ASSESSMENT OF QUADRICEPS MUSCLE INACTIVATION WITH A NEW ELECTRICAL STIMULATION PARADIGM VANESSA WELLAUER, MSc,1 CLAUDIA MORF, MSc,1 MARCO A. MINETTO, MD,2 NICOLAS PLACE, PhD,3 and NICOLA A. MAFFIULETTI, PhD1 1
Neuromuscular Research Laboratory, Schulthess Clinic, Lengghalde 2, 8008 Zurich, Switzerland Division of Endocrinology, Diabetology and Metabolism, Department of Medical Sciences, University of Turin, Turin, Italy 3 Institute of Sport Sciences and Department of Physiology, Faculty of Biology and Medicine, University of Lausanne, Lausanne, Switzerland 2
Accepted 11 April 2014 ABSTRACT: Introduction: In this study we evaluated the validity of garment-based quadriceps stimulation (GQS) for assessment of muscle inactivation in comparison with femoral nerve stimulation (FNS). Methods: Inactivation estimates (superimposed doublet torque), self-reported discomfort, and twitch and doublet contractile properties were compared between GQS and FNS in 15 healthy subjects. Results: Superimposed doublet torque was significantly lower for GQS than for FNS at 20% and 40% maximum voluntary contraction (MVC) (P < 0.01), but not at 60%, 80%, and 100% MVC. Discomfort scores were systematically lower for GQS than for FNS (P < 0.05). Resting twitch and doublet peak torque were lower for GQS, and time to peak torque was shorter for GQS than for FNS (P < 0.01). Conclusions: GQS can be used with confidence for straightforward evaluation of quadriceps muscle inactivation, whereas its validity for assessment of contractile properties remains to be determined. Muscle Nerve 51: 117–124, 2015
Transcutaneous electrical stimulation is used widely to evaluate neuromuscular function in vivo1,2 because it evokes standardized muscle contractions that are independent from motivational factors. Muscle inactivation and contractile properties are assessed commonly to verify the consequences of a disease3–5 or the effect of exerciseinduced fatigue on neuromuscular function,6,7 particularly for the quadriceps muscle. More specifically, electrical stimulation combined with voluntary contractions has found valuable clinical use for detection of the inability to fully activate the quadriceps muscle, which has been reported to have a great impact on orthopedic rehabilitation8,9 as well as to assess the central component of muscle fatigue in patients, healthy subjects, and athletes.5–7,10,11 The most commonly used technique for assessment of quadriceps muscle inactivation is twitch interpolation, which consists of application of supramaximal electrical impulses to the femoral Abbreviations: ANOVA, analysis of variance; FNS, femoral nerve stimulation; GQS, garment-based quadriceps stimulation; MVC, maximal voluntary contraction; SD, standard deviation Key words: activation; contractility; discomfort; quadriceps; twitch interpolation Correspondence to: N.A. Maffiuletti; e-mail: [email protected] C 2014 Wiley Periodicals, Inc. V
Published online 17 April 2014 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/mus.24266
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nerve or to the quadriceps muscle belly during a maximal voluntary contraction (MVC).12,13 The 2 main limitations of femoral nerve stimulation (FNS) are excessive discomfort and the timeconsuming methodological precautions that are required to obtain valid estimates of muscle inactivation (e.g., determination of supramaximal stimulus, femoral nerve localization, and electrode displacement with respect to the nerve). Taken as a whole, these shortcomings preclude clinical acceptability of FNS for evaluation purposes, particularly in frail and highly sensitive individuals. Electrical stimulation can also be applied to the quadriceps muscle belly, which can partly diminish the discomfort,14 but it usually results in submaximal and relatively superficial motor unit recruitment.15,16 Despite these drawbacks, a recent study conducted in our laboratory showed that over-themuscle stimulation and FNS provided similar estimates of quadriceps inactivation at different contraction intensities, including the MVC level.14 In contrast to our previous study in which 2 large electrodes were used to stimulate the quadriceps muscle,14 we propose here a new stimulation paradigm consisting of a garment-integrated set of 4 large electrodes distributed on the anterior aspect of the thigh (hereafter referred to as garmentbased quadriceps stimulation, GQS), which has been introduced recently for rehabilitation purposes.17 This configuration has the potential to maximize spatial recruitment,17,18 even at submaximal stimulation intensities, and to minimize discomfort,17,18 with straightforward preparation and testing procedures. The main aim of this methodological study was to verify the validity of GQS for the assessment of quadriceps muscle inactivation in healthy subjects. We therefore compared inactivation estimates, selfreported discomfort, and muscle contractile properties between the conventional electrical stimulation modality (FNS) and the new paradigm (GQS). Based on a recent study conducted in our laboratory,14 we hypothesized that submaximal GQS would provide similar estimates of muscle inactivation when compared with supramaximal FNS, while minimizing discomfort. MUSCLE & NERVE
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METHODS Subjects.
Fifteen healthy subjects [9 men and 6 women; age (mean 6 SD) 32 6 8 years and 29 6 6 years, height 181 6 6 cm and 171 6 5 cm, mass 76 6 9 kg and 65 6 10 kg, respectively], who were free from known cardiovascular, neurological, or orthopedic problems, volunteered to participate in this study. They took part in non-competitive or competitive sports (both aerobic exercise and resistance training) of a non-professional nature on 3 or more occasions per week, and half of them had previous experience with the twitch interpolation technique. The study protocol was approved by the local research ethics committee, and written consent forms were signed prior to participation. The experiments conformed to the standards set by the Declaration of Helsinki. Experimental Procedure. Participants completed an experimental session that entailed assessment of knee extension torque and discomfort induced by FNS and GQS. The 2 stimulation modalities were presented randomly. For each modality, the procedures consisted of 3 main phases: single stimulations at rest (to obtain the twitch recruitment curve); paired stimulations during and after an MVC (to obtain superimposed and potentiated doublets, respectively); and paired stimulations during submaximal voluntary contractions (to obtain superimposed doublets). The entire experiment was conducted under isometric conditions and lasted approximately 60 min. Subjects were seated comfortably throughout the experimental session with the tested knee (right) at 90 and the trunk–thigh angle at approximately 100 . To ascertain that the testing session did not result in muscle fatigue, MVC trials (with no superimposed stimuli) were also conducted at the beginning and end of the session. MVC torque did not change from the beginning (226 6 64 Nm) to the end (229 6 71 Nm; P > 0.05) of the experiments in both conditions.
positioned in the groin 3–5 cm below the inguinal ligament. A large (5 3 10 cm) self-adhesive electrode was fixed on the gluteal crease to close the stimulation current loop (monopolar stimulation). Monophasic rectangular pulses of 1 ms were produced via a constant-current stimulator (Model DS7AH; Digitimer, Ltd., Hertfordshire, UK), either as single or paired stimuli (interstimulus interval 10 ms). Before starting data collection, current intensity of a single stimulus was increased progressively from 0 mA to the maximal intensity corresponding to the twitch peak torque (95 6 26 mA). The twitch recruitment curve was obtained subsequently by delivering single pulses to the resting muscle at different arbitrarily defined levels (24%, 48%, 72%, 96%, and 120% of maximal intensity, with 2 stimuli per intensity level presented randomly), 1 every 5 s, while recording twitch torque continuously (Fig. 1A). After 3 min of rest, participants were asked to perform 2 MVCs (separated by approximately 45 s) by contracting their knee extensors as forcefully as possible for 4–5 s. Supramaximal paired stimuli (120% of the maximal intensity) were delivered during and approximately 2 s after each MVC to evoke superimposed and potentiated doublets, respectively (Fig. 1B). After 3 min of rest, subjects were instructed to produce 5s-long submaximal voluntary contractions (20%, 40%, 60%, and 80% MVC, with 2 trials per intensity level presented randomly) by contracting their knee extensors to reach a target torque as provided on a screen. Supramaximal paired stimuli (120% of maximal intensity) were delivered during each contraction to evoke a superimposed doublet (Fig. 1C). Rest periods of 30 s were interspersed between the submaximal contractions.
Torque Recordings. Unilateral isometric knee extension torque was recorded continuously by means of an isokinetic dynamometer (Biodex Corp., Shirley, New York) with a lever arm attached 2–3 cm above the lateral malleolus using a non-elastic strap. Participants were fixed to the dynamometer chair using 2 crossover shoulder harnesses and a belt across the abdomen. Torque signal was fed directly from the dynamometer into a 16-bit A/D converter (Model MP150; Biopac Systems, Goleta, California), then into a computer sampling at 2 kHZ using Acqknowledge software (Biopac Systems).
Subject positioning, stimulation procedures, and parameters (including pulse duration) were identical to the FNS condition, except that the Digitimer stimulator was connected to a commercially available GQS apparel (Kneehab XP; Bio-Medical Research, Galway, Ireland). The garment wraps around the thigh and incorporates an array of 4 large electrodes (10 3 20 cm, 3 3 18 cm, 10 3 7.5 cm, and 7 3 14 cm, for a total surface area of 427 cm2) that cover almost the entire quadriceps muscle. In contrast to FNS, maximal stimulation intensity was fixed arbitrarily at 200 mA for all subjects because of the difficulty in obtaining a plateau in twitch peak torque when delivering electrical stimulation over the quadriceps muscle.12,14,19 The twitch recruitment curve was therefore obtained arbitrarily by delivering single pulses at 40, 80, 120, 160, and 200 mA, and all paired stimuli were delivered at 200 mA.
FNS. The femoral nerve was stimulated using a circular self-adhesive electrode (surface 19.6 cm2)
Discomfort. Self-reported discomfort associated with the application of FNS or GQS was evaluated
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GQS.
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FIGURE 1. Representative traces of resting twitches (A), MVC-superimposed and potentiated doublets (B), and submaximal contraction (20% MVC)–superimposed doublets (C) in response to femoral nerve stimulation (gray lines) and garment-based quadriceps stimulation (black lines).
according to a 0–10-cm horizontal visual analog scale (VAS), with 0 5 no discomfort and 10 5 maximum discomfort. Participants were given the VAS immediately after each single pulse of the twitch recruitment curve (discomfort of the Quadriceps Neuromuscular Testing
twitch), after paired stimulation following the MVC trials (discomfort of the potentiated doublet), and after each paired stimuli superimposed to the submaximal voluntary contractions (discomfort of the superimposed doublet). MUSCLE & NERVE
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Data Analysis. The twitch recruitment curve was constructed by plotting twitch peak torque as a function of stimulation intensity (24%, 48%, 72%, 96%, and 120% of the maximal intensity for FNS, and 40, 80, 120, 160, and 200 mA for GQS). Peak torque and time to peak torque (i.e., the main contractile properties) were also quantified from twitch and potentiated doublet traces (both obtained at 120% of the maximal stimulation intensity for FNS and at 200 mA for GQS). Muscle inactivation was estimated by plotting superimposed doublet torque as a function of contraction intensity (20%, 40%, 60%, 80%, and 100% of the MVC torque) as in our previous study.14 For all variables, the average of the 2 consecutive responses obtained in the same conditions was retained.
Normal distribution was verified using the Shapiro–Wilk test. Because all data were normally distributed, they were expressed as mean and SD and were analyzed using paired t-tests or 2way repeated-measures analyses of variance (ANOVAs). One-tailed paired t-tests were used to evaluate differences in MVC torque, twitch peak torque, twitch time to peak torque, potentiated doublet peak torque, potentiated doublet time to peak torque, and discomfort of the potentiated doublet between stimulation modalities (FNS vs. GQS). A first 2 3 5 ANOVA was used to evaluate the effect of stimulation modality (FNS, GQS) and stimulation intensity (24%, 48%, 72%, 96%, and 120% of maximal intensity for FNS, and 40, 80, 120, 160, and 200 mA for GQS) on twitch torque and discomfort from the recruitment curves. A second 2 3 5 ANOVA was used to evaluate the effect of stimulation modality (FNS, GQS) and contraction intensity (20%, 40%, 60%, 80%, and 100% MVC) on superimposed doublet torque and discomfort of the superimposed doublet. In case of significant main effects or interactions, Tukey honestly significant difference post-hoc tests were applied. The threshold for statistical significance was set at P < 0.05. Statistics.
RESULTS Muscle Contractile Properties.
Figure 1A shows the twitch recruitment curves obtained in a representative subject with FNS and GQS. Twitch peak torque was significantly lower for GQS than for FNS at all stimulation intensities (P < 0.01), except the lowest one (Fig. 2). The average difference in twitch peak torque between FNS and GQS was 12.7 6 8.2% at the highest stimulation intensity. Twitch peak torque did not differ significantly between 72%, 96%, and 120% for FNS and between 160 and 200 mA for GQS (i.e., a sort of plateau was attained at 72% and 160 mA, respectively). Both twitch and potentiated doublet peak torque were 120
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FIGURE 2. Twitch peak torque as a function of stimulation intensity for femoral nerve stimulation (FNS) and garmentbased quadriceps stimulation (GQS). Data points are shown as mean value and standard deviation.
significantly lower for GQS than for FNS (Fig. 3A and B; P < 0.001), and both twitch and potentiated doublet time to peak torque were significantly shorter for GQS than for FNS (P < 0.01; Fig. 3C and D). Muscle Inactivation. Superimposed doublet torque was significantly lower for GQS than for FNS at 20% and 40% MVC (P < 0.01), whereas no difference was observed at 60%, 80%, and 100% MVC (Fig. 4). Discomfort. Discomfort of the twitch was significantly lower for GQS than for FNS [233.2%; 95% confidence interval (CI) range for GQS: 0.03–4.57; 95% CI range for FNS: 0.07–5.39], regardless of the stimulation intensity (P < 0.05 for main effect in ANOVA; Fig. 5A). Discomfort of the potentiated doublet was also significantly lower for GQS than for FNS (221.8%; 95% CI range for GQS: 2.17– 5.23; 95% CI range for FNS: 3.26–6.16; P < 0.01; Fig. 5B). Discomfort of the superimposed doublet was significantly lower for GQS than for FNS (225.6%; 95% CI range for GQS: 0.93–4.59; 95% CI range for FNS: 1.47–5.77), regardless of the contraction intensity (P < 0.05 for main effect in ANOVA; Fig. 5C). DISCUSSION
The main findings of this methodological study are that submaximal GQS resulted in similar muscle inactivation estimates compared with supramaximal FNS for contraction intensities >40% MVC, whereas discomfort scores were systematically lower for the former modality. These findings prove the validity of GQS for assessment of quadriceps muscle inactivation despite differences in resting MUSCLE & NERVE
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FIGURE 3. Twitch peak torque (A), potentiated doublet peak torque (B), twitch time to peak torque (C), and potentiated doublet time to peak torque (D) for femoral nerve stimulation (FNS) and garment-based quadriceps stimulation (GQS). The black circles indicate the mean, and the error bars indicate standard deviation.
muscle contractile properties between the 2 stimulation modalities (GQS evoked smaller and faster twitch and doublet responses). FNS (at rest or superimposed on voluntary contractions) is considered to be the optimum modality for assessment of quadriceps neuromuscular function,20 as supramaximal stimulation of the
FIGURE 4. Superimposed doublet torque as a function of contraction intensity for femoral nerve stimulation (FNS) and garment-based quadriceps stimulation (GQS). Data points are shown as mean value and standard deviation. Quadriceps Neuromuscular Testing
nerve trunk results in synchronous recruitment of all motor units. This assumption is evidenced by the consistent presence of a plateau in evoked twitch torque as FNS intensity is progressively increased,14,21 whereas the plateau is not always observed with stimulation of terminal axonal branches,12,14,19 as is the case for GQS. Consistent with these previous observations, our results show lower amplitudes for twitches and potentiated doublets evoked by GQS as compared to FNS for all stimulation intensities, except the lowest. This result confirms that over-the-muscle stimulation may lead to incomplete motor unit recruitment,1,15,16 even when using multiple electrodes that cover the quadriceps muscle almost entirely, as with GQS. It is very likely that some (presumably deep) motor units would be very difficult to recruit with GQS, even at relatively high stimulation intensities. It should, however, be noted that comparable resting twitch and doublet amplitudes were observed for quadriceps muscle stimulation and FNS by some investigators,21,22 even though higher stimulation intensities and different electrode configurations were used compared with our study. The shorter times to peak torque we observed for GQS-evoked twitch and potentiated doublet responses suggest recruitment of fast-contracting MUSCLE & NERVE
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FIGURE 5. Discomfort of the twitch as a function of stimulation intensity (A), discomfort of the potentiated doublet (B), and discomfort of the superimposed doublet as a function of contraction intensity (C) for femoral nerve stimulation (FNS) and garment-based quadriceps stimulation (GQS). Data are shown as mean value and standard deviation.
motor units. This is in agreement with our previous findings obtained when comparing twitches evoked by quadriceps muscle stimulation and FNS,14 and is thought to originate from a predomi122
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nant recruitment of type II muscle fibers with GQS, which have a distribution shown to be higher in superficial than in deeper regions of the anterior thigh muscles.23–25 Surprisingly, these differences in spatial recruitment between GQS and FNS had little or no influence on the estimation of quadriceps muscle inactivation. In fact, our results show similar inactivation levels for GQS and FNS at contraction intensities >40% MVC. Again, these findings are very similar to those obtained in our previous twitch interpolation study14 and are likely attributable to the fact that unrecruited motor units during any given voluntary contraction (those with the highest depolarization threshold) are among the first to be recruited with GQS due to their superficial localization and proximity to the stimulating electrodes.23,24 Our data also confirm recent findings by Bampouras et al.,22 who demonstrated that submaximal paired stimuli (as low as 50% of maximal intensity) delivered by 2 surface electrodes positioned over the quadriceps muscle are sufficiently valid for assessment of muscle inactivation, as stimulus spread to other muscles (including antagonists) is lower compared with higher stimulation intensities. Actually, the use of submaximal (rather than maximal) paired stimuli may be particularly appropriate for assessment of muscle inactivation in individuals who present with large neurological deficits, as submaximal current may lower both the discomfort and the risk of underestimating the level of inactivation.26 As expected, differences in current intensity level between the 2 stimulation modalities (submaximal for GQS vs. supramaximal for FNS) are likely to explain, at least in part, the lower discomfort experienced by our subjects during GQS. It should, however, be noted that absolute current intensity was actually 2-fold higher for GQS (200 mA) than for FNS (95 mA), whereas current density (maximum current intensity/total electrode area) was 10-fold higher for FNS (4.85 mA/cm2) compared with GQS (0.47 mA/cm2) due to different electrode size. Activation of Ad and C nociceptive fibers is the main mechanism underlying the discomfort induced by transcutaneous electrical stimulation.27 Although these nociceptive fibers are located in both the nerve trunk and the dermal–epidermal junction, their density is much higher in the former compared with the latter.28 In addition, the amplitude of nociceptive potentials is well correlated with both stimulation charge and nerve fiber density.29 Stimulation charge density (maximum current intensity 3 pulse duration / total electrode area) delivered to the muscle through the 4 large electrodes with GQS (4.6827 C/cm2) was considerably lower than that delivered to the femoral nerve through the small MUSCLE & NERVE
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electrode (4.8526 C/cm2). Therefore, GQS was unsurprisingly found to generate less discomfort than FNS, in line with previous studies.14,21 Besides the intermodality differences in discomfort scores and recruitment noted earlier, GQS may offer some practical advantages compared with FNS. First, application of the GQS apparel, based on anatomical landmarks and being cablefree (from the electrodes to the garment), is extremely simple and does not require any adjustment, as it is the case with femoral nerve localization. In this respect, GQS also offers a practical advantage in comparison to other over-the-muscle stimulation modalities that require the proper placement of 2 or more electrodes over the anterior thigh muscles after identification of their main motor points. Second, the use of a fixed, although arbitrarily defined, submaximal stimulation intensity for all the subjects reduces considerably the duration of the testing session as compared with individual determination of supramaximal intensity for FNS, which takes at least 10 min. Third, electrode displacement (with respect to the axonal branches) induced by voluntary contractions is certainly less problematic compared with FNS, where the small stimulating electrode is likely to be pushed away from the femoral nerve by the nearby tendon. Taken together, these practical benefits of GQS may favor its clinical implementation for evaluation of short- and long-term changes in neuromuscular function induced by physical exercise (e.g., central fatigue),10,11 and/or pathological conditions (e.g., arthrogenic muscle inhibition).8,9 Owing to its simplicity and its straightforward application, GQS would also be particularly suitable for bedside evaluation of quadriceps muscle function (e.g., in critically ill patients) as well as for multicenter studies. This methodological study has some limitations. We did not evaluate patients with orthopedic or neurological conditions (to avoid imposing burdens on them), who would have displayed higher inactivation scores than the healthy subjects we tested.3,4,8,9 Due to time constraints, we did not verify the validity of GQS for detecting central fatigue. One could, however, conjecture that, for physiologically meaningful reductions in MVC torque of 20–40%, such as those induced by strenuous physical exercise,10 assessment of central fatigue with GQS would be comparable to FNS (based on Fig. 4 results for contraction intensities >40% MVC) and therefore valid. Finally, no attempt was made to increase the GQS intensity beyond 200 mA, to adjust the position of GQS electrodes with respect to individual muscle mass or geometry, or to blind the 2 experimental conditions. Quadriceps Neuromuscular Testing
In conclusion, these findings suggest that GQS can be used with confidence for straightforward assessment of quadriceps muscle inactivation. Although these results were not obtained in patients but in healthy subjects, we suggest that GQS would also be suitable for clinical populations, particularly because of the lower level of discomfort. On the other hand, because resting twitch and potentiated doublet responses were significantly larger with FNS, the validity of GQS for evaluation of muscle contractile properties remains to be ascertained. REFERENCES 1. Maffiuletti NA, Minetto MA, Farina D, Bottinelli R. Electrical stimulation for neuromuscular testing and training: state-of-the art and unresolved issues. Eur J Appl Physiol 2011;111:2391–2397. 2. Millet GY, Martin V, Martin A, Verges S. Electrical stimulation for testing neuromuscular function: from sport to pathology. Eur J Appl Physiol 2011;111:2489–2500. 3. Fitzgerald GK, Piva SR, Irrgang JJ, Bouzubar F, Starz TW. Quadriceps activation failure as a moderator of the relationship between quadriceps strength and physical function in individuals with knee osteoarthritis. Arthritis Rheum 2004;51:40–48. 4. Klein CS, Brooks D, Richardson D, McIlroy WE, Bayley MT. Voluntary activation failure contributes more to plantar flexor weakness than antagonist coactivation and muscle atrophy in chronic stroke survivors. J Appl Physiol (1985) 2010;109:1337–1346. 5. de Haan A, de Ruiter CJ, van der Woude LH, Jongen PJ. Contractile properties and fatigue of quadriceps muscles in multiple sclerosis. Muscle Nerve 2000;23:1534–1541. 6. Kent-Braun JA, Le Blanc R. Quantitation of central activation failure during maximal voluntary contractions in humans. Muscle Nerve 1996;19:861–869. 7. Gandevia SC. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 2001;81:1725–1789. 8. Hurley MV, Jones DW, Newham DJ. Arthrogenic quadriceps inhibition and rehabilitation of patients with extensive traumatic knee injuries. Clin Sci (Lond) 1994;86:305–310. 9. Rice DA, McNair PJ. Quadriceps arthrogenic muscle inhibition: neural mechanisms and treatment perspectives. Semin Arthritis Rheum 2010;40:250–266. 10. Millet GY, Lepers R. Alterations of neuromuscular function after prolonged running, cycling and skiing exercises. Sports Med 2004;34: 105–116. 11. Zwarts MJ, Bleijenberg G, van Engelen BG. Clinical neurophysiology of fatigue. Clin Neurophysiol 2008;119:2–10. 12. Behm DG, St-Pierre DM, Perez D. Muscle inactivation: assessment of interpolated twitch technique. J Appl Physiol (1985) 1996;81:2267– 2273. 13. Folland JP, Williams AG. Methodological issues with the interpolated twitch technique. J Electromyogr Kinesiol 2007;17:317–327. 14. Place N, Casartelli N, Glatthorn JF, Maffiuletti NA. Comparison of quadriceps inactivation between nerve and muscle stimulation. Muscle Nerve 2010;42:894–900. 15. Bickel CS, Gregory CM, Dean JC. Motor unit recruitment during neuromuscular electrical stimulation: a critical appraisal. Eur J Appl Physiol 2011;111:2399–2407. 16. Gregory CM, Bickel CS. Recruitment patterns in human skeletal muscle during electrical stimulation. Phys Ther 2005;85:358–364. 17. Feil S, Newell J, Minogue C, Paessler HH. The effectiveness of supplementing a standard rehabilitation program with superimposed neuromuscular electrical stimulation after anterior cruciate ligament reconstruction: a prospective, randomized, single-blind study. Am J Sports Med 2011;39:1238–1247. 18. Paessler HH. Emerging techniques in orthopedics: advances in neuromuscular electrical stimulation. Am J Orthop 2012;41:1–8. 19. Hanchard NC, Williamson M, Caley RW, Cooper RG. Electrical stimulation of human tibialis anterior: (A) contractile properties are stable over a range of submaximal voltages; (B) high- and lowfrequency fatigue are inducible and reliably assessable at submaximal voltages. Clin Rehabil 1998;12:413–427. 20. Maffiuletti NA. Assessment of hip and knee muscle function in orthopaedic practice and research. J Bone Joint Surg Am 2010;92: 220–229. 21. Rodriguez-Falces J, Maffiuletti NA, Place N. Spatial distribution of motor units recruited during electrical stimulation of the quadriceps muscle versus the femoral nerve. Muscle Nerve 2013;48:752–761.
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22. Bampouras TM, Reeves ND, Baltzopoulos V, Jones DA, Maganaris CN. Is maximum stimulation intensity required in the assessment of muscle activation capacity? J Electromyogr Kinesiol 2012;22:873–877. 23. Knight CA, Kamen G. Superficial motor units are larger than deeper motor units in human vastus lateralis muscle. Muscle Nerve 2005;31:475–480. 24. Lexell J, Henriksson-Larsen K, Sjostrom M. Distribution of different fibre types in human skeletal muscles. 2. A study of cross-sections of whole m. vastus lateralis. Acta Physiol Scand 1983;117:115–122. 25. Travnik L, Pernus F, Erzen I. Histochemical and morphometric characteristics of the normal human vastus medialis longus and vastus medialis obliquus muscles. J Anat 1995;187:403–411.
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26. van Leeuwen DM, De Ruiter CJ, De Haan A. Effect of stimulation intensity on assessment of voluntary activation. Muscle Nerve 2012; 45:841–848. 27. Collins WR Jr, Nulsen FE, Randt CT. Relation of peripheral nerve fiber size and sensation in man. Arch Neurol 1960;3:381–385. 28. Kennedy WR, Wendelschafer-Crabb G. The innervation of human epidermis. J Neurol Sci 1993;115:184–190. 29. Casanova-Molla J, Grau-Junyent JM, Morales M, Valls-Sole J. On the relationship between nociceptive evoked potentials and intraepidermal nerve fiber density in painful sensory polyneuropathies. Pain 2011;152:410–418.
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Neuromuscular Research Laboratory, Schulthess Clinic, Lengghalde 2, 8008 Zurich, Switzerland Division of Endocrinology, Diabetology and Metabolism, Department of Medical Sciences, University of Turin, Turin, Italy 3 Institute of Sport Sciences and Department of Physiology, Faculty of Biology and Medicine, University of Lausanne, Lausanne, Switzerland 2
Accepted 11 April 2014 ABSTRACT: Introduction: In this study we evaluated the validity of garment-based quadriceps stimulation (GQS) for assessment of muscle inactivation in comparison with femoral nerve stimulation (FNS). Methods: Inactivation estimates (superimposed doublet torque), self-reported discomfort, and twitch and doublet contractile properties were compared between GQS and FNS in 15 healthy subjects. Results: Superimposed doublet torque was significantly lower for GQS than for FNS at 20% and 40% maximum voluntary contraction (MVC) (P < 0.01), but not at 60%, 80%, and 100% MVC. Discomfort scores were systematically lower for GQS than for FNS (P < 0.05). Resting twitch and doublet peak torque were lower for GQS, and time to peak torque was shorter for GQS than for FNS (P < 0.01). Conclusions: GQS can be used with confidence for straightforward evaluation of quadriceps muscle inactivation, whereas its validity for assessment of contractile properties remains to be determined. Muscle Nerve 51: 117–124, 2015
Transcutaneous electrical stimulation is used widely to evaluate neuromuscular function in vivo1,2 because it evokes standardized muscle contractions that are independent from motivational factors. Muscle inactivation and contractile properties are assessed commonly to verify the consequences of a disease3–5 or the effect of exerciseinduced fatigue on neuromuscular function,6,7 particularly for the quadriceps muscle. More specifically, electrical stimulation combined with voluntary contractions has found valuable clinical use for detection of the inability to fully activate the quadriceps muscle, which has been reported to have a great impact on orthopedic rehabilitation8,9 as well as to assess the central component of muscle fatigue in patients, healthy subjects, and athletes.5–7,10,11 The most commonly used technique for assessment of quadriceps muscle inactivation is twitch interpolation, which consists of application of supramaximal electrical impulses to the femoral Abbreviations: ANOVA, analysis of variance; FNS, femoral nerve stimulation; GQS, garment-based quadriceps stimulation; MVC, maximal voluntary contraction; SD, standard deviation Key words: activation; contractility; discomfort; quadriceps; twitch interpolation Correspondence to: N.A. Maffiuletti; e-mail: [email protected] C 2014 Wiley Periodicals, Inc. V
Published online 17 April 2014 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/mus.24266
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nerve or to the quadriceps muscle belly during a maximal voluntary contraction (MVC).12,13 The 2 main limitations of femoral nerve stimulation (FNS) are excessive discomfort and the timeconsuming methodological precautions that are required to obtain valid estimates of muscle inactivation (e.g., determination of supramaximal stimulus, femoral nerve localization, and electrode displacement with respect to the nerve). Taken as a whole, these shortcomings preclude clinical acceptability of FNS for evaluation purposes, particularly in frail and highly sensitive individuals. Electrical stimulation can also be applied to the quadriceps muscle belly, which can partly diminish the discomfort,14 but it usually results in submaximal and relatively superficial motor unit recruitment.15,16 Despite these drawbacks, a recent study conducted in our laboratory showed that over-themuscle stimulation and FNS provided similar estimates of quadriceps inactivation at different contraction intensities, including the MVC level.14 In contrast to our previous study in which 2 large electrodes were used to stimulate the quadriceps muscle,14 we propose here a new stimulation paradigm consisting of a garment-integrated set of 4 large electrodes distributed on the anterior aspect of the thigh (hereafter referred to as garmentbased quadriceps stimulation, GQS), which has been introduced recently for rehabilitation purposes.17 This configuration has the potential to maximize spatial recruitment,17,18 even at submaximal stimulation intensities, and to minimize discomfort,17,18 with straightforward preparation and testing procedures. The main aim of this methodological study was to verify the validity of GQS for the assessment of quadriceps muscle inactivation in healthy subjects. We therefore compared inactivation estimates, selfreported discomfort, and muscle contractile properties between the conventional electrical stimulation modality (FNS) and the new paradigm (GQS). Based on a recent study conducted in our laboratory,14 we hypothesized that submaximal GQS would provide similar estimates of muscle inactivation when compared with supramaximal FNS, while minimizing discomfort. MUSCLE & NERVE
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METHODS Subjects.
Fifteen healthy subjects [9 men and 6 women; age (mean 6 SD) 32 6 8 years and 29 6 6 years, height 181 6 6 cm and 171 6 5 cm, mass 76 6 9 kg and 65 6 10 kg, respectively], who were free from known cardiovascular, neurological, or orthopedic problems, volunteered to participate in this study. They took part in non-competitive or competitive sports (both aerobic exercise and resistance training) of a non-professional nature on 3 or more occasions per week, and half of them had previous experience with the twitch interpolation technique. The study protocol was approved by the local research ethics committee, and written consent forms were signed prior to participation. The experiments conformed to the standards set by the Declaration of Helsinki. Experimental Procedure. Participants completed an experimental session that entailed assessment of knee extension torque and discomfort induced by FNS and GQS. The 2 stimulation modalities were presented randomly. For each modality, the procedures consisted of 3 main phases: single stimulations at rest (to obtain the twitch recruitment curve); paired stimulations during and after an MVC (to obtain superimposed and potentiated doublets, respectively); and paired stimulations during submaximal voluntary contractions (to obtain superimposed doublets). The entire experiment was conducted under isometric conditions and lasted approximately 60 min. Subjects were seated comfortably throughout the experimental session with the tested knee (right) at 90 and the trunk–thigh angle at approximately 100 . To ascertain that the testing session did not result in muscle fatigue, MVC trials (with no superimposed stimuli) were also conducted at the beginning and end of the session. MVC torque did not change from the beginning (226 6 64 Nm) to the end (229 6 71 Nm; P > 0.05) of the experiments in both conditions.
positioned in the groin 3–5 cm below the inguinal ligament. A large (5 3 10 cm) self-adhesive electrode was fixed on the gluteal crease to close the stimulation current loop (monopolar stimulation). Monophasic rectangular pulses of 1 ms were produced via a constant-current stimulator (Model DS7AH; Digitimer, Ltd., Hertfordshire, UK), either as single or paired stimuli (interstimulus interval 10 ms). Before starting data collection, current intensity of a single stimulus was increased progressively from 0 mA to the maximal intensity corresponding to the twitch peak torque (95 6 26 mA). The twitch recruitment curve was obtained subsequently by delivering single pulses to the resting muscle at different arbitrarily defined levels (24%, 48%, 72%, 96%, and 120% of maximal intensity, with 2 stimuli per intensity level presented randomly), 1 every 5 s, while recording twitch torque continuously (Fig. 1A). After 3 min of rest, participants were asked to perform 2 MVCs (separated by approximately 45 s) by contracting their knee extensors as forcefully as possible for 4–5 s. Supramaximal paired stimuli (120% of the maximal intensity) were delivered during and approximately 2 s after each MVC to evoke superimposed and potentiated doublets, respectively (Fig. 1B). After 3 min of rest, subjects were instructed to produce 5s-long submaximal voluntary contractions (20%, 40%, 60%, and 80% MVC, with 2 trials per intensity level presented randomly) by contracting their knee extensors to reach a target torque as provided on a screen. Supramaximal paired stimuli (120% of maximal intensity) were delivered during each contraction to evoke a superimposed doublet (Fig. 1C). Rest periods of 30 s were interspersed between the submaximal contractions.
Torque Recordings. Unilateral isometric knee extension torque was recorded continuously by means of an isokinetic dynamometer (Biodex Corp., Shirley, New York) with a lever arm attached 2–3 cm above the lateral malleolus using a non-elastic strap. Participants were fixed to the dynamometer chair using 2 crossover shoulder harnesses and a belt across the abdomen. Torque signal was fed directly from the dynamometer into a 16-bit A/D converter (Model MP150; Biopac Systems, Goleta, California), then into a computer sampling at 2 kHZ using Acqknowledge software (Biopac Systems).
Subject positioning, stimulation procedures, and parameters (including pulse duration) were identical to the FNS condition, except that the Digitimer stimulator was connected to a commercially available GQS apparel (Kneehab XP; Bio-Medical Research, Galway, Ireland). The garment wraps around the thigh and incorporates an array of 4 large electrodes (10 3 20 cm, 3 3 18 cm, 10 3 7.5 cm, and 7 3 14 cm, for a total surface area of 427 cm2) that cover almost the entire quadriceps muscle. In contrast to FNS, maximal stimulation intensity was fixed arbitrarily at 200 mA for all subjects because of the difficulty in obtaining a plateau in twitch peak torque when delivering electrical stimulation over the quadriceps muscle.12,14,19 The twitch recruitment curve was therefore obtained arbitrarily by delivering single pulses at 40, 80, 120, 160, and 200 mA, and all paired stimuli were delivered at 200 mA.
FNS. The femoral nerve was stimulated using a circular self-adhesive electrode (surface 19.6 cm2)
Discomfort. Self-reported discomfort associated with the application of FNS or GQS was evaluated
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GQS.
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FIGURE 1. Representative traces of resting twitches (A), MVC-superimposed and potentiated doublets (B), and submaximal contraction (20% MVC)–superimposed doublets (C) in response to femoral nerve stimulation (gray lines) and garment-based quadriceps stimulation (black lines).
according to a 0–10-cm horizontal visual analog scale (VAS), with 0 5 no discomfort and 10 5 maximum discomfort. Participants were given the VAS immediately after each single pulse of the twitch recruitment curve (discomfort of the Quadriceps Neuromuscular Testing
twitch), after paired stimulation following the MVC trials (discomfort of the potentiated doublet), and after each paired stimuli superimposed to the submaximal voluntary contractions (discomfort of the superimposed doublet). MUSCLE & NERVE
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Data Analysis. The twitch recruitment curve was constructed by plotting twitch peak torque as a function of stimulation intensity (24%, 48%, 72%, 96%, and 120% of the maximal intensity for FNS, and 40, 80, 120, 160, and 200 mA for GQS). Peak torque and time to peak torque (i.e., the main contractile properties) were also quantified from twitch and potentiated doublet traces (both obtained at 120% of the maximal stimulation intensity for FNS and at 200 mA for GQS). Muscle inactivation was estimated by plotting superimposed doublet torque as a function of contraction intensity (20%, 40%, 60%, 80%, and 100% of the MVC torque) as in our previous study.14 For all variables, the average of the 2 consecutive responses obtained in the same conditions was retained.
Normal distribution was verified using the Shapiro–Wilk test. Because all data were normally distributed, they were expressed as mean and SD and were analyzed using paired t-tests or 2way repeated-measures analyses of variance (ANOVAs). One-tailed paired t-tests were used to evaluate differences in MVC torque, twitch peak torque, twitch time to peak torque, potentiated doublet peak torque, potentiated doublet time to peak torque, and discomfort of the potentiated doublet between stimulation modalities (FNS vs. GQS). A first 2 3 5 ANOVA was used to evaluate the effect of stimulation modality (FNS, GQS) and stimulation intensity (24%, 48%, 72%, 96%, and 120% of maximal intensity for FNS, and 40, 80, 120, 160, and 200 mA for GQS) on twitch torque and discomfort from the recruitment curves. A second 2 3 5 ANOVA was used to evaluate the effect of stimulation modality (FNS, GQS) and contraction intensity (20%, 40%, 60%, 80%, and 100% MVC) on superimposed doublet torque and discomfort of the superimposed doublet. In case of significant main effects or interactions, Tukey honestly significant difference post-hoc tests were applied. The threshold for statistical significance was set at P < 0.05. Statistics.
RESULTS Muscle Contractile Properties.
Figure 1A shows the twitch recruitment curves obtained in a representative subject with FNS and GQS. Twitch peak torque was significantly lower for GQS than for FNS at all stimulation intensities (P < 0.01), except the lowest one (Fig. 2). The average difference in twitch peak torque between FNS and GQS was 12.7 6 8.2% at the highest stimulation intensity. Twitch peak torque did not differ significantly between 72%, 96%, and 120% for FNS and between 160 and 200 mA for GQS (i.e., a sort of plateau was attained at 72% and 160 mA, respectively). Both twitch and potentiated doublet peak torque were 120
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FIGURE 2. Twitch peak torque as a function of stimulation intensity for femoral nerve stimulation (FNS) and garmentbased quadriceps stimulation (GQS). Data points are shown as mean value and standard deviation.
significantly lower for GQS than for FNS (Fig. 3A and B; P < 0.001), and both twitch and potentiated doublet time to peak torque were significantly shorter for GQS than for FNS (P < 0.01; Fig. 3C and D). Muscle Inactivation. Superimposed doublet torque was significantly lower for GQS than for FNS at 20% and 40% MVC (P < 0.01), whereas no difference was observed at 60%, 80%, and 100% MVC (Fig. 4). Discomfort. Discomfort of the twitch was significantly lower for GQS than for FNS [233.2%; 95% confidence interval (CI) range for GQS: 0.03–4.57; 95% CI range for FNS: 0.07–5.39], regardless of the stimulation intensity (P < 0.05 for main effect in ANOVA; Fig. 5A). Discomfort of the potentiated doublet was also significantly lower for GQS than for FNS (221.8%; 95% CI range for GQS: 2.17– 5.23; 95% CI range for FNS: 3.26–6.16; P < 0.01; Fig. 5B). Discomfort of the superimposed doublet was significantly lower for GQS than for FNS (225.6%; 95% CI range for GQS: 0.93–4.59; 95% CI range for FNS: 1.47–5.77), regardless of the contraction intensity (P < 0.05 for main effect in ANOVA; Fig. 5C). DISCUSSION
The main findings of this methodological study are that submaximal GQS resulted in similar muscle inactivation estimates compared with supramaximal FNS for contraction intensities >40% MVC, whereas discomfort scores were systematically lower for the former modality. These findings prove the validity of GQS for assessment of quadriceps muscle inactivation despite differences in resting MUSCLE & NERVE
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FIGURE 3. Twitch peak torque (A), potentiated doublet peak torque (B), twitch time to peak torque (C), and potentiated doublet time to peak torque (D) for femoral nerve stimulation (FNS) and garment-based quadriceps stimulation (GQS). The black circles indicate the mean, and the error bars indicate standard deviation.
muscle contractile properties between the 2 stimulation modalities (GQS evoked smaller and faster twitch and doublet responses). FNS (at rest or superimposed on voluntary contractions) is considered to be the optimum modality for assessment of quadriceps neuromuscular function,20 as supramaximal stimulation of the
FIGURE 4. Superimposed doublet torque as a function of contraction intensity for femoral nerve stimulation (FNS) and garment-based quadriceps stimulation (GQS). Data points are shown as mean value and standard deviation. Quadriceps Neuromuscular Testing
nerve trunk results in synchronous recruitment of all motor units. This assumption is evidenced by the consistent presence of a plateau in evoked twitch torque as FNS intensity is progressively increased,14,21 whereas the plateau is not always observed with stimulation of terminal axonal branches,12,14,19 as is the case for GQS. Consistent with these previous observations, our results show lower amplitudes for twitches and potentiated doublets evoked by GQS as compared to FNS for all stimulation intensities, except the lowest. This result confirms that over-the-muscle stimulation may lead to incomplete motor unit recruitment,1,15,16 even when using multiple electrodes that cover the quadriceps muscle almost entirely, as with GQS. It is very likely that some (presumably deep) motor units would be very difficult to recruit with GQS, even at relatively high stimulation intensities. It should, however, be noted that comparable resting twitch and doublet amplitudes were observed for quadriceps muscle stimulation and FNS by some investigators,21,22 even though higher stimulation intensities and different electrode configurations were used compared with our study. The shorter times to peak torque we observed for GQS-evoked twitch and potentiated doublet responses suggest recruitment of fast-contracting MUSCLE & NERVE
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FIGURE 5. Discomfort of the twitch as a function of stimulation intensity (A), discomfort of the potentiated doublet (B), and discomfort of the superimposed doublet as a function of contraction intensity (C) for femoral nerve stimulation (FNS) and garment-based quadriceps stimulation (GQS). Data are shown as mean value and standard deviation.
motor units. This is in agreement with our previous findings obtained when comparing twitches evoked by quadriceps muscle stimulation and FNS,14 and is thought to originate from a predomi122
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nant recruitment of type II muscle fibers with GQS, which have a distribution shown to be higher in superficial than in deeper regions of the anterior thigh muscles.23–25 Surprisingly, these differences in spatial recruitment between GQS and FNS had little or no influence on the estimation of quadriceps muscle inactivation. In fact, our results show similar inactivation levels for GQS and FNS at contraction intensities >40% MVC. Again, these findings are very similar to those obtained in our previous twitch interpolation study14 and are likely attributable to the fact that unrecruited motor units during any given voluntary contraction (those with the highest depolarization threshold) are among the first to be recruited with GQS due to their superficial localization and proximity to the stimulating electrodes.23,24 Our data also confirm recent findings by Bampouras et al.,22 who demonstrated that submaximal paired stimuli (as low as 50% of maximal intensity) delivered by 2 surface electrodes positioned over the quadriceps muscle are sufficiently valid for assessment of muscle inactivation, as stimulus spread to other muscles (including antagonists) is lower compared with higher stimulation intensities. Actually, the use of submaximal (rather than maximal) paired stimuli may be particularly appropriate for assessment of muscle inactivation in individuals who present with large neurological deficits, as submaximal current may lower both the discomfort and the risk of underestimating the level of inactivation.26 As expected, differences in current intensity level between the 2 stimulation modalities (submaximal for GQS vs. supramaximal for FNS) are likely to explain, at least in part, the lower discomfort experienced by our subjects during GQS. It should, however, be noted that absolute current intensity was actually 2-fold higher for GQS (200 mA) than for FNS (95 mA), whereas current density (maximum current intensity/total electrode area) was 10-fold higher for FNS (4.85 mA/cm2) compared with GQS (0.47 mA/cm2) due to different electrode size. Activation of Ad and C nociceptive fibers is the main mechanism underlying the discomfort induced by transcutaneous electrical stimulation.27 Although these nociceptive fibers are located in both the nerve trunk and the dermal–epidermal junction, their density is much higher in the former compared with the latter.28 In addition, the amplitude of nociceptive potentials is well correlated with both stimulation charge and nerve fiber density.29 Stimulation charge density (maximum current intensity 3 pulse duration / total electrode area) delivered to the muscle through the 4 large electrodes with GQS (4.6827 C/cm2) was considerably lower than that delivered to the femoral nerve through the small MUSCLE & NERVE
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electrode (4.8526 C/cm2). Therefore, GQS was unsurprisingly found to generate less discomfort than FNS, in line with previous studies.14,21 Besides the intermodality differences in discomfort scores and recruitment noted earlier, GQS may offer some practical advantages compared with FNS. First, application of the GQS apparel, based on anatomical landmarks and being cablefree (from the electrodes to the garment), is extremely simple and does not require any adjustment, as it is the case with femoral nerve localization. In this respect, GQS also offers a practical advantage in comparison to other over-the-muscle stimulation modalities that require the proper placement of 2 or more electrodes over the anterior thigh muscles after identification of their main motor points. Second, the use of a fixed, although arbitrarily defined, submaximal stimulation intensity for all the subjects reduces considerably the duration of the testing session as compared with individual determination of supramaximal intensity for FNS, which takes at least 10 min. Third, electrode displacement (with respect to the axonal branches) induced by voluntary contractions is certainly less problematic compared with FNS, where the small stimulating electrode is likely to be pushed away from the femoral nerve by the nearby tendon. Taken together, these practical benefits of GQS may favor its clinical implementation for evaluation of short- and long-term changes in neuromuscular function induced by physical exercise (e.g., central fatigue),10,11 and/or pathological conditions (e.g., arthrogenic muscle inhibition).8,9 Owing to its simplicity and its straightforward application, GQS would also be particularly suitable for bedside evaluation of quadriceps muscle function (e.g., in critically ill patients) as well as for multicenter studies. This methodological study has some limitations. We did not evaluate patients with orthopedic or neurological conditions (to avoid imposing burdens on them), who would have displayed higher inactivation scores than the healthy subjects we tested.3,4,8,9 Due to time constraints, we did not verify the validity of GQS for detecting central fatigue. One could, however, conjecture that, for physiologically meaningful reductions in MVC torque of 20–40%, such as those induced by strenuous physical exercise,10 assessment of central fatigue with GQS would be comparable to FNS (based on Fig. 4 results for contraction intensities >40% MVC) and therefore valid. Finally, no attempt was made to increase the GQS intensity beyond 200 mA, to adjust the position of GQS electrodes with respect to individual muscle mass or geometry, or to blind the 2 experimental conditions. Quadriceps Neuromuscular Testing
In conclusion, these findings suggest that GQS can be used with confidence for straightforward assessment of quadriceps muscle inactivation. Although these results were not obtained in patients but in healthy subjects, we suggest that GQS would also be suitable for clinical populations, particularly because of the lower level of discomfort. On the other hand, because resting twitch and potentiated doublet responses were significantly larger with FNS, the validity of GQS for evaluation of muscle contractile properties remains to be ascertained. REFERENCES 1. Maffiuletti NA, Minetto MA, Farina D, Bottinelli R. Electrical stimulation for neuromuscular testing and training: state-of-the art and unresolved issues. Eur J Appl Physiol 2011;111:2391–2397. 2. Millet GY, Martin V, Martin A, Verges S. Electrical stimulation for testing neuromuscular function: from sport to pathology. Eur J Appl Physiol 2011;111:2489–2500. 3. Fitzgerald GK, Piva SR, Irrgang JJ, Bouzubar F, Starz TW. Quadriceps activation failure as a moderator of the relationship between quadriceps strength and physical function in individuals with knee osteoarthritis. Arthritis Rheum 2004;51:40–48. 4. Klein CS, Brooks D, Richardson D, McIlroy WE, Bayley MT. Voluntary activation failure contributes more to plantar flexor weakness than antagonist coactivation and muscle atrophy in chronic stroke survivors. J Appl Physiol (1985) 2010;109:1337–1346. 5. de Haan A, de Ruiter CJ, van der Woude LH, Jongen PJ. Contractile properties and fatigue of quadriceps muscles in multiple sclerosis. Muscle Nerve 2000;23:1534–1541. 6. Kent-Braun JA, Le Blanc R. Quantitation of central activation failure during maximal voluntary contractions in humans. Muscle Nerve 1996;19:861–869. 7. Gandevia SC. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 2001;81:1725–1789. 8. Hurley MV, Jones DW, Newham DJ. Arthrogenic quadriceps inhibition and rehabilitation of patients with extensive traumatic knee injuries. Clin Sci (Lond) 1994;86:305–310. 9. Rice DA, McNair PJ. Quadriceps arthrogenic muscle inhibition: neural mechanisms and treatment perspectives. Semin Arthritis Rheum 2010;40:250–266. 10. Millet GY, Lepers R. Alterations of neuromuscular function after prolonged running, cycling and skiing exercises. Sports Med 2004;34: 105–116. 11. Zwarts MJ, Bleijenberg G, van Engelen BG. Clinical neurophysiology of fatigue. Clin Neurophysiol 2008;119:2–10. 12. Behm DG, St-Pierre DM, Perez D. Muscle inactivation: assessment of interpolated twitch technique. J Appl Physiol (1985) 1996;81:2267– 2273. 13. Folland JP, Williams AG. Methodological issues with the interpolated twitch technique. J Electromyogr Kinesiol 2007;17:317–327. 14. Place N, Casartelli N, Glatthorn JF, Maffiuletti NA. Comparison of quadriceps inactivation between nerve and muscle stimulation. Muscle Nerve 2010;42:894–900. 15. Bickel CS, Gregory CM, Dean JC. Motor unit recruitment during neuromuscular electrical stimulation: a critical appraisal. Eur J Appl Physiol 2011;111:2399–2407. 16. Gregory CM, Bickel CS. Recruitment patterns in human skeletal muscle during electrical stimulation. Phys Ther 2005;85:358–364. 17. Feil S, Newell J, Minogue C, Paessler HH. The effectiveness of supplementing a standard rehabilitation program with superimposed neuromuscular electrical stimulation after anterior cruciate ligament reconstruction: a prospective, randomized, single-blind study. Am J Sports Med 2011;39:1238–1247. 18. Paessler HH. Emerging techniques in orthopedics: advances in neuromuscular electrical stimulation. Am J Orthop 2012;41:1–8. 19. Hanchard NC, Williamson M, Caley RW, Cooper RG. Electrical stimulation of human tibialis anterior: (A) contractile properties are stable over a range of submaximal voltages; (B) high- and lowfrequency fatigue are inducible and reliably assessable at submaximal voltages. Clin Rehabil 1998;12:413–427. 20. Maffiuletti NA. Assessment of hip and knee muscle function in orthopaedic practice and research. J Bone Joint Surg Am 2010;92: 220–229. 21. Rodriguez-Falces J, Maffiuletti NA, Place N. Spatial distribution of motor units recruited during electrical stimulation of the quadriceps muscle versus the femoral nerve. Muscle Nerve 2013;48:752–761.
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