Kilohertz and Low-Frequency Electrical Stimulation

ORIGINAL RESEARCH ARTICLE

Kilohertz and Low-Frequency Electrical Stimulation With the Same Pulse Duration Have Similar Efficiency for Inducing Isometric Knee Extension Torque and Discomfort Flávia Vanessa Medeiros, MS, Martim Bottaro, PhD, Amilton Vieira, PhD, Tiago Pires Lucas, PT, Karenina Arrais Modesto, PT, Antonio Padilha L. Bo, PhD, Gerson Cipriano, Jr, PhD, Nicolas Babault, PhD, and João Luiz Quagliotti Durigan, PhD Objective: To test the hypotheses that, as compared with pulsed current with the same pulse duration, kilohertz frequency alternating current would not differ in terms of evoked-torque production and perceived discomfort, and as a result, it would show the same current efficiency. Design: A repeated-measures design with 4 stimuli presented in random order was used to test 25 women: (1) 500-microsecond pulse duration, (2) 250-microsecond pulse duration, (3) 500-microsecond pulse duration and low carrier frequency (1 kHz), (4) 250-microsecond pulse duration and high carrier frequency (4 kHz). Isometric peak torque of quadriceps muscle was measured using an isokinetic dynamometer. Discomfort was measured using a visual analog scale. Results: Currents with long pulse durations induced approximately 21% higher evoked torque than short pulse durations. In addition, currents with 500 microseconds delivered greater amounts of charge than stimulation patterns using 250-microsecond pulse durations (P < 0.05). All currents presented similar discomfort. There was no difference on stimulation efficiency with the same pulse duration. Conclusions: Both kilohertz frequency alternating current and pulsed current, with the same pulse duration, have similar efficiency for inducing isometric knee extension torque and discomfort. However, neuromuscular electrical stimulation (NMES) with longer pulse duration induces higher NMES-evoked torque, regardless of the carrier frequency. Pulse duration is an important variable that should receive more attention for an optimal application of NMES in clinical settings. Key Words: Current Efficiency, Electrotherapy, Physical Medicine, Rehabilitation (Am J Phys Med Rehabil 2017;96:388–394)

achieve neuromuscular adaptations for rehabilitation purposes, maximum muscle force should be elicited while limiting the perceived discomfort.2 Gains in muscle strength are directly related to the degree of tension of the muscle contraction elicited by NMES. So, to induce high levels of tension and consequently to generate high joint torques, NMES current intensity should be as high as possible.3 However, the strong discomfort associated with the peripheral stimulation limits the current dose and consequently the muscle activation, thereby becoming one important limitation to reach high levels of muscle strength by means of NMES during rehabilitation settings.1,2,4 As the NMES current intensity and pulse duration increase, the evoked torque and resulting force gains augment,2,5 because a larger number of motor units are activated.6 However, discomfort also increases.2,7 Thus, discomfort is considered as a limiting factor in the effectiveness of NMES.2 Two types of NMES currents frequently used are lowfrequency pulsed current (PC) and kilohertz frequency alternating

current (KFAC).8 In theory, KFAC has the advantage to lower skin impedance, which allows less electrical energy to dissipate peripherally and more electrical energy to penetrate into the muscle at terms, and may generate stronger muscle contractions and less discomfort.9 Nevertheless, there are not a clear consensus on which NMES is best to induce higher evoked torque with fewer discomfort.10 The evoked torque and perceived discomfort are directly affected not only by the type of current applied (PC KFAC), but also by the current frequency, pulse duration, and burst duty cycle of KFACs.11,12 Previous research has pursued to determine whether PC or KFAC is more efficacious (current efficiency), that is, elicits greater muscle force with less current intensity.11,13–15 However, the results of these studies do not present a clear consensus on which current type is the best. Recently, a systematic review with meta-analysis has shown that KFAC and PC have similar effects on quadriceps-evoked torque and self-reported discomfort in healthy individuals.10 However, this systematic review reported numerous experimental bias resulting from experimental design (nonblinded and nonrandomized conditions), different muscles assessed, subject recruitment (not

From the Physical Education Department (FVM, MB, AV), Physiotherapy Division (TPL, KAM, GC, JLQD), and Electrical Engineering Department (APLB), University of Brasilia, Federal District, Brazil; and Centre d’Expertise de la Performance G. Cometti, UFR STAPS, Université de Bourgogne, Dijon, France (NB). All correspondence and requests for reprints should be addressed to: João Luiz Quagliotti Durigan, PhD, University of Brasília, College of Ceilândia, Federal District, Centro Metropolitano, conjunto A, lote 01, 72220-900, Brasília, DF, Brazil. This project was supported by the Fundação de Amparo à Pesquisa do Distrito Federal (FAPDF; process no. 193.000.862/2014), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; process no. 447529/2014-5),

and by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES; process no. 88881.068106/2014-01). AV held a PhD grant sponsored by CNPq (process no. 132387/2010-7). TPL and KAM held a scientific initiation fellowship sponsored by CNPq (106927/2013-2). Financial disclosure statements have been obtained, and no conflicts of interest have been reported by the authors or by any individuals in control of the content of this article. Copyright © 2016 Wolters Kluwer Health, Inc. All rights reserved. ISSN: 0894-9115 DOI: 10.1097/PHM.0000000000000631

euromuscular electrical stimulation (NMES) is an imporN tant therapeutic resource used to reduce pain sensation, reduce muscle atrophy, and increase strength. In order to 1

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American Journal of Physical Medicine & Rehabilitation • Volume 96, Number 6, June 2017

Copyright © 2017 Wolters Kluwer Health, Inc. All rights reserved.

Volume 96, Number 6, June 2017

Electrical Therapy on Peak Torque and Discomfort

considering gender and menstrual cycle effects on individual responses to NMES, and mainly the heterogeneity of NMES parameters, which could affect the main outcomes.10 According to these conflicting results, a dependency of evoked-torque and discomfort on BDC, pulse duration, and frequency for the quadriceps muscle should be investigated to determine the best parameters to induce maximum evoked torque with minimum discomfort for an optimal application of NMES in clinical rehabilitation. Considering potential differences between KFAC and PC currents, the aim of this study was to test the hypotheses that, as compared with PC with the same pulse duration, KFAC would not differ in terms of evoked-torque production and perceived discomfort, and as a result, it would show the same current efficiency. In order to compare KFAC currents parameters to PCs in a rigorous way, efforts were made to match the stimulation parameters between the different NMES conditions. These findings may help the rehabilitation team to design more efficient stimulation treatments when the goal is to acutely induce high level of knee joint torque and chronically generate gains in muscle strength.2

METHODS

of motion and function. Subjects self-reported activity levels using the International Physical Activity Questionnaire, and all reported participating in vigorous aerobic-type exercise for at least 20 minutes 3 or more times weekly, moderate-intensity activity 5 or more times weekly, or walking at least 30 minutes daily. Subjects who did not feel comfortable with NMES and did not reach the evoked-torque level of 30% maximal voluntary torque (MVC) were excluded. Subjects were all tested between 8:00 and 11:00 AM in the same room kept at 24°C (SD, 2°C). In addition, data were collected between the first and seventh day of the menstrual cycle (inactive phase), in order to standardize the discomfort perception among volunteers.16 Volunteers were asked to avoid stimulants (e.g., alcohol, caffeine, chocolate) and exercise on test days. They were instructed to maintain their normal hydration in order to ensure that they were in a hydrated state. Volunteers were informed of all the procedures, purposes, benefits, and risks of the study and signed an informed consent form. The research was approved by the institution’s ethics committee in accordance with the Helsinki Declaration of 1975. Before participation, each volunteer read and signed a detailed informed consent form approved by the Ethical Committee on Human Research within the Faculty of Health Sciences 2958-13 of the University of Brasília.

Subjects

Experimental Approach to the Problem

Twenty-five healthy women (mean age, 21 [SD] 3]years; body mass: 59 [SD, 9] kg; height, 162 [SD, 5] cm; quadriceps skinfold thickness, 25 [SD, 6] mm; body fat, 24.4% [SD, 5.1%]; BMI, 22.2 [SD, 0.1] kg/m2) participated voluntarily in this study. Sample size was determined a priori using G*Power (version 3.1.3; University of Trier, Trier, Germany), with the level of significance set at P = 0.05 and power (1 − β) = 0.95 in order to detect a large effect ( f 2 > 0.47). We conducted a pilot study with 5 participants to evaluate the effect size for the main dependent variable (evoked torque from all currents). Based on these a priori calculations and the pilot study, the final sample size was selected. Volunteers were not involved in any resistance training for at least 6 months prior to the beginning of the study and did not have previous experience with NMES. In addition, they met the following criteria: healthy, body mass index between 20 and 25 kg/m2, physically active, and with normal knee range

Subjects performed 2 visits to the laboratory on 2 separate days with a minimum interval of 5 days in between. The first visit served to familiarize subjects with NMES, equipment, and testing procedures and to perform anthropometric measurements to determine height, body mass, and skinfold thickness to estimate body composition. Each subject was tested with 4 different conditions randomly presented: PC500 (50 Hz, 500 microseconds), PC250 (50 Hz, 250 microseconds), KFAC500 (500 microseconds, 1000 Hz), and KFAC250 (250 microseconds, 4000 Hz). Pulsed current is typically delivered with frequency in a range of 1 to 100 Hz and pulse duration ranging from 100 to 500 microseconds.8 Kilohertz frequency alternating current is defined by a biphasic alternating medium frequency carrying current, with either a sinusoidal or rectangular waveform. This current is delivered with frequencies ranging between 1 and 10 kHz, with a burst frequency between 1 and 200 Hz and a burst duty cycle of 10% or more.8,9

TABLE 1. Neuromuscular electrical stimulation parameters for KFAC and PC PC

Pulse frequency Pulse duration Carrier frequency Burst frequency Burst duty cycle Stimulus on time (rise time/fall time) Interburst interval

Alternating Current

PC500

PC250

KFAC500

KFAC250

50 Hz 500 μs Not applicable Not applicable Not applicable 10 s (1/1 s) Not applicable

50 Hz 250 μs Not applicable Not applicable Not applicable 10 s (1/1 s) Not applicable

Not applicable 500 μs 1 kHz 50 Hz 2 ms/10% 10 s (1/1 s) 18 ms

Not applicable 250 μs 4 kHz 50 Hz 4 ms/20% 10 s (1/1 s) 16 ms

PC500, PC with 500 microseconds of pulse duration; PC250, PC with 250 microseconds of pulse duration; KFAC500, KFAC with 500 microseconds of pulse duration; KFAC250, KFAC with 250 microseconds of pulse duration.

© 2016 Wolters Kluwer Health, Inc. All rights reserved.


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FIGURE 1. Representative evoked torque-time traces obtained in the 4 conditions. Currents with the same pulse duration did not show any torque difference. PC500 induced higher evoked torque than PC250 and KFAC250 (P < 0.001). KFAC500-evoked torque was higher than PC250 and than KFAC250.

Additional parameters are described in Table 1. All physical parameters of the stimulator were checked using a digital oscilloscope (DS1050E; Rigol, Oakwood Village, Ohio). Maximum NMES current intensity was determined by gradually increasing intensity until subjects indicated to the operator that their

tolerance limit was reached. Three to 4 attempts were used. This intensity was recorded to be reproduced in the second visit. The second visit included warm-up, assessment of MVC torque, and assessment of NMES torque (Fig. 1). All procedures were performed on the dominant (kicking) side. Subjects

FIGURE 2. Flowchart of the randomized double-blind trial.

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were positioned into the chair of an isokinetic dynamometer (System 3; Biodex Medical Systems, Shirley, New York) with the hip at 100 degrees. The axis of the dynamometer was aligned with the axis of rotation of the knee. The lever arm of the dynamometer was parallel to the anterior aspect of the tibia, with the lower edge of the pad positioned approximately 3 cm proximal to the lateral malleolus. The trunk, waist, and thigh were stabilized using straps. Calibration of the dynamometer was performed before each testing session according to the manufacturer’s specifications. In addition, the subjects had the thigh shaved and the skin cleaned with isopropyl alcohol. Subsequently, subjects completed a warmup consisting of 10 submaximal concentric voluntary knee extensions at 180 degrees per second through a 90-degree range of motion. Then, isometric MVC torque was assessed at 60 degrees of knee flexion. Subjects were requested to perform three 10-second MVC separated by a 3-minute rest interval. During voluntary contractions, participants were encouraged verbally and received visual torque feedback

during each repetition. The greatest peak torque achieved was used for further analysis. Then NMES evoked torque was measured. The stimulator (Neurodyn 2.0; Ibramed, São Paolo, Brazil) was connected to isolated cables, and the cables were connected to 2 pairs of self-adhesive electrodes each measuring 50 50 mm (Valutrode; Axelgaard, Fallbrook, California). For channel 1, the distal electrode was placed at 80% on the line between the anterior superior iliac spine and the anterior border of the medial ligament. The proximal electrode was placed 10 to 15 cm above the distal electrode on the vastus medialis muscle.17 For channel 2, the distal electrode was positioned at 2/3 on the line from the anterior superior iliac spine to the lateral border of the patella on the vastus lateralis muscle, and the proximal electrode was placed 10 to 15 cm above the distal electrode on the vastus lateralis muscle.17 All current modalities were delivered with an “on” time of 10 seconds, with 1 second of ramp-up, and 3-minute rest intervals. Current intensity started from 0 mA and was manually rapidly increased to reach the maximum

FIGURE 3. A, Maximal NMES current intensity elicited by the different NMES protocols. Values are mean (SD). *Significant difference compared with another current (P < 0.05). B, Maximal NMES-evoked torque elicited by the different NMES protocols. Values are mean (SD) presented as a percentage of maximal voluntary contraction. *Significant difference compared with another current (P < 0.05). © 2016 Wolters Kluwer Health, Inc. All rights reserved.


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tolerable intensity determined during the familiarization session. The highest evoked torque was measured at 3 contractions after the subjects reported having attained the maximal tolerated current intensity. The highest evoked torque (peaktorque) of the 3 contractions was recorded for analysis and normalized with respect to the MVC [(evoked voluntary−1) 100]. Also the maximal tolerated intensity was registered. Subjects were instructed to fully relax during NMES in order to enable measurement of evoked torque only. The study was conducted as a double-blind experiment, in which both the volunteers and operator did not know which current was applied. For this, a black cover was placed on the equipment panel to maintain the parameters blinded, except for the intensity current. The total phase charge of an impulse was expressed in microcoulombs (μC). The phase charge was estimated using the formula Qp = it, where Qp represents the phase charge in μC, i is the current intensity in mA, and t is the phase duration in milliseconds.18–20 Finally, the efficiency of stimulation was calculated as NMES-evoked torque/current intensity (N · m · mA−1).21 The maximal discomfort level was assessed by means of a 100-mm visual analog scale (VAS), with 0 representing “no discomfort" and 100 representing “maximum tolerated discomfort.” The VAS was shown to participants when they reported having attained the maximal tolerated current intensity after maximal NMES-evoked torque assessment. They were asked to point a mark on a VAS to rate the level of discomfort. In addition, all the participants had zero pain at baseline evaluation.

Statistical Analysis Values for NMES-evoked torque, NMES-induced discomfort, NMES current intensity, and stimulation efficiency are reported as mean (SD). We used parametric tests given that data were normally distributed (Shapiro-Wilk test) and had homogeneous variances (Levene test). Repeated-measures analyses of variance were conducted for NMES-evoked torque, NMES current intensity, NMES-induced discomfort, and stimulation efficiency. The Bonferroni post hoc test was used. All statistical analyses were performed using SPSS 21 (SPSS Inc., Chicago, Illinois). Significance threshold was set at P < 0.05 for all procedures.

RESULTS A flowchart of this experimental randomized double-blind trial is shown in Figure 2. Thirty-seven individuals were assessed

for eligibility. Among them, 4 subjects did not achieve the minimum evoked-torque level (30% of the MVC), 2 were intolerant to NMES, 3 did not follow the orientations, and 3 subjects did not return to the second day of test. Thus, 25 subjects received the interventions. There was no significant difference in MVC torque between the familiarization and test sessions (156.3 [SD, 21.1] N · m and 158.9 [SD, 29.2] N · m, respectively, P = 0. 57). For current intensity (Fig. 3A, statistical power = 0.99), there was no difference comparing PC500 to KFAC500 (P > 0.05), as well as when comparing PC250 and KFAC250 (P > 0.05). PC500 required approximately 33% lower current intensity than PC250 and KFAC250 (P < 0.01). KFAC500 required approximately 23% lower current intensity than PC250 and KFAC250 (P < 0.01). Similar results were observed for NMES-evoked torque (Fig. 3B, statistical power = 0.89). Currents with the same pulse duration did not show any torque difference (P > 0.05). However, PC500 induced 21% higher evoked torque than PC250 ( 0.05) and for KFAC250 as compared with PC250 (P > 0.05; Table 2, statistical power = 0.98). PC500 delivered greater phase charge than PC250 (P < 0.01) and compared with KFAC250 (P < 0.01). KFAC500 delivered more phase charge than PC250 (P < 0.001), as well as KFAC250 (P < 0.001). Comparable results were observed in current efficiency (Table 2, statistical power = 0.99). PC500 efficiency was greater than PC250 (P < 0.01), as well as when compared with KFAC250 (P < 0.01). KFAC500 efficiency induced more efficiency than PC250 (P < 0.001) and KFAC250 (P < 0.001). Nonetheless, there was no difference on current efficiency with the same pulse duration (P > 0.05). Because of statistical power exceeding 90% in comparisons that were not significant, we are confident that the study was appropriately powered to detect significant differences among means when they existed.

DISCUSSION In agreement with our initial hypothesis, the present study showed that KFAC and PC with the same pulse duration induced similar torque, discomfort, and current efficiency. In addition, the present results revealed a dependency on BDC for KFAC and pulse duration for PC. Considering that the key factor for optimizing NMES effectiveness has been related

TABLE 2. Perceived discomfort, phase charge, and current efficiency elicited by the different NMES protocols PC500

KFAC500

PC250

KFAC250

Discomfort (0–10) 7.80 (1.47) 7.66 (1.26) 6.96 (1.75) 7.13 (0.89) 13.71 (2.36), P < 0.01,b P < 0.001c Phase charge (μC) 18.51 (5.54) 21.01 (5.39), P < 0.001a 13.85 (1.6), P < 0.001b,c Current efficiency (N · m · mA−1) 0.78 (0.29) 0.68 (0.20), P < 0.001a 0.41 (0.11), P < 0.01,b P < 0.001c 0.40 (0.15), P < 0.01,b P < 0.001c Values for discomfort, phase charge, and current efficiency are reported as mean (SD). All currents presented similar discomfort (P = 0.10). a For phase charge, a significant difference compared with PC250 (P < 0.001); for current efficiency, a significant difference compared with PC500 (P < 0.01). b For phase charge, a significant difference compared with PC500 (P < 0.001); for current efficiency, a significant difference compared with PC250 (P < 0.001). c For phase charge, a significant difference compared with KFAC500 (P < 0.001); for current efficiency, a significant difference compared with KFAC500 (P < 0.001).

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to the level of evoked torque with low discomfort perception,2,22 it is reasonable to expect that current modulated with long pulse duration or lower BDC is more suitable for higher NMES training-induced strength gains. This information is essential to guide decision making concerning NMES protocols in clinical settings. Although KFAC was hailed as advantageous in terms of comfort and strength of contractions in the early studies of the 1970s,9 recent studies comparing the efficiency among KFAC and PC produced inconclusive or contradictory findings.11,23,24 The first reported use of BDC was performed by Kots in 1976, who claimed that KFAC with 2.5 kHz (BDC of 50%) could produce force gains of up to 40% in elite athletes compared with voluntary exercises.8 However, lower BDC was not tested, and it appears to have been arbitrarily chosen. Confounding these data is that different BDCs and pulse duration have been used when comparing KFAC and PCs. Ward and colleagues25 demonstrated that KFAC with 500 microseconds induced similar evoked torque compared with PC, although KFAC was more comfortable. In a recent study, Dantas et al.11 showed that KFAC with 500 microseconds and PC were similar for inducing isometric knee extension torque and discomfort perception, whereas KFAC with 250 microseconds was less effective. Similarly, Szecsi and Fornusek 21 demonstrated that KFAC with 50% of BDC (250 microseconds) is equivalent to PC stimulation in terms of evoked torque. However, KFAC stimulation at low BDC (7%–18%) was more effective (+35% torque produced with similar discomfort) than PC or conventional KFAC. Finally, a recent metaanalysis concluded that both KFAC and PC provided similar quadriceps evoked-torque and self-reported discomfort level.10 Collectively, the theoretical statement that KFAC is optimal for muscle strengthening is unclear, because there is no difference between KFAC and PC while using matched parameters in terms of evoked torque and current efficiency. In fact, we clearly demonstrated that pulse duration is the best parameter for torque production. The currents delivered with 500microsecond pulse duration (KFAC500 and PC500) evoked torque approximately 58% of MVC, whereas those modulated with 250 microseconds (KFAC250 and PC250) induced approximately 45% of MVC. In addition, the present study analyzed the efficiency of a given stimulation condition by the relationship between torque and current intensity, which means the higher torque output magnitude with applying the lowest intensity current.22,26 In fact, the current efficiency was similar with currents applying the same pulse duration and phase charge. Therefore, clinicians could choose KFAC or PC and expect similar strength training effects. It is also important to observe that stimulus with longer pulse duration (500 microseconds) required approximately 33% lower current intensity and induced approximately 21% higher evoked torque when compared with stimulus with short pulse duration. We also demonstrated that currents of longer pulse duration delivered greater amount of charge eliciting higher NMES-evoked torque, although required lower current intensity. This result was expected because theoretically NMESevoked torque should be greater for the higher amount of charge delivered to muscle.6,20 Gregory et al.27 studied the influence of NMES on evoked torque by applying constant current stimulation trains (500 milliseconds) and by varying

pulse frequencies and pulse duration (100–700 microseconds). They concluded that estimated total charge plays a key role on evoked torque elicited by NMES; that is, there is a charge dependency of the degree of motor unit recruitment explained by the effects of pulse duration on evoked torque. Then, the longer the pulse/train duration, the greater is the injected charge of the stimulation pulse/train.27,28 This behavior could be explained by longer pulse duration recruiting a greater number of motor units in relation to the cross-sectional area of the stimulated muscle. In our experimental conditions, phase charge and pulse duration were found the main determinant of the evoked torque and stimulation efficiency responses, whereas carrier frequency (KFAC compared with PC) showed no effects on these outcomes. In addition of this, Bergquist et al.29 suggested that the current at shorter pulse duration (0.05–0.4 microsecond) activates contractions primarily by sensory pathways, with no involvement of the central nervous system, whereas with longer pulse duration (0.5–1 microsecond) the activation can be generated by a combination of peripheral pathways and central pathways leading to the development of greater evoked-torque production. Then, longer pulse duration induces greater NMES-evoked torque by activation of motor neurons that triggers motor axons beneath the stimulating electrodes, as central pathways, through the electrically volley.30 In order to compare the discomfort level between PC and KFAC, previous studies found divergent results. Dantas et al.11 showed that there was no significant difference among them, whereas Ward et al.25 showed that KFAC was more comfortable compared with PC. However, this divergence could be due to differences in methodological procedures. Dantas et al.11 evaluated the level of NMES-induced discomfort immediately after application of the stimulus, whereas Ward et al.25 assessed discomfort during stimulation. Ward and colleagues25 used monophasic low-frequency current that induced electrochemical alteration, because of polar effects contributing to greater discomfort.9 Moreover, methods used by researchers to evaluate discomfort were also heterogeneous. The majority of the studies have used VAS,13–15 whereas others25 have measured the number of discomfort reports, creating difficulties in comparing outcomes among studies. It is noteworthy that determination of relative comfort associated with NMES is difficult to assess because of subjective and multidimensional nature of discomfort. Although VAS and numerical rating scales have been broadly used, these tools are related to the physical dimension (current intensity and muscle contraction intensity), ignoring emotional factors. Researchers studying the discomfort associated with NMES have concluded that emotional dimension can interfere in a subject’s response in relation to the perception of NMES discomfort, resulting in great deal of individual variability.4 So, prior negative experience with NMES, fear, apprehension, and anxious level can result in added discomfort associated to electrical stimulus.4 It is important to recognize limitations of this study. As our research was conducted with young and healthy women, future studies with clinical population and athletes are necessary to compare muscle adaptations on NMES-evoked torque and discomfort in relation to KFAC and PC settings. Moreover, as the



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study focused only to assess the acute effects of different NMES currents, we suggest conducting additional studies in order to address the chronic training effects for the various types of current in both healthy and clinical populations. In conclusion, despite the claim that KFAC is best to induce comfort and strength of contractions, our results clearly demonstrated that both KFAC and PC with the same pulse duration produce similar isometric knee extension torque. However, when NMES is indicated to induce higher NMESevoked torque, the longer pulse duration is more suitable, despite the carrier frequency parameters. These results suggest that pulse duration is an important variable that should receive more attention for an optimal application of NMES therapy in clinical settings.

ACKNOWLEDGMENTS The authors thank the Electrical Engineer Department, for the support in checking the calibration of the electrical stimulation device. The authors also thank Prof. Nicola A. Maffiuletti (Neuromuscular Research Laboratory, Zurich, Switzerland) because of critical revision and comments that improved our manuscript. REFERENCES 1. Salvini TF, Durigan JL, Peviani SM, et al: Effects of electrical stimulation and stretching on the adaptation of denervated skeletal muscle: implications for physical therapy. Rev Bras Fisioter 2012;16:175–83 2. Maffiuletti NA, Minetto MA, Fari D: Electrical stimulation for neuromuscular testing and training: state-of-the art and unresolved issues. Eur J Appl Physiol 2011;111:2391–7 3. Maffiuletti NA: Physiological and methodological considerations for the use of neuromuscular electrical stimulation. Eur J Appl Physiol 2010;110:223–34 4. Delitto A, Strube MJ, Shulman AD, et al: A study of discomfort with electrical stimulation. Phys Ther 1992;72:410–21; discussion on 414–21 5. Medeiros FV, Vieira A, Carregaro RL, et al: Skinfold thickness affects the isometric knee extension torque evoked by neuromuscular electrical stimulation. Braz J Phys Ther 2015;19:466–72 6. Selkowitz DM, Rossman EG, Fitzpatrick S: Effect of burst-modulated alternating current carrier frequency on current amplitude required to produce maximally tolerated electrically stimulated quadriceps femoris knee extension torque. Am J Phys Med Rehabil. 2009;88:973–8 7. Laufer Y, Ries JD, Leininger PM, et al: Quadriceps femoris muscle torques and fatigue generated by neuromuscular electrical stimulation with three different waveforms. Phys Ther 2001;81:1307–16 8. Ward AR, Shkuratova N: Russian electrical stimulation: the early experiments. Phys Ther 2002;82:1019–30 9. Robertson V, Ward A, Low J, et al: Electrotherapy Explained: Principles and Practice, 4th ed. Atlanta, GA: Elsevier Health Sciences; 2006 10. da Silva VZM, Durigan JLQ, Arena R, et al: Current evidence demonstrate similar effects of Kilohertz-frequency and low-frequency current on quadriceps evoked torque and

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