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Acute immune signatures and their legacies in severe acute respiratory syndrome coronavirus-2 infected cancer patients

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Sultan Abdul-Jawad, Luca Baù, Thanussuyah Alaguthurai, Irene Del Molino Del Barrio, Adam G Laing, Thomas S Hayday, Leticia Monin, Miguel Muñoz-Ruiz, Louisa McDonald, Isaac Francos Quijorna, Duncan McKenzie, Richard Davis, Anna Lorenc, Julie Nuo En Chan, Sarah Ryan, Eva Bugallo-Blanco, Rozalyn Yorke, Shraddha Kamdar, Matthew Fish, Iva Zlatareva & 31 more Pierre Vantourout, Aislinn Jennings, Sarah Gee, Katie Doores, Katharine Bailey, Sophie Hazell, Julien De Naurois, Charlotte Moss, Beth Russell, Aadil A Khan, Mark Rowley, Reuben Benjamin, Deborah Enting, Doraid Alrifai, Yin Wu, You Zhou, Paul Barber, Tony Ng, James Spicer, Mieke Van Hemelrijck, Mayur Kumar, Jennifer Vidler, Yadanar Lwin, Paul Fields, Sophia N Karagiannis, Anthony C C Coolen, Anne Rigg, Sophie Papa, Adrian C Hayday, Piers E M Patten, Sheeba Irshad

Original languageEnglish
Pages (from-to)257-275.e6
JournalCANCER CELL
Volume39
Issue number2
Early online date5 Jan 2021
DOIs
Accepted/In press30 Dec 2020
E-pub ahead of print5 Jan 2021
Published8 Feb 2021

Bibliographical note

Funding Information: M. Joseph, D. Davies, J. Freedman, L. Martinez, B. Merrick, K. Bisnauthsing, J. Cason, C. Mant, F. Rosa, J. Edgeworth, and M.Shankar-Hari contributed to the COVID-IP project. We thank members of the GSTT and KCH trial teams who contributed to patient recruitment for the SOAP study at Guy's and KCH hospitals; and clinical colleagues at GSTT, KCH, and PRUH for assisting with patient identification and sample collection. The SOAP study (IRAS 282337) is sponsored by King's College London and Guy's & St Thomas? Foundation NHS Trust. It is funded from grants from the KCL Charity funds to S.I. (PS10822), MRC to P.E.P. (T005106), Cancer Research UK to S.I. (C56773/A24869), program grants from Breast Cancer Now including S.I. at King's College London and to the Breast Cancer Now Toby Robin's Research Center at the Institute of Cancer Research, London; and the Wellcome Trust Investigator Award to A.C.H. (106292/Z/14/Z), the Rosetrees and John Black Charitable Foundation award to A.C.H (11130) and is supported by the Cancer Research UK Cancer Immunotherapy Accelerator and the UK COVID-Immunology-Consortium (CIC) (C33499/A20265). Conceptualization S.A-J. L.B. I.D. A.G.L. T.H. L.M. M.M-R. S.P. A.C.H. P.E.P. S.I. Methodology S.A-J. I.D. A.G. T.H. L.M. M.M-R. I.Q. D.M. R.D. K.D. Formal analysis L.B. S.A-J. T.A. I.D. A.G. T.H. L.M. M.M-R. A.L. A.A.K. Y.Z. P.B. M.R. A.C.C. S.I. Investigation S.A-J. I.D. T.A. A.L. T.H. L.M. M.M-R. L.M. I.Q. D.M. R.D. J.C. S.R. E.B. R.Y. S.K. M.F. I.Z. P.V. A.J. S.G. K.D. A.A.K. M.R. Resource T.A. L.M. D.E. K.B. S.H. J.D.N. R.B. Y.L. J.V. M.K. Data curation S.A-J. L.B. T.A. I.D. A.L. T.H. A.L. S.K. C.M. B.R. M.V.H. Visualization L.B. S.A-J. T.A. S.I. Writing original draft P.E.P. S.I. Writing review and editing S.P. A.R. A.C.C, S.N.K. P.F. M.V.H. J.S. T.N. Y.W. D.E. A.A.K. S.A-J. L.B. T.A. I.D. A.G.L. T.H. M.M-R. A.C.H. P.E.P. S.I. Supervision A.C.H. P.E.P. S.I. Project administration S.A-J. A.L. T.H. R.D. Funding acquisition S.I. The authors declare no competing interests. Publisher Copyright: © 2021 Copyright: Copyright 2021 Elsevier B.V., All rights reserved.

King's Authors

Abstract

Given the immune system's importance for cancer surveillance and treatment, we have investigated how it may be affected by SARS-CoV-2 infection of cancer patients. Across some heterogeneity in tumor type, stage, and treatment, virus-exposed solid cancer patients display a dominant impact of SARS-CoV-2, apparent from the resemblance of their immune signatures to those for COVID-19 + non-cancer patients. This is not the case for hematological malignancies, with virus-exposed patients collectively displaying heterogeneous humoral responses, an exhausted T cell phenotype and a high prevalence of prolonged virus shedding. Furthermore, while recovered solid cancer patients' immunophenotypes resemble those of non-virus-exposed cancer patients, recovered hematological cancer patients display distinct, lingering immunological legacies. Thus, while solid cancer patients, including those with advanced disease, seem no more at risk of SARS-CoV-2-associated immune dysregulation than the general population, hematological cancer patients show complex immunological consequences of SARS-CoV-2 exposure that might usefully inform their care.

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