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

Identifieur interne : 001196 ( Pmc/Checkpoint ); précédent : 001195; suivant : 001197

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

Auteurs : Terence Tafatatha [Malawi, Royaume-Uni] ; Miriam Taegtmeyer [Royaume-Uni] ; Bagrey Ngwira [Malawi, Royaume-Uni] ; Amos Phiri [Malawi] ; Mariot Kondowe [Malawi] ; Wilson Piston [Malawi] ; Anna Molesworth [Malawi, Royaume-Uni] ; Ndoliwe Kayuni [Malawi] ; Olivier Koole [Malawi, Royaume-Uni] ; Amelia Crampin [Malawi, Royaume-Uni] ; John Horton [Royaume-Uni] ; Neil French [Malawi, Royaume-Uni]

Source :

RBID : PMC:4456405

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 χ2 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.


Url:
DOI: 10.1371/journal.pntd.0003825
PubMed: 26042839
PubMed Central: 4456405


Affiliations:


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PMC:4456405

Le document en format XML

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<name sortKey="Horton, John" sort="Horton, John" uniqKey="Horton J" first="John" last="Horton">John Horton</name>
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<country xml:lang="fr">Malawi</country>
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</nlm:aff>
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<wicri:regionArea>Institute of Infection and Global Health, University of Liverpool, Liverpool</wicri:regionArea>
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<title level="j">PLoS Neglected Tropical Diseases</title>
<idno type="ISSN">1935-2727</idno>
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<title>Background</title>
<p>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).</p>
</sec>
<sec id="sec002">
<title>Methodology and Principal Findings</title>
<p>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
<sup>2</sup>
for linear trend.</p>
</sec>
<sec id="sec003">
<title>Conclusions/Significance</title>
<p>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.</p>
</sec>
</div>
</front>
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</TEI>
<pmc article-type="research-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">PLoS Negl Trop Dis</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS Negl Trop Dis</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plosntds</journal-id>
<journal-title-group>
<journal-title>PLoS Neglected Tropical Diseases</journal-title>
</journal-title-group>
<issn pub-type="ppub">1935-2727</issn>
<issn pub-type="epub">1935-2735</issn>
<publisher>
<publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, CA USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">26042839</article-id>
<article-id pub-id-type="pmc">4456405</article-id>
<article-id pub-id-type="doi">10.1371/journal.pntd.0003825</article-id>
<article-id pub-id-type="publisher-id">PNTD-D-14-01803</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Human Immunodeficiency Virus, Antiretroviral Therapy and Markers of Lymphatic Filariasis Infection: A Cross-sectional Study in Rural Northern Malawi</article-title>
<alt-title alt-title-type="running-head">Lymphatic Filariasis and HIV</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Tafatatha</surname>
<given-names>Terence</given-names>
</name>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff002">
<sup>2</sup>
</xref>
<xref rid="cor001" ref-type="corresp">*</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Taegtmeyer</surname>
<given-names>Miriam</given-names>
</name>
<xref ref-type="aff" rid="aff003">
<sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Ngwira</surname>
<given-names>Bagrey</given-names>
</name>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff004">
<sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Phiri</surname>
<given-names>Amos</given-names>
</name>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Kondowe</surname>
<given-names>Mariot</given-names>
</name>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Piston</surname>
<given-names>Wilson</given-names>
</name>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Molesworth</surname>
<given-names>Anna</given-names>
</name>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff004">
<sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Kayuni</surname>
<given-names>Ndoliwe</given-names>
</name>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Koole</surname>
<given-names>Olivier</given-names>
</name>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff004">
<sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Crampin</surname>
<given-names>Amelia</given-names>
</name>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff004">
<sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Horton</surname>
<given-names>John</given-names>
</name>
<xref ref-type="aff" rid="aff005">
<sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>French</surname>
<given-names>Neil</given-names>
</name>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff006">
<sup>6</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff001">
<label>1</label>
<addr-line>Karonga Prevention Study, Karonga District, Malawi</addr-line>
</aff>
<aff id="aff002">
<label>2</label>
<addr-line>Centre for Neglected Tropical Diseases, Liverpool School of Tropical Medicine, Liverpool, United Kingdom</addr-line>
</aff>
<aff id="aff003">
<label>3</label>
<addr-line>Department of International Public Health, Liverpool School of Tropical Medicine, Liverpool, United Kingdom</addr-line>
</aff>
<aff id="aff004">
<label>4</label>
<addr-line>London School of Hygiene and Tropical Medicine, London, United Kingdom</addr-line>
</aff>
<aff id="aff005">
<label>5</label>
<addr-line>Tropical Projects, Hitchin, United Kingdom</addr-line>
</aff>
<aff id="aff006">
<label>6</label>
<addr-line>Institute of Infection and Global Health, University of Liverpool, Liverpool, United Kingdom</addr-line>
</aff>
<contrib-group>
<contrib contrib-type="editor">
<name>
<surname>Nutman</surname>
<given-names>Thomas B.</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1">
<addr-line>National Institutes of Health, UNITED STATES</addr-line>
</aff>
<author-notes>
<fn fn-type="conflict" id="coi001">
<p>The authors have declared that no competing interests exist.</p>
</fn>
<fn fn-type="con" id="contrib001">
<p>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.</p>
</fn>
<corresp id="cor001">* E-mail:
<email>ttafatatha@yahoo.com</email>
</corresp>
</author-notes>
<pub-date pub-type="epub">
<day>4</day>
<month>6</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="collection">
<month>6</month>
<year>2015</year>
</pub-date>
<volume>9</volume>
<issue>6</issue>
<elocation-id>e0003825</elocation-id>
<history>
<date date-type="received">
<day>13</day>
<month>10</month>
<year>2014</year>
</date>
<date date-type="accepted">
<day>12</day>
<month>5</month>
<year>2015</year>
</date>
</history>
<permissions>
<copyright-year>2015</copyright-year>
<copyright-holder>Tafatatha et al</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/">
<license-p>This is an open access article distributed under the terms of the
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>
, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:type="simple" xlink:href="pntd.0003825.pdf"></self-uri>
<abstract>
<sec id="sec001">
<title>Background</title>
<p>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).</p>
</sec>
<sec id="sec002">
<title>Methodology and Principal Findings</title>
<p>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
<sup>2</sup>
for linear trend.</p>
</sec>
<sec id="sec003">
<title>Conclusions/Significance</title>
<p>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.</p>
</sec>
</abstract>
<abstract abstract-type="summary">
<title>Author Summary</title>
<p>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.</p>
</abstract>
<funding-group>
<funding-statement>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.</funding-statement>
</funding-group>
<counts>
<fig-count count="2"></fig-count>
<table-count count="3"></table-count>
<page-count count="14"></page-count>
</counts>
<custom-meta-group>
<custom-meta id="data-availability">
<meta-name>Data Availability</meta-name>
<meta-value>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:
<email>mia.crampin@lshtm.ac.uk</email>
(
<ext-link ext-link-type="uri" xlink:href="http://www.lshtm.ac.uk/eph/ide/research/kps/index.html">http://www.lshtm.ac.uk/eph/ide/research/kps/index.html</ext-link>
). 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.</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
<notes>
<title>Data Availability</title>
<p>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:
<email>mia.crampin@lshtm.ac.uk</email>
(
<ext-link ext-link-type="uri" xlink:href="http://www.lshtm.ac.uk/eph/ide/research/kps/index.html">http://www.lshtm.ac.uk/eph/ide/research/kps/index.html</ext-link>
). 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.</p>
</notes>
</front>
</pmc>
<affiliations>
<list>
<country>
<li>Malawi</li>
<li>Royaume-Uni</li>
</country>
<region>
<li>Angleterre</li>
<li>Grand Londres</li>
</region>
<settlement>
<li>Londres</li>
</settlement>
</list>
<tree>
<country name="Malawi">
<noRegion>
<name sortKey="Tafatatha, Terence" sort="Tafatatha, Terence" uniqKey="Tafatatha T" first="Terence" last="Tafatatha">Terence Tafatatha</name>
</noRegion>
<name sortKey="Crampin, Amelia" sort="Crampin, Amelia" uniqKey="Crampin A" first="Amelia" last="Crampin">Amelia Crampin</name>
<name sortKey="French, Neil" sort="French, Neil" uniqKey="French N" first="Neil" last="French">Neil French</name>
<name sortKey="Kayuni, Ndoliwe" sort="Kayuni, Ndoliwe" uniqKey="Kayuni N" first="Ndoliwe" last="Kayuni">Ndoliwe Kayuni</name>
<name sortKey="Kondowe, Mariot" sort="Kondowe, Mariot" uniqKey="Kondowe M" first="Mariot" last="Kondowe">Mariot Kondowe</name>
<name sortKey="Koole, Olivier" sort="Koole, Olivier" uniqKey="Koole O" first="Olivier" last="Koole">Olivier Koole</name>
<name sortKey="Molesworth, Anna" sort="Molesworth, Anna" uniqKey="Molesworth A" first="Anna" last="Molesworth">Anna Molesworth</name>
<name sortKey="Ngwira, Bagrey" sort="Ngwira, Bagrey" uniqKey="Ngwira B" first="Bagrey" last="Ngwira">Bagrey Ngwira</name>
<name sortKey="Phiri, Amos" sort="Phiri, Amos" uniqKey="Phiri A" first="Amos" last="Phiri">Amos Phiri</name>
<name sortKey="Piston, Wilson" sort="Piston, Wilson" uniqKey="Piston W" first="Wilson" last="Piston">Wilson Piston</name>
</country>
<country name="Royaume-Uni">
<noRegion>
<name sortKey="Tafatatha, Terence" sort="Tafatatha, Terence" uniqKey="Tafatatha T" first="Terence" last="Tafatatha">Terence Tafatatha</name>
</noRegion>
<name sortKey="Crampin, Amelia" sort="Crampin, Amelia" uniqKey="Crampin A" first="Amelia" last="Crampin">Amelia Crampin</name>
<name sortKey="French, Neil" sort="French, Neil" uniqKey="French N" first="Neil" last="French">Neil French</name>
<name sortKey="Horton, John" sort="Horton, John" uniqKey="Horton J" first="John" last="Horton">John Horton</name>
<name sortKey="Koole, Olivier" sort="Koole, Olivier" uniqKey="Koole O" first="Olivier" last="Koole">Olivier Koole</name>
<name sortKey="Molesworth, Anna" sort="Molesworth, Anna" uniqKey="Molesworth A" first="Anna" last="Molesworth">Anna Molesworth</name>
<name sortKey="Ngwira, Bagrey" sort="Ngwira, Bagrey" uniqKey="Ngwira B" first="Bagrey" last="Ngwira">Bagrey Ngwira</name>
<name sortKey="Taegtmeyer, Miriam" sort="Taegtmeyer, Miriam" uniqKey="Taegtmeyer M" first="Miriam" last="Taegtmeyer">Miriam Taegtmeyer</name>
</country>
</tree>
</affiliations>
</record>

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