Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on sleep in brain health

LIVE: Thursday 2nd May 2024, 18:00-19:30 (CEST)

Quality sleep is essential for health. But what happens to our brains when sleep patterns are disturbed? Join our experts to explore the interplay between sleep disruption and neurological diseases, and the questions that you need to be asking your patients to help you prevent the harmful effects of sleep deprivation.
ADVANCED SEARCH
Log in
Top
Translational Stroke Research
Published in: Translational Stroke Research 2/2014

01-04-2014 | Original Article

Subarachnoid Hemorrhage: a Review of Experimental Studies on the Microcirculation and the Neurovascular Unit

Authors: Michael K. Tso, R. Loch Macdonald

Published in: Translational Stroke Research | Issue 2/2014

Login to get access

Abstract

Increasingly, experimental research in subarachnoid hemorrhage (SAH) has investigated early brain injury and the microcirculation. A number of pathophysiological changes occur in the cerebral microvessels after SAH including altered vasoreactivity, vasoconstriction, inflammation, blood–brain barrier impairment, increased microthrombi, and inversion of neurovascular coupling. This focused review looks at the current state of knowledge regarding the changes that occur in the microcirculation and the neurovascular unit after SAH.
Literature
1.
Rosengart AJ, Schultheiss KE, Tolentino J, Macdonald RL. Prognostic factors for outcome in patients with aneurysmal subarachnoid hemorrhage. Stroke. 2007;38:2315–21.PubMedCrossRef
2.
Fujii M, Yan J, Rolland WB, Soejima Y, Caner B, Zhang JH. Early brain injury, an evolving frontier in subarachnoid hemorrhage research. Transl Stroke Res. 2013;4:432–46.PubMedCrossRef
3.
Macdonald RL. History and definition of delayed cerebral ischemia. Acta Neurochir Suppl. 2013;115:3–7.PubMed
4.
Ecker A, Riemenschneider PA. Arteriographic demonstration of spasm of the intracranial arteries, with special reference to saccular arterial aneurysms. J Neurosurg. 1951;8:660–7.PubMedCrossRef
5.
Macdonald RL, Kassell NF, Mayer S, Ruefenacht D, Schmiedek P, Weidauer S, et al. 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;39:3015–21.PubMedCrossRef
6.
Macdonald RL, Higashida RT, Keller E, Mayer SA, Molyneux A, Raabe A, et al. 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;10:618–25.PubMedCrossRef
7.
Macdonald RL, Higashida RT, Keller E, Mayer SA, Molyneux A, Raabe A, et al. Randomized trial of clazosentan in patients with aneurysmal subarachnoid hemorrhage undergoing endovascular coiling. Stroke. 2012;43:1463–9.PubMedCrossRef
8.
Herz DA, Baez S, Shulman K. Pial microcirculation in subarachnoid hemorrhage. Stroke. 1975;6:417–24.PubMedCrossRef
9.
Kniesel U, Wolburg H. Tight junctions of the blood–brain barrier. Cell Mol Neurobiol. 2000;20:57–76.PubMedCrossRef
10.
Armulik A, Genove G, Mae M, Nisancioglu MH, Wallgard E, Niaudet C, et al. Pericytes regulate the blood–brain barrier. Nature. 2010;468:557–61.PubMedCrossRef
11.
12.
Fenstermacher J, Gross P, Sposito N, Acuff V, Pettersen S, Gruber K. Structural and functional variations in capillary systems within the brain. Ann N Y Acad Sci. 1988;529:21–30.PubMedCrossRef
13.
Oldendorf WH, Cornford ME, Brown WJ. The large apparent work capability of the blood–brain barrier: a study of the mitochondrial content of capillary endothelial cells in brain and other tissues of the rat. Ann Neurol. 1977;1:409–17.PubMedCrossRef
14.
Sedlakova R, Shivers RR, Del Maestro RF. Ultrastructure of the blood–brain barrier in the rabbit. J Submicrosc Cytol Pathol. 1999;31:149–61.PubMed
15.
Hawkins BT, Davis TP. The blood–brain barrier/neurovascular unit in health and disease. Pharmacol Rev. 2005;57:173–85.PubMedCrossRef
16.
17.
Lecrux C, Hamel E. The neurovascular unit in brain function and disease. Acta Physiol (Oxf). 2011;203:47–59.CrossRef
18.
19.
Zonta M, Angulo MC, Gobbo S, Rosengarten B, Hossmann KA, Pozzan T, et al. Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat Neurosci. 2003;6:43–50.PubMedCrossRef
20.
Koide M, Bonev AD, Nelson MT, Wellman GC. Inversion of neurovascular coupling by subarachnoid blood depends on large-conductance Ca2+-activated K+ (BK) channels. Proc Natl Acad Sci U S A. 2012;109:E1387–95.PubMedCentralPubMedCrossRef
21.
Mulligan SJ, MacVicar BA. Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature. 2004;431:195–9.PubMedCrossRef
22.
Allan S. The neurovascular unit and the key role of astrocytes in the regulation of cerebral blood flow. Cerebrovasc Dis. 2006;21:137–8.PubMedCrossRef
23.
24.
Zhang JH, Badaut J, Tang J, Obenaus A, Hartman R, Pearce WJ. The vascular neural network—a new paradigm in stroke pathophysiology. Nat Rev Neurol. 2012;8:711–6.PubMedCentralPubMedCrossRef
25.
Sehba FA, Friedrich V. Early micro vascular changes after subarachnoid hemorrhage. Acta Neurochir Suppl. 2011;110:49–55.PubMed
26.
27.
Kusaka G, Ishikawa M, Nanda A, Granger DN, Zhang JH. Signaling pathways for early brain injury after subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2004;24:916–25.PubMedCrossRef
28.
Cipolla MJ (2009) “The cerebral microcirculation”. In: Granger DN, Granger J, editors. Integrated systems physiology: From molecule to function #2. San Rafael: Morgan & Claypool Life Sciences.
29.
Britz GW, Meno JR, Park IS, Abel TJ, Chowdhary A, Nguyen TS, et al. Time-dependent alterations in functional and pharmacological arteriolar reactivity after subarachnoid hemorrhage. Stroke. 2007;38:1329–35.PubMedCrossRef
30.
Wiernsperger N, Schulz U, Gygax P. Physiological and morphometric analysis of the microcirculation of the cerebral cortex under acute vasospasm. Stroke. 1981;12:624–7.PubMedCrossRef
31.
Friedrich B, Muller F, Feiler S, Scholler K, Plesnila N. Experimental subarachnoid hemorrhage causes early and long-lasting microarterial constriction and microthrombosis: an in-vivo microscopy study. J Cereb Blood Flow Metab. 2012;32:447–55.PubMedCentralPubMedCrossRef
32.
Sun BL, Zheng CB, Yang MF, Yuan H, Zhang SM, Wang LX. Dynamic alterations of cerebral pial microcirculation during experimental subarachnoid hemorrhage. Cell Mol Neurobiol. 2009;29:235–41.PubMedCrossRef
33.
Ishikawa M, Kusaka G, Yamaguchi N, Sekizuka E, Nakadate H, Minamitani H, et al. Platelet and leukocyte adhesion in the microvasculature at the cerebral surface immediately after subarachnoid hemorrhage. Neurosurgery. 2009;64:546–53.PubMedCrossRef
34.
Kajita Y, Dietrich HH, Dacey Jr RG. Effects of oxyhemoglobin on local and propagated vasodilatory responses induced by adenosine, adenosine diphosphate, and adenosine triphosphate in rat cerebral arterioles. J Neurosurg. 1996;85:908–16.PubMedCrossRef
35.
Katusic ZS, Milde JH, Cosentino F, Mitrovic BS. Subarachnoid hemorrhage and endothelial L-arginine pathway in small brain stem arteries in dogs. Stroke. 1993;24:392–9.PubMedCrossRef
36.
Park KW, Metais C, Dai HB, Comunale ME, Sellke FW. Microvascular endothelial dysfunction and its mechanism in a rat model of subarachnoid hemorrhage. Anesth Analg. 2001;92:990–6.PubMedCrossRef
37.
Park KW, Dai HB, Metais C, Comunale ME, Sellke FW. Isoflurane does not further impair microvascular vasomotion in a rat model of subarachnoid hemorrhage. Can J Anaesth. 2002;49:427–33.PubMedCrossRef
38.
Park IS, Meno JR, Witt CE, Chowdhary A, Nguyen TS, Winn HR, et al. Impairment of intracerebral arteriole dilation responses after subarachnoid hemorrhage. Laboratory investigation. J Neurosurg. 2009;111:1008–13.PubMedCrossRef
39.
Vollmer DG, Takayasu M, Dacey Jr RG. An in vitro comparative study of conducting vessels and penetrating arterioles after experimental subarachnoid hemorrhage in the rabbit. J Neurosurg. 1992;77:113–9.PubMedCrossRef
40.
Nystoriak MA, O’Connor KP, Sonkusare SK, Brayden JE, Nelson MT, Wellman GC. Fundamental increase in pressure-dependent constriction of brain parenchymal arterioles from subarachnoid hemorrhage model rats due to membrane depolarization. Am J Physiol Heart Circ Physiol. 2011;300:H803–12.PubMedCentralPubMedCrossRef
41.
Koide M, Bonev AD, Nelson MT, Wellman GC. Subarachnoid blood converts neurally evoked vasodilation to vasoconstriction in rat brain cortex. Acta Neurochir Suppl. 2013;115:167–71.PubMedCentralPubMed
42.
Ohkuma H, Manabe H, Tanaka M, Suzuki S. Impact of cerebral microcirculatory changes on cerebral blood flow during cerebral vasospasm after aneurysmal subarachnoid hemorrhage. Stroke. 2000;31:1621–7.PubMedCrossRef
43.
del Zoppo GJ, von Kummer R, Hamann GF. Ischaemic damage of brain microvessels: inherent risks for thrombolytic treatment in stroke. J Neurol Neurosurg Psychiatry. 1998;65:1–9.PubMedCrossRef
44.
Tso MK, Macdonald RL. Acute microvascular changes after subarachnoid hemorrhage and transient global cerebral ischemia. Stroke Res Treat. 2013;2013:425281.PubMedCentralPubMed
45.
Titova E, Ostrowski RP, Zhang JH, Tang J. Experimental models of subarachnoid hemorrhage for studies of cerebral vasospasm. Neurol Res. 2009;31:568–81.PubMedCrossRef
46.
Koide M, Wellman GC. SAH-induced suppression of voltage-gated K(+) (K (V)) channel currents in parenchymal arteriolar myocytes involves activation of the HB-EGF/EGFR pathway. Acta Neurochir Suppl. 2013;115:179–84.PubMedCentralPubMed
47.
Cach R, Smock T, Popejoy S. Blood-borne factors regulating microvascular constriction in the rat hippocampal slice. Brain Res. 1987;414:1–7.PubMedCrossRef
48.
Zubkov AY, Tibbs RE, Aoki K, Zhang JH. Prevention of vasospasm in penetrating arteries with MAPK inhibitors in dog double-hemorrhage model. Surg Neurol. 2000;54:221–7.PubMedCrossRef
49.
Ohkuma H, Itoh K, Shibata S, Suzuki S. Morphological changes of intraparenchymal arterioles after experimental subarachnoid hemorrhage in dogs. Neurosurgery. 1997;41:230–5.PubMedCrossRef
50.
Asano T, Sano K. Pathogenetic role of no-reflow phenomenon in experimental subarachnoid hemorrhage in dogs. J Neurosurg. 1977;46:454–66.PubMedCrossRef
51.
Ohkuma H, Suzuki S. Histological dissociation between intra- and extraparenchymal portion of perforating small arteries after experimental subarachnoid hemorrhage in dogs. Acta Neuropathol. 1999;98:374–82.PubMedCrossRef
52.
Ohkuma H, Suzuki S, Ogane K. Phenotypic modulation of smooth muscle cells and vascular remodeling in intraparenchymal small cerebral arteries after canine experimental subarachnoid hemorrhage. Neurosci Lett. 2003;344:193–6.PubMedCrossRef
53.
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.PubMedCrossRef
54.
Johshita H, Kassell NF, Sasaki T, Ogawa H. Impaired capillary perfusion and brain edema following experimental subarachnoid hemorrhage: a morphometric study. J Neurosurg. 1990;73:410–7.PubMedCrossRef
55.
Sehba FA, Friedrich Jr V, Makonnen G, Bederson JB. Acute cerebral vascular injury after subarachnoid hemorrhage and its prevention by administration of a nitric oxide donor. J Neurosurg. 2007;106:321–9.PubMedCrossRef
56.
Friedrich V, Flores R, Muller A, Sehba FA. Luminal platelet aggregates in functional deficits in parenchymal vessels after subarachnoid hemorrhage. Brain Res. 2010;1354:179–87.PubMedCrossRef
57.
Uhl E, Lehmberg J, Steiger HJ, Messmer K. Intraoperative detection of early microvasospasm in patients with subarachnoid hemorrhage by using orthogonal polarization spectral imaging. Neurosurgery. 2003;52:1307–15.PubMedCrossRef
58.
Dorhout Mees SM, Rinkel GJ, Feigin VL, Algra A, van den Bergh WM, Vermeulen M, & van Gijn J (2007) Calcium antagonists for aneurysmal subarachnoid haemorrhage. Cochrane Database Syst Rev. CD000277.
59.
Meyer R, Deem S, Yanez ND, Souter M, Lam A, Treggiari MM. Current practices of triple-H prophylaxis and therapy in patients with subarachnoid hemorrhage. Neurocrit Care. 2010;14:24–36.CrossRef
60.
Ostergaard L, Aamand R, Karabegovic S, Tietze A, Blicher JU, Mikkelsen IK, et al. The role of the microcirculation in delayed cerebral ischemia and chronic degenerative changes after subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2013;33:1825–37.PubMedCentralPubMedCrossRef
61.
Yemisci M, Gursoy-Ozdemir Y, Vural A, Can A, Topalkara K, Dalkara T. Pericyte contraction induced by oxidative–nitrative stress impairs capillary reflow despite successful opening of an occluded cerebral artery. Nat Med. 2009;15:1031–7.PubMedCrossRef
62.
Nihei H, Kassell NF, Dougherty DA, Sasaki T. Does vasospasm occur in small pial arteries and arterioles of rabbits? Stroke. 1991;22:1419–25.PubMedCrossRef
63.
Perkins E, Kimura H, Parent AD, Zhang JH. Evaluation of the microvasculature and cerebral ischemia after experimental subarachnoid hemorrhage in dogs. J Neurosurg. 2002;97:896–904.PubMedCrossRef
64.
Josko J. Cerebral angiogenesis and expression of VEGF after subarachnoid hemorrhage (SAH) in rats. Brain Res. 2003;981:58–69.PubMedCrossRef
65.
Zhou N, Xu T, Bai Y, Prativa S, Xu JZ, Li K, et al. Protective effects of urinary trypsin inhibitor on vascular permeability following subarachnoid hemorrhage in a rat model. CNS Neurosci Ther. 2013;19:659–66.PubMedCrossRef
66.
Ansar S, Edvinsson L. Subtype activation and interaction of protein kinase C and mitogen-activated protein kinase controlling receptor expression in cerebral arteries and microvessels after subarachnoid hemorrhage. Stroke. 2008;39:185–90.PubMedCrossRef
67.
Friedrich V, Flores R, Muller A, Bi W, Peerschke EI, Sehba FA. Reduction of neutrophil activity decreases early microvascular injury after subarachnoid haemorrhage. J Neuroinflammation. 2011;8:103.PubMedCentralPubMedCrossRef
68.
Moore KL. Structure and function of P-selectin glycoprotein ligand-1. Leuk Lymphoma. 1998;29:1–15.PubMedCrossRef
69.
Yatsushige H, Ostrowski RP, Tsubokawa T, Colohan A, Zhang JH. Role of c-Jun N-terminal kinase in early brain injury after subarachnoid hemorrhage. J Neurosci Res. 2007;85:1436–48.PubMedCrossRef
70.
Erdo F, Erdo SL. Bimoclomol protects against vascular consequences of experimental subarachnoid hemorrhage in rats. Brain Res Bull. 1998;45:163–6.PubMedCrossRef
71.
Germano A, Costa C, DeFord SM, Angileri FF, Arcadi F, Pike BR, et al. Systemic administration of a calpain inhibitor reduces behavioral deficits and blood–brain barrier permeability changes after experimental subarachnoid hemorrhage in the rat. J Neurotrauma. 2002;19:887–96.PubMedCrossRef
72.
Germano A, Caffo M, Angileri FF, Arcadi F, Newcomb-Fernandez J, Caruso G, et al. NMDA receptor antagonist felbamate reduces behavioral deficits and blood–brain barrier permeability changes after experimental subarachnoid hemorrhage in the rat. J Neurotrauma. 2007;24:732–44.PubMedCrossRef
73.
Imperatore C, Germano A, d’Avella D, Tomasello F, Costa G. Effects of the radical scavenger AVS on behavioral and BBB changes after experimental subarachnoid hemorrhage. Life Sci. 2000;66:779–90.PubMedCrossRef
74.
Suzuki H, Ayer R, Sugawara T, Chen W, Sozen T, Hasegawa Y, et al. Protective effects of recombinant osteopontin on early brain injury after subarachnoid hemorrhage in rats. Crit Care Med. 2010;38:612–8.PubMedCentralPubMedCrossRef
75.
Yan J, Manaenko A, Chen S, Klebe D, Ma Q, Caner B, et al. Role of SCH79797 in maintaining vascular integrity in rat model of subarachnoid hemorrhage. Stroke. 2013;44:1410–7.PubMedCrossRef
76.
Doczi T, Joo F, Adam G, Bozoky B, Szerdahelyi P. Blood–brain barrier damage during the acute stage of subarachnoid hemorrhage, as exemplified by a new animal model. Neurosurgery. 1986;18:733–9.PubMedCrossRef
77.
Doczi T, Joo F, Sonkodi S, Adam G. Increased vulnerability of the blood–brain barrier to experimental subarachnoid hemorrhage in spontaneously hypertensive rats. Stroke. 1986;17:498–501.PubMedCrossRef
78.
Germano 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;142:575–80.CrossRef
79.
Wang Z, Zuo G, Shi XY, Zhang J, Fang Q, Chen G. Progesterone administration modulates cortical TLR4/NF-kappaB signaling pathway after subarachnoid hemorrhage in male rats. Mediators Inflamm. 2011;2011:848309.PubMedCentralPubMedCrossRef
80.
Smith SL, Scherch HM, Hall ED. Protective effects of tirilazad mesylate and metabolite U-89678 against blood–brain barrier damage after subarachnoid hemorrhage and lipid peroxidative neuronal injury. J Neurosurg. 1996;84:229–33.PubMedCrossRef
81.
Yatsushige H, Calvert JW, Cahill J, Zhang JH. Limited role of inducible nitric oxide synthase in blood–brain barrier function after experimental subarachnoid hemorrhage. J Neurotrauma. 2006;23:1874–82.PubMedCrossRef
82.
Scholler K, Trinkl A, Klopotowski M, Thal SC, Plesnila N, Trabold R, et al. Characterization of microvascular basal lamina damage and blood–brain barrier dysfunction following subarachnoid hemorrhage in rats. Brain Res. 2007;1142:237–46.PubMedCrossRef
83.
Yan J, Chen C, Hu Q, Yang X, Lei J, Yang L, et al. The role of p53 in brain edema after 24 h of experimental subarachnoid hemorrhage in a rat model. Exp Neurol. 2008;214:37–46.PubMedCrossRef
84.
Yan J, Li L, Khatibi NH, Yang L, Wang K, Zhang W, et al. Blood–brain barrier disruption following subarachnoid hemorrhage may be facilitated through PUMA induction of endothelial cell apoptosis from the endoplasmic reticulum. Exp Neurol. 2011;230:240–7.PubMedCrossRef
85.
Gules I, Satoh M, Nanda A, Zhang JH. Apoptosis, blood–brain barrier, and subarachnoid hemorrhage. Acta Neurochir Suppl. 2003;86:483–7.PubMed
86.
Friedrich V, Flores R, Muller A, Sehba FA. Escape of intraluminal platelets into brain parenchyma after subarachnoid hemorrhage. Neuroscience. 2010;165:968–75.PubMedCentralPubMedCrossRef
87.
Sehba FA, Friedrich V. Cerebral microvasculature is an early target of subarachnoid hemorrhage. Acta Neurochir Suppl. 2013;115:199–205.PubMed
88.
Sehba FA, Mostafa G, Knopman J, Friedrich Jr V, Bederson JB. Acute alterations in microvascular basal lamina after subarachnoid hemorrhage. J Neurosurg. 2004;101:633–40.PubMedCrossRef
89.
Sehba FA, Flores R, Muller A, Friedrich V, Chen JF, Britz GW, et al. Adenosine A(2A) receptors in early ischemic vascular injury after subarachnoid hemorrhage. Laboratory investigation. J Neurosurg. 2010;113:826–34.PubMedCentralPubMedCrossRef
90.
91.
Prunell GF, Svendgaard NA, Alkass K, Mathiesen T. Delayed cell death related to acute cerebral blood flow changes following subarachnoid hemorrhage in the rat brain. J Neurosurg. 2005;102:1046–54.PubMedCrossRef
92.
Peterson EW, Cardoso ER. The blood–brain barrier following experimental subarachnoid hemorrhage. Part 1: Response to insult caused by arterial hypertension. J Neurosurg. 1983;58:338–44.PubMedCrossRef
93.
Park S, Yamaguchi M, Zhou C, Calvert JW, Tang J, Zhang JH. Neurovascular protection reduces early brain injury after subarachnoid hemorrhage. Stroke. 2004;35:2412–7.PubMedCrossRef
94.
Claassen J, Carhuapoma JR, Kreiter KT, Du EY, Connolly ES, Mayer SA. Global cerebral edema after subarachnoid hemorrhage: frequency, predictors, and impact on outcome. Stroke. 2002;33:1225–32.PubMedCrossRef
95.
Zhang S, Wang L, Liu M, Wu B. Tirilazad for aneurysmal subarachnoid haemorrhage. Cochrane Database Syst Rev. 2010. CD006778.
96.
Stein SC, Browne KD, Chen XH, Smith DH, Graham DI. Thromboembolism and delayed cerebral ischemia after subarachnoid hemorrhage: an autopsy study. Neurosurgery. 2006;59:781–7.PubMedCrossRef
97.
Sehba FA, Mostafa G, Friedrich Jr V, Bederson JB. Acute microvascular platelet aggregation after subarachnoid hemorrhage. J Neurosurg. 2005;102:1094–100.PubMedCrossRef
98.
Sabri M, Ai J, Lass E, D’abbondanza J, Macdonald RL. Genetic elimination of eNOS reduces secondary complications of experimental subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2013;33:1008–14.PubMedCrossRef
99.
Pisapia JM, Xu X, Kelly J, Yeung J, Carrion G, Tong H, et al. Microthrombosis after experimental subarachnoid hemorrhage: time course and effect of red blood cell-bound thrombin-activated pro-urokinase and clazosentan. Exp Neurol. 2012;233:357–63.PubMedCrossRef
100.
Ramakrishna R, Sekhar LN, Ramanathan D, Temkin N, Hallam D, Ghodke BV, et al. Intraventricular tissue plasminogen activator for the prevention of vasospasm and hydrocephalus after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2010;67:110–7.PubMedCrossRef
101.
van den Bergh WM, Algra A, Dorhout Mees SM, van Kooten F, Dirven CM, van Gijn J, et al. Randomized controlled trial of acetylsalicylic acid in aneurysmal subarachnoid hemorrhage: the MASH Study. Stroke. 2006;37:2326–30.PubMedCrossRef
102.
Dreier JP. The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat Med. 2011;17:439–47.PubMedCrossRef
103.
Nicoletti C, Offenhauser N, Jorks D, Major S, Dreier JP “Assessment of neurovascular coupling”. In: Chen J, Xu X-M, Xu ZC, Zhang JH, editors. Animal models of acute neurological injuries II: Injuries and mechanistic assessments. Springer Protocols Handbooks. Totowa, NJ: Humana; 2012. Volume I. pp. 353–72
Metadata
Title
Subarachnoid Hemorrhage: a Review of Experimental Studies on the Microcirculation and the Neurovascular Unit
Authors
Michael K. Tso
R. Loch Macdonald
Publication date
01-04-2014
Publisher
Springer US
Published in
Translational Stroke Research / Issue 2/2014
Print ISSN: 1868-4483
Electronic ISSN: 1868-601X
DOI
https://doi.org/10.1007/s12975-014-0323-4

Other articles of this Issue 2/2014

Translational Stroke Research 2/2014 Go to the issue

Original Article

Endovascular Management of Cerebral Aneurysm

Original Article

Intracisternal Administration of Tissue Plasminogen Activator Improves Cerebrospinal Fluid Flow and Cortical Perfusion After Subarachnoid Hemorrhage in Mice

Original Article

Tenascin-C Causes Neuronal Apoptosis After Subarachnoid Hemorrhage in Rats

Original Article

Translational Research Using a Mouse Model of Intracranial Aneurysm

Original Article

Cerebral Lactate Correlates with Early Onset Pneumonia after Aneurysmal SAH

Original Article

Effects of Androgens on Early Post-ischemic Neurogenesis in Mice