Longitudinal Evaluation of Severe Acute Respiratory Syndrome Coronavirus 2 T-Cell Immunity Over 2 Years Following Vaccination and Infection

Anna Karina Juhl; Lisa Loksø Dietz; Ole Schmeltz Søgaard; Joanne Reekie; Henrik Nielsen; Isik Somuncu Johansen; Thomas Benfield; Lothar Wiese; Nina Breinholt Stærke; Tomas Østergaard Jensen; Rikke Olesen; Kasper Iversen; Kamille Fogh; Jacob Bodilsen; Lone Wulff Madsen; Susan Olaf Lindvig; Dorthe Raben; Sidsel Dahl Andersen; Astrid Korning Hvidt; Signe Rode Andreasen; Eva Anna Marianne Baerends; Jens Lundgren; Lars Østergaard; Martin Tolstrup; ENFORCE Study Group

doi:10.1093/infdis/jiae215

Longitudinal Evaluation of Severe Acute Respiratory Syndrome Coronavirus 2 T-Cell Immunity Over 2 Years Following Vaccination and Infection

Anna Karina Juhl^*, Lisa Loksø Dietz^*, Ole Schmeltz Søgaard, Joanne Reekie, Henrik Nielsen, Isik Somuncu Johansen, Thomas Benfield, Lothar Wiese, Nina Breinholt Stærke, Tomas Østergaard Jensen, Rikke Olesen, Kasper Iversen, Kamille Fogh, Jacob Bodilsen, Lone Wulff Madsen, Susan Olaf Lindvig, Dorthe Raben, Sidsel Dahl Andersen, Astrid Korning Hvidt, Signe Rode AndreasenEva Anna Marianne Baerends, Jens Lundgren, Lars Østergaard, Martin Tolstrup, ENFORCE Study Group

^*Corresponding author for this work

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

Abstract

Background: Within a year of the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic, vaccines inducing a robust humoral and cellular immune response were implemented worldwide. However, emergence of novel variants and waning vaccine-induced immunity led to implementation of additional vaccine boosters. Methods: This prospective study evaluated the temporal profile of cellular and serological responses in a cohort of 639 SARS-CoV-2-vaccinated participants, of whom a large proportion experienced a SARS-CoV-2 infection. All participants were infection naïve at the time of their first vaccine dose. Proportions of SARS-CoV-2 spike-specific T cells were determined after each vaccine dose using the activation-induced marker assay, while levels of circulating SARS-CoV-2 antibodies were determined by the Meso Scale serology assay. Results: We found a significant increase in SARS-CoV-2 spike-specific CD4+ and CD8+ T-cell responses following the third dose of a SARS-CoV-2 messenger RNA vaccine as well as enhanced CD8+ T-cell responses after the fourth dose. Furthermore, increased age was associated with a poorer response. Finally, we observed that SARS-CoV-2 infection boosts both the cellular and humoral immune response, relative to vaccine-induced immunity alone. Conclusions: Our findings highlight the boosting effect on T-cell immunity of repeated vaccine administration. The combination of multiple vaccine doses and SARS-CoV-2 infections maintains population T-cell immunity, although with reduced levels in the elderly.

Original language	English
Journal	The Journal of Infectious Diseases
Volume	230
Issue	3
Pages (from-to)	e605-e615
ISSN	0022-1899
DOIs	https://doi.org/10.1093/infdis/jiae215
Publication status	Published - 15 Sept 2024

Keywords

COVID-19
Spike-specific T cells
cellular response
hybrid immunity
longitudinal study
vaccination

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10.1093/infdis/jiae215

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Juhl, A. K., Loksø Dietz, L., Schmeltz Søgaard, O., Reekie, J., Nielsen, H., Somuncu Johansen, I., Benfield, T., Wiese, L., Breinholt Stærke, N., Østergaard Jensen, T., Olesen, R., Iversen, K., Fogh, K., Bodilsen, J., Wulff Madsen, L., Olaf Lindvig, S., Raben, D., Dahl Andersen, S., Korning Hvidt, A., ... ENFORCE Study Group (2024). Longitudinal Evaluation of Severe Acute Respiratory Syndrome Coronavirus 2 T-Cell Immunity Over 2 Years Following Vaccination and Infection. The Journal of Infectious Diseases, 230(3), e605-e615. https://doi.org/10.1093/infdis/jiae215

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title = "Longitudinal Evaluation of Severe Acute Respiratory Syndrome Coronavirus 2 T-Cell Immunity Over 2 Years Following Vaccination and Infection",

abstract = "Background: Within a year of the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic, vaccines inducing a robust humoral and cellular immune response were implemented worldwide. However, emergence of novel variants and waning vaccine-induced immunity led to implementation of additional vaccine boosters. Methods: This prospective study evaluated the temporal profile of cellular and serological responses in a cohort of 639 SARS-CoV-2-vaccinated participants, of whom a large proportion experienced a SARS-CoV-2 infection. All participants were infection na{\"i}ve at the time of their first vaccine dose. Proportions of SARS-CoV-2 spike-specific T cells were determined after each vaccine dose using the activation-induced marker assay, while levels of circulating SARS-CoV-2 antibodies were determined by the Meso Scale serology assay. Results: We found a significant increase in SARS-CoV-2 spike-specific CD4+ and CD8+ T-cell responses following the third dose of a SARS-CoV-2 messenger RNA vaccine as well as enhanced CD8+ T-cell responses after the fourth dose. Furthermore, increased age was associated with a poorer response. Finally, we observed that SARS-CoV-2 infection boosts both the cellular and humoral immune response, relative to vaccine-induced immunity alone. Conclusions: Our findings highlight the boosting effect on T-cell immunity of repeated vaccine administration. The combination of multiple vaccine doses and SARS-CoV-2 infections maintains population T-cell immunity, although with reduced levels in the elderly.",

keywords = "COVID-19, Spike-specific T cells, cellular response, hybrid immunity, longitudinal study, vaccination",

author = "Juhl, {Anna Karina} and {Loks{\o} Dietz}, Lisa and {Schmeltz S{\o}gaard}, Ole and Joanne Reekie and Henrik Nielsen and {Somuncu Johansen}, Isik and Thomas Benfield and Lothar Wiese and {Breinholt St{\ae}rke}, Nina and {{\O}stergaard Jensen}, Tomas and Rikke Olesen and Kasper Iversen and Kamille Fogh and Jacob Bodilsen and {Wulff Madsen}, Lone and {Olaf Lindvig}, Susan and Dorthe Raben and {Dahl Andersen}, Sidsel and {Korning Hvidt}, Astrid and {Rode Andreasen}, Signe and Baerends, {Eva Anna Marianne} and Jens Lundgren and Lars {\O}stergaard and Martin Tolstrup and {ENFORCE Study Group} and Tarp, {Britta Damgaard}",

note = "Publisher Copyright: {\textcopyright} 2024 The Author(s).",

year = "2024",

month = sep,

day = "15",

doi = "10.1093/infdis/jiae215",

language = "English",

volume = "230",

pages = "e605--e615",

journal = "The Journal of Infectious Diseases",

issn = "0022-1899",

publisher = "Oxford University Press",

number = "3",

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Juhl, AK , Loksø Dietz, L , Schmeltz Søgaard, O, Reekie, J, Nielsen, H, Somuncu Johansen, I, Benfield, T, Wiese, L, Breinholt Stærke, N, Østergaard Jensen, T, Olesen, R, Iversen, K, Fogh, K, Bodilsen, J, Wulff Madsen, L, Olaf Lindvig, S, Raben, D, Dahl Andersen, S, Korning Hvidt, A, Rode Andreasen, S , Baerends, EAM, Lundgren, J, Østergaard, L , Tolstrup, M & ENFORCE Study Group 2024, 'Longitudinal Evaluation of Severe Acute Respiratory Syndrome Coronavirus 2 T-Cell Immunity Over 2 Years Following Vaccination and Infection', The Journal of Infectious Diseases, vol. 230, no. 3, pp. e605-e615. https://doi.org/10.1093/infdis/jiae215

Longitudinal Evaluation of Severe Acute Respiratory Syndrome Coronavirus 2 T-Cell Immunity Over 2 Years Following Vaccination and Infection. / Juhl, Anna Karina ; Loksø Dietz, Lisa ; Schmeltz Søgaard, Ole et al.
In: The Journal of Infectious Diseases, Vol. 230, No. 3, 15.09.2024, p. e605-e615.

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

TY - JOUR

T1 - Longitudinal Evaluation of Severe Acute Respiratory Syndrome Coronavirus 2 T-Cell Immunity Over 2 Years Following Vaccination and Infection

AU - Juhl, Anna Karina

AU - Loksø Dietz, Lisa

AU - Schmeltz Søgaard, Ole

AU - Reekie, Joanne

AU - Nielsen, Henrik

AU - Somuncu Johansen, Isik

AU - Benfield, Thomas

AU - Wiese, Lothar

AU - Breinholt Stærke, Nina

AU - Østergaard Jensen, Tomas

AU - Olesen, Rikke

AU - Iversen, Kasper

AU - Fogh, Kamille

AU - Bodilsen, Jacob

AU - Wulff Madsen, Lone

AU - Olaf Lindvig, Susan

AU - Raben, Dorthe

AU - Dahl Andersen, Sidsel

AU - Korning Hvidt, Astrid

AU - Rode Andreasen, Signe

AU - Baerends, Eva Anna Marianne

AU - Lundgren, Jens

AU - Østergaard, Lars

AU - Tolstrup, Martin

AU - ENFORCE Study Group

AU - Tarp, Britta Damgaard

PY - 2024/9/15

Y1 - 2024/9/15

N2 - Background: Within a year of the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic, vaccines inducing a robust humoral and cellular immune response were implemented worldwide. However, emergence of novel variants and waning vaccine-induced immunity led to implementation of additional vaccine boosters. Methods: This prospective study evaluated the temporal profile of cellular and serological responses in a cohort of 639 SARS-CoV-2-vaccinated participants, of whom a large proportion experienced a SARS-CoV-2 infection. All participants were infection naïve at the time of their first vaccine dose. Proportions of SARS-CoV-2 spike-specific T cells were determined after each vaccine dose using the activation-induced marker assay, while levels of circulating SARS-CoV-2 antibodies were determined by the Meso Scale serology assay. Results: We found a significant increase in SARS-CoV-2 spike-specific CD4+ and CD8+ T-cell responses following the third dose of a SARS-CoV-2 messenger RNA vaccine as well as enhanced CD8+ T-cell responses after the fourth dose. Furthermore, increased age was associated with a poorer response. Finally, we observed that SARS-CoV-2 infection boosts both the cellular and humoral immune response, relative to vaccine-induced immunity alone. Conclusions: Our findings highlight the boosting effect on T-cell immunity of repeated vaccine administration. The combination of multiple vaccine doses and SARS-CoV-2 infections maintains population T-cell immunity, although with reduced levels in the elderly.

AB - Background: Within a year of the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic, vaccines inducing a robust humoral and cellular immune response were implemented worldwide. However, emergence of novel variants and waning vaccine-induced immunity led to implementation of additional vaccine boosters. Methods: This prospective study evaluated the temporal profile of cellular and serological responses in a cohort of 639 SARS-CoV-2-vaccinated participants, of whom a large proportion experienced a SARS-CoV-2 infection. All participants were infection naïve at the time of their first vaccine dose. Proportions of SARS-CoV-2 spike-specific T cells were determined after each vaccine dose using the activation-induced marker assay, while levels of circulating SARS-CoV-2 antibodies were determined by the Meso Scale serology assay. Results: We found a significant increase in SARS-CoV-2 spike-specific CD4+ and CD8+ T-cell responses following the third dose of a SARS-CoV-2 messenger RNA vaccine as well as enhanced CD8+ T-cell responses after the fourth dose. Furthermore, increased age was associated with a poorer response. Finally, we observed that SARS-CoV-2 infection boosts both the cellular and humoral immune response, relative to vaccine-induced immunity alone. Conclusions: Our findings highlight the boosting effect on T-cell immunity of repeated vaccine administration. The combination of multiple vaccine doses and SARS-CoV-2 infections maintains population T-cell immunity, although with reduced levels in the elderly.

KW - COVID-19

KW - Spike-specific T cells

KW - cellular response

KW - hybrid immunity

KW - longitudinal study

KW - vaccination

UR - http://www.scopus.com/inward/record.url?scp=85205139744&partnerID=8YFLogxK

U2 - 10.1093/infdis/jiae215

DO - 10.1093/infdis/jiae215

M3 - Journal article

C2 - 38687181

SN - 0022-1899

VL - 230

SP - e605-e615

JO - The Journal of Infectious Diseases

JF - The Journal of Infectious Diseases

IS - 3

ER -

Longitudinal Evaluation of Severe Acute Respiratory Syndrome Coronavirus 2 T-Cell Immunity Over 2 Years Following Vaccination and Infection

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Keywords

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