Top

Clinical and Translational Oncology

Published in:

01-11-2019 | NSCLC | Research Article

Consensus on the use of immune-related response criteria to evaluate the efficacy of immunotherapy in non-small cell lung cancer

Authors: M. Provencio, E. Carcereny, Á. Artal

Published in: Clinical and Translational Oncology | Issue 11/2019

Abstract

Introduction

Many methods used to assess the effectiveness of immune checkpoint (programmed death-ligand 1 or cytotoxic T-lymphocyte-associated protein 4) inhibitors for non-small cell lung cancer (NSCLC) are insufficient, as the therapeutic benefit of these agents is often underestimated. Consequently, immune-related evaluation criteria have been developed to better reflect their efficacy. The aim of this consensus was to obtain the opinion of lung cancer experts on the adequacy of immune-response criteria for evaluating the efficacy of these treatments.

Methods

Through two rounds of a modified Delphi consensus, 18 Spanish lung cancer experts participated in a 15-item questionnaire regarding the use of immunotherapies for NSCLC and the assessment criteria used to evaluate their effectiveness.

Results

Consensus was achieved on 80% of the items in the questionnaire. The panelists agreed that although the Response Evaluation Criteria in Solid Tumors (RECIST) are standard for the evaluation of solid tumors, immune-related response criteria would be useful for measuring the efficacy of immunotherapy. In addition, they considered that an overall survival (OS) rate at 2–5 years is the most useful end point for assessing the benefit of immunotherapy, as clinical benefit may extend beyond the RECIST criteria-defined progression of disease.

Conclusions

Although immune-related response criteria have been developed to better evaluate the efficacy of immunotherapy, their use has not been validated and is restricted to investigational applications. However, they may prove to be a useful tool for measuring the efficacy of immunotherapy agents in NSCLC, especially the OS rate at 2–5 years.

Available only for authorised users

Schiller JH, Harrington D, Belani CP, Langer C, Sandler A, Krook J, et al. Comparison of four chemotherapy regimens for advanced non-small-cell lung cancer. N Engl J Med. 2002;346(2):92–8. https://doi.org/10.1056/NEJMoa011954.CrossRefPubMed

Haslam S, Chrisp P. Bevacizumab: the evidence for its clinical potential in the treatment of nonsmall cell lung cancer. Core Evid. 2007;2(1):31–49.PubMedPubMedCentral

Reck M, von Pawel J, Zatloukal P, Ramlau R, Gorbounova V, Hirsh V, et al. Phase III trial of cisplatin plus gemcitabine with either placebo or bevacizumab as first-line therapy for nonsquamous non-small-cell lung cancer: AVAil. J Clin Oncol. 2009;27(8):1227–34. https://doi.org/10.1200/JCO.2007.14.5466.CrossRefPubMed

Sandler A, Gray R, Perry MC, Brahmer J, Schiller JH, Dowlati A, et al. Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer. N Engl J Med. 2006;355(24):2542–50. https://doi.org/10.1056/NEJMoa061884.CrossRefPubMed

Socinski MA, Saleh MN, Trent DF, Dobbs TW, Zehngebot LM, Levine MA, et al. A randomized, phase II trial of two dose schedules of carboplatin/paclitaxel/cetuximab in stage IIIB/IV non-small-cell lung cancer (NSCLC). Ann Oncol. 2009;20(6):1068–73. https://doi.org/10.1093/annonc/mdn745.CrossRefPubMed

Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin. 2016;66(1):7–30. https://doi.org/10.3322/caac.21332.CrossRefPubMed

Lynch TJ, Bondarenko I, Luft A, Serwatowski P, Barlesi F, Chacko R, et al. Ipilimumab in combination with paclitaxel and carboplatin as first-line treatment in stage IIIB/IV non-small-cell lung cancer: results from a randomized, double-blind, multicenter phase II study. J Clin Oncol. 2012;30(17):2046–54. https://doi.org/10.1200/JCO.2011.38.4032.CrossRefPubMed

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. https://doi.org/10.1056/NEJMoa1507643.CrossRefPubMedPubMedCentral

Brahmer J, Reckamp KL, Baas P, Crino L, Eberhardt WE, Poddubskaya E, et al. Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med. 2015;373(2):123–35. https://doi.org/10.1056/NEJMoa1504627.CrossRefPubMedPubMedCentral

10.

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. https://doi.org/10.1056/NEJMoa1501824.CrossRefPubMed

11.

Herbst RS, Baas P, Pérez-Gracia JL, Felip E, Kim DW, Han JY, et al. PD1.06 (also presented as P2.41): pembrolizumab versus docetaxel for previously treated NSCLC (KEYNOTE-010): archival versus new tumor samples for PD-L1 assessment. J Thorac Oncol. 2016;11(10S):S174–5. https://doi.org/10.1016/j.jtho.2016.08.014.CrossRef

12.

Rittmeyer A, Barlesi F, Waterkamp D, Park K, Ciardiello F, von Pawel J, et al. Atezolizumab versus docetaxel in patients with previously treated non-small-cell lung cancer (OAK): a phase 3, open-label, multicentre randomised controlled trial. Lancet. 2017;389(10066):255–65. https://doi.org/10.1016/S0140-6736(16)32517-X.CrossRefPubMed

13.

Fehrenbacher L, Spira A, Ballinger M, Kowanetz M, Vansteenkiste J, Mazieres J, et al. Atezolizumab versus docetaxel for patients with previously treated non-small-cell lung cancer (POPLAR): a multicentre, open-label, phase 2 randomised controlled trial. Lancet. 2016;387(10030):1837–46. https://doi.org/10.1016/S0140-6736(16)00587-0.CrossRefPubMed

14.

Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–74. https://doi.org/10.1016/j.cell.2011.02.013.CrossRefPubMed

15.

Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12(4):252–64. https://doi.org/10.1038/nrc3239.CrossRefPubMedPubMedCentral

16.

Wolchok JD, Hoos A, O’Day S, Weber JS, Hamid O, Lebbe C, et al. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin Cancer Res. 2009;15(23):7412–20. https://doi.org/10.1158/1078-0432.CCR-09-1624.CrossRefPubMed

17.

Nishino M, Jagannathan JP, Krajewski KM, O’Regan K, Hatabu H, Shapiro G, et al. Personalized tumor response assessment in the era of molecular medicine: cancer-specific and therapy-specific response criteria to complement pitfalls of RECIST. AJR Am J Roentgenol. 2012;198(4):737–45. https://doi.org/10.2214/AJR.11.7483.CrossRefPubMedPubMedCentral

18.

Nishino M, Giobbie-Hurder A, Gargano M, Suda M, Ramaiya NH, Hodi FS. Developing a common language for tumor response to immunotherapy: immune-related response criteria using unidimensional measurements. Clin Cancer Res. 2013;19(14):3936–43. https://doi.org/10.1158/1078-0432.CCR-13-0895.CrossRefPubMedPubMedCentral

19.

Hoos A, Britten C. The immuno-oncology framework: enabling a new era of cancer therapy. Oncoimmunology. 2012;1(3):334–9. https://doi.org/10.4161/onci.19268.CrossRefPubMedPubMedCentral

20.

Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer. 2009;45(2):228–47. https://doi.org/10.1016/j.ejca.2008.10.026.CrossRefPubMed

21.

Choi H, Charnsangavej C, Faria SC, Macapinlac HA, Burgess MA, Patel SR, et al. Correlation of computed tomography and positron emission tomography in patients with metastatic gastrointestinal stromal tumor treated at a single institution with imatinib mesylate: proposal of new computed tomography response criteria. J Clin Oncol. 2007;25(13):1753–9. https://doi.org/10.1200/JCO.2006.07.3049.CrossRefPubMed

22.

Lee HY, Lee KS, Hwang HS, Lee JW, Ahn MJ, Park K, et al. Molecularly targeted therapy using bevacizumab for non-small cell lung cancer: a pilot study for the new CT response criteria. Korean J Radiol. 2010;11(6):618–26. https://doi.org/10.3348/kjr.2010.11.6.618.CrossRefPubMedPubMedCentral

23.

Crabb SJ, Patsios D, Sauerbrei E, Ellis PM, Arnold A, Goss G, et al. Tumor cavitation: impact on objective response evaluation in trials of angiogenesis inhibitors in non-small-cell lung cancer. J Clin Oncol. 2009;27(3):404–10. https://doi.org/10.1200/JCO.2008.16.2545.CrossRefPubMed

24.

Hodi FS, Hwu WJ, Kefford R, Weber JS, Daud A, Hamid O, et al. Evaluation of immune-related response criteria and RECIST v1.1 in patients with advanced melanoma treated with pembrolizumab. J Clin Oncol. 2016;34(13):1510–7. https://doi.org/10.1200/jco.2015.64.0391.CrossRefPubMedPubMedCentral

25.

Jones J, Hunter D. Consensus methods for medical and health services research. BMJ. 1995;311(7001):376–80.CrossRefPubMedPubMedCentral

26.

Fitch K, Bernstein SJ, Aguilar MD, Burnand B, LaCalle JR, Lázaro P, et al. The RAND/UCLA appropriateness method user’s manual. http://www.rand.org/pubs/monograph_reports/MR1269.html. Accessed 5 July 2017.

27.

Dolgin E. Cancer immunology community seeks better end points. Nat Rev Drug Discov. 2016;15(12):807–9. https://doi.org/10.1038/nrd.2016.254.CrossRefPubMed

28.

Hoos A, Eggermont AM, Janetzki S, Hodi FS, Ibrahim R, Anderson A, et al. Improved endpoints for cancer immunotherapy trials. J Natl Cancer Inst. 2010;102(18):1388–97. https://doi.org/10.1093/jnci/djq310.CrossRefPubMedPubMedCentral

29.

Ribas A, Kefford R, Marshall MA, Punt CJ, Haanen JB, Marmol M, et al. Phase III randomized clinical trial comparing tremelimumab with standard-of-care chemotherapy in patients with advanced melanoma. J Clin Oncol. 2013;31(5):616–22. https://doi.org/10.1200/JCO.2012.44.6112.CrossRefPubMedPubMedCentral

30.

Nishino M, Ramaiya NH, Chambers ES, Adeni AE, Hatabu H, Janne PA, et al. Immune-related response assessment during PD-1 inhibitor therapy in advanced non-small-cell lung cancer patients. J Immunother Cancer. 2016;4:84. https://doi.org/10.1186/s40425-016-0193-2.CrossRefPubMedPubMedCentral

31.

Reck M, Bondarenko I, Luft A, Serwatowski P, Barlesi F, Chacko R, et al. Ipilimumab in combination with paclitaxel and carboplatin as first-line therapy in extensive-disease-small-cell lung cancer: results from a randomized, double-blind, multicenter phase 2 trial. Ann Oncol. 2013;24(1):75–83. https://doi.org/10.1093/annonc/mds213.CrossRefPubMed

32.

Spiegel ML, editor. A phase I study of exemestane with carboplatin and pemetrexed in postmenopausal women with metastatic, non-squamous non-small cell lung cancer (Poster P.3.01). In:16th World conference on lung cancer; 2015 September 6–9; Denver, Colorado.

33.

Mazieres J, Fehrenbacher L, Rittmeyer A, Spira AI, Park K, Smith DA, Artal-Cortes A, Lewanski CR, Braiteh FS, Yi J, He P, Kowanetz M, Waterkamp D, Ballinger M, Chen DS, Sandler A, Vansteenkiste JF. Non-classical response measured by immune-modified RECIST and post-progression treatment effects of atezolizumab in 2L/3L NSCLC: results from the randomized phase II study POPLAR. J Clin Oncol. 2016;34(15_suppl):9032.CrossRef

34.

Taylor M, Dutcus CE, Schmidt E, Bagulho T, Li D, Shumaker R, et al. A phase 1b trial of lenvatinib (LEN) plus pembrolizumab (PEM) in patients with selected solid tumors. Ann Oncol. 2016;27(6):266–95.

35.

Kim HK, Heo MH, Lee HS, Sun JM, Lee SH, Ahn JS, et al. 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(3):591–8. https://doi.org/10.1007/s00280-017-3396-4.CrossRefPubMed

36.

Tazdait M, Mezquita L, Lahmar J, Ferrara R, Bidault F, Ammari S, et al. Patterns of responses in metastatic NSCLC during PD-1 or PDL-1 inhibitor therapy: comparison of RECIST 1.1, irRECIST and iRECIST criteria. Eur J Cancer. 2018;88:38–47. https://doi.org/10.1016/j.ejca.2017.10.017.CrossRefPubMed

37.

Petrelli F, Coinu A, Cabiddu M, Borgonovo K, Ghilardi M, Lonati V, et al. Early analysis of surrogate endpoints for metastatic melanoma in immune checkpoint inhibitor trials. Medicine (Baltimore). 2016;95(26):e3997. https://doi.org/10.1097/MD.0000000000003997.CrossRef

38.

Robert C, Long GV, Brady B, Dutriaux C, Maio M, Mortier L, et al. Nivolumab in previously untreated melanoma without BRAF mutation. N Engl J Med. 2015;372(4):320–30. https://doi.org/10.1056/NEJMoa1412082.CrossRefPubMed

39.

Postow MA, Chesney J, Pavlick AC, Robert C, Grossmann K, McDermott D, et al. Nivolumab and ipilimumab versus ipilimumab in untreated melanoma. N Engl J Med. 2015;372(21):2006–17. https://doi.org/10.1056/NEJMoa1414428.CrossRefPubMedPubMedCentral

Title: Consensus on the use of immune-related response criteria to evaluate the efficacy of immunotherapy in non-small cell lung cancer
Authors: M. Provencio
E. Carcereny
Á. Artal
Publication date: 01-11-2019
Publisher: Springer International Publishing
Keywords: NSCLC
Solid Tumor
NSCLC
Published in: Clinical and Translational Oncology / Issue 11/2019
Print ISSN: 1699-048X
Electronic ISSN: 1699-3055
DOI: https://doi.org/10.1007/s12094-019-02072-4

Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Watch now

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras

Prof. Fabrice Barlesi

Developed by: Springer Medicine

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Introduction

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 11/2019

Expression of Concern: BRG1 regulation by miR-155 in human leukemia and lymphoma cell lines

Implication of lymph node staging in migration and different treatment strategies for stage T2N0M0 and T1N1M0 resected gastric cancer: a SEER population analysis

Relation between sarcopenia and dose-limiting toxicity in patients with metastatic colorectal cancer who received regorafenib

Effectiveness of fentanyl pectin nasal citrate in controlling episodes of breakthrough cancer pain triggered by routine radiotherapy procedures

Comparison of efficacy of HCAG and FLAG re-induction chemotherapy in acute myeloid leukemia patients of low- and intermediate-risk groups

Predictive factors for central lymph node and lateral cervical lymph node metastases in papillary thyroid carcinoma

Keynote webinar | Spotlight on antibody–drug conjugates in cancer