Advertisement

Neurovascular Network as Future Therapeutic Targets

  • Yujie Chen
  • Yang Zhang
  • Zhenni Guo
  • Ling Liu
  • Feng Gao
  • Yanfeng Lv
  • Meng Zhang
  • Xiaochuan Sun
  • Andre Obenaus
  • Yi Yang
  • Jiping Tang
  • Hua Feng
  • John H. Zhang
Chapter
Part of the Springer Series in Translational Stroke Research book series (SSTSR)

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.

Keywords

Neurovascular network Cerebral veins Stroke 

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

Notes

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).

Conflict of Interest

The authors declare that there are no conflicts of interest.

References

  1. 1.
    Paciaroni M, Bogousslavsky J. How did stroke become of interest to neurologists?: a slow 19th century saga. Neurology. 2009;73:724–8.PubMedCrossRefPubMedCentralGoogle Scholar
  2. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  3. 3.
    Eckert B. Acute stroke therapy 1981-2009. Klin Neuroradiol. 2009;19:8–19.PubMedCrossRefPubMedCentralGoogle Scholar
  4. 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.CrossRefGoogle Scholar
  5. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  6. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  7. 7.
    del Zoppo GJ. Stroke and neurovascular protection. N Engl J Med. 2006;354:553–5.PubMedCrossRefPubMedCentralGoogle Scholar
  8. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  9. 9.
    Iadecola C, Anrather J. Stroke research at a crossroad: asking the brain for directions. Nat Neurosci. 2011;14:1363–8.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Xing C, Hayakawa K, Lok J, Arai K, Lo EH. Injury and repair in the neurovascular unit. Neurol Res. 2012;34:325–30.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Xing C, Lo EH. Help-me signaling: non-cell autonomous mechanisms of neuroprotection and neurorecovery. Prog Neurobiol. 2017;152:181.PubMedCrossRefGoogle Scholar
  12. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  14. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Li Q, Khatibi N, Zhang JH. Vascular neural network: the importance of vein drainage in stroke. Transl Stroke Res. 2014;5:163–6.PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Yin Y, Ge H, Zhang JH, Feng H. Targeting vascular neural network in intracerebral hemorrhage. Curr Pharm Des. 2017;23:2197.PubMedCrossRefPubMedCentralGoogle Scholar
  17. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 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.Google Scholar
  19. 19.
    Xing C, Hayakawa K, Lo EH. Mechanisms, imaging, and therapy in stroke recovery. Transl Stroke Res. 2017;8:1.PubMedCrossRefGoogle Scholar
  20. 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.PubMedCrossRefGoogle Scholar
  21. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Zhai WW, Sun L, Yu ZQ, Chen G. Hyperbaric oxygen therapy in experimental and clinical stroke. Med Gas Res. 2016;6:111–8.PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Linfante I, Cipolla MJ. Improving reperfusion therapies in the era of mechanical thrombectomy. Transl Stroke Res. 2016;7:294–302.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Pound P, Bury M, Ebrahim S. From apoplexy to stroke. Age Ageing. 1997;26:331–7.PubMedCrossRefGoogle Scholar
  27. 27.
    Schiller F. Concepts of stroke before and after Virchow. Med Hist. 1970;14:115–31.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 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.PubMedCrossRefGoogle Scholar
  29. 29.
    del Zoppo GJ. The neurovascular unit in the setting of stroke. J Intern Med. 2010;267:156–71.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Iadecola C. Neurovascular regulation in the normal brain and in Alzheimer’s disease. Nat Rev Neurosci. 2004;5:347–60.CrossRefGoogle Scholar
  31. 31.
    Lo EH, Broderick JP, Moskowitz MA. tPA and proteolysis in the neurovascular unit. Stroke. 2004;35:354–6.PubMedCrossRefGoogle Scholar
  32. 32.
    McHedlishvili G. Physiological mechanisms controlling cerebral blood flow. Stroke. 1980;11:240–8.PubMedCrossRefPubMedCentralGoogle Scholar
  33. 33.
    Hallenbeck JM, Bradley ME. Experimental model for systematic study of impaired microvascular reperfusion. Stroke. 1977;8:238–43.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  35. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  36. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  37. 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.PubMedPubMedCentralGoogle Scholar
  38. 38.
    Andeweg J. Consequences of the anatomy of deep venous outflow from the brain. Neuroradiology. 1999;41:233–41.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Kilic T, Akakin A. Anatomy of cerebral veins and sinuses. Front Neurol Neurosci. 2008;23:4–15.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Schmidek HH, Auer LM, Kapp JP. The cerebral venous system. Neurosurgery. 1985;17:663–78.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 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.PubMedCrossRefGoogle Scholar
  42. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Allt G, Lawrenson JG. Pericytes: cell biology and pathology. Cells Tissues Organs. 2001;169:1–11.PubMedCrossRefPubMedCentralGoogle Scholar
  44. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Tso MK, Macdonald RL. Acute microvascular changes after subarachnoid hemorrhage and transient global cerebral ischemia. Stroke Res Treat. 2013;2013:425281.PubMedPubMedCentralGoogle Scholar
  46. 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.PubMedCrossRefGoogle Scholar
  47. 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.PubMedCrossRefGoogle Scholar
  48. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Matsugi T, Chen Q, Anderson DR. Contractile responses of cultured bovine retinal pericytes to angiotensin II. Arch Ophthalmol. 1997;115:1281–5.PubMedCrossRefGoogle Scholar
  50. 50.
    Murphy DD, Wagner RC. Differential contractile response of cultured microvascular pericytes to vasoactive agents. Microcirculation. 1994;1:121–8.PubMedCrossRefGoogle Scholar
  51. 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.PubMedCrossRefGoogle Scholar
  52. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 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.PubMedCrossRefGoogle Scholar
  54. 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.PubMedGoogle Scholar
  55. 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.PubMedCrossRefGoogle Scholar
  56. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Anderson DR, Davis EB. Glaucoma, capillaries and pericytes. 5. Preliminary evidence that carbon dioxide relaxes pericyte contractile tone. Ophthalmologica. 1996;210:280–4.PubMedCrossRefPubMedCentralGoogle Scholar
  58. 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.PubMedPubMedCentralGoogle Scholar
  59. 59.
    Oishi K, Kamiyashiki T, Ito Y. Isometric contraction of microvascular pericytes from mouse brain parenchyma. Microvasc Res. 2007;73:20–8.PubMedCrossRefPubMedCentralGoogle Scholar
  60. 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.PubMedCrossRefGoogle Scholar
  61. 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.PubMedCrossRefGoogle Scholar
  62. 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.PubMedGoogle Scholar
  63. 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.PubMedCrossRefGoogle Scholar
  64. 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.PubMedCrossRefGoogle Scholar
  65. 65.
    Ramachandran E, Frank RN, Kennedy A. Effects of endothelin on cultured bovine retinal microvascular pericytes. Invest Ophthalmol Vis Sci. 1993;34:586–95.PubMedGoogle Scholar
  66. 66.
    Gillies MC, Su T. High glucose inhibits retinal capillary pericyte contractility in vitro. Invest Ophthalmol Vis Sci. 1993;34:3396–401.PubMedGoogle Scholar
  67. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  68. 68.
    Miller FN, Sims DE. Contractile elements in the regulation of macromolecular permeability. Fed Proc. 1986;45:84–8.PubMedGoogle Scholar
  69. 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.PubMedCrossRefGoogle Scholar
  70. 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.PubMedPubMedCentralGoogle Scholar
  71. 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.PubMedPubMedCentralGoogle Scholar
  72. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  73. 73.
    Pearce WJ, Bevan JA. Retroglenoid venoconstriction and its influence on canine intracranial venous pressures. J Cereb Blood Flow Metab. 1984;4:373–80.PubMedCrossRefPubMedCentralGoogle Scholar
  74. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  75. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  76. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  77. 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.PubMedPubMedCentralGoogle Scholar
  78. 78.
    Little JR, Kerr FWL, Sundt TM. Microcirculatory obstruction in focal cerebral ischemia: an electron microscopic investigation in monkeys. Stroke. 1976;7:25–30.CrossRefGoogle Scholar
  79. 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.PubMedCrossRefGoogle Scholar
  80. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  81. 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.PubMedPubMedCentralGoogle Scholar
  82. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  83. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  84. 84.
    Dalkara T, Arsava EM. Can restoring incomplete microcirculatory reperfusion improve stroke outcome after thrombolysis? J Cereb Blood Flow Metab. 2012;32:2091–9.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  86. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  88. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  89. 89.
    Paciaroni M, Caso V, Agnelli G. The concept of ischemic penumbra in acute stroke and therapeutic opportunities. Eur Neurol. 2009;61:321–30.PubMedCrossRefPubMedCentralGoogle Scholar
  90. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    Nemoto EM. Dynamics of cerebral venous and intracranial pressures. Acta Neurochir Suppl. 2006;96:435–7.PubMedCrossRefPubMedCentralGoogle Scholar
  92. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  93. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  94. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Rahemtullah A, Van Cott EM. Hypercoagulation testing in ischemic stroke. Arch Pathol Lab Med. 2007;131:890–901.PubMedPubMedCentralGoogle Scholar
  96. 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.CrossRefGoogle Scholar
  97. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  98. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  99. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  100. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  101. 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.PubMedCrossRefGoogle Scholar
  102. 102.
    Xi G, Keep RF, Hoff JT. Mechanisms of brain injury after intracerebral haemorrhage. Lancet Neurol. 2006;5:53–63.CrossRefGoogle Scholar
  103. 103.
    Diringer MN. Intracerebral hemorrhage: pathophysiology and management. Crit Care Med. 1993;21:1591–603.PubMedCrossRefGoogle Scholar
  104. 104.
    Prabhakaran S, Naidech AM. Ischemic brain injury after intracerebral hemorrhage: a critical review. Stroke. 2012;43:2258–63.PubMedCrossRefGoogle Scholar
  105. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  106. 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.PubMedCrossRefGoogle Scholar
  107. 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.PubMedCrossRefGoogle Scholar
  108. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  109. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  110. 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.PubMedCrossRefGoogle Scholar
  111. 111.
    Ziai WC. Hematology and inflammatory signaling of intracerebral hemorrhage. Stroke. 2013;44:S74–8.PubMedCrossRefGoogle Scholar
  112. 112.
    Wang J. Preclinical and clinical research on inflammation after intracerebral hemorrhage. Prog Neurobiol. 2010;92:463–77.PubMedPubMedCentralCrossRefGoogle Scholar
  113. 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.PubMedCrossRefGoogle Scholar
  114. 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.PubMedCrossRefGoogle Scholar
  115. 115.
    Etminan N. Aneurysmal subarachnoid hemorrhage—status quo and perspective. Transl Stroke Res. 2015;6:167–70.PubMedCrossRefGoogle Scholar
  116. 116.
    Macdonald RL, Pluta RM, Zhang JH. Cerebral vasospasm after subarachnoid hemorrhage: the emerging revolution. Nat Clin Pract Neurol. 2007;3:256–63.PubMedCrossRefGoogle Scholar
  117. 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.PubMedCrossRefGoogle Scholar
  118. 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.PubMedCrossRefGoogle Scholar
  119. 119.
    Cahill J, Zhang JH. Subarachnoid hemorrhage: is it time for a new direction? Stroke. 2009;40:S86–7.PubMedCrossRefGoogle Scholar
  120. 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.PubMedCrossRefGoogle Scholar
  121. 121.
    Suzuki H. What is early brain injury? Transl Stroke Res. 2015;6:1–3.PubMedCrossRefGoogle Scholar
  122. 122.
    Lo EH, Rosenberg GA. The neurovascular unit in health and disease: introduction. Stroke. 2009;40:S2–3.PubMedCrossRefGoogle Scholar
  123. 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.PubMedCrossRefGoogle Scholar
  124. 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.PubMedCrossRefGoogle Scholar
  125. 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. 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.PubMedCrossRefGoogle Scholar
  127. 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.PubMedCrossRefGoogle Scholar
  128. 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.PubMedCrossRefGoogle Scholar
  129. 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.PubMedCrossRefGoogle Scholar
  130. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  131. 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.PubMedCrossRefGoogle Scholar
  132. 132.
    Cahill J, Calvert JW, Zhang JH. Mechanisms of early brain injury after subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2006;26:1341–53.PubMedCrossRefGoogle Scholar
  133. 133.
    Sehba FA, Hou J, Pluta RM, Zhang JH. The importance of early brain injury after subarachnoid hemorrhage. Prog Neurobiol. 2012;97:14–37.PubMedPubMedCentralCrossRefGoogle Scholar
  134. 134.
    Okubo S, Strahle J, Keep RF, Hua Y, Xi G. Subarachnoid hemorrhage-induced hydrocephalus in rats. Stroke. 2013;44:547–50.PubMedCrossRefGoogle Scholar
  135. 135.
    Shah AH, Komotar RJ. Pathophysiology of acute hydrocephalus following subarachnoid hemorrhage. World Neurosurg. 2013;80:304.PubMedCrossRefGoogle Scholar
  136. 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.PubMedCrossRefGoogle Scholar
  137. 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.PubMedCrossRefGoogle Scholar
  138. 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. 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.PubMedCrossRefGoogle Scholar
  140. 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.PubMedGoogle Scholar
  141. 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.PubMedCrossRefGoogle Scholar
  142. 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.PubMedCrossRefGoogle Scholar
  143. 143.
    Mathews MS, Brown D, Brant-Zawadzki M. Perimesencephalic nonaneurysmal hemorrhage associated with vein of Galen stenosis. Neurology. 2008;70:2410–1.PubMedCrossRefGoogle Scholar
  144. 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.PubMedCrossRefGoogle Scholar
  145. 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.PubMedCrossRefGoogle Scholar
  146. 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.CrossRefGoogle Scholar
  147. 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.PubMedCrossRefGoogle Scholar
  148. 148.
    van der Schaaf IC, Velthuis BK, Gouw A, Rinkel GJ. Venous drainage in perimesencephalic hemorrhage. Stroke. 2004;35:1614–8.PubMedCrossRefGoogle Scholar
  149. 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.PubMedCrossRefGoogle Scholar
  150. 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.CrossRefGoogle Scholar
  151. 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.CrossRefGoogle Scholar
  152. 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.PubMedCrossRefGoogle Scholar
  153. 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.PubMedCrossRefGoogle Scholar
  154. 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.PubMedCrossRefGoogle Scholar
  155. 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.PubMedCrossRefGoogle Scholar
  156. 156.
    Prins M, Greco T, Alexander D, Giza CC. The pathophysiology of traumatic brain injury at a glance. Dis Model Mech. 2013;6:1307.PubMedPubMedCentralCrossRefGoogle Scholar
  157. 157.
    Arbour RB. Traumatic brain injury: pathophysiology, monitoring, and mechanism-based care. Crit Care Nurs Clin North Am. 2013;25:297–319.PubMedCrossRefGoogle Scholar
  158. 158.
    Mustafa AG, Alshboul OA. Pathophysiology of traumatic brain injury. Neurosciences (Riyadh). 2013;18:222–34.Google Scholar
  159. 159.
    Roth P, Farls K. Pathophysiology of traumatic brain injury. Crit Care Nurs Q. 2000;23:14–25; quiz 65.PubMedCrossRefGoogle Scholar
  160. 160.
    Werner C, Engelhard K. Pathophysiology of traumatic brain injury. Br J Anaesth. 2007;99:4–9.PubMedCrossRefGoogle Scholar
  161. 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.PubMedCrossRefGoogle Scholar
  162. 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.PubMedCrossRefGoogle Scholar
  163. 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.PubMedCrossRefGoogle Scholar
  164. 164.
    Maxwell WL, Irvine A, Adams JH, Graham DI, Gennarelli TA. Response of cerebral microvasculature to brain injury. J Pathol. 1988;155:327–35.PubMedCrossRefGoogle Scholar
  165. 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.PubMedGoogle Scholar
  166. 166.
    Chodobski A, Zink BJ, Szmydynger-Chodobska J. Blood-brain barrier pathophysiology in traumatic brain injury. Transl Stroke Res. 2011;2:492–516.PubMedPubMedCentralCrossRefGoogle Scholar
  167. 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.PubMedCrossRefGoogle Scholar
  168. 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.PubMedGoogle Scholar
  169. 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.PubMedCrossRefGoogle Scholar
  170. 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.PubMedCrossRefGoogle Scholar
  171. 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.PubMedCrossRefGoogle Scholar
  172. 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.PubMedCrossRefGoogle Scholar
  173. 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.PubMedCrossRefGoogle Scholar
  174. 174.
    Chung CP, Hu HH. Pathogenesis of leukoaraiosis: role of jugular venous reflux. Med Hypotheses. 2010;75:85–90.PubMedCrossRefGoogle Scholar
  175. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  176. 176.
    Sindou M, Auque J, Jouanneau E. Neurosurgery and the intracranial venous system. Acta Neurochir Suppl. 2005;94:167–75.PubMedCrossRefPubMedCentralGoogle Scholar
  177. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  178. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  179. 179.
    Mayhan WG, Werber AH, Heistad DD. Protection of cerebral vessels by sympathetic nerves and vascular hypertrophy. Circulation. 1987;75:I107–12.PubMedPubMedCentralGoogle Scholar
  180. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  181. 181.
    Rahal JP, Malek AM, Heilman CB. Toward a better model of cerebral venous sinus thrombosis. World Neurosurg. 2014;82:50.PubMedCrossRefPubMedCentralGoogle Scholar
  182. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  183. 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.CrossRefGoogle Scholar
  184. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  185. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  186. 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.CrossRefGoogle Scholar
  187. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  188. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  189. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  190. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  191. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  192. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  193. 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.CrossRefGoogle Scholar
  194. 194.
    Yamada M, Yuzawa I, Fujii K, Miyasaka Y. Chronic cerebral venous hypertension model in rats. Neurol Res. 2003;25:694–6.PubMedCrossRefPubMedCentralGoogle Scholar
  195. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  196. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  197. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  198. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  199. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  200. 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.PubMedCrossRefGoogle Scholar
  201. 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.PubMedCrossRefGoogle Scholar
  202. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  203. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  204. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  205. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  206. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  207. 207.
    Liebeskind DS. Collateral circulation. Stroke. 2003;34:2279–84.PubMedPubMedCentralCrossRefGoogle Scholar
  208. 208.
    Albers GW. Impact of recanalization, reperfusion, and collateral flow on clinical efficacy. Stroke. 2013;44:S11–2.PubMedCrossRefGoogle Scholar
  209. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  210. 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.PubMedCrossRefGoogle Scholar
  211. 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.PubMedCrossRefGoogle Scholar
  212. 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.PubMedCrossRefGoogle Scholar
  213. 213.
    Winship IR. Cerebral collaterals and collateral therapeutics for acute ischemic stroke. Microcirculation. 2015;22:228–36.PubMedCrossRefGoogle Scholar
  214. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  215. 215.
    Edwards EA. Scope and limitations of collateral circulation. Presidential address. Arch Surg. 1984;119:761–5.PubMedCrossRefGoogle Scholar
  216. 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.PubMedCrossRefGoogle Scholar
  217. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  218. 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.PubMedCrossRefGoogle Scholar
  219. 219.
    Coyle P, Heistad DD. Blood flow through cerebral collateral vessels one month after middle cerebral artery occlusion. Stroke. 1987;18:407–11.PubMedCrossRefGoogle Scholar
  220. 220.
    Wei L, Erinjeri JP, Rovainen CM, Woolsey TA. Collateral growth and angiogenesis around cortical stroke. Stroke. 2001;32:2179–84.PubMedCrossRefGoogle Scholar
  221. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  222. 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.CrossRefGoogle Scholar
  223. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  224. 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.Google Scholar
  225. 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.PubMedCrossRefGoogle Scholar
  226. 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.PubMedCrossRefGoogle Scholar
  227. 227.
    Liebeskind DS. Reperfusion for acute ischemic stroke: arterial revascularization and collateral therapeutics. Curr Opin Neurol. 2010;23:36–45.PubMedCrossRefGoogle Scholar
  228. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  229. 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.PubMedCrossRefGoogle Scholar
  230. 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.PubMedCrossRefGoogle Scholar
  231. 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.PubMedCrossRefGoogle Scholar
  232. 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.PubMedCrossRefGoogle Scholar
  233. 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.PubMedCrossRefGoogle Scholar
  234. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  235. 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.PubMedCrossRefGoogle Scholar
  236. 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.PubMedCrossRefGoogle Scholar
  237. 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.PubMedCrossRefGoogle Scholar
  238. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  239. 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.PubMedCrossRefGoogle Scholar
  240. 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.PubMedCrossRefGoogle Scholar
  241. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  242. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  243. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  244. 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.PubMedCrossRefGoogle Scholar
  245. 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.PubMedCrossRefGoogle Scholar
  246. 246.
    Greif DM, Eichmann A. Vascular biology: brain vessels squeezed to death. Nature. 2014;508:50–1.PubMedCrossRefGoogle Scholar
  247. 247.
    O’Farrell FM, Attwell D. A role for pericytes in coronary no-reflow. Nat Rev Cardiol. 2014;11:427–32.PubMedCrossRefGoogle Scholar
  248. 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.PubMedCrossRefGoogle Scholar
  249. 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.PubMedCrossRefGoogle Scholar
  250. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  251. 251.
    Obermeier B, Daneman R, Ransohoff RM. Development, maintenance and disruption of the blood-brain barrier. Nat Med. 2013;19:1584–96.PubMedPubMedCentralCrossRefGoogle Scholar
  252. 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.PubMedCrossRefGoogle Scholar
  253. 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.PubMedCrossRefGoogle Scholar
  254. 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.PubMedCrossRefGoogle Scholar
  255. 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.PubMedCrossRefGoogle Scholar
  256. 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.PubMedCrossRefGoogle Scholar
  257. 257.
    Kloc M, Kubiak JZ, Li XC, Ghobrial RM. Pericytes, microvasular dysfunction, and chronic rejection. Transplantation. 2015;99:658–67.PubMedPubMedCentralCrossRefGoogle Scholar
  258. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  259. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  260. 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.PubMedCrossRefGoogle Scholar
  261. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  262. 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. 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.PubMedCrossRefGoogle Scholar
  264. 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.PubMedCrossRefGoogle Scholar
  265. 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.PubMedCrossRefGoogle Scholar
  266. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  267. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  268. 268.
    Henninger N, Fisher M. Extending the time window for endovascular and pharmacological reperfusion. Transl Stroke Res. 2016;7:284–93.PubMedCrossRefGoogle Scholar
  269. 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.PubMedCrossRefGoogle Scholar
  270. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  271. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  272. 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.PubMedGoogle Scholar
  273. 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.PubMedCrossRefGoogle Scholar
  274. 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.PubMedCrossRefGoogle Scholar
  275. 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.PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2019

Authors and Affiliations

  • Yujie Chen
    • 1
    • 2
    • 3
  • Yang Zhang
    • 4
  • Zhenni Guo
    • 5
  • Ling Liu
    • 6
  • Feng Gao
    • 7
  • Yanfeng Lv
    • 8
  • Meng Zhang
    • 9
  • Xiaochuan Sun
    • 10
  • Andre Obenaus
    • 3
  • Yi Yang
    • 5
  • Jiping Tang
    • 11
  • Hua Feng
    • 1
    • 3
  • John H. Zhang
    • 11
  1. 1.Department of NeurosurgerySouthwest Hospital, Third Military Medical UniversityChongqingChina
  2. 2.Departments of Anesthesiology, Neurosurgery, Neurology and Physiology, Neuroscience Research CenterLoma Linda UniversityLoma LindaUSA
  3. 3.Department of PediatricsLoma Linda UniversityLoma LindaUSA
  4. 4.Department of Laboratory MedicineSouthwest Hospital, Third Military Medical UniversityChongqingChina
  5. 5.Department of NeurologyThe First Hospital of Jilin UniversityChangchunChina
  6. 6.Department of NeurologyThe People’s Hospital of Nanpi CountyNanpiChina
  7. 7.Department of Interventional NeurologyBeijing Tiantan Hospital, Capital Medical UniversityBeijingChina
  8. 8.Department of Interventional NeurologyThe First People’s Hospital of Shijiazhuang CityShijiazhuangChina
  9. 9.Department of NeurologyDaping Hospital, Third Military Medical UniversityChongqingChina
  10. 10.Department of NeurosurgeryThe First Affiliated Hospital of Chongqing Medical UniversityChongqingChina
  11. 11.Department of Anesthesiology and PhysiologyLoma Linda UniversityLoma LindaUSA

Personalised recommendations