The Effect of Rest Intervals on Knee-Extension Torque Production With Neuromuscular Electrical Stimulation

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1 J Sport Rehabil. 2006, 15, Human Kinetics, Inc. The Effect of Rest Intervals on Knee-Extension Torque Production With Neuromuscular Electrical Stimulation William R. Holcomb, Mack D. Rubley, Michael G. Miller, and Tedd J. Girouard Context: Previous studies using neuromuscular electrical stimulation (NMES) have suggested that 30-second rest intervals are too short for sufficient recovery. Objective: To compare the effect of rest interval on knee-extension torque production. Design: Counterbalanced mixed design to test independent variable, rest interval; ANOVA to analyze dependent variable, percentage decline. Setting: Athletic training research laboratory. Participants: 24 healthy men and women. Intervention: Participants performed knee extension under 2 contraction conditions, maximum voluntary isometric contraction (MVIC) and NMES with either 30- or 120-second rest between repetitions. Main Outcome Measure: Peak torque produced during each repetition of a 5-repetition set. Results: The main effect for rest interval was significant (F 1,23 = 30.30, P =.001), as was the main effect for condition (F 1,23 = 11.18, P =.003). Conclusions: A 120-second rest between repetitions is recommended when using NMES in early rehabilitation because force decline across repetitions with 30-second rest during NMES is greater than with MVIC. Key Words: fatigue, accommodation, strength, therapy, rehabilitation In early rehabilitation, neuromuscular electrical stimulation (NMES) can be used to minimize atrophy and strength loss associated with postsurgical immobilization by stimulating motor nerves and creating involuntary muscle actions. In a recent study investigating both voluntary and involuntary contractions, a large decline in force production was seen with each repetition in a 3-repetition set. 1 The force decline was greater with NMES than with maximum voluntary isometric contractions (MVICs) with a 30-second rest interval, which was the maximum duration provided by the electrical stimulator. Selkowitz 2 started with 50-second rest intervals but noticed a large force decrement and so completed the study with rest intervals of 120 seconds, which resulted in high force outputs across the treatment period. Based on Selkowitz, 2 we believed that 30-second rest intervals might be too short. Consequently, the primary purpose of our study was to compare the effect of rest-interval length on knee-extension torque production. In addition, force production during NMES was compared with that of voluntary contractions. Holcomb, Rubley, and Girouard are with Dept of Kinesiology, University of Nevada Las Vegas, Las Vegas, NV Miller is with the Dept of HPER, Western Michigan University, Kalamazoo, MI

2 Fatigue With NMES 117 Design Methods This study used a counterbalanced mixed design with the independent variables of rest interval (30- or 120-second rest between repetitions) and contraction condition (MVIC and NMES-induced contractions without voluntary effort). The dependent variable was percentage decline of peak torque. Participants reported to an athletic training research laboratory on a single day, where they were informed of the potential risks of the study and signed a consent form. The university s institutional review board approved the study. Subjects Twenty-four healthy participants (11 men and 13 women, age 24.6 ± 4.9 years, height ± 10.5 cm, weight 73.8 ± 17.0 kg) volunteered to participate in this study. Participants were randomly assigned to either the 30-second rest-interval or the 120-second rest-interval group. Interventions Participants performed isometric knee extension under 2 contraction conditions: MVIC and NMES-induced contractions without voluntary effort. Five repetitions were completed under each condition with either 30 seconds or 120 seconds rest between repetitions, depending on group assignment. The longest rest interval on the stimulator was 30 seconds, so the leads were disconnected to allow for the 120- second rest interval. An OrthoDx (Rehabilicare, New Brighton, Minn), which is a portable electrical stimulator, was used to deliver electrical stimulation. The unit can be powered by batteries or through an AC adaptor. To ensure a consistent power source the AC adaptor was used for this study. The stimulation specifications are provided in Table 1. Table 1 Electrical-Stimulation Specifications Parameter Current type Intensity Pulse rate OrthoDx symmetrical biphasic maximum comfortable 33 pulses/s Pulse width 600 µs Ramp On time 2 s 10 s

118 Holcomb et al The right anterior thigh of each participant was shaved and the skin cleaned with isopropyl-alcohol wipes. Two electrodes were used to deliver the current. A 4-6.

3 118 Holcomb et al The right anterior thigh of each participant was shaved and the skin cleaned with isopropyl-alcohol wipes. Two electrodes were used to deliver the current. A in electrode was centered on the anterior thigh midway between the anterosuperior iliac spine and the superior pole of the patella over the motor point for the rectus femoris, and a 4-2-in electrode was placed diagonally over the motor point of the vastus medialis oblique (Figure 1). 3-6 A maximum comfortable NMES intensity was used. To find this intensity, the voltage was gradually increased until the participant reported a sensation. The intensity was increased further until a muscle response was noted, and further still until the subject reported a maximum comfortable intensity. This process was repeated 3 times to ensure that a maximum comfortable intensity was identified. This process was repeated for each of the 2 NMES conditions but was not altered between individual repetitions. A standard warm-up that included elliptical cycling, quadriceps stretching, and isometric actions (5 at 50%, 3 at 75%, and 1 MVIC) was performed before testing. Participants were positioned on a Kin-Com dynamometer (Chattanooga Group, Inc, Hixon, Tenn) with hip-flexion angle of 80 and knee-flexion angle of 70. The axis of rotation of the dynamometer was aligned to the anatomical axis of the right knee. To ensure reliable measurements, the dynamometer was calibrated, all stabilization straps were used to prevent unwanted movement, participants hands were required to remain free, and no visual feedback was provided during testing (Figure 2). Figure 1 Electrode placement for the electrical stimulation.

4 Fatigue With NMES 119 Figure 2 Participant positioned on the Kin-Com with knee in 70 flexion. Outcome Measures Peak torque was recorded by the dynamometer while isometric muscle actions were performed under each condition for 10 seconds. For condition 1, participants were asked to extend the knee against the fixed lever arm of the dynamometer with maximum force. For condition 2, participants were asked to relax and allow the knee to passively extend against the fixed lever arm without voluntary effort. Statistical Analyses Peak torque produced during each repetition for each condition was recorded for analysis. The difference in peak torque from first to final repetition was determined. This value was divided by peak torque from the first repetition to provide the percentage decline across the 5-repetition set. 7 Percentage-decline data normalized for body weight were analyzed with a 2 (rest interval) 2 (contraction condition) mixed-model ANOVA, with repeated measures on the second factor. Results The main effect for rest interval was significant (F 1,23 = 30.30, P =.001), indicating a greater percentage decline with 30 seconds rest than with 120 seconds rest. The

120 Holcomb et al main effect for contraction condition was also significant (F 1,23 = 11.18, P =.003), indicating a greater percentage decline with NMES than with MVIC.

5 120 Holcomb et al main effect for contraction condition was also significant (F 1,23 = 11.18, P =.003), indicating a greater percentage decline with NMES than with MVIC. The percentage decline across 5 repetitions with 30 seconds rest was 29.6% with NMES and 11.1% with MVIC. The percentage decline with 120 seconds rest was 8.2% with NMES and 2.8% with MVIC (Figure 3). The Rest Interval Condition interaction was not significant (F 1,23 = 3.31, P =.08), indicating that the change in rest interval did not affect the 2 conditions differently (Figure 4). Figure 3 Percentage decline for the 2 contraction conditions with both 30 and 120 seconds rest. MVIC indicates maximum voluntary isometric contraction, and NMES, neuromuscular electrical stimulation. *Indicates a greater decline in force with 30 seconds rest (F 1,23 = 30.30, P =.001). #Indicates a greater decline in force with NMES (F 1,23 = 11.18, P =.003). Figure 4 Torque production for the 2 contraction conditions with both 30 and 120 seconds rest across 5 repetitions. MVIC indicates maximum voluntary isometric contraction, and NMES, neuromuscular electrical stimulation.

6 Fatigue With NMES 121 Comments The results of our study showed a significantly greater decline in force with 30 seconds rest than with 120 seconds rest. The percentage decline across 5 repetitions using NMES with 30-second rest intervals was 29.6% and only 8.2% with 120- second rest intervals. This was consistent with findings in the literature. Selkowitz 2 reported a large force decline across repetitions when 50-second rest intervals were used in pilot work, so 120-second rest intervals were used for the actual study. The author cited that this time is required for total phosphagen replacement during ATP resynthesis. No direct comparison of the 2 rest intervals was made, but the author reported average contraction intensities of 65% of the pretraining MVIC when 120- second rest intervals were used. 8 Our study was based on similar findings where a notable force decline was seen with 30-second rest intervals. 1 Our study did make a direct comparison between 30-second and 120-second rest intervals, however, and we found significantly less force decline when 120-second rest intervals were used. Packman-Braun 9 directly assessed the effect of recovery (OFF) time on force decline while using the wrist flexors. Duty cycles of 1:5, 1:3, and 1:1 were found to progressively cause more force decline. Cox et al 10 reported similar results with the knee extensors. In their study, rest intervals of 35 seconds resulted in significantly greater force decline than did rest intervals of 50 and 65 seconds. Because longer rest intervals resulted in decreased force decline, it appears that fatigue is a contributing factor to the decline in force when NMES is used. The results of our study revealed a significantly greater decline in force with NMES than with MVIC. The percentage decline across 5 repetitions with 30- second rest intervals was 29.6% with NMES and only 11.1% with MVIC. With 120-second rest intervals the force decline was 8.2% with NMES and only 2.8% with MVIC. We found no study in the literature that compared NMES with MVIC across repetitions; however, the literature does help explain why the decline in force is more pronounced with NMES. The magnitude of force production with MVIC is greater than with NMES. In our study the average force with NMES during the first repetition was 48% of the MVIC. It would make sense that the greater force of the MVIC would be more taxing and thus result in greater fatigue than the contraction of lesser force with NMES. This was clearly not the case. Another consideration is the selective recruitment of fibers that differs with these 2 types of contractions. Larger nerve fibers have a low resistance to electrical current, so they are recruited first with NMES. These nerves innervate type II muscle fibers, which are less resistant to fatigue With voluntary contractions the recruitment order is reversed. The more fatigue-resistant type I muscle fibers are recruited first, and if greater force is required, the recruitment of type II muscle fibers will follow. 14,15 Stimulation of these large-diameter and rapidly fatiguing motor units has been cited, in part, as the explanation for the more rapid rate of fatigue. 16 Another contributing factor to the force decline unique to NMES is accommodation to the current intensity. With repeated stimulation, motor nerves begin to accommodate and a greater intensity is required to excite an equal number of fibers. 17 If the intensity is not periodically increased, the force production will decrease. Because accommodation is not a factor with voluntary contractions, this might account for much of the difference in the decline with NMES versus MVIC.

7 122 Holcomb et al No study was found that directly linked accommodation to a decrease in force, but Snyder-Mackler et al 18 increased intensity from contraction to contraction in an effort to prevent a decline in force. The periodic increase in intensity was possible because of increased tolerance resulting from accommodation. There is a practical concern with force decline because there is a direct correlation between contraction intensity during training with NMES and the resulting strength gains. 2 Training with NMES should begin with forceful contractions, and techniques should be used to prevent a decline in force. This high force must be maintained throughout the treatment period. Preventing a decline in force during training sessions is important because a minimum force production ranging from 33% to 60% of MVIC is reported as a requirement for a positive training effect It has been noted that preventing a decline in force is more significant when using NMES than when using MVIC because the force decline is greater. 1, 2 Binder- Macleod and Snyder-Mackler 23 cited 3 primary factors that affect fatigue with NMES: stimulation intensity, frequency, and the length of rest between stimulation trains. Decreasing stimulation intensity and frequency might be counterintuitive, however. To achieve an initial forceful contraction it is necessary to use a maximum intensity. Therefore, any reduction in intensity to prevent a decline in force adversely affects the initial contraction force. Binder-Macleod and Barker 24 demonstrated that greater frequency results in greater force decline. As with intensity, frequency has an effect on the initial contraction force. For a maximal contraction force it is necessary to use a frequency called the critical fusion frequency that produces tetanic contractions. It would consequently be counterproductive to decrease frequency below the critical fusion frequency in an effort to decrease force decline. Therefore, our study investigated the effect of rest interval. Based on the results of our study we think clinicians should employ 2 techniques to decrease the decline in force. Because 120-second rest intervals resulted in less force decline than 30-second rest intervals, the longer rest interval is recommended when using NMES. Second, because accommodation to current intensity likely contributes to the decline in force, the intensity should be increased periodically to ensure forceful contractions throughout the treatment duration. 18 Two other recommendations, unrelated to these data, were found in the literature that might also help increase force production. One is to use variable-frequency trains where the interpulse intervals are not kept constant. 24 Variable-frequency trains begin with pulses with short interpulse intervals, which provide a high-frequency component followed by a longer interpulse interval, which provides a low-frequency component. This takes advantage of the catchlike property of muscles, wherein there is an increased force production when a high-frequency burst is delivered at the onset of a variable-frequency train. 24 This technique has been shown effective in decreasing the fatigue-induced force decline experienced with electrical stimulation of human muscle Another recommendation is to use multiple channels during the stimulation of a single muscle group. With this technique an alternating or reciprocal mode is used so that 1 channel is firing while the other is inactive. This would mimic normal asynchronous firing while allowing additional time for fibers under the inactive channel to recover. 27 We have made the argument that the greater force decline found with NMES when compared with MVIC suggests that the force decline with NMES results from a combination of fatigue and an accommodation to current intensity because

8 Fatigue With NMES 123 MVIC is only affected by fatigue. One limitation of the study is that the relative contribution of these 2 factors to the overall decline in force cannot be quantified, because these factors cannot be isolated. Another limitation is that a learning effect might have occurred with the MVIC across the 5 repetitions. If subjects improved because of learning, the force decline as a result of fatigue would have been underestimated. Subjects were asked to perform 5 repetitions at roughly 50% intensity, 3 at 75% intensity, and 1 MVIC as a part of the warm-up. It is our belief that this accounted for much of the learning effect that might occur with untrained subjects producing MVICs. Conclusion The force decline with 30-second rest intervals between sets was significantly greater than with 120-second rest intervals whether subjects were performing MVIC or NMES with maximum comfortable intensities. This force decline was significantly greater when using NMES than when performing MVICs, and the difference is likely a result of a combination of greater fatigue and accommodation to the electrical current intensity. Therefore, when using NMES with isometric muscle actions in early rehabilitation, efforts should be made to prevent force decline across repetitions. Because longer rest intervals resulted in less fatigue, longer rest intervals should be used, and to lessen accommodation, periodic increases in intensity are recommended. Further research should examine rest intervals greater than 30 seconds but less than 120 seconds to help guide clinicians in selecting the ideal rest interval to facilitate both forceful contractions and a time-efficient treatment. References 1. Holcomb WR, Rubley MD, Girouard TJ. Effect of the simultaneous application of NMES and HVPC on knee extension torque [abstract]. J Athl Train. 2004;39(suppl): S Selkowitz DM. Improvement in isometric strength of the quadriceps femoris muscle after training with electrical stimulation. Phys Ther. 1985;65(2): Wolf S, Gideon A, Saar D, Penny A, Railey P. The effect of muscle stimulation during resistive training on performance parameters. J Sports Med. 1986;14: McLoda T, Carmack J. Optimal burst duration during a facilitated quadriceps femoris contraction. J Athl Train. 2000;35(2): Caggiano E, Emrey T, Shirley S, Craik RL. Effects of electrical stimulation or voluntary contraction for strengthening the quadriceps femoris muscles in an aged male population. J Orthop Sports Phys Ther. 1994;20(1): Binder-Macleod SA, Lee SC, Russ DW, Kucharski LJ. Effects of activation pattern on human skeletal muscle fatigue. Muscle Nerve. 1998;21(9): Matsunaga T, Shimada Y, Sato K. Muscle fatigue from intermittent stimulation with low and high frequency electrical pulses. Arch Phys Med Rehabil. 1999;80(1): Holcomb W, Golestani S, Hill S. A comparison of knee-extension torque production with biphasic versus Russian current. J Sport Rehabil. 2000;9: Packman-Braun R. Relationship between functional electrical stimulation duty cycle and fatigue in wrist extensor muscles of patients with hemiparesis. Phys Ther. 1988;68(1):51-56.

9 124 Holcomb et al 10. Cox AM, Mendryk SW, Kramer JF, Hunka SM. Effect of electrode placement and rest interval between contractions on isometric knee extension torques induced by electrical stimulation at 100 Hz. Physiother Can. 1986;38: Delitto A, Snyder-Mackler L. Two theories of muscle strength augmentation using percutaneous electrical stimulation. Phys Ther. 1990;70(3): Hamada T, Kimura T, Moritani T. Selective fatigue of fast motor units after electrically elicited muscle contractions. J Electromyogr Kinesiol. 2004;14(5): Sinacore DR, Delitto A, King DS, Rose SJ. Type II fiber activation with electrical stimulation: a preliminary report. Phys Ther. 1990;70(7): Trimble MH, Enoka RM. Mechanisms underlying the training effects associated with neuromuscular electrical stimulation. Phys Ther. 1991;71(4): , discussion Molina RM, Galan AT, Garcia MS. Spectral electromyographic changes during a muscular strengthening training based on electrical stimulation. Electromyogr Clin Neurophysiol. 1997;37: Binder-Macleod SA, Halden EE, Jungles KA. Effects of stimulation intensity on the physiological responses of human motor units. Med Sci Sports Exerc. 1995;27(4): Nelson RM, Currier DP. Clinical Electrotherapy. Norwalk, Conn: Appleton & Lange; Snyder-Mackler L, Ladin Z, Schepsis AA, Young JC. Electrical stimulation of the thigh muscles after reconstruction of the anterior cruciate ligament. effects of electrically elicited contraction of the quadriceps femoris and hamstring muscles on gait and on strength of the thigh muscles. J Bone Joint Surg Am. 1991;73(7): Currier DP, Mann R. Muscular strength development by electrical stimulation in healthy individuals. Phys Ther. 1983;63(6): McDonagh MJ, Davies CT. Adaptive response of mammalian skeletal muscle to exercise with high loads. Eur J Appl Physiol Occup Physiol. 1984;52(2): Miller C, Thepaut-Mathieu C. Strength training by electrostimulation conditions for efficacy. Int J Sports Med. 1993;14(1): Soo CL, Currier DP, Threlkeld AJ. Augmenting voluntary torque of healthy muscle by optimization of electrical stimulation. Phys Ther. 1988;68(3): Binder-Macleod SA, Snyder-Mackler L. Muscle fatigue: clinical implications for fatigue assessment and neuromuscular electrical stimulation. Phys Ther. 1993;73(12): Binder-Macleod SA, Barker CB III. Use of a catchlike property of human skeletal muscle to reduce fatigue. Muscle Nerve. 1991;14(9): Binder-Macleod SA, Lee SC, Baadte SA. Reduction of the fatigue-induced force decline in human skeletal muscle by optimized stimulation trains. Arch Phys Med Rehabil. 1997;78(10): Slade JM, Bickel CS, Warren GL, Dudley GA. Variable frequency trains enhance torque independent of stimulation amplitude. Acta Physiol Scand. 2003;177(1): Pournezam M, Andrews BJ, Baxendale RH, Phillips GF, Paul JP. Reduction of muscle fatigue in man by cyclical stimulation. J Biomed Eng. 1988;10(2):

EFFECT OF TRAINING WITH NEUROMUSCULAR ELECTRICAL STIMULATION ON ELBOW FLEXION

Journal of Sports Science and Medicine (2006) 5, 276-281 http://www.jssm.org Research article EFFECT OF TRAINING WITH NEUROMUSCULAR ELECTRICAL STIMULATION ON ELBOW FLEXION STRENGTH William R. Holcomb University