The haemorrhagic transformation of cerebral infarction: classification; pathogenesis; predictors and effect on the functional outcome

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Abstract

Using specific keywords; we searched for articles from the last 10 years on haemorrhagic transformation (HT) of cerebral infarction (CI); which were available on the PubMed database. This article provides an analysis and a summary of the information on the classification; pathogenesis and predictors (clinical; laboratory; neuroimaging; including the use of integrative assessment scales) of HT; as well as its impact on the functional outcome of the condition. It is emphasized that HT is a multifactorial pathological process in its phenomenology; including brain ischaemia; the development of coagulopathy; disturbances in the integrity of the blood–brain barrier and reperfusion injury. The emphasis is placed on careful monitoring of patients with acute ischaemic infarct after intravenous thrombolytic therapy and/or endovascular intervention; as well as those patients with a high predicted risk of HT. Timely and regular neuroimaging should be carried out to detect HT as soon as possible. Type 2 parenchymal haematomas; the most severe type of HT; are most often associated with high mortality and an unfavourable functional outcome.

About the authors

Dina R. Khasanova

Kazan State Medical University; Interregional Clinical Diagnostic Centre

Email: ninilak@gmail.com
Russian Federation, Kazan

Mikhail N. Kalinin

Kazan State Medical University; Interregional Clinical Diagnostic Centre

Author for correspondence.
Email: ninilak@gmail.com
Russian Federation, Kazan

Мurat M. Ibatullin

Kazan State Medical University; Interregional Clinical Diagnostic Centre

Email: ninilak@gmail.com
Russian Federation, Kazan

Ilnur Sh. Rakhimov

Elabuga Institute (Branch) of the Kazan (Volga Region) Federal University

Email: ninilak@gmail.com
Russian Federation, Elabuga

References

  1. Berger C., Fiorelli M., Steiner T. et al. Hemorrhagic transformation of ischemic brain tissue: asymptomatic or symptomatic? Stroke 2001; 32: 1330–1335. doi: 10.1161/01.STR.32.6.1330. PMID: 11387495.
  2. Lei C., Wu B., Liu M. et al. Asymptomatic hemorrhagic transformation after acute ischemic stroke: is it clinically innocuous? J Stroke Cerebrovasc Dis 2014; 23: 2767–2772. doi: 10.1016/j.jstrokecerebrovasdis.2014.06.024. PMID: 25314946.
  3. Sussman E.S., Connolly E.S.Jr. Hemorrhagic transformation: a review of the rate of hemorrhage in the major clinical trials of acute ischemic stroke. Front Neurol 2013; 4: 69. doi: 10.3389/fneur.2013.00069. PMID: 23772220.
  4. Lee Y.B., Yoon W., Lee Y.Y. et al. Predictors and impact of hemorrhagic transformations after endovascular thrombectomy in patients with acute large vessel occlusions. J Neurointerv Surg 2018; 11: 469–473. doi: 10.1136/neurintsurg-2018-014080. PMID: 30291207.
  5. Wolpert S.M., Bruckmann H., Greenlee R. et al. Neuroradiologic evaluation of patients with acute stroke treated with recombinant tissue plasminogen activator. The rt-PA Acute Stroke Study Group. Am J Neuroradiol 1993; 14: 3-13. PMID: 8427107.
  6. Trouillas P., von Kummer R. Classification and pathogenesis of cerebral hemorrhages after thrombolysis in ischemic stroke. Stroke 2006; 37: 556–561. doi: 10.1161/01.STR.0000196942.84707.71. PMID: 16397182.
  7. von Kummer R., Broderick J.P., Campbell B.C. et al. The Heidelberg Bleeding Classification: classification of bleeding events after ischemic stroke and reperfusion therapy. Stroke 2015; 46: 2981–2986. doi: 10.1161/STROKEAHA.115.010049. PMID: 26330447.
  8. Hacke W., Kaste M., Bluhmki E. et al. Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N Engl J Med. 2008; 359: 1317–1329. doi: 10.1056/NEJMoa0804656. PMID: 18815396.
  9. Gumbinger C., Gruschka P., Böttinger M. et al. Improved prediction of poor outcome after thrombolysis using conservative definitions of symptomatic hemorrhage. Stroke 2012; 43: 240–242. doi: 10.1161/STROKEAHA.111.623033. PMID: 21998049.
  10. Seet R.C., Rabinstein A.A. Symptomatic intracranial hemorrhage following intravenous thrombolysis for acute ischemic stroke: a critical review of case definitions. Cerebrovasc Dis 2012; 34: 106–114. doi: 10.1159/000339675. PMID: 22868870.
  11. Rao N.M., Levine S.R., Gornbein J.A. et al. Defining clinically relevant cerebral hemorrhage after thrombolytic therapy for stroke: analysis of the National Institute of Neurological Disorders and Stroke tissue-type plasminogen activator trials. Stroke 2014; 45: 2728–2733. doi: 10.1161/STROKEAHA.114.005135. PMID: 25096731.
  12. Yaghi S., Willey J.Z., Cucchiara B. et al. Treatment and outcome of hemorrhagic transformation after intravenous alteplase in acute ischemic stroke: a scientific statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2017; 48: e343–e361. doi: 10.1161/STR.0000000000000152. PMID: 29097489.
  13. Jickling G.C., Liu D., Stamova B. et al. Hemorrhagic transformation after ischemic stroke in animals and humans. J Cereb Blood Flow Metab 2014; 34: 185–199. doi: 10.1038/jcbfm.2013.203. PMID: 24281743.
  14. Jaillard A., Cornu C., Durieux A. et al. Hemorrhagic transformation in acute ischemic stroke. The MAST-E study. MAST-E Group. Stroke 1999; 30: 1326–1332. doi: 10.1161/01.STR.30.7.1326. PMID: 10390303.
  15. Bang O.Y., Saver J.L., Kim S.J. et al. Collateral flow averts hemorrhagic transformation after endovascular therapy for acute ischemic stroke. Stroke 2011; 42: 2235-2239. doi: 10.1161/STROKEAHA.110.604603. PMID: 21737798.
  16. Terruso V., D'Amelio M., Di Benedetto N. et al. Frequency and determinants for hemorrhagic transformation of cerebral infarction. Neuroepidemiology 2009; 33: 261–265. doi: 10.1159/000229781. PMID: 19641332.
  17. Paciaroni M., Agnelli G., Corea F. et al. Early hemorrhagic transformation of brain infarction: rate, predictive factors, and influence on clinical outcome: results of a prospective multicenter study. Stroke 2008; 39: 2249–2256. doi: 10.1161/STROKEAHA.107.510321. PMID: 18535273.
  18. Larrue V., von Kummer R.R., Muller A. et al. Risk factors for severe hemorrhagic transformation in ischemic stroke patients treated with recombinant tissue plasminogen activator: a secondary analysis of the European-Australasian Acute Stroke Study (ECASS II) Stroke 2001; 32: 438–441. doi: 10.1161/01.STR.32.2.438. PMID: 11157179.
  19. National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. Tissue plasminogen activator for acute ischemic stroke. N Engl J Med 1995; 333: 1581–1587. doi: 10.1056/NEJM199512143332401. PMID: 7477192.
  20. Intracerebral hemorrhage after intravenous t-PA therapy for ischemic stroke. The NINDS t-PA Stroke Study Group. Stroke 1997; 28: 2109–2118. doi: 10.1161/01.STR.28.11.2109. PMID: 9368550.
  21. Clark W.M., Wissman S., Albers G.W. et al. Recombinant tissue-type plasminogen activator (Alteplase) for ischemic stroke 3 to 5 hours after symptom onset. The ATLANTIS Study: a randomized controlled trial. Alteplase thrombolysis for acute noninterventional therapy in ischemic stroke. JAMA 1999; 282: 2019–2026. doi: 10.1001/jama.282.21.2019. PMID: 10591384.
  22. Hao Y., Zhang Z., Zhang H. et al. Risk of intracranial hemorrhage after endovascular treatment for acute ischemic stroke: systematic review and meta-analysis. Interv Neurol 2017; 6: 57–64. doi: 10.1159/000454721. PMID: 28611835.
  23. Thomalla G., Sobesky J., Kohrmann M. et al. Two tales: hemorrhagic transformation but not parenchymal hemorrhage after thrombolysis is related to severity and duration of ischemia: MRI study of acute stroke patients treated with intravenous tissue plasminogen activator within 6 hours. Stroke 2007; 38: 313–318. doi: 10.1161/01.STR.0000254565.51807.22. PMID: 17204683.
  24. Hamann G.F., del Zoppo G.J., von Kummer R. Hemorrhagic transformation of cerebral infarction--possible mechanisms. Thromb Haemost 1999; 82 Suppl 1: 92–94. PMID: 10695495.
  25. Vandelli L., Marietta M., Gambini M. et al. Fibrinogen decrease after intravenous thrombolysis in ischemic stroke patients is a risk factor for intracerebral hemorrhage. J Stroke Cerebrovasc Dis 2015; 24: 394–400. doi: 10.1016/j.jstrokecerebrovasdis.2014.09.005. PMID: 25497721.
  26. Matosevic B., Knoflach M., Werner P. et al. Fibrinogen degradation coagulopathy and bleeding complications after stroke thrombolysis. Neurology 2013; 80: 1216–1224. doi: 10.1212/WNL.0b013e3182897015. PMID: 23486872.
  27. Lee V.H., Conners J.J., Cutting S. et al. Elevated international normalized ratio as a manifestation of post-thrombolytic coagulopathy in acute ischemic stroke. J Stroke Cerebrovasc Dis 2014; 23: 2139–2144. doi: 10.1016/j.jstrokecerebrovasdis.2014.03.021. PMID: 25081309.
  28. Wang X., Lee S.R., Arai K.иet al. Lipoprotein receptor-mediated induction of matrix metalloproteinase by tissue plasminogen activator. Nat Med 2003; 9: 1313–1317. doi: 10.1038/nm926. PMID: 12960961.
  29. Kelly M.A., Shuaib A., Todd K.G. Matrix metalloproteinase activation and blood-brain barrier breakdown following thrombolysis. Exp Neurol 2006; 200: 38–49. doi: 10.1016/j.expneurol.2006.01.032. PMID: 16624294.
  30. Suzuki Y., Nagai N., Umemura K. Novel situations of endothelial injury in stroke--mechanisms of stroke and strategy of drug development: intracranial bleeding associated with the treatment of ischemic stroke: thrombolytic treatment of ischemia-affected endothelial cells with tissue-type plasminogen activator. J Pharmacol Sci 2011; 116: 25–29. doi: 10.1254/jphs.10R27FM. PMID: 21498957.
  31. Wang X., Tsuji K., Lee S.R. et al. Mechanisms of hemorrhagic transformation after tissue plasminogen activator reperfusion therapy for ischemic stroke. Stroke 2004; 35: 2726–2730. doi: 10.1161/01.STR.0000143219.16695.af. PMID: 15459442.
  32. Hamann G.F., Liebetrau M., Martens H. et al. Microvascular basal lamina injury after experimental focal cerebral ischemia and reperfusion in the rat. J Cereb Blood Flow Metab 2002; 22: 526–533. doi: 10.1097/00004647-200205000-00004. PMID: 11973425.
  33. Rossi D.J., Brady J.D., Mohr C. Astrocyte metabolism and signaling during brain ischemia. Nat Neurosci 2007; 10: 1377–1386. doi: 10.1038/nn2004. PMID: 17965658.
  34. Warach S., Latour L.L. Evidence of reperfusion injury, exacerbated by thrombolytic therapy, in human focal brain ischemia using a novel imaging marker of early blood-brain barrier disruption. Stroke 2004; 35: 2659–2661. doi: 10.1161/01.STR.0000144051.32131.09. PMID: 15472105.
  35. Latour L.L., Kang D.W., Ezzeddine M.A. et al. Early blood-brain barrier disruption in human focal brain ischemia. Ann Neurol 2004; 56: 468–477. doi: 10.1002/ana.20199. PMID: 15389899.
  36. Klohs J., Steinbrink J., Bourayou R. et al. Near-infrared fluorescence imaging with fluorescently labeled albumin: a novel method for non-invasive optical imaging of blood-brain barrier impairment after focal cerebral ischemia in mice. J Neurosci Methods 2009; 180: 126–132. doi: 10.1016/j.jneumeth.2009.03.002. PMID: 19427539.
  37. Sandoval K.E., Witt K.A. Blood-brain barrier tight junction permeability and ischemic stroke. Neurobiol Dis 2008; 32: 200–219. doi: 10.1016/j.nbd.2008.08.005. PMID: 18790057.
  38. Khatri R., McKinney A.M., Swenson B. et al. Blood-brain barrier, reperfusion injury, and hemorrhagic transformation in acute ischemic stroke. Neurology 2012; 79: S52–S57. doi: 10.1212/WNL.0b013e3182697e70. PMID: 23008413.
  39. Kidwell C.S., Saver J.L., Carneado J. et al. Predictors of hemorrhagic transformation in patients receiving intra-arterial thrombolysis. Stroke 2002; 33: 717–724. doi: 10.1161/hs0302.104110. PMID: 11872894.
  40. Whiteley W.N., Slot K.B., Fernandes P. et al. Risk factors for intracranial hemorrhage in acute ischemic stroke patients treated with recombinant tissue plasminogen activator: a systematic review and meta-analysis of 55 studies. Stroke 2012; 43: 2904–2909. doi: 10.1161/STROKEAHA.112.665331. PMID: 22996959.
  41. Lyden P.D. Hemorrhagic transformation during thrombolytic therapy and reperfusion: effects of age, blood pressure, and matrix metalloproteinases. J Stroke Cerebrovasc Dis 2013; 22: 532–538. doi: 10.1016/j.jstrokecerebrovasdis.2013.02.001. PMID: 23453556.
  42. Elgebaly M.M., Ogbi S., Li W. et al. Neurovascular injury in acute hyperglycemia and diabetes: A comparative analysis in experimental stroke. Transl Stroke Res 2011; 2: 391–398. doi: 10.1007/s12975-011-0083-3. PMID: 21909340.
  43. Xing Y., Jiang X., Yang Y. et al. Hemorrhagic transformation induced by acute hyperglycemia in a rat model of transient focal ischemia. Acta Neurochir Suppl 2011; 111: 49–54. doi: 10.1007/978-3-7091-0693-8_9. PMID: 21725731.
  44. Dankbaar J.W., Hom J., Schneider T. et al. Age- and anatomy-related values of blood-brain barrier permeability measured by perfusion-CT in non-stroke patients. J Neuroradiol 2009; 36: 219–227. doi: 10.1016/j.neurad.2009.01.001. PMID: 19251320.
  45. Tejima E., Katayama Y., Suzuki Y. et al. Hemorrhagic transformation after fibrinolysis with tissue plasminogen activator: evaluation of role of hypertension with rat thromboembolic stroke model. Stroke 2001; 32: 1336–1340. doi: 10.1161/01.STR.32.6.1336. PMID: 11387496.
  46. Butcher K., Christensen S., Parsons M. et al. Postthrombolysis blood pressure elevation is associated with hemorrhagic transformation. Stroke 2010; 41: 72–77. doi: 10.1161/STROKEAHA.109.563767. PMID: 19926841.
  47. Ahmed N., Wahlgren N., Brainin M. et al. Relationship of blood pressure, antihypertensive therapy, and outcome in ischemic stroke treated with intravenous thrombolysis: retrospective analysis from Safe Implementation of Thrombolysis in Stroke-International Stroke Thrombolysis Register (SITS-ISTR). Stroke 2009; 40: 2442–2449. doi: 10.1161/STROKEAHA.109.548602. PMID: 19461022.
  48. Jauch E.C., Saver J.L., Adams H.P.Jr. et al. Guidelines for the early management of patients with acute ischemic stroke: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2013; 44: 870–947. doi: 10.1161/STR.0b013e318284056a. PMID: 23370205.
  49. Tuttle J.L., Sanders B.M., Burkhart H.M. et al. Impaired collateral artery development in spontaneously hypertensive rats. Microcirculation 2002; 9: 343–351. doi: 10.1038/sj.mn.7800151. PMID: 12375172.
  50. Pires P.W., Dams Ramos C.M., Matin N. et al. The effects of hypertension on the cerebral circulation. Am J Physiol Heart Circ Physiol 2013; 304: H1598–H1614. doi: 10.1152/ajpheart.00490.2012. PMID: 23585139.
  51. de Courten-Myers G.M., Kleinholz M., Holm P. et al. Hemorrhagic infarct conversion in experimental stroke. Ann Emerg Med 1992; 21: 120–126. doi: 10.1016/S0196-0644(05)80144-1. PMID: 1739195.
  52. Kawai N., Keep R.F., Betz A.L. Hyperglycemia and the vascular effects of cerebral ischemia. Stroke 1997; 28: 149–154. doi: 10.1161/01.STR.28.1.149. PMID: 8996504.
  53. Bruno A., Durkalski V.L., Hall C.E. et al. The Stroke Hyperglycemia Insulin Network Effort (SHINE) trial protocol: a randomized, blinded, efficacy trial of standard vs. intensive hyperglycemia management in acute stroke. Int J Stroke 2014; 9: 246–251. doi: 10.1111/ijs.12045. PMID: 23506245.
  54. Tu H.T., Campbell B.C., Christensen S. et al. Worse stroke outcome in atrial fibrillation is explained by more severe hypoperfusion, infarct growth, and hemorrhagic transformation. Int J Stroke 2015; 10: 534–540. doi: 10.1111/ijs.12007. PMID: 23489996.
  55. Heidbuchel H., Verhamme P., Alings M., et al. Updated European Heart Rhythm Association Practical Guide on the use of non-vitamin K antagonist anticoagulants in patients with non-valvular atrial fibrillation. Europace 2015; 17: 1467–1507. doi: 10.1093/europace/euv309. PMID: 26324838.
  56. Seiffge D.J., Werring D.J., Paciaroni M., et al. Timing of anticoagulation after recent ischaemic stroke in patients with atrial fibrillation. Lancet Neurol 2019; 18: 117–126. doi: 10.1016/S1474-4422(18)30356-9. PMID: 30415934.
  57. Hankey G.J. Dual antiplatelet therapy in acute transient ischemic attack and minor stroke. N Engl J Med 2013; 369: 82–83. doi: 10.1056/NEJMe1305127. PMID: 23803138.
  58. Cucchiara B., Tanne D., Levine S.R. et al. A risk score to predict intracranial hemorrhage after recombinant tissue plasminogen activator for acute ischemic stroke. J Stroke Cerebrovasc Dis 2008; 17: 331–333. doi: 10.1016/j.jstrokecerebrovasdis.2008.03.012. PMID: 18984422.
  59. Nardi K., Leys D., Eusebi P. et al. Influence of lipid profiles on the risk of hemorrhagic transformation after ischemic stroke: systematic review. Cerebrovasc Dis Extra 2011; 1: 130–141. doi: 10.1159/000335014. PMID: 22566990.
  60. Bang O.Y., Saver J.L., Liebeskind D.S. et al. Cholesterol level and symptomatic hemorrhagic transformation after ischemic stroke thrombolysis. Neurology 2007; 68: 737–742. doi: 10.1212/01.wnl.0000252799.64165.d5. PMID: 17182976.
  61. D’Amelio M., Terruso V., Famoso G. et al. Cholesterol levels and risk of hemorrhagic transformation after acute ischemic stroke. Cerebrovasc Dis 2011; 32: 234–238. doi: 10.1159/000329315. PMID: 21860236.
  62. Kim B.J., Lee S.H., Ryu W.S. et al. Low level of low-density lipoprotein cholesterol increases hemorrhagic transformation in large artery atherothrombosis but not in cardioembolism. Stroke 2009; 40: 1627–1632. doi: 10.1161/STROKEAHA.108.539643. PMID: 19286585.
  63. Scheitz J.F., MacIsaac R.L., Abdul-Rahim A.H. et al. Statins and risk of poststroke hemorrhagic complications. Neurology 2016; 86: 1590–1596. doi: 10.1212/WNL.0000000000002606. PMID: 27016519.
  64. Engelter S.T., Soinne L., Ringleb P. et al. IV thrombolysis and statins. Neurology 2011; 77: 888–895. doi: 10.1212/WNL.0b013e31822c9135. PMID: 21849650.
  65. Campos M., García-Bonilla L., Hernández-Guillamon M. et al. Combining statins with tissue plasminogen activator treatment after experimental and human stroke: a safety study on hemorrhagic transformation. CNS Neurosci Ther 2013; 19: 863–870. doi: 10.1111/cns.12181. PMID: 24118905.
  66. Thrift A., McNeil J., Donnan G. et al. Reduced frequency of high cholesterol levels among patients with intracerebral haemorrhage. J Clin Neurosci 2002; 9: 376–380. doi: 10.1054/jocn.2002.1111. PMID: 12217665.
  67. Xing Y., Guo Z.N., Yan S. et al. Increased globulin and its association with hemorrhagic transformation in patients receiving intra-arterial thrombolysis therapy. Neurosci Bull 2014; 30: 469–476. doi: 10.1007/s12264-013-1440-x. PMID: 24871645.
  68. Rodríguez-Yáñez M., Castellanos M., Blanco M. et al. Micro- and macroalbuminuria predict hemorrhagic transformation in acute ischemic stroke. Neurology 2006; 67: 1172–1177. doi: 10.1212/01.wnl.0000238353.89194.08. PMID: 17030748.
  69. Cho B.H., Kim J.T., Chang J. et al. Prediction of hemorrhagic transformation in acute ischaemic stroke by micro- and macroalbuminuria after intravenous thrombolysis. Eur J Neurol 2013; 20: 1145–1152. doi: 10.1111/ene.12127. PMID: 23582041.
  70. Foerch C., Wunderlich M.T., Dvorak F. et al. Elevated serum S100B levels indicate a higher risk of hemorrhagic transformation after thrombolytic therapy in acute stroke. Stroke 2007; 38: 2491–2495. doi: 10.1161/STROKEAHA.106.480111. PMID: 17673718.
  71. Castellanos M., Leira R., Serena J. et al. Plasma cellular-fibronectin concentration predicts hemorrhagic transformation after thrombolytic therapy in acute ischemic stroke. Stroke 2004; 35: 1671–1676. doi: 10.1161/01.STR.0000131656.47979.39. PMID: 15166391.
  72. Lee J.G., Lee K.B., Jang I.M. et al. Low glomerular filtration rate increases hemorrhagic transformation in acute ischemic stroke. Cerebrovasc Dis 2013; 35: 53–59. doi: 10.1159/000345087. PMID: 23428997.
  73. Choi K.H., Park M.S., Kim J.T. et al. The serum ferritin level is an important predictor of hemorrhagic transformation in acute ischaemic stroke. Eur J Neurol 2012; 19: 570–577. doi: 10.1111/j.1468-1331.2011.03564.x. PMID: 21999175.
  74. Nikiforova (Postnikova) T.A., Doronin B.M., Peskov S.A. [Blood serum cytokines as predictors of hemorrhagic transformation of ischemic stroke]. Zh Nevrol Psikhiatr im S.S. Korsakova 2014; 114 (3 Pt 2): 20–26. PMID: 24781237. (In Russ.)
  75. Inzitari D., Giusti B., Nencini P. et al. MMP9 variation after thrombolysis is associated with hemorrhagic transformation of lesion and death. Stroke 2013; 44: 2901–2903. doi: 10.1161/STROKEAHA.113.002274. PMID: 23908067.
  76. Christoforidis G.A., Karakasis C., Mohammad Y. et al. Predictors of hemorrhage following intra-arterial thrombolysis for acute ischemic stroke: the role of pial collateral formation. Am J Neuroradiol 2009; 30: 165–170. doi: 10.3174/ajnr.A1276. PMID: 18768718.
  77. Mendioroz M., Fernández-Cadenas I., Alvarez-Sabín J. et al. Endogenous activated protein C predicts hemorrhagic transformation and mortality after tissue plasminogen activator treatment in stroke patients. Cerebrovasc Dis 2009; 28: 143–50. doi: 10.1159/000225907. PMID: 19546541.
  78. Zhang J., Yang Y., Sun H. et al. Hemorrhagic transformation after cerebral infarction: current concepts and challenges. Ann Transl Med 2014; 2: 81. doi: 10.3978/j.issn.2305-5839.2014.08.08. PMID: 25333056.
  79. Hoffmann A., Zhu G., Wintermark M. Advanced neuroimaging in stroke patients: prediction of tissue fate and hemorrhagic transformation. Expert Rev Cardiovasc Ther 2012; 10: 515–524. doi: 10.1586/erc.12.30. PMID: 22458583.
  80. Rowley H. The four Ps of acute stroke imaging: parenchyma, pipes, perfusion, and penumbra. Am J Neuroradiol 2001; 22: 599–601. PMID: 11290464.
  81. Castellanos M., Leira R., Serena J. et al. Plasma metalloproteinase-9 concentration predicts hemorrhagic transformation in acute ischemic stroke. Stroke 2003; 34: 40–46. doi: 10.1161/01.STR.0000046764.57344.31. PMID: 12511748.
  82. Tan S., Wang D., Liu M. et al. Frequency and predictors of spontaneous hemorrhagic transformation in ischemic stroke and its association with prognosis. J Neurol 2014; 261: 905–912. doi: 10.1007/s00415-014-7297-8. PMID: 24590407.
  83. IMS Study Investigators. Hemorrhage in the Interventional Management of Stroke study. Stroke 2006; 37: 847–851. doi: 10.1161/01.STR.0000202586.69525.ae. PMID: 16439694.
  84. Larrue V., von Kummer R., del Zoppo G. et al. Hemorrhagic transformation in acute ischemic stroke. Potential contributing factors in the European Cooperative Acute Stroke Study. Stroke 1997; 28: 957–960. PMID: 9158632.
  85. Lin K., Zink W.E., Tsiouris A.J. et al. Risk assessment of hemorrhagic transformation of acute middle cerebral artery stroke using multimodal CT. J Neuroimaging 2012; 22: 160–166. doi: 10.1111/j.1552-6569.2010.00562.x. PMID: 21143549.
  86. Molina C.A., Montaner J., Abilleira S. et al. Timing of spontaneous recanalization and risk of hemorrhagic transformation in acute cardioembolic stroke. Stroke 2001; 32: 1079–1084. doi: 10.1161/01.STR.32.5.1079. PMID: 11340213.
  87. Toni D., Fiorelli M., Bastianello S. et al. Hemorrhagic transformation of brain infarct: predictability in the first 5 hours from stroke onset and influence on clinical outcome. Neurology 1996; 46: 341–345. doi: 10.1212/WNL.46.2.341. PMID: 8614491.
  88. Barber P.A., Demchuk A.M., Zhang J. et al. Validity and reliability of a quantitative computed tomography score in predicting outcome of hyperacute stroke before thrombolytic therapy. ASPECTS Study Group. Alberta Stroke Programme Early CT Score. Lancet 2000; 355: 1670–1674. doi: 10.1016/S0140-6736(00)02237-6. PMID: 10905241.
  89. Lin K., Lee S.A., Zink W.E. What ASPECTS value best predicts the 100-mL threshold on diffusion weighted imaging? Study of 150 patients with middle cerebral artery stroke. J Neuroimaging 2011; 21: 229–231. doi: 10.1111/j.1552-6569.2010.00487.x. PMID: 20609038.
  90. Puetz V., Sylaja P.N., Hill M.D. et al. CT angiography source images predict final infarct extent in patients with basilar artery occlusion. Am J Neuroradiol 2009; 30: 1877–1883. doi: 10.3174/ajnr.A1723. PMID: 19643923.
  91. Schwamm L.H., Rosenthal E.S., Swap C.J. et al. Hypoattenuation on CT angiographic source images predicts risk of intracerebral hemorrhage and outcome after intra-arterial reperfusion therapy. Am J Neuroradiol 2005; 26: 1798–1803. PMID: 16091532.
  92. Campbell B.C., Christensen S., Butcher K.S. et al. Regional very low cerebral blood volume predicts hemorrhagic transformation better than diffusion-weighted imaging volume and thresholded apparent diffusion coefficient in acute ischemic stroke. Stroke 2010; 41: 82–88. doi: 10.1161/STROKEAHA.109.562116. PMID: 19959537.
  93. Campbell B.C., Costello C., Christensen S. et al. Fluid-attenuated inversion recovery hyperintensity in acute ischemic stroke may not predict hemorrhagic transformation. Cerebrovasc Dis 2011; 32: 401–405. doi: 10.1159/000331467. PMID: 21986096.
  94. Cho A.H., Kim J.S., Kim S.J. et al. Focal fluid-attenuated inversion recovery hyperintensity within acute diffusion-weighted imaging lesions is associated with symptomatic intracerebral hemorrhage after thrombolysis. Stroke 2008; 39: 3424–3426. doi: 10.1161/STROKEAHA.108.516740. PMID: 18772449.
  95. Kufner A., Galinovic I., Brunecker P. et al. Early infarct FLAIR hyperintensity is associated with increased hemorrhagic transformation after thrombolysis. Eur J Neurol 2013; 20: 281–285. doi: 10.1111/j.1468-1331.2012.03841.x. PMID: 22900825.
  96. Oppenheim C., Samson Y., Dormont D. et al. DWI prediction of symptomatic hemorrhagic transformation in acute MCA infarct. J Neuroradiol 2002; 29: 6–13. PMID: 11984472.
  97. Sakamoto Y., Kimura K., Iguchi Y.et al. Hemorrhagic transformation in acute cerebellar infarction. Cerebrovasc Dis 2011; 32: 327–333. doi: 10.1159/000329259. PMID: 21921595.
  98. Selim M., Fink J.N., Kumar S. et al. Predictors of hemorrhagic transformation after intravenous recombinant tissue plasminogen activator: prognostic value of the initial apparent diffusion coefficient and diffusion-weighted lesion volume. Stroke 2002; 33: 2047–2052. doi: 10.1161/01.STR.0000023577.65990.4E. PMID: 12154261.
  99. Singer O.C., Humpich M.C., Fiehler J. et al. Risk for symptomatic intracerebral hemorrhage after thrombolysis assessed by diffusion-weighted magnetic resonance imaging. Ann Neurol 2008; 63: 52–60. doi: 10.1002/ana.21222. PMID: 17880020.
  100. Tong D.C., Adami A., Moseley M.E. et al. Relationship between apparent diffusion coefficient and subsequent hemorrhagic transformation following acute ischemic stroke. Stroke 2000; 31: 2378–2384. doi: 10.1161/01.STR.31.10.2378. PMID: 11022067.
  101. Huang P., Chen C.H., Lin W.C. et al. Clinical applications of susceptibility weighted imaging in patients with major stroke. J Neurol 2012; 259: 1426–1432. doi: 10.1007/s00415-011-6369-2. PMID: 22186853.
  102. Kakuda W., Thijs V.N., Lansberg M.G. et al. Clinical importance of microbleeds in patients receiving IV thrombolysis. Neurology 2005; 65: 1175–1178. doi: 10.1212/01.wnl.0000180519.27680.0f. PMID: 16247042.
  103. Kidwell C.S., Saver J.L., Villablanca J.P. et al. Magnetic resonance imaging detection of microbleeds before thrombolysis: an emerging application. Stroke 2002; 33: 95–98. doi: 10.1161/hs0102.101792. PMID: 11779895.
  104. Lee S.H., Kang B.S., Kim N. et al. Does microbleed predict haemorrhagic transformation after acute atherothrombotic or cardioembolic stroke? J Neurol Neurosurg Psychiatry 2008; 79: 913–916. doi: 10.1136/jnnp.2007.133876. PMID: 18187478.
  105. Celik Y., Utku U., Asil T. et al. Factors affecting haemorrhagic transformation in middle cerebral artery infarctions. J Clin Neurosci 2004; 11: 656–658. doi: 10.1016/j.jocn.2003.08.001. PMID: 15261244.
  106. Shi Z.S., Loh Y., Liebeskind D.S. et al. Leukoaraiosis predicts parenchymal hematoma after mechanical thrombectomy in acute ischemic stroke. Stroke 2012; 43: 1806–1811. doi: 10.1161/STROKEAHA.111.649152. PMID: 22581819.
  107. Costello C.A., Campbell B.C., Perez de la Ossa N. et al. Age over 80 years is not associated with increased hemorrhagic transformation after stroke thrombolysis. J Clin Neurosci 2012; 19: 360–363. doi: 10.1016/j.jocn.2011.08.014. PMID: 22245278.
  108. Kimura K., Sakai K., Iguchi Y. et al. Does ICA occlusion frequently have intracerebral hemorrhage after IV tissue plasminogen activator therapy for ischemic stroke? Eur Neurol 2011; 65: 245–249. doi: 10.1159/000326338. PMID: 21464569.
  109. Puetz V., Dzialowski I., Hill MD. et al. Intracranial thrombus extent predicts clinical outcome, final infarct size and hemorrhagic transformation in ischemic stroke: the clot burden score. Int J Stroke 2008; 3: 230–236. doi: 10.1111/j.1747-4949.2008.00221.x. PMID: 18811738.
  110. Tan I.Y., Demchuk A.M., Hopyan J. et al. CT angiography clot burden score and collateral score: correlation with clinical and radiologic outcomes in acute middle cerebral artery infarct. Am J Neuroradiol 2009; 30: 525–531. doi: 10.3174/ajnr.A1408. PMID: 19147716.
  111. Flacke S., Urbach H., Keller E. et al. Middle cerebral artery (MCA) susceptibility sign at susceptibility-based perfusion MR imaging: clinical importance and comparison with hyperdense MCA sign at CT. Radiology 2000; 215: 476–482. doi: 10.1148/radiology.215.2.r00ma09476. PMID: 10796928.
  112. Haring H.P., Dilitz E., Pallua A. et al. Attenuated corticomedullary contrast: An early cerebral computed tomography sign indicating malignant middle cerebral artery infarction. A case-control study. Stroke 1999; 30: 1076–1082. doi: 10.1161/01.STR.30.5.1076. PMID: 10229747.
  113. Kharitonova T., Ahmed N., Thorén M. et al. Hyperdense middle cerebral artery sign on admission CT scan--prognostic significance for ischaemic stroke patients treated with intravenous thrombolysis in the safe implementation of thrombolysis in Stroke International Stroke Thrombolysis Register. Cerebrovasc Dis 2009; 27: 51–59. doi: 10.1159/000172634. PMID: 19018138.
  114. Manno E.M., Nichols D.A., Fulgham J.R. et al. Computed tomographic determinants of neurologic deterioration in patients with large middle cerebral artery infarctions. Mayo Clin Proc 2003; 78: 156–160. doi: 10.4065/78.2.156. PMID: 12583526.
  115. Paliwal P.R., Ahmad A., Shen L. et al. Persistence of hyperdense middle cerebral artery sign on follow-up CT scan after intravenous thrombolysis is associated with poor outcome. Cerebrovasc Dis 2012; 33: 446–452. doi: 10.1159/000336863. PMID: 22456065.
  116. Zou M., Churilov L., He A. et al. Hyperdense middle cerebral artery sign is associated with increased risk of hemorrhagic transformation after intravenous thrombolysis for patients with acute ischaemic stroke. J Clin Neurosci 2013; 20: 984–987. doi: 10.1016/j.jocn.2012.10.013. PMID: 23664409.
  117. Abul-Kasim K., Selariu E., Brizzi M. et al. Hyperdense middle cerebral artery sign in multidetector computed tomography: definition, occurrence, and reliability analysis. Neurol India 2009; 57: 143–150. doi: 10.4103/0028-3886.51282. PMID: 19439843.
  118. Koo C.K., Teasdale E., Muir K.W. What constitutes a true hyperdense middle cerebral artery sign? Cerebrovasc Dis 2000; 10: 419–423. doi: 10.1159/000016101. PMID: 11070370.
  119. Shobha N., Bal S., Boyko M. et al. Measurement of length of hyperdense MCA sign in acute ischemic stroke predicts disappearance after IV tPA. J Neuroimaging 2014; 24: 7–10. doi: 10.1111/j.1552-6569.2012.00761.x. PMID: 23316960.
  120. Guo G., Yang Y., Yang W. Validation of hyperintense middle cerebral artery sign in acute ischemic stroke: Comparison between magnetic resonance imaging and angiography. Neural Regen Res 2012; 7: 229–234. doi: 10.3969/j.issn.1673-5374.2012.03.013. PMID: 25767505.
  121. Zheng M., Fan D.S. Acute cardioembolic and thrombotic middle cerebral artery occlusions have different morphological susceptibility signs on T2 (∗) -weighted magnetic resonance images. Biomed Res Int 2015; 2015: 839820. doi: 10.1155/2015/839820. PMID: 26543869.
  122. Hermier M., Nighoghossian N., Derex L. et al. Hypointense transcerebral veins at T2*-weighted MRI: a marker of hemorrhagic transformation risk in patients treated with intravenous tissue plasminogen activator. J Cereb Blood Flow Metab 2003; 23: 1362–1370. doi: 10.1097/01.WCB.0000091764.61714.79. PMID: 14600444.
  123. Hohenhaus M., Schmidt W.U., Brunecker P. et al. FLAIR vascular hyperintensities in acute ICA and MCA infarction: a marker for mismatch and stroke severity? Cerebrovasc Dis 2012; 34: 63–69. doi: 10.1159/000339012. PMID: 22759720.
  124. Arenillas J.F., Rovira A., Molina C.A. et al. Prediction of early neurological deterioration using diffusion- and perfusion-weighted imaging in hyperacute middle cerebral artery ischemic stroke. Stroke 2002; 33: 2197–2203. doi: 10.1161/01.STR.0000027861.75884.DF. PMID: 12215587.
  125. García-Bermejo P., Calleja A.I., Pérez-Fernández S. et al. Perfusion computed tomography-guided intravenous thrombolysis for acute ischemic stroke beyond 4.5 hours: a case-control study. Cerebrovasc Dis 2012; 34: 31–37. doi: 10.1159/000338778. PMID: 22759450.
  126. Kassner A., Mandell D.M., Mikulis D.J. Measuring permeability in acute ischemic stroke. Neuroimaging Clin N Am 2011; 21: 315–325. doi: 10.1016/j.nic.2011.01.004. PMID: 21640302.
  127. Viallon M., Altrichter S., Pereira V.M. et al. Combined use of pulsed arterial spin-labeling and susceptibility-weighted imaging in stroke at 3T. Eur Neurol 2010; 64: 286–296. doi: 10.1159/000321162. PMID: 20980761.
  128. Hjort N., Wu O., Ashkanian M. et al. MRI detection of early blood-brain barrier disruption: parenchymal enhancement predicts focal hemorrhagic transformation after thrombolysis. Stroke 2008; 39: 1025–1028. doi: 10.1161/STROKEAHA.107.497719. PMID: 18258832.
  129. Kassner A., Liu F., Thornhill R.E. et al. Prediction of hemorrhagic transformation in acute ischemic stroke using texture analysis of postcontrast T1-weighted MR images. J Magn Reson Imaging 2009; 30: 933–941. doi: 10.1002/jmri.21940. PMID: 19856407.
  130. Kim E.Y., Na D.G., Kim S.S. et al. Prediction of hemorrhagic transformation in acute ischemic stroke: role of diffusion-weighted imaging and early parenchymal enhancement. Am J Neuroradiol 2005; 26: 1050–1055. PMID: 15891158.
  131. Vo K.D., Santiago F., Lin W., et al. MR imaging enhancement patterns as predictors of hemorrhagic transformation in acute ischemic stroke. Am J Neuroradiol 2003; 24: 674–679. PMID: 12695202.
  132. Hom J., Dankbaar J.W., Soares B.P. et al. Blood-brain barrier permeability assessed by perfusion CT predicts symptomatic hemorrhagic transformation and malignant edema in acute ischemic stroke. Am J Neuroradiol 2011; 32: 41–48. doi: 10.3174/ajnr.A2244. PMID: 20947643.
  133. Kassner A., Roberts T.P., Moran B. et al. Recombinant tissue plasminogen activator increases blood-brain barrier disruption in acute ischemic stroke: an MR imaging permeability study. Am J Neuroradiol 2009; 30: 1864–1869. doi: 10.3174/ajnr.A1774. PMID: 19661169.
  134. Kassner A., Roberts T., Taylor K. et al. Prediction of hemorrhage in acute ischemic stroke using permeability MR imaging. Am J Neuroradiol 2005; 26: 2213–2217. PMID: 16219824.
  135. Vidarsson L., Thornhill R.E., Liu F., et al. Quantitative permeability magnetic resonance imaging in acute ischemic stroke: how long do we need to scan? J Magn Reson Imaging 2009; 27: 1216–1222. doi: 10.1016/j.mri.2009.01.019. PMID: 19695816.
  136. Whiteley W.N., Thompson D., Murray G. et al. Targeting recombinant tissue-type plasminogen activator in acute ischemic stroke based on risk of intracranial hemorrhage or poor functional outcome: an analysis of the third international stroke trial. Stroke 2014; 45: 1000–1006. doi: 10.1161/STROKEAHA.113.004362. PMID: 24603072.
  137. Gore J.M., Sloan M., Price T.R., et al. Intracerebral hemorrhage, cerebral infarction, and subdural hematoma after acute myocardial infarction and thrombolytic therapy in the Thrombolysis in Myocardial Infarction Study: Thrombolysis in Myocardial Infarction, Phase II, pilot and clinical trial. Circulation 1991; 83: 448–459. PMID: 1899364.
  138. Hacke W., Kaste M., Fieschi C. et al. Randomised double-blind placebo-controlled trial of thrombolytic therapy with intravenous alteplase in acute ischaemic stroke (ECASS II): Second European-Australasian Acute Stroke Study Investigators. Lancet 1998; 352: 1245–1251. doi: 10.1016/S0140-6736(98)08020-9. PMID: 9788453.
  139. Wahlgren N., Ahmed N., Dávalos A. et al. Thrombolysis with alteplase for acute ischaemic stroke in the Safe Implementation of Thrombolysis in Stroke-Monitoring Study (SITS-MOST): an observational study. Lancet 2007; 369: 275–282. doi: 10.1016/S0140-6736(07)60149-4. PMID: 17258667.
  140. Strbian D., Sairanen T., Meretoja A. et al. Patient outcomes from symptomatic intracerebral hemorrhage after stroke thrombolysis. Neurology 2011; 77: 341–348. doi: 10.1212/WNL.0b013e3182267b8c. PMID: 21715707.
  141. del Zoppo G.J., von Kummer R., Hamann G.F. Ischaemic damage of brain microvessels: inherent risks for thrombolytic treatment in stroke. J Neurol Neurosurg Psychiatry 1998; 65: 1–9. doi: 10.1136/jnnp.65.1.1. PMID: 9667553.
  142. Arnould M.C., Grandin C.B., Peeters A. et al. Comparison of CT and three MR sequences for detecting and categorizing early (48 hours) hemorrhagic transformation in hyperacute ischemic stroke. Am J Neuroradiol 2004; 25: 939–944. PMID: 15205127.
  143. Barber P.A., Darby D.G., Desmond P.M. et al. Identification of major ischemic change. Diffusion-weighted imaging versus computed tomography. Stroke 1999; 30: 2059–2065. PMID: 10512907.
  144. Goos J.D., van der Flier W.M., Knol D.L. et al. Clinical relevance of improved microbleed detection by susceptibility-weighted magnetic resonance imaging. Stroke 2011; 42: 1894–1900. doi: 10.1161/STROKEAHA.110.599837. PMID: 21566235.
  145. Harada M., Morita N., Uno M. et al. Incidence and clinical correlation of intracranial hemorrhages observed by 3-tesla gradient echo T(2)*-weighted images following intravenous thrombolysis with recombinant tissue plasminogen activator. Cerebrovasc Dis 2010; 29: 571–575. doi: 10.1159/000306644. PMID: 20375500.
  146. Lin Y.H., Lou M., Zhu R.Y. et al. [Multi-mode MRI-based intravenous thrombolysis with recombinant tissue plasminogen activator (rtPA) reduces hemorrhagic transformation in ischemic stroke patients]. Zhejiang Da Xue Xue Bao Yi Xue Ban 2012; 41: 665–671. PMID: 23239659. (In Chinese)
  147. Lindley R.I., Wardlaw J.M., Sandercock P.A. et al. Frequency and risk factors for spontaneous hemorrhagic transformation of cerebral infarction. J Stroke Cerebrovasc Dis 2004; 13: 235–246. doi: 10.1016/j.jstrokecerebrovasdis.2004.03.003. PMID: 17903981.
  148. Renou P., Sibon I., Tourdias T. et al. Reliability of the ECASS radiological classification of postthrombolysis brain haemorrhage: a comparison of CT and three MRI sequences. Cerebrovasc Dis 2010; 29: 597–604. doi: 10.1159/000312867. PMID: 20413970.
  149. Lees K.R., Bluhmki E., von Kummer R. et al. Time to treatment with intravenous alteplase and outcome in stroke: an updated pooled analysis of ECASS, ATLANTIS, NINDS, and EPITHET trials. Lancet 2010; 375: 1695–1703. doi: 10.1016/S0140-6736(10)60491-6. PMID: 20472172.
  150. Fiorelli M., Bastianello S., von Kummer R. et al. Hemorrhagic transformation within 36 hours of a cerebral infarct: relationships with early clinical deterioration and 3-month outcome in the European Cooperative Acute Stroke Study I (ECASS I) cohort. Stroke 1999; 30: 2280–2284. doi: 10.1161/01.STR.30.11.2280. PMID: 10548658.
  151. Fiehler J., Remmele C., Kucinski T. et al. Reperfusion after severe local perfusion deficit precedes hemorrhagic transformation: an MRI study in acute stroke patients. Cerebrovasc Dis 2005; 19: 117–124. doi: 10.1159/000083180. PMID: 15640606.
  152. Thevathasan A., Naylor J., Churilov L. et al. Association between hemorrhagic transformation after endovascular therapy and poststroke seizures. Epilepsia 2018; 59: 403–409. doi: 10.1111/epi.13982. PMID: 29288487.
  153. Dzialowski I., Pexman J.H., Barber P.A. et al. Asymptomatic hemorrhage after thrombolysis may not be benign: prognosis by hemorrhage type in the Canadian alteplase for stroke effectiveness study registry. Stroke 2007; 38: 75–79. doi: 10.1161/01.STR.0000251644.76546.62. PMID: 17122437.
  154. Park J.H., Ko Y., Kim W.J. et al. Is asymptomatic hemorrhagic transformation really innocuous. Neurology 2012; 78: 421–426. doi: 10.1212/WNL.0b013e318245d22c. PMID: 22282643.
  155. Motto C., Ciccone A., Aritzu E., et al. Hemorrhage after an acute ischemic stroke. MAST-I Collaborative Group. Stroke 1999; 30: 761–764. PMID: 10187875.
  156. Menon B.K., Saver J.L., Prabhakaran S. et al. Risk score for intracranial hemorrhage in patients with acute ischemic stroke treated with intravenous tissue–type plasminogen activator. Stroke 2012; 43: 2293–2299. doi: 10.1161/STROKEAHA.112.660415. PMID: 22811458.
  157. Pisters R., Lane D.A., Nieuwlaat R. et al. A novel user-friendly score (HAS-BLED) to assess 1-year risk of major bleeding in patients with atrial fibrillation: the Euro Heart Survey. Chest 2010; 138: 1093–1100. doi: 10.1378/chest.10-0134. PMID: 20299623.
  158. Lou M., Safdar A., Mehdiratta M. et al. The HAT score: a simple grading scale for predicting hemorrhage after thrombolysis. Neurology 2008; 71: 1417–1423. doi: 10.1212/01.wnl.0000330297.58334.dd. PMID: 18955684.
  159. Marsh E.B., Llinas R.H., Hillis A.E. et al. Hemorrhagic transformation in patients with acute ischaemic stroke and an indication for anticoagulation. Eur J Neurol 2013; 20: 962–967. doi: 10.1111/ene.12126. PMID: 23521544.
  160. Kalinin M.N., Khasanova D.R., Ibatullin M.M. The hemorrhagic transformation index score: a prediction tool in middle cerebral artery ischemic stroke. BMC Neurol 2017; 17: 177. doi: 10.1186/s12883-017-0958-3. PMID: 28882130.
  161. Saposnik G., Fang J., Kapral M.K. et al. The iScore predicts effectiveness of thrombolytic therapy for acute ischemic stroke. Stroke 2012; 43: 1315–1322. doi: 10.1161/STROKEAHA.111.646265. PMID: 22308252.
  162. Strbian D., Engelter S., Michel P. et al. Symptomatic intracranial hemorrhage after stroke thrombolysis: the SEDAN score. Ann Neurol 2012; 71: 634–641. doi: 10.1002/ana.23546. PMID: 22522478.
  163. Mazya M., Egido J.A., Ford G.A. et al. Predicting the risk of symptomatic intracerebral hemorrhage in ischemic stroke treated with intravenous alteplase: Safe Implementation of Treatments in Stroke (SITS) symptomatic intracerebral hemorrhage risk score. Stroke 2012; 43: 1524–1531. doi: 10.1161/STROKEAHA.111.644815. PMID: 22442178.
  164. Flint A.C., Faigeles B.S., Cullen S.P. et al. THRIVE score predicts ischemic stroke outcomes and thrombolytic hemorrhage risk in VISTA. Stroke 2013; 44: 3365–3369. doi: 10.1161/STROKEAHA.113.002794. PMID: 24072004.
  165. Saposnik G., Guzik A.K., Reeves M. et al. Stroke prognostication using age and NIH Stroke Scale: SPAN-100. Neurology 2013; 80: 21–28. doi: 10.1212/WNL.0b013e31827b1ace. PMID: 23175723.

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