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European Journal of Nuclear Medicine and Molecular Imaging

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20.08.2018 | Review Article

Longitudinal PET imaging of tumor hypoxia during the course of radiotherapy

verfasst von: Sonja Stieb, Afroditi Eleftheriou, Geoffrey Warnock, Matthias Guckenberger, Oliver Riesterer

Erschienen in: European Journal of Nuclear Medicine and Molecular Imaging | Ausgabe 12/2018

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Abstract

Hypoxia results from an imbalance between oxygen supply and consumption. It is a common phenomenon in solid malignant tumors such as head and neck cancer. As hypoxic cells are more resistant to therapy, tumor hypoxia is an indicator for poor prognosis. Several techniques have been developed to measure tissue oxygenation. These are the Eppendorf O2 polarographic needle electrode, immunohistochemical analysis of endogenous (e.g., hypoxia-inducible factor-1α (HIF-1a)) and exogenous markers (e.g., pimonidazole) as well as imaging methods such as functional magnetic resonance imaging (e.g., blood oxygen level dependent (BOLD) imaging, T1-weighted imaging) and hypoxia positron emission tomography (PET). Among the imaging modalities, only PET is sufficiently validated to detect hypoxia for clinical use. Hypoxia PET tracers include 18F-fluoromisonidazole (FMISO), the most commonly used hypoxic marker, 18F-flouroazomycin arabinoside (FAZA), 18Ffluoroerythronitroimidazole (FETNIM), 18F-2-nitroimidazolpentafluoropropylacetamide (EF5) and 18F-flortanidazole (HX4). As technical development provides the opportunity to increase the radiation dose to subregions of the tumor, such as hypoxic areas, it has to be ensured that these regions are stable not only from imaging to treatment but also through the course of radiotherapy. The aim of this review is therefore to characterize the behavior of tumor hypoxia during radiotherapy for the whole tumor and for subregions by using hypoxia PET tracers, with focus on head and neck cancer patients.

Vaupel P, Harrison L. Tumor hypoxia: causative factors, compensatory mechanisms, and cellular response. Oncologist. 2004;9(Suppl 5):4–9. https://doi.org/10.1634/theoncologist.9-90005-4.CrossRefPubMed

Harris AL. Hypoxia—a key regulatory factor in tumour growth. Nat Rev Cancer. 2002;2:38–47. https://doi.org/10.1038/nrc704.CrossRefPubMed

Hockel M, Vaupel P. Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J Natl Cancer Inst. 2001;93:266–76.CrossRef

Vaupel P. The role of hypoxia-induced factors in tumor progression. Oncologist. 2004;9(Suppl 5):10–7. https://doi.org/10.1634/theoncologist.9-90005-10.CrossRefPubMed

Janssen HL, Haustermans KM, Balm AJ, Begg AC. Hypoxia in head and neck cancer: how much, how important? Head Neck. 2005;27:622–38. https://doi.org/10.1002/hed.20223.CrossRefPubMed

Lyng H, Sundfor K, Rofstad EK. Oxygen tension in human tumours measured with polarographic needle electrodes and its relationship to vascular density, necrosis and hypoxia. Radiother Oncol. 1997;44:163–9.CrossRefPubMed

Kallinowski F, Zander R, Hoeckel M, Vaupel P. Tumor tissue oxygenation as evaluated by computerized-pO2-histography. Int J Radiat Oncol Biol Phys. 1990;19:953–61.CrossRefPubMed

Nordsmark M, Bentzen SM, Overgaard J. Measurement of human tumour oxygenation status by a polarographic needle electrode. An analysis of inter- and intratumour heterogeneity. Acta Oncol. 1994;33:383–9.CrossRefPubMed

Le QT, Courter D. Clinical biomarkers for hypoxia targeting. Cancer Metastasis Rev. 2008;27:351–62. https://doi.org/10.1007/s10555-008-9144-9.CrossRefPubMedPubMedCentral

10.

Horsman MR, Mortensen LS, Petersen JB, Busk M, Overgaard J. Imaging hypoxia to improve radiotherapy outcome. Nat Rev Clin Oncol. 2012;9:674–87. https://doi.org/10.1038/nrclinonc.2012.171.CrossRefPubMed

11.

Horsman MR. Measurement of tumor oxygenation. Int J Radiat Oncol Biol Phys. 1998;42:701–4.CrossRefPubMed

12.

Vaupel P. Tumor hypoxia: pathophysiology, clinical significance and therapeutic perspectives; with 19 tables. Stuttgart, Wissenschaftliche Verlagsgesellschaft; 1999.

13.

Busk M, Horsman MR, Overgaard J. Resolution in PET hypoxia imaging: voxel size matters. Acta Oncol. 2008;47:1201–10. https://doi.org/10.1080/02841860802307716.CrossRefPubMed

14.

Chang JH, Wada M, Anderson NJ, Lim Joon D, Lee ST, Gong SJ, et al. Hypoxia-targeted radiotherapy dose painting for head and neck cancer using (18)F-FMISO PET: a biological modeling study. Acta Oncol. 2013;52:1723–9. https://doi.org/10.3109/0284186X.2012.759273.CrossRefPubMed

15.

Hendrickson K, Phillips M, Smith W, Peterson L, Krohn K, Rajendran J. Hypoxia imaging with [F-18] FMISO-PET in head and neck cancer: potential for guiding intensity modulated radiation therapy in overcoming hypoxia-induced treatment resistance. Radiother Oncol. 2011;101:369–75. https://doi.org/10.1016/j.radonc.2011.07.029.CrossRefPubMedPubMedCentral

16.

Lopci E, Grassi I, Chiti A, Nanni C, Cicoria G, Toschi L, et al. PET radiopharmaceuticals for imaging of tumor hypoxia: a review of the evidence. Am J Nucl Med Mol Imaging. 2014;4:365–84.PubMedPubMedCentral

17.

Carlin S, Humm JL. PET of hypoxia: current and future perspectives. J Nucl Med. 2012;53:1171–4. https://doi.org/10.2967/jnumed.111.099770.CrossRefPubMed

18.

Fleming IN, Manavaki R, Blower PJ, West C, Williams KJ, Harris AL, et al. Imaging tumour hypoxia with positron emission tomography. Br J Cancer. 2015;112:238–50. https://doi.org/10.1038/bjc.2014.610.CrossRefPubMed

19.

Halmos GB. Bruine de Bruin L, Langendijk JA, van der Laan BF, Pruim J, Steenbakkers RJ. Head and neck tumor hypoxia imaging by 18F-fluoroazomycin-arabinoside (18F-FAZA)-PET: a review. Clin Nucl Med. 2014;39:44–8. https://doi.org/10.1097/RLU.0000000000000286.CrossRefPubMed

20.

Joiner MC, Van der Kogel A. Basic clinical radiobiology. Boca Raton, FL, CRC Press; 2016.

21.

Bruehlmeier M, Roelcke U, Schubiger PA, Ametamey SM. Assessment of hypoxia and perfusion in human brain tumors using PET with 18F-fluoromisonidazole and 15O-H2O. J Nucl Med. 2004;45:1851–9.

22.

Gagel B, Piroth M, Pinkawa M, Reinartz P, Zimny M, Kaiser HJ, et al. pO polarography, contrast enhanced color duplex sonography (CDS), [18F] fluoromisonidazole and [18F] fluorodeoxyglucose positron emission tomography: validated methods for the evaluation of therapy-relevant tumor oxygenation or only bricks in the puzzle of tumor hypoxia? BMC Cancer. 2007;7:113. https://doi.org/10.1186/1471-2407-7-113.CrossRefPubMedPubMedCentral

23.

Troost EG, Laverman P, Kaanders JH, Philippens M, Lok J, Oyen WJ, et al. Imaging hypoxia after oxygenation-modification: comparing [18F]FMISO autoradiography with pimonidazole immunohistochemistry in human xenograft tumors. Radiother Oncol. 2006;80:157–64. https://doi.org/10.1016/j.radonc.2006.07.023.CrossRefPubMed

24.

Sato J, Kitagawa Y, Yamazaki Y, Hata H, Okamoto S, Shiga T, et al. 18F-fluoromisonidazole PET uptake is correlated with hypoxia-inducible factor-1alpha expression in oral squamous cell carcinoma. J Nucl Med. 2013;54:1060–5. https://doi.org/10.2967/jnumed.112.114355.CrossRefPubMed

25.

Norikane T, Yamamoto Y, Maeda Y, Kudomi N, Matsunaga T, Haba R, et al. Correlation of (18)F-fluoromisonidazole PET findings with HIF-1alpha and p53 expressions in head and neck cancer: comparison with (18)F-FDG PET. Nucl Med Commun. 2014;35:30–5. https://doi.org/10.1097/MNM.0000000000000010.CrossRefPubMed

26.

Rajendran JG, Schwartz DL, O'Sullivan J, Peterson LM, Ng P, Scharnhorst J, et al. Tumor hypoxia imaging with [F-18] fluoromisonidazole positron emission tomography in head and neck cancer. Clin Cancer Res. 2006;12:5435–41. https://doi.org/10.1158/1078-0432.CCR-05-1773.CrossRefPubMedPubMedCentral

27.

Rischin D, Hicks RJ, Fisher R, Binns D, Corry J, Porceddu S, 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. 2006;24:2098–104. https://doi.org/10.1200/JCO.2005.05.2878.CrossRef

28.

Lee ST, Scott AM. Hypoxia positron emission tomography imaging with 18f-fluoromisonidazole. Semin Nucl Med. 2007;37:451–61. https://doi.org/10.1053/j.semnuclmed.2007.07.001.CrossRefPubMed

29.

Roels S, Slagmolen P, Nuyts J, Lee JA, Loeckx D, Maes F, et al. Biological image-guided radiotherapy in rectal cancer: is there a role for FMISO or FLT, next to FDG? Acta Oncol. 2008;47:1237–48. https://doi.org/10.1080/02841860802256434.CrossRefPubMed

30.

Segard T, Robins PD, Yusoff IF, Ee H, Morandeau L, Campbell EM, et al. Detection of hypoxia with 18F-fluoromisonidazole (18F-FMISO) PET/CT in suspected or proven pancreatic cancer. Clin Nucl Med. 2013;38:1–6. https://doi.org/10.1097/RLU.0b013e3182708777.CrossRefPubMed

31.

Kumar PSD, Xia H, McEwan AJB, Machulla HJ, Wiebe LI. Fluoroazomycin arabinoside (FAZA): synthesis, 2H and 3H-labelling and preliminary biological evaluation of a novel 2-nitroimidazole marker of tissue hypoxia. J Label Compounds Radiopharm. 1999;42(1):3–16.CrossRef

32.

Okamoto S, Shiga T, Yasuda K, Ito YM, Magota K, Kasai K, et al. High reproducibility of tumor hypoxia evaluated by 18F-fluoromisonidazole PET for head and neck cancer. J Nucl Med. 2013;54:201–7. https://doi.org/10.2967/jnumed.112.109330.CrossRefPubMed

33.

Busk M, Jakobsen S, Horsman MR, Mortensen LS, Iversen AB, Overgaard J, et al. PET imaging of tumor hypoxia using 18F-labeled pimonidazole. Acta Oncol. 2013;52:1300–7. https://doi.org/10.3109/0284186X.2013.815797.CrossRefPubMed

34.

Nehmeh SA, Lee NY, Schroder H, Squire O, Zanzonico PB, Erdi YE, et al. Reproducibility of intratumor distribution of (18)F-fluoromisonidazole in head and neck cancer. Int J Radiat Oncol Biol Phys. 2008;70:235–42. https://doi.org/10.1016/j.ijrobp.2007.08.036.CrossRefPubMedPubMedCentral

35.

Lin Z, Mechalakos J, Nehmeh S, Schoder H, Lee N, Humm J, et al. The influence of changes in tumor hypoxia on dose-painting treatment plans based on 18F-FMISO positron emission tomography. Int J Radiat Oncol Biol Phys. 2008;70:1219–28. https://doi.org/10.1016/j.ijrobp.2007.09.050.CrossRefPubMedPubMedCentral

36.

Grkovski M, Schwartz J, Rimner A, Schoder H, Carlin SD, Zanzonico PB, et al. Reproducibility of 18F-fluoromisonidazole intratumour distribution in non-small cell lung cancer. EJNMMI Res. 2016;6:79. https://doi.org/10.1186/s13550-016-0210-y.CrossRefPubMedPubMedCentral

37.

Wuest M, Wuest F. Positron emission tomography radiotracers for imaging hypoxia. J Labelled Comp Radiopharm. 2013;56:244–50. https://doi.org/10.1002/jlcr.2997.CrossRefPubMed

38.

Zips D, Zophel K, Abolmaali N, Perrin R, Abramyuk A, Haase R, et al. Exploratory prospective trial of hypoxia-specific PET imaging during radiochemotherapy in patients with locally advanced head-and-neck cancer. Radiother Oncol. 2012;105:21–8. https://doi.org/10.1016/j.radonc.2012.08.019.CrossRefPubMed

39.

Servagi-Vernat S, Differding S, Hanin FX, Labar D, Bol A, Lee JA, et al. A prospective clinical study of (1)(8)F-FAZA PET-CT hypoxia imaging in head and neck squamous cell carcinoma before and during radiation therapy. Eur J Nucl Med Mol Imaging. 2014;41:1544–52. https://doi.org/10.1007/s00259-014-2730-x.CrossRefPubMed

40.

Mortensen LS, Johansen J, Kallehauge J, Primdahl H, Busk M, Lassen P, et al. FAZA PET/CT hypoxia imaging in patients with squamous cell carcinoma of the head and neck treated with radiotherapy: results from the DAHANCA 24 trial. Radiother Oncol. 2012;105:14–20. https://doi.org/10.1016/j.radonc.2012.09.015.CrossRefPubMed

41.

Li L, Hu M, Zhu H, Zhao W, Yang G, Yu J. Comparison of 18F-Fluoroerythronitroimidazole and 18F-fluorodeoxyglucose positron emission tomography and prognostic value in locally advanced non-small-cell lung cancer. Clin Lung Cancer. 2010;11:335–40. https://doi.org/10.3816/CLC.2010.n.042.CrossRefPubMed

42.

Yue J, Yang Y, Cabrera AR, Sun X, Zhao S, Xie P, et al. Measuring tumor hypoxia with (1)(8)F-FETNIM PET in esophageal squamous cell carcinoma: a pilot clinical study. Dis Esophagus. 2012;25:54–61. https://doi.org/10.1111/j.1442-2050.2011.01209.x.CrossRefPubMed

43.

Lehtio K, Eskola O, Viljanen T, Oikonen V, Gronroos T, Sillanmaki L, et al. Imaging perfusion and hypoxia with PET to predict radiotherapy response in head-and-neck cancer. Int J Radiat Oncol Biol Phys. 2004;59:971–82. https://doi.org/10.1016/j.ijrobp.2003.12.014.CrossRefPubMed

44.

Komar G, Seppanen M, Eskola O, Lindholm P, Gronroos TJ, Forsback S, et al. 18F-EF5: a new PET tracer for imaging hypoxia in head and neck cancer. J Nucl Med. 2008;49:1944–51. https://doi.org/10.2967/jnumed.108.053785.CrossRefPubMed

45.

Silvoniemi A, Suilamo S, Laitinen T, Forsback S, Loyttyniemi E, Vaittinen S, et al. Repeatability of tumour hypoxia imaging using [(18)F]EF5 PET/CT in head and neck cancer. Eur J Nucl Med Mol Imaging. 2018;45:161–9. https://doi.org/10.1007/s00259-017-3857-3.CrossRefPubMed

46.

Chen L, Zhang Z, Kolb HC, Walsh JC, Zhang J, Guan Y. (1)(8)F-HX4 hypoxia imaging with PET/CT in head and neck cancer: a comparison with (1)(8)F-FMISO. Nucl Med Commun. 2012;33:1096–102. https://doi.org/10.1097/MNM.0b013e3283571016.CrossRefPubMed

47.

Zegers CM, van Elmpt W, Szardenings K, Kolb H, Waxman A, Subramaniam RM, et al. Repeatability of hypoxia PET imaging using [(1)(8)F]HX4 in lung and head and neck cancer patients: a prospective multicenter trial. Eur J Nucl Med Mol Imaging. 2015;42:1840–9. https://doi.org/10.1007/s00259-015-3100-z.CrossRefPubMedPubMedCentral

48.

Takahashi N, Fujibayashi Y, Yonekura Y, Welch MJ, Waki A, Tsuchida T, et al. Evaluation of 62Cu labeled diacetyl-bis(N4-methylthiosemicarbazone) as a hypoxic tissue tracer in patients with lung cancer. Ann Nucl Med. 2000;14:323–8.CrossRefPubMed

49.

Dehdashti F, Grigsby PW, Mintun MA, Lewis JS, Siegel BA, Welch MJ. Assessing tumor hypoxia in cervical cancer by positron emission tomography with 60Cu-ATSM: relationship to therapeutic response—a preliminary report. Int J Radiat Oncol Biol Phys. 2003;55:1233–8.CrossRefPubMed

50.

Divgi CR, Pandit-Taskar N, Jungbluth AA, Reuter VE, Gonen M, Ruan S, et al. Preoperative characterisation of clear-cell renal carcinoma using iodine-124-labelled antibody chimeric G250 (124I-cG250) and PET in patients with renal masses: a phase I trial. Lancet Oncol. 2007;8:304–10. https://doi.org/10.1016/S1470-2045(07)70044-X.CrossRefPubMed

51.

Yang DJ, Wallace S, Cherif A, Li C, Gretzer MB, Kim EE, et al. Development of F-18-labeled fluoroerythronitroimidazole as a PET agent for imaging tumor hypoxia. Radiology. 1995;194:795–800. https://doi.org/10.1148/radiology.194.3.7862981.CrossRefPubMed

52.

Evans SM, Judy KD, Dunphy I, Jenkins WT, Nelson PT, Collins R, et al. Comparative measurements of hypoxia in human brain tumors using needle electrodes and EF5 binding. Cancer Res. 2004;64:1886–92.CrossRefPubMed

53.

Evans SM, Fraker D, Hahn SM, Gleason K, Jenkins WT, Jenkins K, et al. EF5 binding and clinical outcome in human soft tissue sarcomas. Int J Radiat Oncol Biol Phys. 2006;64:922–7. https://doi.org/10.1016/j.ijrobp.2005.05.068.CrossRefPubMed

54.

Dubois LJ, Lieuwes NG, Janssen MH, Peeters WJ, Windhorst AD, Walsh JC, et al. Preclinical evaluation and validation of [18F]HX4, a promising hypoxia marker for PET imaging. Proc Natl Acad Sci U S A. 2011;108:14620–5. https://doi.org/10.1073/pnas.1102526108.CrossRefPubMedPubMedCentral

55.

Riedl CC, Brader P, Zanzonico PB, Chun YS, Woo Y, Singh P, et al. Imaging hypoxia in orthotopic rat liver tumors with iodine 124-labeled iodoazomycin galactopyranoside PET. Radiology. 2008;248:561–70. https://doi.org/10.1148/radiol.2482071421.CrossRefPubMedPubMedCentral

56.

Hoigebazar L, Jeong JM, Choi SY, Choi JY, Shetty D, Lee YS, et al. Synthesis and characterization of nitroimidazole derivatives for 68Ga-labeling and testing in tumor xenografted mice. J Med Chem. 2010;53:6378–85. https://doi.org/10.1021/jm100545a.CrossRefPubMed

57.

Hoigebazar L, Jeong JM, Hong MK, Kim YJ, Lee JY, Shetty D, et al. Synthesis of 68Ga-labeled DOTA-nitroimidazole derivatives and their feasibilities as hypoxia imaging PET tracers. Bioorg Med Chem. 2011;19:2176–81. https://doi.org/10.1016/j.bmc.2011.02.041.CrossRefPubMed

58.

Fujibayashi Y, Taniuchi H, Yonekura Y, Ohtani H, Konishi J, Yokoyama A. Copper-62-ATSM: a new hypoxia imaging agent with high membrane permeability and low redox potential. J Nucl Med. 1997;38:1155–60.PubMed

59.

Dearling JL, Lewis JS, Mullen GE, Rae MT, Zweit J, Blower PJ. Design of hypoxia-targeting radiopharmaceuticals: selective uptake of copper-64 complexes in hypoxic cells in vitro. Eur J Nucl Med. 1998;25:788–92.CrossRefPubMed

60.

Bourgeois M, Rajerison H, Guerard F, Mougin-Degraef M, Barbet J, Michel N, et al. Contribution of [64Cu]-ATSM PET in molecular imaging of tumour hypoxia compared to classical [18F]-MISO--a selected review. Nucl Med Rev Cent East Eur. 2011;14:90–5.CrossRefPubMed

61.

Laforest R, Dehdashti F, Lewis JS, Schwarz SW. Dosimetry of 60/61/62/64Cu-ATSM: a hypoxia imaging agent for PET. Eur J Nucl Med Mol Imaging. 2005;32:764–70. https://doi.org/10.1007/s00259-004-1756-x.CrossRefPubMed

62.

Laurens E, Yeoh SD, Rigopoulos A, Cao D, Cartwright GA, O'Keefe GJ, et al. Radiolabelling and evaluation of a novel sulfoxide as a PET imaging agent for tumor hypoxia. Nucl Med Biol. 2014;41:419–25. https://doi.org/10.1016/j.nucmedbio.2014.03.001.CrossRefPubMed

63.

Falzon CL, Ackermann U, Spratt N, Tochon-Danguy HJ, White J, Howells D, et al. F-18 labelled N, N-bis-haloethylamino-phenylsulfoxides—a new class of compounds for the imaging of hypoxic tissue. J Label Compd Radiopharm. 2006;49:1089–103.CrossRef

64.

Lawrentschuk N, Lee FT, Jones G, Rigopoulos A, Mountain A, O'Keefe G, et al. Investigation of hypoxia and carbonic anhydrase IX expression in a renal cell carcinoma xenograft model with oxygen tension measurements and (1)(2)(4)I-cG250 PET/CT. Urol Oncol. 2011;29:411–20. https://doi.org/10.1016/j.urolonc.2009.03.028.CrossRefPubMed

65.

Hoeben BA, Kaanders JH, Franssen GM, Troost EG, Rijken PF, Oosterwijk E, et al. PET of hypoxia with 89Zr-labeled cG250-F(ab')2 in head and neck tumors. J Nucl Med. 2010;51:1076–83. https://doi.org/10.2967/jnumed.109.073189.CrossRefPubMed

66.

Engelhardt EL, Schneider RF, Seeholzer SH, Stobbe CC, Chapman JD. The synthesis and radiolabeling of 2-nitroimidazole derivatives of cyclam and their preclinical evaluation as positive markers of tumor hypoxia. J Nucl Med. 2002;43:837–50.PubMed

67.

Sun W, Chu T. In vivo click reaction between Tc-99m-labeled azadibenzocyclooctyne-MAMA and 2-nitroimidazole-azide for tumor hypoxia targeting. Bioorg Med Chem Lett. 2015;25:4453–6. https://doi.org/10.1016/j.bmcl.2015.09.004.CrossRefPubMed

68.

McMillan KM, Rogers BP, Field AS, Laird AR, Fine JP, Meyerand ME. Physiologic characterisation of glioblastoma multiforme using MRI-based hypoxia mapping, chemical shift imaging, perfusion and diffusion maps. J Clin Neurosci. 2006;13:811–7. https://doi.org/10.1016/j.jocn.2005.12.025.CrossRefPubMed

69.

Howe FA, Robinson SP, McIntyre DJ, Stubbs M, Griffiths JR. Issues in flow and oxygenation dependent contrast (FLOOD) imaging of tumours. NMR Biomed. 2001;14:497–506.CrossRefPubMed

70.

Pacheco-Torres J ZD, Contero A, Mason RP. Differential physiological response to carbogen of two diverse prostate tumor lines detected by tissue water 1H MRI. Proceedings of the 16th Annual Meeting ISMRM, Toronto, Canada. 2008;4337.

71.

Toth V, Forschler A, Hirsch NM, den Hollander J, Kooijman H, Gempt J, et al. MR-based hypoxia measures in human glioma. J Neuro-Oncol. 2013;115:197–207. https://doi.org/10.1007/s11060-013-1210-7.CrossRef

72.

Baudelet C, Gallez B. How does blood oxygen level-dependent (BOLD) contrast correlate with oxygen partial pressure (pO2) inside tumors? Magn Reson Med. 2002;48:980–6. https://doi.org/10.1002/mrm.10318.CrossRefPubMed

73.

Linnik IV, Scott ML, Holliday KF, Woodhouse N, Waterton JC, O'Connor JP, et al. Noninvasive tumor hypoxia measurement using magnetic resonance imaging in murine U87 glioma xenografts and in patients with glioblastoma. Magn Reson Med. 2014;71:1854–62. https://doi.org/10.1002/mrm.24826.CrossRefPubMed

74.

Pacheco-Torres J, Lopez-Larrubia P, Ballesteros P, Cerdan S. Imaging tumor hypoxia by magnetic resonance methods. NMR Biomed. 2011;24:1–16. https://doi.org/10.1002/nbm.1558.CrossRefPubMed

75.

Iversen AB, Ringgaard S, Laustsen C, Stodkilde-Jorgensen H, Bentzen L, Busk M, et al. Hyperpolarized magnetic resonance spectroscopy for assessing tumor hypoxia. Acta Oncol. 2015;54:1393–8. https://doi.org/10.3109/0284186X.2015.1070964.CrossRefPubMed

76.

Varoquaux A, Rager O, Dulguerov P, Burkhardt K, Ailianou A, Becker M. Diffusion-weighted and PET/MR imaging after radiation therapy for malignant head and neck tumors. Radiographics. 2015;35:1502–27. https://doi.org/10.1148/rg.2015140029.CrossRefPubMed

77.

Covello M, Cavaliere C, Aiello M, Cianelli MS, Mesolella M, Iorio B, et al. Simultaneous PET/MR head-neck cancer imaging: preliminary clinical experience and multiparametric evaluation. Eur J Radiol. 2015;84:1269–76. https://doi.org/10.1016/j.ejrad.2015.04.010.CrossRefPubMed

78.

Wehrl HF, Sauter AW, Divine MR, Pichler BJ. Combined PET/MR: a technology becomes mature. J Nucl Med. 2015;56:165–8. https://doi.org/10.2967/jnumed.114.150318.CrossRefPubMed

79.

Boellaard R. Standards for PET image acquisition and quantitative data analysis. J Nucl Med. 2009;50(Suppl 1):11S–20S. https://doi.org/10.2967/jnumed.108.057182.CrossRefPubMed

80.

Boellaard R, Oyen WJ, Hoekstra CJ, Hoekstra OS, Visser EP, Willemsen AT, et al. The Netherlands protocol for standardisation and quantification of FDG whole body PET studies in multi-Centre trials. Eur J Nucl Med Mol Imaging. 2008;35:2320–33. https://doi.org/10.1007/s00259-008-0874-2.CrossRefPubMed

81.

Boellaard R, Hristova I, Ettinger S, Sera T, Stroobants S, Chiti A, et al. EARL FDG-PET/CT accreditation program: Feasibility, overview and results of first 55 successfully accredited sites. J Nucl Med. 2013;54:2052.

82.

Kikuchi M, Koyasu S, Shinohara S, Usami Y, Imai Y, Hino M, et al. Prognostic value of pretreatment 18F-fluorodeoxyglucose positron emission tomography/CT volume-based parameters in patients with oropharyngeal squamous cell carcinoma with known p16 and p53 status. Head Neck. 2015;37:1524–31. https://doi.org/10.1002/hed.23784.CrossRefPubMed

83.

Monnich D, Welz S, Thorwarth D, Pfannenberg C, Reischl G, Mauz PS, et al. Robustness of quantitative hypoxia PET image analysis for predicting local tumor control. Acta Oncol. 2015;54:1364–9. https://doi.org/10.3109/0284186X.2015.1071496.CrossRefPubMed

84.

Eschmann SM, Paulsen F, Reimold M, Dittmann H, Welz S, Reischl G, 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;46:253–60.PubMed

85.

Eschmann SM, Paulsen F, Bedeshem C, Machulla HJ, Hehr T, Bamberg M, et al. Hypoxia-imaging with (18)F-Misonidazole and PET: changes of kinetics during radiotherapy of head-and-neck cancer. Radiother Oncol. 2007;83:406–10. https://doi.org/10.1016/j.radonc.2007.05.014.CrossRefPubMed

86.

Li F, Joergensen JT, Hansen AE, Kjaer A. Kinetic modeling in PET imaging of hypoxia. Am J Nucl Med Mol Imaging. 2014;4:490–506.PubMedPubMedCentral

87.

Innis RB, Cunningham VJ, Delforge J, Fujita M, Gjedde A, Gunn RN, et al. Consensus nomenclature for in vivo imaging of reversibly binding radioligands. J Cereb Blood Flow Metab. 2007;27:1533–9. https://doi.org/10.1038/sj.jcbfm.9600493.CrossRefPubMed

88.

McGowan DR, Macpherson RE, Hackett SL, Liu D, Gleeson FV, McKenna WG, et al. (18) F-fluoromisonidazole uptake in advanced stage non-small cell lung cancer: A voxel-by-voxel PET kinetics study. Med Phys. 2017;44:4665–76. https://doi.org/10.1002/mp.12416.CrossRefPubMedPubMedCentral

89.

Casciari JJ, Graham MM, Rasey JS. A modeling approach for quantifying tumor hypoxia with [F-18]fluoromisonidazole PET time-activity data. Med Phys. 1995;22:1127–39. https://doi.org/10.1118/1.597506.CrossRefPubMed

90.

Thorwarth D, Eschmann SM, Paulsen F, Alber M. A kinetic model for dynamic [18F]-Fmiso PET data to analyse tumour hypoxia. Phys Med Biol. 2005;50:2209–24. https://doi.org/10.1088/0031-9155/50/10/002.CrossRefPubMed

91.

Kelada OJ, Rockwell S, Zheng MQ, Huang Y, Liu Y, Booth CJ, et al. Quantification of tumor hypoxic fractions using positron emission tomography with [(18)F]Fluoromisonidazole ([(18)F]FMISO) kinetic analysis and invasive oxygen measurements. Mol Imaging Biol. 2017;19:893–902. https://doi.org/10.1007/s11307-017-1083-9.CrossRefPubMedPubMedCentral

92.

Grkovski M, Schwartz J, Gonen M, Schoder H, Lee NY, Carlin SD, et al. Feasibility of 18F-Fluoromisonidazole kinetic modeling in head and neck Cancer using shortened acquisition times. J Nucl Med. 2016;57:334–41. https://doi.org/10.2967/jnumed.115.160168.CrossRefPubMed

93.

Grkovski M, Lee NY, Schoder H, Carlin SD, Beattie BJ, Riaz N, et al. Monitoring early response to chemoradiotherapy with (18)F-FMISO dynamic PET in head and neck cancer. Eur J Nucl Med Mol Imaging. 2017;44:1682–91. https://doi.org/10.1007/s00259-017-3720-6.CrossRefPubMed

94.

Nehmeh SA, Schwartz J, Grkovski M, Yeung I, Laymon CM, Muzi M, et al. Inter-operator variability in compartmental kinetic analysis of (18)F-fluoromisonidazole dynamic PET. Clin Imaging. 2018;49:121–7. https://doi.org/10.1016/j.clinimag.2017.12.015.CrossRefPubMedPubMedCentral

95.

Busk M, Mortensen LS, Nordsmark M, Overgaard J, Jakobsen S, Hansen KV, et al. PET hypoxia imaging with FAZA: reproducibility at baseline and during fractionated radiotherapy in tumour-bearing mice. Eur J Nucl Med Mol Imaging. 2013;40:186–97. https://doi.org/10.1007/s00259-012-2258-x.CrossRefPubMed

96.

Lock S, Perrin R, Seidlitz A, Bandurska-Luque A, Zschaeck S, Zophel K, et al. Residual tumour hypoxia in head-and-neck cancer patients undergoing primary radiochemotherapy, final results of a prospective trial on repeat FMISO-PET imaging. Radiother Oncol. 2017;124:533–40. https://doi.org/10.1016/j.radonc.2017.08.010.CrossRefPubMed

97.

Lee N, Schoder H, Beattie B, Lanning R, Riaz N, McBride S, et al. Strategy of using intratreatment hypoxia imaging to selectively and safely guide radiation dose de-escalation concurrent with chemotherapy for locoregionally advanced human papillomavirus-related oropharyngeal carcinoma. Int J Radiat Oncol Biol Phys. 2016;96:9–17. https://doi.org/10.1016/j.ijrobp.2016.04.027.CrossRefPubMedPubMedCentral

98.

Bittner MI, Grosu AL. Hypoxia in head and neck tumors: characteristics and development during therapy. Front Oncol. 2013;3:223. https://doi.org/10.3389/fonc.2013.00223.CrossRefPubMedPubMedCentral

99.

Zschaeck S, Haase R, Abolmaali N, Perrin R, Stutzer K, Appold S, et al. Spatial distribution of FMISO in head and neck squamous cell carcinomas during radio-chemotherapy and its correlation to pattern of failure. Acta Oncol. 2015;54:1355–63. https://doi.org/10.3109/0284186X.2015.1074720.CrossRefPubMed

100.

Dirix P, Vandecaveye V, De Keyzer F, Stroobants S, Hermans R, Nuyts S. Dose painting in radiotherapy for head and neck squamous cell carcinoma: value of repeated functional imaging with (18)F-FDG PET, (18)F-fluoromisonidazole PET, diffusion-weighted MRI, and dynamic contrast-enhanced MRI. J Nucl Med. 2009;50:1020–7. https://doi.org/10.2967/jnumed.109.062638.CrossRefPubMed

101.

Lee N, Nehmeh S, Schoder H, Fury M, Chan K, Ling CC, et al. Prospective trial incorporating pre-/mid-treatment [18F]-misonidazole positron emission tomography for head-and-neck cancer patients undergoing concurrent chemoradiotherapy. Int J Radiat Oncol Biol Phys. 2009;75:101–8. https://doi.org/10.1016/j.ijrobp.2008.10.049.CrossRefPubMedPubMedCentral

102.

Thorwarth D, Eschmann SM, Paulsen F, Alber M. A model of reoxygenation dynamics of head-and-neck tumors based on serial 18F-fluoromisonidazole positron emission tomography investigations. Int J Radiat Oncol Biol Phys. 2007;68:515–21. https://doi.org/10.1016/j.ijrobp.2006.12.037.CrossRefPubMed

103.

Hicks RJ, Rischin D, Fisher R, Binns D, Scott AM, Peters LJ. Utility of FMISO PET in advanced head and neck cancer treated with chemoradiation incorporating a hypoxia-targeting chemotherapy agent. Eur J Nucl Med Mol Imaging. 2005;32:1384–91. https://doi.org/10.1007/s00259-005-1880-2.CrossRefPubMed

104.

Zegers CM, Hoebers FJ, van Elmpt W, Bons JA, Ollers MC, Troost EG, et al. Evaluation of tumour hypoxia during radiotherapy using [(18)F]HX4 PET imaging and blood biomarkers in patients with head and neck cancer. Eur J Nucl Med Mol Imaging. 2016;43:2139–46. https://doi.org/10.1007/s00259-016-3429-y.CrossRefPubMedPubMedCentral

105.

Bittner MI, Wiedenmann N, Bucher S, Hentschel M, Mix M, Weber WA, et al. Exploratory geographical analysis of hypoxic subvolumes using 18F-MISO-PET imaging in patients with head and neck cancer in the course of primary chemoradiotherapy. Radiother Oncol. 2013;108:511–6. https://doi.org/10.1016/j.radonc.2013.06.012.CrossRefPubMed

106.

Georg P, Andrzejewski P, Baltzer P, Daniel M, Wadsak W, Mitterhauser M, et al. Changes in tumor biology during Chemoradiation of cervix Cancer assessed by multiparametric MRI and hypoxia PET. Mol Imaging Biol. 2018;20:160–9. https://doi.org/10.1007/s11307-017-1087-5.CrossRefPubMed

107.

Schuetz M, Schmid MP, Potter R, Kommata S, Georg D, Lukic D, et al. Evaluating repetitive 18F-fluoroazomycin-arabinoside (18FAZA) PET in the setting of MRI guided adaptive radiotherapy in cervical cancer. Acta Oncol. 2010;49:941–7. https://doi.org/10.3109/0284186X.2010.510145.CrossRefPubMed

108.

Tachibana I, Nishimura Y, Shibata T, Kanamori S, Nakamatsu K, Koike R, et al. A prospective clinical trial of tumor hypoxia imaging with 18F-fluoromisonidazole positron emission tomography and computed tomography (F-MISO PET/CT) before and during radiation therapy. J Radiat Res. 2013;54:1078–84. https://doi.org/10.1093/jrr/rrt033.CrossRefPubMedPubMedCentral

109.

Koh WJ, Bergman KS, Rasey JS, Peterson LM, Evans ML, Graham MM, 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;33:391–8. https://doi.org/10.1016/0360-3016(95)00170-4.CrossRefPubMed

110.

Vera P, Bohn P, Edet-Sanson A, Salles A, Hapdey S, Gardin I, et al. Simultaneous positron emission tomography (PET) assessment of metabolism with (1)(8)F-fluoro-2-deoxy-d-glucose (FDG), proliferation with (1)(8)F-fluoro-thymidine (FLT), and hypoxia with (1)(8)fluoro-misonidazole (F-miso) before and during radiotherapy in patients with non-small-cell lung cancer (NSCLC): a pilot study. Radiother Oncol. 2011;98:109–16. https://doi.org/10.1016/j.radonc.2010.10.011.CrossRefPubMed

111.

Vera P, Thureau S, Chaumet-Riffaud P, Modzelewski R, Bohn P, Vermandel M, et al. Phase II study of a radiotherapy total dose increase in hypoxic lesions identified by (18)F-misonidazole PET/CT in patients with non-small cell lung carcinoma (RTEP5 study). J Nucl Med. 2017;58:1045–53. https://doi.org/10.2967/jnumed.116.188367.CrossRefPubMed

112.

Di Perri D, Lee JA, Bol A, Hanin FX, Janssens G, Labar D, et al. Evolution of [(18)F]fluorodeoxyglucose and [(18)F]fluoroazomycin arabinoside PET uptake distributions in lung tumours during radiation therapy. Acta Oncol. 2017;56:516–24. https://doi.org/10.1080/0284186X.2017.1287943.CrossRefPubMed

113.

Song C, Hong BJ, Bok S, Lee CJ, Kim YE, Jeon SR, et al. Real-time tumor oxygenation changes after single high-dose radiation therapy in orthotopic and subcutaneous lung cancer in mice: clinical implication for stereotactic ablative radiation therapy schedule optimization. Int J Radiat Oncol Biol Phys. 2016;95:1022–31. https://doi.org/10.1016/j.ijrobp.2016.01.064.CrossRefPubMed

114.

Boeke S, Thorwarth D, Monnich D, Pfannenberg C, Reischl G, La Fougere C, et al. Geometric analysis of loco-regional recurrences in relation to pre-treatment hypoxia in patients with head and neck cancer. Acta Oncol. 2017;56:1571–6. https://doi.org/10.1080/0284186X.2017.1372626.CrossRefPubMed

115.

Henriques de Figueiredo B, Merlin T, de Clermont-Gallerande H, Hatt M, Vimont D, Fernandez P, et al. Potential of [18F]-fluoromisonidazole positron-emission tomography for radiotherapy planning in head and neck squamous cell carcinomas. Strahlenther Onkol. 2013;189:1015–9. https://doi.org/10.1007/s00066-013-0454-7.CrossRefPubMed

116.

Abolmaali N, Haase R, Koch A, Zips D, Steinbach J, Baumann M, et al. Two or four hour [(1)(8)F]FMISO-PET in HNSCC. When is the contrast best? Nuklearmedizin. 2011;50:22–7. https://doi.org/10.3413/nukmed-00328-10-07.CrossRefPubMed

117.

Overgaard J, Hansen HS, Overgaard M, Bastholt L, Berthelsen A, Specht L, et al. A randomized double-blind phase III study of nimorazole as a hypoxic radiosensitizer of primary radiotherapy in supraglottic larynx and pharynx carcinoma. Results of the Danish head and neck Cancer study (DAHANCA) protocol 5-85. Radiother Oncol. 1998;46:135–46.CrossRefPubMed

118.

Overgaard J. Hypoxic modification of radiotherapy in squamous cell carcinoma of the head and neck—a systematic review and meta-analysis. Radiother Oncol. 2011;100:22–32. https://doi.org/10.1016/j.radonc.2011.03.004.CrossRefPubMed

119.

Thorwarth D, Eschmann SM, Paulsen F, Alber M. Hypoxia dose painting by numbers: a planning study. Int J Radiat Oncol Biol Phys. 2007;68:291–300. https://doi.org/10.1016/j.ijrobp.2006.11.061.CrossRefPubMed

120.

Welz S, Monnich D, Pfannenberg C, Nikolaou K, Reimold M, La Fougere C, et al. Prognostic value of dynamic hypoxia PET in head and neck cancer: results from a planned interim analysis of a randomized phase II hypoxia-image guided dose escalation trial. Radiother Oncol. 2017;124:526–32. https://doi.org/10.1016/j.radonc.2017.04.004.CrossRefPubMed

Titel: Longitudinal PET imaging of tumor hypoxia during the course of radiotherapy
verfasst von: Sonja Stieb
Afroditi Eleftheriou
Geoffrey Warnock
Matthias Guckenberger
Oliver Riesterer
Publikationsdatum: 20.08.2018
Verlag: Springer Berlin Heidelberg
Erschienen in: European Journal of Nuclear Medicine and Molecular Imaging / Ausgabe 12/2018
Print ISSN: 1619-7070
Elektronische ISSN: 1619-7089
DOI: https://doi.org/10.1007/s00259-018-4116-y

Springer Medizin

Abstract

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