Orbitofrontal resections for intractable partial seizures

Orbitofrontal resections for intractable partial seizures

I"~UTT E RWO RTH IIIEIN EMA---- Orbitofrontal Resections for Intractable Partial Seizures 1Steven N. Roper and 2Robin L. Gilmore The orbitofrontal...

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Orbitofrontal Resections for Intractable Partial Seizures 1Steven N. Roper and 2Robin L. Gilmore

The orbitofrontal cortex has extensive connections with limbic structures that are often involved in intractable partial seizures. Although some cases of orbitofrontal epilepsy have been reported, the exact incidence and optimal means of diagnosis and treatment of this condition are not well established. For I year, we included recordings from the orbitofrontal cortex in all cases of limbic epilepsy that required invasive monitoring as part of a preoperative workup. We identified 3 cases in which orbitofrontal resections were performed to control intractable partial seizures. In 1 case, an orbitofrontal resection based on physiologic data disclosed an area of focal cortical dysplasia that had not been identified by preoperative structural and functional imaging. In the second case, the adjacent orbitofrontal area was resected concurrently with a dominant anterior temporal lobectomy (ATL). In the third case, a patient was seizure-free for 6 years after an ATE The seizures recurred, however, and an orbitofrontal resection was performed on the same side as the original surgery. These patients had no unique EEG or semiology profile that identified orbitofrontal seizures before invasive recordings were made. The orbitofrontal cortex may be the source of intractable partial seizures, and this should be considered in electrode implantation strategies for the preoperative evaluation of patients with this disorder. Key Words: Partial epilepsy-Frontal lobe~Surgery.

The orbitofrontal region of the frontal lobe has b e e n s u s p e c t e d and, in some cases, p r o v e n to be i n v o l v e d in the g e n e r a t i o n of partial seizures (1-6). H o w e v e r , its location m a k e s it difficult to m o n i t o r w i t h n o n i n v a s i v e EEG. A l t h o u g h some centers h a v e r e p o r t e d d e p t h electrode studies of this region, it is not r o u t i n e l y targeted for invasive inves-

Received February 3, 1995; accepted February 7, 1995. From the Departments of 1Neurological Surgery and 2Neurology, University of Florida, Gainesville, FL, U.S.A. Address correspondence and reprint requests to Dr. Steven N. Roper at Department of Neurological Surgery, University of Florida, P.O. Box 100265, Gainesville, FL 32610-0265, U.S.A.

J. Epilepsy 1995;8:146-152 © 1995 by Elsevier Science Inc. 655 Avenue of the Americas, New York, NY 10010

tigations in limbic epilepsy. S o m e r e p o r t s h a v e suggested a p a t h o g n o m o n i c EEG a p p e a r a n c e for orbitofrontal seizures (6), b u t this has not b e e n a consistent finding (3,4,7). Published case reports have not identified a specific s e m i n o l o g y for this seizure type. Because of these uncertainties, all patients with intractable limbic epilepsy requiring invasive recording of the mesial t e m p o r a l structures, either b y i n t r a p a r e n c h y m a l or subdural electrodes, also u n d e r w e n t r e c o r d i n g of the adjacent orbitofrontal region with subdural strip electrodes at our institution. We r e p o r t 3 patients w i t h intractable limbic epilepsy in w h o m these recordings identiffed seizure onset in the orbitofrontal cortex, in w h i c h surgical resections w e r e p e r f o r m e d for control of seizures.

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RESECTIONS FOR ORBITOFRONTAL SEIZURES

Methods Three cases in which seizures originated in the orbitofrontal cortex were identified from a group of 15 patients with intractable limbic seizures who u n d e r w e n t invasive monitoring of either one or both temporal lobes and orbitofrontal regions from March 1, 1993 to February 28, 1994. Bitemporal depth electrodes with bilateral orbitofrontal and inferolateral temporal subdural strip electrodes were performed in 7 patients. Unilateral temporal, frontal, and orbitofrontal subdural electrodes were placed in 8 patients. In both the bilateral and unilateral investigations, a single subdural strip electrode was used to sample the orbitofrontal cortex. Of patients not described in the current report, 11 u n d e r w e n t anterior temporal lobectomy (ATL) and 1 was not offered surgery. During this period, 7 patients u n d e r w e n t ATL based on a noninvasive evaluation that included neurologic and neuropsychologic examinations, scalp/sphenoidal videoEEG monitoring, structural and functional imaging studies, and Wada testing. All references to scalp/ sphenoidal electrode positions are in accordance with the modified, combinatorial 10-20 nomenclature (8).

Case Reports Case 1

A 17-year-old, right-handed girl presented after 2 years of daily, intractable partial complex seizures. Perinatal and childhood history were unremarkable. Her auras consisted of a bad taste or smell and an awareness of an accelerated heart rate. Clinical features of the seizure consisted of staring and occasional manual automatisms. Postictal periods were characterized by confusion. The patient's neurologic examination was normal. Scalp/sphenoidal EEG telemetry showed interictal spikes predominating over the right mesial temporal (Sp2) and midtemporal (T8) lobe. Ictal onset was characterized by 2-Hz delta activity apparent at F4 and T8 for 4-8 s, evolving into bifrontal and right midtemporal (T8) delta with simultaneous phase reversal of sharp waves at Sp2. Although this was consistent with mesiotemporal onset, it raised the possibility of a deep frontal origin with rapid propagation to the mesial temporal structures. Magnetic resonance imaging (MRI) scans were interpreted as unremarkable by neuroradiologists, neurologists, and neurosurgeons. MRI-

based quantitative hippocampal volumetrics showed no asymmetry (9). Interictal [18F]fluorodeoxyglucose positron emission tomography (PET) was unremarkable. Performance I.Q. was 84, and verbal I.Q. was 97. Wada testing showed language dominance in the left hemisphere and that global m e m o r y was supported by either h e m i s p h e r e w h e n isolated. Bilateral subtemporal and orbitofrontal subdural strip electrodes were placed. Two ictal events originated in central and lateral contacts of the right orbitofrontal strip electrode before spreading to the right subtemporal strip. Because of concerns that a hippocampal or amygdalar onset was not detected by the subtemporal strip electrodes, she returned to surgery for stereotaxic placement of bitemporal depth electrodes through occipital burr holes. Two additional ictal events confirmed an orbitofrontal seizure onset. The patient underwent a right frontotemporal craniotomy, removal of electrodes, intraoperative electrocorticography (ECoG), and resection of orbitofrontal cortex. ECoG was u s e d to define boundaries of the epileptogenic area that could not be outlined by strip electrodes alone. Interictal spikes localized to the lateral portion of the orbitofrontal cortex. The resection included both the central orbitofrontal cortex implicated by ictal monitoring as well as the more lateral area defined by ECoG. While the cortical resection was being completed through the white matter, an abnormally firm mass of tissue that was slightly discolored was encountered and incorporated into the specimen (Fig. 1). Pathologic examination of the tissue showed a focal cortical dysplasia (Fig. 2). Postoperatively, the patient had no significant neurologic or neuropsychologic deficits. She was seizure-free at 17-month postoperative follow-up and continues to be treated with antiepileptic drugs (AEDs). Retrospective examinations of the MRI and PET scans failed to show an abnormality in the region of the cortical dysplasia.

Case 2

A 42-year-old, right-handed w o m a n had had intractable seizures since age 13 years. Perinatal and childhood history was unremarkable. Most seizures occurred during sleep, and she was unaware of any auras. Seizures consisted of staring and unresponsiveness. Neurologic examination was normal. Neuropsychologic testing identified nonlateralizing deficits in mental tracking, sequencing, and J EPILEPSY, VOL. 8, NO. 2, 1995 147

S. N. ROPER AND R. L. GILMORE

A

Figure 1. Postoperative sagittal (A) and coronal (B) T1weighted MRI images of Patient 1 demonstrating the surgical defect in the right orbitofrontal cortex. The area of deeper resection represents the site of focal cortical dysplasia.

attentional abilities suggestive of frontal lobe dysfunction. Scalp/sphenoidal EEG telemetry demonstrated independent, bitemporal interictal spikes predom148 J EPILEPSY, VOL. 8, NO. 2, 1995

inating on the left side (20:1). Six ictal events were recorded. Three had bifrontotemporal onset. One seizure was characterized by widespread 2-Hz rhythmic delta for 6 s apparent at FP1, F7, T7, P7, Spl, Sp2, A1, and A2 and evolving into 8-Hz rhythmic theta. Two other seizures demonstrated synchronous bifrontal and bitemporal rhythmic, notched 5-Hz activity which was maximal at Sp2. This suggested the possibility of bitemporal or frontal origin. Three seizures began in the left mesial temporal region. Interictal PET scan showed a 10% qualitative decrease in glucose metabolism in the left temporal lobe. MRI scans showed mild, diffuse cortical atrophy without evidence of hippocampal sclerosis on qualitative or quantitative analysis. Wada testing showed language dominance in the left hemisphere and also showed that global memory was supported by either hemisphere. The patient underwent stereotaxic placement of bitemporal depth electrodes through occipital burr holes and placement of bilateral inferolateral temporal and orbitofrontal subdural strip electrodes. Four seizures showed focal left hippocampal onset before spreading to both orbitofrontal strips and, later, the right hippocampus (Fig. 3A). However, four other ictal events clearly began in the central contacts of the left orbitofrontal strip before spreading to the right orbitofrontal strip (Fig. 3B)o These two seizure types were identical with respect to initial semiology, which consisted of staring, eye blinking, and oral automatisms. Three of the four seizures with hippocampal onsets became secondarily generalized, but none of the orbitofrontal-onset seizures generalized. The two different seizure types were evenly spaced across the telemetry admission. Six weeks later, the patient underwent an awake left frontotemporal craniotomy with ECoG, cortical stimulation mapping of speech areas, ATL, and orbitofrontal cortical resection. ECoG demonstrated interictal spikes in the left orbitofrontal cortex and posterior mesial temporal lobe. The surgical resection included 4 cm of the lateral temporal neocortex, 3 cm of hippocampus and parahippocampal gyms, the uncus, the lateral portion of the amygdala, and a 2- x 3-cm section of the posterior orbitofrontal cortex. Pathologic examination showed no evidence of hippocampal sclerosis, although portions of area CA3 were missing from the specimen. No abnormalities were detected in the orbitofrontal cortex. Postoperatively, she experienced mild wordfinding difficulties; this condition improved but did not completely resolve with time. Deficits of

RESECTIONS FOR ORBITOFRONTAL SEIZURES

A

B

Figure 2. Photomicrographs of subcortical sections (hematoxylin & eosin stain) from the pathologic specimen of Patient 1 demonstrating the abnormal morphology and orientation of cells of glial (A) and neuronal (B) origin that are characteristic of cortical dysplasia. this type have been reported after dominant ATL alone (10). Neuropsychologic testing showed some improvement in overall frontal lobe functions but a persistent impairment on the G o - N o Go task and

failed to disclose additional deficits attributable to the orbitofrontal resection. Eleven months postoperatively, the patient experienced two seizures on the day of an unrelated surgical procedure w h e n J EPILEPSY, VOL. 8, NO. 2, 1995 149

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3. Invasiverecordings~om Patient 2 documenting onset of ictalactivi~ in the l~t hi,campus (A) and orbito~ontal cortex ~). In A, the ictalactivitybegins in the ant~ior contactsof the I~ temporal d~th electrode.In B, itbegins in the central ~ o contacts(LOF2 and LOF3) of the l~t orbito~ontalstrip.For both recordings,the montage is refermtial,sensitivi~is 100 +V/mm, chartspeed is 30 mm/s (19 s of the recordingis shown), high-~equen~ filteris off,Iow-~equen~ filteris 5 Hz, and the linefilteris on. Electrodemar~rs: L, left;R, right;OF, orbito~ontalstrip;TD, temporal d~th. The numbers increasemedial to ~t~al (orbito~ontalstrips)and anteriorto posterior(temporald~th electrodes), Fibre

s h e m i s s e d t w o d o s e s of c a r b a m a z e p i n e . N o o t h e r seizures had occurred at 15-month follow-up. She continues treatment with AEDs. Case 3

A 34-year-old, right-handed man had had intract a b l e p a r t i a l c o m p l e x s e i z u r e s s i n c e a g e 13 y e a r s . H e u n d e r w e n t a r i g h t A T L f o r s e i z u r e c o n t r o l at a g e 16 y e a r s . T h e p a t h o l o g y r e p o r t f r o m t h i s o p e r ation described gliosis in the hippocampus but not n e u r o n a l cell l o s s . H e w a s s e i z u r e - f r e e for 6 y e a r s . He then noted a recurrence of his habitual auras: a f e e l i n g o f d 4 j ~ v u . S o o n t h e r e a f t e r , h i s t y p i c a l seiz u r e s r e t u r n e d , c o n s i s t i n g of a s e n s a t i o n of d i s o r i e n t a t i o n . A t a g e 31, h e u n d e r w e n t p l a c e m e n t of a vagal nerve stimulator, but this was not effective in 150

J EPILEPSY, VOL. 8, NO. 2, 1995

controlling his seizures. His neurologic examinat i o n w a s u n r e m a r k a b l e . S c a l p / s p h e n o i d a l E E G tel e m e t r y s h o w e d a r i g h t f r o n t o t e m p o r a l ictal o n s e t and an interictal right frontocentral breach rhythm. MRI showed a defect consistent with a right ATL extending 4.5 cm from the temporal tip over the lateral temporal lobe. Mesial structures h a d a l s o b e e n c o m p l e t e l y r e s e c t e d b a c k to t h a t point. T h e p a t i e n t u n d e r w e n t s u r g e r y for r e o p e n i n g of the right frontotemporal craniotomy, with placem e n t of s u b d u r a l g r i d s o v e r t h e d o r s o l a t e r a l f r o n tal l o b e a n d t h e l a t e r a l p o s t e r i o r t e m p o r a l l o b e a n d subdural strips over the orbitofrontal cortex and the inferomesial posterior temporal lobe. Sevent e e n ictal e v e n t s o r i g i n a t e d i n t h e m e d i a l c o n t a c t s of t h e r i g h t o r b i t o f r o n t a l s t r i p b e f o r e s p r e a d i n g t o

RESECTIONS FOR ORBITOFRONTAL SEIZURES

the dorsolateral frontal lobe. One event became secondarily generalized. He returned to surgery for removal of the subdural electrodes and resection of the orbitofrontal cortex. Pathologic examination of the resected tissue was unremarkable. Postoperatively, the patient had no neurologic deficits. He was seizure-free at 19-month follow-up and continues treatment with AEDs. Discussion

The orbitofrontal cortex occupies the aspect of the frontal lobe adjacent to the floor of the anterior fossa. Although it has been defined according to cytoarchitectonic and connectional criteria in animals (11,12), the way in which these regions correlate with gross anatomic boundaries in humans is less clear. The region includes the gyrus rectus and the various orbital gyri which are separated by the olfactory sulcus. Sulcal boundaries include the inferior rostral sulcus medially and the frontomarginal and frontoorbital sulci laterally (13). The anterior and posterior limits are the frontal pole and the anterior perforated substance, respectively. The orbitofrontal cortex has been grouped with the insula and the temporal pole as a perilimbic area representing a transitional zone from the allocortical pyriform cortex to the isocortex of the dorsolateral frontal lobe (11). It receives significant subcortical afferents from the pars magnocellularis of the medial dorsal nucleus of the thalamus (11). Connections with other limbic structures include the amygdala, entorhinal cortex, hippocampus, and cingulate gyrus (11,14,15). Functional significance of these connections was demonstrated in a depth electrode study that showed the inferomedial frontal region to be the most common pathway of seizure propagation from one temporal lobe to the other in patients with mesial temporal lobe seizures (16). Our results provide evidence that partial seizures may arise from the orbitofrontal cortex. That 2 of these patients (Cases 1 and 3) are seizure-free 17 and 19 months after surgical resection supports the proposed causal relationship between the recorded site of seizure onset and the generation of the seizures in this region. This cannot be said for Patient 2, since an ATL was performed simultaneously with the orbitofrontal resection and since she has not been completely seizure-free. The clear difference between the ECoG profiles of the two seizure types suggests two separate areas of epileptogenesis in this patient. In addition to normal hippocampal volumetry on MRI, pathologic re-

view of this patient's hippocampus with hematoxylin and eosin and cresyl violet staining did not show evidence of hippocampal sclerosis. These observations are suggestive of orbitofrontal epilepsy but not conclusive, and we cannot say what her outcome would have been after an ATL without orbitofrontal resection. The prevalence of orbitofrontal epilepsy is difficult to estimate, and our experience suggests that this may be dependent on how frequently the orbitofrontal region is investigated invasively. Orbital and/or mesiofrontal onset occurred in 11-18% of cases in two large series in which this region was investigated with intracranial electrodes (4,7). The high success rates of centers performing ATLs without routinely studying this region and the finding that incomplete resection of mesial temporal structures is the problem that necessitates the most reoperations for failed epilepsy surgery (17) indicate that the prevalence of orbitofrontal epilepsy is not high. Our study did not identify a unique profile for orbitofrontal seizures based on noninvasive EEG or semiology. Although one report (6) described an EEG pattern in 3 patients which was considered specific for orbitofrontal epilepsy, other centers that have reviewed their cases based on invasive monitoring have not substantiated this finding (1,3,4,7). In the absence of specific noninvasive criteria, invasive monitoring is currently required to prove the orbitofrontal cortex as the area of epileptogenesis. Nevertheless, not all cases of suspected temporal lobe epilepsy require invasive monitoring, because a significant number of patients with concordant, noninvasive diagnostic studies underwent ATL with good results in the same time period in which the current patients were being investigated. We believe that it is clinically relevant that Patients 1 and 2 had hippocampal volume measurements on MRI that were within normal limits. Hippocampal volumetry differentiates between temporal and extratemporal epilepsy (9,18), and the success rate of temporal lobectomy is significantly lower in patients who are not shown by this method to have atrophy (19). Orbitofrontal epilepsy may contribute to this group of patients with intractable limbic seizures who achieve only moderate or poor seizure control after ATL, especially w h e n hippocampal atrophy is absent. The orbitofrontal cortex presents certain challenges for those contemplating surgical resections for control of seizures. Because of imprecise anatomic boundaries, defining the limits of resection presents the same problems as do m a n y other J EPILEPSY, VOL. 8, NO. 2, 1995 151

So No ROPER A N D R. L. GILMORE

cases of extratemporal epilepsy. In the current patients, strip electrodes clearly identified the orbitofrontal cortex as the site of seizure origin but were insufficient to define the actual boundaries of the epileptogenic area. We used intraoperative ECoG to define the boundaries of the area at the time of surgical resection. This has produced satisfactory results, based on 15- to 19-month followup, but more time and patients are needed to confirm these findings. The orbitofrontal cortex has been implicated in diverse behavioral functions, including regulation of emotional (20,21) and autonomic response (22,23), olfaction (24,25), memory of recency (26), and certain aspects of m e m o r y and cognition involving strategy development and self-monitoring (27). However, postoperative testing in this study did not detect neurologic or cognitive deficits that could be specifically attributed to unilateral orbitofrontal resections. These cases confirm that with proper pre- and intraoperative testing unilateral orbitofrontal resections can be safely performed without incurring unacceptable neurologic deficits. Our results add further evidence that the orbitofrontal cortex can be the site of onset of intractable partial complex seizures and that resections limited to this region can abolish such seizures. They also demonstrate that resections in this region can be performed without significant neurologic and neuropsychologic deficits. The orbitofrontal cortex should be considered as an area to be sampled in cases of intractable partial complex seizures that require invasive monitoring, especially w h e n high-resolution imaging studies do not demonstrate hippocampal sclerosis.

Acknowledgment: We thank Dr. R. M. Bauer for review and comments during manuscript preparation.

References 1. Ajmone-Marsan C. Seizures originating from the orbital cortex of the frontal lobe. Epilepsia 1988;29:208. 2. Chang CN, Ojemann LM, Ojemann GA, et al. Seizures of frontoorbital origin: a proven case. Epilepsia 1991;32:48791. 3. Ludwig B, Ajmone Marson C, Van Buren J. Cerebral seizures of probable orbitofrontal origin. Epilepsia 1975;16: 141-58. 4. Munari C, Bancaud J. Electroclinical symptomatology of partial seizures of orbital frontal origin. In: Chauvel P, Delgado-Escueta A, Halgren E, Bancaud J, eds. Advances in neurology, vol 57. New York: Raven Press, 1992:257-65. 152

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5. Rougier A, Loiseau P. Orbital frontal epilepsy: a case report. J Neurol Neurosurg Psychiatry 1988;51:146-7. 6. Tharp BR. Orbitofrontal seizures. A unique electroencephalographic and dinical syndrome. Epilepsia 1972;13:627-42. 7. Williamson PD, Spencer DD, Spencer SS, Novelly RA, Mattson RH. Complex partial seizures of frontal lobe origin. Ann Neurol 1985;18:497-504. 8. American EEG Society. Guidelines for standard electrode nomenclature. J Clin Neurophysiol 1994;11:111-3. 9. Gilmore R, Childress D, Leonard T, et al. Hippocampal volumetrics differentiate temporal lobe and extratemporal lobe epilepsy. Arch Neurol (in press). 10. Rausch R. Effects of temporal lobe surgery on behavior. In: Smith D, Treiman D, Trimble M, eds. Advances in neurology, vol 55. New York: Raven Press, 1991:279-92. 11. Morecraft RJ, Geula C, Mesulam M-M. Cytoarchitecture and neural afferents of orbitofrontal cortex in the brain of the monkey. J Comp Neurol 1992;323:341-58. 12. Walker AE. A cytoarchitectural study of the prefrontal area of the macaque monkey. J Comp Neurol 1940;73:59-86. 13. Ono M, Kubik S, Abernathy CD. Atlas of the cerebral sulci. New York: Thieme Medical Publishers, 1990. 14. Amaral DG, Price JL. Amygdalo-cortical projections in the monkey (Macacafascicularis). J Comp Neurol 1984;230:465-96. 15. Insausti R, Amaral DG, Cowan WM. The entorhinal cortex of the monkey: II. Cortical afferents. J Comp Neurol 1987; 264:356-95. 16. Lieb JP, Dasheiff RM, Engel J. Role of the frontal lobes in the propagation of mesial temporal lobe seizures. Epilepsia 1991;32:822-37. 17. Wyler AR, Hermann BP, Richey ET. Results of reoperation for failed epilepsy surgery. J Neurosurg 1989;71:815-9. 18. Cendes F, Andermann F, Gloor P, et al. Atrophy of mesial structures in patients with temporal lobe epilepsy: cause or consequence of repeated seizures? Ann Neurol 1993;34: 795-801. 19. Jack CR, Sharbrough FW, Cascino GD, et al. Magnetic resonance image-based hippocampal volumetry: correlation with outcome after temporal lobectomy. Ann Neurol 1992; 31:138-46. 20. Butter CM, Mishkin M, Rosvold HE. Conditioning and extinction of a food rewarded response after selective ablations of frontal cortex in rhesus monkeys. Exp Neurol 1963; 7:65-75. 21. Butter CM, Snyder DR, McDonald JA. Effects of orbital frontal lesions on aversive and aggressive behaviors in rhesus monkeys. J Comp Physiol Psychol 1970;72:132-43. 22. Chapman WP, Livingston RB, Livingston KE. Frontal lobotomy and electrical stimulation of frontal lobes. Effects on respiration and blood pressure in man. Arch Neurol Psychiatry 1949;62:701-16. 23. Van Buren JM, Buckman CA, Pritchard WL. Autonomic representation in the human orbitotemporal cortex. Neurology (Minn) 1961;11:214-24. 24. Jones-Gotman M, Zatorre RJ. Odor recognition memory in humans: role of right temporal and orbitofrontal regions. Brain Cogn 1993;22:182-98. 25. Zatorre RJ, Jones-Gotman M, Evans AC, et al. Functional localization and lateralization of human olfactory cortex. Nature 1992;360:339-40. 26. Milner B. Some cognitive effects of frontal-lobe lesions in man. Philos Trans R Soc Lond [Biol] 1982;298:211-26. 27. Stuss DT, Benson DF. The frontal lobes. New York: Raven Press, 1986.