Most studies evaluating epidemiologic relationships between helminths and HIV have been conducted in the pre-ART era, and evidence of the impact of helminth infections on HIV disease progression remains conflicting. Less is known about helminth infection and clinical outcomes in HIV-infected adults receiving antiretroviral therapy (ART). We sampled HIV-infected adults for eight gastrointestinal parasites and correlated parasitic infection with demographic predictors, and clinical and immunologic outcomes. Contrasting with previous studies, we measured parasitic infection with a quantitative, highly sensitive and specific polymerase chain reaction (PCR) method. This cohort study enrolled HIV-infected Ugandans from August-September 2013 in Mbale, Uganda and collected stool and blood samples at enrollment. Real-time PCR quantified stool: Ascaris lumbricoides, Ancylostoma duodenale, Necator americanus, Strongyloides stercoralis, Trichuris trichiura, Cryptosporidium spp., Entamoeba histolytica, and Giardia intestinalis infection. Generalized linear models assessed relationships between parasitic infection and clinical or demographic data. 35% of participants (71/202) tested positive for ≥1 helminth, mainly N. americanus (55/199, 28%), and 4.5% (9/202) were infected with ≥2 stool parasites. Participants with hookworm infection had lower average CD4+cell counts (-94 cells/mcL, 95%CI: -141, -48 cells/mcL; p<0.001) after adjustment for sex, CD4+nadir at clinic entry, and time on ART. The high prevalence of parasitic infection and correlation with decreased CD4+concentrations highlight the need to re-examine the effects of invasive helminth co-infection in rural, HIV-infected populations in the era of widely available ART. Elucidating the relationship between hookworm infection and immune recovery could provide opportunities for health optimization, e.g. integrated deworming, in these vulnerable populations.
Bibliographical noteFunding Information:
This research was supported by the J. B. Hawley Student Research Awards awarded through the University of Minnesota, School of Public Health, Division of Epidemiology and Community Health (to BMM), the University of Minnesota Doctoral Dissertation Fellowship (to BMM), the Lois and Richard King Distinguished Assistant Professorship (to DRB), and the Section of Pediatric Tropical Medicine, Baylor College of Medicine (to RM). Work on this manuscript was also supported by the U.S. National Institutes of Health (NIH) Research Training Grant #R25 TW009345 funded by the Fogarty International Center (to BMM), the NIH Office of the Director of AIDS Research, the NIH Office of the Director of Research on Women?s Health, the National Heart, Lung and Blood Institute, the National Institute of Mental Health, the National Institute of General Medical Sciences, and awarded to the Northern Pacific Global Health Fellows Program by the Fogarty International Center. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank the staff at The AIDS Support Organisation in Mbale, the Translational Laboratory of the Infectious Diseases Institute, the Molecular Laboratory, particularly Lazarus Okoche, and Moses Joloba?s lab at Makerere University for assistance in the conduct of this study. We also thank Drs. Claudia Mu?oz-Zanzi and Richard MacLehose at the University of Minnesota for their critical review of this manuscript.