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Cited by 52Malaria Research and ControlGlobal Maternal and Child HealthPregnancy and preeclampsia studies

Risk factors for malaria and adverse birth outcomes in a prospective cohort of pregnant women resident in a high malaria transmission area of Papua New Guinea

Open access
Stanisic, Danielle I., Moore, Kerryn A., Baiwog, Francesca, Ura, Alice, Clapham, Caroline, King, Christopher L., Siba, Peter M., Beeson, James G. +3 more·2015·Transactions of The Royal Society of Tropical Medicine and Hygiene
DOI 10.1093/trstmh/trv019PMC PMC6592412
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Abstract

BACKGROUND: Low birth weight (LBW), anaemia and malaria are common in Papua New Guinean women. METHODS: To identify risk factors for LBW, anaemia and preterm delivery (PTD), pregnant women recruited into a cohort study in Madang, Papua New Guinea, were followed to delivery. RESULTS: Of 470 women enrolled, delivery data were available for 328 (69.7%). By microscopy, 34.4% (113/328) of women had malaria parasitaemia at enrolment and 12.5% (41/328) at delivery; at each time point, PCR detected sub-microscopic parasitaemia in substantially more. Most infections were with Plasmodium falciparum; the remainder being predominantly P. vivax. Anaemia and smoking were associated with lower birth weight, and LBW (16.7%; 51/305) and PTD (21.8%; 63/290) were common. Histopathologically diagnosed chronic placental malaria was associated with LBW (adjusted odds ratio [aOR] 3.3; p=0.048) and PTD (aOR 4.2; p=0.01). Lack of maternal education predisposed to PTD. Sub-microscopic parasitaemia at delivery appeared to increase the risk of LBW. Of the genetic polymorphisms, Southeast Asian ovalocytosis, α(+)-thalassaemia and complement receptor 1 (CR1) deficiency, a CR1 heterozygous genotype was associated with decreased risk of anaemia and substantial but non-significant effects were noted in other comparisons. CONCLUSIONS: In coastal Papua New Guinea, malaria and anaemia are important causes of adverse pregnancy outcomes.

AI snapshot

Written from the paper’s full text.

TL;DR

In a prospective cohort of pregnant women in coastal Papua New Guinea, malaria and anaemia were common and chronic placental malaria was associated with low birth weight and preterm delivery. Sub-microscopic infection at delivery also appeared to increase low birth weight risk, while common red cell polymorphisms showed limited or non-significant associations with malaria risk.

Key findings

  • Among 328 women with delivery data, 34.4% (113/328) had malaria parasitaemia by microscopy at enrolment and 12.5% (41/328) at delivery; PCR detected substantially more infections, with half to two-thirds being sub-microscopic.
  • Chronic placental malaria was associated with low birth weight (adjusted OR 3.3; p=0.048) and preterm delivery (adjusted OR 4.2; p=0.01).
  • Low birth weight occurred in 16.7% (51/305) and preterm delivery in 21.8% (63/290); anaemia and smoking were associated with lower birth weight, and lack of maternal education predisposed to preterm delivery.
  • Sub-microscopic parasitaemia at delivery was associated with more low birth weight deliveries (20/85, 24%) than in uninfected women (14/110, 12.7%; OR 2.41; p=0.054), and CR1 heterozygous genotype was associated with decreased anaemia risk (OR 0.36; p=0.048).

Methods

  • Prospective cohort study conducted September 2005–October 2007 at the Antenatal Clinic, Alexishafen Health Centre, Madang province, Papua New Guinea; pregnant women >16 years were enrolled at first antenatal visit and followed to delivery.
  • Of 470 women enrolled, delivery data were available for 328 (69.7%); analyses used enrolment and delivery visits only due to missing data.
  • Malaria was assessed by microscopy, PCR/LDR-FMA, and placental histology; haemoglobin and red cell polymorphisms (SAO, CR1, α+-thalassaemia) were measured, and logistic and linear regression models identified risk factors for maternal and infant outcomes.

Limitations

  • The paper states that a convenience sample was recruited, with no information on non-enrolled women, and that malaria or anaemia may be greater problems in more poorly served communities.
  • The paper states that delivery data were available for only 70% of enrolled women, many delivered at home, and the modest sample size limited power to detect significant associations; large non-significant effects may conceal true associations.
  • Evident from the text: malaria prophylaxis was not monitored, gestational age was estimated by fundal height and Ballard scores rather than early ultrasound, and only enrolment and delivery visits were analysed because of missing data.

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

Integrity signals

Registry

Crossref · 10.1093/trstmh/trv019

Cites

32 of 32 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 31 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    Lack of maternal education predisposed to preterm delivery.

    “Lack of maternal education predisposed to PTD.”
    • Also stated in: § Risk factors for adverse infant outcomes-birth weight, low birth weight and preterm birth · plain
      “Preterm birth was significantly less common in women who had had either primary (OR 0.22; p¼0.0072) or secondary education (OR 0.13; p,0.001).”
    Quote in the paperSubstantial claim
  • Findingown data

    Smoking was associated with lower birth weight.

    “Anaemia and smoking were associated with lower birth weight”
    • Also stated in: § Risk factors for adverse infant outcomes-birth weight, low birth weight and preterm birth · plain
      “In adjusted analyses, factors that were independently associated with birth weight included gravidity (p,0.001),smoking (p¼0.005) and SAO genotype.Multigravid women had babies that were on average 325 g heavier than primigravidae (p,0.001), while smokers' babies were 197 g lighter than nonsmokers' (Table 4).”
    Quote in the paperSubstantial claim
  • Findingown data

    PCR detected sub-microscopic parasitaemia in substantially more women than microscopy at each time point.

    “at each time point, PCR detected sub-microscopic parasitaemia in substantially more.”
    • Also stated in: § Prevalence of malaria infection · plain
      “More women were infected as determined by PCR than by microscopy (Table 2).Half the infections detected at enrolment, and two-thirds of infections at delivery, were sub-microscopic.”
    Quote in the paperNot a substantial claim
  • Findingown data

    A CR1 heterozygous genotype was associated with decreased risk of anaemia.

    “a CR1 heterozygous genotype was associated with decreased risk of anaemia”
    • Also stated in: § Risk factors for maternal haemoglobin and anaemia at delivery · plain
      “In adjusted analyses, Transactions of the Royal Society of Tropical Medicine and Hygiene the CR1 HL genotype was associated with protection against anaemia (OR 0.36; p¼0.048), but not with Hb levels (p¼0.50).”
    Quote in the paperNot a substantial claim
  • Findingown data

    At delivery, 12.5% (41/298) of women had peripheral malaria parasitaemia by microscopy.

    “At enrolment, 113/328 women (34.4%) had peripheral parasitaemia by microscopy, which decreased to 41/298 (12.5%) at delivery (p,0.001).”
    • Also stated in: § Abstract · plain
      “By microscopy, 34.4% (113/328) of women had malaria parasitaemia at enrolment and 12.5% (41/328) at delivery; at each time point, PCR detected sub-microscopic parasitaemia in substantially more.”
    Quote in the paperNot a substantial claim
  • May combine two claims. 40
  • Classified as probably not a substantial claim. 29

  • May combine two claims.

    Findingown data

    Most malaria infections were with Plasmodium falciparum; the remainder were predominantly P. vivax.

    “Most infections were with Plasmodium falciparum; the remainder being predominantly P. vivax.”
    • Also stated in: § Prevalence of malaria infection · plain
      “In peripheral blood, P. falciparum was detected in 105/113 (92.9%) parasitaemic women at enrolment, and 35/41 (85%) at delivery.Additionally, 39/44 (89%) positive placental smears showed infection with P. falciparum (Table 2).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Most participants reported using bed nets that were not impregnated with insecticides, and although bed net users were less commonly parasitaemic at delivery, this did not translate into decreases in low birth weight or preterm delivery.

    “Most participants reported using bed nets that were not impregnated with insecticides, and although bed net users were less commonly parasitaemic at delivery, this did not translate into decreases in LBW or preterm delivery.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Haemoglobin concentration was not significantly associated with low birth weight or preterm delivery.

    “Higher Hb at enrolment was associated with higher birth weight (61 g per 1 g/dl increase in Hb; p¼0.005), but Hb concentration was not significantly associated with LBW or preterm delivery.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    High-low (HL) and low-low (LL) CR1 genotypes reduced the odds of preterm birth by almost 50%, but had no effect on the odds of low birth weight compared to the normal high-high (HH) genotype.

    “Large magnitudes of effect with adverse infant outcomes were observed for CR1 and a + -thalassaemia genotypes but these were not statistically significant; high-low (HL) and low-low (LL) CR1 genotypes reduced the odds of preterm birth by almost 50%, but had no effect on the odds of LBW compared to the normal high-high (HH) genotype.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    There were non-significant but substantial associations between SAO and protection from anaemia (p=0.057), and between CR1 LL homozygosity and protection from anaemia (p=0.081).

    “There were non-significant but substantial associations between SAO and protection from anaemia (p¼0.057), and between CR1 LL homozygosity and protection from anaemia (p¼0.081).”
    Quote in the paperNot a substantial claim

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

    Findingown data

    The median gestational age was 38 (interquartile range 37-40) weeks.

    “Mean (SD) birth weight was 2870 (480) grams and the median (interquartile range) gestational age was 38 (37-40) weeks.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Malaria prophylaxis was not highly effective, with parasitaemia detected in peripheral and/or placental blood at delivery in 24% of women.

    “Malaria prophylaxis was not highly effective, with parasitaemia detected in peripheral and/or placental blood at delivery in 24% of women.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Febrile symptoms were associated with lower birth weight in unadjusted analyses, but there was no association between febrile symptoms and malaria as determined by microscopy or PCR.

    “Febrile symptoms were associated with lower birth weight in unadjusted analyses, but there was no association between febrile symptoms and malaria as determined by microscopy or PCR.”
    Quote in the paperSubstantial claim

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

    Findingown data

    Of 328 women, 47 (14.3%) had the SAO polymorphism.

    “Red cell polymorphisms associated with malaria in PNG were common: of 328 women, 47 (14.3%) had the SAO polymorphism; 297 (90.5%) had genotypes associated with intermediate or low CR1 expression on erythrocytes and 265 (80.7%) were heterozygous or homozygous for a + -thalassaemia (Table 1).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    In adjusted analyses, the CR1 HL genotype was associated with protection against anaemia (OR 0.36; p=0.048), but not with haemoglobin levels (p=0.50).

    “In adjusted analyses, Transactions of the Royal Society of Tropical Medicine and Hygiene the CR1 HL genotype was associated with protection against anaemia (OR 0.36; p¼0.048), but not with Hb levels (p¼0.50).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Malaria parasitaemia diagnosed by light microscopy was not associated with birth weight or low birth weight.

    “Malaria parasitaemia diagnosed by light microscopy was not associated with birth weight or LBW, but features of chronic placental infection on placental histology were associated with LBW and with preterm birth.”
    Quote in the paperSubstantial claim

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

    Findingown data

    Of 328 women, 297 (90.5%) had genotypes associated with intermediate or low CR1 expression on erythrocytes.

    “Red cell polymorphisms associated with malaria in PNG were common: of 328 women, 47 (14.3%) had the SAO polymorphism; 297 (90.5%) had genotypes associated with intermediate or low CR1 expression on erythrocytes and 265 (80.7%) were heterozygous or homozygous for a + -thalassaemia (Table 1).”
    Quote in the paperNot a substantial claim

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

    Findingown data

    Of 328 women, 265 (80.7%) were heterozygous or homozygous for alpha+-thalassaemia.

    “Red cell polymorphisms associated with malaria in PNG were common: of 328 women, 47 (14.3%) had the SAO polymorphism; 297 (90.5%) had genotypes associated with intermediate or low CR1 expression on erythrocytes and 265 (80.7%) were heterozygous or homozygous for a + -thalassaemia (Table 1).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingnone given

    Up to two-thirds of pregnant women living in an area of high malaria transmission of coastal PNG had malaria infection at the first antenatal visit and almost one-half at delivery.

    “Up to two-thirds of pregnant women living in an area of high malaria transmission of coastal PNG had malaria infection at the first antenatal visit and almost one-half at delivery.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    CR1 and alpha+-thalassaemia polymorphisms were not significantly associated with birth weight, or with risk of LBW and preterm birth.

    “CR1 and a + -thalassaemia polymorphisms were not significantly associated with birth weight, or with risk of LBW and preterm birth.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingnone given

    Host genetics were associated with haemoglobin levels and pregnancy outcomes, but not with malaria risk.

    “Host genetics were associated with Hb levels and pregnancy outcomes, but not with malaria risk.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    In this cohort, one-third of women had sub-microscopic malaria infection at first presentation, and a similar number at delivery.

    “In this cohort, one-third of women had sub-microscopic malaria infection at first presentation, and a similar number at delivery.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Malaria prevalence by microscopy at enrolment was 34% for all species and at delivery was 14%.

    “All species | 113 (34) | 41 (14) | 222 (229, 215) | ,0.001”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    PCR prevalence of all species at enrolment was 66% and at delivery was 47%.

    “All species | 217 (66) | 110 (47) | 218 (228, 8.9) | ,0.001”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Severe anaemia prevalence at enrolment was 34% and at delivery was 23%.

    “Severe anaemia (,8 g/dl) | 112 (34) | 68 (23) | 211 (217, 24.3) | 0.001”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    SAO was associated with a non-significant increase in risk of low birth weight, and decrease in mean birth weight (but not preterm birth).

    “SAO was associated with a non-significant increase in risk of LBW, and decrease in mean birth weight (but not preterm birth).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingreasoning

    The prevalence of preterm delivery was 21.7%, whereas it was estimated at 6-10% in other studies, probably due to differences in sensitivity of dating techniques used.

    “The prevalence of preterm delivery was 21.7%, whereas it was estimated at 6-10% in other studies, 6,7 probably due to differences in sensitivity of dating techniques used.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [6] Allen, 1998, Causes of preterm delivery and intrauterine growth retardation in a malaria endemic region of Papua New Guinea, Arch Dis Child Fetal Neonatal Ed source

      Not checked in the free run.

    • cites [7] Brabin, 1990, Consequences of maternal anaemia on outcome of pregnancy in a malaria endemic area in Papua New Guinea, Ann Trop Med Parasitol source

      Not checked in the free run.

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

    Premisecitation

    P. vivax placental infection has been reported, but P. falciparum is a more important cause of poor pregnancy outcomes.

    “P. vivax placental infection has been reported, 9 but P. falciparum is a more important cause of poor pregnancy outcomes.1”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [9] Mayor, 2012, Placental infection with Plasmodium vivax: a histopathological and molecular study, J Infect Dis source

      Not checked in the free run.

    • cites [1] Dellicour, 2010, Quantifying the number of pregnancies at risk of malaria in 2007: a demographic study, PLoS Med source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    In coastal Papua New Guinea, malaria and anaemia are important causes of adverse pregnancy outcomes.

    “In coastal Papua New Guinea, malaria and anaemia are important causes of adverse pregnancy outcomes.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Primigravid women are more susceptible to malaria than multigravid women, who typically develop pregnancy-specific immunity, including antibodies to pregnancy-specific parasite variants that confer protection against placental malaria in subsequent pregnancies.

    “Further, primigravid women are more susceptible than multigravid women, who typically develop pregnancy-specific immunity, including antibodies to pregnancy-specific parasite variants that confer protection against placental malaria in subsequent pregnancies.3”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [3] Fried, 1998, Maternal antibodies block malaria, Nature source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductown data

    Of 470 women enrolled, delivery data were available for 328 (69.7%).

    “Of 470 women enrolled, delivery data were available for 328 (69.7%).”
    • Also stated in: § Study cohort · plain
      “Table 1 shows the baseline characteristics of the 470 pregnant women recruited, and of the 328 women (69.7%) with delivery information.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Pregnant women are more susceptible to malaria than non-pregnant adults partly due to the emergence of pregnancy-specific antigenic variants of Plasmodium falciparum that accumulate in the placenta.

    “Pregnant women are more susceptible to malaria than non-pregnant adults partly due to the emergence of pregnancy-specific antigenic variants of Plasmodium falciparum that accumulate in the placenta.2”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [2] Rogerson, 2007, Malaria in pregnancy: pathogenesis and immunity, Lancet Infect Dis source

      Not checked in the free run.

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

    Premisecitation

    The consequences of malaria during pregnancy include maternal deaths due to severe anaemia, and low birth weight babies who have increased perinatal and infant mortality.

    “The consequences of malaria during pregnancy include maternal deaths due to severe anaemia, and low birth weight babies (LBW; ,2500 grams) who have increased perinatal and infant mortality.4”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [4] Desai, 2007, Epidemiology and burden of malaria in pregnancy, Lancet Infect Dis source

      Not checked in the free run.

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

    Premisecitation

    Malaria in pregnancy due to P. falciparum and P. vivax is common in coastal Papua New Guinea, and its greatest impact on birth weight is in primigravid women.

    “Malaria in pregnancy due to P. falciparum and P. vivax is common, 6 and its greatest impact on birth weight is in primigravid women.[6][7][8]”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [6] Allen, 1998, Causes of preterm delivery and intrauterine growth retardation in a malaria endemic region of Papua New Guinea, Arch Dis Child Fetal Neonatal Ed source

      Not checked in the free run.

    • cites [6][7][8]

      Not checked in the free run.

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

    Premisecitation

    Coastal Papua New Guinea experiences some of the highest levels of malaria transmission outside of Africa.

    “Coastal Papua New Guinea (PNG) experiences some of the highest levels of malaria transmission outside of Africa.5”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [5] WHO, 2014

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductown data

    Due to missing data, only enrolment and delivery visits are analysed.

    “Due to missing data, only enrolment and delivery visits are analysed here.”
    Quote in the paperSubstantial claim

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

    Study design and conductown data

    Of 377 women (80.2%) who returned at delivery, 6 women with multiple births and 43 who were not seen ≤3 days after delivery were excluded.

    “Of 377 women (80.2%; 377/470) who returned at delivery, we excluded 6 women with multiple births and 43 who were not seen ≤3 days after delivery.”
    Quote in the paperSubstantial claim

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

    Interpretationnone given

    The increase in haemoglobin levels between enrolment and delivery may reflect combined effects of malaria prophylaxis and iron and folate supplementation.

    “The increase in Hb levels between enrolment and delivery may reflect combined effects of malaria prophylaxis and iron and folate supplementation.”
    Quote in the paperNot a substantial claim

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

    Study design and conductreasoning

    Age and parity showed collinearity with gravidity, which was retained because of well-established differences in risk of malaria during pregnancy between primigravidae and multigravidae.

    “Age and parity showed collinearity with gravidity, which was retained because of well-established differences in risk of malaria during pregnancy between primigravidae and multigravidae.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    The reductions in birth weight in first pregnancies translated into a high rate of low birth weight and preterm birth delivery in primigravid women, possibly due to their lack of pregnancy-specific immunity or the lower general risk of low birth weight associated with increased gravidity.

    “The reductions in birth weight in first pregnancies translated into a high rate of LBW and preterm birth delivery in primigravid women, possibly due to their lack of pregnancyspecific immunity, 2 or the lower general risk of LBW associated with increased gravidity.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [2] Rogerson, 2007, Malaria in pregnancy: pathogenesis and immunity, Lancet Infect Dis source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    The decrease in peripheral blood parasite prevalence at delivery associated with bed net use is consistent with insecticide treated bed net studies from Africa, but bed net use and ownership might be a proxy for higher socio-economic status, better housing and decreased vector exposure, rather than directly mediating decreased malaria prevalence.

    “The decrease in peripheral blood parasite prevalence at delivery associated with bed net use is consistent with insecticide treated bed net studies from Africa, 28 but bed net use and ownership might be a proxy for higher socio-economic status, better housing and decreased vector exposure, rather than directly mediating decreased malaria prevalence.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [28] Gamble, 2007, Insecticide-treated nets for the prevention of malaria in pregnancy: a systematic review of randomised controlled trials, PLoS Med source

      Not checked in the free run.

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

    Premisecitation

    Chloroquine resistance in P. falciparum is common in PNG, with chloroquine resistant P. vivax also well described.

    “Chloroquine resistance in P. falciparum is common in PNG, with chloroquine resistant P. vivax also well described.25”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [25] Karunajeewa, 2008, A trial of combination antimalarial therapies in children from Papua New Guinea, N Engl J Med source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Prospective studies of malaria in pregnancy from the area are rare; the most recent was performed in the 1980s, when malaria prevalence was significantly higher than at present.

    “Prospective studies of malaria in pregnancy from the area are rare; the most recent was performed in the 1980s, when malaria prevalence was significantly higher than at present.7”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [7] Brabin, 1990, Consequences of maternal anaemia on outcome of pregnancy in a malaria endemic area in Papua New Guinea, Ann Trop Med Parasitol source

      Not checked in the free run.

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

    Premisecitation

    Previous studies from the area do show gravidity-dependent susceptibility to malaria, and the gravidity-associated acquisition of antibodies to multiple different placental-binding P. falciparum isolates.

    “Previous studies from the area do show gravidity-dependent susceptibility to malaria, 23 and the gravidity-associated acquisition of antibodies to multiple different placental-binding P. falciparum isolates.24”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [23] Rijken, 2012, Malaria in pregnancy in the Asia-Pacific region, Lancet Infect Dis source

      Not checked in the free run.

    • cites [24] Hommel, 2010, Evaluation of the antigenic diversity of placenta-binding Plasmodium falciparum variants and the antibody repertoire among pregnant women, Infect Immun source

      Not checked in the free run.

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

    Study design and conductnone given

    Prophylaxis was not monitored.

    “Prophylaxis was not monitored.”
    Quote in the paperNot a substantial claim

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

    Premisecitation

    Previous observations in PNG demonstrate the earlier acquisition of immunity to P. vivax than to P. falciparum due to high force of infection.

    “Previous observations in PNG demonstrate the earlier acquisition of immunity to P. vivax than to P. falciparum due to high force of infection.20”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [20] Koepfli, 2013, A high force of Plasmodium vivax blood-stage infection drives the rapid acquisition of immunity in Papua New Guinean children, PLoS Negl Trop Dis source

      Not checked in the free run.

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

    Premisecitation

    There also appears to be a greater increase in pregnancy-associated susceptibility to P. falciparum than to P. vivax.

    “There also appears to be a greater increase in pregnancy-associated susceptibility to P. falciparum than to P. vivax.21”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [21] Martinez-Espinosa, 2004, Malaria during pregnancy in a reference centre from the Brazilian Amazon: unexpected increase in the frequency of Plasmodium falciparum infections, Mem Inst Oswaldo Cruz source

      Not checked in the free run.

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

    Premisecitation

    Studies of SAO and alpha+-thalassaemia in pregnant PNG women did not show clear evidence of protection against placental malaria, but suggested a decrease in intensity of placental infection in SAO heterozygotes, particularly in first-time mothers.

    “Studies of SAO and a + -thalassaemia in pregnant PNG women did not show clear evidence of protection against placental malaria, but suggested a decrease in intensity of placental infection in SAO heterozygotes, particularly in first-time mothers.8,15,16”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [8] Benet, 2006, Placental malaria in women with South-East Asian ovalocytosis, Am J Trop Med Hyg source

      Not checked in the free run.

    • cites [15] O'Donnell, 2006, Alpha+ -thalassaemia and pregnancy in a malaria endemic region of Papua New Guinea, Br J Haematol source

      Not checked in the free run.

    • cites [16] O'Donnell, 2007, Southeast Asian ovalocytosis and pregnancy in a malaria-endemic region of Papua New Guinea, Am J Trop Med Hyg source

      Not checked in the free run.

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

    Premisecitation

    In African women, chronic placental infection (especially massive chronic intervillositis) has been particularly associated with growth restriction, while acute infection with high parasitaemia was associated with preterm delivery.

    “In African women, chronic placental infection (especially massive chronic intervillositis, the accumulation of large numbers of white cells in the maternal blood spaces of the placenta) has been particularly associated with growth restriction, while acute infection with high parasitaemia was associated with preterm delivery.26”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [26] Menendez, 2000, The impact of placental malaria on gestational age and birth weight, J Infect Dis source

      Not checked in the free run.

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

    Study design and conductnone given

    Samples were considered positive only if both species-specific primers generated a positive signal.

    “Samples were considered positive only if both species-specific primers generated a positive signal.”
    Quote in the paperNot a substantial claim

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

    Study design and conductnone given

    Blood films were examined by two independent microscopists, and discordant results were referred for a third reading to adjudicate species and density of infection.

    “Blood films were stained with Giemsa and examined by two independent microscopists.Discordant results were referred for a third reading to adjudicate species and density of infection.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Study design and conductown data

    There were no systematic differences between included women (n=328) and those who were excluded or lost to follow-up (n=142; all p>0.08), except that included women were slightly better educated (p=0.007).

    “There were no systematic differences between included women (n¼328) and those who were excluded or lost to follow-up (n¼142; all p.0.08), except that included women were slightly better educated (p¼0.007;data not shown).”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Study design and conductreasoning

    Adjusted models included all exposure variables, with some exceptions due to collinearity.

    “Adjusted models included all exposure variables, with some exceptions due to collinearity.”
    Quote in the paperSubstantial claim

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

    Premisecitation

    Several red cell genetic abnormalities are common in coastal PNG, including alpha+-thalassaemia, Southeast Asian ovalocytosis (SAO) and complement receptor 1 (CR1) deficiency, and each has been associated with protection against severe malaria, although they do not appear to protect against uncomplicated malaria, parasitaemia or parasite density.

    “Several red cell genetic abnormalities are common in coastal PNG, including a + -thalassaemia, Southeast Asian ovalocytosis (SAO) and complement receptor 1 (CR1) deficiency, and each has been associated with protection against severe malaria, [10][11][12] although they do not appear to protect against uncomplicated malaria, parasitaemia or parasite density.13,14”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [10][11][12]

      Not checked in the free run.

    • cites [13] Lin, 2010, Minimal association of common red blood cell polymorphisms with Plasmodium falciparum infection and uncomplicated malaria in Papua New Guinean school children, Am J Trop Med Hyg source

      Not checked in the free run.

    • cites [14] Fowkes, 2008, Host erythrocyte polymorphisms and exposure to Plasmodium falciparum in Papua New Guinea, Malar J source

      Not checked in the free run.

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

    Study design and conductreasoning

    A convenience sample was enrolled, and data were not available on women not enrolled.

    “As staffing was limited, a convenience sample was enrolled, and data were not available on women not enrolled.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    Due to limited statistical power, both the magnitude of associations and the p-value were considered in the interpretation of potential risk factors.

    “Due to limited statistical power, both the magnitude of associations and the p-value were considered in the interpretation of potential risk factors.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    Malaria and possibly iron deficiency may instead be responsible for the high rates of anaemia detected.

    “malaria and possibly iron deficiency may instead be responsible”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationcitation

    Previous studies in Madang have not shown a significant relationship between SAO and pregnancy outcome, and in the absence of a clear mechanism by which it might affect fetal growth it seems unlikely to be a true effect.

    “Previous studies in Madang have not shown a significant relationship between SAO and pregnancy outcome, 8,15,16 and in the absence of a clear mechanism by which it might affect fetal growth it seems unlikely to be a true effect.”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [8] Benet, 2006, Placental malaria in women with South-East Asian ovalocytosis, Am J Trop Med Hyg source

      Not checked in the free run.

    • cites [15] O'Donnell, 2006, Alpha+ -thalassaemia and pregnancy in a malaria endemic region of Papua New Guinea, Br J Haematol source

      Not checked in the free run.

    • cites [16] O'Donnell, 2007, Southeast Asian ovalocytosis and pregnancy in a malaria-endemic region of Papua New Guinea, Am J Trop Med Hyg source

      Not checked in the free run.

  • May combine two claims.

    Study design and conductown data

    Delivery data were only available on 70% of enrolled women, as many delivered at home.

    “Second, delivery data were only available on 70% of enrolled women, as many delivered at home.”
    Quote in the paperNot a substantial claim

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

    Study design and conductnone given

    A convenience sample of women living close to the health centre was recruited.

    “First, a convenience sample of women living close to the health centre was recruited”
    Quote in the paperNot a substantial claim

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

    Interpretationcitation

    The alpha+-thalassaemia observations were consistent with an earlier study.

    “The a + -thalassaemia observations were consistent with an earlier study, 15”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [15] O'Donnell, 2006, Alpha+ -thalassaemia and pregnancy in a malaria endemic region of Papua New Guinea, Br J Haematol source

      Not checked in the free run.

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

    Premisecitation

    Previous studies performed in the region showed a similar prevalence of malaria infection, low birth weight and anaemia.

    “Previous studies performed in the region showed a similar prevalence of malaria infection, LBW and anaemia.6,7”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [6] Allen, 1998, Causes of preterm delivery and intrauterine growth retardation in a malaria endemic region of Papua New Guinea, Arch Dis Child Fetal Neonatal Ed source

      Not checked in the free run.

    • cites [7] Brabin, 1990, Consequences of maternal anaemia on outcome of pregnancy in a malaria endemic area in Papua New Guinea, Ann Trop Med Parasitol source

      Not checked in the free run.

57 of 57

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.

  • Bed-net use percentage does not match its count

    Minor

    The stated 234 of 321 women is 72.9%, rather than 75%.

    Reported 75 · recomputed 72.897196

  • Delivery microscopy prevalence uses the wrong denominator

    Minor

    The stated 41 infections among 298 women correspond to 13.8%, not 12.5%. The table reports this count as approximately 14%.

    Reported 12.5 · recomputed 13.758389

2 of 2

Cites

Flagged first, then by citations

Research works printed but not linked: 1

  1. WHO, 2014, World Malaria Report 2014: Papua New Guinea

Cited by

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Related

Authors
Stanisic, D. I., Moore, K. A., Baiwog, F., Ura, A., Clapham, C., King, C. L., Siba, P. M., Beeson, J. G., Mueller, I., Fowkes, F. J., & Rogerson, S. J.
Affiliations
  • Griffith University (AU)
  • Burnet Institute (AU)
  • Papua New Guinea Institute of Medical Research (PG)
  • The Royal Melbourne Hospital (AU)
  • Veterans Health Administration (US)
  • Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria 3050, Australia
Corresponding author
Rogerson, Stephen J.
ORCID
Venue
Transactions of The Royal Society of Tropical Medicine and Hygiene
Publisher
Oxford University Press (OUP)
Published
2015-03-10
Volume
109
Issue
5
Pages
313-324
ISSN
  • 0035-9203 (ISSN-L)
  • 1878-3503
DOI
10.1093/trstmh/trv019
PMC
PMC6592412
OpenAlex
W2114964953
Cited by
52
References
32
Citations by year
2025: 1 · 2024: 7 · 2023: 8 · 2022: 4 · 2021: 6 · 2020: 3 · 2019: 8 · 2018: 6 · 2017: 5 · 2016: 2 · 2015: 2
FWCI
5.36
Type
journal article
Language
en
Open access
Locations
  • Transactions of the Royal Society of Tropical Medicine and Hygiene (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Griffith Research Online (submittedVersion)
Funders
  • AusAID
  • National Health and Medical Research Council of Australia
  • Australian Research Council
  • Wellcome Trust
  • Veterans Affairs Research Service
  • the Bill & Melinda Gates Foundation's Global Health Program (# 34678)
  • NHMRC Infrastructure for Research Institutes Support Scheme
  • Victorian State Government Operational Infrastructure Support
  • NIH
Topics
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
  • Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Global Maternal and Child Health
  • Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
Keywords
malaria in pregnancy, low birth weight, preterm birth, anemia in pregnancy, placental malaria, Plasmodium falciparum, Plasmodium vivax, maternal smoking, maternal education, Southeast Asian ovalocytosis, alpha-thalassemia, genetic polymorphism, adverse birth outcomes, Madang
MeSH terms
Adolescent, Adult, Anemia, Female, Follow-Up Studies, Humans, Infant, Low Birth Weight, Infant, Newborn, Longitudinal Studies, Malaria, Papua New Guinea, Pregnancy, Pregnancy Complications, Infectious, Pregnancy Outcome, Prospective Studies, Risk Factors, Pregnancy Complications, Parasitic, Premature Birth

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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