{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T16:13:51Z","timestamp":1791994431338,"version":"4.4.0"},"reference-count":103,"publisher":"MDPI AG","issue":"15","license":[{"start":{"date-parts":[[2023,8,7]],"date-time":"2023-08-07T00:00:00Z","timestamp":1691366400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>As per the latest ILAE definition, status epilepticus (SE) may lead to long-term irreversible consequences, such as neuronal death, neuronal injury, and alterations in neuronal networks. Consequently, there is growing interest in identifying biomarkers that can demonstrate and quantify the extent of neuronal and glial injury. Despite numerous studies conducted on animal models of status epilepticus, which clearly indicate seizure-induced neuronal and glial injury, as well as signs of atrophy and gliosis, evidence in humans remains limited to case reports and small case series. The implications of identifying such biomarkers in clinical practice are significant, including improved prognostic stratification of patients and the early identification of those at high risk of developing irreversible complications. Moreover, the clinical validation of these biomarkers could be crucial in promoting neuroprotective strategies in addition to antiseizure medications. In this study, we present a systematic review of research on biomarkers of neuro-glial injury in patients with status epilepticus.<\/jats:p>","DOI":"10.3390\/ijms241512519","type":"journal-article","created":{"date-parts":[[2023,8,7]],"date-time":"2023-08-07T06:37:31Z","timestamp":1691390251000},"page":"12519","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":25,"title":["Fluid Biomarkers of Neuro-Glial Injury in Human Status Epilepticus: A Systematic Review"],"prefix":"10.3390","volume":"24","author":[{"given":"Giada","family":"Giovannini","sequence":"first","affiliation":[{"name":"Neurology Department, Azienda Ospedaliera-Universitaria di Modena, 41126 Modena, Italy"},{"name":"PhD Program in Clinical and Experimental Medicine, University of Modena and Reggio-Emilia, 41121 Modena, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0334-539X","authenticated-orcid":false,"given":"Stefano","family":"Meletti","sequence":"additional","affiliation":[{"name":"Neurology Department, Azienda Ospedaliera-Universitaria di Modena, 41126 Modena, Italy"},{"name":"Department of Biomedical, Metabolic and Neural Sciences, University of Modena and Reggio-Emilia, 41121 Modena, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,8,7]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"104456","DOI":"10.1016\/j.ebiom.2023.104456","article-title":"A Unified Classification Approach Rating Clinical Utility of Protein Biomarkers across Neurologic Diseases","volume":"89","author":"Bernhardt","year":"2023","journal-title":"eBioMedicine"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1515","DOI":"10.1111\/epi.13121","article-title":"A Definition and Classification of Status Epilepticus\u2014Report of the ILAE Task Force on Classification of Status Epilepticus","volume":"56","author":"Trinka","year":"2015","journal-title":"Epilepsia"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1111\/epi.16405","article-title":"Cerebrospinal Fluid and Blood Biomarkers of Status Epilepticus","volume":"61","author":"Hanin","year":"2020","journal-title":"Epilepsia"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"5868","DOI":"10.1007\/s00415-022-11199-4","article-title":"Clinico-Biological Markers for the Prognosis of Status Epilepticus in Adults","volume":"269","author":"Hanin","year":"2022","journal-title":"J. Neurol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"4048","DOI":"10.1021\/acschemneuro.0c00492","article-title":"Elevated Blood-Based Brain Biomarker Levels in Patients with Epileptic Seizures: A Systematic Review and Meta-Analysis","volume":"11","author":"Simani","year":"2020","journal-title":"ACS Chem. Neurosci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1111\/epi.13965","article-title":"Commonalities in Epileptogenic Processes from Different Acute Brain Insults: Do They Translate?","volume":"59","author":"Klein","year":"2018","journal-title":"Epilepsia"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"106275","DOI":"10.1016\/j.yebeh.2019.04.028","article-title":"Inflammation and Reactive Oxygen Species in Status Epilepticus: Biomarkers and Implications for Therapy","volume":"101","author":"Terrone","year":"2019","journal-title":"Epilepsy Behav."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1111\/nan.12444","article-title":"Review: Neuroinflammatory Pathways as Treatment Targets and Biomarker Candidates in Epilepsy: Emerging Evidence from Preclinical and Clinical Studies","volume":"44","author":"Aronica","year":"2018","journal-title":"Neuropathol. Appl. Neurobiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1081","DOI":"10.1586\/14737175.2015.1079130","article-title":"Immunity and Inflammation in Status Epilepticus and Its Sequelae: Possibilities for Therapeutic Application","volume":"15","author":"Vezzani","year":"2015","journal-title":"Expert Rev. Neurother."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"l6890","DOI":"10.1136\/bmj.l6890","article-title":"Synthesis without Meta-Analysis (SWiM) in Systematic Reviews: Reporting Guideline","volume":"368","author":"Campbell","year":"2020","journal-title":"BMJ"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"n71","DOI":"10.1136\/bmj.n71","article-title":"The PRISMA 2020 Statement: An Updated Guideline for Reporting Systematic Reviews","volume":"372","author":"Page","year":"2021","journal-title":"BMJ"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1956","DOI":"10.1161\/01.STR.28.10.1956","article-title":"S-100 Protein and Neuron-Specific Enolase Concentrations in Blood as Indicators of Infarction Volume and Prognosis in Acute Ischemic Stroke","volume":"28","author":"Missler","year":"1997","journal-title":"Stroke"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1007\/s00134-002-1573-2","article-title":"Serum Neuron-Specific Enolase Predicts Outcome in Post-Anoxic Coma: A Prospective Cohort Study","volume":"29","author":"Meynaar","year":"2003","journal-title":"Intensiv. Care Med."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1016\/S0920-1211(97)00040-5","article-title":"Serum Neuron-Specific Enolase Is a Marker for Neuronal Damage Following Status Epilepticus in the Rat","volume":"28","author":"Sankar","year":"1997","journal-title":"Epilepsy Res."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1006\/exnr.1999.7147","article-title":"Expression of Neuron-Specific Enolase in Adult Rat Brain Following Status Epilepticus","volume":"159","author":"Schreiber","year":"1999","journal-title":"Exp. Neurol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1134","DOI":"10.1212\/WNL.45.6.1134","article-title":"Serum Neuron-Specific Enolase in Human Status Epilepticus","volume":"45","author":"DeGiorgio","year":"1995","journal-title":"Neurology"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"606","DOI":"10.1111\/j.1528-1157.1996.tb00623.x","article-title":"Neuron-Specific Enolase, a Marker of Acute Neuronal Injury, Is Increased in Complex Partial Status Epilepticus","volume":"37","author":"DeGiorgio","year":"1996","journal-title":"Epilepsia"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"746","DOI":"10.1212\/WNL.52.4.746","article-title":"Serum Neuron-Specific Enolase in the Major Subtypes of Status Epilepticus","volume":"52","author":"DeGiorgio","year":"1999","journal-title":"Neurology"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"475","DOI":"10.1111\/j.1528-1157.1995.tb00489.x","article-title":"Neuron-Specific Enolase Is Increased After Nonconvulsive Status Epilepticus","volume":"36","author":"Rabinowicz","year":"1995","journal-title":"Epilepsia"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1388","DOI":"10.1212\/WNL.50.5.1388","article-title":"Status Epilepticus Increases CSF Levels of Neuron-Specific Enolase and Alters the Blood-Brain Barrier","volume":"50","author":"Correale","year":"1998","journal-title":"Neurology"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"3752","DOI":"10.1007\/s00415-022-11004-2","article-title":"Neuron Specific Enolase, S100-Beta Protein and Progranulin as Diagnostic Biomarkers of Status Epilepticus","volume":"269","author":"Hanin","year":"2022","journal-title":"J. Neurol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/j.neucli.2021.01.006","article-title":"Continuous EEG Monitoring in the Follow-up of Convulsive Status Epilepticus Patients: A Proposal and Preliminary Validation of an EEG-Based Seizure Build-up Score (EaSiBUSSEs)","volume":"51","author":"Hanin","year":"2021","journal-title":"Neurophysiol. Clin."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1177\/088307380201700404","article-title":"Cerebrospinal Fluid Neuron-Specific Enolase Following Seizures in Children: Role of Etiology","volume":"17","author":"Wong","year":"2002","journal-title":"J. Child Neurol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1498","DOI":"10.1046\/j.1528-1157.2002.10502.x","article-title":"Lack of Neuronal Damage in Atypical Absence Status Epilepticus","volume":"43","author":"Shirasaka","year":"2002","journal-title":"Epilepsia"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1016\/S1090-3798(98)80019-6","article-title":"Serum Neuron Specific Enolase: A Marker for Neuronal Dysfunction in Children with Continuous EEG Epileptiform Activity","volume":"2","author":"Brown","year":"1998","journal-title":"Eur. J. Paediatr. Neurol."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Wang, M., Yu, J., Xiao, X., Zhang, B., and Tang, J. (2022). Changes of Biochemical Biomarkers in the Serum of Children with Convulsion Status Epilepticus: A Prospective Study. BMC Neurol., 22.","DOI":"10.1186\/s12883-022-02686-2"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"2453","DOI":"10.1089\/neu.2010.1653","article-title":"Elevated Serum Ubiquitin Carboxy-Terminal Hydrolase L1 Is Associated with Abnormal Blood\u2013Brain Barrier Function after Traumatic Brain Injury","volume":"28","author":"Blyth","year":"2011","journal-title":"J. Neurotrauma"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1475","DOI":"10.1002\/jnr.22323","article-title":"Identification and Preliminary Characterization of Ubiquitin C Terminal Hydrolase 1 (UCHL1) as a Biomarker of Neuronal Loss in Aneurysmal Subarachnoid Hemorrhage","volume":"88","author":"Lewis","year":"2010","journal-title":"J. Neurosci. Res."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"861","DOI":"10.1089\/neu.2010.1564","article-title":"Biokinetic Analysis of Ubiquitin C-Terminal Hydrolase-L1 (UCH-L1) in Severe Traumatic Brain Injury Patient Biofluids","volume":"28","author":"Brophy","year":"2011","journal-title":"J. Neurotrauma"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1016\/j.jneuroim.2019.03.018","article-title":"The Role of UCH-L1, MMP-9, and GFAP as Peripheral Markers of Different Susceptibility to Seizure Development in a Preclinical Model of Epilepsy","volume":"332","author":"Chmielewska","year":"2019","journal-title":"J. Neuroimmunol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"2033","DOI":"10.1007\/s11064-017-2260-6","article-title":"Proteomic Analysis After Status Epilepticus Identifies UCHL1 as Protective Against Hippocampal Injury","volume":"42","author":"Reynolds","year":"2017","journal-title":"Neurochem. Res."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.brainres.2018.09.028","article-title":"The Diagnostic Value of Serum UCHL-1 and S100-B Levels in Differentiate Epileptic Seizures from Psychogenic Attacks","volume":"1704","author":"Asadollahi","year":"2019","journal-title":"Brain Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"424","DOI":"10.1590\/0004-282x20200040","article-title":"Evaluation of Ubiquitin C-Terminal Hydrolase-L1 Enzyme Levels in Patients with Epilepsy","volume":"78","author":"Yasak","year":"2020","journal-title":"Arq. Neuro-Psiquiatr."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"879","DOI":"10.1007\/s00381-020-04920-z","article-title":"Circulating Glial Fibrillary Acidic Protein and Ubiquitin Carboxy-Terminal Hydrolase-L1 as Markers of Neuronal Damage in Children with Epileptic Seizures","volume":"37","author":"Elhady","year":"2021","journal-title":"Childs Nerv. Syst."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Mondello, S., Palmio, J., Streeter, J., Hayes, R.L., Peltola, J., and Jeromin, A. (2012). Ubiquitin Carboxy-Terminal Hydrolase L1 (UCH-L1) Is Increased in Cerebrospinal Fluid and Plasma of Patients after Epileptic Seizure. BMC Neurol., 12.","DOI":"10.1186\/1471-2377-12-85"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1016\/j.eplepsyres.2012.08.001","article-title":"Cerebrospinal Fluid Ubiquitin C-Terminal Hydrolase as a Novel Marker of Neuronal Damage after Epileptic Seizure","volume":"103","author":"Li","year":"2013","journal-title":"Epilepsy Res."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"308","DOI":"10.3389\/fnagi.2019.00308","article-title":"Tau Phosphorylation in a Mouse Model of Temporal Lobe Epilepsy","volume":"11","author":"Alves","year":"2019","journal-title":"Front. Aging Neurosci."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"474","DOI":"10.1016\/j.seizure.2009.04.006","article-title":"Cerebrospinal Fluid Tau as a Marker of Neuronal Damage after Epileptic Seizure","volume":"18","author":"Palmio","year":"2009","journal-title":"Seizure"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/j.pediatrneurol.2013.02.015","article-title":"Cerebrospinal Fluid Brain Injury Biomarkers in Children: A Multicenter Study","volume":"49","author":"Shahim","year":"2013","journal-title":"Pediatr. Neurol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"486","DOI":"10.1111\/ene.12336","article-title":"Cerebrospinal Fluid Biomarkers of \u03b2-Amyloid Metabolism and Neuronal Damage in Epileptic Seizures","volume":"21","author":"Shahim","year":"2014","journal-title":"Eur. J. Neurol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"150","DOI":"10.1016\/j.yebeh.2015.04.030","article-title":"Cerebrospinal Fluid Tau Proteins in Status Epilepticus","volume":"49","author":"Monti","year":"2015","journal-title":"Epilepsy Behav."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/j.eplepsyres.2015.04.004","article-title":"Effect of Epileptic Seizures on the Cerebrospinal Fluid\u2014A Systematic Retrospective Analysis","volume":"114","author":"Tumani","year":"2015","journal-title":"Epilepsy Res."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1188","DOI":"10.1111\/ped.12995","article-title":"Diagnostic and Prognostic Factors for Acute Encephalopathy","volume":"58","author":"Motojima","year":"2016","journal-title":"Pediatr. Int."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"782","DOI":"10.1080\/00207454.2021.1976172","article-title":"Role of Cerebrospinal Fluid Tau Protein Levels as a Biomarker of Brain Injury in Pediatric Status Epilepticus","volume":"133","author":"Sood","year":"2021","journal-title":"Int. J. Neurosci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"a018309","DOI":"10.1101\/cshperspect.a018309","article-title":"Neurofilaments and Neurofilament Proteins in Health and Disease","volume":"9","author":"Yuan","year":"2017","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1038\/s41398-018-0194-7","article-title":"Neurofilament Light Interaction with GluN1 Modulates Neurotransmission and Schizophrenia-Associated Behaviors","volume":"8","author":"Yuan","year":"2018","journal-title":"Transl. Psychiatry"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1975","DOI":"10.1093\/brain\/awaa098","article-title":"Neurofilaments: Neurobiological Foundations for Biomarker Applications","volume":"143","author":"Gafson","year":"2020","journal-title":"Brain"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1186\/s13195-019-0562-4","article-title":"CSF Biomarkers of Neuroinflammation in Distinct Forms and Subtypes of Neurodegenerative Dementia","volume":"12","author":"Steinacker","year":"2020","journal-title":"Alzheimer\u2019s Res. Ther."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"106432","DOI":"10.1016\/j.yebeh.2019.07.033","article-title":"Serum Neurofilament Light Chain as a Prognostic Marker in Postanoxic Encephalopathy","volume":"101","author":"Disanto","year":"2019","journal-title":"Epilepsy Behav."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"e679","DOI":"10.1212\/NXI.0000000000000679","article-title":"Association of Intrathecal Pleocytosis and IgG Synthesis with Axonal Damage in Early MS","volume":"7","author":"Engel","year":"2020","journal-title":"Neurol.-Neuroimmunol. Neuroinflamm."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1270","DOI":"10.1177\/1352458518791518","article-title":"Are Neurofilaments Valuable Biomarkers for Long-Term Disease Prognostication in MS?","volume":"24","author":"Khalil","year":"2018","journal-title":"Mult. Scler."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1038\/s41582-018-0058-z","article-title":"Neurofilaments as Biomarkers in Neurological Disorders","volume":"14","author":"Khalil","year":"2018","journal-title":"Nat. Rev. Neurol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1757","DOI":"10.1093\/hmg\/3.10.1757","article-title":"Variants of the Heavy Neurofilament Subunit Are Associated with the Development of Amyotrophic Lateral Sclerosis","volume":"3","author":"Figlewicz","year":"1994","journal-title":"Hum. Mol. Genet."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1136\/jnnp-2016-315077","article-title":"Genetic and Clinical Characteristics of NEFL -Related Charcot-Marie-Tooth Disease","volume":"88","author":"Horga","year":"2017","journal-title":"J. Neurol. Neurosurg. Psychiatry"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"2349","DOI":"10.1038\/npp.2014.81","article-title":"Elevated Concentrations of Neurofilament Light Chain in the Cerebrospinal Fluid of Bipolar Disorder Patients","volume":"39","author":"Jakobsson","year":"2014","journal-title":"Neuropsychopharmacology"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1002\/ana.24954","article-title":"Serum Neurofilament Light: A Biomarker of Neuronal Damage in Multiple Sclerosis: Serum NfL as a Biomarker in MS","volume":"81","author":"Disanto","year":"2017","journal-title":"Ann. Neurol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1016\/0006-8993(95)00109-4","article-title":"Non-Phosphorylated Neurofilament Protein Imrnunoreactivity in Adult and Developing Rat Hippocampus: Specificity and Appfication in Grafting Studies","volume":"676","author":"Sherry","year":"1995","journal-title":"Brain Res."},{"key":"ref_58","first-page":"57","article-title":"Plasticity of Granule Cell-Mossy Fiber System Following Kainic Acid Induced Seizures: An Immunocytochemical Study on Neurofilament Proteins","volume":"26","author":"Yang","year":"1996","journal-title":"Neurosci. Res."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1016\/j.nbd.2004.08.004","article-title":"Resistance of Neurofilaments to Degradation, and Lack of Neuronal Death and Mossy Fiber Sprouting after Kainic Acid-Induced Status Epilepticus in the Developing Rat Hippocampus","volume":"17","author":"Lopezpicon","year":"2004","journal-title":"Neurobiol. Dis."},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Custers, M., Vyver, M.V., Kaltenb\u00f6ck, L., Barb\u00e9, K., Bjerke, M., Van Eeckhaut, A., and Smolders, I. (2023). Neurofilament Light Chain\u2014A Possible Fluid Biomarker in the Intrahippocampal Kainic Acid Mouse Model for Chronic Epilepsy?. Epilepsia, epi.17669.","DOI":"10.1111\/epi.17669"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"922","DOI":"10.1111\/j.1528-1167.2012.03459.x","article-title":"Neurofilament Heavy Chain and Heat Shock Protein 70 as Markers of Seizure-Related Brain Injury: Seizure-Related Neurodegeneration","volume":"53","author":"Rejdak","year":"2012","journal-title":"Epilepsia"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1016\/j.resuscitation.2020.10.027","article-title":"Postanoxic Electrographic Status Epilepticus and Serum Biomarkers of Brain Injury","volume":"158","author":"Lybeck","year":"2021","journal-title":"Resuscitation"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"e23","DOI":"10.1111\/epi.17132","article-title":"Serum Neurofilament Light as Biomarker of Seizure-Related Neuronal Injury in Status Epilepticus","volume":"63","author":"Giovannini","year":"2022","journal-title":"Epilepsia"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"109131","DOI":"10.1016\/j.yebeh.2023.109131","article-title":"Neuro-Glial Degeneration in Status Epilepticus: Exploring the Role of Serum Levels of Neurofilament Light Chains and S100B as Prognostic Biomarkers for Short-Term Functional Outcome","volume":"140","author":"Giovannini","year":"2023","journal-title":"Epilepsy Behav."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"2128","DOI":"10.1007\/s00415-022-11547-4","article-title":"Neurofilament Light (NfL) as Biomarker in Serum and CSF in Status Epilepticus","volume":"270","author":"Margraf","year":"2023","journal-title":"J. Neurol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"265","DOI":"10.2174\/1570159X18666200729100427","article-title":"Targeting S100B Protein as a Surrogate Biomarker and Its Role in Various Neurological Disorders","volume":"19","author":"Langeh","year":"2020","journal-title":"Curr. Neuropharmacol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1111\/jnc.14574","article-title":"The S100B Story: From Biomarker to Active Factor in Neural Injury","volume":"148","author":"Michetti","year":"2019","journal-title":"J. Neurochem."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"723","DOI":"10.1097\/00004647-200206000-00011","article-title":"Astrocytic Activation and Delayed Infarct Expansion after Permanent Focal Ischemia in Rats. Part II: Suppression of Astrocytic Activation by a Novel Agent (R)-(\u2212)-2-Propyloctanoic Acid (ONO-2506) Leads to Mitigation of Delayed Infarct Expansion and Early Improvement of Neurologic Deficits","volume":"22","author":"Tateishi","year":"2002","journal-title":"J. Cereb. Blood Flow Metab."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"3976","DOI":"10.1007\/s12035-015-9336-6","article-title":"S100B as a Potential Biomarker and Therapeutic Target in Multiple Sclerosis","volume":"53","author":"Barateiro","year":"2016","journal-title":"Mol. Neurobiol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"2010","DOI":"10.1038\/jcbfm.2015.165","article-title":"S100B Inhibition Reduces Behavioral and Pathologic Changes in Experimental Traumatic Brain Injury","volume":"35","author":"Kabadi","year":"2015","journal-title":"J. Cereb. Blood Flow Metab."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"508342","DOI":"10.1155\/2015\/508342","article-title":"S100B Inhibitor Pentamidine Attenuates Reactive Gliosis and Reduces Neuronal Loss in a Mouse Model of Alzheimer\u2019s Disease","volume":"2015","author":"Cirillo","year":"2015","journal-title":"BioMed Res. Int."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"e2185","DOI":"10.1212\/WNL.0000000000012918","article-title":"Role of S100B Serum Concentration as a Surrogate Outcome Parameter After Mechanical Thrombectomy","volume":"97","author":"Luger","year":"2021","journal-title":"Neurology"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"915","DOI":"10.1016\/S0197-4580(01)00293-7","article-title":"The Role of Activated Astrocytes and of the Neurotrophic Cytokine S100B in the Pathogenesis of Alzheimer\u2019s Disease","volume":"22","author":"Mrak","year":"2001","journal-title":"Neurobiol. Aging"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"3336","DOI":"10.1093\/brain\/aws250","article-title":"S100B Is Increased in Parkinson\u2019s Disease and Ablation Protects against MPTP-Induced Toxicity through the RAGE and TNF-\u03b1 Pathway","volume":"135","author":"Sathe","year":"2012","journal-title":"Brain"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1016\/j.nbd.2017.07.014","article-title":"Cytokine Profiling in the Prefrontal Cortex of Parkinson\u2019s Disease and Multiple System Atrophy Patients","volume":"106","author":"Rydbirk","year":"2017","journal-title":"Neurobiol. Dis."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"4430","DOI":"10.1038\/ncomms5430","article-title":"Role of Astroglia in Down\u2019s Syndrome Revealed by Patient-Derived Human-Induced Pluripotent Stem Cells","volume":"5","author":"Chen","year":"2014","journal-title":"Nat. Commun."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"868","DOI":"10.1016\/j.jpsychires.2007.10.001","article-title":"S100B-Immunopositive Glia Is Elevated in Paranoid as Compared to Residual Schizophrenia: A Morphometric Study","volume":"42","author":"Steiner","year":"2008","journal-title":"J. Psychiatr. Res."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"842","DOI":"10.1111\/j.1528-1167.2007.01484.x","article-title":"Effects of Early-Life LiCl-Pilocarpine-Induced Status Epilepticus on Memory and Anxiety in Adult Rats Are Associated with Mossy Fiber Sprouting and Elevated CSF S100B Protein","volume":"49","author":"Fischer","year":"2008","journal-title":"Epilepsia"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/j.seizure.2012.10.012","article-title":"Elevated Serum S-100B Levels in Children with Temporal Lobe Epilepsy","volume":"22","author":"Calik","year":"2013","journal-title":"Seizure"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"456","DOI":"10.3389\/fnins.2019.00456","article-title":"Increased Serum S100B Levels in Patients With Epilepsy: A Systematic Review and Meta-Analysis Study","volume":"13","author":"Liang","year":"2019","journal-title":"Front. Neurosci."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"482","DOI":"10.1007\/s12031-018-1164-5","article-title":"Altered S100 Calcium-Binding Protein B and Matrix Metallopeptidase 9 as Biomarkers of Mesial Temporal Lobe Epilepsy with Hippocampus Sclerosis","volume":"66","author":"Meguid","year":"2018","journal-title":"J. Mol. Neurosci."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"281","DOI":"10.3345\/kjp.2018.07017","article-title":"Correlation of Serum S100B Levels with Brain Magnetic Resonance Imaging Abnormalities in Children with Status Epilepticus","volume":"62","author":"Gunawan","year":"2019","journal-title":"Korean J. Pediatr."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1016\/j.brainres.2012.06.008","article-title":"Neuronal Degeneration and Gliosis Time-Course in the Mouse Hippocampal Formation after Pilocarpine-Induced Status Epilepticus","volume":"1470","author":"Langone","year":"2012","journal-title":"Brain Res."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"945","DOI":"10.1111\/epi.14070","article-title":"Nonconvulsive Status Epilepticus in Rats Leads to Brain Pathology","volume":"59","author":"Avdic","year":"2018","journal-title":"Epilepsia"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"416","DOI":"10.1016\/j.expneurol.2006.04.031","article-title":"Degeneration and Proliferation of Astrocytes in the Mouse Dentate Gyrus after Pilocarpine-Induced Status Epilepticus","volume":"201","author":"Borges","year":"2006","journal-title":"Exp. Neurol."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1002\/glia.440120302","article-title":"Loss of Immunoreactivity for Glial Fibrillary Acidic Protein (GFAP) in Astrocytes as a Marker for Profound Tissue Damage in Substantia Nigra and Basal Cortical Areas after Status Epilepticus Induced by Pilocarpine in Rat","volume":"12","author":"Ingvar","year":"1994","journal-title":"Glia"},{"key":"ref_87","doi-asserted-by":"crossref","unstructured":"Griflyuk, A.V., Postnikova, T.Y., and Zaitsev, A.V. (2022). Prolonged Febrile Seizures Impair Synaptic Plasticity and Alter Developmental Pattern of Glial Fibrillary Acidic Protein (GFAP)-Immunoreactive Astrocytes in the Hippocampus of Young Rats. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms232012224"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.seizure.2020.12.009","article-title":"Serum Biomarkers of Cerebral Cellular Stress after Self-Limiting Tonic Clonic Seizures: An Exploratory Study","volume":"85","author":"Nass","year":"2021","journal-title":"Seizure"},{"key":"ref_89","doi-asserted-by":"crossref","unstructured":"Akel, S., Asztely, F., Banote, R.K., Axelsson, M., Zetterberg, H., and Zelano, J. (2023). Neurofilament Light, Glial Fibrillary Acidic Protein, and Tau in a Regional Epilepsy Cohort: High Plasma Levels Are Rare but Related to Seizures. Epilepsia, epi.17713.","DOI":"10.1111\/epi.17713"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"1455","DOI":"10.1046\/j.1528-1157.2003.21603.x","article-title":"Analysis of Cerebrospinal Fluid Glial Fibrillary Acidic Protein after Seizures in Children","volume":"44","author":"Gurnett","year":"2003","journal-title":"Epilepsia"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/j.neuroscience.2013.07.045","article-title":"Neuronal Degeneration Is Observed in Multiple Regions Outside the Hippocampus after Lithium Pilocarpine-Induced Status Epilepticus in the Immature Rat","volume":"252","author":"Scholl","year":"2013","journal-title":"Neuroscience"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"449","DOI":"10.1007\/s004010000305","article-title":"Expression of Connexin 43 and Connexin 32 Gap-Junction Proteins in Epilepsy-Associated Brain Tumors and in the Perilesional Epileptic Cortex","volume":"101","author":"Aronica","year":"2001","journal-title":"Acta Neuropathol."},{"key":"ref_93","doi-asserted-by":"crossref","unstructured":"Bedner, P., and Steinh\u00e4user, C. (2023). Role of Impaired Astrocyte Gap Junction Coupling in Epileptogenesis. Cells, 12.","DOI":"10.20944\/preprints202301.0531.v1"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/j.yebeh.2019.06.023","article-title":"Assessment of Genes Involved in Behavior, Learning, Memory, and Synaptic Plasticity Following Status Epilepticus in Rats","volume":"98","author":"Bayramov","year":"2019","journal-title":"Epilepsy Behav."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"767","DOI":"10.1007\/s13311-023-01355-7","article-title":"Molecular Biomarkers of Neuronal Injury in Epilepsy Shared with Neurodegenerative Diseases","volume":"20","author":"Negi","year":"2023","journal-title":"Neurotherapeutics"},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1046\/j.1528-1157.43.s.5.39.x","article-title":"Delayed Sclerosis, Neuroprotection, and Limbic Epileptogenesis After Status Epilepticus in the Rat","volume":"43","author":"Ebert","year":"2002","journal-title":"Epilepsia"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"1024","DOI":"10.1111\/j.0013-9580.2004.08904.x","article-title":"Progression of Brain Damage after Status Epilepticus and Its Association with Epileptogenesis: A Quantitative MRI Study in a Rat Model of Temporal Lobe Epilepsy","volume":"45","author":"Nairismagi","year":"2004","journal-title":"Epilepsia"},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"919","DOI":"10.1111\/epi.17186","article-title":"Seizure Activity Triggers Tau Hyperphosphorylation and Amyloidogenic Pathways","volume":"63","author":"Canet","year":"2022","journal-title":"Epilepsia"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1016\/j.jns.2013.08.016","article-title":"Histopathological Evidence That Hippocampal Atrophy Following Status Epilepticus Is a Result of Neuronal Necrosis","volume":"334","author":"Kumar","year":"2013","journal-title":"J. Neurol. Sci."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"1201","DOI":"10.1001\/jamaneurol.2016.1572","article-title":"Progressive Brain Atrophy in Super-Refractory Status Epilepticus","volume":"73","author":"Hocker","year":"2016","journal-title":"JAMA Neurol."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"901","DOI":"10.1016\/j.seizure.2013.07.012","article-title":"Pathology of Bilateral Pulvinar Degeneration Following Long Duration Status Epilepticus","volume":"22","author":"Hariri","year":"2013","journal-title":"Seizure"},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1016\/j.nbd.2013.07.015","article-title":"Pharmacological Blockade of IL-1\u03b2\/IL-1 Receptor Type 1 Axis during Epileptogenesis Provides Neuroprotection in Two Rat Models of Temporal Lobe Epilepsy","volume":"59","author":"Noe","year":"2013","journal-title":"Neurobiol. Dis."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"1444","DOI":"10.1111\/epi.17600","article-title":"Review and Standard Operating Procedures for Collection of Biospecimens and Analysis of Biomarkers in New Onset Refractory Status Epilepticus","volume":"64","author":"Hanin","year":"2023","journal-title":"Epilepsia"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/15\/12519\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T20:27:15Z","timestamp":1760128035000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/15\/12519"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,8,7]]},"references-count":103,"journal-issue":{"issue":"15","published-online":{"date-parts":[[2023,8]]}},"alternative-id":["ijms241512519"],"URL":"https:\/\/doi.org\/10.3390\/ijms241512519","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,8,7]]}}}