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Anesth Analg 2005;100:440-447 © 2005 International Anesthesia Research Society doi: 10.1213/01.ANE.0000141678.04200.86
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Abstract |
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The quality of intraoperative motor-evoked potentials (MEPs) largely depends on the stimulation pattern and anesthetic technique. Further improvement in intraoperative MEP recording requires exact knowledge of the modifying effects of each of these factors. Accordingly, we designed this study to characterize the modifying effect of different stimulation patterns during different propofol target plasma concentrations (PTPCs) on intraoperatively recorded transcranial electrical MEPs. In 12 patients undergoing craniotomy, stimulation patterns (300–500 V; 100–1000 Hz; 1–5 stimuli) were varied randomly at different PTPCs (2, 4, and 6 µg/mL). Remifentanil was administered unchanged at 0.2 µg · kg–1 · min–1. MEPs were recorded from the thenar and hypothenar muscles. Analysis of MEPs was blinded to the PTPC. Three-way analysis of variance revealed significant main effects of increasing stimulation intensity, frequency, and number of stimuli on MEP amplitude (P < 0.05). Maximum MEP amplitudes and recording success rates were observed with three or more stimuli delivered at 1000 Hz and
150 V. A significant main effect of PTPC (2 vs 4 and 6 µg/mL) on MEP amplitude was observed at the thenar recording site only (P < 0.05). An amplitude ratio calculated from corresponding MEPs evoked by double and quadruple stimulation proved to be insensitive to changes in PTPC. In conclusion, MEP characteristics varied significantly in response to changes in stimulation pattern and less to changes in PTPC. |
Introduction |
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Intraoperative assessment of motor-evoked potentials (MEPs) has gained increasing popularity in routine clinical practice. Although the clinical value of intraoperative MEP monitoring in detecting impending iatrogenic lesions in the motor system at an early, reversible stage is well documented, its intraoperative usefulness has been improved by the introduction of total IV anesthesia protocols (1,2) and repetitive high-frequency stimulation devices (3,4). Despite such technical advances, meaningful interpretation of intraoperative MEP changes relies on suitable recording conditions that minimize alterations in neuronal impulse generation and conduction and that generate reproducible signals. This, in turn, requires detailed knowledge of the effect of anesthetic technique and stimulation pattern on MEP characteristics.
Previous investigations have examined the effect of various anesthetic techniques and stimulation patterns on the quality of intraoperative MEP recording (1,2,5–9). This study was designed to further define the effect of different stimulation patterns (induced by changes in stimulus number, frequency, and intensity) and various propofol target plasma concentrations (PTPCs) on MEPs evoked by repetitive transcranial electrical stimulation during intracranial neurosurgical procedures. We hypothesized that variations in both stimulation pattern and PTPC would modify MEPs. By analyzing the effect of different stimulation patterns on MEP characteristics under surgical anesthesia, this study aimed to further improve the clinical utility of intraoperative MEP monitoring.
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Methods |
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The study protocol complies with the Declaration of Helsinki. After approval by the institutional Medical Ethics Review Board and after we obtained written, informed consent, 12 patients (4 men and 8 women; ASA physical status classification: I, n = 2; II, n = 5; III, n = 5; age: mean, 49 yr; range, 22–67 yr; weight: mean, 73 kg; range, 50–105 kg) admitted for supratentorial intracranial procedures were studied prospectively. Impairment of the muscle groups targeted for intraoperative investigation was excluded by preoperative clinical and neurophysiological assessment, including electromyography.
To minimize the possibility of intraoperative awareness at small PTPCs (see below), all patients were premedicated with 7.5 mg of midazolam by mouth 1 h before the induction of anesthesia. No other centrally acting drugs were administered. On arrival in the operating room, catheters were inserted in peripheral veins and the radial artery on the arm opposite to the MEP recording site for the administration of fluids and IV anesthetics, continuous recording of mean arterial blood pressure (MAP), and regular blood sampling for blood gas analysis (ABL®; Radiometer, Copenhagen, Denmark), respectively. Peripheral oxygen saturation (Spo2) and depth of anesthesia were monitored continuously via pulse oximetry (Siemens, Erlangen, Germany) and electroencephalographic bispectral index (BIS) (10) (BIS-Monitor; Aspect Medical Systems, Newton, MA), respectively.
Anesthesia was induced by continuous IV infusion of remifentanil (0.2–0.5 µg · kg–1 · min–1) and of propofol administered to achieve PTPCs of 4 µg/mL (Alaris TCI/TIVA 9000, incorporating the DiprifusorTM module; Zeneca Pharmaceuticals, Cheshire, UK). Cisatracurium (0.1 mg/kg) was administered to facilitate endotracheal intubation. Oxygenation, ventilation, body temperature, and systemic perfusion pressure were continuously monitored and kept constant. To ensure systemic arterial oxygen partial pressures (Pao2) of >100 mm Hg at all times, fractional inspired oxygen concentration was administered at a minimum of 0.5 in air and was adjusted to maintain Spo2 at 99% throughout the investigation. To ensure a systemic arterial CO2 partial pressure (Paco2) of 30–40 mm Hg, minute ventilation was adjusted to maintain end-tidal partial pressure of CO2 (Petco2) between 25 and 35 mm Hg throughout the investigation. A warming/cooling blanket was used to maintain rectal temperature between 35°C and 37°C. Hypotension (MAP <60 mm Hg in normotensive or <70 mm Hg in hypertensive patients) was treated by IV administration of 1–2 mL of Akrinor® (Cafedrin-HCl/Theodrenalin-HCl) diluted 2:8 with normal saline solution. All vital variables were recorded continuously (SC 9000®; Siemens). Fluid administration was guided by central venous pressure and urine output. All anesthetics were administered by two of the investigators (WB and H-JP). In each patient, PTPCs were varied randomly among 2, 4, and 6 µg/mL (sealed-envelope technique). Throughout the investigation, remifentanil was administered unchanged at 0.2 µg · kg–1 · min–1. After equilibration of each of the PTPCs, the continuously monitored MAP and heart rate values had to have remained within a 5% range for at least 10 min before MEPs were recorded.
MEPs were recorded by standard neurophysiological equipment (Spirit® evoked-potential system; Nicolet Biomedical, Madison, WI). Compound muscle action potentials were derived from hypodermic needle electrodes placed in the abductor pollicis brevis (thenar) and abductor digiti minimi (hypothenar) muscles by using a belly-tendon montage. Electrode impedances <5 k
were accepted (mean electrode impedance, <1 k). The high- and low-pass filters were set at 30 Hz and 3 kHz, respectively. The notch filter was deactivated. The stimulating device (DigitimerTM D185; Digitimer Ltd., Welwyn Garden City, Hertfordshire, UK) was connected to the SpiritTM evoked potential system and served as an external triggering device. It was capable of delivering trains of constant-voltage rectangular electrical stimuli with a duration of 200 µs at frequencies ranging from 100 to 1000 Hz and stimulating intensities of 1–1000 V. Stimuli were delivered transcranially via hypodermic needle electrodes placed ipsilaterally to the craniotomy site at Cz (cathode) and C3 or C4 (anode) according to the international 10/20 system. After craniotomy and dural opening, the study protocol was started.
Each recording cycle assessed MEPs in response to (a) variation in stimulation current (100, 150, 200, 250, or 300 V) at a constant stimulation frequency (500 Hz) and a constant number of stimuli (n = 4), (b) variation in stimulation frequency (100, 200, 500, or 1000 Hz) at a constant stimulation intensity (300 V) and a constant number of stimuli (n = 4), or (c) variation in the number of stimuli (n = 1–5) at a constant stimulation intensity (300 V) and a constant stimulation frequency (500 Hz). Thus, different stimulation patterns were investigated at each of the 3 PTPCs. Two consecutive MEP recordings (separated by 30 s) were performed after each change in stimulation pattern (i.e., 12 x 2 measurements per PTPC). To exclude conditioning effects of repetitive stimulation on MEP characteristics, the stimulation pattern was varied randomly.
Amplitudes were measured from peak to baseline. Latencies were defined as the interval between the onset of the stimulation artifact and the onset of the MEP. MEP amplitudes and latencies were independently reviewed by two investigators blinded to the PTPCs (PCR and KMS). Data evaluated by two investigators were averaged before further processing.
The sample size required to obtain statistical significance was calculated on the basis of MEP amplitude changes during previous studies (2) and the standard threshold for significant MEP amplitude changes (50% of baseline values). Because assessment of all possible combinations between the various stimulation variables (voltage, frequency, and number of stimuli) and PTPCs was not feasible, our study protocol comprised a reduced factorial design. The individual effects of variation in stimulation pattern and PTPC on MEP characteristics were evaluated independently. Each recording cycle consisted of 12 different stimulation patterns applied twice in random order after each change in PTPC. Thus, 24 measurements were performed at each PTPC in each patient. With 3 changes in PTPC, 72 measurements were performed in each individual. A three-way within-subjects (repeated-measures) analysis of variance (ANOVA) was conducted. PTPC, stimulation variables (voltage, frequency, and number of stimuli), and measurement replication were treated as dependent variables (repeated measures). The 3 repeated-measures factors consisted of the following: (a) PTPC (3 levels: 2, 4, and 6 µg/mL), (b) stimulation pattern (5 levels for voltage [100, 150, 200, 250, and 300 V] and number of stimuli [1, 2, 3, 4, or 5 stimuli]; 4 levels for stimulation frequency [100, 200, 500, or 1000 Hz), and (c) replication of each measurement within the randomized stimulation protocol at each PTPC (2 levels). This resulted in a reduced factorial 3 x 5(4) x 2 design adjusting for repeated measures. In addition to the assessment of each factor’s main effect (i.e., collapsing over the remaining factors), as well as two-way and three-way interactions between the repeated-measures factors (ANOVA), the specific effect of each change in stimulation intensity, frequency, and stimulus number on MEP characteristics was evaluated in each level of PTPC and measurement replication by assigning contrast coefficients to the various levels of each factor (contrast analysis). Friedman’s ANOVA was used to detect differences between corresponding (repeated) measurements during evaluation of the amplitude ratio (see below). Data derived from thenar and hypothenar recording sites are presented separately. Physiological data are expressed as mean ± sd, or as median and range for data that were not normally distributed. Statistical significance was assumed for P < 0.05. Statistical analysis was performed with Statistica 5.0 (StatSoft Inc., Hamburg, Germany).
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Results |
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MAP, heart rate, Pao2, Paco2, Petco2, systemic arterial pH, and rectal temperature were not significantly different (P > 0.05) among the three PTPCs (Table 1) and maintained stable throughout the surgical procedures. BIS values always remained <65 and decreased (P < 0.05) with increasing PTPCs (Table 1). MEP amplitudes (range, 0.04–9.96 mV) and latencies (abductor pollicis brevis muscle: range, 19.6–47.2 ms; abductor digiti minimi muscle: range, 19.6–42.4 ms) varied with stimulation pattern (intensity, frequency, and number of stimuli) and PTPC and between the thenar and hypothenar recording sites.
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With three-way repeated-measures ANOVA (fixed effects) for PTPC, stimulation intensity (voltage), and measurement repetition, significant main effects for MEP amplitude (P < 0.05; Table 2) could be demonstrated for PTPC (2 vs 6 µg/mL; thenar only) and voltage (thenar and hypothenar), but not for measurement replication (Measurement 1 vs 2). Regarding MEP amplitude, contrast analysis revealed no significant two- or three-way interactions among factors. Within each level of the first factor (PTPC), MEP amplitude varied significantly (P < 0.003) between Level 1 (100 V) and Level 2 (150 V) of the second factor (voltage) in both levels of the third factor (i.e., initial observation and 30-s control value). However, significant changes in MEP amplitude between 150 and 200 V (Levels 2 and 3 of the second factor) were observed only for PTPCs of 4 and 6 µg/mL (Fig. 1A). No significant main effects on MEP amplitude resulted from further increases in stimulation intensity (Levels 3–5 of the second factor). PTPC (2 vs 6 µg/mL) and voltage (100 vs 150 V; only for PTPC of 2 µg/mL) had significant main effects on hypothenar MEP latency (Fig. 1B). For thenar latencies, a significant two-way interaction (P < 0.002) between PTPC (first factor) and voltage (second factor) was observed (Table 2). Stimulation intensities of 200 V combined with three or more stimuli delivered at 500 Hz yielded a 97% recording success rate in all patients at all PTPCs.
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With three-way repeated-measures ANOVA (fixed effects) for PTPC, stimulation frequency, and measurement repetition, a significant main effect (P < 0.05) of PTPC (first factor: 2 versus 4 and 6 µg/mL) on MEP amplitude (thenar only) and latency (thenar: 2 versus 4 and 6 µg/mL; hypothenar: 2 versus 6 µg/mL) was observed. Stimulation frequency (second factor, Levels 1–4: 100–1000 Hz) had significant main effects on MEP amplitudes and latencies in both levels of the first factor (PTPC), whereas no significant main effect of measurement replication (third factor) on MEP amplitude and latency was observed (Fig. 2). For MEP latency, a significant two-way interaction (P < 0.05) between PTPC and stimulation frequency was observed (thenar and hypothenar). Incremental increases in stimulation frequency caused progressive increases in MEP amplitudes and in recording success rates at each PTPC (>97% with delivery of four stimuli at 300 V; stimulation frequency, 500 Hz).
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With three-way repeated-measures ANOVA (fixed effects) for PTPC, number of stimuli, and measurement repetition, PTPC (first factor: 2 vs 4 and 6 µg/mL; thenar only) and number of stimuli (second factor), but not measurement replication, displayed significant main effects on MEP amplitude (P < 0.03). At each PTPC, MEP amplitude varied significantly in response to changes in stimulus number (second factor; Levels 1–3). The addition of a fourth and fifth stimulus to the stimulation train did not significantly modify MEP amplitudes, independently of PTPC (Fig. 3A). A significant main effect of stimulus number (one versus two or more stimuli) on MEP latency was observed, whereas neither PTPC nor Factor 3 (measurement replication) showed significant main effects on MEP latency (Fig. 3B). No significant two- or three-way interactions were observed among all factors regarding both MEP amplitude and latency. An increase in the number of stimuli was associated with corresponding increases in MEP amplitudes and signal stability irrespective of PTPC (recording success >97% with delivery of three or more stimuli at 500 Hz and a constant stimulation current of 300 V).
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To identify changes in PTPC as the primary reason for alterations in MEP amplitude, an amplitude ratio was derived from two MEPs recorded consecutively after delivery of two and four stimuli (Ampdoublestim/Ampquadruplestim) at 500 Hz and 300 V. These measurements were performed at each PTPC to evaluate the influence of PTPC on the amplitude ratio. The rationale for developing such an index was the desire to eliminate the well known problems associated with comparing absolute changes in MEP amplitude between successive recordings in the course of prolonged monitoring periods, especially when the target-controlled infusion rate has to be changed during the procedure according to the different levels of surgical stimulation. Whereas considerable variation in absolute MEP amplitudes due to changes in PTPC occurred during each monitoring session (i.e., in each patient), the individual amplitude ratio (Fig. 4) remained constant (Friedman’s ANOVA; P = 0.36) and independent from changes in PTPC.
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Discussion |
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The two main findings of this investigation can be summarized as follows: (a) irrespective of PTPC, the amplitude of myogenic potentials and the recording success rate were highest during quadruple stimulation at 1000 Hz with stimulation intensities exceeding 200 V; and (b) changes in PTPC between 2 vs 4 and 6 µg/mL, but not between 4 and 6 µg/mL, appear to significantly affect MEP amplitude. However, the overall intraoperative recording success rate relied primarily on the choice of suitable stimulation variables. With use of adequate stimulation patterns, changes in PTPC between 2 and 6 µg/mL did not significantly interfere with recording of MEP.
Intraoperative monitoring of the motor tracts has gained increasing acceptance during the past decade because of major advances in electrophysiological and anesthetic techniques (1–3,5–7,11). The safety of the procedure is well established (12). High-frequency repetitive electrical stimulation has emerged as the preferred technique for the recording of myogenic MEPs under various anesthetic techniques (3,7–9,11). Further improvement in intraoperative MEP acquisition requires systematic evaluation of frequency- and anesthetic-dependent modulation of MEPs recorded under standardized clinical conditions.
Our findings of maximum MEP amplitudes after delivery of four stimuli at 1000 Hz indicate increased synchronicity of motor unit discharge compared with recordings obtained at lower stimulation frequencies (100–200 Hz). MEP facilitation during both electrical and magnetoelectrical stimulation of the motor cortex involves both cortical and spinal mechanisms, depending on the mode, intensity, frequency, and direction of the current applied during stimulation (13–19). It has been suggested that electrical or magnetoelectrical stimuli activate corticospinal motoneurons directly at their axon terminals, bypassing the neuronal pacemakers and cortical interneurons (20).
Regarding the propagation of the impulse further downstream within the corticospinal motor system, experimental investigations have shown that the duration of excitatory postsynaptic potentials (EPSP) elicited at the spinal 
-motoneuron by single activation of the corticospinal tract is between 7 and 10 ms (21). Accordingly, temporal summation of EPSP (an important mechanism for MEP facilitation) is to be expected at stimulation frequencies exceeding 150 Hz. The absolute refractory period of axonal conduction of different types of motor units ranges between 0.58 and 0.88 ms (22), theoretically limiting the maximum physiological stimulation frequency to 1000 Hz.
Investigations on human motoneurons illustrate the dependence of motoneuron excitability (defined as the response to composite EPSP inputs) on their background firing rate: excitability is higher at slower firing rates (23). This inverse relationship between the response probability to a transient input (external stimulus) and the background firing rate characteristic of spinal motoneurons (rate effect) is in accordance with the finding that higher stimulation frequencies are more effective with regard to MEP facilitation during deep surgical anesthesia than during light sedation or in awake subjects. In agreement with previous findings (3,24), a train containing three transcranially applied electrical stimuli (each producing a D wave) was sufficient to produce submaximal MEP amplitudes, with only minor additional amplification of MEP amplitude by additional stimuli.
Our findings show that the success rate in obtaining stable and reproducible intraoperative MEPs exceeds 95% when an appropriate stimulation pattern is used and when preexisting significant motor deficits are absent. The differences regarding absolute amplitudes and stimulus-response characteristics observed in the two investigated muscle groups are readily explained by the well known variability in threshold distribution of the constituent motor units within individual muscle groups of the forearm (17,25).
Further improvement in intraoperative signal interpretation may be expected by calculating the MEP amplitude ratio (Ampdoublestim/Ampquadruplestim) after suprathreshold double and quadruple stimulation of the motor cortex. Because this ratio remained essentially unaffected by changes in PTPC in individual patients, it may be used to recalibrate current (absolute) MEP amplitudes to previously established baseline levels whenever such intraoperative changes of PTPC are required. The effect of surgically induced changes in MEP generation and conduction on this MEP amplitude ratio remains to be determined.
Changes in PTPC had little effect on MEP characteristics or the recording success rate. This finding is of considerable clinical interest because it suggests that adjustments in the depth of propofol hypnosis according to surgical requirements do not necessarily lead to clinically relevant problems in the interpretation of intraoperative signal changes. The seeming discrepancies between our results and previous findings of a nonlinear electrophysiological effect of changing PTPCs between 1 and 6 µg/mL on intracortical MEP facilitation/inhibition (2) may be attributed to differences in stimulation technique (magnetoelectrical versus electrical stimulation), anesthetic depth (the administration of propofol alone versus the combination of propofol and remifentanil), or both. We provided adequate surgical analgesia by constant infusion of remifentanil, which has only minimal effects on MEPs (2). Adverse events related to transcranial electrical stimulation (e.g., intraoperative convulsions) did not occur. No patient complained of transient intraoperative awareness, and this was consistent with BIS values of <65 throughout this study.
In conclusion, constant-current transcranial electrical stimulation with multiple stimuli at high frequency and high intensity during total IV anesthesia with target-controlled propofol infusion and constant-rate remifentanil infusion proved to be well suited for intraoperative MEP monitoring. Varying PTPCs had no clinically relevant effect on MEP characteristics or recording success rate. The anesthetic protocol and stimulation patterns presented in this study allow stable recording of myogenic responses under a variety of surgical and anesthetic conditions; are thus well suited for intraoperative MEP monitoring; and have become routine procedure in our institution. The MEP amplitude ratio may provide a new and useful tool for intraoperative MEP baseline amplitude recalibration after necessary intraoperative adjustments in PTPC.
We gratefully acknowledge the considerable contribution to the statistical data analysis of Dr. J. Schulte-Monting, Professor of Biometry and Statistics, University of Freiburg.
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Footnotes |
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Supported by Grant Ze 267/3-2 from the German Research Foundation.
Accepted for publication July 20, 2004.
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