Indirect comparison of nivolumab ± ipilimumab (CheckMate 032) versus other treatments for recurrent small-cell lung cancer
Publication: Journal of Comparative Effectiveness Research
Abstract
Aim: To estimate the comparative efficacy of nivolumab ± ipilimumab versus alternative treatments for small-cell lung cancer after at least one prior line of chemotherapy. Materials & m ethods: A systematic literature review identified six randomized controlled trials (RCTs) that could be connected in a network. The Kaplan–Meier survival curves from these RCTs were synthesized using network meta-analysis models. Aggregate-level matching was used to connect CheckMate 032 to the RCTs. Results: CheckMate 032 was connected to the network by Amrubicin Clinical Trial-1. Nivolumab ± ipilimumab had a more durable tumor response and more favorable long-term survival versus topotecan via intravenous and versus amrubicin. Conclusion: Compared with chemotherapies for recurrent small-cell lung cancer, nivolumab ± ipilimumab improves response duration, which may translate to long-term survival benefits.
Supplementary Material
File (supplementarymaterial.docx)
- Download
- 368.56 KB
References
1.
Byers LA, Rudin CM. Small cell lung cancer: where do we go from here? Cancer 121(5), 664–672 (2015).
2.
Van Meerbeeck JP, Fennell DA, De Ruysscher DK. Small-cell lung cancer. Lancet 378(9804), 1741–1755 (2011).
3.
Früh M, De Ruysscher D, Popat S, Crino L, Peters S, Felip E. Small-cell lung cancer (SCLC): ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann. Oncol. 24(Suppl. 6), vi99–vi105 (2013).
4.
Rudin CM, Ismaila N, Hann CL et al. Treatment of small-cell lung cancer: American Society of Clinical Oncology endorsement of the American College of Chest Physicians Guideline. J. Clin. Oncol. 33(34), 4106–4111 (2015).
5.
Micke P, Faldum A, Metz T et al. Staging small cell lung cancer: Veterans Administration Lung Study Group versus International Association for the Study of Lung Cancer – what limits limited disease? Lung Cancer 37(3), 271–276 (2002).
6.
Turrisi AT 3rd, Kim K, Blum R et al. Twice-daily compared with once-daily thoracic radiotherapy in limited small-cell lung cancer treated concurrently with cisplatin and etoposide. N. Engl. J. Med. 340(4), 265–271 (1999).
7.
Chan BA, Coward JI. Chemotherapy advances in small-cell lung cancer. J. Thorac. Dis. 5(Suppl. 5), S565–S578 (2013).
8.
Simon GR, Turrisi A. Management of small cell lung cancer: ACCP evidence-based clinical practice guidelines (2nd edition). Chest 132(3 Suppl.), 324S–339S (2007).
9.
Hurwitz JL, McCoy F, Scullin P, Fennell DA. New advances in the second-line treatment of small cell lung cancer. Oncologist 14(10), 986–994 (2009).
10.
National Comprehensive Cancer Network. Small cell lung cancer (Version 1.2019) (2018). www.nccn.org/professionals/physician_gls/pdf/sclc_blocks.pdf
11.
Waqar SN, Morgensztern D. Treatment advances in small cell lung cancer (SCLC). Pharmacol. Ther. 180, 16–23 (2017).
12.
O'Brien ME, Ciuleanu TE, Tsekov H et al. Phase III trial comparing supportive care alone with supportive care with oral topotecan in patients with relapsed small-cell lung cancer. J. Clin. Oncol. 24(34), 5441–5447 (2006).
13.
Von Pawel J, Gatzemeier U, Pujol JL et al. Phase II comparator study of oral versus intravenous topotecan in patients with chemosensitive small-cell lung cancer. J. Clin. Oncol. 19(6), 1743–1749 (2001).
14.
Eckardt JR, Von Pawel J, Pujol JL et al. Phase III study of oral compared with intravenous topotecan as second-line therapy in small-cell lung cancer. J. Clin. Oncol. 25(15), 2086–2092 (2007).
15.
Von Pawel J, Jotte R, Spigel DR et al. Randomized Phase III trial of amrubicin versus topotecan as second-line treatment for patients with small-cell lung cancer. J. Clin. Oncol. 32(35), 4012–4019 (2014).
16.
Jotte R, Conkling P, Reynolds C et al. Randomized Phase II trial of single-agent amrubicin or topotecan as second-line treatment in patients with small-cell lung cancer sensitive to first-line platinum-based chemotherapy. J. Clin. Oncol. 29(3), 287–293 (2011).
17.
Von Pawel J, Schiller JH, Shepherd FA et al. Topotecan versus cyclophosphamide, doxorubicin, and vincristine for the treatment of recurrent small-cell lung cancer. J. Clin. Oncol. 17(2), 658–667 (1999).
18.
Danese M, Gleeson M, Lubeck D, Penrod J, Korytowsky B, Yuan Y. P1.15-003 Survival by response to first-line platinum-based therapy among patients with extensive disease small cell lung cancer. J. Thorac. Oncol. 12(11), S2044 (2017).
19.
Antonia SJ, Lopez-Martin JA, Bendell J et al. Nivolumab alone and nivolumab plus ipilimumab in recurrent small-cell lung cancer (CheckMate 032): a multicentre, open-label, Phase 1/2 trial. Lancet Oncol. 17(7), 883–895 (2016).
20.
Taylor M, Antonia S, Bendell J et al. Phase I/II study of nivolumab with or without ipilimumab for treatment of recurrent small cell lung cancer (SCLC): CA209–032. J. Immunother. Cancer 3(Suppl. 2), P376 (2015).
21.
Antonia SJ, Lopez-Martin JA, Bendell JC et al. Checkmate 032: Nivolumab (N) alone or in combination with ipilimumab (I) for the treatment of recurrent small cell lung cancer (SCLC). J. Clin. Oncol. 34(15 Suppl.), 100–100 (2016).
22.
Hellmann M, Ott PA, Zugazagoitia J et al. Nivolumab±ipilimumab in advanced small cell lung cancer: first report of a randomized cohort from CheckMate 032. Presented at: ASCO Annual Meeting. IL, USA, 2–6 June 2017.
23.
Hellmann MD, Callahan MK, Awad MM et al. Tumor mutational burden and efficacy of nivolumab monotherapy and in combination with ipilimumab in small-cell lung cancer. Cancer Cell 33(5), 853–861.e4 (2018).
24.
Opdivo Prescribing Information. Opdivo US Product Information. Bristol-Myers Squibb Company, NJ, USA (2018).
25.
Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J. Clin. Epidemiol. 62(10), 1006–1012 (2009).
26.
Dias S, Welton NJ, Sutton AJ, Caldwell DM, Lu G, Ades AE. Evidence synthesis for decision making 4: inconsistency in networks of evidence based on randomized controlled trials. Med. Decis. Making 33(5), 641–656 (2013).
27.
Jansen JP. Network meta-analysis of survival data with fractional polynomials. BMC Med. Res. Methodol. 11, 61 (2011).
28.
Lu G, Ades AE. Combination of direct and indirect evidence in mixed treatment comparisons. Stat. Med. 23(20), 3105–3124 (2004).
29.
Mills EJ, Ioannidis JP, Thorlund K, Schunemann HJ, Puhan MA, Guyatt GH. How to use an article reporting a multiple treatment comparison meta-analysis. JAMA 308(12), 1246–1253 (2012).
30.
Jansen JP, Naci H. Is network meta-analysis as valid as standard pairwise meta-analysis? It all depends on the distribution of effect modifiers. BMC Med. 11, 159 (2013).
31.
Phillippo DM, Ades AE, Dias S, Palmer S, Abrams KR, Welton KJ. NICE DSU Technical support document 18: methods for population-adjusted indirect comparisons in submissions to NICE (2016). https://scharr.dept.shef.ac.uk/nicedsu/wp-content/uploads/sites/7/2017/05/Population-adjustment-TSD-FINAL.pdf
32.
Ouwens MJNM, Philips Z, Jansen JP. Network meta-analysis of parametric survival curves. Res. Synth. Methods 1(3–4), 258–271 (2011).
33.
Jansen JP, Cope S. Meta-regression models to address heterogeneity and inconsistency in network meta-analysis of survival outcomes. BMC Med. Res. Methodol. 12(1), 152–152 (2012).
34.
Woods BS, Hawkins N, Scott DA. Network meta-analysis on the log-hazard scale, combining count and hazard ratio statistics accounting for multi-arm trials: a tutorial. BMC Med. Res. Methodol. 10, 54 (2010).
35.
Spiegelhalter D, Thomas A, Best N, Lunn D. WinBUGS user manual version 1.4. (2003). www.mrc-bsu.cam.ac.uk/wp-content/uploads/manual14.pdf
36.
Lunn D, Spiegelhalter D, Thomas A, Best N. The BUGS project: evolution, critique and future directions. Statist. Med. 28, 3049–3067 (2009).
37.
Evans TL, Cho BC, Udud K et al. Cabazitaxel versus topotecan in patients with small-cell lung cancer with progressive disease during or after first-line platinum-based chemotherapy. J. Thorac. Oncol. 10(8), 1221–1228 (2015).
38.
Evans T, Cho BC, Udud K et al. Cabazitaxel (Cbz) Vs topotecan (Tpt) in patients (Pts) with small cell lung cancer (SCLC) with progressive disease during/after first-line (1l) treatment with platinum-based chemotherapy (Ctx). Presented at: European Lung Cancer Conference 2014. Geneva, Switzerland, 26–29 March 2014.
39.
Clinical Trials Database: NCT01500720. https://clinicaltrials.gov/ct2/show/NCT01500720?term=NCT01500720&rank=1
40.
Chiappori AA, Otterson GA, Dowlati A et al. A randomized Phase II study of linsitinib (OSI-906) versus topotecan in patients with relapsed small-cell lung cancer. Oncologist 21(10), 1163–1164 (2016).
41.
Gervais R, Le Caer H, Monnet I et al. Second-line oral chemotherapy (lomustine, cyclophosphamide, etoposide) versus intravenous therapy (cyclophosphamide, doxorubicin, and vincristine) in patients with relapsed small cell lung cancer: a randomized Phase II study of GFPC 0501. Clin. Lung Cancer 16(2), 100–105 (2015).
42.
Goto K, Ohe Y, Shibata T et al. Combined chemotherapy with cisplatin, etoposide, and irinotecan versus topotecan alone as second-line treatment for patients with sensitive relapsed small-cell lung cancer (JCOG0605): a multicentre, open-label, randomised Phase 3 trial. Lancet Oncol. 17(8), 1147–1157 (2016).
43.
Seto T, Goto K, Takahashi T et al. O1-21-6A Phase III study of CDDP, ETOP and irinotecan vs, topotecan as 2nd-line chemotherapy for sensitive relaspsed SCLC: JCOG0605. Ann. Oncol. 25(Suppl. 5), v56–v57 (2014).
44.
Inoue A, Sugawara S, Yamazaki K et al. Randomized Phase II trial comparing amrubicin with topotecan in patients with previously treated small-cell lung cancer: North Japan Lung Cancer Study Group Trial 0402. J. Clin. Oncol. 26(33), 5401–5406 (2008).
45.
Nakamura A, Inoue A, Maemondo M et al. Randomized Phase 2 trial comparing amrubicin (A) with re-challenge of platinum doublet (P) in patients (pts) with sensitive-relapsed small-cell lung cancer (SCLC). J. Clin. Oncol. 32(15 Suppl.), 7520–7520 (2014).
46.
Inoue A, Sugawara S, Maemondo M et al. Randomized Phase II trial comparing amrubicin with re-challenge of platinum doublet in patients with sensitive-relapsed small-cell lung cancer: North Japan Lung Cancer Study Group trial 0702. Lung Cancer 89(1), 61–65 (2015).
47.
Chen L, Antras L, Duh MS, Neary M, O'Brien MER. Symptom assessment in relapsed small cell lung cancer: cross-validation of the patient symptom assessment in lung cancer instrument. J. Thorac. Oncol. 3(10), 1137–1145 (2008).
48.
O'Bryan RM, Crowley JJ, Kim PN et al. Comparison of etoposide and cisplatin with bis-chloro-ethylnitrosourea, thiotepa, vincristine, and cyclophosphamide for salvage treatment in small cell lung cancer. A Southwest Oncology Group Study. Cancer 65(4), 856–860 (1990).
49.
Pallis AG, Agelidou A, Agelaki S et al. A multicenter randomized Phase II study of the irinotecan/gemcitabine doublet versus irinotecan monotherapy in previously treated patients with extensive stage small-cell lung cancer. Lung Cancer 65(2), 187–191 (2009).
50.
Sculier JP, Lafitte JJ, Lecomte J et al. A Phase II randomised trial comparing the cisplatin–etoposide combination chemotherapy with or without carboplatin as second-line therapy for small-cell lung cancer. Ann. Oncol. 13(9), 1454–1459 (2002).
51.
Sekine CI, Harada H, Yamamoto N et al. Randomized Phase II trial of code or amrubicin plus cisplatin chemotherapy after chemoradiotherapy for limited-disease small cell lung. J. Thorac. Dis. 2, S400 (2015).
52.
Allen JW, Moon J, Redman M et al. Southwest Oncology Group S0802: a randomized, Phase II trial of weekly topotecan with and without ziv-aflibercept in patients with platinum-treated small-cell lung cancer. J. Clin. Oncol. 32(23), 2463–2470 (2014).
53.
Clinical Trials Database: NCT00828139. https://clinicaltrials.gov/ct2/show/NCT00828139?term=NCT00828139&rank=1
54.
Chen L, Antras L, Mei SD et al. Psychometric validation of the patient symptom assessment in lung cancer instrument for small cell lung cancer. Curr. Med. Res. Opin. 23(11), 2741–2752 (2007).
55.
Yoon S, Lee DH, Choi CM, Lee JC, Lee JS, Kim SW. Randomized Phase II study of belotecan or topotecan as second-line chemotherapy after platinum based chemotherapy for small cell lung cancer. J. Thorac. Dis. 2, S787–S788 (2015).
56.
Loveman E, Jones J, Hartwell D et al. The clinical effectiveness and cost–effectiveness of topotecan for small cell lung cancer: a systematic review and economic evaluation. Health Technol. Assess. 14(19), 1–204 (2010).
57.
Navada S, Lai P, Schwartz AG, Kalemkerian GP. Temporal trends in small cell lung cancer: analysis of the national Surveillance, Epidemiology, and End-Results (SEER) database. J. Clin. Oncol. 24(18 Suppl.), 7082–7082 (2006).
58.
Source: Bristol-Myers Squibb. Bristol-Myers Squibb announces Phase 3 CheckMate -331 study does not meet primary endpoint of overall survival with Opdivo versus chemotherapy in patients with previously treated relapsed small cell lung cancer. Press release: https://news.bms.com/press-release/corporatefinancial-news/bristol-myers-squibb-announces-phase-3-checkmate-331-study-doe
59.
Horn L, Mansfield AS, Szczęsna A et al. First-line atezolizumab plus chemotherapy in extensive-stage small-cell lung cancer. N. Engl. J. Med. 379(23), 2220–2229 (2018).
60.
Clinical Trialss Database: NCT02538666. https://clinicaltrials.gov/ct2/show/NCT02538666
61.
Hellmann MD, Nathanson T, Rizvi H et al. Genomic features of response to combination immunotherapy in patients with advanced non-small-cell lung cancer. Cancer Cell 33(5), 843–852 e844 (2018).
62.
Carbone DP, Reck M, Paz-Ares L et al. First-line nivolumab in stage IV or recurrent non-small-cell lung cancer. N. Engl. J. Med. 376(25), 2415–2426 (2017).
63.
Galsky MD, Saci A, Szabo PM et al. Impact of tumor mutation burden on nivolumab efficacy in second-line urothelial carcinoma patients: exploratory analysis of the Phase II CheckMate 275 study, [abstract 848PD]. Ann. Oncol. 28(Suppl. 5), v295–v329 (2017).
64.
Snyder A, Makarov V, Merghoub T et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N. Engl. J. Med. 371(23), 2189–2199 (2014).
65.
Boumber Y. Tumor mutational burden (TMB) as a biomarker of response to immunotherapy in small cell lung cancer. J. Thorac. Dis. 10(8), 4689–4693 (2018).
Information & Authors
Information
Published In
Pages: 733 - 751
PubMed: 31237143
Copyright
© 2019 Future Medicine Ltd.
History
Received: 3 December 2018
Accepted: 7 May 2019
Published online: 25 June 2019
Keywords:
Topics
Authors
Metrics & Citations
Metrics
Article Usage
Article usage data only available from February 2023. Historical article usage data, showing the number of article downloads, is available upon request.
Citations
How to Cite
Indirect comparison of nivolumab ± ipilimumab (CheckMate 032) versus other treatments for recurrent small-cell lung cancer. (2019) Journal of Comparative Effectiveness Research. DOI: 10.2217/cer-2018-0130
Export citation
Select the citation format you wish to export for this article or chapter.
Citing Literature
- Luis Guilherme de Oliveira Silva, Fabian Fellipe Bueno Lemos, Marcel Silva Luz, Samuel Luca Rocha Pinheiro, Mariana dos Santos Calmon, Gabriel Lima Correa Santos, Gabriel Reis Rocha, Fabrício Freire de Melo, New avenues for the treatment of immunotherapy-resistant pancreatic cancer, World Journal of Gastrointestinal Oncology, 10.4251/wjgo.v16.i4.1134, 16, 4, (1134-1153), (2024).
- Julie E. Park, Harlan Campbell, Kevin Towle, Yong Yuan, Jeroen P. Jansen, David Phillippo, Shannon Cope, Unanchored Population-Adjusted Indirect Comparison Methods for Time-to-Event Outcomes Using Inverse Odds Weighting, Regression Adjustment, and Doubly Robust Methods With Either Individual Patient or Aggregate Data, Value in Health, 10.1016/j.jval.2023.11.011, 27, 3, (278-286), (2024).
- Song Zhang, Small Cell Lung Carcinoma, Diagnostic Imaging of Lung Cancers, 10.1007/978-981-99-6815-2_3, (65-78), (2024).
- Cinzia Vetrei, Margherita Passariello, Guendalina Froechlich, Rosa Rapuano Lembo, Nicola Zambrano, Claudia De Lorenzo, Immunomodulatory mAbs as Tools to Investigate on Cis-Interaction of PD-1/PD-L1 on Tumor Cells and to Set Up Methods for Early Screening of Safe and Potent Combinatorial Treatments, Cancers, 10.3390/cancers13122858, 13, 12, (2858), (2021).
- Sam T Keeping, Shannon Cope, Keith Chan, Florence R Wilson, Jeroen P Jansen, John R Penrod, Pranav Abraham, D Ross Camidge, Beata Korytowsky, Tao Gu, Ariadna Juarez Garcia, Trong K Le, Yong Yuan, Comparative effectiveness of nivolumab versus standard of care for third-line patients with small-cell lung cancer, Journal of Comparative Effectiveness Research, 10.2217/cer-2020-0134, 9, 18, (1275-1284), (2020).
- Venu Madhav Konala, Bhaskar Reddy Madhira, Sara Ashraf, Stephen Graziano, Use of Immunotherapy in Extensive-Stage Small Cell Lung Cancer, Oncology, 10.1159/000508516, 98, 11, (749-754), (2020).
- Jingjie Chen, Shengnan Li, Qigu Yao, Nannan Du, Xiaojun Fu, Yuanmei Lou, Mengru Wang, Feiyan Mao, Danyi Mao, Parikshit Asutosh Khadaroo, Yingying Tang, The efficacy and safety of combined immune checkpoint inhibitors (nivolumab plus ipilimumab): a systematic review and meta-analysis, World Journal of Surgical Oncology, 10.1186/s12957-020-01933-5, 18, 1, (2020).