Electroencephalographic features of epileptic drop attacks and absence seizures: a case study

Brain & Development, 15 (1993) 226-230 0387-7604/93/$06.00 © 1993 Elsevier Science Publishers B.V. All rights reserved BRADEV 00025

Case Reports

Electroencephalographic features of epileptic drop attacks and absence seizures: a case study Hirokazu Oguni, MD, Yuichi Imaizumi, MD, Takashi Uehara, MD, Miyako Oguni, MD and Yukio Fukuyama, MD Department of Pediatrics, Tokyo Women's Medical College, 8-1 Kawada-cho, Shinjuku-ku, Tokyo, Japan Received 24 August 1992; accepted 21 December 1992 A study of epileptic drop attacks (EDA) by simultaneous video-polygraphic recordings was carried out in one epileptic patient with myoclonic astatic seizures (Doose syndrome). EDA was shown to correspond to a burst of generalized bilaterally synchronous spike and wave complexes (GBSSW) at 3 Hz. Absence seizures were also observed with a burst of GBSSW with similar characteristics. The amplitudes of the corresponding slow wave component of GBSSW among the three intensities of atonia, i.e. complete atonia, minor atonia and no discernible atonia (control), was compared. A high amplitude was demonstrated to correspond with more pronounced atonia and a lower amplitude with reduced or absent atonia. These findings suggest that EDA corresponding to GBSSW have a neurophysiological mechanism in common with absence seizures, and that if the GBSSW is intense, it may be sufficient to cause immediate loss of global muscle tone. Key words." Epileptic drop attack; Generalized spike and wave complex; Absence seizure; Epilepsy with myoclonic astatic seizure; Simultaneous video-EEG analysis

INTRODUCTION We report here one patient with both frequent epileptic drop attacks and absence seizures, associated with generalized spike and wave complexes, and present evidence which may elucidate the neurophysiological mechanism of atonia in this type of seizure. CASE PRESENTATION The patient, a 3-year and 11-month-old boy, had epilepsy with myoclonic astatic seizure of early childhood [1]. His family history was negative for convulsive disorders. His developmental milestones had been normal until the age of 3 years 1 month when he had his first epileptic attack. Subsequently, he suffered repeated astatic seizures, absence seizures and generalized tonic clonic seizures (GTCS). At the age of 3 years 10 months, he was referred to our hospital, at which time Correspondence address: H. Oguni, MD, Department of Pediatrics, Tokyo Women's Medical College, 8-1 Kawada-cho, Shinjuku-ku, Tokyo 162, Japan.

226

he had daily drop attacks, absence seizures and occasional GTCS. Physical and neurological findings were normal. His intelligence quotient (modified Binet method) was 92. CT as well as MRI scan findings were non-contributory. lnterietal EEG findings. Background activity during wakefulness showed continuous diffuse 4-5 Hz theta activity with parietal accentuation. Intermittent generalized bilaterally synchronous single or multiple spike(s) and wave discharges at 2-3 Hz were seen during wakefulness and sleep. There was no focal epileptic discharge. METHOD

The seizures were investigated by means of simultaneous split-screen video taping (patient and EEG on the same screen) and EEG-EMG polygraphic recording. Surface EMGs were placed on the trapezius, sternocleidomastoideus and erector spinae muscles bilaterally. All drop seizures were analyzed using slow motion and frame-by-frame video replay mode. The EMG poBrain & Development, 1Iol 15, No 3, 1993

FpI-BNE FpI-BNE T3-BNE

-,~..~., ~,~.j,,,,A~J',/\ ~,./~'

T4-BNE

C3-BNE

'<',~ ",'',/ J'~"

C4-BNE

'W

F3-BNE F4-BNE

/~Ij/.y,)( i,i

i

O1-BNE

/

02-BNE

LI Tiipezilir~l !1 liileZili

J

,

r

,.~w~~n'~,~ J

'~"~

Rt SCH

i

I

,

q I

i

,'~,~,+etl¢

LI Erector Spinal RI Erector Spinal

,,,,,, ,,, i,, EGG

,oo,, +,

1 IlC.

i

l ~ , ~ , J ~/J

,

Fig 1. lctal polygraph of the two types of atonia and control, l: Type 1 - c o m p l e t e atonia; strong inhibition of E M G discharges was seen in all 6 E M G leads• 2: Type 2 - m i n o r atonia; brief attenuation of E M G discharges was seen only in the E M G leads of the two erector spine muscles• 3: Control - no discernible attenuation of E M G discharges was observed. Arrows indicate atonic events• Definitions of Types 1, 2 and Control, are given in the text. ']' in the figure indicate the real points of positive and negative peaks to estimate the amplitude measured at F4.

tential during falling was assessed to distinguish myoclonic or tonic from atonic events. In addition, we studied the correlation between the amplitude of the slow wave component in generalized bilaterally synchronous spike and wave complexes (GBSSW) accompanying atonic seizures and the extent of the atonic dropping (intensity of atonia, Fig 1). The amplitude was measured from the positive to the negative peak of the slow wave component at electrode F4 (F3 and F4 showed bilateral symmetry of amplitude), at the point which seemed largest on an EEG recorded with a reference montage using a balanced non-cephalic reference electrode (BNE) [2]. The intensity of the atonia in this patient was assessed on the basis of the Octal video findings and divided into 2 types according to degree of atonia relative to the previous position. In addition, we compared the amplitude of GBSSW corresponding to each type of atonia with that not accompanied by atonia (control). Type I = complete atonia; the head and body fell to the floor. Type 2 = minor atonia; only mild nodding of the head and/or the body was observable. Control - we selected the largest GBSSW Brain & Development, Vol 15, No 3, 1993

without accompanying atonia among those seen in every 20 s epoch during the 37 men of consecutive EEG recording. RESULT

Ictal video-polygraphic findings We documented eight (6 of those recorded with BNE) epileptic drop attacks (EDA). They were characterized by sudden slumping of the whole body to the floor followed by immediate recovery. Polygraphic recordings showed sudden interruption of E M G discharges corresponding to these events (Fig 2a). In addition, 14 head nodding attacks, which seemed to be minor EDA, were observed. Absence seizures were frequently seen and occasionally preceded EDA. Sudden arrest of motion and blank staring, with or without decreasing postural tone, were observed in association with bursts of GBSSW, showing the same characteristics as those of EDA (Fig 2b).

227

+ a * * ,' * , N T T ~ ' g l

f' ( T ] ' ~ ' a T l ~ ' ~ , w r

Fp 1-13 ~ , a , < , . T3-01

.......................

F3-C3

I l / I [ ¢ T t T l l I I r i y l ~ l i rT? i T FI~FI~II+~

..... , ..... A~.~.,_ ] \7~+,,/~(~,te?,,j(~ ~, m

.

.~@,p-..~-.~%a-..+..~.j~,,

.

.

.

C4-02

".

. . . . . . . . . . . . . . . . .+°v

' " , . . '+

,.,

, .., .

.

.

.

.

.

~

.

-+'

(

+

F4-C4

]"+,/ ',,/%~+ +lj~i~+'

.............. "-,~-,*,'-~-~-.;",/"~/~/%vq{i

. . . . . . - / + ' , / ' , / " + ..0 ......

/ "-~',-~-,/'.'%+1

,#'.~-..

+-N'~]~ ]

,, ,,,,,,+, ,,

n~ scu

I i I

//,v 2

{ ~.++"rlr+,,..P-,.+~.a~+,*

.

....

Fp2-F4

? * TT ~ * T T

,,/+-wqv%?, '

",

,,+

~ ~..,~...#~..~~~..~,~,,~'+..~,~..~,~r~~--

LI EIICIOl S p i l l l ~ - ~

. . . . .

+.V,,~.,~,~,~...~,~....., .....,,~

Q

I

lOOny

+

F p'- T 4

.... ". . . . . . . . . .

FpI-F3-

"

r . . . . . .

'+

%I' "

' " "+ " +'' , , e , + 0"('++ + ~ "

+ ~ 1' e~J ' ~

.. :, +.g{/,:,+<..%;v ,Aa~+++,,,,,~,v J;

:° '-~

-

•

,

,

•

•

,r.•

•

~

,

Fp2-F4 F4-C4

" ""

-

C4-02

-.-' "'.'

,

......... "

~' ++"" '"~'

..- ~,

1_1

I "

, ~ --

II

i

~ '

I

I

'~7I~

,

'

'

'

'

RI

lOOny

,

i

~--

Fig 2+ lctal polygraphic findings of the epileptic drop attack and the absence seizure, a: epileptic drop attack. Before the seizure, the patient was looking at a picture book (I). He then showed sudden blank staring, not focusing on the book for I s (2.3). Immediately thereafter, the patient's head and body suddenly fell d o w n w a r d (4). A burst of generalized bilaterally synchronous spike and wave complexes (GBSSW) was seen with a rhythmic build up of amplitude and slowing in frequency from 3 4 Hz to 1.5 2 Hz. A falling of the body corresponded to the last spike and wave complex with the largest amplitude and slowest frequency, b: absence seizure. The patient was sitting and playing with his mother• He suddenly' showed arrest of motion and blank staring (A). Then. his body started to sway slightly forward and backward (B) and he began to fall forward but then regained normal consciousness and resumed an upright position (('). Note that the morphology of G B S S W is similar to those of EDA.

228

Brain & Development. Vol 15. No 3, 1993

1400

n--6

1200 1000 Amplitude of Slow Wave (~V)

1 0 5 8+ 128/aV

n=14

8OO 73{I-+ 118~V 6O0 541 * 123 ~IV 400 200

•

t__

P=55~.oo,

P-,oo,
-

]

0

Type I

Type 2

Intensity

Type 3

of Atonia

Fig. 3. Comparison of the amplitude of the slow wave c o m p o n e n t corresponding to the atonia a m o n g 2 types with different intensities and control. The amplitude of the slow wave complex was measured at F4, where it was maximal. The method of measuring the amplitude and the definitions o f Types 1, 2 and 3, are given in the text. A statistically significant positive correlation was found in all 3 comparisons (P<0.01).

Analysis of the relationship between the amplitude of the slow wave component of GBSSW and the intensity of the atonia (Fig 3) There were 6 GBSSW of type 1, 14 of type 2, and 109 of type 3 in the record. When we made amplitude comparisons among the 2 intensities of atonia and the control, a statistically significant positive correlation was found in all 3 comparisons (P<0.01), i.e. a higher amplitude corresponded with more pronounced atonia, a lower amplitude with reduced atonia and the lowest with the control (Student's t-test for non-paired data, P values of ~<0.01 (two-tailed) were considered to be significant). DISCUSSION According to the International Classification of Epileptic Seizures [3], epileptic drop attacks (EDA) are defined as atonic seizures of extremely brief duration which lead patients to fall suddenly to the ground. They differ from falling due to flexor spasms [4] or tonic seizures. The recent advent of simultaneous splitscreen video taping [5 7] has allowed us to observe the falling attacks more precisely. Several studies using this method have demonstrated that most such attacks are caused by flexor spasms or generalized tonic seizures, and found genuine EDA to be rare. These studies focused primarily on differentiation of clinical phenomena (whether they are tonic, atonic or myoclonic falling) while the mechanism underlying the sudden, widespread loss of muscle tone, which leads the patient to fall, has been left uninvestigated. Is it due to complete Brain & Development, Vol 15, No 3, 1993

loss of consciousness, as in absence seizures, or to sudden loss of muscle tone caused by inhibition of motor control, as with inhibitory seizures? Gastaut and Broughton [4] considered EDA to be related to very brief but intense inhibitory mechanisms, suggesting the importance of participation of the motor cortex, as well as a 'centrencephalic mechanism' in the production of hypotonia, Our results offer clues which may elucidate the underlying mechanism of EDA corresponding to the generalized bilaterally synchronous spike and wave complexes (GBSSW). Taking into consideration the progression from the absence state to EDA, the morphology of ictal EEG changes in the two being the same, and the positive relationship between the amplitude of the slow wave component of GBSSW and the intensity of atonia, there seems to be a close relationship between EDA and absence seizures in terms of their underlying neurophysiological mechanisms. Absence seizures have recently been studied extensively, both clinically [8] and experimentally [9, 10]. Recent hypotheses regarding the neurophysiological mechanism of absence seizures are based largely on studies of feline penicillin-induced generalized epilepsy. This type of seizure is generally assumed to be due to the presence of underlying mild cortical hyperexcitability producing a summation of EPSPs (spike component) which in turn generates IPSPs (slow wave component) in order to prevent seizure development. This rhythmic alteration of excitation and inhibition in the cortical pyramidal neuron producing the sequence of bursts of spike and wave discharges on surface EEG, causes interference with cortical functions such as the arrest of perceptual, cognitive, mnemonic, and voluntary motor functions (referred to as recurrent cortical inhibition). These transient arrests of cortical function, caused mainly by IPSPs secondary to EPSPs, are considered to be the fundamental cause of 'loss of consciousness' during absence seizures [10]. In this context, the stronger the EPSPs, the stronger the IPSPs generated to prevent the development of a seizure. On the basis of our findings, EDA associated with GBSSW seem to be the result of stronger interference with cortical function, i.e. loss of consciousness as described above. Absence seizures themselves occasionally accompany strong atonic manifestations, such as stepwise head dropping or leaning of the body (absence seizures with atonic components [3]). Recently, we have observed a unique type of childhood partial epilepsy in which brief focal atonia of the arm escalated to generalized atonic attacks, according to generalization of the spike and wave complexes in 229

the contralateral rolandic region [1 l]. In such cases, the focal and generalized atonia seemed to result not from the loss of consciousness itself but from the sudden inhibition of muscle tone caused by spike and wave complexes. These observations suggest that the sudden brief abolition of muscle tone in the anti-gravity muscles, leading the present case to fall, is produced by strong inhibition in the motor cortex, as a part of generalized interference, caused by high amplitude spike and wave complexes. In other words, E D A corresponding to GBSSW may have a neurophysiological mechanism in c o m m o n with absence seizures. Furthermore, if the GBSSW is intense, it may be sufficient to cause immediate loss of global muscle tone. This hypothesis is applicable only to E D A corresponding to GBSSW and not to those of other epileptic abnormalities. ACKNOWLEDGEMENTS We dedicate this article in commemoration of 25 years of professorship of Dr. Yukio Fukuyama.

REFERENCES 1. Doose H. Myoclonic astatic epilepsy of early childhood. In: Roger J, Dravet C, Bureau M, Dreifuss FE, Wolf P, eds. Epileptic

230

syndrotnes in in/ant.v, childhood and adolescence. London: John Libbey Eurotext Ltd., 1985:78 88. 2. Stephenson WA, Gibbs FA. A balanced non-cephalic reference electrode. Electroencephalogr Clin Neurophvsiol 1951, 3:237 40. 3. Commission on Classification and Terminology of the ILAE. Proposal for revised clinical and electroencephalographic classification of epileptic seizures. Epilepsia 1981; 22:489 501. 4. Gastaut H, Broughton R. Atonic seizures. In: Gastaut H, Broughton R. eds. Epileptic .wizures." clinical and electroencephalographic./eatures, diagnosi.~, and treatment. Springfield: Charles C Thomas. 1972:55 63. 5. Egli M, Mothersill 1, O ' K a n c M, O ' K a n c F. The axial spasm: the predominant type of drop seizurc in patients with secondary generalized epilepsy. Epilepsia 1985: 26:401 15. 6. lkeno T, Shigematsu H, Miyakoshi M, et al. An analytic study of epileptic fidls. Epih,psia 1985: 26:612 21. 7. Nolte R, Wolff M, Krfigeloh-Mann 1. The atonic (astatic) drop attacks and their diffcrential diagnosis. In: Niedermeyer E, Degan R, eds. The Lemlov Gastaul syndrome. New York: Liss, 1988:95 108. 8. Penry JK, Porter R J, Dreifuss FE. Simultaneous recording of absence seizures with video tape and electroencephalography: a study of 374 seizures in 48 patients. Brain 1975: 98:427 40. 9, Fisher RS, Prince DA. Spike-wave rhythms in cat cortex induced by parenteral penicillin. II. Cellular features. Electroencephalogr ('l#7 Neurophysio/ 1977: 42:625 39. 10. Gloor P. Elcetrophysiology of generalized epilepsy. In: Schwartzkroin PA, Wheel H, eds. Eh, ctrophysiology ~?['epilep.s3'. New York: Academic Prcss, !984:107 36. I1. Oguni H, Sato F, Hayashi K, Wang PJ, Fukuyama Y. A study of unilateral focal atonia in childhood partial epilepsy. Epih,psia 1992: 33:75 83.

Brain & Development. ~ l 15. No 3. 1993