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Cited by 26Malaria Research and ControlPregnancy and preeclampsia studiesBlood groups and transfusion

Clinical outcomes of submicroscopic infections and correlates of protection of VAR2CSA antibodies in a longitudinal study of pregnant women in Colombia

Open access
Gavina, Kenneth, Gnidehou, Sedami, Arango, Eliana, Hamel-Martineau, Chloe, Mitran, Catherine, Agudelo, Olga, Lopez, Carolina, Karidio, Aisha +7 more·2018·Infection and Immunity
DOI 10.1128/iai.00797-17PMC PMC5865023
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Abstract

Malaria in pregnancy can cause serious adverse outcomes for the mother and the fetus. However, little is known about the effects of submicroscopic infections (SMIs) in pregnancy, particularly in areas where Plasmodium falciparum and Plasmodium vivax cocirculate. A cohort of 187 pregnant women living in Puerto Libertador in northwest Colombia was followed longitudinally from recruitment to delivery. Malaria was diagnosed by microscopy, reverse transcription-quantitative PCR (RT-qPCR), and placental histopathology. Gestational age, hemoglobin concentration, VAR2CSA-specific IgG levels, and adhesion-blocking antibodies were measured during pregnancy. Statistical analyses were performed to evaluate the impact of SMIs on birth weight and other delivery outcomes. Twenty-five percent of women (45/180) were positive for SMIs during pregnancy. Forty-seven percent of infections (21/45) were caused by P. falciparum , 33% were caused by P. vivax , and 20% were caused by mixed Plasmodium spp. Mixed infections of P. falciparum and P. vivax were associated with lower gestational age at delivery ( P = 0.0033), while other outcomes were normal. Over 60% of women had antibodies to VAR2CSA, and there was no difference in antibody levels between those with and without SMIs. The anti-adhesion function of these antibodies was associated with protection from SMI-related anemia at delivery ( P = 0.0086). SMIs occur frequently during pregnancy, and while mixed infections of both P. falciparum and P. vivax were not associated with a decrease in birth weight, they were associated with significant risk of preterm birth. We propose that the lack of adverse delivery outcomes is due to functional VAR2CSA antibodies that can protect pregnant women from SMI-related anemia.

AI snapshot

Written from the paper’s full text.

TL;DR

In a prospective cohort of 180 pregnant women in northwest Colombia, 25% had submicroscopic malaria infection (SMI), but SMI was not associated with lower birth weight. Mixed *P. falciparum* and *P. vivax* SMIs were associated with preterm birth, while functional VAR2CSA adhesion-blocking antibodies were associated with protection from SMI-related maternal anemia.

Key findings

  • SMI prevalence was 25% (45/180); among these, 47% (21/45) were *P. falciparum*, 33% (15/45) *P. vivax*, and 20% (9/45) mixed infections.
  • Mean birth weight was 3,220 ± 510 g in SMI pregnancies versus 3,259 ± 451 g without SMI (difference 38.4 g; 95% CI −121 to 198; P = 0.63).
  • Mixed *P. falciparum*/*P. vivax* SMI was associated with lower gestational age at delivery (mean difference 2.3 weeks; P = 0.0033) and higher risk of preterm birth (RR 3.40; 95% CI 1.45–7.97; P = 0.005).
  • VAR2CSA-specific IgG was present in 65% (117/180) of women and did not differ by SMI status; functional adhesion-blocking antibodies predicted higher maternal hemoglobin at delivery (P = 0.0086), and women without functional antibodies had higher anemia risk (RR 1.87; 95% CI 1.13–2.79; P = 0.014).

Methods

  • Prospective longitudinal cohort of 187 pregnant women in Puerto Libertador, Colombia, followed from recruitment to delivery; 180 were analyzed after excluding 7 microscopy-positive women, with 45 SMI cases.
  • Malaria was diagnosed by microscopy, RT-qPCR, and placental histopathology; gestational age, hemoglobin, VAR2CSA-specific IgG, and adhesion-blocking antibodies were measured during pregnancy.
  • Analyses included Fisher’s exact, t tests, Mann-Whitney, linear/mixed-effects models, and relative risks; the study had 80% power to detect a 250-g birth weight difference.

Limitations

  • Stated: loss to follow-up affected final sample size, and not all women attended monthly antenatal visits, so infections may have been missed.
  • Evident from the text: mixed-infection outcome analyses relied on only 9 women; RT-qPCR was performed retrospectively, SMIs were not treated, and no IPTp program existed, so natural clearance and immunity may explain the lack of adverse outcomes.
  • Evident from the text: no active placental infections were observed by histopathology, limiting assessment of placental malaria.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1128/iai.00797-17

Cites

Statistics

Nothing to recompute.

Claims the paper makes

0 of 25 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    25% (45/180) of pregnant women in the cohort were positive for submicroscopic malaria infection at least once during pregnancy.

    “Twenty-five percent of women (45/180) were positive for SMIs during pregnancy.”
    • Also stated in: § Prevalence of MiP. · plain
      “Of the 180 women included in the data analysis, 25% (n ϭ 45) were positive for an SMI at least once during pregnancy.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: RT-qPCR-positive peripheral blood samples indicate submicroscopic Plasmodium infection relevant to pregnancy outcomes.
  • Findingown data

    Active placental infections were not observed among the 180 women by histopathology.

    “Based on histopathology, active placental infections were not observed among the 180 women”
    Quote in the paperSubstantial claim
  • Findingown data

    No significant association was observed between SMIs during pregnancy and submicroscopic placental infection by RT-qPCR (P = 0.08).

    “or submicroscopic placental infection by RT-qPCR (P ϭ 0.08).”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: RT-qPCR-positive peripheral blood samples indicate submicroscopic Plasmodium infection relevant to pregnancy outcomes.
  • Findingown data

    Hemozoin was detected in the placentas of 12 women (6.7%).

    “hemozoin was detected in the placentas of 12 women (6.7%)”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: Hemozoin detected in the placenta indicates a past Plasmodium infection in pregnancy.
  • Findingown data

    Mixed infections of P. falciparum and P. vivax were associated with lower gestational age at delivery (P = 0.0033).

    “Mixed infections of P. falciparum and P. vivax were associated with lower gestational age at delivery (P ϭ 0.0033), while other outcomes were normal.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: RT-qPCR-positive peripheral blood samples indicate submicroscopic Plasmodium infection relevant to pregnancy outcomes.
  • May combine two claims. 18
  • Classified as probably not a substantial claim. 17

  • May combine two claims.

    Findingown data

    Among the submicroscopic infections, 47% were caused by P. falciparum, 33% by P. vivax, and 20% by mixed Plasmodium spp.

    “Forty-seven percent of infections (21/45) were caused by P. falciparum, 33% were caused by P. vivax, and 20% were caused by mixed Plasmodium spp.”
    • Also stated in: § Prevalence of MiP. · plain
      “Forty-seven percent (21/45) of these women were infected with P. falciparum, 33% (15/45) were infected with P. vivax, and 20% (9/45) were infected with mixed infections”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: RT-qPCR-positive peripheral blood samples indicate submicroscopic Plasmodium infection relevant to pregnancy outcomes.

  • May combine two claims.

    Findingown data

    The mean birth weight of infants born to mothers with an SMI was 3,220 g ± 510 g, and it was 3,259 g ± 451 g among those without an SMI.

    “The mean birth weight (Ϯ standard deviation [SD]) of infants born to mothers with an SMI was 3,220 g Ϯ 510 g, and it was 3,259 g Ϯ 451 g among those without an SMI”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: RT-qPCR-positive peripheral blood samples indicate submicroscopic Plasmodium infection relevant to pregnancy outcomes.

  • May combine two claims.

    Findingown data

    Among women with functional antibodies, 28% (5/18) were primigravid and 48% (13/27) were multigravid.

    “28% (5/18) were primigravid, and 48% (13/27) were multigravid (Fig. 4B).”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: Functional anti-adhesion antibody activity measured at enrollment reflects antibody function at delivery and protection from anemia.

  • May combine two claims.

    Findingown data

    No significant association was observed between percent inhibition and birth weight, gestational age, or small for gestational age.

    “No significant association was observed between the percent inhibition and birth weight (P ϭ 0.85) (Fig. 5A), gestational age (P ϭ 0.80) (Fig. 5B), or SGA (P ϭ 0.33) (Fig. 5C).”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Functional anti-adhesion antibody activity measured at enrollment reflects antibody function at delivery and protection from anemia.

  • May combine two claims.

    Findingown data

    VAR2CSA antibody levels were independent of parity, and 64% of primigravid women were seropositive at enrollment.

    “Furthermore, VAR2CSA antibody levels were independent of parity, and 64% of primigravid women were seropositive at enrollment.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Antibody levels in primigravid and multigravid women were similar (P = 0.76), as were the proportions of primigravid (64%) and multigravid (65%) women with antibodies.

    “Antibody levels in primigravid and multigravid women were similar (P ϭ 0.76), as were the proportions of primigravid (64%) and multigravid (65%) women with antibodies”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    In women with a submicroscopic infection, CSA adhesion-blocking antibodies correlate with hemoglobin levels at delivery but not with other delivery outcomes (birth weight, gestational age at delivery, or SGA).

    “CSA adhesion-blocking antibodies correlate with hemoglobin levels at delivery but not with other delivery outcomes in women with a submicroscopic infection.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    VAR2CSA antibodies are associated with protection from placental malaria and other adverse delivery outcomes.

    “These antibodies can block adhesion of IEs to CSA in vitro (4,5) and are associated with protection from placental malaria and other adverse delivery outcomes (6,7).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [6] source

      Not checked in the free run.

    • cites [7] source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Plasmodium vivax infection during pregnancy was associated with adverse outcomes in studies from Thailand and Indonesia.

    “Plasmodium vivax infection during pregnancy was associated with adverse outcomes in studies from Thailand and Indonesia (8,9); however, studies in Latin America reported varying results.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [8] source

      Not checked in the free run.

    • cites [9] source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    In another study in Colombia, no changes in mean birth weight, gestational age, or hemoglobin levels at delivery were observed with P. vivax infection.

    “while in another study, also in Colombia, no changes in mean birth weight, gestational age, or hemoglobin levels at delivery were observed (11).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [11] source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data

    A total of 148 women were lost to follow-up, with specified reasons.

    “A total of 148 women were lost to follow-up: 16 women delivered in their homes, 19 women delivered in their local villages, 98 women delivered at a distant regional hospital, 5 women delivered when study staff were unavailable, and 10 women were lost to follow-up without any known reason.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    SMIs are frequently detected in pregnant women in sub-Saharan Africa and were associated with adverse outcomes in several cross-sectional and longitudinal studies.

    “SMIs are also frequently detected in pregnant women in sub-Saharan Africa and were associated with adverse outcomes in several cross-sectional (21)(22)(23)(24) and longitudinal studies (25,26).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [21] source

      Not checked in the free run.

    • cites [22] source

      Not checked in the free run.

    • cites [23] source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data

    Of 402 women recruited into the study, 187 participated through to delivery.

    “Of the 402 women recruited into the study, 187 women participated through to delivery (Fig. 1).”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    In studies from Brazil, Bolivia, Peru, and Venezuela, P. vivax was associated with anemia, reduced birth weight, and histological changes in the placenta.

    “In studies from Brazil, Bolivia, Peru, and Venezuela, P. vivax was associated with anemia, reduced birth weight, and histological changes in the placenta (12)(13)(14)(15).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [12] source

      Not checked in the free run.

    • cites [13] source

      Not checked in the free run.

    • cites [14] source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    Pregnant women acquire antibodies to VAR2CSA following exposure to malaria in pregnancy, usually in a parity-dependent manner.

    “Pregnant women acquire antibodies to VAR2CSA following exposure to MiP, usually in a parity-dependent manner (1).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [1] source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    In a multicenter study of pregnant women in Colombia, Guatemala, Brazil, India, and PNG, submicroscopic P. falciparum and P. vivax infections were not associated with either maternal anemia or low birth weight.

    “In a multicenter study of pregnant women in Colombia, Guatemala, Brazil, India, and PNG, submicroscopic P. falciparum and P. vivax infections were not associated with either maternal anemia or LBW (29).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [29] source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    One study in Colombia demonstrated that P. vivax infection during pregnancy was associated with lower birth weight.

    “One study in Colombia demonstrated that P. vivax infection during pregnancy was associated with lower birth weight (10), while in another study, also in Colombia, no changes in mean birth weight, gestational age, or hemoglobin levels at delivery were observed (11).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [10] source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductreasoning

    Seven women were excluded from downstream data analysis due to a smear-positive Plasmodium result by microscopy.

    “because of the focus on SMI, seven women were excluded from downstream data analysis due to a smear-positive Plasmodium result by microscopy.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    P. falciparum and P. vivax SMIs at delivery were associated with poor outcomes in one study from Papua New Guinea but not in studies conducted in Colombia and India.

    “P. falciparum and P. vivax SMIs at delivery were associated with poor outcomes in one study from Papua New Guinea (PNG) (27) but not in studies conducted in Colombia and India (10,28).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [27] source

      Not checked in the free run.

    • cites [10] source

      Not checked in the free run.

    • cites [28] source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    Antibodies that protect women from adverse outcomes in pregnancy predominantly target the VAR2CSA surface antigen.

    “Antibodies that protect women from adverse outcomes in pregnancy predominantly target the VAR2CSA surface antigen (1,2).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [1] source

      Not checked in the free run.

    • cites [2] source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    The data suggest that women had immunity that facilitated parasite clearance and prevented sequestration of infected erythrocytes in the placenta.

    “Our data suggest that women had immunity that facilitated parasite clearance and prevented sequestration of IEs in the placenta.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Functional anti-adhesion antibody activity measured at enrollment reflects antibody function at delivery and protection from anemia.

  • May combine two claims.

    Study design and conductreasoning

    Women with SMIs were not treated with antimalarials because RT-qPCR was performed retrospectively, and no intermittent preventive treatment in pregnancy program is available in the study communities.

    “In our study, women with SMIs were not treated with antimalarials as RT-qPCR was performed retrospectively, and no intermittent preventive treatment in pregnancy (IPTp) program is available in the study communities”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationcitation

    Antibodies that blocked adhesion of infected erythrocytes to chondroitin sulfate A were associated with reduced risk of anemia in women exposed to SMIs during pregnancy, suggesting a role for these antibodies in opsonization of infected erythrocytes.

    “Antibodies that blocked adhesion of IEs to CSA were associated with reduced risk of anemia in women exposed to SMIs during pregnancy, suggesting a role for these antibodies in opsonization of IEs (35).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [35] source

      Not checked in the free run.

    • Rests on an assumption: Functional anti-adhesion antibody activity measured at enrollment reflects antibody function at delivery and protection from anemia.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductown data

    Visual inspection of residual plots did not reveal any obvious deviations from homoscedasticity or normality in the linear mixed-effects model.

    “Visual inspection of residual plots did not reveal any obvious deviations from homoscedasticity or normality.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data

    VAR2CSA was expressed on the surface of IEs infected with P. falciparum CS2, as confirmed by flow cytometry.

    “Expression of VAR2CSA on the surface of IEs infected with P. falciparum CS2 was confirmed by flow cytometry using a rabbit anti-VAR2CSA polyclonal antibody (1:40 dilution) and detected using a goat anti-rabbit secondary conjugated to Alexa Fluor 647 (1:500 dilution; Life Technologies).”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductnone given

    Not all women attended monthly antenatal visits, and infections may have been missed during follow-up.

    “Additionally, not all women attended monthly antenatal visits, and infections may have been missed during follow-up.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductnone given

    All microscopists were trained and underwent proficiency testing.

    “All microscopists were trained and underwent proficiency testing.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductreasoning

    A sample size of 115 mother-infant pairs was needed to detect a clinically significant difference of 250 g in birth weight between groups.

    “a sample size of 115 mother-infant pairs was needed to detect a clinically significant difference of 250 g in birth weight between groups.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    The final sample size was affected by loss to follow-up in the early stages of the study.

    “First, the final sample size was affected by the loss to follow-up in the early stages of the study.”
    Quote in the paperNot a substantial claim
29 of 29

  • The paper relies on this without support.

    RT-qPCR-positive peripheral blood samples indicate submicroscopic Plasmodium infection relevant to pregnancy outcomes.

    “Malaria was diagnosed by microscopy, reverse transcription-quantitative PCR (RT-qPCR), and placental histopathology.”
    “Samples were tested by reverse-transcription real-time quantitative PCR (RT-qPCR) retrospectively.”

  • The paper relies on this without support.

    Hemozoin detected in the placenta indicates a past Plasmodium infection in pregnancy.

    “hemozoin was detected in the placentas of 12 women (6.7%), indicating a past Plasmodium infection in pregnancy.”

  • The paper relies on this without support.

    Functional anti-adhesion antibody activity measured at enrollment reflects antibody function at delivery and protection from anemia.

    “we measured the functional activity of antibodies at enrollment in the 45 women with SMIs.”
    “inhibitory antibody function was a significant independent predictor of higher maternal Hb levels at delivery (P ϭ 0.0086) (Fig. 5D).”

  • The paper relies on this without support.

    Loss to follow-up did not bias the primary birth weight comparison.

    “First, the final sample size was affected by the loss to follow-up in the early stages of the study.”
    “Nevertheless, our study was adequately powered not to reject the null hypothesis of our primary objective to test whether SMIs during pregnancy are significantly associated with birth weight at delivery.”
4 of 4

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Mixed Plasmodium infections were associated with a higher risk of preterm birth but did not result in lower birth weight compared to single-species infections.

    “Another study found that mixed Plasmodium infections were associated with a higher risk of preterm birth but did not result in lower birth weight compared to single-species infections [97].”

    From Current update on malaria in pregnancy: a systematic review (2025) · cites this paper as [97]

    The Prevalence of MiP results and Table 3 report a higher risk of preterm birth with mixed P. falciparum and P. vivax infection, and the paper says mixed infections were not associated with decreased birth weight. However, the reported risk comparisons use uninfected women as the reference, not women with single-species infections. The claimed comparison with single-species infections is therefore not established by these results. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • Submicroscopic cases are not detected or treated, resulting in severe outcomes for the mother and child (anemia and severe malaria) while also perpetuating parasite transmission and disease endemicity.

    “submicroscopic cases are not detected or treated, resulting in severe outcomes for the mother and child (anemia and severe malaria) while also perpetuating parasite transmission and disease endemicity [20,23,24,25,26]”

    From Diagnostic Accuracy of a Thick Blood Smear Compared to qPCR for Malaria Associated with Pregnancy in Colombia (2023) · cites this paper as [20]

  • The similar proportion of P. vivax and P. falciparum in PM would contradict several assumptions about P. vivax's lower capacity for clinical damage.

    “the similar proportion of P. vivax and P. falciparum in PM would contradict several assumptions about P. vivax’s lower capacity for clinical damage [20,21,22,48]”

    From Diagnostic Accuracy of a Thick Blood Smear Compared to qPCR for Malaria Associated with Pregnancy in Colombia (2023) · cites this paper as [20]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Gestational-age difference falls outside its reported confidence interval

    Major

    The reported 95% confidence interval of 35 to 38 weeks cannot be the confidence interval for a mean difference of 2.3 weeks. The interval appears to describe a gestational age rather than the stated difference.

  • Gravidity counts differ between Table 1 and the antibody analysis

    Major

    The antibody analysis uses denominators of 18 primigravid and 27 multigravid women among the 45 women with SMIs. Table 1 instead lists 16 primigravid, 11 secundigravid, and 18 multigravid women in that group.

  • Incorrect percentage for PCR-negative multigravid women

    Minor

    Table 1 lists 64 multigravid women among 135 PCR-negative women, which is 47.4%, not 44.4%.

    Reported 44.4 · recomputed 47.407407

  • Gestational-age result cites the hemoglobin panel

    Minor

    The text directs readers to Figure 2D for gestational age, but the figure caption identifies gestational age as panel B and maternal hemoglobin as panel D.

4 of 4

The citation lists haven’t been fetched yet

References 47 · Cited by 26

Authors
Gavina, K., Gnidehou, S., Arango, E., Hamel-Martineau, C., Mitran, C., Agudelo, O., Lopez, C., Karidio, A., Banman, S., Carmona-Fonseca, J., Salanti, A., Tuikue Ndam, N., Hawkes, M., Maestre, A., & Yanow, S. K.
Affiliations
  • University of Alberta (CA)
  • Department of Biology, Campus Saint-Jean, University of Alberta, Edmonton, Alberta, Canada
  • Universidad de Antioquia (CO)
  • Grupo Salud y Comunidad, Facultad de Medicina, Universidad de Antioquia, Medellín, Colombia
  • University of Copenhagen (DK)
  • University of Ghana, Accra, Ghana
ORCID
Venue
Infection and Immunity
Publisher
American Society for Microbiology
Published
2018-04
Volume
86
Issue
4
ISSN
  • 0019-9567 (ISSN-L)
  • 1098-5522
DOI
10.1128/iai.00797-17
PMC
PMC5865023
OpenAlex
W2787058498
Cited by
26
References
47
Citations by year
2025: 1 · 2024: 3 · 2023: 5 · 2022: 6 · 2021: 3 · 2020: 3 · 2019: 4 · 2018: 1
FWCI
2.62
Type
journal article
Language
en
Update notices
correction (2018-07-23)
Open access
Licence
journals.asm.org/non-commercial-tdm-license (tdm)
Locations
  • Infection and Immunity (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, other-oa)
  • PubMed (publishedVersion)
  • Institutional Repository University of Antioquia (University of Antioquia) (publishedVersion, cc-by)
Funders
  • COLCIENCIAS
  • Emerging Leaders of the Americas
  • Gouvernement du Canada | Natural Sciences and Engineering Research Council of Canada
  • Gouvernement du Canada | Canadian Institutes of Health Research
  • Universidad de Antioquia
  • University of Alberta
Topics
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
  • Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
  • Health Sciences › Medicine › Hematology › Blood groups and transfusion
Keywords
malaria in pregnancy, submicroscopic malaria infection, placental adhesions, Plasmodium falciparum, Plasmodium vivax, mixed malaria infection, preterm birth, birth weight, placental pathology, pregnancy outcomes

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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

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Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-10.

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