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Age and Influenza-Specific Pre-Vaccination Antibodies Strongly Affect Influenza Vaccine Responses in the Icelandic Population whereas Disease and Medication Have Small Effects

Influenza vaccination remains the best strategy for the prevention of influenza virus-related disease and reduction of disease severity and mortality. However, there is large individual variation in influenza vaccine responses. In this study, we investigated the effects of gender, age, underlying di...

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Autores principales: Olafsdottir, Thorunn A., Alexandersson, Kristjan F., Sveinbjornsson, Gardar, Lapini, Giulia, Palladino, Laura, Montomoli, Emanuele, Del Giudice, Giuseppe, Gudbjartsson, Daniel F., Jonsdottir, Ingileif
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5766658/
https://www.ncbi.nlm.nih.gov/pubmed/29358933
http://dx.doi.org/10.3389/fimmu.2017.01872
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author Olafsdottir, Thorunn A.
Alexandersson, Kristjan F.
Sveinbjornsson, Gardar
Lapini, Giulia
Palladino, Laura
Montomoli, Emanuele
Del Giudice, Giuseppe
Gudbjartsson, Daniel F.
Jonsdottir, Ingileif
author_facet Olafsdottir, Thorunn A.
Alexandersson, Kristjan F.
Sveinbjornsson, Gardar
Lapini, Giulia
Palladino, Laura
Montomoli, Emanuele
Del Giudice, Giuseppe
Gudbjartsson, Daniel F.
Jonsdottir, Ingileif
author_sort Olafsdottir, Thorunn A.
collection PubMed
description Influenza vaccination remains the best strategy for the prevention of influenza virus-related disease and reduction of disease severity and mortality. However, there is large individual variation in influenza vaccine responses. In this study, we investigated the effects of gender, age, underlying diseases, and medication on vaccine responses in 1,852 Icelanders of broad age range who received trivalent inactivated influenza virus vaccination in 2012, 2013, or 2015. Hemagglutination inhibition (HAI) and microneutralization (MN) titers were measured in pre- and post-vaccination sera. Of the variables tested, the strongest association was with level of pre-vaccination titer that explained a major part of the variance observed in post-vaccination titers, ranging from 19 to 29%, and from 7 to 21% in fold change (FC), depending on the strain and serological (HAI or MN) analysis performed. Thus, increasing pre-vaccination titer associated with decreasing FC (P = 1.1 × 10(−99)–8.6 × 10(−30)) and increasing post-vaccination titer (P = 2.1 × 10(−159)–1.1 × 10(−123)). Questionnaires completed by 87% of the participants revealed that post-vaccination HAI titer showed association with repeated previous influenza vaccinations. Gender had no effect on vaccine response whereas age had a strong effect and explained 1.6–3.1% of HAI post-vaccination titer variance and 3.1% of H1N1 MN titer variance. Vaccine response, both fold increase and seroprotection rate (percentage of individuals reaching HAI ≥ 40 or MN ≥ 20), was higher in vaccinees ≤37 years of age (YoA) than all other age groups. Furthermore, a reduction was observed in the H1N1 MN titer in people ≥63 YoA, demonstrating a decreased neutralizing functionality of vaccine-induced antibodies at older age. We tested the effects of underlying autoimmune diseases, asthma and allergic diseases and did not observe significant associations with vaccine responses. Intake of immune modulating medication did not show any association. Taken together, our results show that previous encounter of influenza vaccination or infection, reflected in high HAI and MN pre-vaccination titer has the strongest negative effect on vaccine responses measured as FC and the strongest positive effect on post-vaccination titer. Increasing age had also an effect but not gender, underlying disease or medication.
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spelling pubmed-57666582018-01-22 Age and Influenza-Specific Pre-Vaccination Antibodies Strongly Affect Influenza Vaccine Responses in the Icelandic Population whereas Disease and Medication Have Small Effects Olafsdottir, Thorunn A. Alexandersson, Kristjan F. Sveinbjornsson, Gardar Lapini, Giulia Palladino, Laura Montomoli, Emanuele Del Giudice, Giuseppe Gudbjartsson, Daniel F. Jonsdottir, Ingileif Front Immunol Immunology Influenza vaccination remains the best strategy for the prevention of influenza virus-related disease and reduction of disease severity and mortality. However, there is large individual variation in influenza vaccine responses. In this study, we investigated the effects of gender, age, underlying diseases, and medication on vaccine responses in 1,852 Icelanders of broad age range who received trivalent inactivated influenza virus vaccination in 2012, 2013, or 2015. Hemagglutination inhibition (HAI) and microneutralization (MN) titers were measured in pre- and post-vaccination sera. Of the variables tested, the strongest association was with level of pre-vaccination titer that explained a major part of the variance observed in post-vaccination titers, ranging from 19 to 29%, and from 7 to 21% in fold change (FC), depending on the strain and serological (HAI or MN) analysis performed. Thus, increasing pre-vaccination titer associated with decreasing FC (P = 1.1 × 10(−99)–8.6 × 10(−30)) and increasing post-vaccination titer (P = 2.1 × 10(−159)–1.1 × 10(−123)). Questionnaires completed by 87% of the participants revealed that post-vaccination HAI titer showed association with repeated previous influenza vaccinations. Gender had no effect on vaccine response whereas age had a strong effect and explained 1.6–3.1% of HAI post-vaccination titer variance and 3.1% of H1N1 MN titer variance. Vaccine response, both fold increase and seroprotection rate (percentage of individuals reaching HAI ≥ 40 or MN ≥ 20), was higher in vaccinees ≤37 years of age (YoA) than all other age groups. Furthermore, a reduction was observed in the H1N1 MN titer in people ≥63 YoA, demonstrating a decreased neutralizing functionality of vaccine-induced antibodies at older age. We tested the effects of underlying autoimmune diseases, asthma and allergic diseases and did not observe significant associations with vaccine responses. Intake of immune modulating medication did not show any association. Taken together, our results show that previous encounter of influenza vaccination or infection, reflected in high HAI and MN pre-vaccination titer has the strongest negative effect on vaccine responses measured as FC and the strongest positive effect on post-vaccination titer. Increasing age had also an effect but not gender, underlying disease or medication. Frontiers Media S.A. 2018-01-08 /pmc/articles/PMC5766658/ /pubmed/29358933 http://dx.doi.org/10.3389/fimmu.2017.01872 Text en Copyright © 2018 Olafsdottir, Alexandersson, Sveinbjornsson, Lapini, Palladino, Montomoli, Del Giudice, Gudbjartsson and Jonsdottir. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Immunology
Olafsdottir, Thorunn A.
Alexandersson, Kristjan F.
Sveinbjornsson, Gardar
Lapini, Giulia
Palladino, Laura
Montomoli, Emanuele
Del Giudice, Giuseppe
Gudbjartsson, Daniel F.
Jonsdottir, Ingileif
Age and Influenza-Specific Pre-Vaccination Antibodies Strongly Affect Influenza Vaccine Responses in the Icelandic Population whereas Disease and Medication Have Small Effects
title Age and Influenza-Specific Pre-Vaccination Antibodies Strongly Affect Influenza Vaccine Responses in the Icelandic Population whereas Disease and Medication Have Small Effects
title_full Age and Influenza-Specific Pre-Vaccination Antibodies Strongly Affect Influenza Vaccine Responses in the Icelandic Population whereas Disease and Medication Have Small Effects
title_fullStr Age and Influenza-Specific Pre-Vaccination Antibodies Strongly Affect Influenza Vaccine Responses in the Icelandic Population whereas Disease and Medication Have Small Effects
title_full_unstemmed Age and Influenza-Specific Pre-Vaccination Antibodies Strongly Affect Influenza Vaccine Responses in the Icelandic Population whereas Disease and Medication Have Small Effects
title_short Age and Influenza-Specific Pre-Vaccination Antibodies Strongly Affect Influenza Vaccine Responses in the Icelandic Population whereas Disease and Medication Have Small Effects
title_sort age and influenza-specific pre-vaccination antibodies strongly affect influenza vaccine responses in the icelandic population whereas disease and medication have small effects
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5766658/
https://www.ncbi.nlm.nih.gov/pubmed/29358933
http://dx.doi.org/10.3389/fimmu.2017.01872
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