1,367
Views
1
CrossRef citations to date
0
Altmetric
Melanoma Immunotherapy SF – Reviews

Neoadjuvant immune checkpoint inhibitors in high-risk stage III melanoma

&
Article: 1971015 | Received 18 May 2021, Accepted 15 Aug 2021, Published online: 09 Dec 2021

References

  • Gershenwald JE, Scolyer RA. Melanoma staging: American Joint Committee on Cancer (AJCC) 8th edition and beyond. Ann Surg Oncol. 2018;25(8):2105–2110.
  • Creagan ET, Dalton RJ, Ahmann DL, Jung SH, Morton RF, Langdon RM Jr, Kugler J, Rodrigue LJ. Randomized, surgical adjuvant clinical trial of recombinant interferon alfa-2a in selected patients with malignant melanoma. J Clin Oncol. 1995;2776–11. doi:https://doi.org/10.1200/JCO.1995.13.11.2776
  • Ascierto PA, Gogas HJ, Grob JJ, Algarra SM, Mohr P, Hansson J, Hauschild A. Adjuvant interferon alfa in malignant melanoma: an interdisciplinary and multinational expert review. Crit Rev Oncol Hematol. 2013;85(2):149–61. doi:https://doi.org/10.1016/j.critrevonc.2012.07.004.
  • Kirkwood JM, Manola J, Ibrahim J, Sondak V, Ernstoff MS. A pooled analysis of eastern cooperative oncology group and intergroup trials of adjuvant high-dose interferon for melanoma. Cil Cancer Res. 2004;10(5):1670–77. doi:https://doi.org/10.1158/1078-0432.CCR-1103-3.
  • Malczewski A, Marshall A, Payne MJ, Mao L, Bafaloukos D, Si L, Pectasides D, Fountzilas G, Guo J, Gogas H, et al. Intravenous high‐dose interferon with or without maintenance treatment in melanoma at high risk of recurrence: meta‐analysis of three trials. Cancer Med. 2016 Jan;5(1):17–23.
  • Ascierto PA, Del Vecchio M, Mandalá M, Gogas H, Arance AM, Dalle S, Cowey CL, Schenker M, Grob -J-J, Chiarion-Sileni V, et al. Adjuvant nivolumab versus ipilimumab in resected stage IIIB-C and stage IV melanoma (CheckMate 238): 4-year results from a multicentre, double-blind, randomised, controlled, phase 3 trial. Lancet Oncol. 2020;21(11):1465–77. doi:https://doi.org/10.1016/S1470-2045(20)30494-0.
  • Eggermont AMM, Blank CU, Mandala M, Long GV, Atkinson VG, Dalle S, Haydon A, Lichinitser M, Khattak A, Carlino MS, et al. Prognostic and predictive value of AJCC-8 staging in the phase III EORTC1325/KEYNOTE-054 trial of pembrolizumab vs placebo in resected high-risk stage III melanoma. Eur J Cancer. 2019;116:148–57. doi:https://doi.org/10.1016/j.ejca.2019.05.020.
  • Eggermont AM, Chiarion-Sileni V, Grob JJ, Dummer R, Wolchok JD, Schmidt H, Hamid O, Robert C, Ascierto PA, Richards JM, et al. Adjuvant ipilimumab versus placebo after complete resection of high-risk stage III melanoma (EORTC 18071): a randomised, double-blind, phase 3 trial. Lancet Oncol. 2015;16(5):522–30. doi:https://doi.org/10.1016/S1470-2045(15)70122-1.
  • Owen CN, Shoushtari AN, Chauhan D, Palmieri DJ, Lee B, Rohaan MW, Mangana J, Atkinson V, Zaman F, Young A, et al. Management of early melanoma recurrence despite adjuvant anti-PD-1 antibody therapy. Ann Oncol. 2020;31(8):1075–82. doi:https://doi.org/10.1016/j.annonc.2020.04.471.
  • Cortazar P, Zhang L, Untch M, Mehta K, Costantino JP, Wolmark N, Bonnefoi H, Cameron D, Gianni L, Valagussa P, et al. Pathological complete response and long-term clinical benefit in breast cancer: the CTNeoBC pooled analysis. Lancet. 2019;384(9938):164–72. doi:https://doi.org/10.1016/S0140-6736(13)62422-8.
  • Amaria RN, Menzies AM, Burton EM, Scolyer RA, Tetzlaff MT, Antdbacka R, Ariyan C, Bassett R, Carter B, Daud A, et al. Neoadjuvant systemic therapy in melanoma: recommendations of the International Neoadjuvant Melanoma Consortium. Lancet Oncol. 2019;20(7):e378–89. doi:https://doi.org/10.1016/S1470-2045(19)30332-8.
  • Lui VK, Karpuchas J, Dent PB, McCulloch PB, Blajchman MA. Cellular immunocompetence in melanoma: effect of extent of disease and immunotherapy. Br J Cancer. 1975;32(3):323–30. doi:https://doi.org/10.1038/bjc.1975.230.
  • Amaria RN, Reddy SM, Tawbi HA, Davies MA, Ross MI, Glitza IC, Cormier JN, Lewis C, Hwu W-J, Hanna E, et al. Neoadjuvant immune checkpoint blockade in high-risk resectable melanoma. Nat Med. 2018;24(11):1649–54. doi:https://doi.org/10.1038/s41591-018-0197-1.
  • Amaria RN, Reddy SM, Tawbi HA, Davies MA, Ross MI, Glitza IC, Cormier JN, Lewis C, Hwu WJ, Hanna E, et al. Publisher correction: neoadjuvant immune checkpoint blockade in high-risk resectable melanoma. Nat Med. 2018;24(12):1942. doi:https://doi.org/10.1038/s41591-018-0252-y.
  • Polak ME, Borthwick NJ, Gabriel FG, Johnson P, Higgins B, Hurren J, McCormick D, Jager MJ, Cree IA. Mechanisms of local immunosuppression in cutaneous melanoma. Br J Cancer. 2007;96(12):1879–87. doi:https://doi.org/10.1038/sj.bjc.6603763.
  • Rozeman EA, Menzies AM, Van Akkooi ACJ, Adhikari C, Bierman C, van de Wiel BA, Scolyer RA, Krijgsman O, Sikorska K, Eriksson H, et al. Identification of the optimal combination dosing schedule of neoadjuvant ipilimumab plus nivolumab in macroscopic stage III melanoma (OpACIN-neo): a multicentre, phase 2, randomised, controlled trial. Lancet Oncol. 2019;20(7):948–60. doi:https://doi.org/10.1016/S1470-2045(19)30151-2.
  • Rozeman EA, Hoefsmit EP, Reijers ILM, Saw RPM, Versluis JM, Krijgsman O, Dimitriadis P, Sikorska K, van de Wiel BA, Eriksson H, et al. Survival and biomarker analyses from the OpACIN-neo and OpACIN neoadjuvant immunotherapy trials in stage III melanoma. Nat Med. 2021;27(2):256–63. doi:https://doi.org/10.1038/s41591-020-01211-7.
  • Hodi FS, O’Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010;363(8):711–723. doi:https://doi.org/10.1056/NEJMoa1003466.
  • Eggermont AM, Chiarion-Sileni V, Grob JJ, Dummer R, Wolchok JD, Schmidt H, Hamid O, Robert C, Ascierto PA, Richards JM, et al. Prolonged survival in stage III melanoma with Ipilimumab adjuvant therapy. Med N Engl J. 2016;375(19):1845–55. Erratum in: N Engl J Med. 2018., p. 379(22):2185. doi:https://doi.org/10.1056/NEJMoa1611299.
  • Tarhini AA, Edington H, Butterfield LH, Lin Y, Shuai Y, Tawbi H, Sander C, Yin Y, Holtzman M, Johnson J, et al. Immune monitoring of the circulation and the tumor microenvironment in patients with regionally advanced melanoma receiving neoadjuvant ipilimumab. PLoS One. 2014;9(2):e87705. doi:https://doi.org/10.1371/journal.pone.0087705.
  • Tarhini A, Lin Y, Lin H, Rahman Z, Vallabhaneni P, Mendiratta P, Pingpank JF, Holtzman MP, Yusko EC, Rytlewski JA, et al. Neoadjuvant ipilimumab (3 mg/kg or 10 mg/kg) and high dose IFN-α2b in locally/regionally advanced melanoma: safety, efficacy and impact on T-cell repertoire. J Immunother Cancer. 2018;6(1):112. doi:https://doi.org/10.1186/s40425-018-0428-5.
  • Postow MA, Callahan MK, Wolchok JD. Immune checkpoint blockade in cancer therapy. J Clin Oncol. 2015;33(17):1974‐1982. doi:https://doi.org/10.1200/JCO.2014.59.4358.
  • Schachter J, Ribas A, Long GV, Arance A, Grob -J-J, Mortier L, Daud A, Carlino MS, McNeil C, Lotem M, et al. Pembrolizumab versus ipilimumab for advanced melanoma: final overall survival results of a multicentre, randomised, open‐label phase 3 study (KEYNOTE‐006). Lancet. 2017;390(10105):1853‐1862. doi:https://doi.org/10.1016/S0140-6736(17)31601-X.
  • Hodi FS, Chiarion‐Sileni V, Gonzalez R, Grob -J-J, Rutkowski P, Cowey CL, Lao CD, Schadendorf D, Wagstaff J, Dummer R, et al. Nivolumab plus ipilimumab or nivolumab alone versus ipilimumab alone in advanced melanoma (CheckMate 067): 4‐year outcomes of a multicentre, randomised, phase 3 trial. Lancet Oncol. 2018;19(11):1480–1492. doi:https://doi.org/10.1016/S1470-2045(18)30700-9.
  • Huang AC, Orlowski RJ, Xu X, Mick R, George SM, Yan PK, Manne S, Kraya AA, Wubbenhorst B, Dorfman L, et al. A single dose of neoadjuvant PD-1 blockade predicts clinical outcomes in resectable melanoma. Nat Med. 2019;25(3):454–61. doi:https://doi.org/10.1038/s41591-019-0357-y.
  • Huang AC, Xu X, Orlowski RJ, Sangeeth MG, Chilukuri L, Kozlov A, Carberry M, Giles L, McGettigan S, Kreider K, et al. Safety, activity, and biomarkers for neoadjuvant anti-PD-1 therapy in melanoma. Abstract CT181. Clin Trials. 2018;2018:78.
  • Eggermont AMM, Blank CU, Mandala M, Long GV, Atkinson V, Dalle S, Haydon A, Lichinitser M, Khattak A, Carlino MS, et al. Adjuvant pembrolizumab versus placebo in resected stage III melanoma. N Engl J Med. 2018;378(19):1789–801. doi:https://doi.org/10.1056/NEJMoa1802357.
  • Blank CU, Versluis JM, Reijers ILM, Sikorska K, van Houdt WJ, van Thienen JV, Adriaansz S, Mallo HA, Van Tinteren H, van de Wiel BA, et al. 3-years relapse-free survival (RFS), overall survival (OS) and long-term toxicity of (neo)adjuvant Ipilimumab (IPI) + Nivolumab (NIVO) in macroscopic stage III melanoma (OPACIN TRIAL). Ann Oncol. 2019;30(Suppl. 5):v533–v563. doi:https://doi.org/10.1093/annonc/mdz255.003.
  • Lebbé C, Meyer N, Mortier L, Marquez-Rodas I, Robert C, Rutkowski P, Menzies AM, Eigentler T, Ascierto PA, Smylie M, et al. Two dosing regimens of nivolumab plus ipilimumab for advanced melanoma: 3-year results of CheckMate 511. ASCO. Presentation number 9516; 2021.
  • Long GV, Schadendorf D, Del Vecchio M, Larkin J, Atkinson V, Schenker M, Pigozzo J, Gogas HJ, Dalle S, Meyer N, et al. Adjuvant therapy with nivolumab (NIVO) combined with ipilimumab (IPI) vs NIVO alone in patients (pts) with resected stage IIIB-D/IV melanoma (CheckMate 915). AACR. Abstract CT004; 2021.
  • Schermers B, Franke V, Rozeman EA, van de Wiel BA, Bruining A, Wouters MW, van Houdt WJ, ten Haken B, Muller SH, Bierman C, et al. Surgical removal of the index node marked using magnetic seed localization to assess response to neoadjuvant immunotherapy in patients with stage III melanoma. Br J Surg. 2019;106(5):519–22. doi:https://doi.org/10.1002/bjs.11168.
  • Blank CU, Reijers ILM, Pennington T, Versluis JM, Saw RP, Rozeman EA, Kapiteijn E, Van Der Veldt AAM, Suijkerbuijk K, Hospers G, et al. First safety and efficacy results of PRADO: a phase II study of personalized response-driven surgery and adjuvant therapy after neoadjuvant ipilimumab (IPI) and nivolumab (NIVO) in resectable stage III melanoma. J Clin Oncol. 2020;38(15_suppl):10002–10002. s.l.: Clinical trial information: NCT02977052. doi:https://doi.org/10.1200/JCO.2020.38.15_suppl.10002.
  • Van Den Heuvel NMJ, Reijers ILM, Versluis JM, Rozeman AE, Jóźwiak K, Blommers KH, Saw RPM, Suijkerbuijk KPM, Kapiteijn E, Van der Veldt AAM, et al. 1085P-health-related quality of life in stage III melanoma patients treated. Ann Oncol. 2020.  31:S737. Clinical trial information OpACIN-neo/PRADO extension cohort NCT02977052.
  • Woo SR, Turnis ME, Goldberg MG, Bankoti J, Selby M, Nirschl CJ, Bettini ML, Gravano DM, Vogel P, Liu CL, et al. Immune inhibitory molecules LAG-3 and PD-1 synergistically regulate T-cell function to promote tumoral immune escape. Cancer Res. 2012;72:917–927.
  • Anderson AC, Joller N, Kuchrooet VK. Lag-3, tim-3, and TIGIT: co-inhibitory receptors with specialized functions in immune regulation. Immunity. 2016;44(5):989–1004. doi:https://doi.org/10.1016/j.immuni.2016.05.001.
  • Ascierto PA, Melero I, Bhatia S,Bono P, Sanborn RE, Lipson EJ, Callahan MK, Gajewski T, Gomez-Roca CA, Hodi FS, et al. Initial efficacy of anti-lymphocyte activation gene-3 (Anti–LAG-3; BMS986016) in combination with nivolumab (Nivo) in pts with melanoma (MEL) previously treated with anti–PD-1/PD-L1 therapy. J Clin Oncol. 2017;35(15_suppl):9520. doi:https://doi.org/10.1200/JCO.2017.35.15_suppl.9520.
  • Ascierto PA, Bono P, Bhatia S,Melero I, NyakasI MS, Svane M, Larkin J, Gomez-Roca C, Schadendorf D, Dummer R, et al. Efficacy of BMS-986016, a monoclonal antibody that targets lymphocyte activation gene-3 (LAG-3), in combination with nivolumab in pts with melanoma who progressed during prior anti–PD-1/PD-L1 therapy in all-comer and biomarker-enriched populations. ESMO, Abstract LBA18; 2017.
  • Amaria RN, Postow M, Tetzlaff MT,Ross MI, Glitza IC, McQuade JL, Wong MKK, Gershenwald JE, Goepfert R, Keung EZY, et al. Neoadjuvant AND adjuvant nivolumab with anti-lag3 antibody relatlimab for patients with resectable clinical stage III melanoma. ASCO; 2021.
  • Tronnier M, Mitteldorf C. Treating advanced melanoma: current insights and opportunities. Cancer Manag Res. 2014;6:349–56. doi:https://doi.org/10.2147/CMAR.S49494.
  • Parato KA, Senger D, Forsyth PA, Bell JC. Recent progress in the battle between oncolytic viruses and tumours. Nat Rev Cancer. 2005;5(12):965–76. 26. doi:https://doi.org/10.1038/nrc1750.
  • Forbes NE, Krishnan R, Diallo JS. Pharmacological modulation of antitumor immunity induced by oncolytic viruses. Front Oncol. 2014;4(191):27. doi:https://doi.org/10.3389/fonc.2014.00191.
  • Russell SJ, Peng KW, Bell JC. Oncolytic virotherapy. Nat Biotechnol. 2012;30(7):658–70. doi:https://doi.org/10.1038/nbt.2287.
  • Andtbacka RH, Kaufman HL, Collichio F, Amatruda T, Senzer N, Chesney J, Delman KA, Spitler LE, Puzanov I, Agarwala SS,et al. Talimogene laherparepvec improves durable response. Clin Oncol. 2015;33(25):2780–88.
  • Dummer R, Gyorki D, Hyngstrom J,Berger AC, Conry RM, Demidov LV, Sharma A, Treichel S, Faries MB, Ross MI. Improved Recurrence-Free Survival (RFS) from a randomized phase 2 study of Neoadjuvant (Neo) Talimogene Laherparepvec (T-VEC) Plus Surgery (Surg) vs Surg for resectable stage IIIB-IVM1a Melanoma (MEL). Presented At: The 16th International Congress of the Society for Melanoma Research. Salt Lake City, UT-2019.
  • Dummer R, Gyorki D, Hyngstrom J, Berger A, Conry R, Demidov L, Chan E, Radcliffe H-S, Faries M, Ross M, et al. 3- year results of the phase 2 randomized trial for Talimogene Laherparepvec (T-VEC) Neoadjuvant treatment plus surgery vs Surgery in patients with resectable stage IIIB-IVM1a Melanoma. J Immunother Cancer. 2020. doi:https://doi.org/10.1136/jitc-2020-SITC2020.0432.
  • Davar D, Karunamurthy A, Hartman D,De Blasio R, Chauvin JM, Ding Q, Pagliano O, Rose A, Kirkwood J and Zarour H. Phase II trial of Neoadjuvant Nivolumab (Nivo) and Intra-Tumoral (it) CMP-001 in high-risk resectable melanoma (Neo-C-Nivo): preliminary results. Presented At SITC 2019. J ImmunoTher Cancer. 2020;8.
  • Davar D, Karunamurthy A, Hartman D, DeBlasio R, Chauvin J-M, Ding Q, Pagliano O, Rose A, Kirkwood J, Zarour H, et al. Phase II trial of Neoadjuvant Nivolumab (Nivo) and intra-tumoral (it) CMP-001 in high-risk resectable melanoma (Neo-C-Nivo): final results. J Immunother Cancer. 2020;8(Suppl 3):A330–A330. doi:https://doi.org/10.1136/jitc-2020-SITC2020.0303.
  • Menzies AM, Amaria RN, Rozeman EA, Huang AC, Tetzlaff MT, van de Wiel BA, Lo S, Tarhini AA, Burton EM, Pennington TE, et al. Pathological response and survival with neoadjuvant therapy in melanoma: a pooled analysis from the International Neoadjuvant Melanoma Consortium. Nat Med. 2021;27(2):301–09. doi:https://doi.org/10.1038/s41591-020-01188-3.
  • Schadendorf D, Wolchok JD, Hodi FS, Chiarion-Sileni V, Gonzalez R, Rutkowski P, Grob -J-J, Cowey CL, Lao CD, Chesney J, et al. Efficacy and safety outcomes in patients with advanced melanoma who discontinued treatment with nivolumab and ipilimumab because of adverse events: a pooled analysis of randomized phase II and III trials. J Clin Oncol. 2017;35(34):3807–14. doi:https://doi.org/10.1200/JCO.2017.73.2289.
  • Ugurel S, Röhmel J, Ascierto PA, Becker JC, Flaherty KT, Grob JJ, Hauschild A, Larkin J, Livingstone E, Long GV, et al. Survival of patients with advanced metastatic melanoma: the impact of MAP kinase pathway inhibition and immune checkpoint inhibition - update 2019. Eur J Cancer. 2020;130:126–38. doi:https://doi.org/10.1016/j.ejca.2020.02.021.
  • Moschos SJ, Edington HD, Land SR, Rao UN, Jukic D, Shipe-Spotloe J, Kirkwood JM. Neoadjuvant treatment of regional stage IIIB melanoma with high-dose interferon alfa-2b induces objective tumor regression in association with modulation of tumor infiltrating host cellular immune responses. Oncol J Clin. 2006;24(19):3164–71. doi:https://doi.org/10.1200/JCO.2005.05.2498.
  • Seymour L, Bogaerts J, Perrone A, Ford R, Schwartz LH, Mandrekar S, Lin NU, Litière S, Dancey J, et al; RECIST working group. iRECIST: guidelines for response criteria for use in trials testing immunotherapeutics. Lancet Oncol. 2019 May; 20(5): e242. Erratum in: Lancet Oncol. PMID: 28271869; PMCID: PMC5648544. 2017, p. 18(3):e143-e152.
  • Trebeschi S, Drago SG, Birkbak NJ, Kurilova I, Cǎlin AM, Delli Pizzi A, Lalezari F, Lambregts DMJ, Rohaan MW, Parmar C, et al. Predicting response to cancer immunotherapy using noninvasive radiomic biomarkers. Ann Oncol. 2019;30(6):998–1004. doi:https://doi.org/10.1093/annonc/mdz108.
  • Dummer R, Brase JC, Garrett J, Campbell CD, Gasal E, Squires M, Gusenleitner D, Santinami M, Atkinson V, Mandalà M, et al. Adjuvant dabrafenib plus trametinib versus placebo in patients with resected, BRAFV600-mutant, stage III melanoma (COMBI-AD): exploratory biomarker analyses from a randomised, phase 3 trial. Lancet Oncol. 2020;21(3):358–72. doi:https://doi.org/10.1016/S1470-2045(20)30062-0.