Response assessment in non-small cell lung cancer immunotherapy: initial experiences in utilizing FDG PET/CT and the PD-1 blocker nivolumab

Zurück zum Zitat Molina JR, Yang P, Cassivi SD, Schild SE, Adjei AA. Non-small cell lung cancer: epidemiology, risk factors, treatment, and survivorship. Mayo Clin Proc. 2008;83:584–94.CrossRef Molina JR, Yang P, Cassivi SD, Schild SE, Adjei AA. Non-small cell lung cancer: epidemiology, risk factors, treatment, and survivorship. Mayo Clin Proc. 2008;83:584–94.CrossRef

Zurück zum Zitat Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. Ca Cancer J Clin. 2015;65:87–108.CrossRef Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. Ca Cancer J Clin. 2015;65:87–108.CrossRef

Zurück zum Zitat Borghaei H, Paz-Ares L, Horn L, Spigel DR, Steins M, Ready NE, Chow LQ, Vokes EE, Felip E, Holgado E, Barlesi F, Kohlhaufl M, Arrieta O, Burgio MA, Fayette J, Lena H, Poddubskaya E, Gerber DE, Gettinger SN, Rudin CM, Rizvi N, Crino L, Blumenschein GR Jr., Antonia SJ, Dorange C, Harbison CT, Graf Finckenstein F, Brahmer JR. Nivolumab versus Docetaxel in advanced Nonsquamous non-small-cell lung cancer. N Engl J Med. 2015;373:1627–39.CrossRef Borghaei H, Paz-Ares L, Horn L, Spigel DR, Steins M, Ready NE, Chow LQ, Vokes EE, Felip E, Holgado E, Barlesi F, Kohlhaufl M, Arrieta O, Burgio MA, Fayette J, Lena H, Poddubskaya E, Gerber DE, Gettinger SN, Rudin CM, Rizvi N, Crino L, Blumenschein GR Jr., Antonia SJ, Dorange C, Harbison CT, Graf Finckenstein F, Brahmer JR. Nivolumab versus Docetaxel in advanced Nonsquamous non-small-cell lung cancer. N Engl J Med. 2015;373:1627–39.CrossRef

Zurück zum Zitat Brahmer J, Reckamp KL, Baas P, Crino L, Eberhardt WE, Poddubskaya E, Antonia S, Pluzanski A, Vokes EE, Holgado E, Waterhouse D, Ready N, Gainor J, Frontera AO, Havel L, Steins M, Garassino MC, Aerts JG, Domine M, Paz-Ares L, Reck M, Baudelet C, Harbison CT, Lestini B, Spigel DR. Nivolumab versus Docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med. 2015;373:123–35.CrossRef Brahmer J, Reckamp KL, Baas P, Crino L, Eberhardt WE, Poddubskaya E, Antonia S, Pluzanski A, Vokes EE, Holgado E, Waterhouse D, Ready N, Gainor J, Frontera AO, Havel L, Steins M, Garassino MC, Aerts JG, Domine M, Paz-Ares L, Reck M, Baudelet C, Harbison CT, Lestini B, Spigel DR. Nivolumab versus Docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med. 2015;373:123–35.CrossRef

Zurück zum Zitat Reck M, Rodriguez-Abreu D, Robinson AG, Hui R, Csoszi T, Fulop A, Gottfried M, Peled N, Tafreshi A, Cuffe S, O’Brien M, Rao S, Hotta K, Leiby MA, Lubiniecki GM, Shentu Y, Rangwala R, Brahmer JR, Investigators K. Pembrolizumab versus chemotherapy for PD-L1-positive non-small-cell lung cancer. N Engl J Med. 2016;375:1823–33.CrossRef Reck M, Rodriguez-Abreu D, Robinson AG, Hui R, Csoszi T, Fulop A, Gottfried M, Peled N, Tafreshi A, Cuffe S, O’Brien M, Rao S, Hotta K, Leiby MA, Lubiniecki GM, Shentu Y, Rangwala R, Brahmer JR, Investigators K. Pembrolizumab versus chemotherapy for PD-L1-positive non-small-cell lung cancer. N Engl J Med. 2016;375:1823–33.CrossRef

Zurück zum Zitat Nishino M, Ramaiya NH, Chambers ES, Adeni AE, Hatabu H, Janne PA, Hodi FS, Awad MM. Immune-related response assessment during PD-1 inhibitor therapy in advanced non-small-cell lung cancer patients. J Immunother Cancer. 2016;4:84.CrossRef Nishino M, Ramaiya NH, Chambers ES, Adeni AE, Hatabu H, Janne PA, Hodi FS, Awad MM. Immune-related response assessment during PD-1 inhibitor therapy in advanced non-small-cell lung cancer patients. J Immunother Cancer. 2016;4:84.CrossRef

Zurück zum Zitat Wolchok JD, Hoos A, O’Day S, Weber JS, Hamid O, Lebbe C, Maio M, Binder M, Bohnsack O, Nichol G, Humphrey R, Hodi FS. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin Cancer Res. 2009;15:7412–20.CrossRef Wolchok JD, Hoos A, O’Day S, Weber JS, Hamid O, Lebbe C, Maio M, Binder M, Bohnsack O, Nichol G, Humphrey R, Hodi FS. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin Cancer Res. 2009;15:7412–20.CrossRef

Zurück zum Zitat Goeckenjan G, Sitter H, Thomas M, Branscheid D, Flentje M, Griesinger F, Niederle N, Stuschke M, Blum T, Deppermann KM, Ficker JH, Freitag L, Lubbe AS, Reinhold T, Spath-Schwalbe E, Ukena D, Wickert M, Wolf M, Andreas S, Auberger T, Baum RP, Baysal B, Beuth J, Bickeboller H, Bocking A, Bohle RM, Bruske I, Burghuber O, Dickgreber N, Diederich S, Dienemann H, Eberhardt W, Eggeling S, Fink T, Fischer B, Franke M, Friedel G, Gauler T, Gutz S, Hautmann H, Hellmann A, Hellwig D, Herth F, Heussel CP, Hilbe W, Hoffmeyer F, Horneber M, Huber RM, Hubner J, Kauczor HU, Kirchbacher K, Kirsten D, Kraus T, Lang SM, Martens U, Mohn-Staudner A, Muller KM, Muller-Nordhorn J, Nowak D, Ochmann U, Passlick B, Petersen I, Pirker R, Pokrajac B, Reck M, Riha S, Rube C, Schmittel A, Schonfeld N, Schutte W, Serke M, Stamatis G, Steingraber M, Steins M, Stoelben E, Swoboda L, Teschler H, Tessen HW, Weber M, Werner A, Wichmann HE, Irlinger Wimmer E, Witt C, Worth H, Deutsche Gesellschaft fur Pneumologie und Beatmungsmedizin und die Deutsche K. Prevention, diagnosis, therapy, and follow-up of lung cancer. Pneumologie. 2010;64(Suppl 2):e1–e164.CrossRef Goeckenjan G, Sitter H, Thomas M, Branscheid D, Flentje M, Griesinger F, Niederle N, Stuschke M, Blum T, Deppermann KM, Ficker JH, Freitag L, Lubbe AS, Reinhold T, Spath-Schwalbe E, Ukena D, Wickert M, Wolf M, Andreas S, Auberger T, Baum RP, Baysal B, Beuth J, Bickeboller H, Bocking A, Bohle RM, Bruske I, Burghuber O, Dickgreber N, Diederich S, Dienemann H, Eberhardt W, Eggeling S, Fink T, Fischer B, Franke M, Friedel G, Gauler T, Gutz S, Hautmann H, Hellmann A, Hellwig D, Herth F, Heussel CP, Hilbe W, Hoffmeyer F, Horneber M, Huber RM, Hubner J, Kauczor HU, Kirchbacher K, Kirsten D, Kraus T, Lang SM, Martens U, Mohn-Staudner A, Muller KM, Muller-Nordhorn J, Nowak D, Ochmann U, Passlick B, Petersen I, Pirker R, Pokrajac B, Reck M, Riha S, Rube C, Schmittel A, Schonfeld N, Schutte W, Serke M, Stamatis G, Steingraber M, Steins M, Stoelben E, Swoboda L, Teschler H, Tessen HW, Weber M, Werner A, Wichmann HE, Irlinger Wimmer E, Witt C, Worth H, Deutsche Gesellschaft fur Pneumologie und Beatmungsmedizin und die Deutsche K. Prevention, diagnosis, therapy, and follow-up of lung cancer. Pneumologie. 2010;64(Suppl 2):e1–e164.CrossRef

Zurück zum Zitat Novello S, Barlesi F, Califano R, Cufer T, Ekman S, Levra MG, Kerr K, Popat S, Reck M, Senan S, Simo GV, Vansteenkiste J, Peters S, Committee EG. Metastatic non-small-cell lung cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2016;27:v1–v27.CrossRef Novello S, Barlesi F, Califano R, Cufer T, Ekman S, Levra MG, Kerr K, Popat S, Reck M, Senan S, Simo GV, Vansteenkiste J, Peters S, Committee EG. Metastatic non-small-cell lung cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2016;27:v1–v27.CrossRef

Zurück zum Zitat Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, Dancey J, Arbuck S, Gwyther S, Mooney M, Rubinstein L, Shankar L, Dodd L, Kaplan R, Lacombe D, Verweij J. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer. 2009;45:228–47.CrossRef Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, Dancey J, Arbuck S, Gwyther S, Mooney M, Rubinstein L, Shankar L, Dodd L, Kaplan R, Lacombe D, Verweij J. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer. 2009;45:228–47.CrossRef

Zurück zum Zitat 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):122–50.CrossRef 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):122–50.CrossRef

Zurück zum Zitat Kaira K, Higuchi T, Naruse I, Arisaka Y, Tokue A, Altan B, Suda S, Mogi A, Shimizu K, Sunaga N, Hisada T, Kitano S, Obinata H, Yokobori T, Mori K, Nishiyama M, Tsushima Y, Asao T. 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;45:56–66.CrossRef Kaira K, Higuchi T, Naruse I, Arisaka Y, Tokue A, Altan B, Suda S, Mogi A, Shimizu K, Sunaga N, Hisada T, Kitano S, Obinata H, Yokobori T, Mori K, Nishiyama M, Tsushima Y, Asao T. 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;45:56–66.CrossRef

Zurück zum Zitat Zhang M, Wang D, Sun Q, Pu H, Wang Y, Zhao S, Wang Y, Zhang Q. Prognostic significance of PD-L1 expression and (18)F-FDG PET/CT in surgical pulmonary squamous cell carcinoma. Oncotarget. 2017;8:51630–40.PubMedPubMedCentral Zhang M, Wang D, Sun Q, Pu H, Wang Y, Zhao S, Wang Y, Zhang Q. Prognostic significance of PD-L1 expression and (18)F-FDG PET/CT in surgical pulmonary squamous cell carcinoma. Oncotarget. 2017;8:51630–40.PubMedPubMedCentral

Zurück zum Zitat Tirkes T, Hollar MA, Tann M, Kohli MD, Akisik F, Sandrasegaran K. Response criteria in oncologic imaging: review of traditional and new criteria. Radiographics. 2013;33:1323–41.CrossRef Tirkes T, Hollar MA, Tann M, Kohli MD, Akisik F, Sandrasegaran K. Response criteria in oncologic imaging: review of traditional and new criteria. Radiographics. 2013;33:1323–41.CrossRef

Zurück zum Zitat O JH, Lodge MA, Wahl RL. Practical PERCIST: a simplified guide to PET response criteria in solid tumors 1.0. Radiology. 2016;280:576–84.CrossRef O JH, Lodge MA, Wahl RL. Practical PERCIST: a simplified guide to PET response criteria in solid tumors 1.0. Radiology. 2016;280:576–84.CrossRef

Zurück zum Zitat Ratain MJ, Eckhardt SG. Phase II studies of modern drugs directed against new targets: if you are fazed, too, then resist RECIST. J Clin Oncol. 2004;22:4442–5.CrossRef Ratain MJ, Eckhardt SG. Phase II studies of modern drugs directed against new targets: if you are fazed, too, then resist RECIST. J Clin Oncol. 2004;22:4442–5.CrossRef

Zurück zum Zitat Rosner GL, Stadler W, Ratain MJ. Randomized discontinuation design: application to cytostatic antineoplastic agents. J Clin Oncol. 2002;20:4478–84.CrossRef Rosner GL, Stadler W, Ratain MJ. Randomized discontinuation design: application to cytostatic antineoplastic agents. J Clin Oncol. 2002;20:4478–84.CrossRef

Zurück zum Zitat Hodi FS, Hwu WJ, Kefford R, Weber JS, Daud A, Hamid O, Patnaik A, Ribas A, Robert C, Gangadhar TC, Joshua AM, Hersey P, Dronca R, Joseph R, Hille D, Xue D, Li XN, Kang SP, Ebbinghaus S, Perrone A, Wolchok JD. Evaluation of immune-related response criteria and RECIST v1.1 in patients with advanced melanoma treated with Pembrolizumab. J Clin Oncol. 2016;34:1510–7.CrossRef Hodi FS, Hwu WJ, Kefford R, Weber JS, Daud A, Hamid O, Patnaik A, Ribas A, Robert C, Gangadhar TC, Joshua AM, Hersey P, Dronca R, Joseph R, Hille D, Xue D, Li XN, Kang SP, Ebbinghaus S, Perrone A, Wolchok JD. Evaluation of immune-related response criteria and RECIST v1.1 in patients with advanced melanoma treated with Pembrolizumab. J Clin Oncol. 2016;34:1510–7.CrossRef

Zurück zum Zitat Kim HK, Heo MH, Lee HS, Sun JM, Lee SH, Ahn JS, Park K, Ahn MJ. Comparison of RECIST to immune-related response criteria in patients with non-small cell lung cancer treated with immune-checkpoint inhibitors. Cancer Chemother Pharmacol. 2017;80:591–8.CrossRef Kim HK, Heo MH, Lee HS, Sun JM, Lee SH, Ahn JS, Park K, Ahn MJ. Comparison of RECIST to immune-related response criteria in patients with non-small cell lung cancer treated with immune-checkpoint inhibitors. Cancer Chemother Pharmacol. 2017;80:591–8.CrossRef

Zurück zum Zitat Di Giacomo AM, Danielli R, Guidoboni M, Calabro L, Carlucci D, Miracco C, Volterrani L, Mazzei MA, Biagioli M, Altomonte M, Maio M. Therapeutic efficacy of ipilimumab, an anti-CTLA-4 monoclonal antibody, in patients with metastatic melanoma unresponsive to prior systemic treatments: clinical and immunological evidence from three patient cases. Cancer Immunol Immunother. 2009;58:1297–306.CrossRef Di Giacomo AM, Danielli R, Guidoboni M, Calabro L, Carlucci D, Miracco C, Volterrani L, Mazzei MA, Biagioli M, Altomonte M, Maio M. Therapeutic efficacy of ipilimumab, an anti-CTLA-4 monoclonal antibody, in patients with metastatic melanoma unresponsive to prior systemic treatments: clinical and immunological evidence from three patient cases. Cancer Immunol Immunother. 2009;58:1297–306.CrossRef

Zurück zum Zitat Nishino M. Immune-related response evaluations during immune-checkpoint inhibitor therapy: establishing a “common language” for the new arena of cancer treatment. J Immunother Cancer. 2016;4:30.CrossRef Nishino M. Immune-related response evaluations during immune-checkpoint inhibitor therapy: establishing a “common language” for the new arena of cancer treatment. J Immunother Cancer. 2016;4:30.CrossRef