Asymptomatic malaria and anaemia among pregnant women during high and low malaria transmission seasons in Burkina Faso: household-based cross-sectional surveys in Burkina Faso, 2013 and 2017

Every year, about 25% of maternal deaths in hyperendemic malaria regions are due to malaria infection in pregnancy (MiP) [1]. In sub-Saharan African (SSA) countries, MiP is often asymptomatic, which is one of the main challenges in controlling MiP. Indeed, asymptomatic carriage has substantial health consequences for the mother, her unborn baby, and her future newborn. Adverse consequences of MiP for both the mother and her unborn baby include fetal loss [2‐4], intrauterine growth retardation [5, 6], preterm delivery [5, 6], low birth weight [5‐8], congenital malaria  [3, 9], perinatal mortality [2, 6], and increased risks of maternal anaemia [6, 7]. Several studies reported a high prevalence of asymptomatic MiP (ranging from 21 to 58.4%) in SSA countries [10‐14], including Burkina Faso, and this represents a major public health problem since pregnant women living in these communities are not aware they are asymptomatic carriers of malaria parasites.

To protect women from asymptomatic MiP and its consequences, the World Health Organization (WHO) recommends combined intervention, including intermittent preventive treatment during pregnancy with sulfadoxine–pyrimethamine (IPTp–SP) and iron + folic acid supplementation during antenatal care (ANC) [15]. Albeit, the effectiveness of IPTp–SP seemed to be compromised by the spread of resistance to SP in most African countries [16, 17], several studies reported that the IPTp-SP continues to reduce the incidence of malaria parasites carriage and the malaria-attributable adverse pregnancy outcomes namely, low birthweight, and maternal anaemia [18‐22]. Even in areas with excellent SP sensitivity, such as in many parts of West Africa, there is still a high prevalence of placental infections in women receiving less than three doses of SP, particularly during the peak of malaria transmission season [23].

In Burkina Faso, around three-quarters of the population use self-medication or traditional therapy when signs of malaria are suspected [24]. By implication, around one-quarter of the population attends a clinic when they feel ill or due to scheduled visits (namely ANC), and are treated when there is confirmed malaria. Consequently, asymptomatic MiP cases and anaemia remain untreated. The prevalence of asymptomatic MiP among women attending routine ANC was estimated at about 19–51% based on malaria rapid diagnostic tests (RDTs) [25‐28], whereas anaemia prevalence was estimated at around 60% [27, 28]. There are only a few community-based published studies that have estimated the prevalence of MiP [29] at the household level; in this case, conducted in Nanoro and nested within a cluster-randomized controlled trial. In Burkina Faso, the majority of published data on the subject have been obtained in healthcare settings (i.e., in health facilities). It is, therefore, important to have better insight into asymptomatic MiP and its corollary anaemia, at the community level. This will provide useful indicators to guide decision-making regarding control strategies and to optimize interventions in the context of resource constraints.

This study, aimed to estimate the prevalence of asymptomatic carriage of malaria parasites and anaemia among pregnant women in their community through a household survey during low and high malaria transmission seasons in Burkina Faso. The study also aimed to identify the potential factors associated with asymptomatic carriage and anaemia among pregnant women surveyed at their household.

The presence of malaria and anaemia in pregnancy, regardless of the gestational stage, are potentially harmful to both the fetus and mother as well as to the family and community [1, 2, 5‐8, 37, 38]. This study provides insights into the extent of asymptomatic MiP and its corollary, anaemia, at the community level (i.e., pregnant women surveyed in their own family home) throughout different malaria transmission periods of the year in Burkina Faso.

The study findings show that the prevalence of asymptomatic MiP and anaemia at the household level was high. In this present study, the MiP prevalence was higher among young women, increased significantly during the high transmission season and increased the risk of maternal anaemia. For the survey conducted in 2017, the risk of MiP was higher during the first trimester of pregnancy.

The prevalence of asymptomatic carriage of malaria parasites found in this household-based study was lower compared with the estimated prevalence reported in previous studies, where it was reported to range from 19 to 51%, among pregnant women attending health facilities as part of their ANC in Burkina Faso [25‐28]. However, the overall aggregate prevalence of asymptomatic MiP (11.0%) reported in our study corroborates the results (12.2%) from the COSMIC household-based survey conducted in Burkina Faso between March 2014 and January 2016 [29, 39]. In addition, the prevalence of asymptomatic MiP at the community level during the low transmission season was slightly lower compared to the prevalence of 9.1% reported from a community-based study conducted in Ethiopia during the minor (“low”) malaria transmission season [40]. Therefore, the results underline the need for maintaining effective prevention measures throughout the entire course of pregnancy. These results showed that pregnant women living in Burkina Faso (or other SSA countries) are consistently exposed to malaria risk and its harmful consequences at any time of the year. However, the highest risk of asymptomatic carriage of malaria parasites in the study seemed to occur among younger women (primi- or secundigravida), in the second and third trimester of pregnancy, and during the high malaria transmission season. These risk factors have been documented in other previous studies [10, 25‐27, 33, 34, 41‐43]. Thus, more efforts are needed to increase IPTp–SP coverage (i.e. monthly from the second trimester to delivery), at both the health facility level and community/household level through the community-based health workers (CHWs), in order to reduce anaemia and contribute to preventing low birth weight prevent poor pregnancy outcomes [19, 44]. From this perspective and according to the WHO recommendations [45], several countries, including Burkina Faso, have set up strategies involving CHWs whose tasks include community-based sensitization activities, prevention measures, conducting malaria home diagnoses by RDT, and treatment of uncomplicated malaria within their respective communities [29, 46].

The study showed a high prevalence of anaemia among pregnant Burkinabe women living in their communities, though this prevalence seemed to be slightly lower compared with the prevalence among pregnant women attending health facilities as part of their ANC [27, 28]. According to the literature, the nutritional deficiencies, particularly deficiency in iron and folic acid constitute the main causes of anaemia in pregnancy. The difference in prevalence of anaemia observed during the transmission season (especially between October–November 2014 and April June 2017) could be also explained by the food shortage period in Burkina Faso. In addition to the nutritional factors, in our context, malaria (sequestration of parasitized red blood cells in the placenta), second trimester of pregnancy, and the high malaria transmission season may not be the only causes of anaemia in pregnant women. Indeed, the causes of anaemia during pregnancy in developing countries are multifactorial and may be a result of other co-morbidities (worm infestation), complication events (including placenta previa, placental abruption), chronic diseases (HIV, sickle cell disease, and TB), or nutritional deficiency (inadequate intake of iron and folic acid and/or inadequate iron + folic acid supplementation) [47‐53]. Appropriate community-based strategies to prevent anaemia in pregnancy can help to significantly reduce the occurrence of maternal anaemia and, thereby, avoid progression to fatal outcomes. In this respect, the capacity of CHWs should be strengthened to allow them to carry out targeted sensitization of the risk factors leading to anaemia, ensure effective adherence to preventive measures among the community, detect clinical signs of anaemia (pallor, fatigue, bleeding), and direct people to a health centre for appropriate clinical management (such as administering of a double dose of iron) [54].

Although the findings of this study provide an overview of the extent of asymptomatic malaria and anaemia in pregnant women at the community level, both during the high and the low transmission seasons in Burkina Faso, some potential limitations need to be considered. First, asymptomatic carriage of malaria parasites was defined by using a malaria RDT, which could lead to underestimation (due to false negatives) or overestimation (false positives) of the true prevalence. False negatives from the malaria RDT may be due to the detection threshold of the test (around 200 parasites/μL) [55]. Regarding the false negative results, some studies found that more than half of all false negatives were in cases of parasitemia in which the detected antigen was under the detection threshold (i.e., lower density). False positives could be due to prolonged antigen circulation following clearance of malaria parasites. Indeed, it was shown that HRP2 antigens can persist in the bloodstream of pregnant women for up to four weeks after successful treatment [56]. However, in high-transmission areas such as Burkina Faso, HRP2 RDT could be a useful tool for malaria diagnosis, since previous studies found its performance was better than that of microscopy when used in pregnant women [31]. Second, the cross-sectional study design did not allow us to determine cause and effect. Third, the two survey periods (not overlapping) did not allow us to compare outcomes over time, although this was not in the scope of this study. Fourth, the estimation of the gestational age through mainly the recall of last menstrual cycle could introduce classification bias in the estimation of  trimester of pregnancy. The absence of indicator related to the use of ITNs by the pregnant women (a good proxy of protection conferred by bed nets) did not allow us to raise the effect of protection conferred by ITNs. In addition, information regarding the number of doses taken by pregnant woman was not available. However, since the IPTp-SP is planned to be systematically given to the pregnant women after the first trimester of pregnancy, regardless the month of the year, suggests that there was not difference related to season. Therefore, the absence of any benefit of bed nets ownership should be interpreted with caution.

This study showed a high prevalence of both asymptomatic malaria and anaemia during pregnancy, and it indicated the risks increased dramatically during the high transmission season. Thus, infected anaemic (or non-anaemic) women, apart from consequences to their unborn babies (being considered as reservoirs of parasites that may promote mother-to-child transmission), represent an important parasite reservoir contributing to the cycle of malaria transmission in the community. In order to mitigate the harmful effects of asymptomatic carriage of malaria parasites and anaemia for both the mother and her fetus, health programmes aimed at increasing the number of pregnant women coming into contact with health workers should be at least maintained or strengthened. Therefore, more efforts are needed to increase IPTp–SP coverage, at both the health facility and community/household level, to prevent poor pregnancy outcomes [19, 44]. This could be implemented by strengthening the activities of community-based health workers (regular screening for malaria and anaemia in villages and households) in order to reduce the progression of asymptomatic cases to clinical, or even severe cases before pregnant women can reach the health centres for ANC.