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TECHNOLOGY, COMPUTING, AND SIMULATION

A Comparison of State and Response Entropy Versus Bispectral Index Values During the Perioperative Period

Paul F. White, PhD, MD^*, Jun Tang, MD, Gladys F. Romero, MD^*, Ronald H. Wender, MD, Robert Naruse, MD, Alexander Sloninsky, MD, and Robert Kariger, MD

*Department of Anesthesiology and Pain Management, University of Texas, Southwestern Medical Center at Dallas, Texas; and Department of Anesthesiology, Cedars-Sinai Medical Center, Los Angeles, California

Address correspondence and reprint requests to Paul F. White, Professor and McDermott Chair of Anesthesiology, Department of Anesthesiology and Pain Management, University of Texas Southwestern Medical Center at Dallas, 5323 Harry Hines Blvd., F2.208A, Dallas, TX 75390-9068. Address e-mail to paul.white{at}utsouthwestern.edu.

	Abstract

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Cerebral monitoring indices are associated with a large degree of inter-patient variability and electrical signal interference during surgery. We designed this clinical study to test the hypothesis that use of the spectral entropy (Entropy) module is associated with less frequent intraoperative interference with the displayed indices than the bispectral index (BIS) monitor when used during general anesthesia with propofol and desflurane. Thirty consenting patients scheduled for major laparoscopic surgery procedures were enrolled in this prospective study. The elapsed time to obtain a baseline index value was recorded, as well as the simultaneous state entropy (SE), response entropy (RE), and BIS values at specific time intervals during the induction, maintenance, and emergence periods in patients administered a standardized general anesthetic technique. During the maintenance period, the changes in these indices were evaluated after a bolus dose of propofol (20 mg IV) and a 2% increase or decrease in the inspired concentration of desflurane. As expected, the baseline SE values were less than the RE and BIS values (88 ± 2 versus 96 ± 3 and 96 ± 4, respectively). However, the SE and RE values correlated with the BIS value during the induction (r = 0.77 and 0.78, respectively) and emergence (r = 0.86 and 0.91, respectively) periods. The area under the receiver operating characteristic curve for detection of consciousness also indicated a similar performance of the SE (0.93 ± 0.04) relative to the RE (0.98 ± 0.04) and BIS (0.97 ± 0.04). During the maintenance period, the responses to changes in propofol and desflurane concentrations were consistent with all three indices. Finally, the entropy indices were less interfered with by the electrocautery unit during the operation (12% versus 62% for the BIS monitor). Because the average selling prices of the Entropy and BIS disposable electrode strips ($14.25 versus $14.95 USD, respectively) are comparable, we conclude that the Entropy module is a cost-equivalent alternative to the BIS monitor.

	Introduction

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A wide variety of electroencephalographic (EEG)-based monitoring systems have been introduced to evaluate the depressant effects of anesthetic drugs on the central nervous system (1–6). The most frequently used cerebral monitoring device, the bispectral index (BIS) monitor (Aspect Medical Systems, Newton, MA), has been reported to improve the titration of both volatile and IV anesthetics (7,8). Although different EEG algorithms have been used for cerebral monitoring, all have similar effects on the ability of anesthesiologists to improve titration of anesthetic drugs (as reflected by anesthetic-sparing effects) in paralyzed patients under general anesthesia (4–12). However, all of these EEG-based indices have a disturbingly large degree of inter-patient variability, as well as variability in their responses to different classes of anesthetic drugs (13–17). Another difference among the various cerebral monitoring devices relates to the susceptibility of the EEG signal to interference by electromyographic activity and the electrocautery (15,16).

The most recently introduced cerebral monitor is the M-entropy module (Datex-Ohmeda S/5 Entropy^TM Module, Instrumentarium Corp, Helsinki, Finland). In contrast to the other EEG-based monitoring systems that combine several disparate descriptors of the EEG into a single value, the Entropy module quantifies the regularity of the EEG signal and generates both a state entropy (SE) and a response entropy (RE) value (18). Whereas approximate, and Shannon's entropy values are calculated in the time domain, the SE and RE values are based on both time- and frequency-balanced spectral entropy. Preliminary clinical studies with the Entropy module suggest that the regularity of the EEG increases with increasing concentrations of both IV (e.g., propofol) (19–21) and volatile (e.g., desflurane and sevoflurane) (22,23) anesthetics. Using logistic regression to compare the power of the BIS and entropy in distinguishing awake from hypnotic (asleep) states, the BIS was alleged to display a higher predictive power (24). However, during the maintenance and recovery periods, the BIS was alleged to be less reliable than entropy because of suppression ratio artifacts (25). It has also been suggested that approximate entropy is more sensitive than the BIS in detecting deepening of anesthesia with propofol (26). Therefore, it is possible that there will be differences between the two cerebral monitors with respect to both inter-patient and inter-anesthetic variations.

We hypothesized that the use of the Entropy module would be less susceptible to intraoperative interference with the displayed index values during operation of the electrosurgical unit than the BIS monitor. A secondary objective of this study was to compare the sensitivity and specificity of the entropy and BIS values with respect to predicting loss of consciousness and emergence from a standardized general anesthetic technique.

	Methods

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After obtaining local IRB approval for this exempt monitoring study, 30 consenting ASA physical status I and II patients scheduled for laparoscopic surgery under general anesthesia were evaluated. Patients with known neurologic or psychiatric disorders, chronic use of anticonvulsant or other centrally active medications, those with clinically significant cardiovascular, respiratory, hepatic, renal, or metabolic disease, long-term drug or alcohol abuse, a body weight >50% more than their ideal body weight, or where there was difficulty obtaining an acceptable EEG signal from either cerebral monitor were excluded from participating in this observational study.

All patients received midazolam 2 mg IV for premedication in the preoperative holding area. Both the BIS XP^TM sensor (10 k impedance limit) and Entropy sensor (7.5 k impedance limit) strips were simultaneously applied to the patient's forehead on arrival in the operating room. If the electrode impedance is above 7.5 k for the entropy or 10 k for the BIS, the devices will not provide initial (baseline) index values. The sigma quality index (SQI) values (for the BIS monitor) and the skin impedance values (for the entropy monitor) were inspected at 10-min intervals during the procedure to ensure adequate EEG signal quality. The time required to obtain baseline (awake) BIS, SE, and RE values was recorded. The moving average windows used to calculate the entropy values are 2–15 s and 15–60 s for the RE (32–47 Hz) and SE (<32 Hz) values, respectively, compared with a fixed 15-s interval for the BIS value. Anesthesia was induced with propofol 2.0 mg/kg IV, and fentanyl 1 µg/kg IV was injected for 15–30 s. Cisatracurium 0.3 mg/kg IV was administered to facilitate tracheal intubation, followed by desflurane 4% (initial inspired concentration) in combination with nitrous oxide (N₂O) 60% in oxygen for maintenance of anesthesia. Intermittent bolus doses of cisatracurium (0.05 mg/kg IV) were administered to minimize electromyographic interference with the EEG signal acquisition.

If the patient displayed autonomic signs consistent with inadequate anesthesia (e.g., increased heart rate, diaphoresis, or lacrimation), supplemental doses of propofol 20 mg IV were administered during the maintenance period. The inspired desflurane concentration was increased by 2% if the patient manifested a sustained (5 min) increase in mean arterial blood pressure (MAP) 20% of the preincision baseline value. In response to clinical signs of excessive anesthetic effect (e.g., a decrease in MAP 20% of the preincision value), the inspired concentration of desflurane was decreased by 2%. At the end of surgery, the inhaled anesthetics were discontinued, and residual neuromuscular blockade was reversed with neostigmine 0.05 mg/kg IV and glycopyrrolate 0.01 mg/kg IV.

The MAP, heart rate, BIS, SE, and RE values were recorded at 1-min intervals during the induction and emergence periods, as well as immediately before and up to 5 min after a 20-mg IV bolus of propofol or a 2% change in the inspired concentration of desflurane during the maintenance period. Three investigators were simultaneously involved in the conduct of the study. The staff anesthesiologist (RHW, RN, AS, or RK) was responsible for administering the anesthetic drugs and for monitoring the clinical depth of anesthesia. Both the BIS and Entropy monitor screens were positioned out of the anesthesiologist's line of sight, and the second investigator (GFR) recorded data at specific time intervals throughout the perioperative period. The incidence of electrocautery interference with the BIS, RE, and SE reading was determined by whether a displayed BIS, RE, or SE value was present or absent each time the electrocautery unit was activated during the operation. The third investigator (JT) was responsible for recording the recovery times and analyzing these data.

Data regarding the patient's state of consciousness (e.g., ability to follow verbal commands to open their eyes, squeeze the investigator's hand, and oriented to person, place, and time) were obtained at 15- to 30-s intervals from the start of the injection of the induction dose of propofol until loss of responsiveness to verbal commands and from discontinuation of the inhaled anesthetics until the patient was awake (i.e., eye opening) and oriented to person and place. At a 24 h follow-up interview, patients were asked if they had recall of any events during the operation.

One-way analysis of variance was used to analyze normally distributed continuous variables, and when a significant difference was noted, the Newman-Keuls test was performed for post hoc comparisons among the three indices. Repeated-measures of analysis of variance with a post hoc Bonferroni correction was used to compare the changes in the specific BIS, RE, and SE values (versus baseline values). Categorical data were analyzed by the ² test. The relationship among BIS, RE, and SE values during the induction and emergence periods was analyzed using linear regression to determine the correlation coefficients. Assessment of the nonlinear association among BIS, RE, and SE values and the probability of unconsciousness were accomplished using the logistic regression procedure, which estimated the probability of a binary "yes/no" response.

Using the NCSS 6.0 software program, the area under the receiver operating characteristic (ROC) curve for each index was determined by plotting the sensitivity (fraction of unresponsive patients who were correctly predicted to be unconscious) against 1-specificity (fraction of responsive patients who were correctly predicted to be awake), and reflects the discriminating power of the indices. The area under the ROC curve summarizes the predictive power of the index to achieve a high specificity at any given sensitivity (27). An area >0.5 indicates that the measurement is predictive, and a measurement with 100% accuracy would have an area of 1.0. However, an area under the ROC of 0.5 has the same predictive value as a coin flip. All tests were two-sided, and a P value < 0.05 was considered statistically significant. Data are presented as mean ± sd and percentages.

	Results

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Five men and 25 women with a mean age of 45 ± 13 yr (range, 28–70 yr) and weight of 101 ± 34 kg (range, 56–163 kg) were evaluated in this study. Two women were excluded from the data analysis because of inadequate signal quality (i.e., low SQI values). The mean duration of surgery was 80 ± 36 min (range, 23–150 min). The total dosages of propofol and fentanyl were 219 ± 81 mg and 109 ± 33 µg, respectively. In addition, the average end-tidal concentration of desflurane was 4.4% ± 1.5%. Times to eye opening and orientation were 8 ± 3 and 10 ± 3 min, respectively. No patient reported intraoperative recall at the 24-h follow-up interview.

The BIS, RE, and SE values decreased progressively from preinduction (baseline) values of 96 ± 4, 96 ± 3, and 88 ± 2 to preincision values of 39 ± 11, 40 ± 13, and 38 ± 12, respectively (Table 1). A similar degree of inter-patient variability (±sd) was observed in the BIS, RE, and SE values. During the maintenance period, the SE values tended to be lower than the RE and BIS values (Fig. 1). However, the pattern of the changes in the RE, SE, and BIS values was similar after bolus doses of propofol and changes in the inspired concentration of desflurane (Table 2).

View larger version (19K): [in this window] [in a new window]   Figure 1. Changes in the bispectral index (BIS), response entropy (RE), and state entropy (SE) values during the perioperative period. BIS value:; RE value: ; and SE value: . Values are presented as mean ± sd. *P < 0.05 versus BIS and RE values; P < 0.05 versus BIS; P < 0.05 versus baseline values.

Compared with the BIS monitor, the Entropy module experienced significantly less interference (i.e., artifact) during use of the electrosurgical unit (12% versus 62%, respectively). Although the indices were comparable during the induction period, the SE values were significantly less than the RE and BIS values during the emergence period. Nevertheless, the SE correlated with the RE and BIS values during both the induction (Fig. 2) and emergence (Fig. 3) periods. In addition, the BIS, RE, and SE values all increased significantly after reversal of residual neuromuscular blockade at the end of the operation (Table 3). During the interval from discontinuing the maintenance anesthetics until the patients were alert and oriented, the BIS, RE, and SE values increased from 47 ± 13, 46 ± 15, and 42 ± 13 to 93 ± 4, 95 ± 3, and 85 ± 5, respectively (Table 4).

View larger version (18K): [in this window] [in a new window]   Figure 2. Correlation of (1) the response entropy (RE) and the bispectral index (BIS) (r = 0.78), as well as (2) the state entropy (SE) and the bispectral index (BIS) (r = 0.77), during the induction period.

View larger version (22K): [in this window] [in a new window]   Figure 3. Correlation of (1) the response entropy (RE) and the bispectral index (BIS) (r = 0.91), as well as (2) the state entropy (SE) and the bispectral index (BIS) (r = 0.86), during the emergence period.

Logistic regression analysis demonstrated that the BIS, RE, and SE were all significant predictors of unconsciousness (P < 0.01), with area under the ROC curve values of 0.97 ± 0.04, 0.98 ± 0.04, and 0.93 ± 0.04 for the BIS, RE, and SE, respectively (Fig. 4). Of interest, the BIS, RE, and SE values all correlated poorly with the end-tidal desflurane concentrations at eye opening (Fig. 5) and at tracheal extubation (Fig. 6).

View larger version (20K): [in this window] [in a new window]   Figure 4. Receiver operating characteristics curves for discrete threshold values of the response entropy (RE), the state entropy (SE), and the bispectral index (BIS). The area under Entropy (RE and SE) curve was similar to the area under the BIS curve (0.98 ± 0.04, 0.93 ± 0.04, and 0.97 ± 0.04, respectively). No significant differences among the three indices.

View larger version (12K): [in this window] [in a new window]   Figure 5. Correlation of (1) the bispectral index (BIS) (r = 0.06), the response entropy (RE) (r = 0.16), and the state entropy (SE) (r = 0.07), with the end-tidal concentration of desflurane at the time of eye opening.

View larger version (14K): [in this window] [in a new window]   Figure 6. Correlation of (1) the bispectral index (BIS) (r = 0.04), the response entropy (RE) (r = 0.11), and the state entropy (SE) (r = 0.10), with the end-tidal concentration of desflurane at the time of tracheal extubation.

Finally, the time required to apply the electrode strip (9 ± 3 s) and obtain the baseline index values (42–48 s) were not significantly different with the two monitoring systems (Table 5). In addition, the costs of the monitoring devices and their disposable units were comparable for both cerebral monitors.

	Discussion

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A depth of anesthesia monitor should display a good correlation between the measured index value and the patient's physiologic responses during the perioperative period, independent of the anesthetic being administered (1,2). Available EEG-based cerebral monitors have failed to achieve this goal largely because of their inability to assess pain responses or the central effects of opioid analgesics. Analogous to other cerebral monitoring devices, the Entropy module seems to quantify the central hypnotic effect of IV and volatile anesthetics that affect the gamma-aminobutyric acid neurotransmitter system (28). Our data are also consistent with recent publications comparing these two monitors during general anesthesia (23) and IV sedation (29).

The induction of general anesthesia is usually accompanied by an increase in high-frequency EEG activity that spreads from the frontal region to more posterior regions of the brain, resulting in an increasing degree of sedation and eventually loss of consciousness (25). The BIS is capable of monitoring the level of consciousness during sedation (13,14) and general anesthesia (4,15,16). Importantly, the pattern of changes in the entropy and BIS values was similar during the induction, maintenance, and emergence periods in the current study. However, greater differences may be found between the two monitors when other classes of anesthetic drugs (e.g., etomidate, ketamine, N₂O) are used during surgery (21,28).

A previous study demonstrated that the EEG effects of propofol were similarly quantified by both the BIS and Entropy monitors (26). However, the BIS was slower than Entropy in responding to the onset of burst suppression with increasing levels of propofol-induced hypnosis. The present comparative study demonstrated that both monitoring systems were capable of discriminating between the awake and anesthetized states. These cerebral monitors display greater index values before the induction of anesthesia (awake) and upon recovery of consciousness compared with the index values during the maintenance anesthetic period. The SE values were consistently lower than the BIS values after supplemental boluses of propofol or changes in the inspired desflurane concentration. As expected, the SE values were always less than the RE values because the maximum SE value is 91 (versus 100 for the RE and BIS values). Importantly, all three EEG-based indices returned to their preinduction baseline value upon reorientation of the patient to person and place. Therefore, there seems to be no difference between the two monitors with respect to their sensitivity to the residual (subhypnotic) effects of anesthetic drugs administered during the maintenance period.

Analogous to earlier clinical studies with the BIS, patient state analyzer, and auditory evoked potential monitors (5–12), these data suggest that the Entropy module will also prove to be useful in improving the titration of both IV and inhaled anesthetics. Recent studies involving anesthetized and paralyzed patients demonstrated that the anesthetic- or analgesic-sparing effect associated with cerebral monitoring can also contribute to reduced recovery times and an improved quality of recovery (11,12). However, there have been no published clinical utility studies involving the Entropy module.

The ability of the Entropy module to display SE and RE values during intraoperative use of the electrosurgical unit was superior to the BIS monitor. This observation is consistent with our earlier findings in comparative studies involving the BIS monitor and patient state analyzer (15,16). This difference might suggest that the Entropy module is less sensitive than the BIS monitor in detecting contamination of the EEG signal during use of the electrocautery unit. However, Bruhn et al. (30) reported that the entropy parameters were superior to EEG spectral edge frequency and ratios with respect to robustness against artifacts. The areas under the ROC curves also suggest that the entropy indices have similar sensitivity and specificity to the BIS value with respect to anesthesia-induced changes in the level of consciousness. Moreover, the entropy indices demonstrated a good correlation with the BIS during the induction and emergence from general anesthesia. However, the importance of the correlation coefficients is limited because if the values range is small, the correlation may be low, although the agreement was very good. Finally, given the comparable costs of the two monitoring units and disposable electrode strips, these data would suggest that the Entropy module is a cost-equivalent alternative to the BIS monitor.

This observational study can be criticized because only a small group of patients undergoing one type of surgical procedure were studied using a highly standardized anesthetic technique. In contrast to the extensive clinical experience with the BIS monitor (4,7,8,10–16), there is a more limited clinical database for the Entropy algorithm (17,19–26). Further comparative studies involving the Entropy module are clearly required in patients undergoing more varied surgical procedures.

In conclusion, the changes in SE and RE values followed a similar pattern to the BIS values during the perioperative period. Analogous to the BIS, the entropy indices display a high degree of sensitivity and specificity in assessing consciousness during the induction of and emergence from anesthesia and were able to detect changes associated with administration of IV (propofol) and volatile (desflurane) anesthetics during the maintenance period. Finally, the Entropy module experienced less interference with the displayed indices during use of the electrocautery unit than the BIS monitor.

	Footnotes

 
Accepted for publication July 29, 2005.

Supported, in part, by an educational grant from GE/Datex/Ohmeda to the White Mountain Institute, a non-for-profit private educational and research foundation dedicated to art and medicine. Endowment funds from the Margaret Milam McDermott Distinguished Chair of Anesthesiology were used to support Dr. White's academic activities.

	References

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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