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

Volumn 34, Issue 10, 2014, Pages 1655-1665

  Cramer, Stig P ^a   Larsson, Henrik B W ^a,b  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

blood brain barrier; cerebral hemodynamics; MRI; multiple sclerosis; perfusion weighted MRI

Indexed keywords

ACCURACY; ADULT; ARTICLE; BLOOD BRAIN BARRIER; BRAIN BLOOD FLOW; BRAIN BLOOD VOLUME; BRAIN DAMAGE; CLINICAL ARTICLE; COMPARTMENT MODEL; CONTRAST ENHANCEMENT; CONTROLLED STUDY; DYNAMIC CONTRAST ENHANCED MAGNETIC RESONANCE IMAGING; EXTRACELLULAR SPACE; FEMALE; GRAY MATTER; HUMAN; IN VIVO STUDY; MALE; MEASUREMENT ACCURACY; MULTIPLE SCLEROSIS; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; OPTIC NEURITIS; PERFUSION WEIGHTED IMAGING; PRIORITY JOURNAL; WHITE MATTER; ALGORITHM; BIOLOGICAL MODEL; COMPUTER SIMULATION; EVALUATION STUDY; METABOLISM; PATHOLOGY; PERMEABILITY; PROCEDURES; SENSITIVITY AND SPECIFICITY; YOUNG ADULT;

ADULT; ALGORITHMS; BLOOD-BRAIN BARRIER; COMPUTER SIMULATION; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MODELS, BIOLOGICAL; MULTIPLE SCLEROSIS; PERMEABILITY; SENSITIVITY AND SPECIFICITY; YOUNG ADULT;

EID: 84921730327     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2014.126     Document Type: Article

References (34)

1. Larsson HB, Stubgaard M, Frederiksen JL, Jensen M, Henriksen O, Paulson OB. Quantitation of blood-brain barrier defect by magnetic resonance imaging and gadolinium-DTPA in patients with multiple sclerosis and brain tumors. Magn Reson Med 1990; 16: 117-131.
2. Tofts PS, Kermode AG. Measurement of the blood-brain barrier permeability and leakage space using dynamic MR imaging. 1. Fundamental concepts. Magn Reson Med 1991; 17: 357-367.
3. Tofts PSP, Brix GG, Buckley DLD, Evelhoch JLJ, Henderson EE, Knopp MVM 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.
4. Sourbron SP, Buckley DL. On the scope and interpretation of the Tofts models for DCE-MRI. Magn Reson Med 2011; 66: 735-745.
5. Luypaert R, Sourbron S, de Mey J. Validity of perfusion parameters obtained using the modified Tofts model: a simulation study. Magn Reson Med 2010; 65: 1491-1497.
6. Patlak CS, Blasberg RG, Fenstermacher JD. Graphical evaluation of blood-to-brain transfer constants from multiple-time uptake data. J Cereb Blood Flow Metab 1983; 3: 1-7.
7. Larsson HBW, Courivaud F, Rostrup E, Hansen AE. Measurement of brain perfusion, blood volume, and blood-brain barrier permeability, using dynamic contrastenhanced T1-weighted MRI at 3 tesla. Magn Reson Med 2009; 62: 1270-1281.
8. Larsson HB, Rosenbaum S, Fritz-Hansen T. Quantification of the effect of water exchange in dynamic contrast MRI perfusion measurements in the brain and heart. Magn Reson Med 2001; 46: 272-281.
9. Moody AR, Martel A, Kenton A, Allder S, Horsfield MA, Delay G et al. Contrastreduced imaging of tissue concentration and arterial level (CRITICAL) for assessment of cerebral hemodynamics in acute stroke by magnetic resonance. Invest Radiol 2000; 35: 401-411.
10. Singh A, Haris M, Rathore D, Purwar A, Sarma M, Bayu G et al. Quantification of physiological and hemodynamic indices using T(1) dynamic contrast-enhanced MRI in intracranial mass lesions. J Magn Reson Imaging 2007; 26: 871-880.
11. Larsson HBW, Hansen AE, Berg HK, Rostrup E, Haraldseth O. Dynamic contrastenhanced quantitative perfusion measurement of the brain using T1-weighted MRI at 3T. J Magn Reson Imaging 2008; 27: 754-762.
12. 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.
13. Hansen AE, Pedersen H, Rostrup E, Larsson HBW. Partial volume effect (PVE) on the arterial input function (AIF) in T1-weighted perfusion imaging and limitations of the multiplicative rescaling approach. Magn Reson Med 2009; 62: 1055-1059.
14. Jelescu IO, Leppert IR, Narayanan S, Araú jo D, Arnold DL, Pike GB. Dual-temporal resolution dynamic contrast-enhanced MRI protocol for blood-brain barrier permeability measurement in enhancing multiple sclerosis lesions. J Magn Reson Imaging 2011; 33: 1291-1300.
15. Brix G, Kiessling F, Lucht R, Darai S, Wasser K, Delorme S et al. Microcirculation and microvasculature in breast tumors: pharmacokinetic analysis of dynamic MR image series. Magn Reson Med 2004; 52: 420-429.
16. Cramer SP, Simonsen H, Frederiksen JL, Rostrup E, Larsson HBW. Abnormal blood-brain barrier permeability in normal appearing white matter in multiple sclerosis investigated by MRI. Neuroimage Clin 2013; 4: 182-189.
17. Lund H, Krakauer M, Skimminge A, Sellebjerg F, Garde E, Siebner HR et al. Bloodbrain barrier permeability of normal appearing white matter in relapsing-remitting multiple sclerosis. PLoS ONE 2013; 8: e56375.
18. Silver NC, Tofts PS, Symms MR, Barker GJ, Thompson AJ, Miller DH. Quantitative contrast-enhanced magnetic resonance imaging to evaluate blood-brain barrier integrity in multiple sclerosis: a preliminary study. Mult Scler 2001; 7: 75-82.
19. Kim SY, Buckwalter M, Soreq H, Vezzani A, Kaufer D. Blood-brain barrier dysfunction-induced inflammatory signaling in brain pathology and epileptogenesis. Epilepsia 2012; 53: 37-44.
20. Oby E, Janigro D. The blood-brain barrier and epilepsy. Epilepsia 2006; 47: 1761-1774.
21. Starr JM, Farrall AJ, 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.
22. Anderson VC, Lenar DP, Quinn JF, Rooney WD. The blood-brain barrier and microvascular water exchange in alzheimer's disease. Cardiovasc Psychiatry Neurol 2011; 2011: 1-9.
23. Taheri S, Gasparovic C, Huisa BN, Adair JC, Edmonds E, Prestopnik J et al. Bloodbrain barrier permeability abnormalities in vascular cognitive impairment. Stroke 2011; 42: 2158-2163.
24. Edvinsson L, Tfelt-Hansen P. The blood-brain barrier in migraine treatment. Cephalalgia 2008; 28: 1245-1258.
25. Gao H-M, Le Li, Zhang K-L, Chen X-H, Tian S-Q, Zhang Z-L. Impact of migraine attacks on the blood-brain barrier. Chin Med J (Engl) 2010; 123: 2559-2561.
26. Winkler MKL, Chassidim Y, Lublinsky S, Revankar GS, Major S, Kang E-J et al. Impaired neurovascular coupling to ictal epileptic activity and spreading depolarization in a patient with subarachnoid hemorrhage: possible link to blood-brain barrier dysfunction. Epilepsia 2012; 53: 22-30.
27. Bell RD, Winkler EA, Sagare AP, Singh I, LaRue B, Deane R et al. Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron 2010; 68: 409-427.
28. Iannotti F, Fieschi C, Alfano B, Picozzi P, Mansi L, Pozzilli C et al. Simplified, noninvasive PET measurement of blood-brain barrier permeability. J Comput Assist Tomogr 1987; 11: 390-397.
29. Ingrisch M, Sourbron S, Morhard D, Ertl-Wagner B, Kü mpfel T, Hohlfeld R et al. Quantification of perfusion and permeability in multiple sclerosis. Invest Radiol 2012; 47: 252-258.
30. Taheri S, Rosenberg GA, Ford C. Quantification of blood-to-brain transfer rate in multiple sclerosis. Mult Scler Relat Disord 2013; 2: 124-132.
31. Ewing JR, Knight RA, Nagaraja TN, Yee JS, Nagesh V, Whitton PA et al. Patlak plots of Gd-DTPA MRI data yield blood-brain transfer constants concordant with those of 14C-sucrose in areas of blood-brain opening. Magn Reson Med 2003; 50: 283-292.
32. Aerts HJWL, Jaspers K, Backes WH. The precision of pharmacokinetic parameters in dynamic contrast-enhanced magnetic resonance imaging: the effect of sampling frequency and duration. Phys Med Biol 2011; 56: 5665-5678.
33. Larsson C, Kleppestø M, Rasmussen I, Salo R, Vardal J, Brandal P et al. Sampling requirements in DCE-MRI based analysis of high grade gliomas: simulations and clinical results. J Magn Reson Imaging 2013; 37: 818-829.
34. Ostergaard L, Weisskoff RM, Chesler DA, Gyldensted C, Rosen BR. High resolution measurement of cerebral blood flow using intravascular tracer bolus passages. Part I: mathematical approach and statistical analysis. Magn Reson Med 1996; 36: 715-725.