Environmental Modifications in sub-Saharan Africa: Changing Epidemiology, Transmission and Pathogenesis of Plasmodium falciparum and P. vivax
Lead Institution: University of California, Irvine
ICEMR website: https://www.icemreastafrica.org/
The overarching goal of this ICEMR is to assess the impact of human-induced environmental modifications such as dam construction, irrigation, and shifting agricultural practices on the epidemiology, transmission, pathogenesis, and immunology of Plasmodium falciparum and P. vivax malaria in Kenya and Ethiopia. Major investments in water resource development are taking place in these highly populated countries, but it is unclear how these environmental modifications are impacting the risk of malaria.
African countries are building dams to address the issues of food insecurity and increasing demand for electricity. A number of large and small dams are currently under construction in sub-Saharan Africa. While dams could solve some problems, they may exacerbate others such as malaria. Mosquitoes that transmit malaria breed and lay their eggs in shallow pools of water. Dams and irrigation canals provide shorelines that may contain many such shallow pools.
ICEMR investigators have found that the number of people living within approximately three miles of large dam reservoirs in sub-Saharan Africa increased from around 14 million to about 19 million between 2000 and 2015. During these 15 years, the number of large dams increased from 884 to 919 in Africa based on the dams registered in the World Register of Dams database.
The relationship between dams and malaria is not entirely straightforward. Dams do not always result in an increase in malaria cases, and when they do, the degree of increase is not uniform. Multivariate analysis of the relationship between malaria incidence and environmental variables found the slope of the dam reservoir shoreline to be the most important predictor for the degree of malaria transmission surrounding the dam. ICEMR researchers have shown that in regions which are otherwise suitable for mosquito breeding, the slope of the reservoir shore plays the largest critical role in determining the occurrence of malaria in the vicinity of dams. Reservoirs with a lower slope at the shoreline have higher impacts on malaria. A gentle slope generally corresponds to poor drainage, promoting the persistence of surface water bodies and the formation of stable pools that are favorable habitats for mosquito breeding. Gentle slopes also provide suitable areas for cattle to drink water resulting in numerous hoof-prints that also are conducive for mosquito breeding. In contrast, a steeper slope facilitates drainage and reduces the likelihood that pools will form for periods long enough for mosquitoes to complete their aquatic development.
ICEMR researchers found that agricultural irrigation practices also play a key role in altering malaria vector populations. Observational studies at ICEMR sites in Ethiopia and Kenya showed that agricultural irrigation increased anopheline mosquito breeding habitat diversity, larval occurrence, and abundance, contributing to the proliferation of suitable breeding habitats for malaria vectors. Integration of a high resolution distributed hydrological model with remotely-sensed data in a study site in Ethiopia (Arjo-Dedessa irrigation development site) found that irrigation increased the probability of occurrence of larval habitats significantly during the dry season and during the rainy season. The stability of the habitats was prolonged, with a significant shift from semi-permanent to permanent habitats. The high-risk window (June to September) for larval breeding was also extended by two months due to irrigation. Incorporating larval source management into routine malaria vector control strategies could help reduce mosquito population density and malaria transmission around irrigation schemes. Consequently, increased Anopheles species diversity, abundance, and density were found during both dry and wet seasons. The presence of such diversified malaria-transmitting Anopheles species could contribute to increased risk of year-round malaria transmission complicate disease prevention and control.
The World Health Organization has set a target of reducing global malaria cases and mortality rates by at least 90% by 2030. However, ICEMR investigators caution that dam reservoirs will continue to be focal points for malaria transmission in sub-Saharan Africa, home to 90% of the global malaria burden. Researchers urge that more rigorous impact prediction assessments must be done at the planning stages to determine the likely malaria impacts when considering new dams. Greater consideration must be given to the design of the dam reservoir, water management, and developing new malaria control tools suitable to dam and irrigation settings where larval breeding sites are very abundant.
The existing first-line vector control tools (long-lasting insecticidal nets and indoor residual spraying) have led to a significant reduction in the malaria burden globally over the past decade. However, these tools alone are not sufficient to achieve malaria control and elimination in Africa due to their reduced efficacy resulting from widespread insecticide resistance and outdoor mosquito biting. Interventions that utilize alternative mechanisms of action—such as repellents and chemical compounds that inhibit adult vectorial capacity—may provide a valuable supplement to existing vector control tools. However, the effectiveness of these products against insecticide resistant malaria vectors is unknown. The ICEMR team is conducting a study to evaluate the effectiveness of spatial repellents currently on the market and new technologies in controlling malaria vector populations.
ICEMR researchers tested spatial repellents to determine if they deter pyrethroid resistant mosquitoes from house entry in MalariaSpheres, which are contained semi-natural systems for studying mosquito behavior. For the study, two huts were present inside the Malariasphere, one untreated and the other treated with a candidate spatial repellent. Unfed insecticide resistant female An. gambiae mosquitoes and unfed susceptible female An. gambiae mosquitoes, marked with different fluorescent dyes, were simultaneously released midway between the two huts. Those mosquitoes that entered each hut were recaptured using MM-X traps baited with an odor blend mimicking human odor to evaluate the impacts of spatial repellents on house entry of insecticide resistant mosquitoes.
Three key general mosquito behavioral patterns were observed: a) there were fewer An. gambiae mosquitoes (susceptible and resistant) in huts treated with commercial repellent products, b) more resistant than susceptible An. gambiae mosquitoes ‘chose’ untreated huts, and c) more resistant than susceptible An. gambiae mosquitoes were repelled by commercial repellent products administered through electric vaporization of impregnated vapor mats and liquids. These data indicate that commercial repellent products sold in Africa may be effective in repelling resistant strains of An. gambiae mosquitoes. Thus, these products may be effective supplements to the traditional vector control tools.
The next step in the study will be to examine the impact of the repellent compounds on house entry and exiting behavior of malaria vectors and the effect of different repellent concentrations using bioassays in MalariaSpheres and video-recorded flight track 3D analysis. ICEMR researchers hope the results from this project will provide an important foundation to determine whether future open-field trials of the entomological and epidemiological impacts of spatial repellent strategies are warranted in the context of rising pyrethroid resistance in malaria vectors in Africa.
Surveillance of malaria vectors is critical to determine malaria transmission intensity and to evaluate the impact of control interventions. In most African countries, malaria vector surveillance activities have mainly relied on sampling host-seeking and indoor resting mosquitoes. The most commonly used methods for sampling host-seeking vectors are human landing catches (HLC) and CDC light traps. In addition, indoor-resting vectors are often sampled by pyrethrum spray catches (PSC) and aspirators. Over the past decade, there has been an increasing shift in vector species composition from anthropophagic (human biting), endophilic (indoor resting) vectors to zoophagic (animal biting), exophilic (outdoor resting) sibling species following the widespread use of insecticide-treated nets and indoor residual spraying. Yet, outdoor resting vector sampling is seldom included in the routine vector surveillance system due to a lack of standardized and efficient traps.
The ICEMR aims to develop low-cost, exposure-free malaria vector surveillance methods. One tool ICEMR researchers have tested is the sticky pot, which is a sticky variant of a clay pot. Clay pots have been used previously to collect outdoor resting Anopheles mosquitoes. In a sticky pot, the internal surface of the clay pot is covered with waterproof black papers coated with Tangle-Trap sticky substance. The addition of this sticky substance allows for mosquitoes that rest within the pot to be continually trapped for surveillance, rather than only observing the fraction of mosquitoes that happen to be resting at the time of collection in a standard clay pot. Sticky pots are made using locally available clay pots, so they are low cost. Additionally, sticky pots do not require a battery like some alternative trapping methods. In ICEMR study sites, sticky pots collected about 58% more An. gambiae mosquitoes than clay pots and 19% fewer mosquitoes than CDC light traps.
ICEMR researchers also evaluated the human-odor baited CDC light trap (HBLT) and the human-baited double net/CDC light trap combination (HDNT) for outdoor host-seeking malaria vector surveillance. The HBLT consists of a CDC light trap baited with human-odor pumped from an ordinary sleeping room. HDNT is a variant of the previously designed double net trap with an integrated CDC light trap; mosquitoes attracted to the human-bait are collected by setting a CDC light trap between the two nets. These two trapping methods used human odor as an attractant, but they are exposure-free tools since the lured mosquitoes are captured by the CDC light trap rather than by the person acting as a bait and as a collector. In the ICEMR study sites, HBLT captured 2-3 times as many malaria vectors as the regular CDC light trap. HDNT caught 6 times as many malaria vectors as the CDC light trap, similar to the number of mosquitoes collected by the traditional human landing catch method.
These new alternative mosquito surveillance tools could be safer and effective complementary tools for outdoor resting and host-seeking malaria vector surveillance. For example, compared to the most commonly used CDC light trap method, sticky pots can be scaled up as an outdoor malaria vector surveillance method at a fraction of the cost of CDC light traps. Because mosquito collection using HDNT and HBLT does not expose human collectors to mosquito bites but requires more expensive CDC light traps, they can be used for malaria vector surveillance in sentinel sites.
In the past decade, sub-Saharan African countries have experienced a new era of large dam constructions and expansion of irrigated agricultural farms to resolve famine and food shortage. These environmental changes may have unforeseen ecologic consequences that adversely affect human health. Knowledge gained from this ICEMR is important to malaria control, not only for the two study countries studied, but also to other regions of Africa prone to drought, famine, and large scale human population movement.
View Associated sites for the Sub-Saharan Africa ICEMR in a larger map.
Map description: Associated sites in Ethiopia (Gambella Rice Irrigation area, Ajro Dam site, Jimma Zone) and Kenya (Chulaimbo site, Kendu Bay)
Principal Investigator: Guiyun Yan, Ph.D.
- Guiyun Yan, University of California, Irvine
- Ming-Chieh Lee, University of California, Irvine
- James Kazura, Case Western Reserve University, Cleveland
- Delenasaw Yawhalaw, Jimma University, Ethiopia
- Jimma University, Jimma, Ethiopia
- Addis Ababa University, Addis Ababa, Ethiopia
- Kenya Medical Research Institute, Kismu, Kenya
- Maseno University, Kisumu, Kenya
- University of Nairobi, Nairobi, Kenya
- Burnet Institute, Melbourne, Australia
- Case Western Reserve University, Cleveland