SARS-CoV-2 mRNA vaccination exposes progressive adaptive immune dysfunction in patients with chronic lymphocytic leukemia

Chronic lymphocytic leukemia (CLL) patients have lower seroconversion rates and antibody titers following SARS-CoV-2 vaccination, but the reasons for this diminished response are poorly understood. Here, we studied humoral and cellular responses in 95 CLL patients and 30 healthy controls after two BNT162b2 or mRNA-2173 mRNA immunizations. We found that 42% of CLL vaccinees developed SARS-CoV-2-specific binding and neutralizing antibodies (NAbs), while 32% had no response. Interestingly, 26% were seropositive, but had no detectable NAbs, suggesting the maintenance of pre-existing endemic human coronavirus-specific antibodies that cross-react with the S2 domain of the SARS-CoV-2 spike. These individuals had more advanced disease. In treatment-naive CLL patients, mRNA-2173 induced 12-fold higher NAb titers and 1.7-fold higher response rates than BNT162b2. These data reveal a graded loss of immune function, with pre-existing memory being preserved longer than the capacity to respond to new antigens, and identify mRNA-2173 as a superior vaccine for CLL patients.

[1]  C. Sanders,et al.  Anti-spike T-cell and Antibody Responses to SARS-CoV-2 mRNA Vaccines in Patients with Hematologic Malignancies , 2022, Blood cancer discovery.

[2]  M. Farcet,et al.  Omicron Severe Acute Respiratory Syndrome Coronavirus 2 Neutralization by Immunoglobulin Preparations Manufactured From Plasma Collected in the United States and Europe , 2022, The Journal of infectious diseases.

[3]  S. Ostrowski,et al.  Patients with CLL have a lower risk of death from COVID-19 in the Omicron era , 2022, Blood.

[4]  M. Clerici,et al.  Dating the Emergence of Human Endemic Coronaviruses , 2022, Viruses.

[5]  D. Segev,et al.  Comparison of SARS-CoV-2 Antibody Response After 2-Dose mRNA-1273 vs BNT162b2 Vaccines in Incrementally Immunosuppressed Patients , 2022, JAMA network open.

[6]  Shuo Ma,et al.  CLO22-043: Humoral Immune Response Following COVID-19 Vaccination in Patients With Chronic Lymphocytic Leukemia and Other Indolent Lymphomas: A Large, Single-Center Observational Study , 2022, Journal of the National Comprehensive Cancer Network.

[7]  P. Maes,et al.  Serum neutralization of SARS-CoV-2 Omicron sublineages BA.1 and BA.2 in patients receiving monoclonal antibodies , 2022, Nature Medicine.

[8]  P. Goepfert,et al.  Comprehensive mapping of SARS-CoV-2 peptide epitopes for development of a highly sensitive serological test for total and neutralizing antibodies. , 2022, Protein engineering, design & selection : PEDS.

[9]  M. Kemp,et al.  The P132H mutation in the main protease of Omicron SARS-CoV-2 decreases thermal stability without compromising catalysis or small-molecule drug inhibition , 2022, Cell Research.

[10]  H. Ljunggren,et al.  T-cell immune responses following vaccination with mRNA BNT162b2 against SARS-CoV-2 in patients with chronic lymphocytic leukemia: results from a prospective open-label clinical trial , 2022, Haematologica.

[11]  R. Bruton,et al.  Impaired neutralisation of SARS-CoV-2 delta variant in vaccinated patients with B cell chronic lymphocytic leukaemia , 2022, Journal of Hematology & Oncology.

[12]  G. Rahav,et al.  Efficacy of a third BNT162b2 mRNA COVID-19 vaccine dose in patients with CLL who failed standard 2-dose vaccination , 2021, Blood.

[13]  E. Montserrat,et al.  COVID-19 severity and mortality in patients with CLL: an update of the international ERIC and Campus CLL study , 2021, Leukemia.

[14]  Patrick W. Johnson,et al.  Antibody response to SARS-CoV-2 vaccines in patients with hematologic malignancies , 2021, Cancer Cell.

[15]  B. Hahn,et al.  SARS-CoV-2-specific circulating T follicular helper cells correlate with neutralizing antibodies and increase during early convalescence , 2021, PLoS pathogens.

[16]  Chaim A. Schramm,et al.  Ultrapotent antibodies against diverse and highly transmissible SARS-CoV-2 variants , 2021, Science.

[17]  John P. Moore,et al.  Predictors of Nonseroconversion after SARS-CoV-2 Infection , 2021, Emerging infectious diseases.

[18]  S. Madhi,et al.  Reduced neutralization of SARS-CoV-2 B.1.617 by vaccine and convalescent serum , 2021, Cell.

[19]  G. Shefer,et al.  Efficacy of the BNT162b2 mRNA COVID-19 vaccine in patients with chronic lymphocytic leukemia , 2021, Blood.

[20]  Cynthia Liu,et al.  A Comprehensive Review of the Global Efforts on COVID-19 Vaccine Development , 2021, ACS central science.

[21]  G. Debnath,et al.  Antibody responses to SARS-CoV-2 mRNA vaccines are detectable in saliva , 2021, bioRxiv.

[22]  J. Mascola,et al.  Efficacy and Safety of the mRNA-1273 SARS-CoV-2 Vaccine , 2020, The New England journal of medicine.

[23]  P. Dormitzer,et al.  Safety and Efficacy of the BNT162b2 mRNA Covid-19 Vaccine , 2020, The New England journal of medicine.

[24]  S. Mallal,et al.  Comprehensive analysis of T cell immunodominance and immunoprevalence of SARS-CoV-2 epitopes in COVID-19 cases , 2020, bioRxiv.

[25]  John P. Moore,et al.  Convalescent plasma-mediated resolution of COVID-19 in a patient with humoral immunodeficiency , 2020, Cell Reports Medicine.

[26]  G. Marti,et al.  Effect of Bruton tyrosine kinase inhibitor on efficacy of adjuvanted recombinant hepatitis B and zoster vaccines , 2020, Blood.

[27]  P. Hotez,et al.  Neutralizing antibodies for the treatment of COVID-19 , 2020, Nature Biomedical Engineering.

[28]  E. Fischer,et al.  Case Study: Prolonged Infectious SARS-CoV-2 Shedding from an Asymptomatic Immunocompromised Individual with Cancer , 2020, Cell.

[29]  R. Baric,et al.  Safety and Immunogenicity of SARS-CoV-2 mRNA-1273 Vaccine in Older Adults , 2020, The New England journal of medicine.

[30]  H. Goossens,et al.  Seasonal coronavirus protective immunity is short-lasting , 2020, Nature Medicine.

[31]  S. Mallal,et al.  Selective and cross-reactive SARS-CoV-2 T cell epitopes in unexposed humans , 2020, Science.

[32]  A. Zelenetz,et al.  Outcomes of COVID-19 in patients with CLL: a multicenter international experience , 2020, Blood.

[33]  J. Babik,et al.  COVID-19 in Immunocompromised Hosts: What We Know So Far. , 2020, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[34]  S. Rowland-Jones,et al.  Tracking Changes in SARS-CoV-2 Spike: Evidence that D614G Increases Infectivity of the COVID-19 Virus , 2020, Cell.

[35]  M. Gentile,et al.  Response to the conjugate pneumococcal vaccine (PCV13) in patients with chronic lymphocytic leukemia (CLL) , 2020, Leukemia.

[36]  C. Rice,et al.  Measuring SARS-CoV-2 neutralizing antibody activity using pseudotyped and chimeric viruses , 2020, bioRxiv.

[37]  M. V. van Breemen,et al.  Potent neutralizing antibodies from COVID-19 patients define multiple targets of vulnerability , 2020, Science.

[38]  M. Wener,et al.  Performance Characteristics of the Abbott Architect SARS-CoV-2 IgG Assay and Seroprevalence in Boise, Idaho , 2020, Journal of Clinical Microbiology.

[39]  M. Cascella,et al.  Features, Evaluation and Treatment Coronavirus (COVID-19) , 2020 .

[40]  A. Walls,et al.  Structure, Function, and Antigenicity of the SARS-CoV-2 Spike Glycoprotein , 2020, Cell.

[41]  G. Herrler,et al.  SARS-CoV-2 Cell Entry Depends on ACE2 and TMPRSS2 and Is Blocked by a Clinically Proven Protease Inhibitor , 2020, Cell.

[42]  Young-Jun Park,et al.  Structure, Function, and Antigenicity of the SARS-CoV-2 Spike Glycoprotein , 2020, Cell.

[43]  E. Dong,et al.  An interactive web-based dashboard to track COVID-19 in real time , 2020, The Lancet Infectious Diseases.

[44]  J. Cyster,et al.  B Cell Responses: Cell Interaction Dynamics and Decisions , 2019, Cell.

[45]  C. Scheibenbogen,et al.  Current clinical practice and challenges in the management of secondary immunodeficiency in hematological malignancies , 2019, European journal of haematology.

[46]  Henry A. Utset,et al.  Influenza Virus Vaccination Elicits Poorly Adapted B Cell Responses in Elderly Individuals. , 2019, Cell host & microbe.

[47]  J. Byrd,et al.  iwCLL guidelines for diagnosis, indications for treatment, response assessment, and supportive management of CLL. , 2018, Blood.

[48]  E. Kimby,et al.  Pneumococcal conjugate vaccine triggers a better immune response than pneumococcal polysaccharide vaccine in patients with chronic lymphocytic leukemia A randomized study by the Swedish CLL group. , 2018, Vaccine.

[49]  I. Barr,et al.  Ibrutinib may impair serological responses to influenza vaccination , 2017, Haematologica.

[50]  Mark M. Davis,et al.  Phylogenetic analysis of the human antibody repertoire reveals quantitative signatures of immune senescence and aging , 2017, Proceedings of the National Academy of Sciences.

[51]  M. Eichelberger,et al.  Seasonal Influenza Vaccination in Patients With Chronic Lymphocytic Leukemia Treated With Ibrutinib. , 2016, JAMA oncology.

[52]  P. Moss,et al.  Perturbation of the normal immune system in patients with CLL. , 2015, Blood.

[53]  Greg Finak,et al.  COMPASS identifies T-cell subsets correlated with clinical outcomes , 2015, Nature Biotechnology.

[54]  J. Gribben,et al.  T cells from CLL patients exhibit features of T-cell exhaustion but retain capacity for cytokine production. , 2013, Blood.

[55]  É. Vivier,et al.  FCRL6 distinguishes mature cytotoxic lymphocytes and is upregulated in patients with B‐cell chronic lymphocytic leukemia , 2008, European journal of immunology.

[56]  A Benner,et al.  Genomic aberrations and survival in chronic lymphocytic leukemia. , 2000, The New England journal of medicine.

[57]  S. Peller,et al.  Decreased CD45RA T cells in B-cell chronic lymphatic leukemia patients: correlation with disease stage. , 1991, Blood.

[58]  B. Clarkson,et al.  Abnormal T lymphocyte subpopulations in patients with B cell chronic lymphocytic leukemia: an analysis by monoclonal antibodies. , 1982, Journal of immunology.