Clinical Neurology and Neurosurgery 122 (2014) 9–11
Contents lists available at ScienceDirect
Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Case Report
Concomitant use of stereoelectroencephalography (SEEG) and magnetoencephalographic (MEG) in the surgical treatment of refractory focal epilepsy Sumeet Vadera, Richard Burgess, Jorge Gonzalez-Martinez ∗ Department of Neurological Surgery, Neurological Institute, Cleveland Clinic, Cleveland, USA
a r t i c l e
i n f o
Article history: Received 4 May 2013 Received in revised form 28 March 2014 Accepted 9 April 2014 Available online 18 April 2014 Keywords: Epilepsy Epileptogenic zone Stereoelectroencephalography (SEEG) Magnetoencephalography (MEG)
1. Introduction In patients with refractory focal epilepsy, the success in localizing and completely resecting the epileptic focus has been shown to be the most important predictor of seizure freedom in patients who undergo surgical resections [1]. In order to achieve these goals, various non-invasive conventional tools are available, including analysis of seizure semiology, prolonged video-scalp electroencephalographic (video-EEG) recordings, ictal SPECT and PET scans. When no non-invasive data congruency is achieved, additional localizing methods may be required. At our institution and others, stereoelectroencephalography (SEEG) and magenetoencephalography (MEG) have increasingly been used as complimentary localizing tools to assist with the localization of the EZ in patients with “difficult to localize” medically refractory focal epilepsy [2,3]. The authors report a case of a 29-year-old male with nonlesional epilepsy who underwent multiple non-invasive studies for preoperative work-up of epilepsy. After multidisciplinary Epilepsy Management Conference, the decision was made to perform SEEG implantation for the localization of the EZ. A MEG study was performed with SEEG electrodes in place and both studies localized the EZ to a small area in the right peri-rolandic opercular region. Currently, there are no reports describing the utility of
∗ Corresponding author. Tel.: +1 216 445 4425; fax: +1 216 444 0343. E-mail address: [email protected] (J. Gonzalez-Martinez). http://dx.doi.org/10.1016/j.clineuro.2014.04.002 0303-8467/© 2014 Published by Elsevier B.V.
concomitant SEEG and MEG procedures in the localization and treatment of medically refractory focal epilepsy and postoperative seizure free outcomes. 2. Case report 2.1. History and examination The patient is a 29-year-old left-handed male who initially presented to the epilepsy neurology team with medically intractable focal epilepsy, which began at the age of 12. Originally, the patient had seizures at night, which consisted of chest heaviness, stiffening of the left arm followed by a generalized tonic–clonic seizure. More recently, the patient noted an aura of a tingling sensation deep in his throat, which spread to the left face, followed by left face clonus and left arm posturing. The patient often developed difficulty breathing, drooling and garbled speech with excessive salivation immediately after seizures. Seizure duration was approximately 30 s and these occurred 10 times a day. Consciousness was preserved entirely during these events. The patient had failed two anti-epileptic medications in the past and was currently on three medications but his seizures were still poorly controlled. The patient had a normal birth and development history and had no epilepsy risk factors. Two video-electroencephalograms (vEEG) were performed in the past, which were both non-localizable and a three-tesla magnetic resonance imaging (MRI) study was performed, which was negative. During the patient’s current epilepsy work-up, he
10
S. Vadera et al. / Clinical Neurology and Neurosurgery 122 (2014) 9–11
Fig. 1. Ictal SPECT showing (a) coronal and (b) sagittal planes. Hyperperfusion can be noted in right posterior insular region and peri-rolandic region as well as left posterior cingulate gyrus and lateral temporal lobe (not shown).
underwent an ictal single-photon emission computed tomography (SPECT), which showed hyperperfusion in the right precentral rolandic area and right posterior insular regions as well as the left basal ganglia (Fig. 1). The case was presented at the multidisciplinary Epilepsy Management Conference and unanimous decision was that the patient had focal epilepsy possibly arising from the right perisylvian and insula regions based on the ictal semiology and ictal SPECT. Although vEEG was non-localizable and MRI was normal, the generated hypothesis was that his seizures might be explained by a deep-seated focus located in the peri-sylvian areas or in the adjacent insular cortex. Nevertheless, due to the lack of localizing and congruent information by the non-invasive methods, an invasive monitoring study was indicated. Due to the possibility of a deep-seated focus, SEEG implantation was the chosen invasive method. 2.2. Operations and perioperative course The patient underwent implantation of 11 SEEG electrodes in standard stereotactic fashion with no complications noted intraoperatively. Because of the preoperative hypothesis, the majority of the electrodes were concentrated within the right perisylvian, opercular regions and insula. The patient was monitored for eight days in the Epilepsy Monitoring Unit, during which he had multiple seizures that were all localized within a focal region within the M, S and R electrodes, which were located in the perisylvian rolandic area. To better delineate the EZ, MEG was performed on this patient using the Elekta Neuromag system at the Cleveland Clinic. The sources of interictal discharges were localized by single equivalent current dipole modeling using the xfit software and coregistration to the patient’s MRI using the MRILab software (both from Elekta Neuromag). This showed a tight cluster of dipoles all with a consistent vertical orientation in the right peri-rolandic opercular region, in close anatomical relation of the SEEG ictal activity recorded from electrodes S and R. The SEEG electrodes were removed on postoperative day eight and patient was discharged home (Fig. 2a–d). Two-months later, the patient was readmitted for a focal resection of the area that correlated with both the MEG spiking and the SEEG ictal areas. The M, R, and S scalp entry points were used to assist with the localization of the incision site and a curvilinear incision was performed. A small craniotomy was made that encompassed the three electrodes of interest and the MEG cluster. Stereotactic navigation was performed and a small piece of abnormally appearing tissue within the peri-rolandic opercular region (approximately 2 cm3 ) was removed and sent for pathology with the depth of the resection extending to the adjacent insular via (Fig. 2e and f).
2.3. Postoperative course The patient did well during the immediate post-operative period. As expected, a contralateral lower face weakness was noticed soon after surgery, but completely recovered after 2 weeks. The patient was last seen at the 24 month follow-up period and he remains completely seizure-free and is now completely off medication. The final pathology for this specimen was malformation of cortical development with balloon cells.
3. Discussion From an epilepsy surgery perspective, patients with nonlesional focal epilepsy are some of the most challenging patients to treat, with disappointing long-term seizure outcome results [4]. In select cases, excellent outcomes have been described when the EZ is localized based upon precise pre-surgical hypothesis and combined with the use of intracranial electrode monitoring [1]. We describe a patient who underwent simultaneous MEG and SEEG recordings and the subsequent seizure outcome after respective surgery. The concomitant SEEG ictal/interictal pattern recordings and the MEG cluster activity complemented one another, guiding the surgeon in performing a relative small focal resection, resulting in pathological substrate confirmation and sustained seizure control. This case highlights some of the advantages of coupling different non-invasive (MEG) and minimally invasive (SEEG) methods of explorations in patients with “difficult to localize epilepsy.” Ultimately, the combined approach offered an additional opportunity for seizure freedom associated with minimal morbidity, in a clinical scenario unlikely to be successfully resolved with the standard methods of invasive monitoring. The fact that the MEG dipoles correlated strongly with the SEEG ictal map lends a great deal of weight to the original hypothesis and further supported the SEEG data, even in the face of negative scalp vEEG recordings. The whole head recording capability of modern magnetoencephalographs provides localization data that complements the SEEG localization by “filling in the blanks” between SEEG electrodes. Recording MEG simultaneous with SEEG helps to clarify the extent of the abnormal activity being recorded by the SEEG electrodes and to reassure the surgical team that the SEEG electrodes are providing a complete picture [5]. While other studies have looked at MEG and intra-operative EEG or subdural depths and grids this case is the first described usage of concomitant SEEG and MEG studies and the outcome after focal resection of corresponding regions. In referencing previous studies not including SEEG, Knowlton stated that “nearly all MEG–EEG comparison studies” support the two studies as complimentary to
S. Vadera et al. / Clinical Neurology and Neurosurgery 122 (2014) 9–11
11
Fig. 2. Postoperative (a) AP X-ray after SEEG implantation, (b) electrode map showing three electrodes with ictal spikes (red circles), (c) coronal, and (d) sagittal MEG study showing large cluster of vertically oriented dipoles along right peri-rolandic opercular region, and postoperative MRI showing, (e) coronal, and (f) sagittal section along the resection cavity.
each other [2]. This study suggests that the same may be possible with SEEG. 4. Conclusion This case is the first described successful usage of concomitant SEEG and MEG studies and the outcome after focal resection of corresponding regions. The concomitant application of different modalities of exploration is promising, offering precise localization possibilities with minimal morbidity. Longer follow-up and larger cohorts will be necessary to validate the utility of the reported approach in patients with medical refractory focal epilepsy and “difficult to localize” epileptic foci.
References [1] Luders HO, Najm I, Nair D, Widdess-Walsh P, Bingman W. The epileptogenic zone: general principles. Epileptic Disord 2006;8(Suppl. 2):S1–9. [2] Knowlton R. Can Magnetoencephalography aid epilepsy surgery? Epilepsy Curr 2008;8(1):1–5. [3] Vadera S, Mullin J, Bulacio J, Najm I, Bingaman W, Gonzalez-Martinez J. Stereoelectroencephalography following subdural grid placement for difficult to localize epilepsy. Neurosurgery 2013;72(5):723–9. [4] Siegel AM, Jobst BC, Thadani VM, Rhodes CH, Lewis PJ, Roberts DW, et al. Medically intractable, localization-related epilepsy with normal MRI: presurgical evaluation and surgical outcome in 43 patients. Epilepsia 2001;42: 883–8. [5] Mamelak AN, Lopez N, Akhtari M, Sutherling WW. Magnetoencephalographydirected surgery in patients with neocortical epilepsy. J Neurosurg 2002;97(4):865–73.
Contents lists available at ScienceDirect
Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Case Report
Concomitant use of stereoelectroencephalography (SEEG) and magnetoencephalographic (MEG) in the surgical treatment of refractory focal epilepsy Sumeet Vadera, Richard Burgess, Jorge Gonzalez-Martinez ∗ Department of Neurological Surgery, Neurological Institute, Cleveland Clinic, Cleveland, USA
a r t i c l e
i n f o
Article history: Received 4 May 2013 Received in revised form 28 March 2014 Accepted 9 April 2014 Available online 18 April 2014 Keywords: Epilepsy Epileptogenic zone Stereoelectroencephalography (SEEG) Magnetoencephalography (MEG)
1. Introduction In patients with refractory focal epilepsy, the success in localizing and completely resecting the epileptic focus has been shown to be the most important predictor of seizure freedom in patients who undergo surgical resections [1]. In order to achieve these goals, various non-invasive conventional tools are available, including analysis of seizure semiology, prolonged video-scalp electroencephalographic (video-EEG) recordings, ictal SPECT and PET scans. When no non-invasive data congruency is achieved, additional localizing methods may be required. At our institution and others, stereoelectroencephalography (SEEG) and magenetoencephalography (MEG) have increasingly been used as complimentary localizing tools to assist with the localization of the EZ in patients with “difficult to localize” medically refractory focal epilepsy [2,3]. The authors report a case of a 29-year-old male with nonlesional epilepsy who underwent multiple non-invasive studies for preoperative work-up of epilepsy. After multidisciplinary Epilepsy Management Conference, the decision was made to perform SEEG implantation for the localization of the EZ. A MEG study was performed with SEEG electrodes in place and both studies localized the EZ to a small area in the right peri-rolandic opercular region. Currently, there are no reports describing the utility of
∗ Corresponding author. Tel.: +1 216 445 4425; fax: +1 216 444 0343. E-mail address: [email protected] (J. Gonzalez-Martinez). http://dx.doi.org/10.1016/j.clineuro.2014.04.002 0303-8467/© 2014 Published by Elsevier B.V.
concomitant SEEG and MEG procedures in the localization and treatment of medically refractory focal epilepsy and postoperative seizure free outcomes. 2. Case report 2.1. History and examination The patient is a 29-year-old left-handed male who initially presented to the epilepsy neurology team with medically intractable focal epilepsy, which began at the age of 12. Originally, the patient had seizures at night, which consisted of chest heaviness, stiffening of the left arm followed by a generalized tonic–clonic seizure. More recently, the patient noted an aura of a tingling sensation deep in his throat, which spread to the left face, followed by left face clonus and left arm posturing. The patient often developed difficulty breathing, drooling and garbled speech with excessive salivation immediately after seizures. Seizure duration was approximately 30 s and these occurred 10 times a day. Consciousness was preserved entirely during these events. The patient had failed two anti-epileptic medications in the past and was currently on three medications but his seizures were still poorly controlled. The patient had a normal birth and development history and had no epilepsy risk factors. Two video-electroencephalograms (vEEG) were performed in the past, which were both non-localizable and a three-tesla magnetic resonance imaging (MRI) study was performed, which was negative. During the patient’s current epilepsy work-up, he
10
S. Vadera et al. / Clinical Neurology and Neurosurgery 122 (2014) 9–11
Fig. 1. Ictal SPECT showing (a) coronal and (b) sagittal planes. Hyperperfusion can be noted in right posterior insular region and peri-rolandic region as well as left posterior cingulate gyrus and lateral temporal lobe (not shown).
underwent an ictal single-photon emission computed tomography (SPECT), which showed hyperperfusion in the right precentral rolandic area and right posterior insular regions as well as the left basal ganglia (Fig. 1). The case was presented at the multidisciplinary Epilepsy Management Conference and unanimous decision was that the patient had focal epilepsy possibly arising from the right perisylvian and insula regions based on the ictal semiology and ictal SPECT. Although vEEG was non-localizable and MRI was normal, the generated hypothesis was that his seizures might be explained by a deep-seated focus located in the peri-sylvian areas or in the adjacent insular cortex. Nevertheless, due to the lack of localizing and congruent information by the non-invasive methods, an invasive monitoring study was indicated. Due to the possibility of a deep-seated focus, SEEG implantation was the chosen invasive method. 2.2. Operations and perioperative course The patient underwent implantation of 11 SEEG electrodes in standard stereotactic fashion with no complications noted intraoperatively. Because of the preoperative hypothesis, the majority of the electrodes were concentrated within the right perisylvian, opercular regions and insula. The patient was monitored for eight days in the Epilepsy Monitoring Unit, during which he had multiple seizures that were all localized within a focal region within the M, S and R electrodes, which were located in the perisylvian rolandic area. To better delineate the EZ, MEG was performed on this patient using the Elekta Neuromag system at the Cleveland Clinic. The sources of interictal discharges were localized by single equivalent current dipole modeling using the xfit software and coregistration to the patient’s MRI using the MRILab software (both from Elekta Neuromag). This showed a tight cluster of dipoles all with a consistent vertical orientation in the right peri-rolandic opercular region, in close anatomical relation of the SEEG ictal activity recorded from electrodes S and R. The SEEG electrodes were removed on postoperative day eight and patient was discharged home (Fig. 2a–d). Two-months later, the patient was readmitted for a focal resection of the area that correlated with both the MEG spiking and the SEEG ictal areas. The M, R, and S scalp entry points were used to assist with the localization of the incision site and a curvilinear incision was performed. A small craniotomy was made that encompassed the three electrodes of interest and the MEG cluster. Stereotactic navigation was performed and a small piece of abnormally appearing tissue within the peri-rolandic opercular region (approximately 2 cm3 ) was removed and sent for pathology with the depth of the resection extending to the adjacent insular via (Fig. 2e and f).
2.3. Postoperative course The patient did well during the immediate post-operative period. As expected, a contralateral lower face weakness was noticed soon after surgery, but completely recovered after 2 weeks. The patient was last seen at the 24 month follow-up period and he remains completely seizure-free and is now completely off medication. The final pathology for this specimen was malformation of cortical development with balloon cells.
3. Discussion From an epilepsy surgery perspective, patients with nonlesional focal epilepsy are some of the most challenging patients to treat, with disappointing long-term seizure outcome results [4]. In select cases, excellent outcomes have been described when the EZ is localized based upon precise pre-surgical hypothesis and combined with the use of intracranial electrode monitoring [1]. We describe a patient who underwent simultaneous MEG and SEEG recordings and the subsequent seizure outcome after respective surgery. The concomitant SEEG ictal/interictal pattern recordings and the MEG cluster activity complemented one another, guiding the surgeon in performing a relative small focal resection, resulting in pathological substrate confirmation and sustained seizure control. This case highlights some of the advantages of coupling different non-invasive (MEG) and minimally invasive (SEEG) methods of explorations in patients with “difficult to localize epilepsy.” Ultimately, the combined approach offered an additional opportunity for seizure freedom associated with minimal morbidity, in a clinical scenario unlikely to be successfully resolved with the standard methods of invasive monitoring. The fact that the MEG dipoles correlated strongly with the SEEG ictal map lends a great deal of weight to the original hypothesis and further supported the SEEG data, even in the face of negative scalp vEEG recordings. The whole head recording capability of modern magnetoencephalographs provides localization data that complements the SEEG localization by “filling in the blanks” between SEEG electrodes. Recording MEG simultaneous with SEEG helps to clarify the extent of the abnormal activity being recorded by the SEEG electrodes and to reassure the surgical team that the SEEG electrodes are providing a complete picture [5]. While other studies have looked at MEG and intra-operative EEG or subdural depths and grids this case is the first described usage of concomitant SEEG and MEG studies and the outcome after focal resection of corresponding regions. In referencing previous studies not including SEEG, Knowlton stated that “nearly all MEG–EEG comparison studies” support the two studies as complimentary to
S. Vadera et al. / Clinical Neurology and Neurosurgery 122 (2014) 9–11
11
Fig. 2. Postoperative (a) AP X-ray after SEEG implantation, (b) electrode map showing three electrodes with ictal spikes (red circles), (c) coronal, and (d) sagittal MEG study showing large cluster of vertically oriented dipoles along right peri-rolandic opercular region, and postoperative MRI showing, (e) coronal, and (f) sagittal section along the resection cavity.
each other [2]. This study suggests that the same may be possible with SEEG. 4. Conclusion This case is the first described successful usage of concomitant SEEG and MEG studies and the outcome after focal resection of corresponding regions. The concomitant application of different modalities of exploration is promising, offering precise localization possibilities with minimal morbidity. Longer follow-up and larger cohorts will be necessary to validate the utility of the reported approach in patients with medical refractory focal epilepsy and “difficult to localize” epileptic foci.
References [1] Luders HO, Najm I, Nair D, Widdess-Walsh P, Bingman W. The epileptogenic zone: general principles. Epileptic Disord 2006;8(Suppl. 2):S1–9. [2] Knowlton R. Can Magnetoencephalography aid epilepsy surgery? Epilepsy Curr 2008;8(1):1–5. [3] Vadera S, Mullin J, Bulacio J, Najm I, Bingaman W, Gonzalez-Martinez J. Stereoelectroencephalography following subdural grid placement for difficult to localize epilepsy. Neurosurgery 2013;72(5):723–9. [4] Siegel AM, Jobst BC, Thadani VM, Rhodes CH, Lewis PJ, Roberts DW, et al. Medically intractable, localization-related epilepsy with normal MRI: presurgical evaluation and surgical outcome in 43 patients. Epilepsia 2001;42: 883–8. [5] Mamelak AN, Lopez N, Akhtari M, Sutherling WW. Magnetoencephalographydirected surgery in patients with neocortical epilepsy. J Neurosurg 2002;97(4):865–73.
