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      Human Immunodeficiency Virus, Antiretroviral Therapy and Markers of Lymphatic Filariasis Infection: A Cross-sectional Study in Rural Northern Malawi

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          Abstract

          Background

          Lymphatic filariasis (LF) and human immunodeficiency virus (HIV) are major public health problems. Individuals may be co-infected, raising the possibility of important interactions between these two pathogens with consequences for LF elimination through annual mass drug administration (MDA).

          Methodology and Principal Findings

          We analysed circulating filarial antigenaemia (CFA) by HIV infection status among adults in two sites in northern Malawi, a region endemic for both LF and HIV. Stored blood samples and data from two geographically separate studies were used: one a recruitment phase of a clinical trial of anti-filarial agent dosing regimens, and the other a whole population annual HIV sero-survey. In study one, 1,851 consecutive adult volunteers were screened for HIV and LF infection. CFA prevalence was 25.4% (43/169) in HIV-positive and 23.6% (351/1487) in HIV-negative participants (p=0.57). Geometric mean CFA concentrations were 859 and 1660 antigen units per ml of blood (Ag/ml) respectively, geometric mean ratio (GMR) 0.85, 95%CI 0.49-1.50. In 7,863 adults in study two, CFA prevalence was 20.9% (86/411) in HIV-positive and 24.0% (1789/7452) in HIV–negative participants (p=0.15). Geometric mean CFA concentrations were 630 and 839 Ag/ml respectively (GMR 0.75, 95%CI 0.60-0.94). In the HIV-positive group, antiretroviral therapy (ART) use was associated with a lower CFA prevalence, 12.7% (18/142) vs. 25.3% (67/265), (OR 0.43, 95%CI 0.24-0.76). Prevalence of CFA decreased with duration of ART use, 15.2% 0-1 year (n=59), 13.6% >1-2 years (n=44), 10.0% >2-3 years (n=30) and 0% >3-4 years treatment (n=9), p<0.01 χ 2 for linear trend.

          Conclusions/Significance

          In this large cross-sectional study of two distinct LF-exposed populations, there is no evidence that HIV infection has an impact on LF epidemiology that will interfere with LF control measures. A significant association of ART use with lower CFA prevalence merits further investigation to understand this apparent beneficial impact of ART.

          Author Summary

          Lymphatic filariasis (LF) and HIV are both major public health problems worldwide and where they co-exist have the potential to interact. The main strategy for LF elimination is annual mass drug administration (MDA). A particular concern is whether HIV, through its impact on the immune system, will interfere with the effectiveness of this approach to control and eliminate LF. We report findings from cross-sectional studies in two separate populations in northern Malawi where both HIV and LF are common. One group (1,851 individuals) were studied at enrolment into a trial of anti-LF treatments, whilst the other study used samples stored from adult participants in a whole population HIV survey (7,863 individuals). Between 5–10% of the study participants were HIV-positive and 24% were LF-infected. We found no evidence that LF infection was more or less common in HIV-positive adults in either population. However, we identified robust evidence that antiretroviral therapy use was associated with lower LF prevalence rates. We have no evidence to suggest HIV will have a detrimental effect on LF control. On the contrary, the evidence suggests that antiretroviral therapy may have beneficial effects and merits further careful evaluation of the anti-filarial properties of these compounds.

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          Most cited references21

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          The ICT Filariasis Test: A rapid-format antigen test for diagnosis of bancroftian filariasis.

          Antigen testing is now recognized as the method of choice for detection of Wuchereria bancrofti infections. Unlike tests that detect microfilariae, antigen tests can be performed with blood collected during the day or night. However, existing enzyme-linked immunosorbent assay (ELISA) tests for filarial antigenemia are difficult to perform in the field, and this has limited their use in endemic countries. In this article, Gary Weil, Patrick Lammie and Niggi Weiss review their experience with a new rapid-format filarial antigen test. They found that the ICT card test was very easy to perform and that it was comparable with ELISA for the detection of filarial antigen in sera from people with microfilaremia. The introduction now of an antigen test suitable for use in the field is especially timely, in that it may facilitate implementation of new strategies proposed by the World Health Organization for control and elimination of lymphatic filariasis.
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            Profile: The Karonga Health and Demographic Surveillance System

            The Karonga Health and Demographic Surveillance System (Karonga HDSS) in northern Malawi currently has a population of more than 35 000 individuals under continuous demographic surveillance since completion of a baseline census (2002–2004). The surveillance system collects data on vital events and migration for individuals and for households. It also provides data on cause-specific mortality obtained by verbal autopsy for all age groups, and estimates rates of disease for specific presentations via linkage to clinical facility data. The Karonga HDSS provides a structure for surveys of socio-economic status, HIV sero-prevalence and incidence, sexual behaviour, fertility intentions and a sampling frame for other studies, as well as evaluating the impact of interventions, such as antiretroviral therapy and vaccination programmes. Uniquely, it relies on a network of village informants to report vital events and household moves, and furthermore is linked to an archive of biological samples and data from population surveys and other studies dating back three decades.
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              Helminth infection is not associated with faster progression of HIV disease in coinfected adults in Uganda.

              We studied a cohort of human immunodeficiency virus (HIV)-infected adults in Uganda who were not receiving antiretroviral therapy, to explore the impact of helminths on HIV progression in areas where antiretrovirals are not available. A total of 663 patients were screened for helminths, treated presumptively with albendazole and selectively with praziquantel, and monitored for 6 months. Blood samples were analyzed for CD4+ cell count and HIV-1 RNA. Schistosoma mansoni, hookworm, Strongyloides stercoralis, and Mansonella perstans were the most prevalent helminths. Helminth infection was not associated with higher viral load, lower CD4+ cell count, or faster decrease in CD4+ cell count preceding antihelminthic therapy. The effect of coinfection on HIV disease progression varied with species. CD4+ cell counts were highest in subjects with hookworm and Mansonella perstans infection. For most helminths, effective treatment was associated with greater decrease in CD4+ cell count than in those in whom infection was still present at follow-up. A highly significant decrease in viral load at 6 months was seen in patients with persistent Mansonella perstans infection at follow-up. Mortality was lower in subjects with hookworm infection at enrollment. Helminth infection was not associated with more-advanced HIV disease or faster disease progression. Antihelminthic therapy may not be beneficial in slowing HIV progression in coinfected adults.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                4 June 2015
                June 2015
                : 9
                : 6
                : e0003825
                Affiliations
                [1 ]Karonga Prevention Study, Karonga District, Malawi
                [2 ]Centre for Neglected Tropical Diseases, Liverpool School of Tropical Medicine, Liverpool, United Kingdom
                [3 ]Department of International Public Health, Liverpool School of Tropical Medicine, Liverpool, United Kingdom
                [4 ]London School of Hygiene and Tropical Medicine, London, United Kingdom
                [5 ]Tropical Projects, Hitchin, United Kingdom
                [6 ]Institute of Infection and Global Health, University of Liverpool, Liverpool, United Kingdom
                National Institutes of Health, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: NF JH BN AC TT. Performed the experiments: TT AP MK WP. Analyzed the data: TT MT BN NF. Contributed reagents/materials/analysis tools: MT NF. Wrote the paper: TT BN MT AP MK WP AM NK JH NF OK AC. Read, gave comments and approved final version of the manuscript: MT AM OK AC JH NF TT.

                Article
                PNTD-D-14-01803
                10.1371/journal.pntd.0003825
                4456405
                26042839
                45e50371-4368-4338-a88a-e9d6301e1727
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 13 October 2014
                : 12 May 2015
                Page count
                Figures: 2, Tables: 3, Pages: 14
                Funding
                Study 1 was supported by an award from the Task Force for Child Survival, Emory University (Grant No 43922) and Study 2 was supported by a grant from The Wellcome Trust (Grant No 079828/Z/06/Z). Additional analysis conducted on stored samples from Study 1 and 2 was funded by the Centre for Neglected Tropical Diseases (CNTD), Liverpool School of Tropical Medicine, with a grant from the Department for International Development. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                The data for this study comes from the Karonga Prevention Study (KPS) which has been conducting research in Karonga district, rural northern Malawi for more than 30 years. KPS is fully committed to making its data fully accessible and available to other researchers and fully support the PLOS data sharing policy. To this effect, arrangements for setting up an institutional data repository are in the process through funding from the Wellcome Trust for a four-year project. This will make our extensive data (on ~300,000 individuals and > 1 million participant contacts) for the whole project more accessible, and will ensure that, as we continue to add to this unique resource, it remains usable, flexible and available to local and international researchers. This is a large undertaking and involves making major changes to the data structure, the user interface and the way new data are collected, whilst maintaining the integrity and relationships in the existing database. Meanwhile, a procedure for data sharing is in place, which requires the consent of the programme director in consultation with senior scientific staff. Applications to access the data can be made to the Deputy Director/ Scientific Programme Manager: mia.crampin@ 123456lshtm.ac.uk ( http://www.lshtm.ac.uk/eph/ide/research/kps/index.html). No reasonable data sharing requests are turned down and the programme is committed to ensuring as much access as possible to the data, while maintaining full confidentiality.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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