Assessment of blood-brain barrier disruption using dynamic contrast-enhanced MRI. A systematic review

NeuroImage: Clinical

Volumn 6, Issue , 2014, Pages 262-274

  Heye, Anna K ^a   Culling, Ross D ^b   Valdés Hernández, Maria Del C ^a   Thrippleton, Michael J ^a   Wardlaw, Joanna M ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Blood brain barrier; Dynamic contrast enhanced; MRI; Perfusion; Permeability

Indexed keywords

CONTRAST MEDIUM;

ALZHEIMER DISEASE; BLOOD BRAIN BARRIER; BRAIN CAPILLARY ENDOTHELIAL CELL; BRAIN ISCHEMIA; BRAIN TISSUE; BRAIN TUMOR; DATA ANALYSIS; DYNAMIC CONTRAST ENHANCED DYNAMIC MAGNETIC RESONANCE IMAGING; HUMAN; INFORMATION PROCESSING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OUTCOME ASSESSMENT; REVIEW; SYSTEMATIC REVIEW; AGED; ANIMAL; MIDDLE AGED; PATHOLOGY; PROCEDURES;

AGED; ANIMALS; BLOOD-BRAIN BARRIER; CONTRAST MEDIA; HUMANS; MAGNETIC RESONANCE IMAGING; MIDDLE AGED;

EID: 84907783871     PISSN: None     EISSN: 22131582     Source Type: Journal    
DOI: 10.1016/j.nicl.2014.09.002     Document Type: Review

References (101)

1. Abbott N.J., and Friedman A. Overview and introduction: the blood-brain barrier in health and disease Epilepsia 53 Suppl 6 2012 1 6 10.1111/j.1528-1167.2012.03696.x 23134489
2. Abo-Ramadan U., Durukan A., Pitkonen M., Marinkovic I., Tatlisumak E., and Pedrono E. Post-ischemic leakiness of the blood-brain barrier: a quantitative and systematic assessment by Patlak plots Experimental Neurology 219 2009 328 333 10.1016/j.expneurol.2009.06.002 19520075
3. Aksoy D., Bammer R., Mlynash M., Venkatasubramanian C., Eyngorn I., and Snider R.W. Magnetic resonance imaging profile of blood-brain barrier injury in patients with acute intracerebral hemorrhage Journal of the American Heart Association 2 2013 e000161 10.1161/JAHA.113.000161 23709564
4. Ali M.M., Janic B., Babajani-Feremi A., Varma N.R.S., Iskander A.S.M., and Anagli J. Changes in vascular permeability and expression of different angiogenic factors following anti-angiogenic treatment in rat glioma PLoS ONE 5 2010 e8727 10.1371/journal.pone.0008727 20090952
5. Armitage P., Behrenbruch C., Brady M., and Moore N. Extracting and visualizing physiological parameters using dynamic contrast-enhanced magnetic resonance imaging of the breast Medical Image Analysis 9 2005 315 329 10.1016/j.media.2005.01.001 15950895
6. Armitage P.A., Farrall A.J., Carpenter T.K., Doubal F.N., and Wardlaw J.M. Use of dynamic contrast-enhanced MRI to measure subtle blood-brain barrier abnormalities Magnetic Resonance Imaging 29 2011 305 314 10.1016/j.mri.2010.09.002 21030178
7. Aryal M.P., Nagaraja T.N., Keenan K.A., Bagher-Ebadian H., Panda S., and Brown S.L. Dynamic contrast enhanced MRI parameters and tumor cellularity in a rat model of cerebral glioma at 7 T Society of Magnetic Resonance in Medicine 71 2014 2206 2214 10.1002/mrm.24873 23878070
8. Awasthi R., Pandey C.M., Sahoo P., Behari S., Kumar V., and Kumar S. Dynamic contrast-enhanced magnetic resonance imaging-derived kep as a potential biomarker of matrix metalloproteinase 9 expression in patients with glioblastoma multiforme: a pilot study Journal of Computer Assisted Tomography 36 2012 125 130 10.1097/RCT.0b013e31823f6c59 22261782
9. Bagher-Ebadian H., Jain R., Nejad-Davarani S.P., Mikkelsen T., Lu M., and Jiang Q. Model selection for DCE-T1 studies in glioblastoma Magnetic Resonance in Medicine: Official Journal of the Society of Magnetic Resonance in Medicine / Society of Magnetic Resonance in Medicine 68 2012 241 251 10.1002/mrm.23211 22127934
10. Barnes S.L., Whisenant J.G., Loveless M.E., and Yankeelov T.E. Practical dynamic contrast enhanced MRI in small animal models of cancer: data acquisition, data analysis, and interpretation Pharmaceutics 4 2012 442 478 10.3390/pharmaceutics4030442 23105959
11. Brandt C.T., Simonsen H., Liptrot M., Søgaard L.V., Lundgren J.D., and Ostergaard C. In vivo study of experimental pneumococcal meningitis using magnetic resonance imaging BMC Medical Imaging 8 2008 1 10.1186/1471-2342-8-1 18194516
12. Brix G., Semmler W., and Port R. Pharmacokinetic parameters in CNS Gd-DTPA enhanced MR imaging Journal of Computer Assisted Tomography 15 1991 621 628 10.1097/00004728-199107000-00018 2061479
13. Brookes J.A., Redpath T.W., Gilbert F.J., Murray A.D., and Staff R.T. Accuracy of T1 measurement in dynamic contrast-enhanced breast MRI using two- and three-dimensional variable flip angle fast low-angle shot Journal of Magnetic Resonance Imaging: JMRI 9 1999 163 171 10.1002/(SICI)1522-2586(199902)9:2<163::AID-JMRI3>3.0.CO;2-L 10077009
14. Budde M.D., Gold E., Jordan E.K., and Frank J.A. Differential microstructure and physiology of brain and bone metastases in a rat breast cancer model by diffusion and dynamic contrast enhanced MRI Clinical & Experimental Metastasis 29 2012 51 62 10.1007/s10585-011-9428-2 22042553
15. Calamante F. Arterial input function in perfusion MRI: a comprehensive review Progress in Nuclear Magnetic Resonance Spectroscopy 74 2013 1 32 10.1016/j.pnmrs.2013.04.002 24083460
16. Cao Y., Tsien C.I., Sundgren P.C., Nagesh V., Normolle D., and Buchtel H. Dynamic contrast-enhanced magnetic resonance imaging as a biomarker for prediction of radiation-induced neurocognitive dysfunction Clinical Cancer Research: an Official Journal of the American Association for Cancer Research 15 2009 1747 1754 10.1158/1078-0432.CCR-08-1420 19223506
17. Cha S., Yang L., Johnson G., Lai A., Chen M.H., and Tihan T. Comparison of microvascular permeability measurements, K Trans, determined with pass T2∗-weighted MR imaging methods in gliomas and meningiomas AJNR. American Journal of Neuroradiology 27 2006 409 417 16484420
18. Chen J., Yao J., and Thomasson D. Automatic determination of arterial input function for dynamic contrast enhanced MRI in tumor assessment Medical Image Computing and Computer-Assisted Intervention: MICCAI. International Conference on Medical Image Computing and Computer-Assisted Intervention 11 2008 594 601 18979795
19. Chu J.-P., Mak H.K.-F., Yau K.K.-W., Zhang L., Tsang J., and Chan Q. Pilot study on evaluation of any correlation between MR perfusion (Ktrans) and diffusion (apparent diffusion coefficient) parameters in brain tumors at 3 Tesla Cancer Imaging: the Official Publication of the International Cancer Imaging Society 12 2012 1 6 10.1102/1470-7330.2012.0001 22275724
20. Cramer S.P., and Larsson H.B.W. Accurate determination of blood-brain barrier permeability using dynamic contrast-enhanced T1-weighted MRI: a simulation and in vivo study on healthy subjects and multiple sclerosis patients Journal of Cerebral Blood Flow and Metabolism: Official Journal of the International Society of Cerebral Blood Flow and Metabolism 2014 1 11 10.1038/jcbfm.2014.126 25074746
21. Cramer S.P., Simonsen H., Frederiksen J.L., Rostrup E., and Larsson H.B.W. Abnormal blood-brain barrier permeability in normal appearing white matter in multiple sclerosis investigated by MRI NeuroImage. Clinical 4 2014 182 189 10.1016/j.nicl.2013.12.001 24371801
22. DCE MRI Technical Committee DCE MRI Quantification Profile, Quantitative Imaging Biomarkers Alliance Version 1.0. Reviewed Draft 2012 Available from: http://rsna.org/QIBA.aspx
23. Durukan A., Marinkovic I., Strbian D., Pitkonen M., Pedrono E., and Soinne L. Post-ischemic blood-brain barrier leakage in rats: one-week follow-up by MRI Brain Research 1280 2009 158 165 10.1016/j.brainres.2009.05.025 19450568
24. Ewing J.R., and Bagher-Ebadian H. Model selection in measures of vascular parameters using dynamic contrast-enhanced MRI: experimental and clinical applications NMR in Biomedicine 26 2013 1028 1041 10.1002/nbm.2996 23881857
25. Ewing J.R., Knight R.A., Nagaraja T.N., Yee J.S., Nagesh V., and Whitton P.A. Patlak plots of Gd-DTPA MRI data yield blood-brain transfer constants concordant with those of 14C-sucrose in areas of blood-brain opening Magnetic Resonance in Medicine: Official Journal of the Society of Magnetic Resonance in Medicine / Society of Magnetic Resonance in Medicine 50 2003 283 292 10.1002/mrm.10524 12876704
26. Ferl G.Z., Xu L., Friesenhahn M., Bernstein L.J., Barboriak D.P., and Port R.E. An automated method for nonparametric kinetic analysis of clinical DCE-MRI data: application to glioblastoma treated with bevacizumab Magnetic Resonance in Medicine: Official Journal of the Society of Magnetic Resonance in Medicine / Society of Magnetic Resonance in Medicine 63 2010 1366 1375 10.1002/mrm.22335 20432307
27. Ferrier M.C., Sarin H., Fung S.H., Schatlo B., Pluta R.M., and Gupta S.N. Validation of dynamic contrast-enhanced magnetic resonance imaging-derived vascular permeability measurements using quantitative autoradiography in the RG2 Rat brain tumor model Neoplasia (New York, N.Y.) 9 2007 546 555 10.1593/neo.07289 17710157
28. Gaitán M.I., and Shea C.D. Evolution of the blood-brain barrier in newly forming multiple sclerosis lesions Annals of Neurology 70 2011 22 29 10.1002/ana.22472 21710622
29. Gal Y., Mehnert A., Bradley A., McMahon K., Kennedy D., and Crozier S. A new denoising method for dynamic contrast-enhanced MRI Annual International Conference of the IEEE Engineering in Medicine and Biology Society 2008 847 850
30. Gupta R.K., Awasthi R., Rathore R.K.S., Verma A., Sahoo P., and Paliwal V.K. Understanding epileptogenesis in calcified neurocysticercosis with perfusion MRI Neurology 78 2012 618 625 10.1212/WNL.0b013e318248deae 22302547
31. Guyatt G.H., Oxman A.D., Vist G.E., Kunz R., Falck-Ytter Y., and Alonso-Coello P. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations BMJ (Clinical Research Ed.) 336 2008 924 926 10.1136/bmj.39489.470347.AD 18436948
32. Haris M., Gupta R.K., Singh A., Husain N., Husain M., and Pandey C.M. Differentiation of infective from neoplastic brain lesions by dynamic contrast-enhanced MRI Neuroradiology 50 2008 531 540 10.1007/s00234-008-0378-6 18379766
33. Haris M., Husain N., Singh A., Awasthi R., Singh Rathore R.K., and Husain M. Dynamic contrast-enhanced (DCE) derived transfer coefficient (ktrans) is a surrogate marker of matrix metalloproteinase 9 (MMP-9) expression in brain tuberculomas Journal of Magnetic Resonance Imaging: JMRI 28 2008 588 597 10.1002/jmri.21491 18777539
34. Haris M., Husain N., Singh A., Husain M., Srivastava S., and Srivastava C. Dynamic contrast-enhanced derived cerebral blood volume correlates better with Leak correction than with No correction for vascular endothelial growth factor, microvascular density, and grading of astrocytoma Journal of Computer Assisted Tomography 32 2008 955 965 10.1097/RCT.0b013e31816200d1 19204461
35. Harrer J.U., Parker G.J.M., Haroon H.A., Buckley D.L., Embelton K., and Roberts C. Comparative study of methods for determining vascular permeability and blood volume in human gliomas Journal of Magnetic Resonance Imaging: JMRI 20 2004 748 757 10.1002/jmri.20182 15503330
36. Hoff B.A., Bhojani M.S., Rudge J., Chenevert T.L., Meyer C.R., and Galbán S. DCE and DW-MRI monitoring of vascular disruption following VEGF-Trap treatment of a rat glioma model NMR in Biomedicine 25 2012 935 942 10.1002/nbm.1814 22190279
37. Iannotti F., Fieschi C., and Alfano B. Simplified, noninvasive PET measurement of blood-brain barrier permeability Journal of Computer Assisted Tomography 11 1987 390 397 10.1097/00004728-198705000-00004 3106433
38. Ingrisch M., Sourbron S., Morhard D., Ertl-Wagner B., and Kümpfel T. Quantification of perfusion and permeability in multiple sclerosis: dynamic contrast-enhanced MRI in 3D at 3T Investigative Radiology 47 2012 252 258 10.1097/RLI.0b013e31823bfc97 22373532
39. Jain R. Measurements of tumor vascular leakiness using DCE in brain tumors: clinical applications NMR in Biomedicine 26 2013 1042 1049 10.1002/nbm.2994 23832526
40. Jelescu I.O., Leppert I.R., Narayanan S., Araújo D., Arnold D.L., and Pike G.B. Dual-temporal resolution dynamic contrast-enhanced MRI protocol for blood-brain barrier permeability measurement in enhancing multiple sclerosis lesions Journal of Magnetic Resonance Imaging: JMRI 33 2011 1291 1300 10.1002/jmri.22565 21590997
41. Jia Z.Z., Geng D.Y., Liu Y., Chen X.R., and Zhang J. Microvascular permeability of brain astrocytoma with contrast-enhanced magnetic resonance imaging: correlation analysis with histopathologic grade Chinese Medicine J2013 126 2013 1953 1956 23673117
42. Kassner A., Roberts T., Taylor K., Silver F., and Mikulis D. Prediction of hemorrhage in acute ischemic stroke using permeability MR imaging AJNR. American Journal of Neuroradiology 26 2005 2213 2217 16219824
43. Kassner A., Roberts T.P.L., Moran B., Silver F.L., and Mikulis D.J. Recombinant tissue plasminogen activator increases blood-brain barrier disruption in acute ischemic stroke: an MR imaging permeability study AJNR. American Journal of Neuroradiology 30 2009 1864 1869 10.3174/ajnr.A1774 19661169
44. Kermode A.G., Tofts P.S., Thompson A.J., MacManus D.G., Rudge P., and Kendall B.E. Heterogeneity of blood-brain barrier changes in multiple sclerosis: an MRI study with gadolinium-DTPA enhancement Neurology 40 1990 229 235 10.1212/WNL.40.2.229 2300240
45. Krueck W.G., Schmiedl U.P., Maravilla K.R., Spence A.M., Starr F.L., and Kenney J. MR assessment of radiation-induced blood-brain barrier permeability changes in rat glioma model AJNR. American Journal of Neuroradiology 15 1994 625 632 8010261
46. Larsen V.A., Simonsen H.J., Law I., Larsson H.B.W., and Hansen A.E. Evaluation of dynamic contrast-enhanced T1-weighted perfusion MRI in the differentiation of tumor recurrence from radiation necrosis Neuroradiology 55 2013 361 369 10.1007/s00234-012-1127-4 23262559
47. Larsson C., Kleppestø M., Rasmussen I., Salo R., Vardal J., and Brandal P. Sampling requirements in DCE-MRI based analysis of high grade gliomas: Simulations and clinical results Journal of Magnetic Resonance Imaging: JMRI 37 2013 818 829 10.1002/jmri.23866 23086710
48. Larsson H.B., Stubgaard M., Frederiksen J.L., Jensen M., Henriksen O., and Paulson O.B. Quantitation of blood-brain barrier defect by magnetic resonance imaging and gadolinium-DTPA in patients with multiple sclerosis and brain tumors Magnetic Resonance in Medicine: Official Journal of the Society of Magnetic Resonance in Medicine / Society of Magnetic Resonance in Medicine 16 1990 117 131 10.1002/mrm.1910160111 2255233
49. Larsson H.B.W., Courivaud F., Rostrup E., and Hansen A.E. Measurement of brain perfusion, blood volume, and blood-brain barrier permeability, using dynamic contrast-enhanced T(1)-weighted MRI at 3 tesla Magnetic Resonance in Medicine: Official Journal of the Society of Magnetic Resonance in Medicine / Society of Magnetic Resonance in Medicine 62 2009 1270 1281 10.1002/mrm.22136 19780145
50. Larsson H.B.W., Frederiksen J., Kjaer L., Henriksen O., and Olesen J. In vivo determination of T1 and T2 in the brain of patients with severe but stable multiple sclerosis Magnetic Resonance in Medicine: Official Journal of the Society of Magnetic Resonance in Medicine / Society of Magnetic Resonance in Medicine 7 1988 43 55 10.1002/mrm.1910070106 3386521
51. Lavini C., and Verhoeff J.J.C. Reproducibility of the gadolinium concentration measurements and of the fitting parameters of the vascular input function in the superior sagittal sinus in a patient population Magnetic Resonance Imaging 28 2010 1420 1430 10.1016/j.mri.2010.06.017 20817379
52. Leach M.O., Morgan B., Tofts P.S., Buckley D.L., Huang W., and Horsfield M.A. Imaging vascular function for early stage clinical trials using dynamic contrast-enhanced magnetic resonance imaging European Radiology 22 2012 1451 1464 10.1007/s00330-012-2446-x 22562143
53. Li K.-L., Buonaccorsi G., Thompson G., Cain J.R., Watkins A., and Russell D. An improved coverage and spatial resolution - using dual injection dynamic contrast-enhanced (ice-DICE) MRI: a novel dynamic contrast-enhanced technique for cerebral tumors Magnetic Resonance in Medicine: Official Journal of the Society of Magnetic Resonance in Medicine / Society of Magnetic Resonance in Medicine 68 2012 452 462 10.1002/mrm.23252 22791559
54. Li K.L., Zhu X.P., Waterton J., and Jackson A. Improved 3D quantitative mapping of blood volume and endothelial permeability in brain tumors Journal of Magnetic Resonance Imaging: JMRI 12 2000 347 357 10.1002/1522-2586(200008)12:2<347::AID-JMRI19>3.3.CO;2-Z 10931600
55. Li X., Rooney W.D., Várallyay C.G., Gahramanov S., Muldoon L.L., and Goodman J.A. Dynamic-contrast-enhanced-MRI with extravasating contrast reagent: Rat cerebral glioma blood volume determination Journal of Magnetic Resonance (San Diego, Calif.: 1997) 206 2010 190 199 10.1016/j.jmr.2010.07.004 20674422
56. Lüdemann L., Hamm B., and Zimmer C. Pharmacokinetic analysis of glioma compartments with dynamic Gd-DTPA-enhanced magnetic resonance imaging Magnetic Resonance Imaging 18 2000 1201 1214 10.1016/S0730-725X(00)00223-X 11167040
57. Lüdemann L., Warmuth C., Plotkin M., Förschler A., Gutberlet M., and Wust P. Brain tumor perfusion: comparison of dynamic contrast enhanced magnetic resonance imaging using T1, T2, and T2∗ contrast, pulsed arterial spin labeling, and H2(15)O positron emission tomography European Journal of Radiology 70 2009 465 474 10.1016/j.ejrad.2008.02.012 18359598
58. Ludemann L., Wurm R., and Zimmer C. Pharmacokinetic modeling of Gd-DTPA extravasation in brain tumors Investigative Radiology 37 2002 562 570 10.1097/00004424-200210000-00005 12352165
59. Manuchehri A.M., Sathyapalan T., Lowry M., Turnbull L.W., Rowland-Hill C., and Atkin S.L. Effect of dopamine agonists on prolactinomas and normal pituitary assessed by dynamic contrast enhanced magnetic resonance imaging (DCE-MRI) Pituitary 10 2007 261 266 10.1007/s11102-007-0048-4 17557207
60. Mills S.J., Soh C., O'Connor J.P.B., Rose C.J., Buonaccorsi G.A., and Cheung S. Tumour enhancing fraction (EnF) in glioma: relationship to tumour grade European Radiology 19 2009 1489 1498 10.1007/s00330-008-1288-z 19198847
61. Miyati T., Banno T., Mase M., Kasai H., Shundo H., and Imazawa M. Dual dynamic contrast-enhanced MR imaging Journal of Magnetic Resonance Imaging: JMRI 7 1997 230 235 10.1002/jmri.1880070136 9039621
62. Nagaraja T.N., Karki K., Ewing J.R., Divine G.W., Fenstermacher D., and Patlak C.S. The MRI-measured arterial input function resulting from a bolus injection of Gd-DTPA in a rat model of stroke slightly underestimates that of Gd-[14C]DTPA and marginally overestimates the blood-to-brain influx rate constant determined by Patlak plots Magnetic Resonance Imaging 63 2010 1502 1509
63. Noseworthy M.D., and Bray T.M. Zinc deficiency exacerbates loss in blood-brain barrier integrity induced by hyperoxia measured by dynamic MRI Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine (New York, N.Y.) 223 2000 175 182 10.1111/j.1525-1373.2000.22324.x 10654621
64. O'Connor J.P.B., Jackson A., Parker G.J.M., Roberts C., and Jayson G.C. Dynamic contrast-enhanced MRI in clinical trials of antivascular therapies Nature Reviews. Clinical Oncology 9 2012 167 177 10.1038/nrclinonc.2012.2 22330689
65. Obermeier B., Daneman R., and Ransohoff R.M. Development, maintenance and disruption of the blood-brain barrier Nature Medicine 19 2013 1584 1596 10.1038/nm.3407 24309662
66. Parker G.J.M., Roberts C., Macdonald A., Buonaccorsi G.A., Cheung S., and Buckley D.L. Experimentally-derived functional form for a population-averaged high-temporal-resolution arterial input function for dynamic contrast-enhanced MRI Magnetic Resonance in Medicine: Official Journal of the Society of Magnetic Resonance in Medicine / Society of Magnetic Resonance in Medicine 56 2006 993 1000 10.1002/mrm.21066 17036301
67. Provenzale J.M., York G., Moya M.G., Parks L., Choma M., and Kealey S. Correlation of relative permeability and relative cerebral blood volume in high-grade cerebral neoplasms AJR. American Journal of Roentgenology 187 2006 1036 1042 10.2214/AJR.04.0676 16985154
68. Quarles C.C., Gore J.C., Xu L., and Yankeelov T.E. Comparison of dual-echo DSC-MRI- and DCE-MRI-derived contrast agent kinetic parameters Magnetic Resonance Imaging 30 2012 944 953 10.1016/j.mri.2012.03.008 22617148
69. Roberts H.C., Roberts T.P., Brasch R.C., and Dillon W.P. Quantitative measurement of microvascular permeability in human brain tumors achieved using dynamic contrast-enhanced MR imaging: correlation with histologic grade AJNR. American Journal of Neuroradiology 21 2000 891 899 10815665
70. Rosenberg G.A. Neurological diseases in relation to the blood-brain barrier Journal of Cerebral Blood Flow and Metabolism: Official Journal of the International Society of Cerebral Blood Flow and Metabolism 32 2012 1139 1151 10.1038/jcbfm.2011.197 22252235
71. Schabel M.C., and Parker D.L. Uncertainty and bias in contrast concentration measurements using spoiled gradient echo pulse sequences Physics in Medicine and Biology 53 2008 2345 2373 10.1088/0031-9155/53/9/010 18421121
72. Shames D.M., Kuwatsuru R., Vexler V., Mühler A., and Brasch R.C. Measurement of capillary permeability to macromolecules by dynamic magnetic resonance imaging: a quantitative noninvasive technique Magnetic Resonance in Medicine: Official Journal of the Society of Magnetic Resonance in Medicine / Society of Magnetic Resonance in Medicine 29 1993 616 622 10.1002/mrm.1910290506 8505897
73. Shinohara R.T., Crainiceanu C.M., and Caffo B.S. Population-wide principal component-based quantification of blood-brain-barrier dynamics in multiple sclerosis Neuroimage 57 2011 1430 1446 10.1016/j.neuroimage.2011.05.038 21635955
74. Singh A., Haris M., Rathore D., Purwar A., Sarma M., and Bayu G. Quantification of physiological and hemodynamic indices using T(1) dynamic contrast-enhanced MRI in intracranial mass lesions Journal of Magnetic Resonance Imaging: JMRI 26 2007 871 880 10.1002/jmri.21080 17896358
75. Song S.K., Lee S.-K., Lee J.J., Lee J.E., Choi H.S., and Sohn Y.H. Blood-brain barrier impairment is functionally correlated with clinical severity in patients of multiple system atrophy Neurobiology of Aging 32 2011 2183 2189 10.1016/j.neurobiolaging.2009.12.017 20149484
76. Sourbron S., Ingrisch M., Siefert A., Reiser M., and Herrmann K. Quantification of cerebral blood flow, cerebral blood volume, and blood-brain-barrier leakage with DCE-MRI Magnetic Resonance in Medicine: Official Journal of the Society of Magnetic Resonance in Medicine / Society of Magnetic Resonance in Medicine 62 2009 205 217 10.1002/mrm.22005 19449435
77. Sourbron S.P., and Buckley D.L. Classic models for dynamic contrast-enhanced MRI NMR in Biomedicine 26 2013 1004 1027 10.1002/nbm.2940 23674304
78. Sourbron S.P., and Buckley D.L. On the scope and interpretation of the Tofts models for DCE-MRI Magnetic Resonance in Medicine: Official Journal of the Society of Magnetic Resonance in Medicine / Society of Magnetic Resonance in Medicine 66 2011 735 745 10.1002/mrm.22861 21384424
79. Sourbron S.P., and Buckley D.L. Tracer kinetic modelling in MRI: estimating perfusion and capillary permeability Physics in Medicine and Biology 57 2012 R1 33 10.1088/0031-9155/57/2/R1 22173205
80. Starr J.M., Farrall A.J., Armitage P., McGurn B., and Wardlaw J. Blood-brain barrier permeability in Alzheimer's disease: A case-control MRI study Psychiatry Research 171 2009 232 241 10.1016/j.pscychresns.2008.04.003 19211227
81. Starr J.M., Wardlaw J., Ferguson K., MacLullich A., Deary I.J., and Marshall I. Increased blood-brain barrier permeability in type II diabetes demonstrated by gadolinium magnetic resonance imaging Journal of Neurology, Neurosurgery, and Psychiatry 74 2003 70 76 10.1136/jnnp.74.1.70 12486269
82. Su M.Y., Head E., Brooks W.M., Wang Z., Muggenburg B.A., and Adam G.E. Magnetic resonance imaging of anatomic and vascular characteristics in a canine model of human aging Neurobiology of Aging 19 1998 479 485 10.1016/S0197-4580(98)00081-5 9880050
83. Taheri S., Candelario-Jalil E., Estrada E.Y., and Rosenberg G.A. Spatiotemporal correlations between blood-brain barrier permeability and apparent diffusion coefficient in a rat model of ischemic stroke PloS One 4 2009 e6597 10.1371/journal.pone.0006597 19668371
84. Taheri S., Gasparovic C., Huisa B.N., Adair J.C., Edmonds E., and Prestopnik J. Blood-brain barrier permeability abnormalities in vascular cognitive impairment Stroke; a Journal of Cerebral Circulation 42 2011 2158 2163 10.1161/STROKEAHA.110.611731 21719768
85. Taheri S., Gasparovic C., Shah N.J., and Rosenberg G.A. Quantitative measurement of blood-brain barrier permeability in human using dynamic contrast-enhanced MRI with fast T1 mapping Magnetic Resonance in Medicine: Official Journal of the Society of Magnetic Resonance in Medicine / Society of Magnetic Resonance in Medicine 65 2011 1036 1042 10.1002/mrm.22686 21413067
86. Thompson E.M., Guillaume D.J., Dósa E., Li X., Nazemi K.J., and Gahramanov S. Dual contrast perfusion MRI in a single imaging session for assessment of pediatric brain tumors Journal of Neuro-Oncology 109 2012 105 114 10.1007/s11060-012-0872-x 22528798
87. Thornhill R.E., Chen S., Rammo W., Mikulis D.J., and 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. American Journal of Neuroradiology 31 2010 1015 1022 10.3174/ajnr.A2003 20190209
88. Tofts P.S., Brix G., Buckley D.L., Evelhoch J.L., Henderson E., and Knopp M.V. Contrast-enhanced T 1 -Weighted MRI of a diffusible tracer: Standardized quantities and symbols Journal of Magnetic Resonance Imaging 232 1999 223 232
89. Tofts P.S., and Kermode A.G. Measurement of the blood-brain barrier permeability and leakage space using dynamic MR imaging. 1. Fundamental concepts Magnetic Resonance in Medicine: Official Journal of the Society of Magnetic Resonance in Medicine / Society of Magnetic Resonance in Medicine 17 1991 357 367 10.1002/mrm.1910170208 2062210
90. Topakian R., Barrick T.R., Howe F.A., and Markus H.S. Blood-brain barrier permeability is increased in normal-appearing white matter in patients with lacunar stroke and leucoaraiosis Journal of Neurology, Neurosurgery, and Psychiatry 81 2010 192 197 10.1136/jnnp.2009.172072 19710048
91. Türkbey B., Thomasson D., Pang Y., Bernardo M., and Choyke P.L. The role of dynamic contrast-enhanced MRI in cancer diagnosis and treatment Diagnostic and Interventional Radiology (Ankara, Turkey) 16 2010 186 192 10.4261/1305-3825.DIR.2537-08.1 19885783
92. Vidarsson L., Thornhill R.E., Liu F., Mikulis D.J., and Kassner A. Quantitative permeability magnetic resonance imaging in acute ischemic stroke: how long do we need to scan? Magnetic Resonance Imaging 27 2009 1216 1222 10.1016/j.mri.2009.01.019 19695816
93. Wang H., Golob E.J., and Su M.-Y. Vascular volume and blood-brain barrier permeability measured by dynamic contrast enhanced MRI in hippocampus and cerebellum of patients with MCI and normal controls Journal of Magnetic Resonance Imaging: JMRI 24 2006 695 700 10.1002/jmri.20669 16878309
94. Wardlaw J.M., Doubal F., Armitage P., Chappell F., Carpenter T., and Muñoz Maniega S. Lacunar stroke is associated with diffuse blood-brain barrier dysfunction Annals of Neurology 65 2009 194 202 10.1002/ana.21549 19260033
95. Wardlaw J.M., Farrall A., Armitage P.A., Carpenter T., Chappell F., and Doubal F. Changes in background blood-brain barrier integrity between lacunar and cortical ischemic stroke subtypes Stroke; a Journal of Cerebral Circulation 39 2008 1327 1332 10.1161/STROKEAHA.107.500124 18309161
96. Wei X.-E., Wang D., Li M.-H., Zhang Y.-Z., Li Y.-H., and Li W.-B. A useful tool for the initial assessment of blood-brain barrier permeability after traumatic brain injury in rabbits: dynamic contrast-enhanced magnetic resonance imaging Journal of Trauma 71 2011 1645 1650 10.1097/TA.0b013e31823498eb 22182873
97. Weinmann H.J., Laniado M., and Mützel W. Pharmacokinetics of GdDTPA/dimeglumine after intravenous injection into healthy volunteers Physiological Chemistry and Physics and Medical NMR 16 1984 167 172 6505043
98. Wilkinson I.D., Jellineck D.A., Levy D., Giesel F.L., Romanowski C.A.J., and Miller B.-A. Dexamethasone and enhancing solitary cerebral mass lesions: alterations in perfusion and blood-tumor barrier kinetics shown by magnetic resonance imaging Neurosurgery 58 2006 640 646 10.1227/01.NEU.0000204873.68395.A0 16575327
99. Yankeelov T.E., Luci J.J., Lepage M., Li R., Debusk L., and Lin P.C. Quantitative pharmacokinetic analysis of DCE-MRI data without an arterial input function: a reference region model Magnetic Resonance Imaging 23 2005 519 529 10.1016/j.mri.2005.02.013 15919597
100. Zhang N., Zhang L., Qiu B., Meng L., Wang X., and Hou B.L. Correlation of volume transfer coefficient Ktrans with histopathologic grades of gliomas Journal of Magnetic Resonance Imaging: JMRI 36 2012 355 363 10.1002/jmri.23675 22581762
101. Zhu X.P., Li K.L., Kamaly-Asl I.D., Checkley D.R., Tessier J.J., and Waterton J.C. Quantification of endothelial permeability, leakage space, and blood volume in brain tumors using combined T1 and T2∗ contrast-enhanced dynamic MR imaging Journal of Magnetic Resonance Imaging: JMRI 11 2000 575 585 10.1002/1522-2586(200006)11:6<575::AID-JMRI2>3.0.CO;2-1 10862055