Are Proprioceptive-Induced Reflex Seizures Epileptically-Enhanced
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Original article with video sequences Epileptic Disord 2012; 14 (2): 149-54 Are proprioceptive-induced reflex seizures epileptically-enhanced stretch reflex manifestations? Anna Szucs˝ 1, György Rásonyi 1, Péter Orbay 1, András Sólyom 1, András Holló 2, Zsuzsanna Arányi 3, József Janszky 4, Lóránd Eross˝ 1, Anita Kamondi 1 1 National Institute of Neurosciences, Budapest 2 National Institute of Rehabilitation, Budapest 3 Semmelweis University, Budapest 4 University of Pécs, Medical School, Pécs, Hungary Received December 17, 2010; Accepted February 29, 2012 ABSTRACT – In reflex seizures induced by proprioceptive stimuli, the activated network may be identified as a single anatomo-functional cir- cuit; the sensory-motor network. These seizures may be considered as epileptically-enhanced stretch reflexes. Proprioceptive reflex epilepsies are a good example of the so-called “system epilepsies”. We present three cases discussing the clinical features of such epilepsies. [Published with videosequences] Key words: proprioceptive-induced, stretch reflex, sensory-motor, long-loop, seizure, system epilepsy, neural systems The definition of reflex epilepsies somato-sensory, and proprio- states that seizures are provoked by ceptive; thinking, reading, eating, certain stimuli or, less commonly, music, hot water (Grosso et al., 2004), mental processes. Individuals with and startle (Zifkin and Andermann, reflex epilepsy may have seizures 1998). exclusively in response to specific Reflex attacks induced by move- stimuli without suffering sponta- ment were reported more than neous seizures. Alternatively, reflex 100 years ago (Gowers, 1901). Early seizures may coexist with sponta- reports described seizures induced neously occurring seizures. They by movement (Lishman et al., 1962, may clinically manifest as partial or Falconer et al., 1963), but later generalised seizures and can simi- work demonstrated the role of pro- larly be associated with either focal prioceptive afferents (Chauvel and or generalised ictal epileptic dis- Lamarche, 1975). Thus, seizures orig- Correspondence: charges at onset (Engel, 2001). inally described as “movement-, Anna Szucs˝ Common precipitating stimuli or gait-induced” (Iriarte et al., National Institute of Neuroscience, for reflex seizures may be visual 2001) are more accurately defined Amerikai ut 57, 1147 Budapest, Hungary (Binnie and Wilkins, 1998; Zifkin as“proprioceptive-induced”(Vignal <[email protected]> and Kasteleijn-Nolst Trenité, 2000), et al., 1998). Proprioceptive-induced doi:10.1684/epd.2012.0499 Epileptic Disord, Vol. 14, No. 2, June 2012 149 A. Szucs,˝ et al. seizures are included as a reflex seizure type in the We present here three cases in order to demonstrate proposed classification of epilepsy syndromes (Engel, the clinical features of such epilepsies. 2001). Proprioceptive-induced seizures are provoked by Case l passive or active movement. The seizures are usually simple partial attacks manifested as tonic or clonic Her partial epilepsy started at age 10 and she did not motor movements of a limb; they may begin with become seizure-free despite many antiepileptic drugs. sensory manifestations. Sometimes they occur in Her left-sided lower limb sensory-motor seizures, subjects with cerebral lesions and motor deficit. They frequently leading to falls, could be provoked by have been described as transient phenomena during passive or active movement of the left leg, leading to non-ketotic hyperglycaemia, resolving with metabolic the stretching of her sole and generally unexpected correction (Brick et al., 1989) and as self-induced kinetic stimuli; slipping or lapse during walking. On attacks with proprioceptive self-stimulation (Guerrini her interictal EEG, Cz and C4 spikes were seen and et al., 1992). The epileptic nature of these seizures has could be provoked by movement, e.g. cycling. Scalp been confirmed by ictal EEG recordings (Arseni et al., ictal EEG recordings and clinical seizure manifestations 1967) and video telemetry. Reflex drop attacks may suggested the central, frontal or parietal region as the occur with walking in patients with EEG vertex spikes, seizure-onset zone (figure 1 A, B, C, D). The patient did evoked by percussion of the sole of the foot (Tassinari not agree to invasive monitoring which would have et al., 1988, Tedrus et al., 2005). provided better localisation. A Fp2 F8 Roham F8 T4 T4 T6 T6 O2 200uV Fp1 F7 F7 T3 T3 T5 1sec T5 O1 Fp2 F4 F4 C4 C4 P4 Seizure onset P4 O2 Fp1 F3 F3 C3 C3 P3 P3 O1 Fpz Fz Fz Cz Cz CPz CPz Pz EOG1+EOG1- EOG1 EOG1+ EMG1+EMG1- B Fp2 F8 F8 T4 T4 T6 T6 O2 Fp1 F7 200uV F7 T3 T3 T5 1sec T5 O1 Fp2 F4 F4 C4 C4 P4 P4 O2 Fp1 F3 F3 C3 C3 P3 P3 O1 Fpz Fz Fz Cz Cz CPz CPz Pz EOG1+EOG1- EOG1 EOG1+ EMG1+EMG1- Figure 1 (A-D)– Patient 1. EEG sequence of a seizure provoked by movement of the left leg. The electrographic seizure starts at the Cz electrode. (EEG low pass filter: 0.3Hz; high pass filter: 70Hz). 150 Epileptic Disord, Vol. 14, No. 2, June 2012 Proprioceptive reflex seizures C Fp2 F8 F8 T4 T4 T6 T6 O2 Fp1 F7 F7 T3 200uV T3 T5 T5 O1 1sec Fp2 F4 F4 C4 C4 P4 P4 O2 Fp1 F3 F3 C3 C3 P3 P3 O1 Fpz Fz Fz Cz Cz CPz CPz Pz EOG1+EOG1- ECG1- ECG1+ EMG1+EMG1- D Fp2 F8 F8 T4 T4 T6 T6 O2 Fp1 F7 F7 T3 200uV T3 T5 T5 O1 1sec Fp2 F4 F4 C4 C4 P4 P4 O2 Fp1 F3 F3 C3 C3 P3 P3 O1 Fpz Fz Fz Cz Cz CPz CPz Pz EOG1+EOG1- ECG1- ECG1+ EMG1+EMG1- Figure 1 (A-D)– Patient 1. (Continued) Her brain MRI and tibial nerve somato-sensory evoked position with rare clonus-like jerks. She could neither potentials (SEPs) were normal. extend nor bend the knee, making her unable to stand On combined antiepileptic therapy, lamotrigine and or walk. topiramate, she had 1-2 seizures/month. Brain MRI was normal. We consider this case to be partial epilepsy with reflex Her seizures could be provoked by the movement somato-sensory seizures, elicited by proprioceptive of the left leg, but also by imaginative spatial experi- stimuli. ences without movement, e.g. looking down the stairs or from a great height. Some of her motor seizures developed during sleep, when, according to her Case 2 report, she had a dream with spatial experiences. Her interictal EEG showed sharp waves and spikes with Her epilepsy started at age 22. Her stereotyped left maximum amplitude at the centro-parietal electrodes, lower limb sensory-motor simple partial attacks lasted most frequently during non-REM sleep. for 25-35 seconds and occurred several times a day. The ictal electrical activity appeared 6-7 seconds after These attacks started with the strange feeling “Ido a clinical seizure had started in Pz, involving some- not feel my leg below my knee”. Subsequently, a left times also the Cz electrode. The ictal electrical activity, leg cramp developed. Her left foot took an extended lasting only for 6-9 seconds on the scalp, was an 8-Hz Epileptic Disord, Vol. 14, No. 2, June 2012 151 A. Szucs,˝ et al. rhythm, gradually slowing down to 6 Hz and disappear- Case 3 ing before clinical seizure offset (figure 2). During a morning of video-EEG monitoring, the patient His falls induced by jogging started at age 21. When reported dreaming of a seizure. There was no clin- he ran, he fell stereotypically after 10-15 steps (see ical seizure during that night, but during REM sleep video sequence). He remembered his right leg becom- a 9-second EEG seizure pattern without obvious clin- ing rigid, his right arm elevating, and falling on the ical manifestation was registered; a fast ictal rhythm right side without loss of consciousness. He was starting in the Cz-Pz electrodes, rapidly involving the also able to provoke his falls by cycling. Brain MRI para-sagittal areas (figure 3). revealed a large left temporal arachnoidal cyst. Video- She had rare seizures on carbamazepine and EEG monitoring showed clear left frontal interictal lamotrigine therapy. sharp waves and he could provoke his stereotyped We consider this case as partial epilepsy with sensory- reflex seizures, with no clear ictal EEG pattern iden- motor seizures, elicited by proprioceptive stimuli of tified during the violent movements. However, these the leg (and also by “proprioceptive imagination”). The events were stopped on carbamazepine treatment probable seizure-onset zone seems to be the central and he has been seizure-free for more than a year region. now. G2 G2 Fp2 F8 1,000F8 T4 Hz Low pass filter: 70 Hz Gain: 0200 µV/cm T4 T6 T6 O2 Fp1 F7 F7 T3 T3 T5 200uV T5 O1 Fp2 F4 F4 C4 1sec 1sec C4 P4 P4 O2 Fp1 F3 F3 C3 C3 P3 P3 O1 Fpz Fz Fz Cz Cz Pz Pz Oz Zyg2 Ft10 Ft10 Tp10 Tp10 Po10 Zyg1 Ft9 Ft9 Tp9 Tp9 Po9 Zyg2 Zyg1 emg1 emg2 ecg G2 Figure2–Patient 2. EEG of a seizure provoked by movement of the left leg. The electrographic seizure starts at the Pz-Oz channel. (EEG low pass filter: 0.3Hz; high pass filter: 70Hz). G2 G2 elektromos roham rem-ben Fp2 F8 F8 T4 T4 T6 T6 O2 Fp1 F7 F7 T3 200uVT3 T5 T5 O1 seizure Fp2 F4 1sec F4 C4 C4 P4 P4 O2 Fp1 F3 F3 C3 C3 P3 P3 O1 Fpz Fz Fz Cz Cz Pz Pz Oz Zyg2 Ft10 Ft10 Tp10 Tp10 Po10 Zyg1 Ft9 Ft9 Tp9 Tp9 Po9 Zyg2 Zyg1 emg1 emg2 ecg G2 Figure3–Patient 2. EEG of an electrographic seizure during REM sleep. (EEG low pass filter: 0.3Hz; high pass filter: 70Hz). 152 Epileptic Disord, Vol. 14, No. 2, June 2012 Proprioceptive reflex seizures Tibial nerve SEPs were normal but cortical magnetic seizure is the epileptic hyperexcitability of the involved stimulation revealed hyperexcitability of the motor cortical area.