Localization of ictal pouting in frontal lobe epilepsy: A case report.

Introduction

Changes in facial expression in frontal lobe epilepsy (FLE) have been described in the literature [1], [2]. However, this discrete feature of ictal semiology is often missed because of more striking events such as hypermotor or bizarre behaviors. One such facial feature, characterized by a turned-down mouth, is traditionally described in French as the “chapeau de gendarme,” referring to the shape of the French policeman's hat during the reign of Napoleon. Ictal pouting (IP), which mimics expressions of fear, displeasure, or disgust, appears frequently during focal seizures. IP is described as an inverted smile. It consists of a turned-down mouth with puckering of the lips and symmetrical sustained (> 5 s) lowering of the labial commissures, commonly accompanied by contraction of the chin. This very interesting sign of FLE is related to the involvement of the mesial frontal areas, particularly the anterior cingulate cortex (ACC) [3]. We report a case whose ictal semiology consisted only of pouting.

Brain magnetic resonance imaging (MRI) studies revealed that focal cortical dysplasia (FCD) in the right mesial frontal lobe and ACC and tissue histopathology confirmed FCD type IIB.

Case report

A 24-year-old woman was admitted to our video-EEG monitoring (VEM) unit for evaluation of seizures that began at the age of 5 years and occurred 15–20 times a day. According to her description, she had preserved conscious and remembered what happened during seizures. Her seizures began with blurred vision, followed by tearful appearance, and ended with a minor contraction of the chin. If these events occurred while she was walking, she was able to continue, although her motion was slower. She also had palpitations, a flushed face, and hot flashes during seizures. Her interictal neurological examination and neurocognitive functions were normal. There was no history of behavioral or psychotic disorders and no family history of epilepsy. She had been on 200 mg lamotrigine daily after her previous antiseizure drugs, valproate and primidone, were discontinued due to inefficacy.

During VEM, she had 11 stereotypical seizures. She stared at the beginning of her seizure for 2–4 s to mimic an expression of sadness. It appeared like an inverted smile, the mouth was turned down with puckering of her lips that was symmetrical and sustained for 10–20 s. Lowering of the labial corners at the very end accompanied by contraction of the chin (Fig. 1, Video 1). She was able to communicate during seizures. The EEG background activity suddenly changed at the onset of seizures, with diffuse attenuation and subsequent rhythmic delta activity bilaterally before changing to spike-and-waves that were dominant over the right hemisphere during the last 3–4 s (Fig. 2, Fig. 3). Before and during seizures, heart rate on the ECG increased from 72 beats per minute to 96 beats per minute respectively. The seizures lasted for 15–25 s. All the seizures were similar, with the only ictal semiology being IP. Brain MRI revealed focal cortical dysplasia on the right mesial frontal lobe and ACC (Fig. 4).

Fig. 1

Facial expression of the patient with ictal pouting and distress. This seizure pattern ends with contraction of the chin.

Fig. 2

Fifth seizure; the first arrow marks an abrupt attenuation change of background activity with ictal EEG onset, and the second arrow indicates the beginning of ictal pouting and clinical seizure onset.

Fig. 3

Eleventh seizure; rhythmic delta activity in the right hemisphere as the activity evolved. The morphology changed to spike-and-wave at the end of the seizure. Slow-wave activity was higher amplitude over the right hemisphere.

Fig. 4

Sagittal (a & b), axial (c), and coronal (d) brain MRI revealed a hyperintense lesion consistent with focal cortical dysplasia (FLAIR sequence).

After VEM, the patient was considered a favorable candidate for epilepsy surgery and was referred for further evaluation; however, she declined surgery at that time. Topiramate was initiated as an add-on therapy at 200 mg/day and subsequently discontinued due to cognitive side effects. Carbamazepine and levetiracetam were initiated as add-on therapy at 600 and 1000 mg/day, respectively. Despite treatment with 200 mg/day lamotrigine, 600 mg/day carbamazepine, and 1000 mg/day levetiracetam, the patient continued to have seizures 5–10 times per day. After participating in multiple antiseizure drug trials that did not affect her seizures, she decided to undergo epilepsy surgery. Pathological examination revealed type II focal cortical dysplasia with balloon cell. After surgery without any complications, she has remained seizure free for 9 months (Engel Class I) and remains under antiseizure drug treatment [4].

Discussion

The ictal semiology of this case consisted of pouting with contraction of the chin at the end. There were no other semiological features that showed seizure propagation. Souirti et al. investigated 11 patients with IP; the epileptogenic zone was localized to ACC (n = 4), the orbito-frontal region (n = 2), the mesial prefrontal, premotor cortex (n = 3), the supplementary motor area (n = 1), and the inferior frontal gyrus (n = 1). All the patients had neurovegetative symptoms with pouting, consistent with the symptoms observed in our patient. In addition to IP, the ictal semiology of these patients included vocalization, head and eye deviation, tonic posturing, agitation, and hyperkinetic movements, which were not observed in our patient [3]. Tan et al. presented a patient with ictal pouting with an epileptogenic zone localized to the left frontal operculum extending to the insula. In this case, the semiology consisted of right gaze deviation and tonic extension of the right arm, followed by the left arm. Despite remaining conscious, our patient could not speak during seizures. This may be explained because her lesion was in the right hemisphere, while the other patient's was on the left side [5]. Leitinger et al. reported a patient with ictal pouting as an early component of seizure without ictal EEG changes in the intracranial frontomesial electrodes. However, Chassoux commented that these results may be due to an insufficient sampling area [6], [7]. In our patient, IP was not an early sign of semiology and it presumed no spreading to other areas of the frontal lobe. After resection of the focal cortical dysplasia from the mesial frontal area and ACC, the patient has remained seizure free for 9 months, which suggests that the epileptogenic zone was localized to the lesion.

An average of 80% of patients remain seizure-free after complete resection of lesional epilepsy [8].

The anterior cingulate cortex and the supplementary sensorimotor area (SSMA) are the most extensively studied areas of the mesial frontal lobe [9]. ACC plays an important role in the motor, limbic, and central autonomic networks. It receives afferent connections from the dorsolateral, frontal, orbitofrontal, and insular areas as well as the thalamic nuclei and sends efferent connections to the premotor area, orbitofrontal cortex, amygdala, and brain stem structures [10]. The SSMA also plays a role in sensorimotor response, negative motor response, and head and eye version.

The network involves afferent connections with the thalamic nuclei, basal ganglia, cerebellar nuclei, cingulate cortex, and premotor and postcentral areas and efferent connections with the corticospinal and corticobulbar projections [11]. Because of its anatomical complexity and interconnectivity, mesial FLE involving ACC presents with various clinical features, including complex stereotypic movements (in particular, thrashing, kicking, grasping, and running with or without vocalization), behavioral disturbances (motor or verbal aggression), paranoid delusions, and personality changes (autistic, obsessive–compulsive, and self-mutilating behavior). Fear with or without a matching facial expression and laughter without mirth may be early manifestations of mesial frontal lobe seizures [9], [12], consistent with reports that negative emotional stimuli activate the mesial prefrontal lobe and ACC [13]. The IP semiology is a behavioral manifestation rather than a motor manifestation and is presumed to be a response to stimuli with an affective or a cognitive component [3]. In this case, the facial expression appears to indicate feelings of distress and this unhappy expression suggests that the affective division of ACC is involved. Although there is a heterogeneity in the ictal semiology, mesial FLE seizures share the common features of frontal lobe seizures, including abrupt onset, short duration, and clusters of multiple daily seizures [14].

IP is a very unusual sign when it is encountered. However, it is subtle and can be easily missed, particularly during sleep or during more striking events. IP can be distinguished from grimacing by a horizontally stretched mouth. IP has been associated with the involvement of the mesial frontal areas and ACC epileptogenic zones. It is highly valuable as a localizing sign but provides no information as a lateralizing sign. The ictal semiology, ictal EEG, brain MRI findings and freedom from seizure after surgery in our case provide further support to the existing literature [3].

Conclusion

Finally, this case showed that ictal pouting may be the only finding of semiology, without any propagation of seizures. It highlights the finding that seizure freedom after complete resection of FCD on the mesial frontal lobe and ACC validated individual localization of epileptogenic zone in this unique case.

The following is the supplementary data related to this article.

Video 1

Seizure semiology of patients shows that ictal pouting is the only symptom during seizures. The patient could to speak and did not lose contact.