Login Register Cart 0
Generic placeholder image

Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

The Updated Role of the Blood Brain Barrier in Subarachnoid Hemorrhage: From Basic and Clinical Studies

Author(s): Sheng Chen*, PengLei Xu, YuanJian Fang and Cameron Lenahan

Volume 18, Issue 12, 2020

Page: [1266 - 1278] Pages: 13

DOI: 10.2174/1570159X18666200914161231

Price: $65

Abstract

Subarachnoid hemorrhage (SAH) is a type of hemorrhagic stroke associated with high mortality and morbidity. The blood-brain-barrier (BBB) is a structure consisting primarily of cerebral microvascular endothelial cells, end feet of astrocytes, extracellular matrix, and pericytes. Post-SAH pathophysiology included early brain injury and delayed cerebral ischemia. BBB disruption was a critical mechanism of early brain injury and was associated with other pathophysiological events. These pathophysiological events may propel the development of secondary brain injury, known as delayed cerebral ischemia. Imaging advancements to measure BBB after SAH primarily focused on exploring innovative methods to predict clinical outcome, delayed cerebral ischemia, and delayed infarction related to delayed cerebral ischemia in acute periods. These predictions are based on detecting abnormal changes in BBB permeability. The parameters of BBB permeability are described by changes in computed tomography (CT) perfusion and magnetic resonance imaging (MRI). Kep seems to be a stable and sensitive indicator in CT perfusion, whereas Ktrans is a reliable parameter for dynamic contrast-enhanced MRI. Future prediction models that utilize both the volume of BBB disruption and stable parameters of BBB may be a promising direction to develop practical clinical tools. These tools could provide greater accuracy in predicting clinical outcome and risk of deterioration. Therapeutic interventional exploration targeting BBB disruption is also promising, considering the extended duration of post-SAH BBB disruption.

Keywords: Subarachnoid hemorrhage, blood brain barrier, imaging, clinical trial, early brain injury, delayed cerebral ischemia.

« Previous Next »
Graphical Abstract

[1]
Lovelock, C.E.; Rinkel, G.J.; Rothwell, P.M. Time trends in outcome of subarachnoid hemorrhage: Population-based study and systematic review. Neurology, 2010, 74(19), 1494-1501.
[http://dx.doi.org/10.1212/WNL.0b013e3181dd42b3] [PMID: 20375310]
[2]
Nieuwkamp, D.J.; Setz, L.E.; Algra, A.; Linn, F.H.; de Rooij, N.K.; Rinkel, G.J. Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: a meta-analysis. Lancet Neurol., 2009, 8(7), 635-642.
[http://dx.doi.org/10.1016/S1474-4422(09)70126-7] [PMID: 19501022]
[3]
Al-Khindi, T.; Macdonald, R.L.; Schweizer, T.A. Cognitive and functional outcome after aneurysmal subarachnoid hemorrhage. Stroke, 2010, 41(8), e519-e536.
[http://dx.doi.org/10.1161/STROKEAHA.110.581975] [PMID: 20595669]
[4]
Suzuki, H. What is early brain injury? Transl. Stroke Res., 2015, 6(1), 1-3.
[http://dx.doi.org/10.1007/s12975-014-0380-8] [PMID: 25502277]
[5]
Eagles, M.E.; Jaja, B.N.R.; Macdonald, R.L. Incorporating a modified graeb score to the modified fisher scale for improved risk prediction of delayed cerebral ischemia following aneurysmal subarachnoid hemorrhage. Neurosurgery, 2018, 82(3), 299-305.
[http://dx.doi.org/10.1093/neuros/nyx165] [PMID: 28419304]
[6]
Dorhout Mees, S.M.; Kerr, R.S.; Rinkel, G.J.; Algra, A.; Molyneux, A.J. Occurrence and impact of delayed cerebral ischemia after coiling and after clipping in the International Subarachnoid Aneurysm Trial (ISAT). J. Neurol., 2012, 259(4), 679-683.
[http://dx.doi.org/10.1007/s00415-011-6243-2] [PMID: 21947244]
[7]
Rosengart, A.J.; Schultheiss, K.E.; Tolentino, J.; Macdonald, R.L. Prognostic factors for outcome in patients with aneurysmal subarachnoid hemorrhage. Stroke, 2007, 38(8), 2315-2321.
[http://dx.doi.org/10.1161/STROKEAHA.107.484360] [PMID: 17569871]
[8]
Eagles, M.E.; Tso, M.K.; Macdonald, R.L. Cognitive impairment, functional outcome, and delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. World Neurosurg., 2019, S1878-8750(19), 30020-8.
[http://dx.doi.org/10.1016/j.wneu.2018.12.152] [PMID: 30639483]
[9]
Sweeney, M.D.; Zhao, Z.; Montagne, A.; Nelson, A.R.; Zlokovic, B.V. Blood-brain barrier: From physiology to disease and back. Physiol. Rev., 2019, 99(1), 21-78.
[http://dx.doi.org/10.1152/physrev.00050.2017] [PMID: 30280653]
[10]
Tso, M.K.; Macdonald, R.L. Subarachnoid hemorrhage: a review of experimental studies on the microcirculation and the neurovascular unit. Transl. Stroke Res., 2014, 5(2), 174-189.
[http://dx.doi.org/10.1007/s12975-014-0323-4] [PMID: 24510780]
[11]
Schöller, K.; Trinkl, A.; Klopotowski, M.; Thal, S.C.; Plesnila, N.; Trabold, R.; Hamann, G.F.; Schmid-Elsaesser, R.; Zausinger, S. Characterization of microvascular basal lamina damage and blood- brain barrier dysfunction following subarachnoid hemorrhage in rats. Brain Res., 2007, 1142, 237-246.
[http://dx.doi.org/10.1016/j.brainres.2007.01.034] [PMID: 17303089]
[12]
Macdonald, R.L.; Kassell, N.F.; Mayer, S.; Ruefenacht, D.; Schmiedek, P.; Weidauer, S.; Frey, A.; Roux, S.; Pasqualin, A. CONSCIOUS-1 Investigators. Clazosentan to overcome neurological ischemia and infarction occurring after subarachnoid hemorrhage (CONSCIOUS-1): randomized, double-blind, placebo-controlled phase 2 dose-finding trial. Stroke, 2008, 39(11), 3015-3021.
[http://dx.doi.org/10.1161/STROKEAHA.108.519942] [PMID: 18688013]
[13]
Macdonald, R.L.; Higashida, R.T.; Keller, E.; Mayer, S.A.; Molyneux, A.; Raabe, A.; Vajkoczy, P.; Wanke, I.; Bach, D.; Frey, A.; Marr, A.; Roux, S.; Kassell, N. Clazosentan, an endothelin receptor antagonist, in patients with aneurysmal subarachnoid haemorrhage undergoing surgical clipping: a randomised, double-blind, placebo-controlled phase 3 trial (CONSCIOUS-2). Lancet Neurol., 2011, 10(7), 618-625.
[http://dx.doi.org/10.1016/S1474-4422(11)70108-9] [PMID: 21640651]
[14]
Peeyush Kumar, T.; McBride, D.W.; Dash, P.K.; Matsumura, K.; Rubi, A.; Blackburn, S.L. Endothelial cell dysfunction and injury in subarachnoid hemorrhage. Mol. Neurobiol., 2019, 56(3), 1992-2006.
[http://dx.doi.org/10.1007/s12035-018-1213-7] [PMID: 29982982]
[15]
Smith, M.; Citerio, G. What’s new in subarachnoid hemorrhage. Intensive Care Med., 2015, 41(1), 123-126.
[http://dx.doi.org/10.1007/s00134-014-3548-5] [PMID: 25403754]
[16]
Muehlschlegel, S. Subarachnoid hemorrhage. Continuum (Minneap. Minn.), 2018, 24(6), 1623-1657.
[http://dx.doi.org/10.1212/CON.0000000000000679] [PMID: 30516599]
[17]
Benjamin, E.J.; Virani, S.S.; Callaway, C.W.; Chamberlain, A.M.; Chang, A.R.; Cheng, S.; Chiuve, S.E.; Cushman, M.; Delling, F.N.; Deo, R.; de Ferranti, S.D.; Ferguson, J.F.; Fornage, M.; Gillespie, C.; Isasi, C.R.; Jiménez, M.C.; Jordan, L.C.; Judd, S.E.; Lackland, D.; Lichtman, J.H.; Lisabeth, L.; Liu, S.; Longenecker, C.T.; Lutsey, P.L.; Mackey, J.S.; Matchar, D.B.; Matsushita, K.; Mussolino, M.E.; Nasir, K.; O’Flaherty, M.; Palaniappan, L.P.; Pandey, A.; Pandey, D.K.; Reeves, M.J.; Ritchey, M.D.; Rodriguez, C.J.; Roth, G.A.; Rosamond, W.D.; Sampson, U.K.A.; Satou, G.M.; Shah, S.H.; Spartano, N.L.; Tirschwell, D.L.; Tsao, C.W.; Voeks, J.H.; Willey, J.Z.; Wilkins, J.T.; Wu, J.H.; Alger, H.M.; Wong, S.S.; Muntner, P. American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics-2018 update: A report from the american heart association. Circulation, 2018, 137(12), e67-e492.
[http://dx.doi.org/10.1161/CIR.0000000000000558] [PMID: 29386200]
[18]
Kusaka, G.; Ishikawa, M.; Nanda, A.; Granger, D.N.; Zhang, J.H. Signaling pathways for early brain injury after subarachnoid hemorrhage. J. Cereb. Blood Flow Metab., 2004, 24(8), 916-925.
[http://dx.doi.org/10.1097/01.WCB.0000125886.48838.7E] [PMID: 15362722]
[19]
Rass, V.; Helbok, R. Early brain injury after poor-grade subarachnoid hemorrhage. Curr. Neurol. Neurosci. Rep., 2019, 19(10), 78.
[http://dx.doi.org/10.1007/s11910-019-0990-3] [PMID: 31468197]
[20]
Sehba, F.A.; Hou, J.; Pluta, R.M.; Zhang, J.H. The importance of early brain injury after subarachnoid hemorrhage. Prog. Neurobiol., 2012, 97(1), 14-37.
[http://dx.doi.org/10.1016/j.pneurobio.2012.02.003] [PMID: 22414893]
[21]
Dhar, R.; Diringer, M.N. Relationship between angiographic vasospasm, cerebral blood flow, and cerebral infarction after subarachnoid hemorrhage. Acta Neurochir. Suppl. (Wien), 2015, 120, 161-165.
[http://dx.doi.org/10.1007/978-3-319-04981-6_27] [PMID: 25366617]
[22]
Macdonald, R.L. Delayed neurological deterioration after subarachnoid haemorrhage. Nat. Rev. Neurol., 2014, 10(1), 44-58.
[http://dx.doi.org/10.1038/nrneurol.2013.246] [PMID: 24323051]
[23]
Hansen-Schwartz, J.; Vajkoczy, P.; Macdonald, R.L.; Pluta, R.M.; Zhang, J.H. Cerebral vasospasm: looking beyond vasoconstriction. Trends Pharmacol. Sci., 2007, 28(6), 252-256.
[http://dx.doi.org/10.1016/j.tips.2007.04.002] [PMID: 17466386]
[24]
Connolly, E.S., Jr; Rabinstein, A.A.; Carhuapoma, J.R.; Derdeyn, C.P.; Dion, J.; Higashida, R.T.; Hoh, B.L.; Kirkness, C.J.; Naidech, A.M.; Ogilvy, C.S.; Patel, A.B.; Thompson, B.G.; Vespa, P. American Heart Association Stroke Council; Council on Cardiovascular Radiology and Intervention; Council on Cardiovascular Nursing; Council on Cardiovascular Surgery and Anesthesia; Council on Clinical Cardiology. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke, 2012, 43(6), 1711-1737.
[http://dx.doi.org/10.1161/STR.0b013e3182587839] [PMID: 22556195]
[25]
Zhao, Z.; Nelson, A.R.; Betsholtz, C.; Zlokovic, B.V. Establishment and dysfunction of the blood-brain barrier. Cell, 2015, 163(5), 1064-1078.
[http://dx.doi.org/10.1016/j.cell.2015.10.067] [PMID: 26590417]
[26]
Hawkins, B.T.; Davis, T.P. The blood-brain barrier/neurovascular unit in health and disease. Pharmacol. Rev., 2005, 57(2), 173-185.
[http://dx.doi.org/10.1124/pr.57.2.4] [PMID: 15914466]
[27]
Gautam, J.; Cao, Y.; Yao, Y. Pericytic laminin maintains blood-brain barrier integrity in an age-dependent manner. Transl. Stroke Res., 2020, 11(2), 228-242.
[http://dx.doi.org/10.1007/s12975-019-00709-8] [PMID: 31292838]
[28]
Armulik, A.; Genové, G.; Mäe, M.; Nisancioglu, M.H.; Wallgard, E.; Niaudet, C.; He, L.; Norlin, J.; Lindblom, P.; Strittmatter, K.; Johansson, B.R.; Betsholtz, C. Pericytes regulate the blood-brain barrier. Nature, 2010, 468(7323), 557-561.
[http://dx.doi.org/10.1038/nature09522] [PMID: 20944627]
[29]
Zhang, Y.; Zhang, X.; Wei, Q.; Leng, S.; Li, C.; Han, B.; Bai, Y.; Zhang, H.; Yao, H. Activation of sigma-1 receptor enhanced pericyte survival via the interplay between apoptosis and autophagy: Implications for blood-brain barrier integrity in stroke. Transl. Stroke Res., 11(2), 267-287.
[http://dx.doi.org/10.1007/s12975-019-00711-0] [PMID: 31290080]
[30]
Xu, W.; Mo, J.; Ocak, U.; Travis, Z.D.; Enkhjargal, B.; Zhang, T.; Wu, P.; Peng, J.; Li, T.; Zuo, Y.; Shao, A.; Tang, J.; Zhang, J.; Zhang, J.H. Activation of melanocortin 1 receptor attenuates early brain injury in a rat model of subarachnoid hemorrhage via the suppression of neuroinflammation through ampk/tbk1/nf-kappab pathway in rats. Neurotherapeutics, 2020, 17(1), 294-308.
[http://dx.doi.org/10.1007/s13311-019-00772-x] [PMID: 31486022]
[31]
Thurgur, H.; Pinteaux, E. Microglia in the neurovascular unit: Blood-brain barrier-microglia interactions after central nervous system disorders. Neuroscience, 2019, 405, 55-67.
[http://dx.doi.org/10.1016/j.neuroscience.2018.06.046] [PMID: 31007172]
[32]
Haruwaka, K.; Ikegami, A.; Tachibana, Y.; Ohno, N.; Konishi, H.; Hashimoto, A.; Matsumoto, M.; Kato, D.; Ono, R.; Kiyama, H.; Moorhouse, A.J.; Nabekura, J.; Wake, H. Dual microglia effects on blood brain barrier permeability induced by systemic inflammation. Nat. Commun., 2019, 10(1), 5816.
[http://dx.doi.org/10.1038/s41467-019-13812-z] [PMID: 31862977]
[33]
Germanò, A.; d’Avella, D.; Imperatore, C.; Caruso, G.; Tomasello, F. Time-course of blood-brain barrier permeability changes after experimental subarachnoid haemorrhage. Acta Neurochir. (Wien), 2000, 142(5), 575-580.
[http://dx.doi.org/10.1007/s007010050472] [PMID: 10898366]
[34]
Toyota, Y.; Wei, J.; Xi, G.; Keep, R.F.; Hua, Y. White matter T2 hyperintensities and blood-brain barrier disruption in the hyperacute stage of subarachnoid hemorrhage in male mice: The role of lipocalin-2. CNS Neurosci. Ther., 2019, 25(10), 1207-1214.
[http://dx.doi.org/10.1111/cns.13221] [PMID: 31568658]
[35]
Egashira, Y.; Hua, Y.; Keep, R.F.; Iwama, T.; Xi, G. Lipocalin 2 and blood-brain barrier disruption in white matter after experimental subarachnoid hemorrhage. Acta Neurochir. Suppl. (Wien), 2016, 121, 131-134.
[http://dx.doi.org/10.1007/978-3-319-18497-5_23] [PMID: 26463936]
[36]
Wang, K.C.; Tang, S.C.; Lee, J.E.; Li, Y.I.; Huang, Y.S.; Yang, W.S.; Jeng, J.S.; Arumugam, T.V.; Tu, Y.K. Cerebrospinal fluid high mobility group box 1 is associated with neuronal death in subarachnoid hemorrhage. J. Cereb. Blood Flow Metab., 2017, 37(2), 435-443.
[http://dx.doi.org/10.1177/0271678X16629484] [PMID: 26823474]
[37]
Ostrowski, R.P.; Colohan, A.R.; Zhang, J.H. Molecular mechanisms of early brain injury after subarachnoid hemorrhage. Neurol. Res., 2006, 28(4), 399-414.
[http://dx.doi.org/10.1179/016164106X115008] [PMID: 16759443]
[38]
Pisapia, J.M.; Xu, X.; Kelly, J.; Yeung, J.; Carrion, G.; Tong, H.; Meghan, S.; El-Falaky, O.M.; Grady, M.S.; Smith, D.H.; Zaitsev, S.; Muzykantov, V.R.; Stiefel, M.F.; Stein, S.C. Microthrombosis after experimental subarachnoid hemorrhage: time course and effect of red blood cell-bound thrombin-activated pro-urokinase and clazosentan. Exp. Neurol., 2012, 233(1), 357-363.
[http://dx.doi.org/10.1016/j.expneurol.2011.10.029] [PMID: 22079156]
[39]
Shao, A.; Zhu, Z.; Li, L.; Zhang, S.; Zhang, J. Emerging therapeutic targets associated with the immune system in patients with intracerebral haemorrhage (ICH): From mechanisms to translation. EBioMedicine, 2019, 45, 615-623.
[http://dx.doi.org/10.1016/j.ebiom.2019.06.012] [PMID: 31208948]
[40]
Chaichana, K.L.; Pradilla, G.; Huang, J.; Tamargo, R.J. Role of inflammation (leukocyte-endothelial cell interactions) in vasospasm after subarachnoid hemorrhage. World Neurosurg., 2010, 73(1), 22-41.
[http://dx.doi.org/10.1016/j.surneu.2009.05.027] [PMID: 20452866]
[41]
Shao, Z.; Tu, S.; Shao, A. Pathophysiological mechanisms and potential therapeutic targets in intracerebral hemorrhage. Front. Pharmacol., 2019, 10, 1079.
[http://dx.doi.org/10.3389/fphar.2019.01079] [PMID: 31607923]
[42]
Shao, A.; Zhou, Y.; Yao, Y.; Zhang, W.; Zhang, J.; Deng, Y. The role and therapeutic potential of heat shock proteins in haemorrhagic stroke. J. Cell. Mol. Med., 2019, 23(9), 5846-5858.
[http://dx.doi.org/10.1111/jcmm.14479] [PMID: 31273911]
[43]
Hänggi, D.; Etminan, N.; Aldrich, F.; Steiger, H.J.; Mayer, S.A.; Diringer, M.N.; Hoh, B.L.; Mocco, J.; Faleck, H.J.; Macdonald, R.L.; Investigators, N. NEWTON Investigators. Randomized, open-label, phase 1/2a study to determine the maximum tolerated dose of intraventricular sustained release nimodipine for subarachnoid hemorrhage (newton nimodipine microparticles to enhance recovery while reducing toxicity after subarachnoid hemorrhage). Stroke, 2017, 48(1), 145-151.
[http://dx.doi.org/10.1161/STROKEAHA.116.014250] [PMID: 27932607]
[44]
Gathier, C.S.; Dankbaar, J.W.; van der Jagt, M.; Verweij, B.H.; Oldenbeuving, A.W.; Rinkel, G.J.E.; van den Bergh, W.M.; Slooter, A.J.C.; Grp, H.S. HIMALAIA Study Group. Effects of induced hypertension on cerebral perfusion in delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage a randomized clinical trial. Stroke, 2015, 46(11), 3277-3281.
[http://dx.doi.org/10.1161/STROKEAHA.115.010537] [PMID: 26443829]
[45]
Gathier, C.S.; van den Bergh, W.M.; van der Jagt, M.; Verweij, B.H.; Dankbaar, J.W.; Müller, M.C.; Oldenbeuving, A.W.; Rinkel, G.J.E.; Slooter, A.J.C.; Grp, H.S. HIMALAIA Study Group. Induced hypertension for delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage a randomized clinical trial. Stroke, 2018, 49(1), 76-83.
[http://dx.doi.org/10.1161/STROKEAHA.117.017956] [PMID: 29158449]
[46]
Dreier, J.P. The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat. Med., 2011, 17(4), 439-447.
[http://dx.doi.org/10.1038/nm.2333] [PMID: 21475241]
[47]
Matsuda, N.; Naraoka, M.; Ohkuma, H.; Shimamura, N.; Ito, K.; Asano, K.; Hasegawa, S.; Takemura, A. Effect of cilostazol on cerebral vasospasm and outcome in patients with aneurysmal subarachnoid hemorrhage: A randomized, double-blind, placebo- controlled trial. Cerebrovasc. Dis., 2016, 42(1-2), 97-105.
[http://dx.doi.org/10.1159/000445509] [PMID: 27070952]
[48]
Niu, P.P.; Yang, G.; Xing, Y.Q.; Guo, Z.N.; Yang, Y. Effect of cilostazol in patients with aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. J. Neurol. Sci., 2014, 336(1-2), 146-151.
[http://dx.doi.org/10.1016/j.jns.2013.10.027] [PMID: 24211059]
[49]
Sugimoto, K.; Nomura, S.; Shirao, S.; Inoue, T.; Ishihara, H.; Kawano, R.; Kawano, A.; Oka, F.; Suehiro, E.; Sadahiro, H.; Shinoyama, M.; Oku, T.; Maruta, Y.; Hirayama, Y.; Hiyoshi, K.; Kiyohira, M.; Yoneda, H.; Okazaki, K.; Dreier, J.P.; Suzuki, M. Cilostazol decreases duration of spreading depolarization and spreading ischemia after aneurysmal subarachnoid hemorrhage. Ann. Neurol., 2018, 84(6), 873-885.
[http://dx.doi.org/10.1002/ana.25361] [PMID: 30341966]
[50]
Tani, E.; Matsumoto, T. Continuous elevation of intracellular Ca2+ is essential for the development of cerebral vasospasm. Curr. Vasc. Pharmacol., 2004, 2(1), 13-21.
[http://dx.doi.org/10.2174/1570161043476492] [PMID: 15320829]
[51]
Muehlschlegel, S.; Sims, J.R. Dantrolene: mechanisms of neuroprotection and possible clinical applications in the neurointensive care unit. Neurocrit. Care, 2009, 10(1), 103-115.
[http://dx.doi.org/10.1007/s12028-008-9133-4] [PMID: 18696266]
[52]
Salomone, S.; Soydan, G.; Moskowitz, M.A.; Sims, J.R. Inhibition of cerebral vasoconstriction by dantrolene and nimodipine. Neurocrit. Care, 2009, 10(1), 93-102.
[http://dx.doi.org/10.1007/s12028-008-9153-0] [PMID: 18923817]
[53]
Muehlschlegel, S.; Rordorf, G.; Sims, J. Effects of a single dose of dantrolene in patients with cerebral vasospasm after subarachnoid hemorrhage: a prospective pilot study. Stroke, 2011, 42(5), 1301-1306.
[http://dx.doi.org/10.1161/STROKEAHA.110.603159] [PMID: 21454813]
[54]
Muehlschlegel, S.; Carandang, R.; Hall, W.; Kini, N.; Izzy, S.; Garland, B.; Ouillette, C.; van der Bom, I.M.J.; Flood, T.F.; Gounis, M.J.; Weaver, J.P.; Barton, B.; Wakhloo, A.K. Dantrolene for cerebral vasospasm after subarachnoid haemorrhage: a randomised double blind placebo-controlled safety trial. J. Neurol. Neurosurg. Psychiatry, 2015, 86(9), 1029-1035.
[http://dx.doi.org/10.1136/jnnp-2014-308778] [PMID: 25344064]
[55]
Sen, J.; Belli, A.; Albon, H.; Morgan, L.; Petzold, A.; Kitchen, N. Triple-H therapy in the management of aneurysmal subarachnoid haemorrhage. Lancet Neurol., 2003, 2(10), 614-621.
[http://dx.doi.org/10.1016/S1474-4422(03)00531-3] [PMID: 14505583]
[56]
Rinkel, G.J.; Feigin, V.L.; Algra, A.; van Gijn, J. Circulatory volume expansion therapy for aneurysmal subarachnoid haemorrhage. Cochrane Database Syst. Rev., 2004, (4), CD000483.
[http://dx.doi.org/10.1002/14651858.CD000483.pub2] [PMID: 15494997]
[57]
Ekelund, A.; Reinstrup, P.; Ryding, E.; Andersson, A.M.; Molund, T.; Kristiansson, K.A.; Romner, B.; Brandt, L.; Säveland, H. Effects of iso- and hypervolemic hemodilution on regional cerebral blood flow and oxygen delivery for patients with vasospasm after aneurysmal subarachnoid hemorrhage. Acta Neurochir. (Wien), 2002, 144(7), 703-712.
[http://dx.doi.org/10.1007/s00701-002-0959-9] [PMID: 12181704]
[58]
Raabe, A.; Beck, J.; Keller, M.; Vatter, H.; Zimmermann, M.; Seifert, V. Relative importance of hypertension compared with hypervolemia for increasing cerebral oxygenation in patients with cerebral vasospasm after subarachnoid hemorrhage. J. Neurosurg., 2005, 103(6), 974-981.
[http://dx.doi.org/10.3171/jns.2005.103.6.0974] [PMID: 16381183]
[59]
Dankbaar, J.W.; Slooter, A.J.; Rinkel, G.J.; Schaaf, I.C. Effect of different components of triple-H therapy on cerebral perfusion in patients with aneurysmal subarachnoid haemorrhage: a systematic review. Crit. Care, 2010, 14(1), R23.
[http://dx.doi.org/10.1186/cc8886] [PMID: 20175912]
[60]
Geraghty, J.R.; Testai, F.D. Delayed cerebral ischemia after subarachnoid hemorrhage: Beyond vasospasm and towards a multifactorial pathophysiology. Curr. Atheroscler. Rep., 2017, 19(12), 50.
[http://dx.doi.org/10.1007/s11883-017-0690-x] [PMID: 29063300]
[61]
Gathier, C.S.; van den Bergh, W.M.; Slooter, A.J. Himalaia (hypertension induction in the management of aneurysmal subarachnoid haemorrhage with secondary ischaemia): A randomized single-blind controlled trial of induced hypertension vs. No induced hypertension in the treatment of delayed cerebral ischemia after subarachnoid hemorrhage. Int. J. Stroke, 2014, 9(3), 375-380.
[http://dx.doi.org/10.1111/ijs.12055] [PMID: 23692645]
[62]
Murphy, A.; de Oliveira Manoel, A.L.; Macdonald, R.L.; Baker, A.; Lee, T.Y.; Marotta, T.; Montanera, W.; Aviv, R.; Bharatha, A. Changes in cerebral perfusion with induced hypertension in aneurysmal subarachnoid hemorrhage: A pilot and feasibility study. Neurocrit. Care, 2017, 27(1), 3-10.
[http://dx.doi.org/10.1007/s12028-017-0379-6] [PMID: 28244000]
[63]
Sanelli, P.C.; Anumula, N.; Johnson, C.E.; Comunale, J.P.; Tsiouris, A.J.; Riina, H.; Segal, A.Z.; Stieg, P.E.; Zimmerman, R.D.; Mushlin, A.I. Evaluating CT perfusion using outcome measures of delayed cerebral ischemia in aneurysmal subarachnoid hemorrhage. AJNR Am. J. Neuroradiol., 2013, 34(2), 292-298.
[http://dx.doi.org/10.3174/ajnr.A3225] [PMID: 22859289]
[64]
Dorhout Mees, S.M.; Rinkel, G.J.; Feigin, V.L.; Algra, A.; van den Bergh, W.M.; Vermeulen, M.; van Gijn, J. Calcium antagonists for aneurysmal subarachnoid haemorrhage. Cochrane Database Syst. Rev., 2007, (3), CD000277.
[http://dx.doi.org/10.1002/14651858.CD000277.pub3] [PMID: 17636626]
[65]
Pickard, J.D.; Murray, G.D.; Illingworth, R.; Shaw, M.D.; Teasdale, G.M.; Foy, P.M.; Humphrey, P.R.; Lang, D.A.; Nelson, R.; Richards, P. Effect of oral nimodipine on cerebral infarction and outcome after subarachnoid haemorrhage: British aneurysm nimodipine trial. BMJ, 1989, 298(6674), 636-642.
[http://dx.doi.org/10.1136/bmj.298.6674.636] [PMID: 2496789]
[66]
Choi, H.A.; Ko, S.B.; Chen, H.; Gilmore, E.; Carpenter, A.M.; Lee, D.; Claassen, J.; Mayer, S.A.; Schmidt, J.M.; Lee, K.; Connelly, E.S.; Paik, M.; Badjatia, N. Acute effects of nimodipine on cerebral vasculature and brain metabolism in high grade subarachnoid hemorrhage patients. Neurocrit. Care, 2012, 16(3), 363-367.
[http://dx.doi.org/10.1007/s12028-012-9670-8] [PMID: 22262041]
[67]
Sandow, N.; Diesing, D.; Sarrafzadeh, A.; Vajkoczy, P.; Wolf, S. Nimodipine dose reductions in the treatment of patients with aneurysmal subarachnoid hemorrhage. Neurocrit. Care, 2016, 25(1), 29-39.
[http://dx.doi.org/10.1007/s12028-015-0230-x] [PMID: 26690937]
[68]
Hänggi, D.; Etminan, N.; Mayer, S.A.; Aldrich, E.F.; Diringer, M.N.; Schmutzhard, E.; Faleck, H.J.; Ng, D.; Saville, B.R.; Macdonald, R.L. NEWTON Investigators. Clinical trial protocol: Phase 3, multicenter, randomized, double-blind, placebo-controlled, parallel-group, efficacy, and safety study comparing eg-1962 to standard of care oral nimodipine in adults with aneurysmal subarachnoid hemorrhage. Neurocrit. Care, 2019, 30(1), 88-97.
[http://dx.doi.org/10.1007/s12028-018-0575-z] [PMID: 30014184]
[69]
Beer, R.; Lackner, P.; Pfausler, B.; Schmutzhard, E. Nosocomial ventriculitis and meningitis in neurocritical care patients. J. Neurol., 2008, 255(11), 1617-1624.
[http://dx.doi.org/10.1007/s00415-008-0059-8] [PMID: 19156484]
[70]
Champey, J.; Mourey, C.; Francony, G.; Pavese, P.; Gay, E.; Gergele, L.; Manet, R.; Velly, L.; Bruder, N.; Payen, J.F. Strategies to reduce external ventricular drain-related infections: a multicenter retrospective study. J. Neurosurg., 2018, 1-6.
[http://dx.doi.org/10.3171/2018.1.Jns172486] [PMID: 29932377]
[71]
Ecker, A.; Riemenschneider, P.A. Arteriographic demonstration of spasm of the intracranial arteries, with special reference to saccular arterial aneurysms. J. Neurosurg., 1951, 8(6), 660-667.
[http://dx.doi.org/10.3171/jns.1951.8.6.0660] [PMID: 14889314]
[72]
Hansen-Schwartz, J. Cerebral vasospasm: a consideration of the various cellular mechanisms involved in the pathophysiology. Neurocrit. Care, 2004, 1(2), 235-246.
[http://dx.doi.org/10.1385/NCC:1:2:235] [PMID: 16174921]
[73]
Koskinen, L.D.; Sundström, N.; Hägglund, L.; Eklund, A.; Olivecrona, M. Prostacyclin affects the relation between brain interstitial glycerol and cerebrovascular pressure reactivity in severe traumatic brain injury. Neurocrit. Care, 2019, 31(3), 494-500.
[http://dx.doi.org/10.1007/s12028-019-00741-4] [PMID: 31123992]
[74]
Moncada, S.; Higgs, E.A.; Vane, J.R. Human arterial and venous tissues generate prostacyclin (prostaglandin x), a potent inhibitor of platelet aggregation. Lancet, 1977, 1(8001), 18-20.
[http://dx.doi.org/10.1016/S0140-6736(77)91655-5] [PMID: 63657]
[75]
Brandt, L.; Ljunggren, B.; Andersson, K.E.; Hindfelt, B.; Uski, T. Effects of indomethacin and prostacyclin on isolated human pial arteries contracted by CSF from patients with aneurysmal SAH. J. Neurosurg., 1981, 55(6), 877-883.
[http://dx.doi.org/10.3171/jns.1981.55.6.0877] [PMID: 6795316]
[76]
Koskinen, L.O.; Olivecrona, M.; Rodling-Wahlström, M.; Naredi, S. Prostacyclin treatment normalises the MCA flow velocity in nimodipine-resistant cerebral vasospasm after aneurysmal subarachnoid haemorrhage: a pilot study. Acta Neurochir. (Wien), 2009, 151(6), 595-599.
[http://dx.doi.org/10.1007/s00701-009-0295-4] [PMID: 19350202]
[77]
Rasmussen, R.; Wetterslev, J.; Stavngaard, T.; Juhler, M.; Skjøth-Rasmussen, J.; Grände, P.O.; Olsen, N.V. Effects of prostacyclin on cerebral blood flow and vasospasm after subarachnoid hemorrhage: randomized, pilot trial. Stroke, 2015, 46(1), 37-41.
[http://dx.doi.org/10.1161/STROKEAHA.114.007470] [PMID: 25414173]
[78]
Gybel-Brask, M.; Rasmussen, R.; Stensballe, J.; Johansson, P.I.; Ostrowski, S.R. Effect of delayed onset prostacyclin on markers of endothelial function and damage after subarachnoid hemorrhage. Acta Neurochir. (Wien), 2017, 159(6), 1073-1078.
[http://dx.doi.org/10.1007/s00701-017-3168-2] [PMID: 28386837]
[79]
Endres, M.; Laufs, U.; Huang, Z.; Nakamura, T.; Huang, P.; Moskowitz, M.A.; Liao, J.K. Stroke protection by 3-hydroxy-3-methylglutaryl (HMG)-CoA reductase inhibitors mediated by endothelial nitric oxide synthase. Proc. Natl. Acad. Sci. USA, 1998, 95(15), 8880-8885.
[http://dx.doi.org/10.1073/pnas.95.15.8880] [PMID: 9671773]
[80]
Weitz-Schmidt, G. Statins as anti-inflammatory agents. Trends Pharmacol. Sci., 2002, 23(10), 482-486.
[http://dx.doi.org/10.1016/S0165-6147(02)02077-1] [PMID: 12368073]
[81]
McGirt, M.J.; Lynch, J.R.; Parra, A.; Sheng, H.; Pearlstein, R.D.; Laskowitz, D.T.; Pelligrino, D.A.; Warner, D.S. Simvastatin increases endothelial nitric oxide synthase and ameliorates cerebral vasospasm resulting from subarachnoid hemorrhage. Stroke, 2002, 33(12), 2950-2956.
[http://dx.doi.org/10.1161/01.STR.0000038986.68044.39] [PMID: 12468796]
[82]
Chou, S.H.; Smith, E.E.; Badjatia, N.; Nogueira, R.G.; Sims, J.R., II; Ogilvy, C.S.; Rordorf, G.A.; Ayata, C. A randomized, double-blind, placebo-controlled pilot study of simvastatin in aneurysmal subarachnoid hemorrhage. Stroke, 2008, 39(10), 2891-2893.
[http://dx.doi.org/10.1161/STROKEAHA.107.505875] [PMID: 18658043]
[83]
Lynch, J.R.; Wang, H.; McGirt, M.J.; Floyd, J.; Friedman, A.H.; Coon, A.L.; Blessing, R.; Alexander, M.J.; Graffagnino, C.; Warner, D.S.; Laskowitz, D.T. Simvastatin reduces vasospasm after aneurysmal subarachnoid hemorrhage: results of a pilot randomized clinical trial. Stroke, 2005, 36(9), 2024-2026.
[http://dx.doi.org/10.1161/01.STR.0000177879.11607.10] [PMID: 16051891]
[84]
Tseng, M.Y.; Czosnyka, M.; Richards, H.; Pickard, J.D.; Kirkpatrick, P.J. Effects of acute treatment with pravastatin on cerebral vasospasm, autoregulation, and delayed ischemic deficits after aneurysmal subarachnoid hemorrhage: a phase II randomized placebo-controlled trial. Stroke, 2005, 36(8), 1627-1632.
[http://dx.doi.org/10.1161/01.STR.0000176743.67564.5d] [PMID: 16049199]
[85]
Wong, G.K.C.; Chan, D.Y.C.; Siu, D.Y.W.; Zee, B.C.Y.; Poon, W.S.; Chan, M.T.V.; Gin, T.; Leung, M. HDS-SAH Investigators. High-dose simvastatin for aneurysmal subarachnoid hemorrhage: multicenter randomized controlled double-blinded clinical trial. Stroke, 2015, 46(2), 382-388.
[http://dx.doi.org/10.1161/STROKEAHA.114.007006] [PMID: 25516195]
[86]
Kirkpatrick, P.J.; Turner, C.L.; Smith, C.; Hutchinson, P.J.; Murray, G.D. STASH Collaborators. Simvastatin in aneurysmal subarachnoid haemorrhage (STASH): a multicentre randomised phase 3 trial. Lancet Neurol., 2014, 13(7), 666-675.
[http://dx.doi.org/10.1016/S1474-4422(14)70084-5] [PMID: 24837690]
[87]
Lin, J.; Liu, H.; Jiang, J.; Jia, C.; Zhang, B.; Gao, X. Clinical evidence of efficacy of simvastatin for aneurysmal subarachnoid hemorrhage. J. Int. Med. Res., 2017, 45(6), 2128-2138.
[http://dx.doi.org/10.1177/0300060517713803] [PMID: 28661267]
[88]
Liu, H.; Xu, X. Effect of simvastatin in patients with aneurysmal subarachnoid hemorrhage: A systematic review and meta-analysis. Am. J. Emerg. Med., 2017, 35(12), 1940-1945.
[http://dx.doi.org/10.1016/j.ajem.2017.09.001] [PMID: 28966073]
[89]
Diringer, M.N.; Dhar, R.; Scalfani, M.; Zazulia, A.R.; Chicoine, M.; Powers, W.J.; Derdeyn, C.P. Effect of high-dose simvastatin on cerebral blood flow and static autoregulation in subarachnoid hemorrhage. Neurocrit. Care, 2016, 25(1), 56-63.
[http://dx.doi.org/10.1007/s12028-015-0233-7] [PMID: 26721259]
[90]
Wong, G.K.; Wong, A.; Zee, B.C.; Poon, W.S.; Chan, M.T.; Gin, T.; Siu, D.Y.; Mok, V.C. Cognitive outcome in acute simvastatin treatment for aneurysmal subarachnoid hemorrhage: A propensity matched analysis. J. Neurol. Sci., 2015, 358(1-2), 58-61.
[http://dx.doi.org/10.1016/j.jns.2015.08.013] [PMID: 26285662]
[91]
To, M.S.; Prakash, S.; Poonnoose, S.I.; Bihari, S. Dose-dependent effects of statins for patients with aneurysmal subarachnoid hemorrhage: Meta-regression analysis. World Neurosurg., 2018, 113, 153-162.
[http://dx.doi.org/10.1016/j.wneu.2018.01.184] [PMID: 29425980]
[92]
Bederson, J.B.; Germano, I.M.; Guarino, L. Cortical blood flow and cerebral perfusion pressure in a new noncraniotomy model of subarachnoid hemorrhage in the rat. Stroke, 1995, 26(6), 1086-1091.
[http://dx.doi.org/10.1161/01.STR.26.6.1086] [PMID: 7762027]
[93]
Voldby, B.; Enevoldsen, E.M. Intracranial pressure changes following aneurysm rupture. Part 1: clinical and angiographic correlations. J. Neurosurg., 1982, 56(2), 186-196.
[http://dx.doi.org/10.3171/jns.1982.56.2.0186] [PMID: 7054427]
[94]
Cahill, J.; Calvert, J.W.; Zhang, J.H. Mechanisms of early brain injury after subarachnoid hemorrhage. J. Cereb. Blood Flow Metab., 2006, 26(11), 1341-1353.
[http://dx.doi.org/10.1038/sj.jcbfm.9600283] [PMID: 16482081]
[95]
Xu, W.; Gao, L.; Li, T.; Zheng, J.; Shao, A.; Zhang, J. Apelin-13 alleviates early brain injury after subarachnoid hemorrhage via suppression of endoplasmic reticulum stress-mediated apoptosis and blood-brain barrier disruption: Possible involvement of atf6/chop pathway. Neuroscience, 2018, 388, 284-296.
[http://dx.doi.org/10.1016/j.neuroscience.2018.07.023] [PMID: 30036660]
[96]
Zubkov, A.Y.; Ogihara, K.; Bernanke, D.H.; Parent, A.D.; Zhang, J. Apoptosis of endothelial cells in vessels affected by cerebral vasospasm. Surg. Neurol., 2000, 53(3), 260-266.
[http://dx.doi.org/10.1016/S0090-3019(99)00187-1] [PMID: 10773259]
[97]
Kishore, S.; Ko, N.; Soares, B.P.; Higashida, R.T.; Tong, E.; Bhogal, S.; Bredno, J.; Cheng, S.C.; Wintermark, M. Perfusion-CT assessment of blood-brain barrier permeability in patients with aneurysmal subarachnoid hemorrhage. J. Neuroradiol., 2012, 39(5), 317-325.
[http://dx.doi.org/10.1016/j.neurad.2011.11.004] [PMID: 22197406]
[98]
Schmidt, J.M.; Wartenberg, K.E.; Fernandez, A.; Claassen, J.; Rincon, F.; Ostapkovich, N.D.; Badjatia, N.; Parra, A.; Connolly, E.S.; Mayer, S.A. Frequency and clinical impact of asymptomatic cerebral infarction due to vasospasm after subarachnoid hemorrhage. J. Neurosurg., 2008, 109(6), 1052-1059.
[http://dx.doi.org/10.3171/JNS.2008.109.12.1052] [PMID: 19035719]
[99]
Dankbaar, J.W.; de Rooij, N.K.; Velthuis, B.K.; Frijns, C.J.; Rinkel, G.J.; van der Schaaf, I.C. Diagnosing delayed cerebral ischemia with different CT modalities in patients with subarachnoid hemorrhage with clinical deterioration. Stroke, 2009, 40(11), 3493-3498.
[http://dx.doi.org/10.1161/STROKEAHA.109.559013] [PMID: 19762703]
[100]
Sanelli, P.C.; Ugorec, I.; Johnson, C.E.; Tan, J.; Segal, A.Z.; Fink, M.; Heier, L.A.; Tsiouris, A.J.; Comunale, J.P.; John, M.; Stieg, P.E.; Zimmerman, R.D.; Mushlin, A.I. Using quantitative CT perfusion for evaluation of delayed cerebral ischemia following aneurysmal subarachnoid hemorrhage. AJNR Am. J. Neuroradiol., 2011, 32(11), 2047-2053.
[http://dx.doi.org/10.3174/ajnr.A2693] [PMID: 21960495]
[101]
Wintermark, M.; Sincic, R.; Sridhar, D.; Chien, J.D. Cerebral perfusion CT: technique and clinical applications. J. Neuroradiol., 2008, 35(5), 253-260.
[http://dx.doi.org/10.1016/j.neurad.2008.03.005] [PMID: 18466974]
[102]
Aviv, R.I.; d’Esterre, C.D.; Murphy, B.D.; Hopyan, J.J.; Buck, B.; Mallia, G.; Li, V.; Zhang, L.; Symons, S.P.; Lee, T.Y. Hemorrhagic transformation of ischemic stroke: prediction with CT perfusion. Radiology, 2009, 250(3), 867-877.
[http://dx.doi.org/10.1148/radiol.2503080257] [PMID: 19244051]
[103]
Ivanidze, J.; Kesavabhotla, K.; Kallas, O.N.; Mir, D.; Baradaran, H.; Gupta, A.; Segal, A.Z.; Claassen, J.; Sanelli, P.C. Evaluating blood-brain barrier permeability in delayed cerebral infarction after aneurysmal subarachnoid hemorrhage. AJNR Am. J. Neuroradiol., 2015, 36(5), 850-854.
[http://dx.doi.org/10.3174/ajnr.A4207] [PMID: 25572949]
[104]
Murphy, A.; Manoel, A.L.; Burgers, K.; Kouzmina, E.; Lee, T.; Macdonald, R.L.; Bharatha, A. Early CT perfusion changes and blood-brain barrier permeability after aneurysmal subarachnoid hemorrhage. Neuroradiology, 2015, 57(8), 767-773.
[http://dx.doi.org/10.1007/s00234-015-1529-1] [PMID: 25868518]
[105]
Ivanidze, J.; Kallas, O.N.; Gupta, A.; Weidman, E.; Baradaran, H.; Mir, D.; Giambrone, A.; Segal, A.Z.; Claassen, J.; Sanelli, P.C. Application of blood-brain barrier permeability imaging in global cerebral edema. AJNR Am. J. Neuroradiol., 2016, 37(9), 1599-1603.
[http://dx.doi.org/10.3174/ajnr.A4784] [PMID: 27127002]
[106]
Mir, D.I.; Gupta, A.; Dunning, A.; Puchi, L.; Robinson, C.L.; Epstein, H.A.; Sanelli, P.C. CT perfusion for detection of delayed cerebral ischemia in aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. AJNR Am. J. Neuroradiol., 2014, 35(5), 866-871.
[http://dx.doi.org/10.3174/ajnr.A3787] [PMID: 24309123]
[107]
Ivanidze, J.; Ferraro, R.A.; Giambrone, A.E.; Segal, A.Z.; Gupta, A.; Sanelli, P.C. AJR Am. J. Roentgenol., 2018, 211(4), 891-895.
[http://dx.doi.org/10.2214/AJR.17.18237] [PMID: 30085836]
[108]
Mocco, J.; Prickett, C.S.; Komotar, R.J.; Connolly, E.S.; Mayer, S.A. Potential mechanisms and clinical significance of global cerebral edema following aneurysmal subarachnoid hemorrhage. Neurosurg. Focus, 2007, 22(5), E7.
[http://dx.doi.org/10.3171/foc.2007.22.5.8] [PMID: 17613238]
[109]
Shigeno, T.; Fritschka, E.; Brock, M.; Schramm, J.; Shigeno, S. Cervoś-Navarro, J. Cerebral edema following experimental subarachnoid hemorrhage. Stroke, 1982, 13(3), 368-379.
[http://dx.doi.org/10.1161/01.STR.13.3.368] [PMID: 7080133]
[110]
Dreier, J.P.; Lemale, C.L.; Kola, V.; Friedman, A.; Schoknecht, K. Spreading depolarization is not an epiphenomenon but the principal mechanism of the cytotoxic edema in various gray matter structures of the brain during stroke. Neuropharmacology, 2018, 134(Pt B), 189-207.
[http://dx.doi.org/10.1016/j.neuropharm.2017.09.027]
[111]
Hayman, E.G.; Wessell, A.; Gerzanich, V.; Sheth, K.N.; Simard, J.M. Mechanisms of global cerebral edema formation in aneurysmal subarachnoid hemorrhage. Neurocrit. Care, 2017, 26(2), 301-310.
[http://dx.doi.org/10.1007/s12028-016-0354-7] [PMID: 27995510]
[112]
Zhang, C.; Jiang, M.; Wang, W-Q.; Zhao, S-J.; Yin, Y-X.; Mi, Q-J.; Yang, M-F.; Song, Y-Q.; Sun, B-L.; Zhang, Z-Y. Selective mglur1 negative allosteric modulator reduces blood-brain barrier permeability and cerebral edema after experimental subarachnoid hemorrhage. Transl. Stroke Res., 2019, 11(4), 799-811.
[http://dx.doi.org/10.1007/s12975-019-00758-z] [PMID: 31833035]
[113]
Kreiter, K.T.; Copeland, D.; Bernardini, G.L.; Bates, J.E.; Peery, S.; Claassen, J.; Du, Y.E.; Stern, Y.; Connolly, E.S.; Mayer, S.A. Predictors of cognitive dysfunction after subarachnoid hemorrhage. Stroke, 2002, 33(1), 200-208.
[http://dx.doi.org/10.1161/hs0102.101080] [PMID: 11779911]
[114]
Claassen, J.; Carhuapoma, J.R.; Kreiter, K.T.; Du, E.Y.; Connolly, E.S.; Mayer, S.A. Global cerebral edema after subarachnoid hemorrhage: frequency, predictors, and impact on outcome. Stroke, 2002, 33(5), 1225-1232.
[http://dx.doi.org/10.1161/01.STR.0000015624.29071.1F] [PMID: 11988595]
[115]
Lublinsky, S.; Major, S.; Kola, V.; Horst, V.; Santos, E.; Platz, J.; Sakowitz, O.; Scheel, M.; Dohmen, C.; Graf, R.; Vatter, H.; Wolf, S.; Vajkoczy, P.; Shelef, I.; Woitzik, J.; Martus, P.; Dreier, J.P.; Friedman, A. Early blood-brain barrier dysfunction predicts neurological outcome following aneurysmal subarachnoid hemorrhage. EBioMedicine, 2019, 43, 460-472.
[http://dx.doi.org/10.1016/j.ebiom.2019.04.054] [PMID: 31162113]
[116]
de Rooij, N.K.; Greving, J.P.; Rinkel, G.J.; Frijns, C.J. Early prediction of delayed cerebral ischemia after subarachnoid hemorrhage: development and validation of a practical risk chart. Stroke, 2013, 44(5), 1288-1294.
[http://dx.doi.org/10.1161/STROKEAHA.113.001125] [PMID: 23512975]
[117]
Moroz, J.; Reinsberg, S.A. Dynamic Contrast-Enhanced MRI. Methods Mol. Biol., 2018, 1718, 71-87.
[http://dx.doi.org/10.1007/978-1-4939-7531-0_5] [PMID: 29341003]
[118]
Barnes, S.R.; Ng, T.S.; Montagne, A.; Law, M.; Zlokovic, B.V.; Jacobs, R.E. Optimal acquisition and modeling parameters for accurate assessment of low Ktrans blood-brain barrier permeability using dynamic contrast-enhanced MRI. Magn. Reson. Med., 2016, 75(5), 1967-1977.
[http://dx.doi.org/10.1002/mrm.25793] [PMID: 26077645]
[119]
Russin, J.J.; Montagne, A.; D’Amore, F.; He, S.; Shiroishi, M.S.; Rennert, R.C.; Depetris, J.; Zlokovic, B.V.; Mack, W.J. Permeability imaging as a predictor of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. J. Cereb. Blood Flow Metab., 2018, 38(6), 973-979.
[http://dx.doi.org/10.1177/0271678X18768670] [PMID: 29611451]

Rights & Permissions Print Cite
Article Metrics
24
© 2024 Bentham Science Publishers | Privacy Policy