Angiogenesis

, Volume 13, Issue 2, pp 149–160 | Cite as

Non-invasive imaging of angiogenesis in head and neck squamous cell carcinoma

  • Jacobus F. A. Jansen
  • Jason A. Koutcher
  • Amita Shukla-Dave
Article

Abstract

Squamous cell carcinoma of the head and neck (HNSCC) is the seventh most common cancer in the United States. Angiogenesis, the process by which new blood vessels are formed, is an essential element at the basis of both tumor growth and metastases. This review discusses pertinent aspects of the role of imaging modalities in assessing angiogenesis and anti-angiogenic therapy in advanced HNSCC.

Keywords

Head and neck squamous cell carcinoma Angiogenesis Anti-angiogenic treatment Imaging techniques Magnetic resonance imaging Computed tomography Positron emission tomography Ultrasound Molecular imaging 

Notes

Acknowledgments

We thank Ms. Ada Muellner (B.A.) for editing the manuscript and Dr Diane Carlson (Dept of Pathology) for molecular pathology data on surgical specimens. The work from MSKCC reported in this review was supported by the National Cancer Institute/National Institutes of Health (grant number 1 R01 CA115895).

References

  1. 1.
    Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ (2009) Cancer statistics, 2009. CA Cancer J Clin 59:225–249CrossRefPubMedGoogle Scholar
  2. 2.
    Vokes EE, Weichselbaum RR, Lippman SM, Hong WK (1993) Head and neck cancer. N Engl J Med 328:184–194CrossRefPubMedGoogle Scholar
  3. 3.
    Klem ML, Mechalakos JG, Wolden SL, Zelefsky MJ, Singh B, Kraus D, Shaha A, Shah J, Pfister DG, Lee NY (2008) Intensity-modulated radiotherapy for head and neck cancer of unknown primary: toxicity and preliminary efficacy. Int J Radiat Oncol Biol Phys 70:1100–1107PubMedGoogle Scholar
  4. 4.
    Lee NY, O’Meara W, Chan K, Della-Bianca C, Mechalakos JG, Zhung J, Wolden SL, Narayana A, Kraus D, Shah JP, Pfister DG (2007) Concurrent chemotherapy and intensity-modulated radiotherapy for locoregionally advanced laryngeal and hypopharyngeal cancers. Int J Radiat Oncol Biol Phys 69:459–468PubMedGoogle Scholar
  5. 5.
    Schwartz LH, Ozsahin M, Zhang GN, Touboul E, De Vataire F, Andolenko P, Lacau-Saint-Guily J, Laugier A, Schlienger M (1994) Synchronous and metachronous head and neck carcinomas. Cancer 74:1933–1938CrossRefPubMedGoogle Scholar
  6. 6.
    Day GL, Blot WJ (1992) Second primary tumors in patients with oral cancer. Cancer 70:14–19CrossRefPubMedGoogle Scholar
  7. 7.
    Carmeliet P, Jain RK (2000) Angiogenesis in cancer and other diseases. Nature 407:249–257CrossRefPubMedGoogle Scholar
  8. 8.
    Seiwert TY, Cohen EE (2008) Targeting angiogenesis in head and neck cancer. Semin Oncol 35:274–285CrossRefPubMedGoogle Scholar
  9. 9.
    Palka KT, Slebos RJ, Chung CH (2008) Update on molecular diagnostic tests in head and neck cancer. Semin Oncol 35:198–210CrossRefPubMedGoogle Scholar
  10. 10.
    Weidner N, Folkman J, Pozza F, Bevilacqua P, Allred EN, Moore DH, Meli S, Gasparini G (1992) Tumor angiogenesis: a new significant and independent prognostic indicator in early-stage breast carcinoma. J Natl Cancer Inst 84:1875–1887CrossRefPubMedGoogle Scholar
  11. 11.
    Mendiola M, Barriuso J, Redondo A, Marino-Enriquez A, Madero R, Espinosa E, Vara JA, Sanchez-Navarro I, Hernandez-Cortes G, Zamora P, Perez-Fernandez E, Miguel-Martin M, Suarez A, Palacios J, Gonzalez-Baron M, Hardisson D (2008) Angiogenesis-related gene expression profile with independent prognostic value in advanced ovarian carcinoma. PLoS One 3:e4051CrossRefPubMedGoogle Scholar
  12. 12.
    Angeletti CA, Lucchi M, Fontanini G, Mussi A, Chella A, Ribechini A, Vignati S, Bevilacqua G (1996) Prognostic significance of tumoral angiogenesis in completely resected late stage lung carcinoma (stage IIIA-N2). Impact of adjuvant therapies in a subset of patients at high risk of recurrence. Cancer 78:409–415CrossRefPubMedGoogle Scholar
  13. 13.
    Ito Y, Kamijo T, Yokose T, Kawashima M, Ogino T, Ikeda H, Hayashi R, Sasaki S, Ochiai A (2001) Microvessel density predicts the radiosensitivity of metastatic head and neck squamous cell carcinoma in cervical lymph nodes. Int J Oncol 19:1127–1132PubMedGoogle Scholar
  14. 14.
    Sauter ER, Nesbit M, Watson JC, Klein-Szanto A, Litwin S, Herlyn M (1999) Vascular endothelial growth factor is a marker of tumor invasion and metastasis in squamous cell carcinomas of the head and neck. Clin Cancer Res 5:775–782PubMedGoogle Scholar
  15. 15.
    Pignataro L, Carboni N, Midolo V, Bertolini F, Buffa R, Cesana BM, Neri A, Viale G, Pruneri G (2001) Clinical relevance of microvessel density in laryngeal squamous cell carcinomas. Int J Cancer 92:666–670CrossRefPubMedGoogle Scholar
  16. 16.
    Jain RK, Duda DG, Willett CG, Sahani DV, Zhu AX, Loeffler JS, Batchelor TT, Sorensen AG (2009) Biomarkers of response and resistance to antiangiogenic therapy. Nat Rev Clin Oncol 6:327–338CrossRefPubMedGoogle Scholar
  17. 17.
    Turkbey B, Kobayashi H, Ogawa M, Bernardo M, Choyke PL (2009) Imaging of tumor angiogenesis: functional or targeted? AJR Am J Roentgenol 193:304–313CrossRefPubMedGoogle Scholar
  18. 18.
    Charnley N, Donaldson S, Price P (2009) Imaging angiogenesis. Methods Mol Biol 467:25–51CrossRefPubMedGoogle Scholar
  19. 19.
    Faggioni L, Neri E, Bartolozzi C (2010) CT perfusion of head and neck tumors: how we do it. AJR Am J Roentgenol 194:62–69CrossRefPubMedGoogle Scholar
  20. 20.
    Aksoy FG, Lev MH (2000) Dynamic contrast-enhanced brain perfusion imaging: technique and clinical applications. Semin Ultrasound CT MR 21:462–477CrossRefPubMedGoogle Scholar
  21. 21.
    Shah GV, Wesolowski JR, Ansari SA, Mukherji SK (2008) New directions in head and neck imaging. J Surg Oncol 97:644–648CrossRefPubMedGoogle Scholar
  22. 22.
    Gandhi D, Hoeffner EG, Carlos RC, Case I, Mukherji SK (2003) Computed tomography perfusion of squamous cell carcinoma of the upper aerodigestive tract. Initial results. J Comput Assist Tomogr 27:687–693CrossRefPubMedGoogle Scholar
  23. 23.
    Hermans R, Meijerink M, Van den Bogaert W, Rijnders A, Weltens C, Lambin P (2003) Tumor perfusion rate determined noninvasively by dynamic computed tomography predicts outcome in head-and-neck cancer after radiotherapy. Int J Radiat Oncol Biol Phys 57:1351–1356PubMedGoogle Scholar
  24. 24.
    Gandhi D, Chepeha DB, Miller T, Carlos RC, Bradford CR, Karamchandani R, Worden F, Eisbruch A, Teknos TN, Wolf GT, Mukherji SK (2006) Correlation between initial and early follow-up CT perfusion parameters with endoscopic tumor response in patients with advanced squamous cell carcinomas of the oropharynx treated with organ-preservation therapy. AJNR Am J Neuroradiol 27:101–106PubMedGoogle Scholar
  25. 25.
    Zima A, Carlos R, Gandhi D, Case I, Teknos T, Mukherji SK (2007) Can pretreatment CT perfusion predict response of advanced squamous cell carcinoma of the upper aerodigestive tract treated with induction chemotherapy? AJNR Am J Neuroradiol 28:328–334PubMedGoogle Scholar
  26. 26.
    Ash L, Teknos TN, Gandhi D, Patel S, Mukherji SK (2009) Head and neck squamous cell carcinoma: CT perfusion can help noninvasively predict intratumoral microvessel density. Radiology 251:422–428CrossRefPubMedGoogle Scholar
  27. 27.
    Hylton N (2006) Dynamic contrast-enhanced magnetic resonance imaging as an imaging biomarker. J Clin Oncol 24:3293–3298CrossRefPubMedGoogle Scholar
  28. 28.
    Yankeelov TE, Gore JC (2007) Dynamic contrast enhanced magnetic resonance imaging in oncology: theory, data acquisition, analysis and examples. Curr Med Imaging Rev 3:91–107CrossRefGoogle Scholar
  29. 29.
    Konouchi H, Asaumi J, Yanagi Y, Shigehara H, Hisatomi M, Matsuzaki H, Kishi K (2003) Evaluation of tumor proliferation using dynamic contrast enhanced-MRI of oral cavity and oropharyngeal squamous cell carcinoma. Oral Oncol 39:290–295CrossRefPubMedGoogle Scholar
  30. 30.
    Hoskin PJ, Saunders MI, Goodchild K, Powell ME, Taylor NJ, Baddeley H (1999) Dynamic contrast enhanced magnetic resonance scanning as a predictor of response to accelerated radiotherapy for advanced head and neck cancer. Br J Radiol 72:1093–1098PubMedGoogle Scholar
  31. 31.
    Cao Y, Popovtzer A, Li D, Chepeha DB, Moyer JS, Prince ME, Worden F, Teknos T, Bradford C, Mukherji SK, Eisbruch A (2008) Early prediction of outcome in advanced head-and-neck cancer based on tumor blood volume alterations during therapy: a prospective study. Int J Radiat Oncol Biol Phys 72:1287–1290PubMedGoogle Scholar
  32. 32.
    Kim S, Loevner LA, Quon H, Kilger A, Sherman E, Weinstein G, Chalian A, Poptani H (2010) Prediction of response to chemoradiation therapy in squamous cell carcinomas of the head and neck using dynamic contrast-enhanced MR imaging. AJNR Am J Neuroradiol 31:262–268CrossRefPubMedGoogle Scholar
  33. 33.
    Koh DM, Collins DJ (2007) Diffusion-weighted MRI in the body: applications and challenges in oncology. AJR Am J Roentgenol 188:1622–1635CrossRefPubMedGoogle Scholar
  34. 34.
    Abdel Razek AA, Gaballa G, Elhawarey G, Megahed AS, Hafez M, Nada N (2009) Characterization of pediatric head and neck masses with diffusion-weighted MR imaging. Eur Radiol 19:201–208CrossRefPubMedGoogle Scholar
  35. 35.
    Wang J, Takashima S, Takayama F, Kawakami S, Saito A, Matsushita T, Momose M, Ishiyama T (2001) Head and neck lesions: characterization with diffusion-weighted echo-planar MR imaging. Radiology 220:621–630CrossRefPubMedGoogle Scholar
  36. 36.
    Sumi M, Nakamura T (2009) Diagnostic importance of focal defects in the apparent diffusion coefficient-based differentiation between lymphoma and squamous cell carcinoma nodes in the neck. Eur Radiol 19:975–981CrossRefPubMedGoogle Scholar
  37. 37.
    Abdel Razek AA, Megahed AS, Denewer A, Motamed A, Tawfik A, Nada N (2008) Role of diffusion-weighted magnetic resonance imaging in differentiation between the viable and necrotic parts of head and neck tumors. Acta Radiol 49:364–370CrossRefGoogle Scholar
  38. 38.
    Vandecaveye V, de Keyzer F, Vander Poorten V, Deraedt K, Alaerts H, Landuyt W, Nuyts S, Hermans R (2006) Evaluation of the larynx for tumour recurrence by diffusion-weighted MRI after radiotherapy: initial experience in four cases. Br J Radiol 79:681–687CrossRefPubMedGoogle Scholar
  39. 39.
    Maeda M, Kato H, Sakuma H, Maier SE, Takeda K (2005) Usefulness of the apparent diffusion coefficient in line scan diffusion-weighted imaging for distinguishing between squamous cell carcinomas and malignant lymphomas of the head and neck. AJNR Am J Neuroradiol 26:1186–1192PubMedGoogle Scholar
  40. 40.
    Srinivasan A, Dvorak R, Perni K, Rohrer S, Mukherji SK (2008) Differentiation of benign and malignant pathology in the head and neck using 3T apparent diffusion coefficient values: early experience. AJNR Am J Neuroradiol 29:40–44CrossRefPubMedGoogle Scholar
  41. 41.
    Jansen JF, Stambuk HE, Koutcher JA, Shukla-Dave A (2009) Non-Gaussian analysis of diffusion-weighted MR imaging in head and neck squamous cell carcinoma: a feasibility study. AJNR Am J Neuroradiol. doi: 10.3174/ajnr.A1919 Google Scholar
  42. 42.
    Koh DM, Blackledge M, Collins DJ, Padhani AR, Wallace T, Wilton B, Taylor NJ, Stirling JJ, Sinha R, Walicke P, Leach MO, Judson I, Nathan P (2009) Reproducibility and changes in the apparent diffusion coefficients of solid tumours treated with combretastatin A4 phosphate and bevacizumab in a two-centre phase I clinical trial. Eur Radiol 19:2728–2738CrossRefPubMedGoogle Scholar
  43. 43.
    Liu JG, Wang B, Wang XZ, Niu QL, Zhang Q (2009) Diffusion weighted MRI helps evaluate angiogenesis and vascular endothelial growth factor expression in prostate cancer. Zhonghua Nan Ke Xue 15:403–408PubMedGoogle Scholar
  44. 44.
    Dirix P, De Keyzer F, Vandecaveye V, Stroobants S, Hermans R, Nuyts S (2008) Diffusion-weighted magnetic resonance imaging to evaluate major salivary gland function before and after radiotherapy. Int J Radiat Oncol Biol Phys 71:1365–1371PubMedGoogle Scholar
  45. 45.
    Kim S, Loevner L, Quon H, Sherman E, Weinstein G, Kilger A, Poptani H (2009) Diffusion-weighted magnetic resonance imaging for predicting and detecting early response to chemoradiation therapy of squamous cell carcinomas of the head and neck. Clin Cancer Res 15:986–994CrossRefPubMedGoogle Scholar
  46. 46.
    Galban CJ, Mukherji SK, Chenevert TL, Meyer CR, Hamstra DA, Bland PH, Johnson TD, Moffat BA, Rehemtulla A, Eisbruch A, Ross BD (2009) A feasibility study of parametric response map analysis of diffusion-weighted magnetic resonance imaging scans of head and neck cancer patients for providing early detection of therapeutic efficacy. Transl Oncol 2:184–190PubMedGoogle Scholar
  47. 47.
    Jansen JF, Backes WH, Nicolay K, Kooi ME (2006) 1H MR spectroscopy of the brain: absolute quantification of metabolites. Radiology 240:318–332CrossRefPubMedGoogle Scholar
  48. 48.
    Shah GV, Gandhi D, Mukherji SK (2004) Magnetic resonance spectroscopy of head and neck neoplasms. Top Magn Reson Imaging 15:87–94CrossRefPubMedGoogle Scholar
  49. 49.
    Thakur SB, Yaligar J, Koutcher JA (2009) In vivo lactate signal enhancement using binomial spectral-selective pulses in selective MQ coherence (SS-SelMQC) spectroscopy. Magn Reson Med 62:591–598CrossRefPubMedGoogle Scholar
  50. 50.
    Chawla S, Kim S, Loevner LA, Quon H, Wang S, Mutale F, Weinstein G, Delikatny EJ, Poptani H (2009) Proton and phosphorous MR spectroscopy in squamous cell carcinomas of the head and neck. Acad Radiol 16:1366–1372CrossRefPubMedGoogle Scholar
  51. 51.
    Shukla-Dave A, Poptani H, Loevner LA, Mancuso A, Serrai H, Rosenthal DI, Kilger AM, Nelson DS, Zakian KL, Arias-Mendoza F, Rijpkema M, Koutcher JA, Brown TR, Heerschap A, Glickson JD (2002) Prediction of treatment response of head and neck cancers with P-31 MR spectroscopy from pretreatment relative phosphomonoester levels. Acad Radiol 9:688–694CrossRefPubMedGoogle Scholar
  52. 52.
    Aboagye EO, Bhujwalla ZM (1999) Malignant transformation alters membrane choline phospholipid metabolism of human mammary epithelial cells. Cancer Res 59:80–84PubMedGoogle Scholar
  53. 53.
    Star-Lack J, Spielman D, Adalsteinsson E, Kurhanewicz J, Terris DJ, Vigneron DB (1998) In vivo lactate editing with simultaneous detection of choline, creatine, NAA, and lipid singlets at 1.5 T using PRESS excitation with applications to the study of brain and head and neck tumors. J Magn Reson 133:243–254CrossRefPubMedGoogle Scholar
  54. 54.
    Star-Lack JM, Adalsteinsson E, Adam MF, Terris DJ, Pinto HA, Brown JM, Spielman DM (2000) In vivo 1H MR spectroscopy of human head and neck lymph node metastasis and comparison with oxygen tension measurements. AJNR Am J Neuroradiol 21:183–193PubMedGoogle Scholar
  55. 55.
    Schoder H, Fury M, Lee N, Kraus D (2009) PET monitoring of therapy response in head and neck squamous cell carcinoma. J Nucl Med 50(Suppl 1):74S–88SCrossRefPubMedGoogle Scholar
  56. 56.
    Beer AJ, Haubner R, Wolf I, Goebel M, Luderschmidt S, Niemeyer M, Grosu AL, Martinez MJ, Wester HJ, Weber WA, Schwaiger M (2006) PET-based human dosimetry of 18F-galacto-RGD, a new radiotracer for imaging alpha v beta3 expression. J Nucl Med 47:763–769PubMedGoogle Scholar
  57. 57.
    Beer AJ, Grosu AL, Carlsen J, Kolk A, Sarbia M, Stangier I, Watzlowik P, Wester HJ, Haubner R, Schwaiger M (2007) [18F]galacto-RGD positron emission tomography for imaging of alphavbeta3 expression on the neovasculature in patients with squamous cell carcinoma of the head and neck. Clin Cancer Res 13:6610–6616CrossRefPubMedGoogle Scholar
  58. 58.
    Lee NY, Mechalakos JG, Nehmeh S, Lin Z, Squire OD, Cai S, Chan K, Zanzonico PB, Greco C, Ling CC, Humm JL, Schoder H (2008) Fluorine-18-labeled fluoromisonidazole positron emission and computed tomography-guided intensity-modulated radiotherapy for head and neck cancer: a feasibility study. Int J Radiat Oncol Biol Phys 70:2–13PubMedGoogle Scholar
  59. 59.
    Rasey JS, Koh WJ, Evans ML, Peterson LM, Lewellen TK, Graham MM, Krohn KA (1996) Quantifying regional hypoxia in human tumors with positron emission tomography of [18F]fluoromisonidazole: a pretherapy study of 37 patients. Int J Radiat Oncol Biol Phys 36:417–428PubMedGoogle Scholar
  60. 60.
    Brizel DM, Dodge RK, Clough RW, Dewhirst MW (1999) Oxygenation of head and neck cancer: changes during radiotherapy and impact on treatment outcome. Radiother Oncol 53:113–117CrossRefPubMedGoogle Scholar
  61. 61.
    Nordsmark M, Bentzen SM, Rudat V, Brizel D, Lartigau E, Stadler P, Becker A, Adam M, Molls M, Dunst J, Terris DJ, Overgaard J (2005) Prognostic value of tumor oxygenation in 397 head and neck tumors after primary radiation therapy. An international multi-center study. Radiother Oncol 77:18–24CrossRefPubMedGoogle Scholar
  62. 62.
    Jansen JF, Schöder H, Lee NY, Wang Y, Pfister DG, Fury MG, Stambuk HE, Humm JL, Koutcher JA, Shukla-Dave A (2009) Noninvasive assessment of tumor microenvironment using dynamic contrast-enhanced magnetic resonance imaging and (18)F-fluoromisonidazole positron emission tomography imaging in neck nodal metastases. Int J Radiat Oncol Biol Phys. doi: 10.1016/j.ijrobp.2009.07.009 Google Scholar
  63. 63.
    Barthel H, Cleij MC, Collingridge DR, Hutchinson OC, Osman S, He Q, Luthra SK, Brady F, Price PM, Aboagye EO (2003) 3′-deoxy-3′-[18F]fluorothymidine as a new marker for monitoring tumor response to antiproliferative therapy in vivo with positron emission tomography. Cancer Res 63:3791–3798PubMedGoogle Scholar
  64. 64.
    Cobben DC, van der Laan BF, Maas B, Vaalburg W, Suurmeijer AJ, Hoekstra HJ, Jager PL, Elsinga PH (2004) 18F-FLT PET for visualization of laryngeal cancer: comparison with 18F-FDG PET. J Nucl Med 45:226–231PubMedGoogle Scholar
  65. 65.
    Linecker A, Kermer C, Sulzbacher I, Angelberger P, Kletter K, Dudczak R, Ewers R, Becherer A (2008) Uptake of (18)F-FLT and (18)F-FDG in primary head and neck cancer correlates with survival. Nuklearmedizin 47:80–85 (quiz N12)PubMedGoogle Scholar
  66. 66.
    Richards PS, Peacock TE (2007) The role of ultrasound in the detection of cervical lymph node metastases in clinically N0 squamous cell carcinoma of the head and neck. Cancer Imaging 7:167–178CrossRefPubMedGoogle Scholar
  67. 67.
    Jacob A, Varghese BE, Birchall MB (2006) Validation of laser Doppler fluxmetry as a method of assessing neo-angiogenesis in laryngeal tumours. Eur Arch Otorhinolaryngol 263:444–448CrossRefPubMedGoogle Scholar
  68. 68.
    Massoud TF, Gambhir SS (2003) Molecular imaging in living subjects: seeing fundamental biological processes in a new light. Genes Dev 17:545–580CrossRefPubMedGoogle Scholar
  69. 69.
    Weissleder R, Mahmood U (2001) Molecular imaging. Radiology 219:316–333PubMedGoogle Scholar
  70. 70.
    Winnard P Jr, Raman V (2003) Real time non-invasive imaging of receptor-ligand interactions in vivo. J Cell Biochem 90:454–463CrossRefPubMedGoogle Scholar
  71. 71.
    Daniels TR, Delgado T, Helguera G, Penichet ML (2006) The transferrin receptor part II: targeted delivery of therapeutic agents into cancer cells. Clin Immunol 121:159–176CrossRefPubMedGoogle Scholar
  72. 72.
    Kearsley JH, Furlong KL, Cooke RA, Waters MJ (1990) An immunohistochemical assessment of cellular proliferation markers in head and neck squamous cell cancers. Br J Cancer 61:821–827PubMedGoogle Scholar
  73. 73.
    Shan L, Hao Y, Wang S, Korotcov A, Zhang R, Wang T, Califano J, Gu X, Sridhar R, Bhujwalla ZM, Wang PC (2008) Visualizing head and neck tumors in vivo using near-infrared fluorescent transferrin conjugate. Mol Imaging 7:42–49PubMedGoogle Scholar
  74. 74.
    Liu Y, Miyoshi H, Nakamura M (2007) Nanomedicine for drug delivery and imaging: a promising avenue for cancer therapy and diagnosis using targeted functional nanoparticles. Int J Cancer 120:2527–2537CrossRefPubMedGoogle Scholar
  75. 75.
    Cai W, Chen X (2008) Multimodality molecular imaging of tumor angiogenesis. J Nucl Med 49(Suppl 2):113S–128SCrossRefPubMedGoogle Scholar
  76. 76.
    Cognetti DM, Weber RS, Lai SY (2008) Head and neck cancer: an evolving treatment paradigm. Cancer 113:1911–1932CrossRefPubMedGoogle Scholar
  77. 77.
    Machiels JP, Henry S, Zanetta S, Kaminsky MC, Michoux N, Rommel D, Schmitz S, Bompas E, Dillies AF, Faivre S, Moxhon A, Duprez T, Guigay J (2010) Phase II study of sunitinib in recurrent or metastatic squamous cell carcinoma of the head and neck: GORTEC 2006–01. J Clin Oncol 28:21–28CrossRefPubMedGoogle Scholar
  78. 78.
    Fury MG, Zahalsky A, Wong R, Venkatraman E, Lis E, Hann L, Aliff T, Gerald W, Fleisher M, Pfister DG (2007) A phase II study of SU5416 in patients with advanced or recurrent head and neck cancers. Invest New Drugs 25:165–172CrossRefPubMedGoogle Scholar
  79. 79.
    Gerstner ER, Duda DG, di Tomaso E, Ryg PA, Loeffler JS, Sorensen AG, Ivy P, Jain RK, Batchelor TT (2009) VEGF inhibitors in the treatment of cerebral edema in patients with brain cancer. Nat Rev Clin Oncol 6:229–236CrossRefPubMedGoogle Scholar
  80. 80.
    Zhang XM, Yu D, Zhang HL, Dai Y, Bi D, Liu Z, Prince MR, Li C (2008) 3D dynamic contrast-enhanced MRI of rectal carcinoma at 3T: correlation with microvascular density and vascular endothelial growth factor markers of tumor angiogenesis. J Magn Reson Imaging 27:1309–1316CrossRefPubMedGoogle Scholar
  81. 81.
    Shiyan L, Pintong H, Zongmin W, Fuguang H, Zhiqiang Z, Yan Y, Cosgrove D (2009) The relationship between enhanced intensity and microvessel density of gastric carcinoma using double contrast-enhanced ultrasonography. Ultrasound Med Biol 35:1086–1091CrossRefPubMedGoogle Scholar
  82. 82.
    Guo J, Higashi K, Ueda Y, Oguchi M, Takegami T, Toga H, Sakuma T, Yokota H, Katsuda S, Tonami H, Yamamoto I (2006) Microvessel density: correlation with 18F-FDG uptake and prognostic impact in lung adenocarcinomas. J Nucl Med 47:419–425PubMedGoogle Scholar
  83. 83.
    Lawrentschuk N, Poon AM, Foo SS, Putra LG, Murone C, Davis ID, Bolton DM, Scott AM (2005) Assessing regional hypoxia in human renal tumours using 18F-fluoromisonidazole positron emission tomography. BJU Int 96:540–546CrossRefPubMedGoogle Scholar
  84. 84.
    Jain RK (2005) Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 307:58–62CrossRefPubMedGoogle Scholar
  85. 85.
    Oostendorp M, Post MJ, Backes WH (2009) Vessel growth and function: depiction with contrast-enhanced MR imaging. Radiology 251:317–335CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Jacobus F. A. Jansen
    • 1
    • 2
  • Jason A. Koutcher
    • 1
    • 2
    • 3
  • Amita Shukla-Dave
    • 1
    • 2
  1. 1.Department of Medical PhysicsMemorial Sloan-Kettering Cancer CenterNew YorkUSA
  2. 2.Department of RadiologyMemorial Sloan-Kettering Cancer CenterNew YorkUSA
  3. 3.Department of MedicineMemorial Sloan-Kettering Cancer CenterNew YorkUSA

Personalised recommendations