Abstract
Mapping brain functions is crucial for neurosurgical planning in patients with drug-resistant seizures. However, presurgical language mapping using either functional or structural networks can be challenging, especially in children. In fact, most of the evidence on this topic derives from cross-sectional or retrospective studies in adults submitted to anterior temporal lobectomy. In this prospective study, we used fMRI and DTI to explore patterns of language representation, their predictors and impact on cognitive performances in 29 children and young adults (mean age at surgery: 14.6 ± 4.5 years) with focal lesional epilepsy. In 20 of them, we also assessed the influence of epilepsy surgery on language lateralization. All patients were consecutively enrolled at a single epilepsy surgery center between 2009 and 2015 and assessed with preoperative structural and functional 3T brain MRI during three language tasks: Word Generation (WG), Rhyme Generation (RG) and a comprehension task. We also acquired DTI data on arcuate fasciculus in 24 patients. We first assessed patterns of language representation (relationship of activations with the epileptogenic lesion and Laterality Index (LI)) and then hypothesized a causal model to test whether selected clinical variables would influence the patterns of language representation and the ensuing impact of the latter on cognitive performances. Twenty out of 29 patients also underwent postoperative language fMRI. We analyzed possible changes of fMRI and DTI LIs and their clinical predictors. Preoperatively, we found atypical language lateralization in four patients during WG task, in one patient during RG task and in seven patients during the comprehension task. Diffuse interictal EEG abnormalities predicted a more atypical language representation on fMRI (p = 0.012), which in turn correlated with lower attention (p = 0.036) and IQ/GDQ scores (p = 0.014). Postoperative language reorganization implied shifting towards atypical language representation. Abnormal postoperative EEG (p = 0.003) and surgical failures (p = 0.015) were associated with more atypical language lateralization, in turn correlating with worsened fluency. Neither preoperative asymmetry nor postoperative DTI LI changes in the arcuate fasciculus were observed. Focal lesional epilepsy associated with diffuse EEG abnormalities may favor atypical language lateralization and worse cognitive performances, which are potentially reversible after successful surgery.
Highlights
Patients with drug-resistant epilepsy may benefit from surgical treatment with rates of seizure freedom ranging from 36% to 84% [1]
When analyzing possible clinical predictors of postoperative changes of laterality index (LI) through univariate analysis (S2 Table), we found that abnormal postoperative interictal scalp EEG (p = 0.003), Engel class IB-IV outcome (p = 0.015) and a longer disease duration were significantly associated with a more atypical language representation after surgery
The main aim of this prospective study was to explore the possible patterns of representation of cortical language function and analyze their clinical predictors in 29 children and young adults with focal lesional epilepsy
Summary
Patients with drug-resistant epilepsy may benefit from surgical treatment with rates of seizure freedom ranging from 36% to 84% [1]. Mapping brain functions using either functional or structural networks can be challenging, especially for language assessment. According to the recent practice guidelines of the American Academy of Neurology (AAN) [4], fMRI can be considered an option for lateralizing language functions in place of the intracarotid amobarbital procedure (IAP) in adult patients with medial temporal lobe epilepsy, temporal lobe epilepsy in general, or extratemporal epilepsy, but not in those with neocortical temporal epilepsy and tumoral epilepsy. Cortical mapping is especially challenging in children [5, 6], due to limited cooperation and movement artefacts, forcing the different centers to adopt variable strategies [2]. There are no Class I or II studies assessing the diagnostic yield of fMRI in comparison with IAP and other invasive cortical mapping procedures or outcomes in the younger age ranges [4]. Evidence is even poorer for tractography and is mainly related to the evaluation of Meyer’s loop prior to temporal lobe surgery [11]
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