Infection with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the causative agent of coronavirus disease-19 (COVID-19), can be asymptomatic or lead to a broad spectrum of disease manifestations from mild to severe disease and death. There is evidence showing that acute COVID-19 causes a profound activation of innate and adaptive immune cells, and distinct immunological signatures are shown to correlate with disease outcomes (Mathew et al., 2020). Viral control and mild disease associate with the rapid generation of T-cells and antibodies targeting SARS-CoV-2 (Lucas et al., 2021; Tan et al., 2021), while severe disease is characterised by immune cell hyperactivation and a ‘cytokine storm’ (Chen et al., 2020; Kuri-Cervantes et al., 2020; Ruan et al., 2020). Commonly observed biomarkers of severe COVID-19 include lymphopenia, increased neutrophil to T-cell ratio, and elevated levels of pro-inflammatory cytokines/mediators such as interleukin-6 (IL-6), IL-10, IL-17, monocyte chemoattractant protein-1 (MCP-1), interferon gamma-induced protein 10 (IP-10), CRP, IL-1Rα, and IL-1β. In a smaller proportion of individuals, severe COVID-19 may be driven by pre-existing anti-interferon gamma (anti-IFN-γ) autoantibodies (Bastard et al., 2020; Liu et al., 2020; Lucas et al., 2020; Zhao et al., 2020). Other distinctive features of severe disease include a dysregulation in the myeloid compartment consisting of increased circulating immature/dysfunctional neutrophils and immature Ki67⁺ COX-2^low monocytes (Mann et al., 2020; Schulte-Schrepping et al., 2020; Wu et al., 2020; Mardi et al., 2021), while T-cell activation and proliferation appears to be heterogenous in severe patients (Mathew et al., 2020; Kuri-Cervantes et al., 2020).

The kinetics of immune recovery following the changes occurring during acute COVID-19 are complex and not fully understood. Longitudinal studies show that immune abnormalities and inflammation may persist after severe COVID-19, with highly activated myeloid cells, pro-inflammatory cytokines, and persistently activated T-cells detected 8–12 months after COVID-19 (Bergamaschi et al., 2021; Phetsouphanh et al., 2022; Taeschler et al., 2022).

The potential impact of prolonged immune activation post recovery and whether it may underlie the symptoms of post-acute sequelae of SARS-CoV-2 infection or long COVID - a syndrome characterised by long-lasting symptoms affecting multiple organs - remains unclear. Long COVID is observed in 8–21% of individuals following mild to severe COVID-19, although a higher prevalence of symptoms is reported in patients requiring ICU admission and/or mechanical ventilation (Alwan, 2021; Nalbandian et al., 2021; Ballering et al., 2022). Several studies have reported a correlation between long COVID symptoms and a variety of immune profiles including a more rapid decline of SARS-CoV-2 memory CD8⁺ T-cells and lower levels of cytotoxic SARS-CoV-2 N-specific CD8⁺ T-cells (Peluso et al., 2021), increased levels of cytotoxic CD8⁺ T-cells, and elevated plasma levels of type I cytokines, IL-1β and IL-6 (Shuwa et al., 2021; Schultheiß et al., 2022). Another longitudinal study conducted in 69 patients found long COVID to associate with an altered immune blood cell transcriptome which included significant changes in genes involved in cell cycle, but not with the phenotypic profiles of these cells (Ryan et al., 2022). A large UK cohort study (PHOSP-COVID) of hospitalised COVID-19 patients identified female sex, obesity, and invasive mechanical ventilation as factors associated with a lower likelihood of full recovery, with an overall recovery rate of 28.9% at both 5 and 12 months across all disease severities (Evans et al., 2022). Similarly, other cohort studies have identified associations between poor recovery from COVID-19 and demographic factors such as sex and age, but also highlight a possible role of immune dysregulation that occurs in older age, obesity and asthma, which warrants further investigation (Sneller et al., 2022; Halpin et al., 2021; Thompson et al., 2022). Other hypotheses proposed to explain the mechanisms underlying long COVID include unresolved lung tissue damage, the persistence of SARS-CoV-2 infection, the reactivation of latent viruses such as human cytomegalovirus (CMV) and Epstein-Barr virus and autoimmunity (Proal and VanElzakker, 2021; Gatto et al., 2022; Plüß et al., 2021; Zollner et al., 2022). Due to the limited effectiveness of COVID-19 vaccines in protecting from re-infection, SARS-CoV-2 continues to circulate within our populations and millions of people worldwide are at risk of experiencing long-term health complications from COVID-19. Studies suggest that COVID-19 vaccination may reduce the risk of developing long COVID (Al-Aly et al., 2022; Notarte et al., 2022). Nevertheless the burden of long COVID threatens to increase and further compromise our post-pandemic economic recovery. A better understanding of the mechanisms underlying long COVID and the design/repurposing of drugs to treat or prevent this syndrome is urgently needed.

In this study we investigated whether patients who had COVID-19, 3 months post hospitalisation display persistent immune activation and ongoing inflammation and if there are potential links between the observed immune profiles, COVID-19 disease severity and long COVID symptoms. We also investigated whether persistent immune activation and disease severity have an impact on the capacity of patients to generate and maintain a memory T-cell response and antibodies to SARS-CoV-2. Our immunological analysis of 187 samples from 63 hospitalised patients recovering from mild, moderate, or severe disease showed increased levels of activated CD4⁺ and CD8⁺ T-cells and increased plasma levels of T-cell-related cytokines (IL-4, IL-7, IL-17, and tumor necrosis factor-alpha [TNF-α]) at 3 months in severe compared to moderate/mild patients. T-cell activation and cytokine levels decreased at 12 months and were comparable in mild, moderate, and severe patients. The SARS-CoV-2-specific memory T-cell response to spike, membrane and nucleocapsid was robust and qualitatively similar across the disease severities, however the magnitude of the CD4⁺ and CD8⁺ T-cell and antibody response was higher in patients with moderate compared to mild disease, as were the plasma levels of IFN-γ, a key cytokine for anti-viral immunity. Long COVID symptoms at 3 months were reported in 80% of patients across all disease severities but were more frequent in patients with severe disease. Poisson regression analysis showed a significant association between ongoing symptoms and the frequency of a subset of moderately activated CD4⁺ T and non-cytotoxic HLA-DR⁺ CD8⁺ T-cells in unadjusted analyses, but these associations did not meet the criteria for statistical significance after adjusting for age, sex, and severity grades. Our results demonstrate the presence of immune perturbations in peripheral blood CD4⁺ and CD8⁺ T-cell populations in severe COVID-19 patients 3 months after hospitalisation with no direct association between long COVID symptoms and immune activation/pro-inflammatory cytokines, for the markers that were measured.

Emerging data demonstrates that immune activation may persist for months after COVID-19, however there is heterogeneity in findings particularly between hospitalised versus non-hospitalised cohorts, which by nature of how patients were managed during the peak of the pandemic comprise of patients with a very different spectrum of disease. Here, we report results from a small study performed on a cohort of clinically well-characterised mild, moderate, and severe patients who were all hospitalised at the start of the pandemic and followed up closely through outpatient follow-up clinics up to 12 months post admission. We ask whether ongoing inflammation and immune perturbations, particularly within the T-cell population, associate with long COVID symptoms. Specifically, we ask the following questions: (1) Is there evidence of ongoing inflammatory events post hospitalisation with COVID-19, and are these linked with disease severity at acute infection? (2) Are the magnitude and features of the SARS-CoV-2-specific CD4⁺ and CD8⁺ T-cell memory response influenced by disease severity? (3) Do long COVID symptoms associate with persistent immune activation, inflammation, and/or SARS-CoV-2-specific T-cell immunity? To answer these questions, we performed an in-depth immunological analysis of 187 samples from 63 patients at 3 and 12 months post admission, including a characterisation of activation/proliferation profiles and phenotypic features of circulating CD4⁺ and CD8⁺ T-cells, γδ-T-cells, NK cells, B cells, and CD14^+/-CD16^+/- monocytes by flow cytometry, as well as an analysis of T-cells and antibodies targeting SARS-CoV-2 and pro-inflammatory plasma cytokines/chemokines by Luminex at 3, 8, and 12 months. Our data shows persistent CD4⁺ and CD8⁺ T-cell activation and elevated plasma levels of IL-4, IL-7, IL-17, and TNF-α at 3 months, in severe compared to mild and/or moderate patients. The elevated levels of these cytokines are consistent with ongoing T-cell activation as CD4⁺ T-cells are key producers of IL-4 and IL-17 and both CD4⁺ and CD8⁺ T-cells secrete TNF-α. IL-7 stimulates proliferation of T-cells and can be produced by a variety of cells such as epithelial cells, stromal cells, and dendritic cells. Plasma levels of IL-4, IL-7, and IL-15 were similar at acute infection and 3 months but declined at later time points, suggesting a slow recovery of T-cell-related perturbations within 12 months. CD4⁺ and CD8⁺ T-cell activation was evident when we analysed the flow cytometry data both by manual gating and by FlowSOM/UMAP - where the former method investigates cells expressing known combinations of markers, while the latter identifies clusters of cells in an unsupervised manner based on the combined expression of all markers analysed. Manual gating highlighted increased levels of CD4⁺ T-cells expressing the lung tissue-homing marker CXCR3 in severe patients, suggesting the presence of factors that may be recruiting and priming CD4⁺ T-cells in this site. This finding may suggest unresolved damage/inflammation in the lung, however clinical abnormalities in lung function were evident only in a minority of these patients during the follow-up clinic (Al-Aly et al., 2022). Both manual and FlowSOM/UMAP analysis show increased granzyme B expression in CD8⁺ T-cells from severe patients, suggesting an overall higher cytotoxic ability of these cells. Granzyme B expression is upregulated in cells after T-cell receptor (TCR) stimulation and confers higher cytotoxic abilities to the activated T-cell, hence higher expression could reflect a higher activation state in these cells. Interestingly, expression of CXCR3 is reduced (and undetectable) in both CD4⁺ and CD8⁺ T-cells at 12 compared to 3 months post admission (Figure 2—figure supplement 1). Expression of granzyme B was also decreased in CD8⁺ T-cells at 12 compared to 3 months. Ongoing T-cell activation did not appear to impair the ability of severe patients to mount and maintain memory T-cell or antibody responses to SARS-CoV-2 structural proteins, which were present and robust across all patients. The quality of the T-cell response was also similar across the patient groups, and we could detect monofunctional and polyfunctional SARS-CoV-2-specific T-cells, with the former dominating the response. However, moderate compared to mild patients displayed elevated spike RBD antibody titers and higher magnitudes of CD4⁺ and CD8⁺ T-cells producing IFN-γ and/or TNF-α/CD107a by ICS, after stimulation with spike-1 peptides. The magnitude of the T-cell response is closely linked with viremia (Miller et al., 2008) and higher viral loads during the acute illness may underlie the higher magnitude of IFN-γ/TNF-α producing CD4⁺ and CD8⁺ T-cells. However, viremia data at acute illness was not available for our patient cohort. The frequency of T-cells producing IFN-γ alone did not differ in the ICS analysis, in line with the ELISpot data. Cytokine production following PMA/ionomycin were comparable between patients, suggesting similar T-cell functionality to polyclonal stimulation that bypasses the TCR.

T-cells can be activated through TCR triggering or ‘bystander activated’ by cytokines such as IL-7 and IL-15. Bystander T-cell activation was observed to occur during viral infection and is likely driven by IL-15 (Sandalova et al., 2010; Rivino et al., 2015). Here, we demonstrate that co-culture of plasma from severe patients induced upregulation of the IL-15 receptor (IL-15R)-α-chain on T-cells from healthy donors, suggesting that the low-level proliferation of T-cells we see in severe patients may be bystander in nature and driven by plasma cytokines persistently present at 3 months in severe patients. Highly differentiated T-cells are more responsive to IL-15 due to their higher expression of the IL-15R (Geginat et al., 2003; Rivino et al., 2004). The higher responsiveness of CMV-specific T-cells, which are highly differentiated cells, has been proposed as a mechanism to explain why these cells are commonly activated/proliferating during acute viral infections such as dengue, HBV, and COVID-19 (Sandalova et al., 2010; Rivino et al., 2015; Gregorova et al., 2020). It may be possible that the low-level proliferation of CMV-pp65-specific CD4⁺ T-cells observed in this study is driven by cytokines which are still elevated at 3 months. Our data does not support the persistence of SARS-CoV-2 antigens at 3 months for two reasons. Firstly, we would expect that the persistence of SARS-CoV-2 antigens in vivo would result in the activation of SARS-CoV-2-specific T-cells, however we did not observe expression of markers of activation nor proliferation in spike-1-specific T-cells in our ICS analysis. Secondly, we did not detect any SARS-CoV-2 RNA by RT-PCR - however we cannot exclude that SARS-CoV-2 antigens may still be present but are sequestered in specific sites to which T-cells do not have access.

Prolonged T-cell activation after acute infection has been observed in other severe respiratory infections and may not be specific for COVID-19. In H7N9 influenza infection persistent T-cell activation was associated with fatal disease while T-cell activation early during infection associated with positive clinical outcomes, however the frequencies of bystander-activated T-cells in fatal patients was high (approx. 20% of CD8⁺ T-cells) (Wang et al., 2018). Further studies are needed to understand the impact of prolonged T-cell activation following acute viral infections.

In this study the levels of CRP, albumin, and IL-6 at 3 months were similar across patients, suggesting an overall resolution of the inflammatory processes occurring during the acute infection. In contrast, a recent study showed increased levels of several pro-inflammatory markers at 12 months, including CRP and IL-6, which correlated with the presence of persistently activated T-cells. Interestingly the authors showed that COVID-19 mRNA vaccination and boosting of SARS-CoV-2 immunity did not alter these profiles, suggesting inflammation may be independent of the presence of SARS-CoV-2 antigens in these patients (Taeschler et al., 2022). We cannot exclude that the presence of activated T-cells may be linked to the comorbidities experienced by the patients in this cohort, which included obesity, type-1 and -2 diabetes, and asthma. These comorbidities were present across all groups but increased progressively with disease severity (Table 1). However, at 12 months post admission T-cell activation was similar and largely undetectable in patients with mild, moderate, and severe disease, suggesting that the differences we observe between patients at 3 months may not be driven by differences in T-cell activation already present in these patients prior to COVID-19.

Due to the limited number of cells available we were unable to analyse T-cell phenotypes associated with regulatory and anti-inflammatory activity. This represents a limitation of this study. The relatively small patient cohort as well as the lack of ethnic diversity of patients who were predominately white Caucasians represents another limitation of this study.

Long COVID symptoms were reported in 80% of patients across all disease severities but were more frequent in patients with severe disease, in line with published findings (Cabrera Martimbianco et al., 2021). The factors driving long COVID remain largely unclear, as do those underlying the long-term fatigue syndromes that have previously been observed following other viral infections (Hickie et al., 2006). Although the prevalence of long COVID is reported to be higher in hospitalised patients and those who received intensive care support, the risk factors of developing a severe acute illness (male sex, age, obesity, ethnicity, and cardiovascular disease) only partially overlap with those reported to associate with long COVID (female sex, age, obesity, anxiety, asthma), suggesting that pathogenesis at acute infection and in convalescence may be driven by distinct mechanisms (Evans et al., 2022; Sneller et al., 2022; Halpin et al., 2021; Thompson et al., 2022). In this study, Poisson regression analysis showed no association between ongoing symptoms and immune perturbations after adjusting for age, sex, and severity grades, but identified a significant association between ongoing symptoms and the frequency of a cluster of moderately activated CD4⁺ T-cells (cluster 2) and a cluster of activated, non-cytotoxic HLA-DR⁺ CD8⁺ T-cells (cluster 4) in unadjusted analyses, after FDR correction. Our study adds to emerging data suggesting that a prolonged immune activation can be observed following COVID-19 which may not directly associate with long COVID (Evans et al., 2022; Sneller et al., 2022). The clinical implications of persistent T-cell activation following COVID-19 remain unclear and warrant further investigation.

In summary, our study highlights a complex recovery of the immune system following severe COVID-19 with evidence of persistent activation of CD4⁺ and CD8⁺ T-cells, which may be bystander driven, and elevated levels of T-cell-related cytokines in the plasma of severe patients at 3 months. Our data suggests the lack of a direct association between long COVID and immune activation markers and pro-inflammatory cytokines measured in this study.

All data generated or analysed during this study are included in the manuscript files or supplementary files. Raw file (FCS files) for all flow cytometry data have been deposited in the FlowRepository, the link for access to the data is provided in the Material and Methods, Flow cytometry data analysis section.The code script and data for the analysis in Figure 6 are publicly available on GitHub (copy archived at Hamilton, 2022).

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Author details

1. Marianna Santopaolo

   School of Cellular and Molecular Medicine, University of Bristol, Bristol, United Kingdom

   Contribution

   Formal analysis, Investigation, Writing - review and editing

   Contributed equally with

   Michaela Gregorova

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0009-0008-7593-287X

2. Michaela Gregorova

   School of Cellular and Molecular Medicine, University of Bristol, Bristol, United Kingdom

   Contribution

   Formal analysis, Investigation, Writing - review and editing

   Contributed equally with

   Marianna Santopaolo

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-1605-0558

3. Fergus Hamilton

   Academic Respiratory Unit, North Bristol NHS Trust, Bristol, United Kingdom

   Contribution

   Formal analysis, Funding acquisition, Investigation

   Competing interests

   No competing interests declared

4. David Arnold

   Academic Respiratory Unit, North Bristol NHS Trust, Bristol, United Kingdom

   Contribution

   Funding acquisition, Investigation

   Competing interests

   No competing interests declared

5. Anna Long

   Diabetes and Metabolism, Bristol Medical School, University of Bristol, Bristol, United Kingdom

   Contribution

   Investigation, Methodology

   Competing interests

   No competing interests declared

6. Aurora Lacey

   School of Cellular and Molecular Medicine, University of Bristol, Bristol, United Kingdom

   Contribution

   Formal analysis, Investigation

   Competing interests

   No competing interests declared

7. Elizabeth Oliver

   School of Cellular and Molecular Medicine, University of Bristol, Bristol, United Kingdom

   Contribution

   Investigation

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-1211-1942

8. Alice Halliday

   School of Cellular and Molecular Medicine, University of Bristol, Bristol, United Kingdom

   Contribution

   Formal analysis, Investigation, Methodology

   Competing interests

   No competing interests declared

9. Holly Baum

   School of Cellular and Molecular Medicine, University of Bristol, Bristol, United Kingdom

   Contribution

   Formal analysis, Investigation, Methodology

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-1311-6446

10. Kristy Hamilton

    School of Cellular and Molecular Medicine, University of Bristol, Bristol, United Kingdom

    Contribution

    Formal analysis, Investigation

    Competing interests

    No competing interests declared

11. Rachel Milligan

    School of Cellular and Molecular Medicine, University of Bristol, Bristol, United Kingdom

    Contribution

    Formal analysis, Investigation

    Competing interests

    No competing interests declared

12. Olivia Pearce

    Diabetes and Metabolism, Bristol Medical School, University of Bristol, Bristol, United Kingdom

    Contribution

    Formal analysis, Investigation, Methodology

    Competing interests

    No competing interests declared

13. Lea Knezevic

    Bristol Veterinary School, University of Bristol, Bristol, United Kingdom

    Contribution

    Investigation

    Competing interests

    No competing interests declared

14. Begonia Morales Aza

    School of Cellular and Molecular Medicine, University of Bristol, Bristol, United Kingdom

    Contribution

    Formal analysis, Investigation

    Competing interests

    No competing interests declared

15. Alice Milne

    Academic Respiratory Unit, North Bristol NHS Trust, Bristol, United Kingdom

    Contribution

    Investigation

    Competing interests

    No competing interests declared

16. Emily Milodowski

    Bristol Veterinary School, University of Bristol, Bristol, United Kingdom

    Contribution

    Investigation

    Competing interests

    No competing interests declared

17. Eben Jones

    School of Cellular and Molecular Medicine, University of Bristol, Bristol, United Kingdom

    Contribution

    Formal analysis, Writing - review and editing

    Competing interests

    No competing interests declared

18. Rajeka Lazarus

    University Hospitals Bristol and Weston NHS Foundation Trust, Bristol, United Kingdom

    Contribution

    Resources, Writing - review and editing

    Competing interests

    No competing interests declared

19. Anu Goenka

    1. School of Cellular and Molecular Medicine, University of Bristol, Bristol, United Kingdom
    2. Department of Paediatric Immunology and Infectious Diseases, Bristol Royal Hospital for Children, Bristol, United Kingdom

    Contribution

    Supervision, Funding acquisition, Writing - review and editing

    Competing interests

    No competing interests declared

20. Adam Finn

    1. School of Cellular and Molecular Medicine, University of Bristol, Bristol, United Kingdom
    2. Department of Paediatric Immunology and Infectious Diseases, Bristol Royal Hospital for Children, Bristol, United Kingdom
    3. School of Population Health Sciences, University of Bristol, Bristol, United Kingdom

    Contribution

    Supervision, Funding acquisition

    Competing interests

    No competing interests declared

21. Nicholas Maskell

    Academic Respiratory Unit, North Bristol NHS Trust, Bristol, United Kingdom

    Contribution

    Resources, Supervision, Funding acquisition

    Competing interests

    No competing interests declared

22. Andrew D Davidson

    School of Cellular and Molecular Medicine, University of Bristol, Bristol, United Kingdom

    Contribution

    Formal analysis, Supervision, Investigation

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0002-1136-4008

23. Kathleen Gillespie

    Diabetes and Metabolism, Bristol Medical School, University of Bristol, Bristol, United Kingdom

    Contribution

    Resources, Formal analysis, Supervision, Methodology

    Competing interests

    No competing interests declared

24. Linda Wooldridge

    Bristol Veterinary School, University of Bristol, Bristol, United Kingdom

    Contribution

    Supervision, Funding acquisition, Writing - review and editing

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0002-6213-347X

25. Laura Rivino

    School of Cellular and Molecular Medicine, University of Bristol, Bristol, United Kingdom

    Contribution

    Conceptualization, Supervision, Funding acquisition, Writing - original draft, Project administration

    For correspondence

    laura.rivino@bristol.ac.uk

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0001-6213-9794

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