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Lobar localization in epilepsy patients: Comparison of EEG and MEG
International Congress Series 1300 (2007) 677 – 680
www.ics-elsevier.com
Lobar localization in epilepsy patients: Comparison of EEG and MEG Andrea Paulini a,⁎, Michael Fischer a , Gabriela Scheler a , Rüdiger Hopfengärtner a , Stefan Rampp a , Martin Kaltenhäuser a , Arnd Dörfler b , Michael Buchfelder c , Johann Romstöck c , Hermann Stefan a a
Epilepsy-and Neurocenter, Department of Neurology, Schabachanlage 6-10, 91054 Erlangen, Germany b Department of Neuroradiology, Schabachanlage 6-10, 91054 Erlangen, Germany c Department of Neurosurgery, Schabachanlage 6-10, 91054 Erlangen, Germany
Abstract. Epilepsy surgery is an established therapy for pharmacoresistant focal epilepsy. The contribution of MEG in presurgical evaluation compared to long-term video-EEG-monitoring is illustrated concerning at the resolution of anatomical lobes the additional benefit of MEG investigation in cases with ambiguous or without EEG findings. In total 84 subsequent patients with intractable focal epilepsy who underwent surgical treatment were included. Percentages of presurgical results located in one anatomical lobe of both diagnostic means were analyzed. In cases with a diagnostic finding, MEG localized in 84% within one anatomical lobe, ictal EEG in 70%, interictal EEG in 64%. In 20 of 84 patients no clear localization within one lobe was found either in interictal or in ictal EEG. In 10 of these cases MEG localized within one lobe matching the resected lobe. Five patients became seizure free and five had at least 50% reduction of seizure rate 1 year after resection. In summary MEG yields an important contribution to focus hypothesis in the workup for epilepsy surgery. © 2007 Elsevier B.V. All rights reserved. Keywords: Epilepsy surgery; Magnetoencephalography; Video-EEG-monitoring; Focus hypothesis; Lobar localization result
1. Introduction Epilepsy surgery requires preoperative localization of focal epileptic activity [1–5]. The center of gravity of epileptic activity is located within one anatomical lobe in the majority of ⁎ Corresponding author. Tel.: +49 91318536921; fax: +49 91318536469. E-mail address: [email protected] (A. Paulini). 0531-5131/ © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.ics.2007.03.010
678
A. Paulini et al. / International Congress Series 1300 (2007) 677–680
cases. The decision for surgery relies on the findings of several diagnostic procedures among them most prominently video-EEG. Video-EEG-monitoring is a widely applied technique in presurgical evaluation of epilepsy patients. Several studies concern the value of MEG in presurgical evaluation [6–15]. This study describes the contribution of MEG in respect to the results of video-EEG-monitoring in the presurgical evaluation focusing the part of circumscribed localizations limited to one anatomical lobe and the MEG results when video EEG failed to point to a single lobe. The presurgical focus hypothesis was derived from the resected lobe. 2. Patients and methods A total of 84 patients with intractable focal epilepsy, which had presurgical video-EEGmonitoring and MEG investigation as well as epilepsy surgery were included. The average age at the time of surgery was 36 years (range 13–66) (47 females, 37 males). Resections were temporal resections in 83%, 14 were extratemporal. Used data were retrieved from the epilepsy center's database. In case the diagnostic modality yielded a localization result, it was categorized into side and lobe. Percentages of presurgical results in one anatomical lobe (monolobar), multiple lobes (multilobar) or without localization findings were compared between the diagnostic means and the resection lobe. The postoperative outcome by Engel was used for validation. Video-EEG was continuously recorded for several days, on average for 6 days. A minimum of 19 gold plated silver electrodes were positioned due to the international 10/20 system extended by eight temporobasal and two sphenoidal electrodes. Additional electrodes were placed in extratemporal cases. Identified spikes and ictal data were visually analyzed for localization findings. Patients' description of aura and behaviour during seizure onset lead to localization of semiology (side and/or lobe). MEG recordings were performed using a two-unit 74-channel system with first order gradiometers (MagnesII, 4-D Neuroimaging, San Diego, CA, USA). On average MEG was recorded in two to four different sensor positions lasting 20 to 30 min each. Measurement positions and durations were based on previous diagnostic findings. Epileptic spikes were visually identified. A single dipole analysis assuming a spherical head model was performed by MSI-software (4D-Neuroimaging). 3. Results If a localization result was in MEG found (57 patients of 84 in MEG), MEG results localized within one anatomical lobe in 84%. Ictal EEG localized in one lobe in 70%, interictal Table 1 Percentages of monolobar localizations for all studied modalities No localization (number) Localization result total (number) Monolobar (%) Multilobar (%) MEG 27 Semiology 11 Interictal EEG 7 Ictal EEG 11
57 73 77 73
48 35 49 51
(84%) (48%) (64%) (70%)
9 (16%) 38 (52%) 28 (36%) 22 (30%)
A. Paulini et al. / International Congress Series 1300 (2007) 677–680
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EEG in 64%. Seizure semiology was indicating monolobar localization in 48%. In summary see Table 1. Surgical resection lobe was identical with the single lobe identified by MEG in 88% (n = 42 of 48 patients), by interictal EEG in 92% (n = 45 of 49) and by ictal in 92% either (n = 47 of 51). For the patients with monolobar localizations matching the resection lobe good outcome (Engel classification 1 to 3A 1 year after resection) was achieved for MEG in 90% (n = 38 of 42), for interictal EEG in 80% (n = 36 of 45) and for ictal EEG in 83% (n = 39 of 47). In 20 of the total of 84 patients there was neither in ictal nor in interictal EEG localization within one lobe. In 10 (50%) of these 20 cases MEG localized within the resection lobe. The other 10 cases had no spikes (8) or a multilobar result in MEG. These 10 patients with clear monolobar localization in MEG all showed at least 50% reduced seizure rate 1 year after resection (Engel classification 1 to 3A), five became seizure free. For results separated into interictal EEG, ictal EEG alone and combined see Fig. 1. 4. Discussion For epilepsy surgery a presurgical focus hypothesis with one main focus is necessary. This implies that a circumscribed focus, limited to one lobe is the desired result for all diagnostic methods in the presurgical decision-making process. In patients with spikes in MEG, MEG had the highest percentage of localizations confined to only one anatomical lobe. Monolobar resection lobe matching cases in MEG had good outcomes in 90%. MEG provided results within one lobe matching the resection lobe in about half of the patients, when ictal/interictal video-EEG gave no or a multilobar result. The chance to get a focus result by MEG was relatively constant (50%), no matter whether ictal or interictal EEG or both provided an inconclusive localization result. All patients without conclusive EEG localization information and with monolobar resection lobe matching MEG localization had an improved postoperative outcome. These results are comparable to a study of 113 epilepsy
Fig. 1. MEG localizations in patients where EEG did not indicate a single lobe: interictal EEG (n=35), ictal EEG (n=33) and combined (n=20), (numbers in columns show absolute number of patients, black=monolobar resection lobe matching cases, white=monolobar non-matching cases, hatched right=multilobar localization results, hatched left=no localization results).
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A. Paulini et al. / International Congress Series 1300 (2007) 677–680
surgery patients where MEG yielded additional focus information to video-EEG-monitoring in 40% [16]. MEG indicated the side of the resection in a higher rate compared to ictal and interictal EEG [17]. Nakasato and colleagues [18] saw excellent agreement between MEG dipole sources and ECoG sources as well as surgical outcome and presence of MRI lesions in 6 patients and found less consistent results by EEG source analyses compared to MEG. These findings at the resolution of anatomical lobes support that MEG is a valuable complementary modality to video-EEG and provide additional information for presurgical focus hypothesis of particular importance when the results of the video-EEG-monitoring do not yield a monolobar result. References [1] C. Tonini, et al., Predictors of epilepsy surgery outcome: a meta-analysis, Epilepsy Res. 62 (1) (Nov 2004) 75–87. [2] C. Kilpatrick, et al., Non-invasive investigations successfully select patients for temporal lobe surgery, J. Neurol. Neurosurg. Psychiatry 63 (3) (Sep 1997) 327–333. [3] V.M. Thadani, et al., Successful epilepsy surgery without intracranial EEG recording: criteria for patient selection, Epilepsia 36 (1) (1995) 7–15. [4] A.T. Berg, et al., The multicenter study of epilepsy surgery: recruitment and selection for surgery, Epilepsia 44 (11) (Nov 2003) 1425–1433. [5] R.X. Xu, et al., Temporal lobe epilepsy surgery and preoperative factors predictive of postoperative outcome: retrospective analysis of 143 cases, Di Yi Jun Yi Da Xue Xue Bao 23 (7) (Jul 2003) 663–667. [6] C. Baumgartner, E. Pataraia, Revisiting the role of magnetoencephalography in epilepsy, Curr. Opin. Neurol. 19 (2) (Apr 2006) 181–186. [7] A.C. Papanicolaou, et al., A review of clinical applications of magnetoencephalography, Int. Rev. Neurobiol. 68 (2005) 223–247. [8] M. Oishi, et al., Single and multiple clusters of magnetoencephalographic dipoles in neocortical epilepsy: significance in characterizing the epileptogenic zone, Epilepsia 47 (2) (Feb 2006) 355–364. [9] H. Stefan, G. Scheler, M.J.M. Fischer, Stellenwert der Magnetenzephalographie für die Epilepsiediagnostik, Klin. Neurophys. 4. (2003). [10] H. Stefan, et al., Magnetic brain source imaging of focal epileptic activity: a synopsis of 455 cases, Brain 126 (7/2003) 1–10. [11] H. Stefan, et al., Magnetic source localization and morphological changes in temporal lobe epilepsy: comparison of MEG/EEG, ECoG and volumetric MRI in presurgical evaluation of operated patients, Acta Neurol. Scand., Suppl. 152 (1994) 83–88. [12] B.A. Minassian, et al., Magnetoencephalographic localization in pediatric epilepsy surgery: comparison with invasive intracranial electroencephalography, Ann. Neurol. 46 (4) (10/1999) 627–633. [13] M. Aung, et al., Potential contribution of bilateral magnetic source imaging to the evaluation of epilepsy surgery candidates, Neurosurgery 37 (6) (1995) 1113–1120. [14] M. Oishi, et al., Epileptic spikes: magnetoencephalography versus simultaneous electrocorticography, Epilepsia 43 (11) (Nov 2002) 1390–1395. [15] M. Iwasaki, et al., Detection of epileptiform activity by human interpreters: blinded comparison between electroencephalography and magnetoencephalography, Epilepsia 46 (1) (Jan 2005) 59–68. [16] E. Pataraia, et al., Does magnetoencephalography add to scalp video-EEG as a diagnostic tool in epilepsy surgery? Neurology 62 (6) (Mar 23 2004) 943–948. [17] J.W. Wheless, et al., A comparison of magnetoencephalography, MRI, and V-EEG in patients evaluated for epilepsy surgery, Epilepsia 40 (7) (7/1999) 931–941. [18] N. Nakasato, et al., Comparisons of MEG, EEG, and ECoG source localization in neocortical partial epilepsy in humans, Electroencephalogr. Clin. Neurophysiol. 91 (3) (1994) 171–178.
www.ics-elsevier.com
Lobar localization in epilepsy patients: Comparison of EEG and MEG Andrea Paulini a,⁎, Michael Fischer a , Gabriela Scheler a , Rüdiger Hopfengärtner a , Stefan Rampp a , Martin Kaltenhäuser a , Arnd Dörfler b , Michael Buchfelder c , Johann Romstöck c , Hermann Stefan a a
Epilepsy-and Neurocenter, Department of Neurology, Schabachanlage 6-10, 91054 Erlangen, Germany b Department of Neuroradiology, Schabachanlage 6-10, 91054 Erlangen, Germany c Department of Neurosurgery, Schabachanlage 6-10, 91054 Erlangen, Germany
Abstract. Epilepsy surgery is an established therapy for pharmacoresistant focal epilepsy. The contribution of MEG in presurgical evaluation compared to long-term video-EEG-monitoring is illustrated concerning at the resolution of anatomical lobes the additional benefit of MEG investigation in cases with ambiguous or without EEG findings. In total 84 subsequent patients with intractable focal epilepsy who underwent surgical treatment were included. Percentages of presurgical results located in one anatomical lobe of both diagnostic means were analyzed. In cases with a diagnostic finding, MEG localized in 84% within one anatomical lobe, ictal EEG in 70%, interictal EEG in 64%. In 20 of 84 patients no clear localization within one lobe was found either in interictal or in ictal EEG. In 10 of these cases MEG localized within one lobe matching the resected lobe. Five patients became seizure free and five had at least 50% reduction of seizure rate 1 year after resection. In summary MEG yields an important contribution to focus hypothesis in the workup for epilepsy surgery. © 2007 Elsevier B.V. All rights reserved. Keywords: Epilepsy surgery; Magnetoencephalography; Video-EEG-monitoring; Focus hypothesis; Lobar localization result
1. Introduction Epilepsy surgery requires preoperative localization of focal epileptic activity [1–5]. The center of gravity of epileptic activity is located within one anatomical lobe in the majority of ⁎ Corresponding author. Tel.: +49 91318536921; fax: +49 91318536469. E-mail address: [email protected] (A. Paulini). 0531-5131/ © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.ics.2007.03.010
678
A. Paulini et al. / International Congress Series 1300 (2007) 677–680
cases. The decision for surgery relies on the findings of several diagnostic procedures among them most prominently video-EEG. Video-EEG-monitoring is a widely applied technique in presurgical evaluation of epilepsy patients. Several studies concern the value of MEG in presurgical evaluation [6–15]. This study describes the contribution of MEG in respect to the results of video-EEG-monitoring in the presurgical evaluation focusing the part of circumscribed localizations limited to one anatomical lobe and the MEG results when video EEG failed to point to a single lobe. The presurgical focus hypothesis was derived from the resected lobe. 2. Patients and methods A total of 84 patients with intractable focal epilepsy, which had presurgical video-EEGmonitoring and MEG investigation as well as epilepsy surgery were included. The average age at the time of surgery was 36 years (range 13–66) (47 females, 37 males). Resections were temporal resections in 83%, 14 were extratemporal. Used data were retrieved from the epilepsy center's database. In case the diagnostic modality yielded a localization result, it was categorized into side and lobe. Percentages of presurgical results in one anatomical lobe (monolobar), multiple lobes (multilobar) or without localization findings were compared between the diagnostic means and the resection lobe. The postoperative outcome by Engel was used for validation. Video-EEG was continuously recorded for several days, on average for 6 days. A minimum of 19 gold plated silver electrodes were positioned due to the international 10/20 system extended by eight temporobasal and two sphenoidal electrodes. Additional electrodes were placed in extratemporal cases. Identified spikes and ictal data were visually analyzed for localization findings. Patients' description of aura and behaviour during seizure onset lead to localization of semiology (side and/or lobe). MEG recordings were performed using a two-unit 74-channel system with first order gradiometers (MagnesII, 4-D Neuroimaging, San Diego, CA, USA). On average MEG was recorded in two to four different sensor positions lasting 20 to 30 min each. Measurement positions and durations were based on previous diagnostic findings. Epileptic spikes were visually identified. A single dipole analysis assuming a spherical head model was performed by MSI-software (4D-Neuroimaging). 3. Results If a localization result was in MEG found (57 patients of 84 in MEG), MEG results localized within one anatomical lobe in 84%. Ictal EEG localized in one lobe in 70%, interictal Table 1 Percentages of monolobar localizations for all studied modalities No localization (number) Localization result total (number) Monolobar (%) Multilobar (%) MEG 27 Semiology 11 Interictal EEG 7 Ictal EEG 11
57 73 77 73
48 35 49 51
(84%) (48%) (64%) (70%)
9 (16%) 38 (52%) 28 (36%) 22 (30%)
A. Paulini et al. / International Congress Series 1300 (2007) 677–680
679
EEG in 64%. Seizure semiology was indicating monolobar localization in 48%. In summary see Table 1. Surgical resection lobe was identical with the single lobe identified by MEG in 88% (n = 42 of 48 patients), by interictal EEG in 92% (n = 45 of 49) and by ictal in 92% either (n = 47 of 51). For the patients with monolobar localizations matching the resection lobe good outcome (Engel classification 1 to 3A 1 year after resection) was achieved for MEG in 90% (n = 38 of 42), for interictal EEG in 80% (n = 36 of 45) and for ictal EEG in 83% (n = 39 of 47). In 20 of the total of 84 patients there was neither in ictal nor in interictal EEG localization within one lobe. In 10 (50%) of these 20 cases MEG localized within the resection lobe. The other 10 cases had no spikes (8) or a multilobar result in MEG. These 10 patients with clear monolobar localization in MEG all showed at least 50% reduced seizure rate 1 year after resection (Engel classification 1 to 3A), five became seizure free. For results separated into interictal EEG, ictal EEG alone and combined see Fig. 1. 4. Discussion For epilepsy surgery a presurgical focus hypothesis with one main focus is necessary. This implies that a circumscribed focus, limited to one lobe is the desired result for all diagnostic methods in the presurgical decision-making process. In patients with spikes in MEG, MEG had the highest percentage of localizations confined to only one anatomical lobe. Monolobar resection lobe matching cases in MEG had good outcomes in 90%. MEG provided results within one lobe matching the resection lobe in about half of the patients, when ictal/interictal video-EEG gave no or a multilobar result. The chance to get a focus result by MEG was relatively constant (50%), no matter whether ictal or interictal EEG or both provided an inconclusive localization result. All patients without conclusive EEG localization information and with monolobar resection lobe matching MEG localization had an improved postoperative outcome. These results are comparable to a study of 113 epilepsy
Fig. 1. MEG localizations in patients where EEG did not indicate a single lobe: interictal EEG (n=35), ictal EEG (n=33) and combined (n=20), (numbers in columns show absolute number of patients, black=monolobar resection lobe matching cases, white=monolobar non-matching cases, hatched right=multilobar localization results, hatched left=no localization results).
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A. Paulini et al. / International Congress Series 1300 (2007) 677–680
surgery patients where MEG yielded additional focus information to video-EEG-monitoring in 40% [16]. MEG indicated the side of the resection in a higher rate compared to ictal and interictal EEG [17]. Nakasato and colleagues [18] saw excellent agreement between MEG dipole sources and ECoG sources as well as surgical outcome and presence of MRI lesions in 6 patients and found less consistent results by EEG source analyses compared to MEG. These findings at the resolution of anatomical lobes support that MEG is a valuable complementary modality to video-EEG and provide additional information for presurgical focus hypothesis of particular importance when the results of the video-EEG-monitoring do not yield a monolobar result. References [1] C. Tonini, et al., Predictors of epilepsy surgery outcome: a meta-analysis, Epilepsy Res. 62 (1) (Nov 2004) 75–87. [2] C. Kilpatrick, et al., Non-invasive investigations successfully select patients for temporal lobe surgery, J. Neurol. Neurosurg. Psychiatry 63 (3) (Sep 1997) 327–333. [3] V.M. Thadani, et al., Successful epilepsy surgery without intracranial EEG recording: criteria for patient selection, Epilepsia 36 (1) (1995) 7–15. [4] A.T. Berg, et al., The multicenter study of epilepsy surgery: recruitment and selection for surgery, Epilepsia 44 (11) (Nov 2003) 1425–1433. [5] R.X. Xu, et al., Temporal lobe epilepsy surgery and preoperative factors predictive of postoperative outcome: retrospective analysis of 143 cases, Di Yi Jun Yi Da Xue Xue Bao 23 (7) (Jul 2003) 663–667. [6] C. Baumgartner, E. Pataraia, Revisiting the role of magnetoencephalography in epilepsy, Curr. Opin. Neurol. 19 (2) (Apr 2006) 181–186. [7] A.C. Papanicolaou, et al., A review of clinical applications of magnetoencephalography, Int. Rev. Neurobiol. 68 (2005) 223–247. [8] M. Oishi, et al., Single and multiple clusters of magnetoencephalographic dipoles in neocortical epilepsy: significance in characterizing the epileptogenic zone, Epilepsia 47 (2) (Feb 2006) 355–364. [9] H. Stefan, G. Scheler, M.J.M. Fischer, Stellenwert der Magnetenzephalographie für die Epilepsiediagnostik, Klin. Neurophys. 4. (2003). [10] H. Stefan, et al., Magnetic brain source imaging of focal epileptic activity: a synopsis of 455 cases, Brain 126 (7/2003) 1–10. [11] H. Stefan, et al., Magnetic source localization and morphological changes in temporal lobe epilepsy: comparison of MEG/EEG, ECoG and volumetric MRI in presurgical evaluation of operated patients, Acta Neurol. Scand., Suppl. 152 (1994) 83–88. [12] B.A. Minassian, et al., Magnetoencephalographic localization in pediatric epilepsy surgery: comparison with invasive intracranial electroencephalography, Ann. Neurol. 46 (4) (10/1999) 627–633. [13] M. Aung, et al., Potential contribution of bilateral magnetic source imaging to the evaluation of epilepsy surgery candidates, Neurosurgery 37 (6) (1995) 1113–1120. [14] M. Oishi, et al., Epileptic spikes: magnetoencephalography versus simultaneous electrocorticography, Epilepsia 43 (11) (Nov 2002) 1390–1395. [15] M. Iwasaki, et al., Detection of epileptiform activity by human interpreters: blinded comparison between electroencephalography and magnetoencephalography, Epilepsia 46 (1) (Jan 2005) 59–68. [16] E. Pataraia, et al., Does magnetoencephalography add to scalp video-EEG as a diagnostic tool in epilepsy surgery? Neurology 62 (6) (Mar 23 2004) 943–948. [17] J.W. Wheless, et al., A comparison of magnetoencephalography, MRI, and V-EEG in patients evaluated for epilepsy surgery, Epilepsia 40 (7) (7/1999) 931–941. [18] N. Nakasato, et al., Comparisons of MEG, EEG, and ECoG source localization in neocortical partial epilepsy in humans, Electroencephalogr. Clin. Neurophysiol. 91 (3) (1994) 171–178.