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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.
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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.