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Acute Effect of Static Stretching on Hardness of the Gastrocnemius Muscle

AKAGI, RYOTA; TAKAHASHI, HIDEYUKI

Medicine & Science in Sports & Exercise: July 2013 - Volume 45 - Issue 7 - p 1348–1354
doi: 10.1249/MSS.0b013e3182850e17
APPLIED SCIENCES
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Purpose The objective of this study is to investigate the acute effects of static stretching (SS) on muscle hardness of the gastrocnemius medialis (MG) and gastrocnemius lateralis (LG).

Methods Twenty young men participated in this study. MG and LG hardness was measured using shear wave ultrasound elastography before and after three bouts of 2-min SS. The measurement site of muscle hardness was at 30% of the lower leg length from the popliteal crease to the lateral malleolus. Similarly, the passive range of motion (ROM) of dorsiflexion, musculotendinous unit (MTU) stiffness determined by the slope of the portion of the passive torque-angle curve from 15° to 25°, and joint torque developed during isometric maximal voluntary plantarflexion at 0° of ankle joint angle were also measured before and after SS.

Results SS increased ROM and decreased MTU stiffness significantly but did not change joint torque. The main effects of test time and muscle group on muscle hardness were significant without a significant interaction of these variables. Both differences between the relative changes in the MG and LG hardness and between the muscle hardness ratios before and after SS were not significant. A significant correlation between the muscle hardness ratios before and after SS was found.

Conclusion The results of this study suggest that three bouts of 2-min SS of the plantar flexors is useful for preventing muscle injury, improving muscle condition, and maintaining muscle strength, and that the acute effects of SS on the muscle hardness of MG and LG are of the same degree.

Department of Sports Science, Japan Institute of Sports Sciences, Tokyo, JAPAN

Address for correspondence: Hideyuki Takahashi, Ph.D., Department of Sports Science, Japan Institute of Sports Sciences, 3-15-1 Nishigaoka, Kita-ku, Tokyo 115-0056, Japan; E-mail: hideyuki.takahashi@jpnsport.go.jp.

Submitted for publication November 2012.

Accepted for publication December 2012.

Muscle hardness is a mechanical property that represents transverse muscle stiffness (30) and is distinguished from musculotendinous unit (MTU) stiffness along the longitudinal axis of a muscle (13). Muscle hardness can indicate muscle condition objectively (28,39) because muscles become harder under several conditions, including those involving cramps, spasms, and damage (10,30). Therefore, it is important to decrease muscle hardness to improve muscle condition and/or maintain good muscle condition.

It has been indicated that stretching a muscle speeds relief from cramp (27). Therefore, given that muscles become harder under a variety of conditions including those involving cramps (10), stretching can be useful for decreasing the muscle hardness. Static stretching (SS) increases the joint range of motion (ROM). When the SS duration is short such as 1–2 min (24,25), the ROM increases because of increased stretch tolerance. In contrast, when the SS duration is comparatively long, SS changes not only ROM but also MTU stiffness (29,31). This decrease in MTU stiffness is likely due to a decrease in muscle stiffness (20,29,31). Previously, the intramuscular connective tissue has been suggested to consist of parallel elastic components (e.g., the endomysium, perimysium, and epimysium) causing passive tension (12), and the connective tissue, particularly the perimysium, has been reported to be a major extracellular contributor to passive stiffness (34). Thus, changes in properties of the intramuscular connective tissue causing passive tension appear to relate to the decrease in muscle stiffness (31). It is therefore not surprising that SS results in not only a decrease in the muscle stiffness but also a decrease in the muscle hardness. To our knowledge, however, the only study (32) investigating the effect of SS on muscle hardness did not find a decrease in muscle hardness with SS. That is, so far, the study of the effect of SS on muscle hardness has been superficial. It is important to investigate this topic to obtain knowledge for improvement of muscle condition and/or maintenance of good muscle condition.

This study quantified the hardness of the gastrocnemius muscle, where cramping commonly occurs (36), before and after SS using shear wave ultrasound elastography (33,37) in addition to MTU stiffness of the plantar flexors (the gastrocnemius muscle and the soleus muscle). On the basis of the given description, we hypothesized that when MTU stiffness of the plantar flexors declines with SS, the SS also results in a decrease in the hardness of the gastrocnemius muscle. In addition, given that the gastrocnemius muscle has two heads (i.e., gastrocnemius medialis (MG) and gastrocnemius lateralis (LG) muscles), the intermuscle difference in hardness was also investigated. The purpose of this study was to determine the acute effect of SS on the hardness of MG and LG.

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METHODS

Subjects.

After having provided written informed consent, 20 young men (age, 25.0 ± 3.4 yr; body height, 173.6 ± 4.7 cm; body mass, 74.0 ± 13.5 kg (mean ± SD)) with no orthopedic abnormalities in their lower legs participated in the present study. Four subjects were sedentary, and the others reported engaging in 1–8 h·wk−1 of recreational sports. None of the subjects were competitive athletes or were engaged in systematic resistance training and stretching programs. Either the right or left leg was randomly selected to perform SS in each subject. The study protocol was approved by the Ethics Committee of the Japan Institute of Sports Sciences.

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Experimental protocol.

Before SS, the 1) passive ROM of dorsiflexion, 2) hardness of MG and LG, 3) MTU stiffness of the plantar flexors, and 4) joint torque of the plantar flexors were measured in this order. After SS, the same measurements were performed. Both sets of measurements were completed within 20 min, respectively. The temperature of the experimental room was kept constant at around 25°C throughout the measurements and SS.

During the measurements, each subject was instructed to lie in a prone position on a reclining seat attached to a dynamometer (Biodex System 3; Biodex Medical Systems Inc., Shirley, NY). The ankle was secured to a footplate attached to the dynamometer by an inelastic belt, with the hip and knee joints fully extended, so the ankle joint was aligned with the axis of the dynamometer. The setup of ankle joint angle during each measurement is described in the succeeding part of this article.

SS was performed with a stretching board (H-7295; Toei Light Co., Ltd., Tokyo, Japan) (Fig. 1). The subjects were instructed to stand erect on one foot on the stretching board during SS, with arms supported on the wall anterior to the body and the other foot attached the verge of the stretching board in order not to lose their balance (Fig. 1). A 2-min SS was performed three times with a 1-min interval between sets. During this interval, the subjects got off the stretching board, sat on a chair, and relaxed. When SS duration is comparatively long (7,29,31), ROM and MTU stiffness are significantly changed. Moreover, previous findings have indicated that isometric muscle strength in the plantar flexors does not change significantly with SS totaling 3–10 min (7,18,23). Thus, SS for a total of 6 min was expected to increase ROM, to decrease MTU stiffness, but not to decrease muscle strength in this study. For each subject, the ankle joint angle during SS was 3° lower than the ROM. For subjects with ROM of more than 35°, however, the ankle joint angle during SS was set as 32°, which was the maximum angle of the stretching board. During SS, we confirmed that the subjects could perform the SS without suffering discomfort or pain and feel that their plantar flexors were fully stretched.

FIGURE 1

FIGURE 1

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Passive ROM.

To determine the passive ROM of dorsiflexion, the footplate of the dynamometer was moved manually by an examiner, starting at 0° and increasing to the dorsiflexion angle at which subjects felt discomfort or pain. This dorsiflexion angle was measured three times, and the integral mean value of the three was defined as passive ROM. A previous study (38) indicated that active ROM may be decreased because of pain or weakness, and thus, passive ROM better estimates actual joint motion. On the basis of this indication, not active but passive ROM was determined in this study. The coefficient of variation (CV) for the three values was 4.4% ± 2.1% with an intraclass correlation coefficient (ICC (1,2)) of 0.958 (P < 0.001).

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Muscle hardness.

Hardness of MG and LG was measured at 30% of the lower leg length from the popliteal crease to the lateral malleolus where almost the maximal cross-sectional area in the lower leg is observed (17). Lower leg length measurement was performed before all of the other measurements. Subjects stood with their leg muscles relaxed during the measurement of the lower leg length to the nearest 0.5 cm with a steel tape.

The muscle hardness was measured at 30° of plantarflexion using shear wave ultrasound elastography images obtained by an ultrasonic apparatus (Aixplorer; SuperSonic Imagine, Aix-en-Provence, France). At this angle, passive torque around the ankle has been shown to be near zero (19,35), and thus, the muscle hardness were expected to reflect the hardness of MG and LG themselves. For each of these muscles, an electronic linear array probe (SuperLinear 15-4, SuperSonic Imagine) was transversely placed on the muscle because the highest muscle thickness in the mediolateral direction was observed near the transverse center of the image (Fig. 2). Water-soluble transmission gel was applied to the contact surface.

FIGURE 2

FIGURE 2

As shown in Figure 2, shear wave ultrasound elastography generated color-coded images with a scale from blue (soft) to red (hard) depending on the magnitude of Young’s modulus. Of the stored images in the ultrasonic apparatus at 11 Hz, a single image, on which a stable color distribution was observed during a certain time, was selected to determine the muscle hardness. In the image, a region of interest (10 mm × 10 mm) was set near the center part where the muscle was thickest. In addition, a 5-mm-diameter circle was set near the center of the region of interest. In doing so, the Young’s modulus within the circle was automatically calculated and was determined as the muscle hardness.

The hardness measurements for MG and LG were performed five times each, in random order. Of the five measured values, the group of three measurements showing the lowest CV among the 10 possible groups was adopted, and their mean value was used for further analysis. The CV values for the adopted three values were 4.0% ± 2.6% in MG and 3.2% ± 2.2% in LG with ICC (1,2) of 0.991 in MG and 0.988 in LG, respectively (P < 0.001).

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MTU stiffness.

Passive plantarflexion torque was measured using the dynamometer while the footplate of the dynamometer was moved at a constant velocity of 5°·s−1 by motor control from 30° of plantarflexion to 25° of dorsiflexion, which was achieved by all subjects without pain. The slope of the portion of the passive torque-angle curve from 15° to 25° was defined as MTU stiffness (22,31). The MTU stiffness measurement was performed twice, and the mean value of the two measurements was adopted. The CV for the two values was 2.8% ± 3.5% with an ICC (1,3) of 0.997 (P < 0.001).

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Joint torque.

Joint torque of the plantar flexors was measured using the dynamometer as an index of muscle strength. The subjects performed maximal voluntary contraction of isometric plantarflexion at 0° of ankle joint angle with the hip and knee joints fully extended for 3 s. Joint torque was expected to be highest near the set angle (11). The joint torque data were digitally recorded at a 100-Hz sampling frequency. The joint torque measurements were performed twice with at least a 2-min interval. If the difference between two values of joint torque was more than 10% of the higher value, joint torque was measured once more. Of the two or three joint torque measurements, the highest values were adopted.

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Day-to-day reproducibility of the measurements.

To ensure day-to-day reproducibility of the measurements, the same procedures were performed on another day for two subjects. The CV values of the two measured values were 2.5% ± 2.6% in ROM of dorsiflexion, 2.2% ± 1.6% in the MG hardness, 3.5% ± 2.9% in the LG hardness, 8.4% ± 3.7% in MTU stiffness of the plantar flexors, and 8.9% ± 3.7% in joint torque.

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Statistical analyses.

Descriptive data are presented as mean ± SD. The Student paired t-test was used to test differences in passive ROM of dorsiflexion, MTU stiffness of the plantar flexors, and joint torque of the plantar flexors between before and after SS. To examine the effect of SS on the muscle hardness, two-way ANOVA (test time (before and after SS) × muscle group (MG and LG)) with repeated measures was used. When both significant main effects of test time and muscle group with no significant interaction of these variables were found, relative changes in the MG and LG hardness from before to after SS and ratios of the MG hardness to the LG hardness before and after SS were calculated. The Student paired t-test was used to examine differences between the relative changes in the MG and LG hardness and between the muscle hardness ratios before and after SS. Pearson product–moment correlation coefficient between the muscle hardness ratios before and after SS was also calculated. Statistical significance was set at P < 0.05. When the results of the Student paired t-test and two-way ANOVA are presented, r or η p 2 are shown as indices of effect size with the P value.

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RESULTS

There were significant differences in passive ROM and MTU stiffness before and after SS, whereas joint torque before SS was not significantly different from that after SS (Table 1). Main effects of test time and muscle group on muscle hardness were significant, and a significant interaction of these variables was not found (Table 1).

TABLE 1

TABLE 1

Relative changes in the MG and LG hardness from before to after SS were 12.4% ± 8.1% and 12.7% ± 7.3%, and ratios of the MG hardness to the LG hardness before and after SS were 0.827 ± 0.152 and 0.833 ± 0.167, respectively. There were no significant differences between the relative changes in the MG and LG hardness (P = 0.895, r = 0.031) and between the muscle hardness ratios before and after SS (P = 0.805, r = 0.058). The correlation coefficient between the muscle hardness ratios before and after SS was significant (r = 0.793, P < 0.001).

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DISCUSSION

As expected, passive ROM of dorsiflexion increased and MTU stiffness of the plantar flexors decreased significantly with acute SS (Table 1), which is consistent with previous findings (20,29,31). When SS duration is short such as 90-s SS (24) or three repetitions of 45-s SS (25), ROM increases due to increased stretch tolerance rather than changes in MTU mechanical properties. On the other hand, when SS duration is comparatively long (29,31), as in this study, both ROM and MTU stiffness are significantly changed. According to previous studies (20,29,31), the SS-induced decrease in MTU stiffness is influenced by that in muscle stiffness. It has been suggested that the intramuscular connective tissue consists of parallel elastic components (e.g., the endomysium, perimysium, and epimysium) causing passive tension (12). Furthermore, Purslow (34) has reported that the connective tissue, particularly the perimysium, is a major extracellular contributor to passive stiffness. Thus, the decrease in muscle stiffness is considered to be affected by changes in properties of the intramuscular connective tissue causing passive tension (31). These phenomena can result in a decrease in the muscle hardness.

The muscle hardness of MG and LG after SS was significantly lower than those before SS (Table 1). In a previous study (32), two repetitions of 2.5-min SS did not result in a decrease in the MG hardness because changes in passive torque after SS could be mainly explained by an acute increase in muscle length without any changes in intrinsic muscle mechanical property. As described in the previous paragraph, however, a total of 5-min SS duration is sufficient time to produce a decrease in MTU stiffness that is attributable to the decrease in muscle stiffness (29,31). Hence, the aforementioned viewpoint of Nordez et al. (32) seems not to be reasonable. In other words, although there is a discrepancy in SS-induced decrease in muscle hardness between the studies, it is possible that three bouts of 2-min SS contribute to the decrease in muscle hardness, i.e., improvement of muscle condition.

Joint torque of the plantar flexors after SS was not significantly different from that before SS (Table 1). Previous findings on the acute effect of SS on muscle strength are still controversial (2–5,7,15,18,23). As a reason for this discrepancy, the differences in duration of SS between studies are considered. Review articles about the acute effect of SS on muscle strength (6,21) have indicated that SS for >90 s could well reduce muscle strength. Meanwhile, other studies (4,7,9,18,23,40) found no significant stretching-induced deficit in muscle strength using 1–10 min of stretching duration. It is thus difficult to clearly determine the duration that would produce a muscle strength deficit. In the plantar flexors, however, isometric muscle strength measured at 0° of ankle joint angle did not change significantly with SS totaling 3–10 min. It has been suggested that whether SS decreases muscle strength is dependent on the muscle length (i.e., the joint angle) (16,26). Hence, the current results can be influenced not only by the duration of SS but also by the setup of the ankle joint angle during the measurement of joint torque.

The muscle hardness of MG was lower than that of LG both before and after SS (Table 1). On the other hand, differences between the relative changes in the MG and LG hardness and between the muscle hardness ratios before and after SS were not significant, and there was a significant correlation between the muscle hardness ratios before and after SS. These results suggest that the original difference in the muscle hardness between MG and LG does not change greatly with three bouts of 2-min SS of the plantar flexors. In other words, the muscle hardness of MG and LG should be acutely affected by SS of the plantar flexors to the same degree.

Before concluding the current study, we would like to refer some limitations. The first limitation is that the ankle joint angle during SS for subjects with ROM more than 35° was uniformly set as 32°. Consequently, the acute effect of SS on each variable for the subjects with ROM more than 35° might have been different from that for the other subjects. To examine this possibility, changes in passive ROM and MTU stiffness of the plantar flexors and relative changes in the MG and LG muscle hardness from before to after SS were calculated, and their differences between those with ROM more than 35° (n = 6) and the others (n = 14) were tested by an unpaired t-test. As a result, there were no significant differences in the variables between them, suggesting that the restriction of the set ankle angle during SS had a small effect on the results of this study. The second limitation is that the MG and LG hardness was measured transversely, but not longitudinally. A previous study (14) reported that the contraction-induced increase in muscle hardness determined longitudinally was greater than that determined transversely, resulting from anisotropy of the muscle. This implies that the assessment of the effect of SS on the MG and LG hardness can change on the basis of whether the muscle hardness is measured transversely or longitudinally. In the present study, however, the MG and LG hardness was evaluated at 30° of plantarflexion, where passive torque around the ankle has been shown to be near zero (19,35). That is, the muscle hardness was expected to reflect the hardness of MG and LG themselves. Consequently, the mean value of the MG hardness before SS (27.6 kPa) was close to the values of MG hardness measured using a longitudinal image obtained by ultrasound real-time tissue elastography in previous studies (around 28–29 kPa) (1,8). Thus, it is suggested that the current results are less affected by the difference between the longitudinal and transverse directions of the ultrasound probe. The third limitation is that the soleus, which is one of the plantar flexors, was not investigated in this study. Beforehand, we explored measurement means of the muscle hardness of the soleus, MG, and LG. However, the soleus is located deeper than MG and LG, and therefore, the measurement value of the soleus hardness varied more than those of MG and LG. In addition, it was expected that the longer measuring time could be a negative factor in precisely examining the acute effect of SS on each variable. Based on these problematic points, we did not determine the muscle hardness of the soleus. Although determination of an acute effect of SS on the soleus hardness remains an issue, the fact that SS decreases the muscle hardness of both MG and LG strongly suggests that the muscle hardness of the soleus should also be decreased with SS. Further study is needed to clarify this point to more strongly support the findings obtained in this study. The last limitation is that only three bouts of 2-min SS were used in this study. As described previously, this SS was expected to induce an increase in ROM, a decrease in MTU stiffness, and no change in joint torque. All of these expectations were satisfied. However, whether the SS duration used in this study (i.e., three bouts of 2-min SS) is practical or not is open to question. This is the first study to demonstrate that SS decreases both MTU stiffness and muscle hardness, and therefore, it is still debatable whether the SS duration can be shortened while maintaining this availability of SS.

In summary, three bouts of 2-min SS of the plantar flexors significantly increased passive ROM of dorsiflexion and decreased MTU stiffness of the plantar flexors and muscle hardness of MG and LG, whereas joint torque was not significantly changed with SS. These results suggest that this SS is useful for preventing muscle injury, improving muscle condition, and maintaining muscle strength in the plantar flexors. The muscle hardness of MG was lower than that of LG before and after SS. However, both differences between the relative changes in the MG and LG hardness and between the muscle hardness ratios before and after SS were not significant, and a significant correlation between the muscle hardness ratios before and after SS was found. Thus, it is likely that the original difference in the muscle hardness between MG and LG remained after three bouts of 2-min SS of the plantar flexors, and that the acute effect of SS on the muscle hardness of MG and LG are of the same degree.

This study was supported by a Grant-in-Aid for Young Scientists (B) (no. 24700689).

The authors declare that they have no conflicts of interest.

The results of the present study do not constitute endorsement by the American College of Sports Medicine.

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Keywords:

SHEAR WAVE ULTRASOUND ELASTOGRAPHY; YOUNG’S MODULUS; JOINT ROM; MTU STIFFNESS; MG AND LATERALIS; JOINT TORQUE

© 2013 American College of Sports Medicine