Top

Published in:

01-12-2008

Non-invasive assessment of tumor neovasculature: techniques and clinical applications

Authors: Rodolfo Perini, Regine Choe, Arjun G. Yodh, Chandra Sehgal, Chaitanya R. Divgi, Mark A. Rosen

Published in: Cancer and Metastasis Reviews | Issue 4/2008

Abstract

The ability to induce and sustain angiogenesis is regarded as one of the hallmarks of cancer growth and metastasis. Marked advances in understanding vascular physiology and mechanisms of angiogenesis have led to the development of vascularly-targeted anti-cancer therapies. Two broad subclasses of agents are in clinical use currently: those with anti-angiogenic activity (i.e. those that target angiogenic pathways) and those that have direct cytotoxic activity against proliferating endothelial cells (i.e. vascular disruptive agents (VDAs)). This article reviews the various imaging modalities, including magnetic resonance imaging, computed tomography, photon emission imaging (positron emission tomography and single photon emission computed tomography), ultrasound and optical (near-infrared absorption and scattering) techniques that have been used in an attempt to assess the status of tumor neovasculature in vivo. In each case, we describe the basic imaging methodology, methods for image quantification, technical standardization and reproducibility, and current and potential clinical applications for monitoring the status of tumor neovasculature before and during treatment with vascular targeted agents.

Carmeliet, P., & Jain, R. K. (2000). Angiogenesis in cancer and other diseases. Nature, 407, 249–257.PubMed

Hanahan, D., & Weinberg, R. A. (2000). The hallmarks of cancer. Cell, 100, 57–70.PubMed

O’Connor, J. P., Jackson, A., Parker, G. J., & Jayson, G. C. (2007). DCE-MRI biomarkers in the clinical evaluation of antiangiogenic and vascular disrupting agents. British Journal of Cancer, 96(2), 189–195.PubMed

Padhani, A. R. (2005). Where are we with imaging oxygenation in human tumours. Cancer Imaging, 5(1), 128–130.PubMed

Evelhoch, J., Garwood, M., Vigneron, D., Knopp, M., Sullivan, D., & Menkens, A. (2005). Expanding the use of magnetic resonance in the assessment of tumor response to therapy: workshop report. Cancer Research, 65(16), 7041–7044.PubMed

Leach, M. O., Brindle, K. M., Evelhoch, J., Griffiths, J. R., Horsman, M. R., Jackson, A., et al. (2005). The assessment of antiangiogenic and antivascular therapies in early-stage clinical trials using magnetic resonance imaging: issues and recommendations. British Journal of Cancer, 92(9), 1599–1610.PubMed

Roberts, C., Buckley, D. L., & Parker, G. J. M. (2006a). Comparison of errors associated with single- and multi-bolus injection protocols in low-temporal-resolution dynamic contrast-enhanced tracer kinetic analysis. Magnetic Resonance in Medicine, 56, 611–619.PubMed

Henderson, E., Rutt, B. K., & Lee, T. Y. (1998). Temporal sampling requirements for the tracer kinetics modeling of breast disease. Magnetic Resonance Imaging, 16, 1057–1073.PubMed

Evelhoch, J. (1999). Key factors in the acquisition of contrast kinetic data for oncology. Journal of Magnetic Resonance Imaging, 10, 254–259.PubMed

10.

Kety, S. S. (1951). The theory and applications of the exchange of inert gas at the lungs and tissues. Pharmacological Reviews, 3, 1–41.PubMed

11.

Tofts, P. S., Berkowitz, B., & Schnall, M. D. (1995). Quantitative analysis of dynamic Gd-DTPA enhancement in breast tumors using a permeability model. Magnetic Resonance of Medicine, 33, 564–568.

12.

Tofts, P. S., Brix, G., Buckley, D. L., Evelhoch, J., Henderson, E., Knopp, M. V., et al. (1999). Estimating kinetic parameters from dynamic contrast-enhanced T(1)-weighted MRI of a diffusable tracer: standardized quantities and symbols. Journal of Magnetic Resonance Imaging, 10, 223–232.PubMed

13.

Tofts, P. S., & Kermode, A. G. (1991). Measurement of the blood-brain barrier permeability and leakage space using dynamic MR imaging. 1. Fundamental concepts. Magnetic Resonance in Medicine, 17, 357–367.PubMed

14.

Yankeelov, T. E., Rooney, W. D., Li, X., & Springer, C. S. (2003). Variation of the relaxographic “shutter-speed” for transcytolemmal water exchange affects the CR bolustracking curve shape. Magnetic Resonance in Medicine, 50, 1151–1169.PubMed

15.

Li, S., Peck-Radosavljevic, M., Kienast, O., Preitfellner, J., Hamilton, G., & Kurtaran, A. (2003). Imaging gastrointestinal tumours using vascular endothelial growth factor-165 (VEGF165) receptor scintigraphy. Annals of Oncology, 4, 1274–1277.

16.

Galbraith, S. M., Lodge, M. A., Taylor, N. J., Rustin, G. J. S., Bentzen, S. M., Stirling, J. J., et al. (2002a). Reproducibility of dynamic contrast-enhanced MRI in human muscle and tumours: comparison of quantitative and semi-quantitative analysis. NMR in Biomedicine, 15, 132–142.PubMed

17.

Lankester, K. J., Taylor, N. J., Stirling, J. J., Boxall, J., d’Arcy, J. A., & Leach, M. O. (2005). Effects of platinum/taxane based chemotherapy on acute perfusion in human pelvic tumours measured by dynamic MRI. British Journal of Cancer, 93, 979–985.PubMed

18.

Roberts, C., Issa, B., Stone, A., Jackson, A., Waterton, J. C., & Parker, G. J. M. (2006b). Comparative study into the robustness of compartmental modeling and model-free analysis in DCE-MRI studies. Journal of Magnetic Resonance Imaging, 23, 554–563.PubMed

19.

Morgan, B., Utting, J. F., Higginson, A., Thomas, A. L., Steward, W. P., & Horsfield, M. A. (2006). A simple, reproducible method for monitoring the treatment of tumours Effect of thalidomide in hepatocellular carcinoma: assessment with power doppler US and analysis of circulating angiogenic factors. Radiology, 235, 509–516.

20.

Parker, G. J. M., Roberts, C., Macdonald, A., Buonaccorsi, G. A., Cheung, S., & Buckley, D. L. (2006). Experimentally derived functional form for a population-averaged high-temporal-resolution arterial input function for dynamic contrast-enhanced MRI. Magnetic Resonance in Medicine, 56, 993–1000.PubMed

21.

Knopp, M. V., Brix, G., Junkermann, H. J., & Sinn, H. P. (1994). MR mammography with pharmacokinetic mapping for monitoring of breast cancer treatment during neoadjuvant therapy. Magnetic Resonance Imaging Clinics of North America, 2, 633–658.PubMed

22.

Mross, K., Drevs, J., Muller, M., Medinger, M., Marme, D., Hennig, J., et al. (2005). Phase I clinical and pharmacokinetic study of PTK/ZK, a multiple VEGF receptor inhibitor, in patients with liver metastases from solid tumours. European Journal of Cancer, 23, 1291–1299.

23.

Liu, G., Rugo, H. S., Wilding, G., McShane, T. M., Evelhoch, J. L., Ng, C., et al. (2005). 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.[see comment]. Journal of Clinical Oncology, 23(24), 5464–5473.PubMed

24.

O’Donnell, A., Padhani, A. R., Hayes, C., Kakkar, A. J., Leach, M., Trigo, J. M., et al. (2005). A Phase I study of the angiogenesis inhibitor SU5416 (semaxanib) in solid tumours, incorporating dynamic contrast MR pharmacodynamic end points. British Journal of Cancer, 93(8), 876–883.PubMed

25.

Xiong, H. Q., Herbst, R., Faria, S. C., Scholz, C., Davis, D., Jackson, E. F., et al. (2004). A phase I surrogate endpoint study of SU6668 in patients with solid tumors. Investigational New Drugs, 22(4), 459–466.PubMed

26.

Thomas, A. L., Morgan, B., Horsfield, M. A., Higginson, A., Kay, A., & Lee, L. (2005). Phase I study of the safety, tolerability, pharmacokinetics, and pharmacodynamics of PTK787/ZK 222584 administered twice daily in patients with advanced cancer. Journal of Clinical Oncology, 23(18), 4162–4171.PubMed

27.

Morgan, B., Thomas, A. L., Drevs, J., Hennig, J., Buchert, M., Jivan, A., et al. (2003). 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.[see comment]. Journal of Clinical Oncology, 21, 3955–3964.PubMed

28.

Wedam, S. B., Low, J. A., Yang, S. X., Chow, C. K., Choyke, P. L., Danforth, D., et al. (2006). Antiangiogenic and antitumor effects of bevacizumab in patients with inflammatory and locally advanced breast cancer. Journal of Clinical Oncology, 24(5), 769–777.PubMed

29.

ODwyer, P. J., Rosen, M., Gallagher, M., Schwartz, B., & Flaherty, K. T. (2005). Pharmacodynamic study of BAY 43–9006 in patients with metastatic renal cell carcinoma. Journal of Clinical Oncology/ 2005 ASCO Annual Meeting Proceedings, 23, 3005.

30.

Hahn, O., Yeng, C., Medved, M., Karczmar, G. S., Kistner, E., & Manchen, B. (2007). Dyamic contrast enhanced MRI (DCE-MRI) pharmacodynamic (PD) study of sorafenib in metastatic renal cell carcinoma (RCC): Results of a randomized, phase II trial. Journal of Clinical Oncology/ 2007 ASCO Annual Meeting Proceedings, 25, 3545.

31.

Galbraith, S. M., Rustin, G. J. S., Lodge, M. A., Taylor, N. J., Stirling, J. J., & Jameson, M. (2002b). Effects of 5,6-dimethylxanthenone-4-acetic acid on human tumor microcirculation assessed by dynamic contrast-enhanced magnetic resonance imaging. Journal of Clinical Oncology, 20, 3826–3840.PubMed

32.

Dowlati, A., Robertson, K., Cooney, M., Petros, W. P., Stratford, M., Jesberger, J., et al. (2002). 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 Research, 62, 3408–3416.PubMed

33.

Galbraith, S. M., Maxwell, R. J., Lodge, M. A., Tozer, G. M., Wilson, J., & Taylor, N. J. (2003). Combretastatin A4 phosphate has tumor antivascular activity in rat and man as demonstrated by dynamic magnetic resonance imaging. Journal of Clinical Oncology, 21(15), 2831–2842.PubMed

34.

Stevenson, J. P., Rosen, M. A., Sun, W., Gallagher, M., Haller, D. G., Vaughn, D., et al. (2003). Phase I trial of the antivascular agent combretastatin A4 phosphate on a 5-day schedule to patients with Rosen, MS 43 cancer: magnetic resonance imaging evidence for altered tumor blood flow. Journal of Clinical Oncology, 21(23), 4428–4438.PubMed

35.

Evelhoch, J. L., LoRusso, P. M., He, Z., DelProposto, Z., Polin, L., Corbett, T. H., et al. (2004). Magnetic resonance imaging measurements of the response of murine and human tumors to the vasculartargeting agent ZD6126. Clinical Cancer Research, 10(11), 3650–3657.PubMed

36.

Barrett, T., Kobayashi, H., Brechbiel, M., & Choyke, P. L. (2006). Macromolecular MRI contrast agents for imaging tumor angiogenesis. European Journal of Radiology, 60, 353–366.PubMed

37.

Preda, A., Novikov, V., Moglich, M., Turetschek, K., Shames, D. M., & Brasch, R. C. (2004). MRI monitoring of Avastin antiangiogenesis Rosen, MS 42 therapy using B22956/1, a new blood pool contrast agent, in an experimental model of human cancer. Journal of Magnetic Resonance Imaging, 20, 865–873.PubMed

38.

Marzola, P., Degrassi, A., Calderan, L., Farace, P., Nicolato, E., Crescimanno, C., et al. (2005). Early antiangiogenic activity of SU11248 evaluated in vivo by dynamic contrast-enhanced magnetic resonance imaging in an experimental model of colon carcinoma. Clinical Cancer of Research, 11, 5827–5832.

39.

Goyen, M., Edelman, M., Perreault, P., O’Riordan, E., Bertoni, H., Taylor, J., et al. (2005). MR angiography of aortoiliac occlusive disease: a phase III study of the safety and effectiveness of the bloodpool contrast agent MS-325. Radiology, 236, 825–833.PubMed

40.

Detre, J. A., & Alsop, D. C. (1999). Perfusion magnetic resonance imaging with continuous arterial spin labeling: methods and clinical applications in the central nervous system. European Journal of Radiology, 30(2), 115–124.PubMed

41.

Alsop, D. C., & Detre, J. A. (1998). Multisection cerebral blood flow MR imaging with continuous arterial spin labeling. Radiology, 208, 410–416.PubMed

42.

Wintermark, M., Sesay, M., Barbier, E., Borbely, K., Dillon, W. P., Eastwood, J. D., et al. (2005). Comparative overview of brain perfusion imaging techniques. Stroke, 36(9), e83–e99.PubMed

43.

Wolf, R. L., & Detre, J. A. (2007). Clinical neuroimaging using arterial spin-labeled perfusion magnetic resonance imaging. Neurotherapeutics, 4(3), 346–359.PubMed

44.

Kimura, H., Takeuchi, H., Koshimoto, Y., Arishima, H., Uematsu, H., & Kawamura, Y. (2006). Perfusion imaging of meningioma by using continuous arterial spin-labeling: comparison with dynamic susceptibility-weighted contrastenhanced MR images and histopathologic features. American Journal of Neuroradiology, 27(1), 85–93.PubMed

45.

Wolf, R. L., Wang, J., Wang, S., Melhem, E. R., O’Rourke, D. M., & Judy, K. D. (2005). Grading of CNS neoplasms using continuous arterial spin labeled perfusion MR imaging at 3 Tesla. Journal of Magnetic Resonance Imaging, 22(4), 475–482.PubMed

46.

Boss, A., Martirosian, P., Schraml, C., Clasen, S., Fenchel, M., & Anastasiadis, A. (2006). Morphological, contrast-enhanced and spin labeling perfusion imaging for monitoring of relapse after RF ablation of renal cell carcinomas. European Radiology, 16(6), 1226–1236.PubMed

47.

De Bazelaire, C., Rofsky, N. M., Duhamel, G., Michaelson, M. D., George, D., & Alsop, D. C. (2005). Arterial spin labeling blood flow magnetic resonance imaging for the characterization of metastatic renal cell carcinoma(1). Academic Radiology, 12(3), 347–357.PubMed

48.

Logothetis, N. K., & Pfeuffer, J. (2004). On the nature of the BOLD fMRI contrast mechanism. Magnetic Resonance Imaging, 22(10), 1517–1531.PubMed

49.

Hillis, A. E. (2007). Magnetic resonance perfusion imaging in the study of language. Brain & Language, 102(2), 165–175.

50.

Gaillard, W. D., Grandin, C. B., & Xu, B. (2001). Developmental aspects of pediatric fMRI: considerations for image acquisition, analysis, and interpretation. Neuroimage, 13, 239–249.PubMed

51.

Mattay, V. S., & Weinberger, D. R. (1999). Organization of the human motor system as studied by functional magnetic resonance imaging. European Journal of Radiology, 30(2), 105–114.PubMed

52.

Thoeny, H. C., Zumstein, D., Simon-Zoula, S., Eisenberger, U., De Keyzer, F., Hofmann, L., et al. (2006). Functional evaluation of transplanted kidneys with diffusion-weighted and BOLD MR imaging: initial experience. Radiology, 241, 812–821.PubMed

53.

Prasad, P. V. (2006). Evaluation of intra-renal oxygenation by BOLD MRI. Nephron clinical practice, 103(2), c58–c65.PubMed

54.

dos Santos, E. A., Li, L., Ji, L., & Prasad, P. V. (2007). Early changes with diabetes in renal medullary hemodynamics as evaluated by fiberoptic probes and BOLD magnetic resonance imaging. Investigative Radiology, 42(3), 157–162.PubMed

55.

Prasad, P. V., & Priatna, A. (1999). Functional imaging of the kidneys with fast MRI techniques. European Journal of Radiology, 29(2), 133–148.PubMed

56.

Robinson, S. P., Howe, F. A., Rodrigues, L. M., Stubbs, M., & Griffiths, J. R. (1998). Magnetic resonance imaging techniques for monitoring changes in tumor oxygenation and blood flow. Seminars in Radiation Oncology, 8(3), 197–207.PubMed

57.

Rijpkema, M., Kaanders, J. H. A. M., Joosten, F. B. M., van der Kogel, A. J., & Heerschap, A. (2002). Effects of breathing a hyperoxic hypercapnic gas mixture on blood oxygenation and vascularity of head-and-neck tumors as measured by magnetic resonance imaging. International Journal of Radiation Oncology, Biology, Physics, 53(5), 1185–1191.PubMed

58.

Taylor, N. J., Baddeley, H., Goodchild, K. A., Powell, M. E., Thoumine, M., Culver, L. A., et al. (2001). BOLD MRI of human tumor oxygenation during carbogen breathing. Journal of Magnetic Resonance Imaging, 14, 156–163.PubMed

59.

Gilead, A., Meir, G., & Neeman, M. (2004). The role of angiogenesis, vascular maturation, regression and stroma infiltration in dormancy and growth of implanted MLS ovarian carcinoma spheroids. International Journal of Cancer, 108, 524–531.

60.

Axel, L. (1980). Cerebral blood flow determination by rapid-sequence computed tomography: theoretical analysis. Radiology, 137, 679–686.PubMed

61.

Dawson, P. (2006). Functional imaging in CT. European Journal of Radiology, 60(3), 331–340.PubMed

62.

Laking, G. R., West, C. M. L., Buckley, D. L., Matthews, J., & Price, P. M. (2006). Imaging vascular physiology to monitor cancer treatment. Critical Oncology Hematology, 58(2), 95–113.

63.

Miles, K. A. (2003). Perfusion CT for the assessment of tumour vascularity: which protocol. British Journal of Radiology, 76, S36–S42.PubMed

64.

Bisdas, S., Konstantinou, G. N., Lee, P. S., Thng, C. H., Wagenblast, J., & Baghi, M. (2007). Dynamic contrast-enhanced CT of head and neck tumors: perfusion measurements using a distributed-parameter tracer kinetic model. Initial results and comparison with deconvolution-based analysis. Physics in Medicine and Biology, 52, 6181–6196.PubMed

65.

Haider, M. A., Milosevic, M., Fyles, A., Sitartchouk, I., Yeung, I., & Henderson, E. (2005). Assessment of the tumor microenvironment in cervix cancer using dynamic contrast enhanced CT, interstitial fluid pressure and oxygen measurements. International Journal of Radiation Oncology, Biology, Physics, 62(4), 1100–1107.PubMed

66.

Mayr, N. A., Yuh, W. T., Magnotta, V. A., Ehrhardt, J. C., Wheeler, J. A., Sorosky, J. I., et al. (1996). Tumor perfusion studies using fast magnetic resonance imaging technique in advanced cervical cancer: a new noninvasive predictive assay. International Journal of Radiation Oncology, Biology, Physics, 36, 623–633.PubMed

67.

Bellomi, M., Petralia, G., Sonzogni, A., Zampino, M. G., & Rocca, A. (2007). CT perfusion for the monitoring of neoadjuvant chemotherapy and radiation therapy in rectal carcinoma: initial experience. Radiology, 244(2), 486–493.PubMed

68.

Koukourakis, M. I., Mavanis, I., Kouklakis, G., Pitiakoudis, M., Minopoulos, G., & Manolas, C. (2007). Early antivascular effects of bevacizumab anti-VEGF monoclonal antibody on colorectal carcinomas assessed with functional CT imaging. American Journal of Clinical Oncology, 30(3), 315–318.PubMed

69.

Zima, A., Carlos, R., Gandhi, D., Case, I., Teknos, T., & Mukherji, S. K. (2007). Can pretreatment CT perfusion predict response of advanced squamous cell carcinoma of the upper aerodigestive tract treated with induction chemotherapy. American Journal of Neuroradiology, 28(2), 328–334.PubMed

70.

Makari, Y., Yasuda, T., Doki, Y., Miyata, H., Fujiwara, Y., Takiguchi, S., et al. (2007). Correlation between tumor blood Flo w assessed by perfusion CT and effect of neoadjuvant therapy in advanced esophageal Cancers. Journal of Surgical Oncology, 96, 220–229.PubMed

71.

Schnall, M. D., & Rosen, M. A. (2006). Primer on imaging technologies for cancer. Journal of Clinical Oncology, 24(20), 3225–3233.PubMed

72.

Huang, S. C. (2000). Anatomy of SUV. Standardized uptake value. Nuclear Medicine and Biology, 27, 643–646.PubMed

73.

Westerterp, M., Pruim, J., Oyen, W., Hoekstra, O., Paans, A., & Visser, E. (2007). Quantification of FDG PET studies using standardised uptake values in multi-centre trials: effects of image reconstruction, resolution and ROI definition parameters. European Journal of Nuclear Medicine and Molecular Imaging, 34, 392–404.PubMed

74.

Madsen, M. T. (2007). Recent advances in SPECT imaging. Journal of Nuclear Medicine, 48(4), 661–673.PubMed

75.

Beyer, T., Townsend, D. W., Brun, T., Kinahan, P. E., Charron, M., & Roddy, R. (2000). A combined PET/CT scanner for clinical oncology. Journal of Nuclear Medicine, 41, 1369–1379.PubMed

76.

Surti, S., Kuhn, A., Werner, M. E., Perkins, A. E., Kolthammer, J., & Karp, J. S. (2007). Performance of Philips Gemini TF PET/CT scanner with special consideration for its time-of-flight imaging capabilities. Journal of Nuclear Medicine, 48, 471–480.PubMed

77.

Phelps, M. E., Huang, S. C., Hoffman, E. J., & Kuhl, D. E. (1979). Validation of tomographic measurement of cerebral blood volume with C-11-labeled carboxyhemoglobin. Journal of Nuclear Medicine, 20, 328–334.PubMed

78.

Martin, W. R., Powers, W. J., & Raichle, M. E. (1987). Cerebral blood volume measured with inhaled C15O and positron emission tomography. Journal of Cerebral Blood Flow and Metabolism, 7, 421–426.PubMed

79.

Herscovitch, P., Markham, J., & Raichle, M. E. (1983). Brain blood flow measured with intravenous H2(15)O. I. Theory and error analysis. Journal of Nuclear Medicine, 24, 782–789.PubMed

80.

West, J. B., & Dollery, C. T. (1962). Uptake of oxygen-15-labeled CO2 compared with carbon-11-labeled CO2 in the lung. Journal of Applied Physiology, 17(1), 9–13.PubMed

81.

Taniguchi, H., Kunishima, S., & Koh, T. (2003). The reproducibility of independently measuring human regional hepatic arterial, portal and total hepatic blood flow using [15O]water and positron emission tomography. Nuclear Medicine Communications, 24(5), 497–501.PubMed

82.

Wells, P., Jones, T., & Price, P. (2003). Assessment of inter- and intrapatient variability in C15O2 positron emission tomography measurements of blood flow in patients with intra-abdominal cancers. Clinical Cancer Research, 9, 6350–6356.PubMed

83.

Wilson, C. B., Lammertsma, A. A., McKenzie, C. G., Sikora, K., & Jones, T. (1992). Measurements of blood flow and exchanging water space in breast tumors using positron emission tomography: a rapid and noninvasive dynamic method. Cancer Research, 52, 1592–1597.PubMed

84.

Mankoff, D. A., Dunnwald, L. K., Gralow, J. R., Ellis, G. K., Schubert, E. K., & Charlop, A. W. (2002). [Tc-99m]-sestamibi uptake and washout in locally advanced breast cancer are correlated with tumor blood flow. Nuclear Medicine Biology, 29(7), 719–727.

85.

Mankoff, D. A., Dunnwald, L. K., Gralow, J. R., Ellis, G. K., Schubert, E. K., & Tseng, J. (2003). Changes in blood flow and metabolism in locally advanced breast cancer treated with neoadjuvant chemotherapy. Journal of Nuclear Medicine, 44(11), 1806–1814.PubMed

86.

Miller, K. D., Soule, S. E., Calley, C., Emerson, R. E., Hutchins, G. D., & Kopecky, K. (2005). Randomized phase II trial of the anti-angiogenic potential of doxorubicin and docetaxel; primary chemotherapy as Biomarker Discovery Laboratory. Breast Cancer Research and Treatment, 89(2), 187–197.PubMed

87.

Kurdziel, K. A., Figg, W. D., Carrasquillo, J. A., Huebsch, S., Whatley, M., Sellers, D., et al. (2003). Using positron emission tomography 2-deoxy-2-[18F]fluoro-D-glucose, 11CO, and 15O-water for monitoring androgen independent prostate cancer. Molecular Imaging and Biology, 5, 86–93.PubMed

88.

Herbst, R. S., Mullani, N. A., Davis, D. W., Hess, K. R., McConkey, D. J., Charnsangavej, C., et al. (2002). Development of biologic markers of response and assessment of antiangiogenic activity in a clinical trial of human recombinant endostatin. Journal of Clinical Oncology, 20(18), 3804–3814.PubMed

89.

Lara, P. N., Quinn, D. I., Margolin, K., Meyers, F. J., Longmate, J., Frankel, P., et al. (2003). SU5416 plus interferon alpha in advanced renal cell carcinoma: a phase II California Cancer Consortium Study with biological and imaging correlates of angiogenesis inhibition. Clinical Cancer Research, 9, 4772–4781.PubMed

90.

Anderson, H., Yap, J. T., Wells, P., Miller, M. P., Propper, D. J., & Price, P. (2003a). Measurement of renal tumour and normal tissue perfusion using positron emission tomography in a phase II clinical trial of razoxane. British Journal of Cancer, 89(2), 262–267.PubMed

91.

Anderson, H. L., Yap, J. T., Miller, M. P., Robbins, A., Jones, T., & Price, P. M. (2003b). Assessment of pharmacodynamic vascular response in a phase I trial of combretastatin A4 phosphate. Journal of Clinical Oncology, 21(15), 2823–2830.PubMed

92.

Logan, T. F., Jadali, F., Egorin, M. J., Mintun, M., Sashin, D., Gooding, W. E., et al. (2002). Decreased tumor blood flow as measured by positron emission tomography in cancer patients treated with interleukin-1 and carboplatin on a phase I trial. Cancer Chemotherapy and Pharmacology, 50(6), 433–444.PubMed

93.

Hockel, M., Schlenger, K., Aral, B., Mitze, M., Schaffer, U., & Vaupel, P. (1996). Association between tumor hypoxia and malignant progression in advanced cancer of the uterine cervix. Cancer Research, 56(19), 4509–4515.PubMed

94.

Fyles, A., Milosevic, M., Hedley, D., Pintilie, M., Levin, W., & Manchul, L. (2002). Tumor hypoxia has independent predictor impact only in patients with nodenegative cervix cancer. Journal of Clinical Oncology, 20(3), 680–687.PubMed

95.

Brizel, D. M., Dodge, R. K., Clough, R. W., & Dewhirst, M. W. (1999). Oxygenation of head and neck cancer: changes during radiotherapy and impact on treatment outcome. Radiotherapy and Oncology, 53, 113–117.PubMed

96.

Brizel, D. M., Scully, S. P., Harrelson, J. M., Layfield, L. J., Bean, J. M., & Prosnitz, L. R. (1996). Tumor oxygenation predicts for the likelihood of distant metastases in human soft tissue sarcoma. Cancer Research, 56, 941–943.PubMed

97.

Nordsmark, M., Alsner, J., Keller, J., Nielsen, O. S., Jensen, O. M., & Horsman, M. R. (2001). Hypoxia in human soft tissue sarcomas: adverse impact on survival and no association with p53 mutations. British Journal of Cancer, 84(8), 1070–1075.PubMed

98.

Nordsmark, M., & Overgaard, J. (2000). A confirmatory prognostic study on oxygenation status and loco-regional control in advanced head and neck squamous cell carcinoma treated by radiation therapy. Radiotherapy and Oncology: Journal of the European Society for Therapeutic Radiology and Oncology, 57, 39–43.

99.

Rudat, V., Vanselow, B., Wollensack, P., Bettscheider, C., Osman-Ahmet, S., & Eble, M. J. (2000). Repeatability and prognostic impact of the pretreatment pO(2) histography in patients with advanced head and neck cancer. Radiotherapy and Oncology: Journal of the European Society for Therapeutic Radiology and Oncology, 57, 31–37.

100.

Padhani, A. R., Krohn, K. A., Lewis, J. S., & Alber, M. (2007). Imaging oxygenation of human tumours. European Radiology, 17, 861–872.PubMed

101.

Rischin, D., Hicks, R. J., Fisher, R., Binns, D., Corry, J., & Porceddu, S. (2006). Prognostic significance of [18F]-misonidazole positron emission tomography-detected tumor hypoxia in patients with advanced head and neck cancer randomly assigned to chemoradiation with or without tirapazamine: a substudy of Trans-Tasman Radiation Oncology Group Study 98.02. Journal of Clinical Oncology, 24, 2098–2104.PubMed

102.

Gagel, B., Reinartz, P., Demirel, C., Kaiser, H. J., Zimny, M., Piroth, M., et al. (2006). [18F] fluoromisonidazole and [18F] fluorodeoxyglucose positron emission tomography in response evaluation after chemo-/radiotherapy of non-small-cell lung cancer: a feasibility study. BMC Cancer, 6, 51.PubMed

103.

Cher, L. M., Murone, C., Lawrentschuk, N., Ramdave, S., Papenfuss, A., Hannah, A., et al. (2006). Correlation of hypoxic cell fraction and angiogenesis with glucose metabolic rate in gliomas using 18Ffluoromisonidazole, 18F-FDG PET, and immunohistochemical studies. Journal of Nuclear Medicine, 47, 410–418.PubMed

104.

Bruehlmeier, M., Roelcke, U., Schubiger, P. A., & Ametamey, S. M. (2004). Assessment of hypoxia and perfusion in human brain tumors using PET with 18F-fluoromisonidazole and 15O-H2O. Journal of Nuclear Medicine, 45, 1851–1859.PubMed

105.

Swietach, P., Vaughan-Jones, R. D., & Harris, A. L. (2007). Regulation of tumor pH and the role of carbonic anhydrase 9. Cancer and Metastasis Reviews, 26, 299–310.PubMed

106.

Steffens, M. G., Boerman, O. C., Oosterwijk-Wakka, J. C., Oosterhof, G. O., Witjes, J. A., Koenders, E. B., et al. (1997). Targeting of renal cell carcinoma with iodine-131-labeled chimeric monoclonal antibody G250. Journal of Clinical Oncology, 15, 1529–1537.PubMed

107.

Brouwers, A. H., Buijs, W. C., Oosterwijk, E., Boerman, O. C., Mala, C., & De Mulder, P. H. (2003). Targeting of metastatic renal cell carcinoma with the chimeric monoclonal antibody G250 labeled with (131)I or (111)In: an intrapatient comparison. Clinical Cancer Research, 9, 3953S–3960S.PubMed

108.

Steffens, M. G., Oosterwijk, E., Kranenborg, M. H., Manders, J. M., Debruyne, F. M., & Corstens, F. H. (1999). In vivo and in vitro characterizations of three 99mTc-labeled monoclonal antibody G250 preparations. Journal of Nuclear Medicine, 40, 829–836.PubMed

109.

Divgi, C. R., O’Donoghue, J. A., Welt, S., O’Neel, J., Finn, R., Motzer, R. J., et al. (2004). Phase I clinical trial with fractionated radioimmunotherapy using 131I-labeled chimeric G250 in metastatic renal cancer. Journal of Nuclear Medicine, 45, 1412–1421.PubMed

110.

Divgi, C. R., Pandit-Taskar, N., Jungbluth, A. A., Reuter, V. E., Gönen, M., Ruan, S., et al. (2007). Preoperative characterization of clear-cell renal carcinoma using iodine-124-labelled antibody chimeric G250 (124IcG250) and PET in patients with renal masses: a phase I trial. Lancet Oncology, 8, 304–310.PubMed

111.

Warburg, O. (1956). On the origin of cancer cells. Science, 123(3191), 309–314.PubMed

112.

Bos, R., van Der Hoeven, J. J., van Der Wall, E., van Der Groep, P., van Diest, P. J., Comans, E., et al. (2002). Biologic correlates of (18)fluorodeoxyglucose uptake in human breast cancer measured by positron emission tomography. Journal of Clinical Oncology, 20(2), 379–387.PubMed

113.

Zasadny, K. R., Tatsumi, M., & Wahl, R. L. (2003). FDG metabolism and uptake versus blood flow in women with untreated primary breast cancers. European Journal of Nuclear Medicine Molecular Imaging, 30(2), 274–280.

114.

Li, K., Wilmes, L. J., Henry, R. G., Pallavicini, M. G., Park, J. W., Hu-Lowe, D. D., et al. (2005). 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. Journal of Magnetic Resonance Imaging, 22, 511–519.PubMed

115.

Jayson, G. C., Zweit, J., Jackson, A., Mulatero, C., Julyan, P. J., Ranson, M., et al. (2002). Molecular imaging and biological evaluation of HuMV833 anti-VEGF antibody: implications for trial design of antiangiogenic antibodies. Journal of the National Cancer Institute, 24(19), 1484–1493.

116.

Cai, W., Chen, K., Mohamedali, K. A., Cao, Q., Gambhir, S. S., & Rosenblum, M. G. (2006). PET of vascular endothelial growth factor receptor expression. Journal of Nuclear Medicine, 47(12), 2048–2056.PubMed

117.

Hsu, A. R., Cai, W., Veeravagu, A., Mohamedali, K. A., Chen, K., Kim, S., et al. (2007). Multimodality molecular imaging of glioblastoma growth inhibition with vasculature-targeting fusion toxin VEGF121/rGel. Journal of Nuclear Medicine, 48(3), 445–454.PubMed

118.

Collingridge, D. R., Carroll, V. A., Glaser, M., Aboagye, E. O., Osman, S., Hutchinson, O. C., et al. (2002). The development of [(124)I]iodinated-VG76e: a novel tracer for imaging vascular endothelial growth factor in vivo using positron emission tomography. Cancer Research, 62, 5912–5919.PubMed

119.

Sivolapenko, G. B., Skarlos, D., Pectasides, D., Stathopoulou, E., Milonakis, A., & Sirmalis, G. (1998). Imaging of metastatic melanoma utilising a technetium-99m labelled RGD-containing synthetic peptide. European Journal of Nuclear Medicine, 25(10), 1383–1389.PubMed

120.

Haubner, R., Wester, H. J., Weber, W. A., Mang, C., Ziegler, S. I., & Goodman, S. L. (2001). Noninvasive imaging of alpha(v)beta3 integrin expression using 18F-labeled RGD-containing glycopeptide and positron emission tomography. Cancer Research, 61, 1781–1785.PubMed

121.

Beer, A. J., Haubner, R., Sarbia, M., Goebel, M., Luderschmidt, S., Grosu, A. L., et al. (2006). Positron emission tomography using [18F]Galacto-RGD identifies the level of integrin alpha(v)beta3 expression in man. Clinical Cancer Research, 12(13), 3942–3949.PubMed

122.

Chen, X., Park, R., Khankaldyyan, V., Gonzales-Gomez, I., Tohme, M., & Moats, R. A. (2006). Longitudinal microPET imaging of brain tumor growth with F-18-labeled RGD peptide. Molecular Imaging and Biology, 8(1), 9–15.PubMed

123.

Jung, K. H., Lee, K. H., Paik, J. Y., Ko, B. H., Bae, J. S., & Lee, B. C. (2006). Favorable biokinetic and tumor-targeting properties of 99mTc-labeled glucosamino RGD and effect of paclitaxel therapy. Journal of Nuclear Medicine, 47(12), 2000–2007.

124.

Meyerowitz, C. B., Fleischer, A. C., Pickens, D. R., Thurman, G. B., Borowsky, A. D., & Thirsk, G. (1996). Quantification of tumor vascularity and flow with amplitude color Doppler sonography in an experimental model: preliminary results.[erratum appears in J Ultrasound Med 1997 Mar;16(3):218]. Journal of Ultrasound Medicine, 15, 827–833.

125.

Arger, P. H., Malkowicz, S. B., VanArsdalen, K. N., Sehgal, C. M., Holzer, A., & Schultz, S. M. (2004). Color and power Doppler sonography in the diagnosis of prostate cancer: comparison between vascular density and total vascularity. Journal of Ultrasound in Medicine, 23, 623–630.PubMed

126.

Yang, W. T., Tse, G. M. K., Lam, P. K. W., Metreweli, C., & Chang, J. (2002). Correlation between color power Doppler sonographic measurement of breast tumor vasculature and immunohistochemical analysis of microvessel density for the quantitation of angiogenesis. Journal Ultrasound in Medicine, 21, 1227–1235.

127.

Ferrara, K. W., Merritt, C. R., Burns, P. N., Foster, F. S., Mattrey, R. F., & Wickline, S. A. (2000). Evaluation of tumor angiogenesis with US: imaging, Doppler, and contrast agents. Academic Radiology, 7, 824–839.PubMed

128.

Sehgal, C. M., Arger, P. H., Rowling, S. E., Conant, E. F., Reynolds, C., & Patton, J. A. (2000). Quantitative vascularity of breast masses by Doppler imaging: regional variations and diagnostic implications. Journal of Ultrasound Medicine, 19, 427–440 quiz 441–422.

129.

Wood, A. K. W., Ansaloni, S., Ziemer, L. S., Lee, W. M. F., Feldman, M. D., & Sehgal, C. M. (2005). The antivascular action of physiotherapy ultrasound on murine tumors. Ultrasound in Medicine Biology, 31, 1403–1410.PubMed

130.

Kamotani, Y., Lee, W. M. F., Arger, P. H., Cary, T. W., & Sehgal, C. M. (2003). Multigated contrast-enhanced power Doppler to measure blood flow in mice tumors. Ultrasound in Medicine Biology, 29, 977–984.PubMed

131.

Bertolotto, M., Pozzato, G., Croce, L. S., Nascimben, F., Gasparini, C., & Cova, M. A. (2006). Blood flow changes in hepatocellular carcinoma after the administration of thalidomide assessed by reperfusion kinetics during microbubble infusion: preliminary results. Investigative Radiology, 41, 15–21.PubMed

132.

McCarville, M. B., Streck, C. J., Dickson, P. V., Li, C.-S., Nathwani, A. C., & Davidoff, A. M. (2006). Angiogenesis inhibitors in a murine neuroblastoma model: quantitative assessment of intratumoral blood flow with contrast-enhanced gray-scale US.[see comment]. Radiology, 240, 73–81.PubMed

133.

Thomas, J. P., Arzoomanian, R. Z., Alberti, D., Marnocha, R., Lee, F., Friedl, A., et al. (2003). Phase I pharmacokinetic and pharmacodynamic study of recombinant human endostatin in patients with advanced solid tumors. Journal of Clinical Oncology, 21, 223–231.PubMed

134.

Hsu, C., Chen, C. N., Chen, L. T., Wu, C. Y., Hsieh, F. J., & Cheng, A. L. (2005). Effect of thalidomide in hepatocellular carcinoma: assessment with power Doppler US and analysis of circulating angiogenic factors. Radiology, 235, 509–516.PubMed

135.

Yodh, A. G., & Chance, B. (1995). Spectroscopy and imaging with diffusing light. Physics Today, 48, 34–40.

136.

Yodh, A. G., & Boas, D. (2003). Functional imaging with diffusing light. Biomedical Photonics Handbook, 21(1), 21–45.

137.

Intes, X., Ripoll, J., Chen, Y., Nioka, S., Yodh, A. G., & Chance, B. (2003). In vivo continuous-wave optical breast imaging enhanced with Indocyanine Green. Medical Physics, 30, 1039–1047.PubMed

138.

Ntziachristos, V., Yodh, A. G., Schnall, M. D., & Chance, B. (2000). Concurrent MRI and diffuse optical tomography of breast after indocyanine green enhancement. Proceedings of the National Academy of Sciences of the United States of America, 97(6), 2767–2772.PubMed

139.

Corlu, A., Choe, R., Durduran, T., Rosen, M. A., Schweiger, M., & Arridge, S. R. (2007). Three-dimensional in vivo fluorescence diffuse optical tomography of breast cancer in humans. Optics Express, 15(11), 1–21.

140.

Jakubowski, D. B., Cerussi, A. E., Bevilacqua, F., Shah, N., Hsiang, D., & Butler, J. (2004). Monitoring neoadjuvant chemotherapy in breast cancer using quantitative diffuse optical spectroscopy: a case study. Journal of Biomedical Optics, 9(1), 230–238.PubMed

141.

Choe, R., Corlu, A., Lee, K., Durduran, T., Konecky, S. D., Grosicka-Koptyra, M., et al. (2005). Diffuse optical tomography of breast cancer during neoadjuvant chemotherapy: a case study with comparison to MRI. Medical Physics, 32(4), 1128–1139.PubMed

142.

Zhu, Q., Kurtzma, S. H., Hegde, P., Tannenbaum, S., Kane, M., Huang, M., et al. (2005). Utilizing optical tomography with ultrasound localization to image heterogeneous hemoglobin distribution in large breast cancers. Neoplasia, 7(3), 263–270.

143.

Cerussi, A. E., Hsiang, D., Shah, N., Mehta, R., Durkin, A., & Butler, J. (2007). Predicting response to breast cancer neoadjuvant chemotherapy using diffuse optical spectroscopy. Proceeding of the National Academy Science USA, 104(10), 4014–4019.

144.

Zhou, C., Choe, R., Shah, N., Durduran, T., Yu, G., Durkin, A., et al. (2007). Diffuse optical monitoring of blood flow and oxygenation in human breast cancer during early stages of neoadjuvant chemotherapy. Journal of Biomedical Optics, 12, 051903.PubMed

145.

Sunar, U., Quon, H., Durduran, T., Zhang, J., Du, J., Zhou, C., et al. (2006). Noninvasive diffuse optical measurement of blood flow and blood oxygenation for monitoring radiation therapy in patients with head and neck tumors: a pilot study. Journal of Biomedical Optics, 11(6), 064021.PubMed

146.

Yu, G., Durduran, T., Zhou, C., Zhu, T. C., Finlay, J. C., & Busch, T. M. (2006). Real-time in situ monitoring of human prostate photodynamic therapy with diffuse light. Photochemistry and Photobiology, 82(5), 1279–1284.PubMed

147.

Sunar, U., Makonnen, S., Zhou, C., Durduran, T., Yu, G., Wang, H., et al. (2007). Hemodynamic responses to antivascular therapy and ionizing radiation assessed by diffuse optical spectroscopies. Optics Express, 15, 15507–15516.

Title: Non-invasive assessment of tumor neovasculature: techniques and clinical applications
Authors: Rodolfo Perini
Regine Choe
Arjun G. Yodh
Chandra Sehgal
Chaitanya R. Divgi
Mark A. Rosen
Publication date: 01-12-2008
Publisher: Springer US
Published in: Cancer and Metastasis Reviews / Issue 4/2008
Print ISSN: 0167-7659
Electronic ISSN: 1573-7233
DOI: https://doi.org/10.1007/s10555-008-9147-6

Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Watch now

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras

Prof. Fabrice Barlesi

Developed by: Springer Medicine

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4/2008

The role of DNA synthesis imaging in cancer in the era of targeted therapeutics

Imaging matrix metalloproteinases in cancer

Molecular profiling of uterine cervix carcinoma: an overview with a special focus on rationally designed target-based anticancer agents

Molecular imaging of epidermal growth factor receptor expression–activity at the kinase level in tumors with positron emission tomography

Preface-imaging in cancer

Cell cycle control and adhesion signaling pathways in the development of metastatic melanoma

Keynote webinar | Spotlight on antibody–drug conjugates in cancer