Download Active muscle stiffness in the human medial gastrocnemius muscle

J Appl Physiol 117: 1020–1026, 2014.
First published August 28, 2014; doi:10.1152/japplphysiol.00510.2014.
Active muscle stiffness in the human medial gastrocnemius muscle in vivo
Keitaro Kubo
Department of Life Science, University of Tokyo, Meguro, Tokyo, Japan
Submitted 12 June 2014; accepted in final form 26 August 2014
plantar flexors; fascicle; tendon; ultrasonography
THE MECHANICAL PROPERTIES of both muscles and tendons are
known to be important determinants of their functional characteristics. Most of the information available on the mechanical properties of the human muscle-tendon complex in vivo has
been obtained using the damped oscillation technique (29, 33),
quick-release method (13, 21), and short-range stretch experiments (1, 2, 30). However, these methodologies cannot assess
the mechanical properties of muscles and tendons separately.
In the last decade, several studies have used ultrasonography to
investigate the plasticity and adaptability of human tendon
structures in vivo (e.g., Refs. 15, 22). Other studies demonstrated the mechanical properties of human muscle under
passive conditions (e.g., Ref. 24). To date, it is difficult to
noninvasively assess the mechanical properties of human muscle in vivo under active conditions.
Morgan (23) developed the alpha method, which assumed
that the series elastic component of the muscle-tendon complex
was modeled as two springs connected in series, one representing the compliance of a torque-dependent component (i.e.,
Address for reprint requests and other correspondence: K. Kubo, Dept. of
Life Science (Sports Sciences), The University of Tokyo, Komaba 3-8-1,
Meguro-ku, Tokyo 153-8902, Japan (e-mail: [email protected]).
1020
muscle), and the other a torque-independent component (i.e.,
tendon). Cook and McDonagh (3) on the first dorsal interosseous muscle and Svantesson et al. (31) on the plantar flexor
muscles applied the alpha method with electrostimulation.
Unfortunately, these studies using electrostimulation included
some drawbacks, e.g., pain and low intensity of force exerted.
To overcome these limitations, Foure et al. (5) adapted the
alpha method during submaximal voluntary contractions [from
30 to 90% maximal voluntary contraction (MVC)], and demonstrated plyometric and eccentric training-induced changes in
both active (i.e., muscle) and passive (i.e., tendon) stiffness in
the series elastic component (4, 6). However, we must note the
limitation of this technique. The alpha method assumed that
tendon stiffness remained constant; however, this has been
rejected by studies using ultrasonography (e.g., Ref. 18). Furthermore, previous findings indicated that changes in the joint
angle did not necessarily correspond to those in muscle fiber
length (e.g., Ref. 7). Therefore, length changes in muscle fibers
need to be directly determined during short-range stretching to
assess active muscle stiffness in vivo.
The aims of this study were to 1) directly assess active
muscle stiffness according to actual length changes in muscle
fibers (fascicles) during short range stretching; and 2) compare
actual measured active muscle and tendon stiffness using
ultrasonography with estimated active (i.e., muscle) and passive (i.e., tendon) stiffness in the series elastic component by
the alpha method. I hypothesized that actual measured muscle
and tendon stiffness using ultrasonography may not be related
to the values calculated by the alpha method.
METHODS
Subjects. Twenty-four healthy men (age: 22.2 ⫾ 3.6 yr, height:
172.3 ⫾ 5.5 cm, body mass: 66.4 ⫾ 8.1 kg, mean ⫾ SD) volunteered
for this study. Subjects were physically active, but had not participated in any organized program of regular exercise for at least 1 yr
before testing. They were fully informed of the procedures to be
utilized, as well as the purposes of the study. Written, informed
consent was obtained from all subjects. This study was approved by
the Ethics Committee for Human Experiments, Department of Life
Science (Sports Sciences), University of Tokyo.
Passive muscle stiffness during slow stretching. A specially designed dynamometer (Applied Office, Tokyo, Japan) was used to
measure external torque and ankle joint angles. Before the measurements, subjects sat on a chair to acclimate to the laboratory conditions
for 20 min. All measurements were performed on the right lower limb.
Subjects lay prone on a test bench, and their waist and shoulders were
secured by adjustable lap belts and held in position. The right ankle
joint was set at 100° (with the foot perpendicular to the tibia ⫽ 90°
with angles more than 90° being in plantar flexion) with the knee joint
at full extension, and the foot was securely strapped to a foot plate
connected to the lever arm of the dynamometer. Subjects did not
warm up before the stretch maneuver. The platform of the dynamometer, which was attached to the sole of the subject’s foot, was moved
from 100 to 80°, with a constant velocity of 5°/s. During slow
stretching, subjects were requested to relax completely and not offer
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Kubo K. Active muscle stiffness in the human medial gastrocnemius muscle in vivo. J Appl Physiol 117: 1020 –1026, 2014. First
published August 28, 2014; doi:10.1152/japplphysiol.00510.2014.—
The aims of this study were to 1) directly assess active muscle
stiffness according to actual length changes in muscle fibers (fascicles) during short range stretching; and 2) compare actual measured
active muscle and tendon stiffness using ultrasonography with the
stiffness of active (i.e., muscle) and passive (i.e., tendon) parts in
series elastic component of plantar flexors using the alpha method.
Twenty-four healthy men volunteered for this study. Active muscle
stiffness in the medial gastrocnemius muscle was calculated according
to changes in estimated muscle force and fascicle length during fast
stretching after submaximal isometric contractions [10, 30, 50, 70,
and 90% maximal voluntary contractions (MVC)]. Using the variables
measured during this fast stretch experiment, the stiffness of active
(i.e., muscle) and passive (i.e., tendon) parts in plantar flexors was
assessed using alpha method. Tendon stiffness was determined during
isometric plantar flexion by ultrasonography. Active muscle stiffness
increased with the exerted torque levels. At 30, 50, 70, and 90%
MVC, there were no significant correlations between muscle stiffness
using ultrasonography and stiffness of active part (i.e., muscle) by
alpha method, although this relationship at 10% MVC was significant
(r ⫽ 0.552, P ⫽ 0.005). In addition, no correlation was noted in
tendon stiffness between the two different methods (r ⫽ 0.226, P ⫽
0.209). The present study demonstrated that ultrasonography could
quantified active muscle stiffness in vivo. Furthermore, active muscle
stiffness and tendon stiffness using ultrasonography were not related
to active (i.e., muscle) or passive (i.e., tendon) stiffness in series
elastic component of plantar flexors by alpha method.
any voluntary resistance. To minimize thixotropic effects as preconditioning (12, 26), we collected data during the sixth cycle after five
cycles. Passive torque (TQ) during slow stretching was detected by
the dynamometer. The TQ measured by the dynamometer during slow
stretch was converted to muscle force (Fm) using the following
equation:
A
Fm ⫽ k · Ft
Ft ⫽ TQ · MA⫺1
Angular velocity
-1)
B
Torque (Nm)
C
•
1021
Kubo K
100
95
90
85
80
-100 -80 -60 -40 -20
0
20
40
60
80 100
0
20
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80 100
0
20
40
60
80 100
250
150
50
-50
-100 -80 -60 -40 -20
150
100
50
-100 -80 -60 -40 -20
Time (ms)
Fig. 1. Typical examples of changes in the ankle joint angle (A), angular
velocity (B), and torque (C) during the short-range stretch experiment. The left
vertical dotted line represents the stretch onset. The first 60 ms (right vertical
dotted lines) of the stretch was used to calculate active muscle stiffness.
active stretch trials (2). Short-range stretching was performed at five
levels of the submaximal torque in a random order (two tests at each
20% MVC from 10 to 90% MVC) with the visual aid of exerted
torque on an oscilloscope. The measured values were the means of
two trials.
During the short-range stretch experiment, fascicle length in the
medial gastrocnemius muscle was determined using a real-time ultrasonic apparatus (Fig. 2). Ultrasonic images were stored at 98 Hz in the
computer memory of the apparatus (32). An electric signal was
superimposed on the images to synchronize them to the torque, joint
angle, and EMG activity (see below). The location of the probe,
analysis of fascicle length, and calculated muscle force were similar to
those for the measurement of passive muscle stiffness, as described
above. The slope of the muscle force-fascicle length curve between
100 and 92° was defined as active muscle stiffness.
The repeatability of active muscle stiffness was investigated on
2 separate days in a preliminary study with nine young men. No
significant differences were observed between the test and retest
values of active muscle stiffness for the measured torque levels
(10, 30, 50, 70, and 90% MVC). The test-retest correlation coefficient (r) and the coefficients of variance were 0.911 and 11.8%
for 10% MVC, 0.870 and 10.4% for 30% MVC, 0.865 and 10.3%
for 50% MVC, 0.888 and 10.9% for 70% MVC, and 0.846 and
10.5% for 90% MVC, respectively.
Muscle and tendon stiffness by the alpha method. Previous studies
(3, 5, 23) reported that the alpha method could separate muscle-tendon
complex stiffness into two components. Joint compliance (i.e., the
inverse of joint stiffness) was considered as the compliance of two
springs placed in series, one representing the compliance of a torquedependent component (muscle stiffness), and the other a torqueindependent component (tendon stiffness). The inverted force and
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where Ft and k represent the tendon force and relative contribution
of the physiological cross-sectional area of the medial gastrocnemius muscle within plantar flexor muscles (8), respectively, and
MA is the moment arm length of the triceps surae muscles at 90°
of the ankle joint, which is estimated from the lower leg length of
each subject (10).
During slow stretching, a real-time ultrasonic apparatus (SSD6500, Aloka, Japan) was used to record continuously longitudinal
ultrasonic images of the medial gastrocnemius muscle. At 30% of the
distance from the center of the malleolus lateralis to the articular cleft
between the femur and tibia condyles, the scanning probe (7.5-MHz
wave frequency with an 80-mm scanning length; UST 5047-5, Aloka,
Tokyo, Japan) of the apparatus was secured with adhesive tape on the
skin. Ultrasonic images were recorded on a videotape at 30 Hz and
synchronized with recordings of a clock timer for subsequent analysis.
Fascicle length was defined as the distance between the insertion of
the fascicle into the superficial and deep aponeurosis. In the present
study, the fascicle length was measured five times for the same
images. The average value of the three measurements, excluding the
largest and the smallest values, was proposed and used as a representative value. The coefficient of variation of three measurements
ranged from 0 to 4.1%.
TQ, joint angle, fascicle length, and electromyographic (EMG)
activity in the triceps surae muscles (see below) were continuously
recorded over the entire range of stretch maneuvers. The slope of the
portion of the passive muscle force-fascicle length curve, from 100 to
92°, was defined as passive muscle stiffness.
The repeatability of passive muscle stiffness measurements was
investigated on 2 separate days in a preliminary study with nine young
men. No significant differences were observed between the test and
retest values for passive muscle stiffness. The test-retest correlation
coefficient (r) and coefficients of variance were 0.89 and 5.6%,
respectively.
Active muscle stiffness using ultrasonography during fast stretching. The posture of the subject and setup were similar to that for the
measurement of passive muscle stiffness, as described above. After a
standardized warm-up, the subjects performed two or three isometric
MVCs at 100° of the ankle angle. The peak torque was recorded in
every trial, and the highest MVC value (121.0 ⫾ 23.1 N·m) was used
to determine the target torque during the short-range stretch experiment (see below). Maximum dorsiflexion was also performed at the
same ankle angle to normalize the antagonist muscle activation with
respect to MVC (see below).
After a 5-min rest period, subjects performed the short-range
stretch experiment using a previously described procedure (5). The
ankle ergometer was programmed to apply dorsiflexion stretches from
100 to 80°. Subjects were instructed to relax as soon as ankle motion
was perceived. A 60-ms period after the stretch was analyzed, because
this time period was chosen to avoid any potential neural effects (1, 2,
5). During this period (60 ms), the range of motion was ⬃8°, and the
angular velocity reached ⬃250°/s (Fig. 1). Before the experiment,
subjects performed a familiarization to the short-range stretch experiments at 50% MVC. An additional measurement was conducted two
times at 0% MVC (relaxed condition) before the short range stretch
experiment for data correction purposes (see below). The averaged
torque during the relaxed condition (caused by inertia and passive
elasticity) was subtracted from the measured torque during each of the
Ankle angle (deg)
Measurement of Active Muscle Stiffness
1022
Measurement of Active Muscle Stiffness
A
100 deg
•
Kubo K
C
96.5 deg
D
92 deg
MG
Fig. 2. Typical sequence longitudinal ultrasonic images of the medial gastrocnemius
(MG) muscle during the short-range stretch
experiment. A–D: 100, 99, 96.5, and 92°, respectively. In each image, the pennation of
fascicle is identifiable as the diagonal striations running across the muscle from the deep
to the superficial aponeurosis. SOL, soleus.
See text for a more detailed explanation.
SOL
B
99 deg
change in length (from a calculated change in length of 7 mm of the
total muscle-tendon complex during 60 ms) divided by the change in
force were plotted for each torque level (Fig. 1 of Ref. 3). The slope
calculated from this plot was defined as passive part (i.e., tendon)
stiffness. Active part (i.e., muscle) stiffness values at each torque level
were calculated by subtracting tendon stiffness from the total stiffness
of the muscle-tendon complex (3, 5, 23).
Stiffness of tendon structures using ultrasonography. The posture
of the subject (except for the ankle angle) and procedure used were
similar to those for the measurement of passive muscle stiffness, as
described above. The right ankle joint was set at 90° (anatomical
position) with the knee joint at full extension. Before the test, the
subject performed a standardized warm-up and submaximal contractions to become accustomed to the test procedure. Subjects were
instructed to develop a gradually increasing force from a relaxed state
to MVC within 5 s. The task was repeated two times per subject with
at least 3 min between trials. A real-time ultrasonic apparatus was
used to obtain a longitudinal ultrasonic image of the medial gastrocnemius muscle during the contraction. The tester visually confirmed
echoes from the aponeurosis and fascicles. The point at which one
fascicle was attached to the aponeurosis was visualized on the
ultrasonic image. This cross-point moved proximally during the
development of isometric torque up to the maximum (Fig. 1 of Ref.
15). Displacement of the cross-point was considered to indicate the
lengthening of tendon structures (deep aponeurosis and distal
tendon) (16, 18).
Tendon displacement has been attributed to both angular rotation
and contractile tension, because any angular joint rotation occurs in
the direction of ankle plantar flexion during an “isometric” contraction
(e.g., Ref. 22). To monitor ankle joint angular rotation, an electrical
goniometer (Penny and Giles, Biometrics, Gwent, UK) was placed on
the lateral aspect of the ankle. Additional measurements were made
under passive conditions to correct the measurements taken for the
elongation of tendon structures. Displacement of the cross-point
caused by rotation of the ankle from 100 to 80° was digitized in the
sonographs taken, as described above. Thus displacement of the
cross-point obtained from the ultrasound images of each subject could
be corrected for that attributed to joint rotation alone (e.g., Ref. 22).
Only values corrected for angular rotation have been reported in the
present study.
Torque measured by the dynamometer during isometric plantar
flexion was converted to muscle force by the same procedure used to
measure passive muscle stiffness (see above). In this study, muscle
force and elongation of the tendon structures above 50% of MVC
were fit to a linear regression equation, the slope of which was
adopted as tendon stiffness (16, 18). The reliability of tendon stiffness
measurements using ultrasonography has been confirmed in our previous studies (16, 18).
EMGs. EMG activity was recorded during the measurements of
passive muscle stiffness (slow stretch), active muscle stiffness (fast
stretch), and tendon stiffness (ramp isometric contraction). Bipolar
surface electrodes (5 mm in diameter) were placed over the bellies of
the medial gastrocnemius, lateral gastrocnemius, soleus, and tibial
anterior muscles with a constant interelectrode distance of 25 mm.
EMG signals were transmitted to a computer at a sampling rate of 1
kHz. EMG values were normalized to the values obtained during
MVC for a 100-ms period before and after the stretch (4). EMG was
also full-wave rectified and averaged over two different phases, a
60-ms period just before the stretch (mEMGa) and a 60-ms period
after the stretch (mEMGb).
Statistics. Descriptive data included means ⫾ SD. A one-way
ANOVA was used to detect significant effects of torque level
(%MVC) on increments in force, changes in fascicle length, and
active muscle stiffness. If the F-statistic of the analysis of variance
was significant, differences between means were assessed using the
Tukey post hoc test. Before the ANOVA analysis, Mauchly’s sphericity test was performed to assess homogeneity of variance and
covariance. Greenhouse-Geisser correction was used to adjust the
degree of freedom, when phericity assumption was violated. A linear
regression analysis was performed on the relationship between the
measured variables. The level of significance was set at P ⬍ 0.05.
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10 mm
Measurement of Active Muscle Stiffness
***
***
***
40
***
20
0
10%
Active muscle stiffness
-1)
50%
70%
90%
4
800
***
600
*
400
***
***
200
0
10%
*
3
30%
50%
%MVC
70%
90%
Fig. 4. Active part stiffness by the alpha method during the short-range stretch
experiment. Values are means ⫾ SD. Significant difference from the preceding
torque level exerted: *P ⬍ 0.05, ***P ⬍ 0.001.
2
1
0
C
30%
5
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Kubo K
10%
30%
50%
70%
90%
120
**
100
**
80
***
60
***
40
method also increased as the torque levels exerted became
higher (P ⬍ 0.001, Fig. 4).
No significant relationships were observed between active
muscle stiffness using ultrasonography and active part (i.e.,
muscle) stiffness by the alpha method at 30, 50, 70, and 90%
MVC, whereas this relationship at 10% MVC was significant
(r ⫽ 0.552, P ⫽ 0.005; Fig. 5). No correlation was noted in
tendon stiffness between the two different methods (r ⫽ 0.226,
20
0
10%
30%
50%
70%
The increase in torque during stretching was enhanced as the
torque levels exerted became higher (P ⬍ 0.001, Fig. 3A).
Changes in the fascicle length during stretching decreased
slightly with increases in the exerted torque levels, with differences in fascicle length between 70 and 90% being significant (P ⫽ 0.047, Fig. 3B). Active muscle stiffness increased as
torque levels exerted became higher (P ⬍ 0.001, Fig. 3C). The
correlation coefficients tended to be higher for active muscle
stiffness and changes in the fascicle length than active muscle
stiffness and changes in torque at all exerted torque levels
(Table 1). Active part (i.e., muscle) stiffness by the alpha
100
600
400
r=0.552
(p<0.01)
50
Active part stiffness by alpha method (N · mm-1)
RESULTS
D
1000
800
%MVC
Fig. 3. Change in torque (A), change in fascicle length (B), and active muscle
stiffness (C) during the short-range stretch experiment. MVC, maximal voluntary contraction. Values are means ⫾ SD. Significant difference from the
preceding torque level exerted: *P ⬍ 0.05, **P ⬍ 0.01, ***P ⬍ 0.001.
A
150
90%
r=0.236
(n.s)
200
0
0
0
10
B
20
30
0
1200
300
E
50
100
1000
800
200
600
r=0.319
(n.s)
100
400
r=-0.099
(n.s)
200
0
0
0
800
C
20
40
60
0
80
r=-0.008
(n.s)
600
50
100
150
Active muscle stiffness
(N · mm-1)
400
Table 1. Correlation coefficients between active muscle
stiffness using ultrasonography and changes in toque and
fascicle length
10% MVC 30% MVC 50% MVC 70% MVC 90% MVC
Change in torque
0.594†
0.667‡ 0.439*
0.574†
0.469*
Change in fascicle length ⫺0.708‡ ⫺0.766‡ ⫺0.821‡ ⫺0.673‡ ⫺0.784‡
MVC, maximal voluntary contraction. *P ⬍ 0.05, †P ⬍ 0.01, ‡P ⬍ 0.001.
200
0
0
20
40
60
80
100
Active muscle stiffness
(N · mm-1)
Fig. 5. Relationships between active muscle stiffness using ultrasonography
and active part (i.e., muscle) stiffness by the alpha method at each torque level
exerted. A–E: 10, 30, 50, 70, and 90% MVC, respectively.
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Change in fascicle length
(mm)
B
60
Active part stiffness by alpha method
-1)
Change in torque
(Nm)
A
•
1024
Passive part stiffness by alpha method
(N · mm -1)
Measurement of Active Muscle Stiffness
600
400
200
r=0.266
(n.s)
0
0
10
20
30
40
50
Tendon stiffness by ultrasonography
(N · mm -1)
P ⫽ 0.209; Fig. 6). Passive muscle stiffness did not correlate
with active muscle stiffness at any force level (Table 2).
Short- and long-latency stretch reflexes could not be identified at any exerted torque level (Fig. 7). mEMGb was significantly higher than mEMGa at 10, 30, and 50% MVC (all P ⬍
0.001), while no significant differences were observed between
mEMGa and mEMGb at 70 and 90% MVC (P ⫽ 0.065 and
P ⫽ 0.169) (Table 3).
DISCUSSION
The main finding of this study was that active muscle
stiffness and tendon stiffness using ultrasonography were not
related to active (i.e., muscle) or passive (i.e., tendon) stiffness
in the series elastic component by the alpha method. To the
best of our knowledge, this is the first study to assess active
muscle stiffness according to actual length changes in fascicles
during short-range stretching in vivo.
When muscle stiffness is evaluated under active conditions,
the effects of the stretch reflex on the muscle stiffness measured needs to be considered. In the present study, changes in
torque and fascicle length were determined when the ankle
joint commenced movement and then 60-ms thereafter. This
time period was chosen to avoid any potential neural effects (1,
2, 5). In the present study, the neural stretch reflex could not be
identified at any of the exerted torque levels (Fig. 7). However,
mEMG values for a 60-ms period after stretching (mEMGb)
were significantly higher than those for a 60-ms period before
stretching (mEMGa) at 10, 30, and 50% MVC, while no
significant difference was observed between mEMGa and
mEMGb at the higher force levels (70 and 90% MVC) (Table
3). These results implied that a short-latency stretch reflex has
affected mEMG values, but it could not be confirmed visually.
The neural stretch reflex response is known to be enhanced
when the exerted force increases up to intermediate levels (e.g.,
Ref. 25). Moreover, previous studies demonstrated that
stretch reflex-induced stiffness decreased at high force levels (1, 30). Based on these findings, if the active muscle
stiffness values obtained in the present study included the
neural stretch reflex, they would decrease at the higher
torque levels. On the other hand, the present results showed
Kubo K
that both the increase in torque and active muscle stiffness
was enhanced as the torque levels exerted became higher
(Fig. 3, A and C). Therefore, the active muscle stiffness
values obtained in the present study were not affected by
any potential neural effects.
An interesting finding of this study was that no significant
relationships were observed between active muscle stiffness
using ultrasonography and that by the alpha method at each
torque level, except for 10% MVC. These results indicated that
changes in fascicle length could not be estimated from those in
the joint angle due to tendon compliance beyond 10% MVC.
Previous studies reported that the mechanical properties of
human tendons (i.e., stiffness, hysteresis) varied markedly
among individuals (e.g., Ref. 19). Furthermore, the correlation
coefficients tended to be higher for active muscle stiffness and
changes in the fascicle length than active muscle stiffness and
changes in torque at all exerted torque levels (Table 1). These
findings suggest that changes in fascicle length must be determined to assess active muscle stiffness in vivo. Furthermore, it
would be necessary to reconsider the more recent findings
concerning the training-induced changes in calculated muscle
stiffness by alpha method (4, 6).
Human muscle stiffness in vivo has only been examined
under passive conditions (11, 24). Using this technique, previous studies reported changes in the stiffness of the overall
muscle-tendon complex and muscle during and after various
stretching procedures (24, 27). Naturally enough, the measured
“muscle stiffness” by this technique just represented the properties of the muscle under passive conditions, but not active
conditions. “Passive” muscle stiffness is known to be influenced by a lengthening deformation in the connective tissues of
the endomysium, perimysium, and epimysium in the muscle
belly (9). Although all three components of the connective
tissue in the muscle belly contribute to resistance when a
muscle is passively stretched, the larger amount of the perimysium has been identified as the tissue that is the major contributor to extracellular passive resistance to stretch (28). In the
present study, passive muscle stiffness did not correlate with
active muscle stiffness at any torque level exerted (Table 2).
Therefore, passive and active muscle stiffness clearly represented respective mechanical properties. In future studies, we
can assess acute and chronic changes in the mechanical properties of the series elastic component (mainly active muscle
stiffness) and parallel elastic component (mainly passive muscle stiffness) within muscles separately.
The alpha method developed by Morgan (23) assumed that
tendon stiffness remained constant throughout the range of
force. However, previous studies using ultrasonography rejected this assumption. For example, Kubo et al. (18) reported
that the ratio of the estimated muscle force to tendon elongation at every 10% MVC increased curvilinearly with an increase in force. The present results revealed no correlation in
tendon stiffness between the two different methods (Fig. 6).
Table 2. Correlation coefficients between passive muscle
stiffness and active muscle stiffness using ultrasonography
Passive muscle stiffness
10%
MVC
30%
MVC
50%
MVC
70%
MVC
90%
MVC
0.062
0.199
0.240
0.252
0.203
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Fig. 6. Relationship between tendon stiffness using ultrasonography and
passive part (i.e., tendon) stiffness by the alpha method.
•
Measurement of Active Muscle Stiffness
100
•
1025
Kubo K
A
50
0
-100
100
B
-80
-60
-40
-20
0
20
40
60
80
100
-80
-60
-40
-20
0
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100
-80
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-40
-20
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-20
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-40
-20
0
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60
80
100
50
100
C
50
0
-100
100
D
50
0
-100
100
E
Fig. 7. Changes in the electromyographic (EMG) activities of
the MG (thick black line), lateral gastrocnemius (thin gray
line), SOL (thick gray line), and tibial anterior muscles (thin
black line) obtained 100 ms before and after stretching. The
vertical dotted line represented the stretch onset. A–F: 0, 10,
30, 50, 70, and 90% MVC, respectively.
50
0
-100
100
F
50
0
-100
Time (ms)
Similarly, Foure et al. (5) inferred in a preliminary study that
there was no significant correlation (n ⫽ 32, P ⬎ 0.05)
between these two parameters. As the reason for these discrepancies, Foure et al. (5) explained the differences in the assessed
structures (i.e., tendon-aponeurosis structures of the medial
gastrocnemius muscle for the ultrasonographic method, passive structures of the series elastic component for the alpha
method) and stretching velocity (i.e., low velocity for the
ultrasonographic method, high velocity for the alpha method).
Furthermore, passive part (i.e., tendon) stiffness by the alpha
method affected active part (i.e., muscle) stiffness by the alpha
method because the former was used to calculate the latter.
In the present study, I must draw the attention to large
differences in muscle and tendon stiffness values between the
two methods. The reason for these differences was attributed to
the difference in calculation of force. I used the estimated
muscle (medial gastrocnemius muscle) force for the active
muscle stiffness and tendon stiffness using ultrasonography,
because I investigated the fascicle length of the medial gastrocnemius muscle and elongation of its aponeurosis (including
outer tendon). On the other hand, the previous studies using the
alpha method used the tendon force (i.e., force exerted by the
whole plantar flexor muscles) to calculate the active (i.e.,
muscle) and passive (i.e., tendon) stiffness in the series elastic
Table 3. Electromyographic activities of the plantar flexors 60 ms before and after stretching
mEMGa
mEMGb
10% MVC
30% MVC
50% MVC
70% MVC
90% MVC
0.025 (0.013)
0.037 (0.017)*
0.056 (0.026)
0.067 (0.029)*
0.093 (0.036)
0.110 (0.046)*
0.159 (0.083)
0.169 (0.073)
0.218 (0.101)
0.228 (0.098)
Values are means (SD) in mV. mEMGa and mEMGb: electromyographic activities 60 ms before and after stretching, respectively. *Significantly different from
mEMGa: P ⬍ 0.001.
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EMG (% of maximal EMG)
0
-100
1026
Measurement of Active Muscle Stiffness
ACKNOWLEDGMENTS
We thank Fusao Akasaki and Ryosuke Akasaki (Applied Office) for
technical support in the design and construction of the device.
GRANTS
This study was supported by a Grant-in-Aid for Young Scientists (A)
(21680047 to K. Kubo) from the Japan Society for the Promotion of Science.
DISCLOSURES
No conflicts of interest, financial or otherwise, are declared by the author(s).
AUTHOR CONTRIBUTIONS
Author contributions: K.K. conception and design of research; K.K. performed experiments; K.K. analyzed data; K.K. interpreted results of experiments; K.K. prepared figures; K.K. drafted manuscript; K.K. edited and
revised manuscript; K.K. approved final version of manuscript.
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component. However, I considered that this point did not affect
the main results of this study.
In addition, there may be the heterogeneity of changes in
fascicle length within the muscle. In the present study, the
fascicle length was measured five times for the same images.
This procedure has been adopted in many previous studies
concerning the dynamics of human fascicle during exercises
(e.g., Refs. 17, 20). As far as we know, no reports have shown
site differences in fascicle length changes during dynamic
exercises. Kawakami et al. (14) reported that the fascicle length
was almost uniform throughout the human medial gastrocnemius muscle, in both relaxed and submaximal isometric contracted conditions. Therefore, I believed that the measured
fascicle length in this study represented the dynamics of all
fascicles within the medial gastrocnemius muscle.
In conclusion, the present study demonstrated that ultrasonography could quantify active muscle stiffness in vivo. Active
muscle stiffness as assessed using ultrasonography could represent a new index of physical resources. Furthermore, the present
method, as well as the measurement of tendon properties by
ultrasonography (e.g., 16), could be used to assess the relationship
between sport performance and muscle-tendon properties and
their plasticity to various interventions.
•