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 Table of Contents  
ORIGINAL ARTICLE
Year : 2016  |  Volume : 33  |  Issue : 3  |  Page : 310-316

Pregnancy and fetal outcome of placental malaria parasitemia in Ile-Ife, Nigeria


1 Department of Obstetrics and Gynaecology, Bowen University Teaching Hospital, Ogbomoso, Oyo State, Nigeria
2 Department of Community Health, Bowen University Teaching Hospital, Ogbomoso, Oyo State, Nigeria
3 Department of Obstetrics and Gynaecology, Obafemi Awolowo University Teaching Hospitals Complex, Ile-Ife, Osun State, Nigeria
4 Department of Obstetrics and Gynaecology, Ondo State Specialist Hospital, Akure, Ondo State, Nigeria
5 Department of Community Health, Ondo State Specialist Hospital, Akure, Ondo State, Nigeria

Date of Web Publication8-Feb-2017

Correspondence Address:
A O Fehintola
Department of Obstetrics and Gynaecology, Bowen University Teaching Hospital, Ogbomoso, Oyo State
Nigeria
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0189-5117.199811

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  Abstract 

Background: Placental malaria constitutes a major threat to the well-being of both the mother and fetus (es). It is a common complication of malaria in pregnancy, in areas where malaria is endemic. It is, therefore, imperative to study the prevalence as well as pregnancy and fetal outcome of placental malaria in our area.
Methodology: The study was a cross-sectional study carried out over a 6-month period. A total of 300 eligible subjects were involved in the study. A pretested questionnaire was administered. Maternal peripheral blood was taken for malaria parasites while cord and placental blood samples were taken at delivery for neonatal packed cell volume and malaria parasite. Neonatal anthropometric measurements were recorded in a standardized pro forma. Data were analyzed using STATA 10. Descriptive and bivariate analyses were performed.
Results: Of the 300 participants studied, 48% had placental malaria parasitemia while 57.7% had peripheral malaria parasitemia. Pregnancy and perinatal outcome that was strongly associated with placental parasitemia includes maternal anemia (P < 0.0001); low birth weight (LBW) (P < 0.0001); and congenital malaria.
Conclusion: Placental parasitemia constitutes a major challenge in pregnancy as it is significantly and adversely associated with perinatal outcomes such as LBW and congenital malaria as well as with maternal anemia. Therefore, the need for adequate protection of pregnant women in malaria endemic area from the harmful effect of placental malaria is, therefore, absolutely essential.

Keywords: Perinatal outcome; placental malaria; pregnancy.


How to cite this article:
Fehintola A O, Fehintola F O, Loto O M, Fasubaa O B, Bakare B, Ogundele O. Pregnancy and fetal outcome of placental malaria parasitemia in Ile-Ife, Nigeria. Trop J Obstet Gynaecol 2016;33:310-6

How to cite this URL:
Fehintola A O, Fehintola F O, Loto O M, Fasubaa O B, Bakare B, Ogundele O. Pregnancy and fetal outcome of placental malaria parasitemia in Ile-Ife, Nigeria. Trop J Obstet Gynaecol [serial online] 2016 [cited 2020 Sep 26];33:310-6. Available from: http://www.tjogonline.com/text.asp?2016/33/3/310/199811


  Introduction Top


Malaria poses a great burden to the world's population, with 214 million cases and 438,000 deaths attributable to this mosquito-transmitted parasite in 2015 alone.[1],[2] The burden is mostly borne by Africa where 91% of deaths occurred, with pregnant women, their unborn babies, and under-five children most at risk of infection and adverse outcomes.[1] These groups are at high risk due to weakened and immature immunity, respectively.[2] Each year, there are an estimated 25 million pregnancies in Sub-Saharan Africa at risk of malaria; the consequences of which can be serious for both mother and fetus in terms of morbidity and mortality.[1],[2],[3] Malaria has been said to account for up to 40% of public health spending in the most endemic countries.[2] Malaria and the costs of treatment can result in frequent illness, suffering, and poverty in the family.[4] In malaria endemic countries such as Nigeria, pregnant women along with children under 5 years represent the most vulnerable group to Plasmodium falciparum infection.[5],[6],[7],[8]

Placental parasitization is quite common and affects up to one-third or more of all births in this part of the world.[9],[10] The risk is greater in the first than in subsequent pregnancies. The extent of placental parasitization bears no relation to febrile episodes or intensity of malaria parasitemia in the peripheral blood. Placental parasite density is influenced largely by the availability of the chondroitin sulfate A (CSA), a glycosaminoglycan receptor in the extracellular matrix to the parasite antigen, P. falciparum CSA-binding antigen. These putative ligands expressed by the parasite have been found to be antigenically conserved among global cases of placental (or maternal) malaria.[11] Most recently, it has been discovered that multigravid women can form strain – independent antibodies against CSA – specific parasite ligands and they demonstrate greatly diminished placental parasite load.[12]

The life cycle of the malaria parasites involves phases when the parasites invade red blood cells (RBCs) and produce proteins with which they attach themselves to receptors in the walls of blood vessels. This causes the blood cells to accumulate in organ capillaries, resulting in life-threatening symptoms such as severe anemia and convulsion. Individual who successfully survives P. falciparum malaria episode in childhood develop natural immunity against the parasite, by adolescence, they are more or less protected from severe malaria illness.[5] In women, however, this protective immunity is lost at pregnancy due to pregnancy-induced immune suppression. When the placenta is formed, a new environment is introduced with a different set of receptors. This makes available, a new growth niche for a subpopulation of the P. falciparum parasites which express an antigenically distinct form of P. falciparum erythrocyte membrane protein. Multiplication of this phenotype and extensive accumulation of P. falciparum infected RBCs in the placenta could lead to massive infiltration of mononuclear cells and induction of pro-inflammatory cytokines, causing severe placental pathology.[6],[7]

The course and outcome of pregnancy can be adversely influenced by placental malaria. The risk of primary postpartum hemorrhage is high in women who are already anemic from placental malaria before labor. Malaria is a known cause of puerperal pyrexia and should be borne in mind while treating this condition. The need for adequate protection of pregnant women in malaria endemic area from the harmful effect of P. falciparum is, therefore, absolutely essential.

Various studies on placental malaria parasitemia and its effects on pregnancy and its outcomes have been conducted in different parts of Nigeria.[5],[6],[7],[8] A similar study conducted in Ile-Ife by Obiajunwa et al. in the pediatrics department of this hospital in 2005 focused on the prevalence of congenital malaria.[13] However, this study is broader as it was conducted to establish the prevalence as well as the pregnancy and fetal outcome of placental malaria parasitemia in this environment. It will surely go a long way to providing data for an evidence-based policy-making process in malaria control program and better appraisal of the baseline characteristic of placental malaria.


  Methodology Top


The study was cross-sectional in design, carried out over 6 months between May and October 2013. It was conducted at the Obstetrics and Gynaecology departments of Obafemi Awolowo University Teaching Hospital Complex (OAUTHC). The teaching hospital comprises two units; Ife Hospital Unit Ile-Ife and Wesley Guild Hospital, Ilesa. These hospitals serve as tertiary referral centers, and the two obstetric units conduct an average of 2500 deliveries/year. The study populations were patients who presented for delivery at OAUTHC, irrespective of mode of delivery and booking status during the period of study. Both symptomatic and asymptomatic patients were enrolled. Mother and neonate pairs were enrolled for the study. Excluded were patients who refused participation in the study and those who had antimalaria treatment within the last 2 weeks before onset of labor and delivery.

Consecutive sampling techniques were employed to recruit the study participants while sample size was determined using Fisher's formula.[14]

Using a prevalence rate of placental parasitemia of 21.5% from the previous studies,[6],[15] the sample size needed to achieve a precision of 5% at 95% confident interval was obtained from the equation.

N = Z2 P (1 − P)/d2, where d = 0.05, Z = 1.96, and P = 0.215. The calculated sample size was 260. To allow for nonrespondents and those who will be excluded due to breach in the study protocol, a total of 300 subjects were enrolled for the study.

A structured interviewer-administered pretested questionnaire was used in data collection. The questionnaire obtained information on basic demographic such as age, parity, booking status, and other characteristics such as the educational status of the patient and the job description of the husband used for socio–economic stratification into Class 1–5.[16] In this study, Class 1 and 2 were grouped as upper social Class, Class 3 as the middle social class, while Class 4 and 5 were grouped as the lower social class to aid data analysis. Standardized pro forma was used to obtain relevant obstetric data such as gestational age at the onset of labor, mode of delivery, and neonatal anthropometric measurements. At delivery, 5 ml of venous peripheral blood was taken from the mother through venipuncture for maternal packed cell volume (PCV), ABO blood group, and blood film for the malaria parasite. Estimation of baby's PCV and blood film for malaria parasites was done by collecting 2 ml of cord blood from the portion of the cord attached to the placenta.

The placental aspirate was obtained from the blood welling up from an incision on one of the cotyledons on the maternal surface of the placenta immediately after cleaning under running water. Thick and thin blood smears were prepared from maternal, umbilical cord sample, and placental aspirates. Malaria diagnosis was based on the identification of asexual forms of malaria parasites in thick films while thin films were for species identification.

Data analysis

Data entry was carried out through the use of Statistical Package for Social Science version 16 [SPSS Inc. Released 2007. SPSS for Windows, Chicago] while editing and analysis were done through the use of statistical package version 10 (STATA 10) [StataCorp. 2007. Stata Statistical Software: Release 10. College Station, TX: StataCorp LP]. The univariate analysis was carried out to determine the proportion of women with the primary and secondary outcome of interest. Bivariate analysis, involving Chi-square and t-tests, was carried out to determine the association between the primary outcome (presence of placenta malaria parasitemia) and selected pregnancy and perinatal outcome. For all statistical analyses, P < 0.05 was considered statistically significant.

Ethical consideration

Ethical clearance was obtained from the Ethics and Research Committee of OAUTHC. During data collection, individuals were informed about the purpose of the study, confidentiality, and the right not to participate or withdraw at any time in the study was assured. Laboratory investigations were done free of charge for the patient for the purpose of this study.


  Results Top


A total of 256 (85.33%) parturient were booked while the remaining were not. One hundred and forty-one (47%) had a tertiary education while 33 (11%) had primary or no education. Seventy-eight (26.0%) were of upper social class while 105 (35%) were of lower social class. One hundred and twenty-one study participants (40.3%) were primigravidae. The overall prevalence of low birth weight (LBW) babies was 19.7%, and the proportion of preterm delivery was 11% as shown in [Table 1].
Table 1: Sociodemographics and obstetric characteristics of respondents (n=300)

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Of the 300 parturients, there was a total of 173 (maternal and/or placental) positive peripheral smears with asexual forms of P. falciparum; this giving a peripartum prevalence of malaria of 57.7%. Those with positive placental parasitemia were 144 (48%). The parturients with positive cord parasitemia were 120 (40%). Only 81 (27%) parturients used insecticide-treated net (ITN) while 125 (41.7%) parturients used intermittent preventive therapy (IPT) as shown in [Table 2].
Table 2: Patterns of malaria parasitemia and malaria control measures used

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Placental parasitemia was strongly associated with anemia in the mothers (χ2 = 28.2, df = 1, P < 0.001) and low parity (χ2 = 15.5, df = 1, P = 0.02). Placental parasitemia was significantly associated with lower mean birth weight 2900 ± 600 g versus 3200 ± 400 g among babies born to mothers with placental parasitemia compared with those without (t = 4.24, df = 298 P < 0.0001). Placental parasitemia was significantly associated with LBW babies (χ2 = 38.0, df = 1, P < 0.001). The mean ± standard deviation (SD) hematocrit of the babies with placental parasitemia was 34.9% ± 6.1% while that for those without placental parasitemia was 42.0% ± 4.8% (t = 13.96, df = 298, P < 0.0001).

Placental parasitemia was strongly associated with shorter neonatal full length and head circumference. The mean (SD) neonatal length of babies with placental parasitemia was 46.6 ± 3.1 cm while that of those without placental parasitemia was 47.8 ± 3.4 cm (t = 3.35 P < 0.001). The mean (SD) head circumference for babies with placental parasitemia was 33.4 ± 1.9 cm while that those without placental parasitemia was 34.2 ± 1.6 (t = 3.35 P < 0.001) [Table 3].
Table 3: Association between placental parasitemia, and pregnancy and neonatal outcomes

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The use of IPT with sulfadoxine-pyrimethamine in pregnancy was strongly associated with lower prevalence of placental parasitemia (χ2 = 19.12, P = 0.014) as shown in [Table 4].
Table 4: Association between intermittent preventive therapy used and maternal malaria parasitemia

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  Discussion Top


Studies from various geographical areas, especially areas of high transmission, have reported placental malaria to be a cause of varying degree of adverse pregnancy and perinatal outcome,[15],[17],[18] The prevalence of placental malaria of 48% in this study was higher than values quoted from some other studies in the Southwest; Falade et al.[19] found a prevalence rate of 13.1% in Ibadan. The high prevalence of malaria parasites in this study may be traced to the very low utilization rate of IPT compared to 84.4% obtained by Falade et al.[19] Furthermore, this study was carried out during the rainy season when the malaria transmission is at its peak; however, this result is comparable to that from different areas in Osun State.[20] The average placental parasitemia prevalence rate quoted by a multicenter study in Nigeria was 21.5% with a range between 19 and 80% depending on the method of diagnosis.[1]

The utilization rate of IPT during pregnancy in this study was 41.7%. This was lower than 80% recommended by the World Health Organization.[8] Many other studies in Sub-Saharan African have confirmed this low utilization.[18],[20] In this study, there was a statistically significant reduction in the prevalence of placental malaria with the use of IPT with pyrimethamine-sulfadoxine during pregnancy. This was in accordance with the submission of Kayentao et al.[18] and Akinboro et al.[20]

In this study, there was a significant association between low parity and placental malaria parasitemia. This observation was consistent with the findings of Scherf et al.,[11] Staalsoe et al.,[21] and Fried et al.,[22] who found the prevalence of placental malaria to be higher in primigravidae than multigravidae. In these studies, the results were controlled for age and several other factors and parity independently influenced placental malaria parasitemia prevalence. They, therefore, established the superiority of anti-cytoadherent antibody theory in primigravidae.[11],[21],[22]

Placental parasitemia was found to be significantly associated with lower maternal PCV. This was not unexpected as the association of malaria in pregnancy, and lower maternal hematocrit has been recognized and reported by the previous workers.[20],[21],[22] The drop in hematocrit occurs as a result of the fact that parasitized and unparasitized RBCs are destroyed by the spleen during malaria infestation. Placental accumulation of pigmented monocytes has been associated with maternal anemia perhaps due to the release pro-inflammatory mediators from such cells leading to suppression of erythropoiesis. In pregnancy, this is often superimposed on micronutrient deficiency (e.g., iron and folic acid), HIV infection, hookworm infestation, or chronic inflammation. Placental accumulation of pigmented monocytes has been associated with maternal anemia, perhaps because these cells release inflammatory mediators such as tumor necrosis factor-alpha that suppress erythropoiesis in the absence of interleukin-10 (IL-10) or because they cause oxidative stress, altering erythrocyte membranes and leading to increased erythrocyte destruction.[1] At present, to what extent anemia results from reduced erythropoiesis or removal of erythrocytes damaged in the placenta or elsewhere is unclear? It is, however, known that using drugs that are normally effective against malaria within a locality significantly reduces the occurrence of this anemia.[23],[24],[25],[26],[27]

Cord blood infection rate in this study was 40%. Cord blood infection is common,[1],[23] but clinical disease in the newborn baby is rare, probably because the transplacental transfer of variant-specific and other antibodies protects the baby although this remains debatable.[13],[23] Fetal infection could be acquired by transplacental microtransfusion antenatally [18] and this might be responsible for priming of B cells and T cells responses to malaria.[15],[17] Placental malaria also induces cord blood CD4+, CD25+ T regulatory cells, IL-10, and decreasing interferon-γ levels,[15] which could influence newborn baby's susceptibility to disease. Under low maternal immunity, congenital malaria can present as a severe illness 2–6 weeks after birth and infection in utero has been associated with stillbirth.[23]

Accumulation of monocytes at the placenta bed with the release of cytokines can lead to hypoxia and reduction in the transplacental transfer of nutrients leading to intrauterine growth restriction (IUGR). Active infection of the placenta leads to LBW by causing preterm delivery while chronic placental malaria leads to LBW through IUGR.[23]

The LBW rate of 31.8% among mothers with positive placental parasitemia is higher than 8%–25% range reported from the previous studies from Sub-Saharan Africa.[3],[28],[29],[30],[31] The reason for this is not clear but may be due to declining in proper utilization of integrated vector control measures. Furthermore, other risk factors for LBW such as hypertensive disorders of pregnancy were not excluded from the target population. Nevertheless, the impact of placental malaria on LBW has been extensively reviewed.[28],[30] It has been estimated that in areas where malaria is endemic, about 19% of LBW infants are due to malaria and 6% of infant's death are due to LBW caused by malaria. These estimates imply that around 1,000,000 infants death each year could be due to LBW caused by malaria during pregnancy in areas of malaria endemicity.[31]

Babies born to mothers with placental malaria were found to be of a shorter neonatal full length, of a smaller head circumference and lower mean hematocrit. This is consistent with several other studies and further supports the assertion that the effect of placental malaria is detrimental to intra-uterine growth as well as perinatal outcome.[28],[32],[33],[34]

The observed impact of placental malaria on the mother and their newborns adds justification to promote the use of malaria preventive measures in pregnancy. The tools for achieving effective malaria control are now available; these include the use of ITN, IPT, effective treatment, and environmental control of vectors. The use of these tools has also been facilitated with the production of a number of treatment guidelines and policy documents.[24],[25],[26]

In the present study, the level of utilization of malaria preventive measures was generally low. It is essential that all stakeholders combine efforts to ensure successful implementation in the deployment of these various tools to achieve a reduction in the burden of placental malaria.

Findings from this study should be interpreted in the light of some limitations. First, it is a cross-sectional study and this limits causal conclusion. In addition, all samples were taken at delivery; hence, the presence or absence of malaria parasites, especially in the placenta, may not reflect past or chronic infection which usually has a profound effect on pregnancy and perinatal outcome.


  Conclusion Top


Placental parasitemia constitutes a major challenge in pregnancy as it is significantly and adversely associated with perinatal outcomes such as LBW and congenital malaria as well as with maternal anemia. There is, therefore, the need to intensify control efforts aimed at reducing malaria in pregnancy in Nigeria and low parous women should receive more focused attention.

Acknowledgments

The authors would like to acknowledge useful contributions from Professor Adesegun Fatusi of the Community Health Department, Obafemi Awolowo University Teaching Hospitals Complex, Ile-Ife, Osun State, Nigeria, for their inputs in writing of this article.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
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34.
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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]


This article has been cited by
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