This study aimed to measure the burden of Plasmodium spp. infections amongst asymptomatic and symptomatic school-age children living in rural and urban areas in Kinshasa, DRC.
Kinshasa, the capital city of DRC, constitutes an urban malaria facies where malaria prevalence is moderate, with an average of eight percent of the population infected at any given time in the city, with increase prevalence variations away from the city centre (23, 25). Malaria transmission rates are not homogenous throughout the city and depend on the population density and level of urbanization. The prevalence is highest in the more densely populated and less urbanized zones in the periphery (23, 26). Additionally, malaria infection usually follows a seasonal pattern regulated by mosquito population fluctuations controlled by climate (26, 27). This study was conducted at the beginning of the rainy season between October and November when conditions of temperature and humidity are favourable for malaria transmission. Temperature, humidity, and rainfall constitute important drivers of mosquito dynamics and malaria risk (27-29).
School-age children currently constitute a neglected group regarding the control and prevention of malaria in the DRC, which currently predominantly targets children under five years old and pregnant women (23). The prevalence of malaria parasite infections found in this study was 62.3% (80.0% in rural area and 45.2% in urban area) in asymptomatic children and 94.7% (97.2 % in rural area and 92.2% in urban area) in those children with symptoms suggestive of malaria. The high prevalence found in both asymptomatic and symptomatic children highlights the importance of malaria in this age group in Kinshasa.
At least nine out of ten children that presented at a health facility with fever or malaria-related symptoms were found to be infected with malaria parasites. The WHO recommends that anti-malaria treatment is given only after a positive confirmatory test for malaria, by means such as microscopy or RDT. However, both microscopy and RDTs carry some risk of false negative results, compromising treatment in some cases. Additionally, not all symptomatic children can attend health facilities despite the fact that the NMCP provide diagnosis and treatment free to all children attending health facilities for confirmatory test. This situation may be due to sub-optimal communication between NMCP health professionals and community members or due to a lack of available transportation fees for access to the health facility. In this study, among the children surveyed, nearly 66% (rural) and 62% (urban) of children did not go to health facilities for confirmatory testing in the last time they had malaria-like symptoms, and among them, 44% and 17% reported having self-medicated, respectively.
We observed a high prevalence of Plasmodium spp. infection in asymptomatic school-age children of 45% and 80% in the urban and rural settings, Our findings are similar to those found in a survey conducted in Lualaba, DRC (77%) (30), and in the national malaria survey in Cote d’Ivoire (63.3%) (31), whilst differing from a study conducted in Uganda (30%) (20). Studies conducted in Kenyan schools between 2008 and 2010 showed a prevalence of 4% with a range between 0 and 71% (32). Discrepancies in prevalence may be explained by differences in detection techniques used, differences in season of sampling, and transmission setting differences (13, 20, 33). Malaria management policies regarding prevention and control measure also differ between countries and may be expected to account for some of the differences in prevalence observed.
In asymptomatic children, all Plasmodium species infections were significantly more prevalent in the rural area compared to the urban setting. There was a significant difference in malaria prevalence in children living in rural as opposed to urban areas, with the former five times more likely to be infected with malaria parasites. This finding is an agreement with numerous previous reports, and likely reflects the fact that the ratio of mosquitoes to humans is higher in rural areas than in urban areas (26, 27, 34).
It has been shown that, in urban areas, modern housing, high human population densities, awareness of use of insecticides and bed nets may reduce the risk of malaria transmission by reduction of human-mosquito contacts and individual biting rates (35, 36). An increase in the density of dwellings in older urban districts of Kinshasa has contributed to the scarcity of Anopheles breeding sites through elimination and pollution except in areas using urban agriculture and gardens (26). A relationship between areas close to agriculture fields and high malaria prevalence or transmission was found in Ghana, Uganda, Benin, and Cote d’Ivoire(37-42). Proximity to permanent larval habitats sites (43), inadequate social-health resources and lower health spending (44) may facilitate transmission in rural zones.
A study previously conducted in Kinshasa showed that in urban areas of the city, most of the mosquito nuisance is caused by Culex quinquefasciatus which accounted for 96% of the 121 bites/ person/night (b/p/n). The only malaria-vector mosquito detected was Anopheles gambiae sensu stricto which accounted for an average of 5.1 bites/person/night with a sporozoite rate of 1.86%, while in rural areas, mosquito nuisance is lower (20bites/person/night), and almost entirely due to six species of Anopheles including four vectors of malaria: An. gambiae, An. funestus, An. nili and An. brunnipes with mean sporozoite rates of 7.85%, 6.60%, 6.63% and 0.53% respectively. The study concluded that Anopheles gambiae had higher daily mean survival rates in rural areas (0.91) than in urban areas (0.78) leading to a greater malaria transmission rate in the former setting (27). This is supported by a meta-analysis which found that in sub-Saharan African cities, the mean annual entomologic inoculation rates (EIR) were 7.1 in city centers, 45.8 in periurban areas, and 167.7 in rural areas (45). However, apid and unprecedented urbanization in sub-Saharan African, combined with often increasing rates of poverty amongst city dwellers may increase the proportion of the malaria burden borne by urbanites (46).
We found no significant difference in Plasmodium spp. infections between genders in either asymptomatic and symptomatic children in both rural and urban areas. These findings agree with previous studies that demonstrated equal exposure between males and females to malaria risk at or below 12 years of age (47, 48).
We found that age, generally, was not associated with Plasmodium spp. infections. However, there was a significant association between age and asymptomatic P. malariae and P. ovale infections in the rural area, and P. falciparum infections in urban setting, with children aged 10 to 14 years more infected than those aged 6 to 9 years. Older children were also the group most likely to harbour more single and mixed infections than younger ones. The proportion of children infected with P. falciparum remained constant for all ages in the rural area, while it increased with age in the urban setting. Plasmodium malariae and P. ovale infections increased with age in the rural area while they did not do so in the urban setting. That difference may be due to age-related acquisition of parasite-tolerating immunity (49, 50). It has been shown that in malaria tropical facies, malaria pre-immunity starts building up around 10 years (23). It may also reflect the relative force of infection of the species, with that of P. falciparum being higher than the other two species in the rural setting.
The presence of P. ovale and P. malariae, co-infected with P. falciparum, highlights the impact of those two parasites in asymptomatic and chronic malaria infection. Plasmodium malariae and P. ovale are not usually associated with severe malaria but P. malariae may be responsible for chronic nephrotic syndrome which can be fatal (51), and chronic infections that can last for years (52), even after leaving endemic regions (44, 53). Plasmodium ovale is responsible for relapses after months or even years without symptoms due to the presence of hypnozoites (54-60) and it has been shown to cause severe disease and even death on occasion (61-63). Younger school children become sicker with malaria and receive treatment more often, while older children, due to increasing immunity, are more likely to be asymptomatic and receive treatment less often (26).
Our data are in agreement with previous reports that show that P. malariae is much less likely to be observed in mixed species infections with P. falciparum in symptomatic malaria infections when the transmission rate of malaria is high (64, 65). The reason for this is currently unclear. It is possible that there is a protective effect of mixed infection with P. malariae on the severity of the disease caused by P. falciparum, perhaps mediated through cross-immunity. It is also possible that in symptomatic P. falciparum infections, this species competitively excludes co-infecting species due to increased parasitaemia. This exclusion could result from within-host competition for resources (66). Or through host-immune mediated mechanisms in which the innate immune response triggered by the high parasitaemia P. falciparum disproportionately affects the less dominant of the species in the co-infection. A further possibility is that the nested PCR methodology used here to determine parasite species may miss the less common of co-infecting species when the disparity between them is large as is likely in symptomatic P. falciparum infected patients.
We did not detect P. vivax in any child in this study. This may be due to the high prevalence of the Duffy blood-group-negative phenotype amongst the children surveyed (67), or due to a lack of circulation of the P. vivax parasites in these areas. However, Kavunga et al (68) describe P. vivax in children under five living Kinshasa and North-Kivu in DRC emphasizing the need for continued monitoring of this species among Duffy blood-group-negative populations (49, 50).
Based on the high prevalence of malaria parasites in this study, we advocate integration of the WHO T3 (Test-treat-track) strategy in schools, including the training of teachers in health education, particularly regarding the use of mosquito bed nets (69). It has been shown that net coverage is relatively low in school-age children (12). In this study, use of mosquito bed net was not associated with plasmodium infection prevalence maybe due to small number of interviewed children. However, the coverage of use of mosquito bed net among them was low. Only 46% of children surveyed had mosquito bed nets in their houses but 38% of these did not use a net the previous night.
It is important to enhance control measures for asymptomatic malaria parasite carriage amongst school-age children to protect them against conditions such as chronic anaemia, absenteeism, reduced school performance, and other complications (17, 19). We found that 45% of children surveyed had previously missed classes due to malaria and of these, 40% had missed five days or more of school, illustrating the high educational burden of the disease amongst this age group.
The government should consider revising its policy regarding malaria control if the target of a 75% reduction in malaria mortality and incidence is to be achieved by 2025 (70). Regarding the global technical strategy for malaria 2016-2030 initiated by the WHO, the DRC is currently working on strategies to entirely implement the first pillar, ensuring universal access to malaria prevention, diagnosis, and treatment. Furthermore, the DRC ministry of health is exploring for mechanisms and strategies for control and prevention which will have positive impacts on malaria elimination in the country. We advocate the inclusion of school-age children in country-wide malaria survey, control, and prevention. We believe that malaria elimination in the DRC may only be possible if all age groups are included in intervention strategies, not just children under five and pregnant women. Thus, the implementation of malaria preventive treatment in younger and older children will help to reduce the burden of malaria in these susceptible groups.
It has been shown that continuous systematic malaria screening and treatment of asymptomatic individuals, such as school-aged children, in high-transmission settings may reinforce malaria intervention measures (7, 71, 72). Moreover, school-based malaria prevalence surveys (are easier to conduct and are cost-effective for more defined assessments at the local level, including routine longitudinal malaria surveillance as it is a reliable indicator of malaria burden and transmission intensity in a defined community (30, 73).