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Open Access 01-12-2024 | COVID-19 | Research

Accelerated immune ageing is associated with COVID-19 disease severity

Authors: Janet M. Lord, Tonny Veenith, Jack Sullivan, Archana Sharma-Oates, Alex G. Richter, Neil J. Greening, Hamish J. C. McAuley, Rachael A. Evans, Paul Moss, Shona C. Moore, Lance Turtle, Nandan Gautam, Ahmed Gilani, Manan Bajaj, Louise V. Wain, Christopher Brightling, Betty Raman, Michael Marks, Amisha Singapuri, Omer Elneima, Peter J. M. Openshaw, Niharika A. Duggal, on behalf of the PHOSP-COVID Study collaborative group, ISARIC4C investigators

Published in: Immunity & Ageing | Issue 1/2024

Abstract

Background

The striking increase in COVID-19 severity in older adults provides a clear example of immunesenescence, the age-related remodelling of the immune system. To better characterise the association between convalescent immunesenescence and acute disease severity, we determined the immune phenotype of COVID-19 survivors and non-infected controls.

Results

We performed detailed immune phenotyping of peripheral blood mononuclear cells isolated from 103 COVID-19 survivors 3–5 months post recovery who were classified as having had severe (n = 56; age 53.12 ± 11.30 years), moderate (n = 32; age 52.28 ± 11.43 years) or mild (n = 15; age 49.67 ± 7.30 years) disease and compared with age and sex-matched healthy adults (n = 59; age 50.49 ± 10.68 years). We assessed a broad range of immune cell phenotypes to generate a composite score, IMM-AGE, to determine the degree of immune senescence. We found increased immunesenescence features in severe COVID-19 survivors compared to controls including: a reduced frequency and number of naïve CD4 and CD8 T cells (p < 0.0001); increased frequency of EMRA CD4 (p < 0.003) and CD8 T cells (p < 0.001); a higher frequency (p < 0.0001) and absolute numbers (p < 0.001) of CD28^−ve CD57^+ve senescent CD4 and CD8 T cells; higher frequency (p < 0.003) and absolute numbers (p < 0.02) of PD-1 expressing exhausted CD8 T cells; a two-fold increase in Th17 polarisation (p < 0.0001); higher frequency of memory B cells (p < 0.001) and increased frequency (p < 0.0001) and numbers (p < 0.001) of CD57^+ve senescent NK cells. As a result, the IMM-AGE score was significantly higher in severe COVID-19 survivors than in controls (p < 0.001). Few differences were seen for those with moderate disease and none for mild disease. Regression analysis revealed the only pre-existing variable influencing the IMM-AGE score was South Asian ethnicity (\(\beta\) = 0.174, p = 0.043), with a major influence being disease severity (\(\beta\) = 0.188, p = 0.01).

Conclusions

Our analyses reveal a state of enhanced immune ageing in survivors of severe COVID-19 and suggest this could be related to SARS-Cov-2 infection. Our data support the rationale for trials of anti-immune ageing interventions for improving clinical outcomes in these patients with severe disease.

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Title: Accelerated immune ageing is associated with COVID-19 disease severity
Authors: Janet M. Lord
Tonny Veenith
Jack Sullivan
Archana Sharma-Oates
Alex G. Richter
Neil J. Greening
Hamish J. C. McAuley
Rachael A. Evans
Paul Moss
Shona C. Moore
Lance Turtle
Nandan Gautam
Ahmed Gilani
Manan Bajaj
Louise V. Wain
Christopher Brightling
Betty Raman
Michael Marks
Amisha Singapuri
Omer Elneima
Peter J. M. Openshaw
Niharika A. Duggal
on behalf of the PHOSP-COVID Study collaborative group
ISARIC4C investigators
Publication date: 01-12-2024
Publisher: BioMed Central
Keyword: COVID-19
Published in: Immunity & Ageing / Issue 1/2024
Electronic ISSN: 1742-4933
DOI: https://doi.org/10.1186/s12979-023-00406-z

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