Download Tendinous movement of a human muscle during voluntary

Tendinous movement of a human muscle during voluntary
contractions determined by real-time ultrasonography
TETSUO FUKUNAGA,
MASAMITSU
SHINYA KUNO, YASUO KAWmMI,
Department
of Life Science, University
Tsukuba Advanced Research Alliance,
ITO, YOSHIHO
ICHINOSE,
AND SENSHI FUKASHIRO
of Tokyo, Tokyo 153, and
University of Tsukuba, Tsukuba
Fukunaga,
Tetsuo, Masamitsu
Ito, Yoshiho
Ichinose,
Shinya
Kuno, Yasuo Kawakami,
and Senshi Fukashiro.
Tendinous
movement
of a human muscle during voluntary
contractions
determined
by real-time
ultrasonography.
J.
AppZ. Physiol. M(3): 1430-1433,
1996.-The
degree of shortening or lengthening
of muscles during joint actions has not
been clarified
in humans,
although
such information
is
essential in understanding
human muscle functions.
In this
study, the tendinous
movement
of a muscle was determined
by real-time
ultrasonography
during voluntary
contractions.
The tibialis
anterior
muscle (TA) was tested in five healthy
men who performed
dorsi- and plantar
flexion movements
(shortening
and lengthening
of TA) at two frequencies
(0.1
and 1.5 Hz). The insertion
point (q) of fascicles onto the
aponeurosis
was clearly visualized
on the ultrasonogram,
and
its position relative to a fixed marker moved proximally
and
distally according to dorsi- and plantar flexion of ankle joint.
The movement
of q occurred
in phase with the angular
change of ankle joint, giving high correlations
(r = 0.93 to
0.97) between
the displacement
of q and the angle. The
displacement
of q for one radian of joint angle change, 46.5 t
1.7 (SD) mm, was comparable
to the reported moment arm of
TA. The present method has many potential
applications
in
the field of muscle physiology
and biomechanics
in humans.
305, Japan
know the behavior of a muscle-tendon
unit from observation of a joint movement. Information
on the relationship between joint angles and tendinous movement of
the muscle helps the understanding
of physiological
characteristics
of human muscles such as force-velocity
and force-length relationships.
Previous studies (2, 3) have presented estimates of
the movement
of contracting
human
elbow flexor
muscles by using X-ray photography
or needles inserted into the muscles, but these methods are invasive
in nature and applicable only to parallel-fibered
muscles.
Recently, Henriksson-Larsen
et al. (4) and Kawakami
et al. (5) have shown that fascicles and aponeuroses in
human muscles can be visualized by the use of ultrasonography.
The purpose of the present study is to
quantify
tendinous
movements
of in vivo human
muscles during dynamic voluntary actions by real-time
ultrasonography
and to determine
the relationship
between joint angles and the movement of the tendon.
METHODS
OF MUSCLE
FIBERS
result
in movements
Of
the tendon that produce joint motions. Because muscle
contraction cannot be observed easily, in vivo functions
of muscle fibers in humans have been estimated from
joint actions through
measurements
of torque and
angular velocity. However, this procedure has some
limitations
and sometimes gives inaccurate estimates
of muscle fiber behavior. One cannot get information
on
how much muscle shortening
or lengthening
occurs
during joint actions because joint actions are the results of various interactions
among anatomic factors
such as fascicles, aponeuroses or tendons of the muscle,
and muscle relative to the joint (1). By using a simple
anatomic model, the force-velocity relationship
of human elbow flexor muscles has been reported to be
similar to that of muscle fibers (12), but that similarity
is controversial
if one considers the multiple
factors
lying between muscle fibers and a joint. Especially in
pennate muscles in which fascicles are arranged diagonally to the line of pull of the muscle, it is impossible to
The subjects of this study were five healthy men. Their
physical characteristics
are presented
in Table 1. Informed
consent was obtained
from each subject before the study
began. The muscle tested in this study was the tibialis
anterior
(TA), a bipennate
muscle with fascicles attached
obliquely
onto the central (distal) aponeurosis.
The ultrasonic
apparatus
(model SSD-2000, ALOKA)
was
used with an electronic
linear array probe of 7.5MHz
wave
frequency. The scanning head was coated with water-soluble
transmission
gel, which provided
acoustic contact without
depressing
the dermal surface. The transducer
was placed
perpendicular
to the tissue interface and parallel to the tibia
located at a point 50% distal from the proximal
end of the
tibia1 bone. The experimenter
visually
confirmed
the echoes
reflected from the aponeurosis
and from interspaces
among
fascicles (5). The point at which one fascicle was attached to
the aponeurosis
(q) was visualized
on the ultrasonogram
(Fig.
1, top)*
Each subject lay supine on a bed and was requested
to
perform
dorsi- and plantar
flexion movements
(shortening
and lengthening
of TA) for 10 s at two different
frequencies
(0.1 and 1.5 H z >, with no additional
load. Real-time ultrasonic
images during contraction
were continuously
recorded on a
videotape
at 40 Hz, synchronized
with recordings
of a clock
timer every 1 ms and angles of the ankle joint (0) measured by
an electrogoniometer.
Frame-by-frame
ultrasonic
images recorded on the tape were printed
every 25 ms onto image
1430
the
pennate
muscle; tibialis
anterior
muscle
CONTRACTIONS
0161-7567/96
$5.00
Copyright
o 1996
American
Physiological
Society
IN VIVO TENDINOUS
Table 1. Physical characteristics
Subj. No.
1
26
52
29
26
39
2
3
4
5
Meant
SD
of subjects
Height,
Age, yr
m
Weight,
1.65
1.67
1.71
1.78
1.82
34+-11
MOVEMENT
kg
63
68
68
91
83
1.73 + 0.07
75%12
1431
BY ULTRASOUND
probe did not move during measurement. !Ib test the reproducibility of the measurement, 6X was measured three times for two
subjects. The intertest variability was <l mm for the dorsiflexion
of 0.18 rad, and the coefficient of variation was 6%.
A simple linear regression analysis was applied to the
relationships between 6X and 8 and between estimated moment arms and physical measurements such as body height
and tibia1 length. In all cases, the level of significance was set
at P < 0.05.
RESULTS
recording paper. The displacement (6X) of q during shortening
and lengthening was determined as the tendinous movement
between two consecutive images. A marker made of a fish
bone and an acoustic standoff (K in Fig. 1) was placed between
the skin and the probe as a landmark to confirm that the
Angle (rad)
Time (set)
reference mark
t
01: 12
K
0.00
-
i- ,\_ a
.m.w-=aii adipose tissue
L
aponeurosis
fascicle
.‘.rl
-
a2:1e
-
Figure 1 shows successive ultrasonic images at three
different values of 8 during dorsiflexion.
It was observed that +Qmoved by 15 mm proximally
with a
dorsiflexion of 0.35 rad. Figure 2 shows an example (1
subject) of 6X and 0 during dorsi- and plantar flexion at
two frequencies. 6X appeared to synchronize with the
changes in 8 both at low and high frequencies. Highly
significant correlations were observed between Sh and 8
(Fig. 3) in all subjects (r = 0.93-0.99).
DISCUSSION
Through a comparison of ultrasonic measurements
with direct measures on human cadavers, the ultrasonic echoes have been confirmed to be from the
aponeuroses and fascicles of muscles (5). 6X in the
present study is thus considered to be the movement of
a point on the central aponeurosis;
i.e., tendinous
movement, resulting from shortening and lengthening
of fascicles. The methods that have been proposed so far
A
PI:&?
0
f
0.4
m
-
0.2
2
4
6
8
10
Lo
4
I
I
10 mm
Fig. 1. Ultrasonic images of anterior aspect of lower leg at midpoint
of tibia1 bone. Subcutaneous adipose tissue, muscle [tibialis anterior
(TA)], and central aponeurosis are visualized. Point at which 1
fascicle was attached to aponeurosis was determined as 9. During
dorsiflexion, ni, which is of relaxed position of ankle, moved proximally to qa by 0.015 m when joint dorsiflexed by 0.35 rad. Placement
marker was fixed to skin on anterior aspect of lower leg at midpoint of
tibia1 bone as reference point (K) that did not move during contractions.
e
1
0.01
-J
I
I
I
1
I
I
I
0
2
4
6
8
10
Time
(s)
Fig. 2. Displacement of n @Xl and angle of ankle joint (0) during
dorsi- and plantar flexion movements at 91 (slow;A) and 1.5 (fast; B)
Hz. 6X was measured every 25 ms.
IN VIVO
l
MOVEMENT
slow (0.03 rad/s)
y - 1.15 +48.3x
-----I
01.
TENDINOUS
fast (0.20 l-ad/s)
y = 0.67 + 48.1x
r = 0.97
I
02.
I
03.
I
04.
0 (rad)
Fig. 3. Relationship
between
6X and 8 during
ments
[0.5 (slow) and 1.5 (fast) Hz]. Data points
movement
(dorsiflexion
phase)
for 1 subject.
correlations
were observed
in both conditions.
dorsiflexion
moveare from 1 range of
Significant
positive
to estimate the displacement
of human muscles in vivo
involve insertion of needles into a muscle (3) and X-ray
tine recordings of injected m arkers into the muscletendinous junctions (2), both of which test th .e biceps
brachii muscle. These methods have some drawbacks;
for example, in the former it is not clear whether the
position of the tips of the needle remained unchanged
in the muscle, especially when the muscle is voluntarily
tensed, and in the latter a limitation
exists for the
allowable
duration
of X-ray exposure. In addition,
pennate muscles in which fibers are arranged diagonally to the longitudinal
direction of the muscle cannot
be studied with these methods. The present technique
iS noninvasive
in nature, and one can observe the
actual movement
of aponeuroses of pennate muscles
during contraction in a real-time fashion.
q moved proximally during dorsiflexion and distally
duri .ng plantar flexion. This implied that TA shortened
and lengthened
in pha se wi .th dorsi - and plantar flexion, respectively. Amis et al. (2) also reported that there
was no detectable phase shift between intramuscular
and joint displacements during voluntary elbow flexionextension movements
with no additional
load. The
muscle-tendon
unit consists of elastic and contractile
components, and a major part of the elastic component
is occupied by tendinous tissues that are lengthened by
a tension applied to them (12). Because no additional
load other than the mass of the foot was applied to the
muscle-tendon
unit in this study, the lengthening
of the
elastic component was negligible. This could explain
the lack of a phase shift of 6X from joint movements,
although it is possible that the present method was not
sensitive enough to detect the small phase shift that
might have occurred. At other intensities
of contraction, the tendinous
movement
might shift from the
joint motions. In this way, the length-tension
relationship of the tendon could be determined in vivo by using
the present method. However, as discussed below, it
should be noted that the present results are limited to a
certain point on the aponeurosis of muscle.
BY
ULTRASOUND
Because TA is a bipennate muscle with its proximal
fibers attached to the tibia1 bone, it is reasonable to
assume that the proximal attachment
does not move
during contraction.
Thus displacement
of the central
aponeurosis, i.e., 8X in this study, is considered to be
equivalent
to the movement
of the distal tendon. It
therefore follows that the slope of the regression lines
@X/0> represents the average moment arm length of TA
for this joint range (10). The values ranged from 44 to
48 mm among subjects, which were highly correlated
with the body height (r = 0.98) (Table 2) and were
comparable to direct measurement
by using magnetic
resonance imaging (8). Longer tibias mean there are
more sarcomeres in series. Subjects with longer tibias
have more sarcomeres and thus larger, and possibly
faster, muscle excursions to account for the longer
moment arms.
Some methods have been proposed to measure moment arms of human muscles: most of these are based
on measurements
on cadaver specimens. One study
(10) that used a similar (tendon travel) method to the
present one determined
moment arms of the cadaver
quadriceps
muscles. In that study, tendinous
movement of the muscles in situ was measured and related
to the joint angles to give average moment arms. The
present technique is similar, but it enables determination of the moment arm length in vivo. However, the
moment
arms determined
in this manner
are the
average values over the joint range of motion, and it
has been shown that the moment arm length changes
at different joint angles (8). By studying the tendinous
movement over a small joint angle range, changes in
the moment arms over a whole range of motion could be
determined
and compared with the anatomically
determined values.
The tendinous movement observed in this study was
presumably
caused by the change in length of muscle
fibers. However, as noted above, the tendinous movement might also include elongation of the aponeurosis.
Furthermore,
it has been shown (7) that the fibers do
not run from origin to insertion
but taper within
fascicles. Elasticity of the attachments
between tapering fibers might affect the tendinous movement. The
present study cannot distinguish
what amount of the
measured tendinous
movements
is muscle and what
amount is tendon in origin. In addition, the present
results are based on the measurements
of the movement of one certain point on the aponeurosis. It has
Table 2. Estimated moment arms of tibialis anterior
muscle from relationships between tendinous
movement and joint angles
Subj. No.
Arm, mm
44.4
45.6
46.2
48.1
48.4
1
2
3
4
5
Mean
Moment
+ SD
46.5 2 1.7
IN VIVO
TENDINOUS
MOVEMENT
been shown in rat muscles that there is some variability in the elasticity over the aponeurosis (13). Such a
heterogeneity
may exist in human muscles, in which
case the movement of separate areas on the aponeurosis might not be the same. Considering
also that the
pennation angle changes during contraction,
the present measurements
do not correspond to the muscle
movement but are limited to the movement of a certain
point on the aponeurosis. These uncertainties
could be
investigated with the present method in future studies.
This method could also have other applications in the
field of muscle physiology and biomechanics in humans.
Quantification
of changes in fascicle length and pennation angles in a contracting muscle, which is currently
under investigation,
is an example. Force-velocity and
force-length relationships
in human muscles could also
be determined in human muscles in vivo.
Address
for reprint
requests:
T. Fukunaga,
Laboratory
of Sports
Sciences,
Department
of Life Sciences,
University
of Tokyo,
3-8-1,
Komaba,
Meguro,
Tokyo 153, Japan.
Received
14 September
1995;
accepted
in final
form
19 April
1996.
REFERENCES
ankle
R. M.,
muscles
and
and A. Vernon.
the forces they
The
exert.
dimensions
J. Hum.
1992.
11. Wilkie,
of knee and
Mou. Stud.
1:
115-123,1975.
2. Amis,
Ward.
human
3. Fellows,
S. J., and P M. H. Rack.
Changes
in the length of the
human
biceps brachii
muscle during
elbow movements.
J. PhysioZ.
Lond.383:
405-412,1987.
4. Henriksson-Larsen,
K., M.-L.
Wretling,
R. Lorentzon,
and
L. Oberg.
Do muscle
fibre size and fibre angulation
correlate
in
pennated
human
muscles?
Eur. J. Appl. Physiol.
Occup. Physiol.
64: 68-72,1992.
5. Kawakami,
Y., T. Abe, and T. Fukunaga.
Muscle-fibre
pennation angles are greater
in hypertrophied
than in normal
muscles.
J. AppZ. PhysioZ.
74: 2740-2744,
1993.
6. Kuno,
S., and
T. Fukunaga.
Measurement
of muscle
fibre
displacement
during
contraction
by real-time
ultrasonography
in
humans.
Eur. J. AppZ. PhysioZ.
Occup. Physiol.
70: 45-48,
1995.
7. Loeb,
G. E., C. A. Pratt,
C. M. Chanaud,
and
F. J. R.
Richmond.
Distribution
and innervation
of short,
interdigitated muscle
fibers
in parallel-fibered
muscles
of the cat hindlimb. J. Morphol.
191: 1-15, 1987.
8. Rugg,
S. G., R. J. Gregor,
B. R. Mandelbaum,
and L. Chiu.
In vivo moment
arm calculations
at the ankle
using
magnetic
resonance
imaging
(MRI).
J. Biomech.
23: 495-501,199O.
9. Rutherford,
0. M., and D. A. Jones.
Measurement
of fibre
pennation
using
ultrasound
in the human
quadriceps
in vivo.
Eur. J. AppZ. Physiol.
Occup. PhysioZ.
65: 433-437,
1992.
10. Spoor,
C. W., and J. L. van Leewen.
Knee muscle
moment
arms from MRI and from tendon
travel.
J. Biomech.
25: 201-206,
12.
1. Alexander,
A., A. Prochazka,
D. Short,
P. S. T. Trend,
Relative
displacements
in muscle
and tendon
arm movements.
J. PhysioZ. Lond. 389: 37-44,1987.
13.
and A.
during
1433
BY ULTRASOUND
D. R. The relation
between
force and
muscle.
J. Physiol.
Lond.
110: 249-280, 1950.
Woo,
S.-L. Y. The effect of exercise
on the
biochemical
properties
of swine
digital
flexor
mech.Eng.
103:51-56,1981.
Zuurbier,
C. J., A. J. Everard,
P. van der
Huijing.
Length-force
characteristics
of the
passive
and active muscle
condition
and in the
J. Biomech.
27: 445-453,1994.
velocity
biomechanical
tendons.
in human
and
J. Bio-
Wees,
and P. A.
aponeurosis
in the
isolated
condition.