. 2022 Nov;10(11):e005732.

doi: 10.1136/jitc-2022-005732.

Immune checkpoint inhibitor therapy and outcomes from SARS-CoV-2 infection in patients with cancer: a joint analysis of OnCovid and ESMO-CoCARE registries

Alessio Cortellini^{1

2}, Gino M Dettorre³, Urania Dafni⁴, Juan Aguilar-Company^{5

6}, Luis Castelo-Branco^{7

8}, Matteo Lambertini^{9

10}, Spyridon Gennatas¹¹, Vasileios Angelis¹¹, Ailsa Sita-Lumsden¹², Jacobo Rogado¹³, Paolo Pedrazzoli^{14

15}, David Viñal¹⁶, Aleix Prat^{17

18}, Maura Rossi¹⁹, Rossana Berardi²⁰, Teresa Alonso-Gordoa²¹, Salvatore Grisanti²², Georgia Dimopoulou⁴, Paola Queirolo²³, Sylvain Pradervand²⁴, Alexia Bertuzzi²⁵, Mark Bower²⁶, Dirk Arnold²⁷, Ramon Salazar²⁸, Marco Tucci^{29

30}, Kevin J Harrington³¹, Francesca Mazzoni³², Uma Mukherjee³³, Zoi Tsourti³⁴, Olivier Michielin²⁴, Fanny Pommeret³⁵, Joan Brunet³⁶, Bruno Vincenzi², Giuseppe Tonini², Andrea Patriarca³⁷, Federica Biello³⁸, Marco Krengli³⁹, Josep Tabernero⁴⁰, George Pentheroudakis⁷, Alessandra Gennari³⁸, Solange Peters^{7

24}, Emanuela Romano^#⁴¹, David J Pinato^#^{42

38}

Affiliations

¹ Department of Surgery & Cancer, Hammersmith Hospital Campus, Imperial College London, London, UK alessiocortellini@gmail.com.
² Medical Oncology, Fondazione Policlinico Universitario Campus Bio-Medico, Via Alvaro del Portillo, 200 - 00128, Roma, Italy.
³ Department of Internal Medicine, Washington University School of Medicine, St. Louis, Missouri, USA.
⁴ Laboratory of Biostatistics, School of Health Sciences, National and Kapodistrian University of Athens, Athens, Greece.
⁵ Medical Oncology, Vall d'Hebron University Hospital and Institute of Oncology (VHIO), Barcelona, Spain.
⁶ Infectious Disease, Vall d'Hebron University Hospital, Barcelona, Spain.
⁷ Scientific and Medical Division, ESMO (European Society for Medical Oncology), Lugano, Switzerland.
⁸ NOVA National School of Publich Health, NOVA University, Lisbon, Portugal.
⁹ Department of Internal Medicine and Medical Specialties (DiMI), School of Medicine, University of Genoa, Genova, Italy.
¹⁰ Medical Oncology Department, U.O. Clinica di Oncologia Medica, IRCCS Ospedale Policlinico San Martino, Genova, Italy.
¹¹ Medical Oncology Department, The Royal Marsden Hospital and NHS Foundation Trust, London, UK.
¹² Medical Oncology, Guy's and St Thomas' NHS Foundation Trust (GSTT), London, UK.
¹³ Medical Oncology Department, Hospital Universitario Infanta Leonor, Madrid, Spain.
¹⁴ Medical Oncology, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy.
¹⁵ Department of Internal Medicine and Medical Therapy, University of Pavia, Pavia, Italy.
¹⁶ Medical Oncology Department, Hospital Universitario La Paz, Madrid, Spain.
¹⁷ Department of Medical Oncology, Hospital Clinic de Barcelona, Barcelona, Spain.
¹⁸ Translational Genomics and Targeted Therapies in Solid Tumors, Institut d'Investigacions Biomediques August Pi i Sunyer (IDIBAPS), Barcelona, Spain.
¹⁹ Oncology Department, ASO 'SS Antonio Biagio e Cesare Arrigo', Alessandria, Italy.
²⁰ Medical Oncology, AOU Ospedali Riuniti, Polytechnic University of the Marche Region, Ancona, Italy.
²¹ Medical Oncology Department, Hospital Universitario Ramón y Cajal, Madrid, Spain.
²² Medical Oncology Unit, Spedali Civili, Brescia, Italy.
²³ Melanoma Sarcoma and Rare Tumors, IEO, European Institute of Oncology IRCCS, Milan, Italy.
²⁴ Oncology Department, Centre Hospitalier Universitaire Vaudois (CHUV), Lausanne, Switzerland.
²⁵ Medical Oncology and Hematology Unit, Humanitas Cancer Center, IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy.
²⁶ Department of Oncology and National Centre for HIV Malignancy, Chelsea and Westminster Hospital, London, UK.
²⁷ Oncology, Haematology, Palliative Care Department, Asklepios Klinik Altona e Asklepios Kliniken, Hamburg, Germany.
²⁸ Department of Medical Oncology, ICO L'Hospitalet, Oncobell Program (IDIBELL), CIBERONC, Hospitalet de Llobregat, Barcelona, Spain.
²⁹ Section of Medical Oncology, Department of Interdisciplinary Medicine (DIM), University of Bari 'Aldo Moro', Bari, Italy.
³⁰ IRCCS Istituto Tumori Giovanni Paolo II, Bari, Italy.
³¹ Division of Radiotherapy and Imaging, The Royal Marsden Hospital and The Institute of Cancer Research NIHR Biomedical Research Centre, London, UK.
³² Medical Oncology, Careggi University Hospital, Florence, Italy.
³³ Medical Oncology, Barts Health NHS Trust, London, UK.
³⁴ Frontier Science Foundation-Hellas, Athens, Greece.
³⁵ Department of Cancer Medicine, Institut Gustave Roussy, University of Paris Saclay, 114 rue Edouard Vaillant, Villejuif, France.
³⁶ Department of Medical Oncology, Catalan Institute of Oncology, University Hospital Josep Trueta, Girona, Spain.
³⁷ Division of Haematology, Department of Translational Medicine, University of Piemonte Orientale and Azienda Ospedaliera Maggiore della Carità, Novara, Italy.
³⁸ Division of Oncology, Department of Translational Medicine, University of Piemonte Orientale and Azienda Ospedaliera Maggiore della Carità, Novara, Italy.
³⁹ Division of Radiotherapy, Department of Translational Medicine, University of Piemonte Orientale and Azienda Ospedaliera Maggiore Della Carita, Novara, Italy.
⁴⁰ Medical Oncology, Vall d'Hebron University Hospital and Institute of Oncology (VHIO), IOB-Quiron, UVic-UCC, Barcelona, Spain.
⁴¹ Center for Cancer Immunotherapy, Department of Oncology, PSL Research University, Institut Curie, Paris, France.
⁴² Department of Surgery & Cancer, Hammersmith Hospital Campus, Imperial College London, London, UK.

^# Contributed equally.

PMID: 36450384
PMCID: PMC9716413
DOI: 10.1136/jitc-2022-005732

Immune checkpoint inhibitor therapy and outcomes from SARS-CoV-2 infection in patients with cancer: a joint analysis of OnCovid and ESMO-CoCARE registries

Alessio Cortellini et al. J Immunother Cancer. 2022 Nov.

. 2022 Nov;10(11):e005732.

doi: 10.1136/jitc-2022-005732.

Authors

Affiliations

¹ Department of Surgery & Cancer, Hammersmith Hospital Campus, Imperial College London, London, UK alessiocortellini@gmail.com.
² Medical Oncology, Fondazione Policlinico Universitario Campus Bio-Medico, Via Alvaro del Portillo, 200 - 00128, Roma, Italy.
³ Department of Internal Medicine, Washington University School of Medicine, St. Louis, Missouri, USA.
⁴ Laboratory of Biostatistics, School of Health Sciences, National and Kapodistrian University of Athens, Athens, Greece.
⁵ Medical Oncology, Vall d'Hebron University Hospital and Institute of Oncology (VHIO), Barcelona, Spain.
⁶ Infectious Disease, Vall d'Hebron University Hospital, Barcelona, Spain.
⁷ Scientific and Medical Division, ESMO (European Society for Medical Oncology), Lugano, Switzerland.
⁸ NOVA National School of Publich Health, NOVA University, Lisbon, Portugal.
⁹ Department of Internal Medicine and Medical Specialties (DiMI), School of Medicine, University of Genoa, Genova, Italy.
¹⁰ Medical Oncology Department, U.O. Clinica di Oncologia Medica, IRCCS Ospedale Policlinico San Martino, Genova, Italy.
¹¹ Medical Oncology Department, The Royal Marsden Hospital and NHS Foundation Trust, London, UK.
¹² Medical Oncology, Guy's and St Thomas' NHS Foundation Trust (GSTT), London, UK.
¹³ Medical Oncology Department, Hospital Universitario Infanta Leonor, Madrid, Spain.
¹⁴ Medical Oncology, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy.
¹⁵ Department of Internal Medicine and Medical Therapy, University of Pavia, Pavia, Italy.
¹⁶ Medical Oncology Department, Hospital Universitario La Paz, Madrid, Spain.
¹⁷ Department of Medical Oncology, Hospital Clinic de Barcelona, Barcelona, Spain.
¹⁸ Translational Genomics and Targeted Therapies in Solid Tumors, Institut d'Investigacions Biomediques August Pi i Sunyer (IDIBAPS), Barcelona, Spain.
¹⁹ Oncology Department, ASO 'SS Antonio Biagio e Cesare Arrigo', Alessandria, Italy.
²⁰ Medical Oncology, AOU Ospedali Riuniti, Polytechnic University of the Marche Region, Ancona, Italy.
²¹ Medical Oncology Department, Hospital Universitario Ramón y Cajal, Madrid, Spain.
²² Medical Oncology Unit, Spedali Civili, Brescia, Italy.
²³ Melanoma Sarcoma and Rare Tumors, IEO, European Institute of Oncology IRCCS, Milan, Italy.
²⁴ Oncology Department, Centre Hospitalier Universitaire Vaudois (CHUV), Lausanne, Switzerland.
²⁵ Medical Oncology and Hematology Unit, Humanitas Cancer Center, IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy.
²⁶ Department of Oncology and National Centre for HIV Malignancy, Chelsea and Westminster Hospital, London, UK.
²⁷ Oncology, Haematology, Palliative Care Department, Asklepios Klinik Altona e Asklepios Kliniken, Hamburg, Germany.
²⁸ Department of Medical Oncology, ICO L'Hospitalet, Oncobell Program (IDIBELL), CIBERONC, Hospitalet de Llobregat, Barcelona, Spain.
²⁹ Section of Medical Oncology, Department of Interdisciplinary Medicine (DIM), University of Bari 'Aldo Moro', Bari, Italy.
³⁰ IRCCS Istituto Tumori Giovanni Paolo II, Bari, Italy.
³¹ Division of Radiotherapy and Imaging, The Royal Marsden Hospital and The Institute of Cancer Research NIHR Biomedical Research Centre, London, UK.
³² Medical Oncology, Careggi University Hospital, Florence, Italy.
³³ Medical Oncology, Barts Health NHS Trust, London, UK.
³⁴ Frontier Science Foundation-Hellas, Athens, Greece.
³⁵ Department of Cancer Medicine, Institut Gustave Roussy, University of Paris Saclay, 114 rue Edouard Vaillant, Villejuif, France.
³⁶ Department of Medical Oncology, Catalan Institute of Oncology, University Hospital Josep Trueta, Girona, Spain.
³⁷ Division of Haematology, Department of Translational Medicine, University of Piemonte Orientale and Azienda Ospedaliera Maggiore della Carità, Novara, Italy.
³⁸ Division of Oncology, Department of Translational Medicine, University of Piemonte Orientale and Azienda Ospedaliera Maggiore della Carità, Novara, Italy.
³⁹ Division of Radiotherapy, Department of Translational Medicine, University of Piemonte Orientale and Azienda Ospedaliera Maggiore Della Carita, Novara, Italy.
⁴⁰ Medical Oncology, Vall d'Hebron University Hospital and Institute of Oncology (VHIO), IOB-Quiron, UVic-UCC, Barcelona, Spain.
⁴¹ Center for Cancer Immunotherapy, Department of Oncology, PSL Research University, Institut Curie, Paris, France.
⁴² Department of Surgery & Cancer, Hammersmith Hospital Campus, Imperial College London, London, UK.

^# Contributed equally.

PMID: 36450384
PMCID: PMC9716413
DOI: 10.1136/jitc-2022-005732

Abstract

Background: As management and prevention strategies against COVID-19 evolve, it is still uncertain whether prior exposure to immune checkpoint inhibitors (ICIs) affects COVID-19 severity in patients with cancer.

Methods: In a joint analysis of ICI recipients from OnCovid (NCT04393974) and European Society for Medical Oncology (ESMO) CoCARE registries, we assessed severity and mortality from SARS-CoV-2 in vaccinated and unvaccinated patients with cancer and explored whether prior immune-related adverse events (irAEs) influenced outcome from COVID-19.

Findings: The study population consisted of 240 patients diagnosed with COVID-19 between January 2020 and February 2022 exposed to ICI within 3 months prior to COVID-19 diagnosis, with a 30-day case fatality rate (CFR₃₀) of 23.6% (95% CI 17.8 to 30.7%). Overall, 42 (17.5%) were fully vaccinated prior to COVID-19 and experienced decreased CFR₃₀ (4.8% vs 28.1%, p=0.0009), hospitalization rate (27.5% vs 63.2%, p<0.0001), requirement of oxygen therapy (15.8% vs 41.5%, p=0.0030), COVID-19 complication rate (11.9% vs 34.6%, p=0.0040), with a reduced need for COVID-19-specific therapy (26.3% vs 57.9%, p=0.0004) compared with unvaccinated patients. Inverse probability of treatment weighting (IPTW)-fitted multivariable analysis, following a clustered-robust correction for the data source (OnCovid vs ESMO CoCARE), confirmed that vaccinated patients experienced a decreased risk of death at 30 days (adjusted OR, aOR 0.08, 95% CI 0.01 to 0.69).Overall, 38 patients (15.8%) experienced at least one irAE of any grade at any time prior to COVID-19, at a median time of 3.2 months (range 0.13-48.7) from COVID-19 diagnosis. IrAEs occurred independently of baseline characteristics except for primary tumor (p=0.0373) and were associated with a significantly decreased CFR₃₀ (10.8% vs 26.0%, p=0.0462) additionally confirmed by the IPTW-fitted multivariable analysis (aOR 0.47, 95% CI 0.33 to 0.67). Patients who experienced irAEs also presented a higher median absolute lymphocyte count at COVID-19 (1.4 vs 0.8 10⁹ cells/L, p=0.0098).

Conclusion: Anti-SARS-CoV-2 vaccination reduces morbidity and mortality from COVID-19 in ICI recipients. History of irAEs might identify patients with pre-existing protection from COVID-19, warranting further investigation of adaptive immune determinants of protection from SARS-CoV-2.

Keywords: COVID-19; Cytotoxicity, Immunologic; Immunogenicity, Vaccine; Immunotherapy; Vaccination.

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Conflict of interest statement

Competing interests: KJH declares research funding from AstraZeneca, Boehringer-Ingelheim, MSD, Replimune and advisory board fees/honoraria from Arch Oncology, AstraZeneca, BMS, Boehringer-Ingelheim, Codiak Biosciences, Inzen Therapeutics, Merck-Serono, MSD, Pfizer, Replimune. DA reports consultation/advisory role for AstraZeneca, Bristol Myers Squibb, Merck Sharp reports speaker’s engagement from AstraZeneca, Bristol Myers Squibb, Merck Sharp reports serving as local PI for Bristol Myers Squibb, Pierre Fabre Pharma and coordinating PI for OncoLytics; reports grant funding from AbbVie; reports being/been DSMB chair of Sanofi (Genzyme); reports being/been a steering committee member of Roche. Olivier Michielin reports personal fees from Bristol-Myers Squibb, MSD, Novartis, Roche, Amgen, NeraCare, outside the submitted work. JR received speaker or advisory fees from Roche, Astra Zeneca, Merck, Ferrer, Persan Farma, Teva Pharma, Leo Pharma, Fresenius kabi, MSD, BMS. Travel expenses support from BMS, MSD, RocheUrania Dafni reports honorarium as Member of the Tumor Agnostic Evidence Generation Working Group of Roche, outside the submitted work. GP reports grants from Amgen, Lilly; grants, personal fees and nonfinancial support from Merck; grants and non-financial support from AstraZeneca; grants and personal fees from Roche, Bristol Myers Squibb, MSD, Novartis, outside the submitted work. Solange Peters reports consultation/advisory role for AbbVie, Amgen, AstraZeneca, Bayer, BeiGene, Biocartis, Bio Invent, Blueprint Medicines, Boehringer Ingelheim, Bristol- Myers Squibb, Clovis, Daiichi Sankyo, Debiopharm, Eli Lilly, Elsevier, F Hoffmann-La Roche/Genentech, Foundation Medicine, Illumina, Incyte, IQVIA, Janssen, Medscape, Merck Sharp and Dohme, Merck Serono, Merrimack, Mirati, Novartis, Pharma Mar, Phosplatin Therapeutics, Pfizer, Regeneron, Sanofi, Seattle Genetics, Takeda, Vaccibody; talk in a company’s organized public event for AstraZeneca, Boehringer Ingelheim, Bristol-Myers Squibb, e-cancer, Eli Lilly, F. Hoffmann-La Roche/Genentech, Illumina, Medscape, Merck Sharp and Dohme, Novartis, PER, Pfizer, Prime, RTP, Sanofi, Takeda; receipt of grants/research supports from being a (sub)investigator in trials (institutional financial support for clinical trials) sponsored by Amgen, AstraZeneca, Biodesix, Boehringer Ingelheim, Bristol-Myers Squibb, Clovis, F Hoffmann-La Roche/Genentech, GSK, Illumina, Lilly, Merck Sharp and Dohme, Merck Serono, Mirati, Novartis, and Pfizer, Phosplatin Therapeutics. Emanuela Rromano reports investigator-initiated trial (funds paid to the institution) supported by Astra-Zeneca, BMS; serves on the consultancy/advisory board for Astra-Zeneca, Merck, Roche, Pierre Fabre. ML acted as consultant for Roche, Novartis, Lilly, AstraZeneca, Exact Sciences, MSD, Pfizer, Seagen and received speaker honoraria from Roche, Novartis, Lilly, Pfizer, Takeda, Ipsen and Sandoz outside the submitted work.Alessandra Gennari has declared consulting/advisory role for Roche, MSD, Eli Lilly, Pierre Fabre, EISAI, and Daichii Sankyo; speakers bureau for Eisai, Novartis, Eli Lilly, Roche, Teva, Gentili, Pfizer, Astra Zeneca, Celgene, and Daichii Sankyo; research funds: EISAI, Eli Lilly, and Roche. CMV has received travel grants and other honoraria from BMS, MSD, Novartis and Roche. Joan Brunet has declared consulting/advisory role for MSD and Astra Zeneca. Aleix Prat has declared personal honoraria from Pfizer, Roche, MSD Oncology, Eli Lilly, and Daiichi Sankyo; travel, accommodations, and expenses paid by Daiichi Sankyo; research funding from Roche and Novartis; and consulting/advisory role for NanoString Technologies, Amgen, Roche, Novartis, Pfizer and Bristol-Myers Squibb. Mark Bower received speakers’ fee from EISAI pharma, Gilead Sciences, Merck and ViiV. JT reports consulting fees from Array Biopharma, AstraZeneca, Avvinity, Bayer, Boehringer Ingelheim, Chugai, Daiichi Sankyo, F Hoffmann-La Roche, Genentech, HalioDX SAS, Hutchison MediPharma International, Ikena Oncology, Inspirna, IQVIA, Lilly, Menarini, Merck Serono, Merus, MSD, Mirati, Neophore, Novartis, Ona Therapeutics, Orion Biotechnology, Peptomyc, Pfizer, Pierre Fabre, Samsung Bioepis, Sanofi, Seattle Genetics, Scandion Oncology, Servier, Sotio Biotech, Taiho, Tessa Therapeutics, and TheraMyc; speaker’s fees from Imedex, Medscape Education, MJH Life Sciences, PeerView Institute for Medical Education, and Physicians Education Resource; and institutional research support from Amgen, Array Biopharma, AstraZeneca Pharmaceuticals, BeiGene, Boehringer Ingelheim, Bristol Myers Squibb, Celgene, Debiopharm International, F Hoffmann-La Roche, Genentech, HalioDX, Hutchison MediPharma International, Janssen-Cilag, MedImmune, Menarini, Merck Health, Merck Sharp and has had leadership roles in the European AIDS Clinical Society, UNAIDS, WHO, and The European Hematology Association/ European Society of Medical Oncology. DJP received lecture fees from ViiV Healthcare, Bayer Healthcare, BMS, Roche, EISAI, Falk Foundation, travel expenses from BMS and Bayer Healthcare; consulting fees for Mina Therapeutics, EISAI, Roche, DaVolterra and Astra Zeneca; research funding (to institution) from MSD and BMS. AC received consulting fees from MSD, BMS, AstraZeneca, Roche; speakers’ fee from AstraZeneca, MSD, Novartis and Eisai. All remaining authors have declared no conflicts of interest.

Figures

**Figure 1**
Study flow diagram. ESMO, European Society for Medical Oncology; ICI, immune checkpoint inhibitor; SACT, systemic anti-cancer therapies.

**Figure 2**
Histogram plot summarizing all COVID-19 outcomes according to the vaccination status. All rates with 95% CIs are available in online supplemental table 4. CFR30, 30-day case fatality rate; ICU, intensive care unit.

**Figure 3**
Summary of the inverse probability of treatment weighing (IPTW) fitted multivariable analyses for each COVID-19 outcomes according to the vaccination status prior to (blue) and after (red) the clustered-robust SE and 95% CI adjustments for the data source. Adjusting covariates for each COVID-19 outcome were country of origin, comorbidities, tumor status, and tumor stage at COVID-19. Full multivariable models are available in online supplemental table 6. aOR, adjusted OR; CFR30, 30-day case fatality rate.

**Figure 4**
(A) Histogram plot summarizing the all-cause 30-day case fatality rate (CFR30) analysis according to the occurrence of any grade immune-related adverse events prior to COVID-19. Inverse probability of treatment weighing (IPTW) fitted adjusted OR for the risk of death at 30 days with clustered robust 95% CI correction for the data source is presented. All rates with 95% CI are available in online supplemental table 9. Adjusting covariates were country of origin, primary tumor, tumor stage at COVID-19 and vaccination status. Full multivariable model is available in online supplemental table 11. (B) Violin plot reporting the median absolute lymphocyte count at COVID-19 (within 1 week of diagnosis) according to the prior occurrence or any grade irAEs. IrAEs, immune-related adverse events.

See this image and copyright information in PMC

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Immune checkpoint inhibitor therapy and outcomes from SARS-CoV-2 infection in patients with cancer: a joint analysis of OnCovid and ESMO-CoCARE registries

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Immune checkpoint inhibitor therapy and outcomes from SARS-CoV-2 infection in patients with cancer: a joint analysis of OnCovid and ESMO-CoCARE registries

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