Hochfrequenzoszillationen (>80 Hz) als Marker für epileptogene Areale

Zusammenfassung

EEG-Frequenzen oberhalb von 80 Hz haben in den letzten Jahren zunehmend an Bedeutung gewonnen. Besonders im Bereich der prächirurgischen Epilepsidiagnostik bei Patienten mit therapierefraktärer Epilepsie verspricht die Analyse von physiologischen und pathologischen Hochfrequenzoszillationen (HFOs) zwischen 80–500 Hz die bisherigen diagnostischen Möglichkeiten zu verbessern. Im intrakraniellen EEG aufgezeichnete pathologische HFOs lassen sich klar von anderen EEG-Markern wie epileptischen Spikes unterscheiden. HFOs zeigen eine stärkere Verbindung zu epileptogenen Arealen und ihre intraoperative Entfernung korreliert mit der postoperativen Anfallsfreiheit. Zusätzlich hat die Analyse von Hochfrequenzoszillationen den entscheidenenden Vorteil, dass für ihre Erfassung 5 min intrakranielles EEG oder sogar intraoperativ aufgezeichnetem EEG-Abschnitte ausreichen. Hierdurch könnte die notwendige Zeit der EEG-Aufzeichnung im Sinne des Patienten verkürzt werden. Neuere Studien zeigen HFOs, die im Oberflächen-EEG aufgezeichnet wurden. Dies eröffnet die Möglichkeit zu Langzeitstudien und der Untersuchung von weniger komplizierten Epilepsien. Dieser Review fasst das bisherige Wissen zu physiologischen und pathologischen HFOs bei Epilepsien zusammen. Klinische Anwendungsmöglichkeiten und methodische Schwierigkeiten von HFOs als Marker für epileptogene Areale werden diskutiert.

Abstract

Frequencies above 80 Hz have gained importance in the analysis of EEG over the past few years. Especially in the presurgical evaluation of patients with refractory epilepsy, the analysis of physiological as well as pathological high frequency oscillations (HFO) may lead to improved diagnostic possibilities. Pathological HFOs recorded for intracranial EEG are distinct from other EEG markers, have been clearly linked to epileptogenicity and may improve the predictability of the postsurgical outcome patients with epilepsy. Moreover most of the analysis can be done from 5 min of interictal intracranial EEG and even intraoperative ECOG recordings. Thus the time needed for an investigation may be reduced in comparison to classical chronic EEG analysis. First studies discuss high frequency findings in the surface EEG which may allow extending the method to patients with less severe epilepsy and long-term studies. This review provides an overview over the knowledge of pathological and physiological HFOs in the field of epilepsy as well as discusses possible future clinical applications and methodological challenges of HFOs as markers of epileptogenicity.

Schlüsselwörter

Epilepsie - Ripple - Fast ripple - Hochfrequenzoszillationen

Key words

epilepsy - ripple - fast ripple - high frequency oscillations

Literatur

• 1 Akiyama T, Otsubo H, Ochi A. et al . Focal cortical high-frequency oscillations trigger epileptic spasms: confirmation by digital video subdural EEG.  Clin Neurophysiol. 2005;  116 2819-2825
• 2 Axmacher N, Elger CE, Fell J. Ripples in the medial temporal lobe are relevant for human memory consolidation.  Brain. 2008;  131 1806-1817
• 3 Bagshaw AP, Jacobs J, LeVan P. et al . Effect of sleep stage on interictal high-frequency oscillations recorded from depth macroelectrodes in patients with focal epilepsy.  Epilepsia. 2009;  50 617-628
• 4 Blanco JA, Stead M, Krieger A. et al . Unsupervised classification of high-frequency oscillations in human neocortical epilepsy and control patients.  J Neurophysiol. 2010;  104 2900-2912
• 5 Bragin A, Engel Jr J, Wilson CL. et al . High-frequency oscillations in human brain.  Hippocampus. 1999b;  9 137-142
• 6 Bragin A, Engel Jr J, Wilson CL. et al . Hippocampal and entorhinal cortex high-frequency oscillations (100–500 Hz) in human epileptic brain and in kainic acid-treated rats with chronic seizures.  Epilepsia. 1999a;  40 127-137
• 7 Bragin A, Mody I, Wilson CL. et al . Local generation of fast ripples in epileptic brain.  J Neurosci. 2002;  22 2012-2021
• 8 Bragin A, Wilson CL, Almajano J. et al . High-frequency oscillations after status epilepticus: epileptogenesis and seizure genesis.  Epilepsia. 2004;  45 1017-1023
• 9 Chakraborty A, McEvoy AW. Presurgical functional mapping with functional MRI.  Curr Opin Neurol. 2008;  21 446-451
• 10 Chrobak JJ, Buzsaki G. High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat.  J Neurosci. 1996;  16 3056-3066
• 11 Cohen-Gadol AA, Wilhelmi BG, Collignon F. et al . Long-term outcome of epilepsy surgery among 399 patients with nonlesional seizure foci including mesial temporal lobe sclerosis.  J Neurosurg. 2006;  104 513-524
• 12 Cossu M, Lo RG, Francione S. et al . Epilepsy surgery in children: results and predictors of outcome on seizures.  Epilepsia. 2008;  49 65-72
• 13 Curio G. High frequency (600 Hz) bursts of spike-like activities generated in the human cerebral somatosensory system.  Electroencephalogr Clin Neurophysiol Suppl. 1999;  49 56-61
• 14 Diehl B, Luders HO. Temporal lobe epilepsy: when are invasive recordings needed?.  Epilepsia. 2000;  41 (S 03) S61-S74
• 15 Draguhn A, Traub RD, Bibbig A. et al . Ripple (approximately 200-Hz) oscillations in temporal structures.  J Clin Neurophysiol. 2000;  17 361-376
• 16 Engel Jr J, Bragin A, Staba R. et al . High-frequency oscillations: what is normal and what is not?.  Epilepsia. 2009;  50 598-604
• 17 Fisher RS, Webber WR, Lesser RP. et al . High-frequency EEG activity at the start of seizures.  J Clin Neurophysiol. 1992;  9 441-448
• 18 Gardner AB, Worrell GA, Marsh E. et al . Human and automated detection of high-frequency oscillations in clinical intracranial EEG recordings.  Clin Neurophysiol. 2007;  118 1134-1143
• 19 Gotman J. Relationships between interictal spiking and seizures: human and experimental evidence.  Can J Neurol Sci. 1991;  18 573-576
• 20 Hufnagel A, Dumpelmann M, Zentner J. et al . Clinical relevance of quantified intracranial interictal spike activity in presurgical evaluation of epilepsy.  Epilepsia. 2000;  41 467-478
• 21 Jacobs J, Kobayashi K, Gotman J. High-frequency changes during interictal spikes detected by time-frequency analysis.  Clin Neurophysiol. 2011;  122 32-42
• 22 Jacobs J, LeVan P, Chander R. et al . Interictal high-frequency oscillations (80–500 Hz) are an indicator of seizure onset areas independent of spikes in the human epileptic brain.  Epilepsia. 2008;  49 1893-1907
• 23 Jacobs J, LeVan P, Chatillon CE. et al . High frequency oscillations in intracranial EEGs mark epileptogenicity rather than lesion type.  Brain. 2009a;  132 1022-1037
• 24 Jacobs J, LeVan P, Dubeau F. et al . Generation of High Frequency oscillations (80–500 Hz) in different anatomical structures and their relation to the Seizure onset zone.  2009b;  120 e29-e30
• 25 Jacobs J, Zijlmans M, Zelmann R. et al . High-frequency electroencephalographic oscillations correlate with outcome of epilepsy surgery.  Ann Neurol. 2010;  67 209-220
• 26 Jirsch JD, Urrestarazu E, LeVan P. et al . High-frequency oscillations during human focal seizures.  Brain. 2006;  129 1593-1608
• 27 Jones-Gotman M. Neuropsychological techniques in the identification of epileptic foci.  Epilepsy Res Suppl. 1992;  5 87-94
• 28 Jones-Gotman M, Harnadek MC, Kubu CS. Neuropsychological assessment for temporal lobe epilepsy surgery.  Can J Neurol Sci. 2000;  27 (S 01) S39-S43
• 29 Kobayashi K, Agari T, Oka M. et al . Detection of seizure-associated high-frequency oscillations above 500 Hz.  Epilepsy Res. 2009a; 
• 30 Kobayashi K, Jacobs J, Gotman J. Detection of changes of high-frequency activity by statistical time-frequency analysis in epileptic spikes.  Clin Neurophysiol. 2009b;  120 1070-1077
• 31 Kobayashi K, Oka M, Akiyama T. et al . Very fast rhythmic activity on scalp EEG associated with epileptic spasms.  Epilepsia. 2004;  45 488-496
• 32 Kobayashi K, Watanabe Y, Inoue T. et al . Scalp-recorded high-frequency oscillations in childhood sleep-induced electrical status epilepticus.  Epilepsia. 2010; 
• 33 Le Van QM, Bragin A, Staba R. et al . Cell type-specific firing during ripple oscillations in the hippocampal formation of humans.  J Neurosci. 2008;  28 6104-6110
• 34 Ochi A, Otsubo H, Donner EJ. et al . Dynamic changes of ictal high-frequency oscillations in neocortical epilepsy: using multiple band frequency analysis.  Epilepsia. 2007;  48 286-296
• 35 Oostendorp TF, Delbeke J, Stegeman DF. The conductivity of the human skull: results of in vivo and in vitro measurements.  IEEE Trans Biomed Eng. 2000;  47 1487-1492
• 36 Ray A, Tao JX, Hawes-Ebersole SM. et al . Localizing value of scalp EEG spikes: a simultaneous scalp and intracranial study.  Clin Neurophysiol. 2007;  118 69-79
• 37 Roopun AK, Simonotto JD, Pierce ML. et al . A nonsynaptic mechanism underlying interictal discharges in human epileptic neocortex.  Proc Natl Acad Sci USA. 2010;  107 338-343
• 38 Rosenow F, Luders H. Presurgical evaluation of epilepsy.  Brain. 2001;  124 1683-1700
• 39 Spencer S, Huh L. Outcomes of epilepsy surgery in adults and children.  Lancet Neurol. 2008;  7 525-537
• 40 Spencer SS, Goncharova II, Duckrow RB. et al . Interictal spikes on intracranial recording: behavior, physiology, and implications.  Epilepsia. 2008;  49 1881-1892
• 41 Staba RJ, Frighetto L, Behnke EJ. et al . Increased fast ripple to ripple ratios correlate with reduced hippocampal volumes and neuron loss in temporal lobe epilepsy patients.  Epilepsia. 2007;  48 2130-2138
• 42 Staba RJ, Wilson CL, Bragin A. et al . Quantitative analysis of high-frequency oscillations (80–500 Hz) recorded in human epileptic hippocampus and entorhinal cortex.  J Neurophysiol. 2002;  88 1743-1752
• 43 Staba RJ, Wilson CL, Bragin A. et al . High-frequency oscillations recorded in human medial temporal lobe during sleep.  Ann Neurol. 2004;  56 108-115
• 44 Tao JX, Baldwin M, Hawes-Ebersole S. et al . Cortical substrates of scalp EEG epileptiform discharges.  J Clin Neurophysiol. 2007;  24 96-100
• 45 Tao JX, Ray A, Hawes-Ebersole S. et al . Intracranial EEG substrates of scalp EEG interictal spikes.  Epilepsia. 2005;  46 669-676
• 46 Urrestarazu E, Chander R, Dubeau F. et al . Interictal high-frequency oscillations (100–500 Hz) in the intracerebral EEG of epileptic patients.  Brain. 2007;  130 2354-2366
• 47 Usui N, Terada K, Baba K. et al . Very high frequency oscillations (over 1 000 Hz) in human epilepsy.  Clin Neurophysiol. 2010;  121 1825-1831
• 48 Widdess-Walsh P, Jeha L, Nair D. et al . Subdural electrode analysis in focal cortical dysplasia: predictors of surgical outcome.  Neurology. 2007;  69 660-667
• 49 Worrell GA, Gardner AB, Stead SM. et al . High-frequency oscillations in human temporal lobe: simultaneous microwire and clinical macroelectrode recordings.  Brain. 2008;  131 928-937
• 50 Wu JY, Koh S, Sankar R. et al . Paroxysmal fast activity: an interictal scalp EEG marker of epileptogenesis in children.  Epilepsy Res. 2008;  82 99-106
• 51 Wu JY, Sankar R, Lerner JT. et al . Removing interictal fast ripples on electrocorticography linked with seizure freedom in children.  Neurology. 2010;  75 1686-1694
• 52 Yamazaki M, Chan D, Tovar-Spinoza Z. et al . Interictal epileptogenic fast oscillations on neonatal and infantile EEGs in hemimegalencephaly.  Epilepsy Res. 2009;  83 198-206
• 53 Zelmann R, Zijlmans M, Jacobs J. et al . Improving the identification of High Frequency Oscillations.  Clin Neurophysiol. 2009;  120 1457-1464
• 54 Zijlmans M, Jacobs J, Kahn YU. et al . Ictal and interictal high frequency oscillations in patients with focal epilepsy.  Clin Neurophysiol. 2010; 
• 55 Zijlmans M, Jacobs J, Zelmann R. et al . High-frequency oscillations mirror disease activity in patients with epilepsy.  Neurology. 2009;  72 979-986

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