The benefit of treatment beyond progression with immune checkpoint inhibitors: a multi-center retrospective cohort study.
Beyond progression
Immune checkpoint inhibitor
Immunotherapy
Progressive disease
Journal
Journal of cancer research and clinical oncology
ISSN: 1432-1335
Titre abrégé: J Cancer Res Clin Oncol
Pays: Germany
ID NLM: 7902060
Informations de publication
Date de publication:
Jul 2023
Jul 2023
Historique:
received:
17
07
2022
accepted:
04
08
2022
medline:
5
7
2023
pubmed:
13
8
2022
entrez:
12
8
2022
Statut:
ppublish
Résumé
Treatment beyond progression (TBP) with immune checkpoint inhibitors (ICIs) is an evolving field due to the limitations of conventional imaging in response evaluation. However, real-life data on the benefit of TBP is scarce, especially from the limited resource settings and patients treated in the later lines. Therefore, we aimed to investigate the survival benefit of TBP with ICIs in patients with advanced tumors from a limited resource setting. For this multi-center retrospective cohort study, we included 282 patients treated with ICIs and had radiological progression according to RECIST 1.1 criteria. We evaluated post-progression survival according to the use of TBP (TBP and non-TBP groups) with univariate and multivariate analyses. The cohort's median age was 61, and 84.4% were treated in the second or later lines. 82 (29.1%) of 282 patients continued on ICIs following the initial progression. In multivariate analyses, patients in the TBP group had improved post-progression survival compared to non-TBP (13.18 vs. 4.63 months, HR: 0.500, 95% CI: 0.349-0.717, p < 0.001). The benefit of the TBP was independent of the tumor type, treatment line, and age. Furthermore, TBP with ICIs remained associated with improved post-progression survival (HR: 0.600, 95% CI: 0.380-0.947, p = 0.028) after excluding the patients with no further treatment after progression in the non-TBP arm. In this study, we observed that patients receiving ICIs beyond progression had considerably longer survival. Continuation of ICIs after progression should be considered a reasonable management option for patients with advanced cancer, specifically for patients with limited alternative options.
Identifiants
pubmed: 35960374
doi: 10.1007/s00432-022-04268-8
pii: 10.1007/s00432-022-04268-8
doi:
Substances chimiques
Immune Checkpoint Inhibitors
0
Types de publication
Multicenter Study
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3599-3606Informations de copyright
© 2022. Crown.
Références
Beaver JA, Hazarika M, Mulkey F et al (2018) Patients with melanoma treated with an anti-PD-1 antibody beyond RECIST progression: a US Food and Drug Administration pooled analysis. Lancet Oncol 19(2):229–239. https://doi.org/10.1016/s1470-2045(17)30846-x
doi: 10.1016/s1470-2045(17)30846-x
pubmed: 29361469
pmcid: 5806609
Benavente S, Sánchez-García A et al (2020) Therapy-Induced Modulation of the Tumor Microenvironment: New Opportunities for Cancer Therapies. Frontiers in Oncology. https://doi.org/10.3389/fonc.2020.582884
doi: 10.3389/fonc.2020.582884
pubmed: 33224883
pmcid: 7670964
Bennouna J, Sastre J, Arnold D et al (2013) Continuation of bevacizumab after first progression in metastatic colorectal cancer (ML18147): a randomised phase 3 trial. Lancet Oncol 14(1):29–37. https://doi.org/10.1016/s1470-2045(12)70477-1
doi: 10.1016/s1470-2045(12)70477-1
pubmed: 23168366
Borcoman E, Kanjanapan Y, Champiat S et al (2019) Novel patterns of response under immunotherapy. Ann Oncol 30(3):385–396. https://doi.org/10.1093/annonc/mdz003
doi: 10.1093/annonc/mdz003
pubmed: 30657859
Budimir N, Thomas GD, Dolina JS, Salek-Ardakani S (2022) Reversing T-cell Exhaustion in Cancer: Lessons Learned from PD-1/PD-L1 Immune Checkpoint Blockade. Cancer Immunol Res 10(2):146–153. https://doi.org/10.1158/2326-6066.Cir-21-0515
doi: 10.1158/2326-6066.Cir-21-0515
pubmed: 34937730
Chen S, Zhang Z, Zheng X et al (2021) Response Efficacy of PD-1 and PD-L1 Inhibitors in Clinical Trials: A Systematic Review and Meta-Analysis. Front Oncol. https://doi.org/10.3389/fonc.2021.562315
doi: 10.3389/fonc.2021.562315
pubmed: 35399820
pmcid: 8756138
Czarnecka AM, Sobczuk P, Rogala P et al (2022) Efficacy of immunotherapy beyond RECIST progression in advanced melanoma: a real-world evidence. Cancer Immunol Immunother. https://doi.org/10.1007/s00262-021-03132-x
doi: 10.1007/s00262-021-03132-x
pubmed: 35075516
Dromain C, Beigelman C, Pozzessere C, Duran R, Digklia A (2020) Imaging of tumour response to immunotherapy. European Radiology Experimental 4(1):2–2. https://doi.org/10.1186/s41747-019-0134-1
doi: 10.1186/s41747-019-0134-1
pubmed: 31900689
pmcid: 6942076
Eisenhauer EA, Therasse P, Bogaerts J et al (2009) New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer 45(2):228–247. https://doi.org/10.1016/j.ejca.2008.10.026
doi: 10.1016/j.ejca.2008.10.026
pubmed: 19097774
Emens LA, Ascierto PA, Darcy PK et al (2017) Cancer immunotherapy: Opportunities and challenges in the rapidly evolving clinical landscape. Eur J Cancer 81:116–129. https://doi.org/10.1016/j.ejca.2017.01.035
doi: 10.1016/j.ejca.2017.01.035
pubmed: 28623775
Enomoto T, Tamiya A, Matsumoto K et al (2021) Nivolumab treatment beyond progressive disease in advanced non-small cell lung cancer. Clin Transl Oncol 23(3):582–590. https://doi.org/10.1007/s12094-020-02452-1
doi: 10.1007/s12094-020-02452-1
pubmed: 32661824
Escudier B, Motzer RJ, Sharma P et al (2017) Treatment Beyond Progression in Patients with Advanced Renal Cell Carcinoma Treated with Nivolumab in CheckMate 025. Eur Urol 72(3):368–376. https://doi.org/10.1016/j.eururo.2017.03.037
doi: 10.1016/j.eururo.2017.03.037
pubmed: 28410865
Esfahani K, Roudaia L, Buhlaiga N et al (2020) A review of cancer immunotherapy: from the past, to the present, to the future. Current Oncology(toronto, Ont). https://doi.org/10.3747/co.27.5223
doi: 10.3747/co.27.5223
pubmed: 32368178
Fujimoto D, Yoshioka H, Kataoka Y et al (2019) Pseudoprogression in Previously Treated Patients with Non-Small Cell Lung Cancer Who Received Nivolumab Monotherapy. J Thorac Oncol 14(3):468–474. https://doi.org/10.1016/j.jtho.2018.10.167
doi: 10.1016/j.jtho.2018.10.167
pubmed: 30468872
Gandara DR, von Pawel J, Mazieres J et al (2018) Atezolizumab Treatment Beyond Progression in Advanced NSCLC: Results From the Randomized, Phase III OAK Study. J Thorac Oncol 13(12):1906–1918. https://doi.org/10.1016/j.jtho.2018.08.2027
doi: 10.1016/j.jtho.2018.08.2027
pubmed: 30217492
Ge X, Zhang Z, Zhang S et al (2020) Immunotherapy beyond progression in patients with advanced non-small cell lung cancer. Translational Lung Cancer Research 9(6):2391–2400. https://doi.org/10.21037/tlcr-20-1252
doi: 10.21037/tlcr-20-1252
pubmed: 33489801
pmcid: 7815351
George S, Motzer RJ, Hammers HJ et al (2016) Safety and Efficacy of Nivolumab in Patients With Metastatic Renal Cell Carcinoma Treated Beyond Progression: A Subgroup Analysis of a Randomized Clinical Trial. JAMA Oncol 2(9):1179–1186. https://doi.org/10.1001/jamaoncol.2016.0775
doi: 10.1001/jamaoncol.2016.0775
pubmed: 27243803
pmcid: 5568541
Girard N, Jacoulet P, Gainet M et al (2009) Third-line chemotherapy in advanced non-small cell lung cancer: identifying the candidates for routine practice. J Thorac Oncol 4(12):1544–1549. https://doi.org/10.1097/JTO.0b013e3181bbf223
doi: 10.1097/JTO.0b013e3181bbf223
pubmed: 19884862
Goldinger SM, Buder-Bakhaya K, Lo SN et al (2022) Chemotherapy after immune checkpoint inhibitor failure in metastatic melanoma: a retrospective multicentre analysis. Eur J Cancer 162:22–33. https://doi.org/10.1016/j.ejca.2021.11.022
doi: 10.1016/j.ejca.2021.11.022
pubmed: 34952480
Gonzales Carazas MM, Pinto JA, Casado FL (2021) Biological bases of cancer immunotherapy. Expert Rev Mol Med 23:e3. https://doi.org/10.1017/erm.2021.5
doi: 10.1017/erm.2021.5
pubmed: 33762030
pmcid: 8086397
Goto Y, Tanai C, Yoh K et al (2017) Continuing EGFR-TKI beyond radiological progression in patients with advanced or recurrent, EGFR mutation-positive non-small-cell lung cancer: an observational study. ESMO Open 2(4):e000214–e000214. https://doi.org/10.1136/esmoopen-2017-000214
doi: 10.1136/esmoopen-2017-000214
pubmed: 29018574
pmcid: 5604715
Guven C, D., Sahin, T. K., Dizdar, O., & Kilickap, S. (2020) Predictive biomarkers for immunotherapy efficacy in non-small-cell lung cancer: current status and future perspectives. Biomark Med 14(14):1383–1392. https://doi.org/10.2217/bmm-2020-0310
doi: 10.2217/bmm-2020-0310
pubmed: 33064030
Haddad R, Concha-Benavente F, Blumenschein G Jr et al (2019) Nivolumab treatment beyond RECIST-defined progression in recurrent or metastatic squamous cell carcinoma of the head and neck in CheckMate 141: A subgroup analysis of a randomized phase 3 clinical trial. Cancer 125(18):3208–3218. https://doi.org/10.1002/cncr.32190
doi: 10.1002/cncr.32190
pubmed: 31246283
Haslam A, Prasad V (2019) Estimation of the Percentage of US Patients With Cancer Who Are Eligible for and Respond to Checkpoint Inhibitor Immunotherapy Drugs. JAMA Netw Open 2(5):e192535–e192535. https://doi.org/10.1001/jamanetworkopen.2019.2535
doi: 10.1001/jamanetworkopen.2019.2535
pubmed: 31050774
pmcid: 6503493
Iacovelli R, Ciccarese C, Facchini G et al (2020) Cabozantinib After a Previous Immune Checkpoint Inhibitor in Metastatic Renal Cell Carcinoma: A Retrospective Multi-Institutional Analysis. Target Oncol 15(4):495–501. https://doi.org/10.1007/s11523-020-00732-y
doi: 10.1007/s11523-020-00732-y
pubmed: 32671807
Jia W, Gao Q, Han A, Zhu H, Yu J (2019) The potential mechanism, recognition and clinical significance of tumor pseudoprogression after immunotherapy. Cancer Biol Med 16(4):655–670. https://doi.org/10.20892/j.issn.2095-3941.2019.0144
doi: 10.20892/j.issn.2095-3941.2019.0144
pubmed: 31908886
pmcid: 6936240
Khoja L, Kibiro M, Metser U et al (2016) Patterns of response to anti-PD-1 treatment: an exploratory comparison of four radiological response criteria and associations with overall survival in metastatic melanoma patients. Br J Cancer 115(10):1186–1192. https://doi.org/10.1038/bjc.2016.308
doi: 10.1038/bjc.2016.308
pubmed: 27701388
pmcid: 5104887
Khozin S, Blumenthal GM, Pazdur R (2017) Real-world Data for Clinical Evidence Generation in Oncology. JNCI Journal of the National Cancer Institute. https://doi.org/10.1093/jnci/djx187
doi: 10.1093/jnci/djx187
pubmed: 29059439
Long GV, Weber JS, Larkin J et al (2017) Nivolumab for Patients With Advanced Melanoma Treated Beyond Progression: Analysis of 2 Phase 3 Clinical Trials. JAMA Oncol 3(11):1511–1519. https://doi.org/10.1001/jamaoncol.2017.1588
doi: 10.1001/jamaoncol.2017.1588
pubmed: 28662232
pmcid: 5710191
Luo J, Wu S, Rizvi H et al (2022) Deciphering radiological stable disease to immune checkpoint inhibitors. Ann Oncol. https://doi.org/10.1016/j.annonc.2022.04.450
doi: 10.1016/j.annonc.2022.04.450
pubmed: 35872166
Ma, Y., Wang, Q., Dong, Q., Zhan, L., & Zhang, J. (2019). How to differentiate pseudoprogression from true progression in cancer patients treated with immunotherapy. American journal of cancer research, 9(8), 1546–1553. Retrieved from https://pubmed.ncbi.nlm.nih.gov/31497342
McDermott DF, Lee J-L, Bjarnason GA et al (2021) Open-Label, Single-Arm Phase II Study of Pembrolizumab Monotherapy as First-Line Therapy in Patients With Advanced Clear Cell Renal Cell Carcinoma. J Clin Oncol 39(9):1020–1028. https://doi.org/10.1200/JCO.20.02363
doi: 10.1200/JCO.20.02363
pubmed: 33529051
pmcid: 8078336
Motzer RJ, Escudier B, Oudard S et al (2008) Efficacy of everolimus in advanced renal cell carcinoma: a double-blind, randomised, placebo-controlled phase III trial. Lancet 372(9637):449–456. https://doi.org/10.1016/s0140-6736(08)61039-9
doi: 10.1016/s0140-6736(08)61039-9
pubmed: 18653228
Motzer RJ, Escudier B, McDermott DF et al (2015) Nivolumab versus Everolimus in Advanced Renal-Cell Carcinoma. N Engl J Med 373(19):1803–1813. https://doi.org/10.1056/NEJMoa1510665
doi: 10.1056/NEJMoa1510665
pubmed: 26406148
pmcid: 5719487
Nazha B, Yang JCH, Owonikoko TK (2020) Benefits and limitations of real-world evidence: lessons from EGFR mutation-positive non-small-cell lung cancer. Future Oncol 17(8):965–977. https://doi.org/10.2217/fon-2020-0951
doi: 10.2217/fon-2020-0951
pubmed: 33242257
Nishino M, Giobbie-Hurder A, Manos MP et al (2017) Immune-Related Tumor Response Dynamics in Melanoma Patients Treated with Pembrolizumab: Identifying Markers for Clinical Outcome and Treatment Decisions. Clinical Cancer Research : an Official Journal of the American Association for Cancer Research 23(16):4671–4679. https://doi.org/10.1158/1078-0432.CCR-17-0114
doi: 10.1158/1078-0432.CCR-17-0114
pubmed: 28592629
Park K, Yu CJ, Kim SW et al (2016) First-Line Erlotinib Therapy Until and Beyond Response Evaluation Criteria in Solid Tumors Progression in Asian Patients With Epidermal Growth Factor Receptor Mutation-Positive Non-Small-Cell Lung Cancer: The ASPIRATION Study. JAMA Oncol 2(3):305–312. https://doi.org/10.1001/jamaoncol.2015.4921
doi: 10.1001/jamaoncol.2015.4921
pubmed: 26720423
Ricciuti B, Genova C, Bassanelli M et al (2019) Safety and Efficacy of Nivolumab in Patients With Advanced Non-small-cell Lung Cancer Treated Beyond Progression. Clin Lung Cancer 20(3):178-185.e172. https://doi.org/10.1016/j.cllc.2019.02.001
doi: 10.1016/j.cllc.2019.02.001
pubmed: 30910574
Rittmeyer A, Barlesi F, Waterkamp D et al (2017) Atezolizumab versus docetaxel in patients with previously treated non-small-cell lung cancer (OAK): a phase 3, open-label, multicentre randomised controlled trial. The Lancet 389(10066):255–265. https://doi.org/10.1016/S0140-6736(16)32517-X
doi: 10.1016/S0140-6736(16)32517-X
Robert C, Long GV, Brady B et al (2014) Nivolumab in Previously Untreated Melanoma without BRAF Mutation. N Engl J Med 372(4):320–330. https://doi.org/10.1056/NEJMoa1412082
doi: 10.1056/NEJMoa1412082
pubmed: 25399552
Schuler M, Yang JCH, Park K et al (2016) Afatinib beyond progression in patients with non-small-cell lung cancer following chemotherapy, erlotinib/gefitinib and afatinib: phase III randomized LUX-Lung 5 trial. Ann Oncol 27(3):417–423. https://doi.org/10.1093/annonc/mdv597
doi: 10.1093/annonc/mdv597
pubmed: 26646759
Seymour L, Bogaerts J, Perrone A et al (2017) iRECIST: guidelines for response criteria for use in trials testing immunotherapeutics. Lancet Oncol 18(3):e143–e152. https://doi.org/10.1016/s1470-2045(17)30074-8
doi: 10.1016/s1470-2045(17)30074-8
pubmed: 28271869
pmcid: 5648544
Sharma P, Hu-Lieskovan S, Wargo JA, Ribas A (2017) Primary, Adaptive, and Acquired Resistance to Cancer Immunotherapy. Cell 168(4):707–723. https://doi.org/10.1016/j.cell.2017.01.017
doi: 10.1016/j.cell.2017.01.017
pubmed: 28187290
pmcid: 5391692
Vaddepally RK, Kharel P, Pandey R, Garje R, Chandra AB (2020) Review of Indications of FDA-Approved Immune Checkpoint Inhibitors per NCCN Guidelines with the Level of Evidence. Cancers (basel). https://doi.org/10.3390/cancers12030738
doi: 10.3390/cancers12030738
pubmed: 32245016
Wang Z-X, Wu H-X, Xie L et al (2021) Exploration of modified progression-free survival as a novel surrogate endpoint for overall survival in immuno-oncology trials. J Immunother Cancer 9(4):e002114. https://doi.org/10.1136/jitc-2020-002114
doi: 10.1136/jitc-2020-002114
pubmed: 33795385
pmcid: 8021890
Yang J, Zhang Q, Wang J et al (2022) Dynamic profiling of immune microenvironment during pancreatic cancer development suggests early intervention and combination strategy of immunotherapy. EBioMedicine. https://doi.org/10.1016/j.ebiom.2022.103958
doi: 10.1016/j.ebiom.2022.103958
pubmed: 36571902
pmcid: 9800295
Yu X, Chu X, Wu Y et al (2021) Favorable clinical outcomes of checkpoint inhibitor-based combinations after progression with immunotherapy in advanced non-small cell lung cancer. Cancer Drug Resistance (alhambra, Calif). 4(3):728–739
pubmed: 35582303
pmcid: 9086517