Applications and development of permeability imaging in ischemic stroke (Review)
- Authors:
- Hui Chen
- Guangming Zhu
- Nan Liu
- Ying Li
- Yonghong Xia
-
Affiliations: Department of Neurology, Military General Hospital of Beijing PLA, Beijing 100700, P.R. China, Department of Critical Care Medicine, Yantai Yuhuangding Hospital, Yantai, Shandong 264000, P.R. China - Published online on: July 17, 2018 https://doi.org/10.3892/etm.2018.6454
- Pages: 2203-2207
This article is mentioned in:
Abstract
Milej D, Abdalmalak A, Desjardins L, Ahmed H, Lee TY, Diop M and Lawrence KS: Quantification of blood-brain barrier permeability by dynamic contrast-enhanced NIRS. Sci Rep. 7:17022017. View Article : Google Scholar : PubMed/NCBI | |
Villringer K, Sanz Cuesta BE, Ostwaldt AC, Grittner U, Brunecker P, Khalil AA, Schindler K, Eisenblätter O, Audebert H and Fiebach JB: DCE-MRI blood-brain barrier assessment in acute ischemic stroke. Neurology. 88:433–440. 2017. View Article : Google Scholar : PubMed/NCBI | |
Yang GY and Betz AL: Reperfusion-induced injury to the blood-brain barrier after middle cerebral artery occlusion in rats. Stroke. 25:1658–1665. 1994. View Article : Google Scholar : PubMed/NCBI | |
Hoffmann A, Zhu G and Wintermark M: Advanced neuroimaging in stroke patients: Prediction of tissue fate and hemorrhagic transformation. Expert Rev Cardiovasc Ther. 10:515–524. 2012. View Article : Google Scholar : PubMed/NCBI | |
Hatashita S and Hoff JT: Brain edema and cerebrovascular permeability during cerebral ischemia in rats. Stroke. 21:582–588. 1990. View Article : Google Scholar : PubMed/NCBI | |
Sun FL, Wang W, Cheng H, Wang Y, Li L, Xue JL, Wang XF, Ai HX, Zhang L, Xu JD, et al: Morroniside improves microvascular functional integrity of the neurovascular unit after cerebral ischemia. PLoS One. 9:e1011942014. View Article : Google Scholar : PubMed/NCBI | |
Liebeskind DS, Kim D, Starkman S, Changizi K, Ohanian AG, Jahan R and Viñuela F: Collateral failure? Late mechanical thrombectomy after failed intravenous thrombolysis. J Neuroimaging. 20:78–82. 2010. View Article : Google Scholar : PubMed/NCBI | |
Hacke W, Furlan AJ, Al-Rawi Y, Davalos A, Fiebach JB, Gruber F, Kaste M, Lipka LJ, Pedraza S, Ringleb PA, et al: Intravenous desmoteplase in patients with acute ischaemic stroke selected by MRI perfusion-diffusion weighted imaging or perfusion CT (DIAS-2): A prospective, randomised, double-blind, placebo-controlled study. Lancet Neurol. 8:141–150. 2009. View Article : Google Scholar : PubMed/NCBI | |
Shobha N, Buchan AM and Hill MD; Canadian Alteplase for Stroke Effectiveness Study (CASES), : Thrombolysis at 3-4.5 hours after acute ischemic stroke onset-evidence from the Canadian Alteplase for Stroke Effectiveness Study (CASES) registry. Cerebrovasc Dis. 31:223–228. 2011. View Article : Google Scholar : PubMed/NCBI | |
Smith WS, Sung G, Starkman S, Saver JL, Kidwell CS, Gobin YP, Lutsep HL, Nesbit GM, Grobelny T, Rymer MM, et al: Safety and efficacy of mechanical embolectomy in acute ischemic stroke: Results of the MERCI trial. Stroke. 36:1432–1438. 2005. View Article : Google Scholar : PubMed/NCBI | |
Smith WS, Sung G, Saver J, Budzik R, Duckwiler G, Liebeskind DS, Lutsep HL, Rymer MM, Higashida RT, Starkman S, et al: Mechanical thrombectomy for acute ischemic stroke: Final results of the Multi MERCI trial. Stroke. 39:1205–1212. 2008. View Article : Google Scholar : PubMed/NCBI | |
Zhang J, Yang Y, Sun H and Xing Y: Hemorrhagic transformation after cerebral infarction: Current concepts and challenges. Ann Transl Med. 2:812014.PubMed/NCBI | |
Hafez S, Hoda MN, Guo X, Johnson MH, Fagan SC and Ergul A: Comparative analysis of different methods of Ischemia/Reperfusion in hyperglycemic stroke outcomes: Interaction with tPA. Transl Stroke Res. 6:171–180. 2015. View Article : Google Scholar : PubMed/NCBI | |
Souza LC, Payabvash S, Wang Y, Kamalian S, Schaefer P, Gonzalez RG, Furie KL and Lev MH: Admission CT perfusion is an independent predictor of hemorrhagic transformation in acute stroke with similar accuracy to DWI. Cerebrovasc Dis. 33:8–15. 2012. View Article : Google Scholar : PubMed/NCBI | |
Furtado AD, Adraktas DD, Brasic N, Cheng SC, Ordovas K, Smith WS, Lewin MR, Chun K, Chien JD, Schaeffer S and Wintermark M: The triple rule-out for acute ischemic stroke: Imaging the brain, carotid arteries, aorta, and heart. AJNR Am J Neuroradiol. 31:1290–1296. 2010. View Article : Google Scholar : PubMed/NCBI | |
Kaesmacher J, Kaesmacher M, Maegerlein C, Zimmer C, Gersing AS, Wunderlich S, Friedrich B, Boeckh-Behrens T and Kleine JF: Hemorrhagic transformations after thrombectomy: Risk factors and clinical relevance. Cerebrovasc Dis. 43:294–304. 2017. View Article : Google Scholar : PubMed/NCBI | |
Kim JM, Park KY, Lee WJ, Byun JS, Kim JK, Park MS, Ahn SW and Shin HW: The cortical contrast accumulation from brain computed tomography after endovascular treatment predicts symptomatic hemorrhage. Eur J Neurol. 22:1453–1458. 2015. View Article : Google Scholar : PubMed/NCBI | |
Zhu G, Michel P, Zhang W and Wintermark M: Standardization of stroke perfusion CT for reperfusion therapy. Transl Stroke Res. 3:221–227. 2012. View Article : Google Scholar : PubMed/NCBI | |
Durst C, Monteith S, Sheehan J, Moldovan K, Snell J, Eames M, Huerta T, Walker W, Viola F, Kassell N and Wintermark M: Optimal imaging of in vitro clot sonothrombolysis by MR-guided focused ultrasound. J Neuroimaging. 23:187–191. 2013. View Article : Google Scholar : PubMed/NCBI | |
Hamann GF, Okada Y and del Zoppo GJ: Hemorrhagic transformation and microvascular integrity during focal cerebral ischemia/reperfusion. J Cereb Blood Flow Metab. 16:1373–1378. 1996. View Article : Google Scholar : PubMed/NCBI | |
Dijkhuizen RM, Asahi M, Wu O, Rosen BR and 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. 33:2100–2104. 2002. View Article : Google Scholar : PubMed/NCBI | |
Kelly MA, Shuaib A and Todd KG: Matrix metalloproteinase activation and blood-brain barrier breakdown following thrombolysis. Exp Neurol. 200:38–49. 2006. View Article : Google Scholar : PubMed/NCBI | |
Jiang Q, Zhang RL, Zhang ZG, Knight RA, Ewing JR, Ding G, Lu M, Arniego P, Zhang L, Hu J, et al: Magnetic resonance imaging characterization of hemorrhagic transformation of embolic stroke in the rat. J Cereb Blood Flow Metab. 22:559–568. 2002. View Article : Google Scholar : PubMed/NCBI | |
Jiang Q, Ewing JR, Ding GL, Zhang L, Zhang ZG, Li L, Whitton P, Lu M, Hu J, Li QJ, et al: Quantitative evaluation of BBB permeability after embolic stroke in rat using MRI. J Cereb Blood Flow Metab. 25:583–592. 2005. View Article : Google Scholar : PubMed/NCBI | |
Amtul Z and Hepburn JD: Protein markers of cerebrovascular disruption of neurovascular unit: Immunohistochemical and imaging approaches. Rev Neurosci. 25:481–507. 2014. View Article : Google Scholar : PubMed/NCBI | |
Hacke W, Kaste M, Bluhmki E, Brozman M, Dávalos A, Guidetti D, Larrue V, Lees KR, Medeghri Z, Machnig T, et al: Thrombolysis with Alteplase 3 to 4.5 hours after acute ischemic stroke. N Engl J Med. 359:1317–1329. 2008. View Article : Google Scholar : PubMed/NCBI | |
Chen H, Wu B, Liu N, Wintermark M, Su Z, Li Y, Hu J, Zhang Y, Zhang W and Zhu G: Using standard first-pass perfusion computed tomographic data to evaluate collateral flow in acute ischemic stroke. Stroke. 46:961–967. 2015. View Article : Google Scholar : PubMed/NCBI | |
Zaidat OO, Lazzaro MA, Liebeskind DS, Janjua N, Wechsler L, Nogueira RG, Edgell RC, Kalia JS, Badruddin A, English J, et al: Revascularization grading in endovascular acute ischemic stroke therapy. Neurology. 79 Suppl 1:S110–S116. 2012. View Article : Google Scholar : PubMed/NCBI | |
Marks MP, Lansberg MG, Mlynash M, Olivot JM, Straka M, Kemp S, McTaggart R, Inoue M, Zaharchuk G, Bammer R, et al: Effect of collateral blood flow on patients undergoing endovascular therapy for acute ischemic stroke. Stroke. 45:1035–1039. 2014. View Article : Google Scholar : PubMed/NCBI | |
Guan J, Zhang S, Zhou Q, Li C and Lu Z: Usefulness of transcranial Doppler ultrasound in evaluating cervical-cranial collateral circulations. Interv Neurol. 2:8–18. 2013. View Article : Google Scholar : PubMed/NCBI | |
Kortman HG, Smit EJ, Oei MT, Manniesing R, Prokop M and Meijer FJ: 4D-CTA in neurovascular disease: A review. AJNR Am J Neuroradiol. 36:1026–1033. 2015. View Article : Google Scholar : PubMed/NCBI | |
Stolz E, Mendes I, Gerriets T and Kaps M: Assessment of intracranial collateral flow by transcranial color-coded duplex sonography using a temporal and frontal axial insonation plane. J Neuroimaging. 12:136–143. 2002. View Article : Google Scholar : PubMed/NCBI | |
Roach BA, Donahue MJ, Davis LT, Faraco CC, Arteaga D, Chen SC, Ladner TR, Scott AO and Strother MK: Interrogating the functional correlates of collateralization in patients with intracranial stenosis using multimodal hemodynamic imaging. AJNR Am J Neuroradiol. 37:1132–1138. 2016. View Article : Google Scholar : PubMed/NCBI | |
Seidel G, Kaps M and Gerriets T: Potential and limitations of transcranial color-coded sonography in stroke patients. Stroke. 26:2061–2066. 1995. View Article : Google Scholar : PubMed/NCBI | |
Hernández-Pérez M, Puig J, Blasco G, Pérez de la Ossa N, Dorado L, Dávalos A and Munuera J: Dynamic magnetic resonance angiography provides collateral circulation and hemodynamic information in acute ischemic stroke. Stroke. 47:531–534. 2016. View Article : Google Scholar : PubMed/NCBI | |
Kaku Y, Iihara K, Nakajima N, Kataoka H, Fukushima K, Iida H and Hashimoto N: The leptomeningeal ivy sign on fluid-attenuated inversion recovery images in moyamoya disease: Positron emission tomography study. Cerebrovasc Dis. 36:19–25. 2013. View Article : Google Scholar : PubMed/NCBI | |
Wu B, Wang X, Guo J, Xie S, Wong EC, Zhang J, Jiang X and Fang J: Collateral circulation imaging: MR perfusion territory arterial spin-labeling at 3T. AJNR Am J Neuroradiol. 29:1855–1860. 2008. View Article : Google Scholar : PubMed/NCBI | |
Chang SM, Petersen ET, Zimine I, Sitoh YY, Lim CC and Golay X: Territorial arterial spin labeling in the assessment of collateral circulation: Comparison with digital subtraction angiography. Stroke. 39:3248–3254. 2008. View Article : Google Scholar : PubMed/NCBI | |
McVerry F, Liebeskind DS and Muir KW: Systematic review of methods for assessing leptomeningeal collateral flow. AJNR Am J Neuroradiol. 33:576–582. 2012. View Article : Google Scholar : PubMed/NCBI | |
Chen H, Wu B, Zhu G, Wintermark M, Wu X, Su Z, Xu X, Tian C, Ma L, Zhang W and Lou X: Permeability imaging as a biomarker of leptomeningeal collateral flow in patients with intracranial arterial stenosis. Cell Biochem Biophys. 71:1273–1279. 2015. View Article : Google Scholar : PubMed/NCBI | |
Ono Y, Abe K, Suzuki K, Iimura H, Sakai S, Uchiyama S and Okada Y: Usefulness of 4D-CTA in the detection of cerebral dural sinus occlusion or stenosis with collateral pathways. Neuroradiol J. 26:428–438. 2013. View Article : Google Scholar : PubMed/NCBI | |
Sheth SA and Liebeskind DS: ‘Imaging evaluation of collaterals in the brain: Physiology and clinical translation’. Curr Radiol Rep. 2:292014. View Article : Google Scholar : PubMed/NCBI | |
Lim M, Cheshier S and Steinberg GK: New vessel formation in the central nervous system during tumor growth, vascular malformations, and Moyamoya. Curr Neurovasc Res. 3:237–245. 2006. View Article : Google Scholar : PubMed/NCBI | |
Ding G, Jiang Q, Li L, Zhang L, Gang Zhang Z, Ledbetter KA, Ewing JR, Li Q and Chopp M: Detection of BBB disruption and hemorrhage by Gd-DTPA enhanced MR after embolic stroke in rat. Brain Res. 1114:195–203. 2006. View Article : Google Scholar : PubMed/NCBI | |
Vallon M, Chang J, Zhang H and Kuo CJ: Developmental and pathological angiogenesis in the central nervous system. Cell Mol Life Sci. 71:3489–3506. 2014. View Article : Google Scholar : PubMed/NCBI | |
Moisan A, Favre IM, Rome C, Grillon E, Naegele B, Barbieux M, De Fraipont F, Richard MJ, Barbier EL, Remy C and Detante O: Microvascular plasticity after experimental stroke: A molecular and MRI study. Cerebrovasc Dis. 38:344–353. 2014. View Article : Google Scholar : PubMed/NCBI | |
Darpolor MM, Molthen RC and Schmainda KM: Multimodality imaging of abnormal vascular perfusion and morphology in preclinical 9L gliosarcoma model. PLoS One. 6:e166212011. View Article : Google Scholar : PubMed/NCBI | |
Dvorak HF, Nagy JA, Feng D, Brown LF and Dvorak AM: Vascular permeability factor/vascular endothelial growth factor and the significance of microvascular hyperpermeability in angiogenesis. Curr Top Microbiol Immunol. 237:97–132. 1999.PubMed/NCBI | |
Neeman M: Functional and molecular MR imaging of angiogenesis: Seeing the target, seeing it work. J Cell Biochem Suppl. 39:11–17. 2002. View Article : Google Scholar : PubMed/NCBI | |
Dickie BR, Rose CJ, Kershaw LE, Withey SB, Carrington BM, Davidson SE, Hutchison G and West CML: The prognostic value of dynamic contrast-enhanced MRI contrast agent transfer constant Ktrans in cervical cancer is explained by plasma flow rather than vessel permeability. Br J Cancer. 116:1436–1443. 2017. View Article : Google Scholar : PubMed/NCBI | |
Jain R: Measurements of tumor vascular leakiness using DCE in brain tumors: Clinical applications. NMR Biomed. 26:1042–1049. 2013. View Article : Google Scholar : PubMed/NCBI | |
Seevinck PR, Deddens LH and Dijkhuizen RM: Magnetic resonance imaging of brain angiogenesis after stroke. Angiogenesis. 13:101–111. 2010. View Article : Google Scholar : PubMed/NCBI | |
Jiang Q, Zhang ZG, Ding GL, Zhang L, Ewing JR, Wang L, Zhang R, Li L, Lu M, Meng H, et al: Investigation of neural progenitor cell induced angiogenesis after embolic stroke in rat using MRI. Neuroimage. 28:698–707. 2005. View Article : Google Scholar : PubMed/NCBI | |
Zhang ZG, Zhang L, Jiang Q and Chopp M: Bone marrow-derived endothelial progenitor cells participate in cerebral neovascularization after focal cerebral ischemia in the adult mouse. Circ Res. 90:284–288. 2002. View Article : Google Scholar : PubMed/NCBI | |
Ding G, Jiang Q, Li L, Zhang L, Zhang ZG, Ledbetter KA, Gollapalli L, Panda S, Li Q, Ewing JR and Chopp M: Angiogenesis detected after embolic stroke in rat brain using magnetic resonance T2*WI. Stroke. 39:1563–1568. 2008. View Article : Google Scholar : PubMed/NCBI | |
Yano A, Shingo T, Takeuchi A, Yasuhara T, Kobayashi K, Takahashi K, Muraoka K, Matsui T, Miyoshi Y, Hamada H and Date I: Encapsulated vascular endothelial growth factor-secreting cell grafts have neuroprotective and angiogenic effects on focal cerebral ischemia. J Neurosurg. 103:104–114. 2005. View Article : Google Scholar : PubMed/NCBI | |
Slevin M, Kumar P, Gaffney J, Kumar S and Krupinski J: Can angiogenesis be exploited to improve stroke outcome? Mechanisms and therapeutic potential. Clin Sci (Lond). 111:171–183. 2006. View Article : Google Scholar : PubMed/NCBI |