Stimulation of lumbosacral nerve roots using a monopolar needle electrode was compared with magnetic stimulation using a 7-cm diameter surface coil. Compound muscle action potentials were recorded from the tibialis anterior (TA) and flexor hallucis brevis (FHB) muscles. Although the mean latency of CMAPs did not differ using the two techniques, amplitudes were considerably larger using a needle. Mean amplitudes were 66% (TA) and 64% (FHB) of the direct M response obtained by distal, supramaximal stimulation compared with mean values using maximal magnetic coil stimulation of 36% (TA) and 25% (FHB). Minimum F-wave latencies from FHB were used to estimate the site of nerve root stimulation using both techniques. Although there was a large amount of variability in the data from individual subjects, the results suggested that, on the average, both forms of stimulation act proximal to the intervertebral foramen. We conclude that a needle electrode is a more suitable technique for stimulating lumbosacral nerve roots. 0 1992 John Wiley & Sons, Inc. Key words: lumbosacral nerve root magnetic stimulation MUSCLE & NERVE 15:885-890 1992
LUMBOSACRAL NERVE ROOT STIMULATION COMPARING ELECTRICAL WITH SURFACE MAGNETIC COIL TECHNIQUES R. A. L. MACDONELL, MD, FRACP, D. CROS, MD, and B. T. SHAHANI, MD, DPhil(0xon)
Electrophysiological detection of pathology affecting lumbosacral nerve roots has proven difficult because of their deep, relatively inaccessible location. Electrical stimulation of these roots can only be performed using high voltage techniques" or by using needle electrodes inserted to the depth of the vertebral Both methods are painful, and the latter is also invasive. Indirect methods, such as F waves, although more tolerable, have proved to have a low sensitivity in the detection of lumbosacral radicu10pathies.l~ The recent development of surface magnetic coil stimulation has allowed deeply situated nerve fibers to be stimulated less painfully.2,6.8~1" Its application to the stimulation of nerve roots has been
From the Spaulding Rehabilitation Hospital, Boston, Massachusetts (Drs. Macdonell and Shahani) and Clinical Neurophysiology Laboratory, Massachusetts General Hospital, Boston, Massachusetts (Drs. Macdonell. Cros, and Shahani)
considered by previous authors mainly in relationship to cervical nerve roots.628It has some drawbacks, most notably the difficulty in evoking a supramaximal response. However, a recent study suggested that magnetic coil stimulation may be useful in the diagnosis of lumbosacral radiculopathies5 T h e object of this study was to examine magnetic coil stimulation of the L-5 and S-1 lumbosacral nerve roots. Our aims were: (1) to determine the optimum site for stimulation of these roots; (2) to determine the optimum direction of current flow within the coil for stimulation; (3) to compare needle electrode with magnetic coil stimulation in terms of latency and amplitude of the evoked response; and (4) by using the minimum F-wave latency from an S1 innervated muscle, to calculate the sites at which stimulation of the S-1 nerve root by the magnetic coil and needle electrode occur. Preliminary findings have already been reported."
Presented in part at the AAEM meeting, Chicago, September 1990 Address reprint requests to Richard Macdonell, MD, FRACP, Department of Neurology, Austin Hospital, Studley Road, Heidelberg, Victoria 3084, Australia Accepted for publication December 1, 1991 CCC 0148-639X/92/080885-06 $04.00 0 1992 John Wiley 8, Sons, Inc.
Lumbosacral Root Stimulation
MATERIALS AND METHODS
Eighteen subjects with no history or electrophysiological evidence of disorders affecting the peripheral nervous system were studied. Their ages ranged from 25 to 72 years, and 10 were males.
MUSCLE & NERVE
August 1992
885
All gave informed consent and the study was approved by the Hospital Ethics Committee. Ag-AgC1 EEG recording electrodes were placed 3 cm apart over the tibialis anterior (TA) (16 subjects) and flexor hallucis brevis (FHB) muscIes bilaterally. Peripheral compound muscle action potentials (CMAPs) were obtained by supramaximal electrical stimulation of the tibia1 nerve at the ankle (FHB) and peroneal nerve at the knee (TA). The minimum F-wave latency was obtained in 12 subjects, by evoking 10 consecutive F responses from FHB using conventional techniques. Lumbosacral magnetic stimulation was performed with the patient comfortably seated, with the back straight and legs extended. A 7-cm mean diameter coil was used with a MAGSTIM 200 stimulator. The coil was placed tangential to the surface with the coil centered over a spinous process and the handle at right angles to the vertebral column. The current pulse through the coil was largely monophasic with a rise time of 75 ks and a maximum duration of less than 1 ms. This produced a magnetic field whose maximum strength was 1.5 T at the centre of the coil. Responses from all 4 muscles were recorded simultaneously using filter settings of 10 Hz to 10 kHz and a gain of 200 IJ.V to 5 mV per centimeter. Sweep duration was 50 ms. Stimulation was performed at the maximum output of the device using both clockwise and counterclockwise directions of current flow in the coil. In all subjects, stimulation was performed with the coil centered over the L-5 and the S-1 spinous processes. In addition, 4 subjects were stimulated from T-12 to S-1 levels inclusive, using both directions of current flow. Needle root electrical stimulation was performed at the L-5 and S-1 levels on each side in addition to magnetic coil stimulation in 14 subjects. A monopolar needle electrode was inserted to the depth of the vertebral lamina 1 cm lateral to the appropriate spinous process. A surface electrode was placed over the spinous process to act as anode. Stimulus intensity was at maximal output (300 V) with a duration of 1 ms. At least 2 stimuli were given at each site to ensure the reproducibility of the response. EMG recordings were made using a 4-channel Mystro electromyograph (Teca Corp.).
Maximal CMAP responses were obtained with the coil centered over L-5 and S-1. Despite a significant increase in amplitude obtained by stimulating more caudally, there was little change in latency of the responses evoked by stimulating at different levels. The mean latency difference was 0.5 ms (SD = 0.7). If only responses over 500 pV are considered, this difference was less, with a mean of 0.25 ms (SD = 0.47). There was no significant difference in the amplitudes of CMAPs from either muscle comparing L-5 with S-1 stimulation.
RESULTS
FIGURE 1. Latencies of CMAPs evoked from tibialis anterior (Tib Ant) and flexor hallucis brevis (FHB) by magnetic coil stim~ ulation of L-3s-1nerve roots plotted against height in 18 normal subjects. The positive correlation between height and CMAP latency was more marked for FHB (r = 0.72) than Tib Ant (r = 0.45).
Optimum Site for C M increased ~ ~ in amp1itude as the 'Oil was moved cauda'ly from T-12. In 3 subjects, responses could not be obtained above L-4 for FHB or above L-2 for TA.
886
Lurnbosacral Root Stimulation
The effects of the direction of coil current flow on CMAPs from FHB and T A following stimulation at L-5 and S-1 were examined in all subjects. N o significant differences emerged for either latency or amplitude that could be related to the direction of current flow. The coil current direction producing the largest amplitude CMAPs on each side was unpredictable. Coil Current Flow Direction.
Stimulation of Lumbosacral Nerve Roots Using the Magnetic Coil. The mean latency of responses
from FHB was 24.9 ms (SD = 2.3 ms) and, from TA, 13.7 ms (SD = 1.6 ms). The mean amplitude of responses from FHB, expressed as a percentage of the CMAP evoked by distal stimulation, was 32% (range: 2% to 100%) and, from TA, 41% (range: 9% to 100%). Interside latency differences for TA and FHB were slight, 0.6 (0.6) ms and 0.7 (0.6) ms, (mean and SD), respectively. There was also less interside variability in amplitude compared with the overall findings. Expressed as a percentage of the peripheral CMAP amplitude,
301
24
r
0 Ti& Ant
Y)
20
X FHB
18
..
60
.
.
.
.
.
.
.
.
.
62
64
66
68
70
72
74
76
78
Height (ins)
MUSCLE & NERVE
August 1992
the mean difference between sides for FHB was 10% (range: 0% to 25%) and, for TA, 21% (range: 2% to 70%). T h e latencies of CMAPs evoked by magnetic coil stimulation showed a positive correlation with subject height (Fig. 1).
A. Mean latency and amplitude values
Needle Electrode Compared With Magnetic Coil Stimulation of Lumbosacral Nerve Roots. Twelve
Muscle
n
Magnet
Needle
Magnet
Needle
Tib. ant. Range FHB Range
12
13.6 (1.2) 11.2-15.8 24.7 (2.2) 20.6-28.9
13.5 (1.2) 11.4-15.9 25.1 (2.0) 21.7-29.7
36 (25) 9-92 25 (17.4) 2-61
66 (31)* 7-100 64 (19)* 25-100
Table 1. A comparison of needle electrical and magnetic coil lumbosacral root stimulation in 14 normal subjects.
Mean amplitude as % of peripheral M response
Mean latency (SD) (ms)
of the 14 subjects studied with both techniques had CMAPs recorded from T A and FHB. In the other 2 subjects, CMAPs were only recorded from FHB. The latency of CMAPs evoked from FHB and TA did not differ significantly comparing electric with magnetic stimulation (Table 1). CMAP amplitudes following needle root stimulation were significantly larger in both muscles compared with magnetic coil stimulation ( P < 0.01) (Figs. 2 and 3).
14
B. Difference in CMAP latencies subtracting the latency using the magnetic coil from that using needle electrical stirnulation Muscle
n
Mean difference (SD) needle-magnet (ms)
Range (ms)
Tib. ant. FHB
12 14
-0.3 (1.O) 0.7 (0.5)
-2.7-0.8 0.1-1.5
*P < 0 01 using the Wilcoxon signed rank test
The magnetic coil preferentially stimulates the lar e fastest-conducting peripheral nerve fibers. F-Wave Latencies and the Site of Stimulation.
5.4
nique with the latency of the F wave. T h e latency of conduction from the anterior horn cell pool to FHB was calculated using the F-wave latency and the distal latency of the direct M response (F latency + M latency - 1) X 0.5.6 Subtraction
These fibers are also responsible for the conduction of F waves.13 Consequently, the site of activation of nerve roots by the magnet can be estimated by comparing the latency to FHB using this tech-
18000
1
0
16000
0 Amplitude FHB (M response) X Amplitude FHB (Magnet) + Amplitude FHB (Needle)
+
14000
5
a m
12000
t
0
a 10000-
D
3
.-
0
8000.
a
X 0
6000-
.
2000-
+
+ 0
1
2
3
0
+
+
0
0
0
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+
X
0
+ 40001
0
4
5
+
X
6
+ 7
8
0
+ x
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jti 9
1
0
1
1
1
2
1
3
+ 1
4
Subject No. FIGURE 2. Comparison of CMAP amplitudes evoked in flexor hallucis brevis (FHB) by supramaximal tibia1 nerve stimulation at the ankle (peripheral M response) and needle electric and magnetic coil stimulation of the S-1 nerve root.
Lumbosacral Root Stimulation
MUSCLE & NERVE
August 1992
887
PERIPHERAL
FIGURE 3. CMAPs recorded in 1 subject from FHB following supramaximal tibia1 nerve stimulation at the ankle (peripheral M response) and needle electric and magnetic coil stimulation of the S-1 nerve root.
of latencies following needle electrode and magnetic coil stimulation from this value gives the time taken for impulses to travel in the fastestconducting fibers from the anterior horn cell pool to the site of stimulation of the needle and magnet respectively. If one assumes a conduction velocity of 50 m/s in these proximal motor roots, the distance between these two points can then be calculated. The mean difference for needle stimulation was 2.6 nis (SD = 1.6 ms), indicating that the mean point of stimulation occurred 13 cm distal to the anterior horn cell pool of S-1. In the case of the magnet, the equivalent figures were 2.7 ms (SD = 1.2 ms) and 13.5 cm, respectively (Table 2). T h e length of the S-1 nerve root measured from its exit from the spinal cord to its termination varies from 15.6 cm to 18.8 cm depending on whether the upper or lower border is m e a ~ u r e d . ' ~ Our results suggest that, on the average, both magnetic coil and needle electrode stimulation of spinal motor nerve roots occurs within the spinal canal prior to the entry of the root into the S1 intervertebral foramen.
DISCUSSION
Lumbosacral nerve roots can be stimulated reliably using the magnetic coil. It was well tolerated and preferred to needle electrode stimulation by those subjects who had both techniques. The optimum site for stimulating S-1 and L-5 nerve roots was with the coil centered over these spinous pro-
888
Lumbosacral Root Stimulation
cesses." Maximal responses from TA and FHB from the two sites varied unpredictably with clockwise and anticlockwise directions of coil current flow. Thus, we advise bilateral recordings using both directions of current flow and stimulation of both L-5 and S-1 vertebral levels to obtain the maximal CMAP response from these muscles. CMAP amplitudes varied widely, both in absolute terms and as a percentage of the peripheral M response, indicating the difficulty in obtaining supramaximal stimulation of nerve roots using this technique. This reduces the usefulness of the test as a means of detecting proximal conduction block. The amplitude of CMAPs evoked by needle electrode stimulation were considerably larger indicating that the needle electrode is more effective than the magnet in stimulating nerve root motor axons. In the individual patient, particularly for FHB, interside differences in CMAP latencies and amplitudes evoked by the magnet varied less. Interside differences may thus be useful in establishing a unilateral conduction abnormality. Comparison of F-wave latencies with the latencies of responses in FHB to needle and magnetic stimulation suggested that both techniques, on the average, stimulate lumbosacral nerve roots proximal to the intervertebral foramen. The lack of change in latency of the motor responses when stimulation is performed at multiple levels implies that there is a low threshold point on the nerve root that is susceptible to stimulation by applied current. This may be due either to
MUSCLE & NERVE
August 1992
Table 2. Latencies to FHB using magnetic and needle electrical lumbosacral stimulation, FHB F-wave latencies, and the latency and distance from the F-wave turnaround point (anterior horn cell) to the point of stimulation using needle and magnetic techniques, assuming a conduction velocity in proximal nerve root segments of 50 m/s.
1 2 3 4 5 6 7
a 9 10 11 12 13 14 15 16 17 18 Mean SD
-
76 65 69 68 64 74 72 63 65 65 69 70 66 65 64 71 72 62 68 4.1
-
-
24.8 29.7 27.8 21.7 22.5 24.2 24.0 26.6 28.0 25.9 23.8 25.7 27.5 23.4 25.4 2.3
28.1 21 .a 25.3 27.5 26.1 27.4 28.9 20.6 22.2 23.0 23.2 25.8 25.3 24.7 23.6 24.5 26.2 24.5 24.9 2.3
56.0 48.2 49.0 54.5 54.5 57.2 54.6 44.5 48.1 47.0 -
2.1 4.0 0.9 2.4 3.9 4.8 1.3 3.2 3.6 2.1 -
5.2 2.5 2.4 2.1 3.3 0.9 -
-
26.0 12.5 12.0 10.5 16.5 4.5 -
-
-
-
-
-
-
-
-
-
-
-
49.6 50.7 51.1 4.1
-
-
-
-
-
-
1.4 2.8 2.7 1.2
0.1 3.9 2.6 1.6
7.0 14.0 13.5 6.1
0.5 19.5 13.0 8.1
+
-
10.5 20.0 4.5 12.0 19.5 24.0 6.5 16.0 18.0 10.5
-
+
Abbreviations: Hi, height; f/(m) (f M - 7)/2minus latency to f H B using the magnet over the lumbosacral spine; fl(n), (f M - 1)/2 minus latency to fHB using the needle electrical stimulation at the lumbosacral spine; D/(m), distance from f-wave turnaround point to point of excitation using the magnet; D/(n), distance from F-wave turnaround point to point of excitation using the needle.
changes in nerve anatomy or to the configuration of electric currents produced in different areas by the stimulus. The transition of central to peripheral myelin is one point at which the characteristics of nerve anatomy change. This zone extends < 1 mm into the lumbosacral nerve roots and lies within the cord in the cervical region.15 It appears unlikely, from our results, that this is the point of lumbosacral nerve root stimulation. It may be important in the cervical region where there is some evidence that stimulation occurs in the vicinity of the exit of the nerve root from the spinal cord.6 T h e next region of anatomical change is where the nerve root alters direction to pass from the spinal canal into the intervertebral foramen. This is also a region where the induced current density in CSF tends to be greater.g The local increase in current density is thought to occur due to the focusing effects of the cavity in bone that the foramen represent^.',^,'^ This effect may explain why there is little change in latency of the response at different lumbar levels.16 Currents are more easly induced in CSF than nervous tissue by either stimulus, and the development of eddy currents together with the focusing effects of the intervertebral foramen will tend to concentrate current in
Lumbosacral Root Stimulation
this area regardless of the level of stimulus.12 The nerve root is surrounded by CSF u p to the extent of the dural sleeve, which ends just before the root enters the intervertebral f ~ r a m e n This . ~ is the point to which induced currents would be maximally focused, and is consistent with the mean point of stimulation obtained in our experiments. As both techniques can stimulate proximal to the most common site of pathology affecting these nerve roots, namely compression in the intervertebral foramen by extruded disc material or osteophytes, both techniques theoretically should be useful in the diagnosis of radiculopathies affecting lumbosacral nerve roots. One approach would be to use the less painful magnetic coil stimulation as a screening procedure. If results are equivocal, the more invasive needle electrode technique could then be used to clarify the findings.
REFERENCES 1. Agnew WF, McCreery DB: Consideration for safety in the use of extracranial stimulation for motor evoked responses. Ncurosurgely 1987;ZO:143- 146. 2. Barker AT, Freeston IL, Jarratt JA: Magnetic stimulation
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of the human brain and peripheral nervous system: An introduction and the results of an initial clinical evaluation. Neurosurgery 1987;m:100- 109. 3. Berger AR, Shahani KT: Electrophysiologic evaluation of spinal cord motor conduction. Muscle N e r v e 1989; 12:976980. 4. Carpenter MB, Sutiri .J: Human Neuroanatomy ( 8 ed). Baltimore, Williams & Wilkins, 1983, pp 1-25. 5. Chokroverty S, Sachdeo R, Dilullo J. Duvoisin RC: Magnetic stimulation in the diagnosis of lumbosacral radiculopathy. J Neurol Neurosurg Psychiatry 1989;52:767-772. 6. Cros D, Chiappa KH, Gominak S, Fang J , Santamaria J , King PJ, Shahani BT: Cervical magnetic stimulation. Neuro1o.q 1990;40:1751- 1756. 7. Cros D, Day TJ, Shahani BT: Spatial dispersion of magnetic stimulation in peripheral nerves. Muscle NenJr 1990;13:1076- 1082. 8. Evans HA, Daube JR, Litchy WJ: A comparison of magnetic and electrical stimulation of spinal nerves. Muscle Neme 1990;13:414-420. 9. Maccabee PJ, Amassian VE, Eberle LP, Rudell AP, Cracco RQ, Lai KS, Somasundarum M: Measurement of the electric field induced into inhomogeneous volume conductors by magnetic coils: Application to human spinal neurogeometry. Electrorncephalogr Clin Neurophysiol 3991;81:224237. 10. Macdonell RAL, Rich JM, Cros D, Shahani RI': 1.umbosac-
890
Lurnbosacral Root Stimulation
ral nerve root stimulation with needle electrode and surface magnetic coil techniques. Muscle Nerue 1990;13:880. 11. Maertens d e Noordhut A, Rothwell JC, 'I'hompson PD, Day BL, Marsden CD: Percutaneous electrical stimulation of lumbosacral roots in man. J Neurol Neurosurg Psychiatry 1988;51: 174- 181. 12. Rosler KM, Hess CW, Schmid UD: Investigation of facial motor pathways by electrical and magnetic stimulation: sites and mechanisms of excitation. J Neurol Neurosurg Psychiatry 1989;52:1149-1156. 13. Shahani BT, Macleod WN, Bertics GM: Minimal F response latencies as a measure of conduction in largest diameter alpha motor neurons. Neurology 1987;37(suppl 1):114. 14. Sunderland S: Avulsion of nerve roots, in Vinken PJ, Bruyn GW (eds): Handbook of Clinzcal Neurology, vol 11, Elsevier, Amsterdam, 1976, pp 393-435. 15. Tarlov IM: Structure of the nerve root. 11: Differentiation of sensory from motor nerve roots. Observations o n identification of function in roots of mixed cranial nerves. Arch Neurol Psychiatry 1937;37: 1338- 1355. 16. Ugawa Y , Rothwell JC, Day BL, Thompson PD, Marsden CD: Magnetic stimulation over the spinal enlargements. J Neurol Neurosurgy Psychiatry 1989;52:1025- 1032. 17. Wilbourn AJ, Aminoff MJ: T h e electrophysiology examination in patients with radiculopathies. Muscle N e r v e 1988;11:1099- 11 14.
MUSCLE & NERVE
August 1992
LUMBOSACRAL NERVE ROOT STIMULATION COMPARING ELECTRICAL WITH SURFACE MAGNETIC COIL TECHNIQUES R. A. L. MACDONELL, MD, FRACP, D. CROS, MD, and B. T. SHAHANI, MD, DPhil(0xon)
Electrophysiological detection of pathology affecting lumbosacral nerve roots has proven difficult because of their deep, relatively inaccessible location. Electrical stimulation of these roots can only be performed using high voltage techniques" or by using needle electrodes inserted to the depth of the vertebral Both methods are painful, and the latter is also invasive. Indirect methods, such as F waves, although more tolerable, have proved to have a low sensitivity in the detection of lumbosacral radicu10pathies.l~ The recent development of surface magnetic coil stimulation has allowed deeply situated nerve fibers to be stimulated less painfully.2,6.8~1" Its application to the stimulation of nerve roots has been
From the Spaulding Rehabilitation Hospital, Boston, Massachusetts (Drs. Macdonell and Shahani) and Clinical Neurophysiology Laboratory, Massachusetts General Hospital, Boston, Massachusetts (Drs. Macdonell. Cros, and Shahani)
considered by previous authors mainly in relationship to cervical nerve roots.628It has some drawbacks, most notably the difficulty in evoking a supramaximal response. However, a recent study suggested that magnetic coil stimulation may be useful in the diagnosis of lumbosacral radiculopathies5 T h e object of this study was to examine magnetic coil stimulation of the L-5 and S-1 lumbosacral nerve roots. Our aims were: (1) to determine the optimum site for stimulation of these roots; (2) to determine the optimum direction of current flow within the coil for stimulation; (3) to compare needle electrode with magnetic coil stimulation in terms of latency and amplitude of the evoked response; and (4) by using the minimum F-wave latency from an S1 innervated muscle, to calculate the sites at which stimulation of the S-1 nerve root by the magnetic coil and needle electrode occur. Preliminary findings have already been reported."
Presented in part at the AAEM meeting, Chicago, September 1990 Address reprint requests to Richard Macdonell, MD, FRACP, Department of Neurology, Austin Hospital, Studley Road, Heidelberg, Victoria 3084, Australia Accepted for publication December 1, 1991 CCC 0148-639X/92/080885-06 $04.00 0 1992 John Wiley 8, Sons, Inc.
Lumbosacral Root Stimulation
MATERIALS AND METHODS
Eighteen subjects with no history or electrophysiological evidence of disorders affecting the peripheral nervous system were studied. Their ages ranged from 25 to 72 years, and 10 were males.
MUSCLE & NERVE
August 1992
885
All gave informed consent and the study was approved by the Hospital Ethics Committee. Ag-AgC1 EEG recording electrodes were placed 3 cm apart over the tibialis anterior (TA) (16 subjects) and flexor hallucis brevis (FHB) muscIes bilaterally. Peripheral compound muscle action potentials (CMAPs) were obtained by supramaximal electrical stimulation of the tibia1 nerve at the ankle (FHB) and peroneal nerve at the knee (TA). The minimum F-wave latency was obtained in 12 subjects, by evoking 10 consecutive F responses from FHB using conventional techniques. Lumbosacral magnetic stimulation was performed with the patient comfortably seated, with the back straight and legs extended. A 7-cm mean diameter coil was used with a MAGSTIM 200 stimulator. The coil was placed tangential to the surface with the coil centered over a spinous process and the handle at right angles to the vertebral column. The current pulse through the coil was largely monophasic with a rise time of 75 ks and a maximum duration of less than 1 ms. This produced a magnetic field whose maximum strength was 1.5 T at the centre of the coil. Responses from all 4 muscles were recorded simultaneously using filter settings of 10 Hz to 10 kHz and a gain of 200 IJ.V to 5 mV per centimeter. Sweep duration was 50 ms. Stimulation was performed at the maximum output of the device using both clockwise and counterclockwise directions of current flow in the coil. In all subjects, stimulation was performed with the coil centered over the L-5 and the S-1 spinous processes. In addition, 4 subjects were stimulated from T-12 to S-1 levels inclusive, using both directions of current flow. Needle root electrical stimulation was performed at the L-5 and S-1 levels on each side in addition to magnetic coil stimulation in 14 subjects. A monopolar needle electrode was inserted to the depth of the vertebral lamina 1 cm lateral to the appropriate spinous process. A surface electrode was placed over the spinous process to act as anode. Stimulus intensity was at maximal output (300 V) with a duration of 1 ms. At least 2 stimuli were given at each site to ensure the reproducibility of the response. EMG recordings were made using a 4-channel Mystro electromyograph (Teca Corp.).
Maximal CMAP responses were obtained with the coil centered over L-5 and S-1. Despite a significant increase in amplitude obtained by stimulating more caudally, there was little change in latency of the responses evoked by stimulating at different levels. The mean latency difference was 0.5 ms (SD = 0.7). If only responses over 500 pV are considered, this difference was less, with a mean of 0.25 ms (SD = 0.47). There was no significant difference in the amplitudes of CMAPs from either muscle comparing L-5 with S-1 stimulation.
RESULTS
FIGURE 1. Latencies of CMAPs evoked from tibialis anterior (Tib Ant) and flexor hallucis brevis (FHB) by magnetic coil stim~ ulation of L-3s-1nerve roots plotted against height in 18 normal subjects. The positive correlation between height and CMAP latency was more marked for FHB (r = 0.72) than Tib Ant (r = 0.45).
Optimum Site for C M increased ~ ~ in amp1itude as the 'Oil was moved cauda'ly from T-12. In 3 subjects, responses could not be obtained above L-4 for FHB or above L-2 for TA.
886
Lurnbosacral Root Stimulation
The effects of the direction of coil current flow on CMAPs from FHB and T A following stimulation at L-5 and S-1 were examined in all subjects. N o significant differences emerged for either latency or amplitude that could be related to the direction of current flow. The coil current direction producing the largest amplitude CMAPs on each side was unpredictable. Coil Current Flow Direction.
Stimulation of Lumbosacral Nerve Roots Using the Magnetic Coil. The mean latency of responses
from FHB was 24.9 ms (SD = 2.3 ms) and, from TA, 13.7 ms (SD = 1.6 ms). The mean amplitude of responses from FHB, expressed as a percentage of the CMAP evoked by distal stimulation, was 32% (range: 2% to 100%) and, from TA, 41% (range: 9% to 100%). Interside latency differences for TA and FHB were slight, 0.6 (0.6) ms and 0.7 (0.6) ms, (mean and SD), respectively. There was also less interside variability in amplitude compared with the overall findings. Expressed as a percentage of the peripheral CMAP amplitude,
301
24
r
0 Ti& Ant
Y)
20
X FHB
18
..
60
.
.
.
.
.
.
.
.
.
62
64
66
68
70
72
74
76
78
Height (ins)
MUSCLE & NERVE
August 1992
the mean difference between sides for FHB was 10% (range: 0% to 25%) and, for TA, 21% (range: 2% to 70%). T h e latencies of CMAPs evoked by magnetic coil stimulation showed a positive correlation with subject height (Fig. 1).
A. Mean latency and amplitude values
Needle Electrode Compared With Magnetic Coil Stimulation of Lumbosacral Nerve Roots. Twelve
Muscle
n
Magnet
Needle
Magnet
Needle
Tib. ant. Range FHB Range
12
13.6 (1.2) 11.2-15.8 24.7 (2.2) 20.6-28.9
13.5 (1.2) 11.4-15.9 25.1 (2.0) 21.7-29.7
36 (25) 9-92 25 (17.4) 2-61
66 (31)* 7-100 64 (19)* 25-100
Table 1. A comparison of needle electrical and magnetic coil lumbosacral root stimulation in 14 normal subjects.
Mean amplitude as % of peripheral M response
Mean latency (SD) (ms)
of the 14 subjects studied with both techniques had CMAPs recorded from T A and FHB. In the other 2 subjects, CMAPs were only recorded from FHB. The latency of CMAPs evoked from FHB and TA did not differ significantly comparing electric with magnetic stimulation (Table 1). CMAP amplitudes following needle root stimulation were significantly larger in both muscles compared with magnetic coil stimulation ( P < 0.01) (Figs. 2 and 3).
14
B. Difference in CMAP latencies subtracting the latency using the magnetic coil from that using needle electrical stirnulation Muscle
n
Mean difference (SD) needle-magnet (ms)
Range (ms)
Tib. ant. FHB
12 14
-0.3 (1.O) 0.7 (0.5)
-2.7-0.8 0.1-1.5
*P < 0 01 using the Wilcoxon signed rank test
The magnetic coil preferentially stimulates the lar e fastest-conducting peripheral nerve fibers. F-Wave Latencies and the Site of Stimulation.
5.4
nique with the latency of the F wave. T h e latency of conduction from the anterior horn cell pool to FHB was calculated using the F-wave latency and the distal latency of the direct M response (F latency + M latency - 1) X 0.5.6 Subtraction
These fibers are also responsible for the conduction of F waves.13 Consequently, the site of activation of nerve roots by the magnet can be estimated by comparing the latency to FHB using this tech-
18000
1
0
16000
0 Amplitude FHB (M response) X Amplitude FHB (Magnet) + Amplitude FHB (Needle)
+
14000
5
a m
12000
t
0
a 10000-
D
3
.-
0
8000.
a
X 0
6000-
.
2000-
+
+ 0
1
2
3
0
+
+
0
0
0
b
X
X '
+
X
0
+ 40001
0
4
5
+
X
6
+ 7
8
0
+ x
X
jti 9
1
0
1
1
1
2
1
3
+ 1
4
Subject No. FIGURE 2. Comparison of CMAP amplitudes evoked in flexor hallucis brevis (FHB) by supramaximal tibia1 nerve stimulation at the ankle (peripheral M response) and needle electric and magnetic coil stimulation of the S-1 nerve root.
Lumbosacral Root Stimulation
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PERIPHERAL
FIGURE 3. CMAPs recorded in 1 subject from FHB following supramaximal tibia1 nerve stimulation at the ankle (peripheral M response) and needle electric and magnetic coil stimulation of the S-1 nerve root.
of latencies following needle electrode and magnetic coil stimulation from this value gives the time taken for impulses to travel in the fastestconducting fibers from the anterior horn cell pool to the site of stimulation of the needle and magnet respectively. If one assumes a conduction velocity of 50 m/s in these proximal motor roots, the distance between these two points can then be calculated. The mean difference for needle stimulation was 2.6 nis (SD = 1.6 ms), indicating that the mean point of stimulation occurred 13 cm distal to the anterior horn cell pool of S-1. In the case of the magnet, the equivalent figures were 2.7 ms (SD = 1.2 ms) and 13.5 cm, respectively (Table 2). T h e length of the S-1 nerve root measured from its exit from the spinal cord to its termination varies from 15.6 cm to 18.8 cm depending on whether the upper or lower border is m e a ~ u r e d . ' ~ Our results suggest that, on the average, both magnetic coil and needle electrode stimulation of spinal motor nerve roots occurs within the spinal canal prior to the entry of the root into the S1 intervertebral foramen.
DISCUSSION
Lumbosacral nerve roots can be stimulated reliably using the magnetic coil. It was well tolerated and preferred to needle electrode stimulation by those subjects who had both techniques. The optimum site for stimulating S-1 and L-5 nerve roots was with the coil centered over these spinous pro-
888
Lumbosacral Root Stimulation
cesses." Maximal responses from TA and FHB from the two sites varied unpredictably with clockwise and anticlockwise directions of coil current flow. Thus, we advise bilateral recordings using both directions of current flow and stimulation of both L-5 and S-1 vertebral levels to obtain the maximal CMAP response from these muscles. CMAP amplitudes varied widely, both in absolute terms and as a percentage of the peripheral M response, indicating the difficulty in obtaining supramaximal stimulation of nerve roots using this technique. This reduces the usefulness of the test as a means of detecting proximal conduction block. The amplitude of CMAPs evoked by needle electrode stimulation were considerably larger indicating that the needle electrode is more effective than the magnet in stimulating nerve root motor axons. In the individual patient, particularly for FHB, interside differences in CMAP latencies and amplitudes evoked by the magnet varied less. Interside differences may thus be useful in establishing a unilateral conduction abnormality. Comparison of F-wave latencies with the latencies of responses in FHB to needle and magnetic stimulation suggested that both techniques, on the average, stimulate lumbosacral nerve roots proximal to the intervertebral foramen. The lack of change in latency of the motor responses when stimulation is performed at multiple levels implies that there is a low threshold point on the nerve root that is susceptible to stimulation by applied current. This may be due either to
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August 1992
Table 2. Latencies to FHB using magnetic and needle electrical lumbosacral stimulation, FHB F-wave latencies, and the latency and distance from the F-wave turnaround point (anterior horn cell) to the point of stimulation using needle and magnetic techniques, assuming a conduction velocity in proximal nerve root segments of 50 m/s.
1 2 3 4 5 6 7
a 9 10 11 12 13 14 15 16 17 18 Mean SD
-
76 65 69 68 64 74 72 63 65 65 69 70 66 65 64 71 72 62 68 4.1
-
-
24.8 29.7 27.8 21.7 22.5 24.2 24.0 26.6 28.0 25.9 23.8 25.7 27.5 23.4 25.4 2.3
28.1 21 .a 25.3 27.5 26.1 27.4 28.9 20.6 22.2 23.0 23.2 25.8 25.3 24.7 23.6 24.5 26.2 24.5 24.9 2.3
56.0 48.2 49.0 54.5 54.5 57.2 54.6 44.5 48.1 47.0 -
2.1 4.0 0.9 2.4 3.9 4.8 1.3 3.2 3.6 2.1 -
5.2 2.5 2.4 2.1 3.3 0.9 -
-
26.0 12.5 12.0 10.5 16.5 4.5 -
-
-
-
-
-
-
-
-
-
-
-
49.6 50.7 51.1 4.1
-
-
-
-
-
-
1.4 2.8 2.7 1.2
0.1 3.9 2.6 1.6
7.0 14.0 13.5 6.1
0.5 19.5 13.0 8.1
+
-
10.5 20.0 4.5 12.0 19.5 24.0 6.5 16.0 18.0 10.5
-
+
Abbreviations: Hi, height; f/(m) (f M - 7)/2minus latency to f H B using the magnet over the lumbosacral spine; fl(n), (f M - 1)/2 minus latency to fHB using the needle electrical stimulation at the lumbosacral spine; D/(m), distance from f-wave turnaround point to point of excitation using the magnet; D/(n), distance from F-wave turnaround point to point of excitation using the needle.
changes in nerve anatomy or to the configuration of electric currents produced in different areas by the stimulus. The transition of central to peripheral myelin is one point at which the characteristics of nerve anatomy change. This zone extends < 1 mm into the lumbosacral nerve roots and lies within the cord in the cervical region.15 It appears unlikely, from our results, that this is the point of lumbosacral nerve root stimulation. It may be important in the cervical region where there is some evidence that stimulation occurs in the vicinity of the exit of the nerve root from the spinal cord.6 T h e next region of anatomical change is where the nerve root alters direction to pass from the spinal canal into the intervertebral foramen. This is also a region where the induced current density in CSF tends to be greater.g The local increase in current density is thought to occur due to the focusing effects of the cavity in bone that the foramen represent^.',^,'^ This effect may explain why there is little change in latency of the response at different lumbar levels.16 Currents are more easly induced in CSF than nervous tissue by either stimulus, and the development of eddy currents together with the focusing effects of the intervertebral foramen will tend to concentrate current in
Lumbosacral Root Stimulation
this area regardless of the level of stimulus.12 The nerve root is surrounded by CSF u p to the extent of the dural sleeve, which ends just before the root enters the intervertebral f ~ r a m e n This . ~ is the point to which induced currents would be maximally focused, and is consistent with the mean point of stimulation obtained in our experiments. As both techniques can stimulate proximal to the most common site of pathology affecting these nerve roots, namely compression in the intervertebral foramen by extruded disc material or osteophytes, both techniques theoretically should be useful in the diagnosis of radiculopathies affecting lumbosacral nerve roots. One approach would be to use the less painful magnetic coil stimulation as a screening procedure. If results are equivocal, the more invasive needle electrode technique could then be used to clarify the findings.
REFERENCES 1. Agnew WF, McCreery DB: Consideration for safety in the use of extracranial stimulation for motor evoked responses. Ncurosurgely 1987;ZO:143- 146. 2. Barker AT, Freeston IL, Jarratt JA: Magnetic stimulation
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of the human brain and peripheral nervous system: An introduction and the results of an initial clinical evaluation. Neurosurgery 1987;m:100- 109. 3. Berger AR, Shahani KT: Electrophysiologic evaluation of spinal cord motor conduction. Muscle N e r v e 1989; 12:976980. 4. Carpenter MB, Sutiri .J: Human Neuroanatomy ( 8 ed). Baltimore, Williams & Wilkins, 1983, pp 1-25. 5. Chokroverty S, Sachdeo R, Dilullo J. Duvoisin RC: Magnetic stimulation in the diagnosis of lumbosacral radiculopathy. J Neurol Neurosurg Psychiatry 1989;52:767-772. 6. Cros D, Chiappa KH, Gominak S, Fang J , Santamaria J , King PJ, Shahani BT: Cervical magnetic stimulation. Neuro1o.q 1990;40:1751- 1756. 7. Cros D, Day TJ, Shahani BT: Spatial dispersion of magnetic stimulation in peripheral nerves. Muscle NenJr 1990;13:1076- 1082. 8. Evans HA, Daube JR, Litchy WJ: A comparison of magnetic and electrical stimulation of spinal nerves. Muscle Neme 1990;13:414-420. 9. Maccabee PJ, Amassian VE, Eberle LP, Rudell AP, Cracco RQ, Lai KS, Somasundarum M: Measurement of the electric field induced into inhomogeneous volume conductors by magnetic coils: Application to human spinal neurogeometry. Electrorncephalogr Clin Neurophysiol 3991;81:224237. 10. Macdonell RAL, Rich JM, Cros D, Shahani RI': 1.umbosac-
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ral nerve root stimulation with needle electrode and surface magnetic coil techniques. Muscle Nerue 1990;13:880. 11. Maertens d e Noordhut A, Rothwell JC, 'I'hompson PD, Day BL, Marsden CD: Percutaneous electrical stimulation of lumbosacral roots in man. J Neurol Neurosurg Psychiatry 1988;51: 174- 181. 12. Rosler KM, Hess CW, Schmid UD: Investigation of facial motor pathways by electrical and magnetic stimulation: sites and mechanisms of excitation. J Neurol Neurosurg Psychiatry 1989;52:1149-1156. 13. Shahani BT, Macleod WN, Bertics GM: Minimal F response latencies as a measure of conduction in largest diameter alpha motor neurons. Neurology 1987;37(suppl 1):114. 14. Sunderland S: Avulsion of nerve roots, in Vinken PJ, Bruyn GW (eds): Handbook of Clinzcal Neurology, vol 11, Elsevier, Amsterdam, 1976, pp 393-435. 15. Tarlov IM: Structure of the nerve root. 11: Differentiation of sensory from motor nerve roots. Observations o n identification of function in roots of mixed cranial nerves. Arch Neurol Psychiatry 1937;37: 1338- 1355. 16. Ugawa Y , Rothwell JC, Day BL, Thompson PD, Marsden CD: Magnetic stimulation over the spinal enlargements. J Neurol Neurosurgy Psychiatry 1989;52:1025- 1032. 17. Wilbourn AJ, Aminoff MJ: T h e electrophysiology examination in patients with radiculopathies. Muscle N e r v e 1988;11:1099- 11 14.
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