- Email: [email protected]
Migrainous aura during carotid artery clamping: An ictal EEG study
650
Letters to the Editor / Clinical Neurophysiology 125 (2014) 647–651
Segawa M. Hereditary progressive dystonia with marked diurnal fluctuation. Brain Dev 2011;33:195–201. Segawa M, Hoshino K, Hachimori K, Nomura Y. A single gene for dystonia involves both or either of the two striatal pathways. In: Nicholson LFB, Faull RLM, editors. The basal ganglia VII, advances in behavioral biology 2002;vol. 52. New York: Kluwer Academic/Plenum Publishers; 2002. p. 155–63. Shaikh AG, Xu-Wilson M, Grill S, Zee DS. ’Staircase’ square-wave jerks in early Parkinson’s disease. Br J Ophthalmol 2011;95:705–9. Terao Y, Fukuda H, Ugawa Y, Hikosaka O. New perspectives on the pathophysiology of Parkinson’s disease as assessed by saccade performance: a clinical review. Clin Neurophysiol 2013;124:1491–506. Terao Y, Fukuda H, Yugeta A, Hikosaka O, Nomura Y, Segawa M, et al. Initiation and inhibitory control of saccades with the progression of Parkinson’s disease – changes in three major drives converging on the superior colliculus. Neuropsychologia 2011a;49:1794–806. Terao Y, Fukuda H, Yugeta A, Hanajima R, Ugawa Y, Nomura Y, et al., Saccade abnormalities in hereditary progressive dystonia. In: The 15th international congress of Parkinson’s disease and movement disorders, Toronto, Canada, 2011b [abstract]. Trender-Gerhard I, Sweeney MG, Schwingenschuh P, Mir P, Edwards MJ, Gerhard A, et al. Autosomal-dominant GTPCH1-deficient DRD: clinical characteristics and long-term outcome of 34 patients. J Neurol Neurosurg Psychiatry 2009;80:839–45. Yaltho TC, Jankovic J, Lotze T. The association of Tourette syndrome and Doparesponsive dystonia. Mov Disord 2011;26:359–60.
Yasuo Terao Graduate School of Medicine, University of Tokyo, Department of Neurology, 7-3-1 Hongo, Bunkyo-ku, Tokyo, Japan Tel.: +81 3 3815 5411; fax: +81 3 5800 6548. E-mail address: [email protected] Available online 19 August 2013 1388-2457/$36.00 Ó 2013 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. doi:http://dx.doi.org/10.1016/j.clinph.2013.07.010
Migrainous aura during carotid artery clamping: An ictal EEG study
Migraine is a disorder in which central nervous system dysfunction play a pivotal role. As there are no consistent structural disturbances, clinical neurophysiology methods seem particularly suited to studying its pathophysiology. The noninvasive detection of a brief focal depolarization wave in the human brain is difficult. We report a migrainous patient who described a visual migrainous aura, likely provoked by carotid artery clamping, during which EEG monitoring was carried out. A 53-year-old woman, with a previous history of migraine with aura with migrainous headache, was hospitalized for the exploration of a left clivus chordoma. She had since the age of 30, episodes of scintillating scotoma during 20 min, followed by headache with migraine characteristics. She also complained from episodes of typical aura without headache. Her daughter also has a history of migraine without aura. Before surgery, bilateral temporary internal carotid artery (ICA) clamping was carried out. Clinical testing and EEG monitoring were performed during ICA clamping. EEG was recorded using the DeltamedÓ system with 12-channel EEG amplifier. EEG signals were amplified with an online digital band-pass filter (0.5–200 Hz) and digitized at a rate of 512 kHz per channel. In order to observe EEG modification during right or left ICA clamp and during scotoma, beta, alpha, theta and delta normalized band power were quantified during a ten second time window every 5 min on the Cz–Pz bipolar lead. In addition, we used wavelet-based time–frequency analysis to describe EEG modification. Right carotid occlusion in the migrainous patient led to no clinical or neurophysiological modifications. However 20 min (T20) after left carotid occlusion, the patient described a typical migrainous visual aura, corresponding to a scintillating scotoma. She had
previously experienced such migrainous aura, and she identified the visual symptoms as totally similar with the previous migraine with aura attacks. This phenomenon occurred in isolation without headache, nausea, phonophobia and photophobia, and disappeared immediately after clamping was released. This visual aura had the International Headache Society criteria for typical aura without headache. Gradual development, duration no longer than 1 h, reproductability of symptoms, and complete reversibility characterize this aura without headache, and are arguments against a transient ischaemic attack. In fact, ICA clamping was stopped at 27 min inducing complete regression of the visual scotoma. During this episode, there was no altered state of consciousness. Scalp EEG showed widespread bilateral slow wave activity in the delta band around 2 Hz occurring before and during the visual symptoms (Fig. 1). Before clamping several recordings in rest condition show variation in band power without increase of slow activity (delta power). During right ICA clamping, no significant modification was observed in beta, alpha, theta or delta normalized band power. In contrast, 5 min before the occurrence of scotoma (T15) we recorded an increase of delta power (50%, p < 0.05) concomitant to decrease of alpha and beta power (15%, p < 0.05). This modification persisted during the occurrence of scotoma (T25 scotoma, 57%, p < 0.01) until the end of left ICA clamping. At T30, in the resting condition, the delta band power had returned to base level (24%). There was no clearly defined spatial organization of the EEG change, which was bilateral and without clear antero-posterior difference. Cortical spreading depression (CSD) is believed to be the pathophysiological phenomenon underlying migraine aura. CSD is a propagating wave of neuronal and glial depolarization and has been implicated in disorders of neurovascular regulation such as ischemic stroke, head trauma and migraine (Lauritzen et al., 2011). The depolarization is self-propagating and is associated with depressed neuronal bioelectrical activity and transient nearcomplete loss of membrane ion gradients, with massive surges of extracellular potassium and neurotransmitters as well as intracellular calcium. In human, the registration of CSD has been realized using electrocorticography (Lauritzen et al., 2011). This case report is of interest for 2 reasons: the first is the neurophysiological demonstration that cortical spreading depression can be evidenced prior to onset of clinical symptoms. We observed a decrease of physiological alpha-band activity. In addition, we recorded an increase of slow wave delta-band signals. We could hypothesize that the co-occurrence of decrease alpha-band activity and increase of delta-band activity is the electrophysiological phenomenon described by Drenckhahn et al. (2012) during spreading depolarization with the simultaneous occurrence of a slow potential change and depression of spontaneous activity. However, non-invasive recording of CSD by conventional surface EEG technique is difficult due to the brief duration of the depolarization wave (Lauritzen et al., 2011). Recently, Drenckhahn et al. (2012) demonstrated that in contrast to electrocorticography, no spread of electroencephalographic slow potential changes was seen, presumably due to superposition of volume-conducted electroencephalographic signals from widespread cortical generators. This is explained by the high impedance of dura and skull and the very limited surface area of cortex, only a few square centimeters, that undergoes local electrical EEG silence (Lauritzen et al., 2011). The second interest is the clinical validation of Nozari’s hypothesis (Nozari et al., 2010) that cortical spreading depression appears to be related to the magnitude and duration of flow reduction. The link between spreading depression and an interruption of the circulation was previously described by Leão (1947). He described the slow voltage shift that accompanies SD as well as sudden total ischemia of the brain: ‘‘The areas involved in a spreading depression exhibit a distinctive susceptibility to sudden interruption of
Letters to the Editor / Clinical Neurophysiology 125 (2014) 647–651
651
Fig. 1. EEG recording before ICA clamp (1), during scotoma (2) and after ICA clamp (3). (A) (1) Before ICA clamp, alpha-band EEG activity was recorded. (2) EEG change activity was observed during the scotoma with slow wave activity (Delta Band) superimposed on the base alpha activity. (3) Slow wave decreased after ICA clamp. (B) Wavelet-based time frequency analysis on Cz–Pz derivation before ICA clamp (1), during scotoma (2) and after ICA clamps (3). Note the slow wave activity during the scotoma (2) marked by dashed line.
the circulation. This susceptibility appears only after a certain time’’ (Leão, 1947). In our case report, the first carotid occlusion led to no clinical symptoms. Migrainous aura appeared 20 min after left carotid occlusion and disappeared immediately after the interruption of ICA clamping. Leão has previously described long latency between the onset of left ICA clamping and the onset of reported symptoms (Leão, 1947). If our case reinforces the hypothesis that hypoxic episodes can induce migraine with aura attacks, the precise chain of events remains problematic. As visual aura may develop when the slow depolarization waves expand through the occipital area, these three case reports are particular, because CSD is induced by carotid ischemia. Dreier has demonstrated that endothelial irritation may provoke CSD, and that endothelin-1 may be a trigger for migrainous aura (Dreier, 2011). As suggested by Dreier, from the tissue initially exposed to the hypoxia in the parieto-occipital junction, spreading depolarization can invade naïve tissue in the occipital area (Dreier, 2011). Our findings confirm the notion that in migrainous subjects, a transient hypoxic ischemic event may serve as a trigger for CSD. References Dreier JP. The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat Med 2011;17:439–47. Drenckhahn C, Winkler MK, Major S, Scheel M, Kang EJ, Pinczolits A, et al. Correlates of spreading depolarization in human scalp electroencephalography. Brain 2012;135:853–68. Lauritzen M, Dreier JP, Fabricius M, Hartings JA, Graf R, Strong AJ. Clinical relevance of cortical spreading depression in neurological disorders: migraine, malignant
stroke, subarachnoid and intracranial hemorrhage, and traumatic brain injury. J Cerebral Blood Flow Metab 2011;31:17–35. Leão AAP. Further observations on the spreading depression of activity in the cerebral cortex. J Neurophysiol 1947;10:409–14. Nozari A, Dilekoz E, Sukhotinsky I, Stein T, Eikermann-Haerter K, Liu C, et al. Microemboli may link spreading depression, migraine aura, and patent foramen ovale. Ann Neurol 2010;67:221–9.
Anne Donnet Neurological Department, Timone Hospital, Rue St Pierre, 13005 Marseille, France Tel.: +33 4 91 38 43 45; fax: +33 4 91 38 80 48. E-mail address: [email protected] Xavier Combaz Neuroradiological Department, Timone Hospital, Rue St Pierre, 13005 Marseille, France Henry Dufour Neurosurgical Department, Timone Hospital, Rue St Pierre, 13005 Marseille, France Agnès Trebuchon Neurophysiological Department, Timone Hospital, Rue St Pierre, 13005 Marseille, France Available online 5 October 2013 1388-2457/$36.00 Ó 2013 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. doi:http://dx.doi.org/10.1016/j.clinph.2013.07.019
Letters to the Editor / Clinical Neurophysiology 125 (2014) 647–651
Segawa M. Hereditary progressive dystonia with marked diurnal fluctuation. Brain Dev 2011;33:195–201. Segawa M, Hoshino K, Hachimori K, Nomura Y. A single gene for dystonia involves both or either of the two striatal pathways. In: Nicholson LFB, Faull RLM, editors. The basal ganglia VII, advances in behavioral biology 2002;vol. 52. New York: Kluwer Academic/Plenum Publishers; 2002. p. 155–63. Shaikh AG, Xu-Wilson M, Grill S, Zee DS. ’Staircase’ square-wave jerks in early Parkinson’s disease. Br J Ophthalmol 2011;95:705–9. Terao Y, Fukuda H, Ugawa Y, Hikosaka O. New perspectives on the pathophysiology of Parkinson’s disease as assessed by saccade performance: a clinical review. Clin Neurophysiol 2013;124:1491–506. Terao Y, Fukuda H, Yugeta A, Hikosaka O, Nomura Y, Segawa M, et al. Initiation and inhibitory control of saccades with the progression of Parkinson’s disease – changes in three major drives converging on the superior colliculus. Neuropsychologia 2011a;49:1794–806. Terao Y, Fukuda H, Yugeta A, Hanajima R, Ugawa Y, Nomura Y, et al., Saccade abnormalities in hereditary progressive dystonia. In: The 15th international congress of Parkinson’s disease and movement disorders, Toronto, Canada, 2011b [abstract]. Trender-Gerhard I, Sweeney MG, Schwingenschuh P, Mir P, Edwards MJ, Gerhard A, et al. Autosomal-dominant GTPCH1-deficient DRD: clinical characteristics and long-term outcome of 34 patients. J Neurol Neurosurg Psychiatry 2009;80:839–45. Yaltho TC, Jankovic J, Lotze T. The association of Tourette syndrome and Doparesponsive dystonia. Mov Disord 2011;26:359–60.
Yasuo Terao Graduate School of Medicine, University of Tokyo, Department of Neurology, 7-3-1 Hongo, Bunkyo-ku, Tokyo, Japan Tel.: +81 3 3815 5411; fax: +81 3 5800 6548. E-mail address: [email protected] Available online 19 August 2013 1388-2457/$36.00 Ó 2013 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. doi:http://dx.doi.org/10.1016/j.clinph.2013.07.010
Migrainous aura during carotid artery clamping: An ictal EEG study
Migraine is a disorder in which central nervous system dysfunction play a pivotal role. As there are no consistent structural disturbances, clinical neurophysiology methods seem particularly suited to studying its pathophysiology. The noninvasive detection of a brief focal depolarization wave in the human brain is difficult. We report a migrainous patient who described a visual migrainous aura, likely provoked by carotid artery clamping, during which EEG monitoring was carried out. A 53-year-old woman, with a previous history of migraine with aura with migrainous headache, was hospitalized for the exploration of a left clivus chordoma. She had since the age of 30, episodes of scintillating scotoma during 20 min, followed by headache with migraine characteristics. She also complained from episodes of typical aura without headache. Her daughter also has a history of migraine without aura. Before surgery, bilateral temporary internal carotid artery (ICA) clamping was carried out. Clinical testing and EEG monitoring were performed during ICA clamping. EEG was recorded using the DeltamedÓ system with 12-channel EEG amplifier. EEG signals were amplified with an online digital band-pass filter (0.5–200 Hz) and digitized at a rate of 512 kHz per channel. In order to observe EEG modification during right or left ICA clamp and during scotoma, beta, alpha, theta and delta normalized band power were quantified during a ten second time window every 5 min on the Cz–Pz bipolar lead. In addition, we used wavelet-based time–frequency analysis to describe EEG modification. Right carotid occlusion in the migrainous patient led to no clinical or neurophysiological modifications. However 20 min (T20) after left carotid occlusion, the patient described a typical migrainous visual aura, corresponding to a scintillating scotoma. She had
previously experienced such migrainous aura, and she identified the visual symptoms as totally similar with the previous migraine with aura attacks. This phenomenon occurred in isolation without headache, nausea, phonophobia and photophobia, and disappeared immediately after clamping was released. This visual aura had the International Headache Society criteria for typical aura without headache. Gradual development, duration no longer than 1 h, reproductability of symptoms, and complete reversibility characterize this aura without headache, and are arguments against a transient ischaemic attack. In fact, ICA clamping was stopped at 27 min inducing complete regression of the visual scotoma. During this episode, there was no altered state of consciousness. Scalp EEG showed widespread bilateral slow wave activity in the delta band around 2 Hz occurring before and during the visual symptoms (Fig. 1). Before clamping several recordings in rest condition show variation in band power without increase of slow activity (delta power). During right ICA clamping, no significant modification was observed in beta, alpha, theta or delta normalized band power. In contrast, 5 min before the occurrence of scotoma (T15) we recorded an increase of delta power (50%, p < 0.05) concomitant to decrease of alpha and beta power (15%, p < 0.05). This modification persisted during the occurrence of scotoma (T25 scotoma, 57%, p < 0.01) until the end of left ICA clamping. At T30, in the resting condition, the delta band power had returned to base level (24%). There was no clearly defined spatial organization of the EEG change, which was bilateral and without clear antero-posterior difference. Cortical spreading depression (CSD) is believed to be the pathophysiological phenomenon underlying migraine aura. CSD is a propagating wave of neuronal and glial depolarization and has been implicated in disorders of neurovascular regulation such as ischemic stroke, head trauma and migraine (Lauritzen et al., 2011). The depolarization is self-propagating and is associated with depressed neuronal bioelectrical activity and transient nearcomplete loss of membrane ion gradients, with massive surges of extracellular potassium and neurotransmitters as well as intracellular calcium. In human, the registration of CSD has been realized using electrocorticography (Lauritzen et al., 2011). This case report is of interest for 2 reasons: the first is the neurophysiological demonstration that cortical spreading depression can be evidenced prior to onset of clinical symptoms. We observed a decrease of physiological alpha-band activity. In addition, we recorded an increase of slow wave delta-band signals. We could hypothesize that the co-occurrence of decrease alpha-band activity and increase of delta-band activity is the electrophysiological phenomenon described by Drenckhahn et al. (2012) during spreading depolarization with the simultaneous occurrence of a slow potential change and depression of spontaneous activity. However, non-invasive recording of CSD by conventional surface EEG technique is difficult due to the brief duration of the depolarization wave (Lauritzen et al., 2011). Recently, Drenckhahn et al. (2012) demonstrated that in contrast to electrocorticography, no spread of electroencephalographic slow potential changes was seen, presumably due to superposition of volume-conducted electroencephalographic signals from widespread cortical generators. This is explained by the high impedance of dura and skull and the very limited surface area of cortex, only a few square centimeters, that undergoes local electrical EEG silence (Lauritzen et al., 2011). The second interest is the clinical validation of Nozari’s hypothesis (Nozari et al., 2010) that cortical spreading depression appears to be related to the magnitude and duration of flow reduction. The link between spreading depression and an interruption of the circulation was previously described by Leão (1947). He described the slow voltage shift that accompanies SD as well as sudden total ischemia of the brain: ‘‘The areas involved in a spreading depression exhibit a distinctive susceptibility to sudden interruption of
Letters to the Editor / Clinical Neurophysiology 125 (2014) 647–651
651
Fig. 1. EEG recording before ICA clamp (1), during scotoma (2) and after ICA clamp (3). (A) (1) Before ICA clamp, alpha-band EEG activity was recorded. (2) EEG change activity was observed during the scotoma with slow wave activity (Delta Band) superimposed on the base alpha activity. (3) Slow wave decreased after ICA clamp. (B) Wavelet-based time frequency analysis on Cz–Pz derivation before ICA clamp (1), during scotoma (2) and after ICA clamps (3). Note the slow wave activity during the scotoma (2) marked by dashed line.
the circulation. This susceptibility appears only after a certain time’’ (Leão, 1947). In our case report, the first carotid occlusion led to no clinical symptoms. Migrainous aura appeared 20 min after left carotid occlusion and disappeared immediately after the interruption of ICA clamping. Leão has previously described long latency between the onset of left ICA clamping and the onset of reported symptoms (Leão, 1947). If our case reinforces the hypothesis that hypoxic episodes can induce migraine with aura attacks, the precise chain of events remains problematic. As visual aura may develop when the slow depolarization waves expand through the occipital area, these three case reports are particular, because CSD is induced by carotid ischemia. Dreier has demonstrated that endothelial irritation may provoke CSD, and that endothelin-1 may be a trigger for migrainous aura (Dreier, 2011). As suggested by Dreier, from the tissue initially exposed to the hypoxia in the parieto-occipital junction, spreading depolarization can invade naïve tissue in the occipital area (Dreier, 2011). Our findings confirm the notion that in migrainous subjects, a transient hypoxic ischemic event may serve as a trigger for CSD. References Dreier JP. The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat Med 2011;17:439–47. Drenckhahn C, Winkler MK, Major S, Scheel M, Kang EJ, Pinczolits A, et al. Correlates of spreading depolarization in human scalp electroencephalography. Brain 2012;135:853–68. Lauritzen M, Dreier JP, Fabricius M, Hartings JA, Graf R, Strong AJ. Clinical relevance of cortical spreading depression in neurological disorders: migraine, malignant
stroke, subarachnoid and intracranial hemorrhage, and traumatic brain injury. J Cerebral Blood Flow Metab 2011;31:17–35. Leão AAP. Further observations on the spreading depression of activity in the cerebral cortex. J Neurophysiol 1947;10:409–14. Nozari A, Dilekoz E, Sukhotinsky I, Stein T, Eikermann-Haerter K, Liu C, et al. Microemboli may link spreading depression, migraine aura, and patent foramen ovale. Ann Neurol 2010;67:221–9.
Anne Donnet Neurological Department, Timone Hospital, Rue St Pierre, 13005 Marseille, France Tel.: +33 4 91 38 43 45; fax: +33 4 91 38 80 48. E-mail address: [email protected] Xavier Combaz Neuroradiological Department, Timone Hospital, Rue St Pierre, 13005 Marseille, France Henry Dufour Neurosurgical Department, Timone Hospital, Rue St Pierre, 13005 Marseille, France Agnès Trebuchon Neurophysiological Department, Timone Hospital, Rue St Pierre, 13005 Marseille, France Available online 5 October 2013 1388-2457/$36.00 Ó 2013 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. doi:http://dx.doi.org/10.1016/j.clinph.2013.07.019