Fixation-Off and Eyes Closed Catamenial Generalized Nonconvulsive Status Epilepticus with Eyelid Myoclonic Jerks
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1 ~ ~ ~~ ~ ~~~~ Epilepsia, 39(6): Lippincott-Raven Publishers, Philadelphia 0 International League Against Epilepsy Fixation-Off and Eyes Closed Catamenial Generalized Nonconvulsive Status Epilepticus with Eyelid Myoclonic Jerks Xue Ming and *Peter W. Kaplan Division of Pediatric Neurology, University of Medicine and Dentistry of New Jersey, New Jersey Medical School, Newark, New Jersey; and *Johns Hopkins Bayview Medical Center, Johns Hopkins School of Medicine, Baltimore, Maryland, U.S.A. Summary: Purpose: Eyelid myoclonic jerks have been described in fixation-off-sensitive (FOS) epilepsy, but their relationship to nonconvulsive status epilepticus (NCSE) or to catamenial exacerbations is little reported. Methods: We describe a woman of normal intelligence with catamenial periods of prolonged NCSE who exhibited various intra- and interseizure thresholds of polyspike suppression when her eyes were open, with particular visual inputs and with antiepileptic drug (AED) treatment. Results: In one episode, on the first day of the woman s menstrual period, bursts of bilateral synchronous polyspike activity were briefly suppressed with visual fixation but were more lastingly suppressed after administration of lorazepam (LZP). During another period of NCSE, the SE was completely suppressed by visual fixation on objects and patterned checkerboard screens and by ocular convergence, was incompletely suppressed when her eyes were open in a dark room and when her eyes were open without visual fixation, but was not suppressed by mental activation alone. Conclusions: FOS polyspike bursts with eyelid myoclonic jerks may exhibit catamenial exacerbations, varying from completely suppressible with visual fixation to nonsuppressible during NCSE.These findings suggest an interplay between humoral factors, AEDs, and seizure threshold in this condition. Key Words: Generalized nonconvulsive status-fixation off-eyes closed-catamenial-eyelid myoclonic jerks. The induction of epileptic seizures, particularly eyelid myoclonic jerks with absences on eye closure (EMA) associated with bursts of EEG spike-slow-wave activity has long been recognized (14). Jeavons in 1982 (5) and Panayiotopoulos in 1987 (6) reported that inhibition of central vision, blinking, photic stimulation or darkness triggered generalized and posterior epileptiform discharges. Status epilepticus (SE) is rare (7) and may be limited by eye opening (3). We describe the clinical and EEG features in an adult with normal intelligence with fixation-off-sensitive (FOS) catamenial generalized nonconvulsive status epilepticus (GNSE). CASE REPORT The patient is a 24-year-old, gravida 0, para 0, college student with onset of seizures at age 8 years. She was noted to have episodes of staring, appearing dazed, walking in circles, and becoming lost on her way home. Further history regarding these episodes could not be obtained. Routine interictal EEG recorded at age 8 years showed normal posterior rhythm with generalized 2- to Accepted January 29, Address correspondence and reprint requests to Dr. P. W. Kaplan at JHBMC, 4940 Eastern Ave., Baltimore, MD U.S.A. 4-Hz high-voltage spike-and-wave discharges (SWD), maximally in the frontocentral regions. These were not induced by photic stimulation, but were by hyperventilation. There were no reported clinical correlations with the EEG bursts of spike-wave activity. During sleep, the EEG showed frequent bursts of generalized 1- to 2-Hz spike-waves with some polyspike-waves, lasting 2-10 s. She was treated with phenobarbital, but control of seizures was poor; after substitution of valproate (VPA), she had good seizure control for several years. She discontinued VPA because of weight gain, and had 4-6 tonic-clonic seizures and 8-12 observed episodes of prolonged staring each year, with onset at age 10 years. At age 11 years, the EEG showed bursts of frontocentrav generalized spikes and polyspikes with no change with intermittent photic stimulation (IPS). With improvement of compliance she had good seizure control for several years, but when antiepileptic drugs (AEDs) were discontinued, tonic-clonic seizures and staring recurred, with interictal EEGs showing generalized 2- to 4-Hz spikewave activity similar to that in the EEG recorded at age 11. Eye opening and closing produced no EEG paroxysms. When the patient, often noncompliant with AEDs treatment, was eiamined at age 15, her mother reported that the girl had had tonic-clonic seizures as well 664
2 NCSE AND EYELID MYOCLONIC JERKS 665 as pfolonged periods of blinking and staring and being distracted and sluggish. At age 16 years, the flickering effect of bright sunlight shining through tree leaves or seeing firecrackers caused her to have episodes of staring and confusion for several minutes. She was not followed by a neurologist and no EEG was obtained, although she continued VPA treatment. At age 22, with treatment with VPA lglday, she developed more frequent prolonged episodes of staring and eye blinking, with anxiety and emotional lability. Her speech became slurred and was decreased in output and volume; her sentences became fragmented, although her level of comprehension appeared intact. She was clumsy and uncoordinated, with a waxing and waning level of consciousness. During this time, flickering lights, or physical or emotional stress precipitated seizures, although she was not able to induce them herself. Seizures tended to occur on weekends and holidays (Thanksgiving, Christmas, or New Year s Eve) and were unrelated to medication compliance. She noted that about half her episodes occurred a few days before or during her menstrual periods. During these episodes, which lasted 6-38 h, she would lie still, was reluctant to talk, and refused to drink or eat or engage in daily activities. An EEC at this time showed bursts of eyelid myoclonic jerks when her eyes were closed, associated with ongoing generalized bursts of 10- to 14-Hz polyspike discharges apparent synchronously, bilaterally (each lasting s) through- out the record. The bursts of polyspikes occurred with the bursts of rapid, fine rhythmic eyelid flickering with upward jerking of the eyes. When her eyes were open, there was then an almost complete suppression of polyspike bursts, which recurred only when her eyes were closed. Eyes-open suppression was not tested longer than 10 s. With eyes closed, mental activation, counting and talking did not attenuate the polyspike bursts; she remained alert, orientated, and counted backward faultlessly. The effects of darkness when eyes were open and closed and during visual fixation were not tested at that time. At age 23 years, when she was noted to be mildly confused, her EEG showed ongoing bursts of polyspike activity-only when her eyes were closed-that continued throughout the recording (Fig. 1). There were eyelid myoclonic jerks. She remained fluent, answered questions appropriately, could count backward, and was oriented to time, place, and person. An interictal EEG showed only brief, generalized polyspike bursts that also occurred during IPS stimulation, but that did not outlast the stimulus. At age 24, the patient had a recorded episode that contrasted with previous EEG findings: Polyspike burst threshold was altered by administration of intravenous benzodiazepines. The patient s mother called regarding one of the patient s episodes. The patient felt unwell and had eyelid flickering and was asked to come to the FIG. 1. EEG recorded when the patient was 23 years old. The recording with eyes closed shows ongoing bursts of diffuse, bilateral, synchronous polyspike activity with eyelid myoclonic jerks. When her eyes were open, the polyspike bursts were almost completely suppressed, but recurred on eye closure. Mental activation with eyes closed did not affect ongoing EEG polyspike bursts.
3 666 X. MING AND P. W. KAPLAN hospital. When examined, she was crying and moved slowly. She manifested ongoing high-frequency eyelid myoclonic jerks, with intermittent upward rolling of the eyes. She was awake, but her alertness was reduced. She followed one-step commands slowly but had great difficulty with complex commands and was slow in attempted rapid fine motor movements. She was oriented to person only; speech was dysarthric and slow, with frequent perseveration. Comprehension was relatively preserved, but counting to 20 took her almost 5 min with perseveration and many mistakes. The remainder of her neurological examination was nonfocal. The EEG showed ongoing bursts of polyspike activity with polyspike bursts lasting as long as 1.5 s. This activity was not affected when her eyes were closed, either voluntarily or forced, and she had no response to photic stimulation, hyperventilation, or mental activation. Visual fixation on a point -40 cm from her face caused polyspike activity to be suppressed for 1-4 s. Hand waving behind the objects at focus resulted in immediate return of polyspike activity. After administration of lorazepam (LZP), polyspike activity continued but could then be immediately blocked by visual fixation. There was subsequent regression of all spike activity and normalization of mental status in s 5 min. Measured before LZP administration, progesterone level was 0.1 ng/ml; luteinizing hormone level was c 1.O MIU/ml, follicle stimulating hormone level 0.3 MIU/ml, and prolactin level was 10.3 ng/ml. Lamotrigine (LTG) treatment was started, and VPA dosage was increased. Two months later, on the first day of her menstrual cycle, her mother noted her to be confused and lethargic, with eyelid fluttering. Her physical examination performed 5 h later showed her condition to be similar to that previously described, but EEG showed the following features. There was continuous, generalized polyspike activity for s with different levels of polyspike burst reactivity to testing: (a) It was unaffected by counting and mental activation; (b) it was incompletely suppressed by her eyes being open in a dark room, by her staring at her raised thumb (although she could not see it) or at a red light in a dark room; or by her eyes being open but without visual fixation; (c) it was completely suppressed by her eyes being open in a lighted room with visual fixation on a white lamp, on objects, and on a patterned checker-board screen (Figs. 2 and 3); and it FIG. 2. At age 24 years, during an episode of nonconvulsive status epilepticus (NCSE): The patient opened her eyes, causing a brief suppression of seizure activity for 2 s (arrow). Complete suppression occurred 3 s later during mental activation and visual scanning of a picture while she, described the contents. 10, and 10, are inferior orbital electrode placements below the left and right eyes, respectively. The patient demonstrated improvement in nonvisual cognitive tasks improved when her eyes were open.
4 NCSE AND EYELID MYOCLONIC JERKS 667 FIG. 3. The patient s eyes were open in a lighted room (first arrow). EEG shows the reappearance of diffuse polyspike bursts afler the patient s eyes were closed (second arrow). was suppressed by ocular convergence and by visual fixation on a white dot in a darkened room. There was minimal symmetric photic driving. Hyperventilation was poorly performed and caused no EEG change. DISCUSSION Our case presents several points of interest, including: (a) a variable threshold of FOS epileptiform activity in an adult with normal intelligence; (b) frequent catamenial exacerbations, and (c) GNSE with prolonged polyspike complexes and eyelid myoclonic jerks. The catamenial appearance of seizures in our patient, the lack of clear triggering of NCSE by photic stimulation or hyperventilation, and the stepwise suppression of seizure activity with various visual maneuvers all support an additional nonreflex contribution to her condition. FOS is evident in many epileptic conditions and was initially described in benign childhood epilepsy with occipital paroxysms and other rare conditions (6-9). Panayiotopoulos (6,8) emphasizes the distinction between FOS epilepsy and photosensitive epilepsy, in which photoparoxysmal discharges occur only when the patient fixes on the center of the lamp, when fixation on patterns increases,photosensitivity, and when abnormal discharges in the resting EEG are induced by eye closure. These differences suggest that photosensitive epilepsies and FOS are at opposite ends of a spectrum (6,8). The sensoryhisual epileptic interactions are complex and poorly understood (10). Speculation on epileptic triggers centers on changes in afferent light and retinal illumination in which epileptiform activity in different patients may increase or decrease with retinal illumination (10). When the eyes are closed, there may be a modification of retinal input, resulting in diffusion of light and a filtering effect, thus permitting red frequencies to reach the retina. Because the visual system may be particularly sensitive to red light with a difference in cortical response to patterns or diffuse inputs, the epileptogenic circuit may involve modification of the corticoreticular firing threshold with particular visual inputs (10). Othq investigators have speculated that eye position may act as a trigger because patients, when closing their eyes even in total darkness, may trigger seizures (1). As noted by Lewis (lo), the EEG changes that occur when the subject s eyes are closed may represent the summation of several different excitatory and inhibitory mechanisms. A new pattern in GNSE GNSE has been described in four groups of patients: (a) patients with a history of childhood absences and
5 668 X. MING AND P. W. KAPLAN EEGs. characterized by continuous or frequent 3-Hz/ spike-waves; (b) patients with childhood-onset, secondary generalized epilepsy, often with mental retardation, greater confusion, and myoclonus; (c) elderly patients usually without epilepsy but with status induced by drugs or drug discontinuation; and (d) patients with generalized SE arising from a temporal or frontal lobe focus (11). Our patient does not fit any of these categories. She has idiopathic (primary) generalized epilepsy without typical absences. There were no limb jerks to suggest juvenile myoclonic epilepsy, and she did have tonic-clonic seizures. The GNSE was not characterized by typical 3-Hz spike-and-wave patterns; instead, there were prolonged polyspike bursts and FOS features. Despite the many prolonged episodes of GNSE (S38 h) she experienced for years, there was little if any discernible lasting effect on her cognitive function interictally, as evidenced by her excellent academic performance and results of formal neurospsychological tests. This finding is in keeping with the lack of cognitive deficits observed in GNSE (1 1). Catamenial seizures and SE Catamenial epilepsy (CE)--exacerbation of epilepsy with the menstrual period-has long been recognized since Gowers description in 1885 (12). Seizures in CE typically occur just before and during menses (12,13), but some researchers have cast doubt on the existence of CE (14). Problems in identifying this disorder include inexact documentation of catamenial exacerbations, cyclical seizures unrelated to menses, poor descriptions of seizure type and relation to cycle, and brief follow-up (13). A recent report, however, more clearly defines partial CE into three patterns on the basis of the neuroactive properties of estradiol and progesterone, but there is reason to believe that catamenial exacerbation can occur with idiopathic generalized epilepsies (15). The firsttype of CE, perimenstrual (catamenial l), generally occurs from about day -3 to +3 of the first day of the menstrual cycle >3 days after progesterone withdrawal. This occurs when the estradiouprogesterone ratio is high and AED levels may be reduced by a perimenstrual increase in hepatic enzyme induction. The second type of CE, periovulatory (catamenial2), occurs at about days 10 to -13 of the cycle and is purportedly due to the surge in estrogen unaccompanied by increases in progesterone until ovulation occurs. In the third type, anovulatory exacerbations (inadequate luteal phase cycles, catamenial 3) occur at about days in the midluteal phase when estradiouprogesterone ratios are highest (15). Our patient most frequently had catamenial GNSE that corresponded to the timing of the catamenial 1 type, and progesterone levels were low. Photoconvulsive photosensitivity can vary with the menstrual cycle, and generalized spike- and-waves may also increase during menses in women with EMA (3,7); catamenial status has also been described in some of these patients (6,7). In our patient, there was an evolution from absence seizures to tonic-clonic seizures to a frequently catamenial GNSE with different thresholds of seizure suppression (immediately after administration of intravenous LZP) when her eyes were open and with visual fixation. The initial recorded episode showed no suppression of polyspike activity when her eyes were open, and no suppression induced by fixation until LZP was added, whereas a subsequent episode occurring after addition of LTG showed clear FOS features. These findings suggest that FOS genetic epilepsies can have a highly variable seizure threshold that can be modulated by endocrine states, AEDs, and sensory inputs. As emphasized by Lewis (lo), such day-to-day variability in clinical seizure expression with different interactions between and among eye closure, eye opening, seizures, and menses suggest a more complex explanation than one of a specific reflex epilepsy (10) or of idiopathic generalized epilepsy. Acknowledgment: We thank Sylvia Parham for excellent EEG technical assistance. REFERENCES 1. Green JB. Seizures on closing the eyes: electroencephalographic studies. Neurology 1968;18: Vignaendra V, Ghee T, Loh, Lee C, Lim Siew Tin. Epileptic discharges triggered by blinking eye closure. Electroencephatogr Clin Neurophysiol 1976;40: Veggiotti P, Viri M, Lanzi G. Electrical status epilepticus on eye closure: a case report. Neurophysiol Ctin 1991; Gastaut H, Tassinari CA. Triggering mechanisms in epilepsy: the electroclinical point of view. Epilepsia 1966;7: Jeavons PM. Photosensitive epilepsy. In: Laidlaw J, Richens A, eds. A textbook of epilepsy. Edinburgh: Churchill Livingstone, 1982: Panayiotopoulos CP. Fixation-off-sensitive epilepsy in eyelid myoclonic jerks with absence seizures. Ann Neurol 1987;22: Agathonikou A, Koutroumanidis M, Panayiotopoulos C. Fixationoff-sensitive epilepsy with absences and absence status: video- EEO documentation. Neurology 1997;48: Panayiotopoulos CP. Conversion of photosensitive to scotosensitive epilepsy. Neurology 1979;30: 155G5. 9. Giqnakodimos S, Panayiotopoulos CP. Eyelid myoclonic jerks with absences in adults: a clinical and video-eeg study. Epilepsia 1996;37: Lewis JA. Eye closure as a motor trigger for seizures. Neurology 1972;22: Kaplan PW. Nonconvulsive status epilepticus. Semin Neurol 1996; Gowers WR. Epilepsy and other chronic convulsive diseases: their causes, symptoms and treatment. 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