The postictal electroencephalogram

Electroencephalography and chmcal Neurophyswlogy, 1988, 7 0 : 9 9 - 1 0 4

99

Elsevier Scientific Pubhshers Ireland, Ltd

EEG03484

The postictal electroencephalogram Masako

Kaibara

a n d W a r r e n T. B l u m e

Epdepsy Umt, Umverslty Hospttal, Umoersrty of Western Ontarto, London, Ont N6A 5A5 (Canada) (Accepted for publicaUon 30 December 1987)

Summary Postactal phenomena, their laterahty and duration, were studied among 51 patients with scalp EEG-recorded seizures whose origin, evolution and postlctal phase were clearly depicted. Regoonal delta was the most c o m m o n postlctal change (PIC), a p p e a n n g in 29 p a a e n t s (57%) Regional attenuation occurred m 15 cases (29%) while the E E G reverted immediately to its mtenctal nature m 16 instances (31%)_ 'Activation' of spikes post~ctally occurred after 13 of the 51 seizures (25%), always over the lobe of setzure onset. PIC, whatever Rs nature, appeared pnnclpally or exclusively lpsdaterai to seizure origin in all 35 pauents Moreover, when such changes were bdaterally distributed, they persisted longer on the side of seizure origin m all but one case when durataons were bilaterally equal A muluple PIC ( > 1 phenomenon) occurred after 21 seizures (41%) whale a single change appeared after 14 attacks (27%) Multiple changes occurred more commonly when the seizures had evolved to independent bdateral seizures or to grand real (77%) than when they were c o n h n e d to the hermsphere of o n g m (14%)_ Thus multiple changes were more often distributed bdaterally (90%) than were single changes (29%) Conversely, seizures without any propagatton (focal only) were those most hkely to show no posttctal change Multiple changes lasted longer (mean 406 sec) than single changes (79 sec), but duration of PIC was unaffected by seizure propagation or its nature, except for grand mal Seizure duration had no effect on PIC d u r a u o n except for grand real attacks whose postlctal effects were predictably longer Our data suggest that (1) laterahsatmn of PIC can rehably indicate s~de of seizure ongon, (2) duration of brain recovery after a seizure correlates better with the complexity of posUctal perturbation than w~th aspects of the seizure ~tself

Key words: Postlctal epdepsy, E E G

That regtonal attenuation a n d / o r delta E E G activity follow most partial (focal) epdeptic seizures is known to electroencephalographers and ~s described m some textbooks (Amlnoff 1980; Sharbrough 1982). Yet a formal study of postlctal phenomena is not yet available. We investigated the nature, incidence, multiplicity, location and duration of postlctal phenomena and related such aspects to ictal and lnterictal E E G features.

Correspondence to Dr W T Blume, EEG Department, Umverstty HospRal, 339 Windermere Road, London, Ont_ N 6 A 5A5 (Canada)

Method All patients had EEG-recorded simple or complex parUal seizures between 1977 and 1985 Only the first seizure meeting criteria outhned below was stud~ed. To minimlse confusion with lntenctal diffuse abnormalities, patients below age 5 years and those with a subnormal level of consciousness pre-ictally were excluded. Most attacks occurred during the resting awake recording. A few occurred dunng hyperventdatlon or sleep. D a t a from telemetred recordings were employed if all criteria were met. N o convulsant agents were used. Requiting a consistent postictal state of alertness assured that postlctal changes did not simply reflect a change of state.

0013-4649/88/$03_50 © 1988 Elsevier Soentlflc Publishers Ireland, Ltd

100 The clinical p a r t i a l seizure h a d to be clearly and entirely d e p i c t e d on the E E G with an identifiable focus of o n ~ n E E G s were r e c o r d e d on 16channel i n s t r u m e n t s using the 10-20 system of electrode p l a c e m e n t . In addition, s p h e n o i d a l a n d a n t e r i o r t e m p o r a l electrodes (T1, T2) were emp l o y e d on m a n y p a t i e n t s All seizures occurred on b i p o l a r montages, although this h a d not been a criterion for entry O f the 51 seizures meeting these c n t e n a , 42 o r i g i n a t e d m a t e m p o r a l lobe. Other regions of o n s e t were p o s t e r i o r t e m p o r a l - o c c i p i t a l (3), p a n e t a l - p o s t e n o r t e m p o r a l (2), r o l a n d i c - f r o n t a l (2), p a n e t a l - o c c x p i t a l (1), and rola_n&c-panetal (1). A technically satisfactory postlctal recording for at least 60 sec was required. In all cases, the E E G was c o n t i n u o u s l y r e c o r d e d t h r o u g h o u t the ictal a n d p o s t l c t a l p e r i o d s with no a l t e r a t i o n of m o n t a g e until the record once again r e s e m b l e d the pre-ictal E E G . The rare cases with alteration of E E G settings d u r i n g the postictal p e r i o d were included if expression of postictal p h e n o m e n a was not m h i b l t e d or altered Ranges of E E G settings a m o n g recordings were: sensitivity 5 - 3 0 / ~ V / m m , H L F 3 5 - 7 0 Hz, L L F 0 3 - 1 Hz F r o m a pilot study, we defined a single postictal change as that c o n t a i n i n g p r e d o m i n a n t l y a single E E G feature of either delta, attenuation, or theta, or spikes Postictal delta or theta was defined as either its new a p p e a r a n c e or a greater than 50% increase m voltage as c o m p a r e d to the preictal state_ A t t e n u a t i o n was defined as a postlctal reduction of b a c k g r o u n d activity (excluding delta) to absent o r m i n i m a l ( < 10 /~V). Postlctal spike "activation' was defined as e~ther the new a p p e a r a n c e of spikes d u n n g the first 5 mln postictally or an at least 3-fold increase m spike q u a n tity beginning d u r i n g this period_ A m u l t i p l e postlctal change consisted of m o r e than one of the a b o v e features either s~multaneously or sequentially. D u r a t i o n of postlctal change was m e a s u r e d for each E E G d e r i v a t i o n (electrode pair) m d w i d u ally and d u r a t i o n of p o s t i c t a l change for that p a t i e n t was c o n s i d e r e d as the longest of the individual derivation durations. Each seizure was electrographically classified into 1 of 4 types d e p e n d i n g u p o n the presence and n a t u r e of p r o p a g a t i o n (1) focal only - - seizure

M KAIBARA, WT BLUME confined to region or hemisphere of onset without bilateral involvement, (2) focal b e c o m i n g bilaterally s y n c h r o n o u s -- b i s y n c h r o n o u s spikes, spikeand-waves, r h y t h m i c delta or theta a d d e d w i t h o u t evolution to g r a n d real, (3) focal b e c o m i n g g r a n d real - - clinically a n d electrographlcally, (4) focal b e c o m i n g i n d e p e n d e n t bilateral - - evolution to a s y n c h r o n o u s i n d e p e n d e n t l y occurring seizures m each h e m i s p h e r e All E E G recordings were i n d e p e n d e n t l y assessed by each author_ Rare d i s a g r e e m e n t s were resolved b y m u t u a l record review

Results

Types of posttctal change R e g i o n a l delta or regionally a c c e n t u a t e d diffuse delta was the most c o m m o n p o s t i c t a l c h a n g e (PIC), a p p e a n n g after 29 of 51 seizures (57%) (Fig. l a ) . A t t e n u a t i o n of regional activity was n o t e d in 15 cases (29%) ( F i g l b ) , while i m m e d i a t e reversion to the I n t e n c t a l E E G occurred after 16 attacks (31%) (Fig_ lc). T h e t a was a p r o m i n e n t single feature on 1 occasion A clear increase in spike q u a n t i t y o c c u r r e d after 13 of the 51 seizures (25%), always over the lobe of seizure onset_ Such ' a c t i v a t i o n ' of spikes b e g a n within 30 sec of seizure t e r m i n a t i o n in 10 of the 13 patients, while the spike Increase wa~ d e l a y e d from 100 to 244 sec p o s t i c t a l l y in the other 3 cases A m o n g the 13 patients, the p e n o d of spike activation lasted from 8 sec to 590 sec postictally ( m e d i a n 167 sec). Spike activation always a p p e a r e d s i m u l t a n e o u s l y or sequentially with delta a n d / o r attenuation. In 5 instances the spikes repeated in a p e r i o d i c fashion. As c o m p a r e d to spike q u a n t i t y for 200 sec p n o r to seizure onset, a clear decrease of spikes occurred p o s t l c t a l l y in 3 of 35 patients with a PIC_ This decrease in spike incidence lasted 90, 95 and 100 sec postictally. A g e of p a t i e n t s had no effect on incidence of PIC. T h i r t y - o n e of the 42 patients (74%) whose ~eizures arose from a t e m p o r a l lobe h a d a PIC, c o m p a r e d to 4 of 9 seizures (44%) f r o m e x t r a t e m poral sites. However, our n u m b e r s were insufficient for significance (Ftsher's exact test = 0.075)_

T H E POSTICTAL EEG

101 POST-ICTAL DELTA

ICTAL

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(a)

28 yrs

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was revolved in all 35 patients and the ipsdateral parasagittal region in 30 (86%). PIC appeared pnncipally over the lobe of origin in all 31 patients with temporal lobe seizures, but area of maximum expression vaned independently of origin in the 4 patients with extratemporal attacks. A contralateral parasagittal postictal change appeared in 19 of the 35 paUents (54%) and a contralateral temporal PIC in 18 (51%). When bilateral, postictal changes persisted longer on the side of seizure origin than on the contralateral side in all but a single instance when they were equal m duration.

POST- ICTAL A T T E N U A T I O N (b)

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_ _ 1 ,~.uv iSEC Fig. 1 a left temporal delta post]ctally 5 Hz rhythmic left temporal waves axe [etal lctal slow waves at T4 axe artefactual. b: diffuse left hemisphere attenuaUon of act~vaty 14 sec post, ctally (only paxasagittal leads shown) c no posuctal change; EEG tmmediately reverts to pre-~ctal state, i e., normal, at seizure tenmnatlon (arrow).

Location Posbctal change(s) appeared pnncipally or excluswely ipsilateral to seizure origin m all 35 patmnts with postictal change. The temporal lobe

Single and multtple changes A multiple change (more than one phenomenon) was observed after 21 of 51 seizures (41%) while a single change (principally one phenomenon) appeared after 14 attacks (27%) (Table I). Of 29 patients with delta, it was virtually the only phenomenon in 8 (28%). Among the other 21 patients with delta, several sequences of delta with other features occurred. In order of incidence these were: attenuation with, or followed by, delta; delta w~tb spikes both gradually abating; delta alone evolving to delta with spikes; spikes alone, then delta and spikes; and delta evolving to theta alone. Among the 15 patients with attenuation, ~t was virtually the only phenomenon m 5 (33%). When part of a multiple change, attenuation occurred simultaneously with delta or preceded it; delta never preceded attenuation. Nineteen of 21 (90%) multiple changes appeared bilaterally winle only 4 of 14 (29%) single changes did so ( P < 0.005) (Fig. 2). However, Fig. 2 shows that the tendency to bilaterahty did not depend upon the phenomena compnsmg PIC. The multiplicity of postictal change depended upon whether the seizure had propagated and the nature of such propagation. Thus, only 3 of the 22 seizures (14%) without propagation (focal only) were followed by a multiple PIC (Fig. 3). In contrast, 10 of the 13 seizures (77%) winch evolved to independently occurring bilateral seizures or to grand mal had multiple PIC ( P < 0.005) Fig. 3 also shows that seizures with focal and then bisynchronous phenomena occupied an intermediate pos]t~on m this respect. Focal only seizures were

102

M KAIBARA, W T BLUME

TABLE I D u r a t i o n s of p o s t l c t a l c h a n g e s b y type (msec)_ PIC

Number of seizures

Mean

Median

S D

Range

Single Multiple D e l t a (total) Delta only Delta and attenuation only D e l t a a n d a t t e n u a t i o n plus

14 21 29 8 2

79 406 324 109 1 ll0

58 164 154 99

82 616 543 1(K) 1 244

7 - 268 7 2450 7 2 450 7 - 254 230-1990

( t h e t a o r spikes) D e l t a a n d ( t h e t a o r spikes) A t t e n u a t i o n (total) Attenuaaon only All P I C s

8 11 15 5 35

508 204 434 45 275

154 164 154 29 100

806 188 ~22 514

2 0 - 2 450 7 590 8-2450 8 100 7-2450

35

79

68

47

lu

D u r a t m n of se, r u r e s with PIC

also those most hkely to show no postictal change (14 of 22, 64%) whereas only 2 of 29 seizures (7%) with any type of bilateral propagation showed no postictal change ( P < 0.005). The lobe of seizure origin had no effect on the nature of PIC, including phenomena and multiplicity. Duration

Although duration of PIC varied considerably,

24-

237

its mean duration of 275 sec (S.D = 514 sec), exceeded the mean seizure duration of 79 sec (S.D = 47 sec) for the 35 patients. Similarly, the duration of postlctal change exceeded seizure duration m 21 of the 35 cases. However, Fig. 4 shows that setzure duration had no effect on duration of postlctal change except for grand mal Mulaple changes averaged 5 times longer (406 sec) than single changes (79 sec) (Table I), but the

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Fig 2 ' P a u e n t s " = n u m b e r of p a t i e n t s P I C = p o s u c t a l change_ M e a n d u r a t i o n = m e a n P I C d u r a t i o n m s e c o n d s All p a U e n t s with m u l t t p l e c h a n g e s h a d delta; all m last 2 g r o u p s h a d a t t e n u a t i o n w i t h d e l t a See T a b l e I for m e a n d u r a U o n s as n u m e r i c a l values

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Fxg 3 D u r a t i o n = m e a n PIE' d u r a t i o n See text for d e f t m t l o n s of seizure types, single a n d m u l t i p l e P I C P r e - l c t a l = i m m e d i a t e reversion to pre-Jctal E E G , L e , n o P I C . N u m b e r s at b a r s = n u m b e r of p a U e n t s w i t h p h e n o m e n o n _ M e a n P I C d u r a U o n for g r a n d real = 2220 sec_

103

THE POSTICTAL EEG SEIZURE AND PIC DURATIONS

E E G changes whereas 13 of 26 patients (50%) without such spikes had PICs ( P < 0.005). However, persistent or mtermattent regional delta activity, whether ipsllateral or contralateral to seizure onset, had no effect on PIC incidence or morphology. N o other interlctal phenomenon was studied.

(1~o) (2450)

(sec)

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Discussion > SEIZURE

oql, 200

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SEIZURE

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

< SEIZURE

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I [00

I 200

I 300

DURATION (sec) Fig. 4 O r d i n a t e = n u m b e r of seconds each P I C exceeds ( > s e c u r e ) or Is less t h a n ( < seizure) seizure d u r a t i o n P a t i e n t s at zero o r d i n a t e = no P I C Points = indivadual p a t t e n t data. Abscissa: duraUon of each seizure.

standard deviations and ranges were considerable. PICs wath delta averaged 324 sec while those with attenuation averaged 434 sec, but the medians of such PICs were the same (154 sec). Delta with attenuation was the longest lasting (mean: 1110 see).

However, duration of PIC was unaffected by seizure propagation or its nature, except for grand real (Fig. 3). Excluding patients without PIC, mean duration of PIC for each lctal E E G type was. focal only - - 164 sec (S.D. = 151 sec), focal--* bilaterally synchronous - - 164 sec (S.D. = 186 sec), focal --* grand mal - - 2220 sec (S.D. = 230 sec), and focal ~ independent bifocal - - 141 sec (S.D. = 106 sec). The large standard deviations reflect the considerable interpatient variability. Intertctal E E G Twenty-two of 25 patients (88%) with interictal spikes contralateral to seizure origin had postictal

The neurophyslological bases of the 2 pnncipal postlctal phenomena, attenuation and delta, remain incompletely explored. Attenuation may represent relative neuronal inactivity from postictal hyperpolarisation (Matsumoto and Ajmone Marsan 1964; Ajmone Marsan 1969). Funcuonally deafferentated cortex in the postictal period is thought to be responsible for polymorphic delta ( A m m o f f 1980; Sharbrough 1982), Mechanisms tending to increase spike quantity postictally in some patients (25% in tlus senes) likely include the increase in extracellular potassmm wluch occurs when either the cerebral neocortex or the hippocampus is involved in a seizure, and the usual lowering of extracellular calcium under these circumstances (see H e i n e m a n n et al. 1986; Somjen et al 1986 for reviews). Such ionic alterations have each been shown to increase spontaneous epileptlform acUvaty (Heinemann et al. 1986). Gotm a n (1985) found an increase m spike rate m the m a j o n t y of patients after both partial and generalised seizures studied by scalp or intracerebral electrodes. Immediate reversion to the interictal E E G occurred in 31% of our patients. This occurred m almost half of the patients studied by Klass et al. (1973, cited by Klass 1975) and in 15% of convulsant-mduced seizures by Ajmone Marsan and Ralston (1957a). In our material, ttus occurred more commonly when the seizure faded to propagate. Such varying percentages from those studies m a y therefore reflect their varying incidence of propagated seizures, but this aspect is not fully outhned in the earher works. Duration for E E G recovery m our study hmged more on the multiplicity of such poslactal changes than on the presence of any specific postlctal

104

component or on aspects of the setzures themselves Thus, recovery time, i.e., durataon of the postlctal change, averaged 5 times longer when more than 1 postictal phenomenon was present (406 sec) than when a single phenomenon appeared (79 sec). However, little difference m PIC duratxon between delta and attenuation was found. Surprisingly, recovery time was not influenced by seizure duration in our material, except for grand mal. The electrographic nature of the seizure influenced recovery time only through its effect on multiplicity of postictal changes. It was not surprising that morphologically more complex seizures (independent bilateral and grand mal) usually resulted m multiple postictal phenomena However, the lack of any direct relationship between the presence and type of seizure propagation and recovery time was unexpected and remains unexplained That all 35 postictal changes appeared principally lpsdateral to seizure o n g m agrees with impressions of earher authors (Ajmone Marsan and Ralston 1957b; Klass 1975; Gabor 1981; Wieser 1983; Leppik 1984). However, Gloor (1975) cautions that postictal changes are situated pnnc~pally over the regton most intensely involved in the seizure which usually, but not always, coincides with the area of seizure onset Subsequent studies may show that the most intense seizure activity occurs contralateral to or otherwise distant from seizure origm only when mtenctal abnormahties are prominent at the propagated sxte. If this is so, the location of post~ctal changes could be considered to represent seizure origin if such correspond to the site of most lntenctal spikes. In these instances mVaslve recordings would not be necessary even if the site of seizure origin were obscure Joanna Borghesl and Conrad Ylm are acknowledged for their helpful adwce Mrs_ Maria Raffa carefully prepared the manuscnpt

References Ajmone Marsan, C Acute effects of topical epdeptogemc agents In- H_H Jasper, A A_ Ward and A Pope (Eds_),

M KAIBARA, W T B L U M E Basic M e c h a m s m s of the Epilepsies Little, Brown and ( o Boston, MA, 1969 299-319 Ajmone Marsan, C and Ralston. B L EEG changes their classlficahon and sxgnlflcance In C Ajmone Marsan and B L Ralston (Eds), The Epileptic Seizure_ Thomas, Spnngfield, IL, 1957a 51-76 Ajmone Marsan, C and Ralston, B L Electro-clinical correlations In C Ajmone Marsan and B L Ralston (Eds). The Epileptic Seizure Thomas, Spnngfleld, IL, 1957b 139-183 Armnoff, M J EEG findings m patients with neurologlc disorders In M J. Armnoff (Ed). Electrodlagnosls m Chmcal Neurology Churclull Livangstone, New York, 1980 41-66 Gabor, A J The lctal E E G In B A Tharp (Chaarman), Chmcal Electroencephalography American Academy of Neurology Annual Course No 1 April 27, 1981 57 Gloor. P Contributions of electroencephalography and electrocortlcography to the neurosurgacal treatment of the epilepsies_ In D P Purpura, J K Penry and RD_ Waiter (Eds). Advances m Neurology, Vol 8 Raven Press, New York, 1975 59-105 Gotman, J Electroencephalographlt. spiking activity, drug levels and setzure occurrence m epdepuc patients A n n Neurol_. 1985, 17 597-603 Hememann, V , Konnerth A and Pumam, R Extracellular calcmm and potassium concentration changes m chromc eplleptxc brain tissue In A V Delgado-Escueta, A A Ward, Jr, D M Woodbury and R_J Porter (Eds), Advances m Neurology, Vol_ 44 Raven Press, New York, 1986 641-661 Klass, D W Electrographtc m a m f e s t a u o n s of complex parual seizures In J K Penry and D D Daly (Eds.), Advances in Neurology, Vol 11 Raven Press, New York, 1975 113-140 Lepptk, I E The electroencephalogram m partial seizures In State of the Science m E E G American E E G Socwty 19th Annual Course in Chmcal EEG and Electrophyslology. 1984 Matsumoto, H and Ajmone Marsan, C Cortical cellular phenomena m expenmental epdepsy lCtal mamfestauons. Exp_ Neurol, 1964, 9 305-326 Sharbrough, F W N o n specific abnormal E E G patterns In- E Nledermeyer and F Lopes da Sdva (Eds), Electroencephalography Basic Pnnclples, Chmcal Apphcatlons and Related F~elds U r b a n and Schwarzenberg, Baltimore. MD, 1982 152-153 Somjen, G G , AJtken, P G , Gmcchmo, J L and McNamara, J O Intenctal xon concentrations and paroxysmal discharges m bappocampal formation and spinal cord In A V Delgado-Escueta, A A Ward, Jr, D M Woodbury and R J. Porter (Eds), Advances m Neurology, Vol 44 Raven Press, New York, 1986 663 Wleser, H_G Ictal surface E E G In H G Wleser (Ed), Electrochmcal Features of the Psychomotor Seizure Butterworth, New York, 1983 184-185