No, COVID-19 is NOT a new HIV

"SARS-CoV-2 might be like HIV" because

– it “exhausts” our immune system –

– it survives despite our immune system –

– it infects our immune system –

NO, NO, and NO


Introduction

A few days ago, a friend told me that they had just read that “coronavirus might be like HIV”. When I asked them what they meant, they told me “Yes, read about it - they say people might remain permanently infected with the virus.”

Coming from a scientific background, I tend to simply ignore this kind of sensationalism. Too much misinformation. But this was a bit much. Letting people take pseudo-medical headlines at face value is too unhealthy. My goal here is to demystify COVID-19 / SARS-CoV-2, fact-check the researcher's interpretations, and establish the ground zero of what we actually know.

The idea being to keep this essay as accessible as possible, I will also add a running metaphor for everyone to enjoy: our body will be a country, our immune system its military, and the infection an invading army. I will always compare the facts and the way they are reported as part of this running metaphor. If you are not into metaphors, please feel free to skip those sections and stick to the boring talk.

Last caveat: I did study molecular biology and pathologies, but it was a decade ago and I do not work in the field. Even though I spent a significant amount of time researching SARS-CoV-2, I am still not a virologist. If you find any inconsistency in my analysis, if you have any questions, or if you would want me to verify additional allegations, please do contact me at valentin [dot] vincendon [at] gmail [dot] com. I am genuinely interested in improving this essay from readers' feedback and challenge.

Spoiler

This is a very long-form article (8,500+ words).

If you only want to skim through it, here are my findings regarding the current state of academic research on SARS-CoV-2 / COVID-19:

  1. statistical significance is often ignored,

  2. references are usually missing at the weakest logical points,

  3. most of those papers have not undergone peer review,

  4. reproducibility is largely missing.

The 4 items above are the broadly accepted pillars of scientific publications. Missing one is usually enough for irrelevance. Missing several is a cause of discredit.

I would strongly advise anyone to wait for better research coverage before drawing any conclusions on SARS-CoV-2.

Definitions

The World Health Organization has named the virus and disease it causes as follows:

Virus: severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2)

Disease: coronavirus disease (COVID-19)

This is important to remember as academic papers usually refer to both.

The difference is exactly the same as HIV vs. AIDS: HIV (Human Immunodeficiency Virus) is the virus, and AIDS (Acquired Immunodeficiency Syndrome) is the disease it causes.


SARS-CoV-2 might be like HIV because it “exhausts” our immune system

Let's look at two recently published papers that are used to support this sensational statement.

Then we'll look at facts in details.

Data

In our cohort of 68 COVID-19 patients admitted [...] there were 55 cases of mild disease (MD) and 13 cases of severe disease (SD).

Is 68 large enough a sample?

Upon admission, the neutrophil count was remarkably higher in SD patients than in MD cases, whereas the lymphocyte count was significantly lower in SD cases than in MD cases. [...] Specifically, T cell and CD8+ T cell counts were decreased significantly in MD and SD patients compared with those in healthy controls (HCs). The number of T cells and CD8+ T cells was significantly lower in SD patients than that in MD cases. The counts of NK cells were reduced remarkably in SD patients compared with those in MD cases and HCs.

Are these figures statistically significant?

Are they even reliable? Another paper, 2020 - Zhou et al. - Pathogenic T cells and inflammatory monocytes incite inflammatory storm in severe COVID-19 patients (peer-reviewed?), says the exact opposite about NK cells:

The number of total leukocytes in peripheral blood had no significant differences between COVID-19 patients and healthy controls, whereas the number of lymphocytes decreased significantly in ICU patients. Specifically, monocytes from both ICU and non-ICU patients significantly decreased compared with healthy controls. The number of T cells also significantly decreased from both ICU and non-ICU patients. The CD4+ T cells from both patients in ICU and non-ICU decreased remarkably, whereas CD8+T cells decreased more significantly in ICU patients. Other kinds of leukocytes, including granulocyte, B cells and NK cells are not been significantly changed in numbers between COVID-19 patients and healthy controls.

So much for reproducibility...


Interpretation

Cytotoxic lymphocytes such as cytotoxic T lymphocytes (CTLs) and natural killer (NK) cells are necessary for the control of viral infection, and the functional exhaustion of cytotoxic lymphocytes is correlated with disease progression.

That’s a lot of affirmations in a single sentence.

  • CTLs and NKs do participate in the control of some viral infections, but they also have the unfortunate tendency to overreact and create more damages than the disease itself. We’ll come back on that when we talk about cytokines storms.

  • CTLs are not always necessary - we'll discuss it below.

  • Functional "exhaustion" has neither been defined nor proven - we’ll also come back on that.

  • Let's imagine exhaustion has been properly defined (as we'll do it together below)... The authors quote a source to prove the correlation between functional "exhaustion" of cytotoxic lymphocytes and disease progression. This source is a paper on chronic infection by the hepatitis C virus (2019 - Zhang et al. - NKG2A is a NK cell exhaustion checkpoint for HCV persistence). Only problem: SARS-CoV-2 is neither proven to be a chronic disease, nor a hepatic infection.

Together, these results suggest the functional exhaustion of cytotoxic lymphocytes in COVID-19 patients. Hence, SARS-CoV-2 may break down antiviral immunity at an early stage.

This is intrinsically incorrect: functional exhaustion does not happen at an early stage by definition. The two sentences simply cannot be logically linked.

What the facts are pointing us to is called T-cell impairment. We’ll come back on that below.


MILITARY METAPHOR

Facts: We are getting invaded, and our heavy artillery is retreating from densely-populated areas in order to avoid friendly casualties.

Interpretation: When an army keeps retreating for a very long period of times, it means it is losing. Since our artillery retreated yesterday, it means we are losing.

Headline: The enemy has special weapons which can wipe out our artillery!


This article is not peer-reviewed.

We retrospectively reviewed the counts of total T cells, CD4+, CD8+ T cell subsets, and serum cytokine concentration from inpatient data of 522 patients with laboratory-confirmed COVID-19 [...] and 40 healthy controls, who came to the hospitals for routine physical examination. In addition, the expression of T cell exhaustion markers PD-1 and Tim-3 were measured by flow cytometry in the peripheral blood of 14 COVID-19 cases.

Decent sample size (522) for T cells count... but 14 samples only with exhaustion markers?

The number of total T cells, CD4+ and CD8+ T cells were dramatically reduced in COVID-19 patients, especially among elderly patients (≥60 years of age) and in patients requiring Intensive Care Unit (ICU) care. Counts of total T cells, CD8+ T cells or CD4+ T cells lower than 800/μL, 300/μL, or 400/μL, respectively, are negatively correlated with patient survival.

First. To their credit, the authors provide satisfying statistical significance for the correlation. But as the famous quote explains it: correlation does not imply causation.

Second, the reduced number of T cells is once again part of T cell impairment reaction.

T cells from COVID-19 patients have markedly higher levels of PD-1 compared to healthy controls. Furthermore, statistical analysis showed that the percentage of PD-1+CD8+ T cells from ICU patients was significantly higher than from both Non-ICU cases and healthy controls, indicating that SARS-CoV-2 viruses induce T cell exhaustion in COVID-19 patients, particularly in those requiring ICU care.

First, I would not trust a 14-data-point "statistical" analysis if my life depended on it.

Second, PD-1 markers are one of the standard pathways responsible for the T-cell impairment reaction, as we'll see in 2019 - Rogers & Williams - Reining in the CD8+ T cell: Respiratory virus infection and PD-1-mediated T-cell impairment. This pathway happens to be hijacked by some chronic infections in order for them to exhaust our T cells and thus avoid immune reactions that would clear them from our organism, as we'll see in 2011 - Hofmeyer, Jeon & Zang - The PD-1/PD-L1 (B7-H1) Pathway in Chronic Infection-Induced Cytotoxic T Lymphocyte Exhaustion. Only this hijacking phenomenon is qualified of "exhaustion", by definition. Again, the authors are jumping the gun with the above interpretation.


MILITARY METAPHOR

Facts: Some of our soldiers looked tired. We just talked to fourteen in our whole military organisation though. Oh, and also the information just comes from Randy asking around - no one double checked.

Interpretation: Most of our forces are exhausted due to the enemy's advanced military techniques.

Headline: The enemy has special weapons which incapacitate our soldiers!


Facts

The immune system is a complex and delicate balance - "overreaction" can lead to death


Pushing the thinking to the extreme, if our immune system was to kill everything that moved, infections would not stand a chance… but we would be dead with them. In case of infection, there is an extremely complex succession of checks and balances to try and make sure that our immune system does not overreact. But he still often does, leading to immunopathologies. Below is a very high-level summary of the different signalling. Each can go wrong in many ways. When this signalling goes very wrong, it is sometimes called a cytokine storm, as you most likely have read many times in the news.

2014 - Huber et al. - T cell responses to viral infections – opportunities for peptide vaccination

T cells are capable of producing a wide range of cytokines and chemokines and can even exert cytotoxic functions themselves. Based on cytokine production, CD4+ T cells can be divided into several subsets, the most classical being Th1, Th2, and Tregs. Th1 cells are generally characterized by the production of IFN-γ. Th2 cells, on the other hand, produce mainly IL-4, IL-5, and IL-13 and are important for providing an immune response against helminths by activating eosinophils, basophils, mast cells, and B cells. The third classical subset are the Treg cells, which are characterized by the production of IL-10 and TGF-b, and have mainly regulatory tasks such as dampening effector functions and limiting immunopathology.


A significant part of SARS-CoV-2 deaths are attributable to the host's own immune system "overreacting" (immunopathology)


Looking specifically at T cells, their overreaction in the lungs can cause fatal damages to this vital organ.

2020 - Zhou et al. - Pathogenic T cells and inflammatory monocytes incite inflammatory storm in severe COVID-19 patients

Given that large amount of inflammatory cells infiltrations have been observed in lungs from severe COVID-19 patients, these aberrant pathogenic Th1 cells and inflammatory monocytes may enter the pulmonary circulation in huge numbers and play an immune damaging role to causing lung functional disability and quick mortality. Our results demonstrate that excessive non-effective host immune responses by pathogenic T cells and inflammatory monocytes may associate with severe lung pathology.

[...]

Excessive activated immune response caused by pathogenic GM-CSF+ Th1 cells and inflammatory CD14+CD16+ monocytes may connect pulmonary immunopathology leading to deleterious clinical manifestations and even acute mortality after SARS-CoV-2 infections.


Cytokine storms (a trigger of overreaction) are also triggered by the flu and other respiratory-infection-causing coronaviruses


Example of the flu.

2017 - Guo & Thomas - New fronts emerge in the influenza cytokine storm

After internalization into epithelial cells, influenza virus can be detected by innate immune sensors and trigger downstream immune responses, including tremendous cytokine production, sometimes called the “cytokine storm”. Cytokines directly induced in a virally infected cell versus those downstream from other cytokine signaling can be segregated as primary cytokines and secondary cytokines, respectively. In the primary cytokine wave, virus-infected lung epithelial, endothelial, and other immune cells produce type I and III IFNs, IL-1β, IL-18, TNF-α, IL-6, IL-33 and other cytokines, mainly to limit viral replication.


Example of other coronaviruses: SARS-CoV and MERS-CoV.

2020 - Zhou et al. - Pathogenic T cells and inflammatory monocytes incite inflammatory storm in severe COVID-19 patients

Consistent with the situation with SARS-CoV or MERS-CoV, it is remarkable that children always experience mild-moderate clinical illness, elderly individuals exhibit worse outcomes after infection with SARS-CoV-2, further indicating that mature excessive immune response towards these pathogenic human coronavirus infections play a key role in inducing severe pulmonary syndrome and even organ failure.


Thus T cells impairment (downregulation) is vital in the case of many respiratory infections


Example of the flu.

2015 - Liu, Zhou & Yang - The cytokine storm of severe influenza and development of immunomodulatory therapy

Complications arising from severe influenza are associated with inflammatory cells. Monocytes/macrophages are the main cells recruited into the alveolar space as an initial response to viral infection They then increase their cytokine production and chemoattract additional immune cells into the lesion area. Nevertheless, they are also susceptible to influenza viral infection. Depleting the monocytes/macrophages does not prevent immunopathology, indicating their important role in viral clearance.

Both CD4 and CD8 T cells are responsible for the immunopathology and viral clearance of infection. A lethal lung injury can be triggered by the transfer of antigen-specific CD8 T cells into transgenic mice expressing the influenza HA antigen. However, a lethal lung injury cannot be triggered in mice with defects in the epithelial early growth response-1 (Egr-1), suggesting that Egr-1 is a critical regulator of the immunopathology of CD8 T cells. CD4 T cells (including Th1, Th2, Th17, and Treg) have been identified to contribute to both immunopathology and viral clearance of influenza infection. Severe respiratory disease of influenza is often characterized by the early secretion of Th1 and Th17 cytokines. Tregs (regulatory CD4 Foxp3 T cells) are key managers in controlling the degree of cellular immune responses to viral infections.

Particularly, the proliferation of memory CD8 cells can be effectively controlled by the memory Tregs in an Ag-specific manner that is MHC class II dependent.

2017 - Guo & Thomas - New fronts emerge in the influenza cytokine storm

Neutralization of CD4 and CD8 T cells significantly decreases the IL-10 and IFN-γ levels in H1N1-infected lungs.

[...]

IL-10 itself may not be causative of poor outcome, but an indicator that inflammation is unrestrained. Taken together, IL-10 appears to play a time-dependent regulatory role, and may serve as an indicator of a detrimental response.


Other examples of respiratory infection viruses

2018 - Schmidt & Varga - The CD8 T Cell Response to Respiratory Virus Infections

Given the potential of CD8 T cell effector functions to cause immunopathology following respiratory virus infection, the immune system has evolved critical regulatory mechanisms to prevent prolonged CD8 T cell effector activity following viral clearance. CD8 T cell effector functions, including production of IFN-γ and TNF, are suppressed in the lung following the resolution of IAV and RSV infections. One of the primary mechanisms utilized to limit the CD8 T cell response is through suppression by regulatory CD4 T cells (Tregs). Tregs accumulate in the lungs following either RSV or IAV infection peaking at approximately day 6 post-infection, prior to the peak of the CD8 T cell response. Antibody-mediated depletion of CD25+ Tregs prior to RSV infection resulted in exacerbated weight loss, pulmonary dysfunction, and lung inflammation. This enhanced illness corresponded to an increased frequency of RSV-specific CD8 T cells and elevated levels of IFN-γ and TNF protein in the lung. Consistent with the Treg depletion studies, increasing RSV-specific Tregs prior to RSV infection using RSV peptide-immunization resulted in an amelioration of weight loss and a reduction in CD8 T cell numbers in the blood and spleen, but not the lung. Tregs also can suppress CD8 T cell effector functions following a secondary infection with IAV. Antibody-mediated CD25+ Treg depletion prior to heterosubtypic IAV challenge resulted in enhanced inflammation and pulmonary dysfunction corresponding to an increase in CD8 T cell numbers and IFN-γ production. One mechanism through which Tregs may suppress CD8 T cell responses is through the production of the anti-inflammatory cytokine IL-10. FoxP3+ Tregs secrete IL-10 following primary infection with RSV or IAV. Infection of either IL-10-deficient mice or mice treated with IL-10 receptor blocking antibody resulted in increased numbers of either IFN-γ+ or IFN-γ+TNF+ CD8 T cells, suggesting that IL-10 suppresses CD8 T cell effector functions following respiratory virus infection. Interestingly, IL-10 production by FoxP3− CD4 T cells and CD8 T cells following either RSV or IAV infection has also been reported, indicating that effector T cell responses may self-regulate their effector functions. Together, these studies demonstrate that Tregs and IL-10 production play a critical role in regulating CD8 T cells following primary and secondary respiratory virus infections to prevent immunopathology.

2019 - Rogers & Williams - Reining in the CD8+ T cell: Respiratory virus infection and PD-1-mediated T-cell impairment

Infections due to a broad range of acute viruses, including influenza virus, respiratory syncytial virus (RSV), pneumonia virus of mice, vaccinia virus (respiratory but not systemic infection), human metapneumovirus (HMPV), and others, have been associated with a state called T-cell impairment.


T cell impairment exists to prevent immunopathology - it is very different from T cell exhaustion


T cell impairment is a well-known and well-documented immune reaction to prevent immunopathology.

2011 - Hofmeyer, Jeon & Zang - The PD-1/PD-L1 (B7-H1) Pathway in Chronic Infection-Induced Cytotoxic T Lymphocyte Exhaustion

The PD-1/PD-L1 pathway regulates T cell functional capabilities by inhibiting proliferation and production of associated effector cytokines. In concert with the wide expression of PD-L1 in peripheral nonlymphoid tissues, the negative regulatory function of this pathway makes it important for preventing T-cell-mediated autoimmunity and immunopathology. However, this type of protective regulation can be usurped by pathogens, allowing them to escape immune recognition and establish a chronic infection. Overwhelming evidence shows that this does occur, particularly for chronic viral infections where CTL overexpression of PD-1 renders T cells exhausted.

2018 - Saeidi et al. - T-Cell Exhaustion in Chronic Infections: Reversing the State of Exhaustion and Reinvigorating Optimal Protective Immune Responses

Chronic antigen stimulation alone is known to be adequate in conferring T-cell exhaustion and inducing PD-1 expression. PD-1 limits T-cell activation by attenuating TCR signaling, thus preventing immunopathology.


I can't explain it better than this paper. If you are to read only one of the references quoted in this essay, this is the one.

2019 - Rogers & Williams - Reining in the CD8+ T cell: Respiratory virus infection and PD-1-mediated T-cell impairment

Left unchecked, effector T cells, inflammatory cytokines, and other immune mediators could damage healthy tissue alongside virus-infected cells. Indeed, a significant portion of lung injury after serious infections is due to immunopathology rather than to the virus infecting and killing cells. Therefore, it is necessary for the immune system to balance virus clearance and immune-mediated damage during infection, and CD8+ T-cell impairment likely represents a host mechanism of protective immunoregulation.

Similarly, once a respiratory virus is cleared, normal lung homeostasis must be restored. T-cell impairment likely represents a regulatory mechanism to restore the normal state by reducing function or survival of cytotoxic virus-specific CD8+ T cells.

[...]

T-cell impairment, mediated by PD-1 and other inhibitory receptors, represents a regulatory adaptation by the immune system to preserve healthy lung tissue during acute viral infection.


This T cell impairment is so important to prevent immunopathology that our body relies on several inhibitory channels

2018 - Schmidt & Varga - The CD8 T Cell Response to Respiratory Virus Infections

Interactions between inhibitory receptors on CD8 T cells with their ligands represents another important mechanism mediating the inhibition of CD8 T cell effector functions following infection. Regulation of CD8 T cells through the PD-1:PD-L1 pathway is a common inhibitory pathway utilized following respiratory virus infection. Expression of PD-1 on pulmonary CD8 T cells is upregulated following RSV, IAV, or HMPV infection in mice. Blockade of PD-L1 in primary RSV, IAV, or HMPV and secondary HMPV infections results in enhanced CD8 T cell effector functions, including IFN-γ, TNF, and granzyme B production. CD8 T cell effector functions are also enhanced following either HMPV or IAV infections in PD-1-deficient mice. Importantly, the PD-1:PD-L1 pathway has also been associated with human CD8 T cell responses. Human CD8 T cells in the nasal cavity significantly upregulated PD-1 following RSV infection compared to CD8 T cells from the blood of either healthy or RSV-infected individuals. PD-1 and PD-L1 are also both upregulated in the lung tissue following severe infections with either RSV or the 2009 H1N1 IAV pandemic strain. In vitro human studies have demonstrated that PD-L1 is constitutively expressed on human airway and bronchial epithelial cells, but expression is significantly upregulated following either IAV or RSV infection. Similar to in vivo mouse studies, in vitro PD-L1 blockade resulted in significantly increased CD8 T cell production of IFN-γ, IL-2, and granzyme B following RSV infection. Together, these studies demonstrate a critical role for PD-1 in the suppression of CD8 T cell-mediated immunopathology and cytokine production in both mice and humans. In the absence of PD-1 signaling following HMPV infection, CD8 T cell IFN-γ production remains impaired, suggesting the involvement of compensatory inhibitory pathways. Antigen-specific lung CD8 T cells express inhibitory receptors Tim-3, LAG-3, and 2B4 following HMPV infection and exhibit enhanced cytokine production following in vitro blockade of each receptor individually. In vivo blockade of LAG-3 partially restored CD8 T cell IFN-γ production in PD-1-deficient mice following HMPV infection. Tim-3 has also been demonstrated to be critical in suppressing CD8 T cell responses in vivo, as Tim-3 receptor (Galectin-9)-deficient mice exhibited significantly enhanced CD8 T cell responses following both primary and secondary IAV infections. Together, these studies indicate that multiple inhibitory receptor pathways are utilized following pulmonary virus infection to dampen the pathogenic CD8 T cell response and prevent immunopathology.

2019 - Rogers & Williams - Reining in the CD8+ T cell: Respiratory virus infection and PD-1-mediated T-cell impairment

Other inhibitory receptors, including Lag-3, Tim-3, 2B4, and CTLA-4 are up-regulated in response to respiratory virus infection and appear to contribute to some degree of T-cell impairment, but thus far PD-1 appears to be the dominant inhibitory receptor for ARI.


By definition, T cell exhaustion is associate with chronic diseases only

The academic literature is quite in agreement on this.

2019 - Rogers & Williams - Reining in the CD8+ T cell: Respiratory virus infection and PD-1-mediated T-cell impairment

Is T-cell impairment the same as T-cell exhaustion?

Although many of the same inhibitory receptors have been implicated in both impairment and exhaustion, these two states differ in a few significant ways. T-cell exhaustion is defined by antigen-unresponsive T cells after a prolonged antigenic stimulus, such as during chronic infections or cancer.

[...]

However, one major difference between T-cell impairment and exhaustion is timing. T-cell exhaustion requires long-term antigen exposure before inhibitory receptors become up-regulated. Acute LCMV infection is associated with transient PD-1 expression, whereas chronic LCMV infection leads to sustained PD-1 expression on epitope-specific T cells. In contrast, T-cell impairment is seen relatively early (day 7–8) in the adaptive immune response to ARI, and PD-1 expression remains high on lung lymphocytes weeks after virus is cleared.

2010 - Yi, Cox & Zajac - T-cell exhaustion: characteristics, causes and conversion

T-cell exhaustion is characterized by the stepwise and progressive loss of T-cell functions and can culminate in the physical deletion of the responding cells. Exhaustion is well-defined during chronic lymphocytic choriomeningitis virus infection and commonly develops under conditions of antigen-persistence, which occur following many chronic infections that are of significant public health concern including hepatitis B virus, hepatitis C virus and human immunodeficiency virus infections, as well as during tumour outgrowth.

[...]

Exhausted T-cell responses have been documented following numerous infections, including lymphocytic choriomeningitis virus (LCMV), polyoma virus, adenovirus, Friend leukaemia virus, mouse hepatitis virus, human immunodeficiency virus (HIV), hepatitis B virus (HBV) and hepatitis C virus (HCV), and have also been observed in patients with malignancies.1,6,10,12–29 In each of these cases initial T-cell responses are elicited, but a spectrum of phenotypic and functional defects arises as the responding cells lose their functional capabilities in a progressive and stepwise manner.

In many ways the factors that promote and maintain exhaustion are still being defined.

2004 - Fuller et al. - Maintenance, Loss, and Resurgence of T Cell Responses During Acute, Protracted, and Chronic Viral Infections

How CD8 T cell responses are impacted by changing viral loads, as well as the long-term consequences of sustained exposure to high viral burdens, is not well understood.

[...]

Virus-specific CD8 T cells are not maintained indefinitely in a functionally unresponsive state. Thus, if high viral loads persist, there is a continued attrition of virus-specific CD8 T cells as these cells become deleted from the chronically infected host. Our data show that the functional robustness of the virus-specific CD8 T cell response is determined in part by the duration of exposure to high viral loads.

2018 - Saeidi et al. - T-Cell Exhaustion in Chronic Infections: Reversing the State of Exhaustion and Reinvigorating Optimal Protective Immune Responses

Exhaustion appears to be often restricted to CD8+ T cells responses in the literature, although CD4+ T cells have also been reported to be functionally exhausted in certain chronic infections.

[...]

Chronic antigen stimulation alone is known to be adequate in conferring T-cell exhaustion and inducing PD-1 expression. PD-1 limits T-cell activation by attenuating TCR signaling, thus preventing immunopathology.


As of now, SARS-CoV-2 has been proved neither to be a chronic disease, nor to trigger T cell exhaustion


As discussed above, SARS-CoV-2 is an acute disease, not a chronic disease. Its name definitely hints us towards this fact: SARS = "Severe Acute Respiratory Syndrome". - it would be named SCRS otherwise.

By definition, T cell exhaustion is associated with chronic diseases only, who exploit the immune system's natural checks and balances that are T cell impairment in order to proliferate in the long run.

What researchers have proved so far is that SARS-CoV-2, like many other respiratory diseases, leads our immune system to moderate its own answer via T cell impairment in order to avoid collateral damages on the lungs, a vital organ.


We still don't even know for sure how SARS-CoV-2 infection is cleared


Depending on the disease, different types of T cells can be vital for our immune system to clear the infection, while some others can/should be downregulated.

2018 - Saeidi et al. - T-Cell Exhaustion in Chronic Infections: Reversing the State of Exhaustion and Reinvigorating Optimal Protective Immune Responses

Exhaustion appears to be often restricted to CD8+ T cells responses in the literature, although CD4+ T cells have also been reported to be functionally exhausted in certain chronic infections.


Namely, a low number of CD8+ T cells is associated with certainty of death in the case of the flu (in mice), but apparently had zero impact on recovery in the case of SARS-CoV (one of the viruses closest-related to SARS-CoV-2).

2009 - Chen et al. - Cellular Immune Responses to Severe Acute Respiratory Syndrome Coronavirus (SARS-CoV) Infection in Senescent BALB/c Mice: CD4+ T Cells Are Important in Control of SARS-CoV Infection

In a pneumonia model of SARS in senescent mice, we have identified a biphasic cellular immune response to SARS-CoV and found that CD4+ T cells (but not CD8+ T cells) are important in the control of disease pathogenesis and SARS-CoV replication.

The second novel finding of our study is that CD8+ T cells are not required but CD4+ T cells are important for the control of viral replication in primary SARS-CoV infection in senescent mice. CD8+ CTLs alone are not sufficient to clear SARS-CoV in the absence of both CD4+ T cells and Abs.

Depletion of CD8+ T cells alone does not affect clearance of the virus. These findings are rather surprising because CD8+ T cells are required for the control of influenza virus and other respiratory viruses. Depletion of CD8+ T cells results in prolonged replication of influenza virus and is associated with 100% mortality in mice.


As of today, we simply cannot conclude whether T cell number decrease in SARS-CoV-2 patients is due to a "healthy" downregulation or to the virus actively corrupting natural immune response.


SARS-CoV-2 might be like HIV because it survives despite our immune system

This article is not peer-reviewed.

We examined antibody generation and virus clearance in 26 patients with SARS-CoV-2 caused coronavirus disease 2019 (COVID-19) in Jinan, China.

[...]

A striking feature of some patients is that SARS-CoV-2 could exist in patients who have virus-specific IgG antibodies for a very long period, with one case for up to 36 days.

26 is hardly a reliable sample size. Even if the unique measurement of a 36-day coexistence of the virus and the host's humoral response was significant, it hardly makes SARS-CoV-2 a chronic diseases.

Whether SARS-CoV-2 can act as HCV that have developed strategies to subvert humoral immunity and persists in the body is worth further investigation.

This is absolutely non-informative. I'm coming back to HCV (herpes virus) later: the authors probably quote it randomly, but that specific comparison does not help their case.

We observed that patient 26, a 5-10 year-old female, was SARS-CoV-2 nucleic acid positive in a stool sample after 46 days of illness but became nucleic acid testing negative in specimens of sputum, stool, and nasopharyngeal swabs on day 47 post illness (Table 1). No SARS-CoV-2−specific antibodies were detected in the patient’s serum until the latest sample collection day, which was the 66th day post illness.

Although we did not collect data about virus-specific cellular immunity, it is known that cellular immunity is generated concomitantly with humoral immunity, so we could preliminarily exclude the potential role of cellular immunity in SARS-CoV-2 elimination in this case. Thus, from the data on patient 26, we may conclude that innate immunity, the first line of host defense, can play an essential role in SARS-CoV-2 clearance; moreover, innate immunity alone might be enough to clear the virus. This case may also indicate that some individuals may not generate specific antibodies after infection with SARS-CoV-2; thus, only testing SARS-CoV-2−specific antibodies is not a good standard to determine infection, but combination with the nucleic acid testing method may improve the accuracy of SARS-CoV-2 detection.

[...]

In this study, in the case of patient 26, we observed that innate immunity alone may be enough to completely clear SARS-CoV-2 infection. This is the first report that innate immunity plays such an essential role in the host defense against SARS-CoV-2, which highlights the importance of innate immunity in SARS-CoV-2 clearance. Further studies are required to determine which factors or signaling pathways of innate immunity contribute to this process. Whether individuals with such responses are still at risk for reinfection needs further exploration.

I think this is one of my new favourite academic papers. Such boldness and confidence:

  • first, mention only one data point (which seems like a measurement issue)

  • second, admitting you have not collected any control data,

  • third explaining you did not really need to... while not providing any supporting citation,

  • and finally draw three "conclusions" in a row, without the slightest logical link with the start of your argument and while several other explanations are equally plausible (which, unlike the authors, I took the time to research)

Simply incredible. All the more as they could have quoted an excellent paper on SARS-CoV (a fortiori a related virus), that supports their last statement (2009 - Chen et al. - Cellular Immune Responses to Severe Acute Respiratory Syndrome Coronavirus (SARS-CoV) Infection in Senescent BALB/c Mice: CD4 T Cells Are Important in Control of SARS-CoV Infection):

These data indicate that in the absence of both T cells and Abs [antibodies], innate defense mechanisms are able to control SARS-CoV infection.

And the authors of that article have both facts and logic on their side.


MILITARY METAPHOR

Facts: One of our informants saw some enemy troops in a part of town they were occupying. The next day, they were gone from that town. A week later, he saw some of our infantry there as well, which he had not seen before.

Interpretation: The enemy is usually routed out by our infantry. Our unique informant saw them arrive after the enemy was gone, which does not make sense because our infantry only attacks positions where we know the enemy is. Thus it must be that our artillery got rid of the enemy on its own. But this also does not make sense since our artillery and infantry always attack together. Our logical conclusion is that this specific enemy can be defeated with artillery only.

Headline: Infantry proved useless - focusing on blind bombing only from now on!


Facts


Herpes co-evolved with humans for millions of years - that's how it is "allowed" to hide


Herpes viruses are avoiding our immune system not only by escaping humoral response (antibodies), but also by "hiding" in a latent state in neurons. This is because the virus evolved a strategy of minimising symptoms in order to favour a lifelong chance of contamination (2016 - Goodrum - Human Cytomegalovirus Latency: Approaching the Gordian Knot):

Herpesviruses are ancient viruses that persist by establishing lifelong latent infections: the maintenance of viral genomes in the absence of active replication and progeny virus production. Critical to survival of the virus is the capacity to reactivate replication from latency in response to changes in the host.

CMV persistence has been fine-tuned over millions of years of coevolution with the human host, resulting in a complex Gordian knot that will require an integrated and in-depth inquiry into the viral, cellular, and host components to be fully untangle.


If the experiment results are valid, a legitimate interpretation is that the body tolerates the acute infection for some time in order to minimise collateral damage to the host from defending itself to brutally


To keep with the military metaphor: when our body gets infected, it tends to think twice before nuking reasonably useful organs such as the lungs or the liver. Instead, it tolerates infection for some time until it can train the population to resist on its own to some extent (survivor cells), and kills the rest with snipper-techniques.

2019 - Fiege et al. - Long-term surviving influenza infected cells evade CD8+ T cell mediated clearance

CD8+ T cells have been shown to control hepatitis B virus, sindbis virus, lymphocytic choriomeningitis virus, and simian immunodeficiency virus in the absence of cell lysis.

As discussed above, collateral damages by cytokine storms - and by immunopathologies in general - can be much more destructing that the virus itself.


This is proved to be the case in the case of the flu - at least some strains, such as Influenza A virus (IAV).

2019 - Fiege et al. - Long-term surviving influenza infected cells evade CD8+ T cell mediated clearance

Influenza A virus (IAV) is a negative sense segmented RNA virus causing significant morbidity and mortality annually. IAV has a broad tropism in the respiratory tract infecting club cells, ciliated cells, type I and type II alveolar cells among others. IAV drives destruction of infected cells directly through lytic virus replication and indirectly from the innate and adaptive immune response’s efforts to eliminate the infection. However, we and others, have previously shown IAV infected pulmonary epithelial cells can survive acute IAV infection.

Survivor cells express a robust interferon simulated gene (ISG) signature, facilitating a transient non-specific antiviral environment in the lung, and protecting against secondary viral infection. Despite the extensive damage caused by viral replication and antiviral immune responses, the lung is able to recover through significant remodeling and repair. While the turnover of pulmonary epithelial cells in the steady state is slow, after injury epithelial cells undergo proliferation to prevent vascular leakage and differentiation to restore lung function. In addition, rare pulmonary progenitor cells are also critical for the repair of the upper and lower airway.

CD8+ T cells are critical for the control of acute IAV infections. CD8+ T cells use perforin and granzyme as well as FasL and TRAIL to specifically kill IAV infected cells. There are several mechanisms by which cells can evade CD8+ T cell-mediated control. Cells can downregulate MHC-I, a strategy employed by quiescent stem cells, tumor cells, and cells infected with some viruses. The inhibitory ligand, PD-L1, can bind to PD-1 on CD8+ T cells and inhibit T cell effector functions. During IAV infection epithelial cells upregulate PD-L1 resulting in decreased IAV titers. CD8+ T cells can also control virus infected cells without destroying the cell. After hepatitis B virus infection, CD8+ T cells secrete IFN-γ and TNF-α to stop viral replication and cure infected hepatocytes. It is unclear if survivor epithelial cells are inherently resistant to cytolysis, downregulate MHC-I, or if non-cytolytic control of IAV facilitates their survival and evasion from CD8+ T cell-mediated elimination. In this study we demonstrate that in addition to club cells, ciliated epithelial cells, type I and type II alveolar cells can survive IAV infection. Surviving cells undergo enhanced proliferation compared to uninfected cells after IAV clearance and survivor cells are stable in the lungs until at least 99 days post infection. When we investigated how the adaptive immune system fails to kill survivor cells, we discovered that survivor cells are not inherently resistant to CD8+ T cell killing, do not employ active mechanisms to dampen the response and demonstrate that they lack IAV antigen. These results suggest that survivor cells rapidly clear the infection to evade killing from the adaptive immune system. This study sheds new light on the biology of cells that survive acute IAV infection.


This is the case for SARS-CoV as well (one of the viruses closest-related to SARS-CoV-2).

2007 - Cheng et al. - Severe Acute Respiratory Syndrome Coronavirus as an Agent of Emerging and Reemerging Infection

Since SARS-CoV appears to evade the triggering of IFN-α and IFN-β in human macrophages in vitro, the lack of an antiviral innate immune response may permit uncontrolled viral replication with progressive increases in viral load and the accompanying proinflammatory systemic response. This situation continues into the second week of illness until the appearance of the adaptive immune response, which brings viral replication under control.


This is even the case for Hepatitis B, which targets one of the fastest-regenerating organs in the human body, the liver.

1996 - Guidotti et al. - Intracellular Inactivation of the Hepatitis B Virus by Cytotoxic T Lymphocytes

In hepatitis B virus (HBV)-infected humans, viral clearance is associated with the development of a vigorous cellular immune response and an acute necroinflammatory liver disease, termed viral hepatitis (reviewed by Chisari and Ferrari 1995). Hence, it is widely assumed that HBV clearance is mediated principally by the destruction of infected cells by virus-specific MHC class I–restricted CTL. This assumption may be incorrect, however, for at least two reasons. First, the CTL response may not be able to reach, recognize, and destroy the vast number of infected hepatocytes (up to 10^11 cells) in the liver by direct physical contact. Second, HBV clearance is usually associated with clinical recovery, not death, despite the fact that the virus can infect virtually all hepatocytes. Rapid and complete viral clearance, without massive hepatocellular necrosis, is also the rule following woodchuck hepatitis virus (WHV) infection, during which virtually all the woodchuck hepatocytes are infected (Kajino et al. 1994). For these reasons, we favor the notion that viral clearance during HBV infection may be mediated by noncytolytic antiviral effects of CTL, and that the associated liver disease is an unfortunate complication of CTL activation rather than a determining factor in viral clearance.

The experimental approaches to HBV pathogenesis have been hampered because the host range of HBV is limited to man and chimpanzees and because culture systems for the propagation of HBV do not exist. Recently, however, we produced transgenic mice that replicate the HBV genome and sustain the HBV lifecycle in their hepatocytes (Guidotti et al. 1995). We now report that HBV-specific CD8+ CTL can abolish HBV gene expression and replication in the liver of these transgenic mice while killing only a small fraction of the hepatocytes. This effect is mediated by inflammatory cytokines such as IFNγ and TNFα, apparently activating the hepatocytes to eliminate cytoplasmic HBV nucleocapsid particles with their replicating viral genomes and to destabilize the viral RNA, thereby interrupting viral replication. All of these events occur in perfectly viable hepatocytes that are entirely normal cytologically.


Another very reasonable explanation remains: this single datapoint was a false positive


Yeah, it happens. Not even talking about human mistakes (which might be the case here considering the odd data point): tests are never 100% accurate. Moreover, tests are usually leaning towards favouring false positives rather than false negatives. It makes sense. We'd rather be woken up by an annoying alarm once at night to discover that there is no actual fire, rather than not being woken up the day there is an actual fire and die. Similarly with infections or cancers.

I could not find any proper research on this in the case of SARS-CoV-2 (please write to me if you do), BUT


1. This has been confirmed by the South Korean government (one of the most extensively testing countries in the world).

Most direct/reliable source I could find:

The Korea Herald - Tests in recovered patients found false positives, not reinfections, experts say

South Korea’s infectious disease experts said Thursday that dead virus fragments were the likely cause of over 260 people here testing positive again for the novel coronavirus days and even weeks after marking full recoveries.

[...]

The tests detected the ribonucleic acid of the dead virus,” said Oh, a Seoul National University hospital doctor, at a press conference Thursday held at the National Medical Center.

[...]

“The respiratory epithelial cell has a half-life of up to three months, and RNA virus in the cell can be detected with PCR testing one to two months after the elimination of the cell,” Oh said.


2. This was the case for SARS-CoV (one of the viruses closest-related to SARS-CoV-2)

2004 - Woo et al. - False-Positive Results in a Recombinant Severe Acute Respiratory Syndrome-Associated Coronavirus (SARS-CoV) Nucleocapsid Enzyme-Linked Immunosorbent Assay Due to HCoV-OC43 and HCoV-229E Rectified by Western Blotting with Recombinant SARS-CoV Spike Polypeptide

Three of the 21 and 1 of the 7 convalescent-phase serum samples from persons with increases in antibodies against HCoV-OC43 and HCoV-229E, respectively, tested positive by the recombinant SARS-CoV nucleocapsid protein-based ELISA. None of these samples were found to contain a specific antibody in the recombinant SARS-CoV spike polypeptide-based Western blot assay.

2005 - Maache et al. - False-Positive Results in a Recombinant Severe Acute Respiratory Syndrome-Associated Coronavirus (SARS-CoV) Nucleocapsid-Based Western Blot Assay Were Rectified by the Use of Two Subunits (S1 and S2) of Spike for Detection of Antibody to SARS-CoV

To evaluate the reactivity of the recombinant proteins expressed in Escherichia coli strain BL21(DE3), a Western blot assay was performed by using a panel of 78 serum samples obtained, respectively, from convalescent-phase patients infected with severe acute respiratory syndrome-associated coronavirus (SARS-CoV) (30 samples) and from healthy donors (48 samples). As antigen for detection of SARS-CoV, the nucleocapsid protein (N) showed high sensitivity and strong reactivity with all samples from SARS-CoV patients and cross-reacted with all serum samples from healthy subjects, with either those obtained from China (10 samples) or those obtained from France (38 serum samples), giving then a significant rate of false positives.

Specifically, our data indicated that the two subunits, S1 (residues 14 to 760) and S2 (residues 761 to 1190), resulted from the divided spike reacted with all samples from SARS-CoV patients and without any cross-reactivity with any of the healthy serum samples. Consequently, these data revealed the nonspecific nature of N protein in serodiagnosis of SARS-CoV compared with the S1 and S2, where the specificity is of 100%. Moreover, the reported results indicated that the use of one single protein as a detection antigen of SARS-CoV infection may lead to false-positive diagnosis. These may be rectified by using more than one protein for the serodiagnosis of SARS-CoV.

Mind me. This is not enough to categorically rule out actual virus persistence and/or reinfection, as claimed by the authors of the article we are analysing in this section. But it is certainly enough to cast doubt on their conclusions.


SARS-CoV-2 might be like HIV because it infects our immune system

Surprisingly, over several replicates, we saw that the T-cell lines were significantly more sensitive to SARS-CoV-2 infection when compared with SARS-CoV.

[...]

Similar to MERS-CoV, SARS-CoV-2 failed to replicate in MT-2 cells.

[MT-2 is an immortalised cell line of T lymphocytes (T-cells).]

Translation: so far, no one has been able to identify any replication of SARS-CoV-2 inside T-cells.

I don't even have a metaphor for this one. Self-explanatory.


Facts


Many other viruses infect immune cells


COVID-19 is not the flu. But in the case of the flu, monocytes/macrophages are also infected by the virus responsible for the infection.

2015 - Liu, Zhou & Yang - The cytokine storm of severe influenza and development of immunomodulatory therapy

Complications arising from severe influenza are associated with inflammatory cells. Monocytes/macrophages are the main cells recruited into the alveolar space as an initial response to viral infection. They then increase their cytokine production and chemoattract additional immune cells into the lesion area. Nevertheless, they are also susceptible to influenza viral infection. Depleting the monocytes/macrophages does not prevent immunopathology, indicating their important role in viral clearance.


SARS-CoV-2 is one of many other zoonotic diseases


It means it has "jumped" to infecting humans, from usually infecting animals.

2009 - Chen et al. - Cellular Immune Responses to Severe Acute Respiratory Syndrome Coronavirus (SARS-CoV) Infection in Senescent BALB/c Mice: CD4+ T Cells Are Important in Control of SARS-CoV Infection

Coronaviruses are well-known to undergo genetic recombination, which may lead to new genotypes and outbreaks. The presence of a large reservoir of SARS-CoV-like viruses in horseshoe bats, together with the culture of eating exotic mammals in southern China, is a timebomb. The possibility of the reemergence of SARS and other novel viruses from animals or laboratories and therefore the need for preparedness should not be ignored.


Sadly, zoonotic are rather well-studied considering their significant prevalence and impact on mankind, especially in the past decades.

AIDS, Ebola, Chichikungunya, Dengue, and Zika are all diseases induced by infection from viruses that originate from animals.

2018 - Supramaniam et al. - How myeloid cells contribute to the pathogenesis of prominent emerging zoonotic diseases

Up to 75 % of emerging human diseases are zoonoses, spread from animals to humans. Although bacteria, fungi and parasites can be causative agents, the majority of zoonotic infections are caused by viral pathogens. During the past 20 years many factors have converged to cause a dramatic resurgence or emergence of zoonotic diseases. Some of these factors include demographics, social changes, urban sprawl, changes in agricultural practices and global climate changes. In the period between 2014–2017 zoonotic viruses including ebola virus (EBOV), chikungunya virus (CHIKV), dengue virus (DENV) and zika virus (ZIKV), caused prominent outbreaks resulting in significant public health and economic burdens, especially in developing areas where these diseases are most prevalent.


Most Zoonic diseases that (might) establish lifelong latency replicate or can replicate in the immune cells they use as infection niche

In the case of Ebola, Chikungunya, Dengue and Zika, that reservoir seems to be myeloid cells. Lymphocytes are not part of the myeloid cells family. They are part of the lymphoid cells family.

But the important part is not which cell group they are from, because HIV does use lymphoid cells as a chronic infection niche. What really matters is that in all cases, and whether the infection is chronic or latent, the virus remains either replicating or replication-competent inside the immune cells it has infected.

2018 - Forrester - Ebola virus and persistent chronic infection: when does replication cease?

In chronic persistent infection, disease is caused by an actively replicating virus, but presumably at low level. In contrast, in latent infection replication has ceased, although the virus remains replication competent.

EBOV induces an exaggerated innate immune response.

[...]

Survival depends on how well the innate and adaptive immune responses can contain viral proliferation.

A myeloid cell niche has been proposed as a common mechanism for viral persistence in other infections such as Dengue, Chikungunya and Marburg virus.

In tissues such as the uveal tract, the meninges, the synovium and the testis, where the infected myeloid cell has limited exposure to memory T cells, the newly recruited infected dendritic cell may survive and permit the virus to proliferate unchecked or partially checked (low grade chronic inflammation). This might explain the random recurrence of disease in these tissues, since the balance between low level immune cell surveillance and low level viral replication will be constantly shifting.

2018 - Supramaniam et al. - How myeloid cells contribute to the pathogenesis of prominent emerging zoonotic diseases

When a viral pathogen invades a new human host, it is the innate immune system that serves as the first line of defence. Myeloid cells are especially important to help fight viral infections, including those of zoonotic origins. However, viruses such as EBOV, CHIKV, DENV and ZIKV have evolved mechanisms that allow circumvention of the host’s innate immune response, avoiding eradication and leading to severe clinical disease.

SARS-CoV-2 has not been shown capable to replicate in infected immune cells.


The mechanism behind HIV's lifelong latency is much much more complex than just "killing" T cells


HIV does not randomly kill T cells. That would be too simple. After the initial infection, HIV very efficiently uses a fast-generating subset of CD4+ T cells as a niche to keep replicating. This triggers the chronic infection, the progressive immunodeficiency, and ultimately the host's death by opportunistic infections. It is a tragically brilliant way to corrupt our immune system.

2013 - Okoye & Picker - CD4+ T cell depletion in HIV infection: mechanisms of immunological failure

Transmitted strains of HIV use CCR5 as co-receptor, which confers ′CCR5-tropism′. Importantly, CCR5 is not expressed by all CD4+ T cells, but rather, in keeping with its role in direction of the migration of effector-differentiated T cells to extra-lymphoid sites of inflammation or host defense, its expression is upregulated as part of the late differentiation of effector and effector memory T cells. It is therefore predominantly expressed by CD4+ T cells in effector sites like the lamina propria of the intestinal mucosa. CCR5-tropism is not accidental. It represents a fundamental adaption of the virus that allows infection of a subset of CD4+ T cells (effector-differentiated cells in extra-lymphoid effector sites and their immediate precursors in secondary lymphoid tissues) that can be rapidly regenerated from less differentiated, CCR5− precursors. This adaptation provides the virus with a large initial target population (CD4+ T cells in effector sites), and once these are depleted, the host courteously provides a continuous stream of new targets that maintain infection over the long-term and increase the likelihood of viral transmission.

We are very far from any evidence that SARS-CoV-2 could be doing something similar.

Conclusion

I already wrote way too much on this so I'll be brief:

  1. statistical significance is often ignored,

  2. references are usually missing at the weakest logical points,

  3. most of those papers have not undergone peer review,

  4. reproducibility is largely missing.

The 4 items above are the broadly accepted pillars of scientific publications. Missing one is usually enough for irrelevance. Missing several is a cause of discredit.

I would strongly advise anyone to wait for better research coverage before drawing any conclusions on SARS-CoV-2.


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References

Other

2004 - Fuller et al. - Maintenance, Loss, and Resurgence of T Cell Responses During Acute, Protracted, and Chronic Viral Infections

2004 - Woo et al. - False-Positive Results in a Recombinant Severe Acute Respiratory Syndrome-Associated Coronavirus (SARS-CoV) Nucleocapsid Enzyme-Linked Immunosorbent Assay Due to HCoV-OC43 and HCoV-229E Rectified by Western Blotting with Recombinant SARS-CoV Spike Polypeptide

2005 - Maache et al. - False-Positive Results in a Recombinant Severe Acute Respiratory Syndrome-Associated Coronavirus (SARS-CoV) Nucleocapsid-Based Western Blot Assay Were Rectified by the Use of Two Subunits (S1 and S2) of Spike for Detection of Antibody to SARS-CoV

2007 - Cheng et al. - Severe Acute Respiratory Syndrome Coronavirus as an Agent of Emerging and Reemerging Infection

2009 - Chen et al. - Cellular Immune Responses to Severe Acute Respiratory Syndrome Coronavirus (SARS-CoV) Infection in Senescent BALB/c Mice: CD4+ T Cells Are Important in Control of SARS-CoV Infection

2010 - Yi, Cox & Zajac - T-cell exhaustion: characteristics, causes and conversion

2011 - Hofmeyer, Jeon & Zang - The PD-1/PD-L1 (B7-H1) Pathway in Chronic Infection-Induced Cytotoxic T Lymphocyte Exhaustion

2013 - Okoye & Picker - CD4+ T cell depletion in HIV infection: mechanisms of immunological failure

2014 - Häggström - Medical gallery of Mikael Häggström

2014 - Huber et al. - T cell responses to viral infections – opportunities for peptide vaccination

2015 - Liu, Zhou & Yang - The cytokine storm of severe influenza and development of immunomodulatory therapy

2016 - Goodrum - Human Cytomegalovirus Latency: Approaching the Gordian Knot

2017 - Guo & Thomas - New fronts emerge in the influenza cytokine storm

2018 - Forrester - Ebola virus and persistent chronic infection: when does replication cease?

2018 - Saeidi et al. - T-Cell Exhaustion in Chronic Infections: Reversing the State of Exhaustion and Reinvigorating Optimal Protective Immune Responses

2018 - Supramaniam et al. - How myeloid cells contribute to the pathogenesis of prominent emerging zoonotic diseases

2018 - Schmidt & Varga - The CD8 T Cell Response to Respiratory Virus Infections

2019 - Fiege et al. - Long-term surviving influenza infected cells evade CD8+ T cell mediated clearance

2019 - Rogers & Williams - Reining in the CD8+ T cell: Respiratory virus infection and PD-1-mediated T-cell impairment

2019 - Zhang et al. - NKG2A is a NK cell exhaustion checkpoint for HCV persistence