White Matter and Subcortical Gray Matter Microstructural Integrity in Mesial Temporal Lobe Epilepsy: A Combined Diffusion Tensor and Kurtosis Imaging Study
-
Hossein Sanjari Moghaddam
,
Roya Sharifpour
,
Amir Hossein Rasouli
,
Neda Mohammadi Mobarakeh
,
Sohrab Hashemi-Fesharaki
,
Jafar Mehvari Habibabadi
,
Mohmmad-Reza Nazem-Zadeh
Abstract
Purpose: The present study aimed to assess structural asymmetry in patients with mesial Temporal Lobe Epilepsy (mTLE) in the diffusion properties of brain white matter and subcortical gray matter tracts using Diffusion Tensor Imaging (DTI) and Diffusion Kurtosis Imaging (DKI). We considered a lower order DTI measure, Fractional Anisotropy (FA), and a higher-order DKI measure, Kurtosis Anisotropy (KA), as quantitative measures of the white matter diffusion properties in facing mTLE. We also made a comparison between these two measures in terms of the sensitivity to capture microstructural changes in concordance with TLE.
Materials and Methods: Thirty-two subjects with mTLE participated in this study. All the cases underwent multi-shell diffusion MRI acquisition. The subjects were grouped according to their epileptogenic side of the brain (19 Left-sided and 13 Right-sided TLE). Each group were analyzed separately using FSL package, then laterality analysis based on Tract-Based Spatial Statistics (TBSS) was performed on FA and KA images. After each analysis the left side of the patients’ brain was flipped and subtracted from the right side of the patients’s brain, and a voxel-wise z-score comparison was applied to find the significantly different areas.
Results: The results showed a considerable laterality effect on the temporal lobe white matters both in FA and KA, more emphasized in patients with Right-sided mTLE.
Conclusion: It can be concluded that these two measures, even though extracted from skeletonized images, can serve as decent biomarkers of laterality in case of mTLE, when the conventional MRI fails to capture the laterality.
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35-A. Arab, A. Wojna-Pelczar, A. Khairnar, N. Szabo, and J. Ruda-Kucerova, "Principles of diffusion kurtosis imaging and its role in early diagnosis of neurodegenerative disorders," (in eng), Brain Res Bull, vol. 139, pp. 91-98, May 2018.
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43-X. Yin et al., "Inferior frontal white matter asymmetry correlates with executive control of attention," (in eng), Hum Brain Mapp, vol. 34, no. 4, pp. 796-813, Apr 2013.
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45-J. H. Jensen and J. A. Helpern, "MRI quantification of non-Gaussian water diffusion by kurtosis analysis," vol. 23, no. 7, pp. 698-710, 2010.
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49-S. Jbabdi, T. E. Behrens, and S. M. Smith, "Crossing fibres in tract-based spatial statistics," (in eng), Neuroimage, vol. 49, no. 1, pp. 249-56, Jan 1 2010.
50-S. B. Vos, D. K. Jones, B. Jeurissen, M. A. Viergever, and A. Leemans, "The influence of complex white matter architecture on the mean diffusivity in diffusion tensor MRI of the human brain," (in eng), Neuroimage, vol. 59, no. 3, pp. 2208-16, Feb 1 2012.
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2-S. Ocklenburg, P. Friedrich, O. Gunturkun, and E. Genc, "Intrahemispheric white matter asymmetries: the missing link between brain structure and functional lateralization?," (in eng), Rev Neurosci, vol. 27, no. 5, pp. 465-80, Jul 1 2016.
3-H. Takao, N. Hayashi, and K. Ohtomo, "White matter asymmetry in healthy individuals: a diffusion tensor imaging study using tract-based spatial statistics," (in eng), Neuroscience, vol. 193, pp. 291-9, Oct 13 2011.
4-A. W. Toga and P. M. Thompson, "Mapping brain asymmetry," Nature Reviews Neuroscience, vol. 4, no. 1, pp. 37-48, 2003/01/01 2003.
5-J. Zhu et al., "Performances of diffusion kurtosis imaging and diffusion tensor imaging in detecting white matter abnormality in schizophrenia," (in eng), Neuroimage Clin, vol. 7, pp. 170-6, 2015.
6-R. A. Carper, J. M. Treiber, S. Y. DeJesus, and R. A. Muller, "Reduced Hemispheric Asymmetry of White Matter Microstructure in Autism Spectrum Disorder," (in eng), J Am Acad Child Adolesc Psychiatry, vol. 55, no. 12, pp. 1073-1080, Dec 2016.
7-H. Sanjari Moghaddam, F. Rahmani, M. H. Aarabi, M. R. Nazem-Zadeh, E. Davoodi-Bojd, and H. Soltanian-Zadeh, "White matter microstructural differences between right and left mesial temporal lobe epilepsy," (in eng), Acta Neurol Belg, Jan 11 2019.
8-M. E. Ahmadi et al., "Side matters: diffusion tensor imaging tractography in left and right temporal lobe epilepsy," (in eng), AJNR Am J Neuroradiol, vol. 30, no. 9, pp. 1740-7, Oct 2009.
9-P. Besson et al., "Structural connectivity differences in left and right temporal lobe epilepsy," (in eng), Neuroimage, vol. 100, pp. 135-44, Oct 15 2014.
10-H. J. Jo et al., "Relationship Between Seizure Frequency and Functional Abnormalities in Limbic Network of Medial Temporal Lobe Epilepsy," (in English), Original Research vol. 10, no. 488, 2019-May-08 2019.
11-A. Lemkaddem et al., "Connectivity and tissue microstructural alterations in right and left temporal lobe epilepsy revealed by diffusion spectrum imaging," NeuroImage: Clinical, vol. 5, pp. 349-358, 2014/01/01/ 2014.
12-J. Engel, Jr., "Introduction to temporal lobe epilepsy," (in eng), Epilepsy Res, vol. 26, no. 1, pp. 141-50, Dec 1996.
13-M. Catani, R. J. Howard, S. Pajevic, and D. K. Jones, "Virtual in vivo interactive dissection of white matter fasciculi in the human brain," (in eng), Neuroimage, vol. 17, no. 1, pp. 77-94, Sep 2002.
14-S. Mori et al., "Imaging cortical association tracts in the human brain using diffusion-tensor-based axonal tracking," (in eng), Magn Reson Med, vol. 47, no. 2, pp. 215-23, Feb 2002.
15-M.-R. Nazem-Zadeh et al., "DTI-based Response-Driven Modeling of mTLE Laterality " NeuroImage Clinical, 2015.
16-M. R. Nazem-Zadeh, J. M. Schwalb, K. V. Elisevich, H. Bagher-Ebadian, and H. Soltanian-Zadeh, "Lateralization of Temporal Lobe Epilepsy using a Novel Uncertainty Analysis of MR Diffusion in Hippocampus, Cingulum, and Fornix, and Hippocampal Volume and FLAIR Intensity," presented at the Gordon Research Conference on Mechanisms of Epilepsy & Neural Synchronization, West Dover, VT, USA, 2014.
17-M. R. Nazem-Zadeh, J. M. Schwalb, K. V. Elisevich, H. Bagher-Ebadian, and H. Soltanian-Zadeh, "Lateralization of Temporal Lobe Epilepsy by Analysis of Asymmetric Fractional Anisotropy in the Cingulum," presented at the 67th Annual Meeting of the American Epilepsy Society (AES), Washington, DC, USA, 2013.
18-P. J. Basser and D. K. Jones, "Diffusion-tensor MRI: theory, experimental design and data analysis - a technical review," (in eng), NMR Biomed, vol. 15, no. 7-8, pp. 456-67, Nov-Dec 2002.
19-D. S. Tuch, T. G. Reese, M. R. Wiegell, and V. J. Wedeen, "Diffusion MRI of complex neural architecture," (in eng), Neuron, vol. 40, no. 5, pp. 885-95, Dec 4 2003.
20-E. S. Hui, M. M. Cheung, L. Qi, and E. X. Wu, "Towards better MR characterization of neural tissues using directional diffusion kurtosis analysis," (in eng), Neuroimage, vol. 42, no. 1, pp. 122-34, Aug 1 2008.
21-H. Lu, J. H. Jensen, A. Ramani, and J. A. Helpern, "Three-dimensional characterization of non-gaussian water diffusion in humans using diffusion kurtosis imaging," (in eng), NMR Biomed, vol. 19, no. 2, pp. 236-47, Apr 2006.
22-V. Adisetiyo et al., "Attention-deficit/hyperactivity disorder without comorbidity is associated with distinct atypical patterns of cerebral microstructural development," (in eng), Hum Brain Mapp, vol. 35, no. 5, pp. 2148-62, May 2014.
23-I. Blockx et al., "Identification and characterization of Huntington related pathology: an in vivo DKI imaging study," (in eng), Neuroimage, vol. 63, no. 2, pp. 653-62, Nov 1 2012.
24-M. F. Falangola et al., "Age-related non-Gaussian diffusion patterns in the prefrontal brain," (in eng), J Magn Reson Imaging, vol. 28, no. 6, pp. 1345-50, Dec 2008.
25-E. J. Grossman et al., "Thalamus and cognitive impairment in mild traumatic brain injury: a diffusional kurtosis imaging study," (in eng), J Neurotrauma, vol. 29, no. 13, pp. 2318-27, Sep 2012.
26-S. Van Cauter et al., "Gliomas: diffusion kurtosis MR imaging in grading," (in eng), Radiology, vol. 263, no. 2, pp. 492-501, May 2012.
27-S. M. Smith et al., "Advances in functional and structural MR image analysis and implementation as FSL," Neuroimage, vol. 23, pp. S208-S219, 2004.
28-C. H. Chapman, M. R. Nazem-Zadeh, T. S. Lawrence, C. I. Tsien, and Y. Cao, "Regional variation in white matter diffusion index changes following chemoradiotherapy: A prospective study using tract-based spatial statistics," Submitted to PLOS ONE, 2012.
29-S. M. Smith et al., "Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data," Neuroimage, vol. 31, no. 4, pp. 1487-1505, 2006.
30-A. Ashraf-Ganjouei et al., "White matter correlates of disease duration in patients with temporal lobe epilepsy: updated review of literature," Neurological Sciences, vol. 40, no. 6, pp. 1209-1216, 2019/06/01 2019.
31-B. M. de Campos, A. C. Coan, C. Lin Yasuda, R. F. Casseb, and F. Cendes, "Large-scale brain networks are distinctly affected in right and left mesial temporal lobe epilepsy," (in eng), Hum Brain Mapp, vol. 37, no. 9, pp. 3137-52, Sep 2016.
32-Z. Haneef, A. Lenartowicz, H. J. Yeh, H. S. Levin, J. Engel, Jr., and J. M. Stern, "Functional connectivity of hippocampal networks in temporal lobe epilepsy," (in eng), Epilepsia, vol. 55, no. 1, pp. 137-45, Jan 2014.
33-F. R. Pereira et al., "Asymmetrical hippocampal connectivity in mesial temporal lobe epilepsy: evidence from resting state fMRI," (in eng), BMC Neurosci, vol. 11, p. 66, Jun 2 2010.
34-X. Zhao et al., "Reduced Interhemispheric White Matter Asymmetries in Medial Temporal Lobe Epilepsy With Hippocampal Sclerosis," (in English), Original Research vol. 10, no. 394, 2019-April-24 2019.
35-A. Arab, A. Wojna-Pelczar, A. Khairnar, N. Szabo, and J. Ruda-Kucerova, "Principles of diffusion kurtosis imaging and its role in early diagnosis of neurodegenerative disorders," (in eng), Brain Res Bull, vol. 139, pp. 91-98, May 2018.
36-N. Kemmotsu et al., "MRI analysis in temporal lobe epilepsy: cortical thinning and white matter disruptions are related to side of seizure onset," (in eng), Epilepsia, vol. 52, no. 12, pp. 2257-66, Dec 2011.
37-W. M. Otte, P. van Eijsden, J. W. Sander, J. S. Duncan, R. M. Dijkhuizen, and K. P. Braun, "A meta-analysis of white matter changes in temporal lobe epilepsy as studied with diffusion tensor imaging," (in eng), Epilepsia, vol. 53, no. 4, pp. 659-67, Apr 2012.
38-M. Pail, M. Brazdil, R. Marecek, and M. Mikl, "An optimized voxel-based morphometric study of gray matter changes in patients with left-sided and right-sided mesial temporal lobe epilepsy and hippocampal sclerosis (MTLE/HS)," (in eng), Epilepsia, vol. 51, no. 4, pp. 511-8, Apr 2010.
39-N. L. Voets, C. F. Beckmann, D. M. Cole, S. Hong, A. Bernasconi, and N. Bernasconi, "Structural substrates for resting network disruption in temporal lobe epilepsy," (in eng), Brain, vol. 135, no. Pt 8, pp. 2350-7, Aug 2012.
40-V. Duboc, P. Dufourcq, P. Blader, and M. Roussigne, "Asymmetry of the Brain: Development and Implications," (in eng), Annu Rev Genet, vol. 49, pp. 647-72, 2015.
41-S. J. Gotts, H. J. Jo, G. L. Wallace, Z. S. Saad, R. W. Cox, and A. Martin, "Two distinct forms of functional lateralization in the human brain," (in eng), Proc Natl Acad Sci U S A, vol. 110, no. 36, pp. E3435-44, Sep 3 2013.
42-A. W. Toga and P. M. Thompson, "Mapping brain asymmetry," (in eng), Nat Rev Neurosci, vol. 4, no. 1, pp. 37-48, Jan 2003.
43-X. Yin et al., "Inferior frontal white matter asymmetry correlates with executive control of attention," (in eng), Hum Brain Mapp, vol. 34, no. 4, pp. 796-813, Apr 2013.
44-W. Cao et al., "Abnormal asymmetry in benign epilepsy with unilateral and bilateral centrotemporal spikes: A combined fMRI and DTI study," (in eng), Epilepsy Res, vol. 135, pp. 56-63, Sep 2017.
45-J. H. Jensen and J. A. Helpern, "MRI quantification of non-Gaussian water diffusion by kurtosis analysis," vol. 23, no. 7, pp. 698-710, 2010.
46-J. H. Jensen, J. A. Helpern, A. Ramani, H. Lu, and K. Kaczynski, "Diffusional kurtosis imaging: The quantification of non-gaussian water diffusion by means of magnetic resonance imaging," vol. 53, no. 6, pp. 1432-1440, 2005.
47-A. J. Steven, J. Zhuo, and E. R. Melhem, "Diffusion kurtosis imaging: an emerging technique for evaluating the microstructural environment of the brain," (in eng), AJR Am J Roentgenol, vol. 202, no. 1, pp. W26-33, Jan 2014.
48-G. Douaud et al., "DTI measures in crossing-fibre areas: increased diffusion anisotropy reveals early white matter alteration in MCI and mild Alzheimer's disease," (in eng), Neuroimage, vol. 55, no. 3, pp. 880-90, Apr 1 2011.
49-S. Jbabdi, T. E. Behrens, and S. M. Smith, "Crossing fibres in tract-based spatial statistics," (in eng), Neuroimage, vol. 49, no. 1, pp. 249-56, Jan 1 2010.
50-S. B. Vos, D. K. Jones, B. Jeurissen, M. A. Viergever, and A. Leemans, "The influence of complex white matter architecture on the mean diffusivity in diffusion tensor MRI of the human brain," (in eng), Neuroimage, vol. 59, no. 3, pp. 2208-16, Feb 1 2012.
51-M. Lazar, J. H. Jensen, L. Xuan, and J. A. Helpern, "Estimation of the orientation distribution function from diffusional kurtosis imaging," (in eng), Magn Reson Med, vol. 60, no. 4, pp. 774-81, Oct 2008.
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| Issue | Vol 7 No 1 (2020) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/fbt.v7i1.2724 | |
| Keywords | ||
| Microstructural Integrity Mesial Temporal Lobe Epilepsy Laterality Seizure Zone Epileptogenic Side Diffusion Tensor Imaging Diffusion Kurtosis Imaging | ||
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How to Cite
1.
Sanjari Moghaddam H, Sharifpour R, Rasouli AH, Mohammadi Mobarakeh N, Hashemi-Fesharaki S, Mehvari Habibabadi J, Nazem-Zadeh M-R. White Matter and Subcortical Gray Matter Microstructural Integrity in Mesial Temporal Lobe Epilepsy: A Combined Diffusion Tensor and Kurtosis Imaging Study. Frontiers Biomed Technol. 2020;7(1):41-51.
