Submicroscopic infection of placenta by Plasmodium produces Th1/Th2 cytokine imbalance, inflammation and hypoxia in women from north-west Colombia
Open accessAbstract
BACKGROUND: A large-scale study was set up in order to study the epidemiology, clinical aspects, and immunopathology of gestational and placental malaria in north-west Colombia. In this region, recent reports using a qPCR technique, confirmed frequencies of infection, by Plasmodium falciparum or Plasmodium vivax, up to 45%. Given the high rates of infection observed both in mother and placenta, a first exploratory study was proposed in order to characterize the effect on the inflammation status, tissue damage and hypoxia in Plasmodium spp. infected placentas. METHODS: A descriptive, prospective, cross-sectional design was applied to pregnant women with (PM+) and without (PM-) placental malaria. Messenger RNA expression of Fas, FasL; COX-1, COX-2, HIF, VEGF, and the cytokines IL-2, IL-4, IL-10, IFN-γ and TNF, were measured in peripheral and placental blood using a quantitative PCR. The percentage of apoptotic cells was determined with a TUNEL assay. RESULTS: In total 50 placentas were studied: 25 were positive for submicroscopic infection and 25 were negative for Plasmodium infection. Expression of IL-4 and IL-10 was observed high in placental tissue of PM+, while IL-2 was high in peripheral blood of the same group. Expression of TNF and IFNγ in peripheral blood of the PM + group was high. Similarly, the apoptotic index and Fas expression were significantly high in PM+. However, FasL expression was observed low in PM + compared to PM-. Inflammation markers (HIF, VEGF) and hypoxia markers (COX-1, COX-2) were high in the PM + group. CONCLUSION: During placental malaria expression of some pro-inflammatory cytokines is up-regulated and markers of hypoxia and tissue damage are increased in cases of submicroscopic infection.
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TL;DR
In 50 pregnant women from north-west Colombia, submicroscopic placental *Plasmodium* infection (25 qPCR-positive, microscopy-negative) was associated with higher placental and peripheral cytokine expression, increased apoptosis, and elevated hypoxia/inflammation markers compared with uninfected placentas. Similar patterns were seen for *P. falciparum* and *P. vivax*, though the study was exploratory and small.
Key findings
- Among 50 placentas, all were microscopy-negative; 25 were qPCR-positive (16 *P. falciparum*, 6 *P. vivax*, 3 mixed) and 25 were negative by both tests.
- Placental mRNA expression was higher in infected vs uninfected for IFN-γ (9.00 ± 0.811 vs 0.46 ± 0.37), TNF (6.16 ± 0.75 vs 0.83 ± 0.45), IL-4 (1.60 ± 0.40 vs 1.05 ± 0.62), and IL-10 (3.50 ± 0.93 vs 0.18 ± 0.18), all p = 0.0001; peripheral blood showed higher IL-2 (3.65 ± 1.11 vs 1.18 ± 0.50), IFN-γ (6.53 ± 2.38 vs 1.10 ± 0.72), TNF (1.53 ± 0.41 vs 0.76 ± 0.46), and IL-10 (2.45 ± 0.64 vs 0.65 ± 0.50), p = 0.0001, while peripheral IL-4 did not differ (p > 0.05).
- Apoptotic index was 62.37% ± 10.02 in infected vs 44.88% ± 2.15 in uninfected (p = 0.0001); Fas expression was higher (6.53 ± 2.49 vs 3.42 ± 0.84, p = 0.0001) and FasL lower (5.60 ± 2.13 vs 6.95 ± 1.16, p = 0.003).
- HIF (0.96 ± 1.15 vs 0.21 ± 0.22, p = 0.0001), COX-1 (6.95 ± 3.14 vs 0.73 ± 0.41, p = 0.0001), and COX-2 (2.86 ± 0.99 vs 0.42 ± 0.29, p = 0.0001) were higher in infected placentas; VEGF was not significantly different (0.14 ± 0.14 vs 0.12 ± 0.15, p > 0.05). Similar patterns were observed by species, with no differences between *P. vivax* and *P. falciparum*.
Methods
- Descriptive, prospective, cross-sectional study; subset of 50 non-matched pregnant women selected from 2,000 recruited January 2007–April 2011 at hospitals in Monteria and Puerto Libertador, Colombia; 25 with qPCR-confirmed placental infection (microscopy-negative) and 25 negative by microscopy and qPCR.
- Placental and maternal peripheral blood tested by thick smear and qPCR; mRNA expression of Fas, FasL, COX-1, COX-2, HIF, VEGF, IL-2, IL-4, IL-10, IFN-γ, and TNF measured by RT-PCR; apoptosis by TUNEL assay; non-parametric Mann–Whitney and Kruskal–Wallis tests, p < 0.05.
Limitations
- Stated: exploratory first study; small sample; authors call for larger series of *P. vivax*-infected placentas and studies of naturally acquired humoral immunity and consequences in Asia/America.
- Evident: cross-sectional design cannot establish causality; non-matched subset selected based on availability/quality of material; small species subgroups (*P. vivax* n = 6, mixed n = 3); all infections were submicroscopic and microscopy-negative, so findings may not generalize to microscopic or higher-density placental malaria.
Model-written summary. Check it against the paper before relying on it.
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Claims the paper makes
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- Findingown data
FasL expression was higher in PM- than in PM+ placentas (6.95 vs 5.60, p < 0.05).
“However, FasL expression was higher in PM- than in PM + (6.95 vs. 5.60, p < 0.05) (Table 5).”
Quote in the paperNot a substantial claim - Findingown data
In maternal peripheral blood, IL-2 mRNA expression was significantly higher in PM+ than PM- (mean ratio 3.65 vs 1.18, p=0.0001).
“Meanwhile, expression of IL-4 was high in placentas in PM+, and IL-2 was high in peripheral blood of the same group (Table 3).”
- Also stated in: § Cytokine expression in pregnant women and placentas · plain
“IL-2 | 3.65 ± 1.11 | 1.18 ± 0.50 | 0.0001”
Quote in the paperSubstantial claim- Rests on an assumption: Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
- Also stated in: § Cytokine expression in pregnant women and placentas · plain
- Findingown data
In peripheral blood, IL-2 and IFN-γ were positively correlated (rho=0.760, p=0.000, n=50).
“Other positive correlations included IL-2 and TNF (rho = 0.676, p = 0.000 n = 50), IL-2 and IFN-γ (rho = 0.760, p = 0.000 n = 50), all in peripheral blood.”
Quote in the paperNot a substantial claim- Rests on an assumption: Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
- Findingown data
VEGF expression was high in the PM+ group.
“Inflammation markers (HIF, VEGF) and hypoxia markers (COX-1, COX-2) were high in the PM + group.”
Quote in the paperSubstantial claim- Rests on an assumption: Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
- Findingown data
In placental tissue, IFN-γ mRNA expression was significantly higher in PM+ than PM- (mean ratio 9.00 vs 0.46, p=0.0001).
“In both compartments, expression of IFN-γ, TNF, and IL-10 was significantly higher in PM + when compared to PM-.”
- Also stated in: § Cytokine expression in pregnant women and placentas · plain
“IFN-γ | 9.00 ± 0.811 | 0.46 ± 0.37 | 0.0001”
Quote in the paperSubstantial claim- Rests on an assumption: Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
- Also stated in: § Cytokine expression in pregnant women and placentas · plain
- Findingown data
In placental tissue, TNF mRNA expression was significantly higher in PM+ than PM- (mean ratio 6.16 vs 0.83, p=0.0001).
“In both compartments, expression of IFN-γ, TNF, and IL-10 was significantly higher in PM + when compared to PM-.”
- Also stated in: § Cytokine expression in pregnant women and placentas · plain
“TNF | 6.16 ± 0.75 | 0.83 ± 0.45 | 0.0001”
Quote in the paperSubstantial claim- Rests on an assumption: Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
- Also stated in: § Cytokine expression in pregnant women and placentas · plain
- Findingown data
HIF expression was high in the PM+ group.
“Inflammation markers (HIF, VEGF) and hypoxia markers (COX-1, COX-2) were high in the PM + group.”
Quote in the paperSubstantial claim- Rests on an assumption: Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
- Findingown data
19 of 25 peripheral blood samples from mothers with positive placentas were also positive, either by microscopy or qPCR, for the same Plasmodium species infecting the placenta.
“Interestingly, 19/25 peripheral blood samples from mothers with positive placentas were also positive, either by microscopy or qPCR by the same Plasmodium species infecting the placenta.”
Quote in the paperNot a substantial claim - Findingown data
The differences in cytokine expression between PM+ and PM- in peripheral blood and placenta persisted when analysis was performed taking into account the infecting species.
“In general, the differences observed in expression of cytokines in peripheral blood and placenta between PM + and PM-, persisted when analysis was performed taking into account the infecting species (Table 4).”
Quote in the paperNot a substantial claim- Rests on an assumption: Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
- Findingown data
FasL negatively correlated with the remaining cytokine variables.
“Meanwhile, FasL negatively correlated with the remaining variables (Table 7).”
Quote in the paperNot a substantial claim - Findingown data
No significant correlation was observed between the expression of FasL, VEGF and IL-2 and the copies of parasite DNA.
“However, no significant correlation (p ≥ 0.078) was observed between expression of FasL, VEGF and IL-2 in relation to the copies of parasite DNA.”
Quote in the paperNot a substantial claim - Findingown data
In maternal peripheral blood, IL-10 mRNA expression was significantly higher in PM+ than PM- (mean ratio 2.45 vs 0.65, p=0.0001).
“In both compartments, expression of IFN-γ, TNF, and IL-10 was significantly higher in PM + when compared to PM-.”
- Also stated in: § Cytokine expression in pregnant women and placentas · plain
“IL-10 | 2.45 ± 0.64 | 0.65 ± 0.50 | 0.0001”
Quote in the paperSubstantial claim- Rests on an assumption: Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
- Also stated in: § Cytokine expression in pregnant women and placentas · plain
- Findingown data
No significant correlation was observed between IL-2 and any of the apoptosis, inflammation or hypoxia markers.
“No significant correlation was observed between IL-2 and any of the apoptosis/inflammation/hypoxia markers.”
Quote in the paperNot a substantial claim - Findingown data
FasL expression was lower in PM+ compared to PM-.
“However, FasL expression was observed low in PM + compared to PM-.”
Quote in the paperNot a substantial claim- Rests on an assumption: Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
- Findingown data
Mean Fas expression was significantly higher in PM+ than in PM- placentas (6.52 vs 3.42).
“Similarly, mean Fas expression was significantly higher in PM + than in PM- (6.52 vs. 3.42).”
Quote in the paperSubstantial claim - Findingown data
Fas expression was significantly higher in PM+ than PM-.
“Similarly, the apoptotic index and Fas expression were significantly high in PM+.”
Quote in the paperNot a substantial claim- Rests on an assumption: Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
- Findingown data
COX-1 expression was high in the PM+ group.
“Inflammation markers (HIF, VEGF) and hypoxia markers (COX-1, COX-2) were high in the PM + group.”
Quote in the paperSubstantial claim- Rests on an assumption: Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
- Findingown data
In placenta, IL-4 and IL-10 were positively correlated (rho=0.431, P=0.002, n=50).
“In addition, for IL-4 and IL-10 a lower (rho = 0.431, P = 0.002 with n = 50), but nevertheless significant, correlation was observed in placenta, but not in peripheral blood (rho = 0.048, P = 0.740 with n = 50).”
Quote in the paperNot a substantial claim- Rests on an assumption: Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
- Findingown data
In peripheral blood, IL-4 and IL-10 did not correlate (rho=0.048, P=0.740, n=50).
“In addition, for IL-4 and IL-10 a lower (rho = 0.431, P = 0.002 with n = 50), but nevertheless significant, correlation was observed in placenta, but not in peripheral blood (rho = 0.048, P = 0.740 with n = 50).”
Quote in the paperNot a substantial claim- Rests on an assumption: Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
- Findingown data
In placental tissue, IL-4 mRNA expression was significantly higher in PM+ than PM- (mean ratio 1.60 vs 1.05, p=0.0001).
“Meanwhile, expression of IL-4 was high in placentas in PM+, and IL-2 was high in peripheral blood of the same group (Table 3).”
- Also stated in: § Cytokine expression in pregnant women and placentas · plain
“IL-4 | 1.60 ± 0.40 | 1.05 ± 0.62 | 0.0001”
Quote in the paperSubstantial claim- Rests on an assumption: Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
- Also stated in: § Cytokine expression in pregnant women and placentas · plain
- Findingown data
In placental tissue, IL-10 mRNA expression was significantly higher in PM+ than PM- (mean ratio 3.50 vs 0.18, p=0.0001).
“In both compartments, expression of IFN-γ, TNF, and IL-10 was significantly higher in PM + when compared to PM-.”
- Also stated in: § Cytokine expression in pregnant women and placentas · plain
“IL-10 | 3.50 ± 0.93 | 0.18 ± 0.18 | 0.0001”
Quote in the paperSubstantial claim- Rests on an assumption: Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
- Also stated in: § Cytokine expression in pregnant women and placentas · plain
- Findingown data
In peripheral blood, IL-2 and TNF were positively correlated (rho=0.676, p=0.000, n=50).
“Other positive correlations included IL-2 and TNF (rho = 0.676, p = 0.000 n = 50), IL-2 and IFN-γ (rho = 0.760, p = 0.000 n = 50), all in peripheral blood.”
Quote in the paperNot a substantial claim- Rests on an assumption: Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
- Findingown data
VEGF expression did not differ significantly between PM+ and PM- placentas (0.14 vs 0.12, p > 0.05).
“| VEGF | 0,14 ± 0.14 | 0.12 ± 0.15 | >0.05 |”
Quote in the paperNot a substantial claim - Findingown data
In peripheral blood of the PM+ group, TNF and IFN-γ were positively correlated (rho=0.749, P=0.000, n=50).
“In peripheral blood of the PM + group, the cytokines TNF and IFN-γ were elevated and positively correlated (rho = 0.749, P = 0.000 with n = 50).”
Quote in the paperSubstantial claim- Rests on an assumption: Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
- Findingown data
The percentage of apoptotic cells and the expression of Fas, COX1, COX2 and HIF positively correlated with IFN-gamma, TNF, IL-4 and IL-10 in placental tissue.
“On the other hand, the percentage of apoptotic cells and the expression of Fas, COX1, COX2 and HIF positively correlated with IFN-γ, TNF, IL-4 and IL-10.”
- Also stated in: § Discussion · plain
“In the current study, increased apoptosis in infected placentas was also associated with high expression of the pro-inflammatory cytokines IFN-γ and TNF.”
Quote in the paperSubstantial claim - Also stated in: § Discussion · plain
- Findingown data
HIF expression was significantly higher in PM+ than in PM- placentas (0.96 vs 0.21, p = 0.0001).
“| HIF | 0.96 ± 1.15 | 0.21 ± 0.22 | 0.0001 |”
Quote in the paperSubstantial claim - Findingown data
COX-2 expression was high in the PM+ group.
“Inflammation markers (HIF, VEGF) and hypoxia markers (COX-1, COX-2) were high in the PM + group.”
Quote in the paperSubstantial claim- Rests on an assumption: Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
- Findingown data
In maternal peripheral blood, IL-4 mRNA expression was not significantly different between PM+ and PM- (mean ratio 1.63 vs 1.41, p>0.05).
“IL-4 | 1.63 ± 0.34 | 1.41 ± 0.50 | >0.05”
Quote in the paperNot a substantial claim- Rests on an assumption: Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
- Findingown data
In placental tissue, IL-2 mRNA expression was not significantly different between PM+ and PM- (mean ratio 1.00 vs 0.96, p>0.05).
“IL-2 | 1.00 ± 0.42 | 0.96 ± 0.30 | >0.05”
Quote in the paperNot a substantial claim- Rests on an assumption: Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
- Findingown data
In maternal peripheral blood, IFN-γ mRNA expression was significantly higher in PM+ than PM- (mean ratio 6.53 vs 1.10, p=0.0001).
“In both compartments, expression of IFN-γ, TNF, and IL-10 was significantly higher in PM + when compared to PM-.”
- Also stated in: § Cytokine expression in pregnant women and placentas · plain
“IFN-γ | 6.53 ± 2.38 | 1.10 ± 0.72 | 0.0001”
Quote in the paperSubstantial claim- Rests on an assumption: Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
- Also stated in: § Cytokine expression in pregnant women and placentas · plain
- Findingown data
The apoptotic index was significantly higher in PM+ than PM-.
“Similarly, the apoptotic index and Fas expression were significantly high in PM+.”
Quote in the paperNot a substantial claim- Rests on an assumption: Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
- Findingown data
In maternal peripheral blood, TNF mRNA expression was significantly higher in PM+ than PM- (mean ratio 1.53 vs 0.76, p=0.0001).
“In both compartments, expression of IFN-γ, TNF, and IL-10 was significantly higher in PM + when compared to PM-.”
- Also stated in: § Cytokine expression in pregnant women and placentas · plain
“TNF | 1.53 ± 0.41 | 0.76 ± 0.46 | 0.0001”
Quote in the paperSubstantial claim- Rests on an assumption: Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
- Also stated in: § Cytokine expression in pregnant women and placentas · plain
- Findingown data
Significant differences were observed between the no-infection group (Group 1) and the remaining parasite-density groups as a whole.
“In general, significant differences were observed between Group 1 and the remaining groups as a whole.”
Quote in the paperSubstantial claim - Findingown data
Analysis of apoptosis, inflammation and hypoxia markers by infecting Plasmodium species confirmed results similar to those observed between the PM+ group and non-infected placentas.
“Analysis of apoptosis, inflammation and hypoxia markers according to the Plasmodium species observed in placenta, confirmed similar results to those observed between the PM + group and non-infected placentas (Table 6).”
Quote in the paperNot a substantial claim - Findingown data
Submicroscopic placental infection by malaria parasites failed to induce major clinical effects on the mother or foetus.
“In conclusion, submicroscopic placental infection by malaria parasites failed to induce major clinical effects on mother or foetus but associated with a pro-inflammatory cytokine profile, regardless of the infecting species, and this was more evident in the placental tissue.”
Quote in the paperSubstantial claim - Findingnone given
The pro-inflammatory cytokine profile associated with submicroscopic placental infection was more evident in placental tissue.
“In conclusion, submicroscopic placental infection by malaria parasites failed to induce major clinical effects on mother or foetus but associated with a pro-inflammatory cytokine profile, regardless of the infecting species, and this was more evident in the placental tissue.”
Quote in the paperSubstantial claim - Findingown data
Higher IL-10 expression was observed in infected than in uninfected placentas.
“This hypothesis is supported in the current study by the higher expression of IL-10 observed in the infected vs. uninfected placentas.”
Quote in the paperSubstantial claim - Findingown data
No differences were observed between the changes in the markers studied in P. vivax-infected placentas and those infected with P. falciparum.
“Interestingly, no differences were observed between the changes in the markers studied in P. vivax infected placentas compared with those infected with P. falciparum.”
Quote in the paperSubstantial claim - Findingown data
Submicroscopic placental infection was associated with a pro-inflammatory cytokine profile, regardless of the infecting species.
“In conclusion, submicroscopic placental infection by malaria parasites failed to induce major clinical effects on mother or foetus but associated with a pro-inflammatory cytokine profile, regardless of the infecting species, and this was more evident in the placental tissue.”
Quote in the paperSubstantial claim - Interpretationnone given
This is the first study to report on apoptosis and tissue injury during submicroscopic placental infection.
“This is a first exploratory study on the subject in women from a region where both P. falciparum and P. vivax are endemic and is the first study to report on apoptosis and tissue injury during submicroscopic placental infection.”
Quote in the paperSubstantial claim- Rests on an assumption: Complex cellular and molecular mechanisms such as apoptosis, hypoxia and inflammation have not been evaluated in cases of placental infection by Plasmodium spp. in this endemic region.
- Study design and conductcitation
The study included subjects in whom diagnosis of infection was confirmed by qPCR.
“Based on these findings, the current study included subjects in which diagnosis of infection was confirmed by qPCR.”
Quote in the paperSubstantial claim - Premisecitation
The epidemiological characteristics and the consequences associated with submicroscopic plasmodial infection in pregnant women have been poorly evaluated.
“However, the epidemiological characteristics and the consequences associated with submicroscopic plasmodial infection in pregnant women have been poorly evaluated [19,20].”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [19] Arango E, Maestre A, Carmona J: Efecto de la infección submicroscópica o policlonal de Plasmodium falciparum sobre la madre y el producto de la gestación Revisión sistemática. Rev Bras Epidemiol. 2010, 13: 373-386. 10.1590/S1415-790X2010000300002. source
Not checked in the free run.
- cites [20] Rantala AM, Taylor SM, Trottman PA, Luntamo M, Mbewe B, Maleta K, Kulmala T, Ashorn P, Meshnick SR: Comparison of real-time PCR and microscopy for malaria parasite detection in Malawian pregnant women. Malar J. 2010, 9: 269-10.1186/1475-2875-9-269. source
Not checked in the free run.
- Premisecitation
Common histological changes associated with infection, such as basal membrane thickening, mononuclear infiltrates and presence of parasites in the intervillous space, affect oxygen transport across the placenta.
“Common histological changes associated with infection such as basal membrane thickening, mononuclear infiltrates and presence of parasites in the intervillous space, affect oxygen transport across the placenta.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [36] Takem EN, D’Alessandro U: Malaria in pregnancy. Mediterr J Hematol Infect Dis. 2013, 5: e2013010- source
Not checked in the free run.
- Interpretationreasoning
Some complications of P. vivax infection might be explained by the production of pro-inflammatory cytokines, which alter the balance at the foetal-maternal interface.
“Some complications of P. vivax infection might be explained by the production of pro-inflammatory cytokines, which alter the balance at the foetal-maternal interface.”
Quote in the paperSubstantial claim - Premisecitation
Thick smear microscopy examination failed to diagnose most placental infections at delivery in this region.
“According to a recent report [16], most placental infections at delivery in this region were sub-clinical and thick smear microscopy examination failed to diagnose them.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [16] Arango EM, Samuel R, Agudelo OM, Carmona-Fonseca J, Maestre A, Yanow SK: Molecular detection of malaria at delivery reveals a high frequency of submicroscopic infections and associated placental damage in pregnant women from Northwest Colombia. Am J Trop Med Hyg. 2013, 89: 178-183. 10.4269/ajtmh.12-0669. source
Not checked in the free run.
- Interpretationcitation
The increased COX-2 and IL-10 observed in placental infection in this study are consistent with the results reported by Sarr et al.
“These results are consistent with the findings herein reported regarding increased COX-2 and IL-10 in cases of placental infection.”
Quote in the paperNot a substantial claim - Interpretationnone given
COX-1 is reported for the first time in association with placental malaria.
“Furthermore, COX-1 is reported for the first time in association with placental malaria.”
Quote in the paperNot a substantial claim - Premisecitation
Most placental infections at delivery in this region were sub-clinical.
“According to a recent report [16], most placental infections at delivery in this region were sub-clinical and thick smear microscopy examination failed to diagnose them.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [16] Arango EM, Samuel R, Agudelo OM, Carmona-Fonseca J, Maestre A, Yanow SK: Molecular detection of malaria at delivery reveals a high frequency of submicroscopic infections and associated placental damage in pregnant women from Northwest Colombia. Am J Trop Med Hyg. 2013, 89: 178-183. 10.4269/ajtmh.12-0669. source
Not checked in the free run.
- Interpretationown data
P. vivax might be equivalent to P. falciparum in the pathophysiology of placental damage.
“The current results demonstrate that P. vivax might also be equivalent in the pathophysiology of placental damage.”
Quote in the paperSubstantial claim
- Classified as probably not a substantial claim. 24
- May combine two claims. 14
- The quote only partly states this claim. 2
Probably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataVEGF failed to correlate with the expression of any cytokine.
“Similarly, VEGF failed to correlate with the expression of any cytokine.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataPlacental parasite DNA copy number correlated positively and significantly with the percentage of apoptotic cells and the expression of Fas, COX1, COX2, HIF, IFN-gamma, TNF, IL-4 and IL-10.
“Copy number correlated positively and significantly with the percentage of apoptotic cells, and expression of Fas, COX1, COX2, HIF, IFN-γ, TNF, IL-4 and IL-10 (p = 0.000 and for IL4 p = 0.017).”
Quote in the paperSubstantial claimThe quote only partly states this claim.
Findingown dataCOX-2 expression was significantly higher in PM+ than in PM- placentas (2.86 vs 0.42, p = 0.0001).
“As for the hypoxia markers, COX-1 and COX-2, both were significantly high in the PM + group.”
Quote in the paperSubstantial claimThe quote only partly states this claim.
Findingown dataCOX-1 expression was significantly higher in PM+ than in PM- placentas (6.95 vs 0.73, p = 0.0001).
“As for the hypoxia markers, COX-1 and COX-2, both were significantly high in the PM + group.”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataIn placentas with placental malaria (PM+), the mean apoptotic index was 62.37% (range 55-79%), significantly higher than in uninfected placentas (PM-, 44.88%).
“According to TUNEL assay, the mean apoptotic index observed in the group PM + was 62.37% (range 55-79%) (Table 5), and this was significantly higher when compared with the PM- group (44.88%).”
- Also stated in: § Discussion · plain
“Importantly, the apoptotic index in the PM + placentas herein studied was higher than in PM-.”
- Also stated in: § Discussion · plain
“Finally, increased apoptosis was common in Plasmodium spp. infected placentas.”
Quote in the paperSubstantial claim- Also stated in: § Discussion · plain
May combine two claims.
Findingown dataAll fifty placentas were negative for Plasmodium spp. by microscopy, and 25 of them were positive for infection by qPCR: 16 P. falciparum, six P. vivax and three mixed infection.
“All fifty placentas were negative for Plasmodium spp. by microscopy, and 25 of them were positive for infection by qPCR: 16 P. falciparum, six P. vivax and three mixed infection.”
Quote in the paperSubstantial claimMay combine two claims.
PremisecitationIn P. falciparum, adherence of infected erythrocytes to chondroitin sulfate A (CSA) on the trophoblast surface is crucial in the pathophysiology of the disease, since parasite sequestration results in inflammatory responses that can be harmful to both the mother and the foetus.
“In the case of P. falciparum, adherence of infected erythrocytes to chondroitin sulfate A (CSA), present on the trophoblast surface, is crucial in the pathophysiology of the disease [4], since parasite sequestration results in inflammatory responses that can be harmful to both the mother and the foetus [5].”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [4] Fried M, Duffy PE: Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science. 1996, 272: 1502-1504. 10.1126/science.272.5267.1502. source
Not checked in the free run.
- cites [5] Umbers AJ, Boeuf P, Clapham C, Stanisic DI, Baiwog F, Mueller I, Siba P, King CL, Beeson JG, Glazier J, Rogerson SJ: Placental malaria-associated inflammation disturbs the insulin-like growth factor axis of fetal growth regulation. J Infect Dis. 2011, 203: 561-569. 10.1093/infdis/jiq080. source
Not checked in the free run.
May combine two claims.
Study design and conductnone givenAll studied groups came from the same malaria endemic region, which controlled for socio-epidemiological bias.
“All studied groups came from the same malaria endemic region as to control for any socio-epidemiology associated bias.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationFew reports identified a relationship between hypoxia and placental malaria.
“In addition, few reports identified a relationship between hypoxia and placental malaria [12,13], although an association between hypoxia and intrauterine growth retardation was observed in preeclampsia [14].”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [12] Boeuf P, Tan A, Romagosa C, Radford J, Mwapasa V, Molyneux ME, Meshnick SR, Hunt NH, Rogerson SJ: Placental hypoxia during placental malaria. J Infect Dis. 2008, 197: 757-765. 10.1086/526521. source
Not checked in the free run.
- cites [13] Sarr D, Aldebert D, Marrama L, Frealle E, Gaye A, Brahim HO, Niang M, Dangou JM, Mercereau-Puijalon O, Lehesran J, Jambou R: Chronic infection during placental malaria is associated with up-regulation of cycloxygenase-2. Malar J. 2010, 9: 45-10.1186/1475-2875-9-45. source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationApplication of highly sensitive molecular techniques confirmed that the frequency of low level (submicroscopic) infections is higher than expected in all endemic regions.
“However, application of highly sensitive molecular techniques confirmed that the frequency of low level (submicroscopic) infections is higher than expected in all endemic regions [16,17].”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [16] Arango EM, Samuel R, Agudelo OM, Carmona-Fonseca J, Maestre A, Yanow SK: Molecular detection of malaria at delivery reveals a high frequency of submicroscopic infections and associated placental damage in pregnant women from Northwest Colombia. Am J Trop Med Hyg. 2013, 89: 178-183. 10.4269/ajtmh.12-0669. source
Not checked in the free run.
- cites [17] McGready R, Tan SO, Ashley EA, Pimanpanarak M, Viladpai-Nguen J, Phaiphun L, Wüstefeld K, Barends M, Laochan N, Keereecharoen L, Lindegardh N, Singhasivanon P, White NJ, Nosten F: A randomised controlled trial of artemether-lumefantrine versus artesunate for uncomplicated Plasmodium falciparum treatment in pregnancy. PLoS Med. 2008, 5: e263- source
Not checked in the free run.
May combine two claims.
Interpretationown dataDuring placental malaria, expression of some pro-inflammatory cytokines is up-regulated and markers of hypoxia and tissue damage are increased in cases of submicroscopic infection.
“During placental malaria expression of some pro-inflammatory cytokines is up-regulated and markers of hypoxia and tissue damage are increased in cases of submicroscopic infection.”
Quote in the paperSubstantial claim- Rests on an assumption: Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationIn in vitro studies with cell models and placental tissue explants stimulated with pro-inflammatory cytokines, Fas and FasL expression was high.
“In in vitro studies with cell models and placental tissue explants stimulated with pro-inflammatory cytokines, the expression of Fas and FasL was high and similar to the results reported here [31].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [31] Aschkenazi S, Straszewski S, Verwer KM, Foellmer H, Rutherford T, Mor G: Differential regulation and function of the Fas/Fas ligand system in human trophoblast cells. Biol Reprod. 2002, 66: 1853-1861. 10.1095/biolreprod66.6.1853. source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductown dataHaemoglobin levels were similar in the PM+ and PM- groups.
“haemoglobin levels were similar in the two groups”
Quote in the paperNot a substantial claimClassified as probably not a substantial claim. May combine two claims.
Study design and conductnone givenPlacental infection status was defined by thick smear and real-time PCR of placental blood; positive units were microscopy-negative and qPCR-positive, and negative units were negative by both tests.
“The status of infection was defined by thick smear and real-time PCR (qPCR) of placental blood. Positive infected units were those with a negative diagnosis by microscopy and a positive qPCR result; negative units were negative by both tests.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationHaemozoin deposition and haemozoin-loaded macrophages have been implicated in the induction of inflammation in the trophoblast.
“haemozoin deposition and haemozoin-loaded macrophages have implicated in the induction of inflammation in the throphoblast [30,32].”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [30] Crocker IP, Tanner OM, Myers JE, Bulmer JN, Walraven G, Baker PN: Syncytiotrophoblast degradation and the pathophysiology of the malaria-infected placenta. Placenta. 2004, 25: 273-282. 10.1016/j.placenta.2003.09.010. source
Not checked in the free run.
- cites [32] Tkachuk AN, Moormann AM, Poore JA, Rochford RA, Chensue SW, Mwapasa V, Meshnick SR: Malaria enhances expression of CC chemokine receptor 5 on placental macrophages. J Infect Dis. 2001, 183: 967-972. 10.1086/319248. source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationA significant role for increased cytokines (TNF, IFN-γ and IL-10) and apoptosis in trophoblast damage, low birth weight and preterm delivery during placental malaria has been observed.
“A significant role for increased cytokines (TNF, IFN-γ and IL-10) and apoptosis in trophoblast damage, low birth weight and preterm delivery during placental malaria, has been observed [3].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [3] Rogerson SJ, Hviid L, Duffy PE, Leke RF, Taylor DW: Malaria in pregnancy: pathogenesis and immunity. Lancet Infect Dis. 2007, 7: 105-117. 10.1016/S1473-3099(07)70022-1. source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationSome studies concluded that complications during pregnancy and foetal death in P. falciparum placental malaria might be determined by changes in the regulation of apoptosis via Fas/FasL and increased Th1 immune responses in the syncytiotrophoblast.
“Some studies concluded that complications during pregnancy and foetal death observed in P. falciparum placental malaria might be determined by changes in the regulation of apoptosis, via Fas /FasL [9], and increased Th1 immune responses in the syncytiotrophoblast [10,11].”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites [9] Uckan D, Steele A, Cherry , Wang BY, Chamizo W, Koutsonikolis A, Gilbert-Barness E, Good RA: Trophoblasts express Fas ligand: a proposed mechanism for immune privilege in placenta and maternal invasion. Mol Hum Reprod. 1997, 3: 655-662. 10.1093/molehr/3.8.655. source
Not checked in the free run.
- cites [10] Conroy A, Serghides L, Finney C, Owino SO, Kumar S, Gowda DC, Liles WC, Moore JM, Kain KC: C5a Enhances dysregulated inflammatory and angiogenic responses to malaria in vitro: potential implications for placental malaria. PLoS One. 2009, 4: e4953-10.1371/journal.pone.0004953. source
Not checked in the free run.
- cites [11] Lucchi NW, Peterson DS, Moore JM: Immunologic activation of human syncytiotrophoblast by Plasmodium falciparum. Malar J. 2008, 7: 42-10.1186/1475-2875-7-42. source
Not checked in the free run.
May combine two claims.
InterpretationreasoningApoptosis is a host response or a downstream effect of malaria infection in the placenta.
“Taken together, these observations implicate apoptosis as a host response or a downstream effect of malaria infection in the placenta.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationIn Colombia, P. vivax represents 60-70% of the total reported malaria cases, and malaria in pregnancy constitutes a public health problem with a high frequency of submicroscopic infections.
“In Colombia, where P. vivax represents 60-70% of the total reported cases, malaria in pregnancy constitutes a public health problem [15,21] with a high frequency of submicroscopic infections [16,15].”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites [15] Campos IM, Uribe ML, Cuesta C, Franco-Gallego A, Carmona-Fonseca J, Maestre A: Diagnosis of gestational, congenital, and placental malaria in Colombia: comparison of the efficacy of microscopy, nested polymerase chain reaction, and histopathology. Am J Trop Med Hyg. 2011, 84: 929-935. 10.4269/ajtmh.2011.10-0507. source
Not checked in the free run.
- cites [21] Carmona-Fonseca J, Maestre A: Incidencia de la malaria gestacional, congénita y placentaria en Urabá (Antioquia, Colombia), 2005–2007. Rev Colomb Obstet Ginecol. 2009, 60: 15- source
Not checked in the free run.
- cites [16] Arango EM, Samuel R, Agudelo OM, Carmona-Fonseca J, Maestre A, Yanow SK: Molecular detection of malaria at delivery reveals a high frequency of submicroscopic infections and associated placental damage in pregnant women from Northwest Colombia. Am J Trop Med Hyg. 2013, 89: 178-183. 10.4269/ajtmh.12-0669. source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationBoth Plasmodium falciparum and Plasmodium vivax can cause adverse pregnancy outcomes, including maternal anaemia and low birth weight, albeit different mechanisms appear to be involved depending on the infecting species.
“Both Plasmodium falciparum and Plasmodium vivax can cause adverse pregnancy outcomes, including maternal anaemia and low birth weight, albeit different mechanisms appear to be involved depending on the infecting species [3].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [3] Rogerson SJ, Hviid L, Duffy PE, Leke RF, Taylor DW: Malaria in pregnancy: pathogenesis and immunity. Lancet Infect Dis. 2007, 7: 105-117. 10.1016/S1473-3099(07)70022-1. source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationIncreased expression of Th1 cytokines such as IL-2, TNF and IFN-gamma and decreased Th2 cytokines such as IL-6 and TGF-beta in placental malaria has been reported by others.
“Similar observations with increased expression of Th1 cytokines such as IL-2, TNF, IFN-γ and decreased Th2 cytokines such as IL-6 and TGF-β have been reported by others [31]”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [31] Aschkenazi S, Straszewski S, Verwer KM, Foellmer H, Rutherford T, Mor G: Differential regulation and function of the Fas/Fas ligand system in human trophoblast cells. Biol Reprod. 2002, 66: 1853-1861. 10.1095/biolreprod66.6.1853. source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationIL-10 has been proposed as a biomarker of placental infection and as a definitive marker of inflammation during placental malaria.
“Other authors, based on high levels detected in serum of women with gestational malaria, have proposed IL-10 as biomarker of placental infection [33] and a definitive marker of inflammation during placental malaria [34].”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [33] Kossodo S, Monso C, Juillard P, Velu T, Goldman M, Grau GE: Interleukin-10 modulates susceptibility in experimental cerebral malaria. Immunology. 1997, 91: 536-540. 10.1046/j.1365-2567.1997.00290.x. source
Not checked in the free run.
- cites [34] Kabyemela ER, Muehlenbachs A, Fried M, Kurtis JD, Mutabingwa TK, Duffy PE: Maternal peripheral blood level of IL-10 as a marker for inflammatory placental malaria. Malar J. 2008, 7: 26-10.1186/1475-2875-7-26. source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Study design and conductnone givenThe TUNEL assay for apoptosis was performed in a blinded fashion, with samples assigned a code that was revealed once all results were available.
“The test was performed in a blinded fashion, for this samples were assigned a code which was revealed once all results were available.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationEarly reports on apoptosis in malaria-infected placentas showed no difference in the proportion of apoptotic cells compared with uninfected placentas.
“Early reports on apoptosis in malaria infected placentas showed no difference in the proportion of apoptotic cells when compared to uninfected ones [30].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [30] Crocker IP, Tanner OM, Myers JE, Bulmer JN, Walraven G, Baker PN: Syncytiotrophoblast degradation and the pathophysiology of the malaria-infected placenta. Placenta. 2004, 25: 273-282. 10.1016/j.placenta.2003.09.010. source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationThe host immune response and the histopathology of the placenta are specifically associated with complications observed before birth and around the neonatal period.
“Although the effects of malaria infection on the mother and the foetus depend upon multiple factors, the host immune response and the histopathology of the placenta are specifically associated with complications observed before birth and around the neonatal period [3].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [3] Rogerson SJ, Hviid L, Duffy PE, Leke RF, Taylor DW: Malaria in pregnancy: pathogenesis and immunity. Lancet Infect Dis. 2007, 7: 105-117. 10.1016/S1473-3099(07)70022-1. source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationIn a study by Sarr et al., increased expression of COX-2 and IL-10 was detected in chronic placental malaria.
“In a study published by Sarr et al., increased expression of COX-2 and IL-10 in chronic placental malaria was detected, and COX-2 was associated with maternal anaemia, placental macrophage infiltration and haemozoin deposition [13].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [13] Sarr D, Aldebert D, Marrama L, Frealle E, Gaye A, Brahim HO, Niang M, Dangou JM, Mercereau-Puijalon O, Lehesran J, Jambou R: Chronic infection during placental malaria is associated with up-regulation of cycloxygenase-2. Malar J. 2010, 9: 45-10.1186/1475-2875-9-45. source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationApoptosis, hypoxia and inflammation mechanisms are important to a healthy pregnancy because they contribute to implantation and promote placental development.
“Such mechanisms are important to a healthy pregnancy since they contribute to implantation and promote placental development [16].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [16] Arango EM, Samuel R, Agudelo OM, Carmona-Fonseca J, Maestre A, Yanow SK: Molecular detection of malaria at delivery reveals a high frequency of submicroscopic infections and associated placental damage in pregnant women from Northwest Colombia. Am J Trop Med Hyg. 2013, 89: 178-183. 10.4269/ajtmh.12-0669. source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationNo direct association between placental malaria and hypoxia could be confirmed in the study by Boeuf and colleagues.
“Similar to the current report, Boeuf and colleagues in 2008, observed increased expression of HIF-1α and VEGF during placental infection, however not direct association between placental malaria and hypoxia could be confirmed [12].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [12] Boeuf P, Tan A, Romagosa C, Radford J, Mwapasa V, Molyneux ME, Meshnick SR, Hunt NH, Rogerson SJ: Placental hypoxia during placental malaria. J Infect Dis. 2008, 197: 757-765. 10.1086/526521. source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationHypoxia has been associated with complications from placental malaria infection.
“Hypoxia has been associated with complications from placental malaria infection [35].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [35] Cooke BM, Mohandas N, Cowman AF, Coppel RL: Cellular adhesive phenomena in apicomplexan parasites of red blood cells. Vet Parasitol. 2005, 132: 273-295. 10.1016/j.vetpar.2005.07.002. source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationBoeuf and colleagues in 2008 observed increased expression of HIF-1alpha and VEGF during placental infection.
“Similar to the current report, Boeuf and colleagues in 2008, observed increased expression of HIF-1α and VEGF during placental infection, however not direct association between placental malaria and hypoxia could be confirmed [12].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [12] Boeuf P, Tan A, Romagosa C, Radford J, Mwapasa V, Molyneux ME, Meshnick SR, Hunt NH, Rogerson SJ: Placental hypoxia during placental malaria. J Infect Dis. 2008, 197: 757-765. 10.1086/526521. source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationA physiological adaptation to hypoxia results in syncytial knot formation, an alteration often reported during placental infection by Plasmodium.
“In consequence, a physiological adaptation to hypoxia results in syncytial knot formation, an alteration often reported during placental infection by Plasmodium[8].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [8] Uneke CJ: Diagnosis of Plasmodium falciparum malaria in pregnancy in sub-Saharan Africa: the challenges and public health implications. Parasitol Res. 2008, 102: 333-342. 10.1007/s00436-007-0782-6. source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationCOX-2 was associated with maternal anaemia, placental macrophage infiltration and haemozoin deposition in chronic placental malaria.
“In a study published by Sarr et al., increased expression of COX-2 and IL-10 in chronic placental malaria was detected, and COX-2 was associated with maternal anaemia, placental macrophage infiltration and haemozoin deposition [13].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [13] Sarr D, Aldebert D, Marrama L, Frealle E, Gaye A, Brahim HO, Niang M, Dangou JM, Mercereau-Puijalon O, Lehesran J, Jambou R: Chronic infection during placental malaria is associated with up-regulation of cycloxygenase-2. Malar J. 2010, 9: 45-10.1186/1475-2875-9-45. source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationCOX-2 has been proposed as a marker of preeclampsia and of recovery after infectious conditions.
“In addition, COX-2 has been proposed as a marker of preeclampsia and recovery after infectious conditions [37].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [37] Koga K, Aldo PB, Mor G: Toll-like receptors and pregnancy: trophoblast as modulators of the immune response. J Obstet Gynaecol Res. 2009, 35: 191-202. 10.1111/j.1447-0756.2008.00963.x. source
Not checked in the free run.
The paper relies on this without support.
The phenomena of apoptosis, inflammation, and hypoxia in P. vivax infection during pregnancy remain to be studied.
“As for P. vivax infection during pregnancy, these phenomena remain to be studied.”
The paper relies on this without support.
Submicroscopic placental infection detected by qPCR (negative microscopy) is a true infection capable of affecting placental pathophysiology.
“Positive infected units were those with a negative diagnosis by microscopy and a positive qPCR result; negative units were negative by both tests.”
The paper relies on this without support.
Complex cellular and molecular mechanisms such as apoptosis, hypoxia and inflammation have not been evaluated in cases of placental infection by Plasmodium spp. in this endemic region.
“Complex cellular and molecular mechanisms, such as apoptosis, hypoxia and inflammation have not been evaluated in cases of placental infection by Plasmodium spp in this endemic region.”
The paper relies on this without support.
The knowledge gathered so far on the pathophysiology of placental malaria mainly describes cases of P. falciparum infection.
“The knowledge gathered so far on the pathophysiology of placental malaria mainly describes cases of P. falciparum infection.”
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?
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).”
From Clinical outcomes of submicroscopic infections and correlates of protection of VAR2CSA antibodies in a longitudinal study of pregnant women in Colombia (2018) · cites this paper as [11]
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.
Infected-group apoptotic mean conflicts with species breakdown
MajorTable 5 gives 62.37% as the mean for all 25 infected placentas. Weighting Table 6's species means by its reported group sizes of 16, 6 and 3 gives 67.20%, not 62.37%.
“| Apoptotic cells | 62.37% ± 10.02% | 44.88% ± 2.15 | 0.0001 |”
“| Apoptotic cells index | 44.78 (2.15) | 71.32 (4.45) | 61.04 (5.96) | 57.56 (3.06) | 0.000 |”
Significance of HIF and VEGF is reversed in the Results
MajorThe text says only VEGF differed significantly between groups. Table 5 reports the opposite: HIF has P = 0.0001, while VEGF has P > 0.05.
“The inflammation markers HIF and VEGF were observed high in the PM + group, but only VEGF was significantly different.”
“| HIF | 0.96 ± 1.15 | 0.21 ± 0.22 | 0.0001 | | VEGF | 0,14 ± 0.14 | 0.12 ± 0.15 | >0.05 |”
Uninfected-group means differ between Tables 5 and 6
MajorThe tables describe the same PM− group of 25 placentas but give different means. For example, HIF is 0.21 versus 0.1, VEGF is 0.12 versus 0.05, and COX-1 is 0.73 versus 0.43.
“| HIF | 0.96 ± 1.15 | 0.21 ± 0.22 | 0.0001 | | VEGF | 0,14 ± 0.14 | 0.12 ± 0.15 | >0.05 | | Inflammation | | | | | COX-1 | 6.95 ± 3.14 | 0.73 ± 0.41 | 0.0001 |”
“| HIF | 0.1 (0.22) | 0.37 (0.66) | 0.35 (0.47) | 0.82 (2.97) | 0.000 | | VEGF | 0.05 (0.15) | 0.09 (0.17) | 0.06 (0.07) | 0.09 (0.06) | 0.412 | | COX1 | 0.43 (0.41) | 6.64 (3.54) | 5.22 (0.69) | 5.9 (3.4) | 0.000 |”
Reported normal birth-weight range excludes both reported means
MinorThe Results call the mean birth weights normal while defining that range as below 2,500 grams. Table 2 reports means of 2,891 and 3,305 grams, both above that stated threshold.
“the mean birth weight was similar and within normal range (<2,500 grams) in all.”
“| Birth weight (grams) | 2,891 (range 1,780–3,900) | 3,305 (range 2,600–4,400) |”
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Malaria Enhances Expression of CC Chemokine Receptor 5 on Placental Macrophages
Tkachuk, A. N., Moormann, A. M., Poore, J. A., Rochford, R. A., Chensue, S. W., Mwapasa, V., & Meshnick, S. R. (2001) · The Journal of Infectious Diseases · doi:10.1086/319248 · Cited by 78 · see citing works
Campos, I. M., Uribe, M. L., Cuesta, C., Franco-Gallego, A., Carmona-Fonseca, J., & Maestre, A. (2011) · The American Society of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2011.10-0507 · Cited by 59 · see citing works
Self-citationImmunologic activation of human syncytiotrophoblast by Plasmodium falciparum
Lucchi, N. W., Peterson, D. S., & Moore, J. M. (2008) · Malaria Journal · doi:10.1186/1475-2875-7-42 · Cited by 58 · see citing works
Arango, E. M., Samuel, R., Agudelo, O. M., Carmona-Fonseca, J., Maestre, A., & Yanow, S. K. (2013) · The American Society of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.12-0669 · Cited by 55 · see citing works
Self-citationUneke, C. J. (2008) · Parasitology Research · doi:10.1007/s00436-007-0782-6 · Cited by 53 · see citing works
Cellular adhesive phenomena in apicomplexan parasites of red blood cells
Cooke, B. M., Mohandas, N., Cowman, A. F., & Coppel, R. L. (2005) · Veterinary Parasitology · doi:10.1016/j.vetpar.2005.07.002 · Cited by 51 · see citing works
Placental Hypoxia during Placental Malaria
Boeuf, P., Tan, A., Romagosa, C., Radford, J., Mwapasa, V., Molyneux, M. E., Meshnick, S. R., Hunt, N. H., & Rogerson, S. J. (2008) · The Journal of Infectious Diseases · doi:10.1086/526521 · Cited by 50 · see citing works
Pregnancy-associated malaria: Parasite binding, natural immunity and vaccine development
Gamain, B., Smith, J. D., Viebig, N. K., Gysin, J., & Scherf, A. (2006) · International Journal for Parasitology · doi:10.1016/j.ijpara.2006.11.011 · Cited by 49 · see citing works
Prevalence of gestational, placental and congenital malaria in north-west Colombia
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Self-citationCarmona-Fonseca, J., & Maestre-B., A. (2009) · Revista Colombiana de Obstetricia y Ginecología · doi:10.18597/rcog.351 · Cited by 43 · see citing works
Self-citationCarmona-Fonseca, J., Arango, E., & Maestre, A. (2013) · The American Society of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.12-0363 · Cited by 42 · see citing works
Self-citationArango, E., Maestre, A., & Carmona-Fonseca, J. (2010) · Revista Brasileira de Epidemiologia · doi:10.1590/s1415-790x2010000300002 · Cited by 33 · see citing works
Self-citationThe Placental Syncytium and the Pathophysiology of Preeclampsia and Intrauterine Growth Restriction
Guller, S. M., Ma, Y. Y., Fu, H., Krikun, G., Abrahams, V. M., & Mor, G. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1434.015 · Cited by 27 · see citing works
Chronic infection during placental malaria is associated with up-regulation of cycloxygenase-2
Sarr, D., Aldebert, D., Marrama, L., Frealle, E., Gaye, A., Brahim, H. O., Niang, M., Dangou, J. M., Mercereau-Puijalon, O., Lehesran, J. Y., et al. (2010) · Malaria Journal · doi:10.1186/1475-2875-9-45 · Cited by 22 · see citing works
McGready, R. M., Ashley, E. A., Tan, S., Brabin, B. J., & Nosten, F. H. (2006) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.2005.00831.x · Cited by 12 · see citing works
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The immunological balance between host and parasite in malaria
Deroost, K., Pham, T., Opdenakker, G., & den Steen, P. E. V. (2015) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuv046 · Cited by 149 · see citing works
The immunology of Plasmodium vivax malaria
Antonelli, L. R. D. V., Junqueira, C., Vinetz, J. M., Golenbock, D. T., Ferreira, M. U., & Gazzinelli, R. T. (2019) · Immunological Reviews · doi:10.1111/imr.12816 · Cited by 77 · see citing works
Obiri, D., Erskine, I. J., Oduro, D., Kusi, K. A., Amponsah, J. A., Gyan, B. A., Adu‐Bonsaffoh, K., & Ofori, M. F. (2020) · Scientific Reports · doi:10.1038/s41598-020-64736-4 · Cited by 39 · see citing works
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Djontu, J. C., Siewe, S. S., Edene, Y. D. M., Nana, B. C., Foko, E. V. C., Bigoga, J. D., Leke, R. F. G., & Megnekou, R. (2016) · Malaria Journal · doi:10.1186/s12936-016-1611-0 · Cited by 27 · see citing works
Molecular Principles of Intrauterine Growth Restriction in Plasmodium Falciparum Infection
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Maestre, A., & Carmona‐Fonseca, J. (2014) · The Journal of Infection in Developing Countries · doi:10.3855/jidc.3777 · Cited by 27 · see citing works
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Llana, M. N., Sarnacki, S. H., Castañeda, M. D. R. A., Pustovrh, M. C., Gartner, A. S., Buzzola, F. R., Cerquetti, M. C., & Giacomodonato, M. N. (2014) · PLoS ONE · doi:10.1371/journal.pone.0111282 · Cited by 15 · see citing works
Establishing a conceptual framework of the impact of placental malaria on infant neurodevelopment
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Peripheral and Placental Biomarkers in Women With Placental Malaria: A Systematic Review
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Overview of Epidemiology of Malaria Associated with Pregnancy in Northwestern Colombia, 1985-2020
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Álvarez-Larrotta, C., & Carmona‐Fonseca, J. (2019) · Revista chilena de infectología · doi:10.4067/s0716-10182019000300341 · Cited by 5 · see citing works
Self-citationMadanitsa, M. (2016) · University of Liverpool · doi:10.17638/02003527 · Cited by 1 · see citing works
Rahmah, Z., Wahju-Sardjono, T., Fitri, L. E., Ulfiati, A., Ungu, B., Zulhaidah-Arthamin, M., & Norahmawati, E. (2019) · Iranian Journal of Parasitology · doi:10.18502/ijpa.v14i4.2102 · Cited by 1 · see citing works
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Association between Parasite Density and Cytokines in Malaria Infected Human Placentas
Okamgba, O. C. (2021) · Annals of Medical Laboratory Science · doi:10.51374/annalsmls.2021.1.2.0040
Álvarez-Larrotta, C., Agudelo, O. M., Gavina, K., Yanow, S. K., Carmona‐Fonseca, J., & Arango, E. (2022) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.21-0335
Self-citation
- Authors
- Agudelo, O. M., Aristizabal, B. H., Yanow, S. K., Arango, E., Carmona-Fonseca, J., & Maestre, A.
- Affiliations
- Universidad de Antioquia (CO)
- Hospital Pablo Tobon Uribe (CO)
- University of Alberta (CA)
- Corresponding author
- Maestre, Amanda
- Venue
- Malaria Journal
- Published
- 2014-03-27
- Volume
- 13
- Issue
- 1
- Pages
- 122-122
- ISSN
- 1475-2875 (ISSN-L)
- PMC
- PMC3972514
- OpenAlex
- W2115593148
- Cited by
- 37
- References
- 38
- Citations by year
- 2023: 2 · 2022: 3 · 2021: 5 · 2020: 4 · 2019: 5 · 2018: 3 · 2017: 4 · 2016: 4 · 2015: 5 · 2014: 2
- FWCI
- 4.98
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Malaria Journal (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Greater South Information System
- Funders
- Departamento Administrativo de Ciencia, Tecnología e Innovación (COLCIENCIAS)
- Universidad de Antioquia
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
- Keywords
- placental malaria, submicroscopic malaria infection, Plasmodium falciparum, Plasmodium vivax, Th1/Th2 imbalance, inflammation, hypoxia, apoptosis, Fas/FasL, vascular endothelial growth factor, hypoxia-inducible factor, malaria in pregnancy, pregnant women
- MeSH terms
- Adolescent, Adult, Hypoxia, Colombia, Cross-Sectional Studies, Female, Humans, Inflammation, Placenta, Plasmodium falciparum, Plasmodium vivax, Pregnancy, Prospective Studies, Pregnancy Complications, Parasitic, Polymerase Chain Reaction, Cytokines, Malaria, Falciparum, Malaria, Vivax, Apoptosis, Young Adult, Th1-Th2 Balance
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.
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