Possibilities for surgical treatment of the pharmacoresistant form of epilepsy using robot-assisted implantation of deep electrodes for invasive stereoelectroencephalography

The study objective is to determine the effectiveness, safety and information content of robot-assisted implantation of deep electrodes for invasive stereoelectroencephalography (stereo-EEG) monitoring in patients with pharmacoresistant epilepsy.

Materials and methods. The study group included 27 patients from 2016 and 2018, who underwent a robot-assisted implantation of stereo-EEG electrodes followed by a 24-hour video-EEG monitoring. Unilateral implantation of electrodes was performed in 22 patients, bilateral – in 6 patients (in 1 patient, due to the ineffectiveness of the operation to remove the epileptogenic focus, implantation was performed twice). MRI-negative epilepsy was in 16 (59 %) patients; 11 (41 %) patients with multiple structural changes. The average time for invasive video-EEG monitoring was 96 hours (from 46 to 253 hours).

Results. Based on the information obtained during invasive monitoring, the epileptogenic zones and early distribution were verified: in the temporal lobe in 9 (33 %) patients, in the frontal lobe – 6 (22 %), in the parietal lobe – 2 (8 %), in the occipital lobe – 3 (11 %), in more than 2 lobes – 4 (15 %), in both hemispheres – 3 (11 %) patients. Nineteen (70.4 %) patients underwent surgery to remove the epileptogenic zone. In 11 (58 %) patients extratemporal resection was performed and 8 (42 %) patients underwent anterior-medial temporal and amygdal-hippocampectomy. Follow-up history of more than 6 months after removal of the epileptogenic zone detected by stereo-EEG was monitored in 13 patients. The outcomes of surgical resection were as follows: in 8 (61 %) patients – Engel I, in 1 (8 %) – Engel II, in 3 (23 %) – Engel III, in 1 (8 %) – Engel IV.

Conclusion. Robot-assisted implantation of deep electrodes for invasive stereo-EEG monitoring is a safe and effective diagnostic method in patients with pharmacoresistant epilepsy. In patients with MRI-negative epilepsy, stereo-EEG allows to localize and determine the boundaries of the epileptogenic zone, thereby increasing the effectiveness and safety of surgical resection.

1. Beretta S., Carone D., Zanchi C. et al. Long-term applicability of the new ILAE definition of epilepsy. Results from the PRO-LONG study. Epilepsia 2017;58(9):1518–23. DOI: 10.1111/epi.13854.

2. West S., Nolan S.J., Cotton J. et al. Surgery for epilepsy. Cochrane Database Syst Rev 2015;(7):CD010541. DOI: 10.1002/14651858.CD010541.pub2.

3. Rosenow F., Lüders H. Presurgical evaluation of epilepsy. Brain 2001; 124(Pt 9):1683–700. DOI: 10.1093/brain/124.9.1683.

4. Talairach J., Bancaud J. Lesion, “irritative” zone and epileptogenic focus. Confin Neurol 1966;27(1):91–4. DOI: 10.1159/000103937.

5. González-Martínez J., Najm I.M. Indications and selection criteria for invasive monitoring in children with cortical dysplasia. Childs Nerv Syst 2014;30(11):1823–9. DOI: 10.1007/s00381-014-2497-1.

6. Bancaud J., Dell M.B. [Technics and method of stereotaxic functional exploration of the brain structures in man (cortex, subcortex, central gray nuclei) (In French)]. Rev Neurol (Paris) 1959;101:213–27.

7. Bancaud J., Talairach J. [Methodology of stereo EEG exploration and surgical intervention in epilepsy (In French)]. Rev Otoneuroophtalmol 1973;45(4):315–28.

8. Engel J. Jr, Henry T.R., Risinger M.W. et al. Presurgical evaluation for partial epilepsy: relative contributions of chronic depth-electrode recordings versus FDG-PET and scalp-sphenoidal ictal EEG. Neurology 1990;40(11):1670–7. DOI: 10.1212/wnl.40.11.1670.

9. Cabrini G.P., Ettorre G., Marossero F. et al. Surgery of epilepsy: some indications for SEEG. J Neurosurg Sci 1975; 19(1–2):95–104.

10. Kwoh Y.S., Hou J., Jonckheere E.A., Hayati S. A robot with improved absolute positioning accuracy for CT guided stereotactic brain surgery. IEEE Trans Biomedical Eng 1988;35(2):153–60. DOI: 10.1109/10.1354.

11. Goto T., Hongo K., Kakizawa Y. et al. Clinical application of robotic telemanipulation system in neurosurgery. Case report. J Neurosurg 2003;99(6):1082–4. DOI: 10.3171/jns.2003.99.6.1082.

12. Benabid A.L., Hoffmann D., Seigneuret E., Chabardes S. Robotics in neurosurgery: which tools for what? Acta Neurochir Suppl 2006;98:43–50. DOI: 10.1007/978-3-211-33303-7_7.

13. Spire W.J., Jobst B.C., Thadani V.M. et al. Robotic image-guided depth electrode implantation in the evaluation of medically intractable epilepsy. Neurosurg Focus 2008;25(3):E19. DOI: 10.3171/FOC/2008/25/9/E19.

14. Sutherland G.R., Maddahi Y., Gan L.S. et al. Robotics in the neurosurgical treatment of glioma. Surg Neurol Int 2015;6(Suppl 1):S1–8. DOI: 10.4103/2152-7806.151321.

15. Nagahama Y., Schmitt A.J., Nakagawa D. et al. Intracranial EEG for seizure focus localization: evolving techniques, outcomes, complications, and utility of combining surface and depth electrodes. J Neurosurg 2018 May 25:1–13. DOI: 10.3171/2018.1.JNS171808.

16. McGovern R.A., Ruggieri P., Bulacio J. et al. Risk analysis of hemorrhage in stereo-electroencephalography procedures. Epilepsia 2019;60(3):571–80. DOI: 10.1111/epi.14668.

17. González-Martínez J., Bulacio J., Thompson S. et al. Technique, results, and complications related to robot-assisted stereoelectroencephalography. Neurosurgery 2016;78(2):169–80. DOI: 10.1227/NEU.0000000000001034.

18. González-Martínez J., Bulacio J., Alexopoulos A. et al. Stereoelectro-encephalography in the “difficult to localize” refractory focal epilepsy: early experience from a North American epilepsy center. Epilepsia 2013;54(2):323–30. DOI: 10.1111/j.1528-1167.2012.03672.x.

19. Eljamel M.S. Robotic application in epilepsy surgery. Int J Med Robot 2006;2(3):233–7. DOI: 10.1002/rcs.97.

20. Eljamel M.S. Validation of the PathFinder neurosurgical robot using a phantom. Int J Med Robot 2007;3(4):372–7. DOI: 10.1002/rcs.153.

21. Eljamel M.S. Robotic neurological surgery applications: accuracy and consistency or pure fantasy? Stereotact Funct Neurosurg 2009;87(2):88–93. DOI: 10.1159/000202974.

22. Vadera S., Mullin J., Bulacio J. et al. Stereoelectroencephalography following subdural grid placement for difficult to localize epilepsy. Neurosurgery 2013;72(5):723–9. DOI: 10.1227/NEU.0b013e318285b4ae.

23. Serletis D., Bulacio J., Bingaman W. et al. The stereotactic approach for mapping epileptic networks: a prospective study of 200 patients. J Neurosurg 2014;121(5): 1239–46. DOI: 10.3171/2014.7.JNS132306.

24. González-Martínez J., Mullin J., Bulacio J. et al. Stereoelectroencephalography in children and adolescents with difficult-to-localize refractory focal epilepsy. Neurosurgery 2014;75(3):258–68. DOI: 10.1227/NEU.0000000000000453.

25. Wyllie E., Lüders H., Morris H.H. 3 rd et al. Subdural electrodes in the evaluation for epilepsy surgery in children and adults. Neuropediatrics 1988;19(2):80–6. DOI: 10.1055/s-2008-1052406.

26. Bulacio J.C., Jehi L., Wong C. et al. Long-term seizure outcome after resective surgery in patients evaluated with intracranial electrodes. Epilepsia 2012;53(10):1722–30. DOI: 10.1111/j.1528-1167.2012.03633.x.

27. Jeha L.E., Najm I., Bingaman W. et al. Surgical outcome and prognostic factors of frontal lobe epilepsy surgery. Brain 2007;130(Pt 2):574–84. DOI: 10.1093/brain/awl364.

28. McGonigal A., Gavaret M., Da Fonseca A.T. et al. MRI-negative prefrontal epilepsy due to cortical dysplasia explored by stereoelectroencephalography (SEEG). Epileptic Disord 2008;10(4):330–8. DOI: 10.1684/epd.2008.0218.

29. Cardinale F., Cossu M., Castana L. et al. Stereoelectroencephalography: surgical methodology, safety, and stereotactic application accuracy in 500 procedures. Neurosurgery 2013;72(3):353–66. DOI: 10.1227/NEU.0b013e31827d1161.

30. Cossu M., Cardinale F., Colombo N. et al. Stereoelectroencephalography in the presurgical evaluation of children with drugresistant focal epilepsy. J Neurosurg 2005;103(4 Suppl):333–43. DOI: 10.3171/ped.2005.103.4.0333.

31. Quitadamo L.R., Mai R., Gozzo F. et al. Kurtosis-based detection of intracranial high-frequency oscillations for the identification of the seizure onset zone. Int J Neural Syst 2018;28(7):1850001. DOI: 10.1142/S0129065718500016.

32. Britton J.W. Electrical stimulation mapping with stereo-EEG electrodes. J Clin Neurophysiol 2018;35(2):110–4. DOI: 10.1097/WNP.0000000000000443.

33. Guenot M., Isnard J. [Multiple SEEG-guided RF-thermolesions of epileptogenic foci (In French)]. Neurochirurgie 2008;54(3):441–7. DOI: 10.1016/j.neuchi.2008.02.012.

34. Cossu M., Fuschillo D., Cardinale F. et al. Stereo-EEG-guided radio-frequency thermocoagulations of epileptogenic greymatter nodular heterotopy. J Neurol Neurosurg Psychiatry 2014;85(6):611–7. DOI: 10.1136/jnnp-2013-305514.

35. González-Martínez J., Vadera S., Mullin J. et al. Robot-assisted stereotactic laser ablation in medically intractable epilepsy. Neurosurgery 2014; 10 Suppl 2:167–72. DOI: 10.1227/NEU.0000000000000286.