Ictal MEG in two children with partial seizures

Ictal MEG in two children with partial seizures

Brain & Development 26 (2004) 403–408 www.elsevier.com/locate/braindev Case report Ictal MEG in two children with partial seizures Harumi Yoshinagaa...

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Brain & Development 26 (2004) 403–408 www.elsevier.com/locate/braindev

Case report

Ictal MEG in two children with partial seizures Harumi Yoshinagaa,*, Yoko Ohtsukaa, Yoshiaki Watanabea, Miki Inutsukaa, Yoshihiro Kitamurab, Kazushi Kinugasab, Eiji Okaa a

Department of Child Neurology, Okayama University Medical School, Shikatacho 2-5-1, Okayama 700-8558, Japan b Okayama Ryogo Center, Okayama, Japan Received 1 September 2003; received in revised form 12 November 2003; accepted 12 November 2003

Abstract We report on the successful identification of epileptic foci in two children with partial epilepsy using ictal magnetoencephalography (MEG). Case 1 is a 12-year-old male suffering with simple partial seizures with leftwards nystagmus. Ictal SPECT revealed a hyperperfusion area in the right lateral occipital area, and MRI revealed cortical dysplasia in the same area. Interictal EEG dipoles were concentrated in the right mesial occipital lobe. Both interictal and ictal MEG dipoles were concentrated in the right mesial occipital lobe, which corresponded well with neuroimaging data and his clinical features. Case 2 is a 5-year-old female suffering with simple partial seizures with left-side facial twitching. Interictal EEG dipoles were located in her left motor area, the pre-sylvian fissure, close to the location of the interictal MEG-estimated dipoles. Ictal EEGs showed no remarkable changes associated with her clinical manifestations. However, ictal MEG showed high-voltage slow waves over her left hemisphere, and ictal MEG iso-contour maps revealed a clear dipolar pattern, which suggested that the MEG dipole was located in the area of the sylvian fissure. Ictal SPECT revealed hyperperfusion areas around the left sylvian fissure. Conclusion: Ictal MEG is useful for determining the precise location of epileptic focus in patients with motionless seizures, including children. q 2003 Elsevier B.V. All rights reserved. Keywords: Ictal; Magnetoencephalography; EEG; Localization-related epilepsy; Dipole

1. Introduction

2. Patients and methods

The dipole localization method has been widely used for non-invasive localization of spike foci [1 –3]. In contrast to EEG, MEG is not affected by the conductivity of intervening tissue layers (brain, CSF, skull, and scalp), and the accuracy of MEG localization has been well documented [2 – 4]. However, movement artifacts are known to obscure the accuracy of MEG imaging, for which reason there have been few reports of ictal MEG studies on children [5,6]. In an effort to address this deficiency, we report herein on an ictal MEG study of two childhood epilepsy patients.

Subjects were drawn from a group of six children between the ages of 5 and 12 years who underwent MEG at the Okayama Ryogo Center between January and December of 2002. We obtained informed consent from the parents of these patients to perform MEG. Two of these patients, a 12-year-old male and a 5-year-old female, had spontaneous seizures during MEG recordings, and we chose these two patients as the subjects of the present study. We recorded EEGs and MEGs simultaneously. MEGs were recorded with a 148-channel whole-head magnetometer (BTI Magnes, San Diego, CA) with simultaneous 20-channel EEG recording using the international 10 – 20 system with additional electrodes at Oz referenced to the respective ears. The MEG and EEG sampling rates were 678.17 and 500 Hz, respectively. The MEG signal was

* Corresponding author. Tel.: þ 81-86-235-7372; fax: þ81-86-235-7377. E-mail address: [email protected] (H. Yoshinaga). 0387-7604/$ - see front matter q 2003 Elsevier B.V. All rights reserved. doi:10.1016/j.braindev.2003.11.003

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filtered in real time with a high pass of 200 Hz and a low pass of 0.1 Hz. EEG was filtered at 0.5 –100 Hz. Common reference points (nasion, inion, and ear holes) were used for MEG, EEG and MRI for co-registration of data. Both EEG and MEG outputs were monitored on real-time displays. Data epochs were visually selected using both the MEG and EEG waveforms. We calculated MEG dipoles based on data from 64 channels selected over the region of interest. MEG dipoles were analyzed with the single dipole model using the BTI program. In the calculations, the head was modeled as a sphere with a radius that best fit the local skull curvature at the probe positions. The skull shape was derived from a 3D digitalization of the surface of the patient’s scalp before the recording session. We plotted the dipoles that showed a goodness of fit (GOF) of more than 98% and that existed from the spike’s onset to its maximum negative peak for the interictal spikes. For the ictal sessions, we averaged several seconds of rhythmical activity to get a representative waveform. Ictal MEG dipoles were calculated for this representative waveform from its onset to its maximum negative peak. We analyzed the EEG dipoles using the SynaPointPro dipole localization software package (GE Marquette Medical System Japan, Ltd, Tokyo). This software uses a single moving dipole inverse-solution algorithm, a threeshell spherical head model, and electrode positioning data. The dipole fit is calculated every 5 ms. The targets of the dipole fit are the same as MEG recording and we plotted the dipoles that showed a GOF of more than 95%.

3. Results 3.1. Case 1 Case 1 is 12-year-old male suffering with simple partial seizures with eye deviation and leftwards nystagmus. His EEG showed focal spikes at the right occipital electrode. He had simple partial seizures several times during MEG/EEG recordings. During these seizures, fast activity with increasing amplitude and decreasing frequency was observed at the right occipital electrode on EEG. On ictal MEGs, theta trains followed by right occipital sharp waves were observed (Fig. 1). Both interictal EEG dipoles and MEG dipoles were concentrated in the right mesial occipital lobe with a high GOF of more than 98%. In addition, some of interictal MEG dipoles were also concentrated in the left lateral occipital area (Fig. 2A and B). MEG dipoles calculated for these theta trains were located in the right mesial occipital lobe (Fig. 2C). Ictal EEG dipole analysis did not yield a high GOF for these ictal events. Ictal SPECT revealed a hyperperfusion area in the right lateral occipital area (Fig. 2D), and MRI revealed cortical dysplasia in the right mesial to lateral occipital area. The results of interictal/ ictal MEG dipole corresponded well with neuroimaging data and his clinical features. 3.2. Case 2 Case 2 is a 5-year-old female suffering with simple partial seizures with left-side facial twitching associated

Fig. 1. Simultaneous ictal EEG/MEG recordings of case 1. The MEG channels were aligned from anterior to posterior for the left lateral sensor. We analyzed the ictal MEG dipoles at the section indicated by the underline. MEG and EEG changes occurred soon after the seizure onset indicated by the arrow.

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Fig. 2. Dipoles and the neuroimaging results of case 1. (A) Interictal EEG dipoles. Dots show the locations of all the estimated dipoles. (B) Interictal MEG dipoles. Dots show the locations of the main estimated dipoles. Triangles show the locations of the other estimated dipoles. (C) Ictal MEG dipoles. Dots show the locations of all the estimated dipoles for the section indicated by the underline in Fig. 1. (D) Ictal SPECT. A hyperperfusion area was observed in the right lateral occipital area. It is clear that the ictal/interictal EEG and MEG dipoles corresponded well with each other.

with discomfort in her mouth, which is sometimes followed by impairment of consciousness. Her EEGs showed interictal spikes in the left central mid-temporal area during waking recordings, which increased during sleep

recordings. Ictal EEGs showed no remarkable changes associated with her clinical manifestations (Fig. 3). However, ictal MEGs showed high-voltage slow waves over her left hemisphere (Fig. 4). EEG dipoles estimated for

Fig. 3. EEG recordings of case 2. Left, interictal EEG; Center, ictal EEG; Right, interictal EEG during sleep. Note that no difference was observed between the interictal and ictal EEGs.

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Fig. 4. MEG recordings of case 2. Left, interictal MEG recording; Right, ictal MEG recording. The MEG channels were aligned from the left lateral sensor (anterior to posterior) to the right lateral sensor. Note the large delta wave that appeared in the left hemisphere during the ictal MEG recording.

Fig. 5. Dipoles and the neuroimaging results of case 2. (A) Interictal EEG dipoles. Dots show the locations of all the estimated dipoles. (B) Interictal MEG dipoles. Dots show the locations of all the estimated dipoles. (C) MEG iso-contour map based on ictal MEG recordings. The map shows the distribution of the MEG field at the peak of the delta wave shown in Fig. 3. (D) Ictal SPECT. A hyperperfusion area was observed around the left sylvian fissure. Note that the interictal EEG/MEG dipoles corresponded well the hot area on this SPECT image. Furthermore, the MEG iso-contour map also suggested the epileptogenic area was located in the region of the left sylvian fissure.

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the interictal spikes were located in the left motor area, the pre-sylvian fissure, close to the location of the interictal MEG-estimated dipoles (Fig. 5A and B). Ictal MEG isocontour maps revealed a clear dipolar pattern suitable for modeling the source as a single equivalent current dipole, as shown in Fig. 5C. Magnetic flux was observed in the premotor area, which entered from behind the sylvian fissure. This dipolar field suggested that the MEG dipole was located in the area of the sylvian fissure; however, it could not be identified because the estimated dipoles did not have a sufficiently high GOF. Ictal SPECT revealed a hyperperfusion area around the left sylvian fissure, while MRI revealed no abnormal lesions (Fig. 5D). 3.3. Discussion In recent years, MEG has been used for the pre-surgical evaluation of epilepsy and it has proven to be useful for the localization of spike focus [3,4]. Several studies have suggested that MEG is useful in the placement of invasive electrodes, or in eliminating the need for such invasive procedures in some patients [2 – 4]. However, MEG has some limitations in that movement artifacts often obscure the accurate recording of cortical electrical activity. Consequently, there have been relatively few reports of ictal MEG studies since Stefan et al. [7] first reported on measuring ictal MEG activity using the multichannel MEG method. Furthermore, ictal MEG is rarely used in the diagnosis of childhood epilepsy [5,6], although there is an increasing number of reports on interictal MEG recordings [2,8]. In both of the subjects of the present study, we were able to perform ictal MEG successfully. Despite the fact that EEG and MEG recordings can be affected by movements of the eyes and facial muscles, the ictal recordings we obtained for the two patients in this study were not affected by motion artifacts. In case 1, this is because the MEG changes were most obvious in the posterior region of the head, which is least likely to be affected by eye movements. In case 2, the patient’s facial twitching was subtle and limited to her oral muscle, therefore, motion artifacts were not observed on her scalp EEG as shown in Fig. 3 of her EEG recording. The success of ictal MEG recording in these two cases was based on the nature of the patients’ seizures: the seizures were motionless and occurred at least 20 times per day. In case 1, we were able to obtain ictal MEG dipoles that corresponded well with the epileptic focus suggested by neuroimaging data and the patient’s clinical features. In this case, the ictal MEG dipoles were located in a more concentrated area than the interictal MEG dipoles, which were scattered into other areas. Eliashiv et al. [9] reported that the MEG-defined ictal onset zones were smaller than the irritative zone defined by source localizations of interictal spikes. They argued that ictal MEG was more useful than interictal MEG in estimating dipole location, especially in patients who show bilateral interictal abnormalities.

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In case 1, we were unable to estimate the location of the ictal dipole based on EEG recordings. The EEG field is affected by the conductivity of intervening tissue layers, such as skull and scalp, and has a diminished S/N ratio. Thus, the ictal EEG pattern is barely present before the discharges propagate outside the scalp. Furthermore, after this propagation, the dipolar field is distorted. Tilz et al. [10] also reported that ictal MEG dipoles yielded more detailed results than the corresponding EEG data, although they had fewer opportunities to record seizures using MEG. In case 2, ictal MEG showed delta bursts in an area that corresponded well with the epileptogenic zone estimated by other neuroimaging findings, in spite of the absence of marked ictal EEG changes. However, we were unable to estimate the dipole location in this patient with MEG. Although MEG is superior to EEG for the capture of earlier ictal changes, there may be some cases in which ictal MEG shows only the delta activity after the spread of ictal changes. In such cases, invasive recordings are necessary to detect the epileptogenic focus. However, it is still worth noting that MEG yielded valuable information about the nature of this patient’s seizures. Using ictal EEGs alone, we would not have been able to confirm her seizures as epileptic seizures. In conclusion, ictal MEG appears to be a useful tool for the definition of epileptic focus. Additional studies, including studies involving surgical confirmation of MEG findings, will be necessary to further determine the usefulness and limitations of this method.

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