Does socio-economic status explain the differentials in malaria parasite prevalence? Evidence from The Gambia

The worldwide malaria burden is currently estimated at about 207 million cases and 627,000 deaths. Sub-Saharan Africa bears the heaviest brunt, with 90% of all deaths, 77% among children under-five. Nevertheless, between 2000 and 2012, malaria mortality rates have decreased by 42% worldwide (by 48% in children under-five) and by 49% in the African Region (by 54% in children under-five)[1].

Malaria is commonly associated with poverty[2‐10]. Macro-level estimates show strong links between malaria and poverty. For instance, the malaria burden is highest in the poorest countries, particularly in sub-Saharan Africa, where poverty is widespread and with little economic growth over the past quarter century[5, 6]. The gross national product (GNP) in malaria endemic countries is more than half lower than in non-endemic countries[6]. The poorest 20% of the world’s population contribute to 58% of all malaria deaths[11]. Increasing evidence at macro-level suggests that the causal link between malaria and poverty runs in both directions[3‐6].

A review of micro-level (household and population) analyses on the link between malaria and poverty has produced mixed results[12]. Out of nine studies, only two reported a significant association between malaria and poverty[12]. Data from 29 demographic and health surveys (DHS) in 22 countries were used for an aggregate-level regional data analysis for West and Central Africa, and East and Southern Africa, including individual child and country-by-country analysis. No differences were found at the household level in the incidence of fever between the poor and the less poor, though significant differences were found at more aggregate-levels, i.e., country-by-country as opposed to regional-level analysis[13]. In Ghana, social class was not associated with risk of malaria infection[14]. In Tanzania, there was no association between self-reported malaria and socio-economic status (SES) but malaria prevalence was significantly higher among the lower SES individuals[15]. In Nigeria, self-reported malaria or fever was more frequent among the better-off SES and urban dwellers[16] though an earlier study showed a heavier malaria burden among the poor (<US $1/day) compared to the rich[17]. Contrasting results are function of the methodology used to measure malaria and poverty. Studies based on self-reported fever are likely to overestimate the malaria burden while differential reporting of morbidity across socio-economic groups may also influence the results[7, 12].

In 2010/11, The Gambia conducted its first nationwide baseline Malaria Indicator Survey (MIS) in six health regions[18]. The survey covered 4,500 households. Data were collected on long-lasting insecticidal nets (LLINs) coverage and use, malaria case management, intermittent preventive treatment in pregnancy (IPTp), indoor residual spraying (IRS), household assets, general knowledge and practice on malaria prevention and control. In addition, a blood sample to determine the infection status and the haemoglobin level was collected among selected individuals.

In this study, laboratory-confirmed malaria infection and wealth quintiles were used to assess the association between SES including housing quality and malaria infection. The results are reported below.

Over 18,000 blood slides were collected. The overall malaria prevalence among children aged six to 59 months as determined by microscopy was 4% (5,118). SD Bioline Malaria p/f pan had a sensitivity of 99.0% (95% CIs: 97.5-99.7) and specificity 98.1% (95% CIs: 96.7–99.0), consistent with the manufacturer’s estimates[18].

Malaria parasite prevalence among children was highest in the Central River Region (CRR), 9.9% (1,445) and the Upper River Region (URR), 4.4% (964); and lowest in the North Bank East Region (NBER), 0.5% (527) and the Lower River Region (LRR), 0.8% (481). The Western Region (WR) and the North Bank West Region (NBWR) had malaria parasite prevalence of 2.5% (1,027); and 3.1% (674), respectively[18].

The CRR had the highest percentage of poorest households (54.2%), followed by the URR (29.1%) and the NBWR (24.3%) (Table 1). Prevalence was heterogeneous, with values of 0% or <5% in the WR (Figure 1) although some EAs in the NBWR had higher prevalence (Figure 2A). Most EAs with moderate-high to high prevalence were found in the CRR and the URR i.e. the central and eastern parts of the country (Figure 2B-C).

Malaria prevalence was strongly associated with SES, even after adjusting for age, sex and health region, regardless of the age group. These findings are consistent with previous studies carried out in sub-Saharan Africa in which other measures of SES such as occupation, housing type, including the uptake of interventions, e.g., ITNs and expenditure on chemoprophylaxis were associated with malaria infection[12, 26‐31].

The recent findings by Tusting et al.[9], is also consistent with this study. However, these findings differ from Somi et al.[15], who found no association between malaria and SES, and Somi et al.[32], who found negative associations between malaria and SES running in both directions. In addition, the findings of this study are contrary to a study[16] in southeast Nigeria based on self-reported malaria or fever, which found more malaria among better-off SES and urban dwellers compared to the poor.

Age, health region and sex were not significantly associated with malaria prevalence across sub-population groups. However, malaria prevalence was significantly higher in the CRR compared to the URR, with males being more at risk than females. It is interesting noticing that the CRR is the poorest in The Gambia followed by the URR[23, 33].

The high malaria infection in the CRR and the URR (i.e. eastern parts of the country) can be explained by ecological factors such as fresh water, floodplains, swamp and upland rice fields, higher temperatures and lower humidity compared to the WR (western half of the country). Studies have shown that swamp rice fields are important habitat for mosquito larvae[34, 35].

The malaria burden has also shifted from under-five children (six to 59 months) to children aged five to 14 years; OR = 1.4 (95% CI: 0.9; 2.1), p = 0.168, see Table 8). The reasons for the shift in malaria burden from the under-fives to the older children aged five to 14 years are unclear. One hypothesis is that The Gambia NMCP had initially over focused (i.e., activities and information, education and communication (IEC) messages) on the under-fives (0–59 months), particularly for ITN coverage. However, the finding is consistent with a study in northeast Tanzania, which showed that children aged five to 13 years were now at a higher risk of malaria compared to under-five children. The odds of having malaria were also higher for males compared to females in northeast Tanzania and Ethiopia[28, 36].

Historically, malaria elimination in the USA, Italy, Greece, and Spain was achieved through socio-economic development and intensive anti-malarial interventions, such as improved housing. Doors and windows were screened to reduce contacts between mosquitoes and people coupled with combined environmental management, e.g., draining of swampland to eliminate breeding grounds of certain vector mosquitoes and IRS using DDT[6, 9]. For example, in The Gambia, a randomized controlled trial of full screening of doors and windows and closing of eaves showed a 50% decline in the risk of anaemia-related malaria among children[37]. This randomized controlled trial has proved that improvements in housing quality can greatly reduce malaria transmission and incidence.

Interventions aiming at improving the living conditions of populations in endemic communities can have a major impact on the malaria burden[4]. This is also supported by the finding that housing construction materials, e.g., type of wall, floor, roof, and window, are strongly associated with the risk of infection in most age groups, though in the general population this was true only for poor wall housing materials. The association with type of housing and risk of malaria has already been described in other countries. In Mozambique[38], Eritrea[39, 40] and the Lao People’s Democratic Republic, living in houses with grass roof was associated with higher odds of malaria infection[41]. Similarly, houses constructed with bamboo walls, poorly fitted windows and doors, and often inhabited by people from low SES were associated with mosquito house entry[41]. Living in houses with no windows or screens is likely to increase individual contact with the mosquito vector[42]. Mud used as wall material was associated with high prevalence of malaria[43].

However, the study has several limitations. The analysis did not include women aged 15–49 years who were pregnant at the time of the survey due to the paucity of the data (only 148 women). Nonetheless, compared to the other subpopulations in this study, pregnant women had the lowest malaria parasite prevalence of 6.8% (95% CIs: 2.7-10.9%). Also, interventions such as ITN/LLIN ownership and use and IRS were not included due to the paucity of data.

Over the last decade, The Gambia has made significant progress in reducing the malaria burden. All-cause under-five mortality declined from 141 deaths per 1,000 in 2002 to 131 deaths per 1,000 in 2007[19] and further declined significantly to 109 deaths per 1,000 in 2012[44]. A new Malaria Strategic Plan and Policy for the period 2014–2020[45, 46] with a vision of a ‘malaria-free Gambia by 2020’ has been prepared. Nevertheless, malaria transmission is still ongoing, despite the achieved high coverage of preventive and curative interventions. There may be the need of additional interventions targeting the human reservoir of infection and aiming at interrupting transmission.

The findings of this study pose major challenges for malaria prevention and control interventions in The Gambia. First, there is the need to address the unacceptably high malaria burden among the poorest communities in the CRR, URR and NBWR. Studies have shown that malaria infections and mosquito vectors are not homogenously distributed within population groups and areas. Thus, it is argued that countries address the heterogeneity in malaria transmission long before they enter the pre-elimination phase[43, 47, 48]. Second, there is the need to consolidate the gains made as The Gambia moves towards the malaria pre-elimination phase. Increased funding is critical in achieving these objectives. Currently, the country is the only one in the sub-region where malaria interventions are funded from a single source, the Global Fund for AIDS, Tuberculosis and Malaria (GFATM). Funding is therefore a major challenge, which threatens the prospects for sustained malaria decline.

The evidence suggests that malaria infection was strongly associated with low SES. Children from the poorest quintiles, living in poor housing conditions were more at risk of having malaria infection. While intensifying the existing malaria interventions may reduce malaria in the short term, investments in strategies that address socio-economic disparities and improvements in the quality of housing could, in the long term, significantly reduce the malaria burden in the poorest communities.