Purpose. The main purpose is to define more accurately the epileptogenic zone (EZ) with noninvasive methods in those patients with MRI diagnosis of focal cortical dysplasia (FCD) and epilepsy who are candidates of epilepsy surgery. Methods. Twenty patients were evaluated prospectively between 2007 and 2010 with comprehensive clinical evaluation, video-electroencephalography, diffusion tensor imaging (DTI), and high-resolution EEG to localize the equivalent current dipole (ECD). Key Findings. In 11 cases with white matter asymmetries in DTI the ECDs were located next to lesion on MRI with mean distance of 14.63？millimeters with topographical correlation with the EZ. Significance. We could establish a hypothesis of EZ based on Video-EEG, high-resolution EEG, ECD method, MRI, and DTI. These results are consistent with the hypothesis that the EZ in the FCD is complex and is often larger than visible lesion in MRI. 1. Introduction Drug-resistant epilepsy is associated with malformations of cortical development (MCD) in 15–20% of adult cases and in more than 50% of pediatric patients [1–3]. MCD are a heterogeneous group of focal and diffuse anatomical derangements whose pathological features depend largely on the timing of the defect in the developmental process and to a lesser extent on its cause [4, 5]. Focal cortical dysplasia (FCD) is the most frequent type of MCD. Taylor et al. (1971) were the first to describe them as focal anomalies of cortical structure [6]. Numerous classifications of FCD have been proposed; a consensus clinic-pathological classification has been recently published [7]. However, it is widely recognized that existing classifications are unsatisfactory to define a prognosis [8, 9]. Furthermore, the etiology of these abnormalities is often uncertain and the mechanisms generating epilepsy are also unclear [10]. Several studies reported that FCD are intrinsically epileptogenic and most patients often present drug resistant epilepsy [11–16]. Some authors described the epileptogenic zone (EZ) as focal [17], while others suggest a more complex network extending beyond the lesion, an “epileptogenic network” [18]. Resective surgery is frequently a promising therapy in this population. However, the outcome following surgical treatment of these patients has been less successful than in other pathologies such as hippocampal sclerosis, even if the entire magnetic resonance images (MRIs) visible lesion is removed [19]. The surgical failure in these patients may be due to the difficulty in defining the epileptogenic zone, which can be more extensive
References
[1]
A. A. Raymond, D. R. Fish, S. M. Sisodiya, N. Alsanjari, J. M. Stevens, and S. D. Shorvon, “Abnormalities of gyration, heterotopias, tuberous sclerosis, focal cortical dysplasia, microdysgenesis, dysembryoplastic neuroepithelial tumour and dysgenesis of the archicortex in epilepsy. Clinical, EEG and neuroimaging features in 100 adult patients,” Brain, vol. 118, no. 3, pp. 629–660, 1995.
[2]
R. Kuzniecky, A. Murro, D. King et al., “Magnetic resonance imaging in childhood intractable partial epilepsies: pathologic correlations,” Neurology, vol. 43, no. 4, pp. 681–687, 1993.
[3]
A. J. Barkovich, R. I. Kuzniecky, G. D. Jackson, R. Guerrini, and W. B. Dobyns, “A developmental and genetic classification for malformations of cortical development,” Neurology, vol. 65, no. 12, pp. 1873–1887, 2005.
[4]
M. Marín-Padilla, “Developmental neuropathology and impact of perinatal brain damage. III: gray matter lesions of the neocortex,” Journal of Neuropathology and Experimental Neurology, vol. 58, no. 5, pp. 407–429, 1999.
[5]
P. Krsek, T. Pieper, A. Karlmeier et al., “Different presurgical characteristics and seizure outcomes in children with focal cortical dysplasia type I or II,” Epilepsia, vol. 50, no. 1, pp. 125–137, 2009.
[6]
D. C. Taylor, M. A. Falconer, C. J. Bruton, and J. A. Corsellis, “Focal dysplasia of the cerebral cortex in epilepsy,” Journal of Neurology Neurosurgery and Psychiatry, vol. 34, no. 4, pp. 369–387, 1971.
[7]
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, vol. 52, no. 1, pp. 158–174, 2011.
[8]
A. Palmini, I. Najm, G. Avanzini et al., “Terminology and classification of the cortical dysplasias,” Neurology, vol. 62, supplement 1, no. 6, pp. S2–S8, 2004.
[9]
R. Spreafico and I. Blümcke, “Focal Cortical Dysplasias: clinical implication of neuropathological classification systems,” Acta Neuropathologica, vol. 120, no. 3, pp. 359–367, 2010.
[10]
C. Cepeda, V. M. André, M. S. Levine et al., “Epileptogenesis in pediatric cortical dysplasia: the dysmature cerebral developmental hypothesis,” Epilepsy and Behavior, vol. 9, no. 2, pp. 219–235, 2006.
[11]
D. Mattia, A. Olivier, and M. Avoli, “Seizure-like discharges recorded in human dysplastic neocortex maintained in vitro,” Neurology, vol. 45, no. 7, pp. 1391–1395, 1995.
[12]
T. Morioka, S. Nishio, H. Ishibashi et al., “Intrinsic epileptogenicity of focal cortical dysplasia as revealed by magnetoencephalography and electrocorticography,” Epilepsy Research, vol. 33, no. 2-3, pp. 177–187, 1999.
[13]
T. Bast, O. Oezkan, S. Rona et al., “EEG and MEG source analysis of single and averaged interictal spikes reveals intrinsic epileptogenicity in focal cortical dysplasia,” Epilepsia, vol. 45, no. 6, pp. 621–631, 2004.
[14]
E. Widjaja, H. Otsubo, C. Raybaud et al., “Characteristics of MEG and MRI between Taylor's focal cortical dysplasia (type II) and other cortical dysplasia: surgical outcome after complete resection of MEG spike source and MR lesion in pediatric cortical dysplasia,” Epilepsy Research, vol. 82, no. 2-3, pp. 147–155, 2008.
[15]
A. Palmini, A. Gambardella, F. Andermann et al., “Intrinsic epileptogenicity of human dysplastic cortex as suggested by corticography and surgical results,” Annals of Neurology, vol. 37, no. 4, pp. 476–487, 1995.
[16]
A. Palmini, “Electrophysiology of the focal cortical dysplasias,” Epilepsia, vol. 51, supplement 1, pp. 23–26, 2010.
[17]
F. Chassoux, B. Devaux, E. Landré et al., “Stereoelectroencephalography in focal cortical dysplasia. A 3D approach to delineating the dysplastic cortex,” Brain, vol. 123, no. 8, pp. 1733–1751, 2000.
[18]
S. Aubert, F. Wendling, J. Regis et al., “Local and remote epileptogenicity in focal cortical dysplasias and neurodevelopmental tumours,” Brain, vol. 132, no. 11, pp. 3072–3086, 2009.
[19]
J. T. Lerner, N. Salamon, J. S. Hauptman et al., “Assessment and surgical outcomes for mild type i and severe type II cortical dysplasia: a critical review and the UCLA experience,” Epilepsia, vol. 50, no. 6, pp. 1310–1335, 2009.
[20]
P. Widdess-Walsh, B. Diehl, and I. Najm, “Neuroimaging of focal cortical dysplasia,” Journal of Neuroimaging, vol. 16, no. 3, pp. 185–196, 2006.
[21]
H. O. Lüders, I. Najm, D. Nair, P. Widdess-Walsh, and W. Bingman, “The epileptogenic zone: general principles,” Epileptic Disorders, vol. 8, supplement 2, pp. S1–S9, 2006.
[22]
P. Chauvel, et al., “The "epileptogenic zone" in humans: representation of intercritical events by spatio-temporal maps,” Revista de Neurología, vol. 143, no. 5, pp. 443–450, 1987.
[23]
F. Rosenow and H. Lüders, “Presurgical evaluation of epilepsy,” Brain, vol. 124, no. 9, pp. 1683–1700, 2001.
[24]
J. S. Ebersole, “Defining epileptogenic foci: past, present, future,” Journal of Clinical Neurophysiology, vol. 14, no. 6, pp. 470–483, 1997.
[25]
K. Radhakrishnan, “Challenges in the management of epilepsy in resource-poor countries,” Nature Reviews Neurology, vol. 5, no. 6, pp. 323–330, 2009.
[26]
C. M. Michel, M. M. Murray, G. Lantz, S. Gonzalez, L. Spinelli, and R. Grave De Peralta, “EEG source imaging,” Clinical Neurophysiology, vol. 115, no. 10, pp. 2195–2222, 2004.
[27]
J. S. Ebersole and S. Hawes-Ebersole, “Clinical application of dipole models in the localization of epileptiform activity,” Journal of Clinical Neurophysiology, vol. 24, no. 2, pp. 120–129, 2007.
[28]
C. Plummer, A. S. Harvey, and M. Cook, “EEG source localization in focal epilepsy: where are we now?” Epilepsia, vol. 49, no. 2, pp. 201–218, 2008.
[29]
M. Gavaret, A. Trébuchon, F. Bartolomei et al., “Source localization of scalp-EEG interictal spikes in posterior cortex epilepsies investigated by HR-EEG and SEEG,” Epilepsia, vol. 50, no. 2, pp. 276–289, 2009.
[30]
H. Otsubo, A. Ochi, I. Elliott et al., “MEG predicts epileptic zone in lesional extrahippocampal epilepsy: 12 Pediatric surgery cases,” Epilepsia, vol. 42, no. 12, pp. 1523–1530, 2001.
[31]
R. Ramachandrannair, H. Otsubo, M. M. Shroff et al., “MEG predicts outcome following surgery for intractable epilepsy in children with normal or nonfocal MRI findings,” Epilepsia, vol. 48, no. 1, pp. 149–157, 2007.
[32]
A. James Barkovich and R. I. Kuzniecky, “Neuroimaging of focal malformations of cortical development,” Journal of Clinical Neurophysiology, vol. 13, no. 6, pp. 481–494, 1996.
[33]
A. J. Barkovich, R. I. Kuzniecky, A. W. Bollen, and P. E. Grant, “Focal transmantle dysplasia: a specific malformation of cortical development,” Neurology, vol. 49, no. 4, pp. 1148–1152, 1997.
[34]
P. Kwan, A. Arzimanoglou, A. T. Berg et al., “Definition of drug resistant epilepsy: consensus proposal by the ad hoc Task Force of the ILAE Commission on Therapeutic Strategies,” Epilepsia, vol. 51, no. 6, pp. 1069–1077, 2010.
[35]
W. T. Blume, H. O. Lüders, E. Mizrahi, C. Tassinari, W. Van Emde Boas, and J. Engel, “Glossary of descriptive terminology for ictal semiology: report of the ILAE Task Force on classification and terminology,” Epilepsia, vol. 42, no. 9, pp. 1212–1218, 2001.
[36]
A. D. de la Roque, C. Oppenheim, F. Chassoux et al., “Diffusion tensor imaging of partial intractable epilepsy,” European Radiology, vol. 15, no. 2, pp. 279–285, 2005.
[37]
N. Colombo, N. Salamon, C. Raybaud, ？. ？zkara, and A. J. Barkovich, “Imaging of malformations of cortical development,” Epileptic Disorders, vol. 11, no. 3, pp. 194–205, 2009.
[38]
“A glossary of terms most commonly used by clinical electroencephalographers,” Electroencephalography and Clinical Neurophysiology, vol. 37, no. 5, pp. 538–48, 1974.
[39]
C. C. Lim, H. Yin, N. K. Loh, V. G. E. Chua, F. Hui, and A. J. Barkovich, “Malformations of cortical development: high-resolution MR and diffusion tensor imaging of fiber tracts at 3T,” American Journal of Neuroradiology, vol. 26, no. 1, pp. 61–64, 2005.
[40]
S. K. Lee, D. I. Kim, S. Mori et al., “Diffusion tensor MRI visualizes decreased subcortical fiber connectivity in focal cortical dysplasia,” NeuroImage, vol. 22, no. 4, pp. 1826–1829, 2004.
[41]
E. Widjaja, G. Simao, S. Z. Mahmoodabadi et al., “Diffusion tensor imaging identifies changes in normal-appearing white matter within the epileptogenic zone in tuberous sclerosis complex,” Epilepsy Research, vol. 89, no. 2-3, pp. 246–253, 2010.
[42]
S. H. Eriksson, F. J. Rugg-Gunn, M. R. Symms, G. J. Barker, and J. S. Duncan, “Diffusion tensor imaging in patients with epilepsy and malformations of cortical development,” Brain, vol. 124, no. 3, pp. 617–626, 2001.
[43]
E. Wyllie, “Surgical treatment of epilepsy in children,” Pediatric Neurology, vol. 19, no. 3, pp. 179–188, 1998.
[44]
F. Andermann, “Cortical dysplasias and epilepsy: a review of the architectonic, clinical, and seizure patterns,” Advances in neurology, vol. 84, pp. 479–496, 2000.
[45]
N. Colombo, L. Tassi, C. Galli et al., “Focal cortical dysplasias: MR imaging, histopathologic, and clinical correlations in surgically treated patients with epilepsy,” American Journal of Neuroradiology, vol. 24, no. 4, pp. 724–733, 2003.
[46]
J. A. French, “Refractory epilepsy: clinical overview,” Epilepsia, vol. 48, supplement 1, pp. 3–7, 2007.
[47]
H. Otsubo, P. A. Hwang, V. Jay et al., “Focal cortical dysplasia in children with localization-related epilepsy: EEG, MRI, and SPECT findings,” Pediatric Neurology, vol. 9, no. 2, pp. 101–107, 1993.
[48]
S. Fauser, H. J. Huppertz, T. Bast et al., “Clinical characteristics in focal cortical dysplasia: a retrospective evaluation in a series of 120 patients,” Brain, vol. 129, no. 7, pp. 1907–1916, 2006.
[49]
J. F. Bautista, N. Foldvary-Schaefer, W. E. Bingaman, and H. O. Lüders, “Focal cortical dysplasia and intractable epilepsy in adults: clinical, EEG, imaging, and surgical features,” Epilepsy Research, vol. 55, no. 1-2, pp. 131–136, 2003.
[50]
A. Gambardella, A. Palmini, F. Andermann et al., “Usefulness of focal rhythmic discharges on scalp EEG of patients with focal cortical dysplasia and intractable epilepsy,” Electroencephalography and Clinical Neurophysiology, vol. 98, no. 4, pp. 243–249, 1996.
[51]
R. E. Bautista, M. A. Cobbs, D. D. Spencer, and S. S. Spencer, “Prediction of surgical outcome by interictal epileptiform abnormalities during intracranial EEG monitoring in patients with extrahippocampal seizures,” Epilepsia, vol. 40, no. 7, pp. 880–890, 1999.
[52]
A. Rassi-Neto, F. P. Ferraz, C. R. Campos, and F. M. Braga, “Patients with epileptic seizures and cerebral lesions who underwent lesionectomy restricted to or associated with the adjacent irritative area,” Epilepsia, vol. 40, no. 7, pp. 856–864, 1999.
[53]
S. Vulliemoz, L. Lemieux, J. Daunizeau, C. M. Michel, and J. S. Duncan, “The combination of EEG source imaging and EEG-correlated functional MRI to map epileptic networks,” Epilepsia, vol. 51, no. 4, pp. 491–505, 2010.
[54]
M. Wong, “Mechanisms of epileptogenesis in tuberous sclerosis complex and related malformations of cortical development with abnormal glioneuronal proliferation,” Epilepsia, vol. 49, no. 1, pp. 8–21, 2008.
[55]
G. W. Mathern, M. Andres, N. Salamon et al., “A hypothesis regarding the pathogenesis and epileptogenesis of pediatric cortical dysplasia and hemimegalencephaly based on MRI cerebral volumes and NeuN cortical cell densities,” Epilepsia, vol. 48, supplement 5, pp. 74–78, 2007.
[56]
F. Rosenow, H. O. Lüders, D. S. Dinner et al., “Histopathological correlates of epileptogenicity as expressed by electrocorticographic spiking and seizure frequency,” Epilepsia, vol. 39, no. 8, pp. 850–856, 1998.
[57]
K. Boonyapisit, I. Najm, G. Klem et al., “Epileptogenicity of focal malformations due to abnormal cortical development: direct electrocorticographic-histopathologic correlations,” Epilepsia, vol. 44, no. 1, pp. 69–76, 2003.
[58]
C. Cepeda, V. M. André, N. Wu et al., “Immature neurons and GABA networks may contribute to epileptogenesis in pediatric cortical dysplasia,” Epilepsia, vol. 48, supplement 5, pp. 79–85, 2007.
[59]
S. Francione, L. Nobili, F. Cardinale, A. Citterio, C. Galli, and L. Tassi, “Intra-lesional stereo-EEG activity in Taylor's focal cortical dysplasia,” Epileptic Disorders, vol. 5, supplement 2, pp. S105–S114, 2003.
[60]
L. Tassi, N. Colombo, R. Garbelli et al., “Focal cortical dysplasia: neuropathological subtypes, EEG, neuroimaging and surgical outcome,” Brain, vol. 125, no. 8, pp. 1719–1732, 2002.
[61]
L. Tassi, R. Garbelli, N. Colombo et al., “Type I focal cortical dysplasia: surgical outcome is related to histopathology,” Epileptic Disorders, vol. 12, no. 3, pp. 181–191, 2010.
[62]
E. Wyllie, Y. G. Comair, P. Kotagal, J. Bulacio, W. Bingaman, and P. Ruggieri, “Seizure outcome after epilepsy surgery in children and adolescents,” Annals of Neurology, vol. 44, no. 5, pp. 740–748, 1998.
[63]
J. D. Jirsch, E. Urrestarazu, P. LeVan, A. Olivier, F. Dubeau, and J. Gotman, “High-frequency oscillations during human focal seizures,” Brain, vol. 129, no. 6, pp. 1593–1608, 2006.
[64]
S. M. Sisodiya, “Surgery for malformations of cortical development causing epilepsy,” Brain, vol. 123, no. 6, pp. 1075–1091, 2000.
[65]
S. M. Sisodiya, “Surgery for focal cortical dysplasia,” Brain, vol. 127, no. 11, pp. 2383–2384, 2004.
[66]
E. Bertram, “The relevance of kindling for human epilepsy,” Epilepsia, vol. 48, supplement 2, pp. 65–74, 2007.
[67]
W. W. Sutherling, M. F. Levesque, P. H. Crandall, and D. S. Barth, “Localization of partial epilepsy using magnetic and electric measurements,” Epilepsia, vol. 32, supplement 5, pp. S29–S40, 1991.
[68]
P. J. Basser and D. K. Jones, “Diffusion-tensor MRI: theory, experimental design and data analysis—a technical review,” NMR in Biomedicine, vol. 15, no. 7-8, pp. 456–467, 2002.
[69]
D. W. Gross, A. Bastos, and C. Beaulieu, “Diffusion tensor imaging abnormalities in focal cortical dysplasia,” Canadian Journal of Neurological Sciences, vol. 32, no. 4, pp. 477–482, 2005.
[70]
B. Diehl, J. Tkach, Z. Piao et al., “Diffusion tensor imaging in patients with focal epilepsy due to cortical dysplasia in the temporo-occipital region: electro-clinico-pathological correlations,” Epilepsy Research, vol. 90, no. 3, pp. 178–187, 2010.
[71]
E. Widjaja, S. Z. Mahmoodabadi, H. Otsubo et al., “Subcortical alterations in tissue microstructure adjacent to focal cortical dysplasia: detection at diffusion-tensor MR imaging by using magnetoencephalographic dipole cluster localization,” Radiology, vol. 251, no. 1, pp. 206–215, 2009.
