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Background: Malaria in pregnancy leads to serious adverse effects on the mother and the child and accounts for 75,000-200,000 infant deaths every year. Currently, the World Health Organization recommends intermittent preventive treatment of malaria in pregnancy (IPTp) with sulfadoxine-pyrimethamine (SP) at each scheduled antenatal care (ANC) visit. This study aimed to assess IPTp-SP coverage in mothers delivering in health facilities and at the community. In addition, factors associated with low IPTp-SP uptake and malaria adverse outcomes in pregnancy were investigated. Methods: A community and a health facility-based surveys were conducted in mothers delivering in Chókwè district, southern Mozambique. Social-demographic data, malaria prevention practices and obstetric history were recorded through self-report and antenatal records. For women delivering at health facilities, a clinical examination of mother and child was performed, and malaria infection at delivery was determined by rapid diagnostic test, microscopy, quantitative PCR and placental histology. Results: Of 1141 participants, 46.6, 30.2, 13.5 and 9.6% reported taking ≥ 3, two, one and none SP doses, respectively. Low IPTp uptake (< 3 doses) was associated with non-institutional deliveries (AOR = 2.9, P < 0.001), first ANC visit after week 28 (AOR = 5.4, P < 0.001), low awareness of IPTp-SP (AOR = 1.6, P < 0.002) and having no or only primary education (AOR = 1.3, P = 0.041). The overall prevalence of maternal malaria (peripheral and/or placental) was 16.8% and was higher among women from rural areas compared to those from urban areas (AOR = 1.9, P < 0.001). Younger age (< 20 years; AOR = 1.6, P = 0.042) and living in rural areas (AOR = 1.9, P < 0.001) were predictors of maternal malaria at delivery. Being primigravidae (AOR = 2.2, P = 0.023) and preterm delivery (AOR = 2.6, P < 0.001) predicted low birth weight while younger age was also associated with premature delivery (AOR = 1.4, P = 0.031). Conclusion: The coverage for two and ≥ 3 doses of IPTp-SP is moderately higher than estimates from routine health facility records in Gaza province in 2015. However, this is still far below the national target of 80% for ≥ 3 doses. Ongoing campaigns aiming to increase the use of malaria prevention strategies during pregnancy should particularly target rural populations, increasing IPTp-SP knowledge, stimulate early visits to ANC, improve access to health services and the quality of the service provided.
This study was conducted in the Chókwè district between June 2014 and June 2015. Chókwè is located in Gaza Province along the Limpopo River in the southern region of Mozambique, approximately 220 kilometres northwest of Maputo, the capital city of the country. The district has an area of 2466 km2 and an estimated population of 214,183 inhabitants [23]. Chókwè district includes four administrative areas: Chókwè, Liónde, Macarretane and Xilembene (Fig. 1). The main economic activities of the district population are subsistence farming, large rice productions supported by major irrigation systems, livestock keeping and small business. Malaria, which is mostly attributable to P. falciparum, is endemic in this area with the majority of cases occurring during the rainy season from November to April. Map of Chókwè district showing the Chókwè HDSS catchment area and study Health Centres (Source: Chókwè HDSS 2014) A continuous health and demographic surveillance system (HDSS)—including 135,616 habitants (63.3% of the district population) and occupying an area of approximately 600 km2 within a 25 km radius of Chókwè City is run by the “Centro de Investigação e Treino em Saúde de Chókwè”, a clinical research centre affiliated with the National Institute of Health—Ministry of Health of Mozambique. The HDSS catchment area includes fifteen villages, eight of which belong to the Chókwè Municipality (classified as urban) and seven to Liónde and Macarretane (classified as rural). Data routinely registered in the HDSS includes migrations, pregnancies, births and deaths (Bonzela et al. pers.comm.). Although during the last 10 years Mozambique has achieved significant progress in the coverage of institutional deliveries, an important proportion of these still occur mainly in rural communities [18, 19, 22]. Therefore, to obtain accurate data on IPTp coverage in the area under HDSS surveillance, a community and health facility based surveys were conducted. The community survey included women with non-institutional deliveries during the study period, while the health facility survey included women delivering at (i) Chókwè Hospital, (ii) Peripheral Health Centre of Terceiro Bairro, (iii) Peripheral Health Centre of Liónde and (iv) Peripheral Health Centre of Conhane, all located within the Chókwè HDSS catchment area (Fig. 1). Chókwè Hospital is located in urban area (Chókwè municipality) and is the reference hospital providing assistance for all Chókwè district population and neighbouring districts. Women were enrolled in the study if they fulfilled the following inclusion criteria: (i) aged between 15 and 48 years, (ii) having a singleton delivery, and (iii) being a permanent resident of the area under HDSS surveillance in the Chókwè district. HIV positive women receiving antiretroviral treatment or prophylactic treatment with co-trimoxazole were excluded from the study, since IPTp-SP is not recommended in these women due to potential adverse drug reactions [24]. Written informed consents were obtained from all women before enrolment into the study. In Mozambique, WHO’s recommendation of at least three doses of IPTp-SP during pregnancy was implemented in 2014. Therefore, the sample size calculation was based on the estimate of the proportion of pregnant women receiving three or more IPTp-SP in Gaza province. This was approximately 28% in 2014 [21]. With a margin of error of ± 4% using an alpha type-1 error of 5%, at least 1038 delivering women during the study period were estimated to be included. Data were collected by trained midwives and HDSS health-workers who were specifically trained for this study. A structured questionnaire in Portuguese and local Changana language was administrated to document socio-demographic data including age, residence, marital status, education, occupation, knowledge of IPTp and use of ITN. Antenatal data were obtained from the mother’s antenatal card and included parity, gestational age at the first ANC, and timing of IPTp-SP doses. Women with non-institutional deliveries were identified through the HDSS by comparing births registered in the database and hospital registers, and the interviews were conducted within 3 months after the date of delivery to minimize recall bias. In the health facility survey, parturient women were examined by a hospital clinician. Axillary body temperature was recorded and 3 ml of venous blood sample was collected immediately after delivery in ethylene diamine tetra acetic acid (EDTA) containing tubes. Peripheral venous blood samples were used to assess hemoglobin levels (HemoCue 301, Angelholm, Sweden), P. falciparum infection using RDT (SD Bioline Malaria Antigen Pf, Standard Diagnostic Inc, South Korea) and to prepare blood slides and samples for posterior diagnosis by light microscopy and quantitative polymerase chain reaction (qPCR), respectively. Newborn’s birth weight and gestational age were measured within 24 h after delivery: birth weight using a digital scale (Soehnle professional, Soehnle Industrial Solutions GmbH; Germany) and gestational age based on last normal menstrual period; in case of uncertainty, it was estimated with the Ballard score maturational assessment by trained midwives [25]. Placental tissue samples were collected from the maternal side of the placenta with approximately 2 cm × 2 cm in length and width, and 1 cm in depth and immediately placed in 10% neutral buffer formalin and stored at 2–8 °C until processed. Thick and thin smears were prepared and stained with 5% Giemsa for 25 min and examined for malaria parasites by standard microscopy [26]. Slides were examined by two independent microscopists from the National Malaria Reference Laboratory using light microscopy at 100× magnification for the presence of malaria parasites. Parasite density was estimated by counting the number of asexual parasites per 500 white blood cells (WBCs), and parasites per µL calculated assuming a WBC count of 8000 cells per µL of whole blood. A slide was considered to be negative if no parasites were seen after review of 1000 WBCs. In case of discrepant results, the slide was read by a third microscopist and the mean of the two closest reads was used. External quality control with 10% of slides was performed by a fourth experienced reader at the Malariology Unity Laboratory, Institute of Tropical Medicine in Antwerp, Belgium. Molecular detection of P. falciparum infections was performed by qPCR. Briefly, DNA was extracted from 200 μL of erythrocyte pellet with QIAamp 96 DNA blood kit (Qiagen, Germany), and eluted in 200 μL of water. Five microliters of DNA were used for qPCR analysis targeting P. falciparum var gene acidic terminal sequence (var ATS, ~ 59 copies per genome) as previously described [27]. Parasite densities were obtained by interpolating cycle thresholds (Ct) from a standard curve of infected erythrocytes diluted in whole blood (from 100,000 to 0.01 parasites/μL). Samples with Ct values ≤ 38.5 Ct were considered positive. The limit of detection was 0.04 parasite/µL. Placental tissue preparation and histological examination was performed at the Pathology laboratory of the Maputo Central Hospital (Hospital Central de Maputo-HCM) as described elsewhere [28]. Two trained-independent microscopists read the slides, discrepant results were reviewed by a third microscopist and a consensus result was determined. External quality control was performed at Barcelona Institute for Global Health (ISGlobal) by a fourth experienced reader for 10% of slides. The following definitions were used: (a) fever: axillary temperature ≥ 37.5 °C; (b) moderate and severe anaemia: Hb < 11 g/dL and Hb < 8 g/dL respectively; (c) LBW: < 2,500 g; (d) preterm delivery: < 37 weeks of completed gestation. Gravidity was categorized into primigravidae (women in their first pregnancy) and multigravidae (women in their second or more pregnancies). Placental infection was classified according to the histopathology results as: (i) uninfected, no parasites or pigment present; (ii) acute infection, parasites present with no pigment in monocytes or fibrin; (iii) chronic infection, parasites present in erythrocytes with pigment and (iv) past infection, no parasites, pigment confined to fibrin or cells within fibrin indicating past infection [29]. This study was approved by the National Bioethics Committees of Mozambique (CNBS) (IRB00002657), the Institute of Tropical Medicine (ITM) Institutional Review Board (IRBAB/ac/059) and the University of Antwerp (IRB-B300201421228). All procedures were carried out in accordance with the Helsinki Declaration as revised in 2013. Administrative approval to conduct the study was obtained from the local health facilities and the Ministry of Health of Mozambique. Informed consent was obtained at recruitment from all study participants or their representatives. Data from all study forms were double entered and checked for unusual values and inconsistencies between fields using OpenClínica v.3.3 (USA), and then exported to STATA version 14.1 (Stata Corp, College Station, TX, USA) for analysis. For categorical variables, descriptive analysis was performed and the data summarized in proportions and frequency tables. Means with their respective standard deviations and medians with interquartile ranges were used to summarize continuous variables. Kruskal–Wallis rank test was used to compare medians and interquartile ranges (IQRs) of continuous variables, and Chi square test or Fisher exact test for categorical variables. Univariate analysis was performed to analyse factors associated with low IPTp-SP uptake (< 3 doses), maternal malaria infection and density, LBW and preterm deliveries. Explanatory variables with P < 0.20 in the univariate analysis, were included in the multivariable regression analysis. Crude odds ratios (OR), adjusted odds ratios (AOR) and 95% confidence intervals are reported with P values < 0.05 considered statistically significant.
