Cognitive decline and white matter changes in mesial temporal lobe epilepsy

Shang-Wen Xu, Ji-Hui Xi, Chen Lin, Xiao-Yang Wang, Li-Yuan Fu, Stephen Francis Kralik, Zi-Qian Chen, Shang-Wen Xu, Ji-Hui Xi, Chen Lin, Xiao-Yang Wang, Li-Yuan Fu, Stephen Francis Kralik, Zi-Qian Chen

Abstract

Noninvasive imaging plays a pivotal role in assessing the brain structural and functional changes in presurgical mesial temporal lobe epilepsy (MTLE) patients. Our goal was to study the relationship between the changes of cerebral white matter (WM) and cognitive functions in MTLE patients.Voxel-based morphometry (VBM) and tract-based spatial statistics (TBSS) MRI were performed on 24 right-handed MTLE patients (12 with left MTLE and 12 with right MTLE) and 12 matching healthy controls. Gray matter (GM), WM, and whole brain (WB) volumes were measured with VBM while fractional anisotropy (FA), mean diffusivity (MD), axial diffusivity (AD), and radial diffusivity (RD) were measured with TBSS. All patients and controls also underwent Montreal Cognitive Assessment (MoCA) before MRI.WM volume and the ratio of WM volume versus WB volume were significantly lower in MTLE patients compared with controls. WM volume in MTLE patients had a positive correlation with MoCA score (r = 0.71, P < .001) and a negative correlation with the duration of epilepsy (r = -0.693, P < .001). Volumetric differences were mainly located in the corpus callosum, uncinate fasciculus, inferior longitudinal fasciculus, and superior longitudinal fasciculus. FA of both left MTLE and right MTLE groups was significantly decreased, while MD, AD, and RD were significantly increased. Most left MTLE patients showed bilateral WM fiber tract changes versus ipsilateral changes for right MTLE patients.Changes in DTI parameters and WM volume were found in MTLE patients and more ipsilateral changes were seen with right-sided MTLE. Cognitive changes of MTLE patients were found to be correlated with the changes in WM structure. These findings not only provide useful information for lateralization of the seizure focus but can also be used to explain functional connectivity disorders which may be an important physiological basis for cognitive changes in patients with MTLE.

Conflict of interest statement

The authors have no conflicts of interest to disclose.

Figures

Figure 1
Figure 1
Scatter plot of white matter volume versus MoCA score. MoCA = Montreal Cognitive Assessment.
Figure 2
Figure 2
Scatter plot of WM volume versus the duration of epilepsy. WM = white matter.
Figure 3
Figure 3
Maps of statistical difference of FA values. The 2 maps show significant lower FA values that are marked in red-yellow for the comparison between the LMTLE and the control groups (left), and between the RMTLE and the control groups (right). The white matter fiber skeleton is marked in green and the brighter areas in the color scale represent greater difference. FA = fractional anisotropy, LMTLE = left mesial temporal lobe epilepsy, LMTLE = left mesial temporal lobe epilepsy.

References

    1. Liu M, Bernhardt BC, Hong S-J, et al. The superficial white matter in temporal lobe epilepsy: a key link between structural and functional network disruptions. Brain 2016;139:2431–40.
    1. Liao W, Zhang Z, Pan Z, et al. Default mode network abnormalities in mesial temporal lobe epilepsy: a study combining fMRI and DTI. Hum Brain Mapp 2011;32:883–95.
    1. Yu A, Li K, Li L, et al. Whole-brain voxel-based morphometry of white matter in medial temporal lobe epilepsy. Eur J Radiol 2008;65:86–90.
    1. Khan AR, Goubran M, de Ribaupierre S, et al. Quantitative relaxometry and diffusion MRI for lateralization in MTS and non-MTS temporal lobe epilepsy. Epilepsy Res 2014;108:506–16.
    1. Correa DG, Ventura N, Zimmermann N, et al. Evaluation of deep gray matter volume, cortical thickness and white matter integrity in patients with typical absence epilepsy: a study using voxelwise-based techniques. Neuroradiology 2017;59:237–45.
    1. Li J, Chen X, Ye W, et al. Alteration of the alertness-related network in patients with right temporal lobe epilepsy: A resting state fMRI study. Epilepsy Res 2016;127:252–9.
    1. Toller G, Adhimoolam B, Rankin KP, et al. Right fronto-limbic atrophy is associated with reduced empathy in refractory unilateral mesial temporal lobe epilepsy. Neuropsychologia 2015;78:80–7.
    1. Liu F, Wang Y, Li M, et al. Dynamic functional network connectivity in idiopathic generalized epilepsy with generalized tonic-clonic seizure. Hum Brain Mapp 2017;38:957–73.
    1. Otte WM, van Eijsden P, Sander JW, et al. A meta-analysis of white matter changes in temporal lobe epilepsy as studied with diffusion tensor imaging. Epilepsia 2012;53:659–67.
    1. Govindan RM, Makki MI, Sundaram SK, et al. Diffusion tensor analysis of temporal and extra-temporal lobe tracts in temporal lobe epilepsy. Epilepsy Res 2008;80:30–41.
    1. Coan AC, Campos BM, Beltramini GC, et al. Distinct functional and structural MRI abnormalities in mesial temporal lobe epilepsy with and without hippocampal sclerosis. Epilepsia 2014;55:1187–96.
    1. Ashburner J, Friston KJ. Voxel-based morphometry—the methods. Neuroimage 2000;11:805–21.
    1. Son JH, Han DH, Min KJ, et al. Correlation between gray matter volume in the temporal lobe and depressive symptoms in patients with Alzheimer's disease. Neurosci Lett 2013;548:15–20.
    1. Valfre W, Rainero I, Bergui M, et al. Voxel-based morphometry reveals gray matter abnormalities in migraine. Headache 2008;48:109–17.
    1. Lu C, Peng D, Chen C, et al. Altered effective connectivity and anomalous anatomy in the basal ganglia-thalamocortical circuit of stuttering speakers. Cortex 2010;46:49–67.
    1. Ecker C, Rocha-Rego V, Johnston P, et al. Investigating the predictive value of whole-brain structural MR scans in autism: a pattern classification approach. Neuroimage 2010;49:44–56.
    1. Liu F, Guo W, Yu D, et al. Classification of different therapeutic responses of major depressive disorder with multivariate pattern analysis method based on structural MR scans. PLoS One 2012;7:e40968.
    1. Edden RA, Jones DK. Spatial and orientational heterogeneity in the statistical sensitivity of skeleton-based analyses of diffusion tensor MR imaging data. J Neurosci Methods 2011;201:213–9.
    1. Chen Z, Ni P, Zhang J, et al. Evaluating ischemic stroke with diffusion tensor imaging. Neurol Res 2008;30:720–6.
    1. Li H, Xue Z, Dulay MF, et al. Fractional anisotropy asymmetry and the side of seizure origin for partial onset-temporal lobe epilepsy. Comput Med Imaging Graph 2014;38:481–9.
    1. Canu E, Agosta F, Spinelli EG, et al. White matter microstructural damage in Alzheimer's disease at different ages of onset. Neurobiol Aging 2013;34:2331–40.
    1. Shu N, Wang Z, Qi Z, et al. Multiple diffusion indices reveals white matter degeneration in Alzheimer's disease and mild cognitive impairment: a tract-based spatial statistics study. J Alzheimer's Dis 2011;26:275–85.
    1. Lieberman G, Shpaner M, Watts R, et al. White matter involvement in chronic musculoskeletal pain. J Pain 2014;15:1110–9.
    1. Nickl-Jockschat T, Stocker T, Markov V, et al. The impact of a Dysbindin schizophrenia susceptibility variant on fiber tract integrity in healthy individuals: a TBSS-based diffusion tensor imaging study. Neuroimage 2012;60:847–53.
    1. Liu X, Lai Y, Wang X, et al. Reduced white matter integrity and cognitive deficit in never-medicated chronic schizophrenia: a diffusion tensor study using TBSS. Behav Brain Res 2013;252:157–63.
    1. Guo W, Liu F, Liu Z, et al. Right lateralized white matter abnormalities in first-episode, drug-naive paranoid schizophrenia. Neurosci Lett 2012;531:5–9.
    1. Smith SM, Jenkinson M, Johansen-Berg H, et al. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 2006;31:1487–505.
    1. Afzali M, Soltanian-Zadeh H, Elisevich KV. Tract based spatial statistical analysis and voxel based morphometry of diffusion indices in temporal lobe epilepsy. Comput Biol Med 2011;41:1082–91.
    1. Liacu D, Idy-Peretti I, Ducreux D, et al. Diffusion tensor imaging tractography parameters of limbic system bundles in temporal lobe epilepsy patients. J Magn Reson Imaging 2012;36:561–8.
    1. Arfanakis K, Hermann BP, Rogers BP, et al. Diffusion tensor MRI in temporal lobe epilepsy. Magn Reson Imaging 2002;20:511–9.
    1. Gross DW, Concha L, Beaulieu C. Extratemporal white matter abnormalities in mesial temporal lobe epilepsy demonstrated with diffusion tensor imaging. Epilepsia 2006;47:1360–3.
    1. Engel J. Surgery for seizures. N Engl J Med 1996;334:647–53.
    1. van Bloemendaal L, Ijzerman RG, Ten Kulve JS, et al. Alterations in white matter volume and integrity in obesity and type 2 diabetes. Metab Brain Dis 2016;31:621–9.
    1. Purkayastha S, Fadar O, Mehregan A, et al. Impaired cerebrovascular hemodynamics are associated with cerebral white matter damage. J Cereb Blood Flow Metab 2014;34:228–34.
    1. Nasreddine ZS, Phillips NA, Bédirian Vr, et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 2005;53:695–9.
    1. Stejskal EO, Tanner JE. Self-diffusion measurement: spin-echo in presence of time dependent field gradient. J Chem Phys 1965;42:288–92.
    1. Ahmadi ME, Hagler DJ, Jr, McDonald CR, et al. Side matters: diffusion tensor imaging tractography in left and right temporal lobe epilepsy. AJNR Am J Neuroradiol 2009;30:1740–7.
    1. Besson P, Dinkelacker V, Valabregue R, et al. Structural connectivity differences in left and right temporal lobe epilepsy. NeuroImage 2014;100:135–44.
    1. Hofer S, Frahm J. Topography of the human corpus callosum revisited–comprehensive fiber tractography using diffusion tensor magnetic resonance imaging. NeuroImage 2006;32:989–94.
    1. Diehl B, Busch RM, Duncan JS, et al. Abnormalities in diffusion tensor imaging of the uncinate fasciculus relate to reduced memory in temporal lobe epilepsy. Epilepsia 2008;49:1409–18.
    1. Diao L, Yu H, Zheng J, et al. Abnormalities of the uncinate fasciculus correlate with executive dysfunction in patients with left temporal lobe epilepsy. Magn Reson Imaging 2015;33:544–50.
    1. Li Z, Chen Z. Research progress in the fMRI imaging of ognitive impairment of temporal lobe epilepsy. Med Recapitulate 2013;19:1622–4.
    1. Smith ML, Elliott IM, Lach L. Cognitive skills in children with intractable epilepsy: comparison of surgical and nonsurgical candidates. Epilepsia 2002;43:631–7.
    1. Hermann B, Seidenberg M, Bell B, et al. The neurodevelopmental impact of childhood-onset temporal lobe epilepsy on brain structure and function. Epilepsia 2002;43:1062–71.
    1. Stricker NH, Schweinsburg BC, Delano-Wood L, et al. Decreased white matter integrity in late-myelinating fiber pathways in Alzheimer's disease supports retrogenesis. Neuroimage 2009;45:10–6.
    1. Meador KJ. Cognitive outcomes and predictive factors in epilepsy. Neurology 2002;58:s21–6.
    1. Riley JD, Franklin DL, Choi V, et al. Altered white matter integrity in temporal lobe epilepsy: association with cognitive and clinical profiles. Epilepsia 2010;51:536–45.

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