Bilateral volume reduction in posterior hippocampus in psychosis of epilepsy

James Allebone, Richard Kanaan, Jerome Maller, Terry O'Brien, Saul Alator Mullen, Mark Cook, Sophia J. Adams, Simon Vogrin, David N. Vaughan, Alan Connelly, Patrick Kwan, S. F. Berkovic, Wendyl J. D'Souza, Graeme Jackson, Dennis Velakoulis, Sarah J. Wilson

Research output: Contribution to journalArticleResearchpeer-review

Abstract

Objective: Psychosis of epilepsy (POE) occurs more frequently in temporal lobe epilepsy, raising the question as to whether abnormalities of the hippocampus are aetiologically important. Despite decades of investigation, it is unclear whether hippocampal volume is reduced in POE, perhaps due to small sample sizes and methodological limitations of past research. Methods: In this study, we examined the volume of the total hippocampus, and the hippocampal head, body and tail, in a large cohort of patients with POE and patients with epilepsy without psychosis (EC). One hundred adults participated: 50 with POE and 50 EC. Total and subregional hippocampal volumes were manually traced and compared between (1) POE and EC; (2) POE with temporal lobe epilepsy, extratemporal lobe epilepsy and generalised epilepsy; and (3) patients with POE with postictal psychosis (PIP) and interictal psychosis (IP). Results: Compared with EC the POE group had smaller total left hippocampus volume (13.5% decrease, p<0.001), and smaller left hippocampal body (13.3% decrease, p=0.002), and left (41.5% decrease, p<0.001) and right (36.4% decrease, p<0.001) hippocampal tail volumes. Hippocampal head volumes did not differ between groups. Conclusion: Posterior hippocampal volumes are bilaterally reduced in POE. Volume loss was observed on a posteroanterior gradient, with severe decreases in the tail and moderate volume decreases in the body, with no difference in the hippocampal head. Posterior hippocampal atrophy is evident to a similar degree in PIP and IP. Our findings converge with those reported for the paradigmatic psychotic disorder, schizophrenia, and suggest that posterior hippocampal atrophy may serve as a biomarker of the risk for psychosis, including in patients with epilepsy.

Original languageEnglish
Pages (from-to)688-694
Number of pages7
JournalJournal of Neurology, Neurosurgery and Psychiatry
Volume90
Issue number6
DOIs
Publication statusPublished - 16 May 2019

Keywords

  • epilepsy
  • hippocampus
  • interictal psychosis
  • postictal psychosis
  • psychosis

Cite this

Allebone, James ; Kanaan, Richard ; Maller, Jerome ; O'Brien, Terry ; Mullen, Saul Alator ; Cook, Mark ; Adams, Sophia J. ; Vogrin, Simon ; Vaughan, David N. ; Connelly, Alan ; Kwan, Patrick ; Berkovic, S. F. ; D'Souza, Wendyl J. ; Jackson, Graeme ; Velakoulis, Dennis ; Wilson, Sarah J. / Bilateral volume reduction in posterior hippocampus in psychosis of epilepsy. In: Journal of Neurology, Neurosurgery and Psychiatry. 2019 ; Vol. 90, No. 6. pp. 688-694.
@article{686446b6a50a47f8aa82bf9a5b2591be,
title = "Bilateral volume reduction in posterior hippocampus in psychosis of epilepsy",
abstract = "Objective: Psychosis of epilepsy (POE) occurs more frequently in temporal lobe epilepsy, raising the question as to whether abnormalities of the hippocampus are aetiologically important. Despite decades of investigation, it is unclear whether hippocampal volume is reduced in POE, perhaps due to small sample sizes and methodological limitations of past research. Methods: In this study, we examined the volume of the total hippocampus, and the hippocampal head, body and tail, in a large cohort of patients with POE and patients with epilepsy without psychosis (EC). One hundred adults participated: 50 with POE and 50 EC. Total and subregional hippocampal volumes were manually traced and compared between (1) POE and EC; (2) POE with temporal lobe epilepsy, extratemporal lobe epilepsy and generalised epilepsy; and (3) patients with POE with postictal psychosis (PIP) and interictal psychosis (IP). Results: Compared with EC the POE group had smaller total left hippocampus volume (13.5{\%} decrease, p<0.001), and smaller left hippocampal body (13.3{\%} decrease, p=0.002), and left (41.5{\%} decrease, p<0.001) and right (36.4{\%} decrease, p<0.001) hippocampal tail volumes. Hippocampal head volumes did not differ between groups. Conclusion: Posterior hippocampal volumes are bilaterally reduced in POE. Volume loss was observed on a posteroanterior gradient, with severe decreases in the tail and moderate volume decreases in the body, with no difference in the hippocampal head. Posterior hippocampal atrophy is evident to a similar degree in PIP and IP. Our findings converge with those reported for the paradigmatic psychotic disorder, schizophrenia, and suggest that posterior hippocampal atrophy may serve as a biomarker of the risk for psychosis, including in patients with epilepsy.",
keywords = "epilepsy, hippocampus, interictal psychosis, postictal psychosis, psychosis",
author = "James Allebone and Richard Kanaan and Jerome Maller and Terry O'Brien and Mullen, {Saul Alator} and Mark Cook and Adams, {Sophia J.} and Simon Vogrin and Vaughan, {David N.} and Alan Connelly and Patrick Kwan and Berkovic, {S. F.} and D'Souza, {Wendyl J.} and Graeme Jackson and Dennis Velakoulis and Wilson, {Sarah J.}",
year = "2019",
month = "5",
day = "16",
doi = "10.1136/jnnp-2018-319396",
language = "English",
volume = "90",
pages = "688--694",
journal = "Journal of Neurology, Neurosurgery and Psychiatry",
issn = "0022-3050",
publisher = "BMJ Publishing Group",
number = "6",

}

Allebone, J, Kanaan, R, Maller, J, O'Brien, T, Mullen, SA, Cook, M, Adams, SJ, Vogrin, S, Vaughan, DN, Connelly, A, Kwan, P, Berkovic, SF, D'Souza, WJ, Jackson, G, Velakoulis, D & Wilson, SJ 2019, 'Bilateral volume reduction in posterior hippocampus in psychosis of epilepsy', Journal of Neurology, Neurosurgery and Psychiatry, vol. 90, no. 6, pp. 688-694. https://doi.org/10.1136/jnnp-2018-319396

Bilateral volume reduction in posterior hippocampus in psychosis of epilepsy. / Allebone, James; Kanaan, Richard; Maller, Jerome; O'Brien, Terry; Mullen, Saul Alator; Cook, Mark; Adams, Sophia J.; Vogrin, Simon; Vaughan, David N.; Connelly, Alan; Kwan, Patrick; Berkovic, S. F.; D'Souza, Wendyl J.; Jackson, Graeme; Velakoulis, Dennis; Wilson, Sarah J.

In: Journal of Neurology, Neurosurgery and Psychiatry, Vol. 90, No. 6, 16.05.2019, p. 688-694.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Bilateral volume reduction in posterior hippocampus in psychosis of epilepsy

AU - Allebone, James

AU - Kanaan, Richard

AU - Maller, Jerome

AU - O'Brien, Terry

AU - Mullen, Saul Alator

AU - Cook, Mark

AU - Adams, Sophia J.

AU - Vogrin, Simon

AU - Vaughan, David N.

AU - Connelly, Alan

AU - Kwan, Patrick

AU - Berkovic, S. F.

AU - D'Souza, Wendyl J.

AU - Jackson, Graeme

AU - Velakoulis, Dennis

AU - Wilson, Sarah J.

PY - 2019/5/16

Y1 - 2019/5/16

N2 - Objective: Psychosis of epilepsy (POE) occurs more frequently in temporal lobe epilepsy, raising the question as to whether abnormalities of the hippocampus are aetiologically important. Despite decades of investigation, it is unclear whether hippocampal volume is reduced in POE, perhaps due to small sample sizes and methodological limitations of past research. Methods: In this study, we examined the volume of the total hippocampus, and the hippocampal head, body and tail, in a large cohort of patients with POE and patients with epilepsy without psychosis (EC). One hundred adults participated: 50 with POE and 50 EC. Total and subregional hippocampal volumes were manually traced and compared between (1) POE and EC; (2) POE with temporal lobe epilepsy, extratemporal lobe epilepsy and generalised epilepsy; and (3) patients with POE with postictal psychosis (PIP) and interictal psychosis (IP). Results: Compared with EC the POE group had smaller total left hippocampus volume (13.5% decrease, p<0.001), and smaller left hippocampal body (13.3% decrease, p=0.002), and left (41.5% decrease, p<0.001) and right (36.4% decrease, p<0.001) hippocampal tail volumes. Hippocampal head volumes did not differ between groups. Conclusion: Posterior hippocampal volumes are bilaterally reduced in POE. Volume loss was observed on a posteroanterior gradient, with severe decreases in the tail and moderate volume decreases in the body, with no difference in the hippocampal head. Posterior hippocampal atrophy is evident to a similar degree in PIP and IP. Our findings converge with those reported for the paradigmatic psychotic disorder, schizophrenia, and suggest that posterior hippocampal atrophy may serve as a biomarker of the risk for psychosis, including in patients with epilepsy.

AB - Objective: Psychosis of epilepsy (POE) occurs more frequently in temporal lobe epilepsy, raising the question as to whether abnormalities of the hippocampus are aetiologically important. Despite decades of investigation, it is unclear whether hippocampal volume is reduced in POE, perhaps due to small sample sizes and methodological limitations of past research. Methods: In this study, we examined the volume of the total hippocampus, and the hippocampal head, body and tail, in a large cohort of patients with POE and patients with epilepsy without psychosis (EC). One hundred adults participated: 50 with POE and 50 EC. Total and subregional hippocampal volumes were manually traced and compared between (1) POE and EC; (2) POE with temporal lobe epilepsy, extratemporal lobe epilepsy and generalised epilepsy; and (3) patients with POE with postictal psychosis (PIP) and interictal psychosis (IP). Results: Compared with EC the POE group had smaller total left hippocampus volume (13.5% decrease, p<0.001), and smaller left hippocampal body (13.3% decrease, p=0.002), and left (41.5% decrease, p<0.001) and right (36.4% decrease, p<0.001) hippocampal tail volumes. Hippocampal head volumes did not differ between groups. Conclusion: Posterior hippocampal volumes are bilaterally reduced in POE. Volume loss was observed on a posteroanterior gradient, with severe decreases in the tail and moderate volume decreases in the body, with no difference in the hippocampal head. Posterior hippocampal atrophy is evident to a similar degree in PIP and IP. Our findings converge with those reported for the paradigmatic psychotic disorder, schizophrenia, and suggest that posterior hippocampal atrophy may serve as a biomarker of the risk for psychosis, including in patients with epilepsy.

KW - epilepsy

KW - hippocampus

KW - interictal psychosis

KW - postictal psychosis

KW - psychosis

UR - http://www.scopus.com/inward/record.url?scp=85062082657&partnerID=8YFLogxK

U2 - 10.1136/jnnp-2018-319396

DO - 10.1136/jnnp-2018-319396

M3 - Article

VL - 90

SP - 688

EP - 694

JO - Journal of Neurology, Neurosurgery and Psychiatry

JF - Journal of Neurology, Neurosurgery and Psychiatry

SN - 0022-3050

IS - 6

ER -