{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T21:24:34Z","timestamp":1792790674750,"version":"4.5.0"},"reference-count":61,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2022,8,4]],"date-time":"2022-08-04T00:00:00Z","timestamp":1659571200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2022,8,4]],"date-time":"2022-08-04T00:00:00Z","timestamp":1659571200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["J Neuroinflammation"],"abstract":"<jats:title>Abstract<\/jats:title><jats:sec>\n                <jats:title>Background<\/jats:title>\n                <jats:p>Cerebral edema (CE) at admission is a surrogate marker of \u2018early brain injury\u2019 (EBI) after subarachnoid hemorrhage (SAH). Only recently has the focus on the changes in CE after SAH such as delayed resolution or newly developed CE been examined. Among several factors, an early systemic inflammatory response has been shown to be associated with CE. We investigate inflammatory markers in subjects with early CE which does not resolve, i.e., persistent CE after SAH.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Methods<\/jats:title>\n                <jats:p>Computed tomography scans of SAH patients were graded at admission and at 7\u00a0days after SAH for CE using the 0\u20134 \u2018subarachnoid hemorrhage early brain edema score\u2019 (SEBES). SEBES\u2009\u2264\u20092 and SEBES\u2009\u2265\u20093 were considered good and poor grade, respectively. Serum samples from the same subject cohort were collected at 4 time periods (at &lt;\u200924\u00a0h [T1], at 24 to 48\u00a0h [T2]. 3\u20135\u00a0days [T3] and 6\u20138\u00a0days [T4] post-admission) and concentration levels of 17 cytokines (implicated in peripheral inflammatory processes) were measured by multiplex immunoassay. Multivariable logistic regression analyses were step-wisely performed to identify cytokines independently associated with persistent CE adjusting for covariables including age, sex and past medical history (model 1), and additional inclusion of clinical and radiographic severity of SAH and treatment modality (model 2).<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Results<\/jats:title>\n                <jats:p>Of the 135 patients enrolled in the study, 21 of 135 subjects (15.6%) showed a persistently poor SEBES grade. In multivariate model 1, higher Eotaxin (at T1 and T4), sCD40L (at T4), IL-6 (at T1 and T3) and TNF-\u03b1 (at T4) were independently associated with persistent CE. In multivariate model 2, Eotaxin (at T4: odds ratio [OR]\u2009=\u20091.019, 95% confidence interval [CI]\u2009=\u20091.002\u20131.035) and possibly PDGF-AA (at T4), sCD40L (at T4), and TNF-\u03b1 (at T4) was associated with persistent CE.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Conclusions<\/jats:title>\n                <jats:p>We identified serum cytokines at different time points that were independently associated with persistent CE. Specifically, persistent elevations of Eotaxin is associated with persistent CE after SAH.<\/jats:p>\n              <\/jats:sec>","DOI":"10.1186\/s12974-022-02564-1","type":"journal-article","created":{"date-parts":[[2022,8,4]],"date-time":"2022-08-04T14:08:48Z","timestamp":1659622128000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":22,"title":["Systemic inflammatory markers of persistent cerebral edema after aneurysmal subarachnoid hemorrhage"],"prefix":"10.1186","volume":"19","author":[{"given":"Sung-Ho","family":"Ahn","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Angela","family":"Burkett","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Atzhiry","family":"Paz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jude P.","family":"Savarraj","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sarah","family":"Hinds","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Georgene","family":"Hergenroeder","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aaron M.","family":"Gusdon","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xuefeng","family":"Ren","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeong-Ho","family":"Hong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huimahn A.","family":"Choi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2022,8,4]]},"reference":[{"key":"2564_CR1","doi-asserted-by":"publisher","first-page":"349","DOI":"10.1016\/S1474-4422(11)70017-5","volume":"10","author":"GJ Rinkel","year":"2011","unstructured":"Rinkel GJ, Algra A. Long-term outcomes of patients with aneurysmal subarachnoid haemorrhage. Lancet Neurol. 2011;10:349\u201356.","journal-title":"Lancet Neurol"},{"key":"2564_CR2","doi-asserted-by":"publisher","first-page":"1267","DOI":"10.1016\/S0140-6736(02)11314-6","volume":"360","author":"A Molyneux","year":"2002","unstructured":"Molyneux A, Kerr R, Stratton I, Sandercock P, Clarke M, Shrimpton J, Holman R. International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet. 2002;360:1267\u201374.","journal-title":"Lancet"},{"key":"2564_CR3","doi-asserted-by":"publisher","first-page":"315","DOI":"10.1093\/bja\/aes264","volume":"109","author":"MJ Rowland","year":"2012","unstructured":"Rowland MJ, Hadjipavlou G, Kelly M, Westbrook J, Pattinson KT. Delayed cerebral ischaemia after subarachnoid haemorrhage: looking beyond vasospasm. Br J Anaesth. 2012;109:315\u201329.","journal-title":"Br J Anaesth"},{"key":"2564_CR4","doi-asserted-by":"publisher","first-page":"924","DOI":"10.1161\/STROKEAHA.110.597914","volume":"42","author":"MD Vergouwen","year":"2011","unstructured":"Vergouwen MD, Ilodigwe D, Macdonald RL. Cerebral infarction after subarachnoid hemorrhage contributes to poor outcome by vasospasm-dependent and -independent effects. Stroke. 2011;42:924\u20139.","journal-title":"Stroke"},{"key":"2564_CR5","doi-asserted-by":"publisher","first-page":"763","DOI":"10.1038\/sj.jcbfm.9600073","volume":"25","author":"P Vespa","year":"2005","unstructured":"Vespa P, Bergsneider M, Hattori N, Wu HM, Huang SC, Martin NA, Glenn TC, McArthur DL, Hovda DA. Metabolic crisis without brain ischemia is common after traumatic brain injury: a combined microdialysis and positron emission tomography study. J Cereb Blood Flow Metab. 2005;25:763\u201374.","journal-title":"J Cereb Blood Flow Metab"},{"key":"2564_CR6","doi-asserted-by":"publisher","first-page":"1341","DOI":"10.1038\/sj.jcbfm.9600283","volume":"26","author":"J Cahill","year":"2006","unstructured":"Cahill J, Calvert JW, Zhang JH. Mechanisms of early brain injury after subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2006;26:1341\u201353.","journal-title":"J Cereb Blood Flow Metab"},{"key":"2564_CR7","doi-asserted-by":"publisher","first-page":"1761","DOI":"10.1038\/jcbfm.2008.74","volume":"28","author":"MD Vergouwen","year":"2008","unstructured":"Vergouwen MD, Vermeulen M, Coert BA, Stroes ES, Roos YB. Microthrombosis after aneurysmal subarachnoid hemorrhage: an additional explanation for delayed cerebral ischemia. J Cereb Blood Flow Metab. 2008;28:1761\u201370.","journal-title":"J Cereb Blood Flow Metab"},{"key":"2564_CR8","doi-asserted-by":"publisher","first-page":"1225","DOI":"10.1161\/01.STR.0000015624.29071.1F","volume":"33","author":"J Claassen","year":"2002","unstructured":"Claassen J, Carhuapoma JR, Kreiter KT, Du EY, Connolly ES, Mayer SA. Global cerebral edema after subarachnoid hemorrhage: frequency, predictors, and impact on outcome. Stroke. 2002;33:1225\u201332.","journal-title":"Stroke"},{"key":"2564_CR9","doi-asserted-by":"publisher","first-page":"200","DOI":"10.1161\/hs0102.101080","volume":"33","author":"KT Kreiter","year":"2002","unstructured":"Kreiter KT, Copeland D, Bernardini GL, Bates JE, Peery S, Claassen J, Du YE, Stern Y, Connolly ES, Mayer SA. Predictors of cognitive dysfunction after subarachnoid hemorrhage. Stroke. 2002;33:200\u20138.","journal-title":"Stroke"},{"issue":"1","key":"2564_CR10","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1093\/neuros\/nyx364","volume":"83","author":"SH Ahn","year":"2017","unstructured":"Ahn SH, Savarraj JP, Pervez M, Jones W, Park J, Jeon SB, Kwon SU, Chang TR, Lee K, Kim DH, et al. The subarachnoid hemorrhage early brain edema score predicts delayed cerebral ischemia and clinical outcomes. Neurosurgery. 2017;83(1):137\u201345.","journal-title":"Neurosurgery"},{"key":"2564_CR11","doi-asserted-by":"publisher","DOI":"10.3171\/2019.12.JNS192744","author":"M Eibach","year":"2020","unstructured":"Eibach M, Won SY, Bruder M, Keil F, Herrmann E, Berkefeld J, Seifert V, Konczalla J. Age dependency and modification of the subarachnoid hemorrhage early brain edema score. J Neurosurg. 2020. https:\/\/doi.org\/10.3171\/2019.12.JNS192744.","journal-title":"J Neurosurg"},{"issue":"2","key":"2564_CR12","doi-asserted-by":"publisher","first-page":"321","DOI":"10.3390\/jcm10020321","volume":"10","author":"R Torn\u00e9","year":"2021","unstructured":"Torn\u00e9 R, Hoyos J, Llull L, Rodr\u00edguez-Hern\u00e1ndez A, Mu\u00f1oz G, Mellado-Artigas R, Santana D, Pedrosa L, Di Somma A, San Roman L, et al. Edema resolution and clinical assessment in poor-grade subarachnoid hemorrhage: useful indicators to predict delayed cerebral infarctions? J Clin Med. 2021;10(2):321.","journal-title":"J Clin Med"},{"key":"2564_CR13","doi-asserted-by":"publisher","first-page":"1173","DOI":"10.1111\/cns.13202","volume":"25","author":"YJ Fang","year":"2019","unstructured":"Fang YJ, Mei SH, Lu JN, Chen YK, Chai ZH, Dong X, Araujo C, Reis C, Zhang JM, Chen S. New risk score of the early period after spontaneous subarachnoid hemorrhage: for the prediction of delayed cerebral ischemia. CNS Neurosci Ther. 2019;25:1173\u201381.","journal-title":"CNS Neurosci Ther"},{"key":"2564_CR14","doi-asserted-by":"publisher","first-page":"828","DOI":"10.1161\/STROKEAHA.118.024283","volume":"50","author":"V Rass","year":"2019","unstructured":"Rass V, Ianosi BA, Wegmann A, Gaasch M, Schiefecker AJ, Kofler M, Lindner A, Addis A, Almashad SS, Rhomberg P, et al. Delayed resolution of cerebral edema is associated with poor outcome after nontraumatic subarachnoid hemorrhage. Stroke. 2019;50:828\u201336.","journal-title":"Stroke"},{"key":"2564_CR15","doi-asserted-by":"publisher","first-page":"334","DOI":"10.1016\/j.cyto.2018.09.003","volume":"111","author":"JP Savarraj","year":"2018","unstructured":"Savarraj JP, McGuire MF, Parsha K, Hergenroeder G, Bajgur S, Ahn S, Zhu L, Espino E, Chang T, Blackburn S, et al. Disruption of thrombo-inflammatory response and activation of a distinct cytokine cluster after subarachnoid hemorrhage. Cytokine. 2018;111:334\u201341.","journal-title":"Cytokine"},{"key":"2564_CR16","volume":"2014","author":"BA Miller","year":"2014","unstructured":"Miller BA, Turan N, Chau M, Pradilla G. Inflammation, vasospasm, and brain injury after subarachnoid hemorrhage. Biomed Res Int. 2014;2014: 384342.","journal-title":"Biomed Res Int"},{"key":"2564_CR17","doi-asserted-by":"publisher","first-page":"504","DOI":"10.1016\/S1474-4422(10)70087-9","volume":"9","author":"AA Rabinstein","year":"2010","unstructured":"Rabinstein AA, Lanzino G, Wijdicks EF. Multidisciplinary management and emerging therapeutic strategies in aneurysmal subarachnoid haemorrhage. Lancet Neurol. 2010;9:504\u201319.","journal-title":"Lancet Neurol"},{"key":"2564_CR18","doi-asserted-by":"publisher","first-page":"497","DOI":"10.3390\/ijms17040497","volume":"17","author":"BP Lucke-Wold","year":"2016","unstructured":"Lucke-Wold BP, Logsdon AF, Manoranjan B, Turner RC, McConnell E, Vates GE, Huber JD, Rosen CL, Simard JM. Aneurysmal subarachnoid hemorrhage and neuroinflammation: a comprehensive review. Int J Mol Sci. 2016;17:497.","journal-title":"Int J Mol Sci"},{"key":"2564_CR19","doi-asserted-by":"publisher","first-page":"566","DOI":"10.1227\/01.NEU.0000108862.32404.A5","volume":"54","author":"DS Rosen","year":"2004","unstructured":"Rosen DS, Macdonald RL. Grading of subarachnoid hemorrhage: modification of the world federation of neurosurgical societies scale on the basis of data for a large series of patients. Neurosurgery. 2004;54:566\u201376.","journal-title":"Neurosurgery"},{"key":"2564_CR20","doi-asserted-by":"publisher","first-page":"2391","DOI":"10.1161\/STROKEAHA.110.589275","volume":"41","author":"MD Vergouwen","year":"2010","unstructured":"Vergouwen MD, Vermeulen M, van Gijn J, Rinkel GJ, Wijdicks EF, Muizelaar JP, Mendelow AD, Juvela S, Yonas H, Terbrugge KG, et al. Definition of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage as an outcome event in clinical trials and observational studies: proposal of a multidisciplinary research group. Stroke. 2010;41:2391\u20135.","journal-title":"Stroke"},{"key":"2564_CR21","doi-asserted-by":"publisher","first-page":"427","DOI":"10.1161\/01.STR.0000053848.06436.AB","volume":"34","author":"CO Borel","year":"2003","unstructured":"Borel CO, McKee A, Parra A, Haglund MM, Solan A, Prabhakar V, Sheng H, Warner DS, Niklason L. Possible role for vascular cell proliferation in cerebral vasospasm after subarachnoid hemorrhage. Stroke. 2003;34:427\u201333.","journal-title":"Stroke"},{"key":"2564_CR22","doi-asserted-by":"publisher","first-page":"1711","DOI":"10.1161\/STR.0b013e3182587839","volume":"43","author":"ES Connolly Jr","year":"2012","unstructured":"Connolly ES Jr, Rabinstein AA, Carhuapoma JR, Derdeyn CP, Dion J, Higashida RT, Hoh BL, Kirkness CJ, Naidech AM, Ogilvy CS, et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association\/American Stroke Association. Stroke. 2012;43:1711\u201337.","journal-title":"Stroke"},{"key":"2564_CR23","doi-asserted-by":"publisher","first-page":"1535","DOI":"10.1212\/WNL.0000000000003842","volume":"88","author":"JPJ Savarraj","year":"2017","unstructured":"Savarraj JPJ, Parsha K, Hergenroeder GW, Zhu L, Bajgur SS, Ahn S, Lee K, Chang T, Kim DH, Liu Y, Choi HA. Systematic model of peripheral inflammation after subarachnoid hemorrhage. Neurology. 2017;88:1535\u201345.","journal-title":"Neurology"},{"key":"2564_CR24","doi-asserted-by":"publisher","first-page":"213","DOI":"10.1186\/s12974-019-1578-1","volume":"16","author":"SH Ahn","year":"2019","unstructured":"Ahn SH, Savarraj JPJ, Parsha K, Hergenroeder GW, Chang TR, Kim DH, Kitagawa RS, Blackburn SL, Choi HA. Inflammation in delayed ischemia and functional outcomes after subarachnoid hemorrhage. J Neuroinflamm. 2019;16:213.","journal-title":"J Neuroinflamm"},{"key":"2564_CR25","doi-asserted-by":"publisher","first-page":"S86","DOI":"10.1161\/STROKEAHA.108.533315","volume":"40","author":"J Cahill","year":"2009","unstructured":"Cahill J, Zhang JH. Subarachnoid hemorrhage: is it time for a new direction? Stroke. 2009;40:S86-87.","journal-title":"Stroke"},{"key":"2564_CR26","doi-asserted-by":"publisher","first-page":"2185","DOI":"10.1161\/01.CIR.102.18.2185","volume":"102","author":"KJ Haley","year":"2000","unstructured":"Haley KJ, Lilly CM, Yang J-H, Feng Y, Kennedy SP, Turi TG, Thompson JF, Sukhova GH, Libby P, Lee RT. Overexpression of eotaxin and the CCR3 receptor in human atherosclerosis. Circulation. 2000;102:2185\u20139.","journal-title":"Circulation"},{"key":"2564_CR27","doi-asserted-by":"publisher","first-page":"4463","DOI":"10.18632\/aging.102896","volume":"12","author":"Y Li","year":"2020","unstructured":"Li Y, Zhao Y, Qiu C, Yang Y, Liao G, Wu X, Zhang X, Zhang Q, Zhang R, Wang Z. Role of eotaxin-1\/CCL11 in sepsis-induced myocardial injury in elderly patients. Aging (Albany NY). 2020;12:4463\u201373.","journal-title":"Aging (Albany NY)"},{"key":"2564_CR28","doi-asserted-by":"publisher","first-page":"90","DOI":"10.1038\/nature10357","volume":"477","author":"SA Villeda","year":"2011","unstructured":"Villeda SA, Luo J, Mosher KI, Zou B, Britschgi M, Bieri G, Stan TM, Fainberg N, Ding Z, Eggel A, et al. The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature. 2011;477:90\u20134.","journal-title":"Nature"},{"key":"2564_CR29","doi-asserted-by":"publisher","first-page":"497","DOI":"10.1124\/jpet.114.213074","volume":"349","author":"MA Erickson","year":"2014","unstructured":"Erickson MA, Morofuji Y, Owen JB, Banks WA. Rapid transport of CCL11 across the blood\u2013brain barrier: regional variation and importance of blood cells. J Pharmacol Exp Ther. 2014;349:497\u2013507.","journal-title":"J Pharmacol Exp Ther"},{"key":"2564_CR30","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1186\/1742-2094-8-139","volume":"8","author":"A Kovac","year":"2011","unstructured":"Kovac A, Erickson MA, Banks WA. Brain microvascular pericytes are immunoactive in culture: cytokine, chemokine, nitric oxide, and LRP-1 expression in response to lipopolysaccharide. J Neuroinflamm. 2011;8:139.","journal-title":"J Neuroinflamm"},{"key":"2564_CR31","doi-asserted-by":"publisher","first-page":"2274","DOI":"10.1002\/glia.22892","volume":"63","author":"B Parajuli","year":"2015","unstructured":"Parajuli B, Horiuchi H, Mizuno T, Takeuchi H, Suzumura A. CCL11 enhances excitotoxic neuronal death by producing reactive oxygen species in microglia. Glia. 2015;63:2274\u201384.","journal-title":"Glia"},{"key":"2564_CR32","doi-asserted-by":"publisher","first-page":"2146","DOI":"10.1161\/ATVBAHA.109.194134","volume":"29","author":"MS Jamaluddin","year":"2009","unstructured":"Jamaluddin MS, Wang X, Wang H, Rafael C, Yao Q, Chen C. Eotaxin increases monolayer permeability of human coronary artery endothelial cells. Arterioscler Thromb Vasc Biol. 2009;29:2146\u201352.","journal-title":"Arterioscler Thromb Vasc Biol"},{"key":"2564_CR33","doi-asserted-by":"publisher","first-page":"578","DOI":"10.1007\/s12975-017-0545-3","volume":"8","author":"M Roy-O'Reilly","year":"2017","unstructured":"Roy-O\u2019Reilly M, Ritzel RM, Conway SE, Staff I, Fortunato G, McCullough LD. CCL11 (eotaxin-1) levels predict long-term functional outcomes in patients following ischemic stroke. Transl Stroke Res. 2017;8:578\u201384.","journal-title":"Transl Stroke Res"},{"key":"2564_CR34","doi-asserted-by":"publisher","first-page":"2594","DOI":"10.1161\/STROKEAHA.113.002361","volume":"44","author":"N Chalouhi","year":"2013","unstructured":"Chalouhi N, Points L, Pierce GL, Ballas Z, Jabbour P, Hasan D. Localized increase of chemokines in the lumen of human cerebral aneurysms. Stroke. 2013;44:2594\u20137.","journal-title":"Stroke"},{"issue":"14","key":"2564_CR35","doi-asserted-by":"publisher","first-page":"2452","DOI":"10.1016\/j.cell.2022.06.008","volume":"185","author":"A Fern\u00e1ndez-Casta\u00f1eda","year":"2022","unstructured":"Fern\u00e1ndez-Casta\u00f1eda A, Lu P, Geraghty AC, Song E, Lee MH, Wood J, O\u2019Dea MR, Dutton S, Shamardani K, Nwangwu K, et al. Mild respiratory COVID can cause multi-lineage neural cell and myelin dysregulation. Cell. 2022;185(14):2452\u201368.","journal-title":"Cell"},{"key":"2564_CR36","doi-asserted-by":"publisher","first-page":"26","DOI":"10.1186\/s12871-021-01241-9","volume":"21","author":"Y Liang","year":"2021","unstructured":"Liang Y, Zhu C, Sun Y, Li Z, Wang L, Liu Y, Li X, Ma X. Persistently higher serum sCD40L levels are associated with outcome in septic patients. BMC Anesthesiol. 2021;21:26.","journal-title":"BMC Anesthesiol"},{"key":"2564_CR37","doi-asserted-by":"publisher","first-page":"1690","DOI":"10.1161\/01.CIR.0000160349.42665.0C","volume":"111","author":"M Ishikawa","year":"2005","unstructured":"Ishikawa M, Vowinkel T, Stokes KY, Arumugam TV, Yilmaz G, Nanda A, Granger DN. CD40\/CD40 ligand signaling in mouse cerebral microvasculature after focal ischemia\/reperfusion. Circulation. 2005;111:1690\u20136.","journal-title":"Circulation"},{"key":"2564_CR38","doi-asserted-by":"publisher","first-page":"1432","DOI":"10.1007\/s00134-006-0250-2","volume":"32","author":"DP Inwald","year":"2006","unstructured":"Inwald DP, Faust SN, Lister P, Peters MJ, Levin M, Heyderman R, Klein NJ. Platelet and soluble CD40L in meningococcal sepsis. Intensive Care Med. 2006;32:1432\u20137.","journal-title":"Intensive Care Med"},{"key":"2564_CR39","doi-asserted-by":"publisher","first-page":"979","DOI":"10.1007\/s00011-010-0213-5","volume":"59","author":"M Chew","year":"2010","unstructured":"Chew M, Rahman M, Ihrman L, Erson A, Zhang S, Thorlacius H. Soluble CD40L (CD154) is increased in patients with shock. Inflamm Res. 2010;59:979\u201382.","journal-title":"Inflamm Res"},{"key":"2564_CR40","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0051793","volume":"7","author":"DC Davidson","year":"2012","unstructured":"Davidson DC, Hirschman MP, Sun A, Singh MV, Kasischke K, Maggirwar SB. Excess soluble CD40L contributes to blood brain barrier permeability in vivo: implications for HIV-associated neurocognitive disorders. PLoS ONE. 2012;7: e51793.","journal-title":"PLoS ONE"},{"key":"2564_CR41","doi-asserted-by":"publisher","first-page":"22342","DOI":"10.3390\/ijms151222342","volume":"15","author":"C Aloui","year":"2014","unstructured":"Aloui C, Prigent A, Sut C, Tariket S, Hamzeh-Cognasse H, Pozzetto B, Richard Y, Cognasse F, Laradi S, Garraud O. The signaling role of CD40 ligand in platelet biology and in platelet component transfusion. Int J Mol Sci. 2014;15:22342\u201364.","journal-title":"Int J Mol Sci"},{"key":"2564_CR42","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1615\/CritRevNeurobiol.v18.i1-2.150","volume":"18","author":"J Kriz","year":"2006","unstructured":"Kriz J. Inflammation in ischemic brain injury: timing is important. Crit Rev Neurobiol. 2006;18:145\u201357.","journal-title":"Crit Rev Neurobiol"},{"key":"2564_CR43","doi-asserted-by":"publisher","first-page":"217","DOI":"10.1186\/s12974-016-0675-7","volume":"13","author":"A Niwa","year":"2016","unstructured":"Niwa A, Osuka K, Nakura T, Matsuo N, Watabe T, Takayasu M. Interleukin-6, MCP-1, IP-10, and MIG are sequentially expressed in cerebrospinal fluid after subarachnoid hemorrhage. J Neuroinflamm. 2016;13:217.","journal-title":"J Neuroinflamm"},{"key":"2564_CR44","doi-asserted-by":"publisher","first-page":"509","DOI":"10.2334\/josnusd.16-0278","volume":"58","author":"A Wytrykowska","year":"2016","unstructured":"Wytrykowska A, Prosba-Mackiewicz M, Nyka WM. IL-1beta, TNF-alpha, and IL-6 levels in gingival fluid and serum of patients with ischemic stroke. J Oral Sci. 2016;58:509\u201313.","journal-title":"J Oral Sci"},{"key":"2564_CR45","doi-asserted-by":"publisher","first-page":"820","DOI":"10.3171\/jns.2007.106.5.820","volume":"106","author":"J Hillman","year":"2007","unstructured":"Hillman J, Aneman O, Persson M, Andersson C, Dabrosin C, Mellerg\u00e5rd P. Variations in the response of interleukins in neurosurgical intensive care patients monitored using intracerebral microdialysis. J Neurosurg. 2007;106:820\u20135.","journal-title":"J Neurosurg"},{"key":"2564_CR46","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1227\/NEU.0b013e3181ef2a40","volume":"68","author":"P Mellergard","year":"2011","unstructured":"Mellergard P, Aneman O, Sjogren F, Saberg C, Hillman J. Differences in cerebral extracellular response of interleukin-1beta, interleukin-6, and interleukin-10 after subarachnoid hemorrhage or severe head trauma in humans. Neurosurgery. 2011;68:12\u20139 (discussion 19).","journal-title":"Neurosurgery"},{"key":"2564_CR47","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1007\/s12028-017-0471-y","volume":"28","author":"J Savarraj","year":"2018","unstructured":"Savarraj J, Parsha K, Hergenroeder G, Ahn S, Chang TR, Kim DH, Choi HA. Early brain injury associated with systemic inflammation after subarachnoid hemorrhage. Neurocrit Care. 2018;28:203\u201311.","journal-title":"Neurocrit Care"},{"key":"2564_CR48","doi-asserted-by":"publisher","first-page":"512","DOI":"10.1136\/neurintsurg-2012-010386","volume":"5","author":"CJ McMahon","year":"2013","unstructured":"McMahon CJ, Hopkins S, Vail A, King AT, Smith D, Illingworth KJ, Clark S, Rothwell NJ, Tyrrell PJ. Inflammation as a predictor for delayed cerebral ischemia after aneurysmal subarachnoid haemorrhage. J Neurointerv Surg. 2013;5:512\u20137.","journal-title":"J Neurointerv Surg"},{"key":"2564_CR49","doi-asserted-by":"publisher","first-page":"365","DOI":"10.1016\/j.nec.2009.10.008","volume":"21","author":"G Pradilla","year":"2010","unstructured":"Pradilla G, Chaichana KL, Hoang S, Huang J, Tamargo RJ. Inflammation and cerebral vasospasm after subarachnoid hemorrhage. Neurosurg Clin N Am. 2010;21:365\u201379.","journal-title":"Neurosurg Clin N Am"},{"key":"2564_CR50","doi-asserted-by":"publisher","first-page":"N11","DOI":"10.1227\/01.neu.0000479888.94994.7c","volume":"78","author":"GM Weiner","year":"2016","unstructured":"Weiner GM, Ozpinar A, Ducruet AF. The role of matrix metalloproteinase-9 in subarachnoid hemorrhage-induced white matter injury. Neurosurgery. 2016;78:N11-12.","journal-title":"Neurosurgery"},{"key":"2564_CR51","doi-asserted-by":"publisher","DOI":"10.5812\/atr.30165","volume":"4","author":"L Lorente","year":"2015","unstructured":"Lorente L. New prognostic biomarkers in patients with traumatic brain injury. Arch Trauma Res. 2015;4: e30165.","journal-title":"Arch Trauma Res"},{"key":"2564_CR52","doi-asserted-by":"publisher","first-page":"556","DOI":"10.3389\/fimmu.2016.00556","volume":"7","author":"CA McKee","year":"2016","unstructured":"McKee CA, Lukens JR. Emerging roles for the immune system in traumatic brain injury. Front Immunol. 2016;7:556.","journal-title":"Front Immunol"},{"key":"2564_CR53","doi-asserted-by":"publisher","first-page":"905","DOI":"10.1007\/s12028-021-01398-8","volume":"36","author":"RP Martini","year":"2022","unstructured":"Martini RP, Siler D, Cetas J, Alkayed NJ, Allen E, Treggiari MM. A double-blind, randomized, placebo-controlled trial of soluble epoxide hydrolase inhibition in patients with aneurysmal subarachnoid hemorrhage. Neurocrit Care. 2022;36:905\u201315.","journal-title":"Neurocrit Care"},{"key":"2564_CR54","doi-asserted-by":"publisher","first-page":"E12","DOI":"10.3171\/2021.12.FOCUS21663","volume":"52","author":"C Garc\u00eda-Pastor","year":"2022","unstructured":"Garc\u00eda-Pastor C, Navarro-Garcia de Llano JP, Balc\u00e1zar-Padr\u00f3n JC, Trist\u00e1n-L\u00f3pez L, Rios C, D\u00edaz-Ru\u00edz A, Rodr\u00edguez-Hernandez LA, Nathal E. Neuroprotective effect of dapsone in patients with aneurysmal subarachnoid hemorrhage: a prospective, randomized, double-blind, placebo-controlled clinical trial. Neurosurg Focus. 2022;52:E12.","journal-title":"Neurosurg Focus"},{"key":"2564_CR55","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1186\/s12871-020-01215-3","volume":"21","author":"J Zhang","year":"2021","unstructured":"Zhang J, Nie Y, Pang Q, Zhang X, Wang Q, Tang J. Effects of stellate ganglion block on early brain injury in patients with subarachnoid hemorrhage: a randomised control trial. BMC Anesthesiol. 2021;21:23.","journal-title":"BMC Anesthesiol"},{"key":"2564_CR56","doi-asserted-by":"publisher","first-page":"401","DOI":"10.1186\/s12883-020-01908-9","volume":"20","author":"PYM Woo","year":"2020","unstructured":"Woo PYM, Ho JWK, Ko NMW, Li RPT, Jian L, Chu ACH, Kwan MCL, Chan Y, Wong AKS, Wong HT, et al. Randomized, placebo-controlled, double-blind, pilot trial to investigate safety and efficacy of cerebrolysin in patients with aneurysmal subarachnoid hemorrhage. BMC Neurol. 2020;20:401.","journal-title":"BMC Neurol"},{"key":"2564_CR57","doi-asserted-by":"publisher","first-page":"515","DOI":"10.3171\/2016.9.JNS16615","volume":"128","author":"J Galea","year":"2018","unstructured":"Galea J, Ogungbenro K, Hulme S, Patel H, Scarth S, Hoadley M, Illingworth K, McMahon CJ, Tzerakis N, King AT, et al. Reduction of inflammation after administration of interleukin-1 receptor antagonist following aneurysmal subarachnoid hemorrhage: results of the subcutaneous interleukin-1Ra in SAH (SCIL-SAH) study. J Neurosurg. 2018;128:515\u201323.","journal-title":"J Neurosurg"},{"key":"2564_CR58","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1742-2094-11-1","volume":"11","author":"N Singh","year":"2014","unstructured":"Singh N, Hopkins SJ, Hulme S, Galea JP, Hoadley M, Vail A, Hutchinson PJ, Grainger S, Rothwell NJ, King AT, Tyrrell PJ. The effect of intravenous interleukin-1 receptor antagonist on inflammatory mediators in cerebrospinal fluid after subarachnoid haemorrhage: a phase II randomised controlled trial. J Neuroinflamm. 2014;11:1.","journal-title":"J Neuroinflamm"},{"key":"2564_CR59","doi-asserted-by":"publisher","first-page":"726","DOI":"10.1016\/j.jocn.2012.09.012","volume":"20","author":"YX Pan","year":"2013","unstructured":"Pan YX, Chen KF, Lin YX, Wu W, Zhou XM, Zhang XS, Zhang X, Shi JX. Intracisternal administration of SB203580, a p38 mitogen-activated protein kinase inhibitor, attenuates cerebral vasospasm via inhibition of tumor-necrosis factor-\u03b1. J Clin Neurosci. 2013;20:726\u201330.","journal-title":"J Clin Neurosci"},{"key":"2564_CR60","doi-asserted-by":"publisher","first-page":"1156","DOI":"10.1161\/01.STR.20.9.1156","volume":"20","author":"D Hasan","year":"1989","unstructured":"Hasan D, Lindsay KW, Wijdicks EF, Murray GD, Brouwers PJ, Bakker WH, van Gijn J, Vermeulen M. Effect of fludrocortisone acetate in patients with subarachnoid hemorrhage. Stroke. 1989;20:1156\u201361.","journal-title":"Stroke"},{"key":"2564_CR61","doi-asserted-by":"publisher","first-page":"188","DOI":"10.1097\/00008506-199907000-00006","volume":"11","author":"T Niemi","year":"1999","unstructured":"Niemi T, Tanskanen P, Taxell C, Juvela S, Randell T, Rosenberg P. Effects of nonsteroidal anti-inflammatory drugs on hemostasis in patients with aneurysmal subarachnoid hemorrhage. J Neurosurg Anesthesiol. 1999;11:188\u201394.","journal-title":"J Neurosurg Anesthesiol"}],"container-title":["Journal of Neuroinflammation"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12974-022-02564-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s12974-022-02564-1\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12974-022-02564-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,8,4]],"date-time":"2022-08-04T16:08:07Z","timestamp":1659629287000},"score":1,"resource":{"primary":{"URL":"https:\/\/jneuroinflammation.biomedcentral.com\/articles\/10.1186\/s12974-022-02564-1"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,8,4]]},"references-count":61,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2022,12]]}},"alternative-id":["2564"],"URL":"https:\/\/doi.org\/10.1186\/s12974-022-02564-1","relation":{},"ISSN":["1742-2094"],"issn-type":[{"value":"1742-2094","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,8,4]]},"assertion":[{"value":"22 June 2022","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"12 July 2022","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"4 August 2022","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"Our study was reviewed and approved by the institutional review board at the Memorial Herman Hospital-Texas Medical Center, Houston, TX (HSC-MS-12-0637) and written informed consent was obtained from patients or surrogate. The study was adhered to the tenets of the most recent revision of the Declaration of Helsinki.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"All authors have approved the contents of this manuscript and provided their consent for publication.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"199"}}