Imaging tumor vascular heterogeneity and angiogenesis using dynamic contrast-enhanced magnetic resonance imaging

Clinical Cancer Research

Volumn 13, Issue 12, 2007, Pages 3449-3459

  Jackson, Alan ^a   O'Connor, James P B ^a,b   Parker, Geoff J M ^a   Jayson, Gordon C ^b  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b CHRISTIE HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

4 (4 FLUORO 2 METHYL 5 INDOLYLOXY) 6 METHOXY 7 [3 (1 PYRROLIDINYL)PROPOXY]QUINAZOLINE; AXITINIB; BEVACIZUMAB; COMBRETASTATIN; SORAFENIB; VATALANIB;

ANGIOGENESIS; CLINICAL TRIAL; CONTRAST ENHANCEMENT; HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; REVIEW; TUMOR;

ANGIOGENESIS INHIBITORS; ANIMALS; CLINICAL TRIALS; HUMANS; IMAGE ENHANCEMENT; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC;

EID: 34250778970     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-07-0238     Document Type: Review

References (114)

1. Jackson A, Buckley DL, Parker GJM. Dynamic contrast-enhanced magnetic resonance imaging in oncology. Berlin: Springer; 2005.
2. Leach MO, Brindle KM, Evelhoch JL, et al. The assessment of antiangiogenic and antivascular therapies in early-stage clinical trials using magnetic resonance imaging: issues and recommendations. Br J Cancer 2005;92:1599-610.
3. Blasberg R. Imaging update: new windows, new views. Clin Cancer Res 2007;13:3444-8.
4. Tofts PS, Brix G, Buckley DL, 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;10:223-32.
5. 1-weighted DCE-MRI. In: Jackson A, Buckley DL, Parker GJM, editors. Dynamic contrast-enhanced magnetic resonance imaging in oncology. Berlin: Springer 2005; p. 81-92.
6. 1-weighted dynamic contrast-enhanced MRI. In: Jackson A, Buckley DL, Parker GJM, editors. Dynamic contrast-enhanced magnetic resonance imaging in oncology. Berlin: Springer-Verlag 2005; p.69-79.
7. Stack J, Redmond O, Codd M, et al. Breast disease: tissue characterization with Gd-DTPA enhancement profiles. Radiology 1990;174:491-4.
8. Flickinger F, Allison J, Sherry R, Wright J. Differentiation of benign from malignant breast masses by time-intensity evaluation of contrast enhanced MRI. Magn Reson Imaging 1993;11:617-20.
9. Roberts C, Issa B, Stone A, et al. Comparative study into the robustness of compartmental modeling and model-free analysis in DCE-MRI studies. J Magn Reson Imaging 2006;23:554-63.
10. Knopp MV, Weiss E, Sinn HP, et al. Pathophysiologic basis of contrast enhancement in breast tumors. J Magn Reson Imaging 1999;10:260-6.
11. Kuhl CK, Mielcareck P, Klaschik S, et al. Dynamic breast MR imaging: are signal intensity time course data useful for differential diagnosis of enhancing lesions? Radiology 1999;211:101-10.
12. Goto M, Ito H, Akazawa K, et al. Diagnosis of breast tumors by contrast-enhanced MR imaging: comparison between the diagnostic performance of dynamic enhancement patterns and morphologic features. J Magn Reson Imaging 2007;25:104-12.
13. Narisada H, Aoki T, Sasaguri T, et al. Correlation between numeric gadolinium-enhanced dynamic MRI ratios and prognostic factors and histologic type of breast carcinoma. AJR Am J Roentgenol 2006;187: 297-306.
14. Takeda Y, Yoshikawa K. Contrast-enhanced dynamic MR imaging parameters and histological types of invasive ductal carcinoma of breast. Biomed Pharmacother 2005;59:115-21.
15. Jackson A, Haroon H, Zhu XP, et al. Breath-hold perfusion and permeability mapping of hepatic malignancies using magnetic resonance imaging and a first-pass leakage profile model. NMR Biomed 2002;15: 164-73.
16. Aronen HJ, Glass J, Pardo FS, et al. Echo-planar MR cerebral blood volume mapping of gliomas. Clinical utility. Acta Radiol 1995;36:520-8.
17. Aronen HJ, Pardo FS, Kennedy DN, et al. High microvascular blood volume is associated with high glucose uptake and tumor angiogenesis in human gliomas. Clin Cancer Res 2000;6:2189-200.
18. Patankar TF, Haroon HA, Mills SJ, et al. Is volume transfer coefficient (Ktrans) related to histologic grade in human gliomas? AJNR Am J Neuroradiol 2005;26: 2455-65.
19. Knopp EA, Cha S, Johnson G, et al. Glial neoplasms: dynamic contrast-enhanced T2*-weighted MR imaging. Radiology 1999;211:791-8.
20. Mills SJ, Patankar TA, Haroon HA, et al. Do cerebral blood volume and contrast transfer coefficient predict prognosis in human glioma? AJNR Am J Neuroradiol 2006;27:853-8.
21. 1-weighted MR imaging-initial experience. Radiology 2004;233:709-15.
22. Bonnerot V, Charpentier A, Frouin F, et al. Factor analysis of dynamic magnetic resonance imaging in predicting the response of osteosarcoma to chemotherapy. Invest Radiol 1992;27:847-55.
23. Mayr NA, Yuh WT, Magnotta VA, et al. Tumor perfusion studies using fast magnetic resonance imaging technique in advanced cervical cancer: a new noninvasive predictive assay. Int J Radiat Oncol Biol Phys 1996;36:623-33.
24. Hillengass J, Wasser K, Delorme S, et al. Lumbar bone marrow microcirculation measurements from dynamic contrast-enhanced magnetic resonance imaging is a predictor of event-free survival in progressive multiple myeloma. Clin Cancer Res 2007;13:475-81.
25. Zahra MA, Hollingsworth KG, Sala E, Lomas DJ, Tan LT. Dynamic contrast-enhanced MRI as a predictor of tumour response to radiotherapy. Lancet Oncol 2007; 8:63-74.
26. Padhani AR, Husband JE. Dynamic contrast-enhanced MRI studies in oncology with an emphasis on quantification, validation and human studies. Clin Radiol 2001;56:607-20.
27. Akella NS, Twieg DB, Mikkelsen T, et al. Assessment of brain tumor angiogenesis inhibitors using perfusion magnetic resonance imaging: quality and analysis results of a phase I trial. J Magn Reson Imaging 2004; 20:913-22.
28. Batchelor TT, Sorensen AG, di Tomaso E, et al. AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 2007;11:83-95.
29. Conrad C, Friedman H, Reardon D, et al. A phase I/II trial of single-agent PTK 787/ZK 222584 (PTK/ZK), a novel, oral angiogenesis inhibitor, in patients with recurrent glioblastoma multiforme (GBM). J Clin Oncol (Meet Abstr) 2004;22:1512.
30. Drevs J, Medinger M, Mross K, et al. Phase I clinical evaluation of AZD2171, a highly potent VEGF receptor tyrosine kinase inhibitor, in patients with advanced tumors. J Clin Oncol (Meet Abstr) 2005;23:3002.
31. Eder JP, Jr., Supko JG, Clark JW, et al. Phase I clinical trial of recombinant human endostatin administered as a short intravenous infusion repeated daily. J Clin Oncol 2002;20:3772-84.
32. Jayson GC, Parker GJ, Mullamitha S, et al. Blockade of platelet-derived growth factor receptor-β by CDP860, a humanized, PEGylated di-Fab′, leads to fluid accumulation and is associated with increased tumor vascularized volume. J Clin Oncol 2005;23: 973-81.
33. Jayson GC, Zweit J, Jackson A, et al. Molecular imaging and biological evaluation of HuMV833 anti-VEGF antibody: implications for trial design of antiangiogenic antibodies. J Natl Cancer Inst 2002;94: 1484-93.
34. Liu G, Rugo HS, Wilding G, et al. Dynamic contrast-enhanced magnetic resonance imaging as a pharmacodynamic measure of response after acute dosing of AG-013736, an oral angiogenesis inhibitor, in patients with advanced solid tumors: results from a phase I study. J Clin Oncol 2005;23:5464-73.
35. Medved M, Karczmar G, Yang C, et al. Semiquantitative analysis of dynamic contrast enhanced MRI in cancer patients: variability and changes in tumor tissue over time. J Magn Reson Imaging 2004;20: 122-8.
36. Morgan B, Thomas AL, Drevs J, et al. Dynamic contrast-enhanced magnetic resonance imaging as a biomarker for the pharmacological response of PTK787/ZK 222584, an inhibitor of the vascular endothelial growth factor receptor tyrosine kinases, in patients with advanced colorectal cancer and liver metastases: results from two phase I studies. J Clin Oncol 2003;21:3955-64.
37. Mross K, Drevs J, Muller M, et al. Phase I clinical and pharmacokinetic study of PTK/ZK, a multiple VEGF receptor inhibitor, in patients with liver metastases from solid tumours. Eur J Cancer 2005;41:1291-9.
38. Mross K, Scheulen M, Frost A, et al. Phase I study of BAY 57-9352, a VEGFR-2 inhibitor, in cycles of 14 days on/7 days off in patients with advanced solid tumors. J Clin Oncol (Meet Abstr) 2006;24:3089.
39. Mross KB, Gmehling D, Frost A, et al. A clinical Phase I, pharmacokinetic (PK), and pharmacodynamic study of twice daily BIBF 1120 in advanced cancer patients. J Clin Oncol (Meet Abstr) 2005;23:3031.
40. Mullamitha SA, Ton NC, Parker GJ, et al. Phase I evaluation of a fully human anti-{α}v integrin monoclonal antibody (CNTO 95) in patients with advanced solid tumors. Clin Cancer Res 2007;13:2128-35.
41. O'Donnell A, Padhani A, Hayes C, et al. A Phase I study of the angiogenesis inhibitor SU5416 (semaxanib) in solid tumours, incorporating dynamic contrast MR pharmacodynamic end points. Br J Cancer 2005; 93:876-83.
42. O'Dwyer PJ, Rosen M, Gallagher M, Schwartz B, Flaherty KT. Pharmacodynamic study of BAY 43-9006 in patients with metastatic renal cell carcinoma. J Clin Oncol (Meet Abstr) 2005;23:3005.
43. Overmoyer B, Silverman P, Leeming R, et al. Phase II trial of neoadjuvant docetaxel with or without bevacizumab in patients with locally advanced breast cancer. J Clin Oncol 2004;22:727.
44. Padhani AR, Taylor NJ, d'Arcy JA, et al. Dynamic MRI evaluation of the triple receptor tyrosine kinase inhibitor BIBF 1120 in patients with advanced solid tumours. Proc Intl Soc Magn Res on Med 2006;14:765.
45. Rosen LS, Kurzrock R, Jackson E, et al. Safety and pharmacokinetics of AMG 706 in patients with advanced solid tumors. J Clin Oncol (Meet Abstr) 2005;23:3013.
46. Rosen LS, Wilding G, Sweeney C, et al. Phase Idose escalation study to determine the safety, pharmacokinetics and pharmacodynamics of BMS-582664, a VEGFR/FGFR inhibitor in patients with advanced/ metastatic solid tumors. J Clin Oncol (Meet Abstr) 2006;24:3051.
47. Thomas AL, Morgan B, Horsfield MA, et al. Phase I study of the safety, tolerability, pharmacokinetics, and pharmacodynamics of PTK787/ZK 222584 administered twice daily in patients with advanced cancer. J Clin Oncol 2005;23:4162-71.
48. Thomas JP, Arzoomanian RZ, Alberti D, et al. Phase I pharmacokinetic and pharmacodynamic study of recombinant human endostatin in patients with advanced solid tumors. J Clin Oncol 2003;21:223-31.
49. Wedam SB, Low JA, Yang SX, et al. Antiangiogenic and antitumor effects of bevacizumab in patients with inflammatory and locally advanced breast cancer. J Clin Oncol 2006;24:769-77.
50. Xiong HQ, Herbst R, Faria SC, et al. A phase I surrogate endpoint study of SU6668 in patients with solid tumors. Invest New Drugs 2004;22:459-66.
51. Dowlati A, Robertson K, Cooney M, et al. A phase I pharmacokinetic and translational study of the novel vascular targeting agent combretastatin a-4 phosphate on a single-dose intravenous schedule in patients with advanced cancer. Cancer Res 2002;62: 3408-16.
52. Evelhoch JL, LoRusso PM, He Z, et al. Magnetic resonance imaging measurements of the response of murine and human tumors to the vascular-targeting agent ZD6126. Clin Cancer Res 2004;10:3650-7.
53. Galbraith SM, Maxwell RJ, Lodge MA, et al. Combretastatin A4 phosphate has tumor antivascular activity in rat and man as demonstrated by dynamic magnetic resonance imaging. J Clin Oncol 2003;21: 2831-42.
54. Galbraith SM, Rustin GJ, Lodge MA, et al. Effects of 5,6- dimethylxanthenone-4-acetic acid on human tumor microcirculation assessed by dynamic contrast-enhanced magnetic resonance imaging. J Clin Oncol 2002;20:3826-40.
55. McKeage MJ, Fong P, Jeffery M, et al. 5,6-Dimethylxanthenone-4-acetic acid in the treatment of refractory tumors: a phase I safety study of a vascular disrupting agent. Clin Cancer Res 2006;12:1776-84.
56. Stevenson JP, Rosen M, Sun W, et al. Phase I trial of the antivascular agent combretastatin A4 phosphate on a 5-day schedule to patients with cancer: magnetic resonance imaging evidence for altered tumor blood flow. J Clin Oncol 2003;21:4428-38.
57. O'Connor JP, Jackson A, Parker GJ, Jayson GC. DCE-MRI biomarkers in the clinical evaluation of antiangiogenic and vascular disrupting agents. Br J Cancer 2007;96:189-95.
58. Galbraith SM, Lodge MA, Taylor NJ, et al. Reproducibility of dynamic contrast-enhanced MRI in human muscle and tumours: comparison of quantitative and semi-quantitative analysis. NMR Biomed 2002; 15:132-42.
59. Padhani AR, Hayes C, Landau S, Leach MO. Reproducibility of quantitative dynamic MRI of normal human tissues. NMR Biomed 2002;15:143-53.
60. Thomas AL, Morgan B, Drevs J, et al. Vascular endothelial growth factor receptor tyrosine kinase inhibitors: PTK787/ZK 222584. Semin Oncol 2003;30: 32-8.
61. Hecht J, Trarbach T, Jaeger E, et al. A randomized, double-blind, placebo-controlled, phase III study in patients (Pts) with metastatic adenocarcinoma of the colon or rectum receiving first-line chemotherapy with oxaliplatin/5-fluorouracil/leucovorin and PTK787/ZK 222584 or placebo (CONFIRM-1). J Clin Oncol (Meet Abstr) 2005;23:3.
62. Buckley DL. Uncertainty in the analysis of tracer kinetics using dynamic contrast-enhanced T1-weighted MRI. Magn Reson Med 2002;47:601-6.
63. Jayson GC, Waterton JC. Applications of dynamic contrast-enhanced MRI in oncology drug development. In: Jackson A, Buckley DL, Parker GJM, editors. Dynamic contrast-enhanced magnetic resonance imaging in oncology. Berlin: Springer 2005; p. 281-97.
64. Buckley DL, Drew PJ, Mussurakis S, Monson JR, Horsman A. Microvessel density of invasive breast cancer assessed by dynamic Gd-DTPA enhanced MRI. J Magn Reson Imaging 1997;7:461-4.
65. Stomper PC, Winston JS, Herman S, et al. Angiogenesis and dynamic MR imaging gadolinium enhancement of malignant and benign breast lesions. Breast Cancer Res Treat 1997;45:39-46.
66. Hulka CA, Edmister WB, Smith BL, et al. Dynamic echo-planar imaging of the breast: experience in diagnosing breast carcinoma and correlation with tumor angiogenesis. Radiology 1997;205:837-42.
67. Mayr NA, Yuh WT, Zheng J, et al. Prediction of tumor control in patients with cervical cancer: analysis of combined volume and dynamic enhancement pattern by MR imaging. AJR Am J Roentgenol 1998;170: 177-82.
68. Hawighorst H, Knapstein PG, Knopp MV, et al. Uterine cervical carcinoma: comparison of standard and pharmacokinetic analysis of time-intensity curves for assessment of tumor angiogenesis and patient survival. Cancer Res 1998;58:3598-602.
69. Heppner GH. Tumor heterogeneity. Cancer Res 1984;44:2259-65.
70. Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature 2000;407:249-57.
71. Gillies RJ, Schornack PA, Secomb TW, Raghunand N. Causes and effects of heterogeneous perfusion in tumors. Neoplasia 1999;1:197-207.
72. Kumar R, Kuniyasu H, Bucana CD, Wilson MR, Fidler IJ. Spatial and temporal expression of angiogenic molecules during tumor growth and progression. Oncol Res 1998;10:301-11.
73. Casanovas O, Hicklin DJ, Bergers G, Hanahan D. Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell 2005;8:299-309.
74. Parker GJ, Suckling J, Tanner SF, et al. Probing tumor microvascularity by measurement, analysis and display of contrast agent uptake kinetics. J Magn Reson Imaging 1997;7:564-74.
75. Buonaccorsi GA, Roberts C, Cheung S, et al. Comparison of the performance of tracer kinetic model-driven registration for dynamic contrast enhanced MRI using different models of contrast enhancement. Acad Radiol 2006;13:1112-23.
76. Li KL, Jackson A. New hybrid technique for accurate and reproducible quantitation of dynamic contrast-enhanced MRI data. Magn Reson Med 2003;50: 1286-95.
77. Walker-Samuel S, Taylor NJ, Padhani AR, Leach MO, Collins DJ. The effect of heterogeneous tumour enhancement on the assessment of response to treatment. Proc Intl Soc Magn Reson Med 2006;14:761.
78. Issa B, Buckley DL, Turnbull LW. Heterogeneity analysis of Gd-DTPA uptake: improvement in breast lesion differentiation. J Comput Assist Tomogr 1999; 23:615-21.
79. Jackson A, Kassner A, Annesley-Williams D, et al. Abnormalities in the recirculation phase of contrast agent bolus passage in cerebral gliomas: comparison with relative blood volume and tumor grade. AJNR Am J Neuroradiol 2002;23:7-14.
80. Chang YC, Huang CS, Liu YJ, et al. Angiogenic response of locally advanced breast cancer to neoadjuvant chemotherapy evaluated with parametric histogram from dynamic contrast-enhanced MRI. Phys Med Biol 2004;49:3593-602.
81. Hayes C, Padhani AR, Leach MO. Assessing changes in tumour vascular function using dynamic contrast-enhanced magnetic resonance imaging. NMR Biomed 2002;15:154-63.
82. de Lussanet QG, Backes WH, Griffioen AW, et al. Dynamic contrast-enhanced magnetic resonance imaging of radiation therapy-induced microcirculation changes in rectal cancer. Int J Radiat Oncol Biol Phys 2005;63:1309-15.
83. Mayr NA, Yuh WT, Arnholt JC, et al. Pixel analysis of MR perfusion imaging in predicting radiation therapy outcome in cervical cancer. J Magn Reson Imaging 2000;12:1027-33.
84. Jordan BF, Runquist M, Raghunand N, et al. The thioredoxin-1 inhibitor 1-methylpropyl 2-imidazolyl disulfide (PX-12) decreases vascular permeability in tumor xenografts monitored by dynamic contrast enhanced magnetic resonance imaging. Clin Cancer Res 2005;11:529-36.
85. Crokart N, Radermacher K, Jordan BF, et al. Tumor radiosensitization by antiinflammatory drugs: evidence for a new mechanism involving the oxygen effect. Cancer Res 2005;65:7911-6.
86. Checkley D, Tessier JJ, Kendrew J, Waterton JC, Wedge SR. Use of dynamic contrast-enhanced MRI to evaluate acute treatment with ZD6474, a VEGF signalling inhibitor, in PC-3 prostate tumours. Br J Cancer 2003;89:1889-95.
87. O'Connor EL, Fieller N, Holmes A, Waterton J. How to analyse dynamic MRI in oncology; advanced histogram analysis gives better statistical power & insight than simple averaging. Proc Intl Soc Magn Reson Med 2005;13:2101.
88. Li KL, Wilmes LJ, Henry RG, et al. Heterogeneity in the angiogenic response of a BT474 human breast cancer to a novel vascular endothelial growth factor-receptor tyrosine kinase inhibitor: assessment by voxel analysis of dynamic contrast-enhanced MRI. J Magn Reson Imaging 2005;22:511-9.
89. Watson Y, Cheung S, Roberts C, et al. Prognostic power of DCE-MRI heterogeneity analysis in patients with advanced solid tumors. Proc Intl Soc Magn Reson Med 2006;14:755.
90. Emblem KE, Nedregaard B, Due-Tonnessen P, et al. Characterization of intra-axial neoplasms by histogram analysis of total tumor volume from MR-derived cerebral blood volume maps. Proc Int Soc Magn Reson Med 2006;14:823.
91. Young RJ, Pollack E, Lu H, et al. Region-of-interest analysis vs. non-region-of-interest histogram analysis in the evaluation of cerebral gliomas. Proc Int Soc Magn Reson Med 2006;14:3158.
92. Tofts PS, Benton CE, Weil RS, et al. Quantitative analysis of whole-tumor Gd enhancement histograms predicts malignant transformation in low-grade gliomas. J Magn Reson Imaging 2007;25:208-14.
93. Dzik-Jurasz A, Walker-Samuel S, Leach MO, et al. Fractal parameters derived from analysis of DCE-MRI data correlates with response to therapy in rectal carcinoma. Proc Int Soc Magn Reson Med 2004;2:2503.
94. Rose CJ, Buonaccorsi GA, Cheung S, et al. Fractal properties of tumours in dynamic contrast enhanced magnetic resonance imaging. Proc Int Soc Reson Med. 2007;15:2821.
95. Jackson A. Analysis of dynamic contrast enhanced MRI. Br J Radiol 2004;77 Spec No 2:S154-66.
96. Barbier EL, Lamalle L, Decorps M. Methodology of brain perfusion imaging. J Magn Reson Imaging 2001; 13:496-520.
97. Weisskoff R, Boxerman J, Sorensen A, et al. Simultaneous blood volume and permeability mapping using a single Gd-based contrast injection. Proc Int Soc Magn Reson Med 1994;2:279.
98. Kassner A, Annesley DJ, Zhu XP, et al. Abnormalities of the contrast re-circulation phase in cerebral tumors demonstrated using dynamic susceptibility contrast-enhanced imaging: a possible marker of vascular tortuosity. J Magn Reson Imaging 2000;11: 103-13.
99. Rosen BR, Belliveau JW, Aronen HJ, et al. Susceptibility contrast imaging of cerebral blood volume: human experience. Magn Reson Med 1991;22:293-9.
100. 2O positron emission tomography in humans. J Cereb Blood Flow Metab 1998;18:935-40.
101. 2* contrast-enhanced dynamic MR imaging. J Magn Reson Imaging 2000;11:575-85.
102. 2, and chemical-shift imaging. Magn Reson Med 1990;13:77-89.
103. Evelhoch JL. Key factors in the acquisition of contrast kinetic data for oncology. J Magn Reson Imaging 1999;10:254-9.
104. Parker GJ, Roberts C, Macdonald A, et al. 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.
105. Li K, Zhu X, Waterton J, Jackson A. Improved 3D quantitative mapping of blood volume and endothelial permeability in brain tumours. J Magn Reson Imaging 2000;12:347-57.
106. Henderson E, Rutt BK, Lee TY. Temporal sampling requirements for the tracer kinetics modeling of breast disease. Magn Reson Imaging 1998;16:1057-73.
107. Weinmann HJ, Laniado M, Mutzel W. Pharmacokinetics of GdDTPA/dimeglumine after intravenous injection into healthy volunteers. Physiol Chem Phys Med NMR 1984;16:167-72.
108. Fritz-Hansen T, Rostrup E, Larsson HB, et al. Measurement of the arterial concentration of Gd-DTPA using MRI: a step toward quantitative perfusion imaging. Magn Reson Med 1996;36:225-31.
109. Tofts PS, Kermode AG. Measurement of the blood brain barrier permeability and leakage space using dynamic MR imaging: fundamental concepts. Magn Reson Med 1991;17:357-67.
110. Larsson HB, Stubgaard M, Frederiksen JL, et al. Quantitation of blood-brain barrier defect bymagnetic resonance imaging and gadolinium-DTPA in patients with multiple sclerosis and brain tumors. Magn Reson Med 1990;16:117-31.
111. trans measurements obtained with conventional and first pass pharmacokinetic models in human gliomas. J Magn Reson Imaging 2004;19: 527-36.
112. Tofts PS. Modeling tracer kinetics in dynamic Gd-DTPA MR imaging. J Magn Reson Imaging 1997;7: 91-101.
113. St Lawrence K, Lee T. An Adiabatic Approximation to the tissue homogeneity model for water exchange in the brain: i. theoretical derivation. J Cereb Blood Flow Metab 1998;18:1365-77.
114. Walker-Samuel S, Leach MO, Collins DJ. Evaluation of response to treatment using DCE-MRI: the relationship between initial area under the gadolinium curve (IAUGC) and quantitative pharmacokinetic analysis. Phys Med Biol 2006;51:3593-602.