Electroencephalographic source imaging: a prospective study of 152 operated epileptic patients

Verena Brodbeck, Laurent Spinelli, Agustina M Lascano, Michael Wissmeier, Maria-Isabel Vargas, Serge Vulliemoz, Claudio Pollo, Karl Schaller, Christoph M Michel, Margitta Seeck, Verena Brodbeck, Laurent Spinelli, Agustina M Lascano, Michael Wissmeier, Maria-Isabel Vargas, Serge Vulliemoz, Claudio Pollo, Karl Schaller, Christoph M Michel, Margitta Seeck

Abstract

Electroencephalography is mandatory to determine the epilepsy syndrome. However, for the precise localization of the irritative zone in patients with focal epilepsy, costly and sometimes cumbersome imaging techniques are used. Recent small studies using electric source imaging suggest that electroencephalography itself could be used to localize the focus. However, a large prospective validation study is missing. This study presents a cohort of 152 operated patients where electric source imaging was applied as part of the pre-surgical work-up allowing a comparison with the results from other methods. Patients (n = 152) with >1 year postoperative follow-up were studied prospectively. The sensitivity and specificity of each imaging method was defined by comparing the localization of the source maximum with the resected zone and surgical outcome. Electric source imaging had a sensitivity of 84% and a specificity of 88% if the electroencephalogram was recorded with a large number of electrodes (128-256 channels) and the individual magnetic resonance image was used as head model. These values compared favourably with those of structural magnetic resonance imaging (76% sensitivity, 53% specificity), positron emission tomography (69% sensitivity, 44% specificity) and ictal/interictal single-photon emission-computed tomography (58% sensitivity, 47% specificity). The sensitivity and specificity of electric source imaging decreased to 57% and 59%, respectively, with low number of electrodes (<32 channels) and a template head model. This study demonstrated the validity and clinical utility of electric source imaging in a large prospective study. Given the low cost and high flexibility of electroencephalographic systems even with high channel counts, we conclude that electric source imaging is a highly valuable tool in pre-surgical epilepsy evaluation.

Figures

Figure 1
Figure 1
Illustration of the different steps of electric source imaging. (Left) Workflow of the EEG analysis. Spikes are manually selected from the EEG (here: 256 channels) and averaged. The potential map at 50% of the rising phase of the averaged spike is used for source analysis. (Right) Workflow of the automatic MRI analysis. Segmentation of the brain and grey matter allowed building a simplified realistic head model (SMAC model) with the solution points distributed in the grey matter of the individual brain. This head model is used for the inverse solution calculation, which in this study was based on a distributed linear inverse solution called LAURA.
Figure 2
Figure 2
Examples of correct EEG source localization in operated and seizure-free patients. (A) Thirty-five-year-old patient with right frontal epilepsy and normal MRI. After subdural recordings, a polar frontal lobectomy was performed, which rendered the patient seizure-free. Histopathology revealed cortical dysplasia and gliosis. The green spot indicates the source maximum, which is superimposed on the postoperative MRI with the resected area marked in black. (B) Twenty-two-year-old patient with temporal lobe epilepsy and normal MRI. After depth recordings a left anterior temporal lobectomy was performed. Histopathology showed gliotic changes. The source maximum (green) was found within the resected area indicated in black. (C) Six-year-old female with a left occipital cystic lesion due to a ganglioglioma. A partial parieto-occipital lobectomy rendered the patient seizure-free. The source maximum was found in the occipital perilesional space (green) and lay within the resected area (indicated as blue spot in the red area that marks the resected zone).
Figure 3
Figure 3
Example of a patient who was not seizure-free after operation; an 18-year-old patient with a surgical intervention in the right frontal posterior area (indicated in red) as suggested by intracranial recordings. The patient continued to have seizures after surgery. The electric source imaging source (green) showed a right insular maximum, which was concordant with a local hypometabolism found in the PET (right).
Figure 4
Figure 4
Example of a patient with non-concordant results between high- and low-resolution electric source imaging. Solutions using a template MRI are shown on the left, with the individual MRI on the right, low-resolution electric source imaging source superposed in green and high-resolution electric source imaging in red. The patient is a 13-year-old male with Engel Class II outcome after resection of the left temporal lobe. Only high-resolution electric source imaging based on the individual MRI correctly indicated a left anterior temporal source. Low- and high-resolution electric source imaging based on the template MRI indicated a parietal source.
Figure 5
Figure 5
Sensitivity and specificity of the different imaging methods with respect to surgery outcome. High-resolution EEG with 128 or 256 electrodes had highest sensitivity (correct localization in seizure-free or almost seizure-free patients, Engel Classes I and II) and highest specificity (not localized in the resected zone in patients and without major benefit from surgery, Engel Classes III and IV). HR-ESI = high-resolution electric source imaging; LR-ESI = low-resolution electric source imaging; SOZ = seizure onset zone.

References

    1. Ahlfors SP, Han J, Belliveau JW, Hamalainen MS. Sensitivity of MEG and EEG to source orientation. Brain Topogr. 2010;23:227–32.
    1. Alarcon G, Guy CN, Binnie CD, Walker SR, Elwes RD, Polkey CE. Intracerebral propagation of interictal activity in partial epilepsy: implications for source localisation. J Neurol Neurosurg Psychiatry. 1994;57:435–49.
    1. Ary JP, Klein SA, Fender DH. Location of sources of evoked scalp potentials: Corrections for skull and scalp thicknesses. IEEE Trans Biomed Eng. 1981;28:834–6.
    1. Asano E, Muzik O, Shah A, Juhasz C, Chugani DC, Sood S, et al. Quantitative interictal subdural EEG analyses in children with neocortical epilepsy. Epilepsia. 2003;44:425–34.
    1. Brodbeck V, Lascano AM, Spinelli L, Seeck M, Michel CM. Accuracy of EEG source imaging of epileptic spikes in patients with large brain lesions. Clin Neurophysiol. 2009;120:679–85.
    1. Brodbeck V, Spinelli L, Lascano AM, Pollo C, Schaller K, Vargas MI, et al. Electrical source imaging for presurgical focus localization in epilepsy patients with normal MRI. Epilepsia. 2010;51:583–91.
    1. Brunet D, Murray MM, Michel CM. Spatiotemporal analysis of multichannel EEG: CARTOOL. Comput Intell Neurosci. 2011;2011 doi:10.1155/2011/813870.
    1. Chatrian GE Report on the Committee on Terminology. Proceedings of the General Assembly. The VIIIth International £Congress of Electroencephalography and Clinical Neurophysiology. Electroencephalogr Clin Neurophysiol. 1974;37:521–53.
    1. Emerson RG, Turner CA, Pedley TA, Walczak TS, Forgione M. Propagation patterns of temporal spikes. Electroencephalogr Clin Neurophysiol. 1995;94:338–48.
    1. Fuchs M, Wagner M, Kastner J. Development of volume conductor and source models to localize epileptic foci. J Clin Neurophysiol. 2007;24:101–19.
    1. Gavaret M, Badier JM, Marquis P, Bartolomei F, Chauvel P. Electric source imaging in temporal lobe epilepsy. J Clin Neurophysiol. 2004;21:267–82.
    1. Gavaret M, Trebuchon A, Bartolomei F, Marquis P, McGonigal A, Wendling F, et al. Source localization of scalp-EEG interictal spikes in posterior cortex epilepsies investigated by HR-EEG and SEEG. Epilepsia. 2009;50:276–89.
    1. Grave de Peralta Menendez R, Murray MM, Michel CM, Martuzzi R, Gonzalez Andino SL. Electrical neuroimaging based on biophysical constraints. Neuroimage. 2004;21:527–39.
    1. Groening K, Brodbeck V, Moeller F, Wolff S, van Baalen A, Michel CM, et al. Combination of EEG-fMRI and EEG source analysis improves interpretation of spike-associated activation networks in paediatric pharmacoresistant focal epilepsies. Neuroimage. 2009;46:827–33.
    1. Grouiller F, Thornton RC, Groening K, Spinelli L, Duncan JS, Schaller K, et al. With or without spikes: localization of focal epileptic activity by simultaneous electroencephalography and functional magnetic resonance imaging. Brain. 2011;134:2867–86.
    1. Guggisberg AG, Dalal SS, Zumer JM, Wong DD, Dubovik S, Michel CM, et al. Localization of cortico-peripheral coherence with electroencephalography. Neuroimage. 2011;57:1348–57.
    1. Huppertz HJ, Hof E, Klisch J, Wagner M, Lücking CH, Kristeva-Feige R. Localization of interictal delta and epileptiform EEG activity associated with focal epileptogenic brain lesions. Neuroimage. 2001;13:15–28.
    1. Henry TR, Van Heertum RL. Positron emission tomography and single photon emission computed tomography in epilepsy care. Semin Nucl Med. 2003;33:88–104.
    1. Holmes MD, Tucker DM, Quiring JM, Hakimian S, Miller JW, Ojemann JG. Comparing noninvasive dense array and intracranial electroencephalography for localization of seizures. Neurosurgery. 2008;66:354–62.
    1. Kaiboriboon K, Nagarajan S, Mantle M, Kirsch HE. Interictal MEG/magnetic source imaging in intractable mesial temporal lobe epilepsy: spike yield and characterization. Clin Neurophysiol. 2010;121:325–31.
    1. Knowlton RC, Elgavish RA, Bartolucci A, Ojha B, Limdi N, Blount J, et al. Functional imaging: II. Prediction of epilepsy surgery outcome. Ann Neurol. 2008;64:35–41.
    1. Knowlton RC, Razdan SN, Limdi N, Elgavish RA, Killen J, Blount J, et al. Effect of epilepsy magnetic source imaging on intracranial electrode placement. Ann Neurol. 2009;65:716–23.
    1. Lantz G, Grave de Peralta Menendez R, Gonzalez Andino S, Michel CM. Noninvasive localization of electromagnetic epileptic activity. II. Demonstration of sublobar accuracy in patients with simultaneous surface and depth recordings. Brain Topogr. 2001;14:139–47.
    1. Lantz G, Spinelli L, Seeck M, de Peralta Menendez RG, Sottas CC, Michel CM. Propagation of interictal epileptiform activity can lead to erroneous source localizations: a 128-channel EEG mapping study. J Clin Neurophysiol. 2003;20:311–9.
    1. Leijten FS, Huiskamp GJ, Hilgersom I, Van Huffelen AC. High-resolution source imaging in mesiotemporal lobe epilepsy: a comparison between MEG and simultaneous EEG. J Clin Neurophysiol. 2003;20:227–38.
    1. Manford M, Fish DR, Shorvon SD. An analysis of clinical seizure patterns and their localizing value in frontal and temporal lobe epilepsies. Brain. 1996;119:17–40.
    1. McGonigal A, Bartolomei F, Régis J, Guye M, Gavaret M, Trébuchon-Da Fonseca A, et al. Stereoelectroencephalography in presurgical assessment of MRI-negative epilepsy. Brain. 2007;130:3169–83.
    1. Michel CM, He B. EEG Mapping and source imaging. In: Schomer D, Lopes da Silva F, editors. Niedermeyer’s electroencephalography. 6th edn. Chapter 55. Lippincott Williams & Wilkins; 2011. pp. 1179–202.
    1. Michel CM, Lantz G, Spinelli L, De Peralta RG, Landis T, Seeck M. 128-channel EEG source imaging in epilepsy: clinical yield and localization precision. J Clin Neurophysiol. 2004b;21:71–83.
    1. Michel CM, Murray MM, Lantz G, Gonzalez S, Spinelli L, Grave de Peralta R. EEG source imaging. Clin Neurophysiol. 2004a;115:2195–222.
    1. Nahum L, Gabriel D, Spinelli L, Momjian S, Seeck M, Michel CM, et al. Rapid consolidation and the human hippocampus: Intracranial recordings confirm surface EEG. Hippocampus. 2011;21:689–93.
    1. Nayak D, Valentín A, Alarcón G, García Seoane JJ, Brunnhuber F, Juler J, et al. Characteristics of scalp electrical fields associated with deep medial temporal epileptiform discharges. Clin Neurophysiol. 2004;115:1423–35.
    1. Phillips C, Mattout J, Rugg MD, Maquet P, Friston KJ. An empirical Bayesian solution to the source reconstruction problem in EEG. Neuroimage. 2005;24:997–1011.
    1. Plummer C, Harvey AS, Cook M. EEG source localization in focal epilepsy: where are we now? Epilepsia. 2008;49:201–18.
    1. Ray A, Tao JX, Hawes-Ebersole SM, Ebersole JS. Localizing value of scalp EEG spikes: a simultaneous scalp and intracranial study. Clin Neurophysiol. 2007;118:69–79.
    1. Rose S, Ebersole JS. Advances in spike localization with EEG dipole modeling. Clin EEG Neurosci. 2009;40:281–7.
    1. Seo JH, Holland K, Rose D, Rozhkov L, Fujiwara H, Byars A, et al. Multimodality imaging in the surgical treatment of children with nonlesional epilepsy. Neurology. 2011;76:41–8.
    1. Seeck M, Schomer DL, Bergey GK, Niedermeyer E. Intracranial monitoring: depth, subdural and foramen ovale electrodes. In: Schomer DL, Lopes da Silva F, editors. Niedermeyer's textbook of electroencephalography: basic principles, clinical applications, and related fields. VI edn. Chapter 33. Wolters Kluwer and Lippincott; 2010.
    1. Siniatchkin M, Groening K, Moehring J, Moeller F, Boor R, Brodbeck V, et al. Neuronal networks in children with continuous spikes and waves during slow sleep. Brain. 2010;133:2798–813.
    1. Spanaki MV, Spencer SS, Corsi M, MacMullan J, Seibyl J, Zubal IG. Sensitivity and specificity of quantitative difference SPECT analysis in seizure localization. J Nucl Med. 1999;40:730–6.
    1. Sperli F, Spinelli L, Seeck M, Kurian M, Michel CM, Lantz G. EEG source imaging in pediatric epilepsy surgery: a new perspective in presurgical workup. Epilepsia. 2006;47:981–90.
    1. Spinelli L, Andino SG, Lantz G, Seeck M, Michel CM. Electromagnetic inverse solutions in anatomically constrained spherical head models. Brain Topogr. 2000;13:115–25.
    1. Stern Y, Neufeld MY, Kipervasser S, Zilberstein A, Fried I, Teicher M, et al. Source localization of temporal lobe epilepsy using PCA-LORETA analysis on ictal EEG recordings. J Clin Neurophysiol. 2009;26:109–16.
    1. Sutherling WW, Mamelak AN, Thyerlei D, Maleeva T, Minazad Y, Philpott L, et al. Influence of magnetic source imaging for planning intracranial EEG in epilepsy. Neurology. 2008;71:990–6.
    1. Thornton R, Laufs H, Rodionov R, Cannadathu S, Carmichael DW, Vulliemoz S, et al. EEG correlated functional MRI and postoperative outcome in focal epilepsy. J Neurol Neurosurg Psychiatry. 2010;81:922–7.
    1. Urrestarazu E, Chander R, Dubeau F, Gotman J. Interictal high-frequency oscillations (100-500 Hz) in the intracerebral EEG of epileptic patients. Brain. 2007;130:2354–66.
    1. Vergult A, De Clercq W, Palmini A, Vanrumste B, Dupont P, Van Huffel S, et al. Improving the interpretation of ictal scalp EEG: BSS-CCA algorithm for muscle artifact removal. Epilepsia. 2007;48:950–8.
    1. Vulliemoz S, Rodionov R, Carmichael DW, Thornton R, Guye M, Lhatoo SD, et al. Continuous EEG source imaging enhances analysis of EEG-fMRI in focal epilepsy. Neuroimage. 2010;49:3219–29.
    1. Vulliemoz S, Thornton R, Rodionov R, Carmichael DW, Guye M, Lhatoo S, et al. The spatio-temporal mapping of epileptic networks: combination of EEG-fMRI and EEG source imaging. Neuroimage. 2009;46:834–43.
    1. Walczak TS, Jayakar P, Mizrahi EM. Interictal encephalography. In: Engel J Jr, Pedley TA, editors. Epilepsy – a comprehensive textbook. 2nd edn. Wolters-Kluwer Lippincott Williams & Wilkins; 2008. pp. 809–823.
    1. Wennberg R, Valiante T, Cheyne D. EEG and MEG in mesial temporal lobe epilepsy: where do the spikes really come from? Clin Neurophysiol. 2011;122:1295–313.
    1. Worrell GA, Gardner AB, Stead SM, Hu S, Goerss S, Cascino GJ, et al. High-frequency oscillations in human temporal lobe: simultaneous microwire and clinical macroelectrode recordings. Brain. 2008;13:928–37.
    1. Zumsteg D, Friedman A, Wennberg RA, Wieser HG. Source localization of mesial temporal interictal epileptiform discharges: correlation with intracranial foramen ovale electrode recordings. Clin Neurophysiol. 2005;116:2810–8.
    1. Zumsteg D, Friedman A, Wieser HG, Wennberg RA. Source localization of interictal epileptiform discharges: comparison of three different techniques to improve signal to noise ratio. Clin Neurophysiol. 2006;117:562–71.

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