Epilepsy & Behavior 28 (2013) S25–S29
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Review
Chronodependency and provocative factors in juvenile myoclonic epilepsy Dorothée G.A. Kasteleijn- Nolst Trenité a, b,⁎, Al de Weerd c, Sándor Beniczky d, e a
University of Rome “Sapienza” II, Rome, Italy University Medical Centre Utrecht, The Netherlands c Clinical Neurophysiology and Sleep Center SEIN Zwolle-Groningen, Zwolle, The Netherlands d Department of Clinical Neurophysiology, Danish Epilepsy Centre, Dianalund, Denmark e Department of Clinical Neurophysiology, University of Aarhus, Denmark b
a r t i c l e
i n f o
Article history: Accepted 20 November 2012 Keywords: Juvenile myoclonic epilepsy Chronodependency EEG Provocative Reflex Sleep Photosensitivity Reading Cognitive tests
a b s t r a c t In juvenile myoclonic epilepsy (JME), occurrence of seizures and epileptiform EEG discharges is influenced by internal and external factors. The most important internal factor is the chronodependency: the occurrence of myoclonic jerks in the early morning is one of the hallmarks of JME. Approximately two-thirds of the patients with JME report that seizures are provoked by a variety of general factors like stress, fatigue, fever, and sleep and more specific precipitants like flashing sunlight, music, reading, thinking, and excess alcohol. The prevalence rate of photosensitivity (photoparoxysmal EEG response) in patients with JME ranges from 8 to 90%; it is seen more often in females and adolescents and depends on drug use. Since both JME and photosensitivity are connected with generalized types of epilepsy and myoclonus, the two traits are comorbid for that reason. Epileptiform EEG discharges can be provoked by other activation methods: sleep, hyperventilation, and specific cognitive tasks. Attention seems to have a non-specific, inhibitory effect of the epileptiform discharges. Hyperventilation can induce absence seizures in patients with JME, while cognitive tasks are efficient in precipitating myoclonic seizures. This article is part of a supplemental special issue entitled Juvenile Myoclonic Epilepsy: What is it Really? © 2013 Elsevier Inc. All rights reserved.
1. Introduction In JME occurrence of seizures and epileptiform EEG discharges is influenced strongly by factors, like stress, fatigue, fever and sleep and more specific precipitants like flashing sunlight, music, reading, thinking and excess alcohol. The most important internal factor is the chronodependency: the occurrence of myoclonic jerks in the early morning is one of the hallmarks of JME. We will give an update of the knowledge concerning provocative factors and will advice optimal diagnostic strategies. 2. Chronodependency Seizures do not occur randomly over a 24-hour period as is known, for example, from frontal lobe epilepsy and benign epilepsy in childhood with centro-temporal spikes, both characterized by highest prevalence of seizures in the night, and juvenile myoclonic epilepsy (JME), where most seizures occur in the morning shortly after awakening. Indeed, the occurrence of myoclonic jerks in the early morning is one of the hallmarks of JME. Large studies with scalp and intracranial EEG recordings have recently been performed to determine distribution of partial seizures ⁎ Corresponding author at: University Medical Centre Utrecht, The Netherlands. E-mail address:
[email protected] (D.G.A. Kasteleijn- Nolst Trenité). 1525-5050/$ – see front matter © 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.yebeh.2012.11.045
over a 24-hour period [1–4]; in adults and children, complex partial seizures are predominantly seen during daytime between 11 AM and 5 PM, while their occurrence is lowest at night (11 PM–5 AM) (Fig. 1). There are differences between children and adults: partial tonic seizures in children occur mostly between 11 PM and 11 AM, while temporal lobe seizures in adults occur significantly more often between 11 AM and 5 PM. In children with extra-temporal and notably frontal seizures, peak frequencies are found in the period 11 AM–5 PM. Zarowski et al. [5] studied the prevalence of generalized seizures in children and adolescents: clonic seizures had their peak prevalence at 6–9 AM and 1–3 PM, absences between 9–12 AM and 6–12 PM, atonic seizures from 12 AM to 6 PM, myoclonic seizures (mostly patients with JME) between 6 AM and 12 AM, and spasms with two peaks at 6–9 AM and 3–6 PM. For all generalized seizures, the prevalence of seizures was lowest during nighttime. In (Fig. 2) an example of the relationship of day and nighttime and the occurrence of epileptiform discharges in a drug-naïve patient with JME is given. Besides better understanding of underlying pathophysiology, knowledge of biorhythmicity of different types of seizures and epilepsy syndromes helps in timing of diagnostic procedures and intake of antiepileptic medication (Fig. 2). In 1957, Janz and Christian described patients with JME with the sleep/wake rhythm [6]: they tend to get up late in the morning, are most active in the afternoon and evening, and go to bed late. We would say now that they have an evening type circadian rhythm.
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Fig. 1. Bar histograms showing the distribution of seizures over a period of 36 h. For further explanations, see the text (Ref. [1]).
Subsequently, questionnaires on preferred timing of activities over the 24-hour day, leading to “chronotyping”, have been developed and validated in large population studies [7,8]: young children and the elderly tend to be morning types, while adolescents are often evening types. In a study comparing them with patients with temporal lobe epilepsy (TLE), patients with JME showed evening type behavior significantly more often than patients with TLE [9]. This might be an artificial finding, as patients with JME are often teenagers or young adults. Indeed, in a study of patients with various types of epilepsy (N = 38 cases of JME, N = 46 cases of TLE, and N = 30 cases of FLE, all groups with a mean age of 40 years), no significant differences in chronotypes were found: in all three groups, around 55% of the patients classified themselves as tending to be a morning type [10]. Control patients without epilepsy were more evening type oriented. Except for differences in age of the patients in the three above mentioned studies, no explanation can be given for the opposite findings over the course of time.
3. Provocative factors Up to 65% of patients with epilepsy report that seizures are provoked by a variety of general factors like stress, fatigue, fever, and sleep and more specific precipitants like flashing sunlight, music, reading, thinking, and excess alcohol [11–13]. Stress, lack of sleep, and fatigue are by far the most recognized precipitants, and visual stimuli are considered to be a provocative factor in a substantial number of patients (10–15%) [12]. Sleep deprivation and visual stimuli are more often reported as seizure precipitants by patients with generalized epilepsies than by those with partial epilepsies [12]. 3.1. Photosensitivity About 15% of patients with JME report that flickering lights (disco, sunlight, and videogames) are provocative [14]. Electroencephalography studies with intermittent photic stimulation (IPS) have shown that in all epilepsy types, 5–10% of Caucasian patients will show a
Hr
Sleepstages
Generalized Epileptiform discharges Fig. 2. Relation between sleep stage and occurrence of generalized spike-and-wave discharges over a 24-h period in a 38-year-old untreated male patient with JME. Most discharges occurred upon awakening after a daytime nap and especially after a night sleep period. The total duration of spike-and-waves was 34 s. W is awake.
D.G.A. Kasteleijn- Nolst Trenité et al. / Epilepsy & Behavior 28 (2013) S25–S29
generalized photoparoxysmal EEG response (PPR) and that in Japan and India, only 1–2% of patients have a PPR [15–18]. In all countries, PPRs are found with a clear maximum at adolescence. It is, therefore, not surprising that PPRs and visual sensitivity in daily life are often seen and reported in patients with JME. In a study of 57 cases of JME [19], visual sensitivity was reported by 21 patients and confirmed with a PPR in 8 (14%) patients. Ten other patients with no clinical history of visual sensitivity exhibited a PPR to IPS. Thus, 31 of these patients (54.4%) had clinical or laboratory evidence of photosensitivity. While PPRs are more often found in IGE (60%) than in focal epilepsy (30%) compared with 15% IGE and 60% focal epilepsies in nonphotosensitive patients, matched for age and sex [16], the highest prevalence of PPR is found in JME. In studies on JME with photic stimulation performed and published around the world between 1984 and 2007, prevalence rates of PPR positive patients range from 5% to 90%. This difference in results can be explained by the differences in populations (ethnic origin, age, sex, and comedication) and methodology of IPS. When IPS is performed continuously for up to 5 min, a PPR was provoked in 90% of patients with JME [20]. An overview of the different studies is reported in Table 1 with reference numbers [6,19–29]. One of the reasons for differences in prevalence found is undoubtedly treatment and dosage of VPA, which is very effective in patients with a PPR [21]. Another factor might be the timing of the day of the EEG as has been observed by repeating the morning EEG the same day in the afternoon: 5 out of 8 PPR positive patients with JME lost their sensitivity in the afternoon [30]. Although knowing that patients with JME are having jerks mainly in the morning, this is, nevertheless, remarkable; firstly, because patients with JME with a PPR usually do not complain about a greater sensitivity to lights in the early morning, and secondly because in many studies over the past 20 years, with hourly photic stimulation during the day in patients with JME with a PPR, a similar overall effect has not been seen [31–33]. Specially designed prospective studies are necessary to unravel this contradiction in results. Photoparoxysmal response positive patients are predominantly of female sex (2/3), and interestingly indeed, only patients with JME with a PPR do show a sex difference [15]. Patients with a myoclonic type of epilepsy, either benign or progressive, have a high likelihood of being photosensitive. Similarly, during a generalized PPR in photosensitive patients, clinical symptoms were seen in at least 75%, by far the most common being myoclonic jerks [34,35]. Sleep deprivation increases both the likelihood of myoclonic seizures and photosensitivity [36]. This has been demonstrated also nicely by Janz and Christian and published in one of their first papers on JME [6]; a PPR could be elicited in a 35-year-old patient with JME, taking bromide, phenobarbital, and phenytoin, only after additional sleep deprivation and a quantity of beer.
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Other interesting findings on the relation between JME and photosensitivity are the following: • A lady with silent JME for 64 years showed a PPR and myoclonic jerks in the arms at the age of 74 [37]; • Patients with JME with a PPR do not have a predilection for personality disorders [38]; • Drug resistance in patients with JME is not dependent on whether they have a PPR or not [39]; • Likelihood of withdrawal seizures in patients with JME is independent of a PPR [29]. Thus, the prevalence rate of photosensitivity (PPR) in patients with JME, ranging from 8 to 90%, is seen more often in females and adolescents and depends on drug use. Since both JME and photosensitivity are connected with generalized types of epilepsy and myoclonus, the two traits are comorbid. 3.2. Modulation of the ictal and interictal activities by external factors other than photic stimulation Patients with JME often report that seizures are precipitated by external factors such as sleep deprivation, awakening, stress, fatigue, anticipation, alcohol intake, menstruation, and flashing lights [19,40,41]. In a long-term prospective study on 66 patients with JME, Panayiotopoulos et al. found that 93% of the patients had seizures precipitated by external factors [19]. Besides these general factors, patients also report that mental activities and motor activities requiring elaborate planning (“praxis induction”) can facilitate or inhibit seizure occurrence. Based on these clinical observations, several groups used test batteries specifically designed to address the external modulation of the ictal and interictal epileptiform activities (IEDs) during video-EEG recordings. 3.2.1. Provocative effect on the IEDs Matsuoka et al. investigated 480 patients using a test battery of “neuropsychological EEG activation” (NPA) including reading, speaking, writing, written arithmetic calculation, mental arithmetic calculation, and spatial construction [43]. They found provocative effects on the occurrence of IEDs in 38 patients (7.9%). It is remarkable that 36 out of the 38 patients showing this provocative feature had idiopathic generalized epilepsy. This phenomenon was observed most often among patients with JME: 22 out of 45 patients (46.7%) had IEDs provoked by a cognitive task. Most of the patients (32 out of 38) showed provocation induced by mental activities associated with use of the hands (“action programming”). These findings were reproduced by Guaranha et al. in a larger group of 76 patients with JME [44]. They found a provocative effect induced by cognitive tasks in 38.2% of the
Table 1 Prevalence of PPR found in different studies in different populations. % PPR in JME varies per country, time period, and population Author
Year
Country
Age range
F;M
AEDs
Type of IPS
PPR
Janz Delgado and Enrile-Bacsal Penry et al. Canevini et al. Panayatopoulos et al. Aliberti et al. Appleton et al.
1957 1984 1989 1992 1994 1994 2000
Germany USA West USA South-East Italy Saudi Arabia UK UK
14–55 15–69 18–46 15–55 8–40 15–41 7–16
24;23 20;33 34;16 40;20 33;33 17;5 35;26
Br, PB, PHT VPA, PB, PHT VPA VPA, PRM PHT, CBZ VPA None
Double flash + metrazol
Montalenti et al. Calleja et al. Dhanuka and Mahaswari et al. Jain et al. Sokic et al.
2001 2001 2001 2003 2007
Italy Spain India India Serbia
16–63 20–40 9–20 ? 11–51
38;25 15;7 8;7 292;208 62;43
VPA VPA None 80% VPA VPA 83%
Minimal 2?/41 (5%?) 8/50 (16%) 5/60 (8%) 18/66 (27%) 9/56 (40%) 55/61 (90%; 33% only after 4 min) 28/79 (36%) 9/22 (41%) 4/15 (26%) 42/500 (8%) 17/105 (16%)
Flash + pattern Flash + pattern Flash + pattern; 4 min partly sleep-deprived
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patients. Action programming tasks were more effective than thinking. Karachristianou et al. reported provocative effects of the neuropsychological tasks in 76.6% of the 30 patients with JME they tested [45, 47]. Mayer et al. investigated 25 patients with JME and 25 patients with focal epilepsy, using a modified version of the test battery of Matsuoka, with more emphasis on the linguistic tasks [46]. They observed provocative effects in 10 patients with JME (40%) versus only in 2 patients with focal epilepsy. As opposed to Matsuoka [5] and Guaranha, they found that a provocative effect was more often associated with reading and speaking as compared with praxis induction [46]. A possible explanation for this discordant finding is that they studied an enriched population of patients with JME who in a questionnaire had indicated the possible occurrence of perioral reflex myoclonia by praxis and language. Furthermore, the linguistic features specific to the Japanese written languages could have also contributed to this difference. In all these studies, provocation was arbitrarily defined as a twofold increase in the number of IEDs/min, compared with the unprovoked baseline period. However, this evens out the effects of the spontaneous fluctuation of the IEDs during the baseline period. To compensate for this bias, Beniczky et al., in a multicenter study on 60 patients with JME, recorded a longer, standardized baseline period of 50 min and determined the 95% confidence interval (CI) for the frequency of occurrence of the IEDs for each patient [48]. They compared the occurrence of the IEDs during cognitive tasks with this CI. Using this approach, the cognitive tasks had a provocative effect in 18% of the patients, suggesting that part of the provocative effect described in the previous publications might have been due to the spontaneous fluctuation of the IEDs. Several studies have compared the efficacy of the cognitive tasks with the conventional provocation methods. In a study on 25 patients with JME, Matsuoka et al. found that neuropsychological activation (84%) was more efficient than drowsiness (68%), hyperventilation (40%), and IPS (36%) [49]. Mayer et al. found similar results: cognitive tests (40%) versus hyperventilation (28%) and IPS (20%) [46]. Contrary to these, Guaranha et al. found that the conventional provocation methods were more efficient than the neuropsychological activation [6]. Sleep (58%) was the most efficient activation method followed by hyperventilation (39%) and IPS (30%) [44]. These diverging results could possibly be explained by the difference in the seizure frequency between the patient groups in these studies, as Beniczky et al. found that the conventional provocation methods tended to be more efficient in patients who were not seizure-free [48].
In the selected population of patients with JME studied by Mayer et al., perioral myoclonias induced by reading and speaking were recorded in 9 out of the 25 patients, while limb myoclonia induced by praxis were recorded in 2 patients [46]. These studies suggested that linguistic tasks induced perioral myoclonia, while action programming (or praxis) induced limb myoclonia. However, a recent study could not confirm this kind of strict association between the type of task (manual versus orofacial) and location of myoclonia [48]. Perioral myoclonias were observed in 3 patients: during language-related tests in the first patient, during action-programming tests in the second patient, and during both types in the third patient. Upper limb myoclonia (recorded in 6 patients) was also observed during both of these testgroups (language-related tasks: 3 patients and action-programming tests: 2 patients). Two studies found that myoclonias were more often induced by cognitive tasks than the conventional provocation methods, while absence was most often induced during hyperventilation [38,42]. 5. Conclusion Chronodependency (a strong relationship between the seizures and specific time of the day, such as awakening in the morning) and sleep deprivation are the major determinants of seizures and of IEDs in JME. Besides IPS, IEDs can be facilitated in a significant number of patients by other activation methods, including hyperventilation and cognitive tasks. Inhibition of IEDs by cognitive tasks is a non-specific phenomenon probably related to attention. Cognitive tasks are efficient in precipitating myoclonic seizures, while hyperventilation can induce absence seizures in patients with JME. This knowledge must be used for the diagnosis and management of patients with JME. We, therefore, advise to recording EEGs in every patient suspected of having JME in the early morning with standardized IPS after hyperventilation. In those cases where the diagnosis remains unclear, we advise to recording EEG after sleep deprivation and adding surface EMG electrodes; this means a minimum of 30 min of sleep recording followed by provoked awakening and IPS, hyperventilation, and cognitive tasks, including reading, writing, speaking, and praxis. Conflict of interest statement The authors declare that there are no conflicts of interest. References
3.2.2. Inhibitory effect on the IEDs Studies aimed at assessing the provocative effect of cognitive tasks surprisingly found a high incidence (64–90%) of inhibitory effects associated with these tasks [43,44,50] and also with the conventional provocation methods [44]. These studies arbitrarily defined inhibition as >50% decrease in the frequency of IED occurrence, as compared with the baseline. However, when compensating for the spontaneous fluctuation of the IEDs, the incidence of inhibition associated with cognitive tasks was much lower (29%) [48]. Furthermore, as opposed to the provocative effect, the inhibitory one was not task-specific and probably related to a global cognitive activation or attention [48]. This is also supported by the high incidence of inhibitory effects found among patients with other types of epilepsy [43]. 4. Precipitation of seizures Neuropsychological activation proved to be efficient in precipitating seizures. Matsuoka et al. found absence seizures precipitated in 8 patients and myoclonia induced in 15 out of the 38 patients who had provocative effects on the IEDs [43]. Myoclonias usually involved the upper limbs and were precipitated by mental activities associated with use of the hands (“action programming”).
[1] Pavlova MK, Shea SA, Bromfield EB. Day/night patterns of focal seizures. Epilepsy Behav 2004;5:44–9. [2] Hofstra WA, Grootemarsink BE, Dieker R, van der Palen J, de Weerd AW. Temporal distribution of clinical seizures over the 24 hour day. Epilepsia 2009;50:2019–26. [3] Hofstra WA, Spetgens W, Leijten FSS, et al. Diurnal rhythms in seizures detected by intracranial ECoG-monitoring. Epilepsy Behav 2009;14:617–21. [4] Loddenkemper T, Vendrame M, Zarowski M, et al. Circadian patterns of pediatric seizures. Neurology 2011;76:145–53. [5] Zarowski M, Loddenkemper T, Vendrame M, Alexopoulos AV, Wyllie E, Kothare SV. Circadian distribution and sleep/wake patterns of generalized seizures in children. Epilepsia 2011;52:1076–83. [6] Janz D, Christian W. Impulsive petit mal. Dtsch Z Nervenheilkd 1957;176:346–86. [7] Horne JA, Ostberg O. A self-assessment questionnaire to determine morningness– eveningness in human circadian rhythms. Int J Chronobiol 1976;4:97–110. [8] Roenneberg T, Kuehnle T, Juda M, et al. Epidemiology of the human circadian clock. Sleep Med Rev 2007;11:429–38. [9] Pung T, Schmitz B. Circadian rhythm and personality profile in juvenile myoclonus epilepsy. Epilepsia 2006;47(Suppl. 2):111–4. [10] Hofstra WA, Gordijn MCM, van Hemert-van der Poel JC, van der Palen J, de Weerd AW. Chronotypes and sleep preferences in epilepsy patients. Chronobiol Int 2010;27:1271–86. [11] Frucht MM, Quigg M, Schwaner C, Fountain NB. Distribution of seizure precipitants among epilepsy syndromes. Epilepsia 2000;41(12):1534–9. [12] Nakken KO, Solaas MH, Kjeldsen MJ, Friis ML, Pellock JM, Corey LA. Which seizure-precipitating factors do patients with epilepsy most frequently report? Epilepsy Behav 2005;6:l85–l189. [13] Fang PC, Chen YJ, Lee IC, Dev Brain. Seizure precipitants in children with intractable epilepsy. Brain Dev 2008;30(8):527–32.
D.G.A. Kasteleijn- Nolst Trenité et al. / Epilepsy & Behavior 28 (2013) S25–S29 [14] da Silva Sousa P, Lin K, Garzon E, Sakamoto AC, Yacubian EM. Self-perception of factors that precipitate or inhibit seizures in juvenile myoclonic epilepsy. Seizure 2005;14(5):340–6. [15] Wolf P, Goosses R. Relation of photosensitivity to epileptic syndromes. J Neurol Neurosurg Psychiatry 1986;49:1386–91. [16] Kasteleijn-Nolst Trenité DGA. Photosensitivity in epilepsy: electrophysiological and clinical correlates. Acta Neurol Scand 1989;80(S25):1–150. [17] Saleem SM, Thomas M, Jain S, Maheshwari MC. Incidence of photosensitive epilepsy in unselected Indian epileptic population. Acta Neurol Scand 1994;89:5–8. [18] Shiraishi H, Fujiwara T, Inoue Y, Yagi K. Photosensitivity in relation to epileptic syndromes: a survey from an epilepsy center in Japan. Epilepsia 2001;42:393–7. [19] Panayiotopoulos CP, Obeid T, Tahan AR. Juvenile myoclonic epilepsy: a 5-year prospective study. Epilepsia 1994;35(2):285–96. [20] Appleton R, Beirne M, Acomb B. Photosensitivity in juvenile myoclonic epilepsy. Seizure 2000;9:108–11. [21] Jain S, Tripathi M, Srivastava AK, Narula A. Phenotypic analysis of juvenile myoclonic epilepsy in Indian families. Acta Neurol Scand 2003;107(5):356–62. [22] Delgado-Escueta AV, Enrile-Bacsal F. Juvenile myoclonic epilepsy of Janz. Neurology 1984;34(3):285–94. [23] Penry JK, Dean JC, Riela AR. Juvenile myoclonic epilepsy: long-term response to therapy. Epilepsia 1989;30(S4):S19–23. [24] Canevini MP, Mai R, Di Marco C, Bertin C, Minotti L, Pontrelli V, Saltarelli A, Canger R. Juvenile myoclonic epilepsy of Janz: clinical observations in 60 patients. Seizure 1992;1(4):291–8. [25] Aliberti V, Grünewald RA, Panayiotopoulos CP, Chroni E. Focal electroencephalographic abnormalities in juvenile myoclonic epilepsy. Epilepsia 1994;35(2):297–301. [26] Montalenti E, Imperiale D, Rovera A, Bergamasco B, Benna P. Clinical features, EEG findings and diagnostic pitfalls in juvenile myoclonic epilepsy: a series of 63 patients. J Neurol Sci 2001;15,184(1):65–70. [27] Calleja S, Salas-Puig J, Ribacoba R, Lahoz CH. Evolution of juvenile myoclonic epilepsy treated from the outset with sodium valproate. Seizure 2001;10(6):424–7. [28] Dhanuka AK, Jain BK, Daljit S, Maheshwari D. Juvenile myoclonic epilepsy: a clinical and sleep EEG study. Seizure 2001;10(5):374–8. [29] Sokic D, Ristic AJ, Vojvodic N, Jankovic S, Sindjelic AR. Frequency, causes and phenomenology of late seizure recurrence in patients with juvenile myoclonic epilepsy after a long period of remission. Seizure 2007 Sep;16(6):533–7. [30] Labate A, Ambrosio R, Gambardella A, Stumioli M, Pucci F, Quattrone A. Usefulness of a morning routine EEG recording in patients with myoclonic epilepsy. Epilepsy Res 2007;77(1):17–21. [31] Binnie CD, Kasteleijn-Nolst Trenite DGA, de Korte R. Photosensitivity as a model for acute antiepileptic drug studies. Electroencephalogr Clin Neurophysiol 1986;63:35–41. [32] Kasteleijn-Nolst Trenité D, Genton P, Parain D, Masnou P, Steinhoff BJ, Jacobs T, Pigeolet E, Stockis A, Hirsch E. Evaluation of brivaracetam, a novel SV2A ligand, in the photosensitivity model. Neurology 2007;69:1027–34. [33] Kasteleijn- Nolst Trenité DGA, Marescaux C, Stodieck S, Edelbroek PM, Oosting J. Photosensitive epilepsy: a model to study the effects of antiepileptic drugs.
[34]
[35]
[36] [37] [38]
[39] [40]
[41] [42]
[43]
[44]
[45] [46] [47]
[48]
[49] [50]
S29
Evaluation of the piracetam analogue levetiracetam. Epilepsy Res 1996;25(3): 225–30. Kasteleijn-Nolst Trenité DGA, Binnie CD, Meinardi H. Photosensitive patients: symptoms and signs during intermittent photic stimulation and their relation to seizures in daily life. J Neurol Neurosurg Psychiatry 1987;50:1546–9. Piccioli M, Ricci S, Vigevano F, Buttinelli C, Kasteleijn-Nolst Trenité DGA. Visual sensitive children: symptoms and signs during intermittent photic stimulation and video game playing. Epilepsia 2003;44(S9):307. Scollo-Lavizzari G, Scollo-Lavizzari GR. Sleep, sleep deprivation, photosensitivity and epilepsy. Eur Neurol 1974;11:1–21. Jacob S, Martin D, Rajabally YA. Juvenile myoclonic epilepsy in an elderly patient. Age Ageing 2006;35:194–6. De Araujo Filho GM, Lin K, Lin G, Peruchi MM, Caboclo LOSF, Guaranha MSB, Guilhoto LMFF. Are personality traits of juvenile myoclonic epilepsy related to frontal lobe dysfunctions? A proton MRS study. Epilepsia 2009;50(5):1201–9. Gélisse P, Genton P, Samuelian JC, Thomas P, Bureau M. Psychiatric disorders in juvenile myoclonic epilepsy. Rev Neurol (Paris) 2001;157(3):297–302. Janz D, Durner M. Juvenile myoclonic epilepsy. In: Engel Jr J, Pedley TA, editors. Epilepsy: a comprehensive textbook. Philadelphia: Lippincott-Raven Press; 1998. p. 2389–400. Fenwick PB. Self-generation of seizures by an action of mind. Adv Neurol 1998;75: 87–92. Inoue Y, Kubota H. Juvenile myoclonic epilepsy with praxis induced seizures. In: Schmitz B, Sander T, editors. Juvenile myoclonic epilepsy: the Janz syndrome. Petersfield: Wrightson Biomedical Publishing Ltd; 2000. p. 73–81. Matsuoka H, Takahashi T, Sasaki M, Matsumoto K, Yoshida S, Numachi Y, Saito H, Ueno T, Sato M. Neuropsychological EEG activation in patients with epilepsy. Brain 2000;123:318–30. Guaranha MS, da Silva Sousa P, de Araújo-Filho GM, Lin K, Guilhoto LM, Caboclo LO, Yacubian EM. Provocative and inhibitory effects of a video-EEG neuropsychologic protocol in juvenile myoclonic epilepsy. Epilepsia 2009;50:2446–55. Karachristianou S, Bostantjopoulou S, Katsarou Z, Kazis A. Neuropsychological EEG activation in patients with juvenile myoclonic epilepsy. Funct Neurol 2004;19:185–9. Mayer TA, Schroeder F, May TW, Wolf PT. Perioral reflex myoclonias: a controlled study in patients with JME and focal epilepsies. Epilepsia 2006;47:1059–67. Wolf P. Reading epilepsy. In: Roger J, Bureau M, Dravet C, Dreifuss FE, Perret A, Wolf P, editors. Epileptic syndromes in infancy, childhood and adolescence. 2nd edition. London: John Libbey; 1992. p. 281–98. Beniczky S, Guaranha MSB, Conradsen I, Singh M, Rutar V, Lorber B, Braga P, Bogacz Fressola A, Inoue Y, Targas Yacubian EM, Wolf P. Modulation of epileptiform EEG discharges in juvenile myoclonic epilepsy: an investigation of reflex epileptic traits. Epilepsia 2012. http://dx.doi.org/10.1111/j.1528-1167.2012.03454.x. Matsuoka H, Takahashi T, Sato M. The clinical and electroencephalographic studies of juvenile myoclonic epilepsy. Jpn J Psychiatry Neurol 1988;42:556–7. Matsuoka H, Nakamura M, Ohno T, Shimabukuro J, Suzuki T, Numachi Y, Awata S. The role of cognitive-motor function in precipitation and inhibition of epileptic seizures. Epilepsia 2005;46(Suppl. 1):17–20.