Epilepsia, 16:497-501,1975. Raven Press, New York
EEG of a Nocturnal Seizure in a Patient with “Benign Epilepsy of Childhood with Rolandic Spikes” B. Dalla Bernardina and C. A. Tassinari Clinica Pediatrica Universita di Verona, Borgo Roma, Verona, Italy, and I.N.S.E.R.M. and Centre Saint Paul, 280-300, Boulevard Sainte Marguerite, 13009 Marseilles, France
(Received April 1, 1975) Benign epilepsy of childhood with Rolandic (or midtemporal) spikes constitutes a well-defined clinical and EEG syndrome. Usually infrequent and partial, the seizures occur during childhood and disappear during puberty. The interictal EEG shows spikes or spike-waves, or both, involving the Rolandic or midtemporal region on one side. To the best of our knowledge no seizure has been recorded by electroencephalography. We are reporting the clinical and EEG features of a seizure during sleep in a child with typical “benign epilepsy of childhood with Rolandic spikes.” chse report. A 10-year-old boy was referred to the Pediatric Clinic because of partial and generalized seizures during nocturnal sleep. The first partial seizure occurred at the age of 8.5 years and the second at 9.5 year. Since then seizures have occurred every 3 weeks, always during nocturnal sleep. The mother described twitches of the right face lasting about 1 min with deviation of the mouth to the right and hypersalivation. If the child was wakened, consciousness seemed somewhat impaired during the seizure, and for a few minutes after the seizure he could not answer questions. There was no postictal motor deficit. Generalized tonic-clonic seizures occurred twice during sleep, one at 9.5 years and the other a few days before admission. Repeated interictal EEGs
with the child awake showed spikes over the left hemisphere, maximal over the central and midtemporal regions. Dipropylacetic acid (Depakinea) was given t.i.d. during the last 6 months. Neurological examination and routine laboratory tests were normal. The EEG (child awake) showed normal background activity posteriorly with mediumto high-voltage isolated spikes maximal over the left central and midtemporal regions, sometimes spreading to homologous regions on the right (Fig. 1). The frequency of spikes was 9/min (histogram, Fig. 2), and the spikes were not modified by opening the eyes, hyperventilation or intermittent light stimulation. During nocturnal sleep the EEG showed normal sleep phases (Fig. 2), and the physiological sleep patterns (spindles, K complexes, sharp waves at the vertex) were symmetrical. Interictal abnormalities were significantly increased during slow sleep: spikes/min (histogram, Fig. 2) increased from a mean of 9/min to 37/min during stage I, 49/min during stage 11, and 55/min during stages 111 and IV. During REM sleep the spikes averaged 39/min. During slow sleep the spikes spread t o the left hemisphere and t o contralateral regions, and at times they were associated with slow waves to give the appearance of spike-and-wave discharges. During REM sleep the spikes were localized and appeared as when the child was awake (Fig. 1). A spontaneous seizure occurred early in the Key words: Epilepsy - Benign childhood epilepsy - Rolandic spikes -Nocturnal seizure morning, during stage I1 of sleep as indicated by re cording. the arrow on the histogram (Fig. 2). At the 497
B. DALLA BERNARDINA AND C. A. TASSINARI
498
onset of the seizure (Fig. 3, top) the EEG showed low voltage fast activity (12 Hz) maximal over the left temporal and centroparietal regions, which spread after a few seconds to the left anterior and midline regions. The amplitude then increased from 20 to 30 pV to 50 to 100 pV. After about 20 sec this spike activity spread to the right temporal regions. The discharge then appeared as diffuse rhythmic spikes at 9 to 10 Hz (Fig. 3, middle sample, left) which slowed to a regular 8 Hz rhythm and then ended abruptly (Fig. 3, bottom left). There was no postictal focal slowing. Spikes reappeared 1 min after the end of the discharge (Fig. 3, bottom right). The seizure was subclinical at the onset (Fig. 3, top); then myoclonias of the right face
occurred as shown by 8 Hz activity in the right temporal muscles recorded by EMG. The mouth remained closed, probably because of contraction of the jaw muscles as evidenced by bitemporal tonic EMG activity. EMG recording of the extensor of the right wrist showed that the arms were not involved. The seizure did not awaken the patient, nor was he aware next day that he had had a seizure. DISCUSSION The clinical features of the seizures of “benign epilepsy of childhood with Rolandic spikes” have been described on the basis of information from patients and their parents and 81. I
LES. L...
10
VR8.
CPV
471Sl_U_-_
21.11.74
FIG. 1. Shows the focal interictal spikes when the child was awake and the changes during the various stages of sleep (see text). Calibration: 100 pV and 1sec,
499
EEG SEIZURE IN “BENIGN EPILEPSY* witnesses, and the “signs” in 275 seizures of 190 patients (Loiseau and Beaussart, 1973; Beaussart and Loiseau, 1973) are in good agreement with findings of other authors (Lombroso, 1967, Aicardi and Chevrie, 1969; Gibbs and Gibbs, 1970; Blom et al., 1972). EEGs have been recorded while the patients were awake and asleep by conventional techniques (Blom and Heijbel, 1975) and by protracted telemetric recordings (Beaumanoir et al., 1974). Nonetheless, and despite the fact that benign epilepsy of childhood is at least as frequent as typical petit ma1 absences (Beaussart et al., 1970), no EEG recorded during a seizure has been reported hitherto, probably because the seizures are infrequent and usually nocturnal. As found by Beaussart and Loiseau (1973) the seizures of benign epilepsy of childhood with Rolandic spikes are nearly always nocturnal, usually partial tonic-clonic seizures involving the faciobrachial musculature, or
W I
generalized, which account for 75% of the seizures. Other seizures, usually diurnal, involve only the facial muscles of one side. The seizure we recorded belongs to this second group since only the facial muscles were involved. Since it occurred during sleep and would not have come to the notice of the parents, it seems likely that such seizures occur much more often than the histories show, and that they are not in fact mainly diurnal. Our case is the first report of an EEG recording during a seizure. Although there were only two pairs of electrodes over the anterior and midtemporal regions of the right hemisphere, the ictal discharge was probably focal at the onset, beginning in the left hemisphere over the centro-temporal regions, then spreading to the whole left and finally to the right hemisphere. At the onset of the seizure, the EEG showed low voltage fast activity confined to a limited area, in good agreement with the hypothesis of Loiseau and Beaussart (1973).
l
-
U
Jl
%
I
=16
II
= 32.4 %
Ill4V = 26.6 %
Ill-IV
REM = 20.6 %
RIM I
h. 23
LES. L... 10 Y C. P. V.
~ S .
4718/74
I
I
I
I
I
W
I
I1
Ill-IV
REM
FIG. 2. Top: Histogram of the EEG during sleep showing a normal deep pattern and the time when the spontaneous seizure began. Bottom: Mean number of spikeslmin (RS/m) while the child was awake (w)and during the stages of sleep.
B. DALLA BERNARDINA AND C. A. TASSINARI
500
that “the signs,” i.e., the components of seizures of benign epilepsy with Rolandic spikes, “can be explained as due to activation of the Rolandic fissure, particularly the inferior portion, that is just above the Sylvian fissure.” Beaumanoir et al. (1974) recorded generalized 3 Hz spike-and-wavedischarges in children with this syndrome, suggesting that benign epilepsy of childhood with Rolandic spikes and primary generalized epilepsy, petit mal or grand mal, may be related. Furthermore unilateral jerks (hemiclonic seizures?) have been reported to occur (7%) (Beau& et al., 1970; Loiseau and B e a u W , 1973), which sometimes can be
us. L...
10
YRS.
c
PV
4718174
a form of generalized epilepsy with generalized or predominantly unilateral EEG discharges (Gastaut et al., 1974). In addition and probably most importantly Heijbel et al. (1975) reported that “the EEG trait (i.e., Rolandic or centro-temporal spikes) is genetically determined with an age-dependent penetrance and a mode of inheritance like that of centrencephalic seizures such as petit mal absences with 3Isec spike-and-waveactivity.” Recordings of .seizures and particularly those of the “generalized” or “hemiconvulsive” type in typical cases of benign epilepsy of childhood could thus help to establish the eventual
21 11 74
FIG. 3. Spontaneous partial seizure during stage I1 of sleep. The first two records and that at the bottom left are continuous. The record at the bottom right is 1 min after the end of the seizure (see text). Calibration: 1OOpV and 1 sec.
EE G SEIZURE IN “BENIGN EPILEB Y” nosological relationships between the “benign epilepsy of childhood” and the primarily generalized epilepsies.
501
REFERENCES
Aicardi J and Chevrie JJ. Epilepsie partielle avec foyer rolandique de la seconde enfance. In: JournZes Parisiennes de Pgdiatrie. Editions MBdicales Flammarion, Paris, 1969, pp. 125-142. The f i t EEG recording is reported of a child with “benign epilepsy of childhood with Beaumanoir A, Ballis T, Varfis G and Ansari K. Benign epilepsy of childhood with Rolandic Rolandic spikes” during a partial motor (facial) spikes. Epilepsia 15:301-315,1974. seizure, which occurred during Phase 11 of Beaussart M, Beaussart-Boulange L and Mahieu natural sleep. N. L’6pilepsie avec paroxysmes EEG rolandiques. Une nouvelle forme d’pilepsie a ne plus ignorer. Concours Med 10:21 95-2212, 1970. Beaussart M and hiseau P. Evolution et Les auteurs pr6sentent le premier enregistrepronostic de I’Bpilepsie a paroxysmes rolanment EEG d’une crise motrice partielle (faciale) diques. In: E Lugaresi, P Pazzaglia, and CA suvenant spontanement au couni du sommeil Tassinari (Eds), Symposium International dans un cas d’6pilepsie b6nigne de l’enfance sur I’Evolution et le Pronostic des Epilepsies. avec pointes Rolandiques. Gaggi, Bologna, 1973,pp 215-228. Blom S and Heijbel J. Benign epilepsy of children with centro-temporal EEG foci. RESUMEN Discharge rate during sleep. Epilepsia 16:133-140,1975. Se publica el primer trazado electroencef- Blom S, Heijbel J and Bergfors PG. Benign alogrlfico de un niiio con “epilepsia benigna de epilepsy of children with centro-temporal la infancia con puntas Rolhdicas” durante un EEG foci. Prevalence and follow-up study of ataque parcial motor (cara) que ocurrii, en la 40 patients. Epilepsia 13:609-619,1972. fase I1 del suefio espontlneo. Gastaut H, Broughton R, Tassinari CA and Roger J. Unilateral epileptic seizures. In: PJ (A. Portera Sanchez, Madrid) Vinken and GW Bruyn (Eds), Handbook of Clinical Neurology, Vol. 15. North Holland Publishing Co., Amsterdam, 1974, pp. ZUSAMMENFASSUNG 235-245. Gibbs FA and Gibbs EL. Clinical correlates and Bericht uber die 1. EEG-Ableitung von prognostic significance of various types of einem Kind mit “benigner Epilepsie mit midtemporal spike focus. Clinical ElectroenRolandischen Spitzen” wiihrend eines partiellen cepha lography 1:45-64,1970. motorischen (facialen) Anfalles, der im Stadium Heijbel J, Blom S and Rasmuson M. Benign I1 des natiirlichen Schlafes auftrat. epilepsy of childhood with centro-temporal EEG foci. A genetic study. Epilepsia, 1975 (D. Scheffner, Heidelberg) (in press). hiseau P and Beaussart M. The seizures of benign epilepsy with Rolandic paroxysmal ACKNOWLEDGMENT discharges. Epilepsia 14:381-389,1973. Lombroso CT. Sylvian seizures and midtemThe authors are indebted to R. de Battisti poral spike foci in children. Arch Neurol for his technical assistance. 17:52-59,1967. SUMMARY
EEG of a Nocturnal Seizure in a Patient with “Benign Epilepsy of Childhood with Rolandic Spikes” B. Dalla Bernardina and C. A. Tassinari Clinica Pediatrica Universita di Verona, Borgo Roma, Verona, Italy, and I.N.S.E.R.M. and Centre Saint Paul, 280-300, Boulevard Sainte Marguerite, 13009 Marseilles, France
(Received April 1, 1975) Benign epilepsy of childhood with Rolandic (or midtemporal) spikes constitutes a well-defined clinical and EEG syndrome. Usually infrequent and partial, the seizures occur during childhood and disappear during puberty. The interictal EEG shows spikes or spike-waves, or both, involving the Rolandic or midtemporal region on one side. To the best of our knowledge no seizure has been recorded by electroencephalography. We are reporting the clinical and EEG features of a seizure during sleep in a child with typical “benign epilepsy of childhood with Rolandic spikes.” chse report. A 10-year-old boy was referred to the Pediatric Clinic because of partial and generalized seizures during nocturnal sleep. The first partial seizure occurred at the age of 8.5 years and the second at 9.5 year. Since then seizures have occurred every 3 weeks, always during nocturnal sleep. The mother described twitches of the right face lasting about 1 min with deviation of the mouth to the right and hypersalivation. If the child was wakened, consciousness seemed somewhat impaired during the seizure, and for a few minutes after the seizure he could not answer questions. There was no postictal motor deficit. Generalized tonic-clonic seizures occurred twice during sleep, one at 9.5 years and the other a few days before admission. Repeated interictal EEGs
with the child awake showed spikes over the left hemisphere, maximal over the central and midtemporal regions. Dipropylacetic acid (Depakinea) was given t.i.d. during the last 6 months. Neurological examination and routine laboratory tests were normal. The EEG (child awake) showed normal background activity posteriorly with mediumto high-voltage isolated spikes maximal over the left central and midtemporal regions, sometimes spreading to homologous regions on the right (Fig. 1). The frequency of spikes was 9/min (histogram, Fig. 2), and the spikes were not modified by opening the eyes, hyperventilation or intermittent light stimulation. During nocturnal sleep the EEG showed normal sleep phases (Fig. 2), and the physiological sleep patterns (spindles, K complexes, sharp waves at the vertex) were symmetrical. Interictal abnormalities were significantly increased during slow sleep: spikes/min (histogram, Fig. 2) increased from a mean of 9/min to 37/min during stage I, 49/min during stage 11, and 55/min during stages 111 and IV. During REM sleep the spikes averaged 39/min. During slow sleep the spikes spread t o the left hemisphere and t o contralateral regions, and at times they were associated with slow waves to give the appearance of spike-and-wave discharges. During REM sleep the spikes were localized and appeared as when the child was awake (Fig. 1). A spontaneous seizure occurred early in the Key words: Epilepsy - Benign childhood epilepsy - Rolandic spikes -Nocturnal seizure morning, during stage I1 of sleep as indicated by re cording. the arrow on the histogram (Fig. 2). At the 497
B. DALLA BERNARDINA AND C. A. TASSINARI
498
onset of the seizure (Fig. 3, top) the EEG showed low voltage fast activity (12 Hz) maximal over the left temporal and centroparietal regions, which spread after a few seconds to the left anterior and midline regions. The amplitude then increased from 20 to 30 pV to 50 to 100 pV. After about 20 sec this spike activity spread to the right temporal regions. The discharge then appeared as diffuse rhythmic spikes at 9 to 10 Hz (Fig. 3, middle sample, left) which slowed to a regular 8 Hz rhythm and then ended abruptly (Fig. 3, bottom left). There was no postictal focal slowing. Spikes reappeared 1 min after the end of the discharge (Fig. 3, bottom right). The seizure was subclinical at the onset (Fig. 3, top); then myoclonias of the right face
occurred as shown by 8 Hz activity in the right temporal muscles recorded by EMG. The mouth remained closed, probably because of contraction of the jaw muscles as evidenced by bitemporal tonic EMG activity. EMG recording of the extensor of the right wrist showed that the arms were not involved. The seizure did not awaken the patient, nor was he aware next day that he had had a seizure. DISCUSSION The clinical features of the seizures of “benign epilepsy of childhood with Rolandic spikes” have been described on the basis of information from patients and their parents and 81. I
LES. L...
10
VR8.
CPV
471Sl_U_-_
21.11.74
FIG. 1. Shows the focal interictal spikes when the child was awake and the changes during the various stages of sleep (see text). Calibration: 100 pV and 1sec,
499
EEG SEIZURE IN “BENIGN EPILEPSY* witnesses, and the “signs” in 275 seizures of 190 patients (Loiseau and Beaussart, 1973; Beaussart and Loiseau, 1973) are in good agreement with findings of other authors (Lombroso, 1967, Aicardi and Chevrie, 1969; Gibbs and Gibbs, 1970; Blom et al., 1972). EEGs have been recorded while the patients were awake and asleep by conventional techniques (Blom and Heijbel, 1975) and by protracted telemetric recordings (Beaumanoir et al., 1974). Nonetheless, and despite the fact that benign epilepsy of childhood is at least as frequent as typical petit ma1 absences (Beaussart et al., 1970), no EEG recorded during a seizure has been reported hitherto, probably because the seizures are infrequent and usually nocturnal. As found by Beaussart and Loiseau (1973) the seizures of benign epilepsy of childhood with Rolandic spikes are nearly always nocturnal, usually partial tonic-clonic seizures involving the faciobrachial musculature, or
W I
generalized, which account for 75% of the seizures. Other seizures, usually diurnal, involve only the facial muscles of one side. The seizure we recorded belongs to this second group since only the facial muscles were involved. Since it occurred during sleep and would not have come to the notice of the parents, it seems likely that such seizures occur much more often than the histories show, and that they are not in fact mainly diurnal. Our case is the first report of an EEG recording during a seizure. Although there were only two pairs of electrodes over the anterior and midtemporal regions of the right hemisphere, the ictal discharge was probably focal at the onset, beginning in the left hemisphere over the centro-temporal regions, then spreading to the whole left and finally to the right hemisphere. At the onset of the seizure, the EEG showed low voltage fast activity confined to a limited area, in good agreement with the hypothesis of Loiseau and Beaussart (1973).
l
-
U
Jl
%
I
=16
II
= 32.4 %
Ill4V = 26.6 %
Ill-IV
REM = 20.6 %
RIM I
h. 23
LES. L... 10 Y C. P. V.
~ S .
4718/74
I
I
I
I
I
W
I
I1
Ill-IV
REM
FIG. 2. Top: Histogram of the EEG during sleep showing a normal deep pattern and the time when the spontaneous seizure began. Bottom: Mean number of spikeslmin (RS/m) while the child was awake (w)and during the stages of sleep.
B. DALLA BERNARDINA AND C. A. TASSINARI
500
that “the signs,” i.e., the components of seizures of benign epilepsy with Rolandic spikes, “can be explained as due to activation of the Rolandic fissure, particularly the inferior portion, that is just above the Sylvian fissure.” Beaumanoir et al. (1974) recorded generalized 3 Hz spike-and-wavedischarges in children with this syndrome, suggesting that benign epilepsy of childhood with Rolandic spikes and primary generalized epilepsy, petit mal or grand mal, may be related. Furthermore unilateral jerks (hemiclonic seizures?) have been reported to occur (7%) (Beau& et al., 1970; Loiseau and B e a u W , 1973), which sometimes can be
us. L...
10
YRS.
c
PV
4718174
a form of generalized epilepsy with generalized or predominantly unilateral EEG discharges (Gastaut et al., 1974). In addition and probably most importantly Heijbel et al. (1975) reported that “the EEG trait (i.e., Rolandic or centro-temporal spikes) is genetically determined with an age-dependent penetrance and a mode of inheritance like that of centrencephalic seizures such as petit mal absences with 3Isec spike-and-waveactivity.” Recordings of .seizures and particularly those of the “generalized” or “hemiconvulsive” type in typical cases of benign epilepsy of childhood could thus help to establish the eventual
21 11 74
FIG. 3. Spontaneous partial seizure during stage I1 of sleep. The first two records and that at the bottom left are continuous. The record at the bottom right is 1 min after the end of the seizure (see text). Calibration: 1OOpV and 1 sec.
EE G SEIZURE IN “BENIGN EPILEB Y” nosological relationships between the “benign epilepsy of childhood” and the primarily generalized epilepsies.
501
REFERENCES
Aicardi J and Chevrie JJ. Epilepsie partielle avec foyer rolandique de la seconde enfance. In: JournZes Parisiennes de Pgdiatrie. Editions MBdicales Flammarion, Paris, 1969, pp. 125-142. The f i t EEG recording is reported of a child with “benign epilepsy of childhood with Beaumanoir A, Ballis T, Varfis G and Ansari K. Benign epilepsy of childhood with Rolandic Rolandic spikes” during a partial motor (facial) spikes. Epilepsia 15:301-315,1974. seizure, which occurred during Phase 11 of Beaussart M, Beaussart-Boulange L and Mahieu natural sleep. N. L’6pilepsie avec paroxysmes EEG rolandiques. Une nouvelle forme d’pilepsie a ne plus ignorer. Concours Med 10:21 95-2212, 1970. Beaussart M and hiseau P. Evolution et Les auteurs pr6sentent le premier enregistrepronostic de I’Bpilepsie a paroxysmes rolanment EEG d’une crise motrice partielle (faciale) diques. In: E Lugaresi, P Pazzaglia, and CA suvenant spontanement au couni du sommeil Tassinari (Eds), Symposium International dans un cas d’6pilepsie b6nigne de l’enfance sur I’Evolution et le Pronostic des Epilepsies. avec pointes Rolandiques. Gaggi, Bologna, 1973,pp 215-228. Blom S and Heijbel J. Benign epilepsy of children with centro-temporal EEG foci. RESUMEN Discharge rate during sleep. Epilepsia 16:133-140,1975. Se publica el primer trazado electroencef- Blom S, Heijbel J and Bergfors PG. Benign alogrlfico de un niiio con “epilepsia benigna de epilepsy of children with centro-temporal la infancia con puntas Rolhdicas” durante un EEG foci. Prevalence and follow-up study of ataque parcial motor (cara) que ocurrii, en la 40 patients. Epilepsia 13:609-619,1972. fase I1 del suefio espontlneo. Gastaut H, Broughton R, Tassinari CA and Roger J. Unilateral epileptic seizures. In: PJ (A. Portera Sanchez, Madrid) Vinken and GW Bruyn (Eds), Handbook of Clinical Neurology, Vol. 15. North Holland Publishing Co., Amsterdam, 1974, pp. ZUSAMMENFASSUNG 235-245. Gibbs FA and Gibbs EL. Clinical correlates and Bericht uber die 1. EEG-Ableitung von prognostic significance of various types of einem Kind mit “benigner Epilepsie mit midtemporal spike focus. Clinical ElectroenRolandischen Spitzen” wiihrend eines partiellen cepha lography 1:45-64,1970. motorischen (facialen) Anfalles, der im Stadium Heijbel J, Blom S and Rasmuson M. Benign I1 des natiirlichen Schlafes auftrat. epilepsy of childhood with centro-temporal EEG foci. A genetic study. Epilepsia, 1975 (D. Scheffner, Heidelberg) (in press). hiseau P and Beaussart M. The seizures of benign epilepsy with Rolandic paroxysmal ACKNOWLEDGMENT discharges. Epilepsia 14:381-389,1973. Lombroso CT. Sylvian seizures and midtemThe authors are indebted to R. de Battisti poral spike foci in children. Arch Neurol for his technical assistance. 17:52-59,1967. SUMMARY
