Stereotactic Radiosurgery in the Complex Treatment of Patients With Epilepsy Associated With Various Structural Brain Lesions
https://doi.org/10.23934/2223-9022-2021-10-1-73-82
Abstract
BACKGROUND Structural damage to the brain substance in adults is one of the most common causes of epilepsy. Currently, such patients are prescribed drug therapy and/or surgery. With this approach, epileptic symptoms can persist in a significant proportion of patients (up to 30%, depending on the disease).
AIM OF STUDY To clarify the efficacy of stereotactic radiosurgery (STS) as part of the complex treatment of patients suffering from pharmacoresistant symptomatic epilepsy with hippocampal sclerosis, vascular malformations, and some benign tumors of the brain and its membranes.
MATERIAl AND METHODS Examination and radiosurgical treatment were carried out in 45 patients with various brain diseases accompanied by symptomatic epilepsy, provided that the previous conservative or surgical treatment was insufficiently effective. During the observation period, the frequency of seizures was assessed and the presence and nature of postoperative complications were recorded.
RESUlTS With a median follow-up of 30 months, good outcomes (class I–II according to J. Engel’s scale) were observed in 5 out of 8 patients with hippocampal sclerosis who underwent STS after amygdaloghippocamplobectomy; seizure frequency decreased in all patients. Complications of STS were noted in 2 patients and had a transient nature. In the group of patients with meningiomas, in 4 out of 8 patients, seizures completely stopped, in 3 patients the frequency of seizures decreased by more than 90%, in another 1 the frequency of seizures decreased by 60%. There were no complications of STS during the observation period. In
intracerebral tumors (diffuse astrocytoma), Engel Ia outcome was observed in both patients. In the group of patients with cavernous angiomas, there were good outcomes (class I–II according to J. Engel’s scale) in 17 patients (85%). Deterioration (Engel IVc outcome) was observed in 1 patient (5%), 2 patients (10%) had complications of STS. In the group of patients with arteriovenous malformations, good outcomes (classes I–II according to J. Engel’s scale) were found in all 7 patients. The complication after STS was revealed in 1 patient.
CONClUSION The presented results confirm the high efficiency and low risk of side effects when using stereotactic radiosurgery in the complex treatment of patients with epilepsy associated with common structural brain lesions.
About the Authors
V. V. KrylovRussian Federation
Doctor of Medical Sciences, Member of the Russian Academy of Sciences, Doctor of Medicine
20, bldg. 1 Delegatskaya St., Moscow, 127473, Russian Federation
V. A. Rak
Russian Federation
Neurosurgeon
3 B. Sukharevskaya Sq., Moscow, 129090, Russian Federation
A. S. Tokarev
Russian Federation
Candidate of Medical Sciences, Researcher, Department of Emergency Neurosurgery
3 B. Sukharevskaya Sq., Moscow, 129090, Russian Federation
M. V. Sinkin
Russian Federation
Candidate of Medical Sciences, Senior Researcher, Department of Emergency Neurosurgery
20, bldg. 1 Delegatskaya St., Moscow, 127473, Russian Federation
3 B. Sukharevskaya Sq., Moscow, 129090, Russian Federation
I. S. Trifonov
Russian Federation
Candidate of Medical Sciences, Neurosurgeon
20, bldg. 1 Delegatskaya St., Moscow, 127473, Russian Federation
O. L. Yevdokimova
Russian Federation
Head of the Radiosurgery Center
3 B. Sukharevskaya Sq., Moscow, 129090, Russian Federation
V. N. Stepanov
Russian Federation
Radiologist
3 B. Sukharevskaya Sq., Moscow, 129090, Russian Federation
E. N. Rozhnova
Russian Federation
Neurologist at the Center for Radiosurgery
3 B. Sukharevskaya Sq., Moscow, 129090, Russian Federation
G. V. Koinash
Russian Federation
Medical Physicist, Radiosurgery Center
3 B. Sukharevskaya Sq., Moscow, 129090, Russian Federation
References
1. Thijs RD, Surges R, O’Brien TJ, Sander JW. Epilepsy in adults. Lancet. 2019;393(10172):689–701. PMID: 30686584 https://doi.org/10.1016/S0140-6736(18)32596-0
2. Golanov AV, Kostyuchenko VV (eds.) Neyroradiokhirurgiya na gamma-nozhe. Moscow: T. A. Alekseeva Publ.; 2018. (in Russ.)
3. Sutcliffe JC, Forster DM, Walton L, Dias PS, Kemeny AA. Untoward clinical effects after stereotactic radiosurgery for intracranial arteriovenous malformations. Br J Neurosurg. 1992;6(3):177–185. PMID: 1632916 https://doi.org/10.3109/02688699209002925
4. Kondziolka D, Shin SM, Brunswick A, Kim I, Silverman JS. The biology of radiosurgery and its clinical applications for brain tumors. Neuro Oncol. 2015;17(1):29–44. PMID: 25267803 https://doi.org/10.1093/neuonc/nou284
5. Gewirtz RJ, Steinberg GK, Crowley R, Levy RP. Pathological changes in surgically resected angiographically occult vascular malformations after radiation. Neurosurgery. 1998;42(4):738–742; discussion 742–743. PMID: 9574637 https://doi.org/10.1097/00006123-199804000-00031
6. Awad IA, Polster SP. Cavernous angiomas: deconstructing a neurosurgical disease. J Neurosurg. 2019;131(1):1–13. PMID: 31261134 https://doi.org/10.3171/2019.3.JNS181724
7. Szeifert GT, Kemeny AA, Timperley WR, Forster DM. The potential role of myofibroblasts in the obliteration of arteriovenous malformations after radiosurgery. Neurosurgery. 1997;40(1):61–65; discussion 65–66. PMID: 8971825 https://doi.org/10.1097/00006123-199701000-00013
8. Lunsford LD, Niranjan A, Kano H, Monaco Iii EA, Flickinger JC. Leksell Stereotactic Radiosurgery for Cavernous Malformations. Prog Neurol Surg. 2019;34:260–266. PMID: 31096254 https://doi.org/10.1159/000493072
9. McGonigal A, Sahgal A, de Salles A, Hayashi M, Levivier M, Ma L, et al. Radiosurgery for epilepsy: Systematic review and International Stereotactic Radiosurgery Society (ISRS) practice guideline. Epilepsy Res. 2017;137:123–131. PMID: 28939289 https://doi.org/10.1016/j.eplepsyres.2017.08.016
10. Pallud J, McKhann GM. Diffuse Low-Grade Glioma-Related Epilepsy. Neurosurg Clin North Am. 2019;30(1):43–54. PMID: 30470404 https://doi.org/10.1016/j.nec.2018.09.001
11. Manford M. Recent advances in epilepsy. J Neurol. 2017;264(8):1811–1824. PMID: 28120042 https://doi.org/10.1007/s00415-017-8394-2
12. Soldozy S, Norat P, Yağmurlu K, Sokolowski JD, Sharifi KA, Tvrdik P, et al. Arteriovenous malformation presenting with epilepsy: a multimodal approach to diagnosis and treatment. Neurosurg Focus. 2020;48(4):E17. PMID: 32234990 https://doi.org/10.3171/2020.1.FOCUS19899
13. Tanti MJ, Marson AG, Chavredakis E, Jenkinson MD. The impact of epilepsy on the quality of life of patients with meningioma: A systematic review. Br J Neurosurg. 2016;30(1):23–28. PMID: 26982950 https://doi.org/10.3109/02688697.2015.1080215
14. Krylov VV, Gekht AB, Trifonov IS, Lebedeva AV, Kiymovskiy IL, Sinkin MV, et al. Surgical Treatment of Patients With Magnetic Resonance-Negative Drug-Resistant Forms of Epilepsy. Neurological Journal. 2016;21(4):213–218. https://doi.org/10.18821/1560-9545-2016-21-4-213-218
15. Scheffer IE, Berkovic S, Capovilla G, Connolly MB, French J, Guilhoto L, et al. ILAE classification of the epilepsies: Position paper of the ILAE Commission for Classification and Terminology. Epilepsia. 2017;58(4):512–521. PMID: 28276062 https://doi.org/10.1111/epi.13709
16. Pollock BE, Stafford SL, Link MJ, Garces YI, Foote RL. Single-fraction Radiosurgery for Presumed Intracranial Meningiomas: Efficacy and Complications From a 22-Year Experience. Int J Radiat Oncol Biol Phys. 2012;83(5):1414–1418. PMID: https://doi.org/10.1016/j.ijrobp.2011.10.033
17. Kondziolka D, Mathieu D, Lunsford LD, Martin JJ, Madhok R, Niranjan A, et al. Radiosurgery as definitive management of intracranial meningiomas. Neurosurgery. 2008;62(1):53–60. PMID: 18300891 https://doi.org/10.1227/01.NEU.0000311061.72626.0D
18. Akers A, Al-Shahi Salman R, I A Awad, Dahlem K, Flemming K, Hart B, et al. Synopsis of Guidelines for the Clinical Management of Cerebral Cavernous Malformations: Consensus Recommendations Based on Systematic Literature Review by the Angioma Alliance Scientific Advisory Board Clinical Experts Panel. Neurosurgery. 2017;80(5):665–680. PMID: 28387823 https://doi.org/10.1093/neuros/nyx091
19. Engel JJr, Van Ness PC, Rasmussen TB, Ojemann LM. Outcome with respect to epileptic seizures. In: Surgical Treatment of the Epilepsies. New York: Raven Press; 1993. pp. 609–621.
20. Thom M. Review: Hippocampal sclerosis in epilepsy: a neuropathology review. Neuropathol Appl Neurobiol. 2014;40(5):520–543. PMID: 24762203 https://doi.org/10.1111/nan.12150
21. Kitaura H, Shirozu H, Masuda H, Fukuda M, Fujii Y, Kakita A. Pathophysiological Characteristics Associated with Epileptogenesis in Human Hippocampal Sclerosis. EBioMedicine. 2018;29:38–46. PMID: 29478873 https://doi.org/10.1016/j.ebiom.2018.02.013
22. Aoki Y, Hanai S, Sukigara S, Otsuki T, Saito T, Nakagawa E, et al. Altered Expression of Astrocyte-Related Receptors and Channels Correlates with Epileptogenesis in Hippocampal Sclerosis. Pediatr Dev Pathol. 2019;22(6):532–539. PMID: 31166880 https://doi.org/10.1177/1093526619855488
23. Barbaro NM, Quigg M, Ward MM, Chang EF, Broshek DK, Langfitt JT, et al. Radiosurgery versus open surgery for mesial temporal lobe epilepsy: The randomized, controlled ROSE trial. Epilepsia. 2018;59(6):1198–1207. PMID: 29600809 https://doi.org/10.1111/epi.14045
24. Quigg M, Harden C. Minimally invasive techniques for epilepsy surgery: stereotactic radiosurgery and other technologies. J Neurosurg. 2014;121 Suppl:232–240. PMID: 25434958 https://doi.org/10.3171/2014.8.GKS141608
25. Krylov VV. (ed.) Khirurgiya epilepsii. Moscow: ABV-press Publ.; 2019. (in Russ.)
26. Krylov VV, Gekht AB, Trifonov IS, Lebedeva AV, Kaimovskii IL, Sinkin MV, et al. The surgical treatment outcomes in patients suffered from various types of pharmacoresistent epilepsy. Russian Journal of Neurosurgery. 2017;(1):15–22. (In Russ.)
27. Reed CM, Dewar S, Fried I, Engel J, Eliashiv D. Failed epilepsy surgery deserves a second chance. Clin Neurol Neurosurg. 2017;163:110–115. PMID: 29096138 https://doi.org/10.1016/j.clineuro.2017.10.023
28. Yardi R, Morita-Sherman ME, Fitzgerald Z, Punia V, Bena J, Morrison S, et al. Long-term outcomes of reoperations in epilepsy surgery. Epilepsia. 2020;61(3):465–478. PMID: 32108946 https://doi.org/10.1111/epi.16452
29. Lee EM, Kang JK, Kim SJ, Hong SH, Ko TS, Lee SA, et al. Gamma Knife radiosurgery for recurrent or residual seizures after anterior temporal lobectomy in mesial temporal lobe epilepsy patients with hippocampal sclerosis: long-term follow-up results of more than 4 years. J Neurosurg. 2015;123(6):1375–1382. PMID: 26162046 https://doi.org/10.3171/2014.12.JNS141280
30. Whittle IR, Smith C, Navoo P, Collie D. Meningiomas. Lancet. 2004;363(9420):1535–1543. PMID: 15135603 https://doi.org/10.1016/S0140-6736(04)16153-9
31. Lieu AS, Howng SL. Intracranial meningiomas and epilepsy: incidence, prognosis and influencing factors. Epilepsy Res. 1999;38(1):45–52. PMID: 10604605 https://doi.org/10.1016/s0920-1211(99)00066-2
32. Di Franco R, Borzillo V, Ravo V, Falivene S, Romano FJ, Muto M, et al. Radiosurgery and stereotactic radiotherapy with cyberknife system for meningioma treatment. Neuroradiol J. 2018;31(1):18–26. PMID: 29206077 https://doi.org/10.1177/1971400917744885
33. El-Khatib M, El Majdoub F, Hunsche S, Hoevels M, Kocher M, Sturm V, et al. Stereotactic LINAC radiosurgery for the treatment of typical intracranial meningiomas. Efficacy and safety after a follow-up of over 12 years. Strahlenther Onkol. 2015;191(12):921–927. PMID: 26253788 https://doi.org/10.1007/s00066-015-0880-9
34. Berntsson SG, Merrell RT, Amirian ES, Armstrong GN, Lachance D, Smits A, et al. Glioma-related seizures in relation to histopathological subtypes: a report from the glioma international case-control study. J Neurol. 2018;265(6):1432–1442. PMID: 29687214 https://doi.org/10.1007/s00415-018-8857-0
35. Chang EF, Potts MB, Keles GE, Lamborn KR, Chang SM, Barbaro NM, et al. Seizure characteristics and control following resection in 332 patients with low-grade gliomas. J Neurosurg. 2008;108(2):227–235. PMID: 18240916 https://doi.org/10.3171/JNS/2008/108/2/0227
36. Wang LW, Shiau CY, Chung WY, Wu HM, Guo WY, Liu KD, et al. Gamma Knife surgery for low-grade astrocytomas: evaluation of long-term outcome based on a 10-year experience. J Neurosurg. 2006;105 Suppl:127–132. PMID: 18503345 https://doi.org/10.3171/sup.2006.105.7.127
37. Henderson MA, Fakiris AJ, Timmerman RD, Worth RM, Lo SS, Witt TC. Gamma knife stereotactic radiosurgery for low-grade astrocytomas. Stereotact Funct Neurosurg. 2009;87(3):161–167. PMID: 19321969 https://doi.org/10.1159/000209297
38. Park KJ, Kano H, Kondziolka D, Niranjan A, Flickinger JC, Lunsford LD. Early or delayed radiosurgery for WHO grade II astrocytomas. J Neurooncol. 2011;103(3):523–532. PMID: 20848299 https://doi.org/10.1007/s11060-010-0409-0
39. Ryken TC, Parney I, Buatti J, Kalkanis SN, Olson JJ. The role of radiotherapy in the management of patients with diffuse low grade glioma: A systematic review and evidence-based clinical practice guideline. J Neurooncol. 2015;125(3):551–583. PMID: 26530266 https://doi.org/10.1007/s11060-015-1948-1
40. Ding D, Starke RM, Sheehan JP. Radiosurgery for the management of cerebral arteriovenous malformations. Handb Clin Neurol. 2017;143:69–83. PMID: 28552160 https://doi.org/10.1016/B978-0-444-63640-9.00007-2
41. Schramm J. Seizures associated with cerebral arteriovenous malformations. Handb Clin Neurol. 2017;143:31–40. PMID: 28552156 https://doi.org/10.1016/B978-0-444-63640-9.00004-7
42. Cox EM, Bambakidis NC, Cohen ML. Pathology of cavernous malformations. Handb Clin Neurol. 2017;143:267–277. PMID: 28552149 https://doi.org/10.1016/B978-0-444-63640-9.00025-4
43. Kondziolka D, Monaco EA, Lunsford LD. Cavernous malformations and hemorrhage risk. Prog Neurol Surg. 2013;27:141–146. PMID: 23258518 https://doi.org/10.1159/000341774
44. Przybylowski CJ, Ding D, Starke RM, Yen CP, Quigg M, Dodson B, et al. Seizure and anticonvulsant outcomes following stereotactic radiosurgery for intracranial arteriovenous malformations. J Neurosurg. 2015;122(6):1299–1305. PMID: 25614948 https://doi.org/10.3171/2014.11.JNS141388
45. Hasegawa H, Yamamoto M, Shin M, Barfod BE. Gamma Knife Radiosurgery for Brain Vascular Malformations: Current Evidence and Future Tasks. Ther Clin Risk Manag. 2019;15:1351–1367. PMID: 31819462 https://doi.org/10.2147/TCRM.S200813
46. Josephson CB, Sauro K, Wiebe S, Clement F, Jette N. Medical vs invasive therapy in AVM-related epilepsy: Systematic review and meta-analysis. Neurology. 2016;86(1):64–71. PMID: 26643547 https://doi.org/10.1212/WNL.0000000000002240
47. Poorthuis MHF, Rinkel LA, Lammy S, Al-Shahi Salman R. Stereotactic radiosurgery for cerebral cavernous malformations: A systematic review. Neurology. 2019;93(21):e1971–e1979. PMID: 31659093 https://doi.org/10.1212/WNL.0000000000008521
48. Nagy G, Stokes SS, Erőss LG, Bhattacharyya D, Yianni J, Rowe JG, et al. Contemporary radiosurgery of cerebral cavernous malformations: Part 2. Treatment outcome for hemispheric lesions. J Neurosurg. 2018 Jul 1:1–9. Online ahead of print. PMID: 30052157 https://doi.org/10.3171/2018.2.JNS171267
49. Wang P, Zhang F, Zhang H, Zhao H. Gamma knife radiosurgery for intracranial cavernous malformations. Clin Neurol Neurosurg. 2010;112(6):474–477. PMID: 20371149 https://doi.org/10.1016/j.clineuro.2010.03.012
50. Ding D, Quigg M, Starke RM, Xu Z, Yen CP, Przybylowski CJ, et al. Radiosurgery for temporal lobe arteriovenous malformations: effect of temporal location on seizure outcomes. J Neurosurg. 2015;123(4):924–934. PMID: 25884262 https://doi.org/10.3171/2014.10.JNS141807
51. Baranoski JF, Grant RA, Hirsch LJ, Visintainer P, Gerrard JL, Günel M, et al. Seizure control for intracranial arteriovenous malformations is directly related to treatment modality: a meta-analysis. J Neurointervent Surg. 2014;6(9):684–690. PMID: 24319021 https://doi.org/10.1136/neurintsurg-2013-010945
52. Kim W, Stramotas S, Choy W, Dye J, Nagasawa D, Yang I. Prognostic factors for post-operative seizure outcomes after cavernous malformation treatment. J Clin Neurosci. 2011;18(7):877–880. PMID: 21561775 https://doi.org/10.1016/j.jocn.2010.12.008
53. Ding D, Quigg M, Starke RM, Yen CP, Przybylowski CJ, Dodson BK, et al. Cerebral Arteriovenous Malformations and Epilepsy, Part 2: Predictors of Seizure Outcomes Following Radiosurgery. World Neurosurg. 2015;84(3):653–662. PMID: 26026628 https://doi.org/10.1016/j.wneu.2015.04.064
Review
For citations:
Krylov V.V., Rak V.A., Tokarev A.S., Sinkin M.V., Trifonov I.S., Yevdokimova O.L., Stepanov V.N., Rozhnova E.N., Koinash G.V. Stereotactic Radiosurgery in the Complex Treatment of Patients With Epilepsy Associated With Various Structural Brain Lesions. Russian Sklifosovsky Journal "Emergency Medical Care". 2021;10(1):73-82. https://doi.org/10.23934/2223-9022-2021-10-1-73-82