Seizure (2006) 15, 462—467

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CASE REPORT

Ictal spitting in left temporal lobe epilepsy:Report of three cases

Luıs Otavio Sales Ferreira Caboclo a,*, Flavia Saori Miyashira a,Ana Paula Andrade Hamad a, Katia Lin a, Henrique Carrete Jr.b,Americo Ceiki Sakamoto a,c, Elza Marcia Targas Yacubian a

aUnidade de Pesquisa e Tratamento das Epilepsias (UNIPETE), Department of Neurology andNeurosurgery, Division of Neurology, Federal University of Sao Paulo (UNIFESP),R. Napoleao de Barros, 737/138 andar, Sao Paulo 04024-002, SP, BrazilbDepartment of Radiology, Division of Neuroradiology,Federal University of Sao Paulo (UNIFESP), BrazilcDepartment of Neurology, Psychiatry and Clinical Psychology, Division of Neurology,Ribeirao Preto School of Medicine, University of Sao Paulo, Brazil

Received 4 January 2006; received in revised form 10 April 2006; accepted 23 May 2006

KEYWORDSIctal spitting;Automatisms;Temporal lobe epilepsy

Summary

Purpose: Ictal spitting is rarely reported in patients with epilepsy. More often it isobserved in patients with temporal lobe epilepsy (TLE) and is presumed to be alateralizing sign to language nondominant hemisphere. We report three patientswith left TLE who had ictal spitting registered during prolonged video-EEGmonitoring.Methods: Medical charts of all patients with medically refractory partial epilepsysubmitted to prolonged video-EEG monitoring in the Epilepsy Unit at UNIFESPduring a 3-year period were reviewed, in search of reports of ictal spitting. Theclinical, neurophysiological and neuroimaging data of the identified patients werereviewed.Results: Among 136 patients evaluated with prolonged video-EEGmonitoring, three(2.2%) presented spitting automatisms during complex partial seizures. All of themwere right-handed, and had clear signs of left hippocampal sclerosis on MRI. In twopatients, in all seizures in which ictal spitting was observed, EEG seizure onset wasseen in the left temporal lobe. In the third patient, ictal onset with scalp electrodeswas observed in the right temporal lobe, but semi-invasive monitoring with foramenovale electrodes revealed ictal onset in the left temporal lobe, confirming falselateralization in surface records. The three patients became seizure-free followingleft anterior temporal lobectomy.

* Corresponding author at: Av. Cons. Rodrigues Alves, 127/24A, Sao Paulo 04014-010, SP, Brazil. Tel.: +55 11 5579 7357.E-mail address: locaboclo@ig.com.br (L. Otavio Sales Ferreira Caboclo).

1059-1311/$ — see front matter # 2006 British Epilepsy Association. Published by Elsevier Ltd. All rights reserved.doi:10.1016/j.seizure.2006.05.009

Ictal spitting in left temporal lobe epilepsy: Report of three cases 463

Conclusions: Ictal spitting is a rare finding in patients with epilepsy, and may beconsidered a localizing sign of seizure onset in the temporal lobe. It may be observedin seizures originating from the left temporal lobe, and thus should not be con-sidered a lateralizing sign of nondominant TLE.# 2006 British Epilepsy Association. Published by Elsevier Ltd. All rights reserved.

Figure 1 MRI. Coronal IR image showing marked volu-metric reduction and hypointense signal of the left hip-pocampus.

Introduction

Spitting automatisms are rarely reported in patientswith epilepsy.1—8 This stereotyped automatism isoften described as a localizing and lateralizing sign,suggesting seizure onset in the language nondomi-nant temporal lobe.5,8,9 There have been reports ofictal spitting in seizures originating from the lefttemporal lobe,1,2,8,10 though documentation ofthese seizures is seldom available.

We report three cases of patients who presentedictal spitting during prolonged video-EEG monitor-ing for the purpose of pre-surgical evaluation ofmedically refractory temporal lobe epilepsy (TLE).All of them had left TLE due to hippocampal sclero-sis, and became seizure-free after left anteriortemporal lobectomy (ATL).

Materials and methods

We reviewed charts from all patients with medicallyrefractory partial epilepsy submitted to pre-surgicalevaluation, including prolonged video-EEG monitor-ing, during a 3-year period (April 2002 to March2005). Patients were referred to the video-EEG unitfrom the outpatient clinic in our hospital, which is atertiary care center for patients with epilepsy in SaoPaulo. The clinic privileges selection of patientswith refractory epilepsy, particularly of patientswith TLE who are likely suitable for surgical treat-ment.

All patients had MRI exams, following a standardprotocol for study of temporal lobes.

Video-EEG monitoring was performed using 32-channel digital equipment. Electrodes were placedaccording to 10—20 International System, plus addi-tional intermediary temporal electrodes and bilat-eral sphenoidal electrodes in all patients. Duringprolonged video-EEG monitoring, antiepilepticdrug withdrawal was conducted according to thedecision of treating physicians. All seizures wereanalyzed by the medical staff. Reports includeddetailed clinical and electroencephalographiccharacteristics, such as time, duration and typeof each seizure.

Diagnosis of the epileptic syndrome was definedfollowing previously reported criteria.11

We searched for patients who presented spittingautomatisms during video-EEG monitoring.

Results

One hundred and thirty-six patients with refractorypartial epilepsy were submitted to prolonged video-EEG monitoring during the period of the study. Onehundred and twenty patients had diagnosis of TLE.Among these, 108 had unilateral HS diagnosed byMRI.

Three patients (2.2% of the total of patients) hadspitting automatism registered during video-EEGmonitoring.

The clinical, neuroradiological and neurophysio-logical features in each case are described below.

Case 1

A 19-year-old right-handed male patient had, at theage of 2 months, four febrile seizures during anepisode of pulmonary infection. Hewas treated withphenobarbital until the age of 7 years, when thedrug was withdrawn. Two years later he had onset ofhabitual seizures, characterized by a feeling of fearand ill-defined cephalic sensation, followed bybehavioral arrest, oral automatisms and dystonicposturing of the right hand. He frequently presentedspitting automatisms during complex partial sei-zures (CPS). Despite adequate medical treatment,he persisted having three to four CPS permonth, andwas referred to pre-surgical evaluation.

464 L.O.S.F. Caboclo et al.

MRI showed clear signs of left HS (Fig. 1). Pro-longed video-EEGmonitoring revealed bursts of slowactivity over the left temporal lobe; no interictalepileptiform discharges were observed. The patientpresented six CPS during monitoring. In all he pre-sented clear spitting automatism during the com-plex partial phase of these seizures, associated toexcessive salivation. Dystonic posturing of the rightarm preceded spitting automatisms in all seizures.Ictal onset was localized in the left temporal lobe inthe six seizures. In all six seizures ictal activity wasrestricted to the left temporal lobe, without signs ofinvolvement of the contralateral temporal region.

The patient was submitted to surgical treatment— left anterior temporal lobectomy (ALT) — and iscurrently seizure-free, 7 months after this proce-dure.

Case 2

A 26-year-old right handed woman had a past historyof one isolated generalized seizure at the age of 1year, without fever. After 15 years without any, atthe age of 16 she had onset of her habitual seizures.The patient described an ascending epigastric sen-sation, followed by behavioral arrest, staring, oralautomatisms and frequent spitting automatisms.The seizures persisted in spite of use of varioustherapeutic regimens, which included first-linedrugs for treatment of partial seizures.

There were other cases of epilepsy in the family,including the patient’s mother, who reported sei-zures, suggestive of TLE.

After demonstration of drug resistance, thepatient went through pre-surgical evaluation. TheMRI revealed left HS. Prolonged video-EEG monitor-ing showed bursts of slow activity and rare sharpwaves over the left temporal lobe, maximum at

Figure 2 Scalp-sphenoidal record. The arrow poin

the left sphenoidal electrode. Three CPS wererecorded, all with EEG ictal onset in the left tem-poral lobe. In one of the seizures, in which ictalactivity was restricted to the left temporal lobe, thepatient presented ictal spitting in the beginning ofthe seizure, shortly after the behavioral arrest. Ictalimmobility of the right arm, followed by dystonicposturing of this limb was observed in this seizure.

The patient was submitted to left ALT, and after 6months of follow-up she is seizure-free.

Case 3

A 29-year-old right-handed man had several gener-alized non-febrile seizures between the ages of 2and 13 years. Some of the them had lateralizedfeatures, although precise definition of which sidewas affected was not possible. At the age of 13 hestarted to have seizures with aura characterized bya rising epigastric sensation, followed by loss ofconsciousness, staring, oral and hand automatismsand, in some of the seizures, ictal spitting.

MRI scan revealed increased signal and markedatrophy of the left hippocampus. Interictal EEGanalysis showed sharp waves over both temporallobes. Twelve seizures were registered during pro-longed video-EEG monitoring with scalp-sphenoidalelectrodes. Dystonic posturing of the left arm couldbe observed in four. Comprehensible ictal speechwas present in three and ictal spitting was observedin one seizure. In this seizure, spitting automatismwas observed immediately after behavioral arrest,in the first seconds of the seizure, when ictal activitywas observed diffusely over both hemispheres (non-lateralized onset). Later on the patient presentedclonic movements of arms and legs, bilaterally. In 11seizures, ictal onset was clearly localized in theright temporal region or in the right hemisphere

ts the ictal onset over the right temporal lobe.

Ictal spitting in left temporal lobe epilepsy: Report of three cases 465

Figure 3 (A) Semi-invasive record. The arrow marks ictal onset characterized by desynchronization of brain electricactivity in the contacts of the left FO electrode. (B) Aproximatelly 20 seconds later, the arrow shows involvement of therigth FO electrodes contacts by ictal activity.

(Fig. 2). In the remaining seizure, ictal onset couldnot be lateralized. Due to discordant neurophysio-logical and imaging data, foramen ovale (FO) elec-trodes were implanted bilaterally for a newprolonged video-EEG monitoring. With FO electro-des, baseline EEG showed marked slowing over leftbasal temporal region. Bitemporal sharp waves wereregistered. The patient had three seizures. In one ofthem he had spitting automatism. In all three ictalonset consisted of desynchronization of brain elec-tric activity in the contacts of the left FO electrode,followed by emergence of a fast rhythm captured bythe contacts of the right FO electrode (Fig. 3).

The patient underwent left ATL. Few monthsafter surgery he had one seizure with equivocal lossof consciousness, related to skipping three doses ofAED. Since then, he has not had any more seizures,with follow-up of 2 years.

Discussion

Spitting automatisms can be easily recognized dur-ing epileptic seizures. Though quite stereotyped,these automatisms are seldom reported in patientswith epilepsy.1—8

466 L.O.S.F. Caboclo et al.

Automatisms are complex behaviors resemblingnormal movements. Automatic spitting may repre-sent an oral motor automatism similar to the morecommon chewing and swallowing automatisms, fre-quently reported in patients with TLE.1 It may occurin the context of other automatisms such as ictalemesis12 and ictal coughing, presumed to be asso-ciated to right nondominant temporal seizure activ-ity.5 However, ictal spitting is rarely associated toautonomic features such as retching and vomiting,hypersalivation and piloerection. Therefore, it isunlikely that this automatism is due to involvementof central autonomic networks by ictal activity.8 Theexact cortical region responsible for originating thisparticular automatism is not known.1

Spitting may be induced in normal individuals bybad taste in the mouth. In patients with epilepsyspitting automatism might be due to ictal gustatoryhallucinations, though this is rarely the case inpatients previously reported.1,3,5,6,8 None of ourpatients complained of unpleasant gustatory sensa-tions during the simple partial phase of their sei-zures.

Most series and case reports of patients present-ing ictal spitting suggest that this particular auto-matism is a localizing sign pointing to the languagenondominant temporal lobe as the symptomato-genic zone.5,8

Hecker et al.1 reported five patients who pre-sented spitting automatism. In three of them, sei-zures were presumed to be originated in the righttemporal lobe; two of these patients were sub-mitted to surgical treatment–—right temporallobectomy. Two of them had probable seizure onsetin the left temporal lobe, but in only one interictalspikes were registered over this region.

Fakhoury et al.3 described the cases of twopatients with ictal spitting, both appearing to haveseizures originating in the right temporal lobe.

Voss et al.5 reported five patients with ictalspitting. These were right-handed and left hemi-sphere dominant for language, as evaluated byintracarotid amobarbital test. All of them hadlesions in the right temporal lobe, and were sub-mitted to resection on this side, leading to signifi-cant reduction or cessation of the seizures. Theauthors concluded that ictal spitting, althoughuncommon, may be considered a localizing sign tothe nondominant temporal lobe.

Kellinghaus et al.8 described the characteristicsof 12 patients who had ictal spitting. In their series,8 of the 12 had seizures originating from the right,nondominant hemisphere, while only two had sei-zure onset in the language-dominant hemisphere.

Ozkara et al.10 reported the case of a patient withleft HS who had spitting automatisms. However,

Wada test revealed that the patient had right-sideddominance for language and memory. Therefore,spitting automatisms were considered as originatingin nondominant temporal lobe in this particularpatient.

The three patients reported in our series had leftHS. In two, all seizures arose from the left temporallobe. In the third scalp-sphenoidal EEG showedseizures originating from the right temporal lobe,but semi-invasive monitoring with FO electrodesshowed that in fact seizures originated from theleft temporal lobe, concordant with the side of theHS, thus, confirming the hypothesis of false later-alization in surface EEG recording.

One potential limitation of our conclusions is thefact that none of the three patients had Wada testbefore surgery to confirm language dominance inthe left hemisphere. Wada test was not considerednecessary during presurgical evaluation, and hencewas not indicated. Nevertheless, the three patientswere right-handed, and thus most likely had left-sided language dominance.

In these three patients all seizures had clinicaland electrographic features consistent with tem-poral lobe onset, corroborating the localizingvalue of ictal spitting. Most importantly, all threebecame seizure-free after ATL. However, in allthree patients the seizures originated from theleft temporal lobe. Therefore, it appears thatalthough the localizing value of this symptom ishigh, pointing to the temporal lobe as the symp-tomatogenic zone, ictal spitting should not beviewed as a lateralizing semiological sign inpatients with TLE.

Acknowledgements

This work was supported by FAPESP (Fundacao deAmparo a Pesquisa do Estado de Sao Paulo) andCAPES (Coordenacao de Aperfeicoamento de Pessoalde Nıvel Superior)/CNPq (Conselho Nacional deDesenvolvimento Cientıfico e Tecnologico).

References

1. Hecker A, Andermann F, Rodin EA. Spitting automatism intemporal lobe seizures with a brief review of ethological andphylogenetic aspects of spitting. Epilepsia 1972;13:762—72.

2. Carmant L, Riviello J, Thiele EA, Kramer U, Helmers SL,Mikati M, et al. Compulsory spitting: an unusual manifesta-tion of temporal lobe epilepsy. J Epilepsy 1994;7:167—70.

3. Fakhoury T, Abou-Khalil B, Peguero E. Differentiating clinicalfeatures of right and left temporal lobe seizures. Epilepsia1994;35:1038—44.

Ictal spitting in left temporal lobe epilepsy: Report of three cases 467

4. Dantas FG, Yacubian EM, Jorge CL, Pedreira CC, Bueno JF,Valerio RM. Clinical and EEG analysis of mesial and lateraltemporal lobe seizures. Arq Neuropsiquiatr 1998;56:341—9.

5. Voss NF, Davies KG, Boop FA, Montouris GD, Hermann BP.Spitting automatisms in complex partial seizures: a nondo-minant temporal localizing sign? Epilepsia 1999;40:114—6.

6. Kahane P, Minotti L. Spitting automatism. Epileptic Disord2000;2:231—2.

7. Ozkara C, Hanoglu L, Eskazan E, Ozyurt E. Spitting as an ictalevent. Epileptic Disord 2001;3:49.

8. Kellinghaus C, Loddenkemper T, Kotagal P. Ictal spitting:clinical and electroencephalographic features. Epilepsia2003;44:1064—9.

9. Kaplan PW, Kerr DA, Olivi A. Ictus expectorarus: a sign ofcomplex partial seizures usually of nondominant temporallobe origin. Seizure 1999;8:480—4.

10. Ozkara C, Hanoglu L, Eskazan E, Kulaksizogvlu IB, Ozyurt E.Ictal spitting during a left temporal lobe-originated complexpartial seizure: a case report.EpilepticDisord2000;2:169—72.

11. Commission on classification and terminology of the Interna-tional League Against Epilepsy: proposal for revised classifi-cation of epilepsies and epileptic syndromes. Epilepsia1989;30:389—99.

12. Kramer RE, Luders HO, Goldstick LP, Dinner DS, Morris HH,Lesser RP, et al. Ictus emeticus: an electroclinical analysis.Neurology 1988;38:1048—52.