Placental Malaria and Lack of Prenatal Care in an Area of Unstable Malaria Transmission in Eastern Sudan Author(s): Ishag Adam, Gamal K. Adam, Ahmed A. Mohmmed, Magdi M. Salih, Salah A. Ibrahuim, and C. Anthony Ryan Source: Journal of Parasitology, 95(3):751-752. 2009. Published By: American Society of Parasitologists DOI: http://dx.doi.org/10.1645/GE-1912.1 URL: http://www.bioone.org/doi/full/10.1645/GE-1912.1
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J. Parasitol., 95(3), 2009, pp. 751–752 䉷 American Society of Parasitologists 2009
Placental Malaria and Lack of Prenatal Care in an Area of Unstable Malaria Transmission in Eastern Sudan Ishag Adam, Gamal K. Adam*†, Ahmed A. Mohmmed†, Magdi M. Salih‡, Salah A. Ibrahuim, and C. Anthony Ryan§, Faculty of Medicine, University of Khartoum, P.O. Box 102, Sudan 11111; *Gadarif University, Sudan; †Faculty of Medicine, Ribat University, Sudan; ‡Faculty of Medical Laboratory Sciences, University of Khartoum, Sudan; §Neonatal Intensive Care Unit and Department of Pediatrics and Child Health Medical, Cork University Maternity Hospital, Cork, Ireland. e-mail:
[email protected] ABSTRACT: A cross-sectional study was conducted in Gadarif Hospital in eastern Sudan to determine the prevalence, and evaluate the risk factors, of placental malaria. Two hundred and thirty-six delivering women were enrolled in the study. Socio-demographic characteristics were gathered through questionnaires. Maternal hemoglobin was measured, ABO blood groups were determined, and placental histological examinations for malaria were performed. The birth weight of the newborn was also recorded. The mean (SD) maternal age was 25.5 (6.0) yr and the mean (SD) hemoglobin was 9.8 (0.9) g/dl. Placental histology showed acute malaria infections in 13 (5.5%) and chronic infections in 5 (2.1%) women; 28 (11.9%) of the placentas revealed past infection and 190 (80.5%) indicated no infection. Lack of prenatal care was significantly associated with placental infections (OR ⫽ 12.0, 95% CI ⫽ 2.3–16.2; P ⫽ 0.003). There was no significant association between placental malaria infections and maternal age, parity, and blood group. Thirty-two (13.5%) of these pregnancy outcomes resulted in low birthweight babies. There was, however, no significant association between placental malaria and low birth weight (OR ⫽ 2.0, 95% CI ⫽ 0.4–4.1; P ⫽ 0.1). Thus, placental malaria infections affect pregnant women in this area of eastern Sudan regardless of their age or parity. Prenatal care should be encouraged to reduce malaria in the area. Much more research regarding malaria and pregnancy is needed.
It has been estimated that 90% of the global malaria burden occurs in sub-Saharan Africa, where 40% of pregnant women are exposed to malaria infections (Steketee et al., 2001). Malaria during pregnancy poses a substantial risk to the mother, the fetus, and the neonate (Cot and Deloron, 2003). Malaria during pregnancy is a major health problem in Sudan; it is reported to be the main cause of maternal mortality, maternal anemia, and low birth-weight infants (Taha et al., 1993; Dafallah et al., 2003; Adam et al., 2005a, 2005b). Placental malaria has been reported to have higher sensitivity than peripheral or clinical malaria and is more associated with adverse effects for pregnancy outcomes (McGregor et al., 1983). Therefore, research dealing with the epidemiology of placental malaria should be the goal when investigating malaria during pregnancy, even though such research is rather difficult and expensive, especially if placental histology (the gold standard) is involved in this process. Few data exist regarding the impact of placental malaria on pregnancy and on newborns in areas of unstable malaria transmission. The current study was conducted in Gadarif Hospital, eastern Sudan, to determine the prevalence, and evaluate the risk factors, of placental malaria; this was done in an effort to supplement research on malaria during pregnancy in the area (Adam, Nour et al., 2007; Adam et al., 2008; Bayoumi et al., 2008). The area is characterized by unstable malaria transmission; Plasmodium falciparum is the sole species in the area (Hamad et al., 2002). Such study is needed to provide care givers and health planners with the basic data necessary for implementation of preventative measures. The study was conducted between November 2007–January 2008 in the labor ward of Gadarif Hospital, eastern Sudan. Women with a newborn baby were approached to participate in the study. Those with antepartum hemorrhage, hypertensive disorders of pregnancy (diastolic blood pressure ⬎90 mm Hg), and diabetes mellitus were excluded. After informed consent, a structured questionnaire was administered to collect information regarding socio-demographic characteristics. The newborns were weighed soon after birth to the nearest 10 g using a Salter scale. DOI: 10.1645/GE-1912.1 751
Maternal, placental, and cord-blood films were prepared; the slides were stained with Giemsa, the number of asexual P. falciparum parasites per 200 white blood cells was counted, and an expert microscopist performed a blind double-check. Maternal hemoglobin concentrations were estimated using HemoCue hemoglobinometer (HemoCue AB, Angelhom, Sweden). The agglutination method was used to determine maternal blood groups. Full-thickness placental blocks of approximately 2–3 cm2 were taken from the placenta and kept in neutral-buffered formalin for histologic examination. Placental malaria infections were characterized based on the classification of Bulmer et al. (1993), i.e., uninfected (no parasites or pigment), acute (parasites in intervillous spaces), chronic (parasites in maternal erythrocytes and pigment in fibrin or cells within fibrin, chorionic villous syncytiotrophoblast, or both, or stroma), and past (no parasites and pigment confined to fibrin or cells within fibrin). Anemia was defined as hemoglobin ⬍11 g/dl and low birth weight as a weight ⬍2,500 g. Data were entered in a computer using SPSS for windows (SPSS Inc., Chicago, Illinois), and then double-checked before analysis. Means were compared by a Student’s t-test. Logistic regression models were constructed with placental malaria infections as a dependent variable, and age, parity, prenatal attendance, maternal blood group (O versus other blood types), and maternal hemoglobin as possible influencing factors. Others analyses factors included placental infection and low birth weight. The odds ratios and confidence intervals were calculated, and P ⬍ 0.05 was regarded as significant. The study received ethical clearance from the Research Board, Faculty of Medicine, University of Khartoum, Khartoum, Sudan. During the study period, there were 257 deliveries. Of these, 11 were twins and 246 were single-child deliveries. The data for placental histology, maternal hemoglobin, and placental and birth weights were complete for 236 women; these data were included in the final analyses. Of the 236 women, 111 (47.0%) and 125 (57.0%) were primiparae and multiparae, respectively. The mean (SD) age was 25.5 (6.0) yr. Fiftynine (25.0%), 47 (20.0%), 5 (2.0%), and 125 (53.0%) women had blood groups A, B, AB, and O, respectively; 170 (72.0%) were anemic (hemoglobin ⬍11g/dl). The mean (SD) hemoglobin was 9.8 (0.9) g/dl. Sixty-eight (29.0%) of these women elected not to receive prenatal care. The blood films for malaria were positive in 4 sets of peripheral, placental, and cord samples and in 3 placental samples. Placental histology showed acute placental malaria infections in 13 (5.5%) women and chronic infections in 5 (2.1%). Twenty-eight (11.9 %) of the placentae indicated past infection, and 190 (80.5%) showed no infection. Lack of prenatal care was significantly associated with placental infections (OR ⫽ 12.0, 95% CI ⫽ 2.3–16.2; P ⫽ 0.003). There was no significant association between placental malaria infections and maternal age (OR ⫽ 1.0, 95% CI ⫽ 0.7–1.3; P ⫽ 0.9), parity (OR ⫽ 0.9, 95% CI ⫽ 0.7–1.1; P ⫽ 0.5), or between blood group O versus other blood types (OR ⫽ 0.8, 95% CI ⫽ 0.4–1.1; P ⫽ 0.6) (Table I). Thirty-two of these deliveries (13.5%) were low birth-weight babies. There was no significant association between placental malaria and low birth weight (OR ⫽ 2.0, 95% CI ⫽ 0.4–4.1, P ⫽ 0.1. The mean (SD) birth weight was not significantly different between women with placental malaria and those without placental malaria; 2,966.2 (590.9) g versus 2,999.5 (593.5) g, P ⫽ 0.6, respectively. The study was designed to investigate prevalence and risk factors for placental malaria infections. The prevalence of placental malaria infection among pregnant women in the area was 19.5%; placental malaria infections affected pregnant women in the area regardless of their age
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TABLE I. Factors associated with placental malaria among pregnant women of eastern Sudan, using logistic regression analysis. Variable
OR
95% CI
P
Age Parity Lack of prenatal care Hemoglobin Blood group (O vs. others)
1.0 0.9 12.0 0.9 0.8
0.9–1.0 0.7–1.1 2.3–16.2 0.7–1.3 0.4–1.8
0.9 0.5 0.003 0.9 0.6
or parity. With the exception of the lack of prenatal care, no other significant risk factor for placental malaria was observed. It was not unexpected to find an absence of significant association between placental malaria and age or parity. The area is characterized by unstable malaria transmission; low immunity among these women is, therefore, to be expected (Hamad et al., 2002). Thus, these findings add to the epidemiology of malaria during pregnancy in eastern Sudan. According to, and guided by, these results, preventive measures (mainly bed nets and chemoprophylaxis) should be given to pregnant women, regardless of their age and parity. These findings supported our previous reports in a nearby area, where epidemiology and pathogenesis of malaria during pregnancy were not associated with age or parity (Adam et al., 2005a; Adam, Nour et al., 2007; Adam, Babiker et al., 2007; Adam et al., 2008; Bayoumi et al., 2008). In the current study, women who did not attend prenatal care were 12 times more likely to develop placental malaria. This is not surprising, as detection and treatment of malaria cases are part of the current program being provided by prenatal care services in the area. In the future, health planners and caregivers should implement preventative measures, such as bed nets, and intermittent preventive measures in the prenatal clinics. Prenatal care is one of the most-effective ways of reducing maternal mortality and morbidity, and under-use of this care has been associated with adverse maternal outcomes (WHO, 1999). Moreover, recent reports have suggested that the high maternal and perinatal mortality in western Sudan could be reduced by increasing women’s use of prenatal care services (Haggaz et al., 2007, 2008). In the present study, hemoglobin level was not a predictor for placental malaria infection. We recently reported that women with blood group O and placental malaria infection had slightly higher hemoglobin levels (Adam et al., 2007). However, Kabyemela et al. (2008) observed a decreased susceptibility to P. falciparum infection in pregnant women with an iron deficiency. Our observations require further examination in light of the latter study. In the present study, we also did not observe a significant association between placental malaria and low birth weight. As opposed to a recent report in a nearby area (Adam et al., 2008), low birth weight was not associated with the histopathology seen in placental malaria infections, and the explanation for this finding remains unclear. Perhaps, as we stated previously, these women had a very low prevalence of peripheral, placental, and cord microscopically-detected parasitemia; hence, the effect of submicroscopic parasitemia on low birth weight cannot be excluded. In the past, we observed a large burden of submicroscopically detected parasitemia among pregnant women that was associated with morbidity and mortality among non-pregnant individuals in the same geographic area (Adam, Elbasit et al., 2005; Giha et al., 2005). In other studies, malaria infection is known as a risk factor for low birth weight (Taha et al., 1993). However, the latter study was undertaken in a relatively small-sized hospital and may not be a true community representative, because high-risk pregnancy and women with complications were those presented at a major hospital. In summary, placental malaria infections affect pregnant women in this area, regardless of their age or parity. Lack of prenatal care was the main risk factor for placental malaria infection. This study was partially supported by the Research Fund, Medical College University of Cork, Ireland.
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