Widespread abnormalities in white matter integrity and their relationship with duration of illness in temporal lobe epilepsy

Tsuda, Kumi; Tsuji, Takao; Ishida, Takuya; Takahashi, Shun; Yamada, Shinichi; Ohoshi, Yuji; Tomita, Masaki; Shinosaki, Kazuhiro; Ukai, Shigeo

doi:10.1002/epi4.12222

Cited by 11 publications

(10 citation statements)

References 22 publications

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“…Significant associations were present in (1) ipsilateral fornix and (2) contralateral cingulum gyrus of left-TLE patients. Similar associations were shown previously, with a whole brain TBSS analysis by (Tsuda et al, 2018) also showing significant associations between epilepsy duration and FA of the fornix in adult TLE patients after multiple comparisons correction. However contrary to our findings, analyses by (Concha et al, 2009;Kemmotsu et al, 2011;Liu et al, 2012;Chiang et al, 2016;Hatton et al, 2020) found no significant associations between epilepsy duration and FA of the fornix.…”

Section: Discussionsupporting

confidence: 89%

Multivariate white matter alterations are associated with epilepsy duration

Owen

Tisi

Vos

et al. 2020

Eur J of Neuroscience

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Previous studies investigating associations between white matter alterations and duration of temporal lobe epilepsy (TLE) have shown differing results, and were typically limited to univariate analyses of tracts in isolation. In this study, we apply a multivariate measure (the Mahalanobis distance), which captures the distinct ways white matter may differ in individual patients, and relate this to epilepsy duration. Diffusion MRI, from a cohort of 94 subjects (28 healthy controls, 33 left‐TLE and 33 right‐TLE), was used to assess the association between tract fractional anisotropy (FA) and epilepsy duration. Using ten white matter tracts, we analysed associations using the traditional univariate analysis (z‐scores) and a complementary multivariate approach (Mahalanobis distance), incorporating multiple white matter tracts into a single unified analysis. For patients with right‐TLE, FA was not significantly associated with epilepsy duration for any tract studied in isolation. For patients with left‐TLE, the FA of two limbic tracts (ipsilateral fornix, contralateral cingulum gyrus) were significantly negatively associated with epilepsy duration (Bonferonni corrected p < .05). Using a multivariate approach we found significant ipsilateral positive associations with duration in both left, and right‐TLE cohorts (left‐TLE: Spearman's ρ = 0.487, right‐TLE: Spearman's ρ = 0.422). Extrapolating our multivariate results to duration equals zero (i.e., at onset) we found no significant difference between patients and controls. Associations using the multivariate approach were more robust than univariate methods. The multivariate Mahalanobis distance measure provides non‐overlapping and more robust results than traditional univariate analyses. Future studies should consider adopting both frameworks into their analysis in order to ascertain a more complete understanding of epilepsy progression, regardless of laterality.

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Section: Discussionsupporting

confidence: 89%

Multivariate white matter alterations are associated with epilepsy duration

Owen

Tisi

Vos

et al. 2020

Eur J of Neuroscience

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“…These results are consistent with our findings regarding right temporal lobe damage. Tsuda et al () found reduced FA and increased MD and RD in widespread white matter regions of patients with TLE and that these changes were related to the duration of illness. As recurrent epileptiform discharges change the structure and function of both the temporal lobe and the entire brain (Maccotta et al, ), we found that BEN was significantly increased not only in the right middle temporal gyrus but also in other regions, such as the superior and middle frontal gyri, middle occipital gyrus, insula, putamen, and posterior cerebellum of the left hemisphere; these findings may have resulted from damage caused by epileptic discharges from the right temporal lobe to these brain regions, resulting in increased BEN.…”

Section: Discussionmentioning

confidence: 98%

Resting‐state brain entropy in right temporal lobe epilepsy and its relationship with alertness

et al. 2019

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BackgroundTo date, no functional MRI (fMRI) studies have focused on brain entropy in right temporal lobe epilepsy (rTLE) patients. Here, we characterized brain entropy (BEN) alterations in patients with rTLE using resting‐state functional MRI(rs‐fMRI) and explored the relationship between BEN and alertness.MethodThirty‐one rTLE patients and 33 controls underwent MRI scanning to investigate differences in BEN and resting‐state functional connectivity (rs‐FC) in regions of interest (ROIs) between patients and controls. Correlation analyses were performed to examine relationships between the BEN of each ROI and alertness reaction times (RTs) in rTLE patients.ResultsCompared with controls, the BEN of rTLE patients was significantly increased in the right middle temporal gyrus, inferior temporal gyrus, and other regions of the left hemisphere and significantly decreased in the right middle frontal gyrus and left supplementary motor area (p < .05). The rs‐FCs between the ROIs (at p < .01, with the left superior parietal lobule and right precentral gyrus defined as ROI1 and ROI2, respectively) and the whole brain showed an increasing trend in rTLE patients. In addition, the BEN of ROI2 was associated with the intrinsic alertness and phasic alertness RTs of patients with rTLE.ConclusionsOur findings suggest that BEN is altered in patients with rTLE and that decreased BEN in the right precentral gyrus is positively related to intrinsic and phasic alertness; the abnormal FC in the brain regions with altered entropy suggests a reconstruction of brain functional connectivity. These findings suggest that BEN mapping may provide a useful tool for probing brain mechanisms related to TLE.

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“…However, heterogeneity of pathology, disease duration, seizure frequency and severity, and age of disease onset may also lead to attenuated detection of changes in TLE. Further studies on more homogeneous groups are needed to control for these potential confounders 24,25 .…”

Section: Discussionmentioning

confidence: 99%

Hemispheric Regional Based Analysis of Diffusion Tensor Imaging and Diffusion Tensor Tractography in Patients with Temporal Lobe Epilepsy and Correlation with Patient outcomes

Alizadeh

Kozlowski

Muller

et al. 2019

Sci Rep

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Imaging in the field of epilepsy surgery remains an essential tool in terms of its ability to identify regions where the seizure focus might present as a resectable area. However, in many instances, an obvious structural abnormality is not visualized. This has created the opportunity for new approaches and imaging innovation in the field of epilepsy, such as with Diffusion Tensor Imaging (DTI) and Diffusion Tensor Tractography (DTT). In this study, we aim to evaluate the use of DTI and DTT as a predictive model in the field of epilepsy, specifically Temporal Lobe Epilepsy (TLE), and correlate their clinical significance with respect to postsurgical outcomes. A hemispheric based analysis was used to compare the tract density, as well as DTI indices of the specific regions of interest from the pathologic hemisphere to the healthy hemisphere in TLE patients. A total of 22 patients with TLE (12 males, 10 females, 22–57 age range) underwent either a craniotomy, Anterior Temporal Lobectomy (ATL), or a less invasive method of Selective Laser Amygdalohippocampectomy (SLAH) and were imaged using 3.0 T Philips Achieva MR scanner. Of the participants, 12 underwent SLAH while 10 underwent ATL. The study was approved by the institutional review board of Thomas Jefferson University Hospital. Informed consent was obtained from all patients. All patients had a diagnosis of TLE according to standard clinical criteria. DTI images were acquired axially in the same anatomical location prescribed for the T1-weighted images. The raw data set consisting of diffusion volumes were first corrected for eddy current distortions and motion artifacts. Various DTI indices such as Fractional Anisotropy (FA), Mean Diffusivity (MD), Radial Diffusivity (RD) and Axial Diffusivity (AD) were estimated and co-registered to the brain parcellation map obtained by freesurfer. 16 consolidated cortical and subcortical regions were selected as regions of interest (ROIs) by a functional neurosurgeon and DTI values for each ROI were calculated and compared with the corresponding ROI in the opposite hemisphere. Also, track density imaging (TDI) of 68 white matter parcels were generated using fiber orientation distribution (FOD) based deterministic fiber tracking and compared with contralateral side of the brain in each epileptic group: left mesial temporal sclerosis (LMTS) and right MTS (RMTS)). In patients with LMTS, MD and RD values of the left hippocampus decreased significantly using two-tailed t-test (p = 0.03 and p = 0.01 respectively) compared to the right hippocampus. Also, RD showed a marginally significant decrease in left amygdala (p = 0.05). DTT analysis in LMTS shows a marginally significant decrease in the left white matter supramarginal parcel (p = 0.05). In patients with RMTS, FA showed a significant decrease in the ipsilateral mesial temporal lobe (p = 0.02), parahippocampal area (p = 0.03) and thalamus (p = 0.006). RD showed a marginally significant increase in the ipsilateral hippocampus (p = 0.05) and a significant increase in the ipsilatera...

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Widespread abnormalities in white matter integrity and their relationship with duration of illness in temporal lobe epilepsy

Cited by 11 publications

References 22 publications

Multivariate white matter alterations are associated with epilepsy duration

Multivariate white matter alterations are associated with epilepsy duration

Resting‐state brain entropy in right temporal lobe epilepsy and its relationship with alertness

Hemispheric Regional Based Analysis of Diffusion Tensor Imaging and Diffusion Tensor Tractography in Patients with Temporal Lobe Epilepsy and Correlation with Patient outcomes

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