Many adults and children experience prolonged symptoms after severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection. These ongoing, relapsing, or new symptoms as well as other detrimental health effects are referred to as post-acute sequelae of SARS-CoV-2 infection (PASC) or ‘long COVID’ when present 4 or more weeks after the acute phase of SARS-CoV-2 infection. While it has become clear that PASC can present with a myriad of symptoms affecting different organ systems, why this occurs is still largely unknown. Understanding the mechanisms underlying PASC is crucial for the development of appropriate preventive and treatment strategies.

Immune dysregulation has been established as a key pathogenic feature of acute COVID-19 and also plays a role in the pathogenesis of systemic and tissue-specific PASC manifestations. However, the causal mechanisms of immune dysfunction in PASC need to be defined. The mechanisms of immune dysregulation likely vary depending on the PASC clinical phenotype, the severity of the initial COVID-19 infection, as well as the specific tissues involved. Well-designed studies can help elucidate the role of immune mechanisms in PASC.

The NIH-funded Researching COVID to Enhance Recovery (RECOVER) Initiative, which was launched in February 2021, involves more than 100 researchers across the United States who are carrying out studies on PASC (also commonly referred to as ‘long COVID’), either via new studies or by leveraging pre-pandemic long-term cohort studies, implementing the same set of protocols. A central part of RECOVER is the generation of a large SARS-CoV-2 recovery cohort where researchers will collect data from individuals across the lifespan using electronic health records and patient-completed surveys. A subset of participants will also provide biospecimens including blood, nasal swabs, saliva, lymph node aspirants, etc. (https://recovercovid.org/protocols). The ultimate goal is to use the data and resource products to develop preventive and therapeutic treatments in light of the incalculable public health impact of COVID-19 and PASC.

The Mechanistic Pathways Committee within the RECOVER consortium focuses on three mechanistic priority areas – immunopathology, viral persistence, and tissue damage – as the potential salient mechanisms underlying various clinical PASC phenotypes. This perspective article (alongside the companion papers on viral persistence [Chen et al., 2023] and PASC tissue damage [Sherif et al., 2023]) aims to provide a brief overview of current knowledge and raise important questions and hypotheses in these three areas to identify gaps in understanding the mechanisms of disease severity and sequelae of COVID-19, generate new thoughts and ideas, that will help design studies and direct research efforts.

In this article, multiple researchers with wide-ranging expertise in adult and pediatric medicine came together to review the role of the innate and adaptive immune systems in the pathogenesis of acute SARS-CoV-2 infection and PASC. The focus on immune mechanisms here emphasizes the dysregulation of immune processes that are intertwined with the viral persistence and tissue-specific pathologies [discussed in companion reviews] that will likely be needed to address the range of different PASC subtypes which have been defined recently by RECOVER investigators (Reese et al., 2023). Potential hypotheses for PASC-related immune dysregulation are also discussed with suggestions for studies that can help answer these vital questions. Even though there are likely key differences between immune mechanisms during acute COVID-19 and those involved in PASC, the acute immunopathology of COVID-19 can serve as a starting point for examining candidate pathways involved in the immunopathology of PASC. We will therefore outline the established knowledge on acute COVID-19 as well as the limited data on the immunopathology of chronic PASC to highlight important new avenues for research on PASC immunopathology.

The role of the adaptive immune system in COVID-19 and PASC

T and B cells in COVID-19 and PASC

The role of the adaptive immune compartment in the pathophysiology of PASC is an active area of investigation. The SARS-CoV-2-specific T cell response has been well characterized in acute and convalescent COVID-19 (Sette and Crotty, 2021; Moss, 2022), and studies suggest these responses likely contribute to virus clearance (Tan et al., 2021), correlate with both peak and durable antibody responses (Rydyznski Moderbacher et al., 2020; Cohen et al., 2021; Dan et al., 2021; Zuo et al., 2021a; van der Ploeg et al., 2022), and may help protect against re-infection (Moss, 2022). Although the presence of SARS-CoV-2-specific T cell responses has been associated with milder disease in acute and convalescent COVID-19 patients (Rydyznski Moderbacher et al., 2020; Sekine et al., 2020), a robust, proinflammatory T cell response has also been associated with more severe manifestations of acute COVID-19 (Popescu et al., 2022; van der Ploeg et al., 2022). Similarly, a dysregulated B cell response, including germinal center derangements and extrafollicular B cell activation, has also been implicated in the pathogenesis of severe and critical COVID-19 (Kaneko et al., 2020; Nielsen et al., 2020; Woodruff et al., 2020; Röltgen et al., 2022).

Several studies have evaluated the role of SARS-CoV-2-specific T cells in the pathophysiology of PASC, with somewhat mixed findings. An earlier study identified lower and more rapidly waning nucleocapsid-specific cytotoxic CD8+ T cells among individuals with PASC compared with those without PASC (Peluso et al., 2021a). Similarly, another study found that patients with PASC had reduced CD4+ and CD8+ effector memory cell numbers and increased PD-1 (programmed cell death protein 1) expression on central memory cells (Glynne et al., 2022). However, these studies could not determine whether this represented decreased functional capacity of virus-specific CD8+ T cells vs. generalized dysfunction/persistent antigenic stimulation. In contrast, a more recent study reported that patients with pulmonary PASC had significantly higher frequencies of interferon-gamma (IFNg) and TNF producing SARS-CoV-2-specific T cells in peripheral blood compared to individuals without PASC (Littlefield et al., 2022). This study also observed that higher levels of immune activation – manifested by circulating plasma inflammatory biomarkers (IL-6 and CRP) – positively correlated with both PASC and the frequency of SARS-CoV-2-specific T cells (Littlefield et al., 2022). In line with these observations, studies have reported that patients with pulmonary manifestations of PASC have dysregulated tissue-resident memory (TRM) CD8+ T cell responses in bronchial airway lavage fluid, and that these findings were associated with impaired lung function (Vijayakumar et al., 2022). Persistence of specific TRMs has been previously noted after other viral infections and may be related to continued viral antigen presence. However, the limited number of PASC studies has not tested specific TRM responses to SARS-CoV-2 antigens.

Few studies have examined longitudinal changes in T cell profiles in patients with PASC. A few studies have documented T cell dynamics at multiple time points after COVID-19 infection in peripheral blood (Wiech et al., 2022). These studies have found that recovery from COVID-19 leads to a functional shift in T cell subsets after the first 3 months post-infection, and that these longitudinal T cell dynamics are associated with the severity of SARS-CoV-2 infection. Whether these longitudinal changes play a role in the pathophysiology of PASC remains an active area of investigation.

Regarding the role of B cells in PASC, several studies have detailed the presence of B cell-derived autoantibodies in the pathogenesis of PASC (discussed in further detail below). More recently, a transient, naive-derived antibody-secreting B cell (ASC) compartment was identified that was enriched in autoreactive potential. These cells were found to emerge during the acute phase of severe COVID-19 and regress gradually during recovery in most, but not all, patients (Woodruff et al., 2022). Importantly, autoantibodies persisted in a subset of patients with post-acute sequalae, suggesting that these ASC induced during acute COVID-19 may indeed play a role in the pathogenesis of PASC, although this remains to be determined.

Importantly, systems-based analyses have also implicated broad adaptive immune activation in the pathophysiology of PASC (Peluso et al., 2021b; Su et al., 2022). In a large, multi-omics analysis of patients with and without PASC, gastrointestinal PASC was correlated with expansion of both SARS-CoV-2- and CMV-specific populations of cytotoxic CD8+ and CD4+ T cell populations (Su et al., 2022). Notably, these populations were activated not during acute disease, but during convalescence, at the time PASC was identified (Su et al., 2022). This study also implicated SARS-CoV-2 RNAemia and Epstein–Barr virus (EBV) viremia as PASC-anticipating factors (Su et al., 2022). In another multi-omics study utilizing deep immunophenotyping, PASC was associated with increases of multiple adaptive immune populations, including exhausted T cells, IL-4/IL-6-secreting CD4+ T cells, and activated B cells (Klein et al., 2022). Individuals with PASC in this study had higher SARS-CoV-2-specific IgG against Spike and S1, but also had higher antibody responses against herpesvirus lytic antigens, as compared to vaccination-matched controls (Klein et al., 2022). Altogether, these data suggest that chronic inflammation in individuals with PASC – possibly due to persistent viral replication and/or reactivation of latent herpesviruses – may be responsible for the perturbations in the adaptive immune compartment observed.

MIS-C and Multisystem inflammatory syndrome in adults (MIS-A) are considered PASC syndromes yet exhibit a different time course and presentation than other chronic long-COVID syndromes. Children with MIS-C have significantly lower virus-specific CD4+ and CD8+ T cell responses to major SARS-CoV-2 antigens compared with children convalescing from COVID-19. However, T cell repertoire in MIS-C patients has been found in several studies to skew toward both CD4+ and CD8+ T cells expressing the T cell receptor (TCR) TRBV11-2 gene, a hallmark of superantigen-mediated activation (Moreews et al., 2021; Porritt et al., 2021; Sacco et al., 2022). Thus, this shift in TCR repertoire supports the theory that portions of the SARS-CoV-2 spike protein function as a superantigen and activates T cells according through these TCRs (Noval Rivas et al., 2022). A more detailed discussion on the immunological changes in MIS-C can be found in the companion paper on pathogenic mechanisms of PASC (Sherif et al., 2023). While shifts toward TRBV genes have been noted in adults with severe acute COVID-19 (Cheng et al., 2020) limited information currently exists for TCR repertoires in adult patients with long COVID. However, in single patient with T cell myocarditis with MIS-A, post-mortem analyses revealed T lymphocytes within the heart expressing various TRBV genes (Vannella et al., 2021).

Figure 1 shows the arcs of the immune response in COVID-19 including the theoretical schematics of the kinetics of immune responses to SARS-CoV-2 in severe and fatal COVID-19. The ‘Innate immunity’ chart line in the model refers specifically to the peak blood kinetics of innate cytokines and chemokines, which occur in a localized manner throughout the duration of an infection. In the time-controlled adaptive response schematic sketches in the figure, the time points show the important differences in the presence or absence of T cell responses and the magnitude of the viral load (Sette and Crotty, 2021). Furthermore, corresponding changes in gene expression over time in the generation of primary and secondary immune responsive proteins as the disease progresses have been shown to yield valuable insights into the biological mechanisms that distinguish adaptive from maladaptive events (Wang et al., 2022).

Figure 1

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Overall, while GM-CSF and cytokines are not released simultaneously during COVID-19 infection, they are both involved in the immune response to the virus and may play a role in disease severity. When the adaptive immune response is activated, B cells producing antibodies and T cells targeting the virus proliferate. Once the virus is cleared, most immune cells decrease in number and return to a resting state. However, in some individuals like long haulers, a subset of immune cells persists, leading to chronic inflammation and tissue damage (Figure 1). This uncoordinated and dysfunctional adaptive immune response to SARS-CoV-2 infection and viral persistence can result in a range of long-COVID symptoms. There continue to be significant gaps in our knowledge of the clinical spectrum of COVID-19, immune signaling pathways, systemic effects, and long-term pathological signatures and this must be addressed through further investigations into these different immune mechanisms depicted.

Autoantibodies in COVID-19 and PASC

Early in the COVID-19 pandemic it was suggested that autoimmunity might have a role in the hyperinflammatory disease and respiratory failure observed in severe and fatal presentations of SARS-CoV-2 infection (Favalli et al., 2020; Zhou et al., 2020b). Indeed, COVID-19 can be associated with hematological abnormalities and system dysfunction (neurological, pulmonary, cardiovascular, gastrointestinal, constitutional) resembling those previously observed in autoimmune diseases or autoimmune manifestations associated with various infectious agents, in particular viruses, mostly of unknown etiology (reviewed in Ehrenfeld et al., 2020). Moreover, in a proportion of cases, severe pulmonary manifestations have been associated with elevated concentrations of autoantibodies neutralizing type I IFNs (Bastard et al., 2020; Combes et al., 2021), a finding that has been replicated in numerous studies (reviewed in Zhang et al., 2022). These results are in keeping with a key event in COVID-19 pathogenesis, that is, dampened or delayed type I IFN responses (Blanco-Melo et al., 2020; Hadjadj et al., 2020; Galani et al., 2021; Kasuga et al., 2021; Lowery et al., 2021), which result in ineffective early control of viral replication, leading to local and systemic inflammation, vasculopathy, and organ damage (Schultze and Aschenbrenner, 2021; Merad et al., 2022).

The full breadth of autoantibodies directed against immunomodulatory proteins goes well beyond targeting type I IFNs. For example, a high-throughput discovery approach interrogating extracellular proteins showed that COVID-19 patients may bear autoantibody reactivities directed against cytokines, chemokines, and cell-surface proteins (Wang et al., 2021). Some of these reactivities may have functional effects, including neutralization of cytokines and chemokines or engagement of FcR-dependent effector functions, such as antibody-dependent cellular phagocytosis, potentially leading to immune cell depletion. Furthermore, excess autoantibodies targeting antigens expressed on the surface of immune cell subsets were associated with reduced frequencies of the corresponding immune cell types, again suggestive of functional links between autoantibodies and selective immune cell depletion (Wang et al., 2021). Thus, autoantibody production may affect various innate and adaptive immune functions and contribute to ineffective or harmful immune responses.

Autoantibodies associated with COVID-19 may be outright pathogenic. For example, antiphospholipid antibodies may activate endothelial cells and platelets and stimulate neutrophils to release NETs (Knight et al., 2021). Increased NET production correlates with thrombosis and COVID-19 severity (Zuo et al., 2021c). Moreover, elevated antibodies binding to NETs, which impair NET degradation and likely activate complement, also correlate with COVID-19 severity (Zuo et al., 2021b). Thus, abnormal coagulation, vasculopathy, and micro- and macrovascular thrombosis, which are characteristic of severe COVID-19 (Perico et al., 2021), may be associated, at least in part, to the production of these autoantibodies (reviewed in Knight et al., 2021). Autoantibody production has also been correlated with severe disease manifestations secondary to SARS-CoV-2 infection in children. In particular, MIS-C which is characterized by fever, rash, and gastrointestinal symptoms and may also have life-threatening cytopenias, coagulopathy, myocardial dysfunction, coronary aneurysms, and shock (Chou et al., 2022) has been associated with the presence of autoantigens characteristic of classical autoimmune diseases (Gruber et al., 2020). Thus, a broad repertoire of autoantibodies is seen during severe clinical manifestations of SARS-CoV-2 infection across all age groups.

Multiple mechanisms likely underlie the production of autoantibodies in patients with severe COVID-19 manifestations. In one scenario, autoantibodies may precede infection with SARS-CoV-2 and be genetically determined, as proposed, for example, for neutralizing autoantibodies against type I IFNs (Bastard et al., 2020) that, as mentioned above, dampen the early innate antiviral responses, leading to uncontrolled viral replication, hyperinflammation, and tissue damage (Merad et al., 2022). However, more recent data show very low prevalence of IFN autoantibodies in PASC patients, indicating that these antibodies may not play a role in the pathogenesis of long COVID (Peluso et al., 2023). This highlights the need to define whether preexisting auto-antibodies may predispose subjects infected with SAS-CoV-2 to develop more severe forms of PASC immunopathology. In genetically predisposed individuals SARS-CoV-2 infection could act as trigger for new-onset rheumatic autoimmune diseases. The various hypothetical mechanisms include bystander activation triggered by the cytokine storm, viral persistence causing polyclonal activation and the formation of NETs (Shah et al., 2020; Winchester et al., 2021; Zacharias et al., 2021). Arthritis and vasculitis are the most common new-onset rheumatic diseases seen in COVID-19 patients (Gracia-Ramos et al., 2021), however they are not very common.

In a second scenario, autoantibody production occurs de novo in SARS-CoV-2 infection, indicating that severe COVID-19 can break tolerance to self. New-onset IgG autoantibodies were found to react to autoantigens associated with classical and rare autoimmune diseases – ranging from antinuclear antibodies (ANA) to antibodies against connective tissue and various secreted proteins, including cytokines, chemokines, and growth factors (Chang et al., 2021). De novo production of autoantibodies implicates extrafollicular B cells, since, unlike germinal center reactions, extrafollicular maturation lacks some tolerance checkpoints that prevent the activation and maturation of autoreactive B cells, as is the case with system lupus erythematosus (Tipton et al., 2015; Jenks et al., 2018). Indeed, extrafollicular B cells, also known as double-negative B cells, were enriched in severe and fatal cases of COVID-19 (Woodruff et al., 2020) and were found to increase over time even in subjects who had experienced COVID-19 not requiring hospitalization (Mishra et al., 2021).

In a third scenario, autoantibodies may arise from reactivation of latent human herpesvirus in tissues around the time of initial infection. For example, mounting evidence exists that EBV may reactivate during acute SARS-CoV-2 infection, and be related to persistent sequelae such as fatigue and various neurocognitive symptoms (Gold et al., 2021; Peluso et al., 2022a). EBV infection has previously been linked with host antigen molecular mimicry, autoreactive immunity, and pathogenic B cell migration and activity that may lead to diseases such as multiple sclerosis (Bjornevik et al., 2022; Lanz et al., 2022; Robinson and Steinman, 2022). The extent to which latent viral reactivation may play in autoimmunity and PASC is a key area of current research.

Links may exist between the occurrence of PASC and autoimmunity. For example, one study shows that high ANA titers were seen in 43.6% of patients at 12 months post-COVID-19 symptom onset, and the frequency of neurocognitive symptoms correlated with ANA titers (Seeßle et al., 2022). However, a follow-up study in a similar sized cohort was not able to corroborate these findings (Peluso et al., 2022b). Several studies have reported an association between PASC and autoantibodies against G-protein-coupled receptors.(Hohberger et al., 2021; Wallukat et al., 2021; Szewczykowski et al., 2022). Autoantibodies have been included among risk factors for the development of PASC (Su et al., 2022) and it has even been postulated that ‘long COVID’ may be an autoimmune disease (Marshall, 2021). However, in another study, no strong association was observed between autoantigen reactivity and symptoms in COVID-19 convalescent patients. Furthermore, autoantibodies against calprotectin, which was the most common autoantibody target in the study, were associated with return to healthy, normal life 8 months post-infection, suggesting a protective – rather than pathogenic – role for these autoantibodies (Moody et al., 2022). Thus, the role of antibodies in PASC pathogenesis requires further investigation.

The key questions that need to be addressed regarding autoantibodies and PASC immunopathology include: (1) Do preexisting autoantibodies impact the incidence and severity of PASC? (2) Which autoantigens generate de novo autoantibodies, and do these persist beyond the acute phase of SARS-CoV-2 infection? (3) How does genetic predisposition to autoimmune disease affect the de novo diagnosis of classifiable autoimmune disease following the acute SARS-CoV-2 infection? (4) Can we identify specific autoantibodies that are mechanistically tied to specific forms of tissue injury? (5) Does virus-induced autoreactivity underlie some of the clinical phenotypes associated with PASC? These and many other questions raised in this article need to be answered to better understand the mechanisms of PASC.

PASC in the context of SARS-CoV-2 endemicity

Much of the research conducted on PASC has occurred in the context of SARS-CoV-2 as an emerging pathogen. As the pandemic has progressed, it appears likely that the virus will become endemic worldwide, with constant circulation in the population resulting in cyclical peaks of emergence. It is clear that some SARS-CoV-2 variants (such as the Omicron variant) have considerable resistance to preexisting immune responses generated by previous infections or vaccination. Recent studies have shown that protection against re-infection with a different variant is reduced and wanes quickly, although it appears protection against severe disease is more robust. In the context of PASC, it is unknown whether re-infection with different variants, or re-infection with the same variant after immunity wanes, affects the frequency or severity of PASC. For example, do suboptimal immune responses (such as binding antibodies that do not neutralize infection or T cell responses that are not robust) lead to reduced or enhanced pathogenicity in PASC? Furthermore, an important question moving forward is how regular, cyclical infection of SARS-CoV-2 on a population level enhances or subdues PASC frequency and severity. Future studies on this topic should carefully take into consideration the previous infection and vaccination history of study participants.

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Author details

1. Sindhu Mohandas

   Division of Infectious Diseases, Children’s Hospital Los Angeles, Keck School of Medicine, University of Southern California, Los Angeles, United States

   Contribution

   Conceptualization, Methodology, Writing – original draft, Project administration, Writing – review and editing

   For correspondence

   smohandas@chla.usc.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-8397-6249

2. Prasanna Jagannathan

   Division of Infectious Diseases and Geographic Medicine, Department of Medicine, Stanford University, Stanford, United States

   Contribution

   Conceptualization, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-6305-758X

3. Timothy J Henrich

   Division of Experimental Medicine, University of California, San Francisco, San Francisco, United States

   Contribution

   Conceptualization, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

4. Zaki A Sherif

   Department of Biochemistry & Molecular Biology, Howard University College of Medicine, Washington, United States

   Contribution

   Conceptualization, Visualization, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-1772-7041

5. Christian Bime

   Division of Pulmonary, Allergy, Critical Care & Sleep Medicine, Department of Medicine, University of Arizona College of Medicine, Tucson, United States

   Contribution

   Conceptualization, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

6. Erin Quinlan

   National Center for Complementary and Integrative Health, National Institutes of Health, Bethesda, United States

   Contribution

   Conceptualization, Writing – original draft, Writing – review and editing

   Competing interests

   is employed by the NIH which funded the RECOVER trial

7. Michael A Portman

   Seattle Children’s Hospital, Division of Pediatric Cardiology, Department of Pediatrics, University of Washington, Seattle, United States

   Contribution

   Conceptualization, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

8. Marila Gennaro

   Public Health Research Institute and Department of Medicine, Rutgers New Jersey Medical School, Newark, United States

   Contribution

   Conceptualization, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

9. Jalees Rehman

   Department of Biochemistry and Molecular Genetics, University of Illinois, College of Medicine, Chicago, United States

   Contribution

   Conceptualization, Methodology, Writing – original draft, Project administration, Writing – review and editing

   For correspondence

   jalees@uic.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-2787-9292

10. RECOVER Mechanistic Pathways Task Force

    Contribution

    Conceptualization

    Competing interests

    No competing interests declared

    1. Steven B Bradfute, Center for Global Health, Department of Internal Medicine, University of New Mexico Health Sciences Center, Albuquerque, United States
    2. Benjamin K Chen, Division of Infectious Diseases, Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, United States
    3. Thomas J Connors, Department of Pediatrics, Division of Critical Care, Columbia University Vagelos College of Physicians and Surgeons and New York - Presbyterian Morgan Stanley Children's Hospital, New York, United States
    4. K Coombs, NIH RECOVER Research Initiative: Patient representative, Bethesda, United States
    5. Christian R Gomez, Division of Lung Diseases, National Institutes of Health, National Heart, Lung and Blood Institute, Bethesda, United States
    6. Boris D Julg, Infectious Disease Division, Massachusetts General Hospital, Ragon Institute of MGH, MIT and Harvard, Cambridge, United States
    7. C Kim, NIH RECOVER Research Initiative: Patient representative, Bethesda, United States
    8. W Brian Reeves, Department of Medicine, Joe R. and Teresa Lozano Long School of Medicine, University of Texas San Antonio, San Antonio, United States

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