Immunogenicity of Influenza Vaccines: Evidence for Differential Effect of Secondary Vaccination on Humoral and Cellular Immunity.
Identifieur interne : 000014 ( Main/Curation ); précédent : 000013; suivant : 000015Immunogenicity of Influenza Vaccines: Evidence for Differential Effect of Secondary Vaccination on Humoral and Cellular Immunity.
Auteurs : Sietske K. Rosendahl Huber [Pays-Bas] ; Marion Hendriks [Pays-Bas] ; Ronald H J. Jacobi [Pays-Bas] ; Jan Van De Kassteele [Pays-Bas] ; Jolanda C. Mandersloot-Oskam [Pays-Bas] ; Renée A J. Van Boxtel [Pays-Bas] ; Anne M J. Wensing [Pays-Bas] ; Nynke Y. Rots [Pays-Bas] ; Willem Luytjes [Pays-Bas] ; Josine Van Beek [Pays-Bas]Source :
- Frontiers in immunology [ 1664-3224 ] ; 2018.
Descripteurs français
- KwdFr :
- Adjuvants immunologiques (administration et posologie), Adulte (MeSH), Adulte d'âge moyen (MeSH), Anticorps antiviraux (immunologie), Anticorps antiviraux (sang), Anticorps neutralisants (immunologie), Anticorps neutralisants (sang), Femelle (MeSH), Grippe humaine (immunologie), Grippe humaine (prévention et contrôle), Grippe humaine (virologie), Grippe humaine (épidémiologie), Humains (MeSH), Immunogénicité des vaccins (MeSH), Interféron gamma (immunologie), Interféron gamma (métabolisme), Jeune adulte (MeSH), Lymphocytes T (immunologie), Lymphocytes T (métabolisme), Mâle (MeSH), Pandémies (prévention et contrôle), Pays-Bas (épidémiologie), Polysorbates (administration et posologie), Rappel de vaccin (méthodes), Sous-type H1N1 du virus de la grippe A (immunologie), Squalène (administration et posologie), Tests d'inhibition de l'hémagglutination (MeSH), Vaccination (méthodes), Vaccins antigrippaux (administration et posologie), Vaccins antigrippaux (immunologie).
- MESH :
- administration et posologie : Adjuvants immunologiques, Polysorbates, Squalène, Vaccins antigrippaux.
- immunologie : Anticorps antiviraux, Anticorps neutralisants, Grippe humaine, Interféron gamma, Lymphocytes T, Sous-type H1N1 du virus de la grippe A, Vaccins antigrippaux.
- métabolisme : Interféron gamma, Lymphocytes T.
- méthodes : Rappel de vaccin, Vaccination.
- prévention et contrôle : Grippe humaine, Pandémies.
- sang : Anticorps antiviraux, Anticorps neutralisants.
- virologie : Grippe humaine.
- épidémiologie : Grippe humaine, Pays-Bas.
- Adulte, Adulte d'âge moyen, Femelle, Humains, Immunogénicité des vaccins, Jeune adulte, Mâle, Tests d'inhibition de l'hémagglutination.
- Wicri :
- geographic : Pays-Bas.
English descriptors
- KwdEn :
- Adjuvants, Immunologic (administration & dosage), Adult (MeSH), Antibodies, Neutralizing (blood), Antibodies, Neutralizing (immunology), Antibodies, Viral (blood), Antibodies, Viral (immunology), Female (MeSH), Hemagglutination Inhibition Tests (MeSH), Humans (MeSH), Immunization, Secondary (methods), Immunogenicity, Vaccine (MeSH), Influenza A Virus, H1N1 Subtype (immunology), Influenza Vaccines (administration & dosage), Influenza Vaccines (immunology), Influenza, Human (epidemiology), Influenza, Human (immunology), Influenza, Human (prevention & control), Influenza, Human (virology), Interferon-gamma (immunology), Interferon-gamma (metabolism), Male (MeSH), Middle Aged (MeSH), Netherlands (epidemiology), Pandemics (prevention & control), Polysorbates (administration & dosage), Squalene (administration & dosage), T-Lymphocytes (immunology), T-Lymphocytes (metabolism), Vaccination (methods), Young Adult (MeSH).
- MESH :
- chemical , administration & dosage : Adjuvants, Immunologic, Influenza Vaccines, Polysorbates, Squalene.
- chemical , blood : Antibodies, Neutralizing, Antibodies, Viral.
- chemical , immunology : Antibodies, Neutralizing, Antibodies, Viral, Influenza Vaccines, Interferon-gamma.
- geographic , epidemiology : Netherlands.
- epidemiology : Influenza, Human.
- immunology : Influenza A Virus, H1N1 Subtype, Influenza, Human, T-Lymphocytes.
- chemical , metabolism : Interferon-gamma, T-Lymphocytes.
- methods : Immunization, Secondary, Vaccination.
- prevention & control : Influenza, Human, Pandemics.
- virology : Influenza, Human.
- Adult, Female, Hemagglutination Inhibition Tests, Humans, Immunogenicity, Vaccine, Male, Middle Aged, Young Adult.
Abstract
While currently used influenza vaccines are designed to induce neutralizing antibodies, little is known on T cell responses induced by these vaccines. The 2009 pandemic provided us with the opportunity to evaluate the immune response to vaccination in a unique setting. We evaluated both antibody and T cell responses in a cohort of public health care workers (18-52 years) during two consecutive influenza seasons from 2009 to 2011 and compared the MF59-adjuvanted pandemic vaccine with the unadjuvanted seasonal subunit vaccine that included the pandemic strain [The study was registered in the Netherlands Trial Register (NTR2070)]. Antibody responses were determined in serum by a hemagglutination inhibition assay. Vaccine-specific T cell responses were evaluated by detecting IFN-γ producing peripheral blood mononuclear cells using whole influenza virus or vaccine-specific peptide pools as stimulating antigens. Mixed effects regression models were used to correct the data for influenza-specific pre-existing immunity due to previous infections or vaccinations and for age and sex. We show that one dose of the pandemic vaccine induced antibody responses sufficient for providing seroprotection and that the vaccine induced T cell responses. A second dose further increased antibody responses but not T cell responses. Nonetheless, both could be boosted by the seasonal vaccine in the subsequent season. Furthermore, we show that the seasonal vaccine alone is capable of inducing vaccine-specific T cell responses, despite the fact that the vaccine did not contain an adjuvant. In addition, residual antibody levels remained detectable for over 15 months, while T cell levels in the blood had contracted to baseline levels by that time. Hereby, we show that pandemic as well as seasonal vaccines induce both humoral and cellular responses, however, with a different profile of induction and waning, which has its implications for future vaccine design.
DOI: 10.3389/fimmu.2018.03103
PubMed: 30761157
PubMed Central: PMC6362424
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Rosendahl Huber</name><affiliation wicri:level="1"><nlm:affiliation>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven</wicri:regionArea></affiliation></author><author><name sortKey="Hendriks, Marion" sort="Hendriks, Marion" uniqKey="Hendriks M" first="Marion" last="Hendriks">Marion Hendriks</name><affiliation wicri:level="1"><nlm:affiliation>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven</wicri:regionArea></affiliation></author><author><name sortKey="Jacobi, Ronald H J" sort="Jacobi, Ronald H J" uniqKey="Jacobi R" first="Ronald H J" last="Jacobi">Ronald H J. Jacobi</name><affiliation wicri:level="1"><nlm:affiliation>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven</wicri:regionArea></affiliation></author><author><name sortKey="Van De Kassteele, Jan" sort="Van De Kassteele, Jan" uniqKey="Van De Kassteele J" first="Jan" last="Van De Kassteele">Jan Van De Kassteele</name><affiliation wicri:level="1"><nlm:affiliation>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven</wicri:regionArea></affiliation></author><author><name sortKey="Mandersloot Oskam, Jolanda C" sort="Mandersloot Oskam, Jolanda C" uniqKey="Mandersloot Oskam J" first="Jolanda C" last="Mandersloot-Oskam">Jolanda C. Mandersloot-Oskam</name><affiliation wicri:level="1"><nlm:affiliation>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven</wicri:regionArea></affiliation></author><author><name sortKey="Van Boxtel, Renee A J" sort="Van Boxtel, Renee A J" uniqKey="Van Boxtel R" first="Renée A J" last="Van Boxtel">Renée A J. Van Boxtel</name><affiliation wicri:level="1"><nlm:affiliation>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven</wicri:regionArea></affiliation></author><author><name sortKey="Wensing, Anne M J" sort="Wensing, Anne M J" uniqKey="Wensing A" first="Anne M J" last="Wensing">Anne M J. Wensing</name><affiliation wicri:level="1"><nlm:affiliation>Department of Medical Microbiology, University Medical Center Utrecht, Utrecht, Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Department of Medical Microbiology, University Medical Center Utrecht, Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="Rots, Nynke Y" sort="Rots, Nynke Y" uniqKey="Rots N" first="Nynke Y" last="Rots">Nynke Y. Rots</name><affiliation wicri:level="1"><nlm:affiliation>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven</wicri:regionArea></affiliation></author><author><name sortKey="Luytjes, Willem" sort="Luytjes, Willem" uniqKey="Luytjes W" first="Willem" last="Luytjes">Willem Luytjes</name><affiliation wicri:level="1"><nlm:affiliation>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven</wicri:regionArea></affiliation></author><author><name sortKey="Van Beek, Josine" sort="Van Beek, Josine" uniqKey="Van Beek J" first="Josine" last="Van Beek">Josine Van Beek</name><affiliation wicri:level="1"><nlm:affiliation>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven</wicri:regionArea></affiliation></author></analytic><series><title level="j">Frontiers in immunology</title><idno type="eISSN">1664-3224</idno><imprint><date when="2018" type="published">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Adjuvants, Immunologic (administration & dosage)</term><term>Adult (MeSH)</term><term>Antibodies, Neutralizing (blood)</term><term>Antibodies, Neutralizing (immunology)</term><term>Antibodies, Viral (blood)</term><term>Antibodies, Viral (immunology)</term><term>Female (MeSH)</term><term>Hemagglutination Inhibition Tests (MeSH)</term><term>Humans (MeSH)</term><term>Immunization, Secondary (methods)</term><term>Immunogenicity, Vaccine (MeSH)</term><term>Influenza A Virus, H1N1 Subtype (immunology)</term><term>Influenza Vaccines (administration & dosage)</term><term>Influenza Vaccines (immunology)</term><term>Influenza, Human (epidemiology)</term><term>Influenza, Human (immunology)</term><term>Influenza, Human (prevention & control)</term><term>Influenza, Human (virology)</term><term>Interferon-gamma (immunology)</term><term>Interferon-gamma (metabolism)</term><term>Male (MeSH)</term><term>Middle Aged (MeSH)</term><term>Netherlands (epidemiology)</term><term>Pandemics (prevention & control)</term><term>Polysorbates (administration & dosage)</term><term>Squalene (administration & dosage)</term><term>T-Lymphocytes (immunology)</term><term>T-Lymphocytes (metabolism)</term><term>Vaccination (methods)</term><term>Young Adult (MeSH)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Adjuvants immunologiques (administration et posologie)</term><term>Adulte (MeSH)</term><term>Adulte d'âge moyen (MeSH)</term><term>Anticorps antiviraux (immunologie)</term><term>Anticorps antiviraux (sang)</term><term>Anticorps neutralisants (immunologie)</term><term>Anticorps neutralisants (sang)</term><term>Femelle (MeSH)</term><term>Grippe humaine (immunologie)</term><term>Grippe humaine (prévention et contrôle)</term><term>Grippe humaine (virologie)</term><term>Grippe humaine (épidémiologie)</term><term>Humains (MeSH)</term><term>Immunogénicité des vaccins (MeSH)</term><term>Interféron gamma (immunologie)</term><term>Interféron gamma (métabolisme)</term><term>Jeune adulte (MeSH)</term><term>Lymphocytes T (immunologie)</term><term>Lymphocytes T (métabolisme)</term><term>Mâle (MeSH)</term><term>Pandémies (prévention et contrôle)</term><term>Pays-Bas (épidémiologie)</term><term>Polysorbates (administration et posologie)</term><term>Rappel de vaccin (méthodes)</term><term>Sous-type H1N1 du virus de la grippe A (immunologie)</term><term>Squalène (administration et posologie)</term><term>Tests d'inhibition de l'hémagglutination (MeSH)</term><term>Vaccination (méthodes)</term><term>Vaccins antigrippaux (administration et posologie)</term><term>Vaccins antigrippaux (immunologie)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="administration & dosage" xml:lang="en"><term>Adjuvants, Immunologic</term><term>Influenza Vaccines</term><term>Polysorbates</term><term>Squalene</term></keywords><keywords scheme="MESH" type="chemical" qualifier="blood" xml:lang="en"><term>Antibodies, Neutralizing</term><term>Antibodies, Viral</term></keywords><keywords scheme="MESH" type="chemical" qualifier="immunology" xml:lang="en"><term>Antibodies, Neutralizing</term><term>Antibodies, Viral</term><term>Influenza Vaccines</term><term>Interferon-gamma</term></keywords><keywords scheme="MESH" type="geographic" qualifier="epidemiology" xml:lang="en"><term>Netherlands</term></keywords><keywords scheme="MESH" qualifier="administration et posologie" xml:lang="fr"><term>Adjuvants immunologiques</term><term>Polysorbates</term><term>Squalène</term><term>Vaccins antigrippaux</term></keywords><keywords scheme="MESH" qualifier="epidemiology" xml:lang="en"><term>Influenza, Human</term></keywords><keywords scheme="MESH" qualifier="immunologie" xml:lang="fr"><term>Anticorps antiviraux</term><term>Anticorps neutralisants</term><term>Grippe humaine</term><term>Interféron gamma</term><term>Lymphocytes T</term><term>Sous-type H1N1 du virus de la grippe A</term><term>Vaccins antigrippaux</term></keywords><keywords scheme="MESH" qualifier="immunology" xml:lang="en"><term>Influenza A Virus, H1N1 Subtype</term><term>Influenza, Human</term><term>T-Lymphocytes</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Interferon-gamma</term><term>T-Lymphocytes</term></keywords><keywords scheme="MESH" qualifier="methods" xml:lang="en"><term>Immunization, Secondary</term><term>Vaccination</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Interféron gamma</term><term>Lymphocytes T</term></keywords><keywords scheme="MESH" qualifier="méthodes" xml:lang="fr"><term>Rappel de vaccin</term><term>Vaccination</term></keywords><keywords scheme="MESH" qualifier="prevention & control" xml:lang="en"><term>Influenza, Human</term><term>Pandemics</term></keywords><keywords scheme="MESH" qualifier="prévention et contrôle" xml:lang="fr"><term>Grippe humaine</term><term>Pandémies</term></keywords><keywords scheme="MESH" qualifier="sang" xml:lang="fr"><term>Anticorps antiviraux</term><term>Anticorps neutralisants</term></keywords><keywords scheme="MESH" qualifier="virologie" xml:lang="fr"><term>Grippe humaine</term></keywords><keywords scheme="MESH" qualifier="virology" xml:lang="en"><term>Influenza, Human</term></keywords><keywords scheme="MESH" qualifier="épidémiologie" xml:lang="fr"><term>Grippe humaine</term><term>Pays-Bas</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Adult</term><term>Female</term><term>Hemagglutination Inhibition Tests</term><term>Humans</term><term>Immunogenicity, Vaccine</term><term>Male</term><term>Middle Aged</term><term>Young Adult</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Adulte</term><term>Adulte d'âge moyen</term><term>Femelle</term><term>Humains</term><term>Immunogénicité des vaccins</term><term>Jeune adulte</term><term>Mâle</term><term>Tests d'inhibition de l'hémagglutination</term></keywords><keywords scheme="Wicri" type="geographic" xml:lang="fr"><term>Pays-Bas</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">While currently used influenza vaccines are designed to induce neutralizing antibodies, little is known on T cell responses induced by these vaccines. The 2009 pandemic provided us with the opportunity to evaluate the immune response to vaccination in a unique setting. We evaluated both antibody and T cell responses in a cohort of public health care workers (18-52 years) during two consecutive influenza seasons from 2009 to 2011 and compared the MF59-adjuvanted pandemic vaccine with the unadjuvanted seasonal subunit vaccine that included the pandemic strain [The study was registered in the Netherlands Trial Register (NTR2070)]. Antibody responses were determined in serum by a hemagglutination inhibition assay. Vaccine-specific T cell responses were evaluated by detecting IFN-γ producing peripheral blood mononuclear cells using whole influenza virus or vaccine-specific peptide pools as stimulating antigens. Mixed effects regression models were used to correct the data for influenza-specific pre-existing immunity due to previous infections or vaccinations and for age and sex. We show that one dose of the pandemic vaccine induced antibody responses sufficient for providing seroprotection and that the vaccine induced T cell responses. A second dose further increased antibody responses but not T cell responses. Nonetheless, both could be boosted by the seasonal vaccine in the subsequent season. Furthermore, we show that the seasonal vaccine alone is capable of inducing vaccine-specific T cell responses, despite the fact that the vaccine did not contain an adjuvant. In addition, residual antibody levels remained detectable for over 15 months, while T cell levels in the blood had contracted to baseline levels by that time. Hereby, we show that pandemic as well as seasonal vaccines induce both humoral and cellular responses, however, with a different profile of induction and waning, which has its implications for future vaccine design.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">30761157</PMID><DateCompleted><Year>2019</Year><Month>10</Month><Day>25</Day></DateCompleted><DateRevised><Year>2020</Year><Month>03</Month><Day>09</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Electronic">1664-3224</ISSN><JournalIssue CitedMedium="Internet"><Volume>9</Volume><PubDate><Year>2018</Year></PubDate></JournalIssue><Title>Frontiers in immunology</Title><ISOAbbreviation>Front Immunol</ISOAbbreviation></Journal><ArticleTitle>Immunogenicity of Influenza Vaccines: Evidence for Differential Effect of Secondary Vaccination on Humoral and Cellular Immunity.</ArticleTitle><Pagination><MedlinePgn>3103</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.3389/fimmu.2018.03103</ELocationID><Abstract><AbstractText>While currently used influenza vaccines are designed to induce neutralizing antibodies, little is known on T cell responses induced by these vaccines. The 2009 pandemic provided us with the opportunity to evaluate the immune response to vaccination in a unique setting. We evaluated both antibody and T cell responses in a cohort of public health care workers (18-52 years) during two consecutive influenza seasons from 2009 to 2011 and compared the MF59-adjuvanted pandemic vaccine with the unadjuvanted seasonal subunit vaccine that included the pandemic strain [The study was registered in the Netherlands Trial Register (NTR2070)]. Antibody responses were determined in serum by a hemagglutination inhibition assay. Vaccine-specific T cell responses were evaluated by detecting IFN-γ producing peripheral blood mononuclear cells using whole influenza virus or vaccine-specific peptide pools as stimulating antigens. Mixed effects regression models were used to correct the data for influenza-specific pre-existing immunity due to previous infections or vaccinations and for age and sex. We show that one dose of the pandemic vaccine induced antibody responses sufficient for providing seroprotection and that the vaccine induced T cell responses. A second dose further increased antibody responses but not T cell responses. Nonetheless, both could be boosted by the seasonal vaccine in the subsequent season. Furthermore, we show that the seasonal vaccine alone is capable of inducing vaccine-specific T cell responses, despite the fact that the vaccine did not contain an adjuvant. In addition, residual antibody levels remained detectable for over 15 months, while T cell levels in the blood had contracted to baseline levels by that time. Hereby, we show that pandemic as well as seasonal vaccines induce both humoral and cellular responses, however, with a different profile of induction and waning, which has its implications for future vaccine design.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Rosendahl Huber</LastName><ForeName>Sietske K</ForeName><Initials>SK</Initials><AffiliationInfo><Affiliation>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hendriks</LastName><ForeName>Marion</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jacobi</LastName><ForeName>Ronald H J</ForeName><Initials>RHJ</Initials><AffiliationInfo><Affiliation>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>van de Kassteele</LastName><ForeName>Jan</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mandersloot-Oskam</LastName><ForeName>Jolanda C</ForeName><Initials>JC</Initials><AffiliationInfo><Affiliation>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>van Boxtel</LastName><ForeName>Renée A J</ForeName><Initials>RAJ</Initials><AffiliationInfo><Affiliation>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wensing</LastName><ForeName>Anne M J</ForeName><Initials>AMJ</Initials><AffiliationInfo><Affiliation>Department of Medical Microbiology, University Medical Center Utrecht, Utrecht, Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rots</LastName><ForeName>Nynke Y</ForeName><Initials>NY</Initials><AffiliationInfo><Affiliation>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Luytjes</LastName><ForeName>Willem</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>van Beek</LastName><ForeName>Josine</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, Netherlands.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016430">Clinical Trial</PublicationType><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D016448">Multicenter Study</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>01</Month><Day>29</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Front Immunol</MedlineTA><NlmUniqueID>101560960</NlmUniqueID><ISSNLinking>1664-3224</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D000276">Adjuvants, Immunologic</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D057134">Antibodies, Neutralizing</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D000914">Antibodies, Viral</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="C573415">IFNG protein, human</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D007252">Influenza Vaccines</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="C089950">MF59 oil emulsion</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D011136">Polysorbates</NameOfSubstance></Chemical><Chemical><RegistryNumber>7QWM220FJH</RegistryNumber><NameOfSubstance UI="D013185">Squalene</NameOfSubstance></Chemical><Chemical><RegistryNumber>82115-62-6</RegistryNumber><NameOfSubstance UI="D007371">Interferon-gamma</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000276" MajorTopicYN="N">Adjuvants, Immunologic</DescriptorName><QualifierName UI="Q000008" MajorTopicYN="N">administration & dosage</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D000328" MajorTopicYN="N">Adult</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D057134" MajorTopicYN="N">Antibodies, Neutralizing</DescriptorName><QualifierName UI="Q000097" MajorTopicYN="N">blood</QualifierName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D000914" MajorTopicYN="N">Antibodies, Viral</DescriptorName><QualifierName UI="Q000097" MajorTopicYN="N">blood</QualifierName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D005260" MajorTopicYN="N">Female</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D006385" MajorTopicYN="N">Hemagglutination Inhibition Tests</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D007117" MajorTopicYN="N">Immunization, Secondary</DescriptorName><QualifierName UI="Q000379" MajorTopicYN="N">methods</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D000071497" MajorTopicYN="Y">Immunogenicity, Vaccine</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D053118" MajorTopicYN="N">Influenza A Virus, H1N1 Subtype</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="Y">immunology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D007252" MajorTopicYN="N">Influenza Vaccines</DescriptorName><QualifierName UI="Q000008" MajorTopicYN="N">administration & dosage</QualifierName><QualifierName UI="Q000276" MajorTopicYN="Y">immunology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D007251" MajorTopicYN="N">Influenza, Human</DescriptorName><QualifierName UI="Q000453" MajorTopicYN="N">epidemiology</QualifierName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName><QualifierName UI="Q000517" MajorTopicYN="Y">prevention & control</QualifierName><QualifierName UI="Q000821" MajorTopicYN="N">virology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D007371" MajorTopicYN="N">Interferon-gamma</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D008297" MajorTopicYN="N">Male</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D008875" MajorTopicYN="N">Middle Aged</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D009426" MajorTopicYN="N" Type="Geographic">Netherlands</DescriptorName><QualifierName UI="Q000453" MajorTopicYN="N">epidemiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D058873" MajorTopicYN="N">Pandemics</DescriptorName><QualifierName UI="Q000517" MajorTopicYN="Y">prevention & control</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D011136" MajorTopicYN="N">Polysorbates</DescriptorName><QualifierName UI="Q000008" MajorTopicYN="N">administration & dosage</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D013185" MajorTopicYN="N">Squalene</DescriptorName><QualifierName UI="Q000008" MajorTopicYN="N">administration & dosage</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D013601" MajorTopicYN="N">T-Lymphocytes</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D014611" MajorTopicYN="N">Vaccination</DescriptorName><QualifierName UI="Q000379" MajorTopicYN="N">methods</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D055815" MajorTopicYN="N">Young Adult</DescriptorName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">T cells</Keyword><Keyword MajorTopicYN="Y">cellular</Keyword><Keyword MajorTopicYN="Y">humoral</Keyword><Keyword MajorTopicYN="Y">influenza vaccines</Keyword><Keyword MajorTopicYN="Y">pandemic</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2018</Year><Month>08</Month><Day>07</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2018</Year><Month>12</Month><Day>14</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2019</Year><Month>2</Month><Day>15</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate 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