Epilepsy Surgery Outcome in Coexisting Symptomatic Refractory Focal Epilepsy and Benign Focal Epilepsy of Childhood
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1 Epilepsy Surgery Outcome in Coexisting Symptomatic Refractory Focal Epilepsy and Benign Focal Epilepsy of Childhood Tim Wehner, MD*, Deepak K. Lachhwani, MD*, William Bingaman, MD*, Senay Haspolat, MD, Ajay Gupta, MD*, Prakash Kotagal, MD*, Ingrid Tuxhorn, MD*, and Elaine Wyllie, MD* Epilepsy surgery may successfully treat refractory symptomatic focal epilepsy in patients with coexisting benign focal epileptiform discharges. Reported here is the outcome after resective epilepsy surgery in three children with pharmacoresistant lesional focal epilepsy in whom seizures of benign focal epilepsy of childhood had been recorded. Two patients had left temporal epilepsy due to a malformation of cortical development; one of these had dual pathology, with additional ipsilateral hippocampal sclerosis. One child had catastrophic left hemispheric epilepsy due to left hemimegalencephaly. Frequent, habitual seizures of symptomatic epilepsy resolved after surgery (follow-up duration, months); however, rare benign focal seizures of childhood have continued. These cases demonstrate that lesional pharmacoresistant focal epilepsy can be successfully treated with resective epilepsy surgery even when coexisting with benign focal epilepsy of childhood. During postoperative follow-up, careful documentation of breakthrough seizures due to benign focal epilepsy of childhood is important, so that these patients are not labeled as surgical failures. Ó 2011 by Elsevier Inc. All rights reserved. Wehner T, Lachhwani DK, Bingaman W, Haspolat S, Gupta A, Kotagal P, Tuxhorn I, Wyllie E. Epilepsy surgery outcome in coexisting symptomatic refractory focal epilepsy and benign focal epilepsy of childhood. Pediatr Neurol 2011;44: Introduction Benign childhood focal epilepsy syndromes most likely reflect a genetically determined derangement of brain maturation. They comprise benign focal Rolandic epilepsy of childhood and occipital variants such as Panayiotopoulos syndrome [1]. Benign focal epileptiform discharges are incidentally identified with electroencephalography in approximately 2-3% of school aged children and are typically localized to the low or high central supra-sylvian electrodes; fewer than 10% of these children will develop benign focal epilepsy of childhood, a diagnosis established after manifest Rolandic seizures [2]. Seizures of benign focal epilepsy of childhood may be of low frequency (not requiring medications) or controlled easily with medications. Although patients with benign focal epileptiform discharges or benign focal epilepsy of childhood are typically neurologically intact and have normal findings on neuroimaging, a variety of brain lesions and more subtle imaging abnormalities have been described in patients with benign focal epileptiform discharges, including hippocampal asymmetry [3], malformations of cortical development [4], encephalomalacia [5], low grade astrocytoma, cavernous angioma [6], hydrocephalus, and agenesis of the corpus callosum [7]. Patients with symptomatic epilepsy due to brain lesions are more likely to have medically refractory seizures. Such patients may be suitable candidates for epilepsy surgery. Successful outcome after epilepsy surgery was achieved in three children who had benign focal epileptiform From the *Cleveland Clinic Epilepsy Center, Cleveland, Ohio; Interdisciplinary Epilepsy Center Marburg, Department of Neurology, Phillips University Marburg, Marburg, Germany; and Department of Pediatrics, Akdeniz University School of Medicine, Antalya, Turkey. The work reported here was presented in part at the 8th European Congress on Epileptology, Berlin, September Communications should be addressed to: Dr. Lachhwani; Epilepsy Center-S51; Cleveland Clinic; 9500 Euclid Avenue; Cleveland, OH lachhwd@ccf.org Received November 24, 2009; accepted July 6, PEDIATRIC NEUROLOGY Vol. 44 No. 1 Ó 2011 by Elsevier Inc. All rights reserved. doi: /j.pediatrneurol /$ - see front matter
2 discharges coexisting with pharmacoresistant temporal lobe epilepsy due to hippocampal sclerosis [8]. Reported here are the cases of three other patients with documented benign focal epilepsy of childhood (i.e., patients with seizures due to benign focal epileptiform discharges) who had successful epilepsy surgery for intractable seizures in the setting of malformation of cortical development. Patients and Methods After obtaining institutional review board approval, all pediatric epilepsy surgery patients were reviewed who, from 1998 to 2006 (n = 501), had benign focal epileptiform discharges documented (n = 7) during their epilepsy evaluation at Cleveland Clinic. Three of these had electrographic evidence of seizures due to benign focal epilepsy of childhood, in addition to pharmacoresistant lesional focal epilepsy. Case 1 An 8-year-old boy had onset of febrile seizures at 11 months of age. His symptomatic left temporal epilepsy started 1 year later, manifesting with complex partial seizures (staring, lip smacking, hand automatisms) progressing to frequent secondary generalization and occurring approximately once per week. He received speech therapy for mild language delay. Video electroencephalography revealed left temporal sharp waves (Fig 1A), and benign focal epileptiform discharges (low amplitude diphasic sharp waves in the left or right centrotemporal regions that occurred predominantly during sleep) (Fig 1B). Five habitual complex partial seizures were recorded, with electroencephalographic seizure onset in the left temporal region (Figs 1C and 1D). One additional seizure occurred with sudden arousal from sleep, followed by brief shivering of his entire body and drooling. Electrographically, this seizure evolved out of right temporal benign focal epileptiform discharges into a rhythmic alpha pattern (Figs 1E and 1F). Cranial magnetic resonance imaging demonstrated blurring of the gray-white matter and volume reduction in Figure 1. Presurgical electroencephalographic (EEG) and magnetic resonance imaging (MRI) findings in patient 1. (A) Left temporal sharp waves. (B) Bihemispheric independent benign focal epileptiform discharges. (C) Habitual automotor EEG seizure onset with low amplitude left temporal delta. (D) Approximately 30 seconds later, the seizure evolves into a rhythmic temporal theta pattern. (E,F) EEG seizure characterized by gradual evolution of right hemispheric benign focal epileptiform discharges into a rhythmic alpha pattern (F, 50 seconds later). (G,H) Coronal fluid-attenuated inversion recovery (FLAIR) and axial T 2 MRI reveal blurring of the gray-white matter junction and volume reduction in the left temporal pole, suggesting a malformation of cortical development. (I) Postoperative coronal FLAIR MRI visualizes the left temporal resection. Scale bar = 1 second (A-F). Wehner et al: Epilepsy surgery and BFEC 53
3 the left anterior temporal pole, suggesting a malformation of cortical development (Figs 1G and 1H). At the age of 5.5 years, he had a left anterior temporal resection including the mesial structures (Fig 1I). Histopathology confirmed a malformation of cortical development. His postoperative electroencephalogram at 6 months demonstrated right and left central benign focal epileptiform discharges. During 32 months of postoperative follow-up, he has experienced infrequent (3-5/year) seizures of benign focal epilepsy of childhood (generalized motor seizures, associated with drowsiness and intercurrent illness) on oxcarbazepine monotherapy. Complex partial seizures of left temporal epilepsy have not recurred since surgery. Case 2 An 11-year-old girl developed febrile status epilepticus at the age of 15 months, with ensuing pharmacoresistant symptomatic left temporal epilepsy. Her habitual monthly complex partial seizures started with nausea, followed by loss of awareness, aggressive behavior, and retching, coughing, or vomiting. In addition, she had rare seizures of benign focal epilepsy of childhood (2/year nocturnal right hemibody clonic seizures managed with rectal diazepam pro re nata). Video electroencephalography obtained at 6 years of age revealed left temporal and left centroparietal sharp waves, the latter with a morphology akin to benign focal epileptiform discharges with a broad distribution over P3/C3 and Pz/Cz, with shifting predominance and a great abundance during sleep (Fig 2A). Two habitual complex partial seizures with electroencephalographic onset over the left temporal region were recorded (Fig 2B). Cranial magnetic resonance imaging demonstrated loss of normal gray-white matter delineation of the left temporal pole. The patient had a standard left anterior temporal lobectomy at 6 years of age. Histopathology revealed hippocampal sclerosis, microscopic dysplastic foci in the parahippocampal gyrus, and subpial gliosis in the lateral temporal lobe. She has remained free of complex partial seizures arising from the left temporal lobe for 55 months. However she continues to have rare Rolandic seizures (<1-2/year, <2-3 minutes in duration), including a single prolonged event at 30 months after surgery, correlating with benign focal epileptiform discharges (throat gurgling, face tingling, and twitching; all nocturnal or precipitated by sleep deprivation). The longer seizure occurred during a sleep-deprived electroencephalogram and was characterized by right facial twitching, followed by forced eye deviation to the right without loss of awareness. Figure 2. Pre- and postoperative EEG findings in patient 2. (A) Preoperative interictal left temporal and centroparietal sharp waves with a morphology akin to benign focal epileptiform discharges. (B) Preoperative ictal onset of a habitual automotor seizure characterized by rhythmic left temporal delta slowing. The amplitude is much higher in the TP9-TP10 channel compared to the SP1-SP2 channel, suggesting a neocortical seizure focus. (C) Right face clonic seizure recorded 2.5 years postoperatively. Seizure onset characterized by left temporal benign focal epileptiform discharges that evolve into a rhythmic alpha pattern 60 seconds later (D). Note the different amplitude between left and right hemispheric channels to accommodate the EMG artifact in the right temporal chain. Scale bar = 1 second. 54 PEDIATRIC NEUROLOGY Vol. 44 No. 1
4 Figure 3. Pre- and postoperative EEG and MRI findings in patient 3. (A) Preoperative right parietal sharp wave, followed by an epileptic spasm characterized by diffuse electrodecrement. (B) Right face motor seizure onset characterized by evolving left centroparietal sharp waves. (C) Axial T 2 MRI demonstrates diffusely abnormal architecture of the left hemisphere. (D) At 2.5 years postoperatively, postictal EEG shows diphasic right occipital sharp waves with morphology resembling benign focal epileptiform discharges. Scale bar = 1 second (A,B,D). The ictal electroencephalogram evolved from benign focal epileptiform discharges in the left centrotemporal region (Figs 2C and 2D). This was a prolonged event (3 hours long) and required treatment with intravenous lorazepam, valproic acid and phenobarbital. As of writing, she was on topiramate and lamotrigine pharmacotherapy, and avoids sleep deprivation to prevent seizures. Case 3 A boy presented at the age of 2 months with catastrophic epilepsy due to left hemimegalencephaly. Since his third neonatal day, he had experienced several daily clusters of epileptic spasms and seizures characterized by right facial grimacing followed by secondary generalized motor seizures. On examination, he evidenced reduced spontaneous movements and hypotonia in his right extremities. Video electroencephalography indicated modified left hemisphere hypsarrhythmia with reduced background amplitude. Epileptic spasms were associated with a generalized suppression on the electroencephalogram (Fig 3A). Right face tonic seizures with secondary generalization began with a left centroparietal theta rhythm that evolved over the left or both hemispheres (Fig 3B). Cranial magnetic resonance imaging revealed left hemimegalencephaly with an extensive malformation of cortical development involving the entire left cerebral hemisphere (Fig 3C). In view of his catastrophic epilepsy, he had a left anatomic hemispherectomy at the age of 10 weeks. Histopathology revealed marked cortical dysplasia with microcalcifications. He remained seizure free for 28 months; at 2.5 years of age he had a nocturnal convulsion (snorting noises, foaming at the mouth, and diffuse stiffening) with a febrile illness. Two days later, his electroencephalogram indicated right occipital diphasic sharp waves with characteristic morphology of benign focal epileptiform discharges (Fig 3D). During 55 months of postoperative follow-up, he has experienced intermittent (few/year) nocturnal seizures documented on video electroencephalography and not incompatible with benign focal epilepsy of childhood, while remaining cured of the catastrophic left hemispheric epilepsy due to hemimegalencephaly. Discussion Three patients with refractory symptomatic epilepsy and coexisting benign focal seizures had successful resective epilepsy surgery for lesional pharmacoresistant focal epilepsy. All three children were free of their habitual seizures due to symptomatic epilepsy, which had defined their preoperative epilepsy burden. The reported or observed clinical features (interictal electroencephalography, semiology, Wehner et al: Epilepsy surgery and BFEC 55
5 sleep dependence) of isolated postoperative seizures were consistent with benign focal epilepsy of childhood. Although some features (status epilepticus in patient 2, atypical spike location in patient 3) are unusual, they are not incompatible with this diagnosis [9]. A more posterior distribution of spikes is frequently seen, with subsequent anterior migration [9]. An alternative explanation for the postoperative seizures observed in the present cases, such as medical intractability secondary to more extensive malformations of cortical development, cannot be entirely excluded. The natural course of benign focal epilepsy of childhood includes remission of seizures by years of age; this, however, can be judged only with longer follow-up. Few studies have addressed the relationship between surgery for lesional epilepsy and benign focal epileptiform discharges. In a previous report, epilepsy surgery was successful in three children with temporal lobe epilepsy due to hippocampal sclerosis who were initially dismissed as surgical candidates because of abundant bihemispheric benign focal epileptiform discharges [8]. Two similar cases are described as patients 2 and 3 in the series by Degen et al. [10], although hippocampal sclerosis is explicitly mentioned in only one case. Finally, there is one report of a patient in whom parietooccipital benign focal epileptiform discharges were the only type of interictal epileptiform activity, but seizure semiology, ictal electroencephalograph, magnetic resonance imaging, and ictal single-photon emission computed tomography concordantly localized the epileptogenic zone to the left frontal lobe; this patient became seizure free after resection of a left frontal cortical dysplasia [11]. Benign focal epilepsy of childhood is a common problem facing pediatric neurologists and epileptologists, and coexistence of benign focal epilepsy of childhood with lesional epilepsy may be purely coincidental. Children with benign focal epileptiform discharges only, or with benign focal epilepsy of childhood (interictal discharges and clinical seizures), as well as migraine headaches may have subtle findings on magnetic resonance imaging without apparent clinical implication [3,12]. Whereas benign focal epileptiform discharges are considered an autosomal dominant trait with variable penetrance affecting brain maturation [9], a recent study in twins failed to demonstrate concordant benign focal epilepsy of childhood in twin siblings of 18 patients with benign focal epilepsy of childhood, suggesting that nongenetic factors are more important for the manifestation of benign focal epilepsy of childhood [13]. It is therefore conceivable that patients with lesional pharmacoresistant epilepsy who harbor the trait for benign focal epileptiform discharges are more likely to experience seizures due to benign focal epileptiform discharges (i.e., benign focal epilepsy of childhood) than are children without confounding epilepsy. Most children with benign focal epilepsy of childhood experience fewer than 10 seizures altogether. The cases presented here illustrate the importance of recognizing and further investigating those children who exhibit additional complicating features, such as higher seizure frequency, several seizure types, and poor response to anticonvulsants. In conclusion, lesional pharmacoresistant focal epilepsy can be successfully treated with resective epilepsy surgery even when coexisting with benign focal epilepsy of childhood. Careful documentation of breakthrough seizures during postoperative follow-up due to benign focal epilepsy of childhood is important, to avoid mislabeling these patients as surgical failures. The authors acknowledge the help of Richard Burgess, MD, PhD of the Cleveland Clinic Epilepsy Center in Cleveland, OH for helping with the database search. References [1] Panayiotopoulos CP, Michael M, Sanders S, Valeta T, Koutroumanidis M. Benign childhood focal epilepsies: assessment of established and newly recognized syndromes. Brain 2008;131: [2] Lüders H, Lesser RP, Dinner DS, Morris HH. Benign focal epilepsy of childhood. In: Lüders H, Lesser RP, editors. Epilepsy: electroclinical syndromes. New York: Springer, 1987: [3] Lundberg S, Eeg-Olofsson O, Raininko R, Eeg-Olofsson KE. Hippocampal asymmetries and white matter abnormalities on MRI in benign childhood epilepsy with centrotemporal spikes. Epilepsia 1999;40: [4] Sheth RD, Gutierrez AR, Riggs JE. Rolandic epilepsy and cortical dysplasia: MRI correlation of epileptiform discharges. Pediatr Neurol 1997;17: [5] Stephani U, Doose H. Benign idiopathic partial epilepsy and brain lesion. Epilepsia 1999;40: [6] Shevell MI, Rosenblatt B, Watters GV, O Gorman AM, Montes JL. Pseudo-BECRS : intracranial focal lesions suggestive of a primary partial epilepsy syndrome. Pediatr Neurol 1996;14:31-5. [7] Gelisse P, Corda D, Raybaud C, Dravet C, Bureau M, Genton P. Abnormal neuroimaging in patients with benign epilepsy with centrotemporal spikes. Epilepsia 2003;44: [8] Pan A, Gupta A, Wyllie E, Lüders H, Bingaman W. Benign focal epileptiform discharges of childhood and hippocampal sclerosis. Epilepsia 2004;45: [9] Wirrell EC, Camfield CS, Camfield PR. Idiopathic and benign partial epilepsies of childhood. In: Wyllie E, Gupta A, Lachhwani DK, editors. The treatment of epilepsy: principles and practice. 4th ed. Philadelphia: Lippincott Williams & Wilkins, 2006: [10] Degen R, Holthausen H, Pieper T, Tuxhorn I, Wolf P. Benign epileptic discharges in patients with lesional partial epilepsies. Pediatr Neurol 1999;20: [11] Altenmüller DM, Schulze-Bonhage A. Differentiating between benign and less benign: Epilepsy surgery in symptomatic frontal lobe epilepsy associated with benign focal epileptiform discharges of childhood. J Child Neurol 2007;22: [12] Boxerman JL, Hawash K, Bali B, Clarke T, Rogg J, Pal DK. Is rolandic epilepsy associated with abnormal findings on cranial MRI? Epilepsy Res 2007;75: [13] Vadlamudi L, Kjeldsen MJ, Corey LA, et al. Analyzing the etiology of benign rolandic epilepsy: a multicenter twin collaboration. Epilepsia 2006;47: PEDIATRIC NEUROLOGY Vol. 44 No. 1
6 ID Title Pages Epilepsy Surgery Outcome in Coexisting Symptomatic Refractory Focal Epilepsy and Benign Focal Epilepsy of Childhood 5
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