Advances in clinical application of stereoelectroencephalography-based electrical stimulation in the evaluation of refractory epilepsy_West China Medical Journal

Authors：

CHEN Wenjing ¹ , ZHANG Yue ² , LAI Dakun ² ,  LI Zhenlin ³

1. Department of Neurosurgery, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;
2. School of Electronic Science and Engineering, University of Electronic Science and Technology of China, Chengdu, Sichuan 611731, P. R. China;
3. Department of Radiology, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;

Corresponding author：

LI Zhenlin, Email: HX_lizhenlin@126.com

Keywords：

Epilepsy; epileptogenic foci; stereoelectroencephalography; stereo-electric stimulation; assessment of brain functional areas

DOI：

10.7507/1002-0179.202212112

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For refractory epilepsy requiring surgical treatment in clinic, precise preoperative positioning of the epileptogenic zone is the key to improving the success rate of clinical surgical treatment. Although the use of electrical stimulation to locate epileptogenic zone has been widely carried out in many medical centers, the preoperative implantation evaluation of stereoelectroencephalography (SEEG) and the interpretation of electrical stimulation induced EEG activity are still not perfect and rigorous. Especially, there are still technological limitations and unknown areas regarding electrode implantation mode, stimulation parameters design, and surgical prognosis correlation. In this paper, the clinical background, application status, technical progress and development trend of SEEG-based stereo-electric stimulation-induced cerebral electrical activity in the evaluation of refractory epilepsy are reviewed, and applications of this technology in clinical epileptogenic zone localization and cerebral cortical function evaluation are emphatically discussed. Additionally, the safety during both of high-frequency and low-frequency electrical stimulations which are commonly used in clinical evaluation of refractory epilepsy are also discussed.

Citation： CHEN Wenjing, ZHANG Yue, LAI Dakun, LI Zhenlin. Advances in clinical application of stereoelectroencephalography-based electrical stimulation in the evaluation of refractory epilepsy. West China Medical Journal, 2023, 38(5): 645-652. doi: 10.7507/1002-0179.202212112 Copy

1.	Samanta D. Recent developments in stereo electroencephalography monitoring for epilepsy surgery. Epilepsy Behav, 2022, 135: 108914.
2.	中国抗癫痫协会立体定向脑电图与脑定位学专业委员会, 中国医师协会神经外科医师分会, 国家神经外科机器人示范项目专家指导委员会. 立体定向脑电图临床应用的中国专家共识. 中华医学杂志, 2022, 102(39): 3095-3102.
3.	Britton JW. Electrical stimulation mapping with stereo-EEG electrodes. J Clin Neurophysiol, 2018, 35(2): 110-114.
4.	George DD, Ojemann SG, Drees C, et al. Stimulation mapping using stereoelectroencephalography: current and future directions. Front Neurol, 2020, 11: 320.
5.	Suller Marti A, Mirsattari SM, Steven DA, et al. Extraoperative electrical stimulation mapping in epilepsy presurgical evaluation: a proposal and review of the literature. Clin Neurol Neurosurg, 2022, 214: 107170.
6.	Blank LJ, Jette N. Epilepsy research in 2022: clinical advances. Lancet Neurol, 2023, 22(1): 15-17.
7.	Asadi-Pooya AA, Brigo F, Trinka E, et al. Physicians’ beliefs about brain surgery for drug-resistant epilepsy: a global survey. Seizure, 2022, 103: 18-22.
8.	Rheims S, Sperling MR, Ryvlin P. Drug-resistant epilepsy and mortality-why and when do neuromodulation and epilepsy surgery reduce overall mortality. Epilepsia, 2022, 63(12): 3020-3036.
9.	谭启富, 李玲, 吴承远. 癫痫外科学. 2 版. 北京: 人民卫生出版社, 2012: 9-29.
10.	Iwasaki M, Iijima K, Takayama Y, et al. Predictors of seizure outcome after repeat pediatric epilepsy surgery: reasons for failure, sex, electrophysiology, and temporal lobe surgery. Neurol Med Chir (Tokyo), 2022, 62(3): 125-132.
11.	Klodowski DA, George BJ, Sperling MR. Seizure latency and epilepsy localization as predictors of recurrence following epilepsy surgery. Epilepsia, 2022, 63(5): 1074-1080.
12.	Paulo DL, Ball TJ, Englot DJ. Emerging technologies for epilepsy surgery. Neurol Clin, 2022, 40(4): 849-867.
13.	Alim-Marvasti A, Vakharia VN, Duncan JS. Multimodal prognostic features of seizure freedom in epilepsy surgery. J Neurol Neurosurg Psychiatry, 2022, 93(5): 499-508.
14.	Gonzalez-Martinez JA. The stereo-electroencephalography: the epileptogenic zone. J Clin Neurophysiol, 2016, 33(6): 522-529.
15.	Mallela AN, Beiriger J, Gersey ZC, et al. Targeting the future: developing a training curriculum for robotic assisted neurosurgery. World Neurosurg, 2022, 167: e770-e777.
16.	Miller KJ, Fine AL. Decision-making in stereotactic epilepsy surgery. Epilepsia, 2022, 63(11): 2782-2801.
17.	Zhang D, Cui X, Zheng J, et al. Neurosurgical robot-assistant stereoelectroencephalography system: operability and accuracy. Brain Behav, 2021, 11(10): e2347.
18.	Talairach J, Bancaud J, Geier S, et al. The cingulate gyrus and human behaviour. Electroencephalogr Clin Neurophysiol, 1973, 34(1): 45-52.
19.	Abou-Al-Shaar H, Brock AA, Kundu B, et al. Increased nationwide use of stereoencephalography for intracranial epilepsy electroencephalography recordings. J Clin Neurosci, 2018, 53: 132-134.
20.	Mullin JP, Shriver M, Alomar S, et al. Is SEEG safe? A systematic review and meta-analysis of stereo-electroencephalography-related complications. Epilepsia, 2016, 57(3): 386-401.
21.	Bartholow R. Experiments on the functions of the human brain. BMJ, 1874, 1(700): 727.
22.	Drane DL, Pedersen NP, Sabsevitz DS, et al. Cognitive and emotional mapping with SEEG. Front Neurol, 2021, 12: 627981.
23.	McGonigal A, Lagarde S, Trébuchon-Dafonseca A, et al. Early onset motor semiology in seizures triggered by cortical stimulation during SEEG. Epilepsy Behav, 2018, 88: 262-267.
24.	Cardinale F, Rizzi M, Vignati E, et al. Stereoelectroencephalography: retrospective analysis of 742 procedures in a single centre. Brain, 2019, 142(9): 2688-2704.
25.	Baruah S, Olivier A, Hall JA. The changing nature of epilepsy surgery: a retrospective review of practice profiles. Can J Neurol Sci, 2022, 49(3): 387-392.
26.	Trebuchon A, Racila R, Cardinale F, et al. Electrical stimulation for seizure induction during SEEG exploration: a useful predictor of postoperative seizure recurrence?. J Neurol Neurosurg Psychiatry, 2020, 28: jnnp-2019-322469.
27.	Chassoux F, Devaux B, Landré E, et al. Stereoelectroencephalography in focal cortical dysplasia: a 3D approach to delineating the dysplastic cortex. Brain, 2000, 123(8): 1733-1751.
28.	Kahane P, Ryvlin P, Hoffmann D, et al. From hypothalamic hamartoma to cortex: what can be learnt from depth recordings and stimulation?. Epileptic Disord, 2003, 5(4): 205-217.
29.	Trébuchon A, Chauvel P. Electrical stimulation for seizure induction and functional mapping in stereoelectroencephalography. J Clin Neurophysiol, 2016, 33(6): 511-521.
30.	Cuello Oderiz C, von Ellenrieder N, Dubeau F, et al. Association of cortical stimulation-induced seizure with surgical outcome in patients with focal drug-resistant epilepsy. JAMA Neurol, 2019, 76(9): 1070-1078.
31.	Whitaker HA, Ojemann GA. Graded localisation of naming from electrical stimulation mapping of left cerebral cortex. Nature, 1977, 270(5632): 50-51.
32.	Isnard J, Taussig D, Bartolomei F, et al. French guidelines on stereoelectroencephalography (SEEG). Neurophysiol Clin, 2018, 48(1): 5-13.
33.	Hamberger MJ. Cortical language mapping in epilepsy: a critical review. Neuropsychol Rev, 2007, 17(4): 477-489.
34.	Matsumoto R, Nair DR, LaPresto E, et al. Functional connectivity in the human language system: a cortico-cortical evoked potential study. Brain, 2004, 127(10): 2316-2330.
35.	Perrone-Bertolotti M, Alexandre S, Jobb AS, et al. Probabilistic mapping of language networks from high frequency activity induced by direct electrical stimulation. Hum Brain Mapp, 2020, 41(14): 4113-4126.
36.	Thorsteinsdottir J, Vollmar C, Tonn JC, et al. Outcome after individualized stereoelectroencephalography (sEEG) implantation and navigated resection in patients with lesional and non-lesional focal epilepsy. J Neurol, 2019, 266(4): 910-920.
37.	Youngerman BE, Khan FA, McKhann GM. Stereoelectroencephalography in epilepsy, cognitive neurophysiology, and psychiatric disease: safety, efficacy, and place in therapy. Neuropsychiatr Dis Treat, 2019, 15: 1701-1716.
38.	Nowak LG, Bullier J. Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter. II. Evidence from selective inactivation of cell bodies and axon initial segments. Exp Brain Res, 1998, 118(4): 489-500.
39.	McCreery DB, Agnew WF, Yuen TG, et al. Charge density and charge per phase as cofactors in neural injury induced by electrical stimulation. IEEE Trans Biomed Eng, 1990, 37(10): 996-1001.
40.	Shannon RV. A model of safe levels for electrical stimulation. IEEE Trans Biomed Eng, 1992, 39(4): 424-426.
41.	Cogan SF, Ludwig KA, Welle CG, et al. Tissue damage thresholds during therapeutic electrical stimulation. J Neural Eng, 2016, 13(2): 021001.
42.	Gordon B, Lesser RP, Rance NE, et al. Parameters for direct cortical electrical stimulation in the human: histopathologic confirmation. Electroencephalogr Clin Neurophysiol, 1990, 75(5): 371-377.
43.	Taussig D, Lebas A, Chipaux M, et al. Stereo-electroencephalography (SEEG) in children surgically cured of their epilepsy. Neurophysiol Clin, 2016, 46(1): 3-15.
44.	Kovac S, Vakharia VN, Scott C, et al. Invasive epilepsy surgery evaluation. Seizure, 2017, 44: 125-136.
45.	Ley M, Peláez N, Principe A, et al. Validation of direct cortical stimulation in presurgical evaluation of epilepsy. Clin Neurophysiol, 2022, 137: 38-45.
46.	Mazzola L, Mauguière F, Isnard J. Functional mapping of the human insula: data from electrical stimulations. Rev Neurol (Paris), 2019, 175(3): 150-156.

1. Samanta D. Recent developments in stereo electroencephalography monitoring for epilepsy surgery. Epilepsy Behav, 2022, 135: 108914.
2. 中国抗癫痫协会立体定向脑电图与脑定位学专业委员会, 中国医师协会神经外科医师分会, 国家神经外科机器人示范项目专家指导委员会. 立体定向脑电图临床应用的中国专家共识. 中华医学杂志, 2022, 102(39): 3095-3102.
3. Britton JW. Electrical stimulation mapping with stereo-EEG electrodes. J Clin Neurophysiol, 2018, 35(2): 110-114.
4. George DD, Ojemann SG, Drees C, et al. Stimulation mapping using stereoelectroencephalography: current and future directions. Front Neurol, 2020, 11: 320.
5. Suller Marti A, Mirsattari SM, Steven DA, et al. Extraoperative electrical stimulation mapping in epilepsy presurgical evaluation: a proposal and review of the literature. Clin Neurol Neurosurg, 2022, 214: 107170.
6. Blank LJ, Jette N. Epilepsy research in 2022: clinical advances. Lancet Neurol, 2023, 22(1): 15-17.
7. Asadi-Pooya AA, Brigo F, Trinka E, et al. Physicians’ beliefs about brain surgery for drug-resistant epilepsy: a global survey. Seizure, 2022, 103: 18-22.
8. Rheims S, Sperling MR, Ryvlin P. Drug-resistant epilepsy and mortality-why and when do neuromodulation and epilepsy surgery reduce overall mortality. Epilepsia, 2022, 63(12): 3020-3036.
9. 谭启富, 李玲, 吴承远. 癫痫外科学. 2 版. 北京: 人民卫生出版社, 2012: 9-29.
10. Iwasaki M, Iijima K, Takayama Y, et al. Predictors of seizure outcome after repeat pediatric epilepsy surgery: reasons for failure, sex, electrophysiology, and temporal lobe surgery. Neurol Med Chir (Tokyo), 2022, 62(3): 125-132.
11. Klodowski DA, George BJ, Sperling MR. Seizure latency and epilepsy localization as predictors of recurrence following epilepsy surgery. Epilepsia, 2022, 63(5): 1074-1080.
12. Paulo DL, Ball TJ, Englot DJ. Emerging technologies for epilepsy surgery. Neurol Clin, 2022, 40(4): 849-867.
13. Alim-Marvasti A, Vakharia VN, Duncan JS. Multimodal prognostic features of seizure freedom in epilepsy surgery. J Neurol Neurosurg Psychiatry, 2022, 93(5): 499-508.
14. Gonzalez-Martinez JA. The stereo-electroencephalography: the epileptogenic zone. J Clin Neurophysiol, 2016, 33(6): 522-529.
15. Mallela AN, Beiriger J, Gersey ZC, et al. Targeting the future: developing a training curriculum for robotic assisted neurosurgery. World Neurosurg, 2022, 167: e770-e777.
16. Miller KJ, Fine AL. Decision-making in stereotactic epilepsy surgery. Epilepsia, 2022, 63(11): 2782-2801.
17. Zhang D, Cui X, Zheng J, et al. Neurosurgical robot-assistant stereoelectroencephalography system: operability and accuracy. Brain Behav, 2021, 11(10): e2347.
18. Talairach J, Bancaud J, Geier S, et al. The cingulate gyrus and human behaviour. Electroencephalogr Clin Neurophysiol, 1973, 34(1): 45-52.
19. Abou-Al-Shaar H, Brock AA, Kundu B, et al. Increased nationwide use of stereoencephalography for intracranial epilepsy electroencephalography recordings. J Clin Neurosci, 2018, 53: 132-134.
20. Mullin JP, Shriver M, Alomar S, et al. Is SEEG safe? A systematic review and meta-analysis of stereo-electroencephalography-related complications. Epilepsia, 2016, 57(3): 386-401.
21. Bartholow R. Experiments on the functions of the human brain. BMJ, 1874, 1(700): 727.
22. Drane DL, Pedersen NP, Sabsevitz DS, et al. Cognitive and emotional mapping with SEEG. Front Neurol, 2021, 12: 627981.
23. McGonigal A, Lagarde S, Trébuchon-Dafonseca A, et al. Early onset motor semiology in seizures triggered by cortical stimulation during SEEG. Epilepsy Behav, 2018, 88: 262-267.
24. Cardinale F, Rizzi M, Vignati E, et al. Stereoelectroencephalography: retrospective analysis of 742 procedures in a single centre. Brain, 2019, 142(9): 2688-2704.
25. Baruah S, Olivier A, Hall JA. The changing nature of epilepsy surgery: a retrospective review of practice profiles. Can J Neurol Sci, 2022, 49(3): 387-392.
26. Trebuchon A, Racila R, Cardinale F, et al. Electrical stimulation for seizure induction during SEEG exploration: a useful predictor of postoperative seizure recurrence?. J Neurol Neurosurg Psychiatry, 2020, 28: jnnp-2019-322469.
27. Chassoux F, Devaux B, Landré E, et al. Stereoelectroencephalography in focal cortical dysplasia: a 3D approach to delineating the dysplastic cortex. Brain, 2000, 123(8): 1733-1751.
28. Kahane P, Ryvlin P, Hoffmann D, et al. From hypothalamic hamartoma to cortex: what can be learnt from depth recordings and stimulation?. Epileptic Disord, 2003, 5(4): 205-217.
29. Trébuchon A, Chauvel P. Electrical stimulation for seizure induction and functional mapping in stereoelectroencephalography. J Clin Neurophysiol, 2016, 33(6): 511-521.
30. Cuello Oderiz C, von Ellenrieder N, Dubeau F, et al. Association of cortical stimulation-induced seizure with surgical outcome in patients with focal drug-resistant epilepsy. JAMA Neurol, 2019, 76(9): 1070-1078.
31. Whitaker HA, Ojemann GA. Graded localisation of naming from electrical stimulation mapping of left cerebral cortex. Nature, 1977, 270(5632): 50-51.
32. Isnard J, Taussig D, Bartolomei F, et al. French guidelines on stereoelectroencephalography (SEEG). Neurophysiol Clin, 2018, 48(1): 5-13.
33. Hamberger MJ. Cortical language mapping in epilepsy: a critical review. Neuropsychol Rev, 2007, 17(4): 477-489.
34. Matsumoto R, Nair DR, LaPresto E, et al. Functional connectivity in the human language system: a cortico-cortical evoked potential study. Brain, 2004, 127(10): 2316-2330.
35. Perrone-Bertolotti M, Alexandre S, Jobb AS, et al. Probabilistic mapping of language networks from high frequency activity induced by direct electrical stimulation. Hum Brain Mapp, 2020, 41(14): 4113-4126.
36. Thorsteinsdottir J, Vollmar C, Tonn JC, et al. Outcome after individualized stereoelectroencephalography (sEEG) implantation and navigated resection in patients with lesional and non-lesional focal epilepsy. J Neurol, 2019, 266(4): 910-920.
37. Youngerman BE, Khan FA, McKhann GM. Stereoelectroencephalography in epilepsy, cognitive neurophysiology, and psychiatric disease: safety, efficacy, and place in therapy. Neuropsychiatr Dis Treat, 2019, 15: 1701-1716.
38. Nowak LG, Bullier J. Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter. II. Evidence from selective inactivation of cell bodies and axon initial segments. Exp Brain Res, 1998, 118(4): 489-500.
39. McCreery DB, Agnew WF, Yuen TG, et al. Charge density and charge per phase as cofactors in neural injury induced by electrical stimulation. IEEE Trans Biomed Eng, 1990, 37(10): 996-1001.
40. Shannon RV. A model of safe levels for electrical stimulation. IEEE Trans Biomed Eng, 1992, 39(4): 424-426.
41. Cogan SF, Ludwig KA, Welle CG, et al. Tissue damage thresholds during therapeutic electrical stimulation. J Neural Eng, 2016, 13(2): 021001.
42. Gordon B, Lesser RP, Rance NE, et al. Parameters for direct cortical electrical stimulation in the human: histopathologic confirmation. Electroencephalogr Clin Neurophysiol, 1990, 75(5): 371-377.
43. Taussig D, Lebas A, Chipaux M, et al. Stereo-electroencephalography (SEEG) in children surgically cured of their epilepsy. Neurophysiol Clin, 2016, 46(1): 3-15.
44. Kovac S, Vakharia VN, Scott C, et al. Invasive epilepsy surgery evaluation. Seizure, 2017, 44: 125-136.
45. Ley M, Peláez N, Principe A, et al. Validation of direct cortical stimulation in presurgical evaluation of epilepsy. Clin Neurophysiol, 2022, 137: 38-45.
46. Mazzola L, Mauguière F, Isnard J. Functional mapping of the human insula: data from electrical stimulations. Rev Neurol (Paris), 2019, 175(3): 150-156.

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