Ecological Drivers of Mansonella perstans Infection in Uganda and Patterns of Co-endemicity with Lymphatic Filariasis and Malaria
Identifieur interne : 000A31 ( Pmc/Checkpoint ); précédent : 000A30; suivant : 000A32Ecological Drivers of Mansonella perstans Infection in Uganda and Patterns of Co-endemicity with Lymphatic Filariasis and Malaria
Auteurs : Anna-Sofie Stensgaard [Danemark] ; Penelope Vounatsou [Suisse] ; Ambrose W. Onapa [Ouganda] ; Jürg Utzinger [Suisse] ; Erling M. Pedersen [Danemark] ; Thomas K. Kristensen [Danemark] ; Paul E. Simonsen [Danemark]Source :
- PLoS Neglected Tropical Diseases [ 1935-2727 ] ; 2016.
Abstract
We analyzed data from a comprehensive nationwide survey of
Several bioclimatic factors were significantly associated with
This study presents the first geostatistical risk map for
Url:
DOI: 10.1371/journal.pntd.0004319
PubMed: 26793972
PubMed Central: 4721671
Affiliations:
Links toward previous steps (curation, corpus...)
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PMC:4721671Le document en format XML
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Infection in Uganda and Patterns of Co-endemicity with Lymphatic Filariasis and Malaria</title>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Ecological Drivers of <italic>Mansonella perstans</italic>
Infection in Uganda and Patterns of Co-endemicity with Lymphatic Filariasis and Malaria</title>
<author><name sortKey="Stensgaard, Anna Sofie" sort="Stensgaard, Anna Sofie" uniqKey="Stensgaard A" first="Anna-Sofie" last="Stensgaard">Anna-Sofie Stensgaard</name>
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<country xml:lang="fr">Danemark</country>
<wicri:regionArea>Center for Macroecology, Evolution and Climate, The Natural History Museum of Denmark, University of Copenhagen, Copenhagen</wicri:regionArea>
<placeName><settlement type="city">Copenhague</settlement>
<region type="région" nuts="2">Hovedstaden</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Vounatsou, Penelope" sort="Vounatsou, Penelope" uniqKey="Vounatsou P" first="Penelope" last="Vounatsou">Penelope Vounatsou</name>
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<wicri:noRegion>Basel</wicri:noRegion>
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<country xml:lang="fr">Suisse</country>
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<wicri:noRegion>Basel</wicri:noRegion>
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<author><name sortKey="Onapa, Ambrose W" sort="Onapa, Ambrose W" uniqKey="Onapa A" first="Ambrose W." last="Onapa">Ambrose W. Onapa</name>
<affiliation wicri:level="1"><nlm:aff id="aff004"><addr-line>Envision/NTD Program, RTI, Kampala, Uganda</addr-line>
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<author><name sortKey="Utzinger, Jurg" sort="Utzinger, Jurg" uniqKey="Utzinger J" first="Jürg" last="Utzinger">Jürg Utzinger</name>
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</nlm:aff>
<country xml:lang="fr">Suisse</country>
<wicri:regionArea>Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, Basel</wicri:regionArea>
<wicri:noRegion>Basel</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>University of Basel, Basel, Switzerland</addr-line>
</nlm:aff>
<country xml:lang="fr">Suisse</country>
<wicri:regionArea>University of Basel, Basel</wicri:regionArea>
<wicri:noRegion>Basel</wicri:noRegion>
</affiliation>
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<author><name sortKey="Pedersen, Erling M" sort="Pedersen, Erling M" uniqKey="Pedersen E" first="Erling M." last="Pedersen">Erling M. Pedersen</name>
<affiliation wicri:level="3"><nlm:aff id="aff005"><addr-line>Department of Veterinary Disease Biology, University of Copenhagen, Copenhagen, Denmark</addr-line>
</nlm:aff>
<country xml:lang="fr">Danemark</country>
<wicri:regionArea>Department of Veterinary Disease Biology, University of Copenhagen, Copenhagen</wicri:regionArea>
<placeName><settlement type="city">Copenhague</settlement>
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<author><name sortKey="Kristensen, Thomas K" sort="Kristensen, Thomas K" uniqKey="Kristensen T" first="Thomas K." last="Kristensen">Thomas K. Kristensen</name>
<affiliation wicri:level="3"><nlm:aff id="aff005"><addr-line>Department of Veterinary Disease Biology, University of Copenhagen, Copenhagen, Denmark</addr-line>
</nlm:aff>
<country xml:lang="fr">Danemark</country>
<wicri:regionArea>Department of Veterinary Disease Biology, University of Copenhagen, Copenhagen</wicri:regionArea>
<placeName><settlement type="city">Copenhague</settlement>
<region type="région" nuts="2">Hovedstaden</region>
</placeName>
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<author><name sortKey="Simonsen, Paul E" sort="Simonsen, Paul E" uniqKey="Simonsen P" first="Paul E." last="Simonsen">Paul E. Simonsen</name>
<affiliation wicri:level="3"><nlm:aff id="aff005"><addr-line>Department of Veterinary Disease Biology, University of Copenhagen, Copenhagen, Denmark</addr-line>
</nlm:aff>
<country xml:lang="fr">Danemark</country>
<wicri:regionArea>Department of Veterinary Disease Biology, University of Copenhagen, Copenhagen</wicri:regionArea>
<placeName><settlement type="city">Copenhague</settlement>
<region type="région" nuts="2">Hovedstaden</region>
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<series><title level="j">PLoS Neglected Tropical Diseases</title>
<idno type="ISSN">1935-2727</idno>
<idno type="eISSN">1935-2735</idno>
<imprint><date when="2016">2016</date>
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<front><div type="abstract" xml:lang="en"><sec id="sec001"><title>Background</title>
<p><italic>Mansonella perstans</italic>
is a widespread, but relatively unknown human filarial parasite transmitted by <italic>Culicoides</italic>
biting midges. Although it is found in many parts of sub-Saharan Africa, only few studies have been carried out to deepen the understanding of its ecology, epidemiology, and health consequences. Hence, knowledge about ecological drivers of the vector and parasite distribution, integral to develop spatially explicit models for disease prevention, control, and elimination strategies, is limited.</p>
</sec>
<sec id="sec002"><title>Methodology</title>
<p>We analyzed data from a comprehensive nationwide survey of <italic>M</italic>
. <italic>perstans</italic>
infection conducted in 76 schools across Uganda in 2000–2003, to identify environmental drivers. A suite of Bayesian geostatistical regression models was fitted, and the best fitting model based on the deviance information criterion was utilized to predict <italic>M</italic>
. <italic>perstans</italic>
infection risk for all of Uganda. Additionally, we investigated co-infection rates and co-distribution with <italic>Wuchereria bancrofti</italic>
and <italic>Plasmodium</italic>
spp. infections observed at the same survey by mapping geographically overlapping areas.</p>
</sec>
<sec id="sec003"><title>Principal Findings</title>
<p>Several bioclimatic factors were significantly associated with <italic>M</italic>
. <italic>perstans</italic>
infection levels. A spatial Bayesian regression model showed the best fit, with diurnal temperature range, normalized difference vegetation index, and cattle densities identified as significant covariates. This model was employed to predict <italic>M</italic>
. <italic>perstans</italic>
infection risk at non-sampled locations. The level of co-infection with <italic>W</italic>
. <italic>bancrofti</italic>
was low (0.3%), due to limited geographic overlap. However, where the two infections did overlap geographically, a positive association was found.</p>
</sec>
<sec id="sec004"><title>Conclusions/Significance</title>
<p>This study presents the first geostatistical risk map for <italic>M</italic>
. <italic>perstans</italic>
in Uganda. We confirmed a widespread distribution of <italic>M</italic>
. <italic>perstans</italic>
, and identified important potential drivers of risk. The results provide new insight about the ecologic preferences of this otherwise poorly known filarial parasite and its <italic>Culicoides</italic>
vector species in Uganda, which might be relevant for other settings in sub-Saharan Africa.</p>
</sec>
</div>
</front>
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<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">26793972</article-id>
<article-id pub-id-type="pmc">4721671</article-id>
<article-id pub-id-type="doi">10.1371/journal.pntd.0004319</article-id>
<article-id pub-id-type="publisher-id">PNTD-D-15-01478</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Ecological Drivers of <italic>Mansonella perstans</italic>
Infection in Uganda and Patterns of Co-endemicity with Lymphatic Filariasis and Malaria</article-title>
<alt-title alt-title-type="running-head">Ecological Drivers of <italic>Mansonella perstans</italic>
Infection in Uganda</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Stensgaard</surname>
<given-names>Anna-Sofie</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref rid="cor001" ref-type="corresp">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Vounatsou</surname>
<given-names>Penelope</given-names>
</name>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff003"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Onapa</surname>
<given-names>Ambrose W.</given-names>
</name>
<xref ref-type="aff" rid="aff004"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Utzinger</surname>
<given-names>Jürg</given-names>
</name>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff003"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Pedersen</surname>
<given-names>Erling M.</given-names>
</name>
<xref ref-type="aff" rid="aff005"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kristensen</surname>
<given-names>Thomas K.</given-names>
</name>
<xref ref-type="aff" rid="aff005"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Simonsen</surname>
<given-names>Paul E.</given-names>
</name>
<xref ref-type="aff" rid="aff005"><sup>5</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff001"><label>1</label>
<addr-line>Center for Macroecology, Evolution and Climate, The Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark</addr-line>
</aff>
<aff id="aff002"><label>2</label>
<addr-line>Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, Basel, Switzerland</addr-line>
</aff>
<aff id="aff003"><label>3</label>
<addr-line>University of Basel, Basel, Switzerland</addr-line>
</aff>
<aff id="aff004"><label>4</label>
<addr-line>Envision/NTD Program, RTI, Kampala, Uganda</addr-line>
</aff>
<aff id="aff005"><label>5</label>
<addr-line>Department of Veterinary Disease Biology, University of Copenhagen, Copenhagen, Denmark</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Lammie</surname>
<given-names>Patrick J.</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1"><addr-line>Centers for Disease Control and Prevention, 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: ASS AWO PES EMP. Analyzed the data: ASS PV. Wrote the paper: ASS PV AWO JU TKK PES. Designed and carried out the parasitologic field surveys: AWO PES EMP. Read and approved the final manuscript: ASS PV AWO PES EMP JU TKK.</p>
</fn>
<corresp id="cor001">* E-mail: <email>asstensgaard@snm.ku.dk</email>
</corresp>
</author-notes>
<pub-date pub-type="epub"><day>21</day>
<month>1</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection"><month>1</month>
<year>2016</year>
</pub-date>
<volume>10</volume>
<issue>1</issue>
<elocation-id>e0004319</elocation-id>
<history><date date-type="received"><day>21</day>
<month>8</month>
<year>2015</year>
</date>
<date date-type="accepted"><day>2</day>
<month>12</month>
<year>2015</year>
</date>
</history>
<permissions><copyright-statement>© 2016 Stensgaard et al</copyright-statement>
<copyright-year>2016</copyright-year>
<copyright-holder>Stensgaard 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.0004319.pdf"></self-uri>
<abstract><sec id="sec001"><title>Background</title>
<p><italic>Mansonella perstans</italic>
is a widespread, but relatively unknown human filarial parasite transmitted by <italic>Culicoides</italic>
biting midges. Although it is found in many parts of sub-Saharan Africa, only few studies have been carried out to deepen the understanding of its ecology, epidemiology, and health consequences. Hence, knowledge about ecological drivers of the vector and parasite distribution, integral to develop spatially explicit models for disease prevention, control, and elimination strategies, is limited.</p>
</sec>
<sec id="sec002"><title>Methodology</title>
<p>We analyzed data from a comprehensive nationwide survey of <italic>M</italic>
. <italic>perstans</italic>
infection conducted in 76 schools across Uganda in 2000–2003, to identify environmental drivers. A suite of Bayesian geostatistical regression models was fitted, and the best fitting model based on the deviance information criterion was utilized to predict <italic>M</italic>
. <italic>perstans</italic>
infection risk for all of Uganda. Additionally, we investigated co-infection rates and co-distribution with <italic>Wuchereria bancrofti</italic>
and <italic>Plasmodium</italic>
spp. infections observed at the same survey by mapping geographically overlapping areas.</p>
</sec>
<sec id="sec003"><title>Principal Findings</title>
<p>Several bioclimatic factors were significantly associated with <italic>M</italic>
. <italic>perstans</italic>
infection levels. A spatial Bayesian regression model showed the best fit, with diurnal temperature range, normalized difference vegetation index, and cattle densities identified as significant covariates. This model was employed to predict <italic>M</italic>
. <italic>perstans</italic>
infection risk at non-sampled locations. The level of co-infection with <italic>W</italic>
. <italic>bancrofti</italic>
was low (0.3%), due to limited geographic overlap. However, where the two infections did overlap geographically, a positive association was found.</p>
</sec>
<sec id="sec004"><title>Conclusions/Significance</title>
<p>This study presents the first geostatistical risk map for <italic>M</italic>
. <italic>perstans</italic>
in Uganda. We confirmed a widespread distribution of <italic>M</italic>
. <italic>perstans</italic>
, and identified important potential drivers of risk. The results provide new insight about the ecologic preferences of this otherwise poorly known filarial parasite and its <italic>Culicoides</italic>
vector species in Uganda, which might be relevant for other settings in sub-Saharan Africa.</p>
</sec>
</abstract>
<abstract abstract-type="summary"><title>Author Summary</title>
<p><italic>Mansonella perstans</italic>
is a widespread, but relatively unknown human filarial parasite that occurs in many parts of Africa. In a nationwide survey carried out in Uganda in 2000–2003, the distribution of <italic>M</italic>
. <italic>perstans</italic>
was assessed by screening school children. Here, we studied the underlying environmental drivers and ecologic correlates of the observed <italic>M</italic>
. <italic>perstans</italic>
prevalence patterns, produced a predictive risk map, and investigated associations with <italic>Wuchereria bancrofti</italic>
(causative agent of lymphatic filariasis) and <italic>Plasmodium</italic>
(causative agent of malaria). Several Bayesian geostatistical logistic regression models with and without spatially structured random effects were fitted for comparison. The model that fitted the data best was used to predict <italic>M</italic>
. <italic>perstans</italic>
infection risk for all of Uganda. Positive associations with <italic>M</italic>
. <italic>perstans</italic>
infection status were observed with cattle densities, forested areas, and vegetation greenness, whereas negative associations were observed with land surface temperature. Only a small geographic overlap was observed with <italic>W</italic>
. <italic>bancrofti</italic>
, and the overall level of co-infection was low (0.3%). However, where the two infections overlapped, a positive association was found. Our study presents the first nationwide geostatistical risk map for <italic>M</italic>
. <italic>perstans</italic>
, and gives important clues about the ecologic preferences of the still unknown main <italic>Culicoides</italic>
vector species in Uganda.</p>
</abstract>
<funding-group><funding-statement>The field surveys received financial support from the DBL–Centre for Health Research and Development, Denmark. ASS is thankful to the Danish National Research Foundation (<ext-link ext-link-type="uri" xlink:href="http://dg.dk/en/">http://dg.dk/en/</ext-link>
) for its support of the Center for Macroecology, Evolution and Climate. PV is grateful to the Swiss National Science Foundation (SNF, <ext-link ext-link-type="uri" xlink:href="http://www.snf.ch/en/">http://www.snf.ch/en/</ext-link>
) for financial support. 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="4"></fig-count>
<table-count count="4"></table-count>
<page-count count="16"></page-count>
</counts>
<custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name>
<meta-value>All relevant data are within the paper and its Supporting Information files.</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
<notes><title>Data Availability</title>
<p>All relevant data are within the paper and its Supporting Information files.</p>
</notes>
</front>
</pmc>
<affiliations><list><country><li>Danemark</li>
<li>Ouganda</li>
<li>Suisse</li>
</country>
<region><li>Hovedstaden</li>
</region>
<settlement><li>Copenhague</li>
</settlement>
</list>
<tree><country name="Danemark"><region name="Hovedstaden"><name sortKey="Stensgaard, Anna Sofie" sort="Stensgaard, Anna Sofie" uniqKey="Stensgaard A" first="Anna-Sofie" last="Stensgaard">Anna-Sofie Stensgaard</name>
</region>
<name sortKey="Kristensen, Thomas K" sort="Kristensen, Thomas K" uniqKey="Kristensen T" first="Thomas K." last="Kristensen">Thomas K. Kristensen</name>
<name sortKey="Pedersen, Erling M" sort="Pedersen, Erling M" uniqKey="Pedersen E" first="Erling M." last="Pedersen">Erling M. Pedersen</name>
<name sortKey="Simonsen, Paul E" sort="Simonsen, Paul E" uniqKey="Simonsen P" first="Paul E." last="Simonsen">Paul E. Simonsen</name>
</country>
<country name="Suisse"><noRegion><name sortKey="Vounatsou, Penelope" sort="Vounatsou, Penelope" uniqKey="Vounatsou P" first="Penelope" last="Vounatsou">Penelope Vounatsou</name>
</noRegion>
<name sortKey="Utzinger, Jurg" sort="Utzinger, Jurg" uniqKey="Utzinger J" first="Jürg" last="Utzinger">Jürg Utzinger</name>
<name sortKey="Utzinger, Jurg" sort="Utzinger, Jurg" uniqKey="Utzinger J" first="Jürg" last="Utzinger">Jürg Utzinger</name>
<name sortKey="Vounatsou, Penelope" sort="Vounatsou, Penelope" uniqKey="Vounatsou P" first="Penelope" last="Vounatsou">Penelope Vounatsou</name>
</country>
<country name="Ouganda"><noRegion><name sortKey="Onapa, Ambrose W" sort="Onapa, Ambrose W" uniqKey="Onapa A" first="Ambrose W." last="Onapa">Ambrose W. Onapa</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>
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