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Cited by 55Malaria Research and ControlBird parasitology and diseasesHemoglobinopathies and Related Disorders

Molecular Detection of Malaria at Delivery Reveals a High Frequency of Submicroscopic Infections and Associated Placental Damage in Pregnant Women from Northwest Colombia

Open access
Arango, Eliana M., Samuel, Roshini, Agudelo, Olga M., Carmona-Fonseca, Jaime, Maestre, Amanda, Yanow, Stephanie K.·2013·The American Society of Tropical Medicine and Hygiene
DOI 10.4269/ajtmh.12-0669PMC PMC3748479
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Abstract

Plasmodium infection in pregnancy causes substantial maternal and infant morbidity and mortality. In Colombia, both P. falciparum and P. vivax are endemic, but the impact of either species on pregnancy is largely unknown in this country. A cross-sectional study was carried out with 96 pregnant women who delivered at their local hospital. Maternal, placental, and cord blood were tested for malaria infection by microscopy and real-time quantitative polymerase chain reaction (qPCR). A high frequency of infection was detected by qPCR (45%). These infections had low concentrations of parasite DNA, and 79% were submicroscopic. Submicroscopic infections were associated with placental villitis and intervillitis. In conclusion, the overall frequency of Plasmodium infection at delivery in Colombia is much higher than previously reported. These data prompt a re-examination of the local epidemiology of malaria using molecular diagnostics to establish the clinical relevance of submicroscopic infections during pregnancy as well as their consequences for mothers and newborns.

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Written from the paper’s full text.

TL;DR

In a cross-sectional pilot of 96 pregnant women delivering in northwest Colombia, qPCR detected Plasmodium infection in 65% of women in at least one compartment, and 79% of infections were submicroscopic. Submicroscopic infections were associated with placental villitis and intervillitis, prompting re-examination of local malaria epidemiology using molecular diagnostics.

Key findings

  • By qPCR, 65% of women had at least one positive compartment; 45% of all compartment samples were qPCR-positive. The highest frequency was in placenta (57%), followed by peripheral blood (49%) and cord blood (29%).
  • Submicroscopic infections accounted for 79% of infections (48 women were qPCR-positive but microscopy-negative). Placental villitis and intervillitis were more frequent in women with microscopic or submicroscopic infection than in uninfected women (P = 0.04).
  • Malaria pigment deposits were more frequent in women with microscopic infection (62%) than in women with submicroscopic infection (15%) or uninfected women (14%) (P = 0.0009).
  • A history of malaria in pregnancy was associated with lower infant birth weight: 3,132 g versus 3,578 g without history (P = 0.0081). By species history, mean birth weight was 3,053 g for P. vivax, 3,300 g for P. falciparum, and 3,578 g for no history (P = 0.010).

Methods

  • Cross-sectional pilot study at one hospital obstetric facility each in Turbo, Necoclí, and Puerto Libertador, Colombia. A sample of 96 women was randomly selected from a larger cohort of 2,550 parturient women recruited between 2005 and 2011.
  • Maternal peripheral, placental, and cord blood were tested by microscopy and real-time quantitative PCR (qPCR); placental tissue was examined histologically. Clinical data came from questionnaires and hospital charts.
  • Continuous and categorical variables were compared using Kruskal–Wallis and χ² tests, with significance set at P < 0.05.

Limitations

  • Stated: the small sample size is a limitation, and larger studies are required to broaden the findings.
  • Stated: qPCR may detect gametocytes or free parasite DNA rather than intact, pathogenic asexual parasites, which is critical when interpreting qPCR as a diagnostic tool.
  • Evident from the design: this is a cross-sectional pilot in one transmission region, so associations cannot establish causality or temporality.

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

Integrity signals

Registry

Crossref · 10.4269/ajtmh.12-0669

Cites

42 of 42 references verified0 citation errors · 0 not checkable

Statistics

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Claims the paper makes

0 of 54 cited sources checked · 0 supported · 0 flagged

  • Findingown data
    § Results

    DNA concentrations were significantly higher in P. vivax and mixed infections compared with P. falciparum (P = 0.0082).

    “A comparison of the DNA concentrations by species revealed significantly higher DNA concentrations in P. vivax and mixed infections compared with P. falciparum (P = 0.0082).”
    Quote in the paperNot a substantial claim
  • Findingown data
    § Results

    23% of women were positive in all three compartments at delivery by qPCR.

    “Based on qPCR, 65% of women had at least one positive compartment, 25% of women had two positive compartments, and 23% of women were positive in all three compartments.”
    Quote in the paperNot a substantial claim
  • Findingown data
    § Abstract

    79% of the Plasmodium infections detected by qPCR in pregnant women at delivery were submicroscopic.

    “These infections had low concentrations of parasite DNA, and 79% were submicroscopic.”
    • Also stated in: § Results · plain
      “These submicroscopic infections account for 79% of the infections.”
    Quote in the paperSubstantial claim
  • Findingown data
    § Results

    Across all three compartments, most of the P. falciparum infections (78%) had < 2 DNA copies/μL.

    “Across all three compartments, most of the P. falciparum infections (78%) had < 2 DNA copies/μL (Figure 1B).”
    Quote in the paperNot a substantial claim
  • Findingown data
    § Results

    Cord blood was the compartment with the lowest level of Plasmodium infection.

    “Cord was the compartment with the lowest level of infection (Figure 1A).”
    Quote in the paperNot a substantial claim
  • The quote only partly states this claim. 1
  • May combine two claims. 28
  • Classified as probably not a substantial claim. 27

  • The quote only partly states this claim.

    Findingown data
    § Results

    74% of qPCR-positive samples were also positive for at least one species-specific marker.

    “74% of samples were also positive for at least one species-specific marker (Supplemental Table 1).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data
    § Results

    The highest frequency of Plasmodium infection was in the placenta (57%), followed by peripheral blood (49%) and cord (29%).

    “The highest frequency of infection was in the placenta (57%) followed by peripheral blood (49%) and cord (29%).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data
    § Results

    By microscopy, the majority of infections (75%) were identified as P. vivax, whereas over 50% of the infections detected by qPCR were caused by P. falciparum.

    “By microscopy, the majority of infections (75%) were identified as P. vivax, whereas over 50% of the infections detected by qPCR were caused by P. falciparum (Table 2).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data
    § Results

    Age, hemoglobin level, gestational age, parity, and birth weight were similar among women who were negative for malaria and women with microscopic and submicroscopic infections.

    “Age, hemoglobin level, gestational age, parity, and birth weight were similar among the three groups.”
    Quote in the paperNot a substantial claim

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

    Findingown data
    § Results

    The mean infant birth weight in primiparae was 3,061 ± 467 g, and the mean infant birth weight in multiparous women was 3,333 ± 463 g (P = 0.086).

    “The mean infant birth weight in primiparae was 3,061 ± 467 g, and the mean infant birth weight in multiparous women was 3,333 ± 463 g (P = 0.086).”
    Quote in the paperNot a substantial claim

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

    Findingown data
    § Results

    59% of women had at least one previous delivery.

    “59% of women had at least one previous delivery.”
    Quote in the paperNot a substantial claim

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

    Findingown data
    § Results

    Frequencies of pre-term delivery and low birth weight were low (6% and 4%, respectively).

    “Frequencies of pre-term delivery and LBW were low (6% and 4%, respectively).”
    Quote in the paperNot a substantial claim

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

    Findingnone given
    § Results

    All women received treatment at the time of malaria diagnosis.

    “All women received treatment at the time of diagnosis.”
    Quote in the paperNot a substantial claim

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

    Findingown data
    § Results

    Sixteen different species combinations were detected across the compartments.

    “Sixteen different species combinations were detected across the compartments.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data
    § Results

    A total of 48 women (73%) had at least one recorded episode of malaria; 34 women had a history of P. vivax, and 6 women had a history of P. falciparum.

    “A total of 48 women (73%) had at least one recorded episode of malaria; 34 women had a history of P. vivax, and 6 women had a history of P. falciparum.”
    Quote in the paperNot a substantial claim

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

    Findingown data
    § Results

    The history of malaria during the current pregnancy was known for 66 of 96 (69%) women.

    “The history of malaria during the current pregnancy was known for 66 of 96 (69%) women.”
    Quote in the paperNot a substantial claim

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

    Findingown data
    § Results

    Infant birth weight was significantly lower in primiparae and adolescents (≤ 18 years of age).

    “Infant birth weight was significantly lower in primiparae and adolescents (≤ 18 years of age), but this finding was not associated with malaria infection.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data
    § Results

    Placental histological analysis was available for 87 women (91%): 28 women were negative for plasmodial infection, 46 women had submicroscopic infections, and 13 women had microscopic infections.

    “Placental histological analysis was available for 87 women (91%): 28 women were negative for plasmodial infection, 46 women had submicroscopic infections, and 13 women had microscopic infections.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data
    § Discussion

    We detected the highest frequency of infection in the placenta, and the majority of infection was caused by P. falciparum.

    “Consistent with these findings, we detected the highest frequency of infection in the placenta, and the majority of infection was caused by P. falciparum.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data
    § Results

    Adolescent women had infants with a mean weight of 2,992 ± 284 g, whereas the infant birth weight in older women was 3,325 ± 486 g (P = 0.0009).

    “Adolescent women had infants with a mean weight of 2,992 ± 284 g, whereas the infant birth weight in older women was 3,325 ± 486 g (P = 0.0009).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data
    § Results

    The species detected at delivery by qPCR was not statistically associated with birth weight (P = 0.254), with mean birth weights: P. vivax 3,059 ± 459 g, P. falciparum 3,320 ± 512 g, no infection 3,271 ± 469 g.

    “In contrast, the species detected at delivery by qPCR was not statistically associated with birth weight (P = 0.254); however, the mean infant birth weight in women with P. vivax infection at delivery was lower (3,059 ± 459 g) than the mean infant birth weight in women with P. falciparum infection (3,320 ± 512 g) and the mean infant birth weight in women without infection (3,271 ± 469 g).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data
    § Results

    Among women with a history of malaria in pregnancy, infant birth weight differed by species: P. vivax mean 3,053 ± 427 g, P. falciparum 3,300 ± 379 g, no history 3,578 ± 559 g (P = 0.010).

    “In addition, the species detected during the pregnancy influenced the birth weight; infants born from women with a history of P. vivax had a mean birth weight of 3,053 ± 427 g, whereas the infant birth weight from women with a history of P. falciparum was 3,300 ± 379 g. Infant birth weight from women without a history of malaria was 3,578 ± 559 g (P = 0.010).”
    Quote in the paperNot a substantial claim

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

    Premisecitation
    § Introduction

    In areas of high, stable transmission, pregnancy malaria is often asymptomatic but associated with severe maternal anemia and fetal growth retardation.

    “In areas of high, stable transmission, including sub-Saharan Africa, where P. falciparum predominates, pregnancy malaria is often asymptomatic but associated with severe maternal anemia and fetal growth retardation.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [8] Muehlenbachs, 2010, A novel histological grading scheme for placental malaria applied in areas of high and low malaria transmission

      Not checked in the free run.

    • cites [9] Nosten, 2004, Malaria in pregnancy and the endemicity spectrum: what can we learn?

      Not checked in the free run.

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

    Premisecitation
    § Introduction

    In areas of low, unstable transmission, malaria infection is typically symptomatic in women of all parities and associated with high rates of fetal loss and maternal death.

    “In areas of low, unstable transmission, malaria infection is typically symptomatic in women of all parities and associated with high rates of fetal loss and maternal death.9”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [9] Nosten, 2004, Malaria in pregnancy and the endemicity spectrum: what can we learn?

      Not checked in the free run.

  • May combine two claims.

    Premisecitation
    § Introduction

    The epidemiology and clinical significance of submicroscopic malaria infections during pregnancy are not well-understood.

    “However, the epidemiology and clinical significance of submicroscopic malaria infections during pregnancy are not well-understood.13,15–20”
    Quote in the paperSubstantial claim0 of 7 sources checked
    • cites [13] Okell, 2009, Submicroscopic infection in Plasmodium falciparum-endemic populations: a systematic review and meta-analysis

      Not checked in the free run.

    • cites [15] Rantala, 2010, Comparison of real-time PCR and microscopy for malaria parasite detection in Malawian pregnant women

      Not checked in the free run.

    • cites [16] Arango, 2010, Effect of submicroscopic or polyclonal Plasmodium falciparum infection on mother and gestation product: systematic review

      Not checked in the free run.

    • cites [17] Malhotra, 2005, Real-time quantitative PCR for determining the burden of Plasmodium falciparum parasites during pregnancy and infancy

      Not checked in the free run.

    • cites [18] Adegnika, 2006, Microscopic and sub-microscopic Plasmodium falciparum infection, but not inflammation caused by infection, is associated with low birth weight

      Not checked in the free run.

    • cites [19] Mankhambo, 2002, Evaluation of the OptiMAL rapid antigen test and species-specific PCR to detect placental Plasmodium falciparum infection at delivery

      Not checked in the free run.

    • cites [20] Walker-Abbey, 2005, Malaria in pregnant Cameroonian women: the effect of age and gravidity on submicroscopic and mixed-species infections and multiple parasite genotypes

      Not checked in the free run.

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

    Premisecitation
    § Introduction

    Women living in different geographical areas experience variable levels of exposure to Plasmodium, which influences the course of infection in pregnancy.

    “Women living in different geographical areas experience variable levels of exposure to Plasmodium, which influences the course of infection in pregnancy.8”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [8] Muehlenbachs, 2010, A novel histological grading scheme for placental malaria applied in areas of high and low malaria transmission

      Not checked in the free run.

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

    Study design and conductnone given
    § Materials and Methods

    The sensitivity of the qPCR assay for the detection of parasite DNA in clinical samples is limited by the input volume in the qPCR reaction, which corresponds to ∼2.5 μL whole blood.

    “The sensitivity of the qPCR assay for the detection of parasite DNA in clinical samples is limited by the input volume in the qPCR reaction, which corresponds to ∼2.5 μL whole blood.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Study design and conductreasoning
    § Materials and Methods

    A sample size of 96 randomly selected women was calculated from a larger epidemiological study of 2,550 parturient women using a formula with specified parameters.

    “A sample size of 96 randomly selected women was calculated from a larger epidemiological study of 2,550 parturient women recruited between 2005 and 2011 using the formula n = NZ2p(1 − p)/[(Ne2) + (Z2p(1 − p))],27 where N is the reference population (N = 2,550), Z is the confidence level (95%), p is the reported frequency of submicroscopic infection at delivery (18%),12 and e is the sampling error”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [27] Martínez-Bencardino, 1984

      Not checked in the free run.

    • cites [12] Campos, 2011, Diagnosis of gestational, congenital, and placental malaria in Colombia: comparison of the efficacy of microscopy, nested polymerase chain reaction, and histopathology

      Not checked in the free run.

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

    Premisecitation
    § Introduction

    All species of Plasmodium cause malaria infection in pregnant women, but only P. falciparum has been extensively studied in pregnancy, with few studies of P. vivax.

    “All species of Plasmodium cause malaria infection in pregnant women, but only P. falciparum has been extensively studied in pregnancy, with few studies of P. vivax.”
    Quote in the paperNot a substantial claim0 of 4 sources checked
    • cites [4] Rijken, 2012, Malaria in pregnancy in the Asia-Pacific region

      Not checked in the free run.

    • cites [5] Rogerson, 2007, Malaria in pregnancy: pathogenesis and immunity

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    • cites [6] Hartman, 2010, The impact of maternal malaria on newborns

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    • cites [7] Poespoprodjo, 2008, Adverse pregnancy outcomes in an area where multidrug-resistant Plasmodium vivax and Plasmodium falciparum infections are endemic

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

    Premisecitation
    § Introduction

    In a recent study of 2,117 pregnant women in the Urabá region, 220 cases of malaria were diagnosed by microscopy.

    “In a recent study of 2,117 pregnant women in the Urabá region, 220 cases of malaria were diagnosed by microscopy.11”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [11] Carmona-Fonseca, 2009, Incidencia de las malarias gestacional, congénita y placentaria en Urabá (Antioquia, Colombia), 2005–2007

      Not checked in the free run.

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

    Premisecitation
    § Introduction

    Malaria in pregnancy causes substantial maternal and infant morbidity and mortality in tropical areas because of increased risk of maternal anemia and low birth weight infants.

    “Malaria in pregnancy causes substantial maternal and infant morbidity and mortality in tropical areas because of increased risk of maternal anemia and low birth weight (LBW) infants.1”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [1] Desai, 2007, Epidemiology and burden of malaria in pregnancy

      Not checked in the free run.

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

    Premisecitation
    § Materials and Methods

    Treatment guidelines for malaria in pregnancy include chloroquine for vivax malaria and quinine-clindamycin (first trimester) or artemether-lumefantrine (second and third trimesters) for falciparum malaria.

    “Treatment guidelines for malaria in pregnancy include chloroquine for vivax malaria and quinine-clindamycin (first trimester) or artemether-lumefantrine (second and third trimesters) for falciparum malaria.26”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [26] Colombia, 2010

      Not checked in the free run.

  • May combine two claims.

    Premisecitation
    § Introduction

    In a subset of 79 pregnant women at delivery, the frequency of plasmodial infection in peripheral and placental blood samples detected by microscopy was 13% and 9%, respectively, whereas the frequency of infection detected by nested PCR was 32% and 26%, respectively.

    “In a subset of 79 pregnant women at delivery, the frequency of plasmodial infection in peripheral and placental blood samples detected by microscopy was 13% and 9%, respectively, whereas the frequency of infection detected by nested polymerase chain reaction (PCR) was 32% and 26%, respectively.12”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [12] Campos, 2011, Diagnosis of gestational, congenital, and placental malaria in Colombia: comparison of the efficacy of microscopy, nested polymerase chain reaction, and histopathology

      Not checked in the free run.

  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation
    § Introduction

    Both P. falciparum and P. vivax infections can cause adverse pregnancy outcomes.

    “However, both infections can cause adverse pregnancy outcomes.4–7”
    Quote in the paperSubstantial claim0 of 4 sources checked
    • cites [4] Rijken, 2012, Malaria in pregnancy in the Asia-Pacific region

      Not checked in the free run.

    • cites [5] Rogerson, 2007, Malaria in pregnancy: pathogenesis and immunity

      Not checked in the free run.

    • cites [6] Hartman, 2010, The impact of maternal malaria on newborns

      Not checked in the free run.

    • cites [7] Poespoprodjo, 2008, Adverse pregnancy outcomes in an area where multidrug-resistant Plasmodium vivax and Plasmodium falciparum infections are endemic

      Not checked in the free run.

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

    Study design and conductown data
    § Materials and Methods

    The study was approved by the Comité de Ética of Instituto de Investigaciones Médicas, Universidad de Antioquia, and the Health Research Ethics Board of the University of Alberta.

    “The study involved minor risk, and approval was granted by the Comité de Ética of Instituto de Investigaciones Médicas (ethical approval numbers: IIM2484, IIM2509, IIM2530, and IIM2557), Universidad de Antioquia, and the Health Research Ethics Board of the University of Alberta (ethical approval number: Pro00017660).”
    Quote in the paperNot a substantial claim

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

    Premisecitation
    § Introduction

    Similar discrepancies between PCR and microscopy are reported from other endemic population surveys.

    “Similar discrepancies between PCR and microscopy are reported from other endemic population surveys.13,14”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [13] Okell, 2009, Submicroscopic infection in Plasmodium falciparum-endemic populations: a systematic review and meta-analysis

      Not checked in the free run.

    • cites [14] Uneke, 2008, Diagnosis of Plasmodium falciparum malaria in pregnancy in sub-Saharan Africa: the challenges and public health implications

      Not checked in the free run.

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

    Premisecitation
    § Introduction

    In areas of high, stable transmission, placental infection is most frequent in first-time mothers, because women develop immunity against placental parasites that provides protection over successive pregnancies.

    “In these areas, placental infection is most frequent in first-time mothers, because women develop immunity against placental parasites that provides protection over successive pregnancies.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [8] Muehlenbachs, 2010, A novel histological grading scheme for placental malaria applied in areas of high and low malaria transmission

      Not checked in the free run.

    • cites [9] Nosten, 2004, Malaria in pregnancy and the endemicity spectrum: what can we learn?

      Not checked in the free run.

  • May combine two claims.

    Premisecitation
    § Introduction

    The application of more sensitive molecular tests identified 2.5 times more infections than microscopy, classifying these infections as submicroscopic.

    “Importantly, the application of more sensitive molecular tests identified 2.5 times more infections than microscopy, classifying these infections as submicroscopic.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [12] Campos, 2011, Diagnosis of gestational, congenital, and placental malaria in Colombia: comparison of the efficacy of microscopy, nested polymerase chain reaction, and histopathology

      Not checked in the free run.

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

    Premisecitation
    § Materials and Methods

    P. vivax is reported in approximately 70% of malaria cases in the Urabá-Altos Sinú-San Jorge-Bajo Cauca region.

    “P. vivax is reported in approximately 70% of cases.24,25”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [24] Antioquia, 2010

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    • cites [25] Córdoba, 2009

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductreasoning
    § Materials and Methods

    From the entire list of 2,550 women, 96 women were selected using a simple random sampling without replacement method.

    “From the entire list of 2,550 women, 96 women were selected using a simple random sampling without replacement method in accordance with the inclusion criteria (see below).”
    Quote in the paperSubstantial claim

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

    Study design and conductcitation
    § Materials and Methods

    Positive samples were further confirmed by nested and seminested PCR to amplify other sequences within the 18S gene and other microsatellite and gene regions.

    “Positive samples were further confirmed by nested and seminested PCR to amplify other sequences within the 18S gene30 and other microsatellite and gene regions.31–33”
    Quote in the paperNot a substantial claim0 of 4 sources checked
    • cites [30] Snounou, 1993, High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction

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    • cites [31] Anderson, 1999, Twelve microsatellite markers for characterization of Plasmodium falciparum from finger-prick blood samples

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    • cites [32] Felger, 2008, msp2 genotyping of Plasmodium falciparum by capillary electrophoresis and GeneMapper® Program

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    • cites [33] Koepfli, 2009, Evaluation of Plasmodium vivax genotyping markers for molecular monitoring in clinical trials

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  • May combine two claims.

    Premisecitation
    § Discussion

    Previous reports in Colombia on the frequency of malaria infection during pregnancy or at delivery were carried out in municipalities of Urabá; according to microscopy, the frequency of malaria infection in maternal peripheral blood was 11-14%, in placental blood 9-12%, and in cord blood 2-4%.

    “The few previous reports in Colombia on the frequency of malaria infection during pregnancy or at delivery were carried out in municipalities of Urabá; according to microscopy, the frequency of malaria infection in maternal peripheral blood was 11–14%, the frequency of malaria infection in placental blood was 9–12%, and the frequency of malaria infection in cord blood was 2–4%.11,12,41,42”
    Quote in the paperSubstantial claim0 of 4 sources checked
    • cites [11] Carmona-Fonseca, 2009, Incidencia de las malarias gestacional, congénita y placentaria en Urabá (Antioquia, Colombia), 2005–2007

      Not checked in the free run.

    • cites [12] Campos, 2011, Diagnosis of gestational, congenital, and placental malaria in Colombia: comparison of the efficacy of microscopy, nested polymerase chain reaction, and histopathology

      Not checked in the free run.

    • cites [41] Carmona-Fonseca, 2010, Now ICT malaria Pf/Pv® frente a microscopía (gota gruesa-extendido) para diagnóstico de malaria en Urabá (Colombia)

      Not checked in the free run.

    • cites [42] Piñeros-Jiménez, 2011, Congenital malaria in Urabá, Colombia

      Not checked in the free run.

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

    Premisecitation
    § Discussion

    The Brazilian study showed that the ratio of P. falciparum to P. vivax changed in pregnant women from 1:5.6 to 1:2.3, and in Peru, pregnant women were 2.3 times more likely to be infected with P. falciparum than non-pregnant women.

    “The Brazilian study showed that the ratio of P. falciparum to P. vivax changed in pregnant women from 1:5.6 to 1:2.3,43 and in Peru, pregnant women were 2.3 times more likely to be infected with P. falciparum than non-pregnant women.44”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [43] Martínez-Espinosa, 2004, Malaria during pregnancy in a reference centre from the Brazilian Amazon: unexpected increase in the frequency of Plasmodium falciparum infections

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    • cites [44] Padilla, 1997, Gestación y Malaria

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

    Premisecitation
    § Discussion

    Other reports show increased risk of maternal anemia in submicroscopic infections compared with uninfected women.

    “Other reports also show increased risk of maternal anemia in submicroscopic infections compared with uninfected women46,47; however, those studies were carried out in Africa, where P. falciparum is dominant and the intensity of transmission is very high, unlike in Latin America.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [46] Mayor, 2009, Sub-microscopic infections and long-term recrudescence of Plasmodium falciparum in Mozambican pregnant women

      Not checked in the free run.

    • cites [47] Mayor, 2012, How hidden can malaria be in pregnant women? Diagnosis by microscopy, placental histology, polymerase chain reaction and detection of histidine-rich protein 2 in plasma

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  • May combine two claims.

    Interpretationown data
    § Discussion

    Detection by nested PCR was limited by the sensitivity of the assay and Poisson distribution of template in solution, given that the majority of infections had < 2 DNA copies/μL.

    “Given that the majority of infections had < 2 DNA copies/μL, detection by nested PCR was limited by the sensitivity of the assay and Poisson distribution of template in solution.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation
    § Discussion

    One study using nested PCR in addition to microscopy found that the frequency of infection increased from 13% to 32% in peripheral blood, from 9% to 26% in placenta, and from 2% to 13% in cord blood.

    “One study used nested PCR in addition to microscopy to diagnose malaria infection in the three compartments, and the frequency of infection increased markedly from 13% to 32% in peripheral blood, from 9% to 26% in placenta, and from 2% to 13% in cord blood.12”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [12] Campos, 2011, Diagnosis of gestational, congenital, and placental malaria in Colombia: comparison of the efficacy of microscopy, nested polymerase chain reaction, and histopathology

      Not checked in the free run.

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

    Study design and conductnone given
    § Discussion

    One of the limitations of this study is the small sample size.

    “One of the limitations of this study is the small sample size.”
    Quote in the paperNot a substantial claim

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

    Premisecitation
    § Discussion

    There are reports from the Brazilian and Peruvian Amazon that pregnant women are at higher risk of P. falciparum infection compared with the general population.

    “However, there are reports from the Brazilian and Peruvian Amazon that pregnant women are at higher risk of P. falciparum infection compared with the general population.43–45”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [43] Martínez-Espinosa, 2004, Malaria during pregnancy in a reference centre from the Brazilian Amazon: unexpected increase in the frequency of Plasmodium falciparum infections

      Not checked in the free run.

    • cites [44] Padilla, 1997, Gestación y Malaria

      Not checked in the free run.

    • cites [45] Ramal Ayasag, 2008, Malaria en gestantes entre marzo del 2002 y julio del 2003: experiencia en el Hospital Regional de Loreto, Peru

      Not checked in the free run.

43 of 43

  • The paper relies on this without support.

    There are no official reports on the prevalence of Plasmodium infection within the pregnant population in Colombia.

    “There are no official reports on the prevalence of infection within the pregnant population in Colombia.”

  • The paper relies on this without support.

    No national malaria control strategies specific for pregnant women have been implemented in the region, and the use of bed nets is uncommon.

    “No national malaria control strategies specific for pregnant women have been implemented, and the use of bed nets is uncommon.”

  • The paper relies on this without support.

    The three hospitals are public institutions that provide equivalent primary-level healthcare, servicing populations with comparable demographics and socioeconomic status in the region.

    “The three hospitals are public institutions that provide equivalent primary-level healthcare, servicing populations with comparable demographics and socioeconomic status in the region.”

  • The paper relies on this without support.

    In Latin America, both P. falciparum and P. vivax are endemic in areas of low, unstable transmission.

    “In Latin America, both P. falciparum and P. vivax are endemic in areas of low, unstable transmission.”

  • The paper relies on this without support.

    This pilot study is the first in Latin America to evaluate malaria in pregnancy using qPCR diagnostics.

    “This pilot study is the first in Latin America to evaluate malaria in pregnancy using qPCR diagnostics.”

  • The paper relies on this without support.

    The study was sufficiently powered to detect significant findings in the study population.

    “Nevertheless, the study was sufficiently powered to detect significant findings in the study population”
6 of 6

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?

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.

  • Microscopy P. vivax percentage is misstated

    Minor

    Table 2 reports 17 P. vivax-positive samples among 20 microscopy-positive samples across all compartments, which is 85%, not 75%.

    Reported 75 · recomputed 85

  • Histology negative-group counts conflict

    Minor

    The text first says histology was available for 26 women negative for placental infection, then says it was available for 28 women negative for plasmodial infection altogether. Women negative for infection altogether must also be negative for placental infection.

  • Primiparous birth-weight difference is called significant despite P = 0.086

    Minor

    The reported P value for the primiparous-versus-multiparous comparison exceeds the paper's stated significance threshold, so that comparison cannot support the claim of a significant difference.

  • Microscopic-group syncytial-knot percentage does not match its count

    Minor

    Table 3 lists 4 cases among 13 women in the microscopic-infection group. That is about 31%, not 39%.

    Reported 39 · recomputed 30.769231

4 of 4

Cites

Flagged first, then by citations

8 of the 50 references couldn’t be matched to a known paper.

Research works printed but not linked: 1

  1. Arango, 2010, Effect of submicroscopic or polyclonal Plasmodium falciparum infection on mother and gestation product: systematic review, 13, 373

Cited by

Sorted by citations

Related

Authors
Arango, E. M., Samuel, R., Agudelo, O. M., Carmona-Fonseca, J., Maestre, A., & Yanow, S. K.
Affiliations
Universidad de Antioquia (CO)
ORCID
Venue
The American Society of Tropical Medicine and Hygiene
Publisher
American Society of Tropical Medicine and Hygiene
Published
2013-07-10
Volume
89
Issue
1
Pages
178-183
ISSN
  • 0002-9637 (ISSN-L)
  • 1476-1645
DOI
10.4269/ajtmh.12-0669
PMC
PMC3748479
OpenAlex
W2123842569
Semantic Scholar
5ccad582366ba07e4f8a792c310dbd73c8cae795
Cited by
55
References
50
Citations by year
2026: 1 · 2025: 1 · 2024: 1 · 2023: 3 · 2022: 8 · 2021: 5 · 2020: 4 · 2019: 4 · 2018: 3 · 2017: 6 · 2016: 2 · 2015: 7 · 2014: 8 · 2013: 2
FWCI
6.46
Type
journal article
Language
en
Open access
Locations
  • American Journal of Tropical Medicine and Hygiene (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
Canadian Institutes of Health Research (115440_1)
Topics
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
  • Life Sciences › Immunology and Microbiology › Parasitology › Bird parasitology and diseases
  • Health Sciences › Medicine › Genetics › Hemoglobinopathies and Related Disorders
Keywords
malaria in pregnancy, submicroscopic malaria infection, Plasmodium falciparum, Plasmodium vivax, placental malaria, umbilical cord blood, maternal malaria, malaria epidemiology
MeSH terms
Adolescent, Adult, Colombia, Cross-Sectional Studies, Female, Humans, Malaria, Placenta, Plasmodium falciparum, Plasmodium vivax, Pregnancy, Pregnancy Complications, Parasitic, Malaria, Falciparum, Malaria, Vivax, Infectious Disease Transmission, Vertical, Young Adult

About these checks

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.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-10.

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

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

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