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Epileptic Disorders

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Ictal deafness in drug-resistant MRI-negative epilepsy Volume 21, issue 2, April 2019

Figures


  • Figure 1

  • Figure 2

  • Figure 3

  • Figure 4

  • Figure 5

Tables

Patient details

A 20-year-old, right-handed woman had suffered with seizures since the age of six years, consisting of focal tonic seizures beginning in the right side of the face or right limbs and focal impaired awareness seizures with hypersalivation, followed by motor aphasia. These seizures occasionally evolved to bilateral tonic-clonic seizures. She was referred to our hospital four months after the onset of epilepsy. Her seizures occurred monthly despite medication with antiepileptic drugs (AEDs). The seizure frequency gradually increased at age 15 years despite administration of various AEDs, including carbamazepine, valproate, clobazam, levetiracetam, and topiramate. She became aware of impaired hearing before the occurrence of these seizures at around the age of 19 years. She described the aura as “sound became fainter and fainter, and finally disappearing”. Her seizures were characterized by suppressed hearing (ictal deafness [ID]), followed by speech arrest, and then evolved into right facial tonic seizures. She could state verbally when the auditory symptoms would start. She had two or three seizures per week over the last six months under treatment with carbamazepine at 200 mg, levetiracetam at 2,000 mg, and clonazepam at 4 mg. History was normal for gestation, birth, and development, and there was no family history of neurological or epileptic disorders.

Non-invasive investigations

Comprehensive pre-surgical evaluation was performed. A 3.0 Tesla magnetic resonance imaging (MRI) revealed no structural abnormality and fluorodeoxyglucose-positron emission tomography (PET-FDG) showed no local hypometabolism. Long-term video-EEG monitoring demonstrated interictal spikes in the left mid-temporal region and ictal onset from the left temporal area. Neurological examination revealed no abnormalities with no obvious auditory disturbance. Her intelligence and memory function were within normal range based on the Wechsler Adult Intelligence Scale, third edition, and Wechsler Memory Scale-Revised.

Hypothesis

Based on the ictal symptom, we hypothesized that her seizures initially originated from the left auditory cortex and propagated to the surrounding regions, first to the language area and then to the left facial motor cortex, before losing awareness. The scalp EEG findings support this hypothesis. Her normal cognitive function and imaging studies indirectly suggest the presence of a mild or focal epileptogenic lesion.

Invasive investigations

Pre-surgical evaluation was performed with intracranial electrodes. A depth electrode was inserted along Heschl's gyrus (HG) postero-medially using the frameless stereotactic system (VarioGuide®, Brainlab, Germany) (Reddy et al., 2010). Subdural strip and grid electrodes were arrayed at the temporo-parieto-frontal area surrounding HG, including the inferior frontal gyrus, temporo-parietal operculum, superior temporal gyrus (STG), middle temporal gyrus, and angular gyrus (figure 1A, B). The locations of the contacts were identified using automatic fusion images based on postoperative thin-slice computed tomography and preoperative MRI (figure 2). Two events of sudden hearing impairment were recorded during video-EEG monitoring. Intracranial EEG demonstrated the beginning of ictal discharges in the lateral half of HG and part of the posterior STG (figure 3). Interictal discharges were observed in the left middle temporal area. Functional mapping with electrical cortical stimulation (ECS) (biphasic square pulses; frequency: 50 Hz; pulse width: 0.3 ms; stimulation intensity: 1-10 mA; duration of each stimulation: 2 s) reproduced language responses in the posterior STG and suppression of hearing in HG. The patient reported stronger hearing impairment at the medial part of HG. Bipolar stimulation at 2 mA at contacts HG1 and 2 elicited complete deafness, but no or mild hearing suppression was provoked at contacts HG3 to 6. The patient consistently reported predominant hearing impairment in the right (contralateral) ear (figure 1B).

Surgery and outcome

Based on the results of intracranial EEG recording and electrical cortical stimulation, resection of the lateral half of Heschl's gyrus and a small part of the superior temporal gyrus was performed (figure 4). Subsequently, the patient has been seizure-free for one year and four months, except for a single episode of breakthrough seizures upon AED (clobazam) withdrawal at five months after surgery (International League Against Epilepsy Class 3). Histopathological examination revealed focal cortical dysplasia type IIa (figure 5). Her auditory acuity and neuropsychological test scores were stable at one year after surgery and she was able to find employment postoperatively. Her ability to listen to music and sing songs (karaoke) did not change after surgery.

Discussion

Our patient presented with refractory seizures that initiated with ID, and intracranial EEG localized the seizure onset zone to the anterolateral part of HG. Partial removal of HG led to seizure improvement without auditory deficits. This outcome suggests that ID can arise from the anterolateral half of HG.

Ictal deafness was first described as a type of negative or inhibitory auditory seizure which is relatively rare, with an estimated prevalence of 0.1% (6/8,000) among epilepsy patients (Florindo et al., 2006). Only 11 cases have been reported (table 1). The characteristics of these cases indicate that ID can arise from the temporal lobe.

The present case suggests that ID arises from the anterolateral part of HG. Previous electrical cortical stimulation studies support this conclusion (Sinha et al., 2005; Fenoy et al., 2006). Electrical cortical stimulation of HG, especially the anterolateral part of HG, can provoke suppression of hearing (Fenoy et al., 2006). In our study, electrical cortical stimulation of HG also evoked the same phenomenon, but more easily at the posteromedial part of HG. Functional localization of suppression of hearing in HG may differ between patients because of the possible functional re-organization of the auditory system in patients with epilepsy (Sinha et al., 2005).

The reported cases of ID are summarized in table 1. Florindo et al. (2006) suggested that ID may have lateralizing value because all nine previous cases (three reported by Ghosh et al. [2001] and six by Florindo et al. [2006]) had occurred in patients with a left temporal lesion. The present case supports this conclusion. In contrast, Shahar et al. (2010) reported a case of ID arising from the right temporal area. Furthermore, ECS investigation elicited suppression of hearing by stimulation of the right HG in two thirds of patients (Fenoy et al., 2006). Further case experience is necessary to confirm the lateralizing value of ID. The present case further suggests that the epileptogenic side may be lateralized and localized contralaterally to HG on the side of predominant suppression of hearing (Ghosh et al., 2001; Sinha et al., 2005).

The sequelae of HG resection are poorly understood. Removal or damage to the right side of HG may cause amusia (Russell and Golfinos, 2003; Terao et al., 2006). Recently, removal of the right anterolateral part of HG was reported to be possible without auditory deficits (Nagahama et al., 2018). In our case, removal of the left anterolateral part of HG caused no auditory or cognitive dysfunction. Therefore, the left part of HG or the anterolateral part of HG may be resectable with relatively low risk of postoperative auditory dysfunction. Further case experience with specific details of the extent of removal are necessary to validate these suggestions.

The present case is the first report of a patient who underwent epilepsy surgery for drug-resistant epilepsy with ID. Although a single breakthrough seizure on AED withdrawal indicates incomplete resection of the epileptogenic zone, the control of her weekly seizures and focal EEG findings still suggest that ID can arise from the anterolateral part of HG. This ictal symptom is rare but may have localizing value, and good seizure outcome can be achieved after removal without auditory deficits.

Acknowledgements and disclosures

We thank Ms. Satsuki Konno and Dr. Yuuko Saito for their clinical support. This study was supported, in part, by an Intramural Research Grant (28-4: Clinical Research for Diagnostic and Therapeutic Innovations in Developmental Disorders) for Neurological and Psychiatric Disorders of the National Center of Neurology and Psychiatry. None of the authors have any conflict of interest to declare.