Functional antibody and T cell immunity following SARS-CoV-2 infection, including by variants of concern, in patients with cancer: the CAPTURE study.

Adolescent Adult Aged Aged, 80 and over Antibodies, Neutralizing / blood Antibodies, Viral / blood COVID-19 / blood Female Follow-Up Studies Humans Immunity, Cellular Male Middle Aged Neoplasms / blood Prospective Studies SARS-CoV-2 / immunology Spike Glycoprotein, Coronavirus / immunology T-Lymphocytes / immunology Young Adult

Journal

Nature cancer

ISSN: 2662-1347

Titre abrégé: Nat Cancer

Pays: England

ID NLM: 101761119

Informations de publication

Date de publication:
12 2021

Historique:

received: 23 08 2021

accepted: 17 09 2021

entrez: 5 2 2022

pubmed: 6 2 2022

medline: 15 2 2022

Statut: ppublish

Résumé

Patients with cancer have higher COVID-19 morbidity and mortality. Here we present the prospective CAPTURE study, integrating longitudinal immune profiling with clinical annotation. Of 357 patients with cancer, 118 were SARS-CoV-2 positive, 94 were symptomatic and 2 died of COVID-19. In this cohort, 83% patients had S1-reactive antibodies and 82% had neutralizing antibodies against wild type SARS-CoV-2, whereas neutralizing antibody titers against the Alpha, Beta and Delta variants were substantially reduced. S1-reactive antibody levels decreased in 13% of patients, whereas neutralizing antibody titers remained stable for up to 329 days. Patients also had detectable SARS-CoV-2-specific T cells and CD4

Identifiants

DOI: 10.1038/s43018-021-00275-9 PMID: 35121900

pubmed: 35121900

doi: 10.1038/s43018-021-00275-9

pii: 10.1038/s43018-021-00275-9

doi:

Substances chimiques

Antibodies, Neutralizing 0

Antibodies, Viral 0

Spike Glycoprotein, Coronavirus 0

spike protein, SARS-CoV-2 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

Pagination

1321-1337

Subventions

Organisme : NCI NIH HHS

ID : U01 CA247439

Pays : United States

Commentaires et corrections

Type : UpdateOf

Type : CommentIn

Informations de copyright

Références

Saini, K. S. et al. Mortality in patients with cancer and coronavirus disease 2019: a systematic review and pooled analysis of 52 studies. Eur. J. Cancer 139, 43–50 (2020).

pubmed: 32971510 pmcid: 7467090 doi: 10.1016/j.ejca.2020.08.011

Williamson, E. J. et al. Factors associated with COVID-19-related death using OpenSAFELY. Nature 584, 430–436 (2020).

pubmed: 32640463 pmcid: 7611074 doi: 10.1038/s41586-020-2521-4

Garcia-Suarez, J. et al. Impact of hematologic malignancy and type of cancer therapy on COVID-19 severity and mortality: lessons from a large population-based registry study. J. Hematol. Oncol. 13, 133 (2020).

pubmed: 33032660 pmcid: 7542567 doi: 10.1186/s13045-020-00970-7

Garassino, M. C. et al. COVID-19 in patients with thoracic malignancies (TERAVOLT): first results of an international, registry-based, cohort study. Lancet Oncol. 21, 914–922 (2020).

pubmed: 32539942 pmcid: 7292610 doi: 10.1016/S1470-2045(20)30314-4

Lee, L. Y. et al. COVID-19 mortality in patients with cancer on chemotherapy or other anticancer treatments: a prospective cohort study. Lancet 395, 1919–1926 (2020).

pubmed: 32473682 pmcid: 7255715 doi: 10.1016/S0140-6736(20)31173-9

Kuderer, N. M. et al. Clinical impact of COVID-19 on patients with cancer (CCC19): a cohort study. Lancet 395, 1907–1918 (2020).

pubmed: 32473681 pmcid: 7255743 doi: 10.1016/S0140-6736(20)31187-9

Grivas, P. et al. Association of clinical factors and recent anticancer therapy with COVID-19 severity among patients with cancer: a report from the COVID-19 and Cancer Consortium. Ann. Oncol. 32, 787–800 (2021).

pubmed: 33746047 doi: 10.1016/j.annonc.2021.02.024

Lee, L. Y. W. et al. COVID-19 prevalence and mortality in patients with cancer and the effect of primary tumour subtype and patient demographics: a prospective cohort study. Lancet Oncol. 21, 1309–1316 (2020).

pubmed: 32853557 pmcid: 7444972 doi: 10.1016/S1470-2045(20)30442-3

Crolley, V. E. et al. COVID-19 in cancer patients on systemic anti-cancer therapies: outcomes from the CAPITOL (COVID-19 Cancer PatIenT Outcomes in North London) cohort study. Ther. Adv. Med. Oncol. 12, 1758835920971147 (2020).

pubmed: 33178336 pmcid: 7592172 doi: 10.1177/1758835920971147

Robilotti, E. V. et al. Determinants of COVID-19 disease severity in patients with cancer. Nat. Med. 26, 1218–1223 (2020).

pubmed: 32581323 pmcid: 7785283 doi: 10.1038/s41591-020-0979-0

Bange, E. M. et al. CD8

pubmed: 34017137 pmcid: 8291091 doi: 10.1038/s41591-021-01386-7

Abdul-Jawad, S. et al. Acute immune signatures and their legacies in severe acute respiratory syndrome coronavirus-2 infected cancer patients. Cancer Cell 39, 257–275.e256 (2021).

pubmed: 33476581 pmcid: 7833668 doi: 10.1016/j.ccell.2021.01.001

Thakkar, A. et al. Seroconversion rates following COVID-19 vaccination among patients with cancer. Cancer Cell 39, 1081–1090.e2 (2021).

pubmed: 34133951 pmcid: 8179248 doi: 10.1016/j.ccell.2021.06.002

Au, L. et al. Cancer, COVID-19, and antiviral immunity: the CAPTURE study. Cell 183, 4–10 (2020).

pubmed: 32979319 pmcid: 7470737 doi: 10.1016/j.cell.2020.09.005

Marshall, J. C. et al. A minimal common outcome measure set for COVID-19 clinical research. Lancet Infect. Dis. 20, e192–e197 (2020).

doi: 10.1016/S1473-3099(20)30483-7

Lowe, K. E., Zein, J., Hatipoglu, U. & Attaway, A. Association of smoking and cumulative pack-year exposure with COVID-19 outcomes in the Cleveland Clinic COVID-19 registry. JAMA Intern. Med. 181, 709–711 (2021).

pubmed: 33492361 doi: 10.1001/jamainternmed.2020.8360 pmcid: 7835916

Rosenthal, N., Cao, Z., Gundrum, J., Sianis, J. & Safo, S. Risk factors associated with in-hospital mortality in a US national sample of patients with COVID-19. JAMA Netw. Open 3, e2029058 (2020).

pubmed: 33301018 pmcid: 7729428 doi: 10.1001/jamanetworkopen.2020.29058

Sterlin, D. et al. IgA dominates the early neutralizing antibody response to SARS-CoV-2. Sci. Transl. Med. 13, eabd2223 (2021).

pubmed: 33288662 doi: 10.1126/scitranslmed.abd2223

Grifoni, A. et al. Targets of T cell responses to SARS-CoV-2 coronavirus in humans with COVID-19 disease and unexposed individuals. Cell https://doi.org/10.1016/j.cell.2020.05.015 (2020).

Dan, J. M. et al. Immunological memory to SARS-CoV-2 assessed for up to 8 months after infection. Science 371, eabf4063 (2021).

pubmed: 33408181 doi: 10.1126/science.abf4063

Moderbacher, C. R. et al. Antigen-specific adaptive immunity to SARS-CoV-2 in acute COVID-19 and associations with age and disease severity. Cell https://doi.org/10.1016/j.cell.2020.09.038 (2020).

Weiskopf, D. et al. Phenotype and kinetics of SARS-CoV-2-specific T cells in COVID-19 patients with acute respiratory distress syndrome. Sci. Immunol.5, eabd2071 (2020).

pubmed: 32591408 pmcid: 7319493 doi: 10.1126/sciimmunol.abd2071

Mateus, J. et al. Selective and cross-reactive SARS-CoV-2 T cell epitopes in unexposed humans. Science https://doi.org/10.1126/science.abd3871 (2020).

Marra, A. et al. Seroconversion in patients with cancer and oncology health care workers infected by SARS-CoV-2. Ann. Oncol. 32, 113–119 (2021).

pubmed: 33098994 doi: 10.1016/j.annonc.2020.10.473

Dispinseri, S. et al. Neutralizing antibody responses to SARS-CoV-2 in symptomatic COVID-19 is persistent and critical for survival. Nat. Commun. 12, 2670 (2021).

pubmed: 33976165 pmcid: 8113594 doi: 10.1038/s41467-021-22958-8

Earle, K. A. et al. Evidence for antibody as a protective correlate for COVID-19 vaccines. Vaccine 39, 4423–4428 (2021).

pubmed: 34210573 pmcid: 8142841 doi: 10.1016/j.vaccine.2021.05.063

Khoury, D. S. et al. Neutralizing antibody levels are highly predictive of immune protection from symptomatic SARS-CoV-2 infection. Nat. Med. 27, 1205–1211 (2021).

pubmed: 34002089 doi: 10.1038/s41591-021-01377-8

Ju, B. et al. Human neutralizing antibodies elicited by SARS-CoV-2 infection. Nature 584, 115–119 (2020).

pubmed: 32454513 doi: 10.1038/s41586-020-2380-z

Fendler, A. et al. Adaptive immunity and neutralizing antibodies against SARS-CoV-2 variants of concern following vaccination in patients with cancer: the CAPTURE study. Nat. Cancer https://doi.org/10.1038/s43018-021-00274-w (2021).

Seow, J. et al. Longitudinal observation and decline of neutralizing antibody responses in the three months following SARS-CoV-2 infection in humans. Nat. Microbiol. 5, 1598–1607 (2020).

pubmed: 33106674 pmcid: 7610833 doi: 10.1038/s41564-020-00813-8

Gaebler, C. et al. Evolution of antibody immunity to SARS-CoV-2. Nature 591, 639–644 (2021).

pubmed: 33461210 pmcid: 8221082 doi: 10.1038/s41586-021-03207-w

Wang, Z. et al. Naturally enhanced neutralizing breadth against SARS-CoV-2 one year after infection. Nature 595, 426–431 (2021).

pubmed: 34126625 pmcid: 8277577 doi: 10.1038/s41586-021-03696-9

Achiron, A. et al. Humoral immune response to COVID-19 mRNA vaccine in patients with multiple sclerosis treated with high-efficacy disease-modifying therapies. Ther. Adv. Neurol. Disord. https://doi.org/10.1177/17562864211012835 (2021).

Garcia-Beltran, W. F. et al. COVID-19 neutralizing antibodies predict disease severity and survival. Cell 184, 476–488.e11 (2021).

pubmed: 33412089 doi: 10.1016/j.cell.2020.12.015

Vacharathit, V. et al. CoronaVac induces lower neutralising activity against variants of concern than natural infection. Lancet Infect. Dis. 21, 1352–1354 (2021).

pubmed: 34454652 pmcid: 8389976 doi: 10.1016/S1473-3099(21)00568-5

Juno, J. A. et al. Humoral and circulating follicular helper T cell responses in recovered patients with COVID-19. Nat. Med. 26, 1428–1434 (2020).

pubmed: 32661393 doi: 10.1038/s41591-020-0995-0

Murugesan, K. et al. Interferon-γ release assay for accurate detection of severe acute respiratory syndrome coronavirus 2 T-cell response. Clin. Infect. Dis. https://doi.org/10.1093/cid/ciaa1537 (2020).

Pauken, K. E. et al. The PD-1 pathway regulates development and function of memory CD8

pubmed: 32610128 pmcid: 7377452 doi: 10.1016/j.celrep.2020.107827

Konkel, J. E. et al. PD-1 signalling in CD4

pubmed: 20113370 pmcid: 2855797 doi: 10.1111/j.1365-2567.2009.03216.x

Zhao, J., Zhao, J. & Perlman, S. T cell responses are required for protection from clinical disease and for virus clearance in severe acute respiratory syndrome coronavirus-infected mice. J. Virol. 84, 9318–9325 (2010).

pubmed: 20610717 pmcid: 2937604 doi: 10.1128/JVI.01049-10

Muñoz-Fontela, C. et al. Animal models for COVID-19. Nature 586, 509–515 (2020).

pubmed: 32967005 pmcid: 8136862 doi: 10.1038/s41586-020-2787-6

Tan, A. T. et al. Early induction of functional SARS-CoV-2-specific T cells associates with rapid viral clearance and mild disease in COVID-19 patients. Cell Rep. 34, 108728 (2021).

pubmed: 33516277 pmcid: 7826084 doi: 10.1016/j.celrep.2021.108728

Tarke, A. et al. Impact of SARS-CoV-2 variants on the total CD4

Apostolidis, S.A. et al. Cellular and humoral immune responses following SARS-CoV-2 mRNA vaccination in patients with multiple sclerosis on anti-CD20 therapy. Nat. Med. https://doi.org/10.1038/s41591-021-01507-2 (2021).

Sahin, U. et al. COVID-19 vaccine BNT162b1 elicits human antibody and T

pubmed: 32998157 doi: 10.1038/s41586-020-2814-7

Ewer, K. J. et al. T cell and antibody responses induced by a single dose of ChAdOx1 nCoV-19 (AZD1222) vaccine in a phase 1/2 clinical trial. Nat. Med. 27, 270–278 (2021).

pubmed: 33335323 doi: 10.1038/s41591-020-01194-5

Normark, J. et al. Heterologous ChAdOx1 nCoV-19 and mRNA-1273 vaccination. N. Engl. J. Med. 385, 1049–1051 (2021).

pubmed: 34260850 doi: 10.1056/NEJMc2110716

Barros-Martins, J. et al. Immune responses against SARS-CoV-2 variants after heterologous and homologous ChAdOx1 nCoV-19/BNT162b2 vaccination. Nat. Med. 27, 1525–1529 (2021).

pubmed: 34262158 pmcid: 8440184 doi: 10.1038/s41591-021-01449-9

Spencer, A.J. et al. Heterologous vaccination regimens with self-amplifying RNA and adenoviral COVID vaccines induce robust immune responses in mice. Nat. Commun. 12, 2893 (2021).

pubmed: 34001897 pmcid: 8129084 doi: 10.1038/s41467-021-23173-1

Angelis, V. et al. Defining the true impact of coronavirus disease 2019 in the at-risk population of patients with cancer. Eur. J. Cancer 136, 99–106 (2020).

pubmed: 32659475 pmcid: 7340059 doi: 10.1016/j.ejca.2020.06.027

Sekine, T. et al. Robust T cell immunity in convalescent individuals with asymptomatic or mild COVID-19. Cell 183, 158–168 (2020).

pubmed: 32979941 pmcid: 7427556 doi: 10.1016/j.cell.2020.08.017

Aitken, J. et al. Scalable and robust SARS-CoV-2 testing in an academic center. Nat. Biotechnol. 38, 927–931 (2020).

pubmed: 32555528 doi: 10.1038/s41587-020-0588-y

Di Tommaso, P. et al. Nextflow enables reproducible computational workflows. Nat. Biotechnol. 35, 316–319 (2017).

pubmed: 28398311 doi: 10.1038/nbt.3820

Baker, D. J. et al. CoronaHiT: high-throughput sequencing of SARS-CoV-2 genomes. Genome Med. 13, 21 (2021).

pubmed: 33563320 pmcid: 7871948 doi: 10.1186/s13073-021-00839-5

Ewels, P. A. et al. The nf-core framework for community-curated bioinformatics pipelines. Nat. Biotechnol. 38, 276–278 (2020).

pubmed: 32055031 doi: 10.1038/s41587-020-0439-x

Faulkner, N. et al. Reduced antibody cross-reactivity following infection with B.1.1.7 than with parental SARS-CoV-2 strains. eLife 10, e69317 (2021).

pubmed: 34323691 pmcid: 8352583 doi: 10.7554/eLife.69317

Rihn, S. J. et al. A plasmid DNA-launched SARS-CoV-2 reverse genetics system and coronavirus toolkit for COVID-19 research. PLoS Biol. 19, e3001091 (2021).

pubmed: 33630831 pmcid: 7906417 doi: 10.1371/journal.pbio.3001091