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Archives ofDisease in Childhood 1995; 73: 106- 1 1

Non-convulsive status epilepticus

G Stores, Z Zaiwalla, E Styles, A Hoshika

AbstractThe clinical, electrographic and reportedneuropsychological features of 50 childrenwith non-convulsive status epilepticus(NCSE) were reviewed and the children'sprogress followed for one to five years.NCSE occurred in a variety of epilepsies,especially the Lennox-Gastaut syndrome.Clinical manifestations ranged fromobvious mental deterioration to subtlechanges. The condition had often beenoverlooked or misinterpreted and manychildren had experienced repeatedepisodes over long periods. Followingdiagnosis, immediate treatment was oftennot attempted or was not successful.Further episodes ofNCSE occurred in themajority of children during the follow upperiod. Failure to recognise NCSE and totreat episodes promptly, and the high rateof recurrence, is of particular concern inview of fears that repeated exposure tothis condition might be brain damaging.At least 28 children in the present seriesshowed evidence of intellectual oreducational deterioration over the periodduring which NCSE had occurred,although the exact cause was difficult todetermine.(Arch Dis Child 1995; 73: 106-1 1 1)

Keywords: non-convulsive status epilepticus,prognosis.

University of OxfordDepartment ofPsychiatry, ParkHospital for Children,Old Road, Headington,Oxford OX3 7LQG Stores

Park Hospital forChildren, OxfordZ Zaiwalla

University of OxfordDepartnent ofExperimentalPsychologyE Styles

Tokyo Medical CollegeHospital, Tokyo, JapanA Hoshika

Correspondence to:Dr Stores.

Accepted 24 April 1995

Non-convulsive status epilepticus (NCSE)usually consists of a prolonged seizure statepredominantly affecting mental function. Thiscondition is not rare and is likely to be encoun-tered in paediatric practice, especially in dis-abled children with epilepsy. It is oftenmisdiagnosed or undiagnosed and, even whenrecognised, may not be treated with anyurgency.'

Publications on NCSE are scattered andlargely consist of reports of single cases orsmall series. From these accounts andreviews1-3 certain important issues of practicaland theoretical importance can be identified.These include the complexities of classification(especially in children), the wide range ofclinical manifestations of NCSE, the uncer-

tainties of immediate and long term treatment,and the possibility that prolonged exposure toseizure discharge (whether accompanied byprominent clinical manifestations or not) can

cause brain damage and intellectual decline.Clearly, more systematic investigation of thisimportant and intriguing form of epilepsy isrequired but in the meantime what is alreadyknown needs to be more widely disseminated.

The present study consists of a mainly retro-spective review of a large group of children inwhom a diagnosis of NCSE was made whenfirst seen in a children's epilepsy and EEGservice. The analysis of the findings placesspecial emphasis on the type of epilepsy orepilepsy syndrome in which these forms ofstatus had arisen, the relationship betweenelectrographic features and clinical manifesta-tions, the difficulties of recognition that canarise, medical treatment given, and the courseof the disorder.

MethodsSUBJECTSOver a 12 year period 50 children referred tothe epilepsy service or the Oxford regionalpaediatric EEG service at the Park Hospital inOxford were considered to be in NCSE follow-ing EEG investigation. The children had beenreferred to these services for investigation ofchanges in behaviour, poor school progress,unsatisfactory seizure control, or for generalreview. The diagnosis of NCSE was madewhen prolonged periods of seizure activity inthe awake state appeared to have an effect onthe child's mental state in the absence ofobvious motor manifestations. In addition tothis series of 50 children, two others wereidentified over the same period as having elec-trical status epilepticus during slow wave sleep(ESES).4 These have not been included in thepresent account which is concerned with thedirect association between sustained seizureactivity during the awake state and psychologi-cal function. Children with hypsarrhythmia(considered by some to be a form of NCSE)and babies under the age of 2 years were alsonot included in this series on the grounds thatboth of these groups present special problemsin assessing electroclinical correlations.

PROCEDURE AND ASSESSMENTSEEGIn most cases the condition was diagnosedinitially by means of standard EEG recordingswhich revealed continuous or nearly contin-uous seizure discharge, usually generalised indistribution, without obvious motor accom-paniments of a convulsive type. In these casesEEG recordings were repeated as indicated toassess the relationship between EEG andclinical features. In 10 children prolongedrecordings by means of ambulatory EEGmonitoring,5 or combined EEG and video pro-cedures, were necessary to confirm the clinicalsuspicion that NCSE was occurring intermit-tently, usually in subtle form, or to assess theelectroclinical associations in more detail.

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Psychological developmentThe past clinical notes of all the children in theseries were obtained and scrutinised forrecorded details of early and later developmen-tal progress, and past psychological changesthat seemed likely to have marked the onsetand subsequent recurrence of each child'sNCSE. This information was supplemented byinformation obtained by writing to parents,schools, and psychological services for succes-

sive records. These were examined with specialemphasis on the child's abilities or behaviourbefore or soon after the onset of NCSE andsubsequently, including the most recentchanges prior to the investigation by the ParkHospital services.

Psychological assessmentPsychological assessment at the time thatNCSE was diagnosed at the Park Hospitalconsisted principally of general observations bystaff. In six of the children who underwentspecial monitoring, a standardised protocolwas used consisting of orientation assessmentand tests of short term memory, delayed recall,perceptual speed, copying, and visuomotorskills. These assessments were repeated whenthe child was no longer in status.

Medical detailsMedical details concerning the general natureand cause of each child's epilepsy, and anyspecial investigations, were recorded from pastclinical notes.

Follow up informationFollow up information was collected fromparents, schools, physicians, and psychologistsover a period of one to five years after the childwas first assessed at the Park Hospital. Thisinformation covered the more recent course ofthe child's epilepsy, including further episodesof status, and psychological development.

ResultsGENERAL

The 50 children ranged in age from 2 to 15years at the time of referral to the ParkHospital services. Thirty two were boys. Age atonset of the seizures varied from infancy to 10years.

Retrospective inquiries suggested that theduration of the current episode ofNCSE at thetime it was diagnosed at the Park Hospital hadvaried widely from a few hours to a few days(five cases), to several days to a few weeks (30cases) or even longer (up to several months) inthe rest. Twenty children were judged to havehad previous episodes of NCSE before theirassessment at the Park Hospital. This was

inferred largely from parent and teacherrecords indicating periods of mental deteriora-tion of generally uncertain cause, althoughEEG confirmation was available in a few cases.

The period over which these episodes hadoccurred ranged from three months to six years

in 17 children; it was difficult to judge theduration of exposure to NCSE in the otherthree. In all but one child the diagnosis ofepilepsy had preceded the first episode of non-convulsive status.

UNDERLYING EPILEPSIESTable 1 shows the various types of epilepsysyndrome6 associated with NCSE in thepresent series. Eighteen children were classi-fied as having the Lennox-Gastaut syndromeon the grounds that they had a variety ofseizure types (especially tonic, clonic, andatypical absences) starting in early childhoodand associated with developmental delay, plusslow background EEG rhythms, multifocalabnormalities, and slow (less than 3 Hz) spikewave discharges. Thirteen children corre-sponded to the picture of epilepsy withmyoclonic-astatic seizures, that is, early onsetusually with normal initial development, vari-ous seizure types (including those included inthe name of the condition), and irregular fastspike or polyspike wave discharge with some-what slow background rhythms. DuringNCSEthe EEG in both these subgroups containedwidespread irregular 4-7 Hz spike wave activ-ity with a variable proportion of spike to wavesfrom one child to another and from one time toanother in the individual case. Children inthese two subgroups could be described ashaving 'atypical absence status'.

Three children had childhood absenceepilepsy with classical, regular, well organised3 Hz spike wave discharge during NCSE('typical absence status'). Twelve had partialepilepsies: six had predominantly simplepartial seizures and the other six had complexpartial seizures. Sometimes secondary general-isation occurred in both these subgroups. Inthese partial cases the EEG abnormality duringNCSE consisted of widespread slowing withbilateral, or occasionally unilateral, irregularspike wave or sharp wave discharges withinconsistent localisation. In view of the partialnature of these children's epilepsies and theimpairment of consciousness during theirperiods of NCSE, their NCSE was consideredto be complex partial, mixed, or transitional intype. Four children had seizure disorderswhich were difficult to classify. They had amixture of seizure types but no other charac-teristic clinical or EEG features. DuringNCSE, their EEGs contained slow back-ground rhythms and generalised spike wavedischarges at frequencies about 3 Hz.

Table 2 indicates the intellectual levelsassessed during the course of the children'sepilepsy. The majority of the children in the

Table 1 Non-convulsive status epilepticus: subgroupsaccording to type of epilepsy

Type of epilepsy No Male Female

Lennox-Gastaut syndrome 18 11 7Epilepsy with myoclonic-astatic seizures 13 12 1Childhood absence epilepsy 3 1 2Partial epilepsy 12 3 9Unclassifiable 4 4 0Totals 50 31 19

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Table 2 Intellectual levels of children with different types of epilepsy

Severe learning Moderate to mild AverageType of epilepsy No disability learning disability ability

Lennox-Gastaut syndrome 18 16 2 0Epilepsy with myoclonic-astatic seizures 13 2 6 5Childhood absence epilepsy 3 0 0 3Partial epilepsy 12 3 2 7Unclassifiable 4 1 0 3Totals 50 22 10 18

series showed some degree of learning dis-ability, often severe. However, this appliedoverwhelmingly to the Lennox-Gastautsubgroup with many children in the othersubgroups displaying levels of intelligencewithin the normal range.

ELECTROCLINICAL ASSOCIATIONSThe clinical picture of children in NCSE, asjudged by direct observation at the ParkHospital as well as by past descriptions in somecases, varied widely. The change in behaviourwas considered obvious in 32 cases in that theduration of the episode was associated withclear and sustained alteration. This consistedessentially of a reduction of activity, slowness,and impairment of consciousness to varyingdegrees constituting a confusional state or evensemistupor ('pseudodementia'7). Poor balanceor incoordination ('pseudoataxia'7), usuallyassociated with intermittent bilateral jerks ofthe limbs, was reported as an additional promi-nent feature in eight of this group. Table 3 listssome descriptions by parents, teachers, orhospital staff of children during NCSE and onremission. The first group of descriptions referto changes in awareness and responsiveness;the second group to coordination problems.These items show a range of behaviouralchanges, but all are readily recognisable. Inanother 14 children the change was muchmore subtle, such as mild clouding of con-sciousness, even in the presence of gross EEGabnormality including generalised, regular,well organised 3 Hz spike wave in one of thecases of typical absence status. Relationshipsbetween electrographic and clinical featureswere difficult to discern in the remainingchildren because of the severity of their basicintellectual disability.

RECOGNITIONIn only 20 of the 50 children was the diagnosis

Table 3 Non-convulsive status epilepticus: examples ofpsychologicalfeatures as described by observers

Duing NCSE On remission

'forgetful' 'brighter''difficult to motivate' 'more alert''excessively sleepy' 'more talkative''lost and disorientated' 'happier''unresponsive' 'like a fog was lifted from her

mind''switches off''zombie-like''apparently deaf and blind''drugged state''poor balance''frequent falls''poor control of movements'

of NCSE considered by the physician whenreferring the child to the epilepsy or EEG ser-vice. In these cases an EEG was requested toconfirm the diagnosis. In the majority, thereason for referral was usually an open endedinquiry into the reason for the child's deterio-rated behaviour or poor school progress, withmention in some cases of such possible expla-nations as antiepileptic drug intoxication, pro-gressive cerebral pathology, or psychologicaldisorder. One child had previously beenreferred to a child psychiatrist because herearly morning slowness and reluctance to getready for school were interpreted as schoolrefusal. Prolonged EEG recordings showedthat she was frequently in complex partialstatus in the mornings. Only when video/EEGrecordings with simultaneous psychologicaltest results were shown to the teachers ofanother child, were they convinced that herintermittent moodiness and relative unrespon-siveness were manifestations of her epilepsy.

PRECIPITATING FACTORSThere was substantial evidence of a specificfactor immediately preceding the onset of aperiod of NCSE in only four cases in thisseries. In one child this was the onset of afebrile illness, and in the other three casesabrupt withdrawal of antiepileptic medicationseemed to have precipitated the episode.

TREATMENTFollowing their EEG recording indicatingNCSE, the children referred from otherhospitals to the EEG service were returned tothe care of their local paediatric services. Only25 of the total series received immediatetreatment for the condition. This consisted ofintravenous or rectal diazepam. Prompt sup-pression of the seizure activity was achieved in17 children, with clinical improvement notedafter the sedative effects of the treatment hadworn off, although this response lasted only amatter of hours in eight. In the remaining eightno EEG or clinical improvement was appar-ently achieved. Response to treatment did notseem to vary much from one type of epilepsy toanother (table 4). Adjustments in the child'scontinuous medication, in an attempt tosuppress further episodes ofNCSE, were madein only 26 of the series.

FOLLOW UPBy the time of follow up (maximum five years),seizures had ceased to occur for at least 12months in 20 children. Up to the point ofremission in these children, or to the time ofthe follow up in the remainder, furtherepisodes of NCSE had continued to occurafter diagnosis at the Park Hospital in 37 of the50 children.

All but four of the total series were stilltaking antiepileptic medication, including twochildren who had undergone surgery for theirpartial seizure disorder. Those children whohad suffered further episodes of NCSE were

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Table 4 Response to immediate treatmentfor non-convulsive status epilepticus in relationto underlying epilepsy

Sustained Brief response NoType of epilepsy No response only response

Lennox-Gastaut syndrome 9 2 4 3Epilepsy with myoclonic-astatic seizures 8 3 3 2Partial epilepsy 8 4 1 3

Totals 25 9 8 8

not characterised by any particular underlyingepilepsy. The adjustments made to continuousmedication following diagnosis ofNCSE, in anattempt to prevent further episodes, were vari-able in nature. This, as well as the complicatedtreatment regimens (with multiple drugs, andketogenic diet in 12 cases) and the limitationsin the available information for the follow upperiod, made generalisations about the effec-tiveness of these changes of treatment impos-sible. In the 26 cases where such adjustmentswere made, the most consistent change associ-ated with non-recurrence of NCSE was anincrease in the dosage of sodium valproate(seven cases) or the addition of ethosuximideto sodium valproate (four cases). There was noobvious example of NCSE being precipitatedby any particular antiepileptic drug.As far as possible, comparisons were made

between (a) each child's level of intellectual oreducational function before NCSE had devel-oped (or soon after its first occurrence) and (b)the level at the time of follow up or, in the 20cases where the epilepsy had remitted, beforethis improvement had occurred. Twenty sevenof the 50 children showed convincing evidenceof intellectual or educational deterioration overthis period. In the remaining 23 sufficientinformation was not available to allow thecourse of their cognitive development to beassessed reliably. Table 5 shows this deteriora-tion in relation to underlying types of epilepsy.An attempt was then made to judge the edu-

cational or intellectual development during theperiod of remission of the 20 children whoseseizures, including episodes of NCSE, hadapparently ceased. Five appeared to have madea significant improvement but the rest,although often considered by their parents orteachers to be more alert, were still function-ing at the same intellectual level as beforeremission of their seizures.

DiscussionThis study involved the largest published seriesof children with NCSE known to the authors.However, it is subject to limitations imposedby its partly retrospective nature and its

Table 5 Evidence ofmental deterioration from onset ofnon-convulsive status epilepticus to follow up in relation tounderlying type of epilepsy

Evidence ofType of epilepsy No deterioration Uncertain

Lennox-Gastaut syndrome 18 7 11Epilepsy with myoclonic-

astatic epilepsy 13 7 6Childhood absence epilepsy 3 0 3Partial epilepsy 12 11 1Unclassifiable 4 2 2

Totals 50 27 23

reliance on clinical information not compiledspecifically for the purpose of the investigation.Even so, the findings raise a number of issuesand general principles which deserve moreclinical and research attention.NCSE was found to complicate a wide

variety of the childhood epilepsies, sometimesfrom a very early age, often repeatedly and forlong periods. Its clinical presentation rangedfrom dramatic to very subtle effects on mentalfunction but, even in its more clinicallyobvious form, it was commonly not consideredas the cause of mental deterioration.Immediate treatment of the condition wasoften not provided and the recurrence rate washigh. Many children deteriorated intellectuallyduring the course of their exposure to NCSE.

Terminology and classifications are them-selves problems.1 NCSE is a very broad termwhich applies to any prolonged seizure of anon-convulsive type. Although most emphasisis placed on absence status (and to a less extenton complex partial status), patients have beendescribed whose status has consisted of pro-longed expressions of the many other types ofgeneralised and partial non-convulsiveseizures. For the present series, classificationinto absence status (typical or atypical) andcomplex partial status seemed to be sufficientfor those cases where clinical accompanimentsof the prolonged seizure activity could beidentified. Earlier terms such as 'minorepileptic status'7 were avoided because oftheir imprecision.The prevalence of NCSE is unknown and

likely to remain so until the condition is betterrecognised. On the evidence of the presentstudy, it can be expected to occur in any maincategory of epilepsy, both generalised and par-tial. The most usually reported form (absencestatus) is generally thought to occur mainly inpatients with the Lennox-Gastaut syndrome,although children with the less commonmyoclonic-astatic epilepsy are said to be par-ticularly prone.2 The present findings are inkeeping with such reports as 60% of the seriescame from within these two categories ofseizure disorder. The results also indicate thatchildhood NCSE almost always complicates apre-existing epilepsy.

Relatively few cases in the present serieswere suspected to be NCSE on referral to thePark Hospital series. There are probably twomain reasons for this: (1) the relatively non-specific nature of the mental changes oftenseen and lack of familiarity with NCSE as apossible explanation for such changes, and (2)the subtlety of the clinical manifestations insome cases, as mentioned earlier.

In cases where the behavioural changes wereprominent, reduction in activity and mentalprocessing seemed to be equally a feature ofthe examples of generalised, complex partial,and mixed or transitional types of NCSE.Although more florid manifestations might beexpected in seizures of temporal lobe origin,these were not convincingly recorded. This isin keeping with the evidence from pub-lished reports that there is no clear cutseparation in the clinical symptomatology of

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the different types of NCSE, at least inchildren.1

Fluctuation of awareness, which has beenclaimed to be a useful diagnostic sign ofNCSE, was often noted in the present series.Cyclical alternation between complete unre-sponsiveness - speech arrest and stereotypedautomatisms (associated with temporal lobedischarges) and partial responsiveness - partialspeech and apparently purposeful automatisms(associated with bilateral slow activity and lowvoltage fast activity in the EEG) - is said to bea feature of complex partial status in adults.8This was observed in only two children in thisseries.There seems to be nothing specific in these

obvious psychological manifestations ofNCSEalthough the presence of myoclonic jerks,either seen or detected on palpation, is stronglysuggestive of the condition. That being so, asin this series explanations for the mentalchanges other than NCSE may be entertained.These include organic factors, for exampleoverdosage with antiepileptic drugs, postictalstates, or progressive cerebral pathology.Alternatively, a primarily psychiatric diagnosisis made such as depression, hysteria, orpsychosis.The subtle mental changes sometimes

associated with even gross EEG abnormalitycan constitute a major obstacle to correct diag-nosis. This curious dissociation illustrates that,although related to each other to some degree,the clinical and electrographic phenomenadepend on different systems. In this series thefactors generally predictive of obvious clinicaleffect of the seizure discharge were male sex,learning disability before the onset of theseizure disorder, and generalised seizure dis-charge. It is in the more subtle forms ofNCSEthat the use of prolonged EEG monitoring,especially by means of ambulatory cassetterecordings combined with good clinical obser-vations, can be particularly helpful in childrenwhere this condition is suspected.

Clear cut precipitants ofNCSE seemed veryfew in this series. They may well have beenunderestimated by failure to inquire aboutthem at the time or by inadequately accuraterecall of past events and circumstances. A widerange of possibilities exists, including intercur-rent illness, withdrawal of medication, or emo-tional factors, which might be particularlydifficult to identify retrospectively because ofinformants' own involvement in the situation.It is, however, accepted that NCSE may occurwithout any specific precipitating factor.

Both immediate and prophylactic treatmentpredictably posed problems in the presentgroup of children. First, in only about half thechildren was any attempt made to terminatethe episode of NCSE once it had been diag-nosed. This approach, which contrastsmarkedly with that towards convulsive statusepilepticus, presumably arises from the beliefthat the episode will resolve spontaneously andno particular harm will be done in the mean-time. The first of these assumptions is correctalthough, as has already been described, theepisode may last for a long while, and during

this period the child's general wellbeing iscompromised. Unfortunately, where NCSE istreated with some degree of urgency, theresults can be disappointing even when a rangeof treatments are attempted in turn.9 10

Prevention of the recurrence of NCSE byadjustments to continuous medication can besimilarly difficult. Although there seemed to bea trend in the present series for the use ofsodium valproate in particular to be associatedwith non-recurrence of NCSE (in keeping withreports from other sourcesl1), the majority ofthe children continued to have further bouts ofNCSE in the follow up period. The generalimpression gained is that poor prognosis appliesmainly to patients with generalised brain dam-age although in the present series, as in otherreports, it was difficult to judge the thorough-ness with which prevention of further NCSEepisodes had been attempted. More convincingtherapeutic effects may emerge in the futurewith the use ofnewer antiepileptic drugs.The frequent failure to recognise episodes of

NCSE at an early stage, the apparent length ofsome of the episodes, and the commonabsence of prompt treatment or inability toprevent further occurrences are all particularlyworrying features in the present series, in viewof the concern that has been expressed forsome time by a number of authors that pro-longed exposure to NCSE may cause demen-tia.7 12-14 Some support is lent to this fear byexperimental studies which seem to implicateprolonged seizure discharge per se in neuronaldamage.'5 This matter is far from resolved butit is noteworthy how often children in thispresent series showed definite or intellectualdecline over the course of a seizure disorder ofwhich periods of NCSE had been a part. Theinformation available in this study does notpermit any accurate analysis of the nature ofsuch deterioration, or the ways in which itmight have come about.

Detailed prospective studies, with system-atic documentation of cases including neuro-psychological assessment, are clearly requiredto settle these important issues. In particular,there is need to clarify the relative contribu-tions to intellectual decline (and other behav-ioural changes) of NCSE, the underlyingcondition of which the epilepsy is a part, andother aspects of the seizure disorder and itstreatment. In the meantime, however, it isimportant to improve the recognition ofNCSEand treat it more vigorously than is usually thecase. NCSE should be particularly suspectedin children with epilepsy who undergo anotherwise inexplicable change of behaviour.EEG studies will usually be helpful, especiallyif the results can be compared with thoseobtained before the change of behaviour.Treatment should involve attempts to termi-nate the episode and to prevent recurrences.Monitoring of the child's behaviour by meansof parents' and teachers' observations shouldaid early detection of further episodes.

1 Stores G. Nonconvulsive status epilepticus in children. In:Pedley TA, Meidrumi BS, eds. Recent advances in epilepsynumber 3. Edinburgh: Churchill Livingstone, 1986:295-310.



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3 Cascino GD. Nonconvulsive status epilepticus in adults andchildren. Epilepsia 1993; 34 (suppl 1): 521-8.

4 Tassinari CA, Bureau M, Dravet C, Dalla Bemadina B,Roger J. Epilepsy with continuous spikes and wavesduring slow sleep - otherwise described as ESES (epilepsywith electrical status epilepticus during slow sleep). In:Roger J, Bureau M, Dravet C, Dreifuss FE, Perret A,Wolf P, eds. Epileptic syndromes in infancy, childhoodand adolescence, 2nd Ed. London: John Libbey, 1992:245-56.

5 Stores G, Bergel N. Clinical utility of cassette EEG in child-hood seizure disorders. In: Ebersole JS, ed. AmbulatoryEEG monitoring. New York: Raven Press, 1989.

6 Commission on classification and terninology of theInternational League Against Epilepsy. Proposal forrevised classification of epilepsies and epileptic syn-dromes. Epilepsia 1989; 30: 389-99.

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epilepticus. In: Delgado-Escueta AV, Wasterlain CG,Treiman DM, Porter RJ, eds. Advances in neurology volume34: status epilepticus. New York: Raven Press, 1983: 69-81.

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11 Berkovic SF, Andermann F, Guberman A, Hipola D,Bladin PF. Valproate prevents the recurrence of absencestatus. Neurology 1989; 39: 1294-7.

12 Livingstone S, Torres I, Pauli LI, Rider RV. Petit malepilepsy; results of a prolonged follow up study of 117patients. JAMA 1965; 194: 227-32.

13 Ohtahara S, Oka E, Yamatogi Y, et al. Non-convulsivestatus epilepticus in childhood. Folia Psychiatr NeurolJ7apn1979; 33: 345-51.

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