Epilepsies associated with hippocampal sclerosis

Hippocampal sclerosis (HS) is considered the most frequent neuropathological finding in patients with mesial temporal lobe epilepsy (MTLE). Hippocampal specimens of pharmacoresistant MTLE patients that underwent epilepsy surgery for seizure control reveal the characteristic pattern of segmental neuronal cell loss and concomitant astrogliosis. However, classification issues of hippocampal lesion patterns have been a matter of intense debate. International consensus classification has only recently provided significant progress for comparisons of neurosurgical and clinic-pathological series between different centers. The respective four-tiered classification system of the International League Against Epilepsy subdivides HS into three types and includes a term of "gliosis only, no-HS". Future studies will be necessary to investigate whether each of these subtypes of HS may be related to different etiological factors or with postoperative memory and seizure outcome. Molecular studies have provided potential deeper insights into the pathogenesis of HS and MTLE on the basis of epilepsy-surgical hippocampal specimens and corresponding animal models. These include channelopathies, activation of NMDA receptors, and other conditions related to Ca2+ influx into neurons, the imbalance of Ca2+-binding proteins, acquired channelopathies that increase neuronal excitability, paraneoplastic and non-paraneoplastic inflammatory events, and epigenetic regulation promoting or facilitating hippocampal epileptogenesis. Genetic predisposition for HS is clearly suggested by the high incidence of family history in patients with HS, and by familial MTLE with HS. So far, it is clear that HS is multifactorial and there is no individual pathogenic factor either necessary or sufficient to generate this intriguing histopathological condition. The obvious variety of pathogenetic combinations underlying HS may explain the multitude of clinical presentations, different responses to clinical and surgical treatment. We believe that the stratification of neuropathological patterns can help to characterize specific clinic-pathological entities and predict the postsurgical seizure control in an improved fashion. © 2014 Springer-Verlag.Hippocampal sclerosis (HS) is considered the most frequent neuropathological finding in patients with mesial temporal lobe epilepsy (MTLE). Hippocampal specimens of pharmacoresistant MTLE patients that underwent epilepsy surgery for seizure control reveal12812137FAPESP - FUNDAÇÃO DE AMPARO À PESQUISA DO ESTADO DE SÃO PAULO2013/07559-3Andrade-Valenca, L.P.A., Valenca, M.M., Velasco, T.R., Carlotti Jr., C.G., Assirati, J.A., Galvis-Alonso, O.Y., Neder, L., Leite, J.P., Mesial temporal lobe epilepsy: Clinical and neuropathologic findings of familial and sporadic forms (2008) Epilepsia, 49 (6), pp. 1046-1054. , DOI 10.1111/j.1528-1167.2008.01551.xAptel, H., Hilaire, C., Pieraut, S., Boukhaddaoui, H., Mallie, S., Valmier, J., Scamps, F., The Cav3.2/alpha1H T-type Ca2+ current is a molecular determinant of excitatory effects of GABA in adult sensory neurons (2007) Molecular and Cellular Neuroscience, 36 (2), pp. 293-303. , DOI 10.1016/j.mcn.2007.07.009, PII S1044743107001716Arai, N., Umitsu, R., Komori, T., Hayashi, M., Kurata, K., Nagata, J., Tamagawa, K., Morimatsu, Y., Peculiar form of cerebral microdysgenesis characterized by white matter neurons with perineuronal and perivascular glial satellitosis: A study using a variety of human autopsied brains (2003) Pathology International, 53 (6), pp. 345-352. , DOI 10.1046/j.1440-1827.2003.01480.xArruda, F., Cendes, F., Andermann, F., Dubeau, F., Villemure, J.G., Jones-Gotman, M., Poulin, N., Olivier, A., Mesial atrophy and outcome after amygdalohippocampectomy or temporal lobe removal (1996) Annals of Neurology, 40 (3), pp. 446-450Barba, C., Barbati, G., Minotti, L., Hoffmann, D., Kahane, P., Ictal clinical and scalp-EEG findings differentiating temporal lobe epilepsies from temporal 'plus' epilepsies (2007) Brain, 130 (7), pp. 1957-1967. , DOI 10.1093/brain/awm108Bartolomei, F., Cosandier-Rimele, D., McGonigal, A., Aubert, S., Regis, J., Gavaret, M., Wendling, F., Chauvel, P., From mesial temporal lobe to temporoperisylvian seizures: A quantified study of temporal lobe seizure networks (2010) Epilepsia, 51 (10), pp. 2147-2158Becker, A.J., Pitsch, J., Sochivko, D., Opitz, T., Staniek, M., Chen, C.C., Campbell, K.P., Beck, H., Transcriptional upregulation of Cav3.2 mediates epileptogenesis in the pilocarpine model of epilepsy (2008) J Neurosci, 28 (49), pp. 13341-13353Bell, B., Lin, J.J., Seidenberg, M., Hermann, B., The neurobiology of cognitive disorders in temporal lobe epilepsy (2011) Nat Rev Neurol, 7 (3), pp. 154-164Ben-Ari, Y., Tremblay, E., Riche, D., Electrographic, clinical and pathological alterations following systemic administration of kainic acid, bicuculline or pentetrazole: Metabolic mapping using the deoxyglucose method with special reference to the pathology of epilepsy (1981) Neuroscience, 6 (7), pp. 1361-1391. , DOI 10.1016/0306-4522(81)90193-7Berg, A.T., Berkovic, S.F., Brodie, M.J., Buchhalter, J., Cross, J.H., Van Boas, W.E., Engel, J., Scheffer, I.E., Revised terminology and concepts for organization of seizures and epilepsies: Report of the ILAE Commission on Classification and Terminology, 2005-2009 (2010) Epilepsia, 51 (4), pp. 676-685Berg, A.T., Langfitt, J., Shinnar, S., Vickrey, B.G., Sperling, M.R., Walczak, T., Bazil, C., Spencer, S.S., How long does it take for partial epilepsy to become intractable? (2003) Neurology, 60 (2), pp. 186-190Berkovic, S.F., Howell, R.A., Hopper, J.L., Familial temporal lobe epilepsy: A new syndrome with adolescent/adult onset and a benign course (1994) Epileptic Seizures and Syndromes, pp. 259-265. , Wolf P (ed) John Libbey, LondonBerkovic, S.F., McIntosh, A., Anne, H.R., Mitchell, A., Sheffield, L.J., Hopper, J.L., Familial temporal lobe epilepsy: A common disorder identified in twins (1996) Annals of Neurology, 40 (2), pp. 227-235Berkovic, S.F., Scheffer, I.E., Febrile seizures: Genetics and relationship to other epilepsy syndromes (1998) Current Opinion in Neurology, 11 (2), pp. 129-134. , DOI 10.1097/00019052-199804000-00009Bernard, C., Anderson, A., Becker, A., Poolos, N.P., Deck, H., Johnston, D., Acquired dendritic channelopathy in temporal lobe epilepsy (2004) Science, 305 (5683), pp. 532-535. , DOI 10.1126/science.1097065Bernasconi, A., Andermann, F., Cendes, F., Dubeau, F., Andermann, E., Olivier, A., Nocturnal temporal lobe epilepsy (1998) Neurology, 50 (6), pp. 1772-1777Bien, C.G., Urbach, H., Schramm, J., Soeder, B.M., Becker, A.J., Voltz, R., Vincent, A., Elger, C.E., Limbic encephalitis as a precipitating event in adult-onset temporal lobe epilepsy (2007) Neurology, 69 (12), pp. 1236-1244. , DOI 10.1212/01.wnl.0000276946.08412.ef, PII 0000611420070918000009Bien, C.G., Vincent, A., Barnett, M.H., Becker, A.J., Blumcke, I., Graus, F., Jellinger, K.A., Bauer, J., Immunopathology of autoantibody-associated encephalitides: Clues for pathogenesis (2012) Brain, 135 (PART 5), pp. 1622-1638Bilevicius, E., Yasuda, C.L., Silva, M.S., Guerreiro, C.A., Lopes-Cendes, I., Cendes, F., Antiepileptic drug response in temporal lobe epilepsy: A clinical and MRI morphometry study (2010) Neurology, 75 (19), pp. 1695-1701Blumcke, I., Becker, A.J., Klein, C., Scheiwe, C., Lie, A.A., Beck, H., Waha, A., Wiestler, O.D., Temporal lobe epilepsy associated up-regulation of metabotropic glutamate receptors: Correlated changes in mGluR1 mRNA and protein expression in experimental animals and human patients (2000) Journal of Neuropathology and Experimental Neurology, 59 (1), pp. 1-10Blumcke, I., Coras, R., Miyata, H., Ozkara, C., Defining clinico-neuropathological subtypes of mesial temporal lobe epilepsy with hippocampal sclerosis (2012) Brain Pathol, 22 (3), pp. 402-411Blumcke, I., Cross, J.H., Spreafico, R., The international consensus classification for hippocampal sclerosis: An important step towards accurate prognosis (2013) Lancet Neurol, 12 (9), pp. 844-846Blumcke, I., Kistner, I., Clusmann, H., Schramm, J., Becker, A.J., Elger, C.E., Bien, C.G., Hildebrandt, M., Towards a clinico-pathological classification of granule cell dispersion in human mesial temporal lobe epilepsies (2009) Acta Neuropathol, 117 (5), pp. 535-544Blumcke, I., Pauli, E., Clusmann, H., Schramm, J., Becker, A., Elger, C., Merschhemke, M., Hildebrandt, M., A new clinico-pathological classification system for mesial temporal sclerosis (2007) Acta Neuropathologica, 113 (3), pp. 235-244. , DOI 10.1007/s00401-006-0187-0Blumcke, I., Thom, M., Aronica, E., Armstrong, D.D., Bartolomei, F., Bernasconi, A., Bernasconi, N., Spreafico, R., International consensus classification of hippocampal sclerosis in temporal lobe epilepsy: A task force report from the ILAE commission on diagnostic methods (2013) Epilepsia, 54 (7), pp. 1315-1329Blumcke, I., Thom, M., Aronica, E., Armstrong, D.D., Vinters, H.V., Palmini, A., Jacques, T.S., Spreafico, R., The clinicopathologic spectrum of focal cortical dysplasias: A consensus classification proposed by an ad hoc task force of the ilae diagnostic methods commission (2011) Epilepsia, 52 (1), pp. 158-174Blumcke, I., Thom, M., Wiestler, O.D., Ammon's horn sclerosis: A maldevelopmental disorder associated with temporal lobe epilepsy (2002) Brain Pathology, 12 (2), pp. 199-211Bonilha, L., Yasuda, C.L., Rorden, C., Li, L.M., Tedeschi, H., De Oliveira, E., Cendes, F., Does resection of the medial temporal lobe improve the outcome of temporal lobe epilepsy surgery? (2007) Epilepsia, 48 (3), pp. 571-578. , DOI 10.1111/j.1528-1167.2006.00958.xBouchet, C., Cazauvieilh, J.B., De l'épilepsie considéré dans ses rapports avec l'aliénation mentale (1825) Arch Gen Med, 9, pp. 510-542Brewster, A., Bender, R.A., Chen, Y., Dube, C., Eghbal-Ahmadi, M., Baram, T.Z., Developmental Febrile Seizures Modulate Hippocampal Gene Expression of Hyperpolarization-Activated Channels in an Isoform- and Cell-Specific Manner (2002) Journal of Neuroscience, 22 (11), pp. 4591-4599Brockhaus, A., Elger, C.E., Complex partial seizures of temporal lobe origin in children of different age groups (1995) Epilepsia, 36 (12), pp. 1173-1181Brooks-Kayal, A.R., Shumate, M.D., Jin, H., Rikhter, T.Y., Coulter, D.A., Selective changes in single cell GABA(A) receptor subunit expression and function in temporal lobe epilepsy (1998) Nature Medicine, 4 (10), pp. 1166-1172. , DOI 10.1038/2661Bruton, C.J., The neuropathology of temporal lobe epilepsy (1988) Maudsley Monographs, pp. 1-158. , Russel G, Marley E, Williams P (eds) Oxford University Press, LondonCendes, F., Progressive hippocampal and extrahippocampal atrophy in drug resistant epilepsy (2005) Curr Opin Neurol, 18 (2), pp. 173-177Cendes, F., Neuroimaging in investigation of patients with epilepsy (2013) Continuum (Minneap Minn), 19 (3 EPILEPSY), pp. 623-642Cendes, F., Andermann, F., Carpenter, S., Zatorre, R.J., Cashman, N.R., Temporal lobe epilepsy caused by domoic acid intoxication: Evidence for glutamate receptor-mediated excitotoxicity in humans (1995) Ann Neurol, 37 (1), pp. 123-126Cendes, F., Cook, M.J., Watson, C., Andermann, F., Fish, D.R., Shorvon, S.D., Bergin, P., Arnold, D.L., Frequency and characteristics of dual pathology in patients with lesional epilepsy (1995) Neurology, 45 (11), pp. 2058-2064Cendes, F., Dubeau, F., Andermann, F., Quesney, L.F., Gambardella, A., Jones-Gotman, M., Bizzi, J., Arnold, D.L., Significance of mesial temporal atrophy in relation to intracranial ictal and interictal stereo EEG abnormalities (1996) Brain, 119 (4), pp. 1317-1326Cendes, F., Kahane, P., Brodie, M.J., Andermann, F., The mesio-temporal lobe epilepsy syndrome (2012) Epileptic Syndromes in Infancy, Childhood and Adolescence, 5th Edn, , John Libbey Eurotext Ltd, EastleighCendes, F., Knowlton, R.C., Novotny, E., Min, L.L., Antel, S., Sawrie, S., Laxer, K.D., Arnold, D., Magnetic resonance spectroscopy in epilepsy: Clinical issues (2002) Epilepsia, 43 (SUPPL. 1), pp. 32-39Cendes, F., Li, L.M., Andermann, F., Watson, C., Fish, D.R., Shorvon, S.D., Dubeau, F., Arnold, D.L., Dual pathology and its clinical relevance (1999) Adv Neurol, 81, pp. 153-164Chen, K., Aradi, I., Thon, N., Eghbal-Ahmadi, M., Baram, T.Z., Soltesz, I., Persistently modified h-channels after complex febrile seizures convert the seizure-induced enhancement of inhibition to hyperexcitability (2001) Nature Medicine, 7 (3), pp. 331-337. , DOI 10.1038/85480Choi, D., Na, D.G., Byun, H.S., Suh, Y.-L., Kim, S.E., Ro, D.W., Chung, I.G., Hong, S.B., White-matter change in mesial temporal sclerosis: Correlation of MRI with PET, pathology, and clinical features (1999) Epilepsia, 40 (11), pp. 1634-1641. , DOI 10.1111/j.1528-1157.1999.tb02050.xCoan, A.C., Cendes, F., Epilepsy as progressive disorders: What is the evidence that can guide our clinical decisions and how can neuroimaging help? (2013) Epilepsy Behav: E&B, 26 (3), pp. 313-321Coan, A.C., Cendes, F., Understanding the spectrum of temporal lobe epilepsy: Contributions for the development of individualized therapies (2013) Expert Rev Neurother, 13 (12), pp. 1383-1394Coan, A.C., Kubota, B., Bergo, F.P., Campos, B.M., Cendes, F., 3T MRI quantification of hippocampal volume and signal in mesial temporal lobe epilepsy improves detection of hippocampal sclerosis (2014) AJNR Am J Neuroradiol, 35 (1), pp. 77-83Da Costa Neves, R.S., Jardim, A.P., Caboclo, L.O., Lancellotti, C., Marinho, T.F., Hamad, A.P., Marinho, M., Targas Yacubian, E.M., Granule cell dispersion is not a predictor of surgical outcome in temporal lobe epilepsy with mesial temporal sclerosis (2013) Clin Neuropathol, 32 (1), pp. 24-30De Lanerolle, N.C., Kim, J.H., Williamson, A., Spencer, S.S., Zaveri, H.P., Eid, T., Spencer, D.D., A retrospective analysis of hippocampal pathology in human temporal lobe epilepsy: Evidence for distinctive patient subcategories (2003) Epilepsia, 44 (5), pp. 677-687. , DOI 10.1046/j.1528-1157.2003.32701.xDe Tisi, J., Bell, G.S., Peacock, J.L., McEvoy, A.W., Harkness, W.F., Sander, J.W., Duncan, J.S., The long-term outcome of adult epilepsy surgery, patterns of seizure remission, and relapse: A cohort study (2011) Lancet, 378 (9800), pp. 1388-1395Dyhrfjeld-Johnsen, J., Morgan, R.J., Foldy, C., Soltesz, I., Upregulated H-current in hyperexcitable CA1 dendrites after febrile seizures (2008) Front Cell Neurosci, 2, p. 2Emery, J.A., Roper, S.N., Rojiani, A.M., White matter neuronal heterotopia in temporal lobe epilepsy: A morphometric and immunohistochemical study (1997) Journal of Neuropathology and Experimental Neurology, 56 (12), pp. 1276-1282Engel Jr., J., McDermott, M.P., Wiebe, S., Langfitt, J.T., Stern, J.M., Dewar, S., Sperling, M.R., Kieburtz, K., Early surgical therapy for drug-resistant temporal lobe epilepsy: A randomized trial (2012) JAMA: J Am Med Assoc, 307 (9), pp. 922-930. , Early Randomized Surgical Epilepsy Trial Study GEngel Jr., J., Wiebe, S., French, J., Sperling, M., Williamson, P., Spencer, D., Gumnit, R., Enos, B., 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 (2003) Neurology, 60 (4), pp. 538-547Fauser, S., Essang, C., Altenmuller, D.M., Staack, A., Steinhoff, B.J., Strobl, K., Bast, T., Schulze-Bonhage, A., Is there evidence for clinical differences related to the new classification of temporal lobe cortical dysplasia? (2013) Epilepsia, 54 (5), pp. 909-917Frick, A., Magee, J., Johnston, D., LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites (2004) Nature Neuroscience, 7 (2), pp. 126-135. , DOI 10.1038/nn1178Gambardella, A., Reutens, D.C., Andermann, F., Cendes, F., Gloor, P., Dubeau, F., Olivier, A., Late-onset drop attacks in temporal lobe epilepsy: A reevaluation of the concept of temporal lobe syncope (1994) Neurology, 44 (6), pp. 1074-1078Garbelli, R., Meroni, A., Magnaghi, G., Beolchi, M.S., Ferrario, A., Tassi, L., Bramerio, M., Spreafico, R., Architectural (type IA) focal cortical dysplasia and parvalbumin immunostaining in temporal lobe epilepsy (2006) Epilepsia, 47 (6), pp. 1074-1078. , DOI 10.1111/j.1528-1167.2006.00577.xGarbelli, R., Milesi, G., Medici, V., Villani, F., Didato, G., Deleo, F., D'Incerti, L., Spreafico, R., Blurring in patients with temporal lobe epilepsy: Clinical, high-field imaging and ultrastructural study (2012) Brain, 135 (PART 8), pp. 2337-2349Gargaro, A.C., Sakamoto, A.C., Bianchin, M.M., Geraldi Cde, V., Scorsi-Rosset, S., Coimbra, E.R., Carlotti Jr., C.G., Velasco, T.R., Atypical neuropsychological profiles and cognitive outcome in mesial temporal lobe epilepsy (2013) Epilepsy Behav: E&B, 27 (3), pp. 461-469Gloor, P., (1997) The Temporal Lobe and Limbic System, , Oxford University Press, New YorkGoldberg, E.M., Coulter, D.A., Mechanisms of epileptogenesis: A convergence on neural circuit dysfunction (2013) Nat Rev Neurosci, 14 (5), pp. 337-349Grimminger, T., Pernhorst, K., Surges, R., Niehusmann, P., Priebe, L., Von Lehe, M., Hoffmann, P., Becker, A.J., Levetiracetam resistance: Synaptic signatures corresponding promoter SNPs in epileptic hippocampi (2013) Neurobiol Dis, 60, pp. 115-125Hauser, W.A., Annegers, J.F., Rocca, W.A., Descriptive epidemiology of epilepsy - Contributions of population-based studies from Rochester, Minnesota (1996) Mayo Clin Proc, 71 (6), pp. 576-586Hirsch, L.J., Spencer, S.S., Williamson, P.D., Spencer, D.D., Mattson, R.H., Comparison of bitemporal and unitemporal epilepsy defined by depth electroencephalography (1991) Ann Neurol, 30 (3), pp. 340-346Hoffman, D.A., Johnston, D., Downregulation of transient K+ channels in dendrites of hippocampal CA1 pyramidal neurons by activation of PKA and PKC (1998) Journal of Neuroscience, 18 (10), pp. 3521-3528Hoffman, D.A., Magee, J.C., Colbert, C.M., Johnston, D., K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons (1997) Nature, 387 (6636), pp. 869-875. , DOI 10.1038/43119Hughes, E.G., Peng, X., Gleichman, A.J., Lai, M., Zhou, L., Tsou, R., Parsons, T.D., Balice-Gordon, R.J., Cellular and synaptic mechanisms of anti-NMDA receptor encephalitis (2010) J Neurosci, 30 (17), pp. 5866-5875Jackson, J.H., On a particular variety of epilepsy ("intellectual aura"), one case with symptoms of organic brain disease (1880) Brain, 11, pp. 179-207Janszky, J., Janszky, I., Schulz, R., Hoppe, M., Behne, F., Pannek, H.W., Ebner, A., Temporal lobe epilepsy with hippocampal sclerosis: Predictors for long-term surgical outcome (2005) Brain, 128 (2), pp. 395-404. , DOI 10.1093/brain/awh358Jeha, L.E., Najm, I.M., Bingaman, W.E., Khandwala, F., Widdess-Walsh, P., Morris, H.H., Dinner, D.S., Luders, H.O., Predictors of outcome after temporal lobectomy for the treatment of intractable epilepsy (2006) Neurology, 66 (12), pp. 1938-1940. , DOI 10.1212/01.wnl.0000219810.71010.9b, PII 0000611420060627000036Jessberger, S., Nakashima, K., Clemenson Jr., G.D., Mejia, E., Mathews, E., Ure, K., Ogawa, S., Hsieh, J., Epigenetic modulation of seizure-induced neurogenesis and cognitive decline (2007) Journal of Neuroscience, 27 (22), pp. 5967-5975. , http://www.jneurosci.org/cgi/reprint/27/22/5967, DOI 10.1523/JNEUROSCI.0110-07.2007Jimenez-Mateos, E.M., Engel, T., Merino-Serrais, P., McKiernan, R.C., Tanaka, K., Mouri, G., Sano, T., Henshall, D.C., Silencing microRNA-134 produces neuroprotective and prolonged seizure-suppressive effects (2012) Nat Med, 18 (7), pp. 1087-1094Jung, S., Jones, T.D., Lugo Jr., J.N., Sheerin, A.H., Miller, J.W., D'Ambrosio, R., Anderson, A.E., Poolos, N.P., Progressive dendritic HCN channelopathy during epileptogenesis in the rat pilocarpine model of epilepsy (2007) Journal of Neuroscience, 27 (47), pp. 13012-13021. , http://www.jneurosci.org/cgi/reprint/27/47/13012, DOI 10.1523/JNEUROSCI.3605-07.2007Kahane, P., Bartolomei, F., Temporal lobe epilepsy and hippocampal sclerosis: Lessons from depth EG recordings (2010) Epilepsia, 51 (SUPPL. 1), pp. 59-62Kanner, A.M., Epilepsy, suicidal behaviour, and depression: Do they share common pathogenic mechanisms? (2006) Lancet Neurol, 5 (2), pp. 107-108Keller, S.S., Roberts, N., Voxel-based morphometry of temporal lobe epilepsy: An introduction and review of the literature (2008) Epilepsia, 49 (5), pp. 741-757. , DOI 10.1111/j.1528-1167.2007.01485.xKim, J., Jung, S.-C., Clemens, A.M., Petralia, R.S., Hoffman, D.A., Regulation of Dendritic Excitability by Activity-Dependent Trafficking of the A-Type K+ Channel Subunit Kv4.2 in Hippocampal Neurons (2007) Neuron, 54 (6), pp. 933-947. , DOI 10.1016/j.neuron.2007.05.026, PII S0896627307003832Kobayashi, E., D'Agostino, M.D., Lopes-Cendes, I., Andermann, E., Dubeau, F., Guerreiro, C.A.M., Schenka, A.A., Andermann, F., Outcome of surgical treatment in familial mesial temporal lobe epilepsy (2003) Epilepsia, 44 (8), pp. 1080-1084. , DOI 10.1046/j.1528-1157.2003.06503.xKobayashi, E., D'Agostino, M.D., Lopes-Cendes, I., Berkovic, S.F., Li, M.L., Andermann, E., Andermann, F., Cendes, F., Hippocampal atrophy and T2-weighted signal changes in familial mesial temporal lobe epilepsy (2003) Neurology, 60 (3), pp. 405-409Kobayashi, E., Li, L.M., Lopes-Cendes, I., Cendes, F., Magnetic resonance imaging evidence of hippocampal sclerosis in asymptomatic, first-degree relatives of patients with familial mesial temporal lobe epilepsy (2002) Archives of Neurology, 59 (12), pp. 1891-1894. , DOI 10.1001/archneur.59.12.1891Kobayashi, E., Lopes-Cendes, I., Guerreiro, C.A.M., Sousa, S.C., Guerreiro, M.M., Cendes, F., Seizure outcome and hippocampal atrophy in familial mesial temp