Clinical Radiology 69 (2014) 589e596
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Extratemporal abnormalities of brain parenchyma in young adults with temporal lobe epilepsy: A diffusion tensor imaging study X.-y. Yin, S.-j. Qiu*, Z.-y. Liu, H.-z. Wang, W.-f. Xiong, S.-s. Li, Y. Wang Department of Medical Imaging Center, Nanfang Hospital, Southern Medical University, PR China
art icl e i nformat ion Article history: Received 5 July 2013 Received in revised form 19 November 2013 Accepted 7 January 2014
AIM: To examine extratemporal abnormalities of the cerebral parenchyma in young adult temporal lobe epilepsy (TLE) patients using diffusion tensor imaging (DTI). MATERIALS AND METHODS: The study comprised 20 adults with unilateral TLE and 20 controls. The fractional anisotropy (FA), apparent diffusion coefﬁcient (ADC), parallel eigenvalue (lk), and perpendicular eigenvalue (lt) were calculated in the regions of interest (ROIs) using a 3 T MRI system. ROIs included the anterior/posterior limb of the internal capsule (AIC/ PIC), external capsule (EC), head of caudate nucleus (HCN), lenticular nucleus (LN), thalamus (TL), and genu/body/splenium of the corpus callosum (GCC/BCC/SCC). RESULTS: Compared to controls, TLE patients showed lower FA in all ROIs; higher ADC in bilateral ECs, HCNs, TLs, and BCC; lower lk in the ipsilateral LN and bilateral AICs, TL, and GCC; and higher lt in all ROIs except the bilateral PICs. In TLE patients, the ipsilateral TL had decreased FA compared with the contralateral TL. Pearson correlation analysis revealed a negative correlation between the ADC of the GCC and the age at onset of epilepsy; the lk of the ipsilateral PIC and age at onset of epilepsy; the lt of the contralateral AIC and duration of epilepsy, respectively; and a positive correlation between the ADC of the GCC and the duration of epilepsy and the lt of the GCC and the duration of epilepsy, respectively. CONCLUSION: The study revealed bilateral extratemporal abnormalities in young adult TLE patients compared with controls. In addition, TLE patients with younger age at onset or longer duration of epilepsy may have more serious extratemporal changes. Ó 2014 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Introduction Epilepsy is a common chronic disorder of the nervous system characterized by abnormal synchronized excess ﬁrings of a large number of cortical and subcortical neurons. Patients with epilepsy can have a variety of clinical manifestations, such as dyskinesia, sensory disturbance, dysphrenia, and cognitive impairment. The morbidity of * Guarantor and correspondent: S.-j. Qiu, 1838# Guangzhou Avenue North, Guangzhou City, Guangdong Province, 510515, PR China. Tel./fax: þ86 20 62787400. E-mail address: [email protected]
epilepsy in China is approximately 0.5%. Temporal lobe epilepsy (TLE) is the most common form of partial epilepsy. As there is widespread propagation of synchronized neuronal ﬁring in seizure disorders via neuronal networks, other cortical and subcortical regions of the brain can be affected despite a single seizure focus.1e7 Several diffusion tensor imaging (DTI) studies have found that white matter abnormalities are most pronounced in the cerebral hemisphere ipsilateral to the side of seizure onset.8,9 Furthermore, whole-brain voxel analyses of grey matter density and thickness, and other DTI studies, have shown diffuse symmetric abnormalities.3,10,11 Recently, several studies have found increased mean diffusivity (MD)
0009-9260/$ e see front matter Ó 2014 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.crad.2014.01.006
X.-y. Yin et al. / Clinical Radiology 69 (2014) 589e596
and decreased fractional anisotropy (FA) in subcortical structures such as the amygdala, hippocampus, and thalamus, which are ipsilateral to the seizure focus. Other studies have implicated focal white matter regions and fasciculi, including the ipsilateral uncinate fasciculus (UF), fornix, and corpus callosum.5,12e15 Together, these results suggest that TLE can lead to widespread structural alteration in the brain. Therefore, evaluation of extratemporal regions may provide useful information as to the diffuse changes in the brain that accompany TLE. TLE patients selected in previous studies were almost minors or there was no stated age limit. Given the growing brain of minors and degenerating of the brain in the aged, it was hypothesized that different age brackets might affect the ﬁndings of DTI. Therefore, in the present study young adults 18e35 years old were selected as the study cohort to eliminate the possible inﬂuence of age. The aim of the present study was to examine extratemporal abnormalities of the cerebral parenchyma in young adult TLE patients using DTI.
Materials and methods Study participants From May to November 2011, 20 young adult patients with unilateral TLE (10 females; aged 22.7 4.23 years, range 18e32 years; 10 left/10 right laterality TLE; age of epilepsy onset was 11.62 6.98 years, range 0.5e29 years; duration of epilepsy was 11.08 4.70 years, range 3e18 years) were recruited. Twenty healthy controls were matched to the patients based on age and sex (10 females; aged 23.95 4.17 years, range 18e31 years). The selection criteria for TLE patients were a clinical diagnosis of TLE; epileptic activity localized to the temporal lobe by video electroencephalogram (EEG); no other neurological disorders. All participants underwent conventional magnetic resonance imaging (MRI) and DTI, and no abnormalities were detected at conventional MRI, except three TLE patients had hippocampal sclerosis. All participants were right-handed, and informed consent had been obtained from those who participated. The study was approved by an institutional review board and was conducted under strict adherence to the Privacy Rule of HIPAA. All included individuals were fully informed of the purpose, methods, and precautions of the trial, and formally agreed to participate and signed an informed consent document.
MRI acquisition MRI data were obtained using a 3 T GE Signa EXCITE MRI system (General Electric, Milwaukee, WI, USA), with an eight-channel array head coil. Convention MRI consisted of a variety of sequences including axial and sagittal T1-weighted imaging [repetition time (TR) ¼ 2500 ms/echo time (TE) ¼ 24 ms, section thickness ¼ 5 mm, ﬁeld of view ¼ 24 cm, matrix ¼ 320 250]; axial T2-weighted imaging (TR ¼ 5100 ms/TE 130 ms, section thickness ¼ 5 mm, ﬁeld of
view ¼ 24 cm, matrix ¼ 512 288); and oblique coronal T2weighted ﬂuid-attenuated inversion recovery (FLAIR) obtained perpendicular to the long axis of the hippocampus (TR ¼ 9000 ms//TE ¼ 125 ms, section thickness ¼ 3 mm, ﬁeld of view ¼ 24 cm, matrix ¼ 512 256). DTI was performed in the axial plane using single-shot diffusion-weighted echo planar imaging, with the following parameters: TR ¼ 10,000 ms/TE ¼ 88 ms, section thickness ¼ 3 mm, ﬁeld of view ¼ 24 cm, matrix ¼ 130 128, 25 non-colinear directions with a b-value of 1000 s/mm. The duration of the scan was 4 min 40 s.
Imaging analysis All DTI images were transferred to a workstation where image reconstruction and post-processing region of interest (ROI) analyses were performed with Functool (General Electric). The ROIs included the anterior limb of the internal capsule (AIC), the posterior limb of the internal capsule (PIC), the external capsule (EC), the head of the caudate nucleus (HCN), the lenticular nucleus (LN), the thalamus (TL), and the genu of the corpus callosum (GCC), the body of the corpus callosum (BCC), and splenium of the corpus callosum (SCC; see Fig 1). The AIC, PIC, EC, HCN, LN, TL, GCC, and SCC were delineated on the section with the interventricular foramen; BCCs were delineated on the section showing the maximal BCC (see Fig 1). The ROIs were placed on the axial b ¼ 0 maps (the black-and-white pictures in Fig 1) and colour-coded maps (the colour maps in Fig 1). For bilateral ROIs, one side was placed ﬁrst and then a symmetrical line was drawn using the mirrored symmetrical manner of the software to localize the contralateral side. All ROIs were placed manually by one radiologist who was blinded to the patients’ identities. Four DTI parameters were used to quantitatively analyse the ROIs: FA, apparent diffusion coefﬁcient (ADC), parallel eigenvalue (lk), and perpendicular eigenvalue (lt).
Statistical analyses Statistical analyses were performed using SPSS version 13.0 (SPSS, Chicago, IL, USA). A paired-samples t-test was used to compare the bilateral DTI data of all subjects. An independent-sample t-test was used to compare the ipsilateral and contralateral data of patients with controls. Pearson’s correlation analysis was used to examine the correlation between the age at onset and duration of epilepsy, and the DTI parameters. A p-value of