Magnetic resonance angiography visualization of abnormal tumor vasculature in genetically engineered mice.

Previous research on the vasculature of tumor-bearing animals has focused upon the microvasculature. Magnetic resonance angiography (MRA) offers a noninvasive, complementary approach that provides information about larger vessels. Quantitative analysis of MRA images of spontaneous preclinical tumor models has not been previously reported. Eleven TgT121;p53+/- mice, which invariably develop choroid plexus carcinoma (CPC), and nine age-matched healthy controls were imaged using T1, T2, and a high-resolution three-dimensional time-of-flight MRA sequences at 3 T. Tumors and vessels were segmented to determine tumor volume and vascular attributes, including number of terminal branches, vessel count, and the average vessel radii of MRA-visible vessels within the tumor. Differences in the vasculature between tumor-bearing animals and healthy controls were analyzed statistically. Although the spatial resolution of MRA prohibits visualization of capillaries, a high density of intratumor blood vessels was visualized in CPC mice. A significant increase in terminal branch count and vessel count, but not average vessel radius, was observed in CPCs when compared with normal controls. Both terminal branch count and vessel count were highly correlated with tumor volume. This study represents the first MRA analysis of a spontaneous preclinical brain tumor model. Although the spatial resolution of MRA is less than histologic analysis, MRA-obtained vascular attributes provide useful information with full brain coverage. We show that consistent tumor vasculature properties can be determined by MRA. Such methods are critical for developing preclinical therapeutic testing and will help guide the development of human brain tumor analyses.

[1]  Daniel Rueckert,et al.  Nonrigid registration using free-form deformations: application to breast MR images , 1999, IEEE Transactions on Medical Imaging.

[2]  D. Hanahan,et al.  Cross-species comparison of angiogenesis during the premalignant stages of squamous carcinogenesis in the human cervix and K14-HPV16 transgenic mice. , 1997, Cancer research.

[3]  Eun Ja Lee,et al.  Perfusion MR Imaging in Gliomas: Comparison with Histologic Tumor Grade , 2001, Korean journal of radiology.

[4]  M. Muti,et al.  Perfusion MRI in the evaluation of the relationship between tumour growth, necrosis and angiogenesis in glioblastomas and grade 1 meningiomas , 2003, Neuroradiology.

[5]  S. Fox,et al.  c-Myc Interacts with Hypoxia to Induce Angiogenesis In vivo by a Vascular Endothelial Growth Factor-Dependent Mechanism , 2004, Cancer Research.

[6]  D. Hanahan,et al.  Direct Test of Potential Roles of EIIIA and EIIIB Alternatively Spliced Segments of Fibronectin in Physiological and Tumor Angiogenesis , 2004, Molecular and Cellular Biology.

[7]  A L Benabid,et al.  Cerebral blood volume mapping by MR imaging in the initial evaluation of brain tumors. , 2002, Journal of neuroradiology. Journal de neuroradiologie.

[8]  Marleen Verhoye,et al.  Assessment of the neovascular permeability in glioma xenografts by dynamic T1 MRI with Gadomer‐17 , 2002, Magnetic Resonance in Medicine.

[9]  S. Lowe,et al.  p53-Dependent apoptosis suppresses tumor growth and progression in vivo , 1994, Cell.

[10]  G. Magrane,et al.  Selective Inactivation of p53 Facilitates Mouse Epithelial Tumor Progression without Chromosomal Instability , 2001, Molecular and Cellular Biology.

[11]  R. Kerbel,et al.  Therapeutic potential of selective cyclooxygenase-2 inhibitors in the management of tumor angiogenesis. , 2003, Progress in experimental tumor research.

[12]  Yihai Cao Antiangiogenic cancer therapy. , 2004, Seminars in cancer biology.

[13]  Stephen R. Aylward,et al.  Initialization, noise, singularities, and scale in height ridge traversal for tubular object centerline extraction , 2002, IEEE Transactions on Medical Imaging.

[14]  D. Hanahan,et al.  Cathepsin cysteine proteases are effectors of invasive growth and angiogenesis during multistage tumorigenesis. , 2004, Cancer cell.

[15]  Glyn Johnson,et al.  High-grade gliomas and solitary metastases: differentiation by using perfusion and proton spectroscopic MR imaging. , 2002, Radiology.

[16]  A. Aguzzi,et al.  Angiogenesis in transgenic models of multistep angiogenesis. , 2004, Cancer treatment and research.

[17]  M. Dewhirst,et al.  Initial stages of tumor cell-induced angiogenesis: evaluation via skin window chambers in rodent models. , 2000, Journal of the National Cancer Institute.

[18]  Julien Jomier,et al.  Rigid and Deformable Vasculature-to-Image Registration: A Hierarchical Approach , 2004, MICCAI.

[19]  Guido Gerig,et al.  Abnormal Vessel Tortuosity as a Marker of Treatment Response of Malignant Gliomas: Preliminary Report , 2004, Technology in cancer research & treatment.

[20]  Glyn Johnson,et al.  Glioma grading: sensitivity, specificity, and predictive values of perfusion MR imaging and proton MR spectroscopic imaging compared with conventional MR imaging. , 2003, AJNR. American journal of neuroradiology.

[21]  A. Aguzzi,et al.  Angiogenesis in Transgenic Models of Multistep Carcinogenesis , 2004, Journal of Neuro-Oncology.

[22]  Jin-Suh Kim,et al.  Using relative cerebral blood flow and volume to evaluate the histopathologic grade of cerebral gliomas: preliminary results. , 2002, AJR. American journal of roentgenology.

[23]  Glyn Johnson,et al.  Dynamic, contrast‐enhanced perfusion MRI in mouse gliomas: Correlation with histopathology , 2003, Magnetic resonance in medicine.

[24]  Guido Gerig,et al.  Determining Malignancy of Brain Tumors by Analysis of Vessel Shape , 2004, MICCAI.

[25]  S. Pizer,et al.  Measuring tortuosity of the intracerebral vasculature from MRA images , 2003, IEEE Transactions on Medical Imaging.

[26]  J. Simons,et al.  Angiogenesis and prostate cancer: identification of a molecular progression switch. , 2001, Cancer research.

[27]  D. Hanahan,et al.  VEGF-A has a critical, nonredundant role in angiogenic switching and pancreatic beta cell carcinogenesis. , 2002, Cancer cell.

[28]  H. Aronen,et al.  Dynamic susceptibility contrast MRI of gliomas. , 2002, Neuroimaging clinics of North America.

[29]  Guido Gerig,et al.  Automatic brain tumor segmentation by subject specific modification of atlas priors. , 2003, Academic radiology.

[30]  T. van Dyke,et al.  Induction versus progression of brain tumor development: differential functions for the pRB- and p53-targeting domains of simian virus 40 T antigen , 1994, Molecular and cellular biology.