Skip to main content
Erschienen in: Translational Stroke Research 3/2013

01.06.2013 | Original Article

Recommendations for Preclinical Research in Hemorrhagic Transformation

verfasst von: Susan C. Fagan, Paul A. Lapchak, David S. Liebeskind, Tauheed Ishrat, Adviye Ergul

Erschienen in: Translational Stroke Research | Ausgabe 3/2013

Einloggen, um Zugang zu erhalten

Abstract

Hemorrhagic transformation (HT) is an important complication of ischemic stroke and is responsible for most of the mortality associated with acute reperfusion therapy. Although many important publications address the preclinical models of ischemic stroke, there are no current recommendations on the conduct of research aimed at understanding the mechanisms and consequences of HT. The purpose of this review is to present the various models used in HT research, the clinical correlates, and the experimental variables known to influence the quantitation of HT in preclinical investigation. Lastly, recommendations for the conduct of preclinical research in HT are provided.
Literatur
1.
Zurück zum Zitat Del Zoppo GJ, Zeumer H, Harker LA. Thrombolytic therapy in stroke: possibilities and hazards. Stroke. 1986;17(4):595–607.PubMedCrossRef Del Zoppo GJ, Zeumer H, Harker LA. Thrombolytic therapy in stroke: possibilities and hazards. Stroke. 1986;17(4):595–607.PubMedCrossRef
2.
Zurück zum Zitat Fiorelli M, Bastianello S, von Kummer R, del Zoppo GJ, Larrue V, Lesaffre E, 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(11):2280–4.PubMedCrossRef Fiorelli M, Bastianello S, von Kummer R, del Zoppo GJ, Larrue V, Lesaffre E, 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(11):2280–4.PubMedCrossRef
3.
Zurück zum Zitat Hacke W, Kaste M, Bluhmki E, Brozman M, Davalos A, Guidetti D, et al. Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N Engl J Med. 2008;359(13):1317–29.PubMedCrossRef Hacke W, Kaste M, Bluhmki E, Brozman M, Davalos A, Guidetti D, et al. Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N Engl J Med. 2008;359(13):1317–29.PubMedCrossRef
4.
Zurück zum Zitat No Author. 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(24):1581–7. No Author. 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(24):1581–7.
5.
Zurück zum Zitat Eissa A, Krass I, Bajorek BV. Optimizing the management of acute ischaemic stroke: a review of the utilization of intravenous recombinant tissue plasminogen activator (tPA). J Clin Pharm Ther. 2012. doi:10.1111/j.1365-2710.2012.01366.x. Eissa A, Krass I, Bajorek BV. Optimizing the management of acute ischaemic stroke: a review of the utilization of intravenous recombinant tissue plasminogen activator (tPA). J Clin Pharm Ther. 2012. doi:10.​1111/​j.​1365-2710.​2012.​01366.​x.
6.
Zurück zum Zitat Heo JH, Lucero J, Abumiya T, Koziol JA, Copeland BR, del Zoppo GJ. Matrix metalloproteinases increase very early during experimental focal cerebral ischemia. J Cereb Blood Flow Metab. 1999;19(6):624–33.PubMedCrossRef Heo JH, Lucero J, Abumiya T, Koziol JA, Copeland BR, del Zoppo GJ. Matrix metalloproteinases increase very early during experimental focal cerebral ischemia. J Cereb Blood Flow Metab. 1999;19(6):624–33.PubMedCrossRef
7.
Zurück zum Zitat del Zoppo GJ, Frankowski H, Gu YH, Osada T, Kanazawa M, Milner R, et al. Microglial cell activation is a source of metalloproteinase generation during hemorrhagic transformation. J Cereb Blood Flow Metab. 2012;32(5):919–32.PubMedCrossRef del Zoppo GJ, Frankowski H, Gu YH, Osada T, Kanazawa M, Milner R, et al. Microglial cell activation is a source of metalloproteinase generation during hemorrhagic transformation. J Cereb Blood Flow Metab. 2012;32(5):919–32.PubMedCrossRef
8.
Zurück zum Zitat Kamijyo Y, Garcia JH, Cooper J. Temporary regional cerebral ischemia in the cat. A model of hemorrhagic and subcortical infarction. J Neuropathol Exp Neurol. 1977;36(2):338–50.PubMedCrossRef Kamijyo Y, Garcia JH, Cooper J. Temporary regional cerebral ischemia in the cat. A model of hemorrhagic and subcortical infarction. J Neuropathol Exp Neurol. 1977;36(2):338–50.PubMedCrossRef
9.
Zurück zum Zitat de Courten-Myers GM, Kleinholz M, Wagner KR, Myers RE. Fatal strokes in hyperglycemic cats. Stroke. 1989;20(12):1707–15.PubMedCrossRef de Courten-Myers GM, Kleinholz M, Wagner KR, Myers RE. Fatal strokes in hyperglycemic cats. Stroke. 1989;20(12):1707–15.PubMedCrossRef
10.
Zurück zum Zitat Lapchak PA, Chapman DF, Zivin JA. Metalloproteinase inhibition reduces thrombolytic (tissue plasminogen activator)-induced hemorrhage after thromboembolic stroke. Stroke. 2000;31(12):3034–40.PubMedCrossRef Lapchak PA, Chapman DF, Zivin JA. Metalloproteinase inhibition reduces thrombolytic (tissue plasminogen activator)-induced hemorrhage after thromboembolic stroke. Stroke. 2000;31(12):3034–40.PubMedCrossRef
11.
Zurück zum Zitat Yenari MA, Lee LK, Beaulieu C, Sun GH, Kunis D, Chang D, et al. Thrombolysis with reteplase, an unglycosylated plasminogen activator variant, in experimental embolic stroke. J Stroke Cerebrovasc Dis. 1998;7(3):179–86.PubMedCrossRef Yenari MA, Lee LK, Beaulieu C, Sun GH, Kunis D, Chang D, et al. Thrombolysis with reteplase, an unglycosylated plasminogen activator variant, in experimental embolic stroke. J Stroke Cerebrovasc Dis. 1998;7(3):179–86.PubMedCrossRef
12.
Zurück zum Zitat Asahi M, Asahi K, Wang X, Lo EH. Reduction of tissue plasminogen activator-induced hemorrhage and brain injury by free radical spin trapping after embolic focal cerebral ischemia in rats. J Cereb Blood Flow Metab. 2000;20(3):452–7.PubMedCrossRef Asahi M, Asahi K, Wang X, Lo EH. Reduction of tissue plasminogen activator-induced hemorrhage and brain injury by free radical spin trapping after embolic focal cerebral ischemia in rats. J Cereb Blood Flow Metab. 2000;20(3):452–7.PubMedCrossRef
13.
Zurück zum Zitat Chen CH, Manaenko A, Zhan Y, Liu WW, Ostrowki RP, Tang J, et al. Hydrogen gas reduced acute hyperglycemia-enhanced hemorrhagic transformation in a focal ischemia rat model. Neuroscience. 2010;169(1):402–14.PubMedCrossRef Chen CH, Manaenko A, Zhan Y, Liu WW, Ostrowki RP, Tang J, et al. Hydrogen gas reduced acute hyperglycemia-enhanced hemorrhagic transformation in a focal ischemia rat model. Neuroscience. 2010;169(1):402–14.PubMedCrossRef
14.
Zurück zum Zitat Sun L, Zhou W, Heiland S, Marti HH, Veltkamp R. A translationally relevant thromboembolic stroke model for the study of secondary hemorrhage after thrombolysis in rats. Brain Res. 2011;1368:346–54.PubMedCrossRef Sun L, Zhou W, Heiland S, Marti HH, Veltkamp R. A translationally relevant thromboembolic stroke model for the study of secondary hemorrhage after thrombolysis in rats. Brain Res. 2011;1368:346–54.PubMedCrossRef
15.
Zurück zum Zitat Qin Z, Karabiyikoglu M, Hua Y, Silbergleit R, He Y, Keep RF, et al. Hyperbaric oxygen-induced attenuation of hemorrhagic transformation after experimental focal transient cerebral ischemia. Stroke. 2007;38(4):1362–7.PubMedCrossRef Qin Z, Karabiyikoglu M, Hua Y, Silbergleit R, He Y, Keep RF, et al. Hyperbaric oxygen-induced attenuation of hemorrhagic transformation after experimental focal transient cerebral ischemia. Stroke. 2007;38(4):1362–7.PubMedCrossRef
16.
Zurück zum Zitat Fagan SC, Kozak A, Hill WD, Pollock DM, Xu L, Johnson MH, et al. Hypertension after experimental cerebral ischemia: candesartan provides neurovascular protection. J Hypertens. 2006;24(3):535–9.PubMedCrossRef Fagan SC, Kozak A, Hill WD, Pollock DM, Xu L, Johnson MH, et al. Hypertension after experimental cerebral ischemia: candesartan provides neurovascular protection. J Hypertens. 2006;24(3):535–9.PubMedCrossRef
17.
Zurück zum Zitat Murata Y, Rosell A, Scannevin RH, Rhodes KJ, Wang X, Lo EH. Extension of the thrombolytic time window with minocycline in experimental stroke. Stroke. 2008;39(12):3372–7.PubMedCrossRef Murata Y, Rosell A, Scannevin RH, Rhodes KJ, Wang X, Lo EH. Extension of the thrombolytic time window with minocycline in experimental stroke. Stroke. 2008;39(12):3372–7.PubMedCrossRef
18.
Zurück zum Zitat Copin JC, Merlani P, Sugawara T, Chan PH, Gasche Y. Delayed matrix metalloproteinase inhibition reduces intracerebral hemorrhage after embolic stroke in rats. Exp Neurol. 2008;213(1):196–201.PubMedCrossRef Copin JC, Merlani P, Sugawara T, Chan PH, Gasche Y. Delayed matrix metalloproteinase inhibition reduces intracerebral hemorrhage after embolic stroke in rats. Exp Neurol. 2008;213(1):196–201.PubMedCrossRef
19.
Zurück zum Zitat Lu A, Clark JF, Broderick JP, Pyne-Geithman GJ, Wagner KR, Khatri P, et al. Mechanical reperfusion is associated with post-ischemic hemorrhage in rat brain. Exp Neurol. 2009;216(2):407–12.PubMedCrossRef Lu A, Clark JF, Broderick JP, Pyne-Geithman GJ, Wagner KR, Khatri P, et al. Mechanical reperfusion is associated with post-ischemic hemorrhage in rat brain. Exp Neurol. 2009;216(2):407–12.PubMedCrossRef
20.
Zurück zum Zitat Hu Q, Ma Q, Zhan Y, He Z, Tang J, Zhou C, et al. Isoflurane enhanced hemorrhagic transformation by impairing antioxidant enzymes in hyperglycemic rats with middle cerebral artery occlusion. Stroke. 2011;42(6):1750–6.PubMedCrossRef Hu Q, Ma Q, Zhan Y, He Z, Tang J, Zhou C, et al. Isoflurane enhanced hemorrhagic transformation by impairing antioxidant enzymes in hyperglycemic rats with middle cerebral artery occlusion. Stroke. 2011;42(6):1750–6.PubMedCrossRef
21.
Zurück zum Zitat Fagan SC, Garcia JH. Hemorrhagic transformation in focal cerebral ischemia: influence of time to artery reopening and tissue plasminogen activator. Pharmacotherapy. 1999;19(2):139–42.PubMedCrossRef Fagan SC, Garcia JH. Hemorrhagic transformation in focal cerebral ischemia: influence of time to artery reopening and tissue plasminogen activator. Pharmacotherapy. 1999;19(2):139–42.PubMedCrossRef
22.
Zurück zum Zitat Fagan SC, Nagaraja TN, Fenstermacher JD, Zheng J, Johnson M, Knight RA. Hemorrhagic transformation is related to the duration of occlusion and treatment with tissue plasminogen activator in a nonembolic stroke model. Neurol Res. 2003;25(4):377–82.PubMedCrossRef Fagan SC, Nagaraja TN, Fenstermacher JD, Zheng J, Johnson M, Knight RA. Hemorrhagic transformation is related to the duration of occlusion and treatment with tissue plasminogen activator in a nonembolic stroke model. Neurol Res. 2003;25(4):377–82.PubMedCrossRef
23.
Zurück zum Zitat Henning EC, Latour LL, Hallenbeck JM, Warach S. Reperfusion-associated hemorrhagic transformation in SHR rats: evidence of symptomatic parenchymal hematoma. Stroke. 2008;39(12):3405–10.PubMedCrossRef Henning EC, Latour LL, Hallenbeck JM, Warach S. Reperfusion-associated hemorrhagic transformation in SHR rats: evidence of symptomatic parenchymal hematoma. Stroke. 2008;39(12):3405–10.PubMedCrossRef
24.
Zurück zum Zitat Crumrine RC, Marder VJ, Taylor GM, Lamanna JC, Tsipis CP, Scuderi P, et al. Intra-arterial administration of recombinant tissue-type plasminogen activator (rt-PA) causes more intracranial bleeding than does intravenous rt-PA in a transient rat middle cerebral artery occlusion model. Exp Transl Stroke Med. 2011;3(1):10.PubMedCrossRef Crumrine RC, Marder VJ, Taylor GM, Lamanna JC, Tsipis CP, Scuderi P, et al. Intra-arterial administration of recombinant tissue-type plasminogen activator (rt-PA) causes more intracranial bleeding than does intravenous rt-PA in a transient rat middle cerebral artery occlusion model. Exp Transl Stroke Med. 2011;3(1):10.PubMedCrossRef
25.
Zurück zum Zitat Choudhri TF, Hoh BL, Solomon RA, Connolly Jr ES, Pinsky DJ. Use of a spectrophotometric hemoglobin assay to objectively quantify intracerebral hemorrhage in mice. Stroke. 1997;28(11):2296–302.PubMedCrossRef Choudhri TF, Hoh BL, Solomon RA, Connolly Jr ES, Pinsky DJ. Use of a spectrophotometric hemoglobin assay to objectively quantify intracerebral hemorrhage in mice. Stroke. 1997;28(11):2296–302.PubMedCrossRef
26.
Zurück zum Zitat Jia L, Chopp M, Zhang L, Lu M, Zhang Z. Erythropoietin in combination of tissue plasminogen activator exacerbates brain hemorrhage when treatment is initiated 6 hours after stroke. Stroke. 2010;41(9):2071–6.PubMedCrossRef Jia L, Chopp M, Zhang L, Lu M, Zhang Z. Erythropoietin in combination of tissue plasminogen activator exacerbates brain hemorrhage when treatment is initiated 6 hours after stroke. Stroke. 2010;41(9):2071–6.PubMedCrossRef
27.
Zurück zum Zitat Ishiguro M, Kawasaki K, Suzuki Y, Ishizuka F, Mishiro K, Egashira Y, et al. A Rho kinase (ROCK) inhibitor, fasudil, prevents matrix metalloproteinase-9-related hemorrhagic transformation in mice treated with tissue plasminogen activator. Neuroscience. 2012;220:302–12.PubMedCrossRef Ishiguro M, Kawasaki K, Suzuki Y, Ishizuka F, Mishiro K, Egashira Y, et al. A Rho kinase (ROCK) inhibitor, fasudil, prevents matrix metalloproteinase-9-related hemorrhagic transformation in mice treated with tissue plasminogen activator. Neuroscience. 2012;220:302–12.PubMedCrossRef
28.
Zurück zum Zitat Yenari MA, Xu L, Tang XN, Qiao Y, Giffard RG. Microglia potentiate damage to blood–brain barrier constituents: improvement by minocycline in vivo and in vitro. Stroke. 2006;37(4):1087–93.PubMedCrossRef Yenari MA, Xu L, Tang XN, Qiao Y, Giffard RG. Microglia potentiate damage to blood–brain barrier constituents: improvement by minocycline in vivo and in vitro. Stroke. 2006;37(4):1087–93.PubMedCrossRef
29.
Zurück zum Zitat McColl BW, Rose N, Robson FH, Rothwell NJ, Lawrence CB. Increased brain microvascular MMP-9 and incidence of haemorrhagic transformation in obese mice after experimental stroke. J Cereb Blood Flow Metab. 2010;30(2):267–72.PubMedCrossRef McColl BW, Rose N, Robson FH, Rothwell NJ, Lawrence CB. Increased brain microvascular MMP-9 and incidence of haemorrhagic transformation in obese mice after experimental stroke. J Cereb Blood Flow Metab. 2010;30(2):267–72.PubMedCrossRef
30.
Zurück zum Zitat Ishiguro M, Mishiro K, Fujiwara Y, Chen H, Izuta H, Tsuruma K, et al. Phosphodiesterase-III inhibitor prevents hemorrhagic transformation induced by focal cerebral ischemia in mice treated with tPA. PLoS One. 2010;5(12):e15178.PubMedCrossRef Ishiguro M, Mishiro K, Fujiwara Y, Chen H, Izuta H, Tsuruma K, et al. Phosphodiesterase-III inhibitor prevents hemorrhagic transformation induced by focal cerebral ischemia in mice treated with tPA. PLoS One. 2010;5(12):e15178.PubMedCrossRef
31.
Zurück zum Zitat Haddad M, Beray-Berthat V, Coqueran B, Palmier B, Szabo C, Plotkine M, et al. Reduction of hemorrhagic transformation by PJ34, a poly(ADP-ribose)polymerase inhibitor, after permanent focal cerebral ischemia in mice. Eur J Pharmacol. 2008;588(1):52–7.PubMedCrossRef Haddad M, Beray-Berthat V, Coqueran B, Palmier B, Szabo C, Plotkine M, et al. Reduction of hemorrhagic transformation by PJ34, a poly(ADP-ribose)polymerase inhibitor, after permanent focal cerebral ischemia in mice. Eur J Pharmacol. 2008;588(1):52–7.PubMedCrossRef
32.
Zurück zum Zitat Garcia-Yebenes I, Sobrado M, Zarruk JG, Castellanos M, de la Perez OS, Davalos A, et al. A mouse model of hemorrhagic transformation by delayed tissue plasminogen activator administration after in situ thromboembolic stroke. Stroke. 2011;42(1):196–203.PubMedCrossRef Garcia-Yebenes I, Sobrado M, Zarruk JG, Castellanos M, de la Perez OS, Davalos A, et al. A mouse model of hemorrhagic transformation by delayed tissue plasminogen activator administration after in situ thromboembolic stroke. Stroke. 2011;42(1):196–203.PubMedCrossRef
33.
Zurück zum Zitat Howells DW, Porritt MJ, Rewell SS, O’Collins V, Sena ES, van der Worp HB, et al. Different strokes for different folks: the rich diversity of animal models of focal cerebral ischemia. J Cereb Blood Flow Metab. 2010;30(8):1412–31.PubMedCrossRef Howells DW, Porritt MJ, Rewell SS, O’Collins V, Sena ES, van der Worp HB, et al. Different strokes for different folks: the rich diversity of animal models of focal cerebral ischemia. J Cereb Blood Flow Metab. 2010;30(8):1412–31.PubMedCrossRef
34.
Zurück zum Zitat Bacigaluppi M, Comi G, Hermann DM. Animal models of ischemic stroke. Part two: modeling cerebral ischemia. Open Neurol J. 2010;4:34–8.PubMed Bacigaluppi M, Comi G, Hermann DM. Animal models of ischemic stroke. Part two: modeling cerebral ischemia. Open Neurol J. 2010;4:34–8.PubMed
35.
Zurück zum Zitat Guan W, Kozak A, El-Remessy AB, Johnson MH, Pillai BA, Fagan SC. Acute treatment with candesartan reduces early injury after permanent middle cerebral artery occlusion. Transl Stroke Res. 2011;2(2):179–85.PubMedCrossRef Guan W, Kozak A, El-Remessy AB, Johnson MH, Pillai BA, Fagan SC. Acute treatment with candesartan reduces early injury after permanent middle cerebral artery occlusion. Transl Stroke Res. 2011;2(2):179–85.PubMedCrossRef
36.
Zurück zum Zitat Bowes MP, Zivin JA, Thomas GR, Thibodeaux H, Fagan SC. Acute hypertension, but not thrombolysis, increases the incidence and severity of hemorrhagic transformation following experimental stroke in rabbits. Exp Neurol. 1996;141(1):40–6.PubMedCrossRef Bowes MP, Zivin JA, Thomas GR, Thibodeaux H, Fagan SC. Acute hypertension, but not thrombolysis, increases the incidence and severity of hemorrhagic transformation following experimental stroke in rabbits. Exp Neurol. 1996;141(1):40–6.PubMedCrossRef
37.
Zurück zum Zitat Elewa HF, Kozak A, Johnson MH, Ergul A, Fagan SC. Blood pressure lowering after experimental cerebral ischemia provides neurovascular protection. J Hypertens. 2007;25(4):855–9.PubMedCrossRef Elewa HF, Kozak A, Johnson MH, Ergul A, Fagan SC. Blood pressure lowering after experimental cerebral ischemia provides neurovascular protection. J Hypertens. 2007;25(4):855–9.PubMedCrossRef
38.
Zurück zum Zitat Guan W, Kozak A, Fagan SC. Drug repurposing for vascular protection after acute ischemic stroke. Acta Neurochir Suppl. 2011;111:295–8.PubMedCrossRef Guan W, Kozak A, Fagan SC. Drug repurposing for vascular protection after acute ischemic stroke. Acta Neurochir Suppl. 2011;111:295–8.PubMedCrossRef
39.
Zurück zum Zitat Kozak W, Kozak A, Johnson MH, Elewa HF, Fagan SC. Vascular protection with candesartan after experimental acute stroke in hypertensive rats: a dose–response study. J Pharmacol Exp Ther. 2008;326(3):773–82.PubMedCrossRef Kozak W, Kozak A, Johnson MH, Elewa HF, Fagan SC. Vascular protection with candesartan after experimental acute stroke in hypertensive rats: a dose–response study. J Pharmacol Exp Ther. 2008;326(3):773–82.PubMedCrossRef
40.
Zurück zum Zitat Ergul A, Elgebaly MM, Middlemore ML, Li W, Elewa H, Switzer JA, et al. Increased hemorrhagic transformation and altered infarct size and localization after experimental stroke in a rat model type 2 diabetes. BMC Neurol. 2007;7:33.PubMedCrossRef Ergul A, Elgebaly MM, Middlemore ML, Li W, Elewa H, Switzer JA, et al. Increased hemorrhagic transformation and altered infarct size and localization after experimental stroke in a rat model type 2 diabetes. BMC Neurol. 2007;7:33.PubMedCrossRef
41.
Zurück zum Zitat Elgebaly MM, Ogbi S, Li W, Mezzetti EM, Prakash R, Johnson MH, et al. Neurovascular injury in acute hyperglycemia and diabetes: a comparative analysis in experimental stroke. Transl Stroke Res. 2011;2(3):391–8.PubMedCrossRef Elgebaly MM, Ogbi S, Li W, Mezzetti EM, Prakash R, Johnson MH, et al. Neurovascular injury in acute hyperglycemia and diabetes: a comparative analysis in experimental stroke. Transl Stroke Res. 2011;2(3):391–8.PubMedCrossRef
42.
Zurück zum Zitat Elgebaly MM, Prakash R, Li W, Ogbi S, Johnson MH, Mezzetti EM, et al. Vascular protection in diabetic stroke: role of matrix metalloprotease-dependent vascular remodeling. J Cereb Blood Flow Metab. 2010;30(12):1928–38.PubMedCrossRef Elgebaly MM, Prakash R, Li W, Ogbi S, Johnson MH, Mezzetti EM, et al. Vascular protection in diabetic stroke: role of matrix metalloprotease-dependent vascular remodeling. J Cereb Blood Flow Metab. 2010;30(12):1928–38.PubMedCrossRef
43.
Zurück zum Zitat Lo EH. Experimental models, neurovascular mechanisms and translational issues in stroke research. Br J Pharmacol. 2008;153 Suppl 1:S396–405.PubMed Lo EH. Experimental models, neurovascular mechanisms and translational issues in stroke research. Br J Pharmacol. 2008;153 Suppl 1:S396–405.PubMed
44.
Zurück zum Zitat Kozak A, Ergul A, El-Remessy AB, Johnson MH, Machado LS, Elewa HF, et al. Candesartan augments ischemia-induced proangiogenic state and results in sustained improvement after stroke. Stroke. 2009;40(5):1870–6.PubMedCrossRef Kozak A, Ergul A, El-Remessy AB, Johnson MH, Machado LS, Elewa HF, et al. Candesartan augments ischemia-induced proangiogenic state and results in sustained improvement after stroke. Stroke. 2009;40(5):1870–6.PubMedCrossRef
45.
Zurück zum Zitat de Courten-Myers GM, Kleinholz M, Holm P, DeVoe G, Schmitt G, Wagner KR, et al. Hemorrhagic infarct conversion in experimental stroke. Ann Emerg Med. 1992;21(2):120–6.PubMedCrossRef de Courten-Myers GM, Kleinholz M, Holm P, DeVoe G, Schmitt G, Wagner KR, et al. Hemorrhagic infarct conversion in experimental stroke. Ann Emerg Med. 1992;21(2):120–6.PubMedCrossRef
46.
Zurück zum Zitat Tejima E, Katayama Y, Suzuki Y, Kano T, Lo EH. Hemorrhagic transformation after fibrinolysis with tissue plasminogen activator: evaluation of role of hypertension with rat thromboembolic stroke model. Stroke. 2001;32(6):1336–40.PubMedCrossRef Tejima E, Katayama Y, Suzuki Y, Kano T, Lo EH. Hemorrhagic transformation after fibrinolysis with tissue plasminogen activator: evaluation of role of hypertension with rat thromboembolic stroke model. Stroke. 2001;32(6):1336–40.PubMedCrossRef
47.
Zurück zum Zitat Zhang F, Wang S, Luo Y, Ji X, Nemoto EM, Chen J. When hypothermia meets hypotension and hyperglycemia: the diverse effects of adenosine 5′-monophosphate on cerebral ischemia in rats. J Cereb Blood Flow Metab. 2009;29(5):1022–34.PubMedCrossRef Zhang F, Wang S, Luo Y, Ji X, Nemoto EM, Chen J. When hypothermia meets hypotension and hyperglycemia: the diverse effects of adenosine 5′-monophosphate on cerebral ischemia in rats. J Cereb Blood Flow Metab. 2009;29(5):1022–34.PubMedCrossRef
48.
Zurück zum Zitat Zhang L, Zhang ZG, Zhang RL, Lu M, Adams J, Elliott PJ, et al. Postischemic (6-hour) treatment with recombinant human tissue plasminogen activator and proteasome inhibitor PS-519 reduces infarction in a rat model of embolic focal cerebral ischemia. Stroke. 2001;32(12):2926–31.PubMedCrossRef Zhang L, Zhang ZG, Zhang RL, Lu M, Adams J, Elliott PJ, et al. Postischemic (6-hour) treatment with recombinant human tissue plasminogen activator and proteasome inhibitor PS-519 reduces infarction in a rat model of embolic focal cerebral ischemia. Stroke. 2001;32(12):2926–31.PubMedCrossRef
49.
Zurück zum Zitat Lapchak PA. A clinically relevant rabbit embolic stroke model for acute ischemic stroke therapy development: mechanisms and targets. In: Lapchak PA, Zhang JH, editors. Translational stroke research: from target selection to clinical trials. New York: Springer Series in Translational Stroke Research: Springer; 2012. p. 541–84.CrossRef Lapchak PA. A clinically relevant rabbit embolic stroke model for acute ischemic stroke therapy development: mechanisms and targets. In: Lapchak PA, Zhang JH, editors. Translational stroke research: from target selection to clinical trials. New York: Springer Series in Translational Stroke Research: Springer; 2012. p. 541–84.CrossRef
50.
Zurück zum Zitat Dijkhuizen RM, Asahi M, Wu O, Rosen BR, Lo EH. Rapid breakdown of microvascular barriers and subsequent hemorrhagic transformation after delayed recombinant tissue plasminogen activator treatment in a rat embolic stroke model. Stroke. 2002;33(8):2100–4.PubMedCrossRef Dijkhuizen RM, Asahi M, Wu O, Rosen BR, Lo EH. Rapid breakdown of microvascular barriers and subsequent hemorrhagic transformation after delayed recombinant tissue plasminogen activator treatment in a rat embolic stroke model. Stroke. 2002;33(8):2100–4.PubMedCrossRef
51.
Zurück zum Zitat Hornig CR, Dorndorf W, Agnoli AL. Hemorrhagic cerebral infarction—a prospective study. Stroke. 1986;17(2):179–85.PubMedCrossRef Hornig CR, Dorndorf W, Agnoli AL. Hemorrhagic cerebral infarction—a prospective study. Stroke. 1986;17(2):179–85.PubMedCrossRef
52.
Zurück zum Zitat Renou P, Sibon I, Tourdias T, Rouanet F, Rosso C, Galanaud D, et al. Reliability of the ECASS radiological classification of postthrombolysis brain haemorrhage: a comparison of CT and three MRI sequences. Cerebrovasc Dis. 2010;29(6):597–604.PubMedCrossRef Renou P, Sibon I, Tourdias T, Rouanet F, Rosso C, Galanaud D, et al. Reliability of the ECASS radiological classification of postthrombolysis brain haemorrhage: a comparison of CT and three MRI sequences. Cerebrovasc Dis. 2010;29(6):597–604.PubMedCrossRef
53.
Zurück zum Zitat Lapchak PA. Translational stroke research using a rabbit embolic stroke model: a correlative analysis hypothesis for novel therapy development. Transl Stroke Res. 2010;1(2):96–107.PubMedCrossRef Lapchak PA. Translational stroke research using a rabbit embolic stroke model: a correlative analysis hypothesis for novel therapy development. Transl Stroke Res. 2010;1(2):96–107.PubMedCrossRef
54.
Zurück zum Zitat Turner RJ, Jickling GC, Sharp FR. Are underlying assumptions of current animal models of human stroke correct: from STAIRs to high hurdles? Transl Stroke Res. 2011;2(2):138–43.PubMedCrossRef Turner RJ, Jickling GC, Sharp FR. Are underlying assumptions of current animal models of human stroke correct: from STAIRs to high hurdles? Transl Stroke Res. 2011;2(2):138–43.PubMedCrossRef
55.
Zurück zum Zitat Machado LS, Sazonova IY, Kozak A, Wiley DC, El-Remessy AB, Ergul A, et al. Minocycline and tissue-type plasminogen activator for stroke: assessment of interaction potential. Stroke. 2009;40(9):3028–33.PubMedCrossRef Machado LS, Sazonova IY, Kozak A, Wiley DC, El-Remessy AB, Ergul A, et al. Minocycline and tissue-type plasminogen activator for stroke: assessment of interaction potential. Stroke. 2009;40(9):3028–33.PubMedCrossRef
56.
Zurück zum Zitat Park JH, Ko Y, Kim WJ, Jang MS, Yang MH, Han MK, et al. Is asymptomatic hemorrhagic transformation really innocuous? Neurology. 2012;78(6):421–6.PubMedCrossRef Park JH, Ko Y, Kim WJ, Jang MS, Yang MH, Han MK, et al. Is asymptomatic hemorrhagic transformation really innocuous? Neurology. 2012;78(6):421–6.PubMedCrossRef
57.
Zurück zum Zitat Copin JC, Gasche Y. Effect of the duration of middle cerebral artery occlusion on the risk of hemorrhagic transformation after tissue plasminogen activator injection in rats. Brain Res. 2008;1243:161–6.PubMedCrossRef Copin JC, Gasche Y. Effect of the duration of middle cerebral artery occlusion on the risk of hemorrhagic transformation after tissue plasminogen activator injection in rats. Brain Res. 2008;1243:161–6.PubMedCrossRef
Metadaten
Titel
Recommendations for Preclinical Research in Hemorrhagic Transformation
verfasst von
Susan C. Fagan
Paul A. Lapchak
David S. Liebeskind
Tauheed Ishrat
Adviye Ergul
Publikationsdatum
01.06.2013
Verlag
Springer-Verlag
Erschienen in
Translational Stroke Research / Ausgabe 3/2013
Print ISSN: 1868-4483
Elektronische ISSN: 1868-601X
DOI
https://doi.org/10.1007/s12975-012-0222-5

Weitere Artikel der Ausgabe 3/2013

Translational Stroke Research 3/2013 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.