{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,16]],"date-time":"2026-10-16T21:01:50Z","timestamp":1792184510346,"version":"4.4.0"},"reference-count":46,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,3,18]],"date-time":"2021-03-18T00:00:00Z","timestamp":1616025600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,3,18]],"date-time":"2021-03-18T00:00:00Z","timestamp":1616025600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"U.S. Department of Health & Human Services | National Institutes of Health","award":["1R01AI14505"],"award-info":[{"award-number":["1R01AI14505"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Susceptibility to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection and the risk of mortality among people living with human immunodeficiency virus (HIV)\/acquired immunodeficiency syndrome (AIDS) (PLWHA) is largely unknown. PLWHA are unique due to their altered immune system from their history of chronic HIV infection and their use of antiretroviral therapy, some of which have been used experimentally to treat coronavirus disease 2019 (COVID-19). Therefore, we conducted a systematic review and meta-analysis to assess the epidemiology of SARS-COV-2\/HIV coinfection and estimate associated mortality from COVID-19 (Prospero Registration ID: CRD42020187980). PubMed, SCOPUS, OVID and Cochrane Library databases, and medRxiv preprint repositories were searched from January 1, 2020, to December 12, 2020. Data were extracted from studies reporting COVID-19 attack and mortality rates in PLWHA compared to their HIV-negative counterparts. Pooled attack and mortality risks were quantified using random-effects models. We identified 22 studies that included 20,982,498 participants across North America, Africa, Europe, and Asia. The median age was 56\u00a0years, and 50% were male. HIV-positive persons had a significantly higher risk of SARS-CoV-2 infection [risk ratio (RR) 1.24, 95% CI 1.05\u20131.46)] and mortality from COVID-19 (RR 1.78, 95% CI 1.21\u20132.60) than HIV-negative individuals. The beneficial effects of tenofovir and protease-inhibitors in reducing the risk of SARS-CoV-2 infection and death from COVID-19 in PLWHA remain inconclusive. HIV remains a significant risk factor for acquiring SARS-CoV-2 infection and is associated with a higher risk of mortality from COVID-19. In support of the current Centers for Disease Control and Prevention (CDC) guidelines, persons with HIV need priority consideration for the SARS-CoV-2 vaccine.<\/jats:p>","DOI":"10.1038\/s41598-021-85359-3","type":"journal-article","created":{"date-parts":[[2021,3,18]],"date-time":"2021-03-18T16:47:41Z","timestamp":1616086061000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":273,"title":["Epidemiology and outcomes of COVID-19 in HIV-infected individuals: a systematic review and meta-analysis"],"prefix":"10.1038","volume":"11","author":[{"given":"Paddy","family":"Ssentongo","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9868-5495","authenticated-orcid":false,"given":"Emily S.","family":"Heilbrunn","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anna E.","family":"Ssentongo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shailesh","family":"Advani","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vernon M.","family":"Chinchilli","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jonathan J.","family":"Nunez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ping","family":"Du","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,3,18]]},"reference":[{"key":"85359_CR1","unstructured":"Johns Hopkins University. Coronavirus Resource Center, https:\/\/coronavirus.jhu.edu\/ (2020)."},{"key":"85359_CR2","doi-asserted-by":"crossref","unstructured":"Guan, W.-J. et al. Comorbidity and its impact on 1590 patients with Covid-19 in China: A Nationwide Analysis. Eur. Respir. J. 55 (2020).","DOI":"10.1183\/13993003.01227-2020"},{"key":"85359_CR3","doi-asserted-by":"publisher","first-page":"e0238215","DOI":"10.1371\/journal.pone.0238215","volume":"15","author":"P Ssentongo","year":"2020","unstructured":"Ssentongo, P., Ssentongo, A. E., Heilbrunn, E. S., Ba, D. M. & Chinchilli, V. M. Association of cardiovascular disease and 10 other pre-existing comorbidities with COVID-19 mortality: A systematic review and meta-analysis. PLoS ONE 15, e0238215 (2020).","journal-title":"PLoS ONE"},{"key":"85359_CR4","doi-asserted-by":"publisher","first-page":"e001353","DOI":"10.1136\/openhrt-2020-001353","volume":"7","author":"AE Ssentongo","year":"2020","unstructured":"Ssentongo, A. E. et al. Renin\u2013angiotensin\u2013aldosterone system inhibitors and the risk of mortality in patients with hypertension hospitalised for COVID-19: Systematic review and meta-analysis. Open Heart 7, e001353 (2020).","journal-title":"Open Heart"},{"key":"85359_CR5","doi-asserted-by":"publisher","first-page":"1188","DOI":"10.1002\/jmv.26555","volume":"93","author":"P Malik","year":"2021","unstructured":"Malik, P. et al. Obesity a predictor of outcomes of COVID-19 hospitalized patients\u2014A systematic review and meta-analysis. J. Med. Virol. 93, 1188\u20131193 (2021).","journal-title":"J. Med. Virol."},{"key":"85359_CR6","doi-asserted-by":"crossref","unstructured":"Tesoriero, J. M. et al. Elevated COVID-19 outcomes among persons living with diagnosed HIV infection in New York State: Results from a population-level match of HIV, COVID-19, and hospitalization databases. medRxiv (2020).","DOI":"10.1101\/2020.11.04.20226118"},{"key":"85359_CR7","doi-asserted-by":"crossref","unstructured":"Huang, J. 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. (2020).","DOI":"10.1093\/cid\/ciaa1186"},{"key":"85359_CR8","doi-asserted-by":"crossref","unstructured":"Guo, W. et al. A survey for COVID-19 among HIV\/AIDS patients in two districts of Wuhan, China. AIDS Patients in Two Districts of Wuhan, China (3\/4\/2020) (2020).","DOI":"10.2139\/ssrn.3550029"},{"issue":"12","key":"85359_CR9","doi-asserted-by":"publisher","first-page":"e831","DOI":"10.1016\/S2352-3018(19)30196-1","volume":"6","author":"TD Frank","year":"2019","unstructured":"Frank, T. D. et al. Global, regional, and national incidence, prevalence, and mortality of HIV, 1980\u20132017, and forecasts to 2030, for 195 countries and territories: A systematic analysis for the Global Burden of Diseases, Injuries, and Risk Factors Study 2017. Lancet HIV 6(12), e831\u2013e859 (2019).","journal-title":"Lancet HIV"},{"key":"85359_CR10","doi-asserted-by":"publisher","first-page":"e1000097","DOI":"10.1371\/journal.pmed.1000097","volume":"6","author":"D Moher","year":"2009","unstructured":"Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G. & Group, P. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med. 6, e1000097 (2009).","journal-title":"PLoS Med."},{"key":"85359_CR11","volume-title":"The Newcastle-Ottawa Scale (NOS) for Assessing the Quality of Nonrandomised Studies in Meta-analyses","author":"J Peterson","year":"2011","unstructured":"Peterson, J., Welch, V., Losos, M. & Tugwell, P. The Newcastle-Ottawa Scale (NOS) for Assessing the Quality of Nonrandomised Studies in Meta-analyses (Ottawa Hospital Research Institute, 2011)."},{"key":"85359_CR12","doi-asserted-by":"publisher","DOI":"10.1007\/978-3-319-21416-0","volume-title":"Meta-Analysis with R","author":"G Schwarzer","year":"2015","unstructured":"Schwarzer, G., Carpenter, J. R. & R\u00fccker, G. Meta-Analysis with R (Springer, 2015)."},{"key":"85359_CR13","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1016\/j.cct.2006.04.004","volume":"28","author":"R DerSimonian","year":"2007","unstructured":"DerSimonian, R. & Kacker, R. Random-effects model for meta-analysis of clinical trials: An update. Contemp. Clin. Trials 28, 105\u2013114 (2007).","journal-title":"Contemp. Clin. Trials"},{"key":"85359_CR14","doi-asserted-by":"publisher","first-page":"557","DOI":"10.1136\/bmj.327.7414.557","volume":"327","author":"JP Higgins","year":"2003","unstructured":"Higgins, J. P., Thompson, S. G., Deeks, J. J. & Altman, D. G. Measuring inconsistency in meta-analyses. BMJ 327, 557\u2013560 (2003).","journal-title":"BMJ"},{"key":"85359_CR15","doi-asserted-by":"publisher","first-page":"629","DOI":"10.1136\/bmj.315.7109.629","volume":"315","author":"M Egger","year":"1997","unstructured":"Egger, M., Smith, G. D., Schneider, M. & Minder, C. Bias in meta-analysis detected by a simple, graphical test. BMJ 315, 629\u2013634 (1997).","journal-title":"BMJ"},{"key":"85359_CR16","doi-asserted-by":"crossref","unstructured":"Haerter, G. et al. COVID-19 in people living with human immunodeficiency virus: A case series of 33 patients. Infection 1 (2020).","DOI":"10.1007\/s15010-020-01438-z"},{"key":"85359_CR17","doi-asserted-by":"publisher","first-page":"e314","DOI":"10.1016\/S2352-3018(20)30111-9","volume":"7","author":"JL Blanco","year":"2020","unstructured":"Blanco, J. L. et al. COVID-19 in patients with HIV: Clinical case series. Lancet HIV 7, e314\u2013e316 (2020).","journal-title":"Lancet HIV"},{"key":"85359_CR18","unstructured":"Gervasoni, C. et al. Clinical features and outcomes of HIV patients with coronavirus disease 2019. Clin. Infect. Dis. (2020)."},{"issue":"20","key":"85359_CR19","doi-asserted-by":"publisher","first-page":"2052","DOI":"10.1001\/jama.2020.6775","volume":"323","author":"S Richardson","year":"2020","unstructured":"Richardson, S. et al. Presenting characteristics, comorbidities, and outcomes among 5700 patients hospitalized with COVID-19 in the New York City area. JAMA 323(20), 2052\u20132059 (2020).","journal-title":"JAMA"},{"key":"85359_CR20","doi-asserted-by":"publisher","first-page":"1788","DOI":"10.1093\/gerona\/glaa089","volume":"75","author":"T Chen","year":"2020","unstructured":"Chen, T. et al. Clinical characteristics and outcomes of older patients with coronavirus disease 2019 (COVID-19) in Wuhan, China: A single-centered, retrospective study. J. Gerontol. Ser. A 75, 1788\u20131795 (2020).","journal-title":"J. Gerontol. Ser. A"},{"key":"85359_CR21","doi-asserted-by":"crossref","unstructured":"Karmen-Tuohy, S. et al. Outcomes among HIV-positive patients hospitalized with COVID-19. J. Acquir. Immune Defic. Syndr. (1999) (2020).","DOI":"10.1101\/2020.05.07.20094797"},{"key":"85359_CR22","doi-asserted-by":"publisher","first-page":"2012","DOI":"10.1056\/NEJMoa2004500","volume":"382","author":"PK Bhatraju","year":"2020","unstructured":"Bhatraju, P. K. et al. Covid-19 in critically ill patients in the Seattle region\u2014Case series. N. Engl. J. Med. 382, 2012\u20132022 (2020).","journal-title":"N. Engl. J. Med."},{"key":"85359_CR23","doi-asserted-by":"publisher","first-page":"1763","DOI":"10.1016\/S0140-6736(20)31189-2","volume":"395","author":"MJ Cummings","year":"2020","unstructured":"Cummings, M. J. et al. Epidemiology, clinical course, and outcomes of critically ill adults with COVID-19 in New York City: A prospective cohort study. Lancet 395, 1763\u20131770 (2020).","journal-title":"Lancet"},{"key":"85359_CR24","doi-asserted-by":"crossref","unstructured":"Prieto-Alhambra, D. et al. Hospitalization and 30-day fatality in 121,263 COVID-19 outpatient cases. MedRxiv (2020).","DOI":"10.1101\/2020.05.04.20090050"},{"key":"85359_CR25","unstructured":"Argenziano, M. G. et al. Characterization and clinical course of 1000 patients with coronavirus disease 2019 in New York: Retrospective case series. BMJ 369 (2020)."},{"key":"85359_CR26","doi-asserted-by":"publisher","first-page":"e0243027","DOI":"10.1371\/journal.pone.0243027","volume":"15","author":"R Kalyanaraman Marcello","year":"2020","unstructured":"Kalyanaraman Marcello, R. et al. Characteristics and outcomes of COVID-19 patients in New York City\u2019s public hospital system. PLoS ONE 15, e0243027 (2020).","journal-title":"PLoS ONE"},{"key":"85359_CR27","doi-asserted-by":"crossref","unstructured":"Crotty, M. P. et al. Investigation of subsequent and coinfections associated with SARS-CoV-2 (COVID-19) in hospitalized patients. medRxiv (2020).","DOI":"10.1101\/2020.05.29.20117176"},{"key":"85359_CR28","doi-asserted-by":"crossref","unstructured":"Suwanwongse, K. & Shabarek, N. Clinical features and outcome of HIV\/SARS\u2010CoV\u20102 coinfected patients in the Bronx, New York City. J. Med. Virol. (2020).","DOI":"10.1002\/jmv.26077"},{"key":"85359_CR29","doi-asserted-by":"publisher","first-page":"e554","DOI":"10.1016\/S2352-3018(20)30164-8","volume":"7","author":"P Vizcarra","year":"2020","unstructured":"Vizcarra, P. et al. Description of COVID-19 in HIV-infected individuals: A single-centre, prospective cohort. Lancet HIV 7, e554\u2013e564 (2020).","journal-title":"Lancet HIV"},{"key":"85359_CR30","doi-asserted-by":"crossref","unstructured":"Bhaskaran, K. 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. Lancet HIV (2020).","DOI":"10.1101\/2020.08.07.20169490"},{"key":"85359_CR31","unstructured":"Boulle, A. et al. Risk factors for COVID-19 death in a population cohort study from the Western Cape Province, South Africa. Clin. Infect. Dis. (2020)."},{"key":"85359_CR32","doi-asserted-by":"publisher","first-page":"1765","DOI":"10.1097\/QAD.0000000000002639","volume":"34","author":"C Charre","year":"2020","unstructured":"Charre, C. et al. Coronavirus disease 2019 attack rate in HIV-infected patients and in preexposure prophylaxis users. AIDS 34, 1765 (2020).","journal-title":"AIDS"},{"key":"85359_CR33","doi-asserted-by":"crossref","unstructured":"D\u2019Souza, G. et al. COVID-19 symptoms and SARS-CoV-2 infection among people living with HIV in the US: The MACS\/WIHS combined cohort study. HIV Res. Clin. Pract. 1\u201310 (2020).","DOI":"10.1080\/25787489.2020.1844521"},{"key":"85359_CR34","doi-asserted-by":"crossref","unstructured":"Geretti, A. M. et al. Outcomes of coronavirus disease 2019 (COVID-19) related hospitalization among people with human immunodeficiency virus (HIV) in the ISARIC World Health Organization (WHO) clinical characterization protocol (UK): A prospective observational study. Clin. Infect. Dis. (2020).","DOI":"10.1093\/cid\/ciaa1605"},{"key":"85359_CR35","doi-asserted-by":"publisher","first-page":"536","DOI":"10.7326\/M20-3689","volume":"173","author":"J Del Amo","year":"2020","unstructured":"Del Amo, J. et al. Incidence and severity of COVID-19 in HIV-positive persons receiving antiretroviral therapy: A cohort study. Ann. Intern. Med. 173, 536\u2013541 (2020).","journal-title":"Ann. Intern. Med."},{"key":"85359_CR36","doi-asserted-by":"publisher","first-page":"e808","DOI":"10.1016\/j.ijid.2011.08.001","volume":"15","author":"GC De Santis","year":"2011","unstructured":"De Santis, G. C. et al. Hematological abnormalities in HIV-infected patients. Int. J. Infect. Dis. 15, e808\u2013e811 (2011).","journal-title":"Int. J. Infect. Dis."},{"key":"85359_CR37","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1016\/j.ijid.2018.02.009","volume":"70","author":"RA Maciel","year":"2018","unstructured":"Maciel, R. A., Kl\u00fcck, H. M., Durand, M. & Sprinz, E. Comorbidity is more common and occurs earlier in persons living with HIV than in HIV-uninfected matched controls, aged 50 years and older: A cross-sectional study. Int. J. Infect. Dis. 70, 30\u201335 (2018).","journal-title":"Int. J. Infect. Dis."},{"key":"85359_CR38","doi-asserted-by":"publisher","first-page":"875","DOI":"10.1038\/nri3547","volume":"13","author":"AC Shaw","year":"2013","unstructured":"Shaw, A. C., Goldstein, D. R. & Montgomery, R. R. Age-dependent dysregulation of innate immunity. Nat. Rev. Immunol. 13, 875\u2013887 (2013).","journal-title":"Nat. Rev. Immunol."},{"key":"85359_CR39","doi-asserted-by":"publisher","first-page":"107","DOI":"10.3389\/fimmu.2013.00107","volume":"4","author":"MA Moro-Garc\u00eda","year":"2013","unstructured":"Moro-Garc\u00eda, M. A., Alonso-Arias, R. & L\u00f3pez-Larrea, C. When aging reaches CD4+ T-cells: Phenotypic and functional changes. Front. Immunol. 4, 107 (2013).","journal-title":"Front. Immunol."},{"key":"85359_CR40","doi-asserted-by":"crossref","unstructured":"Qin, C. et al. Dysregulation of immune response in patients with COVID-19 in Wuhan, China. Clin. Infect. Dis. (2020).","DOI":"10.2139\/ssrn.3541136"},{"key":"85359_CR41","doi-asserted-by":"publisher","first-page":"1033","DOI":"10.1016\/S0140-6736(20)30628-0","volume":"395","author":"P Mehta","year":"2020","unstructured":"Mehta, P. et al. COVID-19: Consider cytokine storm syndromes and immunosuppression. Lancet 395, 1033 (2020).","journal-title":"Lancet"},{"key":"85359_CR42","doi-asserted-by":"publisher","first-page":"1831","DOI":"10.1097\/00002030-200109280-00012","volume":"15","author":"JE Kaplan","year":"2001","unstructured":"Kaplan, J. E., Hanson, D. L., Jones, J. L. & Dworkin, M. S. Viral load as an independent risk factor for opportunistic infections in HIV-infected adults and adolescents. AIDS 15, 1831\u20131836 (2001).","journal-title":"AIDS"},{"key":"85359_CR43","doi-asserted-by":"publisher","first-page":"939","DOI":"10.1080\/09540121.2010.482126","volume":"22","author":"L Sherr","year":"2010","unstructured":"Sherr, L. et al. Self-reported non-adherence to ART and virological outcome in a multiclinic UK study. AIDS Care 22, 939\u2013945 (2010).","journal-title":"AIDS Care"},{"key":"85359_CR44","doi-asserted-by":"publisher","first-page":"117592","DOI":"10.1016\/j.lfs.2020.117592","volume":"253","author":"AA Elfiky","year":"2020","unstructured":"Elfiky, A. A. Ribavirin, Remdesivir, sofosbuvir, galidesivir, and tenofovir against SARS-CoV-2 RNA dependent RNA polymerase (RdRp): A molecular docking study. Life Sci. 253, 117592 (2020).","journal-title":"Life Sci."},{"key":"85359_CR45","doi-asserted-by":"publisher","first-page":"128","DOI":"10.1111\/joim.13063","volume":"288","author":"J Wu","year":"2020","unstructured":"Wu, J. et al. Early antiviral treatment contributes to alleviate the severity and improve the prognosis of patients with novel coronavirus disease (COVID-19). J. Intern. Med. 288, 128\u2013138 (2020).","journal-title":"J. Intern. Med."},{"key":"85359_CR46","unstructured":"Cao, B. et al. A trial of lopinavir\u2013ritonavir in adults hospitalized with severe Covid-19. N. Engl. J. Med. (2020)."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-85359-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-85359-3","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-85359-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,3]],"date-time":"2022-12-03T05:27:23Z","timestamp":1670045243000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-85359-3"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,3,18]]},"references-count":46,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,12]]}},"alternative-id":["85359"],"URL":"https:\/\/doi.org\/10.1038\/s41598-021-85359-3","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,3,18]]},"assertion":[{"value":"21 August 2020","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"28 February 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"18 March 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"6283"}}