Abstract
Objective
The prognostic value of treatment response in patients with non-small cell lung cancer (NSCLC) treated with immune-checkpoint inhibitors (ICIs) shown by 18F-fludeoxyglucose (FDG) positron emission tomography/computed tomography (PET/CT) results obtained with multiple types of PET scanners using standardized uptake value (SUV) harmonization was evaluated.
Methods
Fifty-eight patients treated with ICIs who underwent 18F-FDG PET/CT examinations with nine types of PET scanners at six hospitals were enrolled. SUV harmonization of multiple PET scanner results was performed using the dedicated software packages “RAVAT” and “RC Tool for Harmonization”. Tumor response was assessed by change in sum of harmonized SUVmax, according to the European Organization for Research and Treatment of Cancer (EORTC5) or the SUV of up to five lesions normalized to lean body mass, according to the PET Response Criteria in Solid Tumors (PERCIST5) and immunotherapy-modified PERCIST (imPERCIST5) criteria. The correlation between tumor response according to those three definitions and overall survival (OS) was evaluated and compared to known prognostic factors.
Results
One-year OS in responders and non-responders for harmonized EROTC5 was 86 and 32%, for harmonized PERCIST5 was 86 and 32%, and for harmonized imPERCIST5 was 80 and 30%, respectively (each p = 0.001). Univariate analysis showed that all response criteria remained as prognostic factors. However, there was an overlap for the categories stable metabolic disease (SMD) and progression metabolic disease (PMD) in survival curves using the PET treatment response criteria.
Conclusion
In patients with NSCLC treated with ICIs, tumor response based on the harmonized response criteria was associated with OS. PET response criteria using harmonized metabolic parameters may be difficult to routinely employ in daily practice due to overlapping SMD and PMD, although may have a supporting role for determining prognosis.
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References
Garon EB, Rizvi NA, Hui R, Leighl N, Balmanoukian AS, Eder JP, et al. Pembrolizumab for the treatment of non-small-cell lung cancer. N Engl J Med. 2015;372(21):2018–28.
Borghaei H, Paz-Ares L, Horn L, Spigel DR, Steins M, Ready NE, et al. Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer. N Engl J Med. 2015;373(17):1627–39.
Reck M, Rodriguez-Abreu D, Robinson AG, Hui R, Csoszi T, Fulop A, et al. Pembrolizumab versus chemotherapy for PD-L1-positive non-small-cell lung cancer. N Engl J Med. 2016;375(19):1823–33.
Langer CJ, Gadgeel SM, Borghaei H, Papadimitrakopoulou VA, Patnaik A, Powell SF, et al. Carboplatin and pemetrexed with or without pembrolizumab for advanced, non-squamous non-small-cell lung cancer: a randomised, phase 2 cohort of the open-label KEYNOTE-021 study. Lancet Oncol. 2016;17(11):1497–508.
Socinski MA, Jotte RM, Cappuzzo F, Orlandi F, Stroyakovskiy D, Nogami N, et al. Atezolizumab for first-line treatment of metastatic nonsquamous NSCLC. N Engl J Med. 2018;378(24):2288–301.
Chiou VL, Burotto M. Pseudoprogression and immune-related response in solid tumors. J Clin Oncol. 2015;33(31):3541–3.
Nishino M, Dahlberg SE, Adeni AE, Lydon CA, Hatabu H, Janne PA, et al. Tumor response dynamics of advanced non-small cell lung cancer patients treated with PD-1 inhibitors: imaging markers for treatment outcome. Clin Cancer Res. 2017;23(19):5737–44.
Kaira K, Higuchi T, Naruse I, Arisaka Y, Tokue A, Altan B, et al. Metabolic activity by (18)F-FDG-PET/CT is predictive of early response after nivolumab in previously treated NSCLC. Eur J Nucl Med Mol Imaging. 2018;45(1):56–66.
Cho SY, Lipson EJ, Im HJ, Rowe SP, Gonzalez EM, Blackford A, et al. Prediction of response to immune checkpoint inhibitor therapy using early-time-point (18)F-FDG PET/CT imaging in patients with advanced melanoma. J Nucl Med. 2017;58(9):1421–8.
Rossi G, Bauckneht M, Genova C, Rijavec E, Biello F, Mennella S, et al. Comparison between (18)F-FDG PET-based and CT-based criteria in non-small cell lung cancer patients treated with nivolumab. J Nucl Med. 2020;61(7):990–8.
Young H, Baum R, Cremerius U, Herholz K, Hoekstra O, Lammertsma AA, et al. Measurement of clinical and subclinical tumour response using [18F]-fluorodeoxyglucose and positron emission tomography: review and 1999 EORTC recommendations. European Organization for Research and Treatment of Cancer (EORTC) PET Study Group. Eur J Cancer (Oxford, England: 1990). 1999;35(13):1773–82.
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.
Ito K, Teng R, Schöder H, Humm JL, Ni A, Michaud L, et al. (18)F-FDG PET/CT for monitoring of ipilimumab therapy in patients with metastatic melanoma. J Nucl Med. 2019;60(3):335–41.
Boellaard R, Delgado-Bolton R, Oyen WJG, 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 Imag. 2015;42(2):328–54.
Tsutsui Y, Daisaki H, Akamatsu G, Umeda T, Ogawa M, Kajiwara H, et al. Multicentre analysis of PET SUV using vendor-neutral software: the Japanese Harmonization Technology (J-Hart) study. EJNMMI Res. 2018;8(1):83.
Daisaki H, Kitajima K, Nakajo M, Watabe T, Ito K, Sakamoto F, et al. Usefulness of semi-automatic harmonization strategy of standardized uptake values for multicenter PET studies. Sci Rep. 2021;11(1):8517.
Anderson JR, Cain KC, Gelber RD. Analysis of survival by tumor response. J Clin Oncol. 1983;1(11):710–9.
Michot JM, Bigenwald C, Champiat S, Collins M, Carbonnel F, Postel-Vinay S, et al. Immune-related adverse events with immune checkpoint blockade: a comprehensive review. European journal of cancer (Oxford, England: 1990). 2016;54:139–48.
Kong BY, Menzies AM, Saunders CA, Liniker E, Ramanujam S, Guminski A, et al. Residual FDG-PET metabolic activity in metastatic melanoma patients with prolonged response to anti-PD-1 therapy. Pigment Cell Melanoma Res. 2016;29(5):572–7.
Acknowledgements
The authors wish to express gratefulness to Dr. Hidehito Horinouchi, Dr. Haruhisa Saito and Prof. Kozo Kuribayashi for their kind support of our work.
Funding
This work was supported by a working group grant from the Japanese Society of Nuclear Medicine (No. 2019-1).
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Ito, K., Kitajima, K., Toriihara, A. et al. 18F-FDG PET/CT for monitoring anti-PD-1 therapy in patients with non-small cell lung cancer using SUV harmonization of results obtained with various types of PET/CT scanners used at different centers. Ann Nucl Med 35, 1253–1263 (2021). https://doi.org/10.1007/s12149-021-01667-8
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DOI: https://doi.org/10.1007/s12149-021-01667-8