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Keywords:

  • Postictal mania;
  • Postictal psychosis;
  • Epilepsy;
  • Frontal lobe;
  • Temporal lobe

Abstract

  1. Top of page
  2. Abstract
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES

Summary: 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.

Postictal psychosis (PIP) has been well studied and documented (Logsdail et al., 1988; Savard et al., 1991; Kanemoto et al., 1996). The symptoms of PIP are pleomorphic including various kinds of delusions, illusions of familiarity, auditory hallucinations, mental diplopia, disinhibited sexual behavior, pressured speech, and mood disturbances (Savard et al., 1991; Kanemoto et al., 1996; Kanner et al., 2004). The symptomatic pleomorphism suggests that the psychopathology that has been called “postictal psychosis” may include heterogeneous mental disorders.

We previously reported a patient with frontal lobe epilepsy who developed mania in the postictal period, and demonstrated functional changes in both hemisphere, especially the right frontal, temporal, and paralimbic areas during the postictal manic episodes (Nishida et al., 2005). Other reports (Wolf, 1982a; Hurwitz et al., 1985; Barczak et al., 1988; Byrne, 1988; Logsdail et al., 1988; Savard et al., 1991; Kanner et al., 1996; Chakrabarti et al., 1999; Kudo et al., 2001) also described cases of postictal mania (PIM) or postictal hypomania or seizure-related psychopathology equivalent to mania. Some cases of PIM or postictal hypomania were also reported after electroconvulsive therapy in patients with depression (Fink and Kahn, 1961; Andrade et al., 1988; Devanand et al., 1988).

However, manic states or manic symptoms in patients with epilepsy have not attracted attention, and only a few reports on interictal mania (Wolf, 1982a; Kudo et al., 2001), interictal dysphoric disorder (Blumer et al., 1995), and manic state after surgery (Kanemoto, 1995; Carran et al., 2003) are found in the literature. Furthermore, although there are reported cases of PIM, no study showed the clinical features and pathology of PIM as an entity.

We postulated that PIM and PIP not only differ in psychopathology, but are also distinct in the underlying biological processes. To examine this hypothesis, we compared patients with PIM to patients with PIP, with respect to the clinical features, localization and hemispheric laterality of the epileptogenic zone, and functional changes of the brain during postictal manic and psychotic episodes.

METHODS

  1. Top of page
  2. Abstract
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES

Patients

From about 5000 patients admitted to our hospital between 1989 and 2004, five patients with postictal mania (postictal mania group: PIM group; patients 1–5) and 17 patients with postictal psychosis (postictal psychosis group: PIP group; patients 6–22) were identified and recruited as subjects of this study. The patients or their close relatives gave their informed consent to the examinations done in this study.

PIM and PIP were diagnosed by the symptoms observed in the postictal period on the basis of ICD-10 (World Health Organization, 1992) criteria.

Ten postictal manic episodes were observed by neuropsychiatrists of our hospital during the five patients' hospitalization. These postictal manic episodes fulfilled the ICD-10 criteria for manic episode (F30), except for etiology. The cardinal symptoms that developed in the PIM group were elated mood, expansive mood, euphoric mood (p = 0.001 versus the PIP group), distractibility (p = 0.000), which showed significantly higher prevalence than those in the PIP group, and hyperactivity (p = 0.003), pressured speech (p = 0.002), decreased need for sleep (p = 0.006), flight of ideas (p = 0.043), grandiosity (p = 0.024), and hyperreligiosity (p = 0.039), which showed a tendency of higher prevalence than those in the PIP group as shown in Table 1.

Table 1. Symptoms of postictal mania and postictal psychosis
 Postictal mania group (n = 5)Postictal psychosis group (n = 17)p-value
  1. Significant level: 0.05/32 = 0.00156.

Elated mood/expansive mood/euphoric mood  5 (100%)2 (12%) 0.001
Emotional lability/irritability  2 (40%) 8 (47%) 1.000
Fear03 (18%) 1.000
Distractibility  5 (100%)00.000
Hyperactivity  4 (80%) 1 (6%)  0.003
Psychomotor excitement  2 (40%) 4 (24%) 0.585
Disinhibited behavior  2 (40%) 2 (12%) 0.210
Pressured speech  5 (100%)3 (18%) 0.002
Decreased need for sleep  3 (60%) 00.006
Flight of ideas  2 (40%) 00.043
Loosing of association01 (6%)  1.000
Sudden delusional ideas  2 (40%) 1 (6%)  0.117
Delusional mood03 (18%) 1.000
Delusional perception01 (6%)  1.000
Grandiosity/grandiose delusions  3 (60%) 1 (6%)  0.024
Hyperreligiosity/religious delusions  4 (80%) 4 (24%) 0.039
Persecutory delusions09 (53%) 0.054
Delusions of reference09 (53%) 0.054
Delusions of guilt03 (18%) 1.000
Forced thinking  1 (20%) 1 (6%)  0.411
Thought broadcasting02 (12%) 1.000
Delusions of control02 (12%) 1.000
Monologue  1 (20%) 6 (35%) 1.000
Auditory hyperesthesia02 (12%) 1.000
Dysgeusia02 (12%) 1.000
Déjà vu/jamais vu03 (18%) 1.000
Verbal auditory hallucinations09 (53%) 0.054
Visual hallucinations01 (6%)  1.000
Somatic hallucinations06 (35%) 0.266
Delusional misidentification07 (41%) 0.135
Insomnia010 (59%)  0.040
Amnesia  1 (20%) 5 (29%) 1.000

Seventeen postictal psychotic episodes were observed by neuropsychiatrists of our hospital during the 17 patients' hospitalization. These postictal psychotic episodes fulfilled the ICD-10 criteria for acute and transient psychotic disorders (F23), except for etiology. The cardinal symptoms that developed in the PIP group were various kinds of delusions and hallucinations; especially persecutory delusions (p = 0.054 versus PIM group), delusions of reference (p = 0.054), and verbal auditory hallucinations (p = 0.054), in addition to insomnia (p = 0.040) which showed a tendency of higher prevalence than those in the PIM group as shown in Table 1. Some of the patients in the PIP group showed emotional lability, elated mood, and euphoric mood, but these symptoms never persisted throughout the episodes.

The PIM group consisted of four right-handed men and one right-handed woman, while the PIP group comprised 10 men (nine were right-handed and one was left-handed) and seven women (six were right-handed and one was left-handed). The mean age at examination was 39.0 years (SD, 10.5; range, 24–53) in the PIM group and 30.5 years (SD, 9.1; range, 14–47) in the PIP group. The language dominant hemisphere was confirmed to be the left side by Wada test in 12 patients (patients 5, 7, 9, 11–18, and 21), was presumed to be the left side because the patients were right-handed in nine patients (patients 1–4, 6, 8, 10, 19, and 22), and was undetermined in patient 20 because she was left-handed. The demographic and clinical features of patients were shown in Table 2. Intelligence quotient (IQ) was examined on Wechsler Adult Intelligence Scale-Revised (WAIS-R).

Table 2. Demographic and clinical features
PatientSexHanded-nessLanguage dominant hemisphereAge (yrs)HistoryFamily historyFSIQ (VIQ/PIQ)
ExaminationOnset of epilepsyOnset of mental disorder
  1. a confirmed by Wada test.

  2. M, male; F, female; L, left; R, right; U, undetermined; FC, febrile convulsion; FSIQ, full-scale intelligence quotient; VIQ, verbal intelligent quotient; PIQ, performance intelligence quotient.

Postictal mania group
 1MRL371635Neonatal jaundiceNone 83 (80/89)
 2MRL241523FCCousin: FC104 (111/92)
 3MRL381523NonePaternal relative: bipolar affective disorder 88 (95/81)
 4MRL433535EncephalitisNone 64 (70/65)
 5FRLa531150FC status, brain surgeryNone 75 (81/76)
Mean ± SD 39.0 ± 10.518.4 ± 9.534.2 ± 10.2  82.8 ± 14.9
Postictal psychosis group
 6FRL461946NoneBrother: FC 73 (76/76)
 7FRLa22 422NoneNone 58 (62/67)
 8FRL28 628FC statusNone 41 (48/<45)
 9MRLa341030FC, meningitisNone 72 (65/87)
10FRL281128FC, FC statusNone 66 (68/70)
11MRLa241024Traffic accidentNone 99 (99/100)
12MRLa401740NoneNone 94 (97/91)
13MRLa29429NoneBrother: FC 47 (51/51)
14FRLa322032FCNone 70 (70/76)
15MRLa24 424FC, traffic accidentNone101 (96/110)
16FRLa25 325Convulsive statusNone 54 (55/69)
17MRLa37 637Brain tumor, brain surgeryNone 73 (77/60)
18MRLa211221FCNone 78 (80/81)
19MRL14 514NoneCousin: FC 64 (62/73)
20FLU311821Meningio-encephalitisBrother: FC 66 (64/75)
21MLLa36 236High fever, FCNone100 (107/91)
22MRL47 447NoneCousin: FC 97 (99/94)
Mean ± SD 30.5 ± 9.19.1 ± 6.129.6 ± 9.1  73.7 ± 18.9

The epileptogenic zone was estimated by clinical seizure semiology and laboratory findings including interictal electroencephalography (EEG), ictal EEG, magnetoencephalography (MEG), magnetic resonance imaging (MRI), interictal single-photon emission computed tomography (SPECT), and ictal SPECT.

Laboratory examinations

Interictal and ictal EEG

Routine EEG and long-term EEG/CCTV monitoring were performed with scalp electrodes placed according to the international 10–20 system. Sphenoidal electrodes were used in 12 patients (patients 7, 9, 11–18, 20, and 21) in the PIP group. Routine EEGs were repeatedly performed in all patients of both the PIM and PIP groups, and all recordings lasted more than 1 h, and included sleep recordings (sleep stages 1 and 2). Ictal EEG was obtained in two patients (patients 2 and 5) in the PIM group, and 16 patients (patients 6, 7, and 9–22) in the PIP group. Intracranial long-term EEG/CCTV monitoring was performed in six patients (patients 7, 9, 14, 16, 17, and 21) in the PIP group.

EEG during postictal manic and psychotic episodes

Scalp EEG was performed during the lucid intervals and postictal periods in six postictal manic episodes of four patients (patients 1 and 3–5) in the PIM group, and in 10 postictal psychotic episodes of 10 patients (patients 6, 7, 9–11, 13–15, 18, and 19) in the PIP group. All recordings included those of waking stage, sleep stage 1, and sleep stage 2. The frequency of appearance of interictal epileptiform discharge (IED frequency) and background activity were examined on EEG during the lucid intervals and postictal manic and psychotic episodes. They were compared with the IED frequency and background activity on EEG performed during the interictal mental disorder-free period before a flurry of seizures. First, the IED frequency was scored according to the maximum IED frequency on EEG as follows: (1) no definite IED during an EEG examination, (2) one or more IEDs during an EEG examination, at a frequency of one or less IED per min, (3) two to 10 IEDs per min, and (4) more than 10 IEDs per min. The score obtained using this grading scale was used to assess whether the IED frequency increased, decreased, or remained unchanged. Second, slowing of background activity was also assessed.

MRI

MRI was performed in all patients in both the PIM and PIP groups. The MRI protocol included T1-weighted, T2-wighted and fluid-attenuated inversion recovery (FLAIR) or proton density images.

Interictal and ictal SPECT

Interictal SPECT was performed in all five patients in the PIM group and 16 patients (patients 6–8 and 10–22) in the PIP group. Ictal SPECT was performed in four patients (patients 11, 12, 14, and 15) in the PIP group. The areas of decreased perfusion on interictal SPECT and the areas of increased perfusion on ictal SPECT were analyzed by visual inspection. SPECT images were acquired with SPECT scanner (Headtome-SET070; Shimazu, Kyoto, Japan, or GE Millenium VG HawkEye; GE Yokogawa, Tokyo, Japan). Technetium-99m-ethyl cysteinate dimmer (99mTc-ECD) 740 MBq, iodine-123 N-isopropyl-p-iodo-amphetamine (123I-IMP) 222MBq, or technetium-99m hexamethyl-propylene-amine-oxime (99mTc-HMPAO) 740 MBq was injected into a peripheral vein as tracer in SPECT examinations.

SPECT during postictal manic and psychotic episodes

SPECT was performed during the lucid intervals and postictal periods in five postictal manic episodes of three patients (patients 3–5) in the PIM group, and three postictal psychotic episodes of three patients (patients 11, 14, and 21) in the PIP group. These images were compared with those obtained during the interictal mental disorder-free period, and areas of increased perfusion in the cerebrum were detected. SPECT data were analyzed by subtraction of ictal and interictal SPECT coregistered to MRI (SISCOM) procedure (O'Brien et al. 1998) in three patients (patients 3, 4, and 5) in the PIM group, and analyzed by visual inspection in three patients (patients 11, 14 and 21) in the PIP group. The 99mTc-ECD 740 MBq was used as tracer in SISCOM procedure. The areas with increased perfusion above 2SDs were superimposed and depicted on a T1-wighted MRI template by SISCOM. Visual comparison was done with images obtained using the same tracer for each patient (123I-IMP in patient 11, 99mTc-HMPAO in patient 14, and 99mTc-ECD in patient 21).

Magnetoencephalography (MEG)

MEG was performed in two patients (patients 3 and 4) in the PIM group and 10 patients (patients 7, 12–16, 18–20, and 22) in the PIP group.

MEG during the postictal manic episodes was performed in patient 3 in the PIM group.

Statistics

The Mann–Whitney test and chi-square test or Fisher's exact test were used for statistical analysis of data. The Bonferroni correction was used for multiple comparisons. Statistical analysis was performed by using SPSS software, version 11.5 for Windows.

RESULTS

  1. Top of page
  2. Abstract
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES

Clinical features of postictal mania and postictal psychosis

Postictal mania, postictal psychosis, and epilepsy (Table 3)
Table 3. Clinical features of postictal mania and postictal psychosis
 Postictal mania group (n = 5)Postictal psychosis group (n = 17)U valuep-value
Age at onset of epilepsy (yrs)18.4 ± 9.5  9.1 ± 6.117.50.048
Age at onset of postictal mania or psychosis (yrs)34.2 ± 10.229.6 ± 9.132.00.446
Duration from onset of epilepsy to onset of postictal mania or psychosis (yrs)16.0 ± 14.520.5 ± 9.928.00.283
Number of postictal manic or psychotic episodes7.6 ± 5.2 2.2 ± 4.1 5.50.001
Duration from onset of postictal mania or psychosis to the last visit to our hospital (yrs) 6.0 ± 3.5  6.5 ± 3.839.00.820

The mean age at onset of epilepsy in the PIM group (mean, 18.4 years; SD, 9.5; median, 15; range, 11–35 years) was significantly (p = 0.048) older than that in the PIP group (mean, 9.1 years; SD, 6.1; median, 6; range, 2–20 years). The PIM group had on average 7.6 manic episodes (SD, 5.2; median, 6; range, 3–16 times) and the PIP group had on average 2.2 psychotic episodes (SD, 4.1; median, 1; range, 1–18 times), with significantly (p = 0.001) more episodes in the PIM group.

Postictal manic and psychotic episodes (Table 4)
Table 4. Clinical features of postictal manic and psychotic episodes
 Postictal mania group (n = 10)Postictal psychosis group (n = 17)U valuep-value
  1. aFisher's exact test.

  2. CPS, complex partial seizure; SGTC, secondarily generalized tonic–clonic seizure.

Preceding seizures
CPS  4 (40%) 4 (24%)a0.415
SGTC, SGTC+CPS  6 (60%)13 (76%)a0.415
Duration of lucid interval (days)2.0 ± 0.71.9 ± 2.153.50.115
Duration of postictal manic or psychotic episode (days)16.1 ± 12.26.0 ± 5.828.50.003
Treatment by neuroleptics10 (100%)14 (82%)a0.274

Both PIM and PIP groups had complex partial seizures and/or secondarily generalized seizures preceding the postictal manic or psychotic episodes. All postictal manic and psychotic episodes had a lucid interval before developing psychiatric symptoms, for a mean duration of 2.0 days (SD, 0.7; median, 2; range, 1–3 days) in the PIM group and 1.9 days (SD, 2.1; median, 1; range, 0.5–9 days) in the PIP group. The mean duration of the postictal manic episodes (mean, 16.1 days; SD, 12.2; median, 13.5; range, 4–40 days) was significantly (p = 0.003) longer than that of the postictal psychotic episode (mean, 6.0 days; SD, 5.8; median, 5; range, 1–23 days). Five patients (100%) in the PIM group took neuroleptics during all 10 postictal manic episodes and 14 patients (82%) in the PIP group took neuroleptics during postictal psychotic episodes.

Epileptogenic zone and epileptic syndrome

Table 5 shows the details of seizure semiology, findings of laboratory examinations (EEG, MEG, MRI and SPECT), and the estimated epileptogenic zone in both the PIM and PIP groups. In the PIM group, the epileptogenic zone was estimated to be in the left frontal lobe in three patients, and in the left temporal lobe in two patients. In the PIP group, the epileptogenic zone was estimated to be in the left temporal lobe in nine patients (left mesial temporal lobe in five), and in the right temporal lobe in six patients (right mesial temporal lobe in one). In the remaining two patients in the PIP group, the epileptogenic zone was estimated to be in the right hemisphere, but the localization could not be decided, because the patients had seizures after surgery.

Table 5. Seizure semiology, laboratory examinations, and epileptogenic zone
PatientSeizure semiologyEEGMEGMRISPECTEstimated epileptogenic zone
Interictal dischargesIctal dischargesInterictal hypoperfusionIctal hyperperfusion
  1. a determined by intracranial recording.

  2. SGTC, secondarily generalized tonic-clonic convulsion; L, left; R, right; Bi, bilateral; HS, hippocampal sclerosis; None, not done.

Postictal mania group
1Reminiscence, impaired consciousness, SGTCL temporal areaNoneNoneNormalL temporal lobeNoneL temporal lobe
2Tonic contraction of upper limb, impaired consciousness, SGTCBi frontal and Bi temporal areasL frontal and temporal areasNoneNormalL frontal and L temporal lobesNoneL frontal lobe
3SGTCBi frontal areasNoneL frontal lobeL frontal and L temporal lobes atrophyL frontal and L temporal lobesNoneL frontal lobe
4Postural, impaired consciousness, SGTCBi frontal and Bi temporal areasNoneL frontal lobeBi HS and Bi frontal and temporal lobes atrophyL frontal and Bi temporal lobesNoneL frontal lobe
5Impaired consciousness, SGTCL temporal areaL temporal areaNoneL anterior and mesial temporal lobe resectionL temporal lobeNoneL temporal lobe
 Postictal psychosis group
6Impaired consciousness, SGTCBi temporal areasFocus unknownNoneL anterior temporal lobe polymicrogyriaL temporal lobeNoneL temporal lobe
7Jamais vu, impaired consciousness, SGTCR temporal areaR temporal lobeaR temporal lobeR temporal and R parietal lobes atrophyR temporal and R parietal lobesNoneR temporal lobe
8Epigastric, impaired consciousness, SGTCBi temporal areasNoneNoneL HSL temporal lobeNoneL mesial temporal lobe
9Auditory, impaired consciousness, SGTCL temporal and L frontal areasL temporal lobeaNoneL HSNoneNoneL temporal lobe
10Epigastric, impaired consciousness, SGTCBi temporal areasL sideNoneL HSL temporal lobeNoneL mesial temporal lobe
11Discomfort, impaired consciousness, SGTCL temporal areaL temporal areaNoneL HSL temporal lobeL temporal lobeL mesial temporal lobe
12Impaired consciousness, SGTCR temporal areaR temporal areaR temporal lobeNormalR temporal lobeR temporal lobeR temporal lobe
13Auditory, impaired consciousness, SGTCR temporal areaR temporal areaR temporal lobeBi HSBi temporal lobesNoneR temporal lobe
14Cephalic, impaired consciousness, SGTCBi temporal areasR temporal lobeaL temporal lobeR HSNormalBi temporal lobesR temporal lobe
15Impaired consciousness, SGTCR temporal areaR temporal areaR temporal lobeR HSR temporal lobeR temporal lobeR mesial temporal lobe
16Epigastric, impaired consciousness, SGTCBi temporal areasL mesial temporal lobeaBi temporal lobesL HSL temporal lobeNoneL mesial temporal lobe
17Impaired consciousness, SGTCR temporal areaR temporoparietal lobeaNoneR temporoparietooccipital lobes resectionR temporoparietooccipital lobesNoneR focus unkown
18Epigastric, impaired consciousness, SGTCL temporal areaL temporal areaL temporal lobeLHSL temporal lobeNoneL mesial temporal lobe
19Auditory, impaired consciousness, SGTCBi temporal areasL sideBi frontal lobesNormalNormalNoneL temporal lobe
20Cephalic, impaired consciousness, SGTCBi temporal areasR temporal areaR temporal lobeBi HSBi temporal and Bi frontal lobesNoneR temporal lobe
21Pilo-erection, impaired consciousness, SGTCR temporal areaR temporal lobeaNoneR HSR temporal lobeNoneR focus unkown
22Vertiginous, impaired consciousness, SGTCL temporal areaL temporal areaL temporal lobeL HSL temporal lobeNoneL temporal lobe

Table 6 shows the epileptic syndromes and hemispheric laterality of the estimated epileptogenic zone concerning language dominancy. The PIM group had frontal lobe epilepsy and temporal lobe epilepsy. The PIM group had a significantly (p = 0.006) higher prevalence of frontal lobe epilepsy than the PIP group. The PIP group tended to have higher prevalence of temporal lobe epilepsy, including mesial temporal lobe epilepsy, than the PIM group, but the differences were not significant. In the PIM group, estimated epileptogenic zone was on the language dominant side in all patients. In the PIP group, the estimated epileptogenic zone was on the language dominant side in nine patients, on the language nondominant side in seven patients, while the language dominant side was undetermined in the remaining patient with the estimated epileptogenic zone in the right temporal lobe.

Table 6. Epileptic syndromes and hemispheric laterality of the epileptogenic zone
 Postictal mania group (n = 5)Postictal psychosis group (n = 17)p-Value
  1. aThe language dominant side was undetermined in one patients with epileptogenic zone on the right temporal lobe.

  2. D, language dominant side; ND, language nondominant side.

Frontal lobe epilepsy (D/ND)3 (3/0)00.006
Temporal lobe epilepsy (D/ND)2 (2/0)15 (9/5)a0.055
Mesial temporal lobe epilepsy (D/ND)06 (5/1)0.266
Other localization-related epilepsy (D/ND)02 (0/2)1.000

Brain functional changes during postictal manic and psychotic episodes

Interictal epileptiform discharge (IED) frequency and background activity on EEG

During the lucid intervals, the IED frequency on EEG was unchanged in patients 1 and 3, and the IED frequency increased and slow waves also increased in patient 4 in the PIM group (Table 7). In the PIP group, the IED frequency was unchanged in patients 11 and 15, and the IED frequency was unchanged while slow waves increased in patients 7, 13, 18, and 19.

Table 7. Brain functional changes during postictal manic and psychotic episodes
 Lucid intervalPostictal manic or psychotic episode
  1. IED, interictal epileptiform discharge; D, language dominant; ND, language nondominant; Bi, bilateral; None, not done.

IED frequency and background activity on EEG
Positical mania group
 Patient 1No changeDecrease (3rd day)
 Patient 3NoneDecrease (1st, 2nd day), Increase + slow (3rd–5th, 8th, 12th day)
No changeDecrease (1st, 2nd day), Increase + slow (3rd–13th day)
 Patient 4NoneDecrease (5th–7th day)
Increase + slowDecrease (3rd, 14th, 22nd, 29th, 35th day)
 Patient 5NoneNo change + slow (8th day)
Postictal psychosis group
 Patient 6NoneNo change (10th day)
 Patient 7No change + slowNone
 Patient 9NoneNo change + slow (6th day)
 Patient 10NoneNo change (1st day)
 Patient 11No changeNone
 Patient 13No change + slowDecrease (1st day), No change + slow (2nd day)
 Patient 14NoneDecrease (3rd day)
 Patient 15No changeNone
 Patient 18No change + slowNone
 Patient 19No change + slowDecrease (1st day)
Increased perfusion on SPECT
Positical mania group
 Patient 3NoneND frontal lobe (1st day), ND frontal lobe (5th day)
Bi frontal lobesND frontal and ND temporal lobes (6th day)
 Patient 4D frontal and ND temporal lobes and Bi basal gangliaND temporal lobe and ND basal ganglia (20th day)
 Patient 5NoneD frontal and Bi occipital lobes (7th day)
NoneBi frontal lobes (3rd day)
Postictal psychosis group
 Patient 11NoneD temporal lobe (1st day)
 Patient 14NoneND frontal and ND temporal lobes (7th day)
 Patient 21NoneND hemishphere (1st day)
Equivalent current dipoles on MEG
Positical mania group
 Patient 3NoneBi frontal lobes (8th day)

During the postictal manic episodes, in the PIM group, the IED frequency decreased in patient 1 (on the 3rd day of postictal manic episode), in two episodes of patient 3 (on the 1st and 2nd day), in one episode of patient 4 (from the 5th to 7th day), and in another episode of patient 4 (on the 3rd, 14th, 22nd, 29th, and 35th day). The IED frequency increased and slow waves also increased in one episode of patient 3 (from the 3rd to 5th, 8th, and 12th day), and in another episode of patient 3 (from the 3rd to 13th day). The IED frequency was unchanged while slow waves increased in patient 5 (on the 8th day).

During the postictal psychotic episodes, in the PIP group, the IED frequency decreased in patient 13 (on the 1st day of postictal psychotic episode), in patient 14 (on the 3rd day), and in patient 19 (on the 1st day). The IED frequency was unchanged in patient 6 (on the 10th day), and in patient 10 (on the 1st day). The IED frequency was unchanged while slow waves increased in patient 9 (on the 6th day), and in patient 13 (on the 2nd day).

Increased perfusion on SPECT

In the PIM group, as shown in Table 7, SPECT during the lucid intervals showed increased perfusion in bilateral frontal lobes (medial prefrontal area, orbitofrontal cortex, and anterior cingulate cortex) in patient 3, and increased perfusion in the language dominant frontal lobe (prefrontal area and anterior cingulate cortex) and language nondominant temporal lobe (medial temporal lobe) and bilateral basal ganglia in patient 4 (Fig. 1A).

image

Figure 1. SPECT findings in patient 4. Colored areas show significant increased perfusion (above 2SDs) compared with the image obtained during mental disorder-free period on SISCOM procedure. (A) Increased perfusion is observed in the left prefrontal, anterior cingulate cortex, and the right medial temporal lobe during the lucid interval. (B) Increased perfusion is observed in the right medial temporal lobe and basal ganglia during the postictal manic episode.

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In the PIM group, SPECT during the postictal manic episodes showed increased perfusion in the language nondominant frontal lobe (medial prefrontal area, frontal pole, anterior cingulate cortex, and superior frontal gyrus) in one episode of patient 3 (on the 1st day of postictal manic episode), and increased perfusion in the language nondominant frontal lobe (lateral prefrontal area and frontal operculum) in the same episode of patient 3 (on the 5th day), and increased perfusion in the language nondominant frontal lobe (frontal operculum) and temporal lobe (superior temporal gyrus) in another episode of patient 3 (on the 6th day). SPECT showed increased perfusion in the language nondominant temporal lobe (medial temporal lobe) and language nondominant basal ganglia in patient 4 (on the 20th day) (Fig. 1B). SPECT showed increased perfusion in the language dominant frontal lobe (medial prefrontal area and orbitofrontal lobe) and bilateral occipital lobes in one episode of patient 5 (on the 7th day), and increased perfusion in bilateral frontal lobes (medial prefrontal area and anterior cingulate cortex) in another episode of patient 5 (on the 3rd day) (Fig. 2).

image

Figure 2. SPECT findings in patient 5. Colored areas show significant increased perfusion (above 2SDs) compared with the image obtained during mental disorder-free period on SISCOM procedure. Increased perfusion is observed in bilateral medial prefrontal lobes and anterior cingulate cortex during the postictal manic episode.

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In the PIP group, SPECT during the postictal psychotic episodes showed increased perfusion in the language dominant temporal lobe in patient 11 (on the 1st day of postictal psychotic episode), increased perfusion in the language nondominant frontal and temporal lobes in patient 14 (on the 7th day), and increased perfusion in the language nondominant hemisphere in patient 21 (on the 1st day).

The areas of increased perfusion during the postictal manic episodes were bilateral or contralateral to the estimated epileptogenic zone in the PIM group, and they were ipsilateral to the estimated epileptogenic zone in the PIP group.

Equivalent current dipoles on MEG

As shown in Table 7, MEG during the postictal manic episode showed a diffuse distribution of equivalent current dipoles in bilateral frontal lobes in patient 3 (on the 8th day of postictal manic episode), while it showed a localization of equivalent current dipoles in the left frontal lobe during the interictal mental disorder-free period.

DISCUSSION

  1. Top of page
  2. Abstract
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES

Clinical features of postictal mania and postictal psychosis

The cardinal symptoms of the PIM group were abnormally elated mood, expansive mood, euphoric mood, and distractibility throughout postictal manic episodes. In addition, patients with PIM tended to show hyperactivity, pressured speech, decreased need for sleep, flight of ideas, grandiosity, and hyperreligiosity. The grandiosity and hyperreligiosity were congruent with their mood throughout the episodes. These symptoms fulfilled the ICD-10 criteria for manic episode (F30), except for etiology, and this mental disorder can be diagnosed as organic mood (affective) disorders (F06.3). On the other hand, patients with PIP tended to show various kinds of delusions and hallucinations; especially persecutory delusions, delusions of reference, verbal auditory hallucinations, and insomnia. As Kanemoto et al. (1996) showed that elated mood was one of the striking features of PIP, some of our patients with PIP also manifested emotional lability, euphoric, and elated mood. However, these symptoms appeared only transiently and never persisted throughout the episode, and the delusions and hallucinations in PIP were not congruent with their mood. These symptoms fulfilled the ICD-10 criteria for acute and transient psychotic disorders (F23), except etiology, and this mental disorder can be diagnosed as organic delusional (schizophrenia-like) disorder (F06.2). These observations verify that patients with PIM can be distinguished from patients with PIP by the clinical symptoms observed in the postictal period based on the ICD-10 criteria.

The patients with PIM experienced significantly more postictal episodes than patients with PIP. All five patients with PIM had relapsing episodes. There may be a difference in propensity toward recurrence of postictal episodes between PIM and PIP although the mechanisms remain unknown.

As our results showed, the age at onset of epilepsy in the PIM group was significantly older than that in the PIP group, although it was not so different from previously reported studies (Logsdail and Toone, 1988; Kanemoto et al., 1996). Further large-scale study is needed to verify this finding, because this may be due to differences in etiology of epilepsy between PIM and PIP.

Patients in both the PIM and PIP groups followed a typical course of postictal manic or psychotic episodes. The preceding seizures were single or a flurry of complex partial seizures and/or secondarily generalized seizures. All patients had a lucid interval, which is the latency between the end of seizures and the beginning of manic or psychotic episodes. This interval has been emphasized to be one of the unique characteristics of PIP (Sengoku et al., 1985). There was no significant difference in duration of the lucid interval between PIM and PIP.

Previous studies showed that the duration of postictal manic or psychotic episodes varies (Logsdail and Toone, 1988; Savard et al., 1991). Our study revealed that the duration of postictal manic episodes in patients with PIM was significantly longer than that of postictal psychotic episodes in patients with PIP. This difference in the duration may also reflect the difference in intrinsic mechanism between PIM and PIP.

All patients (100%) in the PIM group had neuroleptics during 10 postictal manic episodes, and 14 patients (82%) in the PIP group had neuroleptics during postictal psychotic episodes. We could differentiate PIM from PIP clinically under the treatment by neuroleptics throughout the postictal episodes. Treatment by neuroleptics probably had no effect on our conclusions that postictal manic episodes lasted longer than postictal psychotic episodes, because all patients in the PIM group were treated by neuroleptics sufficiently. It was unlikely that we included the patients, who showed initial hypomanic symptoms and whose psychotic symptoms were aborted prematurely by medical intervention, into the postictal mania group, because postictal manic episode lasted longer than postictal psychotic episode and, furthermore, patients in the PIM group never showed psychotic symptoms during the postictal periods.

Epileptogenic zone and epileptic syndrome

The estimated epileptogenic zones or foci on EEG of patients with PIM or postictal hypomania or seizure-related psychopathology equivalent to mania are in the temporal lobe (Wolf, 1982a; Hurwitz et al., 1985; Barczak et al., 1988; Byrne, 1988; Savard et al., 1991; Kudo et al., 2001); frontal lobe (Nishida et al., 2005), or multiple lobes (Kudo et al., 2001). PIM was also reported in idiopathic generalized epilepsy (Logsdail and Toone, 1988; Chakrabarti et al., 1999). On the other hand, PIP was observed predominantly in patients with temporal lobe epilepsy (Kanemoto, 2002). Our study showed that PIM developed in patients with epileptogenic zones estimated in the frontal lobe and temporal lobe. The frontal lobe has integrative and inhibitory faculties of mental activity, and the temporal lobe and limbic area have a faculty associated with emotion (Mesulam, 2000). This supports our results that PIM is related to these cerebral structures.

As regards the relation of psychopathology with hemispheric laterality of the epileptogenic zone, Flor-Henry (1969) and Hurwitz et al. (1985) suggested that manic or hypomanic state was related to the epileptogenic zone on the language nondominant hemisphere. Furthermore, manic states of neurological disorders other than epilepsy were also reported to be associated with the pathology in the right-sided hemisphere (Starkstein et al., 1990; Mendez, 2000). However, some studies reported that patients who had an estimated epileptogenic zone on the left side manifested PIM (Wolf, 1982a; Kudo et al., 2001; Nishida et al., 2005). All our patients with PIM had the estimated epileptogenic zone on the language dominant side. However, SPECT performed during postictal manic episodes showed increased perfusion on the language nondominant side in three episodes of two patients, and bilateral increase in one patient. This suggests that when the epileptogenic zone is on the language dominant side, the functional changes on the language nondominant side or both sides are crucial to develop PIM. On the other hand, there was no specific hemispheric laterality of the estimated epileptogenic zone in patients with PIP in our study.

Brain functional changes during postictal manic and psychotic episodes

Logsdail and Toone (1988) reported increases of right-sided or bilateral spikes and sharp waves, as well as slow waves on EEG during postictal psychotic episodes. In our study, the IED frequency during the lucid interval was unchanged compared to the frequency during the interictal mental disorder-free period, with or without increase of slow waves in background activity in most the patients in both the PIM and PIP groups. In contrast, the IED frequency decreased during the early period of the postictal episode in most the patients in both groups, whereas the IED frequency changed variedly during the latter period of the postictal episode in both groups. The clinicoelectrical findings observed during the early period of postictal manic and psychotic episodes are equivalent to “forced normalization,” a phenomenon in which epileptiform discharges in patients with epilepsy normalize during psychosis (Landolt, 1958). We previously proposed that this phenomenon probably resulted from intrinsic mechanism, not merely from arousal level, in a patient with PIM (Nishida et al., 2005). Takeda et al. (2001) showed that epileptiform discharges increased in the left amygdala during intracranial recording in a patient with acute psychotic state in the postictal period. It is possible that increased perfusion, observed on SPECT during the lucid interval and postictal manic and psychotic episodes, reflects subcortical discharges that do not appear in scalp electrodes and is responsible for the psychopathology observed in the postictal period (Wolf, 1982b; Wieser et al., 1985), although there remains a possibility that the increased perfusion on SPECT reflects nonepileptic activity of the endogenous systems in the brain (Stevens, 1998).

In our study, SPECT showed increased perfusion in the language nondominant frontal and/or temporal lobes in three postictal manic episodes of two patients, and in bilateral frontal or occipital lobes in two postictal manic episodes of one patient. On the other hand, SPECT of three postictal psychotic episodes showed increased perfusion in the language dominant temporal lobe, in the language nondominant frontal and temporal lobes, and in the language nondominant hemisphere in one case each. In some reports of manic patients with bipolar mood disorder, SPECT depicted increased perfusion in the temporal lobe and basal ganglia and decreased perfusion in the prefrontal area (O'Connell et al., 1995), and increased perfusion in the right anterior temporal lobe (Gyulai et al., 1997). Thomas et al. (1999) reported increased perfusion in the right frontopolar area during nonconvulsive status epilepticus with hypomanic state in two patients. These findings suggest that manic state is related to functional changes of the frontal and temporal lobes. As regards PIP, SPECT showed increased perfusion in the mesial frontal lobe (Baumgartner et al., 1995), lateral temporal lobes (Fong et al., 2000; Fong et al., 2002), or bilateral temporal and mesial frontal lobes (Leutmezer et al., 2003). No studies, however, have analyzed the relationship between the finding of SPECT, hemispheric laterality of the epileptogenic zone and psychopathology. In our study, all patients with PIM had the estimated epileptogenic zone on the language dominant side, and increased perfusion during postictal manic episode was bilateral or contralateral to the epileptogenic zone. On the other hand, patients with PIP had the epileptogenic zone either on the language dominant side or the nondominant side, and increased perfusion during postictal psychotic episode was ipsilateral to the epileptogenic zone, irrespective of whether the epileptogenic zone was on the language dominant or nondominant side. When the epileptogenic zone is on the language dominant side, involvement of bilateral or the contralateral frontal and temporal lobes may be a crucial feature in the development of postictal manic episode. Visual inspection of ictal SPECT and SISCOM procedure are confirmed to be helpful to detect the epileptogenic zone (Marks et al., 1992; Ho et al., 1995; O'Brien et al., 1998), and they may be useful to reveal the biological process of postictal mania and postictal psychosis. Our SPECT study was analyzed by SISCOM in patients with PIM and by visual inspection in patients with PIP, therefore the two groups cannot be compared directly. Furthermore, neuroleptics that were used during postictal episodes might have some effect on the findings of SPECT and EEG. More studies are needed to confirm the relationship of the hemispheric laterality of epileptogenic zone and functional changes of the brain with psychopathology observed in the postictal period.

Finally, it is necessary to state the limitations of this study. The total number of patients is small for further analyses with various clinical factors, because of rarity of patients with PIM and PIP. Moreover, this study is retrospective, and lacks uniformity in the examination procedure and medical intervention. However, our results may have significance in elucidating new findings that differentiate PIM and PIP, and contribute to large-scale and prospective studies to reveal definite characteristics of PIM and PIP in the future.

REFERENCES

  1. Top of page
  2. Abstract
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES
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