Cerebrospinal fluid and blood biomarkers of status epilepticus.
critical care
epilepsy
inflammation
neuronal injury
prognosis
Journal
Epilepsia
ISSN: 1528-1167
Titre abrégé: Epilepsia
Pays: United States
ID NLM: 2983306R
Informations de publication
Date de publication:
01 2020
01 2020
Historique:
received:
09
08
2019
revised:
12
11
2019
accepted:
12
11
2019
pubmed:
13
12
2019
medline:
11
7
2020
entrez:
13
12
2019
Statut:
ppublish
Résumé
Status epilepticus is a condition resulting either from the failure of the mechanisms responsible for seizure termination or from the initiation of mechanisms that lead to abnormally prolonged seizures and require urgent administration of antiepileptic drugs. Refractory status epilepticus requires anesthetics drugs and may lead to brain injury with molecular and cellular alterations (eg, inflammation, and neuronal and astroglial injury) that could induce neurologic sequels and further development of epilepsy. Outcome scores based on demographic, clinical, and electroencephalography (EEG) condition are available, allowing prediction of the risk of mortality, but the severity of brain injury in survivors is poorly evaluated. New biomarkers are needed to predict with higher accuracy the outcome of patients admitted with status in an intensive care unit. Here, we summarize the findings of studies from patients and animal models of status epilepticus. Specific protein markers can be detected in the cerebrospinal fluid and the blood. One of the first described markers of neuronal death is the neuron-specific enolase. Gliosis resulting from inflammatory responses after status can be detected through the increase of S100-beta, or some cytokines, like the High Mobility Group Box 1. Other proteins, like progranulin may reflect the neuroprotective mechanisms resulting from the brain adaptation to excitotoxicity. These new biomarkers aim to prospectively identify the severity and development of disability, and subsequent epilepsy of patients with status. We discuss the advantages and disadvantages of each biomarker, by evaluating their brain specificity, stability in the fluids, and sensitivity to external interferences, such as hemolysis. Finally, we emphasize the need for further development and validation of such biomarkers in order to better assess patients with severe status epilepticus.
Substances chimiques
Biomarkers
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
6-18Subventions
Organisme : Agence Nationale de la Recherche
ID : ANR-10-IAIHU-06
Pays : International
Informations de copyright
Wiley Periodicals, Inc. © 2019 International League Against Epilepsy.
Références
Fiest KM, Sauro KM, Wiebe S, Patten SB, Kwon CS, Dykeman J, et al. Prevalence and incidence of epilepsy: a systematic review and meta-analysis of international studies. Neurology. 2017;88:296-303.
Trinka E, Cock H, Hesdorffer D, Rossetti AO, Scheffer IE, Shinnar S, et al. A definition and classification of status epilepticus-Report of the ILAE Task Force on Classification of Status Epilepticus. Epilepsia. 2015;56:1515-23.
Rossetti AO, Lowenstein DH. Management of refractory status epilepticus in adults: still more questions than answers. Lancet Neurol. 2011;10:922-30.
Rossetti AO, Logroscino G, Bromfield EB. A clinical score for prognosis of status epilepticus in adults. Neurology. 2006;66:1736-8.
Leitinger M, Trinka E, Giovannini G, Zimmermann G, Florea C, Rohracher A, et al. Epidemiology of status epilepticus in adults: a population-based study on incidence, causes, and outcomes. Epilepsia. 2019;60:53-62.
Meletti S, Giovannini G, d'Orsi G, Toran L, Monti G, Guha R, et al. New-onset refractory status epilepticus with claustrum damage: definition of the clinical and neuroimaging features. Front Neurol. 2017;8:111.
Tschampa HJ, Greschus S, Sassen R, Bien CG, Urbach H. Thalamus lesions in chronic and acute seizure disorders. Neuroradiology. 2011;53:245-54.
Zetterberg H, Smith DH, Blennow K. Biomarkers of mild traumatic brain injury in cerebrospinal fluid and blood. Nat Rev Neurol. 2013;9:201-10.
Blennow K, Hampel H, Weiner M, Zetterberg H. Cerebrospinal fluid and plasma biomarkers in Alzheimer disease. Nat Rev Neurol. 2010;6:131-44.
Hall S, Surova Y, Öhrfelt A, Zetterberg H, Lindqvist D, Hansson O. CSF biomarkers and clinical progression of Parkinson disease. Neurology. 2015;84:57-63.
Link H, Huang Y-M. Oligoclonal bands in multiple sclerosis cerebrospinal fluid: an update on methodology and clinical usefulness. J Neuroimmunol. 2006;180:17-28.
Trinka E, Kälviäinen R. 25 years of advances in the definition, classification and treatment of status epilepticus. Seizure. 2017;44:65-73.
Ciurans J, Grau-López L, Jiménez M, Fumanal A, Misis M, Becerra JL. Refractory status epilepticus: Impact of baseline comorbidity and usefulness of STESS and EMSE scoring systems in predicting mortality and functional outcome. Seizure. 2018;56:98-103.
Alvarez V, Westover MB, Drislane FW, Dworetzky BA, Curley D, Lee JW, et al. Evaluation of a clinical tool for early etiology identification in status epilepticus. Epilepsia. 2014;55:2059-68.
Jun JS, Lee ST, Kim R, Chu K, Lee SK. Tocilizumab treatment for new onset refractory status epilepticus. Ann Neurol. 2018;84:940-5.
Meldrum BS, Horton RW. Physiology of status epilepticus in primates. Arch Neurol. 1973;28:1-9.
Huang CW, Cheng JT, Tsai JJ, Wu SN, Huang CC. Diabetic hyperglycemia aggravates seizures and status epilepticus-induced hippocampal damage. Neurotox Res. 2009;15:71-81.
Sutter R, Dittrich T, Semmlack S, Rüegg S, Marsch S, Kaplan PW. Acute systemic complications of convulsive status epilepticus-a systematic review. Crit Care Med. 2018;46:138-45.
Jutila L, Immonen A, Partanen K, Partanen J, Mervaala E, Ylinen A, et al. Neurobiology of epileptogenesis in the temporal lobe. Adv Tech Stand Neurosurg. 2002;27:5-22.
Brandt C, Gastens AM, Mz S, Hausknecht M, Löscher W. Treatment with valproate after status epilepticus: effect on neuronal damage, epileptogenesis, and behavioral alterations in rats. Neuropharmacology. 2006;51:789-804.
Sankar R, Shin DH, Wasterlain CG. Serum neuron-specific enolase is a marker for neuronal damage following status epilepticus in the rat. Epilepsy Res. 1997;28:129-36.
Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci Off J Soc Neurosci. 1997;17:3727-38.
Jakubs K, Nanobashvili A, Bonde S, Ekdahl CT, Kokaia Z, Kokaia M, et al. Environment matters: synaptic properties of neurons born in the epileptic adult brain develop to reduce excitability. Neuron. 2006;52:1047-59.
Huchtemann T, Körtvélyessy P, Feistner H, Heinze HJ, Bittner D. Progranulin levels in status epilepticus as a marker of neuronal recovery and neuroprotection. Epilepsy Behav. 2015;49:170-2.
Ravizza T, Gagliardi B, Noé F, Boer K, Aronica E, Vezzani A. Innate and adaptive immunity during epileptogenesis and spontaneous seizures: evidence from experimental models and human temporal lobe epilepsy. Neurobiol Dis. 2008;29:142-60.
Vezzani A, Baram TZ. New roles for interleukin-1 Beta in the mechanisms of epilepsy. Epilepsy Curr. 2007;7:45-50.
Gorter JA, van Vliet EA, Aronica E. Status epilepticus, blood-brain barrier disruption, inflammation, and epileptogenesis. Epilepsy Behav. 2015;49:13-6.
Calabrese VP, Gruemer HD, James K, Hranowsky N, DeLorenzo RJ. Cerebrospinal fluid lactate levels and prognosis in status epilepticus. Epilepsia. 1991;32:816-21.
Chatzikonstantinou A, Ebert AD, Hennerici MG. Cerebrospinal fluid findings after epileptic seizures. Epileptic Disord. 2015;17:453-9.
Sokrab TE, Kalimo H, Johansson BB. Endogenous serum albumin content in brain after short-lasting epileptic seizures. Brain Res. 1989;489:231-6.
Royds JA, Davies-Jones GA, Lewtas NA, Timperley WR, Taylor CB. Enolase isoenzymes in the cerebrospinal fluid of patients with diseases of the nervous system. J Neurol Neurosurg Psychiatry. 1983;46:1031-6.
Rabinowicz AL, Correale J, Boutros RB, Couldwell WT, Henderson CW, DeGiorgio CM. Neuron-specific enolase is increased after single seizures during inpatient video/EEG monitoring. Epilepsia. 1996;37:122-5.
Suzuki Y, Toribe Y, Goto M, Kato T, Futagi Y. Serum and CSF neuron-specific enolase in patients with West syndrome. Neurology. 1999;53:1761-4.
Tanabe T, Suzuki S, Hara K, Shimakawa S, Wakamiya E, Tamai H. Cerebrospinal fluid and serum neuron-specific enolase levels after febrile seizures. Epilepsia. 2001;42:504-7.
Correale J, Rabinowicz AL, Heck CN, Smith TD, Loskota WJ, DeGiorgio CM. Status epilepticus increases CSF levels of neuron-specific enolase and alters the blood-brain barrier. Neurology. 1998;50:1388-91.
DeGiorgio CM, Correale JD, Gott PS, Ginsburg DL, Bracht KA, Smith T, et al. Serum neuron-specific enolase in human status epilepticus. Neurology. 1995;45:1134-7.
DeGiorgio CM, Heck CN, Rabinowicz AL, Gott PS, Smith T, Correale J. Serum neuron-specific enolase in the major subtypes of status epilepticus. Neurology. 1999;52:746-9.
Maiti R, Mishra BR, Sanyal S, Mohapatra D, Parida S, Mishra A. Effect of carbamazepine and oxcarbazepine on serum neuron-specific enolase in focal seizures: A randomized controlled trial. Epilepsy Res. 2017;138:5-10.
Ramont L, Thoannes H, Volondat A, Chastang F, Millet MC, Maquart FX. Effects of hemolysis and storage condition on neuron-specific enolase (NSE) in cerebrospinal fluid and serum: implications in clinical practice. Clin Chem Lab Med. 2005;43:1215-7.
van Vliet EA, da Costa AS, Redeker S, van Schaik R, Aronica E, Gorter JA. Blood-brain barrier leakage may lead to progression of temporal lobe epilepsy. Brain J Neurol. 2007;130:521-34.
Tibbling G, Link H, Ohman S. Principles of albumin and IgG analyses in neurological disorders. I. Establishment of reference values. Scand J Clin Lab Invest. 1977;37:385-90.
Li YJ, Wang ZH, Zhang B, Zhe X, Wang MJ, Shi ST, et al. Disruption of the blood-brain barrier after generalized tonic-clonic seizures correlates with cerebrospinal fluid MMP-9 levels. J Neuroinflammation. 2013;10:80.
Donato R. S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int J Biochem Cell Biol. 2001;33:637-68.
Sen J, Belli A. S100B in neuropathologic states: the CRP of the brain? J Neurosci Res. 2007;85:1373-80.
Beaudeux J-L, Laribi S. S100B protein serum level as a biomarker of minor head injury. Ann Biol Clin (Paris). 2013;71:71-8.
Rezaei O, Pakdaman H, Gharehgozli K, Simani L, Vahedian-Azimi A, Asaadi S, et al. S100 B: A new concept in neurocritical care. Iran J Neurol. 2017;16:83-9.
Freund Y, Bloom B, Bokobza J, Baarir N, Laribi S, Harris T, et al. Predictive value of S100-B and copeptin for outcomes following seizure: the BISTRO International Cohort Study. PLoS One. 2015;10:e0122405.
Vizuete AFK, Hennemann MM, Gonçalves CA, de Oliveira DL. Phase-dependent astroglial alterations in Li-Pilocarpine-induced status epilepticus in young rats. Neurochem Res. 2017;42:2730-42.
Gurnett CA, Landt M, Wong M. Analysis of cerebrospinal fluid glial fibrillary acidic protein after seizures in children. Epilepsia. 2003;44:1455-8.
Chali F, Djelti F, Eugene E, Valderrama M, Marquer C, Aubourg P, et al. Inhibiting cholesterol degradation induces neuronal sclerosis and epileptic activity in mouse hippocampus. Eur J Neurosci. 2015;41:1345-55.
Maroso M, Balosso S, Ravizza T, Liu J, Aronica E, Iyer AM, et al. Toll-like receptor 4 and high-mobility group box-1 are involved in ictogenesis and can be targeted to reduce seizures. Nat Med. 2010;16:413-9.
Lehtimäki KA, Keränen T, Palmio J, Peltola J. Levels of IL-1-beta; and IL-1ra in cerebrospinal fluid of human patients after single and prolonged seizures. NeuroImmunoModulation. 2010;17:19-22.
Lehtimäki KA, Keränen T, Palmio J, Mäkinen R, Hurme M, Honkaniemi J, et al. Increased plasma levels of cytokines after seizures in localization-related epilepsy. Acta Neurol Scand. 2007;116:226-30.
Alapirtti T, Rinta S, Hulkkonen J, Mäkinen R, Keränen T, Peltola J. Interleukin-6, interleukin-1 receptor antagonist and interleukin-1beta production in patients with focal epilepsy: a video-EEG study. J Neurol Sci. 2009;280:94-7.
Shi LM, Chen RJ, Zhang H, Jiang CM, Gong J. Cerebrospinal fluid neuron specific enolase, interleukin-1β and erythropoietin concentrations in children after seizures. Childs Nerv Syst. 2017;33:805-11.
Lehtimäki KA, Peltola J, Koskikallio E, Keränen T, Honkaniemi J. Expression of cytokines and cytokine receptors in the rat brain after kainic acid-induced seizures. Brain Res Mol Brain Res. 2003;110:253-60.
Vezzani A, Conti M, De Luigi A, Ravizza T, Moneta D, Marchesi F, et al. Interleukin-1beta immunoreactivity and microglia are enhanced in the rat hippocampus by focal kainate application: functional evidence for enhancement of electrographic seizures. J Neurosci. 1999;19:5054-65.
Lehtimäki KA, Keränen T, Huhtala H, Hurme M, Ollikainen J, Honkaniemi J, et al. Regulation of IL-6 system in cerebrospinal fluid and serum compartments by seizures: the effect of seizure type and duration. J Neuroimmunol. 2004;152:121-5.
Palmio J, Suhonen J, Keränen T, Hulkkonen J, Peltola J, Pirttilä T. Cerebrospinal fluid tau as a marker of neuronal damage after epileptic seizure. Seizure. 2009;18:474-7.
Monti G, Tondelli M, Giovannini G, Bedin R, Nichelli PF, Trenti T, et al. Cerebrospinal fluid tau proteins in status epilepticus. Epilepsy Behav EB. 2015;49:150-4.
Whittington RA, Bretteville A, Virág L, Emala CW, Maurin TO, Marcouiller F, et al. Anesthesia-induced hypothermia mediates decreased ARC gene and protein expression through ERK/MAPK inactivation. Sci Rep. 2013;3:1388.
Rejdak K, Kuhle J, Rüegg S, Lindberg RL, Petzold A, Sulejczak D, et al. Neurofilament heavy chain and heat shock protein 70 as markers of seizure-related brain injury. Epilepsia. 2012;53:922-7.
Zhu S, Tai C, Petkau TL, Zhang S, Liao C, Dong Z, et al. Progranulin promotes activation of microglia/macrophage after pilocarpine-induced status epilepticus. Brain Res. 2013;1530:54-65.
Lenzer-Fanara JR, Li T, Salerni EA, Payen F, Croll SD. VEGF treatment during status epilepticus attenuates long-term seizure-associated alterations in astrocyte morphology. Epilepsy Behav. 2017;70:33-44.
Simonato M, Zucchini S. Are the neurotrophic factors a suitable therapeutic target for the prevention of epileptogenesis? Epilepsia. 2010;51:48-51.
Raoof R, Jimenez-Mateos EM, Bauer S, Tackenberg B, Rosenow F, Lang J, et al. Cerebrospinal fluid microRNAs are potential biomarkers of temporal lobe epilepsy and status epilepticus. Sci Rep. 2017;7:3328.
Valenza M, Cattaneo E. Cholesterol dysfunction in neurodegenerative diseases: is Huntington’s disease in the list? Prog Neurogibol. 2006;80:165-76.
Meletti S, Lucchi C, Monti G, Giovannini G, Bedin R, Trenti T, et al. Decreased allopregnanolone levels in cerebrospinal fluid obtained during status epilepticus. Epilepsia. 2017;58:e16-20.
Meletti S, Lucchi C, Monti G, Giovannini G, Bedin R, Trenti T, et al. Low levels of progesterone and derivatives in cerebrospinal fluid of patients affected by status epilepticus. J Neurochem. 2018;147:275-84.
Vaitkevicius H, Husain AM, Rosenthal ES, Rosand J, Bobb W, Reddy K, et al. First-in-man allopregnanolone use in super-refractory status epilepticus. Ann Clin Transl Neurol. 2017;4:411-4.
Rosenthal ES, Claassen J, Wainwright MS, Husain AM, Vaitkevicius H, Raines S, et al. Brexanolone as adjunctive therapy in super-refractory status epilepticus. Ann Neurol. 2017;82:342-52.
Ng GJL, Quek AML, Cheung C, Arumugam TV, Seet RCS. Stroke biomarkers in clinical practice: a critical appraisal. Neurochem Int. 2017;107:11-22.
van Engelen TSR, Wiersinga WJ, Scicluna BP, van der Poll T. Biomarkers in sepsis. Crit Care Clin. 2018;34:139-52.
Gnanapavan S, Hegen H, Khalil M, Hemmer B, Franciotta D, Hughes S, et al. Guidelines for uniform reporting of body fluid biomarker studies in neurologic disorders. Neurology. 2014;83:1210-6.
Simon RM, Paik S, Hayes DF. Use of archived specimens in evaluation of prognostic and predictive biomarkers. J Natl Cancer Inst. 2009;101:1446-52.