Seminars in Oncology
Volume 35, Issue 3 , Pages 262-273 , June 2008

Novel Imaging Approaches to Head and Neck Cancer

  • Kenneth A. Krohn

      Affiliations

    • Department of Radiology, University of Washington, Seattle, WA.
    • Corresponding Author InformationAddress correspondence to Kenneth A. Krohn, PhD, University of Washington Medical Center, 1959 NE Pacific St, Room NW041, Box 356004, Seattle, WA 98195-6004.
    • ,
  • Bevan Yeuh

      Affiliations

    • Department of Otolaryngology/Head and Neck Surgery, University of Minnesota, Minneapolis, MN.

References 

  1. Carmellet P, Jain RK. Angiogenesis in cancer and other diseases. Nature. 2000;407:249–257
  2. Sloane BF, Gillies RJ, Mohla S, et al. 12 Imaging: cancer biology and the tumor microenvironment. Cancer Res. 2006;66:11097–11099
  3. Gray LH, Conger AD, Ebert M, et al. The concentration of oxygen dissolved in tissues at the time of irradiation as a factor in radiotherapy. Br J Radiol. 1953;26:638–648
  4. Dewhirst MW, Navia IC, Brizel DM, et al. Multiple etiologies of tumor hypoxia require multifaceted solutions. Clin Cancer Res. 2007;13:375–377
  5. Semenza GL. Targeting HIF-1 for cancer therapy. Nature Rev. 2003;3:721–732
  6. Moeller BJ, Cao Y, Li CY, et al. Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: role of reoxygenation, free radicals, and stress granules. Cancer Cell. 2004;5:429–441
  7. Moeller BJ, Richardson RA, Dewhirst MW. Hypoxia and radiotherapy: opportunities for improved outcomes in cancer treatment. Cancer Metast Rev. 2007;26:241–248
  8. Chan DA, Giaccia AJ. Hypoxia, gene expression, and metastasis. Cancer Metast Rev. 2007;26:333–339
  9. Warburg O. The metabolism of tumors. London: Arnold Constable; 1930;
  10. Hervouet E, Godinot C. Mitochondrial disorders in renal tumors. Mitochondrion. 2006;6:1055–1117
  11. Walenta S, Schroeder T, Mueller-Klieser W. Metabolic mapping with bioluminescence: basic and clinical relevance. Biomol Engr. 2002;18:249–262
  12. Hammond EM, Giaccia AJ. Hypoxia-inducible factor-1 and p53: friends, acquaintances, or strangers?. Clin Cancer Res. 2006;12:5007–5009
  13. Lukashev D, Ohta A, Sitkovsky M. Hypoxia-dependent anti-inflammatory pathways in protection of cancerous tissues. Cancer Metast Rev. 2007;26:273–279
  14. Mueller-Klieser W, Schlenger K-H, Walenta S, et al. Pathophysiological approaches to identifying tumor hypoxia in patients. Radiother Oncol. 1991;20(Suppl):21–28
  15. Vaupel P, Mayer A. Hypoxia in cancer: significance and impact on clinical outcome. Cancer Metast Rev. 2007;26:225–239
  16. Department of Veterans Affairs Laryngeal Cancer Study Group. Induction chemotherapy plus radiation compared with surgery plus radiation in patients with advanced laryngeal cancer. N Engl J Med. 1991;324:1685–1690
  17. Forastiere AA, Goepfert H, Maor M, et al. Concurrent chemotherapy and radiotherapy for organ preservation in advanced laryngeal cancer. N Engl J Med. 2003;349:2091–2098
  18. Beaney RP, Lammertsma AA, Jones T, et al. Positron emission tomography for in-vivo measurement of regional blood flow, oxygen utilization, and blood volume in patients with breast carcinoma. Lancet. 1984;1:131–134
  19. Sorensen M, Horsman MR, Cumming P, et al. Effect of intratumoral heterogeneity in oxygenation status on FMISO PET, autoradiography, and electrode Po2 measurements in murine tumors. Int J Radiat Oncol Biol Phys. 2005;62:854–861
  20. Chapman JD, Franko AJ, Sharplin J. A marker for hypoxic cells in tumours with potential clinical applicability. Br J Cancer. 1981;43:546–550
  21. Rasey JS, Martin GV, Krohn KA. Quantifying hypoxia with radiolabeled fluoromisonidazole: pre-clinical and clinical studies. In:  Machulla H-J editors. The imaging of hypoxia. Dordrecht: Kluwer; 1999;p. 85–117
  22. Workman P. Pharmacokinetics of hypoxic cell radiosensitizers: a review. Cancer Clin Trials. 1980;3:237–251
  23. Wiebe LI, Stypinski D. Pharmacokinetics of SPECT radiopharmaceuticals for imaging hypoxic tissues. Q J Nucl Med. 1996;40:270–284
  24. Martin GV, Cerqueira MD, Caldwell JH, et al. Fluoromisonidazole: a metabolic marker of myocyte hypoxia. Circ Res. 1990;67:240–244
  25. Rasey JS, Nelson NJ, Chin L, et al. Characteristics of the binding of labeled fluoromisonidazole in cells in vitro. Radiat Res. 190;122:301-8.
  26. Rasey JS, Hoffman JM, Spence AM. Hypoxia mediated binding of misonidazole in non-malignant tissue. Int J Radiat Oncol Biol Phys. 1986;12:1255–1258
  27. Hoffman JM, Rasey JS, Spence AM, et al. Binding of the hypoxia tracer [3H]misonidazole in cerebral ischemia. Stroke. 1987;18:168–176
  28. Piert M, Machulla HJ, Becker G, et al. Dependency of the [18F]fluoromisonidazole uptake on oxygen delivery and tissue oxygenation in the porcine liver. Nucl Med Biol. 2000;27:693–700
  29. Piert M, Machulla H, Becker G, et al. Introducing fluorine-18 fluoromisonidazole positron emission tomography for the localisation and quantification of pig liver hypoxia. Eur J Nucl Med. 1999;26:95–109
  30. Smith BR, Born JL. Metabolism and excretion of [3H]misonidazole by hypoxic rat liver. Int J Radiat Oncol Biol Phys. 1984;10:1365–1370
  31. Shelton ME, Dence CS, Hwang DR, et al. In vivo delineation of myocardial hypoxia during coronary occlusion using fluorine-18 fluoromisonidazole and positron emission tomography: a potential approach for identification of jeopardized myocardium. J Am Coll Cardiol. 1990;16:477–485
  32. Caldwell JH, Revenaugh JR, Martin GV, et al. Comparison of fluorine-18-fluorodeoxyglucose and tritiated fluoromisonidazole uptake during low-flow ischemia. J Nucl Med. 1995;36:1633–1638
  33. Prekeges JL, Rasey JS, Grunbaum Z, et al. Reduction of fluoromisonidazole, a new imaging agent for hypoxia. Biochem Pharmacol. 1991;42:2387–2395
  34. Brown JM, Workman P. Partition coefficient as a guide to the development of radiosensitizers which are less toxic than misonidazole. Radiat Res. 1980;82:171–190
  35. Stone HB, Sinesi MS. Testing of new hypoxic cell sensitizers in vivo. Radiat Res. 1982;91:186–198
  36. Paget GE. Toxicity tests: a guide for clinicians. J New Drugs. 1962;2:78–83
  37. Overgaard J. Clinical evaluation of nitroimidazoles as modifiers of hypoxia in solid tumors. Oncol Res. 1994;6:509–518
  38. Graham MM, Peterson LM, Link JM, et al. Fluorine-18-fluoromisonidazole radiation dosimetry in imaging studies. J Nucl Med. 1997;38:1631–1636
  39. Rajendran JG, Schwartz DL, O'Sullivan J, et al. Tumor hypoxia imaging with [F-18]FMISO PET in head and neck cancer: value of pre-therapy FMISO uptake in predicting survival. Clin Cancer Res. 2006;12:5435–5441
  40. Rajendran JG, Mankoff DA, O'Sullivan F, et al. Hypoxia and glucose metabolism in malignant tumors: evaluation by [18F]fluoromisonidazole and [18F]fluorodeoxyglucose positron emission tomography imaging. Clin Cancer Res. 2004;10:2245–2252
  41. Padhani AR, Krohn KA, Lewis JS, et al. Imaging oxygenation of human tumours. Eur Radiol. 2007;17:861–872
  42. Silverman DH, Hoh CK, Seltzer MA, et al. Evaluating tumor biology and oncological disease with positron-emission tomography. Semin Radiat Oncol. 1998;8:183–196
  43. Tatum JL, Kelloff GJ, Gillies RJ, et al. Hypoxia: importance in tumor biology, noninvasive measurement by imaging, and value of its measurement in the management of cancer therapy. Int J Radiat Biol. 2006;82:699–757
  44. Rischin D, Peters L, Hicks R, et al. Phase I trial of concurrent tirapazamine, cisplatin, and radiotherapy in patients with advanced head and neck cancer. J Clin Oncol. 2001;19:535–542
  45. Rischin D, Hicks RJ, Fisher R, et al. 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. J Clin Oncol. 2007;24:2098–2104
  46. Koh WJ, Bergman KS, Rasey JS, et al. Evaluation of oxygenation status during fractionated radiotherapy in human nonsmall cell lung cancers using [F-18]fluoromisonidazole positron emission tomography. Int J Radiat Oncol Biol Phys. 1995;33:391–398
  47. Valk PE, Mathis CA, Prados MD. Hypoxia in human gliomas: demonstration by PET with fluorine-18-fluoromisonidazole. J Nucl Med. 1992;33:2133–2137
  48. Eschmann S-M, Paulsen F, Reimold M, et al. Prognostic impact of hypoxia imaging with 18F-misonidazole PET in non-small cell lung cancer and head and neck cancer before radiotherapy. J Nucl Med. 2005;46:253–260
  49. Eschmann SM, Paulsen F, Bedeshem C, et al. Hypoxia-imaging with 18F-misonidazole and PET: changes of kinetics during radiotherapy of head-and-neck cancer. Radiother Oncol. 2007;83:406–410
  50. Read SJ, Hirano T, Abbott DF, et al. Identifying hypoxic tissue after acute ischemic stroke using PET and 18F-fluoromisonidazole. Neurology. 1998;51:1617–1621
  51. Gagel B, Reinartz P, DiMartino E, et al. pO2 polarography versus positron emission tomography ([18F]fluoromisonidazole, [18F]-2-fluoro-2'-deoxyglucose): an appraisal of radiotherapeutically relevant hypoxia. Strahlenther Onkol. 2004;180:616–622
  52. Thorwarth D, Eschmann S-M, Holzner F, et al. Combined uptake of [18F]FDG and [18F]FMISO correlates with radiation therapy outcome in head-and-neck cancer patients. Radiother Oncol. 2006;80:151–156
  53. Rasey JS, Koh WJ, Evans ML, et al. 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. 1996;36:417–428
  54. Bruehlmeier M, Roelcke U, Schubiger PA. Assessment of hypoxia and perfusion in human brain tumors using PET with 18F-fluoromisonidazole and 15O-H2O. J Nucl Med. 2004;45:1851–1859
  55. Rajendran JG, Krohn KA. Imaging hypoxia and angiogenesis in tumors. Radiol Clin North Am. 2005;43:169–187
  56. Lehtio K, Oikonen V, Gronroos T, et al. Imaging of blood flow and hypoxia in head and neck cancer: initial evaluation with [15O]H2O and [18F]Fluoroerythronitroimidazole PET. J Nucl Med. 2001;42:1643–1652
  57. Sorger D, Patt M, Kumar P, et al. [18F]Fluoroazomycinarabinofuranoside (18FAZA) and [18F]fluoromisonidazole (18FMISO): a comparative study of their selective uptake in hypoxic cells and PET imaging in experimental rat tumors. Nucl Med Biol. 2003;30:317–326
  58. Souvatzoglou M, Grosu AL, Roper B, et al. Tumour hypoxia imaging with [18F]FAZA PET in head and neck cancer patients: a pilot study. Eur J Nucl Med Mol Imaging. 2007;34:1566–1575
  59. McManus ME, Monks A, Collins JM, et al. Nonlinear pharmacokinetics of misonidazole and desmethylmisonidazole in the isolated perfused rat liver. J Pharmacol Exp Ther. 1981;219:669–674
  60. Dubois L, Landuyt W, Haustermans K, et al. Evaluation of hypoxia in an experimental rat tumour model by [18F]fluoromisonidazole PET and immunohistochemistry. Br J Cancer. 2004;91:1947–1954
  61. Shin KH, Diaz-Gonzalez JA, Russell J, et al. Detecting changes in tumor hypoxia with carbonic anhydrase IX and pimonidazole. Cancer Biol Ther. 2007;6:70–75
  62. Rasey JS, Evans ML. Detecting hypoxia in human tumors. In:  Vaupel P,  Jain RK editor. Tumor blood supply and metabolic microenvironment: characterizations and implications for therapy (Funktionanalyze Biologischer Systeme 20). Stuttgart, Germany: Gustav Fischer Verlag; 1991;p. 187–201
  63. Minn H, Clavo AC, Wahl RL. Influence of hypoxia on tracer accumulation in squamous-cell carcinoma: in vitro evaluation for PET imaging. Nucl Med Biol. 1996;23:941–946
  64. Rajendran JG, Wilson DC, Conrad EU, et al. [18F]FMISO and [18F]FDG PET imaging in soft tissue sarcomas: correlation of hypoxia, metabolism and VEGF expression. Eur J Nucl Med Mol Imaging. 2003;30:695–704
  65. Cherk MH, Foo SS, Poon AMT, et al. Lack of correlation of hypoxic cell fraction and angiogenesis with glucose metabolic rate in non-small cell lung cancer assessed by 18F-fluoromisonidazole and 18F-FDG PET. J Nucl Med. 2006;47:1921–1926
  66. Cher LM, Murone C, Lawrentschuk N, et al. Correlation of hypoxic cell fraction and angiogenesis with glucose metabolic rate in gliomas using 18F-fluoromisonidazole, 18F-FDG PET, and immunohistochemical studies. J Nucl Med. 2006;47:410–418
  67. Walenta S, Salameh A, Lyng H, et al. Short communication: correlation of high lactate levels in head and neck tumors with incidence of metastasis. Am J Pathol. 1997;150:409–415
  68. Scheumman GF, Hoang Vu C, Cetin Y, et al. Clinical significance of E-cadherin as a prognostic marker in thyroid carcinomas. J Clin Endocrinol Metab. 1995;80:2168–2172
  69. Koong AC, Denko NC, Hudson KM, et al. Candidate genes for hypoxic tumor phenotype. Cancer Res. 2000;60:883–887
  70. Brizel DM, Schroeder T, Scher RL, et al. Elevated tumor lactate concentrations predict for an increased risk of metastases in head-and-neck cancer. Int J Radiat Oncol Biol. 2001;51:349–353
  71. Adalsteinsson E, Spielman DM, Pauly JM, et al. Feasibility study of lactate imaging of head and neck tumors. NMR Biomed. 1998;11:360–369
  72. Tarnawski R, Sokol M, Pieniazek P, et al. 1H-MRS in vivo predicts the early treatment outcome of postoperative radiotherapy for malignant gliomas. Int J Radiat Oncol Biol Phys. 2002;52:1271–1276
  73. McCabe KJ, Rubinstein D. Advances in head and neck imaging. Otolaryngol Clin North Am. 2005;38:307–319
  74. Menda Y, Graham MM. Update on 18F-fluorodeoxyglucose/positron emission tomography and positron emission tomography/computed tomography imaging of squamous head and neck cancers. Semin Nucl Med. 2005;35:214–219
  75. Foo SS, Abbott DF, Lawrentschuk N, et al. Functional imaging of intratumoral hypoxia. Mol Imag Biol. 2004;6:291–305
  76. Hermans R. Head and neck cancer: how imaging predicts treatment outcome. Cancer Imag. 2006;6:145–153
  77. Ang KK, Harris J, Garden AS, et al. Concomitant boost radiation plus concurrent cisplatin for advanced head and neck carcinomas: Radiation Therapy Oncology Group phase II trial 99-14. J Clin Oncol. 2005;23:3008–3015
  78. Schwartz DL, Ford EC, Rajendran J, et al. FDG-PET/CT–guided intensity modulated head and neck radiotherapy: a pilot investigation. Head Neck. 2005;27:478–487
  79. Van den Brekel MW, Ljumanovic R, Castelijns JA. Imaging characteristics of regional metastasis. In:  Baatenburg de Jong editors. Prognosis in head and neck cancer. London: Taylor & Francis; 2006;p. 197–213
  80. Daisne J-F, Duprez T, Weynand B, et al. Tumor volume in pharyngolaryngeal squamous cell carcinoma: comparison at CT, MR Imaging, and FDG PET and validation with surgical specimen. Radiology. 2004;233:93–100
  81. Connell CA, Corry J, Milner AD, et al. Clinical impact of, and prognostic stratification by, F-18 FDG PET/CT in head and neck mucosal squamous cell carcinoma. Head Neck. 2007;29:986–995
  82. Hermans R, Meijerink M, Van den Bogaert W, et al. Tumor perfusion rate determined noninvasively by dynamic computed tomography predicts outcome in head-and-neck cancer after radiotherapy. Int J Radiat Oncol Biol Phys. 2003;57:1351–1356
  83. Denko NC, Fontana LA, Hudson KM, et al. Investigating hypoxic tumor physiology through gene expression patterns. Oncogene. 2003;22:5907–5914
  84. Chen Y, Shi G, Xia Wei, et al. Identification of hypoxia-regulated proteins in head and neck cancer by proteomic and tissue array profiling. Cancer Res. 2004;64:7302–7310
  85. Winter SC, Buffa FM, Silva P, et al. Relation of a hypoxia metagene derived from head and neck cancer to prognosis of multiple cancers. Cancer Res. 2007;67:3441–3449
  86. Jonathan RA, Wijffels KIEM, Peeters W, et al. The prognostic value of endogenous hypoxia-related markers for head and neck squamous cell carcinomas treated with ARCON. Radiother Oncol. 2006;79:288–297
  87. Vordermark D, Brown JM. Endogenous markers of tumor hypoxia predictors of clinical radiation resistance?. Strahlenther Onkol. 2003;179:801–811
  88. Ling CC, Humm J, Larson S, et al. Towards multidimensional radiotherapy (MD-CRT): Biological imaging and biological conformality. Int J Radiat Oncol Biol Phys. 2000;47:551–560
  89. Thorwarth D, Eschmann S-M, Paulsen F, et al. Hypoxia dose painting by numbers: a planning study. Int J Radiat Oncol Biol Phys. 2007;68:291–300
  90. Kaanders JHAM, Pop LAM, Mares HAM, et al. ARCON: experience in 215 patients with advanced head-and-neck cancer. Int J Radiat Oncol Biol Phys. 2002;52:769–778
  91. Ingram N, Porter CD. Transcriptional targeting of acute hypoxia in the tumour stroma is a novel and viable strategy for cancer gene therapy. Gene Ther. 2005;12:1058–1069
  92. Durand RE. Intermittent blood flow in solid tumours—an under-appreciated source of ‘drug resistance.'. Cancer Metast Rev. 2001;20:57–61
  93. Brown JM. SR 4233 (tirapazamine): a new anticancer drug exploiting hypoxia in solid tumours. Br J Cancer. 1993;67:1163–1170

 Supported by Grant No. P01 CA42045 from the National Cancer Institute.

PII: S0093-7754(08)00064-X

doi: 10.1053/j.seminoncol.2008.03.001

Seminars in Oncology
Volume 35, Issue 3 , Pages 262-273 , June 2008

Article Tools

* Image Usage & Resolution