Fulvia Palesi1, Paul Eugene Summers1, Claudia A.M. Gandini Wheeler-Kingshott2,3,4, Giancarlo Germani1, Valeria Mariani5, Laura Tassi5, and Paolo Vitali1
1Neuroradiology Unit, Brain MRI 3T Research Center, IRCCS Mondino Foundation, Pavia, Italy, 2Queen Square MS Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, Faculty of Brain Sciences, University College London, London, United Kingdom, 3Department of Brain and Behavioural Sciences, University of Pavia, Pavia, Italy, 4Brain MRI 3T Research Center, IRCCS Mondino Foundation, Pavia, Italy, 5”C.Munari” Epilepsy Surgery Centre, ASST Ospedale Metropolitano Niguarda, Milan, Italy
Synopsis
Temporal Lobe Epilepsy (TLE) is the most common form of
focal epilepsy. Neuroimaging and neuropathological studies indicates that the
structural network affected in TLE extends to both temporal and extra-temporal
structures.
In this work, quantitative 3DMT maps were used in a Voxel
Based Morphometry(VBM) framework to assess atrophy in left and right TLE
compared to controls. Our findings revealed that 3DMT maps, thankfully to their
excellent grey-white matter contrast, can be successfully employed for VBM in
epilepsy identifying temporal and extra-temporal grey and white matter alterations in
patients. This study is a proof-of-principle to adopt 3DMT for voxel based
analysis in TLE.
Introduction
Temporal Lobe Epilepsy (TLE) is the most common form of
focal epilepsy, accounting for about 70% of cases undergoing epilepsy surgery.
It is often associated with hippocampal sclerosis, low-grade tumours, or
malformation of cortical development, but some cases remain without specific
pathology even after histological examination (1). Regardless of the underlying
pathology, converging evidence from neuroimaging and neuropathological studies
indicates that the structural network affected in TLE extends to both temporal
and extra-temporal brain structures.
Several studies have explored structural abnormalities in TLE
using Voxel Based Morphometry (VBM) on conventional 3DT1 data (2,3). However,
it has been shown in other diseases that magnetization transfer (MT) maps may provide
a better grey/white matter demarcation (4). This is attractive for detecting
malformations of cortical development, often associated with a loss of
grey/white matter demarcation. This pilot study aimed at evaluating structural
abnormalities in TLE, divided in left and right groups, compared to healthy
controls (HC) using 3DMT maps instead of conventional 3DT1.Methods
Subjects: 33 TLE patients (19 left TLE: 33.2±9.9yrs, 10males, 14 right TLE: 39.5±10.7yrs, 6males) and 32 HC (32.6±8.2yrs, 18males). After temporal
lobectomy, histopathology revealed hippocampal sclerosis (7 cases, 4 left and 3
right), focal lesions (tumours, cavernoma, scars 8 cases, 5 left and 3 right),
focal cortical dysplasia (4 cases, 2 left and 2 right) and cryptogenics with only
a gliosis (14
cases, 8 left and 6 right).
MRI acquisition: A multi-parameter mapping (MPM) (5)
protocol was implemented by acquiring 3D multi-echo PD, R1 and MT-weighted
gradient-echo scans using a Siemens
Skyra 3T scanner (Siemens AG,
Erlangen, Germany).
3DMT and VBM analysis: MPM maps were elaborated with the hMRI tool
(http://hMRI.info) under
Matlab and quantitative 3D maps of MT, pseudo PD, R1 and R2* were generated. 3DMT
maps of all subjects were segmented into grey matter (GM), white matter (WM)
and cerebrospinal fluid (CSF) using the CAT12 toolbox (6). Using the DARTEL framework, the segmented images were normalized
to MNI space (ICBM-152) with 1.5 mm isotropic voxels, and smoothed using a
kernel of 6-6-6 mm3 in SPM12 toolbox (7).
Statistical analysis: The smoothed and normalized images were used as
inputs for the voxel-wise general linear model analysis. A one Way ANOVA
analysis was performed to identify the atrophic regions of right TLE versus HC,
left TLE versus HC and right TLE versus left TLE. Gender, age and total
intracranial volume (TIV) were used as covariates. The significance was set at
p<0.001 with an extension of 100 voxels and with FWE correction at p<0.05
at cluster level.
Results
The 3DMT maps obtained showed an excellent grey/white matter
contrast (Fig.1). The enhanced grey/white matter contrast of the 3DMT compared
to 3DT1 (Fig.1) resulted also in a more accurate segmentation of the two
cerebral tissues and cerebro spinal fluid.
Most of grey matter atrophic changes were identified in the
left hemisphere of both left and right TLE patients, compared to HC. Specifically,
grey matter abnormalities in left TLE were found in left fronto-orbital gyrus,
left superior frontal gyrus, left thalamus, and bilateral precentral gyrus (Fig.2).
Grey matter abnormalities in right TLE were found in bilateral cerebellar
hemispheres and vermis, left fronto-orbital gyrus, left superior temporal gyrus
(Fig.3).
Significant white matter atrophy was identified only in
right TLE patients, mainly in bilateral cerebellum, deep right temporal lobe
and bilateral fornix (Fig.4).
No significant differences were found in direct
comparisons between left and right TLE patients.
Discussion
This pilot study using VBM on 3DMT maps identified grey and
white matter atrophy, localised in the cerebellum and cerebral areas previously
reported for classical VBM studies on conventional 3DT1 (2). For instance, the thalamus
is the subcortical region more often found atrophic in TLE. In our pilot study,
a lack of significant temporo-mesial atrophy may be due to the low percentage of
patients of this study with hippocampal sclerosis, compared to classical TLE
studies. A peculiar lateralized pattern of abnormalities emerged: prevalent
grey matter atrophy in left TLE, and on the contrary a prevailing white matter
atrophy in right TLE.Conclusions
3DMT map obtained by MPM, with excellent grey-white matter
contrast, can be successfully employed for VBM in epilepsy. This study is a
proof-of-principle to adopt 3DMT for voxel based analysis in TLE patients, both
for study groups and single subject analysis.Acknowledgements
3TLE is a
multicentric research project granted by Italian Health Ministry
(NET2013-02355313): Magnetic resonance imaging in drug-refractory temporal lobe
epilepsy: standardization of advanced structural and functional protocols at
3T, to identify hippocampal and extra-hippocampal abnormalities.References
- Blumcke et al. Histopathological findings in brain tissue obtained during epilepsy surgery. N Engl JMed 2017;377:1648-562.
- Keller SS1, Roberts N. Voxel-based morphometry of temporal lobe epilepsy: an introduction andreview of the literature. Epilepsia. 2008 May;49(5):741-573.
- Beheshti I, Sone D, Farokhian F, Maikusa N, Matsuda H. Gray Matter and White MatterAbnormalities in Temporal Lobe Epilepsy Patients with and without Hippocampal Sclerosis. FrontNeurol. 2018;9:107.
- Sethi A, Evelyn-Rahr E, Dowell N, Jain S, Voon V, et al. Magnetization transfer imagingidentifies basal ganglia abnormalities in adult ADHD that are invisible to conventional T1weighted voxel-based morphometry. Neuroimage Clin. 2017;15:8–14.
- Weiskopf N, Suckling J, Williams G, Correia MM, Inkster B et al. Quantitative multi-parameter mapping of R1, PD(*), MT, and R2(*) at 3T: a multi-center validation. Frontiersin Neuroscience. 2013;7:95 doi: 10.3389/fnins.2013.00095.
- Gaser C, Dahnke R. CAT - A Computational Anatomy Toolbox for the Analysis of Structural MRIData. Hum Brain Mapp 2016.
- Ashburner J, Barnes G, Chen C, Daunizeau J, Flandin G, et al. SPM8 Manual The FILMethods Group (and Honorary Members). Functional Imaging Laboratory. 2013: 475–1.