A study on brain asymmetry in temporal lobe epilepsy

Yıl 2024, , 144 - 151, 31.05.2024

Edibe Bilişli Kara Zeynep Fırat , Aziz M. Uluğ Gazanfer Ekinci Ümit Şehirli

https://doi.org/10.5472/marumj.1487475

Öz

Objective: Temporal lobe epilepsy (TLE) accompanied by hippocampal sclerosis (HS) is the most common type of focal epilepsies.
Hemispheric asymmetry is a feature of brain organization in both invertebrates and vertebrates and may be the key to some
neurodegenerative diseases. In this context, we aimed to investigate the volumetric asymmetry difference in cerebral structures
between TLE patients and the healthy control group, based on magnetic resonance imaging (MRI) data that may be used as a new
neuroimaging marker for TLE cases.
Patients and Methods: In this retrospective study the cranial MRIs of fourteen clinically manifesting, radiologically HS-identified,
and diagnosed TLE patients and fourteen healthy individuals from the Radiology Department of Yeditepe University Hospital were
evaluated. Volume measurements and asymmetry index (AI) calculations in the total brain, hippocampus, temporal lobe, amygdala,
thalamus, nucleus accumbens (NAc), premotor cortex, primary and somatosensory cortices were performed using the medical
NeuroQuant® software. A negative AI value represented asymmetry towards the right due to reduced left hemispheric volume; a
positive AI value represented asymmetry towards the left due to reduced right hemispheric volume. Subsequently, differences in
volume and asymmetric patterns were investigated among TLE subgroups (right and left-sided TLE) and controls.
Results: The left-sided TLE patients showed significant bilateral total brain volume reduction compared to the control group. Significant
ipsilateral volumetric declines were also detected in the premotor cortex, the temporal lobe, and NAc with remarkable asymmetry to
the right side. No significant changes were detected in right-sided TLE patients compared to the other groups.
Conclusion: Overall, findings suggest that TLE patients had volumetric alterations with symmetry changes beyond the mesial temporal
structures. With further investigations, the asymmetry measures can provide additional knowledge for TLE diagnosis.

Anahtar Kelimeler

Brain asymmetry, Temporal lobe epilepsy, Asymmetry index, Nucleus accumbens

Kaynakça

• Epilepsy W. A public health imperative. Geneva, Switzerland: WHO, 2019.
• Scheffer IE, Berkovic S, Capovilla G, et al. ILAE classification of the epilepsies: position paper of the ILAE Commission for Classification and Terminology. Zeitschrift Fur Epileptologie 2018; 31:296-306. doi:10.1007/s10309.018.0218-6.
• Blumcke I, Thom M, Aronica E, et al. International consensus classification of hippocampal sclerosis in temporal lobe epilepsy: a Task Force report from the ILAE Commission on Diagnostic Methods. Epilepsia 2013; 54:1315-29. doi:10.1111/ epi.12220.
• Alvarez-Linera J: Temporal lobe epilepsy (TLE) and neuroimaging. In: Barkhof F, Jäger HR, Thurnher MM, Rovira À eds. Clinical Neuroradiology: The ESNR Textbook. Cham: Springer International Publishing, 2019: 891-914.
• Watson C, Andermann F, Gloor P, et al. Anatomic basis of amygdaloid and hippocampal volume measurement by magnetic resonance imaging. Neurology 1992; 42:1743-50. doi:10.1212/wnl.42.9.1743.
• Bernasconi N, Bernasconi A, Caramanos Z, Antel SB, Andermann F, Arnold DL. Mesial temporal damage in temporal lobe epilepsy: a volumetric MRI study of the hippocampus, amygdala and parahippocampal region. Brain 2003; 126(Pt 2):462-9. doi:10.1093/brain/awg034.
• Bernasconi N, Natsume J, Bernasconi A. Progression in temporal lobe epilepsy: differential atrophy in mesial temporal structures. Neurology 2005; 65:223-8. doi:10.1212/01. wnl.000.016.9066.46912.fa.
• Caboclo LO, Garzon E, Oliveira PA, et al. Correlation between temporal pole MRI abnormalities and surface ictal EEG patterns in patients with unilateral mesial temporal lobe epilepsy. Seizure 2007; 16:8-16. doi:10.1016/j. seizure.2006.09.001.
• Berkovic SF, Andermann F, Olivier A, et al. Hippocampal sclerosis in temporal lobe epilepsy demonstrated by magnetic resonance imaging. Ann Neurol 1991; 29:175-82. doi:10.1002/ ana.410290210.
• Cascino GD, Jack CR, Jr., Parisi JE, et al. Magnetic resonance imaging-based volume studies in temporal lobe epilepsy: pathological correlations. Ann Neurol 1991; 30:31-6. doi:10.1002/ana.410300107.
• Cendes F, Andermann F, Gloor P, et al. MRI volumetric measurement of amygdala and hippocampus in temporal lobe epilepsy. Neurology 1993; 43:719-25. doi:10.1212/ wnl.43.4.719.
• Jack CR, Jr., Sharbrough FW, Twomey CK, et al. Temporal lobe seizures: lateralization with MR volume measurements of the hippocampal formation. Radiology 1990; 175:423-9. doi:10.1148/radiology.175.2.2183282.
• Moghaddam HS, Aarabi MH, Mehvari-Habibabadi J, et al. Distinct patterns of hippocampal subfield volume loss in left and right mesial temporal lobe epilepsy. Neurol Sci 2021; 42:1411-21. doi:10.1007/s10072.020.04653-6.
• Thom M. Review: Hippocampal sclerosis in epilepsy: a neuropathology review. Neuropathol Appl Neurobiol 2014; 40:520-43. doi:10.1111/nan.12150.
• Van Paesschen W, Revesz T, Duncan JS, King MD, Connelly A. Quantitative neuropathology and quantitative magnetic resonance imaging of the hippocampus in temporal lobe epilepsy. Ann Neurol 1997; 42:756-66. doi:10.1002/ ana.410420512.
• Bernhardt BC, Bernasconi A, Liu M, et al. The spectrum of structural and functional imaging abnormalities in temporal lobe epilepsy. Ann Neurol 2016; 80:142-53. doi:10.1002/ ana.24691.
• Van Paesschen W. Qualitative and quantitative imaging of the hippocampus in mesial temporal lobe epilepsy with hippocampal sclerosis. Neuroimaging Clin N Am 2004; 14:373-400, vii. doi:10.1016/j.nic.2004.04.004.
• Bernasconi N, Duchesne S, Janke A, Lerch J, Collins DL, Bernasconi A. Whole-brain voxel-based statistical analysis of gray matter and white matter in temporal lobe epilepsy. Neuroimage 2004; 23:717-23. doi:10.1016/j. neuroimage.2004.06.015.
• Dreifuss S, Vingerhoets FJ, Lazeyras F, et al. Volumetric measurements of subcortical nuclei in patients with temporal lobe epilepsy. Neurology 2001; 57:1636-41. doi:10.1212/ wnl.57.9.1636.
• Li J, Zhang Z, Shang H. A meta-analysis of voxel-based morphometry studies on unilateral refractory temporal lobe epilepsy. Epilepsy Res 2012; 98:97-103. doi:10.1016/j. eplepsyres.2011.10.002.
• Riederer F, Lanzenberger R, Kaya M, Prayer D, Serles W, Baumgartner C. Network atrophy in temporal lobe epilepsy: a voxel-based morphometry study. Neurology 2008; 71:419-25. doi:10.1212/01.wnl.000.032.4264.96100.e0.
• Santana MT, Jackowski AP, da Silva HH, et al. Auras and clinical features in temporal lobe epilepsy: a new approach on the basis of voxel-based morphometry. Epilepsy Res 2010; 89:327-38. doi:10.1016/j.eplepsyres.2010.02.006.
• Whelan CD, Altmann A, Botia JA, et al. Structural brain abnormalities in the common epilepsies assessed in a worldwide ENIGMA study. Brain 2018; 141(2):391-408. doi:10.1093/brain/awx341.
• Scanlon C, Mueller SG, Cheong I, Hartig M, Weiner MW, Laxer KD. Grey and white matter abnormalities in temporal lobe epilepsy with and without mesial temporal sclerosis. J Neurol 2013; 260:2320-9. doi:10.1007/s00415.013.6974-3.
• Guadalupe T, Willems RM, Zwiers MP, et al. Differences in cerebral cortical anatomy of left – and right-handers. Front Psychol 2014; 5:261. doi:10.3389/fpsyg.2014.00261.
• Kuo F, Massoud TF. Structural asymmetries in normal brain anatomy: A brief overview. Ann Anat 2022; 241:151894. doi:10.1016/j.aanat.2022.151894.
• Lubben N, Ensink E, Coetzee GA, Labrie V. The enigma and implications of brain hemispheric asymmetry in neurodegenerative diseases. Brain Commun 2021; 3(3):fcab211. doi:10.1093/braincomms/fcab211.
• Zuo Z, Ran S, Wang Y, et al. Asymmetry in cortical thickness and subcortical volume in treatment-naive major depressive disorder. Neuroimage Clin 2019; 21:101614. doi:10.1016/j. nicl.2018.101614.
• Oertel-Knochel V, Knochel C, Stablein M, Linden DE. Abnormal functional and structural asymmetry as biomarker for schizophrenia. Curr Top Med Chem 2012; 12(21):2434-51. doi:10.2174/156.802.612805289926.
• Sarica A, Vasta R, Novellino F, et al. MRI Asymmetry Index of Hippocampal Subfields Increases Through the Continuum From the Mild Cognitive Impairment to the Alzheimer’s Disease. Front Neurosci 2018; 12:576. doi:10.3389/ fnins.2018.00576.
• Pereira FR, Alessio A, Sercheli MS, et al. Asymmetrical hippocampal connectivity in mesial temporal lobe epilepsy: evidence from resting state fMRI. BMC Neurosci 2010; 11:66. doi:10.1186/1471-2202-11-66.
• Pittau F, Grova C, Moeller F, Dubeau F, Gotman J. Patterns of altered functional connectivity in mesial temporal lobe epilepsy. Epilepsia 2012; 53:1013-23. doi:10.1111/j.1528- 1167.2012.03464.x.
• Fisher RS, Cross JH, D’Souza C, et al. Instruction manual for the ILAE 2017 operational classification of seizure types. Epilepsia 2017; 58:531-42. doi:10.1111/epi.13671.
• Bullmore E, Brammer M, Harvey I, Ron M. Against the Laterality Index as a Measure of Cerebral Asymmetry. Psychiatry Research-Neuroimaging 1995; 61:121-24. doi:Doi 10.1016/0925-4927(95)02618-8.
• Zhao X, Kang H, Zhou Z, et al. Interhemispheric functional connectivity asymmetry is distinctly affected in left and right mesial temporal lobe epilepsy. Brain Behav 2022; 12:e2484. doi:10.1002/brb3.2484.
• Li Z, Kang J, Gao Q, et al. Structural brain assessment of temporal lobe epilepsy based on voxel-based and surfacebased morphological features. Neurol Neurochir Pol 2021; 55:369-79. doi:10.5603/PJNNS.a2021.0042.
• Liu M, Bernhardt BC, Bernasconi A, Bernasconi N. Gray matter structural compromise is equally distributed in left and right temporal lobe epilepsy. Hum Brain Mapp 2016; 37:515- 24. doi:10.1002/hbm.23046.
• Pail M, Brazdil M, Marecek R, Mikl M. An optimized voxelbased morphometric study of gray matter changes in patients with left-sided and right-sided mesial temporal lobe epilepsy and hippocampal sclerosis (MTLE/HS). Epilepsia 2010; 51:511-8. doi:10.1111/j.1528-1167.2009.02324.x.
• Jber M, Habibabadi JM, Sharifpour R, et al. Temporal and extratemporal atrophic manifestation of temporal lobe epilepsy using voxel-based morphometry and corticometry: clinical application in lateralization of epileptogenic zone. Neurol Sci 2021; 42:3305-25. doi:10.1007/s10072.020.05003-2.
• Keller SS, Roberts N. Voxel-based morphometry of temporal lobe epilepsy: an introduction and review of the literature. Epilepsia 2008; 49:741-57. doi:10.1111/j.1528- 1167.2007.01485.x.
• Moran NF, Lemieux L, Kitchen ND, Fish DR, Shorvon SD. Extrahippocampal temporal lobe atrophy in temporal lobe epilepsy and mesial temporal sclerosis. Brain 2001; 124(Pt 1):167-75. doi:10.1093/brain/124.1.167.
• Alhusaini S, Doherty CP, Palaniyappan L, et al. Asymmetric cortical surface area and morphology changes in mesial temporal lobe epilepsy with hippocampal sclerosis. Epilepsia 2012; 53:995-1003. doi:10.1111/j.1528-1167.2012.03457.x.
• Chowdhury FA, Silva R, Whatley B, Walker MC. Localisation in focal epilepsy: a practical guide. Pract Neurol 2021; 21:481- 91. doi:10.1136/practneurol-2019-002341.
• Kowski AB, Voges J, Heinze HJ, Oltmanns F, Holtkamp M, Schmitt FC. Nucleus accumbens stimulation in partial epilepsy—a randomized controlled case series. Epilepsia 2015; 56:e78-82. doi:10.1111/epi.12999.
• Schmitt FC, Voges J, Heinze HJ, Zaehle T, Holtkamp M, Kowski AB. Safety and feasibility of nucleus accumbens stimulation in five patients with epilepsy. J Neurol 2014; 261:1477-84. doi:10.1007/s00415.014.7364-1.