Skip to main content
Top
Published in: Translational Stroke Research 4/2016

01-08-2016 | SI: Challenges and Controversies in Translational Stroke Research

Improving Reperfusion Therapies in the Era of Mechanical Thrombectomy

Authors: Italo Linfante, Marilyn J. Cipolla

Published in: Translational Stroke Research | Issue 4/2016

Login to get access

Abstract

Recent positive clinical trials using mechanical thrombectomy proved that endovascular recanalization is an effective treatment for patients with acute stroke secondary to large vessel occlusions. The trials offer definite evidence that in acute ischemia recanalization is a powerful predictor of good outcome. However, even in the era of rapid and effective recanalization using endovascular approaches, the percentage of patients with good outcomes varies between 33 and 71 %. In addition, the number of patients who are eligible for endovascular thrombectomy is small and usually based on having salvageable tissue on imaging. There is therefore room for improvement to both enhance the effectiveness of current practice and expand treatment to a larger subset of stroke patients. In this review, we highlight some of the most promising approaches to improve endovascular therapy by combining with strategies to enhance collateral perfusion and vascular protection.
Literature
1.
go back to reference Berkhemer OA, Fransen PS, Beumer D, van den Berg LA, Lingsma HF, Yoo AJ, et al. A randomized trial of intraarterial treatment for acute ischemic stroke. N Engl J Med. 2015;372:11–20.CrossRefPubMed Berkhemer OA, Fransen PS, Beumer D, van den Berg LA, Lingsma HF, Yoo AJ, et al. A randomized trial of intraarterial treatment for acute ischemic stroke. N Engl J Med. 2015;372:11–20.CrossRefPubMed
2.
go back to reference Goyal M, Demchuk AM, Menon BK, Eesa M, Rempel JL, Thornton J, et al. Randomized assessment of rapid endovascular treatment of ischemic stroke. N Engl J Med. 2015;372:1019–30.CrossRefPubMed Goyal M, Demchuk AM, Menon BK, Eesa M, Rempel JL, Thornton J, et al. Randomized assessment of rapid endovascular treatment of ischemic stroke. N Engl J Med. 2015;372:1019–30.CrossRefPubMed
3.
go back to reference Campbell BC, Mitchell PJ, Kleinig TJ, Dewey HM, Churilov L, Yassi N, et al. Endovascular therapy for ischemic stroke with perfusion-imaging selection. N Engl J Med. 2015;372:1009–18.CrossRefPubMed Campbell BC, Mitchell PJ, Kleinig TJ, Dewey HM, Churilov L, Yassi N, et al. Endovascular therapy for ischemic stroke with perfusion-imaging selection. N Engl J Med. 2015;372:1009–18.CrossRefPubMed
4.
go back to reference Saver JL, Goyal M, Bonafe A, Diener HC, Levy EI, Pereira VM, et al. Stent-retriever thrombectomy after intravenous t-PA vs. t-PA alone in stroke. N Engl J Med. 2015;372:2285–95.CrossRefPubMed Saver JL, Goyal M, Bonafe A, Diener HC, Levy EI, Pereira VM, et al. Stent-retriever thrombectomy after intravenous t-PA vs. t-PA alone in stroke. N Engl J Med. 2015;372:2285–95.CrossRefPubMed
5.
go back to reference Jovin TG, Chamorro A, Cobo E, de Miquel MA, Molina CA, Rovira A, et al. Thrombectomy within 8 hours after symptom onset in ischemic stroke. N Engl J Med. 2015;372:2296–306.CrossRefPubMed Jovin TG, Chamorro A, Cobo E, de Miquel MA, Molina CA, Rovira A, et al. Thrombectomy within 8 hours after symptom onset in ischemic stroke. N Engl J Med. 2015;372:2296–306.CrossRefPubMed
6.
go back to reference Dirnagl U, Endres M. Found in translation: preclinical stroke research predicts human pathophysiology, clinical phenotypes, and therapeutic outcomes. Stroke. 2014;45:1510–8.CrossRefPubMed Dirnagl U, Endres M. Found in translation: preclinical stroke research predicts human pathophysiology, clinical phenotypes, and therapeutic outcomes. Stroke. 2014;45:1510–8.CrossRefPubMed
7.
go back to reference Cumberland Consensus Working Group 1, Cheeran B, Cohen L, Dobkin B, Ford G, Greenwood R, et al. The future of restorative neurosciences in stroke: driving the translational research pipeline from basic science to rehabilitation of people after stroke. Neurorehabil Neural Repair. 2009;23:97–107.CrossRef Cumberland Consensus Working Group 1, Cheeran B, Cohen L, Dobkin B, Ford G, Greenwood R, et al. The future of restorative neurosciences in stroke: driving the translational research pipeline from basic science to rehabilitation of people after stroke. Neurorehabil Neural Repair. 2009;23:97–107.CrossRef
8.
9.
go back to reference Paciaroni M, Caso V, Agnelli G. The concept of ischemic penumbra in acute stroke and therapeutic opportunities. Eur Neurol. 2009;61:321–30.CrossRefPubMed Paciaroni M, Caso V, Agnelli G. The concept of ischemic penumbra in acute stroke and therapeutic opportunities. Eur Neurol. 2009;61:321–30.CrossRefPubMed
10.
go back to reference The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. Tissue plasminogen activator for acute ischemic stroke. N Engl J Med. 1995;333:1581–7.CrossRef The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. Tissue plasminogen activator for acute ischemic stroke. N Engl J Med. 1995;333:1581–7.CrossRef
11.
go back to reference Ciccone A, Valvassori L, Nichelatti M, Sgoifo A, Ponzio M, Sterzi R, et al. Endovascular treatment for acute ischemic stroke. N Engl J Med. 2013;368:2433–4.CrossRefPubMed Ciccone A, Valvassori L, Nichelatti M, Sgoifo A, Ponzio M, Sterzi R, et al. Endovascular treatment for acute ischemic stroke. N Engl J Med. 2013;368:2433–4.CrossRefPubMed
12.
go back to reference Broderick JP, Palesch YY, Demchuk AM, Yeatts SD, Khatri P, Hill MD, et al. Interventional Management of Stroke (IMS) III Investigators Endovascular therapy after intravenous t-PA versus t-PA alone for stroke. N Engl J Med. 2013;368:893–903.CrossRefPubMedPubMedCentral Broderick JP, Palesch YY, Demchuk AM, Yeatts SD, Khatri P, Hill MD, et al. Interventional Management of Stroke (IMS) III Investigators Endovascular therapy after intravenous t-PA versus t-PA alone for stroke. N Engl J Med. 2013;368:893–903.CrossRefPubMedPubMedCentral
13.
go back to reference Kidwell CS, Jahan R, Gornbein J, Alger JR, Nenov V, Ajani Z, et al. A trial of imaging selection and endovascular treatment for ischemic stroke. N Engl J Med. 2013;368:914–23.CrossRefPubMedPubMedCentral Kidwell CS, Jahan R, Gornbein J, Alger JR, Nenov V, Ajani Z, et al. A trial of imaging selection and endovascular treatment for ischemic stroke. N Engl J Med. 2013;368:914–23.CrossRefPubMedPubMedCentral
14.
go back to reference Liebeskind DS, Jahan R, Nogueira RG, Zaidat OO, Saver JL, SWIFT Investigators. Impact of collaterals on successful revascularization in solitaire FR with the intention for thrombectomy. Stroke. 2014;45:2036–40.CrossRefPubMedPubMedCentral Liebeskind DS, Jahan R, Nogueira RG, Zaidat OO, Saver JL, SWIFT Investigators. Impact of collaterals on successful revascularization in solitaire FR with the intention for thrombectomy. Stroke. 2014;45:2036–40.CrossRefPubMedPubMedCentral
15.
go back to reference Lima FO, Furie KL, Silva GS, Lev MH, Camargo EC, Singhal AB, et al. The pattern of leptomeningeal collaterals on CT angiography is a strong predictor of long-term functional outcome in stroke patients with large vessel intracranial occlusion. Stroke. 2010;41:2316–22. Lima FO, Furie KL, Silva GS, Lev MH, Camargo EC, Singhal AB, et al. The pattern of leptomeningeal collaterals on CT angiography is a strong predictor of long-term functional outcome in stroke patients with large vessel intracranial occlusion. Stroke. 2010;41:2316–22.
16.
go back to reference Bang OY, Saver JL, Kim SJ, Kim GM, Chung CS, Ovbiagele B, et al. Collateral flow predicts response to endovascular therapy for acute ischemic stroke. Stroke. 2011;42:693–9.CrossRefPubMedPubMedCentral Bang OY, Saver JL, Kim SJ, Kim GM, Chung CS, Ovbiagele B, et al. Collateral flow predicts response to endovascular therapy for acute ischemic stroke. Stroke. 2011;42:693–9.CrossRefPubMedPubMedCentral
17.
18.
go back to reference Marks MP, Lansberg MG, Mlynash M, Olivot JM, Straka M, Kemp S, et al. 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.CrossRefPubMedPubMedCentral Marks MP, Lansberg MG, Mlynash M, Olivot JM, Straka M, Kemp S, et al. 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.CrossRefPubMedPubMedCentral
19.
go back to reference Bang OY, Saver JL, Buck BH, Alger JR, Starkman S, Ovbiagele B, et al. Impact of collateral flow on tissue fate in acute ischaemic stroke. J Neurol Neurosurg Psychiatry. 2008;79:625–9.CrossRefPubMed Bang OY, Saver JL, Buck BH, Alger JR, Starkman S, Ovbiagele B, et al. Impact of collateral flow on tissue fate in acute ischaemic stroke. J Neurol Neurosurg Psychiatry. 2008;79:625–9.CrossRefPubMed
20.
go back to reference Campbell BC, Christensen S, Tress BM, Churilov L, Desmond PM, Parsons MW, et al. Failure of collateral blood flow is associated with infarct growth in ischemic stroke. J Cereb Blood Flow Metab. 2013;33:1168–72.CrossRefPubMedPubMedCentral Campbell BC, Christensen S, Tress BM, Churilov L, Desmond PM, Parsons MW, et al. Failure of collateral blood flow is associated with infarct growth in ischemic stroke. J Cereb Blood Flow Metab. 2013;33:1168–72.CrossRefPubMedPubMedCentral
21.
go back to reference Bang OY, Saver JL, Kim SJ, Kim GM, Chung CS, Ovbiagele B, et al. Collateral flow averts hemorrhagic transformation after endovascular therapy for acute ischemic stroke. Stroke. 2011;42:2235–9.CrossRefPubMed Bang OY, Saver JL, Kim SJ, Kim GM, Chung CS, Ovbiagele B, et al. Collateral flow averts hemorrhagic transformation after endovascular therapy for acute ischemic stroke. Stroke. 2011;42:2235–9.CrossRefPubMed
22.
go back to reference Brozici M, van der Zwan A, Hillen B. Anatomy and functionality of leptomeningieal anastomoses: a review. Stroke. 2003;34:2750–62.CrossRefPubMed Brozici M, van der Zwan A, Hillen B. Anatomy and functionality of leptomeningieal anastomoses: a review. Stroke. 2003;34:2750–62.CrossRefPubMed
23.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
24.
go back to reference Zhang H, Prabhakar P, Sealock R, Faber JE. Wide genetic variation in the native pial collateral circulation is a major determinant of variation in severity of stroke. J Cereb Blood Flow Metab. 2010;30:923–34.CrossRefPubMedPubMedCentral Zhang H, Prabhakar P, Sealock R, Faber JE. Wide genetic variation in the native pial collateral circulation is a major determinant of variation in severity of stroke. J Cereb Blood Flow Metab. 2010;30:923–34.CrossRefPubMedPubMedCentral
25.
go back to reference Chan S-L, Sweet JG, Bishop N, Cipolla MJ. Pial collateral reactivity during hypertension and aging: understanding the function of collaterals for stroke therapy. Stroke. 2016. Chan S-L, Sweet JG, Bishop N, Cipolla MJ. Pial collateral reactivity during hypertension and aging: understanding the function of collaterals for stroke therapy. Stroke. 2016.
26.
go back to reference Hedera P, Bujdáková J, Traubner P, Pancák J. Stroke risk factors and development of collateral flow in carotid occlusive disease. Acta Neurol Scand. 1998;98:182–6.CrossRefPubMed Hedera P, Bujdáková J, Traubner P, Pancák J. Stroke risk factors and development of collateral flow in carotid occlusive disease. Acta Neurol Scand. 1998;98:182–6.CrossRefPubMed
27.
go back to reference Letourneur A, Roussel S, Toutain J, Bernaudin M, Touzani O. Impact of genetic and renovascular chronic arterial hypertension on the acute spatiotemporal evolution of the ischemic penumbra: a sequential study with MRI in the rat. J Cereb Blood Flow Metab. 2011;31:504–13.CrossRefPubMed Letourneur A, Roussel S, Toutain J, Bernaudin M, Touzani O. Impact of genetic and renovascular chronic arterial hypertension on the acute spatiotemporal evolution of the ischemic penumbra: a sequential study with MRI in the rat. J Cereb Blood Flow Metab. 2011;31:504–13.CrossRefPubMed
28.
go back to reference McCabe C, Gallagher L, Gsell W, Graham D, Dominiczak AF, Macrae IM. Differences in the evolution of the ischemic penumbra in stroke-prone spontaneously hypertensive and Wistar-Kyoto rats. Stroke. 2009;40:3864–8.CrossRefPubMedPubMedCentral McCabe C, Gallagher L, Gsell W, Graham D, Dominiczak AF, Macrae IM. Differences in the evolution of the ischemic penumbra in stroke-prone spontaneously hypertensive and Wistar-Kyoto rats. Stroke. 2009;40:3864–8.CrossRefPubMedPubMedCentral
29.
go back to reference Satoh K, Fukumoto Y, Shimokawa H. Rho-kinase: important new therapeutic target in cardiovascular diseases. Am J Physiol Heart Circ Physiol. 2011;301:H287–96.CrossRefPubMed Satoh K, Fukumoto Y, Shimokawa H. Rho-kinase: important new therapeutic target in cardiovascular diseases. Am J Physiol Heart Circ Physiol. 2011;301:H287–96.CrossRefPubMed
30.
go back to reference Faraci FM, Lamping KG, Modrick ML, Ryan MJ, Sigmund CD, Didion SP. Cerebral vascular effects of angiotensin II: new insights from genetic models. J Cereb Blood Flow Metab. 2006;26:449–55.CrossRefPubMed Faraci FM, Lamping KG, Modrick ML, Ryan MJ, Sigmund CD, Didion SP. Cerebral vascular effects of angiotensin II: new insights from genetic models. J Cereb Blood Flow Metab. 2006;26:449–55.CrossRefPubMed
31.
go back to reference Davies SP, Reddy H, Caivano M, Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J. 2000;351:95–105.CrossRefPubMedPubMedCentral Davies SP, Reddy H, Caivano M, Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J. 2000;351:95–105.CrossRefPubMedPubMedCentral
32.
go back to reference Laufs U, Endres M, Stagliano N, Amin-Hanjani S, Chui DS, Yang SX, et al. Neuroprotection mediated by changes in the endothelial actin cytoskeleton. J Clin Invest. 2000;106:15–24.CrossRefPubMedPubMedCentral Laufs U, Endres M, Stagliano N, Amin-Hanjani S, Chui DS, Yang SX, et al. Neuroprotection mediated by changes in the endothelial actin cytoskeleton. J Clin Invest. 2000;106:15–24.CrossRefPubMedPubMedCentral
33.
go back to reference Nishikawa Y, Doi M, Koji T, Watanabe M, Kimura S, Kawasaki S, et al. The role of rho and rho-dependent kinase in serotonin-induced contraction observed in bovine middle cerebral artery. Tohoku J Exp Med. 2003;201:239–49.CrossRefPubMed Nishikawa Y, Doi M, Koji T, Watanabe M, Kimura S, Kawasaki S, et al. The role of rho and rho-dependent kinase in serotonin-induced contraction observed in bovine middle cerebral artery. Tohoku J Exp Med. 2003;201:239–49.CrossRefPubMed
34.
go back to reference Shin HK, Huang PL, Ayata C. Rho-kinase inhibition improves ischemic perfusion deficit in hyperlipidemic mice. J Cereb Blood Flow Metab. 2014;34:284–7.CrossRefPubMed Shin HK, Huang PL, Ayata C. Rho-kinase inhibition improves ischemic perfusion deficit in hyperlipidemic mice. J Cereb Blood Flow Metab. 2014;34:284–7.CrossRefPubMed
35.
go back to reference Shin HK, Salomone S, Potts EM, Lee SW, Millican E, Noma K, et al. Rho-kinase inhibition acutely augments blood flow in focal cerebral ischemia via endothelial mechanisms. J Cereb Blood Flow Metab. 2007;27:998–1009.PubMed Shin HK, Salomone S, Potts EM, Lee SW, Millican E, Noma K, et al. Rho-kinase inhibition acutely augments blood flow in focal cerebral ischemia via endothelial mechanisms. J Cereb Blood Flow Metab. 2007;27:998–1009.PubMed
37.
go back to reference Wu J, Li J, Hu H, Liu P, Fang Y, Wu D. Rho-kinase inhibitor, fasudil, prevents neuronal apoptosis via the Akt activation and PTEN inactivation in the ischemic penumbra of rat brain. Cell Mol Neurobiol. 2012;32:1187–97.CrossRefPubMed Wu J, Li J, Hu H, Liu P, Fang Y, Wu D. Rho-kinase inhibitor, fasudil, prevents neuronal apoptosis via the Akt activation and PTEN inactivation in the ischemic penumbra of rat brain. Cell Mol Neurobiol. 2012;32:1187–97.CrossRefPubMed
38.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
39.
go back to reference Lee JH, Zheng Y, von Bornstadt D, Wei Y, Balcioglu A, Daneshmand A, et al. Selective ROCK2 inhibition in focal cerebral ischemia. Ann Clin Transl Neurol. 2014;1:2–14.CrossRefPubMed Lee JH, Zheng Y, von Bornstadt D, Wei Y, Balcioglu A, Daneshmand A, et al. Selective ROCK2 inhibition in focal cerebral ischemia. Ann Clin Transl Neurol. 2014;1:2–14.CrossRefPubMed
40.
go back to reference Gibson CL, Srivastava K, Sprigg N, Bath PMW, Bayraktutan U. Inhibition of Rho-kinase protects cerebral barrier from ischaemia-evoked injury through modulations of endothelial cell oxidative stress and tight junctions. J Neurochem. 2014;129:816–26.CrossRefPubMed Gibson CL, Srivastava K, Sprigg N, Bath PMW, Bayraktutan U. Inhibition of Rho-kinase protects cerebral barrier from ischaemia-evoked injury through modulations of endothelial cell oxidative stress and tight junctions. J Neurochem. 2014;129:816–26.CrossRefPubMed
41.
go back to reference Gokina N, Park KM, McElroy-Yaggy K, Osol G. Effects of Rho kinase inhibition on cerebral artery myogenic tone and reactivity. J Appl Physiol (1985). 2005;98:1940–8.CrossRef Gokina N, Park KM, McElroy-Yaggy K, Osol G. Effects of Rho kinase inhibition on cerebral artery myogenic tone and reactivity. J Appl Physiol (1985). 2005;98:1940–8.CrossRef
42.
go back to reference Ledoux J, Werner ME, Brayden JE, Nelson MT. Calcium-activated potassium channels and the regulation of vascular tone. Physiology. 2006;21:69–79. Ledoux J, Werner ME, Brayden JE, Nelson MT. Calcium-activated potassium channels and the regulation of vascular tone. Physiology. 2006;21:69–79.
43.
go back to reference Marrelli SP, Eckmann MS, Hunte MS. Role of endothelial intermediate conductance Kca channels in cerebral EDHF-mediated dilations. Am J Physiol. 2003;285:H1590–9. Marrelli SP, Eckmann MS, Hunte MS. Role of endothelial intermediate conductance Kca channels in cerebral EDHF-mediated dilations. Am J Physiol. 2003;285:H1590–9.
44.
go back to reference Cipolla MJ, Smith J, Kohlmeyer MM, Godfrey JA. SKCa and IKCa Channels, myogenic tone, and vasodilator responses in middle cerebral arteries and parenchymal arterioles: effect of ischemia and reperfusion. Stroke. 2009;40:1451–7.CrossRefPubMedPubMedCentral Cipolla MJ, Smith J, Kohlmeyer MM, Godfrey JA. SKCa and IKCa Channels, myogenic tone, and vasodilator responses in middle cerebral arteries and parenchymal arterioles: effect of ischemia and reperfusion. Stroke. 2009;40:1451–7.CrossRefPubMedPubMedCentral
45.
go back to reference Mishra RC, Belke D, Wulff H, Braun AP. SKA-31, a novel activator of SK(Ca) and IK(Ca) channels, increases coronary flow in male and female rat hearts. Cardiovasc Res. 2013;97:339–48.CrossRefPubMed Mishra RC, Belke D, Wulff H, Braun AP. SKA-31, a novel activator of SK(Ca) and IK(Ca) channels, increases coronary flow in male and female rat hearts. Cardiovasc Res. 2013;97:339–48.CrossRefPubMed
46.
go back to reference An H, Ford AL, Vo K, Eldeniz C, Ponisio R, Zhu H, et al. Early changes of tissue perfusion after tissue plasminogen activator in hyperacute ischemic stroke. Stroke. 2011;2:65–72.CrossRef An H, Ford AL, Vo K, Eldeniz C, Ponisio R, Zhu H, et al. Early changes of tissue perfusion after tissue plasminogen activator in hyperacute ischemic stroke. Stroke. 2011;2:65–72.CrossRef
47.
go back to reference 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:e34–40.CrossRefPubMed 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:e34–40.CrossRefPubMed
48.
go back to reference Busch E, Krüger K, Allegrini PR, Kerskens CM, Gyngell ML, Hoehn-Berlage M, et al. Reperfusion after thrombolytic therapy of embolic stroke in the rat: magnetic resonance and biochemical imaging. J Cereb Blood Flow Metab. 1998;18:407–18.CrossRefPubMed Busch E, Krüger K, Allegrini PR, Kerskens CM, Gyngell ML, Hoehn-Berlage M, et al. Reperfusion after thrombolytic therapy of embolic stroke in the rat: magnetic resonance and biochemical imaging. J Cereb Blood Flow Metab. 1998;18:407–18.CrossRefPubMed
49.
go back to reference 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.PubMedPubMedCentral 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.PubMedPubMedCentral
50.
go back to reference del Zoppo GJ, Mabuchi T. Cerebral microvessel responses to focal ischemia. J Cereb Blood Flow Metab. 2003;23:879–94.CrossRefPubMed del Zoppo GJ, Mabuchi T. Cerebral microvessel responses to focal ischemia. J Cereb Blood Flow Metab. 2003;23:879–94.CrossRefPubMed
51.
go back to reference del Zoppo GJ, Poeck K, Pessin MS, Wolpert SM, Furlan AJ, Ferbert A, et al. Recombinant tissue plasminogen activator in acute thrombotic and embolic stroke. Ann Neurol. 1992;32:78–86.CrossRefPubMed del Zoppo GJ, Poeck K, Pessin MS, Wolpert SM, Furlan AJ, Ferbert A, et al. Recombinant tissue plasminogen activator in acute thrombotic and embolic stroke. Ann Neurol. 1992;32:78–86.CrossRefPubMed
52.
go back to reference Alexandrov AV, Molina CA, Grotta JC, Garami Z, Ford SR, Alvarez-Sabin J, et al. Ultrasound-enhanced systemic thrombolysis for acute ischemic stroke. N Engl J Med. 2004;351:2170–8.CrossRefPubMed Alexandrov AV, Molina CA, Grotta JC, Garami Z, Ford SR, Alvarez-Sabin J, et al. Ultrasound-enhanced systemic thrombolysis for acute ischemic stroke. N Engl J Med. 2004;351:2170–8.CrossRefPubMed
53.
go back to reference Ribo M, Alvarez-Sabin J, Montaner J, Romero F, Delgado P, Rubiera M, et al. Temporal profile of recanalization after intravenous tissue plasminogen activator: selecting patients for rescue reperfusion techniques. Stroke. 2006;37:1000–4.CrossRefPubMed Ribo M, Alvarez-Sabin J, Montaner J, Romero F, Delgado P, Rubiera M, et al. Temporal profile of recanalization after intravenous tissue plasminogen activator: selecting patients for rescue reperfusion techniques. Stroke. 2006;37:1000–4.CrossRefPubMed
54.
go back to reference Lee KY, Han SW, Kim SH, Nam HS, Ahn SW, Kim DJ, et al. Early recanalization after intravenous administration of recombinant tissue plasminogen activator as assessed by pre- and post-thrombolytic angiography in acute ischemic stroke patients. Stroke. 2007;38:192–3.CrossRefPubMed Lee KY, Han SW, Kim SH, Nam HS, Ahn SW, Kim DJ, et al. Early recanalization after intravenous administration of recombinant tissue plasminogen activator as assessed by pre- and post-thrombolytic angiography in acute ischemic stroke patients. Stroke. 2007;38:192–3.CrossRefPubMed
55.
go back to reference Kimura K, Iguchi Y, Shibazaki K, Aoki J, Uemura J. Early recanalization rate of major occluded brain arteries after intravenous tissue plasminogen activator therapy using serial magnetic resonance angiography studies. Eur Neurol. 2009;62:287–92.CrossRefPubMed Kimura K, Iguchi Y, Shibazaki K, Aoki J, Uemura J. Early recanalization rate of major occluded brain arteries after intravenous tissue plasminogen activator therapy using serial magnetic resonance angiography studies. Eur Neurol. 2009;62:287–92.CrossRefPubMed
56.
go back to reference Vanacker P, Lambrou D, Eskandari A, Maeder P, Meuli R, Ntaios G, et al. Improving prediction of recanalization in acute large vessel occlusive Stroke. J Thromb Haemost. 2014;12:814–21.CrossRefPubMed Vanacker P, Lambrou D, Eskandari A, Maeder P, Meuli R, Ntaios G, et al. Improving prediction of recanalization in acute large vessel occlusive Stroke. J Thromb Haemost. 2014;12:814–21.CrossRefPubMed
57.
go back to reference Alexandrov AV, Hall CE, Labiche LA, Wojner AW, Grotta JC. Ischemic stunning of the brain: early recanalization without immediate clinical improvement in acute ischemic stroke. Stroke. 2004;35:449–52.CrossRefPubMed Alexandrov AV, Hall CE, Labiche LA, Wojner AW, Grotta JC. Ischemic stunning of the brain: early recanalization without immediate clinical improvement in acute ischemic stroke. Stroke. 2004;35:449–52.CrossRefPubMed
58.
go back to reference del Zoppo GJ, Schmid-Schönbein 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.CrossRefPubMed del Zoppo GJ, Schmid-Schönbein 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.CrossRefPubMed
59.
go back to reference Hallenbeck JM, Dutka AJ, Tanishima T, Kochanek PM, Kumaroo KK, Thompson CB, et al. Polymorphonuclear leukocyte accumulation in brain regions with low blood flow during the early postischemic period. Stroke. 1986;17:246–53.CrossRefPubMed Hallenbeck JM, Dutka AJ, Tanishima T, Kochanek PM, Kumaroo KK, Thompson CB, et al. Polymorphonuclear leukocyte accumulation in brain regions with low blood flow during the early postischemic period. Stroke. 1986;17:246–53.CrossRefPubMed
60.
go back to reference Faraci FM, Mayhan WG, Heistad DD. Segmental vascular responses to acute hypertension in cerebrum and brain stem. Am J Physiol. 1987;252:H738–42.PubMed Faraci FM, Mayhan WG, Heistad DD. Segmental vascular responses to acute hypertension in cerebrum and brain stem. Am J Physiol. 1987;252:H738–42.PubMed
61.
go back to reference Faraci FM, Heistad DD. Regulation of large cerebral arteries and cerebral microvascular pressure. Circ Res. 1990;66:8–17.CrossRefPubMed Faraci FM, Heistad DD. Regulation of large cerebral arteries and cerebral microvascular pressure. Circ Res. 1990;66:8–17.CrossRefPubMed
62.
go back to reference Faraci FM, Mayhan WG, Schmid PG, Heistad DD. Effects of arginine vasopressin on cerebral microvascular pressure. Am J Physiol. 1988;255:H70–6.PubMed Faraci FM, Mayhan WG, Schmid PG, Heistad DD. Effects of arginine vasopressin on cerebral microvascular pressure. Am J Physiol. 1988;255:H70–6.PubMed
63.
go back to reference Cipolla MJ, Chan SL, Sweet J, Tavares MJ, Gokina N, Brayden JE. Postischemic reperfusion causes smooth muscle calcium sensitization and vasoconstriction of parenchymal arterioles. Stroke. 2014;45:2425–30.CrossRefPubMedPubMedCentral Cipolla MJ, Chan SL, Sweet J, Tavares MJ, Gokina N, Brayden JE. Postischemic reperfusion causes smooth muscle calcium sensitization and vasoconstriction of parenchymal arterioles. Stroke. 2014;45:2425–30.CrossRefPubMedPubMedCentral
64.
go back to reference Cipolla MJ, Sweet J, Chan SL, Tavares MJ, Gokina N, Brayden JE. Increased pressure-induced tone in rat parenchymal arterioles vs. middle cerebral arteries: role of ion channels and calcium sensitivity. J Appl Physiol (1985). 2014;117:53–9.CrossRef Cipolla MJ, Sweet J, Chan SL, Tavares MJ, Gokina N, Brayden JE. Increased pressure-induced tone in rat parenchymal arterioles vs. middle cerebral arteries: role of ion channels and calcium sensitivity. J Appl Physiol (1985). 2014;117:53–9.CrossRef
65.
go back to reference Baumbach GL, Heistad DD. Regional, segmental, and temporal heterogeneity of cerebral vascular autoregulation. Ann Biomed Eng. 1985;13:303–10.CrossRefPubMed Baumbach GL, Heistad DD. Regional, segmental, and temporal heterogeneity of cerebral vascular autoregulation. Ann Biomed Eng. 1985;13:303–10.CrossRefPubMed
66.
go back to reference Baumbach GL, Mayhan WG, Heistad DD. Protection of the blood–brain barrier by hypercapnia during acute hypertension. Am J Physiol. 1986;251:H282–7.PubMed Baumbach GL, Mayhan WG, Heistad DD. Protection of the blood–brain barrier by hypercapnia during acute hypertension. Am J Physiol. 1986;251:H282–7.PubMed
67.
go back to reference Ronaldson PT, Davis TP. Blood–brain barrier integrity and glial support: mechanisms that can be targeted for novel therapeutic approaches in stroke. Curr Pharm Des. 2012;18:3624–44.CrossRefPubMedPubMedCentral Ronaldson PT, Davis TP. Blood–brain barrier integrity and glial support: mechanisms that can be targeted for novel therapeutic approaches in stroke. Curr Pharm Des. 2012;18:3624–44.CrossRefPubMedPubMedCentral
68.
go back to reference Ergul A, Kelly-Cobbs A, Abdalla M, Fagan SC. Cerebrovascular complications of diabetes: focus on stroke. Endocr Metab Immune Disord Drug Targets. 2012;12(2):148–58.CrossRefPubMedPubMedCentral Ergul A, Kelly-Cobbs A, Abdalla M, Fagan SC. Cerebrovascular complications of diabetes: focus on stroke. Endocr Metab Immune Disord Drug Targets. 2012;12(2):148–58.CrossRefPubMedPubMedCentral
69.
go back to reference Cipolla MJ, Huang Q, Sweet JG. Inhibition of protein kinase Cβ reverses increased blood–brain barrier permeability during hyperglycemic stroke and prevents edema formation in vivo. Stroke. 2011;42:3252–7.CrossRefPubMedPubMedCentral Cipolla MJ, Huang Q, Sweet JG. Inhibition of protein kinase Cβ reverses increased blood–brain barrier permeability during hyperglycemic stroke and prevents edema formation in vivo. Stroke. 2011;42:3252–7.CrossRefPubMedPubMedCentral
70.
go back to reference Kumai Y, Ooboshi H, Ibayashi S, Ishikawa E, Sugimori H, Kamouchi M, et al. Postischemic gene transfer of soluble Flt-1 protects against brain ischemia with marked attenuation of blood–brain barrier permeability. J Cereb Blood Flow Metab. 2007;27(6):1152–60.CrossRefPubMed Kumai Y, Ooboshi H, Ibayashi S, Ishikawa E, Sugimori H, Kamouchi M, et al. Postischemic gene transfer of soluble Flt-1 protects against brain ischemia with marked attenuation of blood–brain barrier permeability. J Cereb Blood Flow Metab. 2007;27(6):1152–60.CrossRefPubMed
71.
go back to reference Lyden PD. Hemorrhagic transformation during thrombolytic therapy and reperfusion: effects of age, blood pressure, and matrix metalloproteinases. J Stroke Cerebrovasc Dis. 2013;22(4):532–8.CrossRefPubMed Lyden PD. Hemorrhagic transformation during thrombolytic therapy and reperfusion: effects of age, blood pressure, and matrix metalloproteinases. J Stroke Cerebrovasc Dis. 2013;22(4):532–8.CrossRefPubMed
72.
go back to reference Wang M, Joshi S, Emerson RG. Comparison of intracarotid and intravenous propofol for electrocerebral silence in rabbits. Anesthesiology. 2003;99:904–10.CrossRefPubMed Wang M, Joshi S, Emerson RG. Comparison of intracarotid and intravenous propofol for electrocerebral silence in rabbits. Anesthesiology. 2003;99:904–10.CrossRefPubMed
73.
go back to reference Yamashita J, Handa H, Tokuriki Y, Ha YS, Otsuka SI, Suda K, et al. Intra-arterial ACNU therapy for malignant brain tumors. Experimental studies and preliminary clinical results. J Neurosurg. 1983;59:424–30.CrossRefPubMed Yamashita J, Handa H, Tokuriki Y, Ha YS, Otsuka SI, Suda K, et al. Intra-arterial ACNU therapy for malignant brain tumors. Experimental studies and preliminary clinical results. J Neurosurg. 1983;59:424–30.CrossRefPubMed
74.
go back to reference Joshi S, Young WL, Pile-Spellman J, Duong DH, Vang MC, Hacein-Bey L, et al. The feasibility of intracarotid adenosine for the manipulation of human cerebrovascular resistance. Anesth Analg. 1998;87:1291–8.PubMed Joshi S, Young WL, Pile-Spellman J, Duong DH, Vang MC, Hacein-Bey L, et al. The feasibility of intracarotid adenosine for the manipulation of human cerebrovascular resistance. Anesth Analg. 1998;87:1291–8.PubMed
76.
go back to reference Chen H, Yoshioka H, Kim GS, Jung JE, Okami N, Sakata H, et al. Oxidative stress in ischemic brain damage: mechanisms of cell death and potential molecular targets for neuroprotection. Antioxid Redox Signal. 2011;14:1505–17.CrossRefPubMedPubMedCentral Chen H, Yoshioka H, Kim GS, Jung JE, Okami N, Sakata H, et al. Oxidative stress in ischemic brain damage: mechanisms of cell death and potential molecular targets for neuroprotection. Antioxid Redox Signal. 2011;14:1505–17.CrossRefPubMedPubMedCentral
77.
go back to reference Duong H, Hacein-Bey L, Vang MC, Pile-Spellman J, Joshi S, Young WL. Management of cerebral arterial occlusion during endovascular treatment of cerebrovascular disease. Problems in Anesthesia. 1997;9:99–111. Duong H, Hacein-Bey L, Vang MC, Pile-Spellman J, Joshi S, Young WL. Management of cerebral arterial occlusion during endovascular treatment of cerebrovascular disease. Problems in Anesthesia. 1997;9:99–111.
78.
go back to reference Hillen B. The variability of the circle of Willis: univariate and bivariate analysis. Acta Morphol Neerl Scand. 1986;24:87–101.PubMed Hillen B. The variability of the circle of Willis: univariate and bivariate analysis. Acta Morphol Neerl Scand. 1986;24:87–101.PubMed
79.
go back to reference Hillen B, Hoogstraten HW, Van Overbeeke JJ, Van der Zwan A. Functional anatomy of the circulus arteriosus cerebri (WillisII). Bull Assoc Anat. 1991;75:123–6. Hillen B, Hoogstraten HW, Van Overbeeke JJ, Van der Zwan A. Functional anatomy of the circulus arteriosus cerebri (WillisII). Bull Assoc Anat. 1991;75:123–6.
80.
go back to reference Hillen B, Drinkenburg BA, Hoogstraten HW, Post L. Analysis of flow and vascular resistance in a model of the circle of Willis. J Biomechan. 1988;21:807–14.CrossRef Hillen B, Drinkenburg BA, Hoogstraten HW, Post L. Analysis of flow and vascular resistance in a model of the circle of Willis. J Biomechan. 1988;21:807–14.CrossRef
81.
go back to reference Dedrick RL. Arterial drug infusion: pharmacokinetic problems and pitfalls. J Natl Cancer Inst. 1988;80:84–9.CrossRefPubMed Dedrick RL. Arterial drug infusion: pharmacokinetic problems and pitfalls. J Natl Cancer Inst. 1988;80:84–9.CrossRefPubMed
82.
go back to reference Cipolla MJ. The cerebral circulation. In: Integrated systems physiology—from molecule to function. Morgan & Claypool Life Sciences Publishers:San Rafael, 2009 Cipolla MJ. The cerebral circulation. In: Integrated systems physiology—from molecule to function. Morgan & Claypool Life Sciences Publishers:San Rafael, 2009
83.
go back to reference Butt AM. Effect of inflammatory agents on electrical resistance across the blood–brain barrier in pial microvessels of anaesthetized rats. Brain Res. 1995;696:145–50.CrossRefPubMed Butt AM. Effect of inflammatory agents on electrical resistance across the blood–brain barrier in pial microvessels of anaesthetized rats. Brain Res. 1995;696:145–50.CrossRefPubMed
84.
go back to reference Giraud M, Cho TH, Nighoghossian N, Maucort-Boulch D, Deiana G, Østergaard L, et al. Early blood brain barrier changes in acute ischemic stroke: a sequential MRI study. J Neuroimaging. 2015;25:959–63.CrossRefPubMed Giraud M, Cho TH, Nighoghossian N, Maucort-Boulch D, Deiana G, Østergaard L, et al. Early blood brain barrier changes in acute ischemic stroke: a sequential MRI study. J Neuroimaging. 2015;25:959–63.CrossRefPubMed
85.
go back to reference Prasad S, Sajja RK, Naik P, Cucullo L. Diabetes mellitus and blood–brain barrier dysfunction: an overview. J Pharmacovigil. 2014;2:125.PubMedPubMedCentral Prasad S, Sajja RK, Naik P, Cucullo L. Diabetes mellitus and blood–brain barrier dysfunction: an overview. J Pharmacovigil. 2014;2:125.PubMedPubMedCentral
86.
go back to reference Won SJ, Tang XN, Suh SW, Yenari MA, Swanson RA. Hyperglycemia promotes tissue plasminogen activator-induced hemorrhage by increasing superoxide production. Ann Neurol. 2011;70:583–90.CrossRefPubMedPubMedCentral Won SJ, Tang XN, Suh SW, Yenari MA, Swanson RA. Hyperglycemia promotes tissue plasminogen activator-induced hemorrhage by increasing superoxide production. Ann Neurol. 2011;70:583–90.CrossRefPubMedPubMedCentral
88.
go back to reference Obrist WD, Thompson Jr HK, Wang HS, Wilkinson WE. Regional cerebral blood flow estimated by 133xenon inhalation. Stroke. 1975;6:245–56.CrossRefPubMed Obrist WD, Thompson Jr HK, Wang HS, Wilkinson WE. Regional cerebral blood flow estimated by 133xenon inhalation. Stroke. 1975;6:245–56.CrossRefPubMed
89.
go back to reference Obrist WD, Dolinskas CA, Jaggi JL, Cruz J, Steiman DL. Serial cerebral blood flow studies in acute head injury: application of the intravenous 133 Xe method. 1983. p. 145–50. Obrist WD, Dolinskas CA, Jaggi JL, Cruz J, Steiman DL. Serial cerebral blood flow studies in acute head injury: application of the intravenous 133 Xe method. 1983. p. 145–50.
90.
go back to reference Sanelli PC, Nicola G, Tsiouris AJ, Ougorets I, Knight C, Frommer B, et al. Reproducibility of post processing of quantitative CT perfusion maps. AJR Am J Roentgenol. 2007;188:213–8.CrossRefPubMed Sanelli PC, Nicola G, Tsiouris AJ, Ougorets I, Knight C, Frommer B, et al. Reproducibility of post processing of quantitative CT perfusion maps. AJR Am J Roentgenol. 2007;188:213–8.CrossRefPubMed
91.
go back to reference Morales Palomares S, Cipolla MJ. Vascular protection following ischemia and reperfusion. J Neurol Neurophysiol. 2011;20:S1–4. Morales Palomares S, Cipolla MJ. Vascular protection following ischemia and reperfusion. J Neurol Neurophysiol. 2011;20:S1–4.
92.
go back to reference Cipolla MJ, McCall A, Lessov N, Porter J. Reperfusion decreases myogenic reactivity and alters middle cerebral artery function after focal cerebral ischemia in rats. Stroke. 1997;28:176–80.CrossRefPubMed Cipolla MJ, McCall A, Lessov N, Porter J. Reperfusion decreases myogenic reactivity and alters middle cerebral artery function after focal cerebral ischemia in rats. Stroke. 1997;28:176–80.CrossRefPubMed
93.
go back to reference Linfante I, Walker GR, Castonguay AC, Dabus G, Starosciak AK, Yoo AJ, et al. Predictors of mortality in acute ischemic stroke intervention: analysis of the north American solitaire acute stroke registry. Stroke. 2015;46:2305–8.CrossRefPubMed Linfante I, Walker GR, Castonguay AC, Dabus G, Starosciak AK, Yoo AJ, et al. Predictors of mortality in acute ischemic stroke intervention: analysis of the north American solitaire acute stroke registry. Stroke. 2015;46:2305–8.CrossRefPubMed
94.
go back to reference Linfante I, Starosciak AK, Walker GR, Dabus G, Castonguay AC, Gupta R, et al. Predictors of poor outcome despite recanalization: a multiple regression analysis of the NASA registry. J NeuroIntervent Surg. 2015;8(3):1–6. doi:10.1136/neurintsurg-2014-011525. Linfante I, Starosciak AK, Walker GR, Dabus G, Castonguay AC, Gupta R, et al. Predictors of poor outcome despite recanalization: a multiple regression analysis of the NASA registry. J NeuroIntervent Surg. 2015;8(3):1–6. doi:10.​1136/​neurintsurg-2014-011525.
95.
go back to reference Wardlaw JM, Murray V, Berge E, del Zoppo G, Sandercock P, Lindley RL, et al. Recombinant tissue plasminogen activator for acute ischaemic stroke:an updated systematic review and meta-analysis. Lancet. 2012;379:2364–72. Wardlaw JM, Murray V, Berge E, del Zoppo G, Sandercock P, Lindley RL, et al. Recombinant tissue plasminogen activator for acute ischaemic stroke:an updated systematic review and meta-analysis. Lancet. 2012;379:2364–72.
96.
go back to reference Saver JL, Fonarow GC, Smith EE, Reeves MJ, Grau-Sepulveda MV, Pan W, et al. Time to treatment with intravenous plasminogen activator and outcome from acute ischemic stroke. JAMA. 2013;309:2480–8. Saver JL, Fonarow GC, Smith EE, Reeves MJ, Grau-Sepulveda MV, Pan W, et al. Time to treatment with intravenous plasminogen activator and outcome from acute ischemic stroke. JAMA. 2013;309:2480–8.
97.
go back to reference Broderick JP, Palesch YY, Demchuk AM, Yeatts SD, Khatri P, Hill MD, et al. Endovascular therapy after intravenous t-PA versus t-PA alone for stroke. N Engl J Med. 2013;368:893–903. Broderick JP, Palesch YY, Demchuk AM, Yeatts SD, Khatri P, Hill MD, et al. Endovascular therapy after intravenous t-PA versus t-PA alone for stroke. N Engl J Med. 2013;368:893–903.
98.
go back to reference Hussein HM, Georgiadis AL, Vazquez G, Miley JT, Memon MZ, Mohammad YM, et al. Occurrence and predictorsof futile recanalization following endovascular treatment among patients with acute ischemic stroke. AJNR Am J Neuroradiol. 2010;31:454–458. Hussein HM, Georgiadis AL, Vazquez G, Miley JT, Memon MZ, Mohammad YM, et al. Occurrence and predictorsof futile recanalization following endovascular treatment among patients with acute ischemic stroke. AJNR Am J Neuroradiol. 2010;31:454–458.
Metadata
Title
Improving Reperfusion Therapies in the Era of Mechanical Thrombectomy
Authors
Italo Linfante
Marilyn J. Cipolla
Publication date
01-08-2016
Publisher
Springer US
Published in
Translational Stroke Research / Issue 4/2016
Print ISSN: 1868-4483
Electronic ISSN: 1868-601X
DOI
https://doi.org/10.1007/s12975-016-0469-3

Other articles of this Issue 4/2016

Translational Stroke Research 4/2016 Go to the issue

SI: Challenges and Controversies in Translational Stroke Research

Extending the Time Window for Endovascular and Pharmacological Reperfusion

SI: Challenges and Controversies in Translational Stroke Research

Translational Hurdles in Stroke Recovery Studies

SI: Challenges and Controversies in Translational Stroke Research

Embracing Biological and Methodological Variance in a New Approach to Pre-Clinical Stroke Testing

SI: Challenges and Controversies in Translational Stroke Research

Regulatory T Cells in Post-stroke Immune Homeostasis