Application of scalp electroencephalogram in treatment of refractory epilepsy with vagus nerve stimulation_Journal of Biomedical Engineering

Authors：

QIN Xiaoya ^1,2 , YUAN Yuan ^1,2 , CHEN Yan ³ , LIAO Jianxiang ^3,4 , LIN Sufang ³ , YANG Zhao ² ,  LI Luming ^1,2,5,6

1. Precision Medicine & Healthcare Research Center, Tsinghua-Berkeley Shenzhen Institute, Tsinghua University, Shenzhen, Guangdong 518071, P.R.China;
2. National Engineering Laboratory for Neuromodulation, School of Aerospace Engineering, Tsinghua University, Beijing 100084, P.R.China;
3. Epilepsy Center, Shenzhen Children's Hospital, Shenzhen, Guangdong 518038, P.R.China;
4. Department of Neurology, Shenzhen Children's Hospital, Shenzhen, Guangdong 518038, P.R.China;
5. IDG/McGovern Institute for Brain Research at Tsinghua University, Beijing 100084, P.R.China;
6. Institute of Epilepsy, Beijing Institute for Brain Disorders, Beijing 100093, P.R.China;

Corresponding author：

Keywords：

vagus nerve stimulation; electroencephalogram; therapeutic effect prediction; curative effect evaluation; treatment mechanism

DOI：

10.7507/1001-5515.201909002

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Electroencephalogram (EEG) has been an important tool for scientists to study epilepsy and evaluate the treatment of epilepsy for half a century, since epilepsy seizures are caused by the diffusion of excessive discharge of brain neurons. This paper reviews the clinical application of scalp EEG in the treatment of intractable epilepsy with vagus nerve stimulation (VNS) in the past 30 years. It mainly introduces the prediction of the therapeutic effect of VNS on intractable epilepsy based on EEG characteristics and the effect of VNS on EEG of patients with intractable epilepsy, and expounds some therapeutic mechanisms of VNS. For predicting the efficacy of VNS based on EEG characteristics, EEG characteristics such as epileptiform discharge, polarity of slow cortical potential changes, changes of EEG symmetry level and changes of EEG power spectrum are described. In view of the influence of VNS treatment on patients’ EEG characteristics, the change of epileptiform discharge, power spectrum, synchrony, brain network and amplitude of event-related potential P300 are described. Although no representative EEG markers have been identified for clinical promotion, this review paves the way for prospective studies of larger patient populations in the future to better apply EEG to the clinical treatment of VNS, and provides ideas for predicting VNS efficacy, assessing VNS efficacy, and understanding VNS treatment mechanisms, with broad medical and scientific implications.

Citation： QIN Xiaoya, YUAN Yuan, CHEN Yan, LIAO Jianxiang, LIN Sufang, YANG Zhao, LI Luming. Application of scalp electroencephalogram in treatment of refractory epilepsy with vagus nerve stimulation. Journal of Biomedical Engineering, 2020, 37(4): 699-707. doi: 10.7507/1001-5515.201909002 Copy

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3.	Hoppe C, Poepel A, Elger C E. Epilepsy: accuracy of patient seizure counts. Arch Neurol, 2007, 64(11): 1595-1599.
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12.	de Vos C C, Melching L, van Schoonhoven J, <italic>et al</italic>. Predicting success of vagus nerve stimulation (VNS) from interictal EEG. Seizure, 2011, 20(7): 541-545.
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15.	Ravan M, Sabesan S, D'Cruz O. On quantitative biomarkers of VNS therapy using EEG and ECG signals. IEEE Trans Biomed Eng, 2017, 64(2): 419-428.
16.	Brázdil M, Doležalová I, Koritáková E, <italic>et al</italic>. EEG reactivity predicts individual efficacy of vagal nerve stimulation in intractable epileptics. Front Neurol, 2019, 10: 392.
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36.	Santiago-Rodríguez E, Alonso-Vanegas M, Cárdenas-Morales L, <italic>et al</italic>. Effects of two different cycles of vagus nerve stimulation on interictal epileptiform discharges. Seizure, 2006, 15(8): 615-620.
37.	Wang Haiyang, Chen Xiaoguang, Lin Zhiguo, <italic>et al</italic>. Long-term effect of vagus nerve stimulation on interictal epileptiform discharges in refractory epilepsy. J Neurol Sci, 2009, 284(1/2): 96-102.
38.	Kuba R, Nesvadba D, Brázdil M, <italic>et al</italic>. Effect of chronic vagal nerve stimulation on interictal epileptiform discharges. Seizure, 2010, 19(6): 352-355.
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1. Ulate-Campos A, Coughlin F, Gaínza-Lein M, <italic>et al</italic>. Automated seizure detection systems and their effectiveness for each type of seizure. Seizure, 2016, 40: 88-101.
2. Engineer C T, Hays S A, Kilgard M P. Vagus nerve stimulation as a potential adjuvant to behavioral therapy for autism and other neurodevelopmental disorders. J Neurodev Disord, 2017, 9(1): 20.
3. Hoppe C, Poepel A, Elger C E. Epilepsy: accuracy of patient seizure counts. Arch Neurol, 2007, 64(11): 1595-1599.
4. Akman C I, Montenegro M A, Jacob S, <italic>et al</italic>. Seizure frequency in children with epilepsy: Factors influencing accuracy and parental awareness. Seizure, 2009, 18(7): 524-529.
5. 任国平, 王群. 癫痫的电生理机制研究进展//第六届CAAE脑电图与神经电生理大会会刊. 中国抗癫痫协会脑电图与神经电生理分会, 2018: 58.
6. Aminoff M J. Electrodiagnosis in clinical neurology. 4th ed. New York: Churchill Livingstone, 1999.
7. Nuwer M. Assessment of digital EEG, quantitative EEG, and EEG brain mapping: Report of the American Academy of Neurology and the American Clinical Neurophysiology Society. Neurology, 1997, 49(1): 277-292.
8. 刘晓燕. 临床脑电图学. 第2版. 北京: 人民卫生出版社, 2017.
9. Janszky J, Hoppe M, Behne F, <italic>et al</italic>. Vagus nerve stimulation: Predictors of seizure freedom. J Neurol Neurosurg Psychiatry, 2005, 76(3): 384-389.
10. Majoie H M, Berfelo M W, Aldenkamp A P, <italic>et al</italic>. Vagus nerve stimulation in patients with catastrophic childhood epilepsy, a 2-year follow-up study. Seizure, 2005, 14(1): 10-18.
11. Kim M, Yum M, Kim E, <italic>et al</italic>. An interictal EEG can predict the outcome of vagus nerve stimulation therapy for children with intractable epilepsy. Child's Nervous System, 2017, 33(1): 145-151.
12. de Vos C C, Melching L, van Schoonhoven J, <italic>et al</italic>. Predicting success of vagus nerve stimulation (VNS) from interictal EEG. Seizure, 2011, 20(7): 541-545.
13. Hilderink J, Tjepkema-Cloostermans M C, Geertsema A, <italic>et al</italic>. Predicting success of vagus nerve stimulation (VNS) from EEG symmetry. Seizure, 2017, 48: 69-73.
14. Bayasgalan B, Matsuhashi M, Fumuro T, <italic>et al</italic>. We could predict good responders to vagus nerve stimulation: A surrogate marker by slow cortical potential shift. Clin Neurophysiol, 2017, 128(9): 1583-1589.
15. Ravan M, Sabesan S, D'Cruz O. On quantitative biomarkers of VNS therapy using EEG and ECG signals. IEEE Trans Biomed Eng, 2017, 64(2): 419-428.
16. Brázdil M, Doležalová I, Koritáková E, <italic>et al</italic>. EEG reactivity predicts individual efficacy of vagal nerve stimulation in intractable epileptics. Front Neurol, 2019, 10: 392.
17. Li H, Zhiguo Z. EEG signal processing and feature extraction. Singapore: Springer, 2019.
18. Andersen P, Andersson S A, Lomo T. Thalamo-cortical relations during spontaneous barbiturate spindles. Electroencephalogr Clin Neurophysiol, 1968, 24(1): 90.
19. Timofeev I, Steriade M. Fast (mainly 30-100 Hz) oscillations in the cat cerebellothalamic pathway and their synchronization with cortical potentials. J Physiol, 1997, 504(Pt 1): 153-168.
20. Gaal Z A, Boha R, Stam C J, <italic>et al</italic>. Age-dependent features of EEG-reactivity—Spectral, complexity, and network characteristics. Neurosci Lett, 2010, 479(1): 79-84.
21. Bartolomei F, Bonini F, Vidal E, <italic>et al</italic>. How does vagal nerve stimulation (VNS) change EEG brain functional connectivity? Epilepsy Res, 2016, 126: 141-146.
22. Ilyas A, Toth E, Pizarro D, <italic>et al</italic>. Modulation of neural oscillations by vagus nerve stimulation in posttraumatic multifocal epilepsy: case report. J Neurosurg, 2019, 131(4): 1079-1085.
23. Marrosu F, Santoni F, Puligheddu M, <italic>et al</italic>. Increase in 20-50 Hz (gamma frequencies) power spectrum and synchronization after chronic vagal nerve stimulation. Clin Neurophysiol, 2005, 116(9): 2026-2036.
24. De Herdt V, De Waele J, Raedt R, <italic>et al</italic>. Modulation of seizure threshold by vagus nerve stimulation in an animal model for motor seizures. Acta Neurol Scand, 2010, 121(4): 271-276.
25. Ikeda A, Terada K, Mikuni N, <italic>et al</italic>. Subdural recording of ictal DC shifts in neocortical seizures in humans. Epilepsia, 1996, 37(7): 662-674.
26. Ayala G F, Dichter M, Gumnit R J, <italic>et al</italic>. Genesis of epileptic interictal spikes. New knowledge of cortical feedback systems suggests a neurophysiological explanation of brief paroxysms. Brain Res, 1973, 52: 1-17.
27. Zagon A, Kemeny A A. Slow hyperpolarization in cortical neurons: a possible mechanism behind vagus nerve simulation therapy for refractory epilepsy? Epilepsia, 2000, 41(11): 1382-1389.
28. 姜涛, 吴效明, 叶丙刚. 基于皮质慢电位特征分析的神经皮质运动区功能定位. 中国组织工程研究与临床康复, 2010, 14(26): 4801-4804.
29. van Putten M J. The revised brain symmetry index. Clin Neurophysiol, 2007, 118(11): 2362-2367.
30. Hammond E J, Uthman B M, Reid S A, <italic>et al</italic>. Vagus nerve stimulation in humans: neurophysiological studies and electrophysiological monitoring. Epilepsia, 1990, 31(Suppl 2): S51-S59.
31. Hammond E J, Uthman B M, Reid S A, <italic>et al</italic>. Electrophysiological studies of cervical vagus nerve stimulation in humans: I. EEG effects. Epilepsia, 1992, 33(6): 1013-1020.
32. Koo B. EEG changes with vagus nerve stimulation. J Clin Neurophysiol, 2001, 18(5): 434-441.
33. Kuba R, Guzaninová M, Brázdil M, <italic>et al</italic>. Effect of vagal nerve stimulation on interictal epileptiform discharges: a scalp EEG study. Epilepsia, 2002, 43(10): 1181-1188.
34. Ebus S C, Majoie H J, Arends J B, <italic>et al</italic>. Can spikes predict seizure frequency? Results of a pilot study in severe childhood epilepsies treated with vagus nerve stimulation. Seizure, 2004, 13(7): 494-498.
35. Hallbook T, Lundgren J, Blennow G, <italic>et al</italic>. Long term effects on epileptiform activity with vagus nerve stimulation in children. Seizure, 2005, 14(8): 527-533.
36. Santiago-Rodríguez E, Alonso-Vanegas M, Cárdenas-Morales L, <italic>et al</italic>. Effects of two different cycles of vagus nerve stimulation on interictal epileptiform discharges. Seizure, 2006, 15(8): 615-620.
37. Wang Haiyang, Chen Xiaoguang, Lin Zhiguo, <italic>et al</italic>. Long-term effect of vagus nerve stimulation on interictal epileptiform discharges in refractory epilepsy. J Neurol Sci, 2009, 284(1/2): 96-102.
38. Kuba R, Nesvadba D, Brázdil M, <italic>et al</italic>. Effect of chronic vagal nerve stimulation on interictal epileptiform discharges. Seizure, 2010, 19(6): 352-355.
39. 林志国, 王海洋, 孙伯民, 等. 迷走神经刺激治疗顽固性癫痫脑电变化的初步研究//2011中华医学会神经外科学学术会议论文汇编. 中华医学会、中华医学会神经外科学分会, 2011: 2162.
40. Ravan M, Begnaud J. Investigating the effect of short term responsive VNS therapy on sleep quality using automatic sleep staging. IEEE Trans Biomed Eng, 2019, 66(12): 3301-3309.
41. Salinsky M C, Burchiel K J. Vagus nerve stimulation has no effect on awake EEG rhythms in humans. Epilepsia, 1993, 34(2): 299-304.
42. Bewernitz M, Ghacibeh G, Seref O, et al. Quantification of the impact of vagus nerve stimulation parameters on electroencephalographic measures//Seref O, Kundakcioglu O E, Pardalos P M. AIP Conference Proceedings, 2007: 206.
43. Fraschini M, Puligheddu M, Demuru M, <italic>et al</italic>. VNS induced desynchronization in gamma bands correlates with positive clinical outcome in temporal lobe pharmacoresistant epilepsy. Neurosci Lett, 2013, 536: 14-18.
44. Bodin C, Aubert S, Daquin G, <italic>et al</italic>. Responders to vagus nerve stimulation (VNS) in refractory epilepsy have reduced interictal cortical synchronicity on scalp EEG. Epilepsy Res, 2015, 113: 98-103.
45. Ravan M. Investigating the correlation between short-term effectiveness of VNS Therapy in reducing the severity of seizures and long-term responsiveness. Epilepsy Res, 2017, 133: 46-53.
46. De Taeye L, Vonck K, van Bochove M, <italic>et al</italic>. The P3 event-related potential is a biomarker for the efficacy of vagus nerve stimulation in patients with epilepsy. Neurotherapeutics, 2014, 11(3): 612-622.
47. Wostyn S, Staljanssens W, De Taeye L, <italic>et al</italic>. EEG derived brain activity reflects treatment response from vagus nerve stimulation in patients with epilepsy. Int J Neural Syst, 2017, 27(4): 1650048.
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