Quantitative MRI hippocampal volumes: association with onset and duration of epilepsy, and febrile convulsions in temporal lobectomy patients

doi:10.1016/0920-1211(93)90062-C

Epilepsy Research

Volume 15, Issue 3, July 1993, Pages 247-252

https://doi.org/10.1016/0920-1211(93)90062-C Get rights and content

Abstract

The relationships between preoperatively acquired MRI-based hippocampal volumes (HV), seizure disorder onset and duration, and early childhood febrile convulsions were investigated retrospectively with data from 72 left and 56 right temporal lobectomy patients. Patients with lesional pathology and heterotopic abnormalities were excluded. Age at development of spontaneous seizures unprovoked by an acute illness defined age of seizure disorder onset. Age of onset was subtracted from age at neurosurgery to determine duration. MRI variables included in this study were the right and left HV divided by total intracranial volume (RAHV, LAHV), and the right — left hippocampal difference (DHF). Partial correlations were used to better isolate relationships with onset of recurrent seizures corrected for age at surgery, and age at neurosurgery corrected for age of recurrent seizure onset. Partial correlations between age at neurosurgery and volume were not significant in either group. LAHV (r = 0.42, P <0.0003) and DHF (r = −0.49, P <0.0001) were correlated with age of onset in the left lobectomy group. Correlations in the right lobectomy group were not significant. The presence of a febrile convulsion was associated with smaller LAHV (F(1,70) = 10.54, P <0.002) and larger DHF (F(1,70) = 11.36, P <0.002) in left temporal lobectomy patients. The presence of a febrile convulsion in the right temporal group was associated with a slightly smaller DHF (F(1,56) = 5.90, P <0.02), and slightly smaller RAHV (F(l,56) = 4.49, P < 0.04). These data suggest that hippocampal atrophy remains stable over the duration of temporal lobe onset seizure disorders, and is associated with early onset of recurrent seizures in left temporal patients. The difference across lobectomy groups in the magnitude of effect with regard to presence of a febrile convulsion, and the lack of correlation between hippocampal atrophy and onset of recurrent seizures in the right lobectomy group may be due to the interaction of developmental differences in brain morphology and timing of the insult that produces hippocampal pathology.

References (25)

J. Cavazos et al.
Progressive neuronal loss induced by kindling: a possible mechanism in mossy fiber reorganization and hippocampal sclerosis
Brain Res.
(1990)
T.P. Sutula
Reactive changes in epilepsy: Cell death and axon sprouting induced by kindling
Epilepsy Res.
(1991)
T.L. Babb et al.
Neuronal, dendritic, and vascular profile of human temporal lobe epilepsy correlated with cellular physiology in vivo
T.L. Babb et al.
Pathological findings in epilepsy
S.F. Berkovic et al.
Hippocampal sclerosis in temporal lobe epilepsy demonstrated by magnetic resonance imaging
Ann. Neurol.
(1991)
C.T. Best
The emergence of cerebral asymmetries in early human development: a literature review and neuroembryo-logical model
G.D. Cascino et al.
Magnetic resonance imaging-based volume studies in temporal lobe epilepsy: Pathological correlations
Ann. Neurol.
(1991)
M.J. Cook et al.
Hippocampal volumetric and morphometric studies in frontal and temporal lobe epilepsy
Brain
(1992)
C.M. DeGiorgio et al.
Hippocampal pyramidal cell loss in human status epilepticus
Epilepsia
(1992)
P. Gloor
Mesial temporal sclerosis: Historical background and an overview from a modern perspective

C.R. Jack et al.

Temporal lobe volume measurement from MR images: Accuracy and left-right asymmetry in normal persons

J. Comput. Assist. Tomog.

(1988)

C.R. Jack et al.

Anterior temporal lobes and hippocampal formations: Normative volumetric measurements from MR images in young adults

Radiology

(1989)

Cited by (106)

Subcortical functional connectivity gradients in temporal lobe epilepsy
2023, NeuroImage: Clinical
Functional gradients have been used to study differences in connectivity between healthy and diseased brain states, however this work has largely focused on the cortex. Because the subcortex plays a key role in seizure initiation in temporal lobe epilepsy (TLE), subcortical functional-connectivity gradients may help further elucidate differences between healthy brains and TLE, as well as differences between left (L)-TLE and right (R)-TLE.
In this work, we calculated subcortical functional-connectivity gradients (SFGs) from resting-state functional MRI (rs-fMRI) by measuring the similarity in connectivity profiles of subcortical voxels to cortical gray matter voxels. We performed this analysis in 24 R-TLE patients and 31 L-TLE patients (who were otherwise matched for age, gender, disease specific characteristics, and other clinical variables), and 16 controls. To measure differences in SFGs between L-TLE and R-TLE, we quantified deviations in the average functional gradient distributions, as well as their variance, across subcortical structures.
We found an expansion, measured by increased variance, in the principal SFG of TLE relative to controls. When comparing the gradient across subcortical structures between L-TLE and R-TLE, we found that abnormalities in the ipsilateral hippocampal gradient distributions were significantly different between L-TLE and R-TLE.
Our results suggest that expansion of the SFG is characteristic of TLE. Subcortical functional gradient differences exist between left and right TLE and are driven by connectivity changes in the hippocampus ipsilateral to the seizure onset zone.
Multi-modal characterization and simulation of human epileptic circuitry
2022, Cell Reports
Citation Excerpt :
Electrophysiologically, the most prominent difference in GCs with disease progression is the decreased f-I gain. Yet, shorter spike latency of WG4 GCs vs. their WG1 counterparts leads to elevated, recurring circuit excitability (despite reduced f-I gain), an observation in line with clinical observations that patients with increased HS typically suffer from an increased number of seizures and an earlier stage of onset.9,15,16 Our work suggests that alteration of GC and network excitability with disease progression is mainly attributed to changes in three ionic conductances: BK, Cav2.2, and Kir2.1.
Temporal lobe epilepsy is the fourth most common neurological disorder, with about 40% of patients not responding to pharmacological treatment. Increased cellular loss is linked to disease severity and pathological phenotypes such as heightened seizure propensity. While the hippocampus is the target of therapeutic interventions, the impact of the disease at the cellular level remains unclear. Here, we show that hippocampal granule cells change with disease progression as measured in living, resected hippocampal tissue excised from patients with epilepsy. We show that granule cells increase excitability and shorten response latency while also enlarging in cellular volume and spine density. Single-nucleus RNA sequencing combined with simulations ascribes the changes to three conductances: BK, Cav2.2, and Kir2.1. In a network model, we show that these changes related to disease progression bring the circuit into a more excitable state, while reversing them produces a less excitable, “early-disease-like” state.
Reduction of ipsilateral thalamic volume in temporal lobe epilepsy with hippocampal sclerosis
2018, Journal of Clinical Neuroscience
Citation Excerpt :
In contrast to the previous studies, we did not find any correlation between the volumes of the hippocampus and the duration of epilepsy in TLE patients with HS. While some previous studies found a significant correlation between them [16,33], other studies, like our present study, were also unable to replicate this finding [34,35]. Although several studies showed a negative correlation between hippocampal atrophy and the duration of epilepsy, suggesting a progressive nature of TLE with HS, the true relationship between the volumes of the hippocampus and the duration of epilepsy in TLE with HS remains a matter for discussion.
The thalamus plays an important role in the modulation of both focal and generalized seizures, but the mechanisms related to seizures may be different among epilepsy syndromes. The aim of this study is to investigate the thalamic atrophy in different epilepsy syndromes. We enrolled a total of 72 patients with epilepsy (22 patients with temporal lobe epilepsy with hippocampal sclerosis, 21 patients with extra-temporal lobe epilepsy, and 29 patients with juvenile myoclonic epilepsy). We analyzed structural volumes of the brain with FreeSurfer 5.1 software, and compared them among subgroups of epilepsy and normal control subjects. Moreover, we quantified correlations between the duration of epilepsy and the structural volumes with age and sex as covariates. The volumes of the ipsilateral hippocampus in temporal lobe epilepsy with hippocampal sclerosis were significantly smaller than those in extra-temporal lobe epilepsy and normal control subjects [analysis of variance (ANOVA), p < 0.001]. Although the volumes of the ipsilateral thalamus were not different from those of normal control subjects, the volumes of the ipsilateral thalamus were negatively correlated with duration of epilepsy in temporal lobe epilepsy with hippocampal sclerosis (r = −0.5, p = 0.02). However, the volumes of interest in extra-temporal lobe epilepsy and juvenile myoclonic epilepsy were not different from those in normal control subjects, and none of these structures were correlated with duration of epilepsy. These findings suggest that the role of the thalamus may be different in thalamo-limbic circuits among epilepsy syndromes.
White matter structural connectivity changes correlate with epilepsy duration in temporal lobe epilepsy
2016, Epilepsy Research
Citation Excerpt :
Fourth, use of antiepileptic drugs (Gunbey et al., 2011) and heterogeneity in TLE etiology (Scanlon et al., 2013) have also been shown to affect DTI. Earlier age of onset has also been associated with decreased hippocampal volumes (Trenerry et al., 1993). As a population-based study of TLE, our patient sample inevitably includes patients with several different pathologies.
Temporal lobe epilepsy (TLE) is thought to be a network disease and structural changes using diffusion tensor imaging (DTI) have been shown. However, lateralized differences in the structural integrity of TLE, as well as changes in structural integrity with longer disease duration, have not been well defined.
We examined the fractional anisotropy (FA) and mean diffusivity (MD) in the hippocampus, as well as its primary (cingulum and fornix) and remote (uncinate and external capsule) connections in both right and left TLE. Changes in diffusion measures over the disease course were examined by correlating FA and MD in the various structures with epilepsy duration. The potential for each measure of anisotropy and diffusivity as a marker of TLE laterality was investigated using random forest (RF) analysis.
MD was increased in the bilateral hippocampus, cingulum, fornix and the right external capsule in both left and right TLE compared to controls. In addition, left TLE exhibited an increased MD in the ipsilateral uncinate fasciculus and bilateral external capsules. A decrease in FA was seen in the left cingulum in left TLE. RF analysis demonstrated that MD of the right hippocampus and FA of the left external capsule were important predictors of TLE laterality. An association of increased MD with epilepsy duration was seen in the left hippocampus in left TLE.
Evidence of disrupted white matter architecture in the hippocampus and its primary and remote connections were demonstrated in TLE. While changes in the hippocampus and cingulum were more prominent in right TLE, remote changes were more prominent in left TLE. MD of the right hippocampus and FA of the left external capsule were found to be the strongest structural predictors of TLE laterality. Changes associated with duration of epilepsy indicated that changes in structural integrity may be progressive over the disease course. This study illustrates the potential of structural diffusion tensor imaging in elucidating pathophysiology, enhancing diagnosis and assisting prognostication.
Subcortical and cerebellar atrophy in mesial temporal lobe epilepsy revealed by automatic segmentation
2008, Epilepsy Research
To determine the validity and utility of using automated subcortical segmentation to identify atrophy of the hippocampus and other subcortical and cerebellar structures in patients with mesial temporal lobe epilepsy (MTLE).
Volumetric MRIs were obtained on 21 patients with MTLE (11 right, 10 left) and 21 age- and gender-matched healthy controls. Labeling of subcortical and cerebellar structures was accomplished using automated reconstruction software (FreeSurfer). Multivariate analysis of covariance (MANCOVA) was used to explore group differences in intracranial-normalized, age-adjusted volumes and structural asymmetries. Step-wise discriminant function analysis was used to identify the linear combination of volumes that optimized classification of individual subjects.
Results revealed the expected reduction in hippocampal volume on the side ipsilateral to the seizure focus, as well as bilateral reductions in thalamic and cerebellar gray matter volume. Analysis of structural asymmetries revealed significant asymmetry in the hippocampus and putamen in patients compared to controls. The discriminant function analysis revealed that patients with right and left MTLE were best distinguished from one another using a combination of subcortical volumes that included the right and left hippocampus and left thalamus (91–100% correct classification using cross-validation).
Volumetric data obtained with automated segmentation of subcortical and cerebellar structures approximate data from previous studies based on manual tracings. Our data suggest that automated segmentation can provide a clinically useful means of evaluating the nature and extent of structural damage in patients with MTLE and may increase diagnostic classification of patients, especially when hippocampal atrophy is mild.
Temporal lobe epilepsy
2005, Magnetic Resonance in Epilepsy

View all citing articles on Scopus

^☆: Portions of these data were presented at the annual meeting of the American Epilepsy Society, Seattle, Washington, December 6–9, 1992.

View full text

Research reportQuantitative MRI hippocampal volumes: association with onset and duration of epilepsy, and febrile convulsions in temporal lobectomy patients☆

Abstract

Brain Res.

Epilepsy Res.

Neuronal, dendritic, and vascular profile of human temporal lobe epilepsy correlated with cellular physiology in vivo

Pathological findings in epilepsy

Hippocampal sclerosis in temporal lobe epilepsy demonstrated by magnetic resonance imaging

Ann. Neurol.

The emergence of cerebral asymmetries in early human development: a literature review and neuroembryo-logical model

Magnetic resonance imaging-based volume studies in temporal lobe epilepsy: Pathological correlations

Ann. Neurol.

Hippocampal volumetric and morphometric studies in frontal and temporal lobe epilepsy

Brain

Hippocampal pyramidal cell loss in human status epilepticus

Epilepsia

Mesial temporal sclerosis: Historical background and an overview from a modern perspective

Temporal lobe volume measurement from MR images: Accuracy and left-right asymmetry in normal persons

J. Comput. Assist. Tomog.

Anterior temporal lobes and hippocampal formations: Normative volumetric measurements from MR images in young adults

Radiology

Research report
Quantitative MRI hippocampal volumes: association with onset and duration of epilepsy, and febrile convulsions in temporal lobectomy patients☆