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J Appl Physiol 106: 701-710, 2009. First published August 28, 2008; doi:10.1152/japplphysiol.01051.2007
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HIGHLIGHTED TOPIC
The Physiology and Pathophysiology of the Hyperbaric and Diving Environments

Comparison of electrical and magnetic stimulations to assess quadriceps muscle function

Samuel Verges,1 Nicola A. Maffiuletti,2 Hugo Kerherve,3 Nicolas Decorte,1 Bernard Wuyam,1 and Guillaume Y. Millet3

1REX-S laboratory, Joseph Fourier University and Exercise Research Unit, Grenoble University Hospital, Grenoble, France; 2Neuromuscular Research Laboratory, Schulthess Clinic, Zurich, Switzerland; 3 Exercise Physiology Laboratory, Jean Monnet University, Saint-Etienne, France

Submitted 20 October 2007 ; accepted in final form 19 August 2008


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
This study aimed to 1) compare electrical and magnetic stimulations for quadriceps muscle function assessment, and 2) ascertain whether the ratios of the second twitch elicited by supramaximal electrical and magnetic femoral nerve stimulation at 10 and 100 Hz (T210:100) and the total twitch force elicited by the same types of stimulations (Fpaired10:100) are equivalent to the standard low- to high-frequency force ratio associated with submaximal electrical tetanic stimulations (Ftet10:100). Quadriceps force and vastus lateralis EMG were recorded at rest (n = 21 subjects), immediately after, and 30 min after a 30-min downhill run (n = 10) when 1) supramaximal electrical nerve stimulation (ENS), 2) magnetic nerve stimulation (MNS) and 3) submaximal electrical muscle stimulation (EMS) were delivered in random order at 1 (single stimulation), 10, and 100 Hz (paired stimulations). Ten- and 100-Hz 500-ms tetani were also evoked with EMS to determine Ftet10:100. Before exercise, contractile properties with single and paired stimulations were similar for ENS and MNS (all intraclass correlation coefficients k > 0.90), but smaller for EMS (P < 0.001). M-wave characteristics were also similar for ENS and MNS (all k > 0.90). After exercise, changes in all parameters did not differ between methods. With fatigue, the changes in Ftet10:100 were inconsistently correlated with the changes in T210:100 (r2 = 0.24–0.73, P = 0.002–0.15) but better correlated with the changes in Fpaired10:100 (immediately after exercise: r2 = 0.80–0.83, P < 0.001; 30 min after exercise: r2 = 0.46–0.82, P = 0.001–0.03). We conclude that ENS and MNS provide similar quadriceps muscle function assessment, while Fpaired10:100 is a better index than T210:100 of low- to high-frequency fatigue of the quadriceps in vivo.

nerve stimulation; M-wave; contractile properties; low-frequency fatigue

TO ASSESS MUSCLE FUNCTION, artificial stimulation is widely used both in research and clinical settings. Many studies have specifically investigated the quadriceps femoris because it is a primary locomotor muscle. Percutaneous electrical stimulation was used originally, mainly by placing large stimulating electrodes over the muscle belly (electrical muscle stimulation, EMS), but also by apposing a small cathode over the femoral nerve at the femoral triangle (electrical nerve stimulation, ENS). In 1996, Polkey et al. (22) described a new technique to stimulate the quadriceps by using magnetic nerve stimulation (MNS). By apposing the stimulating coil over the femoral triangle, the authors demonstrated that supramaximal stimulation of the femoral nerve was feasible and well tolerated. To our knowledge, although electrical and magnetic stimulations were used in many different studies to investigate muscle function in both unfatigued and fatigued states, systematic comparisons of these two techniques were performed for phrenic nerve stimulation only, showing different levels of twitch transdiaphragmatic pressure (14, 30). Therefore, whether electrical (ENS and EMS) and magnetic stimulations provide similar quadriceps muscle function assessment remains to be investigated.

Peak twitch force was shown to be a valuable measurement to assess skeletal muscle function (8, 15, 17, 18). However, stimulation trains at different frequencies can also be applied to better assess muscle function and fatigue under conditions more similar to voluntary contractions. Furthermore, tetanic stimulations at different frequencies enable the calculation of low- to high-frequency force ratios which in turn can be used, for example, to distinguish low- and high-frequency fatigue (8). The gold standard to assess low and high frequency forces is the use of supramaximal trains (8). However, tetanic nerve stimulations induce discomfort and are limited to healthy and motivated subjects (18) and not suitable for clinical practice (17). Our group (18) showed that low- to high-frequency force ratio measured during stimulation trains with submaximal EMS as commonly used (see for instance Refs. 4, 6, 12, 26, 28) provide similar assessment of fatigue after exercise compared with supramaximal ENS. Nevertheless, because most magnetic stimulators do not deliver stimulation trains, some authors evaluated the use of paired stimulations as a surrogate for stimulation trains to assess the relative contribution of low and high frequencies to force output as well as induction and recovery of contractile fatigue. By using electrical stimulation of the phrenic nerve in human and of isolated rat diaphragmatic strips, Yan et al. (31) showed that the force evoked by paired stimulations can be viewed as the sum of two successive responses and that the ratio of the second twitch (T2) obtained by subtracting the force response to a single twitch from the force response to paired stimulations at 10 Hz over 100 Hz (T210:100) may provide similar information as tetanic force at 10 Hz over 100 Hz (Ftet10:100). Paired stimulations were used in subsequent studies to detect low and high frequency fatigue (1, 2, 11, 15, 23, 24), but to our knowledge paired stimulations have never been compared with tetanic stimulations for quadriceps function assessment.

We aimed to compare the outcomes of electrical and magnetic stimulations before and after an eccentric exercise to establish the degree of agreement between different methods and indices commonly used to assess quadriceps muscle function. We systematically examined quadriceps force and vastus lateralis M-wave responses obtained with ENS, MNS, and EMS with either single or paired stimulations. Moreover, we compared the T210:100 ratio obtained with paired stimuli via ENS, MNS, and EMS to the Ftet10:100 ratio obtained with tetanic quadriceps stimulation via submaximal EMS as commonly performed in the literature (e.g., Refs. 4, 6, 12, 26, 28). We hypothesized that 1) ENS and MNS would provide similar assessment of the quadriceps function in both unfatigued and fatigued states, and 2) T210:100 ratio would provide similar information regarding quadriceps low-frequency fatigue compared with Ftet10:100 ratio.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Subjects

Twenty-one healthy and physically active male subjects completed the study. The average (± SD) age, body mass, and height were 30 ± 6 y, 78 ± 7 kg, and 181 ± 6 cm, respectively. The study was approved by the local ethics committee and performed according to the Declaration of Helsinki. All subjects gave their written informed consent to participate in the study.

Experimental Setup

All the assessments were performed on the right quadriceps femoris muscle under isometric conditions. Subjects lay supine on a table with the right knee joint angle set at 90° of flexion. A noncompliant strap connected to a strain gauge (SBB 200 kg, Tempo Technologies, Taipei, Taiwan) was attached around the subject's shank, 3–5 cm above the tip of the lateral malleoli. The subjects were secured to the table with noncompliant straps to minimize body movement. Subjects were at rest for at least 20 min before the first measurements, permitting skin preparation, electrode placing, and determination of the stimulation intensities (see Electrical Nerve Stimulation). The experimental setup and stimulation protocol are described in Fig. 1. Three single stimulations were first delivered via ENS, MNS, and EMS, in a random order. The same procedure was repeated for paired stimulations at 10 Hz (100-ms interstimulus interval) and then at 100 Hz (10-ms interstimulus interval). Afterward, three stimulation trains at 10 Hz and three trains at 100 Hz were delivered via EMS. All stimulations were separated by 20-s resting intervals. Lastly, the subjects performed three maximal voluntary contractions (MVC) to assess MVC force. Subjects were instructed to reach maximal force in 1 s and then to maintain this level for 4 s while receiving strong verbal encouragements. No visual feedback was provided.


Figure 1
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  		Fig. 1. A: Experimental setup: subject was secured to the table with noncompliant straps, and cut pad was placed underneath right thigh to allow biceps femoris electromyographic electrode placement. B: Stimulation protocol: single (1 Hz) and paired (10 Hz and 100 Hz) stimulations were delivered via electrical nerve stimulation (ENS), magnetic nerve stimulation (MNS), and electrical muscle stimulation (EMS). Then, 500-ms stimulation trains at 10 Hz and 100 Hz were delivered with EMS (EMStet). Finally, maximal voluntary contractions (MVC) were performed, followed by single stimulations (1 Hz) with ENS, MNS, and EMS. See MATERIALS AND METHODS for details. *Pre-post exercise measurements only.

 
All subjects were investigated in the unfatigued state. Ten subjects were also assessed immediately after and 30 min after a 30-min downhill run performed at a speed of 10 km/h with a 20% negative slope on a motorized treadmill (S 2500, Tecmachine, Andrezieux-Boutheon, France) (18). Because potentiated twitches were shown to be more sensitive to fatigue than unpotentiated twitches (13), each MVC was followed by three single stimulations to obtain potentiated twitches, which were delivered every 4 s via ENS, MNS, and EMS, in a random order.

Electrical Nerve Stimulation

ENS was delivered percutaneously to the femoral nerve by a cathode electrode (20-mm diameter) pressed in the femoral triangle, 3–5 cm below the inguinal ligament. The anode, a 10.2-cm x 5.2-cm gel pad electrode (Compex SA, Ecublens, Switzerland), was located over the gluteal fold. For both single and paired stimulations, square-wave pulses (1-ms duration) were produced via a high-voltage (maximal voltage 400 V) constant-current stimulator (Digitimer DS7, Hertfordshire, UK). For all stimulus modalities, stimulation intensity corresponded to ~120% of the optimal intensity (range 20–90 mA), i.e., the stimulus intensity at which the maximal amplitude of both twitch force and concomitant vastus lateralis M-wave (see Electromyographic Recordings) were reached.

Magnetic Nerve Stimulation

Femoral nerve stimulation was performed with a 45-mm figure-of-eight coil powered by two linked Magstim 200 stimulators (peak magnetic field strength 2.5 T, stimulation duration 0.1 ms; Magstim, Whitland, Dyfed, United Kingdom). The linking circuitry (Bistim Module, Magstim) was capable of precisely controlling the interstimulus interval between 1 and 999 ms to an accuracy of within 0.05 ms. One stimulator was used for single stimulations, while both stimulators were used for paired stimulations. All stimuli were given at maximum stimulator output (22). The stimulating coil head was positioned high in the femoral triangle just lateral to the femoral artery; the best spot allowing the maximal force and concomitant vastus lateralis M-wave was determined with minor adjustments and then marked on the skin for the remainder of the experiment.

Electrical Muscle Stimulation

EMS was delivered percutaneously via two 5.1-cm x 5.1-cm gel pad electrodes (Compex SA) placed on the motor point of the vastus lateralis and vastus medialis muscles and one 5.1-cm x 10.2-cm dispersive electrode positioned proximally, ~5 cm below the femoral triangle (see Fig. 1A). For both single and paired stimulations, square-wave pulses (1-ms duration) were produced via the same constant-current stimulator as for ENS. Individual stimulation intensity was progressively increased until peak twitch force attained 50% of the peak twitch force obtained via ENS (range 65–100 mA). For stimulation trains, 500-ms tetani (EMStet) were delivered, since this duration allows a force plateau to be reached (18).

Electromyographic Recordings

The electromyographic (EMG) signal was recorded from the right vastus lateralis (as a surrogate for quadriceps muscles, see Ref. 20) and biceps femoris muscles (as a surrogate for antagonist hamstring muscles) with two pairs of silver chloride surface electrodes of 20 mm diameter (universal ECG electrode, Control Graphic Medical, Brie Comte Robert, France) during ENS and MNS (electromyographic signals are not available during EMS due to interference with the electrical stimulation). Low resistance (< 10 k{Omega}) between the two electrodes was obtained by light abrasion of the skin and cleaning with alcohol. Recording electrode locations were based on SENIAM recommendations (10) with an interelectrode distance of 25 mm. The reference electrode was fixed over the patella. Electromyographic signals were amplified (EISA 16–4, Freiburg, Germany) with a bandwidth frequency ranging from 10 Hz to 1 kHz (common mode rejection ratio = 90 dB, gain = 1,000). Electromyographic data together with force signals were digitized online at a sampling frequency of 2,000 Hz and recorded by acquisition card (DAQCard-6062E, National Instruments, Austin, Texas), administered by the Imago software developed under Labview (National Instruments).

Data Analysis

The following parameters were calculated from the mean force response obtained for each type of stimulation (i.e., the average of the three single or paired stimulations): peak force; time to peak force, i.e., the time elapsed between the twitch onset and the peak force; and maximal rate of force development (MRFD) and relaxation (MRFR), i.e., respectively, the highest and the lowest value of the first derivative of the force signal. The following parameters were calculated from the M-wave traces: peak-to-peak duration, peak-to-peak amplitude, and area. These force and electromyographic parameters were calculated to assess any difference in contractile and M-wave characteristics between stimulation modalities.

The effect of the interstimulus interval on the amplitude of the force elicited by the second stimulus (T2) was obtained by digitally subtracting the mean force response of the single twitches from the mean of the paired responses at a given interstimulus interval (21, 31). The T210:100 was obtained by division of the T2 force response at 10 Hz by the T2 force response at 100 Hz. The T210:100 ratios obtained with ENS, MNS, and EMS were compared with the ratio of the tetanic forces measured with EMStet for stimulation trains at 10 Hz and 100 Hz (Ftet10:100). The ratios of paired stimulation peak forces at 10 Hz over 100 Hz (Fpaired10:100) were also compared with Ftet10:100.

All descriptive statistics presented are mean values ± SD. Each variable was compared between stimulation methods (ENS, MNS, EMS) by means of a two-factor ANOVA with repeated measures (methods x stimulation frequencies or methods x time). When significant main effects were found, the Fischer's p-test was used for post hoc analysis. To quantify the agreement between the measurements obtained with the different stimulation techniques (ENS, MNS, EMS) when no statistical difference was observed, intraclass correlation coefficients and Bland-Altman plots (3) were used. Intraclass correlation coefficients (type 2,1; k) were calculated with a two-way random effects model with single-measure reliability in which variance over the repeated session is considered (25). Pearson's product-moment correlations were used to assess the agreement between Ftet10:100 and T210:100 ratios and between Ftet10:100 and Fpaired10:100. Fisher's R-to-Z test was used to determine the statistical significance of the correlations. All statistical calculations were performed on standard statistics software (Statview 5.0, SAS Institute, Cary, North Carolina). Significance was set at P < 0.05.


   RESULTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Force and electromyographic recordings for ENS, MNS, and EMS are shown in Figs. 2 and 3 from one representative subject.


Figure 2
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  		Fig. 2. Quadriceps force recordings from one representative subject for ENS (A), MNS (B), and EMS (C). Tetanic (EMStet, D) force traces at high and low frequencies are also shown. 1 Hz, single stimulation (solid line); 10 Hz, paired stimulations with 100-ms interval (dotted line); 100 Hz, paired stimulations with 10-ms interval (dashed line); T2 10 Hz, second twitch of paired stimulations with 100-ms interval (dash-dot); T2 100 Hz, second twitch of paired stimulations with 10-ms interval; (dash-dot-dot); train 10 Hz, stimulation train at 10 Hz; train 100 Hz, stimulation train at 100 Hz. See MATERIALS AND METHODS for further details.

 

Figure 3
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  		Fig. 3. Vastus lateralis (solid line) and biceps femoris (dotted line) electromyographic responses for ENS (A, B, C) and MNS (D, E, F) from one representative subject. A and D relate to single stimulations (1 Hz); B and E relate to paired stimulations with 100-ms interval (10 Hz); C and F relate to paired stimulations with 10-ms interval (100 Hz). Large biceps femoris electromyographic responses in panels B, C, E and F are artifacts due to second stimulations.

 
Measurements in the Unfatigued State (n = 21)

Peak forces.   Mean quadriceps peak forces for ENS, MNS, and EMS are shown in Fig. 4. Similar quadriceps forces were obtained with ENS and MNS (1 Hz, k = 0.91; 10 Hz, k = 0.94; 100 Hz, k = 0.94), while EMS induced significantly smaller forces compared with both ENS and MNS. Peak forces during ENS, MNS, and EMS were: 20 ± 5%, 19 ± 5%, and 10 ± 3% of MVC at 1 Hz; 34 ± 8%, 33 ± 9%, and 18 ± 4% of MVC at 10 Hz; and 41 ± 7%, 41 ± 8%, and 23 ± 4% of MVC at 100 Hz, respectively. Peak forces during EMStet were 23 ± 6% and 57 ± 14% of MVC at 10 and 100 Hz, respectively. Figure 5 shows Bland-Altman plots of individual peak forces obtained with ENS and MNS at 1, 10, and 100 Hz.


Figure 4
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  		Fig. 4. Quadriceps peak forces associated with single and paired stimulations with ENS, MNS, and EMS. Peak forces associated with tetanic EMS (EMStet) at low and high frequency are also shown. Values are means ± SD. 1 Hz, single stimulation; 10 Hz, paired stimulations with 100-ms interval; 100 Hz, paired stimulations with 10-ms interval. *Significantly different from ENS and MNS; # significantly different from ENS, MNS, and EMS.

 

Figure 5
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  		Fig. 5. Bland-Altman plots for quadriceps peak forces associated with ENS and MNS. Lowest and highest horizontal dashed lines represent 95% limits of agreements (random error), whereas middle dashed line represents mean difference between peak forces obtained with ENS and MNS (systematic bias). A: 1 Hz, single stimulation; B: 10 Hz, paired stimulations with 100-ms interval; C: 100 Hz, paired stimulations with 10-ms interval.

 
T2 peak forces at 10 Hz (ENS: 203.2 ± 50.7 N; MNS: 188.9 ± 52.0 N; EMS: 114.3 ± 30.4 N) and 100 Hz (ENS: 197.8 ± 35.8 N; MNS: 189.9 ± 44.6 N; EMS: 121.1 ± 30.7 N) were similar for ENS and MNS (10 Hz: k = 0.93; 100 Hz: k = 0.90) and smaller for EMS compared with ENS and MNS (P < 0.001). T210:100 ratio tended to be higher (P = 0.06) for ENS (1.03 ± 0.15) and MNS (1.03 ± 0.18) compared with EMS (0.96 ± 0.18). Fpaired10:100 ratio was significantly higher for ENS (0.81 ± 0.08) and MNS (0.80 ± 0.08) compared with EMS (0.77 ± 0.09; P < 0.01). For all types of stimulation, T210:100 was significantly higher than Fpaired10:100 (all P < 0.001).

Ftet10:100 (0.43 ± 0.08) was significantly correlated with T210:100 with ENS (r2 = 0.24, P = 0.03) and EMS (r2 = 0.50, P < 0.001) but not with MNS (r2 = 0.05, P = 0.35). On the other hand, Ftet10:100 was significantly correlated with Fpaired10:100 with ENS (r2 = 0.42, P = 0.002), MNS (r2 = 0.34, P = 0.007), and EMS (r2 = 0.61, P < 0.001).

Contractile properties.   Quadriceps contractile properties associated with single and paired stimulations are shown in Table 1. Time to peak force, MRFD, and MRFR were similar for ENS and MNS (1 Hz: k = 0.93, 0.94, and 0.95, respectively; 10 Hz: k = 0.94, 0.94, and 0.95, respectively; 100 Hz: k = 0.93, 0.98, and 0.92, respectively), while MRFD and MRFR were significantly lower for EMS compared with both ENS and MNS.


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  		Table 1. Quadriceps contractile properties associated with single and paired stimulations in the unfatigued state

 
M-wave characteristics.   Vastus lateralis M-wave duration (ENS: 9.5 ± 2.4 ms; MNS 9.4 ± 2.3 ms; k = 0.99), amplitude (ENS: 54.8 ± 15.4 mV; MNS: 54.3 ± 15.0 mV; k = 0.98), and area (ENS: 0.40 ± 0.13 mV·s; MNS: 0.40 ± 0.13 mV·s; k = 0.98) were similar for ENS and MNS. Figure 6 shows Bland-Altman plots of individual M-wave characteristics obtained with ENS and MNS. Biceps femoris M-waves were essentially undetectable during both ENS and MNS (Fig. 3).


Figure 6
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  		Fig. 6. Bland-Altman plots for vastus lateralis M-waves characteristics associated with ENS and MNS. A: M-wave duration; B: M-wave amplitude; C: M-wave area.

 
Measurements in the Fatigued State (n = 10)

Contractile properties associated with single and paired stimulations as well as M-wave characteristics for ENS, MNS, and EMS before and after exercise are shown in Fig. 7, Table 2, and Table 3, respectively. After exercise, peak force, time to peak force, M-wave duration, and area were significantly reduced, while MRFD, MRFR, and M-wave amplitude were not significantly modified. No differences were observed between ENS and MNS parameters, while peak force, MRFD, and MRFD were significantly lower for EMS compared with ENS and MNS. Postexercise changes expressed as a percentage of pre-exercise values were not significantly different between methods (all P > 0.05).


Figure 7
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  		Fig. 7. Quadriceps peak forces for ENS, MNS, and EMS before (Pre), immediately after (Post), and 30 min after (Post30) exercise (as percentage of Pre value, n = 10). Values are means ± SD. A: 1 Hz, single stimulation (unpotentiated twitch); B: 1 Hzpot, single stimulation (potentiated twitch); C: 10 Hz, paired stimulations with 100-ms interval; D: 100 Hz, paired stimulations with 10-ms interval. All peak forces were significantly reduced at Post and Post30 compared with Pre.

 

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  		Table 2. Quadriceps contractile properties associated with single and paired stimulations

 

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  		Table 3. Vastus lateralis M-wave characteristics for ENS and MNS

 
T210:100 obtained via ENS, MNS, and EMS as well as Ftet10:100 were significantly reduced after exercise (Fig. 8). The reduction in T210:100 for ENS and MNS was significantly smaller than the reduction in T210:100 for EMS. Also, the reduction in Ftet10:100 after exercise was significantly higher than the reduction in T210:100 for ENS, MNS, and EMS. With all types of stimulation, Fpaired10:100 was reduced after exercise to an extent similar to T210:100 (all P > 0.1) but less than Ftet10:100 (all P < 0.001).


Figure 8
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  		Fig. 8. Ratio of T2 peak forces measured at 10 and 100 Hz for ENS, MNS, and EMS as well as ratio of peak forces measured at 10 and 100 Hz via tetanic EMS (EMStet) before (Pre), immediately after (Post), and 30 min after (Post30) exercise (n = 10). Values are means ± SD. A: absolute values; B: values as percentage of Pre values. All values were significantly lower at Post and Post30 compared with Pre. *Significantly different compared with ENS and MNS; # significantly different compared with ENS, MNS, and EMS.

 
Correlations between postexercise changes in Ftet10:100 and postexercise changes in T210:100 or Fpaired10:100 are shown in Table 4. Immediately after exercise, the change in Ftet10:100 was significantly correlated with the changes in T210:100 for MNS and EMS as well as with the changes in Fpaired10:100 for all types of stimulation. Thirty minutes after exercise, changes in Ftet10:100 were not significantly correlated with changes in T210:100 but were still significantly correlated with Fpaired10:100 for all types of stimulation.


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  		Table 4. Correlations between the postexercise changes in ratios of peak forces

 

   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
ACKNOWLEDGMENTS
 REFERENCES
 
To our knowledge, this is the first study to compare electrical and magnetic stimulation methods to assess quadriceps function. Force and M-wave characteristics associated with single and paired stimulations were similar for ENS and MNS, both before and after a fatiguing exercise. Also, the exercise-induced reduction in Ftet10:100 did not consistently correlate with the reductions in T210:100 for the three stimulation modalities. Rather, while the amplitude of the changes are different, the reduction in Ftet10:100 after exercise was better related to the reduction in the low- to high-frequency ratio calculated from peak forces during paired stimulations (Fpaired10:100).

Magnetic Stimulation to Assess Quadriceps Muscle Function

The use of MNS was described ten years ago as a new method to assess quadriceps function. Since then, it has been widely used in research settings as well as in clinical practice (1, 9, 15, 17, 24, 29). However, the specificity of magnetic stimulation may present some limitations for muscle function assessment. First, stimulation supramaximality, i.e., the fact that further increase in stimulation intensity gives no further response in both electrical and mechanical response of the muscle, is critical when artificial stimulation is used to assess muscle function. Due to limited power output of commercially available magnetic stimulators, supramaximal stimulation may be difficult to achieve, since maximal muscle response may be reached at or near the maximal power output of the stimulator (9). Second, because the magnetic field is relatively wide and goes deep into the tissue (17), stimulation is less focalized and therefore risks of coactivation may arise. Wragg et al. (30), for example, reported significantly smaller twitch transdiaphragmatic pressure with electrical compared with magnetic phrenic nerve stimulation, potentially due to coactivation of other muscle groups with the latter modality (14). Conversely, with ENS, supramaximal stimulation can be easily achieved because stimulation intensity can be increased without technical limitations. Moreover, the electric field can be selectively applied to the femoral nerve by pressing a small electrode in the femoral triangle. By comparing ENS to MNS, the present results showed that quadriceps force and vastus lateralis M-wave characteristics of single and paired stimulations were very similar for ENS and MNS, as shown by k values > 0.90 and Bland-Altman analysis (Figs. 4 and 5). Therefore, despite the fact that supramaximality of MNS in the present study was verified only a posteriori, these findings confirm that stimulation at 100% of the magnetic stimulator power output can be supramaximal as previously assumed in our and other laboratories (7, 15, 22, 24, 29). Moreover, the quasi-absence of biceps femoris electromyographic activity during both ENS and MNS suggested that potential coactivation of the antagonist muscles did not affect contractile properties assessment.

Furthermore, changes in force and M-wave characteristics via single and paired stimulations following exercise were similar for ENS and MNS, suggesting that both methods are equally sensitive to exercise-induced fatigue. A critical point when twitches are used to assess muscle fatigue following exercise is the confounding effect of potentiation, i.e., the increase in twitch force following voluntary contractions (16, 22). In the present study, stimulations performed immediately after running were potentially influenced by the potentiation effect of exercise. However, we believe that this potential effect does not influence our results regarding comparisons of different quadriceps stimulations modalities, because 1) stimulation modalities were performed in random order and were therefore similarly influenced by the exercise-induced potentiation, 2) comparisons between stimulation modalities provide similar results immediately after exercise and 30 min after exercise (i.e., when the effect of potentiation was abolished), and 3) comparison of potentiated single stimulations also shows no difference between ENS and MNS. Hence, the present results indicated that ENS and MNS provide similar outcomes regarding quadriceps muscle function. While subjects' spontaneous reports also indicated no major discomfort with ENS and MNS, MNS may have the advantage of being easier to handle in clinical practice (17). Also, while voluntary muscle activation was not evaluated in the present study, recent results suggest that electrical and magnetic stimulations of the quadriceps provide similar results regarding quadriceps activation levels (19). Thus these results confirm that magnetic stimulation is an attractive tool to assess muscle function both for clinical and research purposes and further developments, as increase in maximal stimulator power output or repetitive stimulations (27) may improve the potential of this technique.

Paired Stimulations to Assess Quadriceps Muscle Function

The use of paired stimulation to deduce the low- to high-frequency force and fatigue in isolated muscle is long established (5). Figure 4 shows that the increment in force when stimulation frequency increases differ when measured with paired stimulations or stimulation train. Previous studies showed indeed that force-frequency relationships depend on the number of impulses in the train (31). Despite these differences, paired stimulations on muscles in vivo have been proposed as a surrogate for stimulation trains to assess force-frequency ratio (21, 31). Yan et al. (31) suggested that the ratio of T2 at 10 Hz over 100 Hz (T210:100) may provide similar information compared with tetanic force at 10 Hz over 100 Hz (Ftet10:100). These authors indeed observed that T210:100 and Ftet10:100 ratios measured before and after fatiguing contractions were highly correlated in isolated rat diaphragmatic strips. However, paired stimuli and stimulation trains were not compared on the diaphragm in vivo, because phrenic nerve stimulation trains are very painful. In the present study, T210:100 and Ftet10:100 were compared on the quadriceps in vivo. In the unfatigued state, although values comparable to previous studies were obtained (21, 24, 31), correlation between these ratios were weak when T210:100 was measured via ENS and MNS (r2 < 0.3) and moderate when T210:100 was measured via EMS (r2 = 0.50). After exercise, the reduction in T210:100 was smaller than the reduction in Ftet10:100. Also, exercise-induced changes in T210:100 and Ftet10:100 were inconsistently correlated, with significant correlations immediately after exercise with T210:100 measured via MNS and EMS only but no significant correlations 30 min after exercise. Therefore, these results taken as a whole do not confirm that T210:100 and Ftet10:100 ratios are equivalent to assess low- to high-frequency force and fatigue of the human quadriceps in vivo. One potential reason for this difference may be that T210:100 for ENS and MNS was calculated from supramaximal stimulations, while EMS was delivered at submaximal intensities. Therefore, one may argue that Ftet10:100 ratios should have been measured with supramaximal femoral nerve stimulation trains. However, supramaximal femoral nerve train stimulations are very painful. Moreover, our group (18) showed that postexercise changes in low- to high-frequency ratio measured with supramaximal ENS and submaximal EMS (as in the present study) were similar, indicating that low- to high-frequency ratio of stimulation trains with both techniques provide similar assessment of fatigue. Also, the correlation between the changes in T210:100 measured via submaximal EMS and the changes in Ftet10:100 from before to 30 min after exercise was not significant (Table 4). Therefore, the differences observed between T210:100 and Ftet10:100 in the present study were probably due to factors other than the supramaximal characteristic of the stimulations. Interestingly, both resting values and postexercise changes in Ftet10:100 were better correlated with postexercise changes in Fpaired10:100 than in T210:100 (Table 4). These results suggest that postexercise percentage changes in low- to high-frequency ratio of peak forces for paired stimulations is a better surrogate for stimulation trains than T2 ratio to assess low-frequency fatigue in the human quadriceps in vivo. In other words, while amplitude changes (both absolute and relative) are different between Ftet10:100 and Fpaired10:100 after exercise, low-frequency fatigue detection can be performed with Fpaired10:100. This result is important in a clinical perspective, as stimulation trains inducing discomfort in patients and unfeasible with most of the available magnetic stimulators could be replaced by paired stimulations while providing similar information.

In conclusion, the present study indicated that ENS and MNS provided similar force and M-wave responses to single and paired stimulations both in the unfatigued and fatigued quadriceps muscle. Therefore, contrary to other muscle groups like inspiratory muscles, both stimulation modalities can be considered as equivalent for quadriceps muscle function assessment. While previous results on isolated muscles suggest that T210:100 and Ftet10:100 may be equivalent to assess low- to high-frequency force, inconsistent correlations between these two ratios were observed in the present study, and therefore it cannot be confirmed on human muscle in vivo that T210:100 can be used as a surrogate to tetanus for low- to high-frequency force and fatigue assessment. A simple method based on low- to high-frequency ratio of peak forces may be more appropriate.


   ACKNOWLEDGMENTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
REFERENCES
 
We thank the subjects for time and effort dedicated to this study. We are also grateful to Mrs. Benjie R. Bartos for the English revision of the manuscript.


   FOOTNOTES
 

Address for reprint requests and other correspondence: Vergès Samuel; UF Recherche sur l'Exercice, Hôpital Sud; Ave. Kimberley; 38 434 Echirolles; France (e-mail: sverges{at}chu-grenoble.fr)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


   REFERENCES
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 

  1. Amann M, Romer LM, Pegelow DF, Jacques AJ, Hess CJ, Dempsey JA. Effects of arterial oxygen content on peripheral locomotor muscle fatigue. J Appl Physiol 101: 119–127, 2006.[Abstract/Free Full Text]
  2. Babcock MA, Pegelow DF, Taha BH, Dempsey JA. High frequency diaphragmatic fatigue detected with paired stimuli in humans. Med Sci Sports Exerc 30: 506–511, 1998.[Web of Science][Medline]
  3. Bland JM, Altman DG. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1: 307–310, 1986.[CrossRef][Web of Science][Medline]
  4. Child RB, Brown SJ, Day SH, Saxton JM, Donnelly AE. Manipulation of knee extensor force using percutaneous electrical myostimulation during eccentric actions: effects on indices of muscle damage in humans. Int J Sports Med 19: 468–473, 1998.[Web of Science][Medline]
  5. Cooper S. The isometric responses of mammalian muscles. J Physiol 69: 377–385, 1930.[Free Full Text]
  6. Davies CT, Thompson MW. Physiological responses to prolonged exercise in ultramarathon athletes. J Appl Physiol 61: 611–617, 1986.[Abstract/Free Full Text]
  7. Decorte N, Verges S, Flore P, Guinot M, Wuyam B. Effects of acute salbutamol inhalation on quadriceps force and fatigability. Med Sci Sports Exerc 40: 1220–1227, 2008.[CrossRef][Web of Science][Medline]
  8. Edwards RH, Hill DK, Jones DA, Merton PA. Fatigue of long duration in human skeletal muscle after exercise. J Physiol 272: 769–778, 1977.[Abstract/Free Full Text]
  9. Hamnegard CH, Sedler M, Polkey MI, Bake B. Quadriceps strength assessed by magnetic stimulation of the femoral nerve in normal subjects. Clin Physiol Funct Imaging 24: 276–280, 2004.[CrossRef][Web of Science][Medline]
  10. Hermens H, Freriks B. (editors). The state of the art on sensor and sensor placement procedures for surface electromyography: a proposal for sensor placement procedures. Enschede, The Netherlands: Roessingh Research and Development, 1997.
  11. Jeffery Mador M, Kufel TJ, Pineda LA. Quadriceps and diaphragmatic function after exhaustive cycle exercise in the healthy elderly. Am J Respir Crit Care Med 162: 1760–1766, 2000.[Abstract/Free Full Text]
  12. Kesar T, Binder-Macleod S. Effect of frequency and pulse duration on human muscle fatigue during repetitive electrical stimulation. Exp Physiol 91: 967–976, 2006.[Abstract/Free Full Text]
  13. Kufel TJ, Pineda LA, Mador MJ. Comparison of potentiated and unpotentiated twitches as an index of muscle fatigue. Muscle Nerve 25: 438–444, 2002.[CrossRef][Web of Science][Medline]
  14. Laghi F, Harrison MJ, Tobin MJ. Comparison of magnetic and electrical phrenic nerve stimulation in assessment of diaphragmatic contractility. J Appl Physiol 80: 1731–1742, 1996.[Abstract/Free Full Text]
  15. Mador MJ, Kufel TJ, Pineda LA, Steinwald A, Aggarwal A, Upadhyay AM, Khan MA. Effect of pulmonary rehabilitation on quadriceps fatiguability during exercise. Am J Respir Crit Care Med 163: 930–935, 2001.[Abstract/Free Full Text]
  16. Mador MJ, Magalang UJ, Kufel TJ. Twitch potentiation following voluntary diaphragmatic contraction. Am J Respir Crit Care Med 149: 739–743, 1994.[Abstract]
  17. Man WD, Moxham J, Polkey MI. Magnetic stimulation for the measurement of respiratory and skeletal muscle function. Eur Respir J 24: 846–860, 2004.[Abstract/Free Full Text]
  18. Martin V, Millet GY, Martin A, Deley G, Lattier G. Assessment of low-frequency fatigue with two methods of electrical stimulation. J Appl Physiol 97: 1923–1929, 2004.[Abstract/Free Full Text]
  19. O'Brien TD, Reeves ND, Baltzopoulos V, Jones DA, Maganaris CN. Assessment of voluntary muscle activation using magnetic stimulation. Eur J Appl Physiol, 2008.
  20. Place N, Maffiuletti NA, Martin A, Lepers R. Assessment of the reliability of central and peripheral fatigue after sustained maximal voluntary contraction of the quadriceps muscle. Muscle Nerve 35: 486–495, 2007.[CrossRef][Web of Science][Medline]
  21. Polkey MI, Kyroussis D, Hamnegard CH, Hughes PD, Rafferty GF, Moxham J, Green M. Paired phrenic nerve stimuli for the detection of diaphragm fatigue in humans. Eur Respir J 10: 1859–1864, 1997.[Abstract]
  22. Polkey MI, Kyroussis D, Hamnegard CH, Mills GH, Green M, Moxham J. Quadriceps strength and fatigue assessed by magnetic stimulation of the femoral nerve in man. Muscle Nerve 19: 549–555, 1996.[CrossRef][Web of Science][Medline]
  23. Romer LM, Haverkamp HC, Amann M, Lovering AT, Pegelow DF, Dempsey JA. Effect of acute severe hypoxia on peripheral fatigue and endurance capacity in healthy humans. Am J Physiol Regul Integr Comp Physiol 292: R598–R606, 2007.[Abstract/Free Full Text]
  24. Romer LM, Haverkamp HC, Lovering AT, Pegelow DF, Dempsey JA. Effect of exercise-induced arterial hypoxemia on quadriceps muscle fatigue in healthy humans. Am J Physiol Regul Integr Comp Physiol 290: R365–R375, 2006.[Abstract/Free Full Text]
  25. Shrout P, Fleiss J. Intraclass correlations: uses in assessing rater reliability. Psychol Bull 86: 420–428, 1979.[CrossRef][Web of Science][Medline]
  26. Strojnik V, Komi PV. Neuromuscular fatigue after maximal stretch-shortening cycle exercise. J Appl Physiol 84: 344–350, 1998.[Abstract/Free Full Text]
  27. Swallow EB, Reyes D, Hopkinson NS, Man WD, Porcher R, Cetti EJ, Moore AJ, Moxham J, Polkey MI. Quadriceps strength predicts mortality in patients with moderate to severe chronic obstructive pulmonary disease. Thorax 62: 115–120, 2007.[Abstract/Free Full Text]
  28. Tomazin K, Dolenec A, Strojnik V. High-frequency fatigue after alpine slalom skiing. Eur J Appl Physiol 103: 189–194, 2008.[CrossRef][Web of Science][Medline]
  29. Vivodtzev I, Wuyam B, Flore P, Levy P. Changes in quadriceps twitch tension in response to resistance training in healthy sedentary subjects. Muscle Nerve 32: 326–334, 2005.[CrossRef][Web of Science][Medline]
  30. Wragg S, Aquilina R, Moran J, Ridding M, Hamnegard C, Fearn T, Green M, Moxham J. Comparison of cervical magnetic stimulation and bilateral percutaneous electrical stimulation of the phrenic nerves in normal subjects. Eur Respir J 7: 1788–1792, 1994.[Abstract]
  31. Yan S, Gauthier AP, Similowski T, Faltus R, Macklem PT, Bellemare F. Force-frequency relationships of in vivo human and in vitro rat diaphragm using paired stimuli. Eur Respir J 6: 211–218, 1993.[Abstract]



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