Patients with treated indolent lymphomas immunized with BNT162b2 have reduced anti-spike neutralizing IgG to SARS-CoV-2 variants, but preserved antigen-specific T cell responses.

Humans Immunoglobulin G SARS-CoV-2 BNT162 Vaccine COVID-19 / prevention & control T-Lymphocytes Lymphoma, Non-Hodgkin Antibodies, Viral Antibodies, Neutralizing Vaccination

Journal

American journal of hematology
ISSN: 1096-8652
Titre abrégé: Am J Hematol
Pays: United States
ID NLM: 7610369

Informations de publication

Date de publication:
01 2023
Historique:
revised: 08 04 2022
received: 24 01 2022
accepted: 09 05 2022
pubmed: 25 5 2022
medline: 23 12 2022
entrez: 24 5 2022
Statut: ppublish

Résumé

Patients with indolent lymphoma undertaking recurrent or continuous B cell suppression are at risk of severe COVID-19. Patients and healthy controls (HC; N = 13) received two doses of BNT162b2: follicular lymphoma (FL; N = 35) who were treatment naïve (TN; N = 11) or received immunochemotherapy (ICT; N = 23) and Waldenström's macroglobulinemia (WM; N = 37) including TN (N = 9), ICT (N = 14), or treated with Bruton's tyrosine kinase inhibitors (BTKi; N = 12). Anti-spike immunoglobulin G (IgG) was determined by a high-sensitivity flow-cytometric assay, in addition to live-virus neutralization. Antigen-specific T cells were identified by coexpression of CD69/CD137 and CD25/CD134 on T cells. A subgroup (N = 29) were assessed for third mRNA vaccine response, including omicron neutralization. One month after second BNT162b2, median anti-spike IgG mean fluorescence intensity (MFI) in FL ICT patients (9977) was 25-fold lower than TN (245 898) and HC (228 255, p = .0002 for both). Anti-spike IgG correlated with lymphocyte count (r = .63; p = .002), and time from treatment (r = .56; p = .007), on univariate analysis, but only with lymphocyte count on multivariate analysis (p = .03). In the WM cohort, median anti-spike IgG MFI in BTKi patients (39 039) was reduced compared to TN (220 645, p = .0008) and HC (p < .0001). Anti-spike IgG correlated with neutralization of the delta variant (r = .62, p < .0001). Median neutralization titer for WM BTKi (0) was lower than HC (40, p < .0001) for early-clade and delta. All cohorts had functional T cell responses. Median anti-spike IgG decreased 4-fold from second to third dose (p = .004). Only 5 of 29 poor initial responders assessed after third vaccination demonstrated seroconversion and improvement in neutralization activity, including to the omicron variant.

Identifiants

DOI: 10.1002/ajh.26619 PMID: 35607995 PMC: PMC9349368
pubmed: 35607995
doi: 10.1002/ajh.26619
pmc: PMC9349368
doi:

Substances chimiques

Immunoglobulin G 0
BNT162 Vaccine 0
Antibodies, Viral 0
Antibodies, Neutralizing 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

131-139

Informations de copyright

© 2022 The Authors. American Journal of Hematology published by Wiley Periodicals LLC.

Références

Vijenthira A, Gong IY, Fox TA, et al. Outcomes of patients with hematologic malignancies and COVID-19: a systematic review and meta-analysis of 3377 patients. Blood. 2020;136(25):2881-2892.
van Doesum J, Chinea A, Pagliaro M, et al. Clinical characteristics and outcome of SARS-CoV-2-infected patients with hematological diseases: a retrospective case study in four hospitals in Italy, Spain and the Netherlands. Leukemia. 2020;34:2536-2538.
Casulo C, Barr P. How I treat early-relapsing follicular lymphoma. Blood. 2019;133(14):1540-1547.
Dimopoulos M, Tedeschi A, Trotman J, et al. Phase 3 trial of ibrutinib plus rituximab in Waldenström's macroglobulinemia. N Engl J Med. 2018;378:2399-2410.
Besson C. It is time to adapt anti-CD20 administration schedule to allow efficient anti-SARS-CoV-2 vaccination in patients with lymphoid malignancies. Haematologica. 2022;107(3):572-573. doi:10.3324/haematol.2021.279457
Douglas AP, Trubiano JA, Barr I, Leung V, Slavin MA, Tam CS. Ibrutinib may impair serological responses to influenza vaccination. Haematologica. 2017;102(10):e397-e399.
Mazza JJ, Yale SH, Arrowood JR, et al. Efficacy of the influenza vaccine in patients with malignant lymphoma. Clin Med Res. 2005;3(4):214-220.
Maneikis K, Šablauskas K, Ringeleviciute U, et al. Immunogenicity of the BNT162b2 COVID-19 mRNA vaccine and early clinical outcomes in patients with hematological malignancies in Lithuania: a national prospective cohort study. Lancet Haematol. 2021;8(8):e583-e592.
Herishanu Y, Avivi I, Aharon A, et al. Efficacy of the BNT162b2 mRNA COVID-19 vaccine in patients with chronic lymphocytic leukemia. Blood. 2021;137(23):3165-3173.
Painter MM, Mathew D, Goel RR, et al. Rapid induction of antigen-specific CD4+ T cells is associated with coordinated humoral and cellular immunity to SARS-CoV-2 mRNA vaccination. Immunity. 2021;54(9):2133-2142.e3.
Harrington P, de Lavallade H, Doores KJ, et al. Single dose of BNT162b2 mRNA vaccine against SARS-CoV-2 induces high frequency of neutralising antibody and polyfunctional T-cell responses in patients with myeloproliferative neoplasms. Leukemia. 2021;35:3573-3577.
Marasco V, Carniti C, Guidetti A, et al. T-cell immune response after mRNA SARS-CoV-2 vaccines is frequently detected also in the absence of seroconversion in patients with lymphoid malignancies. Br J Haematol. 2022;196:548-558. doi:10.1111/bjh.17877
Tea F, Stella AO, Aggarwal A, et al. SARS-CoV-2 neutralizing antibodies: longevity, breadth, and evasion by emerging viral variants. PLoS Med. 2021;18(7):e1003656.
Tea F, Lopez JA, Ramanathan S, et al. Characterization of the human myelin oligodendrocytes glycoprotein antibody response in demyelination. Acta Neuropathol Commun. 2019;7:145.
Khoury DS, Cromer D, Reynaldi A, et al. Neutralizing antibody levels are highly predictive of immune protection from symptomatic SARS-CoV-2 infection. Nat Med. 2021;27:1205-1211.
Mattiuzzo G, Bentley E M, Hassall M, et al. Establishment of the WHO international standard and reference panel for anti-SARS-CoV-2 antibody. WHO Expert Committee on Biological Standardization. 2020.
Aggarwal A, Stella A, Walker G, et al. Platform for isolation and characterization of SARS-CoV-2 variants enables rapid characerization of Omicron in Australia. Nat Microbiol. 2022;7(6):896-908. doi:10/1038/s41564-022-01135-7.
Mateus J, Grifoni A, Tarke A, et al. Selective and cross-reactive SARS-CoV-2 T cell epitopes in unexposed humans. Science. 2020;370(6512):89-94.
Pent Y, Mentzer AJ, Liu G, et al. Broad and strong memory CD4+ and CD8+ T cells incuded by SARS-CoV-2 in UKconvalescent individuals following COVID-19. Nat Immunol. 2020;21:1336-1345.
Zaunders JJ, Munier ML, Seddiki N, et al. High levels of human antigen-specific CD4+ T cells in peripheral blood revealed by stimulated coexpression of CD25 and CD134 (OX40). J Immunol. 2009;183(4):2827-2836.
Jurgens EM, Ketas TJ, Zhao Z, et al. Serologic response to mRNA COVID-19 vaccination in lymphoma patients. Am J Hematol. 2021;96(11):E410-E413.
Perry C, Luttwak E, Balaban R, et al. Efficacy of the BNT162b2 mRNA COVID-19 vaccine in patients with B-cell non-Hodgkin lymphoma. Blood Adv. 2021;5(16):3053-3061.
Parry H, McIlroy G, Bruton R, et al. Antibody responses after first and second Covid-19 vaccination in patients with chronic lymphocytic leukemia. Blood Cancer J. 2021;11:136.
Ai J, Zhang H, Zhang Y, et al. Omicron variant showed lower neutralizing sensitivity than other SARS-CoV-2 variants to immune sera elicited by vaccines after boost. Emerg Microbes Infect. 2022;11:337-343. doi:10.1080/22221751.2021.2022440
Herishanu Y, Rahav G, Levi S, et al. Efficacy of a third BNT162b2 mRNA COVID-19 vaccine dose in patients with CLL who failed standard two-dose vaccination. Blood. 2022;139:678-685. doi:10.1182/blood.2021014085
Bange EM, Han NA, Wileyto P, et al. CD8+ T cells contribute to survival in COVID-19 patients with hematologic cancer. Nat Med. 2021;27(7):1280-1289.
Loo Y, McTamney PM, Arends RH, et al. AZD7442 demonstrates prophylactic and therapeutic efficacy in non-human primates and extended half life in humans. 2021. doi:10.1101/2021.08.30.21262666
Benotmane I, Velay A, Thaunat O, et al. Pre-exposure prophylaxis with Evusheld elicits limited neutralizing activity against the omicron variant in kidney transplant patients. 2022. doi:10.1101/2022.03.21.22272669
Bruel T, Hadjadj J, Maes P, et al. Serum neutralization of SARS-CoV-2 omicron sublineages BA.1 and BA.2 in patients receiving monoclongal antibodies. Nat Med. Published online March 23, 2022. doi:10/1016/j.kint.2022.05.008

Auteurs

Brendan Beaton (B)

Haematology Department, Concord Repatriation General Hospital, Sydney, New South Wales, Australia.
Concord Clinical School, Faculty of Medicine and Health, The University of Sydney, Sydney, New South Wales, Australia.
ORCID: 0000-0002-9260-720X

Sarah C Sasson (SC)

The Kirby Institute, The University of New South Wales, Sydney, New South Wales, Australia.
Department of Clinical Immunology and Immunopathology, ICPMR Westmead Hospital, Sydney, New South Wales, Australia.

Katherine Rankin (K)

Haematology Department, Concord Repatriation General Hospital, Sydney, New South Wales, Australia.

Juliette Raedemaeker (J)

Haematology Department, Concord Repatriation General Hospital, Sydney, New South Wales, Australia.

Alexander Wong (A)

Haematology Department, Concord Repatriation General Hospital, Sydney, New South Wales, Australia.
Concord Clinical School, Faculty of Medicine and Health, The University of Sydney, Sydney, New South Wales, Australia.

Priyanka Hastak (P)

The Kirby Institute, The University of New South Wales, Sydney, New South Wales, Australia.

Chansavath Phetsouphanh (C)

The Kirby Institute, The University of New South Wales, Sydney, New South Wales, Australia.

Andrew Warden (A)

WMozzies: Australian Patient Support Group for Waldenström's Macroglobulinemia, Sydney, New South Wales, Australia.

Vera Klemm (V)

The Kirby Institute, The University of New South Wales, Sydney, New South Wales, Australia.

C Mee Ling Munier (CML)

The Kirby Institute, The University of New South Wales, Sydney, New South Wales, Australia.

Alexandra Carey Hoppe (AC)

The Kirby Institute, The University of New South Wales, Sydney, New South Wales, Australia.

Fiona Tea (F)

Brain Autoimmunity Group, Kids Neuroscience Centre, Kids Research, The Children's Hospital at Westmead, Sydney, New South Wales, Australia.

Aleha Pillay (A)

Brain Autoimmunity Group, Kids Neuroscience Centre, Kids Research, The Children's Hospital at Westmead, Sydney, New South Wales, Australia.

Alberto Ospina Stella (AO)

The Kirby Institute, The University of New South Wales, Sydney, New South Wales, Australia.

Anupriya Aggarwal (A)

The Kirby Institute, The University of New South Wales, Sydney, New South Wales, Australia.

Orly Lavee (O)

St Vincent's Hospital, Sydney, New South Wales, Australia.

Ian D Caterson (ID)

COVID Vaccination Hub, Sydney Local Health District, Sydney, New South Wales, Australia.

Stuart Turville (S)

The Kirby Institute, The University of New South Wales, Sydney, New South Wales, Australia.

Anthony D Kelleher (AD)

The Kirby Institute, The University of New South Wales, Sydney, New South Wales, Australia.

Fabienne Brilot (F)

Brain Autoimmunity Group, Kids Neuroscience Centre, Kids Research, The Children's Hospital at Westmead, Sydney, New South Wales, Australia.
Sydney Institute of Infectious Disease, The University of Sydney, Sydney, New South Wales, Australia.
The School of Medical Sciences, Faculty of Medicine and Health, The University of Sydney, Sydney, New South Wales, Australia.

Judith Trotman (J)

Haematology Department, Concord Repatriation General Hospital, Sydney, New South Wales, Australia.
Concord Clinical School, Faculty of Medicine and Health, The University of Sydney, Sydney, New South Wales, Australia.

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Patients with treated indolent lymphomas...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Globulines › Sérum-globulines › Immunoglobulines › Anticorps › Isotypes des immunoglobulines › Immunoglobuline G › Patients with treated indolent lymphomas...
questionsmedicales.fr › Virus › Virus à ARN › Virus à ARN à brin positif › Nidovirales › Coronaviridae › Coronavirus › Betacoronavirus › Virus du SRAS › SARS-CoV-2 › Patients with treated indolent lymphomas...
questionsmedicales.fr › Facteurs biologiques › Antigènes › Vaccins synthétiques › Vaccins à base d'acide nucléique › Vaccins à ARNm › Vaccin BNT162 › Patients with treated indolent lymphomas...
questionsmedicales.fr › Maladies de l'appareil respiratoire › Infections de l'appareil respiratoire › Pneumopathie infectieuse › Pneumopathie virale › COVID-19 › Patients with treated indolent lymphomas...
questionsmedicales.fr › Systèmes sanguin et immunitaire › Système immunitaire › Leucocytes › Agranulocytes › Lymphocytes › Lymphocytes T › Patients with treated indolent lymphomas...
questionsmedicales.fr › Maladies du système immunitaire › Syndromes immunoprolifératifs › Syndromes lymphoprolifératifs › Lymphomes › Lymphome malin non hodgkinien › Patients with treated indolent lymphomas...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Globulines › Sérum-globulines › Immunoglobulines › Anticorps › Anticorps antiviraux › Patients with treated indolent lymphomas...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Globulines › Sérum-globulines › Immunoglobulines › Anticorps › Anticorps neutralisants › Patients with treated indolent lymphomas...
questionsmedicales.fr › Environnement et santé publique › Santé publique › Pratiques en santé publique › Prévention primaire › Immunisation › Vaccination › Patients with treated indolent lymphomas...