Neurovascular multiparametric MRI defines epileptogenic and seizure propagation regions in experimental mesiotemporal lobe epilepsy.
blood-brain barrier permeability
cerebrovascular damage
chronic seizure-spreading regions
epileptic foci
status epilepticus
Journal
Epilepsia
ISSN: 1528-1167
Titre abrégé: Epilepsia
Pays: United States
ID NLM: 2983306R
Informations de publication
Date de publication:
05 2021
05 2021
Historique:
revised:
05
03
2021
received:
23
10
2020
accepted:
05
03
2021
pubmed:
6
4
2021
medline:
1
10
2021
entrez:
5
4
2021
Statut:
ppublish
Résumé
Improving the identification of the epileptogenic zone and associated seizure-spreading regions represents a significant challenge. Innovative brain-imaging modalities tracking neurovascular dynamics during seizures may provide new disease biomarkers. With use of a multi-parametric magnetic resonance imaging (MRI) analysis at 9.4 Tesla, we examined, elaborated, and combined multiple cellular and cerebrovascular MRI read-outs as imaging biomarkers of the epileptogenic and seizure-propagating regions. Analyses were performed in an experimental model of mesial temporal lobe epilepsy (MTLE) generated by unilateral intra-hippocampal injection of kainic acid (KA). In the ipsilateral epileptogenic hippocampi, tissue T Combining multi-parametric MRI acquisition and machine-learning analyses delivers specific imaging identifiers to segregate the epileptogenic from the contralateral seizure-spreading hippocampi in experimental MTLE. The potential clinical value of our findings is critically discussed.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1244-1255Informations de copyright
© 2021 International League Against Epilepsy.
Références
Lansberg MG, O'Brien MW, Norbash AM, Moseley ME, Morrell M, Albers GW. MRI abnormalities associated with partial status epilepticus. Neurology. 1999;52(5):1021-7.
Rüber T, David B, Lüchters G, Nass RD, Friedman A, Surges R, et al. Evidence for peri-ictal blood-brain barrier dysfunction in patients with epilepsy. Brain. 2018;141(10):2952-65.
Aellen J, Abela E, Buerki SE, Kottke R, Springer E, Schindler K, et al. Focal hemodynamic patterns of status epilepticus detected by susceptibility weighted imaging (SWI). Eur Radiol. 2014;24(11):2980-8.
Thivard L, Lehéricy S, Krainik A, Adam C, Dormont D, Chiras J, et al. Diffusion tensor imaging in medial temporal lobe epilepsy with hippocampal sclerosis. NeuroImage. 2005;28(3):682-90.
Friedman A. Blood-brain barrier dysfunction, status epilepticus, seizures, and epilepsy: a puzzle of a chicken and egg? Epilepsia. 2011;52:19-20. https://doi.org/10.1111/j.1528-1167.2011.03227.x
van Vliet EA, Aronica E, Gorter JA. Blood-brain barrier dysfunction, seizures and epilepsy. Semin Cell Dev Biol. Academic Press. 2015;38:26-34.
Marchi N, Tierney W, Alexopoulos AV, Puvenna V, Granata T, Janigro D. The etiological role of blood-brain barrier dysfunction in seizure disorders. Cardiovasc Psychiatry Neurol. 2011;2011:1-9.
Arango-Lievano M, Boussadia B, De Terdonck LDT, Gault C, Fontanaud P, Lafont C, et al. Topographic reorganization of cerebrovascular mural cells under seizure conditions. Cell Rep. 2018;23(4):1045-59.
Prager O, Kamintsky L, Hasam-Henderson LA, Schoknecht K, Wuntke V, Papageorgiou I, et al. Seizure-induced microvascular injury is associated with impaired neurovascular coupling and blood-brain barrier dysfunction. Epilepsia. 2019;60(2):322-36. https://doi.org/10.1111/epi.14631
Klement W, Blaquiere M, Zub E, DeBock F, Boux F, Barbier E, et al. A pericyte-glia scarring develops at the leaky capillaries in the hippocampus during seizure activity. Epilepsia. 2019;60(7):1399-411. https://doi.org/10.1111/epi.16019
Milesi S, Boussadia B, Plaud C, Catteau M, Rousset M-C, De Bock F, et al. Redistribution of PDGFRβ cells and NG2DsRed pericytes at the cerebrovasculature after status epilepticus. Neurobiol Dis. 2014;71:151-8.
Rigau V, Morin M, Rousset M-C, de Bock F, Lebrun A, Coubes P, et al. Angiogenesis is associated with blood-brain barrier permeability in temporal lobe epilepsy. Brain. 2007;130(7):1942-56.
Vezzani A, Balosso S, Ravizza T. Neuroinflammatory pathways as treatment targets and biomarkers in epilepsy. Nat Rev Neurol. 2019;15(8):459-72. https://doi.org/10.1038/s41582-019-0217-x. Nature Publishing Group.
Choy MK, Cheung KK, Thomas DL, Gadian DG, Lythgoe MF, Scott RC. Quantitative MRI predicts status epilepticus-induced hippocampal injury in the lithium-pilocarpine rat model. Epilepsy Res. 2010;88(2-3):221-30.
Bernhardt BC, Fadaie F, Vos de Wael R, Hong S-J, Liu M, Guiot MC, et al. Preferential susceptibility of limbic cortices to microstructural damage in temporal lobe epilepsy: a quantitative T1 mapping study. NeuroImage. 2018;182:294-303.
Wang Y, Majors A, Najm I, Xue M, Comair Y, Modic M, et al. Postictal alteration of sodium content and apparent diffusion coefficient in epileptic rat brain induced by kainic acid. Epilepsia. 1996;37(10):1000-6.
Engelhorn T, Weise J, Hammen T, Bluemcke I, Hufnagel A, Doerfler A. Early diffusion-weighted MRI predicts regional neuronal damage in generalized status epilepticus in rats treated with diazepam. Neurosci Lett. 2007;417(3):275-80.
Van Vliet EA, Otte WM, Wadman WJ, Aronica E, Kooij G, de Vries HE, et al. Blood-brain barrier leakage after status epilepticus in rapamycin-treated rats I: magnetic resonance imaging. Epilepsia. 2016;57(1):59-69. https://doi.org/10.1111/epi.13246
Bar-Klein G, Lublinsky S, Kamintsky L, Noyman I, Veksler R, Dalipaj H, et al. Imaging blood-brain barrier dysfunction as a biomarker for epileptogenesis. Brain. 2017;140(6):1692-705.
Hamamoto Y, Hasegawa D, Mizoguchi S, Yu Y, Wada M, Kuwabara T, et al. Changes in the interictal and early postictal diffusion and perfusion magnetic resonance parameters in familial spontaneous epileptic cats. Epilepsy Res. 2017;133:76-82. https://doi.org/10.1016/j.eplepsyres.2017.04.015
Riban V, Bouilleret V, Pham-Lê BT, Fritschy JM, Marescaux C, Depaulis A. Evolution of hippocampal epileptic activity during the development of hippocampal sclerosis in a mouse model of temporal lobe epilepsy. Neuroscience. 2002;112(1):101-11.
Heinrich C, Nitta N, Flubacher A, Müller M, Fahrner A, Kirsch M, et al. Reelin Deficiency and displacement of mature neurons, but not neurogenesis, underlie the formation of granule cell dispersion in the epileptic hippocampus. J Neurosci. 2006;26(17):4701-13.Available from: http://docs.appliedbiosystems.com/pebiodocs/
Pernot F, Heinrich C, Barbier L, Peinnequin A, Carpentier P, Dhote F, et al. Inflammatory changes during epileptogenesis and spontaneous seizures in a mouse model of mesiotemporal lobe epilepsy. Epilepsia. 2011;52(12):2315-25. https://doi.org/10.1111/j.1528-1167.2011.03273.x
Avants BB, Epstein CL, Grossman M, Gee JC. Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med Image Anal. 2008;12(1):26-41.
Zub E, Canet G, Garbelli R, Blaquiere M, Rossini L, Pastori C, et al. The GR-ANXA1 pathway is a pathological player and a candidate target in epilepsy. FASEB J. 2019;33(12):13998-4009.Available from www.fasebj.org
Tropres I, Grimault S, Vaeth A, Grillon E, Julien C, Payen J-F, et al. Vessel size imaging. Magn Reson Med. 2001;45(3):397-408.
Christen T, Bouzat P, Pannetier N, Coquery N, Moisan A, Lemasson B, et al. Tissue oxygen saturation mapping with magnetic resonance imaging. J Cereb Blood Flow Metab. 2014;34(9):1550-7.
Lemasson B, Serduc R, Maisin C, Bouchet A, Coquery N, Robert P, et al. Monitoring blood-brain barrier status in a rat model of glioma receiving therapy: dual injection of low-molecular-weight and macromolecular MR contrast media. Radiology. 2010;257(2):342-52.
Brossard C, Montigon O, Boux F, Delphin A, Christen T, Barbier EL, et al. MP3: medical software for processing multi-parametric images pipelines. Front Neuroinform. 2020;14:594799. https://doi.org/10.3389/fninf.2020.594799
Barbier EL, Lawrence KSS, Grillon E, Koretsky AP, Décorps M. A model of blood-brain barrier permeability to water: Accounting for blood inflow and longitudinal relaxation effects. Magn Reson Med. 2002;47(6):1100-9.
Barbier EL, Liu L, Grillon E, Payen J-F, Lebas J-F, Segebarth C, et al. Focal brain ischemia in rat: acute changes in brain tissue T1 reflect acute increase in brain tissue water content. NMR Biomed. 2005;18(8):499-506.
Lemasson B, Valable S, Farion R, Krainik A, Rémy C, Barbier EL. In vivo imaging of vessel diameter, size, and density: a comparative study between MRI and histology. Magn Reson Med. 2013;69(1):18-26.
Badhwar A, Lerch JP, Hamel E, Sled JG. Impaired structural correlates of memory in Alzheimer's disease mice. NeuroImage Clin. 2013;3:290-300.
Klement W, Garbelli R, Zub E, Rossini L, Tassi L, Girard B, et al. Seizure progression and inflammatory mediators promote pericytosis and pericyte-microglia clustering at the cerebrovasculature. Neurobiol Dis. 2018;113:70-81.
Meier R, Häussler U, Aertsen A, Deransart C, Depaulis A, Egert U. Short-term changes in bilateral hippocampal coherence precede epileptiform events. NeuroImage. 2007;38(1):138-49.
Rudie JD, Colby JB, Salamon N. Machine learning classification of mesial temporal sclerosis in epilepsy patients. Epilepsy Res. 2015;117:63-69. https://doi.org/10.1016/j.eplepsyres.2015.09.005
Del Gaizo J, Mofrad N, Jensen JH, Clark D, Glenn R, Helpern J, et al. Using machine learning to classify temporal lobe epilepsy based on diffusion MRI. Brain Behav. 2017;7(10):1-7.
Cantor-Rivera D, Khan AR, Goubran M, Mirsattari SM, Peters TM. Detection of temporal lobe epilepsy using support vector machines in multi-parametric quantitative MR imaging [Internet]. Comput Med Imaging Graph. 2015;41:14-28.Available from https://ir.lib.uwo.ca/robartspub
Bouilleret V, Nehlig A, Marescaux C, Namer IJ. Magnetic resonance imaging follow-up of progressive hippocampal changes in a mouse model of mesial temporal lobe epilepsy. Epilepsia. 2000;41(6):642-50.
Tokumitsu T, Mancuso A, Weinstein PR, Weiner MW, Naruse S, Maudsley AA. Metabolic and pathological effects of temporal lobe epilepsy in rat brain detected by proton spectroscopy and imaging. Brain Res. 1997;744(1):57-67.
Nairismägi J, Gröhn OHJ, Kettunen MI, Nissinen J, Kauppinen RA, Pitkänen A. Progression of brain damage after status epilepticus and its association with epileptogenesis: a quantitative MRI study in a rat model of temporal lobe epilepsy. Epilepsia. 2004;45(9):1024-34.
Hayward NMEA, Ndode-Ekane XE, Kutchiashvili N, Gröhn O, Pitkänen A. Elevated cerebral blood flow and vascular density in the amygdala after status epilepticus in rats. Neurosci Lett. 2010;484(1):39-42.
van Vliet EA, Otte WM, Gorter JA, Dijkhuizen RM, Wadman WJ. Longitudinal assessment of blood-brain barrier leakage during epileptogenesis in rats. A quantitative MRI study. Neurobiol Dis. 2014;63:74-84.
Runtz L, Girard B, Toussenot M, Espallergues J, Fayd'Herbe De Maudave A, Milman A, et al. Hepatic and hippocampal cytochrome P450 enzyme overexpression during spontaneous recurrent seizures. Epilepsia. 2018;59(1):123-34.
Arabadzisz D, Antal K, Parpan F, Emri Z, Fritschy JM. Epileptogenesis and chronic seizures in a mouse model of temporal lobe epilepsy are associated with distinct EEG patterns and selective neurochemical alterations in the contralateral hippocampus. Exp Neurol. 2005;194(1):76-90.Available from www.fftw.org
Pallud J, Häussler U, Langlois M, Hamelin S, Devaux B, Deransart C, et al. Dentate gyrus and hilus transection blocks seizure propagation and granule cell dispersion in a mouse model for mesial temporal lobe epilepsy. Hippocampus. 2011;21(3):334-43.
Airaksinen AM, Niskanen J-P, Chamberlain R, Huttunen JK, Nissinen J, Garwood M, et al. Simultaneous fMRI and local field potential measurements during epileptic seizures in medetomidine-sedated rats using RASER pulse sequence. Magn Reson Med. 2010;64(4):1191-9.
Blumenfeld H. Functional MRI studies of animal models in epilepsy. Epilepsia. 2007;48(s4):18-26. https://doi.org/10.1111/j.1528-1167.2007.01238.x
Hamelin S, Stupar V, Mazière L, Guo J, Labriji W, Liu C, et al. In vivo γ-aminobutyric acid increase as a biomarker of the epileptogenic zone: an unbiased metabolomics approach. Epilepsia. 2021;62(1):163-75.
Dickie DA, Shenkin SD, Anblagan D, Lee J, Cabez MB, Rodriguez D, et al. Whole brain magnetic resonance image atlases: a systematic review of existing atlases and caveats for use in population imaging. Frontiers in Neuroinformatics. 2017;11:1. Available from: http://www.brainmap.org/
Hasan KM, Walimuni IS, Kramer LA, Narayana PA. Human brain iron mapping using atlas-based T2 relaxometry. Magn Reson Med [Internet]. 2012;67(3):731-9.Available from http://doi.wiley.com/10.1002/mrm.23054
Zhang S, Arfanakis K. Evaluation of standardized and study-specific diffusion tensor imaging templates of the adult human brain: template characteristics, spatial normalization accuracy, and detection of small inter-group FA differences. Neuroimage [Internet]. 2018 [cited 2020];172:40-50.Available from: https://pubmed.ncbi.nlm.nih.gov/29414497/
Arnaud A, Forbes F, Coquery N, Collomb N, Lemasson B, Barbier EL. Fully automatic lesion localization and characterization: application to brain tumors using multiparametric quantitative MRI data. IEEE Trans Med Imaging. 2018;37(7):1678-89.