Seizure activity and brain damage in a model of focal non-convulsive status epilepticus.
brain damage
epilepsy
hippocampus
non-convulsive status epilepticus
seizures
Journal
Neuropathology and applied neurobiology
ISSN: 1365-2990
Titre abrégé: Neuropathol Appl Neurobiol
Pays: England
ID NLM: 7609829
Informations de publication
Date de publication:
08 2021
08 2021
Historique:
revised:
29
12
2020
received:
12
08
2020
accepted:
30
12
2020
pubmed:
10
1
2021
medline:
1
2
2022
entrez:
9
1
2021
Statut:
ppublish
Résumé
Focal non-convulsive status epilepticus (FncSE) is a common emergency condition that may present as the first epileptic manifestation. In recent years, it has become increasingly clear that de novo FncSE should be promptly treated to improve post-status outcome. Whether seizure activity occurring during the course of the FncSE contributes to ensuing brain damage has not been demonstrated unequivocally and is here addressed. We used continuous video-EEG monitoring to characterise an acute experimental FncSE model induced by unilateral intrahippocampal injection of kainic acid (KA) in guinea pigs. Immunohistochemistry and mRNA expression analysis were utilised to detect and quantify brain injury, 3-days and 1-month after FncSE. Seizure activity occurring during the course of FncSE involved both hippocampi equally. Neuronal loss, blood-brain barrier permeability changes, gliosis and up-regulation of inflammation, activity-induced and astrocyte-specific genes were observed in the KA-injected hippocampus. Diazepam treatment reduced FncSE duration and KA-induced neuropathological damage. In the contralateral hippocampus, transient and possibly reversible gliosis with increase of aquaporin-4 and Kir4.1 genes were observed 3 days post-KA. No tissue injury and gene expression changes were found 1-month after FncSE. In our model, focal seizures occurring during FncSE worsen ipsilateral KA-induced tissue damage. FncSE only transiently activated glia in regions remote from KA-injection, suggesting that seizure activity during FncSE without local pathogenic co-factors does not promote long-lasting detrimental changes in the brain. These findings demonstrate that in our experimental model, brain damage remains circumscribed to the area where the primary cause (KA) of the FncSE acts. Our study emphasises the need to use antiepileptic drugs to contain local damage induced by focal seizures that occur during FncSE.
Substances chimiques
Anticonvulsants
0
Kainic Acid
SIV03811UC
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
679-693Informations de copyright
© 2021 British Neuropathological Society.
Références
Wasterlain CG, Fujikawa DG, Penix LR, Sankar R. Pathophysiological mechanisms of brain damage from status epilepticus. Epilepsia. 1993;34:37-53.
Shorvon S. Does convulsive status epilepticus (SE) result in cerebral damage or affect the course of epilepsy - the epidemiological and clinical evidence? Prog Brain Res. 2002;135:85-93.
Young GB, Claassen J. Nonconvulsive status epilepticus and brain damage: Further evidence, more questions. Neurology. 2010;75:760-770.
Claassen J, Mayer SA, Kowalski RG, Emerson RG, Hirsch LJ. Detection of electrographic seizures with continuous EEG monitoring in critically ill patients. Neurology. 2004;62:1743-1748.
Trinka E, Cock H, Hesdorffer D, et al. A definition and classification of status epilepticus - report of the ILAE Task Force on Classification of Status Epilepticus. Epilepsia. 2015;56:1515-1523.
Rabinowicz AL, Correale JD, Bracht KA, Smith TD, DeGiorgio CM. Neuron-specific enolase is increased after nonconvulsive status epilepticus. Epilepsia. 1995;36:475-479.
Cockerell OC, Walker MC, Sander JWAS, Shorvon SD. Complex partial status epilepticus: a recurrent problem. J Neurol Neurosurg Psychiatry. 1994;57:835-837.
Guberman A, Cantu-Reyna G, Stuss D, Broughton R. Nonconvulsive generalized status epilepticus: clinical features, neuropsychological testing, and long-term follow-up. Neurology. 1986;36:1284-1291.
Kaplan PW. No, some types of nonconvulsive status epilepticus cause little permanent neurolooic sequelae (or: « The cure may be worse than the disease »). Neurophysiol Clin. 2000;30:377-382.
Gutierrez C, Chen M, Feng L, Tummala S. Non-convulsive seizures in the encephalopathic critically ill cancer patient does not necessarily portend a poor prognosis. J Intensive Care. 2019;7:1-9.
Sperk G. Kainic acid seizures in the rat. Prog Neurogibol. 1994;42:1-32.
Curia G, Longo D, Biagini G, Jones RSG, Avoli M. The pilocarpine model of temporal lobe epilepsy. J Neurosci Methods. 2008;172:143-157.
Lévesque M, Avoli M. The kainic acid model of temporal lobe epilepsy. Neurosci Biobehav Rev. 2013;37:2887-2899.
Sloviter RS. Hippocampal epileptogenesis in animal models of mesial temporal lobe epilepsy with hippocampal sclerosis: the importance of the “latent period” and other concepts. Epilepsia. 2008;49:85-92.
Henshall DC. Poststatus epilepticus models: focal kainic acid. In: Pitkänen A, Galanopoulou AS Buckmaster PS Moshé SL, eds. Models of Seizures and Epilepsy. 2nd ed. Cambridge, MA, USA: Academic Press. 2017:611-624.
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;112:101-111.
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;194:76-90.
Bouilleret V, Ridoux V, Depaulis A, et al. Recurrent seizures and hippocampal sclerosis following intrahippocampal kainate injection in adult mice: electroencephalography, histopathology and synaptic reorganization similar to mesial temporal lobe epilepsy. Neuroscience. 1999;89:717-729.
Tanaka T, Tanaka S, Fujita T, et al. Experimental complex partial seizures induced by a microinjection of kainic acid into limbic structures. Prog Neurogibol. 1992;38:317-334.
Ben-Ari Y, Tremblay E, Ottersen OP, Meldrum BS. The role of epileptic activity in hippocampal and “remote” cerebral lesions induced by kainic acid. Brain Res. 1980;5:515-518.
Schwob JE, Fuller T, Price JL, Olney JW. Widespread patterns of neuronal damage following systemic or intracerebral injections of kainic acid: a histological study. Neuroscience. 1980;5:991-1014.
Mouri G, Jimenez-Mateos E, Engel T, et al. Unilateral hippocampal CA3-predominant damage and short latency epileptogenesis after intra-amygdala microinjection of kainic acid in mice. Brain Res. 2008;1213:140-151.
Bedner P, Dupper A, Hüttmann K, et al. Astrocyte uncoupling as a cause of human temporal lobe epilepsy. Brain. 2015;138:1208-1222.
Pernot F, Heinrich C, Barbier L, et al. Inflammatory changes during epileptogenesis and spontaneous seizures in a mouse model of mesiotemporal lobe epilepsy. Epilepsia. 2011;52:2315-2325.
Ben-Ari Y. Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience. 1985;14:375-403.
Rattka M, Brandt C, Löscher W. The intrahippocampal kainate model of temporal lobe epilepsy revisited: epileptogenesis, behavioral and cognitive alterations, pharmacological response, and hippoccampal damage in epileptic rats. Epilepsy Res. 2013;103:135-152.
Sloviter RS. “Epileptic” brain damage in rats induced by sustained electrical stimulation of the perforant path. I. Acute electrophysiological and light microscopic studies. Brain Res Bull. 1983;10:675-697.
Lothman EW, Bertram EH, Bekenstein JW, Perlin JB. Self-sustaining limbic status epilepticus induced by “continuous” hippocampal stimulation: electrographic and behavioral characteristics. Epilepsy Res. 1989;3:107-119.
Mazarati AM, Wasterlain CG, Sankar R, Shin D. Self-sustaining status epilepticus after brief electrical stimulation of the perforant path. Brain Res. 1998;801:251-253.
Gorter JA, Van Vliet EA, Lopes da Silva FH, Isom LL, Aronica E. Sodium channel β1-subunit expression is increased in reactive astrocytes in a rat model for mesial temporal lobe epilepsy. Eur J Neurosci. 2002;16:360-364.
Avdic U, Ahl M, Chugh D, et al. Nonconvulsive status epilepticus in rats leads to brain pathology. Epilepsia. 2018;59:945-958.
Noè F, Cattalini A, Vila Verde D, et al. Epileptiform activity contralateral to unilateral hippocampal sclerosis does not cause the expression of brain damage markers. Epilepsia. 2019;1-16.
Carriero G, Arcieri S, Cattalini A, Corsi L, Gnatkovsky V, De Curtis M. A guinea pig model of mesial temporal lobe epilepsy following nonconvulsive status epilepticus induced by unilateral intrahippocampal injection of kainic acid. Epilepsia. 2012;53:1917-1927.
Arcieri S, Velotti R, Noè F, et al. Variable electrobehavioral patterns during focal nonconvulsive status epilepticus induced by unilateral intrahippocampal injection of kainic acid. Epilepsia. 2014;55:1978-1985.
Tavares G, Martins M, Correia JS, et al. Employing an open-source tool to assess astrocyte tridimensional structure. Brain Struct Funct. 2017;222:1989-1999.
van Scheppingen J, Iyer AM, Prabowo AS, et al. Expression of microRNAs miR21, miR146a, and miR155 in tuberous sclerosis complex cortical tubers and their regulation in human astrocytes and SEGA-derived cell cultures. Glia. 2016;64:1066-1082.
Racine RJ. Modification of seizure activity by electrical stimulation: II. Motor seizure. Electroencephalogr Clin Neurophysiol. 1972;32:281-294.
Noé FM, Bellistri E, Colciaghi F, et al. Kainic acid-induced albumin leak across the blood-brain barrier facilitates epileptiform hyperexcitability in limbic regions. Epilepsia. 2016;57:967-976.
Song Y, Gunnarson E. Potassium dependent regulation of astrocyte water permeability is mediated by camp signaling. PLoS One. 2012;7:e34936.
Mathern GW, Cifuentes F, Leite JP, Pretorius JK, Babb TL. Hippocampal EEG excitability and chronic spontaneous seizures are associated with aberrant synaptic reorganization in the rat intrahippocampal kainate model. Electroencephalogr Clin Neurophysiol. 1993;87:326-339.
Pollard H, Charriaut-Marlangue C, Cantagrel S, et al. Kainate-induced apoptotic cell death in hippocampal neurons. Neuroscience. 1994;63:7-18.
Pitkänen A, Kharatishvili I, Narkilahti S, Lukasiuk K, Nissinen J. Administration of diazepam during status epilepticus reduces development and severity of epilepsy in rat. Epilepsy Res. 2005;63:27-42.
Schmued LC, Albertson C, Slikker W. Fluoro-Jade: a novel fluorochrome for the sensitive and reliable histochemical localization of neuronal degeneration. Brain Res. 1997;751:37-46.
Johnson GVW, Jope RS. The role of microtubule-associated protein 2 (MAP-2) in neuronal growth, plasticity, and degeneration. J Neurosci Res. 1992;33:505-512.
Bertram EH, Lothman EW, Lenn NJ. The hippocampus in experimental chronic epilepsy: a morphometric analysis. Ann Neurol. 1990;27:43-48.
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;45:1024-1034.
Pitkänen A, Nissinen J, Nairismägi J, et al. Progression of neuronal damage after status epilepticus and during spontaneous seizures in a rat model of temporal lobe epilepsy. Prog Brain Res. 2002;135:67-83.
Rossini L, Garbelli R, Gnatkovsky V, et al. Seizure activity per se does not induce tissue damage markers in human neocortical focal epilepsy. Ann Neurol. 2017;82:331-341.
Cavazos JE, Das I, Sutula TP. Neuronal loss induced in limbic pathways by kindling: evidence for induction of hippocampal sclerosis by repeated brief seizures. J Neurosci. 1994;14:3106-3121.
French ED, Aldinio C, Schwarcz R. Intrahippocampal kainic acid, seizures and local neuronal degeneration: relationships assessed in unanesthetized rats. Neuroscience. 1982;7:2525-2536.
Vezzani A, Granata T. Brain inflammation in epilepsy: experimental and clinical evidence. Epilepsia. 2005;46:1724-1743.
Devinsky O, Vezzani A, O'Brien TJ, et al. Epilepsy. Nat Rev Dis Prim. 2018;4:18-24.
Binder DK, Steinhäuser C. Functional changes in astroglial cells in epilepsy. Glia. 2006;54:358-368.
Binder DK, Yao X, Zador Z, Sick TJ, Verkman AS, Manley GT. Increased seizure duration and slowed potassium kinetics in mice lacking aquaporin-4 water channels. Glia. 2006;53:631-636.
Seifert G, Steinhäuser C. Neuron-astrocyte signaling and epilepsy. Exp Neurol. 2013;244:4-10.
Steinhäuser C, Seifert G. Glial membrane channels and receptors in epilepsy: Impact for generation and spread of seizure activity. Eur J Pharmacol. 2002;447:227-237.