Dynamic contrast-enhanced magnetic resonance imaging (DCE-MRI) in preclinical studies of antivascular treatments

Pharmaceutics

Volumn 4, Issue 4, 2012, Pages 563-589

  Nielsen, Thomas ^a   Wittenborn, Thomas ^a   Horsman, Michael R ^a  

^a AARHUS UNIVERSITY HOSPITAL   (Denmark)

Author keywords

Angiogenesis inhibitors; DCE MRI; Preclinical studies; Vascular disrupting agents

Indexed keywords

ANGIOGENESIS INHIBITOR; AXITINIB; BEVACIZUMAB; CEDIRANIB; COMBRETASTATIN A1 PHOSPHATE; COMBRETASTATIN A4 PHOSPHATE; EVEROLIMUS; FUMAGILLOL CHLOROACETYLCARBAMATE; GADOCOLETIC ACID; GADODIAMIDE; GADOLINIUM PENTETATE ALBUMIN; GADOLINIUM PENTETATE MEGLUMINE; GADOTERIDOL; IMATINIB; KR 31831; N [2 [(4 HYDROXYPHENYL)AMINO] 3 PYRIDINYL] 4 METHOXYBENZENESULFONAMIDE; N ACETYLCOLCHINOL PHOSPHATE; ORANTINIB; PLINABULIN; SOBLIDOTIN; SORAFENIB; STILBENE 5C; STILBENE 6C; STILBENE DERIVATIVE; SUNITINIB; THALIDOMIDE; UNCLASSIFIED DRUG; UNINDEXED DRUG; VANDETANIB; VASCULAR TARGETING AGENT; VATALANIB;

ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; BLOOD VESSEL PERMEABILITY; BREAST CANCER; BREAST CARCINOMA; BREAST TUMOR; CLINICAL PROTOCOL; CLINICAL RESEARCH; COLON ADENOCARCINOMA; COLON CARCINOMA; CONTRAST ENHANCEMENT; DOSE RESPONSE; DRUG DETERMINATION; DRUG EFFECT; DRUG EFFICACY; FIBROSARCOMA; GLIOBLASTOMA; GLIOMA; HUMAN; IN VIVO STUDY; KIDNEY CARCINOMA; LIVER SARCOMA; LUNG SMALL CELL CANCER; LYMPH NODE METASTASIS; LYMPHOMA; MELANOMA; MOLECULAR IMAGING; MOLECULAR WEIGHT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OPTIMAL DRUG DOSE; OVARY CANCER; OVARY CARCINOMA; PANCREAS CARCINOMA; PROCESS OPTIMIZATION; PROGNOSIS; PROLACTINOMA; PROSTATE CANCER; QUANTITATIVE ANALYSIS; REVIEW; RHABDOMYOSARCOMA; SINGLE DRUG DOSE; SQUAMOUS CELL CARCINOMA; STANDARDIZATION;

EID: 84871547926     PISSN: None     EISSN: 19994923     Source Type: Journal    
DOI: 10.3390/pharmaceutics4040563     Document Type: Review

References (152)

1. Brem, S.; Brem, H.; Folkman, J.; Finkelstein, D.; Patz, A. Prolonged tumor dormancy by prevention of neovascularization in the vitreous. Cancer Res. 1976, 8, 2807-2812.
2. Folkman, J. How is blood vessel growth regulated in normal and neoplastic tissue? G.H.A. Clowes memorial Award lecture. Cancer Res. 1986, 2, 467-473.
3. Hahnfeldt, P.; Panigrahy, D.; Folkman, J.; Hlatky, L. Tumor development under angiogenic signaling: A dynamical theory of tumor growth, treatment response, and postvascular dormancy. Cancer Res. 1999, 19, 4770-4775.
4. Bergers, G.; Benjamin, L.E. Tumorigenesis and the angiogenic switch. Nat. Rev. Cancer. 2003, 6, 401-410.
5. Vaupel, P.; Kallinowski, F.; Okunieff, P. Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: A review. Cancer Res. 1989, 23, 6449-6465.
6. Stoeltzing, O.; Ellis, L.M. The role of microvasculature in metastasis formation. In Vascular-Targeted Therapies in Oncology; Siemann, D.W., Ed.; John Wiley & Sons, Ltd.: Chichester, UK, 2006; pp. 31-62.
7. Vaupel, P. Tumor microenvironmental physiology and its implications for radiation oncology. Semin. Radiat. Oncol. 2004, 3, 198-206.
8. Harris, A.L. Hypoxia-A key regulatory factor in tumour growth. Nat. Rev. Cancer. 2002, 1, 38-47.
9. Siemann, D.W.; Bibby, M.C.; Dark, G.G.; Dicker, A.P.; Eskens, F.A.L.M.; Horsman, M.R.; Marmé, D.; Lorusso, P.M. Differentiation and definition of vascular-targeted therapies. Clin. Cancer Res. 2005, 2, 416-420.
10. Horsman, M.R.; Siemann, D.W. Pathophysiologic effects of vascular-targeting agents and the implications for combination with conventional therapies. Cancer Res. 2006, 24, 11520-11539.
11. Ferrara, N.; Gerber, H.P.; Le Couter, J. The biology of VEGF and its receptors. Nat. Med. 2003, 6, 669-676.
12. Pugh, C.W.; Ratcliffe, P.J. Regulation of angiogenesis by hypoxia: role of the HIF system. Nat. Med. 2003, 6, 677-684.
13. Kerbel, R.; Folkman, J. Clinical translation of angiogenesis inhibitors. Nat Rev Cancer 2002, 10, 727-739.
14. Marme, D. The impact of anti-angiogenic agents on cancer therapy. J. Cancer Res. Clin. Oncol. 2003, 11, 607-620.
15. Eskens, F.A. Angiogenesis inhibitors in clinical development; Where are we now and where are we going? Br. J. Cancer 2004, 1, 1-7.
16. Ferrara, N.; Kerbel, R.S. Angiogenesis as a therapeutic target. Nature 2005, 7070, 967-974.
17. Heath, V.L.; Bicknell, R. Anticancer strategies involving the vasculature. Nat. Rev. Clin. Oncol. 2009, 7, 395-404.
18. National Cancer Institute. Available online: www.cancer.gov/clinicaltrials (accessed on 1 May 2012).
19. Horsman, M.R.; Overgaard, J. Thermal radiosensitization in animal tumors: the potential for therapeutic gain. In Hyperthermia and Oncology; Urano, M., Douple, E., Eds.; VSP: Utrecht, The Netherland, 1985; Vol. 2, pp. 113-145.
20. Chaplin, D.J.; Dougherty, G.J. Tumour vasculature as a target for cancer therapy. Br. J. Cancer 1999, 80, 57-64.
21. Thorpe, P.E. Vascular targeting agents as cancer therapeutics. Clin. Cancer Res. 2004, 2, 415-427.
22. Siemann, D.W.; Chaplin, D.J.; Horsman, M.R. Vascular-targeting therapies for treatment of malignant disease. Cancer 2004, 12, 2491-2499.
23. Baguley, B.C. Antivascular therapy of cancer: DMXAA. Lancet Oncol. 2003, 3, 141-148.
24. Tozer, G.M.; Kanthou, C.; Baguley, B.C. Disrupting tumour blood vessels. Nat. Rev. Cancer 2005, 6, 423-435.
25. Weidner, N.; Semple, J.P.; Welch, W.R.; Folkman, J. Tumor angiogenesis and metastasis-Correlation in invasive breast carcinoma. N. Engl. J. Med. 1991, 1, 1-8.
26. Borre, M.; Offersen, B.V.; Nerstrøm, B.; Overgaard, J. Microvessel density predicts survival in prostate cancer patients subjected to watchful waiting. Br. J. Cancer 1998, 7, 940-944.
27. Hansen, S.; Grabau, D.A.; Sørensen, F.B.; Bak, M.; Rose, W.V.A.C. The prognostic value of angiogenesis by Chalkley counting in a confirmatory study design on 836 breast cancer patients. Clin. Cancer Res. 2000, 1, 139-146.
28. Borre, M.; Nerstrøm, B.; Overgaard, J. Association between immunohistochemical expression of vascular endothelial growth factor (VEGF), VEGF-expressing neuroendocrine-differentiated tumor cells, and outcome in prostate cancer patients subjected to watchful waiting. Clin. Cancer Res. 2000, 5, 1882-1890.
29. Gasparini, G. Clinical significance of determination of surrogate markers of angiogenesis in breast cancer. Crit. Rev. Oncol. 2001, 2, 97-114.
30. Robinson, S.P.; Rijken, P.F.J.W.; Howe, F.A.; McSheehy, P.M.J.; van der Sanden, B.P.J.; Heerschap, A.; Stubbs, M.; van der Kogel, A.J.; Griffiths, J.R. Tumor vascular architecture and function evaluated by non-invasive susceptibility MRI methods and immunohistochemistry. J. Magn. Reson. Imaging 2003, 4, 445-454.
31. Garcia-Barros, M.; Paris, F.; Cordon-Cardo, C.; Lyden, D.; Rafii, S.; Haimovitz-Friedman, A.; Fuks, Z.; Kolesnick, R. Tumor response to radiotherapy regulated by endothelial cell apoptosis. Science 2003, 5622, 1155-1159.
32. Horsman, M.R.; Nielsen, T.; Østergaard, L.; Overgaard, J. Radiation administered as a large single dose or in a fractionated schedule: Role of the tumour vasculature as a target for influencing response. Acta Oncol. 2006, 7, 876-880.
33. Miller, J.C.; Pien, H.H.; Sahani, D.; Sorensen, A.G.; Thrall, J.H. Imaging angiogenesis: Applications and potential for drug development. J. Natl. Cancer Inst. 2005, 3, 172-187.
34. Lassau, N.; Chebil, M.; Chami, L.; Bidault, S.; Girard, E.; Roche, A. Dynamic contrast-enhanced ultrasonography (DCE-US): A new tool for the early evaluation of antiangiogenic treatment. Target Oncol. 2010, 1, 53-58.
35. Mason, R.P.; Zhao, D.; Liu, L.; Trawick, M.L.; Pinney, K.G. A perspective on vascular disrupting agents that interact with tubulin: preclinical tumor imaging and biological assessment. Integr. Biol. (Camb) 2011, 4, 375-387.
36. Tai, J.H.; Tessier, J.; Ryan, A.J.; Hoffman, L.; Chen, X.; Lee, T.Y. Assessment of acute antivascular effects of vandetanib with high-resolution dynamic contrast-enhanced computed tomographic imaging in a human colon tumor xenograft model in the nude rat. Neoplasia 2010, 9, 697-707.
37. Anderson, H.L.; Yap, J.T.; Miller, M.P.; Robbins, A.; Jones, T.; Price, P.M. Assessment of pharmacodynamic vascular response in a phase I trial of combretastatin A4 phosphate. J. Clin. Oncol. 2003, 15, 2823-2830.
38. Leach, M.O.; Brindle, K.M.; Evelhoch, J.L.; Griffiths, J.R.; Horsman, M.R.; Jackson, A.; Jayson, G.C.; Judson, I.R.; Knopp, M.V.; Maxwell, R.J.; et al. Pharmacodynamic/Pharmacokinetic Technologies Advisory Committee, Drug Development Office, Cancer Research UK The assessment of antiangiogenic and antivascular therapies in early-stage clinical trials using magnetic resonance imaging: issues and recommendations. Br. J. Cancer 2005, 9, 1599-1610.
39. Petersen, E.T.; Zimine, I.; Ho, Y.C.; Golay, X. Non-invasive measurement of perfusion: A critical review of arterial spin labelling techniques. Br. J. Radiol. 2006, 944, 688-701.
40. Jarnum, H.; Steffensen, E.G.; Knutsson, L.; Frund, E.T.; Simonsen, C.W.; Lundbye-Christensen, S.; Shankaranarayanan, A.; Alsop, D.C.; Jensen, F.T.; Larsson, E.M. Perfusion MRI of brain tumours: A comparative study of pseudo-continuous arterial spin labelling and dynamic susceptibility contrast imaging. Neuroradiology 2010, 4, 307-317.
41. Van Westen, D.; Petersen, E.T.; Wirestam, R.; Siemund, R.; Bloch, K.M.; Stahlberg, F.; Bjorkman-Burtscher, I.M.; Knutsson, L. Correlation between arterial blood volume obtained by arterial spin labelling and cerebral blood volume in intracranial tumours. Magma Magn. Reson. Mater. Phy. Biol. Med. 2011, 4, 211-223.
42. Østergaard, L.; Weisskoff, R.M.; Chesler, D.A.; Gyldensted, C.; Rosen, B.R. High resolution measurement of cerebral blood flow using intravascular tracer bolus passages. Part I: Mathematical approach and statistical analysis. Magn. Reson. Med. 1996, 5, 715-725.
43. Østergaard, L.; Sørensen, A.G.; Kwong, K.K.; Gyldensted, R.M. W. a. C.; Rosen, B.R. High resolution measurement of cerebral blood flow using intravascular tracer bolus passages. Part II: Experimental comparison and preliminary results. Magn. Reson. Med. 1996, 5, 726-736.
44. Kiselev, V.G.; Strecker, R.; Ziyeh, S.; Speck, O.; Hennig, J. Vessel size imaging in humans. Magn. Reson. Med. 2005, 3, 553-563.
45. Dennie, J.; Mandeville, J.B.; Boxerman, J.L.; Packard, S.D.; Rosen, B.R.; Weisskoff, R.M. NMR imaging of changes in vascular morphology due to tumor angiogenesis. Magn. Reson. Med. 1998, 6, 793-799.
46. Troprès, I.; Grimault, S.; Vaeth, A.; Grillon, E.; Julien, C.; Payen, J.F.; Lamalle, L.; Décorps, M. Vessel size imaging. Magn. Reson. Med. 2001, 3, 397-408.
47. Zahra, M.A.; Hollingsworth, K.G.; Sala, E.; Lomas, D.J.; Tan, L.T. Dynamic contrast-enhanced MRI as a predictor of tumour response to radiotherapy. Lancet Oncol 2007, 1, 63-74.
48. Gadian, D.G.; Payne, J.A.; Bryant, D.J.; Young, I.R.; Carr, D.H.; Bydder, G.M. Gadolinium-DTPA as a contrast agent in MR imaging-Theoretical projections and practical observations. J. Comput. Assist. Tomogr. 1985, 2, 242-251.
49. Grossman, R.I.; Gonzalez-Scarano, F.; Atlas, S.W.; Galetta, S.; Silberberg, D.H. Multiple sclerosis: Gadolinium enhancement in MR imaging. Radiology 1986, 3, 721-725.
50. Miller, D.H.; Rudge, P.; Johnson, G.; Kendall, B.E.; Macmanus, D.G.; Moseley, I.F.; Barnes, D.; McDonald, W.I. Serial gadolinium enhanced magnetic resonance imaging in multiple sclerosis. Brain 1988, Pt 4, 927-939.
51. Pradel, C.; Siauve, N.; Bruneteau, G.; Clement, O.; de Bazelaire, C.; Frouin, F.; Wedge, S.R.; Tessier, J.L.; Robert, P.H.; Frija, G.; et al. Reduced capillary perfusion and permeability in human tumour xenografts treated with the VEGF signalling inhibitor ZD4190: An in vivo assessment using dynamic MR imaging and macromolecular contrast media. Magn. Reson. Imaging 2003, 8, 845-851.
52. De Bazelaire, C.; Siauve, N.; Fournier, L.; Frouin, F.; Robert, P.; Clement, O.; de Kerviler, E.; Cuenod, C.A. Comprehensive model for simultaneous MRI determination of perfusion and permeability using a blood-pool agent in rats rhabdomyosarcoma. Eur. Radiol. 2005, 12, 2497-2505.
53. Sourbron, S.P.; Buckley, D.L. Tracer kinetic modelling in MRI: Estimating perfusion and capillary permeability. Phys. Med. Biol. 2012, 2, R1-R33.
54. Evelhoch, J.L. Key factors in the acquisition of contrast kinetic data for oncology. J. Magn. Reson. Imaging 1999, 3, 254-259.
55. Kety, S.S. The theory and applications of the exchange of inert gas at the lungs and tissues. Pharmacol. Rev. 1951, 3, 1-41.
56. Renkin, E.M. Transport of potassium-42 from blood to tissue in isolated mammalian skeletal muscles. Am. J. Physiol. 1959, 197, 1205-1210.
57. Crone, C. The permeability of capillaries in various organs as determined by use of the "indicator diffusion" method. Acta Physiol. Scand. 1963, 58, 292-305.
58. Patlak, C.S.; Fenstermacher, J.D. Measurements of dog blood-brain transfer constants by ventriculocisternal perfusion. Am. J. Physiol. 1975, 4, 877-884.
59. Tofts, P.S. Modeling tracer kinetics in dynamic Gd-DTPA MR imaging. J. Magn. Reson. Imaging 1997, 1, 91-101.
60. 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, 2, 357-367.
61. Larsson, H.B.; Stubgaard, M.; Frederiksen, J.L.; Jensen, M.; Henriksen, O.; Paulson, O.B. 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, 1, 117-131.
62. Brix, G.; Semmler, W.; Port, R.; Schad, L.R.; Layer, G.; Lorenz, W.J. Pharmacokinetic parameters in CNS Gd-DTPA enhanced MR imaging. J. Comput. Assist. Tomogr. 1991, 4, 621-628.
63. Ewing, J.R.; Knight, R.A.; Nagaraja, T.N.; Yee, J.S.; Nagesh, V.; Whitton, P.A.; Li, L.; Fenstermacher, J.D. 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, 2, 283-292.
64. Tofts, P.S.; Brix, G.; Buckley, D.L.; Evelhoch, J.L.; Henderson, E.; Knopp, M.V.; Larsson, H.B.; Lee, T.Y.; Mayr, N.A.; Parker, G.J.; 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, 3, 223-232.
65. Patlak, C.S.; Blasberg, R.G. Graphical evaluation of blood-to-brain transfer constants from multiple-time uptake data. Generalizations. J. Cereb. Blood Flow Metab. 1985, 4, 584-590.
66. Ewing, J.R.; Brown, S.L.; Lu, M.; Panda, S.; Ding, G.; Knight, R.A.; Cao, Y.; Jiang, Q.; Nagaraja, T.N.; Churchman, J.L.; et al. Model selection in magnetic resonance imaging measurements of vascular permeability: Gadomer in a 9L model of rat cerebral tumor. J. Cereb. Blood Flow Metab. 2006, 3, 310-320.
67. Roberts, T. Technical and practical considerations for permeability modeling of dynamic contrast enhanced MRI. Acad. Radiol. 2005, S34-S37.
68. Weinmann, H.J.; Laniado, M.; Mützel, W. Pharmacokinetics of GdDTPA/dimeglumine after intravenous injection into healthy volunteers. Physiol. Chem. Phys. Med. NMR 1984, 2, 167-172.
69. Wedeking, P.; Eaton, S.; Covell, D.G.; Nair, S.; Tweedle, M.F.; Eckelman, W.C. Pharmacokinetic analysis of blood distribution of intravenously administered 153Gd-labeled Gd(DTPA)2- and 99mTc(DTPA) in rats. Magn. Reson. Imaging 1990, 5, 567-575.
70. Maxwell, R.J.; Wilson, J.; Prise, V.E.; Vojnovic, B.; Rustin, G.J.; Lodge, M.A.; Tozer, G.M. Evaluation of the anti-vascular effects of combretastatin in rodent tumours by dynamic contrast enhanced MRI. NMR Biomed. 2002, 2, 89-98.
71. Furman-Haran, E.; Grobgeld, D.; Degani, H. Dynamic contrast-enhanced imaging and analysis at high spatial resolution of MCF7 human breast tumors. J. Magn. Reson. 1997, 2, 161-171.
72. Yang, C.; Karczmar, G.S.; Medved, M.; Stadler, W.M. Estimating the arterial input function using two reference tissues in dynamic contrast-enhanced MRI studies: Fundamental concepts and simulations. Magn. Reson. Med. 2004, 5, 1110-1117.
73. Yankeelov, T.E.; Luci, J.J.; Lepage, M.; Li, R.; Debusk, L.; Lin, P.C.; Price, R.R.; Gore, J.C. Quantitative pharmacokinetic analysis of DCE-MRI data without an arterial input function: A reference region model. Magn. Reson. Imaging 2005, 4, 519-529.
74. Turetschek, K.; Preda, A.; Novikov, V.; Brasch, R.C.; Weinmann, H.J.; Wunderbaldinger, P.; Roberts, T.P. Tumor microvascular changes in antiangiogenic treatment: Assessment by magnetic resonance contrast media of different molecular weights. J. Magn. Reson. Imaging 2004, 1, 138-144.
75. Brasch, R.; Turetschek, K. MRI characterization of tumors and grading angiogenesis using macromolecular contrast media: status report. Eur. J. Radiol. 2000, 3, 148-155.
76. Daldrup-Link, H.E.; Kaiser, A.; Helbich, T.; Werner, M.; Bjørnerud, A.; Link, T.M.; Rummeny, E.J. Macromolecular contrast medium (feruglose) versus small molecular contrast medium (gadopentetate) enhanced magnetic resonance imaging: differentiation of benign and malignant breast lesions. Acad. Radiol. 2003, 11, 1237-1246.
77. Bentzen, L.; Vestergaard-Poulsen, P.; Nielsen, T.; Overgaard, J.; Bjørnerud, A.; Briley-Saebø, K.; Horsman, M.R.; Ostergaard, L. Intravascular contrast agent-enhanced MRI measuring contrast clearance and tumor blood volume and the effects of vascular modifiers in an experimental tumor. Int. J. Radiat. Oncol. Biol. Phys. 2005, 4, 1208-1215.
78. Brasch, R.; Pham, C.; Shames, D.; Roberts, T.; van Dijke, K.; van Bruggen, N.; Mann, J.; Ostrowitzki, S.; Melnyk, O. Assessing tumor angiogenesis using macromolecular MR imaging contrast media. J. Magn. Reson. Imaging 1997, 1, 68-74.
79. Pham, C.D.; Roberts, T.P.; Bruggen, N. v.; Melnyk, O.; Mann, J.; Ferrara, N.; Cohen, R.L.; Brasch, R.C. Magnetic resonance imaging detects suppression of tumor vascular permeability after administration of antibody to vascular endothelial growth factor. Cancer Invest. 1998, 4, 225-230.
80. Gossmann, A.; Helbich, T.H.; Mesiano, S.; Shames, D.M.; Wendland, M.F.; Roberts, T.P.; Ferrara, N.; Jaffe, R.B.; Brasch, R.C. Magnetic resonance imaging in an experimental model of human ovarian cancer demonstrating altered microvascular permeability after inhibition of vascular endothelial growth factor. Am. J. Obstet. Gynecol. 2000, 4, 956-963.
81. Gossmann, A.; Helbich, T.H.; Kuriyama, N.; Ostrowitzki, S.; Roberts, T.P.; Shames, D.M.; van Bruggen, N.; Wendland, M.F.; Israel, M.A.; Brasch, R.C. Dynamic contrast-enhanced magnetic resonance imaging as a surrogate marker of tumor response to anti-angiogenic therapy in a xenograft model of glioblastoma multiforme. J. Magn. Reson. Imaging 2002, 3, 233-240.
82. Daldrup-Link, H.E.; Okuhata, Y.; Wolfe, A.; Srivastav, S.; Øie, S.; Ferrara, N.; Cohen, R.L.; Shames, D.M.; Brasch, R.C. Decrease in tumor apparent permeability-surface area product to a MRI macromolecular contrast medium following angiogenesis inhibition with correlations to cytotoxic drug accumulation. Microcirculation 2004, 5, 387-396.
83. Preda, A.; Novikov, V.; Moglich, M.; Turetschek, K.; Shames, D.M.; Brasch, R.C.; Cavagna, F.M.; Roberts, T.P. MRI monitoring of Avastin antiangiogenesis therapy using B22956/1, a new blood pool contrast agent, in an experimental model of human cancer. J. Magn. Reson. Imaging 2004, 5, 865-873.
84. Jahnke, K.; Muldoon, L.L.; Varallyay, C.G.; Lewin, S.J.; Kraemer, D.F.; Neuwelt, E.A. Bevacizumab and carboplatin increase survival and asymptomatic tumor volume in a glioma model. Neuro Oncol. 2009, 2, 142-150.
85. Bauerle, T.; Bartling, S.; Berger, M.; Schmitt-Graff, A.; Hilbig, H.; Kauczor, H.U.; Delorme, S.; Kiessling, F. Imaging anti-angiogenic treatment response with DCE-VCT, DCE-MRI and DWI in an animal model of breast cancer bone metastasis. Eur. J. Radiol. 2010, 2, 280-287.
86. Muldoon, L.L.; Gahramanov, S.; Li, X.; Marshall, D.J.; Kraemer, D.F.; Neuwelt, E.A. Dynamic magnetic resonance imaging assessment of vascular targeting agent effects in rat intracerebral tumor models. Neuro Oncol. 2011, 1, 51-60.
87. Keunen, O.; Johansson, M.; Oudin, A.; Sanzey, M.; Rahim, S.A.; Fack, F.; Thorsen, F.; Taxt, T.; Bartos, M.; Jirik, R.; et al. Anti-VEGF treatment reduces blood supply and increases tumor cell invasion in glioblastoma. Proc. Natl. Acad. Sci. USA 2011, 9, 3749-3754.
88. Fruth, K.; Weber, S.; Okcu, Y.; Noppens, R.; Klein, K.U.; Joest, E.; Hedrich, J.; Thilemann, S.; Pogorzelski, B.; Koutsimpelas, D.; et al. Increased basic fibroblast growth factor release and proliferation in xenotransplanted squamous cell carcinoma after combined irradiation/anti-vascular endothelial growth factor treatment. Oncol. Rep. 2012, 5, 1573-1579.
89. Kiessling, F.; Farhan, N.; Lichy, M.P.; Vosseler, S.; Heilmann, M.; Krix, M.; Bohlen, P.; Miller, D.W.; Mueller, M.M.; Semmler, W.; et al. Dynamic contrast-enhanced magnetic resonance imaging rapidly indicates vessel regression in human squamous cell carcinomas grown in nude mice caused by VEGF receptor 2 blockade with DC101. Neoplasia 2004, 3, 213-223.
90. Hoff, B.A.; Bhojani, M.S.; Rudge, J.; Chenevert, T.L.; Meyer, C.R.; Galban, S.; Johnson, T.D.; Leopold, J.S.; Rehemtulla, A.; Ross, B.D.; et al. DCE and DW-MRI monitoring of vascular disruption following VEGF-Trap treatment of a rat glioma model. NMR Biomed. 2012, 25, 935-942.
91. Turetschek, K.; Preda, A.; Floyd, E.; Shames, D.M.; Novikov, V.; Roberts, T.P.; Wood, J.M.; Fu, Y.; Carter, W.O.; Brasch, R.C. MRI monitoring of tumor response following angiogenesis inhibition in an experimental human breast cancer model. Eur. J. Nucl. Med. Mol. Imaging 2003, 3, 448-455.
92. Rudin, M.; McSheehy, P.M.; Allegrini, P.R.; Rausch, M.; Baumann, D.; Becquet, M.; Brecht, K.; Brueggen, J.; Ferretti, S.; Schaeffer, F.; et al. PTK787/ZK222584, a tyrosine kinase inhibitor of vascular endothelial growth factor receptor, reduces uptake of the contrast agent GdDOTA by murine orthotopic B16/BL6 melanoma tumours and inhibits their growth in vivo. NMR Biomed. 2005, 5, 308-321.
93. Ali, M.M.; Janic, B.; Babajani-Feremi, A.; Varma, N.R.; Iskander, A.S.; Anagli, J.; Arbab, A.S. Changes in vascular permeability and expression of different angiogenic factors following anti-angiogenic treatment in rat glioma. PLoS One 2010, 1, e8727.
94. Drevs, J.; Muller-Driver, R.; Wittig, C.; Fuxius, S.; Esser, N.; Hugenschmidt, H.; Konerding, M.A.; Allegrini, P.R.; Wood, J.; Hennig, J.; et al. PTK787/ZK 222584, a specific vascular endothelial growth factor-receptor tyrosine kinase inhibitor, affects the anatomy of the tumor vascular bed and the functional vascular properties as detected by dynamic enhanced magnetic resonance imaging. Cancer Res. 2002, 14, 4015-4022.
95. Marzola, P.; Degrassi, A.; Calderan, L.; Farace, P.; Nicolato, E.; Crescimanno, C.; Sandri, M.; Giusti, A.; Pesenti, E.; Terron, A.; et al. Early antiangiogenic activity of SU11248 evaluated in vivo by dynamic contrast-enhanced magnetic resonance imaging in an experimental model of colon carcinoma. Clin. Cancer Res. 2005, 16, 5827-5832.
96. Casneuf, V.F.; Delrue, L.; van Damme, N.; Demetter, P.; Robert, P.; Corot, C.; Duyck, P.; Ceelen, W.; Boterberg, T.; Peeters, M. Noninvasive monitoring of therapy-induced microvascular changes in a pancreatic cancer model using dynamic contrast-enhanced magnetic resonance imaging with P846, a new low-diffusible gadolinium-based contrast agent. Radiat. Res. 2011, 1, 10-20.
97. Marzola, P.; Degrassi, A.; Calderan, L.; Farace, P.; Crescimanno, C.; Nicolato, E.; Giusti, A.; Pesenti, E.; Terron, A.; Sbarbati, A.; et al. In vivo assessment of antiangiogenic activity of SU6668 in an experimental colon carcinoma model. Clin. Cancer Res. 2004, 2, 739-750.
98. Farace, P.; Galie, M.; Merigo, F.; Daducci, A.; Calderan, L.; Nicolato, E.; Degrassi, A.; Pesenti, E.; Sbarbati, A.; Marzola, P. Inhibition of tyrosine kinase receptors by SU6668 promotes abnormal stromal development at the periphery of carcinomas. Br. J. Cancer 2009, 10, 1575-1580.
99. Checkley, D.; Tessier, J.J.; Kendrew, J.; Waterton, J.C.; Wedge, S.R. 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, 10, 1889-1895.
100. Wilmes, L.J.; Pallavicini, M.G.; Fleming, L.M.; Gibbs, J.; Wang, D.; Li, K.L.; Partridge, S.C.; Henry, R.G.; Shalinsky, D.R.; Hu-Lowe, D.; et al. AG-013736, a novel inhibitor of VEGF receptor tyrosine kinases, inhibits breast cancer growth and decreases vascular permeability as detected by dynamic contrast-enhanced magnetic resonance imaging. Magn. Reson. Imaging 2007, 3, 319-327.
101. Dafni, H.; Kim, S.J.; Bankson, J.A.; Sankaranarayanapillai, M.; Ronen, S.M. Macromolecular dynamic contrast-enhanced (DCE)-MRI detects reduced vascular permeability in a prostate cancer bone metastasis model following anti-platelet-derived growth factor receptor (PDGFR) therapy, indicating a drop in vascular endothelial growth factor receptor (VEGFR) activation. Magn. Reson. Med. 2008, 4, 822-833.
102. Kamoun, W.S.; Ley, C.D.; Farrar, C.T.; Duyverman, A.M.; Lahdenranta, J.; Lacorre, D.A.; Batchelor, T.T.; di Tomaso, E.; Duda, D.G.; Munn, L.L.; et al. Edema control by cediranib, a vascular endothelial growth factor receptor-targeted kinase inhibitor, prolongs survival despite persistent brain tumor growth in mice. J. Clin. Oncol. 2009, 15, 2542-2552.
103. Merz, M.; Komljenovic, D.; Zwick, S.; Semmler, W.; Bauerle, T. Sorafenib tosylate and paclitaxel induce anti-angiogenic, anti-tumour and anti-resorptive effects in experimental breast cancer bone metastases. Eur. J. Cancer 2011, 2, 277-286.
104. Bhujwalla, Z.M.; Artemov, D.; Natarajan, K.; Solaiyappan, M.; Kollars, P.; Kristjansen, P.E. Reduction of vascular and permeable regions in solid tumors detected by macromolecular contrast magnetic resonance imaging after treatment with antiangiogenic agent TNP-470. Clin. Cancer Res. 2003, 1, 355-362.
105. Lane, H.A.; Wood, J.M.; McSheehy, P.M.; Allegrini, P.R.; Boulay, A.; Brueggen, J.; Littlewood-Evans, A.; Maira, S.M.; Martiny-Baron, G.; Schnell, C.R.; et al. mTOR inhibitor RAD001 (everolimus) has antiangiogenic/vascular properties distinct from a VEGFR tyrosine kinase inhibitor. Clin. Cancer Res. 2009, 5, 1612-1622.
106. Yang, J.; Kim, J.H.; Im, G.H.; Heo, H.; Yoon, S.; Lee, J.; Lee, J.H.; Jeon, P. Evaluation of antiangiogenic effects of a new synthetic candidate drug KR-31831 on xenografted ovarian carcinoma using dynamic contrast enhanced MRI. Korean J. Radiol. 2011, 5, 602-610.
107. Ansiaux, R.; Baudelet, C.; Jordan, B.F.; Beghein, N.; Sonveaux, P.; de Wever, J.; Martinive, P.; Gregoire, V.; Feron, O.; Gallez, B. Thalidomide radiosensitizes tumors through early changes in the tumor microenvironment. Clin. Cancer Res. 2005, 2, 743-750.
108. Cyran, C.C.; Sennino, B.; Chaopathomkul, B.; Fu, Y.; Rogut, V.S.; Shames, D.M.; Wendland, M.F.; McDonald, D.M.; Brasch, R.C. Magnetic resonance imaging for monitoring the effects of thalidomide on experimental human breast cancers. Eur. Radiol. 2009, 1, 121-131.
109. Zhao, D.; Jiang, L.; Hahn, E.W.; Mason, R.P. Continuous low-dose (metronomic) chemotherapy on rat prostate tumors evaluated using MRI in vivo and comparison with histology. Neoplasia 2005, 7, 678-687.
110. Lee, D.F.; Hung, M.C. All roads lead to mTOR: Integrating inflammation and tumor angiogenesis. Cell. Cycle 2007, 24, 3011-3014.
111. Beauregard, D.A.; Thelwall, P.E.; Chaplin, D.J.; Hill, S.A.; Adams, G.E.; Brindle, K.M. Magnetic resonance imaging and spectroscopy of combretastatin A4 prodrug-induced disruption of tumour perfusion and energetic status. Br. J. Cancer 1998, 11, 1761-1767.
112. Beauregard, D.A.; Hill, S.A.; Chaplin, D.J.; Brindle, K.M. The susceptibility of tumors to the antivascular drug combretastatin A4 phosphate correlates with vascular permeability. Cancer Res. 2001, 18, 6811-6815.
113. Beauregard, D.A.; Pedley, R.B.; Hill, S.A.; Brindle, K.M. Differential sensitivity of two adenocarcinoma xenografts to the anti-vascular drugs combretastatin A4 phosphate and 5,6-dimethylxanthenone-4-acetic acid, assessed using MRI and MRS. NMR Biomed. 2002, 2, 99-105.
114. Salmon, H.W.; Siemann, D.W. Effect of the second-generation vascular disrupting agent OXi4503 on tumor vascularity. Clin. Cancer Res. 2006, 13, 4090-4094.
115. Lankester, K.J.; Maxwell, R.J.; Pedley, R.B.; Dearling, J.L.; Qureshi, U.A.; El-Emir, E.; Hill, S.A.; Tozer, G.M. Combretastatin A-4-phosphate effectively increases tumor retention of the therapeutic antibody, 131I-A5B7, even at doses that are sub-optimal for vascular shut-down. Int. J. Oncol. 2007, 2, 453-460.
116. Salmon, B.A.; Salmon, H.W.; Siemann, D.W. Monitoring the treatment efficacy of the vascular disrupting agent CA4P. Eur. J. Cancer 2007, 10, 1622-1629.
117. Nielsen, T.; Murata, R.; Maxwell, R.J.; Stødkilde-Jørgensen, H.; Ostergaard, L.; Horsman, M.R. Preclinical studies to predict efficacy of vascular changes induced by combretastatin a-4 disodium phosphate in patients. Int. J. Radiat. Oncol. Biol. Phys. 2008, 3, 859-866.
118. Zhao, D.; Richer, E.; Antich, P.P.; Mason, R.P. Antivascular effects of combretastatin A4 phosphate in breast cancer xenograft assessed using dynamic bioluminescence imaging and confirmed by MRI. FASEB J. 2008, 7, 2445-2451.
119. Nielsen, T.; Mouridsen, K.; Maxwell, R.J.; Stødkilde-Jørgensen, H.; Østergaard, L.; Horsman, M.R. Segmentation of dynamic contrast enhanced magnetic resonance imaging data. Acta Oncol. 2008, 7, 1265-1270.
120. Nielsen, T.; Murata, R.; Maxwell, R.J.; Stodkilde-Jorgensen, H.; Ostergaard, L.; Ley, C.D.; Kristjansen, P.E.; Horsman, M.R. Non-invasive imaging of combretastatin activity in two tumor models: Association with invasive estimates. Acta Oncol. 2010, 7, 906-913.
121. Bohndiek, S.E.; Kettunen, M.I.; Hu, D.E.; Witney, T.H.; Kennedy, B.W.; Gallagher, F.A.; Brindle, K.M. Detection of tumor response to a vascular disrupting agent by hyperpolarized 13C magnetic resonance spectroscopy. Mol. Cancer. Ther. 2010, 12, 3278-3288.
122. Galbraith, S.M.; Maxwell, R.J.; Lodge, M.A.; Tozer, G.M.; Wilson, J.; Taylor, N.J.; Stirling, J.J.; Sena, L.; Padhani, A.R.; Rustin, G.J. S. Combretastatin A4 phosphate has tumor antivascular activity in rat and man as demonstrated by dynamic magnetic resonance imaging. J. Clin. Oncol. 2003, 15, 2831-2842.
123. Zhao, D.; Jiang, L.; Hahn, E.W.; Mason, R.P. Tumor physiologic response to combretastatin A4 phosphate assessed by MRI. Int. J. Radiat. Oncol. Biol. Phys. 2005, 3, 872-880.
124. Thoeny, H.C.; Keyzer, F.D.; Vandecaveye, V.; Chen, F.; Sun, X.; Bosmans, H.; Hermans, R.; Verbeken, E.K.; Boesch, C.; Marchal, G.; et al. Effect of vascular targeting agent in rat tumor model: Dynamic contrast-enhanced versus diffusion-weighted MR imaging. Radiology 2005, 2, 492-499.
125. Wang, H.; Cona, M.M.; Chen, F.; Yu, J.; Feng, Y.; Li, J.; Keyzer, F.D.; Marchal, G.; Ni, Y. Comparison of two vascular-disrupting agents at a clinically relevant dose in rodent liver tumors with multiparametric magnetic resonance imaging biomarkers. Anticancer Drugs 2012, 1, 12-21.
126. Evelhoch, J.L.; LoRusso, P.M.; He, Z.; DelProposto, Z.; Polin, L.; Corbett, T.H.; Langmuir, P.; Wheeler, C.; Stone, A.; Leadbetter, J.; et al. Magnetic resonance imaging measurements of the response of murine and human tumors to the vascular-targeting agent ZD6126. Clin. Cancer Res. 2004, 11, 3650-3657.
127. Vogel-Claussen, J.; Gimi, B.; Artemov, D.; Bhujwalla, Z.M. Diffusion-weighted and macromolecular contrast enhanced MRI of tumor response to antivascular therapy with ZD6126. Cancer. Biol. Ther. 2007, 9, 1469-1475.
128. Robinson, S.P.; McIntyre, D.J.O.; Checkley, D.; Tessier, J.J.; Howe, F.A.; Griffiths, J.R.; Ashton, S.E.; Ryan, A.J.; Blakey, D.C.; Waterton, J.C. Tumour dose response to the antivascular agent ZD6126 assessed by magnetic resonance imaging. Br. J. Cancer 2003, 10, 1592-1597.
129. McIntyre, D.J.; Robinson, S.P.; Howe, F.A.; Griffiths, J.R.; Ryan, A.J.; Blakey, D.C.; Peers, I.S.; Waterton, J.C. Single dose of the antivascular agent, ZD6126 (N-acetylcolchinol-O-phosphate), reduces perfusion for at least 96 hours in the GH3 prolactinoma rat tumor model. Neoplasia 2004, 2, 150-157.
130. Bradley, D.P.; Tessier, J.J.; Ashton, S.E.; Waterton, J.C.; Wilson, Z.; Worthington, P.L.; Ryan, A.J. Correlation of MRI biomarkers with tumor necrosis in Hras5 tumor xenograft in athymic rats. Neoplasia 2007, 5, 382-391.
131. Wang, H.; Li, J.; Chen, F.; De Keyzer, F.; Yu, J.; Feng, Y.; Nuyts, J.; Marchal, G.; Ni, Y. Morphological, functional and metabolic imaging biomarkers: Assessment of vascular-disrupting effect on rodent liver tumours. Eur. Radiol. 2010, 8, 2013-2026.
132. Bertelsen, L.B.; Shen, Y.Y.; Nielsen, T.; Stodkilde-Jorgensen, H.; Lloyd, G.K.; Siemann, D.W.; Horsman, M.R. Vascular effects of plinabulin (NPI-2358) and the influence on tumour response when given alone or combined with radiation. Int. J. Radiat. Biol. 2011, 11, 1126-1134.
133. Durrant, D.; Corwin, F.; Simoni, D.; Zhao, M.; Rudek, M.A.; Salloum, F.N.; Kukreja, R.C.; Fatouros, P.P.; Lee, R.M. cis-3,4',5-Trimethoxy-3'-aminostilbene disrupts tumor vascular perfusion without damaging normal organ perfusion. Cancer Chemother. Pharmacol. 2009, 2, 191-200.
134. Natsume, T.; Watanabe, J.; Ogawa, K.; Yasumura, K.; Kobayashi, M. Tumor-specific antivascular effect of TZT-1027 (Soblidotin) elucidated by magnetic resonance imaging and confocal laser scanning microscopy. Cancer. Sci. 2007, 4, 598-604.
135. Luo, Y.; Hradil, V.P.; Frost, D.J.; Rosenberg, S.H.; Gordon, G.B.; Morgan, S.J.; Gagne, G.D.; Cox, B.F.; Tahir, S.K.; Fox, G.B. ABT-751, a novel tubulin-binding agent, decreases tumor perfusion and disrupts tumor vasculature. Anticancer Drugs 2009, 6, 483-492.
136. Seshadri, M.; Spernyak, J.A.; Mazurchuk, R.; Camacho, S.H.; Oseroff, A.R.; Cheney, R.T.; Bellnier, D.A. Tumor vascular response to photodynamic therapy and the antivascular agent 5,6-dimethylxanthenone-4-acetic acid: implications for combination therapy. Clin. Cancer Res. 2005, 11, 4241-4250.
137. Seshadri, M.; Mazurchuk, R.; Spernyak, J.A.; Bhattacharya, A.; Rustum, Y.M.; Bellnier, D.A. Activity of the vascular-disrupting agent 5,6-dimethylxanthenone-4-acetic acid against human head and neck carcinoma xenografts. Neoplasia 2006, 7, 534-542.
138. Seshadri, M.; Spernyak, J.A.; Maiery, P.G.; Cheney, R.T.; Mazurchuk, R.; Bellnier, D.A. Visualizing the acute effects of vascular-targeted therapy in vivo using intravital microscopy and magnetic resonance imaging: Correlation with endothelial apoptosis, cytokine induction, and treatment outcome. Neoplasia 2007, 2, 128-135.
139. Seshadri, M.; Bellnier, D.A.; Cheney, R.T. Assessment of the early effects of 5,6-dimethylxanthenone-4-acetic acid using macromolecular contrast media-enhanced magnetic resonance imaging: Ectopic versus orthotopic tumors. Int. J. Radiat. Oncol. Biol. Phys. 2008, 4, 1198-1207.
140. Seshadri, M.; Ciesielski, M.J. MRI-based characterization of vascular disruption by 5,6-dimethylxanthenone-acetic acid in gliomas. J. Cereb. Blood Flow Metab. 2009, 8, 1373-1382.
141. Seshadri, M.; Toth, K. Acute vascular disruption by 5,6-dimethylxanthenone-4-acetic Acid in an orthotopic model of human head and neck cancer. Transl. Oncol. 2009, 3, 121-127
142. Seshadri, M.; Sacadura, N.T.; Coulthard, T. Monitoring antivascular therapy in head and neck cancer xenografts using contrast-enhanced MR and US imaging. Angiogenesis 2011, 4, 491-501.
143. Barbera, M.; Kettunen, M.I.; Caputo, A.; Hu, D.E.; Gobbi, S.; Brindle, K.M.; Carrara, M. Immune-modulating and anti-vascular activities of two xanthenone acetic acid analogues: A comparative study to DMXAA. Int. J. Oncol. 2009, 1, 273-279.
144. McPhail, L.D.; McIntyre, D.J.; Ludwig, C.; Kestell, P.; Griffiths, J.R.; Kelland, L.R.; Robinson, S.P. Rat tumor response to the vascular-disrupting agent 5,6-dimethylxanthenone-4-acetic acid as measured by dynamic contrast-enhanced magnetic resonance imaging, plasma 5-hydroxyindoleacetic acid levels, and tumor necrosis. Neoplasia 2006, 3, 199-206.
145. Tang, J.S.; Choy, G.; Bernardo, M.; Thomasson, D.; Libutti, S.K.; Choyke, P.L. Dynamic contrast-enhanced magnetic resonance imaging in the assessment of early response to tumor necrosis factor alpha in a colon carcinoma model. Invest. Radiol. 2006, 9, 691-696.
146. Haney, C.R.; Parasca, A.D.; Fan, X.; Bell, R.M.; Zamora, M.A.; Karczmar, G.S.; Mauceri, H.J.; Halpern, H.J.; Weichselbaum, R.R.; Pelizzari, C.A. Characterization of response to radiation mediated gene therapy by means of multimodality imaging. Magn. Reson. Med. 2009, 2, 348-356.
147. Kiessling, F.; Huber, P.E.; Grobholz, R.; Heilmann, M.; Meding, J.; Lichy, M.P.; Fink, C.; Krix, M.; Peschke, P.; Schlemmer, H. Dynamic magnetic resonance tomography and proton magnetic resonance spectroscopy of prostate cancers in rats treated by radiotherapy. Invest. Radiol. 2004, 1, 34-44.
148. De Keyzer, F.; Vandecaveye, V.; Thoeny, H.; Chen, F.; Ni, Y.; Marchal, G.; Hermans, R.; Nuyts, S.; Landuyt, W.; Bosmans, H. Dynamic contrast-enhanced and diffusion-weighted MRI for early detection of tumoral changes in single-dose and fractionated radiotherapy: Evaluation in a rat rhabdomyosarcoma model. Eur. Radiol. 2009, 11, 2663-2671.
149. Zilberstein, J.; Schreiber, S.; Bloemers, M.C.; Bendel, P.; Neeman, M.; Schechtman, E.; Kohen, F.; Scherz, A.; Salomon, Y. Antivascular treatment of solid melanoma tumors with bacteriochlorophyll-serine-based photodynamic therapy. Photochem. Photobiol. 2001, 3, 257-266.
150. Eichhorn, M.E.; Becker, S.; Strieth, S.; Werner, A.; Sauer, B.; Teifel, M.; Ruhstorfer, H.; Michaelis, U.; Griebel, J.; Brix, G.; et al. Paclitaxel encapsulated in cationic lipid complexes (MBT-0206) impairs functional tumor vascular properties as detected by dynamic contrast enhanced magnetic resonance imaging. Cancer. Biol. Ther. 2006, 1, 89-96.
151. Eichhorn, M.E.; Luedemann, S.; Strieth, S.; Papyan, A.; Ruhstorfer, H.; Haas, H.; Michaelis, U.; Sauer, B.; Teifel, M.; Enders, G.; et al. Cationic lipid complexed camptothecin (EndoTAG-2) improves antitumoral efficacy by tumor vascular targeting. Cancer. Biol. Ther. 2007, 6, 920-929.
152. O'Connor, J.P.; Jackson, A.; Parker, G.J.; Roberts, C.; Jayson, G.C. Dynamic contrast-enhanced MRI in clinical trials of antivascular therapies. Nat. Rev. Clin. Oncol. 2012, 3, 167-177.