Secondary Logo

Journal Logo

Original Research

Neuromuscular Electrical Stimulation Can Elicit Aerobic Exercise Response Without Undue Discomfort in Healthy Physically Active Adults

Crognale, Domenico1,2; Vito, Giuseppe De1,2; Grosset, Jean-Francois1; Crowe, Louis1; Minogue, Conor3; Caulfield, Brian1,2

Author Information
Journal of Strength and Conditioning Research: January 2013 - Volume 27 - Issue 1 - p 208-215
doi: 10.1519/JSC.0b013e318252f5e5
  • Free

Abstract

Introduction

It is often necessary in training and rehabilitation to seek alternative aerobic exercise modalities for those unable to exercise voluntarily or to protect healing tissue after injury. One modality that has received attention in this regard in recent years is neuromuscular electrical stimulation (NMES).

Attempts to elicit a sustained aerobic exercise response using standard tetanic NMES in the 30–70 Hz frequency range to elicit sustained tetanic contractions in leg muscles have not been successful, yielding physiological responses of less than 2 metabolic equivalents (METs) (6). However, more recent studies have indicated that application of an NMES protocol using complex pulse patterns delivered at low stimulating frequencies designed to elicit subtetanic isometric muscle contractions in the large lower extremity muscle groups can result in clinically significant increases in O2 uptake (2,3,6). It does this by eliciting repeating rhythmical muscle contractions that mimics the pattern of muscle activation that occurs during shivering. Repeated application of this subtetanic NMES protocol in sedentary adults with low baseline fitness and in patients with heart failure resulted in an aerobic training response, with increases in peak V[Combining Dot Above]O2 of approximately 10% over a 6-week training period (3) (4). This suggests that subtetanic NMES protocols have the potential as an alternative means of aerobic exercise training. However, these results were achieved in populations with low baseline aerobic capacity. Average peak V[Combining Dot Above]O2 values were 31.5 ml·minute−1·kg−1 and 19.3 ml·minute−1·kg−1 in the sedentary adult and heart failure studies, respectively. It is not clear if the elicited exercise stimulus in these studies would have been sufficient to induce an aerobic training response in a more physically active and younger adult population where the exercise stimulus would have to be higher.

Another limitation in the technique adopted in these studies was the discomfort associated with the electrical stimulation. Banerjee et al. (2) observed moderate to severe discomfort in their study population and proposed that comfort levels would have to be improved to make the technique acceptable to a wider population and achieve a greater aerobic response. This is an issue frequently highlighted in NMES reports (8,11,15). Therefore, taking these above considerations on board, some substantial modifications were applied to the NMES protocol previously employed by Banerjee et al. In particular, sizes of the stimulating electrodes have been increased by 33% to reduce current density. In addition, pulse patterns have been modified to elicit rhythmical contractions at 5 Hz rather than 4 Hz because initial subjective evaluation suggested that this was better tolerated by healthy adult volunteers. It is now necessary to evaluate the impact of these improvements to determine whether this technique might be an effective and comfortable exercise modality. This modified low-frequency subtetanic NMES protocol has been evaluated with respect to its suitability as an alternative exercise modality in a healthy, physically active, adult population in the present investigation by means of quantifying physiological and subjective responses at incremental stimulating intensities before and after a period of habituation to the protocol.

The main purpose of this study was to test our hypothesis that this modified subtetanic NMES protocol could produce effective and sustainable levels of aerobic exercise, without provoking undue discomfort in a healthy and moderately active adult population. The rationale was that an effective protocol could produce a physiological response that was consistent with standard American College of Sports Medicine aerobic exercise guidelines (16) yet would not be associated with a poor subjective response. As such, we evaluated the response to stimulation using a series of physiological and subjective dependent variables, and the target aerobic exercise intensity level to be achieved during stimulation was set at 50% of maximal oxygen uptake and heart rate (HR). Further aims of the study were to establish the relationship between rate of perceived exertion (RPE) and physiological response, the effect that habituation to stimulation had on tolerance and physiological response, to evaluate the consistency of physiological responses at successive stimulation sessions, and to compare physiological and subjective responses between genders.

Methods

Experimental Approach to the Problem

In this study, RPE, subjective discomfort levels, blood lactate (BLa) concentration, HR, and relative energy cost (V[Combining Dot Above]O2) at incremental NMES stimulation intensities were measured in physically active healthy subjects at successive stimulation sessions before and after a period of habituation to NMES (9 self-directed NMES sessions).

Subjects

Sixteen healthy adult volunteers participated in this study. The institutional ethics committee approved the study, and written informed consent was obtained in all cases. The 16 participants (8 men and 8 women) had a mean age of (mean ± SD) 27.3 ± 6.3 years and an average body mass and body mass index of 73.3 ± 13.4 kg and 25.1 ± 3.0 kg·m−2, respectively. All subjects were free from illness or injury and physically active at the time of participation in the study. Participants were involved in recreational sporting activities including jogging, cross-country running, and cycling. The study was conducted during the summer period (April-July), and there was no observed change in activity patterns for any of the study participants during their involvement in the study. The study was conducted on participants who had not previously been exposed to NMES before taking part in this investigation.

Procedures

All laboratory testing sessions were carried out in the morning approximately 2 hours after the ingestion of a breakfast meal that was consistent for each participant from session to session. Each participant first underwent a maximal effort incremental cycle ergometer test protocol with simultaneous gas exchange analysis to identify their baseline maximal aerobic capacity and HR for the purposes of calculating relative exercise intensities achieved during subsequent NMES sessions. Subjects wore a facemask linked to an open circuit gas analysis system (Quark b2; Cosmed, Rome, Italy), which enabled measurement of the expired oxygen and carbon dioxide concentrations and volumes. Heart rate was also recorded throughout the test using a chest strap (Polar, Kempele, Finland). The exercise protocol consisted of a 1-minute incremental test based on Wasserman's equation (21).

The test was conducted to exhaustion or until at least 2 out of the following 3 endpoint criteria were reached: a leveling of V[Combining Dot Above]O2 uptake despite increasing exercise work load, actual HR within ±10 beats from the predicted HRmax (220 − age in years), respiratory exchange ratio higher than 1.15. In practice, all participants terminated the test upon exhaustion. Maximal V[Combining Dot Above]O2 and HR were calculated from the average V[Combining Dot Above]O2 and HR measurements during the last 30 seconds of the cycle test.

Each participant then performed a total of 12 NMES sessions, each of 1-hour duration, scheduled approximately 3 times per week over a 4-week period (Table 1). All sessions were performed in a half lying position. The first NMES session was used to familiarize participants with the NMES protocol and to establish their initial comfortable stimulation threshold. During this session, they were encouraged to modulate the stimulation intensity upward or downward on their own volition to establish their initial comfortable tolerance level. In judging this level, participants were asked to achieve “a reasonable compromise between NMES intensity, perceived exertion, and perceived discomfort.” In session 2, they performed a 10-stage incremental NMES protocol during which the stimulation intensity was turned up every 5 minutes in equal increments from a starting point of 40 mA to reach their initial comfortable tolerance level as identified during session 1. This incremental protocol was preceded and followed by 5 minutes of rest. Sessions 3 to 11 consisted of 9 self-directed NMES habituation sessions, each of 60-minute duration. During each of these habituation sessions, participants turned the intensity up gradually over the first 15 minutes to reach a steady-state stimulation intensity for the following 40 minutes, with a final 5 minutes of cooldown during which the stimulation intensity was gradually turned down again. They were instructed to seek a steady-state intensity that achieved a balance between perceived exertion and subjective discomfort because of the stimulation and were instructed not to exceed their own personal discomfort threshold. The final personal comfortable tolerance level was identified from the training intensity selected during the 11th session. The 12th session comprised a repeat of the first incremental protocol, the only difference being the use of a new comfortable tolerance level for calculation of the increments (as identified during the 11th session).

T1-29
Table 1:
Study outline.

Physiological measurements, including V[Combining Dot Above]O2 and HR, were recorded at rest and throughout the incremental protocols in sessions 2 and 12 using open-circuit spirometry, as described above. Average values over the last 30 seconds of each stage were calculated and used for subsequent analysis. During the last 30 seconds of each stage, subjects were also required to rate their perceived exertion and level of discomfort. Those variables were assessed using the RPE Borg's scale and the Category Partitioning (CP-50) scale, respectively. The CP-50 scale categorizes discomfort into 5 separate 10-point subscales, ranging from no discomfort to very high discomfort (18). Scores of less than 30 or 50 indicate low or medium discomfort. The Borg RPE Scale (5) also has BLa measured with Lactate Pro test analyzer (Arkray, Kyoto, Japan) from fingertip 15 seconds before the end of each NMES stage.

Stimulation Protocol

A specially designed hand held muscle stimulator (NT2010; BioMedical Research Ltd, Galway, Ireland) was used to produce rapid rhythmical contractions in the large lower extremity muscle groups. These contractions were achieved by means of a burst of 4 pulses delivered at a frequency of 5 Hz. The stimulator provided a symmetric biphasic current controlled pulse with a peak amplitude up to 200 mA with a phase duration of 760 microseconds. Impulses were delivered through an array of 4 adhesive electrodes on each leg (area per leg = 800 cm2), with a different combination of electrodes from the array being involved in delivery of each of the 4 pulses in a burst. The current pathways, electrode combinations per pulse, and pulse train characteristics are outlined in Figure 1. The electrode arrays were applied to the lower limb muscles via a neoprene “wrap” garment that was secured to the thigh with Velcro straps.

F1-29
Figure 1:
Location of Stimulating Electrodes, pulse pathways (color coded), and pulse intervals. Main lower limb target muscles were: RUQ (right upper quadriceps), RLQ (right lower quadriceps), RUH (right upper hamstring), RLH (right lower hamstring), LUQ (left upper quadriceps), LLQ (left lower quadriceps), LUH (left upper hamstring), LLH (left lower hamstring). Burst of 4 pulses were delivered at a frequency of 5 Hz.

Statistical Analysis

Values for oxygen uptake (V[Combining Dot Above]O2) (ml·minute−1·kg−1), HR (b·min−1), BLa (mmol/L), stimulation intensity (mA), discomfort (CP-50 rating), and RPE obtained during each stage of both incremental NMES sessions were the dependent variables used as the basis for all data analyses. Previous research has demonstrated strong reliability for all the physiological and subjective report variables used in this investigation. De Mendonça and Pereira (7) have demonstrated intraclass correlation (ICC) values of 0.89–0.94 and 0.93–0.96 for the measurement of V[Combining Dot Above]O2 and HR on different days at different walking loads, respectively, indicating strong measurement reliability for these variables during exercise. Pyne et al. (17) has demonstrated excellent reliability for the lactate pro analyzer for repeat measurement of BLa concentrations during exercise (Pearson's R = 0.99). Regarding the subjective ratings, Shen and Parsons (18) and Skinner et al. (19) have reported ICCs of 0.93 and 0.90 for repeat measurements on the CP-50 and RPE scales, respectively. All results are described as mean ± SD. Peak V[Combining Dot Above]O2 and HR values obtained during the incremental tests, expressed as a percentage of maximum values obtained during maximal effort incremental cycle test, were used to evaluate the relative exercise intensity achieved during the NMES protocol during the first and second incremental exercise sessions. The effect of habituation to NMES was assessed by comparing peak values for all measured variables during incremental sessions 1 and 2. Paired Student's t-tests were used to test for differences between peak responses observed on both occasions. Average male and female group peak values for all measured variables during the second incremental NMES session were used as the basis for gender comparisons, with independent t-tests being used to test for differences between group means. Post hoc power (at an alpha level of 0.05) was calculated using the observed effect sizes.

The relationship between RPE and physiological responses was evaluated by performing a correlation analysis on average values for RPE, V[Combining Dot Above]O2, and HR during each of the stages of the incremental NMES sessions to derive Pearson's correlation coefficients. To evaluate repeatability of the effect of stimulation at given intensities on different days, separate paired t-tests were performed to compare subjective (CP-50, RPE) and physiological (HR, V[Combining Dot Above]O2, and BLa) responses at different current intensity levels (40, 60, 80, and 100 mA). Because of the fact that participants reached their comfortable threshold at different levels of stimulation intensity during the first session, we had different numbers of complete datasets for this analysis (n = 16 @ 40 mA, n = 14 @ 60 mA, n = 13 @ 80 mA, n = 8 @ 100 mA). A Bonferroni correction was applied for each comparison in this analysis because of the large number of separate comparisons (4 for each variable). The adjusted critical p value at 95% confidence level was 0.0125. All statistical analyses were conducted using Statistica 9 software (Statsoft Italia, Vigonza, Italy). The probability level accepted for statistical significance was p ≤ 0.05.

Results

All stimulation sessions and tests were completed by study participants without any difficulty. Group mean V[Combining Dot Above]O2max and HRmax during the baseline incremental cycle test were 36.0 ± 5.2 ml·minute−1·kg−1 and 190.8 ± 8.6 b.min−1, respectively. Group mean values for peak V[Combining Dot Above]O2 and HR obtained during the incremental stimulation sessions were expressed as a percentage of these maximal values to derive relative exercise intensities. Peak V[Combining Dot Above]O2 values were at 40 ± 12% and 53 ± 12% of maximum during the first and second incremental sessions, respectively. Corresponding values for peak HR were 60 ± 11% and 70 ± 12 %, respectively (Table 2).

T2-29
Table 2:
Comparison of group mean values for peak stimulation intensities and physiological responses, and associated subjective ratings of discomfort and RPE during first and second incremental NMES sessions (values are group mean ± SD).

Group mean values for peak NMES intensities and physiological and subjective responses observed during the first and second incremental NMES sessions are presented in Table 2. Significantly higher peak stimulation intensities were observed at the second incremental session compared with the first (p < 0.01; ES = 0.97). This was associated with significantly higher peak V[Combining Dot Above]O2 and HR during the second incremental session (p < 0.01; ES = 0.94 [V[Combining Dot Above]O2], 0.97 [HR]). Peak BLa values obtained during the second incremental session were also higher than those observed in the first; however, the difference was not statistically significant (p > 0.05; ES = 0.48). There were no changes in peak values for subjective discomfort or RPE observed at both incremental NMES sessions (p > 0.05; ES = 0.02 [CP-50], 0.28 [RPE]). Comparison of peak stimulation intensities and physiological and subjective responses observed in men and women indicated that men had higher peak responses for all measured variables (Table 3). However, differences between groups did not reach statistical significance in the case of peak HR observed during NMES or in associated subjective discomfort or RPE ratings (p > 0.05).

T3-29
Table 3:
Comparison of group mean values for peak stimulation intensities and physiological responses, and associated subjective ratings of discomfort and RPE, in male and female participants (values are mean ± SD).

A correlation analysis performed on average RPEs reported during each of the stages of the incremental NMES sessions and associated V[Combining Dot Above]O2 and HR responses revealed very strong relationships between perceived exertion and physiological response. Pearson's correlation coefficients for the relationship between RPE and V[Combining Dot Above]O2 response, and V[Combining Dot Above]O2 and HR response were 0.99 and 0.97, respectively.

Physiological (HR, V[Combining Dot Above]O2, BLa) and subjective (RPE, CP-50) responses at equivalent stimulation intensities (40, 60, 80, and 100 mA) during the first and second incremental sessions are illustrated in Figure 2. Paired t-test results demonstrated that there were no differences in physiological or subjective responses observed at the same stimulation intensity on different days across this range of stimulation intensities (p > 0.05).

F2-29
Figure 2:
Physiological (HR, BLa, V[Combining Dot Above]O2) and subjective (CP-50, RPE) responses at equivalent stimulation intensities (40, 60, 80 and 100 mA) for the 2 incremental NMES sessions (n=16 @40mA, [email protected], [email protected], [email protected]). Values are mean ± SD. No differences in physiological or subjective responses were observed (p > 0.05).

Discussion

The main finding of the present study was that this novel modality of NMES applied at subtetanic frequencies resulted in an effective aerobic exercise level, which could be readily tolerated by subjects for exercise sessions lasting 1 hour. Furthermore, higher stimulating intensities and associated physiological responses, at the same subjective discomfort levels, were observed during the second incremental session, indicating a positive habituation effect. We also observed a very high correlation between RPE and physiological response, suggesting that RPE is an effective barometer of exercise intensity during this form of NMES-induced aerobic exercise. Finally, we observed a consistent physiological response during the first and second incremental NMES session at equivalent stimulating intensities, indicating the presence of a reliable dose-response effect between sessions. This is the first study on subtetanic NMES designed to induce an aerobic exercise effect that has performed simultaneous measurement of physiological responses and subjective ratings of perceived discomfort and exertion at a range of stimulation intensities.

The primary rationale for conducting the study was to determine whether we could achieve an exercise intensity of 50% of V[Combining Dot Above]O2max without undue discomfort using subtetanic NMES. Neuromuscular electrical stimulation–induced exercise intensities observed were in line with the range of therapeutic exercise intensities recommended by the American College of Sports Medicine (16). The average V[Combining Dot Above]O2 response at peak comfortable stimulation intensity was only 40% of the participants' V[Combining Dot Above]O2max during the first stimulation session. This level of exercise intensity would not be expected to stimulate an aerobic training response in this healthy adult population. However, after a period of habituation to NMES, peak V[Combining Dot Above]O2 observed during stimulation had improved significantly to reach an average conditioning intensity of 53% of the participants' V[Combining Dot Above]O2max. Therefore, the NMES technique could be considered to be effective in achieving the goal of 50% of V[Combining Dot Above]O2max. However, the fact that it only reached this level after a period of habituation outlines the importance of allowing a period of habituation to NMES if it is to be effective.

The aerobic exercise intensities observed in this study are much higher than the results obtained in previous studies that measured the physiological effects of NMES-induced tetanic muscle contractions, where peak energy cost values of approximately 2 METs were observed (9,10,20). In contrast, we observed peak energy costs equivalent to 3.4 ± 0.9 METs and 4.6 ± 1.1 METs before and after a habituation period, respectively. The findings of the present study support previous work that has suggested that a subtetanic NMES protocol, as opposed to one that involves tetanic muscle contractions, is required to elicit an aerobic exercise response (1,2). In fact, the exercise intensities observed in this study represent a further improvement on those reported by Banerjee et al. (2), most likely as a result of the modifications made to stimulation parameters.

In our study, RPE was rated as “hard” (14.4 ± 2.1 on Borg's Scale) and the average peak discomfort associated with the highest levels of NMES was reported to be “medium” (25.5 ± 13.3 on CP-50 Scale). It is interesting to note that the range of subjective responses is quite small for RPE yet large for CP-50 ratings, as evidenced by the relatively high SD. This large range of responses in peak CP-50 ratings reflects the subjective nature of perception of discomfort associated with electrical stimulation (6) and suggests that this form of subtetanic NMES may be not suitable for all potential users. A score of 30 on the CP-50 scale is considered to be the point of transition between a category rating of “medium” and “high” discomfort (16). Of the 16 study participants, 7 scored greater than 30 at peak stimulation intensity, with an average score of 38 within this subgroup. However, each of these 7 participants rated the level of discomfort as acceptable, within the context of the exercise intensity achieved, on follow-up questioning. The average rating for the remaining 9 participants was only 16, falling in the “low discomfort” category. Apart from the subjective rating of discomfort, there was no clear difference between these subgroups, in terms of RPE, physiological response, or body mass index. Further work is required to understand the physical and psychological factors that affect subjective responses to this form of NMES to make recommendations as to which target group it is most suitable for.

We observed a significant increase in peak stimulation intensity at the second incremental NMES session compared with the first one. In fact, all participants exhibited an increase in stimulation intensity from the first to second session. However, there were no significant changes in peak CP-50 ratings. This indicates a habituation effect, with greater stimulation intensities achieved at equivalent discomfort levels. This was associated with a consequent increase in physiological responses achieved at equivalent discomfort levels. The habituation effect observed in this study resulted from participants completing 9 habituation sessions of 1 hour each. It is reasonable to suggest that further exposure could result in a greater habituation effect.

Significantly higher values for peak V[Combining Dot Above]O2, BLa, and current intensity were observed in male participants compared with their female counterparts. Current intensities results are in agreement with Maffiuletti et al. (13) who demonstrated that women have a lower sensory threshold than men in relation to exposure to NMES. This threshold indicates the initial perception of stimulus sensation, so a higher level allows men to reach superior stimulation intensities and associated physiological responses. Furthermore, men generally have more lean mass and less fat mass than women (12) so can be electrically stimulated more easily (14). This suggests that NMES-induced aerobic exercise may be more suitable for men than for women. However, it is interesting to note that the habituation effect observed in this study was equally strong in women.

We observed consistent physiological responses when we compared variables at equivalent intensities on separate days. This indicates consistency and reliability of the exercise intensity elicited by a given electrical stimulus and is in agreement with Banerjee et al. (2) who observed a consistent dose-response relationship during NMES-induced aerobic exercise at lower exercise intensities than those observed in the present investigation. There was also a very high correlation between RPE reported by our participants and physiological response during the incremental NMES sessions. The combination of consistency of physiological dose-response relationship and correlation between physiological response and RPE suggests that NMES-induced aerobic exercise could be safely deployed in the field in the absence of extensive monitoring technologies. However, further studies on larger numbers of participants are required before definitive conclusions can be made in this regard.

As our goal in this study was to assess acute effects of stimulation and the impact of habituation, we only asked participants to complete a relatively small number of sessions over a relatively short time frame. Although it is possible, we would not have expected aerobic fitness to improve as a result of completing such a small number of sessions. We would expect that a moderately fit population, such as ours, would need a greater total exposure to exercise at the conditioning intensities observed here. In retrospect, the study could have been improved by asking the participants to complete a larger number of sessions and repeating the incremental cycle test to measure the impact on aerobic fitness. This is something we plan to address in a separate study.

This study has shown that the NMES can be used by physically active adults within their comfortable stimulation threshold to elicit an aerobic exercise response in the range of intensities recommended for aerobic training. All study participants demonstrated a habituation effect, indicating that tolerability improves with repeated exposure, resulting in enhanced exercise intensities being achieved at equivalent comfort levels. This technique could have a role to play in situations where an alternative to traditional modalities of aerobic exercise is warranted. Future investigations could explore the optimal balance between electrode array configurations, pulse patterns, and exposure patterns required to further enhance the tolerability of stimulation and investigating the impact of prolonged exposure on aerobic fitness.

Practical Applications

The results presented in this article suggest that subtetanic NMES can be used effectively as an alternative aerobic exercise modality. The results do not demonstrate that the NMES technique described here is preferable or more effective than traditional aerobic exercise modalities, such as walking/running or cycling. However, it could be considered as a viable alternative to more traditional forms of aerobic exercise in situations where a person may not be able to engage in these forms of exercise. It may be particularly well suited to cases where an athlete or patient cannot bear weight on their lower limbs because of a musculoskeletal or neurological injury, once due consideration is given to the integrity of the injury itself. For example, an athlete returning from an ankle injury should be able to use this technique to perform aerobic exercise without delaying the healing process when walking or running might not be easily achieved. It could also be applied in people with arthritis where limb loading needs to be controlled as much as possible to limit inflammatory reactions. Repeated exposure results in an accommodation process, thus minimizing the comfort barriers normally associated with the application of electrical currents to the body. This does mean that users of the technique may require an accommodation period before they can use it at effective intensities.

Acknowledgments

This research was supported by Biomedical Research Ltd and Enterprise Ireland under the Innovation Partnership program.

References

1. Atherton P, Babraj J, Smith K, Singh J, Rennie M, Wackerhage H. Selective activation of AMPK-PGC-1 or PKB-TSC2-mTOR signaling can explain specific adaptive responses to endurance or resistance training-like electrical muscle stimulation. FASEB J. 2005;19: 786–788.
2. Banerjee P, Clark A, Witte K, Crowe L, Caulfield B. Electrical stimulation of unloaded muscles causes cardiovascular exercise by increasing oxygen demand. Eur J Cardiovasc Prev Rehabil. 2005;12: 503–508.
3. 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. 2005;99: 2307–2311.
4. Banerjee P, Caulfield B, Crowe L, Clark AL. Prolonged electrical muscle stimulation exercise improves strength, peak VO2, and exercise capacity in patients with stable chronic heart failure. J Card Fail 15: 319–326, 2009.
5. Borg G. Borg's Perceived Exertion and Pain Scales. Human Kinetics Publishers, 1998.
6. Caulfield B, Crowe L, Minogue C, Banerjee P, Clark A. The use of electrical muscle stimulation to elicit a cardiovascular exercise response without joint loading: a case study. J Exerc Physiol Online. 2004;7: 84–88.
7. de Mendonça G, Pereira F. Between-day variability of net and gross oxygen uptake during graded treadmill walking: effects of different walking intensities on the reliability of locomotion economy. Appl Physiol Nutr Metab. 2008;33: 1199–1206.
8. Delitto A, Strube MJ, Shulman AD, Minor SD. A study of discomfort with electrical stimulation. Phys Ther. 1992;72:410–421; discussion 421–414.
9. Hamada T, Hayashi T, Kimura T, Nakao K, Moritani T. Electrical stimulation of human lower extremities enhances energy consumption, carbohydrate oxidation, and whole body glucose uptake. J Appl Physiol. 2004;96: 911.
10. Hamada T, Sasaki H, Hayashi T, Moritani T, Nakao K. Enhancement of whole body glucose uptake during and after human skeletal muscle low-frequency electrical stimulation. J Appl Physiol. 2003;94: 2107.
11. Han TR, Shin HI, Kim IS. Magnetic stimulation of the quadriceps femoris muscle: comparison of pain with electrical stimulation. Am J Phys Med Rehabil. 2006;85: 593–599.
12. Jung Lee S, Janssen I, Heymsfield S, Ross R. Relation between whole-body and regional measures of human skeletal muscle. Am J Clin Nutr. 2004;80: 1215.
13. Maffiuletti NA, Herrero AJ, Jubeau M, Impellizzeri FM, Bizzini M. Differences in electrical stimulation thresholds between men and women. Ann Neurol. 2008;63: 507–512.
14. Morrissey M. Electromyostimulation from a clinical perspective. A review. Sports Med. 1988; 6:29–41.
15. Naaman S, Stein R, Thomas C. Minimizing discomfort with surface neuromuscular stimulation. Neurorehabil Neural Repair. 2000;14: 223.
16. Pollock M, Gaesser G, Butcher J, Despres J, Dishman R, Franklin B, Garber C. ACSM position stand: the recommended quantity and quality of exercise for developing and maintaining cardiorespiratory and muscular fitness, and flexibility in healthy adults. Med Sci Sports Exerc. 1998;30: 975.
17. Pyne DB, Boston T, Martin DT, Logan A. Evaluation of the lactate pro blood analyser. Eur J Appl Physiol. 2000;82: 112–116.
18. Shen W, Parsons K. Validity and reliability of rating scales for seated pressure discomfort. Int J Ind Ergon. 1997;20: 441–462.
19. Skinner JS, Hutsler R, Bergsteinova V, Buskirk ER. The validity and reliability of a rating scale of perceived exertion. Med Sci Sports Exerc. 1973;5: 94–96.
20. Theurel J, Lepers R, Pardon L, Maffiuletti N. Differences in cardiorespiratory and neuromuscular responses between voluntary and stimulated contractions of the quadriceps femoris muscle. Respir Physiol Neurobiol. 2007;157: 341–347.
21. Wasserman K, Hansen J, Sue D, Stringer W, Whipp B. Principles of Exercise Testing and Interpretation: Including Pathophysiology and Clinical Applications. Lippincott Williams & Wilkins, 2004.
Keywords:

electromyostimulation; cardiovascular exercise; tolerability

© 2013 National Strength and Conditioning Association