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

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; 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

doi:10.1016/j.ccell.2021.01.001

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

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 ZlatarevaPierre 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

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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.

Original language	English
Pages (from-to)	257-275.e6
Journal	CANCER CELL
Volume	39
Issue number	2
Early online date	5 Jan 2021
DOIs	https://doi.org/10.1016/j.ccell.2021.01.001
Publication status	Published - 8 Feb 2021

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Abdul-Jawad, S., Baù, L., Alaguthurai, T., Del Molino Del Barrio, I., Laing, A. G., Hayday, T. S., Monin, L., Muñoz-Ruiz, M., McDonald, L., Francos Quijorna, I., McKenzie, D., Davis, R., Lorenc, A., Chan, J. N. E., Ryan, S., Bugallo-Blanco, E., Yorke, R., Kamdar, S., Fish, M., ... Irshad, S. (2021). Acute immune signatures and their legacies in severe acute respiratory syndrome coronavirus-2 infected cancer patients. CANCER CELL, 39(2), 257-275.e6. https://doi.org/10.1016/j.ccell.2021.01.001

@article{6606279cfa814dd4874c67b8e8c82ab8,

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

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. ",

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

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: {\textcopyright} 2021 Copyright: Copyright 2021 Elsevier B.V., All rights reserved.",

year = "2021",

month = feb,

day = "8",

doi = "10.1016/j.ccell.2021.01.001",

language = "English",

volume = "39",

pages = "257--275.e6",

journal = "CANCER CELL",

issn = "1535-6108",

publisher = "Cell Press",

number = "2",

}

Abdul-Jawad, S, Baù, L, Alaguthurai, T, Del Molino Del Barrio, I, Laing, AG , Hayday, TS, Monin, L, Muñoz-Ruiz, M, McDonald, L, Francos Quijorna, I, McKenzie, D, Davis, R, Lorenc, A , Chan, JNE, Ryan, S, Bugallo-Blanco, E , Yorke, R , Kamdar, S , Fish, M , Zlatareva, I , Vantourout, P , Jennings, A , Gee, S , Doores, K, Bailey, K, Hazell, S, De Naurois, J, Moss, C , Russell, B, Khan, AA, Rowley, M, Benjamin, R , Enting, D, Alrifai, D, Wu, Y, Zhou, Y, Barber, P , Ng, T , Spicer, J , Van Hemelrijck, M, Kumar, M, Vidler, J, Lwin, Y, Fields, P , Karagiannis, SN, Coolen, ACC, Rigg, A, Papa, S , Hayday, AC , Patten, PEM & Irshad, S 2021, 'Acute immune signatures and their legacies in severe acute respiratory syndrome coronavirus-2 infected cancer patients', CANCER CELL, vol. 39, no. 2, pp. 257-275.e6. https://doi.org/10.1016/j.ccell.2021.01.001

TY - JOUR

T1 - Acute immune signatures and their legacies in severe acute respiratory syndrome coronavirus-2 infected cancer patients

AU - Abdul-Jawad, Sultan

AU - Baù, Luca

AU - Alaguthurai, Thanussuyah

AU - Del Molino Del Barrio, Irene

AU - Laing, Adam G

AU - Hayday, Thomas S

AU - Monin, Leticia

AU - Muñoz-Ruiz, Miguel

AU - McDonald, Louisa

AU - Francos Quijorna, Isaac

AU - McKenzie, Duncan

AU - Davis, Richard

AU - Lorenc, Anna

AU - Chan, Julie Nuo En

AU - Ryan, Sarah

AU - Bugallo-Blanco, Eva

AU - Yorke, Rozalyn

AU - Kamdar, Shraddha

AU - Fish, Matthew

AU - Zlatareva, Iva

AU - Vantourout, Pierre

AU - Jennings, Aislinn

AU - Gee, Sarah

AU - Doores, Katie

AU - Bailey, Katharine

AU - Hazell, Sophie

AU - De Naurois, Julien

AU - Moss, Charlotte

AU - Russell, Beth

AU - Khan, Aadil A

AU - Rowley, Mark

AU - Benjamin, Reuben

AU - Enting, Deborah

AU - Alrifai, Doraid

AU - Wu, Yin

AU - Zhou, You

AU - Barber, Paul

AU - Ng, Tony

AU - Spicer, James

AU - Van Hemelrijck, Mieke

AU - Kumar, Mayur

AU - Vidler, Jennifer

AU - Lwin, Yadanar

AU - Fields, Paul

AU - Karagiannis, Sophia N

AU - Coolen, Anthony C C

AU - Rigg, Anne

AU - Papa, Sophie

AU - Hayday, Adrian C

AU - Patten, Piers E M

AU - Irshad, Sheeba

N1 - 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.

PY - 2021/2/8

Y1 - 2021/2/8

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85099635256&partnerID=8YFLogxK

U2 - 10.1016/j.ccell.2021.01.001

DO - 10.1016/j.ccell.2021.01.001

M3 - Article

C2 - 33476581

SN - 1535-6108

VL - 39

SP - 257-275.e6

JO - CANCER CELL

JF - CANCER CELL

IS - 2

ER -

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

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