JOURNAL OF NEUROTRAUMA Volume 7, Number 2, 1990 Mary Ann Liebert, Inc., Publishers
Quantitative Evaluation of Hemiparesis with
Corticomyographic Motor Evoked Potential Recorded by Transcranial Magnetic Stimulation JIAN
XING,1 YOICHI KATAYAMA, TAKAMITSU YAMAMOTO, TERUYASU HIRAYAMA, and TAKASHI TSUBOKAWA
ABSTRACT motor evoked potentials (MEP) activated by transcranial magnetic stimulation of the motor cortex provide clinicians with an opportunity to evaluate corticospinal motor systems quantitatively and noninvasively. Threshold, amplitude, and latency of the corticomyographic MEP, however, are variable between subjects mainly because current directions and intensities induced by magnetic stimulation cannot be determined precisely due to anatomical variations of subjects. The variability of corticomyographic MEPs has limited the use of corticomyographic MEP for evaluating mild changes in corticospinal motor function. In the present study, we used an internal standard to assess hemiplegia, expressing relative amplitude, latency, and threshold of responses on the paretic side as a function of responses elicited from the intact side (%MEP). Neurological function of paretic muscles, as determined by a muscle maneuver test (MMT), clearly correlated to %MEP threshold, amplitude, and latency. Since corticomyographic MEP are similar when recorded from symmetrical sites on two extremities of normal subjects, %MEP provided a sensitive measure of mild hemiparesis. The %MEP approach revealed abnormal MMT scores of 3 or 4 more frequently than did standard MEP approaches. %MEP amplitude was more sensitive to mild hemiparesis than %MEP latency or %MEP threshold. Since magnetic stimulation with a safe intensity range cannot reliably produce corticomyographic MEP in severely paretic muscles with MMT scores of 2 or less, the MEP appears to be most useful for evaluating mild hemiparesis. This technique should expand significantly the clinical usefulness of corticomyographic MEP in neurosurgical practice.
Corticomyographic
INTRODUCTION
The Morton, 1980; al., 1986;
transcranial electrical stimulation of the motor cortex (Merton and Marsden et al., 1983; Levy et al., 1984; Rossini et al., 1985; Tsubokawa, 1985; Boyd Katayama et al., 1988c) has provided clinicians with an opportunity to evaluate the function of the
ELECTROMYOGRAPHic response to
et
of Neurological Surgery, Nihon University School of Medicine, Tokyo 173, Japan. Department 1 Present address: Division of Neurosurgery, Beijin Neurosurgical Institute, Tiantan Xili, Beijin, China.
57
XING ET AL. Recent advances in technology for magnetic stimulation (Barker et al., 1985,1986; Hess et al., 1986; Mills et al., 1987) have further facilitated studies of corticomyographic motor evoked potentials (MEP). Magnetic stimulation can more effectively activate the brain without direct contact with the scalp and produces less discomfort compared to electrical stimulation. Application of the corticomyographic MEP with magnetic stimulation thus appears to be useful for monitoring corticospinal motor function during therapy. Corticomyographic MEPs, however, are relatively insensitive to small changes in motor function. This is because MEP amplitudes and latencies are widely variable across subjects. In our experience, MEP amplitudes vary with standard deviations exceeding 30% of means. Corticomyographic MEP latencies depend on the length of the extremities and the stimulation intensity, which cannot be quantified precisely in magnetic stimulation. The intensity and direction of the cortical currents induced by magnetic stimulation are difficult to predict at least in currently available devices. Such variability in amplitude and latency limits the usefulness of corticomyographic MEP for evaluating mild losses of corticospinal motor function. In the present study, we evaluated hemiparetic subjects by comparing corticomyographic MEPs recorded from symmetrical sites on two extremities. Since normal subjects tend to have similar MEP latencies and amplitudes when recorded from symmetrical sites, use of the MEP recorded from the intact side as an internal standard should increase the sensitivity of the test to small changes in corticospinal motor function. If true, this approach should significantly expand the usefulness of the corticomyographic MEP in neurosurgical practice.
corticospinal motor system quantitatively and noninvasively.
MATERIALS AND METHODS A total of 25 male and 24 female subjects were studied. Their ages ranged from 14 to 62 years. The population included 17 normal, right-handed subjects and 32 patients with unilateral intracerebral organic lesions (brain trauma, brain tumor, hypertensive intracerebral hemorrhage, and cerebral infarct). Among the 32 patients, 22 had hemiparesis, and the remaining 10 had no motor deficits. All the patients gave informed consent.
Neurological function of each paretic muscle was graded by the muscle maneuver test (MMT) (Table 1) described by DeJong (1955). The motor cortex was stimulated transcranially with a coil (Magstim Model 200, Novametrix Medical System, Inc., U.K.) placed tightly in contact with the scalp. The intensity of the stimuli was expressed as a percentage of the maximum output of the device (400 nm, 2.0 tesla). Stimuli were applied at 20-sec intervals. The intensity was decreased stepwise at 10% intervals for determining threshold until the corticomyographic MEP was no longer observed. The threshold was lowest when the coil was centered on the Table 1.
Muscle Maneuver Test (MMT)
Grade
Description
0
3
No muscular contraction. A flicker, or trace, of contraction, without actual movement, or contraction may be palpated in the absence of apparent movement; no motion of joints (10%). The muscle moves the part through a partial arc of movement with gravity eliminated (25%). The muscle completes the whole arc of movement against
4
The muscle
1
2
5
gravity (50%). completes the whole arc of movement against gravity together with variable amounts of resistance (75%). The muscle completes the whole arc of movement against gravity and maximum amounts of resistance several times without signs of fatigue; this is normal muscular power (100%).
From
DeJong (1955). 58
EVALUATION OF HEMIPARESIS WITH MEP vertex. However, the optimum orientations of the coil for the left and right responses were opposite each other. Stimulus thresholds depended on scalp location of the coil. For any given muscle, we first determined the location and direction of the coil that produced MEP with the lowest threshold. The threshold, amplitudes, and latencies of the responses were then compared between symmetrically placed recording sites in the left and
right arms. The corticomyographic responses were recorded with two 5-mm diameter surface electrodes (of the type used for recording electrocardiograms) separated by 10 mm. The data reported here are from thenar or extensor carpi muscles. Results obtained from other flexor and extensor muscles in the upper extremities were essentially similar. The recordings were always made from symmetrical sites on left and right extremities. The signals were led to an amplifier (7S12, NEC San-ei Inc., Japan) with a bandpass of 15 Hz to 3 kHz. The responses were displayed on a visual display unit and also recorded on an X-Y plotter. Response amplitudes were measured as peak-to-peak. Latencies were measured from the stimulus to the onset of earliest detectable muscle activity. Spontaneous electromyographic activity was always monitored to ensure the absence of background activity that can affect the MEP. The response amplitudes and latencies of the paretic side were expressed as percentages of those responses elicited in the contralateral intact side, based on an
average of five responses.
RESULTS The stimulus thresholds in normal subjects at rest were 60-70% of maximum stimulus intensity. Although MEP could be recorded from the lower extremities, high-intensity stimuli of 80-90% were required. Response amplitudes increased and latencies decreased as stimulus intensities were increased (Fig. 1). Latency changes were less dramatic than amplitude changes. The absolute response amplitudes at any given stimulus intensity varied with >30% standard coefficients of variation. Response latencies varied with > 10% standard coefficients of variation. The variations in responses were normally distributed, and hence the normal range was designated as mean ± 2 SD. Hemiparetic patients had increased threshold and latencies of corticomyographic MEPs with variable decreases in amplitude (Figs. 2 and 3). Amplitude changes dominated. In mildly paretic muscles with a MMT score of 4 (Table 1), only 2 of 7 patients had amplitude decreases below normal range. None of these muscles had increased threshold or latencies exceeding the normal ranges. Thus, absolute amplitude and latency measurements in corticomyographic MEPs were unable to detect mild paresis reliably. Relative thresholds, amplitudes, and latencies of corticomyographic MEPs were expressed as a function of the contralateral side.
left side/right side 100 right side/left side %MEP of the paretic muscle 100 paretic side/intact side %MEP of the left muscle %MEP of the right muscle
=
100
=
•
•
=
•
Amplitude and latencies were measured from responses elicited at 100% stimulus intensity. The %MEP values of latency, amplitude, and thresholds showed relatively little variation in normal subjects (Table 2) and were normally distributed %MEP values. Left side %MEP values did not differ significantly from right side values in normal subjects. The %MEP values of responses in paretic muscles correlated well with MMT scores (Figs. 3 and 4). No paretic muscles with MMT scores of 2 or less showed corticomyographic MEP responses. Two of 3 patients with paretic muscles and MMT scores of 3 had responses, all with %MEP amplitudes of
Quantitative Evaluation of Hemiparesis with
Corticomyographic Motor Evoked Potential Recorded by Transcranial Magnetic Stimulation JIAN
XING,1 YOICHI KATAYAMA, TAKAMITSU YAMAMOTO, TERUYASU HIRAYAMA, and TAKASHI TSUBOKAWA
ABSTRACT motor evoked potentials (MEP) activated by transcranial magnetic stimulation of the motor cortex provide clinicians with an opportunity to evaluate corticospinal motor systems quantitatively and noninvasively. Threshold, amplitude, and latency of the corticomyographic MEP, however, are variable between subjects mainly because current directions and intensities induced by magnetic stimulation cannot be determined precisely due to anatomical variations of subjects. The variability of corticomyographic MEPs has limited the use of corticomyographic MEP for evaluating mild changes in corticospinal motor function. In the present study, we used an internal standard to assess hemiplegia, expressing relative amplitude, latency, and threshold of responses on the paretic side as a function of responses elicited from the intact side (%MEP). Neurological function of paretic muscles, as determined by a muscle maneuver test (MMT), clearly correlated to %MEP threshold, amplitude, and latency. Since corticomyographic MEP are similar when recorded from symmetrical sites on two extremities of normal subjects, %MEP provided a sensitive measure of mild hemiparesis. The %MEP approach revealed abnormal MMT scores of 3 or 4 more frequently than did standard MEP approaches. %MEP amplitude was more sensitive to mild hemiparesis than %MEP latency or %MEP threshold. Since magnetic stimulation with a safe intensity range cannot reliably produce corticomyographic MEP in severely paretic muscles with MMT scores of 2 or less, the MEP appears to be most useful for evaluating mild hemiparesis. This technique should expand significantly the clinical usefulness of corticomyographic MEP in neurosurgical practice.
Corticomyographic
INTRODUCTION
The Morton, 1980; al., 1986;
transcranial electrical stimulation of the motor cortex (Merton and Marsden et al., 1983; Levy et al., 1984; Rossini et al., 1985; Tsubokawa, 1985; Boyd Katayama et al., 1988c) has provided clinicians with an opportunity to evaluate the function of the
ELECTROMYOGRAPHic response to
et
of Neurological Surgery, Nihon University School of Medicine, Tokyo 173, Japan. Department 1 Present address: Division of Neurosurgery, Beijin Neurosurgical Institute, Tiantan Xili, Beijin, China.
57
XING ET AL. Recent advances in technology for magnetic stimulation (Barker et al., 1985,1986; Hess et al., 1986; Mills et al., 1987) have further facilitated studies of corticomyographic motor evoked potentials (MEP). Magnetic stimulation can more effectively activate the brain without direct contact with the scalp and produces less discomfort compared to electrical stimulation. Application of the corticomyographic MEP with magnetic stimulation thus appears to be useful for monitoring corticospinal motor function during therapy. Corticomyographic MEPs, however, are relatively insensitive to small changes in motor function. This is because MEP amplitudes and latencies are widely variable across subjects. In our experience, MEP amplitudes vary with standard deviations exceeding 30% of means. Corticomyographic MEP latencies depend on the length of the extremities and the stimulation intensity, which cannot be quantified precisely in magnetic stimulation. The intensity and direction of the cortical currents induced by magnetic stimulation are difficult to predict at least in currently available devices. Such variability in amplitude and latency limits the usefulness of corticomyographic MEP for evaluating mild losses of corticospinal motor function. In the present study, we evaluated hemiparetic subjects by comparing corticomyographic MEPs recorded from symmetrical sites on two extremities. Since normal subjects tend to have similar MEP latencies and amplitudes when recorded from symmetrical sites, use of the MEP recorded from the intact side as an internal standard should increase the sensitivity of the test to small changes in corticospinal motor function. If true, this approach should significantly expand the usefulness of the corticomyographic MEP in neurosurgical practice.
corticospinal motor system quantitatively and noninvasively.
MATERIALS AND METHODS A total of 25 male and 24 female subjects were studied. Their ages ranged from 14 to 62 years. The population included 17 normal, right-handed subjects and 32 patients with unilateral intracerebral organic lesions (brain trauma, brain tumor, hypertensive intracerebral hemorrhage, and cerebral infarct). Among the 32 patients, 22 had hemiparesis, and the remaining 10 had no motor deficits. All the patients gave informed consent.
Neurological function of each paretic muscle was graded by the muscle maneuver test (MMT) (Table 1) described by DeJong (1955). The motor cortex was stimulated transcranially with a coil (Magstim Model 200, Novametrix Medical System, Inc., U.K.) placed tightly in contact with the scalp. The intensity of the stimuli was expressed as a percentage of the maximum output of the device (400 nm, 2.0 tesla). Stimuli were applied at 20-sec intervals. The intensity was decreased stepwise at 10% intervals for determining threshold until the corticomyographic MEP was no longer observed. The threshold was lowest when the coil was centered on the Table 1.
Muscle Maneuver Test (MMT)
Grade
Description
0
3
No muscular contraction. A flicker, or trace, of contraction, without actual movement, or contraction may be palpated in the absence of apparent movement; no motion of joints (10%). The muscle moves the part through a partial arc of movement with gravity eliminated (25%). The muscle completes the whole arc of movement against
4
The muscle
1
2
5
gravity (50%). completes the whole arc of movement against gravity together with variable amounts of resistance (75%). The muscle completes the whole arc of movement against gravity and maximum amounts of resistance several times without signs of fatigue; this is normal muscular power (100%).
From
DeJong (1955). 58
EVALUATION OF HEMIPARESIS WITH MEP vertex. However, the optimum orientations of the coil for the left and right responses were opposite each other. Stimulus thresholds depended on scalp location of the coil. For any given muscle, we first determined the location and direction of the coil that produced MEP with the lowest threshold. The threshold, amplitudes, and latencies of the responses were then compared between symmetrically placed recording sites in the left and
right arms. The corticomyographic responses were recorded with two 5-mm diameter surface electrodes (of the type used for recording electrocardiograms) separated by 10 mm. The data reported here are from thenar or extensor carpi muscles. Results obtained from other flexor and extensor muscles in the upper extremities were essentially similar. The recordings were always made from symmetrical sites on left and right extremities. The signals were led to an amplifier (7S12, NEC San-ei Inc., Japan) with a bandpass of 15 Hz to 3 kHz. The responses were displayed on a visual display unit and also recorded on an X-Y plotter. Response amplitudes were measured as peak-to-peak. Latencies were measured from the stimulus to the onset of earliest detectable muscle activity. Spontaneous electromyographic activity was always monitored to ensure the absence of background activity that can affect the MEP. The response amplitudes and latencies of the paretic side were expressed as percentages of those responses elicited in the contralateral intact side, based on an
average of five responses.
RESULTS The stimulus thresholds in normal subjects at rest were 60-70% of maximum stimulus intensity. Although MEP could be recorded from the lower extremities, high-intensity stimuli of 80-90% were required. Response amplitudes increased and latencies decreased as stimulus intensities were increased (Fig. 1). Latency changes were less dramatic than amplitude changes. The absolute response amplitudes at any given stimulus intensity varied with >30% standard coefficients of variation. Response latencies varied with > 10% standard coefficients of variation. The variations in responses were normally distributed, and hence the normal range was designated as mean ± 2 SD. Hemiparetic patients had increased threshold and latencies of corticomyographic MEPs with variable decreases in amplitude (Figs. 2 and 3). Amplitude changes dominated. In mildly paretic muscles with a MMT score of 4 (Table 1), only 2 of 7 patients had amplitude decreases below normal range. None of these muscles had increased threshold or latencies exceeding the normal ranges. Thus, absolute amplitude and latency measurements in corticomyographic MEPs were unable to detect mild paresis reliably. Relative thresholds, amplitudes, and latencies of corticomyographic MEPs were expressed as a function of the contralateral side.
left side/right side 100 right side/left side %MEP of the paretic muscle 100 paretic side/intact side %MEP of the left muscle %MEP of the right muscle
=
100
=
•
•
=
•
Amplitude and latencies were measured from responses elicited at 100% stimulus intensity. The %MEP values of latency, amplitude, and thresholds showed relatively little variation in normal subjects (Table 2) and were normally distributed %MEP values. Left side %MEP values did not differ significantly from right side values in normal subjects. The %MEP values of responses in paretic muscles correlated well with MMT scores (Figs. 3 and 4). No paretic muscles with MMT scores of 2 or less showed corticomyographic MEP responses. Two of 3 patients with paretic muscles and MMT scores of 3 had responses, all with %MEP amplitudes of
