Effects of Maternal Worm Infections and Anthelminthic Treatment during Pregnancy on Infant Motor and Neurocognitive Functioning
Identifieur interne : 002699 ( Pmc/Corpus ); précédent : 002698; suivant : 002700Effects of Maternal Worm Infections and Anthelminthic Treatment during Pregnancy on Infant Motor and Neurocognitive Functioning
Auteurs : Margaret Nampijja ; Barbara Apule ; Swaib Lule ; Hellen Akurut ; Lawrence Muhangi ; Emily L. Webb ; Charlie Lewis ; Alison M. Elliott ; Katie J. AlcockSource :
- Journal of the International Neuropsychological Society [ 1355-6177 ] ; 2012.
Abstract
We tested the hypothesis that maternal worm infections in pregnancy affect infant motor
and neurocognitive development, and that anthelminthic treatment during pregnancy can
reverse these effects. We used measures which examine infant motor, cognitive and
executive function, including inhibition. We assessed 983 Ugandan infants aged 15 months,
using locally appropriate measures within the Entebbe Mother and Baby Study, a trial of
anthelminthic treatment during pregnancy. Key exposures were maternal worm infections and
anthelminthic treatment during pregnancy. Effects of other health and social factors were
controlled for statistically. Of the five major worm species found in the pregnant women,
two had influences on the developmental measures: Maternal
Url:
DOI: 10.1017/S1355617712000768
PubMed: 23158229
PubMed Central: 3948080
Links to Exploration step
PMC:3948080Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Effects of Maternal Worm Infections and Anthelminthic Treatment during
Pregnancy on Infant Motor and Neurocognitive Functioning</title><author><name sortKey="Nampijja, Margaret" sort="Nampijja, Margaret" uniqKey="Nampijja M" first="Margaret" last="Nampijja">Margaret Nampijja</name><affiliation><nlm:aff id="aff1"><addr-line>Co-infections Studies Programme</addr-line>,<institution>MRC/UVRI Uganda Research Unit on AIDS</institution>,<addr-line>Entebbe</addr-line>,<country>Uganda</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><addr-line>Department of Psychology</addr-line>,<institution>Lancaster University</institution>,<addr-line>Lancaster</addr-line>,<country>United Kingdom</country></nlm:aff></affiliation></author><author><name sortKey="Apule, Barbara" sort="Apule, Barbara" uniqKey="Apule B" first="Barbara" last="Apule">Barbara Apule</name><affiliation><nlm:aff id="aff3"><addr-line>Department of Obstetrics & Gynecology</addr-line>,<institution>Entebbe General Hospital</institution>,<addr-line>Entebbe</addr-line>,<country>Uganda</country></nlm:aff></affiliation></author><author><name sortKey="Lule, Swaib" sort="Lule, Swaib" uniqKey="Lule S" first="Swaib" last="Lule">Swaib Lule</name><affiliation><nlm:aff id="aff1"><addr-line>Co-infections Studies Programme</addr-line>,<institution>MRC/UVRI Uganda Research Unit on AIDS</institution>,<addr-line>Entebbe</addr-line>,<country>Uganda</country></nlm:aff></affiliation></author><author><name sortKey="Akurut, Hellen" sort="Akurut, Hellen" uniqKey="Akurut H" first="Hellen" last="Akurut">Hellen Akurut</name><affiliation><nlm:aff id="aff1"><addr-line>Co-infections Studies Programme</addr-line>,<institution>MRC/UVRI Uganda Research Unit on AIDS</institution>,<addr-line>Entebbe</addr-line>,<country>Uganda</country></nlm:aff></affiliation></author><author><name sortKey="Muhangi, Lawrence" sort="Muhangi, Lawrence" uniqKey="Muhangi L" first="Lawrence" last="Muhangi">Lawrence Muhangi</name><affiliation><nlm:aff id="aff1"><addr-line>Co-infections Studies Programme</addr-line>,<institution>MRC/UVRI Uganda Research Unit on AIDS</institution>,<addr-line>Entebbe</addr-line>,<country>Uganda</country></nlm:aff></affiliation></author><author><name sortKey="Webb, Emily L" sort="Webb, Emily L" uniqKey="Webb E" first="Emily L." last="Webb">Emily L. Webb</name><affiliation><nlm:aff id="aff4"><addr-line>Department of Clinical Research</addr-line>,<institution>London School of Hygiene and Tropical Medicine</institution>,<addr-line>London</addr-line>,<country>United Kingdom</country></nlm:aff></affiliation></author><author><name sortKey="Lewis, Charlie" sort="Lewis, Charlie" uniqKey="Lewis C" first="Charlie" last="Lewis">Charlie Lewis</name><affiliation><nlm:aff id="aff2"><addr-line>Department of Psychology</addr-line>,<institution>Lancaster University</institution>,<addr-line>Lancaster</addr-line>,<country>United Kingdom</country></nlm:aff></affiliation></author><author><name sortKey="Elliott, Alison M" sort="Elliott, Alison M" uniqKey="Elliott A" first="Alison M." last="Elliott">Alison M. Elliott</name><affiliation><nlm:aff id="aff1"><addr-line>Co-infections Studies Programme</addr-line>,<institution>MRC/UVRI Uganda Research Unit on AIDS</institution>,<addr-line>Entebbe</addr-line>,<country>Uganda</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><addr-line>Department of Clinical Research</addr-line>,<institution>London School of Hygiene and Tropical Medicine</institution>,<addr-line>London</addr-line>,<country>United Kingdom</country></nlm:aff></affiliation></author><author><name sortKey="Alcock, Katie J" sort="Alcock, Katie J" uniqKey="Alcock K" first="Katie J." last="Alcock">Katie J. Alcock</name><affiliation><nlm:aff id="aff2"><addr-line>Department of Psychology</addr-line>,<institution>Lancaster University</institution>,<addr-line>Lancaster</addr-line>,<country>United Kingdom</country></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">23158229</idno><idno type="pmc">3948080</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3948080</idno><idno type="RBID">PMC:3948080</idno><idno type="doi">10.1017/S1355617712000768</idno><date when="2012">2012</date><idno type="wicri:Area/Pmc/Corpus">002699</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">002699</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Effects of Maternal Worm Infections and Anthelminthic Treatment during
Pregnancy on Infant Motor and Neurocognitive Functioning</title><author><name sortKey="Nampijja, Margaret" sort="Nampijja, Margaret" uniqKey="Nampijja M" first="Margaret" last="Nampijja">Margaret Nampijja</name><affiliation><nlm:aff id="aff1"><addr-line>Co-infections Studies Programme</addr-line>,<institution>MRC/UVRI Uganda Research Unit on AIDS</institution>,<addr-line>Entebbe</addr-line>,<country>Uganda</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><addr-line>Department of Psychology</addr-line>,<institution>Lancaster University</institution>,<addr-line>Lancaster</addr-line>,<country>United Kingdom</country></nlm:aff></affiliation></author><author><name sortKey="Apule, Barbara" sort="Apule, Barbara" uniqKey="Apule B" first="Barbara" last="Apule">Barbara Apule</name><affiliation><nlm:aff id="aff3"><addr-line>Department of Obstetrics & Gynecology</addr-line>,<institution>Entebbe General Hospital</institution>,<addr-line>Entebbe</addr-line>,<country>Uganda</country></nlm:aff></affiliation></author><author><name sortKey="Lule, Swaib" sort="Lule, Swaib" uniqKey="Lule S" first="Swaib" last="Lule">Swaib Lule</name><affiliation><nlm:aff id="aff1"><addr-line>Co-infections Studies Programme</addr-line>,<institution>MRC/UVRI Uganda Research Unit on AIDS</institution>,<addr-line>Entebbe</addr-line>,<country>Uganda</country></nlm:aff></affiliation></author><author><name sortKey="Akurut, Hellen" sort="Akurut, Hellen" uniqKey="Akurut H" first="Hellen" last="Akurut">Hellen Akurut</name><affiliation><nlm:aff id="aff1"><addr-line>Co-infections Studies Programme</addr-line>,<institution>MRC/UVRI Uganda Research Unit on AIDS</institution>,<addr-line>Entebbe</addr-line>,<country>Uganda</country></nlm:aff></affiliation></author><author><name sortKey="Muhangi, Lawrence" sort="Muhangi, Lawrence" uniqKey="Muhangi L" first="Lawrence" last="Muhangi">Lawrence Muhangi</name><affiliation><nlm:aff id="aff1"><addr-line>Co-infections Studies Programme</addr-line>,<institution>MRC/UVRI Uganda Research Unit on AIDS</institution>,<addr-line>Entebbe</addr-line>,<country>Uganda</country></nlm:aff></affiliation></author><author><name sortKey="Webb, Emily L" sort="Webb, Emily L" uniqKey="Webb E" first="Emily L." last="Webb">Emily L. Webb</name><affiliation><nlm:aff id="aff4"><addr-line>Department of Clinical Research</addr-line>,<institution>London School of Hygiene and Tropical Medicine</institution>,<addr-line>London</addr-line>,<country>United Kingdom</country></nlm:aff></affiliation></author><author><name sortKey="Lewis, Charlie" sort="Lewis, Charlie" uniqKey="Lewis C" first="Charlie" last="Lewis">Charlie Lewis</name><affiliation><nlm:aff id="aff2"><addr-line>Department of Psychology</addr-line>,<institution>Lancaster University</institution>,<addr-line>Lancaster</addr-line>,<country>United Kingdom</country></nlm:aff></affiliation></author><author><name sortKey="Elliott, Alison M" sort="Elliott, Alison M" uniqKey="Elliott A" first="Alison M." last="Elliott">Alison M. Elliott</name><affiliation><nlm:aff id="aff1"><addr-line>Co-infections Studies Programme</addr-line>,<institution>MRC/UVRI Uganda Research Unit on AIDS</institution>,<addr-line>Entebbe</addr-line>,<country>Uganda</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><addr-line>Department of Clinical Research</addr-line>,<institution>London School of Hygiene and Tropical Medicine</institution>,<addr-line>London</addr-line>,<country>United Kingdom</country></nlm:aff></affiliation></author><author><name sortKey="Alcock, Katie J" sort="Alcock, Katie J" uniqKey="Alcock K" first="Katie J." last="Alcock">Katie J. Alcock</name><affiliation><nlm:aff id="aff2"><addr-line>Department of Psychology</addr-line>,<institution>Lancaster University</institution>,<addr-line>Lancaster</addr-line>,<country>United Kingdom</country></nlm:aff></affiliation></author></analytic><series><title level="j">Journal of the International Neuropsychological Society</title><idno type="ISSN">1355-6177</idno><idno type="eISSN">1469-7661</idno><imprint><date when="2012">2012</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>We tested the hypothesis that maternal worm infections in pregnancy affect infant motor
and neurocognitive development, and that anthelminthic treatment during pregnancy can
reverse these effects. We used measures which examine infant motor, cognitive and
executive function, including inhibition. We assessed 983 Ugandan infants aged 15 months,
using locally appropriate measures within the Entebbe Mother and Baby Study, a trial of
anthelminthic treatment during pregnancy. Key exposures were maternal worm infections and
anthelminthic treatment during pregnancy. Effects of other health and social factors were
controlled for statistically. Of the five major worm species found in the pregnant women,
two had influences on the developmental measures: Maternal <italic>Mansonella
perstans</italic> and <italic>Strongyloides stercoralis</italic> infections showed
negative associations with the A-not B-task, and Language, respectively. Performance on
other psychomotor and cognitive measures was associated with illnesses during infancy and
infants’ behavior during assessment, but not with maternal worm infections. There were no
positive effects of maternal anthelminthic treatment on infant abilities.
<italic>Mansonella perstans</italic> and <italic>Strongyloides stercoralis</italic>infection during pregnancy seem associated with impaired early executive function and
language, respectively, but single-dose anthelminthic treatment during pregnancy was not
beneficial. The biological mechanisms that could underlie these neurocognitive effects are
discussed. (<italic>JINS</italic>, 2012, <italic>18</italic>, 1019–1030)</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Abubakar, A" uniqKey="Abubakar A">A. Abubakar</name></author><author><name sortKey="Holding, P" uniqKey="Holding P">P. Holding</name></author><author><name sortKey="Van Baar, A" uniqKey="Van Baar A">A. Van Baar</name></author><author><name sortKey="Newton, C R" uniqKey="Newton C">C.R. Newton</name></author><author><name sortKey="Van De Vijver, F J" uniqKey="Van De Vijver F">F.J. Van de Vijver</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Abubakar, A" uniqKey="Abubakar A">A. Abubakar</name></author><author><name sortKey="Holding, P" uniqKey="Holding P">P. Holding</name></author><author><name sortKey="Van De Vijver, F" uniqKey="Van De Vijver F">F. Van de Vijver</name></author><author><name sortKey="Bomu, G" uniqKey="Bomu G">G. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">J Int Neuropsychol Soc</journal-id><journal-id journal-id-type="iso-abbrev">J Int Neuropsychol Soc</journal-id><journal-id journal-id-type="publisher-id">INS</journal-id><journal-title-group><journal-title>Journal of the International Neuropsychological Society</journal-title></journal-title-group><issn pub-type="ppub">1355-6177</issn><issn pub-type="epub">1469-7661</issn><publisher><publisher-name>Cambridge University Press</publisher-name><publisher-loc>New York, USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">23158229</article-id><article-id pub-id-type="pmc">3948080</article-id><article-id pub-id-type="doi">10.1017/S1355617712000768</article-id><article-id pub-id-type="pii">S1355617712000768</article-id><article-id pub-id-type="publisher-id">00076</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Articles</subject></subj-group></article-categories><title-group><article-title>Effects of Maternal Worm Infections and Anthelminthic Treatment during
Pregnancy on Infant Motor and Neurocognitive Functioning</article-title><alt-title alt-title-type="left-running">M. Nampijja <italic>et al.</italic></alt-title><alt-title alt-title-type="right-running">Developmental effects of maternal
worms</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Nampijja</surname><given-names>Margaret</given-names></name><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="aff" rid="aff2">2</xref><xref ref-type="corresp" rid="cor1"></xref></contrib><contrib contrib-type="author"><name><surname>Apule</surname><given-names>Barbara</given-names></name><xref ref-type="aff" rid="aff3">3</xref></contrib><contrib contrib-type="author"><name><surname>Lule</surname><given-names>Swaib</given-names></name><xref ref-type="aff" rid="aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Akurut</surname><given-names>Hellen</given-names></name><xref ref-type="aff" rid="aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Muhangi</surname><given-names>Lawrence</given-names></name><xref ref-type="aff" rid="aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Webb</surname><given-names>Emily L.</given-names></name><xref ref-type="aff" rid="aff4">4</xref></contrib><contrib contrib-type="author"><name><surname>Lewis</surname><given-names>Charlie</given-names></name><xref ref-type="aff" rid="aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Elliott</surname><given-names>Alison M.</given-names></name><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="aff" rid="aff4">4</xref></contrib><contrib contrib-type="author"><name><surname>Alcock</surname><given-names>Katie J.</given-names></name><xref ref-type="aff" rid="aff2">2</xref></contrib></contrib-group><aff id="aff1"><label>1</label><addr-line>Co-infections Studies Programme</addr-line>,<institution>MRC/UVRI Uganda Research Unit on AIDS</institution>,<addr-line>Entebbe</addr-line>,<country>Uganda</country></aff><aff id="aff2"><label>2</label><addr-line>Department of Psychology</addr-line>,<institution>Lancaster University</institution>,<addr-line>Lancaster</addr-line>,<country>United Kingdom</country></aff><aff id="aff3"><label>3</label><addr-line>Department of Obstetrics & Gynecology</addr-line>,<institution>Entebbe General Hospital</institution>,<addr-line>Entebbe</addr-line>,<country>Uganda</country></aff><aff id="aff4"><label>4</label><addr-line>Department of Clinical Research</addr-line>,<institution>London School of Hygiene and Tropical Medicine</institution>,<addr-line>London</addr-line>,<country>United Kingdom</country></aff><author-notes><corresp id="cor1">Correspondence and reprint requests to: Margaret Nampijja, Department of
Psychology, Lancaster University, Fylde College, Lancaster LA1 4YF, UK. E-mail: <email>m.nampijja@lancaster.ac.uk</email></corresp></author-notes><pub-date pub-type="ppub"><month>11</month><year>2012</year></pub-date><volume>18</volume><issue>6</issue><fpage>1019</fpage><lpage>1030</lpage><history><date date-type="received"><day>25</day><month>2</month><year>2011</year></date><date date-type="rev-recd"><day>05</day><month>5</month><year>2012</year></date><date date-type="accepted"><day>07</day><month>5</month><year>2012</year></date></history><permissions><copyright-statement>© The International Neuropsychological Society 2012</copyright-statement><copyright-year>2012</copyright-year><copyright-holder>The International Neuropsychological Society</copyright-holder><license license-type="open-access"><license-p><pmc-comment>CREATIVE COMMONS</pmc-comment>The online version of this article is published within an Open Access
environment subject to the conditions of the Creative Commons
Attribution-NonCommercial-ShareAlike licence
<<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc-sa/3.0/">http://creativecommons.org/licenses/by-nc-sa/3.0/</ext-link>>. The written
permission of Cambridge University Press must be obtained for commercial
re-use.</license-p></license></permissions><self-uri xlink:title="pdf" xlink:type="simple" xlink:href="S1355617712000768a.pdf"></self-uri><abstract abstract-type="normal"><p>We tested the hypothesis that maternal worm infections in pregnancy affect infant motor
and neurocognitive development, and that anthelminthic treatment during pregnancy can
reverse these effects. We used measures which examine infant motor, cognitive and
executive function, including inhibition. We assessed 983 Ugandan infants aged 15 months,
using locally appropriate measures within the Entebbe Mother and Baby Study, a trial of
anthelminthic treatment during pregnancy. Key exposures were maternal worm infections and
anthelminthic treatment during pregnancy. Effects of other health and social factors were
controlled for statistically. Of the five major worm species found in the pregnant women,
two had influences on the developmental measures: Maternal <italic>Mansonella
perstans</italic> and <italic>Strongyloides stercoralis</italic> infections showed
negative associations with the A-not B-task, and Language, respectively. Performance on
other psychomotor and cognitive measures was associated with illnesses during infancy and
infants’ behavior during assessment, but not with maternal worm infections. There were no
positive effects of maternal anthelminthic treatment on infant abilities.
<italic>Mansonella perstans</italic> and <italic>Strongyloides stercoralis</italic>infection during pregnancy seem associated with impaired early executive function and
language, respectively, but single-dose anthelminthic treatment during pregnancy was not
beneficial. The biological mechanisms that could underlie these neurocognitive effects are
discussed. (<italic>JINS</italic>, 2012, <italic>18</italic>, 1019–1030)</p></abstract><kwd-group><title>Keywords</title><kwd>Pregnancy</kwd><kwd>Helminths</kwd><kwd>De-worming</kwd><kwd>Infancy</kwd><kwd>Psychomotor</kwd><kwd>Executive function</kwd></kwd-group><counts><fig-count count="0"></fig-count><table-count count="6"></table-count><page-count count="12"></page-count></counts></article-meta></front><body><sec id="sec1"><title>Introduction</title><p>Early cognitive development underlies individual differences in children's behavior and
academic performance (Cooper & Farran, <xref rid="ref16" ref-type="bibr">1988</xref>; Rohde & Thompson, <xref rid="ref57" ref-type="bibr">2007</xref>; see
Tramontana, Hooper, & Selzer, <xref rid="ref69" ref-type="bibr">1988</xref>, for a
review). In the developing world, poverty, disease and malnutrition inhibit children from
attaining their developmental potential. Several studies suggest that worms, affecting
approximately 90 million school-age children (Brooker, Clements, & Bundy, <xref rid="ref11" ref-type="bibr">2006</xref>), impair cognitive functions (e.g., Boivin et al.,
<xref rid="ref8" ref-type="bibr">1993</xref>; Ezeamama et al., <xref rid="ref25" ref-type="bibr">2005</xref>; Jukes et al., <xref rid="ref38" ref-type="bibr">2002</xref>;
Nokes et al.,<xref rid="ref52" ref-type="bibr">1992</xref>, <xref rid="ref53" ref-type="bibr">1999</xref>; Sakti et al., <xref rid="ref59" ref-type="bibr">1999</xref>).</p><p>Worms also infect approximately a third of pregnant women in Sub-Saharan Africa (Bundy,
Chan, & Savioli, <xref rid="ref12" ref-type="bibr">1987</xref>). We hypothesized
that maternal worm infections might influence the development of cognitive function in
infants. Animal studies suggest that by depleting nutrients available to the fetus, maternal
worm infections may interfere with processes such as myelination and the development of
neurotransmitter systems vital for neurological and cognitive functioning (Beard et al.,
<xref rid="ref6" ref-type="bibr">2007</xref>). Beard et al. (<xref rid="ref5" ref-type="bibr">2005</xref>) found that offspring of iron-deficient rats had lower iron
content, lowered activity in the dopamine transporter system in the caudate nucleus and
substantia nigra, reduced motor activity, and higher anxiety levels than controls. In
humans, dopamine influences the limbic system and frontal cortex: disruptions in the
dopamine system interfere with psychomotor and executive function (Goto & Grace,
<xref rid="ref32" ref-type="bibr">2005</xref>; Smith & Kieval, <xref rid="ref63" ref-type="bibr">2000</xref>). Hence, we postulated that early human executive
function might be particularly vulnerable to effects of maternal worm infections. Executive
function comprises processes involved in goal-directed behavior or planning and consists of
complementary sub-skills including working memory, inhibitory control and attentional
flexibility (Hughes, <xref rid="ref36" ref-type="bibr">1998</xref>; Miyake et al., <xref rid="ref45" ref-type="bibr">2000</xref>).</p><p>Maternal worm infections co-exist with several important potential confounders, such as
maternal under-nutrition (Goldenberg, Hoffman, & Cliver, <xref rid="ref31" ref-type="bibr">1998</xref>; Hack, <xref rid="ref35" ref-type="bibr">1998</xref>), maternal
infections, including HIV and malaria (Gay et al., <xref rid="ref29" ref-type="bibr">1995</xref>; Gentile, Boll, Stagno, & Pass, <xref rid="ref30" ref-type="bibr">1989</xref>) and exposures in infancy including malaria (Dugbartey & Spellacy,
<xref rid="ref21" ref-type="bibr">1997</xref>), recurrent diarrhea (Berkman, Lescano,
Gilman, Lopez, & Black, <xref rid="ref7" ref-type="bibr">2002</xref>), anemia
(Clarke, Grantham-McGregor, & Powell, <xref rid="ref14" ref-type="bibr">1991</xref>;
Lozoff, Brittenham, & Wolf, <xref rid="ref42" ref-type="bibr">1987</xref>),
malnutrition (Galler, Ramsey, Solimano, Kucharski, & Harrison, <xref rid="ref28" ref-type="bibr">1984</xref>; Grantham-McGregor, Powell, Walker, Chang, & Fletcher,
<xref rid="ref33" ref-type="bibr">1994</xref>), and inadequate social stimulation (Bradley
et al., <xref rid="ref10" ref-type="bibr">1989</xref>; Grantham-McGregor, Powell, Walker,
& Himes, <xref rid="ref34" ref-type="bibr">1991</xref>; Ramey & Ramey, <xref rid="ref55" ref-type="bibr">1998</xref>).</p><p>Measuring executive function in young children in resource-limited settings is difficult.
Measures that take into account immature verbal and motor skills and low attentional spans,
and adapted to local conditions, are required (Espy, <xref rid="ref24" ref-type="bibr">2004</xref>). One task designed to test motor inhibition that has been translated and
adapted for various cultures is the A-not-B task. In this test, an object is hidden
repeatedly at location A and then at location B. Infants who persistently search at A show
poor motor inhibition. Devised by Piaget (<xref rid="ref54" ref-type="bibr">1954</xref>) to
study object permanence in infants, initial cognitive explanations regarding this task
focused on short term memory (Schacter, Moscovitch, Tulving, McLachlan, & Freedman,
<xref rid="ref60" ref-type="bibr">1986</xref>). Subsequently, it was suggested that
executive functions were important (Diamond, <xref rid="ref18" ref-type="bibr">1988</xref>;
Diamond & Goldman-Rakic, <xref rid="ref20" ref-type="bibr">1989</xref>): two
meta-analyses of over 100 studies (Marcovitch & Zelazo, <xref rid="ref43" ref-type="bibr">1999</xref>; Wellman, Cross, & Bartsch, <xref rid="ref74" ref-type="bibr">1986</xref>) both proposed that the infant's response is driven by interaction
between representation of the location and inhibition of the motoric tendency to search at
the previous location. Initial findings suggested that younger infants perseverate more than
older infants. Subsequent longitudinal studies (e.g., Clearfield et al., <xref rid="ref15" ref-type="bibr">2006</xref>) showed that at first infants do not perseverate,
that this is followed by a stage of perseveration and then at around 12 months competence on
the task. Thus Clearfield and colleagues argue that performance on A-not-B may be determined
by competition between active (faster) and latent (slower) memory processes, and
perseveration may be a consequence of immaturity in processes that guide application of past
experience. Initially, Thelen and Smith (<xref rid="ref67" ref-type="bibr">1994</xref>)
attributed perseveration to motoric rather than cognitive schemes, but more recently Smith,
Thelen, Titzer, and McLin (<xref rid="ref64" ref-type="bibr">1999</xref>) proposed that
infants’ reaching is guided by a dynamic interplay between cognitive, motor, and
visuospatial systems. While processes that underlie the A-not-B task are yet to be
ascertained, the task covers a wide age-group, is sensitive for even very young infants
(e.g., Clearfield et al., <xref rid="ref15" ref-type="bibr">2006</xref>; Diamond &
Doar, <xref rid="ref19" ref-type="bibr">1989</xref>) and, hence, seems suitable for
measuring early executive function.</p><p>A second important aspect of executive function is delay inhibition. Conflict inhibition
tasks such as A-not-B require inhibiting an inappropriate prepotent response while
activating a conflicting novel response. Delay inhibition tasks (e.g., the Self Control
task) require the child simply to refrain from responding until a given signal, and may be
purer measures of inhibition (Carlson, Davis, & Leach, <xref rid="ref13" ref-type="bibr">2005</xref>).</p><p>Executive function emerges in infancy (Diamond, <xref rid="ref17" ref-type="bibr">1985</xref>; Thompson & Nelson, <xref rid="ref68" ref-type="bibr">2001</xref>), and
is thought to integrate input from several developing systems including attention (Rothbart
& Ahadi, <xref rid="ref58" ref-type="bibr">1994</xref>), memory and language (Kopp,
<xref rid="ref40" ref-type="bibr">1982</xref>), and psychosocial functioning (Londerville
& Main, <xref rid="ref41" ref-type="bibr">1981</xref>; Stayton, Hogan, &
Ainsworth, <xref rid="ref65" ref-type="bibr">1971</xref>). Psychomotor skills, language and
socioemotional skills develop concurrently, but draw less upon executive mechanisms and may
therefore be less affected by maternal worm infections.</p><p>We aimed to examine effects of maternal worm infections and anthelminthic treatment in
pregnancy on motor and cognitive outcomes in infants at age 15 months. Our hypothesis was
that two measures known to have high executive loads (the A-not-B and Delay Inhibition
tasks) would be particularly sensitive to effects of maternal worm infections. In a large
sample, we therefore examined different subtests of a locally appropriate assessment
battery, the Kilifi Developmental Inventory-KDI (Abubakar, Holding, Van Baar, Newton,
& Van de Vijver, 2008), to establish effects of maternal worm infections and their
treatment on infants’ developing executive functions, and other developing cognitive and
psychomotor skills.</p></sec><sec sec-type="methods" id="sec2"><title>Methods</title><sec id="sec2-1" sec-type="general"><title>Design and Participants</title><p>This research was part of the Entebbe Mother and Baby Study (EMaBS), a double-blind
randomized placebo-controlled trial of anthelminthic treatment during pregnancy (Elliott
et al., <xref rid="ref22" ref-type="bibr">2007</xref>). Between 2003 and 2005, a total of
2507 pregnant women were enrolled, investigated for parasitic infections and hemoglobin
level, and randomized to receive albendazole (400 mg) or its matching placebo and
praziquantel (40 mg/kg) or its matching placebo in a 2 × 2 factorial design. Albendazole
treats roundworms (nematodes), and has some antiprotozoal effects. Praziquantel targets
flatworms (trematodes), including schistosomiasis. Neither drug has known effects on
bacterial infections. All mothers including those who had received placebos during
pregnancy were treated effectively soon after delivery.</p><p>Infants underwent psychomotor assessments at 15 months using a modification of the KDI.
Cognitive and social abilities were assessed using additional measures. Of 2507 women
enrolled, there were 2345 live births of whom 1022 children were assessed but 39 were
excluded from analysis because they were not tested within 2 months of age 15 months. Of
those not tested, 94 had died (complications of labor or neonatal sepsis) before reaching
age 15 months (infant mortality was not related to maternal worm infections [unpublished
data] or their treatment [Webb et al., <xref rid="ref73" ref-type="bibr">2011</xref>]),
174 were lost to follow-up, 427 were seen at 15 months before the developmental
assessments were introduced, 628 missed the 15 month visit. Of the 983 children (500 boys)
tested, mean age was 15.59 months (<italic>SD</italic> 0.49; min 14.23 months; max 17
months). Of their mothers, 249 received praziquantel and albendazole; 241 praziquantel and
albendazole-matching placebo; 251 albendazole and praziquantel-matching placebo; and 242
received both placebos.</p></sec><sec id="sec2-2" sec-type="general"><title>Ethics</title><p>This research was approved by the Science and Ethics Committee of the Uganda Virus
Research Institute and the Uganda National Council of Science and Technology. Written
informed consent was obtained from all eligible participants. In 1996, WHO recommended
mass treatment of pregnant women in the second and third trimester with albendazole (400
mg) (WHO, <xref rid="ref75" ref-type="bibr">1996</xref>) in settings with high prevalence
of hookworm and anemia. In 2002, WHO recommended treatment of schistosomiasis with
praziquantel (40 mg/kg) during pregnancy and breast-feeding (WHO, <xref rid="ref76" ref-type="bibr">2002</xref>) but there was limited evidence on the risk-benefit ratio of
this intervention. There was concern that anthelminthic drugs might lead to adverse birth
outcomes (Bradley & Horton, <xref rid="ref9" ref-type="bibr">2001</xref>) and that
among HIV positive women anthelminthic treatment might lead to an increase in HIV load and
increased vertical HIV transmission (Elliott et al., <xref rid="ref23" ref-type="bibr">2003</xref>). Thus a condition of equipoise was considered to exist (Elliott et al.,
<xref rid="ref22" ref-type="bibr">2007</xref>). Indeed, WHO subsequently called for
placebo-controlled trials of praziquantel during pregnancy (WHO, <xref rid="ref77" ref-type="bibr">2006</xref>). Our population had a moderate prevalence of hookworm (45%) and
schistosomiasis (18%) but rates of anemia were relatively low and women with severe anemia
(hemoglobin level less than 8.0 g/dL) were excluded from the study and treated. Hence a
placebo-controlled study design was considered justified.</p></sec><sec id="sec2-3" sec-type="general"><title>Motor and Cognitive Assessments</title><p>We used two executive function measures, the A-not-B task and a Self Control (delay
inhibition) task, previously translated and used in rural Kenya (Abubakar, Holding, Van de
Vijver, Bomu, & Van Baar, <xref rid="ref2" ref-type="bibr">2010</xref>). Infants’
skills on Language, Self Care and Recognition of Self and Others were determined using
parental reports (Abubakar et al., <xref rid="ref2" ref-type="bibr">2010</xref>).
Fine-motor and gross-motor function, and non-task behavior (mood, interaction, and
activity) were assessed using ratings originally developed for the KDI (Abubakar et al.,
<xref rid="ref1" ref-type="bibr">2008</xref>). Details of measures are described below.</p><sec id="sec2-3-1" sec-type="general"><title>Fine Motor</title><p>Control of small hand-movements was assessed using items such as building a tower with
blocks and scribbling with a pen. Twenty-seven items were scored as pass/fail and summed
to give a score.</p></sec><sec id="sec2-3-2" sec-type="general"><title>Gross Motor</title><p>Control of the limbs was assessed using 35 items such as kicking a ball or climbing
onto a platform; a total was calculated.</p></sec><sec id="sec2-3-3" sec-type="general"><title>Child's mood, activity, and interaction</title><p>The assessor observed the child's activity, mood, and level of interaction and rated
them on a six-point scale. High scores indicated good mood, activity, or
interaction.</p></sec><sec id="sec2-3-4" sec-type="general"><title>Self Control (delay inhibition)</title><p>In two trials, a biscuit (trial 1) or wrapped gift (trial 2) was presented to the child
who was instructed not to take it until the assessor had completed what he/she was
doing. Waiting time (in seconds) was recorded to a maximum of 150 s. Average waiting
time for the two trials was computed.</p></sec><sec id="sec2-3-5" sec-type="general"><title>The A-not-B task</title><p>A biscuit was placed in one of two wells as the child watched and both wells were then
covered with opaque cups. The board was taken out of sight for 10 s during which the
child was distracted with a song. The board was then brought back and the child asked to
point to the well with the biscuit. The child was given the biscuit if she or he
successfully located it. The location of the biscuit was switched to the other well
after two consecutive correct responses. Ten trials were given; the number of correct
responses was scored.</p></sec><sec id="sec2-3-6" sec-type="general"><title>Language</title><p>This was assessed by interviewing the mother or guardian, asking whether the infant
produced common pre-speech items such as vowels (e.g., aa, aa), babble (e.g., ma, ma) or
gestures (e.g., waving for “bye’), spoke definite words, or named and identified common
household objects (11 items overall).</p></sec><sec id="sec2-3-7" sec-type="general"><title>Recognition of Self and Others</title><p>The caregiver was asked whether the infant reacted to his/her name, or distinguished
his mother and other familiar people from strangers (altogether 12 items).</p></sec><sec id="sec2-3-8" sec-type="general"><title>Self Care</title><p>The interview collected information about behaviors such as how much the infant helped
during dressing and feeding (15 items).</p></sec><sec id="sec2-3-9" sec-type="general"><title>Piloting, training, and scale reliability</title><p>The measures were translated into Luganda and piloted on 50 children. Seven nurses and
two doctors were trained. To assess reliability, every 10th infant was rated by two
assessors on all measures. Comparisons of 80 paired records showed inter-rater
reliability coefficients ranging from 0.75 to 1.00 (<xref ref-type="table" rid="tab1">Table 1</xref>). Scores showed normal distributions on all measures except Self
Control. Overall psychomotor performance (mean 29.58; <italic>SD</italic> 3.79) was
found to be similar to that of an age-matched sample of Kenyan infants (Abubakar et al.,
<xref rid="ref1" ref-type="bibr">2008</xref>). Internal consistency was examined using
Cronbach's alpha and poorly correlated items were deleted. The edited measures had
internal consistency coefficients ranging from 0.62 to 0.78 (<xref ref-type="table" rid="tab1">Table 1</xref>). Principal component analysis confirmed that motor measures
loaded on one component, cognitive measures on another. There was a negative correlation
(<italic>r</italic> = −0.04; <italic>p</italic> = .26) between the two measures of
executive function (A-not-B and Self Control) which was not statistically significant.
Psychomotor items in the KDI had exhibited high test–retest reliability in the Kenyan
sample suggesting that the tool was stable over time (Abubakar et al., <xref rid="ref1" ref-type="bibr">2008</xref>). These psychometric features are summarized in
<xref ref-type="table" rid="tab1">Table 1</xref>.<table-wrap id="tab1" orientation="portrait" position="float"><label>Table 1</label><caption><p>Inter-rater reliability and internal consistency of the measures and factor
loadings</p></caption><alternatives><graphic xlink:href="S1355617712000768_tab1"></graphic><table frame="hsides" rules="groups"><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><thead><tr><th align="left" rowspan="1" colspan="1">Measure</th><th align="center" rowspan="1" colspan="1">Inter-rater reliability coefficient
<italic>N</italic> = 80</th><th align="center" rowspan="1" colspan="1">Cronbach's alpha <italic>N</italic>= 983</th><th align="center" rowspan="1" colspan="1">Component 1</th><th align="center" rowspan="1" colspan="1">Component 2</th></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1">Fine Motor</td><td align="char" char="." rowspan="1" colspan="1">.71</td><td align="char" char="." rowspan="1" colspan="1">.72</td><td align="char" char="." rowspan="1" colspan="1">.62</td><td align="char" char="." rowspan="1" colspan="1">−.32</td></tr><tr><td align="left" rowspan="1" colspan="1">Gross Motor</td><td align="char" char="." rowspan="1" colspan="1">.77</td><td align="char" char="." rowspan="1" colspan="1">.78</td><td align="char" char="." rowspan="1" colspan="1">.63</td><td align="char" char="." rowspan="1" colspan="1">−.19</td></tr><tr><td align="left" rowspan="1" colspan="1">Language</td><td align="char" char="." rowspan="1" colspan="1">1.00</td><td align="char" char="." rowspan="1" colspan="1">.76</td><td align="char" char="." rowspan="1" colspan="1">.42</td><td align="char" char="." rowspan="1" colspan="1">.70</td></tr><tr><td align="left" rowspan="1" colspan="1">Self Control</td><td align="char" char="." rowspan="1" colspan="1">1.00</td><td align="center" rowspan="1" colspan="1">N/A</td><td align="char" char="." rowspan="1" colspan="1">−.31</td><td align="char" char="." rowspan="1" colspan="1">.60</td></tr><tr><td align="left" rowspan="1" colspan="1">Self Care</td><td align="char" char="." rowspan="1" colspan="1">1.00</td><td align="char" char="." rowspan="1" colspan="1">.64</td><td align="char" char="." rowspan="1" colspan="1">.70</td><td align="char" char="." rowspan="1" colspan="1">.18</td></tr><tr><td align="left" rowspan="1" colspan="1">Self Recognition</td><td align="char" char="." rowspan="1" colspan="1">1.00</td><td align="char" char="." rowspan="1" colspan="1">.62</td><td align="char" char="." rowspan="1" colspan="1">.41</td><td align="char" char="." rowspan="1" colspan="1">.16</td></tr><tr><td align="left" rowspan="1" colspan="1">A not B</td><td align="char" char="." rowspan="1" colspan="1">1.00</td><td align="center" rowspan="1" colspan="1">N/A</td><td align="char" char="." rowspan="1" colspan="1">.27</td><td align="char" char="." rowspan="1" colspan="1">.13</td></tr></tbody></table></alternatives></table-wrap></p></sec></sec><sec id="sec2-4" sec-type="general"><title>Testing Procedure</title><p>Testing at age 15 months was postponed if mother or clinician judged the child to be
unwell. Sessions lasted 45 to 65 min. Short breaks were allowed as judged by the assessor
and mother. After the session, a small age-appropriate gift was given to the child and
transport money reimbursed to the parent.</p></sec><sec id="sec2-5" sec-type="general"><title>Additional Data</title><sec id="sec2-5-1" sec-type="general"><title>Parasitology</title><p>Stool samples of the pregnant women and infants were examined for helminth ova using
Kato Katz technique (Katz, Chaves, & Pellegrino, <xref rid="ref39" ref-type="bibr">1972</xref>), and cultured for <italic>Strongyloides stercoralis</italic>.
Blood was examined for <italic>Mansonella perstans</italic> using the modified Knott's
method (Melrose, Turner, Pisters, & Turner, <xref rid="ref44" ref-type="bibr">2000</xref>) and for malaria parasites using thick smears.</p></sec><sec id="sec2-5-2" sec-type="general"><title>Antenatal history and delivery data</title><p>We recorded information on maternal illnesses, medications and vaccines during
pregnancy, mode of delivery, Apgar score at 10 min, birth weight, congenital
abnormalities, and immunization received at birth.</p></sec><sec id="sec2-5-3" sec-type="general"><title>HIV status of the child</title><p>Overall, 97 mothers tested HIV positive during pregnancy. At 6 weeks of age, their
infants were tested for HIV using DNA and RNA polymerase chain reaction. Specific
management of HIV positive women and exposed children is elaborated elsewhere (Elliott
et al., <xref rid="ref22" ref-type="bibr">2007</xref>; Mpairwe et al., <xref rid="ref47" ref-type="bibr">2005</xref>).</p></sec><sec id="sec2-5-4" sec-type="general"><title>Growth monitoring</title><p>Infants’ weight, height, head circumference, and mid upper arm circumference were
recorded at week 6, 10, and 14, and at 6, 9, and 12 months. At 1 year, hemoglobin levels
were measured.</p></sec><sec id="sec2-5-5" sec-type="general"><title>Illnesses in infancy</title><p>Numbers of episodes of malaria, diarrhea, lower respiratory tract infections, and upper
respiratory tract infections were recorded at the study clinic.</p></sec><sec id="sec2-5-6" sec-type="general"><title>Sociodemographic data</title><p>Sociodemographic data including marital status, gravidity, age, education, occupation,
income, and number of people in the home, were collected at enrolment, by interview.
Household socioeconomic status was derived from items owned, building material of the
house and number of rooms.</p></sec></sec></sec><sec sec-type="results" id="sec3"><title>Results</title><sec id="sec3-1" sec-type="general"><title>Participants’ Characteristics</title><p>Characteristics of the 983 participating mothers and children are summarized in <xref ref-type="table" rid="tab2">Table 2</xref>. Characteristics of mothers of participating
and non-participating children were similar with respect to education, household
socioeconomic status, and prevalence of <italic>Schistosoma mansoni</italic> infection.
However, mothers of participants were older and less likely to be primigravida, and had a
lower prevalence of HIV and hookworm (<italic>p</italic> < .01). Children who
participated had mean birth weight, height and weight for age, and hemoglobin level within
WHO normal ranges.<table-wrap id="tab2" orientation="portrait" position="float"><label>Table 2</label><caption><p>Characteristics of participating women and infants</p></caption><alternatives><graphic xlink:href="S1355617712000768_tab2"></graphic><table frame="hsides" rules="groups"><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><thead><tr><th align="left" rowspan="1" colspan="1"></th><th align="center" rowspan="1" colspan="1"></th><th rowspan="1" align="center" colspan="1">Alb+praz</th><th rowspan="1" align="center" colspan="1">Praziquantel</th><th rowspan="1" align="center" colspan="1">Albendazole</th><th rowspan="1" align="center" colspan="1">Placebos</th><th rowspan="1" align="center" colspan="1">Overall</th><th rowspan="0" align="center" colspan="1"></th></tr><tr><th align="left" rowspan="1" colspan="1">Demographic and clinical
characteristics</th><th align="center" rowspan="1" colspan="1">Treatment arms</th><th align="center" rowspan="1" colspan="1"><italic>N</italic> = 249</th><th align="center" rowspan="1" colspan="1"><italic>N</italic> = 241</th><th align="center" rowspan="1" colspan="1"><italic>N</italic> = 251</th><th align="center" rowspan="1" colspan="1"><italic>N</italic> = 242</th><th align="center" rowspan="1" colspan="1"><italic>N</italic> = 983</th><th align="left" rowspan="1" colspan="1"><italic>p</italic> value</th></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1">Mothers’ age (years)</td><td align="left" rowspan="1" colspan="1">Mean</td><td align="center" rowspan="1" colspan="1">23.9</td><td align="center" rowspan="1" colspan="1">23.9</td><td align="center" rowspan="1" colspan="1">24.4</td><td align="center" rowspan="1" colspan="1">23.2</td><td align="center" rowspan="1" colspan="1">24.1</td><td align="char" char="." rowspan="1" colspan="1">.789</td></tr><tr><td align="left" rowspan="1" colspan="1">Mothers’ education</td><td align="left" rowspan="1" colspan="1">None/primary</td><td align="char" char="(" rowspan="1" colspan="1">141 (56.9)<sup>a</sup></td><td align="char" char="(" rowspan="1" colspan="1">118 (49.2)</td><td align="char" char="(" rowspan="1" colspan="1">141 (56.2)</td><td align="char" char="(" rowspan="1" colspan="1">129 (53.5)</td><td align="char" char="(" rowspan="1" colspan="1">529 (54.0)</td><td align="char" char="." rowspan="1" colspan="1">.325</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Secondary/tertiary</td><td align="char" char="(" rowspan="1" colspan="1">107 (43.1)</td><td align="char" char="(" rowspan="1" colspan="1">122 (50.8)</td><td align="char" char="(" rowspan="1" colspan="1">110 (43.8)</td><td align="char" char="(" rowspan="1" colspan="1">112 (46.5)</td><td align="char" char="(" rowspan="1" colspan="1">451 (46.0)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Household SES</td><td align="left" rowspan="1" colspan="1">Lower</td><td align="char" char="(" rowspan="1" colspan="1">105 (43.0)</td><td align="char" char="(" rowspan="1" colspan="1">113 (47.5)</td><td align="char" char="(" rowspan="1" colspan="1">107 (43.3)</td><td align="char" char="(" rowspan="1" colspan="1">105 (44.5)</td><td align="char" char="(" rowspan="1" colspan="1">430 (44.6)</td><td align="char" char="." rowspan="1" colspan="1">.509</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Upper</td><td align="char" char="(" rowspan="1" colspan="1">139 (57.0)</td><td align="char" char="(" rowspan="1" colspan="1">125 (52.5)</td><td align="char" char="(" rowspan="1" colspan="1">140 (56.7)</td><td align="char" char="(" rowspan="1" colspan="1">131 (55.5)</td><td align="char" char="(" rowspan="1" colspan="1">535 (55.4)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Mothers’ occupation</td><td align="left" rowspan="1" colspan="1">Fishing/farming</td><td align="char" char="(" rowspan="1" colspan="1">10 (3.9)</td><td align="char" char="(" rowspan="1" colspan="1">9 (3.5)</td><td align="char" char="(" rowspan="1" colspan="1">13 (5.1)</td><td align="char" char="(" rowspan="1" colspan="1">11 (4.4)</td><td align="char" char="(" rowspan="1" colspan="1">43 (4.2)</td><td align="char" char="." rowspan="1" colspan="1">.278</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Unskilled manual</td><td align="char" char="(" rowspan="1" colspan="1">20 (7.8)</td><td align="char" char="(" rowspan="1" colspan="1">22 (8.7)</td><td align="char" char="(" rowspan="1" colspan="1">9 (3.5)</td><td align="char" char="(" rowspan="1" colspan="1">11 (4.4)</td><td align="char" char="(" rowspan="1" colspan="1">44 (6.1)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Bar/hotel</td><td align="char" char="(" rowspan="1" colspan="1">10 (3.9)</td><td align="char" char="(" rowspan="1" colspan="1">7 (2.8)</td><td align="char" char="(" rowspan="1" colspan="1">16 (6.2)</td><td align="char" char="(" rowspan="1" colspan="1">11 (4.4)</td><td align="char" char="(" rowspan="1" colspan="1">44 (4.3)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">housewife</td><td align="char" char="(" rowspan="1" colspan="1">169 (61.9)</td><td align="char" char="(" rowspan="1" colspan="1">174 (68.5)</td><td align="char" char="(" rowspan="1" colspan="1">166 (64.6)</td><td align="char" char="(" rowspan="1" colspan="1">167 (67.1)</td><td align="char" char="(" rowspan="1" colspan="1">666 (65.5)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">business</td><td align="char" char="(" rowspan="1" colspan="1">32 (12.5)</td><td align="char" char="(" rowspan="1" colspan="1">25 (9.8)</td><td align="char" char="(" rowspan="1" colspan="1">33 (12.5)</td><td align="char" char="(" rowspan="1" colspan="1">35 (14.1)</td><td align="char" char="(" rowspan="1" colspan="1">125 (12.3)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">student</td><td align="char" char="(" rowspan="1" colspan="1">6 (2.3)</td><td align="char" char="(" rowspan="1" colspan="1">5 (2.0)</td><td align="char" char="(" rowspan="1" colspan="1">5 (1.9)</td><td align="char" char="(" rowspan="1" colspan="1">1 (.4)</td><td align="char" char="(" rowspan="1" colspan="1">17 (1.7)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">professional</td><td align="char" char="(" rowspan="1" colspan="1">20 (7.8)</td><td align="char" char="(" rowspan="1" colspan="1">12 (4.7)</td><td align="char" char="(" rowspan="1" colspan="1">15 (5.8)</td><td align="char" char="(" rowspan="1" colspan="1">13 (5.2)</td><td align="char" char="(" rowspan="1" colspan="1">60 (5.9)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Fathers’ occupation</td><td align="left" rowspan="1" colspan="1">None</td><td align="char" char="(" rowspan="1" colspan="1">2 (.8)</td><td align="char" char="(" rowspan="1" colspan="1">2 (.8)</td><td align="char" char="(" rowspan="1" colspan="1">3 (1.2)</td><td align="char" char="(" rowspan="1" colspan="1">3 (2.1)</td><td align="char" char="(" rowspan="1" colspan="1">5 (1.2)</td><td align="char" char="." rowspan="1" colspan="1">.859</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Farmer/fishing</td><td align="char" char="(" rowspan="1" colspan="1">29 (12.2)</td><td align="char" char="(" rowspan="1" colspan="1">37 (15.4)</td><td align="char" char="(" rowspan="1" colspan="1">30 (12.1)</td><td align="char" char="(" rowspan="1" colspan="1">29 (12.2)</td><td align="char" char="(" rowspan="1" colspan="1">125 (13.0)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Unskilled manual</td><td align="char" char="(" rowspan="1" colspan="1">81 (34.2)</td><td align="char" char="(" rowspan="1" colspan="1">84 (35.0)</td><td align="char" char="(" rowspan="1" colspan="1">74 (30.0)</td><td align="char" char="(" rowspan="1" colspan="1">81 (34.0)</td><td align="char" char="(" rowspan="1" colspan="1">320 (33.3)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Bar/hotel</td><td align="char" char="(" rowspan="1" colspan="1">6 (2.5)</td><td align="char" char="(" rowspan="1" colspan="1">2 (.8)</td><td align="char" char="(" rowspan="1" colspan="1">3 (1.2)</td><td align="char" char="(" rowspan="1" colspan="1">3 (1.3)</td><td align="char" char="(" rowspan="1" colspan="1">14 (1.5)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Business</td><td align="char" char="(" rowspan="1" colspan="1">37 (15.6)</td><td align="char" char="(" rowspan="1" colspan="1">33 (13.8)</td><td align="char" char="(" rowspan="1" colspan="1">40 (16.2)</td><td align="char" char="(" rowspan="1" colspan="1">41 (17.2)</td><td align="char" char="(" rowspan="1" colspan="1">151 (15.7)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Student</td><td align="char" char="(" rowspan="1" colspan="1">4 (1.7)</td><td align="char" char="(" rowspan="1" colspan="1">6 (2.5)</td><td align="char" char="(" rowspan="1" colspan="1">3 (1.2)</td><td align="char" char="(" rowspan="1" colspan="1">3 (1.3)</td><td align="char" char="(" rowspan="1" colspan="1">16 (1.7)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Professional</td><td align="char" char="(" rowspan="1" colspan="1">78 (32.9)</td><td align="char" char="(" rowspan="1" colspan="1">76 (31.7)</td><td align="char" char="(" rowspan="1" colspan="1">94 (38.1)</td><td align="char" char="(" rowspan="1" colspan="1">76 (31.9)</td><td align="char" char="(" rowspan="1" colspan="1">324 (33.7)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Mothers’ income</td><td align="left" rowspan="1" colspan="1"><30,000 (£10)</td><td align="char" char="(" rowspan="1" colspan="1">208 (82.5)</td><td align="char" char="(" rowspan="1" colspan="1">208 (83.9)</td><td align="char" char="(" rowspan="1" colspan="1">212 (85.1)</td><td align="char" char="(" rowspan="1" colspan="1">216 (88.2)</td><td align="char" char="(" rowspan="1" colspan="1">844 (84.9)</td><td align="char" char="." rowspan="1" colspan="1">.096</td></tr><tr><td align="left" rowspan="1" colspan="1">(Uganda Shillings)</td><td align="left" rowspan="1" colspan="1">30,000–60,000</td><td align="char" char="(" rowspan="1" colspan="1">31 (12.3)</td><td align="char" char="(" rowspan="1" colspan="1">28 (11.3)</td><td align="char" char="(" rowspan="1" colspan="1">15 (6.0)</td><td align="char" char="(" rowspan="1" colspan="1">20 (8.2)</td><td align="char" char="(" rowspan="1" colspan="1">94 (9.5)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">60,001–100,000</td><td align="char" char="(" rowspan="1" colspan="1">7 (2.8)</td><td align="char" char="(" rowspan="1" colspan="1">4 (1.6)</td><td align="char" char="(" rowspan="1" colspan="1">11 (4.4)</td><td align="char" char="(" rowspan="1" colspan="1">4 (1.6)</td><td align="char" char="(" rowspan="1" colspan="1">26 (2.6)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">>100,000</td><td align="char" char="(" rowspan="1" colspan="1">6 (2.4)</td><td align="char" char="(" rowspan="1" colspan="1">8 (3.2)</td><td align="char" char="(" rowspan="1" colspan="1">11 (4.4)</td><td align="char" char="(" rowspan="1" colspan="1">5 (2.0)</td><td align="char" char="(" rowspan="1" colspan="1">30 (3.0)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Family size</td><td align="left" rowspan="1" colspan="1">mean</td><td align="center" rowspan="1" colspan="1">3.8</td><td align="center" rowspan="1" colspan="1">4.0</td><td align="center" rowspan="1" colspan="1">3.79</td><td align="center" rowspan="1" colspan="1">3.77</td><td align="center" rowspan="1" colspan="1">3.84</td><td align="char" char="." rowspan="1" colspan="1">.602</td></tr><tr><td align="left" rowspan="1" colspan="1">Mothers’ HIV status</td><td align="left" rowspan="1" colspan="1">Positive</td><td align="char" char="(" rowspan="1" colspan="1">22 (8.8)</td><td align="char" char="(" rowspan="1" colspan="1">19 (7.9)</td><td align="char" char="(" rowspan="1" colspan="1">26 (10.4)</td><td align="char" char="(" rowspan="1" colspan="1">25 (10.3)</td><td align="char" char="(" rowspan="1" colspan="1">92 (9.4)</td><td align="char" char="." rowspan="1" colspan="1">.973</td></tr><tr><td align="left" rowspan="1" colspan="1">Mothers’ gravidity</td><td align="left" rowspan="1" colspan="1">Primigravida</td><td align="char" char="(" rowspan="1" colspan="1">72 (28.9)</td><td align="char" char="(" rowspan="1" colspan="1">61 (25.3)</td><td align="char" char="(" rowspan="1" colspan="1">59 (23.5)</td><td align="char" char="(" rowspan="1" colspan="1">54 (22.3)</td><td align="char" char="(" rowspan="1" colspan="1">246 (25.0)</td><td align="char" char="." rowspan="1" colspan="1">.310</td></tr><tr><td align="left" rowspan="1" colspan="1">Mothers’ hookworm status</td><td align="left" rowspan="1" colspan="1">Positive</td><td align="char" char="(" rowspan="1" colspan="1">108 (43.7)</td><td align="char" char="(" rowspan="1" colspan="1">111 (46.0)</td><td align="char" char="(" rowspan="1" colspan="1">89 (35.7)</td><td align="char" char="(" rowspan="1" colspan="1">97 (40.1)</td><td align="char" char="(" rowspan="1" colspan="1">405 (41.4)</td><td align="char" char="." rowspan="1" colspan="1">.150</td></tr><tr><td align="left" rowspan="1" colspan="1">Mother's <italic>S. mansoni</italic>status</td><td align="left" rowspan="1" colspan="1">Positive</td><td align="char" char="(" rowspan="1" colspan="1">44 (17.8)</td><td align="char" char="(" rowspan="1" colspan="1">50 (20.8)</td><td align="char" char="(" rowspan="1" colspan="1">47 (18.9)</td><td align="char" char="(" rowspan="1" colspan="1">46 (19.0)</td><td align="char" char="(" rowspan="1" colspan="1">187 (19.1)</td><td align="char" char="." rowspan="1" colspan="1">.857</td></tr><tr><td align="left" rowspan="1" colspan="1">Sex of the child</td><td align="left" rowspan="1" colspan="1">Female</td><td align="char" char="(" rowspan="1" colspan="1">110 (44.2)</td><td align="char" char="(" rowspan="1" colspan="1">127 (52.7)</td><td align="char" char="(" rowspan="1" colspan="1">122 (48.6)</td><td align="char" char="(" rowspan="1" colspan="1">124 (51.2)</td><td align="char" char="(" rowspan="1" colspan="1">483 (49.1)</td><td align="char" char="." rowspan="1" colspan="1">.122</td></tr><tr><td align="left" rowspan="1" colspan="1">Age of the child (months)</td><td align="left" rowspan="1" colspan="1">Mean (<italic>SD</italic>)</td><td align="char" char="(" rowspan="1" colspan="1">15.6 (.50)</td><td align="char" char="(" rowspan="1" colspan="1">15.6 (.50)</td><td align="char" char="(" rowspan="1" colspan="1">15.6 (.50)</td><td align="char" char="(" rowspan="1" colspan="1">15.6 (.50)</td><td align="char" char="(" rowspan="1" colspan="1">15.6 (.50)</td><td align="char" char="." rowspan="1" colspan="1">.561</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Min.</td><td align="center" rowspan="1" colspan="1">14.2</td><td align="center" rowspan="1" colspan="1">14.3</td><td align="center" rowspan="1" colspan="1">15.1</td><td align="center" rowspan="1" colspan="1">15.0</td><td align="center" rowspan="1" colspan="1">14.2</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Max.</td><td align="center" rowspan="1" colspan="1">17.0</td><td align="center" rowspan="1" colspan="1">17.0</td><td align="center" rowspan="1" colspan="1">17.0</td><td align="center" rowspan="1" colspan="1">16.9</td><td align="center" rowspan="1" colspan="1">17.00</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Gestation age at birth</td><td align="left" rowspan="1" colspan="1">full term (≥38 wks)</td><td align="center" rowspan="1" colspan="1">240</td><td align="center" rowspan="1" colspan="1">234</td><td align="center" rowspan="1" colspan="1">245</td><td align="center" rowspan="1" colspan="1">233</td><td align="center" rowspan="1" colspan="1">952</td><td align="char" char="." rowspan="1" colspan="1">.212</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">preterm</td><td align="center" rowspan="1" colspan="1">8</td><td align="center" rowspan="1" colspan="1">6</td><td align="center" rowspan="1" colspan="1">6</td><td align="center" rowspan="1" colspan="1">6</td><td align="center" rowspan="1" colspan="1">26</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Gestation age in weeks</td><td align="left" rowspan="1" colspan="1">Mean (<italic>SD</italic>)</td><td align="char" char="(" rowspan="1" colspan="1">39.30 (3.41)</td><td align="char" char="(" rowspan="1" colspan="1">39.29 (3.64)</td><td align="char" char="(" rowspan="1" colspan="1">39.68 (3.23)</td><td align="char" char="(" rowspan="1" colspan="1">39.46 (3.48)</td><td align="char" char="(" rowspan="1" colspan="1">39.42 (3.44)</td><td align="char" char="." rowspan="1" colspan="1">.558</td></tr><tr><td align="left" rowspan="1" colspan="1">Birth weight (kg)</td><td align="left" rowspan="1" colspan="1">Mean (<italic>SD</italic>)</td><td align="char" char="(" rowspan="1" colspan="1">3.11 (.47)</td><td align="char" char="(" rowspan="1" colspan="1">3.15 (.48)</td><td align="char" char="(" rowspan="1" colspan="1">3.21 (.48)</td><td align="char" char="(" rowspan="1" colspan="1">3.21 (.50)</td><td align="char" char="(" rowspan="1" colspan="1">3.17 (.48)</td><td align="char" char="." rowspan="1" colspan="1">.172</td></tr><tr><td align="left" rowspan="1" colspan="1">Apgar Score at 10 minutes</td><td align="left" rowspan="1" colspan="1">Mean (<italic>SD</italic>)</td><td align="char" char="(" rowspan="1" colspan="1">9.82 (.54)</td><td align="char" char="(" rowspan="1" colspan="1">9.68 (.53)</td><td align="char" char="(" rowspan="1" colspan="1">9.83 (.59)</td><td align="char" char="(" rowspan="1" colspan="1">9.77 (.65)</td><td align="char" char="(" rowspan="1" colspan="1">9.77 (.71)</td><td align="char" char="." rowspan="1" colspan="1">.172</td></tr><tr><td align="left" rowspan="1" colspan="1">Weight at 15 months (kg)</td><td align="left" rowspan="1" colspan="1">Mean (<italic>SD</italic>)</td><td align="char" char="(" rowspan="1" colspan="1">9.56 (1.18)</td><td align="char" char="(" rowspan="1" colspan="1">9.55 (1.19)</td><td align="char" char="(" rowspan="1" colspan="1">9.63 (1.38)</td><td align="char" char="(" rowspan="1" colspan="1">9.64 (1.27)</td><td align="char" char="(" rowspan="1" colspan="1">9.59 (1.26)</td><td align="char" char="." rowspan="1" colspan="1">.740</td></tr><tr><td align="left" rowspan="1" colspan="1">Height at 15 months (cm)</td><td align="left" rowspan="1" colspan="1">Mean (<italic>SD</italic>)</td><td align="char" char="(" rowspan="1" colspan="1">75.51 (3.26)</td><td align="char" char="(" rowspan="1" colspan="1">75.54 (3.61)</td><td align="char" char="(" rowspan="1" colspan="1">75.73 (3.31)</td><td align="char" char="(" rowspan="1" colspan="1">75.66 (3.11)</td><td align="char" char="(" rowspan="1" colspan="1">75.61 (3.33)</td><td align="char" char="." rowspan="1" colspan="1">.813</td></tr><tr><td align="left" rowspan="1" colspan="1">Infant hemoglobin (g/dL)</td><td align="left" rowspan="1" colspan="1">Mean (<italic>SD</italic>)</td><td align="char" char="(" rowspan="1" colspan="1">10.06 (1.37)</td><td align="char" char="(" rowspan="1" colspan="1">10.05 (1.34)</td><td align="char" char="(" rowspan="1" colspan="1">10.10 (1.48)</td><td align="char" char="(" rowspan="1" colspan="1">10.28 (1.45)</td><td align="char" char="(" rowspan="1" colspan="1">10.12 (1.41)</td><td align="char" char="." rowspan="1" colspan="1">.334</td></tr></tbody></table></alternatives><table-wrap-foot><fn><p><sup>a</sup>Figures are proportions (percent) unless otherwise indicated.</p></fn></table-wrap-foot></table-wrap></p></sec><sec id="sec3-2" sec-type="general"><title>Descriptive Statistics for Psychomotor and Cognitive Measures</title><p>Descriptive statistics for the various measures are summarized in <xref ref-type="table" rid="tab3">Table 3</xref>. The numbers of infants who completed the tasks varied. Fewer
completed the A-not-B task because they cried for the treat on the first trial and refused
to continue. Scores on five of the seven measures were normally distributed. Performance
on Self Control was slightly positively skewed and Recognition of Self and Others was
negatively skewed. Appropriate transformations were conducted before analysis.<table-wrap id="tab3" orientation="portrait" position="float"><label>Table 3</label><caption><p>Descriptive statistics of infants’ scores on the various measures</p></caption><alternatives><graphic xlink:href="S1355617712000768_tab3"></graphic><table frame="hsides" rules="groups"><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><thead><tr><th align="left" rowspan="1" colspan="1">Domain</th><th align="center" rowspan="1" colspan="1"><italic>N</italic></th><th align="center" rowspan="1" colspan="1">Min</th><th align="center" rowspan="1" colspan="1">Max. (max. possible)</th><th align="center" rowspan="1" colspan="1">Mean</th><th align="center" rowspan="1" colspan="1"><italic>SD</italic></th></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1">Fine Motor</td><td align="char" char="." rowspan="1" colspan="1">978</td><td align="char" char="." rowspan="1" colspan="1">1</td><td align="char" char="(" rowspan="1" colspan="1">22 (32)</td><td align="char" char="." rowspan="1" colspan="1">13.16</td><td align="char" char="." rowspan="1" colspan="1">1.74</td></tr><tr><td align="left" rowspan="1" colspan="1">Gross Motor</td><td align="char" char="." rowspan="1" colspan="1">982</td><td align="char" char="." rowspan="1" colspan="1">12</td><td align="char" char="(" rowspan="1" colspan="1">25 (35)</td><td align="char" char="." rowspan="1" colspan="1">17.62</td><td align="char" char="." rowspan="1" colspan="1">2.32</td></tr><tr><td align="left" rowspan="1" colspan="1">Language</td><td align="char" char="." rowspan="1" colspan="1">983</td><td align="char" char="." rowspan="1" colspan="1">1</td><td align="char" char="(" rowspan="1" colspan="1">22 (22)</td><td align="char" char="." rowspan="1" colspan="1">15.39</td><td align="char" char="." rowspan="1" colspan="1">4.29</td></tr><tr><td align="left" rowspan="1" colspan="1">Self Control</td><td align="char" char="." rowspan="1" colspan="1">832</td><td align="char" char="." rowspan="1" colspan="1">1</td><td align="char" char="(" rowspan="1" colspan="1">150 (150)</td><td align="char" char="." rowspan="1" colspan="1">6.60</td><td align="char" char="." rowspan="1" colspan="1">17.55</td></tr><tr><td align="left" rowspan="1" colspan="1">Self Care</td><td align="char" char="." rowspan="1" colspan="1">982</td><td align="char" char="." rowspan="1" colspan="1">0</td><td align="char" char="(" rowspan="1" colspan="1">29 (30)</td><td align="char" char="." rowspan="1" colspan="1">17.14</td><td align="char" char="." rowspan="1" colspan="1">4.22</td></tr><tr><td align="left" rowspan="1" colspan="1">Self Recognition</td><td align="char" char="." rowspan="1" colspan="1">982</td><td align="char" char="." rowspan="1" colspan="1">0</td><td align="char" char="(" rowspan="1" colspan="1">18 (24)</td><td align="char" char="." rowspan="1" colspan="1">10.25</td><td align="char" char="." rowspan="1" colspan="1">.99</td></tr><tr><td align="left" rowspan="1" colspan="1">A not B task</td><td align="char" char="." rowspan="1" colspan="1">792</td><td align="char" char="." rowspan="1" colspan="1">0</td><td align="char" char="(" rowspan="1" colspan="1">10 (10)</td><td align="char" char="." rowspan="1" colspan="1">4.01</td><td align="char" char="." rowspan="1" colspan="1">2.36</td></tr></tbody></table></alternatives><table-wrap-foot><fn><p><italic>Note.</italic> The numbers under each domain are discrete scores therefore
no units are available.</p></fn></table-wrap-foot></table-wrap></p></sec><sec id="sec3-3" sec-type="general"><title>Prevalence of Worms in Mothers</title><p>Prevalence of worm species identified in the mothers is shown in <xref ref-type="table" rid="tab4">Table 4</xref>. Hookworm had the highest prevalence followed by
<italic>Mansonella perstans</italic>. Thirty percent of mothers had mixed infections
with some women having up to five species of worms. A total of 352 (34.9%) women did not
have any worm. Only effects of maternal worms with at least 2% prevalence were
subsequently analyzed.<table-wrap id="tab4" orientation="portrait" position="float"><label>Table 4</label><caption><p>Prevalence of the various worms in the pregnant women whose infants were assessed
on the motor and cognitive measures at 15 months</p></caption><alternatives><graphic xlink:href="S1355617712000768_tab4"></graphic><table frame="hsides" rules="groups"><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><thead><tr><th align="left" rowspan="1" colspan="1">Worm species</th><th align="center" rowspan="1" colspan="1">Infected <italic>N</italic> (%)</th></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1">Hookworm</td><td align="char" char="(" rowspan="1" colspan="1">405 (41)</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Mansonella perstans</italic></td><td align="char" char="(" rowspan="1" colspan="1">192 (20)</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Schistosoma mansoni</italic></td><td align="char" char="(" rowspan="1" colspan="1">187 (19)</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Strongyloides stercoralis</italic></td><td align="char" char="(" rowspan="1" colspan="1">123 (13)</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Trichuris trichiura</italic></td><td align="char" char="(" rowspan="1" colspan="1">84 (9)</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Ascaris lumbricoides</italic></td><td align="char" char="(" rowspan="1" colspan="1">21 (2)</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Trichostrongylus</italic></td><td align="char" char="(" rowspan="1" colspan="1">6 (.60)</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Hymenolepsis nana</italic></td><td align="char" char="(" rowspan="1" colspan="1">2 (.20)</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Fasciola hepaticus</italic></td><td align="char" char="(" rowspan="1" colspan="1">1 (.10)</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Dicrocoelium dendriticum</italic></td><td align="char" char="(" rowspan="1" colspan="1">1 (.10)</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Enterobius vermicularis</italic></td><td align="char" char="(" rowspan="1" colspan="1">1 (.10)</td></tr></tbody></table></alternatives></table-wrap></p></sec><sec id="sec3-4" sec-type="general"><title>Effects of Albendazole and Praziquantel</title><p><italic>T</italic> tests were used to compare performance between children born to treated
versus untreated mothers first across the whole sample to assess the benefit of mass
treatment, and then just those where the mothers had worms susceptible to the drugs. We
found no interactions between albendazole and praziquantel (<italic>p</italic> >
.05). Therefore, the effect of each drug was examined separately (albendazole
<italic>vs</italic>. placebo; praziquantel <italic>vs</italic>. placebo). Overall neither
albendazole nor praziquantel had significant effects on developmental outcomes (all values
of <italic>p</italic> > .05). Of note, after delivery stool analysis showed a
significant decline of the prevalence of hookworm and schistosomiasis among albendazole or
praziquantel-treated women, respectively, but no reductions in <italic>Mansonella
perstans</italic>, <italic>Trichuris trichiura</italic>, and <italic>Strongyloides
stercoralis</italic> (Ndibazza et al., <xref rid="ref51" ref-type="bibr">2010</xref>).</p><p>We found, however, a significant effect of praziquantel on the A-not-B task and Self
Control in children whose mothers were infected with schistosomiasis during pregnancy.
Children whose mothers were treated for schistosomiasis during pregnancy performed better
on Self Control than those who were not treated [<italic>t</italic>(140) = 2.58; mean
difference = 5.96; <italic>p</italic> = .01; Cohen's d = 0.47]. However for the A-not-B
task, children whose mothers were treated performed more poorly than those whose mothers
were not treated [<italic>t</italic>(145) = −2.23; mean difference = −0.93;
<italic>p</italic> = .03; Cohen's d = .37]. We found no effect of albendazole among
infants of mothers with the principal susceptible species, hookworm.</p></sec></sec><sec id="sec4"><title>Associations Between Maternal Worm Infections And Other Exposures, And Infant Outcomes</title><sec id="sec4-1" sec-type="general"><title>Raw Correlations</title><p>First, raw correlations between child test scores and exposure variables were explored to
identify factors that might mediate or mask effects of maternal worm infections. Maternal
worms included were <italic>Schistosoma mansoni</italic>, hookworm, <italic>Mansonella
perstans, Ascaris lumbricoides, Trichuris trichiura,</italic> and <italic>Strongyloides
stercoralis</italic>.</p><p>Background factors included were mother's age, education, occupation, income, gravidity,
HIV status, and hemoglobin at enrolment; household socioeconomic status, family size and
father's occupation; and the child's sex, gestational age at birth, birth weight, Apgar
score at 10 min, malaria, diarrhea, and respiratory infections in the first year,
activity, mood and interaction level during assessment, hemoglobin, weight, and height.
These correlations and regressions were examined across the entire sample irrespective of
treatment status since neither treatment showed any overall effect.</p><p>Three maternal worms showed correlations with the infant test scores:
<italic>Strongyloides stercoralis</italic> correlated positively (in the opposite to
expected direction) with scores on Self Control and negatively with Language.
<italic>Trichuris trichiura</italic> and <italic>Mansonella perstans</italic> correlated
negatively with scores on the A-not-B task. Other factors variably correlated with
performance on the motor and cognitive measures. Of 112 correlations calculated, 34 were
significant at the 0.05 cutoff, even after adjusting for multiple comparisons with false
discovery rate. Only exposures with at least one significant correlation with the outcomes
are shown in <xref ref-type="table" rid="tab5">Table 5</xref>.<table-wrap id="tab5" orientation="portrait" position="float"><label>Table 5</label><caption><p>Pearson correlations between maternal worms and other health and sociodemographic
exposures, and the outcomes</p></caption><alternatives><graphic xlink:href="S1355617712000768_tab5"></graphic><table frame="hsides" rules="groups"><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><thead><tr><th align="left" rowspan="1" colspan="1"></th><th align="center" rowspan="1" colspan="1">Fine Motor</th><th align="center" rowspan="1" colspan="1">Gross Motor</th><th align="center" rowspan="1" colspan="1">Language</th><th align="center" rowspan="1" colspan="1">Sociocognition</th><th align="center" rowspan="1" colspan="1">Self Care</th><th align="center" rowspan="1" colspan="1">A not B</th><th align="center" rowspan="1" colspan="1">Self Control</th></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1">Maternal worms in pregnancy</td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Trichuris trichiura</italic></td><td align="char" char="." rowspan="1" colspan="1">.08</td><td align="char" char="." rowspan="1" colspan="1">−.07</td><td align="char" char="." rowspan="1" colspan="1">−.07</td><td align="char" char="." rowspan="1" colspan="1">−.04</td><td align="char" char="." rowspan="1" colspan="1">−.05</td><td align="char" char="." rowspan="1" colspan="1">−.14*</td><td align="char" char="." rowspan="1" colspan="1">.01</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Strongyloides stercoralis</italic></td><td align="char" char="." rowspan="1" colspan="1">.09</td><td align="char" char="." rowspan="1" colspan="1">−.03</td><td align="char" char="." rowspan="1" colspan="1">−.14*</td><td align="char" char="." rowspan="1" colspan="1">−.03</td><td align="char" char="." rowspan="1" colspan="1">−.04</td><td align="char" char="." rowspan="1" colspan="1">.03</td><td align="char" char="." rowspan="1" colspan="1">.18**</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Mansonella perstans</italic></td><td align="char" char="." rowspan="1" colspan="1">.07</td><td align="char" char="." rowspan="1" colspan="1">−.01</td><td align="char" char="." rowspan="1" colspan="1">−.04</td><td align="char" char="." rowspan="1" colspan="1">.07</td><td align="char" char="." rowspan="1" colspan="1">−.04</td><td align="char" char="." rowspan="1" colspan="1">−.20**</td><td align="char" char="." rowspan="1" colspan="1">.00</td></tr><tr><td align="left" rowspan="1" colspan="1">Maternal & birth related
factors</td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Maternal income</td><td align="char" char="." rowspan="1" colspan="1">.10</td><td align="char" char="." rowspan="1" colspan="1">.13*</td><td align="char" char="." rowspan="1" colspan="1">.12</td><td align="char" char="." rowspan="1" colspan="1">.04</td><td align="char" char="." rowspan="1" colspan="1">.08</td><td align="char" char="." rowspan="1" colspan="1">.06</td><td align="char" char="." rowspan="1" colspan="1">−.03</td></tr><tr><td align="left" rowspan="1" colspan="1">Maternal education</td><td align="char" char="." rowspan="1" colspan="1">−.14*</td><td align="char" char="." rowspan="1" colspan="1">−.13*</td><td align="char" char="." rowspan="1" colspan="1">.10</td><td align="char" char="." rowspan="1" colspan="1">−.03</td><td align="char" char="." rowspan="1" colspan="1">−.03</td><td align="char" char="." rowspan="1" colspan="1">.10</td><td align="char" char="." rowspan="1" colspan="1">−.05</td></tr><tr><td align="left" rowspan="1" colspan="1">Maternal occupation</td><td align="char" char="." rowspan="1" colspan="1">−.01</td><td align="char" char="." rowspan="1" colspan="1">−.004</td><td align="char" char="." rowspan="1" colspan="1">.03</td><td align="char" char="." rowspan="1" colspan="1">.08</td><td align="char" char="." rowspan="1" colspan="1">−.03</td><td align="char" char="." rowspan="1" colspan="1">−.09</td><td align="char" char="." rowspan="1" colspan="1">−.01</td></tr><tr><td align="left" rowspan="1" colspan="1">Father's occupation</td><td align="char" char="." rowspan="1" colspan="1">−.07</td><td align="char" char="." rowspan="1" colspan="1">.12</td><td align="char" char="." rowspan="1" colspan="1">−.03</td><td align="char" char="." rowspan="1" colspan="1">−.11</td><td align="char" char="." rowspan="1" colspan="1">.02</td><td align="char" char="." rowspan="1" colspan="1">.07</td><td align="char" char="." rowspan="1" colspan="1">−.10</td></tr><tr><td align="left" rowspan="1" colspan="1">Household SES</td><td align="char" char="." rowspan="1" colspan="1">−.03</td><td align="char" char="." rowspan="1" colspan="1">−.03</td><td align="char" char="." rowspan="1" colspan="1">.16*</td><td align="char" char="." rowspan="1" colspan="1">−.10</td><td align="char" char="." rowspan="1" colspan="1">.02</td><td align="char" char="." rowspan="1" colspan="1">.08</td><td align="char" char="." rowspan="1" colspan="1">.01</td></tr><tr><td align="left" rowspan="1" colspan="1">HIV exposure</td><td align="char" char="." rowspan="1" colspan="1">.18**</td><td align="char" char="." rowspan="1" colspan="1">−.12</td><td align="char" char="." rowspan="1" colspan="1">.05</td><td align="char" char="." rowspan="1" colspan="1">−.02</td><td align="char" char="." rowspan="1" colspan="1">−.01</td><td align="char" char="." rowspan="1" colspan="1">.07</td><td align="char" char="." rowspan="1" colspan="1">−.05</td></tr><tr><td align="left" rowspan="1" colspan="1">Mother's hemoglobin</td><td align="char" char="." rowspan="1" colspan="1">−.15*</td><td align="char" char="." rowspan="1" colspan="1">.10</td><td align="char" char="." rowspan="1" colspan="1">−.01</td><td align="char" char="." rowspan="1" colspan="1">−.05</td><td align="char" char="." rowspan="1" colspan="1">.09</td><td align="char" char="." rowspan="1" colspan="1">−.01</td><td align="char" char="." rowspan="1" colspan="1">−.05</td></tr><tr><td align="left" rowspan="1" colspan="1">Gestation age</td><td align="char" char="." rowspan="1" colspan="1">−.06</td><td align="char" char="." rowspan="1" colspan="1">.09**</td><td align="char" char="." rowspan="1" colspan="1">.06</td><td align="char" char="." rowspan="1" colspan="1">−.05</td><td align="char" char="." rowspan="1" colspan="1">−.02</td><td align="char" char="." rowspan="1" colspan="1">.04</td><td align="char" char="." rowspan="1" colspan="1">−.07</td></tr><tr><td align="left" rowspan="1" colspan="1">Gender</td><td align="char" char="." rowspan="1" colspan="1">.01</td><td align="char" char="." rowspan="1" colspan="1">−.12</td><td align="char" char="." rowspan="1" colspan="1">−.14*</td><td align="char" char="." rowspan="1" colspan="1">.12</td><td align="char" char="." rowspan="1" colspan="1">.03</td><td align="char" char="." rowspan="1" colspan="1">−.06</td><td align="char" char="." rowspan="1" colspan="1">.01</td></tr><tr><td align="left" rowspan="1" colspan="1">Nutritional factors</td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Weight at 15 months</td><td align="char" char="." rowspan="1" colspan="1">−.02</td><td align="char" char="." rowspan="1" colspan="1">.23**</td><td align="char" char="." rowspan="1" colspan="1">.07</td><td align="char" char="." rowspan="1" colspan="1">−.07</td><td align="char" char="." rowspan="1" colspan="1">.08</td><td align="char" char="." rowspan="1" colspan="1">.00</td><td align="char" char="." rowspan="1" colspan="1">−.05</td></tr><tr><td align="left" rowspan="1" colspan="1">Height at 15 months</td><td align="char" char="." rowspan="1" colspan="1">−.13</td><td align="char" char="." rowspan="1" colspan="1">.17**</td><td align="char" char="." rowspan="1" colspan="1">.06</td><td align="char" char="." rowspan="1" colspan="1">−.10</td><td align="char" char="." rowspan="1" colspan="1">.01</td><td align="char" char="." rowspan="1" colspan="1">−.02</td><td align="char" char="." rowspan="1" colspan="1">−.10</td></tr><tr><td align="left" rowspan="1" colspan="1">MUAC</td><td align="char" char="." rowspan="1" colspan="1">.05</td><td align="char" char="." rowspan="1" colspan="1">.13*</td><td align="char" char="." rowspan="1" colspan="1">.14*</td><td align="char" char="." rowspan="1" colspan="1">−.04</td><td align="char" char="." rowspan="1" colspan="1">.05</td><td align="char" char="." rowspan="1" colspan="1">−.02</td><td align="char" char="." rowspan="1" colspan="1">−.06</td></tr><tr><td align="left" rowspan="1" colspan="1">Infections</td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Malaria episodes</td><td align="char" char="." rowspan="1" colspan="1">.03</td><td align="char" char="." rowspan="1" colspan="1">−.17**</td><td align="char" char="." rowspan="1" colspan="1">.05</td><td align="char" char="." rowspan="1" colspan="1">.10</td><td align="char" char="." rowspan="1" colspan="1">.00</td><td align="char" char="." rowspan="1" colspan="1">−.02</td><td align="char" char="." rowspan="1" colspan="1">.20**</td></tr><tr><td align="left" rowspan="1" colspan="1">Diarrhea episodes</td><td align="char" char="." rowspan="1" colspan="1">.01</td><td align="char" char="." rowspan="1" colspan="1">−.04</td><td align="char" char="." rowspan="1" colspan="1">.08</td><td align="char" char="." rowspan="1" colspan="1">−.08</td><td align="char" char="." rowspan="1" colspan="1">.11</td><td align="char" char="." rowspan="1" colspan="1">−.11</td><td align="char" char="." rowspan="1" colspan="1">.18*</td></tr><tr><td align="left" rowspan="1" colspan="1">Respiratory infections</td><td align="char" char="." rowspan="1" colspan="1">−.02</td><td align="char" char="." rowspan="1" colspan="1">−.04</td><td align="char" char="." rowspan="1" colspan="1">−.07</td><td align="char" char="." rowspan="1" colspan="1">−.05</td><td align="char" char="." rowspan="1" colspan="1">.06</td><td align="char" char="." rowspan="1" colspan="1">.04</td><td align="char" char="." rowspan="1" colspan="1">.22*</td></tr><tr><td align="left" rowspan="1" colspan="1">Child's behavior during the testing
session</td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Mood</td><td align="char" char="." rowspan="1" colspan="1">−.04</td><td align="char" char="." rowspan="1" colspan="1">.24**</td><td align="char" char="." rowspan="1" colspan="1">.13*</td><td align="char" char="." rowspan="1" colspan="1">−.20**</td><td align="char" char="." rowspan="1" colspan="1">.12</td><td align="char" char="." rowspan="1" colspan="1">.15**</td><td align="char" char="." rowspan="1" colspan="1">−.21**</td></tr><tr><td align="left" rowspan="1" colspan="1">Activity</td><td align="char" char="." rowspan="1" colspan="1">−.23**</td><td align="char" char="." rowspan="1" colspan="1">.19**</td><td align="char" char="." rowspan="1" colspan="1">.25**</td><td align="char" char="." rowspan="1" colspan="1">−.31<sup>***</sup></td><td align="char" char="." rowspan="1" colspan="1">.22**</td><td align="char" char="." rowspan="1" colspan="1">.29**</td><td align="char" char="." rowspan="1" colspan="1">−.20**</td></tr><tr><td align="left" rowspan="1" colspan="1">Interaction</td><td align="char" char="." rowspan="1" colspan="1">−.17**</td><td align="char" char="." rowspan="1" colspan="1">.25**</td><td align="char" char="." rowspan="1" colspan="1">.06</td><td align="char" char="." rowspan="1" colspan="1">−.25**</td><td align="char" char="." rowspan="1" colspan="1">.20**</td><td align="char" char="." rowspan="1" colspan="1">.18*</td><td align="char" char="." rowspan="1" colspan="1">−.18**</td></tr></tbody></table></alternatives><table-wrap-foot><fn><p><italic>Note.</italic> MUAC = mid upper-arm circumference.</p></fn><fn><p>*<italic>p</italic> < .05.</p></fn><fn><p>**<italic>p</italic> < .01.</p></fn><fn><p>***<italic>p</italic> < .001.</p></fn></table-wrap-foot></table-wrap></p></sec><sec id="sec4-2" sec-type="general"><title>Multivariate Regression Analysis</title><p>To test the hypothesis that maternal worm infections would independently affect
performance of children on measures of executive function, we performed a series of
hierarchical linear regression analyses in which associations with maternal worms were
examined taking into account associations with potential confounding factors. Using this
technique we explored the unique contribution of maternal worm infections over and above
effects of additional exposures. The independent variables were entered in a single model
which comprised three blocks: maternal-related factors (SES and family factors, health
factors), child-related factors (gender, health, and behavioral factors), and maternal
worms (entered in that order). Each subtest of the motor and cognitive assessment was
examined separately. Categorical measures (worm exposure and drug treatment) were loaded
as dummy variables. Non-significant explanatory variables were dropped from the model one
at a time leaving only the significant factors and therefore the best model that accounts
for performance on each of the measures. Associations between maternal worm infections,
and other factors, and each of the outcomes are summarized in <xref ref-type="table" rid="tab6">Table 6</xref> and described below; the order of entering variables into the
analysis is also listed in this table.<table-wrap id="tab6" orientation="portrait" position="float"><label>Table 6</label><caption><p>Effects of maternal worm infections and of other health and sociodemographic
exposures on the various functions</p></caption><alternatives><graphic xlink:href="S1355617712000768_tab6"></graphic><table frame="hsides" rules="groups"><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><col align="left" width="1*" span="1"></col><thead><tr><th align="left" rowspan="1" colspan="1">Measure</th><th align="left" rowspan="1" colspan="1">Worm/other exposure</th><th align="center" rowspan="1" colspan="1">Unstandardized coefficients (B)</th><th align="center" rowspan="1" colspan="1">Standardized coefficients (B)</th><th align="center" rowspan="1" colspan="1">Std. Error of B</th></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1">Fine motor</td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Maternal HIV</td><td align="char" char="." rowspan="1" colspan="1">.41*</td><td align="char" char="." rowspan="1" colspan="1">.07*</td><td align="char" char="." rowspan="1" colspan="1">.19</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Mood</td><td align="char" char="." rowspan="1" colspan="1">.11*</td><td align="char" char="." rowspan="1" colspan="1">−.10*</td><td align="char" char="." rowspan="1" colspan="1">.05</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Activity</td><td align="char" char="." rowspan="1" colspan="1">−.39***</td><td align="char" char="." rowspan="1" colspan="1">−.20***</td><td align="char" char="." rowspan="1" colspan="1">.08</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Interaction</td><td align="char" char="." rowspan="1" colspan="1">−.12*</td><td align="char" char="." rowspan="1" colspan="1">−.11*</td><td align="char" char="." rowspan="1" colspan="1">.05</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Height</td><td align="char" char="." rowspan="1" colspan="1">−.07***</td><td align="char" char="." rowspan="1" colspan="1">−.13***</td><td align="char" char="." rowspan="1" colspan="1">.02</td></tr><tr><td align="left" rowspan="1" colspan="1">Gross Motor</td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Mood</td><td align="char" char="." rowspan="1" colspan="1">.21**</td><td align="char" char="." rowspan="1" colspan="1">.14**</td><td align="char" char="." rowspan="1" colspan="1">.06</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Interaction</td><td align="char" char="." rowspan="1" colspan="1">.24***</td><td align="char" char="." rowspan="1" colspan="1">.16***</td><td align="char" char="." rowspan="1" colspan="1">.06</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Hb at 1 yr</td><td align="char" char="." rowspan="1" colspan="1">.10*</td><td align="char" char="." rowspan="1" colspan="1">.06*</td><td align="char" char="." rowspan="1" colspan="1">.05</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Height</td><td align="char" char="." rowspan="1" colspan="1">.07*</td><td align="char" char="." rowspan="1" colspan="1">.09*</td><td align="char" char="." rowspan="1" colspan="1">.03</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Weight</td><td align="char" char="." rowspan="1" colspan="1">.20**</td><td align="char" char="." rowspan="1" colspan="1">.11**</td><td align="char" char="." rowspan="1" colspan="1">.08</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Child's age</td><td align="char" char="." rowspan="1" colspan="1">.45**</td><td align="char" char="." rowspan="1" colspan="1">.09**</td><td align="char" char="." rowspan="1" colspan="1">.16</td></tr><tr><td align="left" rowspan="1" colspan="1">Language</td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Household SES</td><td align="char" char="." rowspan="1" colspan="1">.33**</td><td align="center" rowspan="1" colspan="1">09**</td><td align="char" char="." rowspan="1" colspan="1">.12</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Activity</td><td align="char" char="." rowspan="1" colspan="1">1.10***</td><td align="char" char="." rowspan="1" colspan="1">.23***</td><td align="char" char="." rowspan="1" colspan="1">.21</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Interaction</td><td align="char" char="." rowspan="1" colspan="1">−.30*</td><td align="char" char="." rowspan="1" colspan="1">−.11*</td><td align="char" char="." rowspan="1" colspan="1">.12</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Height</td><td align="char" char="." rowspan="1" colspan="1">.11*</td><td align="char" char="." rowspan="1" colspan="1">.08*</td><td align="char" char="." rowspan="1" colspan="1">.04</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Strongyloides stercoralis</td><td align="char" char="." rowspan="1" colspan="1">−.90*</td><td align="char" char="." rowspan="1" colspan="1">−.07*</td><td align="char" char="." rowspan="1" colspan="1">.44</td></tr><tr><td align="left" rowspan="1" colspan="1">Self Control</td><td align="left" rowspan="1" colspan="1">Activity</td><td align="char" char="." rowspan="1" colspan="1">−.10***</td><td align="char" char="." rowspan="1" colspan="1">−.16***</td><td align="char" char="." rowspan="1" colspan="1">.03</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Interaction</td><td align="char" char="." rowspan="1" colspan="1">−.06***</td><td align="char" char="." rowspan="1" colspan="1">−.17***</td><td align="char" char="." rowspan="1" colspan="1">.01</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Height</td><td align="char" char="." rowspan="1" colspan="1">−.02***</td><td align="char" char="." rowspan="1" colspan="1">−.10***</td><td align="char" char="." rowspan="1" colspan="1">.01</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Malaria episodes</td><td align="char" char="." rowspan="1" colspan="1">.06***</td><td align="char" char="." rowspan="1" colspan="1">.11***</td><td align="char" char="." rowspan="1" colspan="1">.02</td></tr><tr><td align="left" rowspan="1" colspan="1">Self Care</td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Activity</td><td align="char" char="." rowspan="1" colspan="1">.71***</td><td align="char" char="." rowspan="1" colspan="1">.16***</td><td align="char" char="." rowspan="1" colspan="1">.15</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">weight</td><td align="char" char="." rowspan="1" colspan="1">.26*</td><td align="char" char="." rowspan="1" colspan="1">.08*</td><td align="char" char="." rowspan="1" colspan="1">.11</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Sex</td><td align="char" char="." rowspan="1" colspan="1">1.32***</td><td align="char" char="." rowspan="1" colspan="1">.16***</td><td align="char" char="." rowspan="1" colspan="1">.27</td></tr><tr><td align="left" rowspan="1" colspan="1">Recognition of self and others</td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Activity</td><td align="char" char="." rowspan="1" colspan="1">−.18***</td><td align="char" char="." rowspan="1" colspan="1">−.17***</td><td align="char" char="." rowspan="1" colspan="1">.03</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Gravidity</td><td align="char" char="." rowspan="1" colspan="1">−.11*</td><td align="char" char="." rowspan="1" colspan="1">−.07*</td><td align="char" char="." rowspan="1" colspan="1">.05</td></tr><tr><td align="left" rowspan="1" colspan="1">A not B task</td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Activity</td><td align="char" char="." rowspan="1" colspan="1">−.75***</td><td align="char" char="." rowspan="1" colspan="1">−.26***</td><td align="char" char="." rowspan="1" colspan="1">.12</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Interaction</td><td align="char" char="." rowspan="1" colspan="1">.22***</td><td align="char" char="." rowspan="1" colspan="1">.14***</td><td align="char" char="." rowspan="1" colspan="1">.07</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Height</td><td align="char" char="." rowspan="1" colspan="1">.08***</td><td align="char" char="." rowspan="1" colspan="1">.11***</td><td align="char" char="." rowspan="1" colspan="1">.02</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Malaria</td><td align="char" char="." rowspan="1" colspan="1">−.18*</td><td align="char" char="." rowspan="1" colspan="1">−.08*</td><td align="char" char="." rowspan="1" colspan="1">.08</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"><italic>Mansonella perstans</italic></td><td align="char" char="." rowspan="1" colspan="1">−.40*</td><td align="char" char="." rowspan="1" colspan="1">−.07*</td><td align="char" char="." rowspan="1" colspan="1">.20</td></tr></tbody></table></alternatives><table-wrap-foot><fn><p><italic>Note.</italic> Maternal-related factors were entered into the model in
this order: mother's age, education level, occupation, income, gravidity, HIV
status, and hemoglobin level at enrollment; household socioeconomic status, family
size, and father's occupation. Child factors were entered into the model in this
order: child's sex, gestation age at birth, birth weight, Apgar score, malaria,
diarrhea, and respiratory infections in the first year, activity, mood, and
interaction level during assessment, hemoglobin level, weight, and height. Hb =
hemoglobin; SES = socioeconomic status.</p></fn><fn><p>*<italic>p</italic> < .05.</p></fn><fn><p>**<italic>p</italic> < .01.</p></fn><fn><p>***<italic>p</italic> < .001.</p></fn></table-wrap-foot></table-wrap></p><sec id="sec4-2-1" sec-type="general"><title>Fine motor</title><p>Child's mood and maternal HIV status were positively associated with fine motor
function, whereas activity, interaction and height were negatively associated with this
outcome (<italic>R</italic><sup>2</sup> = 0.08; <italic>F</italic>(5,956) = 15.89; <italic>p</italic> <
.001). Maternal worm infections had no association.</p></sec><sec id="sec4-2-2" sec-type="general"><title>Gross Motor</title><p>Performance on <italic>Gross Motor</italic> was positively associated with the child's
hemoglobin level at 1 year, height and weight at 15 months, mood and interaction during
assessment and child's age (<italic>R</italic><sup>2</sup> = 0.13; <italic>F</italic>(6,884) = 21.76; <italic>p</italic> <
.001). Maternal worms had no association.</p></sec><sec id="sec4-2-3" sec-type="general"><title>Language</title><p>Maternal <italic>Strongyloides stercoralis</italic> showed a negative association with
infants’ Language. Household socioeconomic status, child's activity and height at the
time of assessment showed positive associations with Language; and child's interaction
during assessment showed a negative association (<italic>R</italic><sup>2</sup> = 0.06; <italic>F</italic>(6,860) = 9.42; <italic>p</italic> <
.001). This model accounted for more variance than the model without maternal worms
(Δ<italic>R</italic><sup>2</sup> = 0.005).</p></sec><sec id="sec4-2-4" sec-type="general"><title>Self Care</title><p>This measure was positively associated with child's sex, activity, and weight at the
time of assessment (<italic>R</italic><sup>2</sup> = 0.05; <italic>F</italic>(3,974) = 16.90; <italic>p</italic> <
.001). Maternal worms had no association.</p><p><italic>Recognition of Self and of Others</italic> was negatively associated with
maternal gravidity and activity of child during assessment (<italic>R</italic><sup>2</sup> = 0.03; <italic>F</italic>(2,975) = 16.29; <italic>p</italic> <
.001). Maternal worm infections had no association.</p></sec><sec id="sec4-2-5" sec-type="general"><title>Self Control</title><p>Performance on <italic>Self Control</italic> was negatively associated with infant's
height, activity, and interaction during assessment and positively related with malaria
episodes in infancy. The raw association with maternal <italic>Strongyloides
stercoralis</italic> infection was no longer significantly associated with the function
when we controlled for the other exposures (<italic>R</italic><sup>2</sup> = 0.11; <italic>F</italic>(5,810) = 19.94; <italic>p</italic> <
.001).</p></sec><sec id="sec4-2-6" sec-type="general"><title>A-not-B task</title><p>Child's activity, interaction, and height were positively associated, while malaria
episodes in infancy and maternal <italic>Mansonella perstans</italic> were negatively
associated on this outcome. The raw association with maternal <italic>Trichuris
trichiura</italic> was no longer significant when we controlled for other factors
(<italic>R</italic><sup>2</sup> = 0.16; <italic>F</italic>(5,774) = 28.71; <italic>p</italic> <
.001). The model with <italic>Mansonella perstans</italic> infection accounted for more
variance than the model without the worm (Δ<italic>R</italic><sup>2</sup> = 0.004).</p><p>In summary, significant maternal worm effects were observed between <italic>Mansonella
perstans</italic> and performance on the A-not-B task, and between
<italic>Strongyloides stercoralis</italic> and performance on Language. Hookworm and
schistosomiasis did not show significant associations with the outcomes although these
were the most prevalent worms in the sample.</p></sec></sec></sec><sec sec-type="discussion" id="sec5"><title>Discussion</title><sec id="sec5-1" sec-type="general"><title>The Impact of Anthelminthic Treatment During Pregnancy</title><p>Treating pregnant women with albendazole or praziquantel had no significant effects on
infant developmental measures. The absence of treatment effects in a setting with high
prevalence of worm infection suggests that there is not much benefit of single-dose mass
anthelminthic treatment during pregnancy for cognitive and psychomotor outcomes in the
child.</p><p>Subgroup analysis suggested that praziquantel treatment in mothers who had
<italic>Schistosoma mansoni</italic> infection had significant effects on both the
A-not-B and Self Control tasks even though the worm did not have significant effects on
these outcomes. We observed a positive effect on Self Control. However, the negative
effect of the drug on the A-not-B task is difficult to explain since <italic>Schistosoma
mansoni</italic> infection has been associated with cognitive deficits and treatment was
therefore expected to be beneficial. This result could have occurred by chance, or the
negative effect of praziquantel might be linked to changes in the host immune responses
following treatment. Treatment of schistosomiasis is associated with an increase in
circulating proinflammatory as well as anti-inflammatory cytokines (Azim, Sedky,
el-Tahawy, Fikry, & Mostafa, <xref rid="ref3" ref-type="bibr">1995</xref>; Mwatha
et al., <xref rid="ref49" ref-type="bibr">1998</xref>); the killing of schistosomes
following praziquantel treatment results in release of worm antigens and a boost in
anti-worm responses (Tweyongyere et al., <xref rid="ref70" ref-type="bibr">2008</xref>;
Walter et al., <xref rid="ref72" ref-type="bibr">2006</xref>). The infection may be
effectively cleared but the high concentration of cytokines induced might perhaps
interfere with neurotransmitter systems, particularly the dopaminergic systems, thereby
affecting cognitive functioning (Reichenberg et al., <xref rid="ref56" ref-type="bibr">2001</xref>).</p></sec><sec id="sec5-2" sec-type="general"><title>Effects of Maternal Worm Infections</title><p>The results provide some support for the main hypothesis that maternal worm infections in
pregnancy might have negative effects, particularly on infant executive function, but this
is restricted to only two species. In line with our prediction, certain maternal worm
infections were associated with performance on both the A-not-B and Self Control tasks. We
observed a negative association between maternal <italic>Mansonella perstans</italic> and
infants’ later performance on the A-not-B task and a positive correlation between
<italic>Strongyloides stercoralis</italic> and Self Control. The latter was contrary to
our predictions and might be an incidental finding, as it suggests that infection improves
infant's skills on this function. It could be that children born to mothers with this
infection are not more self-controlled but rather less active and less interested in their
environment, and hence less interested in the treat. Indeed infant malaria and respiratory
infections likewise showed positive associations with performance on this measure. Thus
apathy may mediate the effect of ill-health on Self Control. However, delay tasks may not
be reliable measures of inhibitory control since performance on these measures varies
greatly with the task, including the type of treat used (Carlson et al., <xref rid="ref13" ref-type="bibr">2005</xref>).</p><p>The results suggest that executive functions might be particularly susceptible to
influences of maternal worms; the effect observed on language has been reported in earlier
childhood studies of worms (e.g., Ezeamama et al., <xref rid="ref25" ref-type="bibr">2005</xref>), and this might be secondary to effects on executive function given that the
two domains emerge within the same period and are reported to be interdependent throughout
life. Moreover, the two domains often show comorbidity (Ribeiro et al., 2011; Tannock
& Schachar, 1996; Willinger et al., 2003 for a review). Rebiero et al. explored
the comorbidity between language and executive functions and found that early executive
function (attention) impairment predicted later language problems but not vice-versa.
Therefore, the disruption of executive function by worms may explain the effect observed
on language. Given these specific influences, the results suggest that maternal worm
infections during pregnancy do not cause generalized cognitive deficits in infancy.
Plausible explanations for the selective nature of maternal worm effects in infancy have
been proposed. Maternal worms are believed to compete with the fetus for nutrients that
are vital for formation of neurological systems (Beard et al., <xref rid="ref6" ref-type="bibr">2007</xref>).</p><p>Naismith (<xref rid="ref50" ref-type="bibr">1969</xref>) suggests that, in cases of
moderate deprivation (e.g., due to mild worm infections), the fetus takes priority over
the nutrients that remain and thrives with minimal effects. Executive functions may
however be more vulnerable due to more specific metabolic effects. It has been proposed,
for example, that the availability of certain neurotransmitters is dependent on the
dietary supply of their amino acid precursors (Wainwright & Colombo, <xref rid="ref71" ref-type="bibr">2006</xref>); for example, tryptophan is the dietary
precursor of serotonin, and tyrosine is the precursor for dopamine and norepinephrine
(Fernstrom, <xref rid="ref26" ref-type="bibr">1990</xref>). Reduced levels of tyrosine may
lead to impaired executive function in children with phenylketonuria (Sharman, Sullivan,
Young, & McGill, <xref rid="ref61" ref-type="bibr">2009</xref>). Therefore,
changes in the availability of different amino acids may result in disturbances of
specific brain functions and behavior. Dopamine, in particular, acts in the prefrontal
cortex in which executive functions including planning, inhibition, and attention are
represented, both in animals (Gaarlen, Brueggeman, Bronius, Schoffelmeer, &
Vanderschuren, <xref rid="ref27" ref-type="bibr">2006</xref>) and humans (Goto &
Grace, <xref rid="ref32" ref-type="bibr">2005</xref>; Smith & Kieval, <xref rid="ref63" ref-type="bibr">2000</xref>).</p><p>However, in worms as in other organisms, tyrosine is an essential nutrient (Moran, <xref rid="ref46" ref-type="bibr">2005</xref>). Impaired tyrosine catabolism in worms is
associated with dramatic effects including a short life span, destruction of the
intestine, and decreased fertility. Given that intestinal worms depend on the host's
digestive contents for this amino acid, prolonged infestation of worms may deprive the
body of this nutrient and this may in turn impact on dopamine synthesis resulting in
impairment of the executive function.</p><p>The associations observed in this study were based on only two measures of executive
function. It is possible that worms affect other executive skills not measured by the
Delay inhibition task, and by the A not B task. Moreover, because assessments were done
later in infancy, we may not completely rule out the possibility that earlier in life
worms could show more generalized cognitive deficits. These are important issues that need
to be resolved by longitudinal studies measuring various cognitive abilities.</p><p>Effects of maternal worm infections on infant cognitive functioning could also be
mediated by iron deficiency. However, in this study we found very weak associations
between maternal worm infections and maternal anemia (Muhangi et al., <xref rid="ref48" ref-type="bibr">2007</xref>), or benefit of anthelminthic treatment for
anemia (Ndibazza et al., <xref rid="ref51" ref-type="bibr">2010</xref>). Moreover, all
women were routinely treated with iron and folic acid during pregnancy, perhaps
compensating for any iron loss due to worm infections. Worms were not causing major iron
deficiency anemia in these mothers, so cognitive effects of worms mediated by maternal
anemia would not have been detectable in this study.</p><p>In addition to worm infections, infant abilities were examined in relation to other
factors. Common infections in infancy, particularly repeated malaria, were found to
influence infants’ performance. As expected, child nutritional factors (hemoglobin,
height, and weight) showed significant positive correlations with developmental outcomes.
Infant mood, activity, and interaction level also consistently influenced scores on the
various developmental measures highlighting the role non-task behavior plays in
performance. Given that numerous factors were affecting infants’ development before and
after birth, a relatively small amount of variance explained by worms alone might be
expected. However, worms affect millions of mothers and children, and hence, the global
impact of even a small effect on child development may be important enough to raise
concern. Regardless of the effect size, these findings are in keeping with our prediction
and deserve further exploration.</p><p>Our study had an experimental design, and this was a strength of our analysis of the
effects of anthelminthic intervention. However, it is of note that the majority of
pregnant women who participated had a low intensity of worm infections; mothers with
hemoglobin below 8 g/dL were excluded from the study, and iron and folic acid were given
during antenatal care. These characteristics limit the extrapolation of our findings to
other populations. It could be that, where infections are heavy and nutritional and
micronutrient status is marginal, maternal worms have stronger and more diverse effects on
the development of the executive system. Future studies should aim specifically to
investigate effects in populations with high intensities of worms.</p><p>Furthermore, in early infancy, cognitive processes are not yet fully developed, which
undermines the validity of developmental effects measured. Moreover, future studies should
assess effects of worms on other aspects of executive functions, other than those measured
in this study. We continue to follow-up these infants and reassess the worm effects at
older ages and to include aspects of executive functions not examined in this study to
re-evaluate the selectivity of these effects.</p><p>In conclusion, the results of this study suggest that certain maternal worm infections
during pregnancy may have negative influences on early executive function in the offspring
but anthelminthic treatment is unlikely to reverse these effects. Further research should
aim to replicate these findings in the light of the limitations mentioned above.</p></sec></sec></body><back><ack id="ack1"><title>Acknowledgments</title><p>This research was funded by Wellcome Trust grant numbers 064693 and 079110 as part of the
overall Entebbe Mother and Baby Study. We thank the EMaBS team for their hard work and
commitment. We also thank the team in Kenya Medical Research Institute for permission to use
their measures and support in training the assessors. We thank the mothers and children from
Entebbe and Katabi for their participation in the study. There were no conflicts of interest
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