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Influences of repetitive muscle contractions with different modes on tendon elasticity in vivo

Keitaro Kubo, Hiroaki Kanehisa, Yasuo Kawakami and Tetsuo Fukunaga Journal of Applied Physiology 91:277-282, 2001. You might find this additional information useful... This article cites 26 articles, 8 of which you can access free at: http://jap.physiology.org/cgi/content/full/91/1/277#BIBL This article has been cited by 3 other HighWire hosted articles: Repeated contractions alter the geometry of human skeletal muscle C. N. Maganaris, V. Baltzopoulos and A. J. Sargeant J Appl Physiol, December 1, 2002; 93 (6): 2089-2094. [Abstract] [Full Text] [PDF]

Effects of different duration isometric contractions on tendon elasticity in human quadriceps muscles K. Kubo, H. Kanehisa and T. Fukunaga J. Physiol., October 15, 2001; 536 (2): 649-655. [Abstract] [Full Text] [PDF] Medline items on this article's topics can be found at http://highwire.stanford.edu/lists/artbytopic.dtl on the following topics: Biophysics .. Muscle Contraction Physiology .. Humans Medicine .. Ultrasonography Updated information and services including high-resolution figures, can be found at: http://jap.physiology.org/cgi/content/full/91/1/277 Additional material and information about Journal of Applied Physiology can be found at: http://www.the-aps.org/publications/jappl

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Journal of Applied Physiology publishes original papers that deal with diverse areas of research in applied physiology, especially those papers emphasizing adaptive and integrative mechanisms. It is published 12 times a year (monthly) by the American Physiological Society, 9650 Rockville Pike, Bethesda MD 20814-3991. Copyright © 2005 by the American Physiological Society. ISSN: 8750-7587, ESSN: 1522-1601. Visit our website at http://www.the-aps.org/.

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Effects of resistance and stretching training programmes on the viscoelastic properties of human tendon structures in vivo K. Kubo, H. Kanehisa and T. Fukunaga J. Physiol., January 2, 2002; 538 (1): 219-226. [Abstract] [Full Text] [PDF]

J Appl Physiol 91: 277–282, 2001.

Influences of repetitive muscle contractions with different modes on tendon elasticity in vivo KEITARO KUBO, HIROAKI KANEHISA, YASUO KAWAKAMI, AND TETSUO FUKUNAGA Department of Life Science (Sports Sciences), University of Tokyo, Komaba 3-8-1, Meguro, Tokyo, Japan Received 28 November 2000; accepted in final form 27 February 2001

stiffness; damage; vastus lateralis muscle; ultrasonography

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.

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

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

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: [email protected] 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.

REPEATED MUSCLE CONTRACTIONS

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METHODS

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Kubo, Keitaro, Hiroaki Kanehisa, Yasuo Kawakami, and Tetsuo Fukunaga. Influences of repetitive muscle contractions with different modes on tendon elasticity in vivo. J Appl Physiol 91: 277–282, 2001.—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.

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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

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

Fig. 1. Four muscle endurance tests protocols: 1) 50 repetitions (rep) of maximum voluntary eccentric action for 3 s with 3 s of relaxation (ET1), 2) three sets of 50 repetitions of maximal voluntary isometric contraction (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).

Fig. 2. Ultrasonic images of longitudinal sections of vastus lateralis (VL) muscle at rest (A) and during 50% MVC contraction (B). Point at which 1 fascicle was attached to deep aponeurosis was determined as P. The distance traveled by P was defined as the length change of tendon and aponeurosis during contraction. VI, vastus intermedius; P1, P at 0% MVC; P2, P at 50% MVC.

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 realtime 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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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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Calculation of the elastic properties. The TQ measured by the dynamometer was converted to muscle force (Fm) by the equation Fm ⫽ k 䡠 TQ 䡠 MA ⫺ 1 where k is the relative contribution of VL to the quadriceps femoris muscle in terms of physiological cross-sectional area (13), and MA is the moment arm length of quadriceps femoris muscle at 80° of knee flexion, which was estimated from the thigh length of each subject as described by Visser et al. (22). In the present study, the Fm and L values above 50% of MVC were fitted to a linear regression equation, the slope of which was adopted as an index of stiffness (6–9). Comparison of stiffness values among four tests (before endurance test) revealed no significant difference and a coefficient of variance of 3.5–9.8% (mean 6.2%). Measurement of Electromyogram

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 Scheffe´’s test. The level of significance was set at P ⬍ 0.05. RESULTS

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. 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 signifiTable 1. iEMG values during ramp isometric contraction before and after ET3

Fig. 3. The changes in torque during the 4 endurance tests expressed as absolute values for the mean of 5 consecutive trials [ET1 (■), ET2 ({, E, ‚), 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.

Before After

RF

VL

VM

BF

1.21 ⫾ 0.53 1.17 ⫾ 0.44

1.46 ⫾ 0.37 1.42 ⫾ 0.30

1.43 ⫾ 0.32 1.40 ⫾ 0.44

0.10 ⫾ 0.03 0.10 ⫾ 0.04

Values are means ⫾ SD given in mV. iEMG, integrated electromyogram; ET3, 50 repetitions of maximal voluntary isometric contraction (MVC) for 1 s with 3 s of relaxation. RF, rectus femoris; VL, vastus lateralis; VM, vastus medius; BF, biceps femoris. There were no significant differences.

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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).

Fig. 4. The integrated torque values during the 4 tasks. Values are means ⫾ SD. The integrated torque value was significantly lower in ET1 than the other 3 ETs, whereas there were no significant differences among the other three tests. *Significantly greater than ET1, P ⬍ 0.05.

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CHANGE OF TENDON ELASTICITY AFTER MUSCLE CONTRACTIONS

Fig. 5. The relationship between muscle force (Fm) and the displacement of P (L) before (䊐) and after (⽧) 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.

durance tests than before. The stiffness decreased significantly after ET3 (P ⫽ 0.016) and ET4 (P ⫽ 0.012) (Table 2). DISCUSSION

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 mea-

Table 2. Measured variables before and after endurance tests MVC, Nm

ET1 ET2 ET3 ET4

Muscle Thickness, mm

Pennation Angle, °

Stiffness, N/mm

Before

After

Before

After

Before

After

Before

After

246 ⫾ 51 240 ⫾ 42 236 ⫾ 35 244 ⫾ 44

174 ⫾ 50* 184 ⫾ 38* 173 ⫾ 44* 171 ⫾ 36*

31.1 ⫾ 4.3 31.6 ⫾ 4.1 31.9 ⫾ 3.5 31.3 ⫾ 3.2

32.8 ⫾ 4.5* 33.0 ⫾ 4.1* 33.1 ⫾ 3.2* 32.9 ⫾ 3.8*

18.2 ⫾ 1.2 18.4 ⫾ 1.0 18.2 ⫾ 1.4 18.6 ⫾ 1.2

19.2 ⫾ 1.1* 19.5 ⫾ 1.6* 19.3 ⫾ 1.5* 19.7 ⫾ 1.1*

58.9 ⫾ 5.0 63.4 ⫾ 7.7 62.6 ⫾ 8.3 64.2 ⫾ 6.8

55.1 ⫾ 10.3 58.2 ⫾ 11.4 45.1 ⫾ 5.8* 47.3 ⫾ 6.5*

Values are means ⫾ SD. ET1, 50 repetitions of maximal voluntary eccentric action for 3 s with 3 s of relaxation; ET2, 3 sets of 50 repetitions of MVC for 3 s with 3 s of relaxation; ET4, 50 repetitions of 50% MVC for 6 s with 6 s of relaxation. * Significantly different from before, P ⬍ 0.05.

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cantly 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. 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 en-

CHANGE OF TENDON ELASTICITY AFTER MUSCLE CONTRACTIONS

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

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sured 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 productionlonger 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

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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. REFERENCES

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