Risk Factors for Psychosis Secondary to Temporal Lobe Epilepsy: A Systematic Review
Abstract
Methods
Results
Quality Index Score | Author, Year, Country | Participants | Control Group/ Additional Experimental Group | Study Design | Method of Data Collection | Assessment of Psychosis | Factors Investigated | Statistical Analyses and Results |
---|---|---|---|---|---|---|---|---|
12 | Adachi et al., 2002,25 Japan | 197 individuals with LRE (123 with TLE) and IIP | 456 individuals with LRE (288 with TLE) and NP | Case–control | Medical file review | Neuropsychiatric assessment using ICD–10 criteria | Age at epilepsy onset. | ANCOVA: |
F=8.19; p=0.004* | ||||||||
12 | D’Alessio et al., 2009,17 Argentina | 63 individuals with TLE-P | 60 individuals with TLE-NP | Case–control | Medical file review | Psychiatric assessment using SCID-I and -II | t-tests: | |
Gender; | p=0.039* | |||||||
Employment; | p=0.001* | |||||||
Unilateral HS; | NS | |||||||
Bilateral HS; | p=0.001* | |||||||
History of SE; | p=0.017* | |||||||
Duration of epilepsy >20 yrs; | p=0.02* | |||||||
Aura; | p=0.054 | |||||||
Age at epilepsy onset | NS | |||||||
12 | Falip et al., 2009,10 Spain | 5 individuals with TLE-PIP | 50 individuals with TLE-NP | Case–control | Review of medical file | Psychiatric assessment | t-tests: | |
Gender; | NS | |||||||
History of febrile seizures; | NS | |||||||
History of SE; | p=0.019* | |||||||
Seizure frequency; | NS | |||||||
Duration of epilepsy; | NS | |||||||
Age at epilepsy onset; | NS | |||||||
Family history of epilepsy; | NS | |||||||
Dialeptic or automotor seizures evolving to secondary generalization; | p=0.025* | |||||||
Lesion side; | χ2 tests: | |||||||
Etiology; | NS | |||||||
Nonlateral ictal EEG | NS | |||||||
p=0.001* | ||||||||
12 | Kalinin et al., 2010,24 Russian Federation | 105 individuals with TLE | N/A | Case–control | Clinical and neuropsychological assessments and MRI | Psychiatric assessment using ICD–10 criteria | t-tests: | |
Handedness; | Paranoia: p NS | |||||||
Psychoticism: NS | ||||||||
Laterality focus; | Paranoia: NS | |||||||
Psychoticism: NS | ||||||||
Alexithymia | Paranoia: p=0.002* Psychoticism: p=0.006* | |||||||
12 | Kanemoto et al., 2001,28 Japan | 132 individuals with epilepsy and IIP | 2,773 individuals with epilepsy and NP | Case–control | Medical file review | Psychiatric assessment using DSM-IV criteria | χ2 tests: | |
Age at epilepsy onset (<10 years); | χ2=4.87; p <0.05* | |||||||
Prolonged febrile seizures | χ2=13.73; p <0.01* | |||||||
11 | Briellmann et al., 2000,39 Australia | 6 individuals with TLE-PIP | 45 individuals with TLE-NP | Case–control | Collection of temporal lobe tissues | Psychiatric assessment using DSM-IV criteria | Volume loss of the anterior hippocampus; | Mann-Whitney U test: p=0.003*; |
Mesial dysplasia | Chi square: p=0.006* | |||||||
11 | Cunha et al., 2003,37 Portugal | 18 medically-treated individuals with TLE; | N/A | Case–control | Clinical and neuropsychological assessment | Assessment of psychotic symptoms, using SCL–90 (self-administered) | Duration and severity of epilepsy | t-tests: |
19 surgically-treated individuals with TLE (examined pre- and postsurgery) | Paranoid Ideation: NS | |||||||
Psychoticism: NS | ||||||||
11 | Kanemoto et al., 1996,27 Japan | 61 individuals with TLE and UHS (31 with PIP); | N/A | Case–control | Medical file review and MRI | Psychiatric assessment, using DSM-IV criteria | χ2 tests: | |
50 individuals with TLE with normal MRI (11 with PIP) | UHS; | χ2=9.7; p <0.01* | ||||||
Age at epilepsy onset (<10 years); | χ2=5.53; p <0.05* | |||||||
UHS, PIP, and atrophy of temporal neocortex | χ2=6.14; p <0.05* | |||||||
11 | Radhakrishnan et al., 2007,43 India | 129 individuals with surgically-treated TLE with CoA build-up; | N/A | Cross-sectional | Psychological and psychiatric assessment; EEG and MRI; collection of temporal lobe tissues | Psychiatric assessment, using ICD–10 criteria | t-tests: | |
244 individuals with surgically-treated TLE without CoA build-up | Frequency of IIP in CoA+ and CoA− groups; | p ≤0.001* | ||||||
Frequency of IIP in Grades 1, 2, or 3 CoA | p=0.006* | |||||||
11 | Suckling et al., 2000,41 U.K. | 6 individuals with TLE-P | 26 individuals with TLE -NP | Case–control | Medical file review and collection of temporal lobe tissues | Neuropsychiatric assessment | Fisher’s exact test: | |
Presence of focal lesions; | p=0.006* | |||||||
Neuron loss in CA1; | p=0.015* | |||||||
Neuron loss in CA4; | NS | |||||||
Neuron loss in dentate gyrus; | NS | |||||||
Dispersion of dentate granule cells | NS | |||||||
10 | De Araújo Filho et al., 2011,35 Brazil | 29 individuals with TLE | 6 individuals with JME | Cross-sectional | Medical file review | Psychiatric assessment, using DSM-IV criteria | Frequencies: 68.9% (20) | |
16 with IIP | 4 with IIP | Left-sided MTS; | ||||||
13 with PIP | 2 with PIP | Right-sided MTS; | 20.6% (6) | |||||
Bilateral MTS | 10.3% (3) | |||||||
10 | De Oliveira et al., 2010,13 Brazil | 73 individuals with TLE | N/A | Cross-sectional | Clinical questionnaires | Mini-International Neuropsychiatric Interview (MINI) Plus, Version 5.0.0 | Bilateral MTS | Fisher’s exact test: NS |
10 | Flügel et al., 2006,26 U.K. | 20 individuals with TLE-IIP | 20 individuals with TLE-NP | Case–control | Neuropsychological assessments; MRI | Neuropsychiatric assessment, using DSM-IV criteria; PANSS | General linear model (multivariate): | |
Age at onset of epilepsy; | F=10.3; p=0.003* | |||||||
History of SE; | F=16.1, p=0.00* | |||||||
Estimate of premorbid IQ; | F=1.4; NS | |||||||
Current IQ; | F=3.16; NS | |||||||
Vocabulary; | F=4.4; p=0.04* | |||||||
Verbal Fluency (animals); | F=8.29; p=0.007* | |||||||
Verbal Fluency (letters); | F=1.81; NS | |||||||
Arithmetic; | F=5.09; p=0.03* | |||||||
Digit Span; | F=3.02; NS | |||||||
Spatial Span; | F=4.90; p=0.03* F=4.88; p=0.03* | |||||||
Spatial Working Memory; | ||||||||
Hippocampal volume | NS | |||||||
10 | Gutierrez-Galve et al., 2012,20 U.K. | 22 individuals with TLE-IIP | 23 individuals with TLE-NP; | Case–control | Medical file review and MRI | Neuropsychiatric assessment and PANSS | χ2 test: | |
21 healthy individuals | Gender; | χ2=0.58; NS | ||||||
Handedness; | Fisher’s exact tests: | |||||||
History of SE; | Fisher’s exact=0.345 | |||||||
Total brain volume; | Fisher’s exact=0.004* | |||||||
Age at epilepsy onset; | ANOVAs: | |||||||
Duration of epilepsy; | F=7.92; p <0.001* | |||||||
Estimates of Premorbid IQ; | t-tests: | |||||||
Current IQ; | t = –2.62; p=0.012* | |||||||
Working Memory Span; | t=1.61; NS | |||||||
Working Memory Manipulation; | t = –1.06; NS | |||||||
Frontal cortical thickness; | t = –2.44, p=0.019* | |||||||
Cortical area; | t = –2.83; p=0.007* | |||||||
Cortical volume | t=2.84; p=0.007* | |||||||
ANOVAs: | ||||||||
F=3.79; p=0.050* | ||||||||
NS | ||||||||
NS | ||||||||
10 | Kandratavicius et al., 2012,21 Brazil | 14 individuals with TLE-IIP | 16 individuals with TLE and no comorbidity; | Case–control | Collection of temporal lobe tissues | Psychiatric assessment, using DSM-IV criteria | ANOVAs: | |
16 individuals with TLE and major depression; | Gender; | NS | ||||||
10 normal autopsy samples | Presence of IPI; | NS | ||||||
Age at epilepsy onset; | F=3.099; p=0.049* | |||||||
Duration of epilepsy; | NS | |||||||
Seizure frequency; | NS | |||||||
Handedness; | NS | |||||||
HS; | NS | |||||||
Current IQ; | NS | |||||||
Education (years); | NS | |||||||
Seizure type; | Fisher’s exact tests: | |||||||
Memory in Verbal Tasks; | p=0.02* | |||||||
Neuronal density in entorhinal cortex; | p=0.003* | |||||||
Fascia dentata inner molecular layer mossy fiber sprouting | ANOVAs: | |||||||
F=3.175, p=0.047* | ||||||||
TLE-IIP and TLE: | ||||||||
F=4.931; Tukey’s post hoc: p=0.014* | ||||||||
10 | Rüsch et al., 2004,38 U.K. | 26 individuals with TLE-P | 24 individuals with TLE-NP; | Case–control | Medical file review and MRI | Neuropsychiatric assessment, using ICD–10 criteria | t-tests: | |
20 healthy individuals | Performance IQ; | t=0.203; NS | ||||||
Verbal IQ; | t=2.307; p=0.02* | |||||||
Current IQ; | t=1.902; p=0.06 | |||||||
Cortical gray-matter volumes; | NS | |||||||
Laterality of HS | NS | |||||||
10 | Sundram et al., 2010,30 Ireland | 10 individuals with TLE-P | 10 individuals with TLE-NP | Case–control | Medical file review and MRI | Neuropsychiatric assessment, which was objectively assessed using the OPCRIT | t-tests: | |
Age at epilepsy onset; | NS | |||||||
Duration of epilepsy; | NS | |||||||
Total brain volume; | Mann-Whitney U tests: | |||||||
Total gray-matter volume; | p=0.07 | |||||||
Total white-matter volume; | p=0.08 | |||||||
Gray-matter regional deficits; | NS | |||||||
White-matter regional deficits | ANCOVAs: | |||||||
Cluster significance threshold: p=0.002*; | ||||||||
Cluster significance threshold: p=0.006* | ||||||||
10 | Tebartz van Elst et al., 2002,34 U.K. | 26 individuals with TLE-P | 24 individuals with TLE-NP; | Case–control | Medical file review and MRI | Neuropsychiatric assessment, using ICD–10 criteria | ANOVAs: | |
20 healthy individuals | Laterality of HS; | NS | ||||||
EEG abnormalities; | NS | |||||||
Total brain volumes; | F=11.750; p <0.001* | |||||||
Hippocampal volumes; | NS | |||||||
Right amygdala volumes; | F=8.211; p=0.001* | |||||||
Left amygdala volumes. | F=9.079; p<0.001* | |||||||
10 | Umbricht et al., 1995,23 U.S.A. | 8 individuals with TLE-PIP; | 29 individuals with TLE-NP | Case–control | Medical file review | Psychiatric assessment, using DSM-III-R criteria | ANOVAs: | |
7 individuals with TLE-IIP | Duration of epilepsy; | NS | ||||||
Bilateral focus; | Fisher’s exact test: p <0.005* | |||||||
Seizure clusters; | χ2 tests: χ2=3.75; p=0.05* | |||||||
Febrile convulsions; | χ2=4.36; p <0.05* | |||||||
Handedness; | p>0.05 | |||||||
Age at epilepsy onset; | t-tests: | |||||||
Time between first seizure and onset of epilepsy; | t=2.67; p <0.05* | |||||||
Full-scale IQ; | t=2.81; p <0.01* | |||||||
Verbal IQ. | Mann-Whitney U tests: | |||||||
z=1.98; p <0.05* | ||||||||
z=2.11; p <0.05* | ||||||||
9 | De Araújo Filho et al., 2008,33 Brazil | 170 individuals with TLE | 100 individuals with JME | Cross-sectional | Medical file review and EEG monitoring | Psychiatric assessment, using SCID-I | Left-sided MTS | χ2 test: p <0.05* |
9 | Flügel et al., 2006,18 U.K. | 20 individuals with TLE-IIP | 20 individuals with TLE-NP; | Case–control | Clinical assessments; MRI | Psychiatric assessment, using DSM-IV criteria; PANSS | Mann-Whitney U tests: | |
23 healthy individuals | Gender; | Z = –0.64; NS | ||||||
Estimated Premorbid IQ; | Z = –0.92; NS | |||||||
Age at epilepsy onset; | Z = –2.91; p=0.004* | |||||||
Min. and max. seizure frequency; | Z = –0.56; NS | |||||||
MTR in the left middle and superior temporal gyri | p ≤0.005* | |||||||
9 | Flügel et al., 2006,48 U.K. | 20 individuals with TLE-IIP | 20 individuals with TLE-NP | Case–control | Neuropsychological assessments and MRI | Neuropsychiatric assessment; PANSS | General linear model (multivariate): | |
FA values in frontal left; | F=5.54; p=0.024* | |||||||
FA values in frontal right; | F=12.18; p=0.001* | |||||||
FA values in temporal left; | F=5.89; p=0.02* | |||||||
FA values in temporal right; | F=6.295; p=0.017* | |||||||
MD values in frontal left; | F=5.203; p=0.029* | |||||||
MD values in frontal right | F=5.88; p=0.02* | |||||||
9 | Fukao et al., 2009,36 Japan | 16 individuals with TLE-P | 41 individuals with TLE-NP | Case–control | Medical file review and magnetoencephalographic measurements | Psychiatric assessment, using DSM-IV criteria | Correlation: | |
Laterality of focus; | NS | |||||||
IH-type spike-dipoles; | NS | |||||||
Left SV-type spike-dipoles; | p=0.002* | |||||||
Plural types of spike-dipoles; | p=0.001* | |||||||
Bilateral magnetic spikes; | p=0.046* | |||||||
MTS | NS | |||||||
9 | Gattaz et al., 2011,8 Brazil | 7 individuals with TLE-IIP | 9 individuals with TLE-NP | Case–control | Collection of temporal lobe tissues | Psychiatric assessment, using DSM-IV criteria | Mann-Whitney U tests: | |
iPLA2 activity; | p=0.016* | |||||||
cPLA2 activity; | NS | |||||||
sPLA2 activity; | NS | |||||||
tPLA2 activity; | NS | |||||||
Duration of epilepsy; | NS | |||||||
Frequency of seizures | NS | |||||||
9 | Hermann et al., 2000,29 U.S.A. | 54 individuals with TLE | 38 healthy individuals | Case–control | Neuropsychological questionnaires | Assessment of psychotic symptoms, using SCL–90-R | Partial correlation: | |
Duration of epilepsy; | Paranoid Ideation r=0.46; p=0.001* | |||||||
Frequency of seizures | Psychoticism: r=0.40; p=0.004* | |||||||
NS | ||||||||
8 | Guarnieri et al., 2005,19 Brazil | 21 individuals with TLE | 23 individuals with TLE-NP | Case–control | SPECT scans | Psychiatric assessment, using DSM-IV criteria | χ2 tests: | |
11 with IIP | Gender; | χ2=0.349, NS | ||||||
10 with PIP | Marital status; | χ2=1.85; NS | ||||||
Handedness; | χ2=0.934; NS | |||||||
Presence of IPI; | χ2=0.02; NS | |||||||
Resonance laterality; | χ2=0.380; NS | |||||||
EEG ictal laterality; | χ2=0.509; NS | |||||||
Education (years); | t-tests: | |||||||
Age at epilepsy onset; | t=0.102; NS | |||||||
Duration of epilepsy; | t=0.046; NS | |||||||
Paid employment; | t=0.480; NS | |||||||
Seizure frequency; | Fisher’s exact test: | |||||||
rCBF | F=2.53; NS | |||||||
Mann-Whitney U test: | ||||||||
U=214.0; NS | ||||||||
ANOVA; NS | ||||||||
6 | Maier et al., 2000,42 U.K. | 12 individuals with TLE-P | 12 individuals with TLE-NP; | Case–control | Medical file review and MRI | Psychiatric assessment | t-tests (TLE-P and HCs): | |
26 individuals with schizophrenia and no epilepsy; | Left NAA; | p <0.001* | ||||||
38 healthy individuals | Right NAA; | p <0.001* | ||||||
Left Cho; | NS | |||||||
Right Cho; | NS | |||||||
Left Cr+PCr; | NS | |||||||
Right Cr+PCr; | NS | |||||||
Left regional H/A volume; | p=0.0001* | |||||||
Right regional H/A volume | p=0.004* |
Quality of Studies
Gender
Handedness
Age at Epilepsy Onset
Seizure History
Seizure Laterality
Seizure Frequency
The Limbic System
Temporal and Extratemporal Features
Cognitive Functioning
Personality Factors
Employment
Discussion
Risk Factor | PIP | IIP | Psychosis Not Ictally-Defined |
---|---|---|---|
Early onset of epilepsy (before age 10) | *** | *** | |
History of prolonged febrile convulsions | *** | ||
History of status epilepticus | *** | *** | *** |
Dialeptic and/or automotor seizures | *** | ||
Left-sided mesial temporal sclerosis | *** | ||
Bitemporal seizures or seizures spreading quickly to the contralateral temporal lobe | *** | ||
Secondarily generalized seizures | *** | ||
Bitemporal seizure foci | *** | ||
Seizure clusters | *** | ||
Bilateral hippocampal white-matter loss | *** | ||
Left hippocampal gray-matter reduction | *** | ||
Neuron loss in CA1 region of hippocampus | *** | *** | †*** |
Bilateral hippocampal sclerosis | *** | ||
Unilateral hippocampal sclerosis | *** | †*** | |
Reduced synaptic activity in left hippocampus | ** | ||
Decreased synaptic reorganization in dentate gyrus | *** | ||
Higher iPLA2 activity in hippocampus | ** | ||
Regional volume-reduction in hippocampus/amygdala | ** †*** | ||
Dysplastic malformations or atrophy of temporal neocortex | *** | ||
Neural abnormalities in left middle and superior temporal gyri | ** | ||
Axonal loss in temporal & frontal lobes, especially right frontal lobe | ** | ||
Extratemporal regional gray- and white-matter deficits | *** | ||
Lower current IQ | *** †*** | *** †*** | |
Alexithymia | *** |
Limitations of the Current Review
Recommendations
Definition, Diagnosis, and Classification of Psychosis
Study Populations
Study Design
Conclusions
Acknowledgments
References
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