High Incidence of SARS-CoV-2 Variant of Concern Breakthrough Infections Despite Residual Humoral and Cellular Immunity Induced by BNT162b2 Vaccination in Healthcare Workers: A Long-Term Follow-Up Study in Belgium

To mitigate the massive COVID-19 burden caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), several vaccination campaigns were initiated. We performed a single-center observational trial to monitor the mid- (3 months) and long-term (10 months) adaptive immune response and to docu...

Full description

Saved in:
Bibliographic Details
Published inViruses Vol. 14; no. 6; p. 1257
Main Authors Calcoen, Bas, Callewaert, Nico, Vandenbulcke, Aline, Kerstens, Winnie, Imbrechts, Maya, Vercruysse, Thomas, Dallmeier, Kai, Van Weyenbergh, Johan, Maes, Piet, Bossuyt, Xavier, Zapf, Dorinja, Dieckmann, Kersten, Callebaut, Kim, Thibaut, Hendrik Jan, Vanhoorelbeke, Karen, De Meyer, Simon F., Maes, Wim, Geukens, Nick
Format Journal Article
LanguageEnglish
Published Basel MDPI AG 09.06.2022
MDPI
Subjects
Adaptive immunity
Antibodies
Belgium
BNT162b2 vaccine
breakthrough infection
CD4 antigen
CD8 antigen
Cell-mediated immunity
Coronaviruses
COVID-19
COVID-19 infection
COVID-19 vaccines
Disease transmission
Enzymes
Health aspects
Health care
health services
healthcare workers
Humoral immunity
Immune response
Immune response (humoral)
Immune system
Immunoassay
Infections
long-term monitoring
Lymphocytes B
Lymphocytes T
Medical personnel
neutralization
Pandemics
Pathogens
Proteins
SARS-CoV-2
Serology
Severe acute respiratory syndrome coronavirus 2
T cells
Vaccination
Vaccines
variants of concern
γ-Interferon
Belgium
Canada
France
United States > US
China
Online AccessGet full text

Cover

Abstract To mitigate the massive COVID-19 burden caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), several vaccination campaigns were initiated. We performed a single-center observational trial to monitor the mid- (3 months) and long-term (10 months) adaptive immune response and to document breakthrough infections (BTI) in healthcare workers (n = 84) upon BNT162b2 vaccination in a real-world setting. Firstly, serology was determined through immunoassays. Secondly, antibody functionality was analyzed via in vitro binding inhibition and pseudovirus neutralization and circulating receptor-binding domain (RBD)-specific B cells were assessed. Moreover, the induction of SARS-CoV-2-specific T cells was investigated by an interferon-γ release assay combined with flowcytometric profiling of activated CD4+ and CD8+ T cells. Within individuals that did not experience BTI (n = 62), vaccine-induced humoral and cellular immune responses were not correlated. Interestingly, waning over time was more pronounced within humoral compared to cellular immunity. In particular, 45 of these 62 subjects no longer displayed functional neutralization against the delta variant of concern (VoC) at long-term follow-up. Noteworthily, we reported a high incidence of symptomatic BTI cases (17.11%) caused by alpha and delta VoCs, although vaccine-induced immunity was only slightly reduced compared to subjects without BTI at mid-term follow-up.
AbstractList To mitigate the massive COVID-19 burden caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), several vaccination campaigns were initiated. We performed a single-center observational trial to monitor the mid- (3 months) and long-term (10 months) adaptive immune response and to document breakthrough infections (BTI) in healthcare workers (n = 84) upon BNT162b2 vaccination in a real-world setting. Firstly, serology was determined through immunoassays. Secondly, antibody functionality was analyzed via in vitro binding inhibition and pseudovirus neutralization and circulating receptor-binding domain (RBD)-specific B cells were assessed. Moreover, the induction of SARS-CoV-2-specific T cells was investigated by an interferon-γ release assay combined with flowcytometric profiling of activated CD4+ and CD8+ T cells. Within individuals that did not experience BTI (n = 62), vaccine-induced humoral and cellular immune responses were not correlated. Interestingly, waning over time was more pronounced within humoral compared to cellular immunity. In particular, 45 of these 62 subjects no longer displayed functional neutralization against the delta variant of concern (VoC) at long-term follow-up. Noteworthily, we reported a high incidence of symptomatic BTI cases (17.11%) caused by alpha and delta VoCs, although vaccine-induced immunity was only slightly reduced compared to subjects without BTI at mid-term follow-up.
To mitigate the massive COVID-19 burden caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), several vaccination campaigns were initiated. We performed a single-center observational trial to monitor the mid- (3 months) and long-term (10 months) adaptive immune response and to document breakthrough infections (BTI) in healthcare workers (n = 84) upon BNT162b2 vaccination in a real-world setting. Firstly, serology was determined through immunoassays. Secondly, antibody functionality was analyzed via in vitro binding inhibition and pseudovirus neutralization and circulating receptor-binding domain (RBD)-specific B cells were assessed. Moreover, the induction of SARS-CoV-2-specific T cells was investigated by an interferon-γ release assay combined with flowcytometric profiling of activated CD4+ and CD8+ T cells. Within individuals that did not experience BTI (n = 62), vaccine-induced humoral and cellular immune responses were not correlated. Interestingly, waning over time was more pronounced within humoral compared to cellular immunity. In particular, 45 of these 62 subjects no longer displayed functional neutralization against the delta variant of concern (VoC) at long-term follow-up. Noteworthily, we reported a high incidence of symptomatic BTI cases (17.11%) caused by alpha and delta VoCs, although vaccine-induced immunity was only slightly reduced compared to subjects without BTI at mid-term follow-up.To mitigate the massive COVID-19 burden caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), several vaccination campaigns were initiated. We performed a single-center observational trial to monitor the mid- (3 months) and long-term (10 months) adaptive immune response and to document breakthrough infections (BTI) in healthcare workers (n = 84) upon BNT162b2 vaccination in a real-world setting. Firstly, serology was determined through immunoassays. Secondly, antibody functionality was analyzed via in vitro binding inhibition and pseudovirus neutralization and circulating receptor-binding domain (RBD)-specific B cells were assessed. Moreover, the induction of SARS-CoV-2-specific T cells was investigated by an interferon-γ release assay combined with flowcytometric profiling of activated CD4+ and CD8+ T cells. Within individuals that did not experience BTI (n = 62), vaccine-induced humoral and cellular immune responses were not correlated. Interestingly, waning over time was more pronounced within humoral compared to cellular immunity. In particular, 45 of these 62 subjects no longer displayed functional neutralization against the delta variant of concern (VoC) at long-term follow-up. Noteworthily, we reported a high incidence of symptomatic BTI cases (17.11%) caused by alpha and delta VoCs, although vaccine-induced immunity was only slightly reduced compared to subjects without BTI at mid-term follow-up.
To mitigate the massive COVID-19 burden caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), several vaccination campaigns were initiated. We performed a single-center observational trial to monitor the mid- (3 months) and long-term (10 months) adaptive immune response and to document breakthrough infections (BTI) in healthcare workers ( n = 84) upon BNT162b2 vaccination in a real-world setting. Firstly, serology was determined through immunoassays. Secondly, antibody functionality was analyzed via in vitro binding inhibition and pseudovirus neutralization and circulating receptor-binding domain (RBD)-specific B cells were assessed. Moreover, the induction of SARS-CoV-2-specific T cells was investigated by an interferon-γ release assay combined with flowcytometric profiling of activated CD4 + and CD8 + T cells. Within individuals that did not experience BTI ( n = 62), vaccine-induced humoral and cellular immune responses were not correlated. Interestingly, waning over time was more pronounced within humoral compared to cellular immunity. In particular, 45 of these 62 subjects no longer displayed functional neutralization against the delta variant of concern (VoC) at long-term follow-up. Noteworthily, we reported a high incidence of symptomatic BTI cases (17.11%) caused by alpha and delta VoCs, although vaccine-induced immunity was only slightly reduced compared to subjects without BTI at mid-term follow-up.
To mitigate the massive COVID-19 burden caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), several vaccination campaigns were initiated. We performed a single-center observational trial to monitor the mid- (3 months) and long-term (10 months) adaptive immune response and to document breakthrough infections (BTI) in healthcare workers (n = 84) upon BNT162b2 vaccination in a real-world setting. Firstly, serology was determined through immunoassays. Secondly, antibody functionality was analyzed via in vitro binding inhibition and pseudovirus neutralization and circulating receptor-binding domain (RBD)-specific B cells were assessed. Moreover, the induction of SARS-CoV-2-specific T cells was investigated by an interferon-γ release assay combined with flowcytometric profiling of activated CD4[sup.+] and CD8[sup.+] T cells. Within individuals that did not experience BTI (n = 62), vaccine-induced humoral and cellular immune responses were not correlated. Interestingly, waning over time was more pronounced within humoral compared to cellular immunity. In particular, 45 of these 62 subjects no longer displayed functional neutralization against the delta variant of concern (VoC) at long-term follow-up. Noteworthily, we reported a high incidence of symptomatic BTI cases (17.11%) caused by alpha and delta VoCs, although vaccine-induced immunity was only slightly reduced compared to subjects without BTI at mid-term follow-up.
To mitigate the massive COVID-19 burden caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), several vaccination campaigns were initiated. We performed a single-center observational trial to monitor the mid- (3 months) and long-term (10 months) adaptive immune response and to document breakthrough infections (BTI) in healthcare workers (n = 84) upon BNT162b2 vaccination in a real-world setting. Firstly, serology was determined through immunoassays. Secondly, antibody functionality was analyzed via in vitro binding inhibition and pseudovirus neutralization and circulating receptor-binding domain (RBD)-specific B cells were assessed. Moreover, the induction of SARS-CoV-2-specific T cells was investigated by an interferon-γ release assay combined with flowcytometric profiling of activated CD4⁺ and CD8⁺ T cells. Within individuals that did not experience BTI (n = 62), vaccine-induced humoral and cellular immune responses were not correlated. Interestingly, waning over time was more pronounced within humoral compared to cellular immunity. In particular, 45 of these 62 subjects no longer displayed functional neutralization against the delta variant of concern (VoC) at long-term follow-up. Noteworthily, we reported a high incidence of symptomatic BTI cases (17.11%) caused by alpha and delta VoCs, although vaccine-induced immunity was only slightly reduced compared to subjects without BTI at mid-term follow-up.
Audience Academic
Author Imbrechts, Maya
Geukens, Nick
Callewaert, Nico
Dallmeier, Kai
Vandenbulcke, Aline
Vercruysse, Thomas
Kerstens, Winnie
Maes, Wim
Zapf, Dorinja
De Meyer, Simon F.
Van Weyenbergh, Johan
Callebaut, Kim
Thibaut, Hendrik Jan
Dieckmann, Kersten
Bossuyt, Xavier
Maes, Piet
Vanhoorelbeke, Karen
Calcoen, Bas
AuthorAffiliation 7 Department of Microbiology, Immunology and Transplantation, KU Leuven, 3000 Leuven, Belgium; xavier.bossuyt@uzleuven.be
8 Department of Laboratory Medicine, University Hospitals Leuven, 3000 Leuven, Belgium
4 PharmAbs, the KU Leuven Antibody Center, KU Leuven, 3000 Leuven, Belgium; maya.imbrechts@kuleuven.be (M.I.); nick.geukens@kuleuven.be (N.G.)
6 Laboratory for Clinical and Epidemiological Virology, KU Leuven Rega Institute, 3000 Leuven, Belgium; johan.vanweyenbergh@kuleuven.be (J.V.W.); piet.maes@kuleuven.be (P.M.)
3 Laboratory of Virology and Chemotherapy, Translational Platform Virology and Chemotherapy, Department of Microbiology, Immunology and Transplantation, KU Leuven Rega Institute, 3000 Leuven, Belgium; winnie.kerstens@kuleuven.be (W.K.); thomas.vercruysse@kuleuven.be (T.V.); hendrikjan.thibaut@kuleuven.be (H.J.T.)
2 AZ Groeninge Hospital, Department of Laboratory Medicine, 8500 Kortrijk, Belgium; kimcallebaut@hotmail.com (K.C.); nico.callewaert@azgroeninge.be (N.C.)
1 Laborat
AuthorAffiliation_xml – name: 5 Laboratory of Virology, Molecular Vaccinology and Vaccine Discovery, Department of Microbiology, Immunology and Transplantation, KU Leuven Rega Institute, 3000 Leuven, Belgium; kai.dallmeier@kuleuven.be
– name: 3 Laboratory of Virology and Chemotherapy, Translational Platform Virology and Chemotherapy, Department of Microbiology, Immunology and Transplantation, KU Leuven Rega Institute, 3000 Leuven, Belgium; winnie.kerstens@kuleuven.be (W.K.); thomas.vercruysse@kuleuven.be (T.V.); hendrikjan.thibaut@kuleuven.be (H.J.T.)
– name: 4 PharmAbs, the KU Leuven Antibody Center, KU Leuven, 3000 Leuven, Belgium; maya.imbrechts@kuleuven.be (M.I.); nick.geukens@kuleuven.be (N.G.)
– name: 1 Laboratory for Thrombosis Research, KU Leuven Campus Kulak Kortrijk, 8500 Kortrijk, Belgium; bas.calcoen@kuleuven.be (B.C.); aline.vandenbulcke@kuleuven.be (A.V.); karen.vanhoorelbeke@kuleuven.be (K.V.); simon.demeyer@kuleuven.be (S.F.D.M.)
– name: 8 Department of Laboratory Medicine, University Hospitals Leuven, 3000 Leuven, Belgium
– name: 9 Institut für Experimentelle Immunologie, EUROIMMUN Medizinische Labordiagnostika AG, 23552 Lübeck, Germany; d.zapf@euroimmun.de (D.Z.); k.dieckmann@euroimmun.de (K.D.)
– name: 7 Department of Microbiology, Immunology and Transplantation, KU Leuven, 3000 Leuven, Belgium; xavier.bossuyt@uzleuven.be
– name: 6 Laboratory for Clinical and Epidemiological Virology, KU Leuven Rega Institute, 3000 Leuven, Belgium; johan.vanweyenbergh@kuleuven.be (J.V.W.); piet.maes@kuleuven.be (P.M.)
– name: 2 AZ Groeninge Hospital, Department of Laboratory Medicine, 8500 Kortrijk, Belgium; kimcallebaut@hotmail.com (K.C.); nico.callewaert@azgroeninge.be (N.C.)
Author_xml – sequence: 1
  givenname: Bas
  surname: Calcoen
  fullname: Calcoen, Bas
– sequence: 2
  givenname: Nico
  surname: Callewaert
  fullname: Callewaert, Nico
– sequence: 3
  givenname: Aline
  surname: Vandenbulcke
  fullname: Vandenbulcke, Aline
– sequence: 4
  givenname: Winnie
  surname: Kerstens
  fullname: Kerstens, Winnie
– sequence: 5
  givenname: Maya
  orcidid: 0000-0002-4467-9831
  surname: Imbrechts
  fullname: Imbrechts, Maya
– sequence: 6
  givenname: Thomas
  orcidid: 0000-0002-8649-777X
  surname: Vercruysse
  fullname: Vercruysse, Thomas
– sequence: 7
  givenname: Kai
  orcidid: 0000-0002-8117-9166
  surname: Dallmeier
  fullname: Dallmeier, Kai
– sequence: 8
  givenname: Johan
  orcidid: 0000-0003-3234-8426
  surname: Van Weyenbergh
  fullname: Van Weyenbergh, Johan
– sequence: 9
  givenname: Piet
  surname: Maes
  fullname: Maes, Piet
– sequence: 10
  givenname: Xavier
  surname: Bossuyt
  fullname: Bossuyt, Xavier
– sequence: 11
  givenname: Dorinja
  surname: Zapf
  fullname: Zapf, Dorinja
– sequence: 12
  givenname: Kersten
  surname: Dieckmann
  fullname: Dieckmann, Kersten
– sequence: 13
  givenname: Kim
  surname: Callebaut
  fullname: Callebaut, Kim
– sequence: 14
  givenname: Hendrik Jan
  orcidid: 0000-0001-5785-8276
  surname: Thibaut
  fullname: Thibaut, Hendrik Jan
– sequence: 15
  givenname: Karen
  surname: Vanhoorelbeke
  fullname: Vanhoorelbeke, Karen
– sequence: 16
  givenname: Simon F.
  surname: De Meyer
  fullname: De Meyer, Simon F.
– sequence: 17
  givenname: Wim
  orcidid: 0000-0002-4629-6674
  surname: Maes
  fullname: Maes, Wim
– sequence: 18
  givenname: Nick
  surname: Geukens
  fullname: Geukens, Nick
BookMark eNqNUstu1DAUjVARfcCCP7DEBhZp_UjshAXSzECZkSqQOtOyjBz7esZtYg9OUjT_yQfhtFWhVRfIi2tfn3OufXQOkz3nHSTJW4KPGSvxyQ3JMCc0Fy-SA1KWZZqVJN_7Z7-fHHbdFcacl1i8SvZZLjIuaHGQ_J7b9QYtnLIanALkDVpOzpfpzF-mFF3KYKXrx-7Mx-vg0DSAvO43wQ-3PAOqt9516DN0W9sDOofO6kE2aD60PsQqnUYzaJqhkQEt2nZwtt9Fph4UaFTv0PTbinBaj9OUsk6Oesg6NAfZ9BslA6AfPlxD6D6iCTrzbp2uILTo1DeN_5VebNGyH_RupEyhWduhfZ28NLLp4M19PUouTr-sZvP07PvXxWxylqo8430qFS8Z1oxITSUTea0l5IxDjQXN4jnDBee1UEphrQ0R2NS5obrQmaiNwDk7ShZ3utrLq2obbCvDrvLSVrcNH9aVDL1VDVTMYGKkyIDWKitKIRkwmRtlDMMU4yJqfbrT2g51C1qB66N7j0Qf3zi7qdb-piopLUiOo8D7e4Hgfw7Q9VVrOxWNlw780FVUkILmFPP_gPKC4JgRziP03RPolR-Ci65GlCgLzgRlf1FrGf9qnfHxiWoUrSaCUpwxlo92HT-DiktDa1WMtLGx_4jw4Y6ggu-6AObBDoKrMfnVQ_Ij9uQJVtn-NktxiG2eYfwB2r8ExQ
CitedBy_id crossref_primary_10_3390_vaccines11020216
crossref_primary_10_1177_10815589231158041
crossref_primary_10_3389_fimmu_2023_1100594
crossref_primary_10_1080_22221751_2023_2287118
crossref_primary_10_3389_fimmu_2023_1145652
crossref_primary_10_3389_fimmu_2023_1050037
crossref_primary_10_3390_jcm13092523
Cites_doi 10.3389/fimmu.2021.740708
10.1101/2022.01.17.22269081
10.1007/s11427-020-1637-5
10.3390/vaccines9020147
10.1016/j.ebiom.2021.103574
10.1016/j.scr.2020.102125
10.1371/journal.pone.0263328
10.1136/annrheumdis-2021-221097
10.3389/fimmu.2022.840136
10.3389/fimmu.2021.722766
10.1002/cti2.1245
10.1371/journal.pone.0249499
10.1126/science.abc5902
10.1038/s41586-020-2639-4
10.1038/s41586-021-03738-2
10.1681/ASN.2021070908
10.1001/jama.2021.23641
10.1007/s40620-022-01257-5
10.1016/j.cub.2021.06.049
10.3390/v13112261
10.1038/s41586-020-2012-7
10.1016/j.jviromet.2010.08.006
10.1038/s41586-021-03324-6
10.1016/j.immuni.2021.08.001
10.1016/j.cell.2020.09.049
10.5937/jomb0-32373
10.3390/vaccines10020272
10.1093/ofid/ofab553
10.3389/fmed.2021.815870
10.1038/s41467-021-26154-6
10.1126/scitranslmed.abn8057
10.3390/vaccines10020285
10.1016/j.chom.2022.01.003
10.1038/s41586-020-2550-z
10.1007/s11739-021-02857-y
10.1016/S2213-2600(21)00220-4
10.3389/fimmu.2021.704773
10.3390/vaccines10020322
10.1126/science.abf4063
10.3390/biomedicines9080868
10.1080/21645515.2021.1984124
10.1016/S0140-6736(03)14630-2
10.3390/v14040802
10.3389/fimmu.2021.657711
10.1111/jcmm.17186
10.1016/j.esmoop.2021.100272
10.3389/fimmu.2021.727850
10.1016/j.cmi.2022.01.019
10.1089/pop.2020.0255
10.1101/2021.11.25.470011
10.1101/2021.09.07.21263229
10.1136/annrheumdis-2021-220503
10.1038/s41467-021-26884-7
10.1002/cti2.1341
10.3390/vaccines9060672
10.1038/s41586-020-2814-7
10.1038/s41586-020-3035-9
10.1016/j.vaccine.2021.11.092
10.2807/1560-7917.ES.2021.26.37.2100824
10.2215/CJN.03500321
10.1016/j.lanepe.2021.100208
10.1056/NEJMoa2105000
10.3390/pathogens11010067
ContentType Journal Article
Copyright COPYRIGHT 2022 MDPI AG
2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2022 by the authors. 2022
Copyright_xml – notice: COPYRIGHT 2022 MDPI AG
– notice: 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: 2022 by the authors. 2022
DBID AAYXX
CITATION
3V.
7U9
7X7
7XB
88E
8FE
8FH
8FI
8FJ
8FK
ABUWG
AFKRA
AZQEC
BBNVY
BENPR
BHPHI
CCPQU
COVID
DWQXO
FYUFA
GHDGH
GNUQQ
H94
HCIFZ
K9.
LK8
M0S
M1P
M7P
PHGZM
PHGZT
PIMPY
PJZUB
PKEHL
PPXIY
PQEST
PQGLB
PQQKQ
PQUKI
PRINS
7X8
7S9
L.6
5PM
DOA
DOI 10.3390/v14061257
DatabaseName CrossRef
ProQuest Central (Corporate)
Virology and AIDS Abstracts
Health & Medical Collection (ProQuest)
ProQuest Central (purchase pre-March 2016)
Medical Database (Alumni Edition)
ProQuest SciTech Collection
ProQuest Natural Science Collection
Hospital Premium Collection
Hospital Premium Collection (Alumni Edition)
ProQuest Central (Alumni) (purchase pre-March 2016)
ProQuest Central (Alumni)
ProQuest Central UK/Ireland
ProQuest Central Essentials
Biological Science Collection
ProQuest Central
Natural Science Collection
ProQuest One
Coronavirus Research Database
ProQuest Central Korea
Health Research Premium Collection
Health Research Premium Collection (Alumni)
ProQuest Central Student
AIDS and Cancer Research Abstracts
SciTech Premium Collection
ProQuest Health & Medical Complete (Alumni)
Biological Sciences
ProQuest Health & Medical Collection
Medical Database
Biological Science Database
ProQuest Central Premium
ProQuest One Academic (New)
Publicly Available Content Database (ProQuest)
ProQuest Health & Medical Research Collection
ProQuest One Academic Middle East (New)
ProQuest One Health & Nursing
ProQuest One Academic Eastern Edition (DO NOT USE)
ProQuest One Applied & Life Sciences
ProQuest One Academic
ProQuest One Academic UKI Edition
ProQuest Central China
MEDLINE - Academic
AGRICOLA
AGRICOLA - Academic
PubMed Central (Full Participant titles)
DOAJ Directory of Open Access Journals
DatabaseTitle CrossRef
Publicly Available Content Database
ProQuest Central Student
ProQuest One Academic Middle East (New)
ProQuest Central Essentials
ProQuest Health & Medical Complete (Alumni)
ProQuest Central (Alumni Edition)
SciTech Premium Collection
ProQuest One Community College
ProQuest One Health & Nursing
ProQuest Natural Science Collection
ProQuest Central China
ProQuest Central
ProQuest One Applied & Life Sciences
ProQuest Health & Medical Research Collection
Health Research Premium Collection
Health and Medicine Complete (Alumni Edition)
Natural Science Collection
ProQuest Central Korea
Health & Medical Research Collection
Biological Science Collection
AIDS and Cancer Research Abstracts
ProQuest Central (New)
ProQuest Medical Library (Alumni)
Virology and AIDS Abstracts
ProQuest Biological Science Collection
ProQuest One Academic Eastern Edition
Coronavirus Research Database
ProQuest Hospital Collection
Health Research Premium Collection (Alumni)
Biological Science Database
ProQuest SciTech Collection
ProQuest Hospital Collection (Alumni)
ProQuest Health & Medical Complete
ProQuest Medical Library
ProQuest One Academic UKI Edition
ProQuest One Academic
ProQuest One Academic (New)
ProQuest Central (Alumni)
MEDLINE - Academic
AGRICOLA
AGRICOLA - Academic
DatabaseTitleList Publicly Available Content Database
MEDLINE - Academic


AGRICOLA

CrossRef
Database_xml – sequence: 1
  dbid: DOA
  name: DOAJ Directory of Open Access Journals
  url: https://www.doaj.org/
  sourceTypes: Open Website
– sequence: 2
  dbid: BENPR
  name: ProQuest Central
  url: https://www.proquest.com/central
  sourceTypes: Aggregation Database
DeliveryMethod fulltext_linktorsrc
Discipline Biology
EISSN 1999-4915
ExternalDocumentID oai_doaj_org_article_3f01fa74e2bc4897a3e3a5fcff302008
PMC9228150
A722043355
10_3390_v14061257
GeographicLocations Belgium
Canada
France
United States--US
China
GeographicLocations_xml – name: Belgium
– name: China
– name: Canada
– name: France
– name: United States--US
GroupedDBID ---
2WC
53G
5VS
7X7
88E
8FE
8FH
8FI
8FJ
A8Z
AADQD
AAFWJ
AAHBH
AAYXX
ABDBF
ABUWG
ACUHS
AFKRA
AFPKN
AFZYC
ALIPV
ALMA_UNASSIGNED_HOLDINGS
BBNVY
BENPR
BHPHI
BPHCQ
BVXVI
CCPQU
CITATION
DIK
E3Z
EBD
ESX
FYUFA
GROUPED_DOAJ
GX1
HCIFZ
HMCUK
HYE
IAO
IHR
ITC
KQ8
LK8
M1P
M48
M7P
MODMG
M~E
O5R
O5S
OK1
PGMZT
PHGZM
PHGZT
PIMPY
PQQKQ
PROAC
PSQYO
RPM
TR2
TUS
UKHRP
PMFND
3V.
7U9
7XB
8FK
AZQEC
COVID
DWQXO
GNUQQ
H94
K9.
PJZUB
PKEHL
PPXIY
PQEST
PQGLB
PQUKI
PRINS
7X8
7S9
L.6
5PM
PUEGO
ID FETCH-LOGICAL-c546t-ac6930d31ad2a375bdae536eb072437540866b7ccc0ddf170fb5f2d8d47bf7053
IEDL.DBID M48
ISSN 1999-4915
IngestDate Wed Aug 27 01:26:57 EDT 2025
Thu Aug 21 18:06:03 EDT 2025
Thu Jul 10 22:27:48 EDT 2025
Mon Jul 21 10:11:19 EDT 2025
Fri Jul 25 10:15:35 EDT 2025
Tue Jun 17 22:21:55 EDT 2025
Tue Jun 10 21:15:09 EDT 2025
Tue Jul 01 02:48:36 EDT 2025
Thu Apr 24 22:58:23 EDT 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 6
Language English
License https://creativecommons.org/licenses/by/4.0
Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c546t-ac6930d31ad2a375bdae536eb072437540866b7ccc0ddf170fb5f2d8d47bf7053
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 14
ObjectType-Article-2
ObjectType-Feature-1
content type line 23
ObjectType-Undefined-3
These authors contributed equally to this work.
ORCID 0000-0002-8649-777X
0000-0002-8117-9166
0000-0002-4629-6674
0000-0001-5785-8276
0000-0002-4467-9831
0000-0003-3234-8426
OpenAccessLink http://journals.scholarsportal.info/openUrl.xqy?doi=10.3390/v14061257
PMID 35746728
PQID 2679863723
PQPubID 2032319
ParticipantIDs doaj_primary_oai_doaj_org_article_3f01fa74e2bc4897a3e3a5fcff302008
pubmedcentral_primary_oai_pubmedcentral_nih_gov_9228150
proquest_miscellaneous_2718252060
proquest_miscellaneous_2681035766
proquest_journals_2679863723
gale_infotracmisc_A722043355
gale_infotracacademiconefile_A722043355
crossref_primary_10_3390_v14061257
crossref_citationtrail_10_3390_v14061257
ProviderPackageCode CITATION
AAYXX
PublicationCentury 2000
PublicationDate 20220609
PublicationDateYYYYMMDD 2022-06-09
PublicationDate_xml – month: 6
  year: 2022
  text: 20220609
  day: 9
PublicationDecade 2020
PublicationPlace Basel
PublicationPlace_xml – name: Basel
PublicationTitle Viruses
PublicationYear 2022
Publisher MDPI AG
MDPI
Publisher_xml – name: MDPI AG
– name: MDPI
References ref_50
Kreye (ref_1) 2020; 183
Tan (ref_75) 2020; 584
Zhou (ref_5) 2020; 579
Zitt (ref_48) 2021; 12
Bromberg (ref_27) 2021; 72
ref_14
Wang (ref_51) 2021; 592
ref_13
Lustig (ref_49) 2021; 9
Cacho (ref_53) 2022; 35
ref_12
ref_11
ref_10
ref_54
Terreri (ref_68) 2022; 30
ref_52
ref_16
ref_15
ref_59
Sahin (ref_70) 2020; 586
ref_60
Ponticelli (ref_78) 2021; 17
Turner (ref_67) 2021; 596
Dan (ref_20) 2021; 371
ref_24
ref_23
ref_22
Zhong (ref_3) 2003; 362
ref_21
ref_63
Achiron (ref_46) 2021; 14
Painter (ref_74) 2021; 54
Groenveld (ref_89) 2022; 9
ref_29
Vercruysse (ref_34) 2021; 590
Reynders (ref_73) 2021; 32
Blanquart (ref_28) 2021; 26
Mulligan (ref_69) 2020; 586
Hacisuleyman (ref_26) 2021; 384
Ciabattini (ref_17) 2021; 12
Colavita (ref_85) 2022; 8
Xu (ref_4) 2020; 63
Carbonell (ref_18) 2021; 12
Kaplan (ref_45) 2021; 80
ref_36
Lombardi (ref_19) 2021; 12
ref_79
Brouwer (ref_65) 2020; 369
ref_33
ref_77
ref_32
ref_76
Bahl (ref_30) 2021; 4
ref_31
Xiaojie (ref_64) 2021; 50
Whitt (ref_35) 2010; 169
Moyon (ref_71) 2021; 81
Oster (ref_81) 2022; 28
ref_39
Hirotsu (ref_56) 2021; 12
ref_38
Otto (ref_25) 2021; 31
Lasagna (ref_72) 2021; 6
Rovida (ref_86) 2021; 12
Amodio (ref_44) 2021; 12
Spitzer (ref_58) 2022; 327
Katz (ref_82) 2022; 40
Lambrechts (ref_37) 2021; 12
ref_80
Naito (ref_83) 2021; 18
Salvagno (ref_61) 2021; 40
Romani (ref_8) 2021; 24
ref_43
ref_87
ref_42
Grupper (ref_47) 2021; 16
ref_41
ref_40
ref_84
Byazrova (ref_66) 2021; 10
ref_2
Naaber (ref_62) 2021; 10
Casado (ref_55) 2021; 10
ref_9
Evans (ref_88) 2022; 14
Bleotu (ref_57) 2022; 26
ref_7
ref_6
References_xml – ident: ref_9
– ident: ref_32
– ident: ref_80
– volume: 12
  start-page: 3751
  year: 2021
  ident: ref_17
  article-title: Evidence of SARS-CoV-2-Specific Memory B Cells Six Months After Vaccination with the BNT162b2 mRNA Vaccine
  publication-title: Front. Immunol.
  doi: 10.3389/fimmu.2021.740708
– volume: 12
  start-page: 3970
  year: 2021
  ident: ref_18
  article-title: Induction of High Levels of Specific Humoral and Cellular Responses to SARS-CoV-2 After the Administration of COVID-19 mRNA Vaccines Requires Several Days
  publication-title: Front. Immunol.
– volume: 4
  start-page: 100065
  year: 2021
  ident: ref_30
  article-title: Vaccination reduces need for emergency care in breakthrough COVID-19 infections: A multicenter cohort study
  publication-title: Lancet Reg. Health Am.
– ident: ref_22
  doi: 10.1101/2022.01.17.22269081
– volume: 63
  start-page: 457
  year: 2020
  ident: ref_4
  article-title: Evolution of the novel coronavirus from the ongoing Wuhan outbreak and modeling of its spike protein for risk of human transmission
  publication-title: Sci. China Life Sci.
  doi: 10.1007/s11427-020-1637-5
– ident: ref_16
  doi: 10.3390/vaccines9020147
– volume: 72
  start-page: 103574
  year: 2021
  ident: ref_27
  article-title: The BNT162b2 vaccine effectiveness against new COVID-19 cases and complications of breakthrough cases: A nation-wide retrospective longitudinal multiple cohort analysis using individualised data
  publication-title: EBioMedicine
  doi: 10.1016/j.ebiom.2021.103574
– volume: 50
  start-page: 102125
  year: 2021
  ident: ref_64
  article-title: Neutralizing antibodies targeting SARS-CoV-2 spike protein
  publication-title: Stem Cell Res.
  doi: 10.1016/j.scr.2020.102125
– ident: ref_39
– ident: ref_84
  doi: 10.1371/journal.pone.0263328
– ident: ref_42
– ident: ref_23
– volume: 81
  start-page: 575
  year: 2021
  ident: ref_71
  article-title: BNT162b2 vaccine-induced humoral and cellular responses against SARS-CoV-2 variants in systemic lupus erythematosus
  publication-title: Ann. Rheum. Dis.
  doi: 10.1136/annrheumdis-2021-221097
– ident: ref_87
  doi: 10.3389/fimmu.2022.840136
– volume: 12
  start-page: 3457
  year: 2021
  ident: ref_56
  article-title: Robust Antibody Responses to the BNT162b2 mRNA Vaccine Occur Within a Week After the First Dose in Previously Infected Individuals and After the Second Dose in Uninfected Individuals
  publication-title: Front. Immunol.
  doi: 10.3389/fimmu.2021.722766
– volume: 10
  start-page: e1245
  year: 2021
  ident: ref_66
  article-title: Pattern of circulating SARS-CoV-2-specific antibody-secreting and memory B-cell generation in patients with acute COVID-19
  publication-title: Clin. Transl. Immunol.
  doi: 10.1002/cti2.1245
– ident: ref_77
– ident: ref_59
  doi: 10.1371/journal.pone.0249499
– ident: ref_31
– volume: 14
  start-page: 17562864211012835
  year: 2021
  ident: ref_46
  article-title: Humoral immune response to COVID-19 mRNA vaccine in patients with multiple sclerosis treated with high-efficacy disease-modifying therapies
  publication-title: Ther. Adv. Neurol. Disord.
– volume: 369
  start-page: 643
  year: 2020
  ident: ref_65
  article-title: Potent neutralizing antibodies from COVID-19 patients define multiple targets of vulnerability
  publication-title: Science
  doi: 10.1126/science.abc5902
– volume: 586
  start-page: 589
  year: 2020
  ident: ref_69
  article-title: Phase I/II study of COVID-19 RNA vaccine BNT162b1 in adults
  publication-title: Nature
  doi: 10.1038/s41586-020-2639-4
– volume: 596
  start-page: 109
  year: 2021
  ident: ref_67
  article-title: SARS-CoV-2 mRNA vaccines induce persistent human germinal centre responses
  publication-title: Nature
  doi: 10.1038/s41586-021-03738-2
– ident: ref_10
– volume: 32
  start-page: 3208
  year: 2021
  ident: ref_73
  article-title: Predictors and Dynamics of the Humoral and Cellular Immune Response to SARS-CoV-2 mRNA Vaccines in Hemodialysis Patients: A Multicenter Observational Study
  publication-title: J. Am. Soc. Nephrol.
  doi: 10.1681/ASN.2021070908
– volume: 327
  start-page: 341
  year: 2022
  ident: ref_58
  article-title: Association of a Third Dose of BNT162b2 Vaccine with Incidence of SARS-CoV-2 Infection among Health Care Workers in Israel
  publication-title: JAMA J. Am. Med. Assoc.
  doi: 10.1001/jama.2021.23641
– volume: 35
  start-page: 769
  year: 2022
  ident: ref_53
  article-title: Incidence of severe breakthrough SARS-CoV-2 infections in vaccinated kidney transplant and haemodialysis patients
  publication-title: J. Nephrol.
  doi: 10.1007/s40620-022-01257-5
– volume: 31
  start-page: R918
  year: 2021
  ident: ref_25
  article-title: The origins and potential future of SARS-CoV-2 variants of concern in the evolving COVID-19 pandemic
  publication-title: Curr. Biol.
  doi: 10.1016/j.cub.2021.06.049
– ident: ref_13
– ident: ref_21
  doi: 10.3390/v13112261
– ident: ref_38
– volume: 579
  start-page: 270
  year: 2020
  ident: ref_5
  article-title: A pneumonia outbreak associated with a new coronavirus of probable bat origin
  publication-title: Nature
  doi: 10.1038/s41586-020-2012-7
– volume: 169
  start-page: 365
  year: 2010
  ident: ref_35
  article-title: Generation of VSV pseudotypes using recombinant ΔG-VSV for studies on virus entry, identification of entry inhibitors, and immune responses to vaccines
  publication-title: J. Virol. Methods
  doi: 10.1016/j.jviromet.2010.08.006
– volume: 592
  start-page: 616
  year: 2021
  ident: ref_51
  article-title: mRNA vaccine-elicited antibodies to SARS-CoV-2 and circulating variants
  publication-title: Nature
  doi: 10.1038/s41586-021-03324-6
– volume: 54
  start-page: 2133
  year: 2021
  ident: ref_74
  article-title: Rapid induction of antigen-specific CD4+ T cells is associated with coordinated humoral and cellular immunity to SARS-CoV-2 mRNA vaccination
  publication-title: Immunity
  doi: 10.1016/j.immuni.2021.08.001
– volume: 183
  start-page: 1058
  year: 2020
  ident: ref_1
  article-title: A Therapeutic Non-self-reactive SARS-CoV-2 Antibody Protects from Lung Pathology in a COVID-19 Hamster Model
  publication-title: Cell
  doi: 10.1016/j.cell.2020.09.049
– ident: ref_7
– volume: 40
  start-page: 327
  year: 2021
  ident: ref_61
  article-title: Anti-spike s1 iga, anti-spike trimeric igg, and anti-spike rbd igg response after bnt162b2 covid-19 mrna vaccination in healthcare workers
  publication-title: J. Med. Biochem.
  doi: 10.5937/jomb0-32373
– ident: ref_79
  doi: 10.3390/vaccines10020272
– volume: 9
  start-page: ofab553
  year: 2022
  ident: ref_89
  article-title: In-depth Characterization of Vaccine Breakthrough Infections with SARS-CoV-2 among Health Care Workers in a Dutch Academic Medical Center
  publication-title: Open Forum Infect. Dis.
  doi: 10.1093/ofid/ofab553
– ident: ref_24
– volume: 8
  start-page: 815870
  year: 2022
  ident: ref_85
  article-title: Virological and Serological Characterisation of SARS-CoV-2 Infections Diagnosed After mRNA BNT162b2 Vaccination Between December 2020 and March 2021
  publication-title: Front. Med.
  doi: 10.3389/fmed.2021.815870
– volume: 12
  start-page: 6032
  year: 2021
  ident: ref_86
  article-title: SARS-CoV-2 vaccine breakthrough infections with the alpha variant are asymptomatic or mildly symptomatic among health care workers
  publication-title: Nat. Commun.
  doi: 10.1038/s41467-021-26154-6
– volume: 14
  start-page: eabn8057
  year: 2022
  ident: ref_88
  article-title: Neutralizing antibody responses elicited by SARS-CoV-2 mRNA vaccination wane over time and are boosted by breakthrough infection
  publication-title: Sci. Transl. Med.
  doi: 10.1126/scitranslmed.abn8057
– ident: ref_11
– ident: ref_63
  doi: 10.3390/vaccines10020285
– volume: 30
  start-page: 400
  year: 2022
  ident: ref_68
  article-title: Persistent B cell memory after SARS-CoV-2 vaccination is functional during breakthrough infections
  publication-title: Cell Host Microbe.
  doi: 10.1016/j.chom.2022.01.003
– volume: 584
  start-page: 457
  year: 2020
  ident: ref_75
  article-title: SARS-CoV-2-specific T cell immunity in cases of COVID-19 and SARS, and uninfected controls
  publication-title: Nature
  doi: 10.1038/s41586-020-2550-z
– volume: 17
  start-page: 481
  year: 2021
  ident: ref_78
  article-title: Response to BNT162b2 mRNA COVID-19 vaccine among healthcare workers in Italy: A 3-month follow-up
  publication-title: Intern. Emerg. Med.
  doi: 10.1007/s11739-021-02857-y
– volume: 9
  start-page: 999
  year: 2021
  ident: ref_49
  article-title: BNT162b2 COVID-19 vaccine and correlates of humoral immune responses and dynamics: A prospective, single-centre, longitudinal cohort study in health-care workers
  publication-title: Lancet Respir. Med.
  doi: 10.1016/S2213-2600(21)00220-4
– volume: 12
  start-page: 2390
  year: 2021
  ident: ref_48
  article-title: The Safety and Immunogenicity of the mRNA-BNT162b2 SARS-CoV-2 Vaccine in Hemodialysis Patients
  publication-title: Front. Immunol.
  doi: 10.3389/fimmu.2021.704773
– ident: ref_52
  doi: 10.3390/vaccines10020322
– volume: 371
  start-page: eabf4063
  year: 2021
  ident: ref_20
  article-title: Immunological memory to SARS-CoV-2 assessed for up to 8 months after infection
  publication-title: Science
  doi: 10.1126/science.abf4063
– ident: ref_50
  doi: 10.3390/biomedicines9080868
– ident: ref_40
– volume: 18
  start-page: 1
  year: 2021
  ident: ref_83
  article-title: Real-world evidence for the effectiveness and breakthrough of BNT162b2 mRNA COVID-19 vaccine at a medical center in Japan
  publication-title: Hum. Vaccines Immunother.
  doi: 10.1080/21645515.2021.1984124
– volume: 362
  start-page: 1353
  year: 2003
  ident: ref_3
  article-title: Epidemiology and cause of severe acute respiratory syndrome (SARS) in Guangdong, People’s Republic of China, in February, 2003
  publication-title: Lancet
  doi: 10.1016/S0140-6736(03)14630-2
– ident: ref_14
– ident: ref_76
  doi: 10.3390/v14040802
– volume: 12
  start-page: 677
  year: 2021
  ident: ref_19
  article-title: Mini Review Immunological Consequences of Immunization With COVID-19 mRNA Vaccines: Preliminary Results
  publication-title: Front. Immunol.
  doi: 10.3389/fimmu.2021.657711
– volume: 26
  start-page: 1293
  year: 2022
  ident: ref_57
  article-title: Kinetics and persistence of cellular and humoral immune responses to SARS-CoV-2 vaccine in healthcare workers with or without prior COVID-19
  publication-title: J. Cell Mol. Med.
  doi: 10.1111/jcmm.17186
– volume: 6
  start-page: 100272
  year: 2021
  ident: ref_72
  article-title: A snapshot of the immunogenicity, efficacy and safety of a full course of BNT162b2 anti-SARS-CoV-2 vaccine in cancer patients treated with PD-1/PD-L1 inhibitors: A longitudinal cohort study
  publication-title: ESMO Open
  doi: 10.1016/j.esmoop.2021.100272
– volume: 12
  start-page: 3947
  year: 2021
  ident: ref_44
  article-title: Humoral and Cellular Response Following Vaccination with the BNT162b2 mRNA COVID-19 Vaccine in Patients Affected by Primary Immunodeficiencies
  publication-title: Front. Immunol.
  doi: 10.3389/fimmu.2021.727850
– volume: 28
  start-page: 735.e1
  year: 2022
  ident: ref_81
  article-title: The effect of a third BNT162b2 vaccine on breakthrough infections in health care workers: A cohort analysis
  publication-title: Clin. Microbiol. Infect.
  doi: 10.1016/j.cmi.2022.01.019
– ident: ref_6
– volume: 24
  start-page: 174
  year: 2021
  ident: ref_8
  article-title: Population Health Strategies to Support Hospital and Intensive Care Unit Resiliency during the COVID-19 Pandemic: The Italian Experience
  publication-title: Popul. Health Manag.
  doi: 10.1089/pop.2020.0255
– ident: ref_36
  doi: 10.1101/2021.11.25.470011
– ident: ref_29
– ident: ref_33
– ident: ref_41
  doi: 10.1101/2021.09.07.21263229
– volume: 80
  start-page: 1317
  year: 2021
  ident: ref_45
  article-title: Disease activity and humoral response in patients with inflammatory rheumatic diseases after two doses of the Pfizer mRNA vaccine against SARS-CoV-2
  publication-title: Ann. Rheum. Dis.
  doi: 10.1136/annrheumdis-2021-220503
– volume: 12
  start-page: 6612
  year: 2021
  ident: ref_37
  article-title: Organ-specific genome diversity of replication-competent SARS-CoV-2
  publication-title: Nat. Commun.
  doi: 10.1038/s41467-021-26884-7
– ident: ref_2
– volume: 10
  start-page: e1341
  year: 2021
  ident: ref_55
  article-title: T-cell response after first dose of BNT162b2 SARS-CoV-2 vaccine among healthcare workers with previous infection or cross-reactive immunity
  publication-title: Clin. Transl. Immunol.
  doi: 10.1002/cti2.1341
– ident: ref_12
– ident: ref_60
  doi: 10.3390/vaccines9060672
– volume: 586
  start-page: 594
  year: 2020
  ident: ref_70
  article-title: COVID-19 vaccine BNT162b1 elicits human antibody and TH1 T cell responses
  publication-title: Nature
  doi: 10.1038/s41586-020-2814-7
– ident: ref_15
– volume: 590
  start-page: 320
  year: 2021
  ident: ref_34
  article-title: A single-dose live-attenuated YF17D-vectored SARS-CoV-2 vaccine candidate
  publication-title: Nature
  doi: 10.1038/s41586-020-3035-9
– volume: 40
  start-page: 512
  year: 2022
  ident: ref_82
  article-title: Early effectiveness of BNT162b2 COVID-19 vaccine in preventing SARS-CoV-2 infection in healthcare personnel in six Israeli hospitals (CoVEHPI)
  publication-title: Vaccine
  doi: 10.1016/j.vaccine.2021.11.092
– volume: 26
  start-page: 2100824
  year: 2021
  ident: ref_28
  article-title: Characterisation of vaccine breakthrough infections of sars-cov-2 delta and alpha variants and within-host viral load dynamics in the community, France, June to July 2021
  publication-title: Eurosurveillance
  doi: 10.2807/1560-7917.ES.2021.26.37.2100824
– volume: 16
  start-page: 1037
  year: 2021
  ident: ref_47
  article-title: Humoral response to the pfizer bnt162b2 vaccine in patients undergoing maintenance hemodialysis
  publication-title: Clin. J. Am. Soc. Nephrol.
  doi: 10.2215/CJN.03500321
– ident: ref_43
– volume: 10
  start-page: 100208
  year: 2021
  ident: ref_62
  article-title: Dynamics of antibody response to BNT162b2 vaccine after six months: A longitudinal prospective study
  publication-title: Lancet Reg. Health Eur.
  doi: 10.1016/j.lanepe.2021.100208
– volume: 384
  start-page: 2212
  year: 2021
  ident: ref_26
  article-title: Vaccine Breakthrough Infections with SARS-CoV-2 Variants
  publication-title: N. Engl. J. Med.
  doi: 10.1056/NEJMoa2105000
– ident: ref_54
  doi: 10.3390/pathogens11010067
SSID ssj0066907
Score 2.3316784
Snippet To mitigate the massive COVID-19 burden caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), several vaccination campaigns were initiated....
SourceID doaj
pubmedcentral
proquest
gale
crossref
SourceType Open Website
Open Access Repository
Aggregation Database
Enrichment Source
Index Database
StartPage 1257
SubjectTerms Adaptive immunity
Antibodies
Belgium
BNT162b2 vaccine
breakthrough infection
CD4 antigen
CD8 antigen
Cell-mediated immunity
Coronaviruses
COVID-19
COVID-19 infection
COVID-19 vaccines
Disease transmission
Enzymes
Health aspects
Health care
health services
healthcare workers
Humoral immunity
Immune response
Immune response (humoral)
Immune system
Immunoassay
Infections
long-term monitoring
Lymphocytes B
Lymphocytes T
Medical personnel
neutralization
Pandemics
Pathogens
Proteins
SARS-CoV-2
Serology
Severe acute respiratory syndrome coronavirus 2
T cells
Vaccination
Vaccines
variants of concern
γ-Interferon
SummonAdditionalLinks – databaseName: DOAJ Directory of Open Access Journals
  dbid: DOA
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1fb9MwELfQJCReEH9FYKADIcFLtMRObJe3tlAVBHvY2mlvke3Yo6Ik09qC-j35QNwlabUAghde7bPi-M6-O_vud4y9zHhpyW6IdRryONPexLpEr1UG7blSuROOXnQ_HcvpPPtwnp9fK_VFMWEtPHC7cEciJGkwKvPcukwPlBFemDy4EETCuzRf1Hk7Z6o9gyX5fC2OkECn_uhbmjWqXPW0TwPS__tR_Gt45DV9M7nDbneGIgzbCd5lN3x1j91sS0du77MfFKABuLvboqBQBzgdnpzG4_os5nCGHjAuGbWOKS_xqoIRWodfuqo8OK4NwapW8Jbe2tceTvyqycsCZDBl7YOpShj75ZLiVOF9k0ay3gKV-nC-BLuF0fEsldzS15xbtLeKsKhgug8pA7qKR_vyDQzhY11dxDPUAzBB0au_x_NLoCDGLQ0Z-eXFYvP1AZtP3s3G07ir0BC7PJPr2DiqpFiK1JTcCJXb0vhcSG8TRUCHaA1qKa1yziVlGVKVBJsHXuoyUzYo3P8P2UFVV_4RA6G0QWtJasJwM0pbLST6OjZTSWYyoyP2ese5wnXw5VRFY1mgG0NMLvZMjtiLPelli9nxJ6IRsX9PQDDbTQMKX9EJX_Ev4YvYKxKegg4DnIwzXU4D_hLBahVDxSn3GG26iB32KHETu373TvyK7hBZFZxeyKRQXETs-b6bRlJgXOXrDdHoNBHoNMq_0KD9wXOeyCRiqifavb_v91SLzw3Y-IBzjU7D4_-xXE_YLU7ZI3SJNThkB-urjX-KNt3aPmu27085nEsv
  priority: 102
  providerName: Directory of Open Access Journals
– databaseName: Health & Medical Collection (ProQuest)
  dbid: 7X7
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1Lj9MwELZgERIXxFMEFmQQElyiTezEdrmgtlAVBHvYbVe9RY4f3YqSlD5A_Z_8IGaSNBBAe43HatKxxzPjb74h5GXCbI5-Q6hin4aJcjpUFqJW4ZVjUqaGG7zR_XwqxtPk4yydNQm3TQOrPNjEylDb0mCO_IThdYHgkvG3q28hdo3C29WmhcZ1cgOpyxDSJWdtwCUw8qvZhDiE9iff46Q60GXnDKqo-v81yH-DJP84dUZ3yO3GXaT9Wr93yTVX3CM36waS-_vkJ8I0KOzxujUoLT0975-dh8PyImT0AuJg-OPw6RCrE9cFHYCP-KXpzQPzaiBWsaHv8MZ96-iZ21TVWRTUjLX7VBeWDt1yiWhV-qEqJtnuKTb8MM7SfE8Hp5NYsBx_zZhFnVuki4KOW2AZxYQ8eJlvaJ9-Kot5OIHTgI5gAZY_wumKIpRxj1MGbjlf7L4-INPR-8lwHDZ9GkKTJmIbaoP9FC2PtWWayzS32qVcuDySSHcIPqESIpfGmMhaH8vI56lnVtlE5l6CFXhIjoqycI8I5VJp8JmEQiY3LVWuuICIJ09klOhEq4C8PmguMw2JOfbSWGYQzKCSs1bJAXnRiq5q5o7_CQ1Q_a0Akm1XD8r1PGv2bsZ9FHstE8dyk6ie1NxxnXrjPY8QPhKQV7h4MjQJ8DJGN5UN8ElIrpX1JcMKZPDsAnLckYStbLrDh-WXNaZkk_1e-AF53g7jTITHFa7coYyKIw6ho7hCBrwQlrJIRAGRnaXd-fruSLG4rCjHe4wpCB0eX_2CT8gthtUhmKTqHZOj7XrnnoLPts2fVRvzFym5QmQ
  priority: 102
  providerName: ProQuest
Title High Incidence of SARS-CoV-2 Variant of Concern Breakthrough Infections Despite Residual Humoral and Cellular Immunity Induced by BNT162b2 Vaccination in Healthcare Workers: A Long-Term Follow-Up Study in Belgium
URI https://www.proquest.com/docview/2679863723
https://www.proquest.com/docview/2681035766
https://www.proquest.com/docview/2718252060
https://pubmed.ncbi.nlm.nih.gov/PMC9228150
https://doaj.org/article/3f01fa74e2bc4897a3e3a5fcff302008
Volume 14
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lj9MwELb2IdBeEE8RWCqDkOASSOzEdpEQasuWgtgKddtVb5HjOKWiJEsfQP8nP4iZJI02sOLAJYd4rMSZmcyMPTMfIU8DlsToN7jKT0M3UFa7KoGoVaTKMilDww2e6J4OxWASfJiG0z2yw9isPuDqytAO8aQmy8WLn9-2b0DhX2PECSH7y-9-UBhquU8OwSBJ1M_ToD5MEBgAlk2FmuRH5DoPEW4DodgvWaWief_fv-g_0yYv2aH-TXKjciBpp-T4LbJns9vkWgkpub1DfmHiBgWtL8FCaZ7Ss87ozO3l5y6j5xAZw6fEuz2sV1xmtAte45cKrQfmlalZ2Yq-xTP4taUjuyrqtSgwHqv5qc4S2rOLBeav0vdFecl6SxECxNiExlvaHY59wWJ8mjHzcreRzjM6qFPNKG7Rg9_5inboxzybuWOwD7QPIpn_cCcXFJMbtzilaxez-ebrXTLpn4x7A7dCbnBNGIi1qw0iLCbc1wnTXIZxom3IhY09iQ0QwUtUQsTSGOMlSepLL43DlCUqCWScSvgv3CMHWZ7Z-4RyqTR4UUJhbzctVay4gBgoDqQX6EArhzzfcS4yVVtzRNdYRBDeIL-jmt8OeVKTXpS9PK4i6iL7awJsv13cyJezqNLmiKeen2oZWBabQLWl5pbrMDVpyj1MKHHIMxSeCMUWXsboqtYBloTttqKOZFiTDL6eQ44blKDcpjm8E79opxsRw5MzwSXjDnlcD-NMTJjLbL5BGuV7IN1C_IMG_BIWMk94DpEN0W6svjmSzT8XTcjbjCkIJh7898yH5IhhKQnuaLWPycF6ubGPwMFbxy2yL6eyRQ67J8NPo1axTQLXd1O_VSj2b8-_VXI
linkProvider Scholars Portal
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV1fb9MwELemTQheEH9FYIBBIHiJltiJ7SIh1HarWtZVqGunvWWO45SKkpT-YeqX4tPwgbhL0kIB7W2v8VlJdOfz7-y7-xHyKmBJjLjBVX4auoGy2lUJRK0iVZZJGRpu8Eb3pCfaw-DjeXi-Q36sa2EwrXLtEwtHneQGz8gPGF4XCC4Z_zD95iJrFN6urik0SrM4tqtLCNnm7zuHoN_XjLWOBs22W7EKuCYMxMLVBtn_Eu7rhGkuwzjRNuTCxp7E5nyAYJQQsTTGeEmS-tJL4zBliUoCGafSQ5YIcPl7AYdQZpfsNY56n_pr3y8w1iz7F3Fe8w6--0EBIeTWrleQA_y7BfydlvnHPte6Q25XAJXWS4u6S3Zsdo_cKCkrV_fJT0wMoeBVSjJSmqf0tN4_dZv5mcvoGUTeoCp82sR6yFlGG4BKv1RsQDCvTP3K5vQQ7_gXlvbtvKgHo2BY2C2A6iyhTTuZYH4s7RTlK4sVRYoRYxMar2ijN_AFi_FtxozL00w6zmh7k8pG8QoAcO07WqfdPBu5A9h_aAtMPr90h1OKyZMrnNKwk9F4-fUBGV6LDh-S3SzP7CNCuVQaUJpQ2DtOSxUrLiDGigPpBTrQyiFv15qLTNU2Hdk7JhGET6jkaKNkh7zciE7LXiH_E2qg-jcC2N67eJDPRlHlLSKeen6qZWBZbAJVk5pbrsPUpCn3MGHFIW_QeCJ0QvAxRle1FPBL2M4rqkuGNc-AJR2yvyUJzsNsD6_NL6qc1zz6vdQc8mIzjDMxIS-z-RJllO9xCFbFFTKAe1jIPOE5RG6Z9tbfb49k489Fk_MaYwqClcdXf-BzcrM9OOlG3U7v-Am5xbA2BY_IavtkdzFb2qeAGBfxs2qZUnJx3Z7hFyJIgRE
linkToPdf http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV3bjtMwELVWi0C8IK6isIBBIHiJmtiJ7SIh1AtVl10qtNuu-hYcxy4VJSm9sOqv8R18EDNJWiigfdvXeKwkmvH4jD0zh5DnIUsTxA2eClzkhcpqT6UQtQqnLJMyMtzgje6HvugNw_ejaLRHfmxqYTCtcuMTC0ed5gbPyOsMrwsEl4zXXZUW8bHTfTv75iGDFN60bug0ShM5sutzCN8Wbw47oOsXjHXfDdo9r2IY8EwUiqWnDTIBpjzQKdNcRkmqbcSFTXyJjfoAzSghEmmM8dPUBdJ3SeRYqtJQJk76yBgB7v-K5FGAa0yOtsGewKiz7GTEecOvfw_CAkzInf2voAn4dzP4O0Hzjx2ve5PcqKAqbZa2dYvs2ew2uVqSV67vkJ-YIkLBv5S0pDR39LR5cuq18zOP0TOIwUFp-LSNlZHzjLYAn36peIFgXpkEli1oB2_7l5ae2EVRGUbBxLBvANVZStt2OsVMWXpYFLIs1xTJRoxNabKmrf4gECzBtxkzKc816SSjvW1SG8XLAEC4r2mTHufZ2BvATkS7YPz5uTecUUyjXOOUlp2OJ6uvd8nwUjR4j-xneWbvE8ql0oDXhMIuclqqRHEB0VYSSj_UoVY18mqjudhUDdSRx2MaQyCFSo63Sq6RZ1vRWdk15H9CLVT_VgAbfRcP8vk4rvxGzJ0fOC1DyxITqobU3HIdOeMc9zF1pUZeovHE6I7gY4yuqirgl7CxV9yUDKufAVXWyMGOJLgRszu8Mb-4cmOL-Peiq5Gn22Gcial5mc1XKKMCn0PYKi6QAQTEIuYLv0bkjmnv_P3uSDb5XLQ7bzCmIGx5cPEHPiHXwB_Ex4f9o4fkOsMiFTwraxyQ_eV8ZR8BdFwmj4s1Ssmny3YKvwCMJYPh
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=High+Incidence+of+SARS-CoV-2+Variant+of+Concern+Breakthrough+Infections+Despite+Residual+Humoral+and+Cellular+Immunity+Induced+by+BNT162b2+Vaccination+in+Healthcare+Workers%3A+A+Long-Term+Follow-Up+Study+in+Belgium&rft.jtitle=Viruses&rft.au=Calcoen%2C+Bas&rft.au=Callewaert%2C+Nico&rft.au=Vandenbulcke%2C+Aline&rft.au=Kerstens%2C+Winnie&rft.date=2022-06-09&rft.pub=MDPI&rft.eissn=1999-4915&rft.volume=14&rft.issue=6&rft_id=info:doi/10.3390%2Fv14061257&rft_id=info%3Apmid%2F35746728&rft.externalDocID=PMC9228150
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1999-4915&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1999-4915&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1999-4915&client=summon