# Novel Early EEG Measures Predicting Brain Recovery after Cardiac Arrest

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## Abstract

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## 1. Introduction

## 2. Quantitative EEG Predicting Long-Term Brain Injury after CA

#### 2.1. Review of Shannon Entropy Based qEEG Measures

#### 2.2. Novel qEEG Measures Exploiting Critical Transition in EEG

## 3. Experimental Methods

## 4. Results

## 5. Conclusions

## Acknowledgments

## Author Contributions

## Conflicts of Interest

## References

- Bedell, S.E.; Delbanco, T.L.; Cook, E.F.; Epstein, F.H. Survival after cardiopulmonary resuscitation in the hospital. N. Engl. J. Med.
**1983**, 309, 569–576. [Google Scholar] [CrossRef] [PubMed] - Longstreth, W.T.; Diehr, P.; Inui, T.S. Prediction of awakening after out of hospital cardiac arrest. N. Engl. J. Med.
**1983**, 308, 1378–1382. [Google Scholar] [CrossRef] [PubMed] - Berek, K.; Jeschow, M.; Aichner, F. The prognostication of cerebral hypoxia after out of hospital cardiac arrest in adults. Eur. Neurol.
**1997**, 37, 135–145. [Google Scholar] [CrossRef] [PubMed] - Safar, P. Cerebral resuscitation after cardiac arrest: A review. Circulation
**1986**, 74, IV138–IV153. [Google Scholar] [PubMed] - Vaagenes, P.; Ginsberg, M.; Ebmeyer, U.; Ernster, L.; Fischer, M.; Gisvold, S.E.; Gurvitch, A.; Hossmann, K.A.; Nemoto, E.M.; Radovsky, A.; et al. Cerebral resuscitation from cardiac arrest: Pathophysiologic mechanisms. Crit. Care Med.
**1996**, 24, S57–S68. [Google Scholar] [CrossRef] [PubMed] - American Heart Association in Collaboration; International Liaison Committee on Resuscitation (IL-COR). Guidelines 2000 for cardiopulmonary resuscitation and emergency cardiovascular care—An international consensus on science. Circulation
**2000**, 102, I-1–I-11. [Google Scholar] - Nolan, J.P.; Morley, P.T.; Hoek, T.L.; Hickey, R.W.; Advancement Life Support Task Force of the International Liaison Committee on Resuscitation. Therapeutic hypothermia after cardiac arrest. An advisory statement by the advancement life support task force of the international liaison committee on resuscitation. Circulation
**2003**, 57, 231–235. [Google Scholar] - Bezerianos, A.; Tong, S.; Thakor, N.V. Time-dependent entropy estimation of EEG rhythm changes following brain ischemia. Ann. Biomed. Eng.
**2003**, 31, 221–232. [Google Scholar] [CrossRef] [PubMed] - Thakor, N.V.; Tong, S. Advances in quantitative electroencephalogram analysis methods. Annu. Rev. Biomed. Eng.
**2004**, 6, 453–495. [Google Scholar] [CrossRef] [PubMed] - Shin, H.C.; Tong, S.; Yamashita, S.; Jia, X.; Geocadin, R.G.; Thakor, N.V. Quantitative EEG and Effect of Hypothermia on Brain Recovery after Cardiac Arrest. IEEE Trans. Biomed. Eng.
**2006**, 53, 1016–1023. [Google Scholar] [CrossRef] [PubMed] - Thakor, N.V.; Shin, H.C.; Tong, S.; Geocadin, R. Quantitative EEG Assessment. IEEE Eng. Med. Biol. Mag.
**2006**, 25, 20–25. [Google Scholar] [CrossRef] [PubMed] - Shin, H.C.; Jia, X.; Nickl, R.; Geocadin, R.G.; Thakor, N.V. A Subband-based Information measure of EEG during Brain Injury and Recovery After Cardiac Arrest. IEEE Trans. Biomed. Eng.
**2008**, 55, 1985–1990. [Google Scholar] [CrossRef] [PubMed] - Rosso, O.A.; Blanco, S.; Yordanova, J.; Kolev, V.; Figliola, A.; Schürmann, M.; Basar, E. Wavelet entropy: A new tool for analysis of short duration brain electrical signals. J. Neurosci. Methods
**2001**, 105, 65–75. [Google Scholar] [CrossRef] - Yordanova, J.; Kolev, V.; Rosso, O.A.; Schürmann, M.; Sakowitz, O.W.; Özgören, M.; Basar, E. Wavelet entropy analysis of event-related potentials indicates modality-independent theta dominance. J. Neurosci. Methods
**2002**, 117, 99–109. [Google Scholar] [CrossRef] - Edgren, E.; Hedstrand, U.; Kelsey, S.; Sutton-Tyrrell, K.; Safar, P.; BRCTI Study Group. Assessment of neurological prognosis in comatose survivors of cardiac arrest. Lancet
**1994**, 343, 1055–1059. [Google Scholar] [CrossRef] - Bernard, S.A.; Gray, T.; Buist, M.; Jones, B.; Silvestar, W.; Gutteridge, G.; Smith, K. Treatment of comatose survivors of out-of-hospital cardiac arrest with induced hypothermia. N. Engl. J. Med.
**2002**, 346, 557–563. [Google Scholar] [CrossRef] [PubMed] - Shannon, C.E. A mathematical theory of communication. Bell Syst. Tech. J.
**1948**, 27, 379–423. [Google Scholar] [CrossRef] - Geocardin, R.G.; Ghodadra, R.; Kimura, T.; Lei, H.; Sherman, D.L.; Hanley, D.F.; Thakor, N.V. A novel quantitative EEG injury measure of global cerebral ischemia. Clin. Neurophysiol.
**2000**, 111, 1779–1787. [Google Scholar] [CrossRef] - Katz, L.; Ebmeyer, U.; Safar, P.; Radovsky, A.; Neumar, R. Outcome model of asphyxia cardiac arrest in rats. J. Cereb. Blood Flow Metab.
**1995**, 15, 1032–1039. [Google Scholar] [CrossRef] [PubMed]

**Figure 1.**Electroencephalogram (EEG) signals and typical time evolution of subband IQ (SIQ). (

**a**) Progression of SIQ for the high neurological deficit score (NDS) (67), 5 min cardiac arrest (CA) and (

**b**) evolution of SIQ for the low NDS (45), 9 min CA.

**Figure 2.**Slope, ${\Delta}_{s}\left(t\right)$, of typical quantitative electroencephalogram (qEEG) evolution.

**Figure 3.**Novel qEEG measures, ${t}_{iso}$ and ${t}_{max}$, of various NDS classes (high, middle, and low). (

**a**) time evolution of ${\Delta}_{s}\left(t\right)$ during high NDS (67); (

**b**) time evolution of ${\Delta}_{s}\left(t\right)$ during middle NDS (54); (

**c**) time evolution of ${\Delta}_{s}\left(t\right)$ during low NDS (41).

**Figure 5.**${t}_{iso}$ and ${t}_{max}$ according to $\epsilon $ and ${t}_{0}$. (

**a**) variation of $\epsilon $ (

**b**) variation of ${t}_{0}$.

**Figure 6.**Correlation coefficients of various measures with NDS. (

**a**) ${t}_{iso}$ vs. NDS (

**b**) (${t}_{iso}$ + asphyxia) vs. NDS (

**c**) ${t}_{fast}$ vs. NDS; and (

**d**) ${\mu}_{SIQ}$ vs. NDS.

**Table 1.**Outcomes of the various measures for the whole data set. Bold indicates the rats applied clinical hypothermia.

Rat Num. | Asphyxia (min) | NDS | ${\mathit{t}}_{\mathit{iso}}$ (min) | ${\mathit{t}}_{\mathit{iso}}$ + Asphyxia | ${\mathit{t}}_{\mathit{fast}}$ (min) | ${\mathit{\mu}}_{\mathit{SIQ}}$ |
---|---|---|---|---|---|---|

1 | 5 | 75 | 6.73 | 11.73 | 6.27 | 1.1920 |

2 | 5 | 71 | 6.33 | 11.33 | 6.14 | 1.0245 |

3 | 5 | 67 | 9.40 | 14.40 | 4.13 | 0.7412 |

4 | 5 | 60 | 11.98 | 16.98 | 3.47 | 0.6222 |

correlation coefficient | $-0.9470$ | $-0.9470$ | 0.9358 | 0.9622 | ||

p-value | 0.0530 | 0.0530 | 0.0642 | 0.0378 | ||

5 | 7 | 70 | 5.35 | 12.35 | 2.67 | 1.0121 |

6 | 7 | 65 | 10.33 | 17.33 | 11.07 | 0.8879 |

7 | 7 | 60 | 14.97 | 21.97 | 11.06 | 0.5869 |

8 | 7 | 54 | 14.58 | 21.58 | 3.60 | 0.9063 |

9 | 7 | 51 | 12.60 | 19.60 | 7.07 | 0.5117 |

10 | 7 | 50 | 16.47 | 23.47 | 5.20 | 0.8929 |

11 | 7 | 47 | 14.20 | 21.20 | 4.80 | 0.6859 |

12 | 7 | 45 | 13.98 | 20.98 | 9.34 | 0.5716 |

13 | 7 | 41 | 13.93 | 20.93 | 5.20 | 0.5619 |

14 | 7 | 39 | 15.67 | 22.67 | 2.93 | 0.5647 |

correlation coefficient | $-0.7376$ | $-0.7376$ | 0.2497 | 0.6806 | ||

p-value | 0.0149 | 0.0149 | 0.4866 | 0.0303 | ||

15 | 9 | 52 | 19.62 | 28.62 | 2.93 | 0.4707 |

16 | 9 | 50 | 18.80 | 27.80 | 1.87 | 0.5584 |

17 | 9 | 49 | 19.32 | 28.32 | 3.46 | 0.6547 |

18 | 9 | 45 | 16.10 | 25.10 | 6.27 | 0.7770 |

19 | 9 | 41 | 16.87 | 25.87 | 3.20 | 0.6253 |

correlation coefficient | 0.8524 | 0.8524 | $-0.4047$ | $-0.6004$ | ||

p-value | 0.0666 | 0.0666 | 0.4991 | 0.2843 | ||

Total | ||||||

correlation coefficient | $-0.7888$ | $-0.7849$ | 0.2025 | 0.7085 | ||

p-value | 0.0001 | 0.0001 | 0.4058 | 0.001 |

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**MDPI and ACS Style**

Cha, K.-M.; Thakor, N.V.; Shin, H.-C. Novel Early EEG Measures Predicting Brain Recovery after Cardiac Arrest. *Entropy* **2017**, *19*, 466.
https://doi.org/10.3390/e19090466

**AMA Style**

Cha K-M, Thakor NV, Shin H-C. Novel Early EEG Measures Predicting Brain Recovery after Cardiac Arrest. *Entropy*. 2017; 19(9):466.
https://doi.org/10.3390/e19090466

**Chicago/Turabian Style**

Cha, Kab-Mun, Nitish V. Thakor, and Hyun-Chool Shin. 2017. "Novel Early EEG Measures Predicting Brain Recovery after Cardiac Arrest" *Entropy* 19, no. 9: 466.
https://doi.org/10.3390/e19090466