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. 2023 Nov 20:14:1272119.
doi: 10.3389/fimmu.2023.1272119. eCollection 2023.

A 12-month follow-up of the immune response to SARS-CoV-2 primary vaccination: evidence from a real-world study

Giorgio Fedele  1 , Ilaria Schiavoni #  1 , Filippo Trentini #  2   3 , Pasqualina Leone  1 , Eleonora Olivetta  4 , Alessandra Fallucca  5 , Stefano Fiore  1 , Angela Di Martino  1 , Sergio Abrignani #  6   7 , Vincenzo Baldo #  8 , Tatjana Baldovin #  8 , Alessandra Bandera #  9   10 , Pierangelo Clerici #  11 , Massimo De Paschale #  11 , Fabiana Diaco #  12 , Alexander Domnich #  13 , Francesca Fortunato #  14 , Irene Giberti #  13 , Andrea Gori #  11   15 , Renata Grifantini #  6 , Tiziana Lazzarotto #  16   17 , Vittorio Lodi #  18 , Claudio Maria Mastroianni #  19 , Rosa Prato #  13 , Vincenzo Restivo #  5 , Francesco Vitale #  5 , Silvio Brusaferro  20 , Stefano Merler  2 , Anna Teresa Palamara  1 , Paola Stefanelli  1 ; Study Group for the Immunological Monitoring post Covid19 vaccination
Affiliations

A 12-month follow-up of the immune response to SARS-CoV-2 primary vaccination: evidence from a real-world study

Giorgio Fedele et al. Front Immunol. .

Abstract

A real-world population-based longitudinal study, aimed at determining the magnitude and duration of immunity induced by different types of vaccines against COVID-19, started in 2021 by enrolling a cohort of 2,497 individuals at time of their first vaccination. The study cohort included both healthy adults aged ≤65 years and elderly subjects aged >65 years with two or more co-morbidities. Here, patterns of anti-SARS-CoV-2 humoral and cell-mediated specific immune response, assessed on 1,182 remaining subjects, at 6 (T6) and 12 months (T12) after the first vaccine dose, are described. At T12 median anti-Spike IgG antibody levels were increased compared to T6. The determinants of increased anti-Spike IgG were the receipt of a third vaccine dose between T6 and T12 and being positive for anti-Nucleocapside IgG at T12, a marker of recent infection, while age had no significant effect. The capacity of T12 sera to neutralize in vitro the ancestral B strain and the Omicron BA.5 variant was assessed in a subgroup of vaccinated subjects. A correlation between anti-S IgG levels and sera neutralizing capacity was identified and higher neutralizing capacity was evident in healthy adults compared to frail elderly subjects and in those who were positive for anti-Nucleocapside IgG at T12. Remarkably, one third of T12 sera from anti-Nucleocapside IgG negative older individuals were unable to neutralize the BA.5 variant strain. Finally, the evaluation of T-cell mediated immunity showed that most analysed subjects, independently from age and comorbidity, displayed Spike-specific responses with a high degree of polyfunctionality, especially in the CD8 compartment. In conclusion, vaccinated subjects had high levels of circulating antibodies against SARS-CoV-2 Spike protein 12 months after the primary vaccination, which increased as compared to T6. The enhancing effect could be attributable to the administration of a third vaccine dose but also to the occurrence of breakthrough infection. Older individuals, especially those who were anti-Nucleocapside IgG negative, displayed an impaired capacity to neutralize the BA.5 variant strain. Spike specific T-cell responses, able to sustain immunity and maintain the ability to fight the infection, were present in most of older and younger subjects assayed at T12.

Keywords: SARS-CoV-2; T-cell; immune response; serology; vaccines.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.

Figures

Figure 1
Figure 1
SARS-CoV-2 trimeric S IgG antibody concentration (log-transformed values) 6 months (T6) and 12 months (T12) after first dose of vaccine. Data are presented for the whole sample (A), healthy adults ≤ 65 years of age (under 65, B), frail elderly > 65 years of age (65+, C). Mean values in each group are indicated (thick lines).
Figure 2
Figure 2
SARS-CoV-2 trimeric S IgG antibody concentration (log-transformed values) 6 months (T6) and 12 months (T12) after first dose of vaccine. Data are stratified according to the receipt of a third vaccine dose and presented for healthy adults ≤ 65 years of age (under 65, A, B) and frail elderly > 65 years of age (65+, C, D). Mean values in each group are indicated (thick lines).
Figure 3
Figure 3
SARS-CoV-2 trimeric S IgG antibody concentration (log-transformed values) 6 months (T6) and 12 months (T12) after first dose of vaccine. Data are stratified according to anti-N IgG positivity at T12 and presented for healthy adults ≤ 65 years of age (under 65, A, B) and frail elderly > 65 years of age (65+, C, D). Mean values in each group are indicated (thick lines).
Figure 4
Figure 4
Microneutralization titers of T12 sera from healthy adults (N=39, A) and frail elderly subjects (N=34, panel B) who received three doses of mRNA vaccine. Data were stratified according to anti-N IgG positivity at T12 and refer to neutralization against WT SARS-CoV-2 reference strain (B) and a BA.5 Omicron variant strain. Individual MNT are reported together with median values. Non-neutralizing sera (cut-off MNT<8) are placed on the x-axis, Statistical differences were calculated by one-way ANOVA test,.
Figure 5
Figure 5
T-cell mediated immune response of COVID-19 healthy adults ≤65 years (Under, N=63) and frail elderly individuals >65 years (Over, N=40) who received three doses of mRNA vaccine. Individual frequencies of CD4+ and CD8+ T cells producing IFNγ, TNFα and IL-12 in healthy adults and frail elderly subjects in response to in vitro stimulation with Spike antigen are shown (A). Pie diagrams show the frequencies of non-responding T cells or T cells producing from 1 to 3 simultaneous cytokines (B).
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