Involvement of Cerebral Venous System in Ischemic Stroke

Part of the Springer Series in Translational Stroke Research book series (SSTSR)


Recently, growing body of clinical evidence revealed the involvement of cerebral veins in ischemic stroke. The cerebral venous vasculature is no more a simple drainage system, but an active modulator for brain perfusion under hypo- or hyperperfusion conditions. In this chapter, evidence about cerebral medullary veins, cortical veins and venous outflow from cranium is provided. And the probable regulatory mechanisms are also described.


Stroke Cerebral veins Treatment 


  1. 1.
    Yu X, Yuan L. Prominence of medullary veins on susceptibility-weighted images provides prognostic information in patients with subacute stroke. AJNR Am J Neuroradiol. 2016;37:423.CrossRefGoogle Scholar
  2. 2.
    Zhu S, Li Y, Lu H, Li H, Tong S. Imaging the early cerebral blood flow changes in rat middle cerebral artery occlusion stroke model. Conf Proc IEEE Eng Med Biol Soc. 2012;2012:2655–8.PubMedGoogle Scholar
  3. 3.
    Liebeskind DS, Feldmann E. Imaging of cerebrovascular disorders: precision medicine and the collaterome. Ann N Y Acad Sci. 2016;1366(1):40–8.CrossRefGoogle Scholar
  4. 4.
    Terasawa Y, Yamamoto N, Morigaki R, Fujita K, Izumi Y, Satomi J, et al. Brush sign on 3-T T2*-weighted MRI as a potential predictor of hemorrhagic transformation after tissue plasminogen activator therapy. Stroke. 2014;45(1):274–6.CrossRefGoogle Scholar
  5. 5.
    Mittal S, Wu Z, Neelavalli J, Haacke EM. Susceptibility-weighted imaging: technical aspects and clinical applications, part 2. AJNR Am J Neuroradiol. 2009;30(2):232–52.CrossRefGoogle Scholar
  6. 6.
    Horie N, Morikawa M, Nozaki A, Hayashi K, Suyama K, Nagata I. “Brush Sign” on susceptibility-weighted MR imaging indicates the severity of moyamoya disease. AJNR Am J Neuroradiol. 2011;32(9):1697–702.CrossRefGoogle Scholar
  7. 7.
    Verma RK, Hsieh K, Gratz PP, Schankath AC, Mordasini P, Zubler C, et al. Leptomeningeal collateralization in acute ischemic stroke: impact on prominent cortical veins in susceptibility-weighted imaging. Eur J Radiol. 2014;83(8):1448–54.CrossRefGoogle Scholar
  8. 8.
    Behfar A, Terzic A. Stem cells versus senescence: the yin and yang of cardiac health. J Am Coll Cardiol. 2015;65(2):148–50.CrossRefGoogle Scholar
  9. 9.
    Kao HW, Tsai FY, Hasso AN. Predicting stroke evolution: comparison of susceptibility-weighted MR imaging with MR perfusion. Eur Radiol. 2012;22(7):1397–403.CrossRefGoogle Scholar
  10. 10.
    Mucke J, Mohlenbruch M, Kickingereder P, Kieslich PJ, Baumer P, Gumbinger C, et al. Asymmetry of deep medullary veins on susceptibility weighted MRI in patients with acute MCA stroke is associated with poor outcome. PLoS One. 2015;10(4):e0120801.CrossRefGoogle Scholar
  11. 11.
    van den Wijngaard IR, Wermer MJ, Boiten J, Algra A, Holswilder G, Meijer FJ, et al. Cortical venous filling on dynamic computed tomographic angiography: a novel predictor of clinical outcome in patients with acute middle cerebral artery stroke. Stroke. 2016;47(3):762–7.CrossRefGoogle Scholar
  12. 12.
    Parthasarathy R, Kate M, Rempel JL, Liebeskind DS, Jeerakathil T, Butcher KS, et al. Prognostic evaluation based on cortical vein score difference in stroke. Stroke. 2013;44(10):2748–54.CrossRefGoogle Scholar
  13. 13.
    Parthasarathy R, Sohn SI, Jeerakathil T, Kate MP, Mishra SM, Nambiar VK, et al. A combined arterial and venous grading scale to predict outcome in anterior circulation ischemic stroke. J Neuroimaging. 2015;25:969.CrossRefGoogle Scholar
  14. 14.
    Beyer SE, Thierfelder KM, von Baumgarten L, Rottenkolber M, Meinel FG, Janssen H, et al. Strategies of collateral blood flow assessment in ischemic stroke: prediction of the follow-up infarct volume in conventional and dynamic CTA. AJNR Am J Neuroradiol. 2015;36(3):488–94.CrossRefGoogle Scholar
  15. 15.
    Munuera J, Blasco G, Hernandez-Perez M, Daunis IEP. Venous imaging-based biomarkers in acute ischaemic stroke. J Neurol Neurosurg Psychiatry. 2017;88(1):62–9.CrossRefGoogle Scholar
  16. 16.
    Abud DG, Spelle L, Piotin M, Mounayer C, Vanzin JR, Moret J. Venous phase timing during balloon test occlusion as a criterion for permanent internal carotid artery sacrifice. AJNR Am J Neuroradiol. 2005;26(10):2602–9.PubMedGoogle Scholar
  17. 17.
    Yura S, Sako K, Yonemasu Y. [The effects of disturbance of cerebral venous drainage on focal cerebral blood flow and ischemic cerebral edema]. No To Shinkei. 1990;42(3):269–75.Google Scholar
  18. 18.
    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(12):3736–9.CrossRefGoogle Scholar
  19. 19.
    Chilian WM, Mass HJ, Williams SE, Layne SM, Smith EE, Scheel KW. Microvascular occlusions promote coronary collateral growth. Am J Phys. 1990;258(4 Pt 2):H1103–11.Google Scholar
  20. 20.
    Faber JE, Chilian WM, Deindl E, van Royen N, Simons M. A brief etymology of the collateral circulation. Arterioscler Thromb Vasc Biol. 2014;34(9):1854–9.CrossRefGoogle Scholar
  21. 21.
    Adamson RH, Sarai RK, Altangerel A, Clark JF, Weinbaum S, Curry FE. Microvascular permeability to water is independent of shear stress, but dependent on flow direction. Am J Physiol Heart Circ Physiol. 2013;304(8):H1077–84.CrossRefGoogle Scholar
  22. 22.
    Faber JE, Moore SM, Lucitti JL, Aghajanian A, Zhang H. Sex differences in the cerebral collateral circulation. Transl Stroke Res. 2017;8:273.CrossRefGoogle Scholar
  23. 23.
    Sbarbati A, Pietra C, Baldassarri AM, Guerrini U, Ziviani L, Reggiani A, et al. The microvascular system in ischemic cortical lesions. Acta Neuropathol. 1996;92(1):56–63.CrossRefGoogle Scholar
  24. 24.
    Pranevicius M, Pranevicius O. Cerebral venous steal: blood flow diversion with increased tissue pressure. Neurosurgery. 2002;51(5):1267–73; discussion 73-4.CrossRefGoogle Scholar
  25. 25.
    Pranevicius O, Pranevicius M, Pranevicius H, Liebeskind DS. Transition to collateral flow after arterial occlusion predisposes to cerebral venous steal. Stroke. 2012;43(2):575–9.CrossRefGoogle Scholar
  26. 26.
    Altura BM, Gebrewold A, Zheng T, Altura BT. Sphingomyelinase and ceramide analogs induce vasoconstriction and leukocyte-endothelial interactions in cerebral venules in the intact rat brain: insight into mechanisms and possible relation to brain injury and stroke. Brain Res Bull. 2002;58(3):271–8.CrossRefGoogle Scholar
  27. 27.
    del Zoppo GJ, Mabuchi T. Cerebral microvessel responses to focal ischemia. J Cereb Blood Flow Metab. 2003;23(8):879–94.CrossRefGoogle Scholar
  28. 28.
    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(1):121–30.CrossRefGoogle Scholar
  29. 29.
    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(8):907–15.CrossRefGoogle Scholar
  30. 30.
    Abumiya T, Fitridge R, Mazur C, Copeland BR, Koziol JA, Tschopp JF, et al. Integrin alpha(IIb)beta(3) inhibitor preserves microvascular patency in experimental acute focal cerebral ischemia. Stroke. 2000;31(6):1402–9; discussion 9-10.CrossRefGoogle Scholar
  31. 31.
    Wang X, Feuerstein GZ. Induced expression of adhesion molecules following focal brain ischemia. J Neurotrauma. 1995;12(5):825–32.CrossRefGoogle Scholar
  32. 32.
    Ames A 3rd, Wright RL, Kowada M, Thurston JM, Majno G. Cerebral ischemia. II. The no-reflow phenomenon. Am J Pathol. 1968;52(2):437–53.PubMedPubMedCentralGoogle Scholar
  33. 33.
    Soares BP, Tong E, Hom J, Cheng SC, Bredno J, Boussel L, et al. Reperfusion is a more accurate predictor of follow-up infarct volume than recanalization: a proof of concept using CT in acute ischemic stroke patients. Stroke. 2010;41(1):e34–40.CrossRefGoogle Scholar
  34. 34.
    Chiang J, Kowada M, Ames A 3rd, Wright RL, Majno G. Cerebral ischemia. III. Vascular changes. Am J Pathol. 1968;52(2):455–76.PubMedPubMedCentralGoogle Scholar
  35. 35.
    Gerber JC, Miaux YJ, von Kummer R. Scoring flow restoration in cerebral angiograms after endovascular revascularization in acute ischemic stroke patients. Neuroradiology. 2015;57(3):227–40.CrossRefGoogle Scholar
  36. 36.
    Chen S, Chen Y, Xu L, Matei N, Tang J, Feng H, et al. Venous system in acute brain injury: mechanisms of pathophysiological change and function. Exp Neurol. 2015;272:4.CrossRefGoogle Scholar
  37. 37.
    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(5):1153–61.CrossRefGoogle Scholar
  38. 38.
    Al-Ali F, Elias JJ, Filipkowski DE, Faber JE. Acute ischemic stroke treatment, part 1: patient selection “the 50% barrier and the capillary index score”. Front Neurol. 2015;6:83.PubMedPubMedCentralGoogle Scholar
  39. 39.
    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(10):1222–30.CrossRefGoogle Scholar
  40. 40.
    Hussein HM, Georgiadis AL, Vazquez G, Miley JT, Memon MZ, Mohammad YM, et al. Occurrence and predictors of futile recanalization following endovascular treatment among patients with acute ischemic stroke: a multicenter study. AJNR Am J Neuroradiol. 2010;31(3):454–8.CrossRefGoogle Scholar
  41. 41.
    Olsen TS, Larsen B, Skriver EB, Herning M, Enevoldsen E, Lassen NA. Focal cerebral hyperemia in acute stroke. Incidence, pathophysiology and clinical significance. Stroke. 1981;12(5):598–607.CrossRefGoogle Scholar
  42. 42.
    Dorn F, Kuntze-Soderqvist A, Popp S, Lockau H, Haller B, Zimmer C, et al. Early venous drainage after successful endovascular recanalization in ischemic stroke—a predictor for final infarct volume? Neuroradiology. 2012;54(7):745–51.CrossRefGoogle Scholar
  43. 43.
    Marchal G, Furlan M, Beaudouin V, Rioux P, Hauttement JL, Serrati C, et al. Early spontaneous hyperperfusion after stroke. A marker of favourable tissue outcome? Brain. 1996;119(Pt 2):409–19.CrossRefGoogle Scholar
  44. 44.
    Ohta H, Nakano S, Yokogami K, Iseda T, Yoneyama T, Wakisaka S. Appearance of early venous filling during intra-arterial reperfusion therapy for acute middle cerebral artery occlusion: a predictive sign for hemorrhagic complications. Stroke. 2004;35(4):893–8.CrossRefGoogle Scholar
  45. 45.
    Mayhan WG, Werber AH, Heistad DD. Protection of cerebral vessels by sympathetic nerves and vascular hypertrophy. Circulation. 1987;75(1 Pt 2):I107–12.PubMedPubMedCentralGoogle Scholar
  46. 46.
    Mayhan WG, Heistad DD. Role of veins and cerebral venous pressure in disruption of the blood-brain barrier. Circ Res. 1986;59(2):216–20.CrossRefGoogle Scholar
  47. 47.
    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(2):226–30.CrossRefGoogle Scholar
  48. 48.
    Budohoski KP, Czosnyka M, Kirkpatrick PJ, Smielewski P, Steiner LA, Pickard JD. Clinical relevance of cerebral autoregulation following subarachnoid haemorrhage. Nat Rev Neurol. 2013;9(3):152–63.CrossRefGoogle Scholar
  49. 49.
    Kulik T, Kusano Y, Aronhime S, Sandler AL, Winn HR. Regulation of cerebral vasculature in normal and ischemic brain. Neuropharmacology. 2008;55(3):281–8.CrossRefGoogle Scholar
  50. 50.
    Palomares SM, Cipolla MJ. Vascular protection following cerebral ischemia and reperfusion. J Neurol Neurophysiol. 2011;2011:S1.PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of NeurologyThe Second Affiliated Hospital of School of Medicine, Zhejiang UniversityHangzhouChina
  2. 2.Department of Anesthesiology and PhysiologyLoma Linda UniversityLoma LindaUSA

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