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Overall Survival with Combined Nivolumab and Ipilimumab in Advanced Melanoma
Open accessAbstract
BACKGROUND: Nivolumab combined with ipilimumab resulted in longer progression-free survival and a higher objective response rate than ipilimumab alone in a phase 3 trial involving patients with advanced melanoma. We now report 3-year overall survival outcomes in this trial. METHODS: We randomly assigned, in a 1:1:1 ratio, patients with previously untreated advanced melanoma to receive nivolumab at a dose of 1 mg per kilogram of body weight plus ipilimumab at a dose of 3 mg per kilogram every 3 weeks for four doses, followed by nivolumab at a dose of 3 mg per kilogram every 2 weeks; nivolumab at a dose of 3 mg per kilogram every 2 weeks plus placebo; or ipilimumab at a dose of 3 mg per kilogram every 3 weeks for four doses plus placebo, until progression, the occurrence of unacceptable toxic effects, or withdrawal of consent. Randomization was stratified according to programmed death ligand 1 (PD-L1) status, BRAF mutation status, and metastasis stage. The two primary end points were progression-free survival and overall survival in the nivolumab-plus-ipilimumab group and in the nivolumab group versus the ipilimumab group. RESULTS: At a minimum follow-up of 36 months, the median overall survival had not been reached in the nivolumab-plus-ipilimumab group and was 37.6 months in the nivolumab group, as compared with 19.9 months in the ipilimumab group (hazard ratio for death with nivolumab plus ipilimumab vs. ipilimumab, 0.55 [P<0.001]; hazard ratio for death with nivolumab vs. ipilimumab, 0.65 [P<0.001]). The overall survival rate at 3 years was 58% in the nivolumab-plus-ipilimumab group and 52% in the nivolumab group, as compared with 34% in the ipilimumab group. The safety profile was unchanged from the initial report. Treatment-related adverse events of grade 3 or 4 occurred in 59% of the patients in the nivolumab-plus-ipilimumab group, in 21% of those in the nivolumab group, and in 28% of those in the ipilimumab group. CONCLUSIONS: Among patients with advanced melanoma, significantly longer overall survival occurred with combination therapy with nivolumab plus ipilimumab or with nivolumab alone than with ipilimumab alone. (Funded by Bristol-Myers Squibb and others; CheckMate 067 ClinicalTrials.gov number, NCT01844505 .).
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“with anti-PD-1 and anti-PD-1/CTLA-4 combination therapy emerging as most effective [3, 4].”
From Relating the gut metagenome and metatranscriptome to immunotherapy responses in melanoma patients (2019) · cites this paper as [4]
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“3-year overall survival rates were 58%, 52%, and 34% in combination therapy, anti-PD-1, and anti-CTLA-4 groups, respectively [4].”
From Relating the gut metagenome and metatranscriptome to immunotherapy responses in melanoma patients (2019) · cites this paper as [4]
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“These chemokines have been identified as the dominant mediators for the recruitment of CXCR3+ and CCR5+ tumor-specific T lymphocytes into the tumors and their intratumoral expression correlated with favorable clinical outcomes in patients with melanoma30–32.”
From Epigenetic state determines the in vivo efficacy of STING agonist therapy (2023) · cites this paper as [30]
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“Third, many of these studies utilized ICIs as monotherapy in a heavily pretreated population whereas current standard first-line therapy often includes a combination of ICIs or ICI with chemotherapy for multiple tumor types (35–40).”
From A Uniform Computational Approach Improved on Existing Pipelines to Reveal Microbiome Biomarkers of Nonresponse to Immune Checkpoint Inhibitors (2021) · cites this paper as [36]
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“By contrast, ICB has shown promise in the adjuvant setting in patients with melanoma or NSCLC57–59”
From Enhancing cancer immunotherapy using antiangiogenics: opportunities and challenges (2018) · cites this paper as [59]
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Immune checkpoint inhibitors: new strategies to checkmate cancer
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“In an open-label, randomized, Phase III study involving patients with ipilimumab-refractory melanoma, nivolumab was associated with a higher ORR than chemotherapy (32 versus 11”
BackgroundInfluentialSevere toxicity from checkpoint protein inhibitors: What intensive care physicians need to know?
Lemiale, V., Meert, A., Vincent, F., Darmon, M., Bauer, P. R., de Louw, A. V., & Azoulay, É. (2019) · Annals of Intensive Care · doi:10.1186/s13613-019-0487-x · Cited by 73
Rogiers, A., Boekhout, A. H., Schwarze, J. K., Awada, G., Blank, C. U., & Neyns, B. (2019) · Journal of Oncology · doi:10.1155/2019/5269062 · Cited by 72
Beyond PD-1/PD-L1 Inhibition: What the Future Holds for Breast Cancer Immunotherapy
Chrétien, S., Zerdes, I., Bergh, J. C. S., Matikas, A., & Foukakis, T. (2019) · Cancers · doi:10.3390/cancers11050628 · Cited by 71
“70) compared with nivolumab alone in patients with metastatic melanoma and PD-L1 expression lower than 1% [350].”
T Cell–Activating Bispecific Antibodies in Cancer Therapy
Trabolsi, A., Arumov, A., & Schatz, J. H. (2019) · The Journal of Immunology · doi:10.4049/jimmunol.1900496 · Cited by 71
“Successful development efforts include immune checkpoint inhibitors to counteract tumors’ immune-inhibitory signals (3, 4), reprogramming of T cells to attack tumors with chimeric Ag receptors (CARs) (5, 6), and, finally, bispecific Abs”
BackgroundHauschild, A., Ascierto, P. A., Schadendorf, D., Grob, J., Ribas, A., Kiecker, F., Dutriaux, C., Демидов, Л. В., Lebbé, C., Rutkowski, P. L., et al. (2020) · European Journal of Cancer · doi:10.1016/j.ejca.2019.10.033 · Cited by 70
Self-citationBomze, D., Meirson, T., Ali, O. H., Goldman, A., Flatz, L., & Habot‐Wilner, Z. (2020) · Ocular Immunology and Inflammation · doi:10.1080/09273948.2020.1773867 · Cited by 70
“Combination therapy of anti-PD-1 and anti-CTLA-4 increases both the frequency and severity of irAEs, with grade 3–4 rate of 59% for nivolumab with ipilimumab versus 21% to 28% for nivolumab or ipilimumab as single agents.(5) Although the eye is considered an immune-privileged site, to date ocular adverse events (oAEs)…”
BackgroundResultThe Evolution of STING Signaling and Its Involvement in Cancer
Vashi, N., & Bakhoum, S. F. W. (2021) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2020.12.010 · Cited by 72
Zhang, Q., Zheng, D., Dong, X., Pan, P., Zeng, S.-M., Gao, F., Cheng, S., & Zhang, X. (2021) · Journal of the American Chemical Society · doi:10.1021/jacs.1c00945 · Cited by 70
Levi, S. T., Copeland, A. R., Nah, S., Crystal, J. S., Ivey, G. D., Lalani, A., Jafferji, M. S., White, B. S., Parikh, N. B., Leko, V., et al. (2022) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-21-4499 · Cited by 72
PRMT7 ablation stimulates anti-tumor immunity and sensitizes melanoma to immune checkpoint blockade
Srour, N., Villarreal, O. D., Hardikar, S., Yu, Z., Preston, S. E. J., Miller, W. H., Szewczyk, M. M., Baršytė-Lovejoy, D., Xu, H., Chen, T., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110582 · Cited by 70
Pavlick, A. C., Ariyan, C. E., Buchbinder, E. I., Davar, D., Gibney, G. T., Hamid, O., Hieken, T. J., Izar, B., Johnson, D. B., Kulkarni, R. P., et al. (2023) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2023-006947 · Cited by 74
Targeting antigen-presenting cells by anti–PD-1 nanoparticles augments antitumor immunity
Ordikhani, F., Uehara, M., Kasinath, V., Dai, L., Eskandari, S. K., Bahmani, B., Yonar, M., Azzi, J. R., Haik, Y., Sage, P. T., et al. (2018) · JCI Insight · doi:10.1172/jci.insight.122700 · Cited by 70
“Nearly 21% of patients treated with nivolumab develop treatment-related adverse effects (10).”
BackgroundInfluential2018 Nobel Prize in physiology or medicine
Smyth, M. J., & Teng, M. W. L. (2018) · Clinical & Translational Immunology · doi:10.1002/cti2.1041 · Cited by 71
“The ultimate in confluence of these approaches came with the description of superior outcomes in advanced melanoma in patients receiving a combination of anti-CTLA-4 and anti-PD-1.(6) This contemporary revolution in cancer treatment owes its success to the dedication and insight that James Allison and Tasuku Honjo dis…”
BackgroundRådestad, E., Klynning, C., Stikvoort, A., Mogensen, O. E., Nava, S., Magalhaes, I., & Uhlin, M. (2018) · OncoImmunology · doi:10.1080/2162402x.2018.1535730 · Cited by 71
“Combination treatment has improved outcome compared to monotherapy but at the cost of increased treatmentrelated toxicities.(12,13) It is clear that much remains to be explored regarding identification of targets, treatment modality, cancer types and benefitting patient groups to further improve the use of checkpoint…”
BackgroundIn Vivo Delivery of Nucleic Acid-Encoded Monoclonal Antibodies
Patel, A. R., Bah, M. A., & Weiner, D. B. (2020) · BioDrugs · doi:10.1007/s40259-020-00412-3 · Cited by 73
Kidney Complications of Immune Checkpoint Inhibitors: A Review
Shingarev, R. A., & Glezerman, I. G. (2019) · American Journal of Kidney Diseases · doi:10.1053/j.ajkd.2019.03.433 · Cited by 70
Neurotoxicities associated with immune checkpoint inhibitor therapy
Duong, S. L.-L., Barbiero, F. J., Nowak, R. J., & Baehring, J. M. (2021) · Journal of Neuro-Oncology · doi:10.1007/s11060-021-03695-w · Cited by 69
Gudd, C. L. C., Au, L., Triantafyllou, E., Shum, B., Liu, T., Nathwani, R., Kumar, N., Mukherjee, S. K., Dhar, A., Woollard, K. J., et al. (2021) · Journal of Hepatology · doi:10.1016/j.jhep.2021.02.008 · Cited by 69
Self-citationPrognostic and Predictive Factors in Advanced Head and Neck Squamous Cell Carcinoma
Magnes, T., Wagner, S. M., Kiem, D., Weiß, L., Rinnerthaler, G., Greil, R., & Melchardt, T. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22094981 · Cited by 74
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Progress in the cryoablation and cryoimmunotherapy for tumor
Chen, Z., Meng, L., Zhang, J., & Zhang, X. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1094009 · Cited by 69
“The combination of CTLA-4 and PD-1 blockade has been shown to improve survival in patients with melanoma, renal cell carcinoma, and many other cancers (85, 86).”
BackgroundGargett, T., Truong, N. T., Gardam, B., Yu, W., Ebert, L. M., Johnson, A., Yeo, E. C. F., Wittwer, N. L., Rico, G. T., Logan, J., et al. (2024) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2023-008659 · Cited by 70
Paulson, K. G., Lahman, M. C., Chapuis, A. G., & Brownell, I. (2019) · International Immunology · doi:10.1093/intimm/dxz012 · Cited by 71
Ocular Adverse Events following Use of Immune Checkpoint Inhibitors for Metastatic Malignancies
Noble, C. W., Gangaputra, S. S., Thompson, I., Yuan, A., Apolo, A. B., Lee, J., Papaliodis, G. N., Kodati, S., Bishop, R. J., Magone, M. T., et al. (2019) · Ocular Immunology and Inflammation · doi:10.1080/09273948.2019.1583347 · Cited by 69
Rewriting History: Epigenetic Reprogramming of CD8+ T Cell Differentiation to Enhance Immunotherapy
Zebley, C. C., Gottschalk, S. M., & Youngblood, B. (2020) · Trends in Immunology · doi:10.1016/j.it.2020.06.008 · Cited by 71
Cardiotoxicity of Immunotherapy: Incidence, Diagnosis, and Management
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“BRAF mutation status was recently reported to describe populations with differing OS after immune checkpoint inhibitors [20].”
BackgroundSelf-citationWhat, Why, Where, and When: Bringing Timing to Immuno-Oncology
Rothschilds, A. M., & Wittrup, K. D. (2018) · Trends in Immunology · doi:10.1016/j.it.2018.11.003 · Cited by 68
The microenvironment in myeloma
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Comprehensive analysis of cutaneous and uveal melanoma liver metastases
Hoefsmit, E. P., Rozeman, E. A., Van, T. M., Dimitriadis, P., Krijgsman, O., Conway, J. W., da Silva, I. P., van der Wal, J. E., Ketelaars, S. L. C., Bresser, K., et al. (2020) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2020-001501 · Cited by 69
Self-citationONCR-177, an Oncolytic HSV-1 Designed to Potently Activate Systemic Antitumor Immunity
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“However, systemic administration as a monotherapy or in combination is associated with immune-mediated adverse events that can be severe (46, 47).”
Virus-specific memory T cell responses unmasked by immune checkpoint blockade cause hepatitis
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MHC Class I Deficiency in Solid Tumors and Therapeutic Strategies to Overcome It
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“Combined immunotherapy (anti-PD1 plus anti-CTLA-4) results in higher objective response rates [2] but is also associated with significant immune-related toxicities that are often severe and can be life-threatening [10,11].”
BackgroundImmunotherapy Treatment for Triple Negative Breast Cancer
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“CheckMate 067 [8] 3 Melanoma NR TC 1% 54 (92/171) 35 (41/117) 0.”
Immune checkpoint blockade in HIV
Gubser, C., Chiu, C. Y. H., Lewin, S. R., & Rasmussen, T. A. (2022) · EBioMedicine · doi:10.1016/j.ebiom.2022.103840 · Cited by 69
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The real-world impact of modern treatments on the survival of patients with metastatic melanoma
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Metadata
- Authors
- Wolchok, J. D., Chiarion-Sileni, V., Gonzalez, R., Rutkowski, P., Grob, J.-J., Cowey, C. L., Lao, C. D., Wagstaff, J., Schadendorf, D., Ferrucci, P. F., Smylie, M., Dummer, R., Hill, A., Hogg, D., Haanen, J., Carlino, M. S., Bechter, O., Maio, M., Marquez-Rodas, I., Guidoboni, M., McArthur, G., Lebbé, C., Ascierto, P. A., Long, G. V., Cebon, J., Sosman, J., Postow, M. A., Callahan, M. K., Walker, D., Rollin, L., Bhore, R., Hodi, F. S., & Larkin, J.
- Affiliations
- University of Siena (IT)
- From the Memorial Sloan Kettering Cancer Center and Weill Cornell Medical College, New York (J.D.W., M.A.P., M.K.C.); Oncology Institute of Veneto Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS), Padua (V.C.-S.), European Institute of Oncology, Milan (P.F.F.), Center for Immuno-Oncology, University Hospital of Siena, Istituto Toscano Tumori, Siena (M.M.), the Immunotherapy and Somatic Cell Therapy Unit, IRCCS Istituto Scientifico Romagnolo per lo Studio e la Cura dei Tumori, Meldola (M.G.),...
- ORCID
- Wolchok, Jedd D.
- Gonzalez, Rene
- Rutkowski, Piotr
- Grob, Jean-Jacques
- Cowey, C. Lance
- Wagstaff, John
- Schadendorf, Dirk
- Ferrucci, Pier F.
- Smylie, Michael
- Dummer, Reinhard
- Hogg, David
- Haanen, John
- Carlino, Matteo S.
- Bechter, Oliver
- Maio, Michele
- Guidoboni, Massimo
- McArthur, Grant
- Ascierto, Paolo A.
- Long, Georgina V.
- Cebon, Jonathan
- Sosman, Jeffrey
- Postow, Michael A.
- Callahan, Margaret K.
- Bhore, Rafia
- Hodi, F. Stephen
- Larkin, James
- Venue
- New England Journal of Medicine
- Publisher
- Massachusetts Medical Society
- Published
- 2017-10-05
- Volume
- 377
- Issue
- 14
- Pages
- 1345-1356
- ISSN
- 0028-4793 (ISSN-L)
- 1533-4406
- PMC
- PMC5706778
- OpenAlex
- W2753432434
- Semantic Scholar
- 23dbeed54cde655fb6a12697b02c9ff303515da7
- Cited by
- 5,357
- References
- 18
- Citations by year
- 2026: 159 · 2025: 282 · 2024: 569 · 2023: 705 · 2022: 746 · 2021: 947 · 2020: 900 · 2019: 578 · 2018: 428 · 2017: 37
- FWCI
- 234.31
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- New England Journal of Medicine (publishedVersion)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, other-oa)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Use Siena air (University of Siena) (submittedVersion, other-oa)
- Universitätsbibliographie, Universität Duisburg-Essen (submittedVersion)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, other-oa)
- Lirias (submittedVersion)
- Institutional Research Information System University of Ferrara (University of Ferrara) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion, other-oa)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- National Cancer Institute (P30CA008748)
- Topics
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Health Sciences › Medicine › Oncology › Cutaneous Melanoma Detection and Management
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Melanoma and MAPK Pathways
- Keywords
- advanced melanoma, nivolumab, ipilimumab, combination immunotherapy, immune checkpoint inhibitors, PD-1 inhibitors, CTLA-4 inhibitors, overall survival, progression-free survival, treatment-related adverse events, immune-related adverse events, PD-L1 expression, BRAF mutation, long-term follow-up
- MeSH terms
- Ipilimumab, Nivolumab, Adult, Aged, Antibodies, Monoclonal, Antineoplastic Combined Chemotherapy Protocols, Double-Blind Method, Humans, Melanoma, Middle Aged, Neoplasm Staging, Skin Neoplasms, Survival Rate, Disease-Free Survival, Kaplan-Meier Estimate
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