Stroke is one of the most common disabling conditions and presents a major public health problem worldwide (9). Following a stroke, central excitatory drive to motor units is disrupted due to lesion in the descending motor pathways (13), causing impaired ability to voluntarily generate muscle force. In addition, other factors such as muscle atrophy and lack of physical activity may also contribute to muscle weakness (33). Muscle weakness has been identified as a major contributing factor to disability among people with stroke (33). For example, decreased leg muscle strength has been associated with reduction in gait speed and quality, walking endurance, transfer capacity, stair climbing ability, and balance function (10,20).
Recent observations have shown the possibility of using whole-body vibration (WBV) as a training tool in rehabilitation to improve muscle strength in a variety of populations, including young athletes, seniors, and people with chronic conditions (2,16,23,26,38). Several studies have shown that muscle activity can be enhanced during the application of WBV (4,14,34,36). Roelants et al. (36) examined the EMG response of rectus femoris, vastus lateralis (VL), vastus medialis, and gastrocnemius (GS) during the performance of three isometric exercises (high squat, low squat, and one-legged squat) with WBV (36). Compared with the no-WBV condition, adding WBV significantly increased the EMG amplitude for all four muscles measured during the performance of all three squatting exercises, by 49%–361% (36). Because of its ability to enhance muscle activity, increasing research has explored whether WBV training for a longer period can lead to an increase in muscle strength in older adults, who often suffer from muscle weakness (23). A recent meta-analysis showed that WBV has significant treatment effect on enhancing certain aspects of leg muscle strength in older adults after 6–10 wk of training (23).
Because most WBV treatment programs involve relatively brief treatment sessions and simple body movements (23), it is deemed suitable for those with neurological conditions, who often sustain considerable motor and cognitive deficits. Indeed, WBV therapy has been reported to have positive effects on muscle strength and motor performance in adults with cerebral palsy (2). Apart from resistance exercise training (11), WBV may thus offer a viable intervention approach for persons with stroke to improve muscle strength. Several randomized controlled studies have investigated the effects of 4–8 wk of WBV therapy on leg muscle strength in stroke patients. The results are mixed, with significant effects reported in some studies (37,39), but not others (4,24). Perhaps the difference in subject characteristics and WBV exercise protocols such as vibration settings, program duration, and exercise posture used in these studies may account for the difference in outcomes. In particular, the vibration intensity used across the different studies varied greatly (peak acceleration ranging from (9.5 to 92.5 m·s−2) (4,24,37,39), and the rationales for the protocols used with physiologically based justifications were often not provided (4,37). Before effective WBV exercise protocols can be identified for this subject group, it is essential to address a more fundamental yet important question: What occurs to the leg muscle activity level during exposure to WBV of different intensities? Understanding the relationship between leg muscle activation and WBV intensity and exercise is essential as it would inform the design of WBV protocols for further efficacy studies (e.g., randomized controlled trials). In addition, it would also provide a physiological basis for the therapeutic effects (or lack thereof) induced by different WBV exercise protocols.
Although it is well known that exercise training is an important adjunct therapy in patients with chronic stroke that can lead to improvements in function (27,31), research evidence is scarce on examining the relationship between outcomes and different modes of exercise, including the effects of WBV exercise. To date, no study has systematically examined the effects of WBV on leg muscle activity in individuals with chronic stroke. The purpose of this study was to determine the influence of different WBV protocols on the amplitude of EMG activity in the VL and GS muscles during the performance of various exercises among people with chronic stroke.
METHODS
Study design.
This was an experimental study, with subjects undergoing three different WBV conditions of no WBV, low-WBV-intensity protocol, and high-WBV-intensity protocol. In each condition, the subjects were asked to perform eight different exercises while leg muscle activity on both sides was measured using surface EMG. The sequence of WBV intensities used and exercises performed was randomized by drawing ballots using an opaque envelope to avoid order effect. For each subject, all measurement procedures were performed on the same day.
Subjects and sample size estimation.
As no study has examined the EMG response during WBV in people with stroke, previous research investigating the EMG response during WBV in healthy adults was used to estimate the sample size needed for this study. In a study involving 15 healthy men, Roelants et al. (36) obtained a large effect size (Cohen’s d = 5–8) for various muscle groups when WBV (35 Hz) was applied. On the basis of ANOVA (three WBV conditions), assuming an effect size f = 0.6 (large), with an alpha of 0.05 and power of 0.8, a minimum of 30 subjects would be required.
Subjects were recruited from stroke self-help groups in the community via convenience sampling. The inclusion criteria were as follows: a diagnosis of a hemispheric stroke with onset ≥6 months (i.e., chronic stroke), community dwelling (i.e., noninstitutionalized), abbreviated Mental Test score ≥6, and having hemiparesis in the lower extremity, as indicated by a composite leg and foot motor score of 13 or lower according to the Chedoke–McMaster Stroke Assessment (12). The exclusion criteria were as follows: neurological conditions in addition to stroke, brainstem or cerebellar stroke, significant musculoskeletal conditions (e.g., recent fractures and amputations), substantial vestibular dysfunctions (e.g., vertigo), peripheral vascular disease, unable to maintain standing for 1 min with standby guarding assistance of one person, severe cardiovascular conditions (e.g., unstable angina, uncontrolled hypertension, and uncontrolled cardiac dysrhythmia), and pain conditions that affected performance in standing, walking, or other daily functional activities.
The study was approved by the Research Ethics Committee of the administrating institute before commencement. The experimental procedures were first fully explained to each subject before written informed consent was obtained. The study was conducted in accordance with the Declaration of Helsinki.
Basic demographics and spasticity.
The basic demographic information (e.g., age, medical history, medications, etc.) was obtained from interviewing the subjects. To test spasticity on the paretic side, subjects were placed in a supine position and asked to relax. The researcher then moved the knee on the paretic side into flexion and extension alternately, and the resistance to passive motion was noted. The same test was done on the ankle joint on the paretic side. The Modified Ashworth Scale was used to indicate the severity of spasticity in each joint tested. A higher score is indicative of more severe spasticity (0 = normal muscle tone, 4 = tested part rigid) (3).
WBV protocol.
The Jet-Vibe System (Danil SMC Co. Ltd., Seoul, Korea) was used to deliver the WBV stimulation. This device generates vertical vibrations and has an adjustable frequency range between 20 and 55 Hz with corresponding preset amplitudes.
The intensity of WBV, represented by the peak acceleration (apeak), was calculated by the following formula: apeak = (2πf)2A, where A is the amplitude and f is the frequency (19). The apeak is usually represented as a unit of the gravitational constant (g = 9.81 m·s−2). The peak acceleration values generated by the device were validated by a triaxial accelerometer (Model 7523A5; Dytran Instruments Inc., Chatsworth, CA).
Each participant was subject to three different WBV conditions: (a) no WBV, (b) low-intensity WBV protocol (peak acceleration = 0.96g, frequency = 20 Hz, amplitude = 0.60 mm), and (c) high-intensity WBV protocol (peak acceleration = 1.61g, frequency = 30 Hz, amplitude = 0.44 mm) while performing different exercises. We chose these frequencies because WBV frequencies lower than 20 Hz may cause destructive resonance effects to the body (35). On the other hand, our pilot experiments showed that frequencies higher than 30 Hz caused discomfort and fatigue in some individuals. The higher peak acceleration values associated with higher frequencies may also be a potential hazard for people with compromised bone mass, such as chronic stroke survivors (30).
Exercise protocol.
The subjects were required to perform eight different exercises while being exposed to the three WBV conditions as described in Table 1. These exercises were commonly used in previous WBV trials in different populations (5,22,23,34,36,38). Practice trials were given to ensure that the subjects were able to perform the exercises properly before actual data collection. The knee angle was measured by a manual goniometer (Baseline® HiRes™ plastic 360° ISOM Goniometer, Fabrication Enterprises, White Plains, NY) to indicate the desired knee flexion angle in standing (10°), semisquat (30°), and deep-squat (90°) exercises. All experimental procedures were monitored closely by the researcher throughout to ensure that the subjects were performing the exercises properly and consistently. For standardization, all subjects were encouraged to gently hold on to the handrail of the WBV device for balance only. To ensure safety, the researcher provided standby guarding assistance while the patient was standing on the vibration platform. The researcher was standing by the patient in a guarding position, using his hands to be ready to guard or guide the patient.
;)
TABLE 1: Static exercises performed while standing on the vibration platform.
Measurement of leg muscle activity responses.
Surface EMG was used to measure activity of the VL and GS muscles in all test conditions. After proper skin preparation, the bipolar bar electrodes (Bagnoli EMG system; Delsys, Inc., Boston, MA) were placed on the muscle belly of GS and distal one third of VL muscles, according to the specifications of the Surface EMG for a Non-invasive Assessment of Muscles (SENIAM) project (15). A reference electrode was placed at the head of fibula. Insulated EMG cables were fastened to avoid movement artifacts.
For each WBV condition, subjects were asked to assume each of the eight postures (Table 1) for 10 s while VL and GS EMG activity was being recorded. A total of three trials were performed for each of the eight exercises in a given WBV condition, with a 1-min rest period in between trials. After all eight exercises were completed in the first WBV condition, the subjects were then asked to do the same eight exercises in the second and third WBV conditions. A 10-min rest period was given between each WBV condition. Only the EMG data obtained during the middle 6 s of each trial was extracted to obtain the EMG root mean squares (EMGrms), and the mean value of the three trials was used for subsequent analysis.
All EMG data collected were preamplified (×1000) and sampled at 1 kHz (Bagnoli-8; DelSys, Inc.) using a personal computer with LabView version 7 software (National Instruments Corp., Austin, TX). Data processing was performed using MyoResearch XP, Master Package version 1.06 (Noraxon USA, Inc., Scottsdale, AZ). The EMG data were filtered with 20- to 500-Hz band-pass Butterworth filter, and the Infinite Impulse Response (IIR) rejector was implemented to eliminate the associated harmonics at the frequencies of 20, 30, and 60 Hz. After filtering, bias was calculated and removed from each EMG signal, and then the data were rectified and the EMGrms calculated in 100-ms windows around every data point (1).
At the beginning of the session, the EMG activity of VL and GS during maximal voluntary isometric contraction (MVC) was first recorded. For measuring the EMG amplitude of VL during MVC of knee extension, each subject was comfortably seated, and the tested leg was fixed horizontally on a dynamometer (Cybex Norm Testing & Rehabilitation System, Stoughton, MA) with hip and knee stabilized at 90°. Subjects were then asked to perform isometric knee extension for 10 s. The same device was used to stabilize the hip and knee when measuring the EMG amplitude of GS during MVC of ankle plantarflexion. The foot was placed at 90° on a wedged platform, and the subjects were instructed to isometrically plantarflex the ankle against the wedge with maximal effort and sustain for 10 s. Subjects were provided with verbal encouragement to ensure a maximal effort during testing.
EMG root mean square values (EMGrms) were calculated during intervals of 0.5 s (8). For each muscle, the maximum EMGrms values from the three MVC trials were averaged to obtain the mean value, which was then used for normalization of the EMGrms value obtained in each WBV condition. Therefore, the EMG amplitude of each muscle obtained in all WBV conditions was expressed as a percentage of the EMG amplitude obtained during the MVC (%MVC). The reliability of the EMGrms data obtained from the three MVC trials was excellent, as demonstrated by the intraclass correlation coefficients (ICC3,1) (paretic VL = 0.99, paretic GS = 0.94, nonparetic VL = 0.99, nonparetic GS = 0.99).
Statistical analysis.
Analysis was performed with IBM SPSS Statistics software (version 20.0; IBM, Armonk, NY). The level of significance was set at P ≤ 0.05. Two-way repeated-measures ANOVA (within-subject factors: intensity [no WBV vs low-intensity WBV vs high-intensity WBV] and exercises) was used to compare the normalized EMGrms data across the different conditions. When sphericity assumption was violated, the Greenhouse–Geisser epsilon adjustment was used. Contrast analysis using paired t-test with Bonferroni adjustment was performed if any overall significant results were obtained for the EMG data. To compare the influence of WBV on the paretic side versus the nonparetic side, the ratio of normalized EMGrms (%MVC) of the VL and GS on the paretic side to the corresponding muscles on the nonparetic side was computed. A ratio greater than 1 indicated that the paretic side achieved a higher %MVC than the nonparetic side. A second two-way repeated-measures ANOVA model (within-subject factors: WBV intensity and exercises) was then constructed, using the EMGrms ratio as the dependent variable. Effect size was denoted by partial eta-squared (partial η2). Large, medium, and small effect sizes were represented by partial η2 values of 0.14, 0.06, and 0.01, respectively (29). To examine the potential effect of spasticity on the EMG data, Spearman’s rho was used to examine the relationship between (a) paretic knee spasticity score and normalized EMGrms of paretic VL and (b) paretic ankle spasticity score and normalized EMGrms of paretic GS in each testing condition.
RESULTS
Demographic characteristics of subjects.
A total of 64 individuals with chronic stroke were screened, and 45 of these (34 men and 11 women) fulfilled all criteria and completed all assessments (Fig. 1). The median lower extremity composite motor score (Chedoke–McMaster Stroke Assessment) was 7 of 14, indicating moderate impairment. Most subjects had no spasticity in the paretic knee (i.e., spasticity score = 0, n = 28) but mild to moderate spasticity in the paretic ankle (spasticity score = 1–2, n = 37). Severe spasticity (i.e., spasticity score = 3–4) in the paretic knee (n = 1) and ankle (n = 1) was rare. The demographic data are summarized in Table 2.
TABLE 2: Characteristics of subjects (N = 45).
FIGURE 1: Study flow chart. A total of 45 subjects with stroke completed all assessment procedures.
EMG activity of paretic leg VL.
There was an overall significant main effect of WBV intensity (F2,88 = 27.006, P < 0.001, partial η2 = 0.380) and exercise (F7,308 = 29.846, P < 0.001, partial η2 = 0.404) (Fig. 2A). The intensity–exercise interaction effect was also significant (F14,616 = 2.312, P = 0.031, partial η2 = 0.050). In post hoc analysis of the main effect of intensity, both the low WBV intensity (P < 0.001) and the high WBV intensity (P < 0.001) protocols induced significantly higher EMG amplitude than the control condition, no matter what exercise was performed. The difference in EMG amplitude was not significant, however, between the low-intensity and the high-intensity WBV protocols (P = 0.744). Regarding the main effect of exercise, deep squat position induced significantly higher paretic VL EMG amplitude than other exercises, regardless of WBV intensity (all P < 0.001).
FIGURE 2: Effect of WBV on EMG amplitude in the paretic leg. The EMGrms amplitude of the VL (A) and GS (B) was expressed as a percentage of that recorded during the MVC (vertical axis) in each test condition is displayed. The EMG amplitude recorded in the no-WBV, low-intensity WBV, and high-intensity WBV conditions is represented by black, gray, and white vertical bars, respectively. Eight exercises were tested: upright standing (ST), semisquat (SS), deep squat (DS), weight shifted forward (FWS), weight shifted backward (BWS), weight shifted to the side (WSTS), forward lunge (FL), and single-leg standing (SLS). The error bars represent 1 SD from the mean. *Significant difference from the no-WBV condition. The same conventions are used in other figures. Adding WBV led to significant increase in paretic leg VL and GS EMG amplitude.
EMG activity of paretic leg GS.
The main effect of intensity (F2,88 = 36.728, P < 0.001, partial η2 = 0.465) and exercise (F7,308 = 6.858, P < 0.001, partial η2 = 0.135) as well as the intensity–exercise interaction effect (F14,616 = 2.701, P = 0.046, partial η2 = 0.058) were all significant (Fig. 2B). Post hoc analysis of the main effect of WBV intensity revealed that the EMG amplitude among the three WBV conditions were all significantly different from each other (P < 0.01). However, the difference in EMG amplitude between the low-intensity and the high-intensity protocols was not significant in any of the exercises after Bonferroni adjustment. Post hoc analysis of the main effect of exercise showed that the weight-shifted-forward position resulted in higher EMG than most of the other exercises (P < 0.01).
EMG activity of nonparetic leg VL.
The main effect of intensity (F2,88 = 30.887, P < 0.001, partial η2 = 0.412) and exercise (F7,308 = 79.302, P < 0.001, partial η2 = 0.643) and the intensity–exercise interaction were all significant (F14,616 = 8.380, P < 0.001, partial η2 = 0.160) (Fig. 3A). Post hoc analysis on the effect of WBV intensity showed that adding the low-intensity or high-intensity WBV induced an overall increase in EMG amplitude when compared with the control condition (P < 0.001). However, there was no significant difference in EMG amplitude between low-intensity and high-intensity WBV conditions (P = 0.071). Post hoc analysis on the effect of exercise showed that the EMG amplitude during the deep squat position was significantly higher than other body postures (P < 0.001). Deep squat position was also the only exercise in which adding WBV induced no significant increase in nonparetic VL EMG amplitude (P > 0.05) (Fig. 3A).
FIGURE 3: Effect of WBV on EMG amplitude in the nonparetic leg. Both high- and low-intensity WBV significantly increased nonparetic leg VL (A), except in deep squat exercise. In nonparetic leg GS (B), both WBV protocols induced significantly higher EMG muscle activity, except in weight-shifted-forward exercise.
EMG activity of nonparetic leg GS.
Significant main effects of intensity (F2,88 = 19.062, P < 0.001, partial η2 = 0.302) and exercise (F7,308 = 17.080, P < 0.001, partial η2 = 0.280) were found (Fig. 3B). The intensity–exercise interaction was also significant (F14,616 = 2.994, P = 0.033, partial η2 = 0.064). Post hoc analysis showed that the nonparetic GS EMG amplitude was significantly lower when no WBV was added (P < 0.001). No significant difference in EMG amplitude was found between low-intensity and high-intensity WBV conditions (P = 0.109). Contrast analysis of the effect of exercise revealed that the weight-shifted-forward position had significantly higher EMG amplitude than other postures (P < 0.01). It was also the only exercise that did not show a significant increase in EMG when WBV was added (P > 0.05) (Fig. 3B).
Paretic to nonparetic EMG amplitude ratio.
The EMGrms ratio of paretic to nonparetic side is shown in Figure 4. The ratio was greater than 1 in all conditions, denoting that the paretic leg achieved a greater %MVC in these conditions than the nonparetic side. For the VL muscle (Fig. 4A), the main effect of WBV intensity was not significant (P = 0.34, partial η2 = 0.02), whereas the main effect of exercise was significant (P <0.001, partial η2 = 0.37), with the weight-shifted-to-the-side and single-leg-standing positions yielding significantly higher paretic to nonparetic EMG ratios than other exercises (P < 0.01). There was an overall significant frequency–exercise interaction effect (P < 0.001, partial η2 = 0.20), with the weight shifted to the side and single-leg standing showing significant reduction in the EMG ratio as high-intensity WBV was added (P = 0.002). For the GS muscle (Fig. 4B), there was an overall significant main effect of exercise (P < 0.001, partial η2 = 0.15), with the weight-shifted-forward exercise showing significantly lower level of EMG ratio than all other exercises (P < 0.05), except upright standing. The main effect of intensity (P = 0.53, partial η2 = 0.01) and intensity–exercise interaction effect (P = 0.39, partial η2 = 0.03) were not significant.
FIGURE 4: Ratio of EMG amplitude of the paretic leg to the nonparetic leg. A ratio greater than 1 is indicative of higher %MVC achieved on the paretic side relative to the nonparetic side for VL (A) and GS (B). The WSTS and the SLS exercises showed a significant reduction in the VL EMG ratio as WBV intensity was increased (A).
Relationship between spasticity and EMG data.
Generally, no relationship was found between normalized EMGrms and spasticity of the paretic knee and ankle (P > 0.05). The only exceptions were a negative association of the ankle spasticity score with the standing posture in the low-intensity WBV (rho = −0.356, P = 0.016) and high-intensity WBV (rho = −0.316, P = 0.035) conditions.
DISCUSSION
This is the first study to investigate the influence of different WBV intensities and exercises and their interactions on leg muscle activity in individuals with chronic stroke. The hypothesis of this study was confirmed because the results showed that adding WBV significantly enhanced muscle activity in VL and GS on both the paretic and the nonparetic sides in all eight different exercise conditions. With a few exceptions, the added WBV enhanced EMG activity in the paretic and nonparetic leg muscles to a similar extent in a variety of exercise conditions.
Effect of WBV intensity.
The results showed that the EMG amplitude of all leg muscles measured was significantly enhanced by adding either the low-intensity or high-intensity WBV. The increase in EMG amplitude ranged from 26% to 165%, from 76% to 243%, from 4% to 253%, and from 14% to 236% for paretic VL, paretic GS, nonparetic VL, and nonparetic GS, respectively, depending on the exercises performed. Our results are generally in line with those from other studies in healthy adults, which also reported a significant increase in EMG magnitude of different leg muscle groups during WBV exposure (5,36). The magnitude of WBV-induced increase in EMG activity differed across the various studies probably due to the use of different populations, vibration devices, frequencies, amplitudes, and data processing methods. For example, Pollock et al. (34) found that adding WBV (5–30 Hz, 2.5–5.5 mm) increased EMG amplitude of various leg muscles by 5%–50% in a sample of 12 healthy adults. Other studies have shown that WBV at 30–45 Hz and amplitudes of 2–5 mm led to augmentation of leg muscle activity up to 34.5% in young adults (5,36).
It is unlikely that the increase in EMG was due to increased spasticity on the paretic side. First, spasticity should have little influence on our results as severe spasticity in either the knee or ankle in the paretic leg was observed in one subject only. Second, no strong relationship was found between the severity of spasticity and the EMG amplitude. Of the two significant correlations identified, the direction of the relationship was negative, indicating that higher EMG amplitude was associated with less severe spasticity. Finally, a previous study reported that ankle spasticity in stroke patients, as indicated by the Modified Ashworth Scale, was significantly reduced in the WBV group, but not in the control group, after a single session of WBV (6).
It is interesting that our low- and high-intensity WBV protocols are equally effective in increasing the EMG activity of all measured muscles in subjects with chronic stroke. This is in contrast with previous studies in young adults, which showed that higher WBV frequencies are associated with higher EMG amplitude (5,14,34). The discrepancies in results may be due to several reasons. First, the subject characteristics are different (chronic stroke vs young healthy adults). The presence of neurological pathology and changes in muscle properties poststroke may lead to very different response to the same WBV stimuli. Second, the WBV protocols used also differ. The protocols used in this study have enabled us to determine the differential effects of a subgravity protocol (0.96g) and a supragravity protocol (1.61g). However, the difference in intensity between the two protocols may not be substantial enough to induce different levels of muscle activity. Perhaps the difference in muscle activation would have been significant if a higher WBV intensity had been used. We did not use a higher WBV intensity because higher peak accelerations would potentially lead to more substantial health hazards (1,19). This study examined the leg muscle activity during high- and low-intensity WBV only. Whether the two protocols are equally effective in improving muscle function after long-term WBV exercise training awaits further research. To date, only one study has compared the effects of a high-intensity WBV protocol (9.43g, 25 Hz, 3.75 mm) with a low-intensity one (0.50g, 25 Hz, 0.2 mm) in stroke patients after 12 sessions of training over a 6-wk period (4). A significant improvement in paretic knee extension strength was found only in the low-intensity WBV group, but the magnitude of improvement was within the limits of measurement errors, denoting no real clinical change. Certainly, more study is required in this area.
Interaction between exercise and WBV intensity.
A unique aspect of this study is that we examined several different exercises during WBV exposure in an effort to identify what combination of exercise and WBV intensity may induce the highest level of muscle activity. The exercises chosen in this study are commonly used in other WBV trials and stroke rehabilitation (23,32,40). Regular training using functional leg strengthening exercises such as squatting movements and heel raises without WBV (e.g., exercise 2, 3, and 4 in Table 1) has been shown to be effective in increasing leg muscle strength in individuals with stroke (32,40). Interestingly, this study found that the muscle activation levels during these exercises are not particularly high (Figs. 2–4, black bars). It may indicate that the threshold intensity for inducing a positive strength training effect may be less than the typical training intensity (50%–80% maximal effort) used in many previous resistance training trials in stroke (33). Nevertheless, this study showed that for all eight exercises, adding WBV would significantly augment the muscle activation levels. WBV may thus be a viable option for further increasing muscle activity during leg strengthening exercises, thereby leading to better strength gains. Further randomized controlled trials are required to test this hypothesis.
The results also showed that the intensity and exercise interaction effect was significant for all four muscle groups, indicating that the WBV-induced increase in EMG activity achieved differed depending on the exercise. For the VL muscle in both the paretic and the nonparetic legs, the increase in muscle activation with the addition of WBV was significantly less in deep squat exercise when compared with other exercises. For GS, the WBV-induced increase in muscle activation in weight-shifted-forward exercise was significantly less when compared with most of the other exercises. Muscle preactivation could be a potential factor affecting the extent of muscle activation caused by WBV (16). For example, it is noted that the level of activation in VL and GS muscles are already quite high in deep squat exercise and weight-shifted-forward exercise, respectively, even without vibration. The potential for a further increase in muscle activation upon the addition of WBV is thus smaller.
Overall, the deep squat and forward-weight-shift exercises, when combined with WBV, resulted in the highest level of EMG activity in paretic VL and GS, respectively. The results thus suggested that these two exercises may be more effective in WBV training programs for enhancing strength of the respective muscles in subjects with chronic stroke. Mikhael et al. (28) studied the effect of standing posture during WBV training on muscle strength outcomes. Interestingly, they found that WBV with flexed knees induced similar gain in leg press strength compared with WBV with locked knees after 29 sessions of training for a 13-wk period. However, the sample size is small (19 subjects), thus making it difficult to draw meaningful conclusions.
Analysis of paretic to nonparetic EMG amplitude ratio.
The analysis of the paretic EMG to nonparetic EMG ratio provided us with some insight into the activation of the paretic leg relative to the nonparetic leg in different WBV conditions. The ratio was greater than 1.0 in all test conditions, indicating that the muscle activity in the paretic leg achieved a greater %MVC in these conditions relative to the nonparetic side. It was most likely due to the fact that the nonparetic leg was much stronger than the paretic leg, as reflected by the greater EMG amplitude recorded during MVC (Table 1). As the EMG amplitude measured in different WBV conditions was normalized according to the EMG data recorded during MVC, it is not surprising that the paretic leg would tend to show a higher normalized EMGrms value compared with the nonparetic leg when performing the same activity, which explained why the ratios were greater than 1.0. The results showed that the choice of exercise did affect the EMG ratio. In general, the weight-shifted-to-the-side and single-leg standing positions resulted in the highest ratios (Fig. 4), mostly due to the relative low level of muscle activation in the nonparetic leg when these two postures were assumed (Fig. 3). In contrast, the semi-squat and deep-squat positions, which involved greater knee and ankle flexion angles, required a higher level of VL muscle activation even on the nonparetic side (Fig. 3). This may in turn account for the lower paretic/nonparetic EMG ratio in VL (Fig. 4A). Similarly, the weight-shifted-forward posture induced a high level of EMG activity in the nonparetic GS muscle, thereby accounting for the lower EMG amplitude ratios (Fig. 4B).
There was no main effect of WBV intensity for both VL and GS EMG amplitude ratios, meaning that application of WBV resulted in similar activation of the paretic and the nonparetic leg muscles in general. The only exception was the weight-shifted-to-the-side and single-leg standing exercises, which demonstrated substantial reduction in the VL EMG ratio as WBV intensity was increased (Fig. 4A), thereby contributing to the significant exercise–intensity interaction effect. This finding indicated that the increasing WBV intensity induced a greater EMG response in the nonparetic VL than the paretic VL when performing the weight-shifted-to-the-side and single-leg standing exercises. The differential response to alterations in WBV intensity was more apparent in these two exercises, probably because the body weight was borne primarily by the exercising leg whereas in the other six exercises, the weight bearing was shared by both legs.
Limitations and future research directions
First, because all of our subjects are ambulatory and community dwelling, the results are only generalizable to a population with similar characteristics. Second, we studied the effects of the overall intensity of WBV (indicated by peak acceleration) on leg EMG activity. However, WBV frequency and amplitude could have independent contribution to muscle activation (34). Pollock et al. (34) demonstrated that WBV amplitude is positively correlated with muscle performance while others believed that frequency is the most important variable in WBV (18). However, the vibration platform used in this study did not allow us to adjust the frequency and amplitude of WBV independently. Hence, the isolated contribution of frequency and amplitude on leg muscle activation requires further study. Third, the EMG amplitude was used as the outcome. Although no muscle torque measurements were done, it is known that EMG amplitude has a strong, positive relationship with muscle force in isometric conditions (21). It is thus reasonable to assume that the muscle force was increased during WBV exposure among our subjects. In addition, the VL and GS muscles were measured because of their key roles in gait and other functional tasks (10,20). Among the various knee extensor muscles (e.g., rectus femoris, vastus medialis, etc.), VL was selected because it has been examined in several previous studies and would facilitate the comparison of results (5,14,36). There is also no consistent evidence proving that the activation of VL relative to other knee extensors is significantly different in various knee extension or squatting exercises in healthy individuals (7,17). However, it is acknowledged that the flexor muscle groups are also important for daily function. For example, toe drag during the swing phase of walking owing to decreased activation of the ankle dorsiflexors on the paretic side is a common clinical observation in hemiparetic gait (25). The response to WBV in the flexor muscle groups after stroke will need further investigations. Finally, while this study showed that WBV could significantly augment leg muscle activity during the performance of various static exercises, whether improvement in muscle strength can be induced by these WBV protocols after a longer intervention period (e.g., 8–10 wk) is uncertain. A randomized controlled study with measurement of maximum voluntary torque as the outcome will be required to test this hypothesis.
CONCLUSIONS
In conclusion, the present study suggested that leg muscle activity on both the paretic and nonparetic sides was increased significantly by adding the low-intensity and high-intensity WBV. The added WBV induced a similar increase in EMG activity in the paretic and nonparetic legs, except in weight-shifted-to-the-side and single-leg standing exercises, where the nonparetic leg VL was more responsive to the added WBV than the paretic VL muscle. A randomized controlled trial will be required to determine whether these two protocols could induce any gain in muscle strength in stroke patients following long-term WBV exercise training, and whether the high-intensity protocol could lead to better muscle strength than the low-intensity one.
This work described in this paper was substantially supported by a general research fund provided by the Research Grants Council of the Hong Kong Special Administrative Region, China (Project No. PolyU 5245/11E).
The authors declare that they have no conflict of interest. The results of the present study do not constitute endorsement by the American College of Sports Medicine.
REFERENCES
1. Abercromby AFJ, Amonette WE, Layne CS, McFarlin BK, Hinman MR, Paloski WH. Variation in neuromuscular responses during acute whole-body vibration exercise.
Med Sci Sports Exerc. 2007; 39 (9): 1642–50.
2. Ahlborg L, Andersson C, Julin P. Whole-body vibration training compared with resistance training, effects on spasticity, muscle strength and motor performance in adults with cerebral palsy.
J Rehabil Med. 2006; 38 (5): 302–8.
3. Bohannon BW, Smith MB. Interrater reliability of a Modified Ashworth Scale of muscle spasticity.
Phys Ther. 1987; 67 (2): 206–7.
4. Brogardh C, Flansbjer U-B, Lexell J. No specific effect of whole-body vibration training in chronic stroke: a double-blind randomized controlled study.
Arch Phys Med Rehabil. 2012; 93 (2): 253–8.
5. Cardinale M, Lim J. Electromyography activity of vastus lateralis muscle during whole-body vibrations of different frequencies.
J Strength Cond Res. 2003; 17 (3): 621–4.
6. Chan K-S, Liu C-W, Chen T-W, Weng M-C, Huang M-H, Chen C-H. Effects of a single session of whole body vibration on ankle plantarflexion spasticity and gait performance in patients with chronic stroke: a randomized controlled trial.
Clin Rehabil. 2012; 26 (12): 1087–95.
7. Earl JE, Schmitz RJ, Arnold BL. Activation of the VMO and VL during dynamic mini-squat exercises with and without isometric hip adduction.
J Electromyogr Kinesiol. 2001; 11 (6): 381–6.
8. Eckhardt H, Wollny R, Müller H, Bärtsch P, Friedmann-Bette B. Enhanced myofiber recruitment during exhaustive squatting performed as whole-body vibration exercise.
J Strength Cond Res. 2011; 25 (4): 1120–5.
9. Feigin VL, Lawes CMM, Bennett DA, Barker-Collo SL, Parag V. Worldwide stroke incidence and early case fatality reported in 56 population-based studies: a systematic review.
Lancet Neurol. 2009; 8 (4): 355–69.
10. Flansbjer U-B, Downham D, Lexell J. Knee muscle strength, gait performance, and perceived participation after stroke.
Arch Phys Med Rehabil. 2006; 87 (7): 974–80.
11. Flansbjer UB, Lexell J, Brogårdh C. Long-term benefits of progressive resistance training in chronic stroke: a 4-year follow-up.
J Rehabil Med. 2012; 44 (3): 218–21.
12. Gowland C, Stratford P, Ward M, et al. Measuring physical impairment and disability with the Chedoke–McMaster Stroke Assessment.
Stroke. 1993; 24 (1): 58–63.
13. Gracies J-M. Pathophysiology of spastic paresis. I: Paresis and soft tissue changes.
Muscle Nerve. 2005; 31 (5): 535–51.
14. Hazell TJ, Kenno KA, Jakobi JM. Evaluation of muscle activity for loaded and unloaded dynamic squats during vertical whole-body vibration.
J Strength Cond Res. 2010; 24 (7): 1860–5.
15. Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G. Development of recommendations for SEMG sensors and sensor placement procedures.
J Electromyogr Kinesiol. 2000; 10 (5): 361–74.
16. Issurin VB, Tenenbaum G. Acute and residual effects of vibratory stimulation on explosive strength in elite and amateur athletes.
J Sports Sci. 1999; 17 (3): 177–82.
17. Jakobsen MD, Sundstrup E, Andersen CH, et al. Muscle activity during knee-extension strengthening exercise performed with elastic tubing and isotonic resistance.
Int J Sports Phys Ther. 2012; 7 (6): 606–16.
18. Jordan MJ, Norris SR, Smith DJ, Herzog W. Vibration training: an overview of the area, training consequences, and future considerations.
J Strength Cond Res. 2005; 19 (2): 459–66.
19. Kiiski J, Heinonen A, Järvinen TL, Kannus P, Sievänen H. Transmission of vertical whole body vibration to the human body.
J. Bone Miner Res. 2008; 23 (8): 1318–25.
20. Kluding P, Gajewski B. Lower-extremity strength differences predict activity limitations in people with chronic stroke.
Phys Ther. 2009; 89 (1): 73–81.
21. Kuriki HU, de Azevedo FM, Takahashi LSO, Mello EM, Filho RFN, Alves N. The relationship between electromyography and muscle force. In: Schwartz M, editor.
EMG Methods for Evaluating Muscle and Nerve Function. Manhattan: Intech; 2012. p. 32–54.
22. Lam FMH, Lau RWK, Chung RCK, Pang MYC. The effect of whole body vibration on balance, mobility and falls in older adults: a systematic review and meta-analysis.
Maturitas. 2012; 72 (3): 206–13.
23. Lau RWK, Liao L-R, Yu F, Teo T, Chung RCK, Pang MYC. The effects of whole body vibration therapy on bone mineral density and leg muscle strength in older adults: a systematic review and meta-analysis.
Clin Rehabil. 2011; 25 (11): 975–88.
24. Lau RWK, Yip SP, Pang MYC. Whole-body vibration has no effect on neuromotor function and falls in chronic stroke.
Med Sci Sports Exerc. 2012; 44 (8): 1409–18.
25. Lin P-Y, Yang Y-R, Cheng S-J, Wang R-Y. The relation between ankle impairments and gait velocity and symmetry in people with stroke.
Arch Phys Med Rehabil. 2006; 87 (4): 562–8.
26. Madou KH. Leg muscle activity level and rate of perceived exertion with different whole-body vibration frequencies in multiple sclerosis patients: an exploratory approach.
Hong Kong Physiother J. 2011; 29 (1): 12–9.
27. Mehta S, Pereira S, Viana R, et al. Resistance training for gait speed and total distance walked during the chronic stage of stroke: a meta-analysis.
Top Stroke Rehabil. 2012; 19 (6): 471–8.
28. Mikhael M, Orr R, Amsen F, Greene D, Singh MAF. Effect of standing posture during whole body vibration training on muscle morphology and function in older adults: a randomised controlled trial.
BMC Geriatr. 2010; 10: 74.
29. Pallant J.
SPSS Survival Manual. 4th ed. New York: McGraw-Hill Education; 2007. p. 254.
30. Pang MYC, Cheng AQ, Warburton D, Jones AYM. Relative impact of neuromuscular and cardiovascular factors on bone strength index of the hemiparetic distal radius epiphysis among individuals with chronic stroke.
Osteoporos Int. 2012; 23 (9): 2369–79.
31. Pang MYC, Charlesworth SA, Lau RWK, Chung RCK. Using aerobic exercise to improve health outcomes and quality of life in stroke: evidence-based exercise prescription recommendations.
Cerebrovasc Dis. 2013; 35 (1): 7–22.
32. Pang MYC, Eng JJ, Dawson AS, McKay HA, Harris JE. A community-based fitness and mobility exercise program for older adults with chronic stroke: a randomized controlled trial.
J Am Geriatr Soc. 2005; 53 (10): 1667–74.
33. Patten C, Lexell J, Brown HE. Weakness and strength training in persons with poststroke hemiplegia: rationale, method, and efficacy.
J Rehabil Res Dev. 2004; 41 (3a): 293–312.
34. Pollock RD, Woledge RC, Mills KR, Martin FC, Newham DJ. Muscle activity and acceleration during whole body vibration: effect of frequency and amplitude.
Clin Biomech (Bristol, Avon). 2010; 25 (8): 840–6.
35. Randall JM, Matthews RT, Stiles MA. Resonant frequencies of standing humans.
Ergonomics. 1997; 40 (9): 879–86.
36. Roelants M, Verschueren SMP, Delecluse C, Levin O, Stijnen V. Whole-body-vibration-induced increase in leg muscle activity during different squat exercises.
J Strength Cond Res. 2006; 20 (1): 124–9.
37. Tihanyi J, Di Giminiani R, Tihanyi T, Gyulai G, Trzaskoma L, Horváth M. Low resonance frequency vibration affects strength of paretic and non-paretic leg differently in patients with stroke.
Acta Physiol Hung. 2010; 97 (2): 172–82.
38. Torvinen S, Kannu P, Sievänen H, et al. Effect of a vibration exposure on muscular performance and body balance. Randomized cross-over study.
Clin Physiol Funct Imaging. 2002; 22 (2): 145–52.
39. van Nes IJ, Latour H, Schils F, Meijer R, van Kuijk A, Geurts AC. Long-term effects of 6-week whole-body vibration on balance recovery and activities of daily living in the postacute phase of stroke.
Stroke. 2006; 37 (9): 2331–5.
40. Yang Y-R, Wang R-Y, Lin K-H, Chu M-Y, Chan R-C. Task-oriented progressive resistance strength training improves muscle strength and functional performance in individuals with stroke.
Clin Rehabil. 2006; 20 (10): 860–70.
