Ictal unilateral hyperkinetic proximal lower limb movements: an independent lateralising sign suggesting ipsilateral seizure onset
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1 Original article Epileptic Disord 2013; 15 (2): Ictal unilateral hyperkinetic proximal lower limb : an independent lateralising sign suggesting ipsilateral seizure onset Rute Teotónio 1,2, Roman Rodionov 1, Andrew W McEvoy 1,3, John Duncan 1, Beate Diehl 1, Tim Wehner 1 1 Department of Clinical and Experimental Epilepsy, University College London/ The National Hospital for Neurology and Neurosurgery, London 2 Neurology Department, Hospitais da Universidade de Coimbra, Coimbra, Portugal 3 Neurosurgery Department, The National Hospital for Neurology and Neurosurgery, London, UK Received November 20, 2012; Accepted February 17, 2013 ABSTRACT Our aim was to determine the lateralising value of ictal repetitive unilateral hyperkinetic proximal lower limb. Among 16 patients with ictal hyperkinetic features who underwent intracranial EEG between 2008 and 2011 in our centre, three had repetitive unilateral hyperkinetic proximal lower limb, sometimes associated with hemiballic-like of the ipsilateral upper limb. There were no other consistent lateralising signs. In all patients, these were ipsilateral to the ictal onset zone and started a few seconds after electroencephalographic seizure onset. In two patients, intracranial EEG showed seizure onset within the parietal lobe and mesial temporal ictal onset was recorded in a third. Two patients underwent resection and became seizure-free. Our results suggest that unilateral ictal repetitive hyperkinetic proximal lower limb may be an independent lateralising sign to the ipsilateral hemisphere. Key words: semiology, hyperkinetic ictal, intracranial EEG, lateralising ictal symptoms Correspondence: Rute Teotónio Hospitais da Universidade de Coimbra, Serviço de Neurologia, Praçeta Mota Pinto, Coimbra, Portugal <rute.teotonio@gmail.com> Ictal hyperkinetic behaviour is mainly characterised by complex involving the trunk and proximal limb segments. These are, by definition, of high speed and large amplitude, which frequently give them a violent appearance (Bianchin and Sakamoto, 2008). They are widely recognised as common features of seizures in frontal lobe epilepsy (Kellinghaus and Lüders, 2004). More recently, insula, parietal, and temporal lobes have been recognised as less frequent alternative sites of origin (Ryvlin et al., 2006; Wang et al., 2008; Nishibayashi et al., 2009; Vaugier et al., 2009). There is, doi: /epd Epileptic Disord, Vol. 15, No. 2, June 2013
2 Unilateral hyperkinetic lower limb however, no consensus on the specific localisation of the symptomatogenic zone responsible for hyperkinetic ictal behaviour. Non-manipulative proximal upper limb automatisms have been linked to the contralateral hemisphere in temporal lobe epilepsy (Kelemen et al., 2010). On the other hand, hemiballic-like (Fluchère et al., 2012) and hyperkinetic automatisms (Barba et al., 2005) of the upper limbs appear to be associated with onset in the ipsilateral hemisphere. To the best of our knowledge, there are no reported studies regarding the lateralising value of hyperkinetic lower limb. In this context, we investigated the lateralising and localising features of repetitive unilateral hyperkinetic proximal lower limb. Patients and methods We retrospectively reviewed all patients (n=80) who had undergone intracranial Video-EEG evaluation between 2008 and 2011 at The National Hospital for Neurology and Neurosurgery, London, UK, and identified 16 patients whose seizures included hyperkinetic features. We analyzed seizures for the presence of repetitive unilateral hyperkinetic proximal lower limb (combination of flexion-extension, rotation, and/or abduction-adduction in the hip) that lasted at least three seconds. We also reviewed ictal EEG onset and association with other possible lateralising signs. Case studies Three of 16 (18.7%) patients with ictal hyperkinetic features presented with repetitive unilateral proximal lower limb that met the inclusion criterion. These occurred in 16 seizures. The clinical and electrophysiological features of these three patients are summarised in table 1. In all three patients, these repetitive unilateral proximal lower limb were observed ipsilateral to the ictal onset zone. In Patient 1, concomitant hemiballic-like of the ipsilateral upper limb occurred in two of 13 seizures. Bilateral upper extremity tonic posturing, more prominent contralateral to the ictal onset, was present in Patient 1, in all 13 seizures evaluated. No simultaneous dystonic posturing was observed in the other two patients. No other concomitant lateralising sign was recorded during or after the seizures. Repetitive unilateral proximal lower limb always started a few seconds after electroencephalographic seizure onset (median: 3.5±3; interquartile range [IQR]), just after the clinical onset. In Patient 1, the rapidly followed and accompanied bilateral upper extremity tonic posturing. In Patient 2, these hyperkinetic were also present at clinical onset, just after an arousal. In Patient 3, they followed brief bilateral hand tapping. Clinical features of Patients 1 and 2 are presented in figure 1. In Patients 1 and 2, the ictal onset was recorded from the parietal lobe and/or supplementary motor area (SMA) (figure 2). The ipsilateral SMA or the immediate vicinity was involved at the time of repetitive unilateral hyperkinetic lower limb in Patient 1 (figure 1a), while ipsilateral parietal operculum involvement was observed in Patient 2 at the time of these (figure 2a). Electrocortical stimulation of the electrode contacts involved at the time of repetitive lower limb in Patient 1 produced a cramp-like feeling in the right leg, compatible with a tonic contraction that may reflect activation of the SMA. Patient 1 chose not to undergo a resection due to close proximity of the ictal onset zone to eloquent cortex. Patient 2 has been seizure-free for one year following right parietal focal cortical dysplasia. In Patient 3, the ictal onset was recorded from the left mesial temporal lobe. The seizure frequency decreased after a left anterior temporal resection which revealed hippocampal sclerosis, and she has been seizure-free for six months after treatment with zonisamide. Discussion Our results suggest that repetitive ictal unilateral hyperkinetic proximal lower limb may be a lateralising sign to the ipsilateral hemisphere. Of note, these were observed within a few seconds after the EEG and clinical seizure onset, and were rarely associated with other lateralising signs. Thus, the appear to be a useful independent clue for ictal onset lateralisation. However, they appear to be a relatively infrequent feature of ictal hyperkinetic behaviour. The lateralising value of hyperkinetic upper limb has been evaluated previously and the results, summarised in table 2, are not concordant between authors. Non-manipulative proximal upper extremity automatisms were found to reliably lateralise the seizure onset to the contralateral side in 11 patients with temporal lobe epilepsy (Kelemen et al., 2010). These were described as repetitive, rhythmic of the upper limbs, often with a circulatory component resembling waving, circling or stirring. In contrast, hyperkinetic automatisms, further characterised as stereotyped repetitive arm, such as tapping towards the thorax (Barba et al., 2005) and hemiballic-like, described as stereotyped repetitive ictal rotational proximal upper limb Epileptic Disord, Vol. 15, No. 2, June
3 R. Teotónio, et al. Table 1. Clinical and electrophysiological features of the three patients with repetitive unilateral proximal hyperkinetic lower limb. Patient 1 Patient 2 Patient 3 Gender Male Female Female Age (years) Age at seizure onset (years) Seizure frequency Daily Daily Weekly MRI Normal Left inferior parietal cortical dysplasia Scalp EEG No ictal EEG changes Left parietal and posterior temporal onset Left temporal atrophy Left temporal onset PET No focal hypometabolism Not done Left temporal hypometabolism Description of lower limb Flexion and extension (11) or abduction and adduction in the right hip (2) Rotational of the left hip with knee extension Flexion and extension in the left hip Associated signs Bilateral upper extremity tonic posturing, more prominent on the left (13/13); hemiballic-like of the right upper extremity (2/13) - - Seizures with repetitive unilateral proximal hyperkinetic lower limb / Total Seizures 13/26 2/10 1/3 Intracranial EEG Parietal lobe and SMA onset Parietal lobe onset Left mesial temporal lobe onset Delay (sec) of appearance of unilateral lower limb movement relative to EEG onset Median 3±2 (IQR) Mean Surgery Not done due to close proximity of the ictal onset zone to eloquent cortex Resection of the left inferior parietal lobule Left temporal lobectomy Histopathology - Focal cortical dysplasia type IIb Hippocampal sclerosis Ultimate outcome (Engel classification) - IA (1 year) IA (6 months) (Fluchère et al., 2012), indicated ipsilateral ictal onset. Of note, contralateral dystonic/tonic posturing was observed in association with the ipsilateral hyperkinetic upper limb in two of these studies (Kelemen et al., 2010; Fluchère et al., 2012). Our patients also presented with repetitive unilateral limb. These lower limb were of large amplitude and were formed by flexionextension, abduction-adduction or rotational/circular in the hip, resembling, to some extent, 144 Epileptic Disord, Vol. 15, No. 2, June 2013
4 Unilateral hyperkinetic lower limb t=0ms t=714ms t=1714ms P1(a) t=0ms t=574ms t=0ms t=1143ms t=1285ms P1(b) P2 t=1714ms Figure 1. Consecutive periods of three different seizures from two patients (Patients 1 and 2). (a) In Patient 1, the flexion and extension of the right thigh associated with bilateral upper extremity posturing is evident. (b) In Patient 1, repetitive abduction and adduction is demonstrated. In Patient 2, there was a rotation of the left hip with knee extension. t: time of progression of one representative unilateral lower limb hypermotor movement (milliseconds). hemiballic-like (Fluchère et al., 2012). This resemblance, together with the fact that hemiballiclike of the right upper extremity were seen in association with ipsilateral hyperkinetic proximal lower limb in two seizures of Patient 1, suggests a similar generator for upper and lower limb proximal ballic. Compared to ictal motor manifestations in the upper limbs, lower limb during seizures have attracted less interest in the literature. This may be explained by the fact that the legs are often covered or not included in video recordings of seizures. Nonetheless, meaningful lower limb appear to be less frequent than upper limb in temporal lobe epilepsy (Chou et al., 2004). Upper limb were observed in 79% of seizures. In contrast, lower limb automatisms were present in only 11%, most often (86%) ipsilateral to the side of ictal origin. Automatisms of the lower extremities were defined by these authors as repetitive stamping, kicking, pedalling Epileptic Disord, Vol. 15, No. 2, June 2013 or of disorderly behaviour. In line with these findings, we found repetitive lower limb in 18.7% of patients with hyperkinetic features and in 3.8% of patients who had undergone intracranial EEG recordings. In three patients with hemiballic-like upper limb, the epileptogenic zone was located in posterior cortex, including the inferior parietal region (Fluchère et al., 2012). Interestingly, in two of our three patients, the ictal onset zone was also found in the parietal lobe. This observation suggests that posterior brain regions might be responsible for producing hyperkinetic limb, either by direct activation or ictal propagation, anteriorly to the SMA. In both reports of Fluchère et al. (2012) and Barba et al. (2005), there is some evidence that supports the SMA as a possible symptomatogenic zone. The SMA was involved at the onset of hyperkinetic limb in three of their six patients. We speculate that the parietal operculum may be another potential symptomatogenic zone, as 145
5 R. Teotónio, et al. A P1 B P2 Figure 2. Left: distribution of electrode contacts at ictal onset and beginning of hyperkinetic lower limb. Right: ictal EEG with selected contacts and referential montages (reference electrodes marked as xx). (a) Upper panel: Patient 1; (b) lower panel: Patient 2. Table 2. Summary of studies addressing ictal hyperkinetic upper limb. Kelemen et al., 2010 Barba et al., 2005 Fluchère et al., 2012 Term used by the author Non-manipulative proximal upper extremity automatisms Hyperkinetic automatisms Hemiballic-like Description of upper limb Repetitive, rhythmic of the upper limbs, often with a circulatory component resembling waving, circling or stirring Stereotyped repetitive arm, such as tapping towards the thorax Stereotyped repetitive ictal rotational proximal upper limb Suggested lateralising value Contralateral side in temporal lobe epilepsy Ipsilateral ictal onset Ipsilateral ictal onset Associated ictal manifestations Contralateral dystonic/tonic posturing was observed in association with the ipsilateral hyperkinetic upper limb None Contralateral dystonic/tonic posturing was observed in association with the ipsilateral hyperkinetic upper limb 146 Epileptic Disord, Vol. 15, No. 2, June 2013
6 Unilateral hyperkinetic lower limb three of four patients had parietal operculum involvement when hemiballic-like first occurred (Fluchère et al., 2012). We observed the involvement of the SMA or the immediate vicinity at the beginning of the unilateral repetitive lower limb in Patient 1, and parietal operculum involvement at the onset of the hyperkinetic lower limb in Patient 2. We suggest, therefore, that these two regions may eventually play an important role in the generation of repetitive hyperkinetic lower limb. Alternatively, automatisms may reflect loss of cortical control over movement programs ( release phenomenon ), rather than the activation of a specific symptomatogenic zone. Limitations of our study are the small number of patients and the inherent sampling bias in intracranial EEG. Further research into the localising or lateralising value of lower limb motor manifestations is needed. Disclosures. None of the authors has any conflict of interests to disclose. References Barba C, Doglietto F, Policicchio D, Caulo M, Colicchio G. Unusual ipsilateral hyperkinetic automatisms in SMA seizures. Seizure 2005; 14: Bianchin MM, Sakamoto AC. Complex motor seizures: localizing and lateralizing value. In: Lüders HO. Textbook of Epilepsy Surgery. 1st Ed. London: Informa, 2008: Chou CW, Yu HY, Shih YH, et al. Lateralisation value of lower limb behaviors in complex partial seizures of temporal lobe origin: a video-eeg analysis. Seizure 2004; 13: Fluchère F, McGonigal A, Villeneuve N, Chauvel P, Bartolomei F P. Ictal hemiballic-like movement: lateralizing and localizing value. Epilepsia 2012; 53: e41-5. Kelemen A, Fogarasi A, Borbély C, et al. Nonmanipulative proximal upper extremity automatisms lateralize contralaterally in temporal lobe epilepsy. Epilepsia 2010; 51: Kellinghaus C, Lüders HO. Frontal lobe epilepsy. Epileptic Disord 2004; 6: Nishibayashi H, Ogura M, Taguchi M, Miki J, Uematsu Y, Itakura T. Nondominant parietotemporal cortical dysplasia manifesting as hypermotor seizures. Epilepsy Behav 2009; 14: Ryvlin P, Minotti L, Demarquay G, et al. Nocturnal hypermotor seizures, suggesting frontal lobe epilepsy, can originate in the insula. Epilepsia 2006; 47: Vaugier L, Aubert S, McGonigal A, et al. Neural networks underlying hyperkinetic seizures of temporal lobe origin. Epilepsy Res 2009; 86: Wang L, Mathews GC, Whetsell WO, Abou-Khalil B. Hypermotor seizures in patients with temporal pole lesions. Epilepsy Res 2008; 82: Epileptic Disord, Vol. 15, No. 2, June
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