Multiparametric imaging of patient and tumour heterogeneity in non-small-cell lung cancer: quantification of tumour hypoxia, metabolism and perfusion

European Journal of Nuclear Medicine and Molecular Imaging

Volumn 43, Issue 2, 2016, Pages 240-248

  van Elmpt, Wouter ^a   Zegers, Catharina M L ^a   Reymen, Bart ^a   Even, Aniek J G ^a   Dingemans, Anne Marie C ^a   Oellers, Michel ^a   Wildberger, Joachim E ^a   Mottaghy, Felix M ^a,b   Das, Marco ^a   Troost, Esther G C ^a   Lambin, Philippe ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

Author keywords

DCE CT; FDG PET; HX4; Hypoxia PET; Image analysis; Multiparametric

Indexed keywords

ARTICLE; BLOOD FLOW; BLOOD VOLUME; CANCER PATIENT; CLINICAL ARTICLE; CLINICAL TRIAL (TOPIC); COMPUTER ASSISTED EMISSION TOMOGRAPHY; COMPUTER ASSISTED TOMOGRAPHY; CONTRAST ENHANCEMENT; FEMALE; FOUR DIMENSIONAL COMPUTED TOMOGRAPHY; HUMAN; HYPOXIA; MALE; METABOLISM; NON SMALL CELL LUNG CANCER; OXYGENATION; PERFUSION; POSITRON EMISSION TOMOGRAPHY; RADIOLOGICAL PARAMETERS; TUMOR VASCULARIZATION; TUMOR VOLUME; CELL HYPOXIA; CLINICAL TRIAL; DIAGNOSTIC IMAGING; LUNG TUMOR; MULTIMODAL IMAGING; OXYGEN CONSUMPTION; PATHOLOGY; X-RAY COMPUTED TOMOGRAPHY;

3-FLUORO-2-(4-((2-NITRO-1H-IMIDAZOL-1-YL)METHYL)-1H-1,2,3-TRIAZOL-1-YL)PROPAN-1-OL; FLUORODEOXYGLUCOSE F 18; NITROIMIDAZOLE DERIVATIVE; OXYGEN; RADIOPHARMACEUTICAL AGENT; TRIAZOLE DERIVATIVE;

CARCINOMA, NON-SMALL-CELL LUNG; CELL HYPOXIA; FEMALE; FLUORODEOXYGLUCOSE F18; HUMANS; LUNG NEOPLASMS; MALE; MULTIMODAL IMAGING; NITROIMIDAZOLES; OXYGEN; OXYGEN CONSUMPTION; POSITRON-EMISSION TOMOGRAPHY; RADIOPHARMACEUTICALS; TOMOGRAPHY, X-RAY COMPUTED; TRIAZOLES;

EID: 84952976175     PISSN: 16197070     EISSN: 16197089     Source Type: Journal    
DOI: 10.1007/s00259-015-3169-4     Document Type: Article

References (50)

1. Lambin P, Petit SF, Aerts HJ, van Elmpt WJ, Oberije CJ, Starmans MH, et al. The ESTRO Breur Lecture 2009. From population to voxel-based radiotherapy: exploiting intra-tumour and intra-organ heterogeneity for advanced treatment of non-small cell lung cancer. Radiother Oncol. 2010;96:145–52. doi:10.1016/j.radonc.2010.07.001.
2. van Elmpt W, Zegers CM, Das M, De Ruysscher D. Imaging techniques for tumour delineation and heterogeneity quantification of lung cancer: overview of current possibilities. J Thorac Dis. 2014;6:319–27. doi:10.3978/j.issn.2072-1439.2013.08.62.
3. Differding S, Hanin FX, Gregoire V. PET imaging biomarkers in head and neck cancer. Eur J Nucl Med Mol Imaging. 2015;42:613–22. doi:10.1007/s00259-014-2972-7.
4. O’Connor JP, Rose CJ, Waterton JC, Carano RA, Parker GJ, Jackson A. Imaging intratumor heterogeneity: role in therapy response, resistance, and clinical outcome. Clin Cancer Res. 2015;21:249–57. doi:10.1158/1078-0432.CCR-14-0990.
5. Yankeelov TE, Abramson RG, Quarles CC. Quantitative multimodality imaging in cancer research and therapy. Nat Rev Clin Oncol. 2014;11:670–80. doi:10.1038/nrclinonc.2014.134.
6. Sauter AW, Schwenzer N, Divine MR, Pichler BJ, Pfannenberg C. Image-derived biomarkers and multimodal imaging strategies for lung cancer management. Eur J Nucl Med Mol Imaging. 2015;42:634–43. doi:10.1007/s00259-014-2974-5.
7. Rijken PF, Bernsen HJ, Peters JP, Hodgkiss RJ, Raleigh JA, van der Kogel AJ. Spatial relationship between hypoxia and the (perfused) vascular network in a human glioma xenograft: a quantitative multi-parameter analysis. Int J Radiat Oncol Biol Phys. 2000;48:571–82.
8. Usmanij EA, de Geus-Oei LF, Troost EG, Peters-Bax L, van der Heijden EH, Kaanders JH, et al. 18F-FDG PET early response evaluation of locally advanced non-small cell lung cancer treated with concomitant chemoradiotherapy. J Nucl Med. 2013;54:1528–34. doi:10.2967/jnumed.112.116921.
9. van Elmpt W, Ollers M, Dingemans AM, Lambin P, De Ruysscher D. Response assessment using 18F-FDG PET early in the course of radiotherapy correlates with survival in advanced-stage non-small cell lung cancer. J Nucl Med. 2012;53:1514–20. doi:10.2967/jnumed.111.102566.
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. doi:10.1038/nrclinonc.2012.171.
11. Peeters SG, Zegers CM, Lieuwes NG, van Elmpt W, Eriksson J, van Dongen GA, et al. A comparative study of the hypoxia PET tracers [(18)F]HX4, [(18)F]FAZA, and [(18)F]FMISO in a preclinical tumor model. Int J Radiat Oncol Biol Phys. 2015;91:351–9. doi:10.1016/j.ijrobp.2014.09.045.
12. Peeters SG, Zegers CM, Yaromina A, van Elmpt W, Dubois L, Lambin P. Current pre-clinical and clinical applications of hypoxia PET imaging using 2-nitroimidazoles. Q J Nucl Med Mol Imaging. 2015;59:39–57.
13. Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature. 2011;473:298–307. doi:10.1038/nature10144.
14. Chang YC, Yu CJ, Chen CM, Hu FC, Hsu HH, Tseng WY, et al. Dynamic contrast-enhanced MRI in advanced nonsmall-cell lung cancer patients treated with first-line bevacizumab, gemcitabine, and cisplatin. J Magn Reson Imaging. 2012;36:387–96. doi:10.1002/jmri.23660.
15. Ng QS, Goh V. Angiogenesis in non-small cell lung cancer: imaging with perfusion computed tomography. J Thorac Imaging. 2010;25:142–50. doi:10.1097/RTI.0b013e3181d29ccf.
16. Wilson WR, Hay MP. Targeting hypoxia in cancer therapy. Nat Rev Cancer. 2011;11:393–410. doi:10.1038/nrc3064.
17. van Elmpt W, De Ruysscher D, van der Salm A, Lakeman A, van der Stoep J, Emans D, et al. The PET-boost randomised phase II dose-escalation trial in non-small cell lung cancer. Radiother Oncol. 2012;104:67–71. doi:10.1016/j.radonc.2012.03.005.
18. 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. doi:10.1016/j.ijrobp.2006.11.061.
19. Meijer G, Steenhuijsen J, Bal M, De Jaeger K, Schuring D, Theuws J. Dose painting by contours versus dose painting by numbers for stage II/III lung cancer: practical implications of using a broad or sharp brush. Radiother Oncol. 2011;100:396–401. doi:10.1016/j.radonc.2011.08.048.
20. Even AJ, van der Stoep J, Zegers CM, Reymen B, Troost EG, Lambin P, et al. PET-based dose painting in non-small cell lung cancer: comparing uniform dose escalation with boosting hypoxic and metabolically active sub-volumes. Radiother Oncol. 2015. doi:10.1016/j.radonc.2015.07.013.
21. Boellaard R, O’Doherty MJ, Weber WA, Mottaghy FM, Lonsdale MN, Stroobants SG, et al. FDG PET and PET/CT: EANM procedure guidelines for tumour PET imaging: version 1.0. Eur J Nucl Med Mol Imaging. 2010;37:181–200. doi:10.1007/s00259-009-1297-4.
22. van Elmpt W, Das M, Hullner M, Sharifi H, Zegers CM, Reymen B, et al. Characterization of tumor heterogeneity using dynamic contrast enhanced CT and FDG-PET in non-small cell lung cancer. Radiother Oncol. 2013;109:65–70. doi:10.1016/j.radonc.2013.08.032.
23. Klotz E, Haberland U, Glatting G, Schoenberg SO, Fink C, Attenberger U, et al. Technical prerequisites and imaging protocols for CT perfusion imaging in oncology. Eur J Radiol. 2015. doi:10.1016/j.ejrad.2015.06.010.
24. Miles KA, Lee TY, Goh V, Klotz E, Cuenod C, Bisdas S, et al. Current status and guidelines for the assessment of tumour vascular support with dynamic contrast-enhanced computed tomography. Eur Radiol. 2012;22:1430–41. doi:10.1007/s00330-012-2379-4.
25. Zegers CM, van Elmpt W, Wierts R, Reymen B, Sharifi H, Ollers MC, et al. Hypoxia imaging with [18F]HX4 PET in NSCLC patients: defining optimal imaging parameters. Radiother Oncol. 2013;109:58–64. doi:10.1016/j.radonc.2013.08.031.
26. Hardcastle N, van Elmpt W, De Ruysscher D, Bzdusek K, Tome WA. Accuracy of deformable image registration for contour propagation in adaptive lung radiotherapy. Radiat Oncol. 2013;8:243. doi:10.1186/1748-717X-8-243.
27. Janssens G, de Xivry JO, Fekkes S, Dekker A, Macq B, Lambin P, et al. Evaluation of nonrigid registration models for interfraction dose accumulation in radiotherapy. Med Phys. 2009;36:4268–76.
28. Spijkerman J, Fontanarosa D, Das M, Van Elmpt W. Validation of nonrigid registration in pretreatment and follow-up PET/CT scans for quantification of tumor residue in lung cancer patients. J Appl Clin Med Phys. 2014;15:4847. doi:10.1120/jacmp.v15i4.4847.
29. Aerts HJ, Bussink J, Oyen WJ, van Elmpt W, Folgering AM, Emans D, et al. Identification of residual metabolic-active areas within NSCLC tumours using a pre-radiotherapy FDG-PET-CT scan: a prospective validation. Lung Cancer. 2012;75:73–6. doi:10.1016/j.lungcan.2011.06.003.
30. Huellner MW, Collen TD, Gut P, Winterhalder R, Pauli C, Diebold J, et al. Multiparametric PET/CT-perfusion does not add significant additional information for initial staging in lung cancer compared with standard PET/CT. EJNMMI Res. 2014;4:6. doi:10.1186/2191-219X-4-6.
31. Gronroos TJ, Lehtio K, Soderstrom KO, Kronqvist P, Laine J, Eskola O, et al. Hypoxia, blood flow and metabolism in squamous-cell carcinoma of the head and neck: correlations between multiple immunohistochemical parameters and PET. BMC Cancer. 2014;14:876. doi:10.1186/1471-2407-14-876.
32. 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. doi:10.1016/j.ijrobp.2003.12.014.
33. Shi J, Schmid-Bindert G, Fink C, Sudarski S, Apfaltrer P, Pilz LR, et al. Dynamic volume perfusion CT in patients with lung cancer: baseline perfusion characteristics of different histological subtypes. Eur J Radiol. 2013;82:e894–900. doi:10.1016/j.ejrad.2013.08.023.
34. Sudarski S, Shi J, Schmid-Bindert G, Manegold C, Pilz LR, Zhou C, et al. Dynamic volume perfusion CT parameters versus RECIST for the prediction of outcome in lung cancer patients treated with conventional chemotherapy. J Thorac Oncol. 2015;10:164–71. doi:10.1097/JTO.0000000000000376.
35. Goh V, Ng QS, Miles K. Computed tomography perfusion imaging for therapeutic assessment: has it come of age as a biomarker in oncology? Invest Radiol. 2012;47:2–4. doi:10.1097/RLI.0b013e318229ff3e.
36. Garcia-Figueiras R, Goh VJ, Padhani AR, Baleato-Gonzalez S, Garrido M, Leon L, et al. CT perfusion in oncologic imaging: a useful tool? AJR Am J Roentgenol. 2013;200:8–19. doi:10.2214/AJR.11.8476.
37. Bradshaw TJ, Bowen SR, Jallow N, Forrest LJ, Jeraj R. Heterogeneity in intratumor correlations of 18F-FDG, 18F-FLT, and 61Cu-ATSM PET in canine sinonasal tumors. J Nucl Med. 2013;54:1931–7. doi:10.2967/jnumed.113.121921.
38. Hansen AE, Kristensen AT, Law I, McEvoy FJ, Kjaer A, Engelholm SA. Multimodality functional imaging of spontaneous canine tumors using 64Cu-ATSM and 18FDG PET/CT and dynamic contrast enhanced perfusion CT. Radiother Oncol. 2012;102:424–8. doi:10.1016/j.radonc.2011.10.021.
39. Nyflot MJ, Harari PM, Yip S, Perlman SB, Jeraj R. Correlation of PET images of metabolism, proliferation and hypoxia to characterize tumor phenotype in patients with cancer of the oropharynx. Radiother Oncol. 2012;105:36–40. doi:10.1016/j.radonc.2012.09.012.
40. Zegers CM, van Elmpt W, Reymen B, Even AJ, Troost EG, Ollers MC, et al. In vivo quantification of hypoxic and metabolic status of NSCLC tumors using [18F]HX4 and [18F]FDG-PET/CT imaging. Clin Cancer Res. 2014;20:6389–97. doi:10.1158/1078-0432.CCR-14-1524.
41. Sauter AW, Spira D, Schulze M, Pfannenberg C, Hetzel J, Reimold M, et al. Correlation between [18F]FDG PET/CT and volume perfusion CT in primary tumours and mediastinal lymph nodes of non-small-cell lung cancer. Eur J Nucl Med Mol Imaging. 2013;40:677–84. doi:10.1007/s00259-012-2318-2.
42. Sauter AW, Winterstein S, Spira D, Hetzel J, Schulze M, Mueller M, et al. Multifunctional profiling of non-small cell lung cancer using 18F-FDG PET/CT and volume perfusion CT. J Nucl Med. 2012;53:521–9. doi:10.2967/jnumed.111.097865.
43. Schuurbiers OC, Meijer TW, Kaanders JH, Looijen-Salamon MG, de Geus-Oei LF, van der Drift MA, et al. Glucose metabolism in NSCLC is histology-specific and diverges the prognostic potential of 18FDG-PET for adenocarcinoma and squamous cell carcinoma. J Thorac Oncol. 2014;9:1485–93. doi:10.1097/JTO.0000000000000286.
44. 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. doi:10.1016/j.radonc.2012.08.019.
45. 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. doi:10.2967/jnumed.112.109330.
46. 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. doi:10.1016/0360-3016(95)00170-4.
47. Zegers CM, van Elmpt W, Szardenings K, Kolb H, Waxman A, Subramaniam RM, et al. Repeatability of hypoxia PET imaging using [F]HX4 in lung and head and neck cancer patients: a prospective multicenter trial. Eur J Nucl Med Mol Imaging. 2015. doi:10.1007/s00259-015-3100-z.
48. Bollineni VR, Kerner GS, Pruim J, Steenbakkers RJ, Wiegman EM, Koole MJ, et al. PET imaging of tumor hypoxia using 18F-fluoroazomycin arabinoside in stage III-IV non-small cell lung cancer patients. J Nucl Med. 2013;54:1175–80. doi:10.2967/jnumed.112.115014.
49. Klaassen R, Bennink RJ, van Tienhoven G, Bijlsma MF, Besselink MG, van Berge Henegouwen MI, et al. Feasibility and repeatability of PET with the hypoxia tracer [F]HX4 in oesophageal and pancreatic cancer. Radiother Oncol. 2015;116:94–99. doi:10.1016/j.radonc.2015.05.009.
50. Monnich D, Troost EG, Kaanders JH, Oyen WJ, Alber M, Thorwarth D. Modelling and simulation of the influence of acute and chronic hypoxia on [18F]fluoromisonidazole PET imaging. Phys Med Biol. 2012;57:1675–84. doi:10.1088/0031-9155/57/6/1675.