Epilepsy & Seizure
Online ISSN : 1882-5567
ISSN-L : 1882-5567
Brief Communication
Detection of subtle periictal hyperperfusion with 1.5-Tesla arterial spin labeling perfusion imaging in a patient with congenital unilateral perisylvian syndrome in a neurological emergency
Takato Morioka, Fumihito Mugita, Satoshi Inoha, Yoshimasa Kinoshita, Tomoaki Akiyama, Takafumi Shimogawa, Nobutaka Mukae, Ayumi Sakata, Hiroshi Shigeto, Koji Yoshimoto
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Keywords: Arterial spin labeling, Electroencephalography, Neurological emergency, Periictal hyperperfusion, Perisylvian syndrome, Polymicrogyria
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2025 Volume 17 Article ID: A000164

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Abstract

We made a pathophysiological diagnosis of epileptic seizures in a 50-year-old male with congenital unilateral perisylvian syndrome due to right perisylvian polymicrogyria, using routine electroencephalography (EEG) and 1.5-Tesla arterial spin labeling (ASL) magnetic resonance perfusion imaging. No paroxysmal discharges were recorded on EEG performed 1 h after the generalized convulsive seizure. Pseudo-continuous and pulsed ASL images taken 1 h 30 min and 1 h 15 min after the seizure, respectively, captured subtle periictal hyperperfusion linked to seizure activity via neurovascular coupling at the perisylvian area. In particular, the fusion of ASL images with the sagittal view of a three-dimensional T1-weighted image clearly revealed periictal hyperperfusion at the area of polymicrogyria, indicating intrinsic epileptogenicity. This case report details how adding ASL to routine EEG data can be useful in the pathophysiological diagnosis of epilepsy in neurological emergencies.

Introduction

Congenital bilateral perisylvian syndrome is a rare disease associated with cortical polymicrogyria around the bilateral Sylvian fissures, which causes epileptic seizures, dysarthria, dysphagia, spastic paralysis predominantly affecting the upper limbs, intellectual disability, and higher brain dysfunction[1]. Congenital unilateral perisylvian syndrome caused by unilateral polymicrogyria has also been reported[2].

In the context of imaging of ictal or periictal hyperperfusion linked to seizure activity by neurovascular coupling in congenital perisylvian syndrome, single photon emission computed tomography (SPECT) has revealed ictal hyperperfusion at the perisylvian polymicrogyria itself, mainly as a preoperative examination for epilepsy surgery[3, 4]. However, the use of SPECT is not feasible in neurological emergencies[5]. We previously reported that capturing periictal hyperperfusion using arterial spin labeling (ASL) perfusion magnetic resonance (MR) imaging, which is completely non-invasive and can be performed 24 h a day, is useful in diagnosing the pathophysiology of epileptic seizures[6,7,8,9,10,11,12].

The quality of ASL images is determined by the effectiveness of labeling[5, 8,9,10,11,12]. 3-Tesla (T) MR machines generally provide better ASL images than 1.5-T MR machines, since it is more useful in higher magnetic fields. However, only a limited number of neurological emergency facilities in Japan are equipped with 3-T MR machines[5, 8,9,10,11,12]. Furthermore, there are two types of labeling methods in clinical practice: pulsed ASL (PASL), which is a classical method that uses only single-pulse labeling for ASL, and pseudo-continuous ASL (cCASL), which is a more recent method that uses numerous labels with high frequency; the latter provides superior ASL images[5, 11]. The drawback of pCASL is that it can only be installed on a limited number of MR machines. Therefore, although 3-T pCASL provides the best images at present, 1.5-T ASL is generally used in neurological emergency facilities[5, 8,9,10,11,12].

Although there has been a single case report of periictal hyperperfusion in perisylvian syndrome using 3-T pCASL[13] as a preoperative examination for epilepsy surgery, no reports have described the use of 1.5-T ASL in neurological emergencies. We report a case of congenital unilateral perisylvian syndrome in which subtle periictal hyperperfusion was detected using both pCASL and PASL on a 1.5-T MR machine.

Case Report

A 50-year-old man with mild intellectual disability and left hemiparesis experienced generalized seizures at 5 years of age. Antiseizure medication (ASM) was initiated to control the seizures, and the patient became seizure-free at 13 years of age. ASM was discontinued at the age of 18 years. He started experiencing generalized seizures again at the age of 20 years, and ASM was resumed. With 700 mg of carbamazepine and 100 mg of topiramate (TPM), he experienced focal impaired awareness seizures (FIAS) 2-3 times a month and focal to bilateral tonic-clonic seizures (FBTCS) 2-3 times a year.

The patient was transferred to our hospital at 48 years of age. Axial T1-weighted imaging (T1WI) revealed shallow sulci in the fronto-temporal lobes around the right Sylvian fissure, and the cortex appeared pachygyric (Fig. 1A). A thin-slice (slice thickness 1.20 mm) sagittal section of a three-dimensional T1WI (3DT1WI) demonstrated polymicrogyria in the same area (Fig. 1B); the cortex in the corresponding area on the left side had a normal structure (Fig. 1C). Polymicrogyria were particularly dense in the right superior and middle temporal gyri (Fig. 1B, red arrows). Further, the original superior temporal sulcus between the two was very poorly developed compared to the left side (Fig. 1C, red arrows) and was partially continuous with the Sylvian fissure. Interictal electroencephalography (EEG) revealed slow waves in both frontal regions, predominantly on the left side, and no paroxysmal discharges (Fig. 2A). With a diagnosis of right-sided unilateral perisylvian syndrome, the TPM dose was increased to 300 mg. As a result, FBTCS did not occur, and FIAS were almost controlled.

Fig. 1.

(A-C) Morphological MRI. Axial view of T1WI (A) and serial sagittal views of 3DT1WI on the right (B) and left (C) of the perisylvian areas. (D-R) Fusion pCASL images with morphological MRI, imaged 1 h 30 min after FBTCS at the age of 49 years. Fusion pCASL images with axial view of T1WI at PLDs of 1.5 s (D), 1.75 s (E) and 2.0 s (F), and with serial sagittal views of 3DT1WI at PLDs of 1.5 s (G, J), 1.75 s (H, K) and 2.0 s (I, R).

MRI, magnetic resonance imaging; T1WI, T1-weighted image; 3DT1WI, three-dimensional T1WI; pCASL, pseudo-continuous arterial spin labeling; FBTCS, focal to bilateral tonic-clonic seizure; PLD, post-labeling delay.

Pseudo-continuous ASL was performed using a 1.5-Tesla scanner (ECHELON OVAL V6; FUJIFILM Healthcare, Tokyo, Japan) equipped with a 15-channel receive-only head coil for signal reception, as previously described[8,9,10,11,12]. ASL was performed using a three-dimensional gradient and spin-echo sequence with background suppression for perfusion imaging of the entire brain. The acquisition parameters were as follows: phase encoding in the z-direction, 28; time to repeat, 4291 ms; echo time, 17.4 ms; field of view, 250 mm; matrix, 128 × 128; slice thickness, 6 mm; reconstruction interval, 3 mm; and number of slices, 48. The labeling duration was 1.5 s. Three post-labeling delays (PLDs) of 1.5 s, 1.75 s, and 2.0 s were selected. The ASL acquisition times for each PLD were 3 min and 1 s.

Fig. 2.

(A) Interictal EEG. (B) periictal EEG performed 1 h after FBTCS at the age of 49 years. (C) Source image of MRA. (D, E) Fusion PASL images with source image of MRA at PLDs of 1.5 s (D) and 2.0 s (E), imaged 1 h 15 min after FBTCS at the age of 47 years.

EEG, electroencephalography; FBTCS, focal to bilateral tonic-clonic seizure; MRA, magnetic resonance angiography; PASL, pulsed arterial spin labeling; PLD, post-labeling delay.

PASL was performed using a 1.5-Tesla scanner (MAGNETOM Amira; Siemens, Erlangen, Germany), equipped with a 16-channel head/neck coil. A 3-D turbo gradient spin-echo was used as previously described[11]. The acquisition parameters were as follows: phase encoding in the z-direction, 24; time to repeat, 500 ms; echo time, 51 ms; field of view, 256 mm; matrix, 62×64, slice thickness, 5.5 mm, and number of slices, 24. Two PLDs (inversion times) of 1,500 ms (1.5 s) and 1,990 ms (2.0 s) were selected. The ASL acquisition times for each PLD were 4 min and 15 s.

At the age of 49, he experienced a few minutes of FBTCS triggered by lack of sleep and was transported to our hospital by ambulance approximately 30 min later. The seizure ceased upon arrival. EEG was performed approximately 30 min after transport, or approximately 1 h after the seizure. Slow waves were prominent, predominantly in the left frontal lobe, and no obvious paroxysmal discharges were recorded (Fig. 2B).

MRI including pCASL was performed 1.5 h after the seizure. No high signal intensity was observed on diffusion-weighted images. Fusion of pCASL images with axial T1WI images showed mild signal elevation in the fronto-temporal cortex around the Sylvian fissure at a post-labeling delay (PLD) of 1.5 s (Fig. 1D, white arrows), attenuation at a PLD of 1.75 s (Fig. 1E, white arrows), and minimal signal elevation at a PLD of 2.0 s (Fig. 1F, white arrows). Fusion of pCASL images with sagittal 3DT1WI showed that the signal intensity increased at a PLD of 1.5 s (Fig. 1G, white arrows), decreased at a PLD of 1.75 s (Fig. 1H, white arrows), and remained very slight at a PLD of 2.0 s (Fig. 1I, white arrows), corresponding to the polymicrogyria in the fronto-temporal lobes around the right Sylvian fissure, compared to that of the contralateral healthy cortex (Fig. 1J-R). In particular, the signal intensity increased in the right superior and middle temporal gyri, where polymicrogyria were densely present (Fig. 1G middle and lower rows, white arrows).

We show fusion of PASL with source images of MR angiography (MRA) (Fig. 2C-E) imaged 1 h and 15 min after a seizure lasting 2 min at the age of 47. A mild signal elevation at the fronto-temporal cortex around the right Sylvian fissure was observed at a PLD of 1.5 s (Fig. 2D, white dotted arrows), which remained very slight at a PLD of 2.0 s (Fig. 2E). The areas with the highest signal elevation corresponded to the Sylvian fissure and the cortical sulcus, particularly the arteries within them (Fig. 2C, red arrows; Fig. 2D, white arrows), which remained very slight at a PLD of 2.0 s (Fig. 2E, white arrows).

Discussion

In this case, both pCASL and PASL visualized periictal hyperperfusion associated with unilateral perisylvian polymicrogyria at a PLD of 1.5 s. Compared to our previous reports on 1.5-T ASL[8,9,10,11,12], it was visually subtle and only a slight signal remained at a PLD of 2.0 s. Visualization of periictal ASL hyperperfusion depends on the intensity and duration of the original seizure as well as the time until imaging[6, 7]. In this case, pCASL and PASL were performed 1 h 30 min and 1 h 15 min after the seizure, respectively, and the intensity of the original FBTCS was presumably lower with a shorter duration.

We have emphasized the importance of creating fusion ASL images with anatomical images to demonstrate such subtle changes on 1.5-T ASL[8,9,10,11,12]. In such cases, it is important to fuse it with an anatomical image that most clearly depicts the epileptogenic lesion. The 3DT1WI provides a good contrast between gray and white matter; therefore, thin slices of the sagittal view are excellent for depicting perisylvian polymicrogyria[13]. The fusion of ASL images with 3DT1WI revealed periictal hyperperfusion to be consistent with perisylvian polymicrogyria, indicating the intrinsic epileptogenicity of cortical dysplasia[14]. However, obtaining 3DT1WI is time consuming, which makes it difficult to perform the procedure within the limited imaging time available in neurological emergency settings. Therefore, it is necessary to capture images in advance during the interictal period, as was done in this case.

Regarding PASL, we did not perform 3DT1WI, which can be used for fusing. Compared to pCASL, PASL is more likely to be contaminated by intravascular signals, that is, arterial transit artifacts (ATA)[5, 8,9,10,11,12]. Therefore, when the PASL image was fused with the source image of MRA, the area with the highest signal increase at a PLD of 1.5 s corresponded to the Sylvian fissure and cortical sulcus, especially its arteries; this was identified as ATA of the distal segment of the middle cerebral artery (MCA)[8, 9, 11]. Since the periphery of the MCA also supplies perisylvian polymicrogyria, we believe that the ATA is involved in periictal hyperperfusion[9]. In addition, we previously reported that subtraction of the ictal (or periictal)-interictal ASL co-registered with conventional MR images (SIACOM) is useful for enhancing periictal hyperperfusion[5, 8,9,10,11,12]. However, in this study, we were unable to create a SIACOM because we did not perform interictal ASL.

Moreover, EEG was recorded before pCASL imaging. Although the overall slow-wave component increased, indicating a postictal state, no paroxysmal discharges were observed. Based on the results of simultaneous intracranial and extracranial EEG recordings, which we performed as a preoperative examination for epilepsy surgery, we reported that ictal discharges occurring in the lateral cortex with an amplitude of 200-2000 μV or more and synchronized with a range of more than 8-15 cm2 could be recorded using scalp EEG, mainly owing to the smearing effect[15]. Although this is a single case report, ASL may have overcome the weakness of EEG, and the results indicate that adding ASL to routine EEG, even with a 1.5-T MR machine, can be useful in diagnosing the pathophysiology of epilepsy[5, 8,9,10,11,12].

Acknowledgments

We thank Ryoji Shiraki and colleagues at the Hachisuga Hospital, for supporting our study. We thank Editage for editing the manuscript.

Informed Consent

The authors confirm that written informed consent was obtained from the patient. Ethical approval was obtained from the Institutional Review Board of the Hachisuga Hospital (No. 22-1).

Conflict of Interest Disclosure

The authors declare that they have no conflicts of interest.

References
 
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