Effects of Electric Stimulation−Assisted Cycling Training in People With Chronic Stroke

Article Outline

• Abstract
• Methods
  • Participants
  • Experimental Design
  • ES-Assisted Cycling Exercise
  • Functional Performance
  • Graded Exercise Test
  • Muscle Strength
  • Training
  • Statistical Analysis
• Results
  • Training Progression
  • Training Effects
• Discussion
  • Training Program
  • Cycling Performance and Aerobic Capacity
  • Muscle Strength
  • Functional Performance
  • Electric Stimulation
  • Study Limitations
• Conclusions
• Acknowledgments
• References
• Copyright

Abstract 

Janssen TW, Beltman JM, Elich P, Koppe PA, Konijnenbelt H, de Haan A, Gerrits KH. Effects of electric stimulation–assisted cycling training in people with chronic stroke.

Objective

To evaluate whether leg cycling training in subjects with chronic stroke can improve cycling performance, aerobic capacity, muscle strength, and functional performance and to determine if electric stimulation (ES) to the contralateral (paretic) leg during cycling has additional effects over cycling without ES.

Design

A randomized controlled trial, with a partial double-blind design.

Setting

A rehabilitation center.

Participants

Twelve stroke patients (range, 18–70y), more than 5 months poststroke, with lower-extremity hemiparesis.

Intervention

Subjects were randomly assigned to groups that performed cycling exercise, one with ES evoking muscle contractions and a control group with ES not evoking muscle contractions. Subjects, blinded for group assignment, trained twice a week for 6 weeks.

Main Outcome Measures

Changes in aerobic capacity and maximal power output, functional performance, and lower-limb muscle strength.

Results

Aerobic capacity and maximal power output significantly increased by 13.8%±19.1% and 38.1%±19.8%, but muscle strength was not significantly enhanced after training. Functional performance improved (ie, scores on the Berg Balance Scale increased by 6.9%±5.8% (P=.000) and the six-minute walk test improved by 14.5%±14.1% (P=.035). There was no significant effect on the Rivermead Mobility Index (P=.165). Training-induced changes were not significantly different between the 2 groups. Changes in cycling performance and aerobic capacity were not significantly related to changes in functional performance.

Conclusions

This study showed that a short cycling training program on a semirecumbent cycle ergometer can markedly improve cycling performance, aerobic capacity, and functional performance of people with chronic stroke. The use of ES had no additional effects in this specific group of subjects with chronic stroke.

Key Words: Aerobic exercise, Cerebrovascular accident, Electric stimulation therapy, Exercise therapy, Rehabilitation

BECAUSE THE INTENSITY of contemporary physical therapy (PT) is generally too low to counteract deconditioning after stroke,¹ exercise therapies such as treadmill or bicycle exercise are necessary to improve cardiovascular fitness in patients with stroke.², ³ However, the efficacy of such a training paradigm may be limited in patients with balance problems or unable to walk. Cycling exercise, which requires less balance capability, can also improve functional mobility.⁴, ⁵, ⁶ However, because the hemiplegic leg can only be partly activated, cycling performance and exercise intensity may be relatively low, thereby limiting the training stimulus. Moreover, in theory, because the paralyzed muscle fibers are not active during training, they are likely to atrophy and become weaker and less fatigue resistant. If, in time, spontaneous recovery occurs and voluntary activation of these previously paralyzed fibers is again possible, they first need to be retrained to optimize functional performance, which elongates the time for functional recovery.

A method that might solve the problem of insufficient and inadequate muscle fiber activation is the application of electric stimulation (ES) to the contralateral (or paretic) leg during cycling. ES can increase the number of activated muscle fibers, including paralyzed fibers, which, in turn, may increase metabolic activity. ES has indeed, mostly successfully, been used in therapy for persons with stroke to enhance walking⁷, ⁸ and arm function⁹, ¹⁰, ¹¹ but not yet during cycling. During the past 2 decades, cycling with ES has been used in people with spinal cord injury (SCI) with predominantly beneficial results,¹², ¹³, ¹⁴, ¹⁵, ¹⁶ such as improved muscle mass and strength, circulation, and increased metabolic activity.¹⁷ According to Kralj and Bajd,¹⁸ ES not only affects the nerve fibers going to the muscles but could also travel to higher brain centers, potentially stimulating reorganization of neuromuscular activity. Hence, the application of ES to the contralateral leg during cycling might be a promising therapeutic tool during rehabilitation of persons with stroke.

A cycle training program with ES might lead to more improvements in cycling performance, aerobic capacity, and functional and muscle performance than without ES. The goals of this study were therefore to evaluate whether (1) a cycling training in people with stroke can improve cycling performance and aerobic capacity, muscle strength, and functional performance; (2) ES to the contralateral leg during cycling has more effects than cycling without ES; and (3) training-related changes in cycling performance, aerobic capacity, and muscle strength are related to changes in functional performance. To minimize effect bias caused by spontaneous recovery, this study only included subjects with chronic stroke.

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Methods 

Participants 

Sixteen patients with stroke, all outpatients of the Rehabilitation Center Amsterdam, participated in this study after medical screening and after having signed an informed consent form approved by the institutional review board. Inclusion criteria were age between 18 and 70, more than 5 months after stroke, and hemiparesis of the lower extremity (as determined by the rehabilitation physician). Exclusion criteria were severe cognitive, communicative, perceptual, or sensory problems preventing understanding and/or following verbal instructions; other neurologic or psychiatric problems causing difficulties following the program; lower-extremity impairments making cycling impossible, such as orthopedic hip or knee problems; unstable cardiorespiratory problems; and the inability to tolerate ES and/or contraindication to it (epilepsy, cancer, skin problems, pacemaker, pregnancy). The level of functional walking ability was rated with the Functional Ambulation Category (FAC) (range, 0–5, with 5 being the best score) by a trained physical therapist. The high average FAC scores (≈4.5) indicate that the subjects generally had a good level of mobility. None of the subjects received regular PT or other treatment.

Experimental Design 

Before baseline testing, the subjects were randomly assigned to 1 of 2 groups: a group performing leg cycling exercise with maximally tolerable ES (ES-LCE) that evoked muscle contractions and a control group (LCE) performing cycling with just sensible ES (ie, the stimulation could just be felt but did not evoke muscle contractions). The goal of the latter procedure was to blind the subjects for group assignment. We informed all subjects before the experiments that they would receive ES, without disclosing the exact degree of ES or the fact that 1 group would receive more than the other. Hence, they were unaware that contractions were important and only focused on the fact that they received ES. Before the training period, subjects came once to the laboratory to get acquainted with the cycle ergometer and to determine the individually preferred cadence and current amplitude of the ES. In 2 subsequent sessions, baseline measurements (cycling graded exercise test [GXT], functional performance test, muscle strength test) were performed, separated by at least 1 day. After the 6-week training program, the same measurements were performed during 2 separate sessions.

ES-Assisted Cycling Exercise 

All cycling was performed on a semirecumbent Ergys2 bicycle ergometer.^a The ergometer, originally developed for people with SCI, uses computer-controlled ES to activate the quadriceps, gluteal, and hamstring muscles. In the (adapted) Ergys2, several parameters can be set, including the target cadence. The Ergys2 raises the current amplitude to a predefined maximum when cadence falls below the target cadence, most commonly because of fatigue. The purpose of this procedure is to recruit additional muscle fibers to maintain the target cadence. When cadence is above the target cadence, current amplitude will decrease again. To ensure that subjects received maximal ES during (almost) the entire training in the present experiments, the target cadence was set higher than the individually preferred cadence. The ES current amplitude for the ES-LCE group was set as high as tolerated, resulting in current levels that induced muscle contractions in all subjects, as determined by visual observation. For the LCE group, the current was set to just sensible stimulation not evoking muscle contractions. The stimulation used was a 60-Hz symmetrical, biphasic sine pulse and a pulse duration of 450μs.

Functional Performance 

Functional performance was evaluated by 3 tests. Walking ability and endurance capacity were evaluated by performing a six-minute walk test (6MWT).¹⁹ Subjects were rated on their balancing skills by using the Berg Balance Scale (BBS) (range, 0–56).²⁰ The 6MWT and the BBS were determined by an experienced physical therapist, blinded for group assignment. Mobility was rated by a self-assessment questionnaire, the Rivermead Mobility Index (RMI) (range, 0–15).²¹ The test concentrates on body mobility covering a range of activities from turning over in bed to running and is valid and sensitive to changes over time.²²

Graded Exercise Test 

Each subject performed without ES a continuous progressive GXT at the subject’s preferred cadence. Resistance was increased every 2 minutes until this cadence could no longer be maintained because of exhaustion. Resistance and cadence were measured at 60Hz to calculate power output. A moving average, the unweighted mean of the previous 30 seconds, was calculated, and maximal power output (POmax) was defined as the highest 30-second average. Aerobic metabolism was determined by measuring oxygen uptake (V̇o₂) by using open-circuit spirometry.^b The highest measured V̇o₂ (V̇o₂max), averaged over 20 seconds, was defined as the maximal aerobic capacity. Heart rate was monitored by using a Polar Sport Tester.^c

Muscle Strength 

Maximal knee extension torque of both legs was evaluated while subjects were sitting on a custom-built chair with hip and knee angles at 90° (0° is full extension).²³ The leg was fixed by a bar placed against the shin connected to a force transducer. Straps restrained the hips and shoulders, reducing movements and making sitting for subjects with balance problems more comfortable. The length of the moment arm, measured from the lateral femoral epicondyle to the center of the force transducer, was kept constant (.26m). The subjects performed isometric maximal voluntary contractions (MVCs) until torque did not further increase with a maximum of 5 attempts. Extension torque data were sampled at 1000Hz and filtered by using a fourth-order low-pass digital Butterworth filter with a 50-Hz cutoff frequency.

Training 

Subjects trained twice a week during 6 weeks for a total of 12 sessions. Because they were relatively sedentary outpatients and needed much time and effort to come to the rehabilitation center, we chose to limit the sessions to 2 a week to prevent overburdening these subjects. The goal of each session, consisting of at least 3 exercise bouts, was to achieve a total of 25 to 30 minutes of exercise. The target time for each exercise bout was between 5 and 10 minutes, followed by a 5-minute rest interval. The resistance was systematically increased every 2 minutes during the exercise bout. The initial level was established by the pretraining GXT. The level was adjusted for each subsequent bout to maintain the 5- to 10-minute target, ensuring continuous overload as exercise capability increased. During each session, the highest power output attained (POpeak) was calculated with a moving average, again by using a 30-second window size.

The maximal exercise intensity of each training was estimated by the highest heart rate (HRpeak) during the training (calculated with a moving average by using a 30-s window size), expressed as a percentage of the individual heart rate reserve ([HRpeak – resting HR]/[maximal HR – resting HR] ×100%). The maximal and resting heart rate were defined as the highest and the lowest recorded heart rate, respectively, during the whole training period, including the GXTs.

Statistical Analysis 

Results are presented in graphs (individual data) and as means ± standard deviations (SDs). Data were analyzed by a general linear model analysis of variance with repeated measures. Bonferroni post hoc comparisons were performed where appropriate. A bivariate, 2-tailed, Pearson correlation analysis evaluated possible relations among changes in functional performance, muscle strength, cycling performance, and aerobic capacity. The significance level was set at α equal to .05.

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Results 

Of the 16 subjects who met the inclusion criteria, 12 completed the study. There were no significant differences between the 2 groups for any of the relevant subject characteristics (table 1). Three subjects withdrew because they were not able to fit the training sessions into their weekly schedule, and 1 was excluded because of health problems not related to the cycling. Of those who completed the study, 6 had randomly been assigned to the ES-LCE group and 6 to the LCE group. Because of technical reasons, V̇o₂ data of 1 subject and torque data of the ipsilateral (nonparetic) leg of 2 subjects are missing. The ES was well tolerated by most subjects in the ES-LCE group. None of the subjects showed signs of serious discomfort, and no balance problems during the cycling exercise were reported.

Table 1. Characteristics for the Subjects Who Performed ES-LCE and for Those Subjects Who Performed Regular LCE

NOTE. There were no significant differences between the 2 groups for any of these variables.

Abbreviation: CVA, cerebrovascular accident.

Training Progression 

In the first training, POpeak, expressed relative to the highest POpeak reached during the total training period, was 63.6%±11.9% for the total group, which increased significantly (P=.000) to 94.4%±7.2% in the last training session. There was no difference (P=.315) in the increase in POpeak between the groups. For the total subject group, maximal exercise intensity increased significantly (P=.000) from 70.6%±12.6% of heart rate reserve (HRR) in the first week to 84.7%±14% of HRR in the last week, with a similar (P=.152) increase for both groups.

Training Effects 

Individual responses to the training program in aerobic capacity, cycling performance, muscle strength, and functional performance are shown in figure 1 and summarized in table 2. V̇o₂max significantly increased for the total group by 13.8%±19.1% (P=.039). The majority of subjects (n=9) showed an increase in V̇o₂max (fig 1A), and this increase was similar for both groups (P=.758). POmax increased in all subjects (fig 1B), with an average increase of 38.1%±19.8% (P=.000) and with similar (P=.534) increases for both groups.

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• Fig 1. 

  Individual data before (pre) and after (post) 6 training weeks of (A) V̇o₂max, (B) POmax, (C) MVC torque in the contralateral leg (CL), (D) MVC torque in the ipsilateral leg (IL), (E) BBS score, (F) 6MWT, and (G) RMI score. Legend: dashed lines are the lines of identity; open triangles denote the ES-LCE group; and closed circles indicate the LCE group.

Table 2. Effects of the Training Program on Physiologic Parameters and Indices of Functional Performance

NOTE. Values are mean ± SD.

Abbreviation: GLM, general linear model.

Before training, MVC torque of the contralateral leg was 61.5%±30% of that of the ipsilateral leg. Furthermore, MVC of the contralateral leg (fig 1C) remained unaltered after training (P=.524), but MVC tended to be somewhat increased (by 9.5%) (P=.151) in the ipsilateral leg (fig 1D), with no differences between ES-LCE and LCE (P=.834).

After the training period, functional performance had increased. All (but 1) subjects showed an improved BBS (fig 1E), with an average increase of 6.9%±5.8% (P=.000). Furthermore, the improved BBS tended (P=.079) to be larger in the ES-LCE group than in the LCE group (10.4% vs 4.1%). The mean increase on the 6MWT was 14.5%±14.1% (P=.035), and this increase was not significantly (P=.994) different between groups (fig 1F). Finally, the RMI remained unaltered after the training (P=.165).

Significant correlations were found between improvements in V̇o₂max and POmax (r=.91, P=.000) and between improvements on the 6MWT and the BBS (r=.64, P=.026). No significant correlations were found between relative changes in V̇o₂max or POmax and relative changes in BBS and 6MWT.

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Discussion 

The main findings of this study are that a relatively short training program increased cycling performance, aerobic capacity, and functional performance but not voluntary muscle strength in patients with chronic stroke and that ES of the contralateral leg during cycling had no marked additional beneficial effects.

Training Program 

To our knowledge, this is the first study imposing cycle exercise training in combination with ES in patients with chronic stroke. The cycle ergometer was comfortable for all subjects, no balance problems were encountered, and the training was mostly well tolerated. The protocol was designed to induce maximal exercise responses at least 3 times a session. Such a training regimen may provide more overload and a better adjustment to improved performance capabilities than the commonly used training protocol of 30 minutes of continuous submaximal exercise.²⁴ Because the effects of this training on aerobic capacity and walking performance are similar to previous studies,²⁴ it seems that short bouts of cycling exercise may be equally effective as more endurance type training.

During the relatively short 6-week training program, the maximal exercise intensity increased significantly, possibly because of peripheral muscular adaptations. This could be the result of the muscle fibers becoming more fatigue resistant and/or an increase in the anaerobic threshold and in the use of energy sources. Also, the subjects were relatively sedentary and, hence, not used to exercising strenuously. During this program, they may have been more and more accustomed to experiencing fatigue as a result of the exercise. The fact that these subjects were exercising at a higher intensity at the end of the training program is very promising because it suggests that more cardiorespiratory training effects and concomitant functional benefits than found in the present short training study may be attainable.²⁵

Cycling Performance and Aerobic Capacity 

The training program significantly improved cycling performance and aerobic capacity, similar to other, mostly longer, training studies.²⁴ Although aerobic capacity increased by 13.8%, values were still far below age-matched normative values. In addition, POmax improved more than V̇o₂max, similar to previous reports assessing effects of a 10-week⁶ and 8-week²⁶ cycling training in patients with hemiparetic stroke. This suggests that cycling efficiency improved more than aerobic capacity. Although it is not entirely clear yet if these improvements are at the peripheral or central level and in the contralateral or ipsilateral leg or both, they seem largely caused by peripheral muscular adaptations, supported by the observation that the cardiovascular system was not limiting because subsequent training sessions persistently resulted in higher peak heart rates. Furthermore, subjects often reported that local fatigue in the legs forced them to end the exercise. It remains to be seen if a longer training period can lead to more improvements such that the central cardiorespiratory system becomes the exercise-limiting factor.

An interesting question is to what extent the contralateral leg contributed to the improved exercise performance. Even though subjects were instructed to use both legs equally during cycling, they understandably did not succeed in general. They often reported to predominantly using their ipsilateral leg when resistance increased and stopped exercising because of local fatigue of the ipsilateral leg. Consequently, it is likely that mainly the ipsilateral leg was trained and, therefore, largely responsible for the improved cycling performance, which is supported by the tendency toward an improved strength of the ipsilateral, but not the contralateral, leg. The current setup was not adequate to differentiate the contribution of each leg to the power output. Future studies might provide the necessary insight into the (changes in) contribution of the contralateral leg to the cycling performance.

Muscle Strength 

In contrast to the marked improvements in voluntary cycling performance, no more than a tendency toward improved muscle strength was found in the ipsilateral leg and no changes in the contralateral leg. This may to some extent be explained by the difference in the nature of the exercise (ie, dynamic cycling involving relatively low forces of several muscle groups vs isometric knee extension involving only the quadriceps muscle). In addition, the training did not involve a specific resistance-type exercise with higher forces that may induce more muscle hypertrophy.²⁷ In addition, training-induced structural changes in muscles occur later in time than adaptations in metabolic properties or peripheral circulation.²⁸ It is, therefore, feasible that other muscle performance parameters than muscle strength, such as fatigue resistance of the muscle, improved more after training. Notably, by testing only the knee extensors, possible effects may be underestimated because other muscle groups are also activated during cycling. Moreover, the effects of additional ES may have been more pronounced when studied in muscles that are more problematic in terms of voluntary activation after stroke such as the hamstring muscles.²⁹

Functional Performance 

Because generally no functional recovery from stroke occurs beyond 5 months after onset,³⁰ the improved functional performance in our subjects can likely be ascribed to the training program. These improvements are even more remarkable when considering that the subjects had a relatively good functional capacity as indicated by the high pretraining values for the FAC, BBS, and RMI. Probably because of an obvious ceiling effect, RMI values did not significantly increase, whereas, despite this effect, BBS values did improve significantly. Hence, a promising result is that even a short cycling training program can improve the condition of people with chronic stroke who have a relatively good functional capacity. It is not unlikely that even more and better results may be achieved in individuals with lower functional capacities and/or if training would start sooner after stroke.

BBS values improved on average by 6.9% and the distance during the 6MWT by 14.5%, which is similar to other training studies in patients with stroke.⁴, ³¹, ³², ³³ In a study by Leroux,³¹ 20 subjects with chronic stroke participated in an 8-week group training program specifically aimed at improving balance, coordination, walking ability and endurance, and strength. The BBS improved significantly from 45.4 to 49.6 (9%), but the increase in distance during the 6MWT (171–189m; 11%) was not significant. The results of the present study suggest that cycling exercise can lead to similar improvements in functional performance compared with protocols specifically aimed at improving functional performance.

The improved functional performance, albeit relatively small, may be important for maintaining function and physical independence and reducing the risk of falling.³⁴, ³⁵ By using the equation of Shumway-Cook et al,³⁵ the 6.9% increase in BBS in our subjects indicates that their risk of falling reduced from 33% to 18% and in the ES-LCE group from 61% to 36%, indicating that mobility and fall risk can be markedly improved with this type of training.

Although correlations between training-related changes in cycling performance and aerobic power and changes in functional performance were, as expected, all positive, no significant correlations were found. This could be because of the large variability in performance changes among subjects, but it more likely reflects that functional performance is to a greater degree affected by stroke-specific impairments than by cardiorespiratory fitness. This was also suggested by Pang et al²⁴ who showed that 6MWT distance was markedly stronger related (r=.85) to BBS values than to V̇o₂max (r=.40) in subjects with chronic stroke. Our finding that changes in BBS were more strongly related to changes in 6MWT than V̇o₂max confirms this phenomenon.

Electric Stimulation 

Although both groups markedly improved after training, the degree of improvements did not differ between groups. The BBS of the ES-LCE group tended toward a larger improvement, but because the LCE group started at somewhat higher BBS levels, this tendency may have been caused by a ceiling effect. These results suggest that the addition of ES did not lead to additional improvements. This may be caused by the relatively small muscle mass that was additionally activated by ES. To avoid pain, only a limited number of fibers could be stimulated and only a part thereof was paralyzed, reducing the extra training stimulus of the stimulation. The obvious conclusion would be that the addition of ES to LCE is not useful. However, during the voluntarily performed GXT and the functional performance tests, the subjects were not able to activate the possibly strengthened paralyzed fibers. Hence, for individuals with chronic stroke, whose paralyzed fibers will likely remain paralyzed, the addition of ES to the cycling training does not seem to benefit functional performance. However, the situation may be completely different for those with acute stroke who may regain control over (a part of) these trained paralyzed fibers. The ES-induced activation of these fibers may then prevent their atrophy and loss of strength, thereby potentially shortening the subsequent rehabilitation period needed to restore functional performance. Future research in people with acute stroke may confirm this possibility.

Study Limitations 

Conclusions of the present study are limited by the relatively small subject group. Despite this small sample size, significant improvements in cycling and functional performance could be observed. The lack of a significant difference in outcome between subject groups, however, might be (partially) because of the small group and resulting relatively low power. Moreover, the fact that we had no subject group that did not exercise or performed other exercise limits our ability to indicate the exact causes of the improvements or whether this training is better than other training forms. Another limitation was the variability in the degree of ES that subjects received because of different tolerance levels. We considered applying a lower level of ES that could be tolerated by every subject but chose not to do so because we wanted the maximum effect of the ES. Moreover, a certain level of ES does not necessarily evoke the same contraction in different subjects. It also depends on factors such as skin resistance and the amount of adipose tissue. Therefore, we standardized the degree of ES by applying the maximal tolerable level. Hence, we cannot draw conclusions about the effects of a certain level of ES in terms of milliamperage, but we can draw conclusions about the effects of subjectively tolerable levels of ES.

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Conclusions 

The present study indicates that a short cycling training program on a semirecumbent cycle ergometer is a useful therapeutic tool to improve cycling and functional performance of individuals with chronic stroke. In addition, the functional improvements were paralleled by increased aerobic capacity, but no increase was observed for muscle strength. The improvements in cycling performance and aerobic capacity were not significantly related to those in functional performance. The application of ES to the contralateral leg had no additional effects in this specific group of subjects with chronic stroke.

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Acknowledgments 

We thank Ludeke Lambeek, MSc, Helen Luiting, MSc, Alwin van Drongelen, MSc, Marjan Kok, MSc, Gerko Franken, MSc, Roeland Kleipool, MSc, Marjolein Pennewaard, MSc, and Danielle van Overbeek, MSc, for their assistance in the data collection and analysis.

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References 

1. MacKay-Lyons MJ, Makrides L. Cardiovascular stress during a contemporary stroke rehabilitation program: is the intensity adequate to induce a training effect?. Arch Phys Med Rehabil. 2002;83:1378–1383
   • View In Article
   • Abstract
   • Full Text
   • Full-Text PDF (95 KB)
   • CrossRef
2. Macko RF, DeSouza CA, Tretter LD, et al. Treadmill aerobic exercise training reduces the energy expenditure and cardiovascular demands of hemiparetic gait in chronic stroke patients (A preliminary report). Stroke. 1997;28:326–330
   • View In Article
   • MEDLINE
   • CrossRef
3. Silver KH, Macko RF, Forrester LW, Goldberg AP, Smith GV. Effects of aerobic treadmill training on gait velocity, cadence, and gait symmetry in chronic hemiparetic stroke: a preliminary report. Neurorehabil Neural Repair. 2000;14:65–71
   • View In Article
   • MEDLINE
4. Giuliani CA, Harro CC, Rosecrance JC. The effects of bicycle pedaling on the temporal distance and EMG characteristics of walking in hemiplegic subjects. Phys Ther. 1989;69:367–371
   • View In Article
5. Holt R, Kendrick C, McGlashan K, Kirker S, Jenner J. Static bicycle training for functional mobility in chronic stroke. Phys Ther. 2001;87:257–260
   • View In Article
   • MEDLINE
   • CrossRef
6. Potempa K, Lopez M, Braun LT, Szidon JP, Fogg L, Tincknell T. Physiological outcomes of aerobic exercise training in hemiparetic stroke patients. Stroke. 1995;26:101–105
   • View In Article
   • MEDLINE
   • CrossRef
7. Bogataj U, Gros N, Kljajic M, Acimovic R, Malezic M. The rehabilitation of gait in patients with hemiplegia: a comparison between conventional therapy and multichannel functional electrical stimulation therapy. Phys Ther. 1995;75:490–502
   • View In Article
   • MEDLINE
8. Burridge J, Taylor P, Hagan S, Swain I. Experience of clinical use of the Odstock dropped foot stimulator. Artif Organs. 1997;21:254–260
   • View In Article
   • MEDLINE
   • CrossRef
9. Hendricks HT, IJzerman M, de Kroon JR, in ’t Groen FA, Zilvold G. Functional electrical stimulation by means of the ‘Ness Handmaster Orthosis’ in chronic stroke patients: an exploratory study. Clin Rehabil. 2001;15:217–220
   • View In Article
   • MEDLINE
   • CrossRef
10. Sonde L, Gip C, Fernaeus SE, Nilsson CG, Viitanen M. Stimulation with low frequency (1.7 Hz) transcutaneous electric nerve stimulation (low-tens) increases motor function of the post-stroke paretic arm. Scand J Rehabil Med. 1998;30:95–99
    • View In Article
    • MEDLINE
    • CrossRef
11. Vuagnat H, Chantraine A. Shoulder pain in hemiplegia revisited: contribution of functional electrical stimulation and other therapies. J Rehabil Med. 2003;35:49–54
    • View In Article
    • MEDLINE
    • CrossRef
12. Bremner LA, Sloan KE, Day RE, Scull ER, Ackland T. A clinical exercise system for paraplegics using functional electrical stimulation. Paraplegia. 1992;30:647–655
    • View In Article
    • MEDLINE
    • CrossRef
13. Glaser RM. Functional neuromuscular stimulation (Exercise conditioning of spinal cord injured patients). Int J Sports Med. 1994;15:142–148
    • View In Article
    • MEDLINE
    • CrossRef
14. Janssen TW, Glaser RM, Shuster DB. Clinical efficacy of electrical stimulation exercise training: effects on health, fitness, and function. Top Spinal Cord Inj Rehabil. 1998;3:33–49
    • View In Article
15. Scremin AM, Kurta L, Gentili A, et al. Increasing muscle mass in spinal cord injured persons with a functional electrical stimulation exercise program. Arch Phys Med Rehabil. 1999;80:1531–1536
    • View In Article
    • Abstract
    • Full-Text PDF (1319 KB)
    • CrossRef
16. Scremin OU, Cuevas-Trisan RL, Scremin AM, Brown CV, Mandelkern MA. Functional electrical stimulation effect on skeletal muscle blood flow measured with H2(15)O positron emission tomography. Arch Phys Med Rehabil. 1998;79:641–646
    • View In Article
    • Abstract
    • Full-Text PDF (997 KB)
    • CrossRef
17. Daly JJ, Marsolais EB, Mendell LM, et al. Therapeutic neural effects of electrical stimulation. IEEE Trans Rehabil Eng. 1996;4:218–230
    • View In Article
    • MEDLINE
    • CrossRef
18. Kralj AR, Bajd T. Functional electrical stimulation: standing and walking after spinal cord injury. Boca Raton: CRC Pr; 1989;
    • View In Article
19. Mossberg KA. Reliability of a timed walk test in persons with acquired brain injury. Am J Phys Med Rehabil. 2003;82:385–390
    • View In Article
    • MEDLINE
    • CrossRef
20. Berg K, Wood-Dauphinee S, Williams JI. The Balance Scale: reliability assessment with elderly residents and patients with an acute stroke. Scand J Rehabil Med. 1995;27:27–36
    • View In Article
    • MEDLINE
21. Collen FM, Wade DT, Robb GF, Bradshaw CM. The Rivermead Mobility Index: a further development of the Rivermead Motor Assessment. Int Disabil Stud. 1991;13:50–54
    • View In Article
    • MEDLINE
22. Hsieh CL, Hsueh IP, Mao HF. Validity and responsiveness of the Rivermead mobility index in stroke patients. Scand J Rehabil Med. 2000;32:140–142
    • View In Article
    • MEDLINE
    • CrossRef
23. Deutekom M, Beltman JG, de Ruiter CJ, de Koning JJ, de Haan A. No acute effects of short-term creatine supplementation on muscle properties and sprint performance. Eur J Appl Physiol. 2000;82:223–229
    • View In Article
    • MEDLINE
    • CrossRef
24. Pang MY, Eng JJ, Dawson AS, Gylfadóttir S. The use of aerobic exercise training in improving aerobic capacity in individuals with stroke: a meta-analysis. Clin Rehabil. 2006;20:97–111
    • View In Article
    • MEDLINE
    • CrossRef
25. Swain DP, Franklin BA. Comparison of cardioprotective benefits of vigorous versus moderate intensity aerobic exercise. Am J Cardiol. 2006;97:141–147
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (113 KB)
    • CrossRef
26. Katz-Leurer M, Shochina M, Carmeli E, Friedlander Y. The influence of early aerobic training on the functional capacity in patients with cerebrovascular accident at the subacute stage. Arch Phys Med Rehabil. 2003;84:1609–1614
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (104 KB)
    • CrossRef
27. Wernbom M, Augustsson J, Thomee R. The influence of frequency, intensity, volume and mode of strength training on whole muscle cross-sectional area in humans. Sports Med. 2007;37:225–264
    • View In Article
    • MEDLINE
    • CrossRef
28. Salmons S. Exercise, stimulation and type transformation of skeletal muscle. Int J Sports Med. 1994;15:136–141
    • View In Article
    • MEDLINE
    • CrossRef
29. Newham DJ, Hsiao SF. Knee muscle isometric strength, voluntary activation and antagonist co-contraction in the first six months after stroke. Disabil Rehabil. 2001;23:379–386
    • View In Article
    • MEDLINE
    • CrossRef
30. Gilman S. Time course and outcome of recovery from stroke: relevance to stem cell treatment. Exp Neurol. 2006;199:37–41
    • View In Article
    • MEDLINE
    • CrossRef
31. Leroux A. Exercise training to improve motor performance in chronic stroke: effects of a community-based exercise program. Int J Rehabil Res. 2005;28:17–23
    • View In Article
    • MEDLINE
    • CrossRef
32. Leroux A, Pinet H, Nadeau S. Task-oriented intervention in chronic stroke: changes in clinical and laboratory measures of balance and mobility. Am J Phys Med Rehabil. 2006;85:820–830
    • View In Article
    • MEDLINE
    • CrossRef
33. Marigold DS, Eng JJ, Dawson AS, Inglis JT, Harris JE, Gylfadóttir S. Exercise leads to faster postural reflexes, improved balance and mobility, and fewer falls in older persons with chronic stroke. J Am Geriatr Soc. 2005;53:416–423
    • View In Article
    • MEDLINE
    • CrossRef
34. Mackintosh SF, Hill KD, Dodd KJ, Goldie PA, Culham EG. Balance score and a history of falls in hospital predict recurrent falls in the 6 months following stroke rehabilitation. Arch Phys Med Rehabil. 2006;87:1583–1589
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (169 KB)
    • CrossRef
35. Shumway-Cook A, Baldwin M, Polissar NL, Gruber W. Predicting the probability for falls in community-dwelling older adults. Phys Ther. 1997;77:812–819
    • View In Article
    • MEDLINE

• a Therapeutic Alliances Inc, 333 N Broad St, Fairborn, OH 45324.
• b Oxycon Alpha; Viasys Healthcare Nederland, De Molen 8-10, 3994 DB Houten, The Netherlands.
• c Polar Electro Inc, Professorintie 5, Kempele, FIN-90440, Finland.