Clinical outcomes and immunological response to SARS-CoV-2 infection among people living with HIV

Abstract

People living with HIV (PLWH) usually suffer from co-infections and co-morbidities including respiratory tract infections. SARS-CoV-2 has been reported to cause respiratory infections. There are uncertainties in the disease severity and immunological response among PLWH who are co-infected with COVID-19. This review outlines the current knowledge on the clinical outcomes and immunological response to SARS-CoV-2 among PLWH. Literature was searched in Google scholar, Scopus, PubMed, and Science Direct conforming with the Preferred Reporting Items for Systematic reviews and Meta-analyses (PRISMA) guidelines from studies published from January 2020 to June 2023. A total of 81 studies from 25 countries were identified, and RT-PCR was used in confirming COVID-19 in 80 of the studies. Fifty-seven studies assessed risk factors and clinical outcomes in HIV patients co-infected with COVID-19. Thirty-nine of the studies indicated the following factors being associated with severe outcomes in HIV/SARS-CoV-2: older age, the male sex, African American race, smoking, obesity, cardiovascular diseases, low CD4⁺ count, high viral load, tuberculosis, high levels of inflammatory markers, chronic kidney disease, hypertension, diabetes, interruption, and delayed initiation of ART. The severe outcomes are patients’ hospitalization, admission at intensive care unit, mechanical ventilation, and death. Twenty (20) studies, however, reported no difference in clinical presentation among co-infected compared to mono-infected individuals. Immune response to SARS-CoV-2 infection was investigated in 25 studies, with some of the studies reporting high levels of inflammatory markers, T cell exhaustion and lower positive conversion rate of IgG in PLWH. There is scanty information on the cytokines that predisposes to severity among HIV/SARS-CoV-2 co-infected individuals on combined ART. More research work should be carried out to validate co-infection-related cytokines and/or immune markers to SARS-CoV-2 among PLWH.

Impact statement

People living with HIV often experience co-infections and co-morbidities, including respiratory tract infections. SARS-CoV-2 which is known to cause severe respiratory tract infections, has been reported among PLWH. There are, however, conflicting reports on HIV patients co-infected with SARS-CoV-2 with scanty information on other human coronaviruses. Studies that reported on clinical outcomes and immunological responses were reviewed through search engines and PRISMA selection criteria, with most studies indicating similar risk factors that predisposes to disease severity. High levels of inflammatory markers, T cell exhaustion and lower positive conversion rate of IgG were identified in individuals co-infected with HIV/SARS-CoV-2. Research on cytokines and immune markers in HIV/SARS-CoV-2 co-infected individuals on combined ART is limited and therefore, necessitating further validation.

Introduction

People living with HIV (PLWH) usually suffer from co-infections and co-morbidities including respiratory tract infections, renal impairment, hypertension, diabetes, obesity, hyperlipidemia, chronic viral hepatitis, and non-AIDS-defining malignancies among others [1, 2]. These co-infections and co-morbidities tend to limit the efficacy of the antiretroviral therapy [3]. Respiratory tract infections are of a major concern due to the compromised immune state of PLWH that makes them vulnerable to severe diseases [4].

In 2019, the novel SARS-CoV-2, a new coronavirus broke out in China, also known as (COVID-19). As of September 2023, WHO reported 770,875,433 confirmed cases of COVID-19, and 6,959,316 deaths [5] spreading throughout the globe. SARS-CoV-2 has been reported to also cause more severe RTIs in HIV patients [6, 7]. Co-infections in humans have become a topic among researchers with wide interest to know their clinical importance [8, 9].

PLWH infected with COVID-19, are thought to have more complicated clinical presentations due to immunodeficiency and immune imbalance [6]. Research has reported COVID-19 in PLWH to be severe [10]. Other studies however, indicated similarity in prevalence and deleterious outcomes among both the co-infected and mono-infected [11, 12]. Bhaskaran and others reported an increased COVID-19 mortality and morbidity risk among PLWH [13], but other researchers were not convinced about this assertion and cautioned its authenticity [14].

T cell immune activation and some cytokines play a role in HIV progression [15]. COVID-19 infection has also been investigated to be associated with some immune profiles [16]. This usually leads to a cytokine storm where cytokines are then released to control inflammation causing more white blood cells to accumulate, creating a cycle of inflammation thereby damaging the lung cells. This indicates that co-infections of these HIV/SARS-CoV-2 conditions among humans may lead to harmful immunological response and a poor prognosis of disease.

This review paper sought to outline the current knowledge of clinical outcomes and immunological response to SARS-CoV-2 infection among PLWH. It also sought to identify gaps in relation to this coinfection study.

Materials and methods

Selection criteria

All studies reporting on clinical outcomes and immune response among PLWH co-infected with SARS-CoV-2 were included. All immunological studies with observational studies, cohort studies, case reports, randomized controlled trials, and case series were also included. All studies meeting the above stated criteria, published from January 2020 to June 2023 and in the English language were included. Studies that do not address clinical outcomes and immunological response among PLWH co-infected with COVID-19 were excluded from this review. Letters to editors, editorials, commentaries, and brief reports that did not report on any clinical data were excluded. Literature reviews, systematic review and meta-analysis data were excluded.

Data sources and search strategy

We searched in PubMed, Google scholar, Scopus, and Science Direct using relevant terms such as “SARS-CoV-2” or “COVID-19” and ‘HIV or “Human Immunodeficiency Syndrome” or AIDS or “Acquired Immunodeficiency Disease” or PLWH or “People Living With HIV.” We then applied extra filters to access articles on “Immunological Response” or “Immune Characterization” or “Immunological Profiles” or “T-Cell Activation and Cytokines Profiles” and “Outcomes.” Also, eligible studies were identified by scanning references by manual search.

Study selection

Titles were imported into Endnotes for every search, and duplicates were eliminated. Titles and abstracts were used by two researchers to independently check records for eligibility. The complete texts of any publications that were thought to be possibly eligible were then retrieved, evaluated, and unanimously chosen to be included in the study. Conflicts were arbitrated by a third investigator or resolved by consensus.

Data extraction and synthesis

Extracted data were imputed into a table. All data were in English language. Studies were curated by sampling date, study design, study place, study participants, assay type, additional tests, author, and year of publication.

Results

Studies selection was done using PRISMA guidelines (Figure 1). Databases searches (Google scholar: 17,500, Scopus: 559, ScienceDirect: 2,475, PubMed: 612) identified a total of 21,146. Eighty-three (81) studies met the eligibility criteria after the selection process (Figure 1). Endnote Software was used to remove duplicates. Also, studies that did not meet the eligibility criteria in the initial screening were 21,031. Fifty-five (55) studies were excluded due to the following reasons: No methods (4), only abstract (8), systematic review, literature review, meta-analysis (3), Brief report (1), editorial (6) and commentary (5). A manual scanning of references resulted in 22 additional reports. Eighty-one studies were included in this analysis.

FIGURE 1

Characteristics of included studies

Studies were identified in 25 countries in this review with United State of America contributing 17 of the included studies. Other countries where studies were carried out included South Africa (12), Italy (10), China (9), Spain (7), United Kingdom (5), France (3), Russia (2) and Brazil (2). Only one study was identified in the following countries (Korea, UAE, Iran, Germany, Japan, Guinea Bissau, Netherlands, Taiwan, Sweden, Israel, Belgium, Zambia, and Indonesia). Study participants included HIV patients, HIV naïve groups, COVID-19 patients. All studies were conducted among HIV patients. RT-PCR was used in confirming human coronaviruses in 99% of the studies. ELISA techniques were also used in 14 of the studies, followed by flow cytometry (n = 9), neutralization assay (n = 5), ELISpot (n = 4).

Fifty-seven studies have assessed clinical outcomes in HIV patients that were co-infected with SARS-CoV-2 (Table 1). Immune response to COVID-19 infection was investigated by 25 studies (Table 2). 18 studies were made up of brief reports, case reports and editorials with clinical and laboratory data. All the studies were carried out from 2020 to 2023.

Thirty (38) studies reported the following risk factors as associated with severity of diseases (Table 1). This includes older age, higher BMI, male sex, deprivation, ethnicity, obesity, smoking, Tuberculosis, chronic kidney disease, higher inflammatory markers, diabetes, cardiovascular disease, lung cancer, African American, high viral load, low CD4⁺ count, high neutrophil-lymphocyte ratio, discontinued ART usage and some ART regimen. Twenty studies however indicated that clinical presentations among the co-infected were the same as the general population therefore there was low risk of disease severity (Table 1).

Twenty-five studies looked at immunological responses (Table 2), out of which four suggested that high inflammatory markers and immune dysregulation are linked to severity of disease and death among people who are coinfected with HIV/SARS-CoV-2 and are on ART, even though the ART is supposed to help with HIV viral suppression and immune reconstitution [17–22]. HIV/SARS-CoV-2 individuals with higher pro-inflammatory markers such as C-reactive protein (CRP), IL-8, IL-6 presented with disease severity and higher mortality than those who recovered [17]. Three other studies on co-infections linked reduction of T cell numbers to increased IL-6, IL-8, and CRP levels, causing a cytokine storm [23–25]. Among the co-infected individuals, unsuppressed HIV hampers T cell cross-recognition and responses to SARS-CoV-2 infection, and thereby leading to severe outcomes [26, 27]. The pre-symptom and post recovery CD4⁺, and CD8⁺ counts showed no significant difference between PLWH and HIV negative individuals who are infected with SARS-CoV-2 [28]. PLWH saw a brief decline in CD4⁺, and CD8⁺ counts during the acute phase of COVID-19 with the CD4+/CD8+ ratio remaining unchanged [11, 28].

Most of the studies were either retrospective or prospective with one time point sample collection, therefore, no subsequent CD4⁺ counts and viral loads to determine relationship with clinical outcomes. Two of the studies were longitudinal with one study investigating two waves of SARS-CoV-2 infection [26] and the other following up for a period of 3 months on HIV/SARS-CoV-2 patients [12]. Snyman et al., indicated in their study that anti-SARS-CoV-2 IgM, IgG, and IgA levels in non-HIV individuals and PLWH on full HIV suppression on ART have similar seroconversion rates [12]. The conversion rate of anti-SARS-CoV-2 IgG was lower and quickly lost in PLWH as compared to HIV negative persons who are SARS-CoV-2 positive [29–31]. Three of the studies indicated that slower generation of anti SARS CoV2 antibodies were attributed to increased COVID-19 severity among PLWH [32–34].

Discussion

We conducted a scoping review to assess specific COVID-19 clinical outcomes and immune response in patients with human immunodeficiency virus (PLWH) and identify gaps. Hospitalisation risk, intensive care unit admission, mechanical ventilation and mortality were the four categories identified as clinical outcomes. Our review showed varied reports on risk of hospitalisation, ICU admission, mechanical ventilation and mortality in cohort studies, case series, and case reports. PLWH who died exhibited higher levels of soluble immune activation and inflammation markers, which are linked to disease severity in COVID-19 [22]. Individuals with non-suppressed HIV viremia have reported lower levels of antibodies against SARS-CoV-2 in their humoral response [35]. Some studies however, associated low risk of hospitalization and death to Tenofovir usage as compared to those on other regimen [35–37].

Immune response to SARS-CoV-2 infection among PLWH on ART

ART does not eradicate HIV completely but significantly reduces morbidity and mortality associated with the virus [38]. ART may also reduce the severity of COVID-19 through immunological reconstitution, although these effects have not yet been confirmed [10, 36, 39]. PLWH with mild COVID-19 presentation, in the presence of high proinflammatory markers, suggested that certain antiretroviral drugs were protective against severity of COVID-19 disease [20]. A study in Russia among 376 HIV/COVID-19 patients (171 without ART and 205 with ART) suggested that elevated anti-inflammatory markers such as IL-10 and TGFβ, reduced CD4+/CD8+ cell ratios led to an increase in exhausted T cells in ART naïve patients. This led to Adverse Respiratory Distress Syndrome among the ART naïve group [32]. Sharov also reiterated that in the presence of uninterrupted ART, HIV patients do not progress to severe SARS-CoV-2 infection [32]. Other studies hypothesized that specific ART (NRTIs, NNRTIs and PI) predisposes to severe COVID-19 but no conclusive findings have been made because of studies involving smaller sample size and inconsistent cases and reports [40, 41].

Signaling pathway of HIV/SARS-CoV-2 coinfection

Viral infections interact mainly with the activated Signal Transducer and Activators of Transcription 1, 2, and 3 (STAT1, STAT2 and STAT3) to release pro-inflammatory cytokines to eliminate viruses [42]. The IL-6-JAK-STAT3 axis is significantly linked to the onset of severe COVID-19 [43, 44]. The dimerized epidermal growth factor receptor (EGFR) can tyrosine-phosphorylate STAT3, which is elevated in cases of acute lung injury [45] and in cases where STAT1 is lacking [46, 47]. As a result, in COVID-19, EGFR signalling may develop into a different pathway that stimulates STAT3 when lung damage occurs, and SARS-CoV-2 infection significantly reduces IFN-I production [48]. This aberrant transcriptional rewiring towards STAT3 may lead to the symptoms most typically reported in hospitalised COVID-19 patients: fast coagulopathy/thrombosis, proinflammatory conditions, profibrotic state, and T cell lymphopenia [49].

Some HIV proteins have been reported to inhibit effective IFNα signalling by degrading certain components of the JAK/STAT signalling pathway like STAT1 and STAT3 [50]. The impaired JAK/STAT signalling pathway is however restored in the presence of uninterrupted combined Antiretroviral therapy (cART) for more than 6 months [51]. Per our search, we found one study available on HIV/COVID-19 signalling pathway that investigated STAT3 but did not look at other STAT pathways [52], and therefore creates a gap that needs to be researched. Understanding the viral co-infection, immune response, and signalling pathway dynamics will help identify particulate markers that predisposes to severity of disease.

Oxidative stress responses among HIV/SARS-CoV-2 coinfection

Hyperactivation of STAT3 affect various biological and physiological functions, leading to oxidative stress (OxS) and poor prognosis of disease [22]. Oxidative stress (OxS) comes about by accumulating reactive oxygen and nitrogen species, which are free radicals that causes injury to organs. Under physiological conditions, these OxS are wiped out by antioxidants especially glutathione (GSH) [53]. Glutathione are endogenous intracellular antioxidants that neutralizes free radical released due to oxidative stress [54]. Deficiency in GSH however, leads to high levels of OxS due to compromised antioxidant defences [55]. Oxidative stress has been studied in HIV or SARS-CoV 2 alone with higher levels reported in each disease [55–58]. There is however scanty information on oxidative stress among HIV/COVID-19 patients, hence the need to investigate if the presence of ART usage affects oxidative stress response.

Limitations

There is lack of information on cellular immunity in other hCoVs apart from COVID-19 co-infection. Cytokine have been studied extensively in HIV or COVID-19 alone but not as a co-infection. The oxidative stress levels among HIV/SARS-CoV-2 co-infection are yet to be studied although research has been done for other co-morbidities or co-infections.

Conclusion

This study highlights the paucity of clinical and immunological data on HIV/SARS-CoV-2 co-infection in sub-Saharan Africa, even though this region has the highest HIV prevalence. Review shows conflicting reports on severity of the co-infection. HIV/SARS-CoV-2 severity and outcomes appear to be worse, when coexisting age-related comorbidities and CD4 + T-cell depletion is present. Discontinued or no evidence of ART usage have also been shown to increase disease severity, which needs to be studied further to ascertain its authenticity.

CD4⁺ T cell lymphopenia in both diseases is influenced by various mechanisms including direct attacks, immune activation, and redistribution of CD4⁺ T cells. Cytokines investigation will help identify markers that are implicated in disease severity among HIV/SARS-CoV-2 patients. Further investigation is needed to confirm co-infection-associated cytokines and/or immunological markers to SARS-CoV-2 in PLWH.

References

• 1

  Schouten J Wit FW Stolte IG Kootstra NA van der Valk M Geerlings SE et al Cross-sectional comparison of the prevalence of age-associated comorbidities and their risk factors between HIV-infected and uninfected individuals: the AGEhIV cohort study. Clin Infect Dis (2014) 59(12):1787–97. 10.1093/cid/ciu701

  • CrossRef
  • Google Scholar

• 2

  Önen NF Overton ET Seyfried W Stumm ER Snell M Mondy K et al Aging and HIV infection: a comparison between older HIV-infected persons and the general population. HIV Clin trials (2010) 11(2):100–9. 10.1310/hct1102-100

  • CrossRef
  • Google Scholar

• 3

  Brown TT Guaraldi G . Multimorbidity and burden of disease. Interdiscip Top Gerontol Geriatr (2017) 42:59–73. 10.1159/000448544

  • CrossRef
  • Google Scholar

• 4

  Kanwugu ON Adadi P . HIV/SARS‐CoV‐2 coinfection: a global perspective. J Med Virol (2021) 93(2):726–32. 10.1002/jmv.26321

  • CrossRef
  • Google Scholar

• 5

  WHO. COVID-19 weekly epidemiological update. 134 edn (2023).

  • Google Scholar

• 6

  Vizcarra P Pérez-Elías MJ Quereda C Moreno A Vivancos MJ Dronda F et al Description of COVID-19 in HIV-infected individuals: a single-centre, prospective cohort. The lancet HIV (2020) 7(8):e554–e564. 10.1016/s2352-3018(20)30164-8

  • CrossRef
  • Google Scholar

• 7

  Collins LF Moran CA Oliver NT Moanna A Lahiri CD Colasanti JA et al Clinical characteristics, comorbidities and outcomes among persons with HIV hospitalized with coronavirus disease 2019 in Atlanta, Georgia. AIDS (London, England) (2020) 34(12):1789–94. 10.1097/qad.0000000000002632

  • CrossRef
  • Google Scholar

• 8

  Calza L Bon I Tadolini M Borderi M Colangeli V Badia L et al COVID-19 in patients with HIV-1 infection: a single-centre experience in northern Italy. Infection (2021) 49(2):333–7. 10.1007/s15010-020-01492-7

  • CrossRef
  • Google Scholar

• 9

  Hartley DM Perencevich EN . Public health interventions for COVID-19: emerging evidence and implications for an evolving public health crisis. Jama (2020) 323(19):1908–9. 10.1001/jama.2020.5910

  • CrossRef
  • Google Scholar

• 10

  Del Amo J Polo R Moreno S Díaz A Martínez E Arribas JR et al Antiretrovirals and risk of COVID-19 diagnosis and hospitalization in HIV-positive persons. Epidemiology (Cambridge, Mass.) (2020) 31(6):e49–e51. 10.1097/ede.0000000000001235

  • CrossRef
  • Google Scholar

• 11

  Sigel K Swartz T Golden E Paranjpe I Somani S Richter F et al Coronavirus 2019 and people living with human immunodeficiency virus: outcomes for hospitalized patients in New York City. Clin Infect Dis (2020) 71(11):2933–8. 10.1093/cid/ciaa880

  • CrossRef
  • Google Scholar

• 12

  Snyman J Hwa SH Krause R Muema D Reddy T Ganga Y et al Similar antibody responses against severe acute respiratory syndrome coronavirus 2 in individuals living without and with human immunodeficiency virus on antiretroviral therapy during the first South African infection wave. Clin Infect Dis (2022) 75(1):e249–e256. 10.1093/cid/ciab758

  • CrossRef
  • Google Scholar

• 13

  Bhaskaran K Rentsch CT MacKenna B Schultze A Mehrkar A Bates CJ et al HIV infection and COVID-19 death: a population-based cohort analysis of UK primary care data and linked national death registrations within the OpenSAFELY platform. The lancet HIV (2021) 8(1):e24–e32. 10.1016/s2352-3018(20)30305-2

  • CrossRef
  • Google Scholar

• 14

  Waters LJ Pozniak AL . COVID-19 death in people with HIV: interpret cautiously. The Lancet HIV (2021) 8(1):e2–e3. 10.1016/s2352-3018(20)30332-5

  • CrossRef
  • Google Scholar

• 15

  Scagnolari C Antonelli G . Type I interferon and HIV: subtle balance between antiviral activity, immunopathogenesis and the microbiome. Cytokine Growth Factor Rev (2018) 40:19–31. 10.1016/j.cytogfr.2018.03.003

  • CrossRef
  • Google Scholar

• 16

  Zhou Z Ren L Zhang L Zhong J Xiao Y Jia Z et al Heightened innate immune responses in the respiratory tract of COVID-19 patients. Cell host & microbe (2020) 27(6):883–90. 10.1016/j.chom.2020.04.017

  • CrossRef
  • Google Scholar

• 17

  Ho H-e. Peluso MJ Margus C Matias Lopes JP He C Gaisa MM et al Clinical outcomes and immunologic characteristics of coronavirus disease 2019 in people with human immunodeficiency virus. J Infect Dis (2021) 223(3):403–8. 10.1093/infdis/jiaa380

  • CrossRef
  • Google Scholar

• 18

  Álvarez H Ruiz-Mateos E Juiz-González PM Vitallé J Viéitez I Vázquez-Friol MC et al SARS-CoV-2 evolution and spike-specific CD4+ T-cell response in persistent COVID-19 with severe HIV immune suppression. Microorganisms (2022) 10(1):143. 10.3390/microorganisms10010143

  • CrossRef
  • Google Scholar

• 19

  d’Ettorre G Recchia G Ridolfi M Siccardi G Pinacchio C Innocenti GP et al Analysis of type I IFN response and T cell activation in severe COVID-19/HIV-1 coinfection: a case report. Medicine (2020) 99(36):e21803. 10.1097/md.0000000000021803

  • CrossRef
  • Google Scholar

• 20

  Mondi A Cimini E Colavita F Cicalini S Pinnetti C Matusali G et al COVID‐19 in people living with HIV: clinical implications of dynamics of the immune response to SARS‐CoV‐2. J Med Virol (2021) 93(3):1796–804. 10.1002/jmv.26556

  • CrossRef
  • Google Scholar

• 21

  Riou C du Bruyn E Stek C Daroowala R Goliath RT Abrahams F et al Relationship of SARS-CoV-2-specific CD4 response to COVID-19 severity and impact of HIV-1 and tuberculosis coinfection. J Clin Invest (2021) 131(12):e149125. 10.1172/jci149125

  • CrossRef
  • Google Scholar

• 22

  Ruan Q Yang K Wang W Jiang L Song J . Clinical predictors of mortality due to COVID-19 based on an analysis of data of 150 patients from Wuhan, China. Intensive Care Med (2020) 46(5):846–8. 10.1007/s00134-020-05991-x

  • CrossRef
  • Google Scholar

• 23

  Sales TLS Souza-Silva MVR Delfino-Pereira P Neves JVB Sacioto MF Assis VC et al COVID-19 outcomes in people living with HIV: peering through the waves. Clinics (2023) 78:100223. 10.1016/j.clinsp.2023.100223

  • CrossRef
  • Google Scholar

• 24

  Vergori A Boschini A Notari S Lorenzini P Castilletti C Colavita F et al SARS-CoV-2 specific immune response and inflammatory profile in advanced HIV-infected persons during a COVID-19 outbreak. Viruses (2022) 14(7):1575. 10.3390/v14071575

  • CrossRef
  • Google Scholar

• 25

  Alrubayyi A Gea-Mallorquí E Touizer E Hameiri-Bowen D Kopycinski J Charlton B et al Characterization of humoral and SARS-CoV-2 specific T cell responses in people living with HIV. Nat Commun (2021) 12(1):5839. 10.1038/s41467-021-26137-7

  • CrossRef
  • Google Scholar

• 26

  Nkosi T Ndhlovu ZM Chasara C Papadopoulos AO Nguni TL Karim F et al Unsuppressed HIV infection impairs T cell responses to SARS-CoV-2 infection and abrogates T cell cross-recognition. Elife (2022) 11:e78374. 10.7554/elife.78374

  • CrossRef
  • Google Scholar

• 27

  Krause R Snyman J Shi-Hsia H Muema D Karim F Ganga Y et al HIV skews the SARS-CoV-2 B cell response towards an extrafollicular maturation pathway. Elife (2022) 11:e79924. 10.7554/eLife.79924

  • CrossRef
  • Google Scholar

• 28

  Adachi E Saito M Nagai H Ikeuchi K Koga M Tsutsumi T et al Transient depletion of T cells during COVID‐19 and seasonal influenza in people living with HIV. J Med Virol (2022) 94(5):1789–91. 10.1002/jmv.27543

  • CrossRef
  • Google Scholar

• 29

  Garshasbi S Bokharaei-Salim F Khanaliha K Kiani SJ Kalantari S Jamshidi Makiani M et al SARS-CoV-2 infection in Iranian people living with human immunodeficiency virus-1 infection. Jundishapur J Microbiol (2022) 15(1). 10.5812/jjm.121929

  • CrossRef
  • Google Scholar

• 30

  Liu Y Xiao Y Wu S Marley G Ming F Wang X et al People living with HIV easily lose their immune response to SARS-CoV-2: result from a cohort of COVID-19 cases in Wuhan, China. BMC Infect Dis (2021) 21(1):1029–7. 10.1186/s12879-021-06723-2

  • CrossRef
  • Google Scholar

• 31

  Wang M Luo L Bu H Xia H . One case of coronavirus disease 2019 (COVID-19) in a patient co-infected by HIV with a low CD4+ T-cell count. Int J Infect Dis (2020) 96:148–50. 10.1016/j.ijid.2020.04.060

  • CrossRef
  • Google Scholar

• 32

  Sharov KS . HIV/SARS-CoV-2 co-infection: T cell profile, cytokine dynamics and role of exhausted lymphocytes. Int J Infect Dis (2021) 102:163–9. 10.1016/j.ijid.2020.10.049

  • CrossRef
  • Google Scholar

• 33

  Ngalamika O Lidenge SJ Mukasine MC Kawimbe M Kamanzi P Ngowi JR et al SARS-CoV-2-specific T cell and humoral immunity in individuals with and without HIV in an African population: a prospective cohort study. Int J Infect Dis (2023) 127:106–15. 10.1016/j.ijid.2022.12.009

  • CrossRef
  • Google Scholar

• 34

  Schuster DJ Karuna S Brackett C Wesley M Li SS Eisel N et al Lower SARS-CoV-2–specific humoral immunity in people living with HIV-1 recovered from nonhospitalized COVID-19. JCI insight (2022) 7(21):e158402. 10.1172/jci.insight.158402

  • CrossRef
  • Google Scholar

• 35

  Huang J Xie N Hu X Yan H Ding J Liu P et al Epidemiological, virological and serological features of coronavirus disease 2019 (COVID-19) cases in people living with human immunodeficiency virus in Wuhan: a population-based cohort study. Clin Infect Dis (2021) 73(7):e2086–e2094. 10.1093/cid/ciaa1186

  • CrossRef
  • Google Scholar

• 36

  Lea AN Leyden WA Sofrygin O Marafino BJ Skarbinski J Napravnik S et al Human immunodeficiency virus status, Tenofovir exposure, and the risk of poor coronavirus disease 19 outcomes: real-world analysis from 6 United States cohorts before vaccine rollout. Clin Infect Dis (2023) 76(10):1727–34. 10.1093/cid/ciad084

  • CrossRef
  • Google Scholar

• 37

  Del Amo J Polo R Moreno S Jarrín I Hernán MA . SARS-CoV-2 infection and coronavirus disease 2019 severity in persons with HIV on antiretroviral treatment. Aids (2022) 36(2):161–8. 10.1097/qad.0000000000003132

  • CrossRef
  • Google Scholar

• 38

  Lohse N Obel N . Update of survival for persons with HIV infection in Denmark. Ann Intern Med (2016) 165(10):749–50. 10.7326/l16-0091

  • CrossRef
  • Google Scholar

• 39

  Suwanwongse K Shabarek N . Clinical features and outcome of HIV/SARS‐CoV‐2 coinfected patients in the Bronx, New York city. J Med Virol (2020) 92(11):2387–9. 10.1002/jmv.26077

  • CrossRef
  • Google Scholar

• 40

  Costenaro P Minotti C Barbieri E Giaquinto C Donà D . SARS‐CoV‐2 infection in people living with HIV: a systematic review. Rev Med Virol (2021) 31(1):1–12. 10.1002/rmv.2155

  • CrossRef
  • Google Scholar

• 41

  Mirzaei H McFarland W Karamouzian M Sharifi H . COVID-19 among people living with HIV: a systematic review. AIDS Behav (2021) 25:85–92. 10.1007/s10461-020-02983-2

  • CrossRef
  • Google Scholar

• 42

  Luo Y Alexander M Gadina M O’Shea JJ Meylan F Schwartz DM . JAK-STAT signaling in human disease: from genetic syndromes to clinical inhibition. J Allergy Clin Immunol (2021) 148(4):911–25. 10.1016/j.jaci.2021.08.004

  • CrossRef
  • Google Scholar

• 43

  Giamarellos-Bourboulis EJ Netea MG Rovina N Akinosoglou K Antoniadou A Antonakos N et al Complex immune dysregulation in COVID-19 patients with severe respiratory failure. Cell host & microbe (2020) 27(6):992–1000. 10.1016/j.chom.2020.04.009

  • CrossRef
  • Google Scholar

• 44

  Hirano T Murakami M . COVID-19: a new virus, but a familiar receptor and cytokine release syndrome. Immunity (2020) 52(5):731–3. 10.1016/j.immuni.2020.04.003

  • CrossRef
  • Google Scholar

• 45

  Finigan JH Downey GP Kern JA . Human epidermal growth factor receptor signaling in acute lung injury. Am J Respir Cel Mol Biol (2012) 47(4):395–404. 10.1165/rcmb.2012-0100tr

  • CrossRef
  • Google Scholar

• 46

  Venkataraman T Coleman CM Frieman MB . Overactive epidermal growth factor receptor signaling leads to increased fibrosis after severe acute respiratory syndrome coronavirus infection. J Virol (2017) 91(12):e00182-17. 10.1128/jvi.00182-17

  • CrossRef
  • Google Scholar

• 47

  Yang L Xu J Guo L Guo T Zhang L Feng L et al Porcine epidemic diarrhea virus-induced epidermal growth factor receptor activation impairs the antiviral activity of type I interferon. J Virol (2018) 92(8):e02095-17. 10.1128/jvi.02095-17

  • CrossRef
  • Google Scholar

• 48

  Hadjadj J Yatim N Barnabei L Corneau A Boussier J Smith N et al Impaired type I interferon activity and inflammatory responses in severe COVID-19 patients. Science (2020) 369(6504):718–24. 10.1126/science.abc6027

  • CrossRef
  • Google Scholar

• 49

  Matsuyama T Kubli SP Yoshinaga SK Pfeffer K Mak TW . An aberrant STAT pathway is central to COVID-19. Cel Death Differ (2020) 27(12):3209–25. 10.1038/s41418-020-00633-7

  • CrossRef
  • Google Scholar

• 50

  Gargan S Ahmed S Mahony R Bannan C Napoletano S O'Farrelly C et al HIV-1 promotes the degradation of components of the type 1 IFN JAK/STAT pathway and blocks anti-viral ISG induction. EBioMedicine (2018) 30:203–16. 10.1016/j.ebiom.2018.03.006

  • CrossRef
  • Google Scholar

• 51

  Liu M-Q Zhao M Kong WH Tang L Wang F Zhu ZR et al Combination antiretroviral therapy (cART) restores HIV-1 infection-mediated impairment of JAK-STAT signaling pathway. Oncotarget (2017) 8(14):22524–33. 10.18632/oncotarget.15121

  • CrossRef
  • Google Scholar

• 52

  Vanetti C Trabattoni D Stracuzzi M Amendola A Fappani C Rubinacci V et al Immunological characterization of HIV and SARS-CoV-2 coinfected young individuals. Cells (2021) 10(11):3187. 10.3390/cells10113187

  • CrossRef
  • Google Scholar

• 53

  Ballatori N Krance SM Notenboom S Shi S Tieu K Hammond CL . Glutathione dysregulation and the etiology and progression of human diseases. bchm (2009) 390:191–214. 10.1515/bc.2009.033

  • CrossRef
  • Google Scholar

• 54

  Yan Y Yang Y Wang F Ren H Zhang S Shi X et al Clinical characteristics and outcomes of patients with severe covid-19 with diabetes. BMJ Open Diabetes Res Care (2020) 8(1):e001343. 10.1136/bmjdrc-2020-001343

  • CrossRef
  • Google Scholar

• 55

  Kumar P Osahon O Vides DB Hanania N Minard CG Sekhar RV . Severe glutathione deficiency, oxidative stress and oxidant damage in adults hospitalized with COVID-19: implications for GlyNAC (glycine and N-acetylcysteine) supplementation. Antioxidants (2021) 11(1):50. 10.3390/antiox11010050

  • CrossRef
  • Google Scholar

• 56

  Pace GW Leaf CD . The role of oxidative stress in HIV disease. Free Radic Biol Med (1995) 19(4):523–8. 10.1016/0891-5849(95)00047-2

  • CrossRef
  • Google Scholar

• 57

  Repetto M Reides C Gomez Carretero ML Costa M Griemberg G Llesuy S . Oxidative stress in blood of HIV infected patients. Clinica Chim Acta (1996) 255(2):107–17. 10.1016/0009-8981(96)06394-2

  • CrossRef
  • Google Scholar

• 58

  Ntyonga-Pono M-P . COVID-19 infection and oxidative stress: an under-explored approach for prevention and treatment?Pan Afr Med J (2020) 35(2):12. 10.11604/pamj.2020.35.2.22877

  • CrossRef
  • Google Scholar

• 59

  Sasset L Di Meco E Cavinato S Cattelan AM . Coinfection of severe acute respiratory syndrome coronavirus 2 and HIV in a teaching hospital: still much to learn. AIDS (2020) 34(11):1694–6. 10.1097/qad.0000000000002609

  • CrossRef
  • Google Scholar

• 60

  Tesoriero JM Swain CAE Pierce JL Zamboni L Wu M Holtgrave DR et al COVID-19 outcomes among persons living with or without diagnosed HIV infection in New York State. JAMA Netw open (2021) 4(2):e2037069. 10.1001/jamanetworkopen.2020.37069

  • CrossRef
  • Google Scholar

• 61

  Dandachi D Geiger G Montgomery MW Karmen-Tuohy S Golzy M Antar AAR et al Characteristics, comorbidities, and outcomes in a multicenter registry of patients with human immunodeficiency virus and coronavirus disease 2019. Clin Infect Dis (2021) 73(7):e1964–e1972. 10.1093/cid/ciaa1339

  • CrossRef
  • Google Scholar

• 62

  Gervasoni C Meraviglia P Riva A Giacomelli A Oreni L Minisci D et al Clinical features and outcomes of patients with human immunodeficiency virus with COVID-19. Clin Infect Dis (2020) 71(16):2276–8. 10.1093/cid/ciaa579

  • CrossRef
  • Google Scholar

• 63

  Hu Y Ma J Huang H Vermund SH . Coinfection with HIV and SARS-CoV-2 in Wuhan, China: a 12-person case series. J acquired immune deficiency syndromes (2020) 85(1):1–5. 10.1097/QAI.0000000000002424

  • CrossRef
  • Google Scholar

• 64

  Stoeckle K Johnston CD Jannat-Khah DP Williams SC Ellman TM Vogler MA et al COVID-19 in hospitalized adults with HIV. Open Forum Infect Dis (2020) 7:ofaa327. Oxford University Press US. 10.1093/ofid/ofaa327

  • CrossRef
  • Google Scholar

• 65

  Madge S Barber TJ Hunter A Bhagani S Lipman M Burns F . Descriptive account of 18 adults with known HIV infection hospitalised with SARS-CoV-2 infection. Sex Transm Infections (2021) 97(5):392–3. 10.1136/sextrans-2020-054660

  • CrossRef
  • Google Scholar

• 66

  Mitha M Maharaj A Nyamande K . People living with HIV and COVID-19: a report on 2 clinical cases from South Africa. Afr J Thorac Crit Care Med (2020) 26(2):59–60. 10.7196/ajtccm.2020.v26i2.078

  • CrossRef
  • Google Scholar

• 67

  Calza L Bon I Borderi M Colangeli V Borioni A Re MC et al COVID-19 outcomes in patients with uncontrolled HIV-1 infection. JAIDS J Acquired Immune Deficiency Syndromes (2021) 86(1):e15–e17. 10.1097/qai.0000000000002537

  • CrossRef
  • Google Scholar

• 68

  Qasim A Mansour M Kousa O Awad D Abuhazeem B Millner P et al A case of coronavirus disease 2019 in acquired immunodeficiency syndrome patient: a case report and review of the literature. Intractable Rare Dis Res (2020) 9(4):256–9. 10.5582/irdr.2020.03081

  • CrossRef
  • Google Scholar

• 69

  Gudipati S Brar I Murray S McKinnon JE Yared N Markowitz N . Descriptive analysis of patients living with HIV affected by COVID-19. JAIDS J Acquired Immune Deficiency Syndromes (2020) 85(2):123–6. 10.1097/qai.0000000000002450

  • CrossRef
  • Google Scholar

• 70

  Isernia V Julia Z Le Gac S Bachelard A Landman R Lariven S et al SARS-COV2 infection in 30 HIV-infected patients followed-up in a French University Hospital. Int J Infect Dis (2020) 101:49–51. 10.1016/j.ijid.2020.09.1436

  • CrossRef
  • Google Scholar

• 71

  Zhang J-C Yu XH Ding XH Ma HY Cai XQ Kang SC et al New HIV diagnoses in patients with COVID-19: two case reports and a brief literature review. BMC Infect Dis (2020) 20(1):771–10. 10.1186/s12879-020-05480-y

  • CrossRef
  • Google Scholar

• 72

  Karmen-Tuohy S Carlucci PM Zervou FN Zacharioudakis IM Rebick G Klein E et al Outcomes among HIV-positive patients hospitalized with COVID-19. JAIDS J Acquired Immune Deficiency Syndromes (2020) 85:6–10. 10.1097/qai.0000000000002423

  • CrossRef
  • Google Scholar

• 73

  Härter G Spinner CD Roider J Bickel M Krznaric I Grunwald S et al COVID-19 in people living with human immunodeficiency virus: a case series of 33 patients. Infection (2020) 48:681–6. 10.1007/s15010-020-01438-z

  • CrossRef
  • Google Scholar

• 74

  Blanco JL Ambrosioni J Garcia F Martínez E Soriano A Mallolas J et al COVID-19 in patients with HIV: clinical case series. The lancet HIV (2020) 7(5):e314–e316. 10.1016/s2352-3018(20)30111-9

  • CrossRef
  • Google Scholar

• 75

  Shalev N Scherer M LaSota ED Antoniou P Yin MT Zucker J et al Clinical characteristics and outcomes in people living with human immunodeficiency virus hospitalized for coronavirus disease 2019. Clin Infect Dis (2020) 71(16):2294–7. 10.1093/cid/ciaa635

  • CrossRef
  • Google Scholar

• 76

  Bachelard A Sautereau A Digumber M Isernia V Phung B Lehur AC et al Risk factors associated with severe/critical COVID-19 in people living with HIV-1. Int J Infect Dis (2022) 122:152–4. 10.1016/j.ijid.2022.05.055

  • CrossRef
  • Google Scholar

• 77

  Gagliardini R Vergori A Lorenzini P Cicalini S Pinnetti C Mazzotta V et al Characteristics and outcomes of COVID-19-related hospitalization among PLWH. J Clin Med (2022) 11(6):1546. 10.3390/jcm11061546

  • CrossRef
  • Google Scholar

• 78

  Kim J-Y Kim JM Peck KR . The first case of an HIV patient diagnosed with COVID-19 in Korea. J Korean Med Sci (2020) 35(39):e358. 10.3346/jkms.2020.35.e358

  • CrossRef
  • Google Scholar

• 79

  Cipolat MM Sprinz E . COVID-19 pneumonia in an HIV-positive woman on antiretroviral therapy and undetectable viral load in Porto Alegre, Brazil. Braz J Infect Dis (2020) 24:455–7. 10.1016/j.bjid.2020.07.009

  • CrossRef
  • Google Scholar

• 80

  Davies M-A . HIV and risk of COVID-19 death: a population cohort study from the Western Cape Province, South Africa. MedRxiv (2020). Available from: https://doi.org/10.1101/2020.07.02.20145185.

  • Google Scholar

• 81

  Du Bruyn E Stek C Daroowala R Said-Hartley Q Hsiao M Schafer G et al Effects of tuberculosis and/or HIV-1 infection on COVID-19 presentation and immune response in Africa. Nat Commun (2023) 14(1):188. 10.1038/s41467-022-35689-1

  • CrossRef
  • Google Scholar

• 82

  Dutschke A Wejse C Nanque J Medina C Hønge B Jespersen S et al SARS-CoV-2 seroprevalence among people living with HIV in Guinea–Bissau. Public Health (2022) 209:36–8. 10.1016/j.puhe.2022.05.017

  • CrossRef
  • Google Scholar

• 83

  Etienne N Karmochkine M Slama L Pavie J Batisse D Usubillaga R et al HIV infection and COVID-19: risk factors for severe disease. AIDS (London, England) (2020) 34(12):1771–4. 10.1097/qad.0000000000002651

  • CrossRef
  • Google Scholar

• 84

  Geretti AM Stockdale AJ Kelly SH Cevik M Collins S Waters L et al Outcomes of COVID-19 related hospitalisation among people with HIV in the ISARIC WHO Clinical Characterisation Protocol UK Protocol: prospective observational study. MedRxiv (2020). Available from: https://doi.org/10.1101/2020.08.07.20170449.

  • Google Scholar

• 85

  Guo W Ming F Dong Y Zhang Q Zhang X Mo P et al A survey for COVID-19 among HIV/AIDS patients in two districts of Wuhan, China (2020). Available from: http://dx.doi.org/10.2139/ssrn.3550029.

  • Google Scholar

• 86

  Hadi YB Naqvi SF Kupec JT Sarwari AR . Characteristics and outcomes of COVID-19 in patients with HIV: a multicentre research network study. AIDS (London, England) (2020) 34(13):F3–F8. 10.1097/qad.0000000000002666

  • CrossRef
  • Google Scholar

• 87

  Kaboré OD Poda A Ouattara CA Michodigni FN Belem AA Sawadogo Y et al Seroprevalence of SARS-CoV-2 IgG and associated factors among people living with HIV over the first 12 months following the outbreak of COVID-19 in Burkina Faso, a sub-Saharan African country. Plos one (2023) 18(6):e0286665. 10.1371/journal.pone.0286665

  • CrossRef
  • Google Scholar

• 88

  Karim F Gazy I Cele S Zungu Y Krause R Bernstein M et al HIV status alters disease severity and immune cell responses in Beta variant SARS-CoV-2 infection wave. Elife (2021) 10:e67397. 10.7554/eLife.67397

  • CrossRef
  • Google Scholar

• 89

  Kassanjee R Davies M Ngwenya O Osei‐Yeboah R Jacobs T Morden E et al COVID‐19 among adults living with HIV: correlates of mortality among public sector healthcare users in Western Cape, South Africa. J Int AIDS Soc (2023) 26(6):e26104. 10.1002/jia2.26104

  • CrossRef
  • Google Scholar

• 90

  Ketels T Gisolf J Claassen M Swanink C van Lochem E Moonen L et al Short communication: prolonged COVID-19 infection in a patient with newly diagnosed HIV/AIDS. AIDS Res Hum retroviruses (2022) 38(5):399–400. 10.1089/aid.2021.0145

  • CrossRef
  • Google Scholar

• 91

  Maggiolo F Zoboli F Arosio M Valenti D Guarneri D Sangiorgio L et al SARS‐CoV‐2 infection in persons living with HIV: a single center prospective cohort. J Med Virol (2021) 93(2):1145–9. 10.1002/jmv.26352

  • CrossRef
  • Google Scholar

• 92

  Mahmood K Rashed ER Oliveros E Chau VQ Hermle T Jacobs S et al Predisposition or protection? COVID-19 in a patient on LVAD support with HIV/AIDS. JACC: Case Rep (2020) 2(9):1337–41. 10.1016/j.jaccas.2020.05.015

  • CrossRef
  • Google Scholar

• 93

  Möller IK Gisslén M Wagner P Sparén P Carlander C . COVID‐19 hospitalization outcomes in adults by HIV status; a nation‐wide register‐based study. HIV Med (2023) 24:1045–55. 10.1111/hiv.13515

  • CrossRef
  • Google Scholar

• 94

  Moreno-Torres V de Mendoza C Martínez-Urbistondo M Mills P Treviño A de la Fuente S et al Predictors of in-hospital mortality in HIV-infected patients with COVID-19. QJM: Int J Med (2023) 116(1):57–62. 10.1093/qjmed/hcac215

  • CrossRef
  • Google Scholar

• 95

  Nagarakanti SR Okoh AK Grinberg S Bishburg E . Clinical outcomes of patients with COVID‐19 and HIV coinfection. J Med Virol (2021) 93(3):1687–93. 10.1002/jmv.26533

  • CrossRef
  • Google Scholar

• 96

  Nasreddine R Florence E Moutschen M Yombi J Goffard J Derdelinckx I et al Clinical characteristics and outcomes of COVID‐19 in people living with HIV in Belgium: a multicenter, retrospective cohort. J Med Virol (2021) 93(5):2971–8. 10.1002/jmv.26828

  • CrossRef
  • Google Scholar

• 97

  Nomah DK Reyes-Urueña J Díaz Y Moreno S Aceiton J Bruguera A et al Sociodemographic, clinical, and immunological factors associated with SARS-CoV-2 diagnosis and severe COVID-19 outcomes in people living with HIV: a retrospective cohort study. The Lancet HIV (2021) 8(11):e701–e710. 10.1016/s2352-3018(21)00240-x

  • CrossRef
  • Google Scholar

• 98

  Peters JL Fall A Langerman SD El Asmar M Nakazawa M Mustapha A et al Prolonged severe acute respiratory syndrome coronavirus 2 Delta variant shedding in a patient with AIDS: case report and review of the literature. Open Forum Infect Dis (2022) 9:ofac479. Oxford University Press US. 10.1093/ofid/ofac479

  • CrossRef
  • Google Scholar

• 99

  Rosenthal EM Rosenberg ES Patterson W Ferguson WP Gonzalez C DeHovitz J et al Factors associated with SARS-CoV-2-related hospital outcomes among and between persons living with and without diagnosed HIV infection in New York State. PLoS One (2022) 17(5):e0268978. 10.1371/journal.pone.0268978

  • CrossRef
  • Google Scholar

• 100

  Sun J Patel RC Zheng Q Madhira V Olex AL Islam JY et al COVID-19 disease severity among people with HIV infection or solid organ transplant in the United States: a nationally-representative, multicenter, observational cohort study. Medrxiv (2021). Avaialble from: https://doi.org/10.1101/2021.07.26.21261028.

  • Google Scholar

• 101

  Tang ME Gaufin T Anson R Zhu W Mathews W Cachay ER . People with HIV have a higher risk of COVID‐19 diagnosis but similar outcomes to the general population. HIV Med (2022) 23(10):1069–77. 10.1111/hiv.13312

  • CrossRef
  • Google Scholar

• 102

  Yang Y Iwasaki A . Impact of chronic HIV infection on SARS-CoV-2 infection, COVID-19 disease and vaccines. Curr HIV/AIDS Rep (2022) 19:5–16. 10.1007/s11904-021-00590-x

  • CrossRef
  • Google Scholar

• 103

  Yunihastuti E Karjadi TH Widhani A Mahdi HIS Sundari S Hapsari AF et al Incidence and severity prediction score of COVID-19 in people living with HIV (SCOVHIV): experience from the first and second waves of the pandemic in Indonesia. AIDS Res Ther (2022) 19(1):47–8. 10.1186/s12981-022-00472-1

  • CrossRef
  • Google Scholar

• 104

  Zhu F Cao Y Xu S Zhou M . Co‐infection of SARS‐CoV‐2 and HIV in a patient in Wuhan city, China. J Med Virol (2020) 92:529–30. 10.1002/jmv.25732

  • CrossRef
  • Google Scholar

• 105

  Hoffmann C Casado JL Härter G Vizcarra P Moreno A Cattaneo D et al Immune deficiency is a risk factor for severe COVID‐19 in people living with HIV. HIV Med (2021) 22(5):372–8. 10.1111/hiv.13037

  • CrossRef
  • Google Scholar

• 106

  Venturas J Zamparini J Shaddock E Stacey S Murray L Richards GA et al Comparison of outcomes in HIV-positive and HIV-negative patients with COVID-19. J Infect (2021) 83(2):217–27. 10.1016/j.jinf.2021.05.020

  • CrossRef
  • Google Scholar

• 107

  Liu W-D Hung CC Wang JT Tsai MJ Kuo PH Chao TL et al Evolution of SARS-CoV-2 neutralizing antibody in an HIV-positive patient with COVID-19. J Formos Med Assoc (2021) 120(12):2186–90. 10.1016/j.jfma.2021.04.010

  • CrossRef
  • Google Scholar

• 108

  Zhao J Liao X Wang H Wei L Xing M Liu L et al Early virus clearance and delayed antibody response in a case of coronavirus disease 2019 (COVID-19) with a history of coinfection with human immunodeficiency virus type 1 and hepatitis C virus. Clin Infect Dis (2020) 71(16):2233–5. 10.1093/cid/ciaa408

  • CrossRef
  • Google Scholar

• 109

  Schnittman SR Jung W Fitch KV Zanni MV McCallum S Lee JSL et al Effect of host factors and COVID-19 infection on the humoral immune repertoire in treated HIV. JCI insight (2023) 8(5):e166848. 10.1172/jci.insight.166848

  • CrossRef
  • Google Scholar

• 110

  Donadeu L Tiraboschi JM Scévola S Torija A Meneghini M Jouve T et al Long-lasting adaptive immune memory specific to SARS-CoV-2 in convalescent coronavirus disease 2019 stable people with HIV. AIDS (2022) 36(10):1373–82. 10.1097/qad.0000000000003276

  • CrossRef
  • Google Scholar