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Evaluation of the estimation of muscle fiber conduction velocity. Surface versus needle method
544
Electroencephalograph)' and clinical Neurophysiology, 1989, 7 3 : 5 4 4 - 5 4 8 Elsevier Scientific Publishers Ireland, Ltd.
EEG 02351
Ev~ua~n
of the estimation of m ~ l e fiber conduction velocity. Surface versus needle method Machiel J. Zwarts
Neurological Clinic, Department of Clinical Neurophysiology, University Hospital, 9713 EZ Groningen (The Netherlands) (Accepted for publication: 19 May 1989)
Summm'y Two techniques to measure muscle fiber conduction velocity (MFCVJ were compared. First. muscle fibers of biceps muscle were directly stimulated with needle electrodes, and the latency of the evoked muscle fiber action potentials was measured at a distance of 5 cm. Subsequently, the M F C V was measured at the same place with surface electrodes using the cross-correlation method. Fourteen controls were studied and illustrative results of the measurements of 6 myopathy patients are given. A clear correlation between the mean values of the two methods was found. The surface E M G technique resulted in a systematically higher M F C V (mean 1.0 m / s e c ) ; the variability of M F C V was m u c h higher with the invasive technique. The reasons for these differences are discussed. M F C V measurements are shown to be of diagnostic value in some myopathies, for example myositis. In myopathies with a global reduction of the M F C V the two methods are of equal value: in some cases of longstanding myositis the needle method demonstrated some very slowly conducting fibers which were not detected with the surface method. Key words: Muscle fiber conduction velocity; Surface E M G method; Needle method
Different techniques exist to measure the muscle fiber conduction velocity (MFCV); for a recent review see Arendt-Nielsen and Zwarts (1989). An important division can be made between invasive (needle EMG) and non-invasive (surface EMG) techniques. The first extensive measurements of MFCV were done by Buchthal et al. (1955) by measuring the time delay of action potentials (APs) between 2 recording needles in the muscle and activating the muscle either by electrical stimulation or voluntary contraction. This method was very time consuming and has not gained general application. Troni et al. (1983) suggested an easier approach by measuring the latency of muscle fiber APs with only one recording electrode. Alternatively, the MFCV can be measured with surface electrodes; the most widely used approach
Correspondence to: Dr. Machiel J. Zwarts, MD, Neurological Clinic, Dept. of Clinical Neurophysiology, University Hospital, Oostersingel 59, 9713 EZ Groningen (The Netherlands).
is the cross-correlation technique. The question arises of which grounds to choose for a certain technique. Further, it is known that the surface results are in general higher than the values obtained with needle methods (Sollie et al. 1985; Arendt-Nielsen and Zwarts 1989). As yet, the reasons for this difference are not clear. It was the purpose of this study to investigate the differences, potential benefits and limitations of both methods. This was done by applying the method of Troni and the cross-correlation technique subsequently on the same muscle and to compare the results. In order to show the difference of these 2 methods with respect to pathological muscles, illustrative measurements of several myopathies were chosen.
Methods Both methods have been described in detail (Troni et al. 1983; Zwarts et al. 1988). The estima-
0013-4649/89/$03.50 ~ 1989 Elsevier Scientific Publishers Ireland, Ltd.
MFCV: SURFACE VS. NEEDLE METHOD tion with needles was always done first, because the direction of the muscle fibers was thereby known; this facilitated the positioning of the surface electrodes parallel to the muscle fibers. The needle E M G measurements were done with a Tt~nnies E M G apparatus (Myograph DA IIR), the signals being amplified with a bandpass filter of 500 H z - 1 0 kHz; the time base was 5 msec per division. Two stimulation electrodes (Disa, 13L64, area of the uninsulated tip: 2 mm 2) were placed in the distal part of the short head of the biceps brachii muscle with the cathode proximal and 2-3 mm from each other. Care was taken to place the electrodes perpendicular to the surface. The muscle was stimulated with gradually increasing strength until a clear twitch was palpable (10-20 V, 0.2 msec, 1 Hz). With the aid of the twitch, the recording electrode (Disa, 13L50) was placed 5 cm proximal and manipulated until APs with the dimensions of fibrillations (bi- or triphasic waves with a duration of 1-5 msec and an amplitude of 20-500 /~V) were seen. After some preliminary experiments we preferred to use a standard concentric E M G needle instead of the single fiber electrode used by Troni, because this resulted in easier finding of more spikes. The resulting APs were generally biphasic, initially positive, spikes. The latency was measured at the initial positive turn. In the case of late potentials 4-trace storage was used to ensure the stimulus-locked occurrence of the APs. As an arbitrary criterion only spikes larger than 0.1 mV were used for the calculations. The measurements were repeated 3 times after small displacements of the electrodes. The mean value of the 3 average MFCV results was used for calculations. Subsequently, the surface E M G records were made from the same place of the muscle, between the motor point and the tendon. The direction of the electrode parallel to the muscle fibers was chosen with the aid of the puncture sites of the needles between the motor point and the distal tendon. The skin was cleaned with alcohol and lightly abraded. Three round bipolar brass electrodes (with a diameter of 2 mm) were used, placed in a longitudinal array, 1 cm apart and the center electrode in common. The force was measured at the wrist with strain gauges and displayed
545 on a voltmeter in front of the subject. The signals were amplified with a Disa E M G amplifier, type 14C13, bandpass 20-2000 Hz, and epochs of 200 msec were digitized with a sampling rate of 6024 Hz on a PDP 11/23 computer. The delay between the two signals was estimated with the cross-correlation technique after interpolation, which raised the sample frequency to 12,000 Hz. The measurements were made twice at different (isometric) contraction levels, from low to maximal in steps of 20 or 40 N, depending on the maximal force; this resulted generally in 4 - 5 steps. Only correlation coefficients higher than 0.85 were accepted. The mean value of these MFCV results was used for calculations. The difference between the fastest and the slowest conduction velocity (range) was expressed as a ratio for both methods: the fastest divided by the slowest MFCV result (F/S). The subjects were 7 healthy males and 7 females, aged 24-44 years. The patients were selected for the illustrative character of the measurements and included 4 myositis patients (the diagnosis being based on proximal muscle weakness, concentric needle E M G findings of myopathic motor units, raised C K and biopsy), one with familial hypokalemic periodic paralysis (from the kinship described in Zwarts et al. 1988) and one with an undetermined myopathy, presumably alcoholic. The relation between variables was analyzed with linear regression analysis, the difference between the paired results with the sign test.
Results The relations between the mean values of the surface and needle estimates (S-MFCV and NMFCV respectively) are shown in Fig. 1. Note that in all cases the surface E M G values were higher than the needle estimates. A clear correlation existed between the results of the two methods. S-MFCV = 1.1 + 1.0 x N-MFCV (n = 20, r = 0.76, P < 0.001). For the different groups, the relation was significant for the male controls (SMFCV=0.5+I.2×N-MFCV, r=0.78, P< 0.05) and the myopathies (S-MFCV = 0.3 + 1.3 x
546
M.J. ZWARTS
non-invasive MFCV (re.s-'}
control
~/-- 3.| m.s" I
6
o°
5 ¸
~1~l W'~-
V-- 4.2 m.s"
-
× o~ 4-
3-
- J 500/uV
."
/
~* female male
5ms
Fig. 2. Examples of conduction velocity measurements with needle recording. Note the late potentials in both myositis patients.
• myopathy
"J
:3
'~
5 invasive MFCV (m.s-')
Fig. 1. The relation between the mean muscle fiber conduction estimation with the invasive and non-invasive method. Note that all data lie above the line: y = x, The 2 data points of the patients with a high conduction velocity are from the cases with long standing myositis.
N-MFCV, r = 0.9, P < 0.01) but not for the female controls. The results of both methods are summarized in Table I. For both controls and patients N-MFCV was always lower than S-MFCV ( P < 0.001, sign test), the mean difference was 1.0 m/sec. The fastest divided by the slowest MFCV ( F / S ratio) was for all the investigated subjects - including the patients - higher with the invasive method (see Table I), indicating a larger range of velocities with the invasive method. Note that the F / S ratio of all myopathy patients was much higher than the control values for the invasive, but not for the non-invasive method. A slight, but
significant relation between force and S-MFCV of the controls was found (r = 0.19, P = 0.029, n =
130). The MFCV of the myositis patients was either higher or lower than the normal values (see Fig. 1). The disease duration of the two myositis patients with low CVs was 1 and 4 months; for the patients with a high MFCV this was 2 and 6 years. Examples of the invasive measurements are given in Fig. 2. Note the late spikes in both myositis patients, resulting in a high F / S ratio.
Discussion The clear correlation between MFCV values found with both methods can be regarded as a validation of the surface E M G method. The lack of a significant relation for females could be due
TABLE I Results of muscle fiber conduction estimation with an invasive and a non-invasive method. Muscle fiber conduction ( m / s e c mean 4- S.D,)
F a s t / s l o w ratio (range)
Invasive
Non-invasive
Invasive
Non-invasive
Controls Male (n = 7) Female (n = 7)
3.2_+0.3 3.1 _+0.4
4.25:0.5 * 4.0_+0.3 *
1.48 (1.2-1.7) 1.45 (1.3-1.7)
1.17 (1.1-1.3) * 1.17 (1.1--1.3) *
Myopathy patients (n = 6)
2.7 _+0.7
3.9_+ 1.1 *
2.92 (2.2-4.1)
1,12 (1.1--1.2) *
n = number of persons. * Significantly different from the value of the invasive method (P < 0.05).
MFCV: SURFACE VS. NEEDLE METHOD to the smallness of the subgroup. The fact that the type II fibers of females have no larger diameter than the type I fibers could perhaps also account for this finding (because MFCV is related to the diameter of the fiber, see below). The difference found between the two methods indicates a systematic higher estimation of about 1 m / s e c with the non-invasive technique. The mean values of the MFCV and the systematic differences between the two methods both agree with the literature (Sollie et al. 1985; Arendt-Nielsen and Zwarts 1989). Several factors could contribute to this difference: (1) MFCV is dependent on the stimulus frequency. The frequency of stimulation with the needle method is 1 Hz. With surface EMG, the measurements are made during voluntary contraction. The firing rate is known to lie between 8 and 20 Hz. Between 10 and 20 Hz the MFCV increases with a mean of 10-20% (Stflberg 1966; Morimoto and Masuda 1984). (2) Every misdirection of the surface electrodes leads to too high an estimation, although this influence is only small (Sollie et al. 1985). A misdirection with the needle method leads also to a wrong estimate, but not in a systematic way. (3) A further cause of the too high surface E M G values could be a bias towards the fast twitch (type II) motor units (MUs), which are known to have higher conduction velocities (Andreassen and Arendt-Nielsen 1987). This bias could occur because of the larger amplitudes of the type II MU action potentials (Wallinga-De Jonge et al. 1985) or to the more superficial position of the type II MUs (Johnson et al. 1973). (4) It is known that with surface E M G estimation standing waves can occur on both channels (thus without time delay), resulting in too high an estimate (Broman et al. 1985a). This could occur because of end-plates beneath the surface electrode, or due to far-field potentials which can arise at the moment the action potential blocks at the end of the muscle fiber (Gootzen et al. 1988). (5) The high-pass filter of 500 Hz used for needle recording could result in small time shifts of the spikes and consequently a lower MFCV result. This influence needs further investigation. A second important difference between the two methods is the much larger range of velocities obtained with Troni's method. With surface E M G
547 the MFCV increases with higher levels of contraction (Arendt-Nielsen et al. 1984; Broman et al. 1985b; Sadoyama and Masuda 1987; Zwarts et al. 1988), because of the orderly recruitment of the MUs (Henneman's size principle), the MUs recruited at higher forces having higher conduction velocities (Andreassen and Arendt-Nielsen 1987). By measuring from low to high forces, a range of velocities is obtained. The estimation of MFCV with surface E M G is the weighted average of all active MUs; this mean value accounts for the much smaller range of the MFCV as measured with surface EMG. Interestingly, the F / S ratio of the invasive measurements of the myopathy patients was much higher than the control values (2.92 versus 1.46). This is in agreement with the increased fiber diameter variability found in most myopathies, resulting in a large range of conduction velocities, because of the dependence of the MFCV on the fiber diameter (HLkansson 1956). Other pathological alterations of the muscle such as fiber splitting could also contribute to an increased variability. The much larger F / S ratio found in the different myopathies - partly due to several very slow conducting fibers - was totally absent in the surface E M G measurements (see Table I). Moreover, the variability of the surface E M G values in these myopathies was even slightly lower than the F / S ratio of the controls. The slow conducting APs stem probably from small, atrophic fibers; the small amplitude of these spikes hardly influences the surface record. Further, the variability of the surface E M G MFCV results from the recruitment order; in myopathies it is well known that early recruitment occurs at slight voluntary contraction. Thereby, the difference between MFCV at low and high forces could be less marked. Of course, in myopathies other factors could play a role, such as a predominant involvement of one motor unit type. A reduced MFCV could be demonstrated with both methods in the patient with hypokalemic periodic paralysis. In several myopathies in which an affection of the membrane exists, a global reduction of the MFCV could be demonstrated with surface E M G (Zwarts et al. 1988; Zwarts and Van Weerden 1989). The results obtained in the
548
myositis patients agree with the findings of Troni et al. (1988). In the 2 cases with acute myositis, MFCV was found to be severely reduced with both methods. The 2 cases with long standing myositis showed a relatively high MFCV with both methods, probably due to the development of hypertrophic muscle fibers as an adaptation to the paresis. In these 2 cases several very slowly conducting fibers (see Fig. 2) were demonstrated with the invasive method, indicating the existence of pathological, probably atrophic, fibers. In conclusion, both needle and surface EMG measurements result in reliable estimates of human muscle fiber conduction velocity. The invasive method is painful but requires only minimal patient cooperation. It gives a good indication of the variability of MFCV; this is of diagnostic value especially in myositis. With surface EMG the estimate is systematically higher. This method is only applicable to a few muscles. An advantage is its painless character and the possibility to measure at different force levels and during continuous contraction. This method is suitable for studying the changes of the MFCV during fatigue. In myopathies with a global reduction of MFCV the two methods have equal value. Alice Burgler, Carla Klein Geltink, Jarmy Van Marwijk and Agnes Wijnandts are thanked for technical assistance. T o m Van Weerden is acknowledged for a helpful review of the article.
References Andreassen, S. and Arendt-Nielsen, L. Muscle fibre conduction velocity in motor units of the h u m a n anterior tibial muscle: a new size principle parameter. J. Physiol. (Lond.), 1987, 391: 561-571. Arendt-Nielsen, L. and Zwarts, M.J. The measurement of muscle fibre conduction velocity in humans. Techniques and applications. J. Clin. Neurophysiol., 1989, 6: 173-190. Arendt-Nielsen, L., Forster, L. and Mills, K.R. The relationship between muscle fiber conduction velocity and force in the h u m a n vastus lateralis. J. Physiol. (Lond.), 1984, 353: 6P. Broman, H., Bilotto, G. and DeLuca, C.J. A note on the
M.J. Z W A R T S noninvasive estimation of muscle fibre conduction velocity. IEEE Trans. Biomed. Eng., 1985a. 32: 341-344. Broman. H.. Bilotto. G. and DeLuca. C.J. Myoelectric signal conduction velocity and spectral parameters: influence of force and time. J. Appl. Physiol.. 1985b. 5 8 : 1 4 2 8 - 1 4 3 7 Buchthal. F., Guld, C. and Rosenfalck. P. Propagation velocity m electrically activated muscle fibres in man. Acta Physiol. Scand.. 1 9 5 5 . 3 4 : 7 5 - 8 9 Gootzen, T . H J . M . . Vingerhoets. H.M. and Stegeman. D.F. Volume conduction modeling of motor unit action potentials in the surface electromyogram. In: W. Wallinga, H . B . K Boom and J. De Vries (Eds& Electrophysiological Kinesiology. Proc. 7th Congr. Int. Soc. Electrophysiologlcal Kinesiology. Elsevier. Amsterdam. 1988: 227-230. H~kansson. C.H. Conduction velocity and amplitude of the action potential as related to circumference in the isolated fibre of frog muscle. Acta Physiol. Scand.. 1956. 39: 291-312. Johnson. M.A., Polgar, J.. Weightman. D. and Appleton, 1). Data on the distribution of fibre types in thirty-six h u m a n muscles. An autopsy study. J. Neurol. Sci., 1973. 18: 111-129. Morimoto. S. and Masuda. M. Dependence of conduction velocity on spike interval during voluntary muscular contraction m h u m a n motor units. Eur. J. Appl. Physiol.. 1984. 53: 191-195. Sadoyama. T. and Masuda. T. Changes of the average muscle fiber conduction velocity during a varying force contraction. Etectroenceph. clin. Neurophysiol., 1987. 67: 495-497, Sollie, G., Hermens, H.J.. Boon. K . L . WaUinga-De Jonge, W. and Zilvold. G. The measurement of the conduction veloctty of muscle fibers with surface E M G according to the cross-correlation method. Electromyogr. Clin. Neurophysiol.. 1985.25: 193-204. Sthlberg, E, Propagation velocity in h u m a n muscle fibers in situ. Acta Physiol. Scand.. 1966, 2 8 7 : 3 - 1 1 2 Troni. W.. Cantello. R. and Ralnero, E. Conduction velocity along h u m a n muscle fibers in situ. Neurology, 1983. 33: 1453-1459. Troni. W.. Doriguzzi. C. and Mongini. T, H u m a n muscle fiber conduction velocity in polymyositis. In: Congress of the Int. Soc. of Motor Dist., I.S.M.D.. 1988. abstr, 149. Wallinga-De Jonge. W.. Gielen, F . L H . . Wirtz. P.. De Jong, P and Broenink, J. The different action potentials of fast and slow muscle fibers. Electroenceph. clin. Neurophysiol., 1985. 60: 539-547. Zwarts, M.J. and Van Weerden, T.W. Transient paresis in myotonic syndromes. A surface E M G study. Brain, 1989. 112: 665-680. Zwarts, M.J., Van Weerden, T.W., Links, T.P., Haenen, H.T.M. and Oosterhuis, H.J.G. The muscle fiber conduction velocity and power spectra in familial hypokalemic periodic paralysis. Muscle Nerve. 1988, 11: 166-173.
Electroencephalograph)' and clinical Neurophysiology, 1989, 7 3 : 5 4 4 - 5 4 8 Elsevier Scientific Publishers Ireland, Ltd.
EEG 02351
Ev~ua~n
of the estimation of m ~ l e fiber conduction velocity. Surface versus needle method Machiel J. Zwarts
Neurological Clinic, Department of Clinical Neurophysiology, University Hospital, 9713 EZ Groningen (The Netherlands) (Accepted for publication: 19 May 1989)
Summm'y Two techniques to measure muscle fiber conduction velocity (MFCVJ were compared. First. muscle fibers of biceps muscle were directly stimulated with needle electrodes, and the latency of the evoked muscle fiber action potentials was measured at a distance of 5 cm. Subsequently, the M F C V was measured at the same place with surface electrodes using the cross-correlation method. Fourteen controls were studied and illustrative results of the measurements of 6 myopathy patients are given. A clear correlation between the mean values of the two methods was found. The surface E M G technique resulted in a systematically higher M F C V (mean 1.0 m / s e c ) ; the variability of M F C V was m u c h higher with the invasive technique. The reasons for these differences are discussed. M F C V measurements are shown to be of diagnostic value in some myopathies, for example myositis. In myopathies with a global reduction of the M F C V the two methods are of equal value: in some cases of longstanding myositis the needle method demonstrated some very slowly conducting fibers which were not detected with the surface method. Key words: Muscle fiber conduction velocity; Surface E M G method; Needle method
Different techniques exist to measure the muscle fiber conduction velocity (MFCV); for a recent review see Arendt-Nielsen and Zwarts (1989). An important division can be made between invasive (needle EMG) and non-invasive (surface EMG) techniques. The first extensive measurements of MFCV were done by Buchthal et al. (1955) by measuring the time delay of action potentials (APs) between 2 recording needles in the muscle and activating the muscle either by electrical stimulation or voluntary contraction. This method was very time consuming and has not gained general application. Troni et al. (1983) suggested an easier approach by measuring the latency of muscle fiber APs with only one recording electrode. Alternatively, the MFCV can be measured with surface electrodes; the most widely used approach
Correspondence to: Dr. Machiel J. Zwarts, MD, Neurological Clinic, Dept. of Clinical Neurophysiology, University Hospital, Oostersingel 59, 9713 EZ Groningen (The Netherlands).
is the cross-correlation technique. The question arises of which grounds to choose for a certain technique. Further, it is known that the surface results are in general higher than the values obtained with needle methods (Sollie et al. 1985; Arendt-Nielsen and Zwarts 1989). As yet, the reasons for this difference are not clear. It was the purpose of this study to investigate the differences, potential benefits and limitations of both methods. This was done by applying the method of Troni and the cross-correlation technique subsequently on the same muscle and to compare the results. In order to show the difference of these 2 methods with respect to pathological muscles, illustrative measurements of several myopathies were chosen.
Methods Both methods have been described in detail (Troni et al. 1983; Zwarts et al. 1988). The estima-
0013-4649/89/$03.50 ~ 1989 Elsevier Scientific Publishers Ireland, Ltd.
MFCV: SURFACE VS. NEEDLE METHOD tion with needles was always done first, because the direction of the muscle fibers was thereby known; this facilitated the positioning of the surface electrodes parallel to the muscle fibers. The needle E M G measurements were done with a Tt~nnies E M G apparatus (Myograph DA IIR), the signals being amplified with a bandpass filter of 500 H z - 1 0 kHz; the time base was 5 msec per division. Two stimulation electrodes (Disa, 13L64, area of the uninsulated tip: 2 mm 2) were placed in the distal part of the short head of the biceps brachii muscle with the cathode proximal and 2-3 mm from each other. Care was taken to place the electrodes perpendicular to the surface. The muscle was stimulated with gradually increasing strength until a clear twitch was palpable (10-20 V, 0.2 msec, 1 Hz). With the aid of the twitch, the recording electrode (Disa, 13L50) was placed 5 cm proximal and manipulated until APs with the dimensions of fibrillations (bi- or triphasic waves with a duration of 1-5 msec and an amplitude of 20-500 /~V) were seen. After some preliminary experiments we preferred to use a standard concentric E M G needle instead of the single fiber electrode used by Troni, because this resulted in easier finding of more spikes. The resulting APs were generally biphasic, initially positive, spikes. The latency was measured at the initial positive turn. In the case of late potentials 4-trace storage was used to ensure the stimulus-locked occurrence of the APs. As an arbitrary criterion only spikes larger than 0.1 mV were used for the calculations. The measurements were repeated 3 times after small displacements of the electrodes. The mean value of the 3 average MFCV results was used for calculations. Subsequently, the surface E M G records were made from the same place of the muscle, between the motor point and the tendon. The direction of the electrode parallel to the muscle fibers was chosen with the aid of the puncture sites of the needles between the motor point and the distal tendon. The skin was cleaned with alcohol and lightly abraded. Three round bipolar brass electrodes (with a diameter of 2 mm) were used, placed in a longitudinal array, 1 cm apart and the center electrode in common. The force was measured at the wrist with strain gauges and displayed
545 on a voltmeter in front of the subject. The signals were amplified with a Disa E M G amplifier, type 14C13, bandpass 20-2000 Hz, and epochs of 200 msec were digitized with a sampling rate of 6024 Hz on a PDP 11/23 computer. The delay between the two signals was estimated with the cross-correlation technique after interpolation, which raised the sample frequency to 12,000 Hz. The measurements were made twice at different (isometric) contraction levels, from low to maximal in steps of 20 or 40 N, depending on the maximal force; this resulted generally in 4 - 5 steps. Only correlation coefficients higher than 0.85 were accepted. The mean value of these MFCV results was used for calculations. The difference between the fastest and the slowest conduction velocity (range) was expressed as a ratio for both methods: the fastest divided by the slowest MFCV result (F/S). The subjects were 7 healthy males and 7 females, aged 24-44 years. The patients were selected for the illustrative character of the measurements and included 4 myositis patients (the diagnosis being based on proximal muscle weakness, concentric needle E M G findings of myopathic motor units, raised C K and biopsy), one with familial hypokalemic periodic paralysis (from the kinship described in Zwarts et al. 1988) and one with an undetermined myopathy, presumably alcoholic. The relation between variables was analyzed with linear regression analysis, the difference between the paired results with the sign test.
Results The relations between the mean values of the surface and needle estimates (S-MFCV and NMFCV respectively) are shown in Fig. 1. Note that in all cases the surface E M G values were higher than the needle estimates. A clear correlation existed between the results of the two methods. S-MFCV = 1.1 + 1.0 x N-MFCV (n = 20, r = 0.76, P < 0.001). For the different groups, the relation was significant for the male controls (SMFCV=0.5+I.2×N-MFCV, r=0.78, P< 0.05) and the myopathies (S-MFCV = 0.3 + 1.3 x
546
M.J. ZWARTS
non-invasive MFCV (re.s-'}
control
~/-- 3.| m.s" I
6
o°
5 ¸
~1~l W'~-
V-- 4.2 m.s"
-
× o~ 4-
3-
- J 500/uV
."
/
~* female male
5ms
Fig. 2. Examples of conduction velocity measurements with needle recording. Note the late potentials in both myositis patients.
• myopathy
"J
:3
'~
5 invasive MFCV (m.s-')
Fig. 1. The relation between the mean muscle fiber conduction estimation with the invasive and non-invasive method. Note that all data lie above the line: y = x, The 2 data points of the patients with a high conduction velocity are from the cases with long standing myositis.
N-MFCV, r = 0.9, P < 0.01) but not for the female controls. The results of both methods are summarized in Table I. For both controls and patients N-MFCV was always lower than S-MFCV ( P < 0.001, sign test), the mean difference was 1.0 m/sec. The fastest divided by the slowest MFCV ( F / S ratio) was for all the investigated subjects - including the patients - higher with the invasive method (see Table I), indicating a larger range of velocities with the invasive method. Note that the F / S ratio of all myopathy patients was much higher than the control values for the invasive, but not for the non-invasive method. A slight, but
significant relation between force and S-MFCV of the controls was found (r = 0.19, P = 0.029, n =
130). The MFCV of the myositis patients was either higher or lower than the normal values (see Fig. 1). The disease duration of the two myositis patients with low CVs was 1 and 4 months; for the patients with a high MFCV this was 2 and 6 years. Examples of the invasive measurements are given in Fig. 2. Note the late spikes in both myositis patients, resulting in a high F / S ratio.
Discussion The clear correlation between MFCV values found with both methods can be regarded as a validation of the surface E M G method. The lack of a significant relation for females could be due
TABLE I Results of muscle fiber conduction estimation with an invasive and a non-invasive method. Muscle fiber conduction ( m / s e c mean 4- S.D,)
F a s t / s l o w ratio (range)
Invasive
Non-invasive
Invasive
Non-invasive
Controls Male (n = 7) Female (n = 7)
3.2_+0.3 3.1 _+0.4
4.25:0.5 * 4.0_+0.3 *
1.48 (1.2-1.7) 1.45 (1.3-1.7)
1.17 (1.1-1.3) * 1.17 (1.1--1.3) *
Myopathy patients (n = 6)
2.7 _+0.7
3.9_+ 1.1 *
2.92 (2.2-4.1)
1,12 (1.1--1.2) *
n = number of persons. * Significantly different from the value of the invasive method (P < 0.05).
MFCV: SURFACE VS. NEEDLE METHOD to the smallness of the subgroup. The fact that the type II fibers of females have no larger diameter than the type I fibers could perhaps also account for this finding (because MFCV is related to the diameter of the fiber, see below). The difference found between the two methods indicates a systematic higher estimation of about 1 m / s e c with the non-invasive technique. The mean values of the MFCV and the systematic differences between the two methods both agree with the literature (Sollie et al. 1985; Arendt-Nielsen and Zwarts 1989). Several factors could contribute to this difference: (1) MFCV is dependent on the stimulus frequency. The frequency of stimulation with the needle method is 1 Hz. With surface EMG, the measurements are made during voluntary contraction. The firing rate is known to lie between 8 and 20 Hz. Between 10 and 20 Hz the MFCV increases with a mean of 10-20% (Stflberg 1966; Morimoto and Masuda 1984). (2) Every misdirection of the surface electrodes leads to too high an estimation, although this influence is only small (Sollie et al. 1985). A misdirection with the needle method leads also to a wrong estimate, but not in a systematic way. (3) A further cause of the too high surface E M G values could be a bias towards the fast twitch (type II) motor units (MUs), which are known to have higher conduction velocities (Andreassen and Arendt-Nielsen 1987). This bias could occur because of the larger amplitudes of the type II MU action potentials (Wallinga-De Jonge et al. 1985) or to the more superficial position of the type II MUs (Johnson et al. 1973). (4) It is known that with surface E M G estimation standing waves can occur on both channels (thus without time delay), resulting in too high an estimate (Broman et al. 1985a). This could occur because of end-plates beneath the surface electrode, or due to far-field potentials which can arise at the moment the action potential blocks at the end of the muscle fiber (Gootzen et al. 1988). (5) The high-pass filter of 500 Hz used for needle recording could result in small time shifts of the spikes and consequently a lower MFCV result. This influence needs further investigation. A second important difference between the two methods is the much larger range of velocities obtained with Troni's method. With surface E M G
547 the MFCV increases with higher levels of contraction (Arendt-Nielsen et al. 1984; Broman et al. 1985b; Sadoyama and Masuda 1987; Zwarts et al. 1988), because of the orderly recruitment of the MUs (Henneman's size principle), the MUs recruited at higher forces having higher conduction velocities (Andreassen and Arendt-Nielsen 1987). By measuring from low to high forces, a range of velocities is obtained. The estimation of MFCV with surface E M G is the weighted average of all active MUs; this mean value accounts for the much smaller range of the MFCV as measured with surface EMG. Interestingly, the F / S ratio of the invasive measurements of the myopathy patients was much higher than the control values (2.92 versus 1.46). This is in agreement with the increased fiber diameter variability found in most myopathies, resulting in a large range of conduction velocities, because of the dependence of the MFCV on the fiber diameter (HLkansson 1956). Other pathological alterations of the muscle such as fiber splitting could also contribute to an increased variability. The much larger F / S ratio found in the different myopathies - partly due to several very slow conducting fibers - was totally absent in the surface E M G measurements (see Table I). Moreover, the variability of the surface E M G values in these myopathies was even slightly lower than the F / S ratio of the controls. The slow conducting APs stem probably from small, atrophic fibers; the small amplitude of these spikes hardly influences the surface record. Further, the variability of the surface E M G MFCV results from the recruitment order; in myopathies it is well known that early recruitment occurs at slight voluntary contraction. Thereby, the difference between MFCV at low and high forces could be less marked. Of course, in myopathies other factors could play a role, such as a predominant involvement of one motor unit type. A reduced MFCV could be demonstrated with both methods in the patient with hypokalemic periodic paralysis. In several myopathies in which an affection of the membrane exists, a global reduction of the MFCV could be demonstrated with surface E M G (Zwarts et al. 1988; Zwarts and Van Weerden 1989). The results obtained in the
548
myositis patients agree with the findings of Troni et al. (1988). In the 2 cases with acute myositis, MFCV was found to be severely reduced with both methods. The 2 cases with long standing myositis showed a relatively high MFCV with both methods, probably due to the development of hypertrophic muscle fibers as an adaptation to the paresis. In these 2 cases several very slowly conducting fibers (see Fig. 2) were demonstrated with the invasive method, indicating the existence of pathological, probably atrophic, fibers. In conclusion, both needle and surface EMG measurements result in reliable estimates of human muscle fiber conduction velocity. The invasive method is painful but requires only minimal patient cooperation. It gives a good indication of the variability of MFCV; this is of diagnostic value especially in myositis. With surface EMG the estimate is systematically higher. This method is only applicable to a few muscles. An advantage is its painless character and the possibility to measure at different force levels and during continuous contraction. This method is suitable for studying the changes of the MFCV during fatigue. In myopathies with a global reduction of MFCV the two methods have equal value. Alice Burgler, Carla Klein Geltink, Jarmy Van Marwijk and Agnes Wijnandts are thanked for technical assistance. T o m Van Weerden is acknowledged for a helpful review of the article.
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