Risk factors and pregnancy outcomes associated with placental malaria in a prospective cohort of Papua New Guinean women
Identifieur interne : 000C32 ( Pmc/Curation ); précédent : 000C31; suivant : 000C33Risk factors and pregnancy outcomes associated with placental malaria in a prospective cohort of Papua New Guinean women
Auteurs : Elvin Lufele [Papouasie-Nouvelle-Guinée] ; Alexandra Umbers [Papouasie-Nouvelle-Guinée] ; Jaume Ordi [Espagne] ; Maria Ome-Kaius [Papouasie-Nouvelle-Guinée] ; Regina Wangnapi [Papouasie-Nouvelle-Guinée] ; Holger Unger [Papouasie-Nouvelle-Guinée] ; Nandao Tarongka [Papouasie-Nouvelle-Guinée] ; Peter Siba [Papouasie-Nouvelle-Guinée] ; Ivo Mueller [France] ; Leanne Robinson [Papouasie-Nouvelle-Guinée] ; Stephen RogersonSource :
- Malaria Journal [ 1475-2875 ] ; 2017.
Abstract
Placental biopsies were examined from 1451 pregnant women who were enrolled in a malaria prevention study at 14–26 weeks gestation. Clinical and demographic information were collected at first antenatal clinic visits and women were followed until delivery. Placental biopsies were collected and examined for PM using histology. The presence of infected erythrocytes and/or the malaria pigment in monocytes or fibrin was used to determine the type of placental infection.
Of 1451 placentas examined, PM infection was detected in 269 (18.5%), of which 54 (3.7%) were acute, 55 (3.8%) chronic, and 160 (11.0%) were past infections. Risk factors for PM included residing in rural areas (adjusted odds ratio (AOR) 3.65, 95% CI 1.76–7.51; p ≤ 0.001), being primigravid (AOR 2.45, 95% CI 1.26–4.77; p = 0.008) and having symptomatic malaria during pregnancy (AOR 2.05, 95% CI 1.16–3.62; p = 0.013). After adjustment for covariates, compared to uninfected women, acute infections (AOR 1.97, 95% CI 0.98–3.95; p = 0.056) were associated with low birth weight babies, whereas chronic infections were associated with preterm delivery (AOR 3.92, 95% CI 1.64–9.38; p = 0.002) and anaemia (AOR 2.22, 95% CI 1.02–4.84; p = 0.045).
Among pregnant PNG women receiving at least one dose of intermittent preventive treatment in pregnancy and using insecticide-treated bed nets, active PM infections were associated with adverse outcomes. Improved malaria prevention is required to optimize pregnancy outcomes.
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DOI: 10.1186/s12936-017-2077-4
PubMed: 29065884
PubMed Central: 5655867
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Alexandra Umbers<affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2179 088X</institution-id><institution-id institution-id-type="GRID">grid.1008.9</institution-id><institution>Department of Medicine and Radiology,</institution><institution>Peter Doherty Institute, University of Melbourne,</institution></institution-wrap>Melbourne, VIC Australia</nlm:aff><wicri:noCountry code="subfield">VIC Australia</wicri:noCountry></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2179 088X</institution-id><institution-id institution-id-type="GRID">grid.1008.9</institution-id><institution>Department of Medicine and Radiology,</institution><institution>Peter Doherty Institute, University of Melbourne,</institution></institution-wrap>Melbourne, VIC Australia</nlm:aff><wicri:noCountry code="subfield">VIC Australia</wicri:noCountry></affiliation><affiliation><nlm:aff id="Aff4"><institution-wrap><institution-id institution-id-type="GRID">grid.1042.7</institution-id><institution>Population Health and Immunity Division,</institution><institution>Walter and Eliza Hall Institute,</institution></institution-wrap>Melbourne, VIC Australia</nlm:aff><wicri:noCountry code="subfield">VIC Australia</wicri:noCountry></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff5"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2353 6535</institution-id><institution-id institution-id-type="GRID">grid.428999.7</institution-id><institution>Institute Pasteur,</institution></institution-wrap>Paris, France</nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Paris</wicri:regionArea></affiliation><affiliation><nlm:aff id="Aff4"><institution-wrap><institution-id institution-id-type="GRID">grid.1042.7</institution-id><institution>Population Health and Immunity Division,</institution><institution>Walter and Eliza Hall Institute,</institution></institution-wrap>Melbourne, VIC Australia</nlm:aff><wicri:noCountry code="subfield">VIC Australia</wicri:noCountry></affiliation><affiliation><nlm:aff id="Aff6"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2224 8486</institution-id><institution-id institution-id-type="GRID">grid.1056.2</institution-id><institution>Burnet Institute,</institution></institution-wrap>Melbourne, VIC Australia</nlm:aff><wicri:noCountry code="subfield">VIC Australia</wicri:noCountry></affiliation><affiliation><nlm:aff id="Aff6"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2224 8486</institution-id><institution-id institution-id-type="GRID">grid.1056.2</institution-id><institution>Burnet Institute,</institution></institution-wrap>Melbourne, VIC Australia</nlm:aff><wicri:noCountry code="subfield">VIC Australia</wicri:noCountry></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2179 088X</institution-id><institution-id institution-id-type="GRID">grid.1008.9</institution-id><institution>Department of Medicine and Radiology,</institution><institution>Peter Doherty Institute, University of Melbourne,</institution></institution-wrap>Melbourne, VIC Australia</nlm:aff><wicri:noCountry code="subfield">VIC Australia</wicri:noCountry></affiliation>Le document en format XML
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uniqKey="Lufele E" first="Elvin" last="Lufele">Elvin Lufele</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2288 2831</institution-id><institution-id institution-id-type="GRID">grid.417153.5</institution-id><institution>Papua New Guinea Institute of Medical Research,</institution></institution-wrap>Madang, Papua New Guinea</nlm:aff><country xml:lang="fr">Papouasie-Nouvelle-Guinée</country><wicri:regionArea>Madang</wicri:regionArea></affiliation></author><author><name sortKey="Umbers, Alexandra" sort="Umbers, Alexandra" uniqKey="Umbers A" first="Alexandra" last="Umbers">Alexandra Umbers</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2288 2831</institution-id><institution-id institution-id-type="GRID">grid.417153.5</institution-id><institution>Papua New Guinea Institute of Medical Research,</institution></institution-wrap>Madang, Papua New Guinea</nlm:aff><country xml:lang="fr">Papouasie-Nouvelle-Guinée</country><wicri:regionArea>Madang</wicri:regionArea></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2179 088X</institution-id><institution-id institution-id-type="GRID">grid.1008.9</institution-id><institution>Department of Medicine and Radiology,</institution><institution>Peter Doherty Institute, University of Melbourne,</institution></institution-wrap>Melbourne, VIC Australia</nlm:aff><wicri:noCountry code="subfield">VIC Australia</wicri:noCountry></affiliation></author><author><name sortKey="Ordi, Jaume" sort="Ordi, Jaume" uniqKey="Ordi J" first="Jaume" last="Ordi">Jaume Ordi</name><affiliation wicri:level="1"><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1763 3517</institution-id><institution-id institution-id-type="GRID">grid.434607.2</institution-id><institution>Barcelona Centre for International Health Research (CRESIB),</institution></institution-wrap>Barcelona, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Barcelona</wicri:regionArea></affiliation></author><author><name sortKey="Ome Kaius, Maria" sort="Ome Kaius, Maria" uniqKey="Ome Kaius M" first="Maria" last="Ome-Kaius">Maria Ome-Kaius</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2288 2831</institution-id><institution-id institution-id-type="GRID">grid.417153.5</institution-id><institution>Papua New Guinea Institute of Medical Research,</institution></institution-wrap>Madang, Papua New Guinea</nlm:aff><country xml:lang="fr">Papouasie-Nouvelle-Guinée</country><wicri:regionArea>Madang</wicri:regionArea></affiliation></author><author><name sortKey="Wangnapi, Regina" sort="Wangnapi, Regina" uniqKey="Wangnapi R" first="Regina" last="Wangnapi">Regina Wangnapi</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2288 2831</institution-id><institution-id institution-id-type="GRID">grid.417153.5</institution-id><institution>Papua New Guinea Institute of Medical Research,</institution></institution-wrap>Madang, Papua New Guinea</nlm:aff><country xml:lang="fr">Papouasie-Nouvelle-Guinée</country><wicri:regionArea>Madang</wicri:regionArea></affiliation></author><author><name sortKey="Unger, Holger" sort="Unger, Holger" uniqKey="Unger H" first="Holger" last="Unger">Holger Unger</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2288 2831</institution-id><institution-id institution-id-type="GRID">grid.417153.5</institution-id><institution>Papua New Guinea Institute of Medical Research,</institution></institution-wrap>Madang, Papua New Guinea</nlm:aff><country xml:lang="fr">Papouasie-Nouvelle-Guinée</country><wicri:regionArea>Madang</wicri:regionArea></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2179 088X</institution-id><institution-id institution-id-type="GRID">grid.1008.9</institution-id><institution>Department of Medicine and Radiology,</institution><institution>Peter Doherty Institute, University of Melbourne,</institution></institution-wrap>Melbourne, VIC Australia</nlm:aff><wicri:noCountry code="subfield">VIC Australia</wicri:noCountry></affiliation></author><author><name sortKey="Tarongka, Nandao" sort="Tarongka, Nandao" uniqKey="Tarongka N" first="Nandao" last="Tarongka">Nandao Tarongka</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2288 2831</institution-id><institution-id institution-id-type="GRID">grid.417153.5</institution-id><institution>Papua New Guinea Institute of Medical Research,</institution></institution-wrap>Madang, Papua New Guinea</nlm:aff><country xml:lang="fr">Papouasie-Nouvelle-Guinée</country><wicri:regionArea>Madang</wicri:regionArea></affiliation></author><author><name sortKey="Siba, Peter" sort="Siba, Peter" uniqKey="Siba P" first="Peter" last="Siba">Peter Siba</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2288 2831</institution-id><institution-id institution-id-type="GRID">grid.417153.5</institution-id><institution>Papua New Guinea Institute of Medical Research,</institution></institution-wrap>Madang, Papua New Guinea</nlm:aff><country xml:lang="fr">Papouasie-Nouvelle-Guinée</country><wicri:regionArea>Madang</wicri:regionArea></affiliation></author><author><name sortKey="Mueller, Ivo" sort="Mueller, Ivo" uniqKey="Mueller I" first="Ivo" last="Mueller">Ivo Mueller</name><affiliation><nlm:aff id="Aff4"><institution-wrap><institution-id institution-id-type="GRID">grid.1042.7</institution-id><institution>Population Health and Immunity Division,</institution><institution>Walter and Eliza Hall Institute,</institution></institution-wrap>Melbourne, VIC Australia</nlm:aff><wicri:noCountry code="subfield">VIC Australia</wicri:noCountry></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff5"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2353 6535</institution-id><institution-id institution-id-type="GRID">grid.428999.7</institution-id><institution>Institute Pasteur,</institution></institution-wrap>Paris, France</nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Paris</wicri:regionArea></affiliation></author><author><name sortKey="Robinson, Leanne" sort="Robinson, Leanne" uniqKey="Robinson L" first="Leanne" last="Robinson">Leanne Robinson</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2288 2831</institution-id><institution-id institution-id-type="GRID">grid.417153.5</institution-id><institution>Papua New Guinea Institute of Medical Research,</institution></institution-wrap>Madang, Papua New Guinea</nlm:aff><country xml:lang="fr">Papouasie-Nouvelle-Guinée</country><wicri:regionArea>Madang</wicri:regionArea></affiliation><affiliation><nlm:aff id="Aff4"><institution-wrap><institution-id institution-id-type="GRID">grid.1042.7</institution-id><institution>Population Health and Immunity Division,</institution><institution>Walter and Eliza Hall Institute,</institution></institution-wrap>Melbourne, VIC Australia</nlm:aff><wicri:noCountry code="subfield">VIC Australia</wicri:noCountry></affiliation><affiliation><nlm:aff id="Aff6"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2224 8486</institution-id><institution-id institution-id-type="GRID">grid.1056.2</institution-id><institution>Burnet Institute,</institution></institution-wrap>Melbourne, VIC Australia</nlm:aff><wicri:noCountry code="subfield">VIC Australia</wicri:noCountry></affiliation></author><author><name sortKey="Rogerson, Stephen" sort="Rogerson, Stephen" uniqKey="Rogerson S" first="Stephen" last="Rogerson">Stephen Rogerson</name><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2179 088X</institution-id><institution-id institution-id-type="GRID">grid.1008.9</institution-id><institution>Department of Medicine and Radiology,</institution><institution>Peter Doherty Institute, University of Melbourne,</institution></institution-wrap>Melbourne, VIC Australia</nlm:aff><wicri:noCountry code="subfield">VIC Australia</wicri:noCountry></affiliation></author></analytic><series><title level="j">Malaria Journal</title><idno type="eISSN">1475-2875</idno><imprint><date when="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p id="Par1"><italic>Plasmodium falciparum</italic> in pregnancy results in substantial poor health outcomes for both mother and child, particularly in young, primigravid mothers who are at greatest risk of placental malaria (PM) infection. Complications of PM include maternal anaemia, low birth weight and preterm delivery, which contribute to maternal and infant morbidity and mortality in coastal Papua New Guinea (PNG).</p></sec><sec><title>Methods</title><p id="Par2">Placental biopsies were examined from 1451 pregnant women who were enrolled in a malaria prevention study at 14–26 weeks gestation. Clinical and demographic information were collected at first antenatal clinic visits and women were followed until delivery. Placental biopsies were collected and examined for PM using histology. The presence of infected erythrocytes and/or the malaria pigment in monocytes or fibrin was used to determine the type of placental infection.</p></sec><sec><title>Results</title><p id="Par3">Of 1451 placentas examined, PM infection was detected in 269 (18.5%), of which 54 (3.7%) were acute, 55 (3.8%) chronic, and 160 (11.0%) were past infections. Risk factors for PM included residing in rural areas (adjusted odds ratio (AOR) 3.65, 95% CI 1.76–7.51; p ≤ 0.001), being primigravid (AOR 2.45, 95% CI 1.26–4.77; p = 0.008) and having symptomatic malaria during pregnancy (AOR 2.05, 95% CI 1.16–3.62; p = 0.013). After adjustment for covariates, compared to uninfected women, acute infections (AOR 1.97, 95% CI 0.98–3.95; p = 0.056) were associated with low birth weight babies, whereas chronic infections were associated with preterm delivery (AOR 3.92, 95% CI 1.64–9.38; p = 0.002) and anaemia (AOR 2.22, 95% CI 1.02–4.84; p = 0.045).</p></sec><sec><title>Conclusions</title><p id="Par4">Among pregnant PNG women receiving at least one dose of intermittent preventive treatment in pregnancy and using insecticide-treated bed nets, active PM infections were associated with adverse outcomes. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Malar J</journal-id><journal-id journal-id-type="iso-abbrev">Malar. 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contrib-type="author"><name><surname>Unger</surname><given-names>Holger</given-names></name><address><email>holiveoil@gmail.com</email></address><xref ref-type="aff" rid="Aff1">1</xref><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author" deceased="yes"><name><surname>Tarongka</surname><given-names>Nandao</given-names></name><address><email>ntaronka@gmail.com</email></address><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Siba</surname><given-names>Peter</given-names></name><address><email>pmaxsiba@gmail.com</email></address><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Mueller</surname><given-names>Ivo</given-names></name><address><email>mueller@wehi.edu.au</email></address><xref ref-type="aff" rid="Aff4">4</xref><xref ref-type="aff" rid="Aff5">5</xref></contrib><contrib contrib-type="author"><name><surname>Robinson</surname><given-names>Leanne</given-names></name><address><email>leanne.robinson@burnet.edu.au</email></address><xref ref-type="aff" rid="Aff1">1</xref><xref ref-type="aff" rid="Aff4">4</xref><xref ref-type="aff" rid="Aff6">6</xref></contrib><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0003-4287-1982</contrib-id><name><surname>Rogerson</surname><given-names>Stephen</given-names></name><address><email>sroger@unimelb.edu.au</email></address><xref ref-type="aff" rid="Aff2">2</xref></contrib><aff id="Aff1"><label>1</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2288 2831</institution-id><institution-id institution-id-type="GRID">grid.417153.5</institution-id><institution>Papua New Guinea Institute of Medical Research,</institution></institution-wrap>Madang, Papua New Guinea</aff><aff id="Aff2"><label>2</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2179 088X</institution-id><institution-id institution-id-type="GRID">grid.1008.9</institution-id><institution>Department of Medicine and Radiology,</institution><institution>Peter Doherty Institute, University of Melbourne,</institution></institution-wrap>Melbourne, VIC Australia</aff><aff id="Aff3"><label>3</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1763 3517</institution-id><institution-id institution-id-type="GRID">grid.434607.2</institution-id><institution>Barcelona Centre for International Health Research (CRESIB),</institution></institution-wrap>Barcelona, Spain</aff><aff id="Aff4"><label>4</label><institution-wrap><institution-id institution-id-type="GRID">grid.1042.7</institution-id><institution>Population Health and Immunity Division,</institution><institution>Walter and Eliza Hall Institute,</institution></institution-wrap>Melbourne, VIC Australia</aff><aff id="Aff5"><label>5</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2353 6535</institution-id><institution-id institution-id-type="GRID">grid.428999.7</institution-id><institution>Institute Pasteur,</institution></institution-wrap>Paris, France</aff><aff id="Aff6"><label>6</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2224 8486</institution-id><institution-id institution-id-type="GRID">grid.1056.2</institution-id><institution>Burnet Institute,</institution></institution-wrap>Melbourne, VIC Australia</aff></contrib-group><pub-date pub-type="epub"><day>24</day><month>10</month><year>2017</year></pub-date><pub-date pub-type="pmc-release"><day>24</day><month>10</month><year>2017</year></pub-date><pub-date pub-type="collection"><year>2017</year></pub-date><volume>16</volume><elocation-id>427</elocation-id><history><date date-type="received"><day>21</day><month>7</month><year>2017</year></date><date date-type="accepted"><day>19</day><month>10</month><year>2017</year></date></history><permissions><copyright-statement>© The Author(s) 2017</copyright-statement><license license-type="OpenAccess"><license-p><bold>Open Access</bold>This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/publicdomain/zero/1.0/">http://creativecommons.org/publicdomain/zero/1.0/</ext-link>) applies to the data made available in this article, unless otherwise stated.</license-p></license></permissions><abstract id="Abs1"><sec><title>Background</title><p id="Par1"><italic>Plasmodium falciparum</italic> in pregnancy results in substantial poor health outcomes for both mother and child, particularly in young, primigravid mothers who are at greatest risk of placental malaria (PM) infection. Complications of PM include maternal anaemia, low birth weight and preterm delivery, which contribute to maternal and infant morbidity and mortality in coastal Papua New Guinea (PNG).</p></sec><sec><title>Methods</title><p id="Par2">Placental biopsies were examined from 1451 pregnant women who were enrolled in a malaria prevention study at 14–26 weeks gestation. Clinical and demographic information were collected at first antenatal clinic visits and women were followed until delivery. Placental biopsies were collected and examined for PM using histology. The presence of infected erythrocytes and/or the malaria pigment in monocytes or fibrin was used to determine the type of placental infection.</p></sec><sec><title>Results</title><p id="Par3">Of 1451 placentas examined, PM infection was detected in 269 (18.5%), of which 54 (3.7%) were acute, 55 (3.8%) chronic, and 160 (11.0%) were past infections. Risk factors for PM included residing in rural areas (adjusted odds ratio (AOR) 3.65, 95% CI 1.76–7.51; p ≤ 0.001), being primigravid (AOR 2.45, 95% CI 1.26–4.77; p = 0.008) and having symptomatic malaria during pregnancy (AOR 2.05, 95% CI 1.16–3.62; p = 0.013). After adjustment for covariates, compared to uninfected women, acute infections (AOR 1.97, 95% CI 0.98–3.95; p = 0.056) were associated with low birth weight babies, whereas chronic infections were associated with preterm delivery (AOR 3.92, 95% CI 1.64–9.38; p = 0.002) and anaemia (AOR 2.22, 95% CI 1.02–4.84; p = 0.045).</p></sec><sec><title>Conclusions</title><p id="Par4">Among pregnant PNG women receiving at least one dose of intermittent preventive treatment in pregnancy and using insecticide-treated bed nets, active PM infections were associated with adverse outcomes. Improved malaria prevention is required to optimize pregnancy outcomes.</p></sec></abstract><kwd-group xml:lang="en"><title>Keywords</title><kwd>Placental malaria</kwd><kwd>Pregnancy</kwd><kwd>Birth outcomes</kwd><kwd>Intermittent preventive treatment in pregnancy</kwd><kwd>Insecticide-treated bed nets</kwd><kwd>Papua New Guinea</kwd></kwd-group><funding-group><award-group><funding-source><institution>Bill & Melinda Gates Foundation</institution></funding-source><award-id>46099</award-id><principal-award-recipient><name><surname>Rogerson</surname><given-names>Stephen</given-names></name></principal-award-recipient></award-group><award-group><funding-source><institution>European Union’s Seventh Framework Programme FP7-2007-HEALTH</institution></funding-source><award-id>PREGVAX 201588</award-id><principal-award-recipient><name><surname>Rogerson</surname><given-names>Stephen</given-names></name></principal-award-recipient></award-group><award-group><funding-source><institution>Spanish Government</institution></funding-source><award-id>EUROSALUD 2008</award-id><principal-award-recipient><name><surname>Rogerson</surname><given-names>Stephen</given-names></name></principal-award-recipient></award-group></funding-group><custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name><meta-value>© The Author(s) 2017</meta-value></custom-meta></custom-meta-group></article-meta></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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