http://informahealthcare.com/ptp ISSN: 0959-3985 (print), 1532-5040 (electronic) Physiother Theory Pract, 2014; 30(4): 276–281 ! 2014 Informa Healthcare USA, Inc. DOI: 10.3109/09593985.2013.868563

RESEARCH REPORT

Neuromuscular electrical stimulation pulse duration and maximum tolerated muscle torque Wayne Scott, PhD, PT, Kathleen Flora, DPT, Barbara J. Kitchin, DPT, Adam M. Sitarski, DPT, and Joshua B. Vance, DPT Department of Physical Therapy, Husson University, One College Circle, Bangor, ME, USA

Abstract

Keywords

Neuromuscular electrical stimulation (NMES) is a physical therapy intervention used to treat muscle weakness. NMES-elicited forces during therapy are correlated with strength gains. Patient discomfort limits NMES-elicited forces potentially compromising strength gains and the efficacy of this invention. The purpose of this study was to determine if NMES containing two different electrical stimulation pulse durations (200 or 500 ms) affected the knee extensor muscle torques subjects tolerated. Other NMES characteristics were identical in the two conditions: monophasic square-wave pulses; 75 pulses per second; and electrical stimulation train duration of one second. The primary dependent variable of interest was the percentage of maximum voluntary isometric contraction (MVIC) tolerated. The two pulse duration conditions were tested during a single session on the opposing lower extremities of 15 subjects. Subjects tolerated 49.3  18.7% of MVIC torques in the 500-ms condition versus 44.5  17.9% of MVIC torques in the 200-ms condition, which was a statistically significant difference (p ¼ 0.02). Further research is needed to explore if the differences observed in this study would lead to clinically significant differences in strength gains and to see if the findings of this study can be generalized to other forms of NMES that contain other types of wave forms.

Maximum tolerance, muscle torque, neuromuscular electrical stimulation

Strength gains can be produced in the weakened muscles of clinical populations using neuromuscular electrical stimulation (NMES) and in some cases use of NMES may be more efficacious for strengthening than volitional exercise alone (e.g. the quadriceps muscle following total knee arthroplasty) (Bourjeily-Habr et al, 2002; Piva et al, 2007; Snyder-Mackler, Delitto, Bailey, and Stralka, 1995; Stevens, Mizner, and SnyderMackler, 2004; Stevens-Lapsley et al, 2012a). This may be in part because NMES recruitment of motor units does not strictly follow the size principle allowing some large Type II motor units to be recruited and presumably strengthened at lower total muscle forces than would occur during volitional exercise (Bickel, Gregory, and Dean, 2011; Gregory and Bickel, 2005). An additional potential mechanism of NMES-induced strength gains is improvement in volitional muscle activation (Maffiuletti, 2010). Regardless, strength gains from NMES are proportional to the forces produced during training with higher training forces resulting in greater strength gains (Filipovic, Kleino¨der, Do¨rmann, and Mester, 2011; Selkowitz, 1985; Snyder-Mackler, Delitto, Stralka, and Bailey, 1994; StevensLapsley et al, 2012b). The force elicited from muscle contractions when using NMES is dependent on the parameters of the electric stimulation. Unless, however, entirely inappropriate parameters are chosen (e.g. a very low frequency) or the stimulator lacks sufficient power, patient

Address correspondence to Wayne Scott, PhD, PT, Department of Physical Therapy, Husson University, One College Circle, Bangor, ME 04401, USA. E-mail: [email protected]

Received 5 March 2013 Revised 16 September 2013 Accepted 17 September 2013 Published online 23 December 2013

discomfort is usually the limiting factor in the production of high muscle forces (Lyons, Robb, Irrgang, and Fitzgerald, 2005; Scott, Causey, and Marshall, 2009). Typically muscle torques generated by NMES do not exceed 80% of the maximal voluntary torque producing capacity of the muscle even in those individuals with the highest tolerance (Lyons, Robb, Irrgang, and Fitzgerald, 2005; Scott, Causey, and Marshall, 2009). People demonstrate a high amount of variability in their tolerance of NMES-generated contractions and the parameters of the electrical stimulation affect the amount of muscle torque a person is willing to tolerate during NMES (Bellew et al, 2012; Delitto, Strube, Shulman, and Minor, 1992; Scott, Causey, and Marshall, 2009). Conventional opinion, largely based on anecdotal evidence, holds that ‘‘Russian’’ stimulation parameters are the most effective for eliciting high force muscle contractions (Ward and Shkuratova, 2002). Russian stimulation parameters consist of very high-frequency bursts (carrier frequency ¼ 2.5 kHz) of alternating current delivered at 50 bursts per second with a 50% duty cycle. It is unclear however that Russian stimulation is optimal for maximizing force production from electrically recruited muscle (Bellew et al, 2012; Ward, 2006, 2009). Although Russian stimulation may not be optimal there is no consensus on the characteristics of NMES that produce the highest force responses. Research has been performed varying the characteristics of a number of different NMES parameters simultaneously, including: waveform, pulse duration and frequency (De Domenico and Strauss, 1986; Gregory, Dixon, and Bickel, 2007). This contributes to the lack of conclusive data regarding the optimal characteristic for any given single stimulation parameter. A study conducted by De Domenico and Strauss (1986) demonstrates the difficulty in interpreting the research on the

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Introduction

History

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selection of stimulation parameters that optimize muscle force or torque production during NMES. They determined the maximum tolerated peak quadriceps femoris muscle torques produced by seven different stimulators. Each of the stimulators had a different waveform, pulse duration and frequency combination. This study did not identify any significant differences that could be attributed to pulse duration, the parameter of interest in this study. The only significant difference noted was between two stimulators that produced the lowest torques in the study. A difference was found between a stimulator with 25-ms pulse durations and a stimulator with 100-ms pulse durations. The 25-ms pulse duration produced higher torques than the 100-ms pulse duration. The fact that the NMES with 25-ms pulse durations produced higher torques than the NMES with 100-ms pulse durations cannot be confidently attributed to the effect of pulse duration alone because other stimulation parameters also differed. In contrast, Scott, Causey, and Marshall (2009) showed when pulse duration was the only stimulation parameter varied, NMES using 200-ms pulse durations allowed subjects to tolerate significantly higher knee extensor muscle torques than NMES using 50-ms pulse durations, suggesting relatively short pulse durations are not optimal for the production of high muscle torques. In this study, we seek to continue a systematic examination of the effect of pulse duration on the tolerance of NMES-elicited muscle torque production. Pulse duration affects the recruitment of muscle and torque production over a range from 0 to approximately 500 ms (Gregory, Dixon, and Bickel, 2007; Kesar, Chou, and Binder-Macleod, 2008). The purpose of this study was to test whether relatively long pulse durations of 500 ms as compared with medium range pulse durations of 200 ms would allow subjects to tolerate higher knee extensor muscle torques. Based on our previous study (Scott, Causey, and Marshall, 2009) that demonstrated NMES of 200-ms pulse durations resulted in tolerance of greater muscle torque than NMES of 50-ms pulse durations, we hypothesized NMES consisting of 500-ms pulse durations would allow for tolerance of higher muscle torques than NMES with 200-ms pulse durations and that this difference would be associated with lower peak voltages but greater phase charges in the 500-ms condition. During threshold testing we hypothesized that the sensory, motor and pain thresholds would be associated with lower peak voltages and greater phase charges in the 500-ms condition as compared with the 200-ms condition. Finally, we hypothesized that the maximum tolerated torques would be associated with similar peak voltages and phase charges in the 200-ms condition to those that produced pain during the threshold testing whereas in the 500-ms condition the peak voltages and phase charges would be lower than those that produced pain during the threshold testing.

Methods Subjects Sixteen adults (7 females, 9 males; mean age in years ¼ 25.4 SD 5.9) participated in the study. All participants were without a history of cardiovascular disease, neurological disease or significant musculoskeletal disorders (e.g. ligament tears or other injury requiring surgery) of either lower extremity which could have limited their ability to generate maximal muscular efforts. Individuals with contraindications to electrical stimulation, such as cardiac pacemakers or other implanted electrical devices, were excluded. Most participants were students in a physical therapy program who had some familiarity with electrical stimulation although not with attempting to tolerate maximum NMESgenerated muscle contractions. All participants received and gave written informed consent prior to participating in the study. The study was completed in accordance with and approval by the

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Husson University Institutional Review Board for Human Subjects. Procedure The entire testing protocol was carried out on one leg with one of the two pulse duration conditions before the participant was repositioned and the testing protocol was repeated on the opposite leg with the second of the two pulse duration conditions. The order of testing was randomized as to which lower extremity and which pulse duration condition was tested first. By using both legs we minimized the participants’ time commitment to a single testing session lasting approximately 45 min. By randomizing the testing order of the legs and pulse duration conditions we accounted for any ordering effect. Participants began with a 5-min warm-up on a lower extremity ergometer (Peak Bike Ergomedic 894 E, Monark Sport & Medicine, Varberg, Sweden) at a low intensity. Next each participant was positioned on the padded seat of a dynamometer (BIODEX System 3 and BIODEX System 3 Advantage Software, BIODEX Medical Systems, Inc., Shirley, NY) and secured with non-elastic shoulder straps, placed in an X-shaped pattern over the chest, along with a waist strap to keep the participant in position. The lower extremity was placed at 90 of knee flexion and held there by the dynamometer in isometric mode. The leg was secured with a padded strap to the distal aspect of the lower leg, just superior to the ankle malleoli. The lever arm of the dynamometer was positioned with the axis of rotation centered at the lateral condyle of the femur of the knee for each participant. Electrical stimulation in the form of monophasic square-wave pulses was delivered via a Grass Technologies S48 Square Pulse Stimulator with a SIU8T Stimulation Isolation Unit. This device was used to deliver two different test conditions: (1) NMES with 200-ms pulse durations or (2) 500-ms pulse durations. These pulse durations were chosen based on the muscle force versus pulse duration relationship. It is known that at a given voltage or current a 200-ms pulse duration is in the middle of this relationship, producing approximately 50–60% of the force produced at longer pulse durations that maximize the influence of pulse duration on the muscle force response. A pulse duration of approximately 500 ms is close to maximizing the force response from a muscle if the voltage or current is held constant (Gregory, Dixon, and Bickel, 2007; Kesar, Chou, and BinderMacleod, 2008). Each condition began with the participants performing three maximum voluntary isometric contractions (MVICs) while receiving verbal encouragement to promote a maximum effort. The MVICs were performed to determine the participants’ maximum voluntary knee extensor torque capacity. The maximum peak torque produced during the trials was used as the reference for determination of the percentage of MVIC produced during NMES. Electrical stimulation of the knee extensor muscles was carried out after MVIC testing using large (7.62  12.7 cm [3  5 in.]) self-adhesive surface electrodes (fastSTARTÔ Vision Quest Industries Inc., Irvine, CA) placed on the anterior thigh. One electrode was placed proximally over the superior aspect of the anterior lateral thigh centered approximately 10 cm inferior to the anterior superior iliac spine of the pelvis over the quadriceps femoris muscle while the other was placed distally over the medial anterior portion of the thigh centered approximately 5 cm superior to the middle of the patella over the vastus medialis obliquus. Both electrodes were oriented at approximately a 45 angle from supero-lateral to infero-medial. The placement of the electrodes on a participant’s opposing leg was identical. Following electrode placement, thresholds for sensory, motor and pain were determined with 1-s electrical stimulation trains of

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pulses at a rate of 5 pulses per second (pps) as the voltage was incrementally increased. The low frequency was chosen to decrease the likelihood of confounding muscle torque-related discomfort with the pain threshold produced by the electrical stimulation itself. The sensory and pain thresholds were recorded based on the participants’ reports of the voltages at which they first felt the stimulation and their assessment of when the stimulation began to hurt. The motor threshold was determined by observation of a visible muscle twitch by an experimenter. Participants were asked to attempt to match the sensation of pain they experienced when they reached their subjective pain threshold in both pulse duration conditions. Next electrical stimulation trains were delivered at a rate of 75 pps for 1 s to determine the maximum peak knee extensor muscle torque the participants were willing to tolerate. The initial voltage used was that of the motor threshold that was determined during the threshold testing. Participants used an 11-point verbal pain scale (0 ¼ ‘‘no pain’’ ranging to 10 ¼ ‘‘worst pain imaginable’’) after the delivery of each electrical stimulation train to rate their discomfort. Trains of electrical stimulation were delivered approximately every 30 s as the voltage was incrementally increased until the participant rated their pain as a 7 or greater on the pain scale or communicated their unwillingness to tolerate any further increase in the stimulation voltage. The incremental increases in voltage were either 10 or 15 V at the beginning and middle of the testing and then reduced to either 5 or 10 V as the participants’ tolerance limit was approached. The reduction in the incremental increase was in order to avoid large increases in torque when approaching the participants’ limit of tolerance. The incremental increases were not standardized because depending on factors such as body size, muscle size and amount of subcutaneous fat, a standardized increase in voltage produces different increases in muscle torque for different people. Generally, for large-bodied participants we used larger incremental increases in the voltage in order to avoid an excessive number of contractions and the risk of fatiguing the muscle, whereas for small-bodied participants we used smaller incremental increases in order to avoid large increases in muscle torque that may have unsettled the participants or greatly exceeded the amount of discomfort the participants were willing to tolerate. The range of the number of stimulation trains required to reach the participants’ maximum tolerance varied between 4 and 8 with 5 or 6 contractions being the most common. Participants understood that the goal was to reach a maximal tolerated muscle contraction and that a rating of greater than 6 on the pain scale would result in termination of the testing. In effect this resulted in every participant using the pain ratings to report a 7 (or higher in one case) at the point when they were unwilling to tolerate another increase in stimulation intensity. We believe based on our previous experience evoking maximum tolerated NMES-induced contractions that each participant was at their maximum tolerated limit. The peak muscle torque produced was recorded for each train of stimulation. The participants were instructed to ‘‘relax and let the stimulation make your muscle contract’’. As in the threshold testing for pain, participants were asked to attempt to match the discomfort that caused them to stop the testing during the second condition with that which stopped the testing during the first condition. Participants were given a 5-min rest period before the alternate pulse duration condition testing was begun on the opposite lower extremity. All data were recorded by an observer who was blinded to the pulse duration condition that was being tested. Participants were also blinded to the pulse duration condition being tested, as well as to the muscle torques that were produced.

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Data analysis Statistical software (Microsoft Office Excel 2007, Microsoft Inc., Redmond, WA and Statistical & Package for the Social Sciences (SPSS) v14.0, SPSS Inc., Chicago, IL) was used to calculate means and standard deviations for the MVIC torques, NMESelicited peak isometric muscle torques as a percentage of the respective MVIC torques for the two pulse duration conditions, the peak voltages and phase charges that generated the maximum torque responses and those that produced the sensory, motor and pain responses during the threshold testing. The phase ‘‘charges’’ were calculated as a product of the pulse duration and voltage because we did not know the current. Paired t-tests were used to compare the mean differences in the MVIC torques, maximum torques tolerated and the peak voltages and phase charges that elicited the maximum responses for the 200- and 500-ms pulse duration conditions. In addition, paired t-tests were used to compare the peak voltages and phase charges at the sensory, motor and pain thresholds for the two conditions, and the peak voltages and phase charges at the pain thresholds as compared with those at the maximum tolerated torques for each condition, respectively.

Results All 16 participants completed the data collection. One participant was excluded in the data analysis due to voluntarily contracting along with the electrical stimulation creating a greater torque than the electrical stimulation would have produced. Therefore, the data of 15 participants were analyzed. The participants produced an average MVIC torque of 198.9 Nm (SD 52.8) with the legs used for the 200-ms pulse duration testing, and 205.1 Nm (SD 60.3) with the legs used for the 500-ms pule duration testing, which were not significantly different from one another (p ¼ 0.20). The primary dependent variable of interest was the percentage of MVIC tolerated in the two pulse duration conditions. Thirteen of the 15 participants tolerated higher torques in the 500-ms pulse duration condition as shown in Figure 1. The analysis of the group data revealed that participants tolerated approximately 5% more of the available knee extensor muscle torque in the 500-ms pulse duration condition (49.3% SD 18.7%) as compared with the 200-ms pulse duration condition (44.5% SD 17.9%) which was a statistically significant difference (p ¼ 0.02). The values for all of the following comparisons are shown in Table 1. The peak voltages at the maximal tolerated torque were significantly greater in the 200-ms condition as compared with the 100.0% 200ms 80.0%

% MVIC

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500ms

60.0% 40.0% 20.0% 0.0%

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Parcipant No.

Figure 1. Individual subject data for the percentage of MVIC produced during NMES in response to stimulation trains containing 200- or 500-ms monophasic, square-wave pulses.

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Table 1. Voltages and phase charges at the sensory, motor and pain thresholds and at the maximum tolerated torque. Data presented as means with standard deviations. See text for significant differences. Variable

Measurement

Pulse duration (ms) Sensory threshold voltage (V) Motor threshold (V) Pain threshold voltage (V) Sensory threshold phase charge (V*ms) Motor threshold phase charge (V*ms) Pain threshold phase charge (V*ms) Voltage at maximum tolerated torque (V) Phase charge at maximum tolerated torque (V*ms)

200 13.2 (4.4) 28.1 (8.1) 108.7 (27.5) 2640.0 (879.0) 5626.7 (1614.0) 21 733.3 (5496.3) 94.3 (22.5) 18 857.1 (4504.0)

500 10.3 (4.2) 26 (4.8) 96.3 (22.6) 5166.7 (2093.1) 13 000.0 (2420.2) 48 166.7 (11 278.4) 80.4 (16.3) 40 178.6 (8172.7)

500-ms condition, while the phase charges were significantly greater in the 500-ms condition as compared with the 200-ms condition (p50.001 for both). The threshold testing revealed that the sensory and pain thresholds were provoked at significantly higher peak voltages (p50.005 for both) but lower phase charges (p50.001 for both) in the 200-ms condition as compared with the 500-ms condition. For the motor threshold although the phase charge was significantly lower in the 200-ms condition (p50.001) there was only a trend for the peak voltage to be higher (p ¼ 0.09). During the testing of maximum tolerated torque in the 200-ms pulse duration condition both the peak voltages and the phase charges were significantly lower than those that provoked pain during the threshold testing (p50.05 for both). The same was true in the 500-ms pulse duration condition for both the peak voltages and phase charges (p50.01 for both). Differences between the self-reported pain levels at the maximum tolerated torques were minimally variable and did not permit statistical analysis. Fourteen of the 15 participants reported the same pain level of 7/10 at the maximum tolerated muscle torques for the two conditions. One participant reported 8/10 pain rating during the 200-ms condition and 7/10 during the 500-ms condition at the maximum tolerated muscle torques.

Discussion The purpose of this study was to investigate the effect of pulse duration on the maximum tolerated electrically elicited muscle torque by comparing NMES with 200- or 500-ms pulse durations. Based on our prior study which showed that NMES with 200-ms pulse durations allowed participants to tolerate greater knee extensor muscle torques than NMES with 50-ms pulse durations we hypothesized that in this study the NMES with 500-ms pulse durations would allow participants to tolerate greater muscle torques than the NMES with 200-ms pulse durations (Scott, Causey, and Marshall, 2009). This was the case for 13 of the 15 individual participants and for the group means. Participants tolerated approximately 5% more of the available volitional muscle torque (49.3% versus 44.5%) in the 500-ms pulse duration condition as compared with the 200-ms pulse duration condition. This difference is unlikely to be explained by participants tolerating more discomfort in the 500-ms pulse duration condition, as all but one participant reported the same level of pain (7) on the 0–10 pain scale when they reached their tolerance limit and testing was terminated, and the one participant who did not reported an 8 for the 200-ms pulse duration condition and a 7 for the 500-ms pulse duration condition. If this had any effect at all it

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would have biased the results in favor of the 200-ms pulse duration condition producing greater muscle torques. Regardless of the reported pain ratings all participants understood that the goal was to tolerate the greatest level of electrical stimulation and muscle torque that they were willing to experience and this is what was achieved during the testing. Participants terminated testing at the point when they were no longer willing to tolerate another increase in the stimulation voltage, as would be the case clinically when the goal is to maximize the efficacy of NMES strengthening. The clinical relevance of the finding that the 500-ms pulse duration as compared with the 200-ms pulse duration condition allowed participants to tolerate recruitment of 5% more of the available MVIC torque is unknown. We are unaware of any study that has compared the strengthening effects of different types of NMES that produced different torques during training. The work that has been done in this area typically examines strength gains from NMES in comparison to control groups or other non-NMES interventions (Filipovic, Kleino¨der, Do¨rmann, and Mester, 2011; Maddocks, Gao, Higginson, and Wilcock, 2013; Stevens, Mizner, and Snyder-Mackler, 2004). We do know that in general there is a positive correlation between the percentages of MVIC produced during training and subsequent strength gains (Filipovic, Kleino¨der, Do¨rmann, and Mester, 2011; Selkowitz, 1989; Snyder-Mackler, Delitto, Stralka, and Bailey, 1994; StevensLapsley et al, 2012a). It may be important to consider that the 5% more of the MVIC that the 500-ms pulse duration allowed participants to tolerate almost certainly resulted from the recruitment of more motor units than the 200-ms pulse duration because given the 75 pps frequency of stimulation in both conditions and the force–frequency relationship any additional torque would have been produced from additional recruitment of motor units not producing more force from a similar number of motor units. Additionally, whatever additional motor units that were recruited would have been producing near maximum force, presumably providing a potent stimulus for hypertrophy and strength increases in those additionally recruited muscle fibers (Gregory, Dixon, and Bickel, 2007). Whether this would be adequate to stimulate greater increases in patients’ strength and improve their function following a training program is unknown and likely would be dependent on other aspects of the training load as well (e.g. number of contractions, duration of contractions and frequency of training sessions). We examined the peak voltages and phase charges associated with the production of the maximum muscle torques as well as the sensory, motor and pain thresholds. The phase charges were significantly greater at the maximum torques in the 500-ms condition as compared with the 200-ms condition. Given that phase charge is considered a primary determinant of nerve recruitment this observation is consistent with recruitment of more motor units and the production of greater muscle torques in the 500-ms condition, and consistent with previous research demonstrating greater phase charges are associated with greater electrically elicited muscle torques (Scott, Causey, and Marshall, 2009; Snyder-Mackler, Garrett, and Roberts, 1989). In our previous study examining the effect of pulse duration on the maximum tolerated muscle torque, the pulse duration condition which resulted in lower maximum muscle torques was associated with significantly higher peak currents (Scott, Causey, and Marshall, 2009). Although in this study we had no way of measuring the current, given that current is proportional to voltage assuming no change in resistance, we can be reasonably confident that the greater peak voltages at the maximum tolerated muscle torques in the 200-ms condition corresponded to greater peak currents. As we suggested in our previous study comparing NMES with 50 or 200-ms pulse durations it may be that high peak

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currents limit the electrically elicited maximum tolerated torque (Scott, Causey, and Marshall, 2009). In contrast to our previous study, however, the peak voltages (currents) and phase charges that provoked pain during threshold testing were significantly greater than those associated with the maximum tolerated torques. In our previous study with NMES of 50-ms pulse durations, the peak current and phase charges at the maximum tolerated torques were not statistically different than those that provoked pain during threshold testing and were in fact nearly identical (Scott, Causey, and Marshall, 2009). In contrast, there were trends (p ¼ 0.07) for the peak currents and phase charges at the maximum tolerated torques in the 200-ms condition to be lower than those that provoked pain during the threshold testing (Scott, Causey, and Marshall, 2009). This led us to suggest that at the higher ranges of pulse durations over which torque varies it may be the muscle contractions producing discomfort rather than recruitment of nociceptors. This suggestion appears to be supported by this study. In the 200-ms condition both the peak voltages and phase charges were significantly lower at the maximum tolerated torque than those that produced pain during the threshold testing. The fact that what was a trend in our previous study and a statistically significant difference in this study is likely explained by a lack of power in our previous study (i.e. only 10 versus 15 participants). In this study, it was also true that in the 500-ms condition, the peak voltages and phase charges at the maximum tolerated muscle torques were significantly lower than those that provoked pain during the threshold testing. This may explain why despite a large difference in where the pulse durations lay on the muscle force versus pulse duration relationship, we observed a relatively small difference in the percentage of MVIC tolerated in the two conditions. That is, there is a ceiling effect where as long as the pulse duration is not so short that particularly high peak voltages (currents) are required to recruit the muscle then it is the muscle forces themselves that produce discomfort and limit people’s ability to tolerate high torques. Personal experience and participants reports support this idea as the discomfort at high muscle torques is not the same subjective feeling of discomfort that produces pain during threshold testing at low muscle forces. Selkowitz (1985) similarly commented that at high muscle torques the discomfort is due to the muscle contractions not the electrical stimulation. Given that it appears that it is the muscle contractions that produce discomfort at pulse durations at or greater than 200 ms it begs the question of why we observed participants tolerating greater muscle torques in the 500-ms condition. A potential explanation is that although the peak voltages and phase charges during the 200-ms condition did not reach the values associated with pain during the threshold testing that nonetheless there was some influence of nociceptors producing an additive effect with the discomfort associated with a given muscle torque resulting in participants terminating testing at lower muscle torques in the 200-ms condition. After all, participants reached sensory, motor and pain thresholds at lower phase charges and higher peak voltages (only a trend for the motor threshold) in the 200-ms condition during the threshold testing and similarly had higher peak voltages and lower phase charges at the maximum tolerated torques in the 200-ms as compared with the 500-ms condition. The frequency of the stimulation was different between the threshold testing and the maximum tolerated torque testing (5 versus 75 pps). Frequency unlike pulse duration would not influence the recruitment of nerves. It does, however, lead to greater temporal summation and therefore influences the force output from the motor units that are recruited (Gregory, Dixon, and Bickel, 2007). It would also be the case that any nociceptors that were recruited would have been activated at this high frequency and therefore

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could have potentially played a role in participants deciding to terminate the testing. Regardless of the physiologic mechanisms limiting NMES, in a clinical population it is important to maximize efficacy with parameters that maximize the tolerated muscle torque in order to produce the greatest strength gains (Snyder-Mackler, Delitto, Stralka, and Bailey, 1994; Selkowitz, 1989; Stevens-Lapsley et al, 2012b). The findings from this study suggest that when using square-waved monophasic pulses, durations of 500-ms optimize the influence of the pulse duration parameter on the maximum tolerated muscle torque response as compared with shorter pulse durations. It is unclear if longer pulse durations (4500-ms) would result in similar or greater or even lower maximum tolerated muscle torques. We suspect based on muscle force-pulse duration curves and what we believe to be the primary cause of discomfort at long pulse durations that there would be no advantage to using longer pulse durations given that the muscle torque would produce the limiting discomfort. The findings from this study cannot identify the pulse duration threshold between 200- and 500-ms where the pulse duration becomes short enough that the maximum tolerated muscle torque is compromised. Furthermore, it is not known if the relatively small differences observed in this study would be large enough to result in clinical differences in strength outcomes in patient populations. Finally, the results from this study may not be applicable to other types of electrical stimulation such as pulsed current with biphasic waves, alternating current or other types of waveforms such as ‘‘Russian’’ stimulation.

Declaration of interest The authors report no conflicts of interest.

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Neuromuscular electrical stimulation pulse duration and maximum tolerated muscle torque.

Neuromuscular electrical stimulation (NMES) is a physical therapy intervention used to treat muscle weakness. NMES-elicited forces during therapy are ...
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