Comprehensive humoral and cellular immune responses to COVID-19 vaccination in adults with cancer

Amy Body; Luxi Lal; Sriganesh Srihari; C Raina MacIntyre; Jim Buttery; Elizabeth Stephanie Ahern; Stephen Opat; Michael Francis Leahy; Nada Hamad; Vivienne Milch; Stuart Turville; Corey Smith; Katie Lineburg; Zin Naing; William Rawlinson; Eva Segelov

doi:10.1016/j.vaccine.2024.126547

Comprehensive humoral and cellular immune responses to COVID-19 vaccination in adults with cancer

Vaccine. 2024 Dec 7:126547. doi: 10.1016/j.vaccine.2024.126547. Online ahead of print.

Authors

Affiliations

¹ Monash Health, Department of Oncology, Melbourne, VIC, Australia; Monash University, Department of Oncology, School of Clinical Sciences, Melbourne, VIC, Australia. Electronic address: amy.body@monash.edu.
² Monash Health, Department of Oncology, Melbourne, VIC, Australia; Monash University, Department of Oncology, School of Clinical Sciences, Melbourne, VIC, Australia.
³ Queensland Institute of Medical Research-Berghofer, QLD, Australia.
⁴ Biosecurity Program, Kirby Institute, University of New South Wales, Sydney, NSW, Australia; School of Public Health and Community Medicine, University of New South Wales, Sydney, NSW, Australia; National Centre for Immunization, Research and Surveillance of Vaccine Preventable Diseases, University of Sydney, Westmead, NSW, Australia.
⁵ University of Melbourne, Child Health Informatics (Paediatrics), Melbourne, VIC, Australia; Royal Children's Hospital, Melbourne, VIC, Australia; Murdoch Children's Research Institute, Parkville, VIC, Australia.
⁶ Department of Haematology, Royal Perth Hospital, WA, Australia; University of Western Australia, School of Medicine & Pharmacology, School of Pathology, Perth, WA, Australia.
⁷ Department of Haematology, St Vincent's Hospital, Kinghorn Cancer Centre, Sydney, NSW, Australia; The University of New South Wales, NSW, Australia.
⁸ Cancer Australia, Sydney, NSW, Australia; Caring Futures Institute, Flinders University, Adelaide, SA, Australia; School of Medicine, The University of Notre Dame Australia, Sydney, NSW, Australia.
⁹ Kirby Institute, University of New South Wales, Sydney, NSW, Australia; University of Sydney, NSW, Australia.
¹⁰ QIMR Berghofer Centre for Immunotherapy and Vaccine Development and Translational and Human Immunology Laboratory, Infection and Inflammation Program, QIMR Berghofer Medical Research Institute, Herston, QLD, Australia; Queensland Immunology Research Centre, Brisbane, QLD, Australia.
¹¹ QIMR Berghofer Centre for Immunotherapy and Vaccine Development and Translational and Human Immunology Laboratory, Infection and Inflammation Program, QIMR Berghofer Medical Research Institute, Herston, QLD, Australia.
¹² Serology and Virology Division (SAViD), NSW Health Pathology East, Department of Microbiology, Prince of Wales Hospital, Randwick, Sydney, NSW, Australia.
¹³ Serology and Virology Division (SAViD), NSW Health Pathology East, Department of Microbiology, Prince of Wales Hospital, Randwick, Sydney, NSW, Australia; Virology Research Laboratory, Prince of Wales Hospital, Randwick, Sydney, NSW, Australia; School of Medical Sciences, Faculty of Medicine, University of New South Wales, Sydney, NSW, Australia.
¹⁴ Monash University, Department of Oncology, School of Clinical Sciences, Melbourne, VIC, Australia; University of Bern, Department of Clinical Research (Medicine), Bern, Switzerland; University Cancer Centre, Bern, Switzerland.

PMID: 39648104
DOI: 10.1016/j.vaccine.2024.126547

Abstract

Background: The COVID-19 pandemic has significantly impacted people with cancer. Initial vaccine studies excluded patients with malignancy. Immunocompromised individuals remain vulnerable to SARS-CoV-2, necessitating detailed understanding of vaccine response. The epidemiology of COVID-19 in Australia offered unique opportunities to study cancer populations with minimal community exposure to SARS-CoV-2.

Methods: SerOzNET prospectively examined previously unvaccinated patients with solid and haematological malignancies receiving up to five COVID-19 vaccine doses. Antibody response was measured by live virus neutralisation assay (neutralising antibody (NAb); positive titre ≥1:20; study primary endpoint) and commercial assay. T cell response was measured by cytometric bead array; positive defined as interferon gamma (IFN-γ) ≥10 pg/mL in response to Spike antigen. Patient and physician-reported adverse events were secondary endpoints.

Outcomes: 395 adults were enrolled prior to receiving mRNA vaccine (BNT162b2 = 347; mRNA-1273 = 1) or viral vector vaccine (ChadOx1-S = 43) for initial two-dose course, plus up to three additional doses. Median age was 58 years (range: 20-85); 60 % were female; 35 % had haematological malignancy, 2/395 (0.5 %) had baseline positive nucleocapsid antibody indicating prior SARS-CoV-2 exposure. NAb response post dose three was demonstrated in 84 % overall; 96 % of patients with solid cancers and 64 % with haematological cancer (p < 0·001). Risk factors for non-response were haematological cancer and anti B-cell therapies. Some patients with haematological cancer seroconverted for the first time after the fourth or fifth dose. IFN-γ response was seen in many patients with haematological cancer who lacked NAb response. Serious adverse events were rare. COVID-19 infection occurred in 29 % with no deaths.

Interpretation: COVID-19 vaccination elicits B and T cell responses in patients with solid and haematological cancers, with an acceptable safety profile. A significant proportion of haematological cancer patients require >3 doses to elicit NAb, with many demonstrating T cell response, which may be an alternative pathway of immune protection.

Keywords: Antibody response; COVID-19; Cancer; SARS-CoV-2; T cell response; Vaccine response.