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Gender Differences In Musculotendinous Stiffness And Range Of Motion In College-Aged Men And Women

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The purpose of the present study was to examine musculotendinous stiffness (MTS) and ankle joint range of motion (ROM) in men and women after an acute bout of passive stretching. Thirteen men (mean ± SD age = 21 ± 2 years; body mass = 79 ± 15 kg; and height = 177 ± 7 cm) and 19 women (21 ± 3 years; 61 ± 9 kg; 165 ± 8 cm) completed stretch tolerance tests to determine MTS and ROM before and after a stretching protocol that consisted of 9 repetitions of passive, constant-torque stretching. The women were all tested during menses. Each repetition was held for 135 seconds. The results indicated that ROM increased after the stretching for the women (means ± SD pre to post: 109.39° ± 10.16° to 116.63° ± 9.63°; p ≤ 0.05) but not for the men (111.79° ± 6.84° to 113.93° ± 8.15°; p > 0.05). There were no stretching-induced changes in MTS (women's pre to postchange in MTS: -0.35 ± 0.38; men's MTS: +0.17 ± 0.40; p > 0.05), but MTS was higher for the men than for the women (MTS: 1.34 ± 0.41 vs. 0.97 ± 0.38; p ≤ 0.05). electromyographic amplitude for the soleus and medial gastrocnemius during the stretching tests was unchanged from pre to poststretching (p > 0.05); however, it increased with joint angle during the passive movements (p ≤ 0.05). Passively stretching the calf muscles increased stretch tolerance in women but not in men. But the stretching may not have affected the viscoelastic properties of the muscles. Practitioners may want to consider the possible gender differences in passive stretching responses and that increases in ROM may not always reflect decreases in MTS.
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GENDER DIFFERENCES IN MUSCULOTENDINOUS
STIFFNESS AND RANGE OF MOTION AFTER AN
ACUTE BOUT OF STRETCHING
KATHERINE M. HOGE,
1
ERIC D. RYAN,
2
PABLO B. COSTA,
1
TRENT J. HERDA,
1
ASHLEY A. WALTER,
1
JEFFREY R. STOUT,
3
AND JOEL T. CRAMER
1
1
Biophysics Laboratory, Department of Health and Exercise Science, University of Oklahoma, Norman, Oklahoma;
2
Applied
Musculoskeletal and Human Physiology Laboratory, Department of Health and Human Performance, Oklahoma State
University, Stillwater, Oklahoma; and
3
Metabolism and Body Composition Laboratory, Department of Health and Exercise
Science, University of Oklahoma, Norman, Oklahoma
ABSTRACT
Hoge, KM, Ryan, ED, Costa, PB, Herda, TJ, Walter, AA,
Stout, JR, and Cramer, JT. Gender differences in musculoten-
dinous stiffness and range of motion after an acute bout of
stretching. J Strength Cond Res 24(10): 2618–2626,
2010—The purpose of the present study was to examine
musculotendinous stiffness (MTS) and ankle joint range of
motion (ROM) in men and women after an acute bout of passive
stretching. Thirteen men (mean 6SD age = 21 62 years; body
mass = 79 615 kg; and height = 177 67 cm) and 19 women
(21 63 years; 61 69 kg; 165 68 cm) completed stretch
tolerance tests to determine MTS and ROM before and after
a stretching protocol that consisted of 9 repetitions of passive,
constant-torque stretching. The women were all tested during
menses. Each repetition was held for 135 seconds. The results
indicated that ROM increased after the stretching for the women
(means 6SD pre to post: 109.39°610.16°to 116.63°6
9.63°;p#0.05) but not for the men (111.79°66.84°to
113.93°68.15°;p.0.05). There were no stretching-induced
changes in MTS (women’s pre to postchange in MTS: 20.35 6
0.38; men’s MTS: +0.17 60.40; p.0.05), but MTS was higher
for the men than for the women (MTS: 1.34 60.41 vs. 0.97 6
0.38; p#0.05). electromyographic amplitude for the soleus and
medial gastrocnemius during the stretching tests was un-
changed from pre to poststretching (p.0.05); however, it
increased with joint angle during the passive movements (p#
0.05). Passively stretching the calf muscles increased stretch
tolerance in women but not in men. But the stretching may
not have affected the viscoelastic properties of the muscles.
Practitioners may want to consider the possible gender differ-
ences in passive stretching responses and that increases in
ROM may not always reflect decreases in MTS.
KEY WORDS constant torque, viscoelastic properties, electro-
myography
INTRODUCTION
Stretching is commonly used to improve perfor-
mance (2,49,51,52) and reduce the risk of injury
(5,18,47) before athletic events. It has been
suggested that stretching will decrease the amount
of strain through a range of motion (ROM), thereby reducing
the risk of injury (12,44,53). A stiffer musculotendinous unit
(MTU) is thought to better withstand large and rapid forces
better than a compliant system, thus reducing the likelihood
of injury (9,20,29,35). However, there is little evidence to
support the relationship between increased flexibility and
reduced incidence of injury (25,26,54,55). Yet, a recent study
by Shehab et al. (48) found that stretching routines are still
performed by high-school athletes as an injury prevention
strategy. In addition, there is little research indicating that
stretching improves performance. An acute bout of static
stretching has been found to reduce muscle strength (14,22)
and power (11), impair balance (3), and increase movement
and reaction times (3). In addition, a study by Nelson and
Kokkonen (37) asked subjects before testing whether
stretching would have a beneficial or detrimental outcome,
and all subjects believed that an acute bout of stretching
would result in better performance. However, because of the
limited evidence supporting stretching before competition,
the President’s Council for Physical Fitness and Sports
released a statement concluding that stretching may not
prevent injury and may also compromise performance (27).
Despite the discrepancy between knowledge and practice,
stretching is still a major component of preactivity warm-up
routines, and therefore, additional research is necessary
to determine the precise effects of stretching on injury
prevention.
Address correspondence to Dr. Joel T. Cramer, jcramer@ou.edu.
24(10)/2618–2626
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Many stretching studies use increases in flexibility as the
primary variable; however, total ROM provides only a fraction
of the information regarding the physiological changes in the
MTU (33). Measures of musculotendinous stiffness (MTS), in
conjunction with ROM, may provide a more comprehensive
understanding of the biomechanical responses of the MTU.
Musculotendinous stiffness is defined as the ratio of change in
passive force in a muscle because of its change in length (35).
It is generally calculated using passive angle-torque or angle–
force curves during a passive stretch (30). The slope of any
tangent to the passive angle-force curve is recorded as the
MTS. Tangential slopes can be calculated at any joint angle to
quantitatively measure the amount of passive resistance
throughout a given ROM. Therefore, stretching-induced
increases in ROM and decreases in MTS imply that not only
is there an increase in ROM, but there are also decreases in
passive stiffness and altered viscoelastic properties of the
MTU.
It is well known that the connective tissues of men and
women differ physiologically (24). However, the mechanisms
contributing to these differen-
ces are not well understood.
Estrogen may play a role, be-
cause estrogen receptors are
present in fibroblasts of tendons
and ligaments, which may alter
collagen synthesis and affect
tissue behavior (24). Other
hormonal fluctuations through-
out the menstrual cycle may
also influence the behavior
of the MTU (13,21,43). Eiling
et al. (13) found significant
decreases in MTS of the knee
flexors during the ovulatory
phase, when estrogen and pro-
gesterone are elevated, com-
pared to all other phases of the
menstrual cycle. In addition,
Ryan et al. (46), using periph-
eral quantitative computed to-
mography, showed a positive
relationship between muscle
size and MTS, providing a pos-
sible explanation for gender
differences in MTS, as men
generally have greater muscle
mass than women.
To our knowledge, only 1
study has compared the MTS
responses to stretching be-
tween men and women (15).
This study used 3, 60-second
constant-angle stretches of the
plantar flexors to measure
viscoelastic stress relaxation and passive elastic stiffness at
each joint angle. However, constant-torque stretches have
been shown to result in greater decreases in MTS and
increases in ROM than constant-angle stretches (56,57).
Therefore, the purpose of this study was to examine the MTS
and ankle joint ROM changes in men and women after an
acute bout of passive, constant-torque stretching.
METHODS
Experimental Approach to the Problem
A repeated-measures design (pre vs. poststretching) that is
depicted in Figure 1 was used to compare the acute effects of
passive stretching of the plantar flexors on MTS and ROM)
in men vs women. Each subject visited the laboratory on 2
separate occasions. The first visit was a familiarization
trial during which the subjects practiced the stretch toler-
ance assessments, and the investigators determined the
maximum tolerable stretching threshold that could be
sustained throughout the entire passive stretching protocol.
This was accomplished by sequentially increasing the
Figure 1. A schematic representation of the experimental design.
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amount of passive torque applied by the dynamometer until
each subject acknowledged discomfort, but not pain elicited
by the stretching protocol. This passive torque setting
was then used during the experimental trial to administer
the stretching protocol. Stretch tolerance, however, was the
maximum amount of passive torque applied by the dyna-
mometer that could be momentarily tolerated by the subject.
To determine stretch tolerance, the passive torque setting
was increased to a supramaximal level, and the dynamometer
was manually stopped by the investigators when the subject
acknowledged the momentary onset of pain during the
ROM. The stretch tolerance test was used to determine each
subject’s maximal ROM and MTS. The second visit was the
experimental trial during which all testing and stretching
took place. Subjects visited the laboratory during normal
hours (8 AM–8 PM). To avoid differences within the menstrual
cycle, the women were all tested during menses, which was
self-reported to the investigators. All subjects were also asked
to refrain from exercise 24 hours before the experimental
trial. Hydration status was not monitored before testing,
which should be noted as a limitation of this study. Figure 1
shows the schedule of assessments for this research design.
Subjects
Thirteen men (mean 6SD age = 20.8 61.8 years; body mass
= 79.0 615.0 kg; height = 176.9 67.2 cm) and 19 women
(age = 20.7 62.5 years; body mass = 60.9 68.9 kg; height =
165.1 67.6 cm) volunteered for this study. None of the
subjects reported any current or ongoing neuromuscular
diseases or musculoskeletal injuries to the foot, knee, or hip.
The women were also required to meet the following criteria:
(a) have consistent, normal menstrual cycles for the past
3 months, (b) report no use of any hormonal contraceptives
for the past 3 months, and (c) have been menstruating for at
least 1 year before the study (13). None of the subjects were
competitive athletes; however, because of their reported
levels of aerobic exercise (mean 6SD men = 3.6 63.9
hwk
21
; women = 3.9 62.6 hwk
21
) and resistance training
(men = 2.6 62.1 hwk
21
; women = 1.1 61.5 hwk
21
), these
individuals might be best classified as normal, recreationally
active participants. This study was approved by the
Institutional Review Board for Human Subjects, and all par-
ticipants completed a written informed consent form and
a Pre-Exercise Testing Health and Exercise Status Question-
naire before testing.
Procedures
Instrumentation. All participants were seated with restraining
straps over the thigh and the tibia just distal to the knee
joint. Each subject’s foot was stabilized in a custom-built
apparatus described and used in previous studies (44) to
measure plantar flexion force equipped with a sensitive load
cell (Omega Engineering Inc., Stamford, CT, USA). Figure 2
shows a picture of a subject situated in the custom apparatus.
The leg flexion angle was kept at 0°below the horizontal
plane (full extension), and a neutral ankle joint angle was
considered 0°(90°between the foot and the leg). The lateral
malleolus of the fibula was aligned with the joint axis of the
custom-built apparatus. The subject’s foot and heel were
stabilized into a thick rubber heel cup and held against the
foot plate with straps over the toes and metatarsals so that
the straps would not impede any passive foot movement
of the ankle joint. The apparatus was also attached to
a calibrated Biodex system 3 isokinetic dynamometer
(Biodex Medical Systems Inc., Shirley, NY, USA) that was
programmed in ‘‘passive’’ mode to stretch the plantar flexor
muscles by passively dorsiflexing the foot at 5°s
21
until the
maximum tolerable torque threshold was met.
Flexibility Assessments and Stretching. Before and after the
passive stretching protocol, 2 stretch tolerance assessments
were performed during which subjects were asked to relax
while their foot was passively and maximally dorsiflexed at
5°s
21
. When the subject acknowledged their maximal ROM
had been reached, the dynamometer was stopped. After the
prestretching flexibility assessments, a 5-minute rest period
was allowed. The stretching protocol was performed in
the same position and in the same fashion as the stretch
tolerance assessments. Nine repetitions of the constant--
torque stretches were performed at the predetermined torque
threshold determined during the familiarization trial. Each
stretch was held for 135 seconds with 10 seconds of rest
between repetitions (22). Immediately after the stretching
protocol, 2 poststretching tolerance assessments were
performed in the same manner as described previously.
The average ROM achieved during the 2 assessments was
used for all subsequent analyses.
Electromyography. Surface electromyographic (EMG) signals
were recorded from bipolar, preamplified electrodes
(EL254S, Biopac Systems, Santa Barbara, CA, USA) placed
over the soleus and medial gastrocnemius muscles. The
Figure 2. Picture of the foot placement in the testing apparatus.
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electrodes had a fixed center-to-center interelectrode distance
of 20 mm and a gain of 350. To reduce interelectrode
impedance, the skin was shaved and lightly abraded, then
cleaned with isopropyl alcohol before electrode placement.
Electrodes were placed in accordance with the recommen-
dations of Hermens et al. (23). The soleus electrode was taped
along the longitudinal axis of the tibia at 66% of the distance
from the medial condyle of the femur to the medial
malleolus, below the base of the medial gastrocnemius.
The electrode for the medial gastrocnemius was taped to
the most prominent bulge of the muscle. A single, disposable,
pregelled, reference electrode (Ag–AgCl, Quinton Quick
Prep, Quinton Instruments Co., Bothell, WA, USA) was
placed on the spinous process of the seventh cervical
vertebrae. All EMG signals were filtered with a passband of
10–500 Hz using a zero-phase shift fourth-order Butterworth
filter. The EMG amplitude values were calculated using
a root-mean squared (RMS)
function and were quantified
with 200-millisecond epochs
corresponding to the same joint
angles used to quantify MTS
(neutral = 0°of dorsiflexion).
These RMS values were then
normalized to each respective
EMG RMS amplitude value
recorded during a maximal
voluntary contraction (MVC)
based on the procedures of
Gajdosik et al. (17). For nor-
malization, the baseline EMG
RMS was subtracted from the
RMS values calculated at each
joint angle and during the
MVC, and then the baseline-
corrected RMS values during
the passive stretches were ex-
pressed as a percentage of the
baseline-corrected MVC value
for each subject.
Signal Processing. The force (kg),
position (°), and EMG (mV)
signals were sampled simul-
taneously at 1 kHz with a
Biopac data acquisition system
(MP150WSW, Biopac Sys-
tems) during each passive
stretch tolerance test. All signals
were recorded and stored on a
personal computer (Dell Inspir-
on 8200, Dell Inc., Round Rock,
TX, USA) to be processed off-
line using custom-written soft-
ware (LabVIEW v. 8.5, National
Instruments, Austin, TX, USA). To calculate MTS, the ankle
joint angle (°) and force (kg) signals were plotted as
angle–force curves (i.e., stress–strain curves) and fit with
a second-order polynomial regression model. Musculotendi-
nous stiffness was calculated at the 3 final joint angles (each
separated by 2°) that were common to both the pre and
poststretching ranges of motion based on the equation
reported by Nordez et al. (38) The force values were gravity
corrected using a cosine function that subtracted the weight
of the foot platform measured at the neutral joint angle.
Statistical Analyses
A 2-way mixed-factorial analysis of variance (ANOVA) (time
[pre vs. poststretch] 3gender [male vs. female]) was used to
analyze the ROM data. A 3-way mixed-factorial ANOVA (time
[pre vs. poststretch] 3gender [male vs. female] 3angle [1 vs. 2
vs. 3]) was usedto analyze the MTS data, and a separate 4-way
Figure 3. Passive range of motion (ROM; °) from pre to poststretching for the men and women. The solid circles
and dark lines are the mean 6SEM values, and the open circles and dashed lines are the individual responses.
*Mean ROM value for the women increased from pre to poststretching (p#0.05).
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mixed-factorial ANOVA (time [pre vs. poststretch] 3gender
[male vs. female] 3angle[1vs.2vs.3]3muscle [soleus vs.
medial gastrocnemius]) was used to analyze the EMG
amplitude data. When appropriate, follow-up analyses were
performed using lower-order ANOVAs and independent and
dependent samples t-tests with Bonferroni corrections. The
assumption of sphericity was not met, so a Greenhouse–
Geisser adjustment was used to
correct for this violation. Pre-
vious test–retest reliability data
for this flexibility assessment in
our laboratory indicated that,
for 15 young men (24 63years)
measured on separate days, the
intraclass correlation coefficient
was 0.94 with a standard error
of measurement of 2.01%. The
SEM for ROM in the present
study was 4.6%, ES = 0.42, and
statistical power = 0.99. An
alpha level of p#0.05 was
considered statistically signifi-
cant for all comparisons. Statis-
tical analyses were performed
using SPSS v. 16.0 (SPSS Inc.,
Chicago, IL, USA).
RESULTS
Range of Motion
There was a significant time 3
gender interaction for ROM
(p= 0.020). Range of motion
increased from pre to post-
stretching for the women
(p,0.001), but not the men
(p= 0.066) (Figure 3).
Musculotendinous Stiffness
There was no 3-way interaction
(time 3angle 3gender, p=
0.258), no 2-way interactions
for time 3angle (p= 0.796) or
time 3gender (p= 0.144), but
there was a 2-way interaction
for angle 3gender (p= 0.019)
and no main effect for time (p=
0.590). The marginal means for
MTS (collapsed across time)
increased such that joint angle
1,joint angle 2 ,joint angle 3
for both the men and women
(p,0.001), and MTS was
greater for the men than the
women at all joint angles (p=
0.008) (Figure 4).
Electromyographic Amplitude
There was no 4-way interaction (time 3angle 3gender 3
muscle, p= 0.262), no 3-way interactions for time 3angle 3
gender (p= 0.168), angle 3muscle 3gender (p= 0.733),
time 3angle 3muscle (p= 0.186), or time 3muscle 3
gender (p= 0.073), no 2-way interactions for time 3gender
(p= 0.249), angle 3gender (p= 0.481), muscle 3gender
Figure 4. Musculotendinous stiffness (MTS; kg°
21
) plotted over the ankle joint angles used to calculate the MTS
values. The open circles represent the mean 6SEM for the women, whereas the solid circles represent the mean 6
SEM for the men. The solid lines represent the prestretching condition, whereas the dashed lines were
poststretching values. *Indicates that the mean MTS values increased from joint angle 1 to joint angle 2 to joint
angle 3 (p#0.05). Mean MTS values were greater for the men than for the women (p#0.05).
Figure 5. Electromyographic amplitude (mean 6SD) values of the soleus and medial gastrocnemius from pre to
poststretching. Electromyographic amplitude values are presented as a percentage of maximal voluntary
contraction. MG denotes medial gastrocnemius and SOL denotes soleus. *Significant difference from pre to
poststretching.
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(p= 0.841), or time 3angle (p= 0.644), but there were
significant 2-way interactions for time 3muscle (p= 0.039)
and angle 3muscle (p= 0.034). The marginal means for
soleus EMG (collapsed across time) increased such that joint
angle 1 ,joint angle 3 (p= 0.040) and joint angle 2 ,joint
angle 3 (p= 0.028); however, the soleus EMG amplitude did
not increase from joint angles 1 to 2 (p= 0.320). The marginal
means for medial gastrocnemius EMG (collapsed across
time) increased such that joint angle 1 ,joint angle 2 (p=
0.025) and joint angle 1 ,joint angle 3 (p= 0.019); however,
the medial gastrocnemius EMG amplitude did not increase
from joint angles 2 to 3 (p= 0.345). The EMG amplitude for
the soleus (p= 0.611) and medial gastrocnemius (p= 0.096)
was unchanged from pre to poststretching.
DISCUSSION
The main findings of the present study were that the ROM
increased after 20 minutes of passive stretching for the women
but not the men. Furthermore, there were no stretching-
induced changes in MTS, but MTS was higher for the men
than for the women throughout the study. These findings
were generally consistent with those of Magnusson et al.
(31,34) in that MTS at fixed joint angles was unchanged after
an acute bout of stretching. Magnusson et al. (31) examined
the effects of static and cyclic stretching of the hamstrings
and reported increases in ROM after both stretching
protocols, but no changes in MTS. The authors attributed
these findings to an increase in stretch tolerance, rather than
to a change in the viscoelastic properties of the MTU (31).
The differences between these studies were that Magnusson
et al. (31) used 1, 90-second stretch for the left and right
hamstrings, whereas the pres-
ent study used a constant-
torque stretching protocol
(22) consisting of 9, 135-second
stretches of the right triceps
surae. Therefore, based on the
hypothesis of Magnusson et al.
(31) that longer stretching du-
rations may elicit viscoelastic
changes in the MTU (i.e.,
decreases in MTS) rather than
simple increases in stretch tol-
erance, it is unclear why the
longer durations of stretching
in the present study did not
elicit changes in MTS.
We propose 4 potential ex-
planations as to why the longer
stretching durations in the pres-
ent study did not decrease
MTS, but improved ROM in
the women compared to pre-
vious studies: (a) differences
between the muscles examined,
(b) different stretching intensities, (c) different stretching
treatments, and (d) gender differences. For example, it is
possible that muscle-specific responses to stretching may
exist when comparing the hamstrings (31) and the triceps
surae. Ryan et al. (45) suggested that the smaller, distal
muscle groups such as the triceps surae may require longer
durations of stretching to elicit stretching-induced decreases
in muscle activation. It is possible that a similar principle
could be applied to changes in MTS. To illustrate, in another
study, Ryan et al. (44) showed that a minimum stretching
duration of 2 minutes was required to elicit decreases in MTS.
Because the duration of stretching in the present study was
longer than the minimum duration recommended by Ryan
et al. (44), our findings may also have been influenced by
stretching intensity.
The subjects’ pain tolerance may also have affected the
ROM and MTS results of the present study if they could
not tolerate higher stretching intensities. In theory, if the
stretching intensity of the present study was less than that of
previous studies that have demonstrated decrease in MTS
(33,36,38,44), then this may have contributed to the lack of
decrease in MTS in the present study. However, Behm et al.
(4) reported no changes in ROM after 3 separate stretching
protocols of varying intensities. The authors (4) suggested
that this may be attributed to either an increase in passive
tension because of delayed-onset muscle soreness from the
stretching or a greater myotatic stretch reflex at higher
stretching intensities that increased the active stiffness of the
muscle. Because EMG amplitude increased with joint angle
in the present study (Figures 5 and 6), our findings supported
the hypothesis of Behm et al. that the myotatic reflex
Figure 6. Electromyographic amplitude (mean 6SD) values of the soleus and medial gastrocnemius by joint angle.
Electromyographic amplitude values are presented as a percentage of maximal voluntary contraction . MG denotes
medial gastrocnemius and SOL denotes soleus. *Joint angle was significantly different from joint angle 1. Joint
angle was significantly different from joint angle 2. Joint angle was significantly different from joint angle 3.
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activation may have limited our ability to measure the
decreases in MTS if indeed they did exist. Thus, our findings
should be used as cautionary notes for future studies to ensure
that the myotatic reflex is quiescent while assessing MTS.
It is also possible that differences in the stretching protocol
could affect changes in MTS and ROM. Ryan et al. (44)
suggested that a constant-torque stretching protocol will
increase the work performed on the MTU, as compared
to a traditional static stretching protocol or constant-angle
stretch, which may not be as demanding. Yeh et al. found that
a constant-torque stretching protocol resulted in greater
decreases in MTS than a constant-angle stretching protocol
of the calf in hypertonic patients, which may have been
because of increased strain relaxation or muscle creep during
the constant-torque stretching (56,57). However, Magnusson
et al. (31) reported increases in ROM but no changes in MTS
after cyclic and static stretching of the hamstrings. Therefore,
the increases in ROM reported by Magnusson et al. (31) and
those reported in the present study may be because of
increases in stretch tolerance, rather than changes in the
viscoelastic properties of the muscle.
Gender differences in the extensibility of the plantar flexor
muscles have been reported by Gajdosik et al. (15) and
Riemann et al. (42). These studies showed that the MTS was
greater through the entire ROM (15) and at 10°dorsiflexion
(42) for the men than for the women, respectively. The
present findings are unique, however, in that only 1 previous
study has examined the passive musculotendinous properties
and responses to an acute bout of stretching in men and
women (15). Our study further delineated the gender
differences by controlling for birth control and menses in
the women. Therefore, our results extended the findings of
Gajdosik et al. (15) and Riemann et al. (42) and suggested
that gender differences can be observed in ROM measure-
ments after a bout of stretching, which may be related to
fundamental hormonal differences.
A few hypotheses have been proposed to explain the
gender differences in neuromuscular properties and visco-
elastic changes. These include fluctuations in hormone levels,
discrepancies in muscle cross-sectional area (CSA) and
anthropometry, and differences in passive properties such
as viscoelastic stress relaxation or viscoelastic creep. Many
studies have examined the effect of estradiol and progesterone
on active MTS and anterior cruciate ligament (ACL) laxity
throughout the menstrual cycle with equivocal findings
(13,21,41,43,50). When a change in MTS or ACL laxity was
observed across the menstrual cycle, it was generally at or
near ovulation when estradiol levels peak (13,21,41,43,50).
Therefore, because we tested during menses when estradiol
levels are lowest, the observed gender differences may have
been even greater if we had tested at or near ovulation.
Several studies also have reported strong positive correla-
tions between muscle CSA and MTS (7,10,16,32,46). Men
generally have a greater muscle mass than do women, which
is believed to result in higher MTS values. In agreement with
our findings, many authors have shown that before or
without stretching intervention, men have higher passive
and active MTS values than do women (6–8,10,19,39,40,42).
However, after accounting for body weight, body mass, or
limb size, no differences were observed in MTS between
genders (7,8,19,39,40). In addition, it has been suggested that
the viscoelastic creep response differs between genders (28),
which is a tissue response that occurs during constant-torque
stretching. Similarly, Gajdosik et al. (15) reported gender
differences in viscoelastic stress relaxation during a 60-second
static stretch, which suggested that men and women may
respond differently to stretching.
Overall, the results of the present study indicated that
an acute bout of passive stretching increased ROM for the
women, but not for the men. In addition, there were no
changes in MTS, which is commonly used to assess the
viscoelastic properties of the muscle. It has been suggested
that a decrease in MTS reduces the total amount of strain
through a given ROM, which may reduce the risk of strain
injuries (44). If the goal of the stretching intervention is to
increase ROM and decrease MTS, the findings of this study
indicated that men may have to stretch at a higher intensity
or longer duration to achieve the same increases in ROM as
women. In contrast, a stiffer MTU is thought to be advan-
tageous, because it can better withstand rapid and large forces
compared to a compliant system, thus reducing the likelihood
of ligamentous injury (42). For women, who are at a 2–8 times
greater chance of sustaining an ACL injury than men (1),
maintaining MTS may be an important factor in reducing this
risk. Because MTS was not decreased after stretching, these
findings indicate that, although it is unknown if stretching
affects the risk of injury, it may be a safe treatment before
competition. However, future research is necessary to de-
termine when the stretching is applied before performance
and how long the changes in ROM may last.
PRACTICAL APPLICATIONS
The findings of this study suggested that passive stretching
increased ROM for the women but not for the men, but there
were no changes in MTS. Thus, the women experienced
increases in stretch tolerance but not changes in muscle
stiffness. Practitioners who use stretching may want to
consider the possible gender differences in passive stretching
responses and that increases in ROM may not always reflect
decreases in MTS. Therefore, men may have to stretch for
a longer duration or at a greater intensity to achieve similar
increases in ROM as women. It is important for coaches and
athletes to know that this type of stretching may not always
result in the desired effects (increases in ROM or decreases in
MTS).
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... A previous study found a significantly greater decrease in tendon stiffness in women than in men after 5 min stretching [11]. However, long-duration stretching (9 sets of 135 s) only increased ROM in women, while no significant changes in MTS were found in either men or women [12]. The authors suggested that the stretch reflex may have occurred during the measurement of MTS, which may explain why MTS did not change. ...
... The healthy volunteers had no current neuromuscular or musculoskeletal disorders of the lower limbs. The women were included only if they had normal menstrual cycles and reported not having taken hormonal contraceptives for the past 3 months [12,20]. All participants were asked to refrain from intensive exercise and alcohol and caffeine consumption for 24 h prior to commencing the study. ...
... Surface electromyography (Noraxon USA, Inc., Scottsdale, AZ, USA) was used to monitor the contraction of the gastrocnemius muscle. The bipolar electrodes were placed 20 mm apart on the belly of the medial gastrocnemius muscle [12]. Practice sessions were performed twice prior to measurement. ...
Article
Full-text available
Purpose Musculotendinous stiffness (MTS) measurement is valuable for assessing stretch-induced effects for sports injury prevention. There is no consensus on whether there are sex-related differences in MTS reduction by stretching, and no effective stretching protocol exists. We aimed to investigate the sex-related differences in stretch-induced MTS changes. Methods Fifteen healthy men (22.0 ± 1.0 years) and fifteen healthy women (22.3 ± 1.1 years) performed stretching of the ankle plantar flexors for four sets of 30 s each. MTS was measured before and after each set of stretching. Results A significant two-way interaction (time × sex) was found for MTS (p = 0.021). MTS significantly decreased after one set of stretching in men (p = 0.024) and after three sets in women (p = 0.001). MTS after one and four sets of stretching was significantly higher in men than in women (p = 0.038 and p = 0.019, respectively). Conclusion Fewer stretching sets are needed for men compared with that required for women to decrease MTS, and the MTS change is greater for men. Thus, the patient’s sex should be considered when designing an optimum stretching protocol.
... Most existing research has focused on using highintensity stretching for muscle elongation. Previous studies examining increased flexibility after stretching have shown that the increase in flexibility in females is comparable or superior to that in males [12][13][14]. This is likely because females have relatively lower musculotendinous stiffness than males, making them more likely to experience an increased range of motion [12]. ...
... Previous studies examining increased flexibility after stretching have shown that the increase in flexibility in females is comparable or superior to that in males [12][13][14]. This is likely because females have relatively lower musculotendinous stiffness than males, making them more likely to experience an increased range of motion [12]. However, little research has been conducted on the effects of specific warm-up performed at a relatively low intensity compared with stretching. ...
... Finally, participants were limited to healthy males. Sexrelated differences exist in the effects of stretching caused by sex hormones [45]. Therefore, further studies are required to investigate the effects of DS in participants of different ages and sexes. ...
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Dynamic stretching (DS) is performed as a warm-up to improve the range of motion and athletic performance. However, the effect of different amounts of DS on muscle performance remains unclear. This study investigated the effects of DS repetitions with one or four sets of 30 s on musculotendinous extensibility and muscle strength. Fourteen healthy men (23.6 ± 1.5 years) underwent DS to ankle plantar flexors for one set (fifteen repetitions) or four sets after warm-up. The maximal ankle dorsiflexion angle, musculotendinous stiffness (MTS), passive torque, peak plantarflexion torque during maximal isometric contraction, and muscle temperature were measured before and after stretching. A significant effect of time was observed on the maximal ankle dorsiflexion angle, MTS, passive torque, and muscle temperature (p < 0.001). However, no interactions or effects between the conditions were observed. After DS, the maximal ankle dorsiflexion angle and muscle temperature significantly increased (p < 0.01), while the MTS and passive torque significantly decreased (p < 0.01). The maximal muscle strength showed no significant effects or interactions (p = 0.198−0.439). These results indicated that one and four sets of DS effectively increased musculotendinous extensibility. Thus, one set of DS may have similar effects as a warm-up before four sets of DS.
... There are isolated reports of a greater likelihood of increased foot dorsiflexion in women following exercise [27]. A number of researchers have highlighted the effectiveness of activity to increase the range of motion in the joints, but they either found no differences between the genders or have not examined such differences [28][29][30][31][32]. ...
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Background The aim of the study was to assess factors affecting the popliteal angle and foot dorsiflexion, in particular gender. The subjects were 142 students from the 2nd and 3rd year of Poznań junior high schools. Methods The participants included 57 girls and 87 boys. Three raters examined each subject: a specialist in orthopaedics, a resident doctor and a physical therapy student. Foot dorsal flexion was tested in a supine position with lower limbs extended. Next, dorsal flexion was evaluated with the knee and hip in 90 degrees of flexion. Finally, a passive knee extension (PKE) test was carried out. The significance of the PKE test is that the lower the angle the more flexible the hamstrings. This is because the PKE measurement is the distance to the right angle, that is a full knee extension with the hip flexed. Results The non-parametric test (Mann–Whitney) and the Student’s t-test showed differences between the female and male gender in the measurements of the popliteal angle (p < .05000). The correlation was negative, which means that the hamstrings are more flexible in girls. No differences were found between gender and passive foot dorsiflexion and dorsiflexion with a flexed hip and knee. No differences were found between the group with the extended PE curriculum and the group with the standard number of PE classes in the range of motion of foot dorsiflexion and the value of the popliteal angle. Conclusions Girls between 13 and 15 years old have a significantly larger hamstring flexibility, which is confirmed by the tests of the popliteal angle. No differences were found in dorsiflexion between girls and boys who have not been trained using a training model.
... Moreover, it is also unclear whether prescribing eccentric exercise is effective for older women, as they tend to be less viable in strength exercises than men, 19 and sex should be considered when observing the sensation or viscoelastic property changes in response to stretching exercise. 20 Furthermore, while there may be benefits associated with the three home-based interventions for functional performance, it is unclear how long these effects may last. ...
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Background Joint inflexibility is acknowledged as a significant contributor to functional limitations in the older adult, with lengthening-type exercises identified as a potential remedial approach. Nevertheless, the responses to eccentric exercise in female older adults have not been extensively studied especially in home-based environment. Here, we aimed to assess the effectiveness of home-based static stretching (ST), dynamic closed-chain stretching (DCS), or eccentric exercise (ECC) interventions on flexibility, musculotendinous architecture, and functional ability in healthy older women. Methods We randomly assigned 51 healthy older women (age 65.9 ± 3.4 years) to one of three interventional exercise groups: DCS (N = 17), ECC (N = 17), or ST (N = 17). The training was performed 3 times a week for 6 weeks. The participants’ musculotendinous stiffness, fascicle length, eccentric strength, and functional capacities were measured before the intervention, after 6 weeks of exercise, and at a 1-month follow-up. Results The results showed that all three interventions improved hamstring flexibility and passive ankle dorsiflexion (p < 0.001), with increased biceps femoris and medial gastrocnemius fascicle length (p < 0.01). However, there was no significant change in musculotendinous stiffness. The ECC intervention produced a greater improvement in knee flexor and calf eccentric peak torque (p < 0.05), and gait speed (p = 0.024) than the other two interventions. The changes in flexibility and knee flexor strength remained for up to 4 weeks after detraining. Conclusion In conclusion, the present study suggests that home-based ECC may be more beneficial in enhancing physical capacities in older women compared with either DCS or SS interventions.
... Previous studies reported that women exhibit greater joint flexibility and lower stiffness than men (Morse, 2011). Conversely, Hoge et al. (2010) reported no significant sex differences in the stretch-induced reduction of stiffness, suggesting that the stretching effects might be comparable between sexes. Therefore, the influence of sex on the results in this study is likely to be negligible. ...
... There are isolated reports of a greater likelihood of increased foot dorsi exion in women following exercise (24). ...
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Full-text available
Background: The aim of the study was to assess factors affecting the popliteal angle and foot dorsiflexion, in particular gender. The subjects were 142 students from the 2nd and 3rd year of Poznań junior high schools. Methods: The participants included 57 girls and 87 boys. Three raters examined each subject: a specialist in orthopaedics, a resident doctor and a physical therapy student. Foot dorsal flexion was tested in a supine position with lower limbs extended. Next, dorsal flexion was evaluated with the knee and hip in 90 degrees of flexion. Finally, a passive knee extension (PKE) test was carried out. The significance of the PKE test is that the lower the angle the more flexible the hamstrings. This is because the PKE measurement is the distance to the right angle, that is a full knee extension with the hip flexed. Results: The non-parametric test (Mann-Whitney) and the Student’s t-test showed a correlation between the female gender and the popliteal angle (p <.05000). The correlation was negative, which means that the hamstrings are more flexible in girls. No correlation was found between gender and passive foot dorsiflexion and dorsiflexion with a flexed hip and knee. Conclusions: Girls between 13 and 15 years old have a significantly larger hamstring flexibility, which is confirmed by the tests of the popliteal angle. No differences were found in dorsiflexion between girls and boys who have not been trained using a training model.
... Baseline measures of flexibility are commonly reported to be greater for women than men [62][63][64][65][66][67][68], which may be partially attributed to differences in muscle mass, joint geometry, and higher musculotendinous stiffness in men [9,16,69]. Hoge et al. [70] reported that following nine passive SS repetitions of 135-s each, ROM increased for the women but not for the men. Not all studies illustrate female flexibility superiority. ...
Article
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Background Although stretching can acutely increase joint range of motion (ROM), there are a variety of factors which could influence the extent of stretch-induced flexibility such as participant characteristics, stretching intensities, durations, type (technique), and muscle or joint tested. Objective The objective of this systematic review and meta-analysis was to investigate the acute effects of stretching on ROM including moderating variables such as muscles tested, stretch techniques, intensity, sex, and trained state. Methods A random-effect meta-analysis was performed from 47 eligible studies (110 effect sizes). A mixed-effect meta-analysis subgroup analysis was also performed on the moderating variables. A meta-regression was also performed between age and stretch duration. GRADE analysis was used to assess the quality of evidence obtained from this meta-analysis. Results The meta-analysis revealed a small ROM standard mean difference in favor of an acute bout of stretching compared to non-active control condition (ES = −0.555; Z = −8.939; CI (95%) −0.677 to −0.434; p < 0.001; I2 = 33.32). While there were ROM increases with sit and reach (P = 0.038), hamstrings (P < 0.001), and triceps surae (P = 0.002) tests, there was no change with the hip adductor test (P = 0.403). Further subgroup analyses revealed no significant difference in stretch intensity (P = 0.76), trained state (P = 0.99), stretching techniques (P = 0.72), and sex (P = 0.89). Finally, meta-regression showed no relationship between the ROM standard mean differences to age (R2 = −0.03; P = 0.56) and stretch duration (R2 = 0.00; P = 0.39), respectively. GRADE analysis indicated that we can be moderately confident in the effect estimates. Conclusion A single bout of stretching can be considered effective for providing acute small magnitude ROM improvements for most ROM tests, which are not significantly affected by stretch intensity, participants’ trained state, stretching techniques, and sex.
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Although stretching exercises can prevent muscle injuries and enhance athletic performance, they can also cause injury. The author explains the four most common types of stretching exercises and explains why he considers static stretching the safest. He also sets up a stretching routine for runners. In setting up a safe stretching program, one should precede stretching exercises with a mild warm-up; use static stretching; stretch before and after a workout; begin with mild and proceed to moderate exercises; alternate exercises for muscle groups; stretch gently and slowly until tightness, not pain, is felt; and hold the position for 30 to 60 seconds.
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The purpose of this study was to compare the dynamic elastic and static viscoelastic stress-relaxation (VSR) properties of the calf muscle-tendon unit (MTU) between men and women. A Kin-Com® dynamometer moved the ankle of 15 men and 14 women (age range 23-35 years) from plantarflexion to maximal dorsiflexion (DF) at 5°/s with negligible surface electromyogram activity to measure the dynamic passive elastic properties. The ankle was then moved to three DF angles defined at 100%, 90% and 80% of the maximal DF force and held for 60 s each to measure the static VSR as the torque decline. ANOVA procedures indicated that the men had greater absolute dynamic maximal passive DF torque, full stretch mean torque, absorbed passive elastic energy (area under the curve) and passive elastic stiffness through the full stretch and through the last 10° of the stretch (P ≤ 0.014). All but the full stretch stiffness remained significantly greater when controlled for body mass (P ≤ 0.042). The absolute torque decline for the three static stretches showed significant group, time and interaction effects (P < 0.001). The percent torque decline during the first 15 s of static stretch, normalized to the total percent decline (100%), was greater for men at the 90% (P = 0.049) and 80% (P = 0.036) stretch angles. The results indicated that the calf MTU of men has greater dynamic elastic and static VSR properties than women, which may influence ambulatory functional activities and adaptations to therapeutic stretching.
Conference Paper
Aim. To elucidate the hormonal influences on sex differences in knee joint behavior, normal-menstruating females were compared to males on serum hormone levels and anterior knee joint laxity (displacement at 46N, 89N and 133N) and stiffness (Linear slope of ΔForce/ΔDisplacement for 46-89N and 89-133N) across the female menstrual cycle. Methods. Twenty-two females were tested daily across one complete menstrual cycle, and 20 males were tested once per week for 4 weeks. Five days each representing the hormonal milieu for menses, the initial estrogen rise near ovulation, and the early and late luteal phases (total of 20 days) were compared to the average value obtained from males across their 4 test days. Results. Sex differences in knee laxity were menstrual cycle dependent, coinciding with significant elevations in estradiol levels. Females had greater laxity than males on day 5 of menses, days 3-5 near ovulation, days 1-4 of the early luteal phase and days 1, 2, 4 and 5 of the late luteal phases. Within females, knee laxity was greater on day 5 near ovulation compared to day 3 of menses, and days 1-3 of the early luteal phase compared to all days of menses and day 1 near ovulation. On average, differences observed between sexes were greater than those within females across their cycle. There were no differences in anterior knee stiffness between sexes or within females across days of the menstrual cycle. Conclusion. These results suggest sex hormones may be a primary mediator of the observed sex differences in knee laxity.
Article
The relationship between hamstring muscle stiffness and the functional ability level of 17 subjects with complete anterior cruciate ligament rupture confirmed at arthroscopy was examined. The hamstring muscles were modelled as a single degree of freedom mass spring system with a damping component. Using this model the stiffness of these muscles was examined at 30, 45, and 60% of a maximum voluntary isometric muscle action. The functional ability of the subjects, attained using the Noyes knee rating system, was then correlated to muscle stiffness measures. Positive correlations of 0.71, 0.72, and 0.62 at the three respective muscle loading levels were observed. These findings suggested that hamstring muscle stiffness may have an important role to play in the functional ability of subjects with anterior cruciate ligament deficiency. At this time there is no single effective treatment for all individuals with anterior cruciate ligament deficiency. Those individuals who undergo a conservative management programme are usually treated with hamstring muscle exercises for improving knee flexion strength. The current study provides evidence that hamstring exercises may alter other properties of muscles, such as their active stiffness, which in turn may influence the functional ability of the anterior cruciate ligament deficient individual.
Article
This study examined the passive compliance and length of the hamstring muscles of 15 healthy men and 15 healthy women (ages 21-37) with passive straight-leg-raising between 65° and 80°. Subjects were positioned on their left sides with the pelvis stabilized and the right thigh fixed at 90° on a horizontal platform. After three practice trials of maximal passive knee extension, subjects received three trials for data collection. Muscle activity was monitored with surface EMG and passive resistance to knee extension was measured with a dynamometer as the limb was photographed at six force-dependent positions. The passive compliance was computed as the ratio of the change in the knee angle (ΔAngle) to the change in passive torque (ΔTorque), (ΔAngle/ΔTorque). Hamstring muscle lengths were measured simultaneously. An ANovA revealed a difference (P = 0·001) between the passive compliance ratios of the men (1·4 ± 0·-03) and women (2·2 ± 0·08) but not between their initial knee angles or their maximal knee angles. Independent t-tests showed a difference (P < 0·001) between the maximal passive torque of the men (41·4 ± 5·7 Nm) and women (27·4 ± 7·7 Nm). The torques were not different when standardized to body mass. Although ANOVAS showed that the absolute hamstring muscle lengths differed between genders, they were not different when standardized as a percentage of the femur length.