|Year : 2021 | Volume
| Issue : 2 | Page : 51-58
Comparison of short-term training effects of two neuromuscular electrical stimulation modalities on muscle functions and mass
Abdulaziz Aldayel, Saad Khalid Aljaloud, Sulaiman O Aljaloud
Department of Exercise Physiology, College of Sport Sciences and Physical Activity, King Saud University, Riyadh, Saudi Arabia
|Date of Submission||05-Jun-2021|
|Date of Acceptance||29-Jul-2021|
|Date of Web Publication||02-Oct-2021|
Department of Exercise Physiology, College of Sport Sciences and Physical Activity, King Saud University, Riyadh
Purpose: The present study thus aimed to compare the effects of neuromuscular electrical stimulation (NMES) training, using alternating current (AC) and pulsed current (PC), on muscle function and muscle mass.
Methods: Twenty-thee healthy male university students (age: 22.68 ± 3.7) were enrolled in this study and divided into two groups (AC = 12, PC = 11) to receive NMES training in both legs simultaneously. Each group underwent a 20-min NMES session using AC or PC, 2 days a week for 5 weeks. AC was delivered at 2.5 kHz (burst frequency: 75 Hz and pulse duration: 400 μs) for the knee extensors of both legs, and PC was delivered at 75 Hz (pulse duration: 400 μs), inducing 60 isometric contractions (on–off ratio: 5–15 s) at a knee joint angle of 100° (0° = full extension). Muscle strength, power, and mass were assessed 1 week before and 1 and 6 weeks after the training program.
Results: Findings show a significant increase in vertical jump height after both NMES training, although no torque gain was detected regardless of the type of modality. A significant increase in the region fat-free mass (trained legs) in both NMES currents without a difference between them was observed in the function of the trained muscles.
Conclusion: Short-term training (5 weeks) using AC or PC could be insufficient to detect an improvement in muscle functions such as torque gain. However, the short-term training using AC may improve physical performance and body composition.
Keywords: Dual-energy X-ray absorptiometry, lean mass, muscle strength, vertical jump
|How to cite this article:|
Aldayel A, Aljaloud SK, Aljaloud SO. Comparison of short-term training effects of two neuromuscular electrical stimulation modalities on muscle functions and mass. Saudi J Sports Med 2021;21:51-8
|How to cite this URL:|
Aldayel A, Aljaloud SK, Aljaloud SO. Comparison of short-term training effects of two neuromuscular electrical stimulation modalities on muscle functions and mass. Saudi J Sports Med [serial online] 2021 [cited 2021 Dec 3];21:51-8. Available from: https://www.sjosm.org/text.asp?2021/21/2/51/327484
| Introduction|| |
Neuromuscular electrical stimulation (NMES) has been widely used in sports training to increase muscle strength,,, power performance,,, muscle mass, and cardiorespiratory endurance and as a complementary method for voluntary exercise training. The use of NMES in healthy populations has been increasing in the last few decades., However, the optimal parameters and currents of NMES to maximize its effects have not been confirmed.,
Numerous studies have investigated the effects of NMES training using either pulsed current (PC),,, or alternating current (AC),, on muscle functions and/or muscle hypertrophy. In a systematic review based on a meta-analysis, Bax et al. have concluded that NMES could effectively increase muscle strength; however, they have suggested the need for further research to understand the optimal parameters of NMES. In addition, a combination of NMES and voluntary training modalities is needed to optimize muscle function improvement.
In a study, both PC and AC NMES training seemed to enhance muscle function; however, only a few studies have compared them. Three-week NMES training (10 min daily) using AC (2500 Hz at 25 Hz) and PC (25 Hz) of the quadriceps muscle for each current type was compared in a study by Stefanovska and Vodovnik on five healthy individuals; they have found a higher increase in the maximal voluntary torque after PC (25% of the maximum voluntary contraction [MVC]) than after AC (13% of MVC). Bircan et al. have compared AC (2.5 kHz at 80 Hz) and PC (80 Hz) and reported no significant difference between the two protocols in terms of the increase in isokinetic strength (18.5% vs 22.7%, respectively) after 3-week NMES training (15 min per session and 5 days a week). In terms of force production during NMES, Snyder-Mackler et al. have found that AC produced 20% more force (2.5 kHz) than PC (50 Hz); however, AC with a higher burst frequency (4 kHz) produced 20% less force than PC. Another study has compared three types of NMES waveforms: PC monophasic (50 Hz), biphasic (50 Hz), and polyphasic (2.5 kHz in 50 Hz) and found that in monophasic and biphasic waveforms, PC produced significantly greater force (36.3% and 38.0%, respectively, of the maximal voluntary isometric contraction [MVIC]) than AC (30.9% of MVIC). A recent study has shown no difference in the peak torque between PC (75 Hz) and AC (2.5 kHz in 75 Hz). Thus, whether the effects of NMES training on muscular strength are different between PC and AC is not yet clear.
In addition, the effects of NMES training on explosive movements, such as jumping, have been of interest to several researchers. Some studies have reported the effects of NMES using PC along with resistance training on vertical jump height.,,,, For example, 12 weeks of NMES training using PC (100 Hz) in rugby players resulted in a significant improvement in squat jump (SJ) (11.8%) and drop jump (DJ) (7.6%) performance. However, no study has investigated the effect of NMES training alone on jump performance. Furthermore, studies that have used AC NMES to examine its effect on jump performance are still rare and debatable.
Applying NMES may prevent muscle atrophy and cause hypertrophy of denervated muscles in patients with spinal cord injuries., However, the effects of NMES training on muscle hypertrophy in healthy individuals remain controversial. A significant increase in the cross-sectional area in healthy populations has been reported in some studies,, but not in others or at least it has be involved in a hybrid approach. For example, Matsuse et al. have reported that NMES hybrid training with volitional contraction significantly increases the elbow flexion and extension torques (56% and 31%, respectively), which were similar to or larger than the gains in conventional exercise. Most studies have used PC NMES to investigate the effects of NMES on muscle hypertrophy, and only the study by Matsuse et al. has used AC NMES.
Authors hypothesis that AC is more effective to enhance muscle function and cause less muscle damage compared to PC. The outcomes of this study may partly contribute to the existing body knowledge on the effects of PC and AC on muscle function, muscle damage, and hormonal responses and provide better understanding of the application of NMES in sports training. Thus, this study compares the effects of AC and PC NMES training on muscle function and mass.
| Methods|| |
Twenty-three healthy active male university students (mean age: 22.68 ± 3.7 years) have been recruited from King Saud University. The inclusion criteria included the range of age between 18 and 35 years old, healthy active male, free from injury and not involved in a resistance training program for at least 6 months before the study. The exclusion criteria include injury, illness, over 35 years old, and smoking individuals. Premeasurement of all subject characteristics is presented in [Table 1]. All participants were informed about the study, and a medical questionnaire and an informed consent written form have been obtained before participation from each subject. Informed consent assures that prospective subjects understood the nature of the study and can knowledgeably and voluntarily decide whether or not to participate. In addition, they have the right to withdraw from the study at any time and for any reason. The required sample size was determined a priori using G * Power (version 3.1.9, Universität Düsseldorf, Germany). Because of the lack of information available regarding the effects of NMES training on muscle functions, a previous study was used to calculate the sample size. Therefore, P values of 0.05 were used to denote statistical significance, and power (1-β) values of 0.80 were used to detect an effect size of f2 > 0.50. According to the calculation, the sample size was determined to be 12 for each group, assuming that NMES training will result in a 20% difference between PC and AC. To account for subject attrition, 24 university male students were recruited and subjected to PC or AC for 5 weeks. One subject has withdrawn in the middle of training and his data were excluded. The study-specific protocol was reviewed and approved by the research committee in the Research Center of the College of Sport Sciences and Physical Activity.
The homogeneity of variance between the groups was met using Levene's test with statistical significance set at P < 0.01.
Neuromuscular electrical stimulation training protocol
The subjects underwent NMES training 2 days a week for 5 weeks (10 sessions), with a 48-hr interval between sessions. During NMES training, the participants were set on a chair with a Biodex System 4 Pro dynamometer (Biodex Medical Systems Inc, Shirley, NY) with their knee joint angle set to 100° (0°= full extension) and trunk angle set to 110°. To minimize any possible movement of the hips and thighs during contractions, straps were used to secure the pelvis and chest. The participants were randomly assigned to counterbalanced NMES currents and were blinded to the type of NMES current used (AC or PC). The Intelect Advanced® Color Stim (Chattanooga Group, TN, USA) equipped with four channels was used to stimulate the quadriceps femoris muscles. For both legs, the skin surface was cleaned using alcohol pads, and then, four self-adhesive electrodes were placed on the anterior surface of each thigh as follows: two positive electrodes (50 mm × 50 mm) over the motor point of the vastus lateralis and vastus medialis muscles and two negative electrodes (50 mm × 100 mm) placed on the proximal portion of the quadriceps femoris muscle following the procedures stated in the study by Sartorio et al. A pen electrode (High-Volt Probe Kit, Chattanooga Group, TN, USA) with 1–Hz stimulation and ~ 10-mA intensity was carefully moved on the skin overlying the target muscle to find the best mechanical response to determine the location of motor points. The placements of the electrodes were kept similar between the NMES sessions. The same current was delivered to both legs simultaneously in this study to complete 60 isometric contractions by either PC or AC at 22% ±2% of the MVC, which was counterbalanced among subjects. The estimated time for each session is approximately 45 min (20 min for placing and removing electrodes, 5 min for determining the intended intensity, and 20 min for conducting NMES contractions).
In AC, the currents were adjusted at 2.5 kHz (pulse duration = 400 μs) and delivered in rectangular bursts with a carrier frequency of 75 Hz, and the duration of each burst was 6.5 ms.,, In PC, the currents were delivered in biphasic symmetrical rectangular and balanced stimulus pulses delivered at a frequency of 75 Hz, and the duration of each pulse was 400 μs.,
These protocols have been chosen and adjusted to provide the best possible identical NMES parameters for both PC and AC, which may help clearly demonstrate the effects of each current. Stimulation time (on–off ratio) was 5 s for the “on time” and 15 s for the “off time” (rest frequency: 0 Hz); therefore, the duty cycle time will be 25%. The ramping time was included in the “on time”; thus, 1 s for the “rise time,” 0 s for the “fall time.” and only 4 s for dosage stimulus intensity were allocated based on previous studies., Stimulation amplitude (intensity) was adjusted based on the maximal subject tolerance (MST), which was determined in the beginning of each session by applying a series (no more than six) of electrically stimulated contractions (2–4 s) with gradually increasing intensity from 30 mA until each subject can no longer tolerate. Once MST is determined, it was recorded and kept constant during each NMES session. This procedure was repeated for each NMES session.
A training diary includes the force produced during each contraction, pain during and after each NMES session, and subjective intensity of each NMES session was recorded and saved in confidant place.
The Biodex System 4 Pro dynamometer and Biodex Advantage software package (Biodex Medical Systems Inc, Shirley, NY) was used to measure isometric torque output before, during, and after NMES sessions. The dominant leg was used for strength assessment.
Vertical jump and power measurements
A cable-extension transducer (PT5 series, Celescon Inc., CA, USA) was fixed above the subjects to measure displacement. The subjects performed three bilateral and six unilateral (three for each leg) SJs and three bilateral and six unilateral (three for each leg) counter-movement jumps (CMJs) on a force plate (400 Series Force Plate, Fitness Technology, Inc., Adelaide, SA) with a 30-s rest between trials and a 3-min rest between the two jump tests. The SJ started from a static semi-squatting position with ~20 cm between feet and ~ 100 knee flexion, for 3 s.; participants were instructed to jump as high as possible without any preliminary movement. The CMJ started from a standing position. Participants were instructed to squat down until a 90 knee flexion angle and to extend the knee in 1 continuous movement. All jumps were performed by both legs (bilateral jump) followed by each leg (unilateral jump) in a random order. The subjects were instructed to keep both hands on their hips during the entire test. The highest jump height and peak power for the bilateral and unilateral SJs and CMJs among three tests were recorded. The Ballistic Measurement System (Fitness Technology, Inc., Adelaide, SA) was used to record the force and power characteristics.
Muscle mass measurements
Dual-energy X-ray absorptiometry (DEXA) (XR-36; Norland Products, South Brunswick Township, NJ, USA) was used to assess muscle mass. Scans were performed with the subjects in the supine position. The QDR-4500W Series software (Hologic®Osteoporosis Assessment, Inc. USA) was used to measure and determine lean mass and fat mass. Fat-free mass was calculated as the sum of lean mass and bone mineral mass. Muscle mass for both legs was estimated according to the equation developed by Shih et al. to estimate the mass of the lower limb skeletal muscle (SM):
MS = (0.692 × fat-free soft tissue)–(0.017 × age) + (0.068 × body mass index) +0.11 (Shih et al. 2000).
Data are presented as mean and standard deviation. Changes in the measurements before, during, and after NMES training were compared between the legs that underwent PC and AC NMES training using a two-way analysis of variance with repeated measures. If a significant effect is found, Tukey post hoc analysis was performed. Shapiro–Wilk test of normality has been ran for all dataset. P < 0.05 was used to denote statistical significance.
| Results|| |
The current was delivered to evoke around 22% of MVC, however no effect of training on the altitude of current to produce the torque for both NMES training modalities [Figure 1]. Though, less current is required to produce the targeted force during PC (Pre 54 ± 10, Post 66 ± 19) in comparison to AC (Pre 79 ± 21 and Post 72 ± 17).
|Figure 1: The difference between current (alternating current: failed bars and pulsed current: open bars) to evoke around 22% of maximal isometric voluntary contraction. A significant difference (*P < 0.05) is found between currents before and after training, but no training effect is determined|
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Over ten sessions of NMES training (AC and PC), results found that there is no significant torque gain was detected for both currents [Figure 2]. However, [Figure 3] illustrates significant fatigue after each NMES session without significant difference between currents (AC and PC).
|Figure 2: Changes in the maximal isometric voluntary contraction over 10 measurements (every session) for alternating current (a) and pulsed current (b). Pretraining measurements are denoted by open bars and posttraining measurements are denoted by filled bars. The horizontal lines above the bars with the * symbol show a significant difference (P < 0.05) between pre and post-training values|
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|Figure 3: The changes in the maximal isometric voluntary contraction (MVC) over 10 measurements (every session) for alternating current (denoted by filled bars) and pulsed current (denoted by open bars). The upper chart (a) shows pretraining values and the lower one (b) shows posttraining values|
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A significant increase has been detected in vertical jump height after both AC (pre: 50.12 ± 9.8 [95% confidence interval (CI): 43%–61%], post: 51.09 ± 8.4 cm [95% CI: 48–62]; d = −0.34) and PC (pre: 53.25 ± 8.8 [95% CI: 41–59], post: 53.82 ± 8.4 cm [95% CI: 46–60]; d = −0.33) NMES training, but no difference was observed between both NMES currents [Figure 4].
|Figure 4: A significant increase (*P < 0.05) in the vertical jump height is observed after NMES training (alternating current: failed bars; pulsed current: open bars), but no difference is found between currents|
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Interestingly, data from [Figure 5] show that DEXA revealed a significant increase in the legs lean mass (trained legs; P < 0.05) in both AC (pre: 17.75 ± 2.0 [95% CI: 16.3–19.1], post: 18.01 ± 2.4 kg [95% CI: 16.4–19.7]; d = −0.15) and PC (pre: 18.5 ± 2.6 [95% CI: 16.8–20.3], post: 18.9 ± 2.5 kg [95% CI: 17.2–20.6]; d = −0.016) NMES currents without a significant difference between currents [Figure 5]. Total body mass remained unchanged. Although there is no significant change in the fat mass of the trained legs between both currents, a significant reduction in fat percentage of the trained legs for AC (pre: 23.0 ± 7.6 [95% CI: 18.3%–27.2%], post: 22.1 ± 7.1 kg [95% CI: 17.6%–26.1%]) and PC (pre: 21.5 ± 6.1 [95% CI: 17.9%–24.9%], post: 21.2 ± 6.7 kg [95% CI: 17.4%–25.0%]) was observed after NMES training (P < 0.05) regardless of the current type used [Figure 6]. Further, Cohen's effect size value for AC (d = 0.097) and PC (d = 0.050) suggested a very low practical significance.
|Figure 5: An increase in lean mass (%) in both legs (#P = 0.05) is found after NMES training using alternating current (denoted by failed bars), but no changes are observed after NMES training using pulsed current (denoted by open bars)|
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|Figure 6: A significant decrease in tissue fat (%) in both legs (*P < 0.05) is found after NMES training (alternating current: failed bars and pulsed current: open bars), but no difference is perceived between currents|
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| Discussion|| |
The main purpose of the present study was to compare the effects of AC and PC NMES training on muscle function and muscle mass. The results of the present study demonstrated that short-term training 5 weeks (10 sessions) may not enough to occur significant difference between the NMES currents (AC and PC). Furthermore, no improvement in strength was shown at the end of the training term. However, vertical jump height was significantly higher after NMES training regardless of the current type used. Moreover, torque significantly decreased in the second session after NMES using both currents [Figure 4], which may be due to prolonged low-frequency force depression or what is commonly known a low-frequency fatigue (LFF). Althoug a recent study shows that AC is more fatigueable than PC, the current work shows contradictory results where greater MVC loss was observed after PC in comparison to PC. The difference finding can be due to the pulse duration of NMES, in de Paz et al. work, for example, they adjusted the pulse duration of PC to 2 ms, while AC to 0.4 ms. However, when both currents use the same pulse duration, they can produce similar torque output and discomfort.,
The delayed recovery from fatigue induced by NMES that leads to a decline in torque lasting days after the excise session can be attributed to LFF., The mechanism of this type of fatigue is not well understood yet. However, it has been suggested to be at the muscle fiber level. This model includes two mechanisms: muscle damage and an impairment in the excitation–contraction (EC) coupling. In this study, NMES evoked torque levels of 22% ± 2% MVC at a high-stimulation frequency (75 Hz) that can result in less calcium being available for muscle contraction. The reduction in Ca2+ release may cause slow strength recovery. Thus, the decreased strength in the following day can be described as LFF.
This study demonstrated that NMES training may independently improve explosive movements such as jumping. The results of this study showed significant improvements in vertical jump performance after NMES training using both currents (AC and PC). Although the effects of AC on improving vertical jump performance were relatively more significant than PC, the results showed no significant differences between both currents (AC vs. PC). Numerous studies have reported the effects of NMES such as PC in combination with resistance training on vertical jump performance.,,,,, Babault et al. have examined the effect of electromyostimulation (EMS) training (PC, 100 Hz) along with resistance training on the knee extensor, plantar flexor, and gluteus muscles in rugby players. Their methods of EMS training lasted for 12 weeks (three times per week in the first 6 weeks and once a week in the last 6 weeks). They have concluded that EMS training significantly improves SJ (11.8%) and DJ (7.6%) performance. However, no significant difference in SJ and DJ performance was observed between before and after 6 weeks of EMS training. Interestingly, the results of a recent study have revealed a significant improvement between pretraining and the 8-week follow-up for the NMES group. Moreover, Malatesta et al. have reported a significant vertical jump improvement after 10 days of EMS training. Even after a relatively short NMES training program alone can improve vertical jump significantly. Paillard et al. have examined the effect of two methods of NMES training (stimulation with an 80 Hz current for 15 min and with a 25 Hz current for 60 min), and both methods improved vertical jump significantly (5 m and 3 m, P < 0.004 and P < 0.009, respectively). One of the interpretations of the improvement in jump performance following a short NMES training program could be due to neural adaptations.
In terms of NMES current types, data from this study did not explore the differences between AC and PC in improving jump performance. These results are in line with previous conclusions that there is no significant difference between the NMES currents in term of strength improvement. Interestingly, this study seems to be one of the forefront studies that found significant improvement in vertical jump performance following NMES AC training alone without voluntary exercise. Although no significant difference in vertical jumP values was observed between AC and PC, the values for AC were higher than those for PC (before: 48.91 ± 8.3 and 51.09 ± 8.4, respectively; after: 53.20 ± 7.0 and 53.82 ± 8.4 cm, respectively). The differences between AC and PC could exist if the training programs are prolonged for a couple of weeks.
| Conclusion|| |
Regardless of the absence of significant differences between AC and PC in all measured variables, short-term training using NMES (AC and PC) may help to improve some muscle functions such as vertical jump. Furthermore, the NMES current type, NMES could improve body composition including fat free mass gain and decreasing body fat percentage.
This is a research project that was supported by a grant from the Research Center for the Sports Science and Physical Activity, deanship of scientific research at King Saud University.
Financial support and sponsorship
This work was supported by the Research Center for the Sports Science and Physical Activity, deanship of scientific research at King Saud University, Riyadh, Saudi Arabia.
Conflicts of interest
There are no conflicts of interest.
| References|| |
Bax L, Staes F, Verhagen A. Does neuromuscular electrical stimulation strengthen the quadriceps femoris? A systematic review of randomised controlled trials. Sports Med 2005;35:191-212.
Iwasaki T, Shiba N, Matsuse H, Nago T, Umezu Y, Tagawa Y, et al.
Improvement in knee extension strength through training by means of combined electrical stimulation and voluntary muscle contraction. Tohoku J Exp Med 2006;209:33-40.
Parker MG, Bennett MJ, Hieb MA, Hollar AC, Roe AA. Strength response in human femoris muscle during 2 neuromuscular electrical stimulation programs. J Orthop Sports Phys Ther 2003;33:719-26.
Herrero JA, Izquierdo M, Maffiuletti NA, García-López J. Electromyostimulation and plyometric training effects on jumping and sprint time. Int J Sports Med 2006;27:533-9.
Maffiuletti NA, Zory R, Miotti D, Pellegrino MA, Jubeau M, Bottinelli R. Neuromuscular adaptations to electrostimulation resistance training. Am J Phys Med Rehabil 2006;85:167-75.
Malatesta D, Cattaneo F, Dugnani S, Maffiuletti NA. Effects of electromyostimulation training and volleyball practice on jumping ability. J Strength Cond Res 2003;17:573-9.
Chandrasekaran S, Davis J, Bersch I, Goldberg G, Gorgey AS. Electrical stimulation and denervated muscles after spinal cord injury. Neural Regen Res 2020;15:1397-407.
] [Full text]
Banerjee P, Caulfield B, Crowe L, Clark A. Prolonged electrical muscle stimulation exercise improves strength and aerobic capacity in healthy sedentary adults. J Appl Physiol (1985) 2005;99:2307-11.
Paillard T. Combined application of neuromuscular electrical stimulation and voluntary muscular contractions. Sports Med 2008;38:161-77.
McLoda TA, Carmack JA. Optimal burst duration during a facilitated quadriceps femoris contraction. J Athl Train 2000;35:145-50.
Bennie SD, Petrofsky JS, Nisperos J, Tsurudome M, Laymon M. Toward the optimal waveform for electrical stimulation of human muscle. (Vers une forme d ' onde optimale pour la stimulation electrique des muscles humains.). Eur J Appl Physiol 2002;88:13-197.
Ward AR, Robertson VJ, Makowski RJ. Optimal frequencies for electric stimulation using medium-frequency alternating current. Arch Phys Med Rehabil 2002;83:1024-7.
Kubiak RJ, Whitman KM, Johnston RM. Changes in quadriceps femoris muscle strength using isometric exercise versus electrical stimulation. J Orthop Sports Phys Ther 1987;8:537-41.
Selkowitz DM. Improvement in isometric strength of the quadriceps femoris muscle after training with electrical stimulation. Phys Ther 1985;65:186-96.
Baldwin ER, Klakowicz PM, Collins DF. Wide-pulse-width, high-frequency neuromuscular stimulation: Implications for functional electrical stimulation. J Appl Physiol (1985) 2006;101:228-40.
Talbot LA, Gaines JM, Ling SM, Metter EJ. A home-based protocol of electrical muscle stimulation for quadriceps muscle strength in older adults with osteoarthritis of the knee. J Rheumatol 2003;30:1571-8.
Laufer Y, Elboim M. Effect of burst frequency and duration of kilohertz-frequency alternating currents and of low-frequency pulsed currents on strength of contraction, muscle fatigue, and perceived discomfort. Phys Ther 2008;88:1167-76.
Ward AR. Electrical stimulation using kilohertz-frequency alternating current. Phys Ther 2009;89:181-90.
Medeiros FV, Bottaro M, Vieira A, Lucas TP, Modesto KA, Bo AP, et al.
Kilohertz and low-frequency electrical stimulation with the same pulse duration have similar efficiency for inducing isometric knee extension torque and discomfort. Am J Phys Med Rehabil 2017;96:388-94.
Stefanovska A, Vodovnik L. Change in muscle force following electrical stimulation. Dependence on stimulation waveform and frequency. Scand J Rehabil Med 1985;17:141-6.
Bircan C, Senocak O, Peker O, Kaya A, Tamci SA, Gulbahar S, et al.
Efficacy of two forms of electrical stimulation in increasing quadriceps strength: A randomized controlled trial. Clin Rehabil 2002;16:194-9.
Snyder-Mackler L, Garrett M, Roberts M. A comparison of torque generating capabilities of three different electrical stimulating currents. J Orthop Sports Phys Ther 1989;10:297-301.
Laufer Y, Ries JD, Leininger PM, Alon G. Quadriceps femoris muscle torques and fatigue generated by neuromuscular electrical stimulation with three different waveforms. Phys Ther 2001;81:1307-16.
Lyons CL, Robb JB, Irrgang JJ, Fitzgerald GK. Differences in quadriceps femoris muscle torque when using a clinical electrical stimulator versus a portable electrical stimulator. Phys Ther 2005;85:44-51.
Maffiuletti NA, Dugnani S, Folz M, Di Pierno E, Mauro F. Effect of combined electrostimulation and plyometric training on vertical jump height. Med Sci Sports Exerc 2002;34:1638-44.
Maffiuletti NA, Cometti G, Amiridis IG, Martin A, Pousson M, Chatard JC. The effects of electromyostimulation training and basketball practice on muscle strength and jumping ability. Int J Sports Med 2000;21:437-43.
Brocherie F, Babault N, Cometti G, Maffiuletti N, Chatard JC. Electrostimulation training effects on the physical performance of ice hockey players. Med Sci Sports Exerc 2005;37:455-60.
Babault N, Cometti G, Bernardin M, Pousson M, Chatard JC. Effects of electromyostimulation training on muscle strength and power of elite rugby players. J Strength Cond Res 2007;21:431-7.
Maffiuletti NA, Green DA, Vaz MA, Dirks ML. Neuromuscular electrical stimulation as a potential countermeasure for skeletal muscle atrophy and weakness during human spaceflight. Front Physiol 2019;10:1031.
Salmons S, Ashley Z, Sutherland H, Russold MF, Li F, Jarvis JC. Functional electrical stimulation of denervated muscles: Basic issues. Artif Organs 2005;29:199-202.
Carvalho de Abreu DC, Júnior AC, Rondina JM, Cendes F. Muscle hypertrophy in quadriplegics with combined electrical stimulation and body weight support training. Int J Rehabil Res 2008;31:171-5.
Turostowski J, Cometti G, Cordano M. Influence of electrostimulation on human quadriceps femoris muscle strength and muscle mass. In: 10th International Symposium on Biomechanics in Sports Proceedings. Milan - Italy: ISBS; 1992.
Martin L, Cometti G, Pousson M, Morlon B. The influence of electrostimulation on mechanical and morphological characteristics of the triceps surae. J Sports Sci 1994;12:377-81.
Matsuse H, Shiba N, Umezu Y, Nago T, Tagawa Y, Kakuma T, et al.
Muscle training by means of combined electrical stimulation and volitional contraction. Aviat Space Environ Med 2006;77:581-5.
Hortobágyi T, Maffiuletti NA. Neural adaptations to electrical stimulation strength training. Eur J Appl Physiol 2011;111:2439-49.
Sartorio A, Jubeau M, Agosti F, De Col A, Marazzi N, Lafortuna CL, et al.
GH responses to two consecutive bouts of neuromuscular electrical stimulation in healthy adults. Eur J Endocrinol 2008;158:311-6.
Ward AR, Shkuratova N. Russian electrical stimulation: The early experiments. Phys Ther 2002;82:1019-30.
Rooney JG, Currier DP, Nitz AJ. Effect of variation in the burst and carrier frequency modes of neuromuscular electrical stimulation on pain perception of healthy subjects. Phys Ther 1992;72:800-6.
Theurel J, Lepers R, Pardon L, Maffiuletti NA. Differences in cardiorespiratory and neuromuscular responses between voluntary and stimulated contractions of the quadriceps femoris muscle. Respir Physiol Neurobiol 2007;157:341-7.
Jubeau M, Sartorio A, Marinone PG, Agosti F, Van Hoecke J, Nosaka K, et al.
Comparison between voluntary and stimulated contractions of the quadriceps femoris for growth hormone response and muscle damage. J Appl Physiol (1985) 2008;104:75-81.
Shih R, Wang Z, Heo M, Wang W, Heymsfield SB. Lower limb skeletal muscle mass: Development of dual-energy X-ray absorptiometry prediction model. J Appl Physiol (1985) 2000;89:1380-6.
Allen DG, Lamb GD, Westerblad H. Skeletal muscle fatigue: Cellular mechanisms. Physiol Rev 2008;88:287-332.
Paz IA, Rigo GT, Sgarioni A, Baroni BM, Frasson VB, Vaz MA. Alternating current is more fatigable than pulsed current in people who are healthy: A double-blind, randomized crossover trial. Phys Ther 2021;101:pzab056.
Pinto Damo NL, Modesto KA, Neto IV, Bottaro M, Babault N, Durigan JL. Effects of different electrical stimulation currents and phase durations on submaximal and maximum torque, efficiency, and discomfort: A randomized crossover trial. Braz J Phys Ther 2021:S1413-1.
Dundon JM, Cirillo J, Semmler JG. Low-frequency fatigue and neuromuscular performance after exercise-induced damage to elbow flexor muscles. J Appl Physiol (1985) 2008;105:1146-55.
Keeton RB, Binder-Macleod SA. Low-frequency fatigue. Phys Ther 2006;86:1146-50.
Venable MP, Venable MP, Collins MA, O'Bryant HS, Denegar CR, Sedivec MJ, et al.
Effect of supplemental electrical stimulation on the development of strength, vertical jump performance and power. J Appl Sport Sci Res 1991;5:139-43.
da Cunha RA, Pinfildi CE, de Castro Pochini A, Cohen M. Photobiomodulation therapy and NMES improve muscle strength and jumping performance in young volleyball athletes: A randomized controlled trial study in Brazil. Lasers Med Sci 2020;35:621-31.
Paillard T, Noe F, Bernard N, Dupui P, Hazard C. Effects of two types of neuromuscular electrical stimulation training on vertical jump performance. J Strength Cond Res 2008;22:1273-8.
Vaz MA, Frasson VB. Low-frequency pulsed current versus kilohertz-frequency alternating current: A scoping literature review. Arch Phys Med Rehabil 2018;99:792-805.
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]