Quantifying blood‐brain barrier leakage in small vessel disease: Review and consensus recommendations

Abstract

Cerebral small vessel disease (cSVD) comprises pathological processes of the small vessels in the brain that may manifest clinically as stroke, cognitive impairment, dementia, or gait disturbance. It is generally accepted that endothelial dysfunction, including blood‐brain barrier (BBB) failure, is pivotal in the pathophysiology. Recent years have seen increasing use of imaging, primarily dynamic contrast‐enhanced magnetic resonance imaging, to assess BBB leakage, but there is considerable variability in the approaches and findings reported in the literature. Although dynamic contrast‐enhanced magnetic resonance imaging is well established, challenges emerge in cSVD because of the subtle nature of BBB impairment. The purpose of this work, authored by members of the HARNESS Initiative, is to provide an in‐depth review and position statement on magnetic resonance imaging measurement of subtle BBB leakage in clinical research studies, with aspects requiring further research identified. We further aim to provide information and consensus recommendations for new investigators wishing to study BBB failure in cSVD and dementia.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 93

1. 1.

   Wardlaw J.M., Smith C., Dichgans M. Mechanisms of sporadic cerebral small vessel disease: insights from neuroimaging. Lancet Neurol. 2013;12:483-497.

   Not in our library10.1016/s1474-4422(13)70060-7

2. 2.

   Wardlaw J.M., Smith E.E., Biessels G.J., Cordonnier C., Fazekas F., Frayne R. Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol. 2013;12:822-838.

   Not in our library10.1016/s1474-4422(13)70124-8

3. 3.

   Blair G.W., Hernandez M.V., Thrippleton M.J., Doubal F.N., Wardlaw J.M. Advanced neuroimaging of cerebral small vessel disease. Curr Treat Options Cardiovasc Med. 2017;19:56.

   Not in our library10.1007/s11936-017-0555-1

4. 4.

   Blair G.W., Appleton J.P., Law Z.K., Doubal F., Flaherty K., Dooley R. Preventing cognitive decline and dementia from cerebral small vessel disease: The LACI-1 Trial. Protocol and statistical analysis plan of a phase IIa dose escalation trial testing tolerability, safety and effect on intermediary endpoints of isosorbide mononitrate and cilostazol, separately and in combination. Int J Stroke. 2018;13:530-538.

   Not in our library10.1177/1747493017731947

5. 5.

   Farrall A.J., Wardlaw J.M. Blood-brain barrier: Ageing and microvascular disease–systematic review and meta-analysis. Neurobiol Aging. 2009;30:337-352.

   Not in our library10.1016/j.neurobiolaging.2007.07.015

6. 6.

   Heye A.K., Culling R.D., Valdes Hernandez Mdel C., Thrippleton M.J., Wardlaw J.M. Assessment of blood-brain barrier disruption using dynamic contrast-enhanced MRI. A systematic review. Neuroimage Clin. 2014;6:262-274.

   Not in our library10.1016/j.nicl.2014.09.002

7. 7.
   Tracer kinetic modelling for DCE-MRI quantification of subtle blood–brain barrier permeability · 2016

   No notice
8. 8.

   Sourbron S.P., Buckley D.L. Classic models for dynamic contrast-enhanced MRI. NMR Biomed. 2013;26:1004-1027.

   Not in our library10.1002/nbm.2940

9. 9.

   Smith E.E., Biessels G.J., De Guio F., de Leeuw F.E., Duchesne S., During M. Harmonizing brain magnetic resonance imaging methods for vascular contributions to neurodegeneration. Alzheimers Dement (Amst). 2019;11:191-204.

   Not in our library10.1016/j.dadm.2019.01.002

10. 10.
    Imaging biomarker roadmap for cancer studies · 2016

    No notice
11. 11.

    Taheri S., Gasparovic C., Huisa B.N., Adair J.C., Edmonds E., Prestopnik J. Blood-brain barrier permeability abnormalities in vascular cognitive impairment. Stroke. 2011;42:2158-2163.

    Not in our library10.1161/strokeaha.110.611731

12. 12.

    Zhang C.E., Wong S.M., van de Haar H.J., Staals J., Jansen J.F., Jeukens C.R. Blood-brain barrier leakage is more widespread in patients with cerebral small vessel disease. Neurology. 2017;88:426-432.

    Not in our library10.1212/wnl.0000000000003556

13. 13.

    Huisa B.N., Caprihan A., Thompson J., Prestopnik J., Qualls C.R., Rosenberg G.A. Long-term blood-brain barrier permeability changes in Binswanger disease. Stroke. 2015;46:2413-2418.

    Not in our library10.1161/strokeaha.115.009589

14. 14.

    Hanyu H., Asano T., Tanaka Y., Iwamoto T., Takasaki M., Abe K. Increased blood-brain barrier permeability in white matter lesions of Binswanger's disease evaluated by contrast-enhanced MRI. Dement Geriatr Cogn Disord. 2002;14:1-6.

    Not in our library10.1159/000058326

15. 15.

    Starr J.M., Farrall A.J., Armitage P., McGurn B., Wardlaw J. Blood-brain barrier permeability in Alzheimer's disease: A case-control MRI study. Psychiatry Res. 2009;171:232-241.

    Not in our library10.1016/j.pscychresns.2008.04.003

16. 16.

    Raja R., Rosenberg G.A., Caprihan A. MRI measurements of Blood-Brain Barrier function in dementia: A review of recent studies. Neuropharmacology. 2017;134:259-271.

    Not in our library10.1016/j.neuropharm.2017.10.034

17. 17.

    Montagne A., Barnes S.R., Sweeney M.D., Halliday M.R., Sagare A.P., Zhao Z. Blood-brain barrier breakdown in the aging human hippocampus. Neuron. 2015;85:296-302.

    Not in our library10.1016/j.neuron.2014.12.032

18. 18.

    Zhang C.E., Wong S.M., Uiterwijk R., Backes W.H., Jansen J.F.A., Jeukens C. Blood-brain barrier leakage in relation to white matter hyperintensity volume and cognition in small vessel disease and normal aging. Brain Imaging Behav. 2019;13:389-395.

    Not in our library10.1007/s11682-018-9855-7

19. 19.

    Wang H., Golob E.J., 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. J Magn Reson Imaging. 2006;24:695-700.

    Not in our library10.1002/jmri.20669

20. 20.

    Bronge L., Wahlund L.O. White matter lesions in dementia: an MRI study on blood-brain barrier dysfunction. Dement Geriatr Cogn Disord. 2000;11:263-267.

    Not in our library10.1159/000017248

21. 21.

    Munoz Maniega S., Chappell F.M., Valdes Hernandez M.C., Armitage P.A., Makin S.D., Heye A.K. Integrity of normal-appearing white matter: Influence of age, visible lesion burden and hypertension in patients with small-vessel disease. J Cereb Blood Flow Metab. 2017;37:644-656.

    Not in our library10.1177/0271678x16635657

22. 22.

    Topakian R., Barrick T.R., Howe F.A., Markus H.S. Blood-brain barrier permeability is increased in normal-appearing white matter in patients with lacunar stroke and leucoaraiosis. J Neurol Neurosur Psychiatry. 2010;81:192-197.

    Not in our library10.1136/jnnp.2009.172072

23. 23.

    Wardlaw J.M., Doubal F., Armitage P., Chappell F., Carpenter T., Munoz Maniega S. Lacunar stroke is associated with diffuse blood-brain barrier dysfunction. Ann Neurol. 2009;65:194-202.

    Not in our library10.1002/ana.21549

24. 24.

    Wardlaw J.M., Doubal F.N., Valdes-Hernandez M., Wang X., Chappell F.M., Shuler K. Blood-brain barrier permeability and long-term clinical and imaging outcomes in cerebral small vessel disease. Stroke. 2013;44:525-527.

    Not in our library10.1161/strokeaha.112.669994

25. 25.

    Wardlaw J.M., Farrall A., Armitage P.A., Carpenter T., Chappell F., Doubal F. Changes in background blood-brain barrier integrity between lacunar and cortical ischemic stroke subtypes. Stroke. 2008;39:1327-1332.

    Not in our library10.1161/strokeaha.107.500124

26. 26.

    Wardlaw J.M., Makin S.J., Hernandez M.C.V., Armitage P.A., Heye A.K., Chappell F.M. Blood-brain barrier failure as a core mechanism in cerebral small vessel disease and dementia: Evidence from a cohort study. Alzheimers Dement. 2017;13:634-643.

    Not in our library

27. 27.

    Starr J.M., Wardlaw J., Ferguson K., MacLullich A., Deary I.J., Marshall I. Increased blood-brain barrier permeability in type II diabetes demonstrated by gadolinium magnetic resonance imaging. J Neurol Neurosurg Psychiatry. 2003;74:70-76.

    Not in our library10.1136/jnnp.74.1.70

28. 28.

    Israeli D., Tanne D., Daniels D., Last D., Shneor R., Guez D. The application of MRI for depiction of subtle blood brain barrier disruption in stroke. Int J Biol Sci. 2011;7:1-8.

    Not in our library10.7150/ijbs.7.1

29. 29.

    van de Haar H.J., Jansen J.F.A., van Osch M.J.P., van Buchem M.A., Muller M., Wong S.M. Neurovascular unit impairment in early Alzheimer's disease measured with magnetic resonance imaging. Neurobiol Aging. 2016;45:190-196.

    Not in our library10.1016/j.neurobiolaging.2016.06.006

30. 30.

    van de Haar H.J., Burgmans S., Jansen J.F., van Osch M.J., van Buchem M.A., Muller M. Blood-brain barrier leakage in patients with early alzheimer disease. Radiology. 2016;281:527-535.

    Not in our library10.1148/radiol.2016152244

31. 31.

    Li Y., Li M., Zuo L., Shi Q., Qin W., Yang L. Compromised blood-brain barrier integrity is associated with total magnetic resonance imaging burden of cerebral small vessel disease. Front Neurol. 2018;9:221.

    Not in our library10.3389/fneur.2018.00221

32. 32.

    Staals J., Makin S.D., Doubal F.N., Dennis M.S., Wardlaw J.M. Stroke subtype, vascular risk factors, and total MRI brain small-vessel disease burden. Neurology. 2014;83:1228-1234.

    Not in our library10.1212/wnl.0000000000000837

33. 33.

    Armitage P.A., Farrall A.J., Carpenter T.K., Doubal F.N., Wardlaw J.M. Use of dynamic contrast-enhanced MRI to measure subtle blood-brain barrier abnormalities. Magn Reson Imaging. 2011;29:305-314.

    Not in our library10.1016/j.mri.2010.09.002

34. 34.

    Cramer S.P., Larsson H.B. 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. J Cereb Blood Flow Metab. 2014;34:1655-1665.

    Not in our library10.1038/jcbfm.2014.126

35. 35.

    Barnes S.R., Ng T.S., Montagne A., Law M., Zlokovic B.V., Jacobs R.E. Optimal acquisition and modeling parameters for accurate assessment of low Ktrans blood-brain barrier permeability using dynamic contrast-enhanced MRI. Magn Reson Med. 2016;75:1967-1977.

    Not in our library10.1002/mrm.25793

36. 36.

    Wong S.M., Jansen J.F.A., Zhang C.E., Staals J., Hofman P.A.M., van Oostenbrugge R.J. Measuring subtle leakage of the blood-brain barrier in cerebrovascular disease with DCE-MRI: Test-retest reproducibility and its influencing factors. J Magn Reson Imaging. 2017;46:159-166.

    Not in our library10.1002/jmri.25540

37. 37.

    Lupo J.M., Cha S., Chang S.M., Nelson S.J. Dynamic susceptibility-weighted perfusion imaging of high-grade gliomas: Characterization of spatial heterogeneity. AJNR Am J Neuroradiol. 2005;26:1446-1454.

    Not in our library

38. 38.

    Thornhill R.E., Chen S., Rammo W., Mikulis D.J., 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.

    Not in our library10.3174/ajnr.a2003

39. 39.

    Arba F., Leigh R., Inzitari D., Warach S.J., Luby M., Lees K.R. Blood-brain barrier leakage increases with small vessel disease in acute ischemic stroke. Neurology. 2017;89:2143-2150.

    Not in our library10.1212/wnl.0000000000004677

40. 40.

    Rost N.S., Cougo P., Lorenzano S., Li H., Cloonan L., Bouts M.J. Diffuse microvascular dysfunction and loss of white matter integrity predict poor outcomes in patients with acute ischemic stroke. J Cereb Blood Flow Metab. 2018;38:75-86.

    Not in our library10.1177/0271678x17706449

41. 41.

    Quarles C.C., Gochberg D.F., Gore J.C., Yankeelov T.E. A theoretical framework to model DSC-MRI data acquired in the presence of contrast agent extravasation. Phys Med Biol. 2009;54:5749-5766.

    Not in our library10.1088/0031-9155/54/19/006

42. 42.

    Sourbron S., Heilmann M., Biffar A., Walczak C., Vautier J., Volk A. Bolus-tracking MRI with a simultaneous T1- and T2*-measurement. Magn Reson Med. 2009;62:672-681.

    Not in our library10.1002/mrm.22042

43. 43.

    Hales P.W., Clark C.A. Combined arterial spin labeling and diffusion-weighted imaging for noninvasive estimation of capillary volume fraction and permeability-surface product in the human brain. J Cerebr Blood F Met. 2013;33:67-75.

    Not in our library10.1038/jcbfm.2012.125

44. 44.

    Lawrence K.S., Owen D., Wang D.J.J. A two-stage approach for measuring vascular water exchange and arterial transit time by diffusion-weighted perfusion MRI. Magn Reson Med. 2012;67:1275-1284.

    Not in our library10.1002/mrm.23104

45. 45.

    Wang J.J., Fernandez-Seara M.A., Wang S.M., St Lawrence K.S. When perfusion meets diffusion: in vivo measurement of water permeability in human brain. J Cerebr Blood F Met. 2007;27:839-849.

    Not in our library10.1038/sj.jcbfm.9600398

46. 46.

    Gregori J., Schuff N., Kern R., Gunther M. T2-based arterial spin labeling measurements of blood to tissue water transfer in human brain. J Magn Reson Imaging. 2013;37:332-342.

    Not in our library10.1002/jmri.23822

47. 47.

    Liu P., Uh J., Lu H. Determination of spin compartment in arterial spin labeling MRI. Magn Reson Med. 2011;65:120-127.

    Not in our library10.1002/mrm.22601

48. 48.

    Schmid S., Teeuwisse W.M., Lu H., van Osch M.J. Time-efficient determination of spin compartments by time-encoded pCASL T2-relaxation-under-spin-tagging and its application in hemodynamic characterization of the cerebral border zones. Neuroimage. 2015;123:72-79.

    Not in our library10.1016/j.neuroimage.2015.08.025

49. 49.

    Lin Z., Li Y., Su P., Mao D., Wei Z., Pillai J.J. Non-contrast MR imaging of blood-brain barrier permeability to water. Magn Reson Med. 2018;80:1507-1520.

    Not in our library10.1002/mrm.27141

50. 50.

    Kim Y.R., Tejima E., Huang S., Atochin D.N., Dai G., Lo E.H. In vivo quantification of transvascular water exchange during the acute phase of permanent stroke. Magn Reson Med. 2008;60:813-821.

    Not in our library10.1002/mrm.21708

51. 51.

    Freeze W.M., Schnerr R.S., Palm W.M., Jansen J.F., Jacobs H.I., Hoff E.I. Pericortical enhancement on delayed postgadolinium fluid-attenuated inversion recovery images in normal aging, mild cognitive impairment, and Alzheimer disease. AJNR Am J Neuroradiol. 2017;38:1742-1747.

    Not in our library10.3174/ajnr.a5273

52. 52.

    Cho A.H., Cho Y.P., Lee D.H., Kwon T.W., Kwon S.U., Suh D.C. Reperfusion injury on magnetic resonance imaging after carotid revascularization. Stroke. 2014;45:602-604.

    Not in our library10.1161/strokeaha.113.003792

53. 53.

    Latour L.L., Kang D.W., Ezzeddine M.A., Chalela J.A., Warach S. Early blood-brain barrier disruption in human focal brain ischemia. Ann Neurol. 2004;56:468-477.

    Not in our library10.1002/ana.20199

54. 54.

    Iannotti F., Fieschi C., Alfano B., Picozzi P., Mansi L., Pozzilli C. Simplified, noninvasive pet measurement of blood-brain-barrier permeability. J Comput Assist Tomo. 1987;11:390-397.

    Not in our library10.1097/00004728-198705000-00004

55. 55.

    Pozzilli C., Picozzi P. Modifications of blood-brain-barrier in multiple-sclerosis - a study with positron emission tomography. Med-Riv Enc Med Ital. 1987;7:457-459.

    Not in our library

56. 56.

    Schlageter N.L., Carson R.E., Rapoport S.I. Examination of blood-brain-barrier permeability in dementia of the Alzheimer Type with [Ga-68] Edta and positron emission tomography. J Cerebr Blood F Met. 1987;7:1-8.

    Not in our library10.1038/jcbfm.1987.1

57. 57.

    Zhou Y., Huang S.C., Hoh C.K., Cloughesy T., Yang J., Phelps M.E. Gallium-68 EDTA PET study of brain tumor BBB permeability changes induced by intra-arterial RMP7. J Nucl Med. 1996;37:642.

    Not in our library

58. 58.

    Partridge W.M. Introduction to the Blood-Brain Barrier: Methodology, Biology and Pathology. 2006.

    Not in our library

59. 59.

    Dysken M.W., Nelson M.J., Hoover K.M., Kuskowski M., McGeachie R. Rapid dynamic CT scanning in primary degenerative dementia and age-matched controls. Biol Psychiatry. 1990;28:425-434.

    Not in our library10.1016/0006-3223(90)90410-4

60. 60.

    Caserta M.T., Caccioppo D., Lapin G.D., Ragin A., Groothuis D.R. Blood-brain barrier integrity in Alzheimer's disease patients and elderly control subjects. J Neuropsychiatry Clin Neurosci. 1998;10:78-84.

    Not in our library10.1176/jnp.10.1.78

61. 61.

    van de Haar H.J., Burgmans S., Hofman P.A.M., Verhey F.R.J., Jansen J.F.A., Backes W.H. Blood-brain barrier impairment in dementia: Current and future in vivo assessments. Neurosci Biobehav R. 2015;49:71-81.

    Not in our library10.1016/j.neubiorev.2014.11.022

62. 62.

    Larsson H.B., Courivaud F., Rostrup E., 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. Magn Reson Med. 2009;62:1270-1281.

    Not in our library10.1002/mrm.22136

63. 63.

    Rohrer M., Bauer H., Mintorovitch J., Requardt M., Weinmann H.J. Comparison of magnetic properties of MRI contrast media solutions at different magnetic field strengths. Invest Radiol. 2005;40:715-724.

    Not in our library10.1097/01.rli.0000184756.66360.d3

64. 64.

    Pintaske J., Martirosian P., Graf H., Erb G., Lodemann K.P., Claussen C.D. Relaxivity of Gadopentetate Dimeglumine (Magnevist), Gadobutrol (Gadovist), and Gadobenate Dimeglumine (MultiHance) in human blood plasma at 0.2, 1.5, and 3 Tesla. Invest Radiol. 2006;41:213-221.

    Not in our library10.1097/01.rli.0000197668.44926.f7

65. 65.

    Taheri S., Gasparovic C., Shah N.J., Rosenberg G.A. Quantitative measurement of blood-brain barrier permeability in human using dynamic contrast-enhanced MRI with fast T1 mapping. Magn Reson Med. 2011;65:1036-1042.

    Not in our library10.1002/mrm.22686

66. 66.

    Lu H., Clingman C., Golay X., van Zijl P.C. Determining the longitudinal relaxation time (T1) of blood at 3.0 Tesla. Magn Reson Med. 2004;52:679-682.

    Not in our library10.1002/mrm.20178

67. 67.

    Wu W.C., Jain V., Li C., Giannetta M., Hurt H., Wehrli F.W. In vivo venous blood T1 measurement using inversion recovery true-FISP in children and adults. Magn Reson Med. 2010;64:1140-1147.

    Not in our library10.1002/mrm.22484

68. 68.

    Stikov N., Boudreau M., Levesque I.R., Tardif C.L., Barral J.K., Pike G.B. On the accuracy of T1 mapping: searching for common ground. Magn Reson Med. 2015;73:514-522.

    Not in our library10.1002/mrm.25135

69. 69.

    Deoni S.C. High-resolution T1 mapping of the brain at 3T with driven equilibrium single pulse observation of T1 with high-speed incorporation of RF field inhomogeneities (DESPOT1-HIFI). J Magn Reson Imaging. 2007;26:1106-1111.

    Not in our library10.1002/jmri.21130

70. 70.

    Yarnykh V.L. Actual flip-angle imaging in the pulsed steady state: A method for rapid three-dimensional mapping of the transmitted radiofrequency field. Magn Reson Med. 2007;57:192-200.

    Not in our library10.1002/mrm.21120

71. 71.

    Sourbron S., Ingrisch M., Siefert A., Reiser M., Herrmann K. Quantification of cerebral blood flow, cerebral blood volume, and blood-brain-barrier leakage with DCE-MRI. Magn Reson Med. 2009;62:205-217.

    Not in our library10.1002/mrm.22005

72. 72.

    van de Haar H.J., Jansen J.F.A., Jeukens C., Burgmans S., van Buchem M.A., Muller M. Subtle blood-brain barrier leakage rate and spatial extent: Considerations for dynamic contrast-enhanced MRI. Med Phys. 2017;44:4112-4125.

    Not in our library10.1002/mp.12328

73. 73.

    Boschi F., Marzola P., Sandri M., Nicolato E., Galie M., Fiorini S. Tumor microvasculature observed using different contrast agents: a comparison between Gd-DTPA-Albumin and B-22956/1 in an experimental model of mammary carcinoma. MAGMA. 2008;21:169-176.

    Not in our library10.1007/s10334-008-0106-6

74. 74.

    Notohamiprodjo M., Pedersen M., Glaser C., Helck A.D., Lodemann K.P., Jespersen B. Comparison of Gd-DTPA and Gd-BOPTA for studying renal perfusion and filtration. J Magn Reson Imaging. 2011;34:595-607.

    Not in our library10.1002/jmri.22640

75. 75.

    Richardson O.C., Bane O., Scott M.L., Tanner S.F., Waterton J.C., Sourbron S.P. Gadofosveset-based biomarker of tissue albumin concentration: Technical validation in vitro and feasibility in vivo. Magn Reson Med. 2015;73:244-253.

    Not in our library10.1002/mrm.25128

76. 76.

    Thomsen H.S., Morcos S.K., Almen T., Bellin M.F., Bertolotto M., Bongartz G. Nephrogenic systemic fibrosis and gadolinium-based contrast media: Updated ESUR Contrast Medium Safety Committee guidelines. Eur Radiol. 2013;23:307-318.

    Not in our library10.1007/s00330-012-2597-9

77. 77.

    EMA. EMA's final opinion confirms restrictions on use of linear gadolinium agents in body scans (EMA/457616/2017). 2017.

    Not in our library

78. 78.

    FDA. FDA Drug Safety Communication: FDA warns that gadolinium-based contrast agents (GBCAs) are retained in the body; requires new class warnings (12-19-2017). 2017.

    Not in our library

79. 79.

    Gulani V., Calamante F., Shellock F.G., Kanal E., Reeder S.B., on behalf of the International Society for Magnetic Resonance in Medicine. Gadolinium deposition in the brain: summary of evidence and recommendations. Lancet Neurol. 2017;16:564-570.

    Not in our library10.1016/s1474-4422(17)30158-8

80. 80.

    Jenkinson M., Bannister P., Brady M., Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage. 2002;17:825-841.

    Not in our library10.1016/s1053-8119(02)91132-8

81. 81.

    Akbudak E., Conturo T.E. Arterial input functions from MR phase imaging. Magn Reson Med. 1996;36:809-815.

    Not in our library10.1002/mrm.1910360602

82. 82.

    Korporaal J.G., van den Berg C.A., van Osch M.J., Groenendaal G., van Vulpen M., van der Heide U.A. Phase-based arterial input function measurements in the femoral arteries for quantification of dynamic contrast-enhanced (DCE) MRI and comparison with DCE-CT. Magn Reson Med. 2011;66:1267-1274.

    Not in our library10.1002/mrm.22905

83. 83.

    Sourbron S.P., Buckley D.L. Tracer kinetic modelling in MRI: Estimating perfusion and capillary permeability. Phys Med Biol. 2012;57:R1-R33.

    Not in our library10.1088/0031-9155/57/2/r1

84. 84.

    Brix G., Zwick S., Kiessling F., Griebel J. Pharmacokinetic analysis of tissue microcirculation using nested models: Multimodel inference and parameter identifiability. Med Phys. 2009;36:2923-2933.

    Not in our library10.1118/1.3147145

85. 85.

    Ingrisch M., Sourbron S., Reiser M.F., Peller M. Model selection in dynamic contrast enhanced MRI: The Akaike Information Criterion. Ifmbe Proc. 2010;25:356-358.

    Not in our library

86. 86.

    Paudyal R., Poptani H., Cai K., Zhou R., Glickson J.D. Impact of transvascular and cellular-interstitial water exchange on dynamic contrast-enhanced magnetic resonance imaging estimates of blood to tissue transfer constant and blood plasma volume. J Magn Reson Imaging. 2013;37:435-444.

    Not in our library10.1002/jmri.23837

87. 87.

    Ingrisch M., Sourbron S., Morhard D., Ertl-Wagner B., Kumpfel T., Hohlfeld R. Quantification of perfusion and permeability in multiple sclerosis: dynamic contrast-enhanced MRI in 3D at 3T. Invest Radiol. 2012;47:252-258.

    Not in our library10.1097/rli.0b013e31823bfc97

88. 88.

    Parker G.J., Roberts C., Macdonald A., Buonaccorsi G.A., Cheung S., Buckley D.L. Experimentally-derived functional form for a population-averaged high-temporal-resolution arterial input function for dynamic contrast-enhanced MRI. Magn Reson Med. 2006;56:993-1000.

    Not in our library10.1002/mrm.21066

89. 89.

    Tofts P.S., Kermode A.G. Measurement of the blood-brain barrier permeability and leakage space using dynamic MR imaging. 1. Fundamental concepts. Magn Reson Med. 1991;17:357-367.

    Not in our library10.1002/mrm.1910170208

90. 90.

    Weinmann H.J., Laniado M., Mutzel W. Pharmacokinetics of GdDTPA/dimeglumine after intravenous injection into healthy volunteers. Physiol Chem Phys Med NMR. 1984;16:167-172.

    Not in our library

91. 91.

    Lavini C., Verhoeff J.J. 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. Magn Reson Imaging. 2010;28:1420-1430.

    Not in our library10.1016/j.mri.2010.06.017

92. 92.

    Tropres I., Pannetier N., Grand S., Lemasson B., Moisan A., Peoc'h M. Imaging the microvessel caliber and density: Principles and applications of microvascular MRI. Magn Reson Med. 2015;73:325-341.

    Not in our library10.1002/mrm.25396

93. 93.

    Tofts P.S., Brix G., Buckley D.L., Evelhoch J.L., Henderson E., Knopp M.V. 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.

    Not in our library10.1002/(sici)1522-2586(199909)10:3<223::aid-jmri2>3.0.co;2-s

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.