BRAIN
AND
LANGUAGE
42, 419-430 (1992)
Recurrent Fluent Aphasia Associated with a Seizure Focus RACHELLE SMITH DOODY,* RICHARD A. HRACHOVY,~ AND EDWARD P. FEHER’ Departments of *Neurology
and fNeurophysiology, Baylor College of Medicine and Houston VA Medical Center
The relationship between dominant hemisphere seizure activity and aphasia is unclear. Although speech arrest, expressive speech problems, and comprehension difficulties have often been associated with temporal lobe seizure activity, neologistic, paraphasic speech is rare. We report a patient with seizures following encephalitis who had recurrent episodes of fluent, severely aphasic speech with impaired comprehension which correlated with continuous, high voltage spike and slow wave activity in the left temporal region. During a several-day period of intermittent electrographic seizure activity, he had fluctuating receptive aphasia, and he developed transient paranoid psychosis following treatment. We discuss the behavioral manifestations of his left temporal seizures and correlate the changing nature of his behavior with therapeutic interventions. This case, as well as a review of others, suggests that paroxysmal fluent aphasia results from a partially treated electrographic seizure focus in the dominant temporal lobe. o 1%~ Academic Press. Inc.
INTRODUCTION Serafetinides and Falconer (1963) reviewed 100 cases of dysphasia and speech automatisms during clinical seizures. They concluded that dysphasia was secondary to the spread of ictal discharges in the dominant hemisphere, while speech automatisms could result from discharges in either hemisphere. They did not specifically characterize their patients as fluent or nonfluent aphasics. In their work, as in more recent retrospective studies (Ardila & Lopez, 1988; Koerner & Laxer, 1988; Gabr, Luders, Dinner, et al., 1989), the descriptions of aphasia were nosologically inadequate and incomplete. The few cases in the literature in which wellPresented, in part, at the American Electroencephalographic Society meeting, September 23, 1990, Houston, TX. Address correspondence and reprint request to Rachelle Smith Doody, M.D., Department of Neurology, Baylor College of Medicine, 6.550Fannin, Suite 1801, Houston, TX 77030. ’ Present address: Memory Assessment Clinics, Inc., Bethesda, MD. 419 0093-934X/92 $5.00 Copyright 0 1992 by Academic Press, Inc. All rights of reproduction in any form reserved.
420
SMITH
DOODY,
HRACHOVY,
AND
FEHER
defined aphasia has been correlated with an electrographic seizure discharge are valuable for theories of the pathogenesis of this rare disorder. Bell, Horner, Logue, et al., (1990) described neologistic speech automatisms in a patient with left temporooccipital seizures. They suggested that epileptic interference, activation, or release phenomena might account for the language disturbance. We describe a patient with a nonreiterative form of fluent jargon aphasia, also associated with a left seizure focus. Our case and literature review suggest that a very limited seizure discharge, most likely in the setting of partial treatment, gives rise to fluent ictal aphasia. Our case also demonstrates that psychotic manifestations may occur in the recovery phase of fluent ictal aphasia and supports theories relating psychotic features to temporal lobe epilepsy. CASE REPORT D.L. was a 47-year-old right-handed Hispanic man. One and one-half years prior to admission (March 1988) he developed a headache followed by fever and a right focal seizure, which then generalized. He was admitted elsewhere with a diagnosis of encephalitis. He did well after discharge until 2 months later when he was readmitted for the sudden onset of confusion. Left frontal brain biopsy was nondiagnostic, and he was discharged on Dilantin and phenobarbital (PBS). Seven months later, he was readmitted for worsening mental status and given a lo-day course of acyclovir. He improved gradually to a baseline of good functioning, although he did not return to work. His family felt that he understood all but the most difficult discussions, and he continued to read and take care of his usual activities, except that he did not handle his finances alone. He took 200 mg Dilantin po BID; phenobarbital was being tapered just prior to admission. The patient was admitted to the Houston VAMC on September 23, 1989 for the sudden onset of altered mental status. He had apparently felt well in the morning and had been talking about job prospects with his family. They left and returned a half hour later to find him crying and confused, unable to explain what was the matter. On mental status examination, he was reportedly alert and disoriented to person, place, time, and situation, although his answers to all questions were confounded by receptive aphasia. General physical examination was unremarkable and general neurological examination showed only slight circumduction of the right lower extremity. An SMAC and CBC were normal, as were thyroid function tests, vasculitis screen, and cerebrospinal fluid examination. Dilantin level was 14.4 and PBS was 8.8. An MRI showed no change compared to his postcraniotomy study 16 months previously: there was a slight generalized increase in ventricular size and no focal abnormalities. On the morning after admission, his EEG showed normal background
FLUENT APHASIA Orientation
(by written
questions)
9/10
correct
on MMS
Attention/concentration
Variable
Memory
Unable to perform recall, memory for or recall individual delay
Spontaneous
speech
*Auditory
(see text)
Fluent, not paraphasias,
comprehension
aloud
Mild, occasional sentences)
*Reading
comprehension
Mildly correct) Variable
Insight praxis
Correctly
coannands
defective (18/60 Naming test)
*Reading
Constructional
(O/8 sentences)
Performed some 1 & Z-step (Z/5 sentences) Moderately on Boston
Naming
verbal story visual designs, words after a
neologistic, occasional some fragmentation
Very defective
*Repetition
421
WITH SEIZURE FOCUS
correct
paraphasias
impaired
(5/7
(5/7
commands
drawing
on MMS
(see text) copied
MMS - Mini-Mental Status Questionnaire *From Boston Aphasia Exam, Revised
FIG. 1. Neuropsychological test results from D.L. on Hospital Day 5
activity with recurrent moderate to high voltage spike and slow and sharp and slow wave activity in the left temporal region that was pseudoperiodic, occurring every 1-3 sec. On the second hospital day, he had two episodes of staring with unresponsiveness that correlated with continuous spike and wave discharges in the left temporooccipital region on EEG. He was given 10 mg of Valium without clinical effect, and loaded with 500 mg Dilantin and 60 mg PBS. A follow-up EEG showed a left temporal slow wave focus with frequent spikes and sharp waves and a normal background. Neurobehavioral
Assessment
We were asked to see the patient on the fifth hospital day. Early in the AM, he underwent formal neuropsychological testing (Fig. 1). Attention-concentration performance was variable: He spelled “world” backward quickly and without errors, but made two errors in stating the months of the year backward. On the “A’s test” of vigilance, he made three omission errors. He could not complete the series l-A, 2-B, 3-C, etc. but was accurate on the Digit-Symbol substitution subtest of the Wechsler Adult Intelligence Scale (WAIS-R). He was fully oriented when persistently questioned in writing, although he did not comprehend the orientation questions when questioned orally. Visual and verbal memory were not testable due to comprehension difficulties. He showed moderate auditory comprehension deficits as assessedby selected items from subtests
422
SMITH DOODY, HRACHOVY,
AND FEHER
of the Boston Aphasia Exam (Boston Aphasia Exam, Revised). He consistently followed simple one- and two-step commands. Speech was fluent and paraphasic, with discernable phrases. A typical speech sample from the testing session was: “I lost my language-I’m just kind of waking up-1 lost my concen-I’m just now concentrating-Everybody that’s talking to me I don’t understand them (spoken rapidly).” Confrontation naming was moderately defective. Reading aloud was only mildly impaired, and reading comprehension was mildly to moderately impaired. His insight into his situation was inconsistent in that he seemed not to realize when he was not making sense, but verbalized his difficulty understanding others. At the end of the session he laughed suddenly, stood up, stared, and began exhibiting motor automatisms (eye blinking, picking movements with fingers). For several minutes he could only respond to questions with “si” or “yes”. He was led back to his bed, and this spell of staring and diminished responsiveness remitted. His aphasia was much worse when he regained fluency a few minutes later. He was alert and tried to communicate, at times expressing frustration by nonverbal gestures. He could not engage in orientation or memory testing as he seemed not to understand what was being asked of him. Speech was now almost completely neologistic and unintelligible. Verbal comprehension was markedly decreased compared to his performance during the testing session: He understood no verbal commands and could imitate only a few whole body actions. He was unable to read aloud, producing neologistic jargon. He could still copy a drawing. At times, he stopped talking and blinked for a few seconds, without vocalization: These episodes lasted less than 1 min. While the patient displayed his severe receptive aphasia as well as during the brief episodes of speech arrest, bedside EEG showed continuous 2Hz spike and slow wave complexes in the left temporal region (See Fig. 2). Ativan, 4 mg, and Dilantin, 200 mg, intravenously did not immediately alter the electrographic seizure activity, although the patient eventually went to sleep. An EEG several hours later no longer showed the continuous left temporal spike and wave discharge; however, there was a slow wave focus mixed with random sharp and spike wave activity in this region. Tegretol was started. The remained of his hospital course is summarized in Table 1, and a follow-up EEG is shown in Fig. 3. DISCUSSION We report a case of fluent, jargon aphasia that is clearly associated with a left temporal electrographic seizure focus. Our case is one of the few reports of epileptic aphasia that meets Rosenbaum’s criteria for ictal aphasia: the patient must be alert, must speak during the event, and must demonstrate dysfluency, dysnomia, or paraphasic speech concurrently with
FLUENT APHASIA
WITH SEIZURE FOCUS
Tegretol started p.o.
“Clinically improved.” Better comprehension, less paraphasias, but still aphasic. Neuropsychiatric testing documented a moderate posterior aphasia. Clinically observed complex partial seizure at the end of testing. Paroxysmal worsening of posterior aphasia with neologistic jargon aphasia and almost no verbal comprehension. Brief episodes consistent with complex partial seizures intermittently. Several hours later, patient lethargic.
10 mg Valium iv, no clinical change. 500 mg Dilantin iv and 60 mg PBS iv. Dilantin level 10.7. PBS level 13.3.
Continuous discharge gone. Left temporal slow wave focus with random sharp and spike wave activity.
“Clinically unchanged.”
3
4 mg Ativan iv, 200 mg Dilantin iv induced sleep but did not change electrographic focus immediately.
No EEG.
Episodes of staring with unresponsiveness during EEG.
2
Dilantin level 14.4 Taking 200 mg BID PBS level 8.8. 60 mg PBS iv given. Maintenance dose of 30 mg TID started.
Therapeutic interventions/drug levels @g/ml)
Continuous ~-HZ spike and slow wave complexes in left temporal region (Fig. 2).
Recurrent spike and wave and sharp and wave complexes in left temporal region, occurring every 1-3 sec. Background normal. Continuous spike and wave discharges in left temporoocciptal region. Normal background. Left temporal slow wave focus with frequent spikes and sharp waves.
“Fluctuating receptive aphasia.” No further description.
1
COURSE
EEG
TABLE 1 EEG, AND TREATMENT
Behavioral observations
Hospital day
BEHAVIORAL,
FLUENT APHASIA
WITH SEIZURE FOCUS
425
FLUENT APHASIA
WITH SEIZURE FOCUS
427
electrographic seizure activity (Rosenbaum, Seigel, Barr, et al., 1986). The paroxysmal occurrence of neologistic speech and severely impaired language comprehension ceased when his electrographic focus disappeared as a result of drug therapy. A similar electrographic focus was, at times, associated with paucity of speech and typical complex partial seizures. Between electrographic seizures, the patient suffered a variable receptive aphasia, most likely due to posticital changes in the speech areas. Our case, considered with that of Bell et al. (1990) suggests that posterior ictal aphasia can manifest as fluent neologistic speech as well as neologistic speech automatisms. After resolution of the electrographic focus the patient experienced paranoia and delusions (Table l), which resolved several days after his seizures were controlled. Although prior studies have not reported the occurrence of psychosis during recovery from epileptic aphasia, Zivi, Broussard, Daymas, Hazard, & Sicard, (1990) suggested a possible relationship among electrographic seizure activity, aphasia, and psychosis in children with acquired epileptic aphasia. Crowe and Kuttner’s recent study suggeststhat patients with temporal lobe epilepsy have more marked positive symptoms, such as hallucinations and delusions, than schizophrenic patients without temporal lobe epilepsy (Crowe & Kuttner, 1991). Our patient’s psychotic manifestations were primarily delusions and paranoia, which is consistent with their findings. The fact that his psychotic features developed after the ictal aphasia resolved suggestsdifferent mechanisms for these two disturbances. Kanemoto and Jantz (1989) investigated the aura manifestations of patients with “complex focal seizures.” They found that ictal aphasia occurred infrequently (17%) and tended to occur late in an aura sequence in association with other sensations (such as deja vu). These findings suggest that a certain threshold of electrical spread must be obtained in order to produce ictal speech. Further, the electrical activity must probably remain at this level, without generalization, in order for aphasia to persist instead of developing into generalized confusion. Such a well-developed but circumscribed seizure focus may occur more readily in partially treated patients, such as our patient. Only four other studies have reported patients with fluent ictal aphasia, although none of them correlated the presence and absence of a seizure focus with full descriptions of neurobehavioral and treatment status (Racy, Osborn, Bern, et al., 1980; Wilson, Petty, Perry, et al., 1983; Knight & Cooper, 1986; Bell, Horner, Logue, et al., 1990). Although treatment details are sketchy for these patients with fluent ictal aphasia, most had received some prior antiepileptic therapy. The rare occurrence of posterior ictal aphasia raises some questions about the relationship between seizure activity and abnormal cellular brain substrates. Structural damage to Wernicke’s area, in the absence of sei-
428
SMITH
DOODY,
HRACHOVY,
AND
FEHER
zures, usually causes persistent receptive aphasia. It has been argued that jargon aphasia due to structural damage such as a cerebrovascular accident may require damage to the arcuate fasciculus as well as to Wernicke’s area (Kertesz & Benson, 1979). Yet, we have clearly shown that recurrent seizure discharges in the dominant temporal region can manifest a posterior aphasia with or without neologistic jargon speech. If the arcuate fasciculus must be involved to produce jargon aphasia, the cortical seizure discharges must interfere with normal functioning of the arcuate fasciculus. Alternatively, jargon aphasia due to ictal discharges may occur by a different mechanism, or arcuate fasciculus damage may not be an essential feature. Bell’s patient with fluent aphasia had an arteriovenous malformation in the dominant temporal lobe, and one of Racy’s cases had a left subdural hematoma. Our patient and Racy’s other case had a history of encephalitis, but no focal lesion on CT and MRI. Knight and Cooper’s patient and Wilson’s patient apparently had ideopathic seizures, with no focal lesions on CT. Although it would be preferable to have MRI studies on all of these patients, evidence so far indicates that recurrent posterior aphasia can occur in the absence of macroscopic structural damage. Ictal fluent aphasia must be rare in cases of infarction, as no such patients have been reported. The mechanism of fluent aphasia associated with seizures appears to be a combination of ictal and postictal cortical dysfunction in partially treated patients, and in a setting of minimal tissue destruction. Arcuate fasciculus pathways are probably not involved, even in patients with jargon aphasia. Interestingly, severe receptive aphasia following neurological disease or trauma is unusual in young children, presumably because of plasticity and the ability of non-language cortex to function in language acquisition (Cole, Andermann, Taylor, et al., 1988). Yet, patients with the onset of Landau-Kleffner syndrome before age 5 have a worse prognosis than older onset patients (Bishop, 1985). It may be that immature brains, possibly because of developmentally limited connectivity, circumscribe the seizure activity in this disorder, similar to the situation in adults with ictal aphasia related to partial treatment. In adult ictal aphasia patients as well as some Landau-Kleffner children (Msal, Shapiro, Balfour, et al., 1986), control of clinically manifest seizure activity may correlate with clinical improvement. APPENDIX:
SPEECH SAMPLES FROM D.L.
A. From history
“I’ve been disabled all this (incomprehensible neologisms), last week I lost a lot of (incomprehensible neologisms), I lost my concern I’m just now concentrated went to the hospital about an hour on my brain.”
FLUENT APHASIA
WITH SEIZURE FOCUS
429
B. Description of Cookie-Theft Picture “O.K. cookie jar, cookin-fallin’ water trees. To interpret what he’s doing? He’s falling . . . to get the cookies I don’t know if he’s trying to say and ofring? The water the sink. I told you about the she’s claimin? the glass. I don’t know if he’s asking him to drink or what the girl I don’t know if I can figure out if he’s a girl I mean a boy that’s about all the wh . . . outside.” REFERENCES Ardilla, A. & Lopez, V. 1988. Paroxysmal Aphasias. Epilepsia, 29(5), 630-634. Bell, W., Homer, J., Logue, P., et al. 1990. Neologistic speech automatisms during complex partial seizures. Neurology, 40, 49-52. Bishop, D. 1985. Age of onset and outcome in acquired aphasia with convulsive disorder. Developmental Medicine and Child Neurology, 27, 705-721. Cole, A., Andermann, F., Taylor, L., et al. 1988. The Landau-Kleffner syndrome of acquired epileptic aphasia: Unusual clinical outcome, surgical experience, and absence of encephalitis. Neurology, XI(l), 31-38. Crowe, S., & Kuttner, M., 1991. Differences between Schizophrenia and the Schizophrenialike psychosis of temporal lobe epilepsy. Neuropsychiutry Neuropsychology and Behavior Neurology, 4, 127-135. De Pasquet, E., Gaudin, E., Bianchi, A., et al. 1976. Prolonged and monosymptomatic dysphasic status epilepticus. Neurology, 26, 244-247. Dinner, D., Lueders, H., Lederman, R., et al. 1981. Aphasic status epilepticus: A case report. Neurology, 31, 889-890. Gabr, M., Lueders, H., Dinner, D:, et al. 1989. Speech manifestations in lateralization of temporal lobe seizures. Annuls of Neurology, 25, 82-87. Hamilton, N., & Matthews, T. 1979. Aphasia: The sole manifestation of focal status epilepticus. Neurology, 29, 745-748. Kanemoto, K., & Jantz, D. 1989. The temporal sequence of aurasensations in patients with complex focal seizures with particular attention to ictal aphasia. Journal of Neurology Neurosurgery
and Psychiatry,
52, 52-56.
Kertesz, A., & Benson, D. 1979. Neologistic jargon: A clinicopathological study. Cortex, 6, 362-386. Knight, R., & Cooper, J. 1986. Status epilepticus manifesting as reversible Wernicke’s aphasia. Epilepsiu, 27(3), 301-304. Koener, M., & Laxer, M. 1988. Ictal speech, postictal language dysfunction and seizure lateralization. Neurology, 38, 634-635. Lesser, R., Luders, J., Morris, H., et al. 1986. Electrical stimulation of Wernicke’s area interferes with comprehension. Neurology, 36, 658-663. Msal, M., Shapiro, B., Balfour, P., et al. 1986. Acquired epileptic aphasia: Diagnostic aspects of progressive language loss in preschool children. Clinical Pediatrics, 35(5), 248-251. Racy, A., Osborn, M., Bern, B., et al. 1980. Epileptic aphasia. Archives of Neurology, 37, 419-422. Rosenbaum, D., Siegel, M., Barr, W., et al. 1986. Epileptic aphasia. Neurology, 36, 822825. Serafetinides, E., & Falconer M. 1963. Speech disturbances in temporal lobe seizures: A study in 100 epileptic patients submitted to anterior temporal lobeectomy. Brain, 86, 333-346.
430
SMITH DOODY, HRACHOVY,
AND FEHER
Serafetinides, E., 1966. Speech findings in epilepsy and electrocortical stimulation: An overview. Cortex, 2, 463-473. Wilson, A., Petty, R., Perry, A., et al. 1983. Paroxysmal language disturbance in an epileptic treated with clobazam. Neurology, 33, 652-654. Zivi, A., Broussaud, G., Daymas, S., Hazard, J., & Sicard, C. 1990. Syndrome aphasie acquise-epilepsie avec psychose. Annales Pidiatrie (Paris), 37(6), 391-394.
AND
LANGUAGE
42, 419-430 (1992)
Recurrent Fluent Aphasia Associated with a Seizure Focus RACHELLE SMITH DOODY,* RICHARD A. HRACHOVY,~ AND EDWARD P. FEHER’ Departments of *Neurology
and fNeurophysiology, Baylor College of Medicine and Houston VA Medical Center
The relationship between dominant hemisphere seizure activity and aphasia is unclear. Although speech arrest, expressive speech problems, and comprehension difficulties have often been associated with temporal lobe seizure activity, neologistic, paraphasic speech is rare. We report a patient with seizures following encephalitis who had recurrent episodes of fluent, severely aphasic speech with impaired comprehension which correlated with continuous, high voltage spike and slow wave activity in the left temporal region. During a several-day period of intermittent electrographic seizure activity, he had fluctuating receptive aphasia, and he developed transient paranoid psychosis following treatment. We discuss the behavioral manifestations of his left temporal seizures and correlate the changing nature of his behavior with therapeutic interventions. This case, as well as a review of others, suggests that paroxysmal fluent aphasia results from a partially treated electrographic seizure focus in the dominant temporal lobe. o 1%~ Academic Press. Inc.
INTRODUCTION Serafetinides and Falconer (1963) reviewed 100 cases of dysphasia and speech automatisms during clinical seizures. They concluded that dysphasia was secondary to the spread of ictal discharges in the dominant hemisphere, while speech automatisms could result from discharges in either hemisphere. They did not specifically characterize their patients as fluent or nonfluent aphasics. In their work, as in more recent retrospective studies (Ardila & Lopez, 1988; Koerner & Laxer, 1988; Gabr, Luders, Dinner, et al., 1989), the descriptions of aphasia were nosologically inadequate and incomplete. The few cases in the literature in which wellPresented, in part, at the American Electroencephalographic Society meeting, September 23, 1990, Houston, TX. Address correspondence and reprint request to Rachelle Smith Doody, M.D., Department of Neurology, Baylor College of Medicine, 6.550Fannin, Suite 1801, Houston, TX 77030. ’ Present address: Memory Assessment Clinics, Inc., Bethesda, MD. 419 0093-934X/92 $5.00 Copyright 0 1992 by Academic Press, Inc. All rights of reproduction in any form reserved.
420
SMITH
DOODY,
HRACHOVY,
AND
FEHER
defined aphasia has been correlated with an electrographic seizure discharge are valuable for theories of the pathogenesis of this rare disorder. Bell, Horner, Logue, et al., (1990) described neologistic speech automatisms in a patient with left temporooccipital seizures. They suggested that epileptic interference, activation, or release phenomena might account for the language disturbance. We describe a patient with a nonreiterative form of fluent jargon aphasia, also associated with a left seizure focus. Our case and literature review suggest that a very limited seizure discharge, most likely in the setting of partial treatment, gives rise to fluent ictal aphasia. Our case also demonstrates that psychotic manifestations may occur in the recovery phase of fluent ictal aphasia and supports theories relating psychotic features to temporal lobe epilepsy. CASE REPORT D.L. was a 47-year-old right-handed Hispanic man. One and one-half years prior to admission (March 1988) he developed a headache followed by fever and a right focal seizure, which then generalized. He was admitted elsewhere with a diagnosis of encephalitis. He did well after discharge until 2 months later when he was readmitted for the sudden onset of confusion. Left frontal brain biopsy was nondiagnostic, and he was discharged on Dilantin and phenobarbital (PBS). Seven months later, he was readmitted for worsening mental status and given a lo-day course of acyclovir. He improved gradually to a baseline of good functioning, although he did not return to work. His family felt that he understood all but the most difficult discussions, and he continued to read and take care of his usual activities, except that he did not handle his finances alone. He took 200 mg Dilantin po BID; phenobarbital was being tapered just prior to admission. The patient was admitted to the Houston VAMC on September 23, 1989 for the sudden onset of altered mental status. He had apparently felt well in the morning and had been talking about job prospects with his family. They left and returned a half hour later to find him crying and confused, unable to explain what was the matter. On mental status examination, he was reportedly alert and disoriented to person, place, time, and situation, although his answers to all questions were confounded by receptive aphasia. General physical examination was unremarkable and general neurological examination showed only slight circumduction of the right lower extremity. An SMAC and CBC were normal, as were thyroid function tests, vasculitis screen, and cerebrospinal fluid examination. Dilantin level was 14.4 and PBS was 8.8. An MRI showed no change compared to his postcraniotomy study 16 months previously: there was a slight generalized increase in ventricular size and no focal abnormalities. On the morning after admission, his EEG showed normal background
FLUENT APHASIA Orientation
(by written
questions)
9/10
correct
on MMS
Attention/concentration
Variable
Memory
Unable to perform recall, memory for or recall individual delay
Spontaneous
speech
*Auditory
(see text)
Fluent, not paraphasias,
comprehension
aloud
Mild, occasional sentences)
*Reading
comprehension
Mildly correct) Variable
Insight praxis
Correctly
coannands
defective (18/60 Naming test)
*Reading
Constructional
(O/8 sentences)
Performed some 1 & Z-step (Z/5 sentences) Moderately on Boston
Naming
verbal story visual designs, words after a
neologistic, occasional some fragmentation
Very defective
*Repetition
421
WITH SEIZURE FOCUS
correct
paraphasias
impaired
(5/7
(5/7
commands
drawing
on MMS
(see text) copied
MMS - Mini-Mental Status Questionnaire *From Boston Aphasia Exam, Revised
FIG. 1. Neuropsychological test results from D.L. on Hospital Day 5
activity with recurrent moderate to high voltage spike and slow and sharp and slow wave activity in the left temporal region that was pseudoperiodic, occurring every 1-3 sec. On the second hospital day, he had two episodes of staring with unresponsiveness that correlated with continuous spike and wave discharges in the left temporooccipital region on EEG. He was given 10 mg of Valium without clinical effect, and loaded with 500 mg Dilantin and 60 mg PBS. A follow-up EEG showed a left temporal slow wave focus with frequent spikes and sharp waves and a normal background. Neurobehavioral
Assessment
We were asked to see the patient on the fifth hospital day. Early in the AM, he underwent formal neuropsychological testing (Fig. 1). Attention-concentration performance was variable: He spelled “world” backward quickly and without errors, but made two errors in stating the months of the year backward. On the “A’s test” of vigilance, he made three omission errors. He could not complete the series l-A, 2-B, 3-C, etc. but was accurate on the Digit-Symbol substitution subtest of the Wechsler Adult Intelligence Scale (WAIS-R). He was fully oriented when persistently questioned in writing, although he did not comprehend the orientation questions when questioned orally. Visual and verbal memory were not testable due to comprehension difficulties. He showed moderate auditory comprehension deficits as assessedby selected items from subtests
422
SMITH DOODY, HRACHOVY,
AND FEHER
of the Boston Aphasia Exam (Boston Aphasia Exam, Revised). He consistently followed simple one- and two-step commands. Speech was fluent and paraphasic, with discernable phrases. A typical speech sample from the testing session was: “I lost my language-I’m just kind of waking up-1 lost my concen-I’m just now concentrating-Everybody that’s talking to me I don’t understand them (spoken rapidly).” Confrontation naming was moderately defective. Reading aloud was only mildly impaired, and reading comprehension was mildly to moderately impaired. His insight into his situation was inconsistent in that he seemed not to realize when he was not making sense, but verbalized his difficulty understanding others. At the end of the session he laughed suddenly, stood up, stared, and began exhibiting motor automatisms (eye blinking, picking movements with fingers). For several minutes he could only respond to questions with “si” or “yes”. He was led back to his bed, and this spell of staring and diminished responsiveness remitted. His aphasia was much worse when he regained fluency a few minutes later. He was alert and tried to communicate, at times expressing frustration by nonverbal gestures. He could not engage in orientation or memory testing as he seemed not to understand what was being asked of him. Speech was now almost completely neologistic and unintelligible. Verbal comprehension was markedly decreased compared to his performance during the testing session: He understood no verbal commands and could imitate only a few whole body actions. He was unable to read aloud, producing neologistic jargon. He could still copy a drawing. At times, he stopped talking and blinked for a few seconds, without vocalization: These episodes lasted less than 1 min. While the patient displayed his severe receptive aphasia as well as during the brief episodes of speech arrest, bedside EEG showed continuous 2Hz spike and slow wave complexes in the left temporal region (See Fig. 2). Ativan, 4 mg, and Dilantin, 200 mg, intravenously did not immediately alter the electrographic seizure activity, although the patient eventually went to sleep. An EEG several hours later no longer showed the continuous left temporal spike and wave discharge; however, there was a slow wave focus mixed with random sharp and spike wave activity in this region. Tegretol was started. The remained of his hospital course is summarized in Table 1, and a follow-up EEG is shown in Fig. 3. DISCUSSION We report a case of fluent, jargon aphasia that is clearly associated with a left temporal electrographic seizure focus. Our case is one of the few reports of epileptic aphasia that meets Rosenbaum’s criteria for ictal aphasia: the patient must be alert, must speak during the event, and must demonstrate dysfluency, dysnomia, or paraphasic speech concurrently with
FLUENT APHASIA
WITH SEIZURE FOCUS
Tegretol started p.o.
“Clinically improved.” Better comprehension, less paraphasias, but still aphasic. Neuropsychiatric testing documented a moderate posterior aphasia. Clinically observed complex partial seizure at the end of testing. Paroxysmal worsening of posterior aphasia with neologistic jargon aphasia and almost no verbal comprehension. Brief episodes consistent with complex partial seizures intermittently. Several hours later, patient lethargic.
10 mg Valium iv, no clinical change. 500 mg Dilantin iv and 60 mg PBS iv. Dilantin level 10.7. PBS level 13.3.
Continuous discharge gone. Left temporal slow wave focus with random sharp and spike wave activity.
“Clinically unchanged.”
3
4 mg Ativan iv, 200 mg Dilantin iv induced sleep but did not change electrographic focus immediately.
No EEG.
Episodes of staring with unresponsiveness during EEG.
2
Dilantin level 14.4 Taking 200 mg BID PBS level 8.8. 60 mg PBS iv given. Maintenance dose of 30 mg TID started.
Therapeutic interventions/drug levels @g/ml)
Continuous ~-HZ spike and slow wave complexes in left temporal region (Fig. 2).
Recurrent spike and wave and sharp and wave complexes in left temporal region, occurring every 1-3 sec. Background normal. Continuous spike and wave discharges in left temporoocciptal region. Normal background. Left temporal slow wave focus with frequent spikes and sharp waves.
“Fluctuating receptive aphasia.” No further description.
1
COURSE
EEG
TABLE 1 EEG, AND TREATMENT
Behavioral observations
Hospital day
BEHAVIORAL,
FLUENT APHASIA
WITH SEIZURE FOCUS
425
FLUENT APHASIA
WITH SEIZURE FOCUS
427
electrographic seizure activity (Rosenbaum, Seigel, Barr, et al., 1986). The paroxysmal occurrence of neologistic speech and severely impaired language comprehension ceased when his electrographic focus disappeared as a result of drug therapy. A similar electrographic focus was, at times, associated with paucity of speech and typical complex partial seizures. Between electrographic seizures, the patient suffered a variable receptive aphasia, most likely due to posticital changes in the speech areas. Our case, considered with that of Bell et al. (1990) suggests that posterior ictal aphasia can manifest as fluent neologistic speech as well as neologistic speech automatisms. After resolution of the electrographic focus the patient experienced paranoia and delusions (Table l), which resolved several days after his seizures were controlled. Although prior studies have not reported the occurrence of psychosis during recovery from epileptic aphasia, Zivi, Broussard, Daymas, Hazard, & Sicard, (1990) suggested a possible relationship among electrographic seizure activity, aphasia, and psychosis in children with acquired epileptic aphasia. Crowe and Kuttner’s recent study suggeststhat patients with temporal lobe epilepsy have more marked positive symptoms, such as hallucinations and delusions, than schizophrenic patients without temporal lobe epilepsy (Crowe & Kuttner, 1991). Our patient’s psychotic manifestations were primarily delusions and paranoia, which is consistent with their findings. The fact that his psychotic features developed after the ictal aphasia resolved suggestsdifferent mechanisms for these two disturbances. Kanemoto and Jantz (1989) investigated the aura manifestations of patients with “complex focal seizures.” They found that ictal aphasia occurred infrequently (17%) and tended to occur late in an aura sequence in association with other sensations (such as deja vu). These findings suggest that a certain threshold of electrical spread must be obtained in order to produce ictal speech. Further, the electrical activity must probably remain at this level, without generalization, in order for aphasia to persist instead of developing into generalized confusion. Such a well-developed but circumscribed seizure focus may occur more readily in partially treated patients, such as our patient. Only four other studies have reported patients with fluent ictal aphasia, although none of them correlated the presence and absence of a seizure focus with full descriptions of neurobehavioral and treatment status (Racy, Osborn, Bern, et al., 1980; Wilson, Petty, Perry, et al., 1983; Knight & Cooper, 1986; Bell, Horner, Logue, et al., 1990). Although treatment details are sketchy for these patients with fluent ictal aphasia, most had received some prior antiepileptic therapy. The rare occurrence of posterior ictal aphasia raises some questions about the relationship between seizure activity and abnormal cellular brain substrates. Structural damage to Wernicke’s area, in the absence of sei-
428
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DOODY,
HRACHOVY,
AND
FEHER
zures, usually causes persistent receptive aphasia. It has been argued that jargon aphasia due to structural damage such as a cerebrovascular accident may require damage to the arcuate fasciculus as well as to Wernicke’s area (Kertesz & Benson, 1979). Yet, we have clearly shown that recurrent seizure discharges in the dominant temporal region can manifest a posterior aphasia with or without neologistic jargon speech. If the arcuate fasciculus must be involved to produce jargon aphasia, the cortical seizure discharges must interfere with normal functioning of the arcuate fasciculus. Alternatively, jargon aphasia due to ictal discharges may occur by a different mechanism, or arcuate fasciculus damage may not be an essential feature. Bell’s patient with fluent aphasia had an arteriovenous malformation in the dominant temporal lobe, and one of Racy’s cases had a left subdural hematoma. Our patient and Racy’s other case had a history of encephalitis, but no focal lesion on CT and MRI. Knight and Cooper’s patient and Wilson’s patient apparently had ideopathic seizures, with no focal lesions on CT. Although it would be preferable to have MRI studies on all of these patients, evidence so far indicates that recurrent posterior aphasia can occur in the absence of macroscopic structural damage. Ictal fluent aphasia must be rare in cases of infarction, as no such patients have been reported. The mechanism of fluent aphasia associated with seizures appears to be a combination of ictal and postictal cortical dysfunction in partially treated patients, and in a setting of minimal tissue destruction. Arcuate fasciculus pathways are probably not involved, even in patients with jargon aphasia. Interestingly, severe receptive aphasia following neurological disease or trauma is unusual in young children, presumably because of plasticity and the ability of non-language cortex to function in language acquisition (Cole, Andermann, Taylor, et al., 1988). Yet, patients with the onset of Landau-Kleffner syndrome before age 5 have a worse prognosis than older onset patients (Bishop, 1985). It may be that immature brains, possibly because of developmentally limited connectivity, circumscribe the seizure activity in this disorder, similar to the situation in adults with ictal aphasia related to partial treatment. In adult ictal aphasia patients as well as some Landau-Kleffner children (Msal, Shapiro, Balfour, et al., 1986), control of clinically manifest seizure activity may correlate with clinical improvement. APPENDIX:
SPEECH SAMPLES FROM D.L.
A. From history
“I’ve been disabled all this (incomprehensible neologisms), last week I lost a lot of (incomprehensible neologisms), I lost my concern I’m just now concentrated went to the hospital about an hour on my brain.”
FLUENT APHASIA
WITH SEIZURE FOCUS
429
B. Description of Cookie-Theft Picture “O.K. cookie jar, cookin-fallin’ water trees. To interpret what he’s doing? He’s falling . . . to get the cookies I don’t know if he’s trying to say and ofring? The water the sink. I told you about the she’s claimin? the glass. I don’t know if he’s asking him to drink or what the girl I don’t know if I can figure out if he’s a girl I mean a boy that’s about all the wh . . . outside.” REFERENCES Ardilla, A. & Lopez, V. 1988. Paroxysmal Aphasias. Epilepsia, 29(5), 630-634. Bell, W., Homer, J., Logue, P., et al. 1990. Neologistic speech automatisms during complex partial seizures. Neurology, 40, 49-52. Bishop, D. 1985. Age of onset and outcome in acquired aphasia with convulsive disorder. Developmental Medicine and Child Neurology, 27, 705-721. Cole, A., Andermann, F., Taylor, L., et al. 1988. The Landau-Kleffner syndrome of acquired epileptic aphasia: Unusual clinical outcome, surgical experience, and absence of encephalitis. Neurology, XI(l), 31-38. Crowe, S., & Kuttner, M., 1991. Differences between Schizophrenia and the Schizophrenialike psychosis of temporal lobe epilepsy. Neuropsychiutry Neuropsychology and Behavior Neurology, 4, 127-135. De Pasquet, E., Gaudin, E., Bianchi, A., et al. 1976. Prolonged and monosymptomatic dysphasic status epilepticus. Neurology, 26, 244-247. Dinner, D., Lueders, H., Lederman, R., et al. 1981. Aphasic status epilepticus: A case report. Neurology, 31, 889-890. Gabr, M., Lueders, H., Dinner, D:, et al. 1989. Speech manifestations in lateralization of temporal lobe seizures. Annuls of Neurology, 25, 82-87. Hamilton, N., & Matthews, T. 1979. Aphasia: The sole manifestation of focal status epilepticus. Neurology, 29, 745-748. Kanemoto, K., & Jantz, D. 1989. The temporal sequence of aurasensations in patients with complex focal seizures with particular attention to ictal aphasia. Journal of Neurology Neurosurgery
and Psychiatry,
52, 52-56.
Kertesz, A., & Benson, D. 1979. Neologistic jargon: A clinicopathological study. Cortex, 6, 362-386. Knight, R., & Cooper, J. 1986. Status epilepticus manifesting as reversible Wernicke’s aphasia. Epilepsiu, 27(3), 301-304. Koener, M., & Laxer, M. 1988. Ictal speech, postictal language dysfunction and seizure lateralization. Neurology, 38, 634-635. Lesser, R., Luders, J., Morris, H., et al. 1986. Electrical stimulation of Wernicke’s area interferes with comprehension. Neurology, 36, 658-663. Msal, M., Shapiro, B., Balfour, P., et al. 1986. Acquired epileptic aphasia: Diagnostic aspects of progressive language loss in preschool children. Clinical Pediatrics, 35(5), 248-251. Racy, A., Osborn, M., Bern, B., et al. 1980. Epileptic aphasia. Archives of Neurology, 37, 419-422. Rosenbaum, D., Siegel, M., Barr, W., et al. 1986. Epileptic aphasia. Neurology, 36, 822825. Serafetinides, E., & Falconer M. 1963. Speech disturbances in temporal lobe seizures: A study in 100 epileptic patients submitted to anterior temporal lobeectomy. Brain, 86, 333-346.
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AND FEHER
Serafetinides, E., 1966. Speech findings in epilepsy and electrocortical stimulation: An overview. Cortex, 2, 463-473. Wilson, A., Petty, R., Perry, A., et al. 1983. Paroxysmal language disturbance in an epileptic treated with clobazam. Neurology, 33, 652-654. Zivi, A., Broussaud, G., Daymas, S., Hazard, J., & Sicard, C. 1990. Syndrome aphasie acquise-epilepsie avec psychose. Annales Pidiatrie (Paris), 37(6), 391-394.
