Critérios de NCSE Kaplan 2012

Epilepsia, 53( 53(Sup Suppl. pl. 3): 3):1–51 1–51,, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

EEGS EE GS IN NO NONC NCON ONVU VULS LSIV IVE E ST STAT ATUS US EP EPIL ILEP EPTI TICU CUS S

Electroen Electr oencep cephal halogr ographi aphic c cri criter teria ia for non noncon convul vulsiv sive e stat st atus us ep epil ilep epti ticu cus: s: Sy Syno nops psis is and co comp mpre rehe hens nsiv ive e su surv rvey ey *yRa Raou oull Su Sutt tter er an and d yPe Pete terr W. Ka Kapl plan an *Divis *Di vision ion of Neu Neurosc roscien iences ces Crit Critical ical Care Care,, Dep Depart artmen ments ts of Ane Anesth sthesi esiolog ology y and Crit Critica icall Care Med Medicin icine, e, The Joh Johns ns Hop Hopkin kinss Uni Univer versit sity y Sch School ool of Med Medicin icine, e, Bal Baltim timore, ore, Mar Maryla yland, nd, U.S U.S.A.; .A.; and andy Department tment of Neurol Neurology, ogy, yDepar The Joh Johns ns Hop Hopkin kinss Bay Bayvie view w Med Medica icall Cen Center ter,, Bal Baltim timore, ore, Mar Maryla yland, nd, U.S U.S.A. .A.

sents clin sents clinica icall desc descrip riptio tions ns and EEG pat patter terns ns of NCSE in the neonatal period, infancy, childhood, adulthood, and late adulthood from a syndromic perspective based on age, encephalopathy, cerebral development, development, etiolo etiology, gy, and syndro syndrome. me. Proceeding ceedin g from the propos proposed ed classifi classification cation of statu statuss epilepticus epilep ticus syndromes in ‘‘Stat ‘‘Status us epilep epilepticus: ticus: its clinica clin icall fea featur tures es and tre treatm atment ent in chi childr ldren en and adults’’ (published in 1994 by Cambridge University Press, New York), we have performed a systema te mati tic c se sear arch ch fo forr re repo port rtss pr pres esen enti ting ng EE EEG G patterns of NCSE using the online medical search engine PubMed for 22 different search strategies. EEG patterns were reviewed by two board-certified fie d ep epil ilep epto tolo logi gist stss wh who o re reac ache hed d co cons nsen ensu suss rega re gardi rding ng pr pres esenc ence e of NC NCSE SE.. Fr From om a to tota tall of 4, 4,32 328 8 search results, 123 cases with corresponding EEG patterns could be allocated to underlying epilepsy syndro syn dromes mes.. Typ Typical ical cha charact racteri eristi stic, c, pro promin minent ent electrograp elect rographic hic patte patterns, rns, and sequen sequential tial arrang arrangeements are elucidated for the different NCSE syndromes. This compendium of patterns by NCSE syndrome classification with illustration of EEGs, and delinea delineation tion of elect electroence roencephalog phalographic raphic features helps define the characteristics and semiologi lo gic c bo bord rder erlin lines es am amon ong g th the e ty type pess of NC NCSE SE.. KEY KE Y WO WORD RDS: S: Epilepsy, Epilepsy, Non Noncon convul vulsiv sive e sta status tus epilep epi lepticu ticus, s, Ele Electr ctroen oencep cephalo halograp graphic hic cri criter teria, ia, Diagnosis Diagno sis crite criteria, ria, Clinical syndr syndromes, omes, Electr Electroenoencephalographic patterns, Neonatal, Infants, Childhood, hoo d, Adu Adults lts,, Late life life..

SUMMARY There have been many attempts at defining the electroence electr oencephalogr phalography aphy (EEG) charac characteristi teristics cs of noncon non convul vulsiv sive e sta status tus epi epilep leptic ticus us (NC (NCSE) SE) wit withou houtt a universally accepted definition. This lack of consens se nsus us ar arise isess be beca caus use e the EE EEG G ex expr press essio ion n of NC NCSE SE does not exist in isolation, but reflects status epilepticus under the variety of pathologic conditions that th at oc occu curr wi with th ag age, e, ce cere rebr bral al de deve velo lopm pmen ent, t, encephalopath enceph alopathy, y, and epileps epilepsy y syndro syndrome. me. Curre Current nt NCSE definitions include ‘‘boundary conditions,’’ in which electr electroencep oencephalogr halographic aphic seizur seizure e activi activity ty occurs without apparent clinical seizures. Furthermore, what what appears to to one interpreter interpreter as as status epiepileptic lep ticus us,, is no nott to ano anoth ther er rea reader der,, refl reflec ectin ting g th the e ‘‘a ‘‘art rt’’ ’’ of EEG int interpr erpreta etation tion.. Seiz Seizures ures and epil epileps epsy y syndromes dro mes hav have e und underg ergone one an evo evoluti lution on tha thatt has moved beyond a classification of focal or generalized ize d co cond ndit itio ions ns int into o a sy synd ndro romi mic c ap appr proa oach ch.. It seems appropriate appropriate to make similar changes changes in the EEG analysis of the syndromes of NCSE. In effect, the lite literat rature ure on epi epilep lepsy sy cla classifi ssificat cation ion has pro pro-gressed to incorporate the different NCSE types with clinical descriptions, but the specific EEG evidence for these types is found largely in individual reports, repor ts, and often by description description only. NCSE classification of EEG patterns should derive from the aggreg agg regate ate of pub publish lished ed EEG pat patter terns ns in the res respec pec-tive clinical subtype, supported by an analysis of these EEG studies. The analysis that follows pre-

Address correspondence to Peter W. Kaplan, Department of Neurology, Johns Hopkins Bayview Medical Center, 301 Mason Lord Drive, Suite 2100, Baltimore, MD 21224, U.S.A. E-mail: [email protected] or Raoul Sutter, Division of Neurosciences Critical Care, Department of Anesthesiolo Anesth esiology, gy, Critic Critical al Care Medicine and Neurol Neurology, ogy, Johns Hopkins University Univer sity School of Medic Medicine, ine, Baltimore, Maryland, U.S.A. E-mail: rsutter rsut ter3@j 3@jhmi hmi.ed .edu u unti untill Jul July y 2013 2013;; fro from m Aug August ust 2013 for forwar ward: d: Department Depart ment of Neurol Neurology ogy and Intens Intensive ive Care Unit, University University Hospit Hospital al Basel,Petersgraben Basel,Petersgra ben 4, 4031Basel, Swit Switzerlan zerland. d. E-mailsutterr@ [email protected] uhbs.ch

Noncon Non convul vulsiv sivee sta status tus epi epilep lepticu ticuss (NC (NCSE) SE) has bee been n defined as a state of ongoing (or nonrecovery between) seizur sei zures es wit withou houtt con convuls vulsion ions, s, usu usually ally for mor moree tha than n 30 min (Shorvon, 1994; Kaplan, 1996). When diagnosing NCSE, the clinician faces challenges in correlating suggestiv ges tivee cli clinic nical al fea feature turess wit with h ele electro ctroenc enceph ephalo alograp graphy hy (EEG) patterns to arrive at a diagnosis of NCSE. The con-

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R. Su Sutt tter er an and d P. W. Ka Kapl plan an firmation of NCSE is largely based on the EEG, given the nonspe non specif cific ic and ple pleomo omorphi rphicc cli clinica nicall man manife ifesta statio tions. ns. Proposed EEG criteria for NCSE are directed mainly at form fo rmss of NC NCSE SE se seen en in ad adul ults ts (Y (You oung ng et al al., ., 19 1996 96;; Kaplan, 2007). This approach has not been used in pediatric patients, as the EEG appearance of NCSE in early life li fe is fu fund ndam amen enta tall lly y in infl flue uenc nced ed by ag age, e, ce cere rebr bral al maturi mat urity, ty, pre presen sence ce of enc enceph ephalo alopat pathy, hy, and und underl erlyin ying g epile ep ilepsy psy sy synd ndrom romes es,, an and d NC NCSE SE do does es no nott le lend nd it itse self lf easily to a set of EEG criteria. Several different epileptic enceph enc ephalo alopat pathie hiess occ occurr urring ing in neo neonat natals als,, inf infant ants, s, and childre chi ldren n may app appear ear as con continu tinuous ous or sub subcon contin tinuou uouss epilep epi leptifo tiform rm act activit ivity, y, suc such h as in Wes Westt syn syndro drome, me, wit with h hypsarrhythmia (Riikonen, 2005), and in other forms of malignant epilepsies of childhood, such as in Ohtahara (Ohtah (Oh tahara ara & Yam Yamato atogi, gi, 200 2006) 6) and Dra Dravet vet syn syndro drome me (Dra (D rave vett et al al., ., 20 2005 05). ). In ot othe herr le less ss-s -spe pecif cific ic ca case ses, s, ence en ceph phal alop opath athy y ca can n be du duee to nu nume mero rous us et etio iolog logie ies, s, including peripartum anoxia, metabolic disorders, infection, tio n, or dev develop elopmen mental tal dis disturb turbanc ances, es, in whi which ch NC NCSE SE may present less-specific features. Fordiagnosi Fordiagn osis, s, theart of andtraini andtraining ng forEEG int interpr erpreta etatio tion n ‘‘seizures’’ ’’ or ‘‘seizure are key to the identification identification of ‘‘seizures or ‘‘ seizure activity,’’ ity, since many epileptiform morphologies may not alone ’’ since represent seizures. Some nonseizure, epileptiform examples include ‘‘ include ‘‘interictal interictal’’ periodic discharges that may be ’’ periodic seen focally, in a generalized pattern, independently/bilaterally, era lly, or whe when n bro brough ughtt out by stim stimula ulatio tion n — periodic periodic lateralized epileptiform discharges (PLEDs), generalized period per iodic ic epi epilep leptifo tiform rm dis discha charges rges (GP (GPED EDs), s), bil bilate ateral ral independent periodic lateralized epileptiform discharges (BIPLEDs), and stimulus-induced rhythmic, periodic, or ictal discharges discharges (SIRPI (SIRPIDs), Ds), respectively. respectively. These discharges discharges have been described as lying along an ictal–interictal continuum ranging from the interictal isolated epileptiform discharge (Chong & Hirsch, 2005), through clustering, or an increased frequency of periodic discharges, to seizures and status epilepticus. There has been an ongoing effort reflected in three international colloquia to define EEG criteria of NCSE (Walker et al., 2005; Shorvon et al., 2007; Trinka & Shorvon, 2009). One challenge to this corralling of EEG characteristics under one roof has been the recognition that just as there are many epilepsies, there are many types of status epilepticus and hence NCSE. Over the last 20 some years, with the increasing recognition of — init NCSE — NCSE i nitia iall lly y id iden entif tifie ied d in am ambul bulat ator ory y co conf nfus used ed — there patien pat ients, ts, and in mil mildly dly con confus fused ed hos hospit pitali alized zed pat patien ients ts — there hass be ha been en in incr crea easin sing g id iden enti tific ficati ation on in le leth thar argi gicc an and d comatose patients in intensive care units. EEG EE G de defin finiti ition onss for NC NCSE SE ha have ve be been en at attem tempt pted ed by reducing the EEG analysis and diagnosis to one of patterns with particular characteristics. characteristics. These were judged to reflect special, spec ial, diag diagnost nostical ically ly impo importan rtantt char characte acterist ristics ics in frequency,, amplitud quency amplitude, e, morphol morphology, ogy, and evolutio evolution n domains. Such Su ch ef effor forts ts ha have ve led to cr crite iteri riaa tha thatt may loo loosel sely y fit all typ types es Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.15 10.1111/j.1528-1167.2012 28-1167.2012.03593.x .03593.x

of NCS NCSE. E. How Howeve ever, r, they larg largely ely and reli reliably ably are appl applicab icable le to the more obvious cases of NCSE, and avoid the more conte co ntenti ntious ous mid middle dle-g -gro round und th that at may lie fur furthe therr dow down n the ictal–inte tal– interict rictal al cont continu inuum. um. What is need needed ed to supp suppleme lement nt EEG definitions for NCSE is an approach contoured to the specific settings and syndromes in which these states exist, and culled from peer-reviewed literature that established status in these cases with EEG documentation. These tailored lore d char characte acteriza rization tionss wou would ld help diff differen erentiat tiatee more clearly clea rly seiz seizures ures or stat status us epil epilepti epticus cus from nons nonseizu eizures, res, leaving less of an uncertain middle-ground, and would reside in a syndromic context for the various NCSEs. Previously published criteria include descriptions of the morphologie morph ologies, s, discha discharge rge freque frequencies, ncies, evolu evolution tion pattern patterns, s, and secondary criteria for NCSE (Young et al., 1996; Claassenet al., 2004;Kaplan, 2007).Incl 2007).Include uded d arecha arechara racte cteris ristic ticss of EEG evolution, rhythmicity, and response to antiepileptic drug dr ugss (A (AED EDs) s).. How Howeve ever, r, the det determ erminat ination ion of stat status us epilepticus on EEG is inevitably subjective. In most publi‘‘leap ’’ to a cations on these entities, authors make the ‘‘ leap’’ diagnosis of status epilepticus without providing objective criteria of frequency, amplitude, morphology, and evolution of EEG characteristics, and often without showing the EEG. Illustrative figures of the EEG patterns are often abse ab sent nt,, ma may y be am ambi bigu guou ous, s, or ma may y sh show ow on only ly th thee mo most st ev eviident cases cases.. With these caveats in mind, this compendium compendium provid provides es the various EEG patterns seen in NCSE from a syndromic perspe per specti ctive, ve, and exp expand andss on acu acute te sym sympto ptomati maticc for forms ms based on etiology.

Mater Ma terial ial and Met Method hods s Setting and des Setting design ign This observational study was performed at the departmentt of Neu men Neurol rology ogy,, Joh Johns ns Hop Hopkins kins Bay Bayvie view w Med Medica icall Center Cen ter in Bal Baltimo timore, re, Mar Marylan yland, d, U.S U.S.A. .A. It is a com compen pendiu dium m of EEG patterns for NCSE in the neonatal period, infancy, childhood, adulthood, and late life. Data and case collection collection A sy syste stemat matic ic sea searc rch h fo forr ca case se rep repor orts, ts, ca case se se serie ries, s, or reviews presenting EEG patterns of NCSE in a syndromic context con text was perf performe ormed d usin using g the onli online ne med medical ical search engine PubMed (http://w (http://www.nc ww.ncbi.nlm.n bi.nlm.nih.gov/p ih.gov/pubmed) ubmed) for 22 search strategies (Table 1) according to the proposed revised revi sed clas classifi sificati cation on of stat status us epil epilepti epticus cus synd syndrome romess by Shor Sh orvo von n (19 (1994 94)) (T (Tab able le 2) 2).. Ca Case sess th that at pr pres esen entt fi figu gure ress of EE EEG G patterns meeting the criteria for NCSE, as defined below, in ‘‘boundary ’’ synassociati asso ciation on with unde underlyin rlying g epil epilepsy epsy or ‘‘ boundary’’ dromes as classified in Table 1 were selected by critical review rev iew of two boa boardrd-cer certif tified ied ep epile ilepto ptolog logist istss (RS and PWK). For all syndromes, one representative EEG figure and the corresponding clinical and EEG description was selected. For all the other identified cases, clinical and

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R. Su Sutt tter er an and d P. W. Ka Kapl plan an firmation of NCSE is largely based on the EEG, given the nonspe non specif cific ic and ple pleomo omorphi rphicc cli clinica nicall man manife ifesta statio tions. ns. Proposed EEG criteria for NCSE are directed mainly at form fo rmss of NC NCSE SE se seen en in ad adul ults ts (Y (You oung ng et al al., ., 19 1996 96;; Kaplan, 2007). This approach has not been used in pediatric patients, as the EEG appearance of NCSE in early life li fe is fu fund ndam amen enta tall lly y in infl flue uenc nced ed by ag age, e, ce cere rebr bral al maturi mat urity, ty, pre presen sence ce of enc enceph ephalo alopat pathy, hy, and und underl erlyin ying g epile ep ilepsy psy sy synd ndrom romes es,, an and d NC NCSE SE do does es no nott le lend nd it itse self lf easily to a set of EEG criteria. Several different epileptic enceph enc ephalo alopat pathie hiess occ occurr urring ing in neo neonat natals als,, inf infant ants, s, and childre chi ldren n may app appear ear as con continu tinuous ous or sub subcon contin tinuou uouss epilep epi leptifo tiform rm act activit ivity, y, suc such h as in Wes Westt syn syndro drome, me, wit with h hypsarrhythmia (Riikonen, 2005), and in other forms of malignant epilepsies of childhood, such as in Ohtahara (Ohtah (Oh tahara ara & Yam Yamato atogi, gi, 200 2006) 6) and Dra Dravet vet syn syndro drome me (Dra (D rave vett et al al., ., 20 2005 05). ). In ot othe herr le less ss-s -spe pecif cific ic ca case ses, s, ence en ceph phal alop opath athy y ca can n be du duee to nu nume mero rous us et etio iolog logie ies, s, including peripartum anoxia, metabolic disorders, infection, tio n, or dev develop elopmen mental tal dis disturb turbanc ances, es, in whi which ch NC NCSE SE may present less-specific features. Fordiagnosi Fordiagn osis, s, theart of andtraini andtraining ng forEEG int interpr erpreta etatio tion n ‘‘seizures’’ ’’ or ‘‘seizure are key to the identification identification of ‘‘seizures or ‘‘ seizure activity,’’ ity, since many epileptiform morphologies may not alone ’’ since represent seizures. Some nonseizure, epileptiform examples include ‘‘ include ‘‘interictal interictal’’ periodic discharges that may be ’’ periodic seen focally, in a generalized pattern, independently/bilaterally, era lly, or whe when n bro brough ughtt out by stim stimula ulatio tion n — periodic periodic lateralized epileptiform discharges (PLEDs), generalized period per iodic ic epi epilep leptifo tiform rm dis discha charges rges (GP (GPED EDs), s), bil bilate ateral ral independent periodic lateralized epileptiform discharges (BIPLEDs), and stimulus-induced rhythmic, periodic, or ictal discharges discharges (SIRPI (SIRPIDs), Ds), respectively. respectively. These discharges discharges have been described as lying along an ictal–interictal continuum ranging from the interictal isolated epileptiform discharge (Chong & Hirsch, 2005), through clustering, or an increased frequency of periodic discharges, to seizures and status epilepticus. There has been an ongoing effort reflected in three international colloquia to define EEG criteria of NCSE (Walker et al., 2005; Shorvon et al., 2007; Trinka & Shorvon, 2009). One challenge to this corralling of EEG characteristics under one roof has been the recognition that just as there are many epilepsies, there are many types of status epilepticus and hence NCSE. Over the last 20 some years, with the increasing recognition of — init NCSE — NCSE i nitia iall lly y id iden entif tifie ied d in am ambul bulat ator ory y co conf nfus used ed — there patien pat ients, ts, and in mil mildly dly con confus fused ed hos hospit pitali alized zed pat patien ients ts — there hass be ha been en in incr crea easin sing g id iden enti tific ficati ation on in le leth thar argi gicc an and d comatose patients in intensive care units. EEG EE G de defin finiti ition onss for NC NCSE SE ha have ve be been en at attem tempt pted ed by reducing the EEG analysis and diagnosis to one of patterns with particular characteristics. characteristics. These were judged to reflect special, spec ial, diag diagnost nostical ically ly impo importan rtantt char characte acterist ristics ics in frequency,, amplitud quency amplitude, e, morphol morphology, ogy, and evolutio evolution n domains. Such Su ch ef effor forts ts ha have ve led to cr crite iteri riaa tha thatt may loo loosel sely y fit all typ types es Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.15 10.1111/j.1528-1167.2012 28-1167.2012.03593.x .03593.x

of NCS NCSE. E. How Howeve ever, r, they larg largely ely and reli reliably ably are appl applicab icable le to the more obvious cases of NCSE, and avoid the more conte co ntenti ntious ous mid middle dle-g -gro round und th that at may lie fur furthe therr dow down n the ictal–inte tal– interict rictal al cont continu inuum. um. What is need needed ed to supp suppleme lement nt EEG definitions for NCSE is an approach contoured to the specific settings and syndromes in which these states exist, and culled from peer-reviewed literature that established status in these cases with EEG documentation. These tailored lore d char characte acteriza rization tionss wou would ld help diff differen erentiat tiatee more clearly clea rly seiz seizures ures or stat status us epil epilepti epticus cus from nons nonseizu eizures, res, leaving less of an uncertain middle-ground, and would reside in a syndromic context for the various NCSEs. Previously published criteria include descriptions of the morphologie morph ologies, s, discha discharge rge freque frequencies, ncies, evolu evolution tion pattern patterns, s, and secondary criteria for NCSE (Young et al., 1996; Claassenet al., 2004;Kaplan, 2007).Incl 2007).Include uded d arecha arechara racte cteris ristic ticss of EEG evolution, rhythmicity, and response to antiepileptic drug dr ugss (A (AED EDs) s).. How Howeve ever, r, the det determ erminat ination ion of stat status us epilepticus on EEG is inevitably subjective. In most publi‘‘leap ’’ to a cations on these entities, authors make the ‘‘ leap’’ diagnosis of status epilepticus without providing objective criteria of frequency, amplitude, morphology, and evolution of EEG characteristics, and often without showing the EEG. Illustrative figures of the EEG patterns are often abse ab sent nt,, ma may y be am ambi bigu guou ous, s, or ma may y sh show ow on only ly th thee mo most st ev eviident cases cases.. With these caveats in mind, this compendium compendium provid provides es the various EEG patterns seen in NCSE from a syndromic perspe per specti ctive, ve, and exp expand andss on acu acute te sym sympto ptomati maticc for forms ms based on etiology.

Mater Ma terial ial and Met Method hods s Setting and des Setting design ign This observational study was performed at the departmentt of Neu men Neurol rology ogy,, Joh Johns ns Hop Hopkins kins Bay Bayvie view w Med Medica icall Center Cen ter in Bal Baltimo timore, re, Mar Marylan yland, d, U.S U.S.A. .A. It is a com compen pendiu dium m of EEG patterns for NCSE in the neonatal period, infancy, childhood, adulthood, and late life. Data and case collection collection A sy syste stemat matic ic sea searc rch h fo forr ca case se rep repor orts, ts, ca case se se serie ries, s, or reviews presenting EEG patterns of NCSE in a syndromic context con text was perf performe ormed d usin using g the onli online ne med medical ical search engine PubMed (http://w (http://www.nc ww.ncbi.nlm.n bi.nlm.nih.gov/p ih.gov/pubmed) ubmed) for 22 search strategies (Table 1) according to the proposed revised revi sed clas classifi sificati cation on of stat status us epil epilepti epticus cus synd syndrome romess by Shor Sh orvo von n (19 (1994 94)) (T (Tab able le 2) 2).. Ca Case sess th that at pr pres esen entt fi figu gure ress of EE EEG G patterns meeting the criteria for NCSE, as defined below, in ‘‘boundary ’’ synassociati asso ciation on with unde underlyin rlying g epil epilepsy epsy or ‘‘ boundary’’ dromes as classified in Table 1 were selected by critical review rev iew of two boa boardrd-cer certif tified ied ep epile ilepto ptolog logist istss (RS and PWK). For all syndromes, one representative EEG figure and the corresponding clinical and EEG description was selected. For all the other identified cases, clinical and

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EEG Cri Criter teria ia for NCS NCSE E Table Tab le 1. Sear Search ch st stra rate tegi gies es us used ed fo forr da data ta acquisi acq uisitio tion n in Pub PubMed Med Life pe period

Search te terms

Neonatal and infantile ‘‘Nonconvulsive ‘‘Nonconvulsive status epilepsy syndromes epilepticus [title]’’ ‘‘West s yn yndrome [ ti title]’’ ‘‘Ohtahara s yn yndrome [title]’ ’ ‘‘Dravet s yn yndrome [ ti title]’’ Childhood epilepsy syndromes

‘‘Panayiotopoulos syndrome synd rome [title [title]’’ ]’’ ‘‘Ring chromoso chromosome me 20 synd syndrome rome [title] [title]’’’’ ‘‘A ‘‘ Ang ngel elma man n syndr dro ome[t me[tit itle le]’ ]’’’ ‘‘Rett s yn yndrome [ ti title]’’ ‘‘My ‘‘ Myoc oclo loni nicc as asta tati ticc ep epile ileps psyy [t [tit itle le]’ ]’’’ ‘‘El ‘‘ Elec ectr tric ical al St Stat atusepil usepilep eptic ticus[tit us[title] le]’’ ’’ ‘‘Land ‘‘L andauau-Kle Kleffn ffner er sy syndr ndrome[title ome[title]’’ ]’’

Search results resul ts (n) 287 378 39 106 68 15 465 46 5 1,325 36 52 190

Epilepsy synd Epilepsy syndrome romess in ‘‘Lenn ‘‘Lennox ox-Ga -Gasta staut ut sy syndr ndrome[title ome[title]’’ ]’’ childhoodand child hoodand ‘‘Ab ‘‘ Abse senc nce e st stat atusepi usepile lept ptic icus[tit us[title le]’ ]’’’ adulthood ‘‘To ‘‘ Ton nicst icstat atu us ep epil ilep epti ticcus [t [tit itle le]’ ]’’’

274 22 7

Epilepsy synd Epilepsy syndrome romess in ‘‘Li ‘‘Limb mbicsta icstatu tuss ep epil ilep epti ticu cuss [t [tit itle le]’ ]’’’ adulthoodand adult hoodand ‘‘Complex ‘‘Com plex parti partial al statu statuss late adult adulthood hood epilepticus [title]’’ ‘‘Late-onset nonconvu nonconvulsive lsive status epilepticus’’ ‘‘Late-life nonconv nonconvulsive ulsive status epilepticus’’ ‘‘Coma nonconvu nonconvulsive lsive status epilepticus’’ ‘‘Epi le leptic p sy sychosis [ ti ti tltle]’’ ‘‘Dr ‘‘ Drug ug-i -ind nduc uced ed st stat atusepi usepile lept ptic icus us’’ ’’ ‘‘Me ‘‘ Meta tabo boli licc st stat atusep usepil ilep epti ticu cus’ s’’’

33 91 52 3 367 47 65 406 40 6

EEG descriptions are provided. The quality of images varied depending on the resolutions of the image sources. ‘‘Bound ‘‘ ’’ were Boundary ary syndro syndromes mes’’ were def defined ined as con conditi ditions ons in which it was not clear to what extent the symptoms were ‘‘boundary due to NCSE (Shorvon, 1994). We classified ‘‘ boundary ’’ into syndromes’’ syndromes into the three following categories: (1) myoclonic status epilepticus in coma in the context of acute severe brain injury; (2) epileptic psychosis and behavior disturbance; and (3) confusional states with epileptiform EEG EE G ch chan ange gess (d (dru rugg-in indu duce ced d or me meta tabo boli lic) c).. In ea each ch,, patients had clinical nonconvulsive symptoms with ongoing seizure activity on the EEG interpreted as NCSE. Consensus on whether the EEG patterns and clinical syndromic descriptions were consistent with NCSE was reached after a second critical review. The EEG criteria for NCSE are presented below. Criteria for NCSE Criteria NCSE NCSE NC SE in ea earl rly y lif lifee ca can n be vi view ewed ed as an ep epile ilept ptic ic response respon se influe influenced nced and config configured ured by cerebr cerebral al devel developopment and integr integrity, ity, the presen presence ce or absen absence ce of enceph encephalopalopathy at hy,, th thee un unde derl rlyi ying ng ep epil ilep epsy sy sy synd ndro rome me,, an and d th thee

neuroanatomic location of seizure activity. It denotes a range ran ge of con conditi ditions ons in wh which ich EE EEG G seiz seizure ure act activi ivity ty is prolonged prolon ged and result resultss in typica typicall clinic clinical al nonco nonconvulsi nvulsive ve syndromes. The following criteria were used for the diagnosis of ‘‘Diagnosis NCSE in early life as proposed in the section ‘‘ Diagnosis of NCSE in children’’ children’’ of of the Oxford conference report in 2005 (Walker et al., 2005). Therefore, a continuous or virtually continuous dysrhythmia or paroxysmal activity on EEG is necessary. Furthermore, a continuous, abnormal electrical dysrhythmia may occur on EEG and be difficult to equate with the clinical state. Such electrical status that occurs every time the child goes to sleep is seen in Landau-Kleffner syndrome and some cases of Lennox-Gastaut syndrome. These continuous dysrhythmias may be acute or chronic. The diagnosis of NCSE ideally must consist of a combination of clinical and EEG features. Therefore, the following four clinical and electroencephalographic criteria for the diagnosis diagnosis of NCSE NCSE in early life were used: used: 1 Cl Clea earr cl clin inica icall ch chan ange ge in be beha havi vior or (m (man anife ifest sted ed as changes in cognition, memory, arousal affect, ataxia, motor learning, learning, and motor behavior) behavior) that lasted at least 30 min. min. The wor word d ‘‘ clear’’ thee co cont ntex extt of NC NCSE SE ‘‘clear ’’ in th implies that an adequate description of behavior before the onset of NCSE was available for comparison and the time of onset could have been defined, given that the onset can be gradual and the duration of the NCSE prolonged. 2 There must have been confirmation by clinical or neuropsychological examination of a clinical change. Continuous ous or virtua virtually lly contin continuous uous parox paroxysmal ysmal epi3 Continu sodes must have been present on EEG. 4 Continuous major seizures either tonic or clonic must have been absent. Alll of th Al thee ab abov ovee cr crite iteria ria had to be fu fulf lfill illed ed fo forr th thee diagnosis of NCSE in early life. A clinical response to anticonvulsant medication such as intravenous/oral benzodi zo diaz azep epin inee wi with th sim simul ulta tane neou ouss im impr prov ovem emen entt in th thee EEG and cli clinica nicall sym sympto ptoms ms add added ed fur furthe therr sup suppor portt to the diagnosis if positive, but did not exclude the diagnosis nos is if neg negati ative ve as pro propos posed ed by Liv Living ingston ston & Bro Brown wn (1987). For NCSE in adults and late adulthood, the definition from fro m the Oxf Oxford ord con confer ferenc encee on NC NCSE SE (Wa (Walke lkerr et al. al.,, 200 2005) 5) wasused as fol follow lows: s: (1)The dia diagno gnosis sis of NCS NCSE E wasdepen wasdepen-dent primarily on the presence of electrographic seizure activity. This allowed the inclusion, within the rubric of NCSE, of a range of ‘‘boundary conditions’’ in in which such ‘‘ boundary conditions’’ activity occurred but in which there were no obvious clini ‘‘seizures. ’’ (2) cal ‘‘ cal seizures.’’ (2) Electro Electrograph graphic ic seizure activity activity can take various forms, some of which clearly denote NCSE (clearcutt cr cu crit iteri eria) a) an and d so some me ofwhic ofwhich h ar aree le less ss ea easy sy to in inte terp rpre rett an and d probab pro bably ly den denote ote NC NCSE SE onl only y in som somee cas cases es (eq (equiv uivoca ocall cri criteteria). ria ). Thesix ‘‘ clear-cut’’ criteriaa includ included: ed: ‘‘clear-cut ’’ criteri Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.152 10.1111/j.1528-1167.2012 8-1167.2012.03593.x .03593.x

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R. Su Sutt tter er an and d P. W. Ka Kapl plan an Table Tab le 2. NC NCSE SE et etio iolo logy gy or cl clin inica icall co cont ntex ext, t, fo form rms, s, an and d re respo sponse nse to tr trea eatm tmen entt Syndrome NCSE in theneona NCSE theneonataland taland inf infant antile ile epi epilep lepsy sy syn syndro dromes mes West syndrome

Ohtahara syndrome Severe my m yoclonic ep epilepsy of of infancy (D (Dravet sy s yndrome) NCSE in in ot other fo f orms of of neonatal or or in i nfantile ep epilepsy NCSE in child childhood hood Earlyonset benig benign n child childhoodoccipital hoodoccipital epile epilepsy psy (Panayiotopoulos (Panayiotop oulos syndrome) NCSEin other form formss of child childhoo hood d epile epileptic ptic encephal ence phalopath opathies, ies, synd syndromes romes,, and etiolo etiologies, gies, (e.g. (e.g.,, ring chromosome chromosom e 20, Angelman syndrome, myoclonic–as myoclonic–astatic tatic epilepsy, epile psy, othe otherr child childhoo hood d myoc myoclonicencephal lonicencephalopat opathies hies)) Elec El ectr tric icalsta alstatu tuss ep epil ilep epti ticu cuss inslo insloww-wa wavesle vesleep ep

Landau-Kleffner sy syndrome

NCSE in adult adulthood hood (andchildhoo (andchildhood) d) with epile epileptic ptic encephalopathy NCSE in i n Le L ennox-Gastaut sy s yndrome

NCSEin otherforms of disru disrupted pted cereb cerebral ral devel developm opment ent (cryptogenic or symptomatic) NCSE in adult adulthood hood (andchildhoo (andchildhood) d) witho without ut epile epileptic ptic encephalopathy Typical ab a bsence st s tatus ep epilepticus

Etiology Etiol ogy or clini clinical cal context Various

Various Genetic Various

Poor Poor Various

Idiopathic

Autonomic s ta tatus epilepticus

Excellent

Various, usu Various, usually ally genetic genet ic or cryptogenic

Atypical abse Atypical absence nce and other nonspecific forms

Generally Gener ally poo poorr

Variou Vari ous,us s,usua uall llyy cryptogenic

No cli clinic nical al sig signs ns butongo butongoing ing electrogra electr ographic phic activ activity ity in sleep

Various, us usually cryptogenic

Clinical corr Clinical correlate elate of electrogra electr ographic phic activ activity ity is severe sever e spee speech ch distu disturban rbance ce

NCSEusually remits but may leave leave cognitive cogn itive defici deficits ts NCSEusually remits but may leave leave cognitive cogn itive defici deficits ts

Various, of o ften cryptogenic

Atypical abse Atypical absence nce statu statuss epilepticusand epilep ticusand tonic status epilepticus Various

Variable

Generalized absence

Excellent

Complex pa partial

Good

Confusional st s tate w itith psychiatric features Coma wi with sm small ir irregular myoclonicjerks myoc lonicjerks Simple Simpl e parti partial al (sen (sensory sory,, spec special ial sensory, cognitive)

Good

Generalized absence

Excellent

Various, often Various, cryptogenic

NCSE i n th the p os ostictal p ha hase o f TCSE Subtle st status ep epilepticus

Various

Aura continua

Various symptomat symp tomatic ic or cryptogenic

NCSE in late adulthoo adulthood d De n ov ovo a bs bsence s ta tatus e pi pilepticus

Responseto Resp onseto treatment or prog treatment prognosi nosiss

Infantile spasms wi with periods of NCSE with no clini clinical cal signsof signsof ongoing ongo ing epilep epileptic tic activ activity ity Tonic spasms Nonspecific Nonspecific

Idiopathic generalized epilepsy Various Vario us symptomat symp tomatic ic or cryptogenic Various

Complex parti Complex partial al statu statuss epilep epilepticus(limbic ticus(limbic and nonlimbic origin)

Clinical fo form

Psychotropic drug withdrawa withd rawall or idiopathic generalized epilepsy

Poor

Poor

Variable Good

Boundary syndromes Coma with epilep epileptifor tiform m EEG chan changes ges Epileptic behavioral disturbance or psychosis Drug-ind Drug -induced uced or metab metabolic olic con confusio fusional nal state with epileptifo epile ptiform rm EEG chan changes ges

Adapted from the revis Adapted revised ed classification classificationss of statu statuss epile epilepticu pticuss in child children ren and adults according according to Shorv Shorvon on (1994 (1994). ). NCSE, nonconvulsive status epilepticus; EEG, electroencephalography.

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EEG Cri Criter teria ia for NCS NCSE E 1 Frequent or conti continuous nuous focal electro electrographi graphicc seizur seizures, es, with ictal patterns that wax and wane with change in amplitude, frequency, and/or spatial distribution. 2 Frequen Frequentt or contin continuous uous gener generalized alized spike-wave spike-wave discharges in patients without a previous history of epileptic encephalopathy or epilepsy syndrome. 3 Freq Frequent uent or con continu tinuous ous gen genera eraliz lized ed spik spike-w e-wave ave discharges, which showed significant changes in intensity or freq frequenc uency y (us (usual ually ly a fas faster ter freq frequen uency) cy) when comp compared ared to baseline EEG, in patients with an epileptic encephalopath lop athy y or epi epileps lepsy y synd syndrome rome.. PLEDss or BIPED BIPEDss that occur occurred red in patients in coma in 4 PLED the aftermath of a generalized tonic–clonic status epilepticus leptic us (subtle status epilept epilepticus). icus). 5 EEG patterns that were less easy to interpret included: Freque Fre quent nt or con contin tinuou uouss EEG abn abnorma ormalit lities ies (sp (spike ikes, s, sharp-waves, rhythmic slow activity, PLEDs, BIPEDs, GPED GP EDs, s, tri triph phasi asicc wa wave ves) s) in pa pati tien ents ts wh whose ose EE EEGs Gs show sh owed ed no pr prev evio ious us si simi mila larr ab abno norma rmali litie ties, s, in th thee contex con textt of acu acute te cer cerebr ebral al dam damage age (e. (e.g., g., ano anoxic xic bra brain in damage, damag e, infect infection, ion, traum trauma). a). 6 Frequent or continuous generalized EEG abnormalities in patien patients ts with epileptic encephalopathies encephalopathies in whom similar interictal interictal EEG patterns were seen, but in whom clinical symptoms were suggestive of NCSE. Categories 3 and 6 reflect the problem of deciding the significance of spike-wave discharges in the setting of epileptic encephalopathy (e.g., Lennox-Gastaut syndrome) in which the ictal and interictal EEG patterns may be very similar. The differentiation of the two is problematic. Category 5 reflects the difficulty of differentiating patterns of epileptic discharges that may lie along an ictal–interictal continuum.

Results From a total of 4,328 search results, 125 cases with clinical descri clinical descriptions ptions and EEG patterns met the criteria for NCSE. For each syndrome, one representative EEG pattern is presented and reports from all identified EEG patt pa tter erns ns ar aree co comp mpou ound nded ed an and d in inde dexe xed d se sepa para rate tely ly (Figs. 1–43). We note that the quality of the EEG figures ur es ma may y be lim limit ited ed.. Th This is ar aris ises es fr from om th thee lit liter erat atur ureebased source of the images. A synthesis of the significant EEG morphologies and evolutions of the individual NCSE syndromes arranged accord acc ording ing to the cla classi ssific ficati ation on of NC NCSE SE syn syndro dromes mes of Shorvo Sho rvon n (1) is pro provid vided ed in Tab Table le 3.

NCSE fro NCSE from m a syn syndrom dromic ic per perspe specti ctive. ve. An una unambi mbiguguouss de ou defi finit nitio ion n of NC NCSE SE th that at ad adeq equa uate tely ly co cove vers rs al alll ‘‘bound ’’ remains types includ including ing ‘‘ boundary ary syndr syndromes omes’’ remains elu elu-sive si ve.. Th Ther eree ar aree se seve veral ral co cond nditi ition onss in wh whic ich h th ther eree is good evidence of ongoin ongoing g electr electrograph ographic ic epilep epileptiform tiform acti ac tivi vity ty bu butt in wh whic ich h th thee cl clin inica icall sy symp mpto toms ms ar aree no nott conven con ventio tional nally ly con conside sidered red to be epi epilep leptic. tic. The def definiinition tio n pro propos posed ed and acc accept epted ed dur during ing the Oxf Oxford ord con confer fer-ence en ce on NC NCSE SE (W (Wal alke kerr et al al., ., 20 2005 05)) de defin fines es NC NCSE SE as a ran range ge of con condit dition ionss in whi which ch ele electr ctrogr ograph aphic ic sei sei-zure zu re ac acti tivi vity ty is pr prol olon onge ged d an and d re resu sult ltss in no nonc ncon onvu vullsivee cli siv clinic nical al symp symptom toms. s. Thi Thiss der derives ives fro from m an ear earlie lierr defi de fini nitio tion n (S (Sho horvo rvon, n, 19 1994 94). ). So Some me po poin ints ts ar aree wo wort rth h emphasizing. empha sizing. (1) The definition is depen dependent dent primarily on th thee pr prese esenc ncee of el elec ectro trogr grap aphi hicc se seiz izur uree ac activ tivity ity.. Thiss all Thi allows ows the inc inclus lusion ion,, wit within hin the rubric of NCS NCSE, E, ‘‘bound ’’ as des of a range of ‘‘ boundary ary condit conditions ions’’ descri cribed bed above. abo ve. In add additio ition, n, (2) ele electro ctrogra graphi phicc sei seizur zuree act activit ivity y can ca n ta take ke va vario rious us fo form rms. s. So Some me se segme gment ntss of EE EEG G pa pattterns ter ns tha thatt wer weree pre presen sented ted in the reviewed reviewed rep report ortss did not qua qualify lify for NC NCSE, SE, alth althoug ough h the cli clinic nical al des descri cripptions tio ns we were re su sugg gges estiv tivee of st statu atuss an and d we were re ex exclu clude ded d from fr om th this is st stud udy. y. Th Thee re reas ason onss fo forr ex excl clus usio ion n we were re absenc abs encee of epi epilep leptic tic ele element ments, s, suc such h as lac lack k of rhy rhyththmic act activi ivity, ty, lac lack k of pro progre gressio ssion, n, and no wax waxing ing and waning wan ing of ict ictal al pat pattern ternss (i.e (i.e., ., no cha change nge in amp amplit litude ude,, freque fre quency ncy,, and and/or /or spa spatial tial dis distrib tributi ution) on).. Thi Thiss may be explai exp lained ned by the fac factt tha thatt the published published EEG exc excerp erpts ts most mo stly ly sh show ow no mo more re th than an 10 10–2 –20 0 s of re reco cord rdin ing, g, wher wh erea eass th thee ci cite ted d ch chan ange gess so some meti time mess ma may y de deve velo lop p over ov er mu much ch mo more re th than an ju just st a fe few w se seco cond nds. s. On st stud udy y of the illustrated electrographic electrographic NCSE pattern patterns, s, particularr ele ula elemen ments ts wer weree ide identi ntifie fied d tha thatt wer weree see seen n in mos mostt synd sy ndrom romes es,, bu butt we were re no nott al alwa ways ys pa part rt of th thee cu curr rren entt sugges sug gested ted crit criteri eriaa for NC NCSE SE (Ta (Table ble 3). Bec Becaus ausee the these se elemen ele ments ts may con contrib tribute ute sub substa stanti ntially ally to rec recogn ogniti ition on and dia diagno gnosis sis of the cor corres respon pondin ding g NC NCSE SE syn syndro dromes mes,, we suggest adding them to the current criteria.

Summary

This study identifies and provides the various EEG patterns ter ns see seen n in NCS NCSE E fro from m a syn syndro dromic mic persp perspect ective. ive. In add addiition, it explor explores es borderline patterns and assoc associations iations with seizures, and it provides clinical and illustrative electroencephalographic descriptions that enable the clinicians to approach and categorize NCSE within the context of specific syndromes with clinical features and subtypes, rather than tha n usi using ng pre previo vious us dis distin tinctio ctions ns into com comple plex x par partial tial Discussion (focal)) and absen (focal absence ce (gene (generalize ralized) d) subtyp subtypes. es. It is hoped that To our knowledg knowledge, e, thi thiss is the first stu study dy ana analyz lyzing ing this compendium will help in moderating semiologic borand an d as asse semb mbli ling ng th thee cl clin inic ical al an and d EE EEG G pa patt tter erns ns of derline disputes on NCSE.

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R. Sutter and P. W. Kaplan Table 3. Prominent electrographic elements and EEG patterns for NCSE syndromes Syndrome NCSE in theneonataland infantile epilepsy syndromes West syndrome

Ohtaharasyndrome

Severe myoclonicepilepsy of infancy (Dravet syndrome)

NCSE in other forms of neonatal or infantile epilepsy NCSE in childhood Early-onset benign childhood occipital epilepsy (Panayiotopoulos syndrome)

NCSEin otherforms of childhood epileptic encephalopathies, syndromes, and etiologies

Electrical status epilepticus in slow-wave sleep Landau–Kleffner syndrome

Prominent elements or sequential arrangements

Generalized continuous or waxing and waning high-voltage polymorphicslow wave discharges (>200 lV) with interspersed multifocal, irregular spikes and sharp waves usually followed by voltage attenuation and irregular 2–4 Hz slow wave discharges. There may be periods of suppressionof background activity or a continuous burst-suppression pattern (Fig. 1A–F) Continuousburst-suppression pattern with repetitiveburstsof high-voltageslow waves (200 to >400 l V) interspersed with multifocal, irregular spikes followed by periods of near isoelectric suppression (Fig. 2A,B) Continuous or waxing and waning, periodic or pseudoperiodic frontal or frontotemporal spikes, whichmay be followed by slow waves in theawaketracing.Spikes tend to be triphasic instead of biphasic and subclinical discharges are slower than in Lennox–Gastaut syndrome. There are no polyspikes in sleep,and discharges that mimic tonic discharges show no recruiting pattern. No clinical tonic or electromyographic features on videoEEG awakeand sleeprecords. Usually background activity is slow and/or suppressed (Fig. 3) Various forms as definedfrom theOxford conference on NCSE (Walker et al., 2005) (Figs. 4 and5).

Waxing and waning low-voltage fast and rhythmic epileptic activity of 1–2.5 Hz predominantly in theoccipital regions, increasing in voltage (>200 lV) anddecreasing in frequency with rapid bilateral frontotemporal spreadingthat is followed by rhythmic spike-and-wave discharges with occipital predominance. Usually background activity is slow and desynchronized (Fig. 6A–E) Ring chromosome 20 syndrome:Generalized continuous or waxing and waning repetitive irregular spikes with frontalpredominance, followed by rhythmic or irregular high-amplitude slow waves at 3–4 Hzwith interspersed multifocal, irregular spikes. Usually the frequency of the spike-and-wave discharges increases, and the slow waves can get polymorphic. Usually background activity is slow and/or suppressed (Fig. 7A–C). Angelman syndrome: Generalizedcontinuous or waxing and waning rhythmic sharpwave discharges with frontocentral predominance. Usually background activity is slow and/or suppressed (Fig. 8A,B). Rett syndrome: Continuous or waxing and waning unilateral, multifocal or generalized spikes usually during 50% of slow wave sleep. Usually background activity is disorganized and desynchronized (Fig. 9A–D). Myoclonic-astatic epilepsy syndrome: Generalized continuous or waxing and waning slow wave discharges of 2–3 Hz with interspersedmultifocal, irregular spikes, polyspikes, and slow wave complexes. Electromyographic channels showmultifocal, erratic myoclonicjerks on a background of mild toniccontraction. The ictal activity then may blendinto a burst-suppression pattern (Fig. 10) Generalized continuous rhythmic or irregular spike-and-wave discharges of up to 3 Hz during slow-wave sleepwith a frontocentral, or posterotemporal predominance. Usually background activity is slow and/or suppressed (Fig. 12) Focal, multifocalor generalized continuous ornearlycontinuousrepetitive high-voltage spike or spike-and-wave discharges, which are activated in slow-wave sleep. The epileptic activity usually involves the dominant temporal area. Usually background activity is slow and/or suppressed (Fig. 13)

NCSE in adulthood (andchildhood) with epileptic encephalopathy NCSE in Lennox–Gastautsyndrome

Atypical absence statusepilepticus: Generalized continuous or waxingand waningirregular 2–2.5 Hz spike and polyspike-slow-wave discharges predominantly frontotemporal and usually with normal background activity (Fig. 14A,B). Tonic status epilepticus: Generalized repetitive runs of polyspikes at high frequencies of 16–20 Hz, beginning with low-voltage and increasing high-voltage (100 l V)and a 10 Hz recruiting rhythm of high-voltage from onset. The runs of polyspikes can be interspersed with slowwaves. Background activity may be disorganized and desynchronized (Fig. 15) NCSEin otherforms of disrupted cerebral Various forms as definedfrom theOxford conference on NCSE (Walker et al., 2005) (Figs 16 and17) development (cryptogenic or symptomatic)

Continued

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EEG Criteria for NCSE Table 3. Continued. Syndrome NCSEin adulthood(and childhood) without epileptic encephalopathy Typical absence statusepilepticus Complex partial status epilepticus (limbic and nonlimbic origin)

NCSEin the postictal phase of TCSE

Subtlestatus epilepticus

Aura continua

NCSE in late adult life De novo absence statusepilepticus Boundary syndromes Coma with epileptiform EEG changes Epileptic behavioral disturbance or psychosis Drug-induced or metabolic confusional state with epileptiform EEG changes

Prominent elements or sequential arrangements

Generalized continuousor waxingand waningrhythmic 3–4 Hzspike and polyspike-slow-wave discharges predominantly anterior and usually with normal background activity (Fig. 18) Limbic: Continuous or waxing and waning periodic or pseudoperiodicsharp wave discharges interspersed with low-voltage spikes and polyspike-and-waves with uni- or bilateral frontocentral predominance and usually generalized slow and/or suppressed background activity. Waxing and waning rhythmic delta activity, only (Fig. 19). Nonlimbic: Continuous or waxing and waning periodic or pseudoperiodicsharp waves and spike-and-wave dischargeswith unilateral, focal onset and frequent seizure progression into generalized sharp wave and slow, and/or suppressed wave discharges usually with frontal predominance and generalized slow background activity (Fig. 20) Generalized orpartial continuousor waxingand waningperiodicepileptic dischargesthatresemble PLEDs or GPEDs with a frontal predominance and usually generalized slow background activity (Fig. 21A,B) Generalized continuousorwaxing and waningperiodicepileptic dischargesresembling GPEDs that may be interrupted by short periods with nearly isoelectric suppression of 3–5 s. Usually background activity is slow and/or suppressed (Fig. 22) Unilateralcontinuousorwaxing and waning rhythmicspike-and-wave or high-voltage slow-wave discharges (>200 lV) usually with generalized slow and/or suppressed background activity (Figs. 23–30)

Generalized continuous or waxingand waningrhythmic3–4 Hz spike, polyspike-slow-wave discharges predominantly anterior and usually with normal background activity (Fig. 31) Generalized waxingand waningperiodicepilepticdischarges that resemble GPEDs with periods of nearly isoelectric suppression. Usually background activity is slow and/or suppressed (Fig. 34) Various formsas defined from the Oxford conference on NCSE (Walker et al., 2005) (Figs. 36–38) Various formsas defined from the Oxford conference on NCSE (Walker et al., 2005) (Figs. 39–43)

NCSE, nonconvulsive status epilepticus; PLEDSs, periodic lateralized epileptiform discharges; GPEDs, generalized periodic epileptiform discharges.


8

R. Sutter and P. W. Kaplan

Electroencephalographic Illustrations and Clinical Descriptions Index Page 1. NCSE occurring in the neonataland infantile epilepsy syndromes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

1a. NCSE in West syndrome (Blitz-Nick-Salaam, infantile spasms). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10 1b. NCSE in Ohtahara syndrome (early infantile epileptic encephalopathy with suppression-bursts). . . . . . . . . . . . . . 12 1c. NCSE in severe myoclonic encephalopathy of infancy (Dravet syndrome) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13 1d. NCSE in other forms of neonatal or infantile epilepsy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14 (i) Ring chromosome 14 syndrome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14 (ii) Systemic lupus erythematosus with encephalopathy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14 2. NCSE occurring only in childhood . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14

2a. NCSE in early onset benign childhood occipital epilepsy (Panayiotopoulos syndrome) . . . . . . . . . . . . . . . . . . . . . . 14 2b. NCSE in other forms of childhood epileptic encephalopathies, syndromes, and etiologies. . . . . . . . . . . . . . . . . . . . 16 (i) Ring chromosome 20 syndrome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16 (ii) Angelman syndrome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17 (iii) Rett syndrome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18 (iv) Myoclonic–astatic epilepsy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18 (v) NCSE in other myoclonic epilepsies in childhood (i.e., Lafora body disease) . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18 2c. NCSE in electrical status epilepticus in slow-wave sleep (ESES) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20 2d. NCSE in Landau-Kleffner syndrome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21 3. NCSE occurring in both childhood and adulthood . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21 With epileptic encephalopathy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 1

3a. NCSE in the Lennox-Gastaut syndrome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 1 (i) Atypical absence status epilepticus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21 (ii) Tonic status epilepticus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22 3b. Other forms of NCSE in patients with learning disability or disturbed cerebral development (cryptogenic or symptomatic) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25 Without epileptic encephalopathy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26

3c. Typical absence status epilepticus in idiopathic generalized epilepsy.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26 3d. Complex partial status epilepticus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26 (i) Limbic status epilepticus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26 (ii) Nonlimbic complex partial status epilepticus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28 3e. NCSE in the postictal phase of tonic–clonic status epilepticus (TCSE) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30 3f. Subtle status epilepticus (myoclonic status after convulsive status epilepticus). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30 3g. Aura continua . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30 (i) Sensory symptoms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30 (ii) Special sensory symptoms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32 (iii) Autonomic symptoms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32 (iv) Cognitive symptoms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34 4. NCSE in late adulthood . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35

4a. De novo absence status epilepticus of late onset . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35 4b. Other forms of NCSE in late adulthood . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 7


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EEG Criteria for NCSE 5. Boundary syndromes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 9

5a. Coma with epileptiform EEG changes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39 (i) Cryptogenic encephalitis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39 (ii) Hypoxic encephalopathy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39 5b. Epileptic behavioral disturbance or psychosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41 5c. Drug-induced or metabolic confusional state with epileptiform EEG changes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 45 (i) Drug-induced confusional state with epileptiform EEG changes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 45 (ii) Metabolic confusional state with epileptiform EEG changes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 49


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R. Sutter and P. W. Kaplan 8 months, Figure 1C,D at the age of 1 year and 6 months, and Figure 1E,F at the age of 1 year and 8 months. Widespread high-voltage slow waves, spikes, and sharp waves are observed at the age of 8 months, particularly during sleep (Fig. 1A,B). In Figure 1C, diffuse epileptiform dis1a. NCSE in West syndrome (Blitz-Nick-Salaam, charges occupy the tracing, when the patient showed proinfantile spasms) longed unresponsiveness without convulsive motions. The mother’s voice calling the name of patient (Fig. 1D; Case 1 Clinical/EEG description (Saito et al., 2010): A girl arrow) elicits a right-sided predominantly tonic seizure known for having West syndrome since the age of lasting several seconds. The epileptiform discharges are 3 months. EEG during wakefulness (Fig. 1A,C–E) and relatively localized to the right posterior areas in sleep (Fig. 1B,F). Figure 1A,B were recorded at the age of Figure 1E,F.

NCSE Occurring in the Neonatal and Infantile Epilepsy Syndromes

Figure 1. (A – F) NCSE in West syndrome (Saito et al., 2010). Calibration: Sensitivity not known. Epilepsia ILAE Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

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EEG Criteria for NCSE Case 2 Clinical/EEG description (Coulter, 1986): A 3-year 6-month-old boy with known West syndrome showed repetitive flexion of the neck and hips every 2–3 s during status epilepticus. He raised his arms, and then relaxed until the next spasm occurred. On some occasions his eyes were deviated to the right and the right leg jerked more than the left, but flexion spasms of the head and trunk were always present. Diffuse high-voltage bursts of polymorphic slow waves with interspersed spikes followed by voltage attenuation; single or serial sharp waves followed by a high-voltage slow waves with interspersed spikes and voltage attenuation; and sharp and slow waves followed by irregular 2–4 Hz

activity. Occasionally lateralized it was also at times seen diffusely. On many occasions, the voltage attenuation of one spasm was terminated by the onset of the next spasm. Scattered multifocal spikes, diffuse spikes and slow waves, and bursts of diffuse voltage attenuation persisted after status epilepticus. Although EEG resembled a burst-suppression pattern at these times, it could be distinguished because of the documented clinical spasms that accompanied the periods of voltage attenuation. On other occasions, an individual spasm was followed by a few seconds of disorganized slowing and multifocal spikes (hypsarrhythmia) before the next clinical spasm, which clearly distinguished the EEG from a burst-suppression pattern.

A

Figure 2. (A,B) NCSE in Ohtahara syndrome (Saneto & Sotero de Menezes, 2007). Calibration: 1 s per horizontal unit; 100 lV per vertical unit. Epilepsia ILAE

B


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R. Sutter and P. W. Kaplan 1b. NCSE in Ohtahara syndrome (early infantile epileptic encephalopathy with suppression-bursts) Case 1 Clinical/EEG description (Saneto & Sotero de Menezes, 2007): All EEG recordings from the first 5 years of a girl with Ohtahara syndrome showed a burst-suppression pattern consisting of high-amplitude bursts, 400– 2,000 lV, slow waves intermixed with multifocal spikes followed by near isoelectric suppression during wake and sleep states (Fig. 2A). A representative of burst-suppression pattern is shown when the patient was approximately 1 year old. This epoch (Fig. 2A) shows high-amplitude bursts of slow delta waves intermixed with multifocal spikes followed by near isoelectric suppression. A representative of burst-suppression pattern is presented when the patient was approximately 5 years old (Fig. 2B). This epoch shows high-amplitude bursts of slow delta waves with reduced multifocal spikes compared with the EEG pattern seen at a younger age. This high-amplitude slowing is again followed by near isoelectric suppression as seen in the EEG from a younger age. Case 2 Clinical/EEG description (Fusco et al., 2001): A 53-day-old female infant had alternation between wakefulness with eyes open and a state of apparent sleep with eyes closed, regular respiration, and poor response to external stimuli. During sleep there was a subtle sign concurrent with an EEG burst discharge,

consisting of a brief arrest of respiration. Tonic spasms were continuous on awakening and during wakefulness. In wakefulness there was a burst-suppression pattern with asymmetric discharge, more evident over the left side. There was tonic contraction of both deltoid muscles for the whole discharge and discontinued at the end of it. The discharge was spikier over the left hemi-megalencephalic hemisphere. Case 3 Clinical/EEG description (Fusco et al., 2001): A newborn girl showed persistent burst-suppression pattern. Each burst was associated with a complex tonic contraction involving the trunk, the arms, and the neck. Repetitive and at times periodic tonic seizures were associated with bursts of high-voltage generalized polymorphic polyspikes with frontocentral dominance. Between the bursts there was suppression. Case 4 Clinical/EEG description (Al-Futaisi et al., 2005): A girl with Ohtahara syndrome had suppression periods >40 s between high-amplitude 1-mV spike bursts lasting up to 5 s. Low-amplitude (30-lV) slow rhythmic (0.3– 0.7 Hz) sharp and slow waves gradually built up over the right temporocentroparietal regions (T6, C4, and P4) during the period of suppression period. These rhythmic slow sharp waves and slow waves over the right hemisphere persisted during the entire EEG without clinical signs. High-amplitude bursts were off-scale at this sensitivity.

Figure 3. NCSE in Dravet syndrome (Nabbout et al., 2008). Calibration: 1 s per horizontal unit; 100 lV per vertical unit. Epilepsia ILAE Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

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EEG Criteria for NCSE 1c. NCSE in severe myoclonic encephalopathy of infancy (Dravet syndrome) Case 1 Clinical/EEG description (Nabbout et al., 2008): An EEG pattern in the adolescent course. It combined frontal spikes (as couplet or triplet), which may have been followed by slow waves on the awake tracing. Sleep may have been activated 5–10 s of subclinical discharges of 8–9 Hz (Fig. 3). In Dravet syndrome, (1) spikes tend to be triphasic instead of biphasic, (2) subclinical discharges are slower (at 8–9 Hz) than in Lennox-Gastaut syndrome, (3) there are no polyspikes in sleep, and (4) discharges that mimic tonic discharges show no recruiting pattern and no clinical tonic or electromyography features on video-EEG awaking and sleeping records. There were no polyspikes in sleep, and discharges that mimic tonic discharges show no recruiting pattern and no

clinical tonic or electromyography features on video-EEG awaking and sleeping records. Case 2 Clinical/EEG description (Moseley et al., 2011): A 10-month-old boy developed continuous right facial twitching, left upper extremity tonic posturing, and accompanying oxygen desaturations. EEG revealed continuous generalized polyphasic periodic as well as right frontotemporal and left temporal epileptiform discharges. Case 3 Clinical/EEG description (Wakai et al., 1996): lctal EEG of a 1-year 7-month-oldboy disclosed persisting irregular spike-and-wave complexes in the left hemisphere, predominantly in the occipital and occipitotemporal areas. After administration of diazepamand midazolam, frequency of the spike-and-wave complexes gradually decreased, although the occipital spikes remained.

Figure 4. NCSE in ring chromosome 14 syndrome (Giovannini et al., 2010). Calibration: 1 s per horizontal unit; 50 lV per vertical unit. Epilepsia ILAE Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

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R. Sutter and P. W. Kaplan 1d. NCSE in other forms of neonatal or infantile epilepsy

alternating gestural automatisms, and vegetative symptoms. Continuous delta activity was resolved after intravenous bolus of phenytoin (Fig. 4; below).

(i) Ring chromosome 14 syndrome Case 1 Clinical/EEG description (Giovannini et al., 2010): At the age of 15 months this boy had afebrile repetitive seizures during sleep with staring, loss of consciousness, breathing difficulties, and generalized hypertonus, followed by four-limb clonias with a right mild predominance, resembling status epilepticus. EEG during seizure revealed bifrontal delta waves followed by an abrupt, 3-s flattening of background activity after which rhythmic anterior triphasic slow waves with intermingled spikes appeared. This was followed by left frontotemporal fast rhythmic spikes with rapid diffusion to the right frontotemporal regions. This activity rapidly generalized with prolonged irregular spike-waves, mostly 2–2.5 complexes/s, and stopped abruptly after 2 min with a diffuse flattening, followed by the reappearance of background rhythms. EEG recording showed bilateral frontal high-voltage continuous delta activity (Fig. 4; above) concomitant with a behavior characterized by confusion, hypotonia,

(ii) Systemic lupus erythematosus with encephalopathy Case 1 Clinical/EEG description (Korff & Nordli, 2007): An 11-year-old girl with systemic lupus erythematosus, seizures, and encephalopathy. EEG revealed PLEDs (parietal and posterior temporal irregular pseudorhythmic polyspike-and-wave discharges) with left-hemisphere predominance, but with a more diffuse manifestation (Fig. 5).

2.

N CS E O cc urr in g On ly i n Childhood

2a. NCSE in early onset benign childhood occipital epilepsy (Panayiotopoulos syndrome) Case 1 Clinical/EEG description (Specchio et al., 2010): Ictal recording (video-EEG) of a 7-year-old girl (Fig. 6A). The ictal discharge starts in sleep over the left occipital area with low-voltage fast activity, increasing

Figure 5. NCSE in systemic lupus erythematosus with encephalopathy (Korff & Nordli, 2007). Calibration: 1 s between gray vertical lines; 100 lV between horizontal lines. Epilepsia ILAE Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

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EEG Criteria for NCSE

Figure 6. (A – E) NCSE in Panayiotopoulos syndrome (Specchio et al., 2010). Calibration: Sensitivity not known. Epilepsia ILAE

in amplitude and decreasing in frequency, and quickly involving temporal and parietal areas. This epileptic activity persists over the right occipital area as independent spike-and-wave activity lasting 22 s. After 50 s, eyes are open and tachycardia is evident. (Fig. 6B) At 3 min, discharge is bilateral, and there are more pronounced slow waves over left posterior area (Fig. 6C). Next there is eye deviation and vomiting with EEG characterized by 2.5-Hz spike-and-waves over the left occipital region and delta waves over the frontal and temporal areas (Fig. 6D,E). After 7 min, the patient has complete loss of consciousness (Fig. 6D), after which the seizure ends (Fig. 6E); slow waves are evident and involve mainly the left hemisphere. Case 2 Clinical/EEG description (Specchio et al., 2010): Ictal recording of a boy 4 years 6 months of age. Seizure onset is characterized by subclinical low-voltage fast activity over the right occipital region during non–rapid eye movement (non-REM) phase II sleep. This activity persists over 3 min and child opens his eyes; rhythmic spikes are also evident over the right posterior region. After 4 min, wider epileptic activity, increasing in amplitude and decreasing in frequency, is evident over the right occipital area. The child is unresponsive and the ictal discharges are more diffuse.

After 11 min, over the occipital regions, high-voltage spikes-and-waves are evident (1–2 Hz), and on the bilateral frontal areas, there are high-amplitude rhythmic sharp waves synchronous with the occipital activity. At this stage, both tachycardia and tachypnea are evident on electrocardiography and airflow traces, respectively. The patient also has some episodes of retching. After 15 min, diazepam is administered intravenously and the epileptic activity becomes less rhythmic. After 19 min, the seizure gradually ends with slow sharp waves on the posterior regions of lower voltage on the right side. Case 3 Clinical/EEG description (Specchio et al., 2010): Ictal EEG of a child showed right temporooccipital spikes with delta waves over the left frontal area and vertex during chewing automatisms and left eye deviation. After 8 min, the activity persisted and tachycardia was evident (150 beats/min). This was followed by left-sided eyelid clonic jerks with persistent spike-andwave discharges, more pronounced over the right posterior areas, which became more rhythmic a few minutes later during abdominal clonic jerks. Seizure ended after midazolam was administered intravenously, and delta waves have involved the right hemisphere with higher amplitude over temporooccipital traces. Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

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Figure 7. (A – C) NCSE in ring chromosome 20 syndrome (Inoue et al., 1997). Calibration: 1 s per horizontal unit; 50 vertical unit (as shown in Fig. 13C). Epilepsia ILAE

2b.

NCSE in other forms of childhood epileptic encephalopathies, syndromes, and etiologies

(i) Ring chromosome 20 syndrome Case 1 Clinical/EEG description (Inoue et al., 1997): A 14-year-old girl with repetitive spikes in the right frontal region (Fig. 7A), followed by 3–4 Hz slow waves and frontal dominant bilateral 3-Hz spike-andwave complexes (Fig. 7B). Spike-and-wave complexes gradually lost the spike component with increasing frequency and became polymorphous (Fig. 7C). Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

lV

per

The seizure lasted 39 min. Verbal response was impaired to various degrees, ranging from simple slowness, perseveration, and inappropriate utterance to muteness. Case 2 Clinical/EEG description (Inoue et al., 1997): A 21year-old woman evinced frontal dominant irregular highvoltage slow waves with occasional spikes that lasted 40 min. The patient looked ‘‘indifferent and weary.’’ Verbal responses were short and often inappropriate. Complex mental action such as calculation or thinking was impossible.

17

EEG Criteria for NCSE Case 3 Clinical/EEG description (Inoue et al., 1997): A 31year-old woman with seizures at the age of 7 years that lasted up to 120 min. Frontal dominant slow-wave rhythm gradually increasing in amplitude with slow waves and spikes. The patient’s mental state fluctuated. She was mute and motionless when high-voltage slow waves became faster or were accompanied by spikes. Case 4 Clinical/EEG description (Inoue et al., 1997): A 25year-old man with first seizures at the age of 11 years. Irregular slow waves over the anterior region were replaced by 3–4 Hz repetitive spikes or spike-andwave complexes, which then decreased in frequency. The amplitude of the spikes and slow waves were higher on the right side. He was mute and his movements were slow. Case 5 Clinical/EEG description (Jacobs et al., 2008): A 4-year-old boy with up to 30 seizures a day of four recognizable types: (1) prolonged atypical absences; (2) tonic

posturing of the arms, extension of the neck and head turning to the left; (3) nocturnal hypermotor seizures with agitation; and (4) focal seizures with terror, visual hallucinations, and impaired consciousness. EEG changes during prolonged absences consisted of generalized suppression, 2–3 Hz rhythmic slow waves and 1 Hz spike-and-slowwave activity over both hemispheres with some focality. Variable EEG patterns with rhythmic slow waves and spike and slow waves recorded focally, followed by lowvoltage fast activity during the tonic phase of the seizure. (ii) Angelman syndrome Case 1 Clinical/EEG description (Weber, 2010): A 7-yearold boy with developmental delay was diagnosed for the first time at the age of 6 months. At the age of 30 months he had convulsive status epilepticus and at the age of 5 years he had atypical absences. He showed a change in his behavior with reduced activity and eye contact. His readiness to laugh was prominently reduced. EEG revealed continuous epileptic discharge with high-voltage sharp waves (Fig. 8A,B).

A

Figure 8. (A,B) NCSE in Angelman syndrome (Weber, 2010). Calibration: 1 s every four vertical lines; sensitivity not known. Epilepsia ILAE

B


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R. Sutter and P. W. Kaplan (iii) Rett syndrome Case 1 Clinical/EEG description (Nissenkorn et al., 2010): These patients with Rett syndrome showed evolution of EEG epileptic pattern in Rett syndrome according to age: Left central spikes during sleep in a 2-year-old girl (Fig. 9A). Multifocal spikes and disorganized background activity in a 3-year 6-month-old girl (Fig. 9B). Multifocal and generalized epileptic activity during 50% of slowwave sleep in a 6-year-old patient (Fig. 9C). Generalized epileptic activity during sleep that fulfills the criteria for ESES (electric status epilepticus during slow sleep) at the age of 7 years (Fig. 9D).

carbamazepine in the same boy who was awake and responsive. There was rhythmic background activity and no epileptiform activity.

(iv) Myoclonic–astatic epilepsy

Case 1 Clinical/EEG description (Fernandez-Torre et al., 2011): A 19-year-old woman with progressive myoclonus epilepsy of Lafora type. A tactile stimulus (Fig. 11; black arrow) elicited a burst of epileptiform discharges in keeping with the definition of stimulus-induced rhythmic, periodic, ictal discharges (SIRPIDs).

Case 1 Clinical/EEG description (Guerrini & Aicardi, 2003): A 4-year 6-month-old boy with myoclonic status epilepticus after carbamazepine. The child was unresponsive and in a sort of ‘‘stupor’’ accompanied by multifocal and generalized myoclonic jerks. EEG showed diffuse slow waves with intermingled multifocal, irregular spikes, and wave complexes (Fig. 10; left). Electromyographic channels showed multifocal, erratic myoclonic jerks on a background of mild tonic contraction. Figure 10 (right) shows polygraphic recording performed 24 h after withdrawal of

Case 2 Clinical/EEG description (Kobayashi et al., 2007): EEG from a boy during a series of spasms with a burstsuppression pattern during sleep with early myoclonic encephalopathy. The ictal activity of spasms blends with the postseries burst-suppression pattern. Myoclonus occurs in association with EEG bursts during sleep.

(v) NCSE in other myoclonic epilepsies in childhood (i.e., Lafora body disease)

Case 2 Clinical/EEG description (Corkill & Hardie, 1999): A 15-year-old boy with eyelid myoclonia during eye closure. Frequent multifocal, spontaneous, and action myoclonic

A

B

C

D

Figure 9. (A – D) NCSE in Rett syndrome (Nissenkorn et al., 2010). Calibration: 1 s per horizontal unit; 100 lV per vertical unit. Epilepsia ILAE Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

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Figure 10. NCSE in myoclonic–astatic epilepsy (Guerrini & Aicardi, 2003). Calibration: 1 s per horizontal unit; 100 lV per vertical unit. Mas, masseter; Orb, oris and OO, orbicularis oris; Delt, deltoid; W Ext, wrist extensors; W Flex, wrist flexors; APB, abductor pollicis brevis; Quad, quadriceps; L, left; R, right; AV, common average reference. Epilepsia ILAE

Figure 11. NCSE in other childhood myoclonic encephalopathies; Lafora body disease (Fernandez-Torre et al., 2011). Calibration: 1 s per horizontal unit; 100 lV per vertical unit. Epilepsia ILAE Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

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R. Sutter and P. W. Kaplan jerks affected the upper limbs. EEG showed absence status epilepticus with generalized polyspike-and-wave activity with photosensitivity (at 10 Hz). Case 3 Clinical/EEG description (Dhamija et al., 2011): A 10-month-old boy with myoclonic jerks. During myoclonic status epilepticus, EEG recording showed continuous generalized epileptiform discharges associated with body jerking, consistent with myoclonic status epilepticus. EEG showed 1–2 Hz generalized spike-and-wave discharges corresponding with myoclonic jerks. A longitudinal bipolar EEG montage revealed maximal discharges over bicentral parietooccipital regions. 2c. NCSE in electrical status epilepticus in slow-wave sleep (ESES) Case 1 Clinical/EEG description (Van Hirtum-Das et al., 2006): A 5-year-old girl with receptive and expressive language problems. In sleep: spike and sharp wave discharges over the vertex, left frontoparietal, and right central head regions independently (Fig. 12; before

subpial transection). These discharges occupied >85% of stage III sleep. Case 2 Clinical/EEG description (Tassinari et al., 2000): A 7-year-old boy during slow-wave sleep. EEG showed continuous, diffuse 2.5-Hz spike-and-wave activity, of higher amplitude on the left side. During REM sleep, diffuse spike-and-wave discharges disappeared, whereas focal left frontotemporal spikes without contralateral diffusion reappeared. Case 3 Clinical/EEG description (Coutelier et al., 2008): An 8-year-old girl with subtle seizures with eyelid myoclonia. Sleep-EEG showed nearly continuous and bitemporal spike-and-wave complexes, while in frontocentral areas, only slow waves were recorded. Case 4 Clinical/EEG description (Zhang et al., 2010): A 5-year-old boy had frequent epileptiform discharges while he was awake. During sleep the EEG revealed continuous spike-and-wave discharges.

Figure 12. NCSE in ESES (Van Hirtum-Das et al., 2006). Calibration: 1 s between vertical lines; 100 lV per vertical unit. Epilepsia ILAE Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

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EEG Criteria for NCSE 2d.

NCSE in Landau-Kleffner syndrome

Case 1 Clinical/EEG description (Nickels & Wirrell, 2008): A 6-year-old boy with Landau-Kleffner syndrome had markedly increased frequency of left centrotemporal periodic spike and slow-wave complexes during sleep (Fig. 13).

3 . NCS E Occurrin g in B oth Childhood and Adulthood With epileptic encephalopathy 3a.

NCSE in the Lennox-Gastaut syndrome

(i) Atypical absence status epilepticus Case 1 Clinical/EEG description (Livingston & Brown, 1987): A 7-year-old girl with prolonged and recurrent febrile seizures and drop attacks. EEG showed rhythmic and polymorphic diffuse delta activity of 1.5–2 Hz without response to benzodiazepines (Fig. 14A,B).

Case 2 Clinical/EEG description (Dravet et al., 1986): An 8-yearold girl with constant confusion, isolated or generalized myoclonias, and drop attacks. Absence status with subcontinuous slowwaves, spike-and-waves andpolyspike-and-waves. Case 3 Clinical/EEG description (Ohtsuka et al., 1999): A 1year 10-month-old girl. At 3 years and 3 months of age, she began to have atypical absences and brief head-nodding seizures in addition to complex partial seizures. These atypical absences and brief head-nodding seizures appeared in a cluster and evolved into NCSE, during which she became unresponsive with frequent head nodding. EEG revealed multifocal spike-and-waves, which were mainly bilateral midtemporal. The patient’s head nodded repeatedly in a sitting position. There was a decrease in response to external stimuli. Although the electromyogram was not recorded on this EEG, the patient’s mother activated the marker at the time of the head-nodding seizures. On another occasion, no discharges were detected by the electromyogram at the time of the head-nodding seizures, which were associated with diffuse spike-wave bursts.

Figure 13. NCSE in Landau-Kleffner syndrome (Nickels & Wirrell, 2008). Calibration: 1 s between vertical lines; 30 lV/mm. Epilepsia ILAE Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

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R. Sutter and P. W. Kaplan A

B

Figure 14. (A,B) NCSE as atypical absence status epilepticus (Livingston & Brown, 1987). Calibration: 1 s per horizontal unit; 100 lV pervertical unit. Epilepsia ILAE

Case 4 Clinical/EEG description (Ohtsuka et al., 1999): A 7year 3-month old girl with left-frontal spike-and-waves. The patient had frequent head-nodding seizures in a sitting position with a decrease in response to external stimuli. Electromyogram showed that discharges from bilateral trapezius muscles suddenly disappeared at the time of a brief atonic seizure, which was time-locked by a diffuse spike-and-wave burst. Case 5 Clinical/EEG description (Ohtsuka et al., 1999): A 2year 2-month-old boy with frequent head-nodding seizures in a sitting position with a decrease in response to external stimuli. EEG showed relatively synchronous, diffuse, 1.5–2 Hz slow spike-and-wave bursts (left-side dominant) when the patient showed a decrease in response to external stimuli. Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

Case 6 Clinical/EEG description (Bauer & Trinka, 2010): A 33-year-old woman with late onset Lennox-Gastaut syndrome (onset at age 16 years). EEG 3 days after start of an atypical absence status (obtundation and occasional twitches) showed continuous generalized sharp and slow waves at 2 Hz, dominant over the anterior regions. The pattern also can be read as triphasic waves.

(ii) Tonic status epilepticus Case 1 Clinical/EEG description (Dravet et al., 1986): Tonic status in a girl aged 11 years 7 months. Diffuse, fast rhythms followed by a burst of high-voltage polyspikes intermixed with slow waves (Fig. 15 top). Clinically: short apnea, followed by superficial polypnea and tachycardia.

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Figure 15. Tonic status epilepticus (Dravet et al., 1986). Calibration: 1 s per horizontal unit; 100 lV per vertical unit. Epilepsia ILAE

At the end, intensive muscular activity recorded on the left muscles. Figure 15; bottom: A long seizure (55 s) involving principally the left hemisphere, with only anterior rapid rhythms and slow waves on the right. No clinical expression. Case 2 Clinical/EEG description (Tassinari et al., 1972): A child with state of confusion with frequent myoclonic jerks, either massive, segmental or discrete. The EEG showed nearly continuous diffuse spike-and-waves of high amplitude and variable frequency, most marked anteriorly. This was followed by absence status with confusion and discrete myoclonic jerks. EEG showed diffuse spike and polyspike-and-wave discharges. Spike and waves persisted between seizures with confusion. Before injection: Discharges of subcontinuous generalized spike and waves and polyspikes-and-waves, sometimes accompanied by repeated clonias recorded from the right deltoid. A few seconds after intravenous injection of 10 mg of diazepam tonic seizures appeared with an EEG characterized by rhythmic spikes, accompanied by intense tonic contraction.

Case 3 Clinical/EEG description (Tassinari et al., 1972): A patient with apnea and bradycardia without motor manifestations, and on EEG fast spikes lasting 4–6 s. The whole episode lasted 45 min. Before activation — bursts of angular diffuse theta waves. After generalized tonic–clonic seizures following intravenous injection of 500 mg of pentylenetetrazol the EEG is characterized by diffuse, continuous slow spike-and-waves appearing immediately after the postcritical depression that followed the grand mal seizure. Case 4 Clinical/EEG description (Bittencourt & Richens, 1981): Several week-long episodes of minor status occurred, in which this girl looked vacant, with occasional twitching of the face and hands. She then had tonic seizures with sleep or drowsiness. EEGs showed a slow spike-and-wave abnormality, sometimes with atypical absences and bursts of repetitive spikes. From the data summarized it can be concluded that diazepam injected as a bolus caused tonic status epilepticus with concomitant bursts of repetitive spikes on the EEG. Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

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B

Figure 16. (A,B) NCSE in learning disability or disturbed cerebral development (Dirik et al., 2006). Calibration: 1 s between vertical prominent lines; sensitivity not known. Epilepsia ILAE Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

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EEG Criteria for NCSE EEG record showed atypical spike-and-wave bursts, the period varying between 2 and 3 Hz. Bursts of repetitive spikes at 16–20 Hz and amplitudes of up to 100 lV were more prominent anteriorly and series of bursts of repetitive spikes, intercalated with large amplitude slow waves.

decreased alertness. In Figure 16A EEG during sleep state demonstrates generalized slow-wave discharges and some spikes between slow-wave discharges. Figure 16B shows disappearance of epileptiform activity 24 h after intravenous valproic acid treatment; however, there is still some slowing.

3b. Other forms of NCSE in patients with learning disability or disturbed cerebral development (cryptogenic or symptomatic)

Case 2 Clinical/EEG description (Shin et al., 2011): A 7year-old girl with cerebral palsy and extensive bilateral polymicrogyria. She has generalized 1–2 Hz spike and waves over several hours while she is taking valproate, levetiracetam, and clobazam (Fig. 17A). Figure 17B shows slowing before complete remission.

Case 1 Clinical/EEG description (Dirik et al., 2006): An 18month-old boy with global neurodevelopmental delay and

A

B

Figure 17. (A,B) NCSE in learning disability or disturbed cerebral development (Shin et al., 2011). Calibration in A: 1 s between prominent vertical lines; 30 mV/mm. Calibration in B: 1 s between prominent vertical lines; 7 mV/mm. Epilepsia ILAE Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

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R. Sutter and P. W. Kaplan Without epileptic encephalopathy 3c. Typical absence status epilepticus in idiopathic generalized epilepsy Case 1 Clinical/EEG description (Cascino,1993):A patient with typical absence status epilepticus. EEG showed generalized continuous 3-Hz spike-and-wave activity that is anterior predominantduring typical absence status epilepticus (Fig.18). Case 2 Clinical/EEG description (Akman, 2010): In this patient with typical absence status epilepticus EEG showed irregular diffuse spike-and-wave discharges that are sometimes synchronous with 3 Hz. Case 3 Clinical/EEG description (Genton et al., 2008): Patient appeared confused, slow, drowsy. EEG showed almost continuous generalized spike-and-wave and polyspike-and-wave discharges at 3 Hz. Intravenous injection of diazepam induced a transient effect, with patient regaining full consciousness, and partially recalling the event; concomitantly EEG showed a normal background activity with only rare generalized polyspike-and-wave discharges. After 15 min, SE reappeared with EEG showing pseudo rhythmic bursts of spike-and-wave and polyspike-wave discharges. Case 4 Clinical/EEG description (Genton et al., 2008): An adult patient with absence status characterized by mild impairment of consciousness and by motor impersistence. EEG shows discontinuous short bursts of slow polyspikeand-waves. When asked to close his eyes, the patient rhythmically opened them concomitantly with the spike component of the polyspike-and-wave complexes on the EEG, despite the reiteration of the order.

Case 5 Clinical/EEG description (Korff & Nordli, 2007): A 6-year-old child with unresponsiveness and subtle twitching of the corner of the mouth. EEG showed continuous rhythmic generalized spike-and-wave discharges with frontal predominance. Case 6 Clinical/EEG description (Fernandez-Torre et al., 2011): A 27-year-old woman known for having GTCS with mutism and no other precipitating factors in her personal history. No further description available. EEG showed presence of continuous polyspike-and-wave and spike-and-wave complexes in keeping with the diagnosis of typical absence status epilepticus. 3d.

Complex partial status epilepticus

(i) Limbic status epilepticus Case 1 Clinical/EEG description (Nahab et al., 2008): A 57year-old woman with a 2-month history of refractory simple partial seizures. She had right upper extremity clonic movements that progressed to a GTCS. These developed into frequent episodes of clonic right face, arm, and occasionally leg movements without alteration of awareness. Epilepsia partialis continua of unclear etiology was diagnosed. Seizure onset was seen over the left frontocentral region. Frequent epileptiform discharges over the left frontocentral region correlating with clinical seizure activity (Fig. 19). Case 2 Clinical/EEG description (Kirkpatrick et al., 2011): A 19-year-old woman with behavioral problems, emotional lability with religious verbalizations. She displayed personality changes and bizarre behaviors, responding to

Figure 18. Typical absence status epilepticus in idiopathic generalized epilepsy (Cascino, 1993). Calibration: 1 s per horizontal unit; 100 lV per vertical unit. Epilepsia ILAE


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Figure 19. Limbic status epilepticus (Nahab et al., 2008). Calibration: 1 s between vertical lines; sensitivity not known. Epilepsia ILAE

hallucinations and reacting aggressively. EEG showed generalized rhythmic delta activity. The evolution of the EEG pattern is difficult to appreciate based on one 10-s epoch. Case 3 Clinical/EEG description (Bayreuther et al., 2009): This 25-year-old woman had unusual headache, auditory hallucinations, and extreme anxiety, consistent with panic attacks. She had fluctuating consciousness with temporal and spatial disorientation and recurrent chewing movements. Over a 4-week period she developed complex abnormal movements, with stereotypic episodes of brief repetitive dystonic posturing of the left hemiface and left upper limb, severe orofacial dyskinesias leading to injury of the lips, bruxism, hypersalivation, oromandibular dystonia with tongue protrusion, and episodes of opisthotonus. During the first EEG, the patient was confused with oroalimentary automatisms. EEG showed right hemispheric 1-Hz rhythmic activity. After intravenous diazepam, the patient became responsive and EEG improved markedly with reappearance of the alpha rhythm.

Case 4 Clinical/EEG description (Espay et al., 2006): A 68-year-old woman with anti-Hu antibodies, rapidly evolving impairment in consciousness, and EEG evidence of lateralized pseudoperiodic sharp-wave discharges. Ataxia and sensory neuropathy developed within the first two weeks. EEG on admission showed predominantly right pseudoperiodic sharp waves, spike-and-wave complexes, and subsequent pseudoperiodic complexes. Background was poorly organized with intermixed, almost continuous, irregular and generalized sharp waves. Case 5 Clinical/EEG description (Kaplan et al., 2012): A 51-year-old woman had a 10-month history of rapid progressive dementia, partial seizures, sudden dystonic movements, and hyponatremia. EEG showed waxing and waning generalized 2–4 Hz rhythmic delta activity. After 5 mg of midazolam the patient began interacting. Case 6 Clinical/EEG description (Kaplan et al., 2012): A 21year-old woman began having brief delusional thoughts Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

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Figure 20. Nonlimbic complex partial status epilepticus (Akman, 2010). Calibration: 1 s between prominent vertical lines; sensitivity not known. Epilepsia ILAE with hallucinations, altering ‘‘between dreams and to make herself a cocktail, and perseverative behaviors reality,’’ that became persistent. Clinical examination such as repeating ‘‘channel 168’’ while manipulating the revealed unresponsiveness to voice, touch, or command, television remote. She had deficits in recall, attention, and and a right gaze preference with increased tone of the four judgment. EEG revealed irregular frontal delta activity limbs without spontaneous movements. EEG showed bilaterally. anterior rhythmic 2.5–3 Hz delta waves. Background was suppressed, runs lasted >4 s, and there was no change with Case 3 Clinical/EEG description (Sensoy et al., 2009): An 11noxious stimuli, indicating that this was not frontal intermonth-old female infant was unconscious and responsive mittent rhythmic delta activity (FIRDA). to only painful stimuli at admission. Left central facial paralysis wasdetected andshe hadno swallow reflex or gag (ii) Nonlimbic complex partial status epilepticus reflex. Brain magnetic resonance imaging (MRI) showed lesions in both frontotemporal lobes. EEG showed persisCase 1 Clinical/EEG description (Akman, 2010): A 2-year- tent epileptic activity at the secondhospitalization. old child with left-sided pachygyria presented with intermittent brief habitual seizures. EEG shows continuous Case 4 Clinical/EEG description (Cascino, 1993): A patient focal seizure lateralized to the left hemisphere (Fig. 20). with complex partial status epilepticus with a simple partial onset. Simple partial onset with focal epileptiform disCase 2 Clinical/EEG description (Stayman & Abou-Khalil, charge was seen in the right superior frontal region (F4 2011): A 51-year-old woman with evolution of bizarre electrode). With seizure progression there was a loss of behavior such as placing her cell phone in the microwave, consciousness and the development of generalized backplacing a glass tumbler into the blender while attempting ground slowing. Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

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EEG Criteria for NCSE A

B

Figure 21. (A,B) NCSE in the postictal phase of TCSE (Langheinrich et al., 2005). Calibration: 1 s per horizontal unit; 100 lV per vertical unit. Epilepsia ILAE Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

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R. Sutter and P. W. Kaplan Case 5 Clinical/EEG description (Kikumoto et al., 2009): Patient at the time of diagnosis of complex partial statusepilepticus. Ictal EEG showed 1.5–3 Hz irregular slow spike and waves and polyspike and waves mixed with 14–16 Hz fastactivity, observedpredominantly in the lefthemisphere. 3e. NCSE in the postictal phase of tonic–clonic status epilepticus (TCSE) Case 1 Clinical/EEG description (Langheinrich et al., 2005): A 39-year-old woman in a stuporous state over 6 days after tonic–clonic status epilepticus. On day 6 the woman was found to be drowsy, feverish (temperature 39.0C), not eating or drinking, slow to obey simple commands, and having attacks every few minutes; she had slight stiffening of the whole body with rolling up of the eyes lasting <10 s. The EEG (Fig. 21A) showed widespread bursts of spike and slow-wave activity with a frontal preponderance. Case 2 Clinical/EEG description (Shorvon & Trinka, 2010): A 24-year-old woman after a GTCS with prolonged mild fluctuating impairment of consciousness. EEG showed polyspike-and-waves, periodic generalized polyspikesand-waves. There was preserved alpha rhythm seen between the generalized polyspikes-and-waves.

Case 4 Clinical/EEG description (Korff & Nordli, 2007):A 10year-old girl in convulsive status epilepticus. EEG obtained after convulsions resolved but while still unresponsive showedperiodic discharges of nonconvulsivestatus epilepticus following convulsive status epilepticus. There were right hemisphere periodicsharp waves witha slow repetition rate. Case 5 Clinical/EEG description (Korff & Nordli, 2007): A 12-year-old girl with prolonged unresponsiveness after convulsive status. EEG showed bilateral periodic lateralized epileptiform discharges (rhythmic 1 Hz spike-andwave discharges). 3f. Subtle status epilepticus (myoclonic status after convulsive status epilepticus) Case 1 Clinical/EEG description (Arzimanoglou & Resnick, 2011): A 39-year-oldwoman with viral encephalitis and secondarygeneralized convulsive statusepilepticus, then comatose with mild bilateral facial twitching. EEG showed subtle status epilepticus with generalized periodic discharges interrupted by short generalizedflat periods (Fig. 22). 3g.

Aura continua

(i) Sensory symptoms Case 3 Clinical/EEG description (Shorvon & Trinka, 2010): A 50-year-old man after a GTCS with prolonged postictal coma. EEG revealed periodic lateralized epileptiform activity over the left frontocentral leads.

Case 1 Clinical/EEG description (Manford & Shorvon, 1992): 23-year-old man with ‘‘butterfly sensations,’’ often felt in the abdomen but not specifically localized, sometimes persisting after the seizure. During prolonged

Figure 22. Subtle status epilepticus (Arzimanoglou & Resnick, 2011). Calibration: 1 s per horizontal unit; 100 lV per vertical unit. Epilepsia ILAE


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Figure 23. Aura continua with sensory symptoms (‘‘butterfly sensations’’) (Manford & Shorvon, 1992). Calibration: 1 s per horizontal unit; 100 lV per vertical unit. Epilepsia ILAE

A

Figure 24. (A,B) Aura continua with special sensory symptoms (anxiety) (Brigo et al., 2011). Calibration: 1 s between vertical lines; sensitivity 100 lV/mm. Epilepsia ILAE

B


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R. Sutter and P. W. Kaplan epigastric sensation, there was rhythmical slow activity, predominantlyin theright frontocentral leads (Fig. 23). (ii) Special sensory symptoms Case 1 Clinical/EEG description (Brigo et al., 2011): A 60year-old with prolonged fear and anxiety. EEG showed continuous, rhythmic 2.5-Hz spike-and-wave activity lateralized to the right, with maximal amplitude in the parietotemporal region (Fig. 24A).

(iii) Autonomic symptoms Case 1 Clinical/EEG description (Panayiotopoulos, 2004): A child with Panayiotopoulos syndrome. EEG (Fig. 25A)

showed high-amplitude spike-and-waves recorded from the bifrontal regions before onset of the electrical discharge, which was also purely bifrontal. Marked tachycardia appeared 13 min from the onset of the electrical discharge, when this had become diffuse. There was tachycardia and ictus emeticus. Case 2 Clinical/EEG description (Koutroumanidis et al., 2005): A 5-year-old child with emetic symptoms and other autonomic phenomena. EEG showed bifrontal spikes that increased during sleep, with additional independent interictal left centrotemporal spikes. The seizure started from stage II sleep with fast activity over the bifrontal areas. After 12 min from onset he had change in heart rate from 65–120 beats/min. Level of cognition fluctuated between reduced awareness and complete unresponsiveness.

A

B


Figure 25. (A,B) Aura continua with autonomic symptoms (visceral, tachycardia) (Panayiotopoulos, 2004). Calibration in A: 2 s per horizontal unit; 200 lV per vertical unit. Calibration in B: 1 s per horizontal unit; 100 lV per vertical unit. Epilepsia ILAE

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Figure 26. Aura continua with cognitive symptoms (isolated alexia) (Kutluay et al., 2007). Calibration: 1 s per horizontal unit; sensitivity not known. Epilepsia ILAE

Figure 27. Aura continua with cognitive symptoms (altered memory task, alexia, and acalculia in ictal neuropsychological assessment) (Profitlich et al., 2008). Calibration: 1 s per horizontal unit; 100 lV per vertical unit. Epilepsia ILAE


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R. Sutter and P. W. Kaplan (iv) Cognitive symptoms Case 1 Clinical/EEG description (Kutluay et al., 2007): A 57year-old man with fluctuations in mental status and an inability to read. During the seizures he was unable to answer questions and had nystagmoid movements of the eyes to the right. Brain MRI revealed fluid-attenuated inversion recovery (FLAIR) hyperintensities over the left

occipitotemporal region. EEG showed ictal activity over the left temporooccipital region with a maximal field at the O1, T3, and T5 electrode sites and intermittent focal slowing over the left posterior head region. Four electrographic seizures came from the left temporooccipital region lasting 150–220 s. Ictal pattern started with periodic sharp waves from the left temporooccipital region, followed by rhythmic 8–9 Hz discharges.

Figure 28. Aura continua with cognitive symptoms (altered vigilance, comprehension, writing, ideomotor praxis, motor and memory tasks, as well as altered visuoconstructive tasks and old memory in ictal neuropsychological assessment) (Profitlich et al., 2008). Calibration: 1 s per horizontal unit; 150 lV per vertical unit. Epilepsia ILAE

Figure 29. Aura continua with cognitive symptoms (altered mood and affect in ictal neuropsychological assessment) (Profitlich et al., 2008). Calibration: 1 s per horizontal unit; 70 lV per vertical unit. Epilepsia ILAE


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EEG Criteria for NCSE Case 2 Clinical/EEG description (Profitlich et al., 2008): A 42-year-old man with altered memory. Speech revealed the use of neologisms and perseverations. Counting, naming, and fluency were reduced. He had alexia, acalculia, and apraxia. EEG revealed bilateral generalized spike and spike-and-wave activity with frontal emphasis (Fig. 27). Case 3 Clinical/EEG description (Profitlich et al., 2008): A 31-year-old woman with reduced psychomotor speeds, learning, and memory. Ictal neuropsychological test showed altered vigilance, comprehension, writing, ideomotor praxis, motor and memory tasks, as well as altered visuoconstructive tasks and old memory. EEG showed cryptogenic generalized bifrontal spike activity with right emphasis (Fig. 28). Case 4 Clinical/EEG description (Profitlich et al., 2008): A 49-year-old man with altered mood and affect. EEG

revealed cryptogenic generalized high-amplitude rhythmic 10–12 Hz alpha activity (Fig. 29). Case 5 Clinical/EEG description (DeToledo et al., 2000): A 69-year-old woman with episodes of inability to talk, without any other motor or cognitive impairment. Episodes lasted as long as 24 h. During aphasia EEG showed 3.5-Hz paroxysmal discharges (continuous spikes), maximal over the right frontal and central regions (Fig. 30).

4. 4a.

NC SE i n L at e A du lt ho od

De novo absence status epilepticus of late onset

Case 1 Clinical/EEG description (Szucs et al., 2008): A 55year-old woman with strange states lasting for hours or days when she could not care for herself, was disoriented, could not perform everyday activities, and sometimes became paranoid and aggressive. At admission, she was extremely slow, smiling, vague, and confused. EEG

Figure 30. Aura continua with cognitive symptoms (isolated aphasia respectively speech arrest) (DeToledo et al., 2000). Calibration: Sensitivity not known. Epilepsia ILAE Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

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R. Sutter and P. W. Kaplan revealed continuous, generalized, 3–4 Hz spike-and-wave pattern during her slow, disoriented state (Fig. 31). Case 2 Clinical/EEG description (Genton et al., 2008): EEG of a 53-year-old confused, slow, and drowsy man showed almost continuous generalized spike-and-wave and polyspike-and-wave discharges at 3 Hz. Intravenous injection of diazepam induced a transient effect, with patient regaining full consciousness and partially recalling the event. After 15 min, status epilepticus reappeared with EEG showing pseudorhythmic bursts of spike-wave and polyspike-and-wave discharges. Case 3 Clinical/EEG description (Szucs et al., 2008): A 56-year-old housewife with sparse, generalized tonic– clonic convulsions as well as frequent ‘‘small seizures’’ with absence-like features. Her movements and speech were unusually slow; she had small, episodic jerks of the jaw; and she seemed to be absent, disoriented, and strange. EEG showed continuous

2.5–3.5 Hz spike-and-wave pattern, which disappeared after intravenous injection of diazepam. Her psychomotor activity improved and she became oriented and responsive. Case 4 Clinical/EEG description (Szucs et al., 2008): A 63year-old woman with tonic–clonic seizures followed by stupor, with no verbal or metacommunicative contact; she stared in a rigid, vague way. She sat or lay and remained in forced positions in a catatonic manner. EEG showed continuous, generalized, 2.5–4 Hz spike-, polyspike-andwave pattern during patient’s stuporous state. Case 5 Clinical/EEG description (Pro et al., 2011): A 72-yearold woman withacute onset of altered consciousness for 5 h. The episodes were characterized by acute onset of mental confusion and ideomotor slowing, apraxia, and speech arrest, without motor abnormalities or incontinence. EEG showed generalized spike and polyspike-and-wave dischargesat 3–3.5 Hz of higher voltage in the anteriorregions.

Figure 31. De novo absence status epilepticus of late onset (Szucs et al., 2008). Calibration: 1 s between prominent vertical lines; sensitivity not known. Epilepsia ILAE Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

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EEG Criteria for NCSE Case 6 Clinical/EEG description (Fernandez-Torre et al., 2011): A 74-year-old woman with slowness in mental activity. She was confused and disoriented to person, time, and place. There were no automatisms or myoclonic jerks. EEG showed nearly continuous generalized spike-and-wave and polyspike-and-wave discharges. At that time, the woman was perplexed and confused. Case 7 Clinical/EEG description (Fernandez-Torre et al., 2011): A 79-year-old woman with abnormal behavior who was confused and disoriented. When she was coma-

tose, EEG revealed continuous ongoing seizure activity constituted by synchronous high-voltage epileptiform discharges with brief periods of flattening. Focal sharp waves localized in the left centroparietal area and vertex after the injection of 10 mg of diazepam. 4b. Other forms of NCSE in late adulthood Case 1 Clinical/EEG description (Thomas et al., 1995): A 47year-old man with rhythmic bilateral clonic twitching of the lower part of the face, lasting up to 5 h. Opening of the mouth when seizure developed provoked a brief arrest of the myoclonus, whereas closing the mouth did not modify

A

B

Figure 32. (A,B) NCSE in late adulthood with opercular origin (Thomas et al., 1995). Calibration in A : 3 s per horizontal unit; 100 lV per vertical unit. Calibration in B: 1 s per horizontal unit; 75 lV per vertical unit. Epilepsia ILAE Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

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R. Sutter and P. W. Kaplan the seizures (Fig. 32B; MO = mouth open, MC = mouth closed). EEG revealed opercular myoclonic–anarthric status epilepticus. Myoclonias were recorded as muscular potentials over the right temporal area (associated left facial palsy) and produced 5–10 mm amplitude quivering of the inferior jaw with no evidence of associated cortical epileptiform EEG activity. During recording, eyes and mouth were opened.

pharyngeal area. Top trace showed occurrence of rhythmic, 2-Hz clonic seizure with a transient postictal silent period. Myoclonus was preceded on surface EEG by a biphasic component localized over the left inferofrontal (F3-F7) and left centrotemporal (C3-T3) areas (arrowheads). Back-averaging of 50 consecutive traces showed that the biphasic component preceded myoclonia onset a )160 msec delay.

Case 2 Clinical/EEG description (Thomas et al., 1995): A 33-year-old right-handed man with sudden expressive aphasia lasting 5 h. Ten months later, he had permanent rhythmic lingual movements. EEG showed continuous slow periodic myoclonias occurring with 3.5–4 s frequency involving the tongue and the hypo-

Case 3 Clinical/EEG description (Thomas et al., 1995): A 62-year-old man developed severe permanent dysarthria with buccofacial apraxia associated with a bilateral lower central facial palsy. There was no impairment of comprehension or vigilance. Brain MRI showed a right opercular tumor. EEG revealed opercular myoclonic–anarthric

A

B


Figure 33. (A,B) NCSE in late adulthood with sporadic Jakob-Creutzfeldt disease (Espinosa et al., 2010). Calibration: 1 s per horizontal unit; 140 lV per vertical unit. Epilepsia ILAE

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EEG Criteria for NCSE status epilepticus due to opercular oligodendroglioma with recurrent left hemifacial somatomotor seizures. Status epilepticus was characterized by bilateral middleamplitude slow myoclonias involving lips, chin, and soft palate with no evidence of associated cortical epileptiform EEG abnormality. Case 4 Clinical/EEG description (Espinosa et al., 2010): A 64-year-old woman with sporadic Jakob-Creutzfeldt disease. Autopsy revealed spongiform changes in cortical and subcortical sections. Interictal EEG showed poorly organized background, generalized slowing, and periodic epileptiform discharges at a frequency of 1–1.5 Hz greater over the right temporal region (Fig. 33A). The ictal EEG revealed bilateral synchronous high-amplitude, periodic sharp wave discharges that evolve in morphology and frequency (Fig. 33B), followed by intermittent brief diffuse suppression without changes in behavior. Case 5 Clinical/EEG description (Bauer & Trinka, 2010): A 65-year-old woman with Jakob-Creutzfeldt disease. After intravenous injection of 4 mg clonazepam, no change of continuously repeated and rhythmic 1–2 Hz ‘‘triphasic’’ waves, no spikes.

5. 5a.

Boundary Syndromes

Coma with epileptiform EEG changes

(i) Cryptogenic encephalitis Case 1 Clinical/EEG description (Fernandez-Torre et al., 2011): A 39-year-old woman in deep coma after cryptogenic encephalitis showed continuous epileptiform discharges consisting of rhythmic sharp waves and sharp-and-slow-wave complexes at 2.5–3 Hz (Fig. 34).

(ii) Hypoxic encephalopathy Case 1 Clinical/EEG description (Holtkamp & Meierkord, 2011): A 56-year-old comatose man after global cerebral hypoxia following ventricular fibrillation had dominating GPEDs at 2 Hz showing maximum amplitudes in bifrontal regions (Fig. 35A). Between the bursts the EEG activity was extremely flat. Five minutes after intravenous administration of 2 mg lorazepam, GPEDs disappeared and there was widespread low-amplitude activity at the end of the trace (Fig. 35B). The changes after administration of benzodiazepines were not associated with any clinical improvement.

Figure 34. Coma with epileptiform EEG changes in cryptogenic encephalitis (Fernandez-Torre et al., 2011). Calibration: 1 s per horizontal unit; 100 lV per vertical unit. Epilepsia ILAE Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

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R. Sutter and P. W. Kaplan Case 2 Clinical/EEG description (Lowenstein & Aminoff, 1992): A 72-year-old man after cardiac arrest with repetitive motor activity of the mouth and extremities. EEG showed continuous spike-and-wave activity. Case 3 Clinical/EEG description (Lowenstein & Aminoff, 1992): A 31-year-old man after cardiac arrest with frequent, stereotyped episodes in which there were clonic movements on the left side of the face and right lower extremity. EEG revealed mixed frequency background activity with episodic accentuation and occasional sharp transients. Case 4 Clinical/EEG description (Lowenstein & Aminoff, 1992): A 79-year-old man with idioventricular cardiac

rhythm and hypotension was unresponsive with absent pupillary light responses, oculocephalic reflex, corneal reflex, and deep tendon reflexes. No clinical seizures were observed. Twenty-four hours after admission he showed episodes of repetitive sharp waves, slightly more marked on the left. Case 6 Clinical/EEG description (Bauer & Trinka, 2010): A 76-year-old comatose woman after status asthmaticus had continuous and very regular generalized 2–3 Hz spikeand-wave activities 8 h after onset of status asthmaticus. Case 7 Clinical/EEG description (Bauer & Trinka, 2010): A 63-year-old man with coma after cardiac arrest showed periodic multiple spikes on a nearly flat background activity on day 2.

A

B


Figure 35. (A,B) Coma with epileptiform EEG changes in hypoxic encephalopathy (Holtkamp & Meierkord, 2011). Calibration: 1 s per horizontal unit; 100 lV per vertical unit. Epilepsia ILAE

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EEG Criteria for NCSE Case 8 Clinical/EEG description (Bauer & Trinka, 2010): A 49-year-old woman in a coma was on respirator due to intoxication with sedative drugs. She had no brainstem reflexes and EEG showed a burst-suppression pattern. Case 9 Clinical/EEG description (Bauer & Trinka, 2010): A 58-year-old man with coma after cardiac arrest showed a burst-suppression pattern containing spikes with short interval on day 3 after the initial event. Case 10 Clinical/EEG description (Bauer & Trinka, 2010): A 53-year-old man in a coma after traumatic brain injury. EEG showed BIPLEDs with a unilateral burst-suppression pattern over the right hemisphere.

5b.

Epileptic behavioral disturbance or psychosis

Case 1 Clinical/EEG description (Chiara et al., 2011): A 76-year-old woman with dementia looked distracted and vacant, and replied to questions after a brief pause and with inadequate answers. She had trouble speaking, and

was uncooperative, disoriented, had a fixed gaze, and was unresponsive to any stimuli. She had oroalimentary automatisms and jerking of the right foot. EEG showed theta–delta activity with sporadic low-voltage spikes prevalent in the bilateral frontotemporal regions (Fig. 36). Case 2 Clinical/EEG description (Valko et al., 2009): A 63year-old right-handed woman who was confused, agitated, dysarthric, and incoherent in her thoughts had widespread right hemispheric attenuation and periodic frontally accentuated focal epileptic discharges consistent with the diagnosis of a NCSE. Periodic 1.5-Hz epileptic discharges were seen with right frontal predominance (Fig. 37A). Case 3 Clinical/EEG description (Sethi et al., 2010): A 93year-old woman with acute right temporooccipital stroke. Video-EEG recording revealed frequent brief right hemispheric focal seizures, every 5–10 min. There was 9– 10 Hz rhythmic activity in the right posterior temporal leads evolving to spread across the entire right hemisphere with intermixed sharp waves and spike-and-wave discharges (Fig. 38A–D).

Figure 36. Epileptic behavioral disturbance in association with dementia (Chiara et al., 2011). Calibration: 1 s between vertical lines; sensitivity not known. Epilepsia ILAE Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

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A

B

Figure 37. (A,B) Epileptic behavioral disturbance in association with cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy (CADASIL) (Valko et al., 2009). Calibration: 1 s per horizontal unit; 50 lV per vertical unit. Epilepsia ILAE


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A

B

Figure 38. (A – D) Epileptic behavioral disturbance with frequent throat clearing (Sethi et al., 2010). Calibration: 1 s per horizontal unit; 50 lV per vertical unit. Epilepsia ILAE


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R. Sutter and P. W. Kaplan C

D

Figure 38b. Continued. Epilepsia ILAE


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EEG Criteria for NCSE 5c. Drug-induced or metabolic confusional state with epileptiform EEG changes

(i) Drug-induced confusion state with epileptiform EEG changes Case 1 Clinical/EEG description (Anzellotti et al., 2011): A 64-year-old woman on cefixime followed by confusion

had continuous generalized spike or double-spike and slow-wave discharges, which were occurring at a frequency of 3–3.5 Hz and amplitudes of 100–120 lV (Fig. 39A), with sporadic inscription of polyspikes at a frequency of 14–15 Hz and amplitudes of 90–100 lV. Case 2 Clinical/EEG description (Thabet et al., 2009): A 15year-old girl on hemodialysis and cefepime who had

A

B

Figure 39. (A,B) Drug-induced confusional state with epileptiform EEG changes by cefixime (Anzellotti et al., 2011). Calibration: 1 s between vertical lines; sensitivity 7 lV/mm. Epilepsia ILAE Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

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R. Sutter and P. W. Kaplan myoclonic arm jerks and become unresponsive. EEG revealed generalized spike and sharp wave activity compatible with NCSE (Fig. 40A). Repeated EEG after cefepime withdrawal was normal (Fig. 40B).

tive than usual. Subcontinuous EEG abnormalities during NCSE with high-amplitude 3–4 Hz sharp waves with irregular runs of atypical spike-and-wave complexes over the anterior regions of both hemispheres.

Case 3 Clinical/EEG description (Piccinelli et al., 2000): A 12-year-old boy on tiagabine became less active and reac-

Case 4 Clinical/EEG description (Knake et al., 1999): A 32year-old woman on tiagabine with mental clouding of

A

B

Figure 40. (A,B) Drug-induced confusional state with epileptiform EEG changes by cefepime (Thabet et al., 2009). Calibration: 1 s between prominent vertical lines; sensitivity 15 lV/mm. Epilepsia ILAE Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

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B

Figure 41. (A,B) Drug-induced confusional state with epileptiform EEG changes by tiagabine (Piccinelli et al., 2000). Calibration: 1 s per horizontal unit; 100 lV per vertical unit. Epilepsia ILAE >4 hours. She had never experienced absences lasting for more than a minute before treatment with tiagabine. During status epilepticus for >6 h EEG showed intermittent generalized slowing and spike-and-wave complexes. Case 5 Clinical/EEG description (Imperiale et al., 2003): A 30-year-old woman who developed NCSE during tiagabine adjunctive therapy. EEG during tiagabine-associated NCSE episode showed diffuse slowing of background

rhythm and frequent spike-and-wave discharges on right temporal derivations spreading to contralateral regions. After intravenous injection of 4-mg lorazepam, EEG revealed clear improvement of background activity with appearance of left temporal spike-wave discharges associated with rare contralateral sharp waves. Case 6 Clinical/EEG description (Mangano et al., 2003): A 4-year-old patient who developed NCSE following Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

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B

Figure 42. (A,B) Drug-induced confusional state with epileptiform EEG changes by topiramate (Brandt et al., 2010). Calibration: 1 s per horizontal unit; 10 lV per vertical unit. Epilepsia ILAE


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B

Figure 43. (A,B) Metabolic confusional state with epileptiform EEG changes in citrullinemia and ammonemia in adult-onset type II citrullinemia (CTLN2) (Funabe et al., 2009). Calibration: 1 s per horizontal unit; 50 lV per vertical unit. Epilepsia ILAE

tiagabine as add-on treatment for refractory partial seizures. Ictal EEG, while patient was confused and unresponsive, showed generalized subcontinuous spike-andsharp-wave discharges during tiagabine. Case 7 Clinical/EEG description (Brandt et al., 2010): A 21year-old man with idiopathic generalized epilepsy who ingested about 8,000 mg of topiramate concentration of 144.6 lg/ml. EEG showed a nearly continuously generalized seizure pattern with changing maximum, most frequently left frontal respectively left frontotemporal with wide potential field (Fig. 42A,B after intravenous injection of lorazepam).

(ii) Metabolic confusional state with epileptiform EEG changes Case 1 Clinical/EEG description (Funabe et al., 2009): A 47-year-old woman with repeated unconsciousness and abnormal behavior. The high plasma ammonia level was not always associated with neurobehavioral symptoms (unconsciousness, disorientation, abnormal behavior, and epilepsy), but paroxysmal EEG discharges were invariably associated with these symptoms. Intravenous injection of diazepam improved neurobehavioral symptoms and EEG discharges (Fig. 43A: before treatment; Fig. 43B: after treatment of citrullinemia). Epilepsia, 53(Suppl. 3):1–51, 2012 doi: 10.1111/j.1528-1167.2012.03593.x

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Disclosure None of the authors has any conflicts of interest to disclose regarding this research activity. Raoul Sutter is supported by the Research Funds of the University of Basel, the Scientific Society of Basel, and the Gottfried Julia Bangerter-Rhyner Foundation. We confirm that we have read the Journal’s position on issues involved in ethical publication and affirm that this report is consistent with those guidelines.

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Critérios de NCSE Kaplan 2012

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