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Bicycling During Complex Partial Seizures 1.235 R. J. Kotloski and C. A. O’Donovan Dept of Neurology, Wake Forest University School of Medicine Winston-Salem, NC Abstract RATIONALE: Loss of consciousness during seizures is a factor which limits activity of patients with epilepsy. Driving restrictions are reported to have the most impact on quality of life and gained the most attention. Testing individuals in the ictal state to determine ability to perform these activities has logistical difficulties. Bicycling is another activity of concern on which the impact of seizures is unclear. We observed two patients who continued to use a stationary bicycle during part of vEEG recorded seizures. METHODS: Two patients with intractable seizures admitted for vEEG evaluation. Several seizures were recorded in both patients and each patient had a seizure while using stationary bicycle. RESULTS: The first patient was a 42 year old male with a long history of intractable complex partial seizures. While using a stationary exercise bicycle, the patient continued to cycle for 30 seconds despite instructions to stop and EEG demonstrated simultaneous left temporal seizure activity. The second patient was a 25 year old male with frontal lobe epilepsy and generalized tonic-clonic seizures. This patient continued to pedal on the bicycle during 30 seconds of generalized epileptiform pattern prior to tonic-clonic seizure. CONCLUSIONS: Pedaling of a stationary bicycle occurred during vEEG-confirmed seizure activity thought to arise from the temporal lobe in one and the frontal lobe in the other patient. Loss of awareness was confirmed in one patient with lateralized seizure activity, and a generalized discharge was present in the other patient. Although using a stationary bicycle may not require the same level of consciousness as cycling, these movements did persist during EEG seizure activity. This suggests that brief seizures during cycling may not result in adverse events related to loss of awareness and is worthy of further study. Case #1 Patient 1 was a 42 year old, left-handed male with an approximately 20 year history of complex partial seizures. The patient’s typical seizures began with an aura of disassociation. The patient then would stare for 5 to 15 seconds. The patient was was amnestic for the event, and often emotionally labile and irritable for several minutes afterwards. The patient had about 6 seizures per month. The patient’s seizures had proved resistant to phenytoin, valproic acid, carbamazepine, topiramate, gabapentin, and oxcarbazepine prior to his current regimen of lamotrigine. 20:33:17 The patient had meningitis as a child, resulting in left-sided hearing loss, was well as a concussion as a child. There was no family history of epilepsy or seizures. The patient had co-morbid depression. An MRI of his brain demonstrated right hippocampal sclerosis (Figure 1). The patient was admitted to the Epilepsy Monitoring Unit for further evaluation. Prior to admission the patient’s lamotrigine was tapered from 325mg twice a day to 100mg twice a day. The patient’s baseline EEG on admission was unremarkable with a posterior dominant rhythm of 9Hz and an amplitude of 20 μV. During a 7 day stay in the EMU the patient had a total of 16 clinical events. Ten of the events had clear EEG changes. During one event the patient was using a stationary exercise bicycle. The patient’s wife asked him to stop pedaling several times. Thirty-six seconds later the patient stopped pedaling but did not recall being asked to stop. He continued to be confused for another 70 seconds before recovering back to baseline. During the episode the patient’s EEG demonstrated a loss of background activity at 20:33:17. Ten seconds prior to his wife asking the patient to stop at 20:33:44, the patient developed 4Hz activity in the left hemisphere, with greater amplitude in the temporal region as compared to the central regions. The rhythmic activity ends at 20:34:02 (Figure 3). The patient eventually underwent a right temporal lobectomy in June 2005 (Figure 2). His seizure frequency greatly improved and he has been seizure-free in July 2008 on lamotrigine 300mg twice a day and levetiracetam 750mg twice a day. Figure 1. Coronal FLAIR MRI demonstrating right hippocampal sclerosis. 20:33:34 20:33:39 Case #2 Discussion Patient 2 was a 25 year male with a 7 year history of epilepsy, following a motor vehicle accident. The patient would rarely have an aura of fear prior to his seizures. The seizures started with head turning to the left and left arm posturing, before secondarily generalizing to tonic-clonic seizure. The patient would have about three seizures a month. These two cases demonstrate that the complex movements of bicycling can continued despite electrographic seizure activity. In the first case, the patient continues to ride an exercise bicycle for 36 seconds despite a right temporal electrographic seizure discharge and impaired consciousness. The second case presents an episode of continued use of an exercise bicycle for nearly 30 seconds despite generalized seizure activity. The patient had initially become seizure-free for greater than a year on phenytoin, but developed elevated liver enzymes. He was tried on topiramate, lamotrigene, oxcarbazepine, tiagabine, and valproic acid with some improvement. He was eventually restarted on phenytoin 100mg BID and continued on valproic acid 500mg TID. The patient was admitted to the Epilepsy Monitoring Unit for further evaluation. The patient’s baseline EEG upon admission was unremarkable, with a posterior dominant rhythm of 10Hz and an amplitude of 20-30 μV. There was no change with photic stimulation or hyperventilation. During a 6 day EMU stay, the patient was weaned off his valproic acid, but continued on his home dose of phenytoin. He had a total of two events during the admission. During the first event the patient was using a stationary bicycle. The patient continued to bicycle for 53 seconds. The patient’s head turned to the left and he continued pedaling for 3 seconds before stopping. The patient then continued on to have a tonic-clonic seizure for 41 seconds (Figure 4). During the event the patient’s EEG slowed from a normal waking rhythm to bifrontal 3Hz activity at 11:20:17. The frequency in the frontal derivations increased to the alpha range, then again slowed to 3Hz at 11:20:25. At 11:20:42 the patient develops sharply contoured alpha activity until the record is obscured by EMG artifact. Figure 2. Coronal FLAIR MRI after right temporal lobe resection. 20:33:45 20:33:50 20:33:55 20:34:00 20:34:05 11:19:52 11:20:02 11:20:12 11:20:22 11:20:32 11:20:42 11:20:43 11:20:44 11:20:45 11:20:47 11:20:49 11:20:51 11:20:53 11:20:55 Figure 4. Video captures of patient 2. Review of literature Complex automatisms, including bipedal movements, have been described during complex partial seizures previously (Tharp, 1972; Sussman et al., 1989; Swartz, 1994). In one series of temporal lobe seizures (Chou et al., 2004), bilateral lower extremities automatisms were reported in 10/123 complex partial seizures. The movements were described as ‘scissoring’, ‘as if he is trying to run away’, ‘pedaling’, and ‘bicycling’ (Swartz, 1994), but to our knowledge there has not been a report of a patient pedaling a bicycle during a seizure. The localizing value of such movements is unclear. The seizure focus in patient 1 was in the right temporal lobe based on his EEG, and further supported by his greatly improved seizure frequency after right temporal resection. The focus in patient 2 was likely frontal. Both orbital frontal and temporal lobe seizure foci have been described as resulting in bicycling movements, although Swartz (1994) found a nearly 4-fold increase in incidence with frontal lobe seizures. Pedaling of the lower extremities has also been reported with seizures arising from the insular cortex (Kaido et al., 2006). The presented cases also highlight the difficulty with assessing alterations in consciousness during seizures. Both patients appeared to continue a purposeful behavior. However, patient 1 was unresponsive to his wife during his seizures. Patient 2 was not tested during the beginning of his seizure, and seizure activity would not have been expected based on his behavior. While the mechanism of impaired consciousness during seizures is not certain (Yu and Blumenfeld, 2009), several theories, such as bilateral electrographic seizures or involvement of subcortical structures leading to network inhibition (for review see Englot and Blumenfeld, 2009). Furthermore, studies have been performed to evaluate driving during seizures (Yang et al., 2010). Yang and colleagues used a video game simulation to evaluate driving performance during seizures. This study demonstrated the feasibility of prospectively studying performance of complex tasks during seizures, which in conjunction with identification of the structures and pathways involved in the seizure activity will help to identify the neural substrates of consciousness. Awareness of the diversity of seizure presentations is important to coming to the correct diagnosis based on semiology. These two cases provide evidence that relatively complex bipedal activities can persist despite generalized electrographic seizures. Several unanswered questions remain. Both patients were bicycling when the seizure activity began. It seems unlikely that the continued pedaling was a direct consequence of the seizure activity. However, it also unlikely that the movements were volitional, as both patients likely had impaired consciousness. Patient 1 was clearly unresponsive to his wife during his seizure, and patient 2 had bilateral electrographic seizure activity as he continued to pedal, although his responsiveness was not tested. One possibility is that the pedaling was an automatism, although the exact etiology of the movements is unknown. Conclusions: • Cycling continued during both seizures, partial temporal in patient 1 and generalized bifrontal in patient 2 • Continuation of complex bipedal movements in the presence of electrographic seizure activity and unresponsiveness suggests it’s an automatic behavior, likely not requiring consciousness, which was tested in patient 1 • The brain structures and networks underlying these movements have not been clearly identified • The question of whether aspects of cycling, such as purposeful and even appropriate responsiveness to external stimuli associated with cycling, is not fully answered, although it has been demonstrated that such a question is addressable (Yang et al., 2010) References: Chou, C-W., Yu, H-Y., Shih, Y-H., Yiu, C-H., Kwan, S-Y., Yen, D-J., Lin, Y-Y. Lateralization valve of lower limb behaviors in complex partial seizures of temporal lobe origin: a video-EEG analysis. Seizure 2004; 13:35-39. Englot, D.J., Blumenfeld, H. Consciousness and epilepsy: why are complex-partial seizures complex? Progress in Brain Research 2009; 177:147-70 Kaido, T., Otsuki, T., Nakama, H., Kaneko, Y., Kubota, Y. Sugia, K., Saito, O. Complex behavioral automatism arising from insular cotex. Epilepsy and Behavior 2006; 8:315-19. Swartz, B.E. Electrophysiology of bimanual-bipedal automatisms. Epilepsia 1994; 35(2):264-74. Sussman, N.M., Jackel, R.A., Kaplan, L.R., Harner, R.N. Bicycling movements as a manifestation of complex partial seizures of temporal lobe origin. Epilepsia 1989; 30(5):527-31. Tharp, B.R. Orbital frontal seizures: 13:627-42. a unique electrophysiologic and clinical syndrome. Epilepsia 1972; Yang, L., et al. A prospective study of loss of consciousness in epilepsy using virtual reality driving simulation and other video games. Epilepsy and Behavior 2010; 18:238-46. Yu, L., Blumenfeld, H. Theories of impaired consciousness in epilepsy. Annals of the New York Academy of Sciences 2009; 1157:48-60 Figure 3. EGG and video captures from Patient 1.