Download Ultrasonography gives directly but noninvasively elastic

Eur J Appl Physiol (1995) 71:555-557
© Springer-Verlag 1995
S. F u k a s h i r o • M. I t o h • Y. Ichinose • Y. K a w a k a m i
T. F u k u n a g a
Ultrasonography gives directly but noninvasively elastic characteristic
of human tendon in vivo
Accepted: 30 August 1995
Abstract. To obtain an insight into tendon elasticity
during human movement, a real-time ultrasonography was
applied to the contracting tibialis anterior muscle. The
insertion point of fascicles onto the aponeurosis was clearly
visualized, and its position relative to a fixed marker on the
skin moved proximally (/11) according to the increasing
dorsiflexion force ( / I F ) with a fixed ankle joint. Notably,
t h e / i l - / i F relationship in the tendon was found to be
quadratic in nature ( / I F = c/i1 2., c = 1 . 4 8 " 2 . 2 4 , r=0.985--0.992, n-9) as has been reported in the isolated tendon,
although the A F - / I 1 curves were slightly underestimated in
comparison with the stiffness constant estimated from
tendon architecture. This underestimation might be caused
by changes in the height of the foot arch with the
application of force.
Key words: Human tendon elasticity • Ultrasonography •
Tibialis anterior muscle • F-L curve
Introduction
According to Hill's classical model, the skeletal muscletendon complex consists of contractile and series elastic
components (CC and SEC, respectively). The SEC
demonstrates elastic behavior in most movement patterns
and especially when the muscle is activated and
simultaneously stretched prior to concentric action (Komi
1984). Although the elastic characteristics of SEC can be
observed through t h e / I F - / l l relation, direct measurement
of this relation has been impossible. For this reason, these
characteristics have been indirectly estimated by special in
vivo and in vitro methods (e.g. Huijing 1992; Poussen, et
al. 1990).
Because the major part of the SEC is located in the
tendinuous tissues of a muscle, we can consider some
fundamental characteristics of the SEC with regard to
tendon (Huijing 1992). The displacement at a certain point
in the human tendon can be directly but noninvasively
observed in vivo by using ultrasonography (Kawakami, et
a1.1993). We can then obtain the delta lengthening of the
tendon with the force by measuring the distance traveled by
a certain point on the tendon during an isometric
contraction with increasing force. The purpose of this study
was to determine the /1 F-/11 characteristics in a distal
tendon of the human tibialis anterior muscle (TA) by
ultrasonography.
Methods
Subjects were 3 healthy male volunteers (24-31 yr of age,
172-178 cm in body height, 62-73kg in body weight).
Informed consent was obtained from each subject before the
study began. As shown in Fig. 1, the subject lay supine on a bed
and was requested to perform isometric dorsiflexion with
gradually increasing force in each trial at three ankle joint
angles (90, 105 and 120 deg) by using a special ergometer
(MYORET, ASICS, JPN). The ultrasonic image of the TA during
contraction was recorded on a videotape synchronized with a
clock timer to record time in ms and dorsiflexion torque. The
lengthening of the distal tendon of the TA was estimated with
ultrasonic apparatus. The ultrasonic apparatus (SSD-2000,
ALOKA, JPN) consists of an electronic linear array probe of
7.5MHz wave frequency. The scanning head is coated with a
water-soluble transmission gel, which provide 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 in the tibial bone length.
The tester visually confirmed the echoes reflected from the
aponeurosis and interspaces between fascicles in the TA.
Frame-by-frame photos of ultrasonic images recorded on video
tape were printed every 25ms onto image recording paper. The
lengthening of distal tendon (1) was calculated from the
displacement of ' z/' between two consecutive images. After the
ultrasonic probe was firmly positioned, a specially-designed
placement marker (K) was set between the body and the probe
so that K did not move, which was confirmed by VTR. The
cross-point (r/) between two echoes; one echo from the deep
aponeuroses and the other from fascicles, was easily determined
on the ultrasonogram as shown in Fig.l. The echoes have been
confirmed to be from the aponeuroses and fascicles through a
comparison of ultrasonic measurements with direct measures on
cadavers, with a measurement error < 10(Kawakami et al. 1993).
Therefore, the displacement (7/) is considered to indicate the
lengthening of the distal tendon. Conversely, the torque
measured by the ergometer was converted to the force at the
distal end of the tibialis anterior muscle, according to the
moment arm of TA (Rugg et al. 1990).
556
2a 800
A 90 deg
600-
•
105 deg
o
120 deg
•
q
Z
400
.<1
200
0
i~Ai i
5
10
15
2b
IOOO
Estimated
750-
12o\\
. ....
/
.
120deg
................ 105deg
z
It-
25
(mm)
A l
degree
105 90
I
20
500-
. . . . . . 90deg
:.." ,,,
z~- '
/,,5 •"
250- j
0
Torque & Angle
0
,
'
I
I
I
5
10
15
20
Al(rnrn)
F i g. 1. Example of an ultrasonic image of the anterior leg at a
point 50% distal to the length of tibial bone.
The
subcutaneous adipose tissue, muscle (TA) and internal
aponeurosis are visualized. The cross-point ;q was determined
from the echoes of the deep aponeuroses and fascicles.
Results
and D i s c u s s i o n
Fig. 2a shows a typical example of the / 1 F - / l l curves in
each trial at three ankle angles. T h e / 1 F - / l l curve at 105
deg of ankle angle is shifted to the left compared to that at
90 deg of ankle angle. Also, a similar shift was observed
among 120 and 105 deg in ankle angles. These shifts are
probably due to the fact that the initial length of the muscle
Fig. 2a: Force-Length relations of human tendon in three
angles of ankle joint. 2b: Force-Length relations that were
arranged on the length axis based upon the onset of the force
generation. The estimated curve was calculated from tendon
architecture.
fibers would have been stretched by plantarflexion from 90
to 120 deg, but not the tendinuous tissue until acted upon
by external and/or internal forces. In order to focus the
elastic characteristics of the tendon itself, the three curves
were arranged on the length axis based upon the onset of the
force generation (Fig. 2b). Each curve in Fig. 2b fitted well
to a quadratic regression. The correlation coefficients of
these regression curves were high at three joint angles of all
subjects (/1F=c/11 2; c=1.48"--2.24, r=0.985"--0.992, n=9).
557
These quadratic characteristics are quite similar to those
isolated tendon (Woo 1981). Since the / 1 F - / l l curve in
tendon mainly depends upon the cross-sectional area and
length of tendon itself (Bobbert, et al. 1986), the stiffness
constant and/or the compliance of each tendon is specific to
its tissue. Therefore, we can estimate the curve from the
tendon architecture that was conventionally used in the
biomechanical analysis (Bobbert, et al. 1986). The curve
measured in the present study agreed well with but slightly
underestimated, the real values. This underestimation may
be due to changes in the height of the arch of the foot with
the application of force. Fukashiro et al. (1994) reported
that the height of foot arch was changed by the external
force body weight vector.
The elastic characteristics of the SEC have usually been
estimated using the following methods. Three methods used
in the isolated preparation are: (i) the quick release method;
(ii) a method using fast constant velocity releases; (iii) a
method calculating compliance from the force-time curve of
an isometric tetanic contraction. These methods have been
briefly reported by Huijing (1992). Also, the compliance of
SEC in elbow flexion was estimated using the quick release
method by Poussen, et al. (1990). However, the elastic
characteristics of human tendon can be directly but
noninvasively measured using the technique presented in
this paper. Then, the technique described in the present
study would provide a powerful tool in determining in vivo
characteristics of human tendon elasticity.
It was concluded that the /1F-z~l curve of the human
tendon can be directly but noninvasively obtained using the
present method.
References
Bobbert MF, PA Huijing, GA van Ingen Schenau (1986)
A model of the human triceps surae muscle-tendon complex
applied to jumping. J.Biomech. 19:887-898
Fukashiro S and T Iraha (1994) How to prevent the navicular
stress fracture by the increased training quantity i n long
distance runner. Bulletin of the Physical Fitness Res Inst,
85:1-5 (in Japanese)
Huijing PA (1992) Elastic potential of muscle. Strength and
Power in Sport, B lackwell Sci.Pub. 151 - 168
Kawakami Y, T Abe and T Fukunaga (1993) Muscle-fiber
pennation angles are greater in hypertrophied than in
normal muscles. J Appl Physiol. 74:2740-2744
Komi PV (1984) Physiological and biomechanical correlates
of muscle function: Effects of muscle structure and stretchshortening cycle on force and speed. In Terjung ed. Exer
Sport Sci Review 12:81-121
Poussen M, JV Hoecke and F Goubel (1990) Changes in elastic
characteristics of human muscle induced b y eccentric
exercise. J Biomech. 23:343-348
Rugg S G, Gregor R J, Mandelbaum B R, Chiu L (1990) In vivo
moment arm calculations at the ankle using magnetic
resonance imaging (MRI). J Biomech 23:495-501
Woo SL-Y (1981) The effect of exercise on the biomechanical
and biochemical properties of swine digital flexor tendons.
J Biomech Engineering, 103:51-56