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Anesth Analg 1999;88:568
© 1999 International Anesthesia Research Society

NEUROSURGICAL ANESTHESIA

A Comparison of Myogenic Motor Evoked Responses to Electrical and Magnetic Transcranial Stimulation During Nitrous Oxide/Opioid Anesthesia

Leon H. Ubags, MD, PhD*, Cor J. Kalkman, MD, PhD*, Henk D. Been, MD, PhD{dagger}, Johannis H. Koelman, MD{ddagger}, and Bram W. Ongerboer de Visser, MD, PhD{ddagger}

Departments of *Anesthesiology, {dagger}Orthopedics, and {ddagger}Clinical Neurophysiology, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands

Address correspondence and reprint requests to Cor J. Kalkman, MD, PhD, Department of Anesthesiology, Academic Hospital, University of Amsterdam, P.O. Box 22700, 1100 DE Amsterdam, The Netherlands. Address e-mail to c.j.kalkman{at}amc.uva.nl


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 References
 
Transcranial motor evoked potentials (tc-MEPs) are used to monitor spinal cord integrity intraoperatively. We compared myogenic motor evoked responses with electrical and magnetic transcranial stimuli during nitrous oxide/opioid anesthesia. In 11 patients undergoing spinal surgery, anesthesia was induced with IV etomidate 0.3 mg/kg and sufentanil 1.5 µg/kg and was maintained with sufentanil 0.5 µg · kg-1 · h-1 and N2O 50% in oxygen. Muscle relaxation was kept at 25% of control with IV vecuronium. Electrical stimulation was accomplished with a transcranial stimulator set at maximal output (1200 V). Magnetic transcranial stimulation was accomplished with a transcranial stimulator set at maximal output (2 T). Just before skin incision, triplicate responses to single stimuli with both modes of cortical stimulation were randomly recorded from the tibialis anterior muscles. Amplitudes and latencies were compared using the Wilcoxon signed rank test. Bilateral tc-MEP responses were obtained in every patient with electrical stimulation. Magnetic stimulation evoked only unilateral responses in two patients. With electrical stimulation, the median tc-MEP amplitude was 401 µV (range 145-1145 µV), and latency was 32.8 ± 2.3 ms. With magnetic stimulation, the tc-MEP amplitude was 287 µV (range 64–506 µV) (P < 0.05), and the latency was 34.7 ± 2.1 ms (P < 0.05). We conclude that myogenic responses to magnetic transcranial stimulation are more sensitive to anesthetic-induced motoneural depression compared with those elicited by electrical transcranial stimulation.

Implications: Transcranial motor evoked potentials are used to monitor spinal cord integrity intraoperatively. We compared the relative efficacy of electrical and magnetic transcranial stimuli in anesthetized patients. It seems that myogenic responses to magnetic transcranial stimulation are more sensitive to anesthetic-induced motoneural depression compared with electrical transcranial stimulation.


   Introduction
Top
 Abstract
 Introduction
Methods
 Results
 Discussion
 References
 
Transcranial motor evoked potentials (tc-MEPs) are used to monitor spinal cord motor pathways intraoperatively. tc-MEPs allow early detection of spinal cord dysfunction during the stage of reversible neuronal ischemia. Intraoperative recording of sufficiently reproducible tc-MEP responses is hampered by the fact that anesthetics depress synaptic conduction in motor pathways. Nitrous oxide (1,2), propofol (3), benzodiazepines (3), barbiturates (4), and, in particular, volatile anesthetics (5) severely depress tc-MEP amplitude. It is therefore important to determine the optimal stimulus paradigm to allow tc-MEP monitoring in all patients at risk of iatrogenic spinal cord injury.

Transcranial stimulation can be accomplished using either electrical (6) or magnetic (7) transcranial stimulators. Both methods of transcranial stimulation differ considerably in the way that they achieve cortical motor neuronal depolarization.

Electrical transcranial motor evoked potentials (tcE-MEPs) are obtained by transcranial stimulation of the motor cortex with a specially designed electrical stimulator. These stimulators provide a brief (50 µs) discharge from a 0.1 µF capacitator, with a peak voltage of 600-1200 V. This stimulus is delivered to the scalp via conventional 9-mm electroencephalogram disk electrodes, affixed to the skin with collodion. The electrical current flows primarily through the skin, and only a small portion of current flow reaches the motor cortex, where it may cause motoneuronal depolarization. The use of electrical transcranial stimulation in the intraoperative setting is still considered an experimental procedure by some governmental regulatory agencies.

Magnetic transcranial motor evoked potentials (tcM-MEPs) are obtained by stimulation of the motor cortex with a magnetic stimulator. These stimulators contain a high-energy capacitator bank. When triggered, a very large pulsed current (5000 A, 150 µs) flows through a circular copper coil, inducing a time-varying magnetic field, with a maximum of 2.5 T. The coil is placed in contact with the scalp approximately overlying the appropriate motor area. The magnetic field induces an electrical current in brain tissue, causing depolarization of cortical motor neurons. There is evidence that magnetic activation of pyramidal tracts is achieved via cortical interneurons (8,9).

The purpose of this study was to compare two transcranial stimulation techniques (electrical and magnetic) that have been used clinically to obtain tc-MEPs both in the clinical neurophysiology laboratory and during operations (10–12). To our knowledge, compound muscle action potentials (CMAPs) to the two modalities of transcranial stimulation have not been compared systematically in anesthetized patients.


   Methods
Top
 Abstract
 Introduction
 Methods
Results
 Discussion
 References
 
Eleven neurologically normal patients undergoing spinal surgery with an inherent risk of spinal cord damage gave written, informed consent to participate in this institutionally approved study protocol. Anesthesia was induced using IV etomidate 0.3 mg/kg and sufentanil 1.5 µg/kg and was maintained with sufentanil 0.5 µg · kg-1 · h-1 and N2O 50% in oxygen. Intubation of the trachea was facilitated with IV vecuronium 0.1 mg/kg. Muscle relaxation was monitored electromyographically at the hypothenar eminence using a Datex Relaxograph (Datex, Helsinki, Finland). When the amplitude of the single twitch response recovered to 25% of control, muscle relaxation was kept at this level with vecuronium using a simple on-off closed-loop IV infusion system. At least 30 min after the induction of anesthesia, just before skin incision, three responses to magnetic stimulation and three responses to electrical transcranial stimulation were randomly recorded.

Electrical transcranial stimulation was accomplished with a Digitimer D180A transcranial stimulator (Digitimer Ltd., Welwyn Garden City, UK). With the stimulator output set at 100% (1200 V), stimuli were delivered to the scalp via 9-mm Ag/AgCl disk electrodes with the anode positioned at Cz and a cathode, consisting of interconnected electrodes, mounted at Fz, A1, and A2 (13) (international 10–20 system).

Magnetic transcranial stimulation was accomplished with a Magstim 200 transcranial stimulator (The Magstim Company, Dyfed, UK) set at maximal output (2.5 T). The stimulus was delivered to the scalp via a butterfly-shaped double coil designed to achieve maximal stimulation of the leg area, positioned over the vertex. Before the study data were acquired, several test tc-MEP recordings were obtained with slight variations of the position and angle of the stimulation coil, to establish the coil position that produced maximal tibialis anterior responses. The magnetic coil was the held in this position for the remainder of the study period.

Myogenic responses were recorded as CMAPs from the skin over the left and right tibialis anterior muscles, using adhesive gel Ag/AgCl electrodes (CleartraceTM; Medtronic Andover Medical, Inc., Haverhill, MA) with the active electrode placed over the muscle belly, referenced to an electrode over the muscle tendon. The signal was amplified 5,000–20,000 times (adjusted to obtain maximal vertical resolution) and filtered between 30 and 1500 Hz using a 3-T PS-800 biologic amplifier (Twente Technology Transfer, Twente, The Netherlands). The responses were displayed and stored on a Macintosh Quadra computer (Apple Computer, Cupertino, CA) with 12-bit analog to digital conversion and motor evoked potential acquisition software written with the LabViewTM data acquisition development system (National Instruments, Austin, TX).

Mean tc-MEP amplitude and latency values from the three responses obtained with each stimulation modality were calculated. Amplitude and latency data were compared using the Wilcoxon signed rank test. Amplitudes are presented as medians (10th and 90th percentiles), and latencies are presented as means ± SD. P < 0.05 was considered statistically significant.


   Results
Top
 Abstract
 Introduction
 Methods
 Results
Discussion
 References
 
With electrical stimulation, bilateral tc-MEP responses were obtained in every patient, magnetic stimulation evoked bilateral responses were obtained in 9 of 11 patients, and unilateral responses were obtained in only 2 patients. Figure 1 shows representative tc-MEP waveforms obtained with both electrical and magnetic stimulation. Figure 2 shows box plots of tcE-MEP and tcM-MEP amplitudes.



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  		Figure 1. Representative transcranial motor evoked potential waveforms obtained with both electrical and magnetic stimulation.

 


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  		Figure 2. Transcranial motor evoked potential amplitudes obtained with both stimulation modalities. Horizontal lines indicate 10th, 25th, 50th (median), 75th, and 90th percentiles. *P < 0.05.

 
CMAP amplitude to electrical transcranial stimulation was 401 µV (145–1145 µV), and latency to onset was 32.8 ± 2.3 ms. When magnetic transcranial stimulation was used, amplitude decreased to 287 µV (64–506 µV) (P < 0.05), and latency to onset was prolonged to 34.7 ± 2.1 ms (P < 0.05).


   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
References
 
The results of this study indicate that, with a single stimulus, both modes of transcranial stimulation elicited bilateral myogenic responses >100 µV in most patients. However, the application of magnetic transcranial stimulation results in a lesser tc-MEP amplitude than that achieved with electrical transcranial stimulation. Furthermore, the success rate for obtaining monitorable CMAPs was smaller when magnetic transcranial stimulation was used because unilateral responses only were obtained in two patients.

The main advantage of magnetic versus electric transcranial stimulation is that magnetic stimulation is painless. Pain receptors in the scalp are not stimulated. Therefore, magnetic stimulation can be performed in awake patients to obtain baseline values before the induction of anesthesia. A disadvantage of magnetic stimulation is that it is necessary to have continuous access to the patient’s head during the operation because the magnetic stimulation coil is hand-held. During correction of scoliosis with the Cotrel-Dubousset system, the patient’s head is mounted in a traction frame, and continuous access is not possible. The differences in CMAP amplitudes obtained by electrical and magnetic transcranial stimulation might be explained by a difference in sensitivity to anesthetic-induced depression of the motor system. It has been postulated that CMAPs to magnetic transcranial stimulation are more sensitive to anesthetics than are tcE-MEPs because the signal has to transverse one extra synaptic junction to activate the motor system. Magnetic transcranial stimulation activates cortical interneurons which, in turn, repetitively activate pyramidal cells transsynaptically, resulting in indirect waves (I-waves) along the spinal cord. Electrical transcranial stimulation activates pyramidal cells directly, resulting in both direct waves (D-waves) and I-waves along the spinal cord (8). Hicks et al. (14) studied the effects of isoflurane on electrical tc-MEPs recorded from the epidural space. The administration of isoflurane resulted in a reduction of the number and amplitude of the I-waves, whereas the D-wave was unaffected. This suggests that anesthetics depress the transsynaptic activation of the pyramidal cells by interneural circuits more than the direct activation of the pyramidal cell.

Our observation that reproducible bilateral tcM-MEPs can only be obtained in a subset of patients during anesthesia is consistent with other reports (7,15–17). However, most authors have reported higher success rates when electrical transcranial stimulation was used to monitor the spinal cord intraoperatively (6,18,19).

There are several alternative stimulation paradigms that are believed to result in a more efficient stimulation of the motor cortex and that might, at least partially, overcome the tc-MEP amplitude reduction caused by most anesthetics. The application of an angulated stimulation coil results in both I-waves and D-waves, provided that the coil is precisely orientated to the preferential area of stimulation (20–22). Both this observation and the need for a device that can be affixed to the scalp in the optimal position have led to the development of a "headcap" stimulation coil (23). Lee et al. (24) successfully monitored thenar and tibialis anterior tc-MEPs intraoperatively using a magnetic stimulator and a headcap stimulation coil. The high success rate suggests that the application of a headcap stimulation coil may indeed improve stimulus efficiency intraoperatively. However, both the latency and the amplitude were highly variable within patients, which suggests low-amplitude responses (absolute amplitude values were not mentioned). The anesthetic regimen used consisted only of a continuous etomidate infusion. Etomidate has little effect on tc-MEPs (3,25), and using this particular anesthetic technique may account for the high success rate. Although the authors reported that none of their patients showed signs of postoperative adrenal insufficiency, current opinion is that prolonged etomidate infusions are undesirable (26,27).

Another method to improve stimulus efficacy is the use of multipulse stimulation. The application of two to five successive transcranial electrical or magnetic stimuli results in a greater CMAP amplitude and decreased threshold stimulation intensity in awake patients (28–30). The intraoperative application of electrical multipulse stimulation greatly enhances tc-MEP amplitude. Successful electrical tc-MEP monitoring with multipulse stimulation has been performed during nitrous oxide/opioid anesthesia (31), propofol/opioid total IV anesthesia (32,33), and isoflurane anesthesia (34). Although both electrical and magnetic transcranial stimulators with multipulse capacity are currently commercially available, we are not aware of any reports describing intraoperative CMAP recordings to multipulse transcranial magnetic stimulation. It is conceivable that the application of multiple magnetic stimuli will result in greater intraoperative CMAP amplitudes. Fujiki et al. (22) recorded corticospinal responses to single and duplicate transcranial magnetic stimuli. With paired stimuli, they observed a facilitatory effect on both D- and I-waves. However, multipulse magnetic transcranial stimulators require one extra capacitor bank for every additional stimulus; as a result, they are bulkier and more expensive.

In conclusion, we demonstrated that electrical transcranial stimulation results in CMAPs of larger amplitude than those resulting from magnetic stimulation during nitrous oxide/opioid anesthesia. Smaller size, lower cost, and consistency of stimulation by scalp-affixed stimulation electrodes may make transcranial electrical stimulation preferable for many procedures in which tc-MEPs are to be recorded. However, magnetic stimulators have the advantage that a preoperative baseline measurement can be obtained in the awake patient. The use of multipulse magnetic stimulators may increase the success rate of intraoperative magnetic tc-MEP monitoring.


   Acknowledgments
 
The authors thank Marjolein Porsius, RN, for her valuable help with the intraoperative recordings.


   Footnotes
 
This work was presented, in part, at the annual meeting of the American Society of Anesthesiologists, San Diego, CA, October 1997.


   References
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 

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Accepted for publication December 11, 1998.




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Lippincott, Williams & Wilkins Anesthesia & Analgesia® is published for the International Anesthesia Research Society® by Lippincott Williams & Wilkins with the assistance of Stanford University Libraries' HighWire Press®. Copyright 2006 by the International Anesthesia Research Society. Online ISSN: 1526-7598   Print ISSN: 0003-2999 HighWire Press