Preview

General Reanimatology

Advanced search

Instantaneous EEG Signal Analysis Based on Empirical Mode Decomposition Applied to Burst-Suppression in Propofol Anaesthesia

https://doi.org/10.15360/1813-9779-2021-5-65-79

Abstract

The human electroencephalogram (EEG) constitutes a nonstationary, nonlinear electrophysiological signal resulting from synchronous firing of neurons in thalamocortical structures of the brain. Due to the complexity of the brain's physiological structures and its rhythmic oscillations, analysis of EEG often utilises spectral analysis methods.
Aim: to improve clinical monitoring of neurophysiological signals and to further explain basic principles of functional mechanisms in the brain during anaesthesia.
Material and methods. In this paper we used Empirical Mode decomposition (EMD), a novel spectral analysis method especially suited for nonstationary and nonlinear signals. EMD and the related Hilbert-Huang Transform (HHT) decompose signal into constituent Intrinsic Mode Functions (IMFs). In this study we applied EMD to analyse burst-suppression (BS) in the human EEG during induction of general anaesthesia (GA) with propofol. BS is a state characterised by cyclic changes between significant depression of brain activity and hyper-active bursts with variable duration, amplitude, and waveform shape. BS arises after induction into deep general anaesthesia after an intravenous bolus of general anaesthetics. Here we studied the behaviour of BS using the burst-suppression ratio (BSR).
Results. Comparing correlations between EEG and IMF BSRs, we determined BSR was driven mainly by alpha activity. BSRs for different spectral components (IMFs 1-4) showed differing rates of return to baseline after the end of BS in EEG, indicating BS might differentially impair neural generators of low-frequency EEG oscillations and thalamocortical functional connectivity.
Conclusion. Studying BS using EMD represents a novel form of analysis with the potential to elucidate neurophysiological mechanisms of this state and its impact on post-operative patient prognosis.

About the Authors

G. Sobolova
Clinic of Anaesthesiology and Intensive Medicine, Jessenius Faculty of Medicine in Martin, Comenius University Bratislava
Slovakia


M. S. Fabus
Wellcome Centre for Integrative Neuroimaging, Nuffield Department of Clinical Neurosciences, University of Oxford
United Kingdom

Marco S. Fabus.
Level 6, West Wing, John Radcliffe Hospital, Oxford OX3 9DU.



M. Fischer
Clinic of Anaesthesiology and Intensive Medicine, Jessenius Faculty of Medicine in Martin, Comenius University Bratislava
Slovakia

Martin Fischer.
2 Kollarova Str., 036 01 Martin.



M. Drobny
Clinic of Anaesthesiology and Intensive Medicine, Jessenius Faculty of Medicine in Martin, Comenius University Bratislava
Slovakia

Michal Drobny.
2 Kollarova Str., 036 01 Martin.



B. Drobna-Saniova
Clinic of Anaesthesiology and Intensive Medicine, Jessenius Faculty of Medicine in Martin, Comenius University Bratislava
Slovakia

Beata Drobna-Saniova.
2 Kollarova Str., 036 01 Martin.



References

1. Sanders R.D., Tononi G, Laureys S., Sleigh J.W. Unresponsiveness # Unconsciousness. Anesthesiology. 2012; 116 (4): 946-959. DOI: 10.1097/ALN.0b013e318249d0a7.

2. Ni Mhuircheartaigh R., Warnaby C., Rogers R., Jbabdi S., Tracey I. Slow-Wave Activity Saturation and Thalamocortical Isolation During Propofol Anesthesia in Humans. Sci Transl Med. 2013; 23; 5 (208): 208ra148. DOI: 10.1126/scitranslmed.3006007.

3. Warnaby C.E., Sleigh J.W., Hight D., Jbabdi S., Tracey I. Investigation of Slow-wave Activity Saturation during Surgical Anesthesia Reveals a Signature of Neural Inertia in Humans. Anesthesiology. 2017; 127 (4): 645-657. DOI: 10.1097/ALN.0000000000001759.

4. Marchant N., Sanders R., Sleigh J., Vanhaudenhuyse A., Bruno A.U., Brichant J.F., Steven Laureys S., Bonhomme V. How Electroencephalography Serves the Anesthesiologist. Clin EEG Neurosci. 2014; 45 (1): 22-32. DOI: 10.1177/1550059413509801.

5. Purdon P.L., Sampson A., Pavone K.J., Brown E.N. Clinical Electroencephalography for Anesthesiologists: Part I: Background and Basic Signatures. Anesthesiology. 2015; 123 (4): 937-960. DOI: 10.1097/ALN.0000000000000841.

6. Marcuse L.V., Fields M.C., Jenna J. Y. The EEG in other neurological and medical conditions and in status epilepticus. In: Rowan's Primer of EEG. 2nd ed. London: Elsevier, 2016: 157-173.

7. Gropper M. A. Miller's Anesthesia, 2-Volume Set E-Book [electronic resource], 9th ed. 2019.

8. Amzica F. What does burst suppression really mean? Epilepsy Behav. 2015; 49: 234-237. DOI: 10.1016/j.yebeh.2015.06.012.

9. Hogan J., Sun H., Aboul Nour H., Jing J., Tabaeizadeh M., Shoukat M., Javed F., Kassa S., Edhi., Bordbar E., Gallagher J., Moura V. J., Ghanta M., Shao Y-P., Akeju O., Cole A.J., Rosenthal E.S., Zafar S., Westover M.B. Burst Suppression: Causes and Effects on Mortality in Critical Illnes. Neurocrit Care 2020; 33: 565-574. DOI: 10.1007/s12028-020-00932-4

10. Pontificia Universidad Catolica de Chile,. Study of the Association Between Burst Suppression During Anesthetic Induction With Propofol in Cardiac Surgery in Patients Over 65 Years of Age With Postoperative Delirium. Clinical trials. gov. Clinical trial registration NCT04713644, Mar. 2021. Accessed: Apr. 14, 2021. [Online]. Available: https: //clinicaltrials.gov/ct2/show/NCT04713644.

11. Soehle M., Dittmann A., Ellerkmann R.K., Baumgarten G., Putensen C., Guenther U. Intraoperative burst suppression is associated with postoperative delirium following cardiac surgery: a prospective, observational study. BMC Anesthesiol. 2015; 15 (61): 1-8. DOI: 10.1186/s12871-015-0051-7.

12. Huang N.E., Shen Z., Long S., Wu M.C., Shih H.H., Zheng Q., Yen N. C., Tung C.C., Liu H.H. The empirical mode decomposition and the Hilbert spectrum for nonlinear and non-stationary time series analysis', Proc. R. Soc. Lond. Ser. Math. Phys. Eng. Sci. 1998; 454 (1971): 903995. DOI: 10.1098/rspa.1998.0193.

13. Huang N.E., Wu Z. A review on Hilbert-Huang transform: Method and its applications to geophysical studies. Rev. Geophys. 2008; 46 (2): 1-23. DOI: 10.1029/2007RG000228.

14. Kortelainen J., Vayrynen E. Assessing EEG slow wave activity during anesthesia using Hilbert-Huang Transform. Annu Int Conf IEEE Eng Med Biol Soc. 2015; 2015: 117-120. DOI: 10.1109/EMBC.2015.7318314.

15. 15 Barbosh M., Singh P., Sadhu A. Empirical mode decomposition and its variants: a review with applications in structural health monitoring. Smart Mater. Struct. 2020; 29 (9): 093001. DOI: 10.1088/1361-665X/aba539.

16. Bueno-Lopez M., Giraldo E., Molinas M., Fosso O.B. The Mode Mixing Problem and its Influence in the Neural Activity Reconstruction. IAENG International Journal of Computer Science. 2019; 46 (3): 11.

17. Yang Y., DengJ., Wu C. Analysis of Mode Mixing Phenomenon in the Empirical Mode Decomposition Method. In 2009 Second International Symposium on Information Science and Engineering, Shanghai, China; 2009: 553-556. DOI: 10.1109/ISISE.2009.19.

18. Wu Z., Huang N.E. Ensemble empirical mode decomposition: a noise-assisted data analysis method. Adv. Adapt. Data Anal. 2009; 01 (01): 1-41. DOI: 10.1142/S1793536909000047.

19. 19 Deering R., Kaiser J.F. The use of a masking signal to improve empirical mode decomposition. In: Proceedings. (ICASSP '05). IEEE International Conference on Acoustics, Speech, and Signal Processing. 2005; 4: iv/485-iv/488. DOI: 10.1109/ICASSP.2005.1416051.

20. Wang Y.H., Hu K., Lo M.T. Uniform Phase Empirical Mode Decomposition: An Optimal Hybridization of Masking Signal and Ensemble Approaches'. IEEE Access. 2018; 6: 34819-34833. DOI: 10.1109/ACCESS.2018.2847634.IEEE Access 2018; 6: 34819-34833.

21. Gramfort A., Luessi M., Larson E., Engemann D.A., Strohmeier D., Brodbeck C.H., Goj R., Brooks T., Parkkonen L., Hamalainen M. MEG and EEG data analysis with MNE-Python. Front Neurosci. 2013; 26 (7): 1-13. DOI: 1O.3389/fnins.2O13.00267.

22. Quinn A.J., Lopes dos Santos V., Dupret D., Nobre A.CH., Mark W. Woolrich M.W. EMD: Empirical Mode Decomposition and Hilbert-Huang Spectral Analyses in Python. J Open Source Softw. 2021; 6 (59): 1-8. DOI: 10.21105/joss.02977.

23. Quinn A.J, Lopes-dos-Santos V., Huang N., Liang W.K., Juan Ch.H., Yeh J-R., Nobre A.C., Dupret D., Woolrich M.W. Within-cycle instantaneous frequency profiles report oscillatory waveform dynamics. bio-Rxiv. 2021.04.12.439547. DOI: 10.1101/2021.04.12.439547.

24. Kenny J.D., Westover M.B., Ching S., Brown E.N., Solt K. Propofol and sevoflurane induce distinct burst suppression patterns in rats. Front. Syst. Neurosci. 2014; 8 (237): 1-13. DOI: 10.3389/fnsys.2014.00237.

25. Vijn P.C., Sneyd J.R. I.v. anaesthesia and EEG burst suppression in rats: bolus injections and closed-loop infusions. Br. J. Anaesth. 1998; 81 (3): 415-421. DOI: 10.1093/bja/81.3.415.

26. Freye E., Levy J.V. Cerebral Monitoring in the Operating Room and the Intensive Care Unit: An Introductory for the Clinician and a Guide for the Novice Wanting to Open a Window to the Brain. J. Clin. Monit. Comput. 2005; 19 (1): 1-76. DOI: 10.1007/s10877-005-0712-z.

27. Hesse S., Kreuzer M., Hight D., Gaskell A., Devari P., Singh D., Taylor N.B., Whalin M.K., Lee S., Sleigh J.W., Garcia P.S.Association of electroencephalogram trajectories during emergence from anaesthesia with delirium in the postanaesthesia care unit: an early sign of postoperative complications'. Br. J. Anaesth. 2019; 122 (5): 622-634. doi: 10.1016/j.bja.2018.09.016.

28. Hight D., L. J. Voss L.J., Garcia P.S., J. Sleigh J.W. Changes in Alpha Frequency and Power of the Electroencephalogram during VolatileBased General Anesthesia. Front. Syst. Neurosci. 2017; 11 (36): DOI: 10.1016/j.bja.2018.09.016.10 doi: 10.3389/fnsys.2017.00036.

29. Sleigh J., Pullon R.M., Vlisides P.E., Warnaby C.E. Electroencephalographic slow wave dynamics and loss of behavioural responsiveness induced by ketamine in human volunteers. Br. J. Anaesth. 2019; 123 (5): 592-600. DOI: 10.1016/j.bja.2019.07.021.

30. Massimini M., Huber R., Ferrarelli F., Hill S., Giulio T. The Sleep Slow Oscillation as a Traveling Wave. J. Neurosci. 2004; 24 (31): 6862-6870. DOI: 10.1523/JNEUROSCI.1318-04.2004.

31. Murphy M., Bruno M-A., Riedner B.A., Boveroux P., Noirhomme Q., Landsness E., Brichant J-F., Phillips Ch., Massimini M., Laureys S., Tononi G., Boly M. Propofol Anesthesia and Sleep: A High-Density EEG Study. Sleep. 2011; 34 (3): 283-291A: DOI: 10.1093/sleep/34.3.283.

32. Lewis L.D., Ching Sh., Weiner V.S., Peterfreund R.A., Eskandar E.N., Cash S.S., Brown E.N., Purdon P.L. Local cortical dynamics of burst suppression in the anaesthetized brain. Brain. 2013; 136 (9) 27272737. DOI: 10.1093/brain/awt174.

33. Ming Q., Liou J-Y., Yang F., Li J., Chu Ch., Zhou Q., Wu D., Xu S., Luo P. Liang J., Li D., Pryor K.O., Lin W., Schwartz T., Ma H. Isoflurane-In-duced Burst Suppression Is a Thalamus-Modulated, Focal-Onset Rhythm With Persistent Local Asynchrony and Variable Propagation Patterns in Rats. Front. Syst. Neurosci. 2021; 14: 1-11. DOI: 10.3389/fnsys.2020.599781.

34. Lang X., Zheng Q., Zhang Z., Lu S., Xie L., Horch A., Su H. Fast Multivariate Empirical Mode Decomposition. IEEE Access PP; 2018; 99: 1-18. DOI: 10.1109/ACCESS.2018.2877150.

35. Rehman N., Mandic D.P. Multivariate empirical mode decomposition. Proc. R. Soc. Math. Phys. Eng. Sci. 2010; 466 (2117): 1291-1302.DOI: 10.1098/rspa.2009.0502.

36. Wu Z., Feng J., Qiao F., Tan Z.-M. Fast multidimensional ensemble empirical mode decomposition for the analysis of big spatio-temporal datasets. Philos. Trans. R. Soc. Math. Phys. Eng. Sci. 2016; 374 (2065): 20150197. DOI: 10.1098/rsta.2015.0197.

37. Amzica F., Steriade M. Electrophysiological correlates of sleep delta waves. Electroencephalogr. Clin. Neurophysiol. 1998; 107 (2): 69-83. DOI: 10.1016/S0013-4694 (98)00051-0.

38. Chen S-J., Peng Ch-J., Chen Y-Ch., Hwang Y-R., Lai Y-S., Fan S-Z., Jen K-K. Comparison of FFT and marginal spectra of EEG using empirical mode decomposition to monitor anesthesia. Comput. Methods Programs Biomed. 2016; 137: 77-85. DOI: 10.1016/j.cmpb.2016.08.024.

39. Li Ch., Li D., Liang Z., Voss L.J., Sleigh J.W. Analysis of depth of anesthesia with Hilbert-Huang spectral entropy. Clin. Neurophysiol. 2008; 119 (11): 2465-2475. DOI: 10.1016/j.clinph.2008.08.006.

40. Cole S. R., Voytek B. Brain Oscillations and the Importance of Waveform Shape. Trends Cogn. Sci. 2017; 21 (2): 137-149. DOI: 10.1016/j.tics.2016.12.008.

41. van Ede F., Quinn A.J., Woolrich M.W., Nobre A.C. Neural Oscillations: Sustained Rhythms or Transient Burst-Events? Trends Neurosci. 2018; 41 (7): 415-417. DOI: 10.1016/j.tins.2018.04.004.

42. Vidaurre D., Quinn A.J., Baker A.P., Dupret D., Tejero-Cantero A.,Wo-olrich M.W. Spectrally resolved fast transient brain states in electrophysiological data. NeuroImage. 2016; 126: 81-95. DOI: 10.1016/j.ne-uroimage.2015.11.047.

43. Bartz S., Avarvand F.S., Leicht G., Nolte G. Analyzing the waveshape of brain oscillations with bicoherence. NeuroImage. 2019; 188: 145-160. DOI: 10.1016/j.neuroimage.2018.11.045.

44. Quinn A.J. Within-cycle instantaneous frequency profiles report oscillatory waveform dynamics. bioRxiv, 2012: 2021.04.12.439547. DOI: 10.1101/2021.04.12.439547.

45. Soler A., Munoz-Gutierrez PA., Bueno-Lopez M., Giraldo E., Molinas M. Low-Density EEG for Neural Activity Reconstruction Using Multivariate Empirical Mode Decomposition. Front. Neurosci; 2020: 14 DOI: 10.3389/fnins.2020.00175.

46. Kortelainen J., Vayrynen E. Assessing EEG slow wave activity during anesthesia using Hilbert-Huang Transform. in 2015 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC). 2015: 117-120. doi: 10.1109/EMBC.2015.7318314.

47. Cole S.R., van der Meij R., Peterson E.J., de Hemptinne C., Starr P.A., Voytek B. Nonsinusoidal Beta Oscillations Reflect Cortical Pathophysiology in Parkinson's Disease. J. Neurosci. 2017; 37 (18): 4830-4840. DOI: 10.1523/JNEUROSCI.2208-16.2017.

48. Amzica F., Steriade M. ‘Electrophysiological correlates of sleep delta waves', Electroencephalogr. Clin. Neurophysiol. 1998; 107 (2): 69-83. DOI: 10.1016/S0013-4694(98)00051-0.

49. Huang N.E., Shen Zh., Long S.R., Wu M.L.C. The empirical mode decomposition and the Hilbert spectrum for nonlinear and non-stationary time series analysis. Lond. Ser. Math. Phys. Eng. Sci. 1998; 454 (1971): 903-995. DOI: 10.1098/rspa.1998.0193.

50. Wang Y.-H, Hu K., Lo M.-T. Uniform Phase Empirical Mode Decomposition: An Optimal Hybridization of Masking Signal and Ensemble Approaches', IEEE Access. 2018; 6: 34819-34833. DOI: 10.1109/ACCESS.2018.2847634.

51. Yang Y., Deng J., Wu C. Analysis of Mode Mixing Phenomenon in the Empirical Mode Decomposition Method', in 2009 Second International Symposium on Information Science and Engineering, Shanghai, China. 2009: 553-556. DOI: 10.1109/ISISE.2009.19.

52. Deering R., Kaiser J.F. The use of a masking signal to improve empirical mode decomposition', in Proceedings. (ICASSP '05). IEEE International Conference on Acoustics, Speech, and Signal Processing. 2005; 4: iv/485-iv/488. DOI: 10.1109/ICASSP.2005.1416051.

53. Wu Z., Huang N.E. Ensemble empirical mode decomposition: a noise-assisted data analysis method. Adv. Adapt. Data Anal. 2009: 01 (01): 1-41. DOI: 10.1142/S1793536909000047.

54. Fabus M.S., Quinn A.J., Warnaby C.E., Woolrich M.W. Automatic decomposition of electrophysiological data into distinct non-sinusoidal oscillatory modes. bioRxiv, 2021: 2021.07.06.451245. DOI: 10.1101/2021.07.06.451245.

55. Lo M.-T., Novak V., Peng C.-K., Liu Y., Hu K. Nonlinear phase interaction between nonstationary signals: A comparison study of methods based on Hilbert-Huang and Fourier transforms. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 2009; 79 (6 Pt 1): 061924 DOI: 10.1103/Phys-RevE.79.061924.


Review

For citations:


Sobolova G., Fabus M.S., Fischer M., Drobny M., Drobna-Saniova B. Instantaneous EEG Signal Analysis Based on Empirical Mode Decomposition Applied to Burst-Suppression in Propofol Anaesthesia. General Reanimatology. 2021;17(5):65-79. https://doi.org/10.15360/1813-9779-2021-5-65-79

Views: 798


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 1813-9779 (Print)
ISSN 2411-7110 (Online)