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Immune-related adverse events and disease outcomes after the third dose of SARS-CoV-2 mRNA-BNT162b2 vaccine in cancer patients receiving immune checkpoint inhibitors

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Abstract

Background

The clinical implications of the third dose of coronavirus disease 2019 (COVID-19) vaccines in patients receiving immune checkpoint inhibitors are currently unknown. We performed a prospective analysis of the Vax-On-Third study to investigate the effects of antibody response on immune-related adverse events (irAEs) and disease outcomes.

Methods

Recipients of the booster dose of SARS-CoV-2 mRNA-BNT162b2 vaccine who had received at least one course of an anti-PD-1/PD-L1 treatment before vaccination for an advanced solid malignancy were eligible.

Results

The current analysis included 56 patients with metastatic disease (median age: 66 years; male: 71%), most of whom had a lung cancer diagnosis and were being treated with pembrolizumab- or nivolumab-based regimens. The optimal cut-point antibody titer of 486 BAU/mL allowed a dichotomization of recipients into low-responders (Low-R, < 486 BAU/mL) or high-responders (High-R, ≥ 486 BAU/mL). After a median follow-up time of 226 days, 21.4% of patients experienced moderate to severe irAEs without any recrudescence of immune toxicities preceding the booster dose. The frequencies of irAE before and after the third dose did not differ, but an increase in the cumulative incidence of immuno-related thyroiditis was observed within the High-R subgroup. On multivariate analysis, an enhanced humoral response correlated with a better outcome in terms of durable clinical benefit, which resulted in a significant reduction in the risk of disease control loss but not mortality.

Conclusions

Our findings would strengthen the recommendation not to change anti-PD-1/PD-L1 treatment plans based on current or future immunization schedules, implying that all these patients should be closely monitored.

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Data availability

The datasets generated and analysed during the current study are available from the corresponding author on reasonable request.

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Authors and Affiliations

  1. Medical Oncology Unit, Department of Oncology and Hematology, Central Hospital of Belcolle, Strada Sammartinese snc, 01100, Viterbo, Italy

    Fabrizio Nelli, Agnese Fabbri, Antonella Virtuoso, Julio Rodrigo Giron Berrios, Eleonora Marrucci, Cristina Fiore, Marta Schirripa, Carlo Signorelli, Mario Giovanni Chilelli, Francesca Primi & Enzo Maria Ruggeri

  2. Biostatistics Unit, Fondazione Policlinico Universitario A. Gemelli, IRCCS, Rome, Italy

    Diana Giannarelli

  3. Microbiology and Virology Unit, Department of Oncology and Hematology, Central Hospital of Belcolle, Viterbo, Italy

    Valentina Panichi, Giuseppe Topini & Maria Assunta Silvestri

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Contributions

FN and EMR designed the study and wrote the manuscript. DG performed the statistical analysis. AF, JRGB, AV, EM, CF, MS, CS, MGC, and FP enrolled the patients, collected clinical and laboratory data and setup the database. VP, GT, and MAS performed serological testing, and contributed to the interpretation of the data. All authors discussed the results and critically revised the manuscript. All authors read and approved the final manuscript.

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Correspondence to Fabrizio Nelli.

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This study was approved by the referring Ethics Committee (Comitato Etico Lazio1, Rome, Italy; protocol number: 1407/CE Lazio1). All patients were required to provide written informed consent before participating in this study. All procedures performed in this study involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

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Nelli, F., Giannarelli, D., Fabbri, A. et al. Immune-related adverse events and disease outcomes after the third dose of SARS-CoV-2 mRNA-BNT162b2 vaccine in cancer patients receiving immune checkpoint inhibitors. Cancer Immunol Immunother 72, 3217–3228 (2023). https://doi.org/10.1007/s00262-023-03489-1

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