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Research Reports |
SCK Lee, PT, is a doctoral candidate in the Interdisciplinary Graduate Program in Biomechanics and Movement Sciences, University of Delaware, Newark, Del
ML Gerdom, is a student in the Master's of Physical Therapy Program, Department of Physical Therapy, University of Delaware
SA Binder-Macleod, PhD, PT, is Chair and Associate Professor, Department of Physical Therapy, University of Delaware, 315 McKinly Lab, Newark, DE 19716 (USA) (sbinder{at}udel.edu). Address all correspondence to Dr Binder-Macleod
Submitted August 3, 1998;
Accepted April 21, 1999
| Abstract |
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Key Words: Catchlike property Fatigue Functional electrical stimulation Human quadriceps femoris muscle Muscle length
| Introduction |
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Recent work suggests that optimal stimulation may consist of a train of pulses containing more than one instantaneous frequency.11 By using catchlike-inducing trains that exploit the catchlike-property of skeletal muscle, higher forces can be elicited than if traditional constant-frequency stimulation trains with comparable frequencies are used.1114 The catchlike property of skeletal muscle is the tension enhancement produced when an initial brief high-frequency burst of pulses (24 pulses) is used at the onset of a subtetanic constant-frequency train to activate the muscle.13,1517 The catchlike property is a fundamental property of muscle that is not due to properties of the motor axon or the neuromuscular junction.13,14,18
In our previous investigations of the human quadriceps femoris muscle, we found that, during isometric contractions with the knee in 90 degrees of flexion, catchlike-inducing trains were highly effective in augmenting forces of fatigued muscle compared with comparable constant-frequency trains.11,12,19 As much as 72% augmentation in peak force and 52% augmentation in force-time integrals (ie, the area of the force curve produced in response to stimulation) with respect to comparable, subtetanic, constant-frequency trains have been observed.12 Additionally, we recently showed that catchlike-inducing trains not only augment force compared with subtetanic, constant-frequency trains but also produce 25% greater force-time integrals than even the best constant-frequency train in fatigued human quadriceps femoris muscle.11 When the muscle is not fatigued, however, catchlike-inducing trains generally produce about the same force as comparable constant-frequency trains, with the only added advantage of producing faster rates of rise of force.11,12
In our previous studies, we activated the human quadriceps femoris muscle at the muscle length that produced near-maximum force, corresponding to a knee joint angle of about 90 degrees. Functional electrical stimulation requires quadriceps femoris muscle activation at or near full knee extension to produce standing and ambulation. The force-frequency characteristics of skeletal muscle are known to be altered in the shortened position.20,21 Higher frequencies of activation are required to produce forces at short muscle lengths than what occurs with optimal muscle lengths (ie, a rightward shift in the force-frequency relationship).20,21 Because of this difference, the purpose of this study was to investigate force production as a function of stimulus frequency using both constant and catchlike-inducing trains prior to and during repetitive activation of the human quadriceps femoris muscle while the knee joint angle was held at 15 degrees of flexion. Relatively simple, doublet-initiated (5-millisecond initial interpulse interval), catchlike-inducing trains were used because they have been shown to be effective in augmenting force from human quadriceps femoris muscle.12 A preliminary report of this work has been presented elsewhere.22
| Method |
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=23.3, SD=3.89). The subjects had no history of lower-extremity orthopedic problems. All subjects signed informed consent forms prior to participation in the study.
Experimental Setup
Subjects were seated at a computer-controlled force dynamometer with their hips flexed to about 75 degrees and the knee positioned in 15 degrees of flexion (Fig. 1). We used a KIN-COM II dynamometer* for 8 subjects and a KIN-COM III dynamometer* for 4 subjects. The dynamometer axis was aligned with the knee joint axis, and the force transducer pad was positioned against the anterior surface of the leg about 3 cm proximal to the lateral malleolus. The right quadriceps femoris muscle was stimulated using a Grass S8800 stimulator
with a SIU8T stimulus isolation unit.
All stimulation pulses were 600 microseconds in duration. Two self-adhesive, 7.6- x 12.7-cm (3- x 5-in) electrodes were used to electrically stimulate the muscle. The anode was placed proximally, over the motor point of the rectus femoris muscle, and the cathode was placed distally, over the motor point of the vastus medialis muscle. The stimulator was driven by a personal computer that controlled all timing parameters of each stimulation protocol. All force data were digitized on-line at a rate of 200 samples per second and stored for subsequent analysis.
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After completing the training protocol, subjects rested a minimum of 5 minutes before we started the experimental protocol, which consisted of a control and a repetitive activation sequence. All stimulation trains contained 6 pulses (5 interpulse intervals). The constant-frequency trains had equal interpulse intervals from 10 milliseconds and increased by 10-millisecond intervals up to 160 milliseconds (total of 16 constant-frequency trains; see Fig. 1B, left panel). Because of the reciprocal relationship between interpulse interval and frequency, these trains had frequencies ranging from 100 to 6.25 pulses per second. The catchlike-inducing trains used to elicit the catchlike response, had one initial, brief interpulse interval equal to 5 milliseconds, followed by a constant-frequency portion containing interpulse intervals comparable to the 16 constant-frequency trains (4 equal interpulse intervals ranging from 10 to 160 milliseconds, for a total of 16 catchlike-inducing trains; see Fig. 1B, right panel).
To set the "stimulus intensity," the output of the stimulator was adjusted until it elicited a force equal to about 20% of the MVIC of the subject's quadriceps femoris muscle when stimulated with a 6-pulse constant-frequency train with 10-millisecond interpulse intervals. The stimulation was then delivered once every 5 seconds until the muscle was potentiated (ie, force did not increase with 3 successive trains). Potentiation required 5 to 10 trains. Stimulation was continued to allow the stimulation intensity to be readjusted to elicit 20% of the MVIC from the potentiated muscle. Stimulation was then stopped, and the intensity was not changed for the remainder of the session. All force measurements were gravity corrected for the weight of the subject's limb in 15 degrees of knee flexion.
Control sequence.
Within 5 seconds of adjustment of the stimulation intensity, the control sequence began. This sequence consisted of the 16 constant-frequency and 16 catchlike-inducing trains first presented in a random order and then repeated in reverse order (total of 64 trains). One train was delivered every 10 seconds to avoid fatiguing the muscle. The same random order was used for each subject.
Repetitive activation sequence.
Ten minutes after completion of the control sequence, the muscle was repotentiated using the same methods outlined earlier and the repetitive activation sequence commenced. Repetitive activation consisted of 192 trains, delivered once per second. The 192 trains were composed of 2 different random sequences of the 16 constant-frequency and 16 catchlike-inducing trains (the first random order was the same as that used in the control protocol). The 2 random sequences formed a block of 64 stimulus trains, which were repeated 3 times to form the 192-train sequence (Fig. 2). The same repetitive activation sequence was used for each subject to allow train-by-train comparisons across subjects.
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Data Analysis
Two-way, within-subjects, factorial analyses of variance (ANOVAs) were performed to test the effects of train type (constant-frequency versus catchlike-inducing trains) and interpulse interval on the force data. Separate ANOVAs were used to test the control and repetitive activation conditions. Furthermore, within each activation condition, peak force and force-time integral data were analyzed separately. If significant effects were observed, Holm's sequentially rejective, Bonferronicorrected, post hoc, 2-tailed paired t tests24 were used to compare the responses of the constant-frequency trains with the responses of catchlike-inducing trains at each interpulse interval. Finally, for both control and repetitive activation data, 2-tailed paired t tests were performed to compare the greatest or "best" constant-frequency train response with the best catchlike-inducing train response (eg, for repetitive activation force-time integral in Fig. 5D, the 60-millisecond interpulse interval constant-frequency train with the 80-millisecond interpulse interval catchlike-inducing train) for each of the 2 force measures (peak force and force-time integral) to determine which stimulus pattern produced the best overall performance. For all group data, means (± standard error) are presented. An observation was significant if P
.05.
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| Results |
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50 milliseconds in the control condition and for all interpulse intervals of
30 milliseconds following repetitive activation (Fig. 5). For both conditions, the augmentation in peak force by catchlike-inducing trains generally increased as interpulse intervals of longer duration were used. The augmentation ranged from about 6% at 50 milliseconds to about 117% at 160 milliseconds in the control condition and from about 4% at 30 milliseconds to about 110% at 160 milliseconds following repetitive activation. The 20-millisecond interpulse interval produced the greatest peak force for both constant-frequency and catchlike-inducing trains both before and after repetitive activation.
Force-time integrals.
For the control condition, catchlike-inducing trains produced greater force-time integrals than the constant-frequency trains produced for all interpulse intervals of
80 milliseconds (Fig. 5). Although the 20-millisecond constant-frequency train produced greater forcetime integrals than its comparable catchlike-inducing train, the difference was small (about 5%). Following repetitive activation, catchlike-inducing trains with interpulse intervals of
70 milliseconds produced greater force-time integrals than their comparable constant-frequency trains produced. For both conditions, the augmentation in forcetime integral by catchlike-inducing trains generally increased as interpulse intervals of longer duration were used. The augmentation ranged from about 18% at 80 milliseconds to about 59% at 160 milliseconds in the control condition and from about 9% at 70 milliseconds to about 49% at 150 milliseconds following repetitive activation. There was no difference in the force-time integrals produced by the best constant-frequency train (60 milliseconds) and the best catchlike-inducing train (60 milliseconds) when the muscle was in the control condition. Following repetitive activation, however, the best catchlike-inducing train (80 milliseconds) produced a 6.2% greater force-time integral than the optimal constant-frequency train (60 milliseconds) produced and a 15.3% greater force-time integral than its comparable constant-frequency train produced.
Additional testing at long and short muscle lengths.
Forcetime integral data from the 4 subjects tested at 15 and 90 degrees of knee flexion (short and long muscle lengths, respectively) with both the present protocol (10160 milliseconds) and the previous protocol (10120 milliseconds) showed that, regardless of protocol, less fatigue occurred at short muscle lengths than at long muscle lengths (Fig. 6). Averaged across interpulse intervals and train types, the present protocol (10160 milliseconds) produced about 11% and 33% declines in force at short and long muscle lengths, respectively. The previous protocol (10120 milliseconds) produced an increase in force of about 9% and a decrease in force of about 46% at short and long muscle lengths, respectively.
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| Discussion |
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We found a small amount of fatigue produced by repetitive activation. In general, constant-frequency and catchlike-inducing train force-time integral responses declined about 2% and peak force responses declined about 12% when averaged across all interpulse intervals. Previous work25,26 has demonstrated less fatigability of human skeletal muscle at shorter lengths, but the profound lack of fatigue we found was somewhat surprising. In a previous study investigating fatigue as a function of muscle length, we observed a 40% decline in peak force at short muscle length (15° of knee flexion) compared with a 53% decline at long muscle length (90° of knee flexion).25 In that study, we used a single 25-millisecond interpulse interval constant-frequency train to activate the muscle repetitively. In another of our previous studies,11 which tested constant-frequency trains with interpulse intervals of 10 to 120 milliseconds and comparable catchlike-inducing trains, a 48% decline in force-time integral and a 47% decline in peak force were observed when the human quadriceps femoris muscle was held at a long length (90° of knee flexion). Because we used multiple frequencies in the present study, including frequencies that produced lower forces than the 120-millisecond interpulse interval train (Fig. 5), the inclusion of these lower frequencies (longer interpulse intervals) may have contributed to the lower amount of fatigue we observed. Our study of the subset of 4 subjects was used to investigate this possibility. We found that, independent of activating sequence, little fatigue was produced when the muscle was held at the shorter length. It appears, therefore, that our findings are consistent with previous findings that less fatigue occurs at shorter muscle lengths than at longer muscle lengths.
The ability to augment force during the control sequence at short muscle lengths may be due to the selective attenuation of force produced at low frequen-cies when muscles are held at short lengths.20,21 This attenuation is consistent with observations that Ca2+ release per pulse27,28 or Ca2+ sensitivity of the myofi-brils2931 is diminished at short muscle lengths compared with long muscle lengths. Duchateau and Hain-aut32 demonstrated that one mechanism by which catchlike-inducing trains augment force is through the increased Ca2+ release from the sarcoplasmic reticulum by the initial high-frequency burst. Thus, greater Ca2+ release by catchlike-inducing trains could partially compensate for the decreased Ca2+ release or sensitivity when the muscle is held at short lengths.
Overall, the augmentations by catchlike-inducing trains following repetitive activation were substantially less than those observed at longer muscle lengths. Optimal catchlike-inducing trains (80-millisecond interpulse intervals) produced approximately 15% greater forcetime integrals than comparable constant-frequency trains and approximately 6% greater force-time integrals than optimal constant-frequency trains (60-millisecond interpulse intervals). In a similar study,11 at longer muscle lengths, optimal catchlike-inducing trains produced approximately 31% greater force-time integrals than comparable constant-frequency trains and approximately 25% greater force-time integrals than optimal constant-frequency trains. The relative lack of augmentation is probably due to the relatively small amount of fatigue produced in the present study. Nonetheless, catchlike-inducing trains appear to be effective in producing force augmentation in muscles at various lengths. Thus, train pattern is a variable that should be considered when attempting to optimize force.
Use of Short-Duration Stimulation Trains
We used short-duration stimulation trains in this study because short bursts of activity typify activation patterns needed to produce functional movements. Hennig and Lømo33 found that motor unit discharge patterns in awake and freely behaving animals typically involved
6 action potentials. Additionally, because functional human movements typically require brief periods of activation of each muscle (eg, walking, eating), we anticipate that electrical stimulators designed to perform FES will require brief trains of activation to mimic natural movements. Lastly, all stimulators used in cardiomyoplasty, a procedure in which a skeletal muscle is wrapped around the heart and stimulated to assist systole, use 6-pulse trains.34
Clinical Implications
We attempted to define the boundary conditions for force augmentation by catchlike-inducing train stimula-tion. The optimal catchlike-inducing train produced more force than any constant-frequency train at short muscle lengths during both control and repetitive activation conditions. Because catchlike-inducing trains produce greater forces during these conditions, they may improve FES applications that require muscle activation at short lengths. Catchlike-inducing trains produce more rapid rates of rise of force than constant-frequency trains.18,35 Therefore, faster FES-induced ambulation speeds, which have been reported to diminish the metabolic demand during FES by improving ambulation efficiency,2 may be attained. Our results are consistent with our previous findings,11 and they show maximal force-time integral production using interpulse interval durations of about 60 to 80 milliseconds (16.712.5 pulses per second). These frequencies are similar to the frequencies observed during physiological activation of motor units during maximal voluntary efforts.36 Stimulation at interpulse interval durations of about 60 to 80 milliseconds produced forces that were subtetanic (ie, force production and relaxation are seen in response to each pulse within the train). The influence that these subtetanic trains may have on the smoothness of the movement produced during FES has yet to be determined.
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| Footnotes |
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This study was approved by the University of Delaware Human Subjects Review Board.
This research was supported, in part, by grants from the Foundation for Physical Therapy Inc, the American Physical Therapy Association, and the University of Delaware Office of Graduate Studies to Mr Lee and the National Institutes of Health (HD41264) to Dr Binder-Macleod.
* Chattecx Corp, 101 Memorial Dr, PO Box 4287, Chattanooga, TN 37405. ![]()
Grass Instruments, Div of Astro-Med Inc, 600 E Greenwich Ave, West Warwick, RI 02893. ![]()
| References |
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