Diagnosis and surgical treatment of non-lesional temporal lobe epilepsy with unilateral amygdala enlargement.
Amygdala enlargement
Automatically volumetric analysis
EEG source imaging
Resective surgery
Temporal lobe epilepsy
Journal
Neurological sciences : official journal of the Italian Neurological Society and of the Italian Society of Clinical Neurophysiology
ISSN: 1590-3478
Titre abrégé: Neurol Sci
Pays: Italy
ID NLM: 100959175
Informations de publication
Date de publication:
Jun 2021
Jun 2021
Historique:
received:
01
07
2020
accepted:
03
10
2020
pubmed:
13
10
2020
medline:
1
6
2021
entrez:
12
10
2020
Statut:
ppublish
Résumé
Exploring the role of amygdala enlargement (AE) in temporal lobe epilepsy (TLE) without ipsilateral mesial temporal sclerosis (MTS) using comprehensive presurgical workup tools including traditional tools, automatically volumetric analysis, high-density EEG (HD-EEG) source imaging (HD-ESI), and stereoelectroencephalography (SEEG). Nine patients diagnosed with TLE-AE who underwent resective surgeries encompassing the amygdala were retrospectively studied. HD-ESI was obtained using 256-channel HD-EEG on the individualized head model. For automatic volumetric analysis, 48 matched controls were enrolled. Diagnosis and surgical strategies were based on a comprehensive workup following the anatomo-electro-clinical principle. At post-operative follow-up (average 30.9 months), eight patients had achieved Engel class I and one Engel class II recovery. HD-ESI yielded unifocal source estimates in anterior mesial temporal region in 85.7% of cases. Automatic volumetric analysis showed the AE sides were consistent with the values determined through other preoperative workup tools. Furthermore, the amygdala volume of the affected sides in AE was significantly greater than that of the larger sides in controls (p < 0.001). Meanwhile, the amygdala volume lateral index (LI) of AE was significantly higher than in controls (p < 0.001). SEEG analysis showed that ictal onsets arose from the enlarged amygdala (and hippocampus) in all cases. In addition to traditional workup tools, automatic volumetric analysis, HD-ESI on individualized head model, and invasive SEEG can provide evidence of epileptogenicity in TLE-AE. Resective surgical strategies encompassing the amygdala result in better prognosis. In suspected TLE cases, more attention should be focused on detecting enlargement of amygdala which sometimes is "hidden" in "MR-negative" non-MTS cases.
Identifiants
pubmed: 33044668
doi: 10.1007/s10072-020-04794-8
pii: 10.1007/s10072-020-04794-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2353-2361Subventions
Organisme : National Natural Science Foundation of China
ID : 81701273
Organisme : National Natural Science Foundation of China
ID : 81701250
Organisme : National Natural Science Foundation of China
ID : 81801290
Organisme : Science and Technology Commission of Shanghai Municipality (CN)
ID : 18JC1410403
Références
Tellez-Zenteno JF, Hernandez Ronquillo L, Moien-Afshari F, Wiebe S (2010) Surgical outcomes in lesional and non-lesional epilepsy: a systematic review and meta-analysis. Epilepsy Res 89(2–3):310–318. https://doi.org/10.1016/j.eplepsyres.2010.02.007
doi: 10.1016/j.eplepsyres.2010.02.007
pubmed: 20227852
So EL, Lee RW (2014) Epilepsy surgery in MRI-negative epilepsies. Curr Opin Neurol 27(2):206–212. https://doi.org/10.1097/wco.0000000000000078
doi: 10.1097/wco.0000000000000078
pubmed: 24553461
Beh SMJ, Cook MJ, D'Souza WJ (2016) Isolated amygdala enlargement in temporal lobe epilepsy: a systematic review. Epilepsy Behav 60:33–41. https://doi.org/10.1016/j.yebeh.2016.04.015
doi: 10.1016/j.yebeh.2016.04.015
pubmed: 27176882
See S-J, Jehi LE, Vadera S, Bulacio J, Najm I, Bingaman W (2013) Surgical outcomes in patients with extratemporal epilepsy and subtle or normal magnetic resonance imaging findings. Neurosurgery 73(1):68–77. https://doi.org/10.1227/01.neu.0000429839.76460.b7
Immonen A, Jutila L, Muraja-Murro A, Mervaala E, Aikia M, Lamusuo S, Kuikka J, Vanninen E, Alafuzoff I, Ikonen A, Vanninen R, Vapalahti M, Kalviainen R (2010) Long-term epilepsy surgery outcomes in patients with MRI-negative temporal lobe epilepsy. Epilepsia 51(11):2260–2269. https://doi.org/10.1111/j.1528-1167.2010.02720.x
doi: 10.1111/j.1528-1167.2010.02720.x
pubmed: 21175607
McGovern RA, Ruggieri P, Bulacio J, Najm I, Bingaman WE, Gonzalez-Martinez JA (2019) Risk analysis of hemorrhage in stereo-electroencephalography procedures. Epilepsia 60(3):571–580. https://doi.org/10.1111/epi.14668
doi: 10.1111/epi.14668
pubmed: 30746685
Mitsueda-Ono T, Ikeda A, Inouchi M, Takaya S, Matsumoto R, Hanakawa T, Sawamoto N, Mikuni N, Fukuyama H, Takahashi R (2010) Amygdalar enlargement in patients with temporal lobe epilepsy. J Neurol Neurosurg Psychiatry 82(6):652–657. https://doi.org/10.1136/jnnp.2010.206342
doi: 10.1136/jnnp.2010.206342
pubmed: 21047879
Coan AC, Morita ME, de Campos BM, Yasuda CL, Cendes F (2013) Amygdala enlargement in patients with mesial temporal lobe epilepsy without hippocampal sclerosis. Front Neurol 4. https://doi.org/10.3389/fneur.2013.00166
Reyes A, Thesen T, Kuzniecky R, Devinsky O, McDonald CR, Jackson GD, Vaughan DN, Blackmon K (2017) Amygdala enlargement: temporal lobe epilepsy subtype or nonspecific finding? Epilepsy Res 132:34–40. https://doi.org/10.1016/j.eplepsyres.2017.02.019
doi: 10.1016/j.eplepsyres.2017.02.019
pubmed: 28284051
pmcid: 5945291
Bower SPC, Vogrin SJ, Morris K, Cox I, Murphy M, Kilpatrick CJ, Cook MJ (2003) Amygdala volumetry in “imaging-negative” temporal lobe epilepsy. Journal of neurology, Neurosurgery &amp; Psychiatry 74(9):1245. https://doi.org/10.1136/jnnp.74.9.1245
doi: 10.1136/jnnp.74.9.1245
Kwan P, Arzimanoglou A, Berg AT, Brodie MJ, Hauser WA, Mathern GW, Moshe SL, Perucca E, Wiebe S, French JA (2010) Erratum: Definition of drug resistant epilepsy. Consensus proposal by the ad hoc task force of the ILAE commission on therapeutic strategies (Epilepsia (2010) 51 (1069-77)). Epilepsia 51(9)
Feng R, Hu J, Wu J, Lang L, Ma C, Sun B, Gu X, Pan L (2018) Accurate source imaging based on high resolution scalp electroencephalography and individualized finite difference head models in epilepsy pre-surgical workup. Seizure 59:126–131. https://doi.org/10.1016/j.seizure.2018.05.009
doi: 10.1016/j.seizure.2018.05.009
pubmed: 29843085
Manjón JV, Coupé P (2016) volBrain: an online MRI brain volumetry system. Frontiers in Neuroinformatics. https://doi.org/10.3389/fninf.2016.00030
Minami N, Morino M, Uda T, Komori T, Nakata Y, Arai N, Kohmura E, Nakano I (2015) Surgery for amygdala enlargement with mesial temporal lobe epilepsy: pathological findings and seizure outcome. J Neurol Neurosurg Psychiatry 86(8):887–894. https://doi.org/10.1136/jnnp-2014-308383
doi: 10.1136/jnnp-2014-308383
pubmed: 25224675
Lv R-J, Ren H-T, Guan H-Z, Cui T, Shao X-Q (2018) Seizure semiology: an important clinical clue to the diagnosis of autoimmune epilepsy. Annals of Clinical and Translational Neurology 5(2):208–215. https://doi.org/10.1002/acn3.520
doi: 10.1002/acn3.520
pubmed: 29468181
pmcid: 5817820
Pascual-Marqui RD (2002) Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods and Findings in Experimental and Clinical Pharmacology 24 Suppl D:5–12
pubmed: 12575463
Perucca P, Dubeau F, Gotman J (2014) Intracranial electroencephalographic seizure-onset patterns: effect of underlying pathology. Brain 137(Pt 1):183–196. https://doi.org/10.1093/brain/awt299
doi: 10.1093/brain/awt299
pubmed: 24176980
Feng R, Hameed NUF, Hu J, Lang L, He J, Wu D, Fan Z, Jiang S, Guo Q, Liu F, Mao Y, Li C, Sun B, Chen L, Pan L (2020) Ictal stereo-electroencephalography onset patterns of mesial temporal lobe epilepsy and their clinical implications. Clin Neurophysiol 131(9):2079–2085. https://doi.org/10.1016/j.clinph.2020.05.033
Malter MP, Widman G, Galldiks N, Stoecker W, Helmstaedter C, Elger CE, Wagner J (2016) Suspected new-onset autoimmune temporal lobe epilepsy with amygdala enlargement. Epilepsia 57(9):1485–1494. https://doi.org/10.1111/epi.13471
doi: 10.1111/epi.13471
pubmed: 27418040
Coan AC, Morita ME, Campos BM, Bergo FPG, Kubota BY, Cendes F (2013) Amygdala enlargement occurs in patients with mesial temporal lobe epilepsy and hippocampal sclerosis with early epilepsy onset. Epilepsy Behav 29(2):390–394. https://doi.org/10.1016/j.yebeh.2013.08.022
doi: 10.1016/j.yebeh.2013.08.022
pubmed: 24074891
Feng R, Hu J, Pan L, Wu J, Lang L, Jiang S, Gu X, Guo J, Zhou L (2016) Application of 256-channel dense array electroencephalographic source imaging in presurgical workup of temporal lobe epilepsy. Clinical Neurophysiology 127(1):108–116. https://doi.org/10.1016/j.clinph.2015.03.009
doi: 10.1016/j.clinph.2015.03.009
pubmed: 25891421
Feng R, Hu J, Wu J, Lang L, Ma C, Jiang S, Sun B, Gu X, Pan L (2017) Comprehensive preoperative work-up and surgical treatment of low grade tumor/benign lesion related temporal lobe epilepsy. Journal of Clinical Neuroscience 39:203–208. https://doi.org/10.1016/j.jocn.2017.01.013
doi: 10.1016/j.jocn.2017.01.013
pubmed: 28202379
Feng R, Hu J, Wu J, Ma C, Lang L, Sun B, Pan L (2018) 135 individualized high-density electroencephalographic source imaging technique in Presurgical workup: contribution to surgical strategy making for intractable epilepsy involving mesial temporal lobe structures. Neurosurgery 65(CN_suppl_1):92. https://doi.org/10.1093/neuros/nyy303.135
doi: 10.1093/neuros/nyy303.135
Brodbeck V, Spinelli L, Lascano AM, Wissmeier M, Vargas M-I, Vulliemoz S, Pollo C, Schaller K, Michel CM, Seeck M (2011) Electroencephalographic source imaging: a prospective study of 152 operated epileptic patients. Brain 134:2887–2897. https://doi.org/10.1093/brain/awr243
doi: 10.1093/brain/awr243
pubmed: 21975586
pmcid: 3187544
Kaiboriboon K, Luders H, Hamaneh MB, Turnbull J, Lhatoo SD (2012) EEG source imaging in epilepsy—practicalities and pitfalls. Nat Rev Neurol 8(9):498–507
doi: 10.1038/nrneurol.2012.150
Lv R-J, Sun Z-R, Cui T, Guan H-Z, Ren H-T, Shao X-Q (2014) Temporal lobe epilepsy with amygdala enlargement: a subtype of temporal lobe epilepsy. BMC Neurol 14(1):194. https://doi.org/10.1186/s12883-014-0194-z
doi: 10.1186/s12883-014-0194-z
pubmed: 25269594
pmcid: 4210593
Kim DW, Lee SK, Chung CK, Koh Y-C, Choe G, Lim SD (2012) Clinical features and pathological characteristics of amygdala enlargement in mesial temporal lobe epilepsy. J Clin Neurosci 19(4):509–512. https://doi.org/10.1016/j.jocn.2011.05.042
doi: 10.1016/j.jocn.2011.05.042
pubmed: 22321366
Suzuki H, Sugano H, Nakajima M, Higo T, Iimura Y, Mitsuhashi T, Fusegi K, Kakita A, Otsubo H, Arai H (2019) The epileptogenic zone in pharmaco-resistant temporal lobe epilepsy with amygdala enlargement. Epileptic Disord 21(3):252–264. https://doi.org/10.1684/epd.2019.1075
doi: 10.1684/epd.2019.1075
pubmed: 31225808
David O, Blauwblomme T, Job AS, Chabardes S, Hoffmann D, Minotti L, Kahane P (2011) Imaging the seizure onset zone with stereo-electroencephalography. Brain 134(Pt 10):2898–2911. https://doi.org/10.1093/brain/awr238
doi: 10.1093/brain/awr238
pubmed: 21975587
Gonzalez-Martinez J, Mullin J, Bulacio J, Gupta A, Enatsu R, Najm I, Bingaman W, Wyllie E, Lachhwani D (2014) Stereoelectroencephalography in children and adolescents with difficult-to-localize refractory focal epilepsy. Neurosurgery 75(3):258–268; discussion 267-258. https://doi.org/10.1227/NEU.0000000000000453
doi: 10.1227/NEU.0000000000000453
pubmed: 24887288
Serletis D, Bulacio J, Bingaman W, Najm I, González-Martínez J (2014) The stereotactic approach for mapping epileptic networks: a prospective study of 200 patients. J Neurosurg 121(5):1239–1246. https://doi.org/10.3171/2014.7.JNS132306
doi: 10.3171/2014.7.JNS132306
pubmed: 25148007
Faught E, Kuzniecky RI, Hurst DC (1992) Ictal EEG wave forms from epidural electrodes predictive of seizure control after temporal lobectomy. Electroencephalogr Clin Neurophysiol 83(4):229–235. https://doi.org/10.1016/0013-4694(92)90116-y
doi: 10.1016/0013-4694(92)90116-y
pubmed: 1382944
Tassi L, Garbelli R, Colombo N, Bramerio M, Russo GL, Mai R, Deleo F, Francione S, Nobili L, Spreafico R (2012) Electroclinical, MRI and surgical outcomes in 100 epileptic patients with type II FCD. Epileptic Disorders 14(3):257–266. https://doi.org/10.1684/epd.2012.0525
doi: 10.1684/epd.2012.0525
pubmed: 22963868
Grimm O, Pohlack S, Cacciaglia R, Winkelmann T, Plichta MM, Demirakca T, Flor H (2015) Amygdalar and hippocampal volume: a comparison between manual segmentation, Freesurfer and VBM. J Neurosci Methods 253:254–261. https://doi.org/10.1016/j.jneumeth.2015.05.024
doi: 10.1016/j.jneumeth.2015.05.024
pubmed: 26057114
Coupe P, Catheline G, Lanuza E, Manjon JV, Alzheimer's Disease Neuroimaging I (2017) Towards a unified analysis of brain maturation and aging across the entire lifespan: a MRI analysis. Hum Brain Mapp 38(11):5501–5518. https://doi.org/10.1002/hbm.23743
doi: 10.1002/hbm.23743
pubmed: 28737295
pmcid: 6866824
Hoffmann C, Distel L, Knippen S, Gryc T, Schmidt MA, Fietkau R, Putz F (2018) Brain volume reduction after whole-brain radiotherapy: quantification and prognostic relevance. Neuro-Oncology 20(2):268–278. https://doi.org/10.1093/neuonc/nox150
doi: 10.1093/neuonc/nox150
pubmed: 29016812
Rodríguez-Cruces R, Velázquez-Pérez L, Rodríguez-Leyva I, Velasco AL, Trejo-Martínez D, Barragán-Campos HM, Camacho-Téllez V, Concha L (2018) Association of white matter diffusion characteristics and cognitive deficits in temporal lobe epilepsy. Epilepsy Behav 79:138–145. https://doi.org/10.1016/j.yebeh.2017.11.040
doi: 10.1016/j.yebeh.2017.11.040
pubmed: 29287217