The changes of white matter diffusion tensor in MRI negative epilepsy comorbid sleep disorder evaluated by tract-based spatial statistics_Journal of Epilepsy

Authors：

ZHENG Qing ¹ , WANG Fuli ² , GUO Qi ² , SUN Haogang ² ,  LIU Songyan ²

1. Department of Neurology, Xiaogan Central Hospital, Xiaogan 432099, China;
2. Department of Neurology, China-Japan Union Hospital of Jilin University, Changchun 130033, China;

Corresponding author：

LIU Songyan, Email: liu_sy@jlu.edu.cn

Keywords：

Epilepsy comorbid with sleep disorders; Diffusion tensor image; Brain network structure; Tract-based spatial statistics

DOI：

10.7507/2096-0247.202410012

Video：

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Objective To investigate the pathological mechanism of epileptic comorbid sleep disorder by analyzing the changes of cerebral white matter diffusion tensor in patients with sleep disorder with negative magnetic resonance imaging (MRI) epilepsy based on the method of tract-based spatial statistics (TBSS). Methods MRI negative epilepsy patients comorbid sleep disorder who were epileptic patients treated l in China-Japan Union Hospital of Jilin University from January 2020 to December 2022 completed the Epworth sleepiness scale (ESS) and Pittsburgh sleep quality index (PSQI) tests, and those who complained of sleep disorder and PSQI index ≥11 were monitored by nighttime polysomnography (PSG) and those with objective sleep disorder confirmed by PSG were included in the epilepsy comorbid sleep disorder group. Healthy volunteers with matching gender, age, education were included in the health control group. Diffusion tensor image ( DTI) was collected for all subjects by using a 3.0T magnetic resonance scanner. Diffusion parameters were compared between the two groups using TBSS. Results This study included 36 epilepsy patients comorbid sleep disorder and 35 healthy volunteers. epilepsy patients comorbid sleep disorder showed significantly lower fraction anisotropy (FA) (P<0.05) and significantly higher mean diffusivity (MD) (P<0.05) than the health control group . Brain regions with statistical differences in FA reduction included middle peduncle of cerebellum, genu of corpus callosum, body of corpus callosum, splenium of corpus callosum, anterior corona radiata, external capsule and right posterior thalamic radiation.Brain regions with statistical differences in MD degradation included genu of corpus callosum, body of corpus callosum, anterior limb of internal capsule, anterior corona radiata, superior corona radiata, external capsule and right posterior limb of internal capsul. Conclusion Patients with epilepsy comorbidities with sleep disorders have widespread and symmetric white matter damage.The white matter damage is concentrated in the front of the brain.

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7.	Peng SJ, Harnod T, Tsai JZ, et al. Evaluation of subcortical grey matter abnormalities in patients with MRI-negative cortical epilepsy determined through structural and tensor magnetic resonance imaging. BMC Neurology, 2014, 14: 104.
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14.	Yogarajah M, Focke NK, Bonelli S B, et al. The structural plasticity of white matter networks following anterior temporal lobe resection. Brain, 2010, 133(Pt 8): 2348-2364.
15.	Spiegelhalder K, Regen W, Prem M, et al. Reduced anterior internal capsule white matter integrity in primary insomnia. Human Brain Mapping, 2014, 35(7): 3431-3438.
16.	Li S, Tian J, Bauer A, et al. Reduced integrity of right lateralized white matter in patients with primary insomnia: a diffusion-tensor imaging study. Radiology, 2016, 280(2): 520-528.
17.	Altena E, Vrenken H, Van Der Werf YD, et al. Reduced orbitofrontal and parietal gray matter in chronic insomnia: a voxel-based morphometric study. Biological Psychiatry, 2010, 67(2): 182-185.
18.	Stoffers D, Moens S, Benjamins J, et al. Orbitofrontal gray matter relates to early morning awakening: a neural correlate of insomnia complaints? Frontiers in Neurology, 2012, 3: 105.
19.	De Vivo L, Nelson AB, Bellesi M, et al. Loss of sleep affects the ultrastructure of pyramidal neurons in the adolescent mouse frontal cortex. Sleep, 2016, 39(4): 861-874.
20.	Uda T, Kunihiro N, Umaba R, et al. Surgical aspects of corpus callosotomy. Brain Sci, 2021, 11(12): 1608.
21.	Mattson RH. Overview: idiopathic generalized epilepsies. Epilepsia, 2003, 44(1): 2-6.
22.	Gorges M, Müller HP, Liepelt-Scarfone I, et al. Structural brain signature of cognitive decline in Parkinson's disease: DTI-based evidence from the LANDSCAPE study. Ther Adv Neurol Disord, 2019, 12: 1756286419843447.
23.	Rocklage M, Williams V, Pacheco J, et al. White matter differences predict cognitive vulnerability to sleep deprivation. Sleep, 2009, 32(8): 1100-1103.
24.	Vulliemoz S, Vollmar C, Koepp MJ, et al. Connectivity of the supplementary motor area in juvenile myoclonic epilepsy and frontal lobe epilepsy. Epilepsia, 2011, 52(3): 507-514.
25.	Sanjari Moghaddam H, Mohammadi E, Dolatshahi M, et al. White matter microstructural abnormalities in primary insomnia: a systematic review of diffusion tensor imaging studies. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 2021, 105: 110132.
26.	冯细梅. 基于MRI的睡眠相关癫痫的脑形态学及结构网络研究. 中南大学, 2023, 硕士学位论文.

1. 王艺霖, 张鸿. 癫痫躯体共患病的研究进展. 癫痫杂志, 2018, 4(4): 334-339.
2. Pereira AM, Bruni O, Ferri R, et al. The impact of epilepsy on sleep architecture during childhood. Epilepsia, 2012, 53(9): 1519-1525.
3. Bifftu BB, Dachew BA, Tiruneh BT, et al. Depression among people with epilepsy in Northwest Ethiopia: a cross-sectional institution based study. BMC Research Notes, 2015, 8: 585.
4. Khatami R, Zutter D, Siegel A, et al. Steep-wake habits and disorders in a series of 100 adult epilepsy patients - a prospective study. Seizure-European Journal of Epilepsy, 2006, 15(5): 299-306.
5. Im HJ, Park SH, Baek SH, et al. Associations of impaired sleep quality, insomnia, and sleepiness with epilepsy: a questionnaire-based case-control study. Epilepsy & Behavior, 2016, 57: 55-59.
6. Buratti L, Natanti A, Viticchi G, et al. Impact Impact of sleep disorders on the risk of seizure recurrence in juvenile myoclonic epilepsy. Epilepsy & Behavior, 2018, 80: 21-24.
7. Peng SJ, Harnod T, Tsai JZ, et al. Evaluation of subcortical grey matter abnormalities in patients with MRI-negative cortical epilepsy determined through structural and tensor magnetic resonance imaging. BMC Neurology, 2014, 14: 104.
8. Berg AT, Mathern GW, Bronen RA, et al. Frequency, prognosis and surgical treatment of structural abnormalities seen with magnetic resonance imaging in childhood epilepsy. Brain, 2009, 132: 2785-2797.
9. Spencer SS. Neural networks in human epilepsy: evidence of and implications for treatment. Epilepsia, 2002, 43(3): 219-227.
10. 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(6): 883-895.
11. Kim SE, Lee JH, Chung HK, et al. Alterations in white matter microstructures and cognitive dysfunctions in benign childhood epilepsy with centrotemporal spikes. European Journal of Neurology, 2014, 21(5): 708-717.
12. Focke NK, Yogarajah M, Bonelli S B, et al. Voxel-based diffusion tensor imaging in patients with mesial temporal lobe epilepsy and hippocampal sclerosis. Neuroimage, 2008, 40(2): 728-737.
13. Schoene-Bake JC, Faber J, Trautner P, et al. Widespread affections of large fiber tracts in postoperative temporal lobe epilepsy. Neuroimage, 2009, 46(3): 569-76.
14. Yogarajah M, Focke NK, Bonelli S B, et al. The structural plasticity of white matter networks following anterior temporal lobe resection. Brain, 2010, 133(Pt 8): 2348-2364.
15. Spiegelhalder K, Regen W, Prem M, et al. Reduced anterior internal capsule white matter integrity in primary insomnia. Human Brain Mapping, 2014, 35(7): 3431-3438.
16. Li S, Tian J, Bauer A, et al. Reduced integrity of right lateralized white matter in patients with primary insomnia: a diffusion-tensor imaging study. Radiology, 2016, 280(2): 520-528.
17. Altena E, Vrenken H, Van Der Werf YD, et al. Reduced orbitofrontal and parietal gray matter in chronic insomnia: a voxel-based morphometric study. Biological Psychiatry, 2010, 67(2): 182-185.
18. Stoffers D, Moens S, Benjamins J, et al. Orbitofrontal gray matter relates to early morning awakening: a neural correlate of insomnia complaints? Frontiers in Neurology, 2012, 3: 105.
19. De Vivo L, Nelson AB, Bellesi M, et al. Loss of sleep affects the ultrastructure of pyramidal neurons in the adolescent mouse frontal cortex. Sleep, 2016, 39(4): 861-874.
20. Uda T, Kunihiro N, Umaba R, et al. Surgical aspects of corpus callosotomy. Brain Sci, 2021, 11(12): 1608.
21. Mattson RH. Overview: idiopathic generalized epilepsies. Epilepsia, 2003, 44(1): 2-6.
22. Gorges M, Müller HP, Liepelt-Scarfone I, et al. Structural brain signature of cognitive decline in Parkinson's disease: DTI-based evidence from the LANDSCAPE study. Ther Adv Neurol Disord, 2019, 12: 1756286419843447.
23. Rocklage M, Williams V, Pacheco J, et al. White matter differences predict cognitive vulnerability to sleep deprivation. Sleep, 2009, 32(8): 1100-1103.
24. Vulliemoz S, Vollmar C, Koepp MJ, et al. Connectivity of the supplementary motor area in juvenile myoclonic epilepsy and frontal lobe epilepsy. Epilepsia, 2011, 52(3): 507-514.
25. Sanjari Moghaddam H, Mohammadi E, Dolatshahi M, et al. White matter microstructural abnormalities in primary insomnia: a systematic review of diffusion tensor imaging studies. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 2021, 105: 110132.
26. 冯细梅. 基于MRI的睡眠相关癫痫的脑形态学及结构网络研究. 中南大学, 2023, 硕士学位论文.

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