Lambros Tselikas, Sandrine Susini, Matthieu Texier, Andrey Yurchenko, Émilie Routier, Mona Amini‐Adlé, Edi Tihic, Séverine Mouraud, François‐Xavier Danlos, Samy Ammari, Thibault Raoult, Séverine Roy, Delphine Bredel, Siham Farhane, Lydie Cassard, Irma Molinaro, Alexander Eggermont, Jean-Charles Soria, Laurence Zitvogel, Christophe Massard, Angélo Paci, T De Baere, Jean‐Yves Scoazec, Nathalie Chaput, Sergey Nikolaev, Nicolas Meyer, Céleste Lebbé, Stephane Dalle, Caroline Robert, Aurélien Marabelle
Abstract Intravenous administration of anti-CTLA4 with anti-PD1 provides durable tumour responses but causes severe treatment-related adverse events in patients with cancer 1 . Intratumoural administration at lower doses but high local concentrations could enhance antitumour efficacy while minimizing systemic exposure and toxicity. Here we report the randomized multicentre phase 1b NIVIPIT trial (ClinicalTrials.gov: NCT02857569 ), which enrolled 61 patients with untreated metastatic melanoma, randomly assigned 2:1 to receive intravenous nivolumab (anti-PD1; 1 mg kg −1 ) combined with either intratumoural ipilimumab (anti-CTLA4; 0.3 mg kg −1 ) or intravenous ipilimumab (3 mg kg −1 ). The primary end-point was met with significantly lower incidence of grade 3 or 4 treatment-related adverse events at 6 months in the intratumoural versus intravenous arm (22.6% versus 57.1%), equivalent to anti-PD1 monotherapy. RECIST (response evaluation criteria in solid tumours) best objective response rate reached 65.7% for anti-CTLA4 injected lesions and 50% for uninjected lesions, confirming the relationship between intratumoural exposure to anti-CTLA4 and efficacy. Baseline tumour immune profiling revealed that protumoural activated regulatory T (T reg ) cells and M2 macrophages predict durable clinical benefit, regardless of the anti-CTLA4 administration route. A decrease in activated intratumoural T reg cells occurred only in patients who showed durable clinical benefit, who also presented high intratumoural Fcγ receptor (FcγR) expression. Our results provide a rationale for intratumoural anti-CTLA4 strategies in oligometastatic and early-stage cancers and indicate that high intratumoural activated T reg cell and FcγR + M2 macrophage numbers are prerequisites for efficacy of combined anti-CTLA4 and anti-PD1.