EFFECTS OF ELECTRICAL STIMULATION PATTERN ON QUADRICEPS FORCE PRODUCTION AND FATIGUE GAELLE DELEY, PhD,1 DAVY LAROCHE, PhD,2 and NICOLAS BABAULT, PhD1 1 INSERM - U1093, Cognition, Action, et Plasticit e Sensorimotrice, Universit e de Bourgogne, Dijon, Bourgogne, France 2 CIC-P INSERM 803, Plateforme d’investigation technologique, CHU de Dijon, Dijon, Bourgogne, France Received 11 November 2013; Revised 5 February 2014; Accepted 10 February 2014 ABSTRACT: Introduction: Mixed stimulation programs (MIX) that switch from constant frequency trains (CFT) to variable frequency trains have been proposed to offset the rapid fatigue induced by CFT during electrical stimulation. However, this has never been confirmed with long stimulation patterns, such as those used to evoke functional contractions. The purpose of this study was to test the hypothesis that MIX programs were less fatiguing than CFTs in strength training-like conditions (6-s contractions, 30-min). Methods: Thirteen healthy subjects underwent 2 sessions corresponding to MIX and CFT programs. Measurements included maximal voluntary isometric torque and torque evoked by each contraction. Results: There were greater decreases of voluntary and evoked torque (P < 0.05) after CFT than MIX, and mean torque was 13 6 1% higher during the MIX session (P < 0.05). Conclusions: These findings confirm that combining train types might be a useful strategy to offset rapid fatigue during electrical stimulation sessions with long-duration contractions. Muscle Nerve 49:760–763, 2014
Functional electrical stimulation (FES) can be used to activate intramuscular nerve branches to produce functionally useful movements such as leg flexion/extension, standing, walking, cycling, and even rowing.1–4 It has often been used to facilitate exercise in individuals with spinal cord injury (SCI). However, rapid fatigue associated with electrical stimulation is an important issue for FES programs, which prevents them from gaining widespread clinical popularity despite their numerous beneficial effects.5 The ideal stimulation pattern for muscle activation with FES would be one that produces sufficiently high forces while minimizing fatigue. FES traditionally consists of constant-frequency trains (CFT), brief high frequency pulses of stimulation separated by regular interpulse intervals that produce a rapid rate of muscle tension but also rapid fatigue.6 It has been suggested that variablefrequency trains (VFT) may augment force compared with the CFT pattern.7 The VFT pattern begins with 2 or 3 high-frequency pulses followed Abbreviations: CFT, constant-frequency trains; FES, functional electrical stimulation; MIX, combination of constant-frequency trains and variablefrequency trains; MVC, maximal voluntary contraction; SCI, spinal cord injury; SD, standard deviation; VFT, variable-frequency trains Key words: constant frequency trains; fatigue; functional contractions; functional electrical stimulation; variable frequency trains des Sciences du Sport, Correspondence to: G. Deley, Faculte de Bourgogne, BP 27877, 21078 Dijon Cedex, France; Universite e-mail: [email protected] C 2014 Wiley Periodicals, Inc. V
Published online 12 February 2014 in Wiley Online Library (wileyonlinelibrary. com). DOI 10.1002/mus.24210
760
Stimulation Pattern and Fatigue
by regularly spaced pulses with longer interpulse intervals. This pattern is based on the “catchlike phenomenon”; tension is enhanced by the brief tetanic burst added to the beginning of a subtetanic, less-fatiguing train of pulses.8 In addition, the VFT pattern has been demonstrated to be better than the CFT pattern at generating force in fatigued muscles.9 Data also suggest that using VFTs exclusively might be highly fatiguing9 and that switching stimulation patterns from CFTs to VFTs may offset the rapid development of fatigue.10 However, these data were derived from short (167-ms) stimulation trains, whereas functional contractions require longer stimulation patterns, usually ranging from 2 to 6 s.4,11,12 If FES is to be used to facilitate exercise in people with SCI, it is important to find a stimulation pattern that would minimize fatigue to allow exercise at high intensities and for long durations. The aim of this preliminary study, conducted in able-bodied subjects, was to compare force and fatigue development in response to 2 stimulation patterns (CFT and CFT combined with VFT) and to evaluate if one is more fatigue-resistant for FES exercise. It was hypothesized that switching from the CFT pattern to the VFT pattern would overcome fatigue. MATERIALS AND METHODS
Thirteen healthy subjects who were accustomed to electrical stimulation (12 men, 1 woman, 4.1 6 2.4 h of physical activity per week, age 28.5 6 7.2 years, height 178.1 6 5.6 cm, body mass 75.0 6 7.6 kg, body mass index 23.4 6 2.2, body fat 11.4 6 4.1%) participated in the study. Subjects were instructed to refrain from training 48 hours before testing. The study was conducted according to the declaration of Helsinki, and approval for the project was obtained from the local Institutional Review Board. Each participant read and signed a written informed consent document outlining the procedures of the experiment.
Subjects.
Experimental Protocol. After an habituation session, each subject underwent 2 30-min testing sessions separated by at least 72 h. During each testing session, isometric muscle force was measured under different electrical stimulation train types. The CFT pattern corresponded to 6 s of MUSCLE & NERVE
May 2014
contraction at 40 HZ with a pulse width of 450 ls; the VFT pattern was an 80-HZ doublet followed by 6 s at 20 HZ with a pulse width of 450 ls. For all sessions, the stimulation program was applied to the right quadriceps muscle. Subjects were placed on an isokinetic dynamometer (Biodex corporation, Shirley, New York) with Velcro straps across the thorax for stability. The leg was fixed to the dynamometer lever-arm, and the axis of rotation of the dynamometer was aligned with the lateral femoral condyle. Stimulation programs were applied at an angle of 90 (0 corresponding to full extension). Stimulation was achieved with a Compex 2 unit (Compex, Medicompex SA, Ecublens, Switzerland) attached to 2 10 3 5 cm self-adhesive electrodes. Electrodes were placed over the muscle belly of the rectus femoris and the vastus medialis muscles. Following set-up, subjects performed 10 to 15 progressive repetitions of isometric contractions followed by 5 to 10 concentric leg extensions at 30 .s21 to warm up. Maximal isometric force was then determined by means of 2 5-s maximal voluntary contractions separated by 2 min (PRE MVC). Then, stimulation intensity was determined for the 2 programs to evoke 35% of each subject’s MVC; 6-s trains were applied every 6 s, and intensity was increased progressively by 10 mA until the evoked torque reached the target value (8–12 trains). Stimulation intensity determinations always started with the CFT pattern followed by VFT after 5 min of passive recovery. There were at least 10 min of rest after intensity determination before the 30-min program. At the end of the 30-min programs, subjects were asked to perform a maximal isometric voluntary contraction (POST MVC). On average, stimulation intensities were 86 6 13 mA during the CFT pattern and 100 6 17 mA during the VFT pattern. Data Analysis. The entire torque record for each session was digitized online at a 2 kHZ sampling frequency (Biopac sytems, Inc., Goleta, CA, USA). Fatigue was quantified using PRE and POST MVC and also by averaging the mean torque of the first and last 5 evoked contractions. The mean torque produced during the entire sessions was also calculated and termed “mean torque.” Lastly, custom written software (Matlab, MathWorks, Natick, Massachusetts) was used to determine the torque at the end of the 10 min of CFT during the MIX session and the time necessary to reach this torque while using VFT.
Data are expressed as mean 6 SD. A two-way analysis of variance with repeated-measures (program 3 time) was used. Program refers to MIX versus CFT, and Time to PRE vs POST. When the P-value from analysis of variance was significant, a post hoc Newman-Keuls test was used. A
Statistics.
Stimulation Pattern and Fatigue
FIGURE 1. (A) Maximal isometric torque before (black symbols) and immediately after (white symbols) the constant-frequency trains program (CFT) and the mixed program (MIX). (B) Average torque evoked during the first 5 (black symbols) and last 5 contractions (white symbols) of each program. Values are shown for each subject and are expressed as mean 6 SD. *statistical difference between PRE and POST values, §statistical difference between decreases obtained with CFT and MIX programs (P < 0.05).
paired t-test was used to compare the mean torque obtained with the 2 programs. Effect sizes (g2) were also determined, with values of 0.2, 0.5, and above 0.8 considered to represent small, medium, and large differences, respectively.13 Statistical significance was accepted when P < 0.05. RESULTS
Figure 1 shows that both stimulation programs induced significant fatigue (P < 0.05) as indicated by MVC decreases [from 278.0 6 61.0 N.m to 186.2 6 50.4 N.m (g2 5 1.64, large difference) and from 284.8 6 50.2 N.m to 217.1648.3 N.m (g2 5 1.37, large difference) for CFT and MIX, respectively]. Torque also decreased between the first and last 5 evoked contractions of the program (from 37.1 6 3.2 to 10.2 6 2.1 % of Pre MVC and from 35.2 6 1.6 to 12.4 6 2.4 % of Pre MVC for MUSCLE & NERVE
May 2014
761
CFT and MIX, respectively). These decreases were significantly greater after CFT than MIX (P < 0.05, large differences with g2 5 0.95 and g2 5 1.11 for MVC and evoked contractions, respectively). The MIX program allowed greater torque to be maintained for a longer time. On average, with MIX, the torque value recorded at the end of the first 10 min (CFT) was only reached after 400 6 250 s of the VFT program. This allowed greater mean torque over the whole MIX session as compared with the CFTs session (26.264.4 vs. 29.564.5 N.m, 113%, P < 0.05, g2 5 0.74, medium differences). DISCUSSION. We found that, in able-bodied subjects, a training session composed of CFTs followed by VFTs induced less fatigue and a greater mean torque than CFTs alone. These results are in accordance with several studies from the literature which reported that a series of CFTs followed by a series of VFTs reached a targeted isometric peak force more times than either CFT or VFT patterns alone.10,14 However, our results are original, given the noticeable differences between the commonly tested protocols and ours. Indeed, in previous studies, trains were 167-ms long, separated by 667 ms of recovery, whereas we chose to use stimulation characteristics close to those usually used during FES-strengthening protocols applied during an entire training session (30 min).4 Although not totally understood, several mechanisms may explain both the higher force production and better force maintenance with the MIX pattern compared with CFT. One of the proposed mechanisms focuses on the stretch of the series elastic elements. It has been suggested that a major effect of catch-like stimulations was to deliver the second pulse when the series elastic elements have been stretched by the contractile response to the first pulse.15,16 The second pulse following closely thereafter will then elicit a force response substantially greater than that of the sum of 2 twitches elicited separately.17 This “mechanical origin” could also explain the lower fatigue observed with the VFT pattern as compared with CFT. However, Ratkevicius and Quistorff18 did not find any difference in the ATP cost of the 2 protocols and concluded that the positive effects of the VFT pattern might be mediated by other mechanisms, such as potentiated Ca21 effects. Increased Ca21 release from the sarcoplasmic reticulum as a result of the initial high-frequency burst has frequently been proposed as a potential mechanism to explain force augmentation with VFTs.19 Moreover, it has been demonstrated that VFTs were particularly effective to augment force 762
Stimulation Pattern and Fatigue
production in fatigued muscles.18,20 It has been suggested that the Ca21 released in response to the initial high-frequency burst overcomes impairments of excitation-contraction coupling that result from reduced Ca21 release from the sarcoplasmic reticulum with fatigue. Ratkevicius and Quistorff,18 therefore, concluded that the major advantage of the VFT pattern is associated with the ability to produce more force in muscles affected by impairments of Ca21 release with fatigue. Lastly, another hypothesis is the motor unit recruitment in relation to stimulation frequencies. It is well known that electrical stimulation imposes continuous contractile activity to the same population of superficial muscle fibers despite neuromuscular transmission propagation failure,21 resulting in great decreases in force production. Changing the stimulation characteristics (frequency, intensity) is therefore the only way to depolarize new fibers. Moreover, it has been shown that lower stimulation frequencies led to less fatigue development.22 On these bases, one can suggest that, whereas CFTs recruit the same pool of motor units during the entire session, VFTs might involve a larger pool, therefore delaying the appearance of fatigue. This is even truer when switching from the CFT to the VFT pattern within the session. Indeed, although VFTs augment force production compared with CFTs, this pattern has been shown to induce an increase in fatigue when used during an entire session.9 In unpublished data from our laboratory we found that, although lower than with CFT, 30 min of the VFT pattern (6 s ON and 6 s OFF) resulted in greater reductions in MVC (227%) and evoked force (270%) than the MIX pattern. This might be explained partly by the higher intensities needed to evoke the required torque with VFTs. In conclusion, this study confirms previous results which suggest that a stimulation program combining CFT and VFT allows greater work and lower fatigue as compared with the CFT pattern only, likely as a result of differences in calcium processes and/or in fiber recruitment. Although they need to be confirmed by further investigation with additional measurements, these results are of particular interest for training and rehabilitation. Indeed, it can be hypothesized that repeated application (several times a week) of the MIX program would induce greater gains than those obtained with the CFT pattern strengthening protocols. Moreover, it would be interesting to adapt the protocol for an application during FES-cycling/ rowing. REFERENCES 1. Rattay F, Resatz S, Lutter P, Minassian K, Jilge B, Dimitrijevic MR. Mechanisms of electrical stimulation with neural prostheses. Neuromodulation 2003;6:42–56.
MUSCLE & NERVE
May 2014
2. Belanger M, Stein RB, Wheeler GD, Gordon T, Leduc B. Electrical stimulation: can it increase muscle strength and reverse osteopenia in spinal cord injured individuals? Arch Phys Med Rehabil 2000;81: 1090–1098. 3. Wheeler GD, Andrews B, Lederer R, Davoodi R, Natho K, Weiss C, et al. Functional electric stimulation-assisted rowing: increasing cardiovascular fitness through functional electric stimulation rowing training in persons with spinal cord injury. Arch Phys Med Rehabil 2002;83:1093–1099. 4. Taylor JA, Picard G, Widrick JJ. Aerobic capacity with hybrid FES rowing in spinal cord injury: comparison with arms-only exercise and preliminary findings with regular training. PM R. 2011;3:817–824. 5. Isakov E, Mizrahi J, Najenson J. Biomechanical and physiological evaluation of FES-activated paraplegic patients. J Rehabil Res Dev 1986;23:9–19. 6. Binder-Macleod SA, Barker CB III. Use of a catchlike property of human skeletal muscle to reduce fatigue. Muscle Nerve 1991;14:850– 857. 7. Binder-Macleod SA, Scott WB. Comparison of fatigue produced by various electrical stimulation trains. Acta Physiol Scand 2001;172: 195–203. 8. Burke RE, Rudomin P, Zajac FE. Catch property in single mammalian motor units. Science 1970;168:122–124. 9. Binder-Macleod SA, Lee SCK, Russ DW, Kucharski LJ. Effects of activation pattern on human skeletal muscle fatigue. Muscle Nerve 1998;21:1145–1152. 10. Scott WB, Binder-Macleod SA. Changing stimulation patterns improves performance during electrically elicited contractions. Muscle Nerve 2003;28:174–180. 11. Crameri RM, Weston AR, Rutkowski S, Middleton JW, Davis GM, Sutton JR. Effects of electrical stimulation leg training during the acute phase of spinal cord injury: a pilot study. Eur J Appl Physiol 2000; 83:409–415.
Stimulation Pattern and Fatigue
12. Sabatier MJ, Stoner L, Mahoney ET, Black C, Elder C, Dudley GA, et al. Electrically stimulated resistance training in SCI individuals increases muscle fatigue resistance but not femoral artery size or blood flow. Spinal Cord 2006;44:227–233. 13. Cohen J. Statistical power analysis for the behavioral sciences, 2nd ed. Hillsdale, NJ: Lawrence Erlbaum Associates; 1988. 14. Scott WB, Lee SC, Johnston TE, Binder-Macleod SA. Switching stimulation patterns improves performance of paralyzed human quadriceps muscle. Muscle Nerve 2005;31:581–588. 15. Parmiggiani F, Stein RB. Nonlinear summation of contractions in cat muscles. II. Later facilitation and stiffness changes. J Gen Physiol 1981;78:295–311. 16. Bigland-Ritchie B, Zijdewind I, Thomas CK. Muscle fatigue induced by stimulation with and without doublets. Muscle Nerve 2000;23: 1348–1355. 17. Binder-Macleod SA, Lee SC. Catchlike property of human muscle during isovelocity movements. J Appl Physiol 1996;80:2051–2059. 18. Ratkevicius A, Quistorff B. Metabolic costs of force generation for constant-frequency and catchlike-inducing electrical stimulation in human tibialis anterior muscle. Muscle Nerve 2001;25:419–426. 19. Abbate F, Bruton JD, De Haan A, Westerblad H. Prolonged force increase following a high-frequency burst is not due to a sustained elevation of [Ca21]i. Am J Physiol Cell Physiol 2002;283:C42– C47. 20. Duchateau J, Hainaut K. Nonlinear summation of contractions in striated muscle. II. Potentiation of intracellular Ca21 movements in single barnacle muscle fibers. J Muscle Res Cell Motil 1986;7:18–24. 21. Zory R, Boeerio D, Jubeau M, Maffiuletti NA. Central and peripheral fatigue of the knee extensor muscles induced by electromyostimulation. Int J Sports Med 2005;26:847–853. 22. Binder-Macleod SA, Snyder-Mackler L. Muscle fatigue: clinical implications for fatigue assessment and Neuromuscular Electrical Stimulation. Phys Ther 1993;73:902–910.
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Functional electrical stimulation (FES) can be used to activate intramuscular nerve branches to produce functionally useful movements such as leg flexion/extension, standing, walking, cycling, and even rowing.1–4 It has often been used to facilitate exercise in individuals with spinal cord injury (SCI). However, rapid fatigue associated with electrical stimulation is an important issue for FES programs, which prevents them from gaining widespread clinical popularity despite their numerous beneficial effects.5 The ideal stimulation pattern for muscle activation with FES would be one that produces sufficiently high forces while minimizing fatigue. FES traditionally consists of constant-frequency trains (CFT), brief high frequency pulses of stimulation separated by regular interpulse intervals that produce a rapid rate of muscle tension but also rapid fatigue.6 It has been suggested that variablefrequency trains (VFT) may augment force compared with the CFT pattern.7 The VFT pattern begins with 2 or 3 high-frequency pulses followed Abbreviations: CFT, constant-frequency trains; FES, functional electrical stimulation; MIX, combination of constant-frequency trains and variablefrequency trains; MVC, maximal voluntary contraction; SCI, spinal cord injury; SD, standard deviation; VFT, variable-frequency trains Key words: constant frequency trains; fatigue; functional contractions; functional electrical stimulation; variable frequency trains des Sciences du Sport, Correspondence to: G. Deley, Faculte de Bourgogne, BP 27877, 21078 Dijon Cedex, France; Universite e-mail: [email protected] C 2014 Wiley Periodicals, Inc. V
Published online 12 February 2014 in Wiley Online Library (wileyonlinelibrary. com). DOI 10.1002/mus.24210
760
Stimulation Pattern and Fatigue
by regularly spaced pulses with longer interpulse intervals. This pattern is based on the “catchlike phenomenon”; tension is enhanced by the brief tetanic burst added to the beginning of a subtetanic, less-fatiguing train of pulses.8 In addition, the VFT pattern has been demonstrated to be better than the CFT pattern at generating force in fatigued muscles.9 Data also suggest that using VFTs exclusively might be highly fatiguing9 and that switching stimulation patterns from CFTs to VFTs may offset the rapid development of fatigue.10 However, these data were derived from short (167-ms) stimulation trains, whereas functional contractions require longer stimulation patterns, usually ranging from 2 to 6 s.4,11,12 If FES is to be used to facilitate exercise in people with SCI, it is important to find a stimulation pattern that would minimize fatigue to allow exercise at high intensities and for long durations. The aim of this preliminary study, conducted in able-bodied subjects, was to compare force and fatigue development in response to 2 stimulation patterns (CFT and CFT combined with VFT) and to evaluate if one is more fatigue-resistant for FES exercise. It was hypothesized that switching from the CFT pattern to the VFT pattern would overcome fatigue. MATERIALS AND METHODS
Thirteen healthy subjects who were accustomed to electrical stimulation (12 men, 1 woman, 4.1 6 2.4 h of physical activity per week, age 28.5 6 7.2 years, height 178.1 6 5.6 cm, body mass 75.0 6 7.6 kg, body mass index 23.4 6 2.2, body fat 11.4 6 4.1%) participated in the study. Subjects were instructed to refrain from training 48 hours before testing. The study was conducted according to the declaration of Helsinki, and approval for the project was obtained from the local Institutional Review Board. Each participant read and signed a written informed consent document outlining the procedures of the experiment.
Subjects.
Experimental Protocol. After an habituation session, each subject underwent 2 30-min testing sessions separated by at least 72 h. During each testing session, isometric muscle force was measured under different electrical stimulation train types. The CFT pattern corresponded to 6 s of MUSCLE & NERVE
May 2014
contraction at 40 HZ with a pulse width of 450 ls; the VFT pattern was an 80-HZ doublet followed by 6 s at 20 HZ with a pulse width of 450 ls. For all sessions, the stimulation program was applied to the right quadriceps muscle. Subjects were placed on an isokinetic dynamometer (Biodex corporation, Shirley, New York) with Velcro straps across the thorax for stability. The leg was fixed to the dynamometer lever-arm, and the axis of rotation of the dynamometer was aligned with the lateral femoral condyle. Stimulation programs were applied at an angle of 90 (0 corresponding to full extension). Stimulation was achieved with a Compex 2 unit (Compex, Medicompex SA, Ecublens, Switzerland) attached to 2 10 3 5 cm self-adhesive electrodes. Electrodes were placed over the muscle belly of the rectus femoris and the vastus medialis muscles. Following set-up, subjects performed 10 to 15 progressive repetitions of isometric contractions followed by 5 to 10 concentric leg extensions at 30 .s21 to warm up. Maximal isometric force was then determined by means of 2 5-s maximal voluntary contractions separated by 2 min (PRE MVC). Then, stimulation intensity was determined for the 2 programs to evoke 35% of each subject’s MVC; 6-s trains were applied every 6 s, and intensity was increased progressively by 10 mA until the evoked torque reached the target value (8–12 trains). Stimulation intensity determinations always started with the CFT pattern followed by VFT after 5 min of passive recovery. There were at least 10 min of rest after intensity determination before the 30-min program. At the end of the 30-min programs, subjects were asked to perform a maximal isometric voluntary contraction (POST MVC). On average, stimulation intensities were 86 6 13 mA during the CFT pattern and 100 6 17 mA during the VFT pattern. Data Analysis. The entire torque record for each session was digitized online at a 2 kHZ sampling frequency (Biopac sytems, Inc., Goleta, CA, USA). Fatigue was quantified using PRE and POST MVC and also by averaging the mean torque of the first and last 5 evoked contractions. The mean torque produced during the entire sessions was also calculated and termed “mean torque.” Lastly, custom written software (Matlab, MathWorks, Natick, Massachusetts) was used to determine the torque at the end of the 10 min of CFT during the MIX session and the time necessary to reach this torque while using VFT.
Data are expressed as mean 6 SD. A two-way analysis of variance with repeated-measures (program 3 time) was used. Program refers to MIX versus CFT, and Time to PRE vs POST. When the P-value from analysis of variance was significant, a post hoc Newman-Keuls test was used. A
Statistics.
Stimulation Pattern and Fatigue
FIGURE 1. (A) Maximal isometric torque before (black symbols) and immediately after (white symbols) the constant-frequency trains program (CFT) and the mixed program (MIX). (B) Average torque evoked during the first 5 (black symbols) and last 5 contractions (white symbols) of each program. Values are shown for each subject and are expressed as mean 6 SD. *statistical difference between PRE and POST values, §statistical difference between decreases obtained with CFT and MIX programs (P < 0.05).
paired t-test was used to compare the mean torque obtained with the 2 programs. Effect sizes (g2) were also determined, with values of 0.2, 0.5, and above 0.8 considered to represent small, medium, and large differences, respectively.13 Statistical significance was accepted when P < 0.05. RESULTS
Figure 1 shows that both stimulation programs induced significant fatigue (P < 0.05) as indicated by MVC decreases [from 278.0 6 61.0 N.m to 186.2 6 50.4 N.m (g2 5 1.64, large difference) and from 284.8 6 50.2 N.m to 217.1648.3 N.m (g2 5 1.37, large difference) for CFT and MIX, respectively]. Torque also decreased between the first and last 5 evoked contractions of the program (from 37.1 6 3.2 to 10.2 6 2.1 % of Pre MVC and from 35.2 6 1.6 to 12.4 6 2.4 % of Pre MVC for MUSCLE & NERVE
May 2014
761
CFT and MIX, respectively). These decreases were significantly greater after CFT than MIX (P < 0.05, large differences with g2 5 0.95 and g2 5 1.11 for MVC and evoked contractions, respectively). The MIX program allowed greater torque to be maintained for a longer time. On average, with MIX, the torque value recorded at the end of the first 10 min (CFT) was only reached after 400 6 250 s of the VFT program. This allowed greater mean torque over the whole MIX session as compared with the CFTs session (26.264.4 vs. 29.564.5 N.m, 113%, P < 0.05, g2 5 0.74, medium differences). DISCUSSION. We found that, in able-bodied subjects, a training session composed of CFTs followed by VFTs induced less fatigue and a greater mean torque than CFTs alone. These results are in accordance with several studies from the literature which reported that a series of CFTs followed by a series of VFTs reached a targeted isometric peak force more times than either CFT or VFT patterns alone.10,14 However, our results are original, given the noticeable differences between the commonly tested protocols and ours. Indeed, in previous studies, trains were 167-ms long, separated by 667 ms of recovery, whereas we chose to use stimulation characteristics close to those usually used during FES-strengthening protocols applied during an entire training session (30 min).4 Although not totally understood, several mechanisms may explain both the higher force production and better force maintenance with the MIX pattern compared with CFT. One of the proposed mechanisms focuses on the stretch of the series elastic elements. It has been suggested that a major effect of catch-like stimulations was to deliver the second pulse when the series elastic elements have been stretched by the contractile response to the first pulse.15,16 The second pulse following closely thereafter will then elicit a force response substantially greater than that of the sum of 2 twitches elicited separately.17 This “mechanical origin” could also explain the lower fatigue observed with the VFT pattern as compared with CFT. However, Ratkevicius and Quistorff18 did not find any difference in the ATP cost of the 2 protocols and concluded that the positive effects of the VFT pattern might be mediated by other mechanisms, such as potentiated Ca21 effects. Increased Ca21 release from the sarcoplasmic reticulum as a result of the initial high-frequency burst has frequently been proposed as a potential mechanism to explain force augmentation with VFTs.19 Moreover, it has been demonstrated that VFTs were particularly effective to augment force 762
Stimulation Pattern and Fatigue
production in fatigued muscles.18,20 It has been suggested that the Ca21 released in response to the initial high-frequency burst overcomes impairments of excitation-contraction coupling that result from reduced Ca21 release from the sarcoplasmic reticulum with fatigue. Ratkevicius and Quistorff,18 therefore, concluded that the major advantage of the VFT pattern is associated with the ability to produce more force in muscles affected by impairments of Ca21 release with fatigue. Lastly, another hypothesis is the motor unit recruitment in relation to stimulation frequencies. It is well known that electrical stimulation imposes continuous contractile activity to the same population of superficial muscle fibers despite neuromuscular transmission propagation failure,21 resulting in great decreases in force production. Changing the stimulation characteristics (frequency, intensity) is therefore the only way to depolarize new fibers. Moreover, it has been shown that lower stimulation frequencies led to less fatigue development.22 On these bases, one can suggest that, whereas CFTs recruit the same pool of motor units during the entire session, VFTs might involve a larger pool, therefore delaying the appearance of fatigue. This is even truer when switching from the CFT to the VFT pattern within the session. Indeed, although VFTs augment force production compared with CFTs, this pattern has been shown to induce an increase in fatigue when used during an entire session.9 In unpublished data from our laboratory we found that, although lower than with CFT, 30 min of the VFT pattern (6 s ON and 6 s OFF) resulted in greater reductions in MVC (227%) and evoked force (270%) than the MIX pattern. This might be explained partly by the higher intensities needed to evoke the required torque with VFTs. In conclusion, this study confirms previous results which suggest that a stimulation program combining CFT and VFT allows greater work and lower fatigue as compared with the CFT pattern only, likely as a result of differences in calcium processes and/or in fiber recruitment. Although they need to be confirmed by further investigation with additional measurements, these results are of particular interest for training and rehabilitation. Indeed, it can be hypothesized that repeated application (several times a week) of the MIX program would induce greater gains than those obtained with the CFT pattern strengthening protocols. Moreover, it would be interesting to adapt the protocol for an application during FES-cycling/ rowing. REFERENCES 1. Rattay F, Resatz S, Lutter P, Minassian K, Jilge B, Dimitrijevic MR. Mechanisms of electrical stimulation with neural prostheses. Neuromodulation 2003;6:42–56.
MUSCLE & NERVE
May 2014
2. Belanger M, Stein RB, Wheeler GD, Gordon T, Leduc B. Electrical stimulation: can it increase muscle strength and reverse osteopenia in spinal cord injured individuals? Arch Phys Med Rehabil 2000;81: 1090–1098. 3. Wheeler GD, Andrews B, Lederer R, Davoodi R, Natho K, Weiss C, et al. Functional electric stimulation-assisted rowing: increasing cardiovascular fitness through functional electric stimulation rowing training in persons with spinal cord injury. Arch Phys Med Rehabil 2002;83:1093–1099. 4. Taylor JA, Picard G, Widrick JJ. Aerobic capacity with hybrid FES rowing in spinal cord injury: comparison with arms-only exercise and preliminary findings with regular training. PM R. 2011;3:817–824. 5. Isakov E, Mizrahi J, Najenson J. Biomechanical and physiological evaluation of FES-activated paraplegic patients. J Rehabil Res Dev 1986;23:9–19. 6. Binder-Macleod SA, Barker CB III. Use of a catchlike property of human skeletal muscle to reduce fatigue. Muscle Nerve 1991;14:850– 857. 7. Binder-Macleod SA, Scott WB. Comparison of fatigue produced by various electrical stimulation trains. Acta Physiol Scand 2001;172: 195–203. 8. Burke RE, Rudomin P, Zajac FE. Catch property in single mammalian motor units. Science 1970;168:122–124. 9. Binder-Macleod SA, Lee SCK, Russ DW, Kucharski LJ. Effects of activation pattern on human skeletal muscle fatigue. Muscle Nerve 1998;21:1145–1152. 10. Scott WB, Binder-Macleod SA. Changing stimulation patterns improves performance during electrically elicited contractions. Muscle Nerve 2003;28:174–180. 11. Crameri RM, Weston AR, Rutkowski S, Middleton JW, Davis GM, Sutton JR. Effects of electrical stimulation leg training during the acute phase of spinal cord injury: a pilot study. Eur J Appl Physiol 2000; 83:409–415.
Stimulation Pattern and Fatigue
12. Sabatier MJ, Stoner L, Mahoney ET, Black C, Elder C, Dudley GA, et al. Electrically stimulated resistance training in SCI individuals increases muscle fatigue resistance but not femoral artery size or blood flow. Spinal Cord 2006;44:227–233. 13. Cohen J. Statistical power analysis for the behavioral sciences, 2nd ed. Hillsdale, NJ: Lawrence Erlbaum Associates; 1988. 14. Scott WB, Lee SC, Johnston TE, Binder-Macleod SA. Switching stimulation patterns improves performance of paralyzed human quadriceps muscle. Muscle Nerve 2005;31:581–588. 15. Parmiggiani F, Stein RB. Nonlinear summation of contractions in cat muscles. II. Later facilitation and stiffness changes. J Gen Physiol 1981;78:295–311. 16. Bigland-Ritchie B, Zijdewind I, Thomas CK. Muscle fatigue induced by stimulation with and without doublets. Muscle Nerve 2000;23: 1348–1355. 17. Binder-Macleod SA, Lee SC. Catchlike property of human muscle during isovelocity movements. J Appl Physiol 1996;80:2051–2059. 18. Ratkevicius A, Quistorff B. Metabolic costs of force generation for constant-frequency and catchlike-inducing electrical stimulation in human tibialis anterior muscle. Muscle Nerve 2001;25:419–426. 19. Abbate F, Bruton JD, De Haan A, Westerblad H. Prolonged force increase following a high-frequency burst is not due to a sustained elevation of [Ca21]i. Am J Physiol Cell Physiol 2002;283:C42– C47. 20. Duchateau J, Hainaut K. Nonlinear summation of contractions in striated muscle. II. Potentiation of intracellular Ca21 movements in single barnacle muscle fibers. J Muscle Res Cell Motil 1986;7:18–24. 21. Zory R, Boeerio D, Jubeau M, Maffiuletti NA. Central and peripheral fatigue of the knee extensor muscles induced by electromyostimulation. Int J Sports Med 2005;26:847–853. 22. Binder-Macleod SA, Snyder-Mackler L. Muscle fatigue: clinical implications for fatigue assessment and Neuromuscular Electrical Stimulation. Phys Ther 1993;73:902–910.
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