Background
According to the World Health Organization (WHO), malaria cases in the year – 2018 were estimated at 228 million cases of malaria worldwide with 405,000 deaths [
1]. Children under 5 years accounted for the largest (67%) deaths [
1]. Of the total number of cases globally, Africa was a home to 93% of malaria cases and 94% of malaria deaths [
1]. In 2013, it was estimated that a total of 437,000 African children died before their fifth birthday due to malaria and the disease caused an estimated global 453,000 under-five deaths in the same year − 2013 [
2]. Through bites of infected mosquitoes, disease causing parasites are transmitted to humans [
1,
3]. Transmission dynamics area shaped by the environmental conditions, lifespan of the vector and the host’s immunity [
1]. Climatic conditions influence the lifespan of the vector while host’s immunity reduce the risk of malaria infection in causing malaria disease in human body [
1]. Several interventions have been implemented over the last decade and have led to observed decline in the malaria burden in sub-Saharan Africa. These interventions have aimed at avoiding mosquito bites through the use of repellents or insecticide treated bed nets, and specific medicines to prevent malaria. However, it still remains a major public health threat in areas within the tropical and subtropical region [
4,
5].
Malaria occurrence has traditionally been observed in the low-land areas, bogs and generally in the plains within the tropical regions [
6]. Comparative analysis have shown the occurrence of such patterns in Africa, Latin America and Caribbean as well as in South East Asia [
7‐
10]. Meanwhile, the afromontane areas characterized with unique biota [
11], that had hitherto been known for being malaria free zones due to altitudinal effect, have seen increased malaria incidences with some areas experiencing a rise while others declining [
12,
13]. Malaria cases have lately been observed to be on the rise in the afromontane ecotones within sub-Saharan Africa such as in the Rwenzori highlands of south western Uganda [
14,
15]. Similar patterns have been experienced in the neighboring highlands of Butare (Rwanda) as well as in the Mount Kilimanjaro area (Tanzania) [
16,
17]. These patterns in malaria have led to increased cost of malaria interventions [
16,
18]. Such trends have been attributed to climate change that is creating ambient conditions within the highland altitudinal belts [
18].
Malaria in Uganda has been endemic in the savannah areas of northern and eastern Uganda especially in Apac district, followed by Tororo district [
19]. All these areas are within 1100 m altitude. However, highland areas especially Elgon region had earlier been reported to experience a surge in malaria cases despite continued intensified control and prevention interventions by both government, private sector and development partners [
14,
16,
20]. These interventions have aimed at reducing malaria infections, reduce morbidity and prevent mortality attributable to malaria [
21]. Control programs like the Uganda National Malaria Control Program (UNMCP) were developed based on the global Roll Back Malaria partnership, United Nations Millennium Development Goal and the 2000 Abuja Declaration [
17,
21]. Implementation of the UNMCP plan is aimed at controlling malaria to reduce its burden on the human population in Uganda, ensure universal access to malaria prevention and treatment, and minimize mortality rate for children under 5 years of age. These strategies have involved integrated vector management, effective diagnosis and treatment, prevention of malaria in pregnancy, and attention to malaria epidemics [
22]. Despite all these interventions, Uganda still ranks among the six countries that contribute more than half of the global malaria cases [
1]. This is partly because of the climate which allows stable, year round malaria transmission with relatively little seasonal variability in most areas [
17]. Within the country, malaria is highly endemic in up to 95% of the country’s area, where 90% of the population of 40 million live [
22]. Despite inadequate information on the type and distribution of malaria parasites, the malaria species that are mainly reported in Uganda include
P. falciparum,
P. vivax,
P. malariae, and
P. ovale [
23,
24].
P. falciparum is responsible for more than three quarters of the cases in Uganda [
23]. It is estimated that other species account for < 5% of cases, with a few percent of infections due to mixed species [
24].
Climate has been pointed out as a key risk factor for spatial-temporal patterns of malaria, especially in the highland areas [
17]. Studies [
19,
25] on malaria patterns in different mountainous areas have been undertaken but only a few [
26,
27] have focused on the patterns of malaria within different altitudinal zones (ecotones). Yet ecotones are characterized with varying environmental conditions that can influence mosquito biology and malaria patterns [
28,
29]. These studies have not documented patterns of malaria following intensified control and prevention interventions in mountainous areas such as Elgon region. This study thus analysed malaria patterns across altitudinal zones of Mount Elgon, one of the areas in Uganda where intensive malaria control and prevention programs have been implemented.
Discussions
There was a declining number of malaria cases across all the altitudinal zones (high, mid and low altitudes) during the study period. This can be attributed to the intensified malaria control and prevention interventions within the study area, and also throughout the whole of Uganda. Intervention efforts by the Ministry of Health in malaria prevention and control through increasing access to health services including basic diagnostics, provision of insecticide-treated mosquito nets could have reduced malaria transmission within the study area. Similar declining trends had been pointed out in other studies conducted throughout the country between 2009 to 2014 [
45]. Conversely, this pattern is contrasts the results in other studies undertaken earlier in highland areas of Kenya that showed malaria incidence to increase over time [
46]. This could be because of the difference in the intensity of the control interventions and other environmental factors that influenced transmission dynamics of malaria. Although a surge in malaria cases was expected in the strongest El Niño years of 2015 and 2016, it was not detected in this study. One of the reasons could be due to the continuing efforts to prevent malaria transmission in Uganda. Recent studies have highlighted distribution of insecticide treated mosquito nets to significantly reduce malaria cases in Uganda [
47]. However, this result could have been masked by the under reporting of the malaria cases.
Malaria patterns revealed a normal curve trend of malaria with the highest peak being in the middle (June–August) of each of the 7 years (Fig.
3). This corresponded to the trends in temperature and precipitation. However, the months of January and December had the least number of malaria cases. This can be linked to the low precipitation amounts during this period limiting availability of water for breeding of mosquitoes. This trend is similar to the results on studies undertaken in highland areas like Mount Kenya where malaria was prevalent during dry seasons [
46,
48]. This trend can be linked to the availability of conditions favorable for growth and development of mosquitoes that transmit malaria parasites. Increase in temperature and availability of water sources favors mosquito breeding and its transmission of malaria parasites [
49].
Spatially, the hotspot of malaria varied over the 7 year period dominating the lowland areas of the district (Fig.
4). The highland areas had lower number of malaria cases compared to the lowland areas. There was a significant negative correlation between malaria patterns in the lower belt and temperature. Also, there was a significantly positive correlation between malaria and rainfall within the lower belt. In the mid altitude areas, malaria had a significant positive correlation with rainfall. Meanwhile in the high altitude areas, malaria had a significantly negative correlation with maximum and minimum temperature. Also, malaria had a significant positive correlation with rainfall.
Although previous studies noted the critical role of increasing temperature in causing surge in malaria within sub-Saharan Africa, recent studies have shown that, temperature at times can significantly reduce the vectorial capacity of the mosquitoes [
50,
51]. Ambient conditions of temperature enhance transmission by influencing vector and parasite life cycles [
27]. However, increased or reduced temperature beyond optimal ranges can undermine the life cycle of mosquitoes limiting its transmission of malaria parasites [
52]. Studies have highlighted the biological amplification nature of temperature on mosquitoes [
53‐
55]. This study showed that the mean temperatures within the three altitudes varied. The difference in the contribution of maximum temperature to malaria cases between different altitudes can be attributed to the differences in prevailing temperatures in the three zones. The lower and mid altitude areas being relatively warmer and the district (Kween) having only one rainfall season was probably the main limiting factor in malaria vector development in the highland, mid and low altitude zones. Hence the onset of rainfall increased the media for vector growth and development. While rainfall creates the media, ambient temperatures favor the development and survival rates of both vectors and parasites. These conditions can be attributed to the trends of malaria in the three zones (high, mid and low) of Kween District. The highly seasonal rainfall within the study area could have limited the growth and development of mosquitoes.
The pronounced malaria cases in the lower altitude zones compared to the higher altitude zones can be linked to the environmental conditions favorable for mosquito growth and development. The alternating trends can be alluded to temperature and rainfall as the latter can either favor or discourage optimal growth and development of mosquitoes [
56]. In the low altitude areas where malaria had a significant relationship with malaria, it has been noted that temperature can determine the length of the time the mosquitos explore food resources while transmitting malaria [
57]. This could be the same case in low altitude areas. This study was limited by lack of data on the actual malaria and mosquito vectors. This would have complemented information on understanding of the life cycle of the parasites. Future studies ought to incorporate these aspects.
Regarding effects of vegetation cover and human population on malaria, malaria had a significant negative correlation with NDVI. Similarly, in the lower altitude, malaria had a significant negative correlation with human population and NDVI. This implies vegetation increase significantly influenced malaria cases in the high altitude areas. Increase in vegetation enhances the habitat range for mosquitoes. This result has been highlighted in some studies that note vegetation cover to influence dynamics of growth and development of mosquitoes and that of the vector [
58]. Also, increase in human population over time in these areas could have caused a decline in vegetation cover that would facilitate transmission of malaria by mosquitoes. Over time, extension of health services also with increasing human population could have contributed to the declines in malaria with increasing human population. Although the result regarding these two aspects in this study reveal interesting results, it was limited by the inability to disintegrate data into shorter time ranges. This was due to the unreliability of the data. Therefore future studies ought to further explore vegetation and population dynamics at monthly level and their effects on malaria incidences. This will generate information on how human activities influence transmission and incidences of such infectious diseases.
Forecasts of malaria patterns revealed a continued decline of malaria cases given conditions remain constant. However, the number of malaria cases may significantly explode if temperature and rainfall increase. This implies that interventions at this point ought to be intensified. There is also a window of opportunity for eradication of malaria in the event that the existing control and prevention interventions are intensified. This thus calls for more studies to inform modification of the interventions.
One of the limitations of this study was the use of data from ministry departments in Uganda. There is therefore no proof of validity of this data as some of it was not complete. However, it gives a general picture of what can be done so as to curtail malaria infections within high altitude areas.
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