- Email: [email protected]
Combining stereo-electroencephalography and subdural electrodes in the diagnosis and treatment of medically intractable epilepsy
Journal of Clinical Neuroscience xxx (2014) xxx–xxx
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Technical Note
Combining stereo-electroencephalography and subdural electrodes in the diagnosis and treatment of medically intractable epilepsy Rei Enatsu a,c, Juan Bulacio a,b, Imad Najm a,b, Elaine Wyllie a, Norman K. So a,b, Dileep R. Nair a,b, Nancy Foldvary-Schaefer a,b, William Bingaman a,c, Jorge Gonzalez-Martinez a,c,⇑ a b c
Epilepsy Center, Desk S60, Cleveland Clinic, 9500 Euclid Avenue, Cleveland, OH 44195, USA Department of Neurology, Cleveland Clinic Foundation, Cleveland, OH, USA Department of Neurosurgery, Cleveland Clinic Foundation, Cleveland, OH, USA
a r t i c l e
i n f o
Article history: Received 24 August 2013 Accepted 30 December 2013 Available online xxxx Keywords: Epilepsy Invasive monitoring Robotics Stereotactic EEG Strip electrode
a b s t r a c t Stereo-electroencephalography (SEEG) has advantages for exploring deeper epileptic foci. Nevertheless, SEEG can only sample isolated cortical areas and its spatial limitation, with the inability to record contiguous cortical regions, may cause difficulties in interpretation. In light of these limitations, the authors describe the hybrid technique of SEEG and subdural strip electrode placement. The hybrid technique was used for a presurgical evaluation in four patients with intractable epilepsy. Initially, the depth electrodes were inserted with a robotic stereotactic system. Thereafter, a skin incision and a small craniectomy were performed at the entry point of the strip electrode trajectory. The dura was opened and, under live fluoroscopic guidance, strip electrodes were slid into the subdural space. In these patients, the additional subdural strip electrodes provided (1) information regarding the precise description of seizure spread in the cortical surface adjacent to the subdural space, (2) identification of epileptogenic zones located near the crown, (3) more precise definition of functional cortex and (4) a better delineation of the interface between epileptogenic zones and functional cortex. This hybrid technique provides additional data compared to either technique alone, offering superior understanding of the dynamics of the epileptic activity and its interaction with functional cortical areas. Ó 2014 Published by Elsevier Ltd.
1. Introduction Stereo-electroencephalography (SEEG) has become one of the standard invasive procedures for exploring the epileptic cortex, especially deep-located epileptic foci [1–5]. This method has advantages including mapping ictal onset and seizure propagation, sampling deep cortical regions, and a relatively low complication rates [2,3]. Nevertheless, SEEG can only sample isolated cortical areas from the brain and is limited by the location or number of implanted electrodes. The spatial limitation of this technique and the relative inferiority of its functional mapping abilities along with the lack of recording contiguous cortical regions may cause difficulties in the precise anatomical delineation between the epileptogenic zone and functional cortex [4]. This limitation can be partially overcome by the use of subdural electrodes, which provide meticulous contiguous mapping of the cortex due to the continuity of its contacts. Taking into account these limitations, we combined both SEEG and subdural electrode methodology for ⇑ Corresponding author. Tel.: +1 216 445 4425; fax: +1 216 444 0343. E-mail address: [email protected] (J. Gonzalez-Martinez).
chronic extraoperative mapping of select patients with medically intractable focal epilepsy. This was performed using the hybrid technique of both SEEG and subdural strip electrode placement.
2. Implantation technique The depth and strip electrode targeting and trajectory are determined using robotic stereotactic software (ROSA; Medtech, Montpellier, France) based on a pre-implantation hypothesis regarding the possible location of the epileptogenic zone. Preoperative contrasted volumetric T1-weighted MR images are acquired and loaded into this robotic system. The planned trajectories are meticulously reviewed to avoid major vessel injury and collisions between the two types of electrodes. If so the trajectory is modified. The patient’s head is fixed to the operating table. The implanted depth electrodes consist of 10 cylindrical 2.3 mm long platinum contacts with a diameter of 0.89 mm (Ad-tech, Racine, WI, USA). The strip electrodes consist of 11 contacts (4 mm diameter) with center-to-center distances of 1 cm (Ad-tech). Initially, under general anesthesia, the depth electrodes are inserted in an orthogonal
http://dx.doi.org/10.1016/j.jocn.2013.12.014 0967-5868/Ó 2014 Published by Elsevier Ltd.
Please cite this article in press as: Enatsu R et al. Combining stereo-electroencephalography and subdural electrodes in the diagnosis and treatment of medically intractable epilepsy. J Clin Neurosci (2014), http://dx.doi.org/10.1016/j.jocn.2013.12.014
2
R. Enatsu et al. / Journal of Clinical Neuroscience xxx (2014) xxx–xxx
or oblique fashion in relation to the midline vertical plane, with robotic assistance. The number of implanted SEEG depth electrodes ranged from 11 to 15 (mean 13.3) per patient. After SEEG implantation is completed, a straight 3 cm skin incision is performed at the entry point of the strip electrode trajectory and skin retractors are applied. A small rectangular craniectomy (measuring 1.5 cm 0.5 cm) is performed using a hydraulic drill (Medtronic Midas Rex, Fort Worth, TX, USA) (Fig. 1A). Before the insertion of the subdural strip electrodes, in order to assure brain relaxation and opening of the subdural space, a reverse Trendelenburg position is applied followed by the administration of intravenous mannitol (1 g/kg). The dura is opened and, under live fluoroscopic guidance, strip electrodes are slid into the subdural space adjacent to the target cortex (Fig. 1B).
3. Case reports 3.1. Patient 1 A 19-year-old ambidextrous woman was referred for pharmacoresistant epilepsy. Her seizures had started at 7 years of age and were characterized by auditory auras followed by consciousness impairment and generalized tonic-clonic seizures with right head version. Scalp video electroencephalography (EEG) monitoring revealed interictal sharp waves in the left posterior temporal, occipital and right fronto-temporal regions. EEG ictal patterns were non-localizable. Brain MRI (1.5 T) was within normal limits. Fluorodeoxyglucose positron emission tomography (FDG-PET) showed focal hypometabolism in the left lateral temporal, left lateral and
Fig. 1. Patient 1. (A) Intraoperative photograph showing skin incisions and burr holes for strip electrodes. (B) Sagittal view of strip electrodes being slid into the target under fluoroscopic guidance. (C) Sagittal diagram with coronal sections of electrode placement and summary of the invasive evaluation. Ictal onset zone was identified in the left planum temporale and the posterior language area was in the supramarginal gyrus. CS = central sulcus.
Please cite this article in press as: Enatsu R et al. Combining stereo-electroencephalography and subdural electrodes in the diagnosis and treatment of medically intractable epilepsy. J Clin Neurosci (2014), http://dx.doi.org/10.1016/j.jocn.2013.12.014
R. Enatsu et al. / Journal of Clinical Neuroscience xxx (2014) xxx–xxx
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Fig. 2. (A) Sagittal diagram with axial section showing electrode placement in Patient 2. The strip electrode recorded the ictal onset zone in the left superior parietal lobule next to the hand sensory area. (B) Sagittal diagram of electrode placement in Patient 3. Ictal onset zone was identified in the left parietal operculum and no language function existed around the ictal onset zone. (C, D) Sagittal and (E, F) axial diagrams of electrode placement in Patient 4. The first stereo-electroencephalography (SEEG) evaluation revealed two different ictal onset patterns. The first pattern arose from the right lateral inferior temporal (C) and the second pattern showed right lateral occipito-parietotemporal onset (D). Ten days after the initial SEEG implantation, one strip electrode was added in the basal temporo-occipital area. This additional strip electrode revealed that the mesial basal temporal area is involved in ictal onset of the first pattern (E), whereas this strip electrode was not involved in the ictal onset of the second pattern (F). CS = central sulcus.
infero-lateral frontal regions, frontal operculum and adjacent insular regions. The Wada test revealed left hemispheric language dominance. Based on the presurgical evaluation, 12 depth electrodes were implanted in the left temporal, parietal, and perisylvian regions and two strip electrodes were inserted to cover the perisylvian region for language mapping (Fig. 1C). During the invasive evaluation, 15 seizures were recorded arising from the left planum temporale and the posterior language area was identified in the supramarginal gyrus. Based on these presurgical evaluations, the patient underwent resection of the left lateral temporal cortex with preservation of the mesial temporal structures and the posterior language area identified by the language mapping. After the resection, she suffered temporary word finding difficulties. Her seizures dramatically improved after the surgery.
3.2. Patient 2 A 51-year-old right-handed woman was referred for pharmacoresistant epilepsy. Her seizures had started at the age of 10 years and were characterized by right hand somatosensory aura followed by right arm tonic and generalized tonic-clonic seizure. Scalp video-EEG monitoring revealed interictal sharp waves in the left posterior quadrant, central and right temporo-parietal regions. EEG ictal patterns were classified as lateralized left hemisphere. MRI showed volume loss of the left thalamus and left hemisphere. FDG-PET showed focal hypometabolism in the left thalamus, mid- to posterior dorsal, dorsolateral and medial frontal regions. Based on presurgical evaluation, nine SEEG depth electrodes were implanted in the left cingulate, left mesial parietal, mesial frontal, left lateral parietal, and left sensorimotor areas
Please cite this article in press as: Enatsu R et al. Combining stereo-electroencephalography and subdural electrodes in the diagnosis and treatment of medically intractable epilepsy. J Clin Neurosci (2014), http://dx.doi.org/10.1016/j.jocn.2013.12.014
4
R. Enatsu et al. / Journal of Clinical Neuroscience xxx (2014) xxx–xxx
(Fig. 2A). Four depth electrodes were implanted in the right mesial frontal, mesial parietal and right cingulate regions. In addition, two strip electrodes were inserted to cover the sensorimotor region for functional mapping. During the invasive evaluation, the strip electrode recorded the ictal onset zone in the crown of the left superior parietal lobule close to the hand sensory area and SEEG electrodes revealed the seizure spread to the left supplementary motor area and lateral parietal regions. Based on these presurgical evaluations the patient underwent resection of the left superior parietal lobule. At the time of writing she had been seizure free for 2 years. 3.3. Patient 3 A 61-year-old right-handed woman with pharmacoresistant epilepsy was referred with a 3 year history of seizures, which were characterized by right face somatosensory aura followed by right face and arm tonic-clonic seizure. Scalp video-EEG monitoring revealed no interictal epileptiform activities and left hemispheric ictal onset. MRI was within normal limits. FDG-PET showed focal hypometabolism in the left inferior occipital region and left parieto-occipital sulcus. Based on presurgical evaluation, 11 depth electrodes were implanted in the left parietal operculum and inferior occipital and temporo-parietal areas. In addition, strip electrodes were inserted to cover the temporo-parietal region for language mapping. During the invasive evaluation, six seizures were recorded arising from the left parietal operculum without involvement of strip electrodes (Fig. 2B). Functional mapping in the strip electrodes revealed that no language function existed around the ictal onset zone. The patient underwent resection of the left parietal operculum. After the resection, she suffered transitory right perioral sensory deficit and word finding difficulties. At the time of writing she had been seizure free for 7 months. 3.4. Patient 4 A 40-year-old right-handed man was referred for pharmacoresistant epilepsy with seizures occurring once or twice per week. His seizures had started at the age of 12 years. The majority of seizures were characterized by visual aura with left-sided light followed by complicated movement of the extremities. Scalp video-EEG monitoring revealed interictal sharp waves in the right and left parieto-occipital and right temporal areas. Ictal activities arose from the right occipital region. Brain MRI was within normal limits. FDG-PET showed focal hypometabolism in the right orbitofrontal, right mid-lateral temporal and right posterior lateral temporal regions. Ictal-interictal subtraction single photon emission computed tomography (SPECT) study injected 30 seconds after seizure onset demonstrated an area of hyperperfusion in the right parieto-temporal cortex and left temporal lobe. Based on presurgical evaluation, an intracranial evaluation was performed using SEEG. Fifteen depth electrodes were implanted in the left and right temporal, parietal, and occipital lobes. During SEEG evaluation, two different patterns of ictal onset were recorded in the right hemisphere. The first pattern arose from the right lateral inferior temporal region (Fig. 2C) and the second pattern had a lateral occipito-parieto-temporal onset (Fig. 2D). Then, 10 days after the initial SEEG implantation, one strip electrode was inserted in the basal temporo-occipital area in order to rule out the possibility that these two ictal onset patterns reflected different seizure propagation patterns from the same basal temporal onset. This additional strip electrode revealed that the mesial basal temporal area was involved in ictal onset of the first pattern (Fig. 2E), but not involved in the ictal onset of the second pattern (Fig. 2F).
Taking these findings, we concluded that the patient had multifocal areas of ictal onset zones and no resection was indicated. 4. Discussion We performed SEEG evaluations combined with strip electrode placements in four patients. As SEEG has a limited ability to record contiguous cortical regions of epileptogenic and functional cortex, the precise anatomical delineation between these two regions can be difficult. In these patients, the additional subdural strip electrodes provided (1) information regarding the precise description of seizure spread in the cortical surface adjacent to the subdural space, (2) identification of epileptogenic zones located near the crown, (3) more precise definition of functional cortex and (4) better delineation of the interface between epileptogenic zones and functional cortex. SEEG has the advantage of exploring deeper epileptic foci and network-related seizure spread [5–7]. Conversely, strip electrodes are advantageous for exploring the cortical extent of epileptogenic regions or functional areas when superficially located [8–10]. Previously, the use of epidural pegs arrayed in a grid-like fashion placed between and around depth entry sites were introduced to improve cortical electrode coverage [11]. Compared to this approach, the additional strip electrodes in our technique enables us to stimulate direct cortical surface for functional mapping (Patients 1–3) and cover the basal aspect of the brain (Patient 4). Consequently, these methods can be considered complementary and the combination of these techniques will likely provide better three-dimensional cortical recordings and stimulation data to guide the surgeon in performing more precise and safer resections. Criticisms of this method include the possibility that placing subdural strip electrodes may displace the depth electrodes or cause injuries related to collisions between the two types of electrodes. Despite the relative small number of implanted subjects, we have not encountered these complications when using the described method. These complications can be avoided by careful presurgical planning. Furthermore, intraoperative visualization of the strip electrodes with fluoroscopy during positioning gives the neurosurgeon the ability to predict final strip electrode position and to identify misplacements and collisions in real time, minimizing complications. 5. Conclusion The combination of SEEG and subdural strip electrodes provides additional and complementary information regarding functional mapping and the detection of seizure onset. This hybrid technique provides additional data, which cannot be obtained by either of the techniques when applied separately, offering superior understanding of the dynamics of the epileptic activity and its interaction with functional cortical areas. In order to validate this technique, a larger series of patients will be necessary. Conflicts of Interest/Disclosures The authors declare that they have no financial or other conflicts of interest in relation to this research and its publication. References [1] Bancaud J, Angelergues R, Bernouilli C, et al. Functional stereotaxic exploration (SEEG) of epilepsy. Electroencephalogr Clin Neurophysiol 1970;28:85–6. [2] Cossu M, Cardinale F, Castana L, et al. Stereoelectroencephalography in the presurgical evaluation of focal epilepsy: a retrospective analysis of 215 procedures. Neurosurgery 2005;57:706–18 [discussion 706–8].
Please cite this article in press as: Enatsu R et al. Combining stereo-electroencephalography and subdural electrodes in the diagnosis and treatment of medically intractable epilepsy. J Clin Neurosci (2014), http://dx.doi.org/10.1016/j.jocn.2013.12.014
R. Enatsu et al. / Journal of Clinical Neuroscience xxx (2014) xxx–xxx [3] Cardinale F, Cossu M, Castana L, et al. Stereoelectroencephalography: surgical methodology, safety, and stereotactic application accuracy in 500 procedures. Neurosurgery 2013;72:353–66 [discussion 66]. [4] Gonzalez-Martinez J, Bulacio J, Alexopoulos A, et al. Stereoelectroencephalography in the ‘‘difficult to localize’’ refractory focal epilepsy: early experience from a north American epilepsy center. Epilepsia 2013;54:323–30. [5] Vadera S, Mullin J, Bulacio J, et al. Stereoelectroencephalography following subdural grid placement for difficult to localize epilepsy. Neurosurgery 2013;72:723–9. [6] Alsaadi TM, Laxer KD, Barbaro NM, et al. False lateralization by subdural electrodes in two patients with temporal lobe epilepsy. Neurology 2001;57:532–4. [7] Talairach J, Bancaud J, Bonis A, et al. Functional stereotaxic exploration of epilepsy. Confin Neurol 1962;22:328–31.
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[8] Bulacio JC, Jehi L, Wong C, et al. Long-term seizure outcome after resective surgery in patients evaluated with intracranial electrodes. Epilepsia 2012;53:1722–30. [9] Najm I, Bingaman W, Luders HO. The use of subdural grids in the management of focal malformations due to abnormal cortical development. Neurosurg Clin N Am 2002;13:87–92 [viii-ix]. [10] Ross DA, Brunberg JA, Drury I, et al. Intracerebral depth electrode monitoring in partial epilepsy: the morbidity and efficacy of placement using magnetic resonance image-guided stereotactic surgery. Neurosurgery 1996;39:327–33 [discussion 333–4]. [11] Olivier A, Boling WW, Tanriverdi T. Stereoelectroencephalography (stereotactic intracranial recording); techniques in epilepsy surgery. Cambridge: Cambridge University Press; 2012 [p. 54–74].
Please cite this article in press as: Enatsu R et al. Combining stereo-electroencephalography and subdural electrodes in the diagnosis and treatment of medically intractable epilepsy. J Clin Neurosci (2014), http://dx.doi.org/10.1016/j.jocn.2013.12.014
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Technical Note
Combining stereo-electroencephalography and subdural electrodes in the diagnosis and treatment of medically intractable epilepsy Rei Enatsu a,c, Juan Bulacio a,b, Imad Najm a,b, Elaine Wyllie a, Norman K. So a,b, Dileep R. Nair a,b, Nancy Foldvary-Schaefer a,b, William Bingaman a,c, Jorge Gonzalez-Martinez a,c,⇑ a b c
Epilepsy Center, Desk S60, Cleveland Clinic, 9500 Euclid Avenue, Cleveland, OH 44195, USA Department of Neurology, Cleveland Clinic Foundation, Cleveland, OH, USA Department of Neurosurgery, Cleveland Clinic Foundation, Cleveland, OH, USA
a r t i c l e
i n f o
Article history: Received 24 August 2013 Accepted 30 December 2013 Available online xxxx Keywords: Epilepsy Invasive monitoring Robotics Stereotactic EEG Strip electrode
a b s t r a c t Stereo-electroencephalography (SEEG) has advantages for exploring deeper epileptic foci. Nevertheless, SEEG can only sample isolated cortical areas and its spatial limitation, with the inability to record contiguous cortical regions, may cause difficulties in interpretation. In light of these limitations, the authors describe the hybrid technique of SEEG and subdural strip electrode placement. The hybrid technique was used for a presurgical evaluation in four patients with intractable epilepsy. Initially, the depth electrodes were inserted with a robotic stereotactic system. Thereafter, a skin incision and a small craniectomy were performed at the entry point of the strip electrode trajectory. The dura was opened and, under live fluoroscopic guidance, strip electrodes were slid into the subdural space. In these patients, the additional subdural strip electrodes provided (1) information regarding the precise description of seizure spread in the cortical surface adjacent to the subdural space, (2) identification of epileptogenic zones located near the crown, (3) more precise definition of functional cortex and (4) a better delineation of the interface between epileptogenic zones and functional cortex. This hybrid technique provides additional data compared to either technique alone, offering superior understanding of the dynamics of the epileptic activity and its interaction with functional cortical areas. Ó 2014 Published by Elsevier Ltd.
1. Introduction Stereo-electroencephalography (SEEG) has become one of the standard invasive procedures for exploring the epileptic cortex, especially deep-located epileptic foci [1–5]. This method has advantages including mapping ictal onset and seizure propagation, sampling deep cortical regions, and a relatively low complication rates [2,3]. Nevertheless, SEEG can only sample isolated cortical areas from the brain and is limited by the location or number of implanted electrodes. The spatial limitation of this technique and the relative inferiority of its functional mapping abilities along with the lack of recording contiguous cortical regions may cause difficulties in the precise anatomical delineation between the epileptogenic zone and functional cortex [4]. This limitation can be partially overcome by the use of subdural electrodes, which provide meticulous contiguous mapping of the cortex due to the continuity of its contacts. Taking into account these limitations, we combined both SEEG and subdural electrode methodology for ⇑ Corresponding author. Tel.: +1 216 445 4425; fax: +1 216 444 0343. E-mail address: [email protected] (J. Gonzalez-Martinez).
chronic extraoperative mapping of select patients with medically intractable focal epilepsy. This was performed using the hybrid technique of both SEEG and subdural strip electrode placement.
2. Implantation technique The depth and strip electrode targeting and trajectory are determined using robotic stereotactic software (ROSA; Medtech, Montpellier, France) based on a pre-implantation hypothesis regarding the possible location of the epileptogenic zone. Preoperative contrasted volumetric T1-weighted MR images are acquired and loaded into this robotic system. The planned trajectories are meticulously reviewed to avoid major vessel injury and collisions between the two types of electrodes. If so the trajectory is modified. The patient’s head is fixed to the operating table. The implanted depth electrodes consist of 10 cylindrical 2.3 mm long platinum contacts with a diameter of 0.89 mm (Ad-tech, Racine, WI, USA). The strip electrodes consist of 11 contacts (4 mm diameter) with center-to-center distances of 1 cm (Ad-tech). Initially, under general anesthesia, the depth electrodes are inserted in an orthogonal
http://dx.doi.org/10.1016/j.jocn.2013.12.014 0967-5868/Ó 2014 Published by Elsevier Ltd.
Please cite this article in press as: Enatsu R et al. Combining stereo-electroencephalography and subdural electrodes in the diagnosis and treatment of medically intractable epilepsy. J Clin Neurosci (2014), http://dx.doi.org/10.1016/j.jocn.2013.12.014
2
R. Enatsu et al. / Journal of Clinical Neuroscience xxx (2014) xxx–xxx
or oblique fashion in relation to the midline vertical plane, with robotic assistance. The number of implanted SEEG depth electrodes ranged from 11 to 15 (mean 13.3) per patient. After SEEG implantation is completed, a straight 3 cm skin incision is performed at the entry point of the strip electrode trajectory and skin retractors are applied. A small rectangular craniectomy (measuring 1.5 cm 0.5 cm) is performed using a hydraulic drill (Medtronic Midas Rex, Fort Worth, TX, USA) (Fig. 1A). Before the insertion of the subdural strip electrodes, in order to assure brain relaxation and opening of the subdural space, a reverse Trendelenburg position is applied followed by the administration of intravenous mannitol (1 g/kg). The dura is opened and, under live fluoroscopic guidance, strip electrodes are slid into the subdural space adjacent to the target cortex (Fig. 1B).
3. Case reports 3.1. Patient 1 A 19-year-old ambidextrous woman was referred for pharmacoresistant epilepsy. Her seizures had started at 7 years of age and were characterized by auditory auras followed by consciousness impairment and generalized tonic-clonic seizures with right head version. Scalp video electroencephalography (EEG) monitoring revealed interictal sharp waves in the left posterior temporal, occipital and right fronto-temporal regions. EEG ictal patterns were non-localizable. Brain MRI (1.5 T) was within normal limits. Fluorodeoxyglucose positron emission tomography (FDG-PET) showed focal hypometabolism in the left lateral temporal, left lateral and
Fig. 1. Patient 1. (A) Intraoperative photograph showing skin incisions and burr holes for strip electrodes. (B) Sagittal view of strip electrodes being slid into the target under fluoroscopic guidance. (C) Sagittal diagram with coronal sections of electrode placement and summary of the invasive evaluation. Ictal onset zone was identified in the left planum temporale and the posterior language area was in the supramarginal gyrus. CS = central sulcus.
Please cite this article in press as: Enatsu R et al. Combining stereo-electroencephalography and subdural electrodes in the diagnosis and treatment of medically intractable epilepsy. J Clin Neurosci (2014), http://dx.doi.org/10.1016/j.jocn.2013.12.014
R. Enatsu et al. / Journal of Clinical Neuroscience xxx (2014) xxx–xxx
3
Fig. 2. (A) Sagittal diagram with axial section showing electrode placement in Patient 2. The strip electrode recorded the ictal onset zone in the left superior parietal lobule next to the hand sensory area. (B) Sagittal diagram of electrode placement in Patient 3. Ictal onset zone was identified in the left parietal operculum and no language function existed around the ictal onset zone. (C, D) Sagittal and (E, F) axial diagrams of electrode placement in Patient 4. The first stereo-electroencephalography (SEEG) evaluation revealed two different ictal onset patterns. The first pattern arose from the right lateral inferior temporal (C) and the second pattern showed right lateral occipito-parietotemporal onset (D). Ten days after the initial SEEG implantation, one strip electrode was added in the basal temporo-occipital area. This additional strip electrode revealed that the mesial basal temporal area is involved in ictal onset of the first pattern (E), whereas this strip electrode was not involved in the ictal onset of the second pattern (F). CS = central sulcus.
infero-lateral frontal regions, frontal operculum and adjacent insular regions. The Wada test revealed left hemispheric language dominance. Based on the presurgical evaluation, 12 depth electrodes were implanted in the left temporal, parietal, and perisylvian regions and two strip electrodes were inserted to cover the perisylvian region for language mapping (Fig. 1C). During the invasive evaluation, 15 seizures were recorded arising from the left planum temporale and the posterior language area was identified in the supramarginal gyrus. Based on these presurgical evaluations, the patient underwent resection of the left lateral temporal cortex with preservation of the mesial temporal structures and the posterior language area identified by the language mapping. After the resection, she suffered temporary word finding difficulties. Her seizures dramatically improved after the surgery.
3.2. Patient 2 A 51-year-old right-handed woman was referred for pharmacoresistant epilepsy. Her seizures had started at the age of 10 years and were characterized by right hand somatosensory aura followed by right arm tonic and generalized tonic-clonic seizure. Scalp video-EEG monitoring revealed interictal sharp waves in the left posterior quadrant, central and right temporo-parietal regions. EEG ictal patterns were classified as lateralized left hemisphere. MRI showed volume loss of the left thalamus and left hemisphere. FDG-PET showed focal hypometabolism in the left thalamus, mid- to posterior dorsal, dorsolateral and medial frontal regions. Based on presurgical evaluation, nine SEEG depth electrodes were implanted in the left cingulate, left mesial parietal, mesial frontal, left lateral parietal, and left sensorimotor areas
Please cite this article in press as: Enatsu R et al. Combining stereo-electroencephalography and subdural electrodes in the diagnosis and treatment of medically intractable epilepsy. J Clin Neurosci (2014), http://dx.doi.org/10.1016/j.jocn.2013.12.014
4
R. Enatsu et al. / Journal of Clinical Neuroscience xxx (2014) xxx–xxx
(Fig. 2A). Four depth electrodes were implanted in the right mesial frontal, mesial parietal and right cingulate regions. In addition, two strip electrodes were inserted to cover the sensorimotor region for functional mapping. During the invasive evaluation, the strip electrode recorded the ictal onset zone in the crown of the left superior parietal lobule close to the hand sensory area and SEEG electrodes revealed the seizure spread to the left supplementary motor area and lateral parietal regions. Based on these presurgical evaluations the patient underwent resection of the left superior parietal lobule. At the time of writing she had been seizure free for 2 years. 3.3. Patient 3 A 61-year-old right-handed woman with pharmacoresistant epilepsy was referred with a 3 year history of seizures, which were characterized by right face somatosensory aura followed by right face and arm tonic-clonic seizure. Scalp video-EEG monitoring revealed no interictal epileptiform activities and left hemispheric ictal onset. MRI was within normal limits. FDG-PET showed focal hypometabolism in the left inferior occipital region and left parieto-occipital sulcus. Based on presurgical evaluation, 11 depth electrodes were implanted in the left parietal operculum and inferior occipital and temporo-parietal areas. In addition, strip electrodes were inserted to cover the temporo-parietal region for language mapping. During the invasive evaluation, six seizures were recorded arising from the left parietal operculum without involvement of strip electrodes (Fig. 2B). Functional mapping in the strip electrodes revealed that no language function existed around the ictal onset zone. The patient underwent resection of the left parietal operculum. After the resection, she suffered transitory right perioral sensory deficit and word finding difficulties. At the time of writing she had been seizure free for 7 months. 3.4. Patient 4 A 40-year-old right-handed man was referred for pharmacoresistant epilepsy with seizures occurring once or twice per week. His seizures had started at the age of 12 years. The majority of seizures were characterized by visual aura with left-sided light followed by complicated movement of the extremities. Scalp video-EEG monitoring revealed interictal sharp waves in the right and left parieto-occipital and right temporal areas. Ictal activities arose from the right occipital region. Brain MRI was within normal limits. FDG-PET showed focal hypometabolism in the right orbitofrontal, right mid-lateral temporal and right posterior lateral temporal regions. Ictal-interictal subtraction single photon emission computed tomography (SPECT) study injected 30 seconds after seizure onset demonstrated an area of hyperperfusion in the right parieto-temporal cortex and left temporal lobe. Based on presurgical evaluation, an intracranial evaluation was performed using SEEG. Fifteen depth electrodes were implanted in the left and right temporal, parietal, and occipital lobes. During SEEG evaluation, two different patterns of ictal onset were recorded in the right hemisphere. The first pattern arose from the right lateral inferior temporal region (Fig. 2C) and the second pattern had a lateral occipito-parieto-temporal onset (Fig. 2D). Then, 10 days after the initial SEEG implantation, one strip electrode was inserted in the basal temporo-occipital area in order to rule out the possibility that these two ictal onset patterns reflected different seizure propagation patterns from the same basal temporal onset. This additional strip electrode revealed that the mesial basal temporal area was involved in ictal onset of the first pattern (Fig. 2E), but not involved in the ictal onset of the second pattern (Fig. 2F).
Taking these findings, we concluded that the patient had multifocal areas of ictal onset zones and no resection was indicated. 4. Discussion We performed SEEG evaluations combined with strip electrode placements in four patients. As SEEG has a limited ability to record contiguous cortical regions of epileptogenic and functional cortex, the precise anatomical delineation between these two regions can be difficult. In these patients, the additional subdural strip electrodes provided (1) information regarding the precise description of seizure spread in the cortical surface adjacent to the subdural space, (2) identification of epileptogenic zones located near the crown, (3) more precise definition of functional cortex and (4) better delineation of the interface between epileptogenic zones and functional cortex. SEEG has the advantage of exploring deeper epileptic foci and network-related seizure spread [5–7]. Conversely, strip electrodes are advantageous for exploring the cortical extent of epileptogenic regions or functional areas when superficially located [8–10]. Previously, the use of epidural pegs arrayed in a grid-like fashion placed between and around depth entry sites were introduced to improve cortical electrode coverage [11]. Compared to this approach, the additional strip electrodes in our technique enables us to stimulate direct cortical surface for functional mapping (Patients 1–3) and cover the basal aspect of the brain (Patient 4). Consequently, these methods can be considered complementary and the combination of these techniques will likely provide better three-dimensional cortical recordings and stimulation data to guide the surgeon in performing more precise and safer resections. Criticisms of this method include the possibility that placing subdural strip electrodes may displace the depth electrodes or cause injuries related to collisions between the two types of electrodes. Despite the relative small number of implanted subjects, we have not encountered these complications when using the described method. These complications can be avoided by careful presurgical planning. Furthermore, intraoperative visualization of the strip electrodes with fluoroscopy during positioning gives the neurosurgeon the ability to predict final strip electrode position and to identify misplacements and collisions in real time, minimizing complications. 5. Conclusion The combination of SEEG and subdural strip electrodes provides additional and complementary information regarding functional mapping and the detection of seizure onset. This hybrid technique provides additional data, which cannot be obtained by either of the techniques when applied separately, offering superior understanding of the dynamics of the epileptic activity and its interaction with functional cortical areas. In order to validate this technique, a larger series of patients will be necessary. Conflicts of Interest/Disclosures The authors declare that they have no financial or other conflicts of interest in relation to this research and its publication. References [1] Bancaud J, Angelergues R, Bernouilli C, et al. Functional stereotaxic exploration (SEEG) of epilepsy. Electroencephalogr Clin Neurophysiol 1970;28:85–6. [2] Cossu M, Cardinale F, Castana L, et al. Stereoelectroencephalography in the presurgical evaluation of focal epilepsy: a retrospective analysis of 215 procedures. Neurosurgery 2005;57:706–18 [discussion 706–8].
Please cite this article in press as: Enatsu R et al. Combining stereo-electroencephalography and subdural electrodes in the diagnosis and treatment of medically intractable epilepsy. J Clin Neurosci (2014), http://dx.doi.org/10.1016/j.jocn.2013.12.014
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Please cite this article in press as: Enatsu R et al. Combining stereo-electroencephalography and subdural electrodes in the diagnosis and treatment of medically intractable epilepsy. J Clin Neurosci (2014), http://dx.doi.org/10.1016/j.jocn.2013.12.014