Passive mechanical properties of rat abdominal wall muscles suggest an important role of the extracellular connective tissue matrix

Article (PDF Available)inJournal of Orthopaedic Research 30(8):1321-6 · August 2012with29 Reads
DOI: 10.1002/jor.22068 · Source: PubMed
Abstract
Abdominal wall muscles have a unique morphology suggesting a complex role in generating and transferring force to the spinal column. Studying passive mechanical properties of these muscles may provide insights into their ability to transfer force among structures. Biopsies from rectus abdominis (RA), external oblique (EO), internal oblique (IO), and transverse abdominis (TrA) were harvested from male Sprague-Dawley rats, and single muscle fibers and fiber bundles (4-8 fibers ensheathed in their connective tissue matrix) were isolated and mechanically stretched in a passive state. Slack sarcomere lengths were measured and elastic moduli were calculated from stress-strain data. Titin molecular mass was also measured from single muscle fibers. No significant differences were found among the four abdominal wall muscles in terms of slack sarcomere length or elastic modulus. Interestingly, across all four muscles, slack sarcomere lengths were quite long in individual muscle fibers (>2.4 µm), and demonstrated a significantly longer slack length in comparison to fiber bundles (p < 0.0001). Also, the extracellular connective tissue matrix provided a stiffening effect and enhanced the resistance to lengthening at long muscle lengths. Titin molecular mass was significantly less in TrA compared to each of the other three muscles (p < 0.0009), but this difference did not correspond to hypothesized differences in stiffness.
Passive Mechanical Properties of Rat Abdominal Wall Muscles Suggest
an Important Role of the Extracellular Connective Tissue Matrix
Stephen H.M. Brown,
1
John Austin Carr,
1
Samuel R. Ward,
1,2,3
Richard L. Lieber
1,2
1
Department of Orthopaedic Surgery, University of California San Diego, Research Service VA San Diego Healthcare System San Diego, California,
2
Deparment of Bioengineering, University of California San Diego, San Diego, California,
3
Department of Radiology, University of California
San Diego, San Diego, California
Received 16 May 2011; accepted 19 December 2011
Published online 20 January 2012 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/jor.22068
ABSTRACT: Abdominal wall muscles have a unique morphology suggesting a complex role in generating and transferring force to the
spinal column. Studying passive mechanical properties of these muscles may provide insights into their ability to transfer force among
structures. Biopsies from rectus abdominis (RA), external oblique (EO), internal oblique (IO), and transverse abdominis (TrA) were
harvested from male Sprague–Dawley rats, and single muscle fibers and fiber bundles (4–8 fibers ensheathed in their connective
tissue matrix) were isolated and mechanically stretched in a passive state. Slack sarcomere lengths were measured and elastic moduli
were calculated from stress–strain data. Titin molecular mass was also measured from single muscle fibers. No significant differences
were found among the four abdominal wall muscles in terms of slack sarcomere length or elastic modulus. Interestingly, across all four
muscles, slack sarcomere lengths were quite long in individual muscle fibers (>2.4 mm), and demonstrated a significantly longer slack
length in comparison to fiber bundles (p < 0.0001). Also, the extracellular connective tissue matrix provided a stiffening effect and
enhanced the resistance to lengthening at long muscle lengths. Titin molecular mass was significantly less in TrA compared to each of
the other three muscles (p < 0.0009), but this difference did not correspond to hypothesized differences in stiffness. ß 2012 Orthopaedic
Research Society. Published by Wiley Periodicals, Inc. J Orthop Res 30:1321–1326, 2012
Keywords: spine; muscle; passive mechanics; sarcomere; transversus abdominis
Abdominal wall muscles play a vital role in generating
controlled movement of the lumbar and thoracic spine.
The unique anatomical arrangement of the four
muscles [rectus abdominis (RA), external oblique (EO),
internal oblique (IO), and transverse abdominis (TrA)]
has inspired descriptions and related hypotheses
regarding its function as a composite-laminate struc-
ture.
1–3
This composite laminate-like morphology has
been hypothesized to enhance the ability of the abdom-
inal wall to transfer force and stiffen the spine. Mate-
rial properties of the components of this composite
must be understood to define the structural basis for
the properties of the abdominal wall. However, the
passive mechanical properties of the abdominal wall
muscle fibers and extracellular matrix remain unclear
and thus motivated this study.
Muscle passive mechanical properties have been
used to describe structural function,
4–6
differentiate be-
tween healthy and diseased muscle,
7,8
and characterize
muscle adaptation to joint-related injury.
9
Studies of
abdominal wall muscle passive properties were per-
formed previously,
3,10,11
identifying varying differences
in stiffness among muscles. However, these studies
were limited by three main factors: (i) no study quanti-
fied and compared the four muscles; (ii) no sarcomere
length measurements were made to normalize strain or
extension data; and (iii) only large muscle strips were
tested, thereby not elucidating differences between in-
tracellular and extracellular sources of passive
stiffness. Previous work demonstrated that differences
that are not apparent on one scale (e.g., a single muscle
fiber) may become apparent on a different scale (e.g., a
bundle of muscle fibers and connective tissue matrix),
highlighting the importance of studying muscle at both
the single cell and muscle fiber bundle levels.
7,8
Architectural analyses of human abdominal wall
muscles predicted that regional fascicles of EO and IO
may lengthen towards or beyond the end of force–
length relationship during maximal contralateral
bend.
12
Passive mechanical properties of the abdomi-
nal wall muscles and the interaction among the
muscles dictate the passive stress and strain that mus-
cle fibers and connective tissues will experience during
such lengthening. Comparison of abdominal wall mus-
cle architectural properties between human and rat
demonstrated similar physiological cross-sectional
areas, relative fascicle and sarcomere lengths, and fi-
ber orientations, suggesting that they have similar
functional roles in moving and supporting the spine.
2
Thus, the use of a rat model to study material proper-
ties may provide insight into the structure and func-
tion of the human abdominal wall muscles.
This study was designed to determine the passive
mechanical properties (stiffness and slack sarcomere
length) of rat abdominal wall muscles at the single
fiber and fiber bundle levels. Molecular mass of titin,
the protein most often suggested to dominate passive
muscle behavior,
4
was also measured to provide
insights into potential differences in mechanical prop-
erties among the muscles.
METHODS
All procedures were approved by the local IACUC. Six adult
male Sprague–Dawley rats were euthanized, and biopsies of
RA, EO, IO, and TrA were immediately obtained and placed
Stephen H.M. Brown present address is Department of Human
Health and Nutritional Sciences, University of Guelph, Guelph,
ON, Canada.
Correspondence to: Richard L. Lieber (T: 858-822-1344; F: 858-
822-3807; E-mail: rlieber@ucsd.edu)
ß 2012 Orthopaedic Research Society. Published by Wiley Periodicals, Inc.
JOURNAL OF ORTHOPAEDIC RESEARCH AUGUST 2012
1321
in storage solution at 208C to prevent hyperpolarization
and destruction of the muscle tissue.
8
All muscles were tested within 2 weeks of harvest. Test-
ing was performed in a relaxing solution
8
to ensure muscle
properties were assessed in a passive state. Single fibers and
small fiber bundles (comprised of 4–8 fibers ensheathed in
their connective tissue matrix) were isolated and tied with
10-0 silk thread to pins secured at one end to a force trans-
ducer (Model 405A, Aurora Scientific, Aurora, ON, Canada),
and at the other end to a high-speed motor (Model 318B,
Aurora Scientific) to manipulate specimen length. Typically,
two single fibers and two fiber bundles were tested from each
muscle. A 7 mW diode laser transilluminated the specimen
and generated a diffraction pattern, enabling sarcomere
length measurement during testing.
13
Specimens were initially lengthened until they started to
generate a measurable passive force above the noise level of
the force transducer; further tests were initiated from this
length (termed slack sarcomere length). The motor was con-
trolled to provide rapid (100 fiber lengths/second) stretch to
the specimens in increments of 0.25 mm/sarcomere (10%
strain). After each stretch, the fiber or fiber bundle was held
at constant length for 3 min to allow stress relaxation to oc-
cur. A minimum of seven stretches were performed on each
specimen. Sarcomere length changes relative to initial slack
length were used to compute specimen strain. Force at the
end of each 3-min relaxation period was normalized to fiber
or fiber bundle cross-sectional area (calculated at slack sarco-
mere length by measuring specimen diameter via cross-hairs
under a microscope and assuming a circular area) to calcu-
late stress.
Pilot data demonstrated that single muscle fibers behaved
differently compared to fiber bundles; stress–strain profiles
of single fibers displayed a small toe region followed by a
linear elastic region, whereas fiber bundles displayed a non-
linear response throughout the range of stretch. Therefore,
elastic moduli were calculated for single fibers as the slope of
the linear region of the stress–strain curve (corresponding to at
least four stretches) and for fiber bundles as the 1st derivative
of 2nd-order polynomials fit to the stress–strain data. Fiber
bundle moduli were then calculated and compared among
muscles at a sarcomere length of 3.2 mm(1/2 the length of
the descending limb of the force–length relationship for rat
muscle).
14
Also, as a second method for comparing fiber and
fiber bundle properties, calculations were made of the sarco-
mere length at which fiber bundles reached a stiffness (from
the 1st derivative of 2nd-order polynomials) that exceeded the
mean stiffness of individual fibers from each muscle.
Titin molecular mass was quantified in single fibers that
had been tested mechanically from each muscle group. Proce-
dures for this vertical agarose gel electrophoresis (VAGE)
method were published previously.
15
Briefly, single fibers
were boiled in sample buffer solution, and SDS–VAGE analy-
sis was used the quantify titin migration relative to the
migration of titin standards (human soleus titin and rat
cardiac titin, masses of 3,700 and 2,992 kD, respectively).
Slack sarcomere lengths and elastic moduli were com-
pared statistically using two-way ANOVA with factors of:
muscle (RA, EO, IO, TrA); and specimen size (individual
fibers vs. fiber bundles). Titin mass was compared among
muscles (for single fibers and fiber bundles) using one-
way ANOVAs. Where appropriate, Tukey’s HSD test was
used for post hoc analysis. The significance level (a) was set
at p < 0.05.
RESULTS
Elastic Modulus
No significant differences in elastic modulus were
found among the four abdominal wall muscles for indi-
vidual fibers (p ¼ 0.35) or fiber bundles (p ¼ 0.84), nor
between individual fibers and fiber bundles at a sarco-
mere length of 3.2 mm(p¼ 0.15) (Fig. 1). Mean
SEM r
2
values for curve fits were 0.99 0.002 for
linear fibers and 0.99 0.003 for nonlinear bundles.
Single fibers displayed a toe region followed by a linear
elastic region, whereas fiber bundles displayed a non-
linear stress–strain relationship best characterized by
a 2nd-order polynomial (Figs. 2 and 3). Thus, to fur-
ther compare properties between fibers and bundles,
we calculated the sarcomere length for each muscle at
which fiber bundles became stiffer than single fibers.
Figure 1. Mean elastic modulus of single fibers and fiber bun-
dles for each abdominal wall muscle. Moduli of single fibers were
calculated as the slope of the linear region of the stress–strain
relationship. Moduli of fiber bundles were calculated by fitting
2nd-order polynomials to the stress–strain data of each sample,
differentiating and solving for modulus at a sarcomere length of
3.2 m m. No significant differences were found among any of the
muscles nor between fibers and bundles at this sarcomere length.
Error bars represent standard error of the mean.
Figure 2. Representative stress–strain raw data points and
curve fits for three individual RA muscle fibers and three RA
fiber bundles. Individual fibers were linearly fit after exceeding
an initial toe region; fiber bundles were fit with 2nd-order poly-
nomials over the stress–strain relationship.
1322 BROWN ET AL.
JOURNAL OF ORTHOPAEDIC RESEARCH AUGUST 2012
These lengths were: RA ¼ 3.05 mm; EO ¼ 3.06 mm;
IO ¼ 3.20 mm; TrA ¼ 2.80 mm.
Slack Sarcomere Length
Slack sarcomere lengths were not significantly differ-
ent among the four abdominal wall muscles (p ¼ 0.38,
Fig. 4). Individual muscle fibers and fiber bundles did
have significantly different slack sarcomere lengths
(p < 0.001), with bundles being shorter (Fig. 4), as pre-
viously reported for human upper extremity muscles.
8
Titin Isoform Size
Titin molecular mass of the TrA was significantly
smaller (p < 0.001) compared to the other three
abdominal wall muscles (Fig. 5).
DISCUSSION
Our results demonstrate that the four abdominal wall
muscles have similar passive mechanical properties in
the rat. The most interesting finding is that, for each
muscle, individual muscle fibers behaved differently
compared to bundles consisting of fibers ensheathed in
their connective tissue matrix. Specifically, fiber bun-
dles had a shorter slack sarcomere length and demon-
strated a nonlinear stress–strain response, whereas
individual fibers had long slack sarcomere lengths and
Figure 3. (A) Second-order polynomial fits of fiber bundle
stress–sarcomere length relationship across all animals for each
muscle. Data were fit to the stress–strain relationship for each
tested fiber bundle, and coefficients were averaged across all
samples for each muscle. Strain was then converted to sarcomere
length based on average slack sarcomere lengths for fiber bun-
dles for each muscle. Stress SEM, calculated from the polynomial
fits at sarcomere length 4.24 mm, were: RA 14.1 kPa; EO
31.0 kPa; IO 23.6 kPa; and TrA 24.5 kPa. (B) Piece-wise linear
fits of individual fiber stress–sarcomere length relationship
across all animals for each muscle. Data were fit to the stress–
strain relationship for each tested fiber, and coefficients were
averaged across all samples for each muscle. The steeper linear
region for each muscle represents the modulus values reported in
Figure 1. In both A and B vertical lines represent sarcomere
length 3.2 mm where comparisons were made in Figure 1.
Figure 4. Mean slack sarcomere length of single fibers and
fiber bundles for each muscle. A significant difference was
observed between single fibers and fiber bundles ( p < 0.0001).
Error bars represent standard error of the mean.
Figure 5. (A) Mean titin molecular mass for single fibers from
each muscle. Star indicates TrA titin was significantly smaller
compared to each of the other three muscles (p < 0.0009). Error
bars represent standard error of the mean. (B) Example SDS–
VAGE gel lanes. Molecular masses were calculated by the migra-
tion of titin relative to standards of known mass (human soleus
and rat cardiac). STD represents the standard lane containing
titin from human soleus (sample) and rat cardiac muscle. RA rep-
resents the lane containing titin from RA (sample) and rat cardi-
ac muscle. TrA represents the lane containing titin from TrA
(sample) and rat cardiac muscle. T2 degradation bands are
degradation forms of the intact titin molecule.
4
ABDOMINAL WALL MUSCLE PASSIVE MECHANICS 1323
JOURNAL OF ORTHOPAEDIC RESEARCH AUGUST 2012
demonstrated a more linear response outside of an
initial toe region. The nonlinear stress–strain response
of fiber bundles makes them effectively much stiffer
than their constituent fibers at longer lengths, sug-
gesting an important stiffening effect of the connective
tissue matrix. Recently, by comparing fiber bundles to
‘‘groups’’ of fibers that were tied together, we showed
that this nonlinearity is due to the material properties
of the extracellular matrix itself and not due to non-
homogeneities among the fibers.
16
The importance of
this stiffening effect is addressed in context of the role
that these muscles play in controlling and stabilizing
the spine.
Mean slack sarcomere lengths of individual abdomi-
nal wall muscle fibers were equal to or longer than
active optimal sarcomere length (2.40 mm for rat).
These slack lengths are much longer, relative to opti-
mal length, than for previously reported human
muscles.
6,17
Bundle slack sarcomere lengths, however,
were much shorter than fiber slack sarcomere lengths.
This may be explained by two phenomena. First, the
connective tissue matrix of intact abdominal wall
muscle may have begun to bear load and resist length-
ening well before individual muscle fibers that make
up the majority of the mass of the tissue. Alternative-
ly, slack sarcomere lengths in fiber bundles may be
determined simply by the ‘‘least slack’’ individual
fiber, rather than by the extracellular matrix (ECM)
itself. This second possibility may explain the highly
nonlinear response of fiber bundles, characterized by
an initial region of low stiffness, where individual
fibers bear load, followed by a rapidly stiffening
response at longer lengths, where ECM begins to
bear load (Fig. 3). In this case, the substantial stiffen-
ing effect in fiber bundles at longer lengths may be
necessitated by the range of lengths these muscles ex-
perience in vivo. Brown et al.,
12
predicted, based on
architectural analyses of human abdominal wall
muscles, that, as the lumbar spine moves through its
full range of motion, abdominal wall muscles (in
particular EO and IO) lengthen well beyond the
plateau of the force–length relationship. If fibers in
these muscles begin to resist load at low sarcomere
lengths (low slack lengths), they would experience
high strain and stress at such long lengths, which
would be amplified during active lengthening. This
could potentially damage muscle fibers
18,19
or influ-
ence strain and/or stress induced cell signaling.
20,21
By
having greater intrinsic slack lengths, individual
fibers experience lower strain and stress when length-
ened. The stiffer connective tissue matrix observed in
the fiber bundles provides the stiffening effect that
may be necessary to transmit loads and stiffen the
spine at moderate and long muscle lengths. Second-or-
der polynomial curves fit to the bundle data suggest
that intact muscle becomes stiffer, when compared to
isolated fibers, on the early (TrA) to mid-range (RA,
EO, IO) of the descending limb of the force–length
relationship.
The important stiffening role of the matrix was sug-
gested in previous work on abdominal wall muscles.
Boriek et al.,
22
based on microdissection of canine IO
and TrA muscles, found that these muscles were pri-
marily comprised of short muscle fibers linked length-
wise to form long fascicles. They suggested that intra-
muscular extracellular connections are necessary to
transmit force between fibers along the muscle, as was
previously suggested for similar muscles.
23–25
Intrafas-
cicular terminating fibers have since been identified in
human abdominal wall muscles;
26
however, this has
not been examined for rat abdominal muscles. On a
more macroscopic scale, Brown and McGill
27
estab-
lished that connective tissue networks play a role in
transmitting force and stiffness between abdominal
wall muscle layers, demonstrating that the matrix
tissue may perform a load transmitting function at
multiple levels.
While no significant differences were found for pas-
sive mechanical properties among the four muscles,
modeled data suggests that TrA may behave in a
somewhat stiffer fashion compared to the other three
muscles. Specifically, TrA bundles become stiffer than
their constituent isolated fibers at shorter lengths
(2.80 mm) compared to the RA (3.05 mm), EO
(3.06 mm), and IO (3.20 mm). Further, as TrA contin-
ues to lengthen, it stiffens to a greater extent than the
other three muscles (Fig. 3), although not by a statisti-
cally significant amount (Fig. 1). Previous work also
indicated that TrA displays greater passive stiffness
than EO as the muscles are stretched beyond optimal
active length.
10
Significance for this may lie in work
that suggested TrA plays a specialized role in spine
control, based on findings that it activates prior to
other abdominal wall muscles in certain controlled
settings
28
and is more tonically active compared to the
other muscles during generation of opposing spine
flexion/extension moments and movements.
29
As the
deepest of the abdominal wall muscles, under certain
conditions, early and/or tonic activation of the stiff
TrA may serve a role of establishing a stiff foundation
upon which the larger IO and EO muscles can gener-
ate more substantial forces and moments.
Titin isoforms in TrA were smaller than in each of
the other muscles, consistent with its slightly stiffer
fiber behavior. Titin is a giant protein that spans the
half-sarcomere by its anchors on the Z-disc and
M-line, and has been thought to be the primary deter-
minant of muscle fiber passive stiffness
4
and slack
sarcomere length.
30
Despite the TrA having smaller
titin isoforms, which should make fibers stiffer with
shorter slack lengths, no difference in fiber stiffness
was found between TrA and the other muscles (Fig. 1);
yet while not significant, TrA did have a shorter slack
sarcomere length than the other three (Fig. 4). The
lack of significant differences for stiffness and slack
length for TrA may not be surprising, as the signifi-
cant difference in titin isoform size is a relatively small
fraction of the titin mass (2%) reported for skeletal
1324 BROWN ET AL.
JOURNAL OF ORTHOPAEDIC RESEARCH AUGUST 2012
muscle (3,300–3,700 kDa
4
). Further, other recent evi-
dence indicates that titin size does not correlate as
strongly with fiber stiffness as may have been previ-
ously thought,
6
suggesting that other structures with-
in the muscle fiber may also contribute to passive
stiffness.
Muscles of the low back and abdominal wall region
play a vital orthopedic role in stabilizing and control-
ling motion of the lumbar spine.
31–33
Recent work
focusing on mechanical and structural properties of
these muscles demonstrated their unique muscular de-
sign for controlling the complex motion and loading
patterns of the spinal column.
6,12,34
Our study further
describes such unique properties in abdominal wall
muscles. This information can be used: to guide proto-
cols to train these muscles for low back injury preven-
tion and rehabilitation; to establish baselines to
examine how these muscles adapt to spinal disorders;
and to refine surgical techniques to optimize mainte-
nance of natural structure and function of these
muscles.
The morphological, vascular, and innervation com-
plexities of the abdominal wall muscles, combined
with their proximity to internal organs, makes use of
an animal model necessary to study much of their ba-
sic physiological and mechanical behavior. Previous
work established morphological and architectural sim-
ilarities between the human and rat abdominal wall
muscles,
2
indicating that they have similar functional
and relative force-generating capabilities. However,
our results should be extrapolated to humans with
caution. Specifically, the nature of the connective tis-
sue within the muscles has not been compared be-
tween human and rat. Also, intact whole muscles
(with complete fascial and connective tissue compo-
nents) may behave differently than their component
fibers and fiber bundles. For example, passive proper-
ties of larger segments of RA, EO, and TrA were com-
pared previously with EO being more compliant than
TrA (Arnold et al.,
10
in hamsters) and RA (Farkas and
Rochester
11
in dogs). These results are not supported
by our data in rats.
Our work demonstrates that in rat abdominal wall
muscles the extracellular connective tissue matrix
plays an important role in regulating passive
mechanical behavior. Specifically, the connective
tissue matrix provides a substantial stiffening effect at
long sarcomere lengths (beyond the range of 2.80–
3.20 mm). While no significant differences in passive
mechanical behavior were found between the four
abdominal wall muscles, TrA fiber bundles did display
a slight trend of greater stiffness and lower slack
sarcomere lengths.
ACKNOWLEDGMENTS
This work was supported by NIH grant HD050837. SHM
Brown was supported by an NSERC post-doctoral
Fellowship.
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1326 BROWN ET AL.
JOURNAL OF ORTHOPAEDIC RESEARCH AUGUST 2012
    • "The human body relies on skeletal muscle, supported by other orthopaedic tissues, for locomotion and posture. Passive properties of muscle are governed by two components of the tissue: the protein titin at the sarcomere level which gives muscle fibers passive stiffness (Magid and Law, 1985; Tskhovrebova and Trinick, 2002), and the collagen rich extracellular matrix which organizes muscle fibers in a hierarchical structure and dominates passive stiffness at the tissue level (Brown et al., 2012; Meyer and Lieber, 2011). In the case of skeletal muscle these passive properties have a multifaceted purpose: allowing for the transmission of internal force generated at muscle fibers to tendons (Gindre et al., 2013; Huijing, 1999), storing energy during locomotion (Cavanagh and Komi, 1979; Ettema, 1996), and maintaining proper resting length for maximum force generation (Fridén and Lieber, 1998). "
    [Show abstract] [Hide abstract] ABSTRACT: The passive tensile properties of skeletal muscle play a key role in its physiological function. Previous research has identified conflicting reports of muscle transverse isotropy, with some data suggesting the longitudinal direction is stiffest, while others show the transverse direction is stiffest. Accurate constitutive models of skeletal muscle must be employed to provide correct recommendations for and observations of clinical methods. The goal of this work was to identify transversely isotropic tensile muscle properties as a function of post mortem handling. Six pairs of tibialis anterior muscles were harvested from Giant Flemish rabbits and split into two groups: fresh testing (within four hours post mortem), and non-fresh testing (subject to delayed testing and a freeze/thaw cycle). Longitudinal and transverse samples were removed from each muscle and tested to identify tensile modulus and relaxation behavior. Longitudinal non-fresh samples exhibited a higher initial modulus value and faster relaxation than longitudinal fresh, transverse fresh, and transverse rigor samples (p<0.05), while longitudinal fresh samples were less stiff at lower strain levels than longitudinal non-fresh, transverse fresh, and transverse non-fresh samples (p<0.05), but exhibited more nonlinear behavior. While fresh skeletal muscle exhibits a higher transverse modulus than longitudinal modulus, discrepancies in previously published data may be the result of a number of differences in experimental protocol. Constitutive modeling of fresh muscle should reflect these data by identifying the material as truly transversely isotropic and not as an isotropic matrix reinforced with fibers.
    Full-text · Article · Jul 2016
    • "Therefore, the material properties of this composite structure have been studied to better understand the abdominal wall mechanical behavior. The passive mechanical properties of the abdominal muscles have been investigated by several authors in different species: rat (Hwang et al., 2005; Brown et al., 2012; Brown, 2012), rabbit (Calvo et al., 2014; Simón-Allué et al., 2015), pig (Van Loocke et al., 2008; Lyons et al., 2014) and human (Förstemann et al., 2011). Moreover, the whole abdominal wall response to an increase of the intra-abdominal pressure has also been studied (Kotidis et al., 2011; Park et al., 2012; Rohlmann et al., 2006). "
    [Show abstract] [Hide abstract] ABSTRACT: In the present study a computational finite element technique is proposed to simulate the mechanical response of muscles in the abdominal wall. This technique considers the active behavior of the tissue taking into account both collagen and muscle fiber directions. In an attempt to obtain the computational response as close as possible to real muscles, the parameters needed to adjust the mathematical formulation were determined from in vitro experimental tests. Experiments were conducted on male New Zealand White rabbits (2047±34g) and the active properties of three different muscles: Rectus Abdominis, External Oblique and multi-layered samples formed by three muscles (External Oblique, Internal Oblique, and Transversus Abdominis) were characterized. The parameters obtained for each muscle were incorporated into a finite strain formulation to simulate active behavior of muscles incorporating the anisotropy of the tissue. The results show the potential of the model to predict the anisotropic behavior of the tissue associated to fibers and how this influences on the strain, stress and generated force during an isometric contraction.
    Article · Apr 2016
    • "The passive properties of skeletal muscle play a key role in force transmission throughout the tissue under active generation and passive stretch (Brown et al., 2012; Gillies and Lieber, 2011; Huijing, 1999; Smith et al., 2011). In tendon transfer procedures, the detachment and re-attachment of a muscle requires the estimation of resting length with manual tensioning, which can lead to deficiencies in contractile function ( Lieber, 2002, 1998). "
    [Show abstract] [Hide abstract] ABSTRACT: Introduction: Computational modeling of skeletal muscle requires characterization at the tissue level. While most skeletal muscle studies focus on hyperelasticity, the goal of this study was to examine and model the nonlinear behavior of both time-independent and time-dependent properties of skeletal muscle as a function of strain. Materials and methods: Nine tibialis anterior muscles from New Zealand White rabbits were subject to five consecutive stress relaxation cycles of roughly 3% strain. Individual relaxation steps were fit with a three-term linear Prony series. Prony series coefficients and relaxation ratio were assessed for strain dependence using a general linear statistical model. A fully nonlinear constitutive model was employed to capture the strain dependence of both the viscoelastic and instantaneous components. Results: Instantaneous modulus (p<0.0005) and mid-range relaxation (p<0.0005) increased significantly with strain level, while relaxation at longer time periods decreased with strain (p<0.0005). Time constants and overall relaxation ratio did not change with strain level (p>0.1). Additionally, the fully nonlinear hyperviscoelastic constitutive model provided an excellent fit to experimental data, while other models which included linear components failed to capture muscle function as accurately. Conclusions: Material properties of skeletal muscle are strain-dependent at the tissue level. This strain dependence can be included in computational models of skeletal muscle performance with a fully nonlinear hyperviscoelastic model.
    Full-text · Article · Sep 2015
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