EEG entropy measures in anesthesia

Highlights: ► Twelve entropy indices were systematically compared in monitoring depth of anesthesia and detecting burst suppression. ► Renyi permutation entropy performed best in tracking EEG changes associated with different anesthesia states. ► Approximate Entropy and Sample Entropy performed best in detecting burst suppression. Objective: Entropy algorithms have been widely used in analyzing EEG signals during anesthesia. However, a systematic comparison of these entropy algorithms in assessing anesthesia drugs' effect is lacking. In this study, we compare the capability of 12 entropy indices for monitoring depth of anesthesia (DoA) and detecting the burst suppression pattern (BSP), in anesthesia induced by GABAergic agents. Methods: Twelve indices were investigated, namely Response Entropy (RE) and State entropy (SE), three wavelet entropy (WE) measures [Shannon WE (SWE), Tsallis WE (TWE), and Renyi WE (RWE)], Hilbert-Huang spectral entropy (HHSE), approximate entropy (ApEn), sample entropy (SampEn), Fuzzy entropy, and three permutation entropy (PE) measures [Shannon PE (SPE), Tsallis PE (TPE) and Renyi PE (RPE)]. Two EEG data sets from sevoflurane-induced and isoflurane-induced anesthesia respectively were selected to assess the capability of each entropy index in DoA monitoring and BSP detection. To validate the effectiveness of these entropy algorithms, pharmacokinetic/pharmacodynamic (PK/PD) modeling and prediction probability (Pk) analysis were applied. The multifractal detrended fluctuation analysis (MDFA) as a non-entropy measure was compared. Results: All the entropy and MDFA indices could track the changes in EEG pattern during different anesthesia states. Three PE measures outperformed the other entropy indices, with less baseline variability, higher coefficient of determination (R2) and prediction probability, and RPE performed best; ApEn and SampEn discriminated BSP best. Additionally, these entropy measures showed an advantage in computation efficiency compared with MDFA. Conclusion: Each entropy index has its advantages and disadvantages in estimating DoA. Overall, it is suggested that the RPE index was a superior measure. Investigating the advantages and disadvantages of these entropy indices could help improve current clinical indices for monitoring DoA.

[1]  Sinikka Münte,et al.  Spectral Entropy as a Measure of Hypnosis and Hypnotic Drug Effect of Total Intravenous Anesthesia in Children during Slow Induction and Maintenance , 2012, Anesthesiology.

[2]  T. Inouye,et al.  Quantification of EEG irregularity by use of the entropy of the power spectrum. , 1991, Electroencephalography and clinical neurophysiology.

[3]  Pere Caminal,et al.  Detrended Fluctuation Analysis of EEG as a Measure of Depth of Anesthesia , 2007, IEEE Transactions on Biomedical Engineering.

[4]  Zhenhu Liang,et al.  Multiscale permutation entropy analysis of EEG recordings during sevoflurane anesthesia , 2010, Journal of neural engineering.

[5]  Sekou Singare,et al.  Recurrence Quantification Analysis of EEG Predicts Responses to Incision During Anesthesia , 2006, ICONIP.

[6]  M. Takashina,et al.  Changes of Electroencephalographic Bicoherence during Isoflurane Anesthesia Combined with Epidural Anesthesia , 2002, Anesthesiology.

[7]  Jeffrey C. Sigl,et al.  Anesthetic Management and One-Year Mortality After Noncardiac Surgery , 2005, Anesthesia and analgesia.

[8]  Erik Olofsen,et al.  Entropies of the EEG: The effects of general anaesthesia , 2001 .

[9]  P. Gifani,et al.  Optimal fractal-scaling analysis of human EEG dynamic for depth of anesthesia quantification , 2007, J. Frankl. Inst..

[10]  G. Plourde THE DEPTH OF ANAESTHESIA , 1986, The Lancet.

[11]  J. Sleigh,et al.  Analysis of depth of anesthesia with Hilbert–Huang spectral entropy , 2008, Clinical Neurophysiology.

[12]  L. Voss,et al.  Using Permutation Entropy to Measure the Electroencephalographic Effects of Sevoflurane , 2008, Anesthesiology.

[13]  A. M. Kowalski,et al.  Fractional Brownian motion, fractional Gaussian noise, and Tsallis permutation entropy , 2008 .

[14]  H. Stanley,et al.  Multifractal Detrended Fluctuation Analysis of Nonstationary Time Series , 2002, physics/0202070.

[15]  J. Bruhn,et al.  Depth of anaesthesia monitoring: what's available, what's validated and what's next? , 2006, British journal of anaesthesia.

[16]  Warren D. Smith,et al.  Measuring the Performance of Anesthetic Depth Indicators , 1996, Anesthesiology.

[17]  S M Pincus,et al.  Approximate entropy as a measure of system complexity. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[18]  D. Abásolo,et al.  Entropy analysis of the EEG background activity in Alzheimer's disease patients , 2006, Physiological measurement.

[19]  Wlodzislaw Duch,et al.  Comparison of Shannon, Renyi and Tsallis Entropy Used in Decision Trees , 2006, ICAISC.

[20]  B. Pompe,et al.  Permutation entropy: a natural complexity measure for time series. , 2002, Physical review letters.

[21]  N. Huang,et al.  The empirical mode decomposition and the Hilbert spectrum for nonlinear and non-stationary time series analysis , 1998, Proceedings of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[22]  Charles L. Webber,et al.  Recurrence Quantification Analysis , 2015 .

[23]  Weiting Chen,et al.  Measuring complexity using FuzzyEn, ApEn, and SampEn. , 2009, Medical engineering & physics.

[24]  Jose Alvarez-Ramirez,et al.  Performance of a high-dimensional R/S method for Hurst exponent estimation , 2008 .

[25]  Wangxin Yu,et al.  Characterization of Surface EMG Signal Based on Fuzzy Entropy , 2007, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[26]  O. G. Okogbaa,et al.  On the investigation of the neurophysiological correlates of knowledge worker mental fatigue using the EEG signal. , 1994, Applied ergonomics.

[27]  Gianluigi Reni,et al.  Infant's emotional variability associated to interactive stressful situation: a novel analysis approach with Sample Entropy and Lempel-Ziv Complexity. , 2010, Infant behavior & development.

[28]  Yan Li,et al.  An Improved Detrended Moving-Average Method for Monitoring the Depth of Anesthesia , 2010, IEEE Transactions on Biomedical Engineering.

[29]  Tarmo Lipping,et al.  Comparison of entropy and complexity measures for the assessment of depth of sedation , 2006, IEEE Transactions on Biomedical Engineering.

[30]  J. Röschke,et al.  Discrimination of sleep stages: a comparison between spectral and nonlinear EEG measures. , 1996, Electroencephalography and clinical neurophysiology.

[31]  Hong Bao,et al.  GPGPU-Aided Ensemble Empirical-Mode Decomposition for EEG Analysis During Anesthesia , 2010, IEEE Transactions on Information Technology in Biomedicine.

[32]  F.C. Morabito,et al.  Brain Activity Investigation by EEG Processing: Wavelet Analysis, Kurtosis and Renyi's Entropy for Artifact Detection , 2007, 2007 International Conference on Information Acquisition.

[33]  I. Rezek,et al.  Stochastic complexity measures for physiological signal analysis , 1998, IEEE Transactions on Biomedical Engineering.

[34]  Alan Forster,et al.  Measuring performance , 2010, Canadian Medical Association Journal.

[35]  J. E. Skinner,et al.  Chaos and physiology: deterministic chaos in excitable cell assemblies. , 1994, Physiological reviews.

[36]  J. Bruhn,et al.  Approximate Entropy as an Electroencephalographic Measure of Anesthetic Drug Effect during Desflurane Anesthesia , 2000, Anesthesiology.

[37]  J. Bruhn,et al.  Shannon Entropy Applied to the Measurement of the Electroencephalographic Effects of Desflurane , 2001, Anesthesiology.

[38]  A. Yli-Hankala,et al.  Description of the Entropy™ algorithm as applied in the Datex‐Ohmeda S/5™ Entropy Module , 2004, Acta anaesthesiologica Scandinavica.

[39]  Robert LIN,et al.  NOTE ON FUZZY SETS , 2014 .

[40]  The Entropy Module® and Bispectral Index® as Guidance for Propofol-Remifentanil Anaesthesia in Combination with Regional Anaesthesia Compared with a Standard Clinical Practice Group , 2010, Anaesthesia and intensive care.

[41]  W. Klonowski,et al.  MONITORING THE DEPTH OF ANAESTHESIA USING FRACTAL COMPLEXITY METHOD , 2006 .

[42]  N. Thakor,et al.  Parameterized entropy analysis of EEG following hypoxic–ischemic brain injury , 2003 .

[43]  J. Sleigh,et al.  Pharmacokinetic-Pharmacodynamic Modeling the Hypnotic Effect of Sevoflurane Using the Spectral Entropy of the Electroencephalogram , 2006, Anesthesia and analgesia.

[44]  C. Bandt Ordinal time series analysis , 2005 .

[45]  R WilsonJames,et al.  Multifractal detrended fluctuation analysis , 2016 .

[46]  E. Basar,et al.  Wavelet entropy: a new tool for analysis of short duration brain electrical signals , 2001, Journal of Neuroscience Methods.

[47]  I. Rampil A Primer for EEG Signal Processing in Anesthesia , 1998, Anesthesiology.

[48]  Tapio Seppänen,et al.  Automatic Analysis and Monitoring of Burst Suppression in Anesthesia , 2002, Journal of Clinical Monitoring and Computing.

[49]  W. Pritchard,et al.  Dimensional analysis of resting human EEG. II: Surrogate-data testing indicates nonlinearity but not low-dimensional chaos. , 1995, Psychophysiology.

[50]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[51]  Abubakr Gafar Abdalla,et al.  Probability Theory , 2017, Encyclopedia of GIS.

[52]  Erik W. Jensen,et al.  EEG complexity as a measure of depth of anesthesia for patients , 2001, IEEE Trans. Biomed. Eng..

[53]  Gaoxiang Ouyang,et al.  Multiscale rescaled range analysis of EEG recordings in sevoflurane anesthesia , 2012, Clinical Neurophysiology.

[54]  L. Jameson,et al.  Using EEG to monitor anesthesia drug effects during surgery , 2006, Journal of Clinical Monitoring and Computing.

[55]  Rudolf Clausius,et al.  The Mechanical Theory of Heat: With Its Applications to the Steam-Engine and to the Physical Properties of Bodies , 2015 .

[56]  G. Ouyang,et al.  Predictability analysis of absence seizures with permutation entropy , 2007, Epilepsy Research.

[57]  Hyeri Yoon,et al.  Automatic detection of seizure termination during electroconvulsive therapy using sample entropy of the electroencephalogram , 2012, Psychiatry Research.

[58]  Zhenhu Liang,et al.  Parameter selection in permutation entropy for an electroencephalographic measure of isoflurane anesthetic drug effect , 2013, Journal of Clinical Monitoring and Computing.

[59]  C. Tsallis,et al.  The role of constraints within generalized nonextensive statistics , 1998 .

[60]  A. Yli-Hankala,et al.  Quantification of Epileptiform Electroencephalographic Activity during Sevoflurane Mask Induction , 2007, Anesthesiology.

[61]  J. Sleigh,et al.  What are electroencephalogram entropies really measuring , 2005 .

[62]  Brain activity. , 2014, Nature nanotechnology.

[63]  L M Hively,et al.  Detecting dynamical changes in time series using the permutation entropy. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[64]  J. Sleigh,et al.  Permutation entropy of the electroencephalogram: a measure of anaesthetic drug effect. , 2008, British journal of anaesthesia.

[65]  O. A. Rosso,et al.  EEG analysis using wavelet-based information tools , 2006, Journal of Neuroscience Methods.

[66]  Alireza Zali,et al.  Clinical analysis of EEG parameters in prediction of the depth of anesthesia in different stages: a comparative study. , 2009 .

[67]  Yan Li,et al.  Improving the accuracy of depth of anaesthesia using modified detrended fluctuation analysis method , 2010, Biomed. Signal Process. Control..

[68]  R. Acharya U,et al.  Nonlinear analysis of EEG signals at different mental states , 2004, Biomedical engineering online.

[69]  A. Yli-Hankala,et al.  Description of the EntropyTM algorithm as applied in the Datex-Ohmeda S / 5 TM Entropy Module , 2004 .

[70]  J. Richman,et al.  Physiological time-series analysis using approximate entropy and sample entropy. , 2000, American journal of physiology. Heart and circulatory physiology.

[71]  Osvaldo A. Rosso,et al.  Brain electrical activity analysis using wavelet-based informational tools (II): Tsallis non-extensivity and complexity measures , 2003 .

[72]  N. Thakor,et al.  Time-Dependent Entropy Estimation of EEG Rhythm Changes Following Brain Ischemia , 2003, Annals of Biomedical Engineering.