mRNA vaccine boosting enhances antibody responses against SARS-CoV-2 Omicron variant in individuals with antibody deficiency syndromes

Ofer Zimmerman; Alexa Michelle Altman Doss; Paulina Kaplonek; Chieh Yu Liang; Laura A. VanBlargan; Rita E. Chen; Jennifer Marie Monroy; H. James Wedner; Anthony Kulczycki; Tarisa L. Mantia; Caitlin C. O'Shaughnessy; Hannah G. Davis-Adams; Harry L. Bertera; Lucas J. Adams; Saravanan Raju; Fang R. Zhao; Christopher Rigell; Tiffany Biason Dy; Andrew L. Kau; Zhen Ren; Jackson S. Turner; Jane A. O'Halloran; Rachel M. Presti; Daved H. Fremont; Peggy L. Kendall; Ali H. Ellebedy; Galit Alter; Michael S. Diamond

doi:10.1016/j.xcrm.2022.100653

mRNA vaccine boosting enhances antibody responses against SARS-CoV-2 Omicron variant in individuals with antibody deficiency syndromes

Ofer Zimmerman, Alexa Michelle Altman Doss, Paulina Kaplonek, Chieh Yu Liang, Laura A. VanBlargan, Rita E. Chen, Jennifer Marie Monroy, H. James Wedner, Anthony Kulczycki, Tarisa L. Mantia, Caitlin C. O'Shaughnessy, Hannah G. Davis-Adams, Harry L. Bertera, Lucas J. Adams, Saravanan Raju, Fang R. Zhao, Christopher Rigell, Tiffany Biason Dy, Andrew L. Kau, Zhen RenJackson S. Turner, Jane A. O'Halloran, Rachel M. Presti, Daved H. Fremont, Peggy L. Kendall, Ali H. Ellebedy, Galit Alter, Michael S. Diamond

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14 Scopus citations

Abstract

Individuals with primary antibody deficiency (PAD) syndromes have poor humoral immune responses requiring immunoglobulin replacement therapy. We followed individuals with PAD after severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccination by evaluating their immunoglobulin replacement products and serum for anti-spike binding, Fcγ receptor (FcγR) binding, and neutralizing activities. The immunoglobulin replacement products tested have low anti-spike and receptor-binding domain (RBD) titers and neutralizing activity. In coronavirus disease 2019 (COVID-19)-naive individuals with PAD, anti-spike and RBD titers increase after mRNA vaccination but wane by 90 days. Those vaccinated after SARS-CoV-2 infection develop higher and more sustained responses comparable with healthy donors. Most vaccinated individuals with PAD have serum-neutralizing antibody titers above an estimated correlate of protection against ancestral SARS-CoV-2 and Delta virus but not against Omicron virus, although this is improved by boosting. Thus, some immunoglobulin replacement products likely have limited protective activity, and immunization and boosting of individuals with PAD with mRNA vaccines should confer at least short-term immunity against SARS-CoV-2 variants, including Omicron.

Original language	English
Article number	100653
Journal	Cell Reports Medicine
Volume	3
Issue number	6
DOIs	https://doi.org/10.1016/j.xcrm.2022.100653
State	Published - Jun 21 2022

Keywords

COVID-19
SARS-CoV-2
combined variable antibody deficiency
hypogammaglobulinemia
immune response
mRNA vaccine
neutralization
specific antibody deficiency
vaccine

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10.1016/j.xcrm.2022.100653

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Zimmerman, O., Altman Doss, A. M., Kaplonek, P., Liang, C. Y., VanBlargan, L. A., Chen, R. E., Monroy, J. M., Wedner, H. J., Kulczycki, A., Mantia, T. L., O'Shaughnessy, C. C., Davis-Adams, H. G., Bertera, H. L., Adams, L. J., Raju, S., Zhao, F. R., Rigell, C., Dy, T. B., Kau, A. L., ... Diamond, M. S. (2022). mRNA vaccine boosting enhances antibody responses against SARS-CoV-2 Omicron variant in individuals with antibody deficiency syndromes. Cell Reports Medicine, 3(6), Article 100653. https://doi.org/10.1016/j.xcrm.2022.100653

@article{19f968ae7d514160a2dceb556597e85a,

title = "mRNA vaccine boosting enhances antibody responses against SARS-CoV-2 Omicron variant in individuals with antibody deficiency syndromes",

abstract = "Individuals with primary antibody deficiency (PAD) syndromes have poor humoral immune responses requiring immunoglobulin replacement therapy. We followed individuals with PAD after severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccination by evaluating their immunoglobulin replacement products and serum for anti-spike binding, Fcγ receptor (FcγR) binding, and neutralizing activities. The immunoglobulin replacement products tested have low anti-spike and receptor-binding domain (RBD) titers and neutralizing activity. In coronavirus disease 2019 (COVID-19)-naive individuals with PAD, anti-spike and RBD titers increase after mRNA vaccination but wane by 90 days. Those vaccinated after SARS-CoV-2 infection develop higher and more sustained responses comparable with healthy donors. Most vaccinated individuals with PAD have serum-neutralizing antibody titers above an estimated correlate of protection against ancestral SARS-CoV-2 and Delta virus but not against Omicron virus, although this is improved by boosting. Thus, some immunoglobulin replacement products likely have limited protective activity, and immunization and boosting of individuals with PAD with mRNA vaccines should confer at least short-term immunity against SARS-CoV-2 variants, including Omicron.",

keywords = "COVID-19, SARS-CoV-2, combined variable antibody deficiency, hypogammaglobulinemia, immune response, mRNA vaccine, neutralization, specific antibody deficiency, vaccine",

author = "Ofer Zimmerman and {Altman Doss}, {Alexa Michelle} and Paulina Kaplonek and Liang, {Chieh Yu} and VanBlargan, {Laura A.} and Chen, {Rita E.} and Monroy, {Jennifer Marie} and Wedner, {H. James} and Anthony Kulczycki and Mantia, {Tarisa L.} and O'Shaughnessy, {Caitlin C.} and Davis-Adams, {Hannah G.} and Bertera, {Harry L.} and Adams, {Lucas J.} and Saravanan Raju and Zhao, {Fang R.} and Christopher Rigell and Dy, {Tiffany Biason} and Kau, {Andrew L.} and Zhen Ren and Turner, {Jackson S.} and O'Halloran, {Jane A.} and Presti, {Rachel M.} and Fremont, {Daved H.} and Kendall, {Peggy L.} and Ellebedy, {Ali H.} and Galit Alter and Diamond, {Michael S.}",

note = "Publisher Copyright: {\textcopyright} 2022 The Author(s)",

year = "2022",

month = jun,

day = "21",

doi = "10.1016/j.xcrm.2022.100653",

language = "English",

volume = "3",

journal = "Cell Reports Medicine",

issn = "2666-3791",

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Zimmerman, O , Altman Doss, AM, Kaplonek, P, Liang, CY, VanBlargan, LA, Chen, RE, Monroy, JM, Wedner, HJ, Kulczycki, A, Mantia, TL, O'Shaughnessy, CC, Davis-Adams, HG, Bertera, HL, Adams, LJ, Raju, S, Zhao, FR , Rigell, C , Dy, TB , Kau, AL , Ren, Z , Turner, JS, O'Halloran, JA, Presti, RM , Fremont, DH , Kendall, PL , Ellebedy, AH, Alter, G & Diamond, MS 2022, 'mRNA vaccine boosting enhances antibody responses against SARS-CoV-2 Omicron variant in individuals with antibody deficiency syndromes', Cell Reports Medicine, vol. 3, no. 6, 100653. https://doi.org/10.1016/j.xcrm.2022.100653

TY - JOUR

T1 - mRNA vaccine boosting enhances antibody responses against SARS-CoV-2 Omicron variant in individuals with antibody deficiency syndromes

AU - Zimmerman, Ofer

AU - Altman Doss, Alexa Michelle

AU - Kaplonek, Paulina

AU - Liang, Chieh Yu

AU - VanBlargan, Laura A.

AU - Chen, Rita E.

AU - Monroy, Jennifer Marie

AU - Wedner, H. James

AU - Kulczycki, Anthony

AU - Mantia, Tarisa L.

AU - O'Shaughnessy, Caitlin C.

AU - Davis-Adams, Hannah G.

AU - Bertera, Harry L.

AU - Adams, Lucas J.

AU - Raju, Saravanan

AU - Zhao, Fang R.

AU - Rigell, Christopher

AU - Dy, Tiffany Biason

AU - Kau, Andrew L.

AU - Ren, Zhen

AU - Turner, Jackson S.

AU - O'Halloran, Jane A.

AU - Presti, Rachel M.

AU - Fremont, Daved H.

AU - Kendall, Peggy L.

AU - Ellebedy, Ali H.

AU - Alter, Galit

AU - Diamond, Michael S.

PY - 2022/6/21

Y1 - 2022/6/21

N2 - Individuals with primary antibody deficiency (PAD) syndromes have poor humoral immune responses requiring immunoglobulin replacement therapy. We followed individuals with PAD after severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccination by evaluating their immunoglobulin replacement products and serum for anti-spike binding, Fcγ receptor (FcγR) binding, and neutralizing activities. The immunoglobulin replacement products tested have low anti-spike and receptor-binding domain (RBD) titers and neutralizing activity. In coronavirus disease 2019 (COVID-19)-naive individuals with PAD, anti-spike and RBD titers increase after mRNA vaccination but wane by 90 days. Those vaccinated after SARS-CoV-2 infection develop higher and more sustained responses comparable with healthy donors. Most vaccinated individuals with PAD have serum-neutralizing antibody titers above an estimated correlate of protection against ancestral SARS-CoV-2 and Delta virus but not against Omicron virus, although this is improved by boosting. Thus, some immunoglobulin replacement products likely have limited protective activity, and immunization and boosting of individuals with PAD with mRNA vaccines should confer at least short-term immunity against SARS-CoV-2 variants, including Omicron.

AB - Individuals with primary antibody deficiency (PAD) syndromes have poor humoral immune responses requiring immunoglobulin replacement therapy. We followed individuals with PAD after severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccination by evaluating their immunoglobulin replacement products and serum for anti-spike binding, Fcγ receptor (FcγR) binding, and neutralizing activities. The immunoglobulin replacement products tested have low anti-spike and receptor-binding domain (RBD) titers and neutralizing activity. In coronavirus disease 2019 (COVID-19)-naive individuals with PAD, anti-spike and RBD titers increase after mRNA vaccination but wane by 90 days. Those vaccinated after SARS-CoV-2 infection develop higher and more sustained responses comparable with healthy donors. Most vaccinated individuals with PAD have serum-neutralizing antibody titers above an estimated correlate of protection against ancestral SARS-CoV-2 and Delta virus but not against Omicron virus, although this is improved by boosting. Thus, some immunoglobulin replacement products likely have limited protective activity, and immunization and boosting of individuals with PAD with mRNA vaccines should confer at least short-term immunity against SARS-CoV-2 variants, including Omicron.

KW - COVID-19

KW - SARS-CoV-2

KW - combined variable antibody deficiency

KW - hypogammaglobulinemia

KW - immune response

KW - mRNA vaccine

KW - neutralization

KW - specific antibody deficiency

KW - vaccine

UR - http://www.scopus.com/inward/record.url?scp=85132745357&partnerID=8YFLogxK

U2 - 10.1016/j.xcrm.2022.100653

DO - 10.1016/j.xcrm.2022.100653

M3 - Article

C2 - 35688161

AN - SCOPUS:85132745357

SN - 2666-3791

VL - 3

JO - Cell Reports Medicine

JF - Cell Reports Medicine

IS - 6

M1 - 100653

ER -

mRNA vaccine boosting enhances antibody responses against SARS-CoV-2 Omicron variant in individuals with antibody deficiency syndromes

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