Epilepsy in multiple sclerosis: The role of temporal lobe damage

Background: Although temporal lobe pathology may explain some of the symptoms of multiple sclerosis (MS), its role in the pathogenesis of seizures has not been clarified yet. Objectives: To investigate the role of temporal lobe damage in MS patients suffering from epilepsy, by the application of advanced multimodal 3T magnetic resonance imaging (MRI) analysis. Methods: A total of 23 relapsing remitting MS patients who had epileptic seizures (RRMS/E) and 23 disease duration matched RRMS patients without any history of seizures were enrolled. Each patient underwent advanced 3T MRI protocol specifically conceived to evaluate grey matter (GM) damage. This includes grey matter lesions (GMLs) identification, evaluation of regional cortical thickness and indices derived from the Neurite Orientation Dispersion and Density Imaging model. Results: Regional analysis revealed that in RRMS/E, the regions most affected by GMLs were the hippocampus (14.2%), the lateral temporal lobe (13.5%), the cingulate (10.0%) and the insula (8.4%). Cortical thinning and alteration of diffusion metrics were observed in several regions of temporal lobe, in insular cortex and in cingulate gyrus of RRMS/E compared to RRMS (p< 0.05 for all comparisons). Conclusions: Compared to RRMS, RRMS/E showed more severe damage of temporal lobe, which exceeds what would be expected on the basis of the global GM damage observed.

[1]  O. Ciccarelli,et al.  Consensus recommendations for MS cortical lesion scoring using double inversion recovery MRI , 2011, Neurology.

[2]  Ganesh Adluru,et al.  Assessment of white matter microstructure in stroke patients using NODDI , 2014, 2014 36th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[3]  M. Battaglini,et al.  Cortical lesions in radiologically isolated syndrome , 2011, Neurology.

[4]  Marit Grønning,et al.  Epileptic seizures in patients with multiple sclerosis. Is the prognosis of epilepsy underestimated? , 1997, Seizure.

[5]  Paul A. Yushkevich,et al.  Multi-Atlas Segmentation with Joint Label Fusion , 2013, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[6]  Daniel C. Alexander,et al.  NODDI: Practical in vivo neurite orientation dispersion and density imaging of the human brain , 2012, NeuroImage.

[7]  R. Reynolds,et al.  Temporal lobe cortical pathology and inhibitory GABA interneuron cell loss are associated with seizures in multiple sclerosis , 2016, Multiple sclerosis.

[8]  Sébastien Ourselin,et al.  Longitudinal measurement of the developing grey matter in preterm subjects using multi-modal MRI , 2015, NeuroImage.

[9]  D. Turnbull,et al.  Review: Mitochondria and disease progression in multiple sclerosis , 2008, Neuropathology and applied neurobiology.

[10]  M. Calabrese,et al.  Cortical pathology in multiple sclerosis patients with epilepsy: a 3 year longitudinal study , 2011, Journal of Neurology, Neurosurgery & Psychiatry.

[11]  Miguel Valencia,et al.  Decoding brain state transitions in the pedunculopontine nucleus: cooperative phasic and tonic mechanisms , 2015, Front. Neural Circuits.

[12]  Frederik Barkhof,et al.  Extensive Hippocampal Demyelination in Multiple Sclerosis , 2007, Journal of neuropathology and experimental neurology.

[13]  F. Barkhof,et al.  Imaging the tip of the iceberg: visualization of cortical lesions in multiple sclerosis , 2011, Multiple sclerosis.

[14]  H. Tobi,et al.  Magnetic Resonance Imaging of Epilepsy in Multiple Sclerosis: A Case Control Study. Implications for Treatment Trials with 4-Aminopyridine , 1996, Multiple sclerosis.

[15]  Mohammad Reza Najafi,et al.  Jacksonian seizure as the relapse symptom of multiple sclerosis , 2013, Journal of research in medical sciences : the official journal of Isfahan University of Medical Sciences.

[16]  J. Helpern,et al.  Diffusional kurtosis imaging: The quantification of non‐gaussian water diffusion by means of magnetic resonance imaging , 2005, Magnetic resonance in medicine.

[17]  Richard Nicholas,et al.  Substantial Archaeocortical Atrophy and Neuronal Loss in Multiple Sclerosis , 2009, Brain pathology.

[18]  P. Basser,et al.  Toward a quantitative assessment of diffusion anisotropy , 1996, Magnetic resonance in medicine.

[19]  M. Calabrese,et al.  Extensive cortical inflammation is associated with epilepsy in multiple sclerosis , 2008, Journal of Neurology.

[20]  Chiara Romualdi,et al.  Detection of cortical inflammatory lesions by double inversion recovery magnetic resonance imaging in patients with multiple sclerosis. , 2007, Archives of neurology.

[21]  R. Reynolds,et al.  Meningeal B-cell follicles in secondary progressive multiple sclerosis associate with early onset of disease and severe cortical pathology. , 2007, Brain : a journal of neurology.

[22]  J. H. Cross,et al.  Revised terminology and concepts for organization of seizures and epilepsies: Report of the ILAE Commission on Classification and Terminology, 2005–2009 , 2010, Epilepsia.

[23]  M. Chakravarty,et al.  Functional Consequences of Neurite Orientation Dispersion and Density in Humans across the Adult Lifespan , 2015, The Journal of Neuroscience.

[24]  M Vapalahti,et al.  MR volumetry of the entorhinal, perirhinal, and temporopolar cortices in drug-refractory temporal lobe epilepsy. , 2001, AJNR. American journal of neuroradiology.

[25]  Brian B. Avants,et al.  Registration based cortical thickness measurement , 2009, NeuroImage.

[26]  M. Koubeissi,et al.  The piriform, perirhinal, and entorhinal cortex in seizure generation , 2015, Front. Neural Circuits.

[27]  B. Scheithauer,et al.  Inflammatory cortical demyelination in early multiple sclerosis. , 2011, The New England journal of medicine.

[28]  S. Vukusic,et al.  Multiple sclerosis and epileptic seizures , 2011, Multiple sclerosis.

[29]  Jeffrey A. Cohen,et al.  Diagnostic criteria for multiple sclerosis: 2010 Revisions to the McDonald criteria , 2011, Annals of neurology.

[30]  Stéphane Lehéricy,et al.  Hippocampal sclerosis in temporal lobe epilepsy: findings at 7 T¹. , 2011, Radiology.

[31]  A Giorgio,et al.  Imaging distribution and frequency of cortical lesions in patients with multiple sclerosis , 2010, Neurology.

[32]  J. Kurtzke Rating neurologic impairment in multiple sclerosis , 1983, Neurology.

[33]  R. Reynolds,et al.  A Gradient of neuronal loss and meningeal inflammation in multiple sclerosis , 2010, Annals of neurology.

[34]  M. Filippi,et al.  A 3‐year magnetic resonance imaging study of cortical lesions in relapse‐onset multiple sclerosis , 2009, Annals of neurology.

[35]  A. Nehlig,et al.  Prolonged refractory status epilepticus with early and persistent restricted hippocampal signal MRI abnormality , 2008, Journal of Neurology.

[36]  J. Spatt,et al.  Epileptic and non-epileptic seizures in multiple sclerosis , 2001, Journal of Neurology.

[37]  M. Calabrese,et al.  Magnetic resonance evidence of cortical onset of multiple sclerosis , 2009, Multiple sclerosis.

[38]  Arno Klein,et al.  Large-scale evaluation of ANTs and FreeSurfer cortical thickness measurements , 2014, NeuroImage.