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Long-Term Seizure Outcome in Pediatric Patients with Focal Cortical

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Long-Term Seizure Outcome in Pediatric Patients with Focal Cortical Seizure: European Journal of Epilepsy 62 (2018) 66–73 Contents lists available at ScienceDirect Seizure: European Journal of Epilepsy journal homepage: www.elsevier.com/locate/seizure Long-term seizure outcome in pediatric patients with focal cortical dysplasia undergoing tailored and standard surgical resections T ⁎ Eva Martinez-Lizanaa,b, , Susanne Fauserc, Armin Brandta,b, Elisabeth Schulerd, Gert Wiegande, Soroush Doostkamb,f, Victoria San Antonio-Arcea,b,i, Julia Jacobsa,b, Thomas Bastb,g, Mukesch Shahb,h, Josef Zentnerb,h, Andreas Schulze-Bonhagea,b a Dept. of Epileptology, Medical Center – University of Freiburg, Germany b Faculty of Medicine, University of Freiburg, Germany c Epilepsy Center Bielefeld, Germany d Dept. of Pediatric Neurology Heidelberg, Germany e Dept. of Pediatric Neurology, University of Kiel, Kiel, Germany f Institute of Neuropathology, Medical Center – University of Freiburg, Germany g Epilepsy Center Kork, Germany h Dept. Neurosurgery, Medical Center – University of Freiburg, Germany i Dept. of Pediatric Neurology, Hospital Sant Joan de Deu, Barcelona, Spain ARTICLE INFO ABSTRACT Keywords: Purpose: Focal cortical dysplasia (FCD) is the major cause of focal intractable epilepsy in childhood. Here we Focal cortical dysplasia analyze the factors influencing the success of surgical treatment in a large cohort of children with histologically Epilepsy surgery ascertained FCD. Children Method: A retrospective study of the effects of FCD type, surgical intervention, and age at surgery in a pediatric Long-term outcome cohort. Results: A total of 113 patients (71 male; mean age at surgery 10.3 years; range 0–18) were analyzed; 45 had undergone lesionectomy, 42 lobectomy, 18 multi-lobectomy, and eight hemispherotomy. Complete seizure control (Engel Ia) was achieved in 56% after two years, 52% at five years, and 50% at last follow-up (18–204 months). Resections were more extensive in younger patients (40% of the surgeries affecting more than one lobe in patients aged nine years or younger vs. 22% in patients older than nine years). While resections were more limited in older children, their long-term outcome tended to be superior (42% seizure freedom in patients aged nine years or younger vs. 56% in patients older than nine years). The outcome in FCD I was not significantly inferior to that in FCD II. Conclusions: Our data confirm the long-term efficacy of surgery in children with FCD and epilepsy. An earlier age at surgery within this cohort did not predict a better long-term outcome, but it involved less-tailored surgical approaches. The data suggest that in patients with an unclear extent of the dysplastic area, later resections may offer advantages in terms of the precision of surgical-resection planning. 1. Introduction imaging findings are limited and a diagnosis of FCD requires histolo- gical confirmation. Patients with FCD frequently present with a severe Focal cortical dysplasia (FCD) is a subgroup of cortical malforma- form of epilepsy characterized by pharmacoresistance to available an- tions characterized by abnormal regional neuronal migration and dif- tiepileptic drugs (AED) [3,4]. Surgery is considered to be of particular ferentiation that result in aberrant cortical organization [1]. It is the importance in children who—aside from seizures—may suffer from most common anatomo-pathological feature in patients undergoing progressive developmental delay and behavioral disorders if their epi- epilepsy surgery in childhood [2]. Prevalence figures have been rising lepsy is not controlled. over recent years due to improved MRI quality, but, even with the best Several classification schemes have been proposed that rely on pa- methodology currently available, the sensitivity and specificity of thological characteristics. According to Palmini et al. [5], two main ⁎ Corresponding author at: Epilepsiezentrum Universitätsklinikum Freiburg, Breisacherstr. 64, 79106, Freiburg, Germany. E-mail address: [email protected] (E. Martinez-Lizana). https://doi.org/10.1016/j.seizure.2018.09.021 Received 27 June 2018; Received in revised form 21 September 2018; Accepted 25 September 2018 1059-1311/ © 2018 British Epilepsy Association. Published by Elsevier Ltd. All rights reserved. E. Martinez-Lizana et al. Seizure: European Journal of Epilepsy 62 (2018) 66–73 types of FCD can be histopathologically distinguished: Type I refers to Germany). T1-weighted sequences with and without gadolinium-die- architectural disturbances of cortical lamination (IA without, IB with thylenetriaminepentaacetic acid (DTPA), T2-weighted images, fluid- giant or immature pyramidal neurons outside layer 5); Type II is attenuated inversion recovery (FLAIR) sequences, and MPRAGE (mag- characterized by dyslamination and the presence of abnormal cell ele- netization-prepared rapid gradient echo) sequences were performed. To ments (IIA when dysmorphic neurons are present and IIB when eosi- analyze mesio-temporal structures, axial images with a modified an- nophilic balloon cells are also identified). Particularly, giant and dys- gulation parallel to the long axis of the temporal lobe were acquired. morphic neurons are considered responsible for seizure generation in Criteria used for MRI-based FCD detection were gyration anomalies, FCD Type II [6–9]. In 2011, the International League Against Epilepsy focal thickenings of the cortex, blurring of the gray-/white-matter (ILAE) classified FCDs in a three-tiered system that additionally dis- junction, and abnormal cortical and subcortical signal intensity. tinguished whether pathological findings of FCD are isolated or asso- The surgical resections were classified as follows: tailored resections ciated with other epileptogenic lesions [10]. based not on the anatomical border of lobes but on imaging (lesio- Due to the therapeutic challenge that these patients represent, epi- nectomy) or electrophysiological findings (topectomy); unilobar re- lepsy surgery has been increasingly used in recent years, with several section (when the resected area followed one lobe’s anatomical border); reports showing the benefits of the surgical treatment in patients with multilobar resections (when it followed several lobes’ anatomical bor- FCD [3,11–14]. The reported postsurgical outcome in FCD patients has, ders); and hemispherotomy (when functional disconnection was em- however, often been inferior to that in patients with other etiologies ployed). [15,16]. Still, progress in presurgical assessment has improved the outcome of the surgery at increasingly early ages [17,18]. Surgery has 2.2. Histology been found to be more effective in patients younger than 18 years compared to adults [19] and when performed in centers with extensive The cortical specimens of patients with FCD were classified by the experience [20]. Even in patients younger than six months, surgery is Institute of Neuropathology of the University Hospital of Freiburg ac- considered a safe option [21]. cording to the Palmini classification [5]. Additionally, information We analyzed possible associations between age at surgery, type of about the presence of other epileptogenic lesions in MRI or histological resection, FCD type (classified according to Palmini et al. [5]), and specimens, i.e., hippocampal sclerosis (dual pathology), was included long-term outcomes in one of the largest cohorts of patients with [11,22,23]. manifestation and surgery during childhood and with histologically confirmed FCD. 2.3. Postoperative outcome 2. Methods The postoperative seizure outcome was classified according to Engel: Ia. free of seizures; Ib. auras or seizures with drug withdrawal; II. 2.1. Patient selection occasional seizures (< 2 seizures/year or > 90% seizure reduction); III. 90–75% reduction of seizure frequency; IV. < 75% reduction in sei- Patients with structural epilepsy due to FCD who were undergoing zure frequency [24]; and according to Wieser: 1. free of seizures and surgical treatment were identified from electronic charts. The inclusion auras; 2. isolated auras; 3. 1–3 days with seizures per year; 4. at least criteria were: (1) age at surgery younger than 18 years; (2) epilepsy four days with seizures per year or ≥50% seizure reduction; 5. < 50% diagnosis confirmed by video-EEG monitoring; (3) surgical treatment at seizure reduction; 6. > 100% seizure increase in comparison to pre- the University Hospital in Freiburg between 1999 and 2015; (4) his- operative frequencies [25], as assessed at follow-up times evaluated tological confirmation of FCD based on resected specimens; and (5) twice yearly during the first two years and annually thereafter. For clinical follow-up of at least 18 months. those patients who underwent surgery twice, only the last surgery was Patients underwent presurgical evaluation, including long-term considered for outcome analysis. video-EEG recordings of habitual seizures, at the Epilepsy Centers of Kiel, Heidelberg, Kehl-Kork, and Freiburg and were later referred to the 2.4. Statistical analysis University Hospital of Freiburg for intracranial EEG recordings (if re- quired) and surgical treatment. Individualized surgical approaches Statistical analysis was done with IBM SPSS Statistics 23, MS Excel were selected depending on patient characteristics, with particular re- 2010, and R version 3.2.5. P-values were calculated by the chi-square gard to the extension and localization of the lesion as judged by test, Fisher’s exact test, and Kruskal–Wallis test. All tests were two structural and functional investigations. tailed, with the threshold
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