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Early Brain Injury or Cerebral Vasospasm pp 49–55Cite as

Early Micro Vascular Changes After Subarachnoid Hemorrhage

  • Conference paper

Part of the book series: Acta Neurochirurgica Supplements ((NEUROCHIRURGICA,volume 110/1))

Abstract

During the last decade much effort has been invested in understanding the events that occur early after SAH. It is now widely accepted that these early events not only participate in the early ischemic injury but also set the stage for the pathogenesis of delayed vasospasm. That early cerebral ischemia occurs after SAH is documented in both experimental SAH and in human autopsy studies; however, angiographic evidence for vasoconstriction early after SAH is lacking and the source of early ischemic injury is therefore unclear. Recently, the cerebral microvasculature has been identified as an early target of SAH. Changes in the anatomical structure of cerebral microvessels, sufficient to cause functional deficits, are found early after experimental SAH. These changes may explain cerebral ischemia in human in the absence of angiographic evidence of large vessel vasoconstriction. This paper summarizes known alterations in cerebral microvasculature during the first 48h after SAH.

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References

  1. Jakobsen M. Role of initial brain ischemia in subarachnoid hemorrhage following aneurysm rupture. A pathophysiological survey. Acta Neurol Scand. 1992;141:1–33.

    Article  CAS  Google Scholar 

  2. Bederson JB, Germano IM, Guarino L. Cortical blood flow and cerebral perfusion pressure in a new noncraniotomy model of subarachnoid hemorrhage in the rat. Stroke 1995;26:1086–91.

    Article  PubMed  CAS  Google Scholar 

  3. Bederson JB, Levy AL, Ding WH, Kahn R, DiPerna CA, Jenkins ALr et al. Acute vasoconstriction after subarachnoid hemorrhage. Neurosurgery 1998;42:352–60.

    Article  PubMed  CAS  Google Scholar 

  4. Kamiya K, Kuyama H, Symon L. An experimental study of the acute stage of subarachnoid hemorrhage. J Neurosurg. 1983;59:917–24.

    Article  PubMed  CAS  Google Scholar 

  5. Rasmussen G, Hauerberg J, Waldemar G, Gjerris F, Juhler M. Cerebral blood flow autoregulation in experimental subarachnoid haemorrhage in rat. Acta Neurochir. 1992;119:128–33.

    Article  PubMed  CAS  Google Scholar 

  6. Travis MA, Hall ED. The effects of chronic two-fold dietary vitamin E supplementation on subarachnoid hemorrhage-induced brain hypoperfusion. Brain Res. 1987;418:366–70.

    Article  PubMed  CAS  Google Scholar 

  7. Sehba FA, Ding WH, Chereshnev I, Bederson JB. Effects of S-nitrosoglutathione on acute vasoconstriction and glutamate release after subarachnoid hemorrhage. Stroke 1999;30:1955–61.

    Article  PubMed  CAS  Google Scholar 

  8. Hutchinson PJ, O’Connell MT, Al-Rawi PG, Kett-White CR, Gupta AK, Maskell LBet al. Increases in GABA concentrations during cerebral ischaemia: a microdialysis study of extracellular amino acids. J Neurol Neurosurg Psychiatry. 2002;72:99–105.

    Article  PubMed  CAS  Google Scholar 

  9. Sarrafzadeh A, Haux D, Sakowitz O, Benndorf G, Herzog H, Kuechler I, et al. Acute focal neurological deficits in aneurysmal subarachnoid hemorrhage: relation of clinical course, CT findings, and metabolite abnormalities monitored with bedside microdialysis. Stroke 2003;34:1382–8.

    Article  PubMed  CAS  Google Scholar 

  10. Staub F, Graf R, Gabel P, Kochling M, Klug N, Heiss WD. Multiple interstitial substances measured by microdialysis in patients with subarachnoid hemorrhage. Neurosurgery 2000;47:1106–15; discussion 1115–1106.

    Article  PubMed  CAS  Google Scholar 

  11. Grosset DG, Straiton J, McDonald I, Bullock R. Angiographic and Doppler diagnosis of cerebral artery vasospasm following subarachnoid haemorrhage. Br J Neurosurg. 1993;7:291–8.

    Article  PubMed  CAS  Google Scholar 

  12. Weir B, Grace M, Hansen J, Rothberg C. Time course of vasospasm in man. J Neurosurg. 1978;48:173–8.

    Article  PubMed  CAS  Google Scholar 

  13. Hoelper BM, Hofmann E, Sporleder R, Soldner F, Behr R. Transluminal balloon angioplasty improves brain tissue oxygenation and metabolism in severe vasospasm after aneurysmal subarachnoid hemorrhage: case report. Neurosurgery 2003;52:970–4; discussion 974–976.

    Article  PubMed  Google Scholar 

  14. Ono S, Date I, Onoda K, Ohmoto T. Time course of the diameter of the major cerebral arteries after subarachnoid hemorrhage using corrosion cast technique. Neurol Res. 2003;25:383–9.

    Article  PubMed  Google Scholar 

  15. 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; discussion 1315–1307.

    Article  PubMed  Google Scholar 

  16. 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; discussion 553–554.

    Article  PubMed  Google Scholar 

  17. 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.

    Article  PubMed  CAS  Google Scholar 

  18. Sehba FA, Makonnen G, Friedrich V, Bederson JB. Acute cerebral vascular injury occurs after subarachnoid hemorrhage and can be prevented by administration of a Nitric Oxide donor. J Neurosurg. 2007;106:321–9.

    Article  PubMed  CAS  Google Scholar 

  19. Sehba FA, Mostafa G, Knopman J, Friedrich V Jr, Bederson JB. Acute alterations in Microvascular basal lamina after Subarachnoid Hemorrhage. J Neurosurg. 2004;101:633–40.

    Article  PubMed  Google Scholar 

  20. Sehba FA, Mustafa G, Friedrich V, Bederson JB. Acute microvascular platelet aggregation after Subarachnoid hemorrhage. J Neurosurg. 2005;102:1094–100.

    Article  PubMed  Google Scholar 

  21. 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.

    Article  PubMed  Google Scholar 

  22. Critchley GR, Bell BA. Acute cerebral tissue oxygenation changes following experimental subarachnoid hemorrhage. Neurol Res. 2003;25:451–6.

    Article  PubMed  Google Scholar 

  23. Pennings FA, Albrecht KW, Muizelaar JP, Schuurman PR, Bouma GJ. Abnormal responses of the human cerebral microcirculation to papaverin during aneurysm surgery. Stroke 2009;40:317–20.

    Article  PubMed  CAS  Google Scholar 

  24. Gregoire N. The blood-brain barrier. J Neuroradiol. 1989;16:238–50.

    PubMed  CAS  Google Scholar 

  25. Martinez-Hernandez A, Amenta PS. The basement membrane in pathology. Lab Invest. 1983;48:656–77.

    PubMed  CAS  Google Scholar 

  26. Bosman FT, Cleutjens J, Beek C, Havenith M. Basement membrane heterogeneity. Histochem J. 1989;21:629–33.

    Article  PubMed  CAS  Google Scholar 

  27. Stanley JR, Woodley DT, Katz SI, Martin GR. Structure and function of basement membrane. J Invest Dermatol. 1982;79:Suppl 1:69s–72s.

    Article  PubMed  Google Scholar 

  28. Hamann GF, Liebetrau M, Martens H, Burggraf D, Kloss CU, Bultemeier Get al. Microvascular Basal lamina injury after experimental focal cerebral ischemia and reperfusion in the rat. J Cereb Blood Flow Metab. 2002;22:526–33.

    Article  PubMed  Google Scholar 

  29. Heo JH, Lucero J, Abumiya T, Koziol JA, Copeland BR, del Zoppo GJ. Matrix metalloproteinases increase very early during experimental focal cerebral ischemia. J Cereb Blood Flow Metab. 1999;19:624–33.

    Article  PubMed  CAS  Google Scholar 

  30. Wagner S, Tagaya M, Koziol JA, Quaranta V, del Zoppo GJ. Rapid disruption of an astrocyte interaction with the extracellular matrix mediated by integrin alpha 6 beta 4 during focal cerebral ischemia/reperfusion. Stroke 1997;28:858–65.

    Article  PubMed  CAS  Google Scholar 

  31. del Zoppo GJ, Mabuchi T. Cerebral microvessel responses to focal ischemia. J Cereb Blood Flow Metab. 2003;23:879–94.

    Article  PubMed  Google Scholar 

  32. Hatake K, Wakabayashi I, Kakishita E, Hishida S. Impairment of endothelium-dependent relaxation in human basilar artery after subarachnoid hemorrhage. Stroke 1992;23:1111–6; discussion 1116–1117.

    Article  PubMed  CAS  Google Scholar 

  33. Hongo K, Kassell NF, Nakagomi T, Sasaki T, Tsukahara T, Ogawa Het al. Subarachnoid hemorrhage inhibition of endothelium-derived relaxing factor in rabbit basilar artery. J Neurosurg. 1988;69:247–53.

    Article  PubMed  CAS  Google Scholar 

  34. Nakagomi T, Kassell NF, Sasaki T, Fujiwara S, Lehman RM, Johshita H et al. Effect of subarachnoid hemorrhage on endothelium-dependent vasodilation. J Neurosurg. 1987;66:915–23.

    Article  PubMed  CAS  Google Scholar 

  35. Pennings FA, Bouma GJ, Ince C. Direct observation of the human cerebral microcirculation during aneurysm surgery reveals increased arteriolar contractility. Stroke 2004;35:1284–8.

    Article  PubMed  Google Scholar 

  36. Sehba FA, Schwartz AY, Chereshnev I, Bederson JB. Acute decrease in cerebral nitric oxide levels after subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2000;20:604–11.

    Article  PubMed  CAS  Google Scholar 

  37. Gryglewski RJ, Palmer RM, Moncada S. Superoxide anion is involved in the breakdown of endothelium-derived vascular relaxing factor. Nature 1986;320:454–6.

    Article  PubMed  CAS  Google Scholar 

  38. Pabst MJ, Cummings NP, Hedegaard HB, Johnston RB Jr. Human macrophages may normally be “primed” for a strong oxygen radical response. Adv Exp Med Biol. 1983;166:215–21.

    Article  PubMed  CAS  Google Scholar 

  39. Clower BR, Yamamoto Y, Cain L, Haines DE, Smith RR. Endothelial injury following experimental subarachnoid hemorrhage in rats: effects on brain blood flow. Anat Rec. 1994;240:104–14.

    Article  PubMed  CAS  Google Scholar 

  40. 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.

    Article  PubMed  CAS  Google Scholar 

  41. Akopov S, Sercombe R, Seylaz J. Cerebrovascular reactivity: role of endothelium/platelet/leukocyte interactions. Cerebrovasc Brain Metab Rev. 1996;8:11–94.

    PubMed  CAS  Google Scholar 

  42. Cahill J, Calvert JW, Solaroglu I, Zhang JH. Vasospasm and p53-induced apoptosis in an experimental model of subarachnoid hemorrhage. Stroke 2006;37:1868–74.

    Article  PubMed  Google Scholar 

  43. Joris I, Majno G. Endothelial changes induced by arterial spasm. Am J Pathol. 1981;102:346–58.

    PubMed  CAS  Google Scholar 

  44. Simard JM, Geng Z, Woo SK, Ivanova S, Tosun C, Melnichenko L et al. Glibenclamide reduces inflammation, vasogenic edema, and caspase-3 activation after subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2009;29:317–30.

    Article  PubMed  CAS  Google Scholar 

  45. Chaichana[AU3] KL, Pradilla G, Huang J, Tamargo RJ. Role of inflammation (leukocyte-endothelial cell interactions) in vasospasm after subarachnoid hemorrhage. World Neurosurg. 2010;73(1):22–41.

    Article  PubMed  Google Scholar 

  46. Bavbek M, Polin R, Kwan AL, Arthur AS, Kassell NF, Lee KS. Monoclonal antibodies against ICAM-1 and CD18 attenuate cerebral vasospasm after experimental subarachnoid hemorrhage in rabbits. Stroke 1998;29:1930–5; discussion 1935–1936.

    Article  PubMed  CAS  Google Scholar 

  47. Handa Y, Kubota T, Kaneko M, Tsuchida A, Kobayashi H, Kawano H. Expression of intercellular adhesion molecule 1 (ICAM-1) on the cerebral artery following subarachnoid haemorrhage in rats. Acta Neurochir (Wien). 1995;132:92–7.

    Article  CAS  Google Scholar 

  48. Polin RS, Bavbek M, Shaffrey ME, Billups K, Bogaev CA, Kassell NF et al. Detection of soluble E-selectin, ICAM-1, VCAM-1, and L-selectin in the cerebrospinal fluid of patients after subarachnoid hemorrhage. J Neurosurg. 1998;89:559–67.

    Article  PubMed  CAS  Google Scholar 

  49. Rothoerl RD, Schebesch KM, Kubitza M, Woertgen C, Brawanski A, Pina AL. ICAM-1 and VCAM-1 expression following aneurysmal subarachnoid hemorrhage and their possible role in the pathophysiology of subsequent ischemic deficits. Cerebrovasc Dis. 2006;22:143–9.

    Article  PubMed  CAS  Google Scholar 

  50. 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;64:201–5.

    Article  PubMed  Google Scholar 

  51. Rosenblum WI. Platelet adhesion and aggregation without endothelial denudation or exposure of basal lamina and/or collagen. J Vasc Res. 1997;34:409–17.

    Article  PubMed  CAS  Google Scholar 

  52. Said S, Rosenblum WI, Povlishock JT, Nelson GH. Correlations between morphological changes in platelet aggregates and underlying endothelial damage in cerebral microcirculation of mice. Stroke 1993;24:1968–76.

    Article  PubMed  CAS  Google Scholar 

  53. Akopov SE, Sercombe R, Seylaz J. Leukocyte-induced endothelial dysfunction in the rabbit basilar artery: modulation by platelet-activating factor. J Lipid Mediat Cell Signal. 1995;11:267–79.

    Article  PubMed  CAS  Google Scholar 

  54. 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.

    Article  PubMed  CAS  Google Scholar 

  55. 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.

    Article  PubMed  CAS  Google Scholar 

  56. Hamann GF, Okada Y, Fitridge R, del Zoppo GJ. Microvascular basal lamina antigens disappear during cerebral ischemia and reperfusion. Stroke 1995;26:2120–6.

    Article  PubMed  CAS  Google Scholar 

  57. Gasche Y, Fujimura M, Morita-Fujimura Y, Copin JC, Kawase M, Massengale J et al. Early appearance of activated matrix metalloproteinase-9 after focal cerebral ischemia in mice: a possible role in blood-brain barrier dysfunction. J Cereb Blood Flow Metab. 1999;19:1020–8.

    Article  PubMed  CAS  Google Scholar 

  58. Mun-Bryce S, Rosenberg GA. Matrix metalloproteinases in cerebrovascular disease. J Cereb Blood Flow Metab. 1998;18:1163–72.

    Article  PubMed  CAS  Google Scholar 

  59. Zhang ZG, Zhang L, Tsang W, Goussev A, Powers C, Ho K et al. Dynamic platelet accumulation at the site of the occluded middle cerebral artery and in downstream microvessels is associated with loss of microvascular integrity after embolic middle cerebral artery occlusion. Brain Res. 2001;912:181–94.

    Article  PubMed  CAS  Google Scholar 

  60. Mignatti P, Rifkin DB. Plasminogen activators and matrix metalloproteinases in angiogenesis. Enzyme Protein. 1996;49:117–37.

    PubMed  CAS  Google Scholar 

  61. Rosenberg GA. Matrix metalloproteinases in brain injury. J Neurotrauma. 1995;12:833–42.

    Article  PubMed  CAS  Google Scholar 

  62. Clark AW, Krekoski CA, Bou SS, Chapman KR, Edwards DR. Increased gelatinase A (MMP-2) and gelatinase B (MMP-9) activities in human brain after focal ischemia. Neurosci Lett. 1997;238:53–6.

    Article  PubMed  CAS  Google Scholar 

  63. Lukes A, Mun-Bryce S, Lukes M, Rosenberg GA. Extracellular matrix degradation by metalloproteinases and central nervous system diseases. Mol Neurobiol. 1999;19:267–84.

    Article  PubMed  CAS  Google Scholar 

  64. Guo Z, Sun X, He Z, Jiang Y, Zhang X, Zhang JH. Matrix metalloproteinase-9 potentiates early brain injury after subarach-noid hemorrhage. Neurol Res. 2010 Sep;32(7):715–20.

    Google Scholar 

  65. 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.

    Article  PubMed  CAS  Google Scholar 

  66. Josko J, Hendryk S, Jedrzejowska-Szypulka H, Slowinski J, Gwozdz B, Lange D et al. Cerebral angiogenesis after subarachnoid hemorrhage (SAH) and endothelin receptor blockage with BQ-123 antagonist in rats. J Physiol Pharmacol. 2001;52:237–48.

    PubMed  CAS  Google Scholar 

  67. Josko J. Cerebral angiogenesis and expression of VEGF after subarachnoid hemorrhage (SAH) in rats. Brain Res. 2003;981:58–69.

    Article  PubMed  CAS  Google Scholar 

  68. Josko J, Gwozdz B, Hendryk S, Jedrzejowska-Szypulka H, Slowinski J, Jochem J. Expression of vascular endothelial growth factor (VEGF) in rat brain after subarachnoid haemorrhage and endothelin receptor blockage with BQ-123. Folia Neuropathol. 2001;39:243–51.

    PubMed  CAS  Google Scholar 

  69. Scheufler KM, Drevs J, van Velthoven V, Reusch P, Klisch J, Augustin HG et al. Implications of vascular endothelial growth factor, sFlt-1, and sTie-2 in plasma, serum and cerebrospinal fluid during cerebral ischemia in man. J Cereb Blood Flow Metab. 2003;23:99–110.

    Article  PubMed  CAS  Google Scholar 

  70. McGirt MJ, Lynch JR, Blessing R, Warner DS, Friedman AH, Laskowitz DT. Serum von Willebrand factor, matrix metallopro-teinase-9, and vascular endothelial growth factor levels predict the onset of cerebral vasospasm after aneurysmal subarachnoid hemorrhage. Neurosurgery 2002;51:1128–34; discussion 1134–1135.

    Article  PubMed  Google Scholar 

  71. Sun BL, Hu DM, Yuan H, Ye WJ, Wang XC, Xia ZL et al. Extract of Ginkgo biloba promotes the expression of VEGF following subarachnoid hemorrhage in rats. Int J Neurosci. 2009;119:995–1005.

    Article  PubMed  CAS  Google Scholar 

  72. Sawicki G, Salas E, Murat J, Miszta-Lane H, Radomski MW. Release of gelatinase A during platelet activation mediates aggregation. Nature 1997;386:616–9.

    Article  PubMed  CAS  Google Scholar 

  73. 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.

    Article  PubMed  CAS  Google Scholar 

  74. Smith SL, Larson PG, Hall ED. A comparison of the effects of tirilazad on subarachnoid hemorrhage-induced blood-brain barrier permeability in male and female rats. J Stroke Cerebrovasc Dis. 1997;6:389–93.

    Article  PubMed  CAS  Google Scholar 

  75. 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.

    Article  PubMed  Google Scholar 

  76. Antovic J, Bakic M, Zivkovic M, Ilic A, Blomback M. Blood coagulation and fibrinolysis in acute ischaemic and haemorrhagic (intracerebral and subarachnoid haemorrhage) stroke: does decreased plasmin inhibitor indicate increased fibrinolysis in subarachnoid haemorrhage compared to other types of stroke? Scand J Clin Lab Invest. 2002;62:195–9.

    Article  PubMed  CAS  Google Scholar 

  77. Ettinger MG. Coagulation abnormalities in subarachnoid hemorrhage. Stroke 1970;1:139–42.

    Article  PubMed  CAS  Google Scholar 

  78. Filizzolo F, D’Angelo V, Collice M, Ferrara M, Donati MB, Porta M. Fibrinolytic activity in blood and cerebrospinal fluid in subarachnoid hemorrhage from ruptured intracranial saccular aneurysm before and during EACA treatment. Eur Neurol. 1978;17:43–7.

    Article  PubMed  CAS  Google Scholar 

  79. Nina P, Schisano G, Chiappetta F, Luisa Papa M, Maddaloni E, Brunori A et al. A study of blood coagulation and fibrinolytic system in spontaneous subarachnoid hemorrhage. Correlation with hunt-hess grade and outcome. Surg Neurol. 2001;55:197–203.

    Article  PubMed  CAS  Google Scholar 

  80. Denton IC, Robertson JT, Dugdale M. An assessment of early platelet activity in experimental subarachnoid hemorrhage and middle cerebral artery thrombosis in the cat. Stroke 1971;2:268–72.

    Article  PubMed  CAS  Google Scholar 

  81. Clower BR, Yoshioka J, Honma Y, Smith RR. Pathological changes in cerebral arteries following experimental subarachnoid hemorrhage: role of blood platelets. Anat Rec. 1988;220:161–70.

    Article  PubMed  CAS  Google Scholar 

  82. Haining JL, Clower BR, Honma Y, Smith RR. Accumulation of intimal platelets in cerebral arteries following experimental subarachnoid hemorrhage in cats. Stroke 1988;19:898–902.

    Article  PubMed  CAS  Google Scholar 

  83. 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; discussion 787–788.

    Article  PubMed  Google Scholar 

  84. Akopov SE, Zhang L, Pearce WJ. Mechanisms of platelet-induced angiospastic reactions: potentiation of calcium sensitivity. Can J Physiol Pharmacol. 1997;75:849–52.

    Article  PubMed  CAS  Google Scholar 

  85. Fujimoto T, Suzuki H, Tanoue K, Fukushima Y, Yamazaki H. Autoradiographic observation of platelets in cerebrovascular injuries induced by arachidonic acid and its prevention by ticlopidine. Thromb Haemost. 1988;60:319–23.

    PubMed  CAS  Google Scholar 

  86. Umegaki K, Inoue Y, Tomita T. The appearance of platelets at the time of stroke in stroke-prone spontaneously hypertensive rats. Thromb Haemost. 1985;54:764–7.

    PubMed  CAS  Google Scholar 

  87. Kapp J, Mahaley MS Jr, Odom GL. Cerebral arterial spasm. 2. Experimental evaluation of mechanical and humoral factors in pathogenesis. J Neurosurg. 1968;29:339–49.

    Article  PubMed  CAS  Google Scholar 

  88. Fujimoto T, Suzuki H, Tanoue K, Fukushima Y, Yamazaki H. Cerebrovascular injuries induced by activation of platelets in vivo. Stroke 1985;16:245–50.

    Article  PubMed  CAS  Google Scholar 

  89. Andresen J, Shafi NI, Bryan RM Jr. Endothelial influences on cerebrovascular tone. J Appl Physiol. 2006;100:318–27.

    Article  PubMed  CAS  Google Scholar 

  90. Sehba FA, Bederson JB. Mechanisms of acute brain injury after subarachnoid hemorrhage. Neurol Res. 2006;28:381–98.

    Article  PubMed  CAS  Google Scholar 

  91. Zhou Q, Hellermann GR, Solomonson LP. Nitric oxide release from resting human platelets. Thromb Res. 1995;77:87–96.

    Article  PubMed  CAS  Google Scholar 

  92. Moro MA, Russel RJ, Cellek S, Lizasoain I, Su Y, Darley-Usmar VM et al. cGMP mediates the vascular and platelet actions of nitric oxide: confirmation using an inhibitor of the soluble guanylyl cyclase. Proc Natl Acad Sci USA. 1996;93:1480–5.

    Article  PubMed  CAS  Google Scholar 

  93. Smith CC, Stanyer L, Cooper MB, Betteridge DJ. Platelet aggregation may not be a prerequisite for collagen-stimulated platelet generation of nitric oxide. Biochim Biophys Acta. 1999;1473:286–92.

    Article  PubMed  CAS  Google Scholar 

  94. Abumiya T, Fitridge R, Mazur C, Copeland BR, Koziol JA, Tschopp JF et al. Integrin alpha(IIb)beta(3) inhibitor preserves microvascular patency in experimental acute focal cerebral ischemia. Stroke 2000;31:1402–9; discussion 1409–1410.

    Article  PubMed  CAS  Google Scholar 

  95. Ames Ad, Wright RL, Kowada M, Thurston JM, Majno G. Cerebral ischemia. II. The no-reflow phenomenon. Am J Pathol. 1968;52:437–53.

    PubMed  Google Scholar 

  96. del Zoppo GJ. Microvascular responses to cerebral ischemia/inflammation. Ann NY Acad Sci. 1997;823:132–47.

    Article  PubMed  CAS  Google Scholar 

  97. Fukami MH, Holmsen H, Kowalska MA, Niewiarowski S. (2001) Platelet secretion. In: Colman RW, Hirsh J, Marder VJ, Clowes AW, George JN editors. Hemostatis and thrombosis basic principles and clinical practice. Phialdelphia: Lippincott Williams & Wilkins, p. 562–73.

    Google Scholar 

  98. Okada Y, Copeland BR, Mori E, Tung MM, Thomas WS, del Zoppo GJ. P-selectin and intercellular adhesion molecule-1 expression after focal brain ischemia and reperfusion. Stroke 1994;25:202–11.

    Article  PubMed  CAS  Google Scholar 

  99. Reed GL. (2002) Platelet secretion. In: Michelson AD, editor. Platelets. San Diego, CA: Academic press, p. 181–95.

    Google Scholar 

  100. Fernandez-Patron C, Martinez-Cuesta MA, Salas E, Sawicki G, Wozniak M, Radomski MW et al. Differential regulation of platelet aggregation by matrix metalloproteinases-9 and -2. Thromb Haemost. 1999;82:1730–5.

    PubMed  CAS  Google Scholar 

  101. Rosenberg GA, Estrada EY, Dencoff JE. Matrix metalloproteinases and TIMPs are associated with blood-brain barrier opening after reperfusion in rat brain. Stroke 1998;29:2189–95.

    Article  PubMed  CAS  Google Scholar 

  102. Rosenberg GA, Kornfeld M, Estrada E, Kelley RO, Liotta LA, Stetler-Stevenson WG. TIMP-2 reduces proteolytic opening of blood-brain barrier by type IV collagenase. Brain Res. 1992;576:203–7.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Departments of Neurosurgery and of Neuroscience, Mount Sinai School of Medicine, New York, NY, 10029, USA

    Fatima A. Sehba & Victor Friedrich

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  1. Fatima A. Sehba
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  2. Victor Friedrich
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Correspondence to Fatima A. Sehba .

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Editors and Affiliations

  1. Department of Neurosurgery, Southwest Hospital, Third Military Medical University, Gaotanyan 30, Chongqing, 400038, China

    H.-J. Steiger  & Hua Feng  & 

  2. Department of Neurosurgery, Huashan Hospital, Fudan University, Shanghai, China

    Ying Mao

  3. Departments of Physiology and Neurosurgery, Loma Linda University School of Medicine, Risley Hall, Room 223, 92354, Loma Linda, California, USA

    John H. Zhang

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Sehba, F.A., Friedrich, V. (2011). Early Micro Vascular Changes After Subarachnoid Hemorrhage. In: Feng, H., Mao, Y., Zhang, J.H. (eds) Early Brain Injury or Cerebral Vasospasm. Acta Neurochirurgica Supplements, vol 110/1. Springer, Vienna. https://doi.org/10.1007/978-3-7091-0353-1_9

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  • DOI: https://doi.org/10.1007/978-3-7091-0353-1_9

  • Publisher Name: Springer, Vienna

  • Print ISBN: 978-3-7091-0352-4

  • Online ISBN: 978-3-7091-0353-1

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