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Neurovascular Network as Future Therapeutic Targets

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Cerebral Venous System in Acute and Chronic Brain Injuries

Abstract

In recent years, endovascular treatment, including pharmaceutical drugs and intervention therapy, has become one of the most effective strategies for stroke patients. However, neurobiological and neurovascular functions, before, during and after endovascular therapy, have not been fully addressed and remain to be clarified. It is extremely important for basic neurovascular scientists and clinicians to understand the neurobiological and neurovascular fundamentals of neuroimaging mismatches and the infarct size of stroke patients, hyperperfusion or hypoperfusion after thrombolysis or thrombolectomy, and brain swelling and hemorrhage after successful thrombolectomy. These clinical mismatches and complexities after endovascular therapy are related to active tissue connections in the neurovascular network and the function of neurobiological and neurovascular components after stroke. This comprehensive review summarizes the fundamental neurobiology and neurovascular function in endovascular therapy for stroke patients, using both basic science research and clinical studies, with a focus on cerebral hemodynamics, cell energy metabolism, and neurovascular injuries such as brain swelling, hemorrhage or over-reperfusion. A major emphasis is the potential role of cerebral collateral circulation and venous circulation during and after endovascular therapy. It is clear that the cerebral hemodynamic balance, venous function, and autoregulation are all involved in endovascular therapy.

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Abbreviations

CBF:

Cerebral blood flow

CBF:

Cerebral blood flow

CFI:

Collateral flow index

CO2:

Carbon dioxide

CPP:

Cerebral perfusion pressure

CT:

Computed tomography

CTA:

computed tomography angiography

CTP:

Computed tomography perfusion

CTV:

Computed tomography venography

DSA:

Digital subtraction angiography

DVP:

Draining vein pressure

DWI:

Diffusion weighted imaging

ECD:

Echo color Doppler

EG:

Emptying gradient

ET:

Emptying time

FG:

Filling gradient

FLAIR:

Fluid-attenuated inversion recovery

fMUS:

Functional micro-ultrasound

FT:

Filling time

GOS:

Glasgow outcome scale

HBinF:

Head inflow

HBoutF:

Head outflow

MCAO:

Middle cerebral artery occlusion

MRA:

Magnetic resonance angiography

MRI:

Magnetic resonance imaging

MRV:

Magnetic resonance venography

NIHSS:

National Institutes of Health Stroke Scale

NO:

Nitric oxide

OPS:

Orthogonal polarized spectral

PDGF:

Platelet-derived growth factor

PDGF-BB:

Platelet-derived growth factor-BB

PPARγ:

Peroxisome proliferator-activated receptor-gamma

rCBF:

Relative cerebral blood flow

rCBV:

Relative cerebral blood volume

ROS:

Reactive oxygen species

rtPA:

Recombinant tissue plasminogen activator

RV:

Residual volume

SPECT:

Single photon emission computed tomography

SSS:

Superior sagittal sinus

SWI:

Susceptibility weighted imaging

VEGF:

Vascular endothelial growth factor

VV:

Venous volume

References

  1. Paciaroni M, Bogousslavsky J. How did stroke become of interest to neurologists?: a slow 19th century saga. Neurology. 2009;73:724–8.

    Article  PubMed  Google Scholar 

  2. Safavi-Abbasi S, Reis C, Talley MC, Theodore N, Nakaji P, Spetzler RF, Preul MC. Rudolf Ludwig Karl Virchow: pathologist, physician, anthropologist, and politician. Implications of his work for the understanding of cerebrovascular pathology and stroke. Neurosurg Focus. 2006;20:E1.

    Article  PubMed  Google Scholar 

  3. Eckert B. Acute stroke therapy 1981-2009. Klin Neuroradiol. 2009;19:8–19.

    Article  PubMed  Google Scholar 

  4. National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. Tissue plasminogen activator for acute ischemic stroke. The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. N Engl J Med. 1995;333:1581–7.

    Article  Google Scholar 

  5. Lees KR, Bluhmki E, von Kummer R, Brott TG, Toni D, Grotta JC, Albers GW, Kaste M, Marler JR, Hamilton SA, Tilley BC, Davis SM, Donnan GA, Hacke W, Ecass AN, Group, E.r.-P.S., Allen K, Mau J, Meier D, del Zoppo G, De Silva DA, Butcher KS, Parsons MW, Barber PA, Levi C, Bladin C, Byrnes G. Time to treatment with intravenous alteplase and outcome in stroke: an updated pooled analysis of ECASS, ATLANTIS, NINDS, and EPITHET trials. Lancet. 2010;375:1695–703.

    Article  CAS  PubMed  Google Scholar 

  6. O’Collins VE, Macleod MR, Donnan GA, Horky LL, van der Worp BH, Howells DW. 1,026 experimental treatments in acute stroke. Ann Neurol. 2006;59:467–77.

    Article  PubMed  CAS  Google Scholar 

  7. del Zoppo GJ. Stroke and neurovascular protection. N Engl J Med. 2006;354:553–5.

    Article  PubMed  Google Scholar 

  8. Guo S, Lo EH. Dysfunctional cell-cell signaling in the neurovascular unit as a paradigm for central nervous system disease. Stroke. 2009;40:S4–7.

    Article  PubMed  Google Scholar 

  9. Iadecola C, Anrather J. Stroke research at a crossroad: asking the brain for directions. Nat Neurosci. 2011;14:1363–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Xing C, Hayakawa K, Lok J, Arai K, Lo EH. Injury and repair in the neurovascular unit. Neurol Res. 2012;34:325–30.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Xing C, Lo EH. Help-me signaling: non-cell autonomous mechanisms of neuroprotection and neurorecovery. Prog Neurobiol. 2017;152:181.

    Article  PubMed  Google Scholar 

  12. Shi Y, Leak RK, Keep RF, Chen J. Translational stroke research on blood-brain barrier damage: challenges, perspectives, and goals. Transl Stroke Res. 2016;7:89–92.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Chen S, Chen Y, Xu L, Matei N, Tang J, Feng H, Zhang JH. Venous system in acute brain injury: mechanisms of pathophysiological change and function. Exp Neurol. 2015;272:4–10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Chen Y, Li Q, Tang J, Feng H, Zhang JH. The evolving roles of pericyte in early brain injury after subarachnoid hemorrhage. Brain Res. 2015;1623:110–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Li Q, Khatibi N, Zhang JH. Vascular neural network: the importance of vein drainage in stroke. Transl Stroke Res. 2014;5:163–6.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Yin Y, Ge H, Zhang JH, Feng H. Targeting vascular neural network in intracerebral hemorrhage. Curr Pharm Des. 2017;23:2197.

    Article  CAS  PubMed  Google Scholar 

  17. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Zhang Z, Deng X, Dai Z, Chen B, Gao B, Xia C, Chen D, Han H. MRI image of the internal cerebral vein and basilar artery of rabbit following subarachnoid hemorrhage. Chin J Anat. 2012;35:137–40.

    CAS  Google Scholar 

  19. Xing C, Hayakawa K, Lo EH. Mechanisms, imaging, and therapy in stroke recovery. Transl Stroke Res. 2017;8:1.

    Article  CAS  PubMed  Google Scholar 

  20. Ginsberg MD. Expanding the concept of neuroprotection for acute ischemic stroke: the pivotal roles of reperfusion and the collateral circulation. Prog Neurobiol. 2016;145-146:46–77.

    Article  PubMed  Google Scholar 

  21. Liang LJ, Yang JM, Jin XC. Cocktail treatment, a promising strategy to treat acute cerebral ischemic stroke? Med Gas Res. 2016;6:33–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Rodrigues FB, Neves JB, Caldeira D, Ferro JM, Ferreira JJ, Costa J. Endovascular treatment versus medical care alone for ischaemic stroke: systematic review and meta-analysis. BMJ. 2016;353:i1754.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Shi SH, Qi ZF, Luo YM, Ji XM, Liu KJ. Normobaric oxygen treatment in acute ischemic stroke: a clinical perspective. Med Gas Res. 2016;6:147–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Zhai WW, Sun L, Yu ZQ, Chen G. Hyperbaric oxygen therapy in experimental and clinical stroke. Med Gas Res. 2016;6:111–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Linfante I, Cipolla MJ. Improving reperfusion therapies in the era of mechanical thrombectomy. Transl Stroke Res. 2016;7:294–302.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Pound P, Bury M, Ebrahim S. From apoplexy to stroke. Age Ageing. 1997;26:331–7.

    Article  CAS  PubMed  Google Scholar 

  27. Schiller F. Concepts of stroke before and after Virchow. Med Hist. 1970;14:115–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Simon RP, Swan JH, Griffiths T, Meldrum BS. Blockade of N-methyl-D-aspartate receptors may protect against ischemic damage in the brain. Science. 1984;226:850–2.

    Article  CAS  PubMed  Google Scholar 

  29. del Zoppo GJ. The neurovascular unit in the setting of stroke. J Intern Med. 2010;267:156–71.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Iadecola C. Neurovascular regulation in the normal brain and in Alzheimer’s disease. Nat Rev Neurosci. 2004;5:347–60.

    Article  CAS  PubMed  Google Scholar 

  31. Lo EH, Broderick JP, Moskowitz MA. tPA and proteolysis in the neurovascular unit. Stroke. 2004;35:354–6.

    Article  PubMed  Google Scholar 

  32. McHedlishvili G. Physiological mechanisms controlling cerebral blood flow. Stroke. 1980;11:240–8.

    Article  CAS  PubMed  Google Scholar 

  33. Hallenbeck JM, Bradley ME. Experimental model for systematic study of impaired microvascular reperfusion. Stroke. 1977;8:238–43.

    Article  CAS  PubMed  Google Scholar 

  34. Yu W, Rives J, Welch B, White J, Stehel E, Samson D. Hypoplasia or occlusion of the ipsilateral cranial venous drainage is associated with early fatal edema of middle cerebral artery infarction. Stroke. 2009;40:3736–9.

    Article  PubMed  Google Scholar 

  35. al-Rodhan NR, Sundt TM Jr, Piepgras DG, Nichols DA, Rufenacht D, Stevens LN. Occlusive hyperemia: a theory for the hemodynamic complications following resection of intracerebral arteriovenous malformations. J Neurosurg. 1993;78:167–75.

    Article  CAS  PubMed  Google Scholar 

  36. Nakase H, Heimann A, Kempski O. Local cerebral blood flow in a rat cortical vein occlusion model. J Cereb Blood Flow Metab. 1996;16:720–8.

    Article  CAS  PubMed  Google Scholar 

  37. Ames A 3rd, Wright RL, Kowada M, Thurston JM, Majno G. Cerebral ischemia. II. The no-reflow phenomenon. Am J Pathol. 1968;52:437–53.

    PubMed  PubMed Central  Google Scholar 

  38. Andeweg J. Consequences of the anatomy of deep venous outflow from the brain. Neuroradiology. 1999;41:233–41.

    Article  CAS  PubMed  Google Scholar 

  39. Kilic T, Akakin A. Anatomy of cerebral veins and sinuses. Front Neurol Neurosci. 2008;23:4–15.

    Article  PubMed  Google Scholar 

  40. Schmidek HH, Auer LM, Kapp JP. The cerebral venous system. Neurosurgery. 1985;17:663–78.

    Article  CAS  PubMed  Google Scholar 

  41. Dickerman RD, Smith GH, Langham-Roof L, McConathy WJ, East JW, Smith AB. Intra-ocular pressure changes during maximal isometric contraction: does this reflect intra-cranial pressure or retinal venous pressure? Neurol Res. 1999;21:243–6.

    Article  CAS  PubMed  Google Scholar 

  42. Edvinsson L, Hogestatt ED, Uddman R, Auer LM. Cerebral veins: fluorescence histochemistry, electron microscopy, and in vitro reactivity. J Cereb Blood Flow Metab. 1983;3:226–30.

    Article  CAS  PubMed  Google Scholar 

  43. Allt G, Lawrenson JG. Pericytes: cell biology and pathology. Cells Tissues Organs. 2001;169:1–11.

    Article  CAS  PubMed  Google Scholar 

  44. Takahashi A, Ushiki T, Abe K, Houkin K, Abe H. Cytoarchitecture of periendothelial cells in human cerebral venous vessels as compared with the scalp vein. A scanning electron microscopic study. Arch Histol Cytol. 1994;57:331–9.

    Article  CAS  PubMed  Google Scholar 

  45. Tso MK, Macdonald RL. Acute microvascular changes after subarachnoid hemorrhage and transient global cerebral ischemia. Stroke Res Treat. 2013;2013:425281.

    PubMed  PubMed Central  Google Scholar 

  46. 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.

    Article  CAS  PubMed  Google Scholar 

  47. Ferrari-Dileo G, Davis EB, Anderson DR. Glaucoma, capillaries and pericytes. 3. Peptide hormone binding and influence on pericytes. Ophthalmologica. 1996;210:269–75.

    Article  CAS  PubMed  Google Scholar 

  48. Kawamura H, Kobayashi M, Li Q, Yamanishi S, Katsumura K, Minami M, Wu DM, Puro DG. Effects of angiotensin II on the pericyte-containing microvasculature of the rat retina. J Physiol. 2004;561:671–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Matsugi T, Chen Q, Anderson DR. Contractile responses of cultured bovine retinal pericytes to angiotensin II. Arch Ophthalmol. 1997;115:1281–5.

    Article  CAS  PubMed  Google Scholar 

  50. Murphy DD, Wagner RC. Differential contractile response of cultured microvascular pericytes to vasoactive agents. Microcirculation. 1994;1:121–8.

    Article  CAS  PubMed  Google Scholar 

  51. Edwards A, Cao C, Pallone TL. Cellular mechanisms underlying nitric oxide-induced vasodilation of descending vasa recta. Am J Physiol Renal Physiol. 2011;300:F441–56.

    Article  CAS  PubMed  Google Scholar 

  52. Nakaizumi A, Puro DG. Vulnerability of the retinal microvasculature to hypoxia: role of polyamine-regulated K(ATP) channels. Invest Ophthalmol Vis Sci. 2011;52:9345–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Donoghue L, Tyburski JG, Steffes CP, Wilson RF. Vascular endothelial growth factor modulates contractile response in microvascular lung pericytes. Am J Surg. 2006;191:349–52.

    Article  CAS  PubMed  Google Scholar 

  54. Harvey EH, Tyburski JG, Steffes CP, Carlin AM. Inhibition of heme oxygenase-1 in microvascular lung pericytes diminishes at high concentrations of an inflammatory mediator. Am Surg. 2004;70:141–45; discussion 145.

    PubMed  Google Scholar 

  55. Speyer CL, Steffes CP, Ram JL. Effects of vasoactive mediators on the rat lung pericyte: quantitative analysis of contraction on collagen lattice matrices. Microvasc Res. 1999;57:134–43.

    Article  CAS  PubMed  Google Scholar 

  56. Wang S, Cao C, Chen Z, Bankaitis V, Tzima E, Sheibani N, Burridge K. Pericytes regulate vascular basement membrane remodeling and govern neutrophil extravasation during inflammation. PLoS One. 2012;7:e45499.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Anderson DR, Davis EB. Glaucoma, capillaries and pericytes. 5. Preliminary evidence that carbon dioxide relaxes pericyte contractile tone. Ophthalmologica. 1996;210:280–4.

    Article  CAS  PubMed  Google Scholar 

  58. Chen Q, Anderson DR. Effect of CO2 on intracellular pH and contraction of retinal capillary pericytes. Invest Ophthalmol Vis Sci. 1997;38:643–51.

    CAS  PubMed  Google Scholar 

  59. Oishi K, Kamiyashiki T, Ito Y. Isometric contraction of microvascular pericytes from mouse brain parenchyma. Microvasc Res. 2007;73:20–8.

    Article  CAS  PubMed  Google Scholar 

  60. Wu DM, Kawamura H, Sakagami K, Kobayashi M, Puro DG. Cholinergic regulation of pericyte-containing retinal microvessels. Am J Physiol Heart Circ Physiol. 2003;284:H2083–90.

    Article  CAS  PubMed  Google Scholar 

  61. Kelley C, D’Amore P, Hechtman HB, Shepro D. Vasoactive hormones and cAMP affect pericyte contraction and stress fibres in vitro. J Muscle Res Cell Motil. 1988;9:184–94.

    Article  CAS  PubMed  Google Scholar 

  62. Sims DE, Miller FN, Horne MM, Edwards MJ. Interleukin-2 alters the positions of capillary and venule pericytes in rat cremaster muscle. J Submicrosc Cytol Pathol. 1994;26:507–13.

    CAS  PubMed  Google Scholar 

  63. Yamanishi S, Katsumura K, Kobayashi T, Puro DG. Extracellular lactate as a dynamic vasoactive signal in the rat retinal microvasculature. Am J Physiol Heart Circ Physiol. 2006;290:H925–34.

    Article  CAS  PubMed  Google Scholar 

  64. Chakravarthy U, Gardiner TA, Anderson P, Archer DB, Trimble ER. The effect of endothelin 1 on the retinal microvascular pericyte. Microvasc Res. 1992;43:241–54.

    Article  CAS  PubMed  Google Scholar 

  65. Ramachandran E, Frank RN, Kennedy A. Effects of endothelin on cultured bovine retinal microvascular pericytes. Invest Ophthalmol Vis Sci. 1993;34:586–95.

    CAS  PubMed  Google Scholar 

  66. Gillies MC, Su T. High glucose inhibits retinal capillary pericyte contractility in vitro. Invest Ophthalmol Vis Sci. 1993;34:3396–401.

    CAS  PubMed  Google Scholar 

  67. Wakisaka M, Kitazono T, Kato M, Nakamura U, Yoshioka M, Uchizono Y, Yoshinari M. Sodium-coupled glucose transporter as a functional glucose sensor of retinal microvascular circulation. Circ Res. 2001;88:1183–8.

    Article  CAS  PubMed  Google Scholar 

  68. Miller FN, Sims DE. Contractile elements in the regulation of macromolecular permeability. Fed Proc. 1986;45:84–8.

    CAS  PubMed  Google Scholar 

  69. Fernandez N, Monge L, Garcia-Villalon AL, Garcia JL, Gomez B, Dieguez G. Endothelin-1-induced in vitro cerebral venoconstriction is mediated by endothelin ETA receptors. Eur J Pharmacol. 1995;294:483–90.

    Article  CAS  PubMed  Google Scholar 

  70. Hardebo JE, Kahrstrom J, Owman C, Salford LG. Endothelin is a potent constrictor of human intracranial arteries and veins. Blood Vessels. 1989;26:249–53.

    CAS  PubMed  Google Scholar 

  71. Ishine T, Yu JG, Asada Y, Lee TJ. Nitric oxide is the predominant mediator for neurogenic vasodilation in porcine pial veins. J Pharmacol Exp Ther. 1999;289:398–404.

    CAS  PubMed  Google Scholar 

  72. Tomimoto H, Nishimura M, Suenaga T, Nakamura S, Akiguchi I, Wakita H, Kimura J, Mayer B. Distribution of nitric oxide synthase in the human cerebral blood vessels and brain tissues. J Cereb Blood Flow Metab. 1994;14:930–8.

    Article  CAS  PubMed  Google Scholar 

  73. Pearce WJ, Bevan JA. Retroglenoid venoconstriction and its influence on canine intracranial venous pressures. J Cereb Blood Flow Metab. 1984;4:373–80.

    Article  CAS  PubMed  Google Scholar 

  74. Monge L, Garcia-Villalon AL, Fernandez N, Garcia JL, Gomez B, Dieguez G. In vitro relaxation of dog cerebral veins in response to histamine is mediated by histamine H2 receptors. Eur J Pharmacol. 1997;338:135–41.

    Article  CAS  PubMed  Google Scholar 

  75. Gross PM. Histamine H1- and H2-receptors are differentially and spatially distributed in cerebral vessels. J Cereb Blood Flow Metab. 1981;1:441–6.

    Article  CAS  PubMed  Google Scholar 

  76. Edvinsson L, Emson P, McCulloch J, Tatemoto K, Uddman R. Neuropeptide Y: immunocytochemical localization to and effect upon feline pial arteries and veins in vitro and in situ. Acta Physiol Scand. 1984;122:155–63.

    Article  CAS  PubMed  Google Scholar 

  77. Garcia JH, Liu KF, Yoshida Y, Chen S, Lian J. Brain microvessels: factors altering their patency after the occlusion of a middle cerebral artery (Wistar rat). Am J Pathol. 1994;145:728–40.

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Little JR, Kerr FWL, Sundt TM. Microcirculatory obstruction in focal cerebral ischemia: an electron microscopic investigation in monkeys. Stroke. 1976;7:25–30.

    Article  PubMed  Google Scholar 

  79. Belayev L, Pinard E, Nallet H, Seylaz J, Liu Y, Riyamongkol P, Zhao W, Busto R, Ginsberg MD. Albumin therapy of transient focal cerebral ischemia: in vivo analysis of dynamic microvascular responses. Stroke. 2002;33:1077–84.

    Article  PubMed  Google Scholar 

  80. del Zoppo GJ, Schmid-Schonbein GW, Mori E, Copeland BR, Chang CM. Polymorphonuclear leukocytes occlude capillaries following middle cerebral artery occlusion and reperfusion in baboons. Stroke. 1991;22:1276–83.

    Article  PubMed  Google Scholar 

  81. Garcia JH, Liu KF, Yoshida Y, Lian J, Chen S, del Zoppo GJ. Influx of leukocytes and platelets in an evolving brain infarct (Wistar rat). Am J Pathol. 1994;144:188–99.

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Hallenbeck JM, Dutka AJ, Tanishima T, Kochanek PM, Kumaroo KK, Thompson CB, Obrenovitch TP, Contreras TJ. Polymorphonuclear leukocyte accumulation in brain regions with low blood flow during the early postischemic period. Stroke. 1986;17:246–53.

    Article  CAS  PubMed  Google Scholar 

  83. Ritter LS, Orozco JA, Coull BM, McDonagh PF, Rosenblum WI. Leukocyte accumulation and hemodynamic changes in the cerebral microcirculation during early reperfusion after stroke. Stroke. 2000;31:1153–61.

    Article  CAS  PubMed  Google Scholar 

  84. Dalkara T, Arsava EM. Can restoring incomplete microcirculatory reperfusion improve stroke outcome after thrombolysis? J Cereb Blood Flow Metab. 2012;32:2091–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Choudhri TF, Hoh BL, Zerwes HG, Prestigiacomo CJ, Kim SC, Connolly ES Jr, Kottirsch G, Pinsky DJ. Reduced microvascular thrombosis and improved outcome in acute murine stroke by inhibiting GP IIb/IIIa receptor-mediated platelet aggregation. J Clin Invest. 1998;102:1301–10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Liu S, Connor J, Peterson S, Shuttleworth CW, Liu KJ. Direct visualization of trapped erythrocytes in rat brain after focal ischemia and reperfusion. J Cereb Blood Flow Metab. 2002;22:1222–30.

    Article  PubMed  Google Scholar 

  87. Morris DC, Davies K, Zhang Z, Chopp M. Measurement of cerebral microvessel diameters after embolic stroke in rat using quantitative laser scanning confocal microscopy. Brain Res. 2000;876:31–6.

    Article  CAS  PubMed  Google Scholar 

  88. Zhang ZG, Chopp M, Goussev A, Lu D, Morris D, Tsang W, Powers C, Ho KL. Cerebral microvascular obstruction by fibrin is associated with upregulation of PAI-1 acutely after onset of focal embolic ischemia in rats. J Neurosci. 1999;19:10898–907.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Paciaroni M, Caso V, Agnelli G. The concept of ischemic penumbra in acute stroke and therapeutic opportunities. Eur Neurol. 2009;61:321–30.

    Article  PubMed  Google Scholar 

  90. Meoded A, Poretti A, Benson JE, Tekes A, Huisman TA. Evaluation of the ischemic penumbra focusing on the venous drainage: the role of susceptibility weighted imaging (SWI) in pediatric ischemic cerebral stroke. J Neuroradiol. 2014;41:108.

    Article  PubMed  Google Scholar 

  91. Nemoto EM. Dynamics of cerebral venous and intracranial pressures. Acta Neurochir Suppl. 2006;96:435–7.

    Article  CAS  PubMed  Google Scholar 

  92. Ishikawa M, Zhang JH, Nanda A, Granger DN. Inflammatory responses to ischemia and reperfusion in the cerebral microcirculation. Front Biosci. 2004;9:1339–47.

    Article  CAS  PubMed  Google Scholar 

  93. Ishikawa M, Cooper D, Arumugam TV, Zhang JH, Nanda A, Granger DN. Platelet-leukocyte-endothelial cell interactions after middle cerebral artery occlusion and reperfusion. J Cereb Blood Flow Metab. 2004;24:907–15.

    Article  CAS  PubMed  Google Scholar 

  94. Simard JM, Kent TA, Chen M, Tarasov KV, Gerzanich V. Brain oedema in focal ischaemia: molecular pathophysiology and theoretical implications. Lancet Neurol. 2007;6:258–68.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Rahemtullah A, Van Cott EM. Hypercoagulation testing in ischemic stroke. Arch Pathol Lab Med. 2007;131:890–901.

    CAS  PubMed  Google Scholar 

  96. Togay Isikay C, Kural AM, Erden I. Cerebral vein thrombosis as an exceptional cause of transient ischemic attack. J Stroke Cerebrovasc Dis. 2012;21:907.e909–12.

    Article  Google Scholar 

  97. Nakase H, Nagata K, Otsuka H, Sakaki T, Kempski O. Local cerebral blood flow autoregulation following “asymptomatic” cerebral venous occlusion in the rat. J Neurosurg. 1998;89:118–24.

    Article  CAS  PubMed  Google Scholar 

  98. Jacobs K, Moulin T, Bogousslavsky J, Woimant F, Dehaene I, Tatu L, Besson G, Assouline E, Casselman J. The stroke syndrome of cortical vein thrombosis. Neurology. 1996;47:376–82.

    Article  CAS  PubMed  Google Scholar 

  99. Shih AY, Blinder P, Tsai PS, Friedman B, Stanley G, Lyden PD, Kleinfeld D. The smallest stroke: occlusion of one penetrating vessel leads to infarction and a cognitive deficit. Nat Neurosci. 2013;16:55–63.

    Article  CAS  PubMed  Google Scholar 

  100. Fischer EG, Ames A 3rd, Hedley-Whyte ET, O’Gorman S. Reassessment of cerebral capillary changes in acute global ischemia and their relationship to the “no-reflow phenomenon”. Stroke. 1977;8:36–9.

    Article  CAS  PubMed  Google Scholar 

  101. Ito U, Ohno K, Yamaguchi T, Tomita H, Inaba Y, Kashima M. Transient appearance of “no-reflow” phenomenon in Mongolian gerbils. Stroke. 1980;11:517–21.

    Article  CAS  PubMed  Google Scholar 

  102. Xi G, Keep RF, Hoff JT. Mechanisms of brain injury after intracerebral haemorrhage. Lancet Neurol. 2006;5:53–63.

    Article  PubMed  Google Scholar 

  103. Diringer MN. Intracerebral hemorrhage: pathophysiology and management. Crit Care Med. 1993;21:1591–603.

    Article  CAS  PubMed  Google Scholar 

  104. Prabhakaran S, Naidech AM. Ischemic brain injury after intracerebral hemorrhage: a critical review. Stroke. 2012;43:2258–63.

    Article  PubMed  Google Scholar 

  105. Morgenstern LB, Hemphill JC 3rd, Anderson C, Becker K, Broderick JP, Connolly ES Jr, Greenberg SM, Huang JN, MacDonald RL, Messe SR, Mitchell PH, Selim M, Tamargo RJ, American Heart Association Stroke Council and Council on Cardiovascular Nursing. Guidelines for the management of spontaneous intracerebral hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2010;41:2108–29.

    Article  PubMed  PubMed Central  Google Scholar 

  106. Gregoire SM, Charidimou A, Gadapa N, Dolan E, Antoun N, Peeters A, Vandermeeren Y, Laloux P, Baron JC, Jager HR, Werring DJ. Acute ischaemic brain lesions in intracerebral haemorrhage: multicentre cross-sectional magnetic resonance imaging study. Brain. 2011;134:2376–86.

    Article  PubMed  Google Scholar 

  107. Kang DW, Han MK, Kim HJ, Yun SC, Jeon SB, Bae HJ, Kwon SU, Kim JS. New ischemic lesions coexisting with acute intracerebral hemorrhage. Neurology. 2012;79:848–55.

    Article  PubMed  Google Scholar 

  108. Kimberly WT, Gilson A, Rost NS, Rosand J, Viswanathan A, Smith EE, Greenberg SM. Silent ischemic infarcts are associated with hemorrhage burden in cerebral amyloid angiopathy. Neurology. 2009;72:1230–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Menon RS, Burgess RE, Wing JJ, Gibbons MC, Shara NM, Fernandez S, Jayam-Trouth A, German L, Sobotka I, Edwards D, Kidwell CS. Predictors of highly prevalent brain ischemia in intracerebral hemorrhage. Ann Neurol. 2012;71:199–205.

    Article  PubMed  PubMed Central  Google Scholar 

  110. Prabhakaran S, Gupta R, Ouyang B, John S, Temes RE, Mohammad Y, Lee VH, Bleck TP. Acute brain infarcts after spontaneous intracerebral hemorrhage: a diffusion-weighted imaging study. Stroke. 2010;41:89–94.

    Article  PubMed  Google Scholar 

  111. Ziai WC. Hematology and inflammatory signaling of intracerebral hemorrhage. Stroke. 2013;44:S74–8.

    Article  PubMed  Google Scholar 

  112. Wang J. Preclinical and clinical research on inflammation after intracerebral hemorrhage. Prog Neurobiol. 2010;92:463–77.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Hua Y, Keep RF, Hoff JT, Xi G. Brain injury after intracerebral hemorrhage: the role of thrombin and iron. Stroke. 2007;38:759–62.

    Article  CAS  PubMed  Google Scholar 

  114. Bateman GA. Association between arterial inflow and venous outflow in idiopathic and secondary intracranial hypertension. J Clin Neurosci. 2006;13:550–6; discussion 557.

    Article  PubMed  Google Scholar 

  115. Etminan N. Aneurysmal subarachnoid hemorrhage—status quo and perspective. Transl Stroke Res. 2015;6:167–70.

    Article  PubMed  Google Scholar 

  116. Macdonald RL, Pluta RM, Zhang JH. Cerebral vasospasm after subarachnoid hemorrhage: the emerging revolution. Nat Clin Pract Neurol. 2007;3:256–63.

    Article  CAS  PubMed  Google Scholar 

  117. Macdonald RL, Higashida RT, Keller E, Mayer SA, 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;10:618–25.

    Article  CAS  PubMed  Google Scholar 

  118. Macdonald RL, Kassell NF, 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;39:3015–21.

    Article  CAS  PubMed  Google Scholar 

  119. Cahill J, Zhang JH. Subarachnoid hemorrhage: is it time for a new direction? Stroke. 2009;40:S86–7.

    Article  PubMed  Google Scholar 

  120. Sehba FA, Pluta RM, Zhang JH. Metamorphosis of subarachnoid hemorrhage research: from delayed vasospasm to early brain injury. Mol Neurobiol. 2011;43:27–40.

    Article  CAS  PubMed  Google Scholar 

  121. Suzuki H. What is early brain injury? Transl Stroke Res. 2015;6:1–3.

    Article  PubMed  Google Scholar 

  122. Lo EH, Rosenberg GA. The neurovascular unit in health and disease: introduction. Stroke. 2009;40:S2–3.

    Article  PubMed  Google Scholar 

  123. Chen S, Feng H, Sherchan P, Klebe D, Zhao G, Sun X, Zhang J, Tang J, Zhang JH. Controversies and evolving new mechanisms in subarachnoid hemorrhage. Prog Neurobiol. 2014;115:64–91.

    Article  PubMed  Google Scholar 

  124. Chen G, Tariq A, Ai J, Sabri M, Jeon HJ, Tang EJ, Lakovic K, Wan H, Macdonald RL. Different effects of clazosentan on consequences of subarachnoid hemorrhage in rats. Brain Res. 2011;1392:132–9.

    Article  CAS  PubMed  Google Scholar 

  125. Dai Z, Deng X, Zhang Z, Zhu Y, Zhang Y, Li D, Luo X, Mo Z, Han H. MRI study of deep cerebral veins after subarachniod hemorrhage in rabbits. Chin J Clin Anat. 2012;30:176–80.

    Google Scholar 

  126. 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.

    Article  CAS  PubMed  Google Scholar 

  127. 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.

    Article  PubMed  Google Scholar 

  128. 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 

  129. 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; disacussion 1315-1307.

    Article  PubMed  Google Scholar 

  130. Ishikawa M, Kusaka G, Yamaguchi N, Sekizuka E, Nakadate H, Minamitani H, Shinoda S, Watanabe E. Platelet and leukocyte adhesion in the microvasculature at the cerebral surface immediately after subarachnoid hemorrhage. Neurosurgery. 2009;64:546–53; discussion 553-544.

    Article  PubMed  Google Scholar 

  131. Bittencourt LK, Palma-Filho F, Domingues RC, Gasparetto EL. Subarachnoid hemorrhage in isolated cortical vein thrombosis: are presentation of an unusual condition. Arq Neuropsiquiatr. 2009;67:1106–8.

    Article  PubMed  Google Scholar 

  132. Cahill J, Calvert JW, Zhang JH. Mechanisms of early brain injury after subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2006;26:1341–53.

    Article  CAS  PubMed  Google Scholar 

  133. Sehba FA, Hou J, Pluta RM, Zhang JH. The importance of early brain injury after subarachnoid hemorrhage. Prog Neurobiol. 2012;97:14–37.

    Article  PubMed  PubMed Central  Google Scholar 

  134. Okubo S, Strahle J, Keep RF, Hua Y, Xi G. Subarachnoid hemorrhage-induced hydrocephalus in rats. Stroke. 2013;44:547–50.

    Article  PubMed  Google Scholar 

  135. Shah AH, Komotar RJ. Pathophysiology of acute hydrocephalus following subarachnoid hemorrhage. World Neurosurg. 2013;80:304.

    Article  PubMed  Google Scholar 

  136. Csokay A, Pataki G, Nagy L, Belan K. Vascular tunnel construction in the treatment of severe brain swelling caused by trauma and SAH. (evidence based on intra-operative blood flow measure). Neurol Res. 2002;24:157–60.

    Article  PubMed  Google Scholar 

  137. Benabu Y, Mark L, Daniel S, Glikstein R. Cerebral venous thrombosis presenting with subarachnoid hemorrhage. Case report and review. Am J Emerg Med. 2009;27:96–106.

    Article  PubMed  Google Scholar 

  138. El Otmani H, Moutaouakil F, Fadel H, Slassi I. [Subarachnoid hemorrhage induced by cerebral venous thrombosis]. J Mal Vasc. 2012;37:323–25.

    Google Scholar 

  139. Kato Y, Takeda H, Furuya D, Nagoya H, Deguchi I, Fukuoka T, Tanahashi N. Subarachnoid hemorrhage as the initial presentation of cerebral venous thrombosis. Intern Med. 2010;49:467–70.

    Article  PubMed  Google Scholar 

  140. Shukla R, Vinod P, Prakash S, Phadke RV, Gupta RK. Subarachnoid haemorrhage as a presentation of cerebral venous sinus thrombosis. J Assoc Physicians India. 2006;54:42–4.

    CAS  PubMed  Google Scholar 

  141. Shad A, Rourke TJ, Hamidian Jahromi A, Green AL. Straight sinus stenosis as a proposed cause of perimesencephalic non-aneurysmal haemorrhage. J Clin Neurosci. 2008;15:839–41.

    Article  PubMed  Google Scholar 

  142. Lee J, Koh EM, Chung CS, Hong SC, Kim YB, Chung PW, Suh BC, Moon HS. Underlying venous pathology causing perimesencephalic subarachnoid hemorrhage. Can J Neurol Sci. 2009;36:638–42.

    Article  PubMed  Google Scholar 

  143. Mathews MS, Brown D, Brant-Zawadzki M. Perimesencephalic nonaneurysmal hemorrhage associated with vein of Galen stenosis. Neurology. 2008;70:2410–1.

    Article  PubMed  Google Scholar 

  144. Sangra MS, Teasdale E, Siddiqui MA, Lindsay KW. Perimesencephalic nonaneurysmal subarachnoid hemorrhage caused by jugular venous occlusion: case report. Neurosurgery. 2008;63:E1202–3; discussion E1203.

    Article  PubMed  Google Scholar 

  145. Alen JF, Lagares A, Campollo J, Ballenilla F, Kaen A, Nunez AP, Lobato RD. Idiopathic subarachnoid hemorrhage and venous drainage: are they related? Neurosurgery. 2008;63:1106–11; discussion 1111-1102.

    Article  PubMed  Google Scholar 

  146. Kawamura Y, Narumi O, Chin M, Yamagata S. Variant deep cerebral venous drainage in idiopathic subarachnoid hemorrhage. Neurol Med Chir (Tokyo). 2011;51:97–100.

    Article  Google Scholar 

  147. Song JN, Chen H, Zhang M, Zhao YL, Ma XD. Dynamic change in cerebral microcirculation and focal cerebral metabolism in experimental subarachnoid hemorrhage in rabbits. Metab Brain Dis. 2013;28:33–43.

    Article  CAS  PubMed  Google Scholar 

  148. van der Schaaf IC, Velthuis BK, Gouw A, Rinkel GJ. Venous drainage in perimesencephalic hemorrhage. Stroke. 2004;35:1614–8.

    Article  PubMed  Google Scholar 

  149. Yamakawa H, Ohe N, Yano H, Yoshimura S, Iwama T. Venous drainage patterns in perimesencephalic nonaneurysmal subarachnoid hemorrhage. Clin Neurol Neurosurg. 2008;110:587–91.

    Article  PubMed  Google Scholar 

  150. Hashiguchi A, Mimata C, Ichimura H, Morioka M, Kuratsu J. Venous aneurysm development associated with a dural arteriovenous fistula of the anterior cranial fossa with devastating hemorrhage—case report. Neurol Med Chir (Tokyo). 2007;47:70–3.

    Article  Google Scholar 

  151. Matsuyama T, Okuchi K, Seki T, Higuchi T, Murao Y. Perimesencephalic nonaneurysmal subarachnoid hemorrhage caused by physical exertion. Neurol Med Chir (Tokyo). 2006;46:277–81; discussion 281-272.

    Article  Google Scholar 

  152. Czorlich P, Skevas C, Knospe V, Vettorazzi E, Richard G, Wagenfeld L, Westphal M, Regelsberger J. Terson syndrome in subarachnoid hemorrhage, intracerebral hemorrhage, and traumatic brain injury. Neurosurg Rev. 2015;38:129–36; discussion 136.

    Article  PubMed  Google Scholar 

  153. Czorlich P, Skevas C, Knospe V, Vettorazzi E, Westphal M, Regelsberger J. Terson’s syndrome—pathophysiologic considerations of an underestimated concomitant disease in aneurysmal subarachnoid hemorrhage. J Clin Neurosci. 2016;33:182–6.

    Article  PubMed  Google Scholar 

  154. Gutierrez Diaz A, Jimenez Carmena J, Ruano Martin F, Diaz Lopez P, Munoz Casado MJ. Intraocular hemorrhage in sudden increased intracranial pressure (Terson syndrome). Ophthalmologica. 1979;179:173–6.

    Article  CAS  PubMed  Google Scholar 

  155. Joswig H, Epprecht L, Valmaggia C, Leschka S, Hildebrandt G, Fournier JY, Stienen MN. Terson syndrome in aneurysmal subarachnoid hemorrhage-its relation to intracranial pressure, admission factors, and clinical outcome. Acta Neurochir. 2016;158:1027–36.

    Article  PubMed  Google Scholar 

  156. Prins M, Greco T, Alexander D, Giza CC. The pathophysiology of traumatic brain injury at a glance. Dis Model Mech. 2013;6:1307.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Arbour RB. Traumatic brain injury: pathophysiology, monitoring, and mechanism-based care. Crit Care Nurs Clin North Am. 2013;25:297–319.

    Article  PubMed  Google Scholar 

  158. Mustafa AG, Alshboul OA. Pathophysiology of traumatic brain injury. Neurosciences (Riyadh). 2013;18:222–34.

    Google Scholar 

  159. Roth P, Farls K. Pathophysiology of traumatic brain injury. Crit Care Nurs Q. 2000;23:14–25; quiz 65.

    Article  CAS  PubMed  Google Scholar 

  160. Werner C, Engelhard K. Pathophysiology of traumatic brain injury. Br J Anaesth. 2007;99:4–9.

    Article  CAS  PubMed  Google Scholar 

  161. Golding EM, Robertson CS, Bryan RM Jr. The consequences of traumatic brain injury on cerebral blood flow and autoregulation: a review. Clin Exp Hypertens. 1999;21:299–332.

    Article  CAS  PubMed  Google Scholar 

  162. Grundl PD, Biagas KV, Kochanek PM, Schiding JK, Barmada MA, Nemoto EM. Early cerebrovascular response to head injury in immature and mature rats. J Neurotrauma. 1994;11:135–48.

    Article  CAS  PubMed  Google Scholar 

  163. Yamakami I, McIntosh TK. Alterations in regional cerebral blood flow following brain injury in the rat. J Cereb Blood Flow Metab. 1991;11:655–60.

    Article  CAS  PubMed  Google Scholar 

  164. Maxwell WL, Irvine A, Adams JH, Graham DI, Gennarelli TA. Response of cerebral microvasculature to brain injury. J Pathol. 1988;155:327–35.

    Article  CAS  PubMed  Google Scholar 

  165. Xu RX, Yi SY, Wang BY. Experimental evaluation of blood-brain barrier permeability using colloidal gold particles as tracers in early-stage brain injury. Chin Med J. 1991;104:634–8.

    CAS  PubMed  Google Scholar 

  166. Chodobski A, Zink BJ, Szmydynger-Chodobska J. Blood-brain barrier pathophysiology in traumatic brain injury. Transl Stroke Res. 2011;2:492–516.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Dietrich WD, Alonso O, Halley M. Early microvascular and neuronal consequences of traumatic brain injury: a light and electron microscopic study in rats. J Neurotrauma. 1994;11:289–301.

    Article  CAS  PubMed  Google Scholar 

  168. Hartl R, Medary M, Ruge M, Arfors KE, Ghajar J. Blood-brain barrier breakdown occurs early after traumatic brain injury and is not related to white blood cell adherence. Acta Neurochir Suppl. 1997;70:240–2.

    CAS  PubMed  Google Scholar 

  169. Dimopoulou I, Tsagarakis S, Kouyialis AT, Roussou P, Assithianakis G, Christoforaki M, Ilias I, Sakas DE, Thalassinos N, Roussos C. Hypothalamic-pituitary-adrenal axis dysfunction in critically ill patients with traumatic brain injury: incidence, pathophysiology, and relationship to vasopressor dependence and peripheral interleukin-6 levels. Crit Care Med. 2004;32:404–8.

    Article  CAS  PubMed  Google Scholar 

  170. Samadani U, Reyes-Moreno I, Buchfelder M. Endocrine dysfunction following traumatic brain injury: mechanisms, pathophysiology and clinical correlations. Acta Neurochir Suppl. 2005;93:121–5.

    Article  CAS  PubMed  Google Scholar 

  171. Zacest AC, Vink R, Manavis J, Sarvestani GT, Blumbergs PC. Substance P immunoreactivity increases following human traumatic brain injury. Acta Neurochir Suppl. 2010;106:211–6.

    Article  PubMed  Google Scholar 

  172. Stein SC, Chen XH, Sinson GP, Smith DH. Intravascular coagulation: a major secondary insult in nonfatal traumatic brain injury. J Neurosurg. 2002;97:1373–7.

    Article  PubMed  Google Scholar 

  173. Schwarzmaier SM, Kim SW, Trabold R, Plesnila N. Temporal profile of thrombogenesis in the cerebral microcirculation after traumatic brain injury in mice. J Neurotrauma. 2010;27:121–30.

    Article  PubMed  Google Scholar 

  174. Chung CP, Hu HH. Pathogenesis of leukoaraiosis: role of jugular venous reflux. Med Hypotheses. 2010;75:85–90.

    Article  PubMed  Google Scholar 

  175. Burger R, Duncker D, Uzma N, Rohde V. Decompressive craniotomy: durotomy instead of duroplasty to reduce prolonged ICP elevation. Acta Neurochir Suppl. 2008;102:93–7.

    Article  PubMed  Google Scholar 

  176. Sindou M, Auque J, Jouanneau E. Neurosurgery and the intracranial venous system. Acta Neurochir Suppl. 2005;94:167–75.

    Article  CAS  PubMed  Google Scholar 

  177. Tubbs RS, Louis RG Jr, Song YB, Mortazavi M, Loukas M, Shoja MM, Cohen-Gadol AA. External landmarks for identifying the drainage site of the vein of Labbe: application to neurosurgical procedures. Br J Neurosurg. 2012;26:383–5.

    Article  PubMed  Google Scholar 

  178. Ryu CW, Koh JS, Yu SY, Kim EJ. Vasogenic edema of the Basal Ganglia after intra-arterial administration of nimodipine for treatment of vasospasm. J Korean Neurosurg Soc. 2011;49:112–5.

    Article  PubMed  PubMed Central  Google Scholar 

  179. Mayhan WG, Werber AH, Heistad DD. Protection of cerebral vessels by sympathetic nerves and vascular hypertrophy. Circulation. 1987;75:I107–12.

    CAS  PubMed  Google Scholar 

  180. Li G, Zeng X, Ji T, Fredrickson V, Wang T, Hussain M, Ren C, Chen J, Sikhram C, Ding Y, Ji X. A new thrombosis model of the superior sagittal sinus involving cortical veins. World Neurosurg. 2012;82:169.

    Article  PubMed  Google Scholar 

  181. Rahal JP, Malek AM, Heilman CB. Toward a better model of cerebral venous sinus thrombosis. World Neurosurg. 2014;82:50.

    Article  PubMed  Google Scholar 

  182. Wang J, Ji X, Ling F, Luo Y, He X, Guo M, Li S, Miao Z, Zhu F, Xuan Y. A new model of reversible superior sagittal sinus thrombosis in rats. Brain Res. 2007;1181:118–24.

    Article  CAS  PubMed  Google Scholar 

  183. Rottger C, Bachmann G, Gerriets T, Kaps M, Kuchelmeister K, Schachenmayr W, Walberer M, Wessels T, Stolz E. A new model of reversible sinus sagittalis superior thrombosis in the rat: magnetic resonance imaging changes. Neurosurgery. 2005;57:573–80; discussion 573-580.

    Article  PubMed  Google Scholar 

  184. Wang J, Tan HQ, Li MH, Sun XJ, Fu CM, Zhu YQ, Zhou B, Xu HW, Wang W, Xue B. Development of a new model of transvenous thrombosis in the pig superior sagittal sinus using thrombin injection and balloon occlusion. J Neuroradiol. 2010;37:109–15.

    Article  CAS  PubMed  Google Scholar 

  185. Miyamoto K, Heimann A, Kempski O. Microcirculatory alterations in a Mongolian gerbil sinus-vein thrombosis model. J Clin Neurosci. 2001;8(Suppl 1):97–105.

    Article  PubMed  Google Scholar 

  186. Nakase H, Kakizaki T, Miyamoto K, Hiramatsu K, Sakaki T. Use of local cerebral blood flow monitoring to predict brain damage after disturbance to the venous circulation: cortical vein occlusion model by photochemical dye. Neurosurgery. 1995;37:280–5; discussion 285-286.

    Article  CAS  PubMed  Google Scholar 

  187. Takeshima Y, Nakamura M, Miyake H, Tamaki R, Inui T, Horiuchi K, Wajima D, Nakase H. Neuroprotection with intraventricular brain-derived neurotrophic factor in rat venous occlusion model. Neurosurgery. 2011;68:1334–41.

    Article  PubMed  Google Scholar 

  188. Wajima D, Nakamura M, Horiuchi K, Miyake H, Takeshima Y, Tamura K, Motoyama Y, Konishi N, Nakase H. Enhanced cerebral ischemic lesions after two-vein occlusion in diabetic rats. Brain Res. 2010;1309:126–35.

    Article  CAS  PubMed  Google Scholar 

  189. Aydin K, Cokluk C, Ayas B, Onger ME, Keskin I, Ozyasar A, Aslan H, Kaplan S. Hippocampal cell loss after an anterior and posterior anastomotic vein occlusion model in rats. Int J Dev Neurosci. 2011;29:717–22.

    Article  PubMed  Google Scholar 

  190. Cokluk C, Aydin K, Korkmaz A, Senel A, Iyigun O, Onder A. A model of unilateral cerebral anterior and posterior anastomotic vein occlusion in the rat. Minim Invasive Neurosurg. 2005;48:149–53.

    Article  CAS  PubMed  Google Scholar 

  191. Cokluk C, Aydin K, Yemisci M, Colakoglu S, Kaplan S. Cortical anastomotic veins occlusion in the rat including the assessment of cerebral swelling. J Neurosci Methods. 2006;156:203–10.

    Article  PubMed  Google Scholar 

  192. Lavoie P, Metellus P, Velly L, Vidal V, Rolland PH, Mekaouche M, Dubreuil G, Levrier O. Functional cerebral venous outflow in swine and baboon: feasibility of an intracranial venous hypertension model. J Invest Surg. 2008;21:323–9.

    Article  PubMed  Google Scholar 

  193. Kojima T, Miyachi S, Sahara Y, Nakai K, Okamoto T, Hattori K, Kobayashi N, Hattori K, Negoro M, Yoshida J. The relationship between venous hypertension and expression of vascular endothelial growth factor: hemodynamic and immunohistochemical examinations in a rat venous hypertension model. Surg Neurol. 2007;68:277–84; discussion 284.

    Article  PubMed  Google Scholar 

  194. Yamada M, Yuzawa I, Fujii K, Miyasaka Y. Chronic cerebral venous hypertension model in rats. Neurol Res. 2003;25:694–6.

    Article  PubMed  Google Scholar 

  195. Chaigneau E, Oheim M, Audinat E, Charpak S. Two-photon imaging of capillary blood flow in olfactory bulb glomeruli. Proc Natl Acad Sci U S A. 2003;100:13081–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  196. Lecoq J, Parpaleix A, Roussakis E, Ducros M, Goulam Houssen Y, Vinogradov SA, Charpak S. Simultaneous two-photon imaging of oxygen and blood flow in deep cerebral vessels. Nat Med. 2011;17:893–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  197. Parpaleix A, Goulam Houssen Y, Charpak S. Imaging local neuronal activity by monitoring PO(2) transients in capillaries. Nat Med. 2013;19:241–6.

    Article  CAS  PubMed  Google Scholar 

  198. Shih AY, Driscoll JD, Drew PJ, Nishimura N, Schaffer CB, Kleinfeld D. Two-photon microscopy as a tool to study blood flow and neurovascular coupling in the rodent brain. J Cereb Blood Flow Metab. 2012;32:1277–309.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  199. Groner W, Winkelman JW, Harris AG, Ince C, Bouma GJ, Messmer K, Nadeau RG. Orthogonal polarization spectral imaging: a new method for study of the microcirculation. Nat Med. 1999;5:1209–12.

    Article  CAS  PubMed  Google Scholar 

  200. 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 

  201. Thomale UW, Schaser KD, Unterberg AW, Stover JF. Visualization of rat pial microcirculation using the novel orthogonal polarized spectral (OPS) imaging after brain injury. J Neurosci Methods. 2001;108:85–90.

    Article  CAS  PubMed  Google Scholar 

  202. Zamboni P, Sisini F, Menegatti E, Taibi A, Malagoni AM, Morovic S, Gambaccini M. An ultrasound model to calculate the brain blood outflow through collateral vessels: a pilot study. BMC Neurol. 2013;13:81.

    Article  PubMed  PubMed Central  Google Scholar 

  203. van Raaij ME, Lindvere L, Dorr A, He J, Sahota B, Foster FS, Stefanovic B. Quantification of blood flow and volume in arterioles and venules of the rat cerebral cortex using functional micro-ultrasound. NeuroImage. 2012;63:1030–7.

    Article  PubMed  Google Scholar 

  204. Zamboni P, Menegatti E, Conforti P, Shepherd S, Tessari M, Beggs C. Assessment of cerebral venous return by a novel plethysmography method. J Vasc Surg. 2012;56:677–685.e671.

    Article  PubMed  Google Scholar 

  205. Langheinrich AC, Yeniguen M, Ostendorf A, Marhoffer S, Dierkes C, von Gerlach S, Nedelmann M, Kampschulte M, Bachmann G, Stolz E, Gerriets T. In vitro evaluation of the sinus sagittalis superior thrombosis model in the rat using 3D micro- and nanocomputed tomography. Neuroradiology. 2010;52:815–21.

    Article  PubMed  Google Scholar 

  206. Tsui YK, Tsai FY, Hasso AN, Greensite F, Nguyen BV. Susceptibility-weighted imaging for differential diagnosis of cerebral vascular pathology: a pictorial review. J Neurol Sci. 2009;287:7–16.

    Article  PubMed  Google Scholar 

  207. Liebeskind DS. Collateral circulation. Stroke. 2003;34:2279–84.

    Article  PubMed  Google Scholar 

  208. Albers GW. Impact of recanalization, reperfusion, and collateral flow on clinical efficacy. Stroke. 2013;44:S11–2.

    Article  PubMed  Google Scholar 

  209. Marks MP, Lansberg MG, Mlynash M, Olivot JM, Straka M, Kemp S, McTaggart R, Inoue M, Zaharchuk G, Bammer R, Albers GW, Diffusion and Perfusion Imaging Evaluation for Understanding Stroke Evolution 2 Investigators. Effect of collateral blood flow on patients undergoing endovascular therapy for acute ischemic stroke. Stroke. 2014;45:1035–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  210. Pandey AS, Thompson BG, Gemmete JJ, Chaudhary N. Cerebral collateral circulation: integral to defining clinical outcome in acute cerebral ischemia. World Neurosurg. 2012;77:240–2.

    Article  PubMed  Google Scholar 

  211. Ramakrishnan G, Dong B, Todd KG, Shuaib A, Winship IR. Transient aortic occlusion augments collateral blood flow and reduces mortality during severe ischemia due to proximal middle cerebral artery occlusion. Transl Stroke Res. 2016;7:149–55.

    Article  CAS  PubMed  Google Scholar 

  212. Shuaib A, Butcher K, Mohammad AA, Saqqur M, Liebeskind DS. Collateral blood vessels in acute ischaemic stroke: a potential therapeutic target. Lancet Neurol. 2011;10:909–21.

    Article  PubMed  Google Scholar 

  213. Winship IR. Cerebral collaterals and collateral therapeutics for acute ischemic stroke. Microcirculation. 2015;22:228–36.

    Article  PubMed  Google Scholar 

  214. Yeo LL, Paliwal P, Low AF, Tay EL, Gopinathan A, Nadarajah M, Ting E, Venketasubramanian N, Seet RC, Ahmad A, Chan BP, Teoh HL, Soon D, Rathakrishnan R, Sharma VK. How temporal evolution of intracranial collaterals in acute stroke affects clinical outcomes. Neurology. 2016;86:434–41.

    Article  PubMed  PubMed Central  Google Scholar 

  215. Edwards EA. Scope and limitations of collateral circulation. Presidential address. Arch Surg. 1984;119:761–5.

    Article  CAS  PubMed  Google Scholar 

  216. Bullock R, Mendelow AD, Bone I, Patterson J, Macleod WN, Allardice G. Cerebral blood flow and CO2 responsiveness as an indicator of collateral reserve capacity in patients with carotid arterial disease. Br J Surg. 1985;72:348–51.

    Article  CAS  PubMed  Google Scholar 

  217. Katz I, Palgen M, Murdock J, Martin AR, Farjot G, Caillibotte G. Gas transport during in vitro and in vivo preclinical testing of inert gas therapies. Med Gas Res. 2016;6:14–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  218. Coyle P. Interruption of the middle cerebral artery in 10-day-old rat alters normal development of distal collaterals. Anat Rec. 1985;212:179–82.

    Article  CAS  PubMed  Google Scholar 

  219. Coyle P, Heistad DD. Blood flow through cerebral collateral vessels one month after middle cerebral artery occlusion. Stroke. 1987;18:407–11.

    Article  CAS  PubMed  Google Scholar 

  220. Wei L, Erinjeri JP, Rovainen CM, Woolsey TA. Collateral growth and angiogenesis around cortical stroke. Stroke. 2001;32:2179–84.

    Article  CAS  PubMed  Google Scholar 

  221. Matsushima Y, Inaba Y. The specificity of the collaterals to the brain through the study and surgical treatment of moyamoya disease. Stroke. 1986;17:117–22.

    Article  CAS  PubMed  Google Scholar 

  222. Rosengren K. Moya-Moya vessels. Collateral arteries of the basal ganglia. Malignant occlusion of the anterior cerebral arteries. Acta Radiol Diagn (Stockh). 1974;15:145–51.

    Article  CAS  Google Scholar 

  223. Andeweg J. The anatomy of collateral venous flow from the brain and its value in aetiological interpretation of intracranial pathology. Neuroradiology. 1996;38:621–8.

    Article  CAS  PubMed  Google Scholar 

  224. Mikhailov SS, Kagan II. The anastomoses of the venous system of the brain and their role in the collateral circulation. Folia Morphol (Praha). 1968;16:10–8.

    CAS  Google Scholar 

  225. Barboza MA, Mejias C, Colin-Luna J, Quiroz-Compean A, Arauz A. Intracranial venous collaterals in cerebral venous thrombosis: clinical and imaging impact. J Neurol Neurosurg Psychiatry. 2015;86:1314–8.

    Article  PubMed  Google Scholar 

  226. Zamboni P, Consorti G, Galeotti R, Gianesini S, Menegatti E, Tacconi G, Carinci F. Venous collateral circulation of the extracranial cerebrospinal outflow routes. Curr Neurovasc Res. 2009;6:204–12.

    Article  PubMed  Google Scholar 

  227. Liebeskind DS. Reperfusion for acute ischemic stroke: arterial revascularization and collateral therapeutics. Curr Opin Neurol. 2010;23:36–45.

    Article  PubMed  Google Scholar 

  228. Bang OY, Saver JL, Kim SJ, Kim GM, Chung CS, Ovbiagele B, Lee KH, Liebeskind DS. Collateral flow predicts response to endovascular therapy for acute ischemic stroke. Stroke. 2011;42:693–9.

    Article  PubMed  PubMed Central  Google Scholar 

  229. Bang OY, Saver JL, Kim SJ, Kim GM, Chung CS, Ovbiagele B, Lee KH, Liebeskind DS, UCLA-Samsung Stroke Collaborators. Collateral flow averts hemorrhagic transformation after endovascular therapy for acute ischemic stroke. Stroke. 2011;42:2235–9.

    Article  PubMed  Google Scholar 

  230. Weber J, Vida M, Greiner K. Sagittal sinus thrombosis with malignant brain oedema: pathophysiology of cortical veins after decompressive craniectomy. Acta Neurochir. 2013;155:651–3.

    Article  PubMed  Google Scholar 

  231. Miteff F, Levi CR, Bateman GA, Spratt N, McElduff P, Parsons MW. The independent predictive utility of computed tomography angiographic collateral status in acute ischaemic stroke. Brain. 2009;132:2231–8.

    Article  PubMed  Google Scholar 

  232. Ma J, Ma Y, Dong B, Bandet MV, Shuaib A, Winship IR. Prevention of the collapse of pial collaterals by remote ischemic perconditioning during acute ischemic stroke. J Cereb Blood Flow Metab. 2017;37:3001.

    Article  PubMed  Google Scholar 

  233. Qiu ZD, Deng G, Yang J, Min Z, Li DY, Fang Y, Zhang SM. A new method for evaluating regional cerebral blood flow changes: laser speckle contrast imaging in a C57BL/6J mouse model of photothrombotic ischemia. J Huazhong Univ Sci Technolog Med Sci. 2016;36:174–80.

    Article  CAS  PubMed  Google Scholar 

  234. Schaffer CB, Friedman B, Nishimura N, Schroeder LF, Tsai PS, Ebner FF, Lyden PD, Kleinfeld D. Two-photon imaging of cortical surface microvessels reveals a robust redistribution in blood flow after vascular occlusion. PLoS Biol. 2006;4:e22.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  235. Yuan F, Lin X, Guan Y, Mu Z, Chen K, Wang Y, Yang GY. Collateral circulation prevents masticatory muscle impairment in rat middle cerebral artery occlusion model. J Synchrotron Radiat. 2014;21:1314–8.

    Article  PubMed  Google Scholar 

  236. Zhang M, Peng G, Sun D, Xie Y, Xia J, Long H, Hu K, Xiao B. Synchrotron radiation imaging is a powerful tool to image brain microvasculature. Med Phys. 2014;41:031907.

    Article  PubMed  Google Scholar 

  237. Li A, Gong H, Zhang B, Wang Q, Yan C, Wu J, Liu Q, Zeng S, Luo Q. Micro-optical sectioning tomography to obtain a high-resolution atlas of the mouse brain. Science. 2010;330:1404–8.

    Article  CAS  PubMed  Google Scholar 

  238. Xue S, Gong H, Jiang T, Luo W, Meng Y, Liu Q, Chen S, Li A. Indian-ink perfusion based method for reconstructing continuous vascular networks in whole mouse brain. PLoS One. 2014;9:e88067.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  239. Moss G. The adequacy of the cerebral collateral circulation: tolerance of awake experimental animals to acute bilateral common carotid artery occlusion. J Surg Res. 1974;16:337–8.

    Article  CAS  PubMed  Google Scholar 

  240. Shimizu F, Sano Y, Maeda T, Abe MA, Nakayama H, Takahashi R, Ueda M, Ohtsuki S, Terasaki T, Obinata M, Kanda T. Peripheral nerve pericytes originating from the blood-nerve barrier expresses tight junctional molecules and transporters as barrier-forming cells. J Cell Physiol. 2008;217:388–99.

    Article  CAS  PubMed  Google Scholar 

  241. Altay O, Suzuki H, Hasegawa Y, Caner B, Krafft PR, Fujii M, Tang J, Zhang JH. Isoflurane attenuates blood-brain barrier disruption in ipsilateral hemisphere after subarachnoid hemorrhage in mice. Stroke. 2012;43:2513–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  242. Suzuki H, Hasegawa Y, Kanamaru K, Zhang JH. Mechanisms of osteopontin-induced stabilization of blood-brain barrier disruption after subarachnoid hemorrhage in rats. Stroke. 2010;41:1783–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  243. Yan J, Manaenko A, Chen S, Klebe D, Ma Q, Caner B, Fujii M, Zhou C, Zhang JH. Role of SCH79797 in maintaining vascular integrity in rat model of subarachnoid hemorrhage. Stroke. 2013;44:1410–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  244. Zhan Y, Krafft PR, Lekic T, Ma Q, Souvenir R, Zhang JH, Tang J. Imatinib preserves blood-brain barrier integrity following experimental subarachnoid hemorrhage in rats. J Neurosci Res. 2015;93:94–103.

    Article  CAS  PubMed  Google Scholar 

  245. Chen Y, Zhang Y, Tang J, Liu F, Hu Q, Luo C, Tang J, Feng H, Zhang JH. Norrin protected blood-brain barrier via frizzled-4/beta-catenin pathway after subarachnoid hemorrhage in rats. Stroke. 2015;46:529–36.

    Article  CAS  PubMed  Google Scholar 

  246. Greif DM, Eichmann A. Vascular biology: brain vessels squeezed to death. Nature. 2014;508:50–1.

    Article  CAS  PubMed  Google Scholar 

  247. O’Farrell FM, Attwell D. A role for pericytes in coronary no-reflow. Nat Rev Cardiol. 2014;11:427–32.

    Article  PubMed  Google Scholar 

  248. 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.

    Article  CAS  PubMed  Google Scholar 

  249. Ohkuma H, Itoh K, Shibata S, Suzuki S. Morphological changes of intraparenchymal arterioles after experimental subarachnoid hemorrhage in dogs. Neurosurgery. 1997;41:230–5; discussion 235-236.

    Article  CAS  PubMed  Google Scholar 

  250. Li Q, Chen Y, Li B, Luo C, Zuo S, Liu X, Zhang JH, Ruan H, Feng H. Hemoglobin induced NO/cGMP suppression deteriorate microcirculation via pericyte phenotype transformation after subarachnoid hemorrhage in rats. Sci Rep. 2016;6:22070.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  251. Obermeier B, Daneman R, Ransohoff RM. Development, maintenance and disruption of the blood-brain barrier. Nat Med. 2013;19:1584–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  252. Spokoyny I, Raman R, Ernstrom K, Demaerschalk BM, Lyden PD, Hemmen TM, Guzik AK, Chen JY, Meyer BC. Pooled assessment of computed tomography interpretation by vascular neurologists in the STRokE DOC telestroke network. J Stroke Cerebrovasc Dis. 2014;23:511–5.

    Article  PubMed  Google Scholar 

  253. Hagedorn M, Balke M, Schmidt A, Bloch W, Kurz H, Javerzat S, Rousseau B, Wilting J, Bikfalvi A. VEGF coordinates interaction of pericytes and endothelial cells during vasculogenesis and experimental angiogenesis. Dev Dyn. 2004;230:23–33.

    Article  CAS  PubMed  Google Scholar 

  254. Sinha S, Hoofnagle MH, Kingston PA, McCanna ME, Owens GK. Transforming growth factor-beta1 signaling contributes to development of smooth muscle cells from embryonic stem cells. Am J Physiol Cell Physiol. 2004;287:C1560–8.

    Article  CAS  PubMed  Google Scholar 

  255. Gaengel K, Genove G, Armulik A, Betsholtz C. Endothelial-mural cell signaling in vascular development and angiogenesis. Arterioscler Thromb Vasc Biol. 2009;29:630–8.

    Article  CAS  PubMed  Google Scholar 

  256. Cai W, Liu H, Zhao J, Chen LY, Chen J, Lu Z, Hu X. Pericytes in brain injury and repair after ischemic stroke. Transl Stroke Res. 2017;8:107.

    Article  CAS  PubMed  Google Scholar 

  257. Kloc M, Kubiak JZ, Li XC, Ghobrial RM. Pericytes, microvasular dysfunction, and chronic rejection. Transplantation. 2015;99:658–67.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  258. Arboleda-Velasquez JF, Valdez CN, Marko CK, D’Amore PA. From pathobiology to the targeting of pericytes for the treatment of diabetic retinopathy. Curr Diab Rep. 2015;15:573.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  259. Glinskii OV, Huxley VH, Glinskii VV, Rubin LJ, Glinsky VV. Pulsed estrogen therapy prevents post-OVX porcine dura mater microvascular network weakening via a PDGF-BB-dependent mechanism. PLoS One. 2013;8:e82900.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  260. Contard F, Sabri A, Glukhova M, Sartore S, Marotte F, Pomies JP, Schiavi P, Guez D, Samuel JL, Rappaport L. Arterial smooth muscle cell phenotype in stroke-prone spontaneously hypertensive rats. Hypertension. 1993;22:665–76.

    Article  CAS  PubMed  Google Scholar 

  261. Wu J, Zhang Y, Yang P, Enkhjargal B, Manaenko A, Tang J, Pearce WJ, Hartman R, Obenaus A, Chen G, Zhang JH. Recombinant osteopontin stabilizes smooth muscle cell phenotype via integrin receptor/integrin-linked kinase/Rac-1 pathway after subarachnoid hemorrhage in rats. Stroke. 2016;47:1319–27.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  262. Lee MH, Kwon BJ, Seo HJ, Yoo KE, Kim MS, Koo MA, Park JC. Resveratrol inhibits phenotype modulation by platelet derived growth factor-bb in rat aortic smooth muscle cells. Oxidative Med Cell Longev. 2014;2014:572430.

    Google Scholar 

  263. Miyata T, Iizasa H, Sai Y, Fujii J, Terasaki T, Nakashima E. Platelet-derived growth factor-BB (PDGF-BB) induces differentiation of bone marrow endothelial progenitor cell-derived cell line TR-BME2 into mural cells, and changes the phenotype. J Cell Physiol. 2005;204:948–55.

    Article  CAS  PubMed  Google Scholar 

  264. Chimori Y, Hayashi K, Kimura K, Nishida W, Funahashi S, Miyata S, Shimane M, Matsuzawa Y, Sobue K. Phenotype-dependent expression of cadherin 6B in vascular and visceral smooth muscle cells. FEBS Lett. 2000;469:67–71.

    Article  CAS  PubMed  Google Scholar 

  265. Griswold CK. A model of the physiological basis of a multivariate phenotype that is mediated by Ca(2+) signaling and controlled by ryanodine receptor composition. J Theor Biol. 2011;282:14–22.

    Article  CAS  PubMed  Google Scholar 

  266. Munot P, Saunders DE, Milewicz DM, Regalado ES, Ostergaard JR, Braun KP, Kerr T, Lichtenbelt KD, Philip S, Rittey C, Jacques TS, Cox TC, Ganesan V. A novel distinctive cerebrovascular phenotype is associated with heterozygous Arg179 ACTA2 mutations. Brain. 2012;135:2506–14.

    Article  PubMed  PubMed Central  Google Scholar 

  267. Chazalviel L, Haelewyn B, Degoulet M, Blatteau JE, Vallee N, Risso JJ, Besnard S, Abraini JH. Hyperbaric oxygen increases tissue-plasminogen activator-induced thrombolysis in vitro, and reduces ischemic brain damage and edema in rats subjected to thromboembolic brain ischemia. Med Gas Res. 2016;6:64–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  268. Henninger N, Fisher M. Extending the time window for endovascular and pharmacological reperfusion. Transl Stroke Res. 2016;7:284–93.

    Article  CAS  PubMed  Google Scholar 

  269. Ovbiagele B, Saver JL, Starkman S, Kim D, Ali LK, Jahan R, Duckwiler GR, Vinuela F, Pineda S, Liebeskind DS. Statin enhancement of collateralization in acute stroke. Neurology. 2007;68:2129–31.

    Article  CAS  PubMed  Google Scholar 

  270. Lucitti JL, Tarte NJ, Faber JE. Chloride intracellular channel 4 is required for maturation of the cerebral collateral circulation. Am J Physiol Heart Circ Physiol. 2015;309:H1141–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  271. Chalothorn D, Zhang H, Smith JE, Edwards JC, Faber JE. Chloride intracellular channel-4 is a determinant of native collateral formation in skeletal muscle and brain. Circ Res. 2009;105:89–98.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  272. Harrigan MR, Ennis SR, Masada T, Keep RF. Intraventricular infusion of vascular endothelial growth factor promotes cerebral angiogenesis with minimal brain edema. Neurosurgery. 2002;50:589–98.

    PubMed  Google Scholar 

  273. Harrigan MR, Ennis SR, Sullivan SE, Keep RF. Effects of intraventricular infusion of vascular endothelial growth factor on cerebral blood flow, edema, and infarct volume. Acta Neurochir. 2003;145:49–53.

    Article  CAS  PubMed  Google Scholar 

  274. Shimazu T, Inoue I, Araki N, Asano Y, Sawada M, Furuya D, Nagoya H, Greenberg JH. A peroxisome proliferator-activated receptor-gamma agonist reduces infarct size in transient but not in permanent ischemia. Stroke. 2005;36:353–9.

    Article  CAS  PubMed  Google Scholar 

  275. Culman J, Nguyen-Ngoc M, Glatz T, Gohlke P, Herdegen T, Zhao Y. Treatment of rats with pioglitazone in the reperfusion phase of focal cerebral ischemia: a preclinical stroke trial. Exp Neurol. 2012;238:243–53.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the National Institutes of Health (P01 NS082184, R01 NS081740, and R01 NS091042 to John H. Zhang), the National Basic Research Program of China (973 Program, 2014CB541600 to Hua Feng), the Major Technology Innovation Project of Southwest Hospital (SWH2016ZDCX1011 to Hua Feng) and the National Natural Science Foundation of China (81220108009 to Hua Feng, 81501002 to Yujie Chen).

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Chen, Y. et al. (2019). Neurovascular Network as Future Therapeutic Targets. In: Lou, M., et al. Cerebral Venous System in Acute and Chronic Brain Injuries. Springer Series in Translational Stroke Research. Springer, Cham. https://doi.org/10.1007/978-3-319-96053-1_1

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