Antibody landscapes after influenza virus infection or vaccination

Fonville, Judith M.; Wilks, Samuel; James, Sarah L.; Fox, Annette; Ventresca, M.; Aban, Malet; Xue, Lumin; Jones, Terry C.; Le, Nikitina; Trung, Phạm Quang; Tran, Nhu Duong; Wong, Yan; Mosterín, Ana; Katzelnick, Leah C.; Labonte, David; Le, Thi Thanh; Net, G. van der; Skepner, Eugene; Russell, Colin A.; Kaplan, Tommy; Rimmelzwaan, Guus F.; Masurel, N.; Jong, J.C. de; Palache, Abraham; Beyer, Walter; Le, Quynh Mai; Nguyen, Tran; Wertheim, Heiman; Hurt, Aeron C.; Osterhaus, Albert D. M. E.; Barr, Ian G.; Fouchier, Ron A. M.; Horby, Peter; Smith, Derek J.

doi:10.1126/science.1256427

Cited by 402 publications

(539 citation statements)

References 32 publications

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“…Significance: *P < 0·05, **P < 0·01, ***P < 0·001. The important immune responses to older A(H1N1) strains shown in our study, have also been well demonstrated in another longitudinal study [26], and may be due to boosting by continued exposure to influenza viruses [5,11]. Observation of higher serological titres to earlier strains may also be due to a diminished immune response with each subsequent infection [7].…”

Section: Discussionsupporting

confidence: 85%

“…The haemagglutination inhibition (HI) titre is associated with the level of protection [3,4] against a given strain. However, as influenza epidemiological studies adopt a 'life course view' to the immune response, it has become apparent that interpretation of HI titre should be done within the context of the timing, order, and antigenic similarity of the viral strains to which an individual is exposed [5][6][7][8].…”

Section: Introductionmentioning

confidence: 99%

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Immunity against influenza A(H1N1) infections is determined by age at the time of initial strain circulation

et al. 2016

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SUMMARYWe explored age-dependent patterns in haemagglutination inhibition (HI) titre to seasonal [1956 A(H1N1), 1977 A(H1N1), 2007 A(H1N1)] and pandemic [A(H1N1)pdm09] influenza strains using serological data collected from an adult French influenza cohort. Subjects were recruited by their general practitioners from 2008 to 2009 and followed until 2010. We explored age-related differences between strain-specific HI titres using 1053 serological samples collected over the study period from 398 unvaccinated subjects. HI titres against the tested seasonal and pandemic strains were determined using the HI technique. Geometric mean titres (GMTs) were estimated using regression models for interval-censored data. Generalized additive mixed models were fit to log-transformed HI estimates to study the relationship between HI titre and age (age at inclusion and/or age at initial strain circulation). GMT against one strain was consistently highest in the birth cohort exposed to that strain during childhood, with peak titres observed in subjects aged 7-8 years at the time of initial strain circulation. Our results complete previous findings on influenza A(H3N2) strains and identify a strain-dependent relationship between HI titre and age at initial strain circulation.

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Section: Discussionsupporting

confidence: 85%

Section: Introductionmentioning

confidence: 99%

Immunity against influenza A(H1N1) infections is determined by age at the time of initial strain circulation

et al. 2016

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“…If a substantial proportion of first-time vaccinees are individuals who had influenza infection in the previous season, the natural immunity acquired with this prior infection will decrease the risk of influenza compared to repeat vaccinees and may lead to the erroneous conclusion that vaccine protection decreases with multiple doses. Firsttime vaccinees are necessarily younger than repeat vaccinees and their immunological background may differ in terms of the first influenza virus encountered (imprinting), lifetime number of natural infections, and the overall influenza antibody landscape [42]. The usual adjustment for age using continuous or dummy variables may not completely address this problem and residual confounding may persist.…”

Section: Methodsological Challenges For Evaluation Of Repeated Vaccinamentioning

confidence: 96%

“…It is the only vaccine given every year. This has poorly understood effects that may vary depending on whether the vaccine strain has been changed compared to the prior season (s), changes in the genetic and antigenic characteristics of circulating viruses, and the unique 'antibody landscape' determined by cumulative lifetime experience with influenza infection or vaccination [42]. As noted in the 1974 British boarding school outbreak [7], natural infection appears to convey broader and more durable immunity relative to vaccination [43].…”

Section: Possible Immune Mechanisms For Repeated Vaccination Effectsmentioning

confidence: 99%

Repeated annual influenza vaccination and vaccine effectiveness: review of evidence

Belongia

Skowronski

McLean

et al. 2017

Expert Review of Vaccines

216

171

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Introduction: Studies in the 1970s and 1980s signaled concern that repeated influenza vaccination could affect vaccine protection. The antigenic distance hypothesis provided a theoretical framework to explain variability in repeat vaccination effects based on antigenic similarity between successive vaccine components and the epidemic strain. Areas covered: A meta-analysis of vaccine effectiveness studies from 2010-11 through 2014-15 shows substantial heterogeneity in repeat vaccination effects within and between seasons and subtypes. When negative effects were observed, they were most pronounced for H3N2, especially in 2014-15 when vaccine components were unchanged and antigenically distinct from the epidemic strain. Studies of repeated vaccination across multiple seasons suggest that vaccine effectiveness may be influenced by more than one prior season. In immunogenicity studies, repeated vaccination blunts the hemagglutinin antibody response, particularly for H3N2. Expert commentary: Substantial heterogeneity in repeated vaccination effects is not surprising given the variation in study populations and seasons, and the variable effects of antigenic distance and immunological landscape in different age groups and populations. Caution is required in the interpretation of pooled results across multiple seasons, since this can mask important variation in repeat vaccination effects between seasons. Multi-season clinical studies are needed to understand repeat vaccination effects and guide recommendations. ARTICLE HISTORY

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“…In simulations, more evolved viral populations can only survive when the breadth of vaccine-induced immunity is much narrower than that of natural infection, and even in these cases, survival is rare. However, vaccination and infection stimulate similarly broad collective antibody responses (measured by serum HI) [53], suggesting that the breadths of vaccine-induced and natural immunity are similar.…”

Section: Discussionmentioning

confidence: 99%

The beneficial effects of vaccination on the evolution of seasonal influenza

Wen

Malani

Cobey

2017

Preprint

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Although vaccines against seasonal influenza are designed to protect against currently circulating strains, they may also affect the emergence of antigenically divergent strains and thereby change the rate of antigenic evolution. Such evolutionary effects could change the benefits that vaccines confer to vaccinated individuals and the host population (i.e. private and social benefits). To investigate vaccinations potential evolutionary impacts, we simulated the dynamics of an influenza-like pathogen in an annually vaccinated host population. On average, vaccination decreased the cumulative amount of antigenic evolution of the viral population and the incidence of disease. Vaccination at a 5% random annual vaccination rate (48% cumulative vaccine coverage after 20 years) decreased cumulative evolution by 56% and incidence by 76%. To understand how the evolutionary effects of vaccination might affect its private and social benefits over multiple seasons, we fit linear panel models to simulated infection and vaccination histories. Including the evolutionary effects of vaccination lowered the private benefits by 14% but increased the social benefits by 30% (at a 5% annual vaccination rate) compared to when evolutionary effects were ignored. Thus, in the long term, vaccines' private benefits may be lower and social benefits may be greater than predicted by current measurements of vaccine impact, which do not capture long-term evolutionary effects. These results suggest that conventional vaccines against seasonal influenza could greatly reduce the burden of disease by slowing antigenic evolution like universal vaccines. Furthermore, vaccination's evolutionary effects compound a collective action problem, highlighting the importance on social policies concerning vaccination.

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Antibody landscapes after influenza virus infection or vaccination

Cited by 402 publications

References 32 publications

Immunity against influenza A(H1N1) infections is determined by age at the time of initial strain circulation

Immunity against influenza A(H1N1) infections is determined by age at the time of initial strain circulation

Repeated annual influenza vaccination and vaccine effectiveness: review of evidence

The beneficial effects of vaccination on the evolution of seasonal influenza

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