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TECHNOLOGY, COMPUTING, AND SIMULATION

The Effect of Different Stages of Neuromuscular Block on the Bispectral Index and the Bispectral Index-XP Under Remifentanil/Propofol Anesthesia

Ashraf A. Dahaba, MD MSc, PhD^*, Markus Mattweber, MD^*, Andreas Fuchs, MD^*, Wilhelm Zenz, MD^*, Peter H. Rehak, PhD, Werner F. List, MD^*, and Helfried Metzler, MD^*

*Department of Anaesthesiology and Intensive Care Medicine and Department of Surgery, Biomedical Engineering and Computing Unit, Faculty of Medicine, Karl-Franzens University, Graz, Austria

Address correspondence and reprint requests to Ashraf A. Dahaba, MD, MSc, PhD, Department of Anaesthesiology and Intensive Care Medicine, Faculty of Medicine, Karl-Franzens University, Auenbruggerplatz 29, A-8036, Graz, Austria. Address e-mail to ashraf.dahaba{at}meduni-graz.at

	Abstract

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Facial electromyographic activity and neuromuscular block could influence bispectral index (BIS) depth of anesthesia monitoring. In this study we examined, in 30 patients undergoing general surgical procedures, the effect of different stages of neuromuscular block on BIS monitoring and compared the conventional A-2000 BIS^TM (BIS_3.4) with the new BIS-XP^TM (BIS_XP). At deep surgical anesthesia BIS_3.4 of approximately 40, under a propofol 3.61 µg/mL target-controlled infusion and a 0.15–0.3 µg · kg^–1 · min^–1 remifentanil infusion, mivacurium 0.15 mg/kg was administered. The onset of neuromuscular block triggered a brief transient odd divergence in response that manifested as a BIS_3.4 increase from 43 ± 4 to 49 ± 7 (P = 0.007) and a BIS_XP decline from 41 ± 3 to 35 ± 3 (P = 0.003) at 1 ± 0.2 min. Then, 2.5 ± 1 min after mivacurium administration, both monitors returned to baseline values of 43 ± 5 and 40 ± 4, respectively. After that, BIS_3.4 and BIS_XP did not significantly change during complete neuromuscular block or during various levels of neuromuscular recovery. At all phases, BIS_XP was significantly lower than BIS_3.4. Our study indicated that the BIS_3.4/BIS_XP bias and the wide limits of agreement do not allow values given by the two monitors to be used interchangeably.

IMPLICATIONS: The bispectral index (BIS) and its new version, the BIS-XP, monitor the depth of anesthesia. Under propofol/remifentanil anesthesia, the BIS readings did not significantly change during complete neuromuscular block or during various levels of neuromuscular recovery.

	Introduction

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The bispectral index (BIS) algorithm is derived from three electroencephalography (EEG) subvariables in which facial electromyography (EMG) is not a component (1). However, BIS electrodes’ frontal montage renders EMG activity (or lack of it) influencing BIS monitoring a real possibility.

The results of two recent peer-reviewed studies seem to be confusing. The first study (2) showed that, in paid volunteers, neuromuscular blocking drugs (NMBDs) had no effect on BIS monitoring. Conversely, the second study (3) showed that in intensive care unit (ICU) sedated patients, NMBDs caused a marked decline in BIS. Adding to the confusion, authors of a recent study (4) volunteered to self-administer NMBD while fully awake and reported a BIS decline to a value of as low as 9. The BIS algorithm was derived from more than 5000 subjects to correlate with the depth of general anesthesia in the operating room (1) and was not intended for sedated ICU patients or for awake volunteers. No controlled study has appeared in literature specifically examining the effect of neuromuscular block on BIS monitoring in a real operating room setting under deep surgical levels of anesthesia.

The purpose of our study was to assess, in patients undergoing general surgical procedures under propofol/remifentanil anesthesia, the effect of mivacurium chloride 0.15 mg/kg (twice the 95% effective dose) neuromuscular block on BIS monitoring and to compare the conventional A-2000 BIS^TM (BIS_3.4) with the new BIS-XP^TM (BIS_XP) monitors (Aspect Medical Systems, Newton, MA).

	Methods

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A prospective, controlled, clinical consecutive study was conducted in conformity with the guidelines of the Consolidated Standards of Reporting Trials statement (5) and "Good Clinical Research Practice (GCRP) in Pharmacodynamic Studies of Neuromuscular Blocking Agents" (6). After ethics committee approval, all patients who agreed to participate in the study gave their written, informed consent. We excluded potential participants who had neuromuscular disease or neurological disorders, because the awake BIS is reported to be lower with neurological disorders (7). Furthermore, all potential participants were screened to have a normal awake BIS value to exclude genetically determined low-voltage EEGs that could result in an awake BIS values of as low as 40 (8). Thirty consecutive ASA status I–II patients between the ages of 18 and 59 yr who were undergoing elective general surgical procedures expected to last for 1–2 h were recruited into the study.

Neuromuscular function at the adductor pollicis muscle was evaluated with the Relaxometer^TM (Groningen University, Groningen, Holland) mechanomyograph (MMG) (9). The force transducer was attached to the thumb, with the preload maintained between 200 and 400 g. After the induction of anesthesia, the ulnar nerve was stimulated supramaximally at the wrist (pulse width, 200 µs; square wave) with train-of-four (TOF) stimuli (2 Hz for 2 s) at 12-s intervals. The MMG was connected to a laptop computer via the serial port. Data were continuously collected and recorded with the AZG-Relaxometer 5.0 program until all patients fully recovered from neuromuscular block. T₁ (first twitch of the TOF) expressed as a percentage of the control response and the TOF ratio (T₄:T₁) were used for the evaluation of neuromuscular block. The possible contamination of BIS signal by the continuous 12-s TOF stimulation was excluded because a regular 12-s artifact signal did not appear in the BIS tracings.

No electric or forced-air warming devices that could have caused false BIS readings (10) were used in our study. Both monitors were alternatively placed on the left and right sides in consecutive patients to level out any effect of dominance of one cerebral hemisphere. A conventional BIS_3.4 three-electrode (1, 2, and 3) sensor and the new BIS_XP four-electrode (1, 2, 4, and 3) sensor were simultaneously placed, one on each side. The BIS_3.4 sensor strip was transversely placed on the forehead with electrode 1 in the midline and then connected to a conventional BIS_3.4 monitor (software Version 3.4). The displayed BIS_3.4 value was the combined impedance of electrodes 1 and 3. The BIS_XP sensor has a completely different montage, because its sensor strip is not placed transversely but has to be inclined on the forehead for the new electrode 4 to be placed slanting just above the eyebrow. This sloping montage allowed the BIS_3.4 and BIS_XP midline electrodes to be simultaneously placed with the BIS_XP midline electrode slightly higher on the forehead than the BIS_3.4 midline electrode, as demonstrated in Figure 1. The BIS_XP sensor was connected to a BIS_XP monitor (software Version 4.0). The displayed BIS_XP value was the combination of the lowest values of Channel 1 derived from electrodes 1 and 3 and Channel 2 (BIS_{XP CH2}) derived from electrodes 1 and 4.

View larger version (147K): [in this window] [in a new window]   Figure 1. Simultaneous bispectral index (BIS)3.4 and BISXP electrode placement. The BIS3.4 sensor strip is transversely placed on the forehead. The BISXP sensor strip has a different montage, because it is inclined on the forehead with electrode 4 slanting just above the eyebrow and the BISXP midline electrode placed slightly higher on the forehead than the BIS3.4 midline electrode.

Oral midazolam 7.5 mg was administered 1 h before surgery. For induction, a remifentanil 0.15–0.3 µg · kg^–1 · min^–1 infusion and a propofol target-controlled infusion (TCI) with a Diprifusor^TM infusion pump (AstraZeneca, Cheshire, UK) were started. After the patients’ anthropometric data were entered, propofol TCI was set to reach an effect-site concentration of 4 µg/mL over 4 min, during which patients were allowed to breathe spontaneously via a face mask. When the eyelash reflex was obtunded, a laryngeal mask airway (LMA) was inserted. After verification of the proper positioning of the LMA and complete respiratory drive suppression, patients’ lungs were mechanically ventilated with 40% oxygen in air.

A stable BIS of approximately 40 was recommended as deep surgical anesthesia level with the same anesthesia regimen we used in our study (11). Anesthesia of a stable BIS_3.4 of approximately 40 was subsequently maintained via propofol TCI with ±0.2 µg/mg rate adjustments. The Diprifusor’s three-compartment pharmacokinetic algorithm (software Version 2) calculates the required plasma concentration and adjusts the propofol infusion rate accordingly; this proved to accurately correlate with BIS (12). The last propofol TCI rate was recorded and maintained with no further adjustments from the start of a 0.15 mg/kg (twice the 95% effective dose) mivacurium administration until full neuromuscular recovery (100% T₁ recovery). Mivacurium’s complete but short neuromuscular block rendered less likely the possibility of changes in surgical conditions during myorelaxation that would confound BIS monitoring. Hypotension was managed by hydroxyethyl starch 130/0.4 infusion and by increasing the crystalloid fluid infusion. Patients requiring exogenous catecholamines administration, such as ephedrine (10–25 mg) or phenylephrine (50–100 µg), were excluded from the study because exogenous catecholamines were shown to evoke a change in BIS readings (13,14). At the end of surgery, propofol and remifentanil infusions were discontinued, and the patients were allowed to breathe spontaneously. When patients could open their eyes in response to verbal command, the LMA was removed, and patients were discharged.

On the basis of the first 10 pilot patients, our a priori power calculation ( = 0.05), with the primary variable to be the difference between the mean BIS_3.4 value before mivacurium administration and the highest BIS_3.4 value reached during the mivacurium onset phase, showed that 30 patients would be required to reveal a statistically significant difference with >95% power. Repeated-measures analysis of variance was used to analyze the effect of mivacurium onset on BIS_3.4 and BIS_XP. Paired Student’s t-tests were used to analyze the differences between monitors and to compare the two monitors’ biases at different phases. Data were expressed as mean ± SD; P < 0.05 was considered statistically significant.

Data collected from the two monitors were additionally analyzed on the basis of the statistical method of Bland and Altman (15), which does not consider the BIS_3.4 or BIS_XP to be the true standard method for depth of anesthesia monitoring but rather assumes that both monitors are subject to experimental error. Bias defines the mean of the difference between the two monitors. Limits of agreement define the bias ± 1.96 SD, in which 95% of the differences between monitors are expected to lie.

	Results

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The SQI of BIS_3.4 (>93) and BIS_XP (>96) indicated reliable monitoring. The SQI did not decline after mivacurium administration. The mean BIS_3.4 and BIS_XP sensors’ impedances were 2.5 ± 0.4 k and 1.4 ± 0.3 k, respectively, indicating optimal electrode placement throughout our study. Patients’ mean age was 49.7 ± 8.2 yr, and the mean weight was 75 ± 12 kg. The predicted propofol effect-site concentration was 3.61 ± 0.6 µg/mL. The mean duration from anesthesia induction until establishment of a stable BIS_3.4 of approximately 40 was 6.8 ± 2.4 min. At all phases, BIS_XP was constantly lower than BIS_3.4 (P = 0.001). BIS_{XP CH2} was constantly closer to BIS_3.4 than to BIS_XP, and this is why BIS_{XP CH2} was not shown in our figures, because it almost overlapped the BIS_3.4 tracings.

The response to mivacurium administration was a transient BIS_3.4 increase from 43 ± 4 to 49 ± 7 (P = 0.007) and a BIS_XP decline from 41 ± 3 to 35 ± 3 (P = 0.003) at 1 ± 0.2 min (Fig. 2). After 2.5 ± 1 min after mivacurium administration, BIS_3.4 and BIS_XP returned to baseline values of 43 ± 5 and 40 ± 4, respectively.

View larger version (29K): [in this window] [in a new window]   Figure 2. All patients (n = 30): mivacurium onset phase, complete neuromuscular block phase, and neuromuscular recovery phase of bispectral index (BIS)3.4 and BISXP. T1% = first twitch of the train-of-four (TOF); EMG = electromyography; SEF = spectral edge frequency.

View larger version (26K): [in this window] [in a new window]   Figure 3. All patients (n = 30): anesthesia recovery phase after termination of anesthesia until full recovery. BIS = bispectral index; EMG = electromyography; SEF = spectral edge frequency.

View larger version (32K): [in this window] [in a new window]   Figure 4. All patients at all phases: Bland-Altman scatterplot of the difference between the bispectral index (BIS)3.4 and the BISXP against the mean of the two measurements (n = 30). The middle line is the bias, and the upper and middle dotted lines are the limits of agreement.

	Discussion

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In an attempt to explain the peculiar divergence in response between BIS_3.4 and BIS_XP, we can only speculate that the phenomenon of two monitors manifesting the same artifact in two opposite mirror images arises from the different nature of two artifact-recognition algorithms. The BIS_{XP CH2} acquires information from the new fourth above-eyebrow electrode, thus viewing the same signal from a completely new plane. According to the manufacturer, the BIS_XP artifact-recognition algorithm recognizes an artifact from its asymmetry with what they called its BIS_{XP CH2} mirror image. In our study patients, it seemed that while the conventional BIS_3.4 monitor was presenting an artifact in its raw form (an increase), the BIS_XP displayed its BIS_{XP CH2} mirror image (a decline).

High EMG activity in response to surgical stimulation could be misinterpreted by the BIS algorithm as EEG activity and assigned spuriously increased BIS values, making deeply anesthetized patients appear more awake than they really are (19). In our study patients, surgical deep anesthesia levels of BIS 40 and adequate remifentanil analgesia (20) prevented any EMG activity from contaminating or compromising the BIS_3.4 and BIS_XP values. This is why BIS_3.4 and BIS_XP readings did not significantly change during complete neuromuscular block or during various levels of neuromuscular recovery.

Greif et al. (2) showed that under TCI propofol infusion, neither BIS nor EMG was altered by randomly allocated mivacurium neuromuscular block levels. This is in accordance with our study and demonstrates that in the absence of noxious stimuli in paid volunteers (and, hence, no EMG activity artifactually increasing BIS), mivacurium had no effect on BIS monitoring.

Vivien et al. (3) examined 45 ICU patients sedated with midazolam and sufentanil to a Sedation Agitation Scale score of 1. BIS (67 ± 19) and EMG (37 ± 9 dB) significantly declined with atracurium administration in the lightly sedated patients, whereas there was no change in BIS among the 13 deeply sedated patients with minimal EMG activity. This clearly indicates that in most patients in the Vivien et al. (3) study, the doses used were totally inadequate to achieve the deep sedation and analgesia that would have abolished EMG activity. When the same anesthetic regimen of midazolam and sufentanil for cardiac surgery was used (21), the dose of sufentanil required to achieve BIS 50 and BIS 40 was reported to be 5.5 and 8.5 times larger, respectively, than the dose used in the Vivien et al. (3) study.

Another factor that could have confounded the Vivien et al. (3) study is the fact that BIS simply does not correlate with any of the ICU sedation scores and that interindividual BIS values vary widely, even among patients at the deepest level of ICU sedation scores (22–25). This was not the case in our study patients, who were all maintained at a stable BIS value of 40 at the time of NMBD administration. BIS was not derived from data collected from ICU patients but rather was developed from a large database of anesthetized subjects to correlate with the depth of anesthesia in the operating room. This does not necessary apply to critically ill patients sedated in an ICU setting (25).

The wide BIS_3.4/BIS_XP bias indicates a basic inherent difference between the BIS_3.4 and BIS_XP algorithms. The fact that arousal (Table 2) at the anesthesia recovery phase further widened the bias (P = 0.009) emphasizes that with more EEG activity the two algorithms act differently, driving the two systems even further apart. In another situation, the high bias and wide limits of agreement of the mivacurium onset-phase artifacts were significantly narrowed (P = 0.011) by complete neuromuscular block and neuromuscular recovery after the abolishment of the artifacts, leaving just the basic difference between the two monitors.

The manufacturer’s correlation coefficient of BIS_XP 4.0 versus BIS_3.4 was 0.963. This merely shows that the two systems were highly correlated in the manufacturer’s 2563 test volunteers but does not inform us of the inherent differences between the two monitors or of how the two systems somehow act differently in different situations.

BIS_{XP CH2} represents data acquired from the new fourth above-eyebrow electrode that views the same signal from a new plane. Interestingly enough, at all phases in our study, the raw BIS_{XP CH2} of the BIS_XP monitor was constantly closer and almost identical to that of the conventional BIS_3.4 monitor rather than its own BIS_XP. This shows that the data acquired with the two systems, although originating from different electrodes, were still virtually identical. The bias appears only after the two algorithms process these acquired data in a different fashion.

Our study indicated that during deep surgical propofol/remifentanil anesthesia, the onset of neuromuscular block triggered a brief transient odd divergence response that manifested as a BIS_3.4 increase and BIS_XP decline that lasted until relaxation was complete. After that, BIS_3.4 and BIS_XP did not significantly change during complete neuromuscular block or during various levels of neuromuscular recovery. The BIS_3.4/BIS_XP bias and wide limits of agreement do not allow values given by the two monitors to be used interchangeably for individual patients.

	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (11) Citing Articles via Google Scholar Google Scholar Articles by Dahaba, A. A. Articles by Metzler, H. Search for Related Content PubMed PubMed Citation Articles by Dahaba, A. A. Articles by Metzler, H. Related Collections Monitoring (Non-cardiac) Pharmacology

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