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Permeability Parameters Measured with Dynamic Contrast-Enhanced MRI: Correlation with the Extravasation of Evans Blue in a Rat Model of Transient Cerebral Ischemia

  • Choi, Hyun Seok (Department of Radiology, College of Medicine, The Catholic University of Korea) ;
  • Ahn, Sung Soo (Department of Radiology, College of Medicine, Yonsei University) ;
  • Shin, Na-Young (Department of Radiology, College of Medicine, Yonsei University) ;
  • Kim, Jinna (Department of Radiology, College of Medicine, Yonsei University) ;
  • Kim, Jae Hyung (Department of Radiology, College of Medicine, Seoul National University) ;
  • Lee, Jong Eun (Department of Anatomy, College of Medicine, Yonsei University) ;
  • Lee, Hye Yeon (Department of Anatomy, College of Medicine, Yonsei University) ;
  • Heo, Ji Hoe (Department of Neurology, College of Medicine, Yonsei University) ;
  • Lee, Seung-Koo (Department of Radiology, College of Medicine, Yonsei University)
  • Received : 2014.10.14
  • Accepted : 2015.03.16
  • Published : 2015.08.01

Abstract

Objective: The purpose of this study was to correlate permeability parameters measured with dynamic contrast-enhanced magnetic resonance imaging (DCE-MRI) using a clinical 3-tesla scanner with extravasation of Evans blue in a rat model with transient cerebral ischemia. Materials and Methods: Sprague-Dawley rats (n = 13) with transient middle cerebral artery occlusion were imaged using a 3-tesla MRI with an 8-channel wrist coil. DCE-MRI was performed 12 hours, 18 hours, and 36 hours after reperfusion. Permeability parameters ($K^{trans}$, $v_e$, and $v_p$) from DCE-MRI were calculated. Evans blue was injected after DCE-MRI and extravasation of Evans blue was correlated as a reference with the integrity of the blood-brain barrier. Correlation analysis was performed between permeability parameters and the extravasation of Evans blue. Results: All permeability parameters ($K^{trans}$, $v_e$, and $v_p$) showed a linear correlation with extravasation of Evans blue. Among them, $K^{trans}$ showed highest values of both the correlation coefficient and the coefficient of determination (0.687 and 0.473 respectively, p < 0.001). Conclusion: Permeability parameters obtained by DCE-MRI at 3-T are well-correlated with Evans blue extravasation, and $K^{trans}$ shows the strongest correlation among the tested parameters.

Keywords

Acknowledgement

Grant : 연세의과학사업단

References

  1. 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;333:1581-1587 https://doi.org/10.1056/NEJM199512143332401
  2. Lansberg MG, Albers GW, Wijman CA. Symptomatic intracerebral hemorrhage following thrombolytic therapy for acute ischemic stroke: a review of the risk factors. Cerebrovasc Dis 2007;24:1-10
  3. Tanne D, Kasner SE, Demchuk AM, Koren-Morag N, Hanson S, Grond M, et al. Markers of increased risk of intracerebral hemorrhage after intravenous recombinant tissue plasminogen activator therapy for acute ischemic stroke in clinical practice: the Multicenter rt-PA Stroke Survey. Circulation 2002;105:1679-1685 https://doi.org/10.1161/01.CIR.0000012747.53592.6A
  4. Intracerebral hemorrhage after intravenous t-PA therapy for ischemic stroke. The NINDS t-PA Stroke Study Group. Stroke 1997;28:2109-2118 https://doi.org/10.1161/01.STR.28.11.2109
  5. Barber PA, Demchuk AM, Zhang J, Buchan AM. 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 https://doi.org/10.1016/S0140-6736(00)02237-6
  6. Kase CS, Furlan AJ, Wechsler LR, Higashida RT, Rowley HA, Hart RG, et al. Cerebral hemorrhage after intra-arterial thrombolysis for ischemic stroke: the PROACT II trial. Neurology 2001;57:1603-1610 https://doi.org/10.1212/WNL.57.9.1603
  7. Larrue V, von Kummer RR, Muller A, Bluhmki E. 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 https://doi.org/10.1161/01.STR.32.2.438
  8. Lansberg MG, Thijs VN, Bammer R, Kemp S, Wijman CA, Marks MP, et al. Risk factors of symptomatic intracerebral hemorrhage after tPA therapy for acute stroke. Stroke 2007;38:2275-2278 https://doi.org/10.1161/STROKEAHA.106.480475
  9. Alsop DC, Makovetskaya E, Kumar S, Selim M, Schlaug G. Markedly reduced apparent blood volume on bolus contrast magnetic resonance imaging as a predictor of hemorrhage after thrombolytic therapy for acute ischemic stroke. Stroke 2005;36:746-750 https://doi.org/10.1161/01.STR.0000158913.91058.93
  10. Kim EY, Na DG, Kim SS, Lee KH, Ryoo JW, Kim HK. Prediction of hemorrhagic transformation in acute ischemic stroke: role of diffusion-weighted imaging and early parenchymal enhancement. AJNR Am J Neuroradiol 2005;26:1050-1055
  11. Hacke W, Albers G, Al-Rawi Y, Bogousslavsky J, Davalos A, Eliasziw M, et al. The Desmoteplase in Acute Ischemic Stroke Trial (DIAS): a phase II MRI-based 9-hour window acute stroke thrombolysis trial with intravenous desmoteplase. Stroke 2005;36:66-73 https://doi.org/10.1161/01.STR.0000149938.08731.2c
  12. Olivot JM, Mlynash M, Thijs VN, Kemp S, Lansberg MG, Wechsler L, et al. Relationships between infarct growth, clinical outcome, and early recanalization in diffusion and perfusion imaging for understanding stroke evolution (DEFUSE). Stroke 2008;39:2257-2263 https://doi.org/10.1161/STROKEAHA.107.511535
  13. Bang OY, Saver JL, Alger JR, Shah SH, Buck BH, Starkman S, et al. Patterns and predictors of blood-brain barrier permeability derangements in acute ischemic stroke. Stroke 2009;40:454-461 https://doi.org/10.1161/STROKEAHA.108.522847
  14. Selim M, Fink JN, Kumar S, Caplan LR, Horkan C, Chen Y, 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 https://doi.org/10.1161/01.STR.0000023577.65990.4E
  15. Lin K, Kazmi KS, Law M, Babb J, Peccerelli N, Pramanik BK. Measuring elevated microvascular permeability and predicting hemorrhagic transformation in acute ischemic stroke using first-pass dynamic perfusion CT imaging. AJNR Am J Neuroradiol 2007;28:1292-1298 https://doi.org/10.3174/ajnr.A0539
  16. Hom J, Dankbaar JW, Soares BP, Schneider T, Cheng SC, Bredno J, et al. Blood-brain barrier permeability assessed by perfusion CT predicts symptomatic hemorrhagic transformation and malignant edema in acute ischemic stroke. AJNR Am J Neuroradiol 2011;32:41-48 https://doi.org/10.3174/ajnr.A2244
  17. Lin K. Predicting transformation to type 2 parenchymal hematoma in acute ischemic stroke by CT permeability imaging. AJNR Am J Neuroradiol 2011;32:E124; author reply E125 https://doi.org/10.3174/ajnr.A2602
  18. Kassner A, Roberts T, Taylor K, Silver F, Mikulis D. Prediction of hemorrhage in acute ischemic stroke using permeability MR imaging. AJNR Am J Neuroradiol 2005;26:2213-2217
  19. Kassner A, Roberts TP, Moran B, Silver FL, Mikulis DJ. Recombinant tissue plasminogen activator increases blood-brain barrier disruption in acute ischemic stroke: an MR imaging permeability study. AJNR Am J Neuroradiol 2009;30:1864-1869 https://doi.org/10.3174/ajnr.A1774
  20. Larsson HB, Courivaud F, Rostrup E, Hansen AE. Measurement of brain perfusion, blood volume, and blood-brain barrier permeability, using dynamic contrast-enhanced T(1)-weighted MRI at 3 tesla. Magn Reson Med 2009;62:1270-1281 https://doi.org/10.1002/mrm.22136
  21. Thornhill RE, Chen S, Rammo W, Mikulis DJ, Kassner A. Contrast-enhanced MR imaging in acute ischemic stroke: T2* measures of blood-brain barrier permeability and their relationship to T1 estimates and hemorrhagic transformation. AJNR Am J Neuroradiol 2010;31:1015-1022 https://doi.org/10.3174/ajnr.A2003
  22. Warach S, Latour LL. 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(11 Suppl 1):2659-2661 https://doi.org/10.1161/01.STR.0000144051.32131.09
  23. Sandoval KE, Witt KA. Blood-brain barrier tight junction permeability and ischemic stroke. Neurobiol Dis 2008;32:200-219 https://doi.org/10.1016/j.nbd.2008.08.005
  24. Wang CX, Shuaib A. Critical role of microvasculature basal lamina in ischemic brain injury. Prog Neurobiol 2007;83:140-148 https://doi.org/10.1016/j.pneurobio.2007.07.006
  25. Dirnagl U, Iadecola C, Moskowitz MA. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 1999;22:391-397 https://doi.org/10.1016/S0166-2236(99)01401-0
  26. Ahn SK, Hong S, Park YM, Lee WT, Park KA, Lee JE. Effects of agmatine on hypoxic microglia and activity of nitric oxide synthase. Brain Res 2011;1373:48-54 https://doi.org/10.1016/j.brainres.2010.12.002
  27. Kassner A, Mandell DM, Mikulis DJ. Measuring permeability in acute ischemic stroke. Neuroimaging Clin N Am 2011;21:315-325, x-xi https://doi.org/10.1016/j.nic.2011.01.004
  28. Kamada H, Yu F, Nito C, Chan PH. Influence of hyperglycemia on oxidative stress and matrix metalloproteinase-9 activation after focal cerebral ischemia/reperfusion in rats: relation to blood-brain barrier dysfunction. Stroke 2007;38:1044-1049 https://doi.org/10.1161/01.STR.0000258041.75739.cb
  29. Belayev L, Busto R, Ikeda M, Rubin LL, Kajiwara A, Morgan L, et al. Protection against blood-brain barrier disruption in focal cerebral ischemia by the type IV phosphodiesterase inhibitor BBB022: a quantitative study. Brain Res 1998;787:277-285 https://doi.org/10.1016/S0006-8993(97)01499-6
  30. Strbian D, Durukan A, Pitkonen M, Marinkovic I, Tatlisumak E, Pedrono E, et al. The blood-brain barrier is continuously open for several weeks following transient focal cerebral ischemia. Neuroscience 2008;153:175-181 https://doi.org/10.1016/j.neuroscience.2008.02.012
  31. Tofts PS, Brix G, Buckley DL, Evelhoch JL, Henderson E, Knopp MV, et al. Estimating kinetic parameters from dynamic contrast-enhanced T(1)-weighted MRI of a diffusable tracer: standardized quantities and symbols. J Magn Reson Imaging 1999;10:223-232 https://doi.org/10.1002/(SICI)1522-2586(199909)10:3<223::AID-JMRI2>3.0.CO;2-S
  32. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 2012;9:671-675 https://doi.org/10.1038/nmeth.2089
  33. Durukan A, Marinkovic I, Strbian D, Pitkonen M, Pedrono E, Soinne L, et al. Post-ischemic blood-brain barrier leakage in rats: one-week follow-up by MRI. Brain Res 2009;1280:158-165 https://doi.org/10.1016/j.brainres.2009.05.025
  34. Jiang Q, Ewing JR, Ding GL, Zhang L, Zhang ZG, Li L, et al. Quantitative evaluation of BBB permeability after embolic stroke in rat using MRI. J Cereb Blood Flow Metab 2005;25:583-592 https://doi.org/10.1038/sj.jcbfm.9600053
  35. Ding G, Jiang Q, Li L, Zhang L, Gang Zhang Z, Ledbetter KA, et al. Detection of BBB disruption and hemorrhage by Gd-DTPA enhanced MRI after embolic stroke in rat. Brain Res 2006;1114:195-203 https://doi.org/10.1016/j.brainres.2006.07.116
  36. Taheri S, Candelario-Jalil E, Estrada EY, Rosenberg GA. Spatiotemporal correlations between blood-brain barrier permeability and apparent diffusion coefficient in a rat model of ischemic stroke. PLoS One 2009;4:e6597 https://doi.org/10.1371/journal.pone.0006597
  37. Neumann-Haefelin C, Brinker G, Uhlenkuken U, Pillekamp F, Hossmann KA, Hoehn M. Prediction of hemorrhagic transformation after thrombolytic therapy of clot embolism: an MRI investigation in rat brain. Stroke 2002;33:1392-1398 https://doi.org/10.1161/01.STR.0000014619.59851.65

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