The Role of Thromboinflammation in Delayed Cerebral Ischemia after Subarachnoid Hemorrhage

Devin W McBride, Spiros L Blackburn, Kumar T Peeyush, Kanako Matsumura, John H Zhang, Devin W McBride, Spiros L Blackburn, Kumar T Peeyush, Kanako Matsumura, John H Zhang

Abstract

Delayed cerebral ischemia (DCI) is a major determinant of patient outcome following aneurysmal subarachnoid hemorrhage. Although the exact mechanisms leading to DCI are not fully known, inflammation, cerebral vasospasm, and microthrombi may all function together to mediate the onset of DCI. Indeed, inflammation is tightly linked with activation of coagulation and microthrombi formation. Thromboinflammation is the intersection at which inflammation and thrombosis regulate one another in a feedforward manner, potentiating the formation of thrombi and pro-inflammatory signaling. In this review, we will explore the role(s) of inflammation and microthrombi in subarachnoid hemorrhage (SAH) pathophysiology and DCI, and discuss the potential of targeting thromboinflammation to prevent DCI after SAH.

Keywords: cerebral vasospasm; delayed cerebral ischemia; inflammation; subarachnoid hemorrhage; thromboinflammation; thrombosis.

Figures

Figure 1
Figure 1
Initiation of inflammation and thrombosis after subarachnoid hemorrhage. Following rupture of an aneurysm, red blood cells spill into the subarachnoid space, activating macrophages which release cytokines. In response, endothelial cells express adhesion molecules to activate circulating leukocytes and platelets. This results in leukocyte infiltration, phagocytosis of red blood cells, and release of more cytokines. Activated platelets develop into thrombi which may travel downstream to occlude distal microvessels or may cross into the brain parenchyma. Platelet activation and aggregation signal for leukocyte activation, and vice versa, such that even when the aneurysm is treated, thromboinflammation continues via feedforward mechanisms.

References

    1. Connolly ES, Jr, Rabinstein AA, Carhuapoma JR, Derdeyn CP, Dion J, Higashida RT, 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(6):1711–37.10.1161/STR.0b013e3182587839
    1. Grunwald IQ, Kuhn AL, Schmitt AJ, Balami JS. Aneurysmal SAH: current management and complications associated with treatment and disease. J Invasive Cardiol (2014) 26(1):30–7.
    1. de Rooij NK, Linn FH, van der Plas JA, Algra A, Rinkel GJ. Incidence of subarachnoid haemorrhage: a systematic review with emphasis on region, age, gender and time trends. J Neurol Neurosurg Psychiatry (2007) 78(12):1365–72.10.1136/jnnp.2007.117655
    1. Cossu G, Messerer M, Oddo M, Daniel RT. To look beyond vasospasm in aneurysmal subarachnoid hemorrhage. Biomed Res Int (2014) 2014:628597.10.1155/2014/628597
    1. Foreman B. The pathophysiology of delayed cerebral ischemia. J Clin Neurophysiol (2016) 33(3):174–82.10.1097/WNP.0000000000000273
    1. Macdonald RL. Delayed neurological deterioration after subarachnoid haemorrhage. Nat Rev Neurol (2014) 10(1):44–58.10.1038/nrneurol.2013.246
    1. Brilstra EH, Rinkel GJ, Algra A, van Gijn J. Rebleeding, secondary ischemia, and timing of operation in patients with subarachnoid hemorrhage. Neurology (2000) 55(11):1656–60.10.1212/WNL.55.11.1656
    1. Schweizer TA, Al-Khindi T, Macdonald RL. Mini-mental state examination versus montreal cognitive assessment: rapid assessment tools for cognitive and functional outcome after aneurysmal subarachnoid hemorrhage. J Neurol Sci (2012) 316(1–2):137–40.10.1016/j.jns.2012.01.003
    1. Vergouwen MD, Vermeulen M, van Gijn J, Rinkel GJ, Wijdicks EF, Muizelaar JP, 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(10):2391–5.10.1161/STROKEAHA.110.589275
    1. Frontera JA, Fernandez A, Schmidt JM, Claassen J, Wartenberg KE, Badjatia N, et al. Defining vasospasm after subarachnoid hemorrhage: what is the most clinically relevant definition? Stroke (2009) 40(6):1963–8.10.1161/STROKEAHA.108.544700
    1. Schmidt JM, Wartenberg KE, Fernandez A, Claassen J, Rincon F, Ostapkovich ND, et al. Frequency and clinical impact of asymptomatic cerebral infarction due to vasospasm after subarachnoid hemorrhage. J Neurosurg (2008) 109(6):1052–9.10.3171/JNS.2008.109.12.1052
    1. Springer MV, Schmidt JM, Wartenberg KE, Frontera JA, Badjatia N, Mayer SA. Predictors of global cognitive impairment 1 year after subarachnoid hemorrhage. Neurosurgery (2009) 65(6):1043–50; discussion 50–1.10.1227/01.NEU.0000359317.15269.20
    1. Dankbaar JW, Rijsdijk M, van der Schaaf IC, Velthuis BK, Wermer MJH, Rinkel GJE. Relationship between vasospasm, cerebral perfusion, and delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. Neuroradiology (2009) 51(12):813–9.10.1007/s00234-009-0575-y
    1. Etminan N, Vergouwen MDI, Ilodigwe D, Macdonald RL. Effect of pharmaceutical treatment on vasospasm, delayed cerebral ischemia, and clinical outcome in patients with aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. J Cereb Blood Flow Metab (2011) 31(6):1443–51.10.1038/jcbfm.2011.7
    1. Kramer A, Fletcher J. Do endothelin-receptor antagonists prevent delayed neurological deficits and poor outcomes after aneurysmal subarachnoid hemorrhage? A meta-analysis. Stroke (2009) 40(10):3403–6.10.1161/STROKEAHA.109.560243
    1. Macdonald RL, Higashida RT, Keller E, Mayer SA, Molyneux A, Raabe A, et al. Randomised trial of clazosentan, an endothelin receptor antagonist, in patients with aneurysmal subarachnoid hemorrhage undergoing surgical clipping (CONSCIOUS-2). Acta Neurochir Suppl (2013) 115:27–31.10.1007/978-3-7091-1192-5_7
    1. Rabinstein AA, Friedman JA, Nichols DA, Pichelmann MA, McClelland RL, Manno EM, et al. Predictors of outcome after endovascular treatment of cerebral vasospasm. Am J Neuroradiol (2004) 25(10):1778–82.
    1. Chamling B, Gross S, Stoffel-Wagner B, Schubert GA, Clusmann H, Coburn M, et al. Early diagnosis of delayed cerebral ischemia: possible relevance for inflammatory biomarkers in routine clinical practice? World Neurosurg (2017) 104:152–7.10.1016/j.wneu.2017.05.021
    1. Lucke-Wold BP, Logsdon AF, Manoranjan B, Turner RC, McConnell E, Vates GE, et al. Aneurysmal subarachnoid hemorrhage and neuroinflammation: a comprehensive review. Int J Mol Sci (2016) 17(4):497.10.3390/ijms17040497
    1. Ascenzi P, Bocedi A, Visca P, Altruda F, Tolosano E, Beringhelli T, et al. Hemoglobin and heme scavenging. IUBMB Life (2005) 57(11):749–59.10.1080/15216540500380871
    1. Fujii M, Yan J, Rolland WB, Soejima Y, Caner B, Zhang JH. Early brain injury, an evolving frontier in subarachnoid hemorrhage research. Trans Stroke Res (2013) 4(4):432–46.10.1007/s12975-013-0257-2
    1. Sehba FA, Hou J, Pluta RM, Zhang JH. The importance of early brain injury after subarachnoid hemorrhage. Prog Neurobiol (2012) 97(1):14–37.10.1016/j.pneurobio.2012.02.003
    1. McMahon CJ, Hopkins S, Vail A, King AT, Smith D, Illingworth KJ, et al. Inflammation as a predictor for delayed cerebral ischemia after aneurysmal subarachnoid haemorrhage. J Neurointerv Surg (2013) 5(6):512–7.10.1136/neurintsurg-2012-010386
    1. Provencio JJ. Inflammation in subarachnoid hemorrhage and delayed deterioration associated with vasospasm: a review. Acta Neurochir Suppl (2013) 115:233–8.10.1007/978-3-7091-1192-5_42
    1. Chou SH, Feske SK, Atherton J, Konigsberg RG, De Jager PL, Du R, et al. Early elevation of serum tumor necrosis factor-alpha is associated with poor outcome in subarachnoid hemorrhage. J Investig Med (2012) 60(7):1054–8.10.2310/JIM.0b013e3182686932
    1. Gruber A, Rossler K, Graninger W, Donner A, Illievich MU, Czech T. Ventricular cerebrospinal fluid and serum concentrations of sTNFR-I, IL-1ra, and IL-6 after aneurysmal subarachnoid hemorrhage. J Neurosurg Anesthesiol (2000) 12(4):297–306.10.1097/00008506-200010000-00001
    1. Hendryk S, Jarzab B, Josko J. Increase of the IL-1 beta and IL-6 levels in CSF in patients with vasospasm following aneurysmal SAH. Neuro Endocrinol Lett (2004) 25(1–2):141–7.
    1. Ramchand P, Nyirjesy S, Frangos S, Doerfler S, Nawalinski K, Quattrone F, et al. Thromboelastography parameter predicts outcome after subarachnoid hemorrhage: an exploratory analysis. World Neurosurg (2016) 96:215–21.10.1016/j.wneu.2016.04.002
    1. 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(11):1761–70.10.1038/jcbfm.2008.74
    1. Salvarani C, Brown RD, Jr, Hunder GG. Adult primary central nervous system vasculitis. Lancet (2012) 380(9843):767–77.10.1016/S0140-6736(12)60069-5
    1. Albert-Weissenberger C, Mencl S, Schuhmann MK, Salur I, Gob E, Langhauser F, et al. C1-Inhibitor protects from focal brain trauma in a cortical cryolesion mice model by reducing thrombo-inflammation. Front Cell Neurosci (2014) 8:269.10.3389/fncel.2014.00269
    1. De Meyer SF, Denorme F, Langhauser F, Geuss E, Fluri F, Kleinschnitz C. Thromboinflammation in stroke brain damage. Stroke (2016) 47(4):1165–72.10.1161/STROKEAHA.115.011238
    1. Gragnano F, Sperlongano S, Golia E, Natale F, Bianchi R, Crisci M, et al. The role of von Willebrand factor in vascular inflammation: from pathogenesis to targeted therapy. Mediators Inflamm (2017) 2017:5620314.10.1155/2017/5620314
    1. Kehrel BE, Fender AC. Resolving thromboinflammation in the brain after ischemic stroke? Circulation (2016) 133(22):2128–31.10.1161/CIRCULATIONAHA.116.022858
    1. Hartz S, Menart B, Tschoepe D. Leukocyte apoptosis in whole blood involves platelet-dependent coaggregation. Cytometry A (2003) 52(2):117–21.10.1002/cyto.a.10026
    1. Swystun LL, Liaw PC. The role of leukocytes in thrombosis. Blood (2016) 128(6):753–62.10.1182/blood-2016-05-718114
    1. da Fonseca ACC, Matias D, Garcia C, Amaral R, Geraldo LH, Freitas C, et al. The impact of microglial activation on blood-brain barrier in brain diseases. Front Cell Neurosci (2014) 8:362.10.3389/fncel.2014.00362
    1. Munakata A, Naraoka M, Katagai T, Shimamura N, Ohkuma H. Role of cyclooxygenase-2 in relation to nitric oxide and endothelin-1 on pathogenesis of cerebral vasospasm after subarachnoid hemorrhage in rabbit. Trans Stroke Res (2016) 7(3):220–7.10.1007/s12975-016-0466-6
    1. Chauhan AK, Kisucka J, Brill A, Walsh MT, Scheiflinger F, Wagner DD. ADAMTS13: a new link between thrombosis and inflammation. J Exp Med (2008) 205(9):2065–74.10.1084/jem.20080130
    1. Vergouwen MD, Bakhtiari K, van Geloven N, Vermeulen M, Roos YB, Meijers JC. Reduced ADAMTS13 activity in delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. J Cereb Blood Flow Metab (2009) 29(10):1734–41.10.1038/jcbfm.2009.88
    1. Hendrix P, Foreman PM, Harrigan MR, Fisher WSR, Vyas NA, Lipsky RH, et al. Association of plasminogen activator inhibitor 1 (SERPINE1 gene) polymorphisms and aneurysmal subarachnoid hemorrhage. World Neurosurg (2017) 105:672–77.10.3171/2017.2.JNS162933
    1. McGee MP, Foster S, Wang X. Simultaneous expression of tissue factor and tissue factor pathway inhibitor by human monocytes. A potential mechanism for localized control of blood coagulation. J Exp Med (1994) 179(6):1847–54.10.1084/jem.179.6.1847
    1. McCachren SS, Diggs J, Weinberg JB, Dittman WA. Thrombomodulin expression by human blood monocytes and by human synovial tissue lining macrophages. Blood (1991) 78:3128–32.
    1. Galligan L, Livingstone W, Volkov Y, Hokamp K, Murphy C, Lawler M, et al. Characterization of protein C receptor expression in monocytes. Br J Haematol (2001) 115(2):408–14.10.1046/j.1365-2141.2001.03187.x
    1. Shantsila E, Lip GY. The role of monocytes in thrombotic disorders. Insights from tissue factor, monocyte-platelet aggregates and novel mechanisms. Thromb Haemost (2009) 102(5):916–24.10.1160/TH09-01-0023
    1. Pham CT. Neutrophil serine proteases: specific regulators of inflammation. Nat Rev Immunol (2006) 6(7):541–50.10.1038/nri1841
    1. Basavaraj MG, Gruber FX, Sovershaev M, Appelbom HI, Osterud B, Petersen LC, et al. The role of TFPI in regulation of TF-induced thrombogenicity on the surface of human monocytes. Thromb Res (2010) 126(5):418–25.10.1016/j.thromres.2010.07.014
    1. Belaaouaj AA, Li A, Wun TC, Welgus HG, Shapiro SD. Matrix metalloproteinases cleave tissue factor pathway inhibitor. Effects on coagulation. J Biol Chem (2000) 275(35):27123–8.10.1074/jbc.M004218200
    1. Massberg S, Grahl L, von Bruehl ML, Manukyan D, Pfeiler S, Goosmann C, et al. Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat Med (2010) 16(8):887–96.10.1038/nm.2184
    1. Stein SC, Browne KD, Chen XH, Smith DH, Graham DI. Thromboembolism and delayed cerebral ischemia after subarachnoid hemorrhage: an autopsy study. Neurosurgery (2006) 59(4):781–7; discussion 7–8.10.1227/01.NEU.0000227519.27569.45
    1. Suzuki S, Kimura M, Souma M, Ohkima H, Shimizu T, Iwabuchi T. Cerebral microthrombosis in symptomatic cerebral vasospasm – a quantitative histological study in autopsy cases. Neurol Med Chir (Tokyo) (1990) 30(5):309–16.10.2176/nmc.30.309
    1. Hirashima Y, Hamada H, Kurimoto M, Origasa H, Endo S. Decrease in platelet count as an independent risk factor for symptomatic vasospasm following aneurysmal subarachnoid hemorrhage. J Neurosurg (2005) 102(5):882–7.10.3171/jns.2005.102.5.0882
    1. Vinge E, Brandt L, Ljunggren B, Andersson KE. Thromboxane B2 levels in serum during continuous administration of nimodipine to patients with aneurysmal subarachnoid hemorrhage. Stroke (1988) 19(5):644–7.10.1161/01.STR.19.5.644
    1. Boluijt J, Meijers JC, Rinkel GJ, Vergouwen MD. Hemostasis and fibrinolysis in delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage: a systematic review. J Cereb Blood Flow Metab (2015) 35(5):724–33.10.1038/jcbfm.2015.13
    1. Ji Y, Meng QH, Wang ZG. Changes in the coagulation and fibrinolytic system of patients with subarachnoid hemorrhage. Neurol Med Chir (Tokyo) (2014) 54(6):457–64.10.2176/nmc.oa2013-0006
    1. Peltonen S, Juvela S, Kaste M, Lassila R. Hemostasis and fibrinolysis activation after subarachnoid hemorrhage. J Neurosurg (1997) 87(2):207–14.10.3171/jns.1997.87.2.0207
    1. Al-Hamodi ZH, Saif-Ali R, Ismail IS, Ahmed KA, Muniandy S. Plasminogen activator inhibitor-1 4G/5G polymorphism is associated with metabolic syndrome parameters in Malaysian subjects. J Clin Biochem Nutr (2012) 50(3):184–9.10.3164/jcbn.11-48
    1. Sonneveld MA, de Maat MP, Portegies ML, Kavousi M, Hofman A, Turecek PL, et al. Low ADAMTS13 activity is associated with an increased risk of ischemic stroke. Blood (2015) 126(25):2739–46.10.1182/blood-2015-05-643338
    1. Mathiesen T, Edner G, Ulfarsson E, Andersson B. Cerebrospinal fluid interleukin-1 receptor antagonist and tumor necrosis factor-alpha following subarachnoid hemorrhage. J Neurosurg (1997) 87(2):215–20.10.3171/jns.1997.87.2.0215
    1. Graetz D, Nagel A, Schlenk F, Sakowitz O, Vajkoczy P, Sarrafzadeh A. High ICP as trigger of proinflammatory IL-6 cytokine activation in aneurysmal subarachnoid hemorrhage. Neurol Res (2010) 32(7):728–35.10.1179/016164109X12464612122650
    1. Fassbender K, Hodapp B, Rossol S, Bertsch T, Schmeck J, Schutt S, et al. Inflammatory cytokines in subarachnoid haemorrhage: association with abnormal blood flow velocities in basal cerebral arteries. J Neurol Neurosurg Psychiatry (2001) 70(4):534–7.10.1136/jnnp.70.4.534
    1. Gaetani P, Tartara F, Pignatti P, Tancioni F, Rodriguez y Baena R, De Benedetti F. Cisternal CSF levels of cytokines after subarachnoid hemorrhage. Neurol Res (1998) 20(4):337–42.10.1080/01616412.1998.11740528
    1. Hirashima Y, Nakamura S, Endo S, Kuwayama N, Naruse Y, Takaku A. Elevation of platelet activating factor, inflammatory cytokines, and coagulation factors in the internal jugular vein of patients with subarachnoid hemorrhage. Neurochem Res (1997) 22(10):1249–55.10.1023/A:1021985030331
    1. Kikuchi T, Okuda Y, Kaito N, Abe T. Cytokine production in cerebrospinal fluid after subarachnoid haemorrhage. Neurol Res (1995) 17(2):106–8.10.1080/01616412.1995.11740296
    1. Mathiesen T, Andersson B, Loftenius A, von Holst H. Increased interleukin-6 levels in cerebrospinal fluid following subarachnoid hemorrhage. J Neurosurg (1993) 78(4):562–7.10.3171/jns.1993.78.4.0562
    1. Osuka K, Suzuki Y, Tanazawa T, Hattori K, Yamamoto N, Takayasu M, et al. Interleukin-6 and development of vasospasm after subarachnoid haemorrhage. Acta Neurochir (Wien) (1998) 140(9):943–51.10.1007/s007010050197
    1. Osuka K, Watanabe Y, Aoyama M, Nakura T, Matsuo N, Takayasu M. Expression of suppressor of cytokine signaling 3 in cerebrospinal fluid after subarachnoid hemorrhage. J Neuroinflammation (2014) 11:142.10.1186/s12974-014-0142-2
    1. Takizawa T, Tada T, Kitazawa K, Tanaka Y, Hongo K, Kameko M, et al. Inflammatory cytokine cascade released by leukocytes in cerebrospinal fluid after subarachnoid hemorrhage. Neurol Res (2001) 23(7):724–30.10.1179/016164101101199243
    1. Kubo Y, Ogasawara K, Kakino S, Kashimura H, Tomitsuka N, Sugawara A, et al. Serum inflammatory adhesion molecules and high-sensitivity C-reactive protein correlates with delayed ischemic neurologic deficits after subarachnoid hemorrhage. Surg Neurol (2008) 69(6):592–6; discussion 6.10.1016/j.surneu.2008.02.014
    1. Mack WJ, Mocco J, Hoh DJ, Huang J, Choudhri TF, Kreiter KT, et al. Outcome prediction with serum intercellular adhesion molecule-1 levels after aneurysmal subarachnoid hemorrhage. J Neurosurg (2002) 96(1):71–5.10.3171/jns.2002.96.1.0071
    1. Mocco J, Mack WJ, Kim GH, Lozier AP, Laufer I, Kreiter KT, et al. Rise in serum soluble intercellular adhesion molecule-1 levels with vasospasm following aneurysmal subarachnoid hemorrhage. J Neurosurg (2002) 97(3):537–41.10.3171/jns.2002.97.3.0537
    1. Frijns CJ, Kasius KM, Algra A, Fijnheer R, Rinkel GJ. Endothelial cell activation markers and delayed cerebral ischaemia in patients with subarachnoid haemorrhage. J Neurol Neurosurg Psychiatry (2006) 77(7):863–7.10.1136/jnnp.2005.064956
    1. Nissen JJ, Mantle D, Gregson B, Mendelow AD. Serum concentration of adhesion molecules in patients with delayed ischaemic neurological deficit after aneurysmal subarachnoid haemorrhage: the immunoglobulin and selectin superfamilies. J Neurol Neurosurg Psychiatry (2001) 71(3):329–33.10.1136/jnnp.71.3.329
    1. Denis CV, Wagner DD. Platelet adhesion receptors and their ligands in mouse models of thrombosis. Arterioscler Thromb Vasc Biol (2007) 27(4):728–39.10.1161/01.ATV.0000259359.52265.62
    1. Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol (2007) 7(9):678–89.10.1038/nri2156
    1. Wagner DD. New links between inflammation and thrombosis. Arterioscler Thromb Vasc Biol (2005) 25(7):1321–4.10.1161/01.ATV.0000166521.90532.44
    1. Crompton MR. The pathogenesis of cerebral infarction following the rupture of cerebral berry aneurysms. Brain (1964) 87:491–510.10.1093/brain/87.3.491
    1. Gallia GL, Tamargo RJ. Leukocyte-endothelial cell interactions in chronic vasospasm after subarachnoid hemorrhage. Neurol Res (2006) 28(7):750–8.10.1179/016164106X152025
    1. Hughes JT, Schianchi PM. Cerebral artery spasm. A histological study at necropsy of the blood vessels in cases of subarachnoid hemorrhage. J Neurosurg (1978) 48(4):515–25.10.3171/jns.1978.48.4.0515
    1. Pluta RM, Zauner A, Morgan JK, Muraszko KM, Oldfield EH. Is vasospasm related to proliferative arteriopathy? J Neurosurg (1992) 77(5):740–8.10.3171/jns.1992.77.5.0740
    1. Spallone A, Acqui M, Pastore FS, Guidetti B. Relationship between leukocytosis and ischemic complications following aneurysmal subarachnoid hemorrhage. Surg Neurol (1987) 27(3):253–8.10.1016/0090-3019(87)90038-3
    1. Frontera JA, Provencio JJ, Sehba FA, McIntyre TM, Nowacki AS, Gordon E, et al. The role of platelet activation and inflammation in early brain injury following subarachnoid hemorrhage. Neurocrit Care (2017) 26(1):48–57.10.1007/s12028-016-0292-4
    1. Andereggen L, Neuschmelting V, von Gunten M, Widmer HR, Fandino J, Marbacher S. The role of microclot formation in an acute subarachnoid hemorrhage model in the rabbit. Biomed Res Int (2014) 2014:161702.10.1155/2014/161702
    1. Sabri M, Ai J, Lakovic K, D’Abbondanza J, Ilodigwe D, Macdonald RL. Mechanisms of microthrombi formation after experimental subarachnoid hemorrhage. Neuroscience (2012) 224:26–37.10.1016/j.neuroscience.2012.08.002
    1. Tso MK, Macdonald RL. Acute microvascular changes after subarachnoid hemorrhage and transient global cerebral ischemia. Stroke Res Treat (2013) 2013:425281.10.1155/2013/425281
    1. Wang Z, Chen G, Zhu WW, Bian JY, Shen XO, Zhou D. Influence of simvastatin on microthrombosis in the brain after subarachnoid hemorrhage in rats: a preliminary study. Ann Clin Lab Sci (2010) 40(1):32–42.
    1. Herz DA, Baez S, Shulman K. Pial microcirculation in subarachnoid hemorrhage. Stroke (1975) 6(4):417–24.10.1161/01.STR.6.4.417
    1. Sehba FA, Mostafa G, Friedrich V, Jr, Bederson JB. Acute microvascular platelet aggregation after subarachnoid hemorrhage. J Neurosurg (2005) 102(6):1094–100.10.3171/jns.2005.102.6.1094
    1. Maddahi A, Ansar S, Chen Q, Edvinsson L. Blockade of the MEK/ERK pathway with a raf inhibitor prevents activation of pro-inflammatory mediators in cerebral arteries and reduction in cerebral blood flow after subarachnoid hemorrhage in a rat model. J Cereb Blood Flow Metab (2011) 31(1):144–54.10.1038/jcbfm.2010.62
    1. Maddahi A, Povlsen G, Edvinsson L. Regulation of enhanced cerebrovascular expression of proinflammatory mediators in experimental subarachnoid hemorrhage via the mitogen-activated protein kinase kinase/extracellular signal-regulated kinase pathway. J Neuroinflammation (2012) 9:274.10.1186/1742-2094-9-274
    1. Handa Y, Kubota T, Kaneko M, Tsuchida A, Kobayashi H, Kawano H, et al. Expression of intercellular adhesion molecule 1 (ICAM-1) on the cerebral artery following subarachnoid haemorrhage in rats. Acta Neurochir (1995) 132(1):92–7.10.1007/BF01404854
    1. Lin CL, Dumont AS, Calisaneller T, Kwan AL, Hwong SL, Lee KS. Monoclonal antibody against E selectin attenuates subarachnoid hemorrhage-induced cerebral vasospasm. Surg Neurol (2005) 64(3):201–5; discussion 5–6.10.1016/j.surneu.2005.04.038
    1. Friedrich V, Flores R, Muller A, Bi W, Peerschke EIB, Sehba FA. Reduction of neutrophil activity decreases early microvascular injury after subarachnoid haemorrhage. J Neuroinflammation (2011) 8:103.10.1186/1742-2094-8-103
    1. Hayman EG, Patel AP, James RF, Simard JM. Heparin and heparin-derivatives in post-subarachnoid hemorrhage brain injury: a multimodal therapy for a multimodal disease. Molecules (2017) 22(5):724.10.3390/molecules22050724
    1. Satoh S-I, Yamamoto Y, Toshima Y, Ikegaki I, Asano T, Suzuki Y, et al. Fasudil, a protein kinase inhibitor, prevents the development of endothelial injury and neutrophil infiltration in a two-haemorrhage canine subarachnoid model. J Clin Neurosci (1999) 6(5):394–9.10.1016/S0967-5868(99)90034-6
    1. Stokes KY, Granger DN. Platelets: a critical link between inflammation and microvascular dysfunction. J Physiol (2012) 590(5):1023–34.10.1113/jphysiol.2011.225417
    1. Dorhout Mees SM, van den Bergh WM, Algra A, Rinkel GJ. Antiplatelet therapy for aneurysmal subarachnoid haemorrhage. Cochrane Database Syst Rev (2007) 4:CD006184.10.1002/14651858.CD006184.pub2
    1. Kramer AH, Roberts DJ, Holodinsky J, Todd S, Hill MD, Zygun DA, et al. Intraventricular tissue plasminogen activator in subarachnoid hemorrhage patients: a prospective, randomized, placebo-controlled pilot trial. Neurocrit Care (2014) 21(2):275–84.10.1007/s12028-014-9965-z
    1. Litrico S, Almairac F, Gaberel T, Ramakrishna R, Fontaine D, Sedat J, et al. Intraventricular fibrinolysis for severe aneurysmal intraventricular hemorrhage: a randomized controlled trial and meta-analysis. Neurosurg Rev (2013) 36(4):523–30; discussion 30–1.10.1007/s10143-013-0469-7
    1. Etminan N, Beseoglu K, Eicker SO, Turowski B, Steiger H-J, Hanggi D. Prospective, randomized, open-label phase ii trial on concomitant intraventricular fibrinolysis and low-frequency rotation after severe subarachnoid hemorrhage. Stroke (2013) 44:2162–8.10.1161/STROKEAHA.113.001790
    1. Grasso G, Tomasello G, Noto M, Alafaci C, Cappello F. Erythropoietin for the treatment of subarachnoid hemorrhage: a feasible ingredient for a successful medical recipe. Mol Med (2015) 21(1):979–87.10.2119/molmed.2015.00177
    1. Tseng MY, Hutchinson PJ, Richards HK, Czosnyka M, Pickard JD, Erber WN, et al. Acute systemic erythropoietin therapy to reduce delayed ischemic deficits following aneurysmal subarachnoid hemorrhage: a phase II randomized, double-blind, placebo-controlled trial. Clinical article. J Neurosurg (2009) 111(1):171–80.10.3171/2009.3.JNS081332
    1. Veldeman M, Höllig A, Clusmann H, Stevanovic A, Rossaint R, Coburn M. Delayed cerebral ischaemia prevention and treatment after aneurysmal subarachnoid haemorrhage: a systematic review. Br J Anaesth (2016) 117(1):17–40.10.1093/bja/aew095
    1. Gomis P, Graftieaux JP, Sercombe R, Hettler D, Scherpereel B, Rousseaux P. Randomized, double-blind, placebo-controlled, pilot trial of high-dose methylprednisolone in aneurysmal subarachnoid hemorrhage. J Neurosurg (2010) 112(3):681–8.10.3171/2009.4.JNS081377
    1. Mijailovic M, Lukic S, Laudanovic D, Folic M, Folic N, Jankovic S. Effects of nimodipine on cerebral vasospasm in patients with aneurysmal subarachnoid hemorrhage treated by endovascular coiling. Adv Clin Exp Med (2013) 22(1):101–9.
    1. Castanares-Zapatero D, Hantson P. Pharmacological treatment of delayed cerebral ischemia and vasospasm in subarachnoid hemorrhage. Ann Intensive Care (2011) 1(1):12.10.1186/2110-5820-1-12
    1. Raya AK, Diringer MN. Treatment of subarachnoid hemorrhage. Crit Care Clin (2014) 30(4):719–33.10.1016/j.ccc.2014.06.004
    1. Etminan N, Macdonald RL. Management of aneurysmal subarachnoid hemorrhage. Handb Clin Neurol (2017) 140:195–228.10.1016/B978-0-444-63600-3.00012-X
    1. Sanz JM, Chiozzi P, Colaianna M, Zotti M, Ferrari D, Trabace L, et al. Nimodipine inhibits IL-1beta release stimulated by amyloid beta from microglia. Br J Pharmacol (2012) 167(8):1702–11.10.1111/j.1476-5381.2012.02112.x
    1. Martinez LL, Aparecida De Oliveira M, Fortes ZB. Influence of verapamil and diclofenac on leukocyte migration in rats. Hypertension (1999) 34(4 Pt 2):997–1001.10.1161/01.HYP.34.4.997
    1. Zhao J, Zhou D, Guo J, Ren Z, Zhou L, Wang S, et al. Efficacy and safety of fasudil in patients with subarachnoid hemorrhage: final results of a randomized trial of fasudil versus nimodipine. Neurol Med Chir (Tokyo) (2011) 51(10):679–83.10.2176/nmc.51.679
    1. Liu GJ, Wang ZJ, Wang YF, Xu LL, Wang XL, Liu Y, et al. Systematic assessment and meta-analysis of the efficacy and safety of fasudil in the treatment of cerebral vasospasm in patients with subarachnoid hemorrhage. Eur J Clin Pharmacol (2012) 68(2):131–9.10.1007/s00228-011-1100-x
    1. Liu Y-F, Qiu H-Q, Su J, Jiang W-J. Drug treatment of cerebral vasospasm after subarachnoid hemorrhage following aneurysms. Chinese Neurosurg J (2016) 2:4.10.1186/s41016-016-0023-x
    1. Liu AJ, Ling F, Wang D, Wang Q, Lu XD, Liu YL. Fasudil inhibits platelet-derived growth factor-induced human pulmonary artery smooth muscle cell proliferation by up-regulation of p27kip(1) via the ERK signal pathway. Chinese Med J (2011) 124(19):3098–104.
    1. Slotta JE, Braun OO, Menger MD, Thorlacius H. Fasudil, a Rho-kinase inhibitor, inhibits leukocyte adhesion in inflamed large blood vessels in vivo. Inflamm Res (2006) 55(9):364–7.10.1007/s00011-006-6013-2
    1. Wessell A, Kole MJ, Badjatia N, Parikh G, Albrecht JS, Schreibman DL, et al. High compliance with scheduled nimodipine is associated with better outcome in aneurysmal subarachnoid hemorrhage patients cotreated with heparin infusion. Front Neurol (2017) 8:268.10.3389/fneur.2017.00268
    1. Simard JM, Aldrich EF, Schreibman D, James RF, Polifka A, Beaty N. Low-dose intravenous heparin infusion in patients with aneurysmal subarachnoid hemorrhage: a preliminary assessment. J Neurosurg (2013) 119(6):1611–9.10.3171/2013.8.JNS1337
    1. Stapler S, Farris D, Luke C, Diaz J, Henke P, Wakefield T, et al. Efficacy of apixaban on thrombus resolution and anti-inflammation in a murine model of acute deep venous thrombosis. J Vascular Surg Venous Lymphat Disord (2016) 4(1):139–40.10.1016/j.jvsv.2015.10.019
    1. Zemer-Wassercug N, Haim M, Leshem-Lev D, Orvin KL, Vaduganathan M, Gutstein A, et al. The effect of dabigatran and rivaroxaban on platelet reactivity and inflammatory markers. J Thromb Thrombolysis (2015) 40(3):340–6.10.1007/s11239-015-1245-z
    1. Neville B, Fareed J, Florian-Kujawski M, Cera L, Duff R, Valero A, et al. Coagulation profiling of human, non-human, primate, pig, dog, rabbit, and rat plasma: pharmacologic implications. FASEB J (2006) 20:A655–6.
    1. Siller-Matula JM, Plasenzotti R, Spiel A, Quehenberger P, Jilma B. Interspecies differences in coagulation profile. Thromb Haemost (2008) 100(3):397–404.10.1160/TH08-02-0103
    1. Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol (2005) 5(12):953–64.10.1038/nri1733
    1. Sharp FR, Jickling GC. Modelling immunity and inflammation in stroke: differences between rodents and humans? Stroke (2014) 45(9):e179–80.10.1161/STROKEAHA.114.005639

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