Yıl: 2023 Cilt: 53 Sayı: 6 Sayfa Aralığı: 1840 - 1851 Metin Dili: İngilizce DOI: 10.55730/1300-0144.5754 İndeks Tarihi: 18-01-2024

Microstructural evaluation of the brain with advanced magnetic resonance imaging techniques in cases of electrical status epilepticus during sleep (ESES)

Öz:
Background/aim: The cause and treatment of electrical status epilepticus during sleep (ESES), one of the epileptic encephalopathies of childhood, is unclear. The aim of this study was to evaluate possible microstructural abnormalities in the brain using advanced magnetic resonance imaging (MRI) techniques in ESES patients with and without genetic mutations. Materials and methods: This research comprised 12 ESES patients without structural thalamic lesions (6 with genetic abnormalities and 6 without) and 12 healthy children. Whole-exome sequencing was used for the genetic mutation analysis. Brain MRI data were evaluated using tractus-based spatial statistics, voxel-based morphometry, a local gyrification index, subcortical shape analysis, FreeSurfer volume, and cortical thickness. The data of the groups were compared. Results: The mean age in the control group was 9.05 ± 1.85 years, whereas that in the ESES group was 9.45 ± 2.72 years. Compared to the control group, the ESES patients showed higher mean thalamus diffusivity (p < 0.05). ESES patients with genetic mutations had lower axial diffusivity in the superior longitudinal fasciculus and gray matter volume in the entorhinal region, accumbens area, caudate, putamen, cerebral white matter, and outer cerebellar areas. The superior and middle temporal cortical thickness increased in the ESES patients. Conclusion: This study is important in terms of presenting the microstructural evaluation of the brain in ESES patients with advanced MRI analysis methods as well as comparing patients with and without genetic mutations. These findings may be associated with corticostriatal transmission, ictogenesis, epileptogenesis, neuropsychiatric symptoms, cognitive impairment, and cerebellar involvement in ESES. Expanded case-group studies may help to understand the physiology of the corticothalamic circuitry in its etiopathogenesis and develop secondary therapeutic targets for ESES.
Anahtar Kelime: Electrical status epilepticus during sleep microstructural analysis morphometry genetic mutation tractus-based spatial statistics

Belge Türü: Makale Makale Türü: Araştırma Makalesi Erişim Türü: Erişime Açık
  • 1. Sánchez Fernández I, Loddenkemper T, Peters JM, Kothare SV. Electrical status epilepticus in sleep: clinical presentation and pathophysiology. Pediatric Neurology 2012; 47 (6): 390-410. https://doi.org/10.1016/j.pediatrneurol.2012.06.016
  • 2. Wiwattanadittakul N, Depositario-Cabacar D, Zelleke TG. Electrical status epilepticus in sleep (ESES)- treatment pattern and EEG outcome in children with very high spike-wave index. Epilepsy and Behavior 2020; 105: 106965. https://doi. org/10.1016/j.yebeh.2020.106965
  • 3. Arican P, Gencpinar P, Olgac Dundar N, Tekgul H. Electrical status epilepticus during slow-wave sleep (ESES): current perspectives. Journal of Pediatric Neurosciences 2021; 16 (2): 91-96. https://doi.org/10.4103/jpn.JPN_137_20
  • 4. Kilic H, Yilmaz K, Asgarova P, Kizilkilic O, Hatay GH et al. Electrical status epilepticus in sleep: the role of thalamus in etiopathogenesis. Seizure 2021; 93: 44-50. https://doi. org/10.1016/j.seizure.2021.10.010
  • 5. Bernhardt BC, Worsley KJ, Besson P, Concha L, Lerch JP et al. Mapping limbic network organization in temporal lobe epilepsy using morphometric correlations: insights on the relation between mesiotemporal connectivity and cortical atrophy. Neuroimage 2008; 42 (2): 515-524. https://doi.org/10.1016/j. Neuroimage.2008.04.261
  • 6. Han P, Stiller-Stut FP, Fjaeldstad A, Hummel T. Greater hippocampal gray matter volume in subjective hyperosmia: a voxel-based morphometry study. Scientific Reports 2020; 10 (1): 18869. https://doi.org/10.1038/s41598-020-75898-6
  • 7. Li M, Yan J, Wen H, Lin J, Liang L et al. Cortical thickness, gyrification and sulcal depth in trigeminal neuralgia. Scientific Reports 2021; 11 (1): 16322. https://doi.org/10.1038/s41598- 021-95811-z
  • 8. Saini J, Sinha S, Bagepally BS, Ramchandraiah CT, Thennarasu K et al. Subcortical structural abnormalities in juvenile myoclonic epilepsy (JME): MR volumetry and vertex based analysis. Seizure 2013; 22 (3): 230-235.https://doi.org/10.1016/j. seizure.2013.01.001
  • 9. Dahnke R, Yotter RA, Gaser C. Cortical thickness and central surface estimation. Neuroimage 2013; 65: 336-348. https://doi. org/10.1016/j.neuroimage.2012.09.050
  • 10. Luders E, Thompson PM, Narr KL, Toga AW, Jancke L et al. A curvature-based approach to estimate local gyrification on the cortical surface. Neuroimage 2006; 29 (4): 1224-1230. https:// doi.org/10.1016/j.neuroimage.2005.08.049
  • 11. Patenaude B, Smith SM, Kennedy DN, Jenkinson MA. Bayesian model of shape and appearance for subcortical brain segmentation. Neuroimage 2011; 56 (3): 907-922. https://doi. org/10.1016/j.neuroimage.2011.02.046
  • 12. Seiger R, Ganger S, Kranz GS, Hahn A, Lanzenberger R. Cortical thickness estimations of FreeSurfer and the CAT12 Toolbox in patients with Alzheimer’s disease and healthy controls. Journal of Neuroimaging 2018; 28 (5): 515-523. https://doi.org/10.1111/jon.12521
  • 13. Fischl B, Dale AM. Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of the National Academy of Sciences of the United States of America 2000; 97 (20): 11050-11055. https://doi.org/10.1073/pnas.200033797
  • 14. Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 2006; 31 (3): 968-980. https://doi.org/10.1016/j. neuroimage.2006.01.021
  • 15. Poline JB, Worsley KJ, Evans AC, Friston KJ. Combining spatial extent and peak intensity to test for activations in functional imaging. Neuroimage 1997; 5 (2): 83-96. https://doi.org/10.1006/ nimg.1996.0248
  • 16. Beenhakker MP, Huguenard JR. Neurons that fire together also conspire together: is normal sleep circuitry hijacked to generate epilepsy? Neuron 2009; 62 (5): 612-632. https://doi.org/10.1016/j. neuron.2009.05.015
  • 17. Steriade M, McCormick DA, Sejnowski TJ. Thalamocortical oscillations in the sleeping and aroused brain. Science 1993; 262 (5134): 679-685. https://doi.org/10.1126/science.8235588
  • 18. Siniatchkin M, Groening K, Moehring J, Moeller F, Boor R et al. Neuronal networks in children with continuous spikes and waves during slow sleep. Brain 2010; 133 (9): 2798-2813. https://doi. org/10.1093/brain/awq183
  • 19. Leal A, Calado E, Vieira JP, Mendonça C, Ferreira JC et al. Anatomical and physiological basis of continuous spike-wave of sleep syndrome after early thalamic lesions. Epilepsy and Behavior 2018; 78: 243-255. https://doi.org/10.1016/j.yebeh.2017.08.027
  • 20. Gibbs SA, Nobili L, Halász P. Interictal epileptiform discharges in sleep and the role of the thalamus in encephalopathy related to status epilepticus during slow Sleep. Epileptic Disorders 2019; 21 (S1): 54-61. https://doi.org/10.1684/epd.2019.1058
  • 21. Agarwal R, Kumar A, Tiwari VN, Chugani H. Thalamic abnormalities in children with continuous spike-wave during slow-wave sleep: an F-18-fluorodeoxyglucose positron emission tomography perspective. Epilepsia 2016; 57 (2): 263-271. https:// doi.org/10.1111/epi.13278
  • 22. Sánchez Fernández I, Peters JM, Akhondi-Asl A, Klehm J, Warfield SK et al. Reduced thalamic volume in patients with electrical status epilepticus in sleep. Epilepsy Research 2017; 130: 74-80. https:// doi.org/10.1016/j.eplepsyres.2017.01.010
  • 23. Öztürk Z, Karalok ZS, Güneş A. Reduced thalamic volume is strongly associated with electrical status epilepticus in sleep. Acta Neurologica Belgica 2021; 121 (1): 211-217. https://doi. org/10.1007/s13760-019-01202-7
  • 24. Song SK, Yoshino J, Le TQ, Lin SJ, Sun SW et al. Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 2005; 26 (1): 132-140. https://doi.org/10.1016/j. neuroimage.2005.01.028
  • 25. Koshiyama D, Fukunaga M, Okada N, Morita K, Nemoto K et al. Association between the superior longitudinal fasciculus and perceptual organization and working memory: a diffusion tensor imaging study. Neuroscience Letters 2020; 738: 135349. https://doi.org/10.1016/j.neulet.2020.135349
  • 26. Urger SE, de Bellis MD, Hooper SR, Woolley DP, Chen SD et al. The superior longitudinal fasciculus in typically developing children and adolescents: diffusion tensor imaging and neuropsychological correlates. Journal of Child Neurology 2015; 30 (1): 9-20. https://doi.org/10.1177/0883073813520503
  • 27. Miyamoto H, Tatsukawa T, Shimohata A, Yamagata T, Suzuki T et al. Impaired cortico-striatal excitatory transmission triggers epilepsy. Nature Communications 2019; 10 (1): 1917. https:// doi.org/10.1038/s41467-019-09954-9
  • 28. Volman SF, Lammel S, Margolis EB, Kim Y, Richard JM et al. New insights into the specificity and plasticity of reward and aversion encoding in the mesolimbic system. Journal of Neuroscience 2013; 33 (45): 17569-17576. https://doi. org/10.1523/JNEUROSCI.3250-13.2013
  • 29. Wang J, Zhang Y, Zhang H, Wang K, Wang H et al. Nucleus accumbens shell: a potential target for drug-resistant epilepsy with neuropsychiatric disorders. Epilepsy Research 2020; 164: 106365. https://doi.org/10.1016/j.eplepsyres.2020.106365
  • 30. Bonilha L, Rorden C, Castellano G, Pereira F, Rio PA et al. Voxel-based morphometry reveals gray matter network atrophy in refractory medial temporal lobe epilepsy. Archives of Neurology 2004; 61 (9), 1379–1384. https://doi.org/10.1001/ archneur.61.9.1379
  • 31. Garcia AD, Buffalo EA. Anatomy and function of the primate entorhinal cortex. Annual Review of Vision Science 2020; 6: 411- 432. https://doi.org/10.1146/annurev-vision-030320-041115
  • 32. Streng ML, Krook-Magnuson E. The cerebellum and epilepsy. Epilepsy and Behavior 2021; 121 (Pt B): 106909. https://doi. org/10.1016/j.yebeh.2020.106909
  • 33. Buijink AWG, Caan MWA, Tijssen MAJ, Hoogduin JM, Maurits NM et al. Decreased cerebellar fiber density in cortical myoclonic tremor but not in essential tremor. Cerebellum 2013; 12 (2): 199-204. https://doi.org/10.1007/s12311-012-0414-2
  • 34. Allen LA, Vos SB, Kumar R, Ogren JA, Harper RK et al. Cerebellar, limbic, and midbrain volume alterations in sudden unexpected death in epilepsy. Epilepsia 2019; 60 (4): 718-729. https://doi.org/10.1111/epi.14689
  • 35. Wiest R, Estermann L, Scheidegger O, Rummel C, Jann K et al. Widespread grey matter changes and hemodynamic correlates to interictal epileptiform discharges in pharmacoresistant mesial temporal epilepsy. Journal of Neurology 2013; 260 (6): 1601-1610. https://doi.org/10.1007/s00415-013-6841-2
  • 36. Bohnen NI, O’Brien TJ, Mullan BP, So EL. Cerebellar changes in partial seizures: clinical correlations of quantitative SPECT and MRI analysis. Epilepsia 1998; 39 (6): 640-650. https://doi. org/10.1111/j.1528-1157.1998.tb01433.x
  • 37. Popa LS, Hewitt AL, Ebner TJ. The cerebellum for jocks and nerds alike. Frontiers in Systems Neuroscience 2014; 8: 113. https://doi.org/10.3389/fnsys.2014.00113
  • 38. Sokolov AA, Miall RC, Ivry RB. The cerebellum: adaptive prediction for movement and cognition. Trends in Cognitive Sciences 2017; 21 (5): 313-332. https://doi.org/10.1016/j. tics.2017.02.005
  • 39. Kandel ER, Schwartz JH, Jessell TM, Siegelbaum SA, Hudspeth AJ, Mack S (editors). Principles of Neural Science. 5th ed. McGraw Hill; 2014.
  • 40. Canto CB, Onuki Y, Bruinsma B, van der Werf YD, de Zeeuw CI. The sleeping cerebellum. Trends in Neurosciences 2017; 40 (5): 309-23. https://doi.org/10.1016/j.tins.2017.03.001
  • 41. Ewell LA, Liang L, Armstrong C, Soltész I, Leutgeb S et al. Brain state is a major factor in preseizure hippocampal network activity and influences success of seizure intervention. Journal of Neuroscience 2015; 35 (47): 15635-15648. https://doi. org/10.1523/JNEUROSCI.5112-14.2015
  • 42. Khan S, Nobili L, Khatami R, Loddenkemper T, Cajochen C et al. Circadian rhythm and epilepsy. Lancet Neurology 2018; 17 (12): 1098-1108. https://doi.org/10.1016/S1474- 4422(18)30335-1
  • 43. Purnell BS, Thijs RD, Buchanan GF. Dead in the night: sleep- wake and time-of-day influences on sudden unexpected death in epilepsy. Frontiers in Neurology 2018; 9: 1079. https://doi. org/10.3389/fneur.2018.01079
  • 44. Lin JJ, Salamon N, Lee AD, Dutton RA, Geaga JA et al. Reduced neocortical thickness and complexity mapped in mesial temporal lobe epilepsy with hippocampal sclerosis. Cerebral Cortex 2007; 17 (9): 2007-2018. https://doi.org/10.1093/cercor/ bhl109
  • 45. Bernhardt BC, Rozen DA, Worsley KJ, Evans AC, Bernasconi N et al. Thalamo-cortical network pathology in idiopathic generalized epilepsy: insights from MRI-based morphometric correlation analysis. Neuroimage 2009; 46 (2): 373-381. https:// doi.org/10.1016/j.neuroimage.2009.01.055
  • 46. Salin P, Tseng G, Hoffman S, Parada I, Prince DA. Axonal sprouting in layer V pyramidal neurons of chronically injured cerebral cortex. Journal of Neuroscience 1995; 15 (12): 8234- 8245. https://doi.org/10.1523/JNEUROSCI.15-12-08234.1995
  • 47. Colciaghi F, Finardi A, Nobili P, Locatelli D, Spigolon G et al. Progressive brain damage, synaptic reorganization and NMDA activation in a model of epileptogenic cortical dysplasia. PLoS One 2014; 9 (2): e89898. https://doi.org/10.1371/journal. pone.0089898
  • 48. Elger CE, Helmstaedter C, Kurthen M. Chronic epilepsy and cognition. The Lancet Neurology 2004; 3 (11): 663-672. https:// doi.org/10.1016/S1474-4422(04)00906-8
  • 49. McDonald CR, Hagler DJ, Jr Ahmadi ME, Tecoma E, Iragui V et al. Regional neocortical thinning in mesial temporal lobe epilepsy. Epilepsia 2008; 49 (5): 794-803. https://doi. org/10.1111/j.1528-1167.2008.01539.x
  • 50. Ogren JA, Tripathi R, Macey PM, Kumar R, Stern JM et al. Regional cortical thickness changes accompanying generalized tonic-clonic seizures. NeuroImage: Clinical 2018; 20: 205-215. https://doi.org/10.1016/j.nicl.2018.07.015
APA Duzkalir H, genç b, sager s, turkyilmaz a, GUNBEY H (2023). Microstructural evaluation of the brain with advanced magnetic resonance imaging techniques in cases of electrical status epilepticus during sleep (ESES). , 1840 - 1851. 10.55730/1300-0144.5754
Chicago Duzkalir Hanife Gulden,genç barış,sager safiye gunes,turkyilmaz ayberk,GUNBEY HEDIYE PINAR Microstructural evaluation of the brain with advanced magnetic resonance imaging techniques in cases of electrical status epilepticus during sleep (ESES). (2023): 1840 - 1851. 10.55730/1300-0144.5754
MLA Duzkalir Hanife Gulden,genç barış,sager safiye gunes,turkyilmaz ayberk,GUNBEY HEDIYE PINAR Microstructural evaluation of the brain with advanced magnetic resonance imaging techniques in cases of electrical status epilepticus during sleep (ESES). , 2023, ss.1840 - 1851. 10.55730/1300-0144.5754
AMA Duzkalir H,genç b,sager s,turkyilmaz a,GUNBEY H Microstructural evaluation of the brain with advanced magnetic resonance imaging techniques in cases of electrical status epilepticus during sleep (ESES). . 2023; 1840 - 1851. 10.55730/1300-0144.5754
Vancouver Duzkalir H,genç b,sager s,turkyilmaz a,GUNBEY H Microstructural evaluation of the brain with advanced magnetic resonance imaging techniques in cases of electrical status epilepticus during sleep (ESES). . 2023; 1840 - 1851. 10.55730/1300-0144.5754
IEEE Duzkalir H,genç b,sager s,turkyilmaz a,GUNBEY H "Microstructural evaluation of the brain with advanced magnetic resonance imaging techniques in cases of electrical status epilepticus during sleep (ESES)." , ss.1840 - 1851, 2023. 10.55730/1300-0144.5754
ISNAD Duzkalir, Hanife Gulden vd. "Microstructural evaluation of the brain with advanced magnetic resonance imaging techniques in cases of electrical status epilepticus during sleep (ESES)". (2023), 1840-1851. https://doi.org/10.55730/1300-0144.5754
APA Duzkalir H, genç b, sager s, turkyilmaz a, GUNBEY H (2023). Microstructural evaluation of the brain with advanced magnetic resonance imaging techniques in cases of electrical status epilepticus during sleep (ESES). Turkish Journal of Medical Sciences, 53(6), 1840 - 1851. 10.55730/1300-0144.5754
Chicago Duzkalir Hanife Gulden,genç barış,sager safiye gunes,turkyilmaz ayberk,GUNBEY HEDIYE PINAR Microstructural evaluation of the brain with advanced magnetic resonance imaging techniques in cases of electrical status epilepticus during sleep (ESES). Turkish Journal of Medical Sciences 53, no.6 (2023): 1840 - 1851. 10.55730/1300-0144.5754
MLA Duzkalir Hanife Gulden,genç barış,sager safiye gunes,turkyilmaz ayberk,GUNBEY HEDIYE PINAR Microstructural evaluation of the brain with advanced magnetic resonance imaging techniques in cases of electrical status epilepticus during sleep (ESES). Turkish Journal of Medical Sciences, vol.53, no.6, 2023, ss.1840 - 1851. 10.55730/1300-0144.5754
AMA Duzkalir H,genç b,sager s,turkyilmaz a,GUNBEY H Microstructural evaluation of the brain with advanced magnetic resonance imaging techniques in cases of electrical status epilepticus during sleep (ESES). Turkish Journal of Medical Sciences. 2023; 53(6): 1840 - 1851. 10.55730/1300-0144.5754
Vancouver Duzkalir H,genç b,sager s,turkyilmaz a,GUNBEY H Microstructural evaluation of the brain with advanced magnetic resonance imaging techniques in cases of electrical status epilepticus during sleep (ESES). Turkish Journal of Medical Sciences. 2023; 53(6): 1840 - 1851. 10.55730/1300-0144.5754
IEEE Duzkalir H,genç b,sager s,turkyilmaz a,GUNBEY H "Microstructural evaluation of the brain with advanced magnetic resonance imaging techniques in cases of electrical status epilepticus during sleep (ESES)." Turkish Journal of Medical Sciences, 53, ss.1840 - 1851, 2023. 10.55730/1300-0144.5754
ISNAD Duzkalir, Hanife Gulden vd. "Microstructural evaluation of the brain with advanced magnetic resonance imaging techniques in cases of electrical status epilepticus during sleep (ESES)". Turkish Journal of Medical Sciences 53/6 (2023), 1840-1851. https://doi.org/10.55730/1300-0144.5754