Prognostic value of post-induction chemotherapy 18F-FDG PET-CT in stage II/III non-small cell lung cancer before (chemo-) radiation

Autoři: Julien Ganem aff001;  Sebastien Thureau aff001;  Pierrick Gouel aff001;  Bernard Dubray aff002;  Mathieu Salaun aff003;  Edgar Texte aff001;  Pierre Vera aff001
Působiště autorů: Department of Nuclear Medicine, Henri Becquerel Cancer Centre and Rouen University Hospital, Rouen, France aff001;  Department of Radiation Oncology and Medical Physics, Henri Becquerel Cancer Centre and Rouen University Hospital, Rouen, France aff002;  QuantIF-LITIS, EA 4108-FR, CNRS, University of Rouen, Rouen, France aff003;  Department of Pneumology, Rouen University Hospital, Rouen, France aff004
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article



The purpose of our present study was to assess the prognostic impact of FDG PET-CT after induction chemotherapy for patients with inoperable non-small-cell lung cancer (NSCLC).

Material and methods

This retrospective study included 50 patients with inoperable stage II/III NSCLC from January 2012 to July 2015. They were treated for curative intent with induction chemotherapy, followed by concomitant chemoradiation therapy or sequential radiation therapy. FDG PET-CT scans were acquired at initial staging (PET1) and after the last cycle of induction therapy (PET2). Five parameters were evaluated on both scans: SUVmax, SUVpeak, SUVmean, TLG, MTV, and their respective deltas. The prognostic value of each parameter for overall survival (OS) and progression-free survival (PFS) was evaluated with Cox proportional-hazards regression models.


Median follow-up was 19 months. PET1 parameters, clinical and histopathological data were not predictive of the outcome. TLG2 and ΔTLG were prognostic factors for OS. TLG2 was the only prognostic factor for PFS. For OS, log-rank test showed that there was a better prognosis for patients with TLG2< 69g (HR = 7.1, 95%CI 2.8–18, p = 0.002) and for patients with ΔTLG< -81% after induction therapy (HR = 3.8, 95%CI 1.5–9.6, p = 0.02). After 2 years, the survival rate was 89% for the patients with low TLG2 vs 52% for the others. We also evaluated a composite parameter considering both MTV2 and ΔSUVmax. Patients with MTV2> 23cc and ΔSUVmax> -55% had significantly shorter OS than the other patients (HR = 5.7, 95%CI 2.1–15.4, p< 0.01).


Post-induction FDG PET might be an added value to assess the patients’ prognosis in inoperable stage II/III NSCLC. TLG, ΔTLG as well as the association of MTV and ΔSUVmax seemed to be valuable parameters, more accurate than clinical, pathological or pretherapeutic imaging data.

Klíčová slova:

Cancer chemotherapy – Cancer treatment – Lesions – Non-small cell lung cancer – Prognosis – Radiation therapy – Chemoradiotherapy


1. Boyle P, Ferlay J. Cancer Incidence and Mortality in Europe, 2004. Ann Oncol. 2005;16(3):481–8. doi: 10.1093/annonc/mdi098 15718248

2. Farray D, Mirkovic N, Albain KS, Multimodality Therapy for Stage III Non-Small-Cell Lung Cancer. J Clin Oncol. 2005;23(14):3257–69. doi: 10.1200/JCO.2005.03.008 15886313

3. Jerusalem G, Hustinx R, Beguin Y, Fillet G.The Value of Positron Emission Tomography (PET) Imaging in Disease Staging and Therapy Assessment. Ann Oncol. 2002;13 Suppl 4:227–34.

4. Wahl RL, Jacene H, Kasamon Y, Lodge MA. From RECIST to PERCIST: Evolving Considerations for PET Response Criteria in Solid Tumors. J Nucl Med. 2009;50 Suppl 1:122S–50S.

5. Calais J, Thureau S, Dubray B, Modzelewski R, Thiberville L, Gardin I, et al. Areas of High 18F-FDG Uptake on Preradiotherapy PET/CT Identify Preferential Sites of Local Relapse after Chemoradiotherapy for Non-Small Cell Lung Cancer. J Nucl Med. 2015;56(2):196–203. doi: 10.2967/jnumed.114.144253 25572091

6. Machtay M, Duan F, Siegel BA, Snyder BS, Gorelick JJ, Reddin JS, et al. Prediction of Survival by [18F]fluorodeoxyglucose Positron Emission Tomography in Patients with Locally Advanced Non-Small-Cell Lung Cancer Undergoing Definitive Chemoradiation Therapy: Results of the ACRIN 6668/RTOG 0235 Trial. J Clin Oncol. 2013;31(30):3823–30. doi: 10.1200/JCO.2012.47.5947 24043740

7. Abramyuk A, Tokalov S, Zöphel K, Koch A, Szluha Lazanyi K, Gillham C, et al. Is Pre-Therapeutical FDG-PET/CT Capable to Detect High Risk Tumor Subvolumes Responsible for Local Failure in Non-Small Cell Lung Cancer?. Radiother Oncol. 2009;91(3):399–404. doi: 10.1016/j.radonc.2009.01.003 19168248

8. Na F, Wang J, Li C, Deng L, Xue J, Lu Y.Primary Tumor Standardized Uptake Value Measured on F18-Fluorodeoxyglucose Positron Emission Tomography Is of Prediction Value for Survival and Local Control in Non-Small-Cell Lung Cancer Receiving Radiotherapy: Meta-Analysis. J Thorac Oncol. 2014;9(6):834–42. doi: 10.1097/JTO.0000000000000185 24787963

9. Borst GR, Belderbos JS, Boellaard R, Comans EF, De Jaeger K, Lammertsma AA, et al. Standardised FDG Uptake: A Prognostic Factor for Inoperable Non-Small Cell Lung Cancer. Eur J Cancer. 2005;41(11):1533–41. doi: 10.1016/j.ejca.2005.03.026 15953716

10. Paesmans M, Berghmans T, Dusart M, Garcia C, Hossein-Foucher C, Lafitte JJ, et al. Primary Tumor Standardized Uptake Value Measured on Fluorodeoxyglucose Positron Emission Tomography Is of Prognostic Value for Survival in Non-Small Cell Lung Cancer: Update of a Systematic Review and Meta-Analysis by the European Lung Cancer Working Party for the International Association for the Study of Lung Cancer Staging Project. J Thorac Oncol. 2010;5(5):612–9. doi: 10.1097/JTO.0b013e3181d0a4f5 20234323

11. Dooms C, Verbeken E, Stroobants S, Nackaerts K, De Leyn P, Vansteenkiste J. Prognostic Stratification of Stage IIIA-N2 Non-Small-Cell Lung Cancer after Induction Chemotherapy: A Model Based on the Combination of Morphometric-Pathologic Response in Mediastinal Nodes and Primary Tumor Response on Serial 18-Fluoro-2-Deoxy-Glucose Positron Emission Tomography. J Clin Oncol. 2008;26(7):1128–34. doi: 10.1200/JCO.2007.13.9550 18309948

12. Tanvetyanon T, Eikman EA, Sommers E, Robinson L, Boulware D, Bepler G. Computed Tomography Response, but Not Positron Emission Tomography Scan Response, Predicts Survival after Neoadjuvant Chemotherapy for Resectable Non-Small-Cell Lung Cancer. J Clin Oncol. 2008;26(28):4610–6. doi: 10.1200/JCO.2008.16.9383 18824709

13. Soussan M, Chouahnia K, Maisonobe JA, Boubaya M, Eder V, Morère JF, et al. Prognostic Implications of Volume-Based Measurements on FDG PET/CT in Stage III Non-Small-Cell Lung Cancer after Induction Chemotherapy. Eur J Nucl Med Mol Imaging. 2013;40(5):668–76. doi: 10.1007/s00259-012-2321-7 23306807

14. 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 F-Miso PET/CT in Patients with Non-Small Cell Lung Carcinoma (RTEP5 Study). J Nucl Med. 2017;58(7):1045–1053. doi: 10.2967/jnumed.116.188367 28254869

15. Boellaard R, Delgado-Bolton R, Oyen WJ, Giammarile F, Tatsch K, Eschner W, et al. FDG PET/CT: EANM Procedure Guidelines for Tumour Imaging: Version 2.0. Eur J Nucl Med Mol Imaging. 2015;42(2):328–54. doi: 10.1007/s00259-014-2961-x 25452219

16. Berghmans T, Dusart M, Paesmans M, Hossein-Foucher C, Buvat I, Castaigne C, et al. Primary Tumor Standardized Uptake Value (SUVmax) Measured on Fluorodeoxyglucose Positron Emission Tomography (FDG-PET) Is of Prognostic Value for Survival in Non-Small Cell Lung Cancer (NSCLC): A Systematic Review and Meta-Analysis (MA) by the European Lung Cancer Working Party for the IASLC Lung Cancer Staging Project. J Thorac Oncol. 2008;3(1):6–12. doi: 10.1097/JTO.0b013e31815e6d6b 18166834

17. Hyun SH, Ahn HK, Ahn MJ, Ahn YC, Kim J, Shim YM, et al. Volume-Based Assessment With 18F-FDG PET/CT Improves Outcome Prediction for Patients With Stage IIIA-N2 Non-Small Cell Lung Cancer. AJR Am J Roentgenol. 2015;205(3):623–8. doi: 10.2214/AJR.14.13847 26295651

18. Chen HH, Chiu NT, Su WC, Guo HR, Lee BF. Prognostic Value of Whole-Body Total Lesion Glycolysis at Pretreatment FDG PET/CT in Non-Small Cell Lung Cancer. Radiology. 2012;264(2):559–66. doi: 10.1148/radiol.12111148 22692034

19. Im HJ, Pak K, Cheon GJ, Kang KW, Kim IJ, Chung JK, et al. Prognostic Value of Volumetric Parameters of (18)F-FDG PET in Non-Small-Cell Lung Cancer: A Meta-Analysis. Eur J Nucl Med Mol Imaging. 2015 Feb;42(2):241–51. doi: 10.1007/s00259-014-2903-7 25193652

20. Hoang JK, Hoagland LF, Coleman RE, Coan AD, Herndon JE 2nd, Patz EF Jr. Prognostic Value of Fluorine-18 Fluorodeoxyglucose Positron Emission Tomography Imaging in Patients with Advanced-Stage Non-Small-Cell Lung Carcinoma. J Clin Oncol. 2008;26(9):1459–64. doi: 10.1200/JCO.2007.14.3628 18349396

21. Shang J, Ling X, Zhang L, Tang Y, Xiao Z, Cheng Y, et al. Comparison of RECIST, EORTC Criteria and PERCIST for Evaluation of Early Response to Chemotherapy in Patients with Non-Small-Cell Lung Cancer. Eur J Nucl Med Mol Imaging. 2016;43(11):1945–53. doi: 10.1007/s00259-016-3420-7 27236466

22. Hellwig D, Graeter TP, Ukena D, Georg T, Kirsch CM, Schäfers HJ. Value of F-18-Fluorodeoxyglucose Positron Emission Tomography after Induction Therapy of Locally Advanced Bronchogenic Carcinoma. J Thorac Cardiovasc Surg. 2004;128(6):892–9. doi: 10.1016/j.jtcvs.2004.07.031 15573074

23. Lee HY, Lee HJ, Kim YT, Kang CH, Jang BG, Chung DH, et al. Value of Combined Interpretation of Computed Tomography Response and Positron Emission Tomography Response for Prediction of Prognosis after Neoadjuvant Chemotherapy in Non-Small Cell Lung Cancer. J Thorac Oncol. 2010;5(4):497–503. doi: 10.1097/JTO.0b013e3181d2efe7 20195167

24. Eschmann SM, Friedel G, Paulsen F, Reimold M, Hehr T, Dittmann H, et al. Repeat 18F-FDG PET for Monitoring Neoadjuvant Chemotherapy in Patients with Stage III Non-Small Cell Lung Cancer. Lung Cancer. 2007; 55(2):165–71. doi: 10.1016/j.lungcan.2006.09.028 17129635

25. Soussan M, Cyrta J, Pouliquen C, Chouahnia K, Orlhac F, Martinod E, et al. Fluorine 18 Fluorodeoxyglucose PET/CT Volume-Based Indices in Locally Advanced Non-Small Cell Lung Cancer: Prediction of Residual Viable Tumor after Induction Chemotherapy. Radiology. 2014;272(3):875–84. doi: 10.1148/radiol.14132191 24761836

26. Kim KR, Shim HJ, Hwang JE, Cho SH, Chung IJ, Park KS, et al. The Role of Interim FDG PET-CT after Induction Chemotherapy as a Predictor of Concurrent Chemoradiotherapy Efficacy and Prognosis for Head and Neck Cancer. Eur J Nucl Med Mol Imaging. 2017 Sep 22.

27. Vera P, Mezzani-Saillard S, Edet-Sanson A, Ménard JF, Modzelewski R, Thureau S, et al. FDG PET during Radiochemotherapy Is Predictive of Outcome at 1 Year in Non-Small-Cell Lung Cancer Patients: A Prospective Multicentre Study (RTEP2). Eur J Nucl Med Mol Imaging. 2014;41(6):1057–65. doi: 10.1007/s00259-014-2687-9 24562641

28. Study of Interest of Personalized Radiotherapy Dose Redistribution in Patients With Stage III NSCLC—

29. Study of Positron Emission Tomography and Computed Tomography in Guiding Radiation Therapy in Patients With Stage III Non-Small Cell Lung Cancer—

30. Chaft JE, Dunphy M, Naidoo J, Travis WD, Hellmann M, Woo K, et al.Adaptive Neoadjuvant Chemotherapy Guided by (18)F-FDG PET in Resectable Non-Small Cell Lung Cancers: The NEOSCAN Trial. J Thorac Oncol. 2016 Apr;11(4):537–44. doi: 10.1016/j.jtho.2015.12.104 26724474

31. Seyedin SN, Schoenhals JE, Lee DA, Cortez MA, Wang X, Niknam S, et al. Strategies for Combining Immunotherapy with Radiation for Anticancer Therapy. Immunotherapy. 2015;7(9):967–980. doi: 10.2217/imt.15.65 26310908

32. Tang C, Wang X, Soh H, Seyedin S, Cortez MA Krishnan S, et al. Combining Radiation and Immunotherapy: A New Systemic Therapy for Solid Tumors? Cancer Immunol Res. 2014;2(9):831–8 doi: 10.1158/2326-6066.CIR-14-0069 25187273

33. Golden EB, Demaria S, Schiff PB, Chachoua A, Formenti SC.An Abscopal Response to Radiation and Ipilimumab in a Patient with Metastatic Non-Small Cell Lung Cancer. Cancer Immunol Res. 2013;1(6):365–72. doi: 10.1158/2326-6066.CIR-13-0115 24563870

34. Cisplatin and Etoposide Plus Radiation Followed By Nivolumab/Placebo For Locally Advanced NSCLC—

35. Anti-PD-L1 in Stage IIIA(N2) NSCLC—

36. van den Heuvel MM, Verheij M, Boshuizen R, Belderbos J, Dingemans AM, De Ruysscher D, et al. NHS-IL2 Combined with Radiotherapy: Preclinical Rationale and Phase Ib Trial Results in Metastatic Non-Small Cell Lung Cancer Following First-Line Chemotherapy J Transl Med. 2015;13:32. doi: 10.1186/s12967-015-0397-0 25622640

Článek vyšel v časopise


2019 Číslo 10
Nejčtenější tento týden