Typical and atypical perfusion patterns in periictal SPECT of patients with unilateral temporal lobe epilepsy

PURPOSE: To characterize perfusion patterns of periictal single-photon emission tomography (SPECT) in patients with unilateral temporal lobe epilepsy (TLE) and to determine their relationship to the epileptogenic zone (EZ). METHODS: We studied periictal SPECT scans of 53 patients after anterior mesial temporal lobectomy who had good seizure outcome after surgery. Ictal SPECT scans were performed during video-EEG monitoring. Typical SPECT patterns consisted of ipsilateral ictal hyperperfusion or ipsilateral postictal hypoperfusion. Atypical ictal patterns included normal scans, bilateral temporal hyperperfusion, or contralateral patterns. These perfusion patterns were retrospectively analyzed searching for concordance rate with the EZ. RESULTS: We obtained 51 ictal and two early postictal scans. In the typical group, 40 (75.4%) patients had ipsilateral ictal temporal lobe hyperperfusion, and one (1.9%) patient had ipsilateral postictal temporal lobe hypoperfusion. Twelve (22.7%) patients exhibited atypical perfusion patterns: seven (13.2%) patients had bitemporal ictal hyperperfusion (four cases showed asymmetric temporal lobe changes), four (7.6%) patients had contralateral hyperperfusion, and one (1.9%) patient had a normal SPECT scan. All four patients with bitemporal asymmetric hyperperfusions showed greater perfusion lateralized to the side of the EZ. Three of the four patients who had contralateral hyperperfusion also had a complex postictal-like pattern in the ipsilateral temporal lobe consisting of anteromesial hyperperfusion with adjacent lateral hypoperfusion. CONCLUSIONS: This study analyzed typical and atypical perfusion patterns in unilateral TLE, and suggested that not only typical, but also some atypical perfusion patterns may contribute to the lateralization of EZ.     

Postictal mania versus postictal psychosis: differences in clinical features, epileptogenic zone, and brain functional changes during postictal period

PURPOSE: To clarify the differences between postictal mania (PIM) and postictal psychosis (PIP). METHODS: Five patients with PIM were compared to 17 patients with PIP, with respect to clinical, epileptological, electrophysiological, and neuroimaging features. PIM was distinguished from PIP by the symptoms observed in the postictal period based on the ICD-10 criteria. RESULTS: Postictal manic episodes lasted for a longer period than postictal psychotic episodes. Patients with PIM had more recurrent postictal episodes than patients with PIP. The age at onset of epilepsy in patients with PIM was older than that in patients with PIP. PIM was associated with frontal lobe and temporal lobe epilepsies, whereas PIP was associated with temporal lobe epilepsy. The estimated epileptogenic zone was on the language dominant side in PIM, whereas there was no predominant hemispheric laterality in PIP. Electroencephalography (EEG) performed during the early period of postictal manic and psychotic episodes showed decreased frequency of interictal epileptiform discharges in both PIM and PIP. Single-photon emission computed tomography (SPECT) during postictal manic and psychotic episodes showed increased perfusion in the temporal and/or frontal lobes in both PIM and PIP. Three patients with PIM showed increased perfusion during postictal episodes on bilateral or the language nondominant side, which were contralateral to the estimated epileptogenic zone, whereas three patients with PIP showed increased perfusion on the areas, which were ipsilateral to the estimated epileptogenic zone. CONCLUSIONS: PIM has a distinct position among the mental disorders observed in the postictal period.     

TLE patients with postictal psychosis: mesial dysplasia and anterior hippocampal preservation

The authors studied six patients with refractory temporal lobe epilepsy and postictal psychosis using quantitative MRI and histopathology, and compared the results with 45 patients with temporal lobe epilepsy without postictal psychosis. Total hippocampal volumes were not different between the two groups. However, patients with postictal psychosis had a relatively preserved anterior hippocampus, and temporal lobe dysplasia was more frequent (p = 0.006, chi-square test). These findings may be associated with the clinical symptoms.     

Violence and Epilepsy: A Close Relation Between Violence and Postictal Psychosis

Summary: Purpose: We investigated the incidence of well-directed violent behavior and suicide attempts in patients with temporal lobe epilepsy, with special attention to postictal psychosis.
Methods: We compared 57 episodes of postictal psychosis with 62 episodes of acute interictal (or alternative) psychosis and with 134 complex partial seizures. All patients were matched for age and for age at onset of seizures.
Results: The incidence of well-directed violent behavior against human beings was significantly higher (23%) during postictal psychotic episodes than during acute interictal episodes (5%) and postictal confusion (1%). Suicide attempts were also more frequent during postictal psychosis (7%) than during either acute interictal psychosis (2%) or postictal confusion (0%).
Conclusions: Our study showed that well-directed violent and self-destructive behavior was not a feature of epileptic psychosis in general but a specific hallmark of postictal psychosis.     

Late postictal residual perfusion abnormality in epileptogenic zone found on 6-hour postictal SPECT

BACKGROUND: Temporal evolution of regional hyperperfusion in the late postictal stage in epilepsy has not been clearly defined. OBJECTIVE: To establish the late temporal evolution of the perfusion in epileptogenic zones using 6-hour postictal SPECT. METHODS: Ictal 99mTc-hexamethylpropyleneamine oxime (99mTc-HMPAO) SPECT was performed in 10 patients with intractable epilepsy (4 temporal lobe epilepsy, 6 neocortical epilepsy) followed by delayed acquisition and another 6-hour postictal SPECT after reinjection of 99mTc-HMPAO. The delayed acquired SPECT was subtracted from the reinjection SPECT to yield the 6-hour postictal SPECT. Interictal SPECT was acquired on another day. Late postictal perfusion was examined visually, and asymmetric indexes were compared with each other on ictal, 6-hour postictal, and interictal SPECT. RESULTS: Ictal SPECT images of delayed acquisition were visually and quantitatively similar to those of early acquisition. In 7 of 10 patients, 6-hour postictal SPECT showed hyperperfusion. In one patient, the 6-hour postictal SPECT image showed less perfusion than the interictal SPECT image in the epileptogenic zone. CONCLUSIONS: Late postictal hyperperfusion was found in more than half of the patients. Postictal perfusion abnormalities did not come back to the interictal phase 6 hours after ictus and these were identified on ictal/postictal 99mTc- HMPAO SPECT.     

Ictal hyperperfusion patterns according to the progression of temporal lobe seizures

OBJECTIVE: To investigate ictal hyperperfusion patterns during semiologic progression of seizures, the authors performed SPECT subtraction in 50 patients with temporal lobe epilepsy (TLE). METHODS: The patients were categorized into five groups according to semiologic progression during ictal SPECT (Group 1 had aura only; Group 2 had motionless staring with or without aura; Group 3 had motionless staring and then automatism with or without aura; Group 4 had motionless staring and then dystonic posturing with or without aura and automatism; and Group 5 had motionless staring, automatism, then head version and generalized seizures with or without aura and dystonic posturing). RESULTS: In Group 1, three patients showed ipsilateral temporal hyperperfusion and two had bilateral temporal hyperperfusion with ipsilateral predominance. In Group 2, three patients (42.9%) showed bilateral temporal hyperperfusion with unilateral predominance and four patients (57.1%) revealed insular hyperperfusion of epileptic side. In Group 3, 15 patients (88.2%) showed bilateral temporal hyperperfusion with unilateral predominance and 12 patients (70.6%) revealed insular hyperperfusion. In Group 4, 11 patients (84.6%) showed basal ganglia hyperperfusion on the opposite hemisphere to the side of the dystonic posturing. In Group 5, there were multiple hyperperfusion areas in the frontal, temporal, and basal ganglia regions. However, the injection times of radiotracer in five groups were relatively short and similar. CONCLUSIONS: The semiologic progression in TLE seizures were related to the propagation of hyperperfusion from ipsilateral temporal lobe to contralateral temporal lobe, insula, basal ganglia, and frontal lobe. Not only the radiotracer injection time but also semiologic progression after the injection was important to determine hyperperfusion pattern of ictal SPECT.     

Postictal psychosis and its electrophysiological correlates in invasive EEG: a case report study and literature review

We identified two patients with medically refractory temporal lobe epilepsy, from whom intracranial EEG recordings were obtained at the time of postictal psychosis. Both patients had mesial temporal epilepsy associated with hippocampal sclerosis. In both patients, the postictal psychosis was associated with a continual "epileptiform" EEG pattern that differed from their interictal and ictal EEG findings (rhythmical slow wave and "abortive" spike-slow wave complex activity in the right hippocampus and lateral temporal cortex in case 1 and a periodic pattern of triphasic waves in the contacts recording activity from the left anterior cingulate gyrus). Some cases of postictal psychosis might be caused by the transient impairment of several limbic system structures due to the "continual epileptiform discharge" in some brain regions. Case 2 is the first report of a patient with TLE in whom psychotic symptoms were associated with the epileptiform impairment of the anterior cingulate gyrus.     

Temporal Lobe Epilepsy Subtypes: Differential Patterns of Cerebral Perfusion on Ictal SPECT

Summary: Purpose : We studied cerebral perfusion patterns in the various subtypes of TLE, as determined by pathology and good outcome after temporal lobectomy (as confirmation of temporal origin).
Methods : We studied clinical features and ictal technetium ^99m hexamethyl-propyleneamineoxime (99mTc-HM-PAO) single-photon emission-computed tomography (SPECT) in four subgroups of patients with intractable temporal lobe epilepsy (TLE) treated with surgery: hippocampal sclerosis (group 1, n = 10), foreign-tissue lesion in mesial temporal lobe (group 2, n = 8), foreign-tissue lesion in lateral temporal lobe (group 3, n = 7), and normal temporal lobe tissue with good surgical outcome (group 4, n = 5).
Results : No major clinical differences in auras, complex partial seizures or postictal states were identified among the groups. Ictal SPECT showed distinct patterns of cerebral perfusion in these subtypes of TLE. In groups 1 and 2, hyperperfusion was seen in the ipsilateral mesial and lateral temporal regions. In group 3, hyperperfusion was seen bilaterally in the temporal lobes with predominant changes in the region of the lesion. Hyperperfusion was restricted to the ipsilateral anteromesial temporal region in group 4. Ipsilateral temporal hyperperfusion in mesial onset seizures can be explained by known anatomic projections between mesial structures and ipsilateral temporal neocortex. Bilateral temporal hyperperfusion in lateral onset seizures can be explained by the presence of anterior commissural connections between lateral temporal neocortex and the contralateral amygdala.
Conclusions : We conclude that the perfusion patterns seen on ictal SPECT are helpful for subclassification of temporal lobe seizures, whereas clinical features are relatively unhelpful. These perfusion patterns provide an insight into preferential pathways of seizure propagation in the subtypes of TLE.     

Brain perfusion following single seizures

PURPOSE: The aim of this study was to assess the regional relative interictal and postictal perfusion changes in temporal and parietal lobe epilepsy. METHODS: We investigated interictal and postictal magnet resonance perfusion changes in five patients with temporal lobe epilepsy either with hippocampal sclerosis (n = 3) or without (n = 2), and in one patient with extratemporal (parietal lobe) epilepsy. T(2)*-weighted single-shot echo-planar images were acquired after bolus application of 0.2 mmol/kg gadolinium-diethylene triamine pentaacetic acid (GD-DTPA) at baseline and after intervals of 2-12 min, 15-23 min, 28-50 min, 63-72 min, and 180-240 min. The bolus-peak ratio was calculated in regions of interest in the hippocampus (HIP), parahippocampal gyrus (PHG), thalamus (THA), cortex (COR), and white matter (WM), yielding relative perfusion changes. RESULTS: Interictally, we found relative hyperperfusion of the ictogenic side in five of six patients in the HIP. Postictally, the perfusion decreased in the HIP by 25-39% as compared to baseline, whereas the PHG showed a reverse pattern. In the late postictal phase, perfusion increased in the HIP again and decreased in the PHG. In the THA, the inter- and postictal changes were small (5-19%). COR and WM showed equivocal results. CONCLUSION: Postictal relative hypoperfusion in the HIP appears to be associated with the cessation of neuronal ictal discharge, whereas postictal hyperperfusion in the PHG lags behind and may reflect increased metabolism to restore the interictal state of neuronal excitability.     

Postictal mania associated with frontal lobe epilepsy

A 38-year-old man, possibly with frontal lobe epilepsy, developed postictal mania. The changes in psychiatric symptoms and laboratory examinations over time were investigated in two episodes of postictal mania, using long-term electroencephalography with closed circuit television (EEG/CCTV) monitoring, magnetoencephalography (MEG), and single-photon emission computed tomography (SPECT) to elucidate the underlying mechanism of postictal mania. According to the clinical symptoms, the postictal manic episodes of this case had four phases: a lucid interval, manic phase, hypomanic phase, and recovery phase. EEG showed forced normalization during the florid manic phase. The serial findings of EEG, MEG, and SPECT during the postictal manic episodes suggest that functional changes in bilateral frontal lobes, especially the right frontal lobe, right temporal lobe, and right paralimbic area, are crucial in the development of postictal mania, and that these functional changes are dynamic.     

Prolonged postictal psychosis with forced normalization (Landolt) in temporal lobe epilepsy

We report two patients with temporal lobe epilepsy who developed prolonged episodes of postictal psychosis (12 weeks) following a bout of seizures and a lucid interval. No drug toxicity was noted, and no recurrent or continuous seizures were observed during their prolonged psychotic episodes. Repeated EEGs during the period of psychosis showed that their habitual focal epileptiform abnormalities had disappeared. Responses to neuroleptic treatments were not remarkable. Their psychotic symptoms gradually dispelled after their epileptiform abnormalities reappeared. These observations may suggest possible overlapping mechanisms between a prolongation of psychosis and suppression of epileptiform discharges on a scalp EEG.     

Psychosis in epilepsy patients

Summary   Epileptic psychoses reflect a fundamental disruption in the fidelity of mind and occur during seizure freedom or during or after seizures. The psychotic symptoms in epilepsy share some qualities with schizophrenic psychosis, such as positive symptoms of paranoid delusions and hallucinations. Psychotic syndromes in epilepsy are most common but not exclusively associated with temporal lobe epilepsy. De Novo psychosis following epilepsy surgery is rare. Forced normalization—psychosis associated with dramatic reduction of epileptiform activity or seizures is described in small series only. Ictal and postictal psychosis can be prevented with seizure control, but postictal and chronic interictal psychoses require multidisciplinary and psychopharmacologic management.     

Spirituality and religion in epilepsy

Revered in some cultures but persecuted by most others, epilepsy patients have, throughout history, been linked with the divine, demonic, and supernatural. Clinical observations during the past 150 years support an association between religious experiences during (ictal), after (postictal), and in between (interictal) seizures. In addition, epileptic seizures may increase, alter, or decrease religious experience especially in a small group of patients with temporal lobe epilepsy (TLE). Literature surveys have revealed that between .4% and 3.1% of partial epilepsy patients had ictal religious experiences; higher frequencies are found in systematic questionnaires versus spontaneous patient reports. Religious premonitory symptoms or auras were reported by 3.9% of epilepsy patients. Among patients with ictal religious experiences, there is a predominance of patients with right TLE. Postictal and interictal religious experiences occur most often in TLE patients with bilateral seizure foci. Postictal religious experiences occurred in 1.3% of all epilepsy patients and 2.2% of TLE patients. Many of the epilepsy-related religious conversion experiences occurred postictally. Interictal religiosity is more controversial with less consensus among studies. Patients with postictal psychosis may also experience interictal hyper-religiosity, supporting a "pathological" increase in interictal religiosity in some patients. Although psychologic and social factors such as stigma may contribute to religious experiences with epilepsy, a neurologic mechanism most likely plays a large role. The limbic system is also often suggested as the critical site of religious experience due to the association with temporal lobe epilepsy and the emotional nature of the experiences. Neocortical areas also may be involved, suggested by the presence of visual and auditory hallucinations, complex ideation during many religious experiences, and the large expanse of temporal neocortex. In contrast to the role of the temporal lobe in evoking religious experiences, alterations in frontal functions may contribute to increased religious interests as a personality trait. The two main forms of religious experience, the ongoing belief pattern and set of convictions (the religion of the everyday man) versus the ecstatic religious experience, may be predominantly localized to the frontal and temporal regions, respectively, of the right hemisphere.     

Subacute postictal aggression in patients with epilepsy

Three men with epilepsy (age range, 38-62) who exhibited brief episodes of violent behavior during the postictal period are described. Disease duration ranged from 27 to 44 years. Patients had both complex partial seizures and secondarily generalized tonic-clonic seizures, which were refractory to antiepileptic drugs. Postictal aggression occurred shortly after a seizure and lasted 5-30 minutes. The patients displayed physically and verbally aggressive behavior toward others, but regained consciousness promptly and showed regret afterward. Interictal EEGs revealed temporal spikes, SPECT showed hypoperfusion in the temporal and frontal areas in two patients, and neuropsychological examination revealed poor frontal lobe function in two patients. Characteristics of our cases are consistent with subacute postictal aggression (SPA) reported previously. Epilepsy of prolonged duration and brain dysfunction involving a broad area including the temporal and frontal lobes may be associated with the occurrence of subacute postictal aggression.     

Localization of extratemporal epileptic foci during ictal single photon emission computed tomography.

We obtained single photon emission computed tomography (SPECT) scans with technetium-99M-hexamethyl-propylene-amine-oxime in 11 patients during 12 extratemporal partial seizures (9 simple partial, 3 complex partial). Ten ictal SPECT studies in 9 patients showed a focal region of hyperperfusion, which agreed with electrical seizure onset in 5 and with clinical seizure localization in 4 in whom ictal electroencephalography was not localized. Contralateral cerebellar and ipsilateral basal ganglia hyperperfusion was seen in 3 patients with a frontal lobe seizure focus. Ictal hyperperfusion was well circumscribed, unlike the diffuse hyperperfusion changes reported during temporal lobe seizures. This observation may indicate a different degree of seizure spread in temporal as opposed to extratemporal epilepsy. Because electroencephalographic localization is often elusive in extratemporal seizures, ictal SPECT may be very helpful for the localization of extratemporal foci.     

Interictal and postictal alterations of pulsatile secretions of luteinizing hormone in temporal lobe epilepsy in men

Mesial temporal lobe epilepsy has been associated with abnormalities of reproductive physiology, but the mechanisms of hormonal dysregulation are not clear. Chronic effects of the epileptic state and the acute impact of seizures could alter hypothalamic function, which is represented by the downstream pulsatile secretion of luteinizing hormone. This study evaluates the interictal and postictal secretion of luteinizing hormone in mesial temporal lobe epilepsy. We characterized luteinizing hormone secretion in patients with mesial temporal lobe epilepsy during two 24-hour epochs: an interictal baseline and a postictal interval initiated by an electrographically confirmed spontaneous seizure. Males, rather than females, were studied so that menstrual cycles could not account for differences between epochs. Blood luteinizing hormone and prolactin (as a positive control) were measured every 10 minutes. Deconvolution analysis defined luteinizing hormone secretion in terms of interpulse interval, amplitude, and mass. Approximate entropy quantitated relative degradation in the orderliness of serial luteinizing hormone release. Interictal baseline epochs were compared to those of healthy controls with unpaired Student's t tests and between interictal and postictal epochs within epileptic patients with paired t tests. Ten epileptic men completed both interictal and postictal epochs. Interictally, seizure patients had lower mean concentrations, slower pulse rates, and higher peak amplitudes than healthy male controls. Within epileptic patients, mean interpulse interval, pulse amplitude, and pulse mass were not affected by the occurrence of seizures, whereas the orderliness of pulse mass decreased postictally. Acute seizures induced timing irregularity in luteinizing hormone secretion, whereas chronic epilepsy was associated with changes in luteinizing hormone pulse frequency, amplitude, and mass. Altered timing and regularity of neuroendocrine pulse patterns may underlie other disorders of homeostasis in mesial temporal lobe epilepsy.     

Behaviors induced or disrupted by complex partial seizures

We reviewed the neural mechanisms underlying some postictal behaviors that are induced or disrupted by temporal lobe seizures in humans and animals. It is proposed that the psychomotor behaviors and automatisms induced by temporal lobe seizures are mediated by the nucleus accumbens. A non-convulsive hippocampal afterdischarge in rats induced an increase in locomotor activity, which was suppressed by the injection of dopamine D(2) receptor antagonist in the nucleus accumbens, and blocked by inactivation of the medial septum. In contrast, a convulsive hippocampal or amygdala seizure induced behavioral hypoactivity, perhaps by the spread of the seizure into the frontal cortex and opiate-mediated postictal depression. Mechanisms underlying postictal psychosis, memory disruption and other long-term behavioral alterations after temporal lobe seizures, are discussed. In conclusion, many of the changes of postictal behaviors observed after temporal lobe seizures in humans may be found in animals, and the basis of the behavioral change may be explained as a change in neural processing in the temporal lobe and the connecting subcortical structures.     

A prospective study of postictal psychoses with emphasis on the periictal type

PURPOSE: To assess prospectively episodes of postictal psychosis. METHODS: We followed 108 consecutive patients with temporal lobe epilepsy, who were divided into three groups: those without psychotic episodes (n=87, N group), those with interictal psychosis (n=13, IIP group), and those with postictal psychosis (n=8, PIP group). The first episode of postictal psychosis, which was defined as a psychotic episode that occurred within 1 week after the end or within 3 days before the beginning of seizure clusters, was assessed with the Brief Psychiatric Rating Scale (BPRS) and Social Dysfunction and Aggression Scale (SDAS) during the observation period. RESULTS: The duration of illness was significantly different between the N and PIP groups (p=0.004) and between the N and IIP groups (p=0.039). The average initial BPRS score (obtained 3.0 days after the end of the seizure cluster) was 19.7, and then decreased to 5.8 after 1 week, and finally normalized at 1.5 after 1 month. A statistically significant decrease in BPRS scores was found between the initial assessment and those obtained after 1 week (p=0.011). Those who had psychotic episodes without a lucid interval tended to have episodes more often than monthly, and experienced additional seizure recurrence even during the psychotic episodes. Two patients exhibited a frank manic phase, and three patients showed excessively aggressive behavior, as determined by the SDAS. CONCLUSIONS: Postictal psychosis should be subdivided into the nuclear type, with an established clinical picture as an indirect aftereffect of seizure activity, and the atypical periictal type, which is a direct manifestation of limbic discharge.     

Postictal switch in blood flow distribution and temporal lobe seizures.

The ictal increase of regional cerebral blood flow has yet to be fully utilised in the investigation of focal seizures. Although single photon emission tomography (SPECT) is being increasingly used in the localisation of epileptic foci, the evolution and time courses of the peri-ictal perfusion changes have yet to be clarified. We performed serial SPECT studies in the interictal, ictal and immediate postictal states in 12 patients with refractory temporal lobe epilepsy to define the patterns and duration of peri-ictal cerebral blood flow changes. Visual analysis showed a constant pattern of unilateral global increases in temporal lobe perfusion during seizures which suddenly switched to a pattern of relative mesial temporal (hippocampal) hyperperfusion and lateral temporal hypoperfusion in the immediate postictal period. Quantitative analysis confirmed the visual assessment. Lateral temporal cortex ictal/normal side to side ratios were increased by mean 35.1% (95% confidence interval 21.8% to 48.4%) more in the ictal studies than in the interictal studies and mesial temporal cortex ratios increased by mean 30.8% (22.4% to 39.2%). In the postictal state, however, lateral temporal ratios were reduced by mean 7.7% (-15.8% to 0.4%) compared with interictal values, whereas mesial temporal perfusion was maintained compared with the interictal studies. These observations provide critical information for interpreting scans which can be used in the localisation of epileptic foci. This postictal switch in blood flow patterns may reflect the underlying metabolic processes of neuronal activation and recovery and have implications for understanding the neurobiology of human epileptic seizures.     

Acute postictal psychosis: a stereo EEG study

An acute psychosis characterized by auditory hallucinations and paranoid delusions developed in a 19-year-old man with temporal lobe epilepsy after he had a cluster of seizures when antiepileptic drugs (AEDs) had been gradually discontinued. Continuous sterotactic depth and epidural EEG recordings confirmed that this was a postictal rather than an ictal event. Acute postictal psychosis is a self-limited condition phenomenologically distinct from ictal or postictal confusion.