Passive mechanical properties of rat abdominal wall muscles suggest an important role of the extracellular connective tissue matrix
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,
John Austin Carr,
Samuel R. Ward,
Richard L. Lieber
Department of Orthopaedic Surgery, University of California San Diego, Research Service VA San Diego Healthcare System San Diego, California,
Deparment of Bioengineering, University of California San Diego, San Diego, California,
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-
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,
tween healthy and diseased muscle,
muscle adaptation to joint-related injury.
abdominal wall muscle passive properties were per-
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.
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
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.
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
was also measured to provide
insights into potential differences in mechanical prop-
erties among the muscles.
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,
Correspondence to: Richard L. Lieber (T: 858-822-1344; F: 858-
822-3807; E-mail: firstname.lastname@example.org)
ß 2012 Orthopaedic Research Society. Published by Wiley Periodicals, Inc.
JOURNAL OF ORTHOPAEDIC RESEARCH AUGUST 2012
in storage solution at 208C to prevent hyperpolarization
and destruction of the muscle tissue.
All muscles were tested within 2 weeks of harvest. Test-
ing was performed in a relaxing solution
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.
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-
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
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.
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.
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
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.
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).
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.
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.
The importance of
this stiffening effect is addressed in context of the role
that these muscles play in controlling and stabilizing
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
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.,
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
ence strain and/or stress induced cell signaling.
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
The important stiffening role of the matrix was sug-
gested in previous work on abdominal wall muscles.
Boriek et al.,
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.
cicular terminating ﬁbers have since been identiﬁed in
human abdominal wall muscles;
however, this has
not been examined for rat abdominal muscles. On a
more macroscopic scale, Brown and McGill
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
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
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
and is more tonically active compared to the
other muscles during generation of opposing spine
ﬂexion/extension moments and movements.
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
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
). Further, other recent evi-
dence indicates that titin size does not correlate as
strongly with ﬁber stiffness as may have been previ-
suggesting that other structures with-
in the muscle ﬁber may also contribute to passive
Muscles of the low back and abdominal wall region
play a vital orthopedic role in stabilizing and control-
ling motion of the lumbar spine.
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.
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
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
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.,
in hamsters) and RA (Farkas and
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
This work was supported by NIH grant HD050837. SHM
Brown was supported by an NSERC post-doctoral
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