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[Preprint]. 2021 Sep 20:rs.3.rs-916427.

doi: 10.21203/rs.3.rs-916427/v1.

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

Annika Fendler^{1

2}, Lewis Au^{1

3

2}, Scott T C Shepherd^{1

3

2}, Fiona Byrne¹, Maddalena Cerrone^{4

5}, Laura Amanda Boos³, Karolina Rzeniewicz¹, William Gordon¹, Ben Shum^{1

3}, Camille L Gerard¹, Barry Ward¹, Wenyi Xie¹, Andreas M Schmitt³, Nalinie Joharatnam-Hogan³, Georgina H Cornish⁶, Martin Pule^{7

8}, Leila Mekkaoui⁸, Kevin W Ng⁶, Eleanor Carlyle³, Kim Edmonds³, Lyra Del Rosario³, Sarah Sarker³, Karla Lingard³, Mary Mangwende³, Lucy Holt³, Hamid Ahmod³, Richard Stone⁸, Camila Gomes⁸, Helen R Flynn⁹, Ana Agua-Doce¹⁰, Philip Hobson¹⁰, Simon Caidan¹¹, Michael Howell¹², Mary Wu¹², Robert Goldstone¹³, Margaret Crawford¹³, Laura Cubitt¹³, Harshil Patel¹⁴, Mike Gavrielides¹⁵, Emma Nye¹⁶, Ambrosius P Snijders⁹, James I MacRae¹⁷, Jerome Nicod¹³, Firza Gronthoud¹⁸, Robyn L Shea^{18

19}, Christina Messiou²⁰, David Cunningham²¹, Ian Chau²¹, Naureen Starling²¹, Nicholas Turner²², Liam Welsh²³, Nicholas van As²⁴, Robin L Jones²⁵, Joanne Droney²⁶, Susana Banerjee²⁷, Kate C Tatham²⁸, Shaman Jhanji²⁸, Mary O'Brien²⁹, Olivia Curtis²⁹, Kevin Harrington^{30

31}, Shreerang Bhide³⁰, Jessica Bazin³², Anna Robinson³², Clemency Stephenson³², Tim Slattery³, Yasir Khan³, Zayd Tippu³, Isla Leslie³, Spyridon Gennatas^{33

34}, Alicia Okines^{22

33}, Alison Reid³⁵, Kate Young³, Andrew J S Furness³, Lisa Pickering³, Sonia Gandhi^{36

37}, Steve Gamblin³⁸, Charles Swanton^{39

40}, Emma Nicholson³², Sacheen Kumar²¹, Nadia Yousaf^{29

33}, Katalin A Wilkinson^{4

41}, Anthony Swerdlow⁴², Ruth Harvey⁴³, George Kassiotis⁶, James Larkin³, Robert J Wilkinson^{4

5

41}, Samra Turajlic^{1

3}

Affiliations

¹ Cancer Dynamics Laboratory, The Francis Crick Institute, London, NW1 1AT, UK.
² Equal contribution.
³ Skin and Renal Units, The Royal Marsden NHS Foundation Trust, London, SW3 6JJ, UK.
⁴ Tuberculosis Laboratory, The Francis Crick Institute, London, NW1 1AT, UK.
⁵ Department of Infectious Disease, Imperial College London, W12 0NN, UK.
⁶ Retroviral Immunology Laboratory, The Francis Crick Institute, London, NW1 1AT, UK.
⁷ Research Department of Haematology at University College London Cancer Institute, WC1E 6DD, London, UK.
⁸ Autolus Limited, The MediaWorks, 191 Wood Lane, London, W12 7F.
⁹ Mass Spectrometry Proteomics Science Technology Platform, The Francis Crick Institute, London, NW1 1AT, UK.
¹⁰ Flow Cytometry Scientific Technology Platform, The Francis Crick Institute, London, NW1 1AT, UK.
¹¹ Safety, Health & Sustainability, The Francis Crick Institute, London, NW1 1AT, UK.
¹² High Throughput Screening Laboratory, The Francis Crick Institute, London, NW1 1AT, UK.
¹³ Advanced Sequencing Facility, The Francis Crick Institute, London, NW1 1AT, UK.
¹⁴ Department of Bioinformatics and Biostatistics, The Francis Crick Institute, London, UK.
¹⁵ Scientific Computing Scientific Technology Platform, The Francis Crick Institute, London, NW1 1AT, UK.
¹⁶ Experimental Histopathology Laboratory, The Francis Crick Institute, London, NW1 1AT, UK.
¹⁷ Metabolomics Scientific Technology Platform, The Francis Crick Institute, London, NW1 1AT, UK.
¹⁸ Department of Pathology, The Royal Marsden NHS Foundation Trust, London, NW1 1AT, UK.
¹⁹ Translational Cancer Biochemistry Laboratory, The Institute of Cancer Research, London, SW7 3RP, UK.
²⁰ Department of Radiology, The Royal Marsden NHS Foundation Trust, London, SW3 6JJ, UK.
²¹ Gastrointestinal Unit, The Royal Marsden NHS Foundation Trust, London and Surrey SM2 5PT.
²² Breast Unit, The Royal Marsden NHS Foundation Trust, London, SW3 6JJ, UK.
²³ Neuro-oncology Unit, The Royal Marsden NHS Foundation Trust, London, SW3 6JJ, UK.
²⁴ Clinical Oncology Unit, The Royal Marsden NHS Foundation Trust, London, SW3 6JJ, UK.
²⁵ Sarcoma Unit, The Royal Marsden NHS Foundation Trust and Institute of Cancer Research, London, SW3 6JJ, UK.
²⁶ Palliative Medicine, The Royal Marsden NHS Foundation Trust, London, SW3 6JJ, UK.
²⁷ Gynaecology Unit, The Royal Marsden NHS Foundation Trust, London, SW3 6JJ, UK.
²⁸ Anaesthetics, Perioperative Medicine and Pain Department, The Royal Marsden NHS Foundation Trust, London, SW3 6JJ, UK.
²⁹ Lung Unit, The Royal Marsden NHS Foundation Trust, London, SW3 6JJ, UK.
³⁰ Head and Neck, The Royal Marsden NHS Foundation Trust, London, SW3 6JJ, UK.
³¹ Targeted Therapy Team, The Institute of Cancer Research, London, SW7 3RP, UK.
³² Haemato-oncology Unit, The Royal Marsden NHS Foundation Trust, London, SW3 6JJ, UK.
³³ Acute Oncology Service, The Royal Marsden NHS Foundation Trust, London, SW3 6JJ, UK.
³⁴ Department of Medical Oncology, 14th Floor, Great Maze Pond Road, Tower Wing, Guy's Hospital, London SE1 9RY, UK.
³⁵ Uro-oncology unit, The Royal Marsden NHS Foundation Trust, Surrey, SM2 5PT.
³⁶ Neurodegeneration Biology Laboratory, The Francis Crick Institute, London, NW1 1AT, UK.
³⁷ UCL Queen Square Institute of Neurology, Queen Square, London WC1N 3BG.
³⁸ Structural Biology of Disease Processes Laboratory, The Francis Crick Institute, London, NW1 1AT, UK.
³⁹ Cancer Evolution and Genome Instability Laboratory, The Francis Crick Institute, London, NW1 1AT, UK.
⁴⁰ University College London Cancer Institute, London WC1E 6DD, UK.
⁴¹ Wellcome Center for Infectious Disease Research in Africa, University Cape Town, Observatory 7925, Republic of South Africa.
⁴² Division of Genetics and Epidemiology and Division of Breast Cancer Research, The Institute of Cancer Research, London, SW7 3RP, UK.
⁴³ Worldwide Influenza Centre, The Francis Crick Institute, London, NW1 1AT, UK.

PMID: 34580668
PMCID: PMC8475970
DOI: 10.21203/rs.3.rs-916427/v1

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

Annika Fendler et al. Res Sq. 2021.

[Preprint]. 2021 Sep 20:rs.3.rs-916427.

doi: 10.21203/rs.3.rs-916427/v1.

Authors

Affiliations

¹ Cancer Dynamics Laboratory, The Francis Crick Institute, London, NW1 1AT, UK.
² Equal contribution.
³ Skin and Renal Units, The Royal Marsden NHS Foundation Trust, London, SW3 6JJ, UK.
⁴ Tuberculosis Laboratory, The Francis Crick Institute, London, NW1 1AT, UK.
⁵ Department of Infectious Disease, Imperial College London, W12 0NN, UK.
⁶ Retroviral Immunology Laboratory, The Francis Crick Institute, London, NW1 1AT, UK.
⁷ Research Department of Haematology at University College London Cancer Institute, WC1E 6DD, London, UK.
⁸ Autolus Limited, The MediaWorks, 191 Wood Lane, London, W12 7F.
⁹ Mass Spectrometry Proteomics Science Technology Platform, The Francis Crick Institute, London, NW1 1AT, UK.
¹⁰ Flow Cytometry Scientific Technology Platform, The Francis Crick Institute, London, NW1 1AT, UK.
¹¹ Safety, Health & Sustainability, The Francis Crick Institute, London, NW1 1AT, UK.
¹² High Throughput Screening Laboratory, The Francis Crick Institute, London, NW1 1AT, UK.
¹³ Advanced Sequencing Facility, The Francis Crick Institute, London, NW1 1AT, UK.
¹⁴ Department of Bioinformatics and Biostatistics, The Francis Crick Institute, London, UK.
¹⁵ Scientific Computing Scientific Technology Platform, The Francis Crick Institute, London, NW1 1AT, UK.
¹⁶ Experimental Histopathology Laboratory, The Francis Crick Institute, London, NW1 1AT, UK.
¹⁷ Metabolomics Scientific Technology Platform, The Francis Crick Institute, London, NW1 1AT, UK.
¹⁸ Department of Pathology, The Royal Marsden NHS Foundation Trust, London, NW1 1AT, UK.
¹⁹ Translational Cancer Biochemistry Laboratory, The Institute of Cancer Research, London, SW7 3RP, UK.
²⁰ Department of Radiology, The Royal Marsden NHS Foundation Trust, London, SW3 6JJ, UK.
²¹ Gastrointestinal Unit, The Royal Marsden NHS Foundation Trust, London and Surrey SM2 5PT.
²² Breast Unit, The Royal Marsden NHS Foundation Trust, London, SW3 6JJ, UK.
²³ Neuro-oncology Unit, The Royal Marsden NHS Foundation Trust, London, SW3 6JJ, UK.
²⁴ Clinical Oncology Unit, The Royal Marsden NHS Foundation Trust, London, SW3 6JJ, UK.
²⁵ Sarcoma Unit, The Royal Marsden NHS Foundation Trust and Institute of Cancer Research, London, SW3 6JJ, UK.
²⁶ Palliative Medicine, The Royal Marsden NHS Foundation Trust, London, SW3 6JJ, UK.
²⁷ Gynaecology Unit, The Royal Marsden NHS Foundation Trust, London, SW3 6JJ, UK.
²⁸ Anaesthetics, Perioperative Medicine and Pain Department, The Royal Marsden NHS Foundation Trust, London, SW3 6JJ, UK.
²⁹ Lung Unit, The Royal Marsden NHS Foundation Trust, London, SW3 6JJ, UK.
³⁰ Head and Neck, The Royal Marsden NHS Foundation Trust, London, SW3 6JJ, UK.
³¹ Targeted Therapy Team, The Institute of Cancer Research, London, SW7 3RP, UK.
³² Haemato-oncology Unit, The Royal Marsden NHS Foundation Trust, London, SW3 6JJ, UK.
³³ Acute Oncology Service, The Royal Marsden NHS Foundation Trust, London, SW3 6JJ, UK.
³⁴ Department of Medical Oncology, 14th Floor, Great Maze Pond Road, Tower Wing, Guy's Hospital, London SE1 9RY, UK.
³⁵ Uro-oncology unit, The Royal Marsden NHS Foundation Trust, Surrey, SM2 5PT.
³⁶ Neurodegeneration Biology Laboratory, The Francis Crick Institute, London, NW1 1AT, UK.
³⁷ UCL Queen Square Institute of Neurology, Queen Square, London WC1N 3BG.
³⁸ Structural Biology of Disease Processes Laboratory, The Francis Crick Institute, London, NW1 1AT, UK.
³⁹ Cancer Evolution and Genome Instability Laboratory, The Francis Crick Institute, London, NW1 1AT, UK.
⁴⁰ University College London Cancer Institute, London WC1E 6DD, UK.
⁴¹ Wellcome Center for Infectious Disease Research in Africa, University Cape Town, Observatory 7925, Republic of South Africa.
⁴² Division of Genetics and Epidemiology and Division of Breast Cancer Research, The Institute of Cancer Research, London, SW7 3RP, UK.
⁴³ Worldwide Influenza Centre, The Francis Crick Institute, London, NW1 1AT, UK.

PMID: 34580668
PMCID: PMC8475970
DOI: 10.21203/rs.3.rs-916427/v1

Update in

Functional antibody and T cell immunity following SARS-CoV-2 infection, including by variants of concern, in patients with cancer: the CAPTURE study.
Fendler A, Au L, Shepherd STC, Byrne F, Cerrone M, Boos LA, Rzeniewicz K, Gordon W, Shum B, Gerard CL, Ward B, Xie W, Schmitt AM, Joharatnam-Hogan N, Cornish GH, Pule M, Mekkaoui L, Ng KW, Carlyle E, Edmonds K, Rosario LD, Sarker S, Lingard K, Mangwende M, Holt L, Ahmod H, Stone R, Gomes C, Flynn HR, Agua-Doce A, Hobson P, Caidan S, Howell M, Wu M, Goldstone R, Crawford M, Cubitt L, Patel H, Gavrielides M, Nye E, Snijders AP, MacRae JI, Nicod J, Gronthoud F, Shea RL, Messiou C, Cunningham D, Chau I, Starling N, Turner N, Welsh L, van As N, Jones RL, Droney J, Banerjee S, Tatham KC, Jhanji S, O'Brien M, Curtis O, Harrington K, Bhide S, Bazin J, Robinson A, Stephenson C, Slattery T, Khan Y, Tippu Z, Leslie I, Gennatas S, Okines A, Reid A, Young K, Furness AJS, Pickering L, Gandhi S, Gamblin S, Swanton C; Crick COVID-19 Consortium; Nicholson E, Kumar S, Yousaf N, Wilkinson KA, Swerdlow A, Harvey R, Kassiotis G, Larkin J, Wilkinson RJ, Turajlic S; CAPTURE consortium. Fendler A, et al. Nat Cancer. 2021 Dec;2(12):1321-1337. doi: 10.1038/s43018-021-00275-9. Epub 2021 Oct 27. Nat Cancer. 2021. PMID: 35121900

Abstract

Patients with cancer have higher COVID-19 morbidity and mortality. Here we present the prospective CAPTURE study (NCT03226886) integrating longitudinal immune profiling with clinical annotation. Of 357 patients with cancer, 118 were SARS-CoV-2-positive, 94 were symptomatic and 2 patients died of COVID-19. In this cohort, 83% patients had S1-reactive antibodies, 82% had neutralizing antibodies against WT, whereas neutralizing antibody titers (NAbT) against the Alpha, Beta, and Delta variants were substantially reduced. Whereas S1-reactive antibody levels decreased in 13% of patients, NAbT remained stable up to 329 days. Patients also had detectable SARS-CoV-2-specific T cells and CD4+ responses correlating with S1-reactive antibody levels, although patients with hematological malignancies had impaired immune responses that were disease and treatment-specific, but presented compensatory cellular responses, further supported by clinical. Overall, these findings advance the understanding of the nature and duration of immune response to SARS-CoV-2 in patients with cancer.

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Figures

**Figure 1:. SARS-CoV-2 infection status, viral shedding, and COVID-19 symptoms of recruited patients.**
a) Patients with cancer irrespective of cancer type, stage, or treatment were recruited. Follow-up schedules for patients with cancer were bespoke to their COVID-19 status and account for their clinical schedules (inpatients: every 2 – 14 days; outpatients: every clinical visit maximum every 3–6 weeks in year one and every six months in year two, and at the start of every or every-second cycle of treatment). Clinical data, oronasopharyngeal swabs and blood were collected at each study visit. Viral antigen testing (RT-PCR on swabs), antibody (ELISA, flow cytometric assay), T cell response and IFN-γ activation assays were performed. b) Distribution of SARS-CoV-2 infection, and S1-reactive Ab status and COVID-19 severity in patients with cancer. 357 patients with cancer were recruited between May 4, 2020 and March 31st 2021. SARS-CoV-2 infection status by RT-PCR and S1-reactive Ab were analysed at recruitment and in serial samples. RT-PCR results prior to recruitment were extracted from electronic patient records. COVID-19 case definition includes all patients with either RT-PCR confirmed SARS-CoV-2 infection or S1-reactive Ab. c) Viral shedding in 43 patients with serial positive swabs. Solid bars indicate time to the last positive test, dotted lines denote the time from the last positive test to the first negative test. d) Distribution of symptoms in 118 COVID-19 patients. Bar graph denotes the number of patients. Each row in the lower graph denotes one patient. ONP, Oronasopharyngeal; ELISA, enzyme-linked immunoassay; PBMCs, peripheral blood mononuclear cells; WGS - whole genome sequencing, RTx, radiotherapy, HSCT, human stem cell transplant.

**Figure 2:. S1-reactive and antibody response in patients with cancer**
a) S1-reactive AbT by COVID-19 severity (n=112 patients). Significance was tested by Kruskal-Wallis test, p = 0.074. b) S1-reactive AbT by cancer type (Solid patients: n= 92, Haematological patients: n=20). Significance was tested by two-sided Wilcoxon Wilcoxon-Mann-Whitney U test, p = 0.011. c) NAbT by COVID-19 severity (n=112 patients). Significance was tested by Kruskal-Wallis test, p = 0.0027. d) NAbT by cancer type (Solid patient: n= 92, Haematological patients: n=20). Significance was tested by two-sided Wilcoxon-Mann-Whitney U test, p = 0.052. Boxes indicate 25 and 75 percentiles, line indicates median, and whiskers indicate 1.5 times the IQR. Dots represent individual samples. Dotted lines and grey boxes denote the limit of detection. e) Multivariate binary logistic regression evaluating association with lack of NAb in patients with cancer (n=112). Wald z-statistic was used two calculate two-sided p-values. *, p = 0.038. f) Multivariate binary logistic regression evaluating the association of lack of NAb in patients with solid cancer (n = 92). g) Multivariate binary logistic regression evaluating the association of lack of NAb in patients with solid cancer (n = 92). Dot denotes odds ratio (blue, positive odds ratio; red, negative odds ratio); whiskers indicate 1.5 times the IQR. h) NAbT against WT, Alpha, Beta, and Delta VOCs in patients (n=112) infected with WT SARS-CoV-2 or Alpha VOC. Violin plots denote density of data points. PointRange denotes median and 25 and 75 percentiles. Dots represent individual samples. Significance was tested by Kruskal Wallis test, p = 3.5e-07, two-sided Wilcoxon Mann Whitney U-test with Bonferroni correction (post-hoc test) was used for pairwise comparisons. p-values are denoted in the graph. i) S1-reactive AbT and j) NAbT post onset of disease (n=97 patients). Blue line denotes loess regression line with 95% confidence bands in grey. Black dots denote patients with one sample, coloured dots denote patients with serial samples (n=51 patients). Samples from individual patients are connected. Dotted lines and grey areas at bottom indicate limit of detection. NAb, neutralising antibody, NAbT, neutralising antibody titres, AbT, Antibody titres.

**Figure 3:. T cell response in patients with cancer**
**a,b)** Representative plots of CD4⁺CD137⁺OX40⁺ (CD4⁺) and CD8⁺CD137⁺CD69⁺ (CD8⁺) T cells in a patient with confirmed COVID-19 and a cancer patient without COVID-19 after in vitro stimulation with S, M, and N peptide pools, positive control (Staphylococcal enterotoxin B, SEB) or negative control (NC). Frequency of Sars-CoV-2-specific c) CD4⁺ and d) CD8⁺ T cells in solid patients with cancer (n= 83). Frequency of Sars-CoV-2-specific e) CD4⁺ and f) CD8⁺ T cells in haematological patients with cancer (n= 21). Stimulation index was calculated by dividing the percentage of positive cells in the stimulated sample by the percentage of positive cells in the negative control (NC). To obtain the total number of SsT cells the sum of cells activated by S, M, and N was calculated (SMN). Boxes indicate the 25 and 75 percentiles, line indicates the median, and whiskers indicate 1.5 times the IQR. Individual patients are represented as dots. Dots represent individual samples. Dotted lines and grey boxes denote the limit of detection. SsT cells, Sars-CoV-2-specific T cells.

**Figure 4:. Comparison of antibody and T cell responses in patients with cancer**
a) S1-reactive AbT in patients with leukaemia (n=11), myeloma (n=4), and lymphoma (n=6). b) Neutralising antibody titres in patients with leukaemia (n=10), myeloma (n=4), and lymphoma (n=6). c) CD4⁺ and CD8⁺ cells T cells across patients with leukemia (n=10), myeloma (n=4), or lymphoma (n=6). Stimulation index was calculated by dividing the percentage of CD4⁺CD137⁺OX40⁺ (CD4⁺) and CD8⁺CD137⁺CD69⁺ (CD8⁺) T cells in the stimulated sample by the percentage of positive cells in the negative control (NC). Significance was tested by Kruskal-Wallis test, p < 0.05 was considered significant. d) S1-reactive AbT in patients with haematological malignancy receiving anti-CD20 treatment (n=6) vs other SACT (n=15). e) NAbT in patients with haematological malignancy receiving anti-CD20 treatment (n=6) vs other SACT (n=15). Significance was tested by two-sided Wilcoxon-Mann-Whitney U test, p < 0.05 was considered significant. f) Comparison of CD4⁺/CD8⁺ T cells between patients with haematological malignancies on anti-CD20 therapy (n=5, administered within six months) and not on anti-CD20 therapy (n=15). Significance was tested by two-sided Wilcoxon-Mann-Whitney U test, p < 0.05 was considered significant. g) CD4⁺ and CD8⁺ cells T cells across patients with solid cancer (n=81) by cancer subtype. Boxes indicate the 25 and 75 percentiles, line indicates the median, and whiskers indicate 1.5 times the IQR. Dots represent individual patient samples. Dotted lines and grey boxes denote the limit of detection. Significance was tested by Kruskal-Wallis test, p < 0.05 was considered significant. SACT, systemic anti-cancer therapy.

**Figure 5:. Associations between SARS-CoV-2-specific T cells with patient or cancer-specific features**
Multivariate binary logistic regression analysis evaluating associations between SARS-CoV-2-specific a) CD4⁺ and b) CD8⁺ T cells with cancer diagnosis (solid vs haematological malignancies), comorbidities, age, sex, and COVID-19 disease severity in 100 patients. Wald z-statistic was used two calculate two-sided p-values. *, p = 0.038. Multivariate binary logistic regression analysis evaluating associations between SARS-CoV-2-specific c) CD4⁺ and d) CD8⁺ T cells with anti-cancer intervention, age, sex, and COVID-19 disease severity in patients with solid cancer (n=81). Wald z-statistic was used two calculate two-sided p-values. *, p = 0.045. Dot denotes odds ratio (blue and red dots indicate positive or negative odds ratio, respectively); whiskers indicate 1.5 times the IQR. e) Comparison of SARS-CoV-2-specific CD4⁺/CD8⁺ T cells between patients with solid malignancies on CPI (n=13, administered within three months) and not on CPI (n=68). Boxes indicate the 25th and 75th percentiles, line indicates the median, and whiskers indicate 1.5 times the IQR. Dots represent individual samples. Significance was tested by two-sided Wilcoxon-Mann-Whitney U test (p = 0.038 and 0.53).

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This is a preprint.

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

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

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