Partial epilepsy presenting as focal atonic seizure: A case report
Article Outline
Abstract
A case of atonic seizures localized to the frontal lobe by video-EEG monitoring is reported. The patient is a 38-year-old female with intractable atonic seizures characterized by abrupt onset of facial grimacing and a slow head drop. The onset of atonic seizures was about 6 years before presentation. Video-EEG monitoring showed that her atonic seizures were emanating from the right frontal head region. A high voltage spike and slow wave discharge invariably coincided with the onset of atonic seizures in the patient, similar to the interruption of tonic muscular activity time-locked to a spike on the EEG described in epileptic negative myoclonus; a syndrome associated with epileptic activity in the premotor cortex.
Since routine MRI imaging in this patient was normal, diffusion tensor imaging (DTI) was applied to analyze the white matter integrity of the normal-appearing white matter in the frontal lobes of the patient. We compared the fractional anisotropy, parallel diffusivity and perpendicular diffusivity of normal-appearing white matter in the right versus left frontal lobe. Our results showed no significant difference between the two sides. Possible reasons for the normal DTI findings are discussed.
Keywords: Atonic seizure, Frontal lobe, Partial seizure, Diffusion tensor imaging
1. Introduction
Atonic seizures are epileptic attacks characterized by a sudden loss or diminution of muscle tone, which may be confined to a segment (limb, jaw, head) or involve all postural muscles, leading to a slumping to the ground (epileptic drop attacks).1, 2 In atonic seizures, the loss or diminution of muscle tone is without apparent preceding myoclonic or tonic events.1 The seizure usually lasts less than 15
s and patients remain conscious or only have very brief loss of consciousness.3
Atonic seizures are usually classified as generalized seizures.2, 4 They are well known to occur commonly in the Lennox-Gastaut syndrome of early childhood5, 6 although the introduction of video-electroencephalographic (EEG) monitoring has clarified that pure atonic seizures characterized only by loss or diminution tone are distinctly rare in that population.7
Atonic seizures have also been reported to occur in the context of partial epilepsy in adults.7, 8 In such cases, video-EEG monitoring is mandatory to achieve a correct diagnosis, while magnetic resonance imaging (MRI) is needed to evaluate for specific etiologies, such as cortical malformations.7 Satow et al. investigated atonic seizures in two patients with frontal and parietal lobe epilepsy with prolonged video-EEG monitoring and MRI.8 In their patient with frontal lobe epilepsy, MRI of the brain was normal. In another study of focal inhibitory seizures, magnetic resonance imaging (MRI) of the brain did not reveal structural lesions.9
When MRI of the brain does not reveal structural lesions in patients with atonic seizures whose focality is confirmed by EEG, other imaging modalities may be considered. Diffusion properties of brain tissues have shown high sensitivity to pathological changes in white matter and can potentially identify epileptogenic lesions.10 Diffusion tensor imaging (DTI) is a magnetic resonance imaging technique which measures water molecule diffusion in three dimensions and also measures diffusion anisotropy.11 DTI provides quantitative information for detecting micro-structural abnormalities of white matter, it can detect lesions in regions that appear normal on traditional magnetic resonance imaging (so called normal-appearing white matter, NAWM).12
We report one patient with atonic seizures of frontal lobe origin diagnosed and localized by video/EEG monitoring. We applied DTI to analyze the white matter integrity of the normal-appearing white matter in the frontal lobes of the patient.
2. Patients and methods
2.1. Case report
The patient is a 38-year-old, right handed white female referred to us for evaluation and management of intractable seizures. Her first seizure was a generalized tonic-clonic seizure without aura, at the age of 23 years. The onset of her seizures was preceded by a car accident when she was 21-year-old, during which she hit her head on the steering wheel with loss of consciousness. Imaging studies at that time were normal. She has had a total of about eight generalized tonic-clonic seizures in the past 10 years. Her last generalized tonic-clonic seizure was about a year prior to presentation. She began to have drop attacks, characterized by head drop and loss of tone in all limbs, onset at the age of 32 years. If the patient was standing at the onset of seizure, she would fall backwards or forwards and had sustained scalp and facial lacerations on several occasions. The drop attacks were associated with impairment of consciousness. The drop attacks had increased in frequency over the years, and were occurring at a frequency of 2–3 times a day at the time of presentation to our clinic. She had been tried on therapeutic doses of Dilantin, Zonegran, Keppra and Lamictal, with no efficacy. She did not tolerate low doses of Depakote. Her anti-epileptic medication at presentation to our clinic was Topamax 250mg BID.
A review of her past medical history showed that the patient had a normal delivery and development, and did not have a history of febrile seizures. She completed 2 years of college education and worked as a marketer for several years. Her physical examination was normal and her neurological examination did not show any focal deficits. A routine scalp EEG done prior to referral to our clinic was noted to show bilateral spike and slow wave discharges which were thought to be compatible with primary generalized epilepsy. An MRI of the head with contrast, also completed prior to referral to our clinic, was normal.
3. Methods
3.1. Video/EEG monitoring
Informed consent was obtained and the purpose of the seizure monitoring study was explained to the patient. She was admitted to the Comprehensive Seizure Monitoring Unit of the Methodist University Hospital in Memphis, TN for 5 days. Digital EEG (NICOLET BMSI 6000) was recorded with scalp electrodes placed according to the 10–20 system, with a sampling rate of 200Hz. The low-frequency filter was set to 0.1Hz and high frequency filter was set to 70Hz. EEG data were analyzed offline, and the display montage was adjusted as needed.
3.2. MR imaging acquisition protocol
MRI and DTI were acquired with a 1.5T MR scanner (Siemens, Erlangen, Germany). DTI was performed with single-shot pulsed-gradient, echo-planar imaging protocol (TR=8000ms, TE=109ms, FOV=240×240mm, matrix=128×128, in-plane resolution=1.875×1.875, section thickness=3mm). Diffusion gradients were applied in 12 non-collinear directions. At each slice position, two b values (0 and 1000s/mm2) were applied individually.
3.3. DTI data analysis
Post-processing of diffusion tensor was performed using DTI Studio software (Johns Hopkins University, Baltimore, MD, http://cmrm.med.jhmi.edu). All DTI raw data were visually inspected before applying DTI tensor calculation. No obvious motion artifacts were visualized. Regions of interest (ROIs) were placed bilaterally on normal-appearing white matter (NAWM) of the frontal lobe. The most inferior slices started where the frontal horns of the lateral ventricle were firstly visualized. Frontal lobe white matter was sampled on 5 contiguous sections in each hemisphere. Small oval ROIs of 9–12 pixels (31.64–42.18mm2) were placed on images acquired without diffusion gradients (b=0s/mm2). ROIs were then superimposed on same sections from the maps of FA and the three eigenvalues respectively. The fractional anisotropy (FA), the largest diffusion direction DA (λ1), and diffusivity perpendicular to the axon fiber DR (DR=(λ2+λ3)/2), for each ROI all three parameters in both hemispheres were obtained. Data were analyzed using Excel 2007(Microsoft, USA). A paired t-test was performed to compare data between the left and right side in the patient. The analysis was repeated in FA, DA, and DR of the NAWM.
4. Results
4.1. Video/EEG monitoring
During the admission patient had 15 seizures, which were confirmed by family members to be her habitual seizures. The patient was sitting or lying in bed during all her seizures. The seizure semiology was quite stereotypical, starting with an abrupt onset of unresponsiveness, followed by facial grimacing and loss of neck muscle tone, which manifested as a slow head drop in either direction depending on her head position at seizure onset. Her head drop occurred over 2–3s. Unfortunately, limb EMGs were not monitored in this case, but limb hypotonia was confirmed during several events by clinical examination and ictal EEG did not show any contamination by EMG artifacts.
The patient's inter-ictal EEG showed intermittent bilateral spike and slow wave discharges as well as intermittent spikes emanating from the right frontal head region.
All ictal EEGs were very stereotyped, starting with right frontal spike and slow wave activity, followed by a bilateral, high amplitude spike and slow wave discharge which always coincided with the onset of head drop (Fig. 1, Fig. 2). Thereafter, there was diffuse background suppression for 4–6s, followed by low voltage, rhythmic 15–20Hz activity which appeared maximal in the right frontal head region. The ictal EEG record then built up into diffuse semi-rhythmic spike and slow wave activity which appeared maximal in the frontal head regions.
Fig. 1.
Ictal EEG showing right frontal onset followed by bilateral high voltage spike discharge which invariably coincided with clinical onset of atonic seizure. There is subsequent diffuse electrodecrement and fast activity.
Fig. 2.
Ictal EEG displayed with referential montage, showing evolution of ictal activity into diffuse spike and slow wave activity.
4.2. DTI results
Fractional anisotropy (FA) data from NAWM on the frontal lobes in both left and right hemispheres are shown in Table 1. There was no significant right–left asymmetry in FA value. Data of directional diffusivities DA and DR are also shown in Table 1. Both right versus left side DA or DR in frontal NAWM were compared. There were no significant differences between right and left side.
Table 1. Diffusion tensor measurement (mean±SD) in patient.
| Diffusion tensor measurement | Right NAWM | Left NAWM | P-value |
|---|---|---|---|
| FA | 0.37±0.04 | 0.37±0.04 | 0.79 |
| DA | 1.66±0.09 | 1.63±0.05 | 0.38 |
| DR | 0.96±0.07 | 0.94±0.07 | 0.60 |
4.3. Clinical course
The inter-ictal and ictal EEG findings during 5 days of video-EEG monitoring indicated that the patient had atonic focal seizures emanating from the right frontal head region. She was continued on Topamax. Vimpat (Lacosamide) was added and titrated up to 200mg BID with significant reduction in seizure frequency.
5. Discussion
The clinical semiology of our patient's seizures was characterized by abrupt onset of impaired consciousness and facial grimacing, followed by atonic head drop. These clinical features are remarkably similar to the clinical presentation of the patient with frontal lobe atonic seizure described by Satow et al.8 Our patient's head drops occurred slowly over 2–3s, again similar to the slow atonic falls described by Satow et al.
Although EMGs were not recorded in our patient, the ictal EEG (Fig. 1, Fig. 2) clearly showed that there was no apparent contamination of the ictal scalp EEG by EMG activity. In addition, limb hypotonia was confirmed by clinical examination during the seizures. These facts in concert with the atonic head drop, confirm that the seizures were atonic, and helped distinguish the ictal grimacing in our case from the facial grimacing that may sometimes occur in frontal lobe seizures with tonic motor manifestations.
The ictal EEG pattern in our patient is also broadly similar to the case reported by Satow et al., with diffuse attenuation followed by low voltage fast activity and repetitive spiking in both cases.8 A distinct feature in our patient's ictal EEG however, was the presence of high voltage spike and slow wave discharges which invariably appeared to coincide with the onset of her atonic seizures, based on our careful review of the patient's video-EEG records; in the absence of polygraphic study of postural and limb muscles. This is reminiscent of the “spike-related epileptic silent periods” described by Tassinari,13 which are periods of muscle inhibition strictly related to a diffuse or focal spike. It also appears to be compatible with the syndrome of “epileptic negative myoclonus”14; which is an interruption of tonic muscular activity, time-locked to a spike on the EEG. Epileptic negative myoclonus has been shown to be associated with epileptic activity in the premotor cortex, including the supplementary motor area.15 It has also been reported to occur from cortical malformation in the post-central gyrus.16
However, it is relevant to note that epileptic negative myoclonus is an epileptic motor phenomenon of much shorter duration than in our case, with usual durations less than 500ms17 and clinically appearing as a brief lapse of muscular tone, or as an abrupt epileptic drop attack in more severe cases. In one case of epileptic negative myoclonus, the duration of the negative myoclonus was 30–340ms.17
Atonic seizures involving the frontal lobe can be explained by inhibitory mechanisms in the negative motor area. There are two areas in the frontal lobe where electric stimulation could cause the inhibition of voluntary movements. To distinguish these two negative motor areas, investigators18 proposed the term primary negative motor area (PNMA, in reference to the area of the inferior frontal gyrus immediately in the front of the primary face motor region) and supplementary negative motor area (SNMA, in regard to the mesial portion of the superior frontal gyrus immediately in front of the supplementary sensorimotor area). Ikeda et al.19 reported two patients with negative motor seizure presenting as praxis, with ictal subdural EEG suggesting epileptogenic focus in the mesial frontal area (SNMA). Cortical stimulation in that area elicited similar negative seizure phenomenon in one of the patients. Another study reported three patients who had contralateral ictal paresis, with subdural recordings localizing the ictal focus to the mesial frontal regions involving the SNMA.20
Since the seizure onset in our patient was localized by video-EEG monitoring to the right frontal head region, we compared the fractional anisotropy (FA), parallel diffusivity (DA) and perpendicular diffusivity (DR) of normal-appearing white matter (NAWM) in right versus left frontal lobe. Our results showed that there was no significant difference between the two sides in our patient. Although the results of FA in the temporal lobe may only be extrapolated to the frontal lobe with caution, our results are similar to those of Nilsson et al. (2008), who found no significant difference of FA in the temporal lobe white matter in TLE patients compared to healthy controls and found no significant difference between FA of the side of seizure onset, when compared to the contralateral side in TLE patients.21 Obviously, our small sample size also limits the power of the investigation. It is possible that future studies with more subjects may reveal subtle changes in white matter diffusivity in frontal lobe atonic seizures.
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PII: S1059-1311(10)00089-0
doi:10.1016/j.seizure.2010.04.014
Published by Elsevier Inc.
