee
FIGURE 11.5. Schematic drawing to illustrate the ligaments have also been documented. 90 The
micromechanical events in collagen and elastin fibers mechanism of failure in a bone-ligament-bone
during tensile deformation of a ligament. structure is variable. With advanced age 77 or

1nnl~---------------------------------,

MICROFAILURE
z
~ 500
~
oLL
FIGURE 11.6. Tensile response
of a ligament showing failure of
individual bundles of collagen
and complete failure of the o 1 2 3 4 5 6 7
structure with a "mop-end"
appearance. (Adapted from
Yahia et al84 and Haut. 212 ) ELONGATION, mm
236
immobilization,91 the mechanism of failure is by
avulsion of adjacent bone. Neumann et al 92 con-
ducted failure tests on human lumbar anterior
longitudinal ligaments (ALLs) from a young
age group showing tensile strength, tensile
modulus, and failure strain of 27.4 ± 5.9MPa,
759 ± 336 MPa, and 4.95% ± 1.51%, respec-
tively. During aging (21-79 years) the tensile
modulus of the ligament midsubstance
increases twofold, whereas that of the insertion
site decreases threefold. The tensile strength
over the same range of ages decreases approx-
imately twofold. 93 Age-related changes
observed for the ALL are lower than those
documented for the ligamentum flavum for
which a fivefold decrease is noted in tensile
modulus and failure stress with increasing age. 61
Since the composition of the ligament flavum is
primarily elastin while that of the anterior lon-
gitudinal ligament is primarily collagen, these
data may suggest differential age-related
changes in each fibrous component, and/or pos-
sibly a more generalized age-dependent change
in their organization within ligaments.
The tensile failure properties of the human
PI' are 29.1 ± 2.4MPa at 30.8% ± 3.1 % strain/3
53.9 ± 2.7MPa,74 or 39.9 ± 15.8MPa at 19% ±
8%.94 Johnson et al95 indicated minimal differ-
ences in the biomechanical properties of the
human PI' from two age groups. The values of
the ultimate tensile strength and failure strain,
respectively, were 64.7 ± 15MPa and 14% ± 6%
for the young group (29-50 years) and 53.6 ±
10 MPa and 15 % ± 5 % for an older group
(64-93 years). Blevins et al96 showed a weak but
significant negative correlation between the
modulus of the human PI' with age for tests at
l00%/s, but not at 10%/s. For specimens aged
34 ± 12 years the tensile strength and modulus
were 37.1 ± 11.8MPa and 310 ± 95 MPa, respec-
tively. Another study using central portions of
the human PI' from a young population (24.5 ±
4.4 years) indicate a tensile stress and failure
strain of 53.4 ± 7.2MPa and 15.1% ± 4.4%,
respectively.
Studies have addressed the influence of
strain rate on the tensile failure properties of
ligaments and tendons. Bone-ligament-bone
preparations fail more often in the ligament
substance, rather than by avulsion, as· the
R.c. Haut
loading rate increases.97,98 While the shape of
the stress-strain curve is not significantly
altered by strain rate, tensile strength and ulti-
mate strain are increased 20% to 30% over a
I,OOO-fold change in strain rate. 99 The strain-
rate sensitivity of tendons has been shown to
vary with age. 21 A recent study indicates that
the elastic modulus of bovine PI' may be under-
estimated by as much as 50% using quasi-
static data versus impact data. 1oo While the
tensile strength of ligaments varies slightly with
strain rate, failure strain does not appear
dependent. 101
Skin
Skin is the largest single organ in the body
(16% of body weight in an human adult). It
consists of the epidermis with its outer charac-
teristic surface contours, and the dermis, which
contains collagen, elastin, cells, blood and
lymph vessels, nerve ending, hair and hair folli-
cles, and glands together with their associated
ducts. All are embedded in the matrix of pro-
teoglycans and glycoproteins. The mechanical
and barrier functions of the epidermis stem
primarily from the stratum corneum, which is
an outer layer of horny keratinized cells. 1OO The
predominant components of the dermis are
collagen fibers in the matrix of proteoglycans.
Collagen accounts for 60% to 80% of the dry
weight of the skin depending on age, sex, and
site on the body.103 The collagen (primarily type
I, with lesser amounts of type III) appears as a
three-dimensional network of wavy or coiled
fibers. In the upper (papillary) layer of the
dermis collagen fibers are fine. 104 This layer is
mainly concerned with connecting the reticular
dermis to the epidermis. The deep, reticular
dermis contains densely packed fibers running
parallel to the surface of the skin,105,l06 with
some fibers running between the planes, pre-
sumably to prevent interplanar shearing. 107 The
fibers within the planes also appear to be ori-
ented in a preferred direction. lOB Skin is nor-
mally under an in vivo tension. This tension
varies from 0 to 20N/m depending on site,
direction, and body posture. 109 This concept was
originally investigated by Langer. 110 The lines
11. Biomechanics of Soft Tissue
drawn by Langer, referred to as "cleavage"
lines, are thought to parallel collagen fibers on
the surface of skin. 111- 1l3
Skin provides the outermost covering of the
body, and its strength plays a role in lacerative
trauma. Observations from accidental injuries,
as well as experiments with laboratory instru-
ments, indicate that skin fails more often in
a tensile manner than from a shear or cutting
action, even when struck by relatively sharp
metal edges or structuresY4 This tensile failure
mechanism plays a role in determining lacera-
tive resistance of skin to grazing or glancing
blows, such as when the head hits the roof
pillar 1l5 or windshield1l6 during an automotive
collision. Critical shear stresses have been com-
puted for laceration of skin.ll7 The severity of
lacerative trauma depends on the applied load,
the lacerative resistance of skin, and the geo-
metrical shape of the impacting surfaceY8
There exists a great degree of variability in
the properties of skin, depending on species,
age, exposure, hydration, obesity, disease, and
biologic differences between individuals. The
basic tensile response of skin is nonlinear stiff-
FIGURE 11.7. Microstructural events
in collagen fiber bundles during
tensile deformation of skin. Note the
recruitment of collagen along the
line of tensile stretch.
237
ening (Fig. 11.7). The first region displays a low
modulus response. Some investigators suggest
elastin is being deformed in this region. 66,1l9
Others suggest this response is due to a few
straightened collagen fibers bearing load. 120 The
primary role of elastin may also be to restore
collagen to its prestretched, crimped configura-
tion after tensile 10ading.121 The initial modulus
of skin is 0.1 to 2MPa. 122,123 Collagen fibers
are then sequentially straightened and bear
load. 105,124 Finally, collagen fibers become
aligned and the tensile response of skin
approaches that of tendon. 125
As expected from the anisotropy noticed in
skin under normal in vivo tension (as evidenced
by Langer's lines), there is a difference in
the response curves obtained from specimens
taken from different sites and different orien-
tations on the body.126.127 Test specimens whose
primary orientation parallel cleavage lines
recruit collagen fibers at lower levels of
strain. 108,128 Typical values of the tensile
modulus for normal human skin over the tibia
are 22 MPa along Langer's lines and 6MPa
perpendicular to these lines. 129 Skin over the
STRAIN, %
238 R.c. Haut

sternum is not directionally dependent, and
the tensile modulus varies from 20 to 80 MPa
from birth to 25 years. 130 Correspondingly over
the thigh the tensile modulus varies from 1
to 5MPa.
Statistically, lacerative facial injuries parallel
the Langer's lines. 118 The resistance of skin to
laceration across Langer's lines is greater than
that parallel to these lines. Lesions produced
when the axis of a skin wound is parallel
versus perpendicular to Langer's lines heal with
less scar tissueY1 The tensile strength of skin
has typical values in the range of 2.5 to 16
MPa. 132 It varies with site,133 is higher in the
main fiber direction,134 and is believed to
increase with age. 132,135 The tensile strength and
failure strain of skin for an average adult is 7.7
MPa and 78%, respectively.136 Both parameters
decrease with age (Fig. 11.8). The tensile
strength and failure strain of skin over the
sternum are approximately 20MPa and 40% to
70%, respectively.103 Over the thigh the tensile
strength and failure strain are 1 to 5 MPa and
40% to 70%, respectively. Studies have shown
3500
Male
43yrs
3000
Male
74yrs
2500
'in
c..
2000
ui
f/)
W derived interfibrillar crosslinks within bundles
D::
t-
1500
f/)
that the failure strain of rat skin varies with ori-
entation and age.137 While failure strains per-
pendicular to skin tension lines decrease with
animal age, parallel to these lines the strain at
failure increases with age. This parallels age-
related changes in the tensile failure strains of
collagen fibers. 21
The tensile strength of skin also depends on
the rate of elongation or strain. Vogel138 showed
that in rat dermis it increases with the logarithm
of strain rate. Gadd et al 114 showed that the
tensile strength and failure strain of aged
human facial skin increases from 7 to 14 MPa to
11 to 20MPa and 30% to 67% to 42% to 62%,
respectively, over three orders of strain rate.
Similar changes have been found in the sensi-
tivity of tensile strength with strain rate in
rats,137 but the failure strain was not found to be
dependent on rate of loading. Haut137 further
shows that the sensitivity of tensile strength to
strain rate decreases with age and correlates
with the content of matrix proteoglycans in
the skin. The results parallel a decrease in the
degree of stress relaxation with age and the
content of tissue proteoglycans.138 These results
are consistent with the notion that the hydrated
matrix plays an important role in the strain-
rate-sensitive responses of connective
tissues. 139
In diabetes mellitis there is an increased stiff-
ening of collagen-rich tissues, such as arteries,
skin, and joints. 140,141 Reihsner and Menzel 127
showed a directional dependent increase in the
stiffness and viscous responses of skin exposed
to glucose in vitro. They suggested these bio-
mechanical changes are due to excessive sugar-
of collagen.

1000
Vascular Tissues
500
Various clinical investigative teams associate
O+--.=-~--~~--~
ruptures or tears of major blood vessels with
death in 30% to 45% of automobile fatalities. 142
o 2.0 4.0 6.0 8.0
Crush injury during soft tissue trauma can also
STRAIN, % adversely affect blood supply and increase sus-
ceptibility of surrounding tissue to infection. 143
FIGURE 11.8. Tensile responses of human skin speci- Arteries are blood vessels with a great range
mens at various ages. (Adapted from Kenedi et al211 ) of diameters. The human proximal aorta, for
11. Biomechanics of Soft Tissue 239

example, has a diameter of approximately TENSION - LENGTH DIAGRAM

2.5 cm, while the small arteries-the HUMAN EXTERNAL ILIAC ARTERY

arterioles-are about 60!lm in diameter. The 160 TRYPSIN FRESH

arterial wall has three layers: the intima, the
media, and the adventitia. The innermost com-
ponent of the intima is a layer of endothelial
cells that offer little resistance to internal pres- e 120
~g
sure. The intima is separated from the media by
an internal elastic membrane composed of z
elastin. The media, which is largely responsible -
0
III
80

for the strength and elasticity of arteries, is Z

IJ
composed of collagen. The adventitia is a thin I-
layer of loose connective tissue also composed 4Q
of "collagen. The walls of veins are thinner, more FORMIC ACID
supple, and less elastic than those of arteries. . "

••~........ ".~": ':.

While most authors distinguish three layers in
the walls of veins, the layers are frequently
indistinct. The intima contains endothelial cells
and is bounded by a network of elastic fibers.
The media is much thinner than arteries and
consists mainly of circular smooth muscle fibers
separated by longitudinal collagen fibers. The
adventitia is usually much thicker than the
media and consists of loose connective tissue
with thick longitudinal collagen fibers in an
intricate network of elastin. In larger veins like
the inferior vena cava, portal, splenic, iliac, and
renal veins, the adventitia makes up the greater
part of the wall.
There exists a significant literature on vas-
cular mechanics and the mechanical responses
of blood vessels with correlations to the
microstructure of their primary constituents:
collagen, elastin, and smooth muscle cells.
Comprehensive reviews are given by Dobrinl44
and HayashU 45 The tensile mechanical
response of the arterial wall stiffens exponen-
tially with elongation similar to skin, ligament,
and tendon. 146,147 Krafka27 noted that the
tangent modulus of strips of aorta varied from
0.15 to 0.19MPa. He suggested that in the phys-
iologic range a loose network of elastin is
largely responsible. Roach and Burtonl48
attempted to separate the contributions of
elastin and collagen in the human iliac artery
using crude trypsin to degrade the elastin, and
formic acid to degrade collagen (Fig. 11.9). They
conclude that elastin fibers primarily bear cir-
cumferentialload at small distentions and col-
lagen fibers bear circumferential load at large
., ,-' •,., .,='::"'-:"-.'..,..
120 140 160 80
" INIT. CIRCUMFERENCE
FIGURE 11.9. Tensile response of human iliac artery
after removal of collagen with formic acid and elastin
with trypsin. (From Roach and Burton. 148)
distentions. These descriptions of the correla-
tion between mechanical properties and ultra-
structure are consistent with histologic studies
of the artery under pressure. 149 They have
shown that under diastolic pressure collagen
fibers show no definite pattern or orientation.
Above diastolic pressures elastic lamellae
appear straight and collagen fibers are circum-
ferentially arranged. They conclude at physio-
logic pressures the aortic media functions as a
two-phase material. At 100mmHg the tangent
modulus of the thoracic aorta is 0.4 to 0.8
MPa. 150,151 At 240mmHg the tangent modulus
varies from 1.2 to 1.6MPa. These data can be
compared with the modulus of elastin26,28
(0.3--O.9MPa) and that of collagen 400 to 600
MPa.8,11
The ratio of elastin to collagen in the aortic
wall decreases away from the heart, until in the
abdominal aorta more collagen exists than
elastin. 152 The corresponding tensile responses
of circumferential and longitudinal specimens
change down the aortic tree. 153 The more distal
and smaller arteries also are shown to relax
more and at faster rates than larger arteries,
reflecting a change in viscoelastic properties
down the aortic tree. While no direct correla-
240 R.c. Raut

tions have been established between the
passive stress-strain properties of arteries and
the ratio of collagen to elastin,154,155 attempts
have been made to describe differences in the
tensile wall mechanics of various vessels with
the following simplified equation: E = WeEe +
!c WeEe, where Ee and Ee are the elastic modulus
of elastin and collagen fibers, respectively, and
We and We represent the fractional content of
these two components. The term!c was included
to reflect differences in the recruitment of col-
lagen fibers between arteries. 154 Demiray156 for-
mulated a more sophisticated mathematical
model that incorporates the elastic properties
of elastin and the viscoelastic properties of col-
lagen. Smooth muscle is included as a viscous
element in other physical models of the
aorta. 157,158
The circumferential tension-elongation
response of the human iliac artery stiffens with
increasing age/ 59 probably due to an increase in
the ratio of collagen to elastin. l44 The longitu-
dinal tensile response also shifts with aging,
reflecting less influence of elastin fibers (Fig.
11.10). The tensile modulus of the human iliac
artery at 30 years of age varies from 0.01 MPa
at zero stretch to 0.7MPa prior to failure. At
100mmHg the tensile modulus is 0.5 MPa,
and the corresponding longitudinal modulus
is approximately 1.7 MPa. These modulii are
increased by factors of 2 to 5 at 80 years of age.
Fewer experimental data exist on the
mechanical properties of veins. The percentage
of collagen is typically greater in veins than
arteries, while the percentage of elastin is less. l60
Comparative tests of pulmonary arteries and
veins indicate that arteries are more compliant
than veins. The mechanical behavior of veins in
the longitudinal direction can be regarded as
essentially elastic, while that in the circumfer-
ential direction is highly viscoelastic. 161 For
veins the tensile response curves shift toward
the stress axis with increasing age,l60 like those
for arteries. 154 Mackay et al l60 state that age-
related changes in both arteries and veins are
largely due to alterations in elastin at the
molecular and lamellar levels.
The tensile failure properties of vascular
tissue have important implications in traumatic
injury to the body. The thoracic aorta is the
single most significant site of serious vascular
injury.162 Transverse tears of the descending
aorta at the isthmus just distal to the left sub-
clavian artery represent a major site of aortic

NO IN GROUP 5 32 31
AGE GROUPS 80-100 60- 80 40-60

jj 160
en
en
u

..
>
I
I
0

% 120 3
l- ID- 20
'"z
'"
..J

::I
<J
.... 80
en
::I
'"
..J

•
..J

~
40
5 - -
FIGURE 11.10. Tension curves for
the human iliac artery showing the
0
0 20 40 60 80 100 ~
effect of aging. (From Roach and
PERCENT INCRE ASE IN CIRCUMFERENCE Burton. 159)
11. Biomechanics of Soft Tissue
injury. Dissecting aneurysms are an important
cause of morbidity and mortality associated
with motor vehicle accidents.163 Dissections
only occur at very high (nonphysiologic) pres-
sures (596 ± 214mmHg). Age has no effect on
strength of the media, but sex, location, and
presence of an atherosclerotic plaque do seem
to playa significant role. While the mechanisms
of aortic rupture are still being debated, both
longitudinal and circumferential failure prop-
erties appear implicated. l64 Collagen is the
primary strength-bearing component of the
aorta. 165 The circumferential strength of
the human ascending, thoracic, and abdominal
aorta averages 1.1, 0.9, and 1.1 MPa, respec-
tively, across all age groups.136 The correspond-
ing longitudinal tensile strengths average 0.7,
0.8, and 0.8MPa, respectively. Strengths in both
directions decrease with age. The circumferen-
tial failure strains are 77%, 71%, and 81%,
respectively, and the corresponding longitudi-
nal failure strains are 81%, 56%, and 69%,
respectively. More recent experiments on
dumbbell-shaped specimens from the human
aorta indicate that the longitudinal tensile
strength in low-speed experiments varies from
approximately 2.7MPa in the young down to
0.8 MPa in older tissues. l64 The circumferential
strengths are slightly higher, but decrease simi-
larly with age. The corresponding failure strains
also decrease with age from approximately
179% in young to 129% in aged tissues. Under
dynamic strain rates the tensile strength of
human thoracic aorta increases, but failure
strain does not change with alterations in strain
rate.
Questions of the dynamic versus static
strength of veins has received attention. Acute
subdural hematoma occurs in approximately
30% of the severely head-injured. 166 The toler-
ance curve for subdural hematoma has been
interpreted in terms of the sensitivity of cere-
bral bridging veins to strain rate. 167 In one early
study, the ultimate strain for these veins signifi-
cantly decreased with strain rate. 168 More
recent experiments, however, indicate that
while the tensile strength of human subdural
bridging veins slightly increases over three
orders of magnitude change in strain rate, the
ultimate stretch ratio is not altered. 169 This is in
241
line with work on human thoracic aorta,164 and
the common carotid artery and jugular vein of
the ferret. 17o
Recent studies have examined the mechani-
cal properties of diseased blood vessels. The
data on atherosclerosis and arteriosclerosis are
often conflicting and inconclusive. One study
shows a stiffening of the aorta and a loss of
strength under hyperlipidemic conditions (Fig.
11.11).171 Hypertension, on the other hand, gen-
erally results in a stiffened artery due to a thick-
ened wall and an increase in its elastic modulus.
The distensibility of small pulmonary blood
vessels is decreased in heart failure patients. 172
Cigarette smoking increases the stiffness of pul-
monary arteries in rats.173 This is thought largely
due to an increase in the volume fractions of
collagen and elastin, and a decrease in the
volume fraction of smooth muscle cells in
smokers' arteries.
Articular Cartilage
Articular cartilage is a connective tissue that
lines the contacting surfaces of bones and
therefore serves as the bearing material in syn-
ovial joints, such as the knee, hip, and shoulder.
To perform the dual functions of load trans-
mission and lubrication of joints, the microar-
chitecture of articular cartilage is unique. It is
composed of 70% to 80% fluid and a solid
organic matrix of collagen, proteoglycans, gly-
coproteins, and lipids. The tissue is aneural and
avascular, and has few cells. Although there is
some degree of disagreement on the arrange-
ment of collagen in articular .cartilage,174.175 a
simplified view has been given.176 Close to the
surface collagen fibrils run parallel to the
surface.177 Below the superficial zone, the fibril
alignment becomes progressively more oblique
to the articular surface down to the deep zone,
where collagen fibers are aligned approxi-
mately perpendicular to the cartilage surface
and the subchondral plate of bone (Fig. 11.12).
Because of its propensity for water, the matrix
of proteoglycans plays a major role in deter-
mining the compressive properties of cartilage.
The rigidity and compliance of articular carti-
lage is due to osmotic swelling of the proteo-
242
STRAIN, %
FIGURE 11.12. A scanning electron micrograph of
articular cartilage showing the arrangement of colla-
gen fibers. (From Kaab et al 179)
glycans against tensile constraint by a network
of type II collagen. The swelling pressure of
"normal" articular cartilage is approximately
0.35 MPa. 178 When stress is applied to articular
cartilage, there is an instantaneous deformation
that changes the shape of the collagen and pro-
R.c. Haut
FIGURE 11.11. A schematic repre-
senting the effect of a hyperlipi-
demic diet on the circumferential
tensile response of the canine aorta.
(Based on data given in Haut et
al171 )
teoglycan networksp9 The instantaneous defor-
mation of this soft tissue is strongly anisotropic
and dependent on collagen.180.l8l The proteo-
glycans secondarily influence the instantaneous
response by providing tension in the col-
lagenous network. At the same time fluid within
the articular cartilage begins to flow out of the
tissue. 182 The time-dependent response of artic-
ular cartilage is largely defined by fluid flow.
The intrinsic modulus of articular cartilage is
dependent on the properties of the solid phase.
The maintenance of tissue hydration under
load has been described in terms of a balance
between the osmotic pressure of the proteogly-
cans, tension in the collagen network, and the
applied stress. 178,183
The functional or biomechanical properties
of articular cartilage are known to significantly
depend on exercise, age, and pathology. Immo-
bilization of a joint results in a significant but
reversible loss of proteoglycans and an increase
in tissue water. 184,185 Immobilization thereby
causes an increase in the rate of creep, a
decrease in long-term equilibrium modulus,
and an increase in the permeability of joint car-
tilage. 186 These changes parallel those observed
in osteoarthritis (OAY87 and closely parallel
11. Biomechanics of Soft Tissue 243

those documented in aging. 188 Aging, however,
has been attributed to alterations in density and
microstructure of collagen, which is distinct
from the "unwinding," fibrillation, or loss of
collagen crosslinking associated with OA. 189 In
general, age-related changes and other nonpro-
gressive degenerative changes of articular car-
tilage are less severe than changes due to OA.
In this disease a softened articular cartilage
becomes invaded by cells and vessels from the
underlying subchondral bone; fraying of the
cartilage surface is observed; surface fissures
penetrate the tissue; and the soft tissue layer is
lost and underlying bone sclerosis prevails. The
radiographic presence of bone spurs, which
limit joint motion, is one major clinical sign of
joint degeneration, along with joint pain,
swelling, etc. 190,191
While the onset of degenerative joint disease
is not well understood, severe mechanical insult
has been suggested to initiate disease. While a
single severe insult has been implicated in a
posttraumatic OA,192 repeated low-level
stresses have also shown similar degenerative
changes in joints. 193 Experimental investiga-
tions of impact-induced injury to articular car-
tilage are few. In vitro impact on human
cartilage/bone samples can produce radial fis-
water without signs of surface damage (Fig.
11.13).197 These parallel some of the early his-
tologic signs in the human disease process.
The function of articular cartilage and its
response under impact loading depend on its
tensile properties. In planes parallel to the
surface the tensile mechanical properties of
cartilage vary with depth and orientation. 198 In
concert with the morphology of collagen, the
tensile response of surface layers of the tissue
is consistently stiffer and stronger than those of
underlying layers. Tensile failure stress corre-
lates positively with the content of collagen, but
not with the content of proteoglycans. 198 Tensile
specimens oriented parallel to the preferred
directions of collagen (split or Hultkrantz lines)
are stiffer and stronger than those oriented per-
pendicular to these lines. The tensile strength
and modulus of the superficial zone increases
PrOI._"'''.n~

sures on the surface that extend into the deep

zone and cause death of chondrocytes at
contact pressures exceeding 25 MPa, corre-
sponding to a compressive strain of 25 % .194
These surface fissures orient on the surface
parallel to the preferred directions of collagen.
Repeated impacts to bovine cartilage-on-bone
specimens with 2 to 12 joules of energy result
in microstructural changes in collagen fibrils
resembling early OA. 195 Impact-induced fis-
sures of cartilage in vitro appear oriented 45
degrees to the articular surface and can extend
to the intermediate zone of the tissue. Severe
blunt impact to the patellofemoral joint can
lead to separation of the cartilage from under-
lying bone and disruption of the collagen ultra-
structure without gross visual damage to the FIGURE 11.13. A schematic of microstructural events
tissue. l96 Subfracture loads on articular carti- in articular cartilage during blunt trauma. Note the
lage of the patellofemoral joint in vivo can lead damage to collagen fibrils and the cleavage of pro-
to changes in the zone of calcified cartilage, an teoglycans, which together allow the tissue to swell
increase in cellular clones, vascular invasion, with fluid and soften posttrauma. (From Donohue
loss of proteoglycans, and an increase in tissue et al l97 )
244
with age to a maximum of approximately
40 MPa and 220 MPa, respectively, in the third
decade, decreasing to 12MPa and 60MPa at 90
years of age. 199,200 Similar results have been
reported for bovine tissue,zO! Studies on bovine
articular cartilage indicate that proteoglycans
act to retard reorganization and alignment of
collagen fibers under tensile load, thereby pro-
tecting the collagenous network from a sudden
extension,zo2 The intrinsic tensile modulus of
human articular cartilage is typically less than
30MPa,z03 Tissues from low-weight-bearing
areas are stiffer than those from high-
weight-bearing areas, correlating with the ratio
of collagen to proteoglycan. Osteoarthritic car-
tilage, showing surface fibrillation (fissuring),
has a tensile stiffness consistently less than
2MPa. This is correlated with damage in the
network of collagen.
Newberry et a1 204 recently conducted
blunt impact experiments on the rabbit
patellofemoral joint and determined impact
stresses in cartilage and underlying bone. A
threshold stress was suggested for acute injury
and chronic changes in bone and cartilage.
Blunt insult that causes surface lesions on
retropatellar cartilage results in statistical soft-
ening of the tissue 1 year posttrauma. 205 Statis-
tical softening of impacted cartilage occurs at 3
months with regular exercise of the anima1. 204
Softening of the impacted cartilage was sug-
gested due to damage of the collagen, as evi-
denced by surface lesions and a loss of tissue
proteoglycans postinsult (Fig. 11.14). Atkinson
et a1 206 suggest that shear stresses produced in
cartilage by blunt insult to a joint are statisti-
cally a better predictor of surface injury than
TABLE 11.1. Some tensile strengths and associated biochemical data, based on percentage of weight, for
representative soft connective tissues.
Collagen
Tissue Strength (MPa) (% of fat free dry weight)
Aorta 0,7-1.0136 23-35
Cartilage 5-40197 60-65
Skin 2-16133 65-70
Ligament 13_3877 75-80
Tendon 3079_55 74 75-80
Biochemical data from Woo et a1. 209
RC. Haut
compressive or tensile stresses. A 50% proba-
bility of injury was predicted at approximately
5 MPa. Tensile stress was a better predictor as
the content of tissue fluid is increased in a
biphasic model of the cartilage. 207 These data
suggest that pathologic cartilage is more sus-
ceptible to blunt impact injury than normal car-
tilage. This supports other studies that suggest
that the time interval between joint injury and
the development of osteoarthritis is signifi-
cantly shorter in older people. 208
Summary
Structural integrity of soft connective tissues is
essential for the support and protection of the
skeleton and major organs of the body. Impact
loads can traumatize and damage these tissues,
leading to disfigurement and/or dysfunction of
a major organ or joint. We have seen in this
chapter that the mechanical properties of soft
tissues are dependent on the concentration and
arrangement of their constituent elements:
namely, the fibrous proteins collagen and
elastin and the hydrated matrix of proteogly-
cans. Numerous studies have shown that the
strength-bearing properties of connective
tissues are associated largely with collagen.
Indeed, a correlation seems evident between
the content of collagen in a tissue and its tensile
strength (Table 11.1). Yet we have seen that
tissue strength per se can vary widely depend-
ing on the complex organization, physical prop-
erties, and concentration of collagen. These
data can also be widely divergent due to exper-
imental procedures, species, etc. We have seen
Elastin
Glycosaminoglycans (GAGs)
40-50 2-2.5
Trace 10-15
5-10 1.5-2
<5 2.5-3
<3 1-1.5
11. Biomechanics of Soft Tissue 245

FIGURE 11.14. Histologic sec-

tions of articular cartilage
showing chronic damage to its
surface 1-year postinsult and
thickening of the underlying
subchondral bone, compared to
a control specimen shown in the
lower slide. (From Newberry
et af04)

that the physical strength of soft connective
tissues generally decreases with age and pathol-
ogy, and likely reflects changes in the mechani-
cal properties of collagen and its interaction
with elastin and matrix proteoglycans.
The role played by the matrix of proteogly-
cans is still not well defined, except possibly for
cartilage. Recent studies suggest that by con-
trolling tissue hydration the matrix may help
define the physical properties of soft tissue in
high-speed impacts.
Another area of current and future research
deals with the biologic functions of modeling
and remodeling of soft connective tissues after
injury. What are the mechanisms by which cells
synthesize specific extracellular constituents to
help heal soft connective tissues after injury?
While some of these data are evolving in the
current literature, this field is in its infancy.
Because of the multidisciplinary nature of these
questions, we need the cooperation of physical,
biologic, and clinical scientists.
246
Acknowledgments. The author would like to
acknowledge the help of Ms. Patti Wilkins and
Ms. Ann Marie Cook in the preparation of this
manuscript.
References
1. Scott 1. Molecules that keep you in shape. New
Sci 1986;24:49-53.
2. Nordin M, Frankel VH. Biomechanics of col-
lagenous tissues. In: Basic biomechanics of the
Skeletal system. Lea and Febiger, Philadelphia,
pp. 87-110, 1980.
3. Nimni ME, Harkness RD. Molecular structure
and functions of collagen. In: Nimni M, ed. Col-
lagen. CRC Press, Cleveland, Ohio, pp. 3-35,
1988.
4. Diamant J, Keller A, Baer E, Litt M, Arridge
RGC. Collagen: ultrastructure and its relation
to mechanical properties as a function of
aging. Proc R Soc Lond [Bioi] 1972;180:293-
315.
5. Ramachandran GN. Treatise on collagen.
In: Ramachandran GN, ed. Chemistry of colla-
gen. Academic Press, New York, pp. 103,
1967.
6. Miller E1. Collagen chemistry. In: Piez KA,
Reedi AH, eds. Extracellular matrix biochem-
istry. Elsevier, New York, pp. 41-81,1984.
7. Vogel HB. Influence of maturation and age on
mechanical and biochemical parameters of
connective tissue of various organs in the rat.
Connect Tissue Res 1978;6:83-94.
8. Haut RC. The effect of a lathyritic diet on the
sensitivity of tendon to strain rate. J Biomech
Eng 1985;107:166-174.
9. Vogel HG. Collagen and mechanical strength in
various organs of rats treated with D-penicil-
lamine or aminoacetonitrile. Connect Tissue
Res 1975;3:237-244.
10. Betsch DF, Baer E. Structure and mechanical
properties of rat tail tendon. Biorheology 1980;
17:83-94.
11. Rigby B, Hirai N, Spikes J, Eryring H. The
mechanical properties of rat tail tendon. J Gen
Physiol 1959;43:265-283.
12. Viidik A. Simultaneous mechanical and light
microscopic studies of collagen fibers. Z Anat
Entugesch 1972;136:204-212.
13. Hooley CJ, Cohen RE. A model for the creep
behavior of tendon. Int J Bioi Macromol 1979;
1:123-132.
R.c. Haut
14. Kastelic J, Palley I, Baer E. A structural
mechanical model for tendon crimping. J
Biomech 1980;13:887-893.
15. Torp S, Arridge RC, Armendiades CD, Baer E.
Structure property relationships in tendon as a
function of age. In: Proceedings of the 1974
Colston Conference, Department of Physics
University of Bristol, u.K. pp. 197-221, 1974.
16. Haut RC. The influence of specimen length in
the tensile failure properties of tendon colla-
gen. J Biomech 1986;19:951-955.
17. Sasaki N, Odajima S. Elongation mechanism of
collagen fibrils and force-strain relations of
tendon at each level of structural hierarchy.
J Biomech 1996;29(9):1131-1135.
18. Kastelic J, Baer E. Deformation in tendon col-
lagen. In: Vincent JFV, Currey JD, eds. The
mechanical properties of biological material.
Cambridge, pp. 397-435, 1980.
19. Yannas IV, Huang C. Fracture of tendon colla-
gen. J Poly Sci 1972;1O(part A-2):577-584.
20. Parkinson J, Brass A, Canova G, Brechet Y. The
mechanical properties of simulated collagen
fibrils. J Biomech 1997;30(6):599-554.
21. Haut RC. Age dependent influence of strain
rate on the tensile failure of rat-tail tendon.
ASME J Biomech Eng 1983;105:296-299.
22. Bailey AJ, Etherington D1. Metabolism of col-
lagen and elastin. In: Florkin M, Neuberger A,
Van Doren LLM, eds. Comprehension bio-
chemistry, vol 19B. Elsevier-North Holland,
Amsterdam, pp. 299-460, 1980.
23. Gray WR, Sandberg LB, Foster JA. Molecular
model of elastin structure and function. Nature
1973;246:461-466.
24. Vesely 1. The role of elastin in aortic valve
mechanics. J Biomech 1998;31:115-123.
25. Jenkins R, Little RW. A constitutive equation
for parallel-fibred elastic tissue. J Biomech
1974;7:397-402.
26. Hoeve CAJ, Flory P1. The elastic properties of
elastin. J Am Chern Soc 1958;80:6523-6526.
27. Krafka 1. Comparative study of the histo-
physics of the aorta. Am J PhysioI1939;125(1):
1-14.
28. Carton RW, Dainauskas J, Clark Jw. Elastic
properties of elastic fibers. J Appl Physiol
1962;17:547-551.
29. Hass GM. Elasticity and tensile strength of
elastic tissue isolated from the human aorta.
Arch PathoI1942;34:971-981.
30. Minns RS, Steven FS. The tensile properties of
developing fetal elastic tissue. J Biomech 1976;
9:9-11.
11. Biomechanics of Soft Tissue
31. Rosenberg LC Proteoglycans. In: Owen R,
Goodfellow J, Bullough P, eds. Scientific Foun-
dations of orthopaedics and traumatology. WB
Saunders, Philadelphia, pp. 36-42, 1980.
32. Lanir Y. Biorheology and fluid flux in swelling
tissues. I. Biocomponent theory for small
deformations, including concentration effects.
Biorheology 1987;24:173-187.
33. Parry DAD, Craig AS. Growth and develop-
ment of collagen fibrils in connective tissue. In:
Ruggeri A, Motta PM, eds. Ultrastructure of the
connective tissue matrix. Martinus Nijhoff,
Boston, pp. 34-64, 1984.
34. Wood GC The formation of fibrils from colla-
gen solutions. Effect of chondroitin sulphate
and some other naturally occurring polyanions
on the rate of formation. Biochem J 1960;75:
605--612.
35. Wood GC The precipitation of collagen fibrils
from solution. Int Rev Connect Tissue Res
1964;2:1-31.
36. Scott JE, Orford CR, Hughes EW. Proteogly-
can-collagen arrangements in developing rat
tail tendon. An electron-microscopical and bio-
chemical investigation. Biochem J 1981;195:
573-581.
37. Partington FR, Wood GC The role of non-
collagen components in the mechanical behav-
ior of tendon fibres. Biochim Biophys Acta
1963;69:485-495.
38. Myers DB, Highton TC, Rayns DG. Ruthenium
red-positive filaments interconnecting collagen
fibrils. J Ultrastruct Res 1973;42:87-92.
39. Kronick PL, Sacks MS. Matrix macromolecules
that affect the viscoelasticity of calfskin. J
Biomech Eng 1994;116(2):140-145.
40. Parry DAD, Barnes GRG, Craig AS. A
comparison of the size distribution of
collagen fibrils in connective tissues as a func-
tion of age and a possible relation between
fibril size distribution and mechanical proper-
ties. Proc R Soc Lond [BioI] 1978;203:305-
321.
41. Li JT, Armstrong CG, Mow VC The effect of
strain rate on mechanical properties of articu-
lar cartilage in tension. ASME Biomech Symp
1983;56:117-120.
42. Minns RJ, Soden PD, Jackson DS. The role of
the fibrous components and ground substance
in the mechanical properties of biological
tissues: a preliminary investigation. J Biomech
1973;6:153-165.
43. Armstrong CG, Mow VC, Lai WM, Rosenberg
LC Biorheological properties of proteoglycan
247
macromolecules. 27th Meeting of the Orthope-
dic Residents Society, Las Vegas, Nevada,
1981.
44. Zhu W, Iatridies JC, Hlibizuk V, Ratcliffe A,
Mow VC Determination of collagen-proteo-
glycon interactions in vitro. J Biomech 1996;
29(6):773-783.
45. Zhu W, Mow VC A nonlinear viscoelastic con-
stitutive equation for the flow behaviors of con-
centrated proteoglycan solutions. ASME
Biomech Symp 1991;AMD-120:247-250.
46. Mason P. Viscoelasticity and structure of
keratin and collagen. Kolloid Z 1965;202:139-
147.
47. Barenberg SA, Filisko FE, Geil PH. Ultrastruc-
tural deformation of collagen. Connect Tissue
Res 1978;6:25-35.
48. Haut RC, DeCou JM. The effect of enzymatic
removal of glycosaminoglycans on the strength
of tendon. ASME Adv Bioeng p. 48, 1984.
49. Lanir Y. Constitutive equations for fibrous con-
nective tissues. J Biomech 1983;16(1):1-22.
50. Hurschler C, Loitz-Ramage B, Vanderby R. A
structurally based stress-stretch relationship for
tendon and ligament. J Biomech Eng
1997;119:392-399.
51. Chen C, McCabe R, Vanderby R. Tho electro-
kinetic phenomena in rabbit patellar tendon:
pressure and voltage. Proceedings of the ASME
Bioengineering Conference, Beaver Creek, CO,
pp. 31-32,1995.
52. Lanir Y, Salond EL, Fona A. Physico-chemical
and microstructural changes in collagen fiber
bundles following stretch in vitro. J Biorheol
1988;25(4):591--604.
53. Hannafin JA, Arnoczky SP. Effect of cyclic and
static tensile loading on the water content and
solute diffusion in canine flexor tendons; an in
vitro study. J Orthop Res 1994;12:350-356.
54. Thielke RJ, Vanderby R, Grood ES. Volumetric
changes in ligaments under tension. Proceed-
ings of the AS ME Bioengineering Conference,
Breckenridge, CO, pp. 197-198, 1995.
55. Wilson AN, Frank CB, Shrive NG. The behav-
ior of water in rabbit medial collateral liga-
ment. In: Blankavoort L, Kooloos JGM, eds.
Proceedings of the 2nd World Congress of Bio-
mechanics. Stichting World Biomechanics,
Nijmegen, Amsterdam, The Netherlands, p.
226b,1994.
56. Atkinson TS, Haut RC, Altiero NJ. A poroelas-
tic model that predicts some phenomenological
responses of ligaments and tendons. J Biomech
Eng 1997;119(4):400-405.
248
57. Chimich DD, Shrive NG, Frank CB, Marcheck
L, Bray Be. Water content alters viscoeleastic
behavior of the normal adolescent rabbit
medial collateral ligament. 1 Biomech 1992;
25(8):831-837.
58. Haut TL, Haut Re. The state of tissue hydra-
tion determines the strain-rate-sensitive stiff-
ness of human patellar tendon. 1 Biomech 1997;
30(1 ):79-81.
59. Amiel D, Frank CB, Harwood FL, Fronek 1,
Akeson WHo Tendons and ligaments: a mor-
phological and biochemical comparison. 1
Orthop Res 1984;1(3):257.
60. Yahia LH, Garzon S, Strykowski H, Rivard CH.
Ultrastructure of the human interspinous liga-
ment and ligamentum flava. A preliminary
study. Spine 1990;15(4):262-268.
61. Nachemson AL, Evans IH. Some mechanical
properties of the third human lumbar inter-
laminar ligament. 1 Biomech 1968;1:211-220.
62. Amiel D, Billings E, Akeson WHo Ligament
structure, chemistry, physiology. In: Daniel D,
Akeson WH, O'Corner 11, eds. Knee ligament:
structure, function, injury and repair. Raven
Press, New York, pp. 77-91, 1990.
63. Woo SL-Y, Gomez MA, Amiel D, Ritter MA,
Gelberman RH, Akeson WHo The effects of
exercise on the biomechanical and biochemical
properties of swine digital flexor tendons.
ASME 1 Biomech Eng 1981;103:51-56.
64. Zernicke RF, Butler DL, Grood ES, Hefzy MS.
Strain topography in human tendons and fascia.
ASME J Biomech Eng 1984;106:177-180.
65. Stouffer DC, Butler DL, Hosny D. The rela-
tionship between crimp pattern and mechanical
response of human patellar tendon-bone. 1
Biomech Eng 1985;107:158-165.
66. Lanir Y. A structural theory for the homoge-
neous biaxial stress-strain relationship in flat
collagenous tissues. 1 Biomech 1979;12:423-
436.
67. Comninou M, Yannas IV Dependence of
stress-strain nonlinearity of connective tissues
on the geometry of collagen fibres. 1 Biomech
1976;9:427-433.
68. Markenscoff X, Yannas IV On the stress
strain relation for skin. 1 Biomech 1979;12:127-
129.
69. Kwan MK, Woo SL-y' A structural model to
describe the nonlinear stress-strain behavior
for parallel fibered collagenous tissues. 1
Biomech Eng 1989;111:361-363.
70. Lanir Y. Structure-strength relations for mam-
malian tendon. Biophys 11978;24:541-554.
Re. Haut
71. Decraemer WF, Maes MA, Van Huyse Vl, Van
Peperstraete P. A nonlinear viscoelastic consti-
tutive equation for soft biological tissues based
upon a structural model. 1 Biomech 1980;
13:559-564.
72. Belkoff SM, Haut Re. A microstructural model
used to study the effect of gamma irradiation
on tendon allografts. Proceedings of the Com-
bined Meeting of the Orthopaedic Research
Societies of USA, lapan, and Canada, 1991.
73. Haut RC, Powlison Ae. The effects of test envi-
ronment and cyclic stretching on the failure
properties of human patellar tendons. 1 Orthop
Res 1990;8(4):532-540.
74. Butler DL, Grood ES, Noyes FR Biomechan-
ics of ligaments and tendons. Exerc Sport Sci
Rev 1978;6:125-181.
75. Hubbard RP, Soutas-Little RW. Mechanical
properties of human tendon and their age
dependence. 1 Biomech Eng 1984;106:144-150.
76. Pintar FA, Yoganandon N, Myers T, Elhagediab
A, Sances A. Biomechanical properties of
human lumbar spine ligaments. 1 Biomech
1992;25(11):1351-1356.
77. Noyes FR, Grood ES. The strength of the ante-
rior cruciate ligament in humans and rhesus
monkey. Age-related and species-related
changes. 1 Bone 10int Surg 1976;58A:1074-
1082.
78. Woo SL-Y, Hollis 1M, Adams Dl, Lyons RM,
Takai S. Tensile properties of the human
femur-anterior cruciate ligamenttibia complex:
the effects of specimen age and orientation. Am
1 Sports Med 1991;19(3):217-225.
79. Haut RC, Powlison AC, Rutherford GW,
Kateley lR Some effects of donor age and sex
on the mechanical properties of patellar tendon
graft tissues. ASME Adv Bioeng 1988;8:75-
78.
80. Haut RC, Lancaster RL, DeCamp CEo
Mechanical properties of the canine patellar
tendon: some correlations with age and the
content of collagen. 1 Biomech 1991;27(8):
1105-1108.
81. Kuiper SD, Amiel D, Harwood FL, et al. Age
related properties of the medial collateral
ligament and anterior cruciate ligament. A
morphological and biochemical analysis. Trans
Orthop Res Soc 1990;15:523.
82. Woo SL-Y, Gomez MA, Woo YK, Akeson WHo
Mechanical properties of tendons and liga-
ments II. The relationship of immobilization
and exercise on tissue remodeling. Biorheology
1982;19:397-408.
11. Biomechanics of Soft Tissue
83. Butler DL, Noyes FR, Walz KA, Gibbons MI
Biomechanics of human knee ligament allo-
graft treatment. Transactions of the 33rd
meeting of the Orthopedics Residents Society,
p. 128, 1987.
84. Yahia LH, Brunet J, Labelle S, Rivard CH. A
scanning electron microscopic study of rabbit
ligaments under strain. Matrix 1990;10:58-64.
85. Panjabi MM, Joldos E, Oxland TR, Crisco 11.
Subfailure injury of the rabbit anterior cruciate
ligament. J Orthop Res 1996;14:216-222.
86. Kwan MK, Woo SL. A structural model to
describe the nonlinear stress-strain behavior of
parallel-fibered collagenous tissues. J Biomech
Eng 1989;11:361-363.
87. Liao H, Belkoff SM. A failure model for liga-
ments. J Biomech 1999;32:183-188.
88. Yahia LH, Drouin G. Microscopical investiga-
tion of canine anterior cruciate ligament and
patellar tendon: collagen fascicle morphology
and architecture. J Orthop Res 1989;7(2):
243-251.
89. Wren TAL, Carter DR. A microstructural
model for the tensile constitutive and failure
behavior of soft skeletal connective tissues.
J Biomech Eng 1998;120:55-61.
90. Kennedy JC, Hawkins RJ, Willis RB, Darylchuk
KD, et al. Tension studies of human knee liga-
ments. J Bone Joint Surg 1976;58A(3):350-355.
91. Noyes FR. Functional properties of knee
ligaments and alterations induced by immobi-
lization. A correlative biomechanical and histo-
logical study in primates. Clin Orthop 1977;
123:210-242.
92. Neumann P, Keller TS, Ekstrom L, Perry L,
Hansson TH, Spengler DM. Mechanical
properties of the human lumbar anterior longi-
tudinalligament. J Biomech 1992;25(10):1185-
1194.
93. Neumann P, Ekstrom LA, Keller TS, Perry L,
Hansson TH. Aging, vertebral density, and
disc degeneration alter the tensile stress-
strain characteristics of the human anterior
longitudinal ligament. J Orthop Res 1994;12:
103-112.
94. Paulos LE, France EP, et al. Comparative mate-
rial properties of allograft tissues for ligament
replacement: effects of type, age, sterilization
and preservation. 33rd meeting of the
Orthopaedic Research Society, p. 129, 1987.
95. Johnson GA, Tramaglini DM, Levine KE, Ohno
K, Choi N-Y, Woo SL-y' Tensile and viscoelas-
tic properties of human patellar tendon. J
Orthop Res 1994;12:796-803.
249
96. Blevins FT, Hecker AT, Bigler GT, Boland AL,
Hayes We. The effects of donor age and strain
rate on the biomechanical properties of bone-
patellar tendon-bone allografts. Am J Sports
Med 1994;22(3):328-333.
97. Noyes FR, De Lucas JL, Torvik PI Bio-
mechanics of anterior cruciate ligament failure:
an analysis of strain rate sensitivity and mech-
anisms of failure in primates. J Bone Joint Surg
1974;56A(2):236-253.
98. Crowninshield RH, Pope MH. The strength
and failure characteristics of the rat medial
collateral ligament. J Trauma 1976;16(2):99-
105.
99. Peterson RH, Woo SL-y' A new methodology
to determine the mechanical properties of liga-
ments at high strain rates. J Biomech Eng
1986;108:365-367.
100. Crisco 11, Dunn TC, McGovern RD. Stress wave
velocities in bovine patellar tendon. J Biomech
Eng 1998;120:321-326.
101. France EP, Paulos L, Abbott P, Roberts P, et al.
Failure characteristics of the medial collateral
ligament of the knee: effects of high strain rate.
Aviat Space Environ Med 1987;58:488.
102. Wilkes GL, Nguyen A, Wildnauer R. Structure-
property relations of human and neonatal rat
stratum corneum-I. Thermal stability of the
crystalline lipid structure as studied by x-ray
diffraction and differential thermal analysis.
Biophys Acta 1973;304:267-275.
103. Hult AM, Goltz RW. The measurement of
elastin in human skin and its quantity in rela-
tion to age. J Invest Dermatol 1965;44:408-
412.
104. Brown IA. A scanning electron microscope
study of the effects of uniaxial tension on
human skin. Br J Dermatol 1973;89:383-393.
105. Finlay B. Scanning electron microscopy of the
human dermis under uniaxial strain. Biomed
Eng 1969;4:322-327.
106. Lavker RM, Zheng P, Gang D. Aged skin: a
study by light, transmission electron, and scan-
ning electron microscopy. J Invest Dermatol
1987;88(3):445-515.
107. Millington PF, Gibson T, Evans JH, Barbenel
Je. Structural and mechanical aspects of con-
nective tissue. In: Kenedi RM, ed. Advances in
biomedical engineering. Academic Press, New
York, pp. 189-248, 1971.
108. Ridge MD, Wright V. The directional effect of
skin-a bioengineering study of skin with
particular reference to Langer's lines. J Invest
DermatoI1966;46:341-346.
250
109. Dick Jc. Tension and resistance to stretching of
human skin and other membranes. J Physiol
1951;112:102-113.
110. Langer K. Zur anatomie und physiologie der
haut.1. Uber die spaltbarkeit der cutis. SB Akad
Wiss Wien 1861;44:19-46.
111. Gibson T, Stark H, Evans JH. Directional vari-
ation in extensibility of human skin in-vivo.
J Biomech 1969;2:201-204.
112. Flint MH. The biological basis of Langer's lines.
In: Longacre JJ, Charles C Thomas, eds. The
ultrastructure of collagen. Springfield, IL, pp.
132-140,1973.
113. Pierard G, Lapiere CM. Microanatomy of the
dermis in relation to relaxed skin tension lines
and Langer's lines. Am J Dermatol 1987;9(3):
219-224.
114. Gadd CW, Peterson F, Lange W, et al. Strength
of skin and its measurement. ASME Trans
1965;65-WAlHUF-8.
115. Peterson FJ, Lange WA, Gadd CWo Tear and
tensile strength of human skin under static and
dynamic loading. ASME Trans 1972;72-
WAlBHF-6.
116. Mackay GM, Smith CA. Facial injuries from
windshields. Am Assoc Auto Med 1983;27:
129-140.
117. Careless CM, Mackay GM. Skin tissue cuttabil-
ity and its relation to laceration severity indices.
Int IRCOBI Conf Biomech Impacts 1982;7:
195-206.
118. Leung YC, Lopat E, Fayor A, et al. Lacerative
properties of the human skin during impact. 3rd
IRCOBI Conference, pp. 399-411,1977.
119. Alexander H, Cook T. Variations with age in the
mechanical properties of human skin in vivo.
In: Kenedi RM, Cowden JM, eds. Bedsore bio-
mechanics. Macmillan, London, pp. 109-117,
1976.
120. Daly CH, Odland GF. Age-related changes
in the mechanical properties of human skin.
J Invest Dermatoll979;73:84--87.
121. Oxlund H, Manschot J, Viidik A. The role of
elastin in the mechanical properties of skin.
J Biomech 1988;21:213-218.
122. Wijn PFF. The alinear viscoelastic properties of
human skin in vivo for small deformations. PhD
Thesis, Katholieke Universiteit, Nijmegen, The
Netherlands, 1980.
123. Jagtman B. Clinical investigation of skin elas-
ticity. MD Thesis, Katholieke Universiteit,
Nijmegen, The Netherlands, 1983.
124. Gibson T, Kenedi RM, Craik JE. The mobile
micro-architecture of dermal collagen: a bio-
engineering study. Br J Surg 1965;52:764-770.
R.c. Haut
125. Dunn MG, Silver FH. Viscoelastic behavior of
human connective tissues: relative contribution
of viscous and elastic components. Connect
Tissue Res 1983;12:59-70.
126. Reihsner R, Balogh B, Menzel EJ. 1\\'0-
dimensional elastic properties of human skin in
terms of an incremental model at the in vivo
configuration. Med Eng Phys 1995;17(4):
304-313.
127. Reihsner R, Menzel EJ. On the orthogonal
anisotropy of human skin as a function of
anatomical region. Connect Tissue Res 1996;34:
145-160.
128. Daly CH. Biomechanical properties of dermis.
J Invest DermatoI1982;79:17-20.
129. Manschot JFM, Brakkee AJM. The measure-
ment and modeling of the mechanical proper-
ties of human skin in vivo-II, the model.
J Biomech 1986;19(7):517-521.
130. Holzmann H, Korting GW, Kobert D, Vogel
HG. Mechanical properties of skin in relation
to age and sex. Orchin Klin Exp DermatoI1971;
239:355.
131. Cacou C, Muir IFK. Effects of plane mechani-
cal forces in wound healing in humans. J R CoIl
Surg Edinb 1995;40:38-41.
132. Rollhauser H. Die zugfestigkeit der men-
schlichen haut; Genenbaurs morphol. Jahrb
1950;90:249-261.
133. Fazekas IG, Kosa F, Basch A. On the tensile
strength of skin in various body areas. Dtsch Z
Ges Gerich Med 1968;64:62-68.
134. Jansen LH, Rottier PB. Some mechanical prop-
erties of human abdominal skin measured on
excised strips. Dermatologica 1958;117:65-83.
135. Fry P, Harkness MLR, Harkness RD. Mechan-
ical properties of the collagenous framework of
skin in rats of different ages. Am J Physiol
1964;206:1425-1429.
136. Yamada H. Tensile properties after skin of
animals. In: Evans FG, ed. Strength of biologi-
cal materials. Williams & Wilkins, Baltimore, pp.
226-231, 1970.
137. Haut RC. The effects of orientation and loca-
tion on the strength of dorsal rat skin in high
and low speed tensile failure experiments.
J Biomech Eng 1989;111:136-140.
138. Vogel HG. Influence of age, treatment with
corticosteroids and strain rate on mechanical
properties of rat skin. Biochim Biophys Acta
1972;286:79-83.
139. Li IT, Armstrong CG, Mow vc. The effect of
strain rate on mechanical properties of articu-
lar cartilage in tension. ASME Biomech Symp
AMD-Vol. 56 FED-Vol. 11983;117-120.
11. Biomechanics of Soft Tissue
140. Goodfield MJD, Millard LG. The skin in
diabetes mellitus. Diabetologia 1988;31:567-
575.
141. Hanna W, Friesen D, Bombardier C, Gladman
D, Hanna A. Pathological features of thick skin.
JAm Acad DermatoI1987;16:546-553.
142. Mulligan GW, et al. An introduction to the
understanding of blunt chest trauma. In: The
human thorax-anatomy, injury and bio-
mechanics. Society of Automobile Engineers,
Warrendale, PA, p. 67, 1976.
143. Cardany CR, Rodeheaver G, Thacker J,
Edgerton MT, Edlich RF. The crush injury: a
high risk wound. JACEP 1976;5(12):965-970.
144. Dobrin PB. Mechanical properties of arteries.
Physiol Rev 1978;58(2):397-460.
145. Hayashi K. Experimental approaches on
measuring the mechanical properties and con-
stitutive relation for arterial wall materials. J
Biomech 1996;29(8):1011-1014.
146. Fung YC, Fronek K, Patitucci P. Pseudoelastic-
ity of arteries and the choice of its mathemati-
cal expression. J Physiol Soc 1979;237(5):
H620-H631.
147. Demiray H, Vito RP. Large deformation analy-
sis of soft biomaterial. Int J Eng Sci 1976;14:
789-793.
148. Roach MR, Burton AC The reason for the
shape of the distensibility curves of arteries.
Can J Biochem PhysioI1957;35:681-690.
149. Wolinsky H, Glagov S. Structural basis for the
static mechanical properties of the aortic
media. Circ Res 1964;14:400-413.
150. Bergel DH. The static elastic properties of the
arterial wall. J PhysioI1961;156:445-457.
151. Gozna ER, Marble AE, Shaw AJ, Winter DA.
Mechanical properties of the ascending tho-
racic aorta of man. Cardiovasc Res 1973;7:
261-265.
152. Wolinsky H, Glagov S. A lamellar unit of aortic
medial structure and function in mammals. Circ
Res 1967;20:90-111.
153. Tanaka TT, Fung YC Elastic and inelastic prop-
erties of the canine aorta and their variation
along the aortic tree. J Biomech 1974;7:357-
370.
154. Cox RH. Regional, species, and age related
variations in the mechanical properties of arter-
ies. Biorheology 1979;16:85-94.
155. Hayashi K, Nagasawa S, Naruo Y, et al.
Mechanical properties of human cerebral arter-
ties. Biorheology 1980;17:211-218.
156. Demiray H. A quasi-linear constitutive relation
for arterial wall materials. J Biomech 1996;
29(8):1011-1014.
251
157. Apter JT. Mathematical development of a phys-
ical model of some visco-elastic properties of
the aorta. Bull Math Biophys 1964;26:367-388.
158. Apter JT. Correlation of visco-elastic proper-
ties with microscopic structure of large arteries:
IV. Thermal responses of collagen, elastin,
smooth muscle, and intact arteries. Circ Res
1967;21:901-918.
159. Roach MR, Burton AC The effect of age on the
elasticity of human iliac arteries. Can J
Biochem PhysioI1959;37:557-569.
160. Mackay EH, Banks J, Sykes B, Lee G. Structural
basis for the changing physical properties of
human pulmonary vessels with age. Thorax
1978;33:335-344.
161. Hasegawa M. Rheological properties and wall
structures of large veins. Biorheology 1983;20:
531-545.
162. Viano DC, Culver CC, Haut RC, et al. Bolster
impacts to the knee and tibia of human cadav-
ers and a part 572 dummy. Soc Auto Eng Trans
1978;78:780-896.
163. Tiessen 1M, Roach MR. Factors in the initiation
and propagation of aortic dissections in human
autopsy aortas. J Biomech Eng 1993;115:123-
125.
164. Mohan D, Melvin Jw. Failure properties of
passive human aortic tissue. I-uniaxial tension
tests. J Biomech 1982;15(11):887-902.
165. Hoffman AS, Park JB. Sequential enzymolysis
of human aorta and resultant stress-strain
behavior. Biomater Med Dev Art Org 1977;
5(2):121-145.
166. Gennarelli TA, Spielman GM, Langfitt TW, et
al. Influence of the type of intracranial lesion on
outcome from severe head injury. J Neurosurg
1982;56:26-32.
167. Gennarelli RA, Thibault LE. Biomechanics of
acute subdural hematoma. J Trauma 1982;22:
680-686.
168. Lowenhielm P. Dynamic properties of the
parasagittal bridging veins. Z Rechtsmed
1974;74:55-62.
169. Lee M-C, Haut RC Insensitivity of tensile
failure properties of human bridging veins to
strain rate: implications in biomechanics of sub-
dural hematoma. J Biomech 1989;22(617):
537-542.
170. Lee M-C, Haut RC Strain rate effects on
tensile failure properties of the human
parasagittal bridging vein and the common
carotid artery and jugular veins of ferrets.
ASME Adv Bioeng 1985;18:111-112.
171. Haut RC, Garg BD, Metke M, Josa M, Kaye
MP. Mechanical properties of the canine aorta
252
following hypercholesterolemia. ASME 1979;
79-WNBio-5.
172. Mehrotra PO, Patel DJ, Coleman BR, et al. Dis-
tensibility of small pulmonary blood vessels. J
Biomech Eng 1993;115:286-289.
173. Liu SQ, Fung Xc. Material coefficients of the
strain energy function of pulmonary arteries in
normal and cigarette smoke-exposed rats. J
Biomech 1993;26(11):1261-1269.
174. Broom ND. The collagenous architecture of
articular cartilage-a synthesis of ultrastructure
and mechanical function. J RheumatoI1986;13:
142-152.
175. Benninghoff A. Form und ban der glenkknor-
pel in ihren beziehungen zur funktion. II. Der
aufbau des gelenkknorpels in seinen beziehun-
gen zur funktion. Z Zellforsch Mikroskop Anat
1925;2:783-862.
176. Egan JM. A constitutive study of the age-
dependent mechanical behavior of deep articu-
lar cartilage: model construction and simulated
failure. Clin Biomech 1988;3:204-214.
177. Hultkrantz W. Uber die spaltrichtungen der
gelenkkorpel. Verh Anat Ges 1898;12:248.
178. Maroudas A, Bannon C. Measurement of
swelling pressure in cartilage and comparison
with the osmotic pressure of constituent pro-
teoglycans. Biorheology 1981;18:619-632.
179. Kaab JJ, Ito K, Clark JM, Notzli HP. Deforma-
tion of articular cartilage collagen structure
under static and cyclic loading. J Orthop Res
1998;16:743-751.
180. Mizrahi J, Maroudas A, Lanir Y, Ziv I, Webber
TJ. The "instantaneous" deformation of
cartilage: effects of collagen fiber orientation
and osmotic stress. Biorheology 1986;23:311-
330.
181. Jurvelin J, Saamanen A, Arokoski J, et al.
Biomechanical properties of the canine knee
articular cartilage as related to matrix proteo-
glycans and collagen. Eng Med 1988;17(4):157-
162.
182. Mow Vc, Kuir SC, Lai WM, et al. Biphasic
creep and stress relaxation of articular cartilage
in compression: theory and experiments. J
Biomech Eng 1980;102:74-85.
183. Lanir Y. Biorheology and fluid flux in swelling
tissues. II. Analysis of unconfined compressive
response of transversely isotropic cartilage disc.
Biorheology 1987;24:187.
184. Behrens F, Kraft E, Oegema TR. Biochemical
changes in articular cartilage after joint immo-
bilization by casting or external fixation. J
Orthop Res 1989;7:335-343.
R.c. Haut
185. Troyer H. The effect of short-term immobiliza-
tion on the rabbit knee joint cartilage. Clin
Orthop ReI Res 1975;105:249-257.
186. Jurvelin J, Kiviranta I, Saamanen A, et al.
Partial restoration of immobilization-induced
softening of canine articular cartilage after
remobilization of the knee (stifle) joint. J
Orthop Res 1989;7:352-358.
187. Hamerman D. The biology of osteoarthritis.
N Engl J Med 1989;320:1322-1330.
188. Armstong CG, Mow Vc. Variations in the
intrinsic mechanical properties of human
articular cartilage with age, degeneration, and
water content. J Bone Joint Surg 1982;64A:88-
94.
189. Mow VC, Setton LA. Mechanical properties of
normal and osteoarthritic articular cartilage. In:
Brandt KD, Doherty M, Lohmander LS, eds.
Osteoarthritis. Oxford University Press, New
York, pp. 108-121, 1998.
190. Brandt KD, Fife RS. Ageing in the pathogene-
sis of osteoarthritis. Clin Rheum Dis 1986;12(1):
117-130.
191. Altman R, Asch E, Bloch G, et al. Development
of criteria for the classification and reporting of
osteoarthritis; classification of osteoarthritis of
the knee. Arthritis Rheum 1986;29(8):1039-
1049.
192. Insall J, Falvo KA, Wise DW. Chondromalacia
patellae: a prospective study. J Bone Joint Surg
1976;58:1-8.
193. Simon SR, Radin EL, Paul IL, Rose RM. The
response of joints to impact loading-II. In vivo
behavior of subchondral bone. J Biomech 1972;
5:267-272.
194. Repo RU, Finlay JB. Survival of articular carti-
lage after known impact. J Bone Joint Surg
1977;60A:1068-1075.
195. Silyn-Roberts H, Broom ND. Fracture behav-
iour of cartilage-on-bone in response to
repeated impact loading. Connect Tissue Res
1990;24:143-156.
196. Armstrong CG, Schoonbeck J, Moss G, et al.
Characterization of impact-induced micro-
trauma to articular cartilage. AS ME Adv
Bioeng 1980;153-156.
197. Donohue MJ, Buss D, Oegema TR, et al. The
effects of indirect blunt trauma on adult canine
articular cartilage. J Bone Joint Surg 1973;65A:
948-957.
198. Kempson JE. Mechanical properties of articu-
lar cartilage. In: Freeman MAR, ed. Articular
cartilage. Grune and Stratton, New York, pp.
171-227,1973.
11. Biomechanics of Soft Tissue
199. Kempson GE. Mechanical properties of
articular cartilage. In: Freeman MAR, ed. Adult
articular cartilage, 2nd ed. Pitman, Kent,
England, pp. 333-414, 1979.
200. Kempson GE. Relationship between the tensile
properties of articular cartilage from the
human knee and age. Ann Rheum Dis 1982;41:
508-511.
201. Woo SL-Y, Akeson W, Jemmott G, et al. Mea-
surements of the nonhomogeneous directional
properties of articular cartilage in tension. J
Biomech 1976;9:785-791.
202. Schmidt MB, Mow VC, Chun L, et al. Effects of
proteoglycan extraction on the tensile behavior
of articular cartilage. J Orthop Res 1990;8:
353-363.
203. Akizuki S, Mow VC, Muller F, et al. Tensile
properties of human knee joint cartilage: I.
Influence of ionic conditions, weight bearing,
and fibrillation on the tensile modulus. J
Orthop Res 1986;4:379-392.
204. Newberry WN, Garcia 11, Mackenzie CD,
DeCamp CE, Haut RC Analysis of acute
mechanical insult in an animal model of post-
traumatic osteoarthritis. J Biomech Eng 1998;
120:704-709.
205. Newberry WN, Mackenzie CD, Haut RC Blunt
impact causes changes in bone and cartilage in
a regularly exercised animal model. J Orthop
Res 1998;16:348-354.
253
206. Atkinson TS, Haut RC, Altiero NJ. Impact
induced fissuring of articular cartilage: an inves-
tigation of failure criteria. J Biomech Eng
1997;120:181-187.
207. Artkinson TS, Haut RC, Alteiro NJ. An investi-
gation of biphasic failure criteria for impact-
induced fissuring of articular cartilage. J
Biomech Eng 1998;120:536-537.
208. Buckwalter JA, Lane NE. Athletes and
osteoarthritis. Am J Sports Med 1997;25(6):
873-881.
209. Woo SL-Y, Gomez MA, Akeson WHo Mechan-
ical behaviors of soft tissues: measurements,
modifications, injuries and treatment. In:
Nahum AM, Melvin J, eds. The biomechanics of
trauma. Appleton, Crofts, Norwalk, CT, pp.
107-133,1985.
210. Panjabi M, Jorneus L, Greenstein G. Physical
properties of lumbar spine ligaments. Trans
Orthop Res Soc 1984;9:112.
211. Kenedi RM, Gibson T, Daly CH. Bio-
engineering studies of the human skin. II. In:
Kenedi R, ed. Biomechanics and related bio-
engineering topics. Pergamon Press, New York,
pp.147-158,1964.
212. Haut RC The mechanical and viscoelastic
properties of the anterior cruciate ligament and
of ACL fascicles. In: Jackson DW, ed. The ante-
rior cruciate ligament: current and future con-
cepts. Raven Press, New York, pp. 63-73, 1993.