Surface EMG of proximal leg muscles in neuromuscular patients and in healthy controls. Relations to force and fatigue

Journal of Electromyography and Kinesiology 9 (1999) 299–307 www.elsevier.com/locate/jelekin

Surface EMG of proximal leg muscles in neuromuscular patients and in healthy controls. Relations to force and fatigue a,*

, Frank Spaans b, Jos P.H. Reulen b, Pieter Leffers c, Jan Drukker

Eline Lindeman

d

a Department of Rehabilitation, University Hospital, Maastricht, Netherlands Department of Clinical Neurophysiology, University Hospital, Maastricht, Netherlands c Department of Epidemiology, University of Maastricht, Maastricht, Netherlands Department of Anatomy and Embryology, University of Maastricht, Maastricht, Netherlands b

d

Received for publication 23 January 1999

Abstract In an effort to find parameters to evaluate patients with neuromuscular disorders, surface electromyography (SEMG) of proximal leg muscles was performed in 33 patients with myotonic dystrophy (MyD), 29 patients with Charcot-Marie-Tooth (CMT) disease and 20 healthy controls. The root mean square (RMS) of the SEMG amplitude (␮V) was calculated at different torque levels. Endurance (seconds) and median frequency (Fmed) of the SEMG power spectrum, used as parameters of fatigue, were determined at 80% of MVC. Maximum voluntary contraction (MVC) was found to be decreased in patients; the ratio between RMS values of antagonists and agonists was increased and torque–EMG ratios (Nm/␮V) were decreased. These differences with respect to controls were more pronounced in MyD than in CMT. The initial Fmed value was lowest in CMT. The greatest decrease in Fmed was found in MyD. SEMG data in relation to force have not been determined before in groups of MyD or CMT patients. In both disorders, parameters differed from controls, which means that adding SEMG to strength measurements could be useful in studying the progress of the disorder and the effects of interventions.  1999 Elsevier Science Ltd. All rights reserved. Keywords: Force; Fatigue; Surface EMG; Charcot-Marie-Tooth; Myotonic dystrophy

1. Introduction The main purpose of the present study was to propose a non-invasive, quantitative method for studying the progress of the disease or the effect of strength training programs in patients with a neuromuscular disorder. A number of studies have claimed beneficial effects of strength training in patients with slowly progressive neuromuscular disorders [1,12,17,18,21,22]. These studies, however, have shown various shortcomings. Numbers of patients have been small and a variety of diagnostic groups have been combined. Measurements on patients in training have not been compared in a blinded setting with measurements in a non-training control group of patients with the same disorder. A trial was designed to study the effects of strength * Corresponding author. Current address: Department of Rehabilitation, University Hospital Utrecht/Rehabilitation Centre ‘de Hoogstraat’, Heidelberglaan 100, 3584 CX Utrecht, Netherlands. Tel.: ⫹ 3130-2506770; fax: ⫹ 31-30-2505450; e-mail: [email protected]

training on knee torques and on a number of leg-related functional abilities in adults with the most common slowly progressive inherited neuromuscular disorders, viz., myotonic dystrophy (MyD), a myopathic disorder, and Charcot-Marie-Tooth disease (CMT, also called hereditary motor and sensory neuropathy [HMSN]), a neuropathic disorder [5]. In both disorders, muscle weakness is the main impairment. Although in both MyD and CMT, weakness of the leg muscles predominates distally, proximal leg muscles were studied for a number of reasons: (i) the impact of proximal muscle dysfunction on daily life activities is high, (ii) disabilities due to distal weakness can be limited by ankle–foot orthotics, (iii) the reliability of isokinetically measured knee torques in patients with MyD and CMT is known to be high [27] and (iv) the trainability of less affected muscles is claimed to be better [6]. Torque measurements were combined with surface EMG (SEMG) recordings of proximal leg muscles, by studying the root mean square (RMS) of the amplitude histogram of the SEMG at various torque levels,

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recorded during isometric contraction. The SEMG data can be used to study the physiological mechanism of changes in strength [23]. An endurance test was performed to quantitate fatigue. For this purpose, the median frequency (Fmed) of the power spectrum of the SEMG was monitored during sustained contraction at 80% of maximum voluntary contraction (MVC) [2]. The present study reports data on baseline measurements which can be used as reference values when determining a possible effect of therapeutic interventions on the deterioration of the muscular system.

2. Materials and methods 2.1. Subjects Thirty-three MyD patients, 29 CMT patients and 20 healthy subjects (controls) participated. Groups were similar with respect to age, height and weight (Table 1). The MyD group included twice as many men as women, whereas the sexes were equally represented in the other two groups. Two patients had the congenital form of MyD, the others the adult form. Cardiac involvement was present in 21 (out of 33) MyD patients, but this involvement was not considered to be a contraindication to participating in the study. Six CMT patients had the axonal form, the others the demyelinating form. Patients had been diagnosed by neurologists in various hospitals in the region. No patient was wheelchair-bound. All patients were candidates for participating in a randomized clinical trial on the effects of strength training on muscle strength and functional abilities [14]. All subjects participated in an instruction session in order to get used to the procedure. The project was approved by the University Hospital’s Ethical Commission and informed consent was obtained from each subject.

Table 1 Demographic data of MyD patients, CMT patients and controls. Mean values (with standard deviations)

Number of subjects Gender (men/women) Age in years Range Height in cm Range Weight in kg Range

MyD

CMT

Controls

33 22/11 39 (10) 18–57 171 (8) 157–193 69 (16) 39–114

29 14/15 37 (11) 15–57 169 (10) 153–195 69 (14) 42–99

20 10/10 35 (11) 16–54 173 (10) 158–198 71 (10) 52–90

2.1.1. Force measurements Because of the increased fatiguability of patients, all tests were performed only once for each leg. Isometric knee extension was performed on a Cybex II isokinetic dynamometer (Lumex, Bay Shore, New York) and was combined with SEMG of the vastus medialis (VM), the rectus femoris (RF), the vastus lateralis (VL) and the long head of the biceps femoris (BF). Knee angle was fixed at 60 degrees from full extension because a pilot study had shown measurements at this angle to provide the most reproducible SEMG parameters. The subject was instructed to extend the knee as forcefully as possible and to maintain maximum force for at least two seconds. This torque value was called MVC. After two minutes of rest, the subject was instructed to contract at, successively, 20, 40, 60 and 80% of MVC, with a one minute rest in between. These force levels could be maintained through feed-back from a display, on which the actual force was presented. The subject was instructed to keep this force at the desired value. For the purpose of analysis, a period of at least 2 seconds of artifact-free SEMG was recorded while force was stable at the desired level. To study endurance, the subject was instructed to maintain a force of 80% of his/her MVC for as long as possible, without reinforcement. 2.1.2. SEMG measurements SEMG was recorded with a 4-channel EMG apparatus (MS6, Medelec, Old Woking, Surrey, UK). Bandwidth was 8–800 Hz ( ⫺ 3dB). Depending on the signal amplitude, sensitivity settings were adjusted between 50 and 2000 ␮V/division. The analog output signals of the recording apparatus were converted into 12 bits digital data with a sampling frequency of 2048 Hz, using an analogto-digital (A/D) converter (Burr–Brown, Digital Signal Processor (DSP), type PCI2000) built into a personal computer. The analog output force signal of the Cybex was also processed. Data were temporarily stored on hard disk for off-line analysis. Further processing of calibration and SEMG data was done with a 80286 processor and DSP. A tape streamer was used for final storage of original and processed data. Recordings were made using bipolar electrodes (Medelec SE 40) with felt electrode pads (20 ⫻ 5 mm) with an inter-electrode distance of 40 mm (heart-toheart). The two pads of the electrodes were soaked in saline solution. Before electrode placing, the skin was abrased and cleaned with ethanol, and electrode paste was rubbed into the skin. Electrode placement was between the motor point and the tendon. VM: distal electrode pad 4 cm proximal and medial to the upper edge of the patella. RF: center of the electrode halfway between the inguinal groove and the superior margin of the patella. VL: center of the electrode at 1/3 of the distance between the patella and the greater trochanter. BF:

E. Lindeman et al. / Journal of Electromyography and Kinesiology 9 (1999) 299–307

center of the electrode halfway between the head of the fibula and the sciatic tuberosity. A grounding electrode was attached to the lower leg. 2.1.3. Off-line SEMG analysis Using visual inspection of the five traces on the computer display, 2 seconds of artifact-free signal were selected for further analysis, while the start and end of the endurance test were also marked. All SEMG segments were analysed in the amplitude and the frequency domain. An amplitude histogram, made up of 4096 samples, was constructed for each SEMG segment. Mean, maximum and minimum amplitudes, standard deviation (RMS), skewness and kurtosis were computed. RMS was chosen for the analysis of the relation between SEMG and torque. The same data were used for frequency analysis with a spectral resolution of 0.5 Hz. After removal of the DClevel and the possible linear trend, a hamming window was applied to the selected signals. For the endurance test, a spectrum was calculated every 2 seconds for every channel. The spectra were computed using a Fast Fourier Transform procedure (FFT) implemented on the DSP, and were finally smoothed with a 5-point triangular digital filter. For each spectrum up to 256 Hz, the median, the maximum, the mean, the ⫺ 10 dB frequency and the relative power above 100 Hz were computed. The median frequency of the power density spectrum (Fmed) during the endurance test at 80% MVC was used to evaluate fatigue. 2.2. Statistical analysis The RMS data from the different SEMG measurements were averaged over the two legs for further analysis. Results of VM, RF and VL were averaged (EXT) but also reported separately. For each subject, the reciprocal innervation coefficient (RIC) [9] was calculated as the ratio between RMSBF and RMSEXT at MVC. Because the individual contributions of the components of the quadriceps femoris to the overall torque could not be determined, the RMS data from the different muscle heads were related to the overall knee torque. For each patient, the torque–EMG ratio (TER) was determined as the regression coefficient (slope) of the linear regression line between RMS and the overall torques measured at 20%, 40%, 60% and 80% MVC (TER20–80) [28,29]. Since investigators may not have the opportunity to measure RMS at different torque levels, the TER was also determined as the ratio of RMS to knee torque measured at MVC. Fatigue was evaluated by determining, for each patient, the Fmed value at 2 seconds after the start of measurement (called the initial value) and the changes in Fmed over time using linear regression analysis. The first 2 seconds of registration were discarded because of

301

movement artifacts and incomplete build-up of muscle contraction. The data from the two legs were averaged for each patient. The distributions of the different parameters (MVC, endurance, as well as the above-mentioned SEMGrelated parameters) were non-Gaussian, so medians and ranges are reported instead of means and standard deviations. Differences in the distributions between the MyD, CMT and control groups were statistically tested using the non-parametric Mann–Whitney rank sum test. TER values for men and women were compared within each diagnostic group. In addition, correlations between MVC and endurance were determined by linear regression analysis for each diagnostic group. The relation between SEMG parameters (RMSext and Fmed) and disease progress (represented by MVC) was analysed using linear regression analysis. Regression coefficients (B) are reported. Scatterplots were prepared in order to find indications for the existence of possible subgroups.

3. Results 3.1. MVC and endurance MVC was lower in both patient groups than in the controls (Table 2). MyD patients had lower knee torque values (p ⫽ 0.005) than CMT patients. Median endurance was decreased in both patient groups, but this decrease was not statistically significant. One MyD and two CMT patients had a longer endurance than the maximum in healthy subjects. These three patients had no deviant torque levels. Within the MyD group, a statistically significant association was found between MVC and endurance: stronger subjects could maintain 80% of their MVC over a longer period. 3.2. RMS at MVC The SEMG recordings during MVC measurements were corrupted in one control; the torque and RMS data of this subject were therefore excluded from the relevant calculations. Compared to the healthy control group, RMSEXT at 100% MVC was significantly lower in the MyD group, but not in the CMT group (Table 3). MVC and RMSEXT were positively correlated within the CMT (B ⫽ 0.37) and the healthy control groups (B ⫽ 0.46); no correlation was observed in the MyD group. RMSBF during knee extension was increased in both patient groups; only in the MyD group was this increase statistically significant. Only for the VM and VL were the RMS values of the MyD group significantly lower than those of the CMT group. RIC was increased in both

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Table 2 Knee torques at maximum voluntary contraction (MVC) and endurance at 80% of MVC. Median values and ranges. P values (Mann–Whitney U– Wilcoxon rank sum test)

MVC (Nm) Range Endurance (s) Range

MyD n ⫽ 33

CMT n ⫽ 29

Controls n ⫽ 20

P MyD vs controls

P CMT vs controls

71 7–139 29 8–103

95 42–238 37 12–115

148 107–263 51 27–84

0.0000

0.0002

0.25

0.79

Table 3 RMS (␮V) at MVC. Median values and ranges. VM: vastus medialis, RF: rectus femoris, VL: vastus lateralis, BF: biceps femoris. EXT: mean of the extensor muscles. RIC ⫽ RMSBF:RMSEXT. P values (Mann–Whitney U–Wilcoxon rank sum test)

VM RF VL BF EXT RIC

MyD n ⫽ 33

CMT n ⫽ 29

Controls n ⫽ 19

P MyD P CMT vs controls vs controls

92 11–444 205 76–324 159 74–370 67 30–161 153 72–371 0.42 0.22–0.93

175 31–379 207 74–491 231 74–541 73 17–189 213 62–470 0.32 0.15–0.78

148 89–505 243 65–430 245 119–529 53 36–109 219 121–401 0.25 0.12–0.54

0.003

0.94

0.02

0.21

0.006

0.65

0.05

0.29

0.001

0.62

0.0000

0.005

patient groups, but RIC was significantly higher in the MyD group than in the CMT group. RMSVM was significantly lower than RMSRF and RMSVL in all three groups of subjects, whereas RMSRF and RMSVL did not differ significantly. 3.3. Relations between torque and RMS Fig. 1 presents typical examples (one individual from each diagnostic group) of TER20–80 (slope of the regression line) and TER100. In both patient groups, TER20–80 (Table 4) as well as TER100 (Table 5) were decreased, the decrease being most pronounced in MyD patients. This means that at an identical torque value, the corresponding RMS was higher in patients than in controls and higher in MyD subjects than in CMT subjects. Only for RF were the differences in TER between the two patient groups statistically significant. Differences between patients and controls were more pronounced for TER100 than for TER20–80, due to the lower variability in TER100. TEREXT values tended to reveal the differences between patients and controls more explicitly than the data on each individual muscle. Differences in TER between men and women were

Fig. 1. Torque–EMG ratios of the rectus femoris muscle. A typical example is shown for each diagnostic group. 䊏 ⫽ MyD, 왖 ⫽ CMT, * ⫽ healthy control. Each symbol represents a single torque measurement (at 20, 40, 60, 80 and 100% MVC). Solid lines represent the regression line over 20, 40, 60 and 80% MVC (TER20–80). TER100 was calculated by dividing extension torque by RMS at MVC (unconnected symbols).

Table 4 Torque/EMG ratio (TER20–80, Nm/␮V) of the three extensor registrations based on regression analysis over the data at 20, 40, 60 and 80% MVC of each subject. Median values and ranges. P values (Mann–Whitney U–Wilcoxon rank sum test)

VM RF VL EXT

MyD n ⫽ 33

CMT n ⫽ 29

Controls n ⫽ 19

P MyD P CMT vs controls vs controls

0.77 0.11–4.01 0.38 0.07–1.03 0.40 0.02–1.06 0.58 0.12–1.74

0.68 0.21–2.91 0.56 0.27–1.06 0.46 0.19–1.04 0.63 0.34–1.46

1.13 0.52–2.11 0.61 0.41–1.53 0.65 0.41–1.30 0.83 0.64–1.35

0.06

0.005

0.0004

0.11

0.02

0.01

0.03

0.004

not found in either of the diagnostic groups (data not shown). TER values of the two subjects with the congenital form of MyD were within the range of TER values found for the other MyD patients. Within the CMT group, data of the six patients with the axonal form

E. Lindeman et al. / Journal of Electromyography and Kinesiology 9 (1999) 299–307

Table 5 Torque/EMG ratio (TER100, Nm/␮V) of the three quadriceps registrations based on the data for MVC. Median values and ranges. P values (Mann–Whitney U–Wilcoxon rank sum test)

VM RF VL EXT

Table 6 Fatigue and Fmed. Endurance test at 80% MVC. Initial Fmed in Hz, based on regression lines (see text). Median values and ranges. P values (Mann–Whitney U–Wilcoxon rank sum test)

MyD n ⫽ 33

CMT n ⫽ 29

Controls n ⫽ 19

P MyD P CMT vs contols vs controls

0.66 0.06–2.71 0.40 0.05–0.78 0.37 0.03–0.91 0.43 0.06–1.02

0.64 0.22–2.42 0.48 0.22–0.86 0.48 0.24–0.94 0.52 0.28–0.93

0.98 0.38–1.95 0.61 0.41–2.08 0.62 0.42–1.24 0.71 0.49–1.28

0.05

0.01

VM

0.0001

0.004

RF

0.004

0.003

VL

0.0007

0.0009

BF EXT

were not significantly different from those with the demyelinating form. 3.4. Fatigue and Fmed Fig. 2 presents typical examples (one individual from each diagnostic group) on changes in Fmed over time and shows the regression lines whose initial values (calculated as the value at 2 seconds) and slopes were used for further analysis. For all muscles, initial Fmed values were significantly lower in the CMT group than among the controls (Table 6) and MyD patients (P ⫽ 0.0000). For the RF and VL (and BF) muscles, the decrease in Fmed due to fatigue was similar for the CMT group and the controls. However, a much greater decrease was found in the MyD group (Table 7). This was also shown by a significantly steeper slope of Fmed for the RF and VL in MyD compared to CMT patients. No decrease in Fmed was found for the VM in 6 MyD patients, 1 CMT

Fig. 2. Changes in Fmed over time for endurance at 80% MVC, presented for the rectus femoris muscle. A typical example is shown for each diagnostic group. 䊏 ⫽ MyD, 왖 ⫽ CMT, * ⫽ healthy control. The regression line used for further analysis (see text) is indicated.

303

MyD n ⫽ 33

CMT n ⫽ 29

Controls n ⫽ 20

P MyD P CMT vs contols vs controls

85 67–120 89 75–107 73 64–113 90 70–121 82 72–110

71 58–96 77 49–90 65 52–78 75 56–93 72 56–85

78 67–92 87 76–99 80 63–91 90 70–101 81 71–89

0.27

0.0000

0.07

0.002

0.27

0.0000

0.65

0.0001

0.21

0.0000

patient and 6 controls, for the RF in 1 CMT patient and for the VL in 5 MyD patients and 3 CMT patients. Within each diagnostic group the correlation between MVC and initial Fmed and between MVC and changes in Fmed over time were calculated. Only in the MyD group were significant correlations found (B initial Fmed vs MVC ⫽ ⫺ 1.79, B changes in Fmed vs MVC ⫽ 48). 4. Discussion 4.1. Weakness Knee extension torque was found to be decreased in both patient groups, even though weakness in both MyD and CMT generally shows a distal preponderance. Loss of muscle strength was more evident in the MyD group than in the CMT group. Although there is a relation between the decrease in knee torques and disabilities as measured by time-scored activities [15] many patients, especially those with CMT, were not aware of proximal weakness. Endurance was also decreased, more so in MyD than in CMT, but differences between the three groups were not statistically significant, probably because of the high degree of variation between individuals, especially in the patient groups. Endurance depends not only on the neuromuscular apparatus, but also on other factors like motivation. In the past, some patients had been advised to prevent muscle damage from overloading. This advice may have influenced motivation, causing more variation in the performance of patients than in that of controls. This suggests that time-scoring of endurance does not represent an appropriate parameter. Although the torque level at which the endurance exercise had to be performed was adapted to each subject’s maximum torque, a positive correlation between MVC and endurance was found in the MyD group. The cause of this relation is unclear.

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Table 7 Fatigue and Fmed. Endurance test at 80% MVC.⌬Fmed versus ⌬time; slopes of regression lines (Hz/s). Median values and ranges. P values (Mann– Whitney U–Wilcoxon rank sum test). (For endurance times: see Table 2) MyD n ⫽ 33 VM RF VL BF EXT

⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺

0.37 2.12 0.51 2.56 0.37 1.87 0.33 1.81 0.41 2.10

CMT n ⫽ 29

to 0.33 to ⫺ 0.06 to 0.22 to 0.21 to 0.85

⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺

0.14 1.02 0.23 0.65 0.11 0.65 0.11 0.84 0.17 0.59

Controls n ⫽ 20

to 0.05 to 0.43 to 0.11 to 0.21 to 0.12

⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺

0.06 0.34 0.22 0.62 0.16 0.59 0.10 0.60 0.16 0.50

P MyD vs controls

P CMT vs controls

0.003

0.02

0.009

0.87

0.11

0/19

0.05

0.32

0.008

0.61

to 0.13 to ⫺ 0.07 to ⫺ 0.04 to 0.31 to ⫺ 0.01

4.2. SEMG

4.3. Force and SEMG

Only in the MyD group was a decreased RMS found at MVC, most prominently for the VL and VM. In MyD, weakness is mainly due to primary degeneration of muscle fibers [8]. To some extent, abnormalities of the electromechanical activation process resulting from the myotonic component of the disorder may contribute to the weakness. In CMT, weakness is mainly due to loss of motor units [4], only partially compensated for by collateral reinnervation of denervated muscle fibers [11]. Suboptimal co-ordination during motor unit recruitment may also play a role. In all three groups, RMSVM was lower than RMSRF and RMSVL. The lower RMSVM may be due to a less favourable position of the recording electrode relative to the VM muscle fibers, due to muscle configuration and/or the distribution of fat tissue. The finding that the VM yielded lower values than the RF and VL for all groups of participants suggests that these three muscles tend to be equally affected in CMT and in MyD. Some information about the degree of hamstring activation at various levels of knee extension was obtained by monitoring the BF. RMSBF during maximum knee extension was high in patients compared to controls; the highest activity was found in the MyD group (Table 3). The RMSantagonist:RMSagonist quotient has been named “reciprocal innervation coefficient” (RIC) [9]. We defined it as RMSBF:RMSEXT. We found RIC to be considerably increased in the MyD group, and to a lesser degree in the CMT group. This has not been reported before for these disorders. It means that during knee extension the BF shows a high electrical activity in patients compared to controls. The resulting activation of the BF not only counteracts the agonistic muscles, but also plays a role in neutralizing the anteflexion torque of the RF on the hip joint during knee extension. It could be that the patients need a relatively stronger activation of the BF in order to stabilize sufficiently, or that their motor co-ordination is decreased.

In most studies done so far, the SEMG of a single agonistic muscle was recorded and related to “overall” torque [13,16,20,23–25,28,29]. The relation between torque and RMS has been called neuromuscular efficiency (NME) [20], a term which suggests a causal interpretation. We opted for the more neutral expression torque–EMG ratio (TER), where the extension torque of the proximal leg musculature as a whole is related to the mean of the RMS values of the VM, RF and VL. It was supposed that the average RMS value of the three main superficial parts of the quadriceps muscle would provide a more reliable measure of the electrical activity of the whole muscle group than the RMS value of a single part. We did indeed find that this averaged value revealed the differences between patients and controls more clearly (Tables 4 and 5). The lowest TER values were found in MyD (Tables 4 and 5, Fig. 1). Different factors may contribute to muscle weakness in MyD [26], leading to primary muscle fiber dysfunction. This means that more fibers have to be activated to generate a certain force than in normal people. The more modest decrease in TER in the CMT group could be due to a suboptimal interaction between motor units, possibly resulting from the continuous process of muscle fiber denervation and reinnervation or from a diminished propriocepsis. Data showing a decreased TER have been presented before in myopathic disorders [13]. For neuropathic disorders, normal values [13] as well as reduced TERs [25] have been reported. It has been advocated to determine torque–EMG ratios by measuring electrical activity at different force levels and constructing regression lines through the relevant points [24,28,29]. In our study, data on MVC were evaluated separately, because at this torque level RMS was expected to show greater variation. However, we found no essential group differences between the two approaches (Tables 4 and 5). This means that, with our techniques, RMS measurements at MVC only are suf-

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ficient for the assessment of the TER, that is, if group comparisons are the purpose of the study. An advantage is that registrations are much easier to perform if they can be limited to MVC. TERs in all three groups were greater for the VM than for the RF and VL. This can be explained from the lower RMS values of the VM, as has been discussed above. The TER values reflected group differences much better than the plain maximum RMS values. 4.4. Fatigue In addition to endurance, the change in Fmed was used as a parameter of fatigue. Fmed was monitored during sustained knee extension at 80% MVC. In accordance with the findings of other authors, we found the decrease in Fmed to be quasi-linear [10,16,30]. Results were evaluated by (i) the slope of the regression lines of Fmed over time and (ii) the value of Fmed calculated 2 seconds from the start of the registration. The latter value is called “initial Fmed” (Table 6). In MyD, it tended to be increased in some subjects, which may be due to the increased number of small polyphasic MUPs in myopathic disorders [8], giving rise to a signal with a higher frequency content. In CMT, initial Fmed was found to be decreased. A possible explanation is the presence of enlarged motor units as a result of longstanding reinnervation [11]. Enlarged motor units may be particularly susceptible to fatigue [19]. In MyD, Fmed decreased rapidly, reflecting the increased fatiguability of these patients (Table 7). In CMT, a diminished endurance could not be related to a steeper Fmed decrease. Only a few authors have reported on changes in SEMG Fmed during endurance tests in chronic neuromuscular disorders. In MyD patients, the Fmed of foot flexors [3] and of the biceps brachii [31] was found not to decrease rapidly during sustained maximum voluntary contraction. Fmed has been studied by needle EMG in elbow flexors in a variety of neuromuscular disorders [7,30]. At 30% MVC, the findings were in agreement with ours: Fmed was increased in 11 out of 20 patients with myopathies and decreased in 7 out of 11 patients with neuropathic disorders (none with CMT) [7]. However, in an endurance test at MVC, initial Fmed was found to be decreased in a group of 13 myotonic patients, whereas normal initial Fmed values were found for a group of 86 patients with neuropathies [30]. No other studies have compared different proximal leg muscles in patients by SEMG. The Fmed of RF and VL in healthy subjects has been found to show similar decreases [10]. The present study showed FmedRF to decrease in almost all subjects because of fatigue, whereas FmedVM and FmedVL did not decrease in some patients. Moreover, the steepest slope of Fmed was found

305

for the RF. Therefore, if endurance is studied according to our protocol, i.e. during isometric knee extension at a knee angle of 60°, the RF seems to show muscle fatigue most clearly.

5. Conclusion We found that measurements of knee extension torques in combination with SEMG revealed quite a number of significant differences between our patient groups and normal controls. It is therefore suggested that findings like the low TER values in both patient groups and low initial value of Fmed in CMT patients and the rapid decrease of Fmed during an endurance test in MyD patients are probably related to the different pathophysiological backgrounds of the two neuromuscular disorders. The findings suggest that, besides strength measurements, RMS might be particularly useful to evaluate progress in the CMT group, while changes in Fmed over time might perform the same function in the MyD group.

Acknowledgements The authors would like to thank H. Hermens, director of Roessingh Research and Development at Enschede, the Netherlands, for assisting in the development of the protocol and the interpretation of the data, M. Theulings for developing the data acquisition software and M. Duijf, M. Kerkhofs and A. Ko¨ke for assisting in the data acquisition.

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IEMG vs torque relationship for the forearm flexors and leg extensors. Am J Phys Med 1992;71:283–7. [29] Woods JJ, Bigland-Ritchie B. Linear and non-linear surface EMG/force relationships in human muscle. Am J Phys Med 1983;62:287–99. [30] Yaar I, Niles L. Muscle fiber conduction velocity and mean power spectrum frequency in neuromuscular disorders and in fatigue. Muscle Nerve 1992;15:780–7. [31] Zwarts MJ, Weerden Van TW. Transient paresis in myotonic syndromes. Brain 1989;112:665–80. Eline Lindeman graduated as a medical doctor from the University of Amsterdam in 1977. She specialized in Rehabilitation Medicine. From 1984 until 1996 she was head of the Rehabilitation Department of the University Hospital of Maastricht. From 1990 until 1994 she followed a training developed by the Health Research Promotion Programme (SGO) on Rehabilitation Medicine, which was set up by the Ministries of Education and of Welfare, Public Health and Cultural Affairs. In 1996 she received her Ph.D. at the University of Maastricht. From 1996 she has worked at the Rehabilitation Department of the University Hospital Utrecht and as a staff member of the Rehabilitation Centre “de Hoogstraat”, The Netherlands. Frank Spaans graduated from the Medical Faculty of Amsterdam in 1964. He specialized in Neurology and received his Ph.D. in medicine from the University of Amsterdam in 1971. Subsequently he became a staff member at the Department of Clinical Neurophysiology of the De Wever Hospital at Heerlan, The Netherlands. In 1978 he joined the Medical Faculty of the Maastricht University, where he became Professor of Clinical Neurophysiology and Head of the Department of Clinical Neurophysiology of the University Hospital in 1985. His research activities are mainly directed to electromyography and neuromuscular disorders. Jos P.H. Reulen holds the M.Sc. of the Technical University in Eindhoven, The Netherlands, and Ph.D. (Free University, Amsterdam) degree in technical and biomedical physics, respectively. From 1973 to 1987 he investigated eyemovement physiology and recording technology at the department of Medical Physics, Free University, Amsterdam. In 1987 he joined as a biomedical engineer the Department of Clinical Neurophysiology at the University Hospital of Maastricht. His scientific activities are in the field of clinical neurophysiology in particular EMG, quantitative EEG and quantitative thermal testing. Pieter Leffers received Masters degrees in environmental sciences from the Agricultural University of Wageningen, The Netherlands (1978), in epidemiology from Harvard School of Public Health (1981), and in medicine from Maastricht University, The Netherlands (1988). He is an assistant professor of clinical epidemiology in the Department of Epidemiology of the medical school of Maastricht University, where he has been since 1982. Apart from teaching for undergraduates, he teaches courses in clinical epidemiology and research protocol development for research fellows and interns in the local teaching hospital and for Dutch rehabilitation specialists. He has also taught several international courses, both in The Netherlands and abroad. He is involved, as a methodologist, in clinical research in many different medical fields.

E. Lindeman et al. / Journal of Electromyography and Kinesiology 9 (1999) 299–307 Jan Drukker graduated as a medical doctor from the University of Amsterdam (UvA) in 1958. In 1961 he received his Ph.D. at the UvA, where in 1970 he became Associate Professor. From 1987 until 1996 he was Professor of Anatomy and Embryology and chairman of the Department of Anatomy and Embryology at the University Maastricht. From 1982 until 1994 he was also chairman of the Board of Governors of the Institute for Rehabilitation Research (iRv) in Hoensbroek, The Netherlands. He is now an Emeritus Professor.

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