Focal cortical dysplasia: Molecular disturbances and clinicopathological classification (Review)
- Authors:
- Monika Siedlecka
- Wiesława Grajkowska
- Ryszard Galus
- Bożenna Dembowska-Bagińska
- Jarosław Jóźwiak
-
Affiliations: Department of Histology and Embryology, Center for Biostructure Research, Medical University of Warsaw, Warsaw, Poland, Department of Pathology, The Childrens' Health Institute, Warsaw, Poland, Department of Oncology, The Childrens' Health Institute, Warsaw, Poland - Published online on: September 29, 2016 https://doi.org/10.3892/ijmm.2016.2760
- Pages: 1327-1337
This article is mentioned in:
Abstract
Bingaman WE: Surgery for focal cortical dysplasia. Neurology. 62(Suppl 3): S30–S34. 2004. View Article : Google Scholar : PubMed/NCBI | |
Taylor DC, Falconer MA, Bruton CJ and Corsellis JA: Focal dysplasia of the cerebral cortex in epilepsy. J Neurol Neurosurg Psychiatry. 34:369–387. 1971. View Article : Google Scholar : PubMed/NCBI | |
Cepeda C, André VM, Levine MS, Salamon N, Miyata H, Vinters HV and Mathern GW: Epileptogenesis in pediatric cortical dysplasia: The dysmature cerebral developmental hypothesis. Epilepsy Behav. 9:219–235. 2006. View Article : Google Scholar : PubMed/NCBI | |
Blümcke I, Thom M, Aronica E, Armstrong DD, Vinters HV, Palmini A, Jacques TS, Avanzini G, Barkovich AJ, Battaglia G, 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. 52:158–174. 2011. View Article : Google Scholar : PubMed/NCBI | |
Coras R, de Boer OJ, Armstrong D, Becker A, Jacques TS, Miyata H, Thom M, Vinters HV, Spreafico R, Oz B, et al: Good interobserver and intraobserver agreement in the evaluation of the new ILAE classification of focal cortical dysplasias. Epilepsia. 53:1341–1348. 2012. View Article : Google Scholar : PubMed/NCBI | |
Crino PB, Miyata H and Vinters HV: Neurodevelopmental disorders as a cause of seizures: Neuropathologic, genetic, and mechanistic considerations. Brain Pathol. 12:212–233. 2002. View Article : Google Scholar : PubMed/NCBI | |
Englund C, Folkerth RD, Born D, Lacy JM and Hevner RF: Aberrant neuronal-glial differentiation in Taylor-type focal cortical dysplasia (type IIA/B). Acta Neuropathol. 109:519–533. 2005. View Article : Google Scholar : PubMed/NCBI | |
Andres M, Andre VM, Nguyen S, Salamon N, Cepeda C, Levine MS, Leite JP, Neder L, Vinters HV and Mathern GW: Human cortical dysplasia and epilepsy: An ontogenetic hypothesis based on volumetric MRI and NeuN neuronal density and size measurements. Cereb Cortex. 15:194–210. 2005. View Article : Google Scholar | |
Rossini L, Medici V, Tassi L, Cardinale F, Tringali G, Bramerio M, Villani F, Spreafico R and Garbelli R: Layer-specific gene expression in epileptogenic type II focal cortical dysplasia: Normal-looking neurons reveal the presence of a hidden laminar organization. Acta Neuropathol Commun. 2:452014. View Article : Google Scholar : PubMed/NCBI | |
Guo W, Zhang CQ, Shu HF, Yang MH, Yin Q and Yang H: Expression of bone morphogenetic protein-4 in the cortical lesions of focal cortical dysplasia IIb and the tuberous sclerosis complex. J Mol Neurosci. 50:7–13. 2013. View Article : Google Scholar | |
Boer K, Lucassen PJ, Spliet WG, Vreugdenhil E, van Rijen PC, Troost D, Jansen FE and Aronica E: Doublecortin-like (DCL) expression in focal cortical dysplasia and cortical tubers. Epilepsia. 50:2629–2637. 2009. View Article : Google Scholar : PubMed/NCBI | |
Guo W, Zheng DH, Sun FJ, Yang JY, Zang ZL, Liu SY, Yin Q, Zhang CQ and Yang H: Expression and cellular distribution of the interleukin 2 signaling system in cortical lesions from patients with focal cortical dysplasia. J Neuropathol Exp Neurol. 73:206–222. 2014. View Article : Google Scholar : PubMed/NCBI | |
Chen J, Tsai V, Parker WE, Aronica E, Baybis M and Crino PB: Detection of human papillomavirus in human focal cortical dysplasia type IIB. Ann Neurol. 72:881–892. 2012. View Article : Google Scholar | |
Liu S, Lu L, Cheng X, Xu G and Yang H: Viral infection and focal cortical dysplasia. Ann Neurol. 75:614–616. 2014. View Article : Google Scholar | |
Buchkovich NJ, Yu Y, Zampieri CA and Alwine JC: The TORrid affairs of viruses: Effects of mammalian DNA viruses on the PI3K-Akt-mTOR signalling pathway. Nat Rev Microbiol. 6:266–275. 2008. View Article : Google Scholar : PubMed/NCBI | |
Shapiro KA, McGuone D, Deshpande V, Sadow PM, Stemmer-Rachamimov A and Staley KJ: Failure to detect human papillomavirus in focal cortical dysplasia type IIb. Ann Neurol. 78:63–67. 2015. View Article : Google Scholar : PubMed/NCBI | |
Becker AJ, Urbach H, Scheffler B, Baden T, Normann S, Lahl R, Pannek HW, Tuxhorn I, Elger CE, Schramm J, et al: Focal cortical dysplasia of Taylor's balloon cell type: Mutational analysis of the TSC1 gene indicates a pathogenic relationship to tuberous sclerosis. Ann Neurol. 52:29–37. 2002. View Article : Google Scholar : PubMed/NCBI | |
Jóźwiak S, Kwiatkowski D, Kotulska K, Larysz-Brysz M, Lewin-Kowalik J, Grajkowska W and Roszkowski M: Tuberin and hamartin expression is reduced in the majority of subependymal giant cell astrocytomas in tuberous sclerosis complex consistent with a two-hit model of pathogenesis. J Child Neurol. 19:102–106. 2004. | |
Schick V, Majores M, Engels G, Hartmann W, Elger CE, Schramm J, Schoch S and Becker AJ: Differential Pi3K-pathway activation in cortical tubers and focal cortical dysplasias with balloon cells. Brain Pathol. 17:165–173. 2007. View Article : Google Scholar : PubMed/NCBI | |
Miyata H, Chiang AC and Vinters HV: Insulin signaling pathways in cortical dysplasia and TSC-tubers: Tissue microarray analysis. Ann Neurol. 56:510–519. 2004. View Article : Google Scholar : PubMed/NCBI | |
Patil VV, Guzman M, Carter AN, Rathore G, Yoshor D, Curry D, Wilfong A, Agadi S, Swann JW, Adesina AM, et al: Activation of extracellular regulated kinase and mechanistic target of rapamycin pathway in focal cortical dysplasia. Neuropathology. 36:146–156. 2016. View Article : Google Scholar | |
Lim JS, Kim WI, Kang HC, Kim SH, Park AH, Park EK, Cho YW, Kim S, Kim HM, Kim JA, et al: Brain somatic mutations in MTOR cause focal cortical dysplasia type II leading to intractable epilepsy. Nat Med. 21:395–400. 2015. View Article : Google Scholar : PubMed/NCBI | |
Cotter D, Honavar M, Lovestone S, Raymond L, Kerwin R, Anderton B and Everall I: Disturbance of Notch-1 and Wnt signalling proteins in neuroglial balloon cells and abnormal large neurons in focal cortical dysplasia in human cortex. Acta Neuropathol. 98:465–472. 1999. View Article : Google Scholar : PubMed/NCBI | |
Lamparello P, Baybis M, Pollard J, Hol EM, Eisenstat DD, Aronica E and Crino PB: Developmental lineage of cell types in cortical dysplasia with balloon cells. Brain. 130:2267–2276. 2007. View Article : Google Scholar : PubMed/NCBI | |
Crino PB, Trojanowski JQ and Eberwine J: Internexin, MAP1B, and nestin in cortical dysplasia as markers of developmental maturity. Acta Neuropathol. 93:619–627. 1997. View Article : Google Scholar : PubMed/NCBI | |
Jozwiak J, Jozwiak S and Wlodarski P: Possible mechanisms of disease development in tuberous sclerosis. Lancet Oncol. 9:73–79. 2008. View Article : Google Scholar : PubMed/NCBI | |
Buccoliero AM, Barba C, Giordano F, Baroni G, Genitori L, Guerrini R and Taddei GL: Expression of glutamine synthetase in balloon cells: A basis of their antiepileptic role? Clin Neuropathol. 34:83–88. 2015. View Article : Google Scholar | |
Cepeda C, Hurst RS, Flores-Hernández J, Hernández-Echeagaray E, Klapstein GJ, Boylan MK, Calvert CR, Jocoy EL, Nguyen OK, André VM, et al: Morphological and electro-physiological characterization of abnormal cell types in pediatric cortical dysplasia. J Neurosci Res. 72:472–486. 2003. View Article : Google Scholar : PubMed/NCBI | |
Cepeda C, André VM, Vinters HV, Levine MS and Mathern GW: Are cytomegalic neurons and balloon cells generators of epileptic activity in pediatric cortical dysplasia? Epilepsia. 46(Suppl 5): 82–88. 2005. View Article : Google Scholar : PubMed/NCBI | |
Cepeda C, André VM, Wu N, Yamazaki I, Uzgil B, Vinters HV, Levine MS and Mathern GW: Immature neurons and GABA networks may contribute to epileptogenesis in pediatric cortical dysplasia. Epilepsia. 48(Suppl 5): 79–85. 2007. View Article : Google Scholar : PubMed/NCBI | |
Calcagnotto ME, Paredes MF, Tihan T, Barbaro NM and Baraban SC: Dysfunction of synaptic inhibition in epilepsy associated with focal cortical dysplasia. J Neurosci. 25:9649–9657. 2005. View Article : Google Scholar : PubMed/NCBI | |
Aronica E, Boer K, Redeker S, Spliet WG, van Rijen PC, Troost D and Gorter JA: Differential expression patterns of chloride transporters, Na+-K+-2Cl− - cotransporter and K+-Cl− - cotransporter, in epilepsy-associated malformations of cortical development. Neuroscience. 145:185–196. 2007. View Article : Google Scholar : PubMed/NCBI | |
Aronica E, Boer K, Doorn KJ, Zurolo E, Spliet WG, van Rijen PC, Baayen JC, Gorter JA and Jeromin A: Expression and localization of voltage dependent potassium channel Kv4.2 in epilepsy associated focal lesions. Neurobiol Dis. 36:81–95. 2009. View Article : Google Scholar : PubMed/NCBI | |
Iyer A, Zurolo E, Spliet WG, van Rijen PC, Baayen JC, Gorter JA and Aronica E: Evaluation of the innate and adaptive immunity in type I and type II focal cortical dysplasias. Epilepsia. 51:1763–1773. 2010. View Article : Google Scholar : PubMed/NCBI | |
Harvey AS, Cross JH, Shinnar S and Mathern GW; ILAE Pediatric Epilepsy Surgery Survey Taskforce: Defining the spectrum of international practice in pediatric epilepsy surgery patients. Epilepsia. 49:146–155. 2008. View Article : Google Scholar | |
Becker AJ, Blümcke I, Urbach H, Hans V and Majores M: Molecular neuropathology of epilepsy-associated glioneuronal malformations. J Neuropathol Exp Neurol. 65:99–108. 2006. View Article : Google Scholar : PubMed/NCBI | |
Spreafico R and Blümcke I: Focal Cortical Dysplasias: Clinical implication of neuropathological classification systems. Acta Neuropathol. 120:359–367. 2010. View Article : Google Scholar : PubMed/NCBI | |
Siegel AM, Cascino GD, Elger CE, Devinsky O, Laff R, Najjar S, Sperling MR, LoRusso G, Cossu M, Urbach H, et al: Adult-onset epilepsy in focal cortical dysplasia of Taylor type. Neurology. 64:1771–1774. 2005. View Article : Google Scholar : PubMed/NCBI | |
Fauser S, Schulze-Bonhage A, Honegger J, Carmona H, Huppertz HJ, Pantazis G, Rona S, Bast T, Strobl K, Steinhoff BJ, et al: Focal cortical dysplasias: Surgical outcome in 67 patients in relation to histological subtypes and dual pathology. Brain. 127:2406–2418. 2004. View Article : Google Scholar : PubMed/NCBI | |
Yao K, Mei X, Liu X, Duan Z, Liu C, Bian Y, Ma Z and Qi X: Clinical characteristics, pathological features and surgical outcomes of focal cortical dysplasia (FCD) type II: Correlation with pathological subtypes. Neurol Sci. 35:1519–1526. 2014. View Article : Google Scholar : PubMed/NCBI | |
Serino D, Freri E, Ragona F, D'Incerti L, Bernardi B, Di Ciommo V, Granata T, Vigevano F and Fusco L: Focal seizures versus epileptic spasms in children with focal cortical dysplasia and epilepsy onset in the first year. Epilepsy Res. 109:203–209. 2015. View Article : Google Scholar | |
Widdess-Walsh P, Kellinghaus C, Jeha L, Kotagal P, Prayson R, Bingaman W and Najm IM: Electro-clinical and imaging characteristics of focal cortical dysplasia: Correlation with pathological subtypes. Epilepsy Res. 67:25–33. 2005. View Article : Google Scholar : PubMed/NCBI | |
Blümcke I: Neuropathology of focal epilepsies: A critical review. Epilepsy Behav. 15:34–39. 2009. View Article : Google Scholar : PubMed/NCBI | |
Cossu M, Fuschillo D, Bramerio M, Galli C, Gozzo F, Pelliccia V, Casaceli G, Tassi L and Lo Russo G: Epilepsy surgery of focal cortical dysplasia-associated tumors. Epilepsia. 54(Suppl 9): 115–122. 2013. View Article : Google Scholar : PubMed/NCBI | |
Krsek P, Pieper T, Karlmeier A, Hildebrandt M, Kolodziejczyk D, Winkler P, Pauli E, Blümcke I and Holthausen H: Different presurgical characteristics and seizure outcomes in children with focal cortical dysplasia type I or II. Epilepsia. 50:125–137. 2009. View Article : Google Scholar | |
Chassoux F, Devaux B, Landré E, Turak B, Nataf F, Varlet P, Chodkiewicz JP and Daumas-Duport C: Stereoelectroencephalography in focal cortical dysplasia: A 3D approach to delineating the dysplastic cortex. Brain. 123:1733–1751. 2000. View Article : Google Scholar : PubMed/NCBI | |
Barkovich AJ, Kuzniecky RI, Bollen AW and Grant PE: Focal transmantle dysplasia: A specific malformation of cortical development. Neurology. 49:1148–1152. 1997. View Article : Google Scholar : PubMed/NCBI | |
Colombo N, Tassi L, Deleo F, Citterio A, Bramerio M, Mai R, Sartori I, Cardinale F, Lo Russo G and Spreafico R: Focal cortical dysplasia type IIa and IIb: MRI aspects in 118 cases proven by histopathology. Neuroradiology. 54:1065–1077. 2012. View Article : Google Scholar : PubMed/NCBI | |
Mühlebner A, Coras R, Kobow K, Feucht M, Czech T, Stefan H, Weigel D, Buchfelder M, Holthausen H, Pieper T, et al: Neuropathologic measurements in focal cortical dysplasias: Validation of the ILAE 2011 classification system and diagnostic implications for MRI. Acta Neuropathol. 123:259–272. 2012. View Article : Google Scholar | |
Wagner J, Weber B, Urbach H, Elger CE and Huppertz HJ: Morphometric MRI analysis improves detection of focal cortical dysplasia type II. Brain. 134:2844–2854. 2011. View Article : Google Scholar : PubMed/NCBI | |
Blauwblomme T, Boddaert N, Chémaly N, Chiron C, Pages M, Varlet P, Bourgeois M, Bahi-Buisson N, Kaminska A, Grevent D, et al: Arterial Spin Labeling MRI: A step forward in non-invasive delineation of focal cortical dysplasia in children. Epilepsy Res. 108:1932–1939. 2014. View Article : Google Scholar : PubMed/NCBI | |
Chan HW, Pressler R, Uff C, Gunny R, St Piers K, Cross H, Bamber J, Dorward N, Harkness W and Chakraborty A: A novel technique of detecting MRI-negative lesion in focal symptomatic epilepsy: Intraoperative ShearWave elastography. Epilepsia. 55:e30–e33. 2014. View Article : Google Scholar : PubMed/NCBI | |
Sisodiya SM, Lin WR, Squier MV and Thom M: Multidrug-resistance protein 1 in focal cortical dysplasia. Lancet. 357:42–43. 2001. View Article : Google Scholar : PubMed/NCBI | |
Aronica E, Gorter JA, Jansen GH, van Veelen CW, van Rijen PC, Leenstra S, Ramkema M, Scheffer GL, Scheper RJ and Troost D: Expression and cellular distribution of multidrug transporter proteins in two major causes of medically intractable epilepsy: Focal cortical dysplasia and glioneuronal tumors. Neuroscience. 118:417–429. 2003. View Article : Google Scholar : PubMed/NCBI | |
Sisodiya SM, Martinian L, Scheffer GL, van der Valk P, Cross JH, Scheper RJ, Harding BN and Thom M: Major vault protein, a marker of drug resistance, is upregulated in refractory epilepsy. Epilepsia. 44:1388–1396. 2003. View Article : Google Scholar : PubMed/NCBI | |
Wong M, Ess KC, Uhlmann EJ, Jansen LA, Li W, Crino PB, Mennerick S, Yamada KA and Gutmann DH: Impaired glial glutamate transport in a mouse tuberous sclerosis epilepsy model. Ann Neurol. 54:251–256. 2003. View Article : Google Scholar : PubMed/NCBI | |
Uhlmann EJ, Wong M, Baldwin RL, Bajenaru ML, Onda H, Kwiatkowski DJ, Yamada K and Gutmann DH: Astrocyte-specific TSC1 conditional knockout mice exhibit abnormal neuronal organization and seizures. Ann Neurol. 52:285–296. 2002. View Article : Google Scholar : PubMed/NCBI | |
Ehninger D, Han S, Shilyansky C, Zhou Y, Li W, Kwiatkowski DJ, Ramesh V and Silva AJ: Reversal of learning deficits in a Tsc2+/− mouse model of tuberous sclerosis. Nat Med. 14:843–848. 2008. View Article : Google Scholar : PubMed/NCBI | |
Krueger DA, Care MM, Holland K, Agricola K, Tudor C, Mangeshkar P, Wilson KA, Byars A, Sahmoud T and Franz DN: Everolimus for subependymal giant-cell astrocytomas in tuberous sclerosis. N Engl J Med. 363:1801–1811. 2010. View Article : Google Scholar : PubMed/NCBI | |
Skirrow C, Cross JH, Cormack F, Harkness W, Vargha-Khadem F and Baldeweg T: Long-term intellectual outcome after temporal lobe surgery in childhood. Neurology. 76:1330–1337. 2011. View Article : Google Scholar : PubMed/NCBI | |
Chen HH, Chen C, Hung SC, Liang SY, Lin SC, Hsu TR, Yeh TC, Yu HY, Lin CF, Hsu SP, et al: Cognitive and epilepsy outcomes after epilepsy surgery caused by focal cortical dysplasia in children: Early intervention maybe better. Childs Nerv Syst. 30:1885–1895. 2014. View Article : Google Scholar : PubMed/NCBI | |
Wagner J, Urbach H, Niehusmann P, von Lehe M, Elger CE and Wellmer J: Focal cortical dysplasia type IIb: Completeness of cortical, not subcortical, resection is necessary for seizure freedom. Epilepsia. 52:1418–1424. 2011. View Article : Google Scholar : PubMed/NCBI | |
Mühlebner A, Gröppel G, Dressler A, Reiter-Fink E, Kasprian G, Prayer D, Dorfer C, Czech T, Hainfellner JA, Coras R, et al: Epilepsy surgery in children and adolescents with malformations of cortical development - outcome and impact of the new ILAE classification on focal cortical dysplasia. Epilepsy Res. 108:1652–1661. 2014. View Article : Google Scholar | |
Kim DW, Lee SK, Chu K, Park KI, Lee SY, Lee CH, Chung CK, Choe G and Kim JY: Predictors of surgical outcome and pathologic considerations in focal cortical dysplasia. Neurology. 72:211–216. 2009. View Article : Google Scholar | |
Mrelashvili A, Witte RJ, Wirrell EC, Nickels KC and Wong-Kisiel LC: Seizure Freedom in Children With Pathology-Confirmed Focal Cortical Dysplasia. Pediatr Neurol. 53:513–518. 2015. View Article : Google Scholar : PubMed/NCBI | |
Jehi L, Yardi R, Chagin K, Tassi L, Russo GL, Worrell G, Hu W, Cendes F, Morita M, Bartolomei F, et al: Development and validation of nomograms to provide individualised predictions of seizure outcomes after epilepsy surgery: A retrospective analysis. Lancet Neurol. 14:283–290. 2015. View Article : Google Scholar : PubMed/NCBI | |
Bulacio JC, Jehi L, Wong C, Gonzalez-Martinez J, Kotagal P, Nair D, Najm I and Bingaman W: Long-term seizure outcome after resective surgery in patients evaluated with intracranial electrodes. Epilepsia. 53:1722–1730. 2012. View Article : Google Scholar : PubMed/NCBI | |
Simasathien T, Vadera S, Najm I, Gupta A, Bingaman W and Jehi L: Improved outcomes with earlier surgery for intractable frontal lobe epilepsy. Ann Neurol. 73:646–654. 2013. View Article : Google Scholar : PubMed/NCBI | |
Ryzí M, Ošlejšková H, Rektor I, Novák Z, Hemza J, Chrastina J, Svoboda M, Hermanová M and Brázdil M: Long-term approach to patients with postsurgical seizures. Epilepsia. 57:597–604. 2016. View Article : Google Scholar : PubMed/NCBI | |
Tassi L, Garbelli R, Colombo N, Bramerio M, Russo GL, Mai R, Deleo F, Francione S, Nobili L and Spreafico R: Electroclinical, MRI and surgical outcomes in 100 epileptic patients with type II FCD. Epileptic Disord. 14:257–266. 2012.PubMed/NCBI | |
Rowland NC, Englot DJ, Cage TA, Sughrue ME, Barbaro NM and Chang EF: A meta-analysis of predictors of seizure freedom in the surgical management of focal cortical dysplasia. J Neurosurg. 116:1035–1041. 2012. View Article : Google Scholar : PubMed/NCBI | |
Fauser S, Essang C, Altenmüller DM, Staack A, Steinhoff BJ, Strobl K, Bast T, Schubert-Bast S, Doostkam S, Zentner J and Schulze-Bonhage A: Is there evidence for clinical differences related to the new classification of temporal lobe cortical dysplasia? Epilepsia. 54:909–917. 2013. View Article : Google Scholar : PubMed/NCBI | |
Giulioni M, Martinoni M and Marucci G: About focal cortical dysplasia (FCD) type IIIa. Epilepsy Res. 108:1955–1957. 2014. View Article : Google Scholar : PubMed/NCBI | |
Giulioni M, Marucci G, Martinoni M, Volpi L, Riguzzi P, Marliani AF, Bisulli F, Tinuper P, Tassinari CA, Michelucci R, et al: Seizure outcome in surgically treated drug-resistant mesial temporal lobe epilepsy based on the recent histopathological classifications. J Neurosurg. 119:37–47. 2013. View Article : Google Scholar : PubMed/NCBI | |
Santos MV, de Oliveira RS and Machado HR: Approach to cortical dysplasia associated with glial and glioneuronal tumors (FCD type IIIb). Childs Nerv Syst. 30:1869–1874. 2014. View Article : Google Scholar : PubMed/NCBI | |
Wu J, Li W, Chen Y, Kang L and Zhao W: Clinical characteristics of 92 patients with temporal lobe focal cortical dysplasia identified by pathological examination. J Clin Neurosci. 21:2170–2174. 2014. View Article : Google Scholar : PubMed/NCBI | |
Fauser S, Essang C, Altenmüller DM, Staack AM, Steinhoff BJ, Strobl K, Bast T, Schubert-Bast S, Stephani U, Wiegand G, et al: Long-term seizure outcome in 211 patients with focal cortical dysplasia. Epilepsia. 56:66–76. 2015. View Article : Google Scholar | |
Tassi L, Garbelli R, Colombo N, Bramerio M, Lo Russo G, Deleo F, Milesi G and Spreafico R: Type I focal cortical dysplasia: Surgical outcome is related to histopathology. Epileptic Disord. 12:181–191. 2010.PubMed/NCBI | |
Tassi L, Meroni A, Deleo F, Villani F, Mai R, Russo GL, Colombo N, Avanzini G, Falcone C, Bramerio M, et al: Temporal lobe epilepsy: Neuropathological and clinical correlations in 243 surgically treated patients. Epileptic Disord. 11:281–292. 2009.PubMed/NCBI | |
Thom M, Eriksson S, Martinian L, Caboclo LO, McEvoy AW, Duncan JS and Sisodiya SM: Temporal lobe sclerosis associated with hippocampal sclerosis in temporal lobe epilepsy: Neuropathological features. J Neuropathol Exp Neurol. 68:928–938. 2009. View Article : Google Scholar : PubMed/NCBI | |
Johnson AM, Sugo E, Barreto D, Cunningham AM, Hiew CC, Lawson JA, Somerville ER, Connolly AM and Bye AM: Clinicopathological associations in temporal lobe epilepsy patients utilising the current ILAE focal cortical dysplasia classification. Epilepsy Res. 108:1345–1351. 2014. View Article : Google Scholar : PubMed/NCBI | |
Simpson SL and Prayson RA: Post-surgical outcome for epilepsy associated with type I focal cortical dysplasia subtypes. Mod Pathol. 27:1455–1460. 2014. View Article : Google Scholar : PubMed/NCBI | |
Yagishita A and Arai N: Cortical tubers without other stigmata of tuberous sclerosis: Imaging and pathological findings. Neuroradiology. 41:428–432. 1999. View Article : Google Scholar : PubMed/NCBI | |
Jozwiak J, Kotulska K and Jozwiak S: Similarity of balloon cells in focal cortical dysplasia to giant cells in tuberous sclerosis. Epilepsia. 47:8052006. View Article : Google Scholar : PubMed/NCBI | |
Hyman MH and Whittemore VH: National Institutes of Health consensus conference: Tuberous sclerosis complex. Arch Neurol. 57:662–665. 2000. View Article : Google Scholar : PubMed/NCBI | |
Jozwiak J, Jozwiak S and Skopinski P: Immunohistochemical and microscopic studies on giant cells in tuberous sclerosis. Histol Histopathol. 20:1321–1326. 2005.PubMed/NCBI | |
Oh HS, Lee MC, Kim HS, Lee JS, Lee JH, Kim MK, Woo YJ, Kim JH, Kim HI and Kim SU: Pathophysiologic characteristics of balloon cells in cortical dysplasia. Childs Nerv Syst. 24:175–183. 2008. View Article : Google Scholar | |
Lazarowski A, Lubieniecki F, Camarero S, Pomata H, Bartuluchi M, Sevlever G and Taratuto AL: Multidrug resistance proteins in tuberous sclerosis and refractory epilepsy. Pediatr Neurol. 30:102–106. 2004. View Article : Google Scholar : PubMed/NCBI | |
Lugnier C, Majores M, Fassunke J, Pernhorst K, Niehusmann P, Simon M, Nellist M, Schoch S and Becker A: Hamartin variants that are frequent in focal dysplasias and cortical tubers have reduced tuberin binding and aberrant subcellular distribution in vitro. J Neuropathol Exp Neurol. 68:1136–1146. 2009. View Article : Google Scholar : PubMed/NCBI | |
Iyer A, Prabowo A, Anink J, Spliet WG, van Rijen PC and Aronica E: Cell injury and premature neurodegeneration in focal malformations of cortical development. Brain Pathol. 24:1–17. 2014. View Article : Google Scholar | |
McMahon J, Huang X, Yang J, Komatsu M, Yue Z, Qian J, Zhu X and Huang Y: Impaired autophagy in neurons after disinhibition of mammalian target of rapamycin and its contribution to epileptogenesis. J Neurosci. 32:15704–15714. 2012. View Article : Google Scholar : PubMed/NCBI | |
Yasin SA, Ali AM, Tata M, Picker SR, Anderson GW, Latimer-Bowman E, Nicholson SL, Harkness W, Cross JH, Paine SM and Jacques TS: mTOR-dependent abnormalities in autophagy characterize human malformations of cortical development: Evidence from focal cortical dysplasia and tuberous sclerosis. Acta Neuropathol. 126:207–218. 2013. View Article : Google Scholar : PubMed/NCBI | |
Lee CH, Inoki K and Guan KL: mTOR pathway as a target in tissue hypertrophy. Annu Rev Pharmacol Toxicol. 47:443–467. 2007. View Article : Google Scholar | |
Kotulska K, Jurkiewicz E, Domańska-Pakieła D, Grajkowska W, Mandera M, Borkowska J and Jóźwiak S: Epilepsy in newborns with tuberous sclerosis complex. Eur J Paediatr Neurol. 18:714–721. 2014. View Article : Google Scholar : PubMed/NCBI |