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Missed opportunities to deliver intermittent preventive treatment for malaria to pregnant women 2003–2013: a systematic analysis of 58 household surveys in sub-Saharan Africa
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Abstract
Background
Despite the availability of effective preventive measures, including intermittent preventive treatment for malaria during pregnancy (IPTp), malaria continues to cause substantial disease burden among pregnant women in malaria-endemic areas. IPTp coverage remains low, despite high antenatal care (ANC) attendance. To highlight areas of potential improvement, trends in IPTp coverage were assessed over time, missed opportunities to deliver IPTp at ANC were quantified, and delivery of IPTp was compared to that of tetanus toxoid (TT).
Methods
Data from 58 Demographic and Health Surveys conducted between 2003 and 2013 in 31 sub-Saharan African countries, with relevant questions on IPTp, ANC and TT were used to assess ANC attendance, and IPTp and TT delivery. A missed opportunity for IPTp delivery is an ANC visit at which IPTp could have been delivered according to policy but was not.
Results
The proportion of pregnant women who received ≥2 doses of IPTp increased in surveyed countries from nearly zero before to a median of 29.6 % (IQR 20.1–42.5 %) seven or more years after IPTp policy adoption. ANC attendance was high (median 76.6 % reported ≥3 visits); however, even seven or more years post policy adoption, a median of 72.9 % (IQR 58.4–79.5 %) ANC visits were missed opportunities to deliver IPTp. Among primigravid women, a median of 61.5 % (IQR 50.9–72.9 %) received two doses of TT; delivery of recommended TT exceeded IPTp in all but one surveyed country.
Conclusions
IPTp coverage measured by household surveys is unsatisfactorily low, even many years after policy adoption. The many missed opportunities to deliver IPTp suggest that deficiencies in delivery at ANC are a significant contributing factor to the low coverage levels. High levels of TT delivery indicate capacity to deliver preventive measures at ANC. Further research is required to determine the factors driving the discrepancies between IPTp and TT coverage, and how these may be addressed to improve IPTp coverage.
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Most cited references15
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Quantifying the Number of Pregnancies at Risk of Malaria in 2007: A Demographic Study
Stephanie Dellicour, Andrew Tatem, Carlos Guerra … (2010)
Introduction Malaria in pregnancy can have devastating consequences to a pregnant woman and the developing fetus, but comprehensive estimates of the annual number of women who become pregnant each year in malaria endemic areas and are therefore at risk of malaria are not available, particularly for Latin America and the Asia-Pacific regions. These figures are an important first step towards informing policy makers and for estimating the regional needs for therapeutic and disease prevention tools for malaria in pregnancy. The most cited global estimate is from the Roll Back Malaria Partnership, which states that “each year approximately 50 million women living in malaria endemic countries throughout the world become pregnant” [1]. However, an explanation of the methods used to derive these estimates is not provided. More comprehensive estimates exist for Africa and are provided by the Africa Regional Office (AFRO) of the World Health Organization (WHO) in their widely quoted strategic framework document for malaria prevention and control during pregnancy in the African region [2]. Their estimate of 24.6 million pregnancies at risk of malaria (predominantly P. falciparum), is based on the number of live born babies delivered in malarious areas of Africa in the year 2000 using a combination of malaria risk maps [3] and estimates of the number of live births from UNICEF [4]. A more recent estimate by the WHO states that “In Africa, 30 million women living in malaria endemic areas become pregnant each year” [5]. Estimates for outside of Africa are less clear, particularly for P. vivax. P. vivax is the most widely distributed human malaria parasite and co-occurs with P. falciparum in tropical areas but also occurs in temperate regions outside the limits of P. falciparum transmission. It is the major cause of malaria in much of Asia and Latin America [6],[7], and recent evidence has shown that P. vivax infections are far from benign and can result in significant morbidity in pregnant women with serious consequences for maternal and infant health [8]–[10]. Here we define a global estimate of the number of pregnancies at risk of P. falciparum and P. vivax malaria in 2007 by combining malaria spatial limits developed by the Malaria Atlas Project (MAP; www.map.ox.ac.uk), which define the total population at risk of malaria [11], with country-specific demographic data on women of childbearing age provided by the United Nations and published data on induced abortions and spontaneous pregnancy loss. Methods Data Sources The global limits of P. falciparum malaria The initial focus of the Malaria Atlas Project has been P. falciparum [12] due to its global epidemiological significance [13] and better prospects for its control and local elimination [14]. The global spatial limits of P. falciparum malaria transmission in 2007 have recently been mapped. This was done by triangulating data on transmission exclusion using biological rules based on temperature and aridity limits on the bionomics of locally dominant Anopheles vectors, data on nationally reported case incidence rates, and other medical intelligence [15]. The resulting map stratifies the malaria endemic world by stable and unstable transmission in 2007 [15]. Unstable transmission refers to areas where transmission is plausible biologically, but limited, with a clinical incidence of less than one case per 10,000 population per year. Stable transmission refers to areas with a minimum of one clinical case per 10,000 population per year [15]. The global limits of P. vivax malaria Initial attempts to map the limits of P. falciparum and P. vivax transmission were made by Guerra et al. [16],[17]. The resulting maps and “masks” (mapped areas that are filtered and excluded from analyses) used were later tested against the Malaria Atlas Project parasite prevalence database to assess their feasibility [18],[19]. This testing revealed that the accuracy to define areas of zero transmission risk due to very low population densities was limited because of the coarse spatial resolution of the initial map. Moreover, in the initial mapping [16],[17], a high density population mask was used on the basis of the assumption that no transmission occurs in areas where the population density is so high that conditions become unsuitable for transmission through the process of urbanization. However, recent analyses [19] provide evidence suggesting that high density population masks and urban extent maps should not be used to map zero risk because some transmission can occur in high density urban areas, although this is significantly lower than in rural areas [18],[19]. Therefore, for the current analyses, the P. vivax limits were redefined using the same methods as in Guerra et al. [16],[17], but without applying the population-based masks. Also, previously excluded P. vivax endemic countries have now been added after a more extensive review of the literature; these include Comoros, Djibouti, Madagascar, and Uzbekistan. This refinement of the spatial limits of transmission for P. vivax accounted for an approximate 19% increase in the population at risk (PAR) compared with previous estimates [16],[17], principally (18%) due to the inclusion of major cities. Gridded population data The Global Rural-Urban Mapping Project (GRUMP) alpha version provides gridded population counts and population density estimates for the years 1990, 1995, and 2000, both adjusted and unadjusted to the United Nations' national population estimates [11],[20]. The adjusted population counts for the year 2000 were projected to 2007 by applying national, medium variant, intercensal growth rates by country [21] using methods described previously [22]. Annual number of pregnancies per country The number of pregnancies was calculated as the sum of the number of live births, induced abortions, and spontaneous pregnancy loss (including miscarriages and stillbirths) in 2007. Live births The annual number of live births in 2007 was estimated per country using demographic data on the proportion of women of childbearing age (WOCBAs) within a population and the total fertility rates. The data were abstracted from the United Nations' national population estimates, which provide publicly accessible demographic information by year, age, sex, and country for Africa, Asia, and the Americas [23]. The number of WOCBAs in each country, defined as the mid-year resident number of women aged between 15 and 49y, was obtained for the years 2005 and 2010 (interim years are not available), and the number of WOCBAs for 2007 was calculated as the midpoint between the 2005 and 2010 estimates. The fraction of WOCBAs per country was then calculated as the number of WOCBAs in 2007 divided by the mid-year resident population at risk in 2007 (available by year). The total fertility rate (TFR) is an age-standardised measure of fertility and corresponds to the total number of children that would be born alive to a woman entering her childbearing years at age 15y if she lived to the end of her childbearing years (age 49y) and if her fertility during these 35 reproductive years was the same as the average woman of childbearing age. The total fertility rate divided by 35 is the average number of live births per WOCBA per year and when multiplied by 1,000 this is expressed as the rate of live births per 1,000 WOCBAs per year. Induced abortions, miscarriages, and stillbirth rates Subregional data on induced abortion rates were obtained from a recently published review that calculated the worldwide, regional, and subregional incidence of safe and unsafe abortions in women of child bearing age in 2003 by use of reports from official national reporting systems, nationally representative demographic health surveys, hospital data, other surveys, and published studies [24]. Country-specific information on stillbirth rates was abstracted from model-based estimates published by Stanton et al. [25] that derived data from vital registration, demographic and health surveys (DHS), and data from study reports integrated into a regression model. Regional estimates were used for three malaria endemic countries for which country-specific estimates were not available (French Guiana, Mayotte, and Timor-Leste). Country-specific data on miscarriages (spontaneous abortions) are not available. To calculate the proportion of pregnancies resulting in miscarriage, a method was applied that uses multipliers to work backwards from the (known) number of live births and induced abortions to recover the (unknown) underlying number of pregnancies that “produced” them, as described in detail previously [24],[26]–[28]. The method takes account of pregnancies that are terminated voluntarily during the period of risk for miscarriage and estimates the number of spontaneous pregnancy loss (stillbirths and miscarriages) as 10% of induced abortions plus 20% of live births. It is based on clinical studies of rates of pregnancy loss by gestational age that indicate that for each 100 induced abortions an additional ten clinically recognised pregnancies will have aborted spontaneously prior to the average gestational age of induced abortions in that population, and that approximately 120 additional clinically recognised pregnancies are required to “produce” 100 live births [27],[28]. For example, in Afghanistan it was estimated that in 2007 1.182 million live births occurred among a population of 27 million and a further 0.284 million induced abortions occurred. The number of spontaneous pregnancy losses (the sum of the number of stillbirths and miscarriages) was therefore estimated at 0.2×1,182 plus 0.1×0.284 = 0.265 million, and the total number of pregnancies as 1.731 million. The reported number of miscarriages used in this manuscript represents the number of spontaneous pregnancy losses calculated through the multiplier method as described above, minus the country-specific number of stillbirths obtained from the review by Stanton et al. [25]. The estimates provided in this study refer to clinically recognised pregnancies and do not take into account the potentially large but unknown rates of embryonic loss that may occur in the first 4–6 wk of gestation. Estimating the annual number of pregnancies exposed to malaria To obtain the total population at risk, the limits of stable and unstable P. falciparum transmission and the limits of P. vivax transmission described above were overlaid onto the Global Rural-Urban Mapping Project (GRUMP) alpha surface, projected to 2007. For every malaria endemic country of the world, the population within each set of limits was extracted, following approaches described previously [13]. The number of pregnancies at risk of malaria was then calculated from the total annual number of pregnancies estimated to have occurred in 2007 in the entire country multiplied by the fraction of the total resident population living within the spatial limits of malaria transmission in that country. Results Tables 1 and 2 provide a summary of the total population living within the global spatial limits of malaria transmission in 2007, and the corresponding number of total population, pregnancies, and live births, stratified by species and transmission patterns (within areas of assumed unstable and stable P. falciparum transmission), globally and by WHO region. 10.1371/journal.pmed.1000221.t001 Table 1 Demographic data for malaria endemic countries. WHORO Region n of MECs Total Population (Both Sexes)a WOCBAsa Total n of Pregnanciesb TPRc Pregnancy Rate per 1,000 WOCBAs§ Percentage Pregnancies Ending in: Live-births Still-births Spontaneous Abortions Induced Abortions AFRO 43 755 178 36 7.16 204 72.4% 2.3% 13.3% 11.9% EMRO/EURO 19 544 142 19 4.76 136 68.8% 2.3% 13.1% 15.8% AMRO 21 530 143 16 3.81 109 63.2% 0.9% 14.0% 22.0% SEARO/WPRO 19 3,327 881 91 3.62 103 62.4% 1.6% 13.1% 22.8% Global 102 5,157 1,343 162 4.23 121 65.5% 1.8% 13.3% 19.5% a Source: United Nations Development Program (in millions). b The total number of pregnancies is the sum of the number of live-births, stillbirths, spontaneous, and induced abortions (in millions). c The total pregnancy rate (TPR) and the annual pregnancy rate per 1,000 WOCBAs are weighted means per region and is for illustration purposes only. The number of pregnancies was derived directly as the sum of the national estimates within each region and globally. MEC, malaria endemic countries; WHORO, World Health Organization Regional Office. 10.1371/journal.pmed.1000221.t002 Table 2 Total population at risk of P. falciparum and/or P. vivax malaria by WHO regional office in 2007 (in millions) (percent of the population in malaria endemic countries at risk). WHORO Region P. falciparum Transmissiona P. vivax Transmissiona Any Species Stable Transmissionb Unstable Transmissionb Overall Overall Overall AFRO 599.9 (79.4) 8.4 (1.1) 607.8 (80.5) 73.2 (9.7) 615.4 (81.5) EMRO/EURO 89.8 (16.5) 101.7 (18.7) 190.9 (35.1) 285.1 (52.4) 343.9 (63.2) AMRO 41.2 (7.8) 50.2 (9.5) 91.4 (17.2) 96.2 (18.2) 138.2 (26.1) SEARO/WPRO 654.9 (19.7) 824.9 (24.8) 1479.3 (44.5) 2,722.3 (81.8) 2,770.1 (83.3) Global 1,385.8 (26.9) 985.1 (19.1) 2,369.4 (45.9) 3,176.9 (61.6) 3,867.6 (75.0) Similar tables with risk estimates by continent and by pregnancy outcome (live-birth, induced abortions, stillbirths, and miscarriages) are provided in Tables S1, S2, S3. a Includes countries where P. falciparum and P. vivax co-exist. b Stable transmission, ≥1 autochthonous P. falciparum cases per 10,000 people per annum; unstable transmission, <1 autochthonous P. falciparum cases per 10,000 people per annum [15]. MEC, malaria endemic countries; TPR, total pregnancy rate; WHORO, World Health Organization Regional Office. The compiled data showed that, globally, 125.2 million women living in areas with P. falciparum and/or P. vivax transmission became pregnant in 2007: 77.4 million (61.8%) in the countries that fall under the regional office of the WHO for the South East Asian (SEARO) and the Western Pacific Region (WPRO); 30.3 million (24.2%) in AFRO; 13.1 million (10.5%) in the Eastern Mediterranean and European Region (EMRO and EURO); and only 4.3 million (3.4%) in the American Region (AMRO) (Table 3). Figures 1 and 2 display the same analysis by species, but depicted by continent rather than by WHO region. Of the 125.2 million pregnancies, 82.6 million (66.0%) are estimated to result in live births; 48.8 million (63.0%), 22.1 million (72.7%), 9.0 million (68.8%), and 2.7 million (63.1%) in the SEARO/WPRO, AFRO, EMRO/EURO, and AMRO regions, respectively (Table 4). It illustrates that the proportional distribution of pregnancies at risk resulting in live births is slightly different from the distribution of total pregnancies at risk, primarily reflecting the differences in the proportion of pregnancies ending in induced abortions, which is much lower in the AFRO region (11.9%) compared to the global average in the malaria endemic countries of 19.5% [24]. 10.1371/journal.pmed.1000221.g001 Figure 1 Malaria risk map for P. falciparum and corresponding number of pregnancies in each continent in 2007. 10.1371/journal.pmed.1000221.g002 Figure 2 Malaria risk map for P. vivax and corresponding number of pregnancies in each continent in 2007. 10.1371/journal.pmed.1000221.t003 Table 3 Number of pregnancies at risk of P. falciparum and/or P. vivax malaria by WHO regional office in 2007 (in millions) (column %). WHORO Region P. falciparum Transmissiona P. vivax Transmissiona Any Species Stable Transmissionb Unstable Transmissionb Overall Overall Overall AFRO 29.6 (54.1) 0.4 (1.2) 30.0 (35.1) 3.6 (3.9) 30.3 (24.2) EMRO/EURO 4.0 (7.3) 4.2 (13.7) 8.2 (9.6) 10.4 (11.2) 13.1 (10.5) AMRO 1.4 (2.5) 1.6 (5.2) 3.0 (3.5) 2.9 (3.1) 4.3 (3.4) SEARO/WPRO 19.7 (36.1) 24.5 (79.9) 44.2 (51.8) 76.0 (81.8) 77.4 (61.8) Global 54.7 30.6 85.3 92.9 125.2 Similar tables with risk estimates by continent and by pregnancy outcome (live-birth, induced abortions, stillbirths, and miscarriages) are provided in Tables S1, S2, S3. a Includes countries where P. falciparum and P. vivax co-exist. b Stable transmission, ≥1 autochthonous P. falciparum cases per 10,000 people per annum; unstable transmission, <1 autochthonous P. falciparum cases per 10,000 people per annum [15]. MEC, malaria endemic countries; TPR, total pregnancy rate; WHORO, World Health Organization Regional Office. 10.1371/journal.pmed.1000221.t004 Table 4 Number of live-births born to pregnancies at risk of at risk of P. falciparum and/or P. vivax malaria by WHO regional office in 2007 (in millions) (column %). WHORO Region P. falciparum Transmissiona P. vivax Transmissiona Any Species Stable Transmissionb Unstable Transmissionb Overall Overall Overall AFRO 21.6 (56.7) 0.3 (1.3) 21.8 (37.4) 2.5 (4.3) 22.1 (26.7) EMRO/EURO 2.8 (7.3) 2.9 (14.1) 5.6 (9.7) 7.1 (12.0) 9.0 (10.9) AMRO 0.8 (2.2) 1.0 (5.0) 1.8 (3.2) 1.8 (3.1) 2.7 (3.3) SEARO/WPRO 12.9 (33.8) 16.1 (79.5) 28.9 (49.7) 48.0 (80.6) 48.8 (59.1) Global 38.0 20.2 58.2 59.5 82.6 Similar tables with risk estimates by continent and by pregnancy outcome (live-birth, induced abortions, stillbirths, and miscarriages) are provided in Tables S1, S2, S3. a Includes countries where P. falciparum and P. vivax co-exist. b Stable transmission, ≥1 autochthonous P. falciparum cases per 10,000 people per annum; unstable transmission, <1 autochthonous P. falciparum cases per 10,000 people per annum [15]. MEC, malaria endemic countries; TPR, total pregnancy rate; WHORO, World Health Organization Regional Office. P. falciparum Malaria Of the 125.2 million pregnancies defined above, 85.3 million occur in areas with P. falciparum transmission, 51.8% of them (44.2 million) are in the combined SEARO-WPRO regions and 35.1% (30.0 million) in the AFRO region. The remainder live in the EMRO-EURO (9.6%) and AMRO regions (3.5%) (Figure 3; Table 3). As expected, the top five ranked countries with the highest number of pregnancies at risk of P. falciparum malaria were the malaria endemic countries with the largest overall populations: India (28.2 million), Nigeria (6.5 million), Indonesia (4.4 million), Pakistan (3.7 million), and the Democratic Republic of the Congo (3.3 million). Overall, 64.1% of 85.3 million pregnancies at risk of P. falciparum malaria live in areas with assumed stable transmission (Figure 3). However, this varies widely by region; from 98.7% in the AFRO region to none in the EURO region. As depicted in Figure 3, 55.3% of the 44.2 million pregnancies at risk of P. falciparum in the WPRO/SEARO region occur in areas of very low and unstable transmission. 10.1371/journal.pmed.1000221.g003 Figure 3 Distribution of the number of pregnancies in areas with P. falciparum malaria in 2007 by WHO regions and the corresponding proportion living under stable versus unstable transmission. Blue, SEARO and WPRO; green, AFRO; orange, EMRO; red, AMRO. P. vivax Malaria Globally, an estimated 92.9 million pregnancies occurred in areas endemic for P. vivax in 2007 (including in areas where both P. falciparum and P. vivax co-exist) (Figure 2). The top five ranked countries include: India (32.9 million), China (21.2 million), Indonesia (6.3 million), Pakistan (5.8 million), and Bangladesh (4.7 million). In the WPRO/SEARO region, where the majority of the populations at risk of P. vivax live (Figure 4), approximately 98.2% of those pregnancies in malaria endemic countries occur in areas with P. vivax transmission (alone or combined with P. falciparum). By contrast this was only 11.9% for the AFRO region where P. vivax transmission is principally restricted to the horn of Africa region, Madagascar, and the Comoros islands (Figure 4). 10.1371/journal.pmed.1000221.g004 Figure 4 Distribution of the number of pregnancies in malaria endemic areas in 2007 by WHO regions and by species (P. vivax transmission only, P. falciparum transmission only or transmission of both species). Blue, SEARO and WPRO; green, AFRO; orange, EMRO; red, AMRO. Pv, P. vivax; Pf, P. falciparum. The country-specific demographic data and population at risk estimates (Table S1), as well as total pregnancies at risk and by specific pregnancy outcomes (live births, induced abortions, stillbirths, and miscarriages; Table S2) and summary estimates by other regional categories (continents instead of WHO regions; Table S3), are provided as supplemental information. In addition, information is provided illustrating which countries are included in the different WHO regions (also see Figure S1) [29]. In brief, all malaria endemic countries on the African continent fall under the Africa Regional Office (AFRO), with the exception of Djibouti, Somalia, and Sudan, which fall under the EMRO office. Discussion This is the first time, to our knowledge, that contemporary species-specific estimates of the annual number of pregnancies at risk of malaria globally have been made. Our findings suggest that in 2007 approximately 125 million pregnancies occurred in areas with P. falciparum and/or P. vivax transmission, resulting in 83 million live births; representing approximately 60% of all pregnancies globally. Approximately 85 million pregnancies occurred in areas with P. falciparum transmission and 93 million in areas with transmission of P. vivax transmission, of which about 53 million occurred in areas where both species co-exist. The pregnancies at risk estimates for P. falciparum and P. vivax in Africa (32 million [30 million in the WHO-AFRO region]) are consistent with the previous estimates by WHO (25–30 million). By contrast, the numbers at risk outside Africa are much higher (95 million) than previously estimated (25 million). Comparisons between the estimates produced in this study and the previous WHO estimates are made difficult because details of the methodology used by the WHO is not provided and it is not clear if they included all transmission areas or only areas with stable malaria transmission. Inclusion of only those areas with stable P. falciparum transmission in our study resulted in global risk estimates of just less than 55 million pregnancies, 31 million in Africa and 23 million in the other regions, i.e., very similar to the previous WHO estimates. However, the numbers of pregnancies at risk outside Africa increase almost 4-fold if areas with unstable P. falciparum transmission are included (clinical incidence <1 per 10,000 population/year) (30 million) and areas situated in the temperate regions outside the limits of P. falciparum transmission that have P. vivax transmission only (40 million) are also included. It is also not clear if the previous WHO estimates included pregnancies resulting in live births only or included adjustments for induced abortions or spontaneous pregnancy loss. Since only approximately two-thirds of all pregnancies result in live births, estimates that include all pregnancies are about one-third higher than estimates based on live births only. Although risk estimates are widely quoted figures, it is important to place them in perspective. The estimates provided here merely define the global distribution of pregnancies that occur within the global spatial limits of malaria transmission. These estimates therefore represent “any risk” of exposure to malaria during pregnancy, and do not represent the distribution of actual incidence or health burden on mothers and unborn babies, which is beyond the scope of this paper. More than half (71 million) of the 125 million pregnancies occur in areas with unstable P. falciparum transmission (31 million) or with transmission of P. vivax only (40 million), and the risk of acquiring malaria in these areas is extremely low. Thus, although these 71 million pregnancies represent more than 50% of the global number of pregnancies at risk, they may only contribute a small proportion to the number of infections in pregnancy. For example, if the actual incidence of malaria infection in these very low transmission areas is 1 in 10,000 per person-year (52 wk), and if the average pregnancy resulting in a live birth takes 38 wk from fertilisation to term, then 71 million pregnancies at risk may result in only 5,188 actual malaria infections, whereas in areas with infection rates of 1.36 or higher per person-year, all term pregnancies have been potentially exposed to malaria. Furthermore, the definition of stable transmission for P. falciparum used included all areas with more than one clinical case per 10,000 population per year. This included almost all pregnancies at risk in the AFRO Region (99% of the 30 million pregnancies at risk) and 25 million of the 95 million (26%) pregnancies in the other WHO regions. However, these stable transmission strata cover a very wide range of transmission intensities and the actual risk of infection to the 55 million individuals and the impact on maternal and infant health varies enormously within this range. At the higher end of the transmission spectrum, the majority of malaria infections in pregnancy remain asymptomatic or pauci-symptomatic, yet are a major cause of severe maternal anaemia and preventable low birth weight, especially in the first and second pregnancies. In areas with stable, but low transmission, and certainly in areas with unstable and exceptionally low transmission, infections can become severe in all gravidae groups because most women of childbearing age in these regions have low levels of pre-pregnancy and pregnancy-specific protective immunity to malaria [30]. The most recent version of the World Malaria Map [28] from the Malaria Atlas Project shows that 89% of the populations in stable P. falciparum areas outside Africa live in areas characterised by low malaria endemicity (defined as P. falciparum parasite rate in children 2–10 y of age of ≤5%). This total includes all of the stable P. falciparum transmission areas in the Americas, and 88% of the populations at risk in the Central and South-East Asia-Pacific region [31]. Our estimates do not take seasonality into account and include all pregnancies occurring throughout the year, whereas those pregnancies that occur outside of the transmission season may be at no risk, or very low risk of exposure. Our risk estimates for P. vivax are likely to be less accurate than those for P. falciparum because of greater uncertainties about the basic biology of transmission and clinical epidemiology. For example, the climatic constraints on P. vivax transmission are less well defined, the accuracy of clinical reporting of P. vivax in areas with coincidental P. falciparum is poor, and the untreated hypnozoite stage of P. vivax, which can remain dormant in infected liver cells for months or years, provides an additional challenge to the interpretation of prevalence and incidence data [15]. We used a refined P. vivax risk map that resulted in a 19% increase over previous population at risk estimates (adjusted for population growth) [18],[19], principally resulting from the removal of the population density masks and thereby the inclusion of many large cities. In most of these cities, pregnancies will be at low or very low risk of autochthonous infections. Imported malaria associated with travel to rural areas may be a greater risk factor in these cities. We did not consider infections with P. ovale or P. malariae, as their distribution is not well described and the adverse effects on maternal health and the newborn infant are unknown. In the current analysis we used the map of the global spatial limits of P. falciparum malaria, which stratifies the malaria endemic world by stable and unstable transmission published in 2008 [15].This map uses a simple divide between very low risk and higher transmission intensities and a crude proxy to account for the corresponding levels of acquired immunity in women of childbearing age. As a next step, we will examine the burden of malaria in pregnancy in terms of health impact on the pregnant women (e.g., febrile episodes, impact on maternal anaemia and maternal mortality), the newborn baby (e.g., impact on the frequency of preterm births and low birth-weight) and the infant (e.g., susceptibility to malaria). For this project, we will use the more refined P. falciparum transmission intensity model of risk within the defined stable limits which was developed recently by the Malaria Atlas Project [31], allowing disease impact calculations across multiple transmission strata to be made. It is also important to take the different pregnancy outcomes into account in these further burden estimates. Of the 125 million pregnancies, one in five are estimated to be terminated voluntarily during the period of risk for miscarriage, and only about two-thirds (82.6 millions) are expected to result in live births. Although malaria in pregnancy is associated with miscarriages and stillbirths [30], the majority of the health and economic burden is likely through the impact on pregnancies that result in live births by increasing the risk of preterm births and low birth-weight [30] and by modifying the susceptibility to malaria in the infant [32]–[34]. Most of the existing research and policy guidance for malaria control in pregnancy has focussed on P. falciparum in the stable transmission regions of sub-Saharan Africa. The results of this study are consistent with the previous WHO-RBM risk estimates for areas with stable P. falciparum malaria in Africa, but our work offers advancement on the existing risk estimates for malaria endemic countries outside Africa. In these regions, the burden of malaria in pregnancy is less well defined, both in terms of the number of pregnancies and its actual impact on health. Policy guidelines for malaria control in pregnancy are also less well developed for these regions. These estimates of the number of pregnancies at risk of malaria provide a first step towards a spatial map of the burden of malaria in pregnancy and a more informed platform with which to estimate the associated disease and economic impact and its geographical distribution. Such global estimates provide guidance in terms of priority setting for resource allocation for both research and policy for the control of malaria in pregnancy. This project provides a dynamic framework that allows risk estimates to be updated when new risk maps of P. falciparum and P. vivax become available as the world attempts to move towards malaria elimination and eradication. Supporting Information Figure S1 Map of the WHO Regions (http://www.who.int/about/regions/en/index.html). (1.07 MB TIF) Click here for additional data file. Table S1 Demographic characteristics and total population at risk of P. falciparum and/or P. vivax malaria by malaria endemic country and by WHO regional office in 2007 (in millions). (0.38 MB PDF) Click here for additional data file. Table S2 Total number of pregnancies by pregnancy outcome in areas with P. falciparum and/or P. vivax transmission by continent in 2007 (in millions). (0.54 MB PDF) Click here for additional data file. Table S3 Total population, number of pregnancies, and number of live-births born to pregnancies in malaria endemic countries by continent in 2007 (in millions). (0.28 MB PDF) Click here for additional data file.
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Factors Affecting the Delivery, Access, and Use of Interventions to Prevent Malaria in Pregnancy in Sub-Saharan Africa: A Systematic Review and Meta-Analysis
Jenny Hill, Jenna Hoyt, Anna van Eijk … (2013)
Introduction Malaria in pregnancy can have important consequences for the mother, foetus, and newborn child, yet the harmful effects are preventable [1]. The adverse outcomes of malaria in pregnancy can be substantially reduced by interventions that have been available for over two decades [2]–[4] and that are inexpensive and cost-effective [5]. Access to and use of these interventions by pregnant women is, however, extremely low, representing a failure of the public health community. In areas of stable malaria transmission in Africa the World Health Organization (WHO) recommends a package of intermittent preventive treatment in pregnancy (IPTp) with sulphadoxine–pyrimethamine (SP) and use of insecticide-treated nets (ITNs), together with effective case management of clinical malaria and anaemia [6]. IPTp consists of two doses of SP taken 1 mo apart commencing in the second trimester [7],[8]. Both IPTp and ITNs are commonly delivered through antenatal clinics (ANCs) through collaboration between malaria and reproductive health programmes. The Roll Back Malaria Partnership aims to ensure that all pregnant women receive IPTp and at least 80% of people at risk from malaria in areas of high-intensity transmission use ITNs by 2010 [9], with even more ambitious targets of 100% for both interventions by 2015 [10]. Achievement of high coverage of these preventive interventions among pregnant women remains elusive for many countries in sub-Saharan Africa [11],[12]. A recent review of national survey data shows that in 27 countries with survey data between the years 2009 and 2011, the median coverage of two doses of SP was 24.5% (range 7.3%–69.4%), even though the median coverage for at least two ANC visits was 84.6% (range 49.7%–96.9%, 22 countries, 2003–2011) (A. M. van Eijk, personal communication), representing substantial missed opportunities at ANCs. Despite the call for universal ITN coverage [13] and all 45 malaria-endemic countries having a policy of providing ITNs to pregnant women, the median use of an ITN the previous night among pregnant women in 37 countries from survey data for the years 2009–2011 was 35.3% (range 5.2%–75.5%) (A. M. van Eijk, personal communication). According to a Countdown to 2015 report, in 20 countries with data, IPTp and ITNs, together with case management of malaria during pregnancy, have the lowest coverage among all the interventions delivered to pregnant women at ANCs [14]. Evidence on the determinants of coverage and reasons for the failure in delivery and uptake of IPTp and ITNs from qualitative [15] and quantitative studies is currently disparate, in addition to which, many relevant reviews are now outdated [5],[16]–[18]. We therefore undertook a systematic review to update the evidence and to integrate findings from three separate syntheses of studies on (1) barriers to achieving high coverage, (2) determinants of uptake, and (3) interventions to increase coverage. We then explored the extent to which the intervention studies have addressed known barriers and determinants, and identified critical gaps in the knowledge required for the formulation of effective strategies. The review was restricted to sub-Saharan Africa as the only malaria-endemic region with a specific WHO strategy for the prevention of malaria in pregnancy, which includes both IPTp with SP and ITNs. Methods Search Strategy We performed a systematic and comprehensive literature search of electronic databases on 23 April 2013, including the Malaria in Pregnancy Library (http://library.mip-consortium.org; updated 20 April 2013) and the Global Health Database [19], and a search of bibliographies of retrieved articles. The Malaria in Pregnancy Library contains peer-reviewed published and unpublished literature compiled from 40 sources including PubMed, the Global Health Library, Google Scholar, Lilacs (Latin American and Caribbean Health Sciences Literature), Popline, the ProQuest Digital Dissertations and Theses database, Web of Knowledge, WorldCat, and registers of trials and studies [20]. A full account of the search terms used is presented in Table S1. Study Inclusion Criteria and Analysis Strategy Titles and abstracts were reviewed independently by two authors (J. Hill and J. Hoyt/A. M. van Eijk). Studies were eligible for inclusion if they met the following criteria: (1) reported an original research study; (2) addressed barriers to, facilitators of, or determinants of the delivery or uptake of IPTp and/or ITNs in pregnancy, or evaluated the impact of an intervention to increase the coverage of IPTp and/or ITNs in pregnancy; (3) were published between 1 January 1990 and 23 April 2013; and (4) were conducted in sub-Saharan Africa. No restrictions were placed on publication language or study design, i.e., quantitative, qualitative, and mixed methods studies were included, and both peer-reviewed papers and grey literature were included. Studies meeting the inclusion criteria were grouped according to whether their content addressed (1) barriers or facilitators, (2) determinants, and/or (3) evaluation of intervention(s); some studies contributed to more than one of these content groups (Figure 2). Studies with content on barriers or facilitators and/or determinants were then further categorised into studies exploring factors among pregnant women, healthcare providers, or both. Studies with content on delivery interventions were categorised by intervention, i.e., IPTp, ITNs, or both. The kappa statistic was used to measure the chance-adjusted inter-rater agreement for eligibility. Data Extraction Two authors extracted data and appraised the quality and content of included studies. J. Hill and J. Hoyt/A. M. van Eijk extracted quantitative and qualitative data on barriers and facilitators from quantitative, qualitative, and mixed methods studies using pre-existing themes used by the authors of the included studies, which were stratified according to whether the views or perspectives were those of pregnant women or healthcare providers; the views or perspectives mainly comprised self-reported information but also observed data. The barrier and facilitator themes were then divided into four predetermined categories adapted from the literature [21],[22] for pregnant or postpartum women (Box 1) and for healthcare providers (Box 2). Because facilitators uniformly reflected the converse of the barriers, we report only the barriers (Table S4). A. M. van Eijk and J. Hoyt/L. D'Mello-Guyett extracted quantitative data from quantitative and mixed methods studies that explored the determinants of receipt of one or two doses of IPTp and ITN ownership and use, henceforth referred to as “determinants”. J. Hill and J. Hoyt/L. D'Mello-Guyett extracted quantitative, qualitative, and descriptive data from the studies evaluating delivery strategies for IPTp and/or ITNs according to the type of delivery intervention, e.g., promotion, training, or type of delivery mechanism. Box 1. Barriers from the Women's Perspective by Level Individual level: factors related to a woman's knowledge, thoughts, beliefs, actions and behaviour, pregnancy, and health status Social/cultural/household level: factors related to a woman's economic and social position, household factors including gender roles, societal and cultural norms and traditions, and religious practices Environmental level: factors related to seasonality of malaria, weather conditions, physical access, and transportation Healthcare system level: factors related to the various components and quality of the healthcare system, such as staff attitudes or performance, medication, service provision, and user fees Box 2. Barriers from the Healthcare Provider Perspective by Level Individual level: factors related to the knowledge, attitudes, and performance of individual healthcare providers Organisational level: factors related to the operation of the health facility unit, such as management, staff rosters/rotation, and services Healthcare system level: factors that are dependent on higher levels of the healthcare system related to the various components and quality of services, such as supply of drugs or ITNs, development and dissemination of policy guidelines, training and supervision of staff, and imposition of user fees Non-Healthcare system: macro-level factors external to the healthcare system such as media, water supply, side effects of medications, and women's practices Two authors (J. Hill and J. Hoyt/L. D'Mello-Guyett) assessed the quality of reporting of individual studies using a checklist of criteria developed a priori based on criteria and methods described in the literature. For observational quantitative studies the criteria of reporting were randomised sample selection, multivariate analysis, and minimising bias through study design and analysis [23],[24]. For qualitative studies the criteria were the extent to which the authors described the sampling strategy, the effects of reflexivity, and methods to ensure reliability and validity [25],[26]. For mixed methods studies, the following reporting criteria were used: justification of mixed methods, clearly described sampling strategy, clear reporting of methods for the qualitative component, analysis strategy, multivariate analyses, minimising bias, and integration of qualitative and quantitative findings [27],[28]. For intervention studies, reporting criteria were presence/type of control, steps to reduce bias, and the extent to which authors described confounding, loss to follow-up, and external validity [29]. No studies were excluded on the basis of quality. Data Synthesis Barriers and facilitators were described and explored using content analysis and narrative synthesis of qualitative and quantitative data. Data from the pregnant women's perspective were synthesised across four levels (individual, household/social/cultural, healthcare system, and environmental) and assessed in relation to receipt of IPTp, ITN ownership, and ITN use. Similarly, data from the healthcare provider perspective were synthesised across four levels (individual, organisational, healthcare system and non-healthcare system) and assessed in relation to the delivery of IPTp and ITNs in the ANC setting. The intervention studies were grouped into common strategies and explored using a narrative synthesis to summarise each intervention and to compare and contrast findings between studies evaluating similar strategies for scaling up one or both malaria interventions. Statistical Analysis We conducted a meta-analysis of data on determinants using Stata version 12 (StataCorp) and Comprehensive Meta-Analysis (Biostat, http://www.meta-analysis.com/). Summary odds ratios (ORs) were calculated using random effects models based on the approach of DerSimonian and Laird [30]. Data were extracted from studies using the following hierarchy based on availability: raw data (numerators and denominators); computed unadjusted ORs, computed adjusted ORs. The use of adjusted (by multivariate analysis) or cluster-adjusted ORs as provided by the studies is indicated in the meta-analysis forest plots. If studies presented results for both “1+ doses” and “2+ doses” of IPTp, only the data for “2+ doses” was used. We conducted sub-group analysis and considered the following factors for IPTp: number of SP doses (1+ or 2+), location of enrolment (community or clinic), study population (postpartum women, a mixed population of postpartum and pregnant women, or pregnant women only), and study country. The subgroup analysis for ITNs considered location of enrolment (community or health facility), study population (postpartum women, a mixed population of postpartum and pregnant women, or pregnant women only), study country, and—for ITNs—type of net (ITN or untreated net) and definition of net use (last night or during pregnancy). Sensitivity analysis was conducted to assess the potential effect of study quality on the examined associations. We assigned studies a score based on the quality assessment, and studies that failed to report on three or more quality criteria scored as low-to-moderate quality. The I 2 and 95% CI were used to quantify heterogeneity [31]. Synthesis across the Barriers, Determinants, and Intervention Studies We compared identified barriers with the determinants identified in the meta-analysis and aligned them with the intervention studies. The barriers were first collapsed into a limited number of key categories using a coding template, and the implications for intervention for each category of barriers were described. We then matched the proposed interventions derived from the barrier studies against the intervention studies included in the review to assess the extent to which the intervention studies addressed the barriers identified in the observational studies. Results Study Selection and Characteristics The primary search identified 1,780 citations (1,240 from the Malaria in Pregnancy Library, 540 from the Global Health Database, and two from bibliographies and authors), from which 271 duplicates were removed (Figure 1). From the remaining 1,511, 1,280 articles were excluded on the basis of abstracts. Of 231 full-text articles reviewed, 133 were excluded as they did not meet the inclusion criteria, the full text was not available, or they contained duplicate data, leaving 98 included articles. There was close agreement between reviewers on the included studies (kappa score of 0.86). 10.1371/journal.pmed.1001488.g001 Figure 1 Flowchart of studies included in the review. 10.1371/journal.pmed.1001488.g002 Figure 2 Analysis strategy. MiP, malaria in pregnancy. Of the 98 included studies, 81 contributed data on barriers and determinants (Table 1), and 20 studies contributed data on interventions that aimed to increase coverage and uptake of IPTp (Table 2) or ITNs (Table 3). One study did not contain data in a usable format for the meta-analysis [32]. The key characteristics of the barrier and determinant studies and of the intervention studies are provided in Table S2. 10.1371/journal.pmed.1001488.t001 Table 1 Data extracted for barriers and determinants by study. Study IPTp ITN Facility-based surveys Barriers Determinants Barriers Determinants Akaba 2013 [34] √ √ √ √ De Allegri 2013 [82] √ √ Aluko 2012 [71] √ √ Amoran 2012a [35] √ √ Amoran 2012b [72] √ √ Arulogun 2012 [55] √ Bouyou-Akotet 2013 [113] √ Diala 2012 [40] √ Iliyasu 2012 [36] √ √ Mubyazi 2012 [63] √ Mutagonda 2012 [43] √ Namusoke 2012 [59] √ Onoka 2012a [37] √ √ Onoka 2012b [114] √ Onwujekwe 2012 [61] √ d'Almeida 2011 [115] √ Donkor 2011 [48] √ Manirakiza 2011 [116] √ √ Napoleon 2011 [117] √ √ Nduka 2011 [118] √ Okonta 2011 [73] √ √ Olajide 2011 [74] √ √ Tutu 2011 [119] √ Smith Paintain 2011 [64] √ Gross 2011 [33] √ Ambrose 2011 [77] √ Sande 2010 [45] √ √ Antwi 2010 [53] √ √ Mubyazi 2010 [52] √ √ Smith 2010 [47] √ Karunamoorthi 2010 [67] √ √ Wagbatsoma 2010 [120] √ Akinleye 2009 [121] √ Takem 2009 [122] √ Klebi 2009 [123] √ Musa 2009 [69] √ Njoroge 2009 [65] √ √ Adjei 2009 [49] √ √ Mubyazi 2008 [18] √ Pettifor 2008 [76] √ √ Anders 2008 [56] √ Onyeaso 2007 [60] √ √ Mnyika 2006 [124] √ Launiala 2007 [44] √ Brentlinger 2007 [62] √ √ Kweku 2007 [83] √ Van Geertruyden 2005 [78] √ √ Gates Malaria Partnership 2005 [39] √ Mubyazi 2005 [41] √ Nganda 2004 [125] √ √ √ Ashwood-Smith 2002 [54] √ Community-based surveys Hill 2013 [126] √ √ Ankomah 2012 [80] √ √ Ansah-Ofei 2011 [46] √ Auta 2012 [81] √ √ Zere 2012 [127] √ √ √ Faye 2011 [128] √ O'Meara 2011 [85] √ Ndyomugyenyi 2010 [50] √ √ Grietens 2010 [51] √ Sangare 2010a [57] √ √ Mbonye 2010 [129] √ Sangare 2010b [70] √ √ Beiersmann 2010 [84] √ Acquah 2009 [130] √ Brabin 2009 [42] √ Gies 2009 [90] √ Gikandi 2008 [131] √ √ Marchant 2008 [58] √ √ Belay 2008 [79] √ √ Hassan 2008 [132] √ Kiwuwa 2008 [133] √ √ Ouma 2007 [91] √ PSI Burundi 2006 [134] √ PSI Rwanda 2006 [135] √ PSI Zambia 2006 [136] √ Mbonye 2006a [38] √ Mbonye 2006b [66] √ van Eijk 2005 [68] √ √ √ Guyatt 2004 [137] √ √ √ Marchant 2002 [75] √ √ Summary total 38 31 28 27 10.1371/journal.pmed.1001488.t002 Table 2 Evaluation of interventions aimed at increasing coverage of IPTp (six studies). Study/Measure Description (Country) Baseline Point of Evaluation Intervention (Percent) Control (Percent) p-Value Intervention (Percent) Control (Percent) p-Valuea p-Valueb Msyamboza 2009 [86] IPTp delivered by community health workers (Malawi) IPTp 2+ 36/87 (41.4) 47/107 (43.9) 0.77 663/912 (72.7) 412/897 (45.9) 19 y) and married women were the most likely to use an ITN. Women with higher education or greater knowledge of malaria or ITNs were more likely to use ITNs than women with lower education or less knowledge, and women who were employed in a wage-paying job were also more likely to use ITNs during pregnancy than farmers or housewives. Women who had received IPTp were more likely to use ITNs. The effect of education on ITN use showed significant variation by country (p = 0.028; Text S2), and the effect of marital status on ITN use varied significantly by location of enrolment (p = 0.001; Text S2). Sensitivity analysis indicated a stronger association between ITN use and marital status in the low-to-moderate quality studies compared to the better quality studies (Text S2). 10.1371/journal.pmed.1001488.g004 Figure 4 Summary odds ratios of determinants of ITN use assessed in 17 studies with quantitative data. SES, Socio-economic status. Intervention Studies Interventions to increase coverage of IPTp The evidence from four studies that evaluated community-based distribution of IPTp suggests that community resources have the potential to complement the delivery of IPTp through ANCs to increase access to and uptake of IPTp among pregnant women [86]–[89] (Table 2). However, there was evidence that community-based distribution may concurrently reduce women's attendance at ANCs, though this was not consistent across the four studies: two studies showed reduced ANC attendance in the intervention sites [86],[87], and two showed increased ANC attendance [88],[89]. An alternative to delivering IPTp through community-based programmes is to employ community-based resource persons to promote IPTp, while referring women to ANCs to be given SP. This approach had substantial success in Burkina Faso, and resulted not only in higher IPTp coverage (71.8% versus 49.2% in intervention and control groups, respectively; p<0.001) but also in women attending the ANC earlier, in their first or second trimester (81.3% versus 70.4% in intervention and control groups, respectively; p<0.001), and in more women making two or more visits (89.3% versus 75.3% in intervention and control groups, respectively; p<0.001) [90]. One intervention study evaluated strategies to improve healthcare provider knowledge and performance on how to deliver IPTp. The study was undertaken in Kenya, 4 y after the national IPTp policy was adopted, and suggests that retraining of healthcare providers on the delivery, timing, and dosing of IPTp significantly increased coverage of IPTp (36.9% versus 10.9% in intervention and control groups, respectively; p<0.001) [91]. Interventions to increase coverage of ITNs The included intervention studies evaluated two main channels for delivering ITNs to pregnant women: campaign delivery (non-targeted) [89],[92]–[94] and routine delivery to pregnant women through ANC services (targeted), with three alternative mechanisms evaluated at ANCs: distribution of free nets with [95]–[97] or without social marketing [98],[99], and distribution of subsidised vouchers [83],[84],[100]–[102]. One study compared the impact of ANC delivery alone versus ANC delivery plus community-based distribution of subsidised nets in Niger (Table 3). Campaign delivery of ITNs to households with pregnant women [89], households with children under 5 y [94], or poor households [93] had limited impact on increasing coverage among pregnant women with one exception, which was a campaign in Senegal that delivered ITN vouchers to all households with children under 5 y, alongside vitamin A and mebendazole (an anthelmintic) [92] (49.2% versus 28.5% ITN coverage in intervention versus control groups, respectively; no statistical analysis reported). In a comparison study in Tanzania, the Tanzania National Voucher Scheme, which provides a voucher subsidy to pregnant women at ANCs, which is then used to purchase an ITN from a contracted retailer, achieved greater coverage than a 3-d mass campaign targeting ITNs to households with infants, based on the assumption that infants sleep with their mothers, a common practice in this setting, or ITNs sourced from retailers [94]. The voucher scheme was, however, inequitable, with fewer poorer women receiving nets [100]. In a comparison study of routine ANC delivery of ITNs alone and ANC delivery plus community-based distribution, there was no significant difference in ITN use among pregnant women between groups [103]. Routine delivery of ITNs through ANCs, by comparison, appeared to be more successful in reaching pregnant women, with four studies demonstrating an increase in ITN coverage among pregnant women compared to baseline [98],[99],[101],[102]. Programmes that delivered vouchers, as opposed to free nets, to women at ANCs experienced more operational challenges [83], and were dependent on retailers having ITN stock available [84]. Social marketing campaigns have been effective in promoting the use of ITNs in some settings through extensive media and educational campaigns that increase awareness about the benefits and importance of ITN use (especially for pregnant women), coupled with provision of readily available ITNs at low cost. They are, however, comparatively expensive to implement and sustain [104]. Implications for Interventions to Address Barriers We aligned the barriers to uptake of IPTp and ITNs against the findings from the intervention studies to determine the extent to which these interventions addressed known barriers (Tables 4 and 5). There were four key categories of barriers to women receiving IPTp: pregnant women's knowledge of IPTp, access to an ANC, affordability of ANC services, and quality of ANC services. Women's lack of knowledge of IPTp was very common and yet may be improved through relatively simple promotional activities delivered through all available channels, such as community-based resource persons, facility-based counselling and education, and messaging via the media and local leaders. We identified only one relevant intervention study, which evaluated community-based promotion of IPTp in Burkina Faso [90]. Women's access to an ANC was a barrier in remote settings, where community-based distribution or outreach services may be required to supplement ANC services. Four studies evaluating community-based distribution of IPTp were identified in the review, using a combination of existing [87],[88] or new community resource persons [86],[89]. 10.1371/journal.pmed.1001488.t004 Table 4 Synthesis matrix comparing findings from observational studies with those of intervention studies for IPTp. Type of Factor Findings from Observational Studies Findings from Intervention Studies Categories Derived from Barriers Implications for Interventions to Increase Uptake Type of Intervention Evaluated Number of Intervention Studies Pregnant women factors Category 1—pregnant women's knowledge Example barriers• Lack of knowledge of the preventive benefits of IPTp• Belief that use of drugs or SP in pregnancy is unsafe, e.g., could cause abortion• Fear of perceived side effects of SP• Unaware of the dangers of malaria in pregnancy Promotion of IPTp strategy and safety of SP for IPTp through a variety of channels, e.g., community-based, clinic-based, media, local leaders Community-based promotion of IPTp and referral of women to ANC 1 study in Burkina Faso (Gies 2009 [90]) Category 2—access to ANC Example barriers• Poor access to ANC• Direct and indirect costs of accessing ANC• Commitments to farming, employment, or childcare• Unwillingness to reveal pregnancy• Lack of awareness of importance of ANC services Community-based distribution of IPTp in hard-to-reach populations with limited access to ANC, e.g., through community-based volunteers and/or community-based referral systems to increase use of ANC Community-based distribution in settings with poor access to ANC, or community-based distribution in settings with existing drug distribution programmes, e.g., onchocerciasis, or community-based referral of women to ANC 3 studies evaluating community-based distribution of IPTp (Okeibunor 2011 [89], Msyamboza 2009 [86], Mbonye 2007 [87]); 1 study in Uganda (Ndyomugyenyi 2009 [88]); 1 study in Burkina Faso (Gies 2009 [90]) Category 3 –affordability of ANC services Example barriers• ANC registration fees• Laboratory fees• Cost of SP• Unofficial penalties charged by healthcare providers for late ANC attendance See healthcare provider factors Category 4—quality of ANC services Example barriers• Providers do not offer IPTp• SP unavailable• Lack of water or cups for DOT• Poor attitudes of healthcare providers• Lack of information or instructions given by healthcare providers regarding IPTp See healthcare provider factors Healthcare provider factors Category 1—provider knowledge Example barriers• Poor knowledge of IPT strategy, timing and dosage of SP• Imprecise estimation of gestational age• Confusion about when to give IPTp in relation to treatment of malaria, HIV, or other• Perception that women will or should not take SP on empty stomach Training and supervision of healthcare providers Training of healthcare providers 1 study in Kenya (Ouma 2007 [91]) Category 2—provider attitudes Example barriers• Health education not given in local language• Information and instructions on IPTp not given to pregnant women• Providers do not offer IPTp• Providers treat women with lack of respect Training and supervision of healthcare providers on provider–client interactions None None Category 3—health facility organisation Example barriers• Restrictive ANC hours• Lack of cups or drinking water• Frequent provider absence from work• Ineffective staff rosters Reorganisation of staff rosters, opening hours, etc., and better management, supervision, and accountability of staff None None Category 4—inadequate guidance on IPTp Example barriers• Variation in information given to healthcare providers on IPTp• No guidelines available at facility• Lack of supervision and monitoring of IPTp• Lack of recent training on IPTp• Private facilities following different practices• Incompatibilities between delivery of IPTp and other health interventions Provision of consistent, simple guidelines to all health facilities, both public and private sectors, together with training and supervision Modelling the effect of simple guidelines on coverage with IPTp 1 study in Tanzania (Gross 2011 [33]) Category 5—fees for ANC services Example barriers• ANC registration fees• Cost of SP• Unofficial penalties charged by healthcare providers for late ANC attendance Modification or removal of user fees and regulation against imposition of penalties None None Category 6—supply of SP Example barriers• SP unavailable• Poor stock control Timely procurement and distribution systems for SP, and system to prioritise use of funds for SP at health facilities None None 10.1371/journal.pmed.1001488.t005 Table 5 Synthesis matrix comparing findings from observational studies with those of intervention studies for ITNs. Type of Factor Findings from Observational Studies Findings from Intervention Studies Categories Derived from Barriers Implications for Interventions to Increase Uptake Type of Intervention Evaluated Number of Intervention Studies Pregnant women factors Category 1—pregnant women's knowledge Example barriers• Lack of knowledge of benefits of ITNs for mother and child• Discomfort of using ITNs• Lack of habit of using ITNs• Fear of chemicals used on ITNs• Perception that there are no mosquitoes Promotion of ITN strategy and safety of insecticides used to treat nets through a variety of channels, e.g., community-based, clinic-based, media, local leaders Promotional campaigns using a variety of channels, e.g., social marketing, clinic-based, media 3 social marketing studies by PSI in Burundi (2007 [97]), Kenya (2008 [95]), and Madagascar (2009 [96]) Category 2—household or cultural constraints Example barriers• Lack of support from husband and/or community• Lack of cultural habit of using ITNs• Cultural beliefs, e.g., resemblance of ITNs to burial shrouds Promotion of ITN strategy and safety of insecticides used to treat nets through a variety of channels, e.g., community-based, clinic-based, media, local leaders As above As above Category 3—access to ITNs Example barriers• Lack of retailers• Cost of ITNs• Inability to pay top-up fees on vouchers• Direct and indirect costs of accessing ITN distribution points Delivery of free ITNs to pregnant women through ANC or campaigns, or delivery of voucher subsidies through ANC or campaigns, or community-based distribution of subsidised ITNs Delivery of free ITNs to pregnant women through ANC or campaigns, or delivery of voucher subsidies through ANC or campaigns, or community-based distribution of subsidised ITNs 3 studies evaluated free ITNs: 2 studies through ANC (Pettifor 2009 [98], Guyatt 2003 [99]) and 1 study through campaign delivery (Thwing 2011 [92]); 7 studies evaluated voucher subsidies: 2 studies via campaign delivery (Ahmed 2010 [93], Khatib 2008 [94]), 5 studies via ANC (Beiersmann 2010 [84], Marchant 2010 [100], Hanson 2009 [101], Muller 2008 [102], Kweku 2007 [83]); 1 study community-based: Nonaka 2012 [103] Healthcare provider factors Category 1—provider knowledge Example barrier• Lack of knowledge of ITN benefits for mother and child Training and supervision of healthcare providers on ITNs None None Category 2—provider attitudes Example barriers• Providers refuse to offer ITNs to pregnant women• Providers impose eligibility criteria for ITNs or vouchers Better training, management, supervision, and accountability of staff None None Category 3—health facility organisation Example barriers• Vouchers not available at facility• As for IPTp Reorganisation of staff rosters, hours, etc., and better management, supervision, and accountability of staff None None Category 4—fees for ANC services Example barriers• ANC registration fees• Cost of ITNs Removal of user fees and regulation against imposition of penalties None None Category 5—supply of ITNs/vouchers Example barriers• Poor stock control• Stockouts of ITNs• Vouchers not available Timely procurement and distribution systems for ITNs or vouchers None None Six key categories of barriers to healthcare providers delivering IPTp were identified: provider knowledge of IPTp, provider attitudes, health facility organisation, policy and guidance, fees for services, and supply of SP. Poor knowledge and poor administration of IPTp guidelines by healthcare providers appear to be substantial barriers to achieving high coverage, as highlighted in several studies included in this review. Provider knowledge of the IPTp strategy could be improved through retraining and closer supervision by district staff; however, only one study was identified that evaluated the impact of retraining of healthcare providers in Kenya on the delivery, timing, and dosing of IPTp [91]. Simplified policy and guidance on IPTp would be a relatively simple intervention to improve healthcare provider practice in delivering IPTp, and while no relevant intervention study was identified, one study in Tanzania modelled the effect of simplified guidelines on coverage with IPTp, demonstrating that coverage could be increased with simplified guidance [33]. No intervention studies were identified that addressed supply of SP, even though this was one of the commonest barriers identified in the observational studies. Poor healthcare provider attitude is a generic problem often entrenched in resource-constrained healthcare system and public sector settings, and may be difficult to address; no relevant intervention studies were identified. Similarly, user fees at ANCs are a generic barrier to ANC services, and no intervention studies were identified that addressed this. Three key categories of barriers to women receiving and using ITNs were identified: pregnant women's knowledge of ITNs, household or cultural constraints, and access to ITNs. As for IPTp, pregnant women's knowledge of ITNs as well as certain household and cultural constraints could be addressed through promotion of ITNs through a variety of channels. Social marketing using extensive media and educational campaigns has been used in a large number of countries, and three evaluation studies were identified in this review [95]–[97]. Access to ITNs has been a problem for women in terms of direct and indirect costs, ITN availability, and access to distribution points. Three studies evaluated the delivery of free ITNs to pregnant women through ANCs [98],[99] or campaigns [92], one study evaluated community-based delivery of subsidised ITNs [103], and seven studies evaluated voucher subsidies delivered through ANCs [83],[84],[100]–[102] or campaigns [93],[94]. Categories of barriers to healthcare providers delivering ITNs were similar to those for the delivery of IPTp: provider knowledge, provider attitudes, health facility organisation, fees for services, and supply of ITNs. We did not find any relevant studies that evaluated interventions that directly addressed these provider barriers. Discussion To our knowledge this is the first systematic review of the factors affecting the delivery, access, and use of interventions to prevent malaria in pregnant women that uses research findings from quantitative, qualitative, and mixed methods studies, that assesses both user and provider perspectives, and that integrates these findings with intervention studies. This analysis provides a comprehensive basis for identifying key bottlenecks in the delivery and uptake of IPTp and ITNs among pregnant women, and for understanding which scale-up interventions have been effective, in order to prioritise which interventions are most likely to have the greatest impact in the short or medium term. Barriers to the delivery of IPTp and ITNs were found at different levels of implementation, and broadly fall into policy and guidance, healthcare system issues, health facility issues, and healthcare provider performance. Whilst many of the barriers reflected broader weaknesses in the healthcare system, some were specific to the intervention. With regard to IPTp, a key identified barrier to effective delivery was healthcare provider confusion about the timing of the two doses of IPTp and whether IPTp can be given on an empty stomach. This confusion stemmed from a combination of unclear policy and guidance, inadequate training, and lack of information and job aids on IPTp. Several studies reported conflicting national policies with regards to provision of IPTp in relation to management of HIV and other diseases or conditions, and when to give IPTp if women have been treated for malaria, a problem also identified in another review [105]. Also, some studies reported that healthcare providers expressed uncertainty over the effectiveness of SP for IPTp. Clearly there is an urgent need for countries to update national IPTp policy and guidance, and to ensure that this information reaches frontline providers at ANCs and outpatient departments providing treatment to pregnant women for illness, e.g., through directives or memos from the Director of Medical Services, as done in Kenya (M. J. Hamel, personal communication). The recent WHO IPTp policy update recommendation with simplified guidance on IPTp dosing, which also restates the continued effectiveness of IPTp with SP, serves as an important opportunity for national programmes to update and reinvigorate their IPTp strategy [106]. Organisational problems at the facility level were also common, such as lack of privacy and confidentiality in the health encounter [51] and the restriction of hours of ANC services, resulting in high client-to-staff ratios, long waiting times [49],[52], and reduced consultation times, all of which contribute to poor quality of care at ANCs. Absenteeism and high staff rotation at the facility leading to lack of continuity of care and high workload among staff on duty was also reported [62]. Most of these organisational problems present another area for improvement in the short term that does not require additional resources, though it will require better management and accountability by the heads of health facilities. Other barriers were, however, dependent on higher levels of the healthcare system, such as high staff turnover [62], understaffing (particularly in remote areas), poor infrastructure [41], poor supervision, and poor use of data to identify problems and inform decision-making. These problems are inherent in the healthcare systems in some areas in some countries, and will require longer term strategies and increased investment in healthcare system strengthening. Also persistently reported across the studies and dependent on action taken at higher levels were stockouts of both SP for IPTp and ITNs, and lack of water or cups for providing IPTp by DOT. The reviewed studies did not explore the reasons for the stockouts, but they are likely to be a combination of lack of funding at the national level for procurement of commodities (i.e., specific to IPTp and ITNs) and problems in supply chain management. Barrier studies among women highlighted additional healthcare system barriers leading to poor uptake of IPTp and/or ITNs. Having to pay user fees or pay for SP, drinking water for DOT, or ITNs was a common barrier, as were the indirect costs associated with visiting ANCs, such as transport, food, and opportunity costs. This finding was supported by the meta-analysis of determinants of coverage among pregnant women, which showed that socio-economic status and employment status are important predictors of IPTp and ITN coverage, respectively. These inequities may to some extent reflect the determinants of women's access to ANCs, where user fees are routinely applied to registration, consultations, laboratory tests, and drugs, as identified in a review of factors affecting utilisation of antenatal care in developing countries [107]. However, in some instances user fees are also applied to SP (e.g., where women have to purchase SP or water to take IPTp by DOT) and to ITNs [108]. This situation calls for a review of charging policies for IPTp and ITNs across national programmes, and of user fees and charges at ANCs in general. Another common barrier to ANC utilisation was the poor quality of interactions between healthcare providers and pregnant women [38],[41]. Women were generally perceived as passive recipients and were provided with little or no information about the services provided [44], and women with a low social position, such as adolescents [51], and less educated women are most vulnerable. This issue appears to be a problem in some resource-poor settings and is more difficult to tackle. However, educating women about their rights and about the ANC services available to them may go some way to empowering women to be able to demand better services. This finding is supported by the fact that pregnant women's lack of knowledge and understanding of IPTp and ITNs was consistently reported in both the barrier and determinant data as an important factor preventing the uptake and use of IPTp and ITNs. Women who understand the benefits of IPTp and the safety of SP, and how and when to take it, are more likely to take it. However, many women do not receive adequate information about IPTp, and this can result in fears that the drug causes harm, even abortion [15], or women showing preference for an alternative drug. Whilst there are some reports that women experience side effects from IPTp, the severity and extent of these events are not clearly described. There were also reports of women fearing that the chemical used on ITNs would harm the foetus [15]. Whilst knowledge is also an important facilitator of ITN use, barrier studies reveal important deterrents to ITN use such as the inconvenience and discomfort of use [109], especially in the dry season, and the lack of a culture or habit of net use. These findings were consistent with the meta-analysis of determinants in that coverage of both IPTp and ITNs was lower among women with no education and, in some countries, women living in rural areas; these women were less likely to access ANC and/or health education services. The meta-analysis was useful in identifying other important risk groups. Younger or adolescent women, unmarried women, and less educated women were significantly less likely to use ITNs. The barrier studies show that this may be related to lower affordability and in-household access among these women. Adolescents, unmarried women, and less educated women therefore constitute high-risk groups for targeting ITNs. This suggests that ministries of health need to pay more attention to IPTp and ITN promotion and health education, with additional targeting of risk groups, as well as using new innovations for communication of messages, since traditional health education is not offered at all facilities or is not always effective. Women seeking care at ANCs often have to overcome barriers at the household or societal level, and these barriers are more challenging to address. Women have commitments to farming or employers and the responsibility of childcare, and often have to defer to their husbands or in-laws in decision-making over accessing ITNs or use of household income to pay for ANC services. In a review of ANC access, use of ANCs was shown to increase with husband's educational level and was an even stronger predictor than women's education in some settings [107]. Local cultural norms and practices present a considerable barrier to women accessing ANC services in some but not all study countries, with wide variation within countries and between countries, a finding also reported in the review by Pell et al. [15]. In comparison to the observational studies, the review identified comparatively few studies that evaluated interventions to promote scale-up of these interventions, particularly for IPTp. Whilst many of the barriers to IPTp and ITN coverage identified in the observational studies related to healthcare providers and service delivery, very few studies that evaluated interventions to improve service delivery were found. Similarly, very few studies explored the determinants of delivery of either IPTp or ITNs among healthcare providers, or supply-side interventions designed to improve the quality of delivery of IPTp or of ITNs with a chosen strategy, whether it be campaigns or routine delivery through ANCs. Of the six studies that evaluated interventions to increase coverage of IPTp, all but one targeted women's knowledge or access, the last being a healthcare provider intervention. Consideration of the context for employing community-based distribution of IPTp is important; this distribution strategy appears to be an effective additional strategy to boost coverage in areas where there is already a successful community-based distribution programme, as seen in the onchocerciasis control programme in Uganda [88], but may serve to undermine women's attendance at ANCs in areas where ANC attendance is fragile. Community-based promotion, on the other hand, has the potential benefit in some settings of increasing access and uptake of IPTp by providing women with information about the importance and benefits of IPTp, and at the same time reinforcing the message that women should obtain antenatal care from ANCs, where they benefit from the full range of focussed ANC services [90]. While 13 studies were identified that evaluated the effectiveness of alternative delivery strategies to increase ITN coverage among pregnant women, the study objectives and designs were heterogeneous; hence, it was not possible to draw generalisable conclusions. Nevertheless, ANC services appear to be an important source of free ITNs for pregnant women in rural areas, a finding supported in a review of best practices of ITN programmes in sub-Saharan eastern Africa [108]. Strengths and Limitations of the Review The review triangulates data from quantitative, qualitative, and mixed methods studies to increase the content validity and comprehensiveness of the review; it does not, however, attempt a full meta-ethnography of qualitative data, which has been undertaken recently by others [15],[110]. The meta-analysis of determinants was used to explore the range of effects between studies and to provide a pooled analysis to support the findings of the narrative (interpretive) synthesis. Although the use of cluster-unadjusted ORs may have overestimated precision, these were limited to four out of 36 studies. There was considerable heterogeneity among studies included in the meta-analysis, and we explored only a limited number of variables in the subgroup analysis to assess whether these could explain the differences between studies (Text S2). The lack of adjustment for ANC attendance in studies using community-based surveys means that the determinants of IPTp use may be partly driven by determinants of ANC access. However, the differences in the results between studies that enrolled women in the community and those that enrolled women in clinics in the subgroup analysis were not significant (Text S2). Whilst distinguishing between use of SP for treatment versus use for prevention poses an important challenge in interpreting community surveys, this limitation was not measured in the studies included in the meta-analysis. Whilst no restrictions were placed on the language of publication, and no studies were excluded on the basis of language, the focus the Malaria in Pregnancy Library (the primary source of studies) to date has been on the European family of languages and predominantly English. Reviewer bias was limited by the use of two independent reviewers to assess inclusion criteria. Reporting of included studies was assessed for quality, and reporting quality for the majority of studies was assessed to be fair. There were three quantitative studies that met no reporting quality criteria and 13 studies that met only one criterion (10 quantitative and three intervention studies). Findings from the studies with data on barriers were found to be entirely consistent with findings from other studies, and provided no new or surprising themes, and inclusion of these studies did not alter the study findings. Our review includes 98 studies from across sub-Saharan Africa, with 77 of these specifically containing data on barriers and determinants of delivery, access, and use of IPTp and ITNs among healthcare providers and pregnant women; this is a sizeable body of evidence. In summary, the delivery and uptake of IPTp and ITNs by pregnant women is impeded by a wide range of factors among both pregnant women and the healthcare system, each influenced by an array of social, cultural, economic, and institutional factors, with each factor influenced by the others in a complex interchange. There are also geographic variations, with some barriers more prominent in some countries than in others. Notwithstanding this complexity, many of the barriers highlighted in this review are relatively consistent across countries and are surmountable: barriers that programmes can address in the near term with limited additional investment. Delivery of ITNs through ANCs presents a narrower range of problems than delivery of IPTp. Actions to increase coverage of IPTp and ITNs in the short term would be (1) to simplify country policies and guidance to align the updated WHO IPTp policy [106] with the new WHO policy for focused antenatal care, consisting of four visits in the second and third trimesters, and ensure effective dissemination to frontline healthcare providers through training and job aids; (2) to earmark funding for procurement of SP and ITNs; (3) to review ANC fee structures; and (4) to launch targeted promotional campaigns to reach high-risk populations of pregnant women, according to local settings, e.g., rural, poor, or adolescent women. Promotional campaigns will need to reflect the needs of women and offer services they will accept at a price they can afford. Other barriers are more entrenched within the overall healthcare system and will require medium- to long-term strategies to improve the overall quality of antenatal services and encourage the habit of ANC use among women. New multifaceted interventions should be explored, such as quality improvement initiatives that link improvements in delivery of IPTp and ITNs to other core ANC services, management tools for facility-level decision-making, and innovations, such as use of mobile phones for defaulter tracing, supply chain/stock control, reporting of health management information systems data on coverage, and surveillance. Increasing drug resistance means that IPTp with SP will most likely be replaced by more complicated and expensive drug regimens [4],[111], or new strategies, such as intermittent screening and treatment [112]. Intermittent screening and treatment will require adjustments to be made in the ANC setting [47],[64], and will not have the added benefit of IPTp in controlling infections that cannot be detected by rapid diagnostic tests or microscopy. Malaria prevention estimates have increased only modestly between 2007 and 2010 (from 13.6% to 21.5% coverage for IPTp and from 17.0% to 38.8% coverage for ITN use) [138]. Conclusion Our synthesis shows that the key barriers to access, delivery, and use of IPTp and ITNs are relatively consistent across countries. These barriers may be helpful as a checklist for use by country malaria programmes and/or policy-makers to identify factors influencing uptake of these interventions in their specific location or context. The review also highlights the need for multi-country studies that evaluate targeted or multifaceted interventions aimed to improve the delivery and uptake of IPTp and ITNs. More research is also needed to understand and improve the policy change process to facilitate future replacement of SP with alternative drug regimens for IPTp or alternative strategies such as screening and treatment that will present even greater challenges for delivery. Supporting Information Table S1 Search terms and databases used in the review. (DOCX) Click here for additional data file. Table S2 Study characteristics. Table S2.1. Characteristics of studies on determinants, barriers, and facilitators. Table S2.2. Characteristics of intervention studies. (DOCX) Click here for additional data file. Table S3 Checklist for quality of reporting. Table S3.1. Checklist for quality of reporting: quantitative studies. Table S3.2. Checklist for quality of reporting: qualitative studies. Table S3.3. Checklist for quality of reporting: mixed methods studies. Table S3.4. Checklist for quality of reporting: intervention studies. (DOCX) Click here for additional data file. Table S4 Barriers and facilitators to delivery, access, and use of IPTp and ITNs. Table S4.1. Barriers and facilitators to receipt of IPTp from the perspective of pregnant and recently delivered women. Table S4.2. Barriers and facilitators to ITN ownership and use from the perspective of pregnant and recently delivered women. Table S4.3. Barriers and facilitators to the delivery of IPTp from the healthcare provider perspective. Table S4.4. Barriers and facilitators to the delivery and use of ITNs from the healthcare provider perspective. (DOCX) Click here for additional data file. Text S1 PRISMA statement. (DOC) Click here for additional data file. Text S2 Meta-analysis of determinants of IPTp and ITN use in pregnancy. (PDF) Click here for additional data file.
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Malaria prevention in pregnancy, birthweight, and neonatal mortality: a meta-analysis of 32 national cross-sectional datasets in Africa.
Thomas P Eisele, David A. Larsen, Philip Anglewicz … (2012)
Low birthweight is a significant risk factor for neonatal and infant death. A prominent cause of low birthweight is infection with Plasmodium falciparum during pregnancy. Antimalarial intermittent preventive therapy in pregnancy (IPTp) and insecticide-treated mosquito nets (ITNs) significantly reduce the risk of low birthweight in regions of stable malaria transmission. We aimed to assess the effectiveness of malaria prevention in pregnancy (IPTp or ITNs) at preventing low birthweight and neonatal mortality under routine programme conditions in malaria endemic countries of Africa. We used a retrospective birth cohort from national cross-sectional datasets in 25 African countries from 2000-10. We used all available datasets from multiple indicator cluster surveys, demographic and health surveys, malaria indicator surveys, and AIDS indicator surveys that were publically available as of 2011. We tried to limit confounding bias through exact matching on potential confounding factors associated with both exposure to malaria prevention (ITNs or IPTp with sulfadoxine-pyrimethamine) in pregnancy and birth outcomes, including local malaria transmission, neonatal tetanus vaccination, maternal age and education, and household wealth. We used a logistic regression model to test for associations between malaria prevention in pregnancy and low birthweight, and a Poisson model for the outcome of neonatal mortality. Both models incorporated the matched strata as a random effect, while accounting for additional potential confounding factors with fixed effect covariates. We analysed 32 national cross-sectional datasets. Exposure of women in their first or second pregnancy to full malaria prevention with IPTp or ITNs was significantly associated with decreased risk of neonatal mortality (protective efficacy [PE] 18%, 95% CI 4-30; incidence rate ratio [IRR] 0·820, 95% CI 0·698-0·962), compared with newborn babies of mothers with no protection, after exact matching and controlling for potential confounding factors. Compared with women with no protection, exposure of pregnant women during their first two pregnancies to full malaria prevention in pregnancy through IPTp or ITNs was significantly associated with reduced odds of low birthweight (PE 21%, 14-27; IRR 0·792, 0·732-0·857), as measured by a combination of weight and birth size perceived by the mother, after exact matching and controlling for potential confounding factors. Malaria prevention in pregnancy is associated with substantial reductions in neonatal mortality and low birthweight under routine malaria control programme conditions. Malaria control programmes should strive to achieve full protection in pregnant women by both IPTp and ITNs to maximise their benefits. Despite an attempt to mitigate bias and potential confounding by matching women on factors thought to be associated with access to malaria prevention in pregnancy and birth outcomes, some level of confounding bias possibly remains. Copyright © 2012 Elsevier Ltd. All rights reserved.
Author and article information
Contributors
Kathryn G. Andrews: kathryn.andrews@mail.harvard.edu
Michael Lynch: mlynch@cdc.gov
Erin Eckert: eeckert@usaid.gov
Julie Gutman: fff2@cdc.gov
Journal
Journal ID (nlm-ta): Malar J
Journal ID (iso-abbrev): Malar. J
Title:
Malaria Journal
Publisher:
BioMed Central
(London
)
ISSN
(Electronic):
1475-2875
Publication date
(Electronic):
23
December
2015
Publication date PMC-release: 23
December
2015
Publication date Collection: 2015
Volume: 14
Electronic Location Identifier: 521
Affiliations
Article
Publisher ID: 1033DOI: 10.1186/s12936-015-1033-4
PMC ID: 4690242
PubMed ID: 26701641
SO-VID: 7b0c71f8-6413-48bc-8bcf-3c08fb93d050
Copyright © © Andrews et al. 2015
License:
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
History
Date
received
: 3
September
2015
Date
accepted
: 3
December
2015
Categories
Subject:
Research
Custom metadata
issue-copyright-statement © The Author(s) 2015
ScienceOpen disciplines: Infectious disease & Microbiology
Data availability:
ScienceOpen disciplines: Infectious disease & Microbiology