Magnetoencephalogram in a Postoperative Case With a Large Skull Defect
after failed epilepsy surgery. Inc. All rights reserved.
© 2008 by Elsevier
Yoshinaga H, Kobayashi K, Hoshida T, Kinugasa K, Ohtuska Y. Magnetoencephalogram in a postoperative case with a large skull defect. Pediatr Neurol 2008;39: 48-51.
Introduction
Harumi Yoshinaga, MD*, Katsuhiro Kobayashi, MD*, Tohru Hoshida, MD†, Kazushi Kinugasa, MD‡, and Yoko Ohtuska, MD* We present a patient in whom magnetoencephalograms were successfully performed in presurgical and postsurgical evaluations. A 12-year-old boy with congenital porencephaly was admitted with refractory adversive seizures and frontal absence seizures. Ictal magnetoencephalographic dipoles with frontal absence seizures were located in the left frontal lobe, anterior to the porencephalic cyst, and concordant with the same area detected by intraoperative electrocorticography. A partial cortical excision was performed, and the patient’s cranial bone flap was removed because of an epidural abscess. The frontal absences then disappeared. The magnetoencephalogram revealed that secondary bilateral synchrony of focal discharges from the lesion may have caused the generalized seizures in this patient. Because of residual partial seizures, second and third magnetoencephalograms were performed, and we detected residual spike dipoles clustering in the area posterior to the cavity of cortical excision and anterior to the porencephalic cyst. Another excision of the area between the cavity and frontal edge of the cyst was performed, and seizure frequency diminished dramatically. In this case, despite the failure of dipole estimation by electroencephalogram in the context of a large bone defect, the magnetoencephalogram was useful in detecting the residual epileptogenic zone
From the *Department of Child Neurology, Okayama University Graduate School of Medicine, Dentistry, and Pharmaceutical Sciences, Okayama, Japan; †Department of Neurosurgery, Nara Prefectural Nara Hospital, Nara, Japan; and ‡Okayama Ryogo Center, Okayama, Japan.
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A magnetoencephalogram can often provide accurate dipole localization without interference from the changes in conductivity caused by intervening tissue layers, including those of the cranial bones. This is one of the major advantages of a magnetoencephalogram over an electroencephalogram. A few reports demonstrated the utility of magnetoencephalograms in evaluating patients with residual seizures after epilepsy surgery [1,2]. In these reports, the authors emphasized the merits of magnetoencephalograms in providing useful information in the diagnostic reevaluation of postoperative epileptic patients in whom skull and dura defects produced a “breach effect” which alters electroencephalograms. However, the skull defect in these reports was small, e.g., a crack produced by surgery. There have been few reports of postoperative magnetoencephalogram recordings with a large skull defect. We report on a patient with porencephaly-related epilepsy in whom a magnetoencephalogram was obtained before and after surgery. Postsurgical magnetoencephalogram dipoles were analyzed successfully despite the patient’s large skull defect in almost the entire left frontal bone. Case Report A 12-year-old boy with refractory, adversive seizures was admitted to Okayama University Hospital (Okayama, Japan) for presurgical evaluation. When the boy was 5 months old, computed tomography revealed left porencephaly, and he began to manifest complex, partial seizures at age 5 years. Despite multiple drug treatments, his seizures gradually became intractable, and occurred several times a day. We received informed consent from his parents for the following presurgical evaluation. He demonstrated mild right hemiparesis and mild mental deficiency. His visual field was normal. Frequent bilateral (left ⬎ right), frontal spike waves with occasional generalizations were observed on his electroencephalogram. His seizures consisted of right arm extension and rotation of his face and eyes to the right, followed by leg automatisms. A simultaneous electroencephalogram revealed an ictal pattern of the complex, partial seizures of
Communications should be addressed to: Dr. Yoshinaga; Department of Child Neurology; Okayama University Graduate School of Medicine, Dentistry, and Pharmaceutical Sciences; Shikatacho 2-5-1; Okayama 700-8558, Japan. E-mail:
[email protected] Received October 24, 2007; accepted March 10, 2008.
© 2008 by Elsevier Inc. All rights reserved. doi:10.1016/j.pediatrneurol.2008.03.010 ● 0887-8994/08/$—see front matter
frontal origin. We also discovered frontal absence seizures accompanied by diffuse 2-3 Hz/second spike-wave bursts over several seconds by video electroencephalogram monitoring. During his frontal absence seizures, he remained motionless, with vacant eyes and occasional face-twitching. This type of seizure was also recorded by a first simultaneous magnetoencephalogram-electroencephalogram. Magnetoencephalogram dipoles were analyzed using a 148-channel magnetometer (4-D Neuroimaging, San Diego, CA). Electroencephalogram dipoles were analyzed using equivalent current dipole localization software for Windows (SynaPointPro, GE Marquette Medical Systems, Tokyo, Japan). More detailed information concerning electroencephalogram and magnetoencephalogram dipole analyses is available in a previous report [3]. Interictal electroencephalogram dipoles were clustered in the posterior region of the left frontal lobe, adjacent to the margin of the porencephalic cyst. Both ictal and interictal magnetoencephalogram dipoles clustered in the same region estimated by electroencephalogram dipoles (Fig 1). In December 2003, the patient was admitted to Nara Prefectural Nara Hospital to undergo the first surgery. He underwent intraoperative electrocorticography and depth electrode recording before cortical resection under general anesthesia, using propofol. These procedures revealed a focal ictal pattern in the same region indicated by magnetoencephalogram. A cortical excision in the frontal area adjacent to the porencephalic cyst was performed, sparing the premotor area because of proximity to an eloquent cortex where residual epileptiform discharges were left unresected. The pathologic examination of the resected lesion revealed a malformation of cortical development. He experienced a wound infection that required debridement of the epidural abscess and removal of the bone flap (approximately 7.5 cm in diameter) in April 2004. After surgery, we confirmed by video electroencephalogram monitoring that his absence seizures disappeared. However, ⬍1 month after surgery, his complex partial seizures recurred. His residual seizures gradually increased up to 10-15 times a day. We again performed presurgical evaluation, including a second and third magnetoencephalogram in May and November 2004. Frequent bilateral (left ⬎ right), frontal spike waves with occasional generaliza-
Figure 1. Electroencephalogram (upper row) and magnetoencephalogram (lower row) dipoles before first surgery. Dots indicate locations of estimated dipoles for the peak of the interictal averaged spike. Note that the locations of electroencephalogram dipoles and magnetoencephalogram dipoles correspond well to each other. Dipoles of the left somatosensory-evoked field could not be estimated well because of the existence of massive spike discharges in the left central area.
Figure 2. Electroencephalogram (upper row) and magnetoencephalogram (lower row) dipoles after first surgery and just before second surgery. The cross indicates the location of the estimated dipoles for the left somatosensory-evoked field. The white line indicates the surgical cavity after the first cortical resection.
tions were observed on his electroencephalogram. His residual seizures were accompanied by the typical electroencephalogram features of complex, partial seizures with right or left frontal onsets. We failed to analyze the electroencephalogram dipoles scattered widely, including those in improbable areas, e.g., inside the ventricle and the porencephalic cyst. The second magnetoencephalogram dipoles were located in two areas: one posterior to the surgical cavity, and the other in the medial portion of the cyst. The third magnetoencephalogram dipoles clustered only in the former area (Fig 2). In January 2005, a second surgery was performed at Nara Prefectural Nara Hospital. An electrocorticography revealed epileptiform discharges in the left premotor and motor areas anterior to the cyst and posterior to the cavity of the previous surgery, where the residual epileptiform discharges remained unresected. An additional cortical excision was performed, including the facial motor area where the epileptic discharges were observed, sparing the hand motor area where they were not observed. We detected the central sulcus intraoperatively, using sensoryevoked potential (Fig 3A) to confirm the hand motor area (Fig 3B). An intraoperative photograph reveals the porencephalic cyst (Fig 3C) and resected area of the face motor area (Fig 3D) and premotor area (Fig 3E,F), where we observed electrocorticographic spikes. It also reveals the unresected area of the hand motor area (Fig 3B), where we observed neither electrocorticographic spikes nor magnetoencephalogram dipoles. The location of electrocorticographic spikes correlated well with the area of dipoles on the third magnetoencephalogram. After a seizure-free period of 1 year, the boy experienced one or two minor seizures per month in 2006, but they were not disabling. His electroencephalogram findings improved remarkably. In August 2006, he underwent cranioplasty.
Discussion Various types of surgeries are performed for porencephaly-related epilepsy, including lesionectomy, hemispherectomy, uncappeling, and cortical resection [4-7].
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Figure 3. Intraoperative photograph after second surgery. (A) Central sulcus, detected by intraoperative sensory evoked potential. (B) Hand motor area (unresected precentral cortex). (C) Porencephalic cyst. (D) Face motor area (resected precentral cortex). (E, F) Resected premotor cortex, where epileptic discharges and magnetoencephalogram dipoles were observed. (F) Appearance of falx after resection. (G) Cavity of first surgery.
Iida et al. [8] reported that cortical resections, including resections of the interictal epileptic areas that extend beyond the margins of the lesion, as guided by electrocorticography, constitute an effective surgical procedure. However, they also stated that intraoperative electrocorticography had some disadvantages because of the short and mostly interictal recordings, the effect of anesthesia, and the lack of full brain coverage. Based on our experience, we think that cases of a porencephalic cyst around the Rolandic region probably require a video electroencephalogram, a magnetoencephalogram study including a somatosensory-evoked field, magnetic resonance imaging, and a careful evaluation of the degree of hemiparesis, to understand the epileptogenic zone and motor function. In our patient, we were able to perform an ictal magnetoencephalogram of the frontal absence seizure, indicating its frontal origin. Some authors, including Iida et al. [8], proposed that bilaterally synchronous spike-andwave discharges might represent a secondary bilateral synchrony of the focal discharges originating from the porencephalic hemisphere. Bancaud et al. [9] indicated that localized stimulation of the frontal cortex could elicit electro-clinical absences. In our patient, after the resection of further anterior to magnetoencephalogram dipoles, only the frontal absence seizures disappeared. It appears that we removed the part of the network that produced secondary, bilateral, synchronous discharges in the first resection. Our experience seems to support the hypothesis of Bancaud et al. [9], i.e., frontal lesions can elicit absences. However, the epileptogenic zone of magnetoencephalogram dipoles remained, to produce residual, complex, partial seizures. After the complete resection of magnetoencephalogram dipoles in the second surgery, the residual, complex, partial seizures disappeared, indicating that the epileptogenic zone was completely resected.
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Two systematic studies of the application of magnetoencephalogram dipole analysis defined the residual epileptogenic area after failed epilepsy surgery [9,10]. These two studies demonstrated the utility of magnetoencephalograms in evaluating patients with residual seizures, emphasizing the merits of magnetoencephalograms even with the partial bone defect after epilepsy surgery without interference from changes in conductivity. Kanno et al. compared sensory-evoked magnetic field dipole locations pre- and postoperatively, and revealed that craniectomy had few effects on magnetic dipole analysis. However, the skull defect in these reports was small, e.g., a crack produced by surgery. On the contrary, the magnetoencephalogram in the present case was performed in the context of a large skull defect because of the removal of a frontal bone flap approximately 7.5 cm in diameter after wound infection. Using an experimental source model, Barth et al. [11] reported that gross heterogeneities in the resistance of the skull resulting from a craniectomy (approximately 7 cm in diameter) exerted a negligible effect on the extracranial magnetic field pattern. However, there are no published cases where such gross surgical skull defects are present. We also demonstrated here that porencephaly did not affect dipole localization with a magnetoencephalogram or an electroencephalogram. In contrast, a skull defect rendered electroencephalogram dipole estimation difficult, whereas it did not interfere with magnetoencephalogram dipole localization. Several studies, including our previous report, investigated the difference between magnetoencephalogram dipole and electroencephalogram dipole estimation preoperatively [3,12,13]. However, postoperative comparisons of these two techniques are not usually performed. It is well-known that distortion of the electroencephalogram signal easily occurs as the result of a hole in the skull [14]. In our patient, we present an actual example of a failure of electroencephalogram dipole estimations in the context of a postoperative skull defect. In conclusion, it is clear from the present patient that magnetoencephalograms are more useful than electroencephalograms in determining the residual epileptogenic zone after failed epilepsy surgery, even in patients who exhibit a large skull defect.
References [1] Kirchberger K, Hummel C, Stefan H. Postoperative multichannel magnetoencephalography in patients with recurrent seizures after epilepsy surgery. Acta Neurol Scand 1998;98:1-7. [2] Mohamed IS, Otsubo H, Ochi A, et al. Utility of magnetoencephalography in the evaluation of recurrent seizures after epilepsy surgery. Epilepsia 2007;48:2150-9. [3] Yoshinaga H, Nakahori T, Yoko O, et al. Benefit of simultaneous recording of EEG and MEG dipole localization. Epilepsia 2004;43:924-8. [4] Tinuper P, Andermann F, Villemure JG, Rasmussen TB, Quesney LF. Functional hemispherectomy for treatment of epilepsy associated with hemiplegia: Rationale, indications, results, and comparison with callosotomy. Ann Neurol 1988;24:27-34. [5] Ho SS, Kuzniecky RI, Gilliam F, Faught E, Bebin M, Morawetz
R. Congenital porencephaly and hippocampal sclerosis: Clinical features and epileptic spectrum. Neurology 1997;49:1382-8. [6] Koch CA, Krahling KH. Porencephalic cysts in children with epilepsy: Treatment by cyst fenestration. Ann Neurol 1999;45:547. [7] Carreño M, Kotagai P, Perez J, Mesa T, Bingaman W, Wyllie E. Intractable epilepsy in vascular congenital hemiparesis: Clinical features and surgical options. Neurology 2002;59:129-31. [8] Iida K, Otsubo H, Arita K, Andermann F, Olivier A. Cortical resection with electrocorticography for intractable porencephaly-related partial epilepsy. Epilepsia 2005;46:76-83. [9] Bancaud J, Talairacha J, Morel P, et al. “Generalized” epileptic seizures elicited by electrical stimulation of the frontal lobe in man. Electroencephalogr Clin Neurophysiol 1974;37:275-82. [10] Kanno A, Nakasato N, Nagamine Y, Shamoto H, Fujiwara S. Effect of craniectomy on current-dipole estimation in MEG [in Japanese]. J Jpn Biomag Bioelectromag 2005;18:122-3. [11] Barth DS, Sutherling W, Broffman J, Beatty J. Magnetic
localization of a dipolar current source implanted in a sphere and a human cranium. Electroencephalogr Clin Neurophysiol 1986;63: 260-73. [12] Ochi A, Otsubo H, Sharma R, et al. Comparison of electroencephalographic dipoles of interictal spikes from prolonged scalp videoelectroencephalography and magnetoencephalographic dipoles form short-term recording in children with extratemporal lobe epilepsy. J Child Neurol 2001;16:661-7. [13] Nakasato N, Levesque MF, Barth DS, Baumgartner C, Roger RL, Sutherling WW. Comparisons of MEG, EEG, and EcoG source localization in neocortical partial epilepsy in humans. Electroencephalogr Clin Neurophysiol 1994;171:171-8. [14] Flemming L, Wang Y, Caprihan A, Eiselt M, Hauseisen J, Okada Y. Evaluation of the distortion of EEG signals caused by a hole in the skull mimicking the fontanel in the skull of human neonates. Clin Neurophysiol 2005;116:1141-52.
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