Medicine & Science in Sports & Exercise:
APPLIED SCIENCES: Biodynamics
Effect of Static and Ballistic Stretching on the Muscle-Tendon Tissue Properties
MAHIEU, NELE NATHALIE1; MCNAIR, PETER2; DE MUYNCK, MARTINE3; STEVENS, VEERLE1; BLANCKAERT, IAN1; SMITS, NELE1; WITVROUW, ERIK1
1Department of Rehabilitation Sciences and Physiotherapy; Faculty of Medicine and Health Sciences, Ghent University, Ghent, BELGIUM; 2Physical Rehabilitation Research Centre, Auckland University of Technology, Auckland, NEW ZEALAND; and 3Department of Physical Medicine and Orthopaedic Surgery, Faculty of Medicine and Health Sciences, Ghent University, Ghent, BELGIUM
Address for correspondence: Nele N. Mahieu, PT, Department of Rehabilitation Sciences and Physical Therapy, University Hospital Ghent, De Pintelaan 185, 6K3, B9000 Ghent, Belgium; E-mail: Nele.Mahieu@UGent.be.
Submitted for publication April 2006.
Accepted for publication September 2006.
Purpose: Many studies have been undertaken to define the effects of static and ballistic stretching. However, most researchers have focused their attention on joint range-of-motion measures. The objective of the present study was to investigate whether static- and ballistic-stretching programs had different effects on passive resistive torque measured during isokinetic passive motion of the ankle joint and tendon stiffness measured by ultrasound imaging.
Methods: Eighty-one healthy subjects were randomized into three groups: a static-stretch group, a ballistic-stretch group, and a control group. Both stretching groups performed a 6-wk stretching program for the calf muscles. Before and after this period, all subjects were evaluated for ankle range of motion, passive resistive torque of the plantar flexors, and the stiffness of the Achilles tendon.
Results: The results of the study reveal that the dorsiflexion range of motion was increased significantly in all groups. Static stretching resulted in a significant decrease of the passive resistive torque, but there was no change in Achilles tendon stiffness. In contrast, ballistic stretching had no significant effect on the passive resistive torque of the plantar flexors. However, a significant decrease in stiffness of the Achilles tendon was observed in the ballistic-stretch group.
Conclusion: These findings provide evidence that static and ballistic stretching have different effects on passive resistive torque and tendon stiffness, and both types of stretching should be considered for training and rehabilitation programs.
It is controversial whether stretching promotes better performances and decreases the number of injuries (34). However, stretching exercises are regularly included in warm-up and cool-down activities. On the sports field, the two most commonly used stretching techniques are static and ballistic stretching. Static stretching involves slow, controlled lengthening of a relaxed muscle (1). A ballistic stretch is a bouncing rhythmic motion that uses the momentum of a swinging body segment to lengthen the muscle. Guissard et al. (11) have reported that ballistic stretching caused facilitation of the stretch reflex, which is mediated by the facilitatory influences of muscle spindles type Ia and II receptors on homonymous alpha motor neuron excitability. This activation of the stretch reflex causes a contraction in the muscle being stretched. Thus, it has been stated that ballistic stretching is disadvantageous for improving range of motion and that it may even be harmful because the muscle may reflexively contract if restretched quickly, creating injury to the muscle fibers (30).
Many studies have attempted to determine whether outcomes such as range of motion or task performance are different depending on the type of stretching undertaken. Sady et al. (29) have compared ballistic, static, and proprioceptive neuromuscular facilitation (PNF) and have shown that all techniques were able to improve range of motion, but PNF was seen as the preferred technique. Similarly, Lucas and Koslow (19) have concluded that all three techniques were able to increase flexibility after a training period of 7 wk. Wallin et al. (33) have compared the effects of a modified contract-relax method and a traditional ballistic-stretch method. These authors have shown that the contract-relax method was significantly better than the ballistic-stretch method for improving range of motion. More recently, some authors have examined the effects of stretching on performance in tasks. For instance, Woolstenhulme et al. (35) have determined the effects of four different warm-up protocols (ballistic stretching, static stretching, sprinting, and basketball shooting (control group)) on range of motion and vertical jump height in basketball players. The findings show that the ballistic-stretch group had the greatest increase in range of motion. However, vertical jump height was not different after 6 wk in any of the groups. More recently, Unick et al. (31) also found no significant difference in vertical jump performance after either static or ballistic stretching.
Most previous work has been focused on range of motion as an outcome. However, dynamometers have allowed the measurement of passive resistive torque associated with the range-of-motion changes (21,23,24). Furthermore, dynamometer measurements, combined with ultrasonography (7,15-17,25), have allowed the appreciation of stretch within tendon structures. To date, no studies have used these techniques to examine whether ballistic or static stretching have different effects on measurements of passive resistive torque and stiffness. Theoretically, the rhythmic bouncing of ballistic stretching has different temporal characteristics in the applied forces (e.g., rate of application of force) compared with the sustained and steady force involved in a static stretch. As such, it might be expected that the contractile elements, together with the serial and parallel elements within the muscle, might respond differently over time to these types of stretch.
Therefore, the objective of the present study was to investigate whether a static and a ballistic-stretching program had different effects on passive resistive torque measured during isokinetic passive motion of the ankle joint, and tendon stiffness measured by ultrasound imaging.
MATERIALS AND METHODS
A randomized controlled pretest-posttest trial was used to assess two common stretching techniques during a 6-wk training program. Ninety-six volunteers were prepared to take part in the study. The subjects were randomly assigned into three groups: a static-stretch group (N = 33), a ballistic-stretch group (N = 33), and a control group (N = 30). Randomization was performed independently. Thirty cards for the control group and 33 cards for both stretching regimes were shuffled in a container. After completion of all preintervention assessments, each subject picked one card in a blinded manner. Both stretching groups performed a stretching program with a duration of 6 wk. They were asked to stretch their calf muscles every day. To supervise their training program, each person had to complete a personalized calendar of their stretching activity and was contacted every week by one of the investigators. The control group did not receive a training program. To supervise this group, the participants were contacted every week and were asked to complete a questionnaire at the end of the study. The main goal of this questionnaire was to make to sure that the subjects of the control group did not undertake additional stretching exercises during the intervention period. Unsatisfactory compliance with the prescribed regimes resulted in exclusion from the study. Before and after the 6 wk of stretching, all subjects were evaluated for ankle range of motion, passive resistive torque of the plantar flexors, and stiffness of the Achilles tendon.
The ethical committee of the Ghent University Hospital approved the study, and each participant gave written informed consent before participating. Subjects were informed that the study was for research purposes and were encouraged to give maximal effort throughout the entire testing procedure. Subjects with a history of lower-leg injuries were excluded from the study. Only recreational athletes were included in the study; competitive elite athletes were excluded. The personal stretching habits beyond the scope of the study protocol were questioned. During the study, all subjects were asked to maintain normal activity. The anthropometric characteristics of the subjects are presented in Table 1.
Before testing, all subjects completed a questionnaire to assess their medical history, their physical activity, and their experience with stretching. To assess possible changes in their lifestyle and to detect the presence of injuries during the 6 wk of training, this questionnaire was completed again after the 6 wk of training. This was done to verify the compliance of each subject. The results of the questionnaires indicated that one person of the control group did additional stretching exercises, eight people did not complete the stretching program successfully, and six people became sick or injured during the intervention period. Consequently, 81 of the 96 volunteers were included in the statistical analysis (37 males, 44 females; static N = 31; ballistic N = 21; control N = 29).
Dorsiflexion range of motion was measured with a universal goniometer (accurate to 1°) by the same investigator to provide good intrarater reliability. This person did not know the group allocation of the subjects. Previous research using radiography has established the validity of goniometric measurements (10). Each measurement was repeated three times, and the mean was used for statistical analyses. The left ankle was evaluated in a weight-bearing position. The measurement was performed according to the method of Ekstrand et al. (5). The subject was standing upright with the feet parallel. The subject was asked to step back with the left foot and to bring the ankle into maximum dorsiflexion, keeping the left knee straight and the heel on the ground. The subject was aware that the front leg must be flexed, the back leg must be kept straight, and the feet must be facing forward. The weight-bearing measurement also was examined with the knee flexed (5). The subject was asked to stand on the floor with the left foot on a bench. Then, the subject was asked to lean forward to produce a maximal dorsiflexion in the left ankle, with the heel in contact with the bench and the knee maximally flexed. The bony landmarks used for these measurements were defined using the method of Elveru (6). The proximal arm of the universal goniometer was aligned with the head of the fibula. The axis of the goniometer was positioned 0.5 cm below the lateral malleolus. The distal arm was aligned parallel to an imaginary line joining the projected point of the heel and the base of the fifth metatarsal. This measurement has been found to be valid and reliable (5,6).
Passive resistive torque measurement.
To test passive resistive torque, a Biodex System 3 isokinetic dynamometer was used. The subject was placed in a supine position with the knee maximally extended. The foot was securely strapped to a footplate connected to the lever arm of the dynamometer. The standard Biodex ankle-unit attachment with the provided Velcro straps was used. All subjects were asked to wear the same sport shoes with a low cut in both test sessions. The same investigator strapped the foot before and after the stretching period. The attachment of the foot was also such that the movement of the ankle joint was not impeded, to avoid an overestimation of the passive resistive torque. The height and the distance of the foot attachment was registered to make the assessment reproducible in the posttest session. During the testing session, the dynamometer moved the ankle passively through four continuous cycles of motion from 20° plantar flexion to 10° dorsiflexion at 5°·s−1, with neutral being the line of the tibia perpendicular to the footplate. These range-of-motion limits were used in the pretesting session and the posttesting session. This range of motion is used during many functional activities (3). A slow stretch speed was used to ensure that the stretch did not elicit reflexive muscle activity. Most authors agree that 5°·s−1 achieves this purpose (9). The subjects were instructed to relax, and before data collection, each person performed a test trial to become familiar with the system. During the test session, electromyographic activity from the plantar and dorsiflexor muscles was recorded (MyoSystem 1400, Noraxon USA Inc., Scottsdale, AZ). Surface electrodes with an electrical surface contact of 1 cm2 (Ag-AgCl, BlueSensor, Medicotest GmbH, Germany) were placed on the soleus, the tibialis anterior, and the medial head of the gastrocnemius muscle according to the guidelines of Basmajian (2) with an interelectrode distance of 10 mm. The EMG tracings were monitored during the tests to ensure that calf muscle activity was less than 0.05 mV above baseline during the passive stretch cycles (9). This EMG activity corresponds to approximately 2% MVC. The bandwidth of the frequency response was 20 Hz to 4 kHz (9). Similar to Gajdosik et al. (9), the raw EMG signals were relayed to an amplifier (×5000) and high-pass filtered at 20 Hz, and the analog signals were converted to digital data at a sampling rate of 500 Hz. The test was repeated if the subject was not relaxed sufficiently, that is, if the muscle activity was higher than 0.05 mV. The peak passive resistance torque (N·m) recorded from the dynamometer during four cycles of motion was used in the statistical analysis. A pilot study demonstrated that the reproducibility was high (ICC = 0.93-0.94, P < 0.001).
Measurement of the Passive Stiffness of the Achilles Tendon
The ratio of the calculated muscle force (Fm) and the elongation of the Achilles tendon (ELONG) provided a measure of the stiffness of the Achilles tendon. With respect to the muscle force, first, the measured torque TQ (N·m) during maximal isometric plantar flexion was converted to muscle force Fm (N) using the following equation:
Equation (Uncited)Image Tools
where k is the relative contribution of the physiological cross-sectional area of the medial gastrocnemius within plantar flexor muscles (18%) (8), and MA is the moment arm length of triceps surae muscle at 90° of ankle joint (50 mm) (28,32). Therefore;
Equation (Uncited)Image Tools
Secondly, the ratio of Fm and ELONG provided the stiffness of the tendon (N·mm−1). In this study, the calculations were based on those of Kubo et al. (18). Both legs were tested. The test-retest reliability of measuring the stiffness of the Achilles tendon using ultrasonography has been shown to be good (ICC = 0.80-0.82) (22).
Measurement of the torque.
The dynamometer (Biodex System 3) was used to determine torque output during isometric plantar flexion. The subject lay prone on a bench. First, the left ankle was placed in a 90° position (anatomical position) with the knee joint at full extension and the foot securely strapped to a footplate connected to the lever arm of the dynamometer. The standard Biodex ankle-unit attachment with the Biodex-provided Velcro straps was used in this study. To prevent ankle-joint changes, the foot was firmly attached to the footplate of the dynamometer with a strap. The position and the height of the Biodex chair were also recorded for each subject individually and were used in the following evaluations. Before the test, the subjects performed three to five submaximal contractions to be accustomed to the test procedure. After this warm-up, the subjects were instructed to develop an isometric maximal voluntary contraction (MVC) for 5 s. The task was repeated three times per subject, with 30 s of rest between trials. Visual examination was undertaken to ensure that the subject's ankle joint did not move during this muscle work. When motion was observed, the trial was discarded. Each subject was verbally encouraged to exert maximal voluntary effort by contracting as hard as possible. The maximal isometric strength was defined as the peak torque recorded. The force of the tendon was estimated from the plantar flexion torque, the physiological cross-sectional area ratio of the medial gastrocnemius to all the plantarflexors, and the moment arm (see formula above).
Measurement of elongation of the tendon.
To obtain a measurement of the elongation of a tendon, the method of Fukashiro et al. (7) was used. In the present study, a real-time ultrasonic apparatus (Siemens Sonoline SL-1) was used to obtain a longitudinal ultrasonic image of the medial gastrocnemius (MG) muscle at 30% of the lower leg (i.e., from the popliteal crease to the center of the lateral malleolus (17). An electronic linear-array probe of 7.5-MHz wave frequency was secured with Velcro straps on the skin. The ultrasonic images were recorded on videotape (Digital Camera Sony). One tester who was not aware of the group allocation of the subjects visually identified the echoes from the aponeurosis and the MG fascicles. Parallel echoes running diagonally represent the collagen-rich connective tissue between the fascicles of the medial gastrocnemius. The darker areas between the bands of echoes represent the fascicles. The echo that runs longitudinally in the middle is from the aponeurosis. The point (x) at which one fascicle was attached to the aponeurosis was visualized on the ultrasonic image. This point (x) moved proximally during isometric torque output. The distance traveled by x(Δx) is considered to indicate the lengthening of the aponeurosis and, therefore, of the tendon (14,25). Displacement was measured with the multimedia player Light Alloy 1D. The mean value of the three measurements was used as a representative value for the elongation of the tendon (ELONG).
The two stretching groups performed calf-stretching exercises every day for an intervention period of 6 wk. The exercises comprised a classic standing wall push performed successively on both legs. The same information and instructions were given to each subject. For example, the subjects were instructed that the holding point of the stretch should be at the point just before discomfort. The static-stretch group was instructed to hold the back knee completely extended. The subjects in the ballistic-stretching group followed an identical stretching protocol, except once these subjects had reached the initial stretching position, they were instructed to move up and down at a pace of one movement per second with the front knee. After 4 wk, all subjects received a wedge to perform the stretching exercise. Hence, subjects could increase the stretching intensity. This wedge (with a height of 5.7 cm) was placed under the forefoot of the back leg. During each stretching session, the stretch was repeated five times at each leg. After performing the stretch for 20 s, the subject rested 20 s before that leg was stretched again. Each subject received an audio CD with the stretch duration, the rest duration, and the rhythm of the exercise to standardize the program as much as possible.
Statistical analysis was performed with Statistical Package for the Social Sciences (version 11.0; SPSS Inc., Chicago, IL). The data were assessed for normality using the Kolmogorov-Smirnov test. One-way ANOVA were used to compare the baseline characteristics of the three groups. To determine the significance of an interaction effect (time × group) or main effect for time, a general linear model for repeated measures (GLM) was performed. Gender and the pretreatment measures were entered as covariates in the model. In these analyses, the Mauchly's test of sphericity was significant, indicating that the assumption of sphericity had been violated. Therefore, a Greenhouse-Geisser correction factor was applied to all P values. Pairwise differences were examined using Bonferroni tests, and the alpha level was set at 0.05 for all hypotheses.
The left ankle of 81 subjects was included in the statistical analyses. No significant differences were observed between the three groups at baseline. The baseline characteristics of the three groups are presented in Table 2.
Range of motion.
Table 3A and 3B shows that both stretching groups had a significantly increased dorsiflexion ROM for both measurements, with the knee flexed and extended. The control group also showed a significant increase in dorsiflexion range of motion. There were no significant interaction effects.
Passive resistive torque.
The results showed a significant main effect for time. Post hoc testing revealed that the PRT decreased significantly in the static-stretch group after 6 wk of stretching. The PRT of the ballistic-stretch group and the control group were not changed significantly. There was no significant interaction effect. The results of these analyses are presented in Table 4A and 4B.
Passive stiffness of the Achilles tendon.
There was a significant main effect for time. Post hoc testing revealed that the stiffness of the Achilles tendon decreased significantly in the ballistic-stretch group. In the static-stretch group and the control group, no significant changes were found after the 6 wk of stretching. There was no significant interaction effect. Table 5A and 5B shows these results.
The results of this study reveal that dorsiflexion range of motion was increased significantly in all groups. Previous studies using goniometry have confirmed that joint range of motion can be increased by stretching (27,29). To assess the effects of static and ballistic stretching more completely, resistive torque during passive motion was examined together with the stiffness of the Achilles tendon.
The results regarding passive resistive torque show that after 6 wk of stretching, it was significantly decreased, albeit by a relatively small amount in the static-stretch group, and it remained unchanged in the ballistic-stretch group. The finding related to the static-stretching group was in agreement with some (16), but not all, previous studies (21,27). Where no change has been observed, authors generally argue that the viscoelastic parameters have not been altered, and changes in torque and range of motion have occurred because of increased stretch tolerance. Because the range of motion in which the passive resistive torque was measured was the same in both pre- and posttesting, the small but significant decrease in passive resistive torque observed in the static-stretch group has to be attributed to structural changes (21). Although it is beyond the methods of the current study to define what structures changed, the most commonly reported would be an increase in sarcomeres (4,9,26). Indeed, Coutinho et al. (4) have investigated the effect of passive stretching applied every 3 d to the soleus muscle of rats and have found an increase in serial sarcomere number during a 3-wk period. Interestingly, in the current study, no change was observed with ballistic stretching, which might indicate that the tension placed on the muscle should be continuous and not intermittent, as would have been occuring with the ballistic techniques used in the current study. Alternatively, it may be that the forces generated in the range of motion tested did not elicit or show the effects of ballistic stretching.
In the present study, we observed no significant changes in tendon stiffness after 6 wk of static stretching. In contrast, after 6 wk of ballistic stretching, the stiffness of the Achilles tendon decreased significantly. Only one previous study has examined the effects of a stretching program on tendon stiffness in vivo. In that study, Kubo et al. (16) investigated the effects of a 3-wk static-stretching program and found that tendon stiffness was unchanged, a finding in agreement with the current study. Why these different responses occurred is not clear, but it may be related to the effect of stretching on the contractile elements versus the tendon. Although the resting contractile elements have been shown to be more compliant than the tendon for a particular length, the much greater length of tendon attached to the plantarflexor muscles in vivo means that when these muscles are stretched, much greater strains are observed in the tendon compared with the contractile elements (12). It may be that these larger strains induce an adaptation in the collagen fibers within the tendon, and this adaptation may require a repetitive changing stimulus (applied force), such as that seen in ballistic stretching, as compared with the sustained steady force associated with static stretching.
Another possible mechanism for the different effects of static and ballistic stretching on tendon stiffness is related to the viscosity of the muscle-tendon complex. Recently, McNair et al. (23) have reported that stiffness was decreased significantly more during cyclic motion compared with static stretching within a single stretching session, and these authors speculate that the more mobile constituents of soft tissues such as the polysaccharides and water are redistributed within the collagen framework more rapidly during cyclic motion. In this respect, Hutton (13) has commented that muscles display thixotropic behavior, a rheological term related to the viscosity of a gel and resistance to molecular deformation, and that motion leads to a decrease in the viscosity of the system. It may be that there are perennial changes in the viscosity of the system as a result of longer-term stretching affecting the composition of these components.
With respect to the findings, it should be kept in mind that the passive resistive torque and the measures of Achilles tendon stiffness cannot be compared directly, primarily because of the extremely different forces associated with these tests. In the range of motion through which passive resistive torque was measured, the forces are many times less than those associated with a maximum-effort activation of the plantarflexor muscles. There are also some limitations to the methodology of the present study. First of all, the position at which the isometric contraction was undertaken was 90° (anatomic position), and it was assumed that there was zero strain in the tendon at this point. However, Muramatsu et al. (25) have shown that this is not so, and hence the amount of displacement in the tendon would be underestimated and the subsequent measurement of stiffness would be overestimated. That said, Figure 8 in their paper (25) shows that the effect on strain between 10 and 90% MVC is relatively small. The ramifications with respect to measurements before and after stretching is that any decrease in stiffness might be overestimated. With respect to the calculation of Fm, we used the same moment arm for all our subjects, a technique used by others (8,14,16-18). For the measurement of individual moment arms, either direct measurements by MRI using the Reuleaux method as previously described (20,22), or by indirect measurement involving the calculation of the ratio of change in tendon length to change in joint rotation, would be required. Similarly, individual measurements of k, which is the relative contribution of the physiological cross-sectional area of the medial gastrocnemius within plantar flexor muscles, would be more accurately assessed by MRI. It should be noted that although tendon-displacement changes were measured during isometric muscle activation, it has been shown that small amounts of ankle-joint rotation (3-7°) can take place, and these can markedly affect the displacement measurements, particularly at high levels of an MVC, leading to overestimation of displacement and, hence, underestimation of stiffness (21,25). In the present study, we looked for these joint-motion changes, but only by visual observation, and if they were observed, the data were discarded and the test was repeated. Finally, why there was an increase in ROM in the control group should be considered. In this regard, because the responses to the questionnaires of the control group subjects indicated that they had undertaken no additional stretching exercise during the intervention period, we believe that the observed changes represent a learning effect. That is, at the second testing session, the subjects were able to undertake the ROM test with greater skill as a result of the practice they had received in the baseline testing session.
In the present study, static stretching resulted in a small decrease of the passive resistive torque in combination with no change in tendon stiffness. In contrast, ballistic stretching had no significant effect on the passive resistive torque. However, a decrease in stiffness of the Achilles tendon was observed after ballistic stretching. These findings have implications for the prevention of injury and for performance. They indicate that a combination of ballistic motion and holds may be most appropriate for training and rehabilitation programs.
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