Preview

Russian neurological journal

Advanced search

Structural epilepsy: current state of the problem

https://doi.org/10.30629/2658-7947-2024-29-4-5-15

Abstract

This review emphasizes modern conceptions in the fundamental and clinical aspects of structural epilepsy. Highly informative neuroimaging, electrophysiological and pathomorphological diagnostic methods contribution to the study of this problem is noted. Current understanding of the pathogenesis and clinical picture of the most common types of drug resistant epilepsy are presented: hippocampal sclerosis, focal cortical dysplasia and their surgical correction methods. We considered perspective directions of fundamental clinical and experimental research, focusing on the study of epileptogenesis mechanisms and developing effective methods for prevention and treatment.

About the Authors

M. Yu. Maksimova
Research Center of Neurology
Russian Federation

Moscow 



T. S. Gulevskaya
Research Center of Neurology
Russian Federation

Moscow 



References

1. Bell GS, Neligan A, Sander JW. An unknown quantity--the worldwide prevalence of epilepsy. Epilepsia. 2014;55(7):958– 62. doi: 10.1111/epi.12605

2. WHO Epilepsy Fact sheet. Updated February 2017. URL: http://www.who.int/mediacentre/factsheets/fs999/en/.

3. Avakyan G.N. Questions modern epileptology. Epilepsy and paroxysmal conditions. 2015;7(4):16–21. (In Russian). doi: 10.17749/2077-8333.2015.7.4.016-021

4. Singh G, Sander JW. The global burden of epilepsy report: Implications for low- and middle-income countries. Epilepsy Behav. 2020;105:106949. doi: 10.1016/j.yebeh.2020.106949

5. Ihme (2020). Epilepsy-level 1impairment. http://www.healthdata.org/results/gbd_summaries/2019/epilepsy-level-1-impairment

6. Kopachev DN, Shishkina LV, Bychenko VG, Shkatova AM, Golovteev AL, Troitskiĭ AA, Grinenko OA. Hippocampal sclerosis: pathogenesis, clinical features, diagnosis, and treatment. Zh. Voprosy Neirokhirurgii Imeni N.N. Burdenko. 2016;80(4):109-116. (In Russian). https://doi.org/10.17116/neiro2016804109-116.

7. Pitskhelauri DI, Kudieva ES, Melikyan AG, Vlasov PA, Kamenetskaya MI, Zaitsev OS, et al. Surgical treatment of drug-resistant epilepsy following hippocampal sclerosis. Zhurnal Voprosy Neirokhirurgii Imeni N.N. Burdenko. 2021;85(5):31–40 (in Russ.). https://doi.org/10.17116/neiro20218505131.

8. Margerison JH, Corsellis JA. Epilepsy and the temporal lobes. A clinical, electroencephalographic and neuropathological study of the brain in epilepsy, with particular reference to the temporal lobes. Brain. 1966 Sep;89(3):499–530. doi: 10.1093/brain/89.3.499

9. Kwan P, Brodie MJ. Early identification of refractory epilepsy. N Engl J Med. 2000;342(5):314–9. doi: 10.1056/NEJM200002033420503

10. French JA. Refractory epilepsy: clinical overview. Epilepsia. 2007;48 Suppl 1:3–7. doi: 10.1111/j.1528-1167.2007.00992.x

11. Thom M. Hippocampal sclerosis: progress since Sommer. Brain Pathol. 2009;19(4):565–72. doi: 10.1111/j.1750-3639.2008.00201.x

12. Thom M., Sisodiya S. Epilepsy. Vol. 1 Chapter 11, P. 683-739. In: Greenfield’s Neuropathology — Two Volume Set Edited By Seth Love, Arie Perry, James Ironside, Herbert Budka. 9th Edition. https://doi.org/10.1201/9781315382715

13. Schijns OE, Hoogland G, Kubben PL, Koehler PJ. The start and development of epilepsy surgery in Europe: a historical review. Neurosurg Rev. 2015;38(3):447–61. doi: 10.1007/s10143-015-0641-3

14. Blumcke I, Spreafico R, Haaker G, Coras R, Kobow K, Bien CG, et al. EEBB Consortium. Histopathological Findings in Brain Tissue Obtained during Epilepsy Surgery. N Engl J Med. 2017;377(17):1648–1656. doi: 10.1056/NEJMoa1703784

15. Cavanagh JB, Meyer A. Aetiological aspects of Ammon’s horn sclerosis associated with temporal lobe epilepsy. Br Med J. 1956;2(5006):1403–7. doi: 10.1136/bmj.2.5006.1403

16. Bruton CJ. The neuropathology of temporal lobe epilepsy. Oxford: Oxford University Press; 1988.

17. Blümcke I, Zuschratter W, Schewe JC, Suter B, Lie AA, Riederer BM, et al. Cellular pathology of hilar neurons in Ammon’s horn sclerosis. J Comp Neurol. 1999;414(4):437–53. doi: 10.1002/(sici)1096-9861(19991129)414:4<437::aid-cne2>3.0.co;2-3

18. Wieser HG. ILAE Commission Report. Mesial temporal lobe epilepsy with hippocampal sclerosis. Epilepsia. 2004;45(6):695– 714. doi: 10.1111/j.0013−9580.2004.09004.x

19. Blümcke I, Thom M, Aronica E, Armstrong DD, Bartolomei F, Bernasconi A, et al. International consensus classification of hippocampal sclerosis in temporal lobe epilepsy: a Task Force report from the ILAE Commission on Diagnostic Methods. Epilepsia. 2013;54(7):1315–29. doi: 10.1111/epi.12220

20. Thom M, Liagkouras I, Elliot KJ, Martinian L, Harkness W, McEvoy A, et al. Reliability of patterns of hippocampal sclerosis as predictors of postsurgical outcome. Epilepsia. 2010;51(9):1801– 8. doi: 10.1111/j.1528-1167.2010.02681.x

21. Houser CR. Granule cell dispersion in the dentate gyrus of humans with temporal lobe epilepsy. Brain Res. 1990;535(2):195– 204. doi: 10.1016/0006-8993(90)91601-c

22. Parent JM. Adult neurogenesis in the intact and epileptic dentate gyrus. Prog Brain Res. 2007;163:529–40. doi: 10.1016/S0079-6123(07)63028-3

23. Mongiat LA, Schinder AF. Adult neurogenesis and the plasticity of the dentate gyrus network. Eur J Neurosci. 2011;33(6):1055– 61. doi: 10.1111/j.1460-9568.2011.07603.x

24. Men S, Lee DH, Barron JR, Muñoz DG. Selective neuronal necrosis associated with status epilepticus: MR findings. AJNR Am J Neuroradiol. 2000;21(10):1837–40. PMID: 11110535.

25. Salmenperä T, Kälviäinen R, Partanen K, Mervaala E, Pitkänen A. MRI volumetry of the hippocampus, amygdala, entorhinal cortex, and perirhinal cortex after status epilepticus. Epilepsy Res. 2000;40(2-3):155–70. doi: 10.1016/s0920-1211(00)00121-2

26. Pitkänen A, Nissinen J, Nairismägi J, Lukasiuk K, Gröhn OH, Miettinen R, Kauppinen R. Progression of neuronal damage after status epilepticus and during spontaneous seizures in a rat model of temporal lobe epilepsy. Prog Brain Res. 2002;135:67–83. doi: 10.1016/S0079-6123(02)35008-8

27. Scott RC, Gadian DG, King MD, Chong WK, Cox TC, Neville BG, Connelly A. Magnetic resonance imaging findings within 5 days of status epilepticus in childhood. Brain. 2002;125(Pt 9):1951–9. doi: 10.1093/brain/awf202

28. Mahler B, Carlsson S, Andersson T, Adelöw C, Ahlbom A, Tomson T. Unprovoked seizures after traumatic brain injury: A population-based case-control study. Epilepsia. 2015;56(9):1438–44. doi: 10.1111/epi.13096

29. Herman ST. Epilepsy after brain insult: targeting epileptogenesis. Neurology. 2002;59(9 Suppl 5):S21-6. doi: 10.1212/wnl.59.9_suppl_5.s21

30. Abou-Khalil B, Ge Q, Desai R, Ryther R, Bazyk A, Bailey R, et al. Partial and generalized epilepsy with febrile seizures plus and a novel SCN1A mutation. Neurology. 2001;57(12):2265–72. doi: 10.1212/wnl.57.12.2265

31. Kasperaviciute D, Catarino CB, Matarin M, Leu C, Novy J, Tostevin A, et al. UK Brain Expression Consortium; Delanty N, Depondt C, Cavalleri GL, Kunz WS, Sisodiya SM. Epilepsy, hippocampal sclerosis and febrile seizures linked by common genetic variation around SCN1A. Brain. 2013;136(Pt 10):3140–50. doi: 10.1093/brain/awt233

32. Stögmann E, Zimprich A, Baumgartner C, Aull-Watschinger S, Höllt V, Zimprich F. A functional polymorphism in the prodynorphin gene promotor is associated with temporal lobe epilepsy. Ann Neurol. 2002;51(2):260–3. doi: 10.1002/ana.10108

33. Cavalleri GL, Lynch JM, Depondt C, Burley MW, Wood NW, Sisodiya SM, Goldstein DB. Failure to replicate previously reported genetic associations with sporadic temporal lobe epilepsy: where to from here? Brain. 2005;128(Pt 8):1832–40. doi: 10.1093/brain/awh524

34. Cavarsan CF, Malheiros J, Hamani C, Najm I, Covolan L. Is Mossy Fiber Sprouting a Potential Therapeutic Target for Epilepsy? Front Neurol. 2018;9:1023. doi: 10.3389/fneur.2018.01023

35. O’Dell CM, Das A, Wallace G 4th, Ray SK, Banik NL. Understanding the basic mechanisms underlying seizures in mesial temporal lobe epilepsy and possible therapeutic targets: a review.J Neurosci Res. 2012;90(5):913–24. doi: 10.1002/jnr.22829

36. Bonilha L, Elm JJ, Edwards JC, Morgan PS, Hicks C, Lozar C, et al. How common is brain atrophy in patients with medial temporal lobe epilepsy? Epilepsia. 2010;51(9):1774–9. doi: 10.1111/j.1528-1167.2010.02576.x

37. Malmgren K, Thom M. Hippocampal sclerosis--origins and imaging. Epilepsia. 2012;53 Suppl 4:19–33. doi: 10.1111/j.1528-1167.2012.03610.x

38. Walker MC. Hippocampal Sclerosis: Causes and Prevention. Semin Neurol. 2015;35(3):193–200. doi: 10.1055/s-0035-1552618

39. Blümcke I, Thom M, Aronica E, Armstrong DD, Vinters HV, Palmini A, et al. The clinicopathologic spectrum of focal cortical dysplasias: a consensus classification proposed by an ad hoc Task Force of the ILAE Diagnostic Methods Commission. Epilepsia. 2011;52(1):158–74. doi: 10.1111/j.1528-1167.2010.02777.x

40. Krylov V.V., Gekht A.B., Trifonov I.S., Lebedeva A.V., Kaimovskii I.L., Sinkin M.V., 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.).

41. de Tisi J, Bell GS, Peacock JL, McEvoy AW, Harkness WF, Sander JW, Duncan JS. The long-term outcome of adult epilepsy surgery, patterns of seizure remission, and relapse: a cohort study. Lancet. 2011;378(9800):1388–95. doi: 10.1016/S0140-6736(11)60890-8

42. Harvey AS, Cross JH, Shinnar S, Mathern GW; ILAE Pediatric Epilepsy Surgery Survey Taskforce. Defining the spectrum of international practice in pediatric epilepsy surgery patients. Epilepsia. 2008;49(1):146–55. doi: 10.1111/j.1528-1167.2007.01421.x

43. Engel J Jr, Wiebe S, French J, Sperling M, Williamson P, Spencer D, et al. Quality Standards Subcommittee of the American Academy of Neurology; American Epilepsy Society; American Association of Neurological Surgeons. Practice parameter: temporal lobe and localized neocortical resections for epilepsy: report of the Quality Standards Subcommittee of the American Academy of Neurology, in association with the American Epilepsy Society and the American Association of Neurological Surgeons. Neurology. 2003 ;60(4):538–47. doi: 10.1212/01.wnl.0000055086.35806.2d

44. de Lanerolle NC, Lee TS. New facets of the neuropathology and molecular profile of human temporal lobe epilepsy.Epilepsy Behav. 2005;7(2):190–203. doi: 10.1016/j.yebeh.2005.06.003

45. Christensen J. The Epidemiology of Posttraumatic Epilepsy. Semin Neurol. 2015;35(3):218–22. doi: 10.1055/s-0035-1552923

46. Lucke-Wold BP, Nguyen L, Turner RC, Logsdon AF, Chen YW, Smith KE, et al. Traumatic brain injury and epilepsy: Underlying mechanisms leading to seizure. Seizure. 2015;33:13–23. doi: 10.1016/j.seizure.2015.10.002

47. Lowenstein DH. Epilepsy after head injury: an overview. Epilepsia. 2009;50 Suppl 2:4–9. doi: 10.1111/j.1528-1167.2008.02004.x

48. Prince DA, Parada I, Scalise K, Graber K, Jin X, Shen F. Epilepsy following cortical injury: cellular and molecular mechanisms as targets for potential prophylaxis. Epilepsia. 2009;50 Suppl 2(Suppl 2):30–40. doi: 10.1111/j.1528-1167.2008.02008.x

49. Thom M, Liu JY, Thompson P, Phadke R, Narkiewicz M, Martinian L, et al. Neurofibrillary tangle pathology and Braak staging in chronic epilepsy in relation to traumatic brain injury and hippocampal sclerosis: a post-mortem study.Brain. 2011;134(Pt 10):2969–81. doi: 10.1093/brain/awr209

50. Thom M, Blümcke I, Aronica E. Long-term epilepsy-associated tumors. Brain Pathol. 2012;22(3):350–79. doi: 10.1111/j.1750-3639.2012.00582.x

51. Buckingham SC, Campbell SL, Haas BR, Montana V, Robel S, Ogunrinu T, Sontheimer H. Glutamate release by primary brain tumors induces epileptic activity. Nat Med. 2011;17(10):1269– 74. doi: 10.1038/nm.2453

52. Feyissa AM, Hasan TF, Meschia JF. Stroke-related epilepsy. Eur J Neurol. 2019;26(1):18–e3. doi: 10.1111/ene.13813

53. Holtkamp M, Schuchmann S, Gottschalk S, Meierkord H. Recurrent seizures do not cause hippocampal damage. J Neurol. 2004;251(4):458–63. doi: 10.1007/s00415-004-0356-9

54. Issues of epidemiology of vascular diseases of the brain. Ed. E.V. Schmidt. M. 1972 (In Russ.).

55. Gabashvili V.M., Prokhorova E.S., Shakarishvili R.R. Epileptic seizures in vascular diseases of the brain — Tbilisi: Metsniereba, 1986. — 337. (In Russ.).

56. Zelano J, Holtkamp M, Agarwal N, Lattanzi S, Trinka E, Brigo F. How to diagnose and treat post-stroke seizures and epilepsy. Epileptic Disord. 2020;22(3):252–263. doi: 10.1684/epd.2020.1159

57. Vereshchagin N.V., Lunev D.K., Prokhorova E.S., Gulevskaya T.S. Clinical forms of epileptic seizures in ischemic circulatory disorders in the area of adjacent blood supply of the anterior and middle cerebral arteries. Journal of Neuropathology and Psychiatry named after. S.S. Korsakov. 1975;79(9):1020–1025 (In Russ.).

58. Maksimova M.Yu., Brutian A.G., Shalimanova E.V. Epilepsy as part of paroxysmal disorders after ischaemic stroke. Annals of clinical and experimental neurology 2020;14(3):11–20. (In Russ.). doi: 10.25692/ACEN.2020.3.2.

59. Prokhorova E.S., Gulevskaya T.S., Morgunov V.A. Status epilepticus in cerebral hemorrhage in patients with hypertension. Journal of Neuropathology and Psychiatry named after. S.S. Korsakov. 1975;75(9):1281–1286. (In Russ.).

60. Khasanova DR, Danilova TV, Latypova ZK. Some clinical and diagnostic features of patients with new-onset epilepsy in the presence of chronic cerebrovascular disease. Nevrology, Neuropsykhiatry, Psykhosomatics. 2015;7(3):28–34. (In Russian). doi: http://dx.doi.org/10.14412/2074-2711-2015-3-28-34.

61. Moran NF, Fish DR, Kitchen N, Shorvon S, Kendall BE, Stevens JM. Supratentorial cavernous haemangiomas and epilepsy: a review of the literature and case series. J Neurol Neurosurg Psychiatry. 1999;66(5):561–8. doi: 10.1136/jnnp.66.5.561

62. Zhao J, Wang S, Li J, Qi W, Sui D, Zhao Y. Clinical characteristics and surgical results of patients with cerebral arteriovenousmalformations. Surg Neurol. 2005 Feb;63(2):156–61; discussion 161. doi: 10.1016/j.surneu.2004.04.021

63. Tadevosyan AR, Sysoev KV, Samochernykh KA, Khachatrian VA. Arteriovenous malformations and epileptic seizures in children: risk factors of seizures and efficacy of their control depending on the surgical treatment modality. Zh. Voprosy Neirokhirurgii Imeni N.N. Burdenko. 2019;83(1):83-89. (In Russian). https://doi.org/10.17116/neiro2019830117583.

64. Egorova E.V., Dmitrienko D.V. Developmental Venous Anomalies and Epilepsy. Doctor.Ru. 2021;20(9):21–25. (in Russian). doi: 10.31550/1727-2378-2021-20-9-21-25

65. Klement W, Blaquiere M, Zub E, deBock F, Boux F, Barbier E, et al. A pericyte-glia scarring develops at the leaky capillaries in the hippocampus during seizure activity. Epilepsia. 2019;60(7):1399–1411. doi: 10.1111/epi.16019

66. Ogaki A, Ikegaya Y, Koyama R. Vascular Abnormalities and the Role of Vascular Endothelial Growth Factor in the Epileptic Brain. Front Pharmacol. 2020;11:20. doi: 10.3389/fphar.2020.00020

67. Areshkina I.G., Sapronova M.R., Schnaider N.A., Narodova E.A., Dmitrenko D.V. Outcomes of Epilepsy Surgery. Doctor.Ru. 2020;19(4):29–34. (in Russian) doi: 10.31550/1727-2378-2020-19-4-29-34.

68. Savateev AN, Golanov AV, Saushev DA, Osinov IK, Kostyuchenko VV, Dalechina AV, et al. Stereotactic radiosurgery for epilepsy related to hypothalamic hamartoma. Zh Vopr Neirokhir Im N N Burdenko. 2022;86(4):14–24. (in Russian). doi: 10.17116/neiro20228604114.

69. Haut SR, Velísková J, Moshé SL.Susceptibility of immature and adult brains to seizure effects. Lancet Neurol. 2004;3(10):608– 17. doi: 10.1016/S1474-4422(04)00881-6

70. Hunter G, Young GB. Status epilepticus: a review, with emphasis on refractory cases. Can J Neurol Sci. 2012;39(2):157–69. doi: 10.1017/s0317167100013160

71. Giblin KA, Blumenfeld H. Is epilepsy a preventable disorder? New evidence from animal models. Neuroscientist. 2010;16(3):253–75. doi: 10.1177/1073858409354385

72. Wong M. Mechanisms of epileptogenesis in tuberous sclerosis complex and related malformations of cortical development with abnormal glioneuronal proliferation. Epilepsia. 2008;49(1):8–21. doi: 10.1111/j.1528-1167.2007.01270.x

73. Sofroniew MV, Vinters HV. Astrocytes: biology and pathology. Acta Neuropathol. 2010;119(1):7–35. doi: 10.1007/s00401-009-0619-8 74. Gómez-Gonzalo M, Losi G, Chiavegato A, Zonta M, Cammarota M, Brondi M, et al. An excitatory loop with astrocytes contributes to drive neurons to seizure threshold. PLoS Biol. 2010 Apr 13;8(4):e1000352. doi: 10.1371/journal.pbio.1000352


Review

For citations:


Maksimova M.Yu., Gulevskaya T.S. Structural epilepsy: current state of the problem. Russian neurological journal. 2024;29(4):5-15. (In Russ.) https://doi.org/10.30629/2658-7947-2024-29-4-5-15

Views: 439


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 2658-7947 (Print)
ISSN 2686-7192 (Online)