Ictal semiology in temporo-frontal epilepsy: A systematic review and meta-analysis

Abstract

We performed a systematic review of the ictal semiology of temporo-frontal seizures with the aim to summarize the state-of-the-art anatomo-clinical correlations in the field, and help guide the interpretation of ictal semiology within the framework of presurgical evaluation. We conducted the systematic review and meta-analysis, and reported its results according to the Preferred Reporting Items for Systematic Review and Meta-Analysis statement. We searched electronic databases (Scopus, PUBMED, Web of Science, and EMBASE) using relevant keywords related to temporal, frontal and sublobar structures, semiology, and electroencephalography/stereoelectroencephalography exploration. The risk of bias was evaluated using the QUADAS2. We included articles in English, reporting the seizure semiology of patients with temporal lobe epilepsy with temporal-frontal involvement and patients with frontal lobe epilepsy and fronto-temporal network involved. We performed hierarchical cluster analysis to determine signs and symptoms associated with the temporo-frontal epileptogenic network for all patients and for each subgroup (frontal/temporal seizure onset). Fisher exact test was performed to evaluate the difference in seizure freedom and clinical sign/symptom occurrence in patients that underwent unilobar versus bilobar resection. Meta-analysis on the prevalence of temporo-frontal/fronto-temporal involvement applying a random-effect model was used. We included 40 articles and we extracted data from 109 patients. The meta-analysis showed the total prevalence of temporo-frontal/fronto-temporal network involvement was 19.75%, CI 12.02-27.47, high heterogeneity (82.71%). For the whole group and subgroups, the main cluster of clinical manifestations is emotional, autonomic, cognitive, grimace, hyperkinetic (association coefficient higher than .6). Elementary motor semiology is significantly associated with multilobar resection (p = .022 whole group and p = .0012 fronto-temporal subgroup). Fifty-eight patients were seizure-free after surgery. There was no significant difference between seizure freedom in uni versus bilobar resections (p = .28). Seizures involving temporo-frontal/fronto-temporal network usually manifest with a cluster of signs and symptoms: emotional, autonomic, grimace, cognitive and hyperkinetic behavior. Based on semiology, one cannot distinguish between fronto-temporal and temporo-frontal cases at individual patient level. In those patients undergoing a surgical procedure, elementary motor seizure semiology is significantly associated with multilobar resection.

Keywords: SEEG; anatomo‐clinical correlation; epilepsy surgery; ictal semiology; systematic review; temporo‐frontal epilepsy.

FIGURE 1

PRISMA chart.

FIGURE 2

Prevalence of ictal clinical signs and symptoms for all patients group and for each subgroup (fronto‐temporal and temporo‐frontal).

FIGURE 3

Cluster analysis for all patients group and for each subgroup, fronto‐temporal and temporo‐frontal showing that emotional, grimacing, hyperkinetic, autonomic, and cognitive clinical manifestations are included in the main cluster of symptoms for all groups.

FIGURE 4

Fronto‐temporal network display. Tracts generated in DSI Studio application using specific ROI to identify main temporo‐frontal structural connections relevant for seizure propagation according to SEEG data. (A) Patients with temporal lobe epilepsy and the frontal sublobar propagation. (B) Patients with frontal lobe epilepsy and temporal sublobar propagation. AF, arcuate fasciculus; IFOF, inferior fronto‐occipital fasciculus.

FIGURE 5

Meta‐analysis showing the prevalence of patients with fronto‐temporal network involvement in each study.