Current status and future directions of the immune checkpoint inhibitors ipilimumab, pembrolizumab, and nivolumab in oncology

Annals of Pharmacotherapy

Volumn 49, Issue 8, 2015, Pages 907-937

  Barbee, Meagan S ^a   Ogunniyi, Adebayo ^a   Horvat, Troy Z ^a   Dang, Thu Oanh ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

CTLA 4; Immune checkpoint inhibitor; Ipilimumab; Nivolumab; PD 1; Pembrolizumab

Indexed keywords

ANTIHISTAMINIC AGENT; ATROPINE; BUDESONIDE; CARBOPLATIN; CISPLATIN; CORTICOSTEROID; DACARBAZINE; DIPHENHYDRAMINE; DIPHENOXYLATE; DOCETAXEL; GEMCITABINE; HYDROXYZINE; IMMUNOSUPPRESSIVE AGENT; IPILIMUMAB; MONOCLONAL ANTIBODY; NIVOLUMAB; PACLITAXEL; PAZOPANIB; PEMBROLIZUMAB; PLACEBO; PLATINUM; PREDNISONE; SARGRAMOSTIM; STEROID; SUNITINIB; ANTINEOPLASTIC AGENT;

ABDOMINAL PAIN; ARTHRITIS; ARTICLE; BLEPHARITIS; CANCER CHEMOTHERAPY; CANCER COMBINATION CHEMOTHERAPY; CANCER PATIENT; CLINICAL PROTOCOL; CLINICAL TRIAL (TOPIC); COLITIS; CONJUNCTIVITIS; DATA EXTRACTION; DRUG EFFICACY; DRUG ERUPTION; DRUG PACKAGING; DRUG SAFETY; DRUG TOLERABILITY; EYE MELANOMA; FATIGUE; HUMAN; KIDNEY FAILURE; MEDLINE; MELANOMA; METASTATIC MELANOMA; MONOTHERAPY; MULTICENTER STUDY (TOPIC); NEOPLASM; NON SMALL CELL LUNG CANCER; ONCOLOGY; OVERALL SURVIVAL; PERICARDITIS; PHARMACODYNAMICS; PHASE 3 CLINICAL TRIAL (TOPIC); PNEUMONIA; PRACTICE GUIDELINE; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PRURITUS; RANDOMIZED CONTROLLED TRIAL (TOPIC); RECURRENCE FREE SURVIVAL; SCLERITIS; STEROID THERAPY; SYSTEMATIC REVIEW; TREATMENT DURATION; TREATMENT RESPONSE; TUMOR MICROENVIRONMENT; UVEA MELANOMA; CELL CYCLE CHECKPOINT; DRUG EFFECTS; IMMUNOLOGY; NEOPLASMS; PATHOLOGY;

ANTIBODIES, MONOCLONAL; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC AGENTS; CELL CYCLE CHECKPOINTS; HUMANS; NEOPLASMS;

EID: 84943143291     PISSN: 10600280     EISSN: 15426270     Source Type: Journal    
DOI: 10.1177/1060028015586218     Document Type: Article

References (91)

1. Schreiber RD, Old LJ, Smyth MJ, et al. Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science. 2011;331:1565-1570.
2. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12:252-264.
3. Chabner BA, Barnes J, Neal J, et al. Targeted therapies: tyrosine kinase inhibitors, monoclonal antibodies, and cytokines. In: Brunton LL, Chabner BA, Knollmann BC. eds. Goodman & Gilman’s The Pharmacological Basis of Therapeutics. 12th ed. New York, NY: McGraw-Hill; 2011:chap 62. http://accessmedicine.mhmedical.com/content.aspx?bookid=374& Sectionid=41266274. Accessed December 8, 2014.
4. Ipilimumab (YervoyR) [prescribing information]. Princeton, NJ: Bristol-Myers Squibb Company; 2013.
5. US National Institutes of Health Clinical Trial Registry. https://clinicaltrials.gov/. Accessed December 30, 2014.
6. Hodi FS, O’Day SJ, McDermott DF, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010;363:711-723.
7. Robert C, Schadendorf D, Messina M, et al. Efficacy and safety of retreatment with ipilimumab in patients with pretreated advanced melanoma who progressed after initially achieving disease control. Clin Cancer Res. 2013;19:2232-2239.
8. Robert C, Thomas L, Bondarenko I, et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med. 2011;364:2517-2526.
9. Maio M, Grob J-J, Aamdal S, et al. Five-year survival rates for treatment-naive patients with advanced melanoma who received ipilimumab plus dacarbazine in a phase iii trial. J Clin Oncol. 2015;33:1191-1196.
10. Attia P, Phan GQ, Maker AV, et al. Autoimmunity correlates with tumor regression in patients with metastatic melanoma treated with anti-cytotoxic t-lymphocyte antigen-4. J Clin Oncol. 2005;23:6043-6053.
11. Maker AV, Phan GQ, Attia P, et al. Tumor regression and autoimmunity in patients treated with cytotoxic t lymphocyteassociated antigen 4 blockade and interleukin 2: a phase I/II study. Ann Surg Oncol. 2005;12:1005-1016.
12. Weber JS, O’Day S, Urba W, et al. Phase I/II study of ipilimumab for patients with metastatic melanoma. J Clin Oncol. 2008;26:5950-5956.
13. Weber JS, Thompson JA, Hamid O, et al. A randomized, doubleblind, placebo-controlled, phase ii study comparing the tolerability and efficacy of ipilimumab administered with or without prophylactic budesonide in patients with unresectable stage III or IV melanoma. Clin Cancer Res. 2009;15:5591-5598.
14. Wolchok JD, Neyns B, Linette G, et al. Ipilimumab monotherapy in patients with pretreated advanced melanoma: a randomised, double-blind, multicentre, phase 2, dose-ranging study. Lancet Oncol. 2010;11:155-164.
15. O’Day SJ, Maio M, Chiarion-Sileni V, et al. Efficacy and safety of ipilimumab monotherapy in patients with pretreated advanced melanoma: a multicenter single-arm phase II study. Ann Oncol. 2010;21:1712-1717.
16. Hersh EM, O’Day SJ, Powderly J, et al. A phase II multicenter study of ipilimumab with or without dacarbazine in chemotherapy-naive patients with advanced melanoma. Invest New Drugs. 2011;29:489-498.
17. Hodi SF, Lee S, McDermott DF, et al. Sargramostim plus ipilimumab vs ipilimumab alone for treatment of metastatic melanoma: a randomized clinical trial. JAMA. 2014;312: 1744-1753.
18. Schadendorf D, Hodi FS, Robert C, et al. Pooled analysis of long-term survival data from phase II and phase III trials of ipilimumab in unresectable or metastatic melanoma [published online February 9, 2015]. J Clin Oncol. doi:10.1200/JCO.2014.56.2736.
19. Coit DG, Thompson JA, Andtbacka R, et al. NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines): melanoma version 3. 2015. http://www.nccn.org/professionals/physician_gls/pdf/melanoma.pdf. Accessed March 29, 2015.
20. Eggermont AM, Chiarion-Sileni V, Grob JJ, et al. Ipilimumab versus placebo after complete resection of stage III melanoma: initial efficacy and safety results from the EORTC 18071 phase III trial [published online March 31, 2015]. J Clin Oncol. doi:10.1016/S1470-2045(15)70122-1.
21. Sarnaik AA, Yu B, Yu D, et al. Extended dose ipilimumab with a peptide vaccine: immune correlates associated with clinical benefit in patients with resected high-risk stage IIIc/ IV melanoma. Clin Cancer Res. 2010;17:896-906.
22. Margolin K, Ernstoff MS, Hamid O, et al. Ipilimumab in patients with melanoma and brain metastases: an open-label, phase 2 trial. Lancet Oncol. 2012;13:459-645.
23. Rodriguez JMP, de Olza MO, Codes M, et al. Phase II study evaluating ipilimumab as a single agent in the firstline treatment of adult patients with metastatic uveal melanoma (MUM): the GEM-1 trial. J Clin Oncol. 2014;32(suppl 5):abstract 9033.
24. Kwon ED, Drake CG, Scher HI, et al. Ipilimumab versus placebo after radiotherapy in patients with metastatic castrationresistant prostate cancer that had progressed after docetaxel chemotherapy (CA184-043): a multicentre, randomised, double-blind, phase 3 trial. Lancet Oncol. 2014;15:700-712.
25. Subudhi SK, Aparicio A, Zurita AJ, et al. Finite androgen deprivation therapy plus ipilimumab in men with hormonenaive metastatic prostate cancer. Ann Oncol. 2014;25(suppl 4):iv361-iv372(abstract 1053PD).
26. Slovin SF, Higano CS, Hamid O, et al. Ipilimumab alone or in combination with radiotherapy in metastatic castration-resistant prostate cancer: results from an open-label, multicenter phase I/II study. Ann Oncol. 2013;24:1813-1821.
27. Madan RA, Mohebtash M, Arlen PM, et al. Ipilimumab and a poxviral vaccine targeting prostate-specific antigen in metastatic castration-resistant prostate cancer: a phase 1 doseescalation trial. Lancet Oncol. 2012;13:501-508.
28. Fong L, Kwek SS, O’Brien S, et al. Potentiating endogenous antitumor immunity to prostate cancer through combination immunotherapy with CTLA4 blockade and GM-CSF. Cancer Res. 2009;69:609-615.
29. Lynch TJ, Bondarenko I, Luft A, 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;30:2046-2054.
30. Reck M, Bondarenko I, Luft A, 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;24:75-83.
31. Yang JC, Hughes M, Kammula U, et al. Ipilimumab (anti- CTLA4 antibody) causes regression of metastatic renal cell cancer associated with enteritis and hypophysitis. J Immunother. 2007;30:825-830.
32. Royal RE, Levy C, Turner K, et al. Phase 2 trial of single agent ipilimumab (anti-CTLA-4) for locally advanced or metastatic pancreatic adenocarcinoma. J Immunother. 2010;33:828-833.
33. Ansell SM, Hurvitz SA, Koenig PA, et al. Phase I study of ipilimumab, an anti–CTLA-4 monoclonal antibody, in patients with relapsed and refractory B-cell non–Hodgkin lymphoma. Clin Cancer Res. 2009;15:6446-6453.
34. Davids MS, Kim HT, Costello CL, et al. A multicenter phase I study of CTLA-4 blockade with ipilimimab for relapsed hematologic malignancies after allogeneic hematopoietic cell transplantation. Blood. 2014;124:abstr. 3964.
35. Bashey A, Medina B, Corringham S, et al. CTLA4 blockade with ipilimumab to treat relapse of malignancy after allogeneic hematopoietic cell transplantation. Blood. 2009;113:1581-1588.
36. Merchant MS, Baird K, Wexler LH, et al. Ipilimumab: first results of a phase I trial in pediatric patients with advanced solid tumors. J Clin Oncol. 2012;30(suppl):abstract 9545.
37. Pembrolizumab (KeytrudaR) [prescribing information]. Whitehouse Station, NJ: Merck Sharp & Dohme Corp; 2014.
38. Hamid O, Robert C, Daud A, et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med. 2013;369:134-144.
39. Daud AI, Hamid O, Ribas A, et al. Antitumor activity of the anti-PD-1 monoclonal antibody MK-3475 in melanoma (MEL): correlation of tumor PD-L1 expression with outcome. Cancer Res. 2014;74:abstract CT104.
40. Robert C, Ribas A, Wolchok JD, et al. Anti-programmeddeath- receptor-1 treatment with pembrolizumab in ipilimumab- refractory advanced melanoma: a randomised dose-comparison cohort of a phase 1 trial. Lancet. 2014;384:1109-1117.
41. Robert C, Joshua AM, Weber JS, et al. Pembrolizumab (Pembro; MK-3475) for advanced melanoma (MEL): randomized comparison of two dosing schedules. Ann Oncol. 2014;25:v1-v41(abstract LBA34).
42. Gandhi L, Balmanoukian A, Hui R, et al. MK-3475 (anti- PD-1 monoclonal antibody) for non-small cell lung cancer (NSCLC): antitumor activity and association with tumor PD-L1 expression (KEYNOTE-025). Cancer Res. 2014;74:abstract CT105.
43. Garon EB, Gandhi L, Rizvi N, et al. Antitumor activity of pembrolizumab (Pembro; MK-3475) and correlation with programmed death ligand 1 (PD-L1) expression in a pooled analysis of patients with advanced NSCLC. Ann Oncol. 2014;25:1-41(abstract LBA43).
44. Muro K, Bang Y, Shankaran V, et al. A phase Ib study of pembrolizumab (Pembro; MK-3475) in patients with advanced gastric cancer. Ann Oncol. 2014;25:v1-v41(abstract LBA15).
45. Moskowitz CH, Ribrag V, Michot JM, et al. PD-1 blockade with the monoclonal antibody pembrolizumab (MK-3475) in patients with classical Hodgkin lymphoma after brentuximab Vedotin failure: preliminary results from a phase 1b study (KEYNOTE-013). Blood. 2014;124(issue 1):abstract 290.
46. Plimack ER, Gupta S, Bellmunt J, et al. A phase Ib study of pembrolizumab (Pembro; MK-3475) in patients with advanced urothelial tract cancer. Ann Oncol. 2014;25:v1- v41(abstract LBA23).
47. Chow LQ, Burtness B, Weiss J, et al. A phase Ib study of pembrolizumab (Pembro; MK-3475) in patients with human papilloma virus (HPV)-positive and negative head and neck cancer. Ann Oncol. 2014;25(5):v1-v41(abstract LBA31).
48. Nivolumab (OpdivoR) [prescribing information]. Princeton, NJ: Bristol-Myers Squibb Company; 2015.
49. Weber JS, D’angelo SP, Minor D, et al. Nivolumab versus chemotherapy in patients with advanced melanoma who progressed after anti-CTLA-4 treatment (CheckMate037): a randomised, controlled, open-label phase 3 trial. Lancet Oncol. 2015;16:375-384.
50. Topalian S, Hodi FS, Brahmer JR, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med. 2012;366:2443-2454.
51. Topalian SL, Sznol M, McDermott DF, et al. Survival, durable tumor remission, and long-term safety in patients with advanced melanoma receiving nivolumab. J Clin Oncol. 2014;32:1020-1030.
52. Robert C, Long GV, Brady B, et al. Nivolumab in previously untreated melanoma without BRAF mutation [published online November 16, 2014]. N Engl J Med. doi:10.1056/NEJMoa1412082.
53. Rizvi NA, Mazieres J, Planchard D, et al. Activity and safety of nivolumab, an anti-PD-1 immune checkpoint inhibitor, for patients with advanced, refractory squamous non-small lung cancer (CheckMate 063): a phase 2, single-arm trial. Lancet Oncol. 2015;16:257-265.
54. Ettinger DS, Wood DE, Akerley W, et al. NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines): nonsmall cell lung cancer version 5. 2015. http://www.nccn.org/professionals/physician_gls/pdf/nscl.pdf. Accessed March 29, 2015.
55. Gettinger SN, Shepherd FA, Antonia SJ, et al. First-line nivolumab (anti-PD-1; BMS-936558, ONO-4538) monotherapy in advanced NSCLC: safety, efficacy, and correlation of outcomes with PD-L1 status. J Clin Oncol. 2014;32(suppl 5):abstract 8024.
56. Brahmer JR, Horn L, Gandhi L, et al. Nivolumab (anti-PD-1, BMS-936558, ONO-4538) in patients (pts) with advanced non-small-cell lung cancer (NSCLC): survival and clinical activity by subgroup analysis. J Clin Oncol. 2014;32(suppl 5):abstract 8112.
57. Gettinger S, Rizvi N, Chow LQ, et al. Nivolumab (anti-PD-1; BMS-936558, ONO-4538) in combination with platinumbased doublet chemotherapy (PT-CD) or erlotinib (ERL) in advanced non-small cell lung cancer (NSCLC). Ann Oncol. 2014;25:iv361-iv372(abstract 1054PD).
58. Hamanishi J, Mandai M, Ikeda T, et al. Efficacy and safety of anti-PD-1 antibody (nivolumab: BMS-936558, ONO- 4538) in patients with platinum-resistant ovarian cancer. J Clin Oncol. 2014;32(suppl 15):abstract 5511.
59. Motzer RJ, Rini BI, McDermott DF, et al. Nivolumab for metastatic renal cell carcinoma: results of a randomized phase II trial [published online December 1, 2014]. J Clin Oncol. doi: JCO.2014.59.0703.
60. Drake CG, McDermogg DF, Sznol M, et al. Survival, safety, and response duration results of nivolumab (anti- PD-1; BMX-936558, ONO-4358) in a phase I trial in patients with previously treated metastatic renal cell carcinoma (mRCC): long-term patient follow-up. J Clin Oncol. 2013;(suppl):abstract 4514.
61. Amin A, Plimack ER, Infante JR, et al. Nivolumab (anti-PD-1; BMS-936558, ONO-4538) in combination with sunitinib or pazopanib in patients (pts) with metastatic renal cell carcinoma (mRCC). Ann Oncol. 2014;25:iv361-iv372(abstract 1052PD).
62. Ansell SM, Lesokhin AM, Borrello I, et al. PD-1 blockade with nivolumab in relapsed or refractory Hodgkin’s lymphoma [published online December 6, 2014]. N Engl J Med. doi:10.1056/NEJMoa1411087.
63. Brahmer JR, Drake CG, Wollner I, et al. Phase I study of single-agent anti–programmed death-1 (MDX-1106) in refractory solid tumors: safety, clinical activity, pharmacodynamics, and immunologic correlates. J Clin Oncol. 2010;28: 3167-3175.
64. Curran MA, Montalvo W, Yagita H, Allison JP. PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc Natl Acad Sci U S A. 2010;107: 4275-4280.
65. Antonia SJ, Larkin J, Ascierto PA. Immuno-oncology combinations: a review of clinical experience and future prospects. Clin Cancer Res. 2014;20:6258-6268.
66. Wolchok JD, Kluger H, Callahan MK, et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med. 2013;369:122-133.
67. Sznol M, Kluger HM, Callahan MK, et al. Survival, response duration, and activity by BRAF mutation status of nivolumab (NIVO, anti-PD-1, BMS-936558, ONO-4538) an ipilimumab (IPI) concurrent therapy in advanced melanoma. J Clin OncoI. 2014;25:iv361-iv372(abstract LBA9003).
68. Hammers H, Plimack ER, Infante JR, et al. Phase I study of nivolumab in combination with ipilimumab in metastatic renal cell carcinoma. J Clin Oncol. 2014;25:iv361-iv372(abstract 1050O).
69. Antonia SJ, Gettinger SN, Chow LQM, et al. Nivolumab (anti- PD-1; BMS-936558; ONO-4538) an ipilimumab in first-line NSCLC: interim phase I results. J Clin OncoI. 2014;25:iv361- iv372(abstract 8023).
70. Tabrizi MA, Tseng C-ML, Roskos LK. Elimination mechanisms of therapeutic monoclonal antibodies. Drug Discov Today. 2006;11:81-88.
71. Huang SM, Zhao H, Lee JI, et al. Therapeutic protein-drug interactions and implications for drug development. Clin Pharmacol Ther. 2010;87:497-503.
72. Weber JS, Kahler KC, Hauschild A. Management of immunerelated adverse events and kinetics of response with ipilimumab. J Clin Oncol. 2012;30:2691-2697.
73. Weber JS, Dummer R, de Pril V, et al. Patterns of onset and resolution of immune-related adverse events of special interest with ipilimumab. Cancer. 2013;119:1675-1682.
74. Beck KE, Blansfield JA, Tran KQ, et al. Enterocolitis in patients with cancer after antibody blockade of cytotoxic T-lymphocyte-associated antigen 4. J Clin Oncol. 2006;24:2283-2289.
75. Horvat TZ, Adel NG, Dang TO, et al. Immune related adverse events (irAEs) and overall survival (OS) in patients (pts) with melanoma (mel) treated outside of a clinical trial with ipilimumab (ipi) at Memorial Sloan Kettering (MSK). Pigment Cell Melanoma Res. 2014;27:1200(abstract). doi:10.1111/pcmr.12317
76. Common Terminology Criteria for Adverse Events v4.0 (CTCAE). US Department of Health and Human Services, National Institutes of Health, National Cancer Institute. http://evs.nci.nih.gov/ftp1/CTCAE/CTCAE_4.03_2010-06-14_QuickReference:5x7.pdf. Accessed December 30, 2013.
77. Chin K, Ibrahim R, Berman D, et al. Treatment guidelines for the management of immune-related adverse events in patients treated with ipilimumab, and anti-CTLA4 therapy. Ann Oncol. 2008;19(suppl 8):vii244(abstract 787P).
78. Baden LR, Bensigner W, Angarone M, et al. NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines): prevention and treatment of cancer-related infections version 2. 2014. http://www.nccn.org/professionals/physician_gls/pdf/ infections.pdf. Accessed December 30, 2014.
79. Wolchok JD, Hoos A, O’Day S, et al. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin Cancer Res. 2009;15:7412-7420.
80. World Health Organization. WHO Handbook for Reporting Results of Cancer Treatment. Geneva, Switzerland: World Health Organization; 1979. Offset Publication No. 48.
81. Eisenhauer EA, Therasse P, Bogaerts J, et al. New response criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer. 2009;45:228-247.
82. Hodi FS, Ribas A, Daud A, et al. Evaluation of immunerelated response criteria (irRC) in patients (pts) with advanced melanoma (MEL) treated with the anti-PD-1 monoclonal antibody MK-3475. J Clin Oncol. 2014;32(suppl 5s):abstract 3006.
83. Lutzky J, Antonia SJ, Blake-Haskins A, et al. A phase 1 study of MEDI4736, an anti–PD-L1 antibody, in patients with advanced solid tumors. J Clin Oncol. 2014;32(suppl 5s):abstract 3001.
84. Hamid O, Schmidt H, Nissan A, et al. A prospective phase II exploring the association between tumor microenvironment biomarkers and clinical activity of ipilimumab in advanced melanoma. J Transl Med. 2011;9:204. doi:10.1186/1479-5876-9-204.
85. Snyder A, Makarov Merghout T, et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl J Med. 2014;371:2189-2199.
86. McDermott DF, Kluger H, Sznol M, et al. Long-term survival of ipilimumab-naive patients with advanced melanoma treated with nivolumab (anti-PD-L, BMS-936558, ONO- 4538). Ann Oncol. 2014;25(suppl 4):iv374-iv393(abstract 1088PD).
87. Grosso J, Horak CE, Inzunza D, et al. Association of tumor PD-L1 expression and immune biomarkers with clinical activity in patients with advanced solid tumors treated with nivolumab (anti-PD-1; BMS-936558; ONO-4538). Ann Oncol. 2014;25(suppl 4):iv374-iv393(abstract 1088PD).
88. Choueiri T, Fishman MN, Escudier B, et al. Immunomodulatory activity of nivolumab in previously treated and untreated metastatic renal cell carcinoma: biomarker-based results from a randomized clinical trial. Ann Oncol. 2014;25(suppl 4):iv361- iv372(abstract 1051PD).
89. Callahan MK, Horak CE, Curran MA, et al. Peripheral and tumor immune correlates in patients with advanced melanoma treated with combination nivolumab (anti-PD-1, BMS-936558, ONO-4538) and ipilimumab. J Clin Oncol. 2013;31(suppl 15):abstract 3003.
90. Berman D, Korman A, Peck R, Feltquate D, Lonberg N, Canetta R. The development of immunomodulatory monoclonal antibodies as a new therapeutic modality for cancer: the Bristol-Myers Squibb experience. Pharmacol Ther. 2015;148:132-153.
91. Page DB, Postow MA, Callahan MK, Allison JP, Wolchok JD. Immune modulation in cancer with antibodies. Annu Rev Med. 2014;65:185-202.