Humoral and cellular responses to SARS-CoV-2 in patients with B-cell haematological malignancies improve with successive vaccination

Patients with haematological malignancies are more likely to have poor responses to vaccination. Here we provide detailed analysis of the humoral and cellular responses to COVID-19 vaccination in 69 patients with B-cell malignancies. Measurement of anti-spike IgG in serum demonstrated a low seroconv...

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Published in	British journal of haematology Vol. 202; no. 6; pp. 1091 - 1103
Main Authors	Pinder, Christopher L, Jankovic, Dylan, Fox, Thomas A, Kirkwood, Amy, Enfield, Louise, Alrubayyi, Aljawharah, Touizer, Emma, Ford, Rosemarie, Pocock, Rachael, Shin, Jin-Sup, Ziegler, Joseph, Thomson, Kirsty J, Ardeshna, Kirit M, Peppa, Dimitra, McCoy, Laura E, Morris, Emma C
Format	Journal Article
Language	English
Published	England Blackwell Publishing Ltd 01.09.2023 John Wiley and Sons Inc
Subjects	Antibodies, Viral Cell size COVID-19 COVID-19 - prevention & control COVID-19 Vaccines Enzyme-linked immunosorbent assay Flow cytometry Hematologic Neoplasms - therapy Hematology Humans Immunization Immunoglobulin G Malignancy Original Paper SARS-CoV-2 Seroconversion Severe acute respiratory syndrome coronavirus 2 Vaccination haematological malignancies infection antibodies B cells T cells vaccines
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Abstract	Patients with haematological malignancies are more likely to have poor responses to vaccination. Here we provide detailed analysis of the humoral and cellular responses to COVID-19 vaccination in 69 patients with B-cell malignancies. Measurement of anti-spike IgG in serum demonstrated a low seroconversion rate with 27.1% and 46.8% of patients seroconverting after the first and second doses of vaccine, respectively. In vitro pseudoneutralisation assays demonstrated a poor neutralising response, with 12.5% and 29.5% of patients producing a measurable neutralising titre after the first and second doses, respectively. A third dose increased seropositivity to 54.3% and neutralisation to 51.5%, while a fourth dose further increased both seropositivity and neutralisation to 87.9%. Neutralisation titres post-fourth dose showed a positive correlation with the size of the B-cell population measured by flow cytometry, suggesting an improved response correlating with recovery of the B-cell compartment after B-cell depletion treatments. In contrast, interferon gamma ELISpot analysis showed a largely intact T-cell response, with the percentage of patients producing a measurable response boosted by the second dose to 75.5%. This response was maintained thereafter, with only a small increase following the third and fourth doses, irrespective of the serological response at these timepoints.
AbstractList	Patients with haematological malignancies are more likely to have poor responses to vaccination. Here we provide detailed analysis of the humoral and cellular responses to COVID‐19 vaccination in 69 patients with B‐cell malignancies. Measurement of anti‐spike IgG in serum demonstrated a low seroconversion rate with 27.1% and 46.8% of patients seroconverting after the first and second doses of vaccine, respectively. In vitro pseudoneutralisation assays demonstrated a poor neutralising response, with 12.5% and 29.5% of patients producing a measurable neutralising titre after the first and second doses, respectively. A third dose increased seropositivity to 54.3% and neutralisation to 51.5%, while a fourth dose further increased both seropositivity and neutralisation to 87.9%. Neutralisation titres post‐fourth dose showed a positive correlation with the size of the B‐cell population measured by flow cytometry, suggesting an improved response correlating with recovery of the B‐cell compartment after B‐cell depletion treatments. In contrast, interferon gamma ELISpot analysis showed a largely intact T‐cell response, with the percentage of patients producing a measurable response boosted by the second dose to 75.5%. This response was maintained thereafter, with only a small increase following the third and fourth doses, irrespective of the serological response at these timepoints. Patients with haematological malignancies are more likely to have poor responses to vaccination. Here we provide detailed analysis of the humoral and cellular responses to COVID‐19 vaccination in 69 patients with B‐cell malignancies. Measurement of anti‐spike IgG in serum demonstrated a low seroconversion rate with 27.1% and 46.8% of patients seroconverting after the first and second doses of vaccine, respectively. In vitro pseudoneutralisation assays demonstrated a poor neutralising response, with 12.5% and 29.5% of patients producing a measurable neutralising titre after the first and second doses, respectively. A third dose increased seropositivity to 54.3% and neutralisation to 51.5%, while a fourth dose further increased both seropositivity and neutralisation to 87.9%. Neutralisation titres post‐fourth dose showed a positive correlation with the size of the B‐cell population measured by flow cytometry, suggesting an improved response correlating with recovery of the B‐cell compartment after B‐cell depletion treatments. In contrast, interferon gamma ELISpot analysis showed a largely intact T‐cell response, with the percentage of patients producing a measurable response boosted by the second dose to 75.5%. This response was maintained thereafter, with only a small increase following the third and fourth doses, irrespective of the serological response at these timepoints. Patients with haematological malignancies often present with immune dysfunction which increases the likelihood of a poor response to vaccination. Our analysis of both the humoral and cellular immune response to repeated SARS‐CoV‐2 immunisation shows a low antibody binding and neutralising response at early timepoints. However, this improves with successive doses, correlating with recovery of the B‐cell compartment following cessation of B‐cell‐depleting therapy. In contrast, the T‐cell response is largely intact and maintained thereafter, with small boosts in magnitude following the third and fourth doses. Summary Patients with haematological malignancies are more likely to have poor responses to vaccination. Here we provide detailed analysis of the humoral and cellular responses to COVID‐19 vaccination in 69 patients with B‐cell malignancies. Measurement of anti‐spike IgG in serum demonstrated a low seroconversion rate with 27.1% and 46.8% of patients seroconverting after the first and second doses of vaccine, respectively. In vitro pseudoneutralisation assays demonstrated a poor neutralising response, with 12.5% and 29.5% of patients producing a measurable neutralising titre after the first and second doses, respectively. A third dose increased seropositivity to 54.3% and neutralisation to 51.5%, while a fourth dose further increased both seropositivity and neutralisation to 87.9%. Neutralisation titres post‐fourth dose showed a positive correlation with the size of the B‐cell population measured by flow cytometry, suggesting an improved response correlating with recovery of the B‐cell compartment after B‐cell depletion treatments. In contrast, interferon gamma ELISpot analysis showed a largely intact T‐cell response, with the percentage of patients producing a measurable response boosted by the second dose to 75.5%. This response was maintained thereafter, with only a small increase following the third and fourth doses, irrespective of the serological response at these timepoints.
Author	Ziegler, Joseph Pinder, Christopher L McCoy, Laura E Shin, Jin-Sup Jankovic, Dylan Alrubayyi, Aljawharah Peppa, Dimitra Pocock, Rachael Ardeshna, Kirit M Touizer, Emma Fox, Thomas A Ford, Rosemarie Kirkwood, Amy Thomson, Kirsty J Morris, Emma C Enfield, Louise
AuthorAffiliation	1 Division of Infection and Immunity University College London London UK 3 CR UK and UCL Cancer Trials Centre UCL Cancer Institute, UCL London UK 2 Department of Clinical Haematology University College London Hospitals, NHS Foundation Trust London UK
AuthorAffiliation_xml	– name: 2 Department of Clinical Haematology University College London Hospitals, NHS Foundation Trust London UK – name: 1 Division of Infection and Immunity University College London London UK – name: 3 CR UK and UCL Cancer Trials Centre UCL Cancer Institute, UCL London UK
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Snippet	Patients with haematological malignancies are more likely to have poor responses to vaccination. Here we provide detailed analysis of the humoral and cellular... Summary Patients with haematological malignancies are more likely to have poor responses to vaccination. Here we provide detailed analysis of the humoral and...
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SubjectTerms	Antibodies, Viral Cell size COVID-19 COVID-19 - prevention & control COVID-19 Vaccines Enzyme-linked immunosorbent assay Flow cytometry Hematologic Neoplasms - therapy Hematology Humans Immunization Immunoglobulin G Malignancy Original Paper SARS-CoV-2 Seroconversion Severe acute respiratory syndrome coronavirus 2 Vaccination
Title	Humoral and cellular responses to SARS-CoV-2 in patients with B-cell haematological malignancies improve with successive vaccination
URI	https://www.ncbi.nlm.nih.gov/pubmed/37402627 https://www.proquest.com/docview/2863186977 https://search.proquest.com/docview/2833646641 https://pubmed.ncbi.nlm.nih.gov/PMC10953351
Volume	202
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