Widespread Abnormalities in White Matter Integrity and Their Relationship with Duration of Illness in Temporal Lobe Epilepsy

Overview

Journal Epilepsia Open

Date 2018 Jun 9

PMID 29881803

Citations 8

Authors

Kumi Tsuda

Tomikimi Tsuji

Takuya Ishida

Shun Takahashi

Shinichi Yamada

Yuji Ohoshi

Masaki Terada

Kazuhiro Shinosaki

Satoshi Ukai

Affiliations

Soon will be listed here.

Abstract

Objective: Elucidation of abnormal connections throughout the whole brain is necessary to understand temporal lobe epilepsy (TLE). We examined abnormalities in whole-brain white matter integrity and their relationship with duration of illness in patients with TLE.

Methods: The subjects were 15 patients with TLE and 17 healthy controls. Mean duration of illness in the TLE group was 21.6 years. Tract-based spatial statistics (TBSS) were used for diffusion tensor imaging (DTI) analysis. Four diffusion tensor metrics, that is, fractional anisotropy (FA), mean diffusivity (MD), axial diffusivity (AD), and radial diffusivity (RD) were calculated and then examined for differences between the TLE and healthy control groups. We also examined for correlations between DTI parameters and duration of illness in the TLE group.

Results: In the TLE group, compared with the healthy control group, FA was reduced, and MD and RD were increased, not only in the limbic and temporal lobe regions and their directly connecting regions in both hemispheres, but also in remote white matter regions. Duration of illness showed a significant negative correlation with mean whole-brain FA and a significant positive correlation with both mean whole-brain MD and RD. Brain regions showing correlation between disease duration and DTI metrics also extended to the limbic area and its connecting regions, and to remote white matter regions.

Significance: The results of this study suggest that widespread abnormalities in white matter integrity in patients with TLE are associated with long-term disease.

Citing Articles

Altered metabolic-functional coupling in the epileptogenic network could predict surgical outcomes of mesial temporal lobe epilepsy.

Yuan S, Huang H, Cai B, Li J, Zhang M, Luo J Front Neurosci. 2023; 17:1165982.

PMID: 37360171 PMC: 10286900. DOI: 10.3389/fnins.2023.1165982.

A tract-based spatial statistics study of white matter integrity in epilepsy.

Hou X, Feng H, Xu B, Li Z, Lu Y, Zhao H Am J Transl Res. 2023; 14(12):8980-8990.

PMID: 36628222 PMC: 9827316.

MEG abnormalities and mechanisms of surgical failure in neocortical epilepsy.

Owen T, Schroeder G, Janiukstyte V, Hall G, McEvoy A, Miserocchi A Epilepsia. 2023; 64(3):692-704.

PMID: 36617392 PMC: 10952279. DOI: 10.1111/epi.17503.

People with mesial temporal lobe epilepsy have altered thalamo-occipital brain networks.

Wills K, Gonzalez H, Johnson G, Haas K, Morgan V, Narasimhan S Epilepsy Behav. 2020; 115:107645.

PMID: 33334720 PMC: 7882020. DOI: 10.1016/j.yebeh.2020.107645.

Multivariate white matter alterations are associated with epilepsy duration.

Owen T, de Tisi J, Vos S, Winston G, Duncan J, Wang Y Eur J Neurosci. 2020; 53(8):2788-2803.

PMID: 33222308 PMC: 8246988. DOI: 10.1111/ejn.15055.

References

Coan A, Campos B, Yasuda C, Kubota B, Bergo F, Guerreiro C . Frequent seizures are associated with a network of gray matter atrophy in temporal lobe epilepsy with or without hippocampal sclerosis. PLoS One. 2014; 9(1):e85843. PMC: 3903486. DOI: 10.1371/journal.pone.0085843. View

Smith S, Jenkinson M, Woolrich M, Beckmann C, Behrens T, Johansen-Berg H . Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage. 2004; 23 Suppl 1:S208-19. DOI: 10.1016/j.neuroimage.2004.07.051. View

Liu R, Lemieux L, Bell G, Sisodiya S, Bartlett P, Shorvon S . Cerebral damage in epilepsy: a population-based longitudinal quantitative MRI study. Epilepsia. 2005; 46(9):1482-94. DOI: 10.1111/j.1528-1167.2005.51603.x. View

Bernhardt B, Worsley K, Kim H, Evans A, Bernasconi A, Bernasconi N . Longitudinal and cross-sectional analysis of atrophy in pharmacoresistant temporal lobe epilepsy. Neurology. 2009; 72(20):1747-54. PMC: 2827310. DOI: 10.1212/01.wnl.0000345969.57574.f5. View

Liu Z, Xu Y, An J, Wang J, Yin X, Huang R . Altered Brain White Matter Integrity in Temporal Lobe Epilepsy: A TBSS Study. J Neuroimaging. 2014; 25(3):460-4. DOI: 10.1111/jon.12154. View

Ercan K, Gunbey H, Bilir E, Zan E, Arslan H . Comparative Lateralizing Ability of Multimodality MRI in Temporal Lobe Epilepsy. Dis Markers. 2016; 2016:5923243. PMC: 5126436. DOI: 10.1155/2016/5923243. View

Oguz K, Tezer I, Sanverdi E, Has A, Bilginer B, Dolgun A . Effect of patient sex on white matter alterations in unilateral medial temporal lobe epilepsy with hippocampal sclerosis assessed by diffusion tensor imaging. AJNR Am J Neuroradiol. 2012; 34(5):1010-5. PMC: 7964661. DOI: 10.3174/ajnr.A3328. View

Williamson P, French J, Thadani V, Kim J, Novelly R, Spencer S . Characteristics of medial temporal lobe epilepsy: II. Interictal and ictal scalp electroencephalography, neuropsychological testing, neuroimaging, surgical results, and pathology. Ann Neurol. 1993; 34(6):781-7. DOI: 10.1002/ana.410340605. View

Concha L, Gross D, Wheatley B, Beaulieu C . Diffusion tensor imaging of time-dependent axonal and myelin degradation after corpus callosotomy in epilepsy patients. Neuroimage. 2006; 32(3):1090-9. DOI: 10.1016/j.neuroimage.2006.04.187. View

10.

Sen P, Basser P . A model for diffusion in white matter in the brain. Biophys J. 2005; 89(5):2927-38. PMC: 1366791. DOI: 10.1529/biophysj.105.063016. View

11.

Labate A, Cherubini A, Tripepi G, Mumoli L, Ferlazzo E, Aguglia U . White matter abnormalities differentiate severe from benign temporal lobe epilepsy. Epilepsia. 2015; 56(7):1109-16. DOI: 10.1111/epi.13027. View

12.

Riley J, Franklin D, Choi V, Kim R, Binder D, Cramer S . Altered white matter integrity in temporal lobe epilepsy: association with cognitive and clinical profiles. Epilepsia. 2010; 51(4):536-45. PMC: 2929974. DOI: 10.1111/j.1528-1167.2009.02508.x. View

13.

Thomalla G, Glauche V, Koch M, Beaulieu C, Weiller C, Rother J . Diffusion tensor imaging detects early Wallerian degeneration of the pyramidal tract after ischemic stroke. Neuroimage. 2004; 22(4):1767-74. DOI: 10.1016/j.neuroimage.2004.03.041. View

14.

Concha L, Kim H, Bernasconi A, Bernhardt B, Bernasconi N . Spatial patterns of water diffusion along white matter tracts in temporal lobe epilepsy. Neurology. 2012; 79(5):455-62. PMC: 3405250. DOI: 10.1212/WNL.0b013e31826170b6. View

15.

Smith S, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols T, Mackay C . Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage. 2006; 31(4):1487-505. DOI: 10.1016/j.neuroimage.2006.02.024. View

16.

Keller S, Schoene-Bake J, Gerdes J, Weber B, Deppe M . Concomitant fractional anisotropy and volumetric abnormalities in temporal lobe epilepsy: cross-sectional evidence for progressive neurologic injury. PLoS One. 2012; 7(10):e46791. PMC: 3469561. DOI: 10.1371/journal.pone.0046791. View

17.

Scanlon C, Mueller S, Cheong I, Hartig M, Weiner M, Laxer K . Grey and white matter abnormalities in temporal lobe epilepsy with and without mesial temporal sclerosis. J Neurol. 2013; 260(9):2320-9. PMC: 3845492. DOI: 10.1007/s00415-013-6974-3. View

18.

Otte W, van Eijsden P, Sander J, Duncan J, Dijkhuizen R, Braun K . A meta-analysis of white matter changes in temporal lobe epilepsy as studied with diffusion tensor imaging. Epilepsia. 2012; 53(4):659-67. DOI: 10.1111/j.1528-1167.2012.03426.x. View

19.

Chiang S, Levin H, Wilde E, Haneef Z . White matter structural connectivity changes correlate with epilepsy duration in temporal lobe epilepsy. Epilepsy Res. 2015; 120:37-46. PMC: 4740226. DOI: 10.1016/j.eplepsyres.2015.12.002. View

20.

Didato G, Chiesa V, Villani F, Pelliccia V, Deleo F, Gozzo F . Bitemporal epilepsy: A specific anatomo-electro-clinical phenotype in the temporal lobe epilepsy spectrum. Seizure. 2015; 31:112-9. DOI: 10.1016/j.seizure.2015.07.013. View