Ictus expectoratus: a sign of complex partial seizures usually of non-dominant temporal lobe origin

Ictus expectoratus: a sign of complex partial seizures usually of non-dominant temporal lobe origin

Seizure 1999; 8: 480–484 Article No. seiz.1999.0345, available online at http://www.idealibrary.com on CASE REPORT Ictus expectoratus: a sign of co...

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Seizure 1999; 8: 480–484

Article No. seiz.1999.0345, available online at http://www.idealibrary.com on

CASE REPORT

Ictus expectoratus: a sign of complex partial seizures usually of non-dominant temporal lobe origin †



PETER W. KAPLAN , DOUGLAS A. KERR & ALESSANDRO OLIVI

∗†



Johns Hopkins Bayview Medical Center, Eastern Avenue, Baltimore, MD 21224, USA; † Johns Hopkins University, School of Medicine, Baltimore, MD, USA Correspondence to: Dr Peter W. Kaplan, Johns Hopkins Bayview Medical Center, 4940 Eastern Avenue, Baltimore, MD 21224, USA

Spitting (or expectoration) is rarely seen with seizures. In Western society, spitting is a striking behavioral aberration. A 13year-old child had intermittent agitated behavior, episodes of rage, spitting and confusion lasting up to 2 minutes. He stood up in church and told the preacher to ‘shut up and sit down’. Epilepsy monitoring revealed spitting with polysharp and spike seizures resolved over the right temporal lobe. Magnetic resonance imaging revealed a right temporal lobe ganglioglioma. Spitting seizures resolved after resection. Ictal expectoration is rare. It may occur with epigastric aura, nausea, chewing, swallowing and fumbling. Literature review disclosed 17 cases, 12 of which arose from the non-dominant hemisphere. Most regressed with surgery and anticonvulsants. c 1999 BEA Trading Ltd

Key words: complex partial seizure; spitting; expectoration; ganglioglioma; temporal lobe.

INTRODUCTION Although initially mentioned by Dr Hughlings Jackson1 in citing a case presented by Sander2 in 1874, spitting (or expectoration) is an uncommon feature of seizures3–6 . Because of the cultural stigma associated with spitting in Western society, its appearance out of context (e.g. not by baseball players during a game) is a striking behavioral aberration. Spitting signals not only attention to the event itself, but probably links the localization of ictal activity to structures subserving the phylogenetically similar areas involved in chewing, smell, swallowing, nausea and vomiting. We present a case of ictal expectoration due to ganglioglioma, and its treatment by temporal lobe resection.

CASE REPORT A 13-year-old, right-handed schoolboy had a year’s history of intermittent agitated behavior, episodes of 1059–1311/99/080480 + 05

$12.00/0

rage, paroxysmal nausea without vomiting and spitting. These episodes lasted between 15 seconds and 2 minutes, but were followed by periods of lethargy. During the 4 weeks prior to admission, the episodes increased in frequency and changed in character. On several occasions he had been noticed to sit up suddenly, reach around for a basket or other receptacle and to spit (but not retch) several times before resuming other activities or lying back and going to sleep. The episodes were often followed by headache. He was brought to the emergency room by his father because of his abnormal behavior. The previous week, the patient had suddenly stood up in church and in a loud voice, had told the preacher to ‘shut up and sit down’. Because his parents were separated, he lived at times with one or the other parent, and on one occasional had awoken suddenly exclaiming to his brother ‘what I am doing here—How did I get here?’, looked markedly agitated and disturbed, and denied any recollection of going to the house. Although he had been doing well in school, the significant social and domestic problems c 1999 BEA Trading Ltd

Ictus expectoratus: a sign of complex partial seizures

had led to concerns that his behavioral disturbances were ‘acting out’. During one episode, the mother reported that his pupils became small, that he got up and looked around ‘aggressively’ and tried to walk into a closet before wandering around the room. During this circuitous episode the patient appeared lucid and carried on a conversation, but subsequently had no memory of the event. Past medical history included asthma as a child, a diagnosis of attention deficit hyperactivity disorder (for which he received methylphenidate hydrochloride until the year before), but no other significant disease. On examination, he was a healthy-appearing, slightly obese but otherwise normal adolescent with normal higher cortical function, cranial motor/sensory and muscle stretch reflex examination. Admitted overnight for epilepsy monitoring, he had several typical spells characterized by his suddenly sitting up in bed, complaining of nausea and reaching for a receptacle to spit into. There was no complaint of bad taste in the mouth, chewing, retching, sniffing, nose wiping or other discernible automatisms. On one occasion he jumped up, ripping off all the EEG leads and went to the bathroom. EEG showed polysharp and spike activity building up progressively to higher voltage, lower frequency discharges from the right temporal lobe. Magnetic resonance imaging showed a 1.5 cm gadolinium-enhancing mass in the mesial right temporal lobe tip. He was treated for 1 month with carbamazepine and had no further seizures until he had a right temporal craniotomy with partial mesial temporal lobe resection. Pathological study of the lesion revealed it to be a ganglioglioma. He remains on carbamazepine and has had no further spitting seizures.

DISCUSSION This patient had bizarre behavioral outbursts for several months that had been attributed to a reaction to his parents’ domestic problems. His outbursts were sudden and inappropriate, but were sufficiently brief that when followed by lethargy and sleep on most occasions, his parents and social entourage had just chalked them up to his ‘psychological make-up’. It was only with an admission to hospital that the brief, explosive nature of these episodes were able to be witnessed by medical personnel, and the acute, aggressive character of these behavioral outbursts were connected to a confusional state and loss of memory for the event. Epilepsy monitoring captured the events and showed that they arose from a right temporal abnormality, later diagnosed pathologically as a ganglioglioma. Gangliogliomas are tumors comprised of both neuronal and glial cell types which account for approximately 1% of

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primary CNS tumors7 . They most commonly present with seizures8–10 . Between 67% and 84% of gangliogliomas occur in the temporal lobe8–10 , a finding which may account for the epileptogenicity of these tumors. Most studies have revealed that total resection of these tumors yields seizure- and recurrencefree survival in more than 90% of patients without adjuvant therapy. A recent study has highlighted the association of gangliogliomas in six children or young adults with behavioral abnormalities post-operatively11 . Four of the five had temporal lobe lesions (two left; two right), but all had delusions, hallucinations, agitation, hostile or aggressive behavior similar to our case. In contrast, our patient’s behavioral manifestations occurred before resection of the tumor. The association of gangliogliomas and aggressive or delusional behavior is poorly understood. Some have postulated that ‘alien tissue’ representing small developmental lesions engender ‘severe social and psychological difficulties, most of which are hard to codify within precise psychiatric categories’12 . No explanation for this association is forthcoming. Spitting is only rarely mentioned in association with complex partial seizures1–6 . In most cases it is involved with other automatisms more clearly suggestive of temporal lobe involvement. In the majority of patients, the act of spitting occurs during the period of confusion, probably as an ictal or post-ictal phenomenon rather than as an aura. Documented cases are given in the Table. Hecker et al.3 reviewed five cases between the ages of 16 and 35 with temporal lobe complex partial seizures. These were often associated with epigastric aura, a sensation of nausea, abnormal taste and automatisms consisting of chewing, swallowing and fumbling. Following the epigastric sensation of cramps, the patient usually became unresponsive during (or after) which the spitting took place. In all cases, seizures lasted only 1–3 minutes. Three of the five cases had some degree of mental retardation. In only three of the five cases was an ictal onset demonstrated on EEG; in one case over the right frontocentral temporal region; or right posterior temporal region, another involved the lateral inferior right temporal region and in the third, a left temporal and frontal origin. A tumor was excised in one patient, but the patient continued to have EEG evidence of irregular bilateral spike-and-wave discharges. Carmant et al.4 report three patients with temporal lobe onset: one left, one right, and one bilateral. Fakhoury et al.5 have described two patients with spitting automatisms due to right mesial temporal sclerosis with a right temporal lobe ictal onset. Both patients were seizure free after temporal lobectomy. More recently, Voss et al.6 reported five patients with spitting automatisms also with right temporal lobe ictal onset.

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P. W. Kaplan et al.

Table 1: Expectoratory seizures (ictus expectoratus): clinical features. Case#

Age Sex

IQ

Epilepsy duration (yr.)

Seizure type

Seizure duration (min)

Spitting

Other features

Lesion localization

EEG

Cause

Outcome

11,2

53

M

NI IQ → Dull Mentally

1

SPS

1–2 up to 12 x/d

Post-ictal SPS → CPS

Dreadful, disagreeable smell, sweating, staring, chewing → face jerks

Lt. fronto temposphenoidal tumor. Olfactory glioma



Tumor



23

21

F

MR



SPS → CPS

0.5–0.83

Nonpurposeful ictal

Epigastric aura; fumbling of hands

Rt. temporal



Prenatal pathology



33

16

F

MR

2

SPS → CPS

2–3

Ictal

Visual aura ‘arms shook’

Lt. temporal



Prenatal anoxia



43

20

F

MR

17

SPS → CPS



Ictal; ‘directed’

‘Abdominal aura’; then olfactory/gustatory aura

Rt. amygdala, uncus, first temporal gyrus

Rt. fronto-temporal Rt. posterior temporal

Rt. temporal astrocytoma resection



53

22

F

NI

9

SPS → CPS



Ictal, but during SPS or CPS

Aura of thirst and dry throat; starting; chewing; swallowing

Rt. temporal

Rt. lateral/inferior temporal

Tumor resection



63

35

M

MR

34

CPS



Ictal CPSz

Head → left; clapping hands; swinging arms

Lt. temporal

Lt. temporal > Lt. frontal

Prenatal anoxia



74

20

F



11

SPS → CPS



Ictal SPS or CPS ‘urge to spit’

Tingling in throat

CT/MRI:Nl

Rt. temporal slowing; rare spikes → bifrontal temporal epileptiform discharges

?

Rt. temp. lobectomy SF

84

21

M



21

CPS



Ictal CPS

‘Strange laugh’; jerking of right arm/leg



Lt. anterior temporal sz. Rt. temp. nocturnal sz.

Tuberous sclerosis



94

11

M



0.25

SPS



Ictal SPS

Headaches; Rt arm tingling; tinnitus

Lt. temporal

Lt. temporal delta waves. Occasional spikes

Lt. temp. pleomorphic glioma

Lt. temp. lobectomy SF

105

20

M

FSIQ 91

13

SPS → CPS

1–1.5

Ictal

Staring; motor automatisms

Rt. temporal MRI + (MTS)

Right inferomesial temporal onset

MTS

Rt. temp. lobectomy SF

115

27

F

FSIQ 99

20

SPS SPS

0.75–1.5

Ictal

Dystonic posturing left arm

Rt. temporal MRI + (MTS)

Right inferomesial temporal onset

Ganglioglioma/MTS

Rt. temp. lobectomy SF

→ CPS 126

21

M

FSIQ 89

6

CPS



Ictal



Rt. mesial temporal MRI +

Rt. interictal scalp

Oligodendroglioma



136

26

M



10

CPS



Ictal



Rt. mesial temporal MRI +

Rt. ictal scalp

DNET

SF

146

38

F

114

33

CPS



Ictal



Rt. mesial temporal MRI +

Rt. ictal scalp Spike & wave

Cavernous angioma

SF

156

27

F

83

22

CPS



Ictal



Rt. mesial temporal

Rt. Ictal scalp 7–10 Hz

Hippocampal gliosis

90% ↓Sz.

166

39

F

86

38.75

CPS



Ictal



Rt. mesial temporal

Bilat Rt. > Lt. Spike & wave

Hippocampal sclerosis

90% ↓ Sz.

17 Present Case 13

M

Normal ‘(Honors Student)’

1

SPS → CPS

0.25–2.0

Ictal

Nausea; vomiting; epigastric discomfort; bizarre behavior; anger; agitation; cursing → lethargy

Rt. temporal ‘cystic lesion’ (MRI +; CT −) Prolactin not ↑

Rt. posterior temporal electrodecremental pattern, then 7–8 Hz sharp waves → 2 Hz

Ganglioglioma

Rt. temp. lobectomy SF

SPS = single partial seizure; CPS = complex partial seizure; MR = mental retardation; NI = normal; Lt = left; Rt = right; Sz = seizure; SF = Seizure free; DNET dysembryoplastic neuroepithelioma; MTS = mesial temporal sclerosis.

Ictus expectoratus: a sign of complex partial seizures

All had surgical right temporal lobe resection of which two had tumors, [dysembryoblastic neuroepithelial tumor (DNET); oligodendroglioma]; one each had cavernous angioma, hippocampal gliosis and hippocampal sclerosis. All patients had at least 90% or greater regression of seizures. In the excellent review of the phylogenetic role and functioning of spitting by Hecker et al.3 , the authors mention that Darwin observed that in humans, ‘spitting seems an almost universal sign of contempt or disgust and obviously represents the rejection of anything offensive from the mouth’. From Shakespeare, the authors quote: (Duke of Norfolk): ‘I spit at him, called him a slanderous coward and a villein’, and out of the mouth of Fallstaff, ‘tell thee what, Hal, if I tell thee a lie, spit in my face’. Conrad Lorenz considered spitting to be a motor pattern common to humans, consisting of a complex behavioral manifestation with different cultural connotations in different population groups (personal communication between Lorenz and Hecker et al.3 ). It is also interesting to speculate that women with such an automatism would come to medical attention earlier that men. As Hecker et al.3 put it: ‘Women often have difficulty in spitting, whereas men, as boys may have had more experience and are rarely unable to do so’. The human ethologist, Eidl-Eibesfeldt regarded spitting as an act of aggression in many populations3 . These observations are in keeping with some of the aggressive outbursts of our patient, but an equally viable explanation is that there is ictal involvement of temporal structures subserving specific automatisms that arise from closely related regions (those involved with smell, nausea, vomiting, chewing and swallowing), most of which were not present in our patient. In the 16 cases cited and in our case, the temporal lobe is involved in the epileptic process (Table 1)1–6 , usually the non-dominant temporal lobe (12 of 16 cases). Other non-dominant temporal lobe ictal signs include vomiting3, 5, 13–16 , fear, and coughing5 , suggesting asymmetry for oroalimentary control in the cortex that lateralizes to the right6 . In all the patients, however, the spitting differs from the act in normal individuals in whom spitting usually follows the perception of a bad taste in the mouth, and a desire to expectorate the contents. Excessive salivation (noted in the case of Sander2 ) has been localized to the post-central gyrus just above the Sylvian fissure17 and is seen in right temporal lobe seizures18 . Seizures arising from diencephalic regions may produce profuse salivation but curiously do not involve spitting. No specific localization for spitting has as yet been defined but it probably involves activation of cortical areas mediating gastrointestinal function such as the insula6 . Although not reported with ictal vomiting, nose wiping or coughing3, 5, 6 , our patient displayed ictal anger.

483

CONCLUSION Most cases of ictus expectoratus arise from the nondominant temporal lobe either with simple or complex partial seizures6 . This may reflect the fact that the seizures involve at some point in their propagation, the non-dominant temporal lobe, rather than being the obligate site of ictal onset.

ACKNOWLEDGEMENTS Many thanks to Dr Keith Davies6 of Baptist Memorial Hospital, Memphis, TN and Dr Toufic Fakhoury5 of Vanderbilt University, Nashville, TN for the data cited on their patients in Table 1.

REFERENCES 1. Jackson, J. H. Selected Writings of John Hughlings Jackson, Vol. 1. (Ed. J. Taylor). New York, Basic Books, 1958. 2. Sander, W. Epileptische Anf¨alle mit subjektiven Geruchsempfindungen bei Zerst¨orung des linken tractus olfactorius durch einen Tumor. Archives of Psychiat. Nervenkr. 1894; 4: 234–243. 3. Hecker, A., Andermann, F. and Rodin, E. A. Spitting automatism in temporal lobe seizures with a brief review of ethological and phylogenetic aspects of spitting. Epilepsia 1972; 13: 767–772. 4. Carmant, L., Riviello, J. J., Thiele, E. A. et al., Compulsory spitting: an unusual manifestation of temporal lobe epilepsy. Journal of Epilepsy 1994; 7: 167–170. 5. Fakhoury, T., Abou-Khalil, B. and Peguero, E. Differentiating clinical features of right and left temporal lobe seizures. Epilepsia 1994; 35: 1038–1044. 6. Voss, N. F., Davies, K. G., Boop, F. A., Montouris, G. D. and Hermann, B. P. Spitting automatism in complex partial seizures: a nondominant temporal localizing sign? Epilepsia 1999; 40: 114–116. 7. Kalyan-Raman, U. P. and Olivero, W. C. Ganglioglioma: a correlative clinicopathological and radiological study of ten surgically treated cases with follow-up. Neurosurgery 1987; 20: 428–433. 8. Wolf, H. K., Muller, M. B., Spanle, M., Zentner, J., Schramm, J. and Wiestler, O. D. Ganglioglioma: a detailed histopathological and immunohistochemical analysis of 61 cases. Acta Neuropathology 1994; 88: 166–173. 9. Zentner, J., Wolf, H. K., Ostertun, B. et al., Gangliogliomas: clinical, radiological, and histopathological findings in 51 patients. Journal of Neurology, Neurosurgery and Psychiatry 1994; 57: 1497–1502. 10. Ventureyra, E., Herder, S., Mallya, B. K. and Keene, D. Temporal lobe gangliogliomas in children. Childs Nervous System 1986; 2: 63–66. 11. Andermann, L. F., Savard, G., Meencke, H. F., McLachlan, R., Mosh´e, S. and Andermann, F. Psychosis after resection of ganglioglioma or DNET: evidence for an association. Epilepsia 1999; 40: 83–87. 12. Taylor, D. C. Factors influencing the occurrence of schizophrenia-like psychosis in patients with temporal lobe epilepsy. Psychology in Medicine 1975; 5: 249–254. 13. Hermann, B. P., Wyler, A. R., Blumer, D. and Richey, E. T.

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15. 16.

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P. W. Kaplan et al. Ictal fear: lateralizing significance and implications for understanding the neurobiology of pathological fear states. Neuropsychiatry, Neuropsychology and Behavioural Neurology 1992; 5: 205–210. Devinsky, O., Frasca, J., Pacia, S. V. et al., Ictus emeticus: further evidence of nondominant temporal involvement. Neurology 1995; 45: 1158–1160. Jacome, D. E. and FitzGerald, R. Ictus emeticus. Neurology 1982; 32: 209–212. Kramer, R. E., Luders, H., Goldstick, L. P. et al., Ictus emeticus: an electroclinical analysis. Neurology 1988; 38: 1048– 1052. Penfield, W. and Faulk, M. E. The insula: further observations on its function. Brain 1955; 78: 445–470. Freeman, R. and Schachter, S. C. Autonomic epilepsy. Seminars in Neurology 1995; 15: 58–168.

EDITOR’S NOTE I am a little troubled by the phrase ‘expectoratus’. I cannot find the word in my edition of Jackson and, in a sense, the patient was not expectorating (the clearing from the throat of unwanted phlegm) but spitting.

If Jackson or others have already coined the phrase, then it would be acceptable as the authors are merely quoting previous usage. If not, have they chosen the right word? Classical Latin only had one meaning for expectorare, which was to get it off the chest (i.e. clear the mind). Expectorate in terms of bringing up phlegm first appeared in the English language in 1601 (in a pharmacological context). It did not acquire the meaning of spit at, or spit on, until the mid nineteenth century. The Latin for spit was sputare: consputare for spit at, exputare for spit out. Spittle was of course, sputum. The word ictus itself in classical Latin meant a blow: its medical use for stroke and/or seizure again seems to have been mid nineteenth century. So if they are coining a new phrase, should it not be ictus consputarum? Tim Betts Editor