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Department of Life Science (Sports Sciences), University of Tokyo, Komaba 3-8-1, Meguro, Tokyo, Japan
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The present study aimed to investigate the effects of repetitive muscle contractions on the elasticity of human tendon structures in vivo. Before and after each endurance test, the elongation of the tendon and aponeurosis of vastus lateralis muscle (L) was directly measured by ultrasonography while the subjects performed ramp isometric knee extension up to maximal voluntary isometric contraction (MVC). Six male subjects performed muscle endurance tests that consisted of knee extension tasks with four different contraction modes: 1) 50 repetitions of maximal voluntary eccentric action for 3 s with 3 s of relaxation (ET1), 2) three sets of 50 repetitions of MVC for 1 s with 3 s of relaxation (ET2), 3) 50 repetitions of MVC for 3 s with 3 s of relaxation (ET3), and 4) 50 repetitions of 50% MVC for 6 s with 6 s of relaxation (ET4). In ET1 and ET2, there were no significant differences in L values at any force production levels between before and after endurance tests. In the cases of ET3 and ET4, however, the extent of elongation after the completion of the tests tended to be greater. The L values above 330 N in ET3 and 440 N in ET4, respectively, were significantly greater after endurance tests than before. These results suggested that the repeated longer duration contractions would make the tendon structures more compliant and that the changes in the elasticity might be not be affected by either muscle action mode or force production level but by the duration of action.
stiffness; damage; vastus lateralis muscle; ultrasonography
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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REPEATED MUSCLE CONTRACTIONS result in a reduction of peak contraction force. Some previous studies demonstrated that this result is accompanied by the lengthening in electromechanical delay and the reduction in rate of force development (e.g., Ref. 27). The mechanisms underlying these phenomena have not been elucidated. Vigreux et al. (21) have found that compliance in the fatigued muscle is significantly higher than that in the nonfatigued muscle. On the other hand, the tendon structures have been assumed to be the major source of series elastic component (16). Therefore, there is a possibility that the changes in the elasticity of tendon structures could be a factor leading to the above-mentioned degradation in muscle contractility.
Previous findings obtained from animal experiments have shown that the elasticity of tendons is changeable through physical training (15, 25). However, the adaptations of tendon structures to training vary with the mode of exercise performed. For example, Woo et al. (25) indicated that the ultimate strength and stiffness of tendon in pigs increased through 12 mo of endurance training. However, Pousson et al. (15) observed a decrease in the stiffness of rat soleus muscle after 11 wk of vertical jumping training. These differences tempt us to assume that, if the elasticity of tendon structures changes by repeated muscle actions, its magnitude will be influenced by the type of muscle action. Furthermore, it is necessary to grasp the effects of acute exercises on the tendon properties for the understanding of the effects of different training regimes.
It is well known that exercises involving high-force eccentric muscle actions induce temporary muscle pain and damage (e.g., Ref. 14). Evidence of damage includes disruption of muscle fibers (2) and changes in voluntary strength and contractile properties in the immediate postexercise period (1). Komi (5) has shown that eccentric stresses exceed conventional concentric and isometric force by threefold. Therefore, it may be assumed that the eccentric contraction will induce greater change in the elasticity of tendon structures than other muscle action modes.
Real-time ultrasonography allows in vivo recording of human tendon structures movement during isometric muscle action (3, 6-11). The present study aimed to examine the changes in the elastic properties of human tendon structures caused by repeated maximal voluntary muscle actions with different modes, force production levels, and durations.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Subjects
Six men [age 24.9 ± 0.8 (SD) yr, height 172.5 ± 10.0 cm, weight 71.3 ± 10.9 kg] voluntarily participated in this study. The subjects were fully informed of the procedures to be utilized as well as the purpose of this study. Written informed consent was obtained from all subjects. None of the subjects was engaged in any sort of competitive exercise, and each took part in sports occasionally, at a recreational level. This study was approved by the office of Department of Sports Sciences, University of Tokyo, and complied with their requirements for human experimentation.Muscle Endurance Test
After a standardized warm-up, the subjects performed muscle endurance tests that consisted of knee extension tasks with four different action modes: 1) 50 repetitions of maximum voluntary eccentric action for 3 s with 3 s of relaxation (ET1), 2) three times 50 repetitions of maximum voluntary isometric action (MVC) for 1 s with 3 s of relaxation (ET2), 3) 50 repetitions of MVC for 3 s with 3 s of relaxation (ET3), and 4) 50 repetitions of 50% MVC for 6 s with 6 s of relaxation (ET4). The four muscle endurance tests are summarized in Fig. 1. Tests were performed by each subject on 4 separate days, with at least 2 wk between sessions, but no longer than 4 wk were allowed to separate the four sessions. The exerted torque (TQ) signal was recorded for each action during the muscle endurance test and then was integrated with respect to time. The obtained integrated TQ was referred to as iTQ.
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Measurement of Elastic Properties of Tendon Structures
Before and after each endurance task, the elongation of the tendon and apponeurosis of the vastus lateralis (VL) muscle as well as TQ was recorded continuously while the subjects performed ramp isometric knee extension up to MVC. For ET2, measurements of tendon elongation were performed after each 50 repetitions.Measurement of TQ. Each subject was seated on the test bench of a dynamometer (Myolet, Asics) at a hip joint angle of 80° flexed (full extension = 0°). The axis of the lever arm of the dynamometer was visually aligned with the center of rotation of the knee joint. The right foot was firmly attached to the lever arm of the dynamometer with a strap and fixed at a knee joint angle of 80° flexed (full extension = 0°). The subjects were asked to exert isometric knee extension TQ increasingly from zero (relax) to MVC within 5 s. TQ signals were analog-to-digital converted at a sampling rate of 1 kHz (MacLab/8, type ML780, AD Instrument) and analyzed by a computer (Macintosh Performa 630, Apple). The task was repeated two times per subject with at least 3 min between trials. The measured values that are shown below are the means of two trials.
Measurement of elongation of tendon structures.
A real-time ultrasonic apparatus (SSD-2000, Aloka) was used to obtain a
longitudinal ultrasonic image of VL at the level of 50% of the thigh
length. The ultrasonic images were recorded on videotape at 30 Hz,
synchronized with recordings of a clock timer for subsequent analyses.
The tester visually confirmed the echoes from the aponeurosis and VL
fascicles. The point at which one fascicle was attached to the
aponeurosis (P) was visualized on the ultrasonic image. The P moved
proximally during isometric TQ development up to maximum (Fig.
2). A marker (X) was placed between the
skin and the ultrasonic probe as the landmark to confirm that the probe
did not move during measurements. The cross-point between superficial
aponeurosis and fascicles did not move. Therefore, the displacement of
P (L) is considered to indicate the lengthening of the deep
aponeurosis and the distal tendon (9). The reliability of
the ultrasound measurement of L has been established
elsewhere (6-9).
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Calculation of the elastic properties.
The TQ measured by the dynamometer was converted to muscle force (Fm)
by the equation
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Measurement of Electromyogram
Bipolar surface electrodes (5 mm in diameter) were placed over the bellies of VL, rectus femoris (RF), vastus medialis (VM) and biceps femoris (BF) muscles with a constant interelectrode distance of 25 mm. The electromyographic (EMG) signals were transmitted to a computer (Macintosh Performa 630, Apple) at a sampling rate of 1 kHz. The EMG was full-wave rectified and integrated for the duration of the contraction to give integrated EMG (iEMG).Measurement of Muscle Architecture
The ultrasonic apparatus was also used to determine the thickness (MT) and pennation angle (PA) of VL. For MT, the cross-sectional image was obtained at a site of the middle of the thigh length. From the ultrasonic image, the interface between the subcutaneous adipose tissue and VL and interface between the muscle [vastus intermedius (VI) muscle] and bone were identified from the ultrasonic image. The distance from the adipose tissue-L interface to the VL-VI interface was defined as MT. Also, at this position, the longitudinal image was obtained for PA. PA was defined as the angle between the fascicle and the deep aponeurosis.Statistics
Descriptive data included means ± SD. The significance of difference between values before and after endurance test was analyzed by Student's t-test. One-way ANOVA was used for the comparison among four conditions. If the F statistic of the analysis of variance was significant, differences among four conditions were assessed by a Scheffé's test. The level of significance was set at P < 0.05.| |
RESULTS |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Figure 3 shows the changes in TQ
values during muscle endurance tests, expressed as absolute values for
the mean of five consecutive trials. In ET4, all the subjects almost
completed the task with their own prescribed force production levels.
The rates of decline in TQ in ET1, ET2, and ET3 were 41.5 ± 15.2, 36.0 ± 18.7, and 44.2 ± 18.1%, respectively. No
significant differences in the rate of decline in TQ were found among
the three endurance tests. The iTQ value was significantly lower in ET1
than in the other three endurance tests (Fig.
4). Among ET2, ET3, and ET4, however, there were no significant differences in iTQ.
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Table 1 shows the iEMG values of RF, VL,
VM, and BF during the measurement of elongation of tendon structures
(i.e., ramp isometric contractions) before and after ET3. The EMG
activities of each quadriceps femoris muscles (RF, VL, VM) did not
differ significantly before and after ET3. The iEMG of BF were very
small and did not change significantly after ET3. Similar results were obtained in the other three tests (ET1, ET2, ET4), too.
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Figure 5 shows the relationship between
Fm and L before and after each endurance test. There were no
significant differences in the rate of decline in MVC value among the
four endurance tests (Table 2).
Similarly, there were no significant differences in the rate of
increment in MT and PA among the four endurance tests (Table 2). In ET1
and ET2, there were no significant differences in L values
at any force production levels between before and after endurance
tests. No significant changes in stiffness values were found after ET1
(P = 0.119) and ET2 (P = 0.156) (Table
2). In the cases of ET3 and ET4, however, the extent of elongation after the completion of the tests tended to be greater. The
L values above 330 N in ET3 and 440 N in ET4, respectively,
were significantly greater after endurance tests than before. The
stiffness decreased significantly after ET3 (P = 0.016)
and ET4 (P = 0.012) (Table 2).
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The major finding of the present study was that the repeated longer duration contractions made the tendon structures more compliant and that the changes in the elasticity were affected by the duration of action but not by force production level. Before interpreting the results obtained, however, we must draw the attention to the limitations and assumptions of the methodology followed. To calculate the muscle force, we estimated moment arm length and relative contribution of VL to the knee extensor muscles in terms of physiological cross-sectional areas. The variation in moment arm length and relative contribution of VL among subjects might have caused the large variability in the measured parameters. The moment arm length and physiological cross-sectional areas of respective muscles of each subject would be necessary for an "accurate" absolute muscle force determination. In the present study, however, we aimed to study whether the tendon properties changed after the repeated muscle contractions. In addition, there were no significant differences in the activation levels (iEMG) of knee extensor muscles before and after the endurance tests (Table 1). Therefore, we considered that this muscle force calculation based on these assumptions would be valid to study the changes of the tendon properties after the endurance tests. The present results demonstrated that the repeated longer duration contractions made the human tendon structures more compliant in vivo. This agrees with the findings of Vigreux et al. (21), suggesting that the fatigued muscle is more compliant than the nonfatigued muscle. However, the extent of changes observed in the elasticity depended on the exercise modes performed. Namely, endurance tests involving either eccentric or rapid isometric muscle actions with high force production did not induce significant changes in the elasticity of tendon structures. Previous studies have shown that exercise involving high-force eccentric muscle actions can produce temporary muscle pain and damage (e.g., Ref. 14). In addition, force production in an explosive exercise such as jumping can yield the lengthening of tendon structures in the lower limb (10). At the beginning of the study, therefore, it was expected that the endurance tests involving either eccentric actions (ET1) or rapid force production (ET2) would induce greater changes in the elasticity compared with the other test conditions. However, no significant changes in stiffness values were found after the ET1 and ET2 (Table 2; P > 0.05). Certainly, the TQ values that developed in the ET1 were significantly greater than those in the other test conditions. However, the duration in which TQ values in ET1 were higher than the level achieved in the other test conditions was relatively short. Similarly, for ET2, the duration in which the peak value of TQ could be maintained was very short. On the other hand, the elongation of tendon structures increased after ET3 and ET4, as characterized by the higher force production-longer duration and the lower force production-longer duration, respectively, compared with ET1 and ET2. Therefore, it may be assumed that the elasticity of tendon structures is influenced not by muscle action mode or force production level but by the duration of force production.
The mechanisms that change the elasticity of tendon structures after the repeated longer duration contractions are unknown. At least for the increased elasticity observed in the present study, however, an acute change in the structure of the tendons might be involved. From the findings of Stromberg and Wiederhielm (19), the collagen fibers follow a wavelike course in the unstressed tendons, but they become aligned or parallel with increasing stress. If a similar phenomenon occurs in the tendon structures on completion of the endurance tests used in the present study, the observed increment in the tendon elongation might be attributed to an acute change in the arrangement of collagen fibers. Recently, we showed that the static stretching of plantar flexors for 10 min made the tendon structures in the medial gastrocnemius muscle more compliant (8). Therefore, we considered that the stretched tendon structures for a given duration (muscle contraction and/or stretching) would lead to an acute change in the structure of the tendons. In addition, these changes might have occurred in the aponeurosis, because the most elasticity was in the aponeurosis (4). In any case, further investigations are needed to clear up this point.
Another possible explanation is the alteration of the viscoelastic properties of the intramuscular connective tissue as a result of an actual muscle temperature increase with contractions. Certainly, it has been shown in a number of studies that dense connective tissue, composed primarily of collagen fibers, becomes more extensible as its temperature is increased within normal physiological limits (18, 24). Warren et al. (24) studied the effects of temperature on rat tail tendon extensibility and concluded that the viscoelastic response of this tissue increases with temperature increase. In contrast, Magnusson et al. (12) demonstrated that 30 min of continuous running elevated intramuscular temperature significantly but did not measurably affect the viscoelastic properties of the hamstring muscle-tendon complex. In the present study, although no attempts were made to monitor the temperatures of muscle and tendon, there were no significant differences in the percent decline of MVC and increments of MT and PA among the four endurance tests (Table 2). Therefore, it is likely that the different changes in tendon structures after four endurance tests would not be caused by muscle temperature increases.
Fatigue leads to failure after repeated applications of stress, which may be much lower than the ultimate stress. The phenomenon is well known in man-made materials such as metals and polymers (e.g., Ref. 20). Recent studies showed that mean extension of wallaby tail tendons increased slowly during the fatigue test but much faster just before rupture (17, 23). Wang et al. (23) implied that this failure would result from cumulative damage. Some of the changes in tendon cells (fibroblasts), collagen fibers, and ultrastructure associated with a response to excessive loading have recently been documented in various animal models (e.g., Ref. 26). For example, Zamora and Marini (26) reported that collagen bundles in the tendon were disrupted and that empty longitudinal spaces were observed. They have suggested that the tendon undergoes a process similar to muscle hypertrophy but that "remodeling of the tendon architecture may involve a transient period of mechanical weakness" because of the observed ultrastructural changes. Therefore, it seems that the observed increase in L values after repeated contractions is a phenomenon corresponding to "a transient period of mechanical weakness" in tendon structures. If so, the stiffer tendon in endurance runners, which was reported in a prior study (6), may be a result of remodeling of the tendon architecture to compensate for mechanical weakness. In any case, longitudinal observations need to clear up this point.
In conclusion, these results suggested that repeated longer duration contractions would make the tendon structures more compliant and that the changes in the elasticity might be affected not by either muscle action mode or force production level but by the duration of actions.
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FOOTNOTES |
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Address for reprint requests and other correspondence: K. Kubo, Dept. of Life Science (Sports Sciences), Univ. of Tokyo, Komaba 3-8-1, Meguro-ku, Tokyo 153-8902, Japan (E-mail: kubo{at}idaten.c.u-tokyo.ac.jp).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 28 November 2000; accepted in final form 27 February 2001.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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), ET2 (
, 
,
), ET3 (closed cross), ET4 (hatched square)]. Values
are means ± SD. There was no significant difference in the rate
of decline of force among 3 tests (ET1, ET2, ET3). In ET4, all subjects
almost completed the prescribed test.
) and after (
)
endurance test. Values are means ± SD. In ET1 (A) and
ET2 (C), there were no significant differences in L
values between before and after. In ET3 (B) and ET4
(D), the extent of elongation before tended to be greater
than that after. *Significantly greater than before, P < 0.05.