Perfusion and vascular permeability: Basic concepts and measurement in DCE-CT and DCE-MRI

Diagnostic and Interventional Imaging

Volumn 94, Issue 12, 2013, Pages 1187-1204

  Cuenod, C A ^a,b   Balvay, D ^b  

^a HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^b PARIS CARDIOVASCULAR RESEARCH CENTER   (France)

Author keywords

Angiogenesis; Capillary permeability; DCE CT; DCE MRI; Perfusion

Indexed keywords

CONTRAST MEDIUM; GADOLINIUM; TRACER;

ARTERIAL BLOOD; ARTICLE; BLOOD FLOW VELOCITY; BLOOD VESSEL PERMEABILITY; BLOOD VOLUME; CAPILLARY WALL; CARDIOVASCULAR SYSTEM; COMPUTED TOMOGRAPHY SCANNER; COMPUTER ASSISTED TOMOGRAPHY; CONTRAST ENHANCEMENT; DATA ANALYSIS; DYNAMIC CONTRAST ENHANCED COMPUTER ASSISTED TOMOGRAPHY; DYNAMIC CONTRAST ENHANCED NUCLEAR MAGNETIC RESONANCE IMAGING; EXTRACELLULAR SPACE; EXTRAVASCULAR SPACE; FIBROSIS; HEMATOCRIT; HUMAN; IMAGING SOFTWARE; INFLAMMATION; INTERSTITIUM; ISCHEMIA; KINETICS; MATHEMATICAL MODEL; MICROCIRCULATION; NEOPLASM; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PERFUSION; PLASMA; PLASMA VOLUME; SURFACE PROPERTY; TISSUE BLOOD FLOW; TISSUE PERFUSION; VENOUS BLOOD;

ANGIOGENESIS; CAPILLARY PERMEABILITY; DCE-CT; DCE-MRI; PERFUSION;

CAPILLARY PERMEABILITY; CONTRAST MEDIA; HUMANS; MAGNETIC RESONANCE IMAGING; MICROCIRCULATION; PERFUSION IMAGING; TOMOGRAPHY, X-RAY COMPUTED;

EID: 84895066688     PISSN: None     EISSN: 22115684     Source Type: Journal    
DOI: 10.1016/j.diii.2013.10.010     Document Type: Short Survey

References (159)

1. Axel L. Cerebral blood flow determination by rapid-sequence computed tomography: theoretical analysis. Radi-ology 1980;137: 679-86. (Pubitemid 11203701)
2. Le Bihan D, Breton E, Lallemand D, Grenier P, Cabanis E, Laval-Jeantet M. MR imaging of intravoxel incoherent motions:application to diffusion and perfusion in neurologic disorders.Radiology 1986;161: 401-7. (Pubitemid 17173295)
3. Detre JA, Eskey CJ, Koretsky AP. Measurement of cerebralblood flow in rat brain by 19F-NMR detection of trifluo-romethane washout. Magn Reson Med 1990;15: 45-57. (Pubitemid 20284012)
4. Schmiedl U, Brasch RC, Ogan MD, Moseley ME. Albuminlabeled with Gd-DTPA. An intravascular contrast-enhancingagent for magnetic resonance blood pool and perfusion imag-ing. Acta Radiol Suppl 1990;374: 99-102.
5. Miles KA. Measurement of tissue perfusion by dynamic com-puted tomography. Br J Radiol 1991;64: 409-12.
6. Tofts PS, Kermode AG. Blood-brain barrier permeability inmultiple sclerosis using labelled DTPA with PET, CT and MRI.J Neurol Neurosurg Psychiatry 1989;52: 1019-20.
7. Larsson HB, Stubgaard M, Frederiksen JL, Jensen M, Henriksen O, Paulson OB. Quantitation of blood-brain barrier defect bymagnetic resonance imaging and gadolinium-DTPA in patientswith multiple sclerosis and brain tumors. Magn Reson Med1990;16: 117-31. (Pubitemid 20353802)
8. Sahani DV, Kalva SP, Hamberg LM, Hahn PF, Willett CG, Saini S, et al. Assessing tumor perfusion and treatment responsein rectal cancer with multisection CT: initial observations.Radiology 2005;234: 785-92. (Pubitemid 40250822)
9. Padhani AR, Hayes C, Assersohn L, Powles T, Makris A, Suck-ling J, et al. Prediction of clinicopathologic response of breastcancer to primary chemotherapy at contrast-enhanced MRimaging: initial clinical results. Radiology 2006;239: 361-74.
10. Morgan B, Utting JF, Higginson A, Thomas AL, Steward WP, Horsfield MA. A simple, reproducible method for monitoringthe treatment of tumours using dynamic contrast-enhancedMR imaging. Br J Cancer 2006;94: 1420-7. (Pubitemid 43772276)
11. O'Connor JP, Jackson A, Parker GJ, Jayson GC. DCE-MRIbiomarkers in the clinical evaluation of antiangiogenicand vascular disrupting agents. Br J Cancer 2007;96: 189-95. (Pubitemid 46160619)
12. Fournier LS, Oudard S, Thiam R, Trinquart L, Banu E, Medioni J, et al. Metastatic renal carcinoma: evaluation of antiangio-genic therapy with dynamic contrast-enhanced CT. Radiology2010;256: 511-8.
13. de Bazelaire C, Calmon R, Thomassin I, Brunon C, Hamy AS, Fournier L, et al. Accuracy of perfusion MRI with high spatialbut low temporal resolution to assess invasive breast can-cer response to neoadjuvant chemotherapy: a retrospectivestudy. BMC Cancer 2011;11:361.
14. Yu HJ, Chen JH, Mehta RS, Nalcioglu O, Su MY. MRI mea-surements of tumor size and pharmacokinetic parameters asearly predictors of response in breast cancer patients under-going neoadjuvant anthracycline chemotherapy. J Magn ResonImaging 2007;26: 615-23. (Pubitemid 350194583)
15. Jain RK, Duda DG, Willett CG, Sahani DV, Zhu AX, Loeffler JS, et al. Biomarkers of response and resistance to antiangiogenictherapy. Nat Rev Clin Oncol 2009;6: 327-38.
16. Kety SS, Schmidt CF. The nitrous oxide method for thequantitative determination of cerebral blood flow in man:theory, procedure and normal values. J Clin Invest 1948;27: 476-83.
17. Johnson JA, Wilson TA. A model for capillary exchange. Am JPhysiol 1966;210: 1299-303.
18. Jacquez JA. Compartmental analysis in biology and medicine.Ann Arbor: The University of Michigan Press; 1985.
19. Kety SS. Regional cerebral blood flow: estimation by means ofnonmetabolized diffusible tracers - an overview. Semin NuclMed 1985;15: 324-8.
20. Patlak CS, Blasberg RG, Fenstermacher JD. Graphical evalua-tion of blood-to-brain transfer constants from multiple-timeuptake data. J Cereb Blood Flow Metab 1983;3: 1-7. (Pubitemid 13129630)
21. Meier P, Zierler KL. On the theory of the indicator-dilutionmethod for measurement of blood flow and volume. J ApplPhysiol 1954;6: 731-44.
22. Villringer A, Rosen BR, Belliveau JW, Ackerman JL, Lauffer RB, Buxton RB, et al. Dynamic imaging with lanthanide chelates innormal brain: contrast due to magnetic susceptibility effects.Magn Reson Med 1988;6: 164-74. (Pubitemid 18066056)
23. Tofts PS, Brix G, Buckley DL, Evelhoch JL, Henderson E, Knopp MV, et al. Estimating kinetic parameters from dynamiccontrast-enhanced T(1)-weighted MRI of a diffusable tracer:standardized quantities and symbols. J Magn Reson Imaging1999;10: 223-32. (Pubitemid 29463104)
24. Brix G, Semmler W, Port R, Schad LR, Layer G, Lorenz WJ.Pharmacokinetic parameters in CNS Gd-DTPA enhanced MRimaging. J Comput Assist Tomogr 1991;15: 621-8.
25. Burstein D, Taratuta E, Manning WJ. Factors in myocardial" perfusion" imaging with ultrafast MRI and Gd-DTPA admin-istration. Magn Reson Med 1991;20: 299-305.
26. Shames DM, Kuwatsuru R, Vexler V, Muhler A, Brasch RC.Measurement of capillary permeability to macromolecules bydynamic magnetic resonance imaging: a quantitative nonin-vasive technique. Magn Reson Med 1993;29: 616-22. (Pubitemid 23138050)
27. Donahue KM, Weisskoff RM, Parmelee DJ, Callahan RJ, Wilkin-son RA, Mandeville JB, et al. Dynamic Gd-DTPA enhanced MRImeasurement of tissue cell volume fraction. Magn Reson Med1995;34: 423-32.
28. Ostergaard L, Weisskoff RM, Chesler DA, Gyldensted C, RosenBR. High resolution measurement of cerebral blood flowusing intravascular tracer bolus passages. Part I: mathe-matical approach and statistical analysis. Magn Reson Med1996;36:715-25. (Pubitemid 26376710)
29. Parker GJ, Tofts PS. Pharmacokinetic analysis of neoplasmsusing contrast-enhanced dynamic magnetic resonance imag-ing. Top Magn Reson Imaging 1999;10: 130-42. (Pubitemid 29510055)
30. Miles KA, Lee TY, Goh V, Klotz E, Cuenod C, Bisdas S, et al. Current status and guidelines for the assessment of tumourvascular support with dynamic contrast-enhanced computedtomography. Eur Radiol 2012;22: 1430-41.
31. Bisdas S, Foo CZ, Thng CH, Vogl TJ, Koh TS. Optimization ofperfusion CT protocol for imaging of extracranial head andneck tumors. J Digit Imaging 2008;22(5): 437-48.
32. Goh V, Halligan S, Bartram CI. Quantitative tumor perfusionassessment with multidetector CT: are measurements fromtwo commercial software packages interchangeable? Radiol-ogy 2007;242: 777-82.
33. Petralia G, Bonello L, Priolo F, Summers P, Bellomi M. BreastMR with special focus on DW-MRI and DCE-MRI. Cancer Imaging2011;11: 76-90.
34. Lassau N, Chapotot L, Benatsou B, Vilgrain V, Kind M, Lacroix J, et al. Standardization of dynamic contrast-enhanced ultrasound for the evaluation of antiangiogenictherapies: the French multicenter Support for Innovativeand Expensive Techniques Study. Invest Radiol 2012;47: 711-6.
35. Folkman J. Tumor angiogenesis: therapeutic implications. NEngl J Med 1971;285: 1182-6.
36. Brasch R, Pham C, Shames D, Roberts T, van Dijke K, vanBruggen N, et al. Assessing tumor angiogenesis using macro-molecular MR imaging contrast media. J Magn Reson Imaging1997;7: 68-74. (Pubitemid 28365640)
37. Miles KA. Tumour angiogenesis and its relation to contrastenhancement on computed tomography: a review. Eur JRadiol 1999;30: 198-205. (Pubitemid 29343737)
38. Neeman M. Preclinical MRI experience in imaging angiogene-sis. Cancer Metastasis Rev 2000;19: 39-43. (Pubitemid 32004690)
39. Padhani AR, Neeman M. Challenges for imaging angiogenesis.Br J Radiol 2001;74: 886-90. (Pubitemid 33064630)
40. Li KC. Angiogenesis imaging in the post-genomic era. Br JRadiol 2003;76(Spec no1):S1-2. (Pubitemid 39530310)
41. McDonald DM, Choyke PL. Imaging of angiogenesis: frommicroscope to clinic. Nat Med 2003;9: 713-25.
42. Choyke PL. Contrast agents for imaging tumor angiogenesis:is bigger better? Radiology 2005;235: 1-2. (Pubitemid 40432224)
43. Cuenod CA, Fournier L, Balvay D, Guinebretiere JM.Tumor angiogenesis: pathophysiology and implications forcontrast-enhanced MRI and CT assessment. Abdom Imaging2006;31: 188-93.
44. Daldrup-Link HE, Simon GH, Brasch RC. Imaging of tumorangiogenesis: current approaches and future prospects. CurrPharm Des 2006;12: 2661-72. (Pubitemid 44017458)
45. Fritz-Hansen T, Rostrup E, Sondergaard L, Ring PB, Amtorp O, Larsson HB. Capillary transfer constant of Gd-DTPA in themyocardium at rest and during vasodilation assessed by MRI.Magn Reson Med 1998;40: 922-9. (Pubitemid 28543845)
46. Lee R, Cheung RT, Hung KN, Au-Yeung KM, Leong LL, Chan FL, et al. Use of CT perfusion to differentiatebetween brain tumour and cerebral infarction. CerebrovascDis 2004;18: 77-83. (Pubitemid 38823838)
47. Wintermark M. Brain perfusion-CT in acute stroke patients.Eur Radiol 2005;15(Suppl 4):D28-31. (Pubitemid 43091063)
48. Choyke PL, Kobayashi H. Functional magnetic resonanceimaging of the kidney using macromolecular contrast agents.Abdom Imaging 2006;31: 224-31.
49. Miles KA, Leggett DA, Bennett GA. CT derived Patlak imagesof the human kidney. Br J Radiol 1999;72: 153-8. (Pubitemid 29095059)
50. Cuenod C, Leconte I, Siauve N, Resten A, Dromain C, Poulet B, et al. Early changes in liver perfusion caused by occultmetastases in rats: detection with quantitative CT. Radiology2001;218: 556-61. (Pubitemid 32121075)
51. Knopp MV, Brix G, Junkermann HJ, Sinn HP. MR mammogra-phy with pharmacokinetic mapping for monitoring of breastcancer treatment during neoadjuvant therapy. Magn ResonImaging Clin N Am 1994;2: 633-58.
52. Thomassin-Naggara I, Bazot M, Darai E, Callard P, Thomassin J, Cuenod CA. Epithelial ovarian tumors: value of dynamiccontrast-enhanced MR imaging and correlation with tumorangiogenesis. Radiology 2008;248: 148-59.
53. Hermans R, Lambin P, Van der Goten A, Van den Bogaert W, Verbist B, Weltens C, et al. Tumoural perfusion as measured bydynamic computed tomography in head and neck carcinoma.Radiother Oncol 1999;53: 105-11.
54. Kauczor HU, Kreitner KF. Contrast-enhanced MRI of the lung.Eur J Radiol 2000;34: 196-207.
55. Kiessling F, Boese J, Corvinus C, Ederle JR, Zuna I, Schoenberg SO, et al. Perfusion CT in patients with advanced bronchialcarcinomas: a novel chance for characterization and treat-ment monitoring? Eur Radiol 2004;14: 1226-33. (Pubitemid 38979216)
56. Dyke JP, Aaron RK. Noninvasive methods of measuring boneblood perfusion. Ann N Y Acad Sci 2010;1192: 95-102.
57. Lin C, Luciani A, Belhadj K, Deux JF, Kuhnowski F, Maatouk M, et al. Multiple myeloma treatment response assessment withwhole-body dynamic contrast-enhanced MR imaging. Radiol-ogy 2010;254: 521-31.
58. Del Vescovo R, Sansoni I, Caviglia R, Ribolsi M, Perrone G, Leoncini E, et al. Dynamic contrast-enhanced magneticresonance imaging of the terminal ileum: differentiationof activity of Crohn's disease. Abdom Imaging 2008;33: 417-24. (Pubitemid 351713068)
59. Bali MA, Metens T, Denolin V, Delhaye M, Demetter P, Clos-set J, et al. Tumoral and nontumoral pancreas: correlationbetween quantitative dynamic contrast-enhanced MR imagingand histopathologic parameters. Radiology 2011;261: 456-66.
60. Salomon LJ, Siauve N, Balvay D, Cuénod CA, Vayssettes C, Luciani A, et al. Placental perfusion MR imaging with contrastagents in a mouse model. Radiology 2005;235: 73-80. (Pubitemid 40432239)
61. Franiel T, Hamm B, Hricak H. Dynamic contrast-enhancedmagnetic resonance imaging and pharmacokinetic models inprostate cancer. Eur Radiol 2011;21: 616-26.
62. Hanna SL, Reddick WE, Parham DM, Gronemeyer SA, Taylor JS, Fletcher BD. Automated pixel-by-pixel mapping of dynamiccontrast-enhanced MR images for evaluation of osteosarcomaresponse to chemotherapy: preliminary results. J Magn ResonImaging 1993;3: 849-53.
63. O'Connor JP, Tofts PS, Miles KA, Parkes LM, Thompson G, Jack-son A. Dynamic contrast-enhanced imaging techniques: CTand MRI. Br J Radiol 2011;84(Spec no2):S112-20.
64. Sourbron SP, Buckley DL. On the scope and interpreta-tion of the Tofts models for DCE-MRI. Magn Reson Med2011;66: 735-45.
65. Stern MD, Lappe DL, Bowen PD, Chimosky JE, HollowayJr GA, Keiser HR, et al. Continuous measurement of tis-sue blood flow by laser-Doppler spectroscopy. Am J Physiol1977;232:H441-8.
66. McDonald DM, Baluk P. Significance of blood vessel leakinessin cancer. Cancer Res 2002;62: 5381-5. (Pubitemid 35024617)
67. Faye N, Fournier L, Balvay D, Taillieu F, Cuenod C, Siauve N, et al. Dynamic contrast-enhanced optical imaging of capillaryleakage. Technol Cancer Res Treat 2011;10: 49-57.
68. Itai Y, Ohtomo K, Kokubo T, Yamauchi T, Minami M, Yashiro N, et al. CT of hepatic masses: significance of pro-longed and delayed enhancement. AJR Am J Roentgenol1986;146: 729-33. (Pubitemid 16117263)
69. Mandeville HC, Ng QS, Daley FM, Barber PR, Pierce G, Finch J, et al. Operable non-small cell lung cancer: correlation ofvolumetric helical dynamic contrast-enhanced CT parameterswith immunohistochemical markers of tumor hypoxia. Radi-ology 2012;264:581-9.
70. Thieme SF, Becker CR, Hacker M, Nikolaou K, Reiser MF, John-son TR. Dual energy CT for the assessment of lung perfusion -correlation to scintigraphy. Eur J Radiol 2008;68(3): 369-74.
71. Goh V, Dattani M, Farwell J, Shekhdar J, Tam E, Patel S, et al. Radiation dose from volumetric helical perfusion CT of thethorax, abdomen or pelvis. Eur Radiol 2011;21: 974-81.
72. Lassau N, Koscielny S, Opolon P, De Baere T, Peronneau P, Leclere J, et al. Evaluation of contrast-enhanced colorDoppler ultrasound for the quantification of angiogenesis invivo. Invest Radiol 2001;36: 50-5. (Pubitemid 32064170)
73. Williams R, Hudson JM, Lloyd BA, Sureshkumar AR, Lueck G, Milot L, et al. Dynamic microbubble contrast-enhancedUS to measure tumor response to targeted therapy: aproposed clinical protocol with results from renal cell car-cinoma patients receiving antiangiogenic therapy. Radiology2011;260: 581-90.
74. van Gelderen P, de Zwart JA, Duyn JH. Pittfalls of MRI mea-surement of white matter perfusion based on arterial spinlabeling. Magn Reson Med 2008;59: 788-95. (Pubitemid 351501944)
75. Detre JA, Zhang W, Roberts DA, Silva AC, Williams DS, Grandis DJ, et al. Tissue specific perfusion imaging using arterial spinlabeling. NMR Biomed 1994;7: 75-82.
76. St Lawrence KS, Owen D, Wang DJ. A two-stage approachfor measuring vascular water exchange and arterial transittime by diffusion-weighted perfusion MRI. Magn Reson Med2012;67: 1275-84.
77. Kwong KK, Belliveau JW, Chesler DA, Goldberg IE, Weisskoff RM, Poncelet BP, et al. Dynamic magnetic resonance imagingof human brain activity during primary sensory stimulation.Proc Natl Acad Sci U S A 1992;89: 5675-9.
78. Gillis P, Peto S, Moiny F, Mispelter J, Cuenod CA. Protontransverse nuclear magnetic relaxation in oxidized blood: anumerical approach. Magn Reson Med 1995;33: 93-100.
79. Towse TF, Slade JM, Ambrose JA, DeLano MC, Meyer RA. Quan-titative analysis of the postcontractile blood-oxygenation-level-dependent (BOLD) effect in skeletal muscle. J ApplPhysiol 2011;111: 27-39.
80. Hunold P, Schlosser T, Vogt FM, Eggebrecht H, Schmermund A, Bruder O, et al. Myocardial late enhancement in contrast-enhanced cardiac MRI: distinction between infarction scarand non-infarction-related disease. AJR Am J Roentgenol2005;184: 1420-6. (Pubitemid 43821809)
81. Thomassin-Naggara I, Darai E, Nassar-Slaba J, Cortez A, Marsault C, Bazot M. Value of dynamic enhanced magneticresonance imaging for distinguishing between ovarian fibromaand subserous uterine leiomyoma. J Comput Assist Tomogr2007;31: 236-42. (Pubitemid 46573362)
82. Ogan MD, Schmiedl U, Moseley ME, Grodd W, Paajanen H, Brasch RC. Albumin labeled with Gd-DTPA. An intravascu-lar contrast-enhancing agent for magnetic resonance bloodpool imaging: preparation and characterization. Invest Radiol1987;22: 665-71. (Pubitemid 17138432)
83. Aicher KP, Dupon JW, White DL, Aukerman SL, Moseley ME, Juster R, et al. Contrast-enhanced magnetic resonance imag-ing of tumor-bearing mice treated with human recombinanttumor necrosis factor alpha. Cancer Res 1990;50: 7376-81.
84. Vexler VS, Clement O, Schmitt-Willich H, Brasch RC. Effectof varying the molecular weight of the MR contrast agent Gd-DTPA-polylysine on blood pharmacokinetics and enhancementpatterns. J Magn Reson Imaging 1994;4: 381-8.
85. Clement O, Vuillemin-Bodaghi V, Cuenod CA, Siauve N, Blus-tajn J, Frija G. Quantification of liver capillary permeabilityusing a macromolecular contrast agent for magnetic reso-nance imaging. Acad Radiol 1996;3(Suppl. 2):S342-3.
86. Jerosch-Herold M, Wilke N, Wang Y, Gong GR, Mansoor AM, Huang H, et al. Direct comparison of an intravascular and anextracellular contrast agent for quantification of myocardialperfusion. Int J Card Imaging 1999;15: 453-64. (Pubitemid 30189171)
87. Daldrup-Link HE, Shames DM, Wendland M, Mühler A, Goss-mann A, Rosenau W, et al. Comparison of Gadomer-17 andgadopentetate dimeglumine for differentiation of benignfrom malignant breast tumors with MR imaging. Acad Radiol2000;7: 934-44.
88. Turetschek K, Floyd E, Shames DM, Roberts TP, Preda A, Novikov V, et al. Assessment of a rapid clearance blood poolMR contrast medium (P792) for assays of microvascular char-acteristics in experimental breast tumors with correlations tohistopathology. Magn Reson Med 2001;45: 880-6. (Pubitemid 32402031)
89. Pradel C, Siauve N, Bruneteau G, Clement O, de Bazelaire C, Frouin F, et al. Reduced capillary perfusion and permeabilityin human tumour xenografts treated with the VEGF signallinginhibitor ZD4190: an in vivo assessment using dynamic MRimaging and macromolecular contrast media. Magn ResonImaging 2003;21: 845-51. (Pubitemid 37377477)
90. de Bazelaire C, Siauve N, Fournier L, Frouin F, Robert P, Clement O, et al. Comprehensive model for simulta-neous MRI determination of perfusion and permeability usinga blood-pool agent in rats rhabdomyosarcoma. Eur Radiol2005;15: 2497-505. (Pubitemid 43153852)
91. Canet E, Revel D, Forrat R, Baldy-Porcher C, de Lorgeril M, Sebbag L, et al. Superparamagnetic iron oxide particlesand positive enhancement for myocardial perfusion studiesassessed by subsecond T1-weighted MRI. Magn Reson Imaging1993;11: 1139-45.
92. Trillaud H, Grenier N, Degreze P, Louail C, Chambon C, Franconi JM. First-pass evaluation of renal perfusion withTurboFLASH MR imaging and superparamagnetic iron oxideparticles. J Magn Reson Imaging 1993;3: 83-91.
93. Morell A, Ahlstrom H, Schoenberg SO, Abildgaard A, Bock M, Bjornerud A. Quantitative renal cortical perfusion inhuman subjects with magnetic resonance imaging using iron-oxide nanoparticles: influence of T1 shortening. Acta Radiol2008;49: 955-62.
94. Kachenoura N, Cluzel P, Frouin F, Toledano D, Grenier P, Cuenod CA, et al. Evaluation of an edge-based registrationmethod: application to magnetic resonance first-pass myocar-dial perfusion data. Magn Reson Imaging 2011;29: 853-60.
95. Xue H, Guehring J, Srinivasan L, Zuehlsdorff S, Saddi K, Chefdhotel C, et al. Evaluation of rigid and non-rigid motioncompensation of cardiac perfusion MRI. Med Image ComputComput Assist Interv 2008;11: 35-43.
96. Buonaccorsi GA, O'Connor JP, Caunce A, Roberts C, Cheung S, Watson Y, et al. Tracer kinetic model-driven registration fordynamic contrast-enhanced MRI time-series data. Magn ResonMed 2007;58: 1010-9. (Pubitemid 350074369)
97. Hachama M, Desolneux A, Cuenod CA, Richard FJ. Aclassifying registration technique for the estimation ofenhancement curves of DCE-CT scan sequences. Med ImageAnal 2010;14: 185-94.
98. Balvay D, Kachenoura N, Espinoza S, Thomassin-Naggara I, Fournier LS, Clement O, et al. Signal-to-noise ratio improve-ment in dynamic contrast-enhanced CT and MR imaging withautomated principal component analysis filtering. Radiology2011;258: 435-45.
99. Bellamy DD, Pereira RS, McKenzie CA, Prato FS, Drost DJ, Sykes J, et al. Gd-DTPA bolus tracking in the myocardium usingT1 fast acquisition relaxation mapping (T1 FARM). Magn ResonMed 2001;46: 555-64. (Pubitemid 32831332)
100. Treier R, Steingoetter A, Fried M, Schwizer W, Boesiger P. Opti-mized and combined T1 and B1 mapping technique for fastand accurate T1 quantification in contrast-enhanced abdom-inal MRI. Magn Reson Med 2007;57: 568-76. (Pubitemid 46385867)
101. Taheri S, Gasparovic C, Shah NJ, Rosenberg GA. Quantitativemeasurement of blood-brain barrier permeability in humanusing dynamic contrast-enhanced MRI with fast T1 mapping.Magn Reson Med 2011;65:1036-42.
102. Utz W, Niendorf T, Wassmuth R, Messroghli D, Dietz R, Schulz-Menger J. Contrast-dose relation in first-pass myocardial MRperfusion imaging. J Magn Reson Imaging 2007;25: 1131-5. (Pubitemid 46870268)
103. De Naeyer D, Verhulst J, Ceelen W, Segers P, De Deene Y, Verdonck P. Flip angle optimization for dynamic contrast-enhanced MRI-studies with spoiled gradient echo pulsesequences. Phys Med Biol 2011;56(16): 5373-95.
104. Zhang JL, Koh TS. On the selection of optimal flip anglesfor T1 mapping of breast tumors with dynamic contrast-enhanced magnetic resonance imaging. IEEE Trans Biomed Eng2006;53: 1209-14. (Pubitemid 43860747)
105. Taillieu F, Salomon LJ, Siauve N, Clément O, Faye N, Balvay D, et al. Placental perfusion and permeability: simultaneousassessment with dual-echo contrast-enhanced MR imaging inmice. Radiology 2006;241: 737-45. (Pubitemid 46190539)
106. Schnall MD, Blume J, Bluemke DA, DeAngelis GA, DeBruhl N, Harms S, et al. Diagnostic architectural and dynamic fea-tures at breast MR imaging: multicenter study. Radiology2006;238: 42-53. (Pubitemid 43010579)
107. Lavini C, de Jonge MC, van de Sande MG, Tak PP, Nederveen AJ, Maas M. Pixel-by-pixel analysis of DCE-MRI curve patternsand an illustration of its application to the imaging of the mus-culoskeletal system. Magn Reson Imaging 2007;25: 604-12. (Pubitemid 46817804)
108. Degani H, Gusis V, Weinstein D, Fields S, Strano S. Mappingpathophysiological features of breast tumors by MRI at highspatial resolution. Nat Med 1997;3: 780-2. (Pubitemid 27298724)
109. Furman-Haran E, Degani H. Parametric analysis of breast MRI.J Comput Assist Tomogr 2002;26: 376-86. (Pubitemid 34564216)
110. Thomassin-Naggara I, Darai E, Cuenod CA, Rouzier R, Callard P, Bazot M. Dynamic contrast-enhanced magnetic resonanceimaging: a useful tool for characterizing ovarian epithelialtumors. J Magn Reson Imaging 2008;28: 111-20. (Pubitemid 351956473)
111. Roberts C, Issa B, Stone A, Jackson A, Waterton JC, ParkerGJ. Comparative study into the robustness of compartmentalmodeling and model-free analysis in DCE-MRI studies. J MagnReson Imaging 2006;23: 554-63.
112. Ostergaard L, Sorensen AG, Kwong KK, Weisskoff RM, Gylden-sted C, Rosen BR. High resolution measurement of cerebralblood flow using intravascular tracer bolus passages. Part II:experimental comparison and preliminary results. Magn ResonMed 1996;36: 726-36. (Pubitemid 26376711)
113. Patel PP, Koppenhafer SL, Scholz TD. Measurement of kineticperfusion parameters of gadoteridol in intact myocardium:effects of ischemia/reperfusion and coronary vasodilation.Magn Reson Imaging 1995;13: 799-806.
114. Miles KA, Kelley BB. CT measurements of capillary permeabil-ity within nodal masses: a potential technique for assessingthe activity of lymphoma. Br J Radiol 1997;70: 74-9. (Pubitemid 27077561)
115. St Lawrence KS, Lee TY. An adiabatic approximation tothe tissue homogeneity model for water exchange in thebrain: I. Theoretical derivation. J Cereb Blood Flow Metab1998;18: 1365-77. (Pubitemid 28559684)
116. Brix G, Bahner ML, Hoffmann U, Horvath A, Schreiber W.Regional blood flow, capillary permeability, and compart-mental volumes: measurement with dynamic CT - initialexperience. Radiology 1999;210: 269-76. (Pubitemid 29004315)
117. Dennis Cheong LH, Tchoyoson Lim CC, Koh TS. Dynamiccontrast-enhanced CT of intracranial meningioma: compar-ison of distributed and compartmental tracer kinetic models- initial results. Radiology 2004;232: 921-30. (Pubitemid 39100283)
118. Balvay D, Frouin F, Calmon G, Bessoud B, Kahn E, Siauve N, et al. New criteria for assessing fit quality in dynamiccontrast-enhanced T1-weighted MRI for perfusion and perme-ability imaging. Magn Reson Med 2005;54: 868-77. (Pubitemid 41457058)
119. Thomassin-Naggara I, Balvay D, Cuenod CA, Darai E, Marsault C, Bazot M. Dynamic contrast-enhanced MR imaging to assessphysiologic variations of myometrial perfusion. Eur Radiol2010;20(4): 984-94.
120. Sourbron S, Ingrisch M, Siefert A, Reiser M, Herrmann K. Quan-tification of cerebral blood flow, cerebral blood volume, andblood-brain-barrier leakage with DCE-MRI. Magn Reson Med2009;62: 205-17.
121. Donaldson SB, West CM, Davidson SE, Carrington BM, Hutchi-son G, Jones AP, et al. A comparison of tracer kinetic modelsfor T1-weighted dynamic contrast-enhanced MRI: applicationin carcinoma of the cervix. Magn Reson Med 2010;63: 691-700.
122. Larsson HB, Courivaud F, Rostrup E, Hansen AE. Measurementof brain perfusion, blood volume, and blood-brain barrier per-meability, using dynamic contrast-enhanced T(1)-weightedMRI at 3 tesla. Magn Reson Med 2009;62: 1270-81.
123. Koh TS, Cheong LH, Hou Z, Soh YC. A physiologic modelof capillary-tissue exchange for dynamic contrast-enhancedimaging of tumor microcirculation. IEEE Trans Biomed Eng2003;50: 159-67. (Pubitemid 36330914)
124. Dennis Cheong LH, Markus Tan CK, Koh TS, Tchoyoson Lim CC, Bisdas S. Functional imaging: dynamic contrast-enhanced ctusing a distributed-parameter physiologic model for accessingstroke and intracranial tumor. Conf Proc IEEE Eng Med Biol Soc2005;1: 294-7. (Pubitemid 46228853)
125. Brochot C, Bessoud B, Balvay D, Cuenod CA, Siauve N, BoisFY. Evaluation of antiangiogenic treatment effects on tumors'microcirculation by Bayesian physiological pharmacokineticmodeling and magnetic resonance imaging. Magn Reson Imag-ing 2006;24: 1059-67. (Pubitemid 44402976)
126. Leach MO, Brindle KM, Evelhoch JL, Griffiths JR, Horsman MR, Jackson A, et al. The assessment of antiangiogenic and anti-vascular therapies in early-stage clinical trials using magneticresonance imaging: issues and recommendations. Br J Cancer2005;92: 1599-610. (Pubitemid 40756468)
127. Tofts PS, Berkowitz B, Schnall MD. Quantitative analysis ofdynamic Gd-DTPA enhancement in breast tumors using a per-meability model. Magn Reson Med 1995;33: 564-8.
128. Sourbron SP, Buckley DL. Tracer kinetic modelling in MRI: esti-mating perfusion and capillary permeability. Phys Med Biol2012;57:R1-33.
129. Ewing JR, Brown SL, Lu M, Panda S, Ding G, Knight RA, et al. Model selection in magnetic resonance imaging measure-ments of vascular permeability: gadomer in a 9L model of ratcerebral tumor. J Cereb Blood Flow Metab 2006;26: 310-20.
130. Brix G, Zwick S, Kiessling F, Griebel J. Pharmacokineticanalysis of tissue microcirculation using nested models: mul-timodel inference and parameter identifiability. Med Phys2009;36: 2923-33.
131. Balvay D, Troprès I, Billet R, Joubert A, Péoc'h M, Cuenod CA, et al. Mapping the zonal organization of tumor per-fusion and permeability in a rat glioma model by usingdynamic contrast-enhanced synchrotron radiation CT. Radi-ology 2009;250: 692-702.
132. Li X, Welch EB, Chakravarthy AB, Xu L, Arlinghaus LR, Farley J, et al. Statistical comparison of dynamic contrast-enhancedMRI pharmacokinetic models in human breast cancer. MagnReson Med 2012;68: 261-71.
133. Cheng HL. Investigation and optimization of parameter accu-racy in dynamic contrast-enhanced MRI. J Magn Reson Imaging2008;28: 736-43.
134. Ashton E, Raunig D, Ng C, Kelcz F, McShane T, Evelhoch J. Scan-rescan variability in perfusion assessment of tumors in MRIusing both model and data-derived arterial input functions. JMagn Reson Imaging 2008;28: 791-6.
135. van der Schaaf I, Vonken EJ, Waaijer A, Velthuis B, Quist M, van Osch T. Influence of partial volume on venous out-put and arterial input function. AJNR Am J Neuroradiol2006;27: 46-50. (Pubitemid 46939882)
136. Calamante F, Morup M, Hansen LK. Defining a local arterialinput function for perfusion MRI using independent compo-nent analysis. Magn Reson Med 2004;52:789-97. (Pubitemid 39314981)
137. Mouridsen K, Christensen S, Gyldensted L, Ostergaard L.Automatic selection of arterial input function using clusteranalysis. Magn Reson Med 2006;55: 524-31. (Pubitemid 43352550)
138. Ashton E, McShane T, Evelhoch J. Inter-operator variabilityin perfusion assessment of tumors in MRI using automatedAIF detection. Med Image Comput Comput Assist IntervInt Conf Med Image Comput Comput Assist Interv 2005;8: 451-8. (Pubitemid 43828282)
139. Padhani AR. Functional MRI for anticancer therapy assess-ment. Eur J Cancer 2002;38: 2116-27. (Pubitemid 35223249)
140. Parker GJ, Roberts C, Macdonald A, Buonaccorsi GA, Cheung S, Buckley DL, et al. Experimentally-derived functional formfor a population-averaged high-temporal-resolution arterialinput function for dynamic contrast-enhanced MRI. MagnReson Med 2006;56: 993-1000. (Pubitemid 44691341)
141. Port RE, Knopp MV, Brix G. Dynamic contrast-enhanced MRIusing Gd-DTPA: interindividual variability of the arterial inputfunction and consequences for the assessment of kinetics intumors. Magn Reson Med 2001;45: 1030-8.
142. Kim SM, Haider MA, Milosevic M, Jaffray DA, Yeung IW.A method for patient dose reduction in dynamic contrast-enhanced CT study. Med Phys 2011;38: 5094-103.
143. Yankeelov TE, Luci JJ, Lepage M, Li R, Debusk L, Lin PC, et al. Quantitative pharmacokinetic analysis of DCE-MRI data with-out an arterial input function: a reference region model. MagnReson Imaging 2005;23: 519-29. (Pubitemid 40779238)
144. Hsiao IT, Liao YP, Liu HL. Study of onset time-shift andinjection duration in DCE-MRI: a comparison of a referenceregion model with the general kinetic model. NMR Biomed2010;23: 375-81.
145. Materne R, Smith AM, Peeters F, Dehoux JP, Keyeux A, Hors-mans Y, et al. Assessment of hepatic perfusion parameterswith dynamic MRI. Magn Reson Med 2002;47: 135-42. (Pubitemid 34019702)
146. Koh TS, Thng CH, Lee PS, Hartono S, Rumpel H, Goh BC, et al. Hepatic metastases: in vivo assessment of perfusionparameters at dynamic contrast-enhanced MR imaging withdual-input two-compartment tracer kinetics model. Radiol-ogy 2008;249: 307-20.
147. d'Arcy JA, Collins DJ, Padhani AR, Walker-Samuel S, Suck-ling J, Leach MO. Informatics in radiology (infoRAD): MagneticResonance Imaging Workbench: analysis and visualization ofdynamic contrast-enhanced MR imaging data. Radiographics2006;26: 621-32. (Pubitemid 43515329)
148. Cuenod CA, Favetto B, Genon-Catalot V, Rozenholc Y, Sam-son A. Parameter estimation and change-point detection fromdynamic contrast-enhanced MRI data using stochastic differ-ential equations. Math Biosci 2011;233(1): 68-76.
149. Hayes C, Padhani AR, Leach MO. Assessing changes in tumourvascular function using dynamic contrast-enhanced magneticresonance imaging. NMR Biomed 2002;15: 154-63. (Pubitemid 34213405)
150. Stoutjesdijk MJ, Veltman J, Huisman H, Karssemeijer N, Bar-entsz JO, Blickman JG, et al. Automated analysis of contrastenhancement in breast MRI lesions using mean shift clusteringfor ROI selection. J Magn Reson Imaging 2007;26: 606-14. (Pubitemid 350194582)
151. O'Connor JP, Rose CJ, Jackson A, Watson Y, Cheung S, Maders F, et al. DCE-MRI biomarkers of tumour heterogeneity pre-dict CRC liver metastasis shrinkage following bevacizumaband FOLFOX-6. Br J Cancer 2011;105: 139-45.
152. Alic L, van Vliet M, van Dijke CF, Eggermont AM, Veen-land JF, Niessen WJ. Heterogeneity in DCE-MRI parametricmaps: a biomarker for treatment response? Phys Med Biol2011;56: 1601-16.
153. Yang X, Knopp MV. Quantifying tumor vascular heterogeneitywith dynamic contrast-enhanced magnetic resonance imag-ing: a review. J Biomed Biotechnol 2011;2011:732848.
154. Kelm BM, Menze BH, Nix O, Zechmann CM, Hamprecht FA.Estimating kinetic parameter maps from dynamic contrast-enhanced MRI using spatial prior knowledge. IEEE Trans MedImaging 2009;28: 1534-47.
155. Zöllner FG, Sance R, Rogelj P, Ledesma-Carbayo MJ, RørvikJ, Santos A, et al. Assessment of 3D DCE-MRI of the kidneysusing non-rigid image registration and segmentation of voxeltime courses. Comput Med Imaging Graph 2009;33: 171-81.
156. Eyal E, Badikhi D, Furman-Haran E, Kelcz F, Kirshenbaum KJ, Degani H. Principal component analysis of breast DCE-MRIadjusted with a model-based method. J Magn Reson Imaging2009;30: 989-98.
157. Chen L, Choyke PL, Chan TH, Chi CY, Wang G, Wang Y.Tissue-specific compartmental analysis for dynamic contrast-enhanced MR imaging of complex tumors. IEEE Trans MedImaging 2011;30: 2044-58.
158. Tofts PS. Modeling tracer kinetics in dynamic Gd-DTPA MRimaging. J Magn Reson Imaging 1997;7: 91-101. (Pubitemid 28365643)
159. Larsson HB, Fritz-Hansen T, Rostrup E, Sondergaard L, Ring P, Henriksen O. Myocardial perfusion modeling using MRI. MagnReson Med 1996;35: 716-26. (Pubitemid 26134567)