Objectives. To summarize data on the radiological and histological diagnosis of benign tumors associated with epilepsy and to provide recommendations for the surgical treatment of epilepsy in these tumors. Materials and methods. Articles from PubMed and our own clinical data were used. Results. Benign glioneuronal tumors are the second most common cause of structural drug-resistant epilepsy in adults after hippocampal sclerosis. Extremely slow growth, location in the cerebral cortex, the presence of neuronal tissue in the tumor stroma, and concomitant epilepsy are common features of these neoplasms. The difficulty of treating glioneuronal tumors lies in the combination of epileptological and neurooncological aspects. The epileptogenic zone may extend beyond the tumor, so isolated resection may not be enough to stop seizures. Conclusions. From a neurooncological point of view, glioneuronal tumors are neoplasms with a very low proliferative potential, but careful differential diagnosis against more aggressive glial tumors is required; this can be extremely difficult but can be achieved using histological and immunohistochemical approaches.
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M. Thom, I. Blümcke, and E. Aronica, “Long-term epilepsy-associated tumors,” Brain Pathol., 22, No. 3, 350–379 (2012), https://doi.org/https://doi.org/10.1111/j.1750-3639.2012.00582.x.
C. Luyken, I. Blümcke, R. Fimmers, et al., “The spectrum of longterm epilepsy-associated tumors: long-term seizure and tumor outcome and neurosurgical aspects,” Epilepsia, 44, No. 6, 822–830 (2003), https://doi.org/https://doi.org/10.1046/j.1528-1157.2003.56102.x.
J. S. Duncan and J. De Tisi, “MRI in the diagnosis and management of epileptomas,” Epilepsia, 54, Suppl. 9, 40–43 (2013), https://doi.org/https://doi.org/10.1111/epi.12442.
I. Blumcke, E. Aronica, H. Urbach, et al., “A neuropathology-based approach to epilepsy surgery in brain tumors and proposal for a new terminology use for long-term epilepsy-associated brain tumors,” Acta Neuropathol., 128, No. 1, 39–54 (2014), https://doi.org/https://doi.org/10.1007/s00401-014-1288-9.
B. S. Kasper and E. M. Kasper, “New classification of epilepsy-related neoplasms: The clinical perspective,” Epilepsy Behav., 67, 91–97 (2017), https://doi.org/https://doi.org/10.1016/j.yebeh.2016.12.020.
V. S. Khalilov, A. A. Kholin, A. N. Kislyakov, et al., “Neuroradiological and pathomorphological features of epilepsy associated brain tumors,” Luch. Diagn. Ter., 12, No. 2, 7–21 (2021, https://doi.org/10.22328/2079-5343-2021-12-2-7-21.
I. Blümcke, E. Aronica, A. Becker, et al., “Low-grade epilepsy-associated neuroepithelial tumours-the 2016 WHO classification,” Nat. Rev. Neurol., 12, No. 12, 732–740 (2016), https://doi.org/https://doi.org/10.1038/nrneurol.2016.173.
D. N. Louis, A. Perry, P. Wesseling, et al., “The 2021 WHO Classification of Tumors of the Central Nervous System: a summary,” Neuro. Oncol., 23, No. 8, 1231–1251 (2021), https://doi.org/https://doi.org/10.1093/neuonc/noab106.
E. J. Rushing, “WHO classification of tumors of the nervous system: preview of the upcoming 5th edition,” Memo – Mag. Europ. Med. Oncol., 14, No. 2, 188–191 (2021), https://doi.org/https://doi.org/10.1007/s12254-021-00680-x.
A. K. Wefers, D. Stichel, D. Schrimpf, et al., “Isomorphic diffuse glioma is a morphologically and molecularly distinct tumour entity with recurrent gene fusions of MYBL1 or MYB and a benign disease course,” Acta Neuropathol., 139, No. 1, 193–209 (2020), https://doi.org/https://doi.org/10.1007/s00401-019-02078-w.
S. Luzzi, A. Elia, M. Del Maestro, et al., “Dysembryoplastic neuroepithelial tumors: What you need to know,” World Neurosurg., 127, 255–265 (2019), https://doi.org/https://doi.org/10.1016/j.wneu.2019.04.056.
A. Cistaro, D. Albano, P. Alongi, et al., “The Role of PET in supratentorial and infratentorial pediatric brain tumors,” Curr. Oncol., 28, No. 4, 2481–2495 (2021), https://doi.org/https://doi.org/10.3390/curroncol28040226.
S. Rheims, S. Rubi, S. Bouvard, et al., “Accuracy of distinguishing between dysembryoplastic neuroepithelial tumors and other epileptogenic brain neoplasms with [11C]methionine PET,” Neuro. Oncol., 16, No. 10, 1417–1426 (2014), https://doi.org/https://doi.org/10.1093/neuonc/nou022.
F. Bernard, I. Zemmoura, A. Ter Minassian, et al., “Anatomical variability of the arcuate fasciculus: a systematical review,” Surg. Radiol. Anat., 41, No. 8, 889–900 (2019), https://doi.org/https://doi.org/10.1007/s00276-019-02244-5.
D. Koshiyama, M. Fukunaga, N. Okada, et al., “Association between the superior longitudinal fasciculus and perceptual organization and working memory: A diffusion tensor imaging study,” Neurosci. Lett., 738, No. 8, 135349 (2020), https://doi.org/10.1016/j.neulet.2020.135349.
R. Nakajima, M. Kinoshita, H. Shinohara, et al., “The superior longitudinal fascicle: reconsidering the fronto-parietal neural network based on anatomy and function,” Brain Imag. Behav., 14, No. 6, 2817–2830 (2020), https://doi.org/https://doi.org/10.1007/s11682-019-00187-4.
A. Sasagawa, R. Enatsu, T. Kuribara, et al., “Cortical regions and networks of hyperkinetic seizures: Electrocorticography and diffusion tensor imaging study,” Epilepsy Behav., 125, 108405 (2021), https://doi.org/10.1016/j.yebeh.2021.108405.
A. J. Ristić, A. V. Alexopoulos, N. So, et al., “Parietal lobe epilepsy: the great imitator among focal epilepsies,” Epileptic Disord., 14, No. 1, 22–31 (2012), https://doi.org/https://doi.org/10.1684/epd.2012.0484.
I. Blümcke, R. Coras, A. K. Wefers, et al., “Review: Challenges in the histopathological classification of ganglioglioma and DNT: microscopic agreement studies and a preliminary genotype-phenotype analysis,” Neuropathol. Appl. Neurobiol., 45, No. 2, 95–107 (2019), https://doi.org/https://doi.org/10.1111/nan.12522.
R. J. Slegers and I. Blumcke, “Low-grade developmental and epilepsy associated brain tumors: A critical update 2020,” Acta Neuropathol. Comm., 8, No. 1, 1–11 (2020), https://doi.org/https://doi.org/10.1186/s40478-020-00904-x.
K. Kobow, S. Baulac, A. von Deimling, et al., “Molecular diagnostics in drug-resistant focal epilepsy define new disease entities,” Brain Pathol., 31, No. 4, 1–9 (2021), https://doi.org/https://doi.org/10.1111/bpa.12963.
M. Simon and A. Grote, “Glioneuronal and other epilepsy-associated tumours,” in: Oxford Textbook of Neurological Surgery, Oxford University Press (2019), pp. 129–140, https://doi.org/10.1093/med/9780198746706.001.0001.
Q. Wang, Y. Xiong, J. Chen, et al., “Cystic angiocentric glioma: a clinical case and literature review,” Childs Nerv. Syst., 37, No. 8, 2701–2705 (2021), https://doi.org/https://doi.org/10.1007/s00381-020-04882-2.
C. Dorfer, “Ganglioglioma,” in: Oncology of CNS Tumors, Springer (2019), pp. 493–502, https://doi.org/10.1007/978-3-030-04152-6.
C. Horbinski, J. Kofler, G. Yeaney, et al., “Isocitrate dehydrogenase 1 analysis differentiates gangliogliomas from infiltrative gliomas,” Brain Pathol., 21, No. 5, 564–574 (2011), https://doi.org/https://doi.org/10.1111/j.1750-3639.2011.00480.x.
M. Pekmezci, J. E. Villanueva-Meyer, B. Goode, et al., “The genetic landscape of ganglioglioma,” Acta Neuropathol. Comm., 6, No. 1, 47 (2018), https://doi.org/10.1186/s40478-018-0551-z.
J. Yoon, M. Cusimano, and D. G. Munoz, “Pilocytic astrocytoma vs. ganglioglioma: Progression, misdiagnosis, and implications in BRAF testing,” J. Clin. Neurosci., 66, 231–234 (2019), https://doi.org/https://doi.org/10.1016/j.jocn.2019.05.002.
J. H. Phi and S.-K. Kim, “clinical pearls and advances in molecular researches of epilepsy-associated tumors,” J. Korean Neurosurg. Soc., 62, No. 3, 313–320 (2019), https://doi.org/https://doi.org/10.3340/jkns.2019.0033.
Y. Yao, D. Zhang, Y. Qi, et al., “Surgical resection of dysembryoplatic neuroepithelioma tumor associated with epilepsy based on imaging classification,” Neurol. Res., 12, No. 5, 1–7 (2022), https://doi.org/https://doi.org/10.1080/01616412.2021.2024730.
M. Yibirin, D. De Oliveira, I. Suarez, et al., “A case of dysembryoplastic neuroepithelial tumor in an adolescent male,” Cureus, 13, No. 3, e13917 (2021), https://doi.org/10.7759/cureus.13917.
M. Chougule, “Neuronal and mixed neuronal-glial tumors,” in: Neuropathology of Brain Tumors with Radiologic Correlates, Springer (2020), pp. 139–166, https://doi.org/10.1007/978-981-15-7126-8_9.
Z. Zheng, H. Jiang, H. Wu, et al., “Epilepsy surgery for low-grade epilepsy-associated neuroepithelial tumor of temporal lobe: a single-institution experience of 61 patients,” Neurol. Sci., 43, No. 5, 3333–3341 (2022), https://doi.org/https://doi.org/10.1007/s10072-021-05703-3.
V. L. Vogt, J. A. Witt, D. Delev, et al., “Cognitive features and surgical outcome of patients with long-term epilepsy-associated tumors (LEATs) within the temporal lobe,” Epilepsy Behav., 88, 25–32 (2018), https://doi.org/https://doi.org/10.1016/j.yebeh.2018.08.028.
L. Maillard, J. P. Vignal, M. Gavaret, et al., “Semiologic and electrophysiologic correlations in temporal lobe seizure subtypes,” Epilepsia, 45, No. 12, 1590–1599 (2004), https://doi.org/https://doi.org/10.1111/j.0013-9580.2004.09704.x.
B. Yang, J. Mo, C. Zhang, et al., “Clinical features of automatisms and correlation with the seizure onset zones: A cluster analysis of 74 surgically-treated cases,” Seizure, 94, No. 119, 82–89 (2022), https://doi.org/https://doi.org/10.1016/j.seizure.2021.11.015.
B. Abarrategui, R. Mai, I. Sartori, et al., “Temporal lobe epilepsy: A never-ending story,” Epilepsy Behav., 34, No. 7, 122 (2021), https://doi.org/10.1016/j.yebeh.2021.108122.
M. Giulioni, G. Rubboli, G. Marucci, et al., “Seizure outcome of epilepsy surgery in focal epilepsies associated with temporomesial glioneuronal tumors: Lesionectomy compared with tailored resection – Clinical article,” J. Neurosurg., 111, No. 6, 1275–1282 (2009), https://doi.org/https://doi.org/10.3171/2009.3.JNS081350.
S. Ljunggren, L. Andersson-Roswall, H. Imberg, et al., “Predicting verbal memory decline following temporal lobe resection for epilepsy,” Acta Neurol. Scand., 140, No. 5, 312–319 (2019), https://doi.org/https://doi.org/10.1111/ane.13146.
I. Blümcke, M. Thom, E. Aronica, 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, 52, No. 1, 158–174 (2011), https://doi.org/https://doi.org/10.1111/j.1528-1167.2010.02777.x.
R. J. Keogh, R. Aslam, M. A. Hennessy, et al., “One year of procarbazine lomustine and vincristine is poorly tolerated in low grade glioma: a real world experience in a national neuro-oncology centre,” BMC Cancer, 21, No. 1, 1–8 (2021), https://doi.org/https://doi.org/10.1186/s12885-021-07809-5.
T. J. C. Wang and M. P. Mehta, “Low-Grade Glioma Radiotherapy Treatment and Trials,” Neurosurg. Clin. N. Am., 30, No. 1, 111–118 (2019), https://doi.org/https://doi.org/10.1016/j.nec.2018.08.008.
J. Wang, L. Yan, P. Ai, et al., “Observation versus radiotherapy with or without temozolomide in postoperative WHO grade II high-risk low-grade glioma: a retrospective cohort study,” Neurosurg. Rev., 44, No. 3, 1447–1455 (2021), https://doi.org/https://doi.org/10.1007/s10143-020-01326-y.
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Translated from Zhurnal Nevrologii i Psikhiatrii imeni S. S. Korsakova, Vol. 122, No. 4, Iss. 1, pp. 127–134, April, 2022.
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Kopachev, D.N., Shishkina, L.V., Shkatova, A.M. et al. Epilepsy-Associated Glioneuronal Tumors. Neurosci Behav Physi 52, 1199–1206 (2022). https://doi.org/10.1007/s11055-023-01348-1
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DOI: https://doi.org/10.1007/s11055-023-01348-1