The physiopathology of spontaneous hemorrhagic stroke: a systematic review
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Alcivan Batista de Morais Filho
, Thiago Luis de Holanda Rego
, Letícia de Lima Mendonça , Sulyanne Saraiva de Almeida , Mariana Lima da Nóbrega , Thais de Oliveira Palmieri , Gabriela Zanotto Della Giustina , Jáderson Pimenta Melo , Francisco Irochima Pinheiro and Fausto Pierdoná Guzen
Abstract
Hemorrhagic stroke (HS) is a major cause of death and disability worldwide, despite being less common, it presents more aggressively and leads to more severe sequelae than ischemic stroke. There are two types of HS: Intracerebral Hemorrhage (ICH) and Subarachnoid Hemorrhage (SAH), differing not only in the site of bleeding, but also in the mechanisms responsible for acute and subacute symptoms. This is a systematic review of databases in search of works of the last five years relating to the comprehension of both kinds of HS. Sixty two articles composed the direct findings of the recent literature and were further characterized to construct the pathophysiology in the order of events. The road to the understanding of the spontaneous HS pathophysiology is far from complete. Our findings show specific and individual results relating to the natural history of the disease of ICH and SAH, presenting common and different risk factors, distinct and similar clinical manifestations at onset or later days to weeks, and possible complications for both.
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Author contribution: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
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Research funding: None declared.
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Conflict of interest statement: The authors declare no conflicts of interest regarding this article.
References
Abraham, M.K. and Chang, W.T.W. (2016). Subarachnoid hemorrhage. Emerg. Med. Clin. North Am. 34: 901–916, https://doi.org/10.1016/j.emc.2016.06.011.Search in Google Scholar PubMed
Abulhasan, Y.B., Alabdulraheem, N., Schiller, I., Rachel, S.P., Dendukuri, N., Angle, M.R., and Frenette, C. (2018). Health care – associated infections after subarachnoid hemorrhage. World Neurosurg. 115: e393–e403, https://doi.org/10.1016/j.wneu.2018.04.061.Search in Google Scholar PubMed
Al-Mufti, F., Amuluru, K., Damodara, N., Dodson, V., Roh, D., Agarwal, S., Meyers, P.M., Connolly, E.S., Schmidt, M.J., Claassen, J., . (2019). Admission neutrophil-lymphocyte ratio predicts delayed cerebral ischemia following aneurysmal subarachnoid hemorrhage. J. Neurointerv. Surg. 11: 1135–1140, https://doi.org/10.1136/neurintsurg-2019-014759.Search in Google Scholar PubMed
Al-Tamimi, Y.Z., Bhargava, D., Orsi, N.M., Teraifi, A., Cummings, M., Ekbote, U.V., Quinn, A.C., Homer-Vanniasinkam, S., and Ross, S. (2019). Compartmentalisation of the inflammatory response following aneurysmal subarachnoid haemorrhage. Cytokine 123: 154778, https://doi.org/10.1016/j.cyto.2019.154778.Search in Google Scholar PubMed
An, S.J., Kim, T.J., and Yoon, B.W. (2017). Epidemiology, risk factors, and clinical features of intracerebral hemorrhage: an update. J. Stroke 19: 3–10, https://doi.org/10.5853/jos.2016.00864.Search in Google Scholar PubMed PubMed Central
Anan, M., Nagai, Y., Fudaba, H., and Fujiki, M. (2020). Lactate and lactate dehydrogenase in cistern as biomarkers of early brain injury and delayed cerebral ischemia of subarachnoid hemorrhage. J. Stroke Cerebrovasc. Dis. 29: 104765, https://doi.org/10.1016/j.jstrokecerebrovasdis.2020.104765.Search in Google Scholar PubMed
Anderson, C.S., Selim, M.H., Molina, C., and Qureshi, A.I. (2017). Intensive blood pressure lowering in intracerebral hemorrhage. Stroke 48: 2034–2037, https://doi.org/10.1161/strokeaha.117.016185.Search in Google Scholar
Appel, D., Seeberger, M., Schwedhelm, E., Czorlich, P., Goetz, A.E., Böger, R.H., and Hannemann, J. (2018). Asymmetric and symmetric dimethylarginines are markers of delayed cerebral ischemia and neurological outcome in patients with subarachnoid hemorrhage. Neurocrit. Care 29: 84–93, https://doi.org/10.1007/s12028-018-0520-1.Search in Google Scholar PubMed
Bian, L., Mao, L.G., Sun, Y., Shen, F., Chen, J.F., Liu, Z., and Zhou, W. (2019). Serum lipoprotein-associated phospholipase A2 as a promising prognostic biomarker in association with 90-day outcome of acute intracerebral hemorrhage. Clin. Chim. Acta 495: 429–435, https://doi.org/10.1016/j.cca.2019.05.017.Search in Google Scholar PubMed
Burns, S.K. (2018). Aneurysmal subarachnoid hemorrhage and vasospasm. Adv. Crit. Care 29: 163–174, https://doi.org/10.4037/aacnacc2018491.Search in Google Scholar PubMed
Calviere, L., Cuvinciuc, V., Raposo, N., Faury, A., Cognard, C., Larrue, V., Viguier, A., and Bonneville, F. (2016). Acute convexity subarachnoid hemorrhage related to cerebral amyloid angiopathy: clinicoradiological features and outcome. J. Stroke Cerebrovasc. Dis. 25: 1009–1016, https://doi.org/10.1016/j.jstrokecerebrovasdis.2015.11.010.Search in Google Scholar PubMed
Can, A., Castro, V.M., Ozdemir, Y.H., Dagen, S., Dligach, D., Finan, S., Yu, S., Gainer, V., Shadick, N.A., Savova, G., et al.. (2018a). Alcohol consumption and aneurysmal subarachnoid hemorrhage. Transl. Stroke Res. 9: 13–19, https://doi.org/10.1007/s12975-017-0557-z.Search in Google Scholar PubMed
Can, A., Castro, V.M., Ozdemir, Y.H., Dagen, S., Dligach, D., Finan, S., Yu, S., Gainer, V., Shadick, N.A., Savova, G., et al.. (2018b). Heroin use is associated with ruptured saccular aneurysms. Transl. Stroke Res. 9: 340–346, https://doi.org/10.1007/s12975-017-0582-y.Search in Google Scholar PubMed
Can, A., Xu, J., Volovici, V., Dammers, R., Dirven, C.M.F., MacRae, C.A., and Du, R. (2015). Fusiform aneurysms are associated with aortic root dilatation in patients with subarachnoid hemorrhage. World Neurosurg. 84: 1681–1685, https://doi.org/10.1016/j.wneu.2015.07.011.Search in Google Scholar PubMed
Carteron, L., Patet, C., Solari, D., Messerer, M., Daniel, R.T., Eckert, P., Meuli, R., and Oddo, M. (2017). Non-ischemic cerebral energy dysfunction at the early brain injury phase following aneurysmal subarachnoid hemorrhage. Front. Neurol. 8: 325, https://doi.org/10.3389/fneur.2017.00325.Search in Google Scholar PubMed PubMed Central
Chang, J.J., Triano, M., Corbin, M.J., Desale, S., Liu, A.H., Felbaum, D.F., Mai, J.C., Armonda, R.A., and Aulisi, E.F. (2020). Transcranial doppler velocity and associations with delayed cerebral ischemia in aneurysmal subarachnoid hemorrhage. J. Neurol. Sci. 415: 116934.10.1016/j.jns.2020.116934Search in Google Scholar PubMed
Chaudhry, S.R., Güresir, E., Vatter, H., Kinfe, T.M., Dietrich, D., Lamprecht, A., and Muhammad, S. (2017). Aneurysmal subarachnoid hemorrhage lead to systemic upregulation of IL-23/IL-17 inflammatory axis. Cytokine 97: 96–103, https://doi.org/10.1016/j.cyto.2017.05.025.Search in Google Scholar PubMed
Chaudhry, S.R., Kinfe, T.M., Lamprecht, A., Niemelä, M., Dobreva, G., Hänggi, D., and Muhammad, S. (2020). Elevated level of cerebrospinal fluid and systemic chemokine CCL5 is a predictive biomarker of clinical outcome after aneurysmal subarachnoid hemorrhage (aSAH). Cytokine 133: 155142, https://doi.org/10.1016/j.cyto.2020.155142.Search in Google Scholar PubMed
Chen, S., Luo, J., Reis, C., Manaenko, A., and Zhang, J. (2017). Hydrocephalus after subarachnoid hemorrhage: pathophysiology, diagnosis, and treatment. BioMed Res. Int. 2017: 8584753, https://doi.org/10.1155/2017/8584753.Search in Google Scholar PubMed PubMed Central
Choi, H.A., Bajgur, S.S., Jones, W.H., Savarraj, J.P.J., Ko, S.B., Edwards, N.J., Chang, T.R., Hergenroeder, G.W., Dannenbaum, M.J., Chen, P.R., et al.. (2016). Quantification of cerebral edema after subarachnoid hemorrhage. Neurocrit. Care 25: 64–70, https://doi.org/10.1007/s12028-015-0229-3.Search in Google Scholar PubMed
Crago, E.A., Sherwood, P.R., Bender, C., Balzer, J., Ren, D., and Poloyac, S.M. (2015). Plasma estrogen levels are associated with severity of injury and outcomes after aneurysmal subarachnoid hemorrhage. Biol. Res. Nurs. 17: 558–566, https://doi.org/10.1177/1099800414561632.Search in Google Scholar PubMed PubMed Central
Dardiotis, E., Siokas, V., Marogianni, C., Aloizou, A.M., Sokratous, M., Paterakis, K., Dardioti, M., Grigoriadis, S., Brotis, A., Kapsalaki, E., et al.. (2019). AQP4 tag SNPs in patients with intracerebral hemorrhage in Greek and Polish population. Neurosci. Lett. 696: 156–161, https://doi.org/10.1016/j.neulet.2018.12.025.Search in Google Scholar PubMed
Dasenbrock, H.H., Rudy, R.F., Lai, P.M.R., Smith, T.R., Frerichs, K.U., Gormley, W.B., Aziz-Sultan, M.A., and Du, R. (2018). Cigarette smoking and outcomes after aneurysmal subarachnoid hemorrhage: a nationwide analysis. J. Neurosurg. 129: 446–457, https://doi.org/10.3171/2016.10.jns16748.Search in Google Scholar PubMed
Di Napoli, M., Slevin, M., Popa-Wagner, A., Singh, P., Lattanzi, S., and Divani, A.A. (2018). Monomeric C-reactive protein and cerebral hemorrhage: from bench to bedside. Front. Immunol. 9: 1–11, https://doi.org/10.3389/fimmu.2018.01921.Search in Google Scholar PubMed PubMed Central
Divani, A.A., Liu, X., Di Napoli, M., Lattanzi, S., Ziai, W., James, M.L., Jafarli, A., Jafari, M., Saver, J.L., Hemphill, J.C., et al.. (2019). Blood pressure variability predicts poor in-hospital outcome in spontaneous intracerebral hemorrhage. Stroke 50: 2023–2029, https://doi.org/10.1161/strokeaha.119.025514.Search in Google Scholar PubMed
Divani, A.A., Liu, X., Petersen, A., Lattanzi, S., Anderson, C.S., Ziai, W., Torbey, M.T., Moullaali, T.J., James, M.L., Jafarli, A., et al.. (2020). The magnitude of blood pressure reduction predicts poor in-hospital outcome in acute intracerebral hemorrhage. Neurocrit. Care 33: 389–398, https://doi.org/10.1007/s12028-020-01016-z.Search in Google Scholar PubMed
Ďuriš, K., Neuman, E., Vybíhal, V., Juráå, V., Gottwaldová, J., Kýr, M., Vašků, A., and Smrčka, M. (2018). Early dynamics of interleukin-6 in cerebrospinal fluid after aneurysmal subarachnoid hemorrhage. J. Neurol. Surgery Part A Cent. Eur. Neurosurg. 79: 145–151.10.1055/s-0037-1604084Search in Google Scholar PubMed
Durocher, M., Ander, B.P., Jickling, G., Hamade, F., Hull, H., Knepp, B., Liu, D.Z., Zhan, X., Tran, A., Cheng, X., et al.. (2019). Inflammatory, regulatory, and autophagy co-expression modules and hub genes underlie the peripheral immune response to human intracerebral hemorrhage. J. Neuroinflamm. 16: 56, https://doi.org/10.1186/s12974-019-1433-4.Search in Google Scholar PubMed PubMed Central
D’Souza, S. (2015). Aneurysmal subarachnoid hemorrhage. J. Neurosurg. Anesthesiol. 27: 222–240.10.1097/ANA.0000000000000130Search in Google Scholar PubMed PubMed Central
Erben, Y., Barrett, K.M., Freeman, W.D., Lin, M., Tawk, R., Ball, C.T., Melton, V.S., Thuro, L.M., Hakaim, A.G., Brott, T.G., et al.. (2019). Prevalence of previously undiagnosed abdominal aortic aneurysms in patients with intracranial aneurysms: from the brain and aortic aneurysms study (BAAS). Neurocrit. Care 32: 796–803, https://doi.org/10.1007/s12028-019-00828-y.Search in Google Scholar PubMed
Etminan, N., Chang, H.S., Hackenberg, K., De Rooij, N.K., Vergouwen, M.D.I., Rinkel, G.J.E., and Algra, A. (2019). Worldwide incidence of aneurysmal subarachnoid hemorrhage according to region, time period, blood pressure, and smoking prevalence in the population: a systematic review and meta-analysis. JAMA Neurol 76: 588–597, https://doi.org/10.1001/jamaneurol.2019.0006.Search in Google Scholar PubMed PubMed Central
Ewelina, G., Krzysztof, S., Marek, M., and Krzysztof, K. (2017). Blood free radicals concentration determined by electron paramagnetic resonance spectroscopy and delayed cerebral ischemia occurrence in patients with aneurysmal subarachnoid hemorrhage. Cell Biochem. Biophys. 75: 351–358, https://doi.org/10.1007/s12013-017-0820-7.Search in Google Scholar PubMed PubMed Central
Feigin, V.L., Norrving, B., and Mensah, G.A. (2017). Global burden of stroke. Circ. Res. 120: 439–448, https://doi.org/10.1161/circresaha.116.308413.Search in Google Scholar PubMed
Fujimura, M., Bang, Y., and Kim, S. (2016). Moyamoya disease. Front. Neurol. Neurosci. 40: 204–220, https://doi.org/10.1159/000448314.Search in Google Scholar PubMed
Geraghty, J.R. and Testai, F.D. (2017). Delayed cerebral ischemia after subarachnoid hemorrhage: beyond vasospasm and towards a multifactorial pathophysiology. Curr. Atheroscler. Rep. 19: 50, https://doi.org/10.1007/s11883-017-0690-x.Search in Google Scholar PubMed
Grasso, G., Alafaci, C., and MacDonald, R. (2017). Management of aneurysmal subarachnoid hemorrhage: state of the art and future perspectives. Surg. Neurol. Int. 8: 1–10, https://doi.org/10.4103/2152-7806.198738.Search in Google Scholar PubMed PubMed Central
Griessenauer, C.J., Shane Tubbs, R., Foreman, P.M., Chua, M.H., Vyas, N.A., Lipsky, R.H., Lin, M., Iyer, R., Haridas, R., Walters, B.C., et al.. (2018a). Association of renin-angiotensin system genetic polymorphisms and aneurysmal subarachnoid hemorrhage. J. Neurosurg. 128: 86–93, https://doi.org/10.3171/2016.9.jns161593.Search in Google Scholar PubMed
Griessenauer, C.J., Starke, R.M., Foreman, P.M., Hendrix, P., Harrigan, M.R., Fisher, W.S., Vyas, N.A., Lipsky, R.H., Lin, M., Walters, B.C., et al.. (2018b). Associations between endothelin polymorphisms and aneurysmal subarachnoid hemorrhage, clinical vasospasm, delayed cerebral ischemia, and functional outcome. J. Neurosurg. 128: 1311–1317, https://doi.org/10.3171/2016.12.jns162594.Search in Google Scholar
Guo, Y., Yue, X., Jing, L., Hua, H., Song, Z., Xiu, Y., Qing, H., Zhang, P., Gui, Y., Chang, L., et al.. (2016). Overweight and obesity in young adulthood and the risk of stroke: a meta-analysis. J. Stroke Cerebrovasc. Dis. 25: 2995–3004, https://doi.org/10.1016/j.jstrokecerebrovasdis.2016.08.018.Search in Google Scholar PubMed
Gupta, K. and Das, J.M. (2020). Charcot Bouchard Aneurysm.Search in Google Scholar
Han, C., Li, M.L., Xu, Y., Ye, T., Xie, C.F., Gao, S., Duan, L., and Xu, W.H. (2016). Adult moyamoya-atherosclerosis syndrome: clinical and vessel wall imaging features. J. Neurol. Sci. 369: 181–184, https://doi.org/10.1016/j.jns.2016.08.020.Search in Google Scholar PubMed
Hankey, G.J. (2017). Stroke. Lancet 389: 641–654, https://doi.org/10.1016/s0140-6736(16)30962-x.Search in Google Scholar
Harary, M., Dolmans, R.G.F., and Gormley, W.B. (2018). Intracranial pressure monitoring—review and avenues for development. Sensors 18: 3–7, https://doi.org/10.3390/s18020465.Search in Google Scholar PubMed PubMed Central
Hauer, A.J., Ruigrok, Y.M., Algra, A., van Dijk, E.J., Koudstaal, P.J., Luijckx, G.J., Nederkoorn, P.J., van Oostenbrugge, R.J., Visser, M.C., Wermer, M.J., et al.. (2017). Age-specific vascular risk factor profiles according to stroke subtype. J. Am. Heart Assoc. 6: 1–11, https://doi.org/10.1161/jaha.116.005090.Search in Google Scholar PubMed PubMed Central
Hendrix, P., Foreman, P.M., Harrigan, M.R., Fisher, W.S., Vyas, N.A., Lipsky, R.H., Lin, M., Walters, B.C., Tubbs, R.S., Shoja, M.M., et al.. (2018). Association of cystathionine beta-synthase polymorphisms and aneurysmal subarachnoid hemorrhage. J. Neurosurg. 128: 1771–1777, https://doi.org/10.3171/2017.2.jns162933.Search in Google Scholar PubMed
Hoh, B.L., Rojas, K., Lin, L., Fazal, H.Z., Hourani, S., Nowicki, K.W., Schneider, M.B., and Hosaka, K. (2018). Estrogen deficiency promotes cerebral aneurysm rupture by upregulation of Th17 cells and interleukin-17a which downregulates E-cadherin. J. Am. Heart Assoc. 7: 1–13, https://doi.org/10.1161/jaha.118.008863.Search in Google Scholar PubMed PubMed Central
Höllig, A., Stoffel-Wagner, B., Clusmann, H., Veldeman, M., Schubert, G.A., and Coburn, M. (2017). Time courses of inflammatory markers after aneurysmal subarachnoid hemorrhage and their possible relevance for future studies. Front. Neurol. 8: 694, https://doi.org/10.3389/fneur.2017.00694.Search in Google Scholar PubMed PubMed Central
Hori, S., Kashiwazaki, D., Yamamoto, S., Acker, G., Czabanka, M., Akioka, N., Kuwayama, N., Vajkoczy, P., and Kuroda, S. (2019). Impact of interethnic difference of collateral angioarchitectures on prevalence of hemorrhagic stroke in moyamoya disease. Clin. Neurosurg. 85: 134–145, https://doi.org/10.1093/neuros/nyy236.Search in Google Scholar PubMed
Howe, M.D., Zhu, L., Sansing, L.H., Gonzales, N.R., McCullough, L.D., and Edwards, N.J. (2018). Serum markers of blood–brain barrier remodeling and fibrosis as predictors of etiology and clinicoradiologic outcome in intracerebral hemorrhage. Front. Neurol. 9: 746, https://doi.org/10.3389/fneur.2018.00746.Search in Google Scholar PubMed PubMed Central
Ironside, N., Chen, C.J., Ding, D., Mayer, S.A., and Connolly, E.S. (2019). Perihematomal edema after spontaneous intracerebral hemorrhage. Stroke 50: 1626–1633, https://doi.org/10.1161/strokeaha.119.024965.Search in Google Scholar PubMed
Ishii, M., Ogawa, H., Unoki, T., An, Y., Iguchi, M., Masunaga, N., Esato, M., Chun, Y.H., Tsuji, H., Wada, H., et al.. (2017). Relationship of hypertension and systolic blood pressure with the risk of stroke or bleeding in patients with atrial fibrillation: the fushimi AF registry. Am. J. Hypertens. 30: 1073–1082, https://doi.org/10.1093/ajh/hpx094.Search in Google Scholar PubMed
Jennum, P., Iversen, H.K., Ibsen, R., and Kjellberg, J. (2015). Cost of stroke: a controlled national study evaluating societal effects on patients and their partners. BMC Health Serv. Res. 15: 1–10, https://doi.org/10.1186/s12913-015-1100-0.Search in Google Scholar PubMed PubMed Central
Joice, S.L., Mydeen, F., Couraud, P.O., Weksler, B.B., Romero, I.A., Fraser, P.A., and Easton, A.S. (2009). Modulation of blood-brain barrier permeability by neutrophils: in vitro and in vivo studies. Brain Res. 1298: 13–23, https://doi.org/10.1016/j.brainres.2009.08.076.Search in Google Scholar PubMed
Jolink, W.M.T., Lindenholz, A., van Etten, E.S., van Nieuwenhuizen, K.M., Schreuder, F.H.B.M., Kuijf, H.J., van Osch, M.J.P., Hendrikse, J., Rinkel, G.J.E., Wermer, M.J.H., et al.. (2020). Contrast leakage distant from the hematoma in patients with spontaneous ICH: a 7 T MRI study. J. Cereb. Blood Flow Metab. 40: 1002–1011, https://doi.org/10.1177/0271678x19852876.Search in Google Scholar PubMed PubMed Central
Joswig, H., Epprecht, L., Valmaggia, C., Leschka, S., Hildebrandt, G., Fournier, J.Y., and Stienen, M.N. (2016). Terson syndrome in aneurysmal subarachnoid hemorrhage—its relation to intracranial pressure, admission factors, and clinical outcome. Acta Neurochir. 158: 1027–1036, https://doi.org/10.1007/s00701-016-2766-8.Search in Google Scholar PubMed
Kaiser, S., Frase, S., Selzner, L., Lieberum, J.L., Wollborn, J., Niesen, W.D., Foit, N.A., Heiland, D.H., and Schallner, N. (2019). Neuroprotection after hemorrhagic stroke depends on cerebral heme oxygenase-1. Antioxidants 8: 1–18, https://doi.org/10.3390/antiox8100496.Search in Google Scholar PubMed PubMed Central
Katan, M. and Luft, A. (2018). Global burden of stroke. Semin. Neurol. 38: 208–211, https://doi.org/10.1055/s-0038-1649503.Search in Google Scholar PubMed
Kremer, P.H.C., Jolink, W.M.T., Kappelle, L.J., Algra, A., Klijn, C.J.M., Van Der Graaf, Y., Grobbee, D.E., Rutten, G.E.H.M., Visseren, F.L.J., Moll, F.L., et al.. (2015). Risk factors for lobar and non-lobar intracerebral hemorrhage in patients with vascular disease. PLoS One 10: e0142338, https://doi.org/10.1371/journal.pone.0142338.Search in Google Scholar PubMed PubMed Central
Kroll, M.E., Green, J., Beral, V., Sudlow, C.L.M., Brown, A., Kirichek, O., Price, A., Yang, T.O., and Reeves, G.K. (2016). Adiposity and ischemic and hemorrhagic stroke. Neurology 87: 1473–1481, https://doi.org/10.1212/wnl.0000000000003171.Search in Google Scholar PubMed PubMed Central
Lattanzi, S. and Silvestrini, M. (2016). Blood pressure in acute intra-cerebral hemorrhage. Ann. Transl. Med. 4: 1–2, https://doi.org/10.21037/atm.2016.08.04.Search in Google Scholar PubMed PubMed Central
Lattanzi, S., Brigo, F., Trinka, E., Cagnetti, C., Di Napoli, M., and Silvestrini, M. (2018). Neutrophil-to-Lymphocyte ratio in acute cerebral hemorrhage: a system review. Transl. Stroke Res. 10: 137–145, https://doi.org/10.1007/s12975-018-0649-4.Search in Google Scholar PubMed
Lattanzi, S., Cagnetti, C., Provinciali, L., and Silvestrini, M. (2017). Neutrophil-to-lymphocyte ratio and neurological deterioration following acute cerebral hemorrhage. Oncotarget 8: 57489–57494, https://doi.org/10.18632/oncotarget.15423.Search in Google Scholar PubMed PubMed Central
Lattanzi, S., Di Napoli, M., Ricci, S., and Divani, A.A. (2020). Matrix metalloproteinases in acute intracerebral hemorrhage. Neurotherapeutics 17: 484–496.10.1007/s13311-020-00839-0Search in Google Scholar PubMed PubMed Central
Lawton, M.T. and Vates, G.E. (2017). Subarachnoid hemorrhage. N. Engl. J. Med. 377: 257–266, https://doi.org/10.1056/nejmcp1605827.Search in Google Scholar PubMed
Leffert, L. R., Clancy, C. R., Bateman, B. T., Cox, M., Schulte, P. J., Smith, E. E., Fonarow, G. C., Schwamm, L. H., Kuklina, E. V., and George, M. G. (2015). Patient characteristics and outcomes after hemorrhagic stroke in pregnancy. Circ. Cardiovasc. Qual. Outcome. 8: S170–S178.10.1161/CIRCOUTCOMES.115.002242Search in Google Scholar PubMed
Leinonen, V., Vanninen, R., and Rauramaa, T. (2017). Raised intracranial pressure and brain edema. Clin. Neurol. 145: 25–37.10.1016/B978-0-12-802395-2.00004-3Search in Google Scholar PubMed
Lekander, I., Willers, C., von Euler, M., Lilja, M., Sunnerhagen, K.S., Pessah-Rasmussen, H., and Borgström, F. (2017). Relationship between functional disability and costs one and two years post stroke. PLoS One 12: e0174861, https://doi.org/10.1371/journal.pone.0174861.Search in Google Scholar PubMed PubMed Central
Li, Y.C., Wang, R., Xu, M.M., Jing, X.R., Ji-Ye, A., Sun, R.B., Na, S.J., Liu, T., Ding, X.S., Sun, C.Y., . (2019). Aneurysmal subarachnoid hemorrhage onset alters pyruvate metabolism in poor-grade patients and clinical outcome depends on more: a cerebrospinal fluid metabolomic study. ACS Chem. Neurosci. 10: 1660–1667, https://doi.org/10.1021/acschemneuro.8b00581.Search in Google Scholar PubMed
Lin, Q., Cai, J.Y., Lu, C., Sun, J., Ba, H.J., Chen, M.H., Chen, X.D., Dai, J.X., and Lin, J.H. (2017). Macrophage migration inhibitory factor levels in serum from patients with acute intracerebral hemorrhage: potential contribution to prognosis. Clin. Chim. Acta 472: 58–63, https://doi.org/10.1016/j.cca.2017.07.016.Search in Google Scholar PubMed
Lindbohm, J.V., Kaprio, J., Jousilahti, P., Salomaa, V., and Korja, M. (2016). Sex, smoking, and risk for subarachnoid hemorrhage. Stroke 47: 1975–1981, https://doi.org/10.1161/strokeaha.116.012957.Search in Google Scholar
Lu, A.Y., Damisah, E.C., Winkler, E.A., Grant, R.A., Eid, T., and Bulsara, K.R. (2018). Cerebrospinal fluid untargeted metabolomic profiling of aneurysmal subarachnoid hemorrhage: an exploratory study. Br. J. Neurosurg. 32: 637–641, https://doi.org/10.1080/02688697.2018.1519107.Search in Google Scholar PubMed
Ma, C., Zhou, W., Yan, Z., Qu, M., and Bu, X. (2015). Toll-like receptor 4 (TLR4) is correlated with delayed cerebral ischemia (DCI) and poor prognosis in aneurysmal subarachnoid hemorrhage. J. Neurol. Sci. 359: 67–71, https://doi.org/10.1016/j.jns.2015.10.018.Search in Google Scholar PubMed
Maekawa, H., Serrone, J.C., Tjahjadi, M., and Hernesniemi, J. (2016). The role of estrogen on the pathology of cerebral aneurysms. Expert Rev. Neurother. 16: 927–935, https://doi.org/10.1080/14737175.2016.1189827.Search in Google Scholar PubMed
Malinova, V., Iliev, B., Tsogkas, I., Rohde, V., Psychogios, M.-N., and Mielke, D. (2019). Assessment of tissue permeability by early CT perfusion as a surrogate parameter for early brain injury after subarachnoid hemorrhage. J. Neurosurg.: 1–6 (Epub ahead of print).10.3171/2019.5.JNS19765Search in Google Scholar PubMed
Marcolini, E., Stretz, C., and DeWitt, K.M. (2019). Intracranial hemorrhage and intracranial hypertension. Emerg. Med. Clin. 37: 529–544, https://doi.org/10.1016/j.emc.2019.04.001.Search in Google Scholar PubMed
Marini, S., Devan, W.J., Radmanesh, F., Miyares, L., Poterba, T., Hansen, B.M., Norrving, B., Jimenez-Conde, J., Giralt-Steinhauer, E., Elosua, R., et al.. (2018b). 17p12 influences hematoma volume and outcome in spontaneous intracerebral hemorrhage. Stroke 49: 1618–1625, https://doi.org/10.1161/strokeaha.117.020091.Search in Google Scholar
Marini, S., Morotti, A., Lena, U.K., Goldstein, J.N., Greenberg, S.M., Rosand, J., and Anderson, C.D. (2018a). Men experience higher risk of pneumonia and death after intracerebral hemorrhage. Neurocrit. Care 28: 77–82, https://doi.org/10.1007/s12028-017-0431-6.Search in Google Scholar PubMed PubMed Central
Michinaga, S. and Koyama, Y. (2015). Pathogenesis of brain edema and investigation into anti-edema drugs. Int. J. Mol. Sci. 16: 9949–9975, https://doi.org/10.3390/ijms16059949.Search in Google Scholar PubMed PubMed Central
Mohme, M., Sauvigny, T., Mader, M.M.D., Schweingruber, N., Maire, C.L., Rünger, A., Ricklefs, F., Regelsberger, J., Schmidt, N.O., Westphal, M., et al.. (2019). Immune characterization in aneurysmal subarachnoid hemorrhage reveals distinct monocytic activation and chemokine patterns. Transl. Stroke Res 11: 1348–1361.10.1007/s12975-019-00764-1Search in Google Scholar PubMed
Morotti, A., Busto, G., Bernardoni, A., Tamborino, C., and Fainardi, E. (2019). Association between perihematomal cerebral blood volume and intracerebral hemorrhage expansion: a computed tomography perfusion study. Ann. Neurol. 85: 943–947, https://doi.org/10.1002/ana.25466.Search in Google Scholar PubMed
Morotti, A., Charidimou, A., Phuah, C.L., Jessel, M.J., Schwab, K., Ayres, A.M., Romero, J.M., Viswanathan, A., Gurol, M.E., Greenberg, S.M., et al.. (2016). Association between serum calcium level and extent of bleeding in patients with intracerebral hemorrhage. JAMA Neurol 73: 1285–1290, https://doi.org/10.1001/jamaneurol.2016.2252.Search in Google Scholar PubMed PubMed Central
Morris, N.A., Robinson, D., Schmidt, J.M., Frey, H.P., Park, S., Agarwal, S., Connolly, E.S., and Claassen, J. (2018). Hunt-Hess 5 subarachnoid haemorrhage presenting with cardiac arrest is associated with larger volume bleeds. Resuscitation 123: 71–76, https://doi.org/10.1016/j.resuscitation.2017.12.015.Search in Google Scholar PubMed PubMed Central
Muehlschlegel, S. (2018). Subarachnoid hemorrhage. Contin. Lifelong Learn. Neurol. 24: 1623–1657, https://doi.org/10.1212/con.0000000000000679.Search in Google Scholar PubMed
Murthy, S.B., Moradiya, Y., Shah, J., Merkler, A.E., Mangat, H.S., Iadacola, C., Hanley, D.F., Kamel, H., and Ziai, W.C. (2016). Nosocomial infections and outcomes after intracerebral hemorrhage: a population-based study. Neurocrit. Care 25: 178–184, https://doi.org/10.1007/s12028-016-0282-6.Search in Google Scholar PubMed
Oberman, D.Z., Rabelo, N.N., Barros, R.R., Lopes, O., and Amorim, J. (2020). Anterior communicating artery aneurysm uncommon hemorrhagic presentation: case report. Arq. Bras. Neurocir. Braz. Neurosurg. 39: 054–057, https://doi.org/10.1055/s-0039-3402488.Search in Google Scholar
Pearce, J.M.S. (2006). Subarachnoid hemorrhage. Semin. Neurol. 26: 148–149, https://doi.org/10.1055/s-2006-933320.Search in Google Scholar PubMed
Qureshi, A.I., Malik, A.A., Saeed, O., Defillo, A., Sherr, G.T., and Suri, M.F.K. (2016). Hormone replacement therapy and the risk of subarachnoid hemorrhage in postmenopausal women. J. Neurosurg. 124: 45–50, https://doi.org/10.3171/2014.12.jns142329.Search in Google Scholar
Ramesh, S.S., Christopher, R., Indira Devi, B., and Bhat, D.I. (2019). The vascular protective role of oestradiol: a focus on postmenopausal oestradiol deficiency and aneurysmal subarachnoid haemorrhage. Biol. Rev. Camb. Phil. Soc. 94: 1897–1917, https://doi.org/10.1111/brv.12541.Search in Google Scholar PubMed
Raposo, N., Calviere, L., Cazzola, V., Planton, M., Patsoura, S., Wargny, M., Albucher, J.F., Sommet, A., Olivot, J.M., Chollet, F., et al.. (2018). Cortical superficial siderosis and acute convexity subarachnoid hemorrhage in cerebral amyloid angiopathy. Eur. J. Neurol. 25: 253–259, https://doi.org/10.1111/ene.13484.Search in Google Scholar PubMed
Rasmussen, R., Bache, S., Stavngaard, T., and Møller, K. (2019). Plasma levels of IL-6, IL-8, IL-10, ICAM-1, VCAM-1, IFNγ, and TNFα are not associated with delayed cerebral ischemia, cerebral vasospasm, or clinical outcome in patients with subarachnoid hemorrhage. World Neurosurg. 128: e1131–e1136, https://doi.org/10.1016/j.wneu.2019.05.102.Search in Google Scholar PubMed
Rasmussen, R., Stavngaard, T., Jessing, I.R., Skjøth-Rasmussen, J., Olsen, N.V., Ostrowski, S.R., Johansson, P.I., and Juhler, M. (2016). High plasma levels of neuropeptide y correlate with good clinical outcome but are not correlated to cerebral blood flow or vasospasm after subarachnoid hemorrhage. J. Neurosurg. Anesthesiol. 28: 65–70, https://doi.org/10.1097/ana.0000000000000191.Search in Google Scholar
Rass, V., Ianosi, B., Wegmann, A., Med, C., Gaasch, M., Schiefecker, A.J., Kofler, M., Lindner, A., Addis, A., Almashad, S.S., et al.. (2019). Delayed resolution of cerebral edema is associated with poor outcome after nontraumatic subarachnoid hemorrhage. Stroke 50: 828–836, https://doi.org/10.1161/strokeaha.118.024283.Search in Google Scholar PubMed
Raya, A.K. and Diringer, M.N. (2014). Treatment of subarachnoid hemorrhage. Crit. Care Clin. 30: 719–733, https://doi.org/10.1016/j.ccc.2014.06.004.Search in Google Scholar PubMed
Ridwan, S., Urbach, H., Greschus, S., von Hagen, J., Esche, J., and Boström, A. (2017). Health care costs of spontaneous aneurysmal subarachnoid hemorrhage for rehabilitation, home care, and in-hospital treatment for the first year. World Neurosurg. 97: 495–500, https://doi.org/10.1016/j.wneu.2016.09.123.Search in Google Scholar PubMed
Riederer, F. (2015). Anticoagulant reversal, blood pressure levels and anticoagulant resumption in patients with anticoagulation-related intracerebral hemorrhage. J. Neurol. Neurochir. Psychiatr. 16: 184–186.Search in Google Scholar
Rizzoni, D., Rizzoni, M., Nardin, M., Chiarini, G., Agabiti-Rosei, C., Aggiusti, C., Paini, A., Salvetti, M., and Muiesan, M.L. (2019). Vascular aging and disease of the small vessels. High Blood Press. Cardiovasc. Prev. 26: 183–189, https://doi.org/10.1007/s40292-019-00320-w.Search in Google Scholar PubMed
Rouanet, C. and Silva, G.S. (2019). Aneurysmal subarachnoid hemorrhage: current concepts and updates. Arq. Neuropsiquiatr. 77: 806–814, https://doi.org/10.1590/0004-282x20190112.Search in Google Scholar PubMed
Rowland, M.J., Garry, P., Westbrook, J., Corkill, R., Antoniades, C.A., and Pattinson, K.T.S. (2017). Acute impairment of saccadic eye movements is associated with delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. J. Neurosurg. 127: 754–760, https://doi.org/10.3171/2016.8.jns16408.Search in Google Scholar PubMed
Said, A.H.M. and El-Ghandour, N.M.F. (2015). Outcome of aneurismal subarachnoid hemorrhage: how far is vasospasm involved? – Retrospective study. Egypt. J. Radiol. Nucl. Med. 46: 111–116, https://doi.org/10.1016/j.ejrnm.2014.12.002.Search in Google Scholar
Savarraj, J., Parsha, K., Hergenroeder, G., Ahn, S., Chang, T.R., Kim, D.H., and Choi, H.A. (2018a). Early brain injury associated with systemic inflammation after subarachnoid hemorrhage. Neurocrit. Care 28: 203–211, https://doi.org/10.1007/s12028-017-0471-y.Search in Google Scholar PubMed
Savarraj, J.P., McGuire, M.F., Parsha, K., Hergenroeder, G., Bajgur, S., Ahn, S., Zhu, L., Espino, E., Chang, T., Blackburn, S., et al.. (2018b). Disruption of thrombo-inflammatory response and activation of a distinct cytokine cluster after subarachnoid hemorrhage. Cytokine 111: 334–341, https://doi.org/10.1016/j.cyto.2018.09.003.Search in Google Scholar PubMed
Sokolov, A.A., Husain, S., Sztajzel, R., Croquelois, A., Lobrinus, J.A., Thaler, D., Städler, C., Hungerbühler, H., Caso, V., Rinkel, G.J., et al.. (2016). Fatal subarachnoid hemorrhage following ischemia in vertebrobasilar dolichoectasia. Medicine (United States) 95: e4020, https://doi.org/10.1097/md.0000000000004020.Search in Google Scholar PubMed PubMed Central
Srinivasan, A., Aggarwal, A., Gaudihalli, S., Mohanty, M., Dhandapani, M., Singh, H., Mukherjee, K.K., and Dhandapani, S. (2016). Impact of early leukocytosis and elevated high-sensitivity C-reactive protein on delayed cerebral ischemia and neurologic outcome after subarachnoid hemorrhage. World Neurosurg. 90: 91–95, https://doi.org/10.1016/j.wneu.2016.02.049.Search in Google Scholar PubMed
Tarver, M. J., Schmidt, T., and Koltz, M. T. (2018). Recurrent hemorrhagic conversion of ischemic stroke in a patient with mechanical heart valve: a case report and literature review. Brain Sci. 8: 12.10.3390/brainsci8010012Search in Google Scholar PubMed PubMed Central
Ungvari, Z., Tarantini, S., Donato, A.J., Galvan, V., and Csiszar, A. (2018). Mechanisms of vascular aging. Circ. Res. 123: 849–867, https://doi.org/10.1161/circresaha.118.311378.Search in Google Scholar
van der Bilt, I.A.C., Vendeville, J.P., van de Hoef, T.P., Begieneman, M.P.V., Lagrand, W.K., Kros, J.M., Wilde, A.A.M., Rinkel, G.J.E., and Niessen, H.W.M. (2016). Myocarditis in patients with subarachnoid hemorrhage: a histopathologic study. J. Crit. Care 32: 196–200, https://doi.org/10.1016/j.jcrc.2015.12.005.Search in Google Scholar PubMed
Van Etten, E.S., Gurol, M.E., Van Der Grond, J., Haan, J., Viswanathan, A., Schwab, K.M., Ayres, A.M., Algra, A., Rosand, J., Van Buchem, M.A., et al.. (2016). Recurrent hemorrhage risk and mortality in hereditary and sporadic cerebral amyloid angiopathy. Neurology 87: 1482–1487, https://doi.org/10.1212/wnl.0000000000003181.Search in Google Scholar PubMed PubMed Central
Veltkamp, R. and Purrucker, J. (2017). Management of spontaneous intracerebral hemorrhage. Curr. Neurol. Neurosci. Rep. 17: 80, https://doi.org/10.1007/s11910-017-0783-5.Search in Google Scholar PubMed PubMed Central
Vial, F., Brunser, A., Lavados, P., and Illanes, S. (2016). Intraventricular bleeding and hematoma size as predictors of infection development in intracerebral hemorrhage: a prospective cohort study. J. Stroke Cerebrovasc. Dis. 25: 2708–2711, https://doi.org/10.1016/j.jstrokecerebrovasdis.2016.07.020.Search in Google Scholar PubMed
Vlachogiannis, P., Hillered, L., Khalil, F., Enblad, P., and Ronne-Engström, E. (2019). Interleukin-6 levels in cerebrospinal fluid and plasma in patients with severe spontaneous subarachnoid hemorrhage. World Neurosurg. 122: e612–e618, https://doi.org/10.1016/j.wneu.2018.10.113.Search in Google Scholar PubMed
Walsh, K.B., Campos, B., Hart, K., Thakar, C., and Adeoye, O. (2017). M2 monocyte microparticles are increased in intracerebral hemorrhage. J. Stroke Cerebrovasc. Dis. 26: 2369–2375, https://doi.org/10.1016/j.jstrokecerebrovasdis.2017.05.027.Search in Google Scholar PubMed PubMed Central
Wang, Z., Gong, Q., Guo, C., Luo, Y., and Chen, L. (2019). Neutrophil-to-lymphocyte ratio predicts hematoma growth in intracerebral hemorrhage. J. Int. Med. Res. 47: 2970–2975, https://doi.org/10.1177/0300060519847866.Search in Google Scholar PubMed PubMed Central
Wermer, M.J.H. and Greenberg, S.M. (2017). The growing clinical spectrum of cerebral amyloid angiopathy. Curr. Opin. Neurol 31: 28–35.10.1097/WCO.0000000000000510Search in Google Scholar PubMed
Wilkinson, D.A., Pandey, A.S., Thompson, B.G., Keep, R.F., Hua, Y., and Xi, G. (2018). Injury mechanisms in acute intracerebral hemorrhage. Neuropharmacology 134: 240–248, https://doi.org/10.1016/j.neuropharm.2017.09.033.Search in Google Scholar PubMed PubMed Central
Wilson, M.H. (2016). Monro-Kellie 2.0: the dynamic vascular and venous pathophysiological components of intracranial pressure. J. Cerebr. Blood Flow Metabol. 36: 1338–1350, https://doi.org/10.1177/0271678x16648711.Search in Google Scholar
Witvoet, E. H., Pelzer, N., Terwindt, G. M., Rinkel, G. J. E., Vlak, M. H. M., Algra, A., and Wermer, M. J. H. (2017). Migraine prevalence in patients with unruptured intracranial aneurysms: a case–control study. Brain Behav. 7: e00662.10.1002/brb3.662Search in Google Scholar PubMed PubMed Central
Woo, K.M., Yang, S.Y., and Cho, K.T. (2012). Seizures after spontaneous intracerebral hemorrha. J. Korean Neurosurg. Soc. 52: 312–319, https://doi.org/10.3340/jkns.2012.52.4.312.Search in Google Scholar PubMed PubMed Central
Yamamoto, S., Funaki, T., Fujimura, M., Takahashi, J.C., Uchino, H., Houkin, K., Tominaga, T., Miyamoto, S., and Kuroda, S. (2019). Development of hemorrhage-prone anastomoses in asymptomatic moyamoya disease—a comparative study with Japan adult moyamoya trial. J. Stroke Cerebrovasc. Dis. 28: 104328, https://doi.org/10.1016/j.jstrokecerebrovasdis.2019.104328.Search in Google Scholar PubMed
Yang, G. and Shao, G.F. (2016). Elevated serum IL-11, TNF α, and VEGF expressions contribute to the pathophysiology of hypertensive intracerebral hemorrhage (HICH). Neurol. Sci. 37: 1253–1259, https://doi.org/10.1007/s10072-016-2576-z.Search in Google Scholar PubMed
Younsi, A., Scherer, M., Unterberg, A.W., and Orakcioglu, B. (2016). Visualization of pressure related vessel compression in the perihemorrhagic zone during endoscopic ICH evacuation. Clin. Neurol. Neurosurg. 147: 64–70, https://doi.org/10.1016/j.clineuro.2016.05.020.Search in Google Scholar PubMed
Yuan, Y., Shan, N., Tan, B., Deng, Q., Liu, Y., Wang, H., Luo, X., He, C., Luo, X., Zhang, H., et al.. (2018). SRC-3 plays a critical role in human umbilical vein endothelial cells by regulating the PI3K/Akt/mTOR pathway in preeclampsia. Reprod. Sci. 25: 748–758, https://doi.org/10.1177/1933719117725818.Search in Google Scholar PubMed
Ziai, W.C. and Carhuapoma, J.R. (2018). Intracerebral hemorrhage. Contin. Lifelong Learn. Neurol. 24: 1603–1622, https://doi.org/10.1212/con.0000000000000672.Search in Google Scholar PubMed
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Articles in the same Issue
- Frontmatter
- Neuronal and glial CSF biomarkers in multiple sclerosis: a systematic review and meta-analysis
- Default mode network activity in depression subtypes
- Physical exercise promotes brain remodeling by regulating epigenetics, neuroplasticity and neurotrophins
- The physiopathology of spontaneous hemorrhagic stroke: a systematic review
- COVID-19 and stroke: from the cases to the causes
- Overview of COVID-19 and neurological complications
Articles in the same Issue
- Frontmatter
- Neuronal and glial CSF biomarkers in multiple sclerosis: a systematic review and meta-analysis
- Default mode network activity in depression subtypes
- Physical exercise promotes brain remodeling by regulating epigenetics, neuroplasticity and neurotrophins
- The physiopathology of spontaneous hemorrhagic stroke: a systematic review
- COVID-19 and stroke: from the cases to the causes
- Overview of COVID-19 and neurological complications