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

Cancer Cell. 2021 Feb 8;39(2):257-275.e6. doi: 10.1016/j.ccell.2021.01.001. Epub 2021 Jan 5.

Authors

Sultan Abdul-Jawad¹, Luca Baù², Thanussuyah Alaguthurai³, Irene Del Molino Del Barrio⁴, Adam G Laing⁵, Thomas S Hayday⁵, Leticia Monin⁶, Miguel Muñoz-Ruiz⁶, Louisa McDonald⁷, Isaac Francos Quijorna⁸, Duncan McKenzie⁶, Richard Davis⁵, Anna Lorenc⁵, Julie Nuo En Chan¹, Sarah Ryan⁹, Eva Bugallo-Blanco¹, Rozalyn Yorke⁹, Shraddha Kamdar⁵, Matthew Fish¹⁰, Iva Zlatareva⁵, Pierre Vantourout⁵, Aislinn Jennings¹⁰, Sarah Gee⁵, Katie Doores¹¹, Katharine Bailey¹², Sophie Hazell¹², Julien De Naurois¹³, Charlotte Moss¹⁴, Beth Russell¹⁴, Aadil A Khan¹⁵, Mark Rowley¹⁶, Reuben Benjamin¹⁷, Deborah Enting¹⁴, Doraid Alrifai¹³, Yin Wu¹⁸, You Zhou¹⁹, Paul Barber¹, Tony Ng¹, James Spicer¹, Mieke Van Hemelrijck¹⁴, Mayur Kumar²⁰, Jennifer Vidler²¹, Yadanar Lwin²¹, Paul Fields²², Sophia N Karagiannis²³, Anthony C C Coolen²⁴, Anne Rigg¹³, Sophie Papa²⁵, Adrian C Hayday²⁶, Piers E M Patten²⁷, Sheeba Irshad²⁸

Affiliations

¹ School of Cancer & Pharmaceutical Sciences, King's College London, London, UK.
² Institute of Biomedical Engineering, University of Oxford, Oxford, UK.
³ School of Cancer & Pharmaceutical Sciences, King's College London, London, UK; Breast Cancer Now Research Unit, King's College London, London, UK.
⁴ Cancer Immunotherapy Accelerator, UCL Cancer Institute, University College and King's College, London, UK; Peter Gorer Department of Immunobiology, King's College London, London, UK.
⁵ Peter Gorer Department of Immunobiology, King's College London, London, UK.
⁶ The Francis Crick Institute, London, UK.
⁷ Oncology and Haematology Clinical Trials (OHCT), Guy's and St Thomas' NHS Foundation Trust, London UK.
⁸ Wolfson Centre for Age-Related Diseases, IoPPN, King's College London, London, UK.
⁹ Department of Inflammation Biology, King's College London, London, UK.
¹⁰ Peter Gorer Department of Immunobiology, King's College London, London, UK; Department of Intensive Care Medicine, Guy's and St Thomas' NHS Foundation Trust, London, UK.
¹¹ Department of Infectious Diseases, King's College London, London, UK.
¹² Department of Haematology, Guy's and St Thomas' NHS Foundation trust, London, UK.
¹³ Department of Medical Oncology Guy's and St Thomas' NHS Foundation Trust, London, UK.
¹⁴ Department of Translational Oncology & Urology Research (TOUR), King's College London, London, UK.
¹⁵ Targeted Therapy Team, The Institute of Cancer Research, London, UK.
¹⁶ London Institute for Mathematical Sciences, Mayfair, London, UK; Saddle Point Science Ltd, London, UK.
¹⁷ School of Cancer & Pharmaceutical Sciences, King's College London, London, UK; Department of Haematological Medicine, King's College Hospital, London, UK.
¹⁸ School of Cancer & Pharmaceutical Sciences, King's College London, London, UK; Cancer Immunotherapy Accelerator, UCL Cancer Institute, University College and King's College, London, UK; Peter Gorer Department of Immunobiology, King's College London, London, UK; The Francis Crick Institute, London, UK.
¹⁹ Systems Immunity University Research Institute and Division of Infection and Immunity, Cardiff University, Cardiff, UK.
²⁰ Department of Gastroenterology, Princess Royal University Hospital, Kent, UK.
²¹ Department of Haematological Medicine, King's College Hospital, London, UK.
²² School of Cancer & Pharmaceutical Sciences, King's College London, London, UK; Department of Haematology, Guy's and St Thomas' NHS Foundation trust, London, UK.
²³ Breast Cancer Now Research Unit, King's College London, London, UK; St. John's Institute of Dermatology, King's College London, London, UK; NIHR Biomedical Research Centre, and King's College London, London, UK.
²⁴ Targeted Therapy Team, The Institute of Cancer Research, London, UK; London Institute for Mathematical Sciences, Mayfair, London, UK; Saddle Point Science Ltd, London, UK; Department of Biophysics, Radboud University, Nijmegen, The Netherlands.
²⁵ School of Cancer & Pharmaceutical Sciences, King's College London, London, UK; Department of Medical Oncology Guy's and St Thomas' NHS Foundation Trust, London, UK.
²⁶ Peter Gorer Department of Immunobiology, King's College London, London, UK; The Francis Crick Institute, London, UK.
²⁷ School of Cancer & Pharmaceutical Sciences, King's College London, London, UK; Department of Haematological Medicine, King's College Hospital, London, UK; Medical Research Council (MRC) Clinical Academic Research Partnership, London, UK.
²⁸ School of Cancer & Pharmaceutical Sciences, King's College London, London, UK; Breast Cancer Now Research Unit, King's College London, London, UK; Department of Medical Oncology Guy's and St Thomas' NHS Foundation Trust, London, UK; Cancer Research UK (CRUK) Clinician Scientist, London, UK. Electronic address: sheeba.irshad@kcl.ac.uk.

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.

Keywords: COVID-19; SARS-CoV-2; antibodies; cancer; hemato-oncological; immune; seroconversion; vaccine; virus shedding.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Adult
Aged
Aged, 80 and over
COVID-19 / etiology
COVID-19 / immunology*
COVID-19 / mortality
Female
Hematologic Neoplasms / immunology
Hematologic Neoplasms / mortality
Hematologic Neoplasms / therapy
Hematologic Neoplasms / virology
Humans
Immunophenotyping
Male
Middle Aged
Nasopharynx / virology
Neoplasms / immunology*
Neoplasms / mortality
Neoplasms / therapy
Neoplasms / virology*
Severe Acute Respiratory Syndrome / etiology
Severe Acute Respiratory Syndrome / immunology*
Severe Acute Respiratory Syndrome / mortality
Severe Acute Respiratory Syndrome / virology
T-Lymphocytes / virology
Virus Shedding
Young Adult

Abstract

Publication types

MeSH terms

Grants and funding