Multicentric development and evaluation of [ 18 F]FDG PET/CT and CT radiomic models to predict regional and/or distant recurrence in early-stage non-small cell lung cancer treated by stereotactic body radiation therapy
[en] Purpose To develop machine learning models to predict regional and/or distant recurrence in patients with early-stage non-small cell lung cancer (ES-NSCLC) after stereotactic body radiation therapy (SBRT) using [ 18 F]FDG PET/CT and CT radiomics combined with clinical and dosimetric parameters. Methods We retrospectively collected 464 patients (60% for training and 40% for testing) from University Hospital of Liège and 63 patients from University Hospital of Brest (external testing set) with ES-NSCLC treated with SBRT between 2010 and 2020 and who had undergone pretreatment [ 18 F]FDG PET/CT and planning CT. Radiomic features were extracted using the PyRadiomics toolbox®. The ComBat harmonization method was applied to reduce the batch effect between centers. Clinical, radiomic, and combined models were trained and tested using a neural network approach to predict regional and/ or distant recurrence. Results In the training (n = 273) and testing sets (n = 191 and n = 63), the clinical model achieved moderate performances to predict regional and/or distant recurrence with C-statistics from 0.53 to 0.59 (95% CI, 0.41, 0.67). The radiomic (origi-nal_firstorder_Entropy, original_gldm_LowGrayLevelEmphasis and original_glcm_DifferenceAverage) model achieved higher predictive ability in the training set and kept the same performance in the testing sets, with C-statistics from 0.70 to 0.78 (95% CI, 0.63, 0.88) while the combined model performs moderately well with C-statistics from 0.50 to 0.62 (95% CI, 0.37, 0.69). Conclusion Radiomic features extracted from pre-SBRT analog and digital [ 18 F]FDG PET/CT outperform clinical parameters in the prediction of regional and/or distant recurrence and to discuss an adjuvant systemic treatment in ES-NSCLC. Prospective validation of our models should now be carried out.
Disciplines :
Radiology, nuclear medicine & imaging
Author, co-author :
Lucia, François ; Département de Physique Médicale > Service médical de médecine nucléaire et imagerie onco ; Belgium ; Belgium
LOUIS, Thomas ; Centre Hospitalier Universitaire de Liège - CHU > > Service médical de médecine nucléaire et imagerie onco ; Belgium ; Belgium
Cousin, François ; Centre Hospitalier Universitaire de Liège - CHU > > Service médical de radiodiagnostic ; Belgium
Bourbonne, Vincent; University Hospital, Brest, France > Radiation Oncology Department
Visvikis, Dimitris; LaTIM, INSERM, UMR 1101, University of Brest, Brest, France
MIEVIS, Carole ; Centre Hospitalier Universitaire de Liège - CHU > > Service médical de radiothérapie ; Belgium
Jansen, Nicolas ; Centre Hospitalier Universitaire de Liège - CHU > > Service médical de radiothérapie ; Belgium
Duysinx, Bernard ; Centre Hospitalier Universitaire de Liège - CHU > > Service de pneumologie - allergologie ; Belgium
Le Pennec, Romain; Nuclear Medicine Department, University Hospital of Brest, Brest, France
Nebbache, Malik; Radiation Oncology Department, University Hospital, Brest, France
Rehn, Martin; Radiation Oncology Department, University Hospital, Brest, France
Hamya, Mohamed; Radiation Oncology Department, University Hospital, Brest, France
Geier, Margaux; Radiation Oncology Department, University Hospital, Brest, France
Salaun, Pierre-Yves; Service de Médecine Nucléaire, CHRU de Brest, Brest, France
Schick, Ulrike; Department of Radiotherapy, University Hospital of Brest, Brest, France
Hatt, Mathieu; LaTIM, INSERM, UMR 1101, Univ Brest, Brest, France
Coucke, Philippe ; Université de Liège - ULiège > Département des sciences cliniques > Radiothérapie ; Belgium
Hustinx, Roland ; Centre Hospitalier Universitaire de Liège - CHU > > Service médical de médecine nucléaire et imagerie onco ; Belgium ; Belgium
Lovinfosse, Pierre ; Centre Hospitalier Universitaire de Liège - CHU > > Service médical de médecine nucléaire et imagerie onco ; Belgium
Multicentric development and evaluation of [ 18 F]FDG PET/CT and CT radiomic models to predict regional and/or distant recurrence in early-stage non-small cell lung cancer treated by stereotactic body radiation therapy
Publication date :
2023
Journal title :
European Journal of Nuclear Medicine and Molecular Imaging
Nagata Y, Hiraoka M, Shibata T, Onishi H, Kokubo M, Karasawa K, et al. Prospective trial of stereotactic body radiation therapy for both operable and inoperable T1N0M0 non-small cell lung cancer: Japan Clinical Oncology Group study JCOG0403. Int J Radiat Oncol Biol Phys. 2015;93:989–96. DOI: 10.1016/j.ijrobp.2015.07.2278
Guckenberger M, Allgäuer M, Appold S, Dieckmann K, Ernst I, Ganswindt U, et al. Safety and efficacy of stereotactic body radiotherapy for stage 1 non-small-cell lung cancer in routine clinical practice: a patterns-of-care and outcome analysis. J Thorac Oncol. 2013;8:1050–8. DOI: 10.1097/JTO.0b013e318293dc45
Ricardi U, Frezza G, Filippi AR, Badellino S, Levis M, Navarria P, et al. Stereotactic ablative radiotherapy for stage I histologically proven non-small cell lung cancer: an Italian multicenter observational study. Lung Cancer. 2014;84:248–53. DOI: 10.1016/j.lungcan.2014.02.015
Timmerman R, Paulus R, Galvin J, Michalski J, Straube W, Bradley J, et al. Stereotactic body radiation therapy for inoperable early stage lung cancer. JAMA. 2010;303:1070–6. DOI: 10.1001/jama.2010.261
Eriguchi T, Takeda A, Nemoto T, Tsurugai Y, Sanuki N, Tateishi Y, et al. Relationship between dose prescription methods and local control rate in stereotactic body radiotherapy for early stage non-small-cell lung cancer: systematic review and meta-analysis. Cancers (Basel). 2022;14:3815. DOI: 10.3390/cancers14153815
Chang JY, Lin SH, Dong W, Liao Z, Gandhi SJ, Gay CM, et al. Stereotactic ablative radiotherapy with or without immunotherapy for early-stage or isolated lung parenchymal recurrent node-negative non-small-cell lung cancer: an open-label, randomised, phase 2 trial. Lancet. 2023;S0140–6736(23):01384–93.
Gao SJ, Jin L, Meadows HW, Shafman TD, Gross CP, Yu JB, et al. Prediction of distant metastases after stereotactic body radiation therapy for early stage NSCLC: development and external validation of a multi-institutional model. J Thorac Oncol. 2023;18:339–49. DOI: 10.1016/j.jtho.2022.11.007
Vaz SC, Adam JA, Delgado Bolton RC, Vera P, van Elmpt W, Herrmann K, et al. Joint EANM/SNMMI/ESTRO practice recommendations for the use of 2-[18F]FDG PET/CT external beam radiation treatment planning in lung cancer V1.0. Eur J Nucl Med Mol Imaging. 2022;49:1386–406. DOI: 10.1007/s00259-021-05624-5
Sharma A, Mohan A, Bhalla AS, Sharma MC, Vishnubhatla S, Das CJ, et al. Role of various metabolic parameters derived from baseline 18F-FDG PET/CT as prognostic markers in non-small cell lung cancer patients undergoing platinum-based chemotherapy. Clin Nucl Med. 2018;43:e8-17. DOI: 10.1097/RLU.0000000000001886
Kwon W, Howard BA, Herndon JE, Patz EF. FDG uptake on positron emission tomography correlates with survival and time to recurrence in patients with stage I non-small-cell lung cancer. J Thorac Oncol. 2015;10:897–902. DOI: 10.1097/JTO.0000000000000534
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;9:834–42. DOI: 10.1097/JTO.0000000000000185
Hoang JK, Hoagland LF, Coleman RE, Coan AD, Herndon JE, Patz EF. Prognostic value of fluorine-18 fluorodeoxyglucose positron emission tomography imaging in patients with advanced-stage non-small-cell lung carcinoma. J Clin Oncol. 2008;26:1459–64. DOI: 10.1200/JCO.2007.14.3628
Agarwal M, Brahmanday G, Bajaj SK, Ravikrishnan KP, Wong C-YO. Revisiting the prognostic value of preoperative (18)F-fluoro-2-deoxyglucose ((18)F-FDG) positron emission tomography (PET) in early-stage (I & II) non-small cell lung cancers (NSCLC). Eur J Nucl Med Mol Imaging. 2010;37:691–8. DOI: 10.1007/s00259-009-1291-x
Lovinfosse P, Janvary ZL, Coucke P, Jodogne S, Bernard C, Hatt M, et al. FDG PET/CT texture analysis for predicting the outcome of lung cancer treated by stereotactic body radiation therapy. Eur J Nucl Med Mol Imaging. 2016;43:1453–60. DOI: 10.1007/s00259-016-3314-8
Dissaux G, Visvikis D, Da-Ano R, Pradier O, Chajon E, Barillot I, et al. Pretreatment 18F-FDG PET/CT radiomics predict local recurrence in patients treated with stereotactic body radiotherapy for early-stage non-small cell lung cancer: a multicentric study. J Nucl Med. 2020;61:814–20. DOI: 10.2967/jnumed.119.228106
Wu J, Aguilera T, Shultz D, Gudur M, Rubin DL, Loo BW, et al. Early-stage non-small cell lung cancer: quantitative imaging characteristics of (18)F fluorodeoxyglucose PET/CT allow prediction of distant metastasis. Radiology. 2016;281:270–8. DOI: 10.1148/radiol.2016151829
Oikonomou A, Khalvati F, Tyrrell PN, Haider MA, Tarique U, Jimenez-Juan L, et al. Radiomics analysis at PET/CT contributes to prognosis of recurrence and survival in lung cancer treated with stereotactic body radiotherapy. Sci Rep. 2018;8:4003. DOI: 10.1038/s41598-018-22357-y
Pyka T, Bundschuh RA, Andratschke N, Mayer B, Specht HM, Papp L, et al. Textural features in pre-treatment [F18]-FDG-PET/CT are correlated with risk of local recurrence and disease-specific survival in early stage NSCLC patients receiving primary stereotactic radiation therapy. Radiat Oncol. 2015;10:100. DOI: 10.1186/s13014-015-0407-7
Opitz D, Maclin R. Popular ensemble methods: an empirical study. JAIR. 1999;11:169–98. DOI: 10.1613/jair.614
Yasaka K, Akai H, Abe O, Kiryu S. Deep learning with convolutional neural network for differentiation of liver masses at dynamic contrast-enhanced CT: a preliminary study. Radiology. 2018;286:887–96. DOI: 10.1148/radiol.2017170706
Bourbonne V, Lucia F, Jaouen V, Bert J, Rehn M, Pradier O, et al. Development and prospective validation of a spatial dose pattern based model predicting acute pulmonary toxicity in patients treated with volumetric arc-therapy for locally advanced lung cancer. Radiother Oncol. 2021;164:43–9. DOI: 10.1016/j.radonc.2021.09.008
Janvary ZL, Jansen N, Baart V, Devillers M, Dechambre D, Lenaerts E, et al. Clinical outcomes of 130 patients with primary and secondary lung tumors treated with Cyberknife robotic stereotactic body radiotherapy. Radiol Oncol. 2017;51:178–86. DOI: 10.1515/raon-2017-0015
Senthi S, Lagerwaard FJ, Haasbeek CJA, Slotman BJ, Senan S. Patterns of disease recurrence after stereotactic ablative radiotherapy for early stage non-small-cell lung cancer: a retrospective analysis. Lancet Oncol. 2012;13:802–9. DOI: 10.1016/S1470-2045(12)70242-5
Schemper M, Smith TL. A note on quantifying follow-up in studies of failure time. Control Clin Trials. 1996;17:343–6. DOI: 10.1016/0197-2456(96)00075-X
Belli ML, Mori M, Broggi S, Cattaneo GM, Bettinardi V, Dell’Oca I, et al. Quantifying the robustness of [18F]FDG-PET/CT radiomic features with respect to tumor delineation in head and neck and pancreatic cancer patients. Phys Med. 2018;49:105–11. DOI: 10.1016/j.ejmp.2018.05.013
Velazquez ER, Parmar C, Jermoumi M, Mak RH, van Baardwijk A, Fennessy FM, et al. Volumetric CT-based segmentation of NSCLC using 3D-Slicer. Sci Rep. 2013;3:3529. DOI: 10.1038/srep03529
Radiomic features — PyRadiomics v3.1.0rc2.post5+g6a761c4 documentation. https://pyradiomics.readthedocs.io/en/latest/features.html. Accessed 29 Jun 2023.
Zwanenburg A, Vallières M, Abdalah MA, Aerts HJWL, Andrearczyk V, Apte A, et al. The image biomarker standardization initiative: standardized quantitative radiomics for high-throughput image-based phenotyping. Radiology. 2020;295:328–38. DOI: 10.1148/radiol.2020191145
Fortin J-P, Cullen N, Sheline YI, Taylor WD, Aselcioglu I, Cook PA, et al. Harmonization of cortical thickness measurements across scanners and sites. Neuroimage. 2018;167:104–20. DOI: 10.1016/j.neuroimage.2017.11.024
Caetano SJ, Sonpavde G, Pond GR. C-statistic: a brief explanation of its construction, interpretation and limitations. Eur J Cancer. 2018;90:130–2. DOI: 10.1016/j.ejca.2017.10.027
Ernani V, Appiah AK, Marr A, Zhang C, Zhen W, Smith LM, et al. Adjuvant systemic therapy in patients with early-stage NSCLC treated with stereotactic body radiation therapy. J Thorac Oncol. 2019;14:475–81. DOI: 10.1016/j.jtho.2018.11.018
Zhou Z, Folkert M, Cannon N, Iyengar P, Westover K, Zhang Y, et al. Predicting distant failure in early stage NSCLC treated with SBRT using clinical parameters. Radiother Oncol. 2016;119:501–4. DOI: 10.1016/j.radonc.2016.04.029
Manafi-Farid R, Askari E, Shiri I, Pirich C, Asadi M, Khateri M, et al. [18F]FDG-PET/CT radiomics and artificial intelligence in lung cancer: technical aspects and potential clinical applications. Semin Nucl Med. 2022;52:759–80. DOI: 10.1053/j.semnuclmed.2022.04.004
Fornacon-Wood I, Faivre-Finn C, O’Connor JPB, Price GJ. Radiomics as a personalized medicine tool in lung cancer: Separating the hope from the hype. Lung Cancer. 2020;146:197–208. DOI: 10.1016/j.lungcan.2020.05.028
Hao H, Zhou Z, Wang J. Distant failure prediction for early stage NSCLC by analyzing PET with sparse representation. In: Medical Imaging 2017: Computer-Aided Diagnosis. SPIE; 2017. p. 1008–14.
Li H, Galperin-Aizenberg M, Pryma D, Simone CB, Fan Y. Unsupervised machine learning of radiomic features for predicting treatment response and overall survival of early stage non-small cell lung cancer patients treated with stereotactic body radiation therapy. Radiother Oncol. 2018;129:218–26. DOI: 10.1016/j.radonc.2018.06.025
Li S, Yang N, Li B, Zhou Z, Hao H, Folkert MR, et al. A pilot study using kernelled support tensor machine for distant failure prediction in lung SBRT. Med Image Anal. 2018;50:106–16. DOI: 10.1016/j.media.2018.09.004
Yu W, Tang C, Hobbs BP, Li X, Koay EJ, Wistuba II, et al. Development and validation of a predictive radiomics model for clinical outcomes in stage I non-small cell lung cancer. Int J Radiat Oncol Biol Phys. 2018;102:1090–7. DOI: 10.1016/j.ijrobp.2017.10.046
Sawayanagi S, Yamashita H, Nozawa Y, Takenaka R, Miki Y, Morishima K, et al. Establishment of a prediction model for overall survival after stereotactic body radiation therapy for primary non-small cell lung cancer using radiomics analysis. Cancers (Basel). 2022;14:3859. DOI: 10.3390/cancers14163859
Lucia F, Bourbonne V, Pleyers C, Dupré P-F, Miranda O, Visvikis D, et al. Multicentric development and evaluation of 18F-FDG PET/CT and MRI radiomics models to predict para-aortic lymph node involvement in locally advanced cervical cancer. Eur J Nucl Med Mol Imaging. 2023. 10.1007/s00259-023-06180-w. DOI: 10.1007/s00259-023-06180-w
Lee TH, Shin H, Ahn YC, Kang MK, Song C, Kim WC, et al. Regional lymph node recurrence after stereotactic body radiation therapy for lung cancer: patterns of recurrence, treatment approaches, and clinical outcomes (KROG 21–09). Radiother Oncol. 2023;183: 109572. DOI: 10.1016/j.radonc.2023.109572
Klement RJ, Sonke J-J, Allgäuer M, Andratschke N, Appold S, Belderbos J, et al. Correlating dose variables with local tumor control in stereotactic body radiation therapy for early-stage non-small cell lung cancer: a modeling study on 1500 individual treatments. Int J Radiat Oncol Biol Phys. 2020;107:579–86. DOI: 10.1016/j.ijrobp.2020.03.005
Hatt M, Cheze Le Rest C, Antonorsi N, Tixier F, Tankyevych O, Jaouen V, et al. Radiomics in PET/CT: current status and future AI-based evolutions. Semin Nucl Med. 2021;51:126–33. DOI: 10.1053/j.semnuclmed.2020.09.002
Hatt M, Tixier F, Pierce L, Kinahan PE, Le Rest CC, Visvikis D. Characterization of PET/CT images using texture analysis: the past, the present… any future? Eur J Nucl Med Mol Imaging. 2017;44:151–65. DOI: 10.1007/s00259-016-3427-0