Immunogenicity of COVID-19 booster vaccination in IEI patients and their one year clinical follow-up after start of the COVID-19 vaccination program

PurposePrevious studies have demonstrated that the majority of patients with an inborn error of immunity (IEI) develop a spike (S)-specific IgG antibody and T-cell response after two doses of the mRNA-1273 COVID-19 vaccine, but little is known about the response to a booster vaccination. We studied...

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Main Authors: Leanne P. M. van Leeuwen, Marloes Grobben, Corine H. GeurtsvanKessel, Pauline M. Ellerbroek, Godelieve J. de Bree, Judith Potjewijd, Abraham Rutgers, Hetty Jolink, Frank L. van de Veerdonk, Marit J. van Gils, Rory D. de Vries, Virgil A. S. H. Dalm, VACOPID Research Group, Eric C.M. van Gorp, Faye de Wilt, Susanne Bogers, Lennert Gommers, Daryl Geers, Marianne W. van der Ent, P. Martin van Hagen, Jelle W. van Haga, Bregtje A. Lemkes, Annelou van der Veen, Rogier W. Sanders, Karlijn van der Straten, Judith A. Burger, Jacqueline van Rijswijk, Khadija Tejjani, Joey H. Bouhuijs, Karina de Leeuw, Annick A.J.M. van de Ven, S.F.J. de Kruijf-Bazen, Pieter van Paassen, Lotte Wieten, Petra H. Verbeek-Menken, Annelies van Wengen, Anke H.W. Bruns, Helen L. Leavis, Stefan Nierkens
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-04-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2024.1390022/full
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author Leanne P. M. van Leeuwen
Leanne P. M. van Leeuwen
Marloes Grobben
Corine H. GeurtsvanKessel
Pauline M. Ellerbroek
Godelieve J. de Bree
Judith Potjewijd
Abraham Rutgers
Hetty Jolink
Frank L. van de Veerdonk
Marit J. van Gils
Rory D. de Vries
Virgil A. S. H. Dalm
Virgil A. S. H. Dalm
VACOPID Research Group
Eric C.M. van Gorp
Faye de Wilt
Susanne Bogers
Lennert Gommers
Daryl Geers
Marianne W. van der Ent
P. Martin van Hagen
Jelle W. van Haga
Bregtje A. Lemkes
Annelou van der Veen
Rogier W. Sanders
Karlijn van der Straten
Judith A. Burger
Jacqueline van Rijswijk
Khadija Tejjani
Joey H. Bouhuijs
Karina de Leeuw
Annick A.J.M. van de Ven
S.F.J. de Kruijf-Bazen
Pieter van Paassen
Lotte Wieten
Petra H. Verbeek-Menken
Annelies van Wengen
Anke H.W. Bruns
Helen L. Leavis
Stefan Nierkens
author_facet Leanne P. M. van Leeuwen
Leanne P. M. van Leeuwen
Marloes Grobben
Corine H. GeurtsvanKessel
Pauline M. Ellerbroek
Godelieve J. de Bree
Judith Potjewijd
Abraham Rutgers
Hetty Jolink
Frank L. van de Veerdonk
Marit J. van Gils
Rory D. de Vries
Virgil A. S. H. Dalm
Virgil A. S. H. Dalm
VACOPID Research Group
Eric C.M. van Gorp
Faye de Wilt
Susanne Bogers
Lennert Gommers
Daryl Geers
Marianne W. van der Ent
P. Martin van Hagen
Jelle W. van Haga
Bregtje A. Lemkes
Annelou van der Veen
Rogier W. Sanders
Karlijn van der Straten
Judith A. Burger
Jacqueline van Rijswijk
Khadija Tejjani
Joey H. Bouhuijs
Karina de Leeuw
Annick A.J.M. van de Ven
S.F.J. de Kruijf-Bazen
Pieter van Paassen
Lotte Wieten
Petra H. Verbeek-Menken
Annelies van Wengen
Anke H.W. Bruns
Helen L. Leavis
Stefan Nierkens
author_sort Leanne P. M. van Leeuwen
collection DOAJ
description PurposePrevious studies have demonstrated that the majority of patients with an inborn error of immunity (IEI) develop a spike (S)-specific IgG antibody and T-cell response after two doses of the mRNA-1273 COVID-19 vaccine, but little is known about the response to a booster vaccination. We studied the immune responses 8 weeks after booster vaccination with mRNA-based COVID-19 vaccines in 171 IEI patients. Moreover, we evaluated the clinical outcomes in these patients one year after the start of the Dutch COVID-19 vaccination campaign.MethodsThis study was embedded in a large prospective multicenter study investigating the immunogenicity of COVID-19 mRNA-based vaccines in IEI (VACOPID study). Blood samples were taken from 244 participants 8 weeks after booster vaccination. These participants included 171 IEI patients (X-linked agammaglobulinemia (XLA;N=11), combined immunodeficiency (CID;N=4), common variable immunodeficiency (CVID;N=45), isolated or undefined antibody deficiencies (N=108) and phagocyte defects (N=3)) and 73 controls. SARS-CoV-2-specific IgG titers, neutralizing antibodies, and T-cell responses were evaluated. One year after the start of the COVID-19 vaccination program, 334 study participants (239 IEI patients and 95 controls) completed a questionnaire to supplement their clinical data focusing on SARS-CoV-2 infections.ResultsAfter booster vaccination, S-specific IgG titers increased in all COVID-19 naive IEI cohorts and controls, when compared to titers at 6 months after the priming regimen. The fold-increases did not differ between controls and IEI cohorts. SARS-CoV-2-specific T-cell responses also increased equally in all cohorts after booster vaccination compared to 6 months after the priming regimen. Most SARS-CoV-2 infections during the study period occurred in the period when the Omicron variant had become dominant. The clinical course of these infections was mild, although IEI patients experienced more frequent fever and dyspnea compared to controls and their symptoms persisted longer.ConclusionOur study demonstrates that mRNA-based booster vaccination induces robust recall of memory B-cell and T-cell responses in most IEI patients. One-year clinical follow-up demonstrated that SARS-CoV-2 infections in IEI patients were mild. Given our results, we support booster campaigns with newer variant-specific COVID-19 booster vaccines to IEI patients with milder phenotypes.
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spelling doaj.art-f5f340a3b6454dfba93ece08a8ba7d1f2024-04-18T04:28:01ZengFrontiers Media S.A.Frontiers in Immunology1664-32242024-04-011510.3389/fimmu.2024.13900221390022Immunogenicity of COVID-19 booster vaccination in IEI patients and their one year clinical follow-up after start of the COVID-19 vaccination programLeanne P. M. van Leeuwen0Leanne P. M. van Leeuwen1Marloes Grobben2Corine H. GeurtsvanKessel3Pauline M. Ellerbroek4Godelieve J. de Bree5Judith Potjewijd6Abraham Rutgers7Hetty Jolink8Frank L. van de Veerdonk9Marit J. van Gils10Rory D. de Vries11Virgil A. S. H. Dalm12Virgil A. S. H. Dalm13VACOPID Research GroupEric C.M. van GorpFaye de WiltSusanne BogersLennert GommersDaryl GeersMarianne W. van der EntP. Martin van HagenJelle W. van HagaBregtje A. LemkesAnnelou van der VeenRogier W. SandersKarlijn van der StratenJudith A. BurgerJacqueline van RijswijkKhadija TejjaniJoey H. BouhuijsKarina de LeeuwAnnick A.J.M. van de VenS.F.J. de Kruijf-BazenPieter van PaassenLotte WietenPetra H. Verbeek-MenkenAnnelies van WengenAnke H.W. BrunsHelen L. LeavisStefan NierkensDepartment of Viroscience, Erasmus MC University Medical Center Rotterdam, Rotterdam, NetherlandsTravel Clinic, Erasmus MC University Medical Center Rotterdam, Rotterdam, NetherlandsDepartment of Medical Microbiology and Infection Prevention, Amsterdam Institute for Infection and Immunity, Amsterdam UMC, University of Amsterdam, Amsterdam, NetherlandsDepartment of Viroscience, Erasmus MC University Medical Center Rotterdam, Rotterdam, NetherlandsDepartment of Internal Medicine, Infectious Diseases, University Medical Center Utrecht, Utrecht, NetherlandsDepartment of Infectious Diseases, Amsterdam UMC, Amsterdam, NetherlandsDepartment of Internal Medicine, Division Clinical Immunology, Maastricht UMC, Maastricht, NetherlandsDepartment of Rheumatology and Clinical Immunology, UMC Groningen, Groningen, NetherlandsDepartment of Infectious Diseases, Leiden University Medical Center, Leiden, NetherlandsDepartment of Internal Medicine, Radboud University Medical Center Nijmegen, Nijmegen, NetherlandsDepartment of Medical Microbiology and Infection Prevention, Amsterdam Institute for Infection and Immunity, Amsterdam UMC, University of Amsterdam, Amsterdam, NetherlandsDepartment of Viroscience, Erasmus MC University Medical Center Rotterdam, Rotterdam, Netherlands0Department of Internal Medicine, Division of Allergy & Clinical Immunology, Erasmus MC University Medical Center Rotterdam, Rotterdam, Netherlands1Department of Immunology, Erasmus MC University Medical Center Rotterdam, Rotterdam, NetherlandsPurposePrevious studies have demonstrated that the majority of patients with an inborn error of immunity (IEI) develop a spike (S)-specific IgG antibody and T-cell response after two doses of the mRNA-1273 COVID-19 vaccine, but little is known about the response to a booster vaccination. We studied the immune responses 8 weeks after booster vaccination with mRNA-based COVID-19 vaccines in 171 IEI patients. Moreover, we evaluated the clinical outcomes in these patients one year after the start of the Dutch COVID-19 vaccination campaign.MethodsThis study was embedded in a large prospective multicenter study investigating the immunogenicity of COVID-19 mRNA-based vaccines in IEI (VACOPID study). Blood samples were taken from 244 participants 8 weeks after booster vaccination. These participants included 171 IEI patients (X-linked agammaglobulinemia (XLA;N=11), combined immunodeficiency (CID;N=4), common variable immunodeficiency (CVID;N=45), isolated or undefined antibody deficiencies (N=108) and phagocyte defects (N=3)) and 73 controls. SARS-CoV-2-specific IgG titers, neutralizing antibodies, and T-cell responses were evaluated. One year after the start of the COVID-19 vaccination program, 334 study participants (239 IEI patients and 95 controls) completed a questionnaire to supplement their clinical data focusing on SARS-CoV-2 infections.ResultsAfter booster vaccination, S-specific IgG titers increased in all COVID-19 naive IEI cohorts and controls, when compared to titers at 6 months after the priming regimen. The fold-increases did not differ between controls and IEI cohorts. SARS-CoV-2-specific T-cell responses also increased equally in all cohorts after booster vaccination compared to 6 months after the priming regimen. Most SARS-CoV-2 infections during the study period occurred in the period when the Omicron variant had become dominant. The clinical course of these infections was mild, although IEI patients experienced more frequent fever and dyspnea compared to controls and their symptoms persisted longer.ConclusionOur study demonstrates that mRNA-based booster vaccination induces robust recall of memory B-cell and T-cell responses in most IEI patients. One-year clinical follow-up demonstrated that SARS-CoV-2 infections in IEI patients were mild. Given our results, we support booster campaigns with newer variant-specific COVID-19 booster vaccines to IEI patients with milder phenotypes.https://www.frontiersin.org/articles/10.3389/fimmu.2024.1390022/fullinborn errors of immunityprimary immunodeficiency disordersSARS-CoV-2mRNA-1273 COVID-19 vaccinebooster vaccinationimmunogenicity
spellingShingle Leanne P. M. van Leeuwen
Leanne P. M. van Leeuwen
Marloes Grobben
Corine H. GeurtsvanKessel
Pauline M. Ellerbroek
Godelieve J. de Bree
Judith Potjewijd
Abraham Rutgers
Hetty Jolink
Frank L. van de Veerdonk
Marit J. van Gils
Rory D. de Vries
Virgil A. S. H. Dalm
Virgil A. S. H. Dalm
VACOPID Research Group
Eric C.M. van Gorp
Faye de Wilt
Susanne Bogers
Lennert Gommers
Daryl Geers
Marianne W. van der Ent
P. Martin van Hagen
Jelle W. van Haga
Bregtje A. Lemkes
Annelou van der Veen
Rogier W. Sanders
Karlijn van der Straten
Judith A. Burger
Jacqueline van Rijswijk
Khadija Tejjani
Joey H. Bouhuijs
Karina de Leeuw
Annick A.J.M. van de Ven
S.F.J. de Kruijf-Bazen
Pieter van Paassen
Lotte Wieten
Petra H. Verbeek-Menken
Annelies van Wengen
Anke H.W. Bruns
Helen L. Leavis
Stefan Nierkens
Immunogenicity of COVID-19 booster vaccination in IEI patients and their one year clinical follow-up after start of the COVID-19 vaccination program
Frontiers in Immunology
inborn errors of immunity
primary immunodeficiency disorders
SARS-CoV-2
mRNA-1273 COVID-19 vaccine
booster vaccination
immunogenicity
title Immunogenicity of COVID-19 booster vaccination in IEI patients and their one year clinical follow-up after start of the COVID-19 vaccination program
title_full Immunogenicity of COVID-19 booster vaccination in IEI patients and their one year clinical follow-up after start of the COVID-19 vaccination program
title_fullStr Immunogenicity of COVID-19 booster vaccination in IEI patients and their one year clinical follow-up after start of the COVID-19 vaccination program
title_full_unstemmed Immunogenicity of COVID-19 booster vaccination in IEI patients and their one year clinical follow-up after start of the COVID-19 vaccination program
title_short Immunogenicity of COVID-19 booster vaccination in IEI patients and their one year clinical follow-up after start of the COVID-19 vaccination program
title_sort immunogenicity of covid 19 booster vaccination in iei patients and their one year clinical follow up after start of the covid 19 vaccination program
topic inborn errors of immunity
primary immunodeficiency disorders
SARS-CoV-2
mRNA-1273 COVID-19 vaccine
booster vaccination
immunogenicity
url https://www.frontiersin.org/articles/10.3389/fimmu.2024.1390022/full
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