HIV is a prevalent infection in KwaZulu-Natal, South Africa (Kharsany et al., 2018) which also has a high SARS-CoV-2 attack rate (Tegally et al., 2021a; Tegally et al., 2021b). HIV depletes CD4 T helper cells (Dalgleish et al., 1984) which are a critical part of the adaptive immune response and are also the main target of HIV infection. CD4 T cell death occurs after cellular infection with HIV (Westendorp et al., 1995), or in bystander or incompletely infected cells due to activation of cellular defense programs (Doitsh et al., 2010; Doitsh et al., 2014), and is halted and, to some extent, reversed by antiretroviral therapy (ART), even sub-optimal therapy (Jackson et al., 2018).

The loss of CD4 T cells leads to dysregulation of many aspects of the immune response, including germinal center formation and antibody affinity maturation, which requires help from the highly HIV susceptible CD4 T follicular helper cells (Okoye and Picker, 2013; Pallikkuth et al., 2012; Perreau et al., 2013). In association with this, HIV also causes B cell dysregulation and dysfunction (Moir and Fauci, 2013). Moreover, T cell trafficking, activation, and exhaustion profiles of both CD4 and CD8 subsets are also modulated by HIV infection (Day et al., 2006; Deeks et al., 2004; Mavigner et al., 2012).

Both antibody and T cell responses are critical for effective control and clearance of SARS-CoV-2. More severe COVID-19 disease correlates with lymphopenia and low T cell concentrations (Lucas et al., 2020; Sekine et al., 2020; Chen et al., 2020a), whilst mild disease correlates with a robust T cell response to SARS-CoV-2 (Grifoni et al., 2020; Sekine et al., 2020; Rydyznski Moderbacher et al., 2020; Mathew et al., 2020; Mateus et al., 2020; Liao et al., 2020; Chen et al., 2020b). Neutralizing antibodies and associated expansion of antibody secreting B cells (ASC) are elicited in most SARS-CoV-2 infected individuals (Woodruff et al., 2020; Robbiani et al., 2020; Quinlan et al., 2020), and neutralizing antibody titers strongly correlate with vaccine efficacy (Khoury et al., 2021; Earle et al., 2021), indicating their key role in the response to SARS-CoV-2 infection. In contrast, high neutrophil numbers are associated with more severe disease and an elevated neutrophil to lymphocyte ratio (NLR) is often considered a risk factor for a more severe COVID-19 outcome (Liu et al., 2020a; Liu et al., 2020b; Zhang et al., 2020).

Results from epidemiological studies of the interaction between HIV and SARS-CoV-2 from other locations are mixed. Several large studies observed that disease severity and/or mortality risk is increased with HIV infection (Western Cape Department of Health in collaboration with the National Institute for Communicable Diseases, South Africa et al., 2021; Geretti et al., 2021; Bhaskaran et al., 2021; Tesoriero et al., 2021; Braunstein et al., 2021; Jassat et al., 2021a) while others found no statistically significant differences in clinical presentation, adverse outcomes, or mortality (Huang et al., 2021; Sigel et al., 2020; Shalev et al., 2020; Vizcarra et al., 2020; Stoeckle et al., 2020; Dandachi et al., 2021; Härter et al., 2020; Karmen-Tuohy et al., 2020; the Northwell COVID-19 Research Consortium et al., 2020; Inciarte et al., 2020; Hadi et al., 2020). Worse outcomes for PLWH tended to be in patients with low CD4 (Hoffmann et al., 2021a; Dandachi et al., 2021; Braunstein et al., 2021) and low absolute CD4 count was a risk factor for more severe disease (Western Cape Department of Health in collaboration with the National Institute for Communicable Diseases, South Africa et al., 2021).

HIV is known to interfere with protective vaccination against multiple pathogens (Avelino-Silva et al., 2016; Carson et al., 1995; Cooper et al., 2011; Fuster et al., 2016), typically as a consequence of sub-optimal antibody responses. In line with this, results from a South-African phase IIb trial of the Novavax NVX-CoV2373 vaccine, which uses a stabilised prefusion spike protein, showed 60% efficacy in HIV-uninfected individuals. However, overall efficacy dropped to 49% upon inclusion of PLWH (Shinde et al., 2021), although it is important to note that the numbers of PLWH in the study were very small. Nonetheless, there were more breakthrough cases in PLWH in the vaccine arm than the placebo arm.

An important consideration in infections in South Africa is the infecting variant, which in the second infection wave peaking January 2021 was predominantly the B.1.351 variant of concern (VOC) now designated as the Beta variant. In the current third infection wave it is predominantly the B.1.617.2 Delta variant. We and others have shown that the Beta variant has evolved the ability to escape neutralization by antibody responses elicited by earlier strains of SARS-CoV-2 or by vaccines based on those strains (Cele et al., 2021; Wibmer et al., 2021; Garcia-Beltran et al., 2021; Hoffmann et al., 2021b). Loss of vaccine efficacy of the AstraZeneca ChAdOx vaccine in South Africa was associated with this drop in neutralization capacity (Madhi et al., 2021). The second infection wave driven by Beta infections also showed increased mortality of hospitalized cases relative to the first infection wave (Jassat et al., 2021b).

What factors contributed to the evolution of the Beta variant in South Africa is yet unclear. One possibility is intra-host evolution in immunosuppressed PLWH with advanced HIV who are unable to clear SARS-CoV-2 (Karim et al., 2021). There is also evidence that variants evolved other adaptations to the host in addition to those in the spike glycoprotein which lead to antibody escape and enhanced transmission. These include evolution of resistance to the host interferon response (Guo et al., 2021; Thorne et al., 2021), as well as enhanced cell-to-cell transmission (Rajah et al., 2021). Changes in the virus may make infection with some variants substantially different in disease course, transmission dynamics, and effect on PLWH relative to ancestral SARS-CoV-2 strains or other variants.

Here, we aimed to determine the effects of HIV on the immune response to SARS-CoV-2 infection in KwaZulu-Natal, South Africa. This is important because we need to better understand COVID-19 disease course and vaccine efficacy in this population, as well as the possible reasons for the emergence of variants which lead to immune escape from neutralizing antibodies. Our results indicate that infections in the Beta variant infection wave led to more severe disease in PLWH relative to HIV-negative participants. Higher severity was associated with a lower CD4 T cell count. Yet, the CD4 count recovered, indicating that these participants may not have had a low CD4 count when first exposed to SARS-CoV-2. In addition, there were changes in the response of immune cell subsets associated with SARS-CoV-2 infection in PLWH relative to HIV-negative participants in the first infection wave, even in the absence of a statistically significant increase in disease severity, indicating that HIV infection may modulate the immune response to SARS-CoV-2.

We observed that in our cohort, COVID-19 disease severity was higher in PLWH, consistent with some of the larger epidemiological studies (Western Cape Department of Health in collaboration with the National Institute for Communicable Diseases, South Africa et al., 2021; Geretti et al., 2021; Bhaskaran et al., 2021; Tesoriero et al., 2021; Braunstein et al., 2021; Jassat et al., 2021a), although in this study differences were detected in the frequency of participants requiring supplemental oxygen and not in mortality. Our cohort may not be a typical ’hospitalized cohort’ as the majority of participants did not require supplemental oxygen. We therefore cannot discern effects of HIV on critical SARS-CoV-2 cases since these numbers are too small in the cohort. However, focusing on lower disease severity enabled us to capture a broader range of outcomes which predominantly ranged from asymptomatic to requiring supplemental oxygen. Understanding this part of the disease spectrum could be important since it may indicate underlying changes in the immune response which affect long-term quality of life and response to vaccines.

We observed a higher fraction of PLWH requiring supplemental oxygen relative to HIV negative participants in the second, Beta variant dominated SARS-CoV-2 infection wave in KwaZulu-Natal, South Africa. The odds ratio for requiring supplemental oxygen in the second wave for PLWH was 4.0 relative to HIV negative participants. The 95% confidence intervals were wide at 1.6–10.4, reflecting the relatively small number of participants. However, confidence intervals did not overlap one.

Consistent with HIV infection leading to more severe SARS-CoV-2 infection outcomes in our study is the much younger age of PLWH requiring supplemental oxygen relative to HIV negative participants (41 versus 63 years). PLWH on supplemental oxygen also had lower frequencies of hypertension and diabetes. Age, hypertension, and diabetes are risk factors for more severe COVID-19 disease (Yang et al., 2020; Guan et al., 2020; Ambrosioni et al., 2021; Jassat et al., 2021a), and their absence may indicate that the more severe outcome is driven by another factor, with HIV infection being the simplest explanation.

The cause of the difference between waves in PLWH may be because PLWH enrolled in the second infection wave had worse suppression of HIV with ART: both the fraction of timepoints where viremia was detected and where ART was absent were about twofold higher and indeed were very high at about 40%. We therefore expected that this showed a direct link between HIV viremia and the requirement for supplemental oxygen during COVID-19 disease in PLWH. However, there was no difference in the frequency of viremia between those requiring supplemental oxygen and those not.

Furthermore, the substantial recovery of CD4 T cell counts in PLWH after SARS-CoV-2 clearance in wave 2 may be consistent with the Beta variant having more impact on the CD4 count relative to the ancestral SARS-CoV-2 strain infections in the first wave. A similar pattern was seen in the NLR, which was higher in wave two relative to wave 1 in PLWH with active SARS-CoV-2 infection, but then decreased to similar levels upon convalescence. The role of the Beta variant is supported by data showing extensive evolution, increasing the ability of Beta to escape the interferon response and result in more efficient viral cell-to-cell transmission (Guo et al., 2021; Thorne et al., 2021; Rajah et al., 2021). Beta variant hospitalizations also led to more deaths in South Africa (Jassat et al., 2021b). Therefore, the effect of the variant on PLWH in addition to HIV suppression status should be considered.

Our data detailing the SARS-CoV-2 response of more defined immune cell subsets in PLWH versus HIV negative participants is limited by the data only being available for the first infection wave. However, even in samples from that wave, there were multiple differences in correlations between cell subsets in PLWH relative to HIV negative participants, which may be another indication of differences in the immune response to SARS-CoV-2. We cannot deduce from these associations whether the differences could have an impact on disease severity. However, the fraction of CXCR3+ CD8 T cells decreased in the blood compartment and PD-1+HLA-DR+ CD8 and CD4 T cells increased. The increase in PD-1+HLA-DR+ T cells indicates T cell activation (Sauce et al., 2007; Vollbrecht et al., 2010) which associates with worse COVID-19 outcomes (Chen et al., 2020b). CXCR3 plays a key role in T cell homing to sites of inflammation and is activated by interferon-inducible ligands CXCL9, CXCL11, and CXCL10 (IP-10) (Groom and Luster, 2011; Rodda et al., 2021). A decrease in CXCR3 indicates either that T cells are less able to home to the site of infection, or that there is more inflammation in PLWH during SARS-CoV-2 infection and therefore more homing of the CXCR3+ CD8 T cells to tissues so that the fraction of CXCR3+ cells left in the blood decreases. Either way, the combination of these changes likely indicates either more pronounced SARS-CoV-2 infection or an impaired response in PLWH despite the similar infection outcomes in this wave.

In summary, PLWH showed increased disease severity mostly restricted to the second infection wave, where the Beta variant was dominant. Increased severity was associated with low CD4 T cell counts and high NLR which stabilized post-SARS-CoV-2 clearance in second wave infected PLWH to close to wave 1 PLWH values, arguing for a synergy between SARS-CoV-2 and HIV to decrease CD4 T cell numbers and increase the NLR rather than the status of HIV infection alone determining these parameters. More work is required to understand how these HIV related immune perturbations influence long-term immunity to SARS-CoV-2 infection and whether vaccine response will be affected.

All data generated or analysed during this study are included in the manuscript and supporting files.

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Author details

1. Farina Karim

   1. Africa Health Research Institute, Durban, South Africa
   2. School of Laboratory Medicine and Medical Sciences, University of KwaZulu-Natal, Durban, South Africa

   Contribution

   Conceptualization, Resources, Data curation, Formal analysis, Project administration

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-9698-016X

2. Inbal Gazy

   1. School of Laboratory Medicine and Medical Sciences, University of KwaZulu-Natal, Durban, South Africa
   2. KwaZulu-Natal Research Innovation and Sequencing Platform, Durban, South Africa

   Contribution

   Formal analysis, Methodology

   Competing interests

   No competing interests declared

3. Sandile Cele

   1. Africa Health Research Institute, Durban, South Africa
   2. School of Laboratory Medicine and Medical Sciences, University of KwaZulu-Natal, Durban, South Africa

   Contribution

   Data curation, Formal analysis

   Competing interests

   No competing interests declared

4. Yenzekile Zungu

   Africa Health Research Institute, Durban, South Africa

   Contribution

   Data curation

   Competing interests

   No competing interests declared

5. Robert Krause

   1. Africa Health Research Institute, Durban, South Africa
   2. School of Laboratory Medicine and Medical Sciences, University of KwaZulu-Natal, Durban, South Africa

   Contribution

   Data curation, Formal analysis

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-1558-0397

6. Mallory Bernstein

   Africa Health Research Institute, Durban, South Africa

   Contribution

   Data curation, Formal analysis

   Competing interests

   No competing interests declared

7. Khadija Khan

   1. Africa Health Research Institute, Durban, South Africa
   2. School of Laboratory Medicine and Medical Sciences, University of KwaZulu-Natal, Durban, South Africa

   Contribution

   Project administration

   Competing interests

   No competing interests declared

8. Yashica Ganga

   Africa Health Research Institute, Durban, South Africa

   Contribution

   Project administration

   Competing interests

   No competing interests declared

9. Hylton Rodel

   1. Africa Health Research Institute, Durban, South Africa
   2. Division of Infection and Immunity, University College London, London, United Kingdom

   Contribution

   Investigation

   Competing interests

   No competing interests declared

10. Ntombifuthi Mthabela

    Africa Health Research Institute, Durban, South Africa

    Contribution

    Investigation

    Competing interests

    No competing interests declared

11. Matilda Mazibuko

    Africa Health Research Institute, Durban, South Africa

    Contribution

    Resources

    Competing interests

    No competing interests declared

12. Daniel Muema

    1. Africa Health Research Institute, Durban, South Africa
    2. School of Laboratory Medicine and Medical Sciences, University of KwaZulu-Natal, Durban, South Africa

    Contribution

    Data curation

    Competing interests

    No competing interests declared

13. Dirhona Ramjit

    Africa Health Research Institute, Durban, South Africa

    Contribution

    Project administration

    Competing interests

    No competing interests declared

14. Thumbi Ndung'u

    1. Africa Health Research Institute, Durban, South Africa
    2. Division of Infection and Immunity, University College London, London, United Kingdom
    3. HIV Pathogenesis Programme, The Doris Duke Medical Research Institute, University of KwaZulu-Natal, Durban, South Africa
    4. Max Planck Institute for Infection Biology, Berlin, Germany

    Contribution

    Methodology

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0003-2962-3992

15. Willem Hanekom

    1. Africa Health Research Institute, Durban, South Africa
    2. Division of Infection and Immunity, University College London, London, United Kingdom

    Contribution

    Resources

    Competing interests

    No competing interests declared

16. Bernadett Gosnell

    Department of Infectious Diseases, Nelson R. Mandela School of Clinical Medicine, University of KwaZulu-Natal, Durban, South Africa

    Contribution

    Resources

    Competing interests

    No competing interests declared

17. COMMIT-KZN Team

    Contribution

    Writing - review and editing

    1. Moherndran Archary, Department of Paediatrics and Child Health, University of KwaZulu-Natal, Durban, South Africa
    2. Kaylesh J Dullabh, Department of Cardiothoracic Surgery, University of KwaZulu-Natal, Durban, South Africa
    3. Jennifer Giandhari, KwaZulu-Natal Research Innovation and Sequencing Platform, Durban, South Africa
    4. Philip Goulder, Africa Health Research Institute and Department of Paediatrics, University of Oxford, Oxford, United Kingdom
    5. Guy Harling, Africa Health Research Institute and the Institute for Global Health, University College London, London, United Kingdom
    6. Rohen Harrichandparsad, Department of Neurosurgery, University of KwaZulu-Natal, Durban, South Africa
    7. Kobus Herbst, Africa Health Research Institute and the South African Population Research Infrastructure Network, Durban, South Africa
    8. Prakash Jeena, Department of Paediatrics and Child Health, University of KwaZulu-Natal, Durban, South Africa
    9. Thandeka Khoza, Africa Health Research Institute, Durban, South Africa
    10. Nigel Klein, Africa Health Research Institute and the Institute of Child Health, University College London, London, United Kingdom
    11. Rajhmun Madansein, Department of Cardiothoracic Surgery, University of KwaZulu-Natal, Durban, South Africa
    12. Mohlopheni Marakalala, Africa Health Research Institute and Division of Infection and Immunity, University College London, London, United Kingdom
    13. Mosa Moshabela, College of Health Sciences, University of KwaZulu-Natal, Durban, South Africa
    14. Kogie Naidoo, Centre for the AIDS Programme of Research in South Africa, Durban, South Africa
    15. Zaza Ndhlovu, Africa Health Research Institute and the Ragon Institute of MGH, MIT and Harvard, Cambridge, United States
    16. Kennedy Nyamande, Department of Pulmonology and Critical Care, University of KwaZulu-Natal, Durban, South Africa
    17. Nesri Padayatchi, Centre for the AIDS Programme of Research in South Africa, Durban, South Africa
    18. Vinod Patel, Department of Neurology, University of KwaZulu-Natal, Durban, South Africa
    19. Theresa Smit, Africa Health Research Institute, Durban, South Africa
    20. Adrie Steyn, Africa Health Research Institute and Division of Infectious Diseases, University of Alabama at Birmingham, Birmingham, United States

18. Richard J Lessells

    1. School of Laboratory Medicine and Medical Sciences, University of KwaZulu-Natal, Durban, South Africa
    2. KwaZulu-Natal Research Innovation and Sequencing Platform, Durban, South Africa
    3. Centre for the AIDS Programme of Research in South Africa, Durban, South Africa

    Contribution

    Writing - review and editing

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0003-0926-710X

19. Emily B Wong

    1. Africa Health Research Institute, Durban, South Africa
    2. Division of Infectious Diseases, Department of Medicine, University of Alabama at Birmingham, Birmingham, United States

    Contribution

    Conceptualization

    Competing interests

    No competing interests declared

20. Tulio de Oliveira

    1. School of Laboratory Medicine and Medical Sciences, University of KwaZulu-Natal, Durban, South Africa
    2. KwaZulu-Natal Research Innovation and Sequencing Platform, Durban, South Africa
    3. Centre for the AIDS Programme of Research in South Africa, Durban, South Africa
    4. Centre for Epidemic Response and Innovation, School of Data Science and Computational Thinking, Stellenbosch University, Stellenbosch, South Africa
    5. Department of Global Health, University of Washington, Seattle, United States

    Contribution

    Resources

    Competing interests

    No competing interests declared

21. Mahomed-Yunus S Moosa

    Department of Infectious Diseases, Nelson R. Mandela School of Clinical Medicine, University of KwaZulu-Natal, Durban, South Africa

    Contribution

    Resources, Supervision

    Competing interests

    No competing interests declared

22. Gil Lustig

    Centre for the AIDS Programme of Research in South Africa, Durban, South Africa

    Contribution

    Formal analysis

    Competing interests

    No competing interests declared

23. Alasdair Leslie

    1. Africa Health Research Institute, Durban, South Africa
    2. School of Laboratory Medicine and Medical Sciences, University of KwaZulu-Natal, Durban, South Africa
    3. Division of Infection and Immunity, University College London, London, United Kingdom

    Contribution

    Formal analysis, Supervision

    For correspondence

    Al.Leslie@ahri.org

    Competing interests

    No competing interests declared

24. Henrik Kløverpris

    1. Africa Health Research Institute, Durban, South Africa
    2. School of Laboratory Medicine and Medical Sciences, University of KwaZulu-Natal, Durban, South Africa
    3. Division of Infection and Immunity, University College London, London, United Kingdom
    4. Department of Immunology and Microbiology, University of Copenhagen, Copenhagen, Denmark

    Contribution

    Formal analysis, Supervision, Investigation

    For correspondence

    Henrik.Kloverpris@ahri.org

    Competing interests

    No competing interests declared

25. Alex Sigal

    1. Africa Health Research Institute, Durban, South Africa
    2. School of Laboratory Medicine and Medical Sciences, University of KwaZulu-Natal, Durban, South Africa
    3. Max Planck Institute for Infection Biology, Berlin, Germany

    Contribution

    Conceptualization, Funding acquisition, Writing - review and editing

    For correspondence

    alex.sigal@ahri.org

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0001-8571-2004

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